Marine diversity

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY Edited by

J.M. Gili, J.L. Pretus and T.T. Packard

Scientia Marina, 65 (Suppl. 2) Institut de Ciències del Mar, CMIMA-CSIC Barcelona, Spain

This volume was printed with the support of:

Consejo Superior de Investigaciones Científicas

U UNIVERSITAT DE BARCELONA

CSIC

CMIMA INSTITUT DE CIÈNCIES DEL MAR

B

FOREWORD Summer programmes are today a normal university activity, particularly in southern Europe. After an academic year, stressful to both faculty and students, the summer programmes, held in clement climates, in remote places, and in a more leisurely academic pace, are free from the strict intellectual confines imposed by classrooms and curricula and are more conducive to freedom of expression and speech. Thus, setting and human inputs combine to make summer courses ideal for the free-flowing, genuinely unimpeded exchange of ideas and concepts between generations. The Universitat Internacional de Menorca Illa del Rey [UIMIR] (Menorca Illa del Rey International University) programme stands out as special among the events held in university settings in the Mediterranean area in summertime. It brings together the faculties of three universities of Catalan speech, the Universitat de Barcelona [University of Barcelona], the Universitat de les Illes Balears [University of the Balearic Islands], and the Universitat de Castelló [University of Castelló], providing them a forum to discuss mutual concerns and ideas. The UIMIR thus offers an ideal setting for the practice of fast-paced, open scientific exchange, which plays an ever more important role in our culture. Faculty members from a broad range of public and private academic institutions and research institutes attend it without constraints or restrictions. The idea for this year's meeting came into being at the summer courses held in 1997. For a week Dr. Ramón Margalef from the University of Barcelona was the great professor we have all yearned for. The courses were an opportunity for deft and seemingly effortless transmission of his teachings between the youngest and the most veteran participants. A few of us were privileged to enjoy that week at our leisure, revelling in Dr. Margalef’s boundless amiability in communicating his ideas and in the shared daily experience of living and working together in such a special setting. There was a wonderful feeling of being free to listen, assimilate, and express oneself. Dr. Margalef’s lectures took us back to the basics of what science should be, a branch of human endeavour that truly helps us to understand our own natures and surroundings. Feelings of freedom and objective thought pervaded that week, and we have been working for two years now in the hopes of rekindling a similar experience for a week in September 2001. In the summer of 1987 a group of us organized the European Marine Biology Symposium (EMBS) in Barcelona. We still hold fond memories of that event, and we thought that if we were going to make the renewed effort of organizing it again, it was only fitting to do so in exceptional circumstances. We have now been able to find the proper setting, to arrange a singular event at summer’s end in Europe, at a truly congenial venue committed to the ideals of freedom and enthusiastically receptive to scientific endeavour. Still, we should not overlook the reality of science today. This modest contribution of ours, intended to make the dissemination of knowledge more humane and objective, requires us to stop and come to the realization that there is much to be done. For instance, meetings like the one we are organizing here are frequently undertaken with good intentions yet even so often become so commercial or top-heavy with bureaucracy that we do not rightly know if we attend them out of routine or because we truly aspire to learn new things. Large meetings are indeed a place for colleagues and specialists to come together, but wouldn’t workshops be more appropriate for such encounters? Meetings are a reflection of the path science has taken in recent decades. There is today a huge rift between those interested in applied science and those interested in basic science. Applied science is heavily supported by the public administrations and by private enterprise, primarily interested in funding work likely to yield short-term profits. This short-sighted state of affairs overlooks a basic fact, namely, that the greatest scientific advances for the human race have been grounded in contributions made by basic theoretical science and which only later have found applied outlets or have been able to set the stage for additional research that has yielded commercial products or contributed to the general welfare. We are not so much concerned here with the need to promote both these areas of

research as we are with the conditioning factors that cause one to garner much more support than the other. Opening science up to commercial interests is curtailing the freedom to do research. Yet that very freedom is essential to allow the formation of new ideas, and there is an element of risk inherent in daring to undertake something new. Large scientific meetings, with a multiplicity of sessions all running simultaneously and short presentations, serving as a platform where a wide range of bodies and companies can peddle their wares, are a reflection of the red tape that is gaining ground today. It is not only meetings but also scientific journals, committees of experts, and the like actively contributing to science that have lost some of the striving inquisitiveness and imagination of years past, when discoveries and theories were accepted and debated for what they were, not as a return on competition, a competition that has overtaken all aspects of our economic and commercial system. We scientists have grown used to meeting to discuss what we can do or what others should do. In a society of rapid communication where e-mails bring instant contact, we spend days and weeks in travel for purposes of discussion. Does the cost of such discussion sessions really inure to the benefit of research? Would it not be better to invest in research projects that would be to everyone’s benefit, not just to that of the most powerful countries? We too live at the frantic pace and suffer the stress of today’s society. Researchers are subject to unending and permanent re-evaluation, and to stay in place we have to publish whatever we can, wherever we can. The journals take full advantage of this, and publishers profit from our work by making us pay exorbitant prices to publish our findings. An outcome of this frenzied need to publish, to mention just one aspect, is that there is now little time available in which to read the literature. Many researchers new to the scene barely read papers published five years before their own work. This intolerable ignorance of scientific culture greatly diminishes the prospects for successful research, and in many cases we are reinventing what was already invented earlier or we are rephrasing in new wording what others before us have already written. Yet improving the situation is an extremely complicated task. Perhaps through modest efforts such as those of the present meeting the new generations will be able to change the present system for doing science to calm the pace while at the same time making it more creative and exciting. Does a science weighed down with bureaucrats and administrative oversight and subordinate to excessive interest in commercial applications really have a bright future? Frankly, we think not, and in fact all that is left to us is to try to stake out a small territory of our own in which we can endeavour to continue to create in freedom without any pressures other than those strictly intrinsic to our profession. The intent of this book you are holding in your hands is to try to help you take the experiences shared during our time together in Menorca with you on your trip back home. We also hope that the message of our meeting will not quickly recede into forgetfulness, or at least that you will have a few moments in your busy daily schedules to recall that experience is one of the cornerstones of science and that the ideas put forward by "elder" generations may be of much more help to us than we have hitherto suspected. Perhaps now is the right time to remember a sentence by an older professor close to our hearts, who has said that “the best idea to work on in this new century that is just beginning may be one that is to be found in a book written at the start of the last century”. With all due respect to the huge technical advances that have been made in recent years and their vast contribution to scientific progress, we think that there is much truth in what he says. And because our message is one of freedom of ideas and of action, we do not want to dwell on our ideas other than to allow them free rein. THE EDITORS

SCI. MAR., 65 (Suppl. 2): 5-30

SCIENTIA MARINA

2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

Emergence in pelagic communities* C.S. REYNOLDS NERC Centre for Ecology and Hydrology, The Ferry House, GB-LA22 0LP AMBLESIDE, Cumbria, UK. Fax: +44 1 539 446 914. E:mail: [email protected]

SUMMARY: Pelagic systems, those based on the open waters of large lakes and seas, provide excellent opportunities for ecological study. This is because, the vastness of the oceans apart, pelagic ecosystems operate on short space and time scales. This affords important opportunities to study the emergence of ecosystems and the basis of striking high-order patterns of ecosystem behaviour. The essay seeks an outline of the processes by which the biologies of individual organisms the largest functional, controlled units in the ecosystem - interact and bias the outcomes in favour of particular network structures recognised by ecologists. Populations build, communities assemble, ecosystems function but always in ways that relate to the match between the adaptations and performances of individual species and the capacities of the environments in which they find themselves. The paper attempts to discern the linkages between the biology of individual and the ways that ecosystems are put together, between organisms and organisation. Drawing on the advantages of absolutely short generation times among the producers, consumers and heterotrophs of the pelagic, I seek to sample the ascendant pathways of ecosystem synthesis, noting the energetic decisions which select for particular outcomes. However, the simple organisational state of many pelagic communities reminds us that ascendancy is frequently restrained by a scarcity of resources and tempered by the frequent intervention of abiotic factors. The presentation does not seek to prove any point about systems: it attempts to reaffirm what is known about organisational hierarchies; then, using approximate quantities, the points of bifurcation between alternative organisational structures are nominated; drawing upon suppositions about the dissipation of energy, the organisational underpinning of function at the level of the whole ecosystem is proposed. Corroboration from observations from the real world is sought throughout. Key words: community organisation, assembly rules, pelagic, phytoplankton, zooplankton, bacterioplankton, energy thresholds.

INTRODUCTION: FROM PELAGIC ORGANISMS TO PELAGIC ORGANISATION Like the other papers presented at the 36th European Marine Biological Symposium (held in Maó, Minorca, Balearic Islands, 17-22 September 2001), mine is intended as a tribute to the shining example and monumental inspiration that the work of Dr Ramón Margalef bequeaths to us. Of the many specific reasons for celebrating his scientific career, I select two above all others. One is his pursuit of robust ecological theory: as his ECI Prize Publica*Received December 8, 2000. Accepted January 9, 2001.

tion (Margalef, 1997) makes abundantly clear, a grasp is required, urgently and correctly, of the mechanisms by which the Earth’s ecosystems regulate themselves. Without this knowledge, we are failing to anticipate the impact of our own over-populous, aspirant, manipulative, destructive species on the resilience of the world’s ecosystems. Without an understanding of their regulatory mechanisms or the consequences of their exceedence, how can we hope to determine what is necessary for us to recover a genuinely, ecologically sustainable tenancy in the biosphere? The second reason is the linkage between the lucidity of Margalef’s theories and his own deep EMERGENCE IN THE PELAGIC 5

understanding of pelagic systems. This is far from having been a unique combination –one immediately recalls the careers of other famous ecological theorists like G.E.Hutchinson, the Odums and David Tilman– but it conforms to a belief of mine that aquatic systems make inspiring subjects for ecological study. The supposition consolidates the valid claim that, aside from the vastness of the oceans themselves, aquatic ecosystems function on sufficiently short spatial and temporal scales for their high-order workings to be amenable to observation and meaningful experiment (Reynolds, 1998a). All that is needed is an acceptance of the analogies and of the basis for their interpretation and quantification. This being so, the first priority is to establish vertical connectivities –the nature of the linkages among the behaviours of individuals and the structures evident at the level of ecosystems and biomes. Some species-specific autecologies of aquatic organisms are relatively well-known, often with a clear understanding of their population dynamics and the features of the environments which most influence them. Good examples include fish (Elliott, 1994), invertebrates (such as the “keystone” water fleas of the genus Daphnia: Haney, 1985) and some planktic autotrophs (a fine case is the biology of Cylindrospermopsis: see Padisák, 1997). At the other end of this spectrum are some recent concepts explaining how ecosystems are organised and regulated (see, e.g., Strasˇ kraba et al., 1999, and other papers in the same series). Such contributions add value to the developing sub-discipline of macroecology (Brown and Maurer, 1989; Brown, 1999) which identifies within the large-scale statistical patterns of species distribution, abundance and richness of species, the processes governing the structure and dynamics of complex ecological systems. Exciting as macroecology has become, some ecologists remain uncomfortable with a deductive but practically untestable model that pitches itself above the real-world complexitities of variable population dynamics and other small-scale assembly processes in fluctuating communities. Crucially, however, macroecological approaches to questions about the operation of the intermediate organisational level –that of the local assemblage of species and its structural regulation– seem to promise legitimate and verifiable insights into the ways that the ecologies of individual species slot together into recognisable, functionally viable ecological communities (Lawton, 1999). The broad challenge accepted here is to develop an overview on how pelagic communi6 C.S. REYNOLDS

ties (those of the open water of large lakes and the sea) are assembled. Thus, the specific aim of this essay is to contribute towards the eventual synthesis of a “rule book” of ecosystem organisation and function. The sequence of ideas to be developed is founded on a “bottom-up” view of biotic sequestration of raw materials by constituent autotrophs and the energetic potential that is harvested from sunlight. The adaptations of individual species of autotrophs and the respective fitness features these impart in the face of intensifying environmental constraints are argued to influence strongly both the directionality of autogenic succession and the responses to allogenic environmental forcing. The analogous behaviour of the phagotrophs and other microbial consumers of primary products are treated in a lesser detail, sufficient only to characterise the interactions among the community’s producers and consumers of organic carbon. The relevance of carbon intensity to the structure of distinctive pelagic communities is considered towards the end of the essay. These are large areas of ecology. It is desirable to adopt some overall framework into which to interface concepts from ecosystem theory with knowledge of the specific adaptations and autecologies of individual species and functional groups. The model I have adopted to provide that framework is an adaptation of the species exergy plots of Nielsen (1992).

EMERGENCE AND EXERGY An earlier draft of this paper was titled “The selforganisation of pelagic communities”. It was changed to the present one because any implication that the striking robust and consistent patterns evident in system development conform to some supraorganismic control is a source of deep concern among practising ecologists. One does not have to go as far as adopting a Gaian interpretation of the biosphere (Lovelock, 1979) before the supposition of some internal design to assembling ecosystems is implicated. The use of terms such as “goal function” (Strasˇ kraba, 1980) or, indeed, “self-organisation” (Pahl-Wostl, 1995) to describe the development of complex, networked communities of interrelated producers and consumers risks the misattribution of a system property to some systemic driver. The high-order patterns in pelagic communities are clear enough, with well-rehearsed attributes and processes (see Reynolds et al., 2000) which are not in dis-

pute. However, it has to be rigourously emphasised that the patterns are exclusively contingent on the behaviours and mutual interactions among the biotic components of the ecosystem, that is, the individual organisms making up the specific populations and the putative multi-species communities. The ecosystem is the sum of the component processes carried out by the aggregate of constituent individuals. Organisms, indeed, are the largest self-regulating units of assembly with any kind of controlling, reproducible set of genomic instructions. In the delightful phrase of Lampert and Sommer (1997), we need look “no further [..for system properties..] than the activities of individual organisms”. This being so, self-organisation is a collective outcome (or “emergent property”) of the aggregate of the independent dynamic responses of individual organisms to the external environmental conditions obtaining. These act as a kind of filter, admitting the growth of tolerant individuals of suitably pre-adapted species while excluding those that are poorly suited. Changing environments may result in changing filters which lead towards alternative outcomes, when the identities of the best-fit of the species available may also be varied (Harris, 1986). How such small-scale responses and interactions of individuals become aggregated and assembled into recurrent, emergent, high-order structures provides the central theme of this essay. To build this around a thermodynamic model permits an approach to community assembly that relates primarily to the fulfilment of functions rather than to the explanation of any particular assemblage. A starting assumption is made that ecosystems do not necessarily comprise the species that happen to be the best adapted to the particular habitat. A preferable analogy is the creation of a series of vacant employment opportunities, each waiting to be filled by able applicants. Changing conditions of employment might determine that only the fittest or most dogged of the applicants will survive. Yet, here again, we must reject at once any implication that such opportunities arise other than as a consequence of the infrastructural requirements for efficient organismic processing of the resources available: there is no central “employment policy”. In this sense, emergent ecosystems have much in common with modern market-driven macroeconomies. Founded on a sound base of natural resources, economies expand through the application of labour and the accumulation of controvertible wealth. Wealth accumulation permits diversification as primary products are

exchanged for secondary manufactures and goods are exchanged for services. Each activity requires specialist personnel and each is supported by the primary resource. The balance of opportunities depends upon the resource availability, the rate of its processing through the economy and the burden of non-primary activities that can be borne. Given an adequate resource base of nutrients (=K), ecosystems harvest primary energy (E) to sustain production (P) and to accumulate biomass (B). Trading in organic carbon as currency (Corg), primary products support the secondary production of phagotrophic animals and heterotrophic organisms, within the supply limits that the primary (“wealth”) generation can fufil. At the systemic level, expansion proceeds as a function of the capacity of the flux of organic carbon ({Corg}’), the concentration base of other elements or nutrients involved ([K]’), and the integral of harvestable energy flux ({E}*). Thus, assembly may be summarised: A = f ({Corg}’, [K]’, {E}*)

(1)

It is well understood that whereas energy can be stored chemically, its ability to support work is not. Ecosystems run almost exclusively on the shortwavelength solar flux, which is harvested and invested in high-energy carbon bonds through the remarkably conserved process of photosynthesis. Provided the supply of nutrients, water and inorganic carbon are each adequate to match the potential rate of fixation, primary production yields around 1 kg of carbohydrate per 15 MJ of energy captured (roughly 470 kJ invested per mol Corg fixed). Some of this carbohydrate is re-activated in growth, which draws on the store of Corg in the synthesis of proteins and new cell mass, and will provide the energy to drive the actual building process. All intracellular energy-consuming processes require the controlled oxidation of the organic carbon bonds, which is effected in the synthesis of ATP. This is another process that is highly-conserved among all living organisms, everywhere resulting in an irretrievable loss of energy as heat. Primary-producer biomass may eventually become the carbon substrate of a heterotrophic decomposer or the carbon intake of a phagotrophic consumer. In either case, oxidation of the organic carbon content provides the raw material of the growth and reproduction of the consumer, as well as providing it with the energy to use in the assembly of its biomass and in the (usually) significant effort required to forage for more organic carEMERGENCE IN THE PELAGIC 7

bon. So it is at each link in the food web, residual organic carbon being gradually oxidised away as it is processed through the prey-predator network. At each point, there are decomposer organisms working on the generated wastes or on the corpses and cadavers of expired organismic components and which, thus, eke out the last of the unoxidised carbon to supply their needs. Ecosystems are simply networks for dissipating energy. The above model illustrates the linkage of macroecological processes to the molecular chemistry of carbon reduction and oxidation, embracing the notions of community structure and function in terms of thermodynamic exchanges. The quantities of energy that are eventually dissipated, either per unit time or per unit area, are influenced by numerous factors, not the least being the rate at which short-wave radiation is captured and transferred to store. Just as the growth of organisms requires an income of energy that, on balance, exceeds the outgoing losses, so assembling communities represent an accumulating wealth of organic carbon as energy income exceeds expenditure. In this respect, ecosystems appear to contravene basic laws of thermodynamics governing the entropic degradation of energy and matter towards the ultimate equilibrium state. Of course, ecosystems are fully open, dissipative systems (Jørgensen, 1992) that operate, like waterwheels in a stream, by exploiting the dissipative flux. More of the flux can be exploited by building more harvesting biomass (more or bigger water wheels) but the capacity of the flux itself cannot be enhanced (the same amount of water runs through the millstream). A positive balance of energy harvest over the rate of its biotic dissipation may be referred to as exergy (Mejer and Jørgensen, 1979). Sometimes termed “negative entropy”, or “negentopy”, it is a thermodynamic measure of the information content of the system. The state of living systems may be characterised by the level of molecular organisation and information represented by their useful gene content (Jørgensen et al., 1995, Jørgensen, 1999). However, it is simpler to adopt the alternative approach of Nielsen (1992) which has the energetic exchanges as its base. Thus, Reynolds (1997a) calculated the exergy-generation capacity of phytoplankton, as a function of radiant energy income and the energetic costs of respiration and maintenance of the alga Chlorella. The model, reproduced in simplified form as Figure 1, supposes a maximum flux of photosynthetically available radiation of 60 mol photons 8 C.S. REYNOLDS

FIG. 1. – The Nielsen-Jørgensen representation of the potential exergy of a system, as the excess energy harvesting capacity relative to the biomass maintenance costs. The quantification is based on the physiology of the alga Chlorella (Reynolds 1997b).

m-2 d-1 (~ 12.6 MJ m-2 d-1 of photosynthetically available radiation, or PAR) and interpolates the interception of photons up to the areal density of lightharvesting centres that could be simultaneously activated at 20oC (the upper curve, expressed as the equivalent standing-crop carbon). The cost of standing-crop maintenance is calculated as a direct linear function of the basal respiration rate of Chlorella. The maximum theoretically sustainable standing crop is that at the point of intersection. The solution given -10.4 mol cell C m-2 (≈125 g C m-2 or, roughly, 2.5 g chl a m-2), compares well to reported natural maximal densities of phytoplankton (~50 g C m-2) and active terrestrial plant biomass (~75 g C m-2: see Margalef, 1997). It is a good deal less than the 2030 kg C m-2 standing crops of forests, though this is, of course, dominated by the accumulated necromass that is wood. The bow-shaped area enclosed between the energy-harvesting capacity and the maintenance costs of the autotrophic biomass represents the potential compartmental exergy flux. It is a measure of the system’s ability to invest in new producer biomass, as represented in eqn (1), and to support the transfer of Corg to other levels in the trophic network. The bow also represents the buffering capacity of the system compartment, which enables it to withstand a variable solar energy income as well as consumer-

FIG. 2. – Assembly of producer biomass (continuous bold line) in relation to the ability of a fluctuating energy income (thin line) to sustain the mainteance requirements of the biomass. A similar relationship exists between the biomass of consumers and the ability of the food resource to meet its maintenance costs. Based on Figure 65 of Reynolds (1997b).

forced variations in the active biomass present (Mejer and Jørgensen, 1979; see also Fig. 2). So long as the net exchanges are positive, the existing structure has a “cushion” of exergy within which its biomass and its further development are wholly sustainable (Reynolds, 1997a). The economic analogy of exergy is a budgetary surplus that is available to support new growth or to fund the diversification of socially valuable but fundamentally non-productive service activities.

PELAGIC CONSTRAINTS AND THE HABITAT TEMPLATE From the foundation that emergence is dependent upon a positive compartmental exergy flux, the task is to determine the mechanisms of growth and selection that influence the identity and function of the key players. In order to do this, however, it is necessary to first consider the nature and scale of the formidable constraints and conditions that pelagic environments pose to their exploitation by organisms and putative systems. These are suggested to act like a series of “filters”, of differing coarseness, that select candidate species on physical, functional and metabolic criteria. The “physical constraints” refer to the generic properties of water and of its motion, as it is moved by gravity, atmospheric forcing and gyratory inertia, from one state to another or from one place to another. In a fluid which is simultaneously non-compressible, relatively dense and viscous, mechanical kinetic energy is dissipated through a spectrum of turbu-

lent eddies, the smallest being eventually overwhelmed by the viscosity. The generation and dissipation of turbulent kinetic energy in lakes and seas, relevant to their biology, were quantified successfully over a decade ago (see e.g., Denman and Gargett, 1983; Spigel and Imberger, 1987) and their importance to pelagic ecosystems was quickly diagnosed (Mann and Lazier, 1991; Reynolds, 1994; Catalan, 1999). Contention with the combination of turbulence and the Archimedean properties of water makes rigidity a lower adaptive priority than tensile strength or the ability to escape turbulent shear by exploiting the viscous end of the eddy spectrum (Reynolds, 1998b). It is no coincidence that the dominant life forms of pelagic primary producers should be almost exclusively pico-, nano- or microplanktonic (i.e., < 0.2 mm; the few exceptions occupy rather specialised niches) and that they share this viscous world with most heterotrophs (bacterioplankton) and many species of phagotrophs (microzooplanktonic protists and rotiferans). Mesoplanktonic feeders (0.2-2 mm) that exploit turbulence in their foraging (Rothschild and Osborn, 1988) are built very differently to withstand shear. For larger pelagic foragers, the principal force countering progression through the water is frictional drag, to which end, the simultaneous investment in powerful musculature, streamlined body form and smooth surface is a long-appreciated adaptation, not just of pelagic fish but among other large animals too (Bainbridge, 1961). The “functional level” invokes the major segregations in pelagic-role fulfilment, with respect to the movement of organic carbon. The essential distinctions are, clearly, among those organisms engaged in its synthesis into primary biomass and those which consume it as a delivered product. It may seem trite to be differentiating plants from animals at this point in the essay but this is an appropriate juncture at which to point out that the interactive, trophic relationships struck among the producer and consumer components –the food web– is generally recognised to represent one of the most important filters in structuring pelagic communities (Carpenter et al., 1985; McQueen et al., 1986), as it is elsewhere (Oksanen et al., 1981). Clearly the interactions go beyond the sequence, carnivore eats herbivore eats plant: in a three dimensional environment, the means of foraging and the accessibility of resources need to be reconciled. Food availability and consumer ontogeny and electivity are prevalent in pelagic food webs (Pahl-Wostl, 1990). The imporEMERGENCE IN THE PELAGIC 9

tant trophic relationships in the pelagic are just as much networks as they are on the land. The components of a Planktothrix-Chironomid-Cyprinid food chain are no more interchangeable with those of a microbially-mediated picoplankton-calanoid-salmonid network than are those of a shrub-aphid-coccinellid sequence with those of a grass-zebra-lion linkage. Functional groups of every trophic level have to match the foraging opportunities of the habitat and trophic networks inevitably reflect these. The “metabolic level” is the finest level of filtration, yet it is possibly the one requiring the greatest flexibility of paradigms held hitherto to explain species selection. In fact, the same principle holds as for the two higher levels, that every species will grow in suitable environments (its spectrum of requirements is satisfied) provided it has the opportunity to do so (a viable inoculum is present). The prominent species are not necessarily the best fitted and, while the opportunity is presented, any of a number of species may increase simultaneously and while individual demands are fully supplied by the collective resources, they are not strictly competitors (Reynolds, 1984a). This is different from the view, implicit in Tilman’s (1977) resource-ratio hypothesis, that the species whose optimum requirements match most closely the conditions obtaining will “outcompete” all others in contention. However, once the supply of one or other of the resources fails to satisfy all the demands of co-habiting species, then there is a competition for limiting resource, and for which superior uptake affinities or alternative uptake strategies will single out the fittest competitors. Demonstrable limitation of performance is the essential prelude to competition, when the selectivity of the filtration is tightened against less welladapted contenders. The difference between the two ideas is narrow and nearly semantic. The principal distinction of the filtration concept is that it allows more species to function in benign environments. This is important to understanding how species that are not equally competitive nevertheless co-exist and, indeed, how a high diversity of potentially redundant species can be maintained. Moreover, the modern view of habitat filtration has much in common with the biocoenotic hypotheses advanced by Thienemann (1918) and others in the early part of the twentieth century (for a convenient summary of which, see Lampert and Sommer, 1997). They recognised the association of low species diversity with “harsh conditions” (i.e, tolerable to relatively few species) but 10 C.S. REYNOLDS

greater numbers of species (albeit, many of them represented by small numbers of individuals) in varied environments permitting many species to approach their optimal performances. The idea that communities might comprise not merely the best-fitted species but that they are, rather, near-random assemblages of all but the nonfitted species, is now strongly advocated by, inter alia, Keddy (1992: see also Weiher and Keddy, 1995), who was motivated by work on wetland plants, by Kelt et al. (1995), working with small mammals, Belyea and Lancaster (1999), inspired by stream fauna, and Rojo et al. (2000) analysing phytoplankton assemblages. Belyea and Lancaster (1999) offer a clear definition of what constitutes an “assembly rule” and discuss which of the rules hitherto proposed might have most relevance to emergence. They accept that many factors shape observable communities but that the internal dynamics are the most influential factors in community building, within constraints imposed by the local environment and the pool of species available. The deductions also bring an exciting complement to the approach to habitat classification, pioneered by Southwood (1977) and Grime (1979). Their templates of available environment anticipate the delimitation of habitat range occupied by species with the appropriate adaptive specialisms. Once again, students of the phytoplankton have not been far removed from these approaches, which find evident analogies in Margalef’s delimitation of evolutionary adaptations (life-forms: Margalef, 1978) and habitat representations (the “mandala” of Margalef et al., 1979). My own attempts to discriminate common behaviours among the phytoplankton and match them, on the one hand, to morphological properties and, on the other, to environmental gradients (Reynolds, 1980, 1984a, 1987) are coincidentally allied. These attempted to convey the profound and potentially selective constraints on the growth and development of phytoplankton imposed by the extreme dilution of nutrient resources in open waters and the impact of light absorption through in deep mixed layers. The first characterisations of habitats were set against axes representing “nutrient availability” (y) and “mixed depth” (x). To emphasise the analogy with Grime’s (1979) work, these were considered pelagic equivalents of (respectively) “stress” and “disturbance”. More recently, they have been quantified in terms of the accessibility of the critical resource (K**, being the

areal concentration of the limiting nutrient, which can be phosphorus, nitrogen, iron or other micronutrient, divided by the product of the depth and the concentration gradient from top to bottom (One is added to the gradient to avoid zero denominators; the units cancel to m) and harvestable processing energy (I**, being the geometric mean daily photon flux divided by the depth of the mixed layer; units: mol photons m-3 d-1). A wide variety of phytoplankton has been fitted to this template (Reynolds, 1997b, 1999a). Most recently, the template has been extended to represent a wider range of pelagic habitats, defined by axes describing “resource constraints” and “processing constraints” (Reynolds, 1999b). This widens the conceptual representation to embrace the food resources of the consumer trophic levels and the oxidative potential which is required for organically stored energy content to be realised. The extended template established “domains” separated by the agent most likely to regulate the metabolism of the system. In this way, the constraint of functioning of the whole system is interpretable, not just as a prob-

lem of nutrient supply but also of energy input, of carbon sourcing and whether the system redox inhibits the cycling of primary products. This habitat template is invoked (see Fig. 3a) here to illustrate the patterns of constraint filtration, primarily as they apply to phytoplankton. To move rightwards, in the x direction, continues to represent the increasing severity of the processing constraints, or, in this instance, diminishing access to photochemical energy; this makes adequate photosynthetic productivity progressively more difficult to achieve. Moving in the y direction from the bottom left-hand corner follows a gradient of alleviating severity of traditional nutrient limitation, to a point where the supply of nitrogen, phosphorus and all the other nutrients is able to sustain a rate of biomass synthesis which consumes carbon dioxide at a rate which exceeds the rate invasion into the water across the surface (it has been calculated that this route can supply no more than 90-100 g C m-2 y-1: Reynolds, 1999b). Even that rate depends upon the maintenance of a steep solution gradient. Smaller water bodies, in which the direct invasive pathway is

FIG. 3. – Development of a habitat template for phytoplankton. The left hand shape is based on the matrix of limnetic metabolic sensitivities (Reynolds, 1999b) in terms of carbon resource (vertical axis) and the rate of its processing (horizontal axis). Starting at a point half way up the left-hand axis, it is supposed that the supply of carbon and nutrients will saturate the fastest rate of carbon fixation. In the downwards direction, nutrient resource availability constrains the biomass assembly; rightwards, the system becomes limited by photosynthesis; upwards, carbon dioxide is the most serious constraint; if the system is relieved by an alternative supply of fixed carbon, processing rates are often constrained by oxidative potential. Quantifying in terms of carbon, phosphorus availability and the harvestable photon flux, the physiological ranges of plankton algae can be represented (the middle shape). Each of the three shown is particularly well-adapted to contend with deficiencies in the supply of one of the requirements. At optimal supply rates, all three species perform to the best of their abilities. The right hand shape is identical to the centre one but now serves as a habitat template that is populated by functional species associations. These are identified by the alphanumeric coda developed by Reynolds (1997b).

EMERGENCE IN THE PELAGIC 11

matched or exceeded by carbon dioxide dissolved in the inflowing water, or is enhanced by the release of gas through the photolysis dissolved organic matter (Maberly, 1996; Thomas, 1997; Whitehead et al., 2000), are represented towards the top of the template, as are the effects of an organic input that exceeds the capacity for its re-oxidation. The template is an aid to recognition of the constraints obtaining in a habitat and provides an index to the intensity of selective filtration operating and of its sensitvity to variation. Moreover, from co-ordinates representing a starting position, the impact of emergent assembly on the habitat might also be tracked. To improve its usefulness in this context, the template can be further tuned to the specific site sensitivities, which, for many freshwater habitats, may reduce to the supply of bioavailable phosphorus, the maximum flux of inorganic carbon and the harvestable light flux in the mixed layer. This rationale is followed in the construction of Figure 3b. The revised template accommodates the maximum photon flux ({E}* ~ 60 mol m-2 d-1) and a range of carbon dioxide concentrations influenced by the solution flux to open water systems ({C}). Capacity limitation by the supply of phosphorus (it could just as easily have been nitrogen or any other nutrient) is inserted on the carbon axis in the appropriate stoichiometric equivalence (1 mol P : 106 mol C). To move downwards from this point is to imply increasing risk of phosphorus deficiency; to move upwards increases the system dependence on external supplies of inorganic or organic carbon. To move rightwards implies the increasing limitation by light energy. The perimeter of Figure 3b can be taken to represent the totality of planktic habitats (at least, with respect to these three dimensions) and to cover all eventualities from relative plenty to relative famine. The plot is then amenable to the insertion of the operational ranges and tolerances of particular species. Where the species plot embraces the habitat co-ordinates, it may be deemed to be filterable and, thus, its growth is tolerant of the environmental conditions obtaining. Outside these bounds, the organism is unable to grow. To show the principle, three filter boxes are inserted in Figure 3b. The range for Microcystis reflects its shortcomings as a light antenna and of its relatively weak affinity for phosphorus at low concentrations. However, Microcystis is one of the Cyanobacteria known to contend with high pH levels and micromolar concentrations of carbon dioxide (Moss, 1973; Talling, 1976), which ability is 12 C.S. REYNOLDS

now known to be attributable to a very sophisticated carbon-concentrating and transport mechanism (Kaplan et al., 1980; Miller et al., 1991; Espie et al., 1991). The range of Microcystis penetrates deeply into the low-CO2 regions of Figure 3b. By analogy, some of the solitary, filamentous forms, like Planktothrix agardhii, are not just demonstrably good light interceptors (Kirk, 1976; Reynolds, 1989) but they have great flexibility in the amount of photosynthetic pigment they contain and, in some species and subspecies, in the amounts of accessory pigments too (Tandeau de Marsac, 1977). The experimental results of Post et al. (1985) provide the data to construct the range of P. agardhii inserted in Figure 3b. The represented tolerance of low phosphorus environments by Synura is not due just to the alga’s high affinity for phosphorus (data of Saxby-Rouen et al., 1997) but to its capacity to live phagotrophically on bacteria (Riemann et al., 1995). It should be said that the capability does not provide a complete explanation (at 10-9 mol l-1, how do the bacteria take up sufficient phosphorus?). In the small, vegetal pools in which Synura thrives, however, sources of terrestrially-formed organic debris are generally disproportionately plentiful. Just to emphasise the point, it is rehearsed again that Synura cannot even use bicarbonate, Microcystis is a very poor light antenna (Reynolds, 1989) and Planktothrix is, relatively, a phosphatophil. For each of the specialisms, one of the organisms is superbly well-adapted but it turns out to be a poor competitor in the other domains. Thus, totality of habitats is subdivided into subsections in which the environment sets up functional funnels or “filters”. The “filtration” is entirely analogous to classical set theory wherein subsets of datapoints (= organisms) may be grouped together but separated from others by the inserted boundaries. The filter is analogous to the Venn diagram of classical set theory and which is passed only by species with appropriate adaptations and which, of course, happen also to be present. The first rule of emergent assemblages is that the component species must be available in substantial numbers (“viable inocula”) and that the habitat conditions obtaining must be adequate to sustain their minimal requirements for net biomass increase. Even without good quantitative data for any but a handful of other species, experience with designing other templates and accommodating named species conforming to one or other of the (alphanumeric) functional classifications (see above and Reynolds,

1997b) permits their distribution in the new template to be plotted provisionally (Fig. 3c). This version of the template is included to assist the next task, which is to establish the properties of individuals of the various species of phytoplankton which contribute to the emergence of the functional guilds of species upon which community structures are founded.

POPULATION GROWTH AND COMMUNITY ASCENDANCY An important feature of the habitat template is that the ranges of species overlap in a domain which represents a general adequacy of resources and processing energy, wherein almost all species can operate without stretching their specialist adaptations. The converse is that, in such benign environments, just about everything else is capable of attaining its its maximal performance too. Nevertheless, these are appropriate co-ordinates at which to observe the mechanisms of emergence. With metabolic filtration at its least exacting, it is predictable that the most successful organisms, of a pool populated by many potential contenders, will be those that furnish the largest inocula (N0) or those that achieve the fastest rates of assembly (r). The connotation, “r-selection” (McArthur and Wilson, 1967), is transparent in the logistic growth Equation (2): N t = N0 e r t

(2)

where e is the base of natural logarithms and t is a period of time through which r holds. The appropriate strategic adaptation under such circumstances is invasiveness, with the ability to invest in propagule production and the capacity to achieve short generation times distinctive attributes. Invasiveness is synonymous with the competitive C strategy in Grime’s (1979) vegetation theory. Usage of the terms, “competitive ability” and “a power to outcompete other species” is not consistent among terrestrial and plankton ecologists (the latter attribute the title to the eventual “winner” –Æsop’s tortoise, not the hare, is the better competitor). The vital recognition is the communal effect of individual species responding idiosyncratically to the growth opportunity with which they are confronted. At this point in the template, where nearly all species are able to perform well, the fastest-growing among them are likely to emerge dominant. This view of “fitness” is preferable to suppositions about “competitive” outcomes.

The fastest growing representatives of the planktonic C-strategists are the smaller, usually unicellular species, having the high surface-to-volume ratios that favour rapid assimilation and conversion of resources with minimal temperature sensitivity (Reynolds, 1997b). Difficulties persist in the determination of in-situ cell replication rates growth, being generally understood to exceed, sometimes considerably, the observable rates of population increase [r = {ln (Nt / N0 )}/t]. The latter are net of all losses befalling intact cells, including mortality, settlement and advection. On the other hand, the measurement of nutrient-uptake or photosynthetic carbon-fixation rates, provide supportive capacities: they cannot be, on average, lower than the rate of growth actually achieved but they are naturally capable of supplying the fastest attainable rates of cell growth and replication. The latter are best determined in controlled cultures in which all needs are supplied in excess, under conditions of continuous saturating light. Species-specific replication rates measured thus are reassuringly consistent. and they are now known to be reliably predictable from morphological properties of the algae (Reynolds, 1989; Reynolds and Irish, 1997). An obvious corollary is that, so long as the supply of resources (sensu lato, taken to include carbon and the harvestable photon flux) exceeds the demands of the assembling biomass, individuals will grow and populations will assemble at the fastest rates that the temperature and photoperiod will allow. These assembly rates are simulable by adequately sensitive and verifiable models (see Elliott et al., 1999a,b). They readily uphold published observations made under optimal conditions: many of the familiar small, unicellular phytoplankters are capable of doubling their mass in under 12 hours, principally as a correlative of their relatively high surface-to volume ratios. Reported resource-saturated replication rates of laboratory strains of Chlorella at 20oC are in the region of r = 1.84 d-1 (21.3 x 10-6 s-1: Reynolds, 1990), which is equivalent to a doubling of biomass every 9.05 hours. Analogising growth to carbon dynamics, doubling the mass is equivalent to fixing, assimilating and deploying 1 mol of new carbon for every 1 mol of cell carbon represented in N0. The same alga has been shown to be capable of photosynthesis that will provide this amount of reduced carbon in under 7 hours and to be able to absorb sufficient carbon dioxide at the air-water solubility equilibrium in 38 minutes (Reynolds, 1997b). Moreover, the affinity for phosphorus is such that it would require only 7 minutes at EMERGENCE IN THE PELAGIC 13

its maximal uptake rate to assimilate sufficient phosphorus to maintain the stoichiometric equivalence with carbon in the daughter cells. The solar energy required to reduce 1 mol of inorganic carbon dioxide to carbohydrate is not less than 8 mol photons (Falkowski, 1992), while there is a further energy cost attaching to protein synthesis. Empirical determinations of photoautotrophic biomass yields do not much exceed the 0.07-0.09 mol C (mol photon)-1 measured by Bannister and Weidmann (1984). Supposing that the formation of 1 mol cell C requires the capture of 13 mol photons (2.8 MJ) and that the area projected by a single Chlorella cell (diameter, ~ 4 x 10-6 m, containing about 0.6 pmol C) is 12.6 x 10-12 m2, then the solar flux required to saturate its maximum growth rate at 20oC, calculated as 7.8 x 10-12 mol photon per 12.6 x 10-12 m2 per 9.05 h, solves to about 19 µmol photon m-2 s-1 (or ~ 4 W m-2 of photosynthetically-active radiation). While these benign conditions persist, the equivalent carbon-specific resource demand will be close to 0.01 mol P and 0.16 mol N per mol new photoautotroph carbon formed. At the same time, each mol of autotroph C added also represents the addition of 0.2-0.3 g chlorophyll a pigment and a commensurate increase in the potential exergy-flux capacity of the assemblage. A positive exergy flux is essential to building autotrophic communities. Just as the most powerful sectors of the buoyant economy are those which generate the most wealth, so the species contributing most to the carbon flow through emergent communities need not be the ones with the greatest mass but those which are the most productive (sensu carbon flux per unit mass per unit time). Analyses of the early assembly stages (e.g., Rojo et al., 2000) reveal no clear patterns in terms of the identity of the main species. While the environmental filter remains coarse, however, “fitness” (as defined above) soon becomes the most important determinant of dominance. Besides Chlorella and similar unicellular chlorococcal nanoplankters, such genera as Ankyra, Chlamydomonas, the cryptophyte Rhodomonas, the haptophyte Chrysochromulina and the xanthophyte Monodus, have all been observed at times to increase in natural plankton at rates exceeding one doubling per day (Reynolds, 1984b). Some larger microplankters, including the diatom Fragilaria, whose morphology maintains a high surface area-tovolume ratio, are believed to achieve comparable rates of replication. Interestingly, the fastest rates of autotroph replication measured in the laboratory 14 C.S. REYNOLDS

(Kratz and Myers, 1955) have been on picoplanktonic species. On the other hand, the in-situ replication rates of larger microplankters and colonial algae are rather slower than Chlorella (at best, doubling every 1-5 days). Even dividing twice in the time that smaller algae divide three times results in only half the biomass, assuming initial parity. Overall, early assembly mechanisms are biassed towards species traits favouring rapid resource acquisition and conversion. The “early-successional”-stage community is characterised by processes leading to the accumulation of biomass which, in turn, delivers the means of further growth and development of the assemblage. This is, of course, a re-statement of long-held understanding the role of r-selection in early succession (Odum, 1969). Species garnering and allocating the most resource contribute most to the increase in carbon biomass, to the replication of new generations and to the communal exergy flux. Subject to the continued satisfaction of demand by the resource and processing fluxes, the cells of other, subdominant, species may behave in an analogous manner way, each building its own population and, so, contributing to the overall producer biomass, without risk of being excluded by resource competition. The more photosynthetic biomass that is built, the greater is the aggregate ability of the developing assemblage to intercept energy. The richer is the species representation the more varied is the network of energy flow and the greater is the information content. The coupling of these statements corresponds, approximately, to the principle of optimal ascendancy, as formulated by Ulanowicz (1986). The main reason for invoking it in the context of assembly rules is that it emphasises again that emergent structures rely wholly on the performances of the component organisms. It is necessary to point out, however, that it is the “fittest” of the developing populations, developing the biggest share of the total biomass, which most influence the mathematical (Shannon-type) diversity of the assemblage. Diversity may decrease even while species richness is accumulating.

SELECTIVE DIRECTIONALITY OF EMERGENCE Still concentrating on phytoplankton, this section attempts to account for emergence trends in sub-

ideal environments when resource or processing constraints are operative and a more rigourous filtration of adaptive traits applies. The constraints may be characteristic of the habitat anyway (it is chronically poor in nutrients or energy or both) or it may be imposed, autogenically, as a consequence of the impacts by the emergent community. However, the outcomes are not necessarily the same, and the pathways to their realisation may differ substantially. Common to all, however, is the selective drive of ascendant processes being biassed towards species contributing strongly to the overall exergy flux. Let us take the example of chronically nutrientdeficient environments. Of those available, the species with the fastest metabolism and the highest biomass-specific potential replication rates, for the necessary high aspect ratio of cell surface area to cell volume confers the same advantages in the uptake and assimilation of resources: diffusion boundary layers are small and intracellular transport distances are short (Chisholm, 1992; Reynolds, 1997a; Agawin et al., 2000). In large oligotrophic lakes, the main autotrophic biomass continues to be represented by picoplanktic and nanoplanktic size fractions, for long periods of time. Part of this depends on their escape from herbivory (see later) but a part is simply that too little scarce resource is sequestered by, transferred to or otherwise available to, larger algae. High nutrient affinity and potentially rapid translation of energy into functional producer biomass provide ready and plausible explanations for the ascendancy of small algal species in open pelagic habitats, especially in warm water and under conditions of high solar flux and resources in excess of uptake demand. So, how is it that, in many water bodies, larger algae or colonial species do dominate frequently? When is larger body size a material advantage? When do large units make the biggest contribution to the exergy flux? There are certainly several contributory causes, all of which are consequences of ascendancy. The most cited and most readily understood is to do with the relative immunity conferred from non-selective feeding by zooplankton (e.g., Ferguson et al., 1982). Another is the easier disentrainment from turbulent eddies –which is another way of saying that they have greater powers of selfdirected movement (migratory velocity and distances travelled in unit time). This permits self-regulation with respect to the underwater light field (Heaney and Talling, 1980; Whittington et al., 2000) and the possibility of gleaning the more remote

nutrient reserves in stabilising water columns (Reynolds, 1976; Ganf and Oliver, 1982; Bormans et al., 1999; Nakano et al., 1999). Yet another is that, in kinetic environments in which disentrainment is difficult but mixing depth forces phytoplankton to spend a substantial proportion of the daylight period beyond the depth of growth-saturating irradiances, attenuated form (that is, size increases in only one, possibly two dimensions, manifest in needle-like cells or chain-forming coenobia) is demonstrably beneficial to prolonged entrainment and improved antennal qualities (Kirk, 1976). In this way, community ascendancy brings in its wake, consequent, or “self-imposed”, environmental changes that alter which organismic properties are decisively advantageous. Rapid, opportunistic, exploitative life history strategies are fine for building biomass but increasing augmentation leads to vulnerability to the population responses of filterfeeding phagotrophs; alternatively or additionally, depletion of nitrogen or phosphorus or other nutrient from the most attractive parts of the trophogenic layer will favour the more explorative, gleaner-type strategies of larger, motile plankton (Anderies and Beisner, 2000) and for which large size and lowered mortality compensate the erstwhile disadvantages of slow growth rates. They are the planktic equivalents of Grime’s (1979) stress-tolerant S strategists. Or again, restrictions on energy harvesting through the imposition of truncated photoperiods, as a consequence of seasonally short day-length, increased turbidity or deeper vertical mixing, favour antennal species. The restricted opportunities for processing the available resources into new biomass are argued to be analogous to the frequent habitat disturbance tolerated by terrestrial ruderals, Grime’s (1979) disturbance-tolerant R strategists. Relevant planktic traits amount to facultative antennal enhancement surface-area attenuation, augmentation of photosynthetic and accessory pigment deployment. The point is that the traits which define the fitness of individuals and species apply under a restricted set of contingencies. When conditions change, the advantage moves with the changing habitat constraints towards species with the appropriate alternative fitness or competitiveness. The only constant is that success tends to move among the alternative species available as the adaptations required to develop the highest exergy are also updated by environmental variation. Dynamic advantage is often transient, provided at certain times to C-type strategists, capable of rapid biomass EMERGENCE IN THE PELAGIC 15

expansion and, at others, towards the alternative Sstrategist adaptations for efficient resource scavenging and biomass conservation. Yet again, the (Rtype) ability of certain organisms to maximise exergy gains within truncated or intermittent processing opportunities identifies the conditions providing relative fitness over less efficient light-harvesting species or poor conservers of biomass. Each of the broad adaptive strategies can be represented in the context of the exergy buffering capacity (Fig. 1), where the filtering role of the habitat constraints is strongly apparent as an energetic analogue to the habitat template, and wherein relative competitiveness is a transient determinand of the environment and not a constant of some species-specific trait. Habitat conditions are changed autogenically by emergence: community ascendancy brings in its wake, consequent, or “self-imposed”, progressive environmental changes that alter the organismic traits most advantageous to sustaining growth. The progression implies a directionality of trait selection which, of course, may lead to a sequence of distinct functional types that is recognised as a species succession. “Autogenic ecological succession” could just as easily be styled “emergent directionality”. Successional sequences in the phytoplankton are rarely predictable in the sense that species composition can be reliably anticipated in advance (save in extremely well-characterised assemblages over very proximal timescales). However, it is often possible to account for the sequence of population responses to environmental changes on the basis of an ecophysiological knowledge of the performance capabilities of individual species available (Reynolds, 1989, 1998c). The reactivity and sensitivity of extant assemblages to further variability should therefore be generally predictable from the size of the resource pool and the possible opportunities for its processing, afforded in terms of the exergy flux. Examples of current understanding may be appreciated within the context of equation (1). So far as assembly of the autotrophic community is concerned, the flux of organic carbon ({Corg}’) is, of course, predominantly self-driven and, at least so long as photosyntetic reduction and carboxylation rates saturate the growth requirement and the supplies of nutrient resources are plentiful, self-limited, at least during daylight (see, e.g., Tortell, 2000). However, the more severe is the diminution of the nutrient pool [K]’ –or, more strictly, the diminution of the nutrient least available relative to demand– or the more severe is the restriction of the integrated 16 C.S. REYNOLDS

energy flux ({E}*), then the more selective the assembly process becomes. The “filtration” exerted by the intensifying environmental constraints refines the species-specific performance criteria for continued function and, thus, on the structure of the emergent community. Depending upon the property in contention, competition favours those fitter species with relevant functional traits. The traits themselves are also reasonably understood. Resource constraints ([K]’ low) invoke two groups of adaptive specialisms. One of those is primarily to do with resource affinity. Excepting the uptake requirements to supply the building of such specialist skeletal structures as the siliceous frustules of diatoms or the calcareous tests of coccolithophorids, the elements needed to assemble protoplasm are broadly similar for all aquatic organisms and, in the main, have to be derived from the common source of the adjacent medium in which they are in (often very dilute) solution. There is little evidence to suggest that that any given species is less dependent on the common resource than any other. There are obvious caveats to this statement, such as the important additional resource opportunity presented to fixers of dissolved atmospheric nitrogen. In general, there is little reason to suppose that the fitness of species is differentiated on the basis of their resource requirements. However, it is equally clear that concentration gradients and the laws of molecular diffusion demand that most nutrients have to be actively captured and transported into the cell. The plasmalemma (cell wall) is equipped with specialised, ligand-specific receptor structures that bind the target molecule, pending its biochemical transfer to an internal biochemical pathway (see Simon, 1995). These facilities carry energetic costs, both in construction and operation; quite naturally, their evolution is subject to natural selection, favouring some resource-uptake specialisms –in which species have a relatively high affinity for certain target molecules, but not others– or generalism, in which uptake affinity is relatively poor. Emphasis here should be on the adverb, since the ability of all planktonic algae to deplete external nutrient concentrations of certain key ligands to close to the limits of their analytical detection is enduringly impressive. The concepts of nutrient limitation and its role in species selection have been refined progressively through physiological experimentation and model development (Dugdale, 1967; Droop, 1973; Tilman and Kilham, 1976; Tilman et al., 1982; Rhee, 1982). However, because the criti-

cal behaviour occurs at such low external concentrations, the functional understanding of affinity has come mainly through the fields of biochemistry and molecular biology. For instance, Falkner et al. (1989) applied force-flow functions derived by Thellier (1970) to show that the external concentrations of phosphate below which cells of Cyanobacteria fail to balance its minimal maintenance requirements fall within a range of 1-50 nmol l-1 (0.03-1.5 µg P l-1). Moreover, the same species of Cyanobacteria are known to maintain full growth down to external concentrations of 100 nmol P l-1 (~3 µg l-1) without producing any of the regulator proteins that signal cell starvation and trigger cell reactions thereto (Mann, 1995; Scanlon and Wilson, 1999). A new radiobioassay technique (Hudson et al., 2000) concurs with the view that the amount of phosphorus in the medium supporting active phytoplankton populations can fall to 10 m2 [mol cell C]-1). The more densely populated with light harvesting centres is the area projected, then the greater is the potential energy harvest from the flux of photons. Species that have lower light-dose thresholds for the initiation and maintenance of net growth in mixed layers, which include the diatoms Asterionella formosa and Aulacoseira subarctica, the xanthophyte Tribonema aequale and, especially, the cyanobacterium, Planktothrix agardhii (Kirk, 1976; Reynolds, 1989) also demonstrate considerable flexibility in the amount of photosynthetic pigment they maintain (by a factor of up to 9: Reynolds, 1997b). Conversely, the greater is an alga’s specific chlorophyll-a complement, the lower is the daily light dose required to support its net growth. Where light levels are continuously low, as in stable, deep chlorophyll maxima, the relevant specialism is to exploit as much of the spectrum of usable energy as possible. This is expressed in the support of accessory photosynthetic pigments, especially the phycobilins, which capture the energy of photons not absorbed by chlorophyll a. The burgundy-red colour attained by deep-stratified populations of Oscillatoria rubescens is one of the most familiar examples of chromatic adaptation (Tandeau de Marsac, 1977): the positive contribution to the growth of such populations has been measured, as well as successfully simulated, by Bright and Walsby, 2000). Emergent directionality is subject to environmentally imposed inhibitions as well as to inadequacies, when tolerance is the selective criterion. Thus, adaptations to withstand or neutralise toxic substances can be highly relevant. High acidity of lakes is sufficiently encountered for distinctive groups of acid-tolerant species to have been recognised (most happen to be Chlorophytes or Euglenophytes). Biochemical adaptations for regulating internal pH have been described (e.g., Lane and Burris, 1981) but mechanisms to deal with mobilised aluminium species (see, for instance, Nakatsu and Hutchinson, 1988) may be decisive. 18 C.S. REYNOLDS

Subjected to increasing severity of constraints set by resource availability or accessibility, or by the energy available to convert resources to biomass, organismic preadaptations and facultative adaptabilities of individual species become increasingly influential in determining the relative (competitive) abilities of individual species to continue functioning and to determine the structure of the appropriate ecosystem component. Moreover, the more severe the constraint, the more selective is its impact and the more robust is the direction of assemblage ascendency. However, the succession of events and their eventual outcome outcome is anticipated by the attributes and performance limits of the species that are available.

HETEROTROPHS AND PHAGOTROPHS Returning to the analogy of a national economy, we have followed development to a state of accumulating wealth and labour diversification to a point where it can support exchange of products for services with other sections of society. However, within a finite productive capacity, itself liable to fluctuation in supply, conditions for ongoing communal ascendency clearly cannot be satisfied indefinitely. Eventually, consumptive demand may come to exceed the supply side of the economy and the socio-political organisation becomes strained by its inability to sustain continuous economic growth. Before progressing to the ways that emergent biological structures react to a recession in the currency flow of individuals, it is useful to consider the role of the heterotrophic members of the pelagic community who are not employed in the primary wealth-generating industries. Pelagic heterotrophs gain energy in two main ways. The more readily comprehended of these is phagotrophy, which is exemplified by the familiar supposition that zooplankters feed on planktic algae and fish then feed on zooplankton. So they do but, as a summary of how pelagic systems work, it is dangerously unrepresentative of the array of carbonflow pathways. Many species of the fish to be found commonly in the open water, especially in their juvenile stages, do feed heavily on crustacean plankton if the opportunity arises and is adequately attractive. However, in all but very large lakes, it is evident that the macroinvertebrates of the littoral and sub-littoral areas represent a more attractive energetic return for foraging effort. Piscivorous predators also

tend to follow their prey species to the inshore regions of the water. Globally, there are other ways in which lacustrine fish may be nourished –from filter-feeding, surface scraping, scavenging and semiparasitism. Primary planktivory is reduced from an option to an obligation mainly in very large and very deep lakes, where, as in the sea, evolutionary adaptations to maximise the area of foraging for what are typically sparse resources are prominent. There is an enormous range of preferred foods and feeding adaptations among the zooplankton, even in freshwaters where the phyletic representation in the plankton is rather poorer than in the sea. Cladoceran filter-feeders are capable of consuming large numbers of planktic algae, provided they are of filterable size and adequately concentrated, but they consume all manner of organic particles, including bacteria and fine detritus. Calanoids are more selective of foods occurring in lower concentrations than could satisfy the needs of obligate filter feeders. Few of the many species are exclusively herbivorous. Diaptomids feed extensively on the ciliates and flagellates of the microzooplankton, mainly protistans in the size range 20-200 µm. The fascinating diversity of form and feeding adaptations among the phagotrophic protists themselves is only now becoming realised (Finlay et al., 1999) but it is already clear that the organisation of pelagic food webs that result in its concentration into large macroplankters and nekton is consequent upon the limited opportunities for gathering organic carbon in dilute environments and the ways in which organisms have evolved to exploit them (see Sorokin, 1999). The other main heterotrophic pathway for second-hand carbon involves the activities of microbes. Once again, functional diversity among the bacteria, archeans and other aquatic microorganisms is striking. Not all of them are strictly heterotrophs: besides a handful of photoautotrophs, there are many chemoautotrophs who make their living by oxidising sulphur or nitrogen compounds (see e.g. Atlas and Bartha, 1993). Space and the central theme necessarily confine the consideration here to the aerobic bacteria that are mainly engaged in the assimilation and oxidation of organic carbon. Some live freely is suspension (bacterioplankton) while others attach themselves to the surfaces of dead and decomposing fragments of plant and animal cadavers and voided wastes. Mineralisation through microorganismic activity is important to the recycling of inorganic nutrients and the renewal of carbon dioxide within the water column.

Of particular interest is the abundance of colloidal and dissolved organic carbon in solution in lakes and in the sea. Often exceeding 1 mg organic C l-1 (Thomas, 1997), it is rarely appreciated that the major fraction of the organic carbon present in aquatic ecosystems is not in biomass but in solution (Wetzel, 1995). Much of this DOC, even in the sea, is refractory –mainly humic and fulvic substances derived originally during the breakdown of terrestrial plants. All natural planktic assemblages also comprise substantial numbers of free-living bacteria, typically in concentrations covering about two orders of magnitude, 105.5-107.5 ml-1 (Vadstein et al., 1993). However, there is some doubt about the ease or extent to which bacterial populations exploit the largest pool of organic carbon: bacterial biomass is scarcely correlated to total DOC availability so much as to phytoplankton productivity (Bird and Kalff, 1984). Moreover, on the premise of experiments by Goldman and Dennett (2000), the C:N ratios for oceanic bacterial biomass that are commonly reported (4.5:1 to 7:1; e.g. Kirchman, 1990) rather indicate that natural bacterial growth is limited by the supply of DOC. It is wrong to suppose that all planktic bacteria use the same organic substrates as carbon sources or that all are simultaneously abundant and simultaneously active. There is abundant evidence for the photolytic breakdown of refractory DOC into assimilable forms in surface waters under high irradiance and for positive responses of bacterial biomass thereto (reviews of Thomas, 1997; Cole, 1999). Equally, the numbers of free-living bacteria increase in response to the production of organic carbon produced by phytoplankton (Nakano et al., 1998; Ziegler and Benner, 2000). The implied “leakiness” of organic products from algal cells seems, at first sight, unduly profligate and unhelpful to primary anabolism. On the other hand, it is necessary to recognise that, in an oligotrophic environment, chronically deficient in other raw materials, the potential production of carbohydrate cannot be invested automatically into proteins or new protoplasm, much less into new biomass. Instead, primary photosynthate (or, more likely, PSI intermediates and alternative metabolites, such as glycollate) is necessarily voided from cells as a selfregulatory measure. This low-molecular weight organic carbon is, nevertheless, readily assimilated by proteobacteria, flavobacteria and other organisms in the bacterioplankton. Note that Chlorophytes actually oxidise (“photorespire”) glycollate back to carbon dioxide, which consumes excess intracellular EMERGENCE IN THE PELAGIC 19

photosynthetic oxygen in the cell, though this process but does little to benefit heterotrophs in the extracellular neighbourhood!). The heterotrophic bacteria of the plankton are no less dependent than photautotrophic algae upon a supply of nutrients such as phosphorus and nitrogen, and which bacteria are able to take up at least as efficiently as the algae, if not more so (e.g., Gurung and Urabe, 1999). Potentially, a mutualism develops between a carbon-limited bacterioplankton and a nutrient-limited phytoplankton. The bacteria comprise an essential sector of the pelagic community, accounting for as much as 25% of the organismic carbon present in oligotrophic systems (Weisse and MacIsaac, 2000). Following the recognition of the pivotal participation of microbes in the flow of organic carbon to the higher trophic levels (“the microbial loop”: Azam et al., 1983), the need to revise the view of energy capture and flow in aquatic ecosystems has become progressively apparent. Only in truly pelagic systems (of large, deep lakes and the open sea) is there a substantial reliance on in-situ photoautotrophic energy capture. The same systems generally operate under a chronic shortage of bioavailable phosphorus (owing to its ready immobilisation on metal oxides, hydroxides and clay minerals) and, in the oceans and in lakes in arid regions and low latitudes, of nitrogen. Biological dinitrogen fixation can overcome one of these deficiencies, but it is itself an energy-expensive process and requires the intervention of iron-and molybdenum-based enzymes (Rueter and Peterson, 1987). That these metals tend also to be scarce in the same types of water rather excludes oceanic nitrogenfixers (Falkowski, 1997), leaving the prospect of a meagre producer biomass, chronically dilute and almost continuously resource-deficient. Under such conditions, it is advantageous to primary producers to be able to minimise sinking and grazing losses: this works in favour of relatively large buoyancy-regulating or swimming microplankters (including the large dinoflagellates), or to be very small and nearly neutrally buoyant (as are the picoplankters). In fact, in seas and lakes where the resource capacity is habitually insufficient to support a biomass of more than 50 µg C l-1 (4 mmol C m-3), picophytoplankton are generally the main primary producers. The biomass of co-existent bacterioplankton is in a comparable range (20 to 100 µg C l-1, or ≤8 mmol C m-3; Lee and Fuhrman, 1987). The trophic relationships among planktic autotrophs, heterotrophs and phagotrophs impact 20 C.S. REYNOLDS

upon the relative importance of the carbon pathways through the pelagic. Productive investment in microplankton is most likely to lead to the export of primary carbon as a sedimentary flux of moribund and increasingly bacterised algae biomass and/or as the faecal pellets of the copepods and other planktic consumers of primary product. The microbial network flourishes on (a part of) the relatively very large pool of recalcitrant DOC, the downward dispersion and slow oxidation of which produces most of the dissolved inorganic carbon (DIC). Near-surface photochemical transformation of DOC also produces DIC as well as some low-molecular weight carboxylic acids (Bertilson and Tranvik, 2000). The balance of these processes determines the extent of the internal cycling of the fixed carbon and nutrient resources as opposed to its export to depth. In the deep ocean, with its global-scale circulation, mineralised carbon and nutrients are ultimately returned to sustain new productive cycles. In lakes between 5 and 200 m in depth, the interception of the vertical flux by the profundal sediments interrupts the aquatic part of the regeneration cycle by retaining significant fractions of the export flux, at least at the ecologically-relevant physiological and biogeochemical scales. Of the organic carbon, some is reprocessed by benthic detritivores, subject to the constraint of oxidative capacity but the return of some sedimentary nutrients to the pelagic, especially silicon and, often, phosphorus too, may be very slow indeed. This is the main reason why the average phytoplankton biomass of many such lakes is reasonably correlated to the external nutrient load. More abundant or more freely recycled nutrients lift the ceiling on pelagic primary production. Higher carrying capacity permits a wider functional width to the types of producer organisms that are supportable and to the variety of animal consumers that can forage successfully. In turn, generic differences in food-web structure are evident, with consequent variance in the principle avenues of carbon transfer.

STRUCTURAL THRESHOLDS IN CARBON FLOW THROUGH FOOD WEBS The recurrent supposition is that reproducible patterns in the structure and function of pelagic communities to differing fluxes of carbon, nutrients and processing energy remain the aggregate of the responses of individual organisms to the driving

variables. This section attempts to show how critical quantities constrain the activities of major functional groups of aquatic species and thus influence the achieveable structures of communities. One such threshold that is well attested provides an illustration of the concentration of appropriate food particles that must be available to meet the metabolic demands of an active planktic filter feeder, such as Daphnia. The maximum volume of water that can be processed by an individual animal depends upon its size and the water temperature (Burns, 1969). The amount of water actually filtered is variable but it is close to maximum when all the food particles are readily filterable but the concentration is insufficient to deliver the food requirement for maximum growth. The size of food particles ingested by Daphnia is also a function of animal size (Burns, 1968). From a classical series of measurements, Lampert (1977) showed that the food concentration required to meet the full requirements of growth and fecundity of the Daphnia, at 20oC, is similar over a quite wide range of animal size, close to 0.5 mg C l-1. This is equivalent to a population of some 800 Cryptomonas ml-1, or 70 000 Chlorella ml-1, or around 4 x 107 free-living bacteria ml-1. Above saturating food concentrations (0.5-0.7 g C m-3; see also Jones et al., 1979: 20-28 mJ ml-1), filtration rates may slow. On the other hand, food concentrations of less than 0.08 mg C l-1 fail to satisfy even the basic respiration and maintenance requirements of Daphnia: animals starve and young ones soon die (Ferguson et al., 1982). Where food concentrations habitually fall below 0.1 mg C l-1, Daphnia spp. are effectively excluded. Supposing there to be even as much as 100 µg biomass C l-1 available (say, 200 µg dry mass l-1; with an energy value of ~ 20 kJ per g; Cummins and Wuychek, 1971), the potential energetic yield (≤4 mJ per ml water filtered) scarcely compensates the harvesting effort. On the other hand, the continuation of the microbial loop, through the browsing of bacteria by phagotrophic nanoflagellates (< 20 µm) and the feeding by small ciliates (generally, 150 µg P l-1; Søndergaard and Moss, 1998). Elsewhere, water depth, substratum type and exposure to wave scour may be decisive in selecting against macrophytes. Except where they are in uniformly or predominantly shallow and, hence amenable to macrophytic establishment across the entire area, the dominance of the limnetic ecology by littoral primary production might persist in lakes in the range 1-10 km2. However, my calculations in respect of the annual net production of phytoplankton (75-90 g dry mass m-2) in Crose Mere, England, (a small, mainly steep-sided eutrophic lake having a maximum depth of 9 m and an area of only 0.15 km2) and the annual biomass generation of macrophytes in its narrow fringing reedswamp (1.5 kg m-2) were quite comparable when extrapolated to the entire lake (Reynolds, 1979). With progressively larger area, the overall contribution of the littoral must diminish but it is significant that, in the Bodensee (Lake of Constance, 540 km2; maximum depth: 250 m), Müller (1967) was able still to demonstrate the influence of littoral production in the pelagic food web. Of course, the scale of the food resource available to planktic herbivores among smaller lakes subject to overriding external nutrient inputs or littoral

processing contrasts with the severe capacity restrictions of the true pelagic. If the levels of bioavailable phosphorus and nitrogen can be maintained by inflows and by internal recycling at > 3 µg P l-1 and > 25 µg N l-1, then it is inferred from the ideal stoichiometry of algal cells that it is possible to accumulate a standing crop of photoautotrophs equivalent to 0.1 mg C l-1, that is, just sufficient to satisfy the minimum requirements of cladoceran filter feeders (Lampert, 1977, 1992). As already indicated, a growing aggregate concentration of cladoceran filter feeders compromises the net recruitment rate of phytoplankton. Against a cell replication rate in the order of a doubling per day (r’ ~0.7 d-1), algal increase cannot be contained until aggregate filtration imposes a removal rate of a comparable or greater magnitude (-0.7 d-1), demanding an aggregate filtration rate of more than 500 ml l-1 d-1. In turn, this requires the activity of equivalent of up to 1 mg Daphnia mass l-1, represented by some 10 large (~2 mm) individuals of D. galeata or D. pulicaria, or perhaps, 100 smaller animals (< 1.0 mm) per litre. Should the aggregate filtration rate exceed the algal recruitment rate, however, rapid depletion of the planktic food resource soon follows, with starvation of the filter feeders and with mass mortalities, especially among the younger animals (George and Reynolds, 1997). Having zooplankton exhaust the phytoplankton to relative clarity of open water is an unstable outcome that must be followed by some restucturing of the community. On the other hand, if there is a substantial alternative supply of detrital and bacterial carbon, originating from the littoral macrophytes or from adjacent terrestrial habitat, starvation is not inevitable and mass mortalities may be spared. The quality of food may be poorer but so long as it can support their minimum maintainenace requirements, the aggregate filtration rates of large cladoceran filter feeders (Daphnia and other species distinctive littoral species, such as Sida and Simocephalus spp.) can stop the algae from becoming abundant again. This behaviour may contribute to the upkeep of the low phytoplankton - high water clarity that is associated with the macrophyte-rich state. However, it is clearly far from being the full story, for the high concentration of cladocerans comes to constitute an attractive food opportunity for planktivorous fish. From the dry mass-length relations collected by Bottrell et al. (1976), the numbers of large or small Daphnia needed to filter 500 ml per litre of water each day are calculated to be equivalent to approxi-

mately 1 mg dry mass l-1. Again approximating from Cummins and Wuychek (1971), such a population offers to an appropriate planktivore, a resource of some 20 J l-1. Now, supposing the measurements of Elliott (1975a,b; Elliott and Hurley, 1999) on captive brown trout (Salmo trutta) to be representative of the daily energetic requirements of active fish (between 330 J per gram fresh weight per day for a 250-g fish and 570 J g-1 d-1 for one of 11 g), then the larger fish needs to crop the zooplankton from ~4 m3 of water each day, while the smaller one requires the harvest from ~300 litres. Given pelagic populations of cladocera or calanoids offering perhaps only one hundredth of this concentration, the assertion that planktivores must forage very large volumes of water (≥400 m3 d-1) or, if the opportunity is open to them, to switch to browsing benthic or littoral macroinvertebrates is powerfully upheld. Conversely, large populations of Daphnia may be attractive to foraging fish; consumption may be voracious, leading to abrupt diminution in Daphnia numbers (Mills et al., 1987). Thus, structural thresholds have significance in both directions. Planktic Daphnia concentrations of the magnitude required to control the phytoplankton are sustainable only if planktivorous fish are scarce or absent (Kasprzak et al., 1999; Scheffer et al., 2000), certainly less than 10 g ww m-3, or if the zooplankton gains adequate protection from planktivorous predators from macrophytic refugia (Irvine et al., 1990, 1991; Søndergaard and Moss, 1998). In all cases, the sustainability of cladoceran filter feeders remains dependent upon the simultaneity of the minimal threshold of filterable algal, bacterial and detrital particles of ≥0.1 g C m-3. This may be fulfilled frequently (Kamjunke et al., 1999) but, away from shallow margins, the scaling difficulties of striking and holding a steady state are strongly apparent. It becomes clear that deliberate manipulation of the food web to control phytoplankton abundance can be usefully applied only if the phytoplankton ceases to be the major vehicle of primary carbon transfer. Alternatives are identifiable in small, shallow ponds with a high input of organic carbon and supplemented by macrophytic autotrophy but not in the open, unpolluted water of the pelagic. The essential deduction is that the structure of the community that may be assembled and the manner in which the limnetic food-web processes its carbon supply are wholly consequential on the resource flux and on the processing capacities of individual organisms that happen to be present and fitted to the task. EMERGENCE IN THE PELAGIC 23

FIG. 4. – Carbon- and energy-flow constraints in the structuring of emergent pelagic communities. Accepting that the amount and distribution of native carbon sources vary over several orders of magnitude, phytoplankton composition varies with the carbon dynamics, while the concentation of food particles determines the type and productivity of the zooplankton and, in turn, the resource and its relative attractiveness to fish. Shaded areas represent the transition but is generally close to a carbon availability of 0.01 mmol l-1 in each instance.

This principle is fully consistent with the concept of a functional habitat template populated by appropriately-adapted species and according to contingent rules of assembly. The community structure is reasonably predictable from the supportive capacity of the habitat (Southwood, 1977; Lamouroux et al., 1997). A provisional guide to the carbon thresholds in the structuring of pelagic ecosystems is presented in Figure 4. The various trophic levels are shown against a logarithmically-scaled spectrum of useable carbon. The entries conform to the discussion in the text.

DISSEMBLY PROCESSES AND THE MAINTENANCE OF DIVERSITY Emergent communities acquire a structure and organisation dominated by the best-adapted, highest-exergy species under the environmental conditions obtaining. The principles of maximum ascendency and the maximum power determine the struc24 C.S. REYNOLDS

tural and functional make-up of the community. Thus it is that the best-fit species in each tangible niche is expected to rise to a steady-state dominance that, theory demands, excludes all inferior competitors, though always within the abiotic resource- and processing-rate limits. Usually, this means that Kselected “gleaners” begin to exclude the r-selected “opportunists” (Tilman, 1977; Anderies and Beisner, 2000). The fact that most of the living world and, most obviously, the conspicuously variable environment of the plankton, fails to comply with any such predicted ideal has long been a fascination to ecologists. The short temporal scales that characterise the lives of planktic organisms have perhaps contributed most to the recognition of what Hutchinson (1961) referred to as the “paradox of the plankton” –it actually applies to all immature (sensu being far short of self-determined steady state) biotic communities– although they have also facilitated the development of several explanative hypotheses. In essence, these acknowledge that food-web interactions promote

co-existence (Paine, 1966); that co-existence is possible through the simultaneous physical or physiological niches (Tilman, 1977); and that temporal variability keeps renewing some resource or processing capacity (Connell, 1978). These explanations are not mutually exclusive. However, conspicuous variability in the physical habitat and the sometimes quite rapid restructuring of the planktic components of the community are intuitively supportive that periodic restructuring of the habitat is symptomatic of “disturbance”. The ordered progress of emergent community assembly is stopped, diverted or completely usurped by the decisive intervention of external factors. Moreover, this can happen repeatedly, so that the frequency of directional change becomes a factor favouring the coexistence of an unexpectedly large number of potentially competing species. Infrequent disturbances allow community emergence to progress towards a competitive exclusion of all but the most successful “gleaner” species and very frequent disturbances are tolerated only by a few opportunists. At intermediate frequencies, a larger number of species are permitted to co-exist. This is the essential provision of Connell’s (1978) intermediate disturbance hypothesis (IDH); the idea does have earlier provenance (Wilkinson, 1999), it is Connell’s articulation by which it is best known. There is little difficulty in understanding the intervention of catastrophes, from fires and storms to volcanic eruptions and lava-flows, arresting, not to say obliterating, the development of self-organising terrestrial vegetation and re-opening the land surface to colonist plants. The pelagic analogues of severe flood and storm events as mechanisms re-setting pelagic successions were promoted in Reynolds (1980). Stochastic, smaller-scale forcing may create just the fluctuating environment which prevents the exclusion of opportunist (“C”) strategists by (R- or S-strategist) gleaners Anderies and Beisner, 2000). However, these possibilities invoke an assumption that there remain simultaneous sources of invasive species, which also rather implies that there has to be a continuity of disturbances and a continuum of patches in different stages of maturation, among which invasive species may migrate. It is self-evident that were this not true, opportunism (r-selection) would have no viability as an adaptive strategy. This view of patch dynamics is explicit in Connell’s (1978) hypothesis and it is implicit in Hutchinson’s (1961) proposed explanation of the diversity paradox, which refers to “contemporaneous disequilib-

ria”. Thus, dispersal constraints are as important to community assembly as are the inevitability of selforganisation and the stochasticity of external disturbances. Careful analysis of structural changes in the phytoplankton has uncovered other interpretative complexities. Not the least of these is that external forcing has no unique scale and certainly no unique response. Storm events do not necessarily break the current species dominance while, elsewhere, relatively trivial events lead to upheavals of species composition (see, for instance, Jacobsen and Simonsen, 1993). Indeed, external forcing relevant to the planktic organisation comes with variable intensity and at a variety of temporal scales. Some, associated with the shift of seasons and interannual differences, occur at scales (100-1000 d). Equally, individuals of a single generation may be subjected to the variability in the intensity of wind mixing and to day-time cloud cover, as well as the alternation between night and day. It is at this scale that planktic light-harvesting takes place and thus, it is this scale which most affects the dynamics of the species present (Huisman et al., 1999). The way these factors are integrated over a generation or two clearly do influence the environment perceived by the individuals, which will set distingishing limits to growth, which will shape the ascendant community and which may well constitute decisive environmental selectivity. Quite manifestly, such developments are not self-organised, but are allogenic consequences of environmental variability. Two other contributions serve to improve the generality of a theory of ecological disturbance. One concerns the importance of distinguishing clearly between the biotic response –the observed disturbance– and the external forcing that precipitates it (Juhász-Nagy, 1993). For example, wind-mixing may have much less effect on the functioning of phytoplankton in a clear, nutrient deficient lake than in a turbid, eutrophic one. Equally, strong mixing will have little lasting effect on the species composition of a turbid, eutrophic lake if it blows for one day compared to the effect of the same wind if it persists for a week. Arguments concerning the distinctions among the intensity, frequency and persistence of disturbance can be addressed, not merely by separating cause and effect but to compare them in comparable units. To be able to make preliminary evaluations of the energy harvest of pelagic photosynthesis and its simultaneous losses to maintenance and, thus, to estimate the margin of exergy buffering EMERGENCE IN THE PELAGIC 25

against external forcing (Reynolds, 1997b) provides the second promising dimension to modelling disturbance reactions in the plankton. These developments also offer the prospect of testing quantitatively the relationship between disturbance and the structural re-setting that favours a more primitive and less self-selected community. The present hypothesis indicates that by resisting severe or continuous resource competition or any bias in favour of a particularly efficient processing, species filtration can also be less exacting and any selective advantage is traded through the assemblage as a whole, before any has the opportunity to exclude others. The diversity thus maintained provides may alternative options and pathways for moving carbon through the ecosystem, while the relative immaturity of the system (where potential exergy is much higher than maintenance costs) favours its ready return to net productivity after each critical forcing. These communal traits are frequently advanced as the benefit of efforts to maintain a high species richness but it is just as probable that diversity and high areal productivity (sensu conversion of resource to biomass per unit area per unit time) are consequential upon a variable but positive exergy flux. The distinction is not entirely academic but with the current focus, quite properly, on the mechanisms and ecological importance of a high natural biodiversity (e.g., Huston, 1994; Lawton et al., 1998; Waide et al., 1999), the small temporal scales of the diversity fluctuations in relation to the internal organisation of planktic communities seem apposite and worthy of further detailed study.

TABLE 1. – Emergence in planktic communities. Summary of statements 1. Component species must be present in substantial numbers (“viable inocula”) and that these must find the conditions obtaining to be adequate to meet their minimal requirements for net biomass increase. 2. Early assembly is biassed towards species-specific adaptive traits favouring rapid resource acquisition and conversion; that is, r-selection predominates in early succession (Odum, 1969). 3. The more photosynthetic biomass that is built, the greater is the aggregate ability of the developing assemblage to intercept energy. The richer is the species representation the more varied is the network of energy flow and the greater is the information content. 4. Relative high nutrient affinity and potentially rapid translation of energy into functional producer biomass provide ready and plausible explanations for the ascendancy of small algal species in open pelagic habitats, especially in warm water and under conditions of high solar flux and resources in excess of uptake demand. Invasive, opportunistic nanoplanktic or small microplanktic species are frequently found to dominate. 5. The advantages of small size persist under a wide range of circumstances. However, larger, more conspicuous components of the plankton often emerge to account for relatively more of the planktic producer biomass than do the nanoplankton. 6. Community ascendancy brings in its wake, consequent, or “selfimposed”, progressive environmental changes that alter the organismic traits that are decisively beneficial to growth. 7. Organismic preadaptations and facultative adaptabilities of individual species become increasingly influential in determining the relative (competitive) abilities of individual species to continue functioning and to determine the structure of the appropriate ecosystem component. Moreover, the more severe is the constraint, the more selective is its impact and the more robust is the direction of assemblage ascendancy. However, the succession of events and their eventual outcome is anticipated by the attributes and performance limits of the species that are available. 8. The structure of the community that may be assembled and the manner in which the limnetic food web processes its carbon supply are wholly consequential on the resource flux and on the processing capacities of individual organisms that happen to be best fitted to the task. 9. The filter behaves as does the Venn diagram of classical set theory: it is passed only by species with appropriate adaptations and which, of course, happen also to be present.

CONCLUSION This dissertation has sought an explanation of the ways in which planktic communities are assembled, essentially on the backs of the biological responses of individuals of particular species attempting to grow and multiply in environments that are not necessarily altogether favourable to them. The short generation times of planktic organisms provide appropriate and sensitive indicators of the ways in which assemblages respond to a background of fluctuating resource constraints and processing opportunities. Analysis at the appropriate timescales reveals that planktic systems generally operate in conspicuously variable environments which are, by degrees, sometimes replete in meet26 C.S. REYNOLDS

10. Individuals of a single generation may be subjected to variability in the intensity of wind mixing and to day-time cloud cover, as well as the alternation between night and day. It is at this scale that planktic light-harvesting takes place and, thus, it is this scale which most affects the dynamics of the species present

ing biotic demands placed upon them, sometimes stressed by resource inadequacy and sometimes so disturbed that the exploitative opportunities are short or intermittent. Thus, emergent behaviour is correspondingly shaped by species responses that invest maximum ascendant power into biomass, or that are efficient in resource uptake and conservation, or those that are efficient in processing resources during very limited opportunities.

While the relatively simple organisational state of many pelagic communities reflects their vulnerability to change and emphasises the fragility of internal processes in the face of a physically dynamic, abiotic environment, the patterns are sufficiently clear for it to be possible to abstract some draft rules of emergence. The statements in Table 1 are culled from sectional conclusions or observations italicised in the text. Refinement of these statements may be helpful to the interpretation of emergence in other systems. For the present, it will be sufficient to have its proposed application to pelagic communities explored and tested, by real experiments and realistic simulations.

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SCIENTIA MARINA

2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

Caught in the food web: complexity made simple?* LAWRENCE R. POMEROY Institute of Ecology, University of Georgia, Athens GA 30602-2202, USA. E-mail: [email protected]

SUMMARY: Several historically separate lines of food-web research are merging into a unified approach. Connections between microbial and metazoan food webs are significant. Interactions of control by predators, defenses against predation, and availability of organic and inorganic nutrition, not any one of these, shape food webs. The same principles of population ecology apply to metazoans and microorganisms, but microorganisms dominate the flux of energy in both marine and terrestrial systems. Microbial biomass often is a major fraction of total biomass, and very small organisms have a very large ratio of production and respiration to biomass. Assimilation efficiency of bacteria in natural systems is often not as high as in experimental systems, so more primary production is lost to microbial respiration than had been thought. Simulation has been a highly useful adjunct to experiments in both population theory and in studies of biogeochemical mass balance, but it does not fully encompass the complexity of real systems. A major challenge for the future is to find better ways to deal with the real complexity of food webs, both in modeling and in empirical observations, and to do a better job of bringing together conceptually the dynamics of population processes and biogeochemistry. Key words: food web, microbial food web, energy flux, community structure.

INTRODUCTION “The classic marine food chain –algae, zooplankton, fish– can now be considered as a variable phenomenon in a sea of microbes (Karl 1999).” The food web is one of the earliest and most fundamental concepts in ecology. Darwin (1845) recognized the existence of a pelagic food chain. Elton is credited with first appreciating the importance of food chain and food web concepts (Lawton 1989), but major antecedents include Petersen’s (1918) quantitative conceptual model of the food web that is supported by eel grass, and Hardy’s (1924) conceptual model of the herring food web. Elton, and later Hutchinson and his students, developed both population and mate*Received March 29, 2001. Accepted April 30, 2001.

rials-flux approaches to food webs (Hagen 1992), but the two approaches quickly diverged. Paine (1980) showed that population interactions do not equate with energy flux, and asserted that energy flux was unimportant and “has generated few insights into ecological processes.” This put studies of population biology and energy-flux on separate paths that only recently have shown signs of beginning to merge into a unified paradigm (e. g. McQueen, et al., 1986; Hunter and Price 1992; Polis and Winemiller 1996). Ecologists recognize that energy input matters, although they agree less on when and how it matters. What clearly matters is formulating tractable hypotheses about ecosystem structure and function. Repeated attempts to simplify the inherent complexity of food webs have led to Sisyphus-like progress in which investigators have made generalizations and then have been forced to qualify them. FOOD WEBS 31

A step not yet firmly taken is the assimilation of microorganisms into conceptual food webs and food web models in spite of evidence that the ocean’s food web, like most others, is primarily microbial (e. g. Fuhrman et al., 1989; Li et al., 1992; Sommer 1993; Karl, 1999). This review views microbial food webs and metazoan food webs as a single, continuous entity and examines evidence that energy flux can influence community structure. Of 113 food web descriptions compiled by Cohen et al., (1990), 20 include bacteria, 9 protozoa, and 8 fungi. Virtually every one of those fails to include 2 or more microbial links. It is equally true that studies of microbial food webs have rarely included interactions with metazoans except as donors of organic matter, sometimes on grounds that the large metazoans constitute such a small fraction of energy flux.

FOOD WEB STRUCTURE Recognizing microbial food webs A very early suggestion of the significance of microorganisms in the sea came from Lohmann (1911), whose observations were imaginatively extrapolated by Vernadskii (1926). At that time, microbiology lacked the technology to enumerate bacteria or to estimate their production. During most of the 20th Century, microorganisms were thought to be significant in regenerating nitrogen and phosphorus but not to be significant components of the flux of carbon in the marine food web (e. g. Steele, 1974; Cohen et al.,, 1982). Because their size is similar to the wavelengths of visible light, most marine bacterioplankton are invisible to conventional microscopy and could not be counted directly until the development of epifluorescence microscopy (Francisco et al., 1973; Hobbie et al., 1977). Their metabolic impact on ecosystems was underestimated until the development of tracer methods (Azam and Hodson 1977; Fuhrman and Azam 1980). The view that the ocean is a microbial system has not been shared by many fisheries scientists (e. g. Steele 1974; Cohen et al., 1982; Boudreau and Dickie 1992; Cury et al., 2000). They acknowledge the existence of the microbial food web but dismiss its significance to the food webs of fishes. A different view has been proposed by oceanographers, based on the work of Moloney and Field (1990) and Painting, et al., (1993) which will be discussed in section 4. 32 L.R. POMEROY

Significant differences exist between terrestrial and aquatic food webs (e g. Cohen 1994; Fenchel 1994) but there is not complete agreement on what the differences are. It is probably important that, unlike single-celled phytoplankton, entire terrestrial plants are rarely consumed completely by grazers, and the standing biomass of terrestrial plants is rarely depleted by them (Hairston et al., 1960), while in the sea only transient phytoplankton blooms temporarily outrun consumption. What is sometimes overlooked is that in terrestrial ecosystems most of the microbial food web is situated in soils, which are not treated as a part of the system in most population models or analyses of terrestrial food webs, but are modeled separately by different investigators. Connections from microbes to consumer populations exist through soil invertebrates and their predators. A significant connection of microbes to higher organisms is through symbiotic mycorrhizae that sequester inorganic nutrients for trees while receiving organic nutrients. Mycorrhizae are consumed by the metazoan food web in the soil, and their sporocarps are eaten copiously by vertebrates, including H. sapiens. Much of the biodiversity and many physically small organisms in terrestrial systems are in the soil, so terrestrial systems may not be as depauperate in those respects as Cohen (1994) suggests. Size versus biomass The total amount of prokaryotic carbon in the biosphere is at least 60% of that in plants and probably exceeds their metabolically active tissue (Whitman et al., 1998). In terrestrial soils, 94-97% of the non-root biomass is bacteria and fungi, present in quantities of tons/ha (Coleman, 1994), similar in magnitude to root biomass (Schlesinger, 1991). In abyssal benthic systems, 87% of the biomass consists of bacteria, present in quantities of kg/ha (Tietjen 1992). In oligotrophic temperate lakes, bacteria comprise up to 58% of the biomass (Biddanda in press). In the oligotrophic Sargasso Sea, bacterioplankton constitute 70-80% of the biomass, and protozoa constitute 7-17% (Fuhrman et al., 1989; Li et al., 1992). In the North Atlantic spring bloom (Table 1), bacterioplankton constitute 15-50% of total biomass and 64-75% of heterotrophic biomass, with mesozooplankton being 0.5-2% (Harrison et al., 1993; Li et al., 1993). The distribution of biomass among different decades of size is not as regular as some earlier work suggested (e. g. Sheldon et al.,

TABLE 1. – Comparison of the biomass, mg C m-3, in a coastal marine system, an oceanic central gyre, and oceanic frontal region. Integrated to 100 m off New Zealand (Bradford-Grieve et al., 1999), and to 200 m in the Sargasso Sea (Fishes: Angel, 1989; Net zooplankton: Ortner et al., 1980 and Ashjian et al., 1994; Protozoa: Caron et al., 1995; autotrophs and bacterioplankton: Li et al., 1992). English Channel sampled only at 10 m (Rodruíguez et al., 2000, except fishes Cohen et al., 1982). English Channel off Plymouth Season Fishes and squid Zooplankton Protozoa Bacterioplankton Autotrophs

spring

summer

autumn

winter

770 500 50 10 45

770 1200 150 20 160

770 1200 25 20 28

770 300 15 15 10

Sargasso Sea spring 1 1.3 4.3 5.6 5

Waters East of New Zealand Subtropical Subtropical front Subantarctic spring winter spring winter spring winter

1.2 1.2 5.1 11.2

29 10.1 22.4 9.7

1.9 1.3 5.7 22.2

5.5 4.7 14.2 43.5

3.1 1 7.9 3.4

3.9 5.9 11.5 10.8

1972). Bacterial biomass in the ocean varies much less than the biomass of phytoplankton and other microorganisms (Table 1), and bacteria tend to be the dominant biomass in extremely oligotrophic environments, such as the central ocean gyres (Fuhrman et al., 1989; Li et al., 1992). Where seasonal studies have been performed, they tend to show major changes in biomass of other components (Donali et al., 1999; Rodruíguez et al., 2000).

system size, but not system productivity (Post et al., 2000). To make matters worse for investigators, a large fraction of the micro- and picoplankton is composed of mixotrophic organisms and internalized mutualistic associations (Safi and Hall, 1999; Caron, 2000; Dolan and Pérez, 2000). Also, chemolithotrophic bacteria have evolved associations with organisms in many phyla (Cavanaugh, 1994; Polz et al., 2000).

Chain length and web complexity

Predator or donor control of structure?

Although not everyone agrees (e. g. Morin, 1999), probably neither the amount of primary production nor the assimilation efficiency of consumers is a major determinant of the length of food chains or diversity of most food webs. Fretwell (1977), while observing terrestrial metazoan food chains, proposed that high productivity produced longer food chains, although Ryther (1969), observing the sea, proposed that the high fish production of coastal upwellings was the result of high primary productivity and a short food chain. We now know that the food web of coastal upwellings contains most of the links present in the food webs of central gyres (Vinogradov and Shushkina, 1978; Moloney and Field, 1990; Painting et al., 1993; Carr, 1998). The emergence of short chains in blooms and upwellings may, nevertheless, be significant for terminal-consumer fishes, as Ryther (1969) suggested (Legendre, 1990). The number of trophic transfers is limited ultimately by dissipation of energy, but simple conclusions may be confounded by re-utilization of organic matter (Strayer, 1988) and by variable effects of scales of time and space. The scales on which system productivity affects system function and structure may be different from those of predator-prey effects (Menge, 2000), and empirical evidence from lakes indicates that food chain length correlates with

The proposition of Hairston et al., (1960) that “the world is green,” because terrestrial predators control the size of grazer populations, instigated a cascade of research and theory which has trickled down to the ocean over four decades. Fretwell (1977) refined the proposition that the number of links in food chains determines whether primary producers were controlled by grazers. In systems with an even number of links, primary producers were grazer-controlled while in systems with an odd number of links primary producers were resource controlled. As Fretwell pointed out, this was most likely to happen in simple food chains with little or no branching. Under the rubric, exploitation ecosystems, this was formalized in models (Oksanen et al., 1981). Based primarily on terrestrial examples, the principles found useful application in lakes (Carpenter and Kitchell, 1993). Further research in fresh water (McQueen et al., 1986), in terrestrial systems (Hunter and Price, 1992), and in microbial microcosms (Lawler, 1998) has revealed a complex interplay of top-down (predator) and bottom-up (resource) effects. A general theory of food web dynamics has to take both into account, as well as other factors. The terrestrial world is green as much because plants have evolved defenses as because predators control herbivores (Polis and Strong, FOOD WEBS 33

1996). Most of the examples of predominant control by predators are from simple webs, such as rocky intertidal communities, or even more sparse experimental ones. More complex systems reveal more complex interactions (Polis, 1991; Polis and Strong, 1996; Polis and Winemiller, 1996). Wiegert and Owen (1971) pointed out that organic matter does not accumulate in ecosystems, despite the low utilization of plant resources, because it is being utilized along detrital-microbial pathways. We are approaching a level of understanding where controls from top and bottom can be seen interacting. A modeling study suggests that the ability of copepods to control phytoplankton abundance may be limited by nitrogen-limited phytoplankton cells (Roelke, 2000). Also, Thingstad (2000) developed a marine planktonic food web model incorporating both resource limitation and grazer-predator controls. The model suggests that the control of relative population sizes is top-down but that the total amount of limiting element (C, N, P) in the entire food web mediates changes in the size of each population. While empirical evidence in the ocean indicates that bacteria are partially resource-limited (Ducklow, 1992), their nearly constant abundance also suggests limitation by predators. Marine bacterioplankton approach the minimum size possible for an organism, having even reduced their water content to a minimum (Simon and Azam, 1989), possibly as a result of grazer selection of the largest prey. However, some of those very small bacteria transform into larger rods in the presence of added C, N. and P. Heterotrophic bacteria attached to detritus, where presumably there is a more favorable microenvironment, are large (2 µm) rods (Boenigk and Arndt, 2000). Their transformation from 0.3 µm spheres to rods and back again has been documented (Wiebe and Pomeroy, 1972; Novitsky and Morita, 1976; Jacobsen and Azam, 1984). These hypotheses of strong control on marine bacterioplankton by both resources and predators have been difficult to test, but some progress has been made in lakes (Pace and Cole, 1996; Langenheder and Jürgens, 2001). Stability: an hierarchical mismatch? Much theoretical work on food web stability has relied upon models, microcosms, and simple, accessible communities, such as the rocky intertidal or upon food chains condensed into trophic levels. Theory, thus derived, has often been extrapolated to 34 L.R. POMEROY

the larger world, although the problems inherent in doing this have been pointed out (Allen and Starr, 1982; Lawton, 1989; Polis and Strong, 1996). Models of food webs are necessarily structurally simple and lack complexity, redundancy, and much of the reticulate nature of real food webs (Polis, 1991; Polis and Strong, 1996). The empirical food web descriptions assembled by Cohen et al., (1990) frequently contain “trophic species,” which are condensations of a guild of species or sometimes much more. Such caricatures of real food webs have been criticized as lacking reality (Lawton, 1989). Cohen et al., (1990) wisely label these simplifying abstractions “spherical horses.” Sometimes, as Cohen et al., say, you can ride a spherical horse, but don’t count on doing so. How effective condensation may be will depend on how similar the combined species are and what questions we ask about them. Suppose, for example, that in a model of an upwelling system we create a trophic species called dinoflagellates, a lesser condensation than the typical trophic species. Dinoflagellates are important in the diet of newly-hatched anchovy larvae (Lasker, 1979). If the dominant dinoflagellate is Gymnodinium, the larvae eat them and grow. If the dominant dinoflagellate is Gonyaulax, the larvae eat them, but cannot digest them, and die. Similar food-source problems have been demonstrated for oysters (Ryther, 1954a) and for Daphnia (Ryther, 1954b). Communities are filled with this sort of minute complexity. The obvious danger is in too casually transferring to the rain forest, or marine plankton, principles shown to work in three-level, five species models. Caswell (1988) quotes Lewontin: “It is not the function of theory to describe what has happened in a particular instance.” But investigators sometimes do that, even though the real world is more complex. Lawton (1989) pointed out the lack of ecological studies encompassing both population structure and energy flux. Pickett et al., (1994) say, “…unboxing organism features and behaviors and examining the reciprocal effects of organisms and ecosystems is a frontier for integration.” An inherent difficulty in this is that populations, communities, and ecosystems are on hierarchically different levels of organization (Allen, 1987) and have different return times (Slobodkin, 1961). A scheme of population structure and energy flux interactions was described for marine planktonic systems by Legendre and Rassoulzadegan (1995) who classified planktonic communities based on relative

fluxes of energy and nutrients. In the most impoverished central regions of oceans, a microbial-loop dominates biomass and energy flux. All community components are present, including large fishes and cetaceans, but the latter are rare. In upwelling systems, eukaryotic autotrophs and consumers are more abundant, but the microbial components are present and their abundance and energy flux is greater in absolute terms than it is in the central gyres (Carr, 1998). The importance of species redundancy for ecosystem function continues to be debated (Hart et al., 2001). By creating “trophic species,” modelers implicitly acknowledge species redundancy, although Polis and Strong (1996), among others, question the realism and usefulness of both trophic species and trophic levels. Systems that appear stable energetically over time may experience catastrophic changes in species interactions. Yet, experiments suggest interaction between biodiversity and system function, although most such experiments are small in scale and may not be representative of larger-scale processes (Moore and Keddy, 1989). In comparing the stability of different systems, it is also essential to consider the generation times of the dominant organisms. Forests appear to be more stable than phytoplankton until we normalize for generation time (Allen 1987).

