The role of Thailand in the international trade in CITES-listed live reptiles and amphibians

Background

International wildlife trade is one of the leading threats to biodiversity conservation. The Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) is the most important initiative to monitor and regulate the international trade of wildlife but its credibility is dependent on the quality of the trade data. We report on the performance of CITES reporting by focussing on the commercial trade in non-native reptiles and amphibians into Thailand as to illustrate trends, species composition and numbers of wild-caught vs. captive-bred specimens.

Methodology/Principal Findings

Based on data in the WCMC-CITES trade database, we establish that a total of 75,594 individuals of 169 species of reptiles and amphibians (including 27 globally threatened species) were imported into Thailand in 1990–2007. The majority of individuals (59,895, 79%) were listed as captive-bred and a smaller number (15,699, 21%) as wild-caught. In the 1990s small numbers of individuals of a few species were imported into Thailand, but in 2003 both volumes and species diversity increased rapidly. The proportion of captive-bred animals differed greatly between years (from 0 to >80%). Wild-caught individuals were mainly sourced from African countries, and captive-bred individuals from Asian countries (including from non-CITES Parties). There were significant discrepancies between exports and imports. Thailand reports the import of >10,000 individuals (51 species) originating from Kazakhstan, but Kazakhstan reports no exports of these species. Similar discrepancies, involving smaller numbers (>100 individuals of 9 species), can be seen in the import of reptiles into Thailand via Macao.

Conclusion/Significance

While there has been an increase in imports of amphibian and reptiles into Thailand, erratic patterns in proportions of captive-bred specimens and volumes suggests either capricious markets or errors in reporting. Large discrepancies with respect to origin point to misreporting or possible violations of the rules and intentions of CITES.     

The trade in bear parts from Myanmar: an illustration of the ineffectiveness of enforcement of international wildlife trade regulations

We assessed the effectiveness of national and international wildlife trade regulations in Asia by surveying four wildlife markets in Myanmar for bears and bear parts. Bears are protected in Myanmar and neighbouring countries, and are included in CITES Appendix I, precluding international trade. Three of the four wildlife markets were situated at the border with neighbouring countries (China and Thailand) whereas the fourth, situated in Myanmar’s interior, also catered to international markets. During seven checks (1999–2006) we recorded 1,200 bear parts, representing a minimum of 215 individual bears. Most items were from Asiatic black bears Ursus thibetanus but also sun bear Helarctos malayanus parts were offered for sale. There were significant temporal and spatial differences in what items were offered for sale. Prices were low (USD 4–40 per item) and the total monetary value of the items for sale was USD 6,500–9,500 (not including gall bladders). Carcasses, skulls, canines, paws, claws, whole skins, pieces of skin, gall bladders and derivates, were openly displayed, with vendors being frank about prices, origin, and potential buyers. Only in the interior were prices quoted in the local currency; at the other three markets currencies of the neighbouring countries were used. Legal (international) trade in bears or bear parts from Myanmar is virtually non-existent, and the observed trade in bear parts strongly indicates a serious lack of enforcement effort. International trade in bear parts from Myanmar is significant, and open, and we conclude that the enforcement of wildlife trade regulations, at least when they concerns bear species, have by and large failed.     

Changes in the trade of bycatch species corresponding to CITES regulations: the case of dried seahorse trade in Thailand

Exploitation for trade is one of the biggest threats to many species, especially for marine fishes. Trade regulations should, therefore, be effective in helping conserve marine fish populations. The Convention of International Trade in Endangered Species of Wild Fauna and Flora (CITES), one of the few multilateral environmental agreements with enforcement capacity, has embraced a number of marine fishes in recent years. However, the impacts of such measures on wildlife trade have rarely been assessed. We conducted a case study of the dried seahorse (Hippocampus spp.) trade in Thailand to understand the trade of these species under CITES regulations. We carried out 203 semi-structured interviews with traders to estimate the economic scale of Thai seahorse trade, and compared perceived changes with official trade datasets. Even though most seahorses were incidentally caught, we estimated that dried seahorses could be worth US$26.5 million per year for Thai fishers. However, the total declared annual export value was only around US$5.5 million, and had decreased to US$1 million in 2013. Considering the economic value of seahorses, the large discrepancy between declared export volumes and catch estimates suggested that trade may be underreported. While official data shows the export volume decreased after the implementation of CITES listing in 2005, our respondents did not report a similar trend. In contrast, the prices of seahorses were reported to be increasing. Our study highlights the economic importance of marine fishes captured as bycatch and the importance of international and domestic management measures for the trade of bycatch species.     

