MANUALF O R T H ED I F F E R E N T I A T I O N O FC A P T I V E - P R O D U C E D A N DW I L D - C A U G H T T U R T L E SA N D T O R T O I S E S( T E S T U D I N E S )

P R E P A R E D B Y S P E C I E S 3 6 0 U N D E R C O N T R A C T F O R T H E C I T E S S E C R E T A R I A T

Image: Peter Paul van Dijk

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Image: Henrik Bringsøe Image: Andrei Daniel Mihalca Image: Beate Pfau

Manual for the differentiation of

captive-produced and wild-caught turtles and

tortoises (Testudines) ThisdocumentwaspreparedbySpecies360undercontractfortheCITESSecretariat.Principal Investigators: Prof.DaliaA.Conde,Ph.D.andJohannaStaerk,Ph.D.,Species360ConservationScienceAlliance,https://www.species360.orgAuthors: Johanna Staerk1,2, A. Rita da Silva1,2, Lionel Jouvet 1,2, Peter Paul van Dijk3,4,5, Beate Pfau5, IoannaAlexiadou1,2andDaliaA.Conde1,2

Affi l iations: 1Species360ConservationScienceAlliance,www.species360.org,2CenteronPopulationDynamics (CPop),DepartmentofBiology, University of Southern Denmark, Denmark, 3 The Turtle Conservancy, www.turtleconservancy.org, 4 GlobalWildlifeConservation,globalwildlife.org, 5 IUCNSSCTortoise&FreshwaterTurtleSpecialistGroup,www.iucn-tftsg.org. 6

DeutscheGesellschaftfürHerpetologieundTerrarienkunde(DGHT)

Images (t it le page): Firstrow,left: Mixedspeciesshipment(imagetakenbyPeterPaulvanDijk)Firstrow,right: WildTestudomarginatafromGreecewithdamageoftheplastron(imagetakenbyHenrikBringsøe)Secondrow,left: WildTestudomarginatafromGreecewithminordamageofthecarapace(imagetakenbyHenrikBringsøe)Secondrow,middle: Ticksontortoiseshell(Amblyommasp.inGeochelonepardalis)(imagetakenbyAndreiDanielMihalca)Secondrow,right: Testudograecawithdogbitemarks(imagetakenbyBeatePfau)

Acknowledgements: The development of this manual would not have been possible without the help, support andguidanceofmanypeople.WethankallthemembersofSpecies360forsupportingthedevelopmentof the Zoological InformationManagement System (ZIMS), and for their dedication on the recordkeepingofall theanimalsundertheircare.Wefurther thanktheSpecies360ConservationScienceAlliance for their support.Weareespeciallygrateful for thesupportofMarkusMonzelandRonnyBakowskie (DeutscheGesellschaft für Herpetologie und Terrarienkunde, DGHT), Chris R. Shepherd(Monitor Conservation Research Society), Kanitha Krishnasamy (TRAFFIC Southeast Asia) and JohnWerth(Pan-AfricanAssociationofZoosandAquaria;NelsonMandelaUniversity;TheSouthAfricanInstitute of Electrical Engineers). The information on parasites is strongly based on informationprovidedbyProf.DavidModrý(FacultyofVeterinaryMedicine,Dept.ofPathologyandParasitology,UniversityofVeterinaryandPharmaceuticalSciencesBrno)andProf.AndreiD.Mihalca(Departmentof Parasitology and Parasitic Diseases, Faculty of Veterinary Medicine, University of AgriculturalSciences and Veterinary Medicine Cluj-Napoca) to whom we are truly grateful for sharing theirknowledge.Wefurtherthankourcolleagues:GeraldBenyr(AustrianCITESScientificSupportAgencyfor Animals), Henrik Bringsøe (Køge, Denmark), Victor Loehr, Joe Flanagan (Houston Zoo), ThaisMorcatty (Oxford Wildlife Trade Research Group), Mike Pingleton, Mona van Schingen (FederalAgency for Nature Conservation, CITES Scientific Authority), Daniel Natusch, and Peter Praschag(Turtle Island,ConservationCenter for EndangeredTurtle andTortoises) forproviding their expertknowledge.WefurtherthanktheCITESSecretariatfortheircommentsandsupport.

Table of contents

Introduction ................................................................................................................. 1 Glossary ....................................................................................................................... 2 How to use this manual ............................................................................................... 3 Part 1: Inspection key ................................................................................................. 4 Part 2: Criteria to determine wild-caugth vs. captive-produced origin ..................... 5 Part 3: Illustrated guide .............................................................................................. 6 Part 4: Advanced methods to determine wild-caugth vs. captive-produced origin 10 References ................................................................................................................. 13

Tables

Table 1 – Criteria to determine wild-caught vs. captive-produced origin ................. 5 Table 2 – Recommended resources for a review of the species most relevant facts ................................................................................................................................... 11 Table 3 – Summary of advanced methods to determine wild-caught vs. captive-produced origin ........................................................................................................ 12

Appendices

Appendix A: Supplemental information on advanced methods for the differentiation of captive vs. wild origin

Appendix B: The Turtles and tortoises demographic traits database for CITES-listed species

Introduction Annually,about865,000specimensoflivetortoisesandfreshwaterturtles(Testudines)listedintheAppendicesoftheConventiononInternationalTradeinEndangeredSpeciesofWildFaunaandFlora(CITES)are legally traded.Thevastmajorityof thoseoriginate fromcaptive-breedingand ranchingfacilities (CITES, CoP17 Doc. 73). CITES requires documentation of the source of a specimen andappliesstrictconditionsthathavetobemetwhenaspecimenisdeclaredasproducedincaptivity.The high number of transactions of specimens claimed to be produced in captivity, however, hasraisedconcernsaboutthepotentialmisuseofsourcecodes.Claimsofcommercialcaptive-breeding(sourcecodeC) isespeciallyquestionableformanyturtlesandtortoisesas itrequiresconsiderableamounts of money and expertise and many turtles and tortoises grow slowly and mature late,making commercial captive-breeding unprofitable (Nijman & Shepherd, 2009; TRAFFIC, 2013).Customofficersandinspectionofficialsarechallengedtoidentifymisuseofsourcecodes,giventhehighnumbersofexportsand imports.Theaimof thismanual is therefore toprovideguidance forinspectionofficialsandcustomsofficersandCITESManagementandScientificAuthorities toaid intheidentificationofpotentialmisuseofsourcecodes.

ThismanualaimstoimplementCITESDecision17.291aii:

Developingguidanceconcerningthedifferentiationofspecimensoftortoisesandfreshwaterturtles (Testudines) originating from the wild, from those from captive and ranchingproductionsystems.

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Glossary

I. CITESSourceCodes

CITES-listedspeciesintheinternationaltraderequirepermitsissuedbytheCITESManagementauthority.CITESpermitsmustcontainasourcecodethatindicatesthesourceofthespecimenbeingtraded.Sourcecodeshavestrictdefinitionsthatmustbemet.

SourcecodeC:Captive-bredAppliestospecimensbredincaptivityofAppendixI,IIorIIIlistedspecies,whetherornottheywerebredforcommercialpurposes;

Ø RefersonlytospecimensbornorotherwiseproducedinacontrolledenvironmentØ Parentsmatedinacontrolledenvironmentorwereinacontrolledenvironmentwhenthedevelopmentoftheoffspring

beganGovernmentauthoritiesoftheexportingcountriesmustbesatisfiedthatthebreedingstock

Ø wasestablishedinaccordancewiththeprovisionsofCITESandrelevantnationallawsandinamannernotdetrimentaltothesurvivalofthespeciesinthewild

Ø ismaintainedwithouttheintroductionofspecimensfromthewild,exceptfortheoccasionaladditionofanimals,eggsorgametes,inaccordancewiththeprovisionsofCITESandrelevantnationallawsandinamannernotdetrimentaltothesurvivalofthespeciesinthewildasadvisedbytheScientificAuthority

Ø hasproducedoffspringofsecondgeneration(F2)orsubsequentgeneration(F3,F4,etc.)inacontrolledenvironment;orismanagedinamannerthathasbeendemonstratedtobecapableofreliablyproducingsecond-generationoffspringinacontrolledenvironment;and

Further,regardingthetradeinspecimensofAppendix-IspeciesbredincaptivityCITESrecommendsthatthetradeinaspecimenbredincaptivitybepermittedonlyifitismarkedinaccordancewiththeprovisionsonmarkingintheResolutionsadoptedbytheConferenceofthePartiesandifthetypeandnumberofthemarkareindicatedonthedocumentauthorizingthetrade.Fulltext:ResolutionConf. 10.16 (Rev.) https://cites.org/eng/res/10/10-16C15.php

SourcecodeF:FarmedAnimalsbornincaptivity(F1orsubsequentgenerations)thatdonotfulfillthedefinitionof“bredincaptivity”inResolutionConf.10.16(Rev,),aswellaspartsandderivativesthereof).AdaptedfromConf.12.3(Rev.CoP17)Permitsandcertificates

SourcecodeR,ranched:Rearinginacontrolledenvironmentofanimalstakenaseggsorjuvenilesfromthewild,wheretheywouldotherwisehavehadaverylowprobabilityofsurvivingtoadulthood.AdaptedfromConf.12.3(Rev.CoP17)Permitsandcertificates

AnadditionalCITESsourcecodeDisdefinedbelow,whichisonlyapplicabletoAppendixIspecies.

