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ORI GIN AL PA PER

Exploited for pets: the harvest and trade of amphibiansand reptiles from Indonesian New Guinea

Daniel J. D. Natusch • Jessica A. Lyons

Received: 5 December 2011 / Accepted: 23 July 2012! Springer Science+Business Media B.V. 2012

Abstract Over-exploitation of wildlife is a significant threat to global biodiversity, butaddressing the sustainability of harvests can be difficult when trade is conducted illegally.The wildlife trade is driven chiefly by consumer demand, largely in developed nations (butincreasingly in Asia), and more species are traded to meet international demand for petsthan for any other purpose. We surveyed traders of amphibians and reptiles in the Indo-nesian provinces of Maluku, West Papua and Papua between September 2010 and April2011. We recorded 5,370 individuals representing 52 species collected solely for the pettrade. At least 44 % were either fully protected or had not been allocated a harvest quota,making their harvest and trade illegal. Approximately half were listed within the Con-vention on International Trade in Endangered Species of Wild Fauna and Flora. Tradeoperates via a complex chain, with hunters receiving little income compared to middlemenand exporters. Examination of Indonesian harvest quotas for amphibians and reptilessuggests limited knowledge of species distributions, with quotas often set for species inprovinces where they do not occur. Illegal trade is due, partly, to an inadequate under-standing of the species being traded and is facilitated by poor monitoring and enforcementat key trade hubs. As a first step to combatting illegal trade, and to better understand theeffects of harvest on wild populations, we recommend the need for increased monitoringand enforcement, improving the knowledge base of species traded and educating con-sumers about the effects their demand for pets has on these species.

Keywords Biodiversity ! CITES ! Exotic pets ! Herpetofauna ! Illegal wildlife trade !Monitor ! Python

D. J. D. Natusch (&) ! J. A. LyonsSchool of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney,NSW 2052, Australiae-mail: d_natusch_14@hotmail.com

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Introduction

The global decline in amphibians and reptiles is fast becoming a major concern for con-servationists (Gibbons et al. 2000; Stuart et al. 2004; Pimenta et al. 2005; McCallum 2007;Sodhi et al. 2008; Reading et al. 2010) and parallels declines in other vertebrate groups(King et al. 2008; Schipper et al. 2008). Several factors have been suggested for thesedeclines viz: habitat loss and degradation (Brooks et al. 2002), disease and parasitism(Berger et al. 1998; Daszak et al. 2003), environmental pollution (Dunson et al. 1992),introduced species (Adams 1999), global climate change (Pounds and Crump 1994; Poundset al. 1999; Reading et al. 2010) and over-exploitation (Gibbons et al. 2000; Oza 1990).Because many of these threatening processes are poorly understood, finding solutions isoften difficult, but without remediation, further declines, extirpations and extinctions willoccur (Gibbons et al. 2000). Conversely, one threatening process, over-exploitation,appears relatively straightforward to correct—simply stop exploiting. However, harmonybetween human needs and sustaining viable populations of species is difficult to achieveand the trade in amphibians and reptiles remains a significant global threatening processwith many well documented declines (Nilson et al. 1990; O’Brien et al. 2003; Zhou andJiang 2004; Shepherd and Ibarrondo 2005; Eisemberg et al. 2011).

Southeast Asian countries rank among the world’s leading nations for exportation ofwildlife and wildlife products (Nash 1993; Sodhi et al. 2004; Grieser-Johns and Thomson2005; Nijman 2010). One group, the tortoises and freshwater turtles, has experienceddrastic declines in the populations of several species due to commercial trade (van Dijket al. 2000). This has been dubbed the ‘‘Asian Turtle Crisis’’ and it is noted that the trade inAsian snakes is fast becoming another crisis (CITES Asian Snake Trade Workshop 2011).Much of the trade in amphibians and reptiles is from Indonesia, the world’s largestarchipelago, and due to its megadiversity status and lack of effective enforcement, Indo-nesia has become an epicentre for illegal wildlife trade (Sodhi et al. 2004; Davies 2005;Shepherd 2010; Nijman 2010). While the Indonesian reptile trade for skins, medicines andmeat has been relatively well studied in a few nominate species (Shine et al. 1999a, b;Shepherd 2000; Auliya 2006; Auliya 2010), the growing harvest of wild amphibians andreptiles for pets includes hundreds of species, but with the exception of Yuwono’s (1998)review, is only recently receiving attention (Shepherd and Nijman 2007; Lyons andNatusch 2011; Natusch and Lyons 2012a; b; Lyons et al. in press).

