DNA Barcoding reveals targeted fisheries for endangered sharks in Indonesia.

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DNA Barcoding reveals targeted fisheries for

endangered sharks in Indonesia

ARTICLE

in

FISHERIES RESEARCH · APRIL 2015

Impact Factor: 1.9 · DOI: 10.1016/j.fishres.2014.11.003

CITATIONS

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302

13 AUTHORS

, INCLUDING:

Dian Pertiwi

Indonesian Biodiversity Research Center

1

PUBLICATION

2

CITATIONS

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Rizki Wulandari

San Diego State University

2

PUBLICATIONS

2

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Dita Cahyani

Indonesian Biodiversity Research Center

6

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Gusti Ngurah Mahardika

Udayana University

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ContentslistsavailableatScienceDirect

Fisheries

Research

jo u r n al h om ep ag e :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

Short

Communication

DNA

barcoding

reveals

targeted

fisheries

for

endangered

sharks

in

Indonesia

Andrianus

Sembiring

a,g

,

Ni

Putu

Dian

Pertiwi

a

,

Angka

Mahardini

a

,

Rizki

Wulandari

a

,

Eka

Maya

Kurniasih

b

,

Andri

Wahyu

Kuncoro

c

,

N.K.

Dita

Cahyani

a

,

Aji

Wahyu

Anggoro

a

,

Maria

Ulfa

d

,

Hawis

Madduppa

b

,

Kent

E.

Carpenter

e

,

Paul

H.

Barber

f

,

Gusti

Ngurah

Mahardika

a,∗

a_The_Indonesian_Biodiversity_Research_Centre,_The_Animal_Biomedical_and_Molecular_Biology_Laboratory_of_Udayana_University,_Jl_{Sesetan-Markisa}_6, Denpasar,Bali,Indonesia

b_Faculty_of_Fisheries_and_Marine_Science,_Bogor_Agricultural_University,_Jl_Rasamala,_Bogor,_West_Java,_Indonesia

c_Marine_Science_Department,_Faculty_of_Husbandry,_Fisheries,_and_Marine_Science,_University_State_of_Papua,_Jalan_Gunung_Salju_Amban,_Manokwari, Papua,Indonesia

d_Flora_and_Fauna_{International,}_Jl_Cumi-Cumi_15,_Banda_Aceh,_Sumatra,_Indonesia e_Department_of_Biological_Sciences,_Old_Dominion_University,_Norfolk,_VA_23529,_USA

f_Department_of_Ecology_and_Evolutionary_Biology,_University_of_California_Los_Angeles,_Los_Angeles,_CA_90095-7239,_USA g_Master_program_in_{Environmental}_Sciences,_Udayana_University,_Jl_P.B._Sudirman,_Denpasar,_Bali,_Indonesia

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received9October2014

Receivedinrevisedform4November2014 Accepted9November2014

HandlingEditorProf.GeorgeA.Rose Availableonline11December2014

Keywords:

Shark DNAbarcoding Indonesia

a

b

s

t

r

a

c

t

Sharksareapexpredatorsandkeystonespeciesthathaveaprofoundinfluenceontheecologyand food-webdynamicsofcoralreefsandepipelagicmarineecosystems.However,sharksarebeingheavily overfishedcompromisingthehealthoftheworld’sreefsandpelagicenvironments.AlthoughIndonesia istheworld’slargestandmostdiversecoralreefecosystem,informationontheexploitationofsharks inthisregionisscarce.ResultsofDNAbarcodingofsharkfinrevealedtwoalarmingfindings:(1)a rar-ityofreefsharksthatshoulddominateIndonesia’scoastalecosystems,and(2)afisherythattargets endangeredsharks.Thediversityandnumberofthreatenedspeciesrecoveredinthisstudyhighlights theurgentneedforimprovedregulationandcontrolofIndonesia’ssharkfishery.

1. Introduction

Asapexpredators,manysharksarekeystonespeciesthathavea significantinfluenceontheecologyandfood-webdynamicsofcoral reefandepipelagicoceanecosystems(Ferrettietal.,2010;Myers etal.,2007).However,sharkpopulationshavedeclinedglobally byupto90%(Myersetal.,2007),largelyasaresultofa multi-billiondollarindustrythatharvestshundredsofmillionsofsharks annually(Chapmanetal.,2013)andlifehistorytraitssuchaslow fecundity,late maturity,and a longgestationperiod that make sharkpopulationsparticularlysensitivetooverfishingandhabitat degradation(Baumetal.,2003).Globalsharkfisheriesarelargely

∗ Correspondingauthorat:TheIndonesianBiodiversityResearchCentre,The AnimalBiomedicalandMolecularBiologyLaboratoryofUdayanaUniversity,Jl Sesetan-Markisa6,Denpasar,Bali80226,Indonesia.Tel.:+623618423061; fax:+62361223791.

