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Glomeraceae and Gigasporaceae differ in their ability to form hyphal networks Introduction Recent studies have revealed that the Glomeraceae and Gigasporaceae differ in their capacity to link hyphae in the same mycorrhizal network (de la Providencia et al., 2005), while interconnection of different networks of the same isolate was demonstrated only with an isolate of Glomus mosseae (Giovannetti et al., 2004). As these results may have major implications for our understanding of how these obligate symbionts explore their environment, the question asked here is whether species of the Gigasporaceae also have the ability to interconnect different networks of the same isolate. Arbuscular mycorrhizal (AM) fungi can colonize a variety of plant species, and their lack of host specificity suggests that they can interconnect plants by means of a common mycelial network (Read, 1998; van der Heijden et al., 1998). These belowground networks have broad implications for resource allocation within the fungal colony, as well as for soil-derived nutrients and plant-derived carbon redistribution in ecosystems (Smith & Read, 1997). To date, it had been assumed that the principal route by which plants are interconnected was through extraradical mycelium spreading from mycorrhizal plants into the soil and colonizing the roots of plants with which they come into contact. Recently, Giovannetti et al. (2004) demonstrated that different mycorrhizal networks of the same isolate of G. mosseae may also become interconnected by anastomoses: ‘a mechanism by which different branches of the same or different hyphae fuse to constitute a mycelial network’ (Kirk et al., 2001). Different studies have illustrated that the capacity for anastomosis formation differs between species of the Glomeraceae and the Gigasporaceae (de Souza & Declerck, 2003; de la Providencia et al., 2005). In the Glomeraceae anastomoses were observed between different hyphae within the same mycelial network, while no anastomoses were detected within the same hypha (de la Providencia et al., 2005). This characteristic provides this AM fungal family with good plasticity to extend the extraradical mycelial network. In contrast, in the Gigasporaceae anastomoses were observed mainly within the same hypha (de Souza & Declerck, 2003; de la Providencia et al., 2005),

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generally related to a hyphal healing mechanism, while anastomoses between different hyphae of the same colony were far less abundant. This observation suggests a strategy based on the establishment of a large-diameter mycelium by means of the individual spreading of single hyphae forming the backbone of the colony (de Souza & Declerck, 2003). However, the question as to whether hyphae of Gigasporaceae species are able to interconnect different networks of the same species, in a similar way to G. mosseae (Giovannetti et al., 2004), remains unresolved and may have major implications for the capacity of AM fungi for rapid colony increase, exploration and exploitation of new environments and substrates, and creation of large networks. Here we report on the capacity of AM fungal isolates belonging to the Gigasporaceae and Glomeraceae to form anastomoses within and between extraradical mycelial networks of the same isolate. For this study, the monoxenic culture system was used, providing a nondestructive, three-dimensional visualization of the development pattern of the extraradical mycelium.

Experimental set-up Two organisms from the genus Glomus, one from Scutellospora and one from Gigaspora, were used for the experiment: isolate MUCL 43194 in the Glomus intraradices clade and isolate MUCL 41827 of Glomus proliferum; Scutellospora reticulata culture no. EMBRAPA CNPAB 1 and Gigaspora margarita BEG 34. Monoxenic cultures of the four organisms were established in association with Ri T-DNA-transformed carrot (Daucus carota) roots on the modified Strullu–Romand (MSR) medium (Declerck et al., 1998 modified from Strullu & Romand, 1986), solidified with 3 g l−1 GelGro (ICN Biomedicals Inc., Irvine, CA, USA) in quadri-compartmental culture plates 12.4 × 8.5 cm (each compartment 3.1 × 8.5 cm) (quadriPERM, Greiner Bio-One, Kremsmünster Austria) (Fig. 1). However, only three compartments were used, left (LC); central (CC) and right (RC), separated by plastic walls. The three compartments were connected through an opening (1 cm wide), cut from bottom to top of the plastic walls, separating CC from LC and RC. The two openings were cut at opposite sides. MSR medium (35 ml) was added to the culture plates, filling the three compartments. A transformed carrot root approx. 8 cm long was placed in the LC and RC and inoculated with AM fungal spores of the same organism. Inoculation of the roots with the four species was achieved following the methods described by Cranenbrouck et al. (2005). Culture plates were incubated in an inverted position at

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Fig. 1 Schematic representation of the quadri-compartmental culture system (plate 12.4 × 8.5 cm; each compartment 3.1 × 8.5 cm). Transformed carrot roots associated to an arbuscular mycorrhizal (AM) fungus developed in the left (LC) and right (RC) compartments on the MSR medium. After colonization of the host root and production of an extensive extraradical mycelium, hyphae passed through an opening in the partition walls and grew in the central compartment (CC). The anastomosis formation was assessed in the CC.