SourcecodeD,captive-bredAppendixIspecies:AppendixIanimalsbredincaptivityforcommercialpurposesandAppendixIplantsartificiallypropagatedforcommercialpurposesaswellaspartsandderivativesthereof,exportedundertheprovisionsofArticleVII,paragraph4oftheConvention.AdaptedfromConf.12.3(Rev.CoP17)PermitsandcertificatesPleasenote:Atpresent,onlyonespeciesoftortoiseorfreshwaterturtlecanbetradedundersourcecode‘D’:Astrochelysradiata,forwhichtwofacilitiesinMauritiusareregistered(https://www.cites.org/eng/common/reg/cb/species.html)

Foraguideonthecorrectapplicationofsourcecode,seealso:GuidetotheapplicationofCITESsourcecodes(2017)-alsoavailableinChinese,Indonesian,Khmer,Lao,Malay,ThaiandVietnamese

II. Partsofaturtleshell.

Credit:PeterPaulvanDijkandErnieCooper,originalfigurefrom CITES document: SC70 Doc. 61 Annex 6 (Guide toPhotographing Live Tortoises and Freshwater Turtles forIdentification)

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How to use this manual:

Fourmainapproachesareusedinthismanualtoidentifythetruesourceofaspecimen:

Part1: AninspectionkeyPart2: Criteriatodeterminewild-caughtversuscaptive-producedoriginPart3: AnillustratedguidePart4:Advancedmethodstodeterminewild-caughtversuscaptive-producedorigin

Theinspectionkeycanbeusedbyinspectionofficialsandcustomofficersforaninitialassessmentonwhetherthetradedspecimensshouldbefurtherinvestigatedwithregardstotheplausibilityofthereportedsourcecode.Thecriteria inPart2andthe illustratedguide inPart3canaid Inspectionofficials,customofficersand CITES Management and Scientific Authorities in differentiating wild-caught from captive-producedspecimens.InPart4weprovideadditionalsupportinginformationthatcanaidCITESManagementandScientificAuthoritiestodifferentiatebetweenwild-caughtandcaptive-producedspecimens:

Ø A table summarizing the species most relevant facts that should be reviewed, includingrelevantreferences(Table2)

Ø Atablereviewingadvancedscientificmethodsthatcanbeusedtodifferentiatewild-caughtandcaptive-producedorigin(Table3),furtherexplainedinAppendixA.

Ø A link to the “Turtles and tortoises demographic traits database for CITES-listed species”,whichprovidesadatabaseofreproductivetraitsextractedfromthescientificliteratureandfromtheSpecies360/ZIMSdatabase,furtherexplainedinAppendixB.

An important note: Theinformationpresentedinthisguidancewillassistrelevantpersonneltoidentifycaseswheretestudinesclaimedtobecaptive-bredareinfactwild-caught.However,allofthemethodologiespresented in this guidance are indicators only, and cannotbeused to unequivocallydeterminethe source of specimens. Instead, relevant personnel should use these indicators to identifyinstancesofsuspicion,forwhichin-depthinspectionandfollow-upisrequired.

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Part 1: Inspection keyThiskeycanhelptoidentifysituationswherethereisconcernaboutthetruesourceofspecimensenteringtrade.

Are you inspecting a shipment or a permanent facility?

Are the permits and documentation accompanying the shipment genuine and valid, is/are the species in the shipment

correctly identified, and is the packaging in accordance with the CITES guidelines for transport (IATA Live Animals Regulations

(LAR) and CITES Guidelines for the non-air transport of live wild animlas and plants*

Shipment

Facility

Do(es) specimen(s) show parasites and signs of sickness (ticks or leeches attached to

animal, intestinal parasites in feces; animals unresponsive, dull, with eyes closed, injuries,

open wounds etc.).

YES

NO

What source code is used for turtle specimens in the shipment?

NO

Investigate plausibility of reported source code. Check criteria to determine

wild-sourced versus captive-produced origin in Part 2.

C, D, F or R

see A

Report and investigate further, see B

Does national legislation or regulation prohibit or

otherwise restrict the import of diseased or parasitized live

turtles?

YESDetain and consult specialist, see CYES

NO

Proceed with standard clearance protocol

W

A. FortheinspectionofpermanentfacilitiespleaserefertothegeneralinformationprovidedinCITESdocumentAC30Inf.25:GuidanceforInspectionofcaptive-breedingandranchingfacilities(Lyons,Jenkins&Natusch,2017)–alsoavailableinChinese,Indonesian,Khmer,Lao,Malay,ThaiandVietnameseandtheInspectionManualforuseinCommercialReptileBreedingFacilitiesinSoutheastAsia(TRAFFIC,2013).

B. Reportandinvestigatefurther.Pleasenote,evenifonlypartoftheshipmentdoesnotmatchdocumentation,stilltheentireshipmenthastobestopped,reportedandinvestigated.Ifspeciesidentificationcannotbedeterminedpleaseuseproperphotodocumentation(seeSC70Doc.61Annex6(GuidetophotographingLiveTortoisesandfreshwaterTurtlesforIdentification,seehttps://cites.org/sites/default/files/eng/com/sc/70/E-SC70-61.pdf)andrefertotherapidspeciesidentificationtaskforce(SC70Doc.61,p.6,item24availableat:https://cites.org/sites/default/files/eng/com/sc/70/E-SC70-61.pdf).Concerningexportoflivespecimens,poorpackagingforshippingmaybeindicativeofwildorigin.Becausecaptivebreedingturtlesandtortoisesrequiressignificantinvestmentoftimeandresources,exportersshouldbemorelikelytoinvestinadequatepackagingtoensuresurvivalduringshipping.Becauseproductionofwildspecimensdoesnotrequiresuchinvestment,theimpetusforensuringadequatepackageisreduced.

C. Reporttohealthandquarantine.Parasitesandsignsofdiseasecantransmitdiseasesandmaybeindicativeofwildorigin; based on national legislation or regulation, such cases should be referred to the health and quarantinespecialist.

NOTE:*CITESGuidelinesforthenon-airtransportoflivewildanimalsandplants:(https://cites.org/eng/resources/transport/index.php)

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Part 2: Criteria to determine wild-caught versus captive-produced origin

Checkifoneormorecriteriaapply.Ifindoubt,expertconsultationisofferedbytheIUCN/SSCTortoiseandFreshwaterTurtleSpecialistGroup(TFTSG)anditsmembers(www.iucn-tftsg.org).

Table1–Criteriatodeterminewild-caughtorcaptive-producedoriginCRITERIA WILD-CAUGHTORIGIN CAPTIVE-PRODUCEDORIGIN

Uniformityandage/size

Specimensofdifferentsize,age,shapeandcoloration.Oldadultswithwornshell,orgroupsofadultsofdifferentsizes/ages.

Usually,specimenssimilarinsize,shape,ageandcolorationindicatecaptive-producedorigin.Howeververyyounganimalsofsimilarsizemayindicatewild-caughtorigininsomespecies(seepointbelowon“Onlyjuveniles”)

Damages/injuries

Minorandmajorscratches,chippedorscarredshells,severeburnmarks,scar-related,openwounds,stubbedtails,missingtoes,holesdrilledintoshell

Animallookscleanandflawless.Littleornosignsofscratches,damages,injuries,abrasionorwear.

BehaviorandHealth

Animalunresponsive,dull,eyesclosed,weak,dehydrated,underweight,freshinjuries,retractionintoshell.Freshinjuries,orinfectionsofolderinjuries,aresometimesfoundinshipmentsofwild-caughtturtlesandtortoises.Signsofdiseaselikenoisybreathing,nasaldischargeorplaquesinthemouthshouldbeassessedbyaspecialist.Loosestooloftenoccursinfrightenedcheloniansandisnotnecessarilyasignofdisease.

Animalalert,responsive,brighteyed,heavy-weight.However,somespeciesareknownfortheirshyness,willcloseupandbecompletelyunresponsiveevenafteryearsofcaptivity.Inhealthycheloniansitneedsquitesomestrengthto(carefully)pullalegout-toavoidbitingtrywithahindleg.

Parasites Freshlycaughtwildcheloniansoftenhaveexternalparasiteseitherattachedtosoftpartsorcrawlingonshell.Checkinfoldsofneckandtailforticksintortoisesorleechesinfreshwaterturtles.Iffound,informhealthandquarantine.

Parasitesinspecimensthatarecaptive-bredindoorsareuncommon,butparasitesmaybepresentinoutdoorenclosuresofwhenwildandcaptive-bredanimalsarekepttogether.Farmedfreshwaterturtlesmayshowleeches.Ifparasitesarefound,contacthealthandquarantineorconsultexpert.

Onlyjuveniles

Usually,shipmentsofmostlyjuvenilesarelikelyofcaptive-producedorigin.However,somespeciesarepronetoegg-poaching,wherepoachersdigupnestsandtheresultingwildsourcedhatchlingsmaybeshippedas“captivebred”or“ranched”.CheckforPig-nosedturtles,andside-neckedturtles(e.g.CarettochelysinsculptaandPodocnemisunifilis(P.unifilisususallyshippedasranched))fromcountrieswhereeggcollectionispopular(Indonesia,PapuaNewGuineaetc.)(Burgess&Lilley,2014).

Youngturtlesandtortoisesfromcaptivityareeasilyshipped(allsmallsizeorsimilarsize),anddifficulttofindinlargequantitiesinthewildformostspecies.Thereforeshipmentsofyoungturtlesandtortoiseswillmostprobablybecaptive-produced.Exceptionsareafewspeciesthatnestenmasseinpredictablelocations;thesearepronetoeggpoaching.However,watchoutforsignsofeggcollectiontosellhatchlings.