The role of the anthropogenic Allee effect in the exotic pet trade on Facebook in Thailand

The impact of the wildlife trade has been accentuated in the Internet age where social media platforms have offered accessible and consumer-friendly avenues in the way species are legally and illegally traded. We explored the exotic pet trade on a social media platform, Facebook, in Thailand. Over the 18-month period, we recorded 761 posts of primates and carnivores’ species, totalling 1190 individuals from 42 species.Using Generalised Linear Models, we developed hypotheses to explain price dynamics. Variables include, species’ native status (if species are found in Thailand), domestic protection (if species are protected under Thai wildlife laws), international regulation (species CITES listing) and species threatened status (species IUCN Red Listing). Overall, we found evidence of an anthropogenic Allee effect where exotic imports from South America and Africa were significantly more expensive than native species (Wald χ² = 969.72, df = 13, p < 0.05). Trade in these legally imported non-native wildlife species contributed to 11% of posts. Illegal trade of native species contributed to 66% of posts. When considering only native species, trends toward an anthropogenic Allee effect were observed where protected illegal species called for higher prices than legal species.Illegal wildlife trade on Facebook was blatant, easily accessible and unchecked. Discrepancies in current domestic wildlife legislation lead to intentional evasion of laws and a lack of enforcement. Disproportionate desire for rare or protected species encourages a cycle of exploitation that threatens species to extinction.     

Conservation Implications of Rapid Shifts in the Trade of Wild African and Asian Pythons

Pythons are harvested for the international leather industry and pet trade. We analyzed the CITES export records (1999–2008) of the most intensively commercialized wild pythons (Python regius, Python sebae, Python reticulatus, Python molurus, Python curtus species complex) from African and Asian countries where reliable data on trade rates and ecology are available. Mean declared annual numbers of exported pythons were 30,000 in five African countries and 164,000 in Indonesia. Trade intensity tripled in Indonesia over the last decade, but declined in Africa. African international trade is exclusively associated with the pet market (mainly United States and Europe), whereas Asian pythons are sold mostly for luxury leather, albeit more recently also for the pet trade. A negative correlation between the annual numbers of pythons traded in Africa vs. Asia suggests a rapid and recent shift of the pressure exerted on wild populations in the two main exporting continents. We also found a strong effect of the currency exchange rate (i.e., U.S.$/€, the currencies used by the major importing countries) on African python exports: when the cost per African python increased, importers relied increasingly on Asian providers for pet trade. Overall, our data indicate that Asian pythons (especially P. reticulatus) might be threatened due to the rapidly increasing pressure, whereas the decreasing international trade in African pythons is likely more sustainable.     

An overview of international wildlife trade from Southeast Asia

Wildlife trade is the very heart of biodiversity conservation and sustainable development providing an income for some of the least economically affluent people and it generates considerable revenue nationally. In Asia the unsustainable trade in wildlife has been identified as one of the main conservation challenges. Internationally, wildlife trade is regulated through the Convention on International Trade in Endangered Species of wild fauna and flora (CITES) to which all Southeast Asian nations are signatory. I obtained data on international trade in CITES-listed animals in the period 1998–2007. In all >35 million animals (0.3 million butterflies; 16.0 million seahorses; 0.1 million other fish; 17.4 million reptiles; 0.4 million mammals; 1.0 million birds) were exported in this period, 30 million (~300 species) of them being wild-caught. In addition 18 million pieces and 2 million kg of live corals were exported. Malaysia, Vietnam, Indonesia and China are the major exporters of wild-caught animals and the European Union and Japan are the most significant importers. Over this period exports in birds significantly decreased, trade in the other taxa either increased or remained stable. For all taxa but butterflies the vast majority of individuals represent wild-caught individuals. Records of illegal or undeclared international trade are scant but can be significantly larger than levels of official exports. It is concluded that there is an urgent need for better assessments of what levels of exploitation are sustainable (including exploring appropriate proxies for Non Detriment Findings), for initiatives to make regulatory mechanisms more effective (including the introduction of minimum mandatory standards and monitoring selected wildlife trade hubs), and for better licensing and registration. Funding for at least some of these initiatives can be obtained by imposing small levies on exports of CITES-listed wildlife.     