27°C in the dark. After profuse colonization of the root in the LC and RC, hyphae passed through the openings and developed in the CC. Roots that passed through the openings or over the partition walls, as well as hyphae crossing the partition walls, were trimmed. Six replicates were considered for each species that consisted of a culture plate with two side compartments (LC and RC) each containing a transformed carrot root inoculated with the same AM fungal species, and a CC where the extraradical mycelia were allowed to develop and contact each other. The culture plates used for the experiment were selected following three criteria: (1) the presence in the CC of the two mycelia intersecting each other; (2) approximately equal development of the two mycelial networks developing in the CC; and (3) total hyphal density within the CC of approx. 25 cm cm−3. Optimal culture plates (matching these three

criteria) were obtained within a period of 4–8 wk according to the AM fungal species. Different parameters were recorded in the CC: total hyphal length, hyphal density, and number and type of anastomoses. Total hyphal length and hyphal density were measured following the method detailed by Declerck et al. (1998). Three types of anastomosis were considered: (1) within the same hypha (hyphal bridge); (2) between different hyphae within the same mycelial network, originating from the same colony (from compartment LC or RC); and (3) between hyphae of the two intersecting mycelial networks developing from the LC and RC. To determine the presence and type of anastomosis, culture plates were observed under a stereomicroscope and a bright-field light microscope at ×10 to ×40, and ×50, ×125 or ×250 magnification, respectively.

Gigasporaceae do not interconnect different mycelia belonging to the same isolate Our data demonstrate for the first time that Glomeraceae and Gigasporaceae differ in their ability to interconnect different mycelial networks belonging to the same isolate. While hyphal fusions (anastomoses) were observed between hyphae from different mycelia of the same isolate with G. proliferum and G. intraradices, this mechanism was never observed with S. reticulata and G. margarita. The results on the abundance and type of anastomoses formed within the same mycelial network of both families further confirmed earlier work by de la Providencia et al. (2005). In cultures belonging to the Glomeraceae, 12.5–20.1% of anastomoses detected in the CC were formed between hyphae from the two different mycelial networks (Table 1; Fig. 2a–c). Anastomoses were always characterized by complete fusion of hyphal walls allowing bidirectional cytoplasmic/protoplasmic flow via the fusion bridge. These results corroborate the observations of Giovannetti et al. (2004), who observed interconnections between mycorrhizal networks of the same

Table 1 Growth parameters and percentage anastomosis formation of different nonperturbed networks of Glomus proliferum, Glomus intraradices, Scutellospora reticulata and Gigaspora margarita Growth parameters*

Percentage anastomoses†

Species

Hyphal length (cm)

Total no. anastomoses per hyphal length (cm)

In the same hypha

In the same network

Between networks

G. proliferum G. intraradices S. reticulata G. margarita

319.6 ± 26.8 a 390.3 ± 38.6 a 374.3 ± 49.6 a 415.5 ± 27.9 a

0.172 ± 0.024 a 0.086 ± 0.013 b 0.020 ± 0.001 c 0.009 ± 0.002 c

0.3 a 0a 94.7 b 95.5 b

79.6 a 87.5 a 5.3 b 4.5 b

20.1 a 12.5 a 0b 0b

Values represent means of six replicates (± SE for growth parameters). *Values of growth parameters in the same column followed by a different letter differ significantly at P < 0.05 (Tukey’s HSD). †Values of percentage anastomoses in the same column followed by a different letter differ significantly at P < 0.05 ( χ2 test for comparison of observed and expected values in contingency tables).

