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The lab, in collaboration with numerous colleagues, recently published a policy recommendation highlighting why the trade of Brown Frogs (Rana) towards the Republic of Korea is bad for biodiversity.

Background

The illegal trade in wildlife has introduced various species to new environments worldwide, including amphibians. Invasive species have harmful effects on local species through competition, predation, and other ecological interactions, including introducing non-native pathogens. Several species in the focus area of this study, including Rana huanrenensis, have been introduced to offshore islands in the Republic of Korea.

The Republic of Korea has a significant amphibian trade, including live animals for both pet trade and human consumption. The trade originates mainly from China and the USA and has grown significantly over the past two decades. As a result, some amphibian species have been designated as Alert Alien Species and invasive species, such as the American bullfrog, and have caused a severe loss of aquatic biodiversity. Eradicating invasive species is very complicated and expensive, making prevention of introduction the most cost-effective approach.

The Republic of Korea imports live Brown frog (Rana) individuals from China for human consumption, and this trade was conducted legally as some native species of the Republic of Korea can be legally traded. However, Rana uenoi, which is endemic to the Korean Peninsula and Tsushima Island in Japan after being split from the Rana dybowskii species complex cannot be legally traded anymore.

The Republic of Korea imports not only legally traded species but also non-native frog species that are morphologically similar to native ones, including Rana amurensis, Rana chensinensis, R. dybowskii, Rana kukunoris and Rana taihangensis. Once traded, some individuals may be released into nearby streams at the end of the legal sale period for welfare reasons, but this is a biosecurity threat because the frogs are not scanned for pathogens, and the African Swine Fever and Avian influenza pandemics have shown how quickly pathogens can spread. In addition, there is a threat of establishment, and hybridisation with local species.

International trade towards Korea requires updated regulations based on science-based recommendations to prevent the loss of biodiversity. Policy recommendations have the potential to help update national laws, especially in the case of the trade of invasive species. A policy recommendation on the trade of invasive American bullfrogs towards the Republic of Korea has coincided with a regulatory update in the trade of amphibians, but the discovery of non-native Rana species in the trade calls for additional updates in regulations. This policy recommendation has the potential to lead to further legal adjustments in the trade of the genus.

Risks of invasion

Amphibian trade can result in invasive species, causing two threats to the survival of native species. These threats include ecological interactions and pathogen dispersion, both of which have been documented in the invasive American bullfrog in the Republic of Korea. This species has impacted the ecology of native amphibians, reptiles, and birds, as well as increasing pathogen loads on native species.

Many Rana species have similar ecological requirements, and the impact of interactions between species pairs is unknown. Geographically distant clades of a single species may have significantly divergent ecological requirements, and displacement of individuals due to the introduction of non-native Rana species can result in competition and hybridisation, driving the extirpation of native Rana species. The negative effect of displacement can also be within a single species, resulting in individuals less adapted to the local environment or even species losses. Hybridisation can also magnify the invasive capacity of a species.

Rana species can transfer two major pathogens: Ranavirus and the chytrid fungus Batrachochytrium dendrobatidis (Bd). There have been mortality events occurring in both captive and wild populations in the Republic of Korea due to Ranavirus. Even if non-native Rana species have not been involved in these events, they pose a risk of escape from farms, and Ranavirus prevalence is higher in invasive Ranids in the Republic of Korea. Rana species can also be reservoirs for Bd, 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.

The Republic of Korea’s Fourth National Biodiversity Strategy (2019-2023) contains action plans to address threats to biodiversity, including establishing mechanisms to control human-mediated species introduction and strengthening policy responses and post-introduction control of invasive species. The strategy also aims to protect endangered and endemic species and strengthen research and response to wildlife diseases, along with an improved wildlife rescue and care system. These actions are in compliance with legal obligations established by the Convention on Biological Diversity.

