Biogenic debris from the pelagic tunicate, Oikoplewu ... - Science Direct

Estuarine, Coastal and Shelf Science (1984) 18, 13-23

Biogenic debris from the pelagic tunicate, Oikoplewu dioicu, and its role in the vertical transport of a transuranium element

Gabriel

Gorskya,

International Laboratory 98000 Monaco

Nicholas of Marine

S. Fishe@

and Scott

Radioactivity,

M&e

W. Fowler

Ockanographique,

MC

Received 26 October 1982 and in revisedform 25 February I983

Keywords: tunicates; biogeochemistry;fecal pellets; sinking; americium; MediterraneanSea The

accumulationand retention of z*rAm by the pelagictunicate OikopZeura

dioica were examinedusing laboratory cultures and radiotracer methodology.

Animals (i.e., trunks and tails) and discardedempty housesaccumulatedAm from seawater,giving volume/volumeconcentrationfactorsof 59i 8 and 10i 1, respectively.The half-time for retention of Am in empty labelledhousestransferred to non-contaminated seawaterwas29 h; the retention half-time of Am in housesdiscardedby larvaceansfeedingon Am-labelleddiatoms was 219 h; the half-time of Am in fecal pelletsproducedby animalsfeedingon a monospecific diet of diatomswas 134h, and 247h for fecal pelletsfrom animalsfed a mixed diet. Approximately30%of filtered cellsremainedin housesafter the houses were discarded.Sinkingratesof discardedhousesandfecal pelletswerefound to vary with temperatureand size, ranging from 26-157m day-1 (houses)and from 25-166m day-l (fecal pellets).The ubiquity andabundance of appendicularians, together with their prodigiousproductionof houses(e.g., lOi housesday-l at 17“C for eachexperimentalanimal)point to their potential significancein the vertical transport of Am, and probably other reactive metals,to intermediate depthsin the ocean. Introduction In their recent review, Beasley & Cross (1980) stressthe lack of available information on biological transfer and transport of transuranic elements in many important components of marine ecosystems.In particular, the plankton have been little studied in this regard, though they play important roles in pollutant transport and food chain transfer (Fowler, 1982). What data are available point to the high reactivity (i.e., high concentration factors for suspendedparticles) of such elementsas Pu, Am and Cf for phytoplankton (Gromov, 1976; Fisher et al., 1980; Fisher et al., 1983~) and crustacean zooplankton (Fowler et al., 1976; Aston & Fowler, 1983; Fisher et al., 1983b). Virtually nothing is known however of the biokinetics of transuranics, or other stable metals, in appendiculariansor other gelatinous zooplankton. The global distribution of appendiculariansand their significance in marine food webs (Fenaux, 1966; Alldredge, 1976; PafFenhiifer, 1976; King et al., 1980; ‘Present address: Station ?o whom correspondence

Zoologique, Villefranche/mer

06230,

France.

should be addressed. 13

0272-7714/84/010013+11

$03.00/O

0 1984 Academic

Press Inc. (London)

Limited

14

G. Go&y,

N. S. Fisher & S. W. Fowler

Silver & Alldredge, 1981; Taguchi, 1982; Alldredge & Madin, 1982) suggest that they may significantly mediate the transport of metals in ocean waters. In particular, their fecal pellets and discarded houses may be expected to transport pollutants to depth, though there is little available information on their production and sinking rates or on their interactions with pollutants. As part of a series of experiments to explore the interactions of marine plankton with transuranic elements, we have addressed the question of americium biokinetics in a typical gelatinous zooplankter, Oik@Zeuru dioica. We have focused on the bioaccumulation and retention of Am by animals and their houses and fecal pellets. In this study, we have pursued a laboratory-based approach employing a well-defined culture system (Fenaux & Gorsky, 1979; Gorsky, 1980) and radiotracer methodology. Materials

and methods

Experimental procedures

Appendicularians are pelagic filter-feeding tunicates. The animals of the family Oikopleuridae live inside mucilaginous houses secreted periodically by specialized epithelial cells of the animal’s trunk (Figure 1). Water is circulated through the house via constant oscillations of the tail. In the house, a filtering apparatus connected to the mouth removes small particles from the water for ingestion (Fenaux, 1971; Galt, 1972).

