Superscript letters denote hauls that were used for community C and stable isotope S analysis.. Benthic substrate type follow notation of: sand S, gravelly mud gM, slightly gravelly mud
Trang 1jo u r n al h om ep a ge :w w w e l s e v i e r c o m / l o c a t e / f i s h r e s
a Faculty of Biology, Hanoi University of Science, Vietnam National University, 334 Nguyen Trai Street, Thanh Xuan District, Hanoi, Viet Nam
b Global Center of Excellence, Center for Marine Environmental Studies, Ehime University, 2-5 Bunkyo-cho, Matsuyama 790-8577, Japan
a r t i c l e i n f o
Article history:
Received 15 February 2011
Received in revised form 18 April 2011
Accepted 19 April 2011
Keywords:
Community structure
Vietnam
Fisheries
Trophic structure
Stable isotopes
Benthic–pelagic coupling
Food web
Phan Thi ´ˆet
Shelf
Marine
a b s t r a c t
Weexaminedthecommunityandtrophicstructureoftheheavilyexploitedbenthic-demersal commu-nityoffPhanThi ´ˆetBay,CentralVietnam.Usingclusteranalysisandnon-metricmultidimensionalscaling (NMS)ofcatchdatafromatrawlsurvey,weexaminedthenektoncommunitystructurepertainingto bottomsubstratetypeanddepth.Fordominantfishandinvertebratetaxaweappliedstableisotope analysis,using␦15Ntoexaminetrophiclevel(TL)andsize-specificontogeneticshifts,and␦13Casa mea-sureofcontributionbybenthicsecondaryproduction.Basedontrawldatasmallfishesandcephalopods werethenumericallyandbiomass-dominanttaxa.Communitystructureanalysisshowedmanyofthe samplesitessharedthesamespeciescomposition,butthattherewassignificantheterogeneityrelated
tosubstratetypesofsandandgravellymuddysand.Resultsfrom␦15Nshowed70%ofthespecieswere betweenTL3.3and3.8,withnospeciesindicatingtruepiscivory(TL4);highestTLwasfromthesquid Loligojaponica(TL3.8).Size-specific␦15N-basedtrophicshiftwasexpressedintaxawhenthe propor-tionalsizerange(Lmax)obtainedforanalysiswasatleast40%ofthelargestreportedsizeforthespecies (Lmax).From␦13C,nektonexpressedbetween35and77%dependenceonbenthicsecondaryproduction Evidenceofover-exploitationfromourstudyincludedtherelativelylowTL’sofdominanttaxa,small sizedistributionofspecimenscollected,andthedominanceoftaxawithveryhighgrowthratessuchas cephalopods(juvenileOctopussp.andcuttlefish)andsmallfishes.Theeffectivenessofstableisotopesas
anindicatorofover-exploitationisdiscussed
© 2011 Elsevier B.V All rights reserved
1 Introduction
About65%ofVietnam’s fisheriesproduction is derivedfrom
itscoastal waters <50mdepth, with intensivefishingover the
last 30 yrs resulting in precipitous declines in fisheries
catch-per-unit-effort (CPUE,vanZwietenet al.,2002; Pomeroy etal.,
2009).Thecoastalregionof Vietnamis alsoexperiencing
mas-sive growth in both industry and tourism, increasing demand
for fisheries productswhile increasingthepotential forcoastal
eutrophication.VulnerabilitiesofVietnam’scoastalecosystemsto
over-exploitationandhabitatdegradationunderscorethe
impor-tanceofimplementing amore adaptivemanagement approach,
one which appliesmultipleindicators of ecosystem health and
functioning(Raakjaeretal.,2007),andnotbasedsolelyon
fisheries-basedcensusdata
The fisheries of Vietnam have been reviewed in a
num-berofstudiesinvolvingover-exploitationandmanagement(van
Zwieten et al., 2002; Raakjaer et al., 2007; Pomeroy et al.,
∗ Corresponding author Tel.: +81 089 927 9643; fax: +81 089 927 9643.
E-mail address: toddomiller@gmail.com (T.W Miller).
2009),andestablishmentofmarineprotectedareas(Dung,2009; Svensson et al., 2009) Yet, almost no ecological information
is available on exploited fish or invertebrate species, informa-tion of which is essential for ecosystem-based management
of Vietnam’s waters (Raakjaer et al., 2007) and a more func-tional perspective ontheflow of energy throughtheexploited ecosystem Over-exploitation can be reflected in a lowering of average trophic level (Pauly et al., 1998), biomass size spectra (Jenningsetal.,2001),ashifttosmallermoreproductivespecies (Myers, 1993; Jennings et al., 2001), shifts in benthic produc-tion (Jennings et al., 2001; Hiddink et al., 2008)and potential shifts through trophic cascades(Frank etal., 2005).How these are measuredcanbeaccomplishedin-part fromfisheries catch data;however theadditionofotheranalytical methodssuchas stableisotopeanalysisofcarbonandnitrogen,whichcanmeasure sourceproductionandtrophicstructure,showparticularpromise Stable isotopesof carbon and nitrogenhave beenshown as time-averaged measuresofrelative trophic positionand source production ofan organism(Petersonand Fry, 1987)and there-foreameasureoffoodwebtrophicstructure(VanderZandenand Rasmussen,1999),degreeofbenthic–pelagiccoupling(Takaietal., 2002;Mincksetal.,2008;Votieretal.,2010),ontogeneticshifts 0165-7836/$ – see front matter © 2011 Elsevier B.V All rights reserved.
