Policy Brief ARTICLE
Policy Recommendation on the Restriction on Amphibian Trade Toward the Republic of Korea
- 1Laboratory of Animal Behaviour and Conservation, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China
- 2Interdisciplinary Program of EcoCreative, Ewha Womans University, Seoul, South Korea
- 3Department of Life Sciences and Division of EcoScience, Ewha Womans University, Seoul, South Korea
Amphibian diseases and invasive amphibian species are both generally introduced through the wildlife trade, either for human consumption or for the pet trade. However, adequate regulations can prevent such introductions. In the Republic of Korea, the establishment of invasive Lithobates catesbeianus populations resulted in the alteration of native species’ ecology and in an increase in Batrachochytrid load on local species. While not exemplified yet, the same risk arises from all species in the trade, some of which are already found in the wild despite the potential threats to the ecosystems. While regulations exist for the trade of wildlife in general, they are not directly addressing the amphibian trade, especially newly traded species. Thus, we recommend a restriction on the trade of amphibians in Korea.
1. Regulation of amphibian trade entering the Republic of Korea (food- and pet-trade),
2. Implementation of a stricter control of amphibian species already in the trade,
3. Establishment of quarantine and testing for all amphibians entering the country.
Both amphibian pathogens and invasive amphibians are generally introduced through the wildlife trade, either for human consumption or for the pet trade, and result in extensive threats to local species (Scheele et al., 2019; Falaschi et al., 2020). A widespread culprit for being both an invasive and introducing pathogens is the American bullfrog (Lithobates catesbeianus; Ficetola et al., 2007; Figure 1), carrying both fungal (Fisher and Garner, 2007) and viral pathogens (Gray et al., 2009). The presence of the species outside of its range has been linked to numerous declines in other species (Snow and Witmer, 2010), and it is also linked to a negative economic impact (Measey et al., 2016). However, the introduction of this invasive species and linked pathogens could have been prevented in numerous countries if adequate regulations had been in place when the species was first transported and introduced at multiple location around the earth. It is consequently the role of the current generation to step up regulations to prevent similar introductions and losses in the future.
Figure 1. Lithobates catesbeianus, the American bullfrog, in the wild in the Republic of Korea. This species has been introduced in the country where it has established feral population that have a significant negative impact on local species, likely resulting in the extirpation of some Hylid populations.
In the Republic of Korea, the invasive L. catesbeianus was found to be responsible for altering the ecological landscape (Ko et al., 1991; Shim et al., 2005; Heo et al., 2014; NIE, 2014; Groffen et al., 2019; Kang et al., 2019), and its presence is linked to the extirpation of Hylid populations (Borzée et al., 2020). The presence of the species is also linked to an increase in fungal load on local species (Borzée et al., 2017). However, L. catesbeianus is not the only non-native amphibian species found in the wild in the country, and species such as Duttaphrynus melanostictus1, Osteopilus septentrionalis, Xenopus laevis, and Rana spp. have also been recorded (National Institute of Ecology, 2016). As of 2014, the Republic of Korea was importing amphibians from 14 countries, accounting for several hundred tons per year (Bang et al., 2006). In 2019, this number had risen to 122 non-native species purchasable from online pet shops, for as little as 3 000 KRW (c. 2.20 euro; Koo et al., 2020), as well as native species of anuran and caudata. Some of the species available are restricted from sale or even listed as CITES (Ministry of Environment, 2018).
Species commonly available in the pet trade such as Litoria caerulea, Rhinella marina, Ceratophrys sp., Phyllomedusa sp., and Kaloula pulchra (Park et al., 2014; Koo et al., 2020) are unlikely to establish feral populations because the local climate is drastically different from the one required by the species. However, other species such as Salamandra salamandra and Dryophytes cinereus (Koo et al., 2020) are very likely to be able to establish populations due to similar ecological requirements and similar habitat characteristics as those found in the native range of these species2.
