Picoplankton and nanoplankton aggregation by appendicularians: Fecal pellet contents of Megalocercus huxleyi in the equatorial Pacific G Gorsky, Mj Chretiennot-Dinet, J Blanchot, I Palazzoli

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G Gorsky, Mj Chretiennot-Dinet, J Blanchot, I Palazzoli. Picoplankton and nanoplankton aggregation by appendicularians: Fecal pellet contents of Megalocercus huxleyi in the equatorial Pacific. Journal of Geophysical Research. Oceans, Wiley-Blackwell, 1999, 104 (C2), pp.3381-3390. ￿10.1029/98JC01850￿. ￿hal-03284913￿

HAL Id: hal-03284913 https://hal.archives-ouvertes.fr/hal-03284913 Submitted on 14 Jul 2021

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Copyright JOURNAL OF GEOPHYSICAL RESEARCH, VOL. 104, NO. C2, PAGES 3381-3390, FEBRUARY 15, 1999

Picoplanktonand nanoplanktonaggregation by appendicularians- Fecal pellet contentsof Megalocercushuxleyi in the equatorial Pacific

G. Gorsky,• M. J.Chr•tiennot-Dinet, 2J. Blanchot, 3and I. Palazzoli•

Abstract. The contentof fecal pelletsof the freshlycollected warm water appendicularian Megalocercushuxleyi was studiedby light and electronmicroscopy and by flow cytometryin the superficial100 m of the water columnat 2øN, 165øE,in September1994, duringthe Flux dans l'Ouestdu ?acifiqueEquatorial (Joint Global OceanFlux Study-France)oceanographic cruise. Microscopicobservations showed that the fecal pellet contentsof M. huxleyireflected the natural compositionof the nanophytoplanktonand small microphytoplankton(<50 [tm). Larger cells were excludedfrom enteringthe filtering systemby the inlet filters. Coccolithophoridsappeared as the main componentfound in the feces.Evidence for ingestionof"naked" cellsby this appendicularianis given. Analysisof picoplanktonin fecal pelletsby flow cytometerconfirmed that appendiculariansefficiently collectsmall particles. Cyanobacteria, -1 gm in diameter,were found in large quantitiesand showedhigh fluorescencein the fecal pellets.Most of these cyanobacteriain the pelletsappeared to be intact,and thusmay be good indicatorsof the appendicularianingestion rate. The situationwas differentfor the prochlorophyteProchlorococcus abundantin the seawaterand for picoeucaryotes(<2 gm). Thesewere foundat very low quantities in the larvaceanfecal pellets.The calculationsshowed that with an averageconcentration of 5 3//. huxleyim -3, >7% of thesmall particulate matter will bedaily removed from the water. Some of thismatter will be assimilated,some trapped in the houses,and the restaggregated into rapidly sinkingfecal pellets.Ingestion of largequantities of coccolithophoridsindicates that appendiculariansare importantnot only in the cycleof organiccarbon but alsoof inorganic carbon.Moreover, if appendicularianssuccessfully aggregate and assimilateœrochlorococcus and picoeucaryotes,then their grazingactivity can representa major pathwayof carbontransformation in the tropical ecosystem