Trang 2(Coleetal.,2004;Milleretal.,2010).Stableisotopesaremeasured
asaratiooftheheavytolightformrelativetoastandardusingthe
followingequation:␦X=[(Rsample/Rstandard)−1]×103,whereXis
theisotopevalueinpartspermil(‰)andRistheratiooftheheavy
tothelightisotopeofthesample(Rsample)toananalyticalstandard
(Rstandard).StandardsarecalibratedtoatmosphericN2fornitrogen
andViennaPeeDeeBelemniteforcarbon(PetersonandFry,1987)
Fornitrogen,theheavier(15N)isotopeisretainedatahigherrate
overthelighterisotope(14N),andthisdifferenceisexpressedasan
approximateenrichmentof3.4‰in␦15Nofanorganismrelativeto
itsdiet(Post,2002).Thisallowsfor␦15Ntobeusedasaneffective
measureofrelativetrophicpositionofanorganism.Differences
in␦15Ncanalsooccuratthebaseofthefoodweb
(phytoplank-ton)and bereflected inhighertrophic levels,where thesource
ofnitrogentoprimaryproducersmayoccurmorefromN-fixing
cyanobacteria(low␦15N)orarefromrecyclednitrate(O’Reillyand
Hecky,2002).Extremelyelevatedlevelscanindicatesomedegree
ofeutrophicationanddenitrification,whichmayoccurnaturally
orfromanthropogenicloading.Carbonstableisotopes(␦13C)are
appliedmoreasarelativemeasureofsourceproduction,because
thedifferencesin␦13Coccurmorebetweenthedifferentsourcesof
carbonfixationatthelevelofprimaryproduction(Fry,2006).For
aquaticsystemsdifferencesin␦13Coccurmorebetweennearshore
(moreenrichedin13C)andoffshorewaters(Milleretal.,2008),
andwithdepth(Bosleyetal.,2004).Measuresof␦15Nand␦13C
thereforeprovidearespectivemeasureofTLandspatialproperties
ofthecoastalcommunity,suchasfrombenthic–pelagiccoupling
orbetweennearshoreandoffshoresystems.Usingstableisotope
analysisinconcertwithcommunitystructuredata,suchascatch
surveyswithquantitativeassessmentofbiomasscanalsoprovide
greaterinsightastothepotentialrelativestrengthsoftrophiclinks
intermsofnearshore-offshoresystemsandalsothebasic
function-ingoftheecosystem
OneofthreemajorcoastalzonesofVietnam,thecentralregion
between10and15◦Nexhibitsstrongsummerupwellingduring
thesouthwestmonsoonmonthsbetweenMayandAugust(Kuo
etal.,2004),contributingnutrientsandmuchoftheprimaryand
highertrophiclevelproductiontotheregion(AnandThu,2007)
PhanThi ´ˆetBay(BìnhThuˆa.nProvince)isjustsouthofthecentral
upwellingcellandisconsideredamajorfisheriesregionofVietnam,
consistingoflocalbottomdraggers,gillnetting,andhook-and-line
fishers.TheshelfregionistypicalofmostofVietnam’scoastline
withdepthsof<50masfaras50kmoffshore,andarelativelyflat
reliefwithbottomsubstratesofsand,mud,andcobble.Asaresult,
thecoastalwatersareeasilyfishedbyuseoftrawlorpushnetsthat
oftenhavesmallmeshsizesthatindiscriminatelytakealmostall
sizesofmacro-organisms(Pomeroyetal.,2009)
Over-exploitation in marine ecosystems can favor smaller,
fastergrowingspecies(Blanchardetal.,2004)butalsoreducedsize
withinaspecies (BevertonandHolt,1957),anda lowertrophic
levelofexploitablebiomass(Paulyetal.,1998).Inthisstudy,by
useofa limitedtrawlsurveyweexaminedthecommunity and
trophicstructureofexploitedbenthic-demersalfishesand
inver-tebratesoffPhanThi ´ˆetBay,Vietnam.Weusedcatchdataandsize
measuresofthemostabundanttaxaandtrophiclevelassignments
from␦15Ntotestthehypothesisthat:(1)theexploitedbiomass
offPhanThi ´ˆetBayisdominatedbysmallernektonwithrelatively
highgrowthrates,and(2)thatTLofthenektoncommunitywould
berelativelylow(TL<3.5).Wealsoapplied␦13Ctodeterminethe
degreeto which benthic and pelagicproduction are
contribut-ingto theproduction of dominant targetspecies Results from
thisstudyprovidethefirstassessmentofVietnam’scoastal
fish-eriesbyintegrationofstableisotopeanalysiswithfisheriescatch
data
2 Methods
2.1 Fieldsampling
Atotalofninebenthic-demersalhaulswereperformedbetween
20and25August,2010forquantifyingthedemersalnektontaxa offPhanThi ´ˆetBay(Fig.1andTable1 andtoobtainsamplesfor stableisotopeanalysis.Thetimeofthisstudywaschosentocapture communitycharacteristicsandisotopic-basedtrophicdynamicsof thesummermonsoonupwellingseason,which typicallyoccurs betweenMayandAugust(Kuoetal.,2004).Benthic-demersalhauls weredoneusingabenthicottertrawlconsistentwithregular fish-inggearbylocalfishers,withamaximummouthopeningof17m wideby15minheight,andanetlengthof30m.Meshsizeatthe mouthwas6cm,taperingdownto1cmtowardthecodend.The trawlwastowedatapproximately3knotswithdurationofhauls varyingduetogearsaturation,inwhichhaulswerediscontinued whenhaul speedwasnotablyreduced Oftheninehauls,eight