In addition, the presence of Rana chinensis in northern Gyeonggi Province following mercy releases of unsold animals from the frog meat trade are under investigation. The presence of the species results from the governmental authorisation to import the same species as the three legally farmed local species (Ministry of Environment, 2017), despite the absence of reliable means to morphologically identify the species, and disregarding the taxonomic split between Rana dybowskii and Rana uenoi (Matsui, 2014).
In addition, there is currently no restriction on the importation of species that are not listed as threatened by CITES. This absence of restriction is critical as over 30% of reported invasive amphibian introductions have resulted in the establishment of new populations (Bomford et al., 2005). Finally, the custom service also recognizes the threats, which resulted in a recommendation for veterinary medical inspection of imported animals (Heo, 2008a, b) and the government enacted a law restricting the import of specific exotic species (Act No. 14513, 2016; Enforcement Date 28 Jun 2017). This law is regularly updated and for instance two invasive freshwater turtles, Pseudemys concinna and Mauremys sinensis, were added to the list of restricted species in March (Ministry of environment, 2020).
Korean amphibians have known to be naturally infected by amphibian-specific emerging disease, including the chytrid fungus Batrachochytrium dendrobatidis (i.e., Batrachochytrid; Yang et al., 2009; Bataille et al., 2013; Borzée et al., 2017; O’Hanlon et al., 2018) and Ranaviruses (Suk et al., 2009; Kwon et al., 2017; Park et al., 2017). Emerging diseases are linked to the current extinction crisis affecting amphibians, and management measures are required to stem all risks (Stuart et al., 2004; Beebee and Griffiths, 2005; Blaustein et al., 2011; Bishop et al., 2012; Wake, 2012; Pimm et al., 2014; Scheele et al., 2019).
Deadly strands of emerging pathogens such as Batrachochytrid are of foreign origin (Suk et al., 2009; Bataille et al., 2013) and Korean amphibian species are likely to be resistant to strands originally present on the peninsula (O’Hanlon et al., 2018). However, amphibian species of foreign origin have been shown to be agents spreading pathogens (Borzée et al., 2017), potentially facilitating recombination and resulting in more virulent lineages (Farrer et al., 2011). Additionally, it has been shown that imported amphibians as pets or zoo animals increase the risk of Chytrid fungus in wild Korean populations (Kim et al., 2017). To avoid the presence of further contamination, such as the salamander chytrid fungus (Batrachochytrium salamandrivorans) affecting European salamanders (Martel et al., 2014) and anurans (Nguyen et al., 2017) with potential lethal implications (Martel et al., 2013; Stegen et al., 2017), it is important to regulate the trade of species susceptible to the infection and susceptible to be carrying the pathogens. An example of species with the potential to spread pathogens through the pet trade is for instance the fire salamanders (S. salamandra; Sabino-Pinto et al., 2015).
While there is no zoo or centre involved in breeding amphibians, pet shops import amphibians, zoos sometimes exhibit species, and specific institutions breed species for conservation purposes. For instance, the Endangered Species Restoration Center breeds Pelophylax chosenicus under the supervision of the National Institute of Ecology. These institutions are the first on the line to prevent the spread of invasive amphibian species and their pathogens and should therefore be strongly involved in preventing their dissemination.
Policy and Practice
Policies have been established but they do not prevent the import of species that were not initially found in the trade, and feral populations can become established before the amendment of the law and their addition to the list of restricted species. Thus, in view of the largely increasing number of emerging diseases targeting amphibians and the critical status of amphibians, in line with administrations aimed at regulating pet trade to prevent the spread of invasive diseases (Gray et al., 2015; Sullivan, 2018), and in agreement with the recommendations of the Amphibian Conservation Action Plan from the IUCN SSC Amphibian Specialist Group (Wren et al., 2015), we recommend a restriction on the import and trade of amphibian species into the Republic of Korea.