FOOD WEB FUNCTION Size versus metabolic rate We have seen that microorganisms –especially bacteria– constitute a major fraction of the biomass in both marine and terrestrial ecosystems. While this alone should indicate a major role in energy flux for microorganisms, the case is made stronger by the relation of production per unit biomass (P/B) to body size. Both metabolic rate and P/B increase by a factor of approximately 1.75 with each order of magnitude decrease in body weight, although this is variable, with a normally distributed range having SD = 0.11 (Peters, 1983). Most compendia of allometric relationships do not include bacteria. Including them extends the range of P/B upward by an order of magnitude while extending the biomass range downward several orders of magnitude (Fig. 1). Bacterial production and bacterial respiration are the dominant processes in ocean waters (Sherr and Sherr, 1996) and in

FIG. 1. – Ranges of annual production per unit biomass (P/B) for organisms of various sizes and taxa. Data from Banse and Mosher (1980) and Ducklow (1992).

most soils and sediments (Coleman and Crossley, 1996). Combining the ranges of bacterial production reported by Ducklow (1992) and the ranges of bacterial growth efficiencies reported by Jahnke and Craven (1995) and del Giorgio and Cole (2000), it is evident that most marine primary production is utilized in the microbial loop. Because analyses of food webs that omit bacterial processes are usually missing most of the flux of energy or carbon, most theoretical population ecology involves a small fraction of the flux of materials. Microbial processes that dissipate large amounts of the energy sequestered by autotrophs have major, quantitative consequences for the production of biomass by terminal consumers (Pomeroy, 2000). While differences in energy flux may not change the length of food chains in predictable ways, they will affect the amount of biomass at the terminal levels, i. e. the rarity of large, terminal consumers such as fishes. To the above, Lenz (1992) adds temperature, pointing out that as temperature increases with the usual Q10 of 2-3, small organisms will have a greater increment in production than large ones. While this is true, we should note that temperature effects are relative and regional. The optimum temperature ranges of both bacteria and phytoplankton vary with latitude, and just because water is “cold” in polar regions does not imply that organisms are growing more slowly than in low latitudes, where water is “warm” (Pomeroy and Wiebe, 2001). FOOD WEBS 35

Assimilation efficiency Only recently has assimilation efficiency received the attention it deserves (del Giorgio and Cole, 2000). Early assumptions of a 10% “ecological efficiency” of each “trophic level” and later assumptions of a generally high growth efficiency of heterotrophic bacteria of around 50%, have been shown to be poor generalizations (Jahnke and Craven, 1995). Modelers conventionally put a constant in their equations to correct for energy losses owing to assimilation efficiency, but they rarely explore the sensitivity to variations in that constant. The efficiency of poikilotherms is generally assumed to be higher than that of homeotherms, with bacteria highest of all. However, these assumptions come largely from laboratory experiments that do not always duplicate natural conditions. In the real world, parasitized, starving beasts and bacteria often are shown to have low assimilation efficiency. Indeed, organisms sometimes subsist on stored materials, including structural proteins, but this is not usually captured in models, although simple sensitivity tests can show the importance of assimilation efficiency (Pomeroy, 2000). An example of the importance of assimilation efficiency can be seen in the study of a Phaeocystis bloom in the North Sea. Rousseau et al., (2000) found that 75% of the carbon sources of the mesozooplankton were diatoms, although diatoms were responsible for only 30% of primary production. Mesozooplankton obtained the other 25% of organic carbon from a microbial food web which originated from the 70% of primary production by Phaeocystis. Trophic efficiency of the food chain from diatoms to mesozooplankton was estimated to be 34%, while that from Phaeocystis via a detritus food chain was estimated to be 1.5%. A detritus food web, such as that originating from Phaeocystis, involves branching and looping food chains in which the passage of materials through bacteria, in particular, may be very inefficient (del Giorgio and Cole, 2000). If, however, as is the case in most oligotrophic waters, the primary producers are not diatoms but primarily a mixture of microflagellates and autotrophic bacteria being eaten by protozoans, the trophic efficiency of the microbial food web can be significantly higher. In both cases, the connections between the microbial chain and the metazoan chain are an intergral part of a coherent food web that is the principal support of larger metazoans. 36 L.R. POMEROY

Although the length of food chains does not correlate well with primary productivity, variable assimilation efficiency can conspire with primary production to render chains beyond a given length energetically small and the terminal consumers rare. This would seem to work against the effectiveness of detritus food chains which tend to be long and to involve food sources of low quality (e. g. high C:N or C:P and a preponderance of aromatic rather than aliphatic organic compounds). But efficiency is not everything in life (Odum and Pinkerton, 1955). Abundant, low-quality food can be as satisfactory as rare, high quality food –ask any ruminant. Although early food web theory suggested that detritus food webs should be unstable and therefore rare in nature (Cohen et al., 1990), empirical work suggests the reverse. Detritus food webs, and their internalized siblings, ruminant food webs, are everywhere (Polis and Strong, 1996), contributing to the reticulation and complexity of food webs, to the intermingling of microbial and metazoan consumers, and to blurring of trophic levels. Efficiency considerations suggest that detritus food webs support high trophic levels best where rumen-like short cuts have evolved. Rumens or rumen-like processes facilitate the transfer of energy from low-quality food sources to consumers (Pomeroy, 2000). Simulation and theory The complex redundancy of most natural food webs is an important attribute. But as Polis and Strong (1996) point out, every species has a different range of food sources. Grazers and predators switch prey, and even “trophic levels,” as necessity dictates. Many terrestrial predators also eat fruit (Polis and Strong, 1996), owls can subsist on earthworms (Elton 1966), and alligators may subsist on snails (T. Jacobsen, pers. com.). The same is true of marine plankton. The detail of food webs only rarely appears in the literature, one of the better examples coming from the Coachella desert (Polis 1991). It is currently impossible to model detail on such a level not only because of the complexity of simulation but because the natural history is not that well known, especially for the microorganisms. Thus, a gap remains between ecological theory, as developed in simple food-web models, and real food webs in real communities (Polis, 1991; Polis and Strong, 1996; Polis and Winemiller, 1996). This leads to questions about the general applicability of simplistic theoretical approaches, and, for fisheries research, this cre-

ates a practical problem. Can one distinguish the effects of overfishing from natural, long-term trends of species abundance resulting from a movement between two or more poorly defined attractors (sensu (Lewontin, 1969) or within the influence of a strange attractor (Sugihara and May, 1990)? While it is necessary that scientists try to do only what is possible and simulate tractable systems, the inherent danger lies in extrapolating the results to more complex natural ecosystems. When overcome by the temptation to do that, we should seek ways to test our conclusions in the real world. At the same time, it should always be remembered that scale is important, and what dominates a microcosm may disappear at the landscape scale (Allen, 1987; Moore and Reddy, 1989) Continuity of microbial and metazoan webs The connectivity between microbial food webs and metazoans has been addressed by several investigators (Petipa et al., 1975; Vinogradov and Shushkina, 1978; Sherr and Sherr, 1987; Painting et al., 1993; Sommer, 1993; Coleman and Crossley, 1996). Whether or not there is a significant flux of energy from a microbial web to metazoans may depend on the assimilation efficiency of the microorganisms (Pomeroy, 2000), which can be highly variable (Jahnke and Craven, 1995; del Giorgio and Cole, 2000). Legendre and Rassoulzadegan (1995) conceptualized a continuum of planktonic food web structure in which connectivity of the microbial loop with metazoans is maximum near the center of the continuum, which they term a multivorous food web. An inevitable consequence of the presence of a microbial food web is that it consumes much of the available organic matter, more in impoverished systems dominated by a ‘microbial loop,’ and less in systems like coastal upwellings that are more dominated by metazoans (Legendre and Rassoulzadegan, 1995). But even in upwellings, microorganisms play quantitatively major roles Painting et al., 1993; Carr, 1998). Coastal upwelling systems have been viewed traditionally as short food chains of metazoans (Ryther, 1969) and are still viewed that way by fisheries scientists (Boudreau and Dickie, 1992; Jarre-Teichmann, 1998; Cury et al., 2000). Upwelling systems are notoriously variable, depending upon the strength and frequency of upwelling, which regulates primary production, and on more subtle population interactions which may precipitate a shift from anchovy dominance to sardine dominance.

According to the models of Moloney and Field (1990) and Carr (1998), the early stages of a bolus of upwelled water are dominated by picoautotrophs, suitable food for small salps or ciliates but not for adult crustacean zooplankton. Copepod nauplii in recently upwelled water may be feeding on ciliates and may even prefer them to diatoms (Paffenhöfer, 1998). Picoautotrophs continue to grow at their maximum rate throughout the lifetime of the bolus and will still be growing and supporting a microbial food web after newly upwelled nitrate has been depleted and diatoms are no longer growing rapidly. However, diatoms will utilize upwelled nitrate and become the main food available for copepods. If copepods have not completed their life cycle when upwelled nitrogen is depleted, they return to eating ciliates (Painting et al., 1993). Much of the primary production in coastal upwellings is shunted through a reticulated microbial food web, as Petipa et al., (1975) told us, and the microorganisms may be a critical link for parts of the metazoan food web. The famous phytoplankton-zooplankton-fish food chain is not the whole story even in upwellings. While what are probably the most complete models of upwelling systems suggest that the phytoplankton-zooplankton-fish chain is energetically dominant (Baird et al., 1991), Carr’s (1998) model suggests that more than half the fixed carbon and energy flux is through picoplankton. Another example of the differences between microbial loop systems and multivorous systems (the terms of Legendre and Rassoulzadegan, 1995), may be provided by a contrast between the continental shelves of Georgia-South Carolina (GASC) and Louisiana-Texas (LATX). The GASC shelf is one of the least productive of fisheries in North America while the LATX shelf is one of the most productive (Pomeroy et al., 2000). The two shelves have similar areas and similar annual inputs of nitrate. The Mississippi River provides the LATX shelf six times as much fresh water as the GASC shelf receives from rivers, together with most of its nitrate, producing a seasonally nitrate-rich, stratified water column and a multivorous food web of diatoms and copepods. The GASC shelf receives a similar amount of nitrate from upwellings along the shelf break which produce local pulses of high primary production offshore. Most of the GASC shelf, most of the time, however, is unstratified and low in nutrients, with a microbial-loop food web. These differences in structure and in trophic efficiency, not the absolute amount of available nitrogen, may make the difference for the production of fishes. FOOD WEBS 37

Future directions: Dealing with complexity Ecology has the disadvantage of being largely a study of middle-numbers systems (Allen and Starr, 1982). Neither simulation models nor mesocosms capture the complexity of even relatively simple communities. Investigators of population dynamics and of the flux of materials are equally guilty of excessive condensation in attempting to simplify interactions within communities. Also, forcing nature into artificial and arbitrary concepts of trophic levels can do as much to obscure community processes as to explain them. Failure to consider differential responses of individual species (Sommer, 1993) and indirect, secondary effects (Leibold and Wilbur, 1992), as well as ignoring the microbial loop (Simon et al., 1992; Sommer, 1993), all lead to oversimple conclusions about system structure and function. Specialization is an enemy of synthesis in ecology. Studies involving input from both microbiologists and fisheries scientists, plus all that lies in between, are rare. A more powerful solution of ecologists’ dilemma of middle numbers and complex interactions has not yet been discovered. Krebs (1985) has compared the present state of ecology to that of chemistry in the Eighteenth Century. We continue to apply brute force, designing better instrumentation to give us more replication, automated measurements delivered from satellites, and computer programs to process data. It is no secret that we need data sets much larger in size and longer in duration than we now possess to deal with ecosystem complexity (Schaffer and Kot, 1985). This helps to test hypotheses derived from small-scale experiments. It is increasingly possible to test hypotheses by measurements of net changes in large systems. Such tests often tell us that complex interactions cannot be ignored. At present, the best way to integrate all ecosystem processes is with empirical measurements of natural, complex systems. History suggests that we progress by making simplistic generalizations based on fragments of the real world and later define the limits of each generalization and how it fits into a more complex whole. To move beyond this, we need radical departures from the present mindset and approaches. One of the immediate challenges we face is assimilation. We have increasingly strong data sets in population ecology, biogeochemistry, and ecoenergetics, which are essentially the top-down and bottom-up approaches to community and ecosys38 L.R. POMEROY

tem structure and function. Neither approach alone provides a full explanation of the events we observe. Combining these approaches will involve bringing together quite separate academic communities for the examination of ecosystems and their function on several hierarchical levels and several scales of space and time.

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SCIENTIA MARINA

2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

Marine diversity: the paradigms in patterns of species richness examined* JOHN S. GRAY Biological Institute, University of Oslo, Pb 1064 Blindern, 0316 Oslo, Norway.

SUMMARY: The two central paradigms of marine diversity are that there is a latitudinal cline of increasing species richness from poles to tropics and that species richness increases with depth to a maximum around 2,000 m and thereafter decreases. However, these paradigms were based on data collected in the late 1950’s and early 1960’s. Here I show that the 1960’s data, are not representative and thus the paradigms need re-examination. New data from coastal areas in the northern hemisphere record species richness as high as the highest recorded in the deep-sea. Whilst this suggests that the cline of increasing diversity from shallow to deep-sea does not exist, however, the database for the deep sea is not sufficient to draw such a conclusion. The basic problem with the data from the 1960s is that samples were taken on ecological scales and yet they are used to answer evolutionary questions. The questions that such data were to answer were why do the tropics have higher species richness than polar regions or why do deep-sea sediments have more species than coastal sediments? Evolutionary questions need data from much larger spatial areas. Recently, data representative of large scales have been collected from coastal areas in the northern hemisphere and show that there is a cline of increasing species richness from the Arctic to the tropics, but there does not yet seem to be a similar cline in the southern hemisphere. A number of hypotheses have been proposed for the observed patterns in biodiversity. In terrestrial ecology the energy-productivity hypothesis has gained wide acceptance as an explanation for the latitudinal gradient. Here I examine this and other hypotheses critically. Finally an analysis of research priorities is made. Assessment is urgently needed of the spatial scales and dynamics of species richness from point samples to assemblages, habitats and landscapes, especially in coastal areas and in the tropics, where the threats to biodiversity are greatest. New technologies are available, such as side-scan sonar, acoustics, and under-water digital video cameras but as yet have been relatively little used. Conservation of marine biodiversity must be based on sound theory, yet marine diversity studies lag well behind those of terrestrial habitats. Key words: shallow-deep, latitude, longitude, hypotheses, conservation.

INTRODUCTION In 1968 Howard Sanders (1968) produced a remarkable paper that stimulated a debate on marine diversity that has continued for 30 years. His basic hypotheses were that marine diversity a) followed the terrestrial pattern showing an increasing cline from the poles to the tropics and that b) contrary to *Received April 19, 2001. Accepted May 18, 2001.

general belief diversity increased with depth from shallow coastal areas to 2000 m, the limit of his study. Thorson, (1957) had earlier showed that species numbers of nudibranchs and amphipods increased in numbers from the Arctic to the Boreal and to the tropics. Likewise Stehli et al. (1967, 1969) had shown similar trends for species numbers of bivalves. Thus the latitudinal gradient of increasing species richness from Arctic to tropics had been established. PARADIGMS IN PATTERNS OF MARINE SPECIES 41

Sanders, however, did not simply count numbers of species, but collected samples from marine soft sediments with a semi-quantitative anchor-dredge. He followed Whittaker (1960) in arguing that one could only compare diversity within similar habitats and that the soft sediments he studied was a withinhabitat comparison. Sanders not only described the patterns, but also proposed mechanisms as to how the patterns had arisen. His stability-time hypothesis states that in environmentally variable shallow and/or polar areas adaptation by individuals is primarily to the physical environment rather than to other species. In contrast in the deep sea and tropical areas the environment is fairly constant and adaptation is by means of competition to other species. Thus the species richness of shallow and polar areas is “physically controlled”, whereas that of the deep sea and tropical areas is “biologically accommodated”, Sanders (1968). This idea was hotly debated and alternative explanations based on disturbance/predation (Dayton and Hessler, 1972), and on species-area relationships, (Abele and Walters, 1978) were proposed. The ideas that, just as on land, there is a trend of increasing diversity from poles to tropics and that coastal diversity is low compared with that of the deep-sea are firmly accepted in modern text-books, (e.g. Gage and Tyler, 1992; Huston 1994; Levinton 1995; Begon et al. 1995). The, low coast-high deep sea diversity idea, was strengthened further by results of Grassle and Maciolek (1992) who analysed samples of deep-sea sediments from depths between 1,500 and 2,100 m off the east coast of North America and report a total of 798 species from 21 m2 of sediment. These results were claimed to “indicate a much greater diversity of species in the deep sea than previously thought” and “in contrast to the deep sea, shallow water marine communities outside of tropical areas have relatively few species”, Grassle (1989, 1991). However, Gray (1994), Coleman et al. (1997) and Gray et al. (1997) showed high species richness in soft sediments in coastal areas and thus questioned whether there is a cline of increasing species diversity from shallow to deep sea. Not all areas of the coast or the deep sea have high species richness. Coastal areas with high physical variability, such as estuaries and exposed sandy beaches, (Brown and Maclachlan, 1990) have low diversity. Similarly Jumars (1976) showed low species numbers in the deep sea Santa Catalina basin, off the coast of California and low diversity 42 J.S. GRAY

occurs in the Norwegian Sea at depths of 4,000 m, (Rex et al., 1993). Thus it is likely that there is a considerable variability in species: area relationships in both coastal and deep-sea areas. In this paper I will critically examine the patterns of marine diversity, identify problems and then suggest ways forward for research. Diversity, of course, is more than simply the number of species, (see Gray, 2000). Yet here I confine myself to one aspect only species richness.

THE PARADIGMS IN PATTERNS OF MARINE SPECIES RICHNESS Levinton (1995), summarizes what have become paradigms of gradients of diversity, (species richness) as “The best-known diversity gradient is an increase of species diversity from high to low latitudes in continental shelf benthos, in the plankton in continental shelf regions and in the open ocean”; and “... there is a regular change in benthic diversity from coast to abyssal plain, (see also Briggs, 1991, 1994). Species diversity of macroinvertebrates and fishes increases with depth, to a maximum just seaward of the continental rise, and then decreases with increasing distance towards the abyssal plain”. These two paradigms represent evolutionary rather than ecological scale processes and ecological scale data sets are inappropriate to answer evolutionary questions, unless the samples are truly representative of evolutionary patterns. Table 1 shows scales of diversity (here species richness) based on Whittaker but modified by Gray (2000). A single sample within a habitat is called point diversity. (Note that replicate grabs summed together constitute a sample). A number of samples within a habitat measures α species richness, οver a large area samples measure γ diversity and at an even larger scale, that of the region or biogeographical province, ε diversity. Note that there is no β diversity as this is a different concept and relates to changes in the identity of species along an environTABLE 1. – Scales of Species richness based on Whittaker (1985) and modified by Gray (2000). Point diversity α diversity γ diversity ε diversity ity

of a single sample of samples within a habitat of a larger unit (e.g. a landscape or island) the total species richness of a group of large areas (a region or biogeographical province)

mental gradient (See Gray, 2000 for a fuller explanation and also Loreau, 2000). The latitudinal gradient of species richness In comparing patterns of species richness the local (ecological-scale) samples should be representative of province-size (evolutionary) scales. Rosenzweig, (1995) defines a biological province as “a self-contained region whose species originate entirely by speciation within the region”. This is unlikely to be an appropriate definition for marine provinces since marine systems are more “open” and immigration of species will be common. Briggs (1995) however, described marine biogeographical provinces and this suggestion has recently been modified by Watling (unpubl. but see http://marine.rutgers.edu/ OBIS/biogeo/watling.htm). Roy et al.’s (1998) study of prosobranch species richness shows clear boundaries between biogeographical provinces on the Atlantic and Pacific coasts of USA. Stuart and Rex (1994) argue that for prosobranch gastropods local diversity is positively and significantly related to regional (i.e. biogeographical province) diversity. Cornell and Karlson (1999) found similar results for corals. Whether or not this is generally true remains to be confirmed. Cornell and Lawton (1992) in a theoretical analysis of local and regional scale processes affecting species richness argue that the principal direction of control is from regional to local. Thus biogeographic rather than local scale processes are the key to understanding species richness patterns. Yet most marine studies have concentrated almost exclusively on local scale processes. Thorson (1957) recorded an apparent increase in species diversity of some taxa of hard substratum epifauna from the Arctic to the tropics (Thorson, 1957). Later Stehli et al. (1967) showed that bivalve molluscs, at species, genus and family levels increased in diversity towards the tropics in the Indo-Pacific. Thorson’s data show an average of 9 species of nudibranch in Arctic areas 22 in the boreal and 128 in the tropics and for Amphipoda 150 species in the Arctic 180 species in the Boreal and 195 in the tropics. Stehli’s data for bivalves shows ca 50 species at 70oN, ca 130 at 50oN, ca 500 in the tropics, ca 200 species at 30oS and ca 70 species at 60oS. These are extremely small numbers of species on which to make general comparisons and clearly do not represent evolutionary-scale patterns. Sanders (1968) synthesis was based on data collected along a transect, from Gayhead, USA to

Bermuda, (Hessler and Sanders, 1967) and then from a variety of different geographical areas, from the boreal to the tropics and from estuaries to the deepsea slope, (Sanders, 1968). The samples were taken with an anchor dredge, which is a semi-quantitative sampler only and designed to catch many species. Sanders used not the total species richness, but the polychaete-bivalve fraction of the fauna. He claimed that this represented usually over 80% of the total number of species. Abele and Walters (1978) reanalysed the data and showed that the polychaetebivalve fraction varied from an average of 38% in estuaries, to 60% on the shelf, around 70% in the deep sea, to over 80% in shallow waters. They argued that the data, therefore, were unlikely to be representative of total species richness. Thus Sanders data relate to whether or not there are gradients in species-richness of polychaetes and bivalves from poles to tropics and shallow to deep-sea. Two questions arise, firstly, are the number of species of polychaetes and bivalves in Sanders analyses representative of the two gradients? And secondly are the methods of comparison used appropriate? The maximal number of species in Sanders comparison was less than 100. Can one base an analysis of evolutionary-scale patterns on such a small number of species? In the Osloford a single 0.1 m2 grab sample will contain up to 50 species of macrofauna retained on a 1 mm mesh sieve. In Port Phillip Bay, Australia, 197 species were recorded from a single set of five simultaneously taken samples from one sandy station, an area of 0.5 m2 (Poore et al., 1975). In the Bass Strait one 0.1 m2 sample comprised 187 species and 12 out of 38 taken on one occasion comprised more than 100 species (Coleman, 1997). Thus, techniques have improved greatly since the 1960’s and today we have good quantitative data rather than the semi-quantitative data available at that time. Since the 1960s there has been extensive environmental monitoring in coastal areas and thus we have a far more detailed knowledge of the occurrence of species today. What is clear is that the species numbers used in comparative studies in the late 1950’s and early 1960’s are almost certainly not representative of regional scale (evolutionary) processes and cannot be used for comparative purposes. Sanders (1968) not only provided data and hypotheses for patterns of species richness but also developed a method for comparing samples of different sizes. Sanders’ rarefaction technique overestimated species number, but Hurlbert (1971) develPARADIGMS IN PATTERNS OF MARINE SPECIES 43

oped the method in order to correct this problem. The rarefaction method is based on the distribution of individuals among species for the total sample. Using an algorithm that assumes a common evenness (dominance) pattern and a random distribution of individuals among species it produces E(Sn), the expected number of species (s) in a sample size of (n) individuals. Fager (1972) and Gage and May (1992) showed that there were problems with these assumptions and that estimates of the number of species was highly dependent on the evenness. Gray (1996) analysed field data and showed that low evenness (high dominance) occurs at small sample sizes and high evenness (low dominance) at large sample sizes. He showed that rarefaction greatly overestimates the true number of species and especially in small samples, the degree of overestimation being proportional to evenness. May (1993) states that E(Sn ) does not measure species richness but evenness and points out “it is possible for two communities to have very different values of E(Sn ) and the same total number of species”. Yet the rarefaction is still widely used to compare diversity, (e.g. see Lambshead’s review, 1993). As an example, Rex et al. (1993) compared deep sea macrofauna from the North and South Atlantic using rarefacted data and showed a significant cline of increasing diversity moving from poles to tropics for isopods, bivalves and gastropods, although the cline in the southern hemisphere was less clear. Table 2 shows the data on which the analyses were based. Again the numbers used in the comparative analyses are extremely small, even though the total number of individuals was 214,508. (No estimate of the total number of species was given). In fact it is quite common to use E(S50) to compare changes in diversity (Rex, 1983). To take a practical example if one were to take a random sample of 50 (or even 250 individuals) from pooled grab samples containing tens of thousands of individuals, would you expect this to provide a good estimate of the total species TABLE 2. – Data on which the latitudinal gradient of deep-sea benthos is based, (Rex et al. 1993). E(Sn ) = the estimated number of species (s) for a sample size of (n) individuals using the rarefaction procedure of Hurlbert (1971). Taxon Isopoda Bivalvia Gastropoda

44 J.S. GRAY

Maximal E(Sn )

n

56 17 23

200 75 50

richness of the area? The answer must be no, yet this is what is done routinely by using the rarefaction technique. For example, Kendall and Aschan (1993) have made a comparison of the sediment-living macrofauna at a site at 123m depth at 78oN off Svalbard, Norway, with a site off Northumberland, 50oN UK at 80m, with that at 30m off the coast of Java, 7oN. Using E(S200 ) they obtained 32.9 ±1.4, 34.6, and 33.2 ±1.9 where the ± are 95% c.i.’s. They claimed that this data showed no trend in latitudinal species richness. Paterson (1993) also has used similar methods to compare deep-sea diversity and did not find the latitudinal cline found by Rex et al. (1993). However, Kendall and Aschan’s data are from small sample sizes of very limited numbers of species, and in addition depth varied considerably. In coastal areas small differences in depth are known to alter species composition and probably species richness (Olsgard and Gray, 1996, Ellingsen 2001 in press). I do not believe one can make generalisations about latitudinal species richness from such small sample sizes and am not convinced that these studies represent evolutionary-scale faunal provinces, but are rather ecological data sets. There are alternatives to rarefaction methods. Colwell and Coddington (1994) have produced a randomization programme that is available over the Internet, (Estimates, available at http:// viceroy.eeb.uconn.edu/EstimateS). This method takes a sample at random and records species number adds a second and calculates cumulative species number and so on. This process is repeated a hundred or more times so that curves of randomized species accumulation with c.i.’s are produced. We, (Gray et al., 1998) have used a similar method, which differs from Colwell’s in that it calculates the cumulative number of species in all samples of size 2, 4, 6, 8 etc until the total sample size. The methods differ in that Colwell’s is sampling without replacement whereas, Gray et al.’s method is with replacement. There is still the problem of setting the appropriate size at which to compare samples. The species-area curve should give a good estimate of the local species richness and comparisons should be at the largest possible size. Comparison of species richness, based on samples of a few hundred individuals, (or of a few square meters), are inappropriate, even for local comparisons let alone over province scales. There are however, recent data sets that do represent provincial (evolutionary) scales. Species

records of prosobranch molluscs taken from along the coasts of N. America, (1,907 species in the eastern Pacific and 2,009 in the western Atlantic), showed clear gradients of increased species richness from the North Pole to the tropics, (Roy et al., 1996, 1998). Although there are likely to be differences in sampling effort over these latitudinal gradients there is little doubt that the large differences in species richness found are real. Roy et al. show convincingly that the gradient correlates with mean sea-surface temperature and suggest that species richness is probably related to some measure of productivity. A recent compilation of all known species along the Norwegian coasts by Brattegard and Holthe, (1997) gives a total of around 4,500 species of macrofauna and macroalgae. The data for 70o N show 90 species of Nudibranch, 246 species of gammarid amphipods alone and 117 species of bivalves. Thus the old data of Thorson and Stehli (still repeated in textbooks) are out of date and far from representative. An analysis of the new Norwegian data does however, show clearly that there is a cline of decreasing diversity from 60o to 70oN, (Olsgard, in prep.). Similarly Boucher and Lambshead (1995) analysed data on nematodes from temperate estuaries and sublittoral, tropical sublittoral, bathyal, abyssal and trench and found that tropical species richness was lower than temperate and there was an inverse relationship between productivity and species richness. What is surprising about Roy et al.’s (1998) paper, is that although the studies were done only in the northern hemisphere conclusions on global scales are made. Roy et al. (1998) state that “latitudinal gradients, peaking in the tropics and tailing off toward the poles” are the rule, yet they did not take any samples in the southern hemisphere! Rex et al.’s (1993) deep sea data show a cline of increasing species richness from the Norwegian Sea to the tropics, but show a much less clear trend in species richness in the southern hemisphere. There is a huge spread in the number of species at each latitude save for the tropics where the two samples had similar, high E(Sn ) values. Had the variance been similar in the tropics it is unlikely that there would be significant trends. Data from isopods from the Pacific and Atlantic oceans, (calculated in a similar manner to that of Rex et al., 1993), do not show an increasing cline of species richness towards the tropics (Poore and Wilson, 1993). Crame (2000) has made a comprehensive study of living marine Bivalvia (Mollusca) based on 29

regional faunas. The data show strong latitudinal gradients in taxonomic diversity, with a strong asymmetry between the Northern and Southern Hemisphere. The gradient in the Northern hemisphere is more regular than the Southern. Northern gradients are also characterized by a marked inflection at approximately 30 degrees N as also shown in gastropods by Roy et al. (1996, 1998). Crame’s study also has a taxonomic and stratigraphic analysis that reveals the steepest latitudinal gradients are associated with the youngest bivalve clades. This provides further evidence that the Tropics have served as a major centre of evolutionary innovation. Even though some sort of retraction mechanism cannot be completely ruled out, these gradients are most likely the product of primary radiations. Clarke (1992) in his review, shows that the Antarctic has high diversity for many taxa and questions that the latitudinal gradient holds for the southern hemisphere. Lowry (pers. comm.) analysed the fauna of islands from New Zealand to Antarctica and found no clear gradient of decreasing species richness, but recorded changes in the frequencies of various taxa. Furthermore, data from Australia (Coleman et al., 1978, 1997) and Gray et al. (1997) show extremely high species richness at 40o S and there are no tropical data yet published showing as high species richness, (see also Crame’s 2000 data on bivalves showing a hot-spot in Australia). Clearly there is a need for more quantitative data from the southern hemisphere and from the tropics, but data available do not show a clear cline of increasing diversity from Antarctica to the tropics. This pattern may also occur in terrestrial systems since the Fynbos of S. Africa, (Cowling et al., 1992) and Kwongan of south-western Australia have extremely high plant species diversity (Hopper, 1992, Marchant, 1991). Thus one can summarise that in the marine domain there is a cline in increasing species richness from Arctic to tropics but no clear evidence yet that there is a similar cline in the southern hemisphere. The longitudinal gradient of species richness Coral reef diversity is highest in Indonesia (600 species) and decreases radially from there across the Pacific and Atlantic, (Veron, 1995). Data on angiosperms in Asia, Europe and N. America show the same pattern (Latham and Ricklefs, 1997). Crame’s study of living and fossil bivalves (Crame, 2000) shows that highest species richness occurs in southern China-Indonesia-NE Australia region and PARADIGMS IN PATTERNS OF MARINE SPECIES 45

TABLE 3. – Comparison of data on which the paradigm of low coastal to high deep-sea species richness is based Deep Sea

No. of species

No. of individuals

Area sampled

Depth (m)

196–365 10–95 80 136 108 798 1597 c. 100 359

3737–25,242 276–9716 2,000 9034 648 90,677 272,009 214,508 6,870

? ?

1330–4680 300–2500

? 2.5 21 139.5 ? ?

70–4970 5500–5800 1500–2100 250–3029 500–4000 200–3150

343 592 580 803 323 c. 300

20,668 290,401 156,274 60,258 13,014 Ca 37,000

20 75 43 10.4 12 11

270–330 70 2–23 11–51 9-111 24-117

Gayhead-Bermuda transect N Atlantic (Hessler and Sanders, 1967) Various tropics to boreal (Sanders, 1968) Massachusetts and Washington State, USA (Sanders, 1969) Gayhead-Bermuda transect N Atlantic (Rex, 1973) Off California USA (Hessler and Jumars, 1974) Off East coast USA (Grassle and Maciolek, 1992) N. Atlantic (Etter and Grassle, 1992) Atlantic and Norwegian Sea (Rex et al., 1993) South eastern Australia (Poore et al., 1994) Coast Snorre Norway (Gray et al., 1998) Frigg, Norway (Gray et al., 1998)Port Phillip Bay, Australia (Gray et al., 1998) Bass Strait, Australia (Gray et al., 1998) Lochs Linnhe and Eil, Scotland (Pearson, 1970) Firth of Lorne, Loch Etive, Loch Creran, Scotland (Gage, 1973)

is closely associated with the world’s richest development of coral reefs. These data suggest that the South East Asian area is a centre of marine faunal species richness and that species have radiated out from this area. Crame’s study shows that the youngest clades occur in tropical areas with markedly lower diversity of some bivalve clades, such as the heteroconchs, in the high-latitude and polar regions. This, he suggests, may simply reflect the fact that they are not yet fully established there and it may take periods of tens or even hundreds of millions of years for bivalve clades to disseminate fully across the earth’s surface. The shallow (coast) to deep sea gradient of species richness Table 3 shows the number of species and individuals, depth and area used to make generalisations about the shallow: deep-sea diversity gradient. It is clear that only recent data are of a quality that allows us to make generalisations. Table 3 shows that similar areas of seabed from coastal habitats of Norway and Australia are as rich in species as that of the only comparable deep-sea study (Grassle and Maciolek, 1992). Grassle and Maciolek reported 698 species from 90,000 individuals whereas the Bass Strait data, the most rich of our four, shows 803 species from 60,258 individuals and 10.2 m2. Other surveys support high number of species in coastal areas: e.g. 572 species from 12.3 m2 in Western Port, Australia (Coleman et al., 1978), and 620 species from 50 m2 and 40,000 individuals on the Norwe46 J.S. GRAY

gian shelf at 70–305 m depth (Gray, 1994). (The extremely high diversity shown for Bass Strait needs a comment. Here the sediment is of biological origin, calcareous shells of Mollusca and Foraminifera etc and is coarse. Shell-gravels are known to be rich in species but usually occur as small patches rather than huge areas such as in the Great Australian Bight. The Australian continent is extremely dry, and there are no major rivers discharging terrigenous material to the southern coasts, so that the sediment type cannot be compared with that of most other continental shelves, which are mainly sand or mud). Thus again data that are available do not suggest that there is a clear gradient of increasing species richness from shallow water to the deep sea; comparable areas of soft sediment habitat have similar numbers of species. Table 3 shows that there is only one recent quantitative survey from the deep sea examining many taxa, that of Grassle and Maciolek (1992). Other data (e.g. Hessler and Wilson, 1983; Poore and Wilson, 1997) suggest that Grassle and Maciolek’s data are not representative of the deep sea as a whole. Thus there are too few data sets yet available to make general statements about deep-sea diversity. Gage (1996) questioned whether one could make valid comparisons of the deep-sea data of Grassle and Maciolek with those of coastal areas. He stated that the deep-sea area sampled by Grassle and Maciolek was a single uniform habitat, whereas coastal samples (e.g. those of Gray, 1994) are invariably from a variety of different types of sediment. Gage argued that one cannot compare species richness of

within habitat (deep-sea) samples with shallow water (between habitat) samples. Gray et al. (1998) countered by suggesting that along a 176 km transect of the deep sea the sediment and biological assemblages must vary so that both the deep sea and coastal samples are from between habitats. They further argue that it is still a valid question to ask whether there are more species per unit area in the deep sea compared with the coast irrespective of any variation between habitats. In summary, as with the southern hemisphere species richness gradient, there is no clear trend in increasing species richness from coasts to deep sea. Hypotheses concerning gradients in species richness From the above it is clear that there is a cline of increasing species richness from the Arctic to the tropics but it is as yet unclear whether or not a similar relationship occurs in the southern hemisphere. Very high species richness of corals, bivalves (and probably many other taxa) occurs in the Indonesian archipelago. Species richness decreases radially from this area both latitudinally and longitudinally. The deep sea has surprisingly high species richness, which may or may not be higher than coastal areas and thus hypotheses are needed to explain this. The key mechanisms suggested to explain these patterns of species richness are: biological interactions, area, energy-productivity, species ranges (Rapoport’s Rule, Stevens 1989), the random boundary hypothesis, and historical (evolutionary) factors.

These seemingly opposing views, were reconciled by Huston (1979) in his “general hypothesis of species diversity”. However, few testable predictions came from these speculations. It is now widely believed that in terrestrial systems local species richness is largely determined by regional richness rather than by local biological interactions, (Ricklefs, 1987; Cornell, 1999; Loreau, 2000). Cornell and Karlson (1997) have shown for corals that there is indeed a strong correlation between local and regional species richness. I have plotted benthos data for the Norwegian continental shelf and a broadly similar relationship holds (Fig. 1). It is likely then that this relationship is a general one. If so this would imply that studies of biological interactions on local scales do not help understanding mechanisms controlling species richness (Lawton, 1999). The species-area hypothesis Williams (1964) cites a study by H.C. Watson from 1859 showing how in Britain the number of plant species increased as the area sampled increased. This log-log relationship has been found

Biological interactions The role of biological interactions as an explanation for the latitudinal gradient was popular in the 1960s and 1970s. Based on marine data Sanders (1968) suggested that in benign environments species competed with each other and the result was small non-overlapping niches with high numbers of species compared with harsher environments where species had to adapt more to the environment. Sanders used this explanation for the high species richness of the deep sea compared with that of the coasts and for the tropics compared with higher latitudes. However, others (Dayton and Hessler, 1977) argued that the gradient could equally be explained by predation/disturbance. The tropics (and deep sea), it was argued have higher numbers of predators/disturbers and keep prey populations low so that more species can co-occur.

FIG. 1. – Relationship between local and regional species richness for Norwegian continental shelf, data from Gray (1994).

FIG. 2. – Species area relationship for Norwegian continental shelf benthos, data from Gray (1994).

PARADIGMS IN PATTERNS OF MARINE SPECIES 47

to apply to a wide variety of animals and plants. The form of the relationship was first deduced by Frank Preston, (1962), who called it the Arrhenius equation after the Swedish physicist who first derived this equation. The equation S = cAz where S = number of species, A is area and c and z are constants. This equation can be written as log S = z log A +log c, z being the slope of the species-area curve and log c the intercept. It is important to remember that the species-area relationship applies to a variety of scales from small, often less than 1 m2 to very large, thousands of km2. (This relationship should not be confused with “collector’s or species accumulation curves” that are plots of how species accumulate as sample size increases, but over one usually small spatial scale, e.g. species accumulation with successive samples). The species-area relationship over large areas has been shown to be one of the most general found in ecology, (Rosenzweig, 1995). Yet there are few examples of marine data that have been plotted over large areas. Abele and Walters (1979) reanalysed Sanders (1968) data and showed convincingly that a simple species-area relationship following the classical Arrhenius curve held and was sufficient to account for the observed pattern of species richness. They concluded that on the basis of this relationship the deep sea is not extraordinarily species rich nor are estuaries and continental shelves species poor. Furthermore, they argued that there was no need to develop other more complex hypotheses (e.g. the stability-time hypothesis, Sanders 1968) as Occam’s Razor should apply and a simple species-area relationship holds. Rohde (1978) has examined marine parasite data. I have plotted data for the benthos of Norwegian continental shelf and the classical Arrhenius equation holds, (Fig. 2). Thus such a relationship is likely to hold since it is a general rule for terrestrial systems. Rosenzweig (1995) has championed the speciesarea relationship as the simplest explanation clarifying the patterns in species richness found. However, Rohde (1992) suggested that Rosenzweig’s hypothesis, that tropical species richness was the greatest simply because on land the tropics covered the largest area, could not hold as the tropics did not have the largest area in his analysis. Rosenzweig and Sandlin (1997) give a convincing counter-argument, (see also Gaston, 1999). Rosenzweig (1995 p 190) gives three arguments for the increase in number of species with area sampled. First, due to space/niche requirements a large 48 J.S. GRAY

area can contain more species than a small area, second a large area can contain more habitats and hence more species than a small area and third a large area can contain more individuals and therefore more species than a small area. Abele and Walters (1979, Table 2, p. 118) showed that Sanders’ data covered sediments ranging from 22% to 86.3% silt and from 6.5% to 35% clay with organic content varying from 0.33% to 6.7% organic carbon. Clearly Sanders original data on which the paradigms of marine biodiversity were erected were not from a uniform habitat, as claimed for example by Gage (1996), but from different sedimentary habitats. Thus Sanders data may not simply be a question of the different areas of the provinces that his samples represent, but rather that low species richness was found within a single habitat and high species richness is found where several habitats were covered. As yet there are few marine studies that examine the relationship between species richness and habitat heterogeneity in a quantitative way. In Bass Strait, Australia mean sediment grain size ranged from 0.3 to 0.9 mm and is remarkably uniform, yet one 0.1 m2 sample comprised 187 species and 12 out of 38 taken on one occasion comprised more than 100 species (Coleman 1997). Clearly habitat diversity is not essential for high species richness. The third hypothesis proposed to explain the species-area relationship is that larger areas have a greater number of individuals and hence species. With larger numbers of individuals it is suggested that there are lower extinction rates (e.g. birds on British islands, Rosenzweig, 1995). Gray et al. (1998) found no evidence that there are fewer individuals per species in deep sea than in coastal areas. With the exception of this observation there are no marine studies that have tested this hypothesis. Recent terrestrial data (Gaston, 1998) suggests that numbers of individuals increase at a faster rate than the area over which they are distributed. This means that more widely distributed species not only tend to have larger numbers of individuals but also tend to occur at higher local densities. Whether this is also true for marine systems remains to be tested. In relation to the latitudinal gradient and speciesarea Rosenzweig, (1995) makes a much broader suggestion, that tropical terrestrial habitats occupy a greater area compared with higher latitudes and thus from the species-area relationship more species should be found in the tropics. However, Rohde (1997) showed that the area of the tropics is not

greater than that in higher latitudes, thus undermining Rosenzweig’s hypothesis. Rodhe (1997) suggests that in the marine domain the areas of tropics to temperate and high latitudes vary with ocean, but overall there is not a greater area within the tropics. Roy et al. (1998) plotted the area of 5o latitudinal segments against species richness for prosobranch gastropod snails. This study compared species richness collected within latitudinal boundaries from a wide variety of different habitats such as soft sediments, sea-grasses, mangroves, hard substrata and corals for geographical provinces in a comparative manner. Although they claimed that that there was no relationship between area and species richness for the continental shelves of the east and west coasts of N. America, they did not test whether or not there was a species area relationship at different spatial scales over the whole area studied. Overall however, they found that the greatest areas were at high latitudes whereas the greatest species richness occurred between 20o N and 30o N not in the tropics. Lyons and Willig (1999) have developed a scaledependency approach, which allows separation of area and latitude effects on species richness. For bats and marsupials only latitude was significant. Thus again area per se does not seem to be important. In summary species-area relationships have been extremely poorly studied in the marine environment. With so few data explicit tests of the hypotheses proposed by Rosenzweig have not been made. It seems unlikely, however, that the reasons for the extremely high tropical species richness, particularly within the S. China-Indonesia-N. Australia province is related to area. The energy-productivity hypothesis The energy-productivity hypothesis is due to Wright (1983) who extended the species-area hypothesis to encompass energy as a more direct controlling factor on species richness than area alone. Briefly the hypothesis states that the available energy is maximal in the tropics and shows a decline polewards and this gradient is also shown in species richness. The correlates of energy are measures of heat such as mean annual temperature, mean summer temperature, seasurface temperature or evapotranspiration. A number of data sets conform to this theory such as butterflies and birds in the British Isles (Turner et al. 1987, 1988; Fraser and Currie, 1996). Gaston (2000) has recently reviewed this topic.

Roy et al. (1998) found a clear correlation with sea surface temperature, a surrogate for energy input, and thus favour this as an explanation for the latitudinal gradient found in prosobranch molluscs in the northern hemisphere. Yet as Lambshead (1993) points out there may not be a gradient of decreasing productivity from tropics to poles. Primary productivity is closely coupled to secondary production in the tropics so that there is little flux to the seabed. Moving polewards the primary bloom becomes more decoupled from the grazing bloom so that much phytoplankton settles to the seabed. The settlement of material is however, highly patchy and patchiness of food is greatest in polar areas, (Grassle, 1989). This patchiness should over evolutionary time lead to higher, not lower, species richness, (Lambshead, 1993). Rosenzweig (1995) shows clearly that the relationship between species richness and productivity is not linear but shows a maximum at intermediate values of productivity in many different ecological systems. It is well known that in eutrophic marine sediment systems species richness is reduced (Pearson and Rosenberg, 1978). However, again a word of caution eutrophication acts over ecological scales not evolutionary scales. In conclusion explicit tests of the energy-area relationship need to be proposed before any conclusions can be drawn concerning the energy-area hypothesis applied to marine data. The species range hypothesis (Rapoport’s rule, 1982) Rapoport’s rule (Rapoport, 1994) suggests that there is a decrease in species range lengths towards lower latitudes and thus more species are able to coexist. It is claimed that a wide variety of species groups show such a trend, (Stevens, 1989) but there are many data sets that do not follow the rule (see Chown and Gaston 2000 for a review.) Roy et al. (1998) showed that the rule did not hold for prosobranch molluscs since along both coasts median latitudinal ranges of species were greatest, not in high but at low latitudes. Thus there seems to be little general support for Rapoport’s rule with recent data, but see Taylor and Gaines (1999). Random boundary hypothesis A more recent explanation for the latitudinal gradient is a model that assumes no environmental gradients but merely a random association between the size and midpoint of the geographical range of PARADIGMS IN PATTERNS OF MARINE SPECIES 49

species, (Colwell and Hurt, 1994; Colwell and Lees, 2000). A peak of species richness in the tropics is predicted since the latitudinal range of a species is bound to the north and south. The bounds may be physical such as mountain ranges or biological such as critical temperatures or precipitation. A species with a range midpoint midway between the bounds can extend a long way, whereas one near the bound can extend only a limited way. As the tropics have a large area either side of the equator more species are packed within their bounds at low latitudes. Colwell and Lees (2000) present convincing data, but again no studies have been made with marine data. The evolutionary age hypothesis One might expect from first principles that the earth’s geological history was important in determining species richness patterns. There are two key processes that control species richness over evolutionary time, speciation and extinction. It is postulated that speciation rates are higher in tropical regions and decrease polewards, e.g. the comparison between angiosperm species richness in Asia compared with Europe and N. America, (Stenseth, 1984; Latham and Ricklefs, 1993). However, over geological time it is known that 90% of all the species that have ever lived have become extinct. Thus interpreting modern patterns on the basis of geological history is difficult, (Kerr and Currie, 1999). One prediction that can be tested, however, is that the mean ages of taxa should differ among regions of high and low richness. Several authors argue that centres of species richness are also evolutionary centres where new species evolve and from which they then spread to marginal areas. The prediction is then that such areas should have a high proportion of young taxa. Stehli and Wells (1971) compiled data on corals and found that this prediction was upheld. However, Ricklefs and Schluter (1993) proposed that areas of high richness should have old and new taxa whereas marginal areas should only have young taxa since species are colonising these areas. Crame’s (2000) comprehensive analyses of bivalve data shows clearly that speciation rates are higher in tropical areas, but he suggests there is no evidence that extinction rates vary with latitude. There is good evidence that the fauna of the Norwegian Sea has low species richness, high endemism, low affinity with the fauna of the North Atlantic deep basin and low speciation rates (Dahl, 1979; Bouchet and Waren, 1979). This area is geologically young, 2 50 J.S. GRAY

million years, and isolated. Thus evolutionary time is a key variable that needs more consideration in the latitudinal species richness debate. Conclusions on hypotheses for patterns of species richness Research on species richness has in the marine domain has concentrated on describing patterns of species richness. The cline from the Arctic to tropics has been established in the Atlantic and Pacific coast of N. America (Rex et al. 1993; Roy et al. 1996, 1998). Yet we still do not know whether there is a cline of increasing species richness from poles to tropics in the southern hemisphere. Crame’s (2000) study suggests that there is likely to be high richness in the biogeographical provinces in Australia. It is difficult to talk of a cline when there are three continents to consider, Antarctica, Australia and Asia. All of these are old and have been free from glaciation for much longer periods than the Northern hemisphere. It is likely that there will be complex patterns of species richness in the southern hemisphere, as Crame (2000) has suggested. Studies along the coasts of Africa and S. America are urgently needed. There seems little doubt that speciation rates are higher in the tropics and particularly in the epicentre for marine tropical development in the Indonesian archipelago and neighbouring regions. The current view, as exemplified by Crame (2000) is that species are radiating from this region, and this explains the clines of species richness decreasing radially from this region (in a north-south latitudinal and an east-west, longitudinal pattern). As with many hypotheses in ecology they are not mutually exclusive. It is likely that a combination of many factors will prove to be the key to understanding. For terrestrial data the energyproductivity hypothesis is perhaps the one receiving most support. Yet for marine data Roy et al.’s. (1996, 1998) data show that temperature was the best correlated variable. Whether this is a direct physical effect, where higher temperatures are somehow associated with higher speciation rates and/or lower extinction rates or temperature simply correlates with energy/productivity has not been studied.

FUTURE ISSUES The primary focus on marine diversity in recent years has been to estimate how many undiscovered species there are in the deep sea. Grassle and Maci-

olek (1992) estimated 10 million, May (1993) countered with 500,000, whilst Briggs (1993) called Grassle and Maciolek’s estimates “statistical legerdemain”. Lambshead (1995) argued that if meiofauna were to be included the figure was more like 100 million undiscovered species from the deep sea! Grassle and Maciolek’s estimates are no more statistical legerdemain than were Erwin’s (1982, 1988), much quoted and debated, estimates of tropical diversity based on samples of beetles from a few tropical trees. All of us surely agree that we simply do not have enough data on which to make valid estimates of the total number of species that might be found in the deep sea (or on the continental shelves) and more data are urgently needed. It is a sad fact that we know more about the backside of the moon than we do about the bottom of the deep sea! Yet do we know enough about coastal biodiversity? Whereas the deep sea is a relatively uniform habitat covered largely by soft sediments, coasts include coral reefs, mangrove forests, kelp forests, sea-grass meadows, salt marshes, estuaries, intertidal sand and mud flats, rocky inter- and sub-tidal areas and the large expanse of continental shelf sediments, (from where most of the commercial living marine resources are obtained). We have very poor knowledge of the patterns of species richness especially at different spatial scales and from tropical regions. With this large variety of habitats, the world’s coastal zones surely must have higher species richness than the deep oceans. This hypothesis is strengthened by recent data, which suggests that the marine tropical region of the Indonesian archipelago is the centre for speciation in the sea and species are radiating out from this region including the deep sea, (Crame, 2000). Another major argument for devoting more effort to understanding coastal diversity is that the threats to coastal biodiversity from habitat loss and degradation, from fishing (especially trawling), from eutrophication and from introduced species, (Gray, 1997). The threats are many and increasing in magnitude. Thus, the top priority for marine diversity research is to gain more knowledge about coastal diversity and how it best can be conserved. Perhaps the most logical place to begin is with a severely neglected topic that of describing the spatial scales over which species richness and diversity occur. Measurement of the spatial scales of assemblages (from point through sample to large areas and biogeographical provinces Gray, 2000), of habitats and landscapes and how these different scales relate

to species richness are topics that are attracting increasing attention (Thrush, 1996, 1997; Zajac, 1999). A variety of new technologies, such as sidescan sonar, acoustic sediment classification systems, digital UW cameras, REMOTS sediment profiler etc. are giving new insights. We need to relate spatial scales of habitats and landscapes to patterns of species richness. Here we need new models for estimation of the total number of species in given areas. Colwell’s Estimates programme (Colwell and Coddington, 1996) is one approach, and there has been an upsurge in interest in models of species abundances (Tokeshi, 1992; Hill, 1997; Smith and Wilson, 1997). Related to this topic is the problem of rareness. Acceptance of the lognormal distribution as a description of the distribution of individuals among species implies that most species are rare, occurring at low abundances per sample unit. A recent study of rarity in Amazonian forest trees documented precisely how hundreds of tropical trees are rare, (Pitman et al., 1999). This study found that 31% of the species were represented by single individuals and of these 45% occurred in only one of the 21 plots studied. Yet the sparse populations were distributed across a wide range of habitats. Thus the results show that tropical trees are not habitat specialists as previously thought. In addition the processes that control the persistence of tree populations within a region operate over much larger spatial scales and longer time periods, (Ricklefs, 2000). Our studies of an extensive data set from the Norwegian continental shelf show that marine data is similar to Pitman’s (Ellingsen, unpubl.) Knowledge of species geographical ranges has provided important information for a variety of new ideas on patterns controlling species diversity. For example, tests of the species : area model and Rapoport’s Rule, relate range size of tropical species to those of higher latitudes. Another aspect of the species : area relationship is whether or not there are positive relationships between range size and speciation and extinction, (Chown and Gaston, 2000). Yet with the exception of the studies of Roy et al. (1996, 1998) on gastropods, Crame (2000) on bivalves and Cornell and Karlson (1997) on corals, there are few marine data covering species ranges. One of the major questions facing biodiversity in general is are all the species in a given assemblage needed for efficient functioning of the system? The suggestion has often been made that most species are rare and contribute little to the overall functionPARADIGMS IN PATTERNS OF MARINE SPECIES 51

ing of the system such as primary production, nutrient regeneration etc. Naeem et al. (1995) and Tilman and Downing (1994) showed in experiments in a laboratory system and in field experiments respectively that terrestrial systems functioned better with more species. The experiments have, however been heavily criticised (Huston, 1997, Grime, 1997) since different species and sizes of organisms were used in the high and low species systems such that they were not comparable. The debate heated up even more with the publication of the results of a large European experiment BIODEPTH, (Hector et al., 1999). The authors claimed that in this study there was an overall log-linear reduction in biomass with loss of species in European grasslands sampled at eight sites. Huston et al. (2000) argued that the results could be explained more simply as a sampling effect. That is that as more species were added to the assemblage it was more likely that one of the new species would be highly productive thus increasing the overall productivity of the plot. Therefore, the major issue is not so much whether or not numbers of species are important for maintenance of system functioning but rather it is which species are present that is important. My personal feeling is that species identity is the key issue rather than numbers of species per se. If this is true then most species are redundant and contribute little to system function. There are surprisingly few marine studies that have tackled this issue, (but see Duarte, 2000). Snelgrove et al. (1997) have reviewed the key ecological processes that are carried out in marine sediments. Primarily microorganisms carry many of these processes, such as carbon, nitrogen and sulphur cycling, out. Determining the interactions between macro- and meiofauna and bacteria over different spatial and temporal scales is a major task. Such experimental studies are only just beginning and need to be linked to structural redundancy. Whether diversity is controlled by local or by regional processes is a major theme of ecological research (Lawton, 1999). Although different levels of community control clearly exist (Latham and Ricklefs, 1997; Silvertown et al., 1999), evidence from diverse systems is now firmly in favour of regional control (Cornell and Lawton, 1992; Caley and Schluter, 1997; Karlson and Cornell, 1999; Cornell, 1999). Cornell and Karlson (1999) studied corals reefs and this is the only marine system that has been explored so far. If Lawton (1999) is correct that it is the regional species pool that determines local species richness then research efforts should be 52 J.S. GRAY

directed at understanding the regional pool, it’s origin and maintenance using genetic tools, rather than concentrating on biological interactions at local scales as has been the marine tradition. Finally marine diversity research must be relevant to the needs of the managers. At a recent meeting of the European Unions Marine Science and Technology (MAST) research programmes in Lisbon, 1998, the Director General for Environmental Research Dr C. Patermann listed what he, as a political manager of research, felt were the key questions for biodiversity. These are: -what are the causes, the rate and the extent of biodiversity loss? -what are the critical thresholds for loss of biodiversity, the relative importance of different species, and the feasible options for both the monetary and non-monetary valuation of biodiversity? -how can society meet the twin objectives of biodiversity preservation and economic utilisation? -what are the trends and scenarios in the evolution of the biological diversity and its interactions with the other ecosystem factors including the human element? Most developed countries are signatories of the Convention on Biodiversity (CBD). In signing they are committed to undertaking inventories of biodiversity and the status of biodiversity. Few countries have done this for their coasts and continental shelf areas. The CBD has talked a lot, but little practical has appeared to help stem the tide of biodiversity loss in coastal and shelf areas. So how can we answer the needs of the politicians and managers as formulated by Patermann and envisaged in the CBD? The causes of biodiversity loss are relatively easy to see. The destruction of coral reefs is well documented and there are few countries that have more than 30% of the mangroves that were present in the 1950’s. Changed sediment loads from rivers, increase from up-river deforestation or decreased caused by damming, have led to huge changes in coastal ecosystems. The development of the tourist industry is also a major factor in coastal habitat destruction. In Europe there are few estuaries that have not been “reclaimed” (i.e. their wetland areas have been destroyed) and coastal “development” is a misnomer for destruction of marine habitats. For large areas of the coast it is relatively easy to document these changes by aerial photography and use of GIS. Subtidally documenting the changes caused by fishing and especially trawling has been done using

video. These show modern beam and otter trawls scraping the sea bed to tens of centimetres deep, leaving behind sediments devoid of rocks and epifauna that were common only a decade or so ago. Off the Canadian coast and along the shelf of Norway the destruction by trawlers of the slow growing and extensive beds of cold-water corals (Lophelia ) is scandalous. Destruction of these habitats almost certainly will lead to negative impacts on fish recruitment, which will require new approaches across a variety of scales from small, a few meters to hundreds of kilometres. In a marine context when lay persons ask us for information on the relative importance of individual species they are usually thinking of seals, birds and fish species. Britain has a total of 193 species of breeding birds, (Rosenzweig, 1995) and with the large number of amateur ornithologists it is a relatively simple to measure change in all the species. This is not so for the marine environment. The coast of Norway has at least 4,500 species of large marine organisms (Brattegard and Holthe, 1997). It is clearly impractical to assess the importance of all of these. Ideas about “keystone” species (Paine, 1974) have changed greatly in recent years. The “classical” examples of a few years ago such as the lobsterurchin-kelp forest system (Mann, 1982) has been shown to be much more complex (Pringle, 1986; Elner and Vadas, 1990). The kelp forest along the coast of northern Norway was decimated over 1,500 km and sea urchin numbers were high. Complex explanations included conservation of seals led to a seal explosion, seals no longer ate catfish, which in turn released urchins from control and they ate the kelp. There was no evidence for this hypothesis and it is now felt that the kelp-urchin link is probably physically controlled, but in a complex way not fully understood, Thus it is generally accepted that there are in fact relatively few clear examples of species which control whole systems, the “keystone” species idea. Conservation of individual species in coastal and continental areas is impractical, save for large species or species where the biology is well known. A more realistic approach is to conserve habitats, since if one conserves the habitat one conserves the species contained therein. The problem is that defining what is a habitat is not a simple task. Whilst we all agree that seagrass beds are different from mangrove forests things are not so straightforward for sediments. Sediments tend to grade one into another with the result that assemblages do the same and there are only

rarely clear boundaries between assemblages. Assemblage and patch dynamics and interactions need to be better understood and modelled. Conservation strategies are usually compromises between what we know and what is practical in a socio-economic context. The dearth of taxonomic expertise for making inventories of marine biodiversity has been stated many times before (Solbrig, 1991). Time is not on our side and we cannot hope to make inventories of all the species that occur in many areas that are threatened. Some success has been had in assessing terrestrial biodiversity using parataxonomists (Oliver and Beattie, 1993). Nonspecialists are trained to distinguish between but not to identify species. Inventories done in this way were accurate enough to make good estimates of the biodiversity of an area. Again these methods have not been tried out in the marine domain, but with the increasing rate of loss of habitats in tropical coastal areas such methods are urgently needed. Another method is to use surrogates for full species inventories, so-called rapid-assessment techniques. A recent example again from terrestrial systems is from data on 47 forests in Uganda (Howard, et al., 1998). Here species inventories were available for many taxa, and the hypothesis was tested that some groups, birds, moths or butterflies could be used to make assessments of which forests or areas of forest should be conserved. Using a simple algorithm it was found that bird species richness alone gave reliable data on which forest conservation strategies could be made. Similar tests are urgently needed in coastal and continental shelf areas, particularly in the tropics. Finally, the value of natural coastal systems, has been assessed by Constanza et al. (1996). Their figures are surprisingly high and although only preliminary estimates, they show that intact systems have high intrinsic value. Whether or not these values are realistic or not will only be borne out by further calculations. There is clearly an urgent need for social and natural scientists to combine to give better assessments of the value of intact biodiversity in coastal systems on local and regional scales. Only when these data are available will we be able to give the politicians the answers they need on the balance between needs for conservation against the pressures for utilisation of coastal systems. One disturbing aspect is that with the globalisation of the world economy the research priorities of most developed countries are directed to wealth creation and provision of new jobs. I believe that it is far more imporPARADIGMS IN PATTERNS OF MARINE SPECIES 53

tant to protect the remaining biodiversity that we have and that wealth protection is far more important than wealth creation. The challenges are there and we know what needs to be done but financial support is lacking and biodiversity is not among the highest priorities for funding. The CBD has moved extremely slowly from its signing and has yet to do anything practical in a co-ordinated way. This will become a lost opportunity unless scientists are prepared to engage more in the policy aspects of biodiversity and its management.

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SCI. MAR., 65 (Suppl. 2): 57-71

SCIENTIA MARINA

2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

Formation and fate of marine snow: small-scale processes with large-scale implications* THOMAS KIØRBOE Danish Institute for Fisheries Research, Kavalergården 6, DK-2920 Charlottenlund. E-mail: [email protected]

SUMMARY: Marine snow aggregates are believed to be the main vehicles for vertical material transport in the ocean. However, aggregates are also sites of elevated heterotrophic activity, which may rather cause enhanced retention of aggregated material in the upper ocean. Small-scale biological-physical interactions govern the formation and fate of marine snow. Aggregates may form by physical coagulation: fluid motion causes collisions between small primary particles (e.g. phytoplankton) that may then stick together to form aggregates with enhanced sinking velocities. Bacteria may subsequently solubilise and remineralise aggregated particles. Because the solubilization rate exceeds the remineralization rate, organic solutes leak out of sinking aggregates. The leaking solutes spread by diffusion and advection and form a chemical trail in the wake of the sinking aggregate that may guide small zooplankters to the aggregate. Also, suspended bacteria may enjoy the elevated concentration of organic solutes in the plume. I explore these small-scale formation and degradation processes by means of models, experiments and field observations. The larger scale implications for the structure and functioning of pelagic food chains of export vs. retention of material will be discussed. Key words: food web structure, coagulation, vertical flux, remineralization, behaviour of heteretrophs.

INTRODUCTION Vertical material fluxes in the ocean are believed to have influence on global climate by eventually leading to net burial of carbon in the seabed and, hence, potentially reduce atmospheric CO2-content. Particles potentially sink, solutes don’t. Thus, vertical material fluxes are primarily due to the sinking of particles. Zooplankton faecal pellets as well as marine snow aggregates are believed to be the main vehicles for vertical material transport in the ocean (Fowler and Knauer 1986). We are therefore interested in the mechanism(s) by which these rapidly sinking particles form, and in the dynamics governing their formation. *Received April 30, 2001. Accepted May 28, 2001.

Marine snow aggregates and faecal pellets are also subject to degradation. Aggregates may disintegrate physically (Alldredge et al., 1990; Milligan and Hill, 1998), and they may be solubilized and remineralized by micro-organisms (Ploug et al., 1999; Smith et al., 1992) and zooplankton (Kiørboe, 2000). Likewise, faecal pellets may leak their contents of solute organics (Urban-Rich, 1999), and be consumed by zooplankters (Gonzales and Smetacek, 1994; Smetacek, 1980). Recent studies suggest that the degradation rates of aggregates and faecal pellets due to these processes can be very high, leading to an efficient retention of limiting elements in the upper ocean (Kiørboe, 2000). We are therefore also interested in exploring the mechanisms that govern large-particle degradation. FORMATION AND FATE OF MARINE SNOW 57

The sinking flux of material out of the euphotic zone, the export production, represents in a broad sense the balance between the formation and degeneration of rapidly sinking particles. However, the sinking flux is not governed by these processes, at least not in a simple fashion. Rather, the sinking of material out of the euphotic zone is governed by the rate at which the matter that limits production (be it nitrogen, phosphorus or iron) becomes available. Considered over sufficiently long time periods, and because mater does not accumulate in the euphotic zone, output (export) balances import. Therefore, the magnitude of the sinking flux is governed by the input of limiting elements to the euphotic zone. The significance of the processes that generate and destroy sinking particles in the euphotic zone is therefore primarily to influence the number of times nutrients are recycled, the magnitude of the pelagic biomass, and the structure of the pelagic food web. In this article I will examine the small-scale processes that govern aggregate formation and degradation. My ambition is to approach a mechanistic understanding of the small-scale biologicalphysical interactions that govern aggregate dynamics. While my focus will be on the small-scale component processes I shall set the scene by first considering the larger-scale pelagic food web context of these processes.

FORMATION AND DEGENERATION OF SINKING PARTICLES AND PELAGIC FOOD WEB STRUCTURE Consider an extremely simple (and simplified) pelagic ecosystem that consists only of phytoplank-

A

ton (Fig. 1a). Limiting elements are made available through turbulent diffusion and entrainment across the pycnocline from below the euphotic zone and are taken up by the growing phytoplankton. The phytoplankton leaves the euphotic zone through aggregation and subsequent sinking. At steady state, the sinking flux balances nutrient input rate. What is the system biomass at steady state? Our constraint that NUp = NDown implies that the concentration of phytoplankton will adjust exactly such that aggregation rate and, hence, sinking flux balances the input rate of limiting elements. Thus, the steady-state concentration of phytoplankton depends on the coagulation rate. Consider next an alternative simplification (Fig. 1b), in which the phytoplankton is grazed by mesozooplankton, and vertical flux occurs only via sedimentation of zooplankton faecal pellets. In this scenario the zooplankton faecal pellet production rate and, hence, grazing rate and zooplankton biomass will at steady state adjust such that it balances the input rate of the limiting element. Note that this will be the case whether there is a microbial loop or not, or whether or not the zooplankton is grazed upon by planktivorous fish. The bottom line is that the zooplankton biomass adjusts to fit the flux, not vice versa (For the purpose of this simple analysis we ignore several complications, e.g., that the zooplankton may be food limited, and that assimilation efficiency may vary with feeding rate). In a more realistic scenario, with two ‘competing’ settling mechanisms, marine snow aggregates and zooplankton faecal pellets, the ‘need’ for zooplankton will be less at steady state (Fig 1c). More generally, with increasing relative importance of settling mechanisms that are alternatives to zooplank-

B

Microbial loop

C

Pycnocline

NUP = NDOWN FIG. 1. – Schematics of euphotic zone pelagic food webs simplified to various extents. The main simplification and assumption made is that the downward flux of limiting elements (NDown) equals the upward transport (NUp) of the same elements if averaged over sufficiently long time. A: The pelagic biota consists of phytoplankton only, and the only sinking vehicle is phytoplankton aggregates. B: Sinking is only by zooplankton faecal pellets. In C sinking is both by aggregates and faecal pellets, and sinking aggregates are also being remineralised within the euphotic zone. See text for further explanation.

58 T. KIØRBOE

FIG. 2. – In situ micrographs of marine snow aggregates. A. Mixed diatom-faecal pellet aggregate. Individual faecal pellets are visible (by courtesy of Alice Alldredge). B. Diatom aggregate. Individual Chaetoceros chains can be seen.

ton faecal pellets, the less is the ‘need’ for zooplankton to drive the vertical flux, and the less the zooplankton biomass will be. In this scenario, thus, zooplankton biomass is determined by the rate at which marine snow form and sink! Finally, in the most realistic scenario considered here we allow remineralization of sinking particles. Remineralization leads to retention of material in the upper ocean and, hence, to either increased zooplankton biomass or aggregate formation rate in order to maintain the balance between in- and output from the euphotic zone. To the extent that remineralization of sinking particles continues below the euphotic zone, the net burial rate of carbon in the deep ocean is reduced. In the past, models of plankton processes have either focussed on aggregation processes –scenario 1– or food web interactions –scenario 2 . In most situations neither provide a complete or even adequate picture. It is only more recently that attempts have been made to combine aggregation and food web models to describe scenario 3 (Jackson, 2001). While the above scenarios and the assumption of steady state may be challenged, the pictures painted here serve to illustrate that aggregation, sinking, and remineralization of sinking particles directly influence the structure of the pelagic food web, the biomass of the plankton biota, and the burial rate of carbon in the deep ocean. The purpose of this article is to describe and discuss the mechanisms and

dynamics of aggregate formation and remineralization within this large context.

MECHANISMS OF MARINE SNOW FORMATION Marine snow aggregates consist of all kinds of primary particles that are glued together in a 3dimensional fractal pattern (Fig. 2): inorganic particles, detritus, phytoplankton, other micro-organisms, feeding webs, exuvia, etc. Aggregates form by a variety of processes and these can be separated in two groups: viz. physical coagulation and zooplankton-mediated aggregation. Physical coagulation Aggregation by physical coagulation requires that primary particles collide by some physical process and stick together upon collision. Coagulation theory dates back to Smoluchowski (1917), but has more recently been applied to describe aggregation of marine particles (McCave, 1984) and, specifically, phytoplankton aggregation (Jackson, 1990; Hill, 1992; Riebesel and Wolf-Gladrow, 1992). Laboratory experiments (Kiørboe et al., 1990; Kiørboe and Hansen 1993, Drapeau et al., 1994), mesocosm experiments (Dam and Drapeau, 1995; Jackson, 1995), and field observations (Kiørboe et al., 1994, 1996, 1998) have all demonFORMATION AND FATE OF MARINE SNOW 59

ing loss rate (Jackson and Lochmann, 1992). If we consider a phytoplankton bloom and ignore all other processes than growth and aggregation (sedimentation), thus resembling scenario 1 in Fig. 1A, then the change in phytoplankton concentration (C) is the difference between the growth and coagulation. Hence, in simplified form (Jackson, 1990):

strated that coagulation theory at times provides an accurate description of phytoplankton aggregate formation (see Kiørboe, 1997). Brownian motion, differences in sinking velocity between particles and fluid shear may all cause primary particles to collide. The collision frequency can be quantified by an encounter rate kernel, β. The encounter rate kernel has units of volume per time and is the imaginary volume of water within which an individual particle will encounter all other particles per unit time (equivalent to a clearance rate). β consists of additive components that are characteristic for each of the individual encounter processes. β is strongly dependent of the size of colliding particles; it scales with particle size to power 1, 2, and 3 for Brownian motion, differential settling and fluid shear, respectively. If we consider a suspension of equally sized particles, such as a phytoplankton bloom dominated by one species, occurring at concentration C, then the collision rate between primary particles becomes βC2 (number of collisions per unit volume and time). If α is the probability that two particles will stick upon collision, then the rate at which aggregates consisting of two particles form is αβC2. After dimers have formed, these may collide with single cells or with one another to form trimers and quadramers, etc, and eventually larger sinking aggregates form. It turns out that, numerically, collisions between single cells by far dominate the process, and that αβC2 is a good first approximation of the aggregation rate and, hence, the sink-

A -2 -1

10

3

10 2 10 1 10 0 10 -1

(2)

The situation described by this very simple model resembles the situation during a spring bloom in temperate neritic waters where zooplankton grazing can be ignored. In fact, the model has successfully been applied to such a situation and describes well both the phytoplankton population dynamics (Eq. 1, Fig. 3a), the steady state concentration of phytoplankton (Eq. 2, see Kiørboe et al., 1994), as well as the temporal variation in sinking fluxes (~αβC2, Fig. 3b). This demonstrates that aggregate formation by physical coagulation may be a quantitatively important process that can account for important properties of pelagic systems including the vertical flux of phytoplankton.

Vertical flux, mg C m d

cells ml -1

10

µ Cˆ = αβ

2000

10 5 4

dC (1) = µC − αβC 2 dt where µ is the specific phytoplankton growth rate of the phytoplankton. At steady state phytoplankton growth will be balanced by aggregation and sedimentation such that

Skeletonema costatum Leptocylindrus danicus Predicted

0

5

10

15

Time, d

20

25

B

Predicted Observed

1500

1000

500

0 0

5

10

15

20

25

Time, d

FIG. 3. – Observed and predicted temporal variation in the population sizes of two species of diatoms (A) and in the vertical flux of phytoplankton (B) in a Danish fjord. Predictions were made using eq. 1 and observations of phytoplankton growth rate, stickiness and ambient fluid shear as well as phytoplankton concentration and sizes. Data from Kiørboe et al. (1994) and Hansen et al. (1995).

60 T. KIØRBOE

FIG. 4. – In situ photographs of a larvacean in its house (A) and of a pteropod (Gleba chordata) with its mucus feeding web (B) (both by courtesy of Alice Alldredge). Both of these zooplankton organisms are sources of marine snow, but the aggregation mechanisms differ. The larvacean strains particles from the ambient water, some of which are retained on an outer coarse filter. Houses with their load of particles are abandoned every few hours and are then marine snow aggregates. Few additional particles are scavenged as the house sinks. In contrast, pteropods collect sinking particles that intercept the blob of mucus secreted by the animal (flux feeding). Abandoned feeding webs are another important source of marine snow.

Zooplankton-mediated aggregation Zooplankton faecal pellets can be considered aggregates of the primary particles that they contain. Zooplankton grazing is therefore an important and well-documented aggregation process that we need not consider in any further detail here. Mucus feeding webs are another source of marine snow (Fig. 4) that can be quantitatively very important (Hansen et al., 1996). Larvaceans in particular seem to be an important source. These animals abandon their mucus houses frequently, and the particle-loaded house is a marine snow aggregate. Because larvaceans can be abundant this type of marine snow may drive the vertical material flux in some situations (e.g. Kiørboe et al., 1996). Recently it has been demonstrated that giant larvaceans, occurring at middepth, may be quantitatively important and account for a substantial fraction of the vertical material flux (Silver et al., 1998). Attachment of small particles to larvacean houses appear mainly to occur while the house is inhabited. The larvacean inside the house draws a water-current through a coarse outer filter on the house, and retains particles for consumption on a finer inner filter. Large particles screened by the outer filter remain attached when the house is abandoned, and some species of larvaceans also ‘store’ their faecal pellets inside the abandoned house. Scav-

enging of additional particles by the sinking house, on the other hand, appears to be of minor importance (Hansen et al., 1996). Fukuda and Koike (2000) suggested yet another zooplankton mediated mechanism of aggregate formation, which may be quantitatively important. They demonstrated how flagellates, Paraphysomona imperforata, that are attached to particles, generate an advective flow towards the host particle by means of their feeding current. Smaller particles entrained in this flow may collide with and subsequently stick to the host particle, hence leading to aggregation. There are likewise some ciliates, e.g. Uronema filificum, that attach to detritus particles and generate strong feeding currents (e.g. Fenchel and Blackburn 1999) that may similarly cause aggregation with smaller particles from the ambient water. In coastal shallow water aggregates may be inhabited by numerous nematodes. Shanks and Walters (1997) described how nematodes residing on aggregates may extend more than half of their body into the surrounding water, with the extending portion thrashing about vigorously. The extending body collects particles from the ambient water and, thus, adds to the host aggregate. Generally some of the protozoans and metazoans residing on aggregates may continuously add new material and, hence, lead to growth of the aggregate. The quantitative importance of this mechanism for aggregate formation remains unknown. FORMATION AND FATE OF MARINE SNOW 61

FIG. 5. – Heterotrophs feeding on aggregates. A: A diatom aggregate of the type shown in Fig. 2B has been colonized by the heterotrophic dinoflagellate Noctiluca scintillans (Tiselius and Kiørboe 1998). The flagellate feeds on the component diatoms, and in this particular situation diatom aggregation rate was exactly balanced by N. scintillans grazing, thus efficiently remeniralizing aggregated material within the upper ocean (Kiørboe et al. 1998). B: Copepods of the genus Oncaea colonize and feed on marine snow (by courtesy of Alice Alldredge).

MECHANISMS OF AGGREGATE DEGRADATION Aggregates formed in the water column are also subject to degradation. Degradation can be due to physical disaggregation due to shear stress that tears aggregates apart (Milligan and Hill, 1998), but this process appears of limited importance at typical turbulent shear rates in the upper ocean (Alldredge et al., 1990). Turbulent shear rather puts an upper limit to the size of aggregates (Jackson et al., 1997). More important for aggregate degradation are biological processes. Aggregates may host a very rich and abundant flora and fauna and appear to be hot spots of heterotrophic activity in the water column (Alldredge and Silver, 1988; Kiørboe 2000). Bacteria colonise and grow on marine snow aggregates. Their activity causes aggregates to solubilise and remineralise, apparently at high rates (Smith et al., 1992; Ploug et al., 1999). Bacteria typically occur on aggregates in concentrations that are 1-many orders of magnitude higher than in the ambient water (Alldredge and Silver, 1988) and they show higher per capita activities than free-living bacteria. Protozoans are also abundant inhabitants of aggregates (Fig. 5a), and they may feed on both bacteria and other particulate components of the aggregate (e.g., Caron, 1987, Tiselius and Kiørboe, 1998). 62 T. KIØRBOE

Mesozooplankters also colonize aggregates and feed on their constituents (Fig. 5b) (Lampitt, 1992; Steinberg et al., 1994; Kiørboe, 2000). Finally, fish and other macrophageous plankters may feed directly on intact aggregates (Larson and Shanks, 1996). These biological processes cause a rapid turnover of aggregated material. Below I first consider the abundance of heterotrophs on aggregates and then provide some estimates of aggregate turnover rates due to their activity. I next explore the mechanisms by which heterotrophs colonize aggregates and finally consider the dynamics of the microbial populations inhabiting aggregate populations.

ABUNDANCE OF HETEROTROPHS ON AGGREGATES Microorganisms: The abundance of microorganisms associated with an aggregate depends on the size of the aggregate, and maybe also on the availability of microbes in the ambient water. The relation between abundance, size and ambient concentration of micro-organisms appears, however, to vary between microbial groups as well as between studies (Fig. 6). I have here compiled studies that report simultaneous measurements of abundances of microorganisms on aggregates and in the ambient

10 7 10 6 10 5 0.01

0.1

1

Encounter volume, ml aggregate -1

10 4 # Flagellates aggregate-1

Flagellates

10 3 10 2 10

1

a = 4.78 b = 2.14 r = 0.54

10 0 0.01

0.1

Encounter volume, ml aggregate -1

10 8 # bacteria aggregate -1

10 3

a = 5.93 b = -0.58 r = 0.10

Bacteria

10 -1

a = 1.52 b = 0.60 r = 0.37

10 1 10 0 10 -1 0.01

0.1 Aggregate radius, cm

1

a = 0.63 b = 0.25 r = 0.088

10 -2 10 -3

0.01

0.1

1

10 2 Flagellates 10 1 10 0 10 -1 10 -2 a = 1.87 b = 2.35 r = 0.49

10 -3 10 -4

10 3 Encounter volume, ml aggregate -1

# ciliates aggregate -1

10 0

0.01

10 3 10 2

10 1

1

Ciliates

Bacteria

10 2

10 2 10 1

0.1

1

0.1 Aggregate radius, cm

1

Ciliater a = 1.47 b = 1.20 r = 0.46

10 0 10 -1 10 -2 10 -3 0.01

FIG. 6. – Abundances of bacteria, flagellates, and ciliates on aggregates collected in situ. In the right columns, abundances have been normalised by ambient concentrations. The normalised abundances (# aggregate-1/# ml-1 = ml aggregate-1) represent the equivalent volume of ambient water that contains the same number of organisms as the aggregate and has here been termed the encounter volume. Regression lines of the form logY=a + b logX, where X is aggregate radius (cm) and Y either absolute or normalised abundance have been shown. Data are derived from Alldredge et al. (1986), Davol and Silver (1986), Silver et al. (1978),Turley and Mackie (1984), and Zimmermann-Timm et al. (1998).

water. Bacteria seem to show the most consistent pattern between investigations: there are about 105107 bacteria per aggregate, corresponding to the number of bacteria occurring in about 1 ml of ambient water (encounter volume = 1 ml = number of organisms per aggregate divided by ambient concentration = normalised abundance), and the abundance of bacteria on an aggregate appears to be almost independent of the size of the aggregate.

Other studies find that the number of bacteria increases slightly with aggregate size. Both Kiørboe (2000) and Alldredge and Gotschalk (1990) found that bacterial abundances scale with aggregate radius raised to a power of about 3/4. The abundance of flagellates on aggregates varies substantially between studies. Flagellates can be either more or less enriched on aggregates than bacteria. However, overall flagellate abundance increases with aggreFORMATION AND FATE OF MARINE SNOW 63

gate size, and considering all the studies together suggests that flagellate abundance scales with aggregate radius squared. Finally, the abundance of ciliates on average increases slightly with the size of an aggregate. The relatively characteristic abundances of microbes on aggregates and characteristic scaling with aggregate size suggest that the microbial populations are subject to some sort of population control. I consider this aspect later. Mesozooplankters: Aggregates are visited or inhabited by numerous meso-zooplankton species that feed on aggregate constituents or on the microbes associated with the aggregate. Some apparently planktonic copepods, e.g. Oncaea spp, appear to be adapted to life on solid surfaces, such as those provided by aggregates, and these copepods may occur abundantly on aggregates. Other numerically important inhabitants include crustacean nauplii. In addition, several invertebrate larvae appear to use aggregates as sinking vehicles when they are ready to metamorphose and settle (Shanks and Carmen, 1997). There are only relatively few quantitative observations on abundances of meso-zooplankters on aggregates because sampling of aggregates with their inhabitant fauna intact requires diving and hand-collection. The available observations suggest that the number of attached meso-zooplankters increases with aggregate size and may reach several hundreds on the largest aggregates (Fig. 7a). If we, as above, normalise with ambient concentrations of organisms a clear scaling emerges: zooplankton abundance increases with the square of aggregate radius (Fig. 7b). The differences in the scaling of

abundances of bacteria, flagellates, ciliates and meso-zooplankters suggest different accumulation mechanisms. We will return to this issue below.

AGGREGATE TURNOVER RATES Leakage of DOM, bacterial remineralization of organic matter, and feeding on aggregated material and other activities by microbes, zooplankton and fish all contribute to aggregate degradation. Here we attempt some numbers. Ploug et al. (1999) and Ploug and Grossart (2000) measured carbon-specific respiration rates due to microorganisms of about 0.1 d-1 in natural and artificially made aggregates. This rate appears size-independent. Ploug and Grossart (2000) found that the microbial metabolism accounted for almost 80 % of the carbon loss rate in aggregates incubated in the laboratory. Others have found that the solubilization of particulate material in aggregates significantly exceeds the microbial remineralization rate and, therefore, that there is a substantial additional loss of material from aggregates in the form of leaking DOM (Cho and Azam, 1988; Smith et al., 1992; Grossart and Simon 1998). Measurements reported by Smith et al. (1992) and Grossart and Simon (1998) suggest specific leakage rates on the order of 0.1-0.2 d-1 (Kiørboe and Thygesen, 2001), which is similar to losses due to microbial respiration. Grazing by colonizing meso-zooplankters may account for additional losses of similar magnitude (Kiørboe, 2000). Grazing on aggregates by fish and macrophageous zooplankters is difficult to estimate

10 2 10

10 5 a = 0.78 b = 1.34 R = 0.71

10 Normalised abundance, -1 ml aggregate

Zooplankton abundance, # aggregate -1

10 3

1

10 0 10 -1

4

a=3.35 b=2.27 R=0.96

10 3 10 2 10 1 10 0 10 -1

10 -2 0.1

0.1

1

1

Aggregate radius, cm FIG. 7. – Absolute and normalised abundances of mesozooplankters on field-collected marine snow aggregates. Data compiled from the literature by Kiørboe (2000).

64 T. KIØRBOE

but is probably relatively minor. Disintegration of marine snow by swimming euphausids (Dilling et al., 2000; Graham et al., 2000) and due to the activity of other zooplankters (Stemmann et al., 2000) may be significant. Disintegration is, of course, different from remineralization, but everything else being equal, disintegration leads to longer residence times and, hence, to further degradation of aggregates. Taken together, the solubilization, grazing, disintegration and other activities of heterotrophic organisms add up to substantial degradation rates of aggregates (cf. also Fig. 5a), particularly in the upper mixed layer, implying that a significant fraction of aggregated material is being remineralized in the upper ocean rather than being exported. For example, a degradation rate of 0.3 d-1 of aggregates sinking at 20 m d-1 implies a degradation rate of 0.015 m-1 (=specific degradation rate/sinking velocity) and that more than 80 % of the organic matter has been remineralized before the aggregate leaves a 50 m deep euphotic zone. Below the euphotic zone, degradation processes continue, albeit presumably at a lower rate, leading to a continuous decline in both the flux and the concentration of particles with depth. Typical decline rates are of order 0.0005 m-1 (Banse, 1990). This would correspond to a sinking velocity of 20 m d-1 and a degradation rate of 0.01 d-1.

COLONIZATION OF AGGREGATES The bacteria and the proto- and mesozooplankters inhabiting marine snow aggregates –or their ancestors– must have colonized the aggregate from the ambient water. There are different possible colonization mechanisms, and colonization can either be active or passive. Active colonization requires some kind of remote detection of aggregates, while passive colonization that the swimming organism randomly bumps into the aggregate and attach. I shall here consider the various potential mechanisms and examine how colonization rate scales with aggregate size. Because of their very different behaviours and perceptive capabilities I will treat microbes (mainly bacteria) and meso-zooplankters separately. Copepods: Many of the zooplankters that colonize marine snow aggregates appear to reside on the aggregate for only a few minutes at the time (Alldredge, 1972; Shanks and Walters, 1997). Presumably they abandon the aggregate once they have filled their guts in order to reduce predation risk. Aggregates are high-risk environments because fish

and other macrophageous planktivores may engulf the intact aggregate with its inhabitants. The high abundances of zooplankters on aggregates and the short residence times imply that encounter rates must be high. This, in turn, implies that zooplankters must be capable of actively colonize aggregates, i.e., detecting aggregates remotely. Kiørboe and Thygesen (2001) argued that copepods, for example, would be unable to use the hydrodynamic disturbance generated by a sinking aggregate because the cue is too weak. However, they should be able to detect aggregates chemically. The bacterial populations residing on aggregates solubilise particulate material faster than they assimilate the solutes and dissolved organics thus leak out of sinking aggregates (Smith et al. 1992). A sinking aggregate therefore paints a chemical trail in its wake (Fig. 8a). Kiørboe and Thygesen (2001) suggested that horizontally swimming copepods may encounter the solute trail behind a sinking aggregate, and follow the trail to find the particle, much the same way that some male copepods encounter and follow pheromone trails of mates (e.g. Tsude and Miller, 1998). The solute distribution around a sinking aggregate can be accurately simulated in the laboratory (Fig. 8b), and some copepods are in fact able to follow amino acid trails generated that way (Fig. 9). Experiments conducted so far have not included copepods of the more relevant genus Oncaea due to difficulties of culturing these animals, but theoretical computations suggest that this encounter mechanism is sufficient to account for observed abundances of copepods on sinking marine snow aggregates (Kiørboe and Thygesen, 2001). Microbes: Passive colonization of aggregates by direct interception of microbes depends on the motility of the microbes and on the scavenging of microorganisms by the sinking aggregate. Each of these processes can by quantified as encounter rate kernels, βi, the imaginary volume of water from which the aggregate ‘collects’ microorganisms per unit time (independent of the mechanism). The kernels from the various encounter mechanisms are additive, such that β = Σβi. The encounter rate kernel for scavenging (differential sinking) is

βscavenging =0.5 πa2U

(3)

where U is the aggregate sinking velocity and a is the radius of the bacteria. Note that the kernel is independent of aggregate size – counterintuitive, yet true. The kernel for motility-colonization depends FORMATION AND FATE OF MARINE SNOW 65

FIG. 8. – The elongated plume of leaking solutes trailing behind a sinking aggregate. A: The mathematical description of the concentration field is based on the assumption of a sinking rigid sphere and involves solving the Navier-Stokes’ and advection-diffusion equations numerically (Kiørboe et al., 2001). B: Physical model has been established in the laboratory by suspending a porous sphere in an upward directed flow. A fluorescent dye is slowly (~ 5 µl min-1) pumped into the sphere and as the dye leaks out of the sphere it visualises the plume of any solute leaking out of the sphere. Sphere dimensions (~ 5 mm diameter) and flow velocities (0.1 cm s-1) are representative of marine snow aggregates.

30 25

Z mm

20 15 10 5 0 -5 10

X

-15

5

mm

-10

0

-5 -5

0 5

-10 -15

10 15

m y m

FIG. 9. – The copepod Temora longicornis tracking amino acid trail. A T. longicornis released in the experimental set-up described in Fig. 8B, where the dye has been replaced by a mixture of amino acids, may encounter the elongated plume and track it to reach the particle. The swimming copepod was filmed simultaneously by two video cameras that viewed the experimental arena at right angles, thus allowing a reconstruction of the 3-dimensional swimming track.

66 T. KIØRBOE

Increasing attractant concentration

FIG. 10. – Chemokinetic behaviour of motile bacteria. A ‘run-tumble’ swimming mode has been described for bacteria and other micro-organisms: straight swimming ‘runs’ are interrupted by ‘tumbles’, where the organism changes to a new, random direction. Such a swimming mode can be characterised as random walk, and the motility quantified by means of a diffusion coefficient. Chemokinetic behaviour may imply that the probability of tumbling decreases if the organism experiences increasing concentration of attractant molecules during a run, and vice versa. Such behaviour will result in a net movement towards the region of high attractant concentration.

on the motility behaviour of the colonizer. We will here consider only the simple case in which the motility can be described as random walk (or biased random walk), which is a good approximation for many micro-organisms. For example, many bacteria swim in a run-and-tumble mode, i.e., they swim in straight lines, ‘runs’, interrupted at random intervals by ‘tumbles’ where they change swimming direction randomly (Fig. 10). For this kind of swimming behaviour, the motility can be quantified by a diffusion coefficient (Berg 1993): v 2τ (4) 6 where v is the swimming velocity and τ the average run length (time). D for bacteria swimming at 100 µm s-1 and tumbling at 1-s intervals is ca. 10-5cm2s-1, which is similar to molecular diffusion. Now the kernel for motility-colonization can be estimated as D

βmotility =4πDrSh

(5)

where r is aggregate radius, and Sh is the Sherwood number. The Sherwood number is the ratio of total to diffusive transport of microorganisms to the aggregate. It is equal to 1 if the aggregate does not move, and > 1 if the aggregate sinks. Kiørboe et al. (2001) estimated Sh numerically and found that a good approximation is Sh = 1 + 0.619Re0.412(ν/D)1/3

(6)

Scavenging, eq. 3 Motility, eq. 5 Chemokinesis, eq. 7

Encounter rate kernel, cm 3 s -1

Chemokinetic behavior of bacteria

where Re (=rU/ν) is the Reynolds number and ν the kinematic viscosity (~10-2 cm2 s-1 for seawater). This relation is only valid for 0.1 < Re < 20 and 30 < Pe < 50000, where the Peclet number Pe = rU/D. A comparison of β-values for the two colonization mechanisms demonstrates that colonization is entirely dominated by motility (Fig. 11), and we can thus ignore scavenging in the following considerations. Many microorganisms, including many bacteria, have chemokinetic swimming behaviour (Mitchell et al., 1996). Some bacteria, for example, modify the duration of the straight runs between tumbles in response to chemical gradients: if the bacterium during a run senses an increasing concentration of attractant molecules, then on average its run length increases. This behaviour leads to the bacteria aggregating in regions of high concentrations of attractant molecules (Fig. 10), such as amino acids. This can be described as biased random walk and may further increase the rate at which microorganisms colonize marine snow: the plume of DOM surrounding the sinking aggregate may guide bacteria with chemosensory capabilities towards the aggregate.