wereusedforquantifyingspeciescatchesandmeasurementsof fishes,andfourwereusedforstableisotopeanalysis(Fig.1).Upon retrievalofthenet,thecatchwasrandomlydispersedinto40L con-tainers,withthetotalnumberofcontainersconsistingofthetotal catch.Onecontainerwasrandomlyselectedasasubsample,with allmajornektontaxaidentified,enumerated,andupto30 individ-ualsofeachtaxarandomlyselectedandmeasuredinmm(±0.1) forlengthastotal lengthfor fishes,dorsalmantle length(DML) forcephalopods,shelldiameterforgastropodsandshellheightfor bivalvescallops(Pectinidae).Totalcatch,includingspeciescounts andweightsforeachhaulwereestimatedbyusingthe40L sub-sample andmultiplying bythe total numberof 40L containers consistingofthehaulcatch.Weightofeach40Lsubsamplewasalso usedtoestimatethetotalbiomassofcatchforeachhaulusingthe samemethod.Thetotalbiomassofindividualtaxafromeachhaul wasestimatedbytakingthesizedistributionoftheindividuals sub-sampledandusingthelength-weightrelationshipfromFishBase (FroeseandPauly,2010)toobtainanestimateofthe40L subsam-plebiomass,thenmultiplyingbythetotalnumberof40Lcontainers consistingofthetotalhaul.Thelogisticsofcountingandmeasuring everyspecieswasproblematicduetotheveryhighdiversity(>100 speciesoffish)andinmanyinstancesthecryptogenictaxonomyof somegroups.Wethereforefocusedon18dominantfishand inver-tebratetaxawhichtogetherconsistedofover50%ofthecollective totalofnethaulsbybiomassandnumber.Fromeachhaul,nekton communitydatawasthenusedforcommunitystructureanalysis 2.2 Communitystructureanalysis
CommunitystructureanalyseswereperformedusingPC-ORD v4.25(McCuneandMefford,1999)inwhichaninitialmatrixwas establishedbasedonthecatchperuniteffort(CPUE)of individ-ualnektonfrom8hauls(rows)and64taxa(columns).TheCPUE wascalculatedforeachhaulasthenumberofindividualswithin eachtaxadividedbythearea(m2)coveredbythehaul Agglom-erativehierarchicalclusteranalysis(AHCA)usingSørensen(Brae Curtis)distanceandflexiblebeta(ˇ=−0.25)linkagefunctionwas applied toarrange hauls into nekton community-based cluster groups.PriortotheAHCAthematrixwastransformedusing gen-eralrelativizationtoallowfor clustergroupingsbasedmore on speciesassociationsandtoavoidclusteringbasedonhighand low-abundantspecies(McCuneandMefford,1999).Optimumnumber
ofclustergroupsfromAHCAwerebasedonacombinationof sev-eralcriteria: (1) biological meaning; (2) significance and effect size(A)ofgroupsusingamulti-responsepermutationprocedure (MRPP,Sørensendistance),frombothaboveandbelowthe opti-mumdendrogramcutofflevel;and(3)thenumberofsignificant
Trang 3Fig 1.Location of hauls (H-1 to H-9) off Phan Thi ´ˆet Bay (Vietnam) during August 2010 Diamond and arrows denote start and finish of each haul path, respectively Superscript letters denote hauls that were used for community (C) and stable isotope (S) analysis Bathyclines are in m.
Table 1
Summary haul data from off Phan Thi ´ˆet Bay (Vietnam), 20–25 August, 2010 Benthic substrate type follow ) notation of: sand (S), gravelly mud (gM), slightly gravelly muddy sand ((g)mS), gravelly muddy sand (gmS), and gravelly sand (gS) Percent substrate denotes the percent area of the benthic haul consisting of the specific sediment type.
Haul Distance (km) Start lat lon Finish lat lon Average depth (m) Substrate (%)
108◦2043.4E 108◦2413.0E
108 ◦ 23 44.3 E 108 ◦ 20 53.1 E gmS (20)
108 ◦ 20 53.1 E 108 ◦ 24 31.8 E
108◦0934.6E 108◦0752.9E gmS (30)
108 ◦ 07 52.5 E 108 ◦ 02 38.6 E gmS (30)
gS (10)
108 ◦ 02 38.1 E 108 ◦ 03 06.3 E
108◦0306.5E 108◦0410.5E
108 ◦ 04 07.9 E 108 ◦ 13 17.4 E S (40)
gM (10)
◦ ◦
Trang 4indicatorspecies withineach groupbyuseof IndicatorSpecies
procedure,MRPPcomparestheAHCA-basedapriorigroupingsto
a randomizedmatrix and tests thehypothesis of nodifference
betweentwoormoregroups(McCuneandGrace,2002).TheISA
assistedinfurtherbalancingtheimportanceofagroupby
indicat-ingcutofflevelsthatresultinhighestspeciesfidelitytoaparticular
group.Thestatisticalsignificanceofaspeciestoaparticulargroup
inISAisexaminedbyaMonteCarlomethodinwhichsampleunits
arerandomlyreassignedn-timestotestiftheindicatorspecies
val-uesarehigherthanwouldbebychance.Forourstudy,1000runs
wereappliedtoeachMonteCarlosimulation
Ordinationofsampleunits(hauls)inspeciesspacewas
per-formedusingnon-metricmultidimensionalscaling(NMS;Kruskal,
1964)andtocomparetheAHCA-basedclustergroupingsto
envi-ronmentalgradients.Thiswasdonebyincludinganenvironmental
