Threatened Freshwater Fishes and the Aquarium Pet Markets

14 Pages·2014·1.09 MB·English

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Rajeev Raghavan
University of Kent, Canterbury, U.K
Neelesh Dahanukar
Zoo Outreach Organization, India
Michael F. Tlusty
New England Aquarium, John H Prescott Marine Laboratory, U.S.A
Andrew L. Rhyne
Roger Williams University, [email protected]
K. Krishna Kumar
St. Albert’s College, Kochi, India
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Raghaven, R., D. Dahanukar, M. Tlusty, A.L. Rhyne, et al. 2013. "Uncovering an Obscure Trade: Threatened
Freshwater Fishes and the Aquarium Pet Markets." Biological Conservation 164: 158-169.
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Rajeev Raghavan, Neelesh Dahanukar, Michael F. Tlusty, Andrew L. Rhyne, K. Krishna Kumar, Sanjay Molur,
and Alison M. Rosser
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BiologicalConservation164(2013)158–169
ContentslistsavailableatSciVerseScienceDirect
Biological Conservation
journal homepage: www.elsevier.com/locate/biocon
Uncovering an obscure trade: Threatened freshwater fishes and the
aquarium pet markets
Rajeev Raghavana,b,c,d,⇑, Neelesh Dahanukare,f, Michael F. Tlustyg, Andrew L. Rhyneg,h,
K. Krishna Kumarb,i, Sanjay Molure, Alison M. Rosserj
aDurrellInstituteofConservationandEcology(DICE),SchoolofAnthropologyandConservation,UniversityofKent,Canterbury,UnitedKingdom
bConservationResearchGroup(CRG),St.Albert’sCollege,Kochi,India
cResearchGroupZoology:BiodiversityandToxicology,CenterforEnvironmentalSciences(CMK),UniversityofHasselt,Diepenbeek,Belgium
dInstituteofAquaculture,FacultyofFisheriesandProtectionofWaters,UniversityofSouthBohemia,CeskeBudejovice,CzechRepublic
eZooOutreachOrganization(ZOO),96,KumudhamNagar,VilankurichiRoad,Coimbatore,India
fIndianInstituteofScienceEducationandResearch(IISER),Pune,India
gNewEnglandAquarium,JohnHPrescottMarineLaboratory,Boston,MA,UnitedStates
hDepartmentofBiologyandMarineBiology,RogerWilliamsUniversity,Bristol,RI,UnitedStates
iCommunityEnvironmentalResourceCenter(CERC),AshokaTrustforResearchinEcologyandEnvironment(ATREE),Alleppey,India
jSpeciesProgramme,UnitedNationsEnvironmentProgramme–WorldConservationMonitoringCenter(UNEP–WCMC),Cambridge,UnitedKingdom
a r t i c l e i n f o a b s t r a c t
Articlehistory: Whilethecollectionoffishfortheaquariumpettradehasbeenflaggedasamajorthreattowildpopu-
Received10September2012 lations,thislinkistenuousfortheunregulatedwildcollectionofendemicspeciesbecauseofthelackof
Receivedinrevisedform30January2013 quantitativedata.Inthispaper,weexaminetheextentandmagnitudeofcollectionandtradeofendemic
Accepted23April2013
andthreatenedfreshwaterfishesfromIndiaforthepetmarkets,anddiscusstheirconservationimplica-
Availableonline19June2013
tions.UsingdataonaquariumfishesexportedfromIndia,wetrytounderstandnatureofthetradein
termsofspeciescomposition,volume,exitpoints,andimportingcountries.MosttradeinIndiaiscarried
Keywords:
outunderagenericlabelof‘‘liveaquariumfish’’;yetdespitethisfact,weextractedexportdataforat
Aquariumtrade
leastthirtyendemicspeciesthatarelistedasthreatenedintheIUCNRedList.Ofthe1.5millionindivid-
Biodiversityhotspots
ualthreatenedfreshwaterfishexported,themajorsharewascontributedbythreespecies;Botiastriata
Conservation
Endemic (Endangered), Carinotetraodon travancoricus (Vulnerable) and the Red Lined Torpedo Barbs (a species
RedLinedTorpedoBarb complexprimarilyconsistingofPuntiusdenisoniiandPuntiuschalakkudiensis,both‘Endangered’).Using
theendangeredRedLinedTorpedoBarbsasacasestudy,wedemonstratehowexistinglocalregulations
onaquariumfishcollectionsandtradearepoorlyenforced,andareoflittleconservationvalue.Inspiteof
thefactthatseveralthreatenedandconservationconcernspeciesareroutinelyexported,Indiahasyetto
framenationallegislationonfreshwateraquariumtrade.Ouranalysisofthetradeinwildcaughtfresh-
waterfishesfromtwoglobalbiodiversityhotspotsprovidesafirstassessmentofthetradeinendangered
andthreatenedspecies.Wesuggestthattheunmanagedcollectionsoftheseendemicspeciescouldbea
much more severe threat to freshwater biodiversity than hitherto recognized, and present realistic
optionsformanagement.
(cid:2)2013ElsevierLtd.Allrightsreserved.
1.Introduction allbut10%arecaptivebred,andtheremaindercompriseofdiverse
wild-caughtspecies(Olivier,2001).
The aquarium fish trade is a large, biodiverse, global industry Collectionoffreshwaterfishesfortheaquariumtradeisalsoa
(Tlusty et al., 2013), worth around 15–30billion US$ (Penning practice that divides opinion (Watson and Moreau, 2006). While
etal.,2009)andinvolving(cid:2)5300freshwaterand1802marinefish some authors consider them an important contributor to local
(Hensen et al., 2010; Rhyne et al., 2012a). Ninety percent of the economiesthatcan provideincentivesfor environmentalconser-
tradevolumerevolvesaroundtropicalfreshwaterfishesofwhich vationif well managed (Tlusty et al., 2008; see also Rhyne et al.,
2012b for a marine example), others question its sustainability
vis-à-vistheunmanagednatureandpopulationdeclineofimpor-
⇑
Correspondingauthorat:DurrellInstituteofConservationandEcology(DICE),
tantspecies(FAO,2003;Gerstneretal.,2006;MoreauandCoomes,
SchoolofAnthropologyandConservation,UniversityofKent,Canterbury,United
2007;Rowleyetal.,2008).Forexample,inMalawi,SouthEastern
Kingdom.Tel.:[phone].
