Microbial food web structure in the Arabian Sea: a US JGOFS study

36 Pages·2000·0.4 MB·English

Deep-SeaResearchII47(2000)1387}1422
Microbial food web structure in the Arabian Sea:
a US JGOFS study
David L. Garrison!,*, Marcia M. Gowing!, Margaret P. Hughes!,
Lisa Campbell", David A. Caron#, Mark R. Dennett$,
Alexi Shalapyonok$, Robert J. Olson$, Michael R. Landry%,
Susan L. Brown%, Hong-Bin Liu&, Farooq Azam’,
Grieg F. Steward), Hugh W. Ducklow*, David C. Smith+
!InstituteofMarineSciences,UniversityofCalifornia,SantaCruz,CA95064,USA
"DepartmentofOceanography,TexasA&MUniversity,CollegeStation,TX77843-3146,USA
#DepartmentofBiologicalSciences,UniversityofSouthCarolina,3616TrousdaleParkway,AHF309,
LosAngeles,CA90089-0371,USA
$BiologyDepartment,WoodsHoleOceanographicInstitution,WoodsHole,MA02543,USA
%DepartmentofOceanography,UniversityofHawaii,1000PopeRd.,Honolulu,HI96822,USA
&MarineSciencesInstitute,TheUniversityofTexasatAustin,750ChannelViewDrive,PortAransas,
TX78373,USA
’ScrippsInstitutionofOceanography,UniversityofCalifornia,SanDiego,CA92093,USA
)MontereyBayAquariumResearchInstitute,P.O.Box628,MossLanding,CA95039,USA
*TheCollegeofWilliamandMary,SchoolofMarineScience;Box1346,GloucesterPoint,VA23062,USA
+GraduateSchoolofOceanography,UniversityofRhodeIsland,Narragansett,RI02882-1197,USA
Received4May1999;receivedinrevisedform16September1999;accepted17September1999
Abstract
OneofthemainobjectivesoftheJointGlobalOceanFluxStudies(JGOFS)programisto
developan understandingof the factors controlling organic carbon production in the ocean
andthetime-varyingvertical#uxofcarbonfromsurfacewaters(USJGOFS(1990)USJGOFS
Planning Report Number 11; Sarmiento and Armstrong (1997) US JGOFS Synthesis and
Modeling Project Implementation Plan). A considerable amount of evidence suggests that
carboncyclingandthepotentialforexportingcarbonfromoceansystemsisafunctionoffood
web structure. As part of the US JGOFS Arabian Sea Studies, the biomass of planktonic
organisms,rangingfromheterotrophicbacteriathroughmicroplankton-sizedorganisms,was
estimatedusingavarietyofmethodsincluding#owcytometryandmicroscopy.Thisisa"rst
attempttocombinebiomassdatafromanumberofsources,evaluatethestructureofthefood
*Correspondingauthor.NationalScienceFoundation,DivisionofOceanSciences,BiologicalOceanog-
raphyProgram,Room725,4201WilsonBlvd.,Arlington,VA22230,USA.Interpretationsandconclusions
arethoseoftheauthoranddonotimplytheendorsementoftheNationalScienceFoundation.
0967-0645/00/$-seefrontmatter ( 2000ElsevierScienceLtd.Allrightsreserved.
PII: S0967-0645(99)00148-4
1388 D.L.Garrisonetal./Deep-SeaResearchII47(2000)1387}1422
web,examinechangesin foodweb structurein relation toseasonal or spatialfeaturesof the
studyarea,andlookforindicationsofhowchangingstructurea!ectscarbon-cyclingprocesses.
