Southeast Asia is currently the centre of the amphibian trade as food for human consumption

Regulations and restrictions on the amphibian pet trade would provide safer conditions for both humans and wildlife. These recommendations resonate well with ethics in civil societies around the world . For instance, following the implementation of the wildlife trade ban in China, a questionnaire was developed by Chinese conservation organisations to understand the public’s point of view. In urban environments the survey received over 100,000 responses with 96.4% supporting a ban on consumption of all wild animals, and over 90% supporting a ban of all trade in wild animals, including for food or medicinal use . In another survey conducted in March 2020, covering several eastern Asian regions , 93% of the 5000 respondents highlighted the same willingness to eliminate illegal and unregulated markets, with 82% of respondents wishing to do so because of fear of further zoonoses . Eastern Asia has therefore shown strong leadership following the current pandemic, the resultant increase in public awareness, and in synergy with the need for quick action to mitigate against further pandemics. However, in this region amphibian trade is not well regulated, amphibian species richness is poorly understood and most species are not nationally protected . For instance, only a small proportion of declining amphibian species are currently listed on CITES , yet the amphibian trade is a major cause of population declines in several species . In view of the global amphibian decline and the risks of zoonoses, we support the current wildlife trade bans, as well as measures to safeguard wildlife from over exploitation, and propose the following recommendations specifically for amphibians.Historically, much of the internationally traded amphibian meat originated in Bangladesh and India ,hydroponic vertical farming until the Indian bullfrog and the Indian green frog were included on Appendix II of CITES, and the trade of the species was banned in both countries due to the illegal and unsustainable capture of wild frogs .

The amphibian legal trade then shifted, primarily to Indonesia, and resulted in an increase from 180 million to 1 billion individual frogs of several species being traded between 1998 and 2007 . The principal importers for the food industry are the European Union and the United States of America , although the trade within the region is not negligible . The domestic harvest of native wild amphibians in the USA and France has already impacted amphibians through the loss of large populations of some species . These countries are now relying on imported frog meat that is generally not traceable . In addition, a significant proportion of the current amphibian trade for food and pets is unsustainable, likely to involve laundering of wild-caught specimens as captive-bred , and likely to spread batrachochytrids and other pathogens . An example of unsustainable trade is the mismatch between the quota set for the white-lipped tree frog by the Indonesian Captive Breeding Production Plan and the potential reproduction based on breeding biology of the species . However, the risks linked to trade need to be mitigated for some species, especially in Indonesia – the primary contributor to the amphibian trade. The Ministry of Agriculture and Rural Development of Vietnam ordered a ban on the trade of wildlife in March 2020, implemented in July by the Prime Minister , stipulating that wild animals and products thereof cannot be traded or consumed even when authorised by CITES permits. In addition, it recommends the closure of illegal wildlife markets, the improvement of wildlife farming management and the development of a database for threatened species currently in captivity . The ban has already resulted in several amphibian species being removed from the trade . However, this is a temporary measure with an extension being discussed , and specific licences for farmers can still be legally acquired. Nonetheless, this ban means that the sale of wild native East Asian bullfrogs has been discontinued in the country and the bullfrog populations may improve from a break in wild harvests . Furthermore, the environment may benefit from a decreased risk of pathogen transmission . If the trade ban is upheld, amphibians currently in captivity would likely need to be either euthanised or released.

While culling without financial subsidy is unlikely, these captive populations would probably be illegally sold or released into the wild, as seen in other species in similar situations . Similar to instances of individuals escaping from farms , the release of farmed amphibians can result in genetic homogenisation and the loss of genetic diversity across wild populations , as well as increasing the likelihood of pathogen transmission between released farmed stock and wild amphibians . Genetic homogenisation is a particularly salient problem in species complexes where cryptic species await formal description, such as H. rugulosusand Andrias spp. . Fortunately, in the case of H. rugulosus, frogs are generally harvested locally for the establishment of farms, therefore escape or release is unlikely to result in the introduction of individuals from segregated or different populations/ species that may threaten genetic integrity . Other native species have the potential to be locally farmed, such as Fejervarya cancrivora and Limnonectes macrodon in Southeast Asia , and Rana spp. in North East Asia, where amphibian farming relies on species that are better adapted to cooler climates . For instance, there were 152 farms breeding Rana in northeastern China in 2007 . In R Korea, farming of three Rana species has been permitted since 2005 , and several dozen facilities are now farming Rana species . While farming native species can sometimes be benign, the available numbers of captive-bred Rana are not currently satisfying the market . In R Korea, farms can apply for permits to import the same species as the one they breed, mostly from China . In China and Russia, this translates to illegal harvesting from the wild , smuggling , unsustainable export , and species laundering under the cover of farming following the significant depletion of wild populations . A complication for the amphibian meat trade arises when a farmed species is non-native, such as the American bullfrog . Multiple escapes and releases have resulted in feral populations of a highly invasive species becoming established in all eastern Asian countries where its ecological requirements are met .