10 -2 10 -3 10 -4 10 -5 10 -6 10 -7 10 -8 10 -9 10 -10 0.01

0.1

1

Aggregate radius, cm FIG. 11. – Encounter rate kernels for various bacterial colonization mechanisms as a function of aggregate size. Scavenging plays an insignificant role, and chemokinetic behaviour does not enhance colonization rates substantially. The main assumptions made regarding the aggregate are that their sinking velocity, U (cm s-1), varies with aggregate radius, r (cm), as U = 0.13r0.26, and that amino acids leak out of sinking aggregates at a rate Q (mol s-1) given by Q = 10-12r1.5 (see Kiørboe et al., 2001 and Kiørboe and Thygesen, 2001). The bacteria are assumed to swim at 100 µm s-1 and tumble at a frequency of 1 s-1. Assumptions regarding chemokinetic behaviour are specified in Kiørboe and Jackson (2001). FORMATION AND FATE OF MARINE SNOW 67

We have simulated colonization rates of bacteria with chemokinetic behaviour assuming a swimming velocity of 100 µm s-1 and a tumbling frequency of 1 s-1 and optimal chemosensory capabilities (Kiørboe and Jackson, 2001). Simulated colonization rate, quantified as an encounter rate kernel, scales with aggregate size as:

βChemokinesis, cm3 s-1 =0.01365rcm1.74

(7)

Chemokinetic behaviour improves colonization rates a little, but not dramatically (Fig. 11). Microorganisms other than bacteria may likewise colonize aggregates because they swim and due to chemosensory behaviour. This can be described in a similar manner. DYNAMICS OF MICROBIAL POPULATIONS ON AGGREGATES The abundance of bacteria, other microorganisms, and small zooplankters scale very differently with aggregate size, suggesting that there are dramatically different accumulation mechanisms. We can distinguish between at least two different components, viz., colonization and population dynamics. For mesozooplankton, only colonization is of importance while for microbes, both colonization and population dynamics are important. Once on the aggregate, the microorganisms grow and are being eaten. If we for simplicity assume that the dynamics of the bacterial population on an aggregate is governed only by bacterial colonization, growth, and by predator-prey interactions between bacteria and flagellates, then we can describe the interactions by a modification of the classical Lotka-Volterra equations: db = βBS + µB − pBF dt (8) dF = aBF − mF dt where B and F are bacterial abundances on the aggregate, Bs (volume-1) is ambient bacterial concentration, β (volume⋅T-1) is the colonization rate as estimated by equation 6 or 7 above, µ(T-1) is the specific growth rate of the bacteria, p is the specific grazing coefficient (T-1) (such that pF is the specific mortality rate of bacteria due to flagellate grazing), a(T-1) is p times the growth yield, and m(T-1) is the mortality rate of the flagellates. The steady state solution to these equations is: 68 T. KIØRBOE

m Bˆ = a * aβ BS µ Fˆ = − pm p

(9)

The steady state solution suggests that the numbers of bacteria residing on an aggregate is constant and independent of colonization rate and aggregate size, whereas the flagellate abundance depends on bacterial colonization rate and, hence, increases with aggregate size. While cyclic oscillations of bacterial and flagellate populations may be more likely than steady state, it can be shown that average population sizes equal equilibrium population sizes (cf. Pielou, 1969). These predictions in fact bear some relation to the observation that bacterial abundance is independent –or nearly independent– of aggregate size, while flagellate abundances increase with aggregate size (Fig. 6). Obviously, however, this model is too simple because other groups, such as ciliates, may be quantitatively important grazers on flagellates and possibly bacteria, and because microorganisms other than bacteria may colonize the aggregate. Also, aggregation is a continuous process and this may further complicate scaling relations. Yet, this simple model may be used as a starting point for more elaborate models.

FUTURE WORK I have argued that the balance between sinking and remineralisation rates of aggregates are important for structuring the pelagic food web and in determining pelagic biomasses. The larger the fractional loss rate of limiting elements is, the smaller will the pelagic biomass be –and vice versa, remineralisation of aggregates and retardation of vertical flux help conserve matter in the upper ocean. Heterotrophs are important for degrading aggregates, and bacteria appear to play a central role. Not only do the bacteria contribute directly to aggregate remineralization, but their solubilization of particulate material leads to leakage of DOM, which generates solute signals that attract other bacteria and other heterotrophs, which, in turn, further enhance remineralization rates. Also, the solutes leaking out of sinking aggregates may constitute a quantitatively important source of DOM for free-living bacteria and the solute plume surrounding the sinking aggregate an important growth habitat for bacteria (Kiør-

boe and Jackson, 2001). Thus, it becomes critical to understand both how the abundance and the activity of aggregate-associated bacteria are regulated. Some of the considerations above may be used to guide future observations and experiments that address this question of regulation. For example, we may ask whether local growth or colonisation from ambient water is the most important for the accumulation of bacteria. To address this, we equate the two accumulation terms in Eq. 8, i.e., βBs = µB*, and solve for B* = µ /βBs, the bacterial abundance at which growth is as important as colonization. For example, assuming µ = 2 d-1 and Bs = 106 cm-3 and that β can be described by equation 7, suggests that B* is about 106 for 0.01 cm radius aggregates and increasing to almost 109 for 1 cm aggregates. Since observed bacterial abundances on aggregates are on order 106 aggregate-1 (Fig. 6), this exercise suggests that colonization is more – or much more - important than growth in accounting for bacteria on aggregates. However, not all suspended bacteria are motile, and not all motile bacteria will necessarily colonise an encountered aggregate. For example, Fenchel (2001) found that about 20 % of pelagic bacteria are motile. Bacteria approaching a surface may show exploratory swimming behaviour and decide to leave rather than attach, and some attached bacteria may detach again (own unpublished observations). Therefore, bacterial composition on aggregates differs from that in the ambient water (e.g. Caron et al., 1982), and growth is more important than this analysis suggests. However, the scaling of B* with aggregate size (increases with radius1.74, cf. Eq. 7) demonstrates that we need worry more about colonization processes for large aggregates, and more about growth dynamics for small aggregates when attempting to describe bacterial dynamics on marine aggregates. Obviously, this is a topic area, which needs be addressed experimentally. Bacteria attached to aggregates solubilze particulate material by means of ectoenzymes (Smith et al., 1992). Do the bacteria regulate ectoenzyme production? This would seem sensible, since ectoenzyme production would be cost with no return when the bacteria are in the free-living phase. If they regulate enzyme release, how do they do it? Likewise, how do bacteria decide whether or not to attach to an encountered particle? Chemical communication between bacteria, ‘quorum sensing’, would offer a means for bacteria to regulate their activities. Many bacteria are known to release signal molecules at low rates, and to respond to the concentration of

such molecules (Eberl, 1998). Release of ectoenzymes, for example, would make particularly sense when bacteria are many together on an aggregate and can collaborate in solubilizing particulate material, and quorum sensing has in fact been demonstrated to play such a role in some systems (Givskov et al., 1997). On the other hand bacteria may also compete for space and resources on an aggregate, and chemical warfare between species is another possible means by which bacterial abundances and activities on aggregates are regulated. These kinds of processes may be further complicated by the fact that aggregates sink, because the flow of water past the aggregate may change concentrations of both signal and warfare molecules (cf. Schmidt and Jumars, 2001). While this is all of a somewhat speculative nature my prediction is that there is a very rich research avenue here to explore in the future. And that the study of these key small-scale processes will help us address the larger issues of ocean biogeochemistry in a more competent manner.

ACKNOWLEDGEMENTS I am grateful to the organizers of the 36 EMBS to invite me to present this paper. This work was supported by a grant from the Danish Natural Sciences Research Council (9801393). George Jackson suggested the application of the modified Lotka-Volterra model.

REFERENCES Alldredge, A.L. – 1972. Abandoned larvacean houses: A unique food source in the pelagic environment. Science,177: 885-887. Alldredge, A.L., J.J. Cole and D.A. Caron. – 1986. Production of heterotrophic bacteria inhabiting macroscopic organic aggregates (marine snow) from surface waters. Limnol. Oceanogr., 31: 68-78. Alldredge, A.L. and C. Gotschalk. – 1990. The relative contribution of marine snow of different origins to biological processes in coastal waters. Cont. Shelf Res., 10: 41-58. Alldredge, A.L., T.C. Granata, C.C. Gotschalk et al. – 1990. The physical strength of marine snow and its implications for particle disaggregation in the ocean. Limnol. Oceanogr., 35, 1415-1428. Alldredge, A.L. and M.W. Silver. – 1988. Characteristics, dynamics and significance of marine snow. Prog. Oceanogr., 20: 41-82. Banse, K. – 1990. New views on the degradation and disposition of organic particles as collected by sediment traps in the open sea. Deep-Sea Res., 37: 1177-1195. Berg, H.C. – 1993. Random walks in biology. Princeton University Press, Princeton, 152 pp Caron, D.A. – 1987. Grazing of attached bacteria by heterotrophic microflagellates. Microb. Ecol., 13: 201-218. Caron, D.A., P.G. Davis and J.M. Sieburth. – 1982. Heterotrophic bacteria and bacterivoreous protozoa in oceanic aggregates. Science, 218: 795-797

FORMATION AND FATE OF MARINE SNOW 69

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70 T. KIØRBOE

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for rapid particle dissolution. Nature, 359: 139-141. Steinberg, D.K., M.W. Silver, C.H. Pilskaln, S.L. Coale and J.B. Paduan. – 1994. Midwater zooplankton communities on pelagic detritus (giant larvacean houses) in Monterey Bay, California. Limnol. Oceanogr., 39: 1606-1620. Stemmann, L., M. Picheral and G. Gorsky. – 2000. Diel variation in the vertical distribution of particulate matter (> 0.15 mm) in the NW Mediterranean Sea investigated with the Underwater Video Profiler. Deep-Sea Res I 47(3): 505-531. Tiselius, P. and T. Kiørboe. – 1998. Colonization of diatom aggregates by the dinoflagellate Noctiluca scintillans. Limnol. Oceanogr., 43: 154-159.

Urban-Rich, J. – 1999. Release of dissolved organic carbon from copepod fecal pellets in the Greenland Sea. J. Exp. Mar. Biol. Ecol., 34: 107-124. Turley, C.M. and P.J. Mackie. – 1994. Biogeochemical significance of attached and free-living bacteria and the flux of particles in the NE Atlantic Ocean. Mar. Ecol. Prog. Ser., 115: 191-203. Tsuda, A. and C.B. Miller – 1998. Mate-finding behaviour in Calanus marshallae Frost. Phil. Trans. R. Soc. Lond. B., 353: 713-720 Zimmermann-Timm, H., H. Holst and S. Müller. – 1998. Seasonal dynamics of aggregates and their typical biocoenosis in the Elbe Estuary. Estuaries, 21: 613-621.

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SCIENTIA MARINA

SCI. MAR., 65 (Suppl. 2): 73-84

2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

Conversaciones con Ramón: big questions for the millennium* FRANK B. GOLLEY Institute of Ecology, University of Georgia.

SUMMARY: Ramón Margalef and I have enjoyed many years of conversation about ecology and my remarks will celebrate our relationship. My life has gradually shifted from the hustle of the market place and consumption of money and goods to a academic career devoted to students and ideas. Students ask how they can avoid becoming trivial, how they can contribute to solving the dreadful problems that face human society? Students want to know from me, their senior, what are the big questions of ecological science. That is the motivation for me to think about the challenging questions ecologists are asking today, that may change the subject tomorrow. Key words: philosophy of ecology, ecosystems, evolutionary ecology, hierarchy of systems, Margalef personal remembrance.

INTRODUCTION I became acquainted with Ramón Margalef when I was a graduate student at Michigan State University in the late 1950’s. About this time I received in the mail a reprint of his landmark paper, Information Theory in Ecology (Margalef, 1957). The significance of this paper to our seminar discussions and to our research was that it applied a method, information theory, to express a broad, interacting, holistic point of view in ecology. We had not yet adopted ecosystem thinking. Eugene Odum’s Fundamentals of Ecology had just been published (Odum, 1953) and while this text would change our way of thinking fundamentally we had not yet applied it effectively. Margalef’s information theory showed us a way of thinking systematically about systems and it was connected to other advanced holistic scientific initiatives, such as Norbert Weiner’s Cybernetics ,which I encountered *Received May 5, 2001. Accepted June 4, 2001.

as an undergraduate in the library of Purdue University, and N. Rashevsky’s (1966) papers in the Bulletin of Mathematical Biophysics and the General System Yearbook. Margelef’s ideas was interesting to us mainly because information theory was oriented toward systems in general and to energetics specifically. His own focus was on combinometrics of spatial structure of populations and biodiversity. These issues were less relevant to our studies at that time. But his lectures and conversations with us at Georgia and at ecologist meetings and his latter papers and books were exciting because of his continued interest in synthetic questions. It was an exciting time to be an ecologist. New questions were being raised and many of us were challenged to apply theory from physics, chemistry, biology and the social sciences to answer them. Later, I was fortunate to be asked to coordinate a course on ecology at the Institute of Mediterranean Agronomy of Zaragoza, Spain. Ramón Margalef was the Spanish coordinator of the course and we CONVERSACIONES CON RAMÓN 73

saw each other frequently. Over the years the course evolved and it is now concerned with rural planning and the environment. I still coordinate it, but now with Juan Bellot of the University of Alicante (Golley and Bellot, 2000). In those earlier times I had many conversations with Ramón Margalef. They were always stimulating because both he and I thought analogically, drawing connections from comments and ideas expressed across the table or desk and suggesting universals. At one of these visits, in his office in the university at Barcelona, in the early 1980’s, Ramón commented to me, “Frank, ecology isn’t fun anymore.” This is a rather arresting statement to make and at the time I thought that I understood his meaning but upon reflection I realized that I had not fully appreciated the comment. I had interpreted Ramón’s comment to mean he recognized that the search for universal ecological concepts, derived from physics or other disciplines, was over. Students were no longer intrigued by analogies between toyshops and marine plankton. They were looking for experimental proofs, statistical designs, data and reductionism. The search for universals of the 40’s and 50’s was replaced with a focus on relativity, specificity,and individualism of the 60’s and 70’s. Modernism had become postmodernism. Ecology was affected by these intellectual movements just as were all the other sciences and humanities. By 1980 it was obvious that the grounds upon which we carried out our conversations and did our research were changed and “it wasn’t fun anymore.” While fun related to an intellectual mood, I also feel that the concept of “fun” characterizes Ramón Margelef in a very special and personal way. I see him standing before us at the black board drawing a relationship between X and Y that is entirely unexpected, with a big smile on his face, as we register surprise and then amusement that X’s and Y’s may be connected in such a way. And we all laugh. And then our minds are stimulated to search out similar connections in other contexts. That is fun, all right! It is a kind of fun that is fundamental to intellectual work.

ECOLOGICAL SCIENCE, GROWTH AND CHANGE I want to use this comment of Ramón’s, made to me in a conversation in Barcelona, as a spring board to consider the nature of ecological science. Ramón was responding to a familiar feature of science; its 74 F.B. GOLLEY

capacity and tendency to grow and change. Our activity and the satisfaction we gain from that activity also changes as science grows. The “fun” of the early years, when ecological science began exponential growth, was a real phenomenon and is recalled with pleasure by those who shared in the time in some way. Growth leads to changes, which require new environments to maintain growth or sustain maturity. In this essay I want to explore some of the features of growth and change in ecology and environment in the twentieth century. Hopefully, these interpretations will help us to understand opportunity and challenges facing our science in the new millennium. The first task is to describe the growth of ecology. Science, in general, has been growing continuously from its origins, when we express growth as increase in various quantitative measures, such as the number of practioners, published papers, citations to papers and so on. The historian of science, Henry Menard (1971), comments that “growth can be measured most easily by the increase in the number of scientific journals, all of which are cataloged and available in libraries.” I am grateful to Stew Gillmor, Wesleyan University and Stanford University for drawing my attention to Henry Menard’s publications. Science can be defined as the material that is published in these journals. According to Menard, journals typically contain about ten articles per issue and thus about 120 per year. Price (1961) has shown that about 6 million scientific papers have been published since they were invented in 1665. After an initial startup period of a century, growth of scientific papers has been exponential with a doubling time of 15 years. Of course, there are individual sciences that grow more slowly. Glacial geology is an example (Menard, page 34-35). In this case dynamic growth began in 1837 when Louis Agassiz published on the existence of an ice age in western Europe. By 1858 growth became exponential with a doubling time of ten years, which continued until 1900 when the moraines of repeated glaciation were mapped in North America. Afterwards a slower growth period began with an average doubling time of 27 years. This rate has continued. Menard proposes that the doubling time of scientific papers is connected to other measures of science. For example, each scientific paper is written by a scientist and, again according to Menard, a typical rate of production of papers by a productive scientist is three papers per year. Thus, he calculates one journal is equivalent to the output of about 40

scientists. Since a doubling time of 15 years is equivalent to an annual interest rate of between 4 and 5 percent and the doubling time for the population of the United States is about 50 years or one percent per year compounded, the consequence is that the number of scientists in the population has increased rapidly. More than 87 percent of all scientists that have ever existed are alive today. Obviously this situation cannot continue indefinitely. Menard finds evidence that resources are beginning to be limited and the capacity to support science is slowing down. Clearly, this is the reason for the repeated efforts in the US Congress, Academy of Science and other bodies to stress the importance of adequate funding to maintain science productivity. Complex, growing, modern societies need science to address new associations of problems. These observations of Menard provide a context within which to consider ecological science. Ecology is a relatively small discipline which is usually placed within the biological sciences. In 1980, the National Science Foundation (NSF) of the United States reported on the number of scientists in the country (NSF 80-308). Of a total of 274,000 scientists, 41,000 were biologists, 15,000 agricultural scientists and 53,000 medical scientists. Each of these categories could contain ecologists but probably most ecologists would be included among the biologists. At this time the total number of ecologists was about 6,000. The problem of determining numbers of scientists is definitional. The term “ecology” was coined in 1866 by the German zoologist Ernst Haeckel and published in his textbook on general morphology. Haeckel defined ecology as the study of the relationships between animals and their environment. If we extend this definition to include plants and microbes, it will serve as the general definition of ecology in the current textbooks. The ecologist focusing on the animal, plant or microbe part of the definition is clearly a biologist, as well as an ecologist. His or her explanations of the patterns observed in nature will be grounded in the basic biological subfields of anatomy, morphology, genetics, physiology and behavior. But if the ecologist is concerned with the environment he or she might be a physical scientist, such as a geologist, hydrologist, chemist or geographer. And further, if we consider that organisms and environments may be created and managed by humans, an ecologist might be an agricultural scientist, an environmental designer or other alternative discipline.

In an actual example of this problem, in 1916 when the Ecological Society of America (ESA) held its inaugural meeting, the membership was made up of 88 plant ecologists, 86 animal ecologists, 43 foresters, 39 entomologists, 12 agriculturalists, and 14 marine ecologists of a total of 307 individuals. The formation of this society attracted scientists from a variety of disciplines. This means that the boundaries of the discipline are fuzzy. Rather than create a precise definition for this heterogeneous group, even if the definition is based on the words of Ernst Haeckel, and then use it to interpret man power statistics of a government to estimate the number of ecological scientists, it is probably more accurate to use the membership of the national ecological societies to estimate the size of the population of these scientists. After all, professional societies are voluntary organizations and the membership is usually made up of self identified individuals who are willing to pay dues and participate in the societies business. Fortunately, we have good information on the membership of the Ecological Society of America and the British Ecological Societies, the two largest societies of ecologists in the world and we can use these to determine the growth of the population of ecologists. Ecology became an active scientific field around the turn of the 19th into the 20th century; although, of course, Ernst Haeckel invented the term “ecology” in 1866. The British Ecological Society was the first professional ecology society to be established. It was formed in 1913 and the Ecological Society of America was formed a few years, later in 1916. If we arbitrarily assume that the beginning of ecology was the time of formation of discrete professional societies, that is about 1915, then the first doubling would be expected in 1930 at a doubling rate of 15 years. The second doubling would occur in 1945, the third in 1960, the fourth in 1975 and the fifth in 1990. This theoretical pattern fits the growth of membership of the Ecological Society of America rather closely (Fig. 1). The ESA started with 286 charter members (Burgess, 1977). The first doubling to 600 members occurred in 1930, as expected. But little growth occurred in the next 15 years due to the Great Depression and the Second World War. There was even a slight decline to 546 members at the height of the depression in 1934. After the Second World War ended, growth in members of ESA increased rapidly, reaching 2000 in 1960. This growth rate continued to 1973, when membership reached 5000. Burgess commented that the doubling CONVERSACIONES CON RAMÓN 75

Fig. 1. – Growth in Membership of the Ecological Society of America from its start in 1914 through 1976 (from Burgess, 1977).

time for the ESA during this postwar period ranged from nine to 13 years. At present (1999) the membership of ESA is about 7400, and it has remained at this level for several years. It appears that the ESA has reached maturity and is no longer doubling each 15 years. These data for the ESA may be compared to data for the British Ecological Society (BES) presented by John Sheail in his 75th anniversary history of the BES (Sheail, 1987). In 1913 there were 47 members present at the inaugural meeting of this new society. By 1917 the BES slightly exceeded 100 members. Of course the BES also suffered from the two world

Fig. 2. – Growth in membership of the British Ecological Society, as compared to the Ecological Society of America. ESA is indicated by solid circles and BES by open circles. Note the change in number from the mid1970’s to the present for ESA.

76 F.B. GOLLEY

wars and the depression but by 1957 it had reached 1000 members. Growth was sustained. There were 2000 members in 1968, 3000 in 1975 and 4322 in 1985. The doubling rate of growth of the BES (Figure 2) is somewhat faster than 15 years. Of course the population base of the UK and the USA are quite different and the ESA is about twice as large as the BES. And, unlike the ESA, the BES is continuing to grow in size. These comparisons suggest that Menard’s model of doubling of 15 years fits ecological science rather well. It also shows that the growth process can be impacted by world wars and depressions. Finally, it demonstrates that the rate of growth of professional societies isn’t the same for all societies. One society reaches maturity and stops growing, while another continues growth. Since the total numbers of members are different in the ESA and the BES, we do not know if the BES will reach an asymptotic level of about 8000 members in 2005 and then stop growing. But we will watch for this prediction. Menard makes the point that these observations are not merely academic exercises. Conditions of life for an ecologist during these phases of growth are very different, indeed. Early in the growth period young individuals can contribute directly to development of the theory of the subject and advance rapidly. At maturity individuals may have difficulty becoming recognized at all and it may take many years to obtain the expected rewards. If we could determine where in the growth cycle a subject is, probably we could improve our career decisions. I have set Ramón Margalef’s comments into this context to show that he was making a highly personal comment, in conversation, that reflected his perception of a real phenomenon - the doubling time in science and its impact on practioners. What about the world population of ecologists? We do not have precise data on the size of ecological societies in other countries. Of course, many foreign ecologists are members of the BES and ESA, but financial exchange problems, languages, national loyalties and other factors have caused ecologists to form societies throughout the world. Presumedly all of these will go through a growth cycle similar to the BES and ESA, but many are quite small and financially unstable and for these, growth is problematical. Our estimate of the size of the world population of ecologists is based on two different studies made for purposes of assisting international organizations. The first was a census of tropical ecologists (Yantko

and Golley, 1978) carried out for the International Society of Tropical Ecology, headquartered at Benaras Hindu University, Varanasi, India. Based on over 4000 census forms mailed world-wide, with a return of about 2000 censuses, we determined that the countries with the largest number of tropical ecologists were the USA, Brazil, India, the UK, Australia, France, Colombia, Venezuela, Canada, Japan, Mexico, Germany and Indonesia, in that order. More than 30 responses were received from each of these countries. We did not ask a question about national ecological societies since we were representing an international society but the data showed that tropical ecologists were distributed world-wide, including in small countries with a relatively small science establishment. Many of these scientists carried out research and published in international journals. In an approximate way, the data suggest that at this time about twenty percent of the world ecologists were studying the tropics. A few years later we calculated the numbers of ecologists in each country based on the authorship of ecological papers abstracted in Biological

Abstracts, 1981 to 1982, by BIOSIS (Golley, 1983). We are grateful to BIOSIS for providing us this data set. This survey of publications (Table 1) showed that there were approximately 17,000 ecologists world-wide, with 6000 addresses in the USA, 1500 in the USSR, 1100 in the UK, 1200 in Canada, 700 in Australia, and 500 both in India and in the combined Germanies. The total publications by ecologists was about 10,000 titles annually, where ecology was the primary designation, and 25,000 titles, where ecology was the secondary designation. The publication rate was about two titles per ecologist per year.

INTERPRETATION OF THE GROWTH OF ECOLOGY Interpretation of the growth curve of the ecological societies must be speculative. Hopefully these speculations will stimulate other ecologists to examine the growth of the discipline and describe and explain the patterns more quantitatively. I feel that

TABLE 1. – Number of ecologists by country, derived from data on published papers classed as ecological in Biological Abstracts, 1981-1982. The author acknowledges the generous contribution of BIOSIS in providing the data for this table Algeria Argentina Australia Austria Bangladesh Barbados Belgium Bermuda Botzwana Brazil Bulgaria Burma Burundi Cameroon Canada Chile China Colombia Costa Rica Cuba Czechoslovakia Denmark Dominica Ecuador Egypt Ethiopia Fiji Finland France Fr. Polynesia Germany, East Germany, West Ghana Greece Hong Kong Total

3 27 699 73 28 4 70 1 1 96 50 2 1 1 1,170 50 86 8 17 6 135 73 2 4 32 2 4 147 465 5 90 458 10 18 17

Hungary Iceland India Indonesia Iran Iraq Ireland Israel Italy Ivory Coast Jamaica Japan Kenya Korea, South Kuwait Madagascar Malawi Malaysia Mauritius Mexico Monaco Nauru Netherlands, The New Caledonia New Zealand Niger Nigeria Norway Oman Pakistan Panama Papaa-New Guinea Paraguay Peru Philippines

51 9 510 12 11 13 37 134 212 9 14 930 14 51 12 1 1 33 1 36 4 1 255 2 216 2 34 185 3 23 24 12 2 1 17

Poland Portugal Puerto Rico Rumania St. Christopher Saudi Arabia Senegal Singapore South Africa SW Africa Spain Sri Lanka Sudan Sweden Switzerland Syria Taiwan Tanzania Thailand Trinidad-Tobago Tunisia Turkey Uganda USSR UK USA Upper Volta Venezuela Vietnam Yemen Yugoslavia Zaire Zambia Zimbabwe

286 12 1 23 1 14 13 1 253 3 137 16 2 253 91 1 18 5 21 1 4 12 1 1,512 1,145 5,917 3 30 1 4 52 1 1 16

16,579

CONVERSACIONES CON RAMÓN 77

there are at least four major factors which help explain either the period of exponential growth or the period of maturation in the growth of ecology in the twentieth century. These are intrinsic elements of population increase, change in the resources available to the science, fragmentation of the science, and changes in the theoretical structure of the subject. I will consider each of these factors below. Henry Menard suggests that growth and change in science, represented by social organizations made up of individual scientists, follows the familiar pattern of growth of organismic populations. Ecology textbooks describe the classic pattern in which three phases can be recognized. First, the population becomes established and begins to grow. The rate of growth at this time is slow. Once establishment occurs, the population begins growing rapidly, at its physiological capacity. This period is analogically similar to the period of doubling described by Menard. For the ecologist, it is the period when the population is growing at its intrinsic rate of natural increase. Eventually, the population begins to experience resistance from the environment, resources begin to limit growth, and growth slows. Following the period of growth the population may exceed its carrying capacity and decline to low numbers or go extinct. Or, the population may pulse around the carrying capacity, increasing and then decreasing over time. Or, new resources or new members may become available and start a new growth cycle. A similar pattern occurs for the individual organism, expressed in terms of weight or volume. In this case, there is a set point where genetic information tells the cells when to stop growth. Growth ends and the organism is mature. Menard is suggesting that there is a fundamental process of growth that is generally true of any entity made up of living organisms, including social organizations. I think that this suggestion is accepted in most disciplines in the social sciences (Teitelbaum and Winter, 1989). However, its value is mainly analogical. It does not help us understand change in patterns of growth or differences in growth rates among organizations. The second factor useful to explain growth of science is a change in the resource base supporting growth. Menard deals with this factor extensively. By analogy with natural populations and from a political point of view it is an obvious candidate to be considered. Sustained growth requires increase in the rate of financial support and, because science is highly technical, an increase in scientific laborers. 78 F.B. GOLLEY

Few countries are able to balance financial and manpower requirements with the result that we observe crises of insufficient manpower and migration of scientists from one country to another and excessive production of graduate scientists who can not find a position. But overall, science has been well supported since it began. A sustained rate of doubling numbers of products or producers over centuries of time testifies to this fact. Nevertheless, individual disciplines have grown slowly or not at all. How is resource supply related to the change in the rate of growth for an individual scientific discipline? In the case of ecological science in the United States there is publicly available information that is helpful in understanding patterns of support. Basic ecological science is supported by the National Science Foundation within its Division of Environmental Biology (DEB), in the Program on Biological Oceanography in the Division of Ocean Science and in a few other small programs. Environmental Biology is the main source. In 1980 DEB support of basic ecology was about $25.3 million and in biological oceanography was about $7.5 million (Golley, 1981). In contrast, applied ecology is supported by a variety of agencies, depending upon the problem needing attention. Obviously, the Environmental Protection Agency (EPA), the Department of Energy and the Department of the Interior are important sources for applied ecology. In 1980 the EPA provided 60% of the funds for applied ecology or $90.7 million. During the decade the ratio of applied to basic environmental science support was 4.6 dollar applied support to 1 dollar of basic support. I served as the Director of the Division of Environmental Biology from 1979 to 1981. This time period was an especially significant period because it included the transfer of the presidency from Jimmy Carter, a Democrat, to Ronald Reagen, a Republican and was the end of a decade, labeled the Decade of the Environment. During the 1970’s a number of notable environmental activities took place. These included the United Nations Stockholm Conference on the Human Environment, the formation of the Man and Biosphere Program within UNESCO, in the United States the establishment of the Environmental Protection Agency and the Council for Environmental Quality within the office of the President and the end, in 1974, of the International Biological Program of the International Council of Scientific Unions (ICSU). The decade also saw an outpouring of public interest in the environment and while ecological science was recognized

as directly relevant to solving the environmental problems, the media soon scrambled the meaning of the term “ecology” and confused it with environment and environmentalism. As a consequence, many notable ecologists lamented their fate and even suggested abandoning the word entirely. This explosion of interest in the environment inevitably led to increased support for environmental research and services. For example, in DEB the ecological science support increased 51% in dollars corrected for inflation from 1970 to 1980 (Golley, 1981). However, the rate of increase was not constant over the decade (Table 2). Highest support occurred in 1972 and after 1975 the level of support was essentially constant. Considering the total federal support of basic environmental biology research (not only NSF support shown in Table 2), the increase from 1969 to 1979 was 88% in dollars corrected for inflation. The increase for nonbiological environmental research, that is research on water, atmosphere and earth sciences, during the same period was 173%. For comparison, the budget for all federal research functions increased 20 % in constant dollars from 1970 to 1980. Clearly there was substantially increased support for environmental studies during the 1970’s, although increase in physical and chemical project support was twice that for biological projects. Evaluation of these data in the context of our interest in changing rates of science activity, suggests some potential connections. Ecological science funded by the NSF, the main source of support TABLE 2. – NSF support of ecological and other biological sciences in Systematic Biology, Support of Systematic Collections, Physiological, Cellular and Molecular Biology, Neurobiology and Psychobiology. Constant dollars in millions.

Year

Ecological Science

Other Biological Science

Total Ecological Biological Science as a Science % of Total

l969 l970 l971 l972 l973 l974 1975 l976 l977 l978 l979 l980 l981

9.7 13.8 20.5 30.0 26.1 23.7 25.5 21.1 20.6 l9.3 20.6 20.9 21.7

41.4 40.4 40.9 49.9 49.1 46.6 48.7 45.3 52.5 55.9 56.0 57.9 57.1

51.1 54.2 61.4 79.9 75.2 70.3 74.2 66.4 73.1 75.2 76.6 78.8 78.8

51%

43%

45%

% Increase 1970-1980

19 25 33 38 35 34 34 32 28 26 27 27 28

for ecology, increased during the decade of the environment but the increase was not constant. During the last half of the decade support in dollars corrected for inflation was constant. Further, during the decade there was a bias toward support of the physical aspect of environment in comparison with the biological aspect. Constant funding in an expanding subject area can translate into lower support for graduate students and postdoctorate students, into smaller individual research grants, and delayed maintenance of equipment and facilities. The impact of constant support will be felt years later when students seek jobs and facilities and services have to be rebuilt. There is no way to trace cause and effect in these numbers but the convergence of funding patterns on the change in rate of numbers of ecologists is suggestive of a relationship. The third factor that may be involved in change in the rate of doubling of ecologists could be fragmentation or splintering of the subject. Ecology is a highly diverse subject to begin with. Even in a spatially restricted habitat we might identify a thousand species, all of which play some role in the ecosystem. Beside the intrinsic problem of biodiversity, there has been two distinct fault lines across ecological science. The first involves the division of the subject into aquatic ecological sciences and terrestrial studies. Aquatic ecologists formed their own professional society, the Limnological Society of America in 1936, which was joined in 1948 by the Oceanographic Society of the Pacific to form the American Society of Limnology and Oceanography. Of course, some aquatic scientists are members of both this society and the ESA but the different methods, habitats, problems and approaches result in a deep divide. The second division is that between basic and applied ecology. There has always tended to be a line drawn between those who did hands on work and those who did not work or worked with the mind. In the university this prejudice might be important but overall Americans have respected applied science. A celebrated example of the pure and applied fault line within the ecological society involves the well known University of Illinois ecologist, Victor Shelford. Shelford was concerned that disturbance by humans was impacting many of the sites where ecologists worked. He formed a committee within the ESA, the preservation committee, that considered this problem and proposed that it was essential to purchase and maintain biological reserves and field sites. It was suggested that ESA be the organization to serve this need. The EcologiCONVERSACIONES CON RAMÓN 79

cal Society of America has always been a peculiar professional society. The membership elect the president and its officers annually but the management of the ESA is done through a Council, chaired by the President. Members of the Council are sometimes elected, appointed or are members by the law of the constitution of the society. Members meet once a year at a business meeting to approve the budget and to debate and vote on various proposals placed before them by the officers and Council. While ESA has an office and staff today, in Shelford’s time the day to day activity of the society was carried out by the Secretary, who’s tenure was frequently a number of years. In this kind of structure political power is in the hands of the President , the Secretary and the Council. At the time Shelford’s committee made its proposal there were other powerful ecologists in the leadership of the society who thought that the ESA should focus on scientific research and instruction of graduate students. They were opposed to the preservation committees conservation proposal for solving applied problems. In their minds ecology was a theoretical or basic science, not an applied science. Shelford was not to be detoured and at his own expense he wrote and distributed to the members of ESA a questionnaire asking their opinion about the proposal of the preservation committee and the role of the ESA in conservation. He found that many members supported his position. In this standoff, the President and Council decided to abolish the preservation committee and several other ad hoc committees. The consequence was fragmentation, with Shelford and his supporters in 1946 organizing The Ecologists Union separate from the ESA. The Ecologists Union became the Nature Conservancy in 1950. The Nature Conservancy in 1989 listed more than 535,000 members and 300 corporate associates and managed 1000 nature sanctuaries (Coker, 1991). Differences of opinion, new opportunities in research and training, new ways to solve problems can result in fragmentation of a society or community. Ecologists tend to be private, individual scientists, who are pleased to have a society that manages technical journals and an annual national meeting efficiently and cheaply. They welcome recognition and support but they feel uncomfortable about speculating from their data and experiences in the public arena. They tend to label that sort of thing unrigorous, which is an ecologists term of disparagement. But, ecological societies can rise above the individualist approach. In the BES Sheail (1987, pp 262) says “Through its very existence, the Society had 80 F.B. GOLLEY

denied the high ground to any particular aspect or grouping of ecologists. No matter what prominence was given to a topic or a person at a meeting or in one of the Societies publications, the term of others would assuredly come.” But, of course, the BES is also smaller in size than the ESA and so has not had quite the same problem of numbers of members to manage and service. The fourth factor I want to suggest might play a role in explanation of change in the rate and direction of growth of a science concerns theory. Cohesion is especially strong when a community of scientists are all addressing a single theoretical issue. The community will be in close communication, there will be considerable competition between its members and progress may occur rapidly and unexpectedly. The subject is hot and students and others can be drawn into the subject easily. Ecology has tended not to have many of these hot topics. This is probably because ecology is faced with an enormous diversity of subjects and habitats. Ecology did experience a time of active theoretical concentration from the late 1940’s to the early 1970’s, focused on the ecosystem. This concept was operationalized by Raymond and Eleanor Hall Lindemen in their study of Cedar Bog Lake in Minnesota (Lindeman, 1941 and 1942) a few years after the word was coined by Arthur Tansley (1935). Eugene Odum gave the ecosystem concept the central theoretical position in his textbook, Fundamentals of Ecology (Odum, 1953). Odum’s text had an enormous influence in training ecologist during a period of rapid increase in manpower. It was rewritten in three editions and translated into many languages. Later the ecosystem concept was a central foundational idea for the International Biological Program, the UNESCO Man and Biosphere Program and the Long-term Ecological study projects and it remains an active organizing principle of the science today. The ecosystem concept bridges the gap between living organisms and environment by focusing on the interaction between these entities. That is, the ecosystem concept operationalizes Haeckels’ definition of ecology. It stresses that there is a system of interactions in nature. These systems are fuzzy, in that their boundaries are weakly defined and are changing in space and time. The ecosystems evolve and change because the organisms within them evolve and adapt to environmental factors which are changing for physical reasons. A second theoretical step in modern ecology occurred in 1980 when the Dutch Society of Land-

scape Ecology held the first international congress in Veldhoven, Netherlands (Tjallingii and de Veer, 1982). This meeting brought the concept of landscape ecology to the ecological community in general. The significance of the landscape concept is that it recognizes that the ecosystems studied by ecologists, a lake or a patch of forest, is embedded in a larger scale system called a landscape. The landscape is the environment of the ecosystem. Ecosystem behavior has a significance within the context of the landscape. Landscapes may be treated as entities, that is, a watershed is a landscape, and they may be scaled at multiple levels leading eventually to the planet Earth which is embedded in the Solar System. Thus, the landscape concept leads us to apply the hierarchical theory of Allen and Starr (1982) and O’Neill et al. (1986) to ecosystem theory in a space and time continuum. This is a very significant achievement because it links interactions across multiple scales of space/time. The third theoretical concept that grows out of the ecosystem and landscape concepts involves human ecology. Ecologists tended to ignore humans as subjects of ecological study. Study of humans have been located in the social sciences and not only are ecologist untrained in the social sciences but they tend to think of themselves as natural scientists, as biologists. But if the scale increases so that the study involves entire landscapes then we cannot ignore human activity. Zev Naveh and Arthur Lieberman (1984) termed this the total human ecosystem. As an approach it brings into the research every thing that is relevant to the question being asked. Where human action is important, then human motivation, human technology, human history are all relevant. This approach transforms ecology. It becomes the bridge science that links the natural and social sciences into a single endeavor. Unfortunately it is not clear how we can implement the total human ecosystem concept. Human ecology, which has existed since the 1930’s, at least, has not developed bridge concepts that link across the social sciences. Many people are studying this problem and one finds interested colleagues through the social sciences, in environmental history, cultural anthropology, historical ecology, ecological economics, social ecology, environmental ethics and so on. But a break-through has not occurred. Viewers of the scene have identified other factors causing change in the success of ecological sciences. For example, Francesco Di Castri and Malcolm Hadley (1985, 1986 and 1988), who led and

managed the Man and Biosphere project which was established in 1971, viewed the period of the 1980’s as a time of trouble. They asked, “was ecology a science in crisis? These authors attributed the trends to lack of scientific rigor, a weak predictive capacity and underuse of modern technology. They suggested that causal reasons for the trends were the fragmentation of ecology, proliferation of programs, a contraction of research especially in developing countries, low budgets, lack of recruitment opportunities and the rarity of concerted action between ecologists and planners. One has to take seriously the opinion of colleagues who have ten years experience in managing an international program involving thousand of scientists in every country of the United Nations. The experience of such people far surpasses the experience of most of us. Therefore, it is pleasing that there is so much overlap between our analyses. Where there are differences of opinion, I suspect that they represent the consequences of a change in growth rather than being a cause of the change. I do not think that ecology is a science in crisis. Rather, I suggest that ecology is a science ready for a new takeoff in development.

MILLENNIAL QUESTIONS My remarks so far focus on the trends of growth and change in ecological science. That is, I have presented data which suggest certain patterns in ecology have changed and I have related our interpretation of these changes to the familiar growth curve of the population, and other concepts familiar to all ecologists and social scientists. I showed that the manpower of the ecological sciences based on the membership of the worlds two largest ecological societies, which make up almost one-half of the world’s ecologists, increased exponentially through the twentieth century. But this rate of increase has slowed in the last decades of the century. I then speculated about the cause of such patterns, exploring the intrinsic character of population growth, change in funding the sciences, fragmentation of ecological societies and the role of theory in creating cohesion of a science. I concluded that there are probably multiple reasons for the observed patterns. Now I want to turn and look from the past toward the future. I want to address the question of the application of ecology to the millennial question of our time. I recall being a graduate student living in the forests of western Washington, studying the blackCONVERSACIONES CON RAMÓN 81

tailed deer, in the early 1950’s, and my growing concern about the state of the natural environment. I was introduced to the books of Paul Sears, William Vogt, and Aldo Leopold through the professional requirements for the degree of wildlife biologist at Washington State University. My personal experience of almost ten years of hiking and camping in the eastern deciduous forest of the United States as a young student provided a practical grounding for my concern. Human population growth was out of control and seemed unstoppable. Forests were being clear cut for no other reason than they were there. Rivers were being polluted. I was deeply troubled; clearly conservation and nature protection deserved our concern. Now, fifty years later, my judgment is that we have not had an improvement in the global environment. Indeed, we see an environmental situation that has become more serious over time. All the trends identified earlier have continued over fifty years and the costs to nature and human well-being have mounted. By tripling and quadrupling the numbers of scientists and environmentalists, organization of green political parties, expanded nongovernmental organizations of all types, and expenditures of vast amounts of money these trends have not changed. Of course, for those who want to put a good face on it, one can identify successes. They are enough to justify our whistling in the dark. But an evaluation that takes a holistic perspective, over fifty years, leads me to another conclusion. The problem of environmental deterioration and destruction is increasing everywhere and has become critical in some places. Human habitation of the earth is being compromised. We try to get ahead of the problems, yet they increase around us beyond our capacity to deal with them. What are we to do? The issue is exceptionally complicated, involving history, philosophy, science and culture. In this context it seems unfortunate that the size of the community of ecological scientists may be increasing at a slower rate. But maybe the data are misleading. What is likely is that our definition of ecology has changed, with a continued increase in applied scientists concerned with environmental problems and a lesser rate of increase of basic ecological scientists. For example, at our Institute of Ecology at the University of Georgia I have noted that more students are choosing to do their thesis in applied ecology. This is partly because we have created a Masters program in Conservation and Sus82 F.B. GOLLEY

tainable Development within the Institute and we have reestablished a Service Program, with the purpose of applying ecological knowledge to environmental problems. Further, many students come to our graduate programs having developed a strong experience in applied ecology at the undergraduate level. While we have administratively declared all these students to be ecologists, students continually force us to stretch our definitional boundaries of the discipline as they follow their creativity and research directions. The field is changing rapidly and there is no question that ecology represented by graduate training is different now from what it was ten to fifteen years ago. A second change I consider of special significance for interpretations of the century long trends is the change in theoretical approach in ecology. In the past we were searching for universal theory that would explain many individual cases. Very few so called theories could stand the scrutiny of ecologists. Gradually we recognized that all theoretical development was contingent upon the methods used, the definitions selected, and the local features of biodiversity and habitat. Each species is different from other species, each habitat differs and the environment changes in time creating continually new opportunities for evolution and adaptation of organisms. Just as in human society we have learned that it is counterproductive for us to lump individuals in categorical groupings, so it is essential in ecology to pay attention to the specific local and individual systems of concern. This change in focus brings us closer to the world but it makes our task immensely more immediate and local. In the world of politics and the media simple solutions to problems that can become slogans for advocates of point of view and the identification of leaders who can represent these points of view are important. Our scientific approach doesn’t fit this scenario and ecologists interested in politics must find some middle ground where they simplify and generalize enough to make an argument that is convincing but where they do not ignore the data. This is difficult, as we know.

CONCLUDING REMARKS At the beginning of a new millennium we recognize a state of change in the human species and in the environment that causes our concern. It is not change that is a problem; change is universal. Rather trends move us toward states that are ecologically

problematic. For example, extinction of species is increasing globally. While extinction is a familiar process in nature, the rate of extinction exceeds any known rate in the history of the Earth. Evolution represents unique genetic properties that make organisms fit. Loss of genetic fitness is tragic. Destruction of mature communities and their replacement with plantations or with spontaneous regeneration has increased world-wide. In my country it is difficult to find mature nature anywhere. We no longer have a basis of comparison of natural processes, except for small fragments of nature in marginal places. Our rivers are filled with sediment and toxic substances. These materials accumulate in the river deltas killing the organisms and creating dead zones that are enlarging. Rivers which were a dynamic part of the landscape have become sewer pipes. These trends converge signifying that we are in an environmental crisis, which is already affecting our system through increasing economic costs, social disruption and health problems. Yet, since we are part of nested hierarchical systems, our personal life may be quite comfortable and positive and environmental problems seem remote. It is a good strategy to maintain ones personal space at as high an environmental quality as one can. This strategy will produce health and well being which will buffer one against the trends. If one can combine with a group of like-mind individuals it may be possible to protect a part of the land and create ecologically healthy environments for the group. Experience may stimulate members of the group to train others and to demonstrate how it is possible to work against the trends and transform society and the environment into sustainable systems. It is really a matter of will to study the ecology of place and then live within the constraints of those environments. All of our deliberations turn out to have similar patterns. All are a function of scale. All concern small scale, individual phenomena which are embedded into local, self-defined systems - of science, of nature, of the environment. This is the arena where we can function and have an effect. The hope that we can move up the scale and from some superior position order everyone to function in an environmentally positive way, to discover a principle that is so simple and so convincing that everyone will be motivated to change their way and be transformed, the hope that some God, some leader, or some organization will overcome the complex behaviors of more than six billion people and will create a global village are, in my opinion, all

dreams. Reality and the future is in the hands of each individual. Individuals organized into effective groups, such as societies of ecologists, are important because creativity, which only comes from the individual human mind, can be recognized, supported and extended by the human group. Our challenge is to be creative and to apply our creativity to solving the human environmental problem. One can be optimistic about that opportunity. From one perspective this conclusion is quite amusing. Who would have thought that we might solve problems through focus on details. Clearly, one has to approach the future with a laugh. It is fun, in Ramón Margalef’s language, to grapple with such questions. Probably some unexpected connections will emerge out of the apparent chaotic behavior of the present and we will be able to use these connections to leap ahead or to maintain our balance.

REFERENCES Allen, T.F.H. and T.B. Starr. – 1982. Hierarchy: perspectives for ecological complexity. University of Chicago Press, Chicago. Burgess, R.L. – 1977. The ecological society of America. Historical data and some preliminary analyses. In: F.N. Egerton and R.P. McIntosh (eds.), History of American Ecology, pp 1-24. Arno Press, NY. Coker, R. – 1991. Pioneer ecologist, the life and work of Victor Ernest Shelford, 1877-1968. Smithsonian Institution Press, Washington. Cooley, J.H. and F.B. Golley. – 1983. Trends in Ecological Research for the 1980s. NATO Conference Series. Plenum Press, NY. DiCastri, F. and M. Hadley. – 1985. Enhancing the credibility of ecology: can research be made more comparable and predictive? GeoJournal, 11.4: 321-338. DiCastri, F. and M. Hadley. – 1986. Enhancing the credibility of ecology: is interdisciplinary research for land planning useful? Geojournal, 13.4: 299-325. DiCastri, F. and M. Hadley. – 1988. Enhancing the credibility of ecology: interacting along and across hierarchical scales. Geojournal, 17.1: 5-35. Doherty, J. and A.W. Cooper. – 1990. The short life and early death of the Institute of Ecology: A case in institution building. Bull. Ecol. Soc., 71: 6-17. Golley, F.B. – 1981. Federal support for ecological research. 7pp. unpublished manuscript. Golley, F.B. – 1983. Introduction. In: J.H. Cooley, and F.B. Golley, Trends in ecological research for the 1980’s, pp 1-4. NATO Conference Series. Plenum Press, NY. Golley, F.B. – 1993. A history of the ecosystem concept in ecology. Yale University Press, New Haven. Golley, F.B. and J.A. Bellot – 2000. Rural planning for an environmental systems perspectives. Springer Verlag, New York. Haeckel, E. – 1866. Generelle morphologie der organismen: Allegemeine grundzuge der organischen formenwWissenschaft, mechanisch begrundet durch die von Charles Darwin reformierte descendenz-theorie. 2 vols. Reimer, Berlin. Keller, D.R. and F.B. Golley. – 2000. The philosophy of ecology: from science to synthesis. University of Georgia Press, Athens. Lindeman, R,L. – 1941 Seasonal food-cycle dynamics in a senescent lake. Amer. Midland Naturalist, 26: 636-73. Lindeman, R.L. – 1942. The trophic-dynamic aspect of ecology. Ecology, 23(4): 399-418. Margalef, R. – 1957. Information Theory in Ecology. Mem. Real Acad. Cien. Art. Barcelona, 23: 373-449.

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Menard, H.W. – 1971. Science: growth and change. Harvard University Press, Cambridge, MA. Naveh, Z. and A. Lieberman. – 1984. Landscape ecology: Theory and application. Springer Verlag, New York. NSF 80-308. 1980. National patterns of science and technology resources, 1980. National Science Foundation, Superintendent of Publications, Washington, DC. Odum, E.P. – 1953. Fundamentals of Ecology. Saunders, Philadelphia. O’Neill, R.V., D.L. DeAngelis, J.B. Waide and T.F.H. Allen. – 1986. A Hierarchical Concept of Ecosystems. Princeton University Press, Princeton. Price, Derek de Solla. – 1961. Science since Babylon. Yale University Press, New Haven. Rashevsky, N. – 1966. Physics, biology and sociology: a reappraisal. Bull. Mathem. Biophys. 28: 283-308.

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Sheail, J. – 1987. Seventy-five years in ecology. The British Ecological Society. Blackwell Sci. Publ., Oxford. Tansley, A.G. – 1935. The use and abuse of vegetation concepts and terms. Ecology, 16(3):284-307. Teitelbaum, M.S. and J.M. Winter. – 1989. Population and resources in western intellectual traditions. Cambridge University Press, Cambridge. Tjallingii, S.P. and A.A. de Veer (eds.). – 1982. Perspectives in landscape ecology,. Proceedings of the international congress of the Netherlands society for landscape ecology. PUDOC, Wageningen, Netherlands. Wiener, N. – 1948. Cybernetics: Control and communication in the animal and the machine. Technology Press, Cambridge, MA. Yantko, J.A. and F.B. Golley. – 1973. A census of tropical ecologists. Bioscience, 28(4): 260-264.

SCI. MAR., 65 (Suppl. 2): 85-105

SCIENTIA MARINA

2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

The oceanic fixed nitrogen and nitrous oxide budgets: Moving targets as we enter the anthropocene?* L.A. CODISPOTI1, JAY A. BRANDES2, J.P. CHRISTENSEN3, A.H. DEVOL4, S.W.A. NAQVI5, HANS W. PAERL6 and T. YOSHINARI7 1

Univ. of Maryland Center for Environmental Science, Horn Point Lab., Cambridge, MD, 21613, U.S.A. E-mail: [email protected] 2 University of Texas, Marine Science Institute, 750 Channelview Drive, Port Aransas, TX 78373, U.S.A. 3 Bigelow Laboratory for Ocean Sciences, 180 McKown Point, West Boothbay Harbor, ME 04575, U.S.A. 4 School of Oceanography, University of Washington, Seattle, WA 98195, U.S.A. 5 National Institute of Oceanography, Dona Paula, Goa 403 004, India. 6 Institute of Marine Sciences, Univ. of North Carolina at Chapel Hill, Morehead City, NC, 28557, U.S.A. 7 Wadsworth Center, New York State Dept. of Health, Albany, NY 12201, U.S.A.

SUMMARY: New data force us to raise previous estimates of oceanic denitrification. Our revised estimate of ~ 450 Tg N yr -1 (Tg = 1012 g) produces an oceanic fixed N budget with a large deficit (~ 200 Tg N yr-1) that can be explained only by positing an ocean that has deviated far from a steady-state, the need for a major upwards revision of fixed N inputs, particularly nitrogen fixation, or both. Oceanic denitrification can be significantly altered by small re-distributions of carbon and dissolved oxygen. Since fixed N is a limiting nutrient, uncompensated changes in denitrification affect the ocean’s ability to sequester atmospheric CO2 via the “biological pump”. We have also had to modify our concepts of the oceanic N2O regime to take better account of the extremely high N2O saturations that can arise in productive, low oxygen waters. Recent results from the western Indian Shelf during a period when hypoxic, suboxic and anoxic waters were present produced a maximum surface N2O saturation of > 8000%, a likely consequence of “stop and go” denitrification. The sensitivity of N2O production and consumption to small changes in the oceanic dissolved oxygen distribution and to the “spin-up” phase of denitrification suggests that the oceanic source term for N2O could change rapidly. Key words: Arabian Sea, denitrification, global change, Indian Shelf, nitrogen budget, nitrogen cycle, nitrogen fixation, nitrous oxide, suboxia.

INTRODUCTION The senior author (LAC) was educated in an era when his geological oceanography instructor felt obliged to teach both the pros and cons of continental drift and when El Niño was described as an essentially Peruvian-scale phenomenon. At that time (the 1960s), limitated observations and the principle of parsimony encouraged many to *Received May 10, 2001. Accepted June 4, 2001.

assume an ocean that was in steady-state. Thus, when LAC’s Ph.D. work (Codispoti, 1973; Codispoti and Richards, 1976) in combination with other studies (e.g. Cline, 1973; Devol, 1975) found enough denitrification to bring the oceanic fixed N budget, as it was then understood, into balance, the result was nothing more than expected. After all, many studies assumed a steady-state ocean, and even though we dutifully note our assumptions, their frequent use tends to color our view of how the real world works. A disturbing, present-day

OCEANIC FIXED NITROGEN AND NITROUS OXIDE BUDGETS 85

manifestation of this is the tendency to call mathematical model outputs, “data”. The development of our view of the oceanic N system, to some extent, parallels the journey of the climate change community. When LAC began his career, most students of climate felt that change was slow enough to permit oceanographers to assume a steadystate for the present-day ocean without being ridiculous. Now, we know from studies of ice-cores (e.g. Alley, 1995) that there are modes of significant global climate change that take place over a few years, and that ocean basins have significant ~ annual to decadal variability, driven by El Niño/La Niña cycles, the North Atlantic Oscillation, the Arctic Oscillation (Thompson and Wallace, 1998), the Pacific Decadal Oscillation (Mantua et al.,1997; Stott et al., 2000), etc. If this paper simply documented our “path to enlightenment” it would have little value. It is our opinion, however, that we cannot neglect the oceanic N cycle when we attempt to understand global change. In particular, we hope to show that the following hypotheses are worth testing: 1. Some of the terms in the oceanic N regime are much larger than thought just a few years ago, and this has implications for the ability of the oceanic N cycle to impact atmospheric CO2 and N2O on the sub-1000 year time scale. 2. Key portions of the oceanic N cycle respond dramatically to relatively small environmental changes, including anthropogenic changes. 3. The oceanic fixed N budget is either considerably out of balance or present-day estimates of oceanic nitrogen fixation are much too low, or both. 4. Increasing inputs of nutrients into coastal waters from the atmosphere, groundwater, and runoff, encourage the development of suboxia and anoxia which lead to significant increases in oceanic denitrification and N2O emissions, and 5. Denitrification may make the ocean more Fe limited. Magnuson (1990) describes how short-term environmental observations are embedded in the “invisible present” and cannot be properly interpreted without addressing longer-term change (in his case driven by El Niño/La Niña cycles). With respect to the oceanic fixed N budget and N2O turnover there is an additional and perhaps more significant issue: most studies have occurred during the last ~ 50 years, a time in which human impingements on the environment have become massive enough to cause some authors to coin a new term for the present era, the Anthropocene (e.g. Falkowski et al., 2000; Crutzen 86 L.A. CODISPOTI et al.

and Ramanathan, 2000). Thus, re-casting our results into periodic variations such as El Niño cycles and the North Atlantic Oscillation may be insufficient, as we move out of the relatively constrained climate realm that is described by ice-core data for the last 420,000 years (Falkowski et al., 2000). One thing is certain, we have already intervened massively in the global N2 cycle (Hellemans, 1998; Smil, 1997; Vitousek et al., 1997a and 1997b). For example, anthropogenic nitrogen fixation is now on the order of 140 Tg N yr-1 vs a “natural” biotic terrestrial rate of 90-130 Tg N yr-1 (Galloway et al., 1995), and human activities have caused major increases in the fixed N content of runoff, groundwater and the atmosphere (Capone and Bautista, 1985; Howarth et al., 1996; Krest et al., 2000; Paerl, 1997; Paerl et al., 2000; Spalding and Exner, 1993).

METHODS The methods used to collect most of our data are already described (Codispoti et al., 1991; Friederich et al., 1990; Morrison et al., 1998; Morrison et al., 1999). In addition, the data collected from the R/V T.G. Thompson, during US JGOFS Arabian Sea Cruises (Morrison et al., 1998) are available on the U.S. JGOFS web site (http://www1.whoi.edu). We employ a new method, for estimating local NO3– removals in the Arabian Sea. This method is based on ratios of inorganic N (NO3– + NO2– + NH3) to PO43 – (reactive phosphorus) in waters of the Arabian Sea. Conceptually, this method differs little from the N* concept of Gruber and Sarmiento (1997). We reverse signs for convenience, and our lower N/P ratio and higher residual P value accounts for non-local denitrification signals advected into the Arabian Sea. Partly because of the necessity for highly precise PO43 – data, previous methods for estimating denitrification mediated nitrate removals in the Arabian Sea generally relied on nitrogen, temperature and oxygen (NTO) relationships. These methods give unrealistic values in the surface layers because of atmospheric exchange and phytoplankton processes, and they appear to underestimate the NO3– removals due to denitrification. Our new method is described more fully elsewhere (Uhlenhopp et al., in prep.). Briefly, it is based on Type II linear regressions of PO43– vs inorganic N (NO3–+ NO2–+ NH3) on samples from the Thompson Arabian Sea cruises from depths of 100-1500 db, with oxygen concentrations > 65 µM. The resulting equation is:

tio n

(NO2-)

NO2-

ati

+I

(X)

0

N2

-I

Ni

-II -III Oxidation State

tro

N2O

ge

n

Fi

xa ti

on

Assimilation

on

A simplified view of the oceanic N cycle is shown in Figure 1. This figure shows: 1. assimilatory uptake and reduction of nitrate during photosynthesis and heterotrophic bacterial growth (green arrows), 2. recycling of –III oxidation state N in the upper layers (purple arrows), 3. oxidation back to nitrate via nitrification (magenta arrows), 4. conversion of nitrate to N2 by denitrification (orange arrows), and 5. conversion of N2 to –III oxidation state N by nitrogen fixation (yellow arrow). In the ocean and atmosphere, N2 at the 0 oxidation state is most abundant, followed by nitrate at the +5 state, and then various forms of N at –III (NH3,

+II

NO2-

fic

Oceanic nitrogen cycle

+III

tri

SCIENTIFIC BACKGROUND

+IV

Ni

where, Ndeficit is the estimate of the inorganic N (NO3–+ NO2– + NH3) removed from a water parcel by denitrification, 14.89 = ∆N/∆P (by atoms) as determined by the Type II regression, P = reactive phosphorus (PO43 –), 0.28 is the PO43– intercept at 0 inorganic N, and 0.86 accounts for the reactive P released by the organic material re-mineralized by denitrification assuming that N/P in local organic matter is 14.89, and that consumption of 94.4 NO3– by denitrification releases one PO43– (Richards, 1965; equation 3). We also present some excess N2 values arising from denitrification in the Arabian Sea (total excess N2 minus excess N2 produced elsewhere). These were calculated from N/Ar ratios determined by mass spectroscopy, and are more fully described in Uhlenhopp et al. (in prep.) and in Emerson et al. (1999). Please note the following nomenclature: We use PO43– to denote reactive phosphorus as determined by our autoanalyzer method (SCOR, 1996); for convenience, in writing stoichiometric equations, etc. we use NH3 to represent the sum of NH3 + NH4+ , and we use HS– to represent the sum of H2S, HS– and S2-. Also note that all forms of nitrogen other than elemental N2 are referred to as fixed nitrogen (fixed N), and that we refer to the Eastern Tropical North Pacific and the Eastern Tropical South Pacific as the ETNP and ETSP, respectively.

NO3-

+V

ica

(1)

De nit rif

Ndeficit = (14.89(P-0.28)-N) µM x 0.86,

N 2O

(Y)

Catabolism

(NH3) ORG N

NH3

Assimilation

FIG. 1. – A simplified diagram of the oceanic nitrogen cycle based on an original figure presented by Liu (1979).

organic N). Nitrite (NO2-) builds up to concentrations that can rival –III and +V N under suboxic conditions (Fig. 2). Although present in trace quantities, the N2O produced in the ocean has an important influence on atmospheric chemistry. Figure 1 leaves out some potentially important components about which we know little. These include, two labile components, hydroxylamine (NH2OH) and nitric oxide (NO) at the –I and + II oxidation states. These compounds have received some attention (e.g. Butler and Gordon, 1996; Ward and Zafiriou; 1988), but we lack sufficient data to draw useful conclusions about the relationship of these components to global change. Figure 1 also describes processes that produce and consume N2O, mainly: 1. the first step of nitrification (the –III to +III change) where N2O can be produced either by the break-down of an intermediate during NH3 oxidation to NO2– or through reduction of NO2–, a process that appears to be enhanced at low O2 and high NO2– concentrations (Capone, 1991; Poth and Focht, 1985; Ritchie and Nicholas, 1972; Ostrom et al., 2000), and 2. during denitrification where, depending on conditions, there may be net production or net consumption of N2O. There may be some uptake of N2O during nitrogen fixation (dashed black arrow in Fig. 1) when N2O

OCEANIC FIXED NITROGEN AND NITROUS OXIDE BUDGETS 87

O2 (µM)

Pressure (db)

0

50

100

150

NO3 (µM) -

200

250

0

0

0

500

500

1000

1000

1500

1500

TN 039 TN 043 TN 045 TN 049 TN 050 TN 054

2000

2500

Pressure (db)

0

5

10

20

30

40

50

2000

2500

NDeficit ( µM) -5

10

NO2 (µM)

15

0

20

0

0

500

500

1000

1000

1500

1500

2000

2000

2500

2500

2

4

6

FIG. 2. – Data from station N9 located in the portion of the Arabian Sea that contains suboxic water at depths between ~100-1000 db. Cruises, TN039, 43, 45, 49, 50 and 54 comprise the U.S. Joint Global Ocean Flux Process Study of the Arabian Sea and they cover a complete annual cycle beginning in September 1994 and ending in December 1995. A nitrate (NO3–) minimum and nitrite (NO2–) maximum within the suboxic zone (O2 < 5 µM) signal the presence of enhanced denitrification. The parameter, Ndeficit estimates the conversion of NO3– to N2 by denitrification. The shaded area indicates the extent of the regions where, on average, the maximum concentration of nitrite (NO2–) in the oxygen minimum zone (the secondary nitrite maximum) exceeds 1 µM as described by Naqvi (1991). All concentrations are in µM.

may be reduced to –III N along with N2 (Yamazaki et al., 1987). This effect is probably small because of the high N2/N2O ratio in seawater. Vertical profiles of N2O taken in N “starved” phytoplankton populations suggest no uptake in the absence of nitrogen fixation 88 L.A. CODISPOTI et al.

(Mantoura et al., 1993). Additional sources of N2O have been suggested, including production during assimilatory and dissimilatory reduction of NO3– to NH3 (e.g. Oudot et al., 1990; Tiedje, 1988), but based on existing knowledge, it seems reasonable to assume

that these sources are not important to the topics that we will discuss. In addition to denitrification, loss to the atmosphere is the other major sink for oceanic N2O. Studies of the isotopic composition of N2O (Dore et al., 1998; Kim and Craig, 1993; Yoshinari et al., 1997; Naqvi et al., 1998) present some conundrums suggesting that we still have more to learn about the pathways and intermediates involved in the production of oceanic N2O under varying environmental conditions. While providing a useful overview, Figure 1 is greatly simplified. It omits, for example, direct reactions between reduced S and NO3– that involve dissimilatory reduction of NO3– to NH3 (Einsle et al., 1999). Lately, there has been heightened interest in bacteria (Thioploca, Beggiatoa, Thiomargarita namibiensis) that can store and transport NO3– from overlying waters to sulfide-bearing sediments (e.g. Fossing et al., 1995; Schulz et al., 1999). These bacteria contain giant vacuoles that can store NO3– at concentrations of several hundred mM (Jørgensen and Gallardo, 1999; Fossing et al., 1995; Otte et al., 1999), with a high of ~ 800 mM reported for Thiomargarita namibiensis (Schulz et al., 1999). The vacuoles have been described as “anaerobic lungs” (Jørgensen and Gallardo, 1999), and they enable the bacteria to support chemotrophic growth (Otte et al., 1999) through dissimilatory nitrate reduction or denitrification linked to the oxidation of hydrogen sulfide (HS-). Most of the NO3– appears to be converted to NH3 during this reduction (Jørgensen and Gallardo, 1999; Otte et al., 1999), but the possibility of some N2 production has not been totally excluded. In addition, there are thiosulfate (S2O32-) oxidizing bacteria that are known to produce N2 (e.g. Thiobacillus denitrificans; Stouthamer, 1988). The following important interactions are also not described by Figure 1: Dependence on dissolved O2 concentrations: Nitrogen fixation, denitrification, and production of N2O during nitrification either require or are enhanced by low oxygen concentrations. Specifically, the enzyme system required for nitrogen fixation (nitrogenase) is poisoned by O2 (e.g. Falkowski, 1997; Paerl and Zehr, 2000), denitrification is inhibited at oxygen concentrations >5 µM (see below), and net production of N2O during nitrification increases markedly at low oxygen concentrations (Codispoti et al., 1992; Goreau et al., 1980; Suntharalingam et al., 2000). Interactions with Fe: By removing fixed N from the ocean, denitrification creates a need for addition-

al nitrogen fixation in order to maintain oceanic primary production. Since nitrogen fixation has an Fe requirement ~60 times greater than uptake of NO3– by phytoplankton (e.g. Falkowski, 1997; Raven, 1988), denitrification may make the ocean more Fe limited. While it is true that oxygen minimum zone (OMZ) waters in the Arabian Sea contain Fe concentrations a few nM higher than surrounding waters (Saagar et al., 1989; Witter et al., 2000), the stoichiometries involved (Bruland et al., 1991) suggest that ~20 nM of Fe are required to support enough nitrogen fixation to account for each µM of fixed N removed by denitrification, and fixed N removals in the suboxic portion of the Arabian Sea water column can exceed 20 µM, thereby imposing an Fe requirement of several hundred nM. Indeed, it is not clear whether elevated Fe concentrations seen in suboxic zones are related to the suboxia/denitrification per se, or to other factors such as advection of Fe from anoxic zones. It is clear that Fe concentrations of >100 nM tend to be associated with anoxia not suboxia, and it is possible that NO3– can oxidize Fe II to less soluble Fe III (Murray et al., 1995). Differential C/N ratios: During phytoplankton growth the atomic ratio of N/C uptake is ~ 6.6 (Redfield et al., 1963), but during denitrification (see equations 2-6, below), the ratio (by atoms) of N2 production to C oxidation is 0.2 to >0.5 µM depending on the region) when using respiration estimates based on the activity of the electron transport system (ETS) to calculate denitrification rates. This helped to account for the possibility of NO2– diffusing out of the denitrification

FIG. 5. – Dissolved oxygen and nitrite sections taken in the Arabian Sea during the first U.S. JGOFS Arabian Sea cruise (TN039, Sept.Oct. 1994). Oxygen concentrations were determined by automated Winkler titration and compared with the low-concentration colorimetric method of Broenkow and Cline (1969). Concentrations are in µM.

zone and escaping further reduction (Anderson et al., 1982; Codispoti and Christensen, 1985), but may be too restrictive for the lower portion of the suboxic zone where suboxia and high Ndeficits extend to considerable depths even though NO2– is low (Figs. 5 and 6). Thus, the deep Ndeficits may arise from a combination of local denitrification as well as from the transport of deficits produced elsewhere. Note that the known suboxic zones in today’s ocean comprise only ~0.1% of the total oceanic volume. We know (Table 1) that globally significant denitrification occurs within this volume. It follows, therefore, that small changes in dissolved oxygen distributions and carbon fluxes can have globally significant effects on water column denitrification. Calculations suggest that an additional 5% of primary production added to the suboxic waters in the ETSP could double the denitrification rate, and this calculation was based on old primary productivity data that might be too low (Codispoti, 1989). In addition, Codispoti and Packard (1980) and Codispoti et al. (1986) have described what appear to be globally significant accelerations in denitrification in the ETSP. One of these followed the collapse of the Peruvian anchoveta fishery, and the other was associated with the 1985 La Niña (Codispoti et al., 1986; Codispoti et al., 1988). The sedimentary record provides evidence for globally significant changes in oceanic denitrification over much longer time intervals (Altabet et al., 1995; Ganeshram et al., 1995). We conclude that not only is the oceanic

FIG. 6. – Distributions of NTOdeficit and Ndeficit in the same section shown in Figure 5. Concentrations are in µM. OCEANIC FIXED NITROGEN AND NITROUS OXIDE BUDGETS 93

denitrification regime sensitive to change, but that it does undergo significant change over a wide range of time scales. Based on the traditional concepts of denitrification and the concept of “Redfield ratios”, Richards (1965) suggested the following two possible stoichiometric equations for oceanic denitrification:

The major difference between the two equations involves the fate of organic N. In Equation (3), total N2 production, exceeds NO3– consumption by 17%. Gruber and Sarmiento (1997) present an updated version of Equation (3) based on the elementary composition of surface ocean plankton (upper 400m) suggested by Anderson (1995) in which total N2 production exceeds NO3– consumption by 15%. As we shall show, even Equation (3) appears to greatly underestimate the ratio of N2 produced to NO3– consumed during denitrification, as do updated versions of Richards’ equations presented by Codispoti and Christensen (1985). This is important when estimating denitrification rates based on parameters such as Ndeficit. In the past, estimates of denitrification have assumed that none or only a fraction of the organic N was converted to N2 (e.g. Codispoti and Richards, 1976). Direct estimates of the excess N2 present in suboxic waters of the Arabian Sea (Fig. 7), however, suggest that the actual production of N2 is much higher as do some preliminary excess N2 estimates from the eastern tropical North Pacific (Brandes, 1996). Although Ndeficit gives integrated water column estimates of the nitrate removed by denitrification that are about twice as high as older methods (Fig. 6), integrated water column values of Ndeficit are only about half as large as the estimates of excess N2. Therefore, integrated excess N2 may exceed the older Arabian Sea nitrate deficits by a factor of ~ 4. Equation (3) and its more recent analogues can explain about 15% of the difference between Ndeficit and excess N2, but where does the rest of the N2 come from? One explanation is that denitrification does not follow the traditional stoichiometries that vary only a little between authors (Richards, 1965; Codispoti and Christensen, 1985; Gruber and Sarmiento, 1997). In support of this notion, Van 94 L.A. CODISPOTI et al.

-10 0

0

10

20

30

500

Pressure (db)

(CH2O)106(NH3)16H3PO4 + 84.8 HNO3 = =106 CO2 + 42.4 N2 + 148.4 H2O + 16 NH3 + H3PO4 (2) and (CH2O)106(NH3)16H3PO4 + 94.4 HNO3 = (3) =106 CO2 + 55.2 N2 + 177.2 H2O + H3PO4 .

(µg-atoms L-1) 0

500

1000

1000

1500

1500 NDeficit M-1 NDeficit N-8 Excess N2

2000

2000

FIG. 7. – A comparison of nitrate deficits (Ndeficit) at stations N8 (TN043, 18.25oN, 67.6oE) and M1, TN049 (see Fig. 4) with our ensemble of excess N2 concentrations in the Arabian Sea. Concentrations are in µg-atoms of N L-1 (for Ndeficit, µM = µg-atoms of N L-1).

Mooy et al’s. (in press) results suggest that denitrifying bacteria in the suboxic portion of the ETNP preferentially attack amino acids with a C/N ratio of about 4 (by atoms) vs the ratio of ~6.6 for “Redfieldian” organic matter. Starting with Gruber and Sarmiento’s (1997) stoichiometric equation for denitrification: C106H175O42N16P + 104NO3– = = 4CO2 + 102HCO3– + 60N2 + 36H2O + HPO42– (4) Van Mooy et al. assumed that the organic carbon oxidized by denitrifiers consists of an ideal protein (Anderson, 1995), and they produced the following equation for denitrification: C61H97O20N16 + 60.2NO3– = = 38.1N2 + 60.2HCO3– + 0.8CO2 + 18.4H2O.

(5)

In Equation (5) the total yield of N2 exceeds NO3– depletion by ~27%. In addition, to the extent that this equation is correct in suggesting that there is no accompanying release of PO43-, Ndeficit would underestimate N2 production by another ~15%. Thus, with no release of PO43– we could now account for ~42% of the “extra excess N2”, but we doubt that no PO43– is released. Instead, we will assume that, with preferential use of amino acids by denitrifiers, we can

account for ~35% of the “extra excess N2”. Codispoti and Christensen (1985) suggest that high rates of N2O production during microaerophilic nitrification at the boundaries of suboxic zones could be coupled with reduction to N2 by denitrifiers. This could increase the N2produced/NO3–consumed by another ~3%. In addition, the Arabian Sea, at times, has high nitrogen fixation rates. N/P ratios (by atoms) during nitrogen fixation range from ~57-140 (Gruber and Sarmiento, 1997; Karl et al., 1992) and community N/P ratios under these conditions may be >20 (Naqvi et al., 1986; Karl et al., 1995) vs the canonical Redfield ratio of 16/1 (by atoms). Thus, if a significant portion of the organic matter supplied to the suboxic zone is supported by nitrogen fixation we could account for an additional fraction of the excess N2. Overall, it is plausible to suggest that these revisions to the stoichiometry could yield a contribution of N2 from the oxidation of organic N that is equivalent to ~40% of the contribution from NO3-, but how do we account for the rest? If sediments contribute N2 or precursors of N2 to the water column without a corresponding contribution of PO43 -, a further portion of the discrepancy between Ndeficit and the excess N2 values might be explained. Sedimentary denitrification rate estimates for the Arabian Sea range from ~6-20% of the pelagic rate (Bange et al.; 2000; Uhlenhopp et al., in prep.). A large fraction of this probably occurs in shallow sediments that are in contact with water that can exchange excess N2 with the atmosphere. In addition, although phosphorite deposits are found in margin sediments in contact with low oxygen waters (e.g. Piper and Codispoti, 1975), suggesting that N2 might be released without proportionate P, we (AHD and JAB) have observed anomalously high (and puzzling) releases of P from sediment underlying suboxic waters. For these reasons, we speculate that, at most, only a few % of the “extra excess N2” (not accounted for by Ndeficit) is likely to come from sedimentary denitrification via the “canonical pathway” that involves coupled nitrification-denitrification (e.g. Seitzinger et al., 1993). There may be an important additional source of excess N2 that arises from the interactions between the S and N cycles described earlier. We have already mentioned that Thioploca, Beggiatoa, and Thiomargarita can transport NO3– into HS– bearing environments and gain energy by using the NO3– to oxidize HS-. NH3 is the most likely nitrogeneous end-product, but some N2 may be produced, as noted earlier (e.g. during thiosulfate oxidation by

Thiobacillus denitrificans). One should expect high N/PO43– export ratios from such sediments because these bacteria are using energy from NO3– oxidation of HS– compounds to fuel growth instead of the oxidation of P containing “Redfieldian” organic matter. High rates of NH3 export have been observed from sediments with Thioploca mats off Chile (Farias, 1998), and Thioplaca mats have been observed in the northwest Arabian Sea (Jørgensen and Gallardo, 1999; Levin et al., 1997). If this NH3 is released into suboxic waters, it may be oxidized to N2. We have already mentioned the possibility of microaerophilic production of N2O from this NH3 via nitrification followed by denitrification as suggested by Codispoti and Christensen (1985). Other possibilities are suggested by data from the Black Sea (Fig. 8). Examination of fixed N-gradients in the suboxic zone of the Black Sea (Fig. 8) shows that there is an apparent downwards flux of NO3– into the suboxic zone and an upwards flux of NH3. Thus, the major observed forms of fixed-N enter this zone and appear to disappear! To explain this, it has been hypothesized (Codispoti et al., 1991; Murray et al., 1995) that all forms of inorganic N are converted to N2 in this region. Two possible pathways for these transformations are the “annamox” reaction and reactions facilitated by Mn redox cycling. In the “annamox” reaction, NO2– (produced from NO3-, in our case) oxidizes NH3 with both species being converted to N2. A bacterium that can carry out the “annamox” reaction has recently been isolated from a biofilm (Strous et al., 1999). Several authors have suggested that oxidation of NH3 by NO3– is thermodynamically possible (e.g. Richards, 1965). In the cycle facilitated by Mn redox processes, Mn (II) is oxidized to Mn (III, IV) by NO3– which is reduced to N2, and oxidation of NH3 by Mn (III, IV) also produces N2 (Luther et al., 1997). Vertical PO43 – and HS– profiles from the Black Sea (Fig. 8) provide support for this Mn redox cycle. The complex PO43 – profiles can be explained as follows: 1. a dissolved Fe (II) and Mn (II) flux from the anoxic zone to the suboxic zone, 2. oxidation to Fe (III) and Mn (III, IV) by NO2– and NO3– in the suboxic zone, 3. formation of Fe (III) and Mn (III, IV) containing precipitates that scavenge PO43– creating the PO43– minimum in the suboxic zone, and 4. formation of the PO43– maximum in the upper part of the sulfide zone where the precipitates dissolve (Codispoti et al., 1991a; Murray et al., 1995; Spencer and Brewer, 1971;).

OCEANIC FIXED NITROGEN AND NITROUS OXIDE BUDGETS 95

5NH3 + 3HNO3 → 4N2 + 9H2O

NH3 0

10

20

30

40

50

1.5

2.0

2.5 0

NO2 -

Pressure (db)

0.0 0

0.5

1.0

100

100

200

200

PO4

+ -

NO3 -

NO2 NH3

300

300

-

HS Micro O2 Winkler O2

0

1

2

3

4

5

PO4 0

50

3-

6

7

8

9

10

, NO3 -

100 O2 , HS

150

200

-

FIG. 8. – Continuous vertical profiles of NO3-, NO2-, NH3, PO43-and sulfide (H2S + HS- + S2-) in a pump profile that sampled oxic, suboxic and anoxic portions of the Black Sea’s water column. Discrete Winkler and colorimetric dissolved oxygen concentrations taken with the low-concentration method of Broenkow and Cline (1969) are also included. The shaded area denotes the suboxic zone. Sulfide is essentially zero in this zone, and oxygen concentrations are generally less than 5 µM, although in these data there is one depth within the zone were dissolved oxygen concentrations were ~ 7 µM. The low nitrite (NO2-) concentrations (~0.01-0.02 µM) in the anoxic zone are probably artifacts, The nitrite peak near the bottom of the suboxic zone was often more pronounced than in this pump profile (Codispoti et al., 1991a). These data are from (Friederich et al., 1990). Concentrations are in µM.

Luther et al. (1997) performed laboratory experiments, compared nitrogen cycling in Mn rich and Mn poor sediments, and provided thermodynamic calculations suggesting that such a N2 producing Mn redox cycle is possible. Since it is likely that both Mn (II) and NH3 are released from sediments underlying suboxic waters, we have another mechanism for producing excess N2. Because Mn can be re-cycled it functions like a catalyst. Thus, we can write the same stoichiometric equation for both the annamox reaction and the Mn-NH3- NO3– redox cycle: 96 L.A. CODISPOTI et al.

(6)

For this reaction, the total N2 produced exceeds the N2 contributed by NO3– by 167%. Clearly, to the extent that there are fluxes of NH3 that are coupled to energy production from the NO3– - HS– couple and not to remineralization of P-containing organic matter, we have the potential for a reaction that could contribute powerfully to the pool of “extra excess N2” (Fig. 7). We should also note that Luther et al. (1997) point out that oxidation of organic matter by MnO2 produces N2 and that this under-appreciated pathway for N2 production may enhance sedimentary denitrification rates in Mn rich sediments. Lewis and Luther (2000) found elevated Mn concentrations at mid-depths in the Arabian Sea’s suboxic waters suggesting that the catalytic Mn redox cycle may occur there as well. Maximum values were ~8 nM, so the quantitative significance of this process away from the sediments may be small even though the Mn can be recycled. Moreoever, the yield of “extra excess N2” will be smaller than suggested in Equation 6 because, at mid-depths, the cycle is likely to be fueled largely by organic matter, not NH3. Farrenkopf et al. (1997a, b) have shown that bacteria can use IO3– to oxidize organic matter and gain a similar amount of free energy as gained from the use of NO3–. This is another process that could produce N2 (from organic N) without consuming NO3–. The bacteria convert IO3– to I-, and Farrenkopf et al. found that maximum I– concentrations in the suboxic waters of the Arabian Sea approach 1 µM. Based on Equation (5) and an oxidation state change from +V to –I, it is possible that IO3– reduction could produce ~ 0.3 µg-atoms of N2, about 3% of the maximum “extra excess N2” values (Fig. 7). Of course, for this process or the water column Mn redox cycle to account for N2 production not already included in Ndeficit, PO43– releases would have to be low. Overall, there are several processes that could contribute to the “extra excess N2”. We believe that these data imply that existing estimates of water column denitrification are too low. The oceanic N2O regime In addition to its importance as an intermediate in the nitrogen cycle, N2O is an important trace gas that is increasing in the atmosphere. Depending on the chosen time frame, N2O (per molecule) has a global warming potential 170 to 310 times greater than CO2 (Manne and Richels, 2001). It adds several percent

to the greenhouse effect under present-day conditions and plays a role in the destruction of stratospheric ozone (Andreae and Crutzen, 1997; Nevison and Holland, 1997). The ocean is a net source of N2O to the atmosphere but there is a wide range in the estimates. A widely accepted value is Nevinson et al.’s (1995) estimate of ~ 4 Tg N yr-1 (Table 1) with a range of 1.2-6.8 Tg N yr-1. Bange et al. (1996) suggest that some estimates did not sufficiently account for high N2O concentrations found in coastal and upwelling regions and estimate the oceanic source, excluding estuaries, as 4.5-7.4 Tg N yr-1. A biologically constrained approach yielded an estimate of ~10.5 Tg N yr-1 for the open ocean and coastal regions (Capone, 1991). Because N2O production and consumption are enhanced at low oxygen concentrations (Codispoti and Christensen, 1985; Codispoti et al., 1992; Goreau et al., 1980; Suntharalingam et al., 2000), the distribution of N2O in the ocean is highly non-uniform. Indeed, the highest and lowest concentrations, can often be found in close proximity with the lowest values occurring in the core of suboxic zones or in anoxic zones and the highest values occurring at the boundaries of suboxic zones (Codispoti et al., 1986; Law and Owens, 1990; Naqvi and Noronha, 1991; Naqvi et al., 2000, Pierotti and Rasmussen, 1980; Yoshinari et al., 1997). Results from the ETSP (Codispoti et al., 1992) and the Arabian Sea (Naqvi et al., 2000) where such conditions exist suggest that N2O saturations in excess of 1000% can be found at the sea surface. Bange et al. (2000), Law and Owens (1990) and Naqvi and Noronha (1991) suggest that this situation leads to globally significant transport of N2O from the Arabian Sea to the atmosphere, despite this region’s small area (~2% of the oceanic total). Recently, Naqvi et al. (2000a) have reported record high N2O concentrations during seasonal development of upwelling and low oxygen conditions over the western Indian shelf. Maximum values were > 500 nM, and the maximum surface value was 436 nM, or 8,250% saturation. Given that open ocean surface N2O saturation values are generally less than 105%, the high surface values observed off Peru and India demonstrate the highly non-linear distribution of oceanic N2O. Although nitrification at low oxygen concentrations could contribute to the high values on the western Indian shelf, Naqvi et al. (2000a) suggest that the major contributor is “stop and go” denitrification. Laboratory experiments, suggest that nitrous oxide reductase is slow to be induced relative to the other enzymes involved in denitrification, and some stud-

ies suggest that it is relatively susceptible to oxygen inhibition (Dendooven and Anderson, 1994; Firestone and Tiedje, 1979). Thus, a portion of the high N2O values found at the boundaries of suboxic zones probably arises from denitrification that is in the “spin-up” phase (Codispoti et al., 1992). In the shallow waters studied by Naqvi et al. (2000a), there were strong gradients, with conditions varying from oxic to anoxic. In addition, meteorological events should have a strong influence on these shallow waters. Thus, the conditions are ripe for “stop and go” denitrification. Naqvi et al. (2000a) suggest that the N2O flux to the atmosphere arising from these conditions is 0.04-0.25 Tg N yr-1. Bange et al. (2000) suggest an average value for the Arabian Sea of 0.4 Tg N yr-1 not including the high N2O values observed by Naqvi et al. (2000a). Considering the wide range of estimates, and as yet undiscovered N2O “hotspots” that may occur during upwelling off Oman, one can speculate that the ~2% of the global oceanic area represented by the Arabian Sea might provide ~ 1 Tg N yr-1 of N2O to the atmosphere under present-day conditions, a significant fraction of the global oceanic total (Table 1). To our knowledge, observations of other seasonal low oxygen zones that develop over other shelves such as the “dead zone” off the mouth of the Mississippi River (Rabalais et al., 2000) have not been examined for their potential impact on oceanic N2O emissions. DISCUSSION Perspective The major goal of this paper is not to provide definitive answers vis a vis the oceanic fixed N budget and N2O cyling, but to suggest that prior studies (including some of our own!) suffer from a rigidity imposed by a tendency to prefer budgets that balance and systems that are in a steady-state. So far, we have suggested that many traditional estimates of the oceanic water-column denitrification rate (including our own) are too low and that prevailing estimates of N2O emissions from the ocean (Table 1) may also be low. We think that our upwards revisions are conservative, but given the present state of knowledge, our revised estimates are speculative. We use them not to provide a rigorous budget, but to show that prevailing budgets (e.g. Codispoti and Christensen, 1985; Table 1) may be misleading and that we might not be asking the right questions.

OCEANIC FIXED NITROGEN AND NITROUS OXIDE BUDGETS 97

An oceanic denitrification rate of > 400 Tg N yr-1? Our data suggest that Ndeficit underestimates the excess N2 burden in the water column by a factor of ~2 (Fig. 7), and that some prior nitrate deficit and denitrification rate estimates based on NTO relationships underestimate the excess N2 burden by a factor of ~4 (Compare Figs. 4 and 7). Similarly, estimates of denitrification based on ETS activities (Codispoti and Packard, 1980; Codispoti et al., 1986; Naqvi and Shailaja, 1993) did not account for the higher ratios of N2 production to NO3– consumption during denitrification suggested by our Arabian Sea data (Fig. 7). In addition, they may have been applied to volumes that were too small due to the assumption that denitrification was important only in suboxic waters with NO2– concentrations > 0.2 -0.5 µM. Although there is a wide range in recent denitrification rate estimates for the Arabian Sea water column (10-44 Tg N yr-1, Uhlenhopp et al., in prep.), for a variety of reasons we believe that a value of ~30 Tg N yr-1 is reasonable for the NO3– consumption portion of the denitrification rate, in agreement with the recent results of Bange et al. (2000). Since water column burdens of excess N2 exceed traditional NTO based nitrate deficit estimates by a factor of 4 (Fig. 7), it might seem reasonable to quadruple the existing estimate of ~ 30 Tg N yr-1 in order to account for the additional sources of N2 that we have discussed. A significant portion of the “extra excess N2”, however, occurs in the deeper portion of the water column where water residence times are likely to be longer. Therefore, for the purposes of this discussion, we will assume that a reasonable estimate for water column denitrification in the Arabian Sea’s “permanently” suboxic portion of the OMZ is twice the “traditional” estimate, or 60 Tg N yr-1. Our prior estimates for the denitrification rate in the suboxic portions of the OMZ in the ETNP and ETSP total ~50 Tg N yr-1 (Codispoti, 1989). The estimate for the ETSP included some transient sites on the margin of the “permanent” suboxic zone (Codispoti and Packard, 1980). Assuming that the methods used to estimate nitrate deficits in the Pacific adequately accounted for NO3– removals, we might expect water column burdens of excess N2 to exceed nitrate deficits by a factor of ~2, a conclusion that is supported by some preliminary excess N2 data from the ETNP (Brandes et al., 1996). We will assume, therefore, that it is conservative to increase our previous estimates of water column denitrification in this region by 50% and to suggest that the 98 L.A. CODISPOTI et al.

true value in today’s ocean is closer to 75 Tg N yr-1. Thus, we arrive at a total rate for the three largest suboxic portions of the oceanic water column of 135 Tg N yr-1 (60 + 75 Tg N yr-1). We must also account for the contributions of the smaller/more transient sites of water column denitrification mentioned earlier. Based on the data in Naqvi et al. (2000a), Naqvi et al. (2000b) have estimated a denitrification rate for the seasonal hypoxic/suboxic/anoxic zones over the western Indian Shelf to be ~ 5 Tg N yr-1. Estimates for similar sites such as one that develops off the mouth of the Mississippi River (Rabalais et al., 2000) are not available, but given the increase in such sites (Malakoff, 1998) in recent decades, it might be conservative to suggest a total denitrification rate of >5 Tg N yr-1, for all such regions. An examination of the size of the suboxic zone off SW Africa (Calvert and Price, 1971) suggests that this region could also contribute several Tg N yr-1 to the overall oceanic water column denitrification rate. Existing water column denitrification estimates for the Baltic Sea, Cariaco Trench and Black Seas total no more than 0.5 Tg N yr-1, (Cline, 1973; Goering et al., 1973; Rönner, 1983) but they must be adjusted upwards for the same reasons that we have adjusted the Pacific and Arabian Sea estimates upwards. In addition, anthropogenic impacts have increased maximum NO3– concentrations in the Black Sea in recent decades and the thickness of the suboxic zone may have increased (Codispoti et al., 1991a; Murray et al., 1989), so the older estimates for the Black Sea could be massive underestimates. All in all, we think it reasonable to suggest that a conservative estimate for the additional sites of oceanic suboxic water column denitrification would be ~10 Tg N yr-1. There is another potential contributor to the oceanic water column denitrification rate about which we know next to nothing, the possibility of denitrification in oxygenated waters and within microenvironments in oxygenated waters (Tsunogai, 1971; Yoshinari and Koike, 1994). Some studies suggest the presence of denitrification in microenvironments (Alldredge and Cohen, 1987; Wolgast et al., 1998), but they do not allow us to scale up to a global rate for oxygenated waters. Remember, however, that the identified water column sites of denitrification comprise only ~0.1% of the total oceanic volume. Thus, an extremely small rate of N2 production in oxygenated waters by any of the processes that we have mentioned could add significantly to the total oceanic water column rate. Laboratory

experiments (Lloyd, et al., 1987) suggest that N2 production by denitrifiers can persist in the presence of oxygen in excess of 100 µM. In addition, the energetics of oxidation of organic matter under oxic conditions by Mn (IV) compares favorably with direct oxidation, and the organic N oxidized by Mn (IV) may be converted to N2 (Froelich et al., 1979; Luther et al., 1998). Overall, it seems that we can conservatively estimate a water column denitrification rate in the present-day ocean of ~150 Tg N yr-1. Middleburg et al. (1996) suggest an oceanic sedimentary denitrification rate between 230-285 Tg N yr-1 based on canonical stoichiometries similar to those that underestimate water column production of N2. This estimate could, therefore, be conservative, particularly, since the potential importance of Mn redox processes to sedimentary production of N2 has not received sufficient attention as noted by Luther et al. (1997). In addition, consideration of the isotopic composition of oceanic NO3– suggests that the sedimentary rate, on average, should exceed the water column production of N2 from NO3– by several times (Brandes, 1996). This argument needs refinement due to the changing nature of our understanding of sources, sinks and pathways, but the essentials are as follows. Oceanic NO3– has a δ15N of ~ +5 ‰ (Sigman et al., 1999), and this value arises from a balance of the inputs and losses. Neglecting the minor terms, the major input is nitrogen fixation, which produces fixed nitrogen with a δ15N of ~ 0‰ (Hoering and Ford, 1960; Minagawa and Wada, 1986), and the major losses are water column and sedimentary denitrification. Water column denitrification, which in most suboxic zones occurs with only partial depletion of the NO3– pool, removes NO3– with a δ15N of ~ -20‰ (Brandes et al., 1998). In contrast, the isotopic fractionation during sedimentary denitrification is small and removes fixed N with a δ15N of ~ 3‰. We will assume that the processes that produce the “extra excess N2” observed in suboxic waters also removes fixed N with a δ15N +3‰. Therefore, for the isotopic composition of the overall denitrification loss to match that of the nitrogen fixation input (~0 ‰), the overall denitrification rate would need to be about 8 times larger than the water column rate of nitrate removal by denitrification (i.e. {6.7x(+3)} + (-20) = 0). One eighth is, of course accounted for by water column conversion of NO3– to N2. Another 1/8 would also come from water column processes since the water column burden of excess N2 values in the suboxic portions of the Arabian Sea (Fig. 7) is about

twice the Ndeficit burden, indicating that processes other than NO3– reduction produce about 1/2 the excess N2. The remaining 3/4 would come from sedimentary denitrification and would amount to 6 x 75 or 450 Tg N yr-1. In addition to the preliminary nature of the isotopic argument, a possible weakness is that it is true only for periods long enough for us to assume a steady-state budget with respect to the δ15N of oceanic NO3–. This may not be the case as we enter the Anthropocene. We employ the isotopic data, at this point, only to demonstrate that they do not contradict the assertion that our selected rate of 300 Tg N yr-1 for sedimentary denitrification (Table 1) could be conservative. How can we reconcile our total denitrification rate for continental shelves and the open ocean of ~ 450 Tg N yr-1 with the other budget terms (Table 1)? Perhaps the simplest explanation is that the presentday oceanic N budget is more or less in balance, but we have underestimated the source terms. We have already adjusted the anthropogenic source terms upwards (Table 1) and noted that the atmospheric anthropogenic DON term and groundwater inputs (e.g. Krest et al., 2000) are poorly documented. Reasonable increases in atmospheric, runoff and groundwater inputs appear, however, to be unlikely to completely balance the budget. If the budget is to be balanced, the oceanic nitrogen fixation term will have to be increased. A conundrum is that even Gruber and Sarmiento’s (1997) estimate for oceanic nitrogen fixation of 125 Tg N yr-1 (Table 1) is high in relation to the results of direct incubations (e.g. Lipshultz and Owens, 1996). Studies of primary production rates in the Arctic are, however, instructive with regard to this type of a discrepancy between rates estimated from incubations and rates estimated from water mass properties. Traditional incubation-based estimates for Arctic primary production are lower than many estimates based on water mass properties (Codispoti et al., 1991b). In the case of the Arctic, the discrepancy arose, in part, because many incubation studies were conducted in the post-bloom period when ice conditions were most favorable to navigation. Since primary productivity events in the Arctic tend to be localized, it is also easy to miss peak events. Water mass properties integrate over time and space and are not as subject to these problems. In addition, most studies of oceanic nitrogen fixation have concentrated on Trichodesmium, yet there are many other species that may have the ability to fix N. Finally, the incubations employed to obtain nitrogen fixation rates are

OCEANIC FIXED NITROGEN AND NITROUS OXIDE BUDGETS 99

highly subject to experimental artifacts (Paerl, 1990; Paerl and Zehr, 2000). We suggest that it is possible that the oceanic nitrogen fixation rate is considerably higher than present estimates. The large deficit (~200 Tg N yr-1) in our revised oceanic fixed-N budget (Table 1) could also arise because all studies bearing on this subject have been made during the climatic transition from the Holocene to the Anthropocene. Thus, our observations were taken from a “moving target”. How do we combine observations taken over several decades if we are in a period of rapid change? In addition, large imbalances are certainly possible during rapid transition. Firstly, there would be effects due to changes in circulation and stratification that are related to climate change, per se. For example, anthropogenic activities may be increasing the frequency of major El Niño/La Niña cycles, and we have already noted that an acceleration of the denitrification rate in the ETSP was noted during the 1985 Niña (Codispoti et al., 1986). Recently, a combination of development and increased hurricane frequency have led to large pulses of fixed N to the North Carolina coastline (Paerl et al., 2000, 2001). We have already mentioned increases in coastal hypoxia/anoxia, and the increase in maximum NO3– concentrations in the Black Sea. In mentioning, the two accelerations of denitrification off Peru, we noted that one followed the collapse of the Peruvian anchoveta fishery (Codispoti and Packard, 1980). We know of no other studies that have attempted to relate fishing pressure to oceanic denitrification rates, but we do know that fishing pressure has massively influenced oceanic ecosystems. Margalef (1974) and Watling and Norse (1998) have, for example, commented on major ecosystem changes arising from bottom trawling. Overall, we believe that more attention must be given to how climate change and more direct anthropogenic impacts alter the oceanic fixed N regime. Our revised budget (Table 1) and a similar budget by Middleburg et al. (1996) produce a much shorter turnover time for oceanic fixed N (Table 2) and a significant reduction in the oceanic biological pump’s ability to sequester atmospheric CO2 because of decreases in fixed N. Multiplying the deficit in our budget by a Redfield C/N ratio of 6.6 (by atoms) gives a ~1.3 1015 g of C yr-1 potential reduction in oceanic new primary production. Given the present state of knowledge, the fixed N deficit in our budget could be much smaller or much larger. It is also likely that these values are changing. Until we better understand how far out of balance anthro100 L.A. CODISPOTI et al.