Biomass in the upper 100m of the water column ranged from approximately 1.5 to
’5.2gCm~2. Heterotrophic bacteria (Hbac) made up from 16 and 44% of the biomass;
autotrophscomprised43}64%;and theremainder wasmade upof nano-and microheterot-
rophs.Autotrophsandnano-andmicroheterotrophsshowedageneralpatternofhighervalues
atcoastalstations,withthelowestvalueso!shore.Heterotrophicbacteria(Hbac)showedno
signi"cantspatialvariations.TheSpringIntermonsoonandearlyNEMonsoonweredomin-
atedbyautotrophicpicoplankton,ProchlorococcusandSynechococcus.ThelateNEMonsoon
andlateSWMonsoonperiodsshowedanincreaseinthelargersizefractionsof theprimary
producers.AtseveralstationsduringtheSWMonsoon,autotrophicmicroplankton,primarily
diatomsandPhaeocystiscolonies,predominated.Increasesinthesizeofautotrophswerealso
re#ectedin increasingsizes ofnano-andmicroheterorophs.Thebiomass estimatesbasedon
cytometry and microscopy are consistent with measurement of pigments, POC and PON.
Changes in community structure were assessed using the percent similarity index (PSI) in
conjunctionwithmultidimensionalscaling(MDS)orsingle-linkageclusteringanalysistoshow
how assemblages di!ered among cruises and stations. Station clustering re#ected environ-
mentalheterogeneity,andmanyoftheconspicuouschangescouldbeassociatedwithchanges
intemperature,salinityandnutrientconcentrations.Despiteinherentproblemsincombining
datafromavarietyofsources,thepresentcommunitybiomassestimateswerewellconstrained
by bulk measurements such as Chl a, POC and PON, and by comparisons with other
quantitativeandqualitativestudies.
The most striking correlation between food web structure and carbon cycling was the
dominanceoflargephytoplankton,primarilydiatoms,andtheseasonalmaximaofmass#ux
duringtheSWMonsoon.HighnutrientconditionsassociatedwithupwellingduringtheSW
Monsoonwouldexplainthepredominanceofdiatomsduringthisseason.Thesinkingoflarge,
ungrazed diatom cells is one possible explanation for the #ux observations, but may not be
consistentwiththeobservationofconcurrentincreasesinlargermicrozooplanktonconsumers
(heterotrophicdino#agellatesandciliates)andmesozooplanktonduringthisseason.Food-web
structure during the early NE Monsoon and Intermonsoons suggests carbon cycling by the
microbialcommunitypredominated. ( 2000ElsevierScienceLtd.Allrightsreserved.
1. Introduction
Thepelagicfoodwebiscomprisedofadiversityoforganismsvaryingoverseveral
ordersofmagnitudeinsizeanddi!eringintaxonomica$nitiesandtrophicfunctions
(e.g.,Sieburthetal.,1978).Manyofthesmallerplanktonicorganisms,suchasbacteria,
picoplanktonicautotrophsand phagotrophic protists, were unknown orlargely over-
looked until relatively recently (e.g., Azam et al., 1983; Sherr and Sherr, 1984; Porter
etal.,1985).Nonetheless,thisassemblage,collectivelyknownasthe microbialfoodweb ,
‘ a
isnowrecognizedasubiquitousandabundantinoceanenvironments(e.g.,Garrison
and Gowing, 1993; Buck et al., 1996; Table 5 in Garrison et al., 1998) with integral
roles in system tropho-dynamics and biogeochemical transformations (Capriulo,
1990; Stoecker and Capuzzo, 1990; Caron et al., 1990; Caron, 1991; Gi!ord, 1991).
Assessingthestructureandbiomasscompositionofthepelagicfoodwebhasbeen
one of the enduring research activities of plankton ecologists. Progress has largely
D.L.Garrisonetal./Deep-SeaResearchII47(2000)1387}1422 1389
followedtechnicalimprovementsindetectingandenumeratingprogressivelysmaller
organisms (e.g., Fuhrman and McManus, 1984; Glover et al., 1986; Chisholm et al.,
1988), as well as quantifying the abundance of organisms too rare to be adequately
sampledinbottlesortoodelicatetobecollectedwithnets(e.g.,GowingandGarrison,
1992).Forthemicrobialcommunity,epi#uorescencemicroscopy(Booth,1993;Sherr
et al., 1993, Verity and Sieracki, 1993) and #ow cytometry (Olson et al., 1990,1993;
ButtonandRobison,1993)techniqueshavebeencriticalinallowingroutinequantit-
ativedescriptionsof,at least,thefunctionalgroupscomprisingthepelagicfoodweb
(e.g., see citations in Table 5 in Garrison et al., 1998).