Shellgrowth Signsofslowgrowthsuchasnarrowgrowthringsorsmoothlookingshellscanbeindicatorsofwildorigininsomespecies(seepicturedguide)

Insomespeciesoftortoises,animalsraisedquicklytoadultsizewillshowsignsofexcessivegrowth(unusuallywide,sometimespale,growthrings)and/orpyramidalshellgrowth(seeillustratedguide).However,pyramidingmayoccurnaturallyforexampleinStartortoises,andrarelyoccursinfreshwaterturtles.

Color Colormorphsorunusualcolorstrainsorpatternsofcaptive-bredspecimensarepopularamongbreeders.Albinoturtles(whichlackallpigments),amelanistic(withoutblackpigment)andhypo-melanistic(reducedblackpigmentation)andleucistic(excessiveyellowpigment)specimensareknownforseveraltortoiseandfreshwaterturtlespecies.

Highnumbers/Breedingsuccess

Highnumbersofindividualsinasingleshipmentthatareknowntobedifficulttobreedincaptivitymaybewild-caught.Anindicatoronwhetheraspeciesisdifficulttobreedisthespeciesreproductivebiology(e.g.latesexualmaturity,feweggslaidperyeara).Furtherresearchintothespeciesmostrelevantfactsandbreedingbiologymaybenecessary(seePart4).

Onlyfewspeciesofturtlesandtortoisesareeasytobreedinhighnumbers,suchasforexampletheChineseSoftshellturtle(Pelodiscussinensis).Seefurtherinformation.Furtherresearchintothespeciesmostrelevantfactsandbreedingbiologymaybenecessary(seePart4).

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Part 3: I l lustrated guide Uniformityandage/sizeShipments of turtles or tortoises ofmixed species and/or turtles and tortoises that aredifferentinsize,age,shape,and/orcolorationarehighlyindicativeofwild-caughtorigin.

Damages,injuriesDamages to the shell, such as scars, minor and major scratches, chipping of the shell,stubbedtails,missingtoesorinjuriesarehighlyindicativeofwild-caughtorigin.

Physicaldamagetotheshellisafrequentoccurrenceinwildturtlesandtortoisesandincludesminorandmajorscratches,chipping,orbadlyscarredshells.Wild-caughtanimalscanshowvariousabnormalities,openwounds,stubbed tails, ormissing toes (Brenneret al., 2009; TRAFFIC, 2013;Benyr, 2014). Scratches on the shell arecommon especially in land tortoises that live in scrub habitats (especially those originating from drierenvironments, e.g. theMediterraneanor desert). Some tortoisesmay showmore severe injuries that occurfrom traffic accidents or agricultural machinery, such as ploughs. Significant damage may also occur fromtortoisesorfreshwaterturtlesfallingoffwalls(Meeketal.,1981;Sos,2012),fromdomesticanimals,suchassheeporcowsaccidentallysteppingontortoises,frombirdsofprey,foxes,dogsandothercarnivoresthatmayattack,gnawonaturtle’sshell,orbiteofflimbs(especiallyoflandtortoises)(pers.comm.H.Bringsøe;Meeketal.,1981).Somespeciesmayoccasionallypresentholesdrilledthroughtheedgeoftheshell,whichisdonebycollectorstotemporarilysecureanimalscapturedinthewild(TRAFFIC,2013).

Image:PeterPaulvanDijkImage:PeterPaulvanDijk

ShipmentofwildMalayemyssp.Animalsofvarioussizes,colora@onandshape.Damagesoftheshellindicatewildorigin.

ShipmentofwildKeeledboxturtles(Cuoramouho=i).Animalsofvarioussizes,colora@onandshape.TheyellowspotintheanimalattheboDomofthepictureisaburnmarktypicalforwildindividuals.

Marginatedtortoise,Testudomarginata(wild,Greece).Minorscratchesontheshellofawildtortoise.Seldomseenincap@ve-bredtortoises.Alsonotetheclearlyvisiblegrowthrings.

Marginatedtortoise,Testudomarginata(wild,Greece).Agoatorsheephassteppedontheshell.

Sicilianpondturtle,Emystrinacris(wild).Plastronscarsasusualinfreshwaterturtles.

Image:JoaquimSoler

Image:HenrikBringsøe Image:HenrikBringsøe

Image:HenrikBringsøe

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Burnmarkscausedbyforestfiresarehighlyindicativeofwild-caughtorigin.Forest fires or the common practice of agricultural burning kills many tortoises; surviving individuals oftenpossessburnmarksontheirshell.

BehaviorandhealthAnimals that are unresponsive, dull, with eyes closed, weak, dehydrated, underweight,sickorwithfreshinjuriesareindicativeofwild-caughtorigin.

Marginatedtortoise,Testudomarginata(wild,Greece).Minorscratchesontheshellofawildtortoise.Seldomseenincap@ve-bredtortoises.Alsonotetheclearlyvisiblegrowthrings.

Marginatedtortoise,Testudomarginata(wild,Greece).Agoatorsheephassteppedontheshell.

Sicilianpondturtle,Emystrinacris(wild).Plastronscarsasusualinfreshwaterturtles.

Image:JoaquimSoler

Image:HenrikBringsøe Image:HenrikBringsøe

Image:HenrikBringsøe

Testudohermanni(wild,Greece)Severedamagebyfireontheupperhindshell.Thewhitepartsaretheexposedboneyelementsunderlyingthehornscutes.Aroundthewhitepartsthehornscutesares@llpartlyintactbutshapeandcolora@onareirregular.

Terrapenecarolina(wild)Theyellowareasaresevereburnscars,probablyfrombushfires.

Image:Ju*aWiechert Image:HenrikBringsøe

Image:PeterPaulvanDijk

Shipmentofmixedspecies,wildandcap@ve:Mauremysreevesii(likelycap@ve,roundwithblacklines);Trachemyssp.(unknownorigin,ornamentedcarapace);Manouriaimpressa(likelywild,singleindividualwithspikes);Indotestudosp.(likelywild,farright,rounded).Interes@ngisthedifferenceinbehaviorbetweencap@veandwildspecimens.Cap@veonesarealertwithheads@ckingout;wildonesareunresponsive.

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Captive-bredindividualscanbehabituatedtothepresenceofhumans,smallspaces,theconstantavailabilityoffood and water, and the absence of predators (El Balaa & Blouin-Demers, 2011). Signs of captive originthereforeincludethattheanimalsarewell-fed,areresponsiveoroccasionallyevenaggressivetowardshumans(Benyr, 2014). This, however, may not apply to captive animals that are sick or were kept under poorhusbandryorafterlongtimetransportation,whichisstressfulformostanimals.Whenanimalsaretakenfromthewild,theanimalsareoftenkeptunderpoorconditionspriortotransportandmayshowsignsofdisease,andbedesiccatedorunder-fedandthereforelightinweight.Wildanimalsareunaccustomedtobeinghandledortotakefoodfromhumansandaremorelikelytoshowsignsofstressanddisease,withdrawintotheirshell,orareunresponsive,lethargic,dull,and/orrefusetoeat.ParasitesThepresenceofticksorleechesisindicativeofwild-caughtorigin.

Externalparasitessuchasticksorleechescanbehighlyindicativeofwild-caughtorigin.Somespeciesofticksandleechesrequireseveralhostspeciesandhavewelldefinedgeographicboundariesthatcanhelptracktheorigin of the specimen that they are attached to. For example, the tickHyalomma aegyptiumis typical forTestudo species and occurs in the Mediterranean, Middle East and Central Asia (Brianti et al., 2010);Amblyommasparsum typical forAfricanGeochelone species (Mihalca,2015).Leechescanusuallynotsurvivelong incaptivityandaretypicalvectors (carriers)ofotherbloodparasites (hemogregarines); thepresenceofbothcanbehighlyindicativeofwild-caughtorigin.Whereas,parasitessuchasticksorleechesaregenerallynotpresentincaptive-bredturtleindividualsthatarebredindoors,butleechesmaybepresentinfarmedturtles,or if wild-caught and captive-produced individuals are raised together or in outdoor enclosure in rangecountries. Often require several host species, and with well defined geographical boundaries. The correctsampling and the determination of the type of parasite is therefore of crucial importance and needs to beassessedbyanexpert(forfurtherdetails,seeAppendixA).

Amblyommasp.inGeochelonepardalis.TypicalforAfricanGeochelonespecies.

Hyalommaaegyp=uminTestudograeca.TickthattypicallyoccursintheMediterannean,MiddleEastandCentralAsia(Brian@etal.,2010).

Placobdellasp.inEmysorbicularis.Leechesusuallydonotoccurinturtlesincap@vity.Onlysome@mesinfarmedanimalskeptinoutdoorpondsorifwildandcap@veindividualsarekepttogether.

TickhiddeninthecavityofaleginawildTestudomarginata.

Image:AndreiDanielMihalca Image:And

reiD

anielM

ihalca

Image:And

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anielM

ihalca

Image:HenrikBringsøe

Amblyommasp.inGeochelonepardalis.TypicalforAfricanGeochelonespecies.

Hyalommaaegyp=uminTestudograeca.TickthattypicallyoccursintheMediterannean,MiddleEastandCentralAsia(Brian@etal.,2010).

Placobdellasp.inEmysorbicularis.Leechesusuallydonotoccurinturtlesincap@vity.Onlysome@mesinfarmedanimalskeptinoutdoorpondsorifwildandcap@veindividualsarekepttogether.

TickhiddeninthecavityofaleginawildTestudomarginata.

Image:AndreiDanielMihalca Image:And

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anielM

ihalca

Image:And

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Image:HenrikBringsøe

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ShellgrowthNarrow growth rings and a smooth, continuous profile of the shell can be indicative ofwild-caughtorigininsomespecies.