L

‘

Figure 1. Schematic diagram of 0. dioicu (modified from Fenaux & Hirel, 1972). H-house; IF-incurrent filter; Tr-trunk; T-tail; FA--filtering apparatus. Scale bar: 1 mm.

Oikopleura dioica (Tunicata, Appendicularia) individuals were collected in Villefranche Bay, France and maintained in laboratory culture on a mixed algal diet (Fenaux & Gorsky, 1979). Stock cultures for experiments were kept at 17 f 1 “C under cyclic (12 : 12 light : dark) illumination. Experimental animals were cultured on the small (61 um3 cell-l) centric diatom 7’halassiosirapseudonanu (Clone 3H) (cell density: 104 ml-i); three to five-day old animals, with trunk lengths 400-800 ~.un, were used. Volumes of animals and houses were estimated from microscopic assessments of appropriate dimensions; for example, for animals of 650+20 p trunk length, trunk plus tail =6 *2 x 107 ~3 (oblate spheroid) and houses = 1.4 x 1010 l~rn3 (sphere). For measuring 24lAm accumulation from water, five animals were transferred via Gilson micropipette into each of four acid-rinsed 50 ml glass beakers containing 40 ml of sterilefiltered surface Mediterranean seawater (0.2 lun Sartorius cellulose acetate filter) and

Am in an appendicularian

15

7.4 kBq z”Arn (6.65 nM 24*Am).The beakerswere sealedwith Parat?lm,placed on a rotary shaker, and gently agitated at 17+ 1“C in 25 pEin m-2 s-i light for 11h. Five animalswere removed by micropipette at each of four sampletimes (1, 5, 7, 11 h), serially washed 3 times by submersing individuals in 500 ml unspiked sterile-filtered seawater (1 min per wash), and placed in a plastic counting vial. (Additional experiments, in which the radioactivity of animalswas counted without prior washingand the radioactivity of equal sample volumes of experimental medium was subtracted gave identical results). Additionally, uptake of 24*Arn from water by empty 0. dtiica houseswas examined. Empty experimental houseswere produced by starved animalsin unspiked sterile-filtered seawater, transferred by micropipette into beakers containing Am-spiked seawater and treated like the 92-h animals. A separate but similar experiment was designedto examine the possible effect of metabolic breakdown products from discarded mucilaginous houses on the uptake rate of 241Am(see Fowler et al., 1975). In this case empty houseswere collected from cultures in which animals had been maintained for 2-3 h in seawater containing 241Arn(6.65 nM) without algae. In one treatment housesalready labelled with 241Arnwere subsequently transferred at each counting time into fresh sterile-filtered seawater (5 houses per beaker) containing the same concentration of 24iAm. Counting times were at 2, 22, 47 and 92 h, the latter time being the end of the experiment. In a similar treatment, someof the pre-labelled houseswere transferred once to freshly-spiked seawater in which they were maintained for the remainder of the experiment. The retention of 241Amby 0. dioica houses was studied with empty houses (i.e., containing no algal cells) and full houses(containing algal cells) transferred to unspiked sterile-filtered seawater. The empty houses were expended by animals maintained in labelled water for 6 h. The full houses were produced by animals grazing for 5 h on 24*Am-labelled T. pseudonanacells in unspiked sterile-titered seawater. Care was taken to select housescontaining no fecal pellets. Four experiments utilized cell densitiesof 13.0, 9.5, 11.O and 15.3x 10’ ml-l. Labelled algal cells were produced by incubating 3H cells for 4-5 days with 7.4, 7.4, and 29.6 kBq 24iAm, respectively, in f/2 medium (Guillard & Ryther, 1962), minus Cu, Zn and EDTA, prepared from sterile-filtered Mediterranean surface water. Cells were filtered onto l-pm Nuclepore filters and resuspended into unlabelled sterile-filtered seawater (see Fisher et al., 1983a, for details). After being discarded, the houseswere washed, transferred to unspiked sterile-filtered seawater, and sampledperiodically for radioactivity. Fecal material was also collected to measureAm retention times in the fecal pellets. At the end of one of the feeding experiments, fecal pellets (maximum dimension 5 300 pm) dischargedby 0. dioica individuals were collected asfollows: a glasspipette (1 cm opening) was used to transfer fecal pellets and small quantities of seawaterinto a glassPetri dish, viewed under a dissecting microscope, from which individual pellets were removed by micropipette and placed in unlabelled, sterile-filtered seawater for washing. These pellets were then transferred via micropipette into a 2 cm x 0.8 cm (diameter) glass cylinder containing unlabelled sterile-filtered seawater and covered by 30-pm plankton mesh at each end. The cylinder was suspendedin the middle of a column of 11 of sterile-filtered seawater. Periodically, the cylinder containing the fecal pellets was placed in a counting tube, counted for radioactivity, and replaced in fresh sterile-filtered seawater for further loss. Three replicate experiments were conducted with fecal pellets produced by animals feeding on a monospecific diet of T. pseudonana.A fourth experiment wasconducted with fecal pellets produced by animals feeding on a mixed diet of T. pseudonana(same cell density) and a natural particle assemblage< 30 pm.

