Plankton Biol. Ecol. 48 (2): 133-135, 2001

plankton biology & ecology

£' The Plankton Society of Japan 2001 Note

Feeding of the pelagic tunicate, Salpa thompsoni, on flagellates and size-fractionated chlorophyll particles

JUN NlSHIKAWA1 & ATSUSHI TSUDA1'2

'Ocean Research Institute, The University of Tokyo, Minamidai. Nakano, Tokyo, 164-8639 Japan 2present address: Hokkaido National Fisheries Research Institute, Katsumkoi, Kushiro, Hokkaido 085-0802 Japan

Received 20 December 2000; accepted 9 March 2001

The pelagic tunicate, Salpa thompsoni is oneof the key the experiments (Table 1). The buckets with salps and surface macrozooplankton species in the Southern Ocean, exhibiting seawater (temperature at 3°C with no remarkable change dur large biomass stocks at various locations, mainly in the ing experiments) were incubated without any additional ma oceanic region (e.g. Piatkowski et al. 1994; Table 3 in nipulation on deck under natural light conditions. The surface Nishikawa et al. 1995; Chiba et al. 1998; Perissinotto & seawater without salps was used as a control. Incubations Pakhomov 1998a). However, trophic relationships concerning lasted 2 or 4 h. At the beginning and the end of the experi this antarctic salp are poorly understood, both concerning its ments, seawater samples were taken from both experimental predators and prey. Feeding studies on salps from other oceans and control buckets. The concentrations of flagellates and that have clarified that: they are typical filter feeders using mucous of chlorophyll-a were measured. For the total flagellate counts, feeding nets (Madin 1974), and are able to feed upon various 100 ml of the seawater was preserved with gultaraldehyde size ranges of particles from 3-4 fim to lmm (Harbison & (final concentration was 2%) and 2 to 5 ml of the samples were McAlister 1979; Kremer & Madin 1992). Reported clearance rates for mid-latitude salps are several liter animal"1 h~\ and Table 1. Grazing experiments on salps. Filtering rate on size- much higher than almost any other zooplanktonic grazer, on an fractionated chlorophyll-a and on flagellates are shown for the five individual basis (Madin and Deibel 1998). However, informa blastozooid chains. tion on the feeding ecology of antarctic salps is still limited. For Salpa thompsoni, clearance rates have been studied On chlorophyll • On flagellates Exp. number (Reinke 1987; Huntley et al. 1989; Perissinotto & Pakhomov (ml h"1 indiv.-1) 1998b). However, the particle-size range that canbe utilized by 1 (BL40mm, 5 indiv.) 0.2-2^ 257 5. thompsoni has not been reported, even though this may be 2-20/i 118 208 important in characterizing their unique trophic niche as >20/J 75 macrozooplankters in antarctic off-shore food-webs. The goal Total 75 of our study is to clarify the mechanism by which 5. thompsoni 2(BL34mm, 13 indiv.) 0.2-2 33 maintain large stocks in the Southern Ocean. In this study, 2-20 90 43 feeding characteristics such as clearance rates and ingestable >20 45 particle-size ranges are investigated. Total 47 All collections and experiments were carried out during the 3 (BL 20 mm, 65 indiv.) 0.2-2 failed Southern Ocean Expedition of the R/VHakuho Mam K.H-94- 2-20 7 65 4. Grazing experiments were carried out at a station (64°IO'S, >20 2 140°40'E) north of the Antarctic Divergence from 11 to 12 Total 1 4 (BL 35 mm, 13 indiv.) 0.2-2 60 January 1995. Since salps are fragile animals that can be dam 2-20 94 190 aged by ordinary net sampling, swimming chains of salps were >20 92 scooped up gently using 20-liter buckets lowered from the Total 91 deck during thenight when they moved up to the surface. Five 5 (BL 34 mm, 3 indiv.) 0.2-2 42 salp chains, consisting of 3 to 65 blastozooids, with body 2-20 61 368 lengths (oral-atrial distance) from 20 to 40 mm were used for >20 55 Total 55 Corresponding author: Jun Nishikawa; e-mail, [email protected] J.NlSHIKAWA& A.TSUDA 134