Allspeciesofturtles(exceptsoft-shellturtles:Trionychidae,Carettochelysinsculpta,andDermochelyscoriacea)growtheirshellbyformingnewepidermalkeratinlayersbeneathandbeyondthescuteofthepreviousgrowthcycle,liftingtheoldscuteofftheunderlyingboneandconnectivetissue(Zug,1991).Thistypeofgrowthleadsto the formation of concentric growth rings around the edges of the older scutes. Growth rates of captivetestudinesareoftenacceleratedascomparedtoanimalslivinginthewild.Thewidthofthegrowthringscanbe used to determine whether the turtle has shown periods of irregular or excessive growth, indicating aperiodwhere theanimalhasbeenkept incaptivity.Recentlyaddedwider rings inananimalwithotherwisenarrowringscanbean indicationofawildanimal thathas recentlybeen taken intocaptivity.Shellsofwildchelonianstypicallyhaveasmooth,continuousprofileduetoslowgrowthandnarrowgrowthrings(especiallyinoldanimals)and/orduetoabrasionorwear,orcanbeslightlyraised.Pyramidal growth and wide growth rings due to periods of excessive growth can beindicativeofcaptive-productioninsometortoisespecies.

Severaldietary andenvironmentaldifferences in captivity, commonly lead to thedevelopmentofpyramidalshaped horny plates, referred to as pyramidal growth syndrome (Gerlach, 2004). Pyramidal growth ismoreprevalent intortoises,butoccasionallyoccurs in freshwaterturtles. Inthewild, thiscondition israretonon-existent(Wiesner&Iben,2003;Heinrich&Heinrich,2016)butafewspecies,havenaturallydomedscutes(e.g.Geocheloneelegans,Psammobates spp.) (Wiesner& Iben,2003)ormayhave ridgeson the carapace scutes(Stigmochelyspardalis)(pers.comm.Pingleton,M.).Experiencedbreedersthatoffergoodhusbandryareable

Red-footedtortoise,wild(Chelonoidiscarbonarius).Afreshlyimportedwild-caughtfemale;hercarapace(leP)hasasmooth,flowingappearance,butnotethedings,dents,andscratchesevidentalonghersides;thisistypicalforatortoisethatlivesindenseundergrowth,andnottypicalofcap@veanimals.Herplastron(right)iswornsmoothlikeariverpebble,fromalife@meofabrasionfromnaturalsubstrate.Plastraofcap@ve-bredanimalsaretypicallymuchrougherinappearanceandfeel.

Image:MikePingleton Image:M

ikePingleton

Red-footedtortoise,cap@ve(Chelonoidiscarbonarius).Acap@veindividualwithpyramidgrowthandwidegrowthringsoPenseenincap@ve-raisedturtlesandtortoises.

Red-footedtortoise(Chelonoidiscarbonarius).Thepictureisofawild-caughtadultthathasspentsome@meincap@vity,andshelldevelopmenthasalteredasaresult.

Image:MikePingleton

Image:MikePingleton

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to minimize or avoid pyramid growth in their animals. Therefore, the presence of this condition is a fairlyreliableindicatorthatthespecimenwasraisedincaptivity.TransportationTransportation not according to CITES transportation guidelines – (animals crammed,overlytapedetc.).

Illegallytradedshipments,possiblyconcerningwild-collectedturtles,maybepackagedininappropriate(non-IATA-compliant)packaging,orshipped‘disguised’asanotheritem.Shipmentsoflegallytradedtortoisesandfreshwaterturtles,whetherwildorcaptive-produced,arelikelytoadheretorequiredstandardsofpackagingandshipping.Responsiblebreedersinvestconsiderabletimeandmoneyintothecaptivebreedingoftheiranimalsandusuallyhaveaninterestinensuringsecure,hygienictransportation,documentation,andhighstandardsofanimalwelfare,includingshippingtoprevailingstandards. Part 4: Advanced methods to determine wild-caught versus captive-produced origin Whetheraparticulartradeshouldraiseconcernsonthepotentialmisuseofsourcecodeswilldependonmanyfactorsandonthespecificsituation,species,andcountryfromwhichthespeciesisexported.Researchonthespeciesmost relevant facts can be of crucial importance in the evaluation of a fraudulent claim of captiveorigin, suchas thespeciesbreedingbiology, its threatstatus,national legislations,andcountriesofconcern.ResourcesforsuchareviewareprovidedinTable2.Moreover,insomecasesadvancedmethodsandexpertassessment may be necessary. An overview of advanced scientific methods that may be useful in thedifferentiationbetweenwild-caughtandcaptive-producedindividualsisprovidedinTable3.Many species of turtles and tortoises are very difficult to breed in captivity, for examples because they arestress-sensitive, are difficult to keep in groups (e.g. solitary forest turtles), show intraspecific aggression(aggression towards other individuals of the same species) or reproduce and grow slowly. The slowreproduction of some species coupledwith high costs ofmaintenance of the species in captivity (includingcosts for food, space, electricity, veterinary care etc.)makesbreedingofmany testudinesunprofitable on alargecommercialscale(Sigouinetal.2017).Knowledgeonthereproductivetraitsofaspeciescantherefore

SeizureofblackspoDedturtle,Clemmysgu5ata.Individualsarecrammedandoverlytapedandwereillegallysmuggledinsuitcases.

Image:PanjitTansom/TRAFFIC

Image:PanjitTansom/TRAFFIC

Image:PanjitTansom/TRAFFIC

Seizureofradiatedtortoise(Astrochelysradiata)andploughsharetortoise(Astrochelysyniphora).

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give a crude estimation on the biological limits, i.e. on the number of offspring that can maximally beproduced. If thedemandexceeds the reproductive potential, illegal launderingwill becomemoreprofitableandismorelikelytooccur.Toassessthereproductivepotentialofaspeciessomeresearchandunderstandinginto the species life history is necessary. Some traits that are important to consider include: Age at firstreproduction,clutchsize,numberofclutchesperyear,inter-birth-intervals,survivalratesofeggsandjuvenilesandthespeciesreproductivelifespan.To aid in the assessment of biological breeding limitswe developed a database of demographic life historytraits that can help to inform the CITES Management and Scientific Authorities (APPENDIX B). The dataprovidedfromZoosandAquariumsshouldbetakenwithcautionbecausezoosandaquariumsarenotbreedingspecies for commercial purposes, but may give a crude idea on whether breeding is possible. We aim tocontinueadding information to thisdatabaseasmoredatabecomesavailable from fieldbiologist, zoosandaquariums,andregisteredcommercialbreeders.Table2:Recommendedresourcesforareviewofthespeciesmostrelevantfacts:TypeofInformation: Suggestedreferences:Taxonomy Referencelistofidentificationguides:pp.71-81inCoP17Doc.73

https://cites.org/sites/default/files/eng/cop/17/WorkingDocs/E-CoP17-73.pdfCITEStaxonomicnames&Appendices:https://speciesplus.net/speciesGlobalspecieslist:CatalogueofLife:http://www.catalogueoflife.org

Legal FAO,IUCNandUNEP.ECOLEX–thegatewaytoenvironmentallawwww.ecolex.orgUNEP–TheSpecies+website:www.speciesplus.netCITESChecklist:http://checklist.cites.orgLegalAtlas:https://www.legal-atlas.netIUCNRedList:http://www.iucnredlist.org

Threatstatus IUCNRedList(globalandregional):http://www.iucnredlist.orgNationalRedList:http://www.nationalredlist.orgIUCNSSCTortoiseandFreshwaterTurtleSpecialistGroup:TheTop25+mostendangeredspeciesoftortoisesandfreshwaterturtlesintheworld:http://www.iucn-tftsg.org/trouble/

Speciesgeographicalrange CITESChecklist:http://checklist.cites.orgIUCNRedList:http://www.iucnredlist.org

Tradevolumes UNEP-WCMCCITESTradeDatabase:https://trade.cites.orgGuidetousingtheCITESTradedatabase:https://trade.cites.org/cites_trade_guidelines/en-CITES_Trade_Database_Guide.pdfSeeAppendixAfortotalnumbersofliveindividualsexportedforcommercialtradefrom2010-2016fordifferentsources.

Species/Countriesofconcern Thisinformationcanbeobtainedfromvariousonlinesources,suchasnewsreportsorfromorganizationssuchasthewildlifetrademonitoringnetworkTRAFFIC-https://www.traffic.org

Captivebreedingoperations CITES–Registerofcaptivebreedingoperationshttps://www.cites.org/eng/common/reg/e_cb.htmlTheEUWildlifeTradeRegulationCaptiveBreedingDatabasewww.captivebreeding.unep-wcmc.orgSpecies360ZoologicalInformationManagementSystem(ZIMS)https://www.species360.org-seeAppendixAandB

Reproductivedata Turtles and tortoises demographic traits database for CITES-listed speciesThisinformationcanbeobtainedfromvarioussourcesonline,seealsodatabaseAppendixB.

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Table3.Summaryofadvancedmethodstodeterminewild-caughtversuscaptive-producedoriginParasites Theidentificationofparasitespeciesthatrequireoneorseveralintermediatehostspeciestocomplete

theirlifecycle(socalledheteroxenousspecies)areofhighimportancetodetermineifanindividualiswildcaught.Thesetypesofparasitesareveryunlikelytooccurincaptivity,becausetherespectivehostspeciesareusuallynotpresentincaptiveenvironments(seeAppendixA).