The restriction proposed should target all live amphibian individuals traded for leisure and consumption purposes. We recommend that all species traded for consumption should be imported after euthanasia to ascertain their impossibility to establish feral populations. Regarding species aimed at the pet trade, generally labeled as “exotic,” we recommend a total restriction to prevent the introduction of potentially invasive species and pathogens. When a species cannot be restricted from the trade, testing and quarantine procedures should be established in agreement with the Convention on International Trade in Endangered Species of Wild Fauna and Flora. In addition, only amphibian species unable to establish feral populations because of ecological requirements not matching with the ecological variables of the Republic of Korea should be exemptible from the trade restriction. We also recommend the implementation of a stricter control of amphibian species already in the trade, especially for species listed as threatened by The IUCN Red List of Threated Species, and the enforcement of regulations such as CITES to remove all banned species from sale. However, the restriction should not preclude education and research and a potential for exemptions in the case of biological samples should also be established.
AB developed the idea. All authors contributed equally.
This work was supported by the Korea Environmental Industry & Technology Institute, grant number (KEITI RE201709001) to YJ.
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Bang, S. W., Byeon, H. G., Shim, J. H., Choi, B. J., Lee, S. B., Moon, Y. L., et al. (2006). A Study for the Clarification of the Current Status of Introduced Organisms and for the Classification of Dangerous Classes to Korean Endemic Ecosystems. Ministry of Environment of Korea, Seoul. (in Korean).
Bataille, A., Fong, J. J., Cha, M., Wogan, G. O., Baek, H. J., Lee, H., et al. (2013). Genetic evidence for a high diversity and wide distribution of endemic strains of the pathogenic chytrid fungus Batrachochytrium dendrobatidis in wild Asian amphibians. Mol. Ecol. 22, 4196–4209. doi: 10.1111/mec.12385
Bishop, P. J., Angulo, A., Lewis, J. P., Moore, R. D., Rabb, G. B., and Garcia Moreno, J. (2012). The amphibian extinction crisis-what will it take to put the action into the Amphibian Conservation Action Plan? Surveys Perspect. Integrat. Environ. Soc. 5, 97–111.
Blaustein, A. R., Han, B. A., Relyea, R. A., Johnson, P. T., Buck, J. C., Gervasi, S. S., et al. (2011). The complexity of amphibian population declines: understanding the role of cofactors in driving amphibian losses. Ann. N. Y. Acad. Sci. 1223, 108–119. doi: 10.1111/j.1749-6632.2010.05909.x
Bomford, M., Kraus, F., Braysher, M., Walter, L., and Brown, L. (2005). A Report Produced By The Bureau of Rural Sciences for The Department of Environment and Heritage Bureau of Rural Science Canberra, Australia.
Borzée, A., Kosch, T. A., Kim, M., and Jang, Y. (2017). Introduced bullfrogs are associated with increased Batrachochytrium dendrobatidis prevalence and reduced occurrence of Korean treefrogs. PLoS One 12:e0190551. doi: 10.1371/journal.pone.0190551
Borzée, A., Messenger, K. R., Chae, S., Andersen, D., Groffen, J., Kim, Y. I., et al. (2020). Yellow sea mediated segregation between North East Asian Dryophytes species. PLoS One 15:e0234299. doi: 10.1371/journal.pone.0234299
Farrer, R. A., Weinert, L. A., Bielby, J., Garner, T. W., Balloux, F., Clare, F., et al. (2011). Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proc. Natl. Acad. Sci. U.S.A. 108, 18732–18736. doi: 10.1073/pnas.1111915108
Ficetola, G. F., Thuiller, W., and Miaud, C. (2007). Prediction and validation of the potential global distribution of a problematic alien invasive species: the American bullfrog. Divers. Distribut. 13, 476–485. doi: 10.1111/j.1472-4642.2007.00377.x
Fisher, M. C., and Garner, T. W. (2007). The relationship between the emergence of Batrachochytrium dendrobatidis, the international trade in amphibians and introduced amphibian species. Fungal Biol. Rev. 21, 2–9. doi: 10.1016/j.fbr.2007.02.002
Gray, M. J., Lewis, J. P., Nanjappa, P., Klocke, B., Pasmans, F., Martel, A., et al. (2015). Batrachochytrium salamandrivorans: the North American response and a call for action. PLoS Pathog. 11:e1005251. doi: 10.1371/journal.pone.01005251
Groffen, J., Kong, S., Jang, Y., and Borzée, A. (2019). The invasive American bullfrog (Lithobates catesbeianus) in the Republic of Korea: history and recommendation for population control. Manag. Biol. Invas. 10, 517–535. doi: 10.3391/mbi.2019.10.3.08
Heo, J. H., Lee, H. J., Kim, I. H., Fong, J. J., Kim, J. K., Jeong, S., et al. (2014). Can an Invasive Prey Species Induce Morphological and Behavioral Changes in an Endemic Predator? Evidence from a South Korean Snake (Oocatochus rufodorsatus). Asian Herpetol. Res. 5, 245–254.