matrixoftheeighthauls(rows)withcolumnsrepresentingthe
fol-lowingenvironmentalvariables:haultimeofday(h),haulduration
(h),depth(m),percentareaofhaulconsistingofsedimenttype,and
theclustergroupcutofflevel.Benthicsedimentinformationwas
providedfromTienandNghi(2006)basedonadetailed
geolog-icalsurveyoftheentireshelf regionofthestudyarea.Foreach
haul,thepercentareaofeach sedimenttype wascharacterized
byoverlayingthehaulpathoverthesedimentmapbyTienand
Nghi(2006),whichwasthenusedintheenvironmentalmatrixas
apercentareaofthehaulpathconsistingofsedimentsubstrate
types(Table1).ThesedimentsubstratetypedescribedbyTienand
Nghi(2006)followedstandardizedmethodofFolk(1954)which
characterizessedimentsbytheproportionalmixturesofdifferent
sedimentgrainsizesofsand,mudandgravel.Thefollowing
sedi-menttypeswerefromthestudyareawithabbreviationsfollowing
Folk’s(1954)notation:sand(S),gravellymud(gM),slightlygravelly
muddysand((g)mS),gravellymuddysand(gmS),andgravellysand
(gS).UsingPC-ORD,wechosetheSørensendistancemeasureand
the‘slowandthorough’optionforNMS,whichwere500iterations
foratwo-dimensionalsolution
2.3 Stableisotopeanalysis
Samplesobtainedforstableisotopeanalysiswerecollectedfrom
each ofthe 18 majorspecies fromfour separatehauls(Fig.1)
Attemptsweremadetoobtainisotopesamplesfromabroadsize
gradienttodetectpotentialontogeneticshiftsin␦13Cand␦15N
Uponcollection,fishandinvertebratesweremeasuredforsize
fol-lowingthedescriptionabove,withpaenidshrimpalsocollectedfor
stableisotopeanalysis;shrimpweremeasuredfromtheendofthe
telsontotheorbitinmm(±0.1).Tissueforstableisotope
analy-sisdependedonthetaxonomicgroup,withanterior-dorsalmuscle
usedforfishes,dorsalmantleforcephalopods,adductormusclein
bivalves,abdominalmuscleinshrimp,andaportionofthe
muscu-larfootingastropods.Extractionofalltissueswasperformedusing
distilled-watercleanedscalpelandforceps.Uponextractionall
tis-sueswereplacedinindividuallylabeledpolyethyleneeppendorf
tubesandplacedundericeforlaterprocessing.Allsampleswere
broughttothelabwithin72hofextractionandshowedno
indi-cationoflossinbiologicalintegrity.Sampleswerethenplacedin
adryingovenat60◦Cfor48h.Afterdrying,sampleswere
pulver-izedtoafinepowderusingamortarandpestlethenapproximately
1mg(±0.1)wasweighedandencapsulatedinatincapsule.Stable
isotopeanalysisofallsampleswereperformedattheCenterfor
MarineEnvironmentalStudies(CMES),Ehime University,Japan,
usingaCarloErbaElementalAnalyzer2500coupledtoa
Finni-ganMATDeltaPlusstableisotoperatiomassspectrometerviaa
ConFlo-IIIcontinuousflowinterface(measurementerrorforboth
carbonandnitrogen±0.3‰).Becausecarbonisotoperatioscanbe
alteredbychangesinlipidsirrespectiveofthecarbonsource,we
usedinitialisotopeanalysestoexaminetheC:Nratioofallsamples, andthoseexceeding3.5werereanalyzedfor␦13Cfollowinglipid removalbytheBlighandDyer(1959)method.SampleswithC:N values<3.5havebeenshowntohavelittleimpactonthedilution
oflipidson␦13Cvalues(Postetal.,2007)
Comparison of ␦13C and ␦15N values between taxa, when applied,wasperformedusinga t-test(˛=0.05).Examinationof size-specificshifts in␦13C and ␦15Nwithineach taxa was per-formedusinglinearregressionanalysis.Toexaminetheimportance
ofsizerangeindetectingsize-specificshiftsin␦13Cand␦15N,from themaximumsize(Lmax)reportedforeachspeciesfromFishBase (FroeseandPauly,2010)wecalculatedtheproportionalsizerange (Lmax)ofindividualsmeasuredinourstudy.Finally,we exam-inedtrophiclevelassignmentsofeachtaxabyuseof␦15NofPOM (valuesfromLoicketal., 2007)asTL 1.0,byzooplanktonasTL 2.0(valuesfromLoicketal.,2007),andbyuseofthebivalve Pla-copectensp.asTL2.0(thisstudy)asthefoodweb␦15Nbasevalue;a pairedtaxat-testwasperformedforcomparisonbetweeneachof thetaxa-specificTLassignments,andalsocomparedtoTLpositions fromestimatedvaluesobtainedfromFishBase(FroeseandPauly,
2010).The␦15Nbasevalueforthefoodwebwasbasedonthe equal-ity(pairedt-testwithnon-significantdifference)oftheprimaryor secondaryproducer-basedTLwiththeFishBase-derivedvaluefrom eitherfooditemsordietanalyses
Assessment of therelative dependence of a species to ben-thicproductionwasobtainedusing␦13Cvaluesofobligatepelagic zooplanktonand benthic inhabitantsas end-member ␦13C val-ues of their respected habitats The percent contribution of benthic production calculated for each nekton was doneusing the following formula from Vander Zanden and Vadeboncoeur (2002)for percentage of contributionoflittoral secondary pro-duction=(␦13Cc−␦13Cp)/(␦13C1−␦13Cp),where␦13Cc,␦13Cp,and