E-mailaddress:[email protected](R.Raghavan). Africa,collectionofaquariumfishhasbeenknowntosupportthe
0006-3207/$-seefrontmatter(cid:2)2013ElsevierLtd.Allrightsreserved.
http://dx.doi.org/10.1016/j.biocon.2013.04.019
R.Raghavanetal./BiologicalConservation164(2013)158–169 159
employmentofatleast1500people(SM.GrantcitedinHelfman, aquariumfishes.Ingeneral,freshwater fishis viewedas anopen
2007).Butontheotherhand,ithasbeendemonstratedthatprof- accessresource,andafreecommoditythatcanbecollectedfrom
itable aquarium trade cannot be sustained on the basis of wild nature(Raghavan,2010),resultingintheprecariousstateoffresh-
caught freshwater fish in Cameroon (Brummet et al., 2010), and waterbiodiversity(Allenetal.,2010;Moluretal.,2011).
that around 82 species of African freshwater fishes seen in the In this paper, we assess the levels of exports of threatened
aquariumtradearethreatened(UNEP-WCMC,2008).Moreauand freshwaterfishesfromIndiafortheaquariumtrade,whilespecifi-
Coomes (2007) while acknowledging that (cid:2)10,000 people in the callyfocusingontheendangeredRLTBs.Forthefirsttime,wepro-
IquitosregionofPeruearnedatleastsomeincomefromcollecting vide information on species, export quantities, trade routes,
aquariumfishes,alsocautionsthatthetradepresentsnewconser- airportsandimportingcountries.Wheredataallow,wealsoexam-
vation concerns. Similarly, Gerstner et al. (2006) estimated that inetheimpactsoftradeontheconservationoftheseendangered
3000familiesmadealivingfromthetradeandthat100,000people species.
benefitedeconomicallyinPeruvianvillages,wherefewothereco-
nomicopportunitieswereavailable.Yet,therewasnoevidenceto
support that wild caught aquarium trade was sustainable, and 2.Materialsandmethods
added thatanecdotalevidenceindicatedthatthenumberofspe-
ciesavailablewasdeclining. The official export records of aquatic animals in India, main-
InIndia,thecountrythatharboursthemostnumberofendemic tained by the Marine Products Exports Development Authority
freshwaterfishesincontinentalAsia(FroeseandPauly,2012),col- (MPEDA) under the Central Ministry of Commerce, contains only
lection of such species for the aquarium trade is entirely open- ageneralquantificationofaquariumfishexportsanddoesnotpro-
access,unregulatedandevenencouragedbycertaingovernmental vide details of common names, genera, or species (see MPEDA,
and semi-governmental agencies (Raghavan, 2010). Most wild 2010). Currently, there is also no legislation or official reporting
caughtaquariumfishoriginatingfromIndiacomefromtheEastern system in place that requires the declaration of ‘species’ or their
HimalayaandWesternGhats,hotspotsknownfortheirremarkable ‘numbers’priortoexport.Itisknownthatwhilesomeindividual
freshwater biodiversity and endemism (Allen et al., 2010; Molur exportersdoprovidedataonthedetailsofthecargo(speciesand
et al., 2011). Approximately 200 species of freshwater fish from numbers),otherssimplylistaquariumfishexportsunderthegen-
theEasternHimalayahavebeencollectedforthetrade,although eral label ‘live ornamental fish’ or ‘tropical freshwater fish’ (see
lessthanhalfareexportedregularly(Allenetal.,2010).Similarly, Smithetal.,2008).SomeairportsinIndia(e.g.,Bangalore/Bengal-
ofmorethan100speciesthathaveenteredthetradefromWestern uru/BLR) require the labelling of consignments at the genus/spe-
Ghats(Raghavan,2010),closetotwodozenareregularlyexported. cies level before exports, while others (e.g., Kochi/Cochin/COK)
Theremainingspeciesarenon-viableintradeastheyarerare,and donot.Exportersmayalsodeclarethenamesofspecies(andtheir
therefore extremely hard to collect and thus cannot meet a con- size ranges) during export due to such requirements from the
stantmarketdemand,orareextremelysensitivetohandlingand importersside.However,suchinformationisnotpassedontothe
transportation. MPEDAforaggregationinadatabase.
At the centre of attraction of India’s aquarium trade are the Our search for detailed information on aquarium fish exports
charismatic Red Lined Torpedo Barbs (RLTBs), a species complex from India led us to Tips Software Service Private Limited, a
ofcolourfulcyprinids,whoseunmanagedcollectionduringthelast company that maintains a database on export and import
twodecadesisassociatedwithseverepopulationdeclines,andan related information including foreign trade statistics (see
‘Endangered’listingintheIUCNRedListofThreatenedSpecies(Ali www.dailyexportimportdata.com). The company collects data on
etal.,2011;RaghavanandAli,2011).Theincreasingglobalatten- allcommoditiesexportedfromIndiaincludingliveanimals,from
tionontheneedforconservationofRLTBsledtheDepartmentof the customs records available at various airports and seaports.