Kim, E. T., Cho, B. Y., Cho, J. B., Yu, J. H., and Pak, S. I. (2017). Qualitative risk assessment of introducing Batrachochytrium dendrobatidis to South Korea via the importation of live amphibians. J. Prevent. Vet. Med. 41, 26–33. doi: 10.13041/jpvm.2017.41.1.26
Koo, K. S., Park, H. R., Choi, J. H., and Sung, H. C. (2020). Present status of non-native amphibians and reptiles traded in Korean online pet shops. Korea. J. Environ. Ecol. 3, 106–114. doi: 10.13047/kjee.2020.34.2.106
Kwon, S., Park, J., Choi, W.-J., Koo, K.-S., Lee, J.-G., and Park, D. (2017). First case of ranavirus-associated mass mortality in a natural population of the Huanren frog (Rana huanrenensis) tadpoles in South Korea. Anim. Cells Syst. 21, 358–364. doi: 10.1080/19768354.2017.1376706
Martel, A., Blooi, M., Adriaensen, C., Van Rooij, P., Beukema, W., Fisher, M. C., et al. (2014). Recent introduction of a chytrid fungus endangers Western palearctic salamanders. Science 346, 630–631. doi: 10.1126/science.1258268
Martel, A., Spitzen-van der Sluijs, A., Blooi, M., Bert, W., Ducatelle, R., Fisher, M. C., et al. (2013). Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proc. Natl. Acad. Sci. U.S.A. 110, 15325–15329. doi: 10.1073/pnas.1307356110
Measey, G. J., Vimercati, G., De Villiers, F. A., Mokhatla, M., Davies, S. J., Thorp, C. J., et al. (2016). A global assessment of alien amphibian impacts in a formal framework. Divers. Distribut. 22, 970–981. doi: 10.1111/ddi.12462
Ministry of Environment (2017). Wildlife Artificial Proliferation Management Guidelines 622 in Wildlife Protection and Management Law (19-26). 21 Dec 2017. In: 21 Dec 2017,Environment, M.O., Ed. Sejong: Ministry of environment.
Ministry of Environment (2018). Enforcement Decree of the Wildlife Protection and Management Act: Presidential Decree No. 28721, Partial Amendment enforcement on 27 March 2018. 28721 in 28721, Ministry of Environment, R.O.K., Ed. New Delhi: Ministry of Environment.
Ministry of environment (2020). Ecosystem Disturbance Organism Designation Notice 2020-61 in Biodiversity Conservation and Use Act (21-2). 30 Mar 2020. in: 30 Mar 2020, Vol. Biodiversity Conservation and Use Act (21-2). Sejong: Ministry of environment.