16

G. Gorsky,

N.

S. Fisher t3 S. W. Fowler

The sinking rates of 0. &X&Z fecal pellets (800 pm trunk length animals; 200 x 80 pm pellets) and discarded houses (400,600, and 800 pm trunk length animals) were measured at eight different temperatures for houses (from 4-26 “C) and five different temperatures for fecal pellets (from 4-26 “C). Fecal pellets and houses were harvested from continuous cultures of 0. dioica maintained on natural particle assemblages (< 30 pm) in Mediterranean surface water (Fenaux & Gorsky, 1979). Houses and pellets were transferred to a 2-l graduated cylinder containing 2 1 of glass-fiber filtered seawater. The cylinder was illuminated from below (against a black background) and submerged in a continuous flow water bath which maintained a constant temperature (+O* 5 “C) throughout the water column. At each temperature, ten replicate observations were made for each batch of houses or fecal pellets. Techniques and precautions for measuring the descent of these materials generally followed those described by Small et ul. (1979). Isotope

Americium-241 was supplied by the Commissariat Q l’Energie Atomique, Gif-sur-Yvette, France. The isotope was provided in dilute nitric acid and diluted further with distilled water. Isotope was added to experimental media in microlitre quantities using Eppendorf automatic pipettes. Preliminary experiments and results of other experiments (Fisher et al., 1983a) indicated that < 5% of the added isotope adsorbed onto the glassware surface throughout the experiments. The radioactivity of samples was determined by detecting 59.5 keV photon with a multichannel analyser coupled to two 7*6-cm well-type NaI(T1) crystals. Backgrounds and Am standards were counted daily using the same counting geometry and appropriate corrections made. Counting times and backgrounds were such that propagated counting errors were generally less than f 10%. Results Oikopleura dioica individuals accumulated 241Am directly from water, with volume/volume concentration factors (i.e., Am per pm3 trunk + tail/Am per pm3 external medium) reaching = 60 by the end of the 11 h experiment (Figure 2). Owing to the low specific gravity of this species, there is no appreciable difference between volume/volume concentration factors and concentration factors based on wet weight. Bioaccumulation was rapid initially but the uptake rate appeared to decrease after the first hour. After 11 h, these animals died due to a lack of food and their structural integrity was rapidly lost. Empty houses expended in Am-labelled water and transferred once into fresh labelled seawater continued to accumulate Am rapidly over the next few hours; however, by 22 h vol/vol concentration factors had levelled off at steady state values of approximately 8 (Figure 3, curve B). Unlabelled empty houses showed a comparable uptake response when maintained in conditioned, unchanged spiked seawater; i.e., uptake virtually ceased after 22 h (Figure 3, curve C). On the other hand, pre-labelled houses serially transferred to unconditioned aliquots of 24lAm-labelled seawater continued to accumulate the radionuclide throughout the 4 day experiment (Figure 3, curve A). Although final concentration factors for houses were still relatively low ( =lO), these results suggest that accumulated degradation products from the houses may alter the bioavailability of Am, possibly through the formation of organic complexes with the radionuclide. When Am-labelled empty houses were transferred to fresh sterile-filtered seawater containing no isotope, Am loss was rapid, with a calculated biological half life of 29 h for the slower loss compartment measured between 5 and 48 h (Figure 4, curve A). After 2

17

Am in an appendicuiarian

1.