FisheriesinthesouthernIndianstateofKeralatoissueaGovern- Using the database at Tips, we obtained customs-level data on
mentOrderin2008,restrictingcollectionandexports,andpropos- thedailyexportsofaquariumfishesfromtheinternationalairports
ing several management measures including quotas, gear inIndiafromApril2005untilMarch2012.
restrictions,minimumcatchsize,andaseasonaltradeban(Mittal, For the present study, we considered only freshwater fish. All
2009). However, recent studies indicate that these regulations speciesofmarineandbrackishwaterfishes,aswellasfreshwater
weredevelopedwithminimumscientificinputandofferlittlepro- shrimpswereexcluded.Datawereextractedintheformofama-
tectionforthespecies(Solomonetal.,2011).Forexample,asea- trix with information regarding date of export, descriptive label
sonal closure of the fishery was implemented based on the onthecargo(species/tradename,orgenerallabelsuchas‘liveor-
assumptionthattheRLTBsbreedinJune,JulyandOctober(Clarke namental fish’, ‘ornamental live fish’, ‘live aquarium fish’, ‘live
etal.,2009).However,researchonbiologyofthespeciesshowed aquarium ornamental fish’, ‘ornamental fish’, ‘assorted live orna-
that the actual breeding season extends from October to March, mental fish’), export and import airports, quantity, size ranges
and that the seasonal closure is therefore mistimed (Solomon (wherevermentionedbytheexporter)andunits(underfourcate-
et al., 2011). In general, efforts to manage collection and exports gories: ‘PCS’, pieces; ‘NOS’, numbers; ‘DOZ’, dozen; ‘KGS’, kilo-
offreshwateraquariumfishesinIndiahavebeenhinderedbythe grams). After consulting with the data provider, the units ‘PCS’
lackofempiricaldataaboutthetrade. and NOS were considered as same, which indicated the number
Thestatusoffreshwaterfishas‘wildlife’anditsconservationis of individuals in the cargo. Unit ‘DOZ’ was converted to ‘NOS’ by
alsosomewhatanomalousinIndia.Themainwildlifeconservation multiplyingthevalueby12.Sinceitwasnotpossibletodecipher
legislationsinIndiaaretheWildlifeProtectionAct(1972),which the number of individuals shipped as KGS, we omitted this data
lists protected species and prescribes regulations for hunting or fromtheanalysisofnumbersintrade.However,wedidaseparate
harvestingwildanimals;theBiologicalDiversityAct(2002),which analysisonthedatainKGSsoastodecipherthevolumeoftradein
implements aspects of the Convention on Biological Diversity KGS.Currencyexchangerates(IndianRupeetoUSDollar)during
(CBD)andtheIndianForestAct(1927),whichprovidesforhabitat the years covered by the study were obtained from http://
protectionanduseofforestproducts.Noneoftheselegislationsre- www.oanda.com/currency/historical-rates/.
lateexplicitlytotheconservationoffreshwaterfish.Severalstates Additionalinformationonthetradewasgatheredduringfield
have also passed ‘Inland Fisheries’ acts (Dahanukar et al., 2011), researchintheWesternGhats,inretailshopsinEuropeandSouth
but without any focus on conservation and sustainable use of East Asia, and extensive internet searches for aquarium fish
160 R.Raghavanetal./BiologicalConservation164(2013)158–169
retailers, importers and exporters at various intervals during 2005–2006 comprised of unnamed and unidentified species, this
2006–2012.Semi-structured interviews consistingofopen-ended reducedto13%during2011–2012(Fig.2).
questions(Newing,2010)aimedatobtaininginformationonspe- Atleast68generaand136speciescouldbeidentifiedaspresent
ciesharvested,theirnumbers,collectiontechniques,demand,sup- inthetradeduringthestudyperiod(AppendixB).Ofthese,names
ply and marketing channels were obtained from both collectors of only 60 genera and 112 species were encountered in the cus-
(n=7) and exporters (n=4). Five collectors and three exporters tomsrecords.Namesoftheadditionaleightgeneraand24species
operated from the Western Ghats region, while two collectors were obtained as a result of the interviews with collectors and
andoneexporterwereactiveintheEasternHimalaya/NorthEast exportersaftertheyrevealedtheiroccurrenceintrade(seeAppen-
Indian landscape. All respondents agreed to be interviewed and dix B). Of these 24 species, four were also recorded by the first
gave their consent for participating in the study. They were also author at pet stores in Germany and Singapore (Table 2) while
told that the information provided will be subsequently used for anadditionaleightwereknowntobeimportedtotheUSthrough
publication, and available in the public domain. The scientific itsavailabilityonawholesaler’swebsite(Table3).
nameoftheharvestedspecieswasalwaysvalidated,afterthecol- Inaddition,theidentityoffourspecies(Badisruber,Channahar-
lectors confirmed them (via their common names) through the courtbutleri,MacrognathusaculeatusandParambassiswolffii)which
photographs that we provided. An additional seven collectors wereencounteredinthecustomsdatabaseneedsfurtherclarifica-
andtwoexporters(forwhomthesecollectorsworked)refusedto tionastheyarenotknowntooccurinIndia.Theymayeitherbe
beinterviewed. misidentifications on the part of the exporter, or could represent
The first author visited retail shops in Malaysia (2006, 2012), individualsthatmayhavebeenimportedfromMyanmarandsub-
Singapore (2010), Thailand (2011), Hong Kong (2011), Germany sequentlyre-exportedfromIndia.
(2010, 2011), Belgium (2011, 2012), Netherlands (2009, 2011) Fishes were exported under both known species codes and
andtheUnitedKingdom(2009,2010,2011,2012)togetfirst-hand moregenericlabelssuchas‘liveornamentalfish’,‘ornamentallive
informationonthespeciesoriginatingfromWesternGhatsthatare fish’,‘liveaquariumornamentalfish’,‘ornamentalfish’or‘assorted
availableinthesemarkets.Alistofspeciesavailableintheseretail live ornamental fish’. Beginning January 2012, cargos are being
shopswassubsequentlycompiled,bycombiningthenamesofspe- increasingly labelled under a group name (mostly the generic
ciesencounteredintheseoutletsduringrandom(personal)visits, nameorcommonnamesuchas‘BarbGroup’;‘PuntiusGroup’;‘Cat-
and those obtained after discussions with the retailer as having fish Group’ and ‘Snakehead Group’) instead of the more general
beenimportedfromIndiaand/ororiginatingfromIndia.Websites codes such as ‘live aquarium fish’. The reason behind this is not
ofwholesalersandretailersinUS,EuropeandSouthEastAsiawere clear as there seems to be neither a legislative requirement, nor
alsoaccessedatrandomintervalsduring2006–2012,andinforma- anyincentivetodoso.