Thefocusonaccuratedescriptionsofthefoodwebcompositionisdrivenbymore
thandiscoveryortechnology.Ithaslongbeenrecognized,forinstance,thatfoodweb
structure can profoundly a!ect ecosystem characteristics such as "sh yield (Ryther,
1969),carbon#ux,(Azamet al.,1983;MichaelsandSilver,1988; Peinertetal.,1989;
Legendre and LeFevre, 1995; Legendre and Rassoulzadegan, 1996), and nutrient
regeneration (Caron, 1991). Moreover, understanding of the underlying structure of
foodwebsandthefactorsthatcausethemtodevelopindi!erentwaysisessentialfor
developing and testing the predictive ecosystem and global-scale biogeochemical
models that are ultimately desired by the JGOFS Program (e.g., Armstrong, 1994;
Sarmiento and Armstrong, 1997).
TheUSJGOFSArabianSeaProcessStudywasconductedtoexaminespatialand
temporalvariabilityinfoodwebstructureinadynamicpelagicsystem(USJGOFS,
1990;Smithetal.,1991,1998a).Distributionsandabundancesofindividualcompon-
entpopulationshave beenreported previously(picoplankton:Campbellet al., 1998;
Brown et al., 1999; Riemannet al., 1999; Ducklow et al., 2000a,b; nano- and micro-
plankton:Garrisonetal.,1998;Dennettetal.,1999;CaronandDennett,1999).Here
wepresentthe"rstcombinede!orttoprovideacomprehensiveestimateofbiomass
structure and to evaluate spatial and temporal patterns in community structure.
2. Materials and methods
As part of the US JGOFS Arabian Sea Process Study, plankton community
structure was investigated during four di!erent phases of the monsoon cycle of
1995 (Table 1). Data were analyzed from seven stations (Fig. 1) for which we had
reasonablycomplete data sets from all, or most, cruises. These included six stations
(S1, S2, S4, S7, S11 and S15) along the southern transect extending from the
upwelling-in#uencedcoastalenvironmenttotheoligotrophicopenocean(Olson,1991;
Smith et al., 1998a; Garrison et al., 1998), and one o!shore station (N7) on the
northern transect.
Samplesforthisanalysiswerecollectedatfourtosixdepthsintheupper100mof
the water column with 10-l Niskin bottles on a CTD rosette. The microbial assem-
blagewasanalyzedbydividingitintodi!erentsizefractionsandtrophicgroupsthat
were enumerated separately using appropriate methodology (Table 2).
