Pyrosoma atlanticum (Tunicata, Thaliacea): grazing impact on phytoplankton standing stock and role in organic carbon flux

Journal of Plankton Research Vol.14 no.6 pp.799-809, 1992

Pyrosoma atlanticum (Tunicata, Thaliacea): grazing impact onphytoplankton standing stock and role in organic carbon flux

Alexander V.Drits, Elena G.Arashkevich and Tatjana N.SemenovaInstitute of Oceanology Academy of Science USSR, 117218, Krasikova, 23,Moscow, USSR

Abstract. Pyrosomas are the large group of pelagic tunicates whose trophic role in pelagiccommunities has not yet been sufficiently studied. We ran across a local area of high concentration ofthe most widespread and commonest species of pyrosomas, Pyrosoma atlanticum, 450 miles off theCongo river mouth. The following was estimated: gut pigment content, defecation rate, organiccarbon and pigment content of fecal pellets, and sinking rate. Based on these data and the measurednumber of pyrosomas colonies the grazing impact on phytoplankton and the fecal pellet flux werecalculated. During the night swarms of 50-65 mm P.atlanticum removed 53% of phytoplanktonstanding stock in the 0-10 m layer; sparsely distributed pyrosomas consumed only 4%. The grazingimpact in the 0-50 m layer was only 12.5 and <1% respectively. The fecal pellet flux resulting fromnocturnal feeding of P.atlanticum while swarming made up 1.4-1.6 x 106 pellets m~210 h"' or 305-1035 mgCm"210h"' and 1.4 x 105pelletsm"2 10h"' or 87.4mgCm"2 10h"' while non-swarming.Incubation experiments showed the rapid degradation of fecal pellets at 23°C: the loss of pigmentand carbon content was ~60-70% after 45 h. We believe that given the sinking rate of 70 m day"'the main part of fecal material does not leave the upper water column and is retained in the trophicweb of the epipelagic layer.

Introduction

Interest in pelagic tunicates has increased recently because of their high grazingrates and because of their ability to ingest the smallest oceanic particles,including bacteria. Considerable attention has been focused on the role of salps,doliolids and appendicularians in the trophodynamics of plankton ecosystems(Harbison and Gilmer, 1976; Wiebe et al., 1979, Alldredge, 1981; Deibel, 1982,1986, 1988; Madin, 1982; Madin and Cetta, 1984). Another large group ofpelagic tunicates—pyrosomas—apparently has not been studied from this pointof view (at least we could not find any publications in the last decades).

Pyrosomas are colonial organisms consisting of zooids packed into the tunicwith oral siphons opening outside the cloacal siphons joining the mutual colonialcloaca. Free-swimming colonies of different size (from several centimeters toseveral meters) inhabit epipelagic and mesopelagic layers except in the Antarcticand Arctic regions (van Soest, 1981).

During cruise N 20 of RV Vitjaz in the southeast part of the Atlantic Ocean(August-September 1990) we ran across a local area of high concentration of themost widespread and commonest species of pyrosomas—Pyrosoma atlanticumtwice in the same location 450 miles off the mouth of the Congo river (06°7'S,05°10'E): on August 29-September 1 (station 3171) and on October 20 (station3171A).

To estimate the P.atlanticum population grazing pressure on phytoplanktonand its role in the transport of organic matter, we studied gut pigment content,defecation rate, as well as sinking rate, pigment and organic carbon content offecal pellets and their changes during incubation aboard the ship.

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A.V.Drits, E.G.Arashkevich and T.N.Semenova

Method

Field collection

Pyrosomas were collected in tows of a 0.5 m 505 u.m mesh net with a 0.8 1 plasticvessel as the cod end. Colonies for experiments were sampled from the 0-5 mupper layer; each haul lasted 2-3 min. At station 3171 samples were takenon August 30 at 18.00, August 31 at 18.00, 21.00 and 24.00, and September 1 at04.00. To estimate the abundance of pyrosomas samples were taken from 0-10 m at station 3171 and 0-10, 10-25, 25-50, 50-100 m at station 3171A.Number of colonies were estimated in the whole sample. Water samples forpigment concentration at station 3171 were obtained with a 200 1 bottle from0, 20, 50 and 100 m depth.