The presence of L. catesbeianus has been linked to introduced pathogens and higher pathogen prevalence in native amphibians , as the species is a known reservoir of Batrachochytrium dendrobatidis , ranavirus and other parasites . The presence of the species outside of its range has been clearly linked to numerous declines in native species , and negative economic impacts when invasive populations are established . While upholding the trade ban in Vietnam has a strong conservation benefit for many native species, it may also result in the establishment of farms of invasive species, such as L. catesbeianus, and the establishment of invasive populations when farmed individuals release or escape. Similar issues have been expressed about the possibilities of other species becoming invasive. For instance, in the Philippines and in the Malaysian states of Sabah and Sarawak in Borneo, H. rugulosus is a non-native species commercially farmed for the food trade as well as for fishing bait and aquaculture feed , despite the climate of the area being adequate for invasions by the species . Additionally, Chinese giant salamanders that were released in Japan after being farmed for food, now hybridise with the native Japanese giant salamanders and threaten their genetic integrity . Consequently,vertical agriculture we recommend upholding trade bans, especially for live individuals and threatened species. While farming of L. catesbeianus has not been as successful as expected in some countries, such as Indonesia and the R Korea , it is still a widespread practice in some other regions , and escapees from farms in all regions continue to threaten the surrounding wildlife. Farming of native frogs has also been developed into a lucrative business , with Hoplobatrachus spp. individuals reaching marketable size within four months . For comparison, L. catesbeianus takes up to three years in natural weather conditions around 40◦N, or eight months at 25–30 ◦C . Areas with a tropical climate can profitably farm H. rugulosus or Fejervarya spp., especially given that some of these species are considered to be delicacies in some regions . Colder areas can rely on Rana spp., where research shows that the farming of R. chensinensis and R. dybowskii can be profitable and where it is now relatively prevalent . However, the current farming of native species cannot be treated as a net-positive conservation intervention. For instance, harvesters in Indonesia believe that harvested species are declining, although an alternative explanation is competition between harvesters . Similarly, populations of the native H. rugulosus in China have declined by approximately 30% between the 1980s and 2010s , and other large-bodied frog species have declined in Southeast Asia during the last decades . In addition, the genus Rana has declined over 60 to 70% of its range despite the active development of amphibian farming in China, resulting in a 21.5% decrease in populations of Rana over 15 years , on par with the decline in Rana populations in Russia . Breeding of these species in farms has not decreased the intensity of harvesting in the wild , and it is therefore important that the farming of native species starts supporting conservation efforts by relieving pressure on wild populations and that these operations cease the laundering of individuals and contributing to the decline and extirpation of wild populations.

Therefore, we recommend a complete ban on the farming of nonnative amphibian species, especially when there is a high potential for feral populations of such species to become established in the environment surrounding the farm, i.e. non-native species to become naturalised. In the absence of alternatives, and when possible and ecologically sustainable, non-native species should be replaced by local native species. A certification system to trace the provenance and source of animals by both sellers and buyers, as used in fisheries, could help identify and curb illegal wild harvests; however, clear mechanisms to prevent fraud are also needed . Alternatively, regulated harvest of wild populations could still be allowed at specific times of the year and in specific contexts, such as rice fields, as these are the primary habitat of numerous common and non-threatened Asian anuran species . Considering this, rice fields would require protection, as an increasingly high number of rice fields are being developed for non-agricultural uses, especially in northern Asia . Finally, it would be important to give consideration to rectifying the negative impact of farming non-native species, such as the local eradication of feral populations of L. catesbeianus, already planned by some nations , following precedents set elsewhere . Amphibian pathogens are spread and introduced through the wildlife trade , and the pet trade is known to be a significant pathway for the spread of amphibian pathogens . In addition, the pet trade threaten species and may result in the introduction of feral populations, and while no such species has been reported in Asia, to our knowledge, potentially invasive species have been found in the wild, such as Xenopus laevis in R Korea following release or escape . Another amphibian invasion related to the trade is Polypedates megacephalus, which was introduced at several localities with horticultural plants, and the populations have been increasing ever since . However, international trade is not the only problem, and trade of species between provinces of a country with different species assemblages results in the same loss. Southeast Asia is a hub for international amphibian trade, and this has a critical impact on threatened species . As a result, several species in the region have exhibited declines in population sizes and have been locally extirpated . Specifically, the pet trade is now the primary threat to some Southeast Asian newts, with the USA the largest importer until recently . An example is the Lao warty newt in Lao People’s Democratic Republic, where collection for the pet trade is a principal driver for the species’ decline . Villagers relied on the sale of 100 individuals to European, Japanese, and Chinese collectors in 2008 and 2009, an unsustainable number for the species .

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