TABLE 2. – An unauthorized history of minimum turnover time estimates for oceanic fixed-N (Inventory/Total Sink Term) Author(s) Brandt (1899) 1930 estimate quoted by Harvey (1960) Emery, Orr and Rittenburg (1955) Eriksson (1959) Tsunogai & Ikeuchi (1968) Tsunogai (1971) Codispoti (1973) Liu (1979) Codispoti & Christensen (1985) Capone (1991) Codispoti (1995) Middleburg et al. (1996) Gruber and Sarmiento (1997) This paper And going lower???

Years 2 10,000 10,000 10,000 4,000 26,000 8,000 8,000 5,000 3,500 3,000 1,700 – 2,300 3,500 1,500

pogenic activities might drive the oceanic fixed N budget, we cannot neglect its potential influence on atmospheric CO2 concentrations. Potential for change in the oceanic nitrous oxide source term On a per molecule basis, N2O is ~ 200-300 times more powerful than CO2 (Manne and Richels, 2001) as a greenhouse gas, and increases in N2O contribute to the destruction of stratospheric ozone (Nevison and Holland, 1997). Thus, trying to understand how the oceanic source term for N2O may change as we enter the Anthropocene is of more than casual interest. We have revised the prevailing oceanic N2O source term upwards by 2 Tg N yr-1 in our oceanic fixed N budget (Table 1) to account for the expansion of low oxygen conditions in coastal regions (e.g. Naqvi et al., 2000a). Once again, at the present state of knowledge we could argue about whether this revision should be larger or smaller, but to do so misses the more important question of how this term might change. We know that the highest N2O concentrations are found near the boundaries of suboxic waters (Codispoti et al., 1992) and that in the “stop and go” denitrification regime found off the western Indian shelf surface concentrations can achieve saturations in excess of 8,000% (Naqvi et al., 2000a). We also know that, with some exceptions such as the California Borderland Basins (Stott et al., 2000), suboxia in coastal regions is on the increase and that only small changes in carbon and nutrient fluxes, and circulation (e.g. Codispoti, 1989) could cause significant increases in oceanic suboxia and N2O cycling (Codispoti and Chris-

tensen, 1985). Finally, we note that the time scale for change in the oceanic N2O regime is relatively short. The oceanic inventory of N2O is ~ 1000 Tg N (Suntharalingam et al., 2000) and dividing by our source term of 6 Tg N yr-1 (Table 1) gives a turnover time of < 200 years. Most of this turnover probably occurs in the upper 1000m of the water column, so it might be fair to say that the inherent time scale for change is closer to 50 years. Ice core observations (Flückiger et al., 1999; Leuenberger and Siegenthaler, 1992) suggest that variations in atmospheric N2O during the last Glacial - Holocene moved roughly in concert with CH4 and that each gas contributed about 15% to greenhouse forcing during the Glacial – Postglacial transition. Although the concentrations of CO2, CH4 and N2O were all lower during the Glacial, there are significant departures in the trends for each gas. Present-day N2O concentrations are unprecedented in the last 45 kyr. Of perhaps greater interest, are some spikes in the record that have not yet been fully explained. Given a time-scale of ~50 yrs, the potency of N2O as a greenhouse gas, and the expansion of coastal suboxia, can we be in for some surprises vs the oceanic N2O source as we enter the Anthropocene?

uptake that we have employed when asserting that denitrification may make the ocean more Fe limited may be too high. A close reading of Sañudo-Wilhelmy et al. (2001) together with information provided by Brand (1991) and Raven (1988), still suggests to us that the Fe requirement for NO3– uptake by open ocean eukaryotic phytoplankton will prove to be significantly less than for nitrogen fixation, so we still believe that it is reasonable to assert that denitrification may make the ocean more Fe limited, although the Sañudo-Wilhelmy et al. (2001) paper weakens our argument a bit. These authors studied a relatively Fe rich portion of the Atlantic and found that nitrogen fixation was highly correlated to the P content of Trichodesmium and was enhanced at higher irradiance. This is in line with previous studies summarized in the main body of our text that suggest that PO43– may limit nitrogen fixation in some cases and that the energy requirements for nitrogen fixation are high. Finally, please note that the data for station N-8 in Figure 7 were calculated using a preliminary data set and are too low by about 1.5 micromolar.

ACKNOWLEGEMENTS Some cautionary riddles As we enter the Anthropocene, we are likely to hear more and more schemes advanced to engineer global climate, including Fe fertilization of the ocean. Some of the potential downside effects of Fe fertilization on the oceanic N cycle have already been described (e.g. Fuhrman and Capone, 1991). Here are three “cautionary riddles” that the reader can solve based on the information already presented: 1. If you want to make the ocean more Fe limited, add Fe in the wrong place. 2. If you want to make the ocean more N limited add fixed N in the wrong place. 3. If you want to increase greenhouse forcing try to decrease it by adding Fe to the ocean in the wrong place.

NOTE ADDED IN PROOF Recently, Sañudo-Wilhelmy et al. (2001) have suggested that the Fe requirement for nitrogen fixation may have been considerably overestimated in prior studies. Thus, the ~60 times greater Fe requirement for nitrogen fixation in comparison to NO3–

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SCI. MAR., 65 (Suppl. 2): 107-119

SCIENTIA MARINA

2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

Marine benthic faunal successional stages and related sedimentary activity* RUTGER ROSENBERG Department of Marine Ecology, Göteborg University, Kristineberg Marine Research Station, 450 34 Fiskebäckskil, Sweden.

SUMMARY: This paper is a brief review of successional stages and activity of benthic soft-bottom communities. Benthic communities was first described by Petersen in the 1910s and further developed by Molander, Thorson and Margalef. Successional stages of benthic communities chance in a predictable way in relation to environmental disturbance and food availability. Food supply to the bottom can occur as a vertical flux, but transport through lateral advection is more important in some areas. While at the bottom, the infauna processes the food in many different ways, and the feeding modes can be categorised into more than 20 functional groups, but fewer are present in brackish water. This categorisation is based on animal mobility and where and how they ingest the food. Animal activity in the sediment, bioturbation, has a significant effect on redox conditions and diagenetic processes. Structures in the sediment due to infaunal presence and activity can be observed in situ by sediment profile imaging, and the biogenic structures and redox conditions can be parameterised and have been shown to correlate to benthic community successional stages. The largest threat to benthic faunal biodiversity is the spread of near-bottom oxygen deficiency in many enclosed are stratified coastal areas. Key words: benthos, bioturbation, functional group, benthic-pelagic coupling, deposit feeder, hypoxia.

INTRODUCTION Pioneer in marine benthic ecology was the Danish scientist C.G.J. Petersen, who in the 1910s in several papers described benthic communities in Scandinavian waters, (e.g. Petersen, 1913). The different communities were named after dominant or conspicuous species, e.g. the bivalve Macoma, the brittle star Amphiura and the polychaete Melinna, according to when different species showed dominance. Petersen’s work was later followed up by other Scandinavians, notably Molander (1928) and Thorson (1957). Molander described 9 different community types and 12 sub-communities *Received May 15, 2001. Accepted June 12, 2001.

(“facies”) in the Swedish Gullmarsfjord. Thorson stated that benthic communities were true ecological units and partly separated from each other. He developed Petersen’s ideas further and opened the global ecological perspective by showing that benthic communities in Scandinavian waters had ecological parallels in the world oceans. This is here illustrated by an example from benthic communities in Arctic, Boreal, and Northeast Pacific waters showing parallelism between Macoma communities (Fig. 1). Beginning in the 1950s, the Spanish scientist Ramón Margalef developed his ideas about marine ecosystems into a new paradigm. In his view, ecosystems develop over evolutionary times to work unified and in a cybernetic way with feed back loops that synchronize the ecosystem function. In the book MARINE BENTHIC FAUNAL SUCCESSIONAL STAGES 107

FIG. 1. – Illustration of benthic parallel communities with examples from the eastern Atlantic and the Pacific coast of the USA exemplified with the distribution of some bivalve and polychaete genera in both regions (from Thorson 1957).

“Perspectives in Ecological Theory”, Margalef (1968) described succession as “ the occupation of an area by organisms involved in an incessant process of action and reaction which in time results in changes in both the environment and the community, both undergoing continuous reciprocal influence and adjustment”. Margalef further stated that the process of succession is equivalent to a process of accumulating information, and that the final stages of succession should preferably be called 108 R. ROSENBERG

“mature ecosystems” and not labelled “climax” as in earlier ecological literature. Marine benthic communities are frequently characterised by their number of species, abundance and biomass (SAB). Pearson and Rosenberg (1978) showed that these parameters change in a predictable way along a gradient of disturbance, both in time and space (Fig. 2). In a later paper, Pearson and Rosenberg (1987) further developed the concept that food availability is a major structuring factor for

benthic communities, i.e. under low food conditions SAB is also low and when food is abundant the values of SAB are significantly higher. Food for the benthos is generally higher in shallow and coastal areas than in offshore and deeper areas. Over the last decades, the increased input of nutrients has lead to increased primary production and consequently more organic material has accumulated on the bottoms. In enclosed and stratified sea areas, the oxygen consumption can be higher than the supply, leading to oxygen deficiency and reduction of benthic communities. This review focuses on benthic macrofaunal structural changes in relation to various degrees of disturbance and on the impact of the infaunal activity for biogeochemical processes in the sediment. It is restricted to coastal seas and soft sediments. The first part deals with food supply to the benthos and functional feeding groups, and bioturbation. The role of biogenic structures for redox conditions and

chemical processes in the sediment are further discussed. Finally, succession of benthic communities is illustrated with a few examples, particularly in relation to increased oxygen deficiency followed by re-oxygenation. Arntz et al. (1999) have recently, in a partly provocative paper, reviewed several aspects related to benthic fauna: interaction, diversity, larval settlement and recolonisation. These aspects are therefore not treated in the present paper.

BENTHIC-PELAGIC COUPLING In the beginning of the 1980s, scientists from Kiel delivered significant contributions to the understanding of the role of phytodetritus as food for the benthic system (Graf et al., 1982; Smetacek, 1984). They showed that in the shallow waters off Kiel, the benthic response to a settling phytoplankton bloom occurred within less than one week. The immediate

FIG. 2. – General model of distribution of benthic infaunal successional stages along a gradient of increased environmental disturbance from left to right (after Pearson and Rosenberg 1978) and the associated Benthic Habitat Quality (BHQ) index (Nilsson and Rosenberg 1997). Sediment profile images assigned to a successional stage are mounted above the general model (colours are digitally enhanced), where oxidised sediment is rust-brown and reduced sediment is grey or black. In the bottom of the figure the generalised species (S), abundance (A), biomass (B) diagram are illustrated (after Nilsson and Rosenberg 2000).

MARINE BENTHIC FAUNAL SUCCESSIONAL STAGES 109

response of primarily bacteria and meiofauna was demonstrated by increased heat production and oxygen consumption. Graf suggested that most macrofaunal species were too slow to obtain the freshly deposited phytoplankton, but could probably later consume some of the smaller organisms. It has later been shown that maldanid polychaetes can readily react to newly deposited phytodetritus by subducting food, without immediate ingestion, from the sediment surface down to depths of 10 cm or more (Levin et al., 1997). In a summary about benthic-pelagic coupling, Graf (1992) emphasised the importance of quality of the settling material for the magnitude of the response of the benthic system. The organic part of freshly deposited phytoplankton was more or less completely mineralised in a few days. Settling phytodetritus after a bloom may have C/N weight ratios of about 7, close to the value of plankton algae of between 5 and 6, but the ratio may be >10 later in the season. Gray (1992) reviewed the usefulness of C/N ratios for assessing the nutritious quality of settling material. He found that C/N ratios generally are low in coastal surface waters, and that they are higher in the open ocean, around 14. In comparison, the C/N ratios in vascular plants may go up to 100,

showing that they are particularly refractory. The rates of organic matter decomposition and microbial growth have been found to be inversely correlated with age and C/N ratios of the substrate (Kristensen and Blackburn, 1987). Smetacek (1984) and Graf (1992) showed that in boreal systems, the main food supply to the benthos is pulsed and enhanced twice a year; after the spring and autumn blooms. Wassmann (1990) studied the relation between primary production and “export production”, i.e. he estimated the amount of carbon that is transported downwards from the photic zone. He found a linear correlation during moderate primary productions, but during enhanced nutrient conditions and primary production, but the export production increased in an exponential way. Export production is, however, dependent on phytoplankton species composition and grazing intensity and is suggested to vary in relation to this and hydrographical features. General models describing the coupling between the pelagic and the benthic systems have been presented by Ott (1992). These models were developed for the Adriatic Sea in the Mediterranean, but some are applicable also for other marine systems (Fig. 3). In oligotrophic, deep waters most of the organic

FIG. 3. – General model of benthic-pelagic coupling from the Adriatic Sea in the Mediterranean Sea showing the sedimentation of organic matter under different trophic conditions and the importance of a pycnocline (from Ott 1992).

110 R. ROSENBERG

FIG. 4. – Dynamic model of benthic-pelagic coupling showing the particle input to the bottom through vertical sedimentation, lateral advection or resuspension, and possible fluxes out from the sediment to the water column (from Graf 1992).

material will be mineralised in the water column, and the fraction that reaches the bottom will be largely refractory. In mesotrophic waters and medium depths (shelf to 50 m increased with increasing salinity from 3 in the Gulf of Bothnia to about 20 in the Kattegat/Skagerrak. In the Baltic, only one group of (mobile) sub-surface deposit feeders was found, but 5 groups occurred in the Kattegat/Skagerrak. Thus, the functional biodiversity, reflected in different feeding modes and mobility, correlated with increased salinity. On 4 stations in the North Sea, with similar salinities, Dauwe et al. (1998) found instead that the different composition of trophic groups of the benthic fauna was related to food availability, which also was suggested by Pearson and Rosenberg (1987).

BIOTURBATION Bioturbation is related to several different activities of benthic infauna: deposit feeding, reworking, construction of burrows and tubes, and irrigation. All have significant effects on biogeochemical processes in the sediment and at the sedimentwater interface, and on redox conditions in the sediment. Rhoads (1974) was one of the pioneers in this field of research, and in the review of organism-sediment relations he also emphasised the ecological role of biodeposition by benthic animals. Rhoads was the first scientist to show in situ sediment profile images to illustrate biogenic structures in the sediment (see Fig. 2). Several other American scientists have made significant contributions to the biology of deposit feeders. Lopez and Levington (1987) and Jumars and Wheatcroft (1989) elegantly described the life of deposit feeders: they account for the largest bioturbation of particles, they feed on a remarkably poor food source, most species are selective feeders, and they separate sites of ingestion and egestion. Many deposit feeders seem to mainly ingest microbes associated with particles (microbial stripping), as they do not have the digestive capability of fresh phytodetritus. Lopez and Levinton (1987) summarised feeding rates for 20 deposit feeding invertebrates and found that they daily processed at least the same amount of sediment as their own body weight, often much more. 114 R. ROSENBERG

To estimate the amount that sediment deposit feeders may bioturbate, I have made the following simplifications. Assume that the biomass of deposit feeders is 120 g m-2, and that they may be able to rework at least the same amount of sediment daily. If we also assume that the deposit feeders are evenly distributed down to 10 cm depth in the sediment and bioturbate that part of the sediment (Boudreau, 1997b) (sediment volume is then 100 dm3 equivalent to ≈120 kg), they may process about one-third of this superficial sediment per year. However, more recently Sandnes et al. (2000) documented that large animals, e.g. heart urchins such as Ecinocardium cordatum, may dominate the reworking process in some areas, and when they are present larger volumes than those exemplified here might be bioturbated annually. Animal tubes have a fixed structure in the sediment, whereas burrows have a considerable variation and the volume not utilized permanently by the occupant is generally much larger in burrows than in tubes (Lee and Swartz, 1980). Burrows and tubes are micro-environments of chemical significance to sediment-water exchange processes, but measurements of tubes and burrows and their extension in the field is limited to a few examples in the literature. Hylleberg and Henriksen (1980) and Fenchel (1996) have shown that populations of the polychaetes Nereis virens and N. diversicolor, and the amphipod Corophium volutator through their burrowing activity significantly increase the oxic conditions within the sediment. Similarly, Davey (1994) found the increase of surface area due to a natural population of Nereis diversicolor to be about 300%. Mainly burrows of large thallassinidean crustaceans have been investigated by the resin cast technique, (e.g., Astall et al., 1997). Architecture of burrow systems has also been studied by X-radiography (e.g. Schaffner, 1990). Several experimental studies have shown the ecological importance of infaunal bioturbation, irrigation, burrow and tube structures for biogeochemical processes. For example, Forster and Graf (1992) calculated for Callianassa subterranea a 0.7 m2 burrow surface area subjected to oxygenation below every m2 of sediment surface. In situ sediment profile images from the Kattegat clearly demonstrated the great effect of large crustacean burrows on redox conditions in the sediment (Fig. 6). Hylleberg and Henriksen (1980) estimated that the increase in oxic sediment volume due to bioturbation would be 30 to 50 % for 2000 ind. m-2 of the polychaete Nereis virens and 100 to 150 % for 6000 ind. m-2 of the

FIG. 6. – Sediment profile images from depths between 40 and 120 m in the Kattegat (West Sweden). The yellow colour indicates the oxidised sub-oxic zone and the darker zone is reduced sediment (colours are digitally enhanced). The large burrows at 60 to 120 m depth are probably made by the crustaceans Calocaris macandreae and Maera loveni. Several polychaetes are seen in the image from 100 m and appear to be Heteromastus filiformis. The vertical scale is centimetres, and the black rectangle masks reflections of the flash (from Rosenberg et al., 2000).

amphipod Corophium volutator. The authors concluded that bioturbation increases the rates of both nitrification and denitrification. Similarly, Mayer et al. (1995) found that macrofaunal burrows and tubes greatly enhanced the nitrification potential compared to that of oxidised surface sediments. Experiments conducted in situ in the Mediterranean demonstrated a 160 to 280% greater denitrification potential with infauna compared to in defaunated sediments (Gilbert et al., 1998). The burrow walls are important sites for nitrification-denitrification processes in the sediment, since these require a juxtaposition of oxic and anoxic micro-habitats (Jenk-

ins and Kemp, 1984). Reworking of surface sediment by the sea urchin Brissopsis lyrifera was shown to increase oxygenation and precipitation of phosphate, and to decrease the denitrification rate (Widdicombe and Austen, 1998). Ockelmann and Muus (1978) estimated that a single Amphiura filiformis can oxidise an area of 35 cm2 in the sediment, mainly around the disc. Based on that figure, Rosenberg (1995) estimated that high densities (3000 ind. m-2) of A. filiformis, as found in the northern Kattegat, might oxidise an area in the sediment of about 10 m2 per m2 surface area. Aller and Aller (1998) used sediment plugs to simulate spacing of individMARINE BENTHIC FAUNAL SUCCESSIONAL STAGES 115

ual burrow structures in the sediment. They found that the specific geometry of burrow sections was likely to have significant localized effects on chemical fluxes and microbial activity. Further, macrofauna enhanced solute transport 2 to 10 times more than meiofauna (Aller and Aller, 1992). Thus, we have evidence that macrofaunal bioturbation are important for sediment geochemistry and that the infaunal species are important ecological engineers. The challenge for future research is to improve the quantification of these processes and assess their role in the marine ecosystem.

FAUNAL SUCCESSION AND ASSOCIATED SEDIMENT CHANGES Structural changes in marine benthic communities caused by different disturbances such as organic enrichment and physical forces seem to be rather predictable and follow models presented by Pearson and Rosenberg (1978) and Rhoads and Germano (1986). Since their appearance, the models have been tested repeatedly and seem to be generally applicable to various types of changes in many habitats (Heip, 1995). Timing of a disturbance may have a significant effect on succession, particularly in shallow coastal waters as was shown in a study in Connecticut, USA. Zajac and Whitlatch (1982) found that benthic community succession after a disturbance in spring was followed by high species numbers and densities, whereas a disturbance in the autumn was followed by few species in low numbers. In the original models, the importance of biogenic structures for the sedimentary redox conditions was indicated in a schematic way. Recently that part of sedimentary information in the model was supplemented by sediment profile images (SPIs) taken in situ during temporal decline in oxygen concentrations in the Gullmarsfjord in the Skagerrak (Nilsson and Rosenberg, 2000; Fig. 2). The SPI technique was developed by Rhoads and co-workers (Rhoads and Cande, 1971; Rhoads and Germano, 1982, 1986) and it is a cost-effective method to obtain rapid information about the relations between faunal activity, biogenic structures and redox conditions in the sediment. In contrast to grab samples for information about composition and quantitative assessment of the macrofauna, SPI is a non-destructive method that gives information of faunal structures, infaunal activity and chemical properties of the sediment. In the study cited above 116 R. ROSENBERG

from the Gullmarsfjord, it was shown that the sedimentary habitat changed gradually with declining oxygen concentrations in the water above the bottom, and this was correlated with decline in the SAB variables (Nilsson and Rosenberg, 2000). By digitally analysing the SPIs, contrasts between colours of the sediment can be enhanced. Thus, the redox potential discontinuity (RPD), i.e. the zone between oxidised (rust-brown) and reduced (black) sediment, can be determined and the oxidised areas quantified. Following dissolved oxygen, which only penetrates a few millimetres into the mud (Revsbech et al., 1980), the oxidising agents in the oxidised (sub-oxic) zone are in sequence: NO-III, Mn+IV and Fe+III (Aller, 1988). A significant correlation between measurements of the RPD in the sediment has been obtained between measurements with electrodes and with digital analysis of SPIs (Rosenberg et al., 2001). Nilsson and Rosenberg (2000) showed that the four successional stages of the benthic communities in the Pearson-Rosenberg model determined from SAB-curves were significantly correlated with a benthic habitat quality (BHQ) index determined from SPIs. The BHQ index is based on parameterisation of (1) sediment surface structures, (2) subsurface structures, and (3) mean depth of apparent RPD (Nilsson and Rosenberg, 1997). The BHQ index summarises a maximum of 5 scores from each of these three estimates and varies between 0 and 15 (see Fig. 2 for assignment of BHQ to benthic faunal successional stages). In recent studies by Nilsson and Rosenberg (2000) and Rosenberg et al. (manuscript), the successional changes of SAB of the benthic fauna from grab samples and from SPIs were followed during a two-year recovery period subsequent to re-oxygenation of the Gullmarsfjord initiated in April 1998. We can show, for the first time, how benthic communities during decreased and long-term (months) oxygen deficiency deteriorated to poor maturity successional states, and how they successively recovered during re-oxygenation towards mature community states of a similar structure as before the disturbance by hypoxia. The recovery at four stations during 2 years was an almost successive increase for number of species, abundance and biomass. The benthic communities returned to an almost identical faunal structure with the same dominants. Similarly, the BHQ index showed a more or less successive increase over that time period. The fauna on two of the stations returned to Successional Stage (Fig. 2), but the two most severely hypoxiaaffected stations did not quite reach that stage during

the two years of recovery. Thus, the benthic habitat quality also showed a rapid recovery. This was associated with a successively deeper penetration of the RPD indicative of increased bioturbation and irrigation processes. This demonstrates that the benthic faunal activity and their sedimentary habitat quality are closely linked. In New Jersey, USA, hypoxia occurred for about 2 months in 1976. Following hypoxia, a few species returned to previous densities, but the recovery to the previous faunal structure was longer than 2 years (Boesch and Rosenberg, 1981). The authors pointed out that the resiliency of benthic communities to hypoxia is dependent on the constituent species, which have different life-cycles, reproduction periods and patterns of larval dispersion. In Kiel Bay in the southwest Baltic, the benthic communities were suggested to be pre-adapted to hypoxic conditions, especially in the inner part of the bay. These species had opportunistic features, they were fast growing and rapid colonisers, and they returned to pre-hypoxic conditions within about 1 year (Arntz, 1981). In a Swedish fjord, polluted by wastes from a sulphite pulp mill, the recovery to pre-disturbed conditions on 20 to 40 m deep bottoms took between 5 and 8 years. This comparatively slow recovery process was due to unfavourable sediment conditions with high organically enriched and reduced sediment with H2S and fibres (Rosenberg, 1976). In shallow waters and defaunated sediments, the recovery process is generally much quicker and can be in the order of months (e.g. Santos and Simon, 1980).

EUTROPHICATION AND HYPOXIA Eutrophication and hypoxia are spreading worldwide and have significant effects on benthic faunal succession. Eutrophication emerged as an increasing disturbance to coastal marine ecosystems in the 1980s (Rosenberg, 1985), but early warning signals were documented in the brackish Baltic Sea already in the 1960s (Fonselius, 1967). The increased input of nutrients and their effects on the ecosystem have been reported from Scandinavian waters (Ambio 1990, vol. 19). The secondary effects of eutrophication on benthic communities can be simplified as either an increase of food for the animals resulting in increased biomass (Josefson, 1990; Rosenberg et al., 1987), or lead to oxygen deficiency resulting in elimination of some species (Rosenberg et al., 1992) or communities with small individuals (Pearson et al., 1985; Josefson and Jensen, 1992). Gray (1992) presented a model of benthic faunal succession and effects on the animals in relation to different oxygen saturations in the near-bottom water (Fig. 7). The model has a similar layout as that in Figure 2, and Gray used information from (Baden et al., 1990). It is clear from Gray’s model that increased oxygen saturations are correlated with a general increase in sediment RPD. Gray suggested that fish shows avoidance reactions in oxygen saturations between 25 and 40 % and that behavioural responses to hypoxia in invertebrates occur at lower saturations. In a review about the effects of hypoxia (generally defined as O2 concentrations 1000 mm/yr < 200 mm/yr

Meteorological Runoff (P - E) FIG. 1. – Distribution of annual meteorological runoff (P-E) in Europe. Modified from Milliman and Farnsworth (in press).

European Mountains (> 1000 m Elevation) FIG. 2. – Distribution of mountainous terrain in western Europe. Shown in black are elevations higher than 1000 m. Modified from Milliman and Farnsworth (in press). EUROPEAN RIVERS DISCHARGING TO THE SEA 123

FIG. 3. – Runoff for the Glomma (Norway), Oder (Poland) and Loire (France) rivers in northern and western Europe. To the left are annual runoff values (open circles with dashed lines) as well as running 5-yr means (solid lines). To the left are the monthly variations in discharge. Data from various UNESCO Discharge of Selected Rivers of the World reports.

Italy has much greater precipitation and runoff than elsewhere in southern Europe. It is therefore not surprising that hydrologic runoff (discharge divided by drainage basin area) is greatest for northern rivers, such as the Glomma (Norway), decreasing substantially in central and western European rivers (e.g., Oder, Loire and 124 J.D. MILLIMAN

Danube rivers in Figs. 3 and 4). Rivers draining the southern Alps (Ebro and Po in Fig. 4) have somewhat higher runoffs. Discharge varies temporally as well as spatially. For instance, the Oder, Loire and Danube all exhibited near record-high discharge around 1940 and again in the late 70s and early 80s, whereas the Ebro

FIG. 4. – Runoff for the Ebro (Spain), Po (Itlay) and Danube (Romania) rivers in southern and eastern Europe. To the left are annual runoff values (open circles with dashed lines) as well as running 5-yr means (solid lines). To the left are the monthly variations in discharge. Data from various UNESCO Discharge of Selected Rivers of the World reports.

and Po had high discharges in the late 30s and 1961, with low discharges in the early 40s and early 60s (Fig. 4). Most interesting, however, is the inverse relationship between discharge of western and central European rivers (Loire and Oder) and the North Atlantic Oscillation (NAO) index, in contrast to eastern US rivers, which show a positive correlation

(Fig. 5). Although the significance of this observation is uncertain, periods of high and low precipitation (and thus river discharge) seem oscillate back and forth across the Atlantic. It is interesting to speculate that inter-annual net freshwater discharge entering the North Atlantic may be roughly constant, but that the relative importance of North EUROPEAN RIVERS DISCHARGING TO THE SEA 125

discharge during the winter and maximum discharge in mid to late spring. Farther south, the Oder and Loire exhibit highest discharges progressively earlier in the year, and minimum discharges are in the summer months rather than the winter (Fig. 3). The Loire, in fact, displays a Mediterranean climate similar to the Ebro River (high winter runoff, low summer runoff), while the Po and Danube discharge patterns largely reflect the alpine terrain that they drain (Fig. 4).

SOLID AND DISSOLVED LOADS

FIG. 5. – Running 5-yr means of runoff for the Penobscot and Pearl rivers (eastern U.S.A) and the Oder, Loire and Thames rivers compared to the North Atlantic Oscillation (NAO) index. Note that positive NAO values tend to coincide with high discharges in eastern US rivers and low discharges for central and western European rivers, whereas low NAO appears related to the opposite trend in eastern US and European rivers.

American vs. western European rivers changes in response to the NAO. The seasonality of river flow also varies geographically. Scandinavian rivers have minimum 126 J.D. MILLIMAN

The erosion and transport of solid and dissolved sediment are largely a function of climate, geology (reflecting both topography and lithology), and anthropogenic activity. Because of the broad range of climates (particularly precipitation and runoff; Fig. 1), the presence of several major mountain ranges (Fig. 2), the local dominance of both old, hard rocks (e.g., Scandinavia; Fig. 6)) and younger, softer rocks (e.g., southern Alps, and particularly watersheds in central Italy and Albania), and a long history of human activity within many of the drainage basins, European rivers have a wide variety suspended- and dissolved-solid regimes. Fluvial sediment loads are generally related to the topographic relief of the drainage basin, the result of both increased stream gradient and (often) greater tectonic activity (hence landslides). Sediment load also increases with increasing precipitation (Milliman et al., in prep.) and the presence of more erodable rocks (e.g., mudstone compared to granite; Hicks et al., 1996). Although western Scandinavia is mountainous, eastern Scandinavia is low-lying, and rocks throughout the area are mostly old (pre-Mesozoic) and hard (metamorphic, igneous). As a result, Scandinavian rivers have extremely low sediment loads regardless of basin area (sediment load tends to be a function of basin area, being greater in large than in small drainage basins; e.g., Milliman and Syvitski, 1992). Historically much of Scandinavia has been relatively free of industrial pollution, and this combined with the sub-arctic climate and old (i.e. hard) lithology has resulted in low dissolved loads (Fig. 7, left). The headwaters for many northern and western European rivers are located in mountainous regions (Fig. 2), but the rocks are generally old (Fig. 2; and therefore hard). Smaller rivers tend to

Pre-Mesozoic Rocks FIG. 6. – Distribution of pre-Mesozoic rocks in Europe. Older rocks here infer that they generally are harder (and thus more difficult to erode) than younger Mesozoic and Cenozoic rocks. After Larsen and Pittman (1985).

drain lower elevations. As a result rivers draining northern and western Europe have low sediment loads, although generally not as low as those for Scandinavian rivers (Fig. 7). (The Rhine provides an interesting anomaly in that much of its sediment load is trapped in Lake Constance, so that north of Switzerland it behaves more like a low-

land river than one whose headwaters are in mountainous terrain.) Dissolved loads in western European rivers, however, are not only greater than those in Scandinavian rivers, they loads also tend to be greater than suspended loads (Fig. 7, center), one of the few areas on Earth in which this situation occurs.

FIG. 7. – Mean suspended and dissolved loads for Scandinavian (left), northern European (center) and southern European (right) rivers. Note that the relation between dissolved (open diamonds) and suspended (solid dots) loads vary regionally. Both suspended and dissolved loads are low in Scandinavian rivers, dissolved loads are substantially greater in northern European rivers, and suspended loads are much greater in southern European rivers. Data from Meybeck and Ragu (1997) and Milliman and Farnsworth (in press).

EUROPEAN RIVERS DISCHARGING TO THE SEA 127

FIG. 8. – Comparison of mean annual suspended loads (left) and dissolved loads (right) for southern (solid dots) and northern (open diamonds) European rivers . Suspended loads for southern European rivers are clearly much greater than they are for rivers draining northward from the Alps, largely the result of regional geology, morphology, and climate. In contrast, the relationship between dissolved load and basin area for northern and southern European rivers is more or less the same, with the main exception of six rivers (Weser, Rhine, Gauja, Tiber, Po and Rhone) whose dissolved loads are substantially greater than their basin area would suggest. See also Table 1.

Most southern European rivers, in contrast, carry sediment loads that are one to three orders of magnitude greater than similar sized rivers draining northern Europe (Figs. 7, right, and 8). Many of the drainage basins draining the southern Alps (and the Apennines in Italy) contain younger (and therefore more erodable) rocks. But the greater sediment loads of southern European rives also reflect a long history of anthropogenic activity on the alpine and Mediterranean landscape (e.g., Woodward, 1995). Southern European river dissolved loads are much less than their suspended loads (Fig. 7), but are similar to northern European rivers (Fig. 8). It is interesting to note that total dissolved loads TDS) in northern and western European rivers increase essentially linearly as a function of basin size (dissolved load = (0.08)*(basin area)^1.03 (r2 = 0.92) (Fig. 8). If three rivers with anomalously high TDS values (Rhine, Weser and Gauja) were deleted from the correlation, the exponent would 1.00 (r2 = 0.96). Southern European rivers cluster around this correlation except for three rivers –the Tiber, Po and Rhone– who have considerably high TDS values than would be predicted from their basin size. Given the tight fit of the data, in fact, one can calculate theoretical dissolved loads and compare them to measured loads. As inferred from Fig. 8, the measured loads of the Rhine, Weser, Gauja, Rhone, Po and Tiber (shown as asterisks in Fig. 6B) are significantly greater than their basin areas would indicate (Table 1). For European rivers this often is a result of salt mining (e.g., Fraser et al., 1995), 128 J.D. MILLIMAN

suggesting that calculated delivery of dissolved NaCl and KCl might account for much of the “excess” dissolved solids in these anomalous six rivers. Assuming for the moment that all the Cl is derived from dissolved NaCl, one can calculate the total amount of dissolved NaCl delivered by each of the rivers. This assumption, of course, is incorrect, since some Cl is derived from sources other than halite; therefore the calculated numbers in Table 1 must be considered maximum values. Nevertheless, dissolved NaCl can account for most (if not all) of the excess dissolved solids in the Weser and Rhine rivers (Table 1), but practically none of the dissolved solids in the Gauja or (more importantly) in the three rivers draining the southern Alps. The apparent lack of halitederived Cl in these southern rivers suggests that these rivers may be less polluted (at least interms of salt) than the northern rivers, and therefore that natural TFDS values are greater than for similar sized rivers in the north. This is reconfirmed by the Cl to SiO2 ratio, the latter value assumed to be a natural dissolved constituent(1). Northern rivers tend to have significantly greater dissolved Cl/ SiO2 ratios (mean = 37; range = 2.1-308) than southern rivers (mean = 5.5; range = 4.5-6.5), and the heavily industrialized hinterlands in Germany have some of the highest Cl/SiO2 ratios (33, 43 and 308 for the Rhine, Elbe, and Weser rivers, respectively) noted in global rivers. 1 It should be cautioned that SiO2 contents in dammed rivers can be depleted when trapped in artificial lakes for prolonged periods (Humborg et al., 1997).

TABLE 1. – Measured and calculated mean annual dissolved solid loads from various European rivers. Calculated values were based on the equation derived in Fig. 6B [dissolved load = (0.08)x(basin area in thousand of km2)]. NaCl load was computed assuming that all Cl discharged from the various rivers is associated with Na; clearly this calculated load is a maximum, since the Cl has other sources. The first six rivers fall upon the curve shown in Fig. 6B and therefore are assumed to have dissolved loads “normal” for European rivers. Measured and calculated are generally similar, and the slight excess measured load for four of the rivers can be explained in large part by dissolved NaCl. The second six rivers have anomalously high dissolved loads (Fig. 6B). Essentially none of the Gauja’s (Estonia) excess dissolved load is present as NaCl, whereas all of the Rhine and Weser’s excess loads can be explained by dissolved NaCl. In contrast, little of the “excess” dissolved loads from the last three rivers, who drain the southern slopes of the Alps, appear to be derived from dissolved NaCl, suggesting that these high dissolved loads may have less anthropogenic influence than the Rhine or Weser. Measured TDS data from Meybeck and Ragu (1997). River

Basin Area (x 103 km2)

Meas. TDS (x 106 t/yr)

Calc. TDS (x 106 t/yr)

D (x 106 t/yr)

NaCl Load (x 106 t/yr)

Elbe Seine Guadaliquivir Ebro Arno Evros

150 65 56 87 8.2 52

14 6.3 5.9 9.0 1.4 2.6

12 5.2 4.5 7.0 0.7 4.2

2.0 1.1 1.4 2.0 0.7 (1.6)

6.6 0.8 1.9 2.0 0.3 0.4

Gauja Weser Rhine Rhone Tiber Po

8.9 46 220 96 17 70

6.2 26 45 17 5.9 16

0.7 3.7 18 7.7 1.4 5.6

5.6 22 27 9.3 4.5 11

0.02 22 21 1.8 1.2 1.4

The difference in northern and southern European rivers also can be seen with respect to nutrient flux. Although these is some scatter in the data, NNO3 fluxes from northern European rivers (open diamonds in Fig. 9) are generally 2 to 5 times greater than for similar sized rivers draining the south (solid dots in Fig. 9). In contrast, Scandinavian rivers have loads about an order of magnitude smaller for any given basin size. The exceptions to this general trend are Portuguese and Baltic state rivers (all of whom have low nitrate loads), the Rhone (whose load is much lower than similar sized southern rivers), and the Po (whose nitrate load is much higher than other southern rivers). Similar trends are seen for other nutrients, such as dissolved phosphate and silicate (data from Meybeck and Ragu, 1997.

PAST AND FUTURE CHANGE As one can see from the preceding discussion, European rivers have been influenced by both the natural environment (climate and geology) and human activities. Deforestation, mining, industry, and urbanization, in fact, have played major roles in the water quality (or lack therefore) of European rivers and adjacent estuaries for many centuries, and, with reference to Mediterranean rivers, millenia (e.g., McNeil, 1992; Woodward, 1995). In fact, human impact on European river basins can be viewed on the basis of European history: rivers such

FIG. 9. – Dissolved N-NO3 flux versus drainage basin area. Northern European rivers (open diamonds) generally have much greater loads than either southern European or Scandinavian rivers, the major exceptions being Portuguese and Baltic-state rivers, whose loads more closely approximate those found in Scandinavian rivers. Data calculated from data compiled by Meybeck and Ragu (1997).

as the Ebro, Po and Axios (Greece) were affected by human activity as early as 2500 years ago, but the Ebro and Po deltas prograded appreciably over the past 400 years in response to increased deforestation in the upper parts of the respective river basins (Mariño, 1992; Sestini, 1992). In the past 50 years, however, sediment loads for many European rivers have decreased, in some cases precipitously, in response to both changes in EUROPEAN RIVERS DISCHARGING TO THE SEA 129

land use and river diversion (most notably dam construction). Landuse has changed as western Europe has evolved increasingly to a non-agrian society. Frangipane and Paris (1994) reported more than an 85% decrease in sediment load for the Ombrone River (central western Italy) over the past century, which they explained by decreased grazing (by domestic animals) and a corresponding increased forest cover. Dam construction, of course, has only added to the change in water and sediment flux. Spain alone has more than 900 large dams (defined by the International Commission on Large Dams as having a relief greater than 15 m). Damming of the rivers in the latter part of the 20th century not only has stopped delta-front progradation, it also has resulted in local erosion as well as landward intrusion of saline groundwaters. Becchi and Paris (1989; c.f. Billi and Rinaldi, 1997) estimated that the sediment load of the Arno River (Italy) increased from about 2 x 106 t/yr prior to the 16th century to 7.5 x 106 t/yr in 1800, but in the past 50 years has decreased to about 2.7 x 106 t/yr, most of the rest being trapped behind dams. Three Albanian rivers (Drini, Vijose and Semani) formerly had an annual combined sediment load of about 75 x 106 t/yr; but at present their combined load is about 26 x 106 t/yr (Ciavola et al., 1998). The examples of the Rhone and the Ebro are even more extreme, the former decreasing from 5 9 to about 6 x 106 t/yr (Pont, 1997) and the latter delivering less than 1% of its former load to the coastal zone (Guillén and Palaques, 1992). Moreover, the streambeds of many mountainous Mediterranean rivers have been increasingly mined for sand and gravel (even though this is often an illegal activity); the lower reaches of the Arno River, for instance, has been lowered as much as 2-4 m over the past century by river mining (Billi and Rinaldi, 1997). Changes in the dissolved constituents flowing into European estuaries have been widely studied. Etchanchu and Probst (1988), for example, reported that a 14-19% increase in Cl-, SO4-2, and K+ - in the Garonne River between 1971 and 1984, and a 78% increase in NO3 that was almost exclusively related to increased application of fertilizers in throughout the watershed. As industrial and agricultural practices become more efficient and as human waste waters are more effectively treated, however, dissolved solid and nutrient contents should decline in many western 130 J.D. MILLIMAN

European rivers. It may take a bit longer for levels to fall in rivers draining former East-Bloc countries, but one can safely assume that within the next 20 years many (if not most) European rivers will discharge few suspended and dissolved solids than they do at present. One result of these decreased fluxes should be decreased eutrophication of European estuaries and coastal waters. However, changing ratios of dissolved solids may change the composition of biological blooms in coastal waters. Humborg et al. (1997), for instance, found that a decreased flux of dissolved silicate from the Danube River (because of diatom blooms in various dammed lakes, chiefly the reservoir behind the Iron Gates Dam), which has resulted in a shift from a diatom-dominated phytoplankton community in the NW Black Sea to one dominated by dinoflagellates and coccolithorphorids. One implication of this ecosystem shift may be increased hypoxia and anoxia, as well as a greatly diminished coastal fisheries (Humborg et al., 1997). Decreased sediment loads to the coastal zone already has resulted in increased erosion of the Ebro, Rhone and Po deltas (e.g., Mariño, 1992; Corre, 1992; Sestini, 1992), which presumably will only accelerate in the coming years. Similar accelerated erosion should occur along the Albanian coastline in response to decreased sediment loads from their rivers. Such effects, on the other hand, should be minimal for western and northern European rivers, as most of their watersheds already have been so completely “managed” that it seems highly improbable that their already tiny sediment loads can diminish much further. But to assume that one can use mid-20th century values for any European river to estimate future (or even present-day) fluxes to adjacent coastal waters can lead to severe miscalculations. Care must be taken in using up-to-date values, even at a time when the number of rivers and stations being monitored appears to be decreasing (Vorosmarty et al., 2001).

ACKNOWLEDGEMENTS I thank Katherine Farnsworth for her help in compiling many of the data used in this paper. Preparation of this paper was partly supported by research grants from the National Science Foundation (NSF) and the Office of Naval Research (ONR).

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istry and ecosystem. Nature, 386: 385-388. Larsen, R.L. and W.C. Pittman, III. – 1985. The Bedrock Geology of the World. W.H. Freeman and Company, Inc. New York (single map). McNeil, J.R. – 1992. The Mountains of the Mediterranean World. Cambridge Univ. Press, 423 pp. Mariño, M.G. – 1992. Implications of climatic change on the Ebro Delta. In: L. Jeftic, J.D. Milliman and G. Sestini (eds.), Climatic Change and the Mediterranean. Edward Arnold, London, 304-327. Meybeck, M. and A. Ragu. – 1997. River discharges to the oceans: An assessment of suspended solids, major ions and nutrients. GEMS/EAP Report, 245 pp. Milliman, J.D. and K.M. Farnsworth. – (in press). River Runoff, Erosion and Delivery to the Coastal Ocean: A Global Analysis. Oxford University Press. Milliman, J.D. and J.P.M. Syvitski. – 1992. Geomorphic/tectonic control of sediment discharged to the ocean: the importance of small mountainous rivers. J. Geol., 100: 525-544. Pont, D. – 1997. Les debits solides du Rhone a proximité de son embouchure donnees récentes (1994-1995). Rev. Geogr. Lyon, 72: 23-33. Sestini, G. – 1992. Implications of climatic changes for the Po delta and Venice lagoon. In: L. Jeftic, J.D. Milliman and G. Sestini (eds.), Climatic Change and the Mediterranean. Edward Arnold, London, 428-494. Vorosmarty, C.. et al. – 2001. Global water data: a newly endangered species. EOS, 82, 54-58. Woodward, J.C. – 1995. Patterns of erosion and suspended sediment yield in Mediterranean river basins. In: I.D.L. Foster, A.M. Gurnell and B.W. Webb (eds), Sediment and Water Quality in River Catchments, pp 365-389. John Wiley &, Chichester.

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SCIENTIA MARINA

SCI. MAR., 65 (Suppl. 2): 133-140

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A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

Gaia and the Mediterranean Sea* KENNETH J. HSÜ Tarim Associates AG, Frohburgstrasse 96, 8006 Zurich, Switerland.

SUMMARY: The Earth is a self-organizing system liking a living organism. Lovelock proposed Gaia as a metaphor to designate the check and balance ofterrestrial temperatures: the Earth is never too hot so that the ocean could boil, and the Earth is never too cold that the ocean could freeze from top to bottom. Hsü proposed that Gaia is endothermic because the life on Earth has been alternate successions of air-conditioners and heaters which evolved and deactivate or reinforce the terrestial greenhouse of carbon dioxide in atmosphere. When Earth was heating up too much, the air-conditioneers, such as anaerobic bacteria, cyanobacteria, skeletal organisms and trees, and finally calcareous plankton, went to work to bring the terrestrial temperature down. When the Earth was freezing at times of continental glaciation, heaters went to work, such as methanogenic bacteria, Ediacaran faunas, tundra and desert plants, and now Homo sapiens. Gaia has to have other organs to keep the self-organizing system vital. This paper presents a postulate that the Miocene Mediterranean Sea acted as Gaia's kidney. The steady influx of dissolved ions and debris into the ocean causes inevitable increase of ocean's salinity. The fossil and geochemicl records indicate that the ocean has never been too saline nor too brackish for the survival of normal marine organisms: the salinity ranged from about 32 to 36 pro mil during the last billion years. Ocean-drilling cruises to the Mediterranean discovered a very large salt formation, deposited during some 5 million years ago when the Mediterranean dried up. A study of the geochemical balance of the oceans indicates that the deposition of very large salt bodies in isolated basins such as the Miocene Mediterranean every 100 million years or so. The saline giants have the function of Gaia's kidney. With periodical removals of the salt ions and the heavy metals from seawater, the world's ocean have been rendered forever habitable. Gaia has to have a kidney. The desiccation of the Mediterranean is the evidence of a functioning kidney. Earlier "kidney functions" were performed during the deposition of the Cretaceous (South Atlantic), Jurassic (Gulf of Mexico), Permo-Triassic (Europe), Devonian (Canada),.Cambrian/Precambrian (Gondwana) saline giants. Key words: Gaia, self-organizing, terrestrial greenhouse, evolution, Mediterranean, saline giants, Gaia’s kidney.

GAIA AS A SELF-ORGANIZING SYSTEM Venus is dead: with surface temperature more than 600°C; the planet is an inferno of fire. Mars is dead: with surface temperature more than 100°C below freezing; there is no water to sustain life. Our planet is alive and populated with living organisms. Earth has always been alive, during the last 3.5 billion years at least: with the ocean that has never boiled nor completely frozen to the bottom, life on Earth has never been completely extinguished. *Received May 25, 2001. Accepted June 21, 2001.

The surface temperature on planets depends upon (1) solar radiation received, (2) solar radiation lost through reflection from planetary surface - the albedo effect, (3) reflected solar radiation trapped by greenhouse gases (carbon dioxide and methane) in atmosphere, - the greenhouse effect. Solar input was weaker in the beginning of the Solar System, the greenhouse effect of early terrestrial atmosphere had to be some 600 times greater than that of the present in order to keep the global temperatures within the present range. However, the solar radiation increased rapidly and reached the present level some three billion years ago, and the GAIA AND THE MEDITERRANEAN SEA 133

level has remained more or less constant since. Solar variations, small as they are, may have an influence on the terrestrial climate of the last 2 billion years, but we have also to considered the albedo and the greenhouse effects. James Lovelock was the first to propose the Gaia hypothesis. He used the metaphor and a parable of white and black daisies to illustrate his idea that the albedo effect has influenced climate. At the time when white daisies took over the world, the albedo effect would become very large and global temperatures are reduced. The ecological impact of global chill, Lovelock speculated, is to reduce the population of the white daisies and to broaden the distribution of black daisies on Earth. The black dominance should then reduce albedo, causing global warming and a return of the white daisies. His hypothesis of alternate dominance of a pair of mythical plants illustrated the concept of a strange attractor: the rise and fall of different species of living organisms have provided a feedback mechanism to make the Earth a self-organizing system. White daisies exist today, but they have never been a dominant species on the surface of the Earth, whereas black daisies never existed. In fact the history of Earth’s albedo is largely unknown. Lovelock’s idea of Gaia is nevertheless attractive, if we forget about his white and black daisies. The essence is to consider the Earth a self-organizing system. Gaia’s strange attractors in a real world are not the albedo but the greenhouse effects. I presented a modification of the Gaia theory in a talk at the British Association of Advancement of Science, and speculated on a correlation of planetary temperatures to the evolution of organisms which played a significant role in the carbon-cycling of the earth (Hsü, 1992) Carbon dioxide on Venus has been released from the planetary interior at a faster rate than that escaped from the Venusian stratosphere. Accumulating the surplus over billions of years, Venus is enveloped in a dense atmosphere of carbon dioxide, and the planet has become an inferno of fire. Carbon-dioxide has also been released from the interior of Mars, but the rate has been less than the escape rate. The ever-decreasing greenhouse effect could not maintain a habitable surface temperature, and the situation became worse when the lowered temperature caused the last remaining carbon dioxide to be frozen into dry ice. The concentration of the greenhouse gases in the terrestrial atmosphere has varied, but the variation 134 K.J. HSÜ

has been moderated because there is life on Earth. A living organism makes sugar out of carbon dioxide and water. After the organism dies, its dead body is changed back into carbon dioxide and water. As it is said by Jesus: Render to Caesar the things that are Caesar’s, and to God the things that are God’s (Matthew 22:21). In a perfect carbon-recycling process, as much carbon dioxide is returned as it has been utilised by living organisms. At the same time, the planet’s atmosphere should get increasingly enriched by the volcanic carbon dioxide. A perfect recycling by living organisms would thus have given rise to an increasingly denser atmosphere of carbon dioxide. Fortunately, the recycling has not been perfect: a small fraction of life’s dead remains have been fossilised. In coastal swamps, for example, plant remains are carbonised. On tidal flats, cyanobacteria precipitate carbon as calcium carbonate. The carbon-fixation reactions are common sedimentary processes on Earth: dead plants make coal, and cyanobacteria make limestone. There has never been too much, nor too little carbon dioxide in the terrestrial atmosphere. The carbon-cycling on Earth can be compared to moneycirculation in market-economy. More money in circulation causes an inflation. And fear of inflation makes the Federal Reserve Board to increase of interest-rate. The rate hike discourages borrowing and serves to reduce the money circulation, effecting a deflation. Deflation can lead to recession or even to a great depression. The Federal Reserve has to intervene again, and lower the interest rate at the proper moment inflates the economy. Paraphrasing the economic phrases with scientific jargon, we might state that more carbon dioxide in the atmosphere causes a rise of planetary temperature. Before the Earth’s climate got too hot, carbon-fixing organisms evolved and became dominant. They were the “air-conditioners;” they could remove atmospheric carbon dioxide to decreases the global temperature. Global chill can, and did take place several times in the Earth history, and there were ice ages. Gaia has, however, always had newly evolved organisms, which could render a net increase of greenhouse gases in the atmosphere: they were the “heaters.” The biologic evolution on earth has been an alternate dominance of the “air-conditioners” and the “heaters,” to moderate the climate changes on Earth. Venus is dead, even if there ever was life. The organisms that might have once existed were not sufficiently efficient “air-conditioners” to take out enough carbon dioxide from the planetary carbon-

cycling. Venus was to get steadily hotter till the planet became uninhabitable. Mars is dead, even though there may have been life. The living organisms were not sufficiently efficient “heaters” to maintain enough carbon dioxide in Martian atmosphere. With a steady loss, the Martian greenhouse became insufficient to prevent the freezing of the planet. Mars died perhaps some 3 billion years ago, when the solar energy radiated by Sun was only a fraction of what it is now. Without an effective protection by greenhouse gases, no life could exist on Mars. The Earth has the blessing of Gaia: Earth has escaped the fate of Venus or of Mars. How did Gaia manage?

GAIA’S STRANGE ATTRACTORS Climate is an essential environmental factor in our survival. Life prevailed on Earth indicates because the ocean has never boiled nor has it ever been completely frozen to bottom. Gaia has given us a “terrestrial thermostat”, and her regulators are the living organisms. The carbon-cycling by the various forms of living organisms has played the critical role in determining whether the Earth was glaciated or ice-free. Continental glaciers left their signatures in the moraines. Moraines indicative of the last Ice Age are found in Scandinavia, in central Europe, and in North America. Moraines indicative of ancient glaciations are present in older rock formations. The last Ice Age ended only 15,000 years ago. There was an older ice age 350 to 300 million and another 650-600 million years ago. An ice age is not a period of continuously cold climate. The most recent Ice Age lasted for about 2 million years, but it was not always chilly. Giant ice caps covered Europe, and North America during the glacial stages only. The climate was as warm or even warmer than that of the present during the interglacial. The cause for the alternation of glacial and interglacial stages is now attributed to astronomic factors which govern the flux of solar radiation on earth. There has to be, however, an ultimate cause for ice ages, because the earth’s climate has to be cooled down to such an extent before astronomical factors could trigger alternating glacial and interglacial stages. This ultimate cause for the last Ice Age is the steady reduction of the greenhouse gases in terrestrial atmosphere during the last 100 million years.

The present atmosphere has a small concentration of 0.03% carbon dioxide Carbon dioxide absorbs solar radiation, like the glass of a greenhouse, and causes thus atmospheric warming. Theoretical computations indicate that a doubling of the atmospheric carbon dioxide would cause a rise of earth’s surface-temperature by a few degrees celsius. When the atmosphere is depleted of carbon dioxide, the earth’s surface is cooled down. There is geochemical evidence relating atmospheric carbondioxide to climate, but why should the concentration of carbon dioxide ever vary? The variation is a matter of balancing supply and demand. The ultimate source of terrestrial carbon dioxide is volcanic eruption and the sink is carbon sedimentation. The input and deposition cannot always be balanced, and the atmospheric carbon dioxide has been enriched or depleted in response to the evolution of the dominating life forms on earth.

TIME AND CHANCE Geochemical studies indicate that the total living biomass on earth has remained more or less the same during the last three and half billion years, but the kinds of the living biomass have been changing in the course of evolution. In the beginning, some 4 billion years ago, life was sparse or absent on Earth. Volcanism was producing carbon dioxide at such a rate that the primeval world was becoming too hot to be habitable. Gaia intervened: there had to be life to do the “air-conditioning.” The primeval atmosphere consisted of nitrogen, carbon dioxide and methane, and there was no oxygen. The only organisms that could have survived under such anoxic condition were anaerobic bacteria. When they died, their dead bodies should have been changed back into carbon dioxide and water. Some parts, however insignificant, were fossilised as organic carbon and buried underground to become graphite. The rate of carbon-burial was slightly greater than the rate of carbon-input from volcanism. The consequence was a systematic depletion of atmospheric carbon dioxide and global cooling. The “air-conditioning” by anaerobic bacteria was becoming too effective some three billion year ago: there was a threat of frigidity. The Earth was on its way to become too cold to be habitable. Gaia intervened: there had to be “heaters.” GAIA AND THE MEDITERRANEAN SEA 135

Those were methanogenic bacteria. The bacteria ate up calcium carbonate in anoxic environments to produce methane (CH4), a greenhouse gas even more effective than carbon dioxide. The methanogenic bacteria worked hard, and Earth was getting too warm after half a billion years. Gaia had to intervene for the third time: the world would now again be given to the “air-conditioners.” Cyanobacteria, also known as blue-green algae, are seen today forming algal matts on tidal flats. Their photosynthetic activities cause the precipitation of lime muds, to be lithified as limestones with layered structures called stromatolites. The ancient cyanobacteria too were doing too good job, and Earth was to be covered by ice on continents some two billion years ago. Gaia had to interven once more: there had to be “heaters.” Photosynthesis produced oxygen. The terrestrial atmosphere became oxygenated two billion years ago, and the condition was ripe for the survival of animals, which breathed oxygen. Worms started to evolve some 1 billion years ago. They burrowed in muds, feeding on cyanobacteria. After they died, their decayed bodies release carbon dioxide to the atmosphere to ameliorate the climate. The climate was ameliorated, but the first “heaters” lost eventually their war, and cyanobacteria continued their dominance to chill the earth. The continental glaciers came again, during several glacial stages 700 to 600 million years ago. The refrigeration was getting so severe when tropical lowlands were being glaciated. Now Gaia had to produce more “heaters.” Medusa-like animals made a first appearance 600 million years ago. They were to become increasingly dominant while the worms continued to feed on cyanobacteria. Now the combined efforts of those “heaters” won the war: the Earth came out of an ice age, and the road was open to the “Cambrian Explosion”. The end of glaciation coincided in the timing with the dominance of soft-bodied animals. They are called the Ediacarans, named after the locality in Australia where first such fossils were found. Then the Ediacarans went too far, and Gaia had to produce more “air-conditioners”, The event is called “Cambrian Explosion” because there was apparently an explosion of evolutionary development. Is it an explosion or is it only apparent? Conventional wisdom tells us that life started at the beginning of the Cambrian 550 million years ago because no fossils have been found beneath a geo136 K.J. HSÜ

logical formation called Cambrian. It seems that the diverse life appeared suddenly and simultaneously every where. Even more puzzling is the fact that almost all major groups of the animal kingdom are represented by Cambrian fossils. The term “Cambrian Explosion” has been coined to describe an apparently explosive development. Religious fundamentalists who style themselves as Old-Earth Creationists have seized upon the evidence to support their contention that life was created by God at the beginning of the Cambrian Period. Even a Neo-Darwinist like Stephen Jay Gould assumed an explosive beginning of life, and evolution was portrayed as a process of natural selection by eliminating the unfit; only the favoured races have been preserved because they have been adaptable to changing environments. Recent discoveries suggest that so-called explosion is not real. The apparent simultaneous appearance of many organisms is an artifact of fossilpreservation. Assuming that all the first animals were skeletal and preserved as fossils, paleontologists postulated that the ancestors of practically all of the living animals were created during the 30 million years of the Cambrian Period. The numerous findings of Precambrian boneless fossils indicate that the evolution of animals started at a far earlier date. Worms left their trails on tidal flats 1000 million years ago. Sponges evolved and their silica spicules were found in rocks 800 million years old. Then came the medusa-like Ediacaran animals, and they were already diversified 600 million years before present. Other fossil faunas with their soft parts preserved have been found in Cambrian formations. The first animals were not created at the beginning of the Cambrian Period; they had evolved during the Precambrian age from ancestors that had no calcareous skeletons (Hsü, 1996). Toward the end of the Precambrian time, the ubiquitous algal-matt communities were destroyed by the Ediacarans. Calcium carbonate was thus no longer precipitated on tidal flats. The consequence was the release of CO2 to the atmosphere and the flux of calcium to the ocean. Some of that was taken up by green algae that precipitated calcium carbonate, but enough excess was there to cause an increasing concentration of calcium ions in marine waters. Eventually at the beginning of the Cambrian Period, the open ocean became, for the first time in Earth history, saturated with calcium carbonates. Marine animals could now form calcareous hard parts. The evolution of skeletal organisms

can thus be considered Gaia’s counter-measure to curb the Ediacarans’ extreme. She had her new “air-conditioners” and the climatic trend was reversed. Skeletal organisms were not enough, and the Earth was getting still hotter. Gaia needed more “air-conditioners”, and they came in the form of land plants. The warm lowlands were forested. Trees grew, taking carbon dioxide from air, and trees died, storing the carbon as coal underground during the Carboniferous Period. Gaia’s “air-conditioners” again overdid it. The atmospheric carbon dioxide was almost depleted through the spread of the forests. The consequence was another continental glaciation some 300 million years ago. Tropical forests could not survive in such glacial chill, and they were replaced by tundra vegetation or by desert plants. The sparse vegetation gave back (after their demise) to the atmosphere what they had taken. The greenhouse gases were further replendished by volcanism. The Earth was heating up again. Polar ice caps were melted, and shelf seas inundated the continents. The warm climate driven to the extreme was not to produce unhealthy marine habitats. The thermal stratification of the ocean caused periodic stagnations. Some 150 to 100 million years ago, the deficiency of oxygen in ocean water was a hostile environments to ocean life, and there were great dyings of bottom-dwelling animals. Gaia had to intervene again! Trees, the proven “air-conditioners”, were called back, although the newcomers belonged to a new class; they were the ancestors of the flowering plants. Photosynthesis extracted atmospheric carbon dioxide. Calcareous plankton, another kind of “air-conditioners”, also evolved, and they withdraw calcium carbonate from seawater to make pelagic limestone. Both effected a depletion of the atmospheric carbon dioxide. There was a steady cooling of the global temperature during the last 100 million years. Eventually, some 40 million years ago, the Antarctic Ice Cap came and expanded. The albedo of Antarctic ice, the heattransfer by Antarctic Bottom Water (AABW) all contributed to further chilling. The nutrient-transfer by AABW brought phosphorous to the tropics for the blooms of calcareous plankton, cauing further reduction of the terrestrial greenhouse gases. The Earth got colder and colder, and an ice age finally came to the Northern Hemisphere 2 million years ago.

GAIA’S KIDNEY We usually think of our kidneys in connection with their function of producing urine. Another important function of the kidneys is to maintain the composition of our body fluid, our blood, our “internal environment”. The kidneys play a vital role in the precise conservation of salt and water. The body fluid, the circulating blood of Gaia is the ocean, and ocean consists of salt and water. The salt content of ocean water is its salinity. Ocean water trapped in ocean sediments as old as two hundred million years has been routinely analysed by scientists of the Deep Sea Drilling Project. There is no evidence that the ocean water has changed its salinity significantly in the course of the more recent geologic history. Paleontological criteria have verified this conclusion through studies of the habitats of marine organisms. There are normal marine organisms. There are hypersaline, brackish-water or euryhaline organisms. Those organisms live in normal marine, hypersaline, brackish, or euryhaline environments now and they lived in those respective environments during the geologic past. Some organisms, such as bryozoans are very sensitive indicators of the varying salinity of normal marine environments. Specialists among you marine biologists recognise, for example, that the different species of bryozoans live in seawater of slightly different salinity off the Mediterranean coast. The ocean water, like carbon dioxide, comes from the Earth’s interior. The Earth has an ocean, but the moon does not, because the terrestrial gravitational field is sufficiently great to minimize the escape of water vapour from the atmosphere. The vapour condensates and is precipitated in part as rainfall into the ocean, whereas the rainfall on land also finds its way to the ocean. The mineral content of the ocean comes from the erosional debris of rocks on continent transported by rivers into the ocean. Sand, silt, clay, and other relatively insoluble detritus are deposited as detrital sediments. Trace elements are absorbed, at least in part, by living organisms or by sediments and thus removed from the ocean water. More soluble major constituents remain dissolved, and they include sodium, magnesium, potassium and calcium cations, and chloride, sulphate and biocarbonate anions. The ocean salinity range from 32 to 36‰, with an average of about 34.5‰. The average area of ocean is 360 million km2, and the mean depth is 3.7 km. The total volume of GAIA AND THE MEDITERRANEAN SEA 137

the ocean water is thus 1350 million km3, weighing 1.4 x 1018 tons The total salt content of the oceans is thus about 5 X1016 tons. The earth is 4.5 billion years of age. The annual influx of salt should have been 107 tons per year, if all the soluble salts brought to the ocean stay dissolved in the ocean water. Another approach to estimate the annual influx of salt is to calculate the annual water-badget. Assuming an average evaporative rate of 1.2 m per year, the annual water loss of ocean due to evaporation should be about 0.4 million km3. Of those some 3/4 or 0.3 million km3 should have fallen directly back to the ocean, and some 1/4 or 0.1 million km3 represents annual river-discharge. Assuming that the ocean water-volume has not changed, the annual salinity change results from the addition of dissolved material brought in by rivers. The dissolved matter in regions of very wet climate has a very small concentration of 0.1 g/l, i.e., 105 tons per km3 (Clarke, 1924). Using this minimum value as the average for all river-inputs, the annual salt influx to the ocean should have been 1010 tons. The accumulation of salts in the oceans during the last 4.5 billion years should have been about 5 x 1019 tons, i.e., a thousand times more than that calculated on the basis of the salt balance of the oceans. One could assume, of course, the current input has been grossly over-estimated because of the very large land area and the very high erosional rate at the present time. Nevertheless the discrepancy is too great to be overlooked. Furthermore, giant salt formations are present on Earth, and the salt ions must have been removed. Considering Gaia as a self-organizing system, we could ask if she has a kidney? Has her kidney played a vital role in maintaining the salinity of the seawater? Where is her kidney?

THE MEDITERRANEAN SEA WAS A DESERT The Mediterranean Sea 20 years ago was a broad seaway linking the Indian and Atlantic Oceans. With the collision of the African and Asiatic continents and the advent of mountain-building in the Middle East about 15 million years ago, the connection to the Indian Ocean was severed. Meanwhile, the communication to the Atlantic was maintained only by way of two shallow straits: the Betic in southern Spain and the Riphian in North Africa. The Mediterranean environment gradually deteriorated. The Mediterranean 138 K.J. HSÜ

bottom waters, especially those in the eastern basins, became more and more stagnant, leading inevitably to the extinction of bottom dwellers. The swimming and floating populations struggled for existence. As the salinity of the Mediterranean Sea became abnormal, only euryhaline forms survived. The Mediterranean Sea has an area of 2.5 million km2, an average depth of 1.5 km. The water volume of the Mediterranean Sea is thus 3.7 million km3. Lotze (1967) gave the following water balance: E - (P + R)= I - O where E, the annual volume loss by evaporation is 4.69 x 103 km3 P, the annual precipitation is 1.15 x 103 km3 R, the annual volume delivered by river inflow is 0.233 km3 I, the estimated inflow from the Atlantic is 55.2 x 103 km3 O, the estimated outflow to the Atlantic is 51.89 x 103 km3 The net loss of the Mediterranean E - (P + R) amounts to 3310 km3 annually, and this loss has to be compensated by an inflow from the Atlantic. Geological evidence indicates that the net inflow was considerably less than the net loss, and the Mediterranean sea-level was once drawn down until a complete desiccation (Hsü et al., 1972). The history of the Miocene Salinity Crisis has been documented by the Upper Miocene sediments on land. Müller and Hsü (1987) suggested the following scenario for the salinity crisis on the basis of their studies in Spain. The Mediterranean basins were almost completely dry at about 5.7 million years before the present. The isolation was triggered by an expansion of the Antarctic Ice Cap. After a drop of sea level of dozens of meters, the shallow shoal south of the Gibraltar became an isthmus. Canyons were cut by European and African rivers emptied into the Mediterranean basins, with their bottom 2,000 m or more below the global sea-level. The chemical reactions between the desiccated ocean ooze and the groundwaters formed a caliche type of sedimentary rock, called calcaire di base in Sicily. A minor retreat of the Antarctic ice caused a slight rising of the global sea level. The Atlantic water found its way spilling across a series of lakes that extended from Cadiz to Valencia. The seawater flowed through the lakes of descending lake-levels at such a fast rate that the lake water was nearly nor-

mal marine so that coral reefs could grow on lake shores. The Atlantic water cascaded down a grand canyon, which is the now submerged Valencia Trough. Relentless evaporation in seawater in Mediterranean basins caused a conversion of normal saline seawater into brines supersaturated with sodium, potassium and magnesium salts. The average of the Mediterranean Sea is 1.5 km. The thickness of evaporite deposited by a basin full of water filling up the Mediterranean would be only about 20 m thick, if the salt deposit is evenly distributed. If the salt is restricted to the deepest depressions of the Balearic, Tyrrhenian, Ionic and Levantine basins, the thickness of the salt formation from the desiccation of one basin-full of water should be 100 m or so. Seismic evidence indicates a salt thickness of l to 2 km under the abyssal plains of the Mediterranean basins. Obviously, the salt ions have brought in by an influx with a total volume more than 10 times that of the basin, i.e. some 40 million km3 of seawater have cascaded down the Valencia Trough. Geologic evidence dates the salt-deposition to an interval between 5.7 and 5.5 million years before present. The rate of seawater-influx should thus have been 200 km3 per year, a rate larger than that of the Victoria Falls. The influx was not much less than the evaporative loss, because the salt basins were submerged under deep brine-pools when the Lower Evaporite or the Main Salt Body was deposited, the evaporative loss having been one or two orders of magnitude less than the present because of the drastic reduction of the brine-covered area. The salt deposited in the Mediterranean is ions removed from the global ocean. A volume of 40million km3 seawater contains 3 x 1015 tons of salts. If the total salt influx to the oceans was 1010 tons per year, the rivers of the world would have supplied 2 x 1015 tons to the oceans during the 0.2 million years of the Mediterranean desiccation. The reduction of the salinity of the ocean would have been 2%, i.e., the average ocean salinity would have been changed from 34.5 to 33.8‰. If, however, the total salt influx to the oceans was 109 tons or 108 per year, the rivers of the world would have supplied 2 x 1014 or 2 x 1013 tons to the oceans during those 0.2 million years. The reduction of the ocean-salinity would have been 6%, i.e., the average ocean salinity would have been changed to 32.3‰. There has been considerably amount of salt removed from the ocean, but the salinity-change is still sufficiently small not to be detected by any except the most sensitive marine organisms.

Saline giants such as the Mediterranean Evaporite Formation are rare, but not unique, occurrences in the geological record. Comparable giants are the Mid-Cretaceous of the South Atlantic, the Jurassic of the Gulf of Mexico, the Permo-Triassic of Europe, the Devonian of Canada, the Cambrian/Precambrian of the Gondwanaland. Those six giants during the last 600 million years suggest the need for Gaia to maintain her health through the functioning of her “kidney” every 100 million years. This frequency of saline-giant deposition places a limit on the average influx rate of salt ions to the oceans. If the total salt influx to the oceans is 1010 tons per year, some 1018 tons would have been added to the ocean in 100 million years. The ocean salinity would have been 20 times the normal before a saline giant performed its function as a Gaia’s “kidney.” We have no geological evidence that such drastic catastrophe has ever happened. The annual salt influx to the oceans must have been much less. With an annual 5 x 107 tons influx from the continent, the addition would have been 5 x 1015 tons per year after 100 million years. The increase of the ocean salinity would have been 10%, e.g., from about 32.3‰ to 35.2‰. Such a slow change over a long interval should not have been so devastating to influence the ecology of marine organisms. In conclusion, the juggling of figures points out: 1) The addition of salt ions to the oceans cannot have been 1010 tons per year, as estimated by geochemists on the basis of studying the salt flux of Recent rivers. 2) A slow addition of about 5 x 107 tons per year contributes to a gradual increase in ocean salinity, but the change was so slow and so gradual that it could not be manifested by the paleontological and geochemical records. 3) The rapid deposition of dozens of kilometres of salts in isolated basins such as the Miocene Mediterranean is a necessary process in a self-organizing system. Without the removal of the salt ions, and heavy metals such as lead, zinc, osmium, uranium, etc. from normal ocean waters, the world’s ocean would have become uninhabitable. Gaia would have died if she did not have a healthy kidney.

REFERENCES Clarke, F.W. – 1924. The Data of Geochemistry. U.S. Geol Surv. Bull. 770: 1-841. Hsü, K.J., M.B. Cita and W.B.F. Ryan. – 1972. The Origin of the Mediterranean Evaporites. In: W.B.F. Ryan, Hsü, K.J. et al., GAIA AND THE MEDITERRANEAN SEA 139

Initial Reports of the Deep Sea Drilling Project, v. 13, pp. 1203-1230. Hsü, K.J. – 1992. Is Gaia Endothermic? Geol. Mag., 129: 129-141. Hsü, K.J. – 1996. Gaia and Cambrian Explosion. Natural History Musueum, Taichung, Taiwan, 51 pp.

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Lotze, F. – 1957. Steinsalz und Kalisaltze. Borntraeger, Berlin. 465 pp. Müller, D.-W. and K.J Hsü. – 1987. Event stratigraphy and paleoceanography in the Fortuna-basin (SE Spain): A scenario for the Messinian Salinity Crisis. Paleoceanogr., 2: 679-696.

SCIENTIA MARINA

SCI. MAR., 65 (Suppl. 2): 141-152

2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

Sources and fates of silicon in the ocean: the role of diatoms in the climate and glacial cycles* R.C. DUGDALE and F.P. WILKERSON Romberg Tiburon Center, San Francisco State University, 3152 Paradise Drive, Tiburon CA 94920, USA. E-mail: [email protected]

SUMMARY: Diatoms with their fast growth rates and obligate requirement for Si have a unique relationship to the oceanic Si cycle with the potential for controlling the nutrient and CO2 environment of large important areas of the ocean. The new production of diatoms based on both new nitrogen and Si sources is described using a Si-pump based upon the differential regeneration of the two elements. This approach, applied to the eastern equatorial Pacific, showed diatoms to respond as in a Si-limited chemostat, to the low source Si(OH)4 in the Equatorial UnderCurrent. Increased Si(OH)4 results in increased diatom productivity, suppression of non-diatom populations and decreased surface pCO2. The deficiency in source concentrations of Si(OH)4 results from low Si(OH)4:NO3 water originating in the vicinity of the Antarctic Polar Front, a consequence of the extraordinary trapping of Si by the Southern Ocean. In glacial periods this trapping is reduced several fold and likely results in increased Si(OH)4 export to the north, and increased Si(OH)4 production and deposition at the equatorial Pacific which can be expected to reduce surface pCO2. The connections between the eastern equatorial Pacific export production and Southern Ocean Si trapping may provide a major biogeochemical feedback system with implications for contemporary and paleoclimatology. Key words: silicon, nitrogen, phytoplankton, diatom, carbon productivity, Equatorial Pacific, Southern Ocean, paleoclimatology.

INTRODUCTION The biogeochemistry of silicon (Si) is the focus of considerable contemporary attention by geochemists, paleoceanographers and paleoclimatologists. Biologists are showing revived interest in the Si cycle in relation to diatom productivity as it’s very strong role in marine productivity (e.g. Smetacek, 1999) and effect on ocean-atmosphere processes becomes apparent, following a period in which the focus was almost exclusively on smaller and smaller planktonic organisms. The objective of this communication is to review the role of biologi*Received June 8, 2001. Accepted July 5, 2001.

cal processes in the formation of the ocean Si environment first at the broad scale and then in more detail in two special settings, the equatorial Pacific and the Southern Ocean. In doing so, we will follow the evolution of a set of nitrogen (N) based models, that conclude with inclusion of Si and it’s impact on global carbon cycles and paleoclimatology. We will examine the differences between the oceanic Si and N cycle, the existence of areas of unusually low silicate relative to nitrate concentrations and how we think they are formed. The concept of the Pacific equatorial upwelling area as a Si limited chemostatlike system and the model complexity necessary to describe its functioning will be presented. The low Si(OH)4 condition of the equatorial Pacific SOURCES AND FATES OF Si IN THE OCEAN 141

upwelling system will be discussed, along with possible connections between the equator and the Southern Ocean with implications for contemporary and paleoclimatology. This communication is by no means a broad and unbiased view of a piece of modern oceanography, but rather traces the evolution of our present ideas on the role of diatoms in some key ocean processes. Dissolved silicon enters the ocean as silicic acid or silicate (Si(OH)4) from the rivers as a result of weathering of siliceous rocks although some enters also from atmospheric deposition of particles. Through the action of the Broecker conveyer belt (Broecker and Peng, 1982), Si(OH)4 is fractionated between the major ocean basins with the result that the Atlantic Ocean is generally poor in Si(OH)4 at depth compared to the Pacific where very high concentrations up to 170 mmol. m-3 occur in the deep water of the north Pacific (Rageneau et al., 2000). Deep waters from each basin are drawn into the Antarctic Circumpolar Current and released in slow northward currents to furnish water for upwelling. However, a large portion of the annual input of Si to the oceans is trapped in the Southern Ocean through production of biogenic silica (BSi) primarily by diatoms, and exported to the ocean bed, forming a circumpolar band of high Si sediment.

THE CONTRAST IN ELEMENTAL REGENERATION OF SILICON VERSUS NITROGEN The difference between N and Si regeneration can be seen qualitatively in Figure 1, representative of much of the world ocean. Nitrate (NO3) increases more rapidly with depth than Si(OH)4 and reaches a maximum value at relatively shallow depths. Si(OH)4 increases more slowly with depth and continues to increase almost all the way to the bottom depths of the ocean. While organic nitrogen is degraded and oxidized through microorganismal activity high in the water column, the Si from diatom shells or tests is re-dissolved by chemical processes more slowly as particles containing BSi sink. The nitrogen production and regeneration cycle can be diagrammed simplistically as in Figure 2. New nitrogen sources to the euphotic zone are NO3 advected vertically, fixation of atmospheric nitrogen (N2) and ammonium (NH4) and NO3 contained in precipitation. NH4 produced by bacterial degradation of particulate organic nitrogen (PON) occurs 142 R.C. DUGDALE and F.P. WILKERSON

FIG. 1 – Vertical distribution in the Pacific Ocean of NO3 and Si(OH)4 (mmol. m-3) measured off the California coast, USA, June 2000 (station A8) during CoOP WEST (http://ccs.ucsd.edu/coop/west/) cruise.

mainly in the upper portion of the water column, usually within the euphotic zone. NH4 escaping to depth is oxidized to NO3 and so is nearly undetectable in most subsurface waters. The concept of fractionation of nitrogen into new and regenerated forms, and the use of 15N labeled tracers, made it possible to identify the primary production based on new nitrogen sources (new production) and on regenerated nitrogen (regenerated production) (Dugdale and Goering, 1967). The utility of the concept lies in the value of new production setting the upper limit for loss rates, e.g. export production or sedimentation (Eppley and Peterson, 1979) and yield to

FIG. 2 – Schematic diagram of the oceanic nitrogen production and regeneration cycle.

FIG. 3 – Schematic diagram of flow of nitrogen and silicon (Sipump) in a diatom-containing oceanic ecosystem (taken from Dugdale et al., 1995).

higher trophic levels (predation). The proportion of new to total N production (the f-ratio) varies widely, from about 0.1 in oligotrophic systems to 0.8 or more in eutrophic conditions (e.g. Dugdale and Wilkerson, 1991, 1992).

LOW Si(OH)4-HIGH NO3 LOW CHLOROPHYLL AREAS Since diatoms typically dominate new production (Goldman, 1988), a Si pathway was added to the new and regenerated nitrogen model, based on the premise that Si re-dissolution occurs below the euphotic zone. In the Si-pump model (Fig. 3) (Dugdale et al., l995), no regenerated Si pool is allowed in the euphotic zone. Si is taken up by Si(OH)4users, primarily diatoms, and exported through sinking of cells or fecal pellet formation and sinking. In this model all Si(OH)4 uptake is new production and

FIG. 4 – Time series of NO3 and Si(OH)4 concentrations (mmol. m-3) in the mixed layer predicted by a simple Si-pump model (taken from Dugdale et al., 1995).

available for export. The assumption of zero re-dissolution in the euphotic zone is not strictly true, but the general condition, that Si regeneration in the euphotic zone is slower than for nitrogen or phosphorus is certainly correct in most circumstances. Application of this simple model to a continuous upwelling system showed that with time, such systems are driven into Si limitation (Fig. 4) (Dugdale et al., 1995). The principle is simple, new nitrogen (NO3) gets used more than once through regeneration, Si is used only once before being exported. Some ocean systems have been described as productivity paradoxes, in that measurable nutrients are observed with little response by the phytoplankton and resulting in low chlorophyll concentrations. However, these areas, first designated as high nutrient, low chlorophyll (HNLC) areas by Minas et al. (1986), although exhibiting unused NO3, often were even lower in Si(OH)4, suggesting these areas were Si(OH)4 limited for diatoms. Some of these areas were re-designated as low silicate-HNLC (Dugdale and Wilkerson, 1998) and included the Southern Ocean in the region of the polar front, the region between the Peru/Ecuador coast and the Galapagos Islands, and the Eastern Equatorial Pacific (EEP) (Dugdale et al., 1995). The basis for this Si(OH4) limited situation is likely the Si-pump mechanism described above.

THE Si-PUMP IN THE EASTERN EQUATORIAL PACIFIC UPWELLING ECOSYSTEM Upwelling occurs (in the EEP) more or less continuously in a narrow band about 1 degree north and south of the equator driven by the trade winds, with some seasonal changes in intensity (Philander, 1990). Nutrient concentrations are easily detectable in the euphotic layer, NO3 ≈ 5 mmol. m-3, Si(OH)4 about 2 mmol. m-3 and NH4 ≈ 0.1 mmol. m-3 (e.g. Peña et al., 1990; Barber and Chavez, 1991). Chlorophyll concentrations are ≈ 0.1 mg m-3. New production has been measured using 15NO3 at ≈ 0.8 3.0 mmol N m-2 d-1 (5-20 mmol C m-2 d-1), with measured f values about 0.1 to 0.2, (e.g, Dugdale et al., 1992; McCarthy et al., 1996) indicating that most primary production is based on regenerated nutrient supply. Growth rates of the phytoplankton are rapid, approaching one doubling per day (Cullen et al., 1992). The paradox of the equator is the presence of nutrient in surface waters and the low phytoplankton biomass (Barber, 1992). Walsh (1976) was the first SOURCES AND FATES OF Si IN THE OCEAN 143

to suggest that grazing controlled the biomass of this ecosystem and Frost and Franzen (1992) incorporated grazing into an equatorial chemostat like model. Grazing was incorporated as the major loss rate since the growth rate of phytoplankton calculated from the physical dilution rate (as in a classical chemostat) gave unrealistically low values at variance with measured growth rates (see below). Lack of iron (Fe) was suggested as the agent of low biomass and new production also but has not proved to be the primary cause as will be discussed below. Si(OH)4 limitation was implicated by Ku et al. (1995). Using 228Ra, they computed the vertical flux of Si(OH)4 to the upwelling zone of the EEP and concluded that diatoms would be Si limited in that ecosystem. Although the equatorial Pacific phytoplankton biomass was known to be dominated by picoplankton (Chavez et al., 1996) a strong role for diatoms in equatorial new production was indicated by a plot of NO3 vs. Si(OH)4 for data from 140ºW, 0.5ºN with a slope of 1:1 (Dugdale and Wilkerson, 1998). Landry et al. (1997) found a very strong correlation between diatom chlorophyll and 15NO3

uptake in the EEP during US JGOFS (Joint Global Ocean Flux Studies). However, measured f values for the equatorial Pacific upwelling were low, 0.1 to 0.2 and to accommodate this information and the known biomass dominance of the picoplankton, a model based upon the Si-pump model was proposed in which the NO3 was taken up by the diatoms and the NH4 arising from grazing on diatoms was taken up by the picoplankton (Dugdale and Wilkerson, 1998). This idea was not very popular since it was already known that some picoplankton, e.g cultured isolates were capable of NO3 uptake as well as NH4, and it turned out that the 1:1 Si:NO3 slope used to fit the model was an extreme case and a wide range of Si:NO3 slopes could be observed in the equatorial system (Dunne et al., 1999). Recent work suggests that NO3 assimilation may not be universal in all picoplankton and the gene for NO3 assimilation may be lacking in some Synechococcus and Prochloroccocus species (Zehr, pers com.) Nevertheless, this simple model was a step on the way to the development of a more realistic equatorial productivity model.

FIG. 5 – The inter-compartmental flow diagram of the 1-D model for the EEP (taken from Chai et al., in press).

144 R.C. DUGDALE and F.P. WILKERSON

EVOLUTION OF MODELS FOR THE EEP INCORPORATING THE Si-PUMP A one dimensional (1-D) model of the equatorial Pacific upwelling system (Fig. 5) (Chai et al., in press) was then constructed by adding the Si-pump to the model of the EEP ecosystem of Chai et al. (1996). The essential features include incorporation of two phytoplankton components (diatoms and picoplankton, i.e. Si(OH)4 and non Si(OH)4-users) three macro-nutrients, NO3, NH4, and Si(OH)4, Fe as an indirect effect on photosynthesis, and two sizes of zooplankton (microzooplankton and mesozooplankton). Both fractions of the phytoplankton use NO3 and NH4, only diatoms use Si(OH)4 which is not regenerated in the model (a procedure justified by a sensitivity analysis that showed only very low regeneration values gave reasonable steady state solutions; Dugdale et al., in press a). The model was initialized with mean nutrients from Levitus et al. (1993) at 120m for the Wyrtki box (90-180ºW,5ºN-5ºS) and with rate constants and biomass from the literature (Chai et al., in press). The model is very stable and steady state values are generally close to observations, as shown in the model and field data from JGOFS cruise TT011 (Murray et al. 1995), describing the vertical distribution of Si(OH)4 and NO3 (Fig. 6). The surface Si(OH)4 concentration, about 3 mmol. m-3 is about half that of NO3 and the shapes of the curves from data are reproduced faithfully by the model. At the source depth of nutrients for the model (120 m) Si(OH)4 concentrations are lower than for NO3, a condition that would lead to Si limitation of diatoms in a conventional chemostat. However, both the model and the equatorial ecosystem are not exactly equivalent to a conventional chemostat since a mixture of Si(OH)4-using algae and non Si(OH)4users are present, and the loss rates are dominated not by dilution but by grazing of zooplankton.

ACHIEVEMENT OF STEADY STATE IN A CONVENTIONAL CHEMOSTAT Steady state in a conventional chemostat is achieved through the interaction of loss rates and the nutrient uptake kinetics of the organism being continuously cultured. The loss rate (= dilution rate, D) is set by the experimenter by manipulating the flow rate of the nutrient mixture designed to assure limitation of a particular nutrient (F) or the volume of the reactor or culture vessel (V):

FIG. 6 – Comparison of NO3 and Si(OH)4 concentrations from the 1-D model (no symbols) and observed data from JGOFS TT011 cruise (Murray et al., 1995) from 2.5°N (with symbols).

D=µ=F/V

(1)

where µ is growth rate. Provided the maximum growth rate of the organism is not exceeded by the value of D, regulation occurs usually through the Michaelis-Menten equation: V = Vmax * S/(KS + S)

(2)

where S is the concentration of the limiting nutrient and KS is the half-saturation concentration, i.e. the concentration at which the value of V = 1/2 Vmax. The value of D selected by the experimenter sets the steady state value of S and the difference between S and the concentration of the limiting nutrient in the feed, Sf , determines the biomass (B) of the organism in the reactor: B = (Sf - S)

(3)

P = (Sf - S) / Q

(4)

or as cell numbers:

where Q is the concentration of limiting nutrient per cell. The negative feedback mechanism forcing steady state is through the biomass in the reactor. If the biomass exceeds the steady state value, the concentration of the limiting nutrient decreases below the steady state point and the growth rate is reduced until the concentration of S in the reactor increases and the SOURCES AND FATES OF Si IN THE OCEAN 145

growth rate is again at steady state. A complication in chemostat culture of some algae occurs when the cell quota is reduced at low growth rates, tending to maximize the number of cells (e.g. Droop, 1974; Davis et al., 1978). The effect of a reduced cell quota was considered by Dugdale (1976) and can be detected as an increase of Vmax. When appliying chemostat theory to the EEP as a Si-limited system, the effect will be ignored as the kinetics of Si uptake measured on the equator (Leynaert et al., 2001) appear to be unmodified by a variable quota effect.

ACHIEVEMENT OF STEADY STATE IN THE 1-D EQUATORIAL MODEL A sensitivity analysis of the 1-D model for the EEP to changes in source Si(OH)4 showed the diatom population to be limited by Si, the Si(OH)4 concentration varying around a steady state value depending on the loss rate which in turn sets the growth rate. This is appropriate as in the 1-D model Si(OH)4 uptake follows the Michaelis-Menten equation with a KS of 3.0 mmol. m-3. The range of VSi in the model (0.5 to 0.8 d-1) with the source Si concentration varied

from 3 to 15 mmol. m-3 reflects the values of the loss rates for the diatom population and the diatom growth rate, assuming steady state. This value is to be compared with the dilution rate, equivalent to the upwelling rate of 1m. d-1 divided by the depth of the mixed layer (60 m), which equals 0.014 d-1 , very low compared to the VSi values, and shows the dilution model for loss is incorrect for this system. In the 1-D model, specific loss rates due to zooplankton grazing range from 0.45 to 1.1 d-1 indicating that the major loss in the EEP is grazing, not dilution. The main point to be understood for a chemostat-like system such as the equatorial Pacific upwelling is that the loss rate sets the steady state growth rate which in turn requires a specific Si(OH)4 ambient concentration to achieve a balance between loss and growth. This concept is frequently not understood and for example, the question has been asked “why isn’t all of the Si(OH)4 used up if Si(OH)4 is the limiting nutrient?” The answer is that the Michaelis-Menten relationship requires a finite amount of substrate to drive the uptake reaction at the level set by the loss rate. This is somewhat counter-intuitive and requires thinking about the system from the loss end rather than from the growth end.

FIG. 7 – Surface response of the 1-D model to changes in source Si(OH)4 concentration, a) phytoplankton biomass (mmol m-3), b) nutrient concentrations (mmol m-3), c) zooplankton biomass, (mmol m-3), d) NO3 uptake (mmol m-3 d-1), e) TCO2 (mmol m-3).