Gut fluorescence determination

The use of the gut fluorescence method to estimate grazing of herbivores isbased on the assumption that chlorophyll-derived pigments are not degraded tonon-fluorescent compounds. The degradation has not been investigated inpelagic tunicates, but there are a number of publications concerning thisproblem in copepods (Baars and Helling, 1986; Conover et al., 1986, Ki0rboeand Tiselius, 1987; Pasternak and Drits, 1988). At present results regardingpigment destruction in the copepod gut are conflicting and direct evidence ofdestruction is lacking (Durbin et al., 1990). Measurement of pigments in the gutas an index of feeding has been used earlier with salps (Nemoto and Saijo, 1968;Madin and Cetta, 1984). It was found that the filtering rate of salps calculatedfrom gut pigment data was comparable with rates measured in particle clearanceexperiments (Madin and Cetta, 1984). In this study we estimated the amount ofpigment in the gut of P.atlanticum assuming that there is no degradation ofchlorophyll to non-fluorescent compounds during gut passage.

For gut pigment measurement pyrosomas were frozen at — 18°C immediatelyafter collection. Three segments of 3-5 mm width were cut from the middlepart, near the open end and the tip of previously measured colonies. Eachsegment was ground in a glass tissue grinder with 90% aqueous acetone; the finalvolume of the homogenate was 10 ml. After 24 h extraction in the darkness at4°C the homogenate was centrifugated at 5000 r.p.m. for 10 min. Pigmentconcentration was measured with a laser spectrofluorometer (Pasternak et al.,1987). The gut pigment content was calculated by multiplying the average valueper mm of examined segments by the length of a colony. All values are reportedas the total of chlorophyll and phaeopigments (computed as chlorophyll aequivalents).

Defecation rate determination

Colonies for the defecation rate measurement were placed by submerging thecod end in a 40 1 aquarium with surface seawater. The colonies were gentlyremoved one by one with a 200 ml glass vessel and transferred under a dissectingmicroscope. The number of egested fecal pellets was counted during 5-10 min

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P.atlanticum: grazing impact on phytoplankton

continuous observations; two to three colonies were examined simul-taneously.

Fecal pellets analysis

Freshly collected pellets were examined under the light microscope at 600xmagnification and the size of visible intact items measured. For pigmentdetermination 20-40 pellets rinsed in filtered seawater were deposited on a GF/D filter and ground in 90% acetone. Organic carbon was measured in 80-100pellets rinsed twice in filtered water and concentrated on pre-combusted GF/Dfilters. The method of wet oxidation of organic carbon with subsequentcoulonometric measurement of CO2 (Lutsarev and Smetankin, 1980) was used.For dry weight determination 100 pellets were filtered on pre-weightedNuclepore filters (1 u-m pore diameter), dried at 60°C, stored in a desiccatorwith silica gel and finally weighed with a microbalance on land. Sinking rates ofpyrosomas fecal pellets were measured in a glass cylinder 50 cm high and 10 cmin diameter filled with surface seawater. Pellets were introduced at the top with apipette and timed as they fell between two marks 40 cm apart.

Fecal pellets incubation

Four portions of 300-500 fresh pellets collected at station 3171 were placed infour vessels with 200 ml surface seawater. The first one was incubated for 18 h at23°C (temperature of mixed upper layer); the second at the same temperatureduring 45 h. The third and the fourth were incubated in a temperature-controlled chamber at 8°C for 48 h and 11 days. At the end of the incubationperiod pellets were examined under light microscope, and their pigment andcarbon content, as well as sinking rate measured as described above.