␦13C1denotethemeanvaluesoftheconsumer(nekton),pelagic baseline(zooplankton,valuesfromLoicketal.(2007),ofthesame region),andbenthicbaseline(snailPhaliumglaucum,Family Cas-sidae) As with Vander Zanden and Vadeboncoeur (2002), the baselines were primary consumers (TL 2)and we assumed no trophicfractionationin␦13C
3 Results
3.1 Catchdata Fromtheeightbenthichaulsatotalof1150kgoffish,squid,and otherinvertebrateswerecollected(Table2).Themostnumerically abundanttaxawerethefishblotchfindragonet(Callionymus fila-mentosus),juvenileOctopussp.,andBerberponyfish(Leiognathus berbis),whichaccountedfor9.6,3.2,and2.2%ofthetotalbiomass, respectively.ThehighestintermsofoverallbiomasswereC fil-amentosus,squidLoligojaponicas,andsnakefishTrachinocephalus myopsrepresenting9.6,8.0,and7.8%ofthetotalbiomass(25.4%
oftotal),respectively.Fromallsamplestherewasatotalabsence
ofwhatcouldbecategorizedaslargepredatoryfishes,oreventhe juvenilestages
3.2 Communitystructureanalysis Agglomerativehierarchicalclusteranalysis(AHCA)ofstations resultedinadendrogramwithtwomaingroupsthatwere sepa-ratedatthecutofflevelof44%informationremaining.Thecutoff levelwasbasedonthebiologicalreasoningofthegroupings,while retainingthehighestlevelofpercentinformationremainingand obtainingthehighestwithin-groupagreement(MRPP,A-valueof 0.03).Theonlyotherreasonablecutoffwasat3groupsat approx-imately60%informationremainingwitha slightlyhigherMRPP
Trang 5Table 2
Summary catch data of major fish and invertebrate taxa collected between 20 and 25 August, 2010 off Phan Thi ´ˆet Bay (Vietnam) Catch data is presented as catch-per-unit-effort (CPUE) of individuals per m 2
Invertebrates
Octopus sp., juv 1.2 × 10 −3 2.6 × 10 −3 1.8 × 10 −2 4.8 × 10 −4 1.1 × 10 −3 2.2 × 10 −2 4.5 × 10 −3 3.5 × 10 −3
Cuttlefish 1.0 × 10 −3 1.6 × 10 −3 2.9 × 10 −4 4.5 × 10 −4 4.1 × 10 −3 4.5 × 10 −3 1.3 × 10 −3
Loligo japonica 1.7 × 10 −3 5.3 × 10 −3 1.1 × 10 −3 1.4 × 10 −3 6.9 × 10 −4
Argopecten sp 6.2 × 10 −1 5.0 × 10 −1 1.4 × 10 −1 4.1 × 10 −1 2.3 × 10 −1
Pandalid shrimp 2.1 × 10−1 4.9 × 10−1 1.4 × 10−1 2.8 × 10−1 5.9 × 10−1 6.9 × 10−1 Decapod crabs 9.3 × 10 −1 5.0 × 10 −1 1.2 × 10 −1 2.5 × 10 −1 9.0 × 10 −1 1.9 × 10 −1 1.1 × 10 −1 1.5 × 10 −1
Rajiformes
Anguilliformes
Gymnothorax sp 5.4 × 10 −1 1.2 × 10 −1 6.8 × 10 −1 2.4 × 10 −1 1.3 × 10 −1
Dysomma sp 7.0 × 10−1 1.3 × 10−1 1.9 × 10−1 4.5 × 10−1 2.4 × 10−1 5.8 × 10−1 3.8 × 10−1 Siluriformes
Aulopiformes
Saurida tumbil 1.3 × 10 −1 1.0 × 10 0 1.2 × 10 −1 4.8 × 10 −1 1.9 × 10 −1 1.2 × 10 −1 1.8 × 10 −1 9.8 × 10 −1
Trachinocephalus myops 4.5 × 10−1 2.0 × 10−1 2.9 × 10−1 2.4 × 10−1 2.4 × 10−1 1.2 × 10−1 7.4 × 10−1 4.6 × 10−1 Lophiiformes
Lophiomus setigerus 7.7 × 10 −1
Syngnathiformes
Scorpaeniformes
Scorpaenidae sp 1.5 × 10−1 1.0 × 10 0 2.3 × 10−1 4.5 × 10−1 4.1 × 10−1 9.9 × 10−1 1.4 × 10−1
Inegocia japonica 4.6 × 10 −1 1.6 × 10 −1 2.5 × 10 −1 2.7 × 10 −1 1.8 × 10 −1 5.9 × 10 −1 2.5 × 10 −1 2.8 × 10 −1
Perciformes
Mene maculata 7.7 × 10 −1
Leiognathus berbis 1.5 × 10 −1 1.3 × 10 −1 4.8 × 10 −1 5.7 × 10 −1 6.7 × 10 −1 2.9 × 10 −1 1.1 × 10 −1 9.1 × 10 −1
Apogon spp 6.9 × 10−1 4.3 × 10−1 1.4 × 10−1 1.1 × 10−1 7.8 × 10−1 7.6 × 10−1 3.4 × 10−1 9.4 × 10−1
Alectis ciliaris 2.3 × 10 −1
Selaroides leptolepis 2.3 × 10 −1 5.0 × 10 −1 6.8 × 10 −1 1.2 × 10 −1 2.8 × 10 −1 3.5 × 10 −1
Perciformes
Siganus spp 7.7 × 10 −1
Nemipterus spp 7.7 × 10 −1 4.0 × 10 −1 4.2 × 10 −1 3.9 × 10 −1 1.5 × 10 −1 1.2 × 10 −1 3.2 × 10 −1 8.3 × 10 −1
Lutjanus sp 2.3 × 10−1
Paracaesio sp 7.7 × 10 −1 4.0 × 10 −1 6.8 × 10−1 1.9 × 10−1 1.2 × 10−1 1.1 × 10−1
Opistognathus nigromarginatus 3.9 × 10 −1 4.0 × 10 −1 3.4 × 10 −1 2.3 × 10 −1 2.2 × 10 −1 1.2 × 10 −1 2.8 × 10 −1 3.5 × 10 −1
Priacanthus macracanthus 7.7 × 10 −1 6.8 × 10 −1 9.5 × 10 −1 5.6 × 10 −1 2.9 × 10 −1 5.6 × 10 −1 2.8 × 10 −1
Sillago sihama 7.1 × 10 −1 6.8 × 10 −1 1.5 × 10 −1 5.9 × 10 −1 5.6 × 10 −1 6.9 × 10 −1
Callionymus filamentosus 4.5 × 10 −1 1.9 × 10 −1 1.5 × 10 −1 6.9 × 10 −1 5.3 × 10 −1 4.1 × 10 −1 1.5 × 10 −1 2.8 × 10 −1
Synchiropus sp 2.7 × 10−1 9.5 × 10−1 9.0 × 10−1 1.6 × 10−1 4.0 × 10−1 1.4 × 10−1
Pristotis obtusirostris 3.9 × 10 −1 8.0 × 10 −1 1.4 × 10 −1 1.9 × 10 −1 3.4 × 10 −1 1.2 × 10 −1 4.2 × 10 −1
Eleotridae spp 2.5 × 10 −1 4.0 × 10 −1 2.5 × 10 −1 4.8 × 10 −1
Pleuronectiformes
Pseudorhombus arsius 7.0 × 10 −1 5.0 × 10 −1 1.3 × 10 −1 9.5 × 10 −1 3.4 × 10 −1 9.4 × 10 −1 1.5 × 10 −1 1.4 × 10 −1