Thespeci"cmethodologyusedtodeterminebiomassandabundanceoforganisms
hasbeenreportedinanumberofrecentpapers(Campbelletal.,1998;Ducklowetal.,
1390 D.L.Garrisonetal./Deep-SeaResearchII47(2000)1387}1422
S1}S15.Meanand(range)upper20m(datacourtesysurfacereferencevalueasMarra.Chlorophyllvaluesncubations.Alldataand TN05428Nov.}27Dec.EarlyNEMonsoon 27.0(25.8}28.2)36.47(35.85}36.81)0.79(0.01}3.6)0.26(0.00}2.1)63(50}82)0.38(0.12}0.88)1.0(0.7}1.4)
Table1Cruisedates,hydrographicseason,andsummaryofhydrographicconditionsintheupperwatercolumnforstationsonSouthtransect,##ofvaluesareshownforalldata.Temperature,salinity,andtotalnitrogen(NONONH)wereaveragesfromdepthswithinthe324~3ofJ.Morrisonetal.).Mixedlayerdepths(mld)wereestimatedasthedepthwheredensitychangedby0.125kgmfromanear0.125acalculatedandreportedbyW.GardnerandJ.Gundersen.ChlorophyllandprimaryproductiondatacourtesyofR.BarberandJ.areaverageswithintheupper25m.Primaryproductiondataareintegrateddataforthewatercolumnbasedon24hinsituidocumentationareavailablefromtheJGOFSArabianSeadatabase(http://www1.whoi.edu/jgofs.html). CruiseDatesSeasonTN0438Jan.}4Feb.TN04514Mar.}10AprilTN05017Aug.}15Sept.NEMonsoonSpringIntermonsoonLateSWMonsoon Temperature(3C)25.4(24.4}27.2)26.9(25.1}29.1)26.0(19.7}28.36)Salinity(psu)36.33(36.10}36.55)36.31(35.23}36.69)36.22(35.63}36.614lTotalnitrogen(moles)2.27(0.04}4.96)0.25(0.02}2.03)5.83(0.03}22.1)N:Si0.87(0.01}2.2)0.16(0.01}1.11)2.8(0.02}18.0)Mixedlayerdepth(m)72(68}76)30(10}70)54(24}100)l~1aChl(gl)0.36(0.05}0.95)0.34(0.02}0.93)0.67(0.01}1.72)~2~1Primaryproduction(gCmday)1.1(0.6}1.4)1.0(0.7}1.3)1.0(0.6}1.8)
D.L.Garrisonetal./Deep-SeaResearchII47(2000)1387}1422 1391
Fig.1. JGOFSStationsinthenorthernArabianSea.Stationsindicatedwereanalyzedforthisstudy,except
thatstationS1wasnotanalyzedforthe"naloffourcruises(TN054).
2000a,b; Garrison et al., 1998; Dennett et al., 1999). Here, these methods are brie#y
presented and discussed only as needed to explain the present synthesis of data.
2.1. Picoplankton
Picoplankton,includingheterotrophicbacteria(Hbac),Prochlorococcusspp.(Pro),
Synechococcus spp. (Syn), and phototrophic eukaryotes (Peuk), were counted using
#ow cytometry as described by Campbell et al. (1994,1998).
Cellcarbonvaluesforautotrophicpicoplanktonweredeterminedassummarizedin
Table 2. Conversion values for Pro and Syn were based on recent calibrations by
Shalapyonok et al. (2000) from cultures raised under natural light conditions. For
picoeukaryotes,samplesfromTN054weresizedusingforwardanglelightscattering
(FALS)todetermineasize-frequencydistribution,whichweassumedwassimilarfor
all cruises. Approximately 69% (range 27}88%) of the eukaryotic cells were ’2.0
lm. These counts were removed from cytometer data to avoid overlap with micro-
scopical counts of autotrophic nanoplankton. The remaining cells (31%) were
assumed to comprise the picoeukaryotes. Cell volumes were calculated assuming
a 1.5lm-diameter spherical shape, and cell volume-to-carbonconversions based on
amodi"edStrathmannequationfornon-diatomphytoplankton(Eppleyetal.,1970)
were used to estimate carbon.
