Policy recommendations for the Rana trade towards the Republic of Korea

- Ban the trade of non-native species for consumption as food or derived products and for personal use (i.e., as pets).

- Ban the trade of native species when they do not originate from within the nation (i.e., same genetically defined conservation unit).

- Tracking of potential established alien Rana populations.

- Eradication of potentially established alien Rana populations.

1 Introduction

1.1 Species introduction

Wildlife trade is responsible for the introduction of numerous species into new environments globally (Souviron-Priego et al., 2018), including amphibians. Invasive species generally have negative impacts on local species through predation, competition (Mori et al., 2015; Sarashina and Yoshida, 2015) and other ecological interactions (Buckley and Catford, 2016), including carrying non-native pathogens (Bezerra-Santos et al., 2021). This is also the case in Ranidae species, such as Pelophylax ridibundus in the UK (Zeisset and Beebee, 2003), and several species in the focal area of this study, including Rana huanrenensis that has been introduced to offshore islands in the Republic of Korea (Bae et al., 2022).

The amphibian trade towards the Republic of Korea includes live animals both for the pet trade (online and shops; Koo et al., 2020) and for human consumption (shops and markets; Othman et al., 2022). Trade principally originates from the People’s Republic of China (hereafter China; 97% of weight) and the USA (0.94% of weight; Jo et al., 2022). Amphibian imports and sales have increased from 0.2 ton in 2002, to 11.8 tons in 2016, followed by a sharp increase over the last 5 years to reach 37.7 tons in 2021 (Korea Customs Service; https://unipass.customs.go.kr/ets/index.do?menuId=ETS_MNU_00000103). As a result, some amphibian species have been designated as Alert Alien Species (Notification of the Ministry of Environment, No. 2020-79). One of the most widely introduced amphibian species in the world, the American bullfrog (Lithobates catesbeianus; Luque et al., 2014) has become invasive in the Republic of Korea as a result of the trade for human consumption, starting in the 1970s (Groffen et al., 2019). The invasive population of American bullfrog in the Republic of Korea has resulted in a severe loss of aquatic biodiversity (Son et al., 2021), and numerous removal efforts have failed, indicating that eradication is extremely complicated and expensive to achieve (Oh and Hong, 2007; Groffen et al., 2019; Soto et al., 2022), although not impossible (e.g., Simberloff, 2003; Kahrs, 2006; Kamoroff et al., 2020). Therefore, the most efficient and cost-effective approach to prevent the establishment of species known to have the potential of becoming invasive is by prohibiting initial introduction (Othman et al., 2022).

The Republic of Korea imports live Brown frog (Rana spp.) individuals from China for human consumption (Othman et al., 2022). This trade is conducted under a legal umbrella as the species can be exported from China (http://www.gov.cn/zhengce/2020-12/27/content_5573532.htm; see acknowledgements for an English version), and species that are native to the Republic of Korea can be legally traded, including R. uenoi, R. huanrenensis and R. coreana. Two of these species, R. huanrenensis and R. coreana, also occur in China, and are present in the wildlife trade. The last species, R. uenoi, is endemic to the Korean Peninsula and Tsushima Island in Japan. Only described in 2014, R. uenoi has been split from the R. dybowskii species complex (Matsui, 2014). It was however previously treated as R. dybowskii, and was therefore assessed as occurring throughout the Korean Peninsula, northeast China, and the Primorsky region in Russia. However, the two clades are differentiated at the species level following multiple lines of evidence, and all individuals belonging to this species complex in the Republic of Korea are finally recognised as R. uenoi (Jeon et al., 2021). As a result, the legality of trade towards the Republic of Korea between 2014 and 2021 was a point of contention.

A recent study has demonstrated that the ranid species imported to the Republic of Korea do not only include legally traded species, but also some species that are not native to the nation but morphologically similar: R. amurensis, R. chensinensis, R. dybowskii, R. kukunoris and R. taihangensis (Othman et al., 2022; Shen et al., 2022). In addition, these species have not been explicitly listed as banned from the trade by the Ministry of Environment due to the absence of prior data on the potential for invasion, and fall under a broader legislation regarding the general trade of species. In addition to likely escapes from sellers, which could start the invasion process, communication with traders in the Republic of Korea revealed that at the end of the legal sale period, unsold individuals were released in nearby streams, reportedly for welfare reasons, but perhaps also because of costs or methods to keep them, or because of reduced market value. While individually these releases can seem ethical, they are biosecurity threats as the frogs are not scanned for pathogens. Both African Swine Fever and Avian influenza related pandemics are valuable examples of how quickly pathogens can spread.

Following the development of international trade, updated regulations guiding such exchanges are required, and science-based recommendations have the potential to lead the development of regulation to prevent the loss of biodiversity (Pullin et al., 2009). Thus, policy recommendations have the potential to help update national laws, especially in this context. For instance, a policy recommendation on the trade of invasive American bullfrogs towards the Republic of Korea (Borzée et al., 2020) was temporally coincidental with a regulatory update in the trade of amphibians (Korean Law Information Center, 2021). However, new discoveries such as the presence of non-native Rana species in the trade, calls for specific updates in regulations, resulting in this policy recommendation and its potential use for further legal adjustments in the trade of the genus.