Cynoglossus puncticeps 5.4 × 10−1 3.0 × 10−1 1.9 × 10−1 4.8 × 10−1 1.3 × 10−1 1.6 × 10−1
Tetraodontiformes
Paramonacanthus japonicas 2.1 × 10 −1 1.0 × 10 0 2.1 × 10 −1 5.7 × 10 −1 1.4 × 10 −1 7.6 × 10 −1 1.5 × 10 −1 2.3 × 10 −1
× 0
Trang 6Fig 2.Ordination plots of stations in species space from a two-dimensional solution.
Filled and open circles represent the two major cluster groups Most significant
vec-tors shown denote bottom substrate types sand (S) and gravelly muddy sand (gmS)
following Folk’s (1954) notation Species locations are based on species-specific
centroids; species abbreviations are in Table 3
A-value(A=0.07),howeverISAresultsindicatedonlysignificant
indicatorspeciesfromtwoofthethreegroups.Indicatorspecies
analysisusingtwogroupsshowedonegroupwiththree
indica-torspecies(Trypauchenvagina,Decapterussp.,Carangoidessp.)and
anotherwithtwo(Sauridatumbil,Pristotis obtusirostris).Results
fromNMSshowedatwo-dimensionalsolution(stress=3.2)with
thetwoclustergroupsbeingmostseparatedbybottomsediment
typesofsandandgravellymuddysand(Fig.2).TheNMSalongaxes
1and2wereabletoexplain85%ofthevariation,with75%explained
alongaxis1(Fig.2).IndicatorspeciesofT.vagina,Decapterussp.,
andCarangoides sp.weremost associatedwithgravellymuddy
sandwhereasS.tumbilandP.obtusirostrisweremostassociated withsand(Fig.2).Otherenvironmentalparametersoftimeofday, durationofhaul,anddepthwerefoundnon-significant
3.3 Stableisotopeanalysis 3.3.1 Trophicstructure Fromthetaxameasuredforstableisotopes,thebivalvescallop Placopectensp.expressedthelowestaverage␦15N,followedbythe scallopArgopectensp.andfishInegociajaponica(mean␦15N=6.4 and7.7‰,respectively);highest␦15NwereexpressedinL.japonica (mean␦15N=11.1),followedbyT.myopsandCynoglossuspuncticeps (␦15N=10.8and10.6‰,respectively)(Table3andFig.3) Compar-isonofthedifferenttrophiclevelestimatesforeachspeciesbased
onFishBase’sestimatesandthosefrom␦15NbasevaluesfromLoick
etal.(2007)usingPOM(primaryproducer,TL=1)andzooplankton (primaryconsumer,TL=2),andfromourstudyusingPlacopecten
sp.(our study,primary consumer), showed␦15Nbase from POM wassignificantlydifferentfromallothermethods(pairedt-test,
p<0.001),withbothzooplanktonandPlacopecten-based␦15Nbase
TLestimatesbeingnon-significantlydifferentfromFishBase’s val-ues(bothp-values>0.10)andbetweeneachother(p=0.36).Using thePlacopecten-basedTLestimates,ofthe19speciesoffishand invertebratesanalyzed,15werebetweenTL3.0and3.8;thefish InegociajaponicawastheonlyfishtoexhibitaTLbelow3.0(mean 2.8),andtheoverallhighestwasthesquidL.japonica(TL3.8),with highestOsteichthyesbeingT.myopsandC.puncticepsbothatTL3.7 (Fig.3)
Of19taxaanalyzedforsize-specificontogeneticshiftsin␦15N, nineshowedasignificantpositiverelationship.Fishtaxa express-ingthistrend hada greaterproportionalsizerange oftheLmax measured(meanandmaximumLmax=52and40%,respectively) comparedtothosethatfailedtoshowatrend(meanLmax=33%) Withtheexceptionofpandalidshrimpandtheturbinesnail,all taxawhich displayedsignificantsize-specificshiftsin ␦15Nalso expressedshiftsin␦13C(Table4).Therelationshipbetween␦13C and␦15Nwassignificantin11ofthe19taxa(Table4);ofthese, withtheexceptionofshrimp,allhadsignificantontogeneticshifts
in␦15N
Table 3
Summary results from stable isotope analysis and estimated trophic positions of fish and invertebrate species off Phan Thi ´ˆet Bay (Vietnam) Trophic position was based on the mean ␦ 15 N of Placopecten sp (placo) as trophic position 2, with subsequent trophic positions every 3.4‰ increase in ␦ 15 N Zooplankton (zoo) values are from Loick et al (2007) Species abbreviations are in Table 3
Taxa ( Figs 2 and 3 label) n ␦ 15 N Ave (SD) ␦ 13 C Ave (SD) C:N Ave (SD) Length Ave (cm) TL Lmax (cm) Invertebrates
Fishes
Trang 7Fig 3.Mean (SD) values of benthic-demersal fish (filled circles), pelagic fish (open circles), benthic invertebrates (filled triangles), and demersal-pelagic invertebrates (open triangles) Trophic position was based on the mean ␦ 15 N of Placopecten sp (placo) as trophic position 2, with subsequent trophic positions every 3.4% increase in ␦ 15 N Zooplankton (zoo) values are from Loick et al (2007) Species abbreviations are in Table 3
Table 4
Regression results of within-species ␦ 15 N and ␦ 13 C and length, and between ␦ 15 N and ␦ 13 C (␦ 15 N − ␦ 13 C) Significant linear relationships (p < 0.05) are in bold.