Many of the amphibian and reptile species collected for the pet trade originate from Indo-nesian New Guinea (Yuwono 1998). Not surprisingly, our understanding of the biology andtrade of many species inhabiting such remote provinces is poor (Burnett 2007), which presentschallenges when attempting to assess the risk of the pet trade to local populations. Nevertheless,several authors have already identified the potential risk of the pet trade to New Guinea’samphibian and reptile species (Allison 2007a; Frazier 2007; Lyons and Natusch 2011). Here wepresent data on the harvest and trade of amphibians and reptiles in the Indonesian provinces ofMaluku, West Papua and Papua. We examine the trade dynamic and trends, discuss issues ofillegality and sustainability and offer recommendations to improve the conservation of theunique herpetofauna of Indonesian New Guinea.

Materials and methods

We visited 15 wildlife traders in the Indonesian provinces of West Papua, Papua and Maluku’sAru Islands (referred to collectively hereafter as New Guinea) between September 2010 and

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April 2011 (Fig. 1). Survey sites were grouped into five geographic regions and selected basedupon the position of major towns, cities and/or seaports, and therefore areas where trade inwildlife was suspected to occur. We identified wildlife traders using a snowball samplingmethod, whereby traders identify other traders within the trade chain (Bryman 2004). Weconducted semi-structured surveys with traders, with questions relating to the trade chain andtrade dynamics. Finally, we gathered data on the number of each species observed in trade. Weidentified species on site; however, a small number of individuals were later confirmed fromphotographs. Two species could not be identified due to our inability to determine diagnosticcharacters. Data relating to the annual harvest quotas for species listed within the appendices ofthe Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES)and those not listed were examined for each province (Anonymous 2011). We obtained data onthe distribution (range) of quota-listed species from published records (O’Shea 1996; Allison2007b).

Legislation

Indonesia became a party to CITES in 1979, meaning that the trade in Indonesian CITES-listed wildlife is internationally monitored and regulated. Harvests of CITES-listed species

Fig. 1 Sites visited in the Indonesian provinces of Maluku (Aru Islands), West Papua and Papua (separatedby the dashed line) and the final destinations of traded wildlife (insert box)

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are regulated by quotas set by the nominated CITES Scientific Authority, the IndonesianInstitute of Sciences (LIPI), and implemented by the nominated CITES ManagementAuthority, the Directorate General of Forest Protection and Nature Conservation (PHKA).A small number (31) of Indonesian amphibian and reptile species are fully protected undernational legislation and cannot be harvested from the wild (Dilindungi PP No. 7/1999). Fortraded species that are non-protected, quotas are set on an annual basis via a meeting ofvarious stakeholders including PHKA, LIPI, relevant non-government organizations andlicensed wildlife traders (PP No. 8/1999). Hunters and traders require permits for cap-turing, transporting and selling wildlife within Indonesia (Decree of the Ministry of For-estry No. 447/Kpts-11/2003) and must be registered with regional offices of the NaturalResources Conservation Agency (BKSDA), responsible for the regulation of wildlife tradeat the provincial level. Only those species that have an allotted harvest quota can beharvested from the wild for local sale or export, and these quotas only allow harvest fromeach designated province.

Results

Numbers and species composition

We recorded 5,370 amphibians and reptiles representing 52 species during surveys(Table 1). The greatest number of individuals and species were collected from the wild inthe vicinity of Merauke in southern Papua province, but many species were also collectednear to Sorong on the Vogelkop Peninsula (Fig. 1). Collection was mostly opportunistic;however, some species are targeted specifically because they fetch very high prices (e.g.,Morelia boeleni) or are particularly abundant (e.g., Litoria caerulea). Forty eight percentof the species recorded were CITES-listed (Table 1). Trade appeared to be focused onpython and monitor species, which accounted for 45 % of trade. All species were collectedfor both the domestic and international pet trades. Seventeen percent of the species collectedare fully protected in Indonesia and at least 44 % did not have an allocated harvest quota(Table 1), making their collection and trade illegal. Interestingly, 73 % (11/15) of tradersindicated that some species (e.g., Morelia viridis, M. boeleni) had become particularlyscarce due, in part, to over-collection as well as habitat loss at historic collection sites.