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Fig. 2 Anastomosis formation between two hyphae of different arbuscular mycorrhizal (AM) fungal networks of the same isolate of Glomus proliferum. (a) Two anastomoses were observed (square boxes). Bar, 50 µm (b,c) Detailed view of the anastomoses, formed by a tip-to-tip connection (arrows). Bars, 20 µm.

isolate of G. mosseae spreading from different host plants. In contrast, the Gigasporaceae species studied (S. reticulata and G. margarita) never formed anastomoses between hyphae of different mycelial networks of the same isolate ( Table 1). This fundamental observation complements the earlier results obtained by Giovannetti et al. (1999) with hyphae growing from germinated spores. These authors observed that Gigaspora rosea and Scutellospora castanea were unable to form anastomoses between hyphae of germinated spores belonging to the same isolate, while such a mechanism was observed in species belonging to the Glomeraceae, G. intraradices, Glomus caledonium and G. mosseae. Regarding anastomosis formation within the same mycelial network, the two Glomus species mostly formed anastomoses between different hyphae. Anastomosis within the same hypha was noted only once, with G. proliferum (Table 1). Such an event was not reported by de la Providencia et al. (2005), and seldom reported in old colonies of G. intraradices following protrusion of cytoplasmic/protoplasmic material in damaged hyphae and subsequent hyphal bridging (Bago & Cano, 2005), demonstrating its rarity in Glomus species. The number of anastomosis within the same mycelial network was comparable with results obtained by de la Providencia et al. (2005) with the same accessions, but was markedly lower compared with the results of Giovannetti et al. (2004). The lower number of anastomoses found here could be related to the different AM fungal species or host plant, but more probably to the

experimental system. A two-dimensional system was used; as Mosse (1959) states: ‘on cellophane, anastomoses are extremely common, possibly because all hyphae are in the same horizontal plane and must therefore meet frequently’. The Gigasporaceae species studied developed numerous anastomoses within the same hypha, while few anastomoses were detected between different hyphae of the same mycelial network. The proportion between both types of anastomosis (Table 1) was in agreement with the results of de la Providencia et al. (2005). Both types of anastomosis were habitually a consequence of cytoplasmic flow obstruction following damage. We hypothesized that damage was presumably associated with the high pressure of the actively streaming cytoplasm/ protoplasm in the hyphae. This pressure could cause microfractures in the hyphal wall, resulting in an efflux of cytoplasmic/protosplasmic material. This was corroborated by the frequent observation of cytoplasm/protoplasm protrusion from these hyphal sections, and supported by earlier observations (de la Providencia et al., 2005).

Conclusion The dissimilar behaviour of the mycelial networks of the Glomeraceae and Gigasporaceae species under study suggested divergent strategies for the fungal colonies to explore and to exploit new environments and substrates and to create large networks. In Glomus species, anastomoses were observed

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both within and between mycelial networks of the same isolate. This behaviour has physiological as well as genetic implications, enhancing sink-regulated redistribution of resources within a single fungal colony (Rayner, 1991) and between fungal colonies of the same isolate. It may also participate in the maintenance of genetic diversity in the absence of sexual recombination by migration of nuclei via the fusion bridge between mycelia (Giovannetti et al., 2004). In contrast, development of the Scutellospora and Gigaspora species studied is oriented towards the individual spreading of thick hyphae, forming the backbone of the colony (de Souza & Declerck, 2003). These hyphae were not observed to anastomose with hyphae from other mycelial networks belonging to the same isolate; seldom anastomosed with hyphae from the same network; but mainly formed intrahyphal anastomoses (hyphal bridges). This mechanism suggests the propensity of these hyphae to colonize new substrates and new hosts by themselves, without the support of adjacent hyphae.

Acknowledgements This work was supported by a grant of the ‘Fonds Spéciaux de Recherche’ (FSR) of the Université catholique de Louvain. I.E.P. thanks Dr José R. Martin Triana, Director of INCA, for supporting AM fungal research. S.D. gratefully acknowledges financial support from the Belgian Federal Office for Scientific, Technical and Cultural affairs (OSTC, contract BCCM C3/ 10/003). Thanks are also addressed to Professor E. Le Boulengé and Dr E. Kestens for statistical advice. Liesbeth Voets1, Ivan Enrique de la Providencia1,2 and Stéphane Declerck3* 1

Université catholique de Louvain, Unité de Microbiologie; 2Instituto Nacional de Ciencias Agricolas (INCA), Km 31/2 Carretera de Tapaste, Gaveta Postal 1, San José de Las Lajas, La Habana, Cuba; 3Mycothèque de l’Université catholique de Louvain (part of the Belgian Coordinated Collections of Micro-organisms), Unité de Microbiologie, Croix du Sud 3, 1348 Louvain-la-Neuve, Belgium (*Author for correspondence: email [email protected])