Current laws in the Republic of Korea allow for the import and captive breeding of certain Rana species with a permit, but measures are needed to prevent the introduction and establishment of non-native species that could harm native populations. Amphibians will soon be designated as aquatic organisms and regulated similarly to fishery products. Trade bans have already been implemented for some species in the Republic further strengthened.

Actionable recommendations

To prevent the introduction of new alien populations of Rana in the Republic of Korea, a ban on trading non-native Rana species should be implemented. This ban should also include domestic trade, specifically preventing the trade of R. uenoi from Jeju Island on the mainland. However, dead specimens of certain Rana species may be allowed for trade if it does not impact conservation efforts, and to prevent escapes and the release of pathogens.

To prevent the establishment of new invasive alien populations and the spread of pathogens, the release of any alien specimens and their offspring originating from past trade should be banned. Authorities should also use emergency measures to prevent the risk of population depletion, track and control potentially invasive species, and conduct broad-scale surveys for ranavirus and chytrid fungus. An updated National Species List that includes R. uenoi and a species identification key should be established to aid in border control and trade regulation efforts.

Conclusions

Non-native Rana species have been traded legally into the Republic of Korea, but regulations have not kept up with advances in taxonomy. While the establishment of alien Rana populations has not been confirmed, monitoring of populations and the presence of pathogens is necessary to prevent their establishment. The trade of non-native species for human consumption should be banned entirely, with the trade of native species limited to processed products and verifiable data to avoid the risk of invasion. The focus should be on Rana dybowskii, Rana amurensis, Rana chensinensis, Rana taihangensis, and Rana kukunoris, with additional analyses needed for conservation.

Welcoming the Fujian Bamboo Salamander to science! 欢迎虚竹小鲵走进科学！We described a new species, the Fujian Bamboo Salamander (Hynobius bambusicolus).

Human activities, such as anthropogenisation of landscapes, have led to the sixth mass extinction, with species of large size and narrow spatial range being most impacted. Between 900 and 130,000 species have become extinct since the 1500s, and even species that have not yet been described are going extinct without being documented. Amphibians are the most threatened animal class, with habitat loss being a major driver of their decline. To improve their status, a clear taxonomy is needed, especially in southern China where many species still need formal description or taxonomic revision. Conservation actions are crucial for maintaining evolutionary patterns free of anthropomorphic selection, but practitioners need to know what to protect, and thus species need to be described currently, as conservation does not correspond to threat status, and we can only protect what we know.

人类的一系列活动，例如对自然景观的改造，直接或间接导致了第六次物种大规模灭绝，尤其对那些体型庞大但活动空间狭小的物种造成了严重影响。自1500年以来，据记载已有900~130,000个物种灭绝，甚至一些未被描述的物种也在未被“认识”的情况下灭绝。其中，两栖动物受到的威胁最大，主要是由于栖息地的丧失。因此，为了改善两栖动物的生存状况，科研人员需要制定一个明晰的分类系统，特别是中国南部的许多物种，需要对它们进行正式描述或分类修订。此外，保护行动对于维持自然演化模式也是至关重要的，但从业者需要知道保护对象。鉴于物种保护与其受威胁状态并不相符，因此我们需要对一些物种进行正式描述，同时保护我们所了解的物种。

Most Hynobius salamander species in China are expected to have been described, but taxonomic resolutions are ongoing. There are six described species on the Chinese mainland and five on Taiwan island, all terrestrial, partially fossorial and breeding through larval development in water bodies. A Hynobius salamander collected in 1978 from Fujian has not been seen since, potentially because of local extirpations. We tested for phylogenetic clustering within the H. chinensis clade and determined the taxonomic status with phylogenetic tools, resulting in the description of a new species, Hynobius bambusicolus.