Trade chain

The wildlife trade in New Guinea is carried out by a chain of actors who collect, buy,transport, and on-sell animals. Three common scenarios are illustrated in Fig. 2 and theiruse is determined largely by transport distances. Trade in protected species, or thosewithout harvest quotas, is facilitated either by concealing them within shipments of legallyharvested species or by provision of rewards to officials and transport providers. Tradersclaimed that all wildlife collected was destined for licenced breeding farms in Jakarta orBali, where animals are either exported (as captive-bred for protected species, see ‘‘Dis-cussion’’) or sold to pet shops for the domestic pet trade (Fig. 2). We also observed largenumbers of reptiles that were unable to be exported due to injury and death (particularlymonitors and turtles) resulting from improper husbandry at various stages along the tradechain.

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Table 1 Numbers of each species traded in the Aru Islands, Biak, Jayapura, Merauke, and the Vogelkop,their CITES listing (CL), protection status in Indonesia (Pr) and annual harvest quotas for West Papua (WP)and Papua (P)

Species Aru Biak Jaya Mer Vog Total CL P Quota

Boidae

Candoia aspera 0 0 15 0 44 59 Yes No 500(P), 800(WP)

Candoia carinata 0 0 16 3 83 102 Yes No 400(P), 400(WP)

Pythonidae

Antaresia maculosa 0 0 0 4 0 4 Yes No No quota

Apodora papuana 0 0 15 0 9 24 Yes No 100(P), 200(WP)

Leiopython albertisii 0 0 34 0 77 111 Yes No 200(P), 300(WP)

Leiopython biakensis 0 2 0 0 0 2 Yes No No quota

Leiopython hoserae 0 0 0 5 4 9 Yes No No quota

Morelia amethistina 0 0 21 62 14 97 Yes No 200(P), 100(WP)

Morelia boeleni 0 0 40 0 0 40 Yes No No quota

Morelia spilota 0 0 0 247 0 247 Yes No 200(P), 200(WP)

Morelia viridis 123 1,025 70 29 176 1,423 Yes Yes No quota

Colubridae

Boiga irregularis 0 0 0 33 0 33 No No 500(P)

Stegonotus dielhi 0 0 0 0 2 2 No No No quota

Elapidae

Acanthophis laevis 0 0 0 13 0 13 No No No quota

Acanthophis praelongus 0 0 0 4 0 4 No No No quota

Micropechis ikaheka 0 0 0 0 4 4 No No 100(P), 100(WP)

Oxyuranus scutellatus canni 0 0 0 2 0 2 No No 350(WP)

Pseudechis papuana 0 0 0 1 0 1 No No 200(P), 200(WP)

Varanidae

Varanus beccarii 31 0 0 0 0 31 Yes No No quota

Varanus boehmei 0 0 0 0 2 2 Yes No No quota

Varanus panoptes horni 0 0 0 41 0 41 Yes Yes No quota

Varanus doreanus 0 0 3 40 24 67 Yes No 200(P), 400(WP)

Varanus indicus 0 4 36 0 15 55 Yes Yes No quota

Varanus jobiensis 0 0 0 0 3 3 Yes No 200(P), 300(WP)

Varanus kordensis 0 1 0 0 0 1 Yes No No quota

Varanus macraei 0 0 0 0 79 79 Yes No No quota

Varanus prasinus 0 0 11 3 52 66 Yes Yes No quota

Varanus reisingeri 0 0 0 0 6 6 Yes No No quota

Varanus salvadorii 0 0 2 4 22 28 Yes No 150(P), 150(WP)