Results

The population of P.atlanticum at station 3171 consisted of specimens of 50-65 mm length. Our diurnal observations from shipboard showed that pyrosomasconcentrated in the surface layer during the dark period. The first colonies werenoticed at 1700 h, then their number increased and reached a maximum at1900-2000. From this time to 0400-0500 the pyrosomas permanently

Table I. Pyrosoma atlanticum. Gut pigment content at different sampling times at station 3171.Number of pyrosomas examined in parentheses

Time of sampling

1800210024000400Mean value

Size of colonies(mm)

50-5855-6054-6553-63

Gut pigment content(|Ag pigment colony"'x + SD

3.9 + 0.9 (3)2.6 ± 0.7 (3)2.9 ± 0.2 (3)2.7 ± 0 1 (3)3.1 ± 0 8(12)

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inhabited the surface layer. Their horizontal distribution was highly hetero-geneous: zones of high density (on average 9.5 colonies m~3 in the 0-10 m layer)of ~10 m width alternated with zones of low density (on average 0.8 coloniesm~3). At 0700 h pyrosomas abandoned the surface layer and at 1000 h they werefound in the net sample from 100-200 m layer. When we returned to the samelocation 2 months later (station 3171A) we found even denser swarms of 15-21 mm length P.atlanticum. The concentration of colonies at 1900 h was 41colonies m~3 in the 0-10 m layer and 0.26 colonies m~3 in the 10-25 m layer; indeeper layers pyrosomas were absent.

Gut pigment content

The data on gut pigment content of P.atlanticum from the surface layer at station3171 are shown in Table I. The amount of pigment at 1800 was higher than atother times. However, one-way AN OVA showed that the difference betweenthe time series was not significant (F = 1.91, d.f. = 3 and 8, P > 0.05).

Fecal pellets: production, pigment and carbon content

The rate of pellet production was constant in the first 15 min after pyrosomascollection: the difference between the first three successive measurements wasnot significant (Table II). These results suggest that the influence of physicaldisturbance while handling or confinement effect on defecation process wasnegligible and that the defecation rate of P.atlanticum measured in the first 5-15min is a reasonable reflection of in situ defecation rate. After 15 min the numberof egested pellets gradually decreased (Table II), which may be caused bydiminishing food in the experimental vessel.

The total number of pellets produced by one colony is the result of thedefecation process of all zooids and depends on their number. For example, thecolony of ~55 mm length consisted of ~1200 zooids and produced on average1729 pellets h"1; the colony of 18 mm length consisted of 150 zooids andproduced 338 pellets h"1 (Table III). Thus, the average defecation rate of asingle zooid equals 1.4-2.2 pellets h"1. The defecation rates of P.atlanticumamong collections at station 3171 did not differ significantly from those within

Table n . Pyrosoma allanticum. Number of fecal pellets egested by a colony of 55-60 mm size insuccessive 5 min intervals

Time intervals(min)

0-55-10

10-1515-2020-25

Number of fecal pellets(pellets colony"1)x ±SD

105 + 25 (3)137 ± 19 (3)107 ± 4 (3)74 (1)57 (1)

Student's Mest

1.41 (NS)2.12 (NS)

NS = difference not significant at 95% confidence level.

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Tab

le I

II.

Pyr

osom

a al

lant

icum

. D

efec

atio

n ra

te,

feca

l pe

llet

pigm

ent

and

orga

nic

carb

on c

onte

nt.

Num

ber

of r

eplic

ates

in

pare

nthe

ses

Stat

ion

3171

Mea

n va

lue

3171

A

Dat

e

30.0

831

.08

1.09

20.1

0

Tim

e of

sam

plin

g

1800

1800

2100

2400

0400

1900

Size

of

colo

ny(m

m)

49-5

449

-58

51-5

650

-62

50 15-2

1

Def

ecat

ion

rate

(pel

lets

col

ony"

1 h"1)

x ±

SD

1330

± 1

50

(4)

1480

± 1

50

(3)

2166

± 2

49

(3)

2152

± 5

60

(3)

1380

1729

± 4

89 (

14)

338

± 50

(12

)

Feca

l pe

llet

pigm

ent

(ng

pigm

ent

pelle

t"1)

x±

SD

2.1

± 0.

3 (3

)2.

4 ±

0.2

(3)

2.5

± 0.

7 (3

)N

o da

taN

o da

ta2.

4 ±

0.5

(9)

No

data

Feca

l pe

llet

carb

on(M

-gC

pel

let"

1)x±

SD

0.44

± 0

.02

(3)

0.72

± 0

.2 (

3)0.

76N

o da

taN

o da

ta0.

64 ±

0.2

(7)

0.22

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pyrosomas from each collection (one-way ANOVA, F = 2.23, d.f. = 4 and 9,P > 0.05, Table III).