Flowcytometercountswereusedforheterotrophicbacteria(Hbac)estimatesforall
cruises for consistency (no "lter counts were available for TN050). A regression
(ModelII) of all pairedestimatesof Hbac by cytometerand epi#uorescencemicros-
copyproducedtheregression:cytometer(bacteriacellsl~1)"1.044]epi#uorescence
(cellsl~1)!0.870]108(cellsl~1);(R2"0.689,n"421),witharegressioncoe$cient
1392 D.L.Garrisonetal./Deep-SeaResearchII47(2000)1387}1422
mthennettlight 1998) etal.,
dtoestimatecarbonbiomassfordi!erentcomponentsofthemicrobialfoodweb.Valuestakenfroofmethodsusedfornano-andmicroplanktonandinterpretationsofdistributionsarepresentedinDecriptionsofsomemethodsareinthetext.CYT:#owcytometry;EFM:epi#uorescencemicroscopy;LM:l~3m) l~3ConversionsusedforfgCmRemarksandcitations~1biomasspgCCell 0.011380AveragefromTN045andTN049data.Seetext 0.032/0.072235Mixedlayerpopulations/Belowmixedlayer0.101/0.152235Mixedlayerpopulations/Belowmixedlayer1.011Seetext 183TN043,TN045;Caronetal.,1995.!"!logC0.94(logV)0.60210TN050,TN054(Eppleyetal.,1970;Garrisonetal.,1010183TN043,TN045(Caronetal.,1995)!"!logC0.94(logV)0.60(209/211)TN050,TN054(Garrisonetal.,1998)1010 183TN043,TN045(Caronetal.,1995)"!logC0.94(logV)0.60TN050,TN0541010"!logC0.76(logV)0.352AllCruises(Eppleyetal.,1970)1010140TN043,TN045(Stoeckeretal.,1994)!"!logC0.94(logV)0.60(183/165)TN050,TN054(Eppleyetal.,1970)1010 140TN043,TN045!"!logC0.94(logV)0.60(164/160)TN050,TN0541010140TN043,TN045160}190TN050,TN054(PuttandStoecker,1989)53TN043,TN045(VerityandLangdon,1984)160}190TN050,TN054(PuttandStoecker,1989) forcruisesTN050andTN054dataforcomparisonswiththoseusedforTN043andTN045(seeDennett
Table2Overviewofmethodsandconversionfactorsuseliteratureareshownwithsourcecitations.Detailsetal.(1999)andGarrisonetal.(1998).Speci"cdes"<microscopy.Informulaebelowcellvolume( SizefractiongroupMethodsforenumeration l&(0.2}2.0m)Picoplankton HeterotrophicpicoplanktonCYTEFMAutotrophicpicoplankton CYTProchlorococcusCYTSynechococcusPicoeukaryotesCYT l(2}20m)Nanoplankton AutotrophicnanoplanktonEFM HeterotrophicnanoplanktonEFM l’(20m)Microautotrophs OtheralgaeEFM DiatomsLM/EFMDino#agellatesLM/EFM l’(20m)Microheterotrophs Dino#agellatesLM/EFM Non-loricateciliatesLM TintinnidsLM !l~3Averagevalueofcarbonpervolume(fgCm)1999)
D.L.Garrisonetal./Deep-SeaResearchII47(2000)1387}1422 1393
not di!erent from 1.0. The cell sizes of (Hbac) were determined by epi#uorescence
microscopy for cruises TN045 and TN049 (Ducklow et al., 2000a). Mean bacterial
volumes were measured on every cell counted in every sample and cell volume
calculated using the algorithm of Baldwin and Bankston (1988) (mean"0.029lm3;
range"0.019}0.056lm3; N"421, upper 0}200 m), and carbon content was deter-
minedbyassuming380fgClm~3(LeeandFuhrman,1987).Anaveragevalueof11fg
Ccell~1forthesetwocruiseswasusedtoestimatebacterialbiomassfromabundance
for all cruises.
2.2. Nanoplankton
Bothautotrophicandheterotrophicnanoplanktonwereconcentratedon"ltersand
counted by epi#uorescence microscopy as described by Garrison et al. (1998) and
Dennettetal.(1999).Preservationandstainingmethodsvariedamongthecruises(see
Garrisonetal.,1998;Dennettetal.,1999).DuringTN043andTN045(Dennettetal.,
1999),watersampleswerepreservedata"nalconcentrationof1%formalin(madein
natural,"lteredseawater)andstoredat43C.Sampleswerepreparedforenumeration
byepi#uorescencemicroscopywithin24hofpreservationbystainingwithDAPI at
a"nalconcentrationof50lgml~1(Caron,1983;Sherretal.,1993).ForTN050and
TN054 (Garrison et al., 1998), replicate samples were stained separately with the
#uorochromes DAPI (Coleman, 1980) and pro#avine (Haas, 1982)#DAPI (e.g.,
Verity and Sieracki, 1993). Glutaraldehyde and the #uorochromes were added near
theendofthe"ltrationwhenapproximately10mlremainedinthe"lterchimney.The
"nal concentration of glutaraldehyde was &0.5%.