分类学家们已对中国发现的所有小鲵都进行了描述，但分类厘定仍在进行中。中国大陆有六个已描述的小鲵物种，台湾省有五个，它们都是陆生的，其中部分营穴居生活，在水体内进行繁殖及幼体生长。1978年曾有研究者在福建发现一种小鲵并将其鉴定未中国小鲵，但那之后直至本次发现之前，却再未有报道，可能是因为局部灭绝。本研究中，基于研究分析，我们认为该物种是一个未描述新种。研究人员通过对中国小鲵分支进行聚类分析并借助系统发育工具确定其分类地位，将其描述为一种具有特定形态特征的小鲵新种。

We found a significant variation between H. bambusicolus and all 18 other species based on rates of evolutionary divergence between sequence pairs. The average divergence rate was higher than for other pairs, supporting the position of the candidate species as a deeply divergent clade within the Southern Chinese group of East Asian Hynobiids. All phylogenetic trees coherently recovered the candidate species as monophyletic, identified as sister species to H. amjiensis in some trees.

基于序列对之间的进化分歧率，发现候选物种与其它18个物种之间存在显著差异。平均分歧率高于其它物种，这支持将该物种厘定为东亚小鲵在中国南方群体中一个深度分化的类群。同时，所有贝叶斯树结果都表明该物种为单系，部分聚类树结果表明该物种为安吉小鲵的姊妹群。

In the study, we obtained 55 haplotypes based on the gene fragment for COI, representing 16 species of Hynobiid salamanders across East Asia. The haplotype diversity was 0.98, and a shared relationship was observed between the haplotype group of the candidate species and geographically related haplotypes of Southern Chinese Hynobius. Morphometric measurements indicated that the species was larger in size, with a low number of coastal grooves and a toe formula similar to other species in the area. The number of costal grooves was identified as an important character for the non-invasive identification of the species.

本研究基于COI基因片段，获取了55个单倍型，代表了东亚的16种小鲵。结果表明单倍型的多样性为0.98，并观察到该物种和与其有地理交集的中国南方小鲵的单倍群具有共同点。形态测量结构表明，该物种体型较大，肋沟数目较少，趾式与该地区其它三种小鲵相似。肋沟数目是该物种重要的外部鉴别特征。

We described the new species of Hynobiid salamander, H. bambusicolus, based on molecular analysis and morphology. The species was found in Fujian province, China, specifically in bamboo forests and is named the Fujian Bamboo Salamander. The species name comes from the habitat of the holotype and the Chinese name, 虚竹小鲵 (pronounced: Xū Zhú Xiǎo Ní), reflects the scientific name and is named after a character from the Jin Yong’s swordsman fiction, where an unknown Shaolin monk inherits great powers by coincidence and starts a legendary journey.

根据分子和形态学分析，我们描述了一个小鲵新种——虚竹小鲵(H. bambusicolus)。该物种发现于中国福建省的竹林中。种加词 bambusicolus取自模式标本的栖息地，中文名称“虚竹小鲵”与其学名(H. bambusicolus)相对应，“虚竹”取自金庸武侠小说《天龙八部》中的主要人物。

We only found H. bambusicolus in the Quxi village, Liancheng County in China. Its larvae and development stages are typical of Hynobius salamanders, with functional limbs developing slowly. The species can be identified through its location and a combination of 10 or fewer costal grooves with a total length greater than 180 mm. Juveniles have brown coloring and blue speckling that disappears with age, while adults are a uniform dark chocolate colour with light grey and blue speckling on the venter.

目前，虚竹小鲵(H. bambusicolus)仅发现于中国福建省连城县曲溪乡。其幼体各个发育阶段为典型的小鲵发育模式，四肢发育缓慢。可根据栖息地及其肋沟数目对其进行鉴定，肋沟一般不超过10条，且体长大于180毫米。幼体褐色具蓝色斑点，且随着年龄增长，蓝色斑点逐渐消失。成体通体深巧克力色，腹部具浅灰色和蓝色斑点。

Hynobius bambusicolus salamanders breed in shallow pools found in bamboo forests above 1400 m above sea level, laying their egg sacs (containing between 21 and 27 eggs) in pools made by tire tracks. Adult salamanders hide under logs, stones, or dead leaves in wet soil and humus in waterlogged areas. The salamanders emit a short, low-frequency call composed of four strong harmonics, possibly as an alarm call.