1. Introduction develop mechanisms for efficient adaptation to nutritionally dilute or to "extreme" environmental conditions. Pelagic The pelagic filter feeding , appendicularia(= tunicatesare consideredto be nonselectivegrazers, collecting ),are an importantcomponent of the neritic food web. particlesby sieving and also by direct interceptiononto filter Their importanceis consideredinsignificant in openocean or in fibers [.4curiaet al. 1996]. Appendicularianspump water oligotrophic environments. Reports made from manned throughexternal and internal mucous nets in extrudedgelatinous submersiblesin the 1960s [see Barbara, 1979] and recent houses.Colloids >0.1 [tm and otherlarger particles are retained discoveriesof larvaecanpopulations auttptcu...... to ttpnouc oceanic and ingested[Fenaux, i986; Flood et ai.,,j992]. The retention environmentswith low food supplycontradict this view [Fenaux efficiencyis determinedby thepore size'•of the internalnet. It and Youngblurb, 1990; Gors192et al. 1991; Hamnet and generally exceeds90% for particles>3 [tin [Deibe! and Lee, Robison,1992]. Flood 1978, Flood et al. [1992], Deibel and Lee 1992]. The gut passagetime of larvaceansis rapid, and fecal [1992], and Bedo et al. [1993] documentedthe capabilityof pellet productionis high [7'aguchi,1982]. Fecal pellets are appendiculariansto shortcut the microbialfood web anddirectly compactand ellipsoid (Figure l a) and are numerousin sediment feed on submicronicparticles. Hopcroft and Roff [1995] traps [Urrare and Knauer, 1981; Buck and Newton, 1995]. describedthe rapid populationgrowth of larvaceansin warm Megalocercushuxleyi's maximumtrunk size can reach 5 mm, waters. These characteristics indicate that larvaceans can andthe housediameter of adultspecimens can reach more than 3 cm. Appendiculariansfeed continuously.The housesecretion is •ObservatoireOc6anologique, Universit6 Pierre et Marie also a continuousprocess (the daily houseproduction varies Curie/CentreNational de la RechercheScientifique/Institut National des from I to >10 dependingon speciesand temperature [see Flood Sciencesde l'Univers, Villefranche sur ruer, France. and Deibe/, 1998]). Thus, becauseof the rapid population 2ObservatoireOc•anologique de Banyuls,Laboratoire Arago. Laboratoired'Oc•anographie Biologique, Universit• Pierre et Marie growth basedon the short life cycle (<2 days in 29øC for Curie/CentreNational de la RechercheScientifique/Institut National des Oikopleuradioica [seeHoptcrofi and Roll, 1995]) and because Sciencesde l'Univers, Banyulssur mer, France. of three mechanismsrelated to their feedingbiology, (1) 3L'Institut Fran•ais de RechercheScientifique pour le retentionand ingestionof picoparticles,(2) continuoushouse Daveloppementen Cooparationde Noum•a, Noum•a, New Caledonia, France. secretion.and (3) high fecal pellet productionrate, the role of larvaceansin theprocesses of aggregationcan be importanteven Copyright1999 by the AmericanGeophysical Union. in weakly productiveenvironments. Studies on the content of larvaceanfecal pellets and its Paper number 98JC01850. comparisonwith natural sestonare few. The first observations 0148-0227/99/98JC-0185059.00 of the ingestedmatter were made by Lohmann [1909], who