146 R.C. DUGDALE and F.P. WILKERSON

IMPORTANCE OF Si(OH)4 SUPPLY ON DIATOM COMPETITION IN THE EEP The functioning of this complex ecosystem 1-D model for the EEP can be discerned from Figure 7 illustrating changes resulting from varying the source Si(OH)4 concentration from low to high (3 to 15 mmol. m-3) holding NO3 concentration constant at 12 mmol. m-3. The interaction between diatoms and picoplankton is one of the interesting features of the 1-D model results. As source Si(OH)4 increases, diatoms increase in biomass as expected, but the picoplankton decrease strongly and then remain at a lower concentration (Fig. 7a). Ambient Si(OH)4 increases (Fig 7b) in response to increased mesozooplankton grazing on diatoms (Fig. 7c). NH4 concentration increases due to enhanced mesozooplankton grazing and nitrogen regeneration. NO3 concentration increases initially, due to the decreased NO3 uptake by the picoplankton – a result of inhibition by NH4 – then decreases as source Si(OH)4 exceeds the intermediate range (7.5 mmol. m-3) as the diatom population increases. The decrease in picoplankton NO3 uptake that occurs as source Si(OH)4 increases from low to intermediate range, results in a decrease in total phytoplankton NO3 uptake (Fig. 7d). An important consequence of the apparent suppression of picoplankton by an increasing diatom population is the bell shaped TCO2 vs. source Si(OH)4 concentration (Fig. 7e) due to the link between carbon uptake and NO3 uptake. A maximum in surface TCO2 occurs at intermediate source Si(OH)4 concentrations (Fig 7e), whereas TCO2 is reduced at higher source Si(OH)4 concentrations as diatoms increase. Whether this 1-D model result occurs in nature is unresolved at present. An alternative to the hypothesis that diatoms directly impact picoplankton populations is that the picoplankton remain constant and only diatoms and other phytoplankton change in biomass (Le Borgne, pers comm.). Coccolithophorids incorporate carbon from CO2 to form soft parts as do other phytoplankton, but also take up bicarbonate to form their carbonate (calcite) shells. The incorporation of carbon for soft parts reduces the TCO2, but the formation of calcite results through reduced alkalinity (from withdrawal of calcium ions) in an increase in CO2 such that the final result is that pCO2 increases as a result of cocolithophorid growth. Since diatoms, however, reduce TCO2 and pCO2 directly, the proportion of primary production accomplished by diatoms compared to coccolithophorids has the potential to influ-

ence strongly the marine carbon cycle. Consequently, understanding the factors that control the relative success of these two functional groups of phytoplankton is central to understanding the role of biology in the carbon processes of the ocean. Harrison (2000) has proposed that changes in Si(OH)4 supply by influencing the relative success of diatoms and coccolithophorids may have been a key to glacial/interglacial transitions. Mesocosm experiments conducted with semi-continuous nutrient additions showed that a coccolithophore, Emiliania huxleyi, and other picoplankton as well, are unable to compete with diatoms when Si(OH)4 concentrations are above about 2 mmol. m-3 and PO4 and NO3 are present in non-limiting concentrations (Egge and Aksnes, 1992), and formed the basis for an ecosystem model using three functional groups of phytoplankton (Aksnes et al., 1994).

THE ROLE OF IRON IN Si LIMITATION OF DIATOMS Micronutrients may influence the Si(OH)4 limitation (Si-limited chemostat scenario) for EEP diatoms. Iron is necessary for many cell processes and it may be difficult to isolate the exact sites of Fe limitation in natural populations. However, virtually all Fe enrichments show strong effects on diatom growth. The most likely effect of micronutrients on any phytoplankton process was suggested to be on the production of the amount of enzyme for whatever process is being catalyzed and consequently would be expressed in the value of Vmax in the Michaelis-Menten equation (Dugdale, 1967). Regulation in a continuous culture system would still occur on the primary limiting nutrient (for example Si(OH)4 in the EEP), so that with a constant loss rate, the variation observed would be in the ambient concentration of the limiting nutrient and the biomass of the cultured organism. Fe is upwelled in the EEP along with the primary nutrients including Si(OH)4 (Landry et al., 1997), and considering the high growth rates of both diatoms and picoplankton there does not seem to be a clear limitation by Fe; however the kinetic experiments that would reveal a co-limitation by Fe and Si have not been made in the EEP. Enrichment experiments showed Fe to stimulate phytoplankton growth especially diatoms, in the equatorial Pacific (IronEx-1, Martin et al., 1994; IronEx-2, Coale et al., 1996). However, these experSOURCES AND FATES OF Si IN THE OCEAN 147

iments were made outside the upwelling areas. In our 1-D model for the EEP, we do not include Fe as a limiting nutrient explicitly, but rather consider it’s role implicitly through the parameters that determine the growth rate of diatoms. There are two parameters in our current model reflecting Fe limitation, alpha, α, the slope of the photosynthetic rate over irradiance at low irradiance, and KSi(OH)4, the halfsaturation for Si(OH)4 uptake which varies considerably (Nelson and Brzezinski, 1990; Nelson and Treguer, 1992). When the model was run to mimic an Fe enrichment experiment ecological behaviors similar to these observed during the field Fe enrichment experiments (Martin et al., 1994; Coale et al., 1996; Boyd et al., 2000) resulted (Chai et al., in press).

THE SIGNIFICANCE AND CAUSE OF LOW SOURCE Si(OH)4 CONCENTRATIONS The importance of the low Si(OH)4 condition of the equatorial Pacific upwelling system arises from the control of diatom processes especially new carbon and carbon export production. A major role for the equatorial Pacific in the global ocean/atmospheric CO2 exchange has been established by the observation that during El Niño events CO2 efflux from the equator falls to virtually zero and the rise in

atmospheric CO2 is reduced or disappears. The 1-D model results suggest that there may be changes in TCO2 at the equator linked to changes in upwelling source Si(OH)4 concentrations. The low Si(OH)4 condition of the source waters for equatorial upwelling, first noted by Ku et al. (1995) is of southern origin. Sections of nutrients across the equator show a strong asymmetry, e.g. (e.g. Carr et al., 1992, their Fig 5) with isopleths sloping more steeply to the south than to the north. At the equator, the source of upwelling water to the surface is from the upper part of the Equatorial Undercurrent (EUC) originating in the far western Pacific and flowing at depths of 100 to 300 m across to the eastern Pacific boundary. The current system in the western Pacific where the EUC originates is complex, (Fig. 8) (Fine et al., 1994). The northern source of water is the Mindanao Current and the southern source is the New Guinea Coastal Undercurrent (NGCUC). Following the approach of Toggweiler and Carson (1995) for NO3 the fluxes of Si(OH)4 and NO3 were calculated for the north and south sources (Dugdale et al., in press b), and showed both sources for NO3 to be about equal. However, only 30% of the total Si(OH)4 supply was from the south, i.e. the Si(OH)4:NO3 ratio was about 0.7 in the NGCUC compared to 1:1 for the northern source water for the EUC. Consequently the mixture of the two waters as the EUC is formed is lower in

FIG. 8 – Current system of the western equatorial Pacific (from Fine et al., 1994).

148 R.C. DUGDALE and F.P. WILKERSON

FIG. 9 – Values of NO3 – Si(OH)4 at 170ºW, 48º-66ºS, calculated from WOCE (World Ocean Circulation Experiment) nutrient data measured during cruise p15s.

Si(OH)4 compared to NO3 and since the average composition of diatoms occurs in the Si:N ratio of 1:1 (Brzezinski, 1985), the composition of the EUC assures the Si limitation of equatorial diatoms in the upwelling region. The cause of Si limitation in the equatorial Pacific is to be found far to the south, in the Southern Ocean where SubAntarctic Mode Water (SAMW), the source water for the NGCUC, is formed at and to the north of the Polar Front (PF) (Tsuchiya, 1991). Although it has been known for some time that surface waters north of the PF are low in Si(OH)4 but high in NO3 (Broecker and Peng, 1982), the process resulting in this distribution has only become clear recently from JGOFS studies of the US and other countries, especially of France. During austral winter, deep mixing results in high concentrations of nutrients in the mixed layer to the south of the PF. In spring, with light and stratification, a diatom bloom begins near the PF and develops in a southerly direction, taking up Si(OH)4 at high rates, but NO3 and carbon at low rates, leaving behind water low in Si(OH)4 and high in NO3 (Nelson et al., in press; Pondaven et al. (2000). The depletion of Si(OH4) relative to NO3 is a factor of 4 or more in this production system, an extreme example of the Si-pump. A circumpolar band of siliceous sediment is the result. This water moves northward first in an easterly direction and then westerly into the NGCUC and to the EUC. The deficiency in south Pacific water is apparent in Figure 9 (WOCE data) where

the Si(OH)4 concentrations have been subtracted from the NO3 values. With diatom requirements for Si:N of about 1:1, the contours indicate the magnitude of the Si deficiency in this water for the support of diatom populations, e.g. values for NO3 minus Si(OH)4 of up to 20 (Fig. 9). Another source of Si(OH)4 to the equatorial ecosystem is the rivers of the western equatorial Pacific which provide up to 20% of the sediment load to the ocean (Milliman et al., 1999). Rivers typically have very high Si(OH)4 concentrations, 200 mmol. m-3 or greater and during normal, non-El Niño years must provide a substantial amount of Si(OH)4 to the nearby ocean, for example, in the section shown in Figure 10, from the coast of New Guinea to 10ºN, a surface layer of low salinity, enhanced Si(OH)4 layer can be seen. The quantitative contribution of Si(OH)4 from this source is at present unknown.

CONNECTIONS BETWEEN THE SOUTHERN OCEAN AND THE EQUATORIAL PACIFIC: IMPLICATIONS FOR PALEOCLIMATOLOGY A role for the equatorial Pacific in glacial cycles is suggested by the extraordinary capacity of the Southern Ocean to trap Si(OH)4 that would otherwise be transported north to the equatorial Pacific, and the capacity of diatoms to export carbon to the deep ocean due to their relatively large size (Michaels and Silver, 1988). Comparing the ocean

FIG. 10. – Meridional section at 143°E, 3°S-7°N of silicate (mmol m-3) from WEPOCS III data (Lukas et al., 1991).

SOURCES AND FATES OF Si IN THE OCEAN 149

sediment distribution of Si with surface ocean pCO2 suggests such a connection; the two major areas of high sediment Si are the Southern Ocean and the equatorial Pacific. The equatorial Pacific is the major oceanic source of CO2 to the atmosphere. Paleoceanographers and paleoclimatologists have been searching for a long-period (long time scale) feedback system to explain the correlation between glacial maxima and atmospheric CO2, which tends to fall steadily during ice buildup to values about 170µatm (100 µatm below the preindustrial level of 270 µatm). Feedback directly through ocean chemistry and current systems to produce changes in new production occur on a time scale that is too short, about 1000 years or a bit less. A feedback with the correct time scale, i.e. tens of thousands of years might occur as the Antarctic ice builds northward, reducing the Southern Ocean trapping of Si. With more Si(OH)4 transported northward to supply the equatorial diatoms, CO2 at the surface ocean would be reduced and atmospheric CO2 would decline, bringing about additional cooling and ice formation. For example, an additional 15 mmol. m-3 Si(OH)4 (to offset the Si deficiency in Fig. 9) transported northward into the equatorial upwelling system would result in a drawdown of 50 mmol. m-3 TCO2. The 50 mmol. m-3 reduction in TCO2 translates to a reduction of 71.5 µatm pCO2 at the ocean surface. Reduced Southern Ocean production in glacial periods is suggested by Charles et al. (1991), Morlock et al. (1991) and Sigman and Boyle (2000) and increased BSi deposition in the central Equatorial Pacific has been shown by Lyle et al. (1988) at glacial maxima.

CONCLUSION Diatoms with their fast growth rates and unique relationship to the Si cycle have the potential for controlling the nutrient and CO2 environment of large important areas of the ocean. The time scales over which these controls or feedback interactions extends from seasonal to El Niño/LaNiña (e.g. in precipitation cycles in the western tropical Pacific) to the glacial/interglacial scale interactions between the Southern Ocean and the equatorial Pacific. Diatom effects may be direct, as in export production of CO2, or indirect through competition or inhibition of other phytoplankton functional groups, e.g. by reduction of picoplankton activity, or by outcompeting coccolithophores. 150 R.C. DUGDALE and F.P. WILKERSON

The broad-based case for such a strong diatom role in global processes rests on analyses of cores by paleoceanographers, on enclosure and shipboard experimentation, and on modeling. Although the 1D model discussed here seem to predict well conditions in the equatorial Pacific upwelling, there are some poorly known, but crucial parameters needed to assess whether we are on the right track and whether the models may be useful in decision making. The modeling exercise opens up a number of questions. Question 1, What is the dissolution rate for BSi in the equatorial upwelling system, the Southern Ocean, or in most of the ocean for that matter? The techniques to make direct isotopic measurements of this rate in areas of the ocean with low phytoplankton biomass are just becoming available. Question 2, Is there a decrease in picoplankton numbers (concentration) as diatom populations and activity increase? The modeled effect of this interaction between different members of the phytoplankton community is through the NH4 inhibition of NO3 uptake formulation, with increased ambient NH4 supplied through increased grazing fueled by increased diatom biomass. New methods to measure phytoplankton communities rapidly (e.g. HPLC pigment analyses and advances in fllow cytometry). Question 3, Do the picoplankton and the diatoms each have a new and regenerated production cycle, i.e. do both take up both NO3 and NH4, or do the diatoms take up the new nitrogen, NO3, and pass part of it on to the picoplankton that are unable to take up NO3. Marine free living and symbiotic cyanobacteria may use atmospheric N2 as a new N source (Carpenter, pers. comm). Size-fractionated measurements of NO3 and NH4 uptake may answer that question, and molecular techniques are just now available to assess the genetic capability to reduce NO3 of both prokaryotic and eukaryotic phytoplankton. Question 4, How do Si(OH)4 and Fe limitation act on diatoms in an area such as the equatorial Pacific where both are supplied by upwelling? The clean sampling techniques and suitable isotopes are available to test this effectively. Question 5, Why do some Southern Ocean diatoms have the bizarre composition ratio for Si, N and C? There are indications that Fe deficiency is the cause (Franck et al., 2000), but any factor that reduces diatom growth rate, e.g. temperature, may have the same effect. An understanding of the factors controlling diatom composition and their variability in the Southern Ocean is crucial to understanding the role of diatoms in trapping so much of the ocean’s Si supply and its poten-

tial role in climate change. Question 6, How can detailed physiological models of phytoplankton growth (e.g. Flynn and Martin-Jezequel, 2000) be incorporated into general circulation models? With the rapid development of super-computing power, adding more compartments and pathways is feasible in near-future oceanographic models. We biologists have a remarkable opportunity to participate in the quest to understand the role of biology in the grand biogeochemical processes of the earth-ocean system. The diatom-Si story is one of these and whose importance is just beginning to be realized.

ACKNOWLEDGEMENTS We wish to thank the National Science Foundation JGOFS-Synthesis and Modeling Program (OCE9802060 to RCD and FPW) and Coastal Ocean Processes Program (OCE-9910898 to RCD and FPW) for financial support, and to SMP investigators for thoughtful discussions at SMP Workshops.

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SOURCES AND FATES OF Si IN THE OCEAN 151

Iron and grazing constraints on primary production in the central equatorial Pacific: An EqPac synthesis. Limnol. Oceanogr., 42: 405-418. Levitus, S., J.L. Reid, M.E. Conkright and R. Najjar. – 1993. Distribution of nitrate, phosphate and silicate in the world oceans. Progr. Oceanogr., 31: 245-273. Leynaert, A., P. Treguer, C. Lancelot and M. Rodier. – 2001. Silicon limitation of biogenic silica production in the Equatorial Pacific. Deep-Sea Res. I, 48: 639-660. Lukas, R., E. Firing, P. Hacker, P.L. Richardson, C.A. Collins, R.A. Fine and R. Gammon. – 1991. Observations of the Mindanao Current during the western equatorial Pacific Ocean circulation study. J. Geophys. Res., 96: 7089-7104. Lyle, M., D.W. Murray, B.P. Finney, J. Dymond, J.M. Robbins and K. Brooksforce. – 1988. The record of Late Pleistocene biogenic sedimentation in the eastern Tropical Pacific Ocean. Paleoceanography, 3: 39-59. Martin, J.H. and IronEx team – 1994. Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean. Nature, 371: 123-129. McCarthy, J.J., C. Garside, J.L. Nevins and R.T. Barber. – 1996. New production along 140°W in the equatorial Pacific during and following the 1992 El Niño event, Deep-Sea Res. II, 43: 1065-1093. Michaels, A.F. and M.W. Silver. – 1988. Primary production, sinking fluxes and the microbial food web. Deep-Sea Res., 35: 473490. Milliman, J.D., K.L. Farnsworth and C.S. Albertin. – 1999. Flux and fate of fluvial sediments leaving large islands in the East Indies. J. Sea Res., 41: 97-107. Minas, H.J., M. Minas and T.T. Packard. – 1986. Productivity in upwelling areas deduced from hydrographic and chemical fields. Limnol. Oceanogr., 31: 1182-1206. Mortlock, R.M., C.D. Charles, P.N. Froelich, M. Zibello, J. Saltzman, L.D. Burkle and J.D. Hays. – 1991. Evidence for lower productivity in the Antarctic Ocean during the last glaciation. Nature, 351: 220-223. Murray, J.W., E. Johnson and C. Garside. – 1995. A U.S. JGOFS process study in the equatorial Pacific (EqPac): introduction. Deep Sea Res. II, 42: 275-293

152 R.C. DUGDALE and F.P. WILKERSON

Nelson, D.M. and M.A. Brzezinski. – 1990. Kinetics of silicic acid uptake by natural diatom assemblages in two Gulf Stream warm-core rings. Mar. Ecol. Prog. Ser., 62: 283-292. Nelson, D.M. and P. Treguer. – 1992. Role of silicon as a limiting nutrient to Antarctic diatoms: evidence from kinetic studies in the Ross Sea ice-edge zone. Mar. Ecol. Prog. Ser., 80: 255-264. Nelson, D.M., et al. – (in press). A seasonal progression of Si limitation in the Pacific sector of the Southern Ocean. Deep Sea Res. II. Peña, M.A., M.R. Lewis and W.G. Harrison. – 1990. Primary productivity and size structure of phytoplankton biomass on a transect of the equator at 135°W in the Pacific Ocean. Deep-Sea Res., 37: 295-315. Philander, S.G. – 1990. El Niño, La Niña and the Southern Oscillation, Academic Press Inc, New York. Pondaven, P., O. Ragueneau, P. Treguer, A. Hauvespre, L. Dezlieau and J.L. Reyss. – 2000. Resolving the “opal paradox” in the Southern Ocean. Nature, 405: 168-172 Ragueneau, O., P. Treguer, A. Leynaert, R.F. Anderson, M.A. Brzezinski, D.J. DeMaster, R.C. Dugdale, J. Dymond, F.G. Fischer, R. Francois, C. Heinze, E. Maier-Reimer, V. Martin-Jezequel, D.M. Nelson and B. Queguiner. – 2000. A review of the Si cycle in the modern ocean: recent progress and missing gaps in the application of biogenic opal as a paleoproductivity proxy. Global and Planetary Change, 26: 317-365. Sigman, D.M. and E.A. Boyle. – 2000. Glacial/interglacial variations in atmospheric carbon dioxide. Nature, 407: 859-869. Smetacek, V. – 1999. Diatoms and the ocean carbon cycle, Protist, 150: 25-32 Toggweiler, J.R. and S. Carson. – 1995. What are upwelling ecosystems contributing to the ocean’s carbon and nutrient budgets? In: C.P. Summerhayes, K.-C. Emeis, M.V. Angel, R.L. Smith and B. Zeitschel (eds.), Upwelling in the Ocean, Modern processes and ancient records, pp. 337-361. Wiley and Sons. Tsuchiya, M. – 1991. Flow path of the Antarctic Intermediate Water in the western equatorial South Pacific Ocean. Deep Sea Res., 38: 273-279. Walsh, J.J. – 1976. Herbivory as a factor in patterns of nutrient utilization in the sea. Limnol. Oceanogr., 21: 1-13.

SCI. MAR., 65 (Suppl. 2): 153-169

SCIENTIA MARINA

2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

Phytoplanktonic biomass synthesis: application to deviations from Redfield stoichiometry* FERNANDO FRAGA Instituto de Ivestigaciones Marinas, Consejo Superior de Investigaciones Científicas, Eduardo Cabello 6, 36208 Vigo, Spain.

SUMMARY: During biomass formation as a result of phytoplankton photosynthesis, CO2 and the nutrients NO3 and PO4 are consumed and O2 produced in fixed proportions known as the Redfield ratio. Broecker’s tracers, i.e., “NO” = O2+RN·NO3, “PO” =O2+RP·PO4, and “CO” = O2+RC·CO2, remain constant during photosynthesis, because nutrients consumed are offset by O2 formation. When one or several nutrients become depleted, the Redfield ratio no longer holds, and the tracers cease to remain constant. The main causes are formation of excess carbohydrates or lipids, N2 fixation, or production of CaCO3 plates by phytoplanktonic populations that have developed different strategies for obtaining the nutrients they need. This paper presents new tracers that remain constant, irrespective of whether or not Redfield stoichiometry is satisfied. Differences between the values of the new tracers and the values of the conventional tracers reveal the presence of anomalies in biomass production. They also allow quantification of any such anomalies, both globally and by depth stratum, and assessment of each individual anomaly separately, even when more than one anomaly occur simultaneously. Key words: Redfield deviations, phytoplankton stoichiometry, dinoflagellates, coccolithophores, cyanobacteria.

INTRODUCTION Organic matter making up the marine phytoplankton is composed primarily of proteins, carbohydrates, lipids, nucleic acids, and photosynthesizing pigments. All these constituents consist of carbon, oxygen, and hydrogen atoms, and additionally the proteins and photosynthesizing pigments contain nitrogen and the nucleic acids contain nitrogen and phosphorus. The phytoplankton takes all these elements from the sea water, where they are present in mineral form. Using their own data on the proximal composition of the plankton together with data published by Fleming (1940), Redfield et al. (1963) *Received February 25, 2001. Accepted June 27, 2001.

established the -O2:C:N:P ratio of 138:106:16:1 based on the finding that the phytoplankton reduced CO2 to carbohydrates and nitrate to ammonia according to the following stoichiometric equation: 106 CO2 + 16 HNO3 + H3PO4 + 122 H2O → (1) → [(CH2O)106 (NH3)16 (H3PO4)] + 138 O2 This equation holds true for carbohydrate synthesis and provides a good approximation for protein synthesis, but it should be kept in mind that a large proportion, between 12 and 22%, is in the form of lipids, in which the carbon is in a less highly oxidized state than it is in the carbohydrates, and hence the amount of O2 produced is actually higher than the quantity estimated by Equation 1. Thus, ratios of DEVIATIONS FROM REDFIELD STOICHIOMETRY 153

O2 to C, N, and P must be higher. Despite this limitation, Equation 1 has been used quite successfully and is still employed by many researchers today. The elemental composition of the phytoplankton is relatively uniform as long as the sea water contains sufficient amounts of the nutrient salts NO3–, HPO4 2–, and H4SiO4. However, when one or more nutrients are depleted, the phytoplankton may exhibit abnormal behaviour in respect of nutrient usage, and indeed the species ordinarily present may even be replaced by other species that are better able to obtain the nutrients needed for growth (Margalef, 1978), and the conditions for the Redfield ratio are no longer fulfilled, with the resulting impact on the stoichiometry of nutrients and oxygen. These anomalies not only allow us to determine what has taken place but also make it possible to quantify all the deviations. The anomalies most commonly encountered in the photic layer include excess carbohydrate synthesis, a generalized phenomenon among populations that have been aged by nutrient deficiency (Williams, 1995), sometimes giving rise to quite striking situations of gelatinous polysaccharide formation (Vollenweider et al., 1995). On other occasions the anomalies lead to blooms of dinoflagellates or organisms like the photosynthetic ciliate Mesodinium, able to carry out vertical migrations into the photic zone, where they synthesize carbohydrates, and then down to the subphotic zone at dusk, where they take in nutrients and synthesize proteins and nucleic acids from the carbohydrates before returning back to the photic zone (Cullen, 1985; Cullen et al., 1985; Fraga et al., 1992, 1999). Certain large diatoms employ a similar strategy to obtain NO3–, employing a pattern of passive vertical migration as a result of density variations caused by accumulation of carbohydrates (Moore and Villareal, 1996; Richardson et al., 1996; Villareal et al., 1996; Richardson et al., 1998; Villareal et al., 1999). Silicate impoverishment also produces anomalies. While variations in Si(OH)4 do not in themselves affect the –∆O2:∆C ratio, diatoms accumulate lipids as a result of silicate depletion (Taguchi et al., 1987), thus altering the stoichiometry of photosynthesis. When it is nitrogen, not phosphorus, in the nutrient supply that is depleted, cyanobacteria that are able to use dissolved N2 gas in the sea water as a nitrogen source enjoy an advantage. Since they are using an unoxidized form of nitrogen, oxygen production is lower. 154 F. FRAGA

Coccolithophores are another group of organisms that can grow in nutrient-poor environments and can cause profound alterations in the stoichiometry of carbon through coccolith, or calcite plate, formation (Paasche, 1998). Other CaCO3-fixing organisms have a similar effect.

AVERAGE PHYTOPLANKTON COMPOSITION The composition of the plankton can be extremely variable, depending on the species present locally and on prevailing environmental conditions. These differences are the result of variable proportions among proteins, nucleic acids, carbohydrates, and lipids. Still, each of these groups has a quite constant elemental composition, i.e., a sample may contain a high or a low amount of protein, but the elemental composition of that protein will remain practically invariable. Table 2, taken from Fraga and Pérez (1990), gives the composition of each of these groups. This Table shows that the largest difference in the ratio of oxygen to carbon is between the carbohydrates and the lipids, and hence the relative proportions of these two groups of biomolecules are of most importance in calculating the oxygen content in the elemental composition of the phytoplankton. The initial atomic C:N:P ratio and the carbohydrate:lipid ratio, QCL, expressed as number of carbon atoms, can be used as a basis for a system of relations for calculating the average phytoplankton composition, based on chemical formulas 2, 3, 4 and 7 in Table 2. TABLE 1. – List of commonly used abbreviations Ap AT C-Cbh C-Red CO2° CT NO3° QCL RC RCS RN RN/RC RP ZC ZD “XO” “XO”D ∆”XO”

= Potential alkalinity (see Eq. 10) = Total alkalinity = Carbohydrates, expressed as moles of carbon = Organic carbon produced according to Redfield stoichiometry (Eq. 2) = Total preformed inorganic carbon = Total dissolved inorganic carbon (DIC) = Preformed nitrate (see Eq. 5) = Carbohydrate:lipid ratio, expressed as atoms of carbon = -∆O2:∆C, in moles = RC for reserves: Carbohydrates, RCS = 1; lipids, RCS = 1.36 = -∆O2:∆N, in moles = C:N, in moles = -∆O2:∆P, in moles = Compensation depth at which carbohydrate synthesis is equal to carbohydrate usage = Depth at which biological activity no longer results in perturbation of Redfield stoichiometry = Any tracer from Table 4 = Value of “XO” at ZD = “XO” - “XO”D

TABLE 2. – Mean proximate composition for each group of biomolecules making up the marine phytoplankton and the respective RC, RN, and RP values, expressing moles of O2 consumed for complete oxidation of the C, N, or P atoms respectively. Mean atomic formula1 Carbohydrates2 Lipids3 Phosphorus compounds4 Proteins5 Chlorophylls6 Proteins + Chlorophylls7 Proteins + Chlorophylls + Phosphorus compounds8

C17 H28 O14 C53 H89 O6 C45 H76 O31 N12 P5 C138 H217 O45 N39 S C46 H52 O5 N4 Mg C147 H227 O46 N40 S Mg 0.16 C177 H277 O66 N48 P3 S Mg 0.16

RC 1.00 1.36 1.55 1.59 1.35 1.58 1.57

RN

RP

5.81 5.64 15.50 5.80 5.80

13.95

92.86

(1) The atomic formulas shown do not correspond to any chemical molecule but are instead the mean ratio of atoms for all compounds in each group of biomolecules (2) Comprising 83% hexoses, 12% pentoses, and 5% deoxyhexoses, in moles (3) Excluding phospholipids, which have been included in (4) (4) All phosphorus compounds, including both organic and inorganic compounds in the proportion given by Miyata and Hattori (1986) (5) Including tryptophan and 5.72% amidic -N (6) Total chlorophylls with 56% chlorophyll a (7) Proteins include chlorophylls in a ratio of chlorophyll a: protein nitrogen of 1.7 expressed as g Chl a: at N-Prt (8) (Proteins + chlorophylls) + phosphorus compounds in the proportion needed for an atomic N:P ratio of 16:1

A C:N:P ratio = 106:16:1 and a QCL ratio = 0.79 yields a rounded elemental composition of C106 H171 O42 N16 P S0.3 Mg 0.05. This composition works out to a protein composition (including chlorophylls) of 47.4 %, a phosphorus compound composition of 12.0 %, a carbohydrate composition of 23.4 %, and a lipid composition of 17.2 % in weight, and, disregarding S and Mg, the overall equation for photosynthesis can be expressed as: 106 HCO3– + 16 NO3– + HPO42– + 94 H2O → → C106 H171 O42 N16 P + 149 O2 + 124 OH– (2) When the interest of a reaction lies in its stoichiometry, rather than its kinetics, and there are various ions in equilibrium, as in the case of the carbon dioxide or phosphate system, it is best to use the principal ion. For that reason, instead of fitting Equation 2 to CO2, it is fit to the HCO3– ion, and hence the OH– ion provides an approximate idea of changes in the pH during photosynthesis. Using the O2 produced in Equation 2 yields a somewhat better Redfield ratio, namely, -O2:C:N:P = 149:106:16:1. Calculating the ratio of each element to O2 separately is a very useful variation on this general relation and takes the form: RC = –∆O2:∆C, R N = –∆O2:∆N and RP = –∆O2:∆P (3) Based on Equation 2, the coefficient values are: RC = 1.41, RN = 9.3 , and RP = 149. This value of RC is consistent with the value published by Laws (1991), and the expression given above is practically identical to that given by Anderson (1995). The numeric values for the Redfield ratio are

rather controversial (Sambroto et al., 1993) and will continue to be so, and for that reason we always use the symbols RC, RN, and RP instead of their numeric values in the expressions to model anomalies in the Redfield stoichiometry. This means complicating the equations somewhat, but it allows each researcher to use the C:N:P and QCL ratio values he or she deems most appropriate. With these ratios, the equation can be used to calculate the values of RC, RN, and RP in a simple, direct manner (Fraga et al., 1998): RC = (RCH +(RCL–RCH):(1+QCL))·(1 – (C:N)PCP / (C:N))+ (4) + RN(PCP) / (C:N) where RCH and RCL are the RC values for carbohydrates and lipids, respectively; RN(PCP) and (C:N)PCP are the values of RN and C:N for the overall protein + chlorophylls + phosphorus compounds overall. Taking these values from Table 2 gives: RC = (1.00 + 0.36 / (1+QCL))·(1 – 3.69 / (C:N)) + 5.81 / (C:N) The other values are: RN = RC·C:N and RP = RC·C:P. The value of RC in Equation 4 depends on the C:N and QCL ratios and is not dependent on the N:P ratio because, as shown in Table 2, the values of RC and RN for the protein +chlorophyll together and the phosphorus compounds are practically the same.

BROECKER’S TRACERS The preformed nutrient concept originated by Redfield et al. (1963) can be used to detect and quantitatively assess anomalies occurring in phytoDEVIATIONS FROM REDFIELD STOICHIOMETRY 155

plankton photosynthesis in respect of general Equation 2: NO3º = (O2 – O2 sat)/RN + NO3–

(5)

where NO3º is the performed NO3– and O2sat is saturated O2 at the winter formation temperature for the body of water in question; and the same follows for the other nutrients. Use of preformed nutrients is helpful in waters deeper than 200 m, where temperature can be viewed as a conservative property; but the preformed nutrient value is not conservative in the surface layer, where temperature varies as a result of the interchange of heat with the atmosphere. The preceding drawback can be overcome using Broecker’s tracers (Broecker, 1974): –

=

“NO” = O2 + RN·NO3 ; “PO” = O2 + RP·PO4 ; “CO” = O2 + RC·CO2

sis using the dissolved N2 in the water, according to the equation 106 HCO3– + 8 N2 + HPO42– + 86 H2O→ →[C106 H171 O42 N16 P] + 129 O2 + 108 OH– (8) Of the chemical Equations given above (Eqs. 2, 6a, 6b, 7 and 8), only Equation 2 satisfies the Redfield ratio. The others do not satisfy the ratio, and hence the values for Broecker’s tracers “NO”, “PO”, and “CO” in these Equations are not constant. To be able to quantify all the above reactions, new tracers that remain constant are needed for use as reference values. Extension of the tracers One tracer that does fulfil all the preceding equations (Eqs. 2, 6a, 6b, 7 and 8) could be: “XO” = O2 + c CO2 + n NO3 + p PO4 + a Ap

which are characteristic for every body of water and are independent of photosynthetic activity as long as the Redfield stoichiometry holds. Broecker’s tracers vary according to the interchange of O2 with the atmosphere, but, as discussed later, this is not a shortcoming and can even be used to calculate the interchange itself. Synthesis when the Redfield stoichiometry does not hold In the absence of nutrients, only carbohydrate synthesis, HCO3 + H2O → [CH2O] + RCS O2 + OH –

–

(6b)

(7)

If nitrates have been depleted but phosphates are still available, cyanobacteria can still carry on biosynthe156 F. FRAGA

–∆O2 = c ∆CO2 + n ∆NO3 + p ∆PO4 + a ∆Ap where Ap is potential alkalinity, being the sum of total alkalinity (AT) plus NO3–. Ap is not dependent on photosynthetic activity (Robertson et al., 1994), and use of that value instead of AT results in simpler tracers. In surface waters with potentially large quantities of ammonium and nitrite the Equation for potential alkalinity needs to be expanded to: (10)

(6a)

where RCS = 1.36, is possible. Therefore, both Equations 6a and 6b can be considered equivalent if the appropriate value of RCS is used in each case (Ríos et al., 1998). Another important anomaly results from coccolithophore blooms, in which calcite is formed according to the equation HCO3– + Ca2+ + OH– → CaCO3 + H2O

and it therefore follows that

Ap = AT + NO3– –NH4+ + 0.5 NO2–

where RCS = 1, or lipid synthesis, approximately HCO3– + H2O → [CH2O 0.27] + RCS O2 + OH–

(9)

For more details about the equation of Ap, see Annex I. On the basis of the equalities (3) in Equation 2, the amount of CO2 consumed to form 1 mole of O2 is 1/RC; for NO3 the value is 1/RN and for PO4 the value is 1/RP. There is no variation in potential alkalinity. A similar reasoning applies to Equations 6-8. In Equation 8, 5/4 of the nitrogen used has to be subtracted from the O2 according to: 2 N2 + 5 O2 + 2 H2O → 4 HNO3 Table 3 presents this system of Equations in matrix form. The coefficient values for the different tracers in Equation 9 are obtained by taking the values of elements from one or more columns and from

TABLE 3. – Matrix of equations from those listed in the body of the text for calculating the coefficient values in Equation 9. Equation

∆CO2

∆NO3

∆PO4

∆AP

(2) Redfield (6) Carbohydrates. Lipids (7) CaCO3 (8) N2 fixation

1/RC 1/RCS 1 1/RC

1/RN 0 0 0

1/RP 0 0 1/RP

0 0 2 0

–∆O2 c n p a

×

A

1 1 0 1–5/(4 RN)

=

B

C

–1

B=A C RCS = 1 for carbohydrates; RCS = 1.36 for lipids; RC = 1.41; RN = 9.3; RP =149. TABLE 4. – Principal tracers used in calculating anomalies in Redfield stoichiometry (letters appearing in quotation marks {“”} in the tracer nomenclature are the symbols for each of the chemical elements intervening in the calculation) “NO” = O2 + RN·NO3 “PO” = O2 + RP·PO4 “CO” = O2 + RC·CO2 “CAO” = O2 + RC(CO2 – 0.5·AP) “NCO” = O2 + RCS·CO2 + (1 – RCS/RC)RN·NO3 “NPO” = O2 + NO3·5/4 + (1 – 5/(4·RN))RP·PO4 “NCAO” = O2 + RCS(CO2 – 0.5·AP) + (1 – RCS/RC)RN·NO3 “NPCO” = O2 + RCS·CO2 + NO3·5/4 + (1 – RCS/RC – 5/(4·RN))RP·PO4 “NPCAO” = O2 + RCS(CO2 – 0.5·AP) + NO3·5/4 + (1 – RCS/RC – 5/(4·RN))RP·PO4 where O2 and NO3 are the corrected values according to the following equations: O2 = O2 obs – 0.5 NO2– – 2 NH4+ NO3 = NO3– + NO2– + NH4+ AP = AT + NO3– – NH4+ + 0.5 NO2– AT = Total alkalinity. AP = Potential alkalinity

the same number of rows in the matrix. Row 1 is always taken so that all the tracers are in accordance with the Redfield ratio. The different matrix combinations yield a total of 15 tracer values. The tracer most useful in quantifying the most commonly occurring anomalies in the Redfield stoichiometry are summarized in Table 4. Table 5 lists the conditions in which each of the tracer values is unchanged, marked by a black rectangle. Additionally, all the tracers exhibiting the same anomaly per mole of CT used have been indexed using the same letter; differences in those anomalies will thus cancel out in the calculations. For those tracers that contain N but not P, the term RN·NO3 can be changed to RP·PO4 without any change in their properties. As has already been mentioned, the principal anomalies are: a) accumulation or use of carbohydrates or lipids; b) precipitation of CaCO3; and c) fixing of N2. All these anomalies can be quantified by combining the tracer satisfying the condition with another tracer that satisfies only the Redfield ratio. These tracer pairs could be “NCO” and “NO”, “CAO” and “CO”, and “NPO” and “PO”. The most

TABLE 5. – Variations in the tracers for the different reactions; ❚ indicates reactions in which the tracer remains constant; identical letters indicate reactions in which tracers vary in the same amount ∆O2

∆CO2

Cbh

N2

CaCO3

Red.

d d d d d d d d d

❚ ❚ e e f ❚ f f f

g g -h -h ❚ h ❚ ❚ ❚

i -j -j k k ❚ k ❚ ❚

❚ ❚ -l ❚ -m ❚ ❚ -m ❚

❚ ❚ ❚ ❚ ❚ ❚ ❚ ❚ ❚

“NO” “PO” “CO” “CAO” “NCO” “NPO” “NCAO” “NPCO” “NPCAO” ∆O2 and ∆CO2: Cbh: N2: CaCO3: Red:

Interchange with the atmosphere Synthesis or use of carbohydrates or lipids Cyanophycean N2 fixation Coccolithophores or precipitation and dissolution of CaCO3 Biomass synthesis or mineralization according to Redfield stoichiometry

complex case that can occur is a mix of different phytoplanktonic populations giving rise to all three anomalies a, b, and c simultaneously. For this case the tracer “NPCAO” satisfies all three anomalies, whereas the tracers “NPO”, “NPCO”, and “NCAO” each fail to satisfy one, namely, a, b, or c, respectively. Using each of those tracers separately in conjunction with “NPCAO” enables each of the anomalies to be quantified individually within the system as a whole. Thus, all the tracers that contain C are affected by the interchange of CO2 with the atmosphere. Nevertheless, in most cases the interchange can be disregarded, because there is a tendency towards compensation. Solar radiation in the surface layer gives rise to photosynthesis, leading to a CO2 deficit while at the same time raising the water temperature, thereby blocking inputs of CO2 from the atmosphere. The decrease in CO2 pressure (pCO2) of 10 µmoles/kg of organic carbon brought about by photosynthesis is offset by a temperature increase of 1.3ºC. In coccolithophore populations calcite plate formation also reduces the decrease in pCO2 brought DEVIATIONS FROM REDFIELD STOICHIOMETRY 157

about by photosynthesis. For a calcification ratio of 1, the decrease in pressure is only 32% of the level that would attain without precipitation of CaCO3, and a temperature increase of only 0.54ºC per 10 µmoles/kg of organic carbon synthesized suffices to offset any change in pCO2. Furthermore, the slow rate of CO2 interchange means that over an interval of days, values can be considered constant.

∆"CO" ∆"NCO"

_

PHYTOPLANKTON STRATEGIES INVOLVING SYNTHESIS THAT DOES NOT SATISFY THE REDFIELD RATIO This category includes groups of phytoplankton that employ different strategies to obtain one or more nutrients that have been depleted in the photic layer to enable continued growth. This category also includes diatoms, which give rise to alterations in the Redfield ratio when nutrients are depleted in the photic zone, even though they do not have a strategy for continued growth. End of a diatom bloom In the presence of sufficient nutrients and light, diatoms divide exponentially, consuming nutrients until they have been depleted, thereby limiting maximum biomass production. Nutrient-poor conditions prevent diatoms from dividing further, but their photosynthesizing apparatus continues to produce even more carbohydrates than they are able to store, and the excess is released into the environment in soluble form (Goldman et al., 1992). Finally, the population dissipates as a result of sedimentation and predation. Therefore, at the biomass peak during the bloom, photosynthesis no longer follows Equation 2 but instead follows Equation 6a, thereby deviating from the Redfield ratio. The value of “NO” increases, because of O2 production that is not offset by NO3 consumption; and the value of “CO” decreases, because O2 production is only 1 mole per mole of CO2 consumed instead of 1.41 moles, while the value of “NCO” remains unchanged (Table 5). The anomalies in these tracers are graphically represented in Figure 1, where Z1 is the depth of the nutrient-depleted zone and ZD is the depth at which there are no longer any anomalies due to biological activity. “NCO” is a conservative tracer, while “NO” ceases to be conservative and increases with carbohydrate synthesis, hence the amount synthesized in the photic zone can be calculated quantitatively 158 F. FRAGA

Depth

_

∆"NO"

Z1 ZD

-50

0

50

100

150

FIG. 1. – Theoretical plot of anomalies in “NO” and “CO” produced by excess carbohydrate synthesis, also plotting the conservative tracer “NCO”. Z1 is the depth of the region of nutrient depletion; ZD is the depth at which there are no more anomalies.

using the equation: C-Cbh = ∆”NO” – ∆”NCO”

(11)

Broecker’s tracers are all in units of O2, but bearing in mind Equation 6a, one mole of carbohydrate carbon is produced for every mole of O2. Accordingly, the result can be expressed either as moles of O2 or moles of C-Cbh. Because anomalies in “NO” are opposed to anomalies in “CO”, the following Equation can also be used: C-Cbh = (∆”NO” – ∆”CO”)/RC

(12)

in which division by RC is performed to convert from moles of O2 to moles of carbon. In both Equations 11 and 12 ∆”NO” = “NO” – ”NO”D and ∆”NCO” = “NCO” – “NCO”D, where “NO”D and “NCO”D are “NO” and “NCO”, respectively, at the reference depth ZD (Fig. 1). The preceding equations are used to calculate the total carbohydrate value, which includes the carbohydrates stored within each cell plus those released into the environment as exudate.

∆"CO"

Maximum biomass, expressed as carbon, which may be carbon synthesized in keeping with the Redfield ratio, is a function of the available nitrogen in the photic zone. Assuming that to be the same as the amount present in the water at depth ZD taken as the reference value (NO3D), it then follows that:

∆"NO"

ZC

(13)

where C-Red is moles of carbon and NO3 is unconsumed nitrate, in this case zero. This makes it possible to calculate the relative importance of carbohydrate synthesis vs. biomass production consistent with the Redfield ratio. The value of C-Cbh/(C-Cbh + C-Red) can reach 28%.

Depth

C-Red = (NO3 D–NO3) · RN/RC

_

∆"NCO"

_

ZD

Vertically migrating dinoflagellates As mentioned above in the Introduction, certain dinoflagellates that are able to carry out vertical migrations may synthesize carbohydrates in the nutrient-poor photic zone during the daytime. These carbohydrates are then stored within the cell. At dusk the dinoflagellates then descend to the subphotic zone, which is rich in nutrients, where they synthesize proteins and nucleic acids using the stored carbohydrate reserves. At daybreak the dinoflagellates return to the photic zone to begin a fresh cycle (Cullen, 1985; Cullen et al., 1985). This is represented by the following Equations (Fraga et al., 1992, 1999):

-100

0

50

100

0 10

Photic zone:

149 HCO3– + 149 H2O → → 149 [CH2O] + 149 O2 + 149 OH–

-50

FIG. 2. – Theoretical plot of “NO” and “CO” anomalies according to equations (14) and (15) produced by migratory dinoflagellates, also plotting the effect of losses of O2 to the atmosphere.

20 (14)

Figure 2 graphically represents the theoretical variations in the tracers “NO”, “CO”, and “NCO” calculated using Equations 14 and 15. ZC is the depth at which carbohydrate synthesis is in equilibrium with carbohydrate use, and ZD is the depth at which phytoplankton activity no longer produces anomalies in the tracer values. The term photic zone as used here is the water layer from 0 m to ZC, and the subphotic zone is the layer from ZC to ZD. Figure 2 also shows the effect of losses of O2 to the atmosphere, shifting all the tracer values towards lower levels; that effect tapers off with depth.

Zm

30 Subphotic zone: 149 [CH2O] + 16 NO3– + HPO42– + 25 OH– → → [C106 H171 O42 N16 P] + 43 HCO3– + 55 H2O (15)

40 50 "NO" "CO" - 2917 "NCO" - 2075

60 150

200

250

17 Jul.

300

350

400

"NO" FIG. 3. – Distribution of “NO”, “CO”, and “NCO” during a period of upwelling (17 July). An amount of 2917 (= RC·CO2°-RN·NO3°) has been subtracted from “CO” and 2917/RC has been subtracted from “NCO” so that the scales for those tracers will coincide with that for “NO”. DEVIATIONS FROM REDFIELD STOICHIOMETRY 159

0 10 _ Z C

20

Zm

30 40 _

ZD

50 "NO" "CO" - 2917 "NCO" - 2075

60 150

200

250 300 "NO"

25 Jul.

350

400

FIG. 4. – The same plot as in Figure 2 eight days later after a relaxation of upwelling (25 July) and occurrence of a red tide bloom.

Upwelling regions with variable upwelling activity are the best zones for observing the anomalies produced by this strategy on the part of migratory dinoflagellates. In conditions of active upwelling, nutrients are carried to the surface, and photosynthesis follows the Redfield ratio. Consequently, the vertical profiles for the three tracers take the form of straight lines, which may overlap. When upwelling intensity has abated and the nutrients in the photic zone have become depleted, migratory dinoflagellates gain the advantage, and the anomalies shown in the diagram in Figure 2 occur. The area off the northwestern Iberian Peninsula is one such zone, where intense upwelling interspersed with relaxation periods takes place in spring-summer (Álvarez-Salgado et al., 1993). Figure 3 depicts the vertical profiles for the tracers “NO”, “CO”, and “NCO” during an episode of upwelling that carried nitrates up to the surface (17 July), and Figure 4 presents those same profiles at the same geographic location after a week of lower upwelling activity (25 July), with depletion of nutrients down to 20 m. Figure 5 plots the NO3, CO2, and O2 distributions, clearly showing the vertical decoupling between NO3 and 160 F. FRAGA

FIG. 5. – Vertical distribution of O2, CO2, and NO3 at the station in Figure 4 on 25 July. The relative magnitude of each of the units is proportional to inverse Redfield stoichiometry. The preformed CO2° and NO3° values and O2 saturation at ZD have been adjusted to the vertical line in the centre of the Figure. Solid data points are real O2 values; solid line represents the values adjusted for losses of O2 to the atmosphere.

CO2 giving rise to the anomalies in “NO” and “CO” in Figure 4. The dominant species was the ciliate Mesodinium rubrum, whose behavioural pattern is identical to that of migratory dinoflagellates. Equations 11 and 12 described above are applicable both to carbohydrate synthesis and usage. These equations give total values, calculated on a cumulative basis for all days elapsed since the start of nutrient depletion (in this case, six days), independently of whether the carbohydrates are used in the subphotic layer daily, and they are not dependent on losses of O2 to the atmosphere, because such losses affect all three tracers equally. The relative importance of this biomass synthesis strategy compared to the usual pathway (Eq. 2) can be calculated as already described above. Accordingly, at the same station referred to above on 25 July (Fig. 4), integration from 0 m to ZC yields a synthesis value of 987 mmoles of carbohydrate carbon/m2. Since nitrate at depth ZD was 8 µmoles/kg,

the biomass synthesized according to the Redfield ratio, also integrated from 0 m to ZC (15 m), was 817 mmoles/m2, for a total of 1 804 mmoles/m2; that is, 55 % of the carbon was fixed by the carbohydrate pathway and 45% by the normal pathway of Equation 2. The example considered is for peak production by M. rubrum, but even so, the mean value was around 35 % at the locality in question during the period of upwelling relaxation that followed, and hence it is an important pathway for biomass synthesis. Unlike the final stage of a diatom bloom, in which an amount of soluble carbohydrate remained, the final product here is biomass in accordance with Redfield’s C:N ratio. Adding Equation 14 to Equation 15 yields Equation 2, which satisfies the Redfield ratio; thus, even though the ratio is not satisfied in either the photic zone or the subphotic zone, the total of the two zones combined does satisfy the ratio. This is because the carbohydrates synthesized in the photic zone are not a final product but rather a raw material input for the biosynthesis of proteins and nucleic acids in the subphotic zone. Losses of O2 to the atmosphere This section has been included because it is closely related to excess carbohydrate synthesis. NO3º·RN is the maximum quantity of O2 that can be produced beyond the saturation point, provided that the Redfield ratio is satisfied, and even taking into account the rise in surface temperature, it is likely that O2 supersaturation is not much greater than 120%. As already mentioned, even after depletion of nutrients at the surface, certain dinoflagellates are able to continue to carry out photosynthesis and to produce O2, the only constraint being their ability to perform vertical migrations. O2 saturation levels of up to 158% have been measured in these zones. As a consequence, the zones where the greatest losses of O2 occur are those in which the Redfield ratio is not satisfied. The tracer “NO”, sometimes used for this purpose, is only conservative if the Redfield ratio is satisfied, and therefore it should not be used to calculate losses of O2, particularly when nitrate levels in the surface waters are less than 0.5 µmoles/kg. Figure 4 clearly shows that the higher the level of carbohydrate synthesis, and hence O2 production, the higher the value of “NO”. Paradoxically, at high losses of O2, the value calculated using “NO” yields inputs from, rather than losses to, the atmosphere.

When dinoflagellates are present, the “NCO” tracer has to be used. Oxygen losses, O2L, are: O2 L = ∆”NCO” where ∆”NCO” = “NCO” – “NCO”D A negative O2L value reflects losses of O2 to the atmosphere. When coccolithophores or cyanobacteria are present, the corresponding conservative tracer for the species group present should be used instead of “NCO” (Table 5). Strategy of Rhizosolenia The strategy employed by Rhizosolenia and other large diatoms is very similar to that of dinoflagellates, except that proteins and nucleic acids are not synthesized from carbohydrates in the subphotic layer. According to Villareal et al. (1993), Rhizosolenia takes up nitrates (and presumably phosphate as well) in the subphotic zone and transports them to the photic zone, where biomass is photosynthesized. Although there are insufficient data to enable preparation of a definitive flow diagram for the stoichiometric processes, certain possibilities can nonetheless be put forward. To that end, live cell biomass has been designated B, with a mean composition of B = [C106 H171 O42 N16 P]. For ease of comprehension, substances accumulated inside the cell and transported vertically from one zone to the other have been placed in brackets [ ], with an arrow to the right of the brackets indicating the direction of vertical migration of the cells. Photic zone Initially there is excess carbohydrate synthesis, which provides cells with energy reserves and is also conducive to sinking of cells (Richard and Cullen 1995): [B] + a HCO3– + a H2O → [B, aCH2O]↓ + a O2 + a OH– (16) The amount of carbohydrates synthesized has been designated “a”, because there is no theoretical relationship with the nutrients used. Subphotic zone Nutrients in this layer are taken up into the interior of the cells, resulting in carbohydrate oxidation by respiration, which in turn could supply the enerDEVIATIONS FROM REDFIELD STOICHIOMETRY 161

gy needed to drive concentration of the nutrients present in the water at the µmole/l level, from where they are taken up into the cell plasma attaining a concentration on the order of mmoles/l, that is, some thousand times greater. The Equation for this is:

In both cases, i.e. Equations 17a and 17b, cells with their stores of nitrates (Villareal et al., 1996) and phosphates float back to the photic zone.

[B, aCH2O] + 16 NO3– + HPO42– + a O2 + a OH– → → [B, 16NO3–, HPO42–] ↑ + a HCO3– + a H2O (17a)

In the photic zone the cells containing the transported nutrients photosynthesize biomass according to the Equation:

Photic zone

On the other hand, release of soluble carbohydrates into the sea to allow the cells to rise to the surface is also a possibility, according to the equation:

106 HCO3– + [B, 16NO3–, HPO42–] + 94 H2O → (18) → 2 [B] + 149 O2 + 124 OH–

[B, aCH2O] + 16 NO3– + HPO42– → → [B, 16NO3–, HPO42–] ↑ + a CH2O (17b)

Therefore, two stages of the process, namely, those represented by Equations 16 and 18, take place in the photic zone. Taken together, this gives:

This latter possibility would seem to be unlikely, because living organisms tend to optimize utilization of their energy reserves. ∆"CO" ∆"NCO" ∆"NO"

(a+106) HCO3– + [B, 16NO3–, HPO4=] + (a+94) H2O → → [B] + [B, aCH2O]↓+ (a+149) O2 + (a+124) OH– (19)

∆"CO" ∆"NCO" ∆"NO"

0

_ Z C

150 200

ZD

b

a

c 250

250 ∆"CO" ∆"NCO" ∆"NO"

0

∆"CO" ∆"NCO"

∆"NO"

50 100

200

_Z C

100

∆"CO" ∆"NCO"

∆"NO"

100 150 200

ZD

d 0

0 50

150

-200 -100

∆"NO"

100

150 200

∆"CO" ∆"NCO"

50

50 100

0

e 250 200 -200 -100

f 250

0

100

200

-200 -100

0

100

200

FIG. 6. – Changes in the tracers “NO”, “CO”, and “NCO” caused by different processes: a) losses of O2 to the atmosphere; b) transport of NO3- from the subphotic zone to the photic zone; c) carbohydrate synthesis in the photic zone for conversion in the subphotic zone; d) as in c) but carbohydrates are lost as exudate in the subphotic zone; e) sum of processes a+b+c; f) sum of processes a+b+d.

162 F. FRAGA

The anomalies in the tracers “NO”, “CO”, and “NCO” occurring in these two processes, namely, carbohydrate synthesis and transport of NO3– ions, have been graphically represented separately (Fig. 6), and additionally another anomaly has been shown, namely, the anomaly resulting from losses of O2 to the atmosphere (Fig. 6a). The decrease in the values of these tracers brought about by the loss of O2 is the same for all the tracers, hence the differences between the tracers are independent of losses of O2. During transport of the NO3– ions from the subphotic zone to the photic zone (Figure 6b), the tracer “NCO” ceases to be conservative, and the anomaly in this tracer is proportional to the transport of NO3– and is independent of carbohydrate synthesis (Figs. 6c, 6d). Figures 6c and 6d depict the anomalies brought about by carbohydrate synthesis in the photic zone (Eq. 16). In the subphotic zone (Fig. 6c) anomalies occur as a result of the use of carbohydrates in respiration (Eq. 17a), while Figure 6d depicts the case in which carbohydrates are released by the cells to the exterior in soluble form (Eq. 17b). The final outcome is the total of all the anomalies brought about by all three processes, as shown in Figures 6a + 6b + 6c and summarized in Figure 6e, or as shown in Figures 6a + 6b + 6d and summarized in Figure 6f. The presence of an “NO” minimum in the subphotic zone in Figures 6e and 6f agrees with the data published by Emerson and Hayward (1995), who found that when the nutricline in a subtropical region in the North Pacific was below the 1% light level, preformed nitrate (NO3º) was negative, with a minimum at around 140 m. The presence of an “NO” minimum can also be inferred from the relation “NO” = O2sat + RN·NO3º. As already mentioned above, the tracer “NCO” is not conservative when NO3– transport occurs, but there are two levels, ZC and ZD, where it does not undergo any alteration. Interpolation of the “NCO” values between ZC and ZD yields a series of undisturbed values that can be taken as benchmarks for calculating the anomalies. Designating this series of reference values “NCO”r, the quantity of NO3– transported from each level of the subphotic zone to the photic zone is:

C-Cbh = (∆”CO” – ∆”NCO”r) / (RC – 1) expressed as carbon (moles/kg). In the photic zone the sum of synthesized carbohydrates plus organic carbon synthesized from the imported nitrate is given by the relation: C-Cbh + T(NO3–) · RN/RC = (∆”NO” – ∆”CO”) / RC where T(NO3–), expressed as moles/kg of nitrogen (Eq. 20), is converted to carbon by multiplying it by the factor RN/RC. While this is true for each layer separately, the values of C-Cbh and T(NO3–) cannot be calculated independently of each other, because biomass synthesis and carbohydrate synthesis may be vertically decoupled in the photic zone, for which there are no benchmark “NCO”r reference values. Carbohydrate synthesis can be calculated globally for the entire photic zone as a whole by integrating from 0 m to ZC. C-Cbh = (∆”NO” – ∆”CO” – T(NO3–) · RN) / RC T(NO3–) here being the total nitrate imported from the subphotic zone, all values being expressed as moles/m2. The previous schemes did not take into account the input of CO2 from the atmosphere to compensate consumption during photosynthesis. Rhizosolenia occurs during periods of prolonged stability; under these conditions, the exchange of gases can be large, not only by O2 losses, but also due to CO2 inputs; therefore, the signature produced by carbohydrate synthesis in the upper water layers may be fairly weak. Despite these limitations, anomalies in the tracers “NCO”, “NO”, and “CO” can still provide very clear quantitative information as to what has been happening from the surface down to the level below the nutricline. Coccolithophores

T(NO3–) = (∆”NCO”r – ∆”NCO”) / (RN·(1–1/RC)) (20)

According to Buitenhuis et al. (1999), coccolithophores can synthesize calcite from the HCO3– ion. This provides a supply of CO2 without their having to expend energy on concentrating the dissolved free CO2, based on the following intracellular reactions:

where T(NO3–) is transported nitrate expressed as NO3– (moles/kg), and the quantity of carbohydrates used at each level of the subphotic zone is:

HCO3– + Ca2+ → CaCO3 + H+ HCO3– + H+ → CO2 + H2O CO2 + H2O → [CH2O] + O2 DEVIATIONS FROM REDFIELD STOICHIOMETRY 163

TABLE 6. – Changes in the concentration of the principal ions in the CO2 system in the formation of 106 µmol/kg of organic carbon during photosynthesis by coccolithophores (calculations have assumed that Ca2+in·CO32-in = Ca2+fin·CO32-fin) Ion

Initial value

CT A Ca2+ H2CO3 HCO3– CO32– CaCO3

2077* 2317* 10300.9* 13.7 1895.4 167.8 0

Final CT in – 106 – CaCO3.fin = Ain+ 106·RC/RN – 2·CaCO3.fin = Ca2+in – CaCO3.fin = CO32–in · Ca2+in / (Ca2+in– CaCO3.fin) = CaCO3.fin =

Final value

∆: Final – Initial

1863.0 2117.2 10193.0 10.7 1682.8 169.6 107.9

-213.9 -199.8 -107.9 -3.0 -212.7 1.8 107.9

Literature values have been marked with an asterisk (*); all other values have been calculated using the CO2 system dissociation constants S = 35; t = 15; CT = total carbon; A = alkalinity; CaCO3 from coccoliths

where the H+ produced during the formation of CaCO3 releases one mole of CO2, which is used to synthesize organic carbon. Thus, the calcification reaction ∆CaCO3/∆Corg is equal to 1. Another approach is to consider maximum energy usage in the framework of the CaCO3 precipitation-dissolution balance when the system is in chemical equilibrium. Table 6 presents the variations in each ion while the ionic product of calcium carbonate is held constant, CO32– × Ca2+ = const. The “initial value” column gives the characteristic values for biologically undisturbed sea water, and the column setting out the “final” values give the final value and variation for each ion during synthesis of 106 µmoles/kg of organic carbon for coccolithophore biomass formation. Column ∆ shows that the variations in the ∆H2CO3 (free CO2 dissolved in the water) and ∆CO32– are small and opposite, and their difference can be included in the value of ∆HCO3–. The resulting values can be used to construct a simplified stoichiometric equation: 214 HCO3– + 108 Ca2+ + 16 NO3– + HPO42– → →[C106 H171 O42 N16 P, 108 CaCO3] +149 O2 + (21) + 16 OH– + 14 H2O The calcification ratio is 1.02, practically the same as the previous value and slightly closer to the value of 1.07 reported by Paasche (1998) for cultures incubated in nutrient-sufficient conditions. However, this Equation is not practical, because the calcification ratio can vary considerably, from 0.2 (Holligan et al., 1993) to 1.4 (Paasche, 1998). The highest calcification ratios have been observed in cultures grown in nutrient-poor conditions. For that reason, calcium carbonate formation (Eq. 7) and synthesis of organic matter have been considered separately in the Equations in Table 3. Thus, the tracer values used are suitable for all calcification ratios and even for variations caused by the dissolu164 F. FRAGA

tion or precipitation of CaCO3 of chemical origin without any involvement by coccolithophores. The preceding Equation can, accordingly, be considered the sum of Equation 2, which satisfies Redfield stoichiometry, and Equation 7 multiplied by 108. Besides CaCO3, coccolithophores also store accumulations of lipids as energy reserves, in addition to the structural lipids present in all phytoplanktonic cells. Based on the biochemical composition of Emiliania huxleyi reported by Fernández et al. (1994), the reserves would appear to comprise 12% carbohydrates and 88% lipids, yielding RCS = 1.3. Therefore, “NCAO” has to be used as the conservative tracer. This tracer is not dependent on CaCO3 formation or lipid accumulation. The tracers “NCO” and “NO”, the former being invariable with excess lipid synthesis and variable with CaCO3 formation and the latter (“NO”) being the converse. This enables the values for CaCO3 and excess lipid formation to be calculated separately. The respective Equations, expressed as number of carbon atoms, are: CaCO3 = (∆“NCAO” – ∆“NCO”)/RCS C-Lipids = (∆“NO” – ∆“NCAO”)/RCS or

(22)

CaCO3 = – ∆Ap/2 C-Lipids = (∆“NO” – ∆“CAO”)/RC

The plot in Figure 7 illustrates the anomalies in the tracers “NO” and “NCO” as well as in the conservative tracer “NCAO”, in which both photosynthesis and coccolithophore plate formation take place in the upper layer of the water column. The plot is only an approximation because the calcification:photosynthesis ratio is variable (Marañón and González, 1997). Accordingly, “NCO” and “NO” are independent, and the anomalies in those tracers need not follow any fixed pattern. If coccoliths drift down into the subphotic zone from the upper levels and dissolve there, the “NCO” value could increase.

∆"NCO"

∆"NCAO" Lip

Depth

CaCO3

∆"NO"

sibility comes from the finding that when nutrients in the photic zone become scarce, coccolithophores store lipids, which can then be used to synthesize proteins in darkness (Fernández et al., 1994). In addition, coccolith formation increases in nutrientpoor conditions (Paasche, 1998), resulting in an increase in density conducive to sinking. The cells may be able to return to the photic zone by releasing their calcite plates. This has not been demonstrated, however; and, indeed, coccolithophore cultures carried out in conditions of low light levels have shown that coccolith formation continues, though at a slower rate (Balch et al., 1996). Correct use of Broecker’s tracers could thus be a good way to elucidate coccolithophore behaviour in the wild. N2 fixing

-200

-100

0

100

FIG. 7. – Theoretical plot of changes in the tracers “NCO” and “NO” during a coccolithophore bloom, assuming both calcite (CaCO3) scale formation and accumulation of lipids in the cells.

Experimental methodology is a question of great significance in the study of coccolithophores, since when they are present modifications are often required, something usually unnecessary on normal oceanographic cruises. When direct measurements of total CO2 and alkalinity are taken in the presence of coccoliths, samples need to be filtered (Robertson et al., 1994), because at pH 5.2-5.5 coccoliths dissolve in fewer than 30 seconds (Balch et al., 1996), thereby producing erroneously high alkalinity and total CO2 readings. The difference in the alkalinity values for a filtered sample and an unfiltered sample will give the amount of CaCO3 present in the samples. Subtracting the value calculated using Equation 22 from that CaCO3 value yields the amount that has sedimented out of the water layer concerned, if the value is positive, or the amount that has entered that layer from higher levels, if the value is negative. The plot in Figure 7 has disregarded possible reactions in the water level below, but in addition to the dissolution of coccoliths already referred to above, coccolithophores might also employ a strategy analogous to that of dinoflagellates that are able to carry out vertical migrations. Support for this pos-

If the values for “NO”, “PO”, and “CO” are known, the nutrient limiting biological production is the one with the lowest value. “CO” is of course always much higher than the other two, because the rate of CO2 usage is 9.6 times higher than NO3 and PO4 (Redfield et al., 1963). The values of “NO” and “PO” are usually the same, because NO3 and PO4 are depleted together. When the nutrients NO3– + NO2– + NH4+ are depleted in the photic zone but PO4 is still available, “NO” < “PO”, and in those conditions cyanobacteria gain the advantage and begin fixing N2 according to Equation 8. ”NPO” can be used as the conservative tracer until the phosphate is depleted. Figure 8 presents a theoretical plot of what takes place during N2 fixation in the surface layer. Water with “NO” 1. Thus, the amount of successful colonization (fhˆ) from occupied patches must be greater than the rate of clearance (m + e). The condition R˜ > 1 determines the possible dynamic landscapes (in terms of e and hˆ) in which a given species is able to persist. When the species does persist, the equilibrium occupancy is given by a modified version of the standard metapopulation equation: R˜ =

The models of the previous section hypothesize a fixed landscape of patches, subject only to extinction and recolonization. Real landscapes, however, are dynamic, and patches themselves come and go. In a recent publication, Keymer et al. (2000) extended the metapopulation model to landscapes where habitat is created and destroyed dynamically. In this section we propose that the problem of community invasibility and resilience described in the preceding section is equivalent (in the mean field) to the problem of metapopulation persistence in dynamic landscapes (sensu Keymer et al., 2000). Therefore invasion success can be determined by representing the community resident community (prior to invasion) as a dynamic landscape of habitable sites (patch dynamics). Invasion will occur only if the invader is able to persist in the dynamic landscape representing the resident community. Metapopulation persistence in dynamic landscapes Although Keymer et al. (2000) start with a fully spatial stochastic process, in the mean-field approximation metapopulation dynamics can be described by an occupancy function that represents the proportion of occupied sites and follows Levins’ (1969) laws of metapopulation dynamics. The population dynamics, however, depend on the patch dynamics – changes in the proportion of habitable ‘patches’ (or sites available for occupancy). Nonhabitable sites are restored at rate λ, while habitable sites are destroyed or degraded at rate e (thus 1/e gives the mean lifespan of a habitable patch). If p is the proportion of sites that are occupied, and h is the proportion that contain suitable habitat, the dynamics are given by:

pˆ = hˆ (1 – 1/R˜ )

(8)

The resident community as a dynamical landscape Consider a hierarchical community of the form described in the section 3 (Eq. 1). From the point of view of an invader species i, we can define every site occupied by better competitors as a destroyed site. Thus, the amount of available habitat (for the invader) is hˆi =1 – σi-1 .

(9)

Since the resident species are at a dynamic equilibrium, available patches are created by clearance of superior competitors (disturbance) and destroyed by colonization of superior competitors. Thus, the destruction rate of habitat patches from the invader’s point of view is ei = φi –1 .

(10)

Hence, the dynamics of the hierarchical community are equivalent to those of a metapopulation under a patch-dynamic regime. The regime of patch dynamics is a property of the resident community (Eqs. 9, 10) and invasibility is a property resulting from the interaction of residents and invader. COMMUNITY ASSEMBLY AND ECOSYSTEM PATTERN 175

Community invasibility as species persistence in dynamic landscapes Equations 9 and 10 allow us to see a hierarchical community (Eq. 1) as a dynamic landscape (Eq. 6) characterized by patch availability and mean lifespan (1/e). In this framework, the community invasibility problem is equivalent to the problem of metapopulation persistence in a dynamic landscape, and the dynamics of invasion is equivalent to metapopulation dynamics (Eqs. 7, 8). Therefore, we know that a resident community will be successfully invaded by species i if and only if fi h˜i >1 mi + ei

R˜ i =

(11)

The two species case Consider the situation of two species sequentially invading a pristine environment. The first invader finds an empty community (ê1, hˆ1) represented by a static landscape (ê = 0) with all sites being habitat patches (hˆ = 1). Therefore, the condition for this founder species to invade is equivalent to the metapopulation persistence in static landscapes f1 > m1.

(12)

The second species does not neccesarily find an “empty community”. If species 2 is a poorer competitor than species 1 then the environment (ê2, hˆ2) is no longer pristine. Species 2 instead encounters a much “destroyed” (sensu Bascompte and Sole, 1998) and “ephemeral” (sensu Keymer et al., 2000) habitat and therefore will invade it only if f2 hˆ2 > m2 + ê2.

(13)

In other words, invasion will occur if the effective colonization rate is greater than the combined rate of clearance due to intrinsic mortality and patch destruction (invasion by superior competitors). Following Kinzig et al. (1999) we can also think about this problem as a species-packing problem in niche space. If we write the fundamental rate of increase ri = fi – mi, we can represent niche separation between the two species (in R space) as the ratio between their reproductive numbers: R2 r >1+ 1 . R1 m2 176 S.A. LEVIN et al.

(14)

Thus, there is a necessary separation between reproductive numbers before an invader can be successful. This is because of the reduction in available habitat, and the losses due to invasion from superior competitors. If we fix the parameters of the resident (R1 and r1), we see that the invader can increase success either by increasing its reproductive number R2, or by decreasing its life span 1/m2. This is because, for fixed R, shorter-lived species will have faster reproduction, and thus be more effective colonizers. Relaxing the hierarchy Although we focus our analysis here on hierarchical competitive structures, more general cases with non-transitive relationships (Buss and Jackson, 1979) can be incorporated into the patch-dynamic framework by representing communities as landscapes with habitat-quality distributions where patches occupied by stronger competitors are represented as poor-quality habitat, and conversely. In this paper we presented the simplest case of landscape dynamics as patch creation and destruction and showed its equivalence with a hierarchically structured community. More general models of competition for space (sensu Durrett and Levin, 1998) can be represented in the mean field as more complicated cases of patch dynamics. A very promising challenge is to extend this formalism to community dynamics and evolution in spatially explicit frameworks, with more general dispersal (Travis and French, 2000) and competition (Adler and Mosquera, 2000) functions. In these scenarios (spatially dependent) patch quality will represent the resident community’s state. It is clear that more theoretical studies on spatially dependent patch dynamics and metapopulation persistence in dynamic landscapes, and on scale invariance and the emergence of ecosystem patterns, is urgently needed for a better understanding of spatially distributed multispecies communities. However, further study of the implications of scale invariance in simple hierarchical models to the emergence of ecosystem patterns is also worthwhile.

FOOD WEBS, TROPHIC CASCADES AND RESOURSE TRANSFORMATION NETWORKS In 1968, Ramón Margalef (p. 81) wrote: “The energy gates at the places where species interact – or where they interact with environment – are the

organs by which selection is achieved and evolution occurs, the rate of evolution depending on the efficiency of the gate”. Margalef taught us to think about evolution within the framework of ecosystem organization, thus we must extend previous models of space utilization (sections 3 and 4) to incorporate assumptions about nutrient (or biomass) pathways (nutrient utilization). In this new scenario, different spatial patterns of nutrient utilization (at the ecosystem level) are seen as the result of diffusive coevolution operating at the level of individual organisms. Although is clear that more realistic models of spatial competition are needed, it is also worthwhile to extend simple spatial models to incorporate nutrient utilization. The role of community structure in shaping ecosystem patterns Patch occupancy is a natural way to build a theoretical bridge linking the landscape and ecosystem criteria (sensu Allen and Hoekstra, 1992). The question of the units of selection and spatial localization of interactions (Durrett and Levin, 1994) would determine critical scales at which patch occupancy would be meaningful for ecosystem function. In this way, we can think of a patch large enough to hold one organism as the locus for biogeochemical transformations. Thus, organisms, their populations and communities (sometimes nested other organisms) play a catalytic role for such transformations. Thus, scale-invariant patterns of spatial occupancy could be translated into spatio-temporal patterns of nutrient distribution – ecosystem pattern. Recent landscape ecology studies such as the spatiotemporal analysis of nitrogen dynamics in forest watersheds (Bartell and Brenkert, 1990) as well as spatiotemporally embedded food webs (Holt, 1996a,b; Polis et al., 1996) point in directions envisioned by Margalef in the late 1960s.

THE DYNAMICS OF ECOSYSTEMS: REDFIELD RATIOS AND NUTRIENT CYCLES The earlier sections of this paper have examined the evolution of populations in relation to one another, and demonstrated that characteristic patterns can arise in the distribution of species. From simplistic assumptions that reflect nothing more than competition for space, and the evolutionary dynamics that this implies, robust patterns can emerge from the

self-organization of ecological communities (Chave et al., 2001). This is only part of the story, however. The dynamics of competition among species, and indeed the dynamics of persistence of individual populations, are mediated by the physical and chemical environment – by the availability of nutrients (and of water in intertidal and terrestrial systems), as well as by factors such as temperature and salinity. In turn, the biotic composition of ecosystems fundamentally affects the ambient physico-chemical context in which populations evolve. Thus, populations together with their physical and chemical environments constitute interconnected feedback systems, namely ecosystems. It does not detract from the notion of the ecosystem to observe that ecosystems are open systems, whose definition hence is subject to a great deal of arbitrariness. Ecosystems are not evolutionary units, selected for their macroscopic features because those features benefit the constituent populations. Rather, what patterns there are must emerge from the self-organization of components whose evolutionary context is far broader than that of a single ecosystem. The statistical mechanics of the assembly of communities must rest heavily on various laws of large numbers, producing pictures that are to large extent insensitive to many of the fine details, providing therefore an environment whose features are sufficiently predictable to facilitate adaptation and survival. Community ecology concerns itself largely with patterns in the distribution of species; ecosystem ecology concerns itself further with the fluxes of materials such as key elements, and with patterns in their distribution. Integrating these two aspects, the biotic and the abiotic, is the essence of understanding ecosystems, and involves the interplay of processes across diverse scales of space, time and organizational complexity. Life depends on a diversity of elements, but carbon (C), nitrogen (N) and phosphorus (P) are at the core, along with the constituents of water itself, hydrogen (H) and oxygen (O). In 1934, the young animal physiologist Albert Redfield observed that C, N and P in marine plankton occurred in remarkably constant proportions, 106:16:1, across a diverse range of environments (Redfield, 1934). He further noted that the N:P ratio was very similar to those found in dissolved inorganic form in seawater, and proposed that the plankton actually control the nitrate:phosphate levels in the ocean through remineralization (Falkowski, 2001). COMMUNITY ASSEMBLY AND ECOSYSTEM PATTERN 177

The situation is not as simple as envisaged by Redfield. Indeed, later work showed that the Redfield ratios are indeed approximately constant across a wide range of environments, and that plankton ratios match ambient levels very closely, despite great variation in the absolute concentrations. Redfield espoused the view that phosphate limits ocean productivity, but modern work (Falkowski, 1997; Karl et al., 1997) argues that nitrogen can be limiting, because nitrogen fixation has high iron demands. The activities of marine plankton surely influence the cycles of C, N and P, but in turn are controlled by the availability of those nutrients and others in the marine environment. Furthermore, although there is a great deal of similarity in the element ratios of plankton, there are differences. That is, different species utilize resources in different ways, a partial answer to the conundrum of how so many species of plankton manage to coexist (Hutchinson, 1961). Thus to understand the constancy of the element ratios, one cannot simply take the viewpoint that the ambient ratios represent what is remineralized from the plankton. The plankton and the water column are involved in an ongoing colloquy in which each is influenced by the other, within a turbulent environment characterized by incomplete mixing, and the infusion of nutrients from exogenous sources. Why then do constant element ratios emerge, given the considerable heterogeneity in environmental conditions, as well as biological diversity? Such questions direct attention to how such ratios can emerge, and be stabilized, in the face of long-term evolutionary change. How too can so much biotic diversity be sustained, given such constancy in key element ratios? The usual focus is on marine systems, but it is also instructive to ask whether such patterns can be seen in freshwater, or in terrestrial systems. For large lakes, one does indeed see similar ratios, but smaller lakes deviate from the canonical values (Downing and McCauley, 1992). Forests present even greater challenges, even in terms of determining what measurements would be comparable. Other factors also complicate analysis. Lars Hedin, Pamela Matson and Peter Vitousek have been comparing the biogeochemistry of Hawaiian forests across a spectrum ranging from very young forests (300 years old) to very old ones (more than 4 million years). They show that these forests in their early stages of development receive much P from weathering, and are primarily nitrogen limited, but as forests age, P becomes progressively the limiting 178 S.A. LEVIN et al.

nutrient (Hedin et al., submitted). Thus external factors play a crucial role, especially for younger forests, in determining N:P ratios. Marine and terrestrial systems differ fundamentally in terms of how closed they are, how well mixed they are, and how mature they are evolutionarily. These factors are interrelated of course; the limited mixing in terrestrial environments, say among the various Hawaiian Islands, permits local exogenous heterogeneity to exert a greater influence. The challenge is to tease apart these influences, and to determine how much of the pattern we see is exogenously driven, and how much is the result of self-organization. Furthermore, how different should the ratios of elements be in a system in its early stages of development from one that has seen millions of years of evolution? To address issues of this sort, one must start from the bottom up, not from the top down. The individual is where the gene meets the environment, and hence the individual is the primary unit of selection. Valid arguments can be made, of course, to treat the gene itself as the unit of selection (Dawkins, 1982); in other cases, such as for the social insects, the operational unit may involve collections of individuals within a species. Tight interspecific linkages, such as in host-parasite systems, can introduce even higher-level considerations; but these are all a far cry from the ecosystem. With few exceptions, tight coevolution among species is hard to find in Nature (Futuyma and Slatkin, 1983), and we must understand what patterns we do detect at the macroscopic level as having emerged from the collective and selfish evolution of its individual species. These emergent patterns still feed back to influence evolution at lower levels, but the coevolutionary influences are what Ehrlich and Raven (1964) termed “diffuse”. Our agenda, then, in future work, will be to extend the approach of the previous sections to examine the evolution of patterns of resource uptake, nitrogen fixation, chelation and other mechanisms for resource use and sequestration, in order to elucidate how patterns of element cycling emerge. As in the previous sections, an adaptive dynamics is needed that addresses the competitive and other interactions among genetically diverse types, sharing a global commons in which each individual’s actions has a perhaps small effect globally, but where the collective actions of many individuals assumes great importance. This is not much different than the problems we face in understanding the threats to human sustainability from the collective actions of billions of individuals, each of whom sees

his or her actions as having minimal environmental impact (Levin, 1999). Thus the relevant models should be individual-based, or at least represent the statistical mechanics of ensembles of such individuals. They should be spatially explicit, because the localization of interactions is an essential and overriding evolutionary truth. And ultimately, from these overly detailed models, it will be essential to derive robust macroscopic features that do not depend upon the intricate details. It is those regularities that impel such investigations, and that must also be the endpoints.

ACKNOWLEDGMENTS We are pleased to acknowledge the support of the National Science Foundation, award DEB-0083566, The David and Lucile Packard Foundation, awards 8910-48190, 7426-2208-1, and the Andrew W. Mellon Foundation. REFERENCES Adler, F.R. and J. Mosquera. – 2000. Is space necessary? Interference competition and limits to biodiversity. Ecology, 81: 3226-3232. Allen, T.F.H. and T.W. Hoekstra. – 1992. Toward a unified ecology. University Press, New York. Armstrong, R.A. and R. McGehee. – 1980. Competitive exclusion. Am. Nat., 115: 151-170. Bartell, S.B. and A.L. Brenkert. – 1990. A spatial-temporal model of nitrogen dynamics in a deciduous forest watershed In: M.G. Turner and R.H. Gardner (eds.), Quantitative methods in landscape ecology, pp. 379-398. Springer-Verlag, New York. Bascompte, J. and R. Sole. – 1998. Models of habitat fragmentation. In: Modeling spatio-temporal dynamics in ecology. SpringerVerlag, Berlin. Bolker, B.M., and S.W. Pacala. – 1999. Spatial moment equations for plant competition: Understanding spatial strategies and the advantages of short dispersal. Am. Nat., 153: 575-602. Buss, L.W. and J.B.C. Jackson. – 1979. Competitive networks: nontransitive competitive relationships in criptive coral reef environments. Am. Nat., 113: 223-234. Buttel, L., R. Durrett and S.A. Levin. – (in press). Competition and Species Packing in Patchy Environments. Theor. Pop. Bio. Chave, J., H.C. Muller-Landau and S.A. Levin. – (submitted). Comparing classical community models: Theoretical consequences for patterns of diversity. Am. Nat. Dawkins, R. – 1982. The Extended Phenotype: The Gene as the Unit of Seclection. W.H. Freeman, Oxford. Downing, J.A. and E. McCauley. – 1992. The nitrogen: phosphorus relationship in lakes. Limnol. Oceanogr., 37: 936-945. Durrett, R., and S.A. Levin. – 1994. The importance of being discrete (and spatial). Theor. Pop. Biol., 46: 363-394. Durrett, R., and S.A. Levin. – 1998. Spatial aspects of interspecific competition. Theor. Pop. Biol., 52: 30-43. Dushoff, J., L. Worden, S.A. Levin and J.E. Keymer. – (submitted). Scale invariance in community assembly. Ehrlich, P.R. and P.H. Raven. – 1964. Butterflies and plants - a study in coevolution. Evolution, 18: 586-608. Falkowski, P. – 1997. Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature, 387: 272-275. Falkowski, P.G. – 2001. Rationalizing elemental rations in unicellular algae. J. Physiol., 36: 3-6.

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SCI. MAR., 65 (Suppl. 2): 181-192

SCIENTIA MARINA

2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

Landscape challenges to ecosystem thinking: Creative flood and drought in the American Southwest* STUART G. FISHER, JILL WELTER, JOHN SCHADE and JULIA HENRY Department of Biology, Arizona State University, Tempe, AZ 85287, USA.

SUMMARY: Stream ecology is undergoing a transition from ecosystem to landscape science. This change is reflected in many studies; work at Sycamore Creek in Arizona will be used to illustrate the challenges of this transition and several applications. Conceptual challenges involve clear determination of the organization of research objectives. Ecosystem science is largely concerned with how things work while landscape ecology focuses on the influence of spatial pattern and heterogeneity on system functioning. Questions of system scale, hierarchical structure, dimensionality, and currency must be resolved in order to productively execute research objectives. The new stream ecology is more integrative, more realistic spatially, deals with streams at a larger scale, and treats them as branched system more than former approaches. At Sycamore Creek, studies of sand bar patches and their influence on organisms and nutrient cycling illustrate how variations in patch shape and configuration can alter system outputs. Beyond sandbars, inclusion of riparian zones as integral parts of streams produces a more coherent view of nutrient dynamics than previous studies that began at the water’s edge. Integration of streams with the landscape they drain requires that streams be viewed as branched structures, not linear systems. This view in ecology is in its infancy but it provides an opportunity to identify processing hot spots along flow paths and to reveal presumptive effects of climate change in terms of spatial shifts in biogeochemical activity rather than black-box rate changes. Key words: ecosystem, landscape, stream, flood, drought, riparian, nitrogen, biogeochemistry.

INTRODUCTION Stream ecology has been largely an ecosystem science for the past quarter century. Recently, stream ecologists have applied some of the ideas of landscape ecology to stream science. Unfortunately, few landscape ecologists have used streams as research laboratories for testing concepts of general application. Exceptions have viewed streams as arenas for study and have resolved spatial heterogeneity within the bounds of the linear channel (Sinsabaugh et al., 1991; Dent et al., 2001). This conceptual evolution of stream ecology as a sub-discipline has been mirrored in the structure of research in the Sycamore *Received July 9, 2001. Accepted August 2, 2001.

Creek Project in Arizona, USA. Our objectives in this paper are to use the Sycamore Creek project as a case study to illustrate how this conceptual transition has taken place and to discuss several issues that underlie this change from ecosystem ecology to landscape science. The Sycamore Creek study began as a study of succession in running waters. Flash flooding was the disturbance and changes in population, community and ecosystem attributes were monitored over time (Fisher et al., 1982). The sampling scale was essentially the square meter and spatial heterogeneity was scarcely considered. Data were scaled up to the reach (ca. 100 m) but spatial variation was ignored. The ecosystem in these early studies was considered the wetted channel and when the channel dried the STREAMS AS LANDSCAPES 181

ecosystem disappeared. Later studies elaborated recovery mechanisms in terms of life history strategies of invertebrates, primary production, and nutrient cycling (Fisher and Gray, 1983; Busch and Fisher, 1981; Grimm and Fisher, 1986). As research progressed, we met several challenges of interpreting observed patterns by invoking processes within the spatial and temporal confines of the wetted channel. Thus we expanded the system boundaries to include first the hyporheic zone (Valett et al., 1990), then sand bars (Holmes et al., 1994), then the riparian zone (Schade and Fisher, 1997; Marti et al., 2000). Since flash floods originated as precipitation falling at distant sites, we began to consider processes that occurred outside the main stem (e.g. in tributaries) and in upland terrestrial systems. While this required an expanded spatial perspective it also forced us to incorporate spatial (and temporal) heterogeneity. Not surprisingly, the stream was dry at times and places and certain processes occurred there and then as well. Drying was studied first as an alternative disturbance (to flooding) but it forced us to think at large scales and to incorporate the “terrestrial” ecosystem component into our understanding of stream structure and functioning (Stanley et al., 1997; Grimm and Fisher, 1992). This is where we are today and it is this perspective that we will illustrate in this paper. We will present three short case studies illustrating how ecological understanding is enhanced by resolving issues in a spatially explicit manner and will try to highlight research challenges that loom on the horizon. This gradual transition from ecosystem to landscape approaches has required several important changes in the way we think about streams. We think these are general and would apply in an expanded approach to any ecological system. Pattern-process linkage Patterns are the observations we attempt to explain by invoking alternative, multiple processes (hypotheses). As such, the pattern-process connection is central to hypothetico-deductive science (Fisher, 1994). This approach is nothing new but its connection with landscape ecology presents a novel wrinkle. Landscape ecologists may certainly observe patterns in landscapes (spatial patterns) or in landscapes over time (temporal patterns) and search for causes of these patterns. For example, what causes changes in terrestrial vegetation from mountain tops to foothills? Landscape ecology takes 182 S.G. FISHER et al.

this a step further and asks, what are the consequences of spatial pattern for some usually large scale process? For example, do strips of terrestrial vegetation influence the movement of materials downslope? Is this effect altered if the size or sequence (i.e. configuration) of these banded slopes is changed? In this sense, landscape ecology is asking how pattern (in space) alters process; that is, spatial pattern is an independent variable (Turner, 1989; Meentemeyer and Box, 1987). Context In stream ecology, two approaches can be adopted. We may do landscape ecology in streams or we may do landscape ecology of streams (Fisher, 1994). In the former case we would view streams, however defined, as the systems of interest and ask how spatial pattern influences process therein. For example, how do runs and riffles and pools interact? Does their sequence matter? Alternatively, streams can be viewed as a patch in a larger terrestrial landscape. In this case, streams represent transport corridors or boundaries or simply habitat patches for certain organisms such as fish and mosquitoes. Size, scale and hierarchy While there is some disagreement over whether landscape ecology is restricted to certain large scales or applies to the study of spatial heterogeneity wherever it occurs, in practical terms, the scale of an ecological investigation must be determined (Wiens, 1989; Pickett et al., 1989). Often, stream studies are of reaches which are defined in terms of what is seen by a human observer standing on the bank. But excellent smaller (insect habitat selection, leaf decomposition) or larger (river continuum, river basin) studies also exist. Size and scale are related except that scale connotes a relationship with hierarchical structure. A thorough discussion of hierarchy theory as it relates to streams is beyond the scope of this paper. Suffice it to say that there are several ways to increase system size and the most useful is to do it in the context of a hierarchy. For example, a study of fish in a 2 km reach of small stream could be increased in scale by examining a 2 km reach of continental river. Alternatively, scale could be increased by adding ecosystem components, such as the hyporheic or riparian zones or by examining longer and longer linear reaches or by expanding the study to include dendritic drainage networks. Each

of these scaling decisions is grounded in a different concept of the river system. A hierarchical approach forces us to deal with that central question. Furthermore, a hierarchical approach allows us to examine the structure of the system in an objective manner to determine natural scales for analysis, for example, by examining discontinuities (breaks) in fractal dimensions. Dimensionality Stream studies must be grounded in a spatial dimension. Streams are traditionally embraced in one or two-dimensional terms. Streams are considered linear systems (1-D) and several of the most significant advances in understanding of streams are limited to this view (river continuum concept, material spiraling). Other studies, especially those involved in biological sampling are 2-dimensional in that streams are dominated by benthic organisms. Plankton is rare or non existent. Larger rivers with significant plankton and hyporheic studies require a three-dimensional view. Time adds an additional dimension to each of these. Hierarchy theory teaches us that fractal dimensions may be significant as well. The fractal dimension tells us how an entity fills space. A one-dimensional stream is a line and a two-dimensional one is a plane (e.g. a catchment). The branched stream network is a fractional dimension, in this case the fractal is between 1 and 2 and tells us how the branched network fills the plane. Fractal dimensions between 2 and 3 may also be instructive but have not been used to describe streams. Such an analysis would incorporate changes in elevation. Consideration of fractals leads to the concept of self-similarity. Small drainage trees are similar in shape to large drainage trees; meanders in small streams have the same shape parameters as meanders in large rivers (within a limited range of scales). This suggests interesting questions about how ecological function changes as a function of scale (effect of pattern on process) if shape is conserved, or how shape influences function if scale (size) is conserved. Currency and Approach This idea of “function” is related to the idea of currency or “observation set” (O’Neill et al. 1986). Why are we studying the stream? What of the many things it does are we interested in? For example, the stream may provide a habitat for fish and at the same

time it transports water and materials. It may influence riparian vegetation in certain ways and transforms nitrogen in various ways. Each of these perspectives (currencies) may yield a differently structured system in terms of hierarchical units and fractal dimension. Depending on the currency, the appropriate scale for study may change. Or certain currencies may converge on a common structure. Stream ecology has not yet dealt with these questions of general ecological significance. Surely any given study of a stream or set of streams must be focused on a subset of possible observations. In Sycamore Creek for example, we have focused recently on the stream as a biogeochemical processor of nitrogen. This is the observation set that we will emphasize in the case studies presented below. With this approach, we need to identify operative patches in the system of interest, determine how they are connected, and resolve the changes (in through-flowing nitrogen) which occur in each. Once that is determined, effect of altered patch structure, processing, and connections can be evaluated. As you will see in the sections which follow a variety of scales are involved in these studies of Sycamore Creek.

SAND BARS AS FUNCTIONAL LANDSCAPE PATCHES The concept of streams as a surface water system is limited. Water moving in channels exchanges vertically and horizontally with adjacent subsystems such as hyporheic sediments, sand bars, and riparian zones. Sand bars are especially interesting in that they can occur in a variety of sizes and shapes. Furthermore, these shape parameters change over time after disturbance events such as flash flooding. Water moves freely (but slowly) through sand bars, where it experiences a suite of chemical and physical changes. Sand can be incorporated in stream models as an interacting compartment without specifying spatial relationships, but a much more thorough understanding of how sand bars influence the stream as a whole can be understood if sand is modeled in a spatially explicit way. In the discussion below, we will describe not the model itself, but the biologic and chemical interactions upon which such a model might be based. In the surface stream, water flows rapidly and organisms are exposed to light. In contrast, water flows more slowly through the alluvial interstices of STREAMS AS LANDSCAPES 183

sandbars and it does so in complete darkness. These physical differences result in striking biogeochemical differences. For instance, while rates of primary production can be very high in the surface stream of Sycamore Creek (Busch and Fisher, 1981), no photautotrophic production occurs in sandbar sediments. Microbial processes are often elevated in sandbar sediments because water flows more slowly and much sediment surface area is available for microbial attachment. In several stream and river ecosystems including Sycamore Creek, (Triska et al., 1989; Claret et al., 1997; Coleman and Dahm, 1990; Holmes et al., 1994) elevated rates of transformations among forms of nitrogen have been demonstrated in sand and gravel bars. In the surface stream of Sycamore Creek, periphyton removes inorganic nitrogen from solution and convert it to biomass. Ultimately, nitrogen leaves algae as organic nitrogen by excretion or decomposition and enters the surface stream, thereby elevating organic nitrogen concentration. When surface water enters sandbars this organic nitrogen is converted to inorganic nitrogen through heterotrophic breakdown and subsequent nitrification by microbes in oxic sandbar sediments (Holmes et al., 1994). As a result of these processes dissolved nitrate increases as water moves through sandbars and is highest where it exits sandbars and re-enters the surface stream. While nitrate is generally higher at locations farther along flowpaths, not all sandbar flowpaths exhibit net increases in nitrate. For instance, if along sandbar flowpaths, oxygen becomes depleted and sufficient organic matter is present, denitrification may be substantial in sandbar sediments making some sandbar sediments a permanent sink, removing N from the system (Holmes et al., 1995). Spatial differences in nitrogen has important consequences for periphyton community composition, primary production, and stream nitrogen retention, especially in N-limited streams, such as Sycamore Creek (Grimm and Fisher, 1986). Nitrate is highest where water upwells from the hyporheic zone or outwells from sandbars. Chlorophyll-a and primary production are higher at hyporheic upwelling zones than at downwelling zones (Valett et al., 1994). Similarly, blooms of algae occur in locations where water outwells from sandbars, usually at their downstream edges (Holmes et al., 1994). Not only are algae more abundant at outwelling edges than at inwelling edges, but cyanobacteria (free living or symbiotic with certain diatom species) show the 184 S.G. FISHER et al.

reverse pattern, being more abundant at inwelling edges where N is low. We hypothesized that these community differences exist because sources of nitrate are available at outwelling edges of sandbars and algae, which are limited by inorganic nitrogen, can grow more easily at these edges because of this nitrate source. Because nitrogen fixation is metabolically costly, cyanobacteria are poor competitors under high inorganic nitrogen conditions (Gutshik, 1981) and grow well at inwelling edges where nitrogen is low. We have found strong correlations between nitrate concentrations at sandbar edges and algal biovolume (positive) and cyanobacterial biovolume (negative) at sandbar edges. Because of the spatial variation in N availability, “algal” communities are segregated with fixers abundant at inwelling zones at the heads of bars and non-fixers predominating at outwelling edges at the tail of bars. Because cyanobacteria fix dinitrogen, they represent a direct input of N to the ecosystem which is highest at inwelling edges. In contrast, non-fixers remove fixed N (NO3 and NH4) from solution at outwelling edges. We found that from 60-98% of outwelling nitrate is retained by algal mats at outwelling edges through a combination of both nitrate uptake by algae and denitrification in algal mats at sandbar edges. By their mere presence sandbars influence rates of nitrogen inputs, transformation among forms of nitrogen and retention of nitrogen as well as the community composition of periphyton in the surface stream and its spatial variability. However, sandbars themselves vary in size and shape and their variation may influence stream ecosystem processes. The active channel of desert streams is dynamic. During flood events sandbars are rearranged and reshaped. They may also vary in composition in terms of organic inclusions, particle sizes, and packing. The configuration of multiple sandbars in a reach is also variable. Shortly after floods, many small bars of various shapes exist in the channel. Later, these coalesce into fewer larger bars. These structural variations may have several ecological consequences. Rates of organic matter breakdown and nitrification in sandbars and retention by algae at outwelling edges are influenced by rates of flow through the sandbar which are dependent on hydraulic gradient through the sandbar and hydraulic conductivity. Nitrate retained by algal mats at outwelling edges is dependent on flow rates through the sandbar. Deposits of organic material (detritus, roots, root

exudates) can elevate heterotrophic respiration leading to reduced oxygen and elevated denitrification (Schade et al., 2001). Distributions of sand bar vegetation, variations in hydraulic conductivity due to variations in sediment particle sizes, and variations in hydraulic gradient are features that vary substantially from sand bar to sand bar in a desert stream such as Sycamore Creek. The length of a sand bar is also important for stream nitrogen cycling. From research done by Holmes et al. (1994) we know that nitrate concentrations increase along sand bar flowpaths. Therefore, up to a certain distance, a longer sand bar will have higher outwelling nitrate concentrations than a shorter sand bar. Because the nitrate curve plateaus, presumably occurring when the substrate is exhausted, after a certain distance longer bars do not have increasingly higher nitrate concentrations. Because nitrate increases asymptotically with sand bar length, the way in which sand is distributed in multiple sand bars may also be important for stream nitrogen cycling. If a given volume of sand is distributed in a few long sand bars, less organic nitrogen will be transformed to nitrate than if that same amount of sand is distributed in many shorter bars (Fig. 1). In addition, a reach with few long bars may support less algal growth along its sand bar edges (because there are fewer edges) and it may export larger amounts of organic nitrogen to downstream ecosystems than would a stream reach with many small bars. This study has shown that streams extend beyond the wetted perimeter and certainly include sand bars. An understanding of the influence of sand bars cannot be gained without a spatially explicit knowledge

of the patch structure of the system and the relevant biogeochemical functioning of each patch (bar in this case). Since these relationships change dramatically in disturbance time (after flash flooding), patchiness must be resolved in a four-dimensional context. Clearly the black box, well-mixed reactor concepts of ecosystem ecology are inadequate to the task of understanding the structure and functioning of stream channels. This is even more true when the stream is expanded to include the riparian zone with its terrestrial plants.