3.

3. I r’ 3

5

IO Time hours)

Figure 2. Accumulation of Am by 0. dioica suspended in spiked filtered 0 symbols for each replicate experiment. Error bars = 1 (z counting errors.

seawater.

n,

A,

60 Time(h)

Figure 3. Uptake of Am by empty 0. dioica houses. A (0) houses expended in spiked medium and transferred to fresh spiked medium at each sample time. B (v) houses expended in spiked medium and transferred once to fresh spiked medium. C (H) houses expended in unspiked medium and transferred to spiked medium at time zero. Arrow indicates when pre-labelled houses were transferred into fresh radioactive medium. Data points are means from 3 replicate experiments, shown + 1 SD (error bars).

18

G. Gorsky, N. S. Fisher & S. W. Fowler

I

IO

i

i i

i i

i

‘SrA 2

4 Time

6

(days)

Figure 4. Am loss from (A) empty 0. d&a houses, (B) from houses discarded by 0. d&a feeding on labelled T. pseudonanu, (C) from fecal pellets discharged by animals feeding on T. pseudona~ only, and (D) from fecal pellets discharged by 0. dioicu feeding on a mixed algal diet. Error bars indicate 1 (T counting errors (A and D, n = 1) or 1 SD (B and C, n = 3).

days, these transparent houses were no longer detectable. In contrast, houses discarded by animals which had fed on labelled T. pseudonana cells remained intact for one week and retained far more of their Am (Figure 4, curve B). Microscopic examination (50 x magnification) confirmed that no fecal material was contained inside these houses. The biological half life of the Am in these latter houses was calculated to be 219 h. From algal cell counts and analyses of the radioactivity of the houses, it can be calculated that approximately 30% of the total number of diatom cells filtered were retained by the discarded houses (Table 1); the presence of cells in the filtering apparatus of the houses was confirmed by microscopic examination. Radioanalysis of animals during feeding indicated that the full guts contained 6.4 f 1’ 5 x 103 (n = 3) diatom cells, with no significant differences in filtration rates between replicate experiments for a given animal size (Table 1). After gut evacuation, there was no detectable Am in the animal indicating little, if any, assimilation of this metal and its rapid excretion with the feces. Fecal pellets produced by animals feeding on a monospecific diet of T. pseudonanawere diffuse and easily disrupted. Assuming cylindrical shape, the mean volume of a fecal pellet from a 650 p animal was 4.6 + 1.0 x 104 un+. Given that one T. pseudonanacell occupies 61 ~3 (Fisher et al., 1983a), each fecal pellet could contain = 750 perfectly compacted diatom cells. This corresponds with the observation based on Am counts of a content of ~500 cells, or 67% packing efficiency. Upon transfer to unlabelled seawater, the retention half-time of Am in these fecal pellets was 134 hours (Figure 4, curve C); in contrast, the half-time of Am retention in fecal pellets produced by animals feeding on a mixed algal diet was longer-247 hours (Figure 4, curve D)+eflecting the visual observations that the latter pellets appeared more compact. Sinking rates of discarded houses increased with increasing house size and were an exponential function of temperature [Figure 5(a)]. Furthermore, sinking rates were

19

Am in an appendicularian

1. Americium content of 0. dioica houses from animals feeding on Am-labelled T. pseudonana cells. Results of four experiments C propagated 1 CJcounting errors

TABLE

Animal trunk length (pm)

Experiment

Diatom ( i%~),

650f20 65Ok20 650+20 830 k 20

k i

cells

13.0 9.5 11.0 15.3

“Determined

0

4

8

12

Am atoms In-’ (x 10’0)

Am atoms cell-l (x 105)

7.9kO.9 4.6zhO.2 37.Ok1.5 21.2kO.6

6.liO.7 4.8kO.5 33.6k3.4 13.8f0.4

by microscopic

16

Temperature

20 PC)

Cells filtered house-* (x 10’)Q

Am atoms filtered house-l (x 10’0)

Am atoms retained house-l ( x 10’0)

31 28 30 53

19i2 13fl lOlfl0 73$-2

6.1kO.6 4.9kO.7 24.9kO.9 23.2+ 1.2

cell counts using hemacytometer;

2400

Am retained Am filtered 32% 37% 25% 32% y=31.5?5%

CVclO%.