fromLoicketal.(2007)usedforthepelagiccontributionof
sec-ondaryproduction,thebivalvePlacopectensp.expressedthelowest
overalldependenceonbenthicsecondaryproduction,witha con-tributionof34%.Comparisonofthespecies␦13Cvaluestowhether theywasdesignatedasbenthicordemersal-pelagicfishor inver-tebratesshowednoparticulartrend(Fig.3)
4 Discussion
4.1 Catchandcommunitystructure Ourstudyisthefirsttoexaminethecommunitystructureand trophic dynamicsof thebenthic-dermersal shelf ecosystem off Vietnam’scoastalwaters.Theresultsfromcommunitystructure analysis showed differences in species composition as related
to sediment type (Fig 2 indicating community heterogeneity
inshelf watersthathavelowbenthic relief.IndicatorspeciesT vagina,Decapterussp.,andCarangoidessp.showedanassociation
Trang 8with gravelly muddy sand substrate, whereas S tumbil and P.
obtusirostrisweremostassociatedwithsand.BothDecapterussp
andCarangoidessp.areinthejackfamilyCarangidae,andaremore
demersal-pelagicopportunists,notwhatwewouldexpecttobe
closelyassociatedwitha particularsediment type.Itispossible
itsoccurrencemaybeduetopreferentialforagingoversand-mud
substrate at the time of this study or an artifact of sampling
froma relativelylargesamplesize.ThegobyT.vaginahowever
is a known burrower and possibly maybe more connected to
a sand–mud substrate The two species associated with more
sandsubstrate,S.tumbiland P.obtusirostrisareboth commonly
associated with flat-relief trawling grounds (Froese and Pauly,
2010),andP.obtusirostrisisinparticularknowntoexistoversandy
substrate(Allen,1991).Althoughindicatorspecieswerefoundin
ouranalysis,thegreatmajority oftaxaweresharedamongthe
samplehauls(Table2)indicatingthat manyspecies arewidely
distributed across substrate types The relatively weak
within-groupagreementmeasuresfromourMRPP analyses(A=0.03to
0.07)maybeduein-parttothisandcautionshouldbemadeinthe
interpretationoftheclustergroups.Formanagementoftheregion
itwouldappearthatregionsofsandandmudcouldreasonablybe
managedinthesame‘zone’habitattype
4.2 Stableisotopeanalysis
4.2.1 Trophicanalysis
Theoveralltrophicstructureobservedshowednotruepiscivory
(TL4)withalmostallspeciesatorabovesecondaryconsumer(TL
3).Thiswassimilarlyobservedintermsofbiomass,with
approxi-mately40%ofthetotalbiomassfromsixnektontaxawithamean
TLof3.3.ThesquidL.japonica(8.0%oftotalbiomass)wasthe
high-estTLof3.8,followedcloselybyT.myops(7.8%ofbiomass)andC
puncticeps(<1.0%ofbiomass).Formosttaxathereislittledietary
informationtoconfirmtheirobservedtrophiclevels.Loligosquid
havebeenobservedtoconsumeavarietyofpreyfrom
zooplank-tontofishprey(MillerandBrodeur,2007)indicatingaTLbetween
3and4.Thiswassimilarlybeenobservedindietanalysisofthe
snakefishT.myops,inwhichdominantpreyaresmallfishesand
crustaceans(Fischeretal.,1990;SadovyandCornish,2000).Itis
apparentfromthissurveythattherewasanabsenceoftrue
picivo-rouspredators(TL4),eitherbecausethetrophicpotentialofsome
speciesoffisheshasbeenreducedduetotheabsenceoflarge
indi-vidualsorduetotheneareliminationofpredatoryspeciesfrom
overharvest.Ineithercasethisissuggestiveofafished-downfood
webasdefinedbyPaulyetal.(1998).Sharksandotherroaming
pelagicspeciesmayrepresenthighertrophic levelshoweverwe
madenosuchcollectionsofthesetaxa,andtheywereevenabsent
fromlocalmarketsinPhanThi ´ˆet.Furthermore,theproportional
maximumsizeofspeciesinoursamples(Lmax)tothemaximum
sizereportedforeachspecies(Lmax)wereonaverage64%ofthe
LmaxforeachspeciesasreportedinFishBase(Froeseand Pauly,
2010),indicatingsmallerindividuals
Atthetimeofthisstudyanumberofspeciesdisplayed
posi-tiveontogeneticshiftsin␦15Nindicativeofincreasingtrophiclevel
withbodysize(Table4).Significant␦15N-dependentontogenetic
shiftswereobservedwhenthesizerangeofindividualswereon
average52%ofthemaximumlengthrange(Lmax),whereas
non-significantrelationshipswereassociatedonaveragewith33%ofthe
proportionofLmaxexamined.ThismatchesfairlycloselytoGalván
etal.’s(2010)findingsthatontogeneticstudiesshouldaimfor>40%
ofLmax.Itisthereforelikelythatinsometaxaaninsufficientsize
rangewasobtainedtocaptureontogeneticshift,possiblyduetoa