Trends and characteristics of imports of live CITES‐listed bird species into Japan

Understanding the characteristics of the international bird trade is critical for preventing the traffic of endangered species. Japan is the second largest importer of birds for the pet industry globally, yet little research has examined its role in the international trade of live exotic birds. We used reports to the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) Trade Database to conduct the first quantitative analysis of the live commercial bird imports to Japan. We also investigated whether the volume of import is influenced by factors related to species availability. We analysed close to 2 million live bird imports by Japan from 1979 to 2015. The volume of imports peaked in 1999 and then declined until 2008, when imports increased again. Japan imported 603 bird species, mostly parrots (64%), owls (11%) and raptors (9%), from 92 different countries. Most imported birds were reported to be captive‐bred (70%), and key exporters were Belgium (23%), the Netherlands (15%) and Singapore (12%). The most frequently imported bird species had widespread distributions and were not of high conservation concern, so we concluded that bird imports were restricted by the availability of bird species to the international market. Research effort in countries that engage heavily in wildlife trade is necessary to understand the impacts of the trade on bird conservation, and to monitor captive bird populations outside their native ranges.     

Threatened Fishes of the World: Hippocampus comes Cantor1850 (Syngnathidae)

Synopsis Hippocampus comes is presently exploited at significant rates in the central portion of – and possibly throughout – its range. The species is traded in dried form for traditional medicine and alive for the aquarium trade. Here we provide the most current life history, abundance and distribution information available for H. comes. These data should be helpful to researchers, and to management agencies in countries signatory to the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), tasked to implement strategies ensuring that trade is not detrimental to wild populations of H. comes (listed on Appendix II).     

A cryptic invasion within an invasion and widespread introgression in the European water frog complex: consequences of uncontrolled commercial trade and weak international legislation

In Western Europe, many pond owners introduce amphibians for ornamental purposes. Although indigenous amphibians are legally protected in most European countries, retailers are circumventing national and international legislation by selling exotic nonprotected sibling species. We investigated to what extent non‐native species of the European water frog complex (genus Pelophylax) have become established in Belgium, using morphological, mitochondrial and nuclear genetic markers. A survey of 87 sampling sites showed the presence of non‐native water frogs at 47 locations, mostly Marsh frogs (Pelophylax ridibundus). Surprisingly, at least 19% of all these locations also harboured individuals with mitochondrial haplotypes characteristic of Anatolian water frogs (Pelophylax cf. bedriagae). Nuclear genotyping indicated widespread hybridization and introgression between P. ridibundus and P. cf. bedriagae. In addition, water frogs of Turkish origin obtained through a licensed retailer, also contained P. ridibundus and P. cf. bedriagae, with identical haplotypes to the wild Belgian populations. Although P. ridibundus might have invaded Belgium by natural range expansion from neighbouring countries, our results suggest that its invasion was at least partly enhanced by commercial trade, with origins as far as the Middle East. Also the invasion and rapid spread of Anatolian lineages, masked by their high morphological similarity to P. ridibundus, is likely the result of unregulated commercial trade. We expect that Anatolian frogs will further invade the exotic as well as the native range of P. ridibundus and other Pelophylax species elsewhere in Western and Central Europe, with risks of large‐scale hybridization and introgression.     

Is CITES an effective tool for monitoring trade in corals?