E-mailaddress:[email protected](G.N.Mahardika).

drivenbythedemandforsharkfins,akeyingredientintheAsian delicacy,sharkfinsoup.

TheConventiononInternationalTradeinEndangeredSpecies of Wild Fauna and Flora (CITES) currently lists many sharks asAppendixI(speciesthreatenedwithextinction)orAppendix II (species where trade must be regulated to prevent over-utilization).Afurther60sharksandraysarelistedas“vulnerable” or“nearthreatened”(Camhietal.,2009).WhileCITESdesignation shouldpromoteregulationofinternationaltradein shark prod-ucts,theprimarycommodityresultingfromsharkfisheriesarefins. Wholesharksarerarelylandedatcommercialports(Clarkeetal., 2006;Liuetal.,2013)throughoutmuchoftheworld;insteadsharks are“finned”atsea,aprocessbywhichfinsareremovedand bod-iesdiscarded,andthenfinsdriedforsaletowholesalers(Fig.1). Thisprocessiscommonwhethersharksarethetargetedfisheries speciesortheresultofby-catch(Afonsoetal.,2012).Driedfins typ-icallylackkeydiagnosticfeatures,makingidentificationoffinsto species,andthereforeregulationoftradeinfins,extremely chal-lenging.WhileDNAbarcodingbasedona shortfragmentofthe mitochondrialcytochromeoxidaseI(COI)genehasbeenusedto

http://dx.doi.org/10.1016/j.fishres.2014.11.003

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Fig.1.Photographsofsharkandshark-finsamplecollection.Sun-driedfins(left)inBali,November1,2011;wholesharkandelasmobranchauctionattheharbourinLombok (right),July12,2012.

Source:IndonesianBiodiversityResearchCentre.

identifyfinstospecies(Holmesetal.,2009;Moftahetal.,2011; Pinhaletal.,2012;Wongetal.,2009),thistechniqueisnotwidely usedtopromoteregulationofsharkfisheries.

Comprisedofmorethan17,000islands,Indonesiaisthelargest geographic areaand heart of the “Coral Triangle”, a six-nation regionofSouthEastAsiathatishometotheworld’smostdiverse seas(Carpenteretal.,2011;DubinskyandStambler,2011;Roberts et al., 2002). Approximately 30% of the world’s shark and ray speciesarepresentinthisregion(LastandStevens,1994)including regionalendemicsuniquetotheCoralTriangleandotherbroadly distributedIndianandPacificOceanspecies(Barnettetal.,2012; Bondetal.,2012;Campanaetal.,2011;Nadonetal.,2012;Oliver etal.,2011).Thehighvalueofsharkfinsonglobalmarketshas sparked rapid growth in shark-fishing in Indonesia focused on supplyingfinstogrowingmarketsinAsia.Comprisedof a mix-tureofcommercialandopportunisticartisanalfisheries,thetotal elasmobranch catch in Indonesia was estimated at more than 110,000 tonnes in 2007 (Camhi et al., 2009), representing the largestrecordedharvestintheworld(Tull,2009).Despitethesize andvalueofIndonesiansharkfisheries,theexpansivenatureof Indonesiacombinedwiththediffusenatureofthesharkfinfishery meansthatbasicfisheriesdataneededforeffectivemanagement andregulationinIndonesia(e.g.speciescomposition,harvest lev-els,etc.)isseverelylacking.

2. Materialsandmethods

Wecollected582sharkfinsfromtraditionalfishmarketsand shark-finexportersacrossIndonesiafrommid-2012tomid-2014, includingAceh,Jakarta,WestJava,CentralJava,EastJava,Bali,West Kalimantan,South Sulawesi,North Sulawesi,Maluku,andWest Papua.Additionalsampleswerecollectedfromsharkfin export warehousesinCilacap(CentralJava)andTanjungLuar(WestNusa Tenggara)(Fig.2).Wesampleda thinsliceof tissuefromdried finsinfishmarkets.Inexportwarehouses,werandomlysampleda minimumoffivecaudalfinsfromboxesoffreshfins.Thetotal num-bersofdriedandfreshfinswere164and418,respectively.Samples werepreservedin96%alcoholforsubsequentDNAanalysis.