Stableisotopeanalyses

Itispossibletousetheisotopesignaturesinaspecimen’stissuesampletoreconstructpastenvironmentalandclimaticconditions,itsdiet,ortrophiclevel.Isotopicanalysiscanpotentiallybeusedasaregulatorytoolfortheturtle/tortoisetradesuchasindetermining1)ifbatchesofcaptivespecimensalsoincludewild-caughtindividualsand2)ifwild-caughtspecimenshavebeenfraudulentlyclaimedascaptive-bred(seeAppendixA)

Bloodparameters

Bloodparameterdifferencesfoundbetweencaptivebredandwildcaughtindividualsaremostlyattributedtodifferencesindiet,environment,healthandage.Parametersincludecountsofbloodcells,andconcentrationsof:lipids,natrium,kalium,urea,haematocritandhaemoglobin,amongothers,whichinmanycaseshavebeenfoundtobesignificantlydifferentbetweenwildandcaptive-bredindividuals(seeAppendixA)

Geneticsamples

Forensicgeneticscanbeusedforspeciesandsourcepopulationidentificationandcanassistwiththeidentificationonwhetherananimalwascaptive-producedorwild-caughtforexamplebydeterminingthelikelihoodthatatradedspecimenisinfacttheoffspringfromaclaimedbreedingstock.Itisalsopossibletoassigngeneticsamplestoaparticulargeographicorigin(seeAppendixA).

Marking Individualmarkingtechniquescanbeofhighvalueinassistingenforcementauthoritiestotracetheoriginofaspecimen.Theuniquedetailsofthemark,suchasthenumbercodeneedtomatchthenumberontheaccompanyingpermittoensurethatspecimensarethesameasthosereferredtointhedocumentation(seeAppendixA)

Passport ThePan-AfricanAssociationofZoosandAquaria(PAAZA)isdevelopingthePAAZAAnimalPassportthatlinksanimalidentificationwithanationaldatabase.Therefore,authoritieswillhavereadyaccesstoasecuredigitaldatabasetotracetheoriginofanindividual.Intheprocess,itwouldalsoassistEnforcementwithanimalidentificationthroughtransponder/microchipandDNAdata,whichislinkedthroughthevariousStudbookdatabases(seeAppendixA)

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References:

Benyr,G.(2014)DieUnterscheidungvonWildfängenundNachzuchtenbeiReptilien:IhreBedeutungfürdenArtenschutz.ProjektendberichtimAuftragdesBMLFUW(MinisteriumfüreinlebenswertesÖsterreich)Abt.I/8,Nationalparks,Natur-undArtenschutz

Brenner,D.,Lewbart,G.,Stebbins,M.,&Herman,D.,W.(2009).Healthsurveyofwildandcaptivebogturtles(Clemmysmuhlenbergii)inNorthCarolinaandVirginia.dx.doi.org,33,311–316.

Brianti,E.,Dantas-Torres,F.,Giannetto,S.,Risitano,A.,Brucato,G.,Gaglio,G.,&Otranto,D.(2010).RiskfortheintroductionofexoticticksandpathogensintoItalythroughtheillegalimportationoftortoises,Testudograeca.Medicalandveterinaryentomology,24(3),336-339.

Burgess,E.A.andLilley,R.(2014).AssessingtheTradeinPig-nosedTurtlesCarettochelysinsculptainPapua,Indonesia.TRAFFIC.PetalingJaya,Selangor,Malaysia.

CITES-SeventeenthmeetingoftheConferenceofParties,CoP17Doc.73,Tortoisesandfreshwaterturtles(Testudinesspp.)Availableat:https://cites.org/sites/default/files/eng/cop/17/WorkingDocs/E-CoP17-73.pdf

ElBalaa,R.,&Blouin‐Demers,G.(2011).Anti‐predatorybehaviourofwild‐caughtvscaptive‐bredfreshwaterangelfish,Pterophyllumscalare.JournalofAppliedIchthyology,27(4),1052-1056.

Gerlach,J.(2004).Effectsofdietonthesystematicutilityofthetortoisecarapace.AfricanJournalofHerpetology,53(1),77-85.

Heinrich,M.L.,&Heinrich,K.K.(2016).EffectofsupplementalheatincaptiveAfricanleopardtortoises(Stigmochelyspardalis)andspurredtortoises(Centrochelyssulcata)ongrowthrateandcarapacialscutepyramiding.JournalofExoticPetMedicine,25(1),18-25.

Lyons,Jenkins&Natusch(2017).GuidanceforInspectionofCaptiveBreedingandRanchingFacilities.https://cites.org/sites/default/files/eng/com/ac/30/Inf/E-AC30-Inf-25.pdf

Meek,R.,Inskeep,R.(1981).AspectsofthefieldbiologyofapopulationofHermann'stortoise(Testudohermanni)inSouthernYugoslavia.BritishJournalofHerpetology,6,159-164.

Mihalca,A.D.(2015).TicksimportedtoEuropewithexoticreptiles.Veterinaryparasitology,213(1-2),67-71.

Nijman,V.,andShepherd,C.(2009).WildlifetradefromASEANtotheEU:Issueswiththetradeincaptive-bredreptilesfromIndonesia.TRAFFICEuropeReportfortheEuropeanCommission,Brussels,Belgium.Availableat:https://www.traffic.org/site/assets/files/9837/issues-with-the-trade-in-captive-bred-reptiles-from-indonesia.pdf

Sigouin,A.,Pinedo-Vasquez,M.,Nasi,R.,Poole,C.,Horne,B.,&Lee,T.M.(2017).Prioritiesforthetradeoflesscharismaticfreshwaterturtleandtortoisespecies.JournalofAppliedEcology,54(2),345-350.

Sos,T.(2012).TwoextremecasesofregenerationinTestudograecaiberaPallas,1814.BiheareanBiologist,6(2),128-131

TRAFFIC(2013).InspectionManualforuseinCommercialReptileBreedingFacilitiesinSoutheastAsia.ReportpreparedbyTRAFFIC.SecretariatoftheConventiononInternationalTradeinEndangeredSpeciesofWildFaunaandFlora(CITES),Geneva,Switzerland.p.81.Availableat:https://cites.unia.es/cites/file.php/1/files/cb-captive-breeding-manual-en.pdf

Wiesner,C.S.,&Iben,C.(2003).InfluenceofenvironmentalhumidityanddietaryproteinonpyramidalgrowthofcarapacesinAfricanspurredtortoises(Geochelonesulcata).Journalofanimalphysiologyandanimalnutrition,87(1‐2),66-74.

Zug,G.,R.(1991).AgeDeterminationinTurtles.SocietyfortheStudyofAmphibiansandReptiles,HerpetologicalCircular20.Lawrence,Kansas,U.S.

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APPENDIX A Supplemental information on advanced methods for the differentiation of captive vs. wild origin

1. Parasites 2. Stable isotope analysis 3. Blood parameters 4. Genetic samples 5. Individual Marking and Passport

1. Parasites:Parasitescanserveasareliableindicatorofwildoriginoftradedspecimensbecausemanyparasiteshave highly complex life-cycles and restricted geographic ranges. Of particular importance arespeciesthatrequireoneorseveral intermediatehostspeciestocompletetheir lifecycle (socalledheteroxenous species). These are very unlikely to occur in captivity, because the respective hostspeciesareusuallynotpresent in captiveenvironments.Notallparasiteswillbe indicativeofwildorigin, the correct sampling and the determination of the type of parasite is therefore of crucialimportance.Groupsofparasiteswithhighforensicvalueincheloniansincludetheprotozoanbloodparasites Haemogregarines and Haemosporidia, which can be detected in blood smears; internalparasites such as Trematodes (flukes), Cestodes (tapeworms), Acanthocephalans (thorny-headedworms)andNematodes,particularSpirurida&Filaria(roundworms).Theirstages(ususallyeggs)canbedetectedinfecalsamples,andsometimesinorgansorundertheskin,larvaeoffilaria,socalledmicrofilariae,aredetectedinbloodsmears.Externalparasitesincludeticksandleeches.Bloodparasites:Haemogregarines (Protozoa) stages detectable in blood and tissue of turtles and tortoises oftentransmittedviablood-suckinginvertebrates(leeches,ticks,mosquitoesetc.)(Kreier,1977),normallynotpresent in captivity. Infections canbedetected inblood smears and infectionpersists inwild-caught individualsevenafteryearsof rearing incaptivity (Širokýetal.,2004).Haemoliviaspp.andHepatozoonspp.areespeciallyimportantindeterminingthegeographicoriginoflandtortoises(e.g.HaemoliviamauritanicadoesnotoccurinCentralEurope;Hepatozoonfitzsimonsi isonlypresentinAfrican terrestrial tortoises such as in some species of the genusKinixys (Cook et al., 2014)). Thegenus Haemogregarina (Placobdella in Europe) can be an important indicator found mostly inaquaticturtles(DvořÁkovÁetal.,2015).Forexample,Haemogregarinasp.wasdetectedin100%ofthe wild individuals, but not in captive individuals inDermatemys mawii (Rangel-Mendoza et al.,2009).HaemogregarinastepanowicanbefoundinthedistributionrangeofEuropeanturtlespeciesofthegenusEmysandMauremys(Özvegyetal.,2015;Javanbakht&Sharifi,2014).Haemosporidia (Protozoa) - detectable in blood smears; can be proof of wild origin; furthermorphological and genetic examination can determine geographic region of origin for example inTestudograecaandT.horsfieldi(Javanbaghtetal.,2015).Internalparasites:Trematodes (flukes) - Eggs detectable in feces. Require intermediate hosts, (often molluscs) that

cannotcompletelifecycleincaptivity.Cestodes(tapeworms)-Eggsandproglottidsdetectableinfeces,sometimeinorgansorabdominal

cavities (in dead specimens only), and under skin; highly suggestive for wild origin,transmissionincaptivityhighlyunlikely

Acanthocephalans(thorny-headedworms)-liveingut,eggsandlarvawithobvioushornsdetectablein feces; presence is highly suggestive of wild origin, transmission in captivity extremely

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unlikely;Nematodes,particularSpirurida&Filaria (roundworms)–eggsofSpiruidainfecesandpresenceof

microscopic larvae in blood smears in Filaria suggest wild origin. Transmitted by ingestedinsectsasintermediatehostsorbyblood-suckinginsects.