tiononthenamesoffreshwaterfishesthatwerebothendemicto
India,andmentionedasimportedfromIndiagathered. 3.1.Threatenedspeciesintrade
Dataondistributionandconservationstatusofspecieswerere-
trievedfromtheIUCNRedListofThreatenedSpecies(www.iucn- Morethan1.5millionfreshwaterfish(30%oftotal)belongingto
redlist.org), trade names from Hensen et al. (2010) and scientific 30threatenedspecieswereexportedfromIndiaduringtheyears
namesfromEschmeyer(2012)andPethiyagodaetal.(2012). 2005–2012(Table2).Ofthese,Botiastriata(Endangered),Carino-
tetraodontravancoricus(Vulnerable)andtheRLTBs,Puntiusdeniso-
3.Results niiandPuntiuschalakkudiensis(bothspecies‘Endangered’)formed
thebulkofexports(Table2).Rangerestrictedspeciesofconserva-
The reported aquarium fish trade exports from India were tionconcernsuchasGarrahughi(Endangered)andChannaauran-
worth in excess of 1.6million US$ for the 7year period from timaculata (Data Deficient; single location endemic) were also
2005to2012,andwereexportedfromsevenexitpointstoasmany exported.Fourofthe30threatenedspecies,includingtherecently
as 27 countries (Fig. 1; Appendix A). These exports comprised at described Dawkinsia rohani were encountered at retail shops in
leastfivemillionaquariumfishes(Fig.1);(n.b.4%ofconsignments GermanyandSingapore(AppendixB)bythefirstauthor,butwere
wereonly reported as KGs and numberscould not beestimated) notlistedinthecustomsrecordsandsoweremostlikelyexported
(see Table 1). While more than 97% of the exports during underagenericlabel.Thiswasalsothecasewithanadditionalfour
(threatened) species (Nemacheilus petrubanarescui, Horabagrus
nigricollaris, Travancoria elongata and Travancoria jonesi), which
werenotlistedinthecustomsrecords,butwererevealedbycol-
lectorsandexportersasbeinginthetrade.
Arecent(May2012)onlinesearchfor‘Indiannativeornamental
fishes’ helped retrieve information on the export of eight species
(sevenofthemthreatened)totheUSinApril2012(Table3),indi-
catingthatnewspeciesofconservationconcernarebeingcollected
and exportedtosatisfy hobbyistpreferencefor noveland/or rare
varieties.Oftheseeightspecies,Gonoproktopterusthomassi(Criti-
cally Endangered) has an extremely restricted distribution with
anareaofoccupancyof<10km2,whileGlyptothoraxhousei(Endan-
gered)hasanareaofoccupancyof<25km2andisrestrictedtoa
singlelocationintheWesternGhatsHotspot.
3.2.TradeinRLTBs
Over 300,000 RLTBs were exported from India during 2005–
2012tosevencountries(Figs.3and4).Theactualnumberoffish
thatwerecollectedwouldprobablyhavebeenseveraltimeshigher
Fig.1. QuantityandvalueofaquariumfishexportedfromIndiaduringtheyears
2005–2012. to compensate the high post-harvest mortality in these species
R.Raghavanetal./BiologicalConservation164(2013)158–169 161
Table1
DetailsofcargoswithaquariumfishesexportedfromIndiaduringtheyears2005–2012.
Year Totalnumberofcargos Numberofcargos(kg) Weightofcargo(kg)
April2005–March2006 473 6 308.04
April2006–March2007 290 0 0
April2007–March2008 809 33 4860.08
April2008–March2009 1218 0 0
April2009–March2010 1358 6 7372.00
April2010–March2011 1064 121 31068.00
April2011–March2012 783 82 31542.19
Total 5995 248 75150.31
Mumbai,ChennaiandKolkata(Fig.4).Ourexportquantificationis
inallprobabilityunder-estimatedasonlythosecargoslabelledas
either ‘P. denisonii’, ‘P. chalakkudiensis’ or the ‘Red Lined Torpedo
Barbs’wereincludedintheanalyses.SeveralthousandRLTBscould
havebeenexportedundergenericlabels(fore.g.liveornamental
fish) and/or group labels (Barb/Puntius Group), both in ‘PCS’ and
‘KGS’.OnehundredandfortyconsignmentsofRLTBsexporteddur-
ing the years 2005–2012 also had information on the size range
(1.70,2–2.5,3and4in.)oftheindividualfish.
Singapore (48.63%), Hong Kong (30.52%) and Malaysia (18.4%)
were the main markets to which RLTBs were exported during
2005–2012,withnegligiblequantitiesexportedtoGermany,Uni-
tedKingdomandJapan(Fig.4).
3.3.RLTBtraderegulations
Ourresultssuggestthatthelocalregulations(includingaban)
oncollectionsandexportsofRLTBsimplementedinthesouthern
Indian state of Kerala, has been poorly enforced. Although there
seemedtohavebeenanimmediateimpact(during2009),asindi-
Fig. 2. Quantity of named and unnamed species of freshwater aquarium fish catedbyanabsenceofRLTBinthecustomsdatabaseinthemonths
exportedfromIndiaduringtheyears2005–2012.
of the trade ban, these regulations lacked continuity, as at least
11,260RLTBswereexportedduringthemonthsofthebaninthe
(Ramachandranetal.,2004).Bangaloreairportwasthehubforthe subsequent years. This was around 22% of all RLTBs exported
RLTBtradecontributingto96%ofthereportedexportsfollowedby during2010–2012(Fig.5).Collectors(n=5)andexporters(n=3)
Table2
ListofthreatenedandconservationconcernendemicfreshwaterfishspeciesexportedfromIndiaduringtheyears2005–2012.