3381 3382 GORSKY ET AL.: PICOPLANKTON AGGREGATION BY APPENDICULARIANS

describeda new size classof plankton,the nanoplankton,while from the rectdm and intestines of freshly caught adult studyingthe gut contentof appendicularians.Alldredge [1977] individuals. showedin the Gulf of Californiathat largephytoplankton cells were oftenexcluded by the inlet filtersfrom enteringthe house. 2.2. Light Microscopy The internalfeeding filters contained diatoms and dinoflagellates in much lower proportionsthan in sea water. Accordingto A subsampleof fecal pelletswas immediatelyobserved with Alldredge [1977], 75%-96% of the materialin the gut and in a Leitz dialux 20 microscope,equipped with a HBO 50 light fecal pellets was composedof naked flagellatesand small sourceand a Ploemopak2.4 vertical illuminatorcontaining a particles.Coccolithophorids were also abundant in the gut,often 450-490 nm bandpath filter and excitingblock (Figure lb). For in higherproportion than in seawater.Deibel and Turner[1985] the studyof naturalphytoplankton, 250 mL seawatersamples studiedthe sizeof food in fecalpellets and compared it to the werefiltered through 0.8 gm nucleporemembranes. A few drops pore size of the inlet filters. They also comparedthe size and of 37% formaldehyde(Sigma) were addedduring the filtration type of particlesin fecal pellets with those in the environment. for cell fixation.The membranewas then placed upside down on Urban et al. [1992] describedthe seasonaldifferences in the a slide that had been coated with a poly-L-lysine(Sigma contentand composition of Oikopleuravanhoeffeni fecal pellets Diagnostics), an adhesive solution allowing collection of in coastal Newfoundland waters. materialon the slide.After removingthe excesswater the filter The surface waters of tropical oceanic provincesare waspeeled off, anda dropof liquidgelatin was deposited on the dominatedby phytoplanktonof extremelysmall size. In the filteredmaterial. A coverslipwas placed on the preparationand equatorialPacific, 50%-60% of the chlorophyllbiomass is wassealed when the gelatinsolid;fled. Slides were kept at room containedin the <1 [tm size fraction [Chavez, 1989; Le temperaturein the dark and viewed onboardwith the dialux or Bouteilleret al. 1992]. Prochlorococcus[Chisholm et al. 1988, backat the Laboratoryin Banyulssur mer, France,with a Zeiss 1992] seemsto contributethe majorpart of the chlorophyllof microscope,usually at x400 magnification.The contentof the thisfraction even in the equatorialupwelling zone [Landry et al. sampleswas displayed on a colorSony video system fitted to the 1996]. In the westerntropical Pacific, Blanchotand Rodlet microscopeand printed on a Sonyvideo graphic printer UP-850. [1996] foundthe highestProchlorococcus concentrations in the This transfermethod allowed only a semiquantitativestudy of superficial,oligotrophic, nitrate-depleted layer. M. huxleyiwas thenatural populations and was used to comparethe taxa present repeatedlyfound in high concentrationsin the superficial in the water columnand in the feces.Quantitative estimation of equatoriallayer in the studiedzone (Etude du Broutageen Zone diatompopulations was made by scanningelectron microscopy Equatorialecruise 1996 (G. Gorskypersonal observation, 1996)) (SEM) and publishedby Blain et al. [1997]. Other filters have andwas alsodescribed in the easternPacific [Alldredge, 1977]. beenused in similar conditions,and it appearsthat this method In the presentstudy we reporton the contentof the warm water givesa goodaccount of the phytoplanktonpopulations present in M. huxleyi fecal pellets compared to the natural the water and of their relative abundance. picophytoplanktonand nanophytoplankton populations. 2.3. ScanningElectron Microscopy 2. Material and Methods For SEM observations,fecal pelletswere placedon filters,

2.1. Collection andfor naturalphytoplankton, 2q0 mL seawatersamples were filteredthrough 0.8 [tm nucleporemembranes. The membranes were rinsed with distilled water to remove salt and then were air Different appendicularianspecies were collectedduring the Flux dans l'Ouest du Pacifique Equatorialoceanographic dried.They were later mounted on stubs,coated with gold,and cruisecarried out in the tropicalPacific (between20øS and 6øN examinedin a HitachiS 520 scanningelectron microscope in Perpignan,France. along 165øEand 165øE-150øW),from September23 to October 29, 1994. Vertical zooplanktontows were donewith a 200 2.4. Taxonomy mesh pore size Working Part II (Scientific Committee on Oceanic Research) UNESCO, 1968) zooplankton net. Phytoplankton species identification and classification Hydrocastsand water samplingwere madewith a Seabird SBE followingChrdtiennot-Dinet et al. [1993] are givenin Table 1. 9 CTDO2/Rosette system.Nitrate and nitrite analyseswere Taxa arepresented alphabetically with the suffix"-phyceae" for performed onboard with a technicon autoanalyserII [see classesand "-ales" for orders.Coccolithophorid species were Leborgneet al. 1995]. M. huxleyifecal pelletswere dissected identifiedaccording to dotdanand Green [1994] and diatoms

Figure 1. Light microscopy(LM): (a) a compactand ellipsoidfecal pellet of Megalocercushuxleyi characterizedby its surroundingmembrane (arrow)(magnified 130 times), (b) a coccosphereof Discosphaera tubifera(arrow) (Prymnesiophyceae), in the fecalpellet (magnified 870 times)(alsoillustrated in scanning electronmicroscopy, Figure 4a), (c) a smallcolony of Phaeocystissp. (arrow)Prymnesiophyceae and the phycomaphase of Pterospermacf. moebii(P) (Prasinophyceae)(magnified 870 times),(d) disassociated coccolithsof Rhabdosphaeraclavigera variety stylifera (Prymnesiophyceae)(magnified 870 times),(e) one of thesmallest dinoflagellates, Heterocapsa sp. (arrow) (Dinophyceae) (magnified 870 times)(also illustrated in SEM), (f) two small dinoflagellates:Oxytoxum elongatum (arrowhead) and Gymnodinium(arrow) (Dinophyceae)(magnified 870 times),(g) two cellsof Thalassiosiraoestrupii (Diatomophyceae) (magnified 870 times)(also illustrated in SEM, Figure4d), and(h) loosecoccoliths of Umbilicosphaerasibogae (U) (Prymnesiophyceae)and Nitzschia bicapitata (N) (Diatomophyceae)(magnified 870 times)(also illustrated in SEM, Figures3b and 3d for U. sibogae). GORSKY ET AL.: PICOPLANKTON AGGREGATION BY APPENDICULARIANS 3383