The fecal pellets of P.atianticum were drop-shaped with an average size of0.26 x 0.20 x 0.10 mm and a volume of 0.005 mm3. The main part of a freshpellet content consisted of unidentified small phytoplankton cells of 3-5 u-mdiameter and coccoliths of 7-15 urn. In the larger size classes of phytoplankton,40-150 u.m centric diatoms and 50-60 u.m silico-flagellates were common.Besides phytoplankton cells we often found the fragments of small crustaceansand dense cylindrical-shaped particles of ~100 n-m in length, looking like fecalpellets of copepods.

The dry weight of fecal pellets collected on August 30 was on average 2 ± 1ixg pellets"1. Their organic carbon (Table III) made up 22% of the dry weightwhich is within the range of 12-32.4% for copepod pellets (Morales, 1987) andpractically coincides with 24.4% for salp pellets (Madin, 1982). The pigment andcarbon content of pyrosomas pellets collected at 1800 and 2100 h (station 3171)was practically identical (Table III).

Based on the number of colonies in the water column and the data in Table IIIwe calculated the total number of pellets and the fecal carbon produced by theP.atianticum population during the 10 h of its occurrence in the surface layer.The maximum value of fecal pellets production obtained for dense swarms ofpyrosomas at station 3171 was 1.67 x 106 pellets irT2 10 IT1 or 1035 mg C m"2

10 IT1 (Table IV).

Ingestion and population grazing impact

Assuming that the measured defecation rate is an adequate reflection of in situdefecation rate one can calculate the gut turnover time (Tin h) according to T =(5g/Of Sf): where 5g and Sf are gut and fecal pellet pigment content (u.g pigmentind""1) respectively; Df, defecation rate (pellets h"1). The average gut turnovertime of the colonies at station 3171 equalled 0.75 h. The absence of thesignificant differences in the gut pigment defecation rate and fecal pelletcomposition in different collections at station 3171 suggests that pyrosomas feedat a constant rate. In this case the total amount of pigment ingested by onecolony during the period from 1800 to 0400 can be simply calculated as 41.3 u.gpigment colony"1 10 h"1.

Table IV. Pyrosoma atlanticum. Fecal pellet production of population

Station

3171SwarmNon-swarm

Mean value

3171ASwarm

Number of colonies(colony m"2)

958

51.5

410

Fecal pellet production

pellet m"2 10 IT1

1.67 x 10s

0.14 x 106

0.90 x 106

1.38 x 106

mgCm" 2 10h" '

103587

561

305

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The grazing impact of P.atlanticum while swarming was 53% while the non-swarming was only 4% of phytoplankton standing stock in the 0-10 m layer(Table V). As pyrosomas were concentrated in the upper 10 m, their grazingpressure on the phytoplankton of the whole euphotic layer was considerablylower (Table V).

Fecal pellets incubation experiment

In the incubation experiments the pigment and organic carbon decreaseddramatically at 23°C (Table VI). After 18 h the loss of pigment and organiccarbon was 38 and 28% respectively. After 45 h the fecal pellets lost 72 and 59%of their pigment and carbon content. Microscopic observation revealed manybacteria and a few protozoans inside the feces; their membrane was practicallydisrupted. At 8°C fecal pellets pigment remained unchanged during 45 h butshowed an 83% decrease after 11 days. Though the organic carbon of 11 day oldpellets was the same as the initial value, they were pale and loose with disruptedmembrane. We also observed a great number of microorganisms associated withthese fecal particles.

The sinking rate slightly decreased during 45 h at 23°C, but the differencebetween successive measurements was not significant (Student's f-test,P > 0.05). After 11 days of incubation at 8°C the sinking rate was significantlylower (P < 0.01) compared with that of fresh collected pellets.