2700 Specific

gravity

3000 anomaly

(~10~)

Figure 5. (a) Sinking rates (m day-l) of fecal pellets (M) and houses discarded by different sized 0. dioica (O-0 8OOpm trunk; v-----v 6OOpm trunk; C---H 400 pm trunk) at different temperatures. Lines are described by the equation: y=aebx, where a=20.37, b=0,0589 (4OOprn trunks; r10.900); a~23.02, b=0,0703 (600~ trunks; r=0.960); a=31.69, bx0.0692 (800~ trunks; r~0.969); a=19.701, b=0.0885 (fecal pellets; rz0.978). (b) Sinking rates (m day-~) of fecal pellets (G---X)) and houses discarded by different sized 0. dioica. (e-0 800 pm trunk; v----v 600 pm trunk; I---d 4OOun1 trunk) at different water densities (specific gravity anomalies). Densities were calculated by the equation y = ax* + bx +c, where y = specific gravity anomaly, x=temperature (“C), a= -0.459, b = -8.257, and ~~3058.23, using temperature/density data presented in Riley & Chester (1971) for 38% seawater. Lines are described by the equation y=ax+ b, where a = -0.158, b=496’ 1 (400 pm trunks; r= -0.849); a= -0,238, bz742.2 (6OOprn trunks; r= -0.943); a= -0,237, bc7j8.2 (8OOpm trunks; r= -0,982); a= -0.301, b=936’5 (fecal pellets; T= -0.984).

linearly related to the density (specific gravity anomaly) of seawater [Figure 5(b)]. Rates varied widely from 26-t 14 m day-l for houses from small animals (400 pm trunk length) at 4 “C to 157 +20 m day-1 for houses from large animals (800 p trunk length) at 26 “C. Sinking rates of fecal pellets also varied as a function of water temperature or density, ranging from 25 m day-l at 4 “C to 166 m day-l at 26 “C (Figure 5).

20

G. Gorsky, N. S. Fisher & S. W. Fowler

Discussion

The volume/volume Am concentration factors of 0. dioicu houses and naked animals (i.e., trunk and tail) are considerably lower than volume/volume concentration factors for Am in marine phytoplankton, where values are of the order of = 105 (Fisher et al., 1983~~). Marine invertebrates, as a rule, have significantly lower concentration factors (expressed either on wet weight or volume bases) for Am and other transuranic elements than do marine phytoplankton. For example, wet weight concentration factors (for uptake from seawater only) for Am and Pu are typically in the 102 range for euphausiids, shrimp, and worms (Beasley & Cross, 1980). Thus the relative degree of Am uptake measured in 0. dioica is comparable with results obtained with other marine invertebrates. The fact that Am was not efficiently assimilated from ingested food points to the overall importance of the water route in the uptake of this element by 0. dioica. Furthermore, the lack of any apparent *4lAm assimilation is consistent with results for this radionuclide in other small zooplankters (Fowler et al., 1976; Fisher et al., 1983b; Fowler, unpublished data). Americium and other transuranics are passively accumulated from water by marine phytoplankton, euphausiids, and other invertebrates by adsorption onto the organisms’ surfaces (Fowler et al., 1975, 1976; Fisher et al., 1983a,b). This is in agreement with the inverse relationship observed between organism size and plutonium concentration factors in a wide variety of marine forms (Thornann, 1981). While the high concentration factors recorded in phytoplankton may in part be attributable to high surface/volume (s/vol) ratios for unicellular algae, appreciable differences between algal species with comparable s/v01 ratios are observed (Fisher et al., 1983~). Moreover, marine bacteria have been shown to accumulate Pu to a level significantly lower than that of phytoplankton, despite higher s/v01 ratios of the bacterial cells (Carey & Bowen, 1980). Thus, it appears that organism surfaces may vary in their affinity for these reactive elements and it is this characteristic, together with the surface/volume ratio, that primarily determines the level of bioaccumulation of transuranic radionuclides. The *alAm concentration factor in larvacean houses is more than a factor of 10 lower than that in pelagic euphausiids (Fisher et al., 19836) despite the fact that their calculated s/v01 ratios are comparable; this suggests that the chitinous surface of euphausiids is more reactive for these heavy metals than is the mucopolysaccharide surface (Korner, 1952; R. Fenaux, personal communication) of larvacean houses. The lower radioactivity of appendicularian houses stands in contrast to the high reactivity of transuranium nuclides for mucus secreted by a variety of marine species (Guary et ul., 1982; Fowler, unpublished results). Nevertheless, appendicularians may play a significant role in the vertical transport of accumulated transuranic elements, particularly to intermediate depths. Blooms of 0. dioica have been recorded in which mean number of individuals per m3 of surface waters (O-10 m) exceed 103 (Seki, 1973). Taguchi (1982) recorded that 66% of total zooplankton fecal pellet volume in Kaneohe Bay, Hawaii were 0. longicauda fecal pellets. Discarded houses have been shown to average 330m-3 in surface water of the Florida current (Alldredge, 1972) and > 105 m-3 under bloom conditions in Kaneohe Bay (Taguchi, 1982). The mean titration rate of 0. dioica individuals of 650 pm trunk length such as used in some of our experiments) is 37 ml day-l (Gorsky, 1980) which is comparable with results reported elsewhere (King et al., 1980; Alldredge, 1981). In general, particles >O. 1 pm are filtered and retained by these animals (Jorgensen, 1966; Flood, 1978). Once filtered, particles may be digested and eventually defecated, or they may remain in the filtering apparatus of the houses which are expended by the animals at a temperature-dependent rate. Under the