Figure 1. 3384 GORSKY ET AL.: PICOPLANKTON AGGREGATION BY APPENDICULARIANS

Table 1. List of PhytoplanktonicSpecies found in Megalocercushuxleyi Fecal Pellets(M.h) and in AdjacentWaters (A.W.). Phytoplankton Location Chrysophyceae Meringosphaeramediterranea M.h m.w. Diatomophyceae Bacteriastrumhyalinum m.w. Unidentifiedaraphid diatom M.h A.W. Azpeitia neocrenulata M.h A.W. Chaetoceros concavicornis A.W. Chaetoceros lorenzianus A.W. Mastogloia rostrata A.W. Oxytoxumovale M.h A.W. Oxytoxumreticulatum A.W. Oxytoxumscolopax A.W. Oxytoxumstropholatum A.W. Paleophalacromaunicinctum A.W. Prorocentrum nahum M.h A.W. Protoperidiniumspp. M.h A.W Prasinophyceae Pterospermacf. moebii M.h m.w. Prymnesiophyceae Coccolithophorales A canthoicaacanthif era A.W Ceratolithuscristatus variety telesmus A.W Coronosphaeramediterranea M.h A.W Gaarderia corolla A.W. Anoplosoleniabrasiliensis M.h A.W. Calcidiscusleptoporus M.h A.W. Discosphaeratubifera M.h A.W. Emiliania huxleyi M.h A.W. Gephyrocapsaoceanica M.h A.W. Homozygosphaeratriarcha A.W Michaelsarsiasp. M.h A.W. Oolithotus antillarum M.h A.W. Rhabdosphaeraclavigera variety stylifera M.h A.W. Syracosphaerapulchra M.h A.W. Umbellosphaerairregularis M.h A.W. Umbilicosphaerahulburtiana M.h A.W. Umbilicosphaerasibogae M.h A.W. Prymnesiales Phaeocystissp. [colonialstage] M.h A.W.