RIPARIAN VEGETATION AND ECOSYSTEM PROCESSES While higher plants are often included in stream studies, these are usually vascular hydrophytes. i.e. aquatic plants. Recently, studies of riparian trees and their interaction with streams as nutrient filters have been productive. These studies are often based on a three compartment model: upland, riparian strip, and surface water. Vegetation serves to alter water quality by “filtering” materials from water as it moves from upland to stream across the riparian zone. In nature, spatial patterns are more complicated than this and filtration or retention can take several forms. Arid land studies have illuminated the nature of terrestrial - aquatic exchanges by presenting us with more complicated patterns of water movement and we have come to understand that several different types of organisms are involved. Finally, flood prone desert systems have provided an opportunity to place spatially explicit riparian studies in a temporal context that is equally heterogeneous.

FIG. 1. – Hypothetical stream reaches with different sand bar configurations but identical sand bar surface area. A. Reach with many small sand bars. B. Reach with one large sand bar. Small sand bars produce more nitrate because nitrate increases asymptotically with sand bar length

STREAMS AS LANDSCAPES 185

Studies of stream ecosystems have increasingly come to include riparian vegetation as part of the system of interest. The presence of riparian plants has been shown to influence nutrient cycling in streams through the retention of nutrients from subsurface water entering riparian soils from either upland or stream (Peterjohn and Correll, 1984; Lowrance et al., 1984; Groffman et al., 1992; Pinay et al., 1993; Lowrance, 1998; Hill, 2000). Much of the work establishing these relationships has taken place in mesic watersheds and tends to focus on the reach scale (km scale). This focus on the reach scale, although very productive in providing information regarding the general function of riparian zones in the landscape, has limited our ability to either effectively analyze watershed-level influences of riparian zones on retention or clearly determine the precise mechanism by which riparian plants cause retention. Very little work on riparian - stream interactions has explicitly taken a multi-scale approach, or considered the importance of spatial heterogeneity of riparian vegetation in understanding riparian-stream interactions. When rain falls on the Sycamore Creek watershed, it flows overland into small rivulets and channels that transport runoff water to larger perennial streams. In these larger channels water infiltrates coarse channel sediments and exchanges back and forth between stream and riparian zone as it moves down the catchment (Fetter, 1994). In the Sycamore Creek watershed, we have conducted research to help us better understand stream-riparian interactions including, 1) the magnitude and direction of hydrologic linkage between stream and riparian zone; 2) nitrogen retention by the riparian zone; and 3) the relative importance of potential retention mechanisms. However, due to the heterogeneous nature of this interaction, we utilized a multiple scale approach. Reach scale As mentioned above, much of what we know about stream-riparian interactions, particularly nutrient retention and hydrologic linkage, comes from the study of individual reaches. A number of approaches have contributed to our understanding of the mutual influence of stream and riparian zone at this scale. To explore hydrologic linkages, a common approach is to inject a conservative tracer, such as chloride or bromide and study patterns of dilution downstream from the injection site (Harvey and 186 S.G. FISHER et al.

Wagner, 2000). Non-conservative tracers, particularly nitrogen, have been used to gain insight into nutrient exchanges. For instance, nitrogen may be injected simultaneously with a conservative tracer to study declines in nitrogen concentration downstream of the addition point, providing an estimate of uptake length (Newbold et al., 1982) or nitrogen retention (Triska et al., 1989) in a spatial context. We conducted tracer additions, using both bromide (conservative) and 15NH4 (non-conservative) in a 400 m reach of Sycamore Creek to trace the movement of both water and nitrogen through several components of the ecosystem (Schade et al., in prep.). We used these tracers to determine strength and direction of hydrologic linkage and nitrogen exchange between stream and riparian zone and to estimate N retention by riparian vegetation, both through uptake and denitrification. In our investigation, we found an increase in peak bromide concentration in riparian wells with distance downstream from the point of injection. This is contrary to results from many mesic studies where peak concentration decreases with distance from the injection point. We conclude from this pattern that water moves laterally out from stream to riparian zone along the length of this reach and little unlabeled groundwater moves into the riparian zone from either lateral movement from the uplands or up from deeper groundwater sources. Therefore, streamriparian hydrology differs greatly between xeric and mesic ecosystems. We were also able to trace the movement of 15 NH4 from the surface stream into the riparian zone. We found that willow trees (Salix goodingii) were enriched in 15N following the addition, while other species of riparian trees were not (Fraxinus velutina, Platanus wrightii and Prosopis sp). These results indicate that willow trees take up stream water N, while other trees do not. Since willow trees tend to grow closer to the stream channel than these other species, these results, along with mass balance calculations, suggest that N carried into the riparian zone through hydrologic exchange is quickly removed in a narrow strip at the interface between stream and riparian zone (Fig. 2). Different tree species do not have equal access to stream N as a resource simply because of their position in the landscape. Furthermore, nutrient retention does not occur uniformally throughout the riparian zone, but tends to occur more rapidly at areas of interface between riparian zone and either stream (Schade et al., 2001) or upland slope (McClain et al., 1994).

FIG. 2. – Diagram showing hydrologic and nutrient connections between surface flow (“stream”) and riparian zone.

This suggests that, at the reach scale, the riparian zone is not homogeneous and that the species composition and spatial arrangement of vegetation influences retention of stream water nitrogen. A broader look at Sycamore Creek shows that these variables are also heterogeneous at the section scale, and highlights the importance of a broader scale perspective when we consider the influence of the riparian zone on total watershed-level N retention.

2001). If denitrification were included in this analysis, the influence of spatial variation in abundance of vegetation on retention would be much enhanced. We now not only have convincing evidence that riparian zones can be hot spots of N retention, but we have also seen that the importance of riparian zones can vary tremendously in space, necessitating explicit attention to large scale spatial heterogeneity. Stand scale

Catchment scale Estimating the importance of the riparian zone requires more than just scaling up the results from our reach scale study because riparian vegetation is heterogeneously distributed. A good estimate of the relative importance of retention by the riparian zone requires a larger scale analysis of the distribution and abundance of riparian vegetation. Density, species composition, and size distribution of riparian trees were measured along a 12-km section of Sycamore Creek. This information was used to estimate production and N uptake by riparian trees, with an eye towards understanding spatial variation in retention through vegetative uptake. These reaches varied greatly in N uptake, which, not surprisingly, was heavily influenced by abundance and species composition of riparian trees, and was highly variable from reach to reach. In addition, the presence of vegetation has also been shown to have a positive influence on rates of denitrification (Schade et al.,

As mentioned above, the presence of riparian vegetation has a positive influence on both N uptake and denitrification. The common link between these two potential N retention mechanisms and vegetation makes it difficult to determine the relative importance of them without manipulative experiments designed to test them separately. These manipulative experiments are obviously impossible to do at a 12-km scale, and are very difficult at the reach scale as well. What is needed to do these experiments is a reduction in the scale of investigation to a system of manageable size. The active channel of Sycamore Creek consists of both surface water and dry gravel bars. These gravel bars often support the growth of a woody shrub, Baccharis salicifolia, which is often distributed in patches of one or several individual plants bunched together. These patches are relatively isolated from each other by areas of open, uncolonized gravel bar. This distribution allows us to treat these STREAMS AS LANDSCAPES 187

patches as replicates in manipulative experiments. Since these patches are generally less than 1 m2 in area and the plants are relatively hardy, we were able to transplant individual plants, as well as perform other manipulative experiments, allowing us to differentiate the relative importance of uptake and denitrification. In general, we found high rates of N retention and denitrification in sediments from colonized patches. These effects were lost when the plant was removed and established in previously uncolonized locations when plants were transplanted. The results of these experiments provided strong evidence that most N retention observed in Baccharis colonized gravel bars was due to denitrification fueled by organic matter production by the plant (Schade et al., 2001). These studies of the riparian zone show that hydrologic connections between riparian zone and surface stream are strong and significant in terms of processing and retention of materials. Several mechanisms are involved and these processes vary greatly in space and time. To understand how streams operate, we require a multi-scale, spatially explicit understanding of spatial patterns of riparian vegetation and hydrologic exchange with the stream, as well as temporal variation due to season or disturbance effects (succession).

STREAM-UPLAND CONNECTIONS Whether spatially explicit or not, stream studies have usually embraced the stream as a linear ecosystem of indeterminate length. As stated before, tributaries are conceptual nuisances. Watershed (catchment) models usually include a terrestrial, an aquatic, and an atmospheric compartment (Likens et al., 1967). This conception, while useful in mass balance terms, tells us nothing about where and when important transformations occur. Nor does this model help us understand how streams inter-digitate with the land and render the entire complex an integrated throughflow system. In reality, streams begin as precipitation strikes the land surface, and at this point the ratio of terrestrial to aquatic influence is large indeed. Conceptually, stream ecosystems are far away, yet in reality, this is where they begin. Terrestrial-aquatic continuum Raindrops strike dry desert soil and move across the landscape through patches with variable topog188 S.G. FISHER et al.

raphy and vegetative cover, en route to the downstream, more aquatic components of the watershed. Yet, how do we define “terrestrial” and “aquatic” components of watersheds? In reality, we see a continuum from “more terrestrial” to “more aquatic” as we follow the movement of water from the highest ridge tops in the catchment, into the smallest rivulets that drain upland slopes, and into progressively larger channels. To date, most terrestrial studies have ignored the role of streams in nitrogen transport and processing (Vitousek and Reiners, 1975; Peterjohn and Schlesinger, 1990), while most stream studies have neglected the drainage networks that reach up into the terrestrial environment, comprising the terrestrial-aquatic continuum. Likewise, stream ecologists have developed concepts including energy and nutrient budgets (Fisher and Likens, 1973; Meyer and Likens, 1979; Grimm, 1987) and nutrient spiraling (Newbold et al., 1981) in short reaches of large permanent streams; however, these streams occupy the most aquatic end of the continuum and do not adequately represent the complex networks of streams found in any watershed. Stream ecologists have operationally defined first order streams as the smallest streams that maintain perennial flow (Allan, 1995). This typical usage of stream order makes ecosystem comparisons difficult, since a stream defined as first order in the Sonoran Desert may differ dramatically in width, depth, discharge and catchment area from a first order stream located in a temperate deciduous forest. Furthermore, variation in the accuracy of maps, map scale and difference between wet and dry years (Allan, 1995) makes the definition of stream order even more subjective. This operational definition adopted by stream ecologists is not in agreement with the more strict geomorphic definition of stream order originally proposed by Horton (1945) and Strahler (1964), where a first order stream is the smallest unbranched channel on the ground. In our research, we are working to resolve previous “black box” models both spatially and temporally, considering streams as branched networks that occupy the full extent of the terrestrial-aquatic continuum. Nitrogen retention Our interest in nitrogen processing and removal along the terrestrial-aquatic gradient is motivated by several observations. Inorganic nitrogen in Sycamore Creek flood water is high and variable in time. Peak concentrations occur in floods following

long droughts, and concentrations decrease with increasing flood frequency (Grimm and Fisher, 1992). These observations suggest that nitrogen accumulates in the ecosystem between storms, while large infrequent rain storms result in release and transport of nitrogen to downstream ecosystems. In addition, mass-balance calculations show that nitrogen input generally exceeds export in arid lands of the Southwest (Schlesinger et al., 1999; Peterjohn and Schlesinger, 1990), including Sycamore Creek (Grimm, 1987). In the Sycamore Creek watershed, only ten percent of the nitrogen supplied in annual atmospheric deposition is exported in surface runoff from the catchment; yet, we do not know the fate of the missing nitrogen or the location of “hot spots” in the landscape that are responsible for nitrogen removal. In addition, rain that falls on these desert landscapes is highly variable in both space and time. Summer monsoon storms are typically small in spatial extent and short in duration (Sellers and Hill, 1974), but these storms are intense and can produce a large amount of rain in a short period of time. In contrast, winter storms tend to be less intense but of longer duration, and across both summer and winter rain seasons, rainfall amount associated with individual storms is highly variable. This variation in rainfall may influence the location of nitrogen processing and retention in the watershed. There are several mechanisms that may remove nitrogen from runoff water as it moves through the watershed. Nitrogen may be stored in plant biomass or soil, or it may be permanently lost to the atmosphere as a result of volatilization of ammonia or denitrification, which transforms nitrate to nitrogen gas (Sprent, 1987). In general, some retention mechanisms act on ammonium, some on nitrate, and each requires a specific set of conditions to operate; conditions that may vary considerably along the terrestrial-aquatic continuum. Data collected in the Sycamore Creek Watershed indicate that during the earliest storms in a rain season, runoff is dominated by ammonium while later storms produce nitrate-dominated runoff. Since nitrification is more sensitive to water stress than mineralization (Sprent, 1987), nitrification may be quite low prior to the onset of the rain season, causing this seasonal pattern. Soil moisture not only varies seasonally, but also in relation to topographic position, which may influence nitrogen transformations across the landscape. For example, Ohte et al. (1997) found that lysimeter samples from dry slopes

contained both ammonium and nitrate, while samples from wet slopes contained only nitrate, and saturated samples contained neither ammonium nor nitrate. This study suggests that nitrification was inhibited in the driest sites, while dentrification predominated in the saturated sites. Therefore, we would expect nitrogen retention via ammonium adsorption or volatilization to be highest under dry conditions, while denitrification would predominate under saturated conditions. Yet, the mode of retention varies spatially and temporally. The process of denitrification requires organic carbon and localized zones of anoxia (Sprent, 1987); therefore, patches in the landscape with high moisture and organic matter may stimulate denitrification. Given these requirements, we might expect “hot spot” intensity for denitrification to increase with stream order or size, with the highest rates of denitrification occurring along streams with well developed riparian zones where organic matter content and moisture are both high. However, on an areal basis, most of the catchment is composed of dry upland patches, dotted with a mix of desert shrubs and trees. During storms, conditions are also favorable for denitrification under the canopies of these “more terrestrial” desert shrubs. Therefore, storms may in essence, switch on nitrogen transformations in the drier components of the watershed, but they may remain active (on) for only a short period of time. Which of these components (upland terrestrial or downstream aquatic) is greater in a given catchment will depend upon the spatial structure of the landscape and temporal patterns in rainfall. Over the past two years we have been monitoring rainfall amount, rainfall rate and chemistry, as well as the extent of runoff and runoff chemistry contributed from upland slopes and intermittent channels that hydrologically link the terrestrial components of the watershed with more permanent wetlands downstream. The amount of rainfall associated with individual storms, as well as the intensity of the storm, both influence the extent of flow, or hydrologic connectivity in the landscape. Small storms wet upland slopes, which occupy the terrestrial end of the continuum, but do not transport water and nutrients into channel networks. Thus, small storms may activate “hot spots” for nitrogen retention in the terrestrial component of the watershed (e.g. soils); however, as storm size and intensity increases, materials are transported from upland slopes into first and second order rivulets. During STREAMS AS LANDSCAPES 189

FIG. 3. – Hypothetical nitrogen retention “hot spot” maps. A.) Small storms wet and activate (turn on) upland “hot spots.” Rates of nitrogen retention vary across the upland landscape in relation to soil properties and moisture conditions. B.) As storm size increases, materials are mobilized and water and nutrients are transported into the intermittent channel network. During intermediate-sized storms, nitrogen retention may primarily occur in low order channels. C.) During large storms, materials are transported to the largest order channel in the catchment, where nitrogen retention may occur; however, material may also be exported to downstream ecosystems, including larger streams and lakes.

these intermediate-sized storms, low order channels may serve as collection points for materials including nitrogen and organic matter, and under high moisture conditions, these channels may experience pulses of denitrification. As storm size and intensity continues to increase, material transport extends into larger and larger channels. Retention “Hot Spots” Based on these data, we can produce a hypothetical “hot spot” map, depicting the spatial distribution of nitrogen transformation rates in the watershed in relation to storm size and intensity (Fig. 3). Localized zones of nitrogen retention migrate or shift further downslope with increasing storm size. Small storms wet or activate upland slopes, but as storm size increases, materials move into intermittent channels, which may shift activity to progressively larger channels. Only during the largest, relatively infrequent storms does flow reach large perennial streams, including the main stem of Sycamore Creek. Therefore, most of the time, nitrogen retention “hot spots” may be confined to the “more terrestrial” components of the watershed. Just as we see spatial gradients in moisture, vegetation density, and particle size from the terrestrial to the aquatic components of the watershed, we may see gradients in nitrogen retention that correspond with increasing storm size. 190 S.G. FISHER et al.

So, the question remains - where is the missing nitrogen? We suggest that nitrogen retention “hot spots” in the Sycamore Creek Watershed are variable in space and shift in relation to storm size, intensity and frequency. In order to better understand nitrogen transport and retention in watershed ecosystems, we must explicitly consider the link between the spatial structure of the watershed, from “more terrestrial” to “more aquatic” along the hydrologic flowpath, and changes in these patterns over time. Our motivating question “where and when do important nitrogen transformations occur?” is by definition a landscape rather than an ecosystem question because it involves space in an explicit way as an independent variable. The entity of interest is the landscape and because running water perfuses the entire space, the concepts of aquatic (ecosystem) or terrestrial (ecosystem) lose meaning. Clearly this is a continuum. Traditional aquatic organisms such as fish and aquatic plants and mosquito larvae have a restricted distribution as do upland cacti and lichens and rattlesnakes. But, as we have shown, trees are crucial to the functioning of large streams and “aquatic” bacteria fix nitrogen on sporadically moist ridge tops. Viewed from the perspective of flow paths (space) and episodic climatic events (time), the desert landscape emerges as an integrated, interconnected but spatially heterogeneous whole. The challenge of understanding requires that we move beyond our compartmentalized view of ecosystems and incorporate the broader integrative view provided by landscape ecology.

CONCLUSIONS These case studies indicate that stream ecology is expanding conceptually by becoming more spatially explicit. Resolution of ecological function in terms of flow paths, patch shapes, and material processing and/or retention has been a lucrative theme and it conceptually transforms landscapes from static mosaics to spatially explicit, dynamic, spatially-oriented continua with a strong episodic climate and weather-driven functioning. This view has tended to integrate terrestrial and aquatic ecosystems in a functionally meaningful way. Conceptual challenges persist in incorporation of lakes, estuaries, and oceans in this integrated landscape view. Surely many vectors of linkage occur in addition to the hydrologic linkages invoked in the stream landscape

arena. Many of these involve water movements but these may be generated by wind action (currents), pressure systems (seiches), lunar cycles (tides), or rainfall. Other forces such as gravity (landslides, leaf fall, sedimentation), weather systems (atmospheric linkages), and biological factors (migration) can link subsystems in a heterogeneous landscape. We contend that these properties provide a window on cause and effect relationships (process, pattern) by separating them in space. In many ways separation of processes in space helps to resolve them more clearly and to deduce causation more definitively than if processes occur simultaneously or are separated in time only.

ACKNOWLEDGEMENTS This research was supported by NSF grants DEB 9727311 and DEB 0075650.

REFERENCES Allan, J.D. – 1995. Stream ecology: structure and function of running waters. Chapman and Hall. Busch, D.E. and S.G. Fisher. – 1981. Metabolism of a desert stream. Freshwater Biol. 11(4): 301-308. Coleman, R.L. and C.N. Dahm. – 1990. Stream geomorphology: effects on periphyton standing crop and primary production. J. N. Am. Benthol. Soc., 9(4): 293-302. Dent, C.L., N.B. Grimm and S.G. Fisher. – 2001. Multiscale effects of surface-subsurface exchange on stream water nutrient concentrations. J. N. Am. Benthol. Soc., 20: 162-181. Fetter, C.W. – 1994. Applied hydrogeology, 3rd Edition. Macmillan College Publishing company, New York. Fisher, S.G. – 1994. Pattern, process and scale in freshwater ecosystems: Some unifying thoughts. In: P.S. Giller, A.G. Hildrew and D.G. Rafaelli (eds), Aquatic Ecology: Scale, Pattern and Process, pp. 575-591. Blackwell Scientific Publications. Oxford. Fisher, S.G. – 1997. Creativity, idea generation, and the functional morphology of streams. J. N. Am. Benthol. Soc., 16: 305-318. Fisher, S.G. and G.E. Likens. – 1973. Energy flow in Bear Brook, New Hamsphire: an integrative approach to stream ecosystem metabolism. Ecol. Monogr., 43: 421-439. Fisher, S.G., L.J. Gray, N.B. Grimm and D.E. Busch. – 1982. Temporal succession in a desert stream following flash flooding. Ecol. Monogr., 52(1): 93-110. Fisher, S.G. and L.J. Gray. – 1983. Secondary production and organic matter processing by collector macroinvertebrates in a desert stream. Ecology, 64: 1217-1224. Grimm, N.B. – 1987. Nitrogen dynamics during succession in a desert stream. Ecology, 68: 1157-1170. Grimm, N.B. and S.G. Fisher. – 1986. Nitrogen limitation in a Sonoran Desert Stream. J. N. Am. Benthol. Soc., 5: 2-15. Grimm, N.B. and S.G. Fisher. – 1992. Responses of arid land streams to changing climate. In: P. Firth and S.G. Fisher (eds.), Global Climate Change and Freshwater Ecosystems, pp. 211233. Springer-Verlag, New York. Groffman, P.M., A.J. Gold and R.C. Simmons. – 1992. Nitrate dynamics in riparian forests: Microbial studies. J. Environ. Qual., 21: 666-671. Gutshick, V.P. 1981. Evolved strategies in nitrogen acquisition by plants. Am. Nat., 118(5): 607-637. Harvey, J.W. and B.J. Wagner. – 2000. Quantifying hydrologic

interactions between streams and their subsurface hyporheic zones. In: J.B. Jones, Jr., and P.J. Mulholland, (eds.), Streams and Groundwaters, pp. 3-44. Academic Press. Hill, A.R. – 2000. Stream chemistry and riparian zones. In: J.B. Jones, Jr., and P.J. Mulholland (eds.), Streams and Ground Waters, Academic Press. Holmes, R.M., S.G. Fisher, and N.B. Grimm. – 1994. Parafluvial nitrogen dynamics in a desert stream ecosystem. J. N. Am. Benthol. Soc., 13: 468-478. Holmes, R.M., S.G. Fisher and N.B. Grimm. – 1995. Denitrification in a nitrogen-limited stream ecosystem. Biogeochemistry. 33: 125-146. Horton, R.E. – 1945. Erosional development of streams and their drainage basins: hydrophysical approach to quantitative morphology. Geol. Soc. Am. Bull., 56: 281-300. Likens, G.E., F.H. Bormann, N.M. Johnson, and R.S. Pierce. 1967. Tha calcium, magnesium, potassium, and sodium budgets for a small forested ecosystem. Ecology, 48; 772-785. Lowrance, R.R. – 1998. Riparian forest ecosystems as filters for nonpoint-source pollution. In: M.L. Pace and P.M. Groffman, (eds.), Successes, limitations and frontiers in ecosystem science, pp. 113-141. Springer-Verlag. Lowrance, R.R., R. Todd, J. Fail, O. Hendrickson, R. Leonard, and L. Asmussen. – 1984. Riparian forests as nutrient filters in agricultural watersheds. Bioscience, 34: 374-377. Marti, E., S.G. Fisher, J.J. Schade and N.B. Grimm. – 2000. Flood frequency, arid land streams. and their riparian zones. In: J.B. Jones and P.J. Mulholland (eds.), Streams and Ground Waters, pp 111-136. Academic Press. San Diego. McClain, M.E., J.E. Richey, and T.P. Pimetel. – 1994. Groundwater nitrogen dynamics at the terrestrial-lotic interface of a small catchment in the Central Amazon Basin. Biogeochemistry, 27: 113-127. Meentemeyer, V. and E. Box. – 1987. Sale effects in landscape studies. Landscape heterogeneity and Disturbance M.G. Turner (ed.) Pp 15-34. Springer Verlag. N.Y. Meyer, J.L. and G.E. Likens. – 1979. Transport and transformation of phosphorus in a forest stream ecosystem. Ecology, 60: 1255-1269. Newbold, J.D., J.W. Elwood, R.V. O’Neil and W. Van Winkle. – 1981. Measuring nutrient spiralling in streams. Can. J. Fish. Aquat. Sci., 38: 860-863. Newbold, J.D., R.V. O’Neill, J.W. Elwood and W. Van Winkle. – 1982. Nutrient spiraling in streams: Implications for nutrient limitations and invertebrate activity. Am. Nat., 120: 628-652. Ohte, N., N. Tokuchi and M. Suzuki. – 1997. An in situ lysimeter experiment on soil moisture influence in inorganic nitrogen discharge from forest soil. J. Hydrology, 195: 78-98. O’Neill, R.V., D.L. DeAngelis, J.B. Waide and T.F.H. Allen. – 1986. A hierarchical concept of Ecosystems. Princeton University Press, Princeton. Peterjohn, W.J. and D.L. Correll. – 1984. Nutrient dynamics in an agricultural watershed: observations on the role of the riparian forest. Ecology, 65: 1466-1475. Peterjohn, W.T. and W.H. Schlesinger. – 1990. Nitrogen loss from deserts in the southwestern United States. Biogeochemistry 10: 67-79. Pickett, S.T.A., J. Kolasa, J.J. Armesto and S.L. Collins. – 1989. The ecological concept of disturbance and its expression at various hierarchical levels. Oikos, 54: 129-136. Schade, J.D. and S.G. Fisher. – 1997. The influence of leaf litter on a Sonoran desert stream ecosystem. J. N. Am. Benthol. Soc., 16(3): 612-626. Schade J.D., E. Marti, J.R. Welter, S.G. Fisher and N.B. Grimm. – 2001a. Sources of N to the riparian zone of a desert stream: implications for riparian vegetation and nitrogen retention. Ecosystems, (in press). Schade, J.D., S.G. Fisher, N.B. Grimm and J.A. Seddon. – 2001b. The influence of a riparian shrub on nitrogen cycling in a Sonoran Desert Stream. Ecology, (in press). Schlesinger, W.H., A.D. Abrahams, A.J. Parsons, and J. Wainwright. – 1999. Nutrient losses in runoff from grassland and shrubland habitats in Southern New Mexico: I. rainfall simulation experiments. Biogeochemistry 45(1): 21-34. Sellers, W.D. and R.H. Hill. – 1974. Arizona Climate. Univ. of Arizona Press. Tucson. 616 pp. Sinsabaugh, R.L., T. Weiland and A.E. Linkins. – 1991. Epilithon patch structure in a boreal river. J. N. Am. Benthol. Soc., 10: 419-429.

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Sprent, J.I. – 1987. The ecology of the nitrogen cycle. Cambridge University Press, Cambridge. Strahler, A.N. – 1964. Quantitative geomorphology of drainage basins and channel networks. In: V.T. Chow (ed.), Handbook of Applied Hydrology. McGraw-Hill, New York. Stanley, E.H., S.G. Fisher and N.B. Grimm. – 1997. Ecosystem expansion and contraction: a desert stream perspective. BioScience, 47: 427-435. Triska, F.J., V.C. Kennedy, R.J. Avanzino, G.W. Zellweger and K.E. Bencala. – 1989. Retention and transport of nutrients in a

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third-order stream in northwestern California: Hyporheic processes. Ecology, 70: 1893-1905. Turner, M.G. – 1989. Landscape Ecology: the Effects of pattern on Process. Ann. Rev. Ecol. Syst., 20: 171-197. Valett H.M., S.G. Fisher and E.H. Stanley. – 1990. Physical and chemical characteristics of the hyporheic zone of a Sonoran Desert stream. J. N. Am. Benthol. Soc., 9: 201-215. Vitousek, P.M. and W.A. Reiners. – 1975. Ecosystem succession and nutrient retention: a hypothesis. BioScience, 25: 376-381.

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2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

Spirals on the sea* WALTER MUNK University of California at San Diego, Scripps Institution of Oceanography, La Jolla, California 92093 USA. E-mail: [email protected]

SUMMARY: Spiral eddies were first seen in the sun glitter on the Apollo Mission 30 years ago; they have since been recorded on SAR missions and in the infrared. The spirals are globally distributed, 10-25 km in size and overwhelmingly cyclonic. They have not been explained. Under light winds favorable to visualization, linear surface features with high surfactant density and low surface roughness are of common occurrence. We have proposed that frontal formations concentrate the ambient shear and prevailing surfactants. Horizontal shear instabilities ensue when the shear becomes comparable to the coriolis frequency. The resulting vortices wind the liner features into spirals. The hypothesis needs to be tested by prolonged measurements and surface truth. Spiral eddies are a manifestation of a sub-mesoscale oceanography associated with upper ocean stirring; dimensional considerations suggest a horizontal diffusivity of order 103 m2 s-1. Key words: Remote sensing, air-sea boundary, frontal formation, mixing

INTRODUCTION The first photographs of spiral eddies appears to have been taken on Apollo-Saturn in October 1968. In the late 70’s SEASAT with its synthetic aperture radar (SAR) confirmed the early discoveries from crewed spaceflights. But most of the existing material was collected by Paul Scully-Power (the first and so far only oceanographer-astronaut) on 5-13 October 1984: “Far and away the most impressive discovery… is that of the submesoscale ocean (less than 100 km) is far more complex dynamically than ever imagined…. Patterns of this complexity could be seen to be interconnected for hundreds and hundreds of kilometers” (Scully-Power, 1986; Stevenson 1998, 1999). *Received July 20, 2001. Accepted August 16, 2001.

The spiral pattern whose global distribution was reported by Scully-Power is at an awkward scale, virtually impossible to recognize from shipboard, and too large to be encompassed even from high-flying aircraft. Discovery had to await space missions.

SPIRAL IMAGES IN THE SUN GLITTER AND IN SAR Figures 1 and 2 show a visual and SAR image, respectively, of spiral streak patterns. Spirals are globally distributed (Fig. 3). Typical spiral dimensions are from 10 to 20 km, with streaks 50 to 100m wide. Spirals are overwhelmingly cyclonic, wound anti-clockwise (viewed from above) in the Northern Hemisphere, clockwise in the Southern Hemisphere. Ship wakes crossing the streaks (not shown) have a SPIRALS ON THE SEA 193

FIG. 1. – A pair of interconnected spirals in the Mediterranean Sea south of Crete. This vortex pair has a clearly visible stagnation point between the two spirals, the cores of which are aligned with the preconditioning wind field. 7 October 1984.

FIG. 2. – Spirals in the Mediterranean Sea visualized with Shuttle XSAR. The streaks are differentially smooth. 9 October 1994.

194 W. MUNK

13 1

8

6 4 12

10 11

3

7 2

5

equator

9

FIG. 3. – Distribution of spiral eddies from Scully Power’s (1986) visual observations and our collection of 400 images. The 13 numbered locations refer to MAFZ.

cyclonic offset with shears up to 10–3 s–1. We need to refer to Munk, Armi, Fischer and Zachariasen (2000) [henceforth MAFZ] for a more representative selection (13 images out of 400 collected). The observational material poses three questions: - How are the spirals wound? - How is symmetry broken in favour of cyclonic rotation? - What makes spirals visible? On SAR images the streaks are always dark, indicating a reduced scattering cross-section, e.g. differentially smooth water. Natural biogenic surface films are organized by near-surface convergence into linear streaks with over 40% surfactant coverage at low winds. The concentration is associated with nearly inextensible surface films which dissipate capillaries and short gravity waves. The film thickness required to dampen the short waves is only 0.01 to 0.1 mm. On the optical images the smooth streaks are bright in the inner sun glitter (which requires low rms slopes for reflection of the sun into the camera) and dark in the outer glitter. The situation is complex and not well understood, and we refer to MAFZ (1225-30, 1236-7) for further discussion. But evidently the third question can be restated as follows: What is the circulation pattern that collects the surfactant material into streaks (which are subsequently wound into a spiral pattern)? Multiple stripes at km spacing presumably are associated with helical circulation rolls in the atmospheric boundary layer. In addition, frontal instabilities can concentrate and distort the surfactant, as we shall see.

AMBIENT OCEAN VORTICITY Measurement of surface velocity shear du/dy along 1000 km of roughly northward track in the North Pacific (Rudnick and Ferrari, 1999) indicate values of order 10-5 s-1. The situation is conveniently portrayed by a distribution of Rossby Numbers Ro = z / f where z = ∂v/∂x - ∂u/∂y is the vertical component of vorticity (cyclonic is positive) and f is the Coriolis frequency (Fig. 4). The distribution is symmetric, with very few values exceeding 1/4. There are a few outlyers showing a slight preference of cyclonic vorticity for large |Ro|, and this has since been confirmed (Rudnick and Ferrari, 1999).

FIG. 4. – Rossby number in the upper 250 m sampled at 3 km spacing along 1400 W from 250 N to 350 N in the North Pacific (Rudnick and Ferrari, 1999). SPIRALS ON THE SEA 195

50

t = 0.5

40

The above paper also shows that the shear is distributed over a broad band of scales, from kilometers to hundreds of kilometers.

HORIZONTAL SHEAR INSTABILITY 50

t = 1.0

40 30 60 50

t = 1.5

40 30

Starting from parallel shear flow with an inflection point, Figure 5 shows a numerical simulation of the development of the most unstable mode (Corcos and Sherman, 1976, 1984). Time is in units of the initial reciprocal shear at the stagnation point. The numerical experiment was intended to model a vertical shear flow, but may as well be interpreted in terms of a horizontal shear flow. There is no implication of the sense of rotation; in fact we have reversed the published drawing from anticyclonic to cyclonic rotation. Streamlines show the development of Kelvin’s celebrated “cat’s-eye” solution. Particles inserted along the interface exhibit the growth of a spiral.

60

BREAKING SYMMETRY

50

t = 2.0

40 30

FIG. 5. – Computer simulations of a developing shear instability (Corcos and Sherman, 1984). The four panels show the streamlines at times 0.5, 1.0, 1.5, 2.0 (in units of the initial reciprocal shear). Heavy line is the “cat’s-eye” streamline through the stagnation points. The dots represent particle positions initially placed on the interface; they are initially crowded near the two stagnation points to allow for a subsequent large strain. The model allows for diffusion and viscosity. We have reversed the original figure from anticyclonic to cyclonic rotation.

th or

N

y(

w

D(r, q)/Dt = 0, r q = (f + z) ∑ -r where D/Dt is the substantial derivative. The starting point is a vertically mixed layer with a horizontal density transition from warm and light in the south (say) to cold and heavy in the north (Fig. 6, left). The initial density gradient develops into an east-

Rossby number Ro = +1

)

z

Hoskins and Bretherton (1972) have solved a problem of frontogenesis with conservation of density and potential vorticity,

critical shear Ri = 1/4

+3

c

+1

–.4

–. 3

x τ=0

τ = 2.5

τ = 2.75 α = 0.3

FIG. 6. – Cartoon for the generation of ocean spirals (see text).

196 W. MUNK

α = 0.7

ward “thermal wind”, as shown. A deformation field g = ∂u/∂x - ∂v/∂y is superposed, causing the initially vertical isopycnals to tilt northward. Up to this point there has been no breaking of symmetry, all directions can be reversed. In the subsequent development we use “north” and “east” only for convenient reference to the figure. The northward tilting of isopycnals is not uniform; the northern isopycnals converge at the surface, and the southern isopycnals diverge. Accordingly the associated eastward thermal jet has a strong cyclonic shear at its northern (left) flank and a weak anticyclonic shear at it southern (right) flank. At time 2.5 (measured in g -1 units) the associated Rossby numbers are Ro+ = +1 and Ro- = -0.3, respectively. At this stage the underlying rate of strain no longer determines the rate of development. Rather, the isopycnal “collapse” takes the form of a “Rossby Adjustment Problem” with f-1 ª 10-4 s-1 taking the place of g -1 ª 10-5 s-1 as the relevant time scale (Ou, 1984). In the short time interval between 2.5 to 2.75 g -1 the cyclonic shear grows from Ro+ = 1 to Ro+ = 3, and at 2.89 g -1 the density gradient at the left flank develops Ro+ = infinity, while anticyclonic shear remains at Ro- = -0.3. The crucial point is that starting at a time when Ro+ is of order +1 the cyclonic shear zone becomes a breeding ground for spiral eddies long before appreciable anticyclonic vorticity has been generated. In Figure 6 the third panel has been emphasized because at this time the vertical shear at the surface at the front reaches a value of du/dz = 2 N (N is the buoyancy frequency) corresponding to a Richardson number (N/(du/dz))2 = 1/4 and suggesting the onset of vertical shear instability. An independent consideration has to do with the visibility of the spiral arms, presumably the result of the alignment and concentration of surfactants. Consider an elementary surface area dx dy at time zero. With the developing front the area is elongated along the x-axis on both flanks of the developing jet. But in accordance with the Hoskins and Bretherton theory, at the time 2.75 g -1 the area has expanded (by a factor 7/4) on the anticyclonic side, while it has contracted (to 1/4 the original area) on the cyclonic side. Thus the frontal theory has the elements to account for both the visibility and sense of rotation of the spiral eddies. But when examined in detail the story is not as clearcut as presented here, and we must refer to MAFZ for a detailed discussion.

To confuse the issue, there is another independent set of processes to explain the dominance of cyclonic vortices. It follows from the Rayleigh criterion of stability (extended to include coriolos acceleration) that cyclonic circular vortices are stable and anticyclonic vortices are unstable (MAFZ 6.21), and this leads to an “inertial instability” criterion Ro < 1 which goes back to Pedley (1969). Oceanographers are familiar with the vertical shear (Richardson) instability for du/dz > 2N but surprisingly unfamiliar with the horizontal shear (Pedley) instability for du/dy > f.

DISCUSSION We take the following position regarding the three questions. How are the spirals wound? By the cat’s eye circulation associated with horizontal shear instability, almost any spiral pattern of particle distribution can be interpreted as a legacy of past vortex deformation. How is symmetry broken in favour of cyclonic rotation? It is unresolved whether the dominance of cyclonic vortices is associated with a dominance in cyclonic horizontal shear early in the formation process, or with the relative instability of anticyclonic vortices in the mature stage. What makes the spirals visible? By the accumulation of surfactants along lines of horizontal surface convergence which are subsequently twisted into spiral patterns by the developing vortex.

TESTING THE HYPOTHESIS Our hypothesis is based on observational material which consists almost entirely of unrelated glimpses in x,y-space on the sea surface. For a satellite in a low earth orbit (LEO) a given point remains within view for only about 6s. What is required here are prolonged stares or frequent repeat visits coordinated with shipboard observations. We cannot think of any x,y,z,t ocean processes that had been properly identified from measurements in half the coordinate space. We must assume that there are serious flaws in the foregoing presentation. SPIRALS ON THE SEA 197

FIG. 7. – The proposed experiment.

Following his 41-G space mission in October 1984, Scully-Power (1986) wrote: “The almost ubiquitous occurrence (of spiral eddies), whenever submesoscale dynamics was revealed in the sun glitter, indicates that they are perhaps the most fundamental entity in ocean dynamics at this scale. The difficulty is in explaining their structure.” The only serious attempt at analysis has been in a Norwegian Doctoral dissertation which explores baroclinic instabilities in a narrow cyclonic shear zone (Eldevik and Dysthe, 1999). Why has the problem received so little attention in the thirty years since discovery? We assert that the fashion during these years has been statistical rather than phenomenological descriptions of ocean features, and here we are concerned with a truly phenomenological problem. Figure 7 sketches a proposed experiment. SAR imagery from an overhead drone is examined by the authors on shipboard in real time. The image shows the position of the vessel which is about to enter a spiral streak. 198 W. MUNK

REFERENCES Corcos, G.M. and F.S. Sherman. – 1976. Vorticity concentration and the dynamics of unstable free shear layers. J. Fluid Mech., 73: 241-264. Corcos, G.M. and F.S. Sherman. – 1984. The mixing layer: deterministic models of a turbulent flow. Part I. Introduction and the two-dimensional flow. J. Fluid Mech., 139: 29-65. Eldevik, T. and K.B. Dysthe. – 1999. Short frontal waves: can frontal instabilities generate small scale spiral eddies. Selected Papers of the ISOFRP, (eds. A. Zatsepin and Ostrovskii, A.), UNESCO. Hoskins, B.J. and F.P. Bretherton. – 1972. Atmosphere frontogenesis models: mathematical formulation and solution. J. Atmos. Sci., 29: 11-37. Munk, W, L. Armi, K. Fischer and F. Zachariasen. – 2000. Spirals on the Sea. Proc. R. Soc. Lon. A, 456: 1217-1280. Ou, Hsien Wang. – 1984. Geostrophic adjustment: a mechanism for frontogenesis. J. Phys. Oceanogr., 14: 994-1000. Pedley, T. J. – 1969. On the stability of viscous flow in a rapidly rotating pipe. J. Fluid Mech., 36: 177-222. Rudnick, D.L. and R. Ferrari. – 1999. Compensation of horizontal temperature and salinity gradients in the ocean mixed layer. Science, 283: 526-529. Scully-Power, P. – 1986. Navy Oceanographer shuttle observations, STS 41-G Mission Report. Naval Underwater Systems Center. NUSC Technical Document 7611: 71 pp. Stevenson, R.E. – 1998. Spiral eddies: the discovery that changed the face of the oceans. 21st Century Science and Technology. 11: 58-71. Stevenson, R.E. – 1999. A view from space: the discovery of nonlinear waves in the ocean’s near surface layer. 21st Century Science and Technology, 12: 34-47.

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2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

Natural History: the sense of wonder, creativity and progress in ecology* PAUL K. DAYTON and ENRIC SALA Scripps Institution of Oceanography, La Jolla, California 92093, USA.

SUMMARY: This essay addresses the question of blending natural history and ecological wisdom into the genuine creativity exemplified by Prof. Ramon Margalef. Many have observed that modern biology is a triumph of precision over accuracy, and that ecology has sought maturity by striving toward this model in which the precision value of the tools has supplanted important questions. In pursuing a model of hard science, ecology has struggled with Popperian approaches designed to create a thin patina of “real science” over the vast seas of uncertainty so admired by the naturalists. We start with a discussion of the importance of natural history in ecology and conservation, and the present state of natural history in academic ecology. We then discuss the respect for natural history in human cultures, and conclude that an infatuation with authority has obfuscated the important truths to be found in nature. We consider some general processes associated with creativity, and finally we ask how natural history influences creativity in ecology. We conclude that the soaring creativity exemplified by Ramon Margalef is based on a joyful almost spiritual understanding of natural history and the courage to avoid authority. Key words: natural history, ecology, scientific progress, traditional knowledge, authority, understanding of nature.

INTRODUCTION “A nine-story terrace rises up from a basket of dirt” Lao-Tzu, Te-Tao Ching People have impacted essentially all the habitats in the biosphere. There are growing societal needs for an ecological science that can correct the environmental insults and contribute to management of sustainable ecosystems. Questions regarding ecological management are ubiquitous and difficult. For example, all habitats suffer cumulative impacts; how can one evaluate the ecological damage of particular small impacts without a baseline of what is natural? That is, since the system is already perturbed, how *Received May 29, 2001. Accepted July 27, 2001.

can one generalize ecological limits to additional perturbations? One needs to understand stabilizing processes such as persistence, resilience and recoverability or successional processes that can simplify or make communities more complex. Natural systems are characterized by variation at all scales: how do ecologists determine thresholds across the scales? Worse, a priori, can we predict a threshold? Considering the highly perturbed condition of so much of our environment, restoration is another management issue of growing importance. Realistically it almost never can be natural in the sense of restoring ecological conditions characteristic of prehuman contact (Pitcher, 2001). So what arbitrary goals does restoration require? How does one restore a habitat even assuming a desired goal? Which species traits are useful in restoration? How ECOLOGY BASED ON A SENSE OF NATURE 199

do human caused extinctions shape future diversity and evolution? Such insights must come from a very solid understanding of ecological processes in such a way that future trends can be deduced from past and present processes. These issues involve knowledge of minimum population size, genetic connectivity, positive and negative relationships such as symbiosis or diseases. Important insights into the resolution of almost all these questions can be found in the natural history of the ecosystems, and traditional and local ecological knowledge very likely offer some of the most perceptive ideas and hypotheses. But where does natural history fit? Is it a science? Natural history provides the foundation of ecology. Consider Wallace who probably deduced natural selection before Darwin and observed patterns in nature wherever he went. Consider Bates and Muller with their appreciation of mimicry, a subject now considered of fundamental evolutionary importance (for example, perhaps up to 35-50% of all non-venomous snakes are mimics, Harry Greene, pers. comm.). Natural history is therefore the underpinning of ecology and evolution science. There is no ecology, no understanding of the functioning of ecosystems and communities, no restoration, or in fact, little useful environmental science without an understanding of the basic relationships between species and their environment.

THE STATE OF NATURAL HISTORY IN ECOLOGY TODAY Despite its fundamental role, natural history recently has been ignored and dismissed. It has been displaced, expelled from the ivory tower, and it is presently seen as less prestigious than other disciplines. More than ever, ecologists study problems caused by human activity, but they study these problems in the absence of an understanding of natural patterns. Usually ecologists have not sufficiently considered human culture as an integral part of the equation, or unequal power between cultures and how that leads to destruction. Because of funding realities, many scientists pursue funding opportunities themselves rather than asking what are the most appropriate questions and at what scale should they be studied. Finally they continue the tradition of testing hypotheses, often at inappropriate scales, rather than seriously attempting to solve problems. Often they ignore other science traditions, long-term 200 P.K. DAYTON and E. SALA

common sense observations, and their own scientific foundation of natural history. Biology undergraduates at many universities in the United States are not taught the “classic” Botany or Zoology. Many first-year graduate students do not know major phyla or the life history biology of their study organisms. Without grounding in the fundamentals of natural history, students will have difficulties in understanding ecology. Yet, some of them have been taught ecology using textbooks based almost entirely on molecular biology and theoretical population biology. This prevailing attitude denies students the sense of wonder and sense of the place fundamental to the discipline. Worse, there are ecologists who have never seen the communities or populations they model or speculate about, and who could not identify the species composing these communities. This is like having the illusion of conducting heart surgery without knowing what a real heart looks like.

WHY THE DEMISE OF NATURAL HISTORY? Why is natural history so dismissed? Natural history and systematics often are disparaged as stamp collecting, the implication being that the practitioners mindlessly collect facts. This elitist attitude is based on ignorance of the old naturalists and systematists who were deeply observant: they saw much in nature and carefully wrote it down, sometimes in beautiful poetic prose that rings through the ages, or sometimes they struggled under the enormity of the truth they were communicating, and one can sense their commitment to understanding nature. It is a terrible disservice to imply that they were collectors of trivial facts. This was never true; nobody collects facts or describes species in a vacuum. Furthermore, no generalizations can be made without repeated observation. Moreover, we have heard from several prestigious ecologists that natural history is a discipline that does not require a great intellect. Ironically, such opinions are formulated by specialists, masters of techniques rather than true detectives of the natural world. Real progress in understanding nature tends to be made by generalists, but the selection for individual success lies at the extreme – the specialist. Fretwell (1972) described this process in terms of divergent fitness of ecologists attempting to integrate general theory and natural history. In this context, ecologists are judged by specialists, and in

order to be successful in the eyes of specialists, one must specialize also. The selection to specialize is based not on the real understanding of nature, but on social influences from colleagues usually acting as competitors and judges. The irony is that ecological progress depends upon a synthesis of theory and sophisticated analysis, modern technology, and especially natural history. As ecology moved from descriptive to mechanistic phases, our sociology moved toward T.S. Kuhn’s paradigmatic behavior in which we are most comfortable within a larger framework where the questions and rules are clear and there are strong social pressures to conform. This is formalized by the flow of support from individualized small science to very large integrated research programs where the players have small roles well defined by the group. They also have large budgets that reward group mentalities more than individual creativity. What does this imply for scientific creativity? The recent past in the United States has seen a great deal of support for coordinated programs (e.g. IPB, LTER, JGOFS, GLOBEC) as opposed to small individual programs. This general model would tend to preclude proposals by young investigators who have not been accepted into the invisible colleges that control the large programs. It is important to emphasize that large scale programs tend to address important questions, and they must be based on cooperation and integration. But at the same time they are sufficiently expensive that risk absolutely must be minimized, and such risk-averse philosophies select bookkeepers rather than the high-risk poets such as Ramón Margalef. Ironically, while low risk and productive, the large-scale programs have not produced as many great innovative leaps as individual efforts of naturalists. It is clear that respect for natural history is social and is recoverable, but the respect has to be at the ground level. Sadly, the loss of nature itself due to human abuse of the biosphere is much more permanent and central. This leads to a vicious circle in that the loss of our natural heritage inevitably results in the loss of the human experiences in nature where the expectations and love of natural relationships are learned. Thus we are missing our appreciation of what has been lost, and these reduced expectations of nature result in the loss of respect for it. How do we break this circle? This is a serious problem because the beauty of and the empathy with nature represent the soul of ecology. This soul has been eroded as the loss of nature continues with less and less passion exerted in her defense. It seems as

though our self-esteem somehow has been misplaced, and we now focus on the importance of our specialization without much regard for the evolutionary wisdom of the ages that is lost.

NATURAL HISTORY IN TRADITIONAL CULTURES “Out of the ground the Lord God formed every beast of the field and every bird of the air, and brought them to the man to see what he would call them; and whatever the man called every living creature, that was its name.” Genesis 2.19. It would appear that natural history has a long tradition in Judeo-Christian cultures, as Adam’s first task was to establish the natural history of his ecosystem (Farber, 2000). This respect for natural history can be seen far earlier in the ice age caves of southern Europe where artists with remarkably perceptive sensitivity to nature as seen in animal behavior was rendered in the magnificent work reaching back over 30,000 years. Elsewhere, at least that long ago, Australian people were also creating wonderful art that eventually showed a fine understanding of anatomical details, and the Pleistocene history of the manipulation of their habitats shows sophisticated understanding of the natural history (Flannery, 1994). The dreamtime mythology of Australia, so extremely sensitive to the local natural history, is matched by the mythology of most cultures around the world. It is obvious that people have always had a love-fear relationship with nature, and that from the very beginning human beings have been extremely sensitive naturalists. And indeed, while we are fast losing these human cultures (Nettle and Romaine, 2000), many were based on sophisticated understanding of the patterns and processes of the natural world around them (Johannes, 1981). Are there any fundamental differences between such traditional understanding of nature and the type of understanding to which ecologists aspire? Were these early naturalists also ecological scientists? Does modern ecology exclude such sophisticated understanding of nature? Indeed, the urgency to succeed forces young scientists to get along with their elders and to write many papers with rather limited focus, so, to follow the above examples, we do have some short-lived oral history, but where are the artists who paint the cave paintings with such brilliant renditions of nature? ECOLOGY BASED ON A SENSE OF NATURE 201

ECOLOGICAL VALUES (AND THEOLOGICAL PARALLELS) To better understand what we are losing by dismissing natural history, we need to explore the evolution of ecology and of science in general. We believe that human value systems strongly influence science. E.O. Wilson (1998) has written, “Science…is the sword in the stone that humanity finally pulled. The question it poses, of ultimately lawful materialism, is the most important that can be asked in philosophy and religion. Its procedures are not easy to master, even to conceptualize; that is why it took so long to get started, and then mostly in one place, which happened to be Western Europe.” He continued, “Science is the organized systematic enterprise that gathers knowledge about the world and condenses the knowledge into testable laws and principles. The diagnostic features of science that distinguish it from pseudoscience are first, repeatability: the same phenomenon is sought again, preferably by independent investigation, and the interpretation given to it is confirmed or discarded by means of novel analysis and experimentation. Second, economy: scientists attempt to abstract the information into the form that is both simplest and aesthetically most pleasing – the combination called elegance – while yielding the largest amount of information with the least amount of effort. Third, mensuration: if something can be properly measured, using universally accepted scales, generalizations about it are rendered unambiguous. Fourth, heuristics: the best science stimulates further discovery, often in unpredictable new directions. Fifth, consilience: the explanations of different phenomena are most likely to survive are that that can be connected and proved consistent with one another.” What are the scientific values in ecology? How do they evolve? How can one learn the values of an academic discipline? For the most part the academic values are learned from examples and teachings of practitioners. Obviously the values are broad enough to cover almost any type of research, but while it is rarely explicitly stated, the practice of ecology is laden with rules and authorities that interpret these rules. These rules tend to ignore the importance of history at all scales. It is very rare to see an appreciation of the fact that all marine populations evolve in a total environment (abiotic and biotic) that includes geological time as well as oceanographic processes, and that many of these factors are important if not experimentally testable. None of them are approachable with single tools. 202 P.K. DAYTON and E. SALA

Authority By what authority have these important rules evolved? Ecologists surely are not the only ones who love authority. The wonderful Aristotelian natural history of the classic era was largely lost or grotesquely corrupted by Christian authorities that based their concept of reality in their interpretation of the Bible. Much of the interpretation is based on the writings of Augustine of Hippo (Aurelius Augustinus 354-430 AD), who, as an early Christian, developed a fixation on the importance of authority. He searched for truth and dabbled with many religions that based their concepts of truth on assertions and untested authority. He developed an obvious and strong attraction to Plato’s ideal model of truth perceived only as dim shadows in the back of a cave. Augustine struggled through this: “We feast on sewage while dimly remembering the nectar and ambrosia of high heaven.” He persuaded himself that Plato’s ascent to truth equated knowledge with virtue. Augustine compared Babylon, the city of man (necessarily corrupt and evil) with his City of God, which flourishes eternally, beyond all strife. Note the Platonic parallels between perceived and ideal. Augustine saw the sacraments of the church as absolutely necessary. Without their aid, all men would inevitably succumb to evil. He wrote the first Catholic justification for state persecution of those in error of not accepting the authority of the church; to Augustine, error has no right. To disbelieve in forced conversions is to deny the power of God; and God must whip the son He receives per molestias erudito. Interestingly, to Augustine, true education begins with physical abuse. His mind shut down all that opposed his established authority, and Augustine became the father of the Inquisition. This fixation on authority was challenged by the Irish Johannes Scotus Erigena, (810-877) who was anti-Platonic, and whose fundamental principle was reason based on nature. His De Divisione Naturae (the Division of Nature – written in 870) based all authority on reality that he defined as nature. His main theme was that reason (and nature) was a much more powerful means of ascertaining truth than authority or faith. He argued that real authority could only be derived from nature. To Scotus, nature is a synonym for reality, and he considered reality as found in nature to supplant the Platonic thinking codified by ecclesiastical authority of the Church. He emphasized reason and logic over platonic authority. He used this to oppose all authority – every authority not confirmed by true reason

(nature) seems to be weak, whereas true reason (nature) does not need to be supported by any authority. In 1225 Pope Honorius III ordered all copies of De Divisione Naturae burned. But there is an irony: When Honorius died, the new Pope, Clement IV, commissioned Roger Bacon to write his opus in 1266. Roger Bacon was the first renaissance inductionist and advocate of the experimental method that he explicitly developed. He set forth a system of natural knowledge that must have been influenced by the recently burned works of Scotus. He was explicitly anti-authoritarian and defined the following stumbling blocks to comprehending the truth: 1. Beware the example of frail and unworthy authority 2. Beware long established custom 3. Beware the sense of the ignorant crowd 4. Beware the hiding of one’s own ignorance under the pretense of wisdom. Some of this old wisdom must ring true to many ecologists who sat politely though lectures on various theoretical constructs, and thought to themselves: “but in the real world….” Or wondered what has really been learned from exercises designed for the statistical elegance of the analysis rather than interesting general questions about nature. Or have struggled with other statistical rules based on Augustinian authority rather than Scotus’ sense of reality. Or why, when we know the natural history, must we ignore the reality and create null models based on ignorance of this knowledge? It seems that the value of natural history and experimental analysis have been with us for hundreds of years, but our culture easily acquiesces to the Augustinian authority within the infrastructure of our science. Ecologists ought to challenge these self-proclaimed authorities and return to the values of Johannes Scotus and recognize nature as the ultimate authority. Surely this is not to reject the great value to the theoretical work that 1) is based on appropriate natural history, 2) provides answers that can not be determined empirically, or often 3) in conservation where there is great urgency. Nor is this to reject the importance of the established format of developing and testing theory; rather it addresses our questions and allegiance to unworthy authority. Are we looking for significance or truth? It is easy to falsify stupid null hypotheses and obfuscate the truth. Einstein dreamt himself traveling on a light beam and solved one of the most intractable questions of modern physics. His quantum leap was

doubtlessly facilitated by the fact that he was not in academia and hence not limited by any authority. The objective of this essay is to return our focus to nature. The testing of theory remains the cornerstone of science, but if ecologists embed this process in excellent natural history such that the tests are based in reality, we might recover the joy and spirit of natural history from the trivia imposed by some authorities while at the same time developing a better understanding of ecology.

ARE NATURALISTS POETS OR BOOKKEEPERS? Wilson (1998) argues that in science, original discovery is everything: scientists do not discover in order to know, but rather they know in order to discover. He sees a distinction with the social scientists: when attempting to sort out knowledge in order to sift for meaning, and especially when carrying out that knowledge outside the circle of discoverers, he is classified as a scholar in the humanities, but without original discoveries, one is not a scientist. A fundamental distinction thus exists in the natural sciences between process and product. The difference explains “why so many accomplished scientists are narrow, foolish people, and why so many wise scholars in the field are considered weak scientists. Scientific research is an art form; it does not matter how you make a discovery, only if your claim is true and convincingly validated.” To Wilson, the ideal scientist thinks like a poet and works like a bookkeeper. Likewise, Margalef (1997) stated that a naturalist is more a poet than an engineer. A social scientist’s perspective is different: “The closer historians of science look at the great achievements of science, the more difficulty they find in distinguishing science from pseudoscience and from the political, economic, and ideological contexts (Nader, 2000).” She observes that social scientists often fail to perceive scientific progress in the same self-serving Pollyannaish perspective as do the “hard” scientist. “Wisdom is better than strength; Nevertheless the poor man’s wisdom is despised, and his words are not heard.” (Ecclesiastes 9:14-16). There is an age-old dichotomy: realism vs. relativism, scientific novelty vs. permanent wisdom, science vs. religion and all the history summarized as two cultures by C.P. Snow. Social scientists recognize cultural bias in all claims of universal factuality – science is but one system of belief among many as the very concept of scientific truth is a social construction invented by scientists. ECOLOGY BASED ON A SENSE OF NATURE 203

While well known and discussed, like most dichotomies, this is misleading and is hurtful to both sides because it emphasizes the extremes and minimizes the “golden mean” of Aristotle. Obviously both extremes occur: there is a continuing social construction and growing empirical knowledge. Real progress occurs when science can be built on social wisdom in such a way that it is relevant to society as a whole. In this sense we see further when we stand on the shoulders of both giants. Where do ecologists fit into this concept of science? Is ecological science opposed to humanities? What are our original discoveries? Are we poets if we follow these rules? Can we be both wise scholars and good scientists? Where is our creativity in ecology? Is academic ecological knowledge superior to traditional or local ecological knowledge? Our thoughts about the importance of these rules come from experiences with peer review and editorial judgments, professional interactions with colleagues, etc. Are these rules inimical to creativity? Are the distinctions between science and pseudoscience outlined by Wilson and enforced by our reviewing system compatible with ecological poetry? What if we go farther back and look at the ice age hunters’ understanding of natural history? Can anyone imagine that people so sensitive to the behavior of these animals did not understand a great deal about their ecology? Or consider the understanding exemplified by native fishing cultures: “When it comes to understanding fish behavior so as to manage its exploitation efficiently, full-time fishermen may know more than marine biologists…the native fisherman searches with his eyes and ears and he is…more in touch with his prey and their surroundings than his modern mechanized counterpart (Johannes 1981).” In order to avoid false or misleading comparisons between a model of science identified with reason and the domination of nature, and native uses of knowledge, it is imperative to document the process of knowledge formation and its use (Johannes, 1981, 1998). Certainly the same is true now as those who live and work in nature understand it the best.

What is ecological wisdom? With the institution of specialists, wisdom has been lost, and our culture seems much poorer for this. It is interesting to juxtapose the wisdom of the ages that can be found in art and compare it to the progress in ecological research now often divorced from natural history. Certainly this is a matter of scale, perspective, and attitude. Ancient people have always had great respect for scholarship, and our greatest advances have come from very diverse minds. This is true in the arts as well as in science and one only has to look for example to the huge intellectual breadth of artists such as Samuel Coleridge or scientists such as Niels Bohr or especially Leonardo DaVinci. In all cases, wisdom involves the big picture, the entire spectrum of relationships. It is also a matter of keeping your eyes and soul open to the beauty around you. Or, as Confucius said: “Everything has its beauty but not everybody sees it.” Ecological wisdom involves the ability to see the beauty in nature and to integrate it into the patterns and processes studied by ecologists. Interestingly, this puts the values right back to Johannes Scotus. How do we perceive nature? Where is the beauty? Does nature intrinsically foster an attitude of love, empathy and a source of wonder and joy (the biophilia of Wilson)? Throughout human history we have been selected to conquer nature; it is a source of fear and threat, something that can feed us or kill us. Yet primitive people exalt nature. If not a love of nature, most cultures are built around a respect for nature. An empathy and appreciation of nature is solidly built into most human mythology. Certainly it induces a sense of awe and wonder in those who have enjoyed it. But it is fair to ask whether natural history has relevance to the science of ecology. We argue that it does and we are concerned about the loss of respect for natural history and systematics. Do working ecologists build their science on natural history? The answer is not very often, and lost in normative fashionable ecology is respect for nature herself.

ECOLOGICAL WISDOM

PROGRESS: NATURE, CREATIVITY, AND SCIENTIFIC METHODS

Where is the life we have lost living? Where is the knowledge we have lost in information? Where is the wisdom we have lost in knowledge? T.S. Elliot

How does genuine creativity occur? Is there a connection with natural history? We might look for examples associated with creative people. One means of identifying creative insights in science is to evaluate premature ideas. Science is full of pre-

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mature ideas. Some like Mendel’s work was simply ignored. Other premature ideas were considered outrageous and not worthy of attention (e.g. Gondwanaland, catastrophic events). How are we to separate outrageous from ridiculous or silly ideas in ecology? It was Einstein who said that, if an idea did not look absurd the first time, it was hopeless. As the value of Bayesian statistics sinks into ecological thinking, the importance of a subjective source of creativity becomes much more obvious. What are the pathways to creativity? Do they relate to natural history or do they come via some other medium? We can look to artists as well because scientists follow similar paths to creativity. 1. Almost all creative people are very curious about nature: they are inspired by nature. 2. Creative events do not happen de novo: they come from people well versed in their fields. In ecology they must be based on good natural history. Ecological science can be general or specific, but not to be real is fatal. This experience also provides a “feel for the system,” which is nothing else than intuition. Intuition may not be considered “hard science,” although it can be more valuable than other limited approaches to understanding nature. Ecologists ought to understand that intuition is another way to analyze data. The problem with accepting it is that we still do not understand how intuition works. 3. Orthogonal views are common. Creativity is often not so much original as it is simply a different approach, a new twist, the “deductive leap.” It is not luck: it comes from constantly looking for alternative approaches. In ecology the orthogonal views usually come from an appreciation of the natural history of the system wedded to an understanding of various scales. 4. Creative thinking is often associated with social courage to dream and fantasize and be different. Kids do a great job. “Let’s pretend.” Adults are impressed with creativity but often fail to support this process. As Coleridge said, “Genius resides in a combination of a child’s sense of magic and an adult’s trained mentality.” 5. For some reason peer pressure destroys imagination. But consider the observation of Jose Clemente Orozco: “Errors and exaggerations do not matter. What matters is boldness in thinking... in having the temerity to proclaim what one believes to be true without fear of consequences. If one were to await the possession of absolute truth, one must either be a fool or a mute.” Creative ecologists must

have the courage to put imagination at public risk without fear of making a mistake. Finally, 6. Creativity comes from passion. The human brain is the ultimate instrument, and it works best with joy, curiosity and enthusiasm. Yet modern scientists are trained to reject passion. “The ignorant crowd” fails to recognize the importance of joyful enthusiasm. Scientists often push the importance of extreme skepticism. In fact skepticism and a sincere effort to negate hypotheses is critical to science. This is appropriate, it is our most effective tool, but the tool only can be applied to ideas that spring from creative human minds. In this sense it is important to realize that the essential negativism of science can suppress the value of a good hunch, the educated guess that comes from a sense of the place and the problem. The value of enthusiasm, of joy, blended into a real gut feel for the system, is part of the creative process. The enthusiasm, joy, and deep pleasure so often associated with the human passion for nature and natural history is the source of almost all the creative leaps in ecology. Nobody better exemplifies this soaring creativity than Ramón Margalef. Are stimulating hypotheses science? When rigorous application of scientific methods to trivial hypothesis is mistaken for good science, precision triumphs over accuracy. How can ecological scientists move from the mystical artistic relationships to good science? In the 18th century meteorology focused on the beauty of the clouds; great effort went into creating a natural history of cloud forms, and the compilations were esthetically pleasing and much appreciated, but they contributed almost nothing to our understanding of weather and climate which awaited the development of atmospheric sciences based on rather ordinary laws of physics. In the same sense, naturalists such as Aristotle, Elton, Darwin, Wallace, etc. produced spectacular visions of patterns in the natural world – but have these patterns produced solid ecological understanding that can be generalized? Of course they can, but the generalizations depend upon the understanding of the processes that create the patterns.

CONCLUSIONS Wilson (1998) described the structure of science correctly, but he did not define the objectives of science, especially in a way that can relate to ecology. A common problem in recent ecology is that the ECOLOGY BASED ON A SENSE OF NATURE 205

generalizations are based on inappropriate assumptions rather than on good natural history. These generalizations masquerade as science because they are mensurate and precise, esthetically pleasing and appear heuristic and consilient, but they are not easily repeatable, and often are not relevant to reality. We hold that the goal of useful science is to make interesting accurate generalizations about nature based on as few relevant parameters as necessary. Obviously the generalizations must be accurate and general. By accurate they must be based on Scotus’ reality. While trivial generalizations abound, good science, to have value, must produce generalizations interesting to a wide audience. Finally, the relevant parameters are meant in an exclusive sense; good science must weed out the marginally relevant parameters because all of nature is trivially related. The generalizations must be based on those few parameters that can account for most of the uncertainty, following Ockam’s parsimony principle. In this sense good natural history absolutely permeates ecological science because it defines every component of these objectives. Creative ecology is based on a deep sensitivity to natural patterns and processes. Naturalists have the ability to synthesize perceptions of nature into reasonable hypotheses about the processes that cause the patterns, and then shift into the relatively simple scientific technology of testing hypotheses such that they contribute to a more general understanding of nature. In this sense, good natural history is fundamental to ecological science. If we are to conserve what we love, we must imprint this love in our future ecologists. That is, building the house from the basement, teaching sound natural history in all universities having degrees in Biology or Ecology. This might sound evident to most European scientists, but it is not the case in many universities. Without a sound formation on natural history, we risk producing narrowminded ecologists. Naturalists are closer to poets than to engineers (Margalef, 1997), and it is the intuition based on first-hand experience and common

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sense that produced the better leaps of thought. We should imprint on our students the importance of intuition, imagination, creativity, and iconoclasm, and prevent restricting them with the braincuffs of rigid assumption frames and techniques, if we are to revitalize an ecological science that is more than ever becoming a stronghold of fundamentalism.

ACKNOWLEDGEMENTS First, it is a huge pleasure for us to acknowledge the career-long inspiration we have received from the example of Ramón Margalef. His thorough scholarship, his passion, love and understanding of nature, and his courage to be different and follow his own path have offered an example for all humanity. We thank Laura Nader and Reed Noss for sharing unpublished texts of lectures they gave to the Ecological Society of America meeting in August 2000, and S. Abbott, F. Coleman, H. Greene, R. Johannes, P. Levin, E. Parnell, E. Scripps and L. Wesson for comments.

REFERENCES Farber, P.L. – 2000. Finding order in nature; the naturalist tradition from Linnaeus to E.O. Wilson. The Johns Hopkins University Press, Baltimore. 136 pp Flannery, T. – 1994. The future eaters. Reed Books, Chatswood NSW, Australia. 423 pp Fretwell, S.D. – 1972. Populations in a Seasonal Environment. Princeton University Press, Princeton, N.J. 217 pp. Johannes, R. – 1981. Words of the Lagoon; fishing and marine lore in the Palau District of Micronesia. University of California Press. Johannes, R. – 1998. The case for data-less marine resource management: examples from tropical nearshore finfisheries. Trends Ecol. Evol., 13: 243-246. Margalef, R. – 1997. Our Biosphere. Ecology Institute, Oldendorf/Luhe. Nader, L. – 2000. Lecture before the Ecological Society of America (August, 2000) Nettle, D. and S. Romaine. – 2000. Vanishing voices; the extinction of the world’s languages. Oxford University Press. New York. 241 pp Pitcher, T. – 2001. Fisheries managed to rebuild ecosystems? Reconstructing the past to salvage the future. Ecol. Appl. 11(2): 601-617. Wilson, E.O. – 1998. Scientists, scholars, knaves and fools. Am. Sci., 86: 6-7.

SCI. MAR., 65 (Suppl. 2): 207-213

SCIENTIA MARINA

2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

The top layers of water bodies, a most important although relatively neglected piece of the biosphere plumbing* RAMÓN MARGALEF Departament d’Ecologia, Facultat de Biologia, Universitat de Barcelona, Diagonal 645, 08028 Barcelona, Spain.

SUMMARY: Reducing power from light is used by plant life in ways that shift along ecological succession. When nutrients are non limiting, growth prevails; when essential nutrients (in the first place P) become scarce, reducing power is applied somehow and otherwise, often, as in red tides, in the synthesis of toxics. On land, the same reducing capacity results in the production of wood, terpenes, essences, cork or rubber. In water bodies, reduction of nitrate at least adds nitrite to the environment. Very likely this explains the common presence of nitrite-enriched layers around the levels of twilight. A large fraction of the generating capacity might be expected to come from the small prokaryota of phytoplankton, which almost global ubiquity and capacity to persist alive in a state of forced minimal activity are known. The result might be a kind of one-way plankton surface valve, that isolates partially and in some chemical aspects the deeper ocean from the top layers. One could perhaps speak of a surface valve with a planetary role. Key words: picoplankton, light reducing power, nitrite, ocean surface valve, dinoflagellates, coccolithophorides, Western Mediterranean

I feel immensely grateful to friends and colleagues for their very special invitation to attend this meeting. For me it is like a lease on my scientific life, and I will profit of this privilege for expressing myself freely, also in the hope of benefiting from new instruction that could clarify what have been for me, and still in part are, persistent problems. My subject now concerns the functional structure of the surperficial layers of the water bodies –and specifically of the oceans. My feeling is that the rich degree of organization at a small scale of the top layers of the oceans, and their dynamics, isolates very effectively and in a rather complex way the atmosphere from the larger mass of ocean waters. Now there are possible new approaches to old problems, although many doubts remain. The relatively recent *Received February 15, 2001. Accepted March 20, 2001.

recognition of the omnipresence of very small prokaryota, forces any phytoplankton student to reconsider the classical views. The indefinite –even close to “eternal”– vitality of such small things, associated with their capacity to generate reducing power, and their “unsinkability”, explains their presence in important and potentially very active layers of the hydrosphere. I am asking myself if the generated kind of situations might be compared, from a global point of view (could I dare to write Gaia’s point of view?), to those that prevail on land. Plankton communities get reducing power from light and apply it to grow biological organization. The very tiny things for which planktonologists did not care sufficiently until now, are responsible for the creation and maintenance of a sort of “plankton surface valve” effective in controlling gas exchanges with the atmosphere. I remember having discussed THE TOP LAYERS OF WATER BODIES 207

this aspect with Richard Vollenweider many years ago, in relation with lakes and reservoirs, but the validity of the same mechanism in the oceans was not clear to me until recently, when the life and activity of a large number of tiny, pigmented cells, apt to persist inactive in some kind of “suspended animation” became obvious to the students of plankton, as a last or at least penultimate stage in the gradual recognition of small and smaller living elements suspended in water and practically immortal through periods of suspended activity. The quality of being virtually unsinkable matters very much through providing a background quality that “colours” potentially and uniformly a mass of water, to which it confers some reducing power, small or large. I will keep insisting in the very important fact that the smallness of the organisms under consideration bounds them almost solidly to water, in the sense that active or passive, such tiny beasts do not sink naturally or, at least, they should move downwards with extreme slowness. Again, their smallness assures their ubiquitous availability at every level and their perpetual and universal effectivity as potential providers of reducing power. These small organisms absorb radiation and make available reducing power everywhere. Phosphorus is necessary for biosynthesis, and most generally its scarcity is the factor that sets limits to the grow of “real” life. If phosphorus is no more available, light reaching the photosynthetic system results in the generation of extra chemical reducing power that could be put to varied uses, significant in survival and evolution, even if some of their supposed functions might appear not essential or only secondarily helpful in competition. A good argument in favour of this assertion may start considering the role played by wood in terrestrial ecosystems, best expressed in the success of the tree as dominant life-form on land. This could led immediately to suspect some possible utility or positive effect of the reducing power of picoplankton –and also of phytoplankton of larger size, if nutrients (read, mainly, phosphorus!) are only minimally available. To be sure, besides wood leading to occupation and use of space and to historical persistence, reducing power available on land provides further for synthesis of a large spectrum of helpful materials, from essences to cork and rubber. I think that through such kind of considerations we could be better prepared to grasp more adequately any important role for the most tiny organisms suspended in sea water. 208 R. MARGALEF

I think in special of dinoflagellates and of their toxic secretions, that in their variety can be compared with the variety of essences, volatiles, gums, etc. produced by terrestrial plants. It is a new world of static and quiescent material organizations and their ancillary products that not only dissolve in water, but can pass to the atmosphere, as it is recorded that happens in patches above dinoflagellate and coccolithophore blooms, and that can be compared to the essences produced by terrestrial plants, or that can be operative by ingestion, like the many kinds of poisons produced principally, but not exclusively, by dinoflagellates, substances that in a further step, led to resistance to them or mithridatism. Indeed mussels absorbe poisons, that only later become dangerously effective in humans eating them. Speculation wanders freely and phantasy can go ahead many steps. I spent a considerable fraction of time in my life counting plankton samples, although now I feel that the results were barely worth of the effort. In the first place, we used an inadequate fixing fluid with iodide and formaline that destroyed coccoliths badly. They became under- represented in our lists, as the recent and careful study by Lluisa Cros (2001) shows (her Ph D thesis, recently sustained). Coccolithophores seem to be involved in the job of using excess reducing power to produce several compounds, suspected at least to go to the atmosphere and perhaps exploited as to signal to marine birds the probability of finding some source of fish meat. Fish could eat plankton, so the trick would tend to reduce the number of local enemies. It might appear a bit convoluted to be true, but so has been said. I would suspect that the oceans provide convincing scenarios for the evolution of comparable mechanisms. As stated before, dinoflagellates –as well as organisms of other taxonomic groups–, towards the end of their blooms (red tides), when available phosphorus becomes scarce in water, produce a large variety of toxic molecules consisting of hydrocarbon chains, as it could be anticipated, without phosphorus, apt to kill and initiate the decomposition of varied organisms of different taxonomic groups, thus recycling and making available again elements that were disappearing from the liquid environment, probably phosphorus in the first place of importance. Such events contribute, among others, to increase diversification in oceanic life. The basics concern the importance of the role played in survival and evolution by the reducing power gained by pigment bearing cyanobacteria, how effectively it is applied to inorganic –and organ-

ic– compounds present at sea, and how such effectivity is reflected, and eventually could be estimated, first through the spectra of fluorescence emitted by pigment bearing microorganisms, and later and more obviously by their survival. An important fraction of the excedent reducing power is probably invested in the reduction of nitrate to nitrite in the environment (Blasco, 1971). Although the layers enriched in nitrite in many places and seasons have been explained and interpreted in different ways, they have been accepted as common without much discussion, although they were seen often as intermediate stages in a process of fast recycling, “sparing energy” for the legion of organisms that are to take nitrogen compounds again. Now, after recognition of the ubiquity of small cells and their reducing power, as well as the coincidence of the very abundant populations of them with the levels of maximum nitrite, the immediate suggestion points to the importance of the role of such tiny cells in using the energy of light in form of reducing power, its application to nitrate and their contribution to the creation of the layers of maximum nitrite concentration, thus made dependent also on the efficiency of such diminutive organisms. Such layers cannot be only a result of the activity of the larger components of phytoplankton, although their contribution has to be considered as well, although never in exclusive terms. The reduction of nitrate to nitrite would happen at twilight, assuming that algae could outcompete further limits to the biological productivity of the oceans in the present times. A decreasing biological productivity may be one reason why now the depths are not as anoxic as could be suspected or expected. Anyway, it seems to me that the whole pack of heterogeneous layers placed around the level of light extinction, and including at least part of the layers rich in “immortal” chlorophyll bearing tiny things –again remember that their smallness warrants their practical quality of unsinkables–, should play a considerable role in the regulation of the regime of the whole oceans. Falkowsky could agree. This is in coincidence also with views expressed by Vollenweider in relation with problems concerning lake eutrophication. The different contributions (both, from prokaryotes and from true planktonic algae) help to generate more or less complex layers, approximately extended horizontally. One important role for them is that they operate presumably as unidirectional valves, that might be effective, providing in some sense and in one way a relative isolation of the deep-

er oceanic waters from the water layers closer to the surface, more illuminated and where the exchanges with the atmosphere are easy. Obviously, differences in the behaviour of organisms of the different groups (diatoms and different flagellates; Lomas and Glibert, 2000) should be expected, and not only between prokaryota and eucaryota. Further interest in the problem could only reveal that the layer relatively rich in nitrite is generally not much thick, but it is present almost everywhere or in many different marine areas, and, as should be expected, shows particularly well in places where stratification of water has persisted recently for a while. The areas in which such layers are less thick or disappear altogether coincide, as expected, with places subjected to vertical mixing by reasons that have to do with water mechanics. It could be suspected that around such kinds of distributions relevant phenomena exist, and perhaps now unsuspected mechanisms are added as special situations arise. Laboratory experiments by Dolors Blasco complemented the observations on layers relatively enriched in nitrite at sea. The environmental reduction of nitrate to nitrite, using mixed cultures under different conditions was studied by her (Blasco, 1971). Shifts in the chemical environmental through action of the organisms was evident, in part demonstrated by the apparent capacity of phytoplankton populations to take nitrate and excrete nitrite. There is a rather long history of research and speculation concerning this subject. Discussion especially centered around the possibility of some shortcut in the cycle of nitrogen, but now I do not want to go again in the subject, except in one aspect that might be relevant to my present interpretations and hypothesis. The background scenario offered by the oceans differs from the one presented by the surface of continents, in what concerns the final use of the reducing power of the light, as made available through the machinery of photosynthesis, that essentially is the same everywhere. Reducing power seems to have seen applied perhaps much less at sea, or at least in a different way, perhaps less important, or this may be only apparent, as there does not exist the marine equivalent of wood and “true” forests, only a shore of reducing power. Or perhaps other competing mechanisms have been effective in evolution: In fact, rigid, strong, but passive material is not, could not be, perhaps for mechanical or other physical reasons, as successful in generating organisms mechanically successful in the open sea as it has been on THE TOP LAYERS OF WATER BODIES 209

land, except perhaps only on a relatively minor scale, as in few coastal algae, kelp and the floating communities of kelp and sargasso weeds –the mechanical problems are different, as in the sea large plants need to remain mechanically flexible. It seems that the forest and the plankton, as model ecosystems, have been forced along quite diverging paths in their separate evolution in diverging environments (Bates, 1960). Although the scenarios on land and at sea might appear different, they are substantially comparable (Margalef, 1997). In the sea evolution has barely found uses for wood and cork, or for their analogues or equivalents, in the sense to create large complex molecules without phosphorus, but apt to add to the survival value of the organisms, as are mucilages, terpenes and essences in general. We do not know, for the time being, there might exist at sea some other equivalent ways to contribute to the organization and conservation of most ancient or primitive kinds of ecosystems Recognition of the ubiquity of such kind of relations leads to wonder about the different ways in which the reducing power obtained from light in the photosynthetic system has been incorporated and put to work by life and evolution, both at sea as in the terrestrial ecosystem, in which it has been made historically more apparent to our species, at least in the role played by wood, rubber and many varied volatile hydrocarbons. Cycles of nutrients are responsible for local segregations as well as for historical changes expressed as repeated ecological successions. I am grateful to destiny for having introduced me to the study of marine life in the Rias of Galicia, in NW Spain. I was much impressed by regular events of mixing of the water in the interior of the rias, that are relatively narrow inlets, penetrating deeply on land, which water is renovated by mixing with the outside ocean, in a more or less irregular and, at least, discontinuous way. Massive water exchanges reinitialize from time to time the development of populations that ordinarily start with the dominance of diatoms. Succession may end after a few weeks, a time that can be extended up to a couple of months, ending in red tides. To start again the process, always replaying the particular path converging also towards red tides again. Old local fishermen used to compare red tides to menstruation, as seen as a way for the sea of cleansing itself periodically, at least inside the rias. Anyway, the events are terminated in a more or less relatively discon210 R. MARGALEF

tinuous or sudden way by acceleration of the exchange of water between the rias and the Atlantic, an event, relatively rapid, that is always followed by a sharp change in the plankton quality, normally restarted with a dominance of diatoms. I tried, although without total success by reason of technical limitations, to reproduce on rafts at sea such successional sequences. I was later more successful in the laboratory, continuing to experiment with cultures in enriched water, held circulating along plastic flexible and transparent tubes. After some trials, insistence was rewarded by more success in reproducing plankton successions and, with some surprise, I found as a general and repeatable event a shift in the composition of photosynthetic pigments, that I tried to characterize and express by the ratio between the absorptions of acetonic extracts at the respective wavelengths of 430 and 665 µm (Margalef, 1958). Although perhaps it is not essential to my present discourse, I would like to stress the pertinence of the concept of ecological succession and its analysis, in the frame of how one compound or mixed population follows another, in a way in which spatial heterogeneity is essentially generated by, or become associated with, such kind of successional changes, as expressed in the more or less advanced stages in patches of water that are representative of stages in a process of ecological succession. Populations never remain constant in their composition, but continuously shift as the result of differences in growth speed among the different species present and those that might become available in the course of time, or grow in relation with more fundamental (being the cause of change) shifts in the properties of the surrounding volumes of water. In this way, local differences are generated, and their relationship as well as their influence on the populations becomes traceably identified. Repeated ecological succession provides the scenario where persistent trends in selection can be expressed as one common scenario in which evolution becomes more a collective event than a bunch of haphazard adventures. Out of the laboratory experiments, in the open seas, extensive and wider ranging gradients are observed, as they develop and appear or vanish under more or less strong mixing and expressing local trends. These may differ up to the point to generate relatively sharp discontinuities, that manifest themselves over larger volumes and become specially interesting when boundaries attract more attention for being more manifest.

One could expect that vertical patterns (stratification) should be quite general, or at least provide for more expectable or more regular explanations, than differences expressed between points at the same level, in the form of horizontal patchiness. After all, vertical distributions have a number of determining and controlling factors of common and well known operation, as distribution of light, mechanical energy, nutrients, etc. Besides considerations and experiments on the possible generation of gradients in the distributions of organisms, it soon became obvious that the phytoplankton reacts in its composition to the more or less complex structure and properties of the environment. After what has been written it is natural to consider the quality and distribution of phytoplankton in relation with the concentration of reduced nitrogen compounds (nitrite) in local patches or even amplified as large end even continuous layers, which in the Mediterranean are extended normally between 30 and 50 meters (occasionally going down to 70 m) around twilight depths (Margalef et al., 1966; Margalef, 1995). Locally and notoriously, the levels of maximal fluorescence of phytoplankton; that is, of maximal return of radiation not used by photosynthesis, are found between 40 and 80 m depth and tend to coincide with levels where a recent reduction of nitrate to nitrite was probably intense, resulting in relatively high concentrations of nitrite (50-380 ngat/L) in the water at such levels. There are not walls in the sea, and the patterns related to succession, or to stratification or either to shear of water masses, have open boundaries and have to be related to incompleted processes of mixing operating between centers of different chemical activity. Now we begin to have more data –although never enough– concerning the same NW Mediterranean areas, and even experimental approaches, that make us more familiar with the life and distribution of beings much more tiny than coccolithophores, pigmented bacteria and cyanobacteria less or much less than 2 µm across, and it seems obvious, or at least I am ready to accept, that such organisms in tremendous numbers (1000-200000 cels. per mL) and apt to persist, alive and relatively non active, for long periods of time, could be sensibly effective biochemically. What enthuses me is the virtual immortality of such tiny “beasts”, their null or relatively low speed of sedimentation, and their availability everywhere, keeping their capacity to apply their

undeniable reducing power when appropriate conditions presents themselves. This should happen over all the world ocean and, to me, Western Mediterranean could provide an excellent space for consideration. Recent work (Gasol and del Giorgio, 2000, and references there; Denis et al., 2000) provides numbers concerning our NW Mediterranean corner. More information from elsewhere is coming aplenty (see, for instance, papers from French authors concerning the tropical Pacific in J. Geophys. Res., 104: 3223-3422, 1999). An important question that could be asked concerns the true state and activity of every cell (Hagström, 1999). I could add some information concerning the primary production of the NW Mediterranean area that, in general, for the average Mediterranean, is really high. Although the matter relates only indirectly to the present subject in this presentation, I would like to add that my views never were consistent with the frequently expressed hypotheses that “our” area of the formation during the cold season of surface water which density had been increased by strong evaporation under the effect of Western winds and then moved vertically downwards. In fact it is a rather windy region, and strong wind blows often from West to East, more or less in line with the axis of the Pyrenees, and happens to be particularly strong in winter. Such eastward atmospheric transportation along the Pyrenees, can overturn the system only feebly, but is effective in synchronizing somehow what happens in the Biscay Bay and the Northwestern Mediterranean. I mean that the years in which atmospheric circulation is more intense, Atlantic superficial and relatively warm water accumulates in the surface of the Bay of Biscay and the continuation of the same pattern of atmospheric circulation results in a more strong upwelling in the Gulf of Lion. Such pluriannual fluctuations in open waters were observed and recorded by Le Danois (1925, 1943), and confirmed by the associated shifts along the respective shores in the distribution of coastal life, both in French Brittany (approximately in the direction of meridians) and Spanish Galicia refereed to such fluctuations as “marine transgressions” a way of speaking that I find more appropriate than referring to them in the ponderous expression of “El Niño and La Niña”– like phenomena”. The times at which the atmospheric transport from West to East, along the Pyrenees, is more important, allow for surface water of relatively higher temperature to accumulate in the Gulf of THE TOP LAYERS OF WATER BODIES 211

Biscay and at such times warm water fishes, like dolphin (Coryphaena) are found there. In the same years upwelling is more intense in the Gulf of Lion, along the Catalan-French coast, and deep water organisms like the Mediterranean krill Meganyctiphanes, large colonies of Pyrosoma, and small bathypelagic fishes approach surface along the Western coast of the Gulf of Lion, as South as to the latitude of 42°N. In NW Mediterranean the offshore current goes NE and its position and intensity shifts, as mentioned, in a way that the seasons in which it is particularly strong approaches the coast, at the latitude of Palamós (42°N), encroaching in the space in other times occupied by the coastal current. The dominant northeastbound directed current has been well recognized by Ovchinnikov (1966) and LePrieur (1979, 1981) and the last author adds interesting information about the life that it carries along. In the space in which the current hits the Ligurian coast, where water should ascend, Italian observers have signaled repeatedly the presence of small bathypelagic fishes, being stranded on the beaches with dilated and extruded bladders, as should be expected in specimens forced or pushed up by ascending water. This could serve as an abridged description of the scenario of the NW Mediterranean, an area relatively productive (above 70 and even close to 100 g of assimilated C per m2 and year), with the fluctuations to be expected in such situations. I suppose that the minute cyanobacteria in our plankton do not contribute much to the total primary production of our seas. This is one aspect in the subject of general factors of productivity in the NW of Mediterranean that should help to draw the appropriate scenario in which to place recent research on the tiny cells of cyanobacteria in the area, as part of the general interest aroused by their recognition, mass evaluation and significance. Recently The Institut océanographique, Monaco (Charpy and Larkum, 1999) has produced a special publication about the subject, and more papers have been published and are appearing concerning the Western Mediterranean. Experimental work with Chlorella cultures by Maldonado et al. (1974) has shown how nitrate reductase of this green unicellular alga can operate alternatively also as a reducing agent, that is as a regulator. Thus, it could be expected that the reducing environment, expressed by the reduction of nitrate to nitrite just indicates that photosyn212 R. MARGALEF

thetic activity is particularly effective, in conditions where no phosphate is available for synthesis of genuine living material. A “healthy” activity of the “valve” in the pelagic domain could ameliorate the eventual “greenhouse problem”. The effectiveness of the top layers of the oceans as a valve would be related to the ratio, concerning the cycle of nitrogen, f = (new production)/(recycled production). The value of this index falls ordinarily between 0.1 and 0.3; this might be considered as relatively low. Its meaning could be that the increase of extant and eventually dormant populations are limited by other elements, I tend to believe that the principal factor might be the availability of phosphorus. The ubiquity of small green cells is both, an indicator of the general oligotrophic condition of the sea, adscribable ordinarily to lack of phosphorus. (I do not want to enter the discussion about other possible limiting elements. The Mediterranean, by the way, gets lots of iron from the Sahara, but remains in the class of oligotrophic waters.) Anyway, maps that show the distribution of nitrite provide interesting hints about the events past and present going on at sea, in relation with primary productivity. Given such living conditions, the observer is amazed at the vitality and persistence of such small organisms as the chlorophyll bearing protokariota, of their capacity to remain alive in a state of apparently suspended animation, that makes or allows for their immediate availability if any opportunity for restarting active life presents itself. Their smallness assures them indefinite persistence in any level of water and their immediate availability. They provide a damping background for nutrients. Remarkable might be also their prospective symbiotic value in relation with other elements in the planktonic world. All this returns me –full cercle– back to the times in which I found empirically that the pigment index in the form of the ratio between absorption at two wavelengths, actually 430 and 665 µm was a good indicator of the availability of phosphorus and the growth of particular kinds of phytoplankton. Finally, I have had privileged access to the contribution by Codispoti and coworkers that increased my sense of wonder about the net direction and amount and ways of transfer of reducing power between the terrestrial and the oceanic parts of the biosphere along the history of the Earth and left me wondering how it could imprint evolution of life in our planet.