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References Bago B, Cano C. 2005. Breaking myths on arbuscular mycorrhizas in in vitro biology. In: Declerck S, Strullu DG, Fortin JA, eds. In vitro culture of mycorrhizas. Heidelberg, Germany: Springer-Verlag, 111–138. Cranenbrouck S, Voets L, Bivort C, Renard L, Strullu DG, Declerck S. 2005. Methodologies for in vitro cultivation of arbuscular mycorrhizal fungi with root organs. In: Declerck S, Strullu DG, Fortin JA, eds. In vitro culture of mycorrhizas. Heidelberg, Germany: Springer-Verlag, 341–375. Declerck S, Strullu DG, Plenchette C. 1998. Monoxenic culture of the intraradical forms of Glomus sp. isolated from a tropical ecosystem: a proposed methodology for germplasm collection. Mycologia 90: 579–585. Giovannetti M, Azzolini D, Citernesi AS. 1999. Anastomosis formation and nuclear and protoplasmic exchange in arbuscular mycorrhizal fungi. Applied and Environmental Microbiology 65: 5571–5575. Giovannetti M, Sbrana C, Avio L, Strani P. 2004. Patterns of below-ground plant interconnections established by means of arbuscular mycorrhizal networks. New Phytologist 164: 175–181. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69–72. Kirk PM, Cannon PF, David JC, Stalpers JA. 2001. Ainsworth and Bisby’s dictionary of the fungi, 9th edn. Wallingford, UK: CABI Publishing. Mosse B. 1959. The regular germination of resting spores and some observations on the growth requirements of an Endogone sp. causing vesicular–arbuscular mycorrhiza. Transactions of the British Mycological Society 42: 273–286. de la Providencia IE, de Souza FA, Fernandez F, Séjalon-Delmas N, Declerck S. 2005. Arbuscular mycorrhizal fungi reveal distinct patterns of anastomosis formation and hyphal healing mechanisms between different phylogenetic groups. New Phytologist 165: 261–271. Rayner ADM. 1991. The challenge of the individualistic mycelium. Mycologia 83: 48–71. Read DJ. 1998. The ties that bind. Nature 396: 22–23. Smith SE, Read DJ. 1997. Mycorrhizal symbiosis, 2nd edn. San Diego, CA, USA: Academic Press. de Souza FA, Declerck S. 2003. Mycelium development and architecture, and spore production of Scutellospora reticulata in monoxenic culture with Ri T-DNA transformed carrot roots. Mycologia 95: 1004–1012. Strullu DG, Romand C. 1986. Méthode d’obtention d’endomycorrhizas à vésicules et arbuscules en conditions axéniques. Comptes Rendus de l’Académie des Sciences 303: 245–250. Key words: anastomosis, arbuscular mycorrhizal (AM) fungi, Gigasporaceae, Glomeraceae, monoxenic culture, mycelial networks.

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Meetings Variability matters: towards a perspective on the influence of precipitation on terrestrial ecosystems Effects of Precipitation Change on Ecosystems (EPRECOT) – a Terrestrial Ecosystem Response to Atmospheric and Climatic Change (TERACC) and European Commission sponsored precipitation workshop, Elsinore, Denmark, May 2006 The availability of water influences ecosystem structure and function in nearly all terrestrial biomes. Precipitation is the primary input of this limiting resource, which drives both biotic and abiotic processes. As a consequence of global warming, precipitation patterns are expected to change around the world, and data sets from both the USA and Europe demonstrate that changes in rainfall patterns attributable to human activity have already occurred within the last few decades. General circulation models (GCMs) predict changes in the spatial and temporal patterns of precipitation, including shifts in the frequency, intensity and magnitude of precipitation events (IPCC, 2001). Through the use of proxy data, observational studies, experimental manipulations and modeling, scientists are investigating how such changes in precipitation regimes may affect the structure and function of the Earth’s ecosystems and biomes. In May 2006, researchers met in Elsinore, Denmark for a workshop on the Effects of Precipitation Change on Terrestrial Ecosystems (EPRECOT; http://www.climaite.dk/ eprecot/eprecot.html). The meeting focused on reviewing the current state of knowledge, identifying knowledge gaps for future research activities, and generating testable hypotheses about expected outcomes of precipitation change through the use of ecosystem models. Three central questions formed the foundation for presentations and discussions at the workshop. (1) How can ecologists pursue questions relating to precipitation change in terrestrial ecosystems in a synthetic way? Is it possible to achieve an understanding of precipitation as an ecosystem driver that spans multiple regions of the globe and biome types? (2) What are the important response variables in assessing the impacts of precipitation change? How can we conduct