DAPI-stainedandthereafterfilteredontoblack-stainedNucle- >20jUm 2020 oporefilters(2{imopening).Thestainedflagellateswereenu 600 meratedwithanepi-fluorescencemicroscope(ZeissAxio- plan).Toexaminethesizerangeofparticlesuponwhichsalps canfeed,threesizecategoriesofchlorophyJl-acontainingpar ticles;0.2-2.0,2.0-20,and>20^imwereused.Sizefractiona- tionofchJorophyllparticleswasdoneusingascreen(20-/xm mesh)andNucleoporefilters(0.2and2.0/im).Thechloro phyllconcentrationineachfractionwasdeterminedafterex

tractioninN,N-dirnethylformamideandwasmeasuredwitha

fluorometer(TurnerModel111).Clearancerateswerecalcu

latedaccordingtoFrost(1972).

Duringtheexperiments,nosignificantchangesineitherthe

ControlExp.1 Exp.2 Exp.3 Exp.4 Exp.5 chlorophyll-aconcentrationofeachsizefractionortheflagel

lateconcentrationswereobservedinthecontrol.Insituseawa- Fig.1.Sizefractionatedchlorophyll-aconcentrationsinthe

terusedforthegrazingexperimentscontainedpredominatelysurfacewaterusedforsalpfeedingexperiments.

microplankton(>20jum),mostofwhichwerediatoms(Fig.

1).Theclearancerateofsalpsoninsituflagellatesvariedfrom

43to368mlindiv."^"1(Table1).Clearanceratescalculated

1000 forflagellatepreywerehigherthanthoseforchlorophyllparti

cles.Nano-sizedparticlesweremostfrequentlygrazedin4out

of5 cases,butwide a sizerangefrompico-tomicro-sized

phytoplanktonweregrazedatonlyslightlyslowerrates.Fecal 100 CD

pellets,whichwerefragileandamorphousparticles,wereob 1 servedatthebottomoftheexperimentalbucketattheendof

theexperiments. 10

Thelowerclearanceratescalculatedforchlorophyllparti

clesmayhave beenpartiallycausedbyre-suspensionoffecal

pelletmaterial.Althoughwegentlyagitatedandsampledthe O

waterattheendoftheexperiments,fragmentsofthefecalpel 10 20 30 40

letsmayhavecontaminatedthewaterasthepelletswererela Length(mm) tivelyfragilecomparedwiththosefrommid-latitudesalps.

Therefore,webelievethattheclearanceratescalculatedwith Fig.2. ClearanceratesofSalpathompsoniblastozooidsasa

flagellatesaremorerealisticvalues. functionofbodylength.ValuesfromTable1,whichwerecalcu

Theclearanceratesobtainedinthisstudyas"Fo"values latedonflagellates,areshownasdots.Thecontinuousandthe

(Harbison& Gilmer1976)weresimilartothosereportedin dottedlineindicatesthe"Fo"(overall)and"Fh"(maximum)val

Huntleyetal.(1989),althoughwedidnotfindaclearcorrela uesreportedinHuntleyetal.(1989),respectively.Calculations

tionwithanimalsize(Fig.2).Thesevaluesaremuchlower werebasedonTable2andTable3inHuntleyetal.(1989).

thanthosereportedforthetemperateandsubtropicalsalps(see

Table6inHuntleyetal.1989).Severalexplanationsarepossi

bleforthelowerclearanceratesofthisantarcticsalp.Feeding Pakhomov1998b).However,insituconcentrationsofchloro

ofantarcticsalpsmayberestrictedbyreducedmetabolicactiv phyllparticlesusedinourexperimentswerebelowthe"thresh-

ityduetotheextremelylowambienttemperatures.Ifweas hold"leveltheysuggested.Furtherstudyisnecessarytoex

sumeaQ,ovalueof2.03,aswasreportedforthepulserateof plainthelowclearanceratesofthisantarcticsalp.