REFERENCES Including papers relevant in relation with the subject Bates, M. – 1960. The forest and the sea. Time Inc., New York. Blasco, D. – 1971. Acumulación de nitritos en determinados niveles marinos por acción del fitoplancton. Tesis doctoral, Universidad de Barcelona. Broecker, W.S. and T.-H. Peng. – 1984. Gas exchange measurements in natural systems. In: W. Brutsaert and G.H. Jirka (eds.), Gas Transfer at Water Surfaces, pp. 479-493. D. Reidel Publ., Co., Dordrecht, etc. Charpy, L. and A.W.D. Larkum (eds.) – 1999. Marine Cyanobacteria. Bull. Inst. Océanogr. Monaco, Nº special 19: 1-196. Codispoti, L.A., J.A. Brandes, J.P. Chistensen, A.H. Devol, S.W.A. Naqvi, H.W. Paerl and T. Yoshinari – 2001. The oceanic fixed nitrogen and nitrous oxide budgets: Moving targets as we enter the antropocene?. Sci. Mar., 65(Suppl. 2): 85-105. Cros, M.L. – 2001. Planktonic coccolithophores of the NW Mediterranean. Ph D Thesis, Universitat de Barcelona, Barcelona. Dandonneau, Y. – 1999. Introducing a series of papers by several French authors (Raimbault; Blain, Tréguer and Rodier; André and coll.; Gonky, Chrétiennot-Dinet et al., Liu, Landry, Vaulot, Campbell, and Claustre, Morel et al.), under the general title of “Biogeochemical conditions in the aequatorial Pacific, 19801994”, J. Geophys. Res., 104: 3223-3422. Doré, J.E. and D.M. Karl – 1966. Nitrite distribution and dynamics at station ALOHA. Deep Sea Res., P. II, 43: 385-402. Erbacher, J., B.T. Huber, R.D. Norris and M. Margey – 2001. Increased thermohaline stratification as a possible cause for an ocean anoxic event in the Cretaceous period. Nature, 409: 325327. Gasol, J.M. and P.A. Del Giorgio – 2000. Using flowcytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci. Mar., 64: 197-224. Hagström, A. – 1999. Marine bacterioplankton: live, dead or dormant? Amer. Soc. Limnol. Oceanogr., Aquatic Science Meeting in Santa Fe. Karner, M.B., E.F. DeLong and D.M. Karl – 2001. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature, 409: 507-510. Keffer, T. – 1985. The ventilation of the Wold’s Oceans: Maps of the potential vorticity field. J. Phys. Oceanogr., 15: 509-523. Kolber, Z.S., C.L. Van Dover, R.A. Niederman and P.G. Falkowski – 2000. Bacterial photosynthesis in surface waters of theopen ocean. Nature, 407: 177-179. Lang, B.M., T. Rujan, W. Martin and R. Croteau – 2000. Isoprenoid biosynthesis: The evolution of two ancient and distinct pathways across genomes. Proc. Nat. Acad. Sci., 97: 13172-13177. LeDanois, E. – 1925. Remarques générales sur les transgressions atlantiques. Cons. Perm. intern. Expl. Mer., Rapp. Proc. verb. Réunions, 35: 5-11. LePrieur, L. – 1979. Structures hydrologiques, chimiques, biologiques, dans les bassin liguro-provençal. Rapp. Comm. Inter. Mer. Médit., 25/26: 75-76.

LePrieur, L. – 1981. Héterogénéité spatio-temporelle dans le bassin liguro-provençal. Rapp. Comm. Inter. Mer Méditerranée, 27: 77. Lomas, M.W. and P.M. Glibert – 2000. Comparisons of nitrate uptake, storage, and reduction in marine diatoms and flagellates. J. Phycol., 36: 909-913. Luyten, J.R., J. Pedlosly and H. Stommel – 1983. The ventilated thermocline. J. Phys. Oceanogr., 13: 292-309. Maldonado, J.M., M.C. Pueyo and A. Chaparro – 1974. Propiedades reductoras de la nitrato reductasa del alga Chlorella. Rev. Real Acad. Ciencias. Madrid, 68(6): 633-642. Margalef, R. – 1958. Temporal succession and spatial heterogeneity in phytoplankton, In: A.A. Buzzati-Traverso (ed.), Perspectives in Marine Biology, pp. 323-349. University of California Press, Berkeley and Los Angeles. Margalef, R. – 1985. Environmental control of the mesoscale distribution of primary producers and its bearing to primary production in the Western Mediterranean. In: M. Moraitou-Apostolopoulos and V. Kiortsis (eds.) Mediterranean Marine Ecosystems, pp. 213-229. Plenum Press. New York and London. Minas, H.J. and F. Blanc – 1970. Production organique primaire au large et près des côtes méditerranéennes françaises (juin-juillet 1965), influence de la zone de divergence. Téthys, 2: 299-316. Morán, X.A.G., I. Taupier-Letage, E. Vázquez-Domínguez et al. – 2001. Physical-biological coupling in the Algerian Basin (SW Mediterranean): Influence of mesoscale in stabilities on the biomass and production of phytoplankton and bacterioplankton. Deep-Sea Res., I, 48: 405-437. Ovchinikov, I.N. – 1966. Circulation in the surface and intermediate layers in the Mediterranean. Okeanologia. Moscú, 6: 48-59. Pedrós-Alió, C., J.-I. Calderón-Paz, J.J. Guixa-Boixareu, M. Estrada and J.M. Gasol – 1999. Bacterioplankton and phytoplankton biomass and production during summer stratification in the northwestern Mediterranean Sea. Deep-Sea Res., 1, 46: 9851019. Platt, T. and W.K.W. Li, (eds.) – 1986. Photosynthetic Picoplankton. Can. Bull. Fish Aqua. Sci., 214: 1-583. Sournia, A. – 1973. La production primaire planctonique en Méditerranée. Essai de mise à jour. Bull. Et. Comm. Médit., nº sp. 5: 1-128. Stefels, J. – 2000. Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J. Sea Research, 43: 183-197. Vollenweider, R.A. – 1968. Scientific fundamentals of the eutroophication of lakesand flowing waters, with particular reference to nitrogen and phosphorus as factors of eutrophication. Organization for Economic cooperation and Development. Paris, DAS/CSI/68, 27, 159 pp. Vollenweider, R.A. – 1969. Möglichkeiten und Grenzen elementare Modelle der Stoffbilanz von Seen. Archiv. Hydrobiol., 66: 1-36. Weissert, H., J. McKenzie and P. Hochuli – 1978. Cyclic anoxic events in the early Cretaceous Tethys Ocean. Geology, 147151. Whitton, B.A. and M. Potts – 2000. The Ecology of Cyanobacteria. Their diversity in Time and Space. Kluiver Academic Publishers.

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SCI. MAR., 65 (Suppl. 2): 215-229

SCIENTIA MARINA

2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

Following up on a Margalevian concept: Interactions and exchanges among adjacent parcels of coastal landscapes* I. VALIELA1, J.L. BOWEN1, M.L. COLE1, K.D. KROEGER1, D. LAWRENCE1,2, W.J. PABICH3,4, G. TOMASKY1 and S. MAZZILLI1 1

Boston University Marine Program, Marine Biological Laboratory, Woods Hole MA 02543, USA. 2 Present address: LUMCON, 8124 Hwy 56, Chauvin LA 70344, USA. Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge MA 02138, USA. 4 Present address: Environmental Defense, 6 North Market Building, Faneuil Hall Marketplace, Boston MA 02109, USA. 3

This essay is dedicated to Maria Mir, colleague, companion, sounding board, and artist, who has provided lifelong inestimable support for Ramón Margalef’s contribution to environmental science.

SUMMARY: Some decades ago Margalef speculated that study of the exchanges across boundaries that separate different types of ecological systems would provide significant insights about properties and processes within the units that make up ecological mosaics. Although such boundaries might be difficult to define, it seemed likely that such exchanges among units would influence the function and structure of the adjoined systems. In this paper we explore exchanges across such ecological boundaries in coastal ecosystems in Cape Cod, Massachusetts, and elsewhere. We find that, indeed, definition of such boundaries is ambiguous, but study of the exchanges is more useful. In the Cape Cod system, water transport down-gradient is the dominant mechanism exerting influence on down-gradient systems. The direction of ecological control across such boundaries is largely asymmetrical, and properties of up-gradient units exert significant influence on down-gradient units. General properties of donor and receptor parcels are hard to discern, but clearly, parcels making up an ecological mosaic are not independent units, but are coupled by transfers from upgradient tesserae. Studies of controls of ecological systems need to include inter-unit influences as well as internal mechanisms. Key words: Boundaries, ecological mosaics, coastal ecosystems, coastal watersheds, vadose zone, groundwater, estuaries, salt marsh, seagrass meadows, DIN, DON, DOC.

INTRODUCTION Ramón Margalef has been a source of challenging new ideas, grand syntheses, and of new ways to relate ecology, evolution, and other disciplines for our community of researchers and students for more than half a century. Ramón has been –perhaps not a model, for Margalef surely cannot be copied– but *Received August 2, 2001. Accepted August 16, 2001.

rather an example of learning and of daring to think in extraordinarily innovative ways. To have a conversation with Ramón is be involved in an exciting exploration, taking headlong leaps across boundaries, to mull relationships unseen by most of us, to get a feeling for the meaning of genius. And, to see all this done effortlessly, with great generosity of spirit, and utter lack of pretension: there is no more unassuming member of our community than Ramón Margalef, in spite of his accomplishments. INTERACTIONS AMONG ECOLOGICAL TESSERAE 215

Part of the genius of Ramón Margalef is that his thinking and work move effortlessly through, and profit from, what the rest of us may perceive as limiting boundaries. Ramón crosses disciplines to see new relationships, and has also not been shy about crossing ecological boundaries, working in and comparing terrestrial systems, reservoirs, ponds, lakes, rivers, estuaries, upwellings, the deep sea, or the biosphere and other planets. Non-scientific bounds are crossed as well: Margalef easily crosses linguistic barriers. He writes accessibly in Catalán, Castilian, German, French, English; his latest book (Margalef, 2000) –no doubt not his last– is written in three different languages, to reach wider audiences. Margalef’s oeuvre has enormous breadth, and has in many ways pushed ecology in new directions and across different boundaries. In this paper we take the opportunity to dwell on just one of the many topics in which Margalef has forced new insights: the matter of boundaries among units –which we can call ecological tesserae– within environmental mosaics. Many authors have examined boundaries between adjoining ecological tesserae. For example, most texts in ecology discuss ecotones (Shelford, 1963), and in general, refer to the transition of species composition across ecotones, and of a presumed increment of species richness at such boundaries. This richness is due, most likely, to a partial overlap in species lists at regions between adjoining parcels containing different taxonomic assemblages. The adjoining units can be successional stages or distinct habitat parcels. Thus most ecologists have thought of boundaries merely as places where species lists show some change. Early on, Margalef went beyond this notion, suggesting that a more incisive look at these bounds would show much ecological activity. Understanding the dynamics at such boundaries could tell us about the relative organization of the adjoining parcels of environment and could reveal major controls exerted on one parcel by adjoining ones. Similar considerations appear in more recent writings by other researchers (Risser, 1990). The issue of dynamics of boundaries is briefly mentioned in an early paper by Margalef (1962): “…son frecuentes sistemas en que se hallan en contacto subsistemas con diverso grado de organización…el acoplamiento de elementos de estos sistemas tiene interés, porque…(h)ay un flujo…entre los...sistemas…el sistema con más (organización)…encauza las actividades del otro.” The concept of functionally-important boundaries is 216 I. VALIELA et al.

developed somewhat more in the brief but magisterial book, “Perspectives in Ecological Theory” (Margalef, 1967). There Margalef points out that we most often define communities or ecosystems based on descriptions of typical locations in the field, but that the boundaries or ecotones that presumedly separate these typical tesserae are frequently hard to define in the field. Rather than focus effort on mere definition of systems and demarcation of boundaries, Margalef suggests that it might be more fruitful to consider the likely exchanges or interplay among the adjoining systems, and points out that Shelford’s choice of the term “ecotone” insightfully includes an etymological sense (from the Greek τονοσ) that there is a “tension” among the adjoining ecological parcels. Because of the “tension” between such adjoining parcels, Margalef concludes, the tesserae are best studied in the context of the adjoining systems. This dynamic sense of boundaries among systems is further developed in Chapter 26, “Fronteras o interfases asimétricas” in Margalef’s text “Ecología” (Margalef, 1974). There, ecological boundaries are examined, and an argument is made that there are active processes through these boundaries, that the effects of these processes are of sufficient magnitude to actually control structure of the adjoining systems, and that the direction of the controls is most often asymmetric. In addition, the chapter discusses exchanges of dissolved and particulate matter, and of consumers across boundaries in coastal bentho-pelagic coupling, rivers, and terrestrial ecosystems. The chapter develops theoretical ideas that argue that differences in structure and organization, as well as in maturity and level of exploitation, have key roles in determining the consequences of interactions across boundaries separating different tesserae of ecological mosaics. In this paper we use some examples to explore the Margalevian view of boundaries. We consider the difficulty of definition, examine field evidence of active processes, assess the direction of ecological influences, and whether the implied interactions among adjoining units may result in some degree of control on adjoining systems. We dare not follow Margalef into the more theoretical aspects, as we have some difficulty making concepts such as “ecological maturity” empirically operational and hence testable. Perhaps with Ramón’s help we might make progress there, but as Margalef (1974) himself says, those may be “tareas del mañana”. Below we show examples of cross-boundary exchanges of water and dissolved substances, partic-

FIG. 1. – Sketch of the coupled land/estuarine tesserae found in the Waquoit Bay estuarine system. Land covers include residential, agricultural, and natural vegetation. Salt marshes are interposed between land and the receiving estuary. In this glacial terrain, precipitation percolates through soils and the unsaturated vadose zone (tan color), to reach the water table and the aquifer (light green), where it then moves as fresh groundwater (white arrows) toward the estuary, floating over the saline water (darker green) that fills pore spaces under the estuary, and flows into the estuary at the seepage face. Estuarine salinity is identified by intensity of blue color. In the estuary, there are phytoplankton, macroalgae, and seagrasses that contribute to primary production. The estuary exchanges water with the deeper Vineyard Sound, which contributes saltier water to mix with fresh groundwater derived from precipitation and groundwater flow.

ulate materials, and faunal elements, and of controls exerted in the coupled ecological units by these exchanges. We use mainly –but not exclusively– examples from coastal watersheds and estuaries.

BOUNDARIES IN A COASTAL SYSTEM Most of the examples of boundaries, adjacent ecological units, and interactions among these units that we will discuss come from coastal watershed/estuarine systems in Cape Cod, Massachussetts, USA (Fig. 1). In these systems the watersheds contributing freshwater and solutes to the estuaries are covered by parcels of residential land use, agriculture, and forests. Because the glacialderived terrain is unconsolidated sands and gravel, precipitation percolates into soils, crosses the unsaturated vadose zone, and moves down-gradient through the aquifer toward the receiving estuarine waters. Near the seepage face, where fresh groundwater discharges, there is often a fringe of salt marsh. This strip of coastal wetland (replaced in the tropics by mangrove swamps) is characteristically interposed between land and sea. Within the estuary part of the system there are three major types of producers: phytoplankton,

macroalgae, and seagrasses (Fig. 1). The water within the estuary system is fresher near land, and becomes mixed by tidal exchanges and estuarine circulation via tidal outlets connecting to deeper marine waters (Fig. 1). Some ecological boundaries in Fig. 1 are clearly demarcated. For example, the boundary represented by the watershed surface is clearly definable. The relevance of this boundary to the rest of our studies is that throughputs to down-gradient components of the coupled land/water system are significantly affected by the land use mosaic on the watershed surface. Other boundaries in Fig. 1 are less easily defined. Under the watershed surface there is an unsaturated vadose zone. We could consider this zone as a boundary itself or a separate ecological unit, depending on the spatial scales we might prefer. Where the sediment pore spaces become saturated by freshwater there is another apparently evident boundary, the water table. It turns out, however, as we discuss below, that the bound might not really be only the water table itself, but might also include the upper layers of groundwater within the aquifer. The fringe of salt marsh interposed between land and the estuary could also be thought of as a separate ecological tessera or as a boundary (Fig. 1). INTERACTIONS AMONG ECOLOGICAL TESSERAE 217

EXCHANGES AND INTERACTIONS ACROSS BOUNDARIES Water is by far the major motive force underlying exchanges across the various boundaries and tesserae defined in Fig. 1. Water transports solutes, particles, and organisms. To a much lesser extent, motile organisms may add to the exchanges, and gaseous and aerosol transport may also take place. Transport by water Rates of nutrient transport through the watershed surface depend on the mosaic of land use. Interception of nutrients within each type of land use tessera differs (Johnes, 1996; Valiela et al., 1997), so that nitrogen loads from the entire watershed mosaic depend on the relative areas of different land uses within the watershed. We have been primarily concerned with nitrogen because it is the critical ele218 I. VALIELA et al.

200

To the watershed Total

160

120

Nitrogen inputs (10 3 kg N y-1)

Moreover, because of the excursion of tidal water in and out of the intertidal wetlands, and the fractal sinuosity of wetland vegetation zones, the notion of a boundary becomes unclear for coastal wetlands. Do we take the edge of vegetated marsh as the boundary, or do we consider the entire horizontal extent of wetlands as the bound? In addition, there are distinctive vegetation zones within the vegetation of salt marshes, each with their own ecotones, as well as marked spatial patchiness (Valiela et al., 1985) so that definition of boundaries is a challenging task. The tidal outlets that connect the estuary to deeper waters make up another possible boundary (Fig. 1). With tidally-driven mixing, again there is an issue of scale of definition of the boundary. For example, we might think of the entire range over which salinity changes from fresh to seawater across the estuary as the bound (Fig. 1). Alternatively, we might more narrowly choose to conceive of the outlets to deeper water as the bound. All these definitions will be to an extent arbitrary, and subject to effects of scale, as long ago noted by Slobodkin (1964). As Margalef (1974) concludes, the concept of boundaries, though at first might appear as a clear idea, is less evident in actual field situations. It therefore seems more useful and practical to be less concerned with defining bounds or ecotones, and instead focus on the exchanges among adjoining tesserae, without strictly defining the nature of the bounds.

Atmospheric 80 Wastewater

40

Fertilizer

24

To the estuary

Total

20 16

12

Wastewater

8

Atmospheric

4

Fertilizer

1940 1950 1960 1970 1980 1990

Year FIG. 2. – Estimates of land-derived nitrogen loads to the Waquoit Bay watershed surface (top panel), and to the estuary (bottom panel). Loads from wastewater (red), atmospheric (blue), and fertilizer (green) sources were estimated based on changes in land use from 1938 to present. Total loads shown in black. From Bowen and Valiela (2001a).

ment that limits primary production, and hence eutrophication of coastal waters (Nixon, 1995). We find that in the watersheds we have studied –where there is still a considerable area of natural vegetation– atmospheric deposition provides more than half the load to the watershed surface (Table 1). Because of the differential loss rates suffered by the nitrogen from atmospheric, fertilizer, and wastewater sources, wastewater becomes the dominant source of N to the receiving estuary systems. Passage through these boundaries and ecological units therefore substantially changes the relative magnitude of the different sources of nitrogen entering the receiving systems. We applied calculations and models (Valiela et al., 1997; Bowen and Valiela, 2001a,b) to extrapolate nitrogen loading estimates back through recent decades (Fig. 2). The loads to the watershed of Waquoit Bay have increased since mid-20th century, largely because of increases in wastewater nitrogen, even though the major input has remained that of

TABLE 1. – Nitrogen loading from atmosphere, fertilizers, and wastewater to the surface of the watershed of Waquoit Bay, losses during passage through the watershed/aquifer systems, and partition of the N loads received by the estuarine systems. From Valiela et al. (1997). % of N load to watershed

% of N input lost within the watershed/aquifer systems

% of N load to the lagoon/estuary system

Atmospheric deposition Fertilizer use Wastewater disposal

56 16 28

90 67 78

30 17 53

Total

100

81

100

atmospheric deposition (Fig. 2 top). Loads to receiving waters (Fig. 2 bottom) have also increased across the decades, but have been considerably lower than to the watershed, evidence of significant within-watershed retention. Wastewater nitrogen has increased sufficiently to become the major N source to the estuaries. We can further document the predominant role of wastewater nitrogen delivery by use of stable isotopic signatures (McClelland et al., 1997; McClelland and Valiela, 1998). Nitrate derived from wastewater tends to show heavier (15N signatures; the greater the proportion of wastewater in that total land-derived nitrogen load from a watershed, the heavier the signature in the fresh groundwater leaving the aquifer and entering a receiving estuary; this heavier signature can be traced throughout the estuarine food web (McClelland et al., 1997). The losses of ecologically important nutrients incurred during transport through watershed, vadose zone, and aquifer are not constants, but depend on features of the ecological units and boundaries traversed. For instance, throughput of dissolved organic carbon (Pabich et al., in press), of nitrate (Pabich et al., submitted), of ammonium and of dissolved organic nitrogen (Kroeger et al., in prep.) to the groundwater below depends on depth of the vadose zone and on the distance traversed within the aquifer. The pattern in general is that lower concentrations of nutrients are found near the water table under thicker unsaturated vadose zones, and that concentrations of nutrients are dramatically attenuated by passage through aquifers. Differences in nutrient throughput created by differences in vadose zone thickness have consequences for adjoining down-gradient ecological units. One example of these inter-unit couplings is provided by a consideration of vertical nutrient profiles within the groundwater below the vadose zone (Fig. 3). Where depths of vadose zones above were shallow (Fig. 3 top), there were high concentrations

of DOC near the water table. The high concentrations decreased sharply with depth in the aquifer: there was more than an order of magnitude lowering of concentrations by 1 m in depth. In contrast, where the vadose zone was thick (Fig. 3 bottom), DOC

DOC conc. (mg l-1) 0.01 0.01

0.1

V

T

1

10

100

= 0-1.25 m

0.1

1

Depth below water table (m)

Source of nitrogen

10 DOC conc. = 2.13Dwt -0.75 F = 224.6***, R 2= 0.82 100 0.01 0.01

0.1

V

T

1

10

100

>5m

0.1

1

10

F , R 2 n.s.

100 FIG. 3. – Vertical profiles of concentrations of dissolved organic carbon in groundwater beneath the Waquoit Bay watershed surface. Top panel for sites where depth of the vadose zone (VT) was between 0 to 1.25 m, bottom panel for sites where VT was greater than 5 m. Adapted from Pabich et al. (2001).

INTERACTIONS AMONG ECOLOGICAL TESSERAE 219

240

DON (µM)

180

120

60

0

NH4 (µM)

60

40

20

0

NO3 as % of TDN

100 80 60 40 20 0 0

800

1600

2400

Travel distance in aquifer (m) FIG. 4. – Concentration of dissolved organic nitrogen (top) and ammonium (middle) in groundwater of the aquifer under the Waquoit Bay watershed versus the horizontal distance the water has traveled within the aquifer. Nitrate, expressed as percentage of the total nitrogen concentration, plotted vs. the travel distance in the aquifer (bottom). Data of Kevin Kroeger.

concentrations did not reach high values, and there was no significant loss of DOC with depth. We can also show similar profiles of dissolved organic nitrogen, nitrate, and ammonium (Pabich et al., submitted; Kroeger, in prep.). Results such as shown in Fig. 3 show first, that a relatively thin layer of groundwater just below the watertable can be a boundary (or unit?) where there is intense microbial activity. Second, that the rate of loss of DOC (or of other nutrients) in this thin layer depends on rate of delivery from the vadose zone above (Pabich et al., in press). Third, the nature of the vadose zone matters greatly: thicker vadose zones intercept sufficient DOC (and other compounds) to uncouple rates of microbial activity in 220 I. VALIELA et al.

the upper layers of groundwater from influences from above. Thus, properties of one ecological unit, in this case the depth of the vadose zone, greatly affect the functioning of the adjoining ecological unit just below the water table. Passage of materials from the watershed surface through vadose zones or aquifers may alter not only the amounts but also the composition of the materials transferred from one ecological unit to the next (Fig. 4). For example, considerable quantities of reduced nitrogen compounds (DON and NH4) are transported into aquifers. During passage through the aquifer both adsorption and microbial mineralization of DON (Fig. 4 top) and adsorption and nitrification of NH4 to NO3 (Fig. 4 middle) takes place. Nitrate concentrations are also attenuated during passage through aquifers (Pabich et al., submitted), but nitrate is also generated during transport, making the down-gradient trend less evident. The lowering of concentrations of reduced nitrogen compounds is more marked, and hence the proportion of nitrate in the total load increases as the distance traveled within the aquifer increases (Fig. 4 bottom). The net result of differences in sources and transformations during transport is that the mix of reduced and oxidized N that is eventually exported from the aquifer to receiving estuaries varies depending on features within the donor units upgradient. These differences in composition then could affect quite different ecological elements within receiving estuaries. Heterotrophs might respond to DOC and DON supply, autotrophs to nitrate supply. In spite of losses of nitrogen within soils, vadose zone, and aquifer, some fraction of land-derived nitrogen reaches the seepage face. The magnitude of the fraction depends significantly on the disposition of land use tesserae on the watershed surface, as we concluded from discussion of the historical reconstruction of nitrogen loads (Fig. 2). Thus, human activity on the watershed surface reaches across soil, vadose zone, and aquifer, and significantly alters the variable–nitrogen loading–we think might drive ecological change in the receiving estuaries. The couplings among adjacent ecological units might therefore reach across several such units, as if the units were connected in series. In support of the above assertion we can marshal considerable evidence that urbanization of the watersheds during recent decades (Fig. 2) has increased land-derived nitrogen loads, and has been responsible for a major re-shuffle of producer ecology within the estuary complex in Waquoit Bay. Phytoplankton

(Seagrass production/ total production)100

100

% sp = 145.653 N load -0.550, F=15.5***

80 60 40 20 0 0

500

1000

1500

Chlorophyll (mg m-3)

N load (kg N ha-1y-1) CR 601 QR 350 SLP 14

20

80 60 40 20

% sg loss = 0.693 N load + 14.211, F=14.6**

0 0

200

400

J

F

M

A

M

J

J

A

S

O

N

D

Net production (g C m-2 y-1)

400

y = 13.96x + 60.89**, r = 0.78 300

200

100

0 0

4

600

800

ha-1y-1)

FIG. 6. – Top: Seagrass production as % of total production versus land-derived nitrogen load to the estuary. Bottom: Percentage of area of seagrass habitat lost (over last 10 to 30 years) in several estuaries, plotted versus the corresponding land-derived nitrogen load. From Valiela and Cole (in press).

10

0

2500

100

N load (kg N 30

2000

N load (kg N ha-1y-1)

% seagrass area lost

biomass and production (Fig. 5), have increased in estuaries that receive higher land-derived nitrogen loads (Fig. 5 top), and the increased phytoplankton production is related to the concentration of available nitrogen (Fig. 5 bottom), which in turn is related to the magnitude of the load received from land (Valiela et al., 2000a). Similarly, macroalgal biomass and production have also increased (Valiela et al., 1992; 2000b; Peckol et al., 1994; Stieve et al., submitted). In contrast, seagrass biomass and production, as well as areal extent of seagrass meadows, have decreased sharply (Valiela et al., 1992; 2000b; Short and Burdick, 1996). The high sensitivity of seagrasses to nitrogen loads, in spite of their being light-limited (Dennison and Alberte, 1982), has been discussed (Sand-Jensen and Borum, 1991; Duarte, 1995; Valiela and Cole, in press). Shading by increased phytoplankton and macroalgal biomass that follows increased nitrogen supplies sharply lowers seagrass activity (Hauxwell et al., 2001). In general, seagrasses decline sharply in response to increases in nitrogen loads. Both seagrass production (Fig. 6 top), and seagrass meadow habitat area (Fig. 6 bottom) show a significant decreasing trend as N loads increase, so

8

12

Average annual DIN (µM) in the estuary

FIG. 5. – Chlorophyll concentration in three estuaries of the Waquoit Bay estuarine system across the year (top). Annual phytoplankton production for the three estuaries of the top panel, plotted vs. the annual nitrogen load received from the watersheds (bottom). Adapted from Foreman et al. (submitted).

that beyond 100-200 kg N ha-1 yr-1, these environments disappear. The effects of land-derived nitrogen load on estuarine producers are summarized in Fig. 7, which shows that the relative contribution to total estuarine production carried out by seagrasses sharply decreases as N loads increase (largely due to the changes in the land use mosaic on the watershed surface) and is replaced by phytoplankton and macroalgal production. The effects of water residence times on these relationships is discussed below. In the discussion so far we ignored one other bound inserted between land and sea, the salt marsh fringe (Fig. 1). This may be another boundary that is hard to define as a border, for it does vary greatly in dimension and distribution along coastlines. As a simplification, however, we can consider the relative proportion of salt marsh area in different estuaries to make another point: that because of their position between land and estuary, as well as their high rates of denitrification and burial of nitrogen, salt marshes may provide substantial interception of land-derived nitrogen. If indeed INTERACTIONS AMONG ECOLOGICAL TESSERAE 221

Phytoplankton

80

Seagrass 0

100 % sg pro = 1.117(% wetland) + 2.668 F=33.5***

80 60 40 20 0 0

10

20

30

40

50

60

(Wetland area/total estuary area)100

Tr ≥ 45 d 80

100

% seagrass area lost

(Production/total production)/100

Macroalgae 40

(Seagrass production/total production)100

Tr ≤ 3 d

40

0 0

200

N load (kg

400

ha-1

600

y-1)

80 60 40 20 % sg lost = 118.130 * 10 -0.019(% wetland) F=6.7*

0 0

10

20

30

40

50

60

(Wetland area/total estuary area)100

FIG. 7. – Proportion of primary production by phytoplankton, macroalgae, and seagrasses in estuaries subject to different landderived nitrogen loads. Top panel contains information for estuaries whose water residence times (Tr) are less than 3 d, bottom panel for estuaries with Tr greater than 45 d. From Valiela et al. (2000b).

FIG. 8. – Top: Seagrass production expressed as a % of total production in many estuaries, plotted versus the area of fringing wetland expressed as a % of total estuary area. Bottom: % of area of seagrass habitat lost (over last 10 to 30 years) plotted versus the % of area of the estuary made up by fringing wetland. From Valiela and Cole (in press).

nitrogen loads from land are responsible for loss of eelgrass meadows, interception of land-derived nitrogen in coastal wetlands might be interpreted as a protective “subsidy” furnished by salt marshes (and mangrove swamps) to eelgrass meadows. We compiled published data on seagrass production (Fig. 8 top) and loss of seagrass habitat (Fig. 8 bottom) and wetland areas in the same estuaries (Valiela and Cole, in press). The results of the compilation show that the larger the area of salt marsh or mangrove swamp, the greater the production by seagrasses (Fig. 8 top), and the smaller the loss of seagrass meadows that occurred as nitrogen loads increased (Fig. 8 bottom). Thus, whether we think of the coastal wetland as an active bound, an ecological tessera, or as a “third player” of game theory, as suggested by Margalef (1974), the presence of this coastal unit alters the inputs from the watersheds sufficiently to make a difference to the receiving adjoining seagrass meadows.

The quantitative relationships of land-derived loads, nitrogen interception in coastal wetlands, and susceptibility of seagrass meadows remain to be defined, but it is clear that adjoining parcels of landand waterscapes are not isolated units. Rather, recognizably different ecosystems are coupled by transports from one tessera to the next. In our example, transport of land derived-nitrogen can influence seagrass meadows, but that influence is mediated –within a certain range of values of the transport rate– by the sequestration of nitrogen in coastal wetlands interposed between land and estuary. Where we see productive seagrass meadows (Fig. 9), we may appreciate that the nearby salt marshes might be providing an important subsidy by intercepting land-derived nitrogen. This finding has basic interest in terms of controls of adjoining ecological parcels. There are also applied aspects, in that coastal development increases nitrogen loads from land to estuaries, and management of such loads should consider

222 I. VALIELA et al.

FIG. 9. – Photo of a vigorous seagrass (Zostera marina) meadow in Waquoit Bay located off a salt marsh that intercepts land-derived nutrients. Photo by J. Hauxwell.

the importance of coastal wetlands as a mediator of the effects of land-derived eutrophication. The outer bounds of the watershed/estuary system, the tidal outlets to deeper water, allow active mixing and transport in and out of coastal estuaries (Fig. 1). In the vast majority of cases, nutrient-richer estuarine water is mixed with nutrient-poorer coastal water, hence diluting the concentrations. The rates of this dilution are set in part by the residence time of water within the estuaries. The shorter the residence time, the more effective the dilution. Inherent in this simplified idea is that the shorter the residence time, the greater the export of nitrogen to the deeper water beyond the boundary (Howarth et al., 1996). We could conceive of water residence time as a coupling/decoupling mechanism among adjoining systems. Where water residence times within estuaries is short, the land-derived materials transported through an estuary are shunted effectively through the estuarine complex, and the exported materials exert their influence most strongly on the

ecology of the deeper coastal waters. Where water residence times are long, the transformations and sequestration within the estuarine complex may be more influential, and to some undefined extent may uncouple the link between watersheds and the deeper waters offshore. This topic merits future attempts at quantification. Any student of marine data has perceived that there are strong gradients in solutes and particles from the shore to deeper waters of the sea. From this it is logical to suppose that the major sources of these substances are from land to sea. In fact, coastal estuaries, particularly those with wetlands, have for some decades been considered to supply materials that subsidize the metabolism of deeper coastal waters (Teal, 1962; Odum, 1971). Reviews of published data suggest that the majority of salt marshdominated estuaries export ammonium, dissolved organic nitrogen, particulate organic nitrogen, total nitrogen, dissolved organic carbon, particulate organic carbon, and total carbon (Table 2). In contrast, only a minority of such coastal systems export nitrate to deeper waters. Rather, nitrate may be denitrified within the estuaries and lost as N2. The propensity to export energy rich materials is more widespread in more “mature” marsh estuaries (Table 2). Maturity here refers to the degree to which the passage of time has allowed accumulation of sediments within the system, and hence has led to reduction of open water area, and development of tortuous channels. Mass balance studies in a salt marsh-dominated estuary in Cape Cod showed that, as a whole, the system transformed oxidized nitrogen inputs into more energy-rich reduced nitrogen and exported a portion of the inputs as dissolved and particulate organic nitrogen and as ammonium (Valiela and Teal, 1979). Such exports –another example of the changes in composition mentioned earlier when discussing aquifers– thus furnish energy-laden nitrogen supplies to nitrogen and energy-poorer deeper waters. The quantitative importance of exports to deeper waters was demonstrated by Hopkinson (1985), who measured metabolism of coastal waters off salt marsh estuaries and concluded that organic matter export from the fringing salt marshes is the most reasonable source for the organic matter that supports a significant fraction of the metabolism of the coastal water column. So far we have focused on down-gradient transports among adjoining ecological tessera, that is watershed to aquifer, to streams, to estuary, and to INTERACTIONS AMONG ECOLOGICAL TESSERAE 223

TABLE 2. – Summary of studies of exports and imports of ammonium (NH4), nitrate (NO3), dissolved organic nitrogen (DON), particulate nitrogen (PON), total nitrogen (TN), dissolved organic carbon (DOC), particulate organic carbon (POC), and total carbon (TC) from salt marshes to coastal waters1. This table is from Valiela and Cole (2000). E: export, I: import, O: no net transport. Estuary

NH4

NO3

DON

PON

TN

DOC

POC

TC

E

E

E

E O E

I I I I

I I

E E

E I

E E

E E

E O E E E O E E E E

E E

E

Young marshes Canary Creek, DE Crommet Creek, NH Ems-Dollard Marsh, Netherlands Flax Pond, NY Sapelo Island, GA Stroodorpe Marsh, Netherlands

I I

I O

E O

I O

E

E

E

E

I I Mature marshes

Barataria Bay, LA Bly Creek, SC Branford Marsh, CT Carter Creek, VA Coon Creek, TX Dill Creek, SC Gotts’ Creek, MD Great Sippewissett Marsh, MA Kariega Marsh, S. Africa North Inlet, SC Tijuana Estuary, CA (two marshes) Ware Creek, VA

E I

I I

E

I

E

E E

E E

E E

E E

E E E

E E E

E E I

E

E E E

E

E

E E E

Percent of marshes that export materials “young” marshes: “mature” marshes:

25 86

0 57

100 100

33 83

100 100

75 100

20 75

33 100

All marshes:

64

36

100

67

100

91

59

82

1

Data from many sources, summarized by Nixon (1980), Valiela (1983), and Taylor and Allanson (1995).

deeper coastal waters. There are some mechanisms that propel materials reciprocally, upgradient. One example is that during storms, aerosols and larger droplets of salt water are deposited on nearshore land surfaces. These deposits kill vegetation on land, and also the contained salt displaces ammonium adsorbed from soils nearshore. The ammonium then is free to move towards the receiving estuary. This aerosolbased leaching therefore alters nearshore vegetation as well as makes coastal soils poor in available nitrogen (Valiela et al., 1996; 1998). Mass balance calculations suggest, however, that the nitrogen transport involved in this leaching is orders of magnitude smaller than the other items in coastal nitrogen budgets. Similarly, in general tidal exports are considerably higher than tidal imports into estuaries. Organism exchanges Indirect effects Water motions within estuaries may occur at different rates, and these differences, subsumed for convenience as water residence times (Tr), might have 224 I. VALIELA et al.

important indirect consequences for the organisms within these systems. We compiled published values of Tr for as many estuaries as possible, and found that the average, Tr were surprisingly short (Fig. 10 top). The issue seems relevant even for fast-dividing small organisms such as phytoplankton (Vallino and Hopkinson, 1998). Modal division rates of marine and estuarine phytoplankton (Fig. 10 bottom) are 90% if Brevoortia tyrannus is excluded. b

do produce more eggs, but the resulting young will be released in the deeper waters of Vineyard Sound, after the females that were feeding in the specific estuaries are swept out to sea. Direct effects It is well-known that estuaries are used by many organisms as nurseries where larvae and juvenile life stages of species found in deeper waters as adults find abundant food supplies and refuge. An example of these migrations can be found in the assemblage of fish that are often found in estuaries with associated salt marsh fringes (Werme, 1981) (Table 3). Within the estuary, the size of fish that reside in the estuary does not differ from that of the juvenile invader species whose adults live in deeper waters: there are disadvantages to having a larger size in these estuaries, because larger fish are readily eaten by the many top predators including herons, egrets, and other birds. Invader fish, however, have fuller guts, and are far more carnivorous than resident fish. The invaders manage this by taking advantage of their larger gape: although they have similar lengths, they have access to larger food items than the residents. This difference in gape derives from the simple allometric relationships of juveniles vs. adults vertebrates: young vertebrates have relatively larger heads than adults, and invaders are all juveniles. Hence invaders have larger heads and consequently, larger gape (Table 3). Feeding on larger prey places a bound on abundance of invaders, because, as is well known, larger prey are much less abundant than small prey. Hence, invaders are limited to much lower densities (Table 3). The benefit, and probably the evolutionary forcing towards invading estuaries, is made evident by the relative growth reported in Table 3. Invader species attain a growth rate an order 226 I. VALIELA et al.

of magnitude larger than resident species. Thus, though obligatorily rarer, invaders from another adjoining environment can achieve relatively fast growth rates in salt marsh estuaries. The importance of coastal wetlands as nurseries for coastal populations can also be of economic importance. Shrimp yields in the coast of the Gulf of Mexico, for example are proportional to the area of coastal wetland landward of the harvest area (Fig. 12 top). In recent decades the yield of shrimp from

FIG. 12. – Top: Harvest by the shrimp fishery off Louisiana in relation to the area of adjoining coastal wetland. Bottom: Metric tons of shrimp caught annually off Louisiana in relation the cumulative loss of adjoining coastal wetland. Data compiled by Turner (1992).

those areas has fallen, and the reduction in catch can be related to the cumulative loss of coastal wetlands in the Louisiana area (Fig. 12 bottom). These data speak of a clear relationship between the relative area of coastal wetlands, and the commercial harvest of shrimp from nearby deeper waters. The links between these two spatially separate variables are that juvenile shrimp use adjacent wetlands as nurseries, and that materials exported from wetlands support the coastal food web on which adult shrimp depend. The migration of fish and shrimp out of estuaries is another example of a reciprocal exchange across boundaries of ecological tesserae. Much as in the case of salt aerosol exchanges, the amounts of nutrients transported in and out of estuaries via organism migration is orders of magnitude lower than the hydrographically controlled transports (Valiela and Teal, 1979; Deegan, 1993). Invasions by organisms from one ecological tessera to another are not rare. A terrestrial example can be found in feeding patterns of bird assemblages (Fig. 13). Birds from late succession parcels of land-

scape (forests) tend to feed in parcels of environment of earlier succession (fields), particularly during the breeding season when demand for food is highest. In most estuarine situations (but not all), species from down-gradient move up-gradient to find such richer food supplies. It is as if species from downgradient environments live in a relatively more competitive environment, and send their young to upgradient environments where some adaptation allows exploitation of a less intensively used resource (the epitome of such relationships might be the pole-ward migration of birds during the breeding season). The magnitude of the effects exerted on the estuarine system by the invaders is likely minor because of the rarity of the invaders relative to the abundance of the resident species, at least in the example we used. Coastal environments such as the ones we are describing have been unusually subject to invasion by species from elsewhere (Carlton, 1996), via anthropogenic intervention and by natural processes. Such invasions at times have considerably

FIG. 13. – A measure of the frequency of visitor bird species (P) found in forests (white circles) and in fields (black circles) in each of four intervals of % carnivory. The more carnivorous the bird, the more likely it visits adjoining parcels for feeding. “n” is number of species, “v” is number of visitor species in the assemblages of birds recorded. “n.s.” = runs test not significant, “*” = runs test significant at 0.05 probability. Data compiled from published sources, and published in Valiela (1971).

INTERACTIONS AMONG ECOLOGICAL TESSERAE 227

restructured the composition of local communities. It may be that coastal systems share some as yet unidentified features that make for such susceptibility to invasions; study of possible commonalities within both receiving and donor sites might be of considerable ecological interest.

CONCLUSIONS Ecological boundaries per se are ambiguous and perhaps pragmatically their definition is best ignored. On the other hand, exchanges among adjoining ecological units on either side of the undefined boundaries are not only empirically demonstrable, but also may have potentially major consequences for the structure and organization of the adjoined ecological tesserae. In the examples we reviewed above, the direction of the control by processes across boundaries was invariably asymmetrical, and dominated by water transport. We could document reciprocal effects –as in the instances of aerosol transport, and juvenile organism invasions from deeper- to shallower water tesserae– but these reciprocal mechanisms either were of a considerably lesser magnitude, or likely had minor effects, compared to transport of materials by water down-gradient. There is no doubt that fundamentally important processes exert their influences on adjoining ecological units across their boundaries. Tesserae of ecological mosaics are not isolated units but may be coupled by forces generated by properties of adjoining, or even distant and non-contiguous ecological units, as in the case of watershed land use and producers within estuaries. Most inter-tesseral exchanges are carried out via physical mechanisms such as water flow and wind, with a smaller role for organismal movement. It is difficult to generalize about ecological properties of ecological donor vs receptor tesserae: a parsimonious explanation may be that for the most part, and in most circumstances, physical transport simply forces the exchanges. It should take only a little coaxing to perhaps convince Margalef to provide us with a more imaginative explanation.

ACKNOWLEDGEMENTS The work on which this paper is based was supported by grants from the National Center for Envi228 I. VALIELA et al.

ronmental Assessment, Office of Research and Development, U.S. EPA, the U.S. National Science Foundation LMER and REU grants, and National Estuarine Research Reserve and Cooperative Institute and Estuarine Technology grants from the National Oceanic and Atmospheric Administration. Support was also provided by the Woods Hole Oceanographic Institution Sea Grant Program, the Massachusetts Institute of Technology Sea Grant Program, by Graduate Fellowships to K. Kroeger, G. Tomasky, and D. Lawrence from the National Oceanic and Atmospheric Administration, and by the Palmer/McLeod Fellowship to K. Kroeger. REFERENCES Bowen, J.L. and I. Valiela. – 2001a. The ecological effects of urbanization of coastal watersheds: Historical increases in nitrogen loads and eutrophication of Waquoit Bay estuaries. Can. J. Fish. Aquat. Sci., 58: 1489-1500. Bowen, J.L. and I. Valiela. – 2001b. Historical changes in atmospheric nitrogen deposition to Cape Cod, Massachusetts, USA. Atmos. Environ., 35: 1039-1051. Carlton, J.T. – 1996. Marine bioinvasions: The alteration of marine ecosystems by non-indigenous species. Oceanography, 9: 36-43. Cubbage, A., D. Lawrence, G. Tomasky and I. Valiela. – 1999. Relationship of reproductive output in Acartia tonsa, chlorophyll concentration, and land-derived nitrogen loads in estuaries of Waquoit Bay, Massachusetts. Biol. Bull., 197: 294-295. Deegan, L.A. – 1993. Nutrient and energy transport between estuaries and coastal marine ecosystems by fish migration. Can. J. Fish. Aquat. Sci., 50: 74-79. Dennison, W.C. and R.S. Alberte. – 1982. Photosynthetic responses of Zostera marina L. (eelgrass) to in situ manipulations of light intensity. Oecologia, 55: 137-144. Duarte, C.M. – 1995. Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia, 41: 87-112. Foreman, K., G. Tomasky, L.A. Soucy and I. Valiela. – (Submitted). Responses of phytoplankton production to land-derived nitrogen loads in Waquoit Bay, Massachusetts, USA. Aquatic Ecology. Hauxwell, J., J. Cebrián, C. Furlong and I. Valiela. – 2001. Macroalgal canopies contribute to eelgrass (Zostera marina) decline in temperate estuarine ecosystems. Ecology, 82: 10071022. Hopkinson, C.S., Jr. – 1985. Shallow-water benthic and pelagic metabolism: Evidence of heterotrophy in the nearshore Georgia Bight. Mar. Biol., 87: 19-32. Howarth, R.W., G. Billen, D. Swaney, A. Townsend, N. Jaworski, K. Lajtha, J.A. Downing, R. Elmgren, N. Caraco, T. Jordan, F. Berendse, J. Freney, V. Kudeyarov, P. Murdoch and Z. ZhoaLiang. – 1996. Regional nitrogen budgets and riverine N and P fluxes for the drainages to the North Atlantic Ocean: Natural and human influences. Biogeochemistry, 35: 75-139. Johnes, P.J. – 1996. Evaluation and management of the impact of land use changes on the nitrogen and phosphorus load delivered to surface waters: The export coefficient modeling approach. J. Hydrol., 183: 323-349. Lawrence, D.J. – 2000. Estuarine calanoid copepod abundance in Waquoit Bay, MA: Effects of season, salinity, and land-derived nitrogen loading. M. S. thesis, Boston Univ. Margalef, R. – 1962. Adaptación, ecología y evolución: Nuevas formas de plantear antiguos problemas. Bol. R. Soc. Esp. Hist. Nat. (B), 60: 231-246. Margalef, R. – 1967. Perspectives in ecological theory, The University of Chicago Press, Chicago. Margalef, R. – 1974. Ecologia. Omega, Barcelona. Margalef, R. – 2000. Widening vistas: Toward an ecology tailored to our problems. Fundación Cesar Manrique, Madrid.

McClelland, J.W. and Valiela, I. – 1998. Linking nitrogen in estuarine producers to land-derived sources. Limnol. Oceanogr., 43: 577-585. McClelland, J.W., I. Valiela and R.H. Michener. – 1997. Nitrogenstable isotope signatures in estuarine food webs: A record of increasing urbanization in coastal watersheds. Limnol. Oceanogr., 42: 930-937. Nixon, S.W. – 1980. Between coastal marshes and coastal waters a review of twenty years of speculation and research on the role of salt marshes in estuarine productivity and water chemistry. In: P. Hamilton and K.B. MacDonald (eds.), Estuarine and wetland processes with emphasis on modeling, pp. 437-526. Plenum Press, New York. Nixon, S.W. – 1995. Coastal marine eutrophication: A definition, social causes, and future concerns. Ophelia, 41: 199-219. Odum, E.P. – 1971. Fundamentals of ecology, 3rd edition. W.B. Saunders, Philadelphia. Pabich, W.J., H.F. Hemond and I. Valiela. – (Submitted). Denitrification rates in groundwater, Cape Cod, USA: Control by NO3and DOC concentrations. Geochim. Cosmochim. Acta. Pabich, W.J., I. Valiela and H.F. Hemond. – (In press). Relationship between DOC concentration, vadose zone thickness and depth below water table in groundwater of Cape Cod, U.SA. Biogeochemistry. Pace, M.L., S.E.G. Findlay and D. Lints. – 1992. Zooplankton in advective environments: The Hudson River community and a comparative analysis. Can. J. Fish. Aquat. Sci., 49: 1060-1069. Peckol, P., B. DeMeo-Anderson, J. Anderson, I. Valiela, M. Maldonado and J. Yates. – 1994. Growth nutrient uptake capacities and tissue constituents of the macroalgae Cladophora vagabunda and Gracilaria tikvahiae related to site specific nitrogen loads. Mar. Biol., 121: 175-185. Risser, P.G. – 1990. The ecological importance of land-water ecotones. In: R. J. Naiman and H. Décamps (eds.), The ecology and management of aquatic-terrestrial ecotones, Vol. 4. Man and Biosphere Series, pp. 7-22. Parthenon Publ. Group. Sand-Jensen, K. and J. Borum. – 1991. Interactions among phytoplankton, periphyton, and macrophytes in temperate freshwaters and estuaries. Aquat. Bot., 41: 137-175. Shelford, V.E. – 1963. The ecology of North America. University of Illinois Press,Urbana, Illinois. Short, F.T. and D.M. Burdick - 1996. Quantifying eelgrass habitat loss in relation to housing development and nitrogen loading in Waquoit Bay, Massachusetts. Estuaries, 19: 730-739. Slobodkin, L.B. – 1964. Growth and regulation of animal populations. Holt, Rinehart and Winston, Inc, USA. Stieve, E., I. Valiela, J. Hauxwell and J. McClelland. – (Submitted). Macrophyte abundance in Waquoit Bay, MA: Effects of landderived nitrogen loads, light, and canopy depth. Aquat Bot. Taylor, D.I. and B.R. Allanson. – 1995. Organic carbon fluxes between a high marsh and estuary, and the inapplicability of the Outwelling Hypothesis. Mar. Ecol. Prog. Ser., 120: 263-270. Teal, J.M. – 1962. Energy flow in the salt marsh ecosystem of Georgia. Ecology, 43: 614-624.

Tomasky, G. and I. Valiela. – (Submitted). Residence time mediated response of estuarine phytoplankton to nitrogen loads. Estuarine, Coastal and Shelf Science. Turner, R.E. – 1992. Coastal wetlands and penaeid shrimp habitat. In: R.H. Shroud (ed.), Stemming the tide of coastal fish habitat loss, pp. 97-104. National Coalition for Marine Conservation, Inc., Savannah. Valiela, I. – 1971. Food specificity and community succession: Preliminary ornithological evidence for a general framework. General Systems, 16: 77-84. Valiela, I. – 1983. Nitrogen in salt marsh ecosystems. In: E.J. Carpenter and D.G. Capone (eds.), Nitrogen in the marine environment, pp. 649-678. Academic Press, New York. Valiela, I. and M.L. Cole – (In press). Comparative evidence that salt marshes and mangroves may protect seagrass meadows from land-derived nitrogen loads. Ecosystems. Valiela, I., G. Collins, J. Kremer, K. Lajtha, M. Geist, B. Seely, J. Brawley and C-H. Sham. – 1997. Nitrogen loading from coastal watersheds to receiving estuaries: New method and application. Ecol. Appl., 7: 358-380. Valiela, I., K. Foreman, M. LaMontagne, D. Hersh, J. Costa, P. Peckol, B. DeMeo-Anderson, C. D’Avanzo, M. Babione, C-H. Sham, J. Brawley and K. Lajtha. – 1992. Couplings of watersheds and coastal waters: Sources and consequences of nutrient enrichment in Waquoit Bay, Massachusetts. Estuaries, 15: 443-457. Valiela, I., M. Geist, J. McClelland and G. Tomasky. – 2000a. Nitrogen loading from watersheds to estuaries: Verification of the Waquoit Bay nitrogen loading model. Biogeochemistry, 49: 277-293. Valiela, I., P. Peckol, C. D’Avanzo, J. Kremer, D. Hersh, K. Foreman, K. Lajtha, B. Seely, W.R. Geyer, T. Isaji and R. Crawford. – 1998. Ecological effects of major storms on coastal watersheds and coastal watersheds: Hurricane Bob on Cape Cod. J. Coast. Res., 14: 218-238. Valiela, I., P. Peckol, C. D’Avanzo, K. Lajtha. J.N. Kremer, W.R. Geyer, K. Foreman, D. Hersh, B. Seely, T. Isaji and R. Crawford. – 1996. Hurricane Bob on Cape Cod. Am. Sci., 84: 154-165. Valiela, I. and J.M. Teal. – 1979. The nitrogen budget of a salt marsh ecosystem. Nature, 280: 652-656. Valiela, I., J.M. Teal, S.D. Allen, R. Van Etten, D. Goehringer and S. Volkmann. – 1985. Decomposition in salt marsh ecosystems: The phases and major factors affecting disappearance of aboveground organic matter. J. Exp. Mar. Biol. Ecol., 89: 29-54. Valiela, I., G. Tomasky, J. Hauxwell, M.L. Cole, J. Cebrián and K.D. Kroeger. – 2000b. Operationalizing sustainability: Management and risk assessment of land-derived nitrogen loads to estuaries. Ecol. Appl., 10: 1006-1023. Vallino, J.J. and C.S. Hopkinson Jr. – 1998. Estimation of dispersion and characteristic mixing times in Plum Island Sound Estuary. Estuar. Coast. Shelf Sci., 46: 333-350. Werme, C. – 1981. Resource partitioning in a salt marsh fish community. Ph.D. thesis., Boston Univ.

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SCI. MAR., 65 (Suppl. 2): 231-256

SCIENTIA MARINA

2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

Thermohaline feedback loops and Natural Capital* TOM SAWYER HOPKINS Dept. MEAS, Box 8208, NCSU, Raleigh, North Carolina, 27695, USA.

SUMMARY: Human interference now represents an inextricable component of all major ecosystems. Whether this is through top-down overharvesting of ecosystem production or bottom-up alteration (deliberate or inadvertent) of the abiotic conditions, the planet’s ecosphere is in a vicious degradation cycle. For our economy to shift from exploiting to sustaining the natural systems, the solution, if there is to be one, will involve incorporation of the value of natural capital into the economic and political feedback loop. For the science sector, this will involve developing methodologies to evaluate the nonlinear and behavioral dynamics of entire systems in ways that can be coupled with economic models. One essential characteristic of systems science involves the interactions between internal components and external systems. Thermohaline circulations and their feedback loops illustrate a class of such interactive pathways. Examples from the Arctic, Mediterranean, and the US East Coast along with some of their associated ecological impacts are reviewed. Understanding how thermohaline interactions provide stability to the marine biotic environment and under what conditions this stability could be destabilized is a fundamental step toward evaluating the non-linear response of marine systems to anthropogenic stress. Key words: thermohaline, circulation feedback Loops, natural capital, biocomplexity, Arctic, Mediterranean, Pamlico Sound.

INTRODUCTION In considering the theme of this congress, I have often thought about the evolution of marine science (oceanography) over the last thirty-five years. During these reflections, I marvel at the technical advances now available and sometimes wonder about our progress with substance. It seems that, as a community, we have pursued the science more or less as we wanted. Rightly, we wanted to understand marine systems in their pristine form before we tackled the impact of man on these systems. This is, however, no longer possible, as all major systems are under impact. Inevitably, an emerging role for science is that of assisting society in achieving sustainable use of natural resources. While this state*Received August 3, 2001. Accepted August 16, 2001.

ment might not stir up much controversy among the present audience, the public would certainly question the implied urgency. Furthermore, exactly how science might ultimately realize this goal of assisting sustainability would surely be controversial among any group of scientists. Human society is, out of necessity, reorganizing the vast network of interactions that connects it to the planet’s ecosphere. There are multiple solutions to this reorganization, of which the more humanfriendly are a strong function of our own consciousness. Will science passively document the reorganization as it happens or will it proactively guide society to a favorable solution? The choice seems to me so important that I have chosen to insert a brief rationale for this changing role of science into this essay and to illustrate a specific class of interactions as an example of human influence on marine systems. For THERMOHALINE FEEDBACK LOOPS 231

this I will review how and why thermohaline dynamics maintain environmental stability and provide major interactive pathways between the abiotic and the biotic components of marine systems. Finally, in the last section I will try and coalesce these seemingly disparate topics.

A CHANGING ROLE FOR NATURAL SCIENCES For those of us in touch with scientific literature, there is ample evidence concerning the degradation of natural systems. From available data, it is relatively easy to understand that the global rate of degradation exceeds that of regeneration. Further, understanding that regeneration is itself a function of the degradation, leads one to appreciate the condition of an exponentially declining sustainability. Recognizing that the force behind degradation is due to an unreasonable and uncontrolled economic exploitation, leads one to the conclusion that our market economy and growing population will cause a fatal collapse in the natural support systems on which our society depends. Finally, the logic of this sequence leads to the conclusion that the environment should be an integral part of the economy—not an externality to it. A solution that I find tenable involves extending the role of science to include natural capital assessment. I believe there is evidence that this evolution is already occurring, but in a much too weak and fragmented manner. It needs a discussion within the science community and with the public. This extension will require scientific contribution beyond the so-called applied science of “impact statements” and “status and trends analyses” and into the arena of the simulation of complex, nonlinear, behavioral systems. It will also involve a change in how science interacts with society. Natural Capital Adam Smith based his economic theory on the availability of three ingredients: Labor (manpower), Capital (money) and Land (resources). His thesis was that the profit motive would drive a self-regulating market and increase the overall wealth of the community. Unfortunately, he assumed that the resources were unlimited and therefore gratis. The fact that 200 years ago natural resources did appear to be infinite may excuse Smith’s lapse. Now, how232 T.S. HOPKINS

ever, there is no such excuse, and resources are still omitted from the supply-and-demand feedback loop where price optimizes the interplay only between Labor and Capital. In fact, the primary objective of the modern economy has been to convert natural resources into financial resources, using the argument that the process was reversible under a “substitutability” concept. In the 1970s, Daly (cf. Daly, 1991) proposed that the economy should be re-structured to a ‘Sustainable Economy’ by including an accounting of resources (Natural Capital) which, when incorporated into the supply and demand loop, would optimize the use of resources and minimize their degradation and depletion (Fig. 1). Today, having reached the global limits to our resource base, the assumption of infinite resources has become a fatal flaw. Natural Capital implies both the principal, which is the use derived from ecosystems such as the pollination of crops or the filtration of freshwater, and the interest on the principal, which is harvesting of their yield such as the trees from forests and the fish from the sea. In a century of scientific observations, we have come to realize that natural systems are neither necessarily reversible nor inexhaustible. Yet Huxley’s quip, that the fish in the sea are inexhaustible, still rings in the ears of governments looking to subsidize their country’s participation in the tragedy of the marine commons. Because the degradation of natural systems is considered an economic externality, the degradation of their function and yield exerts no force in the market economy. Without credible quantification and insertion of their values into the economic equation, any attempts to conserve the natural systems will be managed through legislative regulation and be necessarily confrontational with economic priorities. That is, there are two main alternatives: let the economy do it or let the governments do it. The former offers a much stronger self-regulatory dynamic (cf. Henderson, 1999; Hawkin et al. 1999). Recent assessments of the Natural Capital value of the world’s ecosystems (cf. Costanza et al. 1997) and their rates of degradation (cf. Vitousek et al. 1997) has underlined the urgent need to better quantify the goods and services derived from Natural Capital in economic terms. Costanza’s evaluation of global renewable resources arrived at a figure of 30 to 55 trillion dollars, which was well above the Global National Product of $18 trillion in 1997. The message is not so much about the absolute value, which in many cases like the atmosphere, is ines-

FIG. 1. – A depiction of the inclusion of natural capital in the economic feedback loop. Driving the price up would be the real scarcity of a natural resource relative to its long-term sustainability and the waste and pollution factors that make a commodity or service unfavorable for a sustainable society. Driving the price down would be the opposite conditions. The inside loop (red) would adjust within the constraints of the outside loop (green). A continuous monitoring of the state of Natural Capital, conducted by scientists and of its value by economists, would provide the information flux driving the outer resource loop.

timable. The message is how much will it cost us to live without, or to find alternatives for, these goods and services as they diminish. Vitousek’s article helps quantify the extent of human domination of natural systems and their rate of degradation. And Vitousek estimates that man’s sequestration of terrestrial primary production is ~ 45%. When viewed from the point of view of global resource wealth, the per capita decrease is alarming. With resources declining annually at ~ 2% and population increasing at 1.4%, the per capita wealth is decreasing at 3.4%. At these rates, we would have about two decades before global resource wealth will be half of its present value, a time scale far too short for a society which is having trouble understanding how its atmosphere –let alone the planet’s biodiversity– is changing, to confront and solve this problem. Meanwhile, the inertia of present policy is moving us toward further degradation. Role of science Once the goods and services of an ecosystem are known, even approximately, the relevant questions deal with how rapidly it is degrading, how resilient it is to further degradation, how it is linked to the degradation of other systems, and under what conditions it could restore itself. Estimates of these

aspects can be translated into terms of risk assessment and probable costs that could steer economic use and policy in the direction of minimum damage. This is the social interface part of the new role. The scientific part, which is perhaps more challenging, is learning to simulate living systems. Annual rates of degradation, as cited above, carry insufficient information to make such important predictions. We cannot assess and cost a function that we cannot understand. We are witnessing an increasing incidence of “environmental surprise” –systems collapsing or changing without formal scientific warning (cf. Bright, 2000; Myers, 1995). These phenomena involve a discontinuity or abrupt shift in what was perceived to be a stable system caused by the supersession of one internal dynamic over another, as for example the sudden loss of the Jamaican coral reefs (Hughes, 1994) or the sudden shift in bottom water production in the Eastern Mediterranean (below). They also occur when the impacts of multiple forcing functions combine synergistically to cause damage much greater than anticipated, as for example, the change in the phytoplankton community in the Danube plume due to increases in nitrogen and decreases in silicate (Humborg et al. 1997) or the record flooding of Hurricane Floyd in North Carolina due to climate variability and landuse practices (below). Addressing these problems THERMOHALINE FEEDBACK LOOPS 233

will require expansion of our methodologies to include an updated version of systems science, the new concepts of biocomplexity, and better observational means of monitoring the interactions between systems and their components. “Biocomplexity” refers to a set of theories that modify, supplement, or limit our understanding of how living systems originate, organize themselves, and interact with the abiotic environment. According to this perspective, living systems can be considered deterministic and reversible only under limited conditions, otherwise they are indeterminate and irreversible. Much of this is explained by the fact that the abiotic environment is never in steady state and thus the living system is likewise in a ‘continuum of organization’ as it adapts to the variability in the mass, energy, and information fluxes that nourish and control it. The reorganizations of living systems do have constraints, (Lotka’s Maximum Power Law, for example (cf. Odum, 1983)), and some aspects like pattern are approximately repeatable, but we know little of the uncertainties of thresholds governing the bifurcation points that result in a change in organizational state (cf. Rapport and Whitford, 1999).

THERMOHALINE INTERACTIONS Thermohaline interactions represent a very important abiotic connection for marine ecosystems. On a basin scale, they buffer the marine environment against atmospheric variability, and on a sub-basin scale, they act to stabilize the environment through recirculations that are beneficial to biological systems. For the reader unfamiliar with thermohaline circulations, I will summarize the principles needed to understand how thermohaline motions promote important ecological interactions and how they are self-regulating. Thermohaline interactions involve inputs and exchanges that affect the buoyancy (density) of the surface water. Solar radiation results in a direct input of heat to the surface layer. Heat and water vapor are directly exchanged with the sea surface. Land runoff of freshwater is an indirect input from the atmosphere, but also dependent on the hydrogeological characteristics and the land use in the catchment basin. When the land receives the water evaporated from the sea, it should be considered as a partial exchange. Momentum is also an important atmospheric exchange that affects buoyancy indirectly 234 T.S. HOPKINS

through the displacement of surface waters. The formation and melting of sea ice represent a lagged exchange of heat and water vapor. The salt in marine systems differentiates them from freshwater systems in their thermohaline circulations, biogeochemical cycling, and biological habitats. In all of these aspects, salt can be an important control variable. Here we mention it only with regard to its atmospheric interaction. While the seasurface temperature has a strong interactive pathway with the atmosphere through its control of latent and sensible heat fluxes, the surface salinity has no direct interaction with the atmosphere. The atmosphere can change the salinity only through two independent exchange processes: precipitation and evaporation. The variable of salinity is not important to an atmospheric scientist, but is essential for an oceanographer. Consequently, salinity is important for coupled atmospheric-ocean models, particularly at high latitudes where the density is mostly controlled by the salinity, and numerical models must include the dynamics of freshwater and convective motions to achieve correct salinities (cf. Bryan, 1986). Convection is an irreversible process as far the atmosphere is concerned: that is, the parcel that lost water to the atmosphere sinks and is no longer available for dilution back to its original salinity. Convection, rain, and ice formation are all processes that can delay or displace the impact of strong atmospheric interactions and thereby contribute to the stability of thermohaline circulations by dispersing the buoyancy disturbance in space and time. Thermohaline circulations Thermohaline circulations are initiated when the buoyancy of surface water is changed at some location relative to another. This is a continuous process because the atmospheric variables responsible for buoyancy exchange vary at different time and space scales relative to the ocean such that there is only rarely a zero-buoyancy flux. Any local change in buoyancy affects the weight of the water column, which in turn affects the internal pressure field and induces circulation. A brief example is that of an ice cube put into a tub of salt water. First, it bobs in the vertical as the ambient pressure field isostatically adjusts so that the ice floats high enough such that weight of the ice, supported above the water is, following Archimedes’ Principle, equal to the weight difference between the submerged ice and the salt water.

As the ice melts, a blob of freshwater will remain floating, slightly elevated, but no longer rigidly contained. The pressure field will induce small currents, which, along with molecular diffusion, will mix salt into the blob. The pressure field is best understood if it is linearly separated into a barotropic component created by the dislevel of the sea surface and a baroclinic component created by the differential weight distribution under the surface. At the sea surface, the barotropic pressure gradient forces the melt water to move outwards from the most elevated point. Underneath, the baroclinic pressure gradient forces water to move toward the same point where the weight difference is a maximum. This compensatory process, provided by the available baroclinicity, leads to two important consequences: the vertical two-way flow that is characteristic of thermohaline circulations and the absorption with depth of barotropic disturbances that otherwise might have impacted the entire water column. In freshwater, the available baroclinicity would have been only a function of the temperature difference and hence these compensatory processes would have been much weaker. If the sea surface is warmed or diluted, buoyancy is added, and a positive thermohaline circulation is initiated. If the source of buoyancy is far from boundaries, an anticyclone (northern hemisphere) would set up; if it is along the coast, a coastal boundary current would be formed; if it were inside a semi-enclosed basin, a surface outflow would occur. In all these cases, the deeper water will be forced to move underneath the surface water, while the surface water will be forced to move away from its source. The result of this estuarine shear is the process of entrainment that serves as such an important abiotic control for estuarine ecosystems. If the sea surface is cooled or evaporated, buoyancy is extracted, and a negative thermohaline circulation is initiated. In this case, however, the affected water sinks to a subsurface level matching its density. If it reaches the bottom, it will move downslope on the right side of the basin and replace any resident deeper waters of lesser density. Typically, we find dense water-mass accumulations where there are bathymetric depressions and/or bottom-water currents along the western sides of the ocean basins. Two other important differences in these circulations need to be mentioned. One involves the timedependency of the buoyancy forcing. Addition of positive buoyancy by river runoff occurs in a continuous but variable form. On the other hand, the

extraction of buoyancy, sufficient to cause strong convection, occurs seasonally with interannual variability. The second difference is that the surface water of the positive circulation entrains the deeper water that it moves over. This is a dissipative process because it weakens the pressure gradients that are driving the flow. On the other hand, the bottomwater flows are less dissipative because there tends to be less kinetic energy, less shear, and less density difference with the overlying waters. Thus, negative buoyancy waters are formed less frequently, but they also dissipate less and tend to accumulate more which gives longer residence times and the circulations that they drive more stability. We can now summarize briefly the thermohaline processes that generate the nonlinear exchange for semi-enclosed regions (cf. Hopkins, 1999). I will use the term “basin” to mean the region and “strait” to mean its constricted connection with the external ocean. The following characteristics describe a positive circulation, with the appropriate words in parenthesis for the negative circulation case. 1. A basin is exposed to significant buoyancy addition (loss) due to differential rates of heating/freshening (cooling/evaporation), relative to that of the ocean. 2. The density of water columns inside the basin decreases (increases) making them have less (more) weight (PE) than a water column outside the strait. The resulting baroclinic pressure gradient at the depth of the sill forces water into (out of) the basin. This baroclinic force increases with depth, because the weight increases, and thus also does the resulting baroclinic flow. The length scale of the baroclinic pressure gradient is several times the length of the strait. 3. Contemporaneously, when the buoyancy is added (subtracted), the basin sea level rises (lowers) and the resulting barotropic pressure gradient generates an outflow (inflow) constant with depth. 4. This initial sea-level difference would be quickly resolved by the one-way barotropic outflow (inflow) were it not for the fact that, as the opposing baroclinic flow enters (exits), it raises (lowers) the sea level. 5. At the bottom, the inflow (outflow) is subject to frictional force that makes the flow decrease at the bottom. This force is proportional to the square of the velocity, the roughness of the bottom, and the bottom area of the strait. Thus the velocity profile has a maximum outflow (inflow) at the surface and a maximum inflow (outflow) above the bottom, as in THERMOHALINE FEEDBACK LOOPS 235

10. The combined flow (thermohaline plus oscillating) can also be large enough such that the constriction in the strait reflects the flow, with the result that efficiency of the exchange is reduced (hydraulic control). 11. In wide straits, the vertical organization of the inflow and outflow gives way to a lateral organization. This allows for a greater exchange, which laterally recirculates inside the basin and can change the internal buoyancy through mixing. Thus, the exchange solution is governed by a fairly simple non-linear relationship. 12. The thermohaline exchange is proportional to the force driving it and the force is reduced by the net exchange that it drives. The proportionality is determined by the characteristics of the strait and of the higher frequency oscillations driving the barotropic pumping. Since the exchange depends on itself (via the force), it has an exponential dependency with time. Knowing the force, the bottom friction, and the buoyancy input, one can compute the net exchange. If the above complicating factors (#9, 10, and 11) exist, they must be accounted for and require additional observations to determine their effect. FIG. 2 – The two-way thermohaline exchange through a strait. a) the pressure differences, b) the baroclinic, barotropic, frictional and combined velocity profiles.

Stability of the exchange

Figure 2. With greater friction the interface, between inflow and outflow, becomes shallower so that the two flows still balance. 6. The two-way exchange is constrained to conserve the volume of water in the basin such that the net exchange equals the internal water balance. 7. The buoyancy is not necessarily conserved, but over time it converges to a running mean condition. 8. The sea-level gradient can be independently influenced by tidal, wind forcing, or atmospheric pressure differences. This causes the sea level to oscillate about a zero- mean level. These generate an oscillating barotropic flow component that is superimposed on the thermohaline exchange. The associated water transport integrates to zero over time. Three complicating situations affect the magnitude of the inflow and outflow. They are mentioned here because they enter in the discussion of the following examples. 9. The sea-level oscillations (#8) can increase the efficiency of the water-property exchange, by sloshing basin-water out of the strait (barotropic pumping) and not sloshing the same basin-water back through the strait.

Item 12 functions to make both the volume and salt exchange self-regulating. The volume is actively conserved (# 6) controlled by a simple sea-level feedback loop that is very similar for the two circulations. If we look at a perturbation in the sea level inside a basin, as for example that caused by an extreme rainfall event, the barotropic outflow increases in proportion to the change in sea level over a very short time scale. The excess water generates a one-way, barotropic supplement to the thermohaline exchange. As the excess volume decreases, so does the outflow until the exchange returns to its previous condition. Thus, we have an effective stabilizing feedback loop (FBL). The above oscillations (#8) are controlled in this manner. Of course, the basin’s barotropic response can be in resonance with an oscillating force and create amplifications (e.g. tides in the Bay of Fundy). The buoyancy feedback loop is more complex, and we need to consider the two circulations separately. For the positive circulation, the most common situation is that of freshwater addition as found in coastal estuarine systems. The freshwater input, whether totally mixed into the internal waters or not,

236 T.S. HOPKINS

a)

b)

FIG. 3 – a. The stabilizing feedback loop for an estuarine situation. Starting at the top, a runoff event increases the freshwater content in the estuary and decreases its mean density relative to that of the ocean. The density difference generates an increased ocean inflow that requires an equal increase in the outflow (plus the runoff). This response increases the net salt influx, which tends to reduce the relative accumulation of freshwater in the system. Likewise, a dry spell slows down the circulation by decreases the ocean inflow and the net salt-exchange. The salt content maps the runoff, buffered by the receiving volume, and varying about its long-term mean. b. The stabilizing feedback loop of the negative thermohaline circulation a Mediterranean-type basin. Starting at the top, a increase in the amount of dense water produced one year due to a cold, dry winter generates more outflow, which increases the inflow of warm, less salty Atlantic waters, and hence decreases the amount of dense water production the following year with the same atmospheric forcing. The reverse perturbation is shown starting at the bottom. If the basin has a large accumulation reservoir, the outflow will be buffered accordingly against annual variations in production.

creates an integrated density difference through the strait (or inlet) that drives a positive exchange. Therefore, a runoff event will increase the exchange with the ocean. The increased inflow of salty ocean water will gradually decrease the buoyancy gradient driving the exchange, and the system will return to its mean situation. This is, then, the stabilizing feedback loop, as sketched in Figure 3a. While it appears directly similar to the sea-level scenario described above, it differs for two reasons. First, the sea-level perturbation creates a one-way flow, and the buoyancy perturbation creates a two-way flow, which is slower in dampening the disturbance. Second, the time required for information about a change in sea

level to reach the strait is much shorter than that required for information about a change in density. For example, the sea-level adjustment about a runoff peak will arrive quickly because it only involves vertical movement as the barotropic wave passes; however, the information about additional freshwater involves the transport of the freshwater itself to the neighborhood of the strait where the baroclinic pressure gradient is formed. Thus, the size and the configuration of the estuary tend to buffer the buoyancy signal and delay the time to re-stabilize the exchange. For the negative circulations, the controlling feedback loop is illustrated in Figure 3b. If, during a THERMOHALINE FEEDBACK LOOPS 237

TABLE 1. - The degree of buoyancy stability provided for by the replacement inflow. The abbreviations are: VS – very strong; S – strong; W – weak; VW – very weak ATMOSPHERE BUOYANCY EXCHANGE Positive INFLOW warm cool fresh salty

Warming strong weak VS S VS S

S W S VW

Negative Wetting strong

weak

strong

weak

VS S VS S

S VW S W

S VS S VS

W S VW S

particularly cold dry winter, an excess of dense water is produced, it will more than replenish the negative buoyancy lost by the outflow during the previous year. The greater accumulation will increase the outflow and thereby cause more buoyancy to be imported from the external ocean. When the next cold season occurs, given the same atmospheric conditions, there will be relatively less densewater production because there had been more opposing buoyancy input. In this way, atmospheric trends will be mapped into the amount of dense water stored in the system and control the compensating import of buoyancy. As the atmospheric conditions return to their mean condition, so will the exchange. There will be a lag and a sensitivity to this compensation that will depend on the reservoir of dense water stored in the system, the distance from the production site to the strait, and the buoyancy characteristics of the replacement flow (Table 1). Even without replacement, the stored deep waters can gain buoyancy and increase the probability of replacement through vertical diffusion processes and even geothermal heating; for example, renewal of the Jabuka Pit in the central Adriatic is virtually assured because the bottom water is invariably cooler and less saline than the overlying waters (Hopkins, et al. 1998a).

THERMOHALINE EXAMPLES I would like to use several specific examples to illustrate how thermohaline feedback loops provide stability to the abiotic environment and how they help stabilize and enrich the biotic environment. A first-order question has to do with how the superposition of natural and anthropogenic climate variability might interfere with or exceed the range of validity of these feedback loops. This introduces the second question: What kind of trends will jeopardize the functioning of these feedback loops or even 238 T.S. HOPKINS

Cooling

Evaporating strong weak S VS S VS

VW S W S

reverse them and completely change the thermohaline structure of a marine system causing a kind of thermohaline environmental surprise? Brief descriptions of three different systems will illustrate how thermohaline interactions process abiotic variability and how they function in controlling the marine environment.

Pamlico Sound system The Pamlico Sound provides an interesting example of a positive thermohaline circulation because it is a complex ecosystem involving a gradual transition from fresh-to-salt water habitats, through which there is also a transition in the type of thermohaline control. In addition, the Pamlico Sound is being increasingly impacted by anthropogenic stresses, for example, through inappropriate land use (flooding), inappropriate agricultural practices (nutrients and pesticides), groundwater overdrafting, habitat destruction (wetland development), beach erosion on the barrier islands, and overexploitation of fisheries resources. To appreciate the natural capital of the system and its vulnerability, it is enough to say that it the Pamlico System is the second largest US estuary, a major nursery and fishing area for the Atlantic coast, one of the fastest developing US coastal areas, and one of the most frequently affected by tropical storms. System The Pamlico Sound and the adjoining Albemarle Sound constitute a shallow (< 7 m) body of water trapped behind the barrier island chain of North Carolina (Fig. 4). Because of their shallow depth and nearly closed geomorphology, the sound system is characterized by low flushing, small tides, and strong wind mixing (e.g. Pietrafesa and Janowitz, 1988)). The four major rivers that provide the land

FIG. 4 – The Pamlico-Albemarle Sound system with the four contributing rivers, Neuse, Pamlico, Roanoke, Chowan. The Pamlico exchanges with the Atlantic Ocean through three inlets in the Outer Banks barrier islands, Ocracoke, Hatteras and Oregon. Duck Pier is situated about 30 n.m. north of Oregon Inlet. Bathymetry is in meters. (From Wells and Kim, 1989)

drainage to the system discharge through four partially stratified estuaries. These estuaries act to process much of the nutrient and organic matter before it reaches the sounds. Thus, the sound system acts as a holding basin for the freshwater and for further biogeochemical processing of discharged organic matter and nutrients. The sounds serve as sites for deposition and re-working of sediments. Significantly, they provide large, brackish-water habitat for all or portions of the life cycles of many commercially valuable species. By regulating the flushing times, determining salinity, and providing a conduit for the recruitment and emigration of many estuarine organisms, the thermohaline exchange with the Atlantic Ocean controls the environment by buffering the oceanic and riverine influences. The flushing time provided by the ocean inflow is ~3 mo whereas that by the runoff is ~12 mo.

The Pamlico is connected to the Atlantic Ocean by three inlets (Oregon, Hatteras, and Ocracoke), to the Albemarle Sound northward through the wide Roanoke Channel, and to the Core Sound southward through a much smaller channel. Its two watersheds are similar. The Neuse River is a little larger and has a greater urban area than the Tar River, which drains a relatively more agricultural area. The combined runoff is ~ 9 km /yr. Both these rivers have narrow, partially stratified estuaries that are similar in size and degree of eutrophication (e.g. Paerl et al., 1998: Stanley, 1997). Both have frequent summertime anoxic events with frequent fish kills as well as occasional outbreaks of harmful algal blooms (e.g. Glasgow and Burkholder, 2000). The adjoining Albemarle Sound is also fed by two major rivers, the Roanoke and the Chowatan, which deliver another ~13 km of freshwater into the Pamlico near the Ore3

3

THERMOHALINE FEEDBACK LOOPS 239

gon Inlet. The Neuse and Tar Estuaries have been well studied, but the Pamlico Sound and the Albemarle Sound, with its river systems, have received are much less attention. Thermohaline exchange We have constructed a preliminary thermohaline exchange model as part of an attempt to study the entire system (Hopkins and Molina, submitted). The Pamlico and Albemarle Sounds were each considered as volumes of homogeneously mixed waters. They receive the freshwater from their respective rivers, the signal of which is delayed and spread out (over 1-2 days) as it is incorporated into each of the Sound’s volumes. The exchange with the ocean is represented with a single inlet having a cross-sectional area equal to that of the three actual inlets. A non-linear process modeling software (EXTEND™) was used to simulate the exchange at a daily time-step. The only period where both input data and in-situ calibration data were available was from January 1998 to September 2000. The runoff data came from the US Geodetic Survey, the atmospheric data from the US Weather Service, the coastal salinity of the Atlantic from the Duck Pier Facility, and the calibration salinity-data from the western part of the Pamlico Sound from Joe Ramus, Duke Marine Lab. The model keeps track of the density, the sea level, and the freshwater in each of the sounds and calculates the respective exchanges according to the sequence outlined above. The two unknowns are the interfacial mixing (function of Richardson’s Number)

salinity in the inlet and the friction (function of square of bottom speed) in the bottom layer. Because they both vary as a function of systems variables and have dissimilar effects on the solution, they can be calibrated quasi-independently. The ocean salinity south of Cape Hatteras has a different variability and amplitude (by ~ 0-3 ppt) than that to the north. In addition, the inflow is greater at the southern inlets during southwesterly winds, common in summer (Xie and Pietrafesa,1999). This uncertainty was partially simulated by adding a seasonally varying correction to the amplitude of the Duck-Pier salinities (Hopkins and Molina, submitted). Stability In the Pamlico Sound, the thermohaline exchange acts to stabilize its brackish water habitats by buffering the internal salinity relative to the variability of the runoff and ocean salinity. There are several basic questions concerning the capacity of this buffer during extreme storm events. For example, the resilience of the ecosystem may be exceeded under the impact of introducing large quantities of water, terrestrial matter, and nutrients into the system. While the physical system may be fairly robust, its interactions with the biological system may not be. Ecological recovery is particularly in question under the present trend for increased incidence of hurricanes, as discussed by Paerl et al. (2001). Understanding how and when these interactions switch from stabilizing to destabilizing for any given system is a fundamental step

FIG. 5 – The salinity of Pamlico Sound from the coupled model referred to in the text. The red points are the vertically integrated salinities from CTD data taken by DML only in the western Pamlico. The ocean salinities were taken from a time series at Duck Pier, north of Oregon Inlet (Fig. 4). The x axis is days starting from January 1998 to December 2000. The discrepancies with the model are due primarily the fact that the ocean salinity data were not taken near the inlets and secondarily due to the assumption of internal homogeneity.

240 T.S. HOPKINS

FIG. 6 – A sketch of an axial cross section through the partially stratified Neuse estuary situated between a riverine-mixed segment and a wind-mixed Sound. Show are its thermohaline circulation and some features discussed in the text.

toward evaluating their non-linear response to anthropogenic stress. Figure 5 shows the salinity response of the Pamlico Sound during a period which included the record flood of Hurricane Floyd on 15-16 September 1999. The storm waters completely overwhelmed the system and continued to freshen the system throughout the nineweek period of elevated land drainage. From the minimum salinities in mid December, it took until the following June to re-establish normal salinities. The hysteresis between the response and the recovery occurred because the freshening was forced by the event, whereas the recovery was a result of the stabilizing feedback loop. For shorter events, the recovery time can be quicker than the duration of the event, as seen with the discrete runoff peak at day 240 in Figure 5. This happens because the restorative action is strongest during the event and tapers off exponentially as the buoyancy gradient force decreases during recovery. Very important is that the recovery time of the salt content does not imply an equivalent flushing time for the particulate organics, nutrients, or flocculated toxins all of which react within the pelagic system and portions of which become stored in the benthic system (ibid.). The Pamlico System offers an example of how the thermohaline control could make a sudden shift to a higher mean salinity as a consequence of a substantial breach in the barrier island system. The barrier islands are vulnerable due to beach development, increased storm frequency, and sea-level rise. A large breach could change the wave environment and hence accelerate wetland shoreline erosion, and any breach would raise the salinity, possibly beyond tolerance, for many of the brackish water organisms. This is an example of a geological (and biological)

thermohaline interaction that would greatly alter the natural capital of the system. Estuary interaction The same thermohaline dynamics control the circulation in all segments of the estuarine system, but they are differently manifested in the case of vertical stratification, and the interaction with the biological system can be quite different. As an example, the Neuse Estuary is a partially stratified segment that is embedded in a larger well-mixed system (Figs. 4 and 6). The upper reaches are river-dominated, slightly brackish, vertically mixed, and input to the upper layer of the Neuse Estuary. At the head of estuary, the cross section widens and deepens such that there is not enough kinetic energy to maintain mixed-water columns. At the mouth where the estuary connects with the Pamlico Sound, the cross-section widens even more, and the situation reverts to a wind- mixed regime. The geomorphology is a strong control, but not exclusive. Consequently, the landward and seaward boundaries can extend in either direction depending on the amount of kinetic energy available (runoff or wind) and the buoyancy differential with adjacent segments. The thermohaline circulation of this segment, like any other, has the same stabilizing feature regarding its exchange: that is, an increased runoff induces an increased inflow. However, the fact that it is connected in series with two other estuarine systems limits its stabilizing capacity. For example, with a large runoff event, the input from the river-segment freshens, the outflow to the Sound freshens, the inflow from the sound freshens, and the entrainment of salt THERMOHALINE FEEDBACK LOOPS 241

decreases, making the outflow to the Sound even fresher, etc., until the upper boundary collapses and the Neuse Estuary loses its partially stratified condition. Note that during such an event, the exchange between the Sound and the Ocean brings in more salt but, as was seen in the above example, the salt recovery time for the Sound is long. Biotic connection Aspects of abiotic-biotic interaction can be illustrated with several examples. Because the runoff discharges both freshwater and nutrients to the system, the freshwater variable becomes a catalyst for abiotic-biotic interaction. An increase in freshwater input increases primary production and also it increases the thermohaline circulation. As the phytoplankton biomass increases, it advects down the estuary; as it dies, it sinks into the lower layer; as it returns up the estuary, some of it regenerates. The regenerated nutrients are then entrained into the surface layer and help sustain the surface-layer production. Were it not for this thermohaline interaction, a pulse in the river flow would generate a bloom that would be advected out of the geographic location, as occurs in a river. In the opposite case of a decrease in the freshwater input, the loop process slows and shortens. Thus, the thermohaline circulation helps stabilize the geographic location of the primary production and reinforce its growth. The bottom oxygen is also indirectly stabilized by the same loop. In the above example of a runoff event, the increased production and subsequent regeneration requires an increased demand for oxygen in the bottom layer, which is then compensated for by an increased advective input of oxygen from the mouth of the estuary. Here we have an example of how the stabilizing effect is restricted over a narrow range of events: for example, a larger runoff event may stimulate a greater production that would extend past the boundaries of the estuary and eventually reduce the oxygen levels of the bottom inflow. A third, related, example concerns the bottom organic loading of particulate matter. At some point near the head of the estuary, there is a flow convergence where the landward, bottom-layer flow of the estuary equals the seaward flow of the riverine mixed segment (Fig. 6). This is the point of furthest consistent advective penetration of salty water and is where the ‘salt wedge’ forms as the isohalines of the partially stratified estuary intersect the bottom. This bottom flow convergence generates a “turbidity maximum” 242 T.S. HOPKINS

where, due to the null-speed at the bottom, particulates can settle out faster than they are resuspended. Note, the location of the null-point migrates, as does the upstream boundary of the estuary. The effect is to accumulate organic-rich sediments on the bottom. For a certain middle range of the thermohaline and primary production, this carbon accumulation can represent a stabilizing storage of labile carbon and a site of nutrient generation. For slower or faster dynamics, it can become significantly destabilizing for the ecosystem. In the extreme runoff event sequence (above), much of the material is resuspended by the kinetic energy of the runoff and transported out to the Sound where, in addition to the increased organic load of the river, it increases the POC, turbidity, BOD, etc. During a summer period of low runoff, higher temperatures, and less advective replacement of oxygen, this accumulated organic matter drives down the bottomlayer oxygen and creates the destabilizing condition of hypoxia for the system. It also provides a site for denitrification, promoting a loss of nitrogen from the system. In the sequence of the above three examples, the primary interactions were among the freshwater, nutrient supply, and primary production. The connections with oxygen and sediments expanded from this first interaction. This partially demonstrates how internal interactions propagate within the system and take on other interactions. In the end, the signal of the abiotic event is either buffered or enhanced as it moves through the network of connections. From the point of view of the physical thermohaline stability, the system is able to recover when exposed to extreme events. Apart from the physical resilience, one might question the resilience of certain organisms exposed to rapid salinity changes or long periods of recovery. Recent findings have shown the flood-related loading to the system of terrestrial organic matter caused an impact of longer duration (Paerl, 2001). Critically important to the natural-capital assessment of the system would be the threshold switches that cause abrupt changes in the network of interactions that stimulate internal reorganization. Mediterranean system The Mediterranean is the reference system for negative thermohaline circulations (cf. Hopkins 1978). The Mediterranean marine, atmospheric and terrestrial environment defines a particular culture that has deep roots in human history. The threat of

losing this environment haunts the cultural consciousness. It is a mute question whether this derives from the dramatic paleo-environmental changes, by analogy with the neighboring Black Sea, or from the modern trends of climate change, sea-level rise, loss of fishery, and loss of a natural aesthetic. Hence, there is a strong use-value associated with preserving the Mediterranean’s marine environment. Fisheries and loss of the coastal zone assets are forced mostly by socio-economic forces. Sea-level rise and changes in thermohaline circulation that could result in hypoxia are forced by climate trends. An often asked question is whether the Mediterranean could serve as a scaled-down model for the study of climate change. Another question regards whether or not the Gibraltar exchange is a sensitive indicator of climatic trends (e.g. Garrett et al., 1990; Hopkins, 1999.) Recently, large changes observed in the Eastern Mediterranean (EMED) concerning the origin and distribution of the intermediate and deep waters (Malanotte-Rizzoli et al. 1999) have raised questions about interactions between the thermohaline circulations of the Mediterranean’s sub-basins. System The Mediterranean’s thermohaline circulation can be characterized as having a primary thermohaline cell circulating west to east in the upper layer above the depth of the two major sills (2500 m. The lettered features are as follows: CB Canadian Basin, LR Lomonosov Ridge, EB Eurasian Basin, FS Fram Strait, GB Greenland Basin, BS Barents Shelf, MR Mohn Ridge, LB Lofoten Basin, NB Norwegian Basin, IP Icelandic Plateau, DS Denmark Strait, IFR Iceland-Faeroe Ridge, FSC Faeroe-Shetland Channel. The arrows labeled a, b, c refer to the locations of the air-temperature time series of Fig. 10: a) Jan Mayen Island, b) Bear Island, c) Angmagssalik. (From Hopkins, 1991b).

THERMOHALINE FEEDBACK LOOPS 247

FIG. 10 – Schematic of the horizontal circulation and location of the three dense-water production areas (upper panel ) and the vertical circulations of these products in connection with the North Atlantic and Polar Sea (lower panel).

integral part of the thermohaline circulations of both the Polar Sea and the North Atlantic. The thermohaline influence on the Atlantic is a critical aspect of the glacial cycles (cf. Broecker and Denton, 1990). Climate models project the Polar Regions to exhibit the greatest sensitivity to greenhouse warming (e.g. Kattenberg et al. 1996). Significant changes have 248 T.S. HOPKINS

recently been reported in the Polar Sea, for example, in the water-mass distribution (e.g. Steele and Boyd, 1998) and in decreasing ice cover (Cavalieri et al., 1997). These findings put in question the stability of both the atmospheric and oceanographic feedback loops that control the stability of the Arctic heat balance and thereby the stability of Global Climate.

System The Greenland, Iceland and Norwegian Seas all have negative thermohaline circulations and produce dense-water products because of thermal buoyancy losses (cf. Hopkins, 1991a). The water masses and their trajectories are sketched in Figure 10a,b. The actual fresh-water balance for the total basin is slightly positive, but due to the large import of salt and heat from the North Atlantic, only a moderate heat loss is needed to produce dense water. Consequently, the negative thermohaline circulation is very sensitive to atmospheric temperature fluctuations and is critically dependent on a high salinity inflow. In the Greenland Sea, the Greenland Deep Water (GDW) is formed, which drives a deep outflow to the north through Fram Strait into the Polar Sea and an outflow over the Mohn Ridge to the south into the Norwegian basin. There it accumulates, and together with contributions from the intermediate water products, it forms the Norwegian Deep Water (NwDW). The Arctic Intermediate Water (ArIW) forms in the Icelandic Sea where it primarily overflows in the Denmark Strait and over the Iceland-Faeroe Ridge. The large accumulation in the Norwegian Basin mainly overflows through the Faeroe-Shetland Channel and thence moves down-slope and westward being joined by the other two overflows. The result of these combined overflows is the North Atlantic Deep Water (NAtDW), which forms the western bottom boundary current and contributes to the relatively high oxygen and lower carbon-dioxide levels of the deep North Atlantic. Therefore, the thermohaline boundary along the Greenland-Scotland Ridge imposes a strong interactive coupling between the Sub-Arctic’s negative circulation and the North Atlantic. The North Atlantic has a similar coupling with the Mediterranean Sea. The replacement waters for the Sub-Arctic, required by its overflows to the North Atlantic, enters through Greenland-Scotland-Ridge system on the eastern sides of its passages. Being less dense than the resident waters to the north, the North Atlantic water moves down the pressure gradient and against the Norwegian continental shelf where it forms the large, broad Norwegian Atlantic Current (NwAtC) (Hopkins, 1991a). Atmospheric cooling of the NwAtC forms several intermediate-water products, which we will simply refer to as the Atlantic Intermediate Water (AtIW). The most important AtIW component is the cooled version of the NwAtC that continues northward, mostly through

via Fram Strait but also through the Barents Sea, and sinks under the halocline of the Polar Sea. The other products contribute to the dense water accumulations in the Norwegian and Greenland Seas. Hence, the NwAtC provides the main source of heat and salt for the entire Arctic Ocean first by contributing to the surface waters of the Sub-Arctic and then to the sub-halocline waters of the Polar Sea. However, this is not the entire thermohaline story of the Arctic Ocean. The northern thermohaline boundary with the Polar Sea is more complicated because of the double thermohaline circulation of the Polar Sea. At intermediate and deeper depths, the Polar Sea has a negative circulation, driven by brine-water formation on the shelves and by the deep entrance of the GDW into the Eurasian Basin. This negative circulation couples in Fram Strait with Polar waters flowing south on the west side and SubArctic water masses flowing northward on the east side. In contrast, the surface layer of the Polar Sea has a positive thermohaline circulation for three major reasons. The Polar Sea receives the large runoff of the Eurasian and North American rivers (cf. Aagaard and Carmack, 1989) and it receives freshwater through the one-way flow of lower salinity water through the Bering Strait. On the other hand, it loses very little buoyancy to the atmosphere because the polar ice-cover insulates the underlying waters from surface heat-loss. This excess surface buoyancy, relative to the adjoining Greenland Sea, generates the positive circulation with its freshwater outflow leaving via the Fram Strait as the East Greenland Current (EGC) and the replacement waters entering via the NwAtC. The EGC carries roughly an equal amount of freshwater in the ice carried southward along the Greenland coast (ibid.) Part of the precarious thermohaline stability of the Arctic system is that this low-salinity water remains geostrophically trapped along the Greenland Coast and during its 1500-km passage it minimally interferes with the negative circulation of the Sub-Arctic (ibid; Hopkins, 1990b). The EGC continues as a coastal current around Greenland, around the Labrador Sea and Baffin Bay and joins the low-salinity surface flow along the East Coast of North America to Cape Hatteras. It has been hypothesized (Wallace, pers. comm.) that the particularly low N:P ratios of the Polar Sea outflow carried by this long trajectory may contribute to the nitrate limitation of primary production along the shelf boundary of the northwestern Atlantic. This would constitute another longreaching thermohaline, abiotic-biotic interaction. THERMOHALINE FEEDBACK LOOPS 249

a)

b)

FIG. 11 – a. (left panels) The annual air temperature series from three locations in the Sub-Arctic Region: Jan Mayen Island; Angmagssalik; Bear Island. b. (right panels) The observed and the calculated temperature response following a forced cooling similar to that at Jan Mayen Island for the periods 1960-69 and 1978-79 and 1981-82 (top). The annual amount of dense water produced of the three dense watermasses in response to the forcing of the same periods of air temperature forcing (bottom). From Hopkins, 1991b.