2.3. Microplankton
WatersampleswerepreservedwithLugol’sIodinesolutionorbu!eredparaformal-
dehyde for analysis of the robust microplanktonincluding diatoms, silico#agellates,
thecateandsomeathecatedino#agellatesandciliates.Thesesampleswerecountedby
inverted microscopy (see Garrison et al., 1998; Dennett et al., 1999). For both
"lter-collectedandwholewatersamples,carbonestimateswerederivedbymeasuring
celldimensions,calculatingcell volumes andapplyingcarbonto volume conversion
factors (Table 2).
2.4. Size fractions
Biomass in conventional size fractions (i.e., pico-, nano- and microplankton) was
calculated as follows: picoplankton sizes were con"rmed by FALS analysis of
cytometerdata,andthefractioncomprisingpico-eukaryoteswasdistinguishedfrom
the wider range of eukaryotic autotrophs detected by the cytometer as described in
Campbelletal.(1994,1998).ForTN043andTN045,biomassdataareseparatedinto
nano-and microplanktonsizefractions Dennett et al. (1999),but taxonomicgroups
within the autotrophic nanoplankton (Anan) and heterotrophic nanoplankton
(Hnan)were not di!erentiated.For TN050 and TN054 microbial groups within the
1394 D.L.Garrisonetal./Deep-SeaResearchII47(2000)1387}1422
nanoplankton were distinguished by taxon and cell volume. To have a consistent
groupingofcategoriesthatwouldallowananalysisamongallcruises,sizefractionsof
nano- and microplankton were grouped using cell volume ranges of ’4.2 to
4190lm3and’4190lm3,respectively,toseparatecellsintonano-andmicroplan-
kton and data recombined in a manner consistent with that used for TN043 and
TN045.
2.5. Analysis of the microbial assemblage
We used community analysis procedures similar to those outlined by Field et al.
(1982) to examine the similarity of assemblage composition between stations and
cruisesandto assesswhichbiomasscomponentswereresponsibleforthevariations.
Biomass was classi"ed within the 12 size and taxonomic components (Table 3).
SimilaritieswerecalculatedbetweenpairedstationsasPercentSimilarityIndex(PSI):
PSI(Sample )"+Minimum[Group(%Sample ,%Sample )]
!," * ! "
where,i"(groups1,22,12)inacomparisonofthesimilaritybetweensamplesaand
b.Theresultingstation-by-stationsimilaritymatrixwasanalyzedusingmulti-dimen-
sional scaling (MDS) and single-linkage cluster analysis (see Field et al., 1982 for
amorecompletediscussionoftheseprocedures).Wedidnotusetransformedbiomass
data, as suggested by Field et al. (1992), to avoid the bias of giving unwarranted
weighting to ciliate biomass. Tintinnid data from TN050 and TN054, in particular,
sometimeswerebasedonsampleswithlowcellcountsandthushavewidecon"dence
limits. Analyses and clustering were performed on both transformed and untran-
sformeddata.Bothproducedsimilarstationclusteringpatternsbutthelatterproved
easier to interpret.