Salpafusiformisaggregates(Harbison& Campenot1979),a Therehavebeenfewstudiesontheminimumsizeofin-

clearancerateof43-368h"1indiv."1 ml forS.thompsoniof gestableparticlesbyantarcticsalps.Previousstudiesinvesti

20-40mm in lengthlivingat 0°C isequivalentto gatingtheparticleretentionefficiencyofmid-latitudespecies

140-1195mlh"1indiv.""1forsalpsat16°C.Thesevaluesareof haveclarifiedthatwarm-watersalpscanretainparticlesof

asimilarorderbutareabout2.2-2.5timeslowerthantheval >3jumwithefficiency high (Harbison& McAlister1979;

uesof302-3012mlh~1indiv."1reportedforS.fusiformisof Caronetal.1989;Kremer& Madin1992).Ourresultsfor

thesamesizerangeatthesametemperature(16°C)(AndersenSalpathompsoniindicatethatitcanfeedon>0.2/miparti

1985).Anotherpossibleexplanationcouldbethatthehigher cles.Thissuggeststhatthissalpmaybeabletoreteinfiner

waterviscosityatlowertemperaturesmayinterferewithactive particlesthanmid-latitudesalps.Inordertoclarifytheparticle

"pumping"bytheanimalorwitheffectivefiltrationbythemu retentionefficiencyofantarcticsalp,moreinformationis

cousnet.Feedingnetcloggingduetohighparticleconcentraneeded,suchasfeedingnetmeshsizeandclearanceratesofa

tionsmayalsoexplainlowclearancerate(Perissinotto& gradationofparticlesizesinintervalsof0.1or1.0jum. Feeding of Salpa thompsoni 135

Generally, pico- and nano-sized phytoplankton dominate the 50. Southern Ocean (Jochem et al. 1995; Hewes et al. 1985; Frost, B. W. 1972. Effects of size and concentration of food particles on Kosaki et al. 1985), and these primary producers are continu the feeding behavior of the marine planktonic copepod Calanus pacifi- cus. Limnol. Oceanogr. 17: 805-815. ouslykept in check through microzooplanktonic grazing Frost, B. W. 1991. The role of grazing in nutrient-rich areas of the open (Burkill et al. 1987,1995; Tsuda & Kawaguchi 1997). The sea. Limnol. Oceanogr. 36: 1616-1630. dominant non-salp antarctic zooplankters, such as euphausiids Harbison G. R. & R. W. Gilmer 1976. The feeding rate of the pelagic tuni and large copepods are basically suspension feeders that feed cate Pegea confederata and two other species. Limnol. Oceanogr. 24: mainly on particles >5fim (Ishii 1986; Atkinson 1995). 875-892 Therefore, the dominant phytoplankton fraction would not be Harbison, G. R. & R. B. Catnpenot 1979. Effects of temperature on the effectively grazed by these suspension feeders. In other words, swimming of salps (Tunicata, Thaliacea): Implications for vertical mi gration. Limnol. Oceanogr. 24: 1081-1091. resource partitioning between microzooplankton and these Harbison, G. R. & V. L. McAlister 1979. The filter-feeding rate and parti larger suspension feeders occurs, or suspension feeders act as cle retention efficiencies of three species of Cyclosalpa (Tunicata, Thali predators of microzooplankton. This was the scenario pro acea). Limnol. Oceanogr. 24: 875-892. posed during the investigation on the "high nutrient/low Hewes, C. D., O. Holm-Hansen & E. Sakshaug 1985. Alternative carbon chlorophyll" conditions in the subarctic Pacific (Frost 1991; pathways at lower trophic levels in the Antarctic foodweb, p. 277-283. Miller et al. 1991). The salps, however, can graze particles in In Antarctic Nutrient Cycles and Food Webs (eds. Siegfried, W. R., P. R. any of the size ranges we measured, including the pico- and Condy & R. M. Laws). Springer, Berlin. Huntley, M. E., P. F. Sykes & V Marin 1989. Biometry and trophodynam- micro- plankton. This suggests that Salpa thompsoni is unique ics of Salpa thompsoni Foxton (Tunicata: Thaliacea) near the Antarctic among the suspension-feeding macrozooplankton as it acts not Peninsula in austral summer, 1983-1984. Polar Biol. 10:59-70. only asa consumer of microzooplankton but also as a potential Ishii, H. 1986. Feeding behaviour of the Antarctic krill, Enphausia su- competitor withthem. The unique feeding characteristics of perba Dana II. Effects of food condition on particle selectivity. Mem. Salpa thompsoni, which enables it to utilize particles of a pico- Natllnst. Polar Res., Spec. Issued: 96-106. and nano-sized particles, together with the unique patterns of Jochem, F. J., S. Mathot & B. Queguiner 1995. 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