Feedback loops The ice cover in the Iceland Sea shows a larger variability from year-to-year than on an interannual scale (Malmberg, 1984). The annual air temperatures on the coast of Greenland and from the small islands in the Sub-Arctic show large variations at one-to-three year periodicity (Fig. 11a). In particular, the temperatures from Jan Mayen Island show a damped annual oscillation following the cold spell of the 1960s. Both of these characteristics are suggestive of a self-regulating mechanism. To test the hypothesis that these effects could be influenced by a thermohaline feedback loop, Hopkins (1991b) constructed a simple model of the dense-water production for the Sub-Arctic. Since each of the three water masses produced have a different water type and residence time in the system, they had to be accounted for separately. The three production areas (Fig. 10 top) were based on the mean SST values from AVHRR images. These three areas summed to the total mean ice-free region of the Sub-Arctic basin. It was assumed that heat lost to the atmosphere by each area contributed either to the preconditioning or to the formation of the associated dense-water product. The dense-water volume began to form when enough heat was removed to bring the temperature equal to that of the target water mass. The entire process was calibrated to mean esti250 T.S. HOPKINS

mates of atmospheric heat-loss, exchange, and residence times. To complete the atmospheric loop for temperature, deviations in the mean air temperature were calculated from the water temperature changes. Model simulations of perturbations in the atmospheric temperature and in the amount of ice cover confirmed the feedback-loop processes shown in Figure 12. In another simulation, the air temperatures were forced to match the 1960s cold spell and then left to be influenced by variations in the sea temperature. These results produced a year-to-year variability similar to that observed (Fig. 11b). The co-production of the three different water masses, each having different residence times and sensitivities, complicated the response. In terms of production, the AtIW is the most influenced by air-temperature variability because of its larger area and more direct coupling with the replacement inflow. This supposition is confirmed by the greater amplitudes in the air-temperature oscillations observed at Bear than at Jan Mayen Island (Fig. 11a). The ArIW outflow was responsive to temporal changes in production because of its short (~ 2-yr) residence time. Therefore, during the simulated 1960s cold spell it responded with the largest increased outflow. This responsiveness of the ArIW production to atmospheric temperature variability and its short trajectory through the Denmark Strait suggest that it could generate a corresponding variability in the NAtDW.

FIG. 12 – The thermohaline processes and feedback loops involved in changes in air temperature, salinity and ice-cover in the Greenland, Norwegian, Iceland Seas of the Arctic Ocean (from Hopkins, 1991b).

The GDW outflow was not responsive in the model to annual variability in its production because of its large accumulation volume. As explained, its outflow has two trajectories and that to the deep Polar Sea (Eurasian Basin) would be more responsive than that to the Norwegian Basin. In either case, a lessening of its production would eventually show up as a weakening of first the deep Fram Strait exchange and later of the Faeroe-Shetland overflow. The observed, multi-decadal trend in its decreased production, implied by its warmer, saltier, and less oxygenated water type (Aagaard et al. 1991), has probably altered its direct outflow to the Eurasian Basin through Fram Strait. In terms of ice cover, the modeled GDW production was the most sensitive to increased ice cover because it reduced the area of its formation. This relates to the concern of an expanded Polar-Sea freshwater outflow (discussed below) that would either inhibit GDW formation through extended ice cover or through salinity decreases.

Stability The negative thermohaline circulation of the Sub-Arctic Sea acts as a buffer to short-term climate variability. The buffering action results both from the residence time of the water mass, which decreases the impact of short perturbations, and from the buoyancy compensating effect of the replacement inflow (Fig. 12). The extent to which one could extrapolate this simple depiction to more complicated perturbations and trends is limited for several reasons involving potential interactions between variables and systems. For example, the above exercise served primarily to demonstrate how the thermohaline feedback loop could couple with the atmosphere through the variable of air temperature. While perturbations of the other two variables are also stabilized by a similar process, as per Figure 12, the model formulation did not include external forcing for salinity and ice cover, nor did it include the important interactions between water THERMOHALINE FEEDBACK LOOPS 251

temperature and salinity with respect to ice cover, or the control of all three variables by wind-driven circulations and so forth. These would enter in a more complicated model. The fact that the Sub-Arctic is situated as an intermediary system between the Polar Sea and Atlantic Ocean makes all three thermohaline systems mutually sensitive to changes in a manner that would defeat the stability of any one system. Further, all three of these systems are linked to the atmospheric system of the Northern Hemisphere. Hence, of great concern would be any interactive response to longer-termed atmospheric trends that could endanger the stability of the present Arctic ocean-climate system. Several examples follow. Of most immediate concern is the response of the AtIW because of trends now observed in the surface layer of the Polar Sea that could change the set of feedback loops controlling global climate. Two ongoing trends are being observed in the Polar Sea: increased precipitation (IPCC, 1996) and decreasing ice cover (Cavalieri et al., 1997). Both of these trigger a faster negative circulation for the Polar Sea and therefore a larger replacement flow, i.e. the NwAtC. A concurrent warming trend in the Norwegian Sea could combine with the increased volume flux to give a greater heat flux to the Polar Sea. Evidence of such an increased influx of Atlantic water into the Polar Sea is suggested by the major advance past the Lomonosov Ridge of Atlantic water-mass assemblies (McLaughlin et al., 1996). Another great concern is whether this increased heat input and the decreased ice cover could lead to a partial flip in surface thermohaline circulation such that large portions over the deep Polar Basins would become ice-free and through convection produce great volumes of dense water that would cascade into the Sub-Arctic Basin and into the deep Atlantic. The replacement requirement would draw in much larger quantities of warm Atlantic water and feed the ice-melting process. The dynamical question would be whether convection could break through the surface halocline and whether the Atlantic waters could remain dynamically separated from the waters freshened by Arctic runoff so that they could provide the high salinity source water for the convection process. This is a difficult question, as is also the question of how associated climate feedback loops would stabilize. Both the decreased albedo and the convective process would warm the atmosphere, but would also put much more moisture into the atmos252 T.S. HOPKINS

phere, which might then increase the snow cover on the arctic landmasses, again increasing the albedo and the freshwater input to the Polar Sea and thereby its ice cover. If nothing else, these uncertainties underline the vulnerability of the Arctic system and argue for better representations of ocean convective processes and thermohaline feedback loops in climate models. For the Arctic, a thermohaline circulation switch from positive to negative or vice versa, would be more aptly described as an environmental crisis rather than a “surprise.” The entire Northern Atlantic/Arctic system is presently negative, and active bottom-water production requires the warm subtropical Atlantic waters to move north to replace it. The heat of this surface influx helps warm the atmosphere. The climate reversal of the Younger Dryas is an excellent example of a thermohaline crisis when the North Atlantic switched to a positive circulation. The name refers to the period, circa 10,000 ybp, when glacial conditions returned to the landmasses surrounding the Northern Atlantic. The suggested cause was a shift in the melt-water drainage from the Mississippi to the St Lawrence Rivers causing a flooding of freshwater into the Northern Atlantic and consequently the ice cover to increase to the point of sealing off the dense-water production and thereby the poleward advection of heat (Broecker and Denton, 1990). Another important aspect of a such mode shift in the Atlantic thermohaline circulation is that stopping production creates a positive feedback loop with respect to the greenhouse effect. The ocean stores roughlyfifty times as much carbon as the atmosphere, mostly in the Pacific deep basin because of it size and slow renewal times. The North Pacific has a positive thermohaline circulation with virtually no dense-water production (cf. Warren, 1983). A reversal of the Atlantic thermohaline circulation would stop its advective, poleward heat flux and thereby cool the Northern Hemisphere. On a longer time scale, the lack of deep flushing would allow a larger accumulation of carbon in its deep reservoir and weaken the greenhouse effect and cool the atmosphere. On the contrary, increasing its negative circulation, as in the above scenario of a convecting Polar Sea, would increase the advective heat flux and increase the flushing, which would then bring more carbon dioxide to the surface and accelerate the Greenhouse effect.

CONCLUDING COMMENTS Thermohaline stability To assess natural systems it is critically important to understand how they sustain themselves in quasistable energy states. Low-entropy, biotic systems increase their resilience against abiotic (external) variability by optimizing how they process fluxes of mass and energy through both internal and external interactions. With many ways to store energy, nutrients, and carbon, they are able to reorganize to accommodate different levels of abiotic input. In contrast, abiotic systems, such as the thermohaline cases we reviewed, are much more limited in how they can reorganize. Thermohaline circulations are driven by heat and salt, and their options for storage are limited by the specific geomorphology of the basin and the circulation of its waters. Generally, their only two modes of reorganization correspond to the positive and negative thermohaline circulations. But for certain dynamics, they can have both modes: in the vertical as the Polar Sea or in the horizontal as the Adriatic Sea. We can study the range of stability of these systems by considering different geomorphic basins and the different climate regimes that drive them. From a comparative study of different systems we can better understand the thermohaline limits to the stability of a given system. The greater challenge is to understand how the thermohaline structure interacts with the resident biotic system and with other marine systems and the atmospheric. In the case studies, we have seen how thermohaline feedback loops can stabilize or destabilize both abiotic and biotic components within a system. For example, the stability of the Albemarle Sound is buffered by the intervening Pamlico Sound, such that the salinity of its replacement water is modified by that of the Pamlico exchange with the ocean. The Neuse estuary has a range of thermohaline stability within which the biological production is stabilized and out of which it was destabilized. Atmospheric trends in precipitation, ice cover, and heating have combined to change the buoyancy of the upper layer of the Polar Sea with great potential consequences to the North Atlantic and Arctic systems. Among these would be a reduced ice cover and convection in the Polar Sea. Another would be increased fluxes of fresh-water from the Polar Sea that would inhibit the dense-water production in the Sub-Arctic. Shifts in the buoyancy balances of the Adriatic and Aegean

Seas have upset the stability of the Eastern Mediterranean deep waters. It is obvious that when these abiotic examples are connected to the complete suit of biotic interactions in a marine ecosystem, evaluating questions of system stability would be greatly complicated. Science and the public A stable, sustainable society depends on a selfregulating mechanism which neither government regulation nor the present market economy can provide (e.g. Henderson, 1999; Hawken et al. 1999; Daly, 1991). The critical missing ingredient is the information on Natural Capital and its value that when inserted into the feedback loop of a sustainable economy would dampen perturbations in resource exploitation and degradation relative to a carrying capacity based on changing population, environmental conditions, and technology. While the information flow has begun spontaneously, other aspects of the changing role of science will need assistance from both the top (government and corporate support) and the bottom (social and natural scientists). An excellent example of a funding initiative is that of the US/NSF Biocomplexity Program (NSF, ). However, for the science community to have momentum beyond trends in funding will require a basic level of commitment and solidarity from the science community itself. This consensus might be only regarding priority and focus in order that the actual role can evolve. For example, marine research priorities could be split into the categories of 1) data acquisition (control, rates, model input), 2) process studies (as presently, but with greater attention to connections and interactions) and 3) systems approach (evaluations and simulations of systems using all of the above). An emphasis on systems science could be the catalyst for the evolving role for science. It would also provide many challenges connected with simulating natural systems and with developing the methodologies for coupling scientific outputs with economic/social needs. Some portion of science must have a proactive role regarding planetary sustainability. The ecosphere cannot be managed with political paradigms, and the political, social and economic sectors do not have the methodologies to acquire or interpret data or simulate management questions involving complex systems. Hindsight is useless for irreversible processes. Given the risks of a cascading global THERMOHALINE FEEDBACK LOOPS 253

degradation cycle, the science sector must prime the transition with information. And even when information has begun to flow, it is of little value to a public unfamiliar with the concepts needed to put it into a meaningful context. Consider, for example, the slowness with which society is confronting the potential threats pertaining to climate change. A strong element of public education is needed. Fortunately, the awareness curve is exponential because the more one learns the easier it becomes to learn more. That is, of course, provided the learning process is not blocked by contrary conviction. The need for a holistic assessment on the state of natural systems has a different trajectory than the need of science to understand individual components of natural systems. Governments now need to know the global carrying capacity (although they do not seem to realize this yet). They need to know how much waste we can put in the atmosphere, how many trees we need, how many fish we can take from the sea, and how many children we can have. So how could we organize our approach to answering such questions? Part of the answer lies in the second time derivative. We cannot assume systems to be in continuous steady state when our objective is to model the system response to variable forcing. In biotic systems, linearity is the exception rather than the rule. Rates of change are insufficient indicators, we need to know how these rates can or will change. We also need more documentation on the ranges of validity of the dynamics we simulate and on the error of omitting interactions. It is the potential interactions and the initial condition that determine the reorganization process. We need to eliminate (or at least try to anticipate) environmental surprises. Another part of the answer lies in complexity. We need to know how a disturbance propagates through a system, how it stimulates reorganization among internal components, and how it changes the function of the system. We also need to consider system memory and the significance of initial condition. We need to know how storage and structure control the response of a system at the onset of an event. We are really talking here about three steps or questions and a decision: Step 1) Evaluate the function and yield of a system. This is the steady-state question. In anthropogenic terms, it means what does the system do for us as it is and how much yield can we take from it. Step 2) Evaluate deviations from sustainability. This is the trends or first-derivative question. We need to evaluate how the system is 254 T.S. HOPKINS

degrading (or recuperating) and how this affects the stability of its function and yield. This would require evaluating its interactions with other systems. Step 3) Estimate the probability of irreversible change and its eventual costs. This is the second-derivative or environmental-surprise question. In most cases we can understand the types of changes possible and give some associated probability. Finally, there is the ultimate multidisciplinary decision to be made in the political, social, and economic sphere: 4) How should humans reorganize their interaction with natural systems? How can we utilize technology, through social and economic implementation, to optimize a sustainable use of natural resources? Each of the first three steps will require a greater understanding of the reorganization processes internal to systems and their interactions with other natural systems and with the anthropogenic system. Steps one and two will require a complex, intelligent monitoring system. Step three will require a complex, evolving network of simulation models. The costs will be a function of the costs to duplicate the necessary function and yield of the system and the collateral costs to interactive systems. How we make the ultimate decision, however, will require a global commitment to achieving sustainability and lots of interactive luck.

ACKNOWLEDGEMENTS The author gratefully thanks North Carolina State University for its administrative support and the following US and International funding agencies that have provided research support: U.S.A. (NSF, ONR, USCGS, NOAA/Sea Grant, NATO/ SACLANT, EU/Environment, CNR/Italy. My thanks also to Lynn Padgett for her expert editing of the manuscript. And I greatly appreciate the thermal interactions and buoyant support provided by many colleagues, students, friends and family. REFERENCES Aagaard, I., E. Fahrbach, J. Meinche and J.H. Swift. – 1991. Saline outflow from the Arctic Ocean: Its contribution to the deep waters of the Greenland, Norwegian and Iceland seas. J. Geophys. Res., 96: 20433-20441. Aagaard, K. and E.C. Carmack. – 1989. The role of sea ice and other freshwater in the Arctic circulation. J. Geophys. Res., 94(C10): 14,485-14,498. Astraldi, M., G.P. Gasparini, T.S. Hopkins and G. Manzella. - 1990. Temporal variability of currents in the eastern Ligurian Sea. J. Geophys. Res. 95(C2): 1515-1522 Bethoux, J.P., B. Gentili, J. Raunet and D. Taillez. – 1990. Warm-

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le-Pamlico Lagoonal System: Synthesis and Hypothesis. Mar. Geol., 88: 263-284. Wust, G. – 1961 . On the vertical circulation of the Mediterranean Sea. J. Geophys. Res. 66: 3261-3271. Xie, L. and L.J. Pietrafesa. – 1999. System-wide Modeling of Wind and Density Driven Circulation in Croatan-Albemarle-Pamlico Estuary System, Part I: Model Configuration and Testing. J. Coastal Res. 15(4): 1163-1177.

SCI. MAR., 65 (Suppl. 2): 257-272

SCIENTIA MARINA

2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

The sedimentary record of dinoflagellate cysts: looking back into the future of phytoplankton blooms* BARRIE DALE Department of Geology, University of Oslo, PB 1047 Blindern, N-0316 Oslo, Norway.

SUMMARY: Marine systems are not as well understood as terrestrial systems, and there is still a great need for more primary observations, in the tradition of the old-time naturalists, before newer methods such as molecular genetics and modeling can be fully utilized. The scientific process whereby the smaller, detailed “building blocks” of observation are ultimately linked towards better understanding natural systems is illustrated from my own career experience, especially with regard to the dinoflagellates and plankton blooms. Some dinoflagellates produce a fossilizable resting stage (cyst) in their life cycle, and dinoflagellate cysts have become one of the most important groups of microfossils used in geological exploration (e.g. oil and gas). This has stimulated both paleontological and biological research producing detailed “building blocks” of information, currently scattered throughout the respective literature. Here, I attempt to bring together the present day perspective, from biology, with the past, from paleontology, as the most comprehensive basis for future work on the group. This shows the cysts to be the critical link needed for focusing future molecular genetics studies towards a more verifiable view of evolutionary pathways, and it also suggests new integrated methods for studying past, present, and future blooms. The large, rapidly growing field of harmful algal bloom studies is producing many different “building blocks”, but plankton blooms as episodic phenomena are still poorly understood. This is largely due to the general lack of long-term datasets allowing identification of the changing environmental factors that permit certain species to bloom at unpredictable intervals of time. Cysts in sediments are useful environmental indicators today, e.g. reflecting aspects of climate and pollution, and provide information directly relevant to some dinoflagellate blooms. They therefore may be used for obtaining retrospective information from the sedimentary record on the history of blooms, in turn suggesting information relevant for future blooms and the way we study them. Key words: dinoflagellate cysts, algal blooms, eutrophication, molecular genetics, paleoceanography, transfer functions.

“you are the best qualified person I know of ……not on the supposition of [your] being a finished naturalist, but as amply qualified for collecting, observing & noting anything new to be noted in Natural History.” Letter from J.S. Henslow, 24 August 1831, to Charles Darwin, recommending him as naturalist to the Beagle voyage. “I believe there exists, and I feel within me, an instinct for truth, or knowledge or discovery, of *Received August 3, 2001. Accepted August 16, 2001.

something of the same nature as the instinct of virtue.” A later letter from Charles Darwin to his by then old friend J.S. Henslow.

PREAMBLE I feel a heavy burden of responsibility, having accepted the invitation to join “a group of senior scientific sages” charged with the task of “transmitting a career’s worth of wisdom and knowledge to young sages-to-be”. This is not lightened by the fact that it DINOFLAGELLATE CYSTS 257

is to be achieved through “candid, honest and open dialogue”, at the EMBS Meeting and in this written contribution. However, I can liken my own early career to hitch-hiking, where the “drivers” of that time were very generous to me as I sat by the roads of science waving my thumb. It is therefore with a deep sense of gratitude to former colleagues, at the Geology Department, Sheffield University, and the Woods Hole Oceanographic Institution, that I can now offer this contribution “from the driving seat”. Geologists generally enjoy synthesizing information from the past, and the main part of this presentation will attempt to pass on at least some knowledge from my own (continuing!) career. Deciding what might be relevant wisdom for today’s young sages-to-be, is harder. The intellectual challenge embodied in Darwin’s words quoted above still represents the main driving force for many of us trying to understand more of the natural world, but increasingly this is perceived as too unrealistic for the modern world, where scientific research is in danger of being absorbed into society’s paid beaurocracy as a service industry. One of my favorite sages, the late Holger Jannasch (1997), commenting on the waste caused by funding pressures, wrote: “The effect is worse on younger scientists, who are not rewarded for tackling a problem with perseverance, but for hopping from one promising or prioritized subject to another; funding, not science, being the ultimate goal”. I hope young scientists are wise enough to balance these destructive pressures with the basic joy of science which Holger stated later in the same article: “My critical remarks notwithstanding, I am, as most of my colleagues are, well aware of the privilege of being paid for work that often feels like the pursuit of a hobby”. One further point that I wish to address, regarding the way we approach basic research, concerns the need to specialize. Especially within educational circles, the need to produce more generalists in science, i.e. people with more than a one discipline view, is often stated. Ironically, my own experience strongly suggests that one of the most effective ways to achieve this, at least in marine science, is by dedicated specialization. Marine systems are still poorly understood (certainly compared to terrestrial systems), and marine science therefore still needs the combination of sample collecting and primary observation that Darwin enjoyed 150 years ago. Contributing the necessary primary observations today demands more specialization, but this may still be carried out in the best traditions of naturalists such as 258 B. DALE

Darwin: curious enough, determined enough, and not least willing to ignore the boundaries between the various natural sciences. Some of the best things happen in marine science, as in natural science in general, by examining some smaller entity in great detail and relating this to a bigger picture. Applying the naturalist approach, it is virtually impossible to delve deep enough to make a significant specialized contribution without being confronted by the need to understand other overlapping fields. Young sages-to-be may well consider this concept, too, to be unrealistic for the modern world. It is certainly difficult to compare the hectic, heavily managed framework for basic research today with visions of Darwin sailing round the world for years, studying all aspects of natural history. A would-beDarwin, today, would have difficulty funding a project with a main objective to concentrate on geological observations, and a secondary objective to contemplate (for a few years) the morphological details of certain finches, and the possible implications of this for creation. Nevertheless, the inquisitive, observant and interdisciplinary approach of the early naturalists still offers the best way of tackling the enormous task of primary observations needed to understand marine systems. This poses problems for today’s scientist. Firstly, it may be difficult to accept that part (much?) of marine science is still at the basic level of observation, whereas the rest of science is already testing paradigms and modeling systems. From this perspective, it is certainly not prudent to cite old sages such as Darwin in the methods section of research proposals. Even those scientists who recognize the basic value of interdisciplinary research may experience difficulty in accepting responsibility for this in practice. Having studied the small entity in great detail, many may feel that it is sufficient to publish this in a specialized journal with minimum discussion of its implications for the bigger picture (safe science). Indeed, this view is rewarded by the career system in academia, which often seems to give more weight to the frequency, and possibly the volume of publications rather than to their scientific depth. In my own career, I have been privileged to be able to follow a somewhat unusual course that has allowed me to wander freely between aspects of geology, biology and oceanography. Inevitably, this has required spending proportionally more time reading than writing compared with a more conventional, single discipline approach; for example, based on following the literature in any one of my

main fields of interest (micropaleontology, plankton biology, harmful algal blooms, eutrophication and marine pollution). Therefore, it might seem negligent for me to recommend that any younger scientist should attempt to follow such a multidisciplinary path today, even though I have argued strongly for the need. However, despite the problems noted above, I remain an optimist by nature, and two reasons prompt me to appeal for a return to a more naturalist approach. The first, and probably by far most important reason, concerns the seemingly unlimited opportunities opened up by modern communication. Basic information for “the other overlapping fields of research” is far more easily available through electronic networks today, and there is a continuous stream of data being collected from satellites and well-equipped ships. This, together with opportunities for various specialists to cooperate in multidisciplinary research projects, or informal networking groups, should provide exciting opportunities for modern scientists to carry on the work started by the old-time naturalists. The second reason concerns the sort of efforts being made through this meeting. The hope here is that senior scientific sages can help draw together some of the otherwise more isolated details, and place them in a larger perspective that somehow improves the way we see things now, and helps shape the way we do our science in future. I will attempt to do this, here, based on my own career’s experience. The main theme concerns the phytoplankton of the oceans, appropriate for a celebration of Professor Margalef, and the large part of his scientific life devoted to unraveling the complexity of their ecology, certainly in the best traditions of natural history.

INTRODUCTION My own career began in geology in the early1960s; helping to develop techniques for extracting some of the wealth of fascinating microfossils found in the geological record. It is now taken for granted that the microfossils provide the main evidence for organic evolution through more than the first three-quarters of the history of life on Earth (e.g. Brasier, 1980), but having seen some of these for the first time has always felt like a privilege. Almost nothing was known regarding their biological affinities, and the next phase in my work involved a move to oceanography, helping to iden-

tify the affinities of a previously unknown group, the hystrichospheres, that were promising to be particularly useful in geology. We proved these to be the resting stages (cysts) of dinoflagellates by incubating living representatives of the group (e.g. Wall and Dale, 1966, 1968; Fig. 1). It is not possible to describe the exciting sense of discovery we experienced, linking these “living fossils” with their biology. For us, this was like finding some unknown egg in a remote desert, today, and incubating it to hatch out a real-life dinosaur (the first cyst we incubated belongs to a genus, Spiniferites, dating back to the time of the dinosaurs). That one of the major groups of microfossils proved to represent a stage in the life cycle of one of the major groups of phytoplankton, opened up new perspectives, and consequently, most of my work since has focussed both on the biology and paleontology of dinoflagellates. A lot of work has been done on dinoflagellates in the past twenty years, mostly by specialists either in micropaleontology or plankton biology. The fossil cysts have been developed as one of the main groups used routinely in biostratigraphy (e.g. in the oil and gas industry; Stover et al., 1996). This, in turn, has stimulated research on living cysts, particularly distribution studies aimed at testing their potential value as paleoenvironmental indicators (e.g. Dale, 1996). Biological studies of dinoflagellates have largely been stimulated by the increasing focus on harmful algal blooms (HABs). Dinoflagellates are one of the main groups causing HABs, and there is increased awareness of the possible role of cysts as seed beds and toxin sinks. From my paleo-biological perspective, I see areas where the knowledge developed within the one discipline is relevant to developments in the other, and therefore should influence it more. Hence, this attempt to build bridges between the two. As the title suggests, I shall first use the paleopart of this perspective to look back into the cyst record in sediments, and identify information of particular relevance to better understanding dinoflagellate biology. The second part of the title relates this to future biological work on the group, most of which is likely to be directed towards understanding blooms. Understandably, much of the basic biological information to date is influenced by chance, (e.g. dependent on which species is available for study in laboratory cultures). The aim, here, is to identify from the cyst record fundamental problems needing to be understood, so that DINOFLAGELLATE CYSTS 259

FIG. 1. – Dinoflagellate cysts - ancient and modern.1-6. One of the first documented excystment series from a dinoflagellate cyst ( Gonyaulax digitalis incubated from local bottom sediment in Woods Hole Harbor, reported by Wall and Dale, 1968: Fig. 2). The prevalvate “gymnodinioid” stage with only one functional flagellum emerged through the archeopyle within just a few minutes (note the gelatinous cover surrounding the protoplast as it emerged by amoeboid movement). 5. Empty cyst remaining after excystment, referable to the paleontologically named cyst Spiniferites bentori (this genus has a fossil record extending back to the Cretaceous). 6. The theca developed by the emerged motile stage after one day; identified as G. digitalis to establish the theca/cyst relationship linking plankton biology and paleontology of the group. 7. Encystment of Protoperidinium oblongum (newly formed cyst inside the theca of the planozygote); Woods Hole plankton, september,1965. 8. Resting phase in Protoperidinium oblongum cyst, showing lipid globules presumably serving as food reserves; bottom sediment, Woods Hole, 1965. 9. Resting cyst of Protoperidinium conicoides; bottom sediment, Woods Hole, 1965. 10. Large round brown protoperidiniod cyst showing archeopyle and partially attached operculum; recent sediment off the coast of Peru. 11. Impagidinium patulum, a warm-water oceanic indicator, with reflected plate pattern; recent sediment, Mediterranean Sea. 12. Impagidinium pallidum, an extremely cold-water oceanic indicator, bipolar; deep-sea sediment trap sample, Fram Straight, N.E. North Atlantic. 13. Spiniferites mirabilis, a cosmopolitan coastal species; recent sediment, Norway. 14. Spiniferites membranaceum, a colder-water coastal species; recent sediment, Norway. 15. Gonyaulax polyedra (= Lingulodinium machaerophorum), cyst in resting phase, a warmer-water coastal species; recent sediment, Los Angeles Harbor, USA. 16. G. polyedra cyst showing reduced, bulbous processes characteristic for low salinity waters (e.g. compare processes with those in 15); recent sediment, Baltic Sea. 17. Peridinium faeroense (= Pentapharsodinium dalei) cyst, a living acritarch produced by a thecate dinoflagellate; recent sediment, Norway (photo by M.L.L. Sætre). 18. Low magnification view of rich concentration of living cysts of the toxic Alexandrium tamarensis, potential seed beds and sinks for large amounts of toxin; deeper water recent sediment, offshore Gulf of Maine, USA. 19-21. Fossil dinoflagellate cysts (photos by R.L. Williams). 19. Leptodinium mirabile, a cyst showing almost complete reflected plate pattern of a dinoflagellate; Jurassic sediment (ca. 155 million years old), Svalbard. 20. Deflandrea phosphoritica, cyst showing some obvious morphologic relationship to the dinoflagellates; Eocene sediment (ca. 50 million years old), Texas, USA. 21. Oligosphaeridium sp., cyst showing less obvious morphologic relationship to the dinoflagellates (apical archeopyle, and each process representing reflection of a plate in the recognizable “thecal” pattern); Cretaceous sediment (ca. 135 million years old), Svalbard. 22. A Paleozoic acritarch showing no obvious morphologic relationship to dinoflagellates, but the rich assemblages of such acritarchs, predating the recognized cyst record, most likely include some earlier dinoflagellate cysts (photo by G.D. Wood).

260 B. DALE

future biological studies can help be more focussed toward these. Biology provides a present-day perspective, paleontology the past, and together they should offer the most comprehensive basis for future work. This short contribution will concentrate more on concepts and ideas; minimum space is used for repeating documentation from the often more specialized literature, but this is covered through a few key references pointing to further reading. Dinoflagellate cysts Dinoflagellates are one of the major groups of microplankton, present in virtually all aquatic environments, where they often account for substantial amounts of the planktic biomass (e.g. Taylor, 1987). Approximately half of the known species are photoautotrophs, and the group was traditionally considered to be part of the phytoplankton, classified within the algae. In fact, they are an ancient, highly complex group, including many heterotrophic species living by predation on other microplankton, and some mixotrophic species combining both trophic methods. They are single-celled, and are now considered to be protists, classified within their own Division, Dinoflagellata (Fensome et al., 1993). Prior to the 1960s, they were studied almost exclusively from the characteristically biflagellated motile cells found regularly in the plankton, and the morphology of this stage still largely forms the basis for classification. The discovery, by paleontologists in the 1960s, of a resting cyst in the life cycles of many species was surprising to plankton biologists (Dale, 1983). A review of the earlier plankton literature shows occasional observations of what we now know to be cysts, but neither the extent nor the significance of this had been realized before. Approximately 10% of the around 2000 marine species of dinoflagellates produce such cysts, and they are widely considered to be formed as hypnozygotes in a sexual cycle. Most of them appear to serve as a benthic resting stage: cell contents full of food-storage products such as starch grains and lipids, enclosed in a protective cell wall, and equipped with a mandatory resting period. The cell wall in many species comprises heavy, complex organic molecules (dinosporin), similar to the sporopollenin of plant spores and pollen grains; others produce thick cyst walls of calcite crystals, and even a few siliceous cysts are known from the fossil record. They are extremely resistant to physical, chemical, and bio-

logical breakdown; some have remained viable for up to ten years in anoxic black mud in my refrigerator, while a few reports elsewhere suggest the possibility for survival over at least several tens of years. The empty non-mineralized cyst walls show various degrees of resistance. In many species these are resistant enough to fossilize, whereas others do not seem to persist from surface sediments into the fossil record, and some degrade within a few minutes of excystment. Little is known regarding why and how cysts form in nature. Cyst-formation has been induced in laboratory cultures of some species by exposing them to nutrient starvation, and this has lead to the widespread concept of cysts forming in response to adverse conditions. However, in general it is hard to correlate the regular, yearly, cyst formation in the natural environment (e.g. in a Norwegian fjord) with adverse conditions. On the contrary, the little available evidence suggests that cyst formation may be associated with maximum population numbers of motile cells (presumably maximizing the chances for successful mating), with no demonstrated lack of nutrients. The inducement of excystment in laboratory experiments is more compatible with observations from nature, at least for temperate to high latitude environments. After completion of dormancy, cysts will excyst if returned to an appropriate temperature for the motiles to grow. This presumably provides a basis for the cysts to function as an overwintering stage at higher latitudes, but offers no plausible explanation for how the many cyst-forming species function at equatorial to low latitudes. At these latitudes, some species, including the HABproducing Gymnodinium catenatum, may in fact produce cysts that excyst normally within a few days without accumulating as potential seed beds (Dale and Amorim, 2000). It should be obvious, even from this very brief summary, that we still know little concerning the basic biology of the cysts. However, a review of the current literature shows an increasing awareness within plankton biology of the need to better understand resting stages in general, and dinoflagellate cysts in particular. I am therefore confident that biologists will continue the research needed to find out more about what the cysts are, and why and how they function in the life cycle. I will try to draw together some points of interest from the fossil record that may help formulate research strategies for increasing the worth of such research to both biology and paleontology. DINOFLAGELLATE CYSTS 261

THE SEDIMENTARY RECORD OF DINOFLAGELLATE CYSTS: WHAT’S IN IT FOR BIOLOGY? It is convenient to consider the record of cysts in sediments on different time scales, as seen by looking back: 1) over the past few years to tens of years represented by recent sediments – allowing us to relate cyst distributions to known environmental parameters , and assess their potential as environmental indicators; 2) tens to hundreds of years in short cores – useful for assessing human impact; 3) thousands to a few millions of years in longer cores or rock sequences – e.g. useful for detecting effects of major climatic change; and 4) hundreds of millions of years in rocks - necessary for tracing pathways of evolution. The past few years time scale: cysts as environmental indicators Both paleontologists and plankton biologists may be surprised by the extent to which cysts in recent sediments reflect their environments. Planktic organisms such as dinoflagellates, easily dispersed from their ecological core regions by water transport, are not usually considered likely to be useful environmental indicators. The standard biogeographic zones in the ocean are therefore defined largely using benthic organisms or others such as fish, able to actively maintain contact with a definable environment. Nevertheless, the first studies on distribution of cysts in recent (surface) sediments showed this to be closely linked to environment (e.g. Wall et al., 1977), and some cyst types are now considered to occupy some of the main biogeographic zones previously established from the benthos, etc. (Dale, 1983, 1996). Some other cysts show biogeographic distributions closely corresponding to those of macro algae. This is presumed to reflect a life cycle in the cyst-forming dinoflagellates incorporating both a planktic phase and a benthic phase (cyst) that effectively “anchors” the species to a preferred environment, e.g. somewhat comparable to mollusks or attached algae, also with planktic life cycle stages. This research has begun to suggest an ecological classification for the cyst types, but in order to establish, and apply, such a classification also requires understanding the sedimentary system. The organicwalled cysts behave as fine silt particles in the sedimentary regime, and tend to be transported and 262 B. DALE

accumulated with this fraction. In cyst distribution studies, it is therefore critical to distinguish between more sheltered coastal waters, with minimal sediment transport, and more exposed offshore waters with possibilities for long distance transport. Many cysts seem to be produced by species living in coastal and neritic waters (not surprising if they are reliant on completing a life cycle with a benthic resting stage). It is studies of these cysts in sheltered bays, fjords, and boat basins along coasts that is revealing consistent biogeographic zones; however, these coastal cysts may be regularly transported further offshore, and eventually dispersed into the deep sea, far outside their ecologically critical core areas. Some investigations (notably those employing transfer functions), discussed below, fail to recognize this, and treat even the cyst assemblages in the deep ocean as representative of surface water conditions immediately overlying sediments in water depths of up to several km. Recent cyst distributions described so far allow basic ecological classification into the following main categories (summarized in Dale, 1996): cosmopolitan species (equatorial to sub-polar in both hemispheres); cold-water coastal species (polar to sub-polar, mostly bipolar); warm-water coastal species (equatorial to temperate); warm-water oceanic species (a few truly pelagic species with cysts functioning in some alternative way to benthic resting stages); and cold-water oceanic species (one so far described, the bipolar Impagidinium pallidum, occupying extremely cold, oceanic, polar waters). Combinations of these cyst assemblages, in turn, allow the identification of ecological signals (i.e. recognition from the cysts of certain environmental parameters) potentially useful for paleoenvironmental interpretations. To date, these (summarized in Dale, 1996) include cyst signals of: sea-water temperature, salinity, coastal versus oceanic waters, and productivity (e.g. oceanic upwelling, and coastal eutrophication). The tens to hundreds of years time scale: cysts as indicators of human impact on the environment The natural sciences are being challenged by public concern over impact on the marine environment of a rapidly growing human population, and associated industrialization. All too often, this requires scientists to provide assessments of changes over time in environments where the necessary long

term monitoring data is inadequate. Micropaleontology is helping by providing retrospective data from microfossils archived in bottom sediments, and the first attempts to apply dinoflagellate cysts in this way are summarized by B. Dale and A.L. Dale (in press). The cyst record shows significant (often considerable) changes in assemblage composition on the scale of tens to hundreds of years. This should be of interest to plankton biologists, since there are very few consistent long term plankton datasets, even within the range of tens of years, offering a framework for assessing their many short term observations. Some of the noted shifts in cyst assemblages may be related to climatic change (discussed in the next section), but others are associated with marine pollution, particularly cultural eutrophication. One cyst signal of cultural eutrophication was described from the Oslofjord (Dale et al., 1999), based on comparing changes in the cyst record in cored sediments (dated by lead isotopes) with the known history of cultural eutrophication. The main elements of this signal are illustrated in Figure 2, and comprise: 1) overall increased cyst concentration (approximately a doubling of numbers of cysts/g dry sediment) –interpreted as reflecting increased productivity, including the cyst-forming dinoflagellates; and 2) a

massive increase of the photoautotrophic species Gonyaulax polyedra (= Lingulodinium polyedrum)– that blooms in the fjord in late summer. This species is thought to have benefited particularly from the nutrients added throughout the year from sewage; the fjord is an otherwise nutrient-limited system in which the spring bloom utilizes much of the available nutrients, and summer-blooming species are restricted to what is remaining. The extra nutrients presumably did not stimulate growth in the spring plankton, since this was not previously limited by nutrients; an assumption supported by the fact that a prominent spring-blooming species, Peridinium faeroense (=Pentapharsodinium dalei) showed no increase (Fig. 2). A very different cyst signal has been obtained from the several examples studied so far of systems presumed not to have been nutrient-limited prior to pollution. However, since the published examples are from sites subjected to both sewage effluent and heavy industrial pollution, this makes it impossible to separate (identify) possible effects of eutrophication from possible effects of the industrial pollution (e.g. in the Frierfjord, Norway, by Sætre et al., 1997; and in Tokyo Bay, Japan, by Matsuoka, 1999; discussed by Dale, 2001). Nevertheless, ongoing analyses by Sætre of several Norwegian fjords not affect-

FIG. 2. – Diagramatic representation of the cyst eutrophication signal in the inner Oslofjord. Box shows time period with documented eutrophication from about 1900 to 1980. Note that the spring blooming species Peridinium faeroense (blue triangles) showed no increase during eutrophication

DINOFLAGELLATE CYSTS 263

ed by massive industrial pollution, suggest this to be an alternative signal of eutrophication (Sætre and Dale, 2001, poster at this meeting). This signal is characterized by: 1) unchanged, or reduced cyst concentrations; and 2) at least a marked proportional shift to more heterotrophic species. The few millions to thousands of years time scale: how were dinoflagellates affected by the Great Ice Ages? It is a sobering thought that for many thousands of years prior to about 10,000 years ago, here where I sit writing this in my home near Oslo would have been covered by an approximately 4 km thick ice sheet. There is a wealth of literature describing how the earth’s climate has changed continuously throughout geological time, on many different time scales, and there is evidence of previous massive glaciation as far back as 2.5 billion years ago (BYA). We know that the last Great Ice Age in the northern hemisphere began about 2.5 MYA, whereas ice on Antarctica occurred at least as far back as 40 MYA. The dramatic effects of the last glaciation on the terrestrial environment are well documented, e.g. fossil pollen showing the migration of vegetational zones such that parts of southern Europe were covered by birch forest and scrub-tundra while Scandinavia was covered by its thickest ice sheet (van der Hammen et al., 1971). Great effort has been made during the past 25 years to generate corresponding information from the oceans. Micropaleontology provides much of the evidence, and of particular interest, here, is the fact that dinoflagellate cysts are proving useful as “marine pollen”. The biogeographic zones established for recent cysts (described above), can be seen to migrate in the world’s oceans in response to climatic oscillations between glacial and interglacial conditions, on the time scale of many thousands of years, analogous to terrestrial vegetation (Dale, 1996). Investigations on the time scale of just a few thousand years have even allowed us to identify fossil “blooms” of species seemingly caused by the smaller scale climatic changes typical within what may well be the present interglacial period. In a series of long sediment cores from the KattegatSkagerrak region of Scandinavia, we documented two periods of marked increased abundance (“blooms”) of what was then considered the cyst of the toxic species Gymnodinium catenatum, dated to around 6000 yrs BP (before present) and 1000 yrs 264 B. DALE

BP. Subsequent studies confirmed the close association of the later of these with the Medieval Warm Period, and its termination corresponding to the Little Ice Age (e.g. Thorsen and Dale, 1998). This species (now called G. nolleri) is not recorded live from the region today (although present in small numbers further down the Danish coast), but at the height of the Medieval Warm Period, it dominated cyst assemblages by up to around 60%. Its known distribution elsewhere confirms this to be a warmer water species (e.g. living along the Iberian Peninsula, and in Australia). That the estimated average temperature increase of around 1-2°C could have caused such an assemblage shift, at least within the cyst-forming species of dinoflagellates, is of interest to both paleontology and biology. At the other extreme of the time scale under consideration, i.e. tens of millions of years, we may explore some of the effects of major climatic change on the dinoflagellates as a group. Comparing the known geological ranges for the different ecological groups classified through our recent cyst distribution database produced interesting results. Figure 3 shows plots for the geological ranges for twenty of the ecologically most important cysts in our global database, suggesting the following main conclusions: 1) the cosmopolitan, and the warmer water coastal species are both long-ranging, with origins predating the onset of major glaciation at around Middle Miocene time; 2) the warmer oceanic species show similar, though not such long ranges; and 3) the colder water coastal species are short ranging, post dating the onset of major glaciation. Not surprisingly, the main interpretation of these results suggests that the plankton living at present includes: 1) cosmopolitan species that have survived a long time due to their broad tolerance for environmental change; 2) warmer species that were able to survive global cooling by remaining in the albeit reduced warmer zones; and 3) newer cold water species presumably having evolved to occupy the colder waters generated by global cooling. The hundreds of millions of years time scale: the big picture The dinoflagellates have an unusual fossil record, with an isolated occurrence of fossil cysts in the Silurian (about 400 million years ago (MYA)), followed by a gap of around 200 MY before the rich and varied, continuous, record from the Late Triassic to the present. While this record certainly is

N. laby

I. acul

P. conicum

S. delic

S. mirab S. hyper O. cent

S. ram S. bull

oceanic

P. faeroen Ant. prots

coastal

P. coni.des C.T. 118

coastal S. elong

coastal M. minuta

warmer

L. sabrina

cosmopolitan

S. lazus

L. mach

colder

O. israel. P. zoharyi

warmer

Quaternary Pliocene

Miocene

Oligocene

?

Eocene

Upper Paleocene

Upper Jurassic

FIG. 3. – Age ranges for twenty of the most ecologically important cyst types in our global database of recent cyst distribution. Ecological groupings for the cysts are defined in the text.

influenced by heavy sampling biases (due largely to where in time and space geologists have explored for oil and gas), the basic pattern including vast amounts of time with no fossil cysts is expected to be representative. There are several reasons why this fossil record should not be taken as the complete picture of dinoflagellate evolution. Organic geochemistry reveals the presence of marker species of compounds (dinosterols) believed to be uniquely produced by dinoflagellates, at least as far back as the Cambrian (Moldowan and Talyzina, 1998), suggesting the presence of the group well before 500 MYA. The seeming conflict between this and the stated fossil record from the cysts may be explained to some extent by the patchy nature of cyst formation and preservation previously outlined. Given that only some species form cysts today, and many of those may not fossilize, maybe the group initially “experimented” with the need for fossilizeable cysts for a long time.

This may have contributed, but a more powerful explanation is to be found through closer examination of the definition of dinoflagellate cysts. As some of the previously unknown hystrichospheres were identified as dinoflagellate cysts, and therefore transferred to that group, a new inserte sedis group, the acritarchs, was erected (Evitt, 1963) to accommodate those remaining. The acritarchs are thus a large group of organic-walled microfossils, of unknown biological affinity, presumed to include representatives from many different biological groups. The dinoflagellates are defined morphologically based on characteristic features of the living motile cells, which do not fossilize, though these diagnostic features may be reflected to some extent in the morphology of cysts, revealing their biological affinities. This is particularly the case in many cysts of thecate dinoflagellates (i.e. those with motile cells covered by series of clearly defined cellulosic plates), where the cyst morphology may reflect at least part of a plate pattern. DINOFLAGELLATE CYSTS 265

This type of reflected morphology allows dinoflagellate cysts to be identified as such, even from the fossil record (Fig. 1), but it is important to realize that by no means all living cysts show such features, and those that do are almost exclusively from thecate dinoflagellates. Incubation experiments with living cysts have thus confirmed the dinoflagellate affinities of some of the important cyst types prominent in the paleontological record (e.g. the ancient genus Spiniferites). They have also revealed many cysts lacking the reflected features of motile stages, that otherwise would be classified as acritarchs in the fossil record. One acritarch, believed to be the living representative of a species originally described from the Eocene (around 40 MY ago), even incubated to produce a thecate dinoflagellate identified as Peridinium faeroense (Dale, 1978). This has serious implications for interpreting the fossil record of the group. Whereas some dinoflagellate cysts are identified morphologically to produce the fossil record, it may be assumed that others remain unidentified within the acritarchs. The acritarch record is characterized by a wealth of described species from the Precambrian to the end of the Paleozoic Era (i.e. before the continuous identified cyst record begins) that most likely include the earliest dinoflagellate cysts. The classification boundary between acritarchs and dinoflagellate cysts is thus at best fuzzy. This is because paleontologists working far back in geological time are generally reluctant to describe the morphology of acritarchs using cyst terminology, with the implication that these could be cysts before their accepted geological record (even though similar, but non-motile-stage, features are now known from some living cysts). Many paleontologists working at the other end of the record, e.g. with Quaternary to recent samples, more or less ignore the acritarchs, and regularly describe and record “dinoflagellate cysts” that show no reflected motile-stage features, and therefore qualify in fact as acritarchs.

IMPLICATIONS AND APPLICATIONS FOR BIOLOGY I realize that it may be difficult for some marine scientists to share a perspective of organic life on Earth subdivided into dinoflagellate cysts and “others”. Even within marine biology there still may be 266 B. DALE

scientists who would question the value, to basic research or applied science, of studying one stage in the life cycle produced by 10% of one group of microplankton. Fortunately, there is no precedence in basic research for having to answer such doubts: you study cysts, or finches, or moldy bread, etc., first, to observe and document the details, so these can be considered together with all the other “building blocks” to develop wider concepts of how natural systems work. In general, science has to happen before applied science; applications become apparent along the way. Having touched on some of the detailed “building blocks” from the cyst work so far, we can now consider possible implications and applications which these suggest. The main concern, here, is to draw together information pertinent to biology, but there is an equal and opposite need for information flow the other way, as illustrated by the comments (below) on paleoceanography. This is not a full review of the possibilities, but a personal selection, with emphasis on those directions in which I know marine science is going. The general need for more basic biological information on which species produce cysts, and the role of cysts in life cycles, etc., will not be elaborated further, since both paleontologists and biologists are aware of this, and in some cases working on it. Inevitably, there are recurring themes (e.g. the need for paleontologically relevant cultures), but for convenience, my comments are gathered under the following selected topics: 1) genetics and evolution; 2) paleoceanography; 3) environmental sciences; and 4) blooms. Genetics and evolution: the ultimate overlap of paleontology and biology The application of molecular genetics to problems concerning evolution and phylogeny is one of the most rapidly developing fields of research in biology. It is also one of the most promising lines of future research that should help develop greater understanding of the evolution of the phytoplankton. For the dinoflagellates, this will necessitate more consideration of the cysts: since the fossil record of dinoflagellates is made up of cysts, the living cysts represent the critical link between biological and paleontological information developed for the group so far. With respect to dinoflagellates, the question, here, is not so much what cysts can do for future applications of molecular genetics, but rather how such studies can proceed without them.

To date, the first attempts to apply these new tools to reconstruct evolutionary pathways for the dinoflagellates have relied heavily on the relatively few available cultures, almost exclusively species with no known cyst record. While these first results seem promising, they hang largely in paleontological limbo. The scientific value of future applications would therefore be strengthened enormously if they could include a selection of cyst-forming species that are as representative as possible of both the main morphological groups of cysts and as wide a span as possible in their geological ranges. This would require close cooperation between paleontologists and geneticists (easy to justify scientifically), and the establishment of paleontologically relevant cultures (long overdue for a wide variety of related studies). Results such as those discussed above, and shown in Figure 3, support the need for future applications to progress from samples of opportunity to targeted species. While such results may be anticipated from basic principles of evolution, they are presented here because they offer a perspective on the plankton not easily attained through biological studies, based on evidence that can only to be gathered from paleontology. Identification not only of the age of individual living species, but also groups of species with significantly different ages, opens up new possibilities for concentrating molecular genetics studies where they will have more impact. Again, this will require new cooperative research between paleontologists and biologists, first to identify many of the cysts through incubation experiments (e.g. 14 of the 20 species illustrated in Figure 3 are known so far only from the cysts), and then to establish cultures that may be used for genetic and e.g. autecological research. Another specific topic identified as particularly relevant to future applications of molecular genetics concerns the acritarchs (discussed above). There are many more living acritarchs than the literature suggests, for reasons stated above. The morphology of many acritarchs is simple, but the fossils have been classified into morphological groups, some of which may be traced through long periods of the Paleozoic and Mesozoic Eras, and are represented by living forms today. This suggests possibilities for future studies to target a selection of the morphological groups of living acritarchs. I advocate this approach, not from an assumption that these simple morphological acritarchs have to necessarily represent identifiable genetic links to their ancient Paleozoic look-alikes, but the possibility is interesting enough to merit investigation. These sort of investigations inevitably

alter the way in which we view our science, and this in itself has great value: discovering that one proper acritarch was the resting cyst of a thecate dinoflagellate does not imply that all are, but it supports the possibility that at least some could be, in which case finding out which would move the subject forward. The fact that athecate dinoflagellates seem to produce only acritarchous cysts today may prove to be particularly significant. The athecate forms represent a large subdivision today, and yet their fossil record is probably excluded from the currently recognized record of dinoflagellates, since this is based solely on cysts reflecting thecate morphology. Paleoceanography: the widening credibility gap One of the major concentrations of scientific resources, today, is invested in climate-related studies, fueled by public concern over the threat of imminent global warming. The main thrust of the research strategy being followed involves modeling past and present climate, as a basis for assessing possible developing changes for the future. Micropaleontology is largely responsible for feeding the modelers with climatic data from the past, using various groups of microfossils from cored ocean bottom sediments as paleoclimatic indicators, and this is now established as a main field within paleoceanography. Virtually nothing was known regarding the living ecology of the first fossil groups to be applied, e.g. planktic foraminifera, precluding possibilities for developing a direct paleoecological basis for interpreting past water temperatures and salinities. A statistically-based alternative, the now famous transfer function method (TFM), was devised by Imbrie and Kipp (1971), and this has formed the basis for applications using different microfossil groups ever since. Description of the method and its application is beyond the scope of this discussion, but it relies on a basic assumption that there is a relationship between the distribution of the organisms and the few selected environmental parameters of interest (i.e. temperature and salinity). The method then uses statistical treatments to relate the distribution of microfossils in present day surface sediments to the known values measured from overlying waters (the transfer function). This, in turn, is used to estimate paleotemperatures etc., from the microfossil assemblages, and in this way, massive amounts of plausible data on estimated winter and summer values have been incorporated into the models over the past 25 years. DINOFLAGELLATE CYSTS 267

Of particular interest, here, is the fact that the transfer function method has also been applied to dinoflagellate cysts (e.g. see de Vernal et al., 1997, and references therein), allowing comparison with the known ecology of cysts referred to above. While the TFM itself is not reliant on ecological interpretations, its scientific value would be increased if ecological credibility could be shown. Comparison between the two, in fact, shows just the opposite: a widening credibility gap. A fuller discussion of this topic is presented elsewhere (Dale, B. and Dale, A.L., in press), and will not be repeated here. Nevertheless, it may be of interest to plankton biologists to consider the main points of contention. The transfer functions used for cysts are largely based on the same data set of assemblages from surface sediments in the northern North Atlantic, and the following points should be considered: 1) many of these samples are from the deep sea, and almost all of the others from exposed offshore sites – cyst assemblages therefore probably reflect long distance transport, rather than local representation; 2) the assemblages include many well known coastal species – seemingly confirming the influence of transport; 3) most of the cysts commonly frequent in the assemblages represent species with well documented broad tolerance levels for water and salinity – suggesting no ecological basis for their use to distinguish the relatively small differences estimated from the TFM; 4) if the cysts are presumed to be in situ, as in the TFM, the main conclusion that they somehow reflect environmental parameters (e.g. temperature, salinity, and ice cover) in winter, when presumably they would be dormant, seems particularly unrealistic; and 5) nutrition, and other environmental factors known elsewhere to be more important for determining the composition of cyst assemblages are generally not considered. We have appealed for a more ecological-based approach to the paleoecological use of cysts and other microfossils, using modern statistical methods (correspondence analysis) developed for terrestrial ecology (Dale, A.L and Dale, B., in press). However, it will probably require a scientific effort corresponding to that already invested in the TFM for such methods to produce similarly detailed data as required by the modelers; if indeed it is realistic to produce such data. In the meantime, micropaleontology will continue to feed in estimates of sea surface temperature and salinity (for February and August) and sea ice cover from records of up to many tens of thousands of years, based on the TFM. This topic is raised, here, because our assessment suggests that, at 268 B. DALE

least for dinoflagellate cysts, the detailed estimates of environmental parameters lack ecological credibility, such that other (as yet unknown) factors must be invoked to explain the established statistical correspondence, if this is to be believed. Some of our criticism pertains especially to the cysts (e.g.the transport problem, and environmental responses during dormancy). Other groups such as planktic foraminifera, which at least are unquestionably pelagic, may be reliable indicators of the estimated paleo-data produced, but as with the cysts, this should be tested against real ecology if possible. Marine biology could be playing a much more active role in this respect, and future work should be targeted to thoroughly investigate the living ecology of the relevant groups for oceanic micropaleontology (dinoflagellates, diatoms, foraminifera, and radiolaria), and provide input to what otherwise would amount to paleontology in biological limbo. Environmental sciences The developing role of dinoflagellate cysts in environmental sciences (discussed above) certainly raises questions of interest to marine biology. We are well on the way towards developing the cysts as state of the environment indicators with respect to eutrophication, although as yet this is based on relatively few examples. The cyst signals we utilize seem to be both valid (e.g. occurring at different times in the same region, and therefore not climatic) and robust (i.e. both increasing and decreasing in tact with pollution). However, much fundamental work is still needed to understand the underlying biological basis for these signals. In many ways, the results from the Oslofjord seem straightforward, and at least provide both signals and explanations for these that should be easy to test against future case studies. Using the Oslofjord example as a model for cultural eutrophication in nutrient limited systems suggests two particular implications for future work: the need to test and develop the method, and implications for studies of blooms (discussed in the next section). The cysts in sediments offer a powerful method for tracing the development of cultural eutrophication in nutrient limited systems; the method should now be field tested elsewhere with emphasis on documenting which particular species benefit from the extra nutrients, and therefore contribute to the local signal. The species important in the Oslofjord signal, Gonyaulax polyedra, is a warmer cosmopolitan

species (equatorial through temperate waters, globally), and therefore a likely candidate also as a summer bloom species elsewhere, at least within the temperate zones. Furthermore, this species also occurs as a prominent member of the plankton in somewhat nutrient enriched neritic waters associated with upwelling systems (e.g. off California, and North West Africa), suggesting the possibility of a more basic link to nutrients than just being a late summer bloomer in the Oslofjord. The cyst signal for cultural eutrophication in systems not considered to have been nutrient limited prior to human impact is less well understood. The elements of the signal are clear: a proportional shift to more heterotroph representation in the cyst assemblages, with no marked increase in cyst concentration in the sediments. This suggests fundamental changes in the species composition of the plankton, rather than increased overall production, as the main effect of increased nutrients (a point of particular interest for plankton biology). The fact that this signal parallels that previously described for oceanic upwelling, strongly suggests this to be a nutrient signal (Dale, 2000), but the underlying details of which species benefit and which species (or groups of organisms) suffer adverse effects remain to be discovered. The explanation suggested by Thorsen and Dale (1997) and Matsuoka (1999), that extra nutrients produce more diatoms as prey for the heterotrophic dinoflagellates, is not fully supported by the evidence. For the proportional increase noted in the cyst assemblages to represent increased production of heterotrophic dinoflagellates (from increased prey), this should also be reflected by increased production of their cysts (cysts/g sediment), which seems not to be the case. However, much of the evidence so far is complicated by the fact that the sites studied are also subjected to massive industrial pollution, including possibilities for increased sediment loads, and this aspect of the signal should become clearer from ongoing studies of other, less polluted, sites. Future work should also test the possibilities for using the eutrophication signal quantitatively. The main question to be answered, here, as elsewhere in cyst-based studies, is just how representative is the cyst record of dinoflagellates, or even of the plankton as a whole. On first consideration, the possibilities for quantitative representation seem limited, but it is interesting to note that the approximate doubling of cyst production in the innermost Oslofjord seems to compare reasonably with other indications

of eutrophication. Meanwhile, using the signals semi-quantitatively should prove useful for tracing the development of eutrophication. Environmental management decisions could thus be helped by indications of the state of eutrophication relative to preimpact levels, and of suggestions as to whether eutrophication is increasing or decreasing. Current work using the cyst signals to test suggested links between eutrophication and the collapse of local fisheries (Sætre and Dale, 2001) is providing two converging lines of evidence that could prove to have important implications for both plankton biology and fisheries biology. Eutrophication has been suggested as a possible cause of the collapse of some local fisheries in Norway, involving a postulated deterioration in the quality of food available for early growth stages in the fish. If, as first results suggest, this coincides with cyst signals of eutrophication based on a fundamental shift in species composition of the plankton, these could be pointing to the same changes in plankton also ultimately affecting the fish. Blooms: the view from below There are many areas within the very active field of HAB research where dinoflagellate cysts can provide useful “building blocks” for future work. The most immediate need is for standardized methods for measuring cysts in sediments. Attempts to model bloom dynamics have revealed the need to consider living cysts in bottom sediments as seed beds, and quantify this (numbers of viable cysts hatching to start a bloom). The evidence suggests this to apply to only some HAB species which may be grouped as follows with respect to seed beds (Dale and Amorim, 2000): 1) those lacking resting cysts (e.g. Gymnodinium breve in Florida); those heavily dependent on cysts as seed beds (e.g. Alexandrium tamarensis in higher latitudes); and 3) those producing cysts without mandatory resting periods, and therefore not forming seed beds (e.g. Gymnodinium catenatum from southwestern Europe and northwestern Africa). Attempts to measure viable cysts in sediments will have to take account of a combination of biological and sedimentological factors. It may not be immediately obvious to a biologist or a sedimentologist how a seed bed in rapidly accumulated, coarser grained sediment (with a lower number of cysts/unit of sediment) may be capable of delivering more motile cells/l to overlying waters than a finer grained example with a much higher cyst concentration. DINOFLAGELLATE CYSTS 269

New toxins and harmful cyst-forming species continue to be discovered, and cysts may be expected to similarly be involved in future discoveries. Two recent examples suggesting future work are of particular interest here: toxins in the cosmopolitan cystforming species Protoceratium reticulatum and L. polyedrum (e.g. see references in Reguera et al., 1998), and the new discovery of toxins for the first time within the genus Protoperidinium. The presence of diarrhetic shellfish poison (DSP) toxins in these two cosmopolitan species has several implications for future HAB research: on the one hand, these produce fossilizable cysts, allowing us to trace the history of past blooms, but also they are dominant members of many cyst assemblages world-wide, in large amounts that could represent sizeable toxin sinks in sediments. The new discovery by Professor T. Yasumoto (personal communication, work in progress) of toxins in a species of Protoperidinium from Ireland is particularly significant: this is one of the largest genera, and may now be expected to contain other toxic species awaiting discovery. From Prof. Yasumoto’s description of the motile cells of this species, I was able to recognize a corresponding cyst type from my previous unpublished incubation records; this in turn allows us to seek for this cyst in our global database of recent assemblages, suggesting other localities where this species could cause HAB problem (Dale and Yasumoto, work in progress). One of the most important areas for future applications of cyst work in HAB (and other bloom) research will involve drawing together some of the various lines of research discussed up to now in this contribution, to explore how these may contribute to better understanding future blooms. This is discussed under its own heading in the following section combining ideas on the future blooms themselves, and the ways they can be studied.

LOOKING BACK INTO THE FUTURE OF BLOOMS AND BLOOMING RESEARCH The research The harmful component of harmful algal blooms (HABs) refers to effects concerning humans. This means that whereas scientific resources are understandably concentrated on HABs, out of concern for human needs, the scientific need is to better understand plankton blooms as such. Apart from the amount of plankton accumulated to constitute a 270 B. DALE

bloom (or its impact on humans in the case of HABs), one of the main factors unifying most blooms is that they are episodic. Species may bloom at a given site with frequencies varying from almost annually (few) to up to tens of years (scientific records do not allow us to consider more). Episodic phenomena with such frequencies are among the most difficult to study, not least because scientific funding tends to be correspondingly episodic. Long term monitoring is arguably the most effective (only?) way to build up sufficient data to address the central questions of why and how certain species periodically bloom where and when they do, as shown by the record of HAB research. Within the past 35 years, HAB research has developed into one of the larger applications of resources in marine biology, fueled by concerns for public health and the commercial interests of fisheries and tourism. The stated primary aims of this research have been to understand, and eventually predict HABs. Looking back over 35 years of research therefore allows us to compare research strategies and to evaluate progress. My personal long term monitoring of research in this field suggests the folowing main conclusions: 1) we still have a lot to learn regarding both understanding and particularly prediction; 2) the most consistent progress has come from research based on long term monitoring, notably in the Seto Inland Sea, Japan, and especially Florida, where records now allow recognition of the combined influence of hydrogrological and meteorological conditions; 3) much other research may be characterized as chasing blooms (i.e. applying often hastily assembled resources to investigate blooms already developing in the field); and 4) experimental work, together with research under 3 above, has however, produced many useful “building blocks”. I believe we would have greater understanding of blooms, today, if more resources had been applied to long term monitoring. Future work should consider the proven value of long term monitoring before dismissing it, perhaps, as unrealistic for the modern world. In any case, it may prove unrealistic to continue along the lines of research covered by points 3 and 4 above, without spending much more collective effort on focussing and integrating the information produced more towards understanding the basic phenomena of blooms. From the literature, and e.g. listening to presentations at the international conferences on HABs held every few years, I sense that bloom research is in danger of losing touch with its own stated goals. Under the general heading of HAB

research, it is accepted that a wide spectrum of specialist research contributions seem increasingly to dig deeper into their own sub-discipline of science without relating to more than the nearest other one. The danger is that increased isolation of sub-disciplines within the auspices of a larger topic of public concern ultimately may lead to the sort of credibility gap experienced by the paleoceanographers (discussed above). This point is raised here for consideration by the would-be-sages, as an example of the difficult decisions that have to be made in research, and the longer-term consequences involved. It is not possible to discuss this as fully as it deserves, here, but at least I feel that in mentioning such things, I am to some extent meeting the appeal for “candid, honest and open dialogue” requested by the organizers of this meeting. However, having appealed so fervently for focussing the detailed sub-disciplines, I should return to integrating the cyst work. The blooms One of the fundamental concerns expressed in HAB research is that cultural eutrophication may be causing a global epidemic of HABs (Smayda, 1990). One of the goals of future research on blooms therefore must be to investigate the possible effects of eutrophication and other human activities (including climate change). I hope to have shown, here, that some of the main lines of dinoflagellate cyst research in fact cover these same concerns. This allows us to consider implications from the cyst work both for future blooms and for future studies of blooms. Cyst work described above suggests that cultural eutrophication could cause increased blooms in the future, particularly of summer blooming species in nutrient limited systems of the temperate zones or higher latitudes. The species most affected in the Oslofjord was G. polyedra (= L. polyedricum), now known to produce DSP toxins, but other species may be expected to produce similarly increased blooms in other regions. We know insufficient detailed information regarding the effects to be expected on blooms from eutrophication in non nutrient limited systems, but the cysts suggest strong possibility for disruptive changes in plankton composition that could threaten fisheries. The cyst work relevant to climate change (referred to above) allows us to estimate to some extent the predicted changes to be expected from global warming. Again, the temperate zones and

higher latitudes may be expected to be most affected by increased temperature: involving marked increases in the warmer water species occurring towards their colder limits in any given region, today (comparable to the fossil blooms of G. nolleri described from previous warmer periods in the Kattegat- Skagerrak). Knowledge of the detailed biogeographic zones mapped out from cyst distribution studies should enable us to identify at least the cystforming species likely to increase. Other kinds of environmental change associated with climate may well affect the warmer zones (e.g. the massive runoff of large amounts of freshwater and mud from large storms in the past few years may represent one of the most disruptive influences on plankton and cysts in sediments along the Portuguese Coast). One of the most pronounced effects of climatic change and various forms of human pollution indicated by the cysts, is an initial spike (from blooms) of P. reticulatum. This most likely represents an opportunistic reaction by this cosmopolitan species to environmental change: of particular interest, now, since this species, too, is known to produce DSP toxins. Cyst analysis of bottom sediments should prove to be a particularly useful method for tracing future changes as they develop. We are already exploring this to trace the joint history of eutrophication (using the eutrophication signal) and toxic blooms of a species, Pyrodinium bahamense, with a fossilizeable cyst (in Manila Bay, The Philippines, in cooperation with Dr. R.V. Azanza). In our work in Norwegian fjords, we are already picking up the first indicators of the present warming trend, and the results serve as a reminder of the need to observe the details in nature with an open mind: they show a marked increase in the colderwater species P. faeroense! Closer examination of the temperature data most likely provides the answer: the consistent measured warming trend in sea surface water temperatures from southern Norway during the past ten years concerns only the winter temperature, summer temperatures are so far not affected. In effect, this allows normal spring temperatures to occur much earlier than otherwise, and extends the spring temperature window by between one and two months. P. faeroense is a colder water species occurring towards the warmer limit of its biogeographic zone in these waters, where it blooms in spring. It is thus most likely to have increased its production in the spring bloom during the past ten years, and contributed correspondingly more cysts to the sedimentary record. DINOFLAGELLATE CYSTS 271

ACKNOWLEDGEMENTS Many different sources of funding have helped us carry out this work over many years. Thanks are particularly due the following for financial support: The Office of Naval Research, and The National Science Foundation in the USA (earlier work at Woods Hole Oceanographic Institution); BP International Ltd., U.K., and BP Petroleum Development Norway (initial global cyst study); the AASP-initiated Palynological Research Consortium: Amoco, Norsk Hydro, Phillips, STATOIL, Elf and UNOCAL (a further four years funding for the study); and the Research Council of Norway (current studies on eutrophication and fisheries). I thank: my dear wife Amy for critical reading and help with figures; the personnel of the Graphics and Photography Department of the Mathematics and Natural Sciences Faculty, University of Oslo, for help with illustrations; and Maria L.L. Sætre, Robert W. Williams and Gordon D. Wood, for kindly allowing me to use their photographs in Figure 1. Finally, I wish to thank Anna Dale and Elise Dale for inspiration that only inquisitive young children can give –I hope that one day this article may help to answer your probing questions about what Pappa really does.

REFERENCES Brasier, M.D. – 1980. Microfossils. Allen and Unwin, London. Dale, B. – 1978. Acritarchous cysts of Peridinium faeroense Paulsen: implications for dinoflagellate systematics. Palynology, 2, 187-193. Dale, B. – 1983. Dinoflagellate resting cysts: “benthic plankton”. In: G.A. Fryxell (ed.), Survival Strategies of the Algae, pp. 69136. Cambridge University Press, Cambridge. Dale, B. – 1996. Dinoflagellate cyst ecology: modeling and geological applications. In: J. Jansonius and D.G. McGregor (eds.), Palynology: Principles and Applications, pp. 1249-1275. AASP Foundation, Vol. 3. Dale, B. – 2000. Dinoflagellate cysts as indicators of cultural eutrophication and industrial pollution in coastal sediments. In: R.E. Martin (ed), Environmental Micropaleontology, 305-321. Kluwer Academic/Plenum publishers, New York. Dale, B. – 2001. Marine dinoflagellate cysts as indicators of eutrophication and industrial pollution: A discussion. Sci. Total Environ., 264: 235-240. Dale, B. and A. Amorim. – 2000. Dinoflagellate resting cysts as seed beds for harmful algal blooms. Ninth International Conference on Harmful Algal Blooms, Abstract. Dale A.L. and Dale, B. – (in press). Appendix on statistical methods. In: S. Haslett, (ed.), Quaternary Environmental Micropalaeontology. Arnold Ltd., London. Dale, B., and A.L. Dale. – (in press). Environmental application of dinoflagellate cysts and acritarchs. In: S. Haslett (ed.), Quater-

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nary Environmental Micropalaeontology. Arnold Ltd., London. Dale, B., T.A. Thorsen and A Fjellså. – 1999. Dinoflagellate cysts as indicators of cultural eutrophication in the Oslofjord, Norway. Estuar. Coast. Shelf Sci., 48: 371-382. Evitt, W.R. – 1963. A discussion and proposals concerning fossil dinoflagellates, hystrichospheres, and acritarchs, I. Proc. Nat. Acad. Sci., 49: 158-164. Fensome, R.A., F.J.R. Taylor, G. Norris, W.A.S. Sarjeant, D.I. Wharton and G.L. Williams. – 1993. A classification of living and fossil dinoflagellates. Micropaleontology, Special Publication, 7: 1-351. Hammen, T. Van Der, T.A. Wijmstra and W.H. Zagwijn. – 1971. The floral record of the Late Cenozoic of Europe. In: K.K. Turekian (ed.), The Late Cenozoic Glacial Ages, pp. 391-424. Yale Univeristy Press, New Haven, USA. Imbrie, J. and N.G. Kipp. – 1971. A new micropaleontologial method for quantitative paleoclimatology: Application to a Late Pleistocene Caribbean core. In: K.K. Turekian (ed.), The Late Cenozoic Glacial Ages, pp. 71-181. Yale University Press, New Haven, USA. Jannasch, H.W. – 1997. Small is powerful: recollections of a micropbiologist and oceanographer. Ann. Rev. Microbiol., 5. Matsuoka, K. – 1999. Eutrophication process recorded in dinoflagellate cyst assemblages – a case of Yokohama Port, Tokyo Bay, Japan. Sci. Total Environ., 231: 17-35. Moldowan, J.M. and N.M. Talyzina. – 1998. Biogeochemical evidence for dinoflagellate ancestors in the early Cambrian. Science, 281: 1168-1170. Reguera, B., J. Blanco, M.L. Fernández and T. Wyatt (eds). – 1998. Harmful Algae, Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO. Smayda, T. – 1990. Novel and nuisance phytoplankton blooms in the sea: evidence for a global epidemic. In: E.Graneli, B. Sundstrøm, L. Edler and D.A. Anderson (eds), Toxic Marine Phytoplankton, pp. 29-40. Elsevier, New York. Stover, L.E., H. Brinkhuis, S.P. Damassa, L. de Verteuil, R.J. Helby, E. Monteil, A.D. Partridge, A.J. Powell, J.B. Riding, M. Smelror and G.L. Williams – 1996. Mesozoic-Tertiary dinoflagellates, acritarchs and prasinophytes. In: J. Jansonius and D.G. McGregor (eds.), Palynology: Principles and Applications. American Association of Stratigraphic Palynologists Foundation, 2: 641-750. Sætre, M.L.L., B. Dale, M.I. Abdullah and G.-P. Sætre. – 1997. Dinoflagellate cysts as possible indicators of industrial pollution in a Norwegian fjord. Mar. Environ. Res., 44(2): 167-189. Sætre, M.L.L. and B. Dale. – 2001. Dinoflagellate cysts in sediment cores as indicators of cultural eutrophication in Norwegian coastal waters. This Meeting, Abstract. Taylor, F.J.R. (ed). – 1987. The Biology of Dinoflagellates. Botanical Monogr., 21. Thorsen, T.A. and B. Dale. – 1997. Dinoflagellate cysts as indicators of pollution and past climate in a Norwegian fjord. The Holocene, 7(4): 433-446. Thorsen, T.A. and B. Dale. – 1998. Climatically influenced distribution of Gymnodinium catenatum during the past 2000 years in coastal sediments of southern Norway. Palaeogeogr. Palaeoclimatol. Palaeoecol., 143: 159-177. de Vernal, A., A. Rochon, J.-L. Turon and J. Matthiessen. – 1997. Organic-walled dinoflagellate cysts: palynological tracers of sea-surface-water conditions in middle to high latitude marine environments. GEOBIOS 30: 905-920. Wall, D. and B. Dale. – 1966. “Living fossils” in Western Atlantic plankton. Nature, 211: 1025-1026. Wall, D. and B. Dale. – 1968. Modern dinoflagellate cysts and evolution of the Peridiniales. Micropaleontology, 14: 265-304. Wall, D., B. Dale, G.P. Lohmann and W.K. Smith. – 1977. The environmental and climatic distribution of dinoflagellate cysts in Modern marine sediments from regions in the North and South Atlantic Oceans and adjacent seas. Mar. Micropaleontol., 2: 121-200.

SCI. MAR., 65 (Suppl. 2): 273-281

SCIENTIA MARINA

2001

A MARINE SCIENCE ODYSSEY INTO THE 21st CENTURY. J.M. GILI, J.L. PRETUS and T.T. PACKARD (eds.)

Unnatural Oceans* JEREMY B.C. JACKSON1,2 and ENRIC SALA1 1

Scripps Institution of Oceanography, University of California, San Diego, La Jolla, California 92093-0244, USA. 2 Center for Tropical Paleoecology and Archeology, Smithsonian Tropical Research Institute, Box 2072, Balboa, Republic of Panama.

SUMMARY: Ecological understanding of the oceans is based on an unnatural mix of mostly small species whose trophic relations are distorted to an unknown degree by the overfishing of megafauna including sharks, sea turtles, sea cows, seals, and whales. Living habitats like seagrass beds, kelp forests, and coral reefs that once provided critical 3-dimensional habitats for refuge and reproduction of most of the biodiversity of the oceans are also greatly reduced by fishing and other factors. Successful restoration and conservation require a more realistic understanding of the ecology of pristine marine ecosystems that can only be obtained by a combination of retrospective analyses, modeling, and intensive studies of succession in very large marine reserves. Key words: overfishing, food webs, biological habitat, body size, historical ecology.

INTRODUCTION Like many others growing up in the 1950s, the senior author marveled at the books and films of Jacques Cousteau and watched television melodramas like Sea Hunt. Amongst the wonders of marine biology, underwater archeology, and intrigue were myriad renditions of frightening adventures with giant sharks, octopus, and “man-eating” clams that have indelibly permeated the popular culture of the oceans to this day. It was, therefore, a genuine personal surprise that he very rarely saw large sharks or large fishes of any kind when he began scientific diving around the Caribbean in 1968; and had to wait until a trip to Truk in the western Pacific the following year to see sharks in any abundance. Now, western Pacific coral reefs and seagrass meadows *Received August 9, 2001. Accepted August 16, 2001.

look increasingly like the Caribbean and scientists are finally waking up to the extraordinary magnitude of the ecological changes on coral reefs and all other marine ecosystems that have been wrought by overfishing (Wilkinson 1992; Hughes 1994; Dayton et al., 1995; Botsford et al., 1997; Jackson, 1997, 2001; Dayton et al., 1998; Jackson et al., 2001; Steneck and Carlton, 2001). Alarm about the collapse of coastal ecosystems worldwide and loss of marine biodiversity has brought about many promising initiatives for conservation and management (Palumbi, 2001; Peterson and Estes, 2001). However, our basic concepts about the ecology of pristine marine ecosystems have hardly been questioned, even though most of our textbook wisdom was obtained long after intensive fishing began. Margalef (1968) observed that fishing reverses ecological succession and explored theoretically the implications for the productivity of UNNATURAL OCEANS 273

ecosystems subjected to varying levels of exploitation. Today, Margalef’s prescience is all too apparent in the replacement of Caribbean reef corals by benthic algae (Lessios, 1988; Hughes, 1994), of temperate kelp forests and other fleshy algal communities by “sea urchin barrens” of crustose coralline algae (Estes and Palmisano, 1974; Simenstad et al., 1978; Dayton et al., 1998; Sala et al., 1998; Steneck and Carlton, 2001), the eutrophication of coastal estuaries (Officer et al. 1984; Elmgren, 1989; Nixon, 1995; Jonas, 1997), and the relentless global fishing down of marine food webs (Pauly et al., 1998). However, we still lack the basic data for a general theory of the relationships between productivity, biomass, and the degree of exploitation in marine ecosystems that seems essential for rational conservation, restoration, and management. An important step in the development of any theory is an examination of the basic assumptions. Here we briefly review our understanding of three basic themes in the ecology of marine ecosystems in the light of increased awareness of the magnitude and consequences of overfishing. The purpose is to question common generalizations about the composition and structure of pristine marine ecosystems that were formulated long after extensive exploitation began. Building more realistic models of pristine marine ecosystems, to the extent this is possible, will require detailed paleoecological, archeological, and historical analyses to determine what and how much was present, combined with observations and manipulations of succession due to the absolute cessation of human exploitation within very large marine protected areas. Such investigations have hardly begun for any marine ecosystem.

BODY SIZE Most species of a higher taxon of free-living animals like mammals, birds, snails, and clams are small compared to the total range in size for the group (May, 1988, 1990, 1994; Brown, 1995). The number of species scales very approximately with decreasing characteristic body length, L, as L-2, or for body mass, M, as M-2/3. Moreover, the ancestral species in a clade are also generally small and lie near the apparent physiologically or biomechanically minimum functional body size for the group (Stanley, 1973). Thus, body size tends to increase over macroevolutionary time, whether by simple 274 J.B.C. JACKSON and E. SALA

evolutionary diffusion from smaller to larger size, or because of adaptive trends associated with evolutionary arms races that actually favor larger species (McShea, 1994, 2000; Vermeij, 1994). Thus, ignoring for the moment the problems of bycatch and indirect ecological effects, selective fishing of large species should affect directly only a very small proportion of the total species diversity of a clade - although more evolutionarily derived species, to the extent that they are larger, should tend to be affected more than ancestral groups. If we look beyond diversity, however, to consider the ecological roles of species, the picture is dramatically different because large animals directly affect ecosystems in profoundly different ways than small animals that go well beyond Pieter Bruegel’s famous pictorial maxim that “big fish eat little fish.” Big animals not only eat much more than smaller animals, but they also physically disturb the habitat by their feeding and behavior in ways impossible for smaller species (Jackson, 1997, 2001). The best documented examples come from East Africa where elephants rip apart forests and vast herds of migrating wildebeest affect the abundance, composition, and nutritional value of the vegetation by their grazing and trampling in ways that affect all the other animals on the plains (Sinclair and Arcese, 1995). Comparably detailed observations are unavailable for most marine ecosystems for the simple reason that most of the big animals were gone before marine ecology began; and that, tragically, there are no marine parks equivalent to the Serengeti where large animals live their entire lives in vast areas that are mostly well protected from human exploitation (Sinclair and Arcese, 1995). Nevertheless, we can still make a list of cases for which there is reasonable evidence that large marine species had comparably dramatic effects in coastal ecosystems (Jackson et al., 2001, Table 1). In contrast, we have almost no idea of the magnitude of the ecological consequences in the open oceans of feeding by formerly abundant baleen whales, swordfish, tuna, and the like. There is no clearer measure of our ecological ignorance of the animals in Table 1 than their virtual absence from the index of the most recent textbook on marine community ecology (Bertness et al., 2001), except for discussions of the geological history of the biota or of human disturbance, conservation, and management. There is an enormous bias towards the study of small species that swell the index of the same textbook, even when larger

TABLE 1. – Some of the ecologically extinct large animals that were keystone species in pristine coastal ecosystems and their ecological effects. For more extensive discussion and references see Jackson et al. (2001). Species

Ecological consequences

References

Seagrass meadows and soft sediments Green turtles Manatees and dugongs Skates and rays

Closely crop turtlegrass and other seagrasses and reduce flux of organic matter to sediments Excavate, break apart, and consume up to 96% of above ground biomass and 71% of below ground biomass of seagrasses Excavate seagrass beds and sediments forming pits of bare sediment for feeding and camouflage

Jackson 1997 Preen1995 Orth 1975, VanBlaricom 1982

Coral reefs Tiger sharks Monk seals Parrotfish Hawksbill turtles Jewfish

Consume large fishes and sea turtles, among others Consume fish Graze directly on coralline substrata including live corals and coralline algae Feed upon and break apart large sponges Consume lobsters, other invertebrates, and fishes

De Crosta 1981 Polovina 1984 Steneck 1983 Meylan 1988, van Dam and Diez, 1997 Randall 1983

Kelp forests Cod, sheephead, and sea otters Consume sea urchins, other benthic invertebrates, and fishes Seals and sea lions Stellar’s sea cow

Consume fish Consumed kelp canopies or intertidal seaweeds

species are still reasonably abundant as on the Great Barrier Reef in Australia. Yet, even in Australia, as for the Caribbean, almost all of the experiments on reef fish recruitment, and the ensuing controversy about the determinants of coral reef fish community structure, including the importance of chance events, competition, and predation, are based on short-term studies of fishes less than 10 cm long (Sale, 1991; Morgan, 2001); and the same is true of other benthic communities. The implications extend far beyond academic ecology, however, because our expectations about the potential recovery of larger species of reef fishes in marine reserves are heavily influenced by the only studies available (Dayton et al., 1998; Palumbi, 2001).

GEOMETRY OF FOOD WEBS One large tiger shark weighs roughly the same as one hundred large groupers, snappers, or parrotfish; or ten thousand damselfish or small wrasses – the species that have been the overwhelmingly favorite subjects of study by coral reef ecologists (Sale, 1991). What percentage of the total free-living animal biomass of pristine ecosystems was comprised of megafauna, such as the species in Table 1, compared to smaller species like damselfish, wrasses, shrimps, and brittlestars? Moreover, what was the

Estes and Palmisano 1974, Steneck and Carlton 2001, Dayton et al. 1998 Wells et al. 1999 Jackson et al. 2001

effect of the removal of megafauna on lower trophic levels? Recent empirical studies of reefs subjected to varying degrees of fishing (but where the “large” predators are not really very large) suggest that the effects are minimal (Hixon, 1991; Russ and Alcala, 1998; Jennings and Polunin, 1997) whereas modeling studies strongly suggest the opposite (Polovina, 1984; Optiz, 1996; Aliñao et al., 1993; Sala and Jackson, unpublished). There are at least two great difficulties in trying to answer these questions. The first is that we cannot observe natural populations of marine megafauna today and will have to wait several decades to do so, even in well-managed, very large marine protected areas. The second problem is that the answers do not depend closely upon the ecological efficiency of energy transfer among trophic levels because of the great differences in generation times of larger and smaller species (Stevens et al., 2000; Jackson, 2001). Ages of first reproduction of sea turtles and many large sharks are measured in decades and their longevities presumably in centuries. Large groupers, sheephead, cod, and other large groundfish mature more rapidly but still live for decades. In contrast, smaller species of fishes and free-living benthic invertebrates typically mature within 1-2 years and live only a few years; and the comparable statistics for most zooplankton are measured in months. Thus vertebrate megafauna could have collectively outUNNATURAL OCEANS 275

TABLE 2. – Comparison of the vertebrate and invertebrate animal faunas of French Frigate Shoals and Bolinao (Polovina 1984, Aliñao et al. 1993). Biomass data are metric tons/km2. Faunal Component Megafaunal vertebrates* Other vertebrates Total vertebrates Invertebrates

French Frigate Shoals

Bolinao

0.61 15.90 16.51 171.35

0 6.83 6.83 351.95

* monk seals, green turtles, sharks, jacks, scombrids

weighed their prey and other species down the food chain by the long-term accumulation of biomass, but there are virtually no biomass data from pristine ecosystems to tell. The only food web for a quasi-pristine coral reef ecosystem is from French Frigate Shoals in the remote western Hawaiian chain, which we compared with a heavily overfished site at Bolinao in the Philippines (Polovina, 1984; Aliñao et al., 1993, Table 2). The total vertebrate biomass/km2 at French Frigate Shoals is 2.4 times greater than at Bolinao. This difference is statistically significant (one sample test, χ2 = 4.02, P80% on the English and French Channel coasts (Ockelmann, 1962). If this should hold true, nailing down Thorson and Mileikowsky to their use of the term pelagic (instead of planktotrophic) larvae would be splitting hairs, because the latter is what Thorson originally meant. However, as we will show below, we are only slowly approaching reliable estimates of species richness in many taxa for different regions, and it may take a long time before we can provide the percentages required for a meaningful discussion. Our conclusion is that we have to be very modest at this time judging on the validity of a latitudinal gradient in larval strategies as claimed by Thorson’s rule. “Faunal species richness in the Southern Ocean should be low obeying to the bell-shaped curve of species distribution from the tropics to the poles” The paradigm of a bell-shaped distribution of benthic species richness along the latitudinal gradient, with high values at low latitudes decreasing towards low values at high latitudes, may be much older than its literature record. Any visitor to the tropics coming from cold or temperate regions is impressed by the richness of mollusc species scattered on many tropical beaches and the diversity of life forms in a coral reef. Furthermore, there seems to be a distinct gradient on the terrestrial side, from rich rain forests to the barren permafrost soils and snow-covered landscapes in polar regions. On the other hand, some marine taxa such as macroalgae clearly do not attain their maximum species richness in the tropics (Warwick 1995). So the subject has been under discussion for some time (see, e.g.

Clarke 1992 b; Arntz et al., 1997; Crame 2000a,b; Gray 2001a,b). Before turning to recent observations in the southern hemisphere which might shed some new light on the subject, we would like to ask a nasty question: Why should there be a latitudinal gradient at all? Latitude by itself is not an ecofactor. Stable day length as opposed to a highly variable light regime during the year, warm water vs. cold water, continuous low production vs. seasonal production pulses, predominantly benign conditions vs. frequent and drastic physical disturbance - are these characteristics of tropical regions (as compared to those of higher latitudes) necessarily inducing higher biodiversity? Obviously calcification is favoured in warm water, and the long existence (not the stability) component of Sanders` stability-time hypothesis may have been favourable for the development of co-existence of many species in the tropical warm water belt, which is much older than either polar region (Crame 2000a), but that is about all we know. On the other hand, along all continents except the Antarctic (where circumantarctic conditions are essentially the same) environmental conditions vary to an extent which makes valid comparisons very difficult. For example along the South American Pacific and Atlantic coasts, conditions are similar (tropical) only in the extreme north. Tropical conditions, modified by enormous river runoff prevail off Brasil. Conversely, the Humboldt current upwelling off Peru and the northern half of Chile combines cool water and very high surface- and shallow-water productivity (but moderate species richness) with an extensive oxygen minimum zone between 30 and 700 m depth, where prokaryotic sulfur bacteria are almost the only life, contrasting with well-oxygenated waters off Uruguay and Argentina. Further south, the highly complex Chilean fjord system with interchanging rocky coasts and sandy beaches, and strong input from inland glaciers, has no counterpart on the Argentinian Atlantic coast although rocks may prevail there in shallow water, as well. There is no reason whatsoever to expect simultaneous latitudinal changes in shallow-water species richness along the two coastlines. The same is true for comparisons within many areas of the tropics, where barren sandy beaches and hypersaline lagoons, both governed by strong environmental fluctuations and characterized by very low species richness, contrast with coral reefs and subtidal bottoms which represent the other extreme. A second problem which impedes valid comparisons is the methodology applied by investigators all

over the world, not only the use of totally different equipment (Warwick, 1995; Arntz et al., 1997) but also the use of inappropriate scales, insufficient data volume and inadequate analytical methods (Gray, 2001a,b). This problem, despite its being well documented in the literature, has hitherto caused very little change in behaviour, badly needed if comparisons are to improve. This is why we will mostly use overall regional species numbers compiled from the literature, which may represent the most reliable data at present. What do we know about species richness in the southern hemisphere, especially in the Antarctic and the regions close to it, and how do these compare with other regions? The investigators who contributed to creating the concept of the bell-shaped curve, e.g. Sanders (1968, soft-bottom macrobenthos); Thorson (1957, hard-bottom epifauna, esp. gastropods), and Stehli et al. (1967, bivalves), based their idea –as did many others following them– on very small sample sizes (Gray, 2001a) and had no data available from the extreme south. These have been accumulating during the last few decades, as can be seen from the increase of species numbers presented successively for various macrobenthic groups by Dell (1972: Table I), White (1984: Table III) and Arntz et al., (1997: Fig. 1.1 A). According to the latter compilation, the actually known number of macrobenthic invertebrates in Antarctic waters may be assessed at about 5000 (Gray 2001a: Table 2). This value has to be used with caution as it may be including, in many taxa, species living north of the Polar Front, i.e. in Subantarctic waters. For the eastern Weddell Sea alone (only shelf and slope) the EASIZ I cruise yielded about 1200 macrofaunal species by close cooperation among specialists on board and a thorough check of trawl catch remains by taxonomists of the St. Petersburg Zoological Institute (Gutt et al., 2000). The true number of species must be distinctly higher because towed gear is not an ideal instrument for this fauna. Still, this species richness appears to be in the same order of magnitude as that derived from larger studies in the North Atlantic (Gray 2001a: Table 1) and the Mediterranean Sea (Fredj and Laubier, 1985). Areas with a distinctly lower species richness are the Baltic (Arntz, 1971) and the North Sea (Daan and Mulder, 2000), and the Peruvian Humboldt upwelling (Tarazona et al., 1988; Tarazona and Valle, 1999). All these seas cover, however, a much smaller area. A CASE FOR TOLERANCE IN MARINE ECOLOGY 293

For the EASIZ III cruise a similar approach was used, yielding species number per trawl haul for the different groups. These data can be used for comparisons with other areas. Species number per haul was several times higher than in the Arctic Laptev Sea (Sirenko et al., 1997), the North Sea or the Baltic (own obs.). Species-area comparisons as those made by Gray (2001a: Table 1) represent (mainly?) infaunal communities. For the Weddell Sea shelf and slope and the Antarctic Peninsula we also have quantitative infaunal data from the multibox corer (Gerdes et al., 1992; Piepenburg et al., in press; Gerdes pers. comm.). These data provide additional information to the species-rich epifaunal communities of the high Antarctic, which contribute most to the total species number in that area. The taxonomic analysis of the infaunal data has not yet been completed, but our impression is that whereas species richness of the high Antarctic epibenthic communities is very high, that of infaunal communities in this area is much lower, and might yield quite a different picture in terms of a latitudinal cline. Around the Antarctic Peninsula the infauna is richer in biomass and, presumably, also in diversity (see, e.g. for polychaetes, Gallardo et al., 1988). A comparison with the area closest to the Antarctic and which separated last, the Magellan region, reveals that most taxa increase in species richness towards the Antarctic (for details see Arntz and Ríos, 1999), i.e. do not follow expectations if the bell-shaped curve was valid. This tendency is particularly obvious in sponges, bryozoans, polychaetes, peracarid crustaceans, pycnogonids and many echinoderms. For example amphipods, the most speciose macrofaunal taxon in the Southern Ocean, increase from (actually described) 232 species in the Magellan region to 391 in the Subantarctic and 531 in the Antarctic (De Broyer and Jazdzewski, 1996). On the other hand, some groups (hydrozoans, molluscs) reveal little difference between the two areas, and a few actually decrease (decapods, stomatopods, acorn barnacles). Barnes and De Grave (2001) studied the encrusting fauna along this gradient, which is not directly comparable with our data. As this is only the “tail” of the southern hemisphere curve, we might –still in very crude terms, i.e. total species registered– look further north. In two recent publications on bivalve species richness (Crame 2000a,b) confirmed the tropics as diversity centres of this group and centres of evolutionary innovation, but found the latitudinal clines less regular in form than was once imagined. In the south294 W.E. ARNTZ and J.M. GILI

ern hemisphere Australia forms a distinct diversity hotspot besides strictly tropical foci in the South China Sea, the Caribbean and the Panamic region in the Pacific. Crame stresses the importance of the historical context involving a warmwater history of at least 60 Ma, i.e. 2-3 times longer than the coldwater history of the Antarctic. At a recent macroecology meeting in Chile (summarized by Wieters, 2001) Roy stated that mollusc species richness along both coasts of the Americas is highest in the tropics, declining drastically poleward (to which latitude?). Conversely, Valdovinos et al. found mollusc diversity in the SE Pacific to increase dramatically south of 42°S due to greater habitat complexity. Litoral fish diversity again decreased south of 42°S for historical reasons (Ojeda). Finally, Fernández et al. emphasize that the larval type of invertebrates may influence species richness: those with planktotrophic larvae corresponded to the bell-shaped distribution along the Pacific coast whereas those without did not (for details see Wieters, 2001). The extraordinary complexity of the 4200 km Chilean coast (Fernández et al., 2000), mentioned already above, may explain in part the conflicting evidence for different taxa. Lancellotti and Vásquez (1999) refer to almost 1600 benthic species described for