3. Results
3.1. Community Composition
Theoverallrangesofabundanceandbiomassofmicrobialgroupsaresummarized
inTable 3.Depth-integratedbiomassoverthe upper100m of the water column(or
85matS1wherebottomdepthdidnotextendto100m)rangedfromapproximately
1.5to’5.2gCm~2(Table4).Overall,autotrophsmadeup43}64%ofthebiomass;
Hbac accountedfor 16}44%, and nano-and microheterotrophicprotists comprised
the remaining portion (Table 4). Biomass estimates for total microbial biota, autot-
rophic, nano- and microheterotrophic, and bacterial biomass were not signi"cantly
di!erentamongthefourcruises(Duncanmultiple-rangetest,a(0.05;SASInstitute
Inc., 1989). Among stations and within cruises, total autotrophic and nano- and
microheterotrophbiomassestimatesweregenerallyhigherforcoastalstations(S1and
S2)and lowerat theo!shorestations (N7}S15),butusually onlythe extremevalues
could be distinguished statistically (see Table 5). Heterotrophic bacteria showed no
statisticallysigni"cantdi!erencesamongstations.Basedonanalysisofdiscrete-depth
D.L.Garrisonetal./Deep-SeaResearchII47(2000)1387}1422 1395
Table3
Rangeofabundanceandbiomassfordi!erentmicrobialgroupsoverthefourcruisesanalyzed(0.0)0.05)
Cruise Biomass Abundance
Sizefraction lgCl~1 celll~1
Microbialgroup Mean Min Max Mean Min Max
TN043
Picoplankton
Heterotrophicbacteria 8.0 0.2 11.5 7.3E#08 1.8E#07 1.0E#09
Prochlorococcus 1.0 0.0 7.2 3.0E#07 3.3E#04 2.3E#08
Synechococcus 3.7 0.1 112.9 3.7E#07 7.9E#04 1.3E#08
Picoeukaryotes 0.6 0.0 1.8 1.3E#06 9.9E#03 3.9E#06
Nanoplankton
Autotrophicnanoplankton 5.6 0.2 18.1 7.6E#05 2.7E#04 2.9E#06
Heterotrophicnanoplankton 4.3 0.9 12.3 3.7E#05 1.3E#05 9.8E#05
Microplankton
Dino#agellates 2.1 0.0 27.6 5.6E#02 0.0E#00 2.2E#03
Diatoms 3.4 0.0 27.6 2.7E#04 2.2E#02 2.0E#05
Autotrophic#agellates 0.3 0.0 7.5 9.9E#01 0.0E#00 9.6E#02
Heterotrophicdino#agellates 2.3 0.0 32.4 5.5E#02 0.0E#00 2.6E#03
Non-loricateciliates 0.5 0.0 2.4 5.0E#02 0.0E#00 2.6E#03
Tintinnids 0.0 0.0 0.1 4.7E#01 2.4E#00 1.3E#02
TN045
Picoplankton
Heterotrophicbacteria 10.2 2.8 31.8 9.2E#08 2.6E#08 2.9E#09
Prochlorococcus 8.6 0.0 47.2 1.7E#08 3.3E#04 7.0E#08
Synechococcus 3.6 0.0 33.0 2.8E#07 1.6E#04 2.2E#08
Picoeukaryotes 0.4 0.0 2.3 9.7E#05 1.0E#04 5.2E#06
Nanoplankton
Autotrophicnanoplankton 4.8 0.1 15.2 5.3E#05 1.1E#04 1.4E#06
Heterotrophicnanoplankton 4.6 0.7 12.1 3.0E#05 1.3E#05 8.0E#05
Microplankton
Dino#agellates 1.4 0.0 5.2 1.4E#03 2.4E#01 5.1E#03
Diatoms 0.8 0.0 8.8 4.7E#03 1.1E#02 6.0E#04
Autotrophic#agellates 0.1 0.0 0.9 6.9E#01 0.0E#00 4.1E#02
Heterotrophicdino#agellates 0.6 0.0 2.2 5.9E#02 1.0E#01 2.2E#03
Non-loricateciliates 0.4 0.0 2.6 3.2E#02 2.1E#01 1.3E#03