Varanus similis 0 0 0 83 0 83 Yes No No quota

Agamidae

Chlamydosaurus kingii 0 5 0 19 0 24 No Yes No quota

Hypsilurus sp. 0 0 0 11 0 11 No No Unknown

Hypsilurus dilophus 0 0 0 2 1 3 No No No quota

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Harvest quotas and species distributions

Examination of Indonesian harvest quotas for the year 2011 revealed that 21 species(Table 2) allocated harvest quotas for the provinces of both Papua and West Papuaoccurred only in Papua (Anonymous 2011). This was particularly true for species thatoriginated from New Guinea’s Trans-Fly region (72 % of species in Table 2). In addition,Emydura subglobosa, Furina tristis and Liasis fuscus were allocated harvest quotas forWest Papua only but do not occur in that province. Demansia olivacea is yet to be recordedfrom New Guinea (Table 2). Examination of quotas also revealed inadequate knowledge ofrecent taxonomic changes so that more than one species is traded under the same name andothers under older synonyms. This creates a loophole for the trade of species withoutquotas.

Table 1 continued

Species Aru Biak Jaya Mer Vog Total CL P Quota

Pygopodidae

Lialis burtonis 0 0 0 44 0 44 No No 1,000(P), 1,000(WP)

Lialis jicari 0 0 0 15 0 15 No No 1,000(P), 1,000(WP)

Gekkonidae

Cyrtodactylus sp. 0 0 0 0 31 31 No No Unknown

Gehyra sp. 0 0 0 0 19 19 No No Unknown

Scincidae

Bellatorias frerei 0 0 0 3 0 3 No No 1,000(P), 1,000(WP)

Ctenotus spaldingii 0 0 0 2 0 2 No No No quota

Tiliqua gigas 0 0 0 0 1 1 No Yes No quota

Tiliqua scincoides 0 0 0 559 0 559 No No 1,000(P), 1,500(WP)

Tribolonotus gracilis 0 0 0 0 49 49 No No 1,000(P), 1,500(WP)

Carettochelyidae

Carettochelys inscapulata 0 0 0 0 5 5 Yes Yes 40(P)

Chelidae

Chelodina parkeri 0 0 0 40 0 40 No No 150(P), 150(WP)

Chelodina reimanni 0 0 0 15 0 15 No No 100(P), 100(WP)

Chelodina(Macrochelodina) rugosa

0 0 0 73 0 73 No No 1,000(P), 1,000(WP)

Elseya branderhorsti 0 0 0 18 0 18 No No No quota

Myuchelys novaeguineae 0 0 0 20 0 20 No Yes 500(P), 500(WP)

Emydura subglobosa 0 0 0 98 0 98 No No 500(P), 500(WP)

Crocodylia

Crocodylus novaguineae 0 0 0 0 3 3 Yes Yes No quota*

Hylidae

Litoria caerulea 0 0 0 1,692 0 1,692 No No 50,000(P), 25,000(WP)

Litoria infrafrenata 0 0 0 6 0 6 No No 40,000(P), 5,000(WP)

Total 154 1,037 263 3,191 725 5,370

* Crocodylus novaguineae has a harvest quota for skins, but not for pets

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Discussion

Although trade in many of the species observed in this study was legal and possiblysustainable, large numbers are traded illegally and many are range restricted island en-demics, suggesting they may be more susceptible to over-exploitation. Illegal trade inwildlife in Indonesia has been relatively well documented (Shepherd 2007; Schoppe 2009;Shepherd 2010; Nijman et al. 2012). However, studies of the trade in reptiles andamphibians focus primarily on export and market volumes and provide little informationabout primary harvests (Pernetta 2009; Yuwono 1998; but see WWF 1998; Suryadi et al.2004), particularly from remote areas such as New Guinea.

Due to the clandestine nature of illegal trade, and the lack of basic biological data formany of the species traded, determining the impact of trade on wild populations is difficult(Gavin et al. 2010; Schoppe 2009). However, the large harvests recorded (e.g., L. caeruleaand M. viridis), coupled with anecodotal evidence of species declines, suggest that theongoing harvest and trade of selected species for pets may be detrimental to wild popu-lations. Lyons and Natusch (2011) found that this trade had already impacted upon islandpopulations of M. viridis. Many of the species observed in the present study have similarlyrestricted distributions (M. boeleni, Varanus boehmei, V. macraei), which may make themparticularly vulnerable to over-collection (Dodd 1993; Purvis et al. 2000). Unsustainableharvests of other Indonesian species has resulted in large declines (van Balen et al. 2000;Cahill et al. 2006)—specifically those collected for the pet trade (Shepherd and Ibarrondo2005; Shepherd 2007).