Am in an appendicularian

21

conditions of our experiments, 8-10 houses day-i are produced (Gorsky, 1980). It was found by our radiotracer studies that 32+ 5% of filtered phytoplankton remained in the houses, comparable with the 29% value obtained using pigment analysis (Gorsky, 1980). Thus, we would expect approximately f of filtered Am to be retained by discardedhouses and f retained in metabolic wastes. The particles which are filtered-mostly phytoplankton-can contain approximately 10% of total water column Am in oligotrophic waters such as in the open Mediterranean, but considerably more (i.e., > 50%) in productive waters (Holm et al., 1980). Discarded houses sink at a size and temperature-dependent rate, ranging between =4&l 50 m day-l over a 13-26 “C range, though at 4 “C, sinking rates were significantly lower, averaging about =30 m day-l. These rates are comparable to sinking rates of appendicularian houses measuredby Silver & Alldredge (1981) and Taguchi (1982) under experimental conditions and are also similar to the sinking rates of appendicularian fecal pellets that we measured. It should be noted that these sinking rates were determined under laboratory conditions and the results may not be identical to those which could be found at sea, with less homogeneousconditions. For example, Taguchi (1982) estimated sinking rates of houses in the field at approximately 7 m day-i, based on sediment trap data. Considering the relatively rapid 9 day half-time for Am in housesand 10 day half-time in fecal pellets discardedby actively feeding 0. dioica, the sinking rates of these debris ( = 102m day-l), and their rapid disintegration rate (this report; Gorsky, unpublished data), it would appear unlikely that abandoned housesand fecal pellets would contribute to transuranic transport to great depths, but it is possiblethat the fecal pellets and marine snow, rich in appendicularian houses (Silver & Alldredge, 1981), would contribute to transuranic enrichment of intermediate depth water. For example, in an idealized column of stationary 18“C water populated by 650 pm trunk length animals, half the Gltered Am would be lost from appendicularian debris by the time it sinks to 750 m. It is of interest that Bowen et al. (1971; 1980) have observed enhancedPu levels at roughly 465 m and 500 m in the north Pacific and Atlantic, respectively. Bowen (1983) also reported an *41Am subsurface maximum in the Pacific at a slightly greater depth ( ~750 m) than that of Pu. Thus, it seemsplausible that, as in the general caseof remineralizing biogenic debris (Edgington, 1981), fecal matter and housesfrom pelagic larvaceanscould contribute towards the overall enrichment of transuranium elements observed at these depths. As abandonedhousescan also serve as a concentrated food source for other animals(Alldredge, 1972), these houses may also act as intermediates in the passageof transuranic elements and other reactive metals from primary producers to higher trophic levels in the marine food web. Acknowledgements The International Laboratory of Marine Radioactivity operates under a tripartite agreement between the International Atomic Energy Agency, the government of the Principality of Monaco, and the Oceanographic Institute of Monaco. One of us (GG) is grateful for a fellowship from the Musee Oceanographique and for permission to use laboratory equipment of the Station Zoologique de Villefranche/Mer. We thank R. Fenaux and R. Fukai for helpful comments on the manuscript. References Alldredge, A. L. 1972 Abandoned 177, 8854387.