 Despite a legal obligation to do so there is a widespread failure to record coral species on CITES trade permits. The complexity of coral taxonomy and the volume of coral specimens in trade mean that in practice this obligation will never be met, and so it may be sensible to ensure that the identification of genera is as accurate as possible. The accuracy of non-specialists in identifying coral genera using four existing guides was tested experimentally. Only three of ten genera were identified to more than 67% accuracy and none of the guides was ideally suited for coral specimens in trade. A guide designed specifically for this purpose and a change in emphasis under CITES to genera rather than species would therefore improve the effectiveness of CITES in monitoring the international coral trade. Accepted: 11 August 1999     

Stable isotope analyses—A method to distinguish intensively farmed from wild frogs

Consumption of frog legs is increasing worldwide, with potentially dramatic effects for ecosystems. More and more functioning frog farms are reported to exist. However, due to the lack of reliable methods to distinguish farmed from wild‐caught individuals, the origin of frogs in the international trade is often uncertain. Here, we present a new methodological approach to this problem. We investigated the isotopic composition of legally traded frog legs from suppliers in Vietnam and Indonesia. Muscle and bone tissue samples were examined for δ¹⁵N, δ¹³C, and δ¹⁸O stable isotope compositions, to elucidate the conditions under which the frogs grew up. We used DNA barcoding (16S rRNA) to verify species identities. We identified three traded species (Hoplobatrachus rugulosus, Fejervarya cancrivora and Limnonectes macrodon); species identities were partly deviating from package labeling. Isotopic values of δ¹⁵N and δ¹⁸O showed significant differences between species and country of origin. Based on low δ¹⁵N composition and generally little variation in stable isotope values, our results imply that frogs from Vietnam were indeed farmed. In contrast, the frogs from the Indonesian supplier likely grew up under natural conditions, indicated by higher δ¹⁵N values and stronger variability in the stable isotope composition. Our results indicate that stable isotope analyses seem to be a useful tool to distinguish between naturally growing and intensively farmed frogs. We believe that this method can be used to improve the control in the international trade of frog legs, as well as for other biological products, thus supporting farming activities and decreasing pressure on wild populations. However, we examined different species from different countries and had no access to samples of individuals with confirmed origin and living conditions. Therefore, we suggest improving this method further with individuals of known origin and history, preferably including samples of the respective nutritive bases.     

The dynamics of trade in live wildlife across the Guangxi border between China and Vietnam during 1993–1996 and its control strategies

A survey on trade in live wild animals was conducted along the Guangxi border between China and Vietnam during 1993–1996. The results showed that there were 55 species, which were underestimated, involved in the trade, including 15 species of mammals, 10 species of birds, 29 species of reptiles and 1 species of amphibian. Many of them were species listed on Appendices I and II of CITES and on China's protection list (known as ASSP). During the investigation, about 2.29–29.325 tons of wildlife per day were imported to China form Vietnam. Some species with a large volume of trade may be over-exploited. Sixty-three percent of middle–high quality restaurants in three border cities and Nanning in Guangxi sold wildlife foods. Twenty kinds of wild animals were eaten at the restaurants. Although numbers of species involved in the trade remained fairly stable over the survey period, numbers of species listed in Appendices I and II of CITES and the state protection list had declined. The scale of wildlife markets in border cities of Guangxi and consumption levels of wildlife in the restaurants had been reduced because border control measures were enforced on the trade by local governments of China. However, the prices of the 5 main species in wildlife markets were still going up. This suggested that demand for wildlife in Guangxi was strong and will facilitate the illegal trade. The key steps to control the illegal wildlife trade between the two countries should focus on (i)suppression of illegal wildlife markets and prohibition of the sale of wildlife food in restaurants consisting of species listed in the ASSP inventory; (ii) international cooperation in the control of the trade; (iii) tighter enforcement of CITES for both countries; (iv) control of invasion of exotic species and epidemics of disease in the trade in China; and (v) education for wildlife conservation in China.     