accordingto Hasle and Syvertsen[1995]. Dinoflagellateswere chlorophyll), orange (OF, phycoerythrin),and green identifiedaccording to Balech[ 1988]and Steidinger and Tangen fluorescence(GF, phycourobilin)were recorded[Wood et al. [ 1995].Dodge [ 1985] andHallegraeff[ 1988]were used for their 1985; Olsonet al. 1988]. The 2 gm Polysciencesfluoresbrite SEM illustrations.Phaeocystis were not identifiedto the species beads(category 18604) were used for calibration,and the Lysis level sincethis groupis underst,•dy. For the taxonomyof this II softwarewas used for signalanalysis. Fecal pelletswere genus,see Vaulot et al. [1994] and Lange et al. [1996]. The homogenizedin ultrasonicbath for 5 min and vortexed for 3 Pterospermaspecies was referredto moebiias definedby Parke min. Seawatercontrols were treatedthe sameway and were et al. [ 1978]. comparedwith nonhomogenizedseawater samples. As no difference was noticed between homogenized and 2.5. Flow cytometry nonhomogenizedseawater, we concludedthat the treatmentdid not alter the examined particles, either qualitatively or Seawateranalyses with a flow cytometer(FCM) were made quantitatively. onboardon 0.1 mL samplesusing a FACScanflow cytometer (Becton-Dickinson)equipped with an argonlaser (15 mW at 488 3. Results nm) as describedby Blanchotand Rodlet [1996]. GF/F filtered deep-seawater from 1000 m was used as the shear fluid. Size The upper 70 m were warm, between28 ø and 29øC and N- side scatter(SSC), forwardlight scatter(FLS), and red (RF, depleted(Figure 2). The chlorophyllmaximum was at 80 m. The GORSKY ET AL.' PICOPLANKTON AGGREGATION BY APPENDICULARIANS 3385 beam attenuation maximum matched that of the fluorescence but Pterospermaphycoma (Figure 1c), which were not abundantin was less marked when comparedto the values obtainedin the the watercolumn, were presentin the feces. upperlayer. Flow cytometer analysis of picoplankton showed that the Table 1 lists species found in the fecal pellets of the Prochlorococcus maximum occurred between 40 and 80 m appendicularianM. huxleyias well as the phytoplanktonspecies depth (Table 2). The cyanobacteria were two orders of observedin the surroundingwaters at 2øN, 165øE, September magnitude less abundant than the Prochlorococcusand were 30, 1994, during the FLUPAC oceanographiccruise. Some homogeneously distributed in the 0-90 m layer. The illustrationsof thesespecies are foundin Figures1, 3, and4. picoeucaryotemaximum occurred between 70 and 140 m (Table In the water columnthe dominantphytoplankton components 2). were coccolithophorids,particularly Discosphaera tubifera Flow cytometry of disrupted fecal pellets confirmed the (Figures 1b and 4a), Umbilicosphaerahulburtiana, potentialof larvaceansto efficientlycollect small particles.The Gephyrocapsaoceanica, Achanthoica acanthifera and cyanobacteriumSynechococcus,-1 [tm in diameter,occurred in Homozygosphaeratriarcha, but diatomsand dinoflagellates largequantities and was stronglyfluorescent in the fecal pellets. were also well represented.The small diatom Nitzschia It seemstherefore that most of these cyanobacteriawere intact, bicapitata(6 x 2.5 pm, Figureslh and 3b) was numerically althoughembedded in the pellets.The situationwas differentfor dominantfrom 0 to 90 m, a featurealready noticed by Lee and the Prochlorococcus population abundant in the seawater Fryxell [1996] and Blain et al. [1997]. Many small (Figures5a and 5b) and for the picoeukaryotes(<2 pm). Both dinoflagellateswere presentat 40 m, with severalspecies of groupswere found in very low quantitiesin the larvaceanfecal Oxytoxum(Figure 4b) and the minuteHeterocapsa (Figure 4c) pellets(Figures 6a and6b). as typical nanoplanktonicrepresentatives. A silicoflagellate, Dictyochafibula, was also abundantat 40 m. Microplanktonic 4. Discussion and nanoplanktoniccells were concentratedin the fecal pellets. Diatoms,dinoflagellates, and coccolithophoridswere recognized The fecal pellet contentsof M. huxleyireflected the natural in light microscopy(Figure 1), and in (SEM) (Figures3 and4). compositionof the nanophytoplaktonand small phytoplankton The use of SEM proved to be particularlyimportant for the (<50 gm). Larger cells or particles such as the diatom identification of small coccolithophorids(<10 pm) such as Rhizosolenia were excluded from entering the house of Gephyrocapsaoceanlea, Eratitania huxleyi (Figure 3b) and Megalocercushuxleyi by the inlet filters. Coccolithophorids Oolithotusantillarum (Figure 3c). That was also the case for appeared as the main componentremaining in the feces. Nitzschiabicapitata, an ubiquitousspecies in the water column. Evidenceof othernaked cells ingestedby this appendicularianis Coccospheresand loose coccolithswere the most abundant the presenceof Phaeocystisand Pterospermain the fecal pellets, elementsin the feces(Figure 3a), but small dinoflagellates<20 observedonly shortly after the collection of living specimens. pm (Figures l e, l f, 4b, and 4c) and small diatoms were also The concomitantdetection of picoeucaryotesby flow cytometry numerous(Figures l h,3d,and4d). Althoughlarger cells suchas is a clear indicationthat the diet of Megalocercusalso includes Protoperidinium or Dinophysis were occasionally observed, flagellatesand coccoidcells devoid of siliceousor calcareous cellsfound in the fecesnever exceeded 50 [tm. It is interestingto cell walls, which representan importantsource of food for these note that the fragile Phaeocystiscolonies (Figure l c) and filter feeders.