Species Tradename Endemism IUCNstatus Quantity(nos)
Bariliuscanarensis WG EN 370
Botiarostrata EH VU 665
Botiastriata StripedLoach WG ENa 382,575
Carinotetraodontravancoricus WG VU 946,050
Channaaurantimaculata Orange-spottedSnakehead EH DDb 225
Daniojaintianensis EH VU 80
Dawkinsiaarulius LongfinBarb WG EN Unknowne
Dawkinsiarohani WG VU Unknowne
Devarioassamensis BloodstripeDevario EH VU Unknowne
Etropluscanarensis BandedChromide WG ENc 172
Garrahughi CardamomGarra WG ENd 2245
Gonoproktopteruscurmuca WG EN 60
Horabagrusbrachysoma WG VU 150
Pethiamanipurensis RedJasperBarb EH EN Unknowne
Pethiashalynius EH VU 120
Pillaiaindica EH EN 150
Puntiusdenisonii RedlinedTorpedoBarb WG EN 310,791
Puntiuschalakkudiensis DenisoniiBarb WG EN
Schismatorhynchosnukta WG EN 100
Torkhudree SA EN 10
WG–WesternGhats;EH–EasternHimalaya;SA–SouthAsia.
EN–Endangered;VU–Vulnerable;DD–DataDeficient.
a Knownonlyfromfourfragmentedlocations(Dahanukar,2011a).
b Knownonlyfromasinglelocation(Chaudhry,2010).
c Knownonlyfromtwolocations(Ali,2011b).
d Knownonlyfromfivelocations(Ali,2011a).
e SpeciesexportedwithoutspeciesspecificlabelandencounteredatretailshopsinEuropeandSingapore.
162 R.Raghavanetal./BiologicalConservation164(2013)158–169
Table3
ListofthreatenedandconservationconcernendemicfreshwaterfishspeciesexportedfromIndiaduringApril2012.a
Species Tradename Endemism IUCNstatus
Batasiotravancoria YellowCatfish WG VUb
Dawkinsiatambraparniei GlimmerBarb WG ENc
Gonoproktopterusthomassi RedTailedBarb WG CRd
Glyptothoraxhousei KalkkariCatfish WG ENe
Laubucafasciata FascinatingHatchetFish WG VUf
Pseudosphromenusdayi SpikeTailParadiseFish WG VUg
Torputitora GoldenMahseer SA ENh
Mesonoemacheilusremadevii NewMalabarLoach WG LCi
a BasedonimportsintotheUS.
b Severelyfragmentedpopulations;areaofoccupancyof1000km2andthreatenedbyhabitatloss.
c Restrictedinoccurrenceto<fivelocationswhicharefragmented.
d Extremelyrestricteddistributionwithanareaofoccupancyof(cid:2)10km2.
e Areaofoccupancyof<25km2andrestrictedtoasinglelocation.
f Areaofoccupancy<30km2.
g Occursin<10locations.
h Pastpopulationdeclinecalculatedat50%.
i Restricteddistribution;knownonlyfromahighlyprotectedNationalParkintheWesternGhatsAbbreviationsofendemismanddistributionasperTable2.
4.Discussion
Effective monitoring and regulation of the aquarium industry
is constrained by lack of accurate, quantitative and un-biased
information (Green, 2003; Smith et al., 2008; Murray et al.,
2012; Rhyne et al., 2012a). Trade figures for aquarium fishes are
often non-existent, or if available are frequently mis-reported
due to the exclusion or misclassification of shipment records
(Olivier,2001)orthroughinappropriateestimatesbytheexport-
ing and importing companies (Rhyne et al., 2012a). The practice
ofshipmentreportingbyweightorvaluemeansthatthenumber
of individuals in trade is difficult to quantify (Wood, 2001). In
addition, the lack of species-specific recording represents an
impediment to assessing the origin and number of individuals
of wild-caught species (Schlaepfer et al., 2005; Smith et al.,
2008; Rhyne et al., 2012a).
Althoughtherewerenocustomsrecordsshowingtheexportsof
Fig.3. QuantityofexportsoftheendangeredRedlineTorpedoBarbs(RLTBs)from 24species,manyspecimensoffourthreatenedcyprinidsDawkinsia
Indiaduringtheyears2005–2012.
arulius,D.rohani,DevarioassamensisandPethiamanipurensis,con-
firmed to have come from India, were encountered in wholesale
disclosedthat,ayearafterthebanwasimplemented;theyaltered andretailshopsinGermanyandSingaporein2010and2011.This
trade routes by transporting RLTBs out of the state of Kerala by is a clear indication that several threatened species are exported
road to the Bangalore airport (in neighbouring Karnataka state), after‘mislabelling’orlabellingunderthegeneral‘liveornamental
wherethebandidnotexist.Demonstratingthisshiftonthebasis fish’code.
ofquantitativedataisimpossibleduetothepoorrecordkeepingat
theairportinKerala(COK/KochiInternationalAirport).
Morethan15,000KGSofaquariumfishwereexportedduring 4.1.Tradeinthreatenedspecies
2005–2012 from Kochi airport without any species codes.