Tintinnids 0.0 0.0 0.2 5.4E#01 1.2E#00 2.5E#02
TN050
Picoplankton
Heterotrophicbacteria 11.4 3.8 23.5 1.0E#09 3.4E#08 2.1E#09
Prochlorococcus 1.6 0.0 9.10 4.4E#07 3.6E#04 2.8E#08
Synechococcus 3.0 0.1 9.5 2.8E#07 3.7E#04 9.4E#07
Picoeukaryotes 0.9 0.0 5.8 2.0E#06 1.1E#04 1.3E#07
Nanoplankton
Autotrophicnanoplankton 4.6 0.1 36.3 4.2E#05 3.2E#03 2.0E#06
Heterotrophicnanoplankton 2.9 0.5 10.1 5.4E#05 3.5E#04 2.2E#06
1396 D.L.Garrisonetal./Deep-SeaResearchII47(2000)1387}1422
Table3(continued)
Cruise Biomass Abundance
Sizefraction lgCl~1 celll~1
Microbialgroup Mean Min Max Mean Min Max
Microplankton
Dino#agellates 0.7 0.0 2.9 4.2E#05 4.2E#05 4.2E#05
Diatoms 5.5 0.0 36.8 3.7E#03 1.0E#01 2.6E#04
Autotrophic#agellates! 3.8 0.1 18.7 6.6E#05 8.2E#03 2.8E#06
Heterotrophicdino#agellates 1.0 0.1 4.6 2.6E#02 3.0E#01 1.0E#03
Non-loricateciliates 0.9 0.1 4.4 3.0E#02 3.0E#01 1.2E#03
Tintinnids 0.2 0.0 1.5 8.0E#01 1.0E#01 3.0E#02
TN054
Picoplankton
Heterotrophicbacteria 11.3 1.5 34.7 1.0E#09 1.4E#08 3.2E#09
Prochlorococcus 2.8 0.2 10.2 8.4E#07 3.2E#05 3.2E#08
Synechococcus 9.8 0.1 54.2 9.7E#07 3.5E#04 5.4E#08
Picoeukaryotes 0.9 0.0 3.3 2.1E#06 1.1E#04 7.4E#06
Nanoplankton
Autotrophicnanoplankton 2.3 0.1 9.8 3.0E#05 9.0E#03 8.0E#05
Heterotrophicnanoplankton 1.7 0.1 9.5 1.8E#05 9.2E#03 7.9E#05
Microplankton
Dino#agellates 0.5 0.0 1.9 1.7E#02 1.0E#01 1.1E#03
Diatoms 0.5 0.0 2.3 6.0E#02 1.0E#01 2.6E#03
Autotrophic#agellates 0.0 0.0 0.0 0.0E#00 0.0E#00 0.0E#00
Heterotrophicdino#agellates 1.3 0.1 6.1 5.0E#02 6.0E#01 1.9E#03
Non-loricateciliates 1.1 0.0 5.2 2.6E#02 2.4E#01 1.1E#03
Tintinnids 0.3 0.0 2.3 8.0E#01 1.0E#01 3.4E#02
!MostlyPhaeocystisnon-motilecellsindisruptedcolonies;seemethodsandGarrisonetal.(1998).
samples, biomass estimates for Hbac, autotrophs, and other heterotrophs were
negatively correlated with depth (Spearman; R"!0.55, !0.70, !0.59; N"240,
172, 171; P(0.01 for the three groups, respectively).
3.2. Seasonal and spatial distributions
The composition of the microbial community varied among stations and cruises
(Table5). To identify seasonal (between cruises) and spatial (between station) di!er-
ences for each of the 12 groups of the microbial community, we examined both the
depth-integrated (Table 5) and discrete-depth data (not shown) using the Duncan
multiple-range test (SAS Institute Inc., 1989). Trends were considered signi"cant at
a(0.05. Pro biomass washigher duringTN045 than duringother cruises, andSyn
biomass was higher during TN054. Autotrophic micro#agellate (A#g) biomass was
highest during TN050, and non-loricate ciliate (Cil) biomass was higher for TN050