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research that accounts for responses across ecological, spatial, and temporal scales? (3) How can experimental design and model development be better integrated? What are the major limitations that exist in interpreting results from both models and experimental research?

‘… treating precipitation as a black box ecosystem driver in terms of mean inputs is inadequate; variability and extremes in precipitation are more important drivers of ecosystem function than are mean conditions’

The complexities associated with precipitation research One of the grand challenges associated with studies of precipitation change is the inherent variability in precipitation itself. This variability, coupled with the complexity inherent to natural ecosystems, complicates simple understanding of effect–response relationships, particularly when feedbacks among the atmosphere, biosphere and geosphere are involved. Precipitation drives many biotic processes, which are the response variables of interest to many ecologists. However, precipitation is most proximally coupled to abiotic characteristics of ecosystems such as soil moisture, the depth of soil wetting and soil moisture recharge, soil temperature, and evaporation (all of which control ecosystem water and energy balance). It is these characteristics that translate the effects of precipitation events and patterns on plant, animal and microbial processes. Biologists and ecologists must therefore incorporate aspects of hydrology into their research and track the movement of water through the atmosphere, soils, and ultimately living organisms. When attempting to understand and characterize ecosystem function, the most simple and parsimonious explanations tend to be the most useful; mean annual precipitation is thus frequently used to describe the availability and influence of water as a resource. However, increasing evidence suggests that treating precipitation as a black box ecosystem driver in terms of mean inputs is inadequate, and that variability and

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extremes in precipitation (e.g. size and intensity of event, extended drought or wet periods, seasonality and antecedent conditions) are more important drivers of ecosystem function than are mean conditions. For example, in the Rain Manipulation Plots (RaMPs) experiment at Konza Prairie Biological Station in Kansas, USA, changes in the relative frequency of rain events during the growing season reduced above-ground net primary productivity (ANPP), increased soil nitrogen (N) availability, changed plant community composition, and shifted allocation of carbohydrates from shoots to roots (Knapp et al., 2002). These changes resulted solely from extending the dry interval length between storms (thereby creating a situation of fewer but more intense storms) (Alan Knapp, Colorado State University, Fort Collins, CO, USA). For many ecosystems, GCMs predict soil moisture deficits and/or greater variability in soil moisture, both of which may affect not only the quantity of water available for uptake by plants, but also the availability and mobility of soil N. Soil N is tightly coupled to soil moisture, both spatially and temporally; consequently, alternate wetting and drying of the soil that will accompany increasingly variable precipitation patterns may give rise to pulses in resources (e.g. water and N). Melany Fisk (Appalachian State University, Boone, NC, USA) described the synchrony between plant nutrient demand and microbial release of resources, and their potential sensitivity to low water availability, which can occur even in temperate forest ecosystems. Reductions in soil moisture are hypothesized not only to restrict movement of nutrients to root zones for uptake, but also to limit the movement of labile carbon (C). Further, the accumulation of C substrates during dry periods may cause a flush of resources upon soil re-wetting, elevating rates of biological activity, nutrient leaching and the transfer of nutrients to unavailable pools (Austin et al., 2004). Ultimately, nutrient limitations could become more important than water limitations. More research is needed to better understand the effect of this interdependent coupling of resources on ecosystem function, as it could have important feedbacks to the climate system by influencing carbon fluxes and storage as well as nutrient cycling. Another aspect of precipitation regimes that adds complexity to interpretation of biological responses is the role of time lags, wherein effects of particular rainfall events or regimes impact biological activity at a later time. Because of the long time-scales involved, the role of previous precipitation can be readily evaluated through the use of proxy data. In the eastern Mediterranean, declines in rainfall since the late 1970s have reduced the annual stem increment of Pinus brutia. Analysis of tree rings has revealed that effects of drought may be manifest several years after the drought; storage of water in the soil during previous years may therefore be a better predictor of growth than current-year precipitation (Dimitris Sarris, University of Patras, Patras, Greece). Time lags can also be demonstrated on smaller spatial and temporal scales more amenable to experimental investigation. For example, Osvaldo

Sala (Brown University, Providence, RI, USA) described how experimental reductions in precipitation on the Patagonian Steppe revealed that annual production was reduced in a year of average annual precipitation when the previous 3 years were characterized by relatively low inputs of precipitation.