AlthoughKochiisknowntobeamajorhubfortheexportsofRLTBs Aquarium trade is known to be a current, or potential future
(Raghavanetal.,2007,2009),therewasnotasinglelabelledcon- threattoatleast22endemicfreshwaterfishesofIndia,ofwhich
signment of these fishes exported from the airport during 2005– 12 are already threatened (Appendix C). Several threatened spe-
2012. cies that are regularly exported from India have very restricted
Duringthe7yearperiodfrom2005to2012,morethan89,000 areasofoccupancy(AOO).Forexample,B.striata,whichoccupies
RLTBs were collected and exported during their breeding season fragmented locations within a limited AOO of 400sq. km
extending from October to March, which comprised 11–44% of (Dahanukar, 2011a), was one of the main species exported dur-
theannualexportsduringtheseyears(Fig.5).AsthetradeinRLTBs ing 2005–2012. During this period, over 380,000 individuals
isdemandorientedwithcollectionstakingplaceonlyafteranor- where shipped from India. Similarly more than 2000 individuals
derisreceived,andtakingintoaccountthatthemaximumholding of G. hughi, a rare and endangered stone sucker having an AOO
time of specimens post-collection and pre-export is 10–15days, of <300sq. km (Ali, 2011a), were also exported during this
thereisverylittledoubtthatthefishwereactuallycollecteddur- period.
ingtheirbreedingmonths.Basedontheavailableinformationon Apartfromthreatsrelatedtocollectionfortheaquariumtrade,
thesizeatfirstmaturityforRLTBs(<4in.)(Solomonetal.,2011), allofthe30threatenedspeciesthatwereexportedareaffectedby
it could be inferred that 46% (n=145,997) of the exports during avarietyofadditionalstressorsincludinglargescalemodifications
thelast7yearscomprisedofspecimensthatareyettoreachfirst totheirhabitats,i.e.sandmining,constructionofdamsandpollu-
maturity. tion from pesticides (Allen et al., 2010; Dahanukar, 2011). Seven
R.Raghavanetal./BiologicalConservation164(2013)158–169 163
Fig.4. ImportingcountriesandexitpointsfromIndiaforRedlineTorpedoBarbs(RLTBs)duringtheyears2005–2012.Thepiechartgivestheproportionofconsignments
exportedfromdifferentportsinIndiaandthedoughnutchartgivestheproportionofconsignmentssenttodifferentcountries.Mauritiusisnotshowasalltheconsignments
wereinKGS.
by both commercial and artisanal fishers in their native range;
juvenilesbeingcollectedforthepettrade.Suchspeciesareoften
subjectedtoindiscriminatefishingincludingtheuseofunscientific
practices such as dynamiting (Kharat et al., 2003; Dahanukar,
2011; Raghavan et al., 2011; Prasad et al., 2012). Nine of the 20
threatenedspeciesthatwereexportedduring2005–2012showa
continuing decline in their populations (see species specific ac-
countsintheIUCNRedListofThreatenedSpecies).
In spite of such threats, India does not possess a legal instru-
mentthatprotectsfreshwaterfishesperse.TheWildlifeProtection
ActofIndia(WPA)1972(withamendmentsin2002,2006,2009),
thefocallegislationforprotectionofthreatenedfloraandfaunain
thecountry,doesnothaveasinglefreshwaterfishspecieslistedin
itsappendices(Raghavan,2010;Dahanukar,2011).TerrestrialPro-
tectedAreas(PAs)mayoffersomeprotectionascommercialaquar-
ium fish collections and food fisheries are not permitted inside
thesePAs(exceptingsomereservoirs)videtheWPA.Butsuchreg-
ulationsarenotalwaysstrictlyenforcedasevidencedbypersonal
Fig.5. ExportsofRedLinedTorpedoBarbs(RLTBs)duringtheiractualspawning
season(JanuarytoMarch)andthemistimedseasonalclosure/tradeban(Juneto interviewswithcollectors(n=5)whorevealedthatRLTBsarecol-
October)duringtheyears2005–2012⁄.Thisfigureshowsthepercentageofexports lectedfromdrainagesinsideatleasttwoPAs.Similarly,aspopula-
thattookplaceduringthemonthsoftheexistingtradebanfrom2009to2012. tionsoftheendangeredG.hughiaremostlyfoundinsidePAsofthe
Western Ghats (Ali, 2011a), there is a high possibility that the
(cid:2)2000 G. hughi specimens exported were collected from one of
species(C.aurantimaculata,Gonoproktopteruscurmuca,G.thomassi, thefivePAsinwhichtheyoccur.Thelaxityofenforcementisfur-
Horabagrus brachysoma, H. nigricollaris, Schismatorhynchos nukta therevidentashundredsofspecimensoftherarebalitoridloach,
and Tor khudree) are also important food fishes that are targeted Mesonoemacheilus remadevii, known only from a single location
164 R.Raghavanetal./BiologicalConservation164(2013)158–169
inside the highly protected Silent Valley National Park (Ali and functioning social–ecological system (Tlusty, 2002; Tlusty et al.,
Raghavan, 2011) were exported to the US during April 2012 2013; Rhyne et al., 2012b).
(Table3).
4.4.ImplicationsoftradeonconservationofRLTBs
4.2.CollectionandexportofRLTBs
Due to its high post harvest mortality (Ramachandran et al.,
Sinceenteringtheaquariumtrade,RLTBshavebeenthemain- 2004), an extremely low fecundity and skewed sex ratio in the
stay of India’s aquarium fish exports. Fetching a retail price be- wild,RLTBshavebeensuggestedtobeunsuitableforwildcollec-
tween $5 and $20/piece (or even higher), these immensely tion(Solomonetal.,2011).Yet,thetradeshowsnosignsofslowing
popularbarbswerethefocusofanintensive‘boomandbust’fish- down as several thousands of RLTBs were exported in the first
erywithcatastrophicimpactsonseverallocalpopulations(Ragha- 3monthsof2012.
vanetal.,2007,2009).Catchesfromseveraltraditionalcollection The suite of management plans initiated by the State
centers increased during the years 2003–2007 (Ali et al., 2011). GovernmentofKeralatoprotectthewildstocksofRLTBshasbeen
Sincethen,studiesbasedonabundance,catchperuniteffort,local largelyflawed,andpoorlyenforced.Firstly,thespawningseasons
knowledge and genetics have all concluded that the RLTBs have ofthesefishesweremiscalculatedandtheseasonalclosuresmist-
beenseverelyoverfishedandbecomerareattraditionalcollection imed(Solomonetal.,2011).Secondly,thecatchsizerecommended
sites(KurupandRadhakrishnan,2006;Lakraetal.,2007;Raghavan by the government encouraged the collection of large spawning
etal.,2009). individualsinsteadofjuveniles.Andfinallybyrestrictingthetrade
Duetotheincomeitprovides,variousgovernmentagenciesin regulationtooneofthetwostatesfromwherethefishiscollected
Indiacontinuetoencouragetradeinnativeaquariumfishesinclud- and exported, the authorities allowed exporters to change trade
ingtheRLTBs.Thisiseitherthroughtheprovisionofsubsidiesand routesandadaptthroughthestatewithlessrestrictiverules.