Although there are regulations and guidelines in place in Indonesia to regulate the tradein wildlife, few actors abide by these laws. Because many species are poorly known byIndonesian authorities they can be easily mis-labeled and thus traded openly (Lyons and

Fig. 2 Three scenarios for the trade chain allowing amphibians and reptiles collected in New Guinea toreach the consumer market. Scissor and aeroplane symbols indicate where wildlife is sent from New Guineaby plane to Jakarta, and therefore where targeted enforcement can take place

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Natusch 2011; Natusch and Lyons 2011). A report submitted by Indonesia at the CITESAsian Snake Trade Workshop (2011) claimed that there was no illegal trade in Indonesiansnakes (PHKA 2011). However, recent seizures in consumer countries of snakes fromIndonesia, as well as observations of trade in various locations throughout Indonesia, tell adifferent story. At breeding facilities, protected species can be easily disguised by laun-dering them under the guise of being captive-bred (Nijman and Shepherd 2009; Lyons andNatusch 2011), and many of the protected species observed in the present study arelaundered in a similar fashion.

The harvest quotas published by PHKA suggests that there is limited knowledge aboutspecies distributions and about many traded species in general. For example, the authors werepresent at a trader’s premises during inspections by BKSDA officers while protected species,and those without harvest quotas, were packed to be shipped to Jakarta. Despite BKSDAofficers observing protected species included within the shipment, their limited species iden-tification skills allowed traders to send animals merely as colour variants of other species.

New Guinean villagers receive a very small proportion of the final sale value foramphibians and reptiles, despite the relatively high price many species demand in theinternational pet trade. This provides little incentive for local people to sustainably harvestthese species or protect the habitats in which they live. Moreover, when trade is conducted

Table 2 Reptile and amphibianspecies allocated harvest quotasby PHKA for the provinces ofWest Papua (WP) and Papua(P) and their currently knowndistributions

Species PHKAallocatedharvest area

Actualdistribution

Amphibians

Litoria caerulea WP, P P

Litoria nasuta WP, P P

Reptiles

Bellatorias frereri WP, P P

Chelodina parkeri WP, P P

Chelodina reimanni WP, P P

Demansia olivacea WP, P Australia

Demansia vestigiata WP, P P

Dendrelaphis punctulatus WP, P P

Emydura subglobosa WP P

Furina tristis WP P

Lialis burtonis WP, P P

Lialis jicari WP, P P

Liasis fuscus WP P

Chelodina (Macrochelodina) rugosa WP, P P

Morelia spilota WP, P P

Oxyuranus scutellatus canni WP, P P

Pelochelys signifera WP, P P

Pseudechis australis WP, P P

Pseudechis papuanus WP, P P

Cryptophis nigrostriatus WP, P P

Tiliqua scincoides WP, P P

Tribolonotus gracilis WP, P P

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illegally, sustainable harvests and community based conservation initiatives can beundermined. Thus, if Indonesia is indeed serious about conserving its unique herpetofaunaldiversity, then immediate action needs to be taken to combat illegal trade. Here we providea number of recommendations in the hope that they may help to increase the transparencyof the trade in live Indonesian amphibians and reptiles.

Better monitoring and enforcement

Increased monitoring of harvests and exports is needed to ensure that quotas are notexceeded and illegal collection is reduced. In an attempt to prevent the laundering ofreptiles through Indonesian breeding farms, Lyons and Natusch (2011) proposed that thesize and shape of reptile eggshells may be used to differentiate between species beingexported. This could be implemented easily and cost effectively, and monitored byauthorities in both the exporting and importing countries. Merely the requirement toenclose eggshells within shipments (and not even counting them) would curtail much ofthis trade because many Indonesian farms do not have the capacity to breed even smallnumbers of these species (Nijman and Shepherd 2009; Lyons and Natusch 2012).