Whole DNA was extracted using a simple Chelex protocol (Walshetal.,1991).Afragmentofthemitochondrialcytochrome oxidaseCsubunit-1(COI)wasamplifiedusingAmplyTaqRedTM (AppliedBiosystems)andthestandardfishDNA-barcodingprimers Fish-BCL andFish-BCH(Baldwinetal.,2009).Theamplification parameterswere aninitialdenaturationof94◦_C _for₁₅_min,₃₈

cyclesof94◦_C_for ₃₀_s, ₅₀◦_C _for₃₀_s,_and ₇₂◦_C _for₄₅_s,_with_a

finalextensionof72◦_C_for₅_min._PCR_products_were_visualized_via

electrophoresisonagarosegelsandethidiumbromidestaining. The COI fragment could be amplified and sequenced from allsamples.Thesequencingwasconducted usingboth forward and reverse directions at the University of California Berkeley SequencingFacility.TheresultwasalignedusingMEGA5(Tamura et al., 2007).We then determined species identity by compar-ing sequences to GenBank and Barcode of Life Data Systems (http://www.boldsystems.org) databases enforcing a sequence homologythresholdof>99%aspreviouslyapplied(Liuetal.,2013).

3. Results

DNAbarcodingofa600–654bpofmitochondrialCOIgene suc-cessfullydeterminedthespeciesidentityof582finscollectedfrom marketsacrosstheIndonesianarchipelagobasedona99%sequence similaritycriterioninGenBankandBarcodeofLifeDataSystems (BOLD)databases.Intotal,analysesdetermined40differentshark species(Table1).Fivespecies(silky,scallopedhammerhead,blue, bigeyethresher,andthreshersharks)representedmorethan50% ofthetotalfinssampled.Silky(19.10%),scallopedhammerhead (10.50%)andbluesharks(8.20%)werethemostcommonspecies recovered,followedbybigeyethresher(7.60%)andthreshersharks (7.20%).Incontrast,29specieswereobservedatlessthan2%ofthe totalsamples,including7speciesthatwererepresentedbyonly oneortwosamples.

Thevastmajorityofthesamples(92%)werelistedas “endan-gered”(1)“vulnerable”(12)or“nearthreatened”(19)whileonly 4specieswerelistedasspeciesofleastconcern.Theremaining 3speciesareclassifiedasdatadeficient.Similarly,83%ofspecies identifiedwerepelagicspeciesofsharkwhileonly17%werereef sharks.

4. Discussion

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Fig.2. Samplingsitesofshark-fincollectioninIndonesiaduring2012–2014.ThesiteswereLampulo,BandaAceh(1),Lhokseumawe,BandaAceh(2),Meulaboh,West Aceh(3),Langsa,BandaAceh(4),SimeulueIsland,Aceh(5),MuaraBaru,Jakarta(6),PelabuhanRatu,WestJava(7),PelabuhanPerikananSamudraCilacap,CentralJava(8), PelabuhanPerikananMuncar,EastJava(9),Bali(10),TanjungLuar,Lombok(11),Paotere,Makassar,SouthSulawesi(12),PelabuhanPerikananBitung,NorthSulawesi(13), PasarRemuSorong,WestPapua(14),PasarJimbatanPuriSorong,WestPapua(15),PasarSanggengManokwari,WestPapua(16),PelabuhanSamudraAmbon,Maluku(17), SingkawangWestKalimantan(18).

asspeciesof“leastconcern”.Giventhatsharksarecharacterized bylowfecundity,latematurity,andalonggestationperiod(Baum etal.,2003),thefindingthatnearly93%ofallfinssampledcame fromspecies viewedby IUCN as threatened withextinction or vulnerabletoover-exploitationstronglysuggeststhatIndonesian sharkfisheriesareunsustainable.