虚竹小鲵在海拔1400米以上的竹林浅水池中繁殖，它们经常将卵（含21至27个卵）产于车轮在土路上轧出的积水凹坑中。成体躲藏在树干、石头或湿润土壤的枯叶下方以及腐殖质中。在实验室中用红虫饲养幼体，有些个体会相互残食。此外，虚竹小鲵会发出由四个强谐波组成的短暂的低频鸣叫，可能是作为屈服或警报呼叫。

We described H. bambusicolus based on divergent genetic origins, unique morphological characteristics, and separate distribution from other Hynobius species. Identification of H. bambusicolus is easiest based on its geographic location, as it has no overlap with other Hynobius species and is an ancient lineage that likely experienced distribution changes due to paleogeographic and climatic variations. The area inhabited by this species also includes other Caudata, and competition with other genera may occur.

虚竹小鲵，是基于分子、形态特征以及分布差异而描述的。根据地理位置来鉴定虚竹小鲵是最容易的，因为它与目前发现的其它小鲵在地理分布上没有重叠，并且可能是一个因古地理和气候变化而经历了分布变化的古老物种。该物种所生活的区域内也有其它有尾目，这可能使得虚竹小鲵会与其它属之间发生竞争。本研究提供了中国南方小鲵进化和分布的新见解。

The H. bambusicolus salamander is micro-endemic and has a restricted distribution with an incredibly small population size, making it highly vulnerable to extinction. The species is adapted to sub-tropical bamboo forests, but also prefers cold temperatures for spawning. Surveys in 2023 confirmed that the species is known from a single locality with only a few extremely small water bodies, potentially containing a maximum of 20 breeding females. The population size is likely to be well below 200 breeding individuals, meeting the IUCN Red List criteria for critically endangered species. The establishment of an ex-situ population is recommended to prevent extinction due to climate instability and other stochastic risks.

从已掌握的信息来看，虚竹小鲵分布范围有限，是狭小空间的特有种，种群极小，这使得它们非常容易灭绝。该物种适应了在热带竹林的生活环境，但更喜欢在寒冷的气候下进行产卵。 据2023 年的调查显示，该物种只生存在单个地点中少量的极小水体周边，并且该地最多可能只有 20 只可繁殖中的雌性个体。虚竹小鲵的种群数量很可能远低于 200 只可繁殖个体，已达到极度濒危物种的衡量标准。因此，我们建议建立自然生境以外的虚竹小鲵人工饲养种群，以避免该物种因气候不稳定和其它随机风险而导致的灭绝

To protect the new species, hobbyists should avoid collecting and trading it, and keep information about its location confidential. Habitat loss, particularly through bamboo plantation and harvest, is the main threat to the species, and climate change is likely to contract its distribution. To reduce stresses on the species, herbicide use and water pumping in the area should be minimized, and habitat restoration efforts such as artificial ponds and rehabilitating old reservoirs should be implemented to boost population growth.

为了保护虚竹小鲵这一新物种，异宠爱好者应该避免捕捉和交易，并对其分布信息进行保密。结合前期调查分析，生境的丧失尤其是竹林的种植和砍伐是该物种面临的主要威胁，此外，气候变化也可能会缩小其分布范围。最后，为了减少对该物种的影响，人们应尽量减少在其栖息地使用除草剂以及民用抽水，同时亟需制定并实施相应的生态恢复措施，如建立人工池塘和修复旧水库，以促进其种群增长。

Reference: Wang Z., Othman S. N., Qiu Z., Lu Y., Prasad V. K., Dong Y., Lu C-H. & Borzée A. (2023). An isolated and deeply divergent Hynobius species from Fujian, China. Animals. 13:1661. DOI: 10.3390/ani13101661.