Discussion

Pelagic tunicates such as salps, doliolids and appendicularians are ubiquitousthroughout the oceans at generally low densities but sometimes a bloom gives

Table V. Pyrosoma atlanticum. Chlorophyll a concentration, population density and populationgrazing impact at station 3171

Depth Chlorophyll a concentration Density Population grazing impact(m) (n.g I"1) (colony m"3) (% of standing stock ingested per 10 h)

Swarm Non-swarm Swarm Non-swarm Mean

0-10 0.74 9.5 0.8 53 4 28.50-50 0.62 1.9 0.016 12.5 0.96 6.2

Table VI. Pyrosoma atlanticum. Changes of fecal pellet pigment, organic carbon content and sinkingrate during incubation under different temperature. Number of replicates in parentheses

Incubation

Initial18 h at 23°45 h a6 23'45 h at 8°11 days at

condition

C

•cC8°C

Fecal pellet(ng pigmentx ±

2.11.50.62.60.36

SD

±3(3)± 0.15±0.3± 1.1±0.06

pigmentpellet"1)

(3)(3)(3)(2)

Fecal pellet(M-g C pellet

x± SD0.44 ± 0.020.32 ± 0.020.18(1)No data0.44 ± 0.03

carbon- )

(2)(3)

(2)

Sinking rate(m day"1)x± SD

70.0 ± 19.157.2 ± 15.954.0 ± 15.1No data49.4 ± 12.7

(40)(9)(5)

(20)

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rise to a high-density population (Berner, 1967; Wiebe etal., 1979; Deibel, 1982,1988). Our observations, as well as data of Braconnot and Goy (1981), indicatethat pyrosomas may also form immense swarms in the upper layers of the ocean.It seems likely that P.atlanticum swarms may persist at the same location for along time, according to our observations at least for 2 months. The night-timeconcentration near the surface and the lack in the upper 100 m layer during theday suggests diurnal migration of P.atlanticum. Nocturnal ascent of P.atlanticumwas also reported by Braconnot and Goy (1981) in the Ligurian sea and vanSoest (1981) near Bermuda. However, whether diurnal vertical migration ofP.atlanticum is obligatory remains an open question.

Pyrosomas seem to be true suspension feeders. Each zooid collects foodparticles by pumping water through the internal mucous sheet produced by theendostyle. We found that P.atlanticum retained small-sized particles of 3-4 ^m.It is well-known that the tunicates are able to ingest bacteria-sized cells(J0rgensen and Goldberg, 1953; Harbison and Gilrner, 1976; Harbison andMcAlister, 1979). Therefore, we believe that the minimum size of particlesavailable for pyrosomas should be considerably <3 n-m, but under the lightmicroscope we could not recognize them.

One of the important features of tunicate feeding is the extremely highclearance rate (Harbison and Gilmer, 1976; Deibel, 1988; Madin and Cetta,1984). To compare the clearance rate of P.atlanticum and other pelagic tunicateswe calculated it for a colony of 55 mm length. Assuming an ingestion rate of4.1 p-g pigment colony"1 h"1 and a chlorophyll a concentration of 0.74 u,g I"1 inthe 0-10 m layer (station 3171) one colony filters 5.5 1 h"1. This value is withinthe range of 3-7.2 1 ind."1 h"1 predicted by the equation of Madin and Cetta(1984) for Salpa maxima and Pegea confoederata of 55 mm length. The highrates at which pyrosomas ingest available food particles make them theimportant consumers of phytoplankton standing stock particularly when inswarms. Our results showed that the grazing impact of a P.atlanticum populationduring 10 h night-time ranged from <1 to 12.5% (average 6.2%) of totalphytoplankton standing stock (Table V). These values are similar to the fewestimates reported for other pelagic tunicates. Alldredge (1981) found thatpopulation grazing impact of Stegasoma magnum was 5-13% of the standingstock of ingestible food particles per day. Deibel (1988) obtained values from <1to 13% for an Oikopleura vanchoeffenii population. A population of Salpathompsoni removed ~1.4% of phytoplankton standing stock a day (Drits andSemenova, 1989). Significant heterogeneity in vertical and horizontal distri-bution of P.atlanticum during nocturnal feeding, however, resulted in theconsiderable difference in grazing pressure on phytoplankton. We found thatswarms of P.atlanticum removed >50% of phytoplankton standing stock in the0-10 m layer compared with 4% removed by sparsely distributed pyrosomas.Also the population grazing impact in the 0-10 m layer was several times greaterthan calculated for the 0-50 m layer. This 'patchiness' in grazing pressure maycontribute to micro-scale heterogeneity in phytoplankton distribution.