1.2 Risks of invasion

The trade of amphibians and the resulting invasive species can pose two major ecological and biosecurity threats for the survival of native species. The first one being the impact on native species through ecological interactions, and the second being through pathogen dispersion (Kraus, 2015; Falaschi et al., 2020; Green et al., 2020). Both of these impacts have already been documented from the invasive American bullfrog (L. catesbeianus) in the Republic of Korea, impacting the ecology of native amphibians, reptiles and birds (reviewed in Groffen et al., 2019), and also increasing the pathogen loads on native species (Borzée et al., 2017).

Many Rana species have overlapping morphological and ecological traits, and are therefore more likely to occupy similar niches. For example, two species pairs, R. coreana plus R. amurensis, and R. dybowskii plus R. uenoi, have similar ecological requirements within pairs. The impact of the interactions between these species pairs is however unknown as the contact zones are in the Democratic People’s Republic of Korea (Borzée et al., 2021). In addition, even within a single species, the ecological requirements of geographically distant clades can be significantly divergent (Stockman and Bond, 2007; Podnar et al., 2014), and the displacement of individuals, and the potentially resulting hybridisation, of the clades can result in the inadequate adaptation to the environment and a decrease in fitness (Parris, 2000) or resistance to pathogens (Parris, 2004). Therefore, the introduction of any of the non-native Rana species, and their establishment in the wild in the Republic of Korea could result in competition and hybridisation with the native species, driving the extirpation of the native Rana. The negative effect of displacements can also be within a single species, such as in R. huanrenensis, as the species ranges from Liaoning in China in the north to the southern edge of the Korean Peninsula in the south, resulting in a latitudinal variation known to be linked to diverging ecological requirements (Andersen et al., 2022). The introduction of individuals from a northern latitude to the south, and any resultant hybridisation, would result in individuals less adequately adapted to the local environment and could even result in species losses. In addition, hybridisation can magnify the invasive capacity of a species (Coulter et al., 2020).

Two major pathogens that are transferred by Rana species include Ranavirus (family Iridoviridae; Kwon et al., 2017) and Batrachochytrium dendrobatidis (Bd; Bataille et al., 2013). Ranavirus is found in both captive and wild populations in the Republic of Korea, resulting in mortality events in both settings (Kwon et al., 2017; Park et al., 2017). Intriguingly, the mass mortality events in the wild occurred in the area where the non-native Rana species focal to this study had been released (although currently not known to have been involved), and even if no individual was intentionally released, all farms provide a substantial risk of individuals escaping over time. In addition, Ranavirus prevalence is known to be higher in invasive ranids in the Republic of Korea (Roh et al., 2022). While Bd is not known to have resulted in mass mortality events in the Republic of Korea, Rana species can be reservoirs for the pathogen (Bataille et al., 2013; Fong et al., 2015), and the introduction of non-native Bd strains could have deadly effects. Therefore, the introduction of Rana species across natural boundaries can have disastrous consequences for local populations, including local extirpation (e.g., Borzée et al., 2017).

To address some of these threats in compliance with the legal obligations established by the Convention on Biological Diversity (CBD), the Republic of Korea’s Fourth National Biodiversity Strategy (2019-2023; Nature Conservation Bureau, 2018; https://www.cbd.int/doc/world/kr/kr-nbsap-v4-en.pdf) contains a number of action plans that aim at managing threats to biodiversity, among others, by establishing mechanisms to control human-mediated species introduction, strengthening policy responses and post-introduction control of invasive species. Biodiversity conservation through the protection of endangered and endemic species is also one of the targets established by the National Biodiversity Strategy of the Republic of Korea and other regulations with a special focus on strengthening research on and response to wildlife diseases, along with an improved wildlife rescue and care system.

2 Policy options and implications

Current laws in the Republic of Korea allow for the import and captive breeding of a number of Rana species such as R. huanrenensis, R. dybowskii and R. coreana as long as authorities have issued a permit. While the trade of native species is legal, further measures need to be implemented to avoid the introduction and establishment of non-native species with serious impacts for the native population of Rana. Recent amendments to the legislations will designate amphibians as aquatic organisms managed by the Ministry of Oceans and Fisheries as of 2023, and treated as fisheries livestock in this regard, and therefore subjected to the same regulation as fishery products (Ministry of Oceans and Fisheries Ordinance N. 543, 2022.4. 29. Partial amendment). Trade bans have already been declared for certain species in the Republic of Korea, and the regulation can be built upon (Kang and Phipps, 2003).

3 Actionable recommendations

To ensure that new alien populations of Rana will not be established in the Republic of Korea, we recommend banning the trade of ecosystem disturbing non-native species or specimens of the native species that are from different genetically defined conservation units (following for instance Othman et al., 2022). “Trade” refers also to operations of import or export and includes notably the trade for human consumption and its derivatives and trade for personal use. To allow for this, authorities could conduct a risk assessment to decide whether alien Rana species are ‘ecosystem disturbing species’. This measure is supported by the scientific literature referenced in this manuscript and by national legislation (Republic of Korea’s Act N. 11257 of 2012 on the Conservation and Use of Biological Diversity Arts. 21 to 24 “The Biological Diversity Act”).