developmentalassistanceforexporters,orbyundertakingexports Frommid2006untillate2008(beforethebancameintoeffect),
themselves.Closeto150,000RLTBswereknowntobeexportedby higherquantitiesof‘RLTBs’wereexportedcomparedtothoseun-
theKeralaAquaticVenturesInternationalLimited(KAVIL),ajoint derthegenerallabelof‘liveornamentalfishes’(i.e.,un-namedspe-
undertaking with private industry and the Government of Kerala cies).However,sincelate2008/early2009,thenumbersof‘RLTBs’
(Babu,2011).Interestingly,theseconsignmentswerenotrecorded decreasedwhilethatof‘liveornamentalfishes’increasedconsider-
tothespecieslevelinthecustomsrecords,andcouldhavebeenex- ably(Fig.6)andequivalently.Wespeculatethatoneofthemain
ported under the general label of ‘live ornamental fishes’. Our reasonsforthisshiftisbecauseexportersbegantostoplabelling
quantification of RLTB exports (Fig. 3) should therefore need to RLTBs and instead used a general ‘live ornamental fish’ label for
be considered as conservative estimates by at least 150,000 exporting these endangered barbs. The export consignment of
individuals. RLTBs from KAVIL (discussed above) was a probable example of
suchpurposefulmaskingandmislabelling.
4.3.ExportmarketsforRLTBs
4.5.Challengesandoptionsformanagement
Lowerfreightcharges,shortdurationoftransportandfrequent
connectivityarethefactorsthatdeterminetheexportmarketsfor One of the prime requisite for responsible aquarium fisheries
Indianaquarium fishes(Sekharan and Ramachandran, 2006). The andtradeismonitoringandrecordkeeping(Rhyneetal.,2012a).
South East Asian markets of Singapore, Hong Kong and Malaysia Increasinggovernment’scapacitytomonitorcollectionsandtrade
together imported (cid:2)98% of all RLTBs exported from India. Singa- has been long recommended as one of the critical needs for the
pore is known to be a hub for the global trade in aquarium pets industry (Moreau and Coomes, 2006), but continues to be ne-
(Collins et al., 2012) where fish imported from various parts of glectedworldwide.
South and South East Asia are then re-packed and exported to InthecaseofIndia,fisheswerescreenedfortheirpotentialin
the US and the European Union. Smith et al. (2008) reports that the aquarium industry on the basis of features that made them
45% of all freshwater fishes imported in the US came from these
threecountries.
Conservation benefits of wild capture and captive rearing in
the aquarium trade have been the focus of several discussions
(see Tlusty, 2002; Rosser, 2003). Concerns have been raised on
thelongtermeffectsofunregulatedtradeinendemicfreshwater
fishes including RLTBs on the loss of genetic property rights
(Raghavan et al., 2007; Raghavan, 2010). Although there is some
information about the development and commercialization of
captive breeding operations for RLTBs in South East Asia (Mittal,
2009), this has not fully eased pressure on wild stocks, as cap-
ture of wild RLTBs continue till date. Nevertheless, whether the
apparent decline in export figures of wild caught RLTBs over
the years is a result of the increased production in South East
Asia, need to be examined in more detail. Furthermore, the
importance of wild RLTBs needs to be assessed in supporting
the entire Indian aquarium fishery. Ornamental fisheries are of-
ten comprised of a few key endemic species, with more com-
monly, widely available species being filler for the orders
(Rhyne et al., 2012a). However, often, these fisheries can help
provide protection to extant ecosystems (Tlusty et al., 2008),
andthuseachspecieswithinafishery,aswellastheentirefish-
Fig. 6. Comparative account of the quantity of RLTB and un-named species
eryneedstobeevaluatedforitsoverallroleinsupportingafully exportedfromIndiaduringtheyears2005–2012.
R.Raghavanetal./BiologicalConservation164(2013)158–169 165
desirableforthetrade,butnotapparentlyonthebasisofbiological localcommunitiesinruralandoftenremotelocations(seeUNEP-
features that would make them robust to trade. Deciding which WCMC, 2008; Rhyne et al., 2012b). However, there is a pressing
speciesshouldfeatureinthetradeandthemannerinwhichthey need to understand, and find solutions for the many challenging
aretobesourced(wildcaughtorcaptivebred)(Tlusty,2002;Tlu- issuesdiscussedabove.
styetal.,2013)shouldbethefirststepforasustainableaquarium Tofullyunderstandthetradeofanywildcaughtspecies,alarge
industry in India. Even a very recent list of potential freshwater amount of information is needed. The health of the populations
species for certification and geographical indication prepared by (e.g. stockassessments), the numberoffish beingharvested,and
theMPEDA(Silasetal.,2011)containsseveralthreatenedspecies thelinkbetweenthesetwoareprimarycomponentsfor deriving
witharestrictedrange,includingthosefoundonlyinsideprotected any management plan focused on sustainability. Collection and
areas.Westronglyrecommendthatanycurrentandfuturelistof trade of wild-caught freshwater fishes is one of the least under-
potentialaquariumfishesfortradeshouldavoidincludingspecies stoodfacetsoftheaquariumindustry,aslittlequantitativedataex-
thatarethreatenedwithextinction,andadditionallycallforalist- ist on the number and composition of species involved (Moreau
ingofthethreatenedspeciesthatarecurrentlyinthetradeunder andCoomes,2006,2007;Collinsetal.,2012),orstockassessments
thenationallegislation(theWPA).Inaddition,specieslevelinfor- ofthewildpopulations.Thereisalsonoinformationonthetotal
mationneedstobecollecteduponexportatalltheairportsinthe valueofthewild-caughtfreshwateraquariumfishtrade.Thedata
countrytoreducethepotentialforendangeredspeciestobecate- presentedwithinfocusisonthelatteraspectofthisequation,that
gorizedandlabelledunderageneralexportcode.Currently,thisis being how many fish are collected and exported. This is a choke
beingfollowedattheBangaloreAirport. pointinthetradechainwheredatacanbeaggregated.However,
Anorganizedcodingsystem(seeGersonetal.,2008),forfresh- to fully understand this trade, it will be likely as important to
wateraquariumfish,especiallywildcaughtspecieswhichshould understand the size and replenishment capabilities of the wild
include all information including species name, capture location, populations.