Externalparasites:Ticks–presentexternallyonthespecimen,eitherattachedorunattached.Oftenrequireseveralhost

species,andwithwelldefinedgeographicalboundaries.Hyalommaaegyptiumistypical forTestudospeciesandoccursintheMediterranean,MiddleEastandCentralAsia(Briantietal.,2010);AmblyommasparsumtypicalforAfricanGeochelonespecies(Mihalca,2015).

Leeches: externally attached to aquatic turtles. Strong indicator as they cannot survive long incaptivity.However,maychangehost in facilitiessharedbetweenwildandcaptiveanimals.Typicalvectorofbloodparasites(hemogregarines).Ifleechesarepresentbloodshouldalsobeexamined.Presenceofbothishighlyindicative.

Howto:Importedanimalsshouldbephysicallyinspected,preferablybyaveterinarianortrainedstaff.Visibleparasites should be documented with protocol and photo-documentation. Parasites are thencollectedfromthebodyand,ifpossiblefromtheoralcavity.Ticksandleechesarecommonlyfoundonsoftpartsofturtlesandtortoiseshiddeninskinfolds,butalsocrawlingontheshelllookingforaplacetoattach.Ifsubcutaneousparasitesarepresent,swellingsornodulesshouldbephotographedandcanbesurgicallyremovedbyaveterinarianforfurtherexamination.Fecalsamplescanbetakennon-invasively,andideallyfreshinquantitiesof5-10g(dependingontheindividualsbodysize)or,ifindividualsamplingisnotpossible,canbetakenfromthetransportationbox.Ingroupsofindividualssamplesshouldbetakenof10%-30%ofindividualsdependingongroupsize.Allsamplesshouldbelabeled(animalID,dataandplaceofcollection),storedcoolinaclosablecontainer(e.g.plastictubewithlid),anddispatchedinacooledboxassoonaspossibletoalaboratory.Ifstorageexceedsthreedayssamplescanbepreserved informalinorethanol.Forbloodanalysisaveterinarian isrequiredwhocantakeabloodsmearandasampleoffullbloodinpureabsoluteethanol.Carcassesofdeadanimals can be submitted for necropsy. Gloves and disinfectants should be used when takingsamples,assomeparasitescantransmitdiseasestohumans.

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2. Stableisotopeanalyses:Isotopesarevariantselements,suchashydrogen,carbon,nitrogenoroxygen,thatslightlydifferbytheirmasses. Because the different isotopes vary their ratios and compositions across geographicregionsortrophiclevels,itispossibletousetheisotopesignaturesinaspecimen’stissuesampletoreconstructpastenvironmentalandclimaticconditions,itsdiet,ortrophiclevel.Isotopicanalysiscanpotentially be used as a regulatory tool for the turtle/tortoise trade such as in determining 1) ifbatchesof captive specimensalso includewild-caught individuals, and2) ifwild-caught specimenshave been fraudulently claimed as captive-bred (Wood, 2012). Isotope analysis can be of strongforensic value, highly accurate and difficult to falsify (Van Schingen et al., 2016) but is highlydependent on the reference data to compare with. At best the isotope signature of all wildpopulationsshouldbecomparedwiththesampleofunknownorigin.Toassessthevariationinthesampleswould be a first rough estimate. The isotopic variation among samples is expected to bemuch lower in captive specimens, because they always have the same food source than in wildanimals that have diverse prey. However, it is important to note that one cannot conclude thatindividuals with similar isotope signature come from the same region, only that physiologicallysimilar individualswithdifferent isotopesignatureareprobablynot fromthesamehabitat (Wood,2012;Benyr,2014).Furtherlimitationsofthemethodincludealackofestablishedprotocolsduetothe limited amount of studies conducted so far, high costs, and time expenses. Themethodmayfurther not be applicable to species with vast distribution ranges and species that are food andhabitatgeneralists(VanSchingenetal.,2016).Moreover,anumberoffactorscaninfluenceisotopesignature in an individual and lead to error, such as heat stress, age, sex, nutritional stress etc.;therefore themethod is only applicablewhendealingwith samples that are similar to samplesofunknown origin (Wood, 2012). In previous studies, isotope analysis has been used to accuratelydifferentiatewildandcaptivecrocodile lizards,Shinisauruscrocodilurus (VanSchingenetal.,2016),to reconstruct resource use over decades for the loggerhead sea turtle, Caretta caretta (VanderZandenetal.,2010),todeterminedietaryswitchesinthedeserttortoise,Gopherusagassizii(Murray&Wolf, 2012), andhas recentlybeendiscussedasa tool to regulate trade in three speciesof thegenusTestudo(Wood,2012).Howto:Tissueshavedifferentturnoverratesandthetissuetobesampleddependsonwhatbestreflectstheperiodofinterest.Tissuesthatmaybeusefulincludeclaw,carapacialandplastralkeratin,blood,andindeadspecimens:bones,liver,andmuscle(Wood,2012).Ofparticularimportanceseemstobemetabolicallyinerttissue,suchasscutematerial,whichcanbesamplednon-invasivelyandtowhichmaterialiscontinuouslyaddedoverthelifetimeinnon-sheddingspecies,becauseisotopesignaturescanbepreservedindefinitely(Wood,2012).Samplingshouldbeconductedbyaveterinarianandthesamplesofspecimenswithunknownoriginshouldbecomparedwithreferencesamplesfromwildspecimensthatshouldideallycoverthespeciesentiredistributionrange.3. Bloodparameters:Health assessmentsmeasuring haematocrit and haemoglobin concentration in blood samples andbodysizehavepreviouslybeenusedincrimeconvictionsbycomparingwildandconfiscatedanimals(Henen et al., 2013). Similar procedures might apply to captive and wild animals. For example,Swimmer(2000)foundsignificantlyhigherlevelsofcorticosterone,lactate,triglyceride,glucose,andcalciuminHawaiianwildascomparedtocaptivegreenturtles(Cheloniamydas). In loggerheadseaturtles(Carettacaretta),countofredbloodcellsandhaemoglobin levelswerehigher incaptiveascompared to wild turtles (Basilie et al., 2012). Rangel-Mendoza et al. (2009) found differencesbetween wild and captive individuals in several hematological parameters in the criticallyendangered Central American river turtle (Dermatemys mawii) and Brenner et al. (2002) in bogturtles (Clemmys muhlenbergii). Captive bog turtles had higher white blood cell counts, a lowerpercentageofheterophils,andlowerlevelsofNatrium,Kalium,andureanitrogen.Studiesinotherreptileshavefoundsimilarresults,suchasanincreaseinwhiteandredbloodcellsinwildtuatara,whichhasbeenrelatedtothehighertickburden(Cartlandetal.,1994).Obesecaptive

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tuatara showedan increasedplasma lipid concentration, suchas cholesterol as compared to theirwild counterparts (Cartland et al., 1998). Differences in blood parameters have been mostlyattributed to differences in diet between captive and wild individuals, such as better nutritionalstatus and the richer diet of captive versuswild animals and lower protein intake inwild animals(Basilieetal.,2012).Moreover,higherdensitiesincaptivitymayresultinelevatedstresslevels,suchas corticosteroneor testosterone in somepopulations (Benyr, 2014). Bloodparameter samples ofspecimenswithunknownorigin shouldbe comparedwith reference samples fromwild specimensthat should ideally cover the species entire distribution range. Moreover, blood values may beaffectedbymany factors suchas the age, health status, themethodofbloodwithdrawal and themethodofanalysis.How to:A veterinarian can collect Blood samples. Experts for example fromveterinary orwildlifeforensics institutionsmaybeable tomake further conclusion, if reference values for thedifferentpopulationsareavailableorcanbecollected.4. Genetics:Forensic genetics is an advanced technique that can be used for species identification and sourcepopulationidentificationandmaythereforealsobeusedtoidentifywhetherananimalwascaptive-bredorwildsourced.Oneadvantageisthatitcanbeappliedtoliveorganismsbutalsotoderivativesandparts.DNA-analysiscanbeusedtodetermineifaspecimenbelongstoaCITESlistedspecies,orto assess how related is an individual to another, in this sense genetic analyses can be used todetermine the likelihood of traded specimen to in fact be the offspring from a claimed breedingstock. It isalsopossibletoassigngeneticsamplestoaparticulargeographicorigin.Likewise, itwaspossibletoassignwildandcaptiveEuropeanpondturtlestotheirregionoforiginusingthegeneticmarker cytochrome b (Velo-Anton et al., 2011). The method of identification of genetic originrequiresthatgeneticpopulationdataexistsfromthevariousregionsandthatthepopulationshavegeneticsignaturesthataresufficientlydistinctfromoneanother(Ogdenetal.,2009).Thismaynotbe the case, for example if populations regularly exchangegeneticmaterial or if populationshaveonly been recently geographically separated. Genetic data is probably still lacking for manytestudines species, but due to advances in genetic technologies they are increasingly stored ingeneticdatabasessuchasGenBank(Benson,2008).Captivepopulationsoftenshowreducedgeneticdiversityascomparedtowildpopulations,forexampleduetoinbreeding.Thismaybeusedtoassisttheidentificationofwhetheranindividualstemfromacaptivepopulation.Howto:Geneticsamplescanbecollectedbyaveterinarianforexampleasbloodortissuesamplesfromliveanimals,butaswellasfrompartsandderivativesforexamplewiththehelpofastandardDNA sampling kit. Specific Wildlife forensic DNA kits including an instruction manual have forexample been published by the ForensicWorkingGroup (FWG) part of the Partnership for ActionagainstWildlifeCrime(PAW).However,therightmolecularmarkershouldbeuseddependingonthequestions. Furtherguidanceonwildlife forensicsmethodscanbeobtained fromTRACE (ToolsandResources for Applied Conservation and Enforcement) – the wildlife forensics networkhttps://www.tracenetwork.org/wp-content/uploads/2012/08/Wildlife_DNA_Sampling_Guide_web.pdf5. IndividualMarkingandPassport