Patterns of species discovery in the Western Ghats,a megadiversity hot spot in India

Even since Linnaeus, naturalists and taxonomists have been systematically describing species new to science. Besides indicating gaps in taxonomic effort, understanding the temporal patterns of species discovery could help in identifying drivers that determine discovery. In this study we report the patterns of discovery of eight taxa — birds, butterflies, frogs, tiger beetles, grasses, asters, ferns and orchids — in the Western Ghats, a megadiversity centre in India. Our results indicate that the discovery curves for birds and butterflies have been saturated while those for frogs and grasses continue to increase. Within each taxon, the major drivers of discovery were commonness of the species and their size. The average years taken for discovery across taxa were directly related to the per cent endemicity and species richness of the taxa. We discuss the trajectories of discovery with respect to rarity or endemicity of the species and life history features, and the implications these might have for strategizing the discovery process in India.     

Preventing horticultural introductions of invasive plants: potential efficacy of voluntary initiatives

Although prevention is the most cost-effective way to avoid the enormous expenses associated with plant invasions, invasive plants continue to be imported as trade commodities for horticultural use. With very little government regulation of horticultural imports of invasive plants, efforts have turned toward fostering voluntary initiatives to encourage self-regulation by the horticulture trade. Our study takes the first step toward evaluating the potential success of these voluntary initiatives. We conducted a survey of nursery professionals to gauge their perceptions of invasive species, the role of the horticulture trade in invasive plant introductions, and their participation—potential and actual—in preventive measures outlined in the St Louis Voluntary Codes of Conduct for nursery professionals. We found nursery professionals to be highly aware of invasive plants and to accept responsibility as a trade for horticultural introductions. Although only 7% of respondents had heard of the St Louis Voluntary Codes of Conduct, the majority (57%) reported having participated in at least two of seven preventive measures, and most (78%) reported willingness to engage in the majority of preventive measures. We found that several factors significantly predict increased participation in preventive measures, particularly awareness of invasive plants and involvement in trade associations. We also identified incentives and obstacles to participating in preventive behaviors, including “concern for the environment” and “lack of information,” respectively. Our results suggest that participation in voluntary initiatives will improve through increased outreach, and we provide specific recommendations for improving participation in voluntary programs in the horticulture trade.     

The Homing Frog: High Homing Performance in a Territorial Dendrobatid Frog Allobates femoralis (Dendrobatidae)

Dendrobatidae (dart‐poison frogs) exhibit some of the most complex spatial behaviors among amphibians, such as territoriality and tadpole transport from terrestrial clutches to widely distributed deposition sites. In species that exhibit long‐term territoriality, high homing performance after tadpole transport can be assumed, but experimental evidence is lacking, and the underlying orientation mechanisms are unknown. We conducted a field translocation experiment to test whether male Allobates femoralis, a dendrobatid frog with paternal extra‐territorial tadpole transport, are capable of homing after experimental removal, as well as to quantify homing success and speed. Translocated individuals showed a very high homing success for distances up to 200 m and successfully returned from up to 400 m. We discuss the potential orientation mechanisms involved and selective forces that could have shaped this strong homing ability.     

A Novel Mini-DNA Barcoding Assay to Identify Processed Fins from Internationally Protected Shark Species

There is a growing need to identify shark products in trade, in part due to the recent listing of five commercially important species on the Appendices of the Convention on International Trade in Endangered Species (CITES; porbeagle, Lamna nasus, oceanic whitetip, Carcharhinus longimanus scalloped hammerhead, Sphyrna lewini, smooth hammerhead, S. zygaena and great hammerhead S. mokarran) in addition to three species listed in the early part of this century (whale, Rhincodon typus, basking, Cetorhinus maximus, and white, Carcharodon carcharias). Shark fins are traded internationally to supply the Asian dried seafood market, in which they are used to make the luxury dish shark fin soup. Shark fins usually enter international trade with their skin still intact and can be identified using morphological characters or standard DNA-barcoding approaches. Once they reach Asia and are traded in this region the skin is removed and they are treated with chemicals that eliminate many key diagnostic characters and degrade their DNA (“processed fins”). Here, we present a validated mini-barcode assay based on partial sequences of the cytochrome oxidase I gene that can reliably identify the processed fins of seven of the eight CITES listed shark species. We also demonstrate that the assay can even frequently identify the species or genus of origin of shark fin soup (31 out of 50 samples).     