Nguyen, T. T., Van Nguyen, T., Ziegler, T., Pasmans, F., and Martel, A. (2017). Trade in wild anurans vectors the urodelan pathogen Batrachochytrium salamandrivorans into Europe. Amphibia Reptilia 38, 554–556. doi: 10.1163/15685381-00003125
Park, D., Min, M.-S., Lasater, K., Song, J.-Y., Suh, J.-H., Son, S.-H., et al. (2014). “). Conservation of amphibians in South Korea,” in Amphibian Biology, Conservation of Amphibians of the Eastern Hemisphere. In: Amphibian Biology, Conservation of Amphibians of the Eastern Hemisphere, Vol. 11, eds I. Das and H. Heatwole (Exeter: Pelagic Publishing), 52–88.
Pimm, S. L., Jenkins, C. N., Abell, R., Brooks, T. M., Gittleman, J. L., Joppa, L. N., et al. (2014). The biodiversity of species and their rates of extinction, distribution, and protection. Science 344, 987–997.
Sabino-Pinto, J., Bletz, M., Hendrix, R., Perl, R. B., Martel, A., Pasmans, F., et al. (2015). First detection of the emerging fungal pathogen Batrachochytrium salamandrivoransin Germany. Amphibia Reptilia 36, 411–416. doi: 10.1163/15685381-00003008
Scheele, B. C., Pasmans, F., Skerratt, L. F., Berger, L., Martel, A., Beukema, W., et al. (2019). Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science 363, 1459–1463. doi: 10.1126/science.aav0379
Snow, N., and Witmer, G. (2010). “American bullfrogs as invasive species: a review of the introduction, subsequent problems, management options, and future directions,” in Proceedings of the 24th Vertebrate Pest Conference, eds R. M. Timm and K. A. Fagerstone (Sacramento: University of California), 86–89.
Stegen, G., Pasmans, F., Schmidt, B. R., Rouffaer, L. O., Van Praet, S., Schaub, M., et al. (2017). Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans. Nature 544:353. doi: 10.1038/nature22059
Stuart, S. N., Chanson, J. S., Cox, N. A., Young, B. E., Rodrigues, A. S., Fischman, D. L., et al. (2004). Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783–1786. doi: 10.1126/science.1103538
Suk, K., Mi-Yeong, S., Ahn-Heum, E., Dae-Sik, P., and Nam-Yong, R. (2009). PCR detection of ranavirus in gold-spotted pond frogs (Rana plancyi chosenica) from Korea. Korea. J. Environ. Biol. 27, 110–113.
Sullivan, P. (2018). Study: Invasive Bullfrogs Linked to Spread of Deadly Fungus in Western United States: Disease Spread by Imports has Decimated Amphibian Populations Worldwide (Oakland: Center for Biological Diversity), 1.
Wren, S., Angulo, A., Meredith, H., Kielgast, J., Santos, M. D., and Bishop, P. (2015). Amphibian Conservation Action Plan. IUCN SSC Amphibian Specialist Group. Available online at: http://www.amphibians.org/acap/ (accessed July 24, 2020).
Yang, H., Baek, H., Speare, R., Webb, R., Park, S., Kim, T., et al. (2009). First detection of the amphibian chytrid fungus Batrachochytrium dendrobatidis in free-ranging populations of amphibians on mainland Asia: survey in South Korea. Dis. Aquat. Organ. 86, 9–13. doi: 10.3354/dao02098
Keywords: amphibian, pet trade, invasive species, emerging diseases, threat, Korea
Citation: Borzée A, Kwon S, Koo KS and Jang Y (2020) Policy Recommendation on the Restriction on Amphibian Trade Toward the Republic of Korea. Front. Environ. Sci. 8:129. doi: 10.3389/fenvs.2020.00129
Received: 08 May 2020; Accepted: 16 July 2020;
Published: 07 August 2020.
Edited by:Franco Andreone, Museo Regionale di Scienze Naturali, Italy
Reviewed by:Alessandro Catenazzi, Florida International University, United States
Ché Weldon, North-West University, South Africa
Copyright © 2020 Borzée, Kwon, Koo and Jang. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Amaël Borzée, email@example.com