Fishing effortfor sharks wasstrong biased with more than 50% of thetotal samplescoming fromfive species: silky, scal-lopedhammerhead,blue,bigeyethresher,and threshersharks. The endangered scalloped hammerhead (CITES Appendix 1) representedmorethan10%ofthetotal finssampled.Most dis-turbing,thishighfrequencyofscallopedhammerheadswasseen acrosssamplinglocations,includingAceh,Java,Lombok,Sulawesi, KalimantanandPapua,indicatingthatfishermanarelikely specif-ically targeting these endangeredsharks acrossthe Indonesian archipelago.Similarly,thevulnerablethresherandbigeyethresher sharkscomprisednearly15%ofthetotalcatch,whilethenearly threatenedsilkyand bluesharksrepresented19.10% and 8.20% respectively.ThehighfrequencyofthesespeciesacrossIndonesia stronglysuggeststhattheyarenottheresultofby-catchor small-scaleartisanalfisheries,butinsteadresultfromlarge-scaletargeted sharkfisheries.

Anotherdisturbingfindingofourstudywasthatthevast major-ity (83%) of the species recovered were pelagic sharks, while commonCarcharhiniformes suchasGalapagos(0.52%),grey reef (01.20%),black-tipreef(3.61%),andwhite-tipreefshark(0.86%) thattypicallydominatecoralreefecosystemswereextremelyrare aswerecommonreefOrectolobiformes,suchastawnynurse(1.37%) andbrown-bandedbamboo(0.86%)sharks.Onpristinecoralreefs, reefsharksmake upa nearly63% oftotal fishbiomass(Sandin etal.,2008).BecausethegreatestfishingpressureinIndonesian watersisinshallowcoastalareaswherereefsharkstypicallythrive, thealarminglylownumberofreefsharksrecoveredinour sam-plingstronglyindicatesthatreef-sharkpopulationsinIndonesia havecollapsed,mostlikeduetooverfishing(AllenandErdmann, 2012)ashappenedintheGreatBarrierReef(Robbinsetal.,2006),

and/orreefdegradation(Burkeetal.,2011).Lowincidenceofreef sharksisconsistentwiththerarityofsharksightingsduringscuba activitiesacrossmostofIndonesia,withtheexceptionofregions ofEasternIndonesiasuchasRajaAmpat(M.Erdmann,pers. com-mun.).Indeedresultsshowthat18reefsharkfinswereidentified fromsamplesinWesternIndonesiaand19inJava,whereas32and 36wereidentifiedfromEasternIndonesiaandCentralIndonesia. Eventhemostcommonreefsharkinoursampling,theblacktip, wasnotobservedin75%ofsamplinglocationsand59%of black-tipfinscamefromonelocalityinPapua.Thesedatasuggestthat manyreefsharksmaybeecologicallyextinctinpartsofIndonesian waters.

While sampling revealedthat a diversity of sharks entering the Indonesian shark fin trade, three species represented new records for Indonesia, including the western spotted gummy, galapagos, andwhitecreek sharks.It is notclearwhetherthese sharkswerecaughtwhilemigratingthroughIndonesianwatersor whetherthereareresidentpopulations.Iftheformeristrue,fishing pressureswithinIndonesianwaterscouldhaveanegativeimpact onresidentpopulationsoutsideIndonesia.Ifthelatteristrue,the rarityofthesespeciesinoursamplemayindicatethattheir popu-lationsareheavilydepressed,requiringspecialconservationstatus withinIndonesia.

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Table1

Distribution,catchfrequency,IUCN/CITESstatusofvarioussharkspeciesharvested indifferentgeographicalareasinIndonesia.