Oxygen(pM kg'l) PAl*,(pE m'•s's) Chlorophylla (mg m '•) 0 50 1O0 150 200 10'l 10ø 10• 10• 10a 104 0 0.1 0.2 0.3 0.4 0.5 0.6 ! I_ I: I i I I,..,I .... I .... Salinity (ø/oo) ,q,,o(','• ,.-') Nilrile 33.5 34.0 34.5 35.0 35,5 36.0 36.5 o.o I 0.03 o. 1 0.3 1 0 0.25 0.5 0.75 1.0 1.25 1.5 I ..... I , , i • J., ,.I.,..I,..,I..,,I.,,,I...,i Temperature(øC) . Nitrate (i,M) •o 1• •o •s •o 0.3 0.35 0.4 0.45 0.5 0 5 10 15 20 IllIll IIIJ IIII Jl l'l I J '; 0 . . J I ?' f t • i 5O )'x' / 'i ' 50 •X•...•..•:• ..,' t,, "'""'"'1 ,,,,'" ß• .•. "•. , .. 100 100 "•'•'% •'"" /, oo: .....';i t ../' / ..•_•' ...e"" / %X i ,/ : ß' .,,,.,,• ß 150 :

200 ' • ( J 200- 200 . / : ß øe'• _ , I 250 . • i • 250 : ., .... gluoI :' : ..• --- n.att.J --••.• 300 300' O2,S,T PAR, Fluo, Beam att. Chl a,NO2,NO3 Figure 2. Depthprofiles of the physicaland chemicalparameters at the studiedsite in the equatorialPacific (2øN, 165øE)during the Flux dansl'Ouest du PacifiqueEquatorial oceanographic cruise September 30, 1994. 3386 GORSKY ET AL.' PICOPLANKTON AGGREGATION BY APPENDICULARIANS

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Figure3. Scanningelectron microscopy (SEM) of fecalpellet contents: (a) a partlycollapsed fecal pellet of M hz•xleyiand its algaecontents, at low magnification,(x 360), (b) coccolithsof Umbilicosphaerasibogae varietysibogae (double arrow) embedded in mucouswith Nitzschiabicapitata (N), (magnified2000 times), (c) two coccospheresof very smallcoccolithophorids Oolithotus antillarum (O) andEmiliania huxleyi (E), (Prymnesiophyceae)(magnified 6000 times),and (d) coccolithsof Umbilicosphaerasibogae (U) and small unidentifieddiatoms (D) (magnified4800 times). GORSKY ET AL.' PICOPLANKTON AGGREGATION BY APPENDICULARIANS 3387

Figure 4. SEM examplesof phytoplanktonicspecies found in the water columnand in the feces:(a) intact coccosphereof Discosphaeratubi•ra (Coccolithophorid,Prymnesiophyceae) (magnified 6000 times), (b) Oxytoxumovale (Dinophyceae,dorsal view) (magnified4200 times), (c) Heterocapsasp. (Dinophyceae, ventralview) (magnified7200 times),and (d) Thalassiosiraoestrupii (Diatomophyceae) (magnified 7200 times). GORSKY ET AL.: PICOPLANKTON AGGREGATION BY APPENDICULARIANS 3387

Figure 4. SEM examplesof phytoplanktonicspecies found in the watercolumn and in the feces:(a) intact coccosphereof Discosphaeratubifera (Coccolithophorid, Prymnesiophyceae) (magnified 6000 times), (b) Oxytoxumovale (Dinophyceae,dorsal view) (magnified4200 times),(c) Heterocapsasp. (Dinophyceae, ventralview) (magnified7200 times),and (d) Thalassiosiraoestrupii (Diatomophyceae) (magnified 7200 times). GORSKY ET AL.: PICOPLANKTON AGGREGATION BY APPENDICULARIANS 3389