5.1IndividualmarkingIndividualmarkingtechniquescanbeofhighvalueinassistingenforcementauthoritiestotracetheoriginofaspecimen.Theuniquedetailsof themark,suchas thenumbercodeneedtomatchthenumberontheaccompanyingpermittoensurethatspecimensarethesameasthosereferredtointhe documentation. European regulations (The EC Wildlife Trade Regulation and some nationallegislations)requirethatalllivevertebratesofspecieslistedonAnnexAbeingusedforcommercialpurposes(CouncilRegulation(EC)No338/97),arepermanentlyanduniquelymarked.AnnexAlistedtestudines should be marked with an unalterable microchip transponder, or where this is not

17

possible, a ring, band, tag, tattoo or another appropriate method. Some Member States haveadditionalguidelinesornational legislationsonwhichmarkingtechniquearetobeusedforcertainspecimens/species.Germany for example requires photo-documentationor other specificmarkingmethods for several testudines species, including Geochelone radiata, Testudo hermanni, and Testudo marginata, (for more information visit www.dght.de) (European Commission, PracticalinformationonMarkingandLabelling).TheInternationalZooVeterinaryGroup(IZVG)reviewedandidentifiedmethodstopermanentlymarkjuveniletortoisesintrade,thataretoosmalltobemarkedbymicrochips(Walteretal.,2009).Howto:Checkwhethertheuniquedetailsofthemark,suchasthenumbercodeneedtomatchthenumberontheaccompanyingpermittoensurethatspecimensarethesameasthosereferredtointhedocumentation.

5.2PassportAninterestingapproachthathasbeendevelopedbythePan-AfricanAssociationofZoosandAquaria(PAAZA)isthePAAZAAnimalPassportthatlinksanimalidentificationwithanationaldatabase.ThePAAZAAnimalPassportwasintroducedasasecure,on-lineelectronicentryofanimalidentificationtocreateaNationaldatabase(SouthAfricanDepartmentofEnvironmentalAffairs)ofinitiallyCITESandTOPS (ThreatenedorProtected Species) captiveWildlife. ThiswouldAssist CITES and regionalNationalTOPSPermittingbyhavingreadyaccesstoasecuredigitaldatabase.Intheprocess,itwouldalso assist Enforcement with animal identification through transponder/microchip and DNA data,whichislinkedthroughthevariousStudbookdatabases.BecauseofthelinkeddatarecordedintheStudbook,theAnimalPassportwouldstrivetoensurethatcaptiveborniscaptivebornandalsobeagood resource in creating internationally viable breeding populations, particularly for endangeredspecies.Mosttaggingmethodscanbeaccommodatedintothedatabasesinceitisanalphanumericprotocol.WithreferencetoTurtles,bothRFIDandSatellitetagscanbeusedandrecorded.RFIDcanberecordedbyhandheldreaders(researchers)orautomaticallythroughembeddedgroundreadersat specific breeding locations (as with many other species) (pers. comm. John Werth, ExecutiveDirector,PAAZA).References Basile,F.,DiSanti,A.,Ferretti,L.,Bentivegna,F.,&Pica,A.(2012).HematologyoftheMediterranean

populationofseaturtle(Carettacaretta):comparisonofbloodvaluesinwildandcaptive,juvenileandadultanimals.ComparativeClinicalPathology,21(6),1401-1406.

Benson,D.A.,Karsch-Mizrachi,I.,Lipman,D.J.,Ostell,J.,&Wheeler,D.L.(2008).GenBank.Nucleicacidsresearch,36(Databaseissue),D25.

Benyr,G.(2014)DieUnterscheidungvonWildfängenundNachzuchtenbeiReptilien:IhreBedeutungfürdenArtenschutz.ProjektendberichtimAuftragdesBMLFUW(MinisteriumfüreinlebenswertesÖsterreich)Abt.I/8,Nationalparks,Natur-undArtenschutz

Brenner,D.,Lewbart,G.,Stebbins,M.,&Herman,D.,W.(2009).Healthsurveyofwildandcaptivebogturtles(Clemmysmuhlenbergii)inNorthCarolinaandVirginia.dx.doi.org,33,311–316.

Brianti,E.,Dantas-Torres,F.,Giannetto,S.,Risitano,A.,Brucato,G.,Gaglio,G.,&Otranto,D.(2010).RiskfortheintroductionofexoticticksandpathogensintoItalythroughtheillegalimportationoftortoises,Testudograeca.Medicalandveterinaryentomology,24(3),336-339.

Cartland,L.K.,Cree,A.,Sutherland,W.H.F.,Grimmond,N.M.,&Skeaff,C.M.(1994).Plasmaconcentrationsoftotalcholesterolandtriacylglycerolinwildandcaptivejuveniletuatara(Sphenodonpunctatus).NewZealandjournalofzoology,21(4),399-406.

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APPENDIX B The Turtles and tortoises demographic traits database for CITES Listed species Manyspeciesofturtlesandtortoiseshavealowreproductivepotential;thatistheygrowslowly,maturelate,and lay feweggsper year. The slow reproduction coupledwithhigh costs ofmaintenanceof the species incaptivity(includingcostsforfood,space,electricity,veterinarycareetc.)makesbreedingofmanyturtlesandtortoisesunprofitableonalargecommercialscale.Knowledgeonthereproductivetraitsofaspeciescangiveacrudeestimationonthebiologicallimits,i.e.onthenumberofoffspringthatcanmaximallybeproduced.Ifthedemandexceedsthereproductivepotential, illegal launderingwillbecomemoreprofitableandismorelikelytooccur.Toassessthereproductivepotentialofaspeciessomeresearchandunderstandingintothespecieslifehistoryisnecessary.Sometraitsthatareimportanttoconsiderincludeageatfirstreproduction,clutchsize,lifespan,andinter-birthintervals.Ageatfirstreproduction(also:Ageatsexualmaturity,Ageatmaturity,Ageatfirstoffspring):Theageatwhichanindividualstartsreproducing).Many turtle and tortoise speciesmature late. Desert tortoises for example reachmaturity only after 10-15years. In captivity, some speciesmay attainmaturity earlier than in thewild. The highly traded Indian startortoise(Geocheloneelegans)forexamplemayattainmaturityaround6-7yearsinthewild,butby3yearsincaptivity (D’Cruze et al. 2016). It is therefore unlikely that a facility that has recently been established sellsadultfemalesthatmaturelateproducealargenumberofoffspring.Clutchsize:Averagenumberofeggsperclutch.Testudines can have clutch sizes as little as one egg per clutch up to ~200 eggs per clutch (e.g. 75-123eggs/clutch for the Arrau turtle (Podocnemis expansa; Vanzolini, 2003); 65-193 eggs/clutch for the narrow-headed softshell turtle, (Chitra indica; Das & Singh, 2009). The average number of eggs laid per clutchmultipliedwiththenumberofclutchesaspeciescanlayperyearindicatestheyearlyreproductiveoutputofafemale.Thiscangivearoughestimateofupperlimitofthenumberofoffspringthatafemalecanproduce,butdoesnotconsidereggorhatchlingmortality.Therecruitmentdescribestheactualnumberofhatchlingsthatsurvive,beingamorerealisticmeasureofthenumberofoffspringafemalecanproduce.Maximumlongevity:MaximumnumberofyearsaspeciescanliveMany testudines species are long lived and some can live over a hundred years. Subtracting age at firstreproduction from the maximum longevity can give an upper limit on the number of years a female canreproduce (called thereproductive lifespanof thespecies).However, it is important toconsider thatnotallindividuals survive to the maximum age. In fact, these constitute only a small proportion of the totalpopulation. This is because, of the initial number of individuals being born at a given time (i.e. cohort), thenumberofindividualsstillaliveatdifferentagesdiminishesastimepasses,whichinturnreducesthenumberoffemalescapableofreproducing.Inter-birthintervals:TimebetweenconsecutivebirtheventsInmanyspecies, individualfemalesdonotreproduceeveryyear,particularlyamonglong-livedspecies.Thus,thereproductivepotentialoffemalesofaspeciesthatreproduceeverytwoyearswillbehalfofthatoffemalesofaspecieswithsameclutchsizesandreproductivelifespanbutthatreproduceeveryyear.Forexample,inawildpopulationinthewet-drytropicsofnorthernAustralia,Doodyetal.,2006,recordedthatfemalesofthePig-nosedturtles(Carettochelysinsculpta)layonlyoneeggeverysecondyear.Unfortunately, data on inter-birth intervals is not widely common, therefore it is not yet included in thedatabase. However,we areworking on obtaining this information fromexperts including registered captivebreedersandfieldbiologist.

IMPORTANTNOTE:Thereproductiveoutputinthewildcanonlygiveacrudemeasureonthereproductiveoutputexpectedincaptivityasthesemayvastlydiffer.Somespecieswillnotbeabletoreproduceincaptivityatall,orthetechniquesmaynotyethavebeendeveloped,whereassomespeciesthatcaneasilybefarmedmayreproduceinmuchhighernumbersthaninthewild.Forexample,individualsexperiencehighergrowthrates,whenresourcesareconstantlyavailableundercaptivebreedingconditions.