Illegal trade is currently operated openly, allowing wildlife to be traded in largenumbers. While complete cessation of illegal harvests is unlikely to occur in the short term,effective monitoring, and particularly enforcement, at all levels of the trade chain mayreduce the number of animals able to be collected, traded and transported covertly,therefore reducing detrimental impacts on wild populations. A number of general rec-ommendations for strengthening environmental enforcement in Papua are reviewed bySuryadi et al. (2007). However, because the vast majority of wildlife exports from Indo-nesian New Guinea pass through Jakarta’s Soekarno Hatta Airport, targeted enforcement atthis, and other regional trade hubs, may help to prevent much of the current trade (Fig. 2).Finally, listing many of the species collected from New Guinea in the appendices of CITESwould allow the Indonesian authorities to engage the international community to assist inmonitoring exports and enforcing regulations.

Species identification

The descrepancies between government allocated harvest areas and the actual naturalranges of many species in this study prompts a thorough review of Indonesian harvestquotas, particularly in New Guinea (Table 2). In addition, it highlights the need for a betterunderstanding of current taxonomy. Production of a photographic guide, in BahasaIndonesian, to the amphibians and reptiles of Maluku, West Papua and Papua should bemade available to PHKA, LIPI and all regional offices of BKSDA (cf. Auliya 2007).Ideally, such a booklet would be updated with important changes and regular training in itsuse would be provided to all relevant personnel. Information on diagnostic characteristics,distributions, basic biology, CITES listing and protection status would enable moreeffective monitoring by Indonesian authorities.

Exploring proxies for traditional non-detriment findings

According to Article IV of CITES, non-detriment findings (NDF) should have beenundertaken for all Appendix II listed species before a harvest quota can be allocated.A NDF should determine aspects of a species distribution, biology as well as population

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and trade status to inform decisions about the potential for trade to negatively affect wildpopulations. It appears that in New Guinea, and indeed other areas of Indonesia (Nash1993; Iskandar and Erdelen 2006), adequate NDFs have not been undertaken for manyspecies. The poor knowledge of species distributions by Indonesian authorities, as illus-trated in the present study, reiterates this (Table 2). However, collecting population dataoften required for a NDF, independently in the field, can be truly daunting logistically andmay not be worthwhile in the long-term (Nash 1993). Alternatively, Indonesian authoritiescould easily gather basic biological data from species collected for the pet trade. This hasalready been achieved, in part, for a number of Indonesian reptiles in trade (Shine et al.1999a; b; Natusch and Lyons 2012a; b; Lyons et al. in press; Natusch and Lyons in press).Nijman (2010) suggested that funding for such studies could be procured through smalllevies on exports of CITES-listed species. In addition, we suggest that Indonesianauthorities should consider promoting the study of traded species to domestic and foreignstudents and herpetologists so that ecological knowledge may be accrued to inform futureconservation management of these species.

Consumer education

The uniquness of New Guinean amphibians and reptiles creates high demand for them onthe international market for pets. Because consumer demand drives this trade, consumersneed to be educated about the potentially negative impacts their purchasing decisions haveon the very species they appreciate. Increasingly, conservation managers may wish toconsider using alternative media (social networking sites, popular reptilian keeper maga-zines) to illuminate the issue of illegal wildlife trade. While Indonesia has the right toutilise its biological resources, if biodiversity in this megadiverse region is to be conserved,alternative means of reducing illegal trade may wish to be considered. Ultimately, becausethe international market determines demand, if it is deemed that wildlife is harvestedillegally or has not received satisfactory NDFs, importing nations have the opportunity toban imports of certain species. Without amelioration of the high demands of consumernations, and adequate monitoring and protection by Indonesian authorities, illegal (andpotentially legal) over-exploitation will continue to be a significant threat to the uniqueamphibian and reptile fauna of Indonesian New Guinea.

Acknowledgments We thank the Indonesian traders and villagers who accommodated us over the courseof our studies. Thanks also to A. Allison and F. Kraus for their assistance in identifying specimens fromphotographs and C. Shepherd and M. Auliya for comments that improved an earlier version of thismanuscript.

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