우리 연구실에서 함께 동물 보전을 위해 연구하고 있는 Andersen 박사님 그리고 장이권 교수님과 새로운 논문을 출판하였습니다.

멸종 위기 종의 제한적인 서식지는 서식지 단편화 및 손실로 인하여 유전적 병목 현상과 환경에 대한 작은 변화를 증폭시킬 위험이 있습니다. 개체군 생존율 분석(Population viability analyses, PVAs)을 포한 생태학적 분석은 연구 종에 대하여 비침습적 또는 유해하지 않은 방법으로 개체군의 궤적을 예측할 수 있습니다. 따라서 연구 종들은 보전을 위하여 개체군을 모델링 하는데 필수적인 요소가 될 수 있습니다. 서식지 적합성 모델은 보호 구역을 지정을 제안하기 위하여 사용되었지만, 개체군 생존율 분석(Population viability analyses, PVAs)은 이 점에 대해 일반적으로 사용되지 않습니다.

수원청개구리(Dryophytes suweonensis)와 노랑배청개구리(Dryophytes flaviventris)는 한국의 고유종이자 멸종 위기 종 입니다. 수원청개구리(D. suweonensis)와 노랑배청개구리(D. flaviventris)가 멸종 위기 처한 것은 서식지 파괴와 단편화 그리고 외래종 외 다른 포식자들에게 포식 당하기 때문입니다. 우리는 생태적 지위와 연결성 그리고 Vortex에 PVAs를 결합한 통합 모델링 접근법을 사용하여 보호 구역 지정에 대한 기준 시나리오에서 각 종의 멸종 가능성을 판단하였습니다.

지정된 시나리오에서는 미래의 운반 능력 감소 중지(보호 지역 상태를 통하여 향후 서식지 파괴 중지), 자연 재해의 영향 감소(가뭄의 영향 완화) 및 사망률 감소(외래종 포식자의 개체수 통제와 올챙이를 성체까지 사육)을 통해 Vortex에서 시뮬레이션 되었습니다. 이러한 보전 관리의 통합성을 현재 실천되고 있는 ‘무 보전’이 아닌 ‘적극적인 보전 활동’으로 분류하였습니다. 또한 단계적 접근 방식을 사용하여 각 지역의 보전 우선 순위를 판단했습니다. 현재 조건(무 보전)에서 100년 후 결과적으로 유효한 메타 모집단은86.5%의 멸종율을 갖는 수원청개구리(Dryophytes suweonensis) 167 ± 325 개체 및 90.3%의 멸종율을 갖는 노랑배청개구리(Dryophytes flaviventris) 165 ± 200 개체였습니다. 전 지역(93개의 서식지, 426.9 km²)을 적극적으로 보전 및 관리를 한 결과 두 종의 메타 모집단 크기가 크게 증가한 멸종율은 0% 수원청개구리(D. suweonensis) 15,910 ± 2,855 노랑배청개구리(D. flaviventris) 4,400 ± 874로 나타났습니다.

우선 지정 순위를 결정하면 정부 기관에 보호해야 서식지 지정과 능동적 또는 수동적 관리를 적용해야 하는지 여부를 판단할 수 있을 것입니다. 어떠한 노력도 하지 않으면 수원청개구리(Dryophytes suweonensis)와, 노랑배청개구리(Dryophytes flaviventris)는 멸종될 것 입니다. 정부가 직접 위와 같은 내용을 적용하여 관리하는 보전은 유용할 뿐만 아니라 우선 순위로 보호 지역을 지정하는 방법론으로 우리의 연구는 향후의 연구로 이어질 수 있을 것 입니다.

Andersen D., Jang Y. & Borzée A. (2022). Influence of landscape and connectivity on anuran conservation: population viability analyses to designate protected areas. Animal Conservation, published online. DOI: 10.1111/acv.12829

New lab paper published in Animal Conservation in collaboration with Dr. Andersen and Prof. Jang!