This ban should also apply to domestic trade, with individuals of R. uenoi from Jeju Island not being traded on the mainland, as this population belongs to a different conservation unit (Jeon et al., 2021). This could be done by designating Jeju Island as a special protection district (Act N. 10977 of 2011 on Wildlife Protection and Management, Article 27).

One exception could be applied to this ban: when the trade of these species is not impacting the conservation of said species in exporting regions (R. huanrenensis and R. coreana), the trade should consist solely of dead specimens to ensure the absence of escapes, and release of pathogens.

Through trade, numerous individuals have been imported, released, or have escaped. As a result, the presence of established alien populations is not impossible. To avoid further disturbances and reducing the potential for economic costs associated with the establishment of an invasive population, the release of any alien specimen and its offspring originating from the past trade should also be banned as far as possible. While the banning measures are decided, we recommend authorities to use the competences granted in Art. 14.2 of the Biological Diversity Act and adopt emergency measures to prevent the risk of depletion or disappearance. In this sense, we recommend that such populations should be tracked, and controlled (captured and removed, or re-exported if the population of origin can be identified and the individuals can be certified to be free of pathogens), before it becomes too late and alien species are not manageable.

In addition, even though released and escaped frogs may not have established populations, they may have spread pathogens, infecting native populations. Thus, broad scale surveys for ranavirus and chytrid fungus (B. dendrobatidis and Batrachochytrium salamandrivorans) should be conducted around the establishments selling frogs traded from abroad, and a plan for the control of pathogens should be established.

Lastly, we recommend the establishment of an updated National Species List of native species that includes R. uenoi along with keys for species identification, which can be useful at borders and custom offices, and especially for the Korea Customs Service, which is in charge of controlling the trade (see identification key in Table 1).

TABLE 1

TABLE 1. Identification key and comparison of 40 morphological characters between eight species of northeastern Asian brown frogs (genus Rana) recorded from the literatures and online databases of amphibians: AmphibiaWeb (https://amphibiaweb.org) and AmphibiaChina (https://www.amphibiachina.org/). The boxes coloured in grey and marked with symbol (+) indicate the presence of the character in the species and the colourless boxes marked with symbol (−) indicate the absence of the character in the species, OR, the absence of definitive information but matching with at least a few individuals of the species. The symbol (?) indicate the lack of information about the specific morphological character. Coloration outside of the breeding season is not specified as the trade is limited to the breeding season when body condition makes frogs more suitable for human consumption. The comparison of morphological characters and classifications of Rana into clades I, II and III in the table are adapted from the operational taxonomic units (OTU) based on the 16S rRNA phylogeny of Othman et al. (2022), where R. chensinensis matches with OTU 7 and R. taihangensis matches with OTU 1 and 2, following Shen et al. (2022).

4 Conclusion

Several non-native Rana species have been traded towards the Republic of Korea over the past decades. The trade was conducted legally. However, trade followed regulations that failed to incorporate current advances in taxonomy. Although the establishment of alien Rana populations in the Republic of Korea has not been confirmed, factors which could potentially result in such establishments have been brought together. It is therefore important to monitor Rana populations with molecular tools around establishments selling frogs to clarify their native status, as well as to monitor the presence of pathogens. In addition, to avoid the establishment of such alien populations and associated pathogens, it is important to ban the trade of non-native species entirely for human consumption. If the trade of native species has to be maintained, it should be limited to processed products, linked to verifiable data informing on the origin of the animals and results of disease screening, so that the risk of establishment of alien populations is nullified. The species of principal focus are R. dybowskii, R. amurensis, R. chensinensis, R. taihangensis and R. kukunoris, although further analyses to provide a clearer definition of taxonomy and conservation units are also needed.

Author contributions

The ideas were developed, and the manuscript drafted by AB, MR, NB and SO. All other authors provided constructive feedback and revised the manuscript.

Funding

This work was supported by the Foreign Youth Talent Program (QN2021014013L) from the Ministry of Science and Technology to AB.

Acknowledgments

We are grateful to Hyuntae Kim and Anna Ryazanova for the use of their photographs. This policy recommendation is also supported by Hankyu Kim and Irina Maslova. Maslova also mentioned residents of Primorsky Krai, Russia catching Rana amurensis on the west coast of Lake Khanka, following the poaching and purchase of Rana dybowskii in Vladivostok by representatives of Rana farms located in China. However, the representatives did not purchase R. amurensis, likely due to their smaller size, and the frogs were released in the vicinity of Vladivostok, 300 km away from their point of capture. One of the reviewers kindly provided a link for an English version of China’s regulation of wildlife export: https://sherloc.unodc.org/cld/en/legislation/chn/regulations_of_the_peoples_republic_of_china_on_administration_of_import_and_export_of_endangered_wild_animals_and_plants/regulations_of_the_peoples_republic_of_china_on_administration_of_import_and_export_of_endangered_wild_animal.html.

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.

Publisher’s note

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