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Interactions with other global change phenomena Because many global changes are occurring simultaneously, an increasing number of experiments are focusing on the interaction of precipitation change with other potential abiotic or biotic driving variables. In many cases, these multifactor experiments are producing unexpected results and demonstrating complex interactions (Shaw et al., 2002). Atmospheric CO2 concentration and N deposition are two human-induced chronic drivers of change that have increased during the last century. As essential inputs to photosynthetic processes, their increase drives ecosystem structure and function; however, the effect of CO2 and N may be enhanced or diminished depending on the availability of water. For example, in the Mojave Desert, annual precipitation determines the relative responsiveness of the ecosystem to CO2 (Smith et al., 2000). In El Niño years, which bring relatively wet winters to south-western North America, primary productivity increases, with both annual and perennial species responding to the combined effects of these global change drivers (Stanley Smith, University of Nevada, Las Vegas, NV, USA). In contrast, primary productivity is unaffected by elevated CO2 in La Niña (or ‘dry’) years. The importance of a secondary driver was similarly observed in serpentine grasslands in western North America, where increases in plant biomass under greater precipitation have been linked to elevated deposition of N (Jeffrey Dukes, University of Massachusetts, Boston, MA, USA). Finally, results from a study in Central Europe suggest that elevated CO2 may effectively buffer trees from droughts, which are predicted to become more common in the future. In a year when annual precipitation was reduced by > 50% (relative to the long-term mean) and ambient temperatures were elevated by 2–4°C, trees growing under conditions of elevated CO2 had improved water relations and higher photosynthetic rates than trees growing at ambient CO2. A reduction in transpiration rates was observed in all species, which suggests that greater water-use efficiency may alleviate conditions of moisture stress for trees in this region (Sebastian Leuzinger, University of Basel, Basel, Switzerland). While global-scale processes are important drivers of change, the role of regional-scale processes (i.e. land use and management) should also be considered when evaluating the effects on precipitation change on ecosystems. In the UK, sheep currently graze the large tracts of grassland that dominate the landscape. Recent evidence suggests that infiltration of rainfall is correlated with grazing intensity, and that halving the stocking density of sheep doubles rates of rainfall

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infiltration (Bridget Emmett, Centre for Ecology and Hydrology, Bangor, UK). In western North America, regional cycles of moisture and drought are tightly coupled with fire (Swetnam & Betancourt, 1990). Fire scars in tree rings are correlated with El Niño and La Niña events, which produce cycles of plant productivity followed by intense drying – conditions that encourage fire (Steve Leavitt, University of Arizona, Tuscon, AZ, USA). Multifactor experiments have been instrumental in demonstrating the importance of interactions among globaland regional-scale drivers (Norby & Luo, 2004); however, they have also demonstrated the complexity of articulating mechanisms when drivers interact in additive or negative ways (Aimée Classen, Oak Ridge National Laboratory, Oak Ridge, TN, USA). During the meeting, Dieter Gerten (Potsdam Institute for Climate Impact Research, Potsdam, Germany) presented model output for several sites where there are ongoing multifactor experiments, which have allowed researchers to compare empirical and modeled results. This generated considerable discussion of model sensitivities, source and sink processes, and ecological processes that may need to be included in models as they continue to be refined.