Threatened species with restricted ranges are at risk from habitat fragmentation and loss, which amplifies genetic bottleneck and impacts of small changes to their environments. Ecological models including population viability analyses (PVAs) can predict the trajectory of populations in a way that is not invasive or detrimental to the study species. They can therefore be a vital tool in modelling populations for conservation purposes. Although habitat suitability models have been used in studies to suggest areas for protected area designation, PVAs are generally not used in this regard.

Dryophytes suweonensis and Dryophytes flaviventris are two threatened treefrog species endemic to the Korean Peninsula. The two species face threats of habitat loss and degradation and predation by invasive species among others. We used an integrated modelling approach combining ecological niche, connectivity, and PVAs in Vortex to determine the likelihood of extinction of each species under baseline and protected area designation scenarios.

Designation scenarios were simulated in Vortex through halting future reduction in carrying capacity (halting future degradation to sites through protected area status), reducing effects of catastrophes (mitigating the effects of drought) and reducing mortality rates (controlling invasive predator populations and ex situ raising of tadpoles to maturity). We classified the combination of these management efforts as “active management” as opposed to “no management” which is currently being practiced. We additionally used a stepwise approach to determine designation priority of individual patches. Under current conditions (no management), the resulting effective metapopulations after 100 years were 167 ± 325 individuals with an 86.5% extinction probability for D. suweonensis and 165 ± 200 individuals with a 90.3% extinction probability for D. flaviventris. Under active management of all sites (93 sites covering 426.9 km2), the extinction probability was 0% for both species with significantly increased metapopulation sizes, 15,910 ± 2,855 for D. suweonensis and 4,400 ± 874 for D. flaviventris.

Determining designation priority can inform the regulatory bodies on which habitat to designate and whether active or passive management should be applied. Without intervention, these species will be likely to face imminent extinction. In addition to being useful for government-imposed conservation management, our study can be followed by future studies as a methodology for prioritizing sites for protected area designation.

Andersen D., Jang Y. & Borzée A. (2022). Influence of landscape and connectivity on anuran conservation: population viability analyses to designate protected areas. Animal Conservation, published online. DOI: 10.1111/acv.12829

一项新的横跨东北亚的合作研究！在演化史和释放叫声的结构之间没有强相关性，释放叫声必须保守，如此才能作为有效的性识别和反捕食警报。与此前的发现相反，这里我们使用了广泛分布在东亚的花背蟾蜍Strauchbufo raddei作为研究模型，提供了景观屏障和过去冰川作用对谱系地理格局和释放叫声变异影响的证据。

这里，我们使用了化石校正的松散分子钟来估计分化的时间格局，并重建整个东亚的S. raddei线粒体谱系地理（图1）。此外，我们还推断了末次冰期蒙古-俄罗斯分支（N 类群=147）的种群动态，并比较了亨廷山山脉两侧、外贝加尔地区和阿穆尔河流域分支释放叫声的地理变化因素。分子钟显示，两个谱系之间存在基本分裂：东北和南部起源于S. raddei约15.00至9.00 个百万年前。祖先范围估测阐明了，南部谱系，通过散布作用，起源于大约6.80个百万年前，并支持了南部范围向中亚草原扩展，北部范围向今天的外贝加尔地区扩展，约2.60 个百万年前（图1）。

我们的研究结果还支持，隔离的西北亨廷分支和广泛分布在黑龙江流域的东部亨廷分支之间的释放叫声的显著差异（图2）。很可能，释放叫声的变化归因于北部分支中的一个近期的种群扩张，适用了冰川后北部避难所的模式，该模式仅限于亨廷山脉的西边缘，南部谱系的外贝加尔地区（图2）。因此，我们阐明了花背蟾蜍的释放叫声反映了分支内的谱系地理结构。

Othman S. N., Choe M., Chuang M.-F., Purevdorj Z., Maslova I., Schepina N., Jang Y. & Borzée A. (2022). Across the Gobi Desert, impact of landscape features on the biogeography and phylogeographically-structured release calls of the Mongolian