The most striking result of our study is the tremendous number of fecal pelletsproduced by pyrosomas. Though the defecation rate of a single zooid, 1.4-2

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pellets h"1, is much lower than 3-8 pellets h"1 reported for herbivorouscopepods (Marshall and Orr, 1955; Petipa, 1981), the total number of pelletsegested from several hundreds to several thousands units per hour exceeds thevalues known for other plankton animals by a factor of 100. To make clear theimpact of pyrosomas in the fecal pellet flux one can compare their pelletproduction with those of a typical herbivorous copepod, Calanus. Nine coloniesof 50-65 mm m"3 (the concentration of P.atlanticum in swarm at station 3171)produced 1.6 x 104 pellets h"1 which equals the fecal pellet production of 3000-5000 Calanus m~3 at their usual defecation rate of 3-5 pellets ind."1 h"1

(Marshall and Orr, 1955). Such high copepod concentrations were not foundanywhere in the open ocean except in the high productive regions during shortperiods (0stvedt, 1955; Voronina, 1984; Timonin, 1990).

The organic carbon flux resulting from the nocturnal feeding of P.atlanticummade up ~300-600 mg C m~2 day"1. Similar values of 107-576 mg C m~2 day"1

were obtained by Morris et al. (1988) based on the sediment-traps data during aSalpa fusiformis bloom, but other results for fecal carbon flux produced by salpswas considerably lower from 0.01-0.05 mg C m~2 day"1 (Caron et al., 1989) to8.5-135 mg C m"2 day"1 (Wiebe et al., 1979).

Of course, the fate of fecal material and its role in the vertical flux of organicmatter is significantly influenced by microbial decomposition and sedimentationrate. Pomeroy et al. (1984) found that fecal pellets of the small neritic salps anddoliolids were degraded by bacteria and protozoans in 2-3 days. Data forcopepod pellets suggest a carbon loss of 16% in the first day and 67% by thesecond day at 22°C but only 10% loss over 14 days at 5°C (Turner, 1979). Ourexperimental studies on pyrosoma pellets also demonstrated that theirdegradation rate was quite rapid at 23°C (pigment and carbon loss of ~60% bythe second day) but much lower at 8°C. The sinking rate of P.atlanticum fecalpellets is similar to a value of 70 m day"1 measured by Dunbar and Berger(1981) for the presumed salp fecal pellets of 0.006 mm3 collected from sedimenttraps, but twice as low as would be expected from their volume according to theequation of Small et al. (1979) for ellipsoidal copepod pellets. The aging ofpyrosomas fecal pellets had no pronounced effect on their sinking rate: thesignificant decrease of 30% was found only after 11 days of incubation.

In the region studied, the 20°C isotherm was found shallower than 150 m andthe 8°C isotherm deeper than 300 m. Sinking pyrosoma fecal pellets wouldspend 2 days in warm surface waters, which coincides with the period of theirsignificant microbial decomposition. So it seems hardly possible that pyrosomafecal material plays an important role in vertical transport of organic matter.Only an insignificant part of the pellets produced by the descending coloniesduring their daytime migration may reach deeper low temperate layers. Themain part of pyrosoma pellets most likely does not leave the upper watercolumn. Fecal material not reingested by coprophagy can be consumed andrespired through the microbial action with relatively rapid and substantiverelease of dissolved organic and inorganic nutrients (Pomeroy et al., 1984). Thisremineralization process is probably very important for a regenerated primaryproduction regime particularly in the nutrient-poor tropical waters.

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The present results are the first attempt to estimate pyrosoma grazing pressureon the phytoplankton and their role in the organic matter flux. Theydemonstrate that local pyrosoma swarms may be important determinants ofphytoplankton abundance and its micro-scale distribution. The enormousamount of fecal material produced by pyrosomas is principally degraded in theupper water column, which suggests their importance in the recycling. However,more and better information on the distribution, abundance, 'patchiness', aswell as feeding behaviour of pyrosomas is needed for more accurate estimationof their role in trophodynamics of pelagic ecosystem of the open ocean.

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Received on May 24, 1991; accepted on December 14, 1991

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Pyrosoma atlanticum (Tunicata, Thaliacea): grazing impact on phytoplankton standing stock and role in organic carbon flux