Cascading responses to precipitation change Because the response of any given ecosystem to a change in precipitation is likely to be complex, experimental research should consider all levels in the ecological hierarchy (i.e. genetic, population, community, and ecosystem) to identify mechanisms or adaptations and compensatory responses to changes in driving variables. During the meeting, a number of studies described an ‘organization’ or progression of events that characterizes the temporal response of ecosystems to changes in precipitation patterns. Because plant water status (and subsequently carbon uptake) is closely linked to availability of soil water, reductions in soil moisture influence the physiologic activity of individual plants with ramifications for integrated ecosystem processes such as ANPP. Similarly, reductions in microbial activity may constrain N availability for plant uptake. As a result, interspecific variability in plant physiology (e.g. water and nutrient relations) may ultimately lead to shifts in the relative abundances of species in response to episodic or chronic directional changes in precipitation patterns. In herbaceous systems such as grasslands, community re-ordering can take place in less than 10 years if changes in precipitation are persistent (Alan Knapp). Under a new climatic regime, either experimental or natural, there are certain to be some ‘winners’ and some ‘losers’ in all ecosystems. While this may be evinced in subtle shifts in community composition or dominance (e.g. one species of a C4 grass replacing another) it may also result in more dramatic community type changes (e.g. grassland to shrubland), functional group substitutions (e.g. C4 to C3 species) and/or

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species losses (Bachelet et al., 2001). Many of the biotic changes will be contingent upon the magnitude of the change in precipitation (and its interaction with other global change drivers) in addition to the buffering mechanisms and thresholds that characterize individual ecosystems. At local scales, communities are composed of multiple species that differ in such characteristics as rooting depth, growth rate, and physiology or morphology, which affect their ability to utilize different resource pools or to conserve water. Josep Peñuelas (Universitat Autònoma de Barcelona, Barcelona, Spain) emphasized the role of phenotypic and genotypic variability as controls over community adaptation to precipitation change, as well as the role of plant species migration. In the Montseny Mountains of Spain, beech trees have migrated to higher elevations from lower elevations commensurate with changes in temperature and aridity. Further, while evolution will lag behind climate change, it is an important aspect of ecosystem response that is difficult to predict.

Need for experimental protocols It is clear that the number of experiments designed to determine the effect of potential changes in precipitation on terrestrial ecosystems has increased from few to many over the course of the last decade. It is equally clear, based on the presentations at the meeting and the current literature, that there are probably as many methodologies in use as there are experiments (Weltzin et al., 2003). This phenomenon probably arises for several reasons. First, by their nature, experiments are hypothesis-driven, and the plethora of sites and questions across a variety of spatial and temporal scales requires a multiplicity of approaches and techniques. Second, simulation of a current precipitation regime, not to mention potential future regimes, is fraught with uncertainty because of the highly variable (and thus uncertain) nature of the various components of this factor: should one manipulate means, extremes, intensity, frequency, serial correlation, etc.? Once this is decided, what is the best technique to catch and store or deliver, and then apply, water to experimental plots? Thus, a theme recurrent in discussion was whether a particular protocol could or should be adopted to facilitate synthesis among precipitation manipulation experiments (e.g. free-air CO2 enrichment experiments that target a CO2 of 550 ppm). Although this issue was unresolved, it was generally agreed that regions of sensitivity to particular aspects of precipitation change should be identified for additional study, and that manipulations need not necessarily be tied to a specific GCM (or more local or regional model), particularly when research questions are mechanistic (e.g. focusing on identification of critical thresholds or the role of infrequent extremes in driving ecosystem structure or function). In addition, new projects should carefully consider the role of droplet size, runoff, water chemistry, etc. from an ecohydrological

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perspective, as these ‘details’ may influence biotic responses. Regardless, a diversity of approaches and methodologies may be required to fully address the diversity of characteristics of contemporary or potential future precipitation regimes.

Acknowledgements The EPRECOT workshop was jointly supported by the European Union under the 6th framework programme and the United States NSF-sponsored research coordination network Terrestrial Ecosystem Response to Atmospheric and Climatic Change (TERACC). Lindsey Rustad and Claus Beier chaired the organizing committee, which also included Wolfgang Cramer, Christian Körner, Josep Peñuelas, Dieter Gerten, Michael Loik, Yiqi Luo, Richard Norby, and William Parton. Jana L. Heisler1* and Jake F. Weltzin2 Department of Biology, Colorado State University, 1878 Campus Delivery, Fort Collins, CO 80523, USA; 2 Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN, USA (*Author for correspondence: tel +1970 491 0453; fax +1970 491 0649; email [email protected]) 1

References Austin AT, Yahdjian ML, Stark JM, Belnap J, Norton U, Porporato A, Ravetta D, Schaeffer SM, Burke IC. 2004. Water pulses and

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