No Species Total Frequency IUCNstatus

1 Carcharhinus falciformis

111 19.07% Nearthreatened

Silkyshark

2 Sphyrnalewini 61 10.48% Nearthreatened

Scalloped hammerhead

3 Prionaceglauca 48 8.25% Endangered

Blueshark 4 Alopias

superciliosus

44 7.56% Vulnerable

Threshershark

5 Alopiaspelagicus 42 7.22% Vulnerable

Bigeyethresher shark

6 Carcharhinussorrah 39 6.70% Nearthreatened Spottailshark

7 Carcharhinus limbatus

Blacktipshark

8 Isurusoxyrinchus 21 3.61% Vulnerable

Shortfinmako 9 Rhizoprionodon

acutus

18 3.09% Leastconcern

White-eyedshark

10 Squalushemipinnis 17 2.92% Nearthreatened

Indonesian shortsnoutspurdog

11 Galeocerdocuvier 12 2.06% Nearthreatened

Tigershark

12 Isuruspaucus 11 1.89% Vulnerable

Longfinmako 13 Carcharhinus

longimanus

10 1.72% Vulnerable

Whitetipoceanic shark

14 Centrophorus niaukang

Taiwangulper shark 15 Carcharhinus

melanopterus

9 1.55 Nearthreatened

Blacktipreefshark

16 Carcharhinussealei 9 1.55% Nearthreatened

Blackspotshark 17 Carcharhinus

brevipinna

Spinnershark 18 Hemipristis

elongata

Snaggletoothshark

19 Nebriusferrugineus 8 1.37% Vulnerable

Tawnynurseshark 20 Carcharhinus

amblyrhynchos

Greyreefshark

21 Hemitriakisfalcata 7 1.20% Leastconcern

Sicklefinhound shark 22 Mustelus

lenticulatus

Spotted smoothhound 23 Hemigaleus

microstoma

6 1.03% Vulnerable

Sicklefinweasel shark

24 Loxodon macrorhinus

Jordan’sblue dogshark

25 Sphyrnazygaena 6 1.03% Vulnerable

Smooth hammerhead

Table1(Continued)

No Species Total Frequency IUCNstatus

26 Chiloscyllium punctatum

Brownbanded bambooshark

27 Triaenodonobesus 5 0.86% Nearthreatened

Whitetipreefshark 28 Hemitriakis

indroyonoi

4 0.69% Datadeficient

Indonesian houndshark 29 Carcharhinus

albimarginatus

Silvertipshark 30 Carcharhinus

galapagensis

3 0.52% Vulnerable

Galapagosshark 31 Carcharhinus

plumbeus

3 0.52% Vulnerable

Sandbarshark

32 Squalusmontalbani 2 0.34% Vulnerable

Philippines spurdog

33 Squatinalegnota 2 0.34% Datadeficient

Indonesian angleshark

34 Carcharhinusleucas 1 0.17% Nearthreatened

Bullshark 35 Carcharhinus

amboinensis

Pigeyeshark 36 Carcharhinus

coatesi

Whitecreekshark

37 Heptranchiasperlo 1 0.17% Nearthreatened

Sharpnose sevengillshark 38 Pseudocarcharias

kamoharai

Crocodileshark 39 Atelomycterus

marmoratus

Coralcatshark 40 Carcharhinus

obscurus

1 0.17% Vulnerable

Duskyshark

Indonesia’smarineecosystemsareanextremelyvaluable nat-uralresource that contributes significantlytoits GDPand food needsofitspeople(Barberetal.,2014).Becauseoftheimportance of sharks in maintaininghealthy marine ecosystems,achieving thebiodiversitypreservationandfoodsecuritygoalsoftheCoral Triangle Initiative (www.coraltriangleinitiative.org)will require enforcementofexisting fisheriesregulationsand expandingthe management of shark fisheries to protect ecologically impor-tant, but highly threatened shark species. Recently, the West Papua Province enacted regulations prohibiting the capture of sharks,raysandcertainotherfishspeciesinRajaAmpatwaters (www.rajaampatkab.go.id/index.php).This initiative serves as a modelthat couldbeadoptedandenforced byotherdistrictsin Indonesia to prevent a further decline in Indonesia’s vulnera-ble sharkpopulation,furtherjeopardizingitsalreadyimperilled marineecosystems(Burkeetal.,2011).

5. Conclusion

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Acknowledgements

This study was funded by the Partnerships for Enhanced EngagementinResearch(PEER)ScienceProgramme (AID-OAA-A-11-00012)funded bytheUnitedStates AgencyforInternational Development(USAID)andtheNationalScienceFoundation(NSF) inpartnershipwithNSFPIREProgramme(OISE-0730256). Facil-itiesandtrainingforthisstudywereprovidedbyUCLAandthe SmithsonianInstitution under USAID (grant number 497-A-00-10-00008-00). We thank B. Subhan,A.A. Wibowo, I.A.Putra,S. Bahri,Rahmad, N.Akbar,P. Akna,WWF Indonesia,D.Suprapti, Agri,Masriana,ReefCheckIndonesia,P.Borsa,N.Putra,A. Yusma-linda,Ambariyanto,S.Indriawan,A.A.Tarekat,Stevanus,A.Arimbi, C.A.K.Hardani,Ma’rufah,A.Kusumafortheirassistancewith sam-pleand/ordatacollection.

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