larvacean

houses: a unique

food source

in the pelagic

environment.

Science

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G. Gorsky,

N. S. Fisher

& S. W. Fowler

Alldredge, A. L. 1976 Discarded appendicularian houses as sources of food, surface habitats, and particulate organic matter in planktonic environments. Limnology and Oceanography 21, 14-23. Alldredge, A. L. 1981 The impact of appendicularian grazing on natural food concentrations in situ. Limnology and Oceanography 26,247-257. Alldredge, A. L. & Madin, L. P. 1982 Pelagic tunicates: unique herbivores in the marine plankton. Bioscience 32,655-663. Aston, S. R. & Fowler, S. W. 1983 Preliminary observations on califomium-252 behavior in sea water, sediments and zooplankton. Health Physics 44, 359-365. Beasley, T. M. & Cross, F. A. 1980 A review of biokinetic and biological transport of transuranic radionuclides in the marine environment. In Transuranic Elements in the enoironment (Hanson, W. C., ed.) US DOE, Springfield, VA. pp. 524-540. Bowen, V. T. 1983. Element specific redistribution processes in the marine water column. In Workshop on Processes Determining the Input, Behaviour and Fate of Radionuclide and Trace Elements in Continenral Shelj Environments. Gaithersburg, Maryland, 7-9 March 1979, US DOE CONF 790382. Bowen, V. T., Noshkin, V. E., Livingston, H. D. & Volchok, H. L. 1980 Fallout radionuclides in the Pacific Ocean: Vertical and horizontal distributions, largely from GEOSECS stations. Earth and Planetary Science Letters 49, 411434. Bowen, V. T., Wong, K. M. & Noshkin, V. E. 1971 Plutonium-239 in and over the Atlantic ocean. ~ournul of Marine Research 29, l-10. Carey, A. E. & Bowen, V. T. 1980 Differential uptake of plutonium (IV) or (VI) by marine bacteria. American Society of Microbiology Annual Meeting. Abstract N 110, p. 182. Edgington, D. N. 1981 A review of the persistence of long-lived radionuclides in the marine environmentsediment/water interactions. In Impacts ojRadionuclide Releases into the Marine Environment. IAEA, Vienna. pp. 67-91. Fenaux, R. 1966 Synonimie et distribution gCographique des appendiculaires. Bulletin of the Institute of Oceanography, Monaco 66, l-23. Fenaux, R. 1971 La couche oikoplastique de 1’Appendiculaire Oikopleura albicans (Leuckart) (Tunicata). Zeitschrift fur Morphologic der Tiere 69, 184-200. Fenaux, R. & Gorsky, G. 1979 Techniques d’elevage des appendiculaires. Annals of the Institute of Oceanography Paris 55, 195-200. Fenaux, R. & Hirel, B. 1972 Cinetique du deploiement de la logette chez l’appendiculaire Oikopleura dioica Fol, 1872. Comptes Rendus de I’Academie des Sciences Paris 275Q 449-452. Fisher, N. S., Bjerregaard, P. & Fowler, S. W. 1983a Interactions of marine plankton with nansuranic elements. I. Biokinetics of neptunium, plutonium, americium, and californium in phytoplankton. Limnology and Oceanography 28,432-447. Fisher, N. S., Bjerregaard, P. & Fowler, S. W. 19836 Interactions of marine plankton with tramuranic elements. III. Biokinetics of americium in euphausiids. 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