lackoflargeindividualsduetooverharvest.Withtheexceptionof
snailandshrimp,allspecieswhichexhibiteda␦15Nshiftinsizealso
hadasimilardirectionalshiftin␦13C.Itislikelythisshiftin␦13C
wasanontogeneticshiftfromfeedingonmoresmall
zooplank-tivorouspreytohighertrophiclevelpreythataremorelinkedto
13C-enrichedbenthicproduction.Supportingthisisthefactthatthe greybonnetgastropod,P.glaucum,showednosuchshiftin␦13C, likelyduetoitsinabilitytoswimandaccessothercarbonsources whereasthenektonweredisplayingthischange
4.2.2 Benthiccontribution For most nekton taxa, at the time of this study 34–77%
of production was derived from secondary benthic production Understandably,mostofthebenthic-orientedinvertebratetaxaof juvenileOctopussp.,cuttlefish,Argopectensp.,andpandalidshrimp expressedthehighestlevelsofbenthic-dependence(≥60%).More demersalnektonwithagreatercapacitytoswimdisplayed rela-tivelylowerdependenceofbetween38and58%,suggestingthere
isahighdegreeofbenthic–pelagiccouplingwithinthissystem Fur-thermore,theabsenceofaclearseparationin␦13Cbetweennekton consideredbenthicandthosemoredemersal-pelagic(Fig.3) indi-catessignificantexchangebetweensurfaceandbenthicproduction Thehighbenthic–pelagiccouplingobservedisunderstandable giventhattheshelfzoneofourstudyisrelativelyshallow(≤40m) anditispartofthecentralupwellingzoneofVietnam.Theextentto whichfisheriesactivitiesmayinfluencebenthicproductioninthis systemisdifficulttoascertain.FromtheNorthSea,Heath(2005) observedhighexploitationofbenthicfisheswhichdecreased pre-dationpressureonbenthicinvertebratesandthereforeincreased theirproduction.Mostofthebottom-fishingvesselsof Vietnam usesmall-meshnetsthatretainallbutthesmallestoffishesand invertebrates(Pomeroyetal.,2009),whichmayexplainthatmost
of thebiomass wasassociated withcephalopods, smallshrimp andfishes,whichweregenerallystronglytiedtobenthic produc-tion.Thesetaxaalsoexhibitahighcapacityforreproductionand growth,whichmayallowforthemtoquicklyexploitopenniches
byfisheries-relatedreleasefrompredationandcompetition
5 Conclusions
Nearlyallofthetaxacollectedatthetimeofthisstudy com-monlyoccurinregionsthroughouttropicalandsubtropicalwaters
ofSoutheastAsia,andtheyarerepresentativeofmanyofthe har-vested taxa fromcoastal fisheries Despite their ecological and economicimportancewefoundverylittlebiologicalinformation
ontheseorganismsthroughouttheirrange,andvirtuallyno infor-mationfromVietnam
Ourapproach ofcombiningstableisotopeanalysistosurvey catchdata provided a very powerfulmethod in examiningnot only the trophic dynamics of individual species, but alsofrom muchoftheexploitedproductionofthesystem.Inparticular,our resultsindicatedarelativelytruncatedfoodwebwithabiomass dominatedbysmallfishesandcephalopods.Fromheavilytrawled waters of the Bay of Biscay (Atlantic), Blanchard et al (2004) testedthe‘dynamicequilibriummodel’byHuston(1994),which states in-partthat heavilyexploitedsystemswould favor more scavenger-typespeciesthat caneffectivelygrowand reproduce betweendisturbanceevents(trawls),whereasless-exploited sys-temswouldallowformorelargerandslower-growingspecies.In thecontextofthe‘dynamicequilibriummodel’,theimportanceof smallscavengers(octopus,cuttlefishandshrimp),aswellassmall fisheswithhighgrowthand reproductiveratesfromourstudy stronglysuggestsaheavilyexploitedsystem
The results from our study provide a benchmark by which futurestudiescanassesschangesinrelativetrophiclevelofspecies withchangesinfisheries management.Expansionof stable iso-topestudiestootherregionsofSoutheastAsiawouldprovidea morecomprehensivepictureastowhatdrivestrophicstructurein exploitedandrelativelyunexploitedecosystems,andwouldhelp revealtheimportanceofover-exploitationinshapingfoodwebs
Trang 9We wish tothank Nguyen Tai Tue, H Hamaoka and J
Shi-bata for assistance in this research, and special thanks to two
anonymousreviewersofthemanuscript.Thisprojectwasfunded
throughtheTRIGAProjectofHanoiUniversityofScience,Vietnam
NationalUniversity (VNU),Hanoi,Vietnam,andtheGlobal
Cen-terofExcellence(GCOE),fromEhimeUniversity,CenterforMarine
EnvironmentalStudies,Matsuyama,Japan
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