size of the specimens, and the names of collector and exporter Inspiteofthesedata-deficienciesmentionedabove,ithasbeen
shouldalsobedevelopedandadoptedatallexitpoints.However, speculated that total number of wild-caught freshwater fishes in
merecollectionofthesedataarenotsufficienttoassurethehar- the trade might probably far exceed wild-caught marine fishes
vest of ornamental fish are conducted in a manner that does not (Gerstneretal., 2006). Forexample,40%of freshwaterfishesim-
leadtofurtherdeclinesinwildspeciesabundance.Itiscriticalto portedintheUSweresourcedfromwildpopulations,withthese
assess the trade data for veracity, and also to annually report on numbers considered an underestimate (Smith et al., 2008). It is
the number and diversity of species being traded (Rhyne et al., knownthat 9–36millionfishes are collected and exported annu-
2012a). Only through the collection and appropriate analysis of ally from the Amazon (Anjos et al., 2009; Gerstner et al., 2006;
tradedata,willitbepossibletomakeanyassurancethatappropri- MoreauandCoomes,2007).Atonepointintime,over30million
ate measures are being sufficiently implemented to deliver wild individuals of a single species, the cardinal tetra, Paracheirodon
sourcedfishforthehomeaquariumhobbythathavefullsocietal axelrodiwasexportedfromtheRio-NegrofloodplainsoftheAma-
andecologicalbenefits(Tlustyetal.,2013). zon(Chaoetal.,2001).Similarly,KottelatandWhitten(1996)esti-
Fishers’complianceandsupportarealsoessentialtoanycon- matedthataround10,000,000individualsoftheclownloach,Botia
servationactionforexploitedspecies(Vincentetal.,2011).Regu- macracanthuswereexportedfromIndonesia.Thiscomparestothe
lation of collections and exports of aquarium fishes although 11million marine fish the United States imports in a single year
existent in many countries including India are deeply resented representingapproximately60%oftheentiremarinetrade(Rhyne
(Moreau and Coomes, 2006, 2007; Mittal, 2009), mainly because etal.,2012a).Around291speciesofAfricanfreshwaterfishesare
they follow a top-down approach of management with little or alsoknowntooccurintheaquariumtrade(UNEP-WCMC,2008),
nostakeholderparticipation(DAFF,2005;Raghavan,2010).InIn- butwithoutanyquantification.
dia,themultipleownershipofkeyaquatichabitatsandtheirjuris- However,for such intensecollectionpressure, geneticinvesti-
dictional complexities, presents yet another challenge (Raghavan gations on the highlycollected cardinal tetra indicate highlevels
et al., 2011). Aquatic habitats inside forest areas are controlled ofvariabilitysuggestingverylargesourcepopulations(Beherega-
bytheForestandWildlifeDepartment,while‘fishes’and‘fisheries’ ray et al., 2004; Cooke and Beheregaray, 2007; Cooke et al.,
per se are subjects of the Fisheries Department. As most of the 2009). While a significant number of animals are collected from
aquarium species are forest-based fish, monitoring and enforce- the wild, initial indications are that these r-selected species are
mentcanonlybesuccessfulifmultiplecustodiansworkinunison, resilient to this pressure. Yet moving forward, it will be very
which has seldom been the case. An increased collaboration be- important to assess the status of wild stocks to assure the level
tween authorities and stakeholder participation is therefore vital oftakeindicatedbytheexportdatapresentedheredoesnotlead
(Phelps et al., 2010). Furthermore, the management of fisheries topopulationdeclines.
has historically tended to be separated from the management of The information here complements a number of prior studies
terrestrialresources.Whilstwildlifeandforestdepartmentshave thatassessthetradeoflivefishfortheaquariumandthelackof
increasinglyseenashiftinemphasisoftheirresponsibilitiesfrom appropriate tracking and statistics for the hobby (Smith et al.,
productiontoconservation,theprimaryfocusoffisheriesdepart- 2008; Rhyne et al., 2012a,b). Overall, we believe that our study
ments is still economic production albeit in terms of sustainable contributes to this body of work, by documenting the exports of
fisheries. endangered and threatened freshwater fishes for the pet trade
fromtwoglobalbiodiversityhotspots.Thiswillhelpcreateaware-
ness and a foundation for effective monitoring, regulation and
5.Conclusions managementofaquariumfisheriesandtradeworldwide,andlead
tothedevelopmentofablueprintforaself-sustainedandrespon-
Although many international aquarium trade organizations siblewild-caughtaquariumindustry.
advocateenvironmentallyresponsiblepractices,andconsidercol-
lectingendangeredspeciesasbadfortheindustry(Hensenetal., Acknowledgements
2010),theyhavenotbeenwidelyacknowledged.Awell-managed
andresponsibleaquariumfisherycancreatelivelihoodopportuni- TheauthorsthankDiogoVeríssimo,ArunKanagavel,Benjamin
ties and a sense of environmental stewardship for thousands of Lee, and Siby Philip for comments and suggestions on the draft