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Figure 6. (a). Dot plot of red fluorescence(y) versusorange fluorescence (x) in the appendicularianfecal pellets.Arrows are as in Figure 5a. (b) Histogramof relativecell densitiesversus the red fluorescenceof the appendicularianfecal pellets. Arrows are as in Figure5a. Note the disappearanceof Prochlorococcusin feces when comparedto the in situ situation. recognizablepicophytoplanktoni,, group (Figures6a and 6b). The ingestionof largequantities of coccolithophoridsby M. Synechococcusare efficiently concentratedinto pellets by huxleyiobserved during this studycorresponds to observations larvaceans.In the superficial0-80 m layerwe found,•3000 cells made in the north Atlantic on anotherlarge appendicularian mL-•, andin one fecal pellet their concentration reached 280,000 species[Deibel and Turner, 1985; Urban et al. 1992, 1993]. cells.Supposing that they are not or are only slightlydegraded Despite the fact that the Prochlorococcuscells display the during the transitionthrough the appendiculariandigestive highestconcentrations in seawaterthey are almostcompletely system(their fluorescence in the fecalpellets is almostsimilar to absentfrom the M. huxleyifecal pellets.Their size is closeto that in the seawater),the fecal pellet Synechococcusversus that of Synechococcus,and thus it seemsreasonable that they naturalseawater Synechococcus ratio may be a goodindicator of wouldbe retainedby the appendicularian'sfeeding filters with the larvaceaningestion rate. In our studyone fecalpellet would nearly the same efficiency as demonstratedabove for the contain cyanobacteriafrom ,•93 mL of seawater.We could not Synechococcuspopulation. Deibe! and Lee [1992] foundthat O. measurethe rate of fecal pelletproduction, but we observedthat vanhoeffeni, a large appendicularian inhabiting the four fecal pelletsare simultaneouslypresent in the digestive Newfoundlandwaters, retain colloidal plastic spheres, 0.6 lamin systemof one adult M. huxleyi, correspondingto 372 mL diameter,with an efficiencyof 44%. Thuswe hypothesizethat seawater.According to Alldredge[1977] the calculatedflow rate the Prochlorococcusare successfullyingested and assimilated throughthe housefor M. huxleyiin the Gulf of Californiais by the appendicularians.To test this, one would need to collect between594 and 1188 mL h -•. Assumingthat in M. huxleyione larvaceanhouses using new methodsbecause larvacean houses fecal pellet is formedevery 10 min (the mean value for the fecal are very fragile and are destroyedby plankton nets. Flow pellet productionof the large Oikopleuraalbicans with the trunk cytometricanalysis could then be usedon the housefilters. If the length>3 mm at 14øC was one fecesevery 9 min, G. Gorsky proportionof the picoplanktoniccomponents in the house personalobservation, 1997), the contentof 558 mL of seawater reflectedthat in theseawater, this hypothesis could be accepted. per hour will be packedin the feces,incorporated in body tissue, If so, it would demonstratethe extraordinaryadaptive and usedas energysupply. The metabolicinfluence of the high capabilitiesand importance of a?pendiculariansin the tropical water temperature(29øC) and the amountof matter filtered but ecosystem. not ingestedare not taken into considerationhere. Thereforewe The ubiquityof appendiculariansin oceanic ecosystems and can assumethat the rate of 558 mL h-• is a low estimate.In some their high clearancerates are of great biogeochemical Mediterraneanintermediate and deep layers the concentrations significance.The major contributionof coccolithophoridsto of largeendemic oikopleurids reached 5 individuals m-3 [Gotsky theirfecal pellets indicates that appendicularians are important et al. 1991; M. Youngbluthpersonal comunication, 1991]. We in thecycling of bothorganic and inorganic carbon in thesea. considerthat this concentrationallows successfulreproduction and ensuresthe survival of the population.If the concentration of M. huxleyireaches 5 individualsm'3, morethan 7% of the Acknowledgments. The FLUPAC cruise was coordinatedby small particulate matter will be daily aggregated,used in JGOFS-Franceas a contributionto the JGOFSinternational study of the equatorialPacific. It was supportedby IFREMER France,INSU/CNRS, metabolic processes,compacted into rapidly sinking fecal andby ORSTOM. Shiptime was coordinatedby GENAVIR/IFREMER. pellets, or trapped in the abandonedhouses forming large We thankthe crewof R/V Atalanteand the chiefscientist, R. Leborgne suspendedaggregates in the water column. from ORSTOM, Noumda,for theirefficient acting during the cruise. 3390 GORSKY ET AL.: PICOPLANKTON AGGREGATION BY APPENDICULARIANS

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