Selection of radio transmitter and attachment method for post-release monitoring of captive-bred reintroduced Red-billed Curassow Crax blumenbachii, Brazil

Long-term monitoring of reintroduced individuals is a central component of many endangered species reintroduction programs. Radio-telemetry techniques are rarely used to monitor reintroduced captive-bred Cracids and few data exist regarding possible adverse effects of radio-tagging Cracids. In this study, we identify an appropriate radio transmitter design and develop a suitable attachment method that minimizes anthropogenic influence and enables long-term, post-release monitoring (2–3 years) of reintroduced captive-bred Red-billed Curassows in the Brazilian Atlantic Rainforest. We also review studies about the effects of different VHF radio transmitter models on survival, reproduction, behavior, and physiology of Galliformes.     

Forensic genetic identification of sturgeon caviars traveling in world trade

Caviar is among the world’s most valuable wildlife products. Exploitation of sturgeon and paddlefish for the caviar trade has severely reduced abundance, and harvest of most species is regulated under CITES. International trade requires that importing nations verify the species source of caviars they receive; the US domestic trade has no such requirement. We report the results of forensic species identifications of US caviar imports from 1998 to 2008 and of US domestic market caviars from 1997 to 1998. Twelve species were identified overall and species origins were mislabeled three times as often among US domestic market caviars (14.7 %) as among imports (4.9 %). Industry practices associated with the re-packaging of caviars for domestic markets and re-export from intermediate countries have created opportunities for the co-mingling of legitimate caviars with those from illegal, unreported and unregulated sources.     

Floral fragrances in two closely related fruit fly orchids,Bulbophyllum hortorum and B. macranthoides (Orchidaceae): assortments of phenylbutanoids to attract tephritid fruit fly males

Floral chemical components are important cues used by plants to attract pollinators. One outstanding case is “fruit fly orchids” in the genus of Bulbophyllum to attract their pollinators by releasing characteristic fragrances. Dacini fruit flies are main or exclusive pollinators which are strongly attracted to certain natural chemicals, either methyl eugenol (ME: a phenylpropanoid) or raspberry ketone (RK: a phenylbutanoid). Furthermore, zingerone (ZN: a phenylbutanoid) has been characterized as the attractant for both ME- and RK-sensitive fruit fly species. In the present study, we examined chemical profiles of two closely related Bulbophyllum orchids—B. hortorum, and B. macranthoides subsp. tollenoniferum—distributed in Papua New Guinea and the Southeast Asian countries, respectively. We first observed that RK-sensitive flies were attracted to these orchids by ex situ cultivation in Penang, Malaysia. These Bulbophyllum orchids contained RK and/or ZN as their main floral components. Other than these attractants, multiple phenylbutanoids including potential attractants for RK-sensitive species were identified from these orchids. Therefore, we examined attractiveness of potential phenylbutanoid attractants to an RK-sensitive melon fly, Zeugodacus cucurbitae, using laboratory-reared flies. Furthermore, we analyzed molecular phylogenetic relationships among phenylpropanoid- or phenylbutanoid-producing orchids to see a relation between chemical profiles and phylogenetic classification in the related species.     

Poison frogs rely on experience to find the way home in the rainforest

Among vertebrates, comparable spatial learning abilities have been found in birds, mammals, turtles and fishes, but virtually nothing is known about such abilities in amphibians. Overall, amphibians are the most sedentary vertebrates, but poison frogs (Dendrobatidae) routinely shuttle tadpoles from terrestrial territories to dispersed aquatic deposition sites. We hypothesize that dendrobatid frogs rely on learning for flexible navigation. We tested the role of experience with the local cues for poison frog way-finding by (i) experimentally displacing territorial males of Allobates femoralis over several hundred metres, (ii) using a harmonic direction finder with miniature transponders to track these small frogs, and (iii) using a natural river barrier to separate the translocated frogs from any familiar landmarks. We found that homeward orientation was disrupted by the translocation to the unfamiliar area but frogs translocated over similar distances in their local area showed significant homeward orientation and returned to their territories via a direct path. We suggest that poison frogs rely on spatial learning for way-finding in their local area.