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ThedatabaseincludesallCITESlistedspeciesofturtlesandtortoises(181):31inAppendixI,130inAppendixII,29inAppendixIII,andoneinAppendixI/III.WematchedtheCITESlistedspecieswiththeIUCNRedList,ofthe191 CITED listed species one is assessed as extinct in thewild (EW), 33 as critically endangered (CR), 35 asendangered (EN), 33 as Vulnerable (VU), 15 as near threatened (NT), 18 as least concern (LC), 4 as datadeficient (DD)and43havenotbeenevaluated (NE).Howevernot forall listed species there is information.Demographicdata isnotavailable forallCITES-listedspecies.Forexample,dataonageat first reproductionwas only available for 31% of all species (55/181), clutch size for 74% of species (133/181) and number ofclutches per year for 38% (71/181) of species. We included data on other demographic variables and thenumberofexportsreportedbytheexporterintheWCMCCITESTradeDatabase(seeTableB.1)How to: Determine whether the species can likely be bred in captivity, given its reproductive potential,information on reproductive traits from the literature and derived from Species360 zoos and aquariumsmember institutions is provided in the Turtles and tortoises demographic traits database for CITES ListedSpecies(https://www.species360.org/serving-conservation/turtles-tortoises-cites/).Methods:To create the Turtles and tortoise’s demographic traits database for CITES Listed species we compiled andstandardized data from: i) existing peer-review databases and ii) from zoo and aquariums members ofSpecies360thatholdturtlesandtortoises.Furthermore,weretrievedthecurrentIUCNRedListStatusandthenumberofexportsofliveanimalsfromtheUNEPWCMCTradeDatabase.Demographicdatafromexistingdatabases:WeuseddatafromourrecentlydevelopeddatabasetogeneratetheSpeciesKnowledgeIndexonDemography(Condeetal.inprep).Forthisdatabasewecompiledandstandardizeddatafromtwodatabasesandtheliterature.Theavailabledatacovers186speciesofturtlesandtortoises(completedatabaseavailableinAppendixC)ofthe344extantspeciesdescribedintheCatalogueOfLife(Roskovetal.,2018).ThedatasourcesincludetheAmnioteLifeHistoryDatabase(Myhrvoldetal.2015),AnAge(DeMagalhaes&Costa2009),whichcompriseanextensiveliteraturesearchondemographicandotherlifehistorytraits.Furthermore,weincludeddatafromGrimmetal.(2014)andShine&Iverson(1995).Therawdataandthereferencestoitareprovidedinthedatabasewithitscorrespondingmetadata. DemographicdataderivedfromSpecies360/ZIMS:We obtained data on reproduction and maximum lifespan from the Species360 Zoological InformationManagement System (ZIMS) (Species360 ZIMS, 2018). Species360 is a Non-Profit Non-Governmental,internationalmemberdriven institutionthatdevelopsandmanages theZoological InformationManagementSoftware(ZIMS).Species360has1,100memberzoosandaquariumsinstitutionsacross96countries,thatsharestandardizedrecordsthroughZIMSfor10millionhistoricallyandlivinganimalsacross21,000species.Foreachspecieswithrecordsformorethan20individuals,weextractedagesatfirstreproduction,maximumlifespan,andmeanyearlyrecruitment(recruitmentisthenumberofnewbornsurvivingbirth/hatching).Weexcludedrecordsforindividualsthatwereeithercontracepted,managedasgroups,thatwereolderthanoneyearwhenenteringZIMS,andthatnevergavebirthintheirlifespan.Fromtheageatfirstreproductionandthemaximumlifespan,wecalculatedthereproductiveperiodofeachspecies:ReproductivePeriod=(Maximumlifespan)–(ageatfirstreproduction).Weusedthemeanoftheobservedyearlyrecruitmentsofaspeciestodeterminethereproductiveoutput.WehighlightthatmostZIMSmembersdonotattempttobreedturtlesandtortoisesinlargenumbers.Wefurtherexpectanunderestimationoftherecruitmentpotentialbecausewedonothaverecordsofbirthcontrol(physicalseparationofsexes).Underestimationoftherecruitmentcanalsobeinducedbyunavailabledataon interbreedingperiods.Ontheotherhand,only reproducinganimalswereconsideredfor thecalculation,whichmayoverestimate reproductiveoutput. Still this information shouldbe takenwithcautionsinceZoosandAquariumsarenotbreeding the species for commercialpurposes.Therefore,weareworking with experts to further expand demographic information from farms and registered commercialbreeders.CITESUNEP-WCMCsummarytradedata:Weextracteddataonexports,reportedbytheexporter,ofliveanimalssince2005percountryanditssourcecodefromtheUNEP-WCMCCITESTradedatabase(UNEP-WCMC,2018) incasethis information isneededtoknowifthespeciesiscommonlyexported.

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Table B.1. Names and description of variables contained in the Turtles and Tortoises demographic traitsdatabaseforCITESListedSpeciesVariablename VariabledescriptionSpecies.name.CITES SpeciesnamesasintheCITESTradeDatabaseSpecies.name.CoL SpeciesnamesaccordingtotaxonomyintheCatalogueofLife(http://www.catalogueoflife.org)Common.name CommonnameasintheCITESTradeDatabaseFamily TaxonomicfamilyasintheCITESTradeDatabase

CITES.AppendixCITES(ConventiononInternationalTradeinEndangeredSpeciesofWildFaunaandFlora)listingappendixin2018(https://www.cites.org/eng)

IUCN.StatusThreatenedcategoryaccordingtotheIUCNRedListassessment(http://www.iucnredlist.org/)version2017-1

AFR.MinimumMinimumageatfirstreproduction,inyearsfrompeer-revieweddatarepositories(seemetadataforthesourceofeachrecord)

AFR.AverageAverageageatfirstreproduction,inyearsfrompeer-revieweddatarepositories(seemetadataforthesourceofeachrecord)

CLY.MinimumMinimumnumberofclutchesperyearfrompeer-revieweddatarepositories(seemetadataforthesourceofeachrecord)

CLY.AverageAverageclutchesperyear,frompeer-revieweddatarepositories(seemetadataforthesourceofeachrecord)

CLY.MaximumMaximumclutchesperyearfrompeer-revieweddatarepositories(seemetadataforthesourceofeachrecord)

CS.MinimumMinimumclutchsizeperreproductiveevent,frompeer-revieweddatarepositories(seemetadataforthesourceofeachrecord)

CS.AverageAverageclutchsizeperreproductiveevent,frompeer-revieweddatarepositories(seemetadataforthesourceofeachrecord)

CS.MaximumMaximumclutchsizeperreproductiveevent,frompeer-revieweddatarepositories(seemetadataforthesourceofeachrecord)

ML.MaximumMaximumlifespanindaysfrompeer-revieweddatarepositories(seemetadataforthesourceofeachrecord)

Nr.IndividualsNumberofindividualsusedtocalculatedemographicdatafromSpecies360ZoologicalInformationManagementSystem(ZIMS)(2017),`.Species360.org.

Nr.Institutions Numberofzoologicalinstitutionfromwhodatawasusedfortheanalysis

ConfidenceLevelofconfidenceofaverageageatfirstreproductionbasedonthenumberofindividuals(<20:VeryLow,21-100:Medium,>101:High)inZIMS.Species360.org.

AFR.ZIMS.AverageAverageageatfirstreproduction,inyearsfromtheSpecies360ZoologicalInformationManagementSystem(ZIMS)(2017),.Species360.org.

AFR.ZIMS.Standard.deviationStandarddeviationofAverageageatfirstreproduction,inyearsfromtheSpecies360ZoologicalInformationManagementSystem(ZIMS)(2017),ZIMS.Species360.org.

ML.ZIMS.MaximumMaximumLifespaninyears(maximumrecordedlifespanfromZIMSdataandfromstandardizedpeer-reviewdatarepositoriesfromCondeetal,inprep)

R.Per.YearNumberofoffspringperyear,fromtheSpecies360ZoologicalInformationManagementSystem(ZIMS)(2017),Species360.org.

R.Per.Year.Standard.deviationNumberofoffspringperyear(Standarddeviation),fromtheSpecies360ZoologicalInformationManagementSystem(ZIMS)(2017),Species360.org.

C,R,F,D Numberofindividualscommerciallyexportedbetween2010and2015fromacaptivesource(sources:C,R,F,D).fromUNEP-WCMCCITESTradeDatabase

C Numberofindividualscommerciallyexportedbetween2010and2015fromacaptive-bredsource(source:C),fromUNEP-WCMCCITESTradeDatabase

R Numberofindividualscommerciallyexportedbetween2010and2015fromaranchedsource(i.e.animalsrearedinacontrolledenvironment,takenaseggsorjuvenilesfromthewild)(source:R),asreportedfromUNEP-WCMCCITESTradeDatabase

F Numberofindividualscommerciallyexportedbetween2010and2015thatwerebornincaptivity(F1orsubsequentgenerationsthatdonotfulfillthedefinitionof"captive-bred,source:F)fromUNEP-WCMCCITESTradeDatabase

D Numberofindividualscommerciallyexportedbetween2010and2015listedinAppendixIas(source:DfromUNEP-WCMCCITESTradeDatabase

W Numberofindividualscommerciallyexportedbetween2010and2015fromawildsource(source:W),fromUNEP-WCMCCITESTradeDatabase

References CITEStradestatisticsderivedfromtheCITESTradeDatabase,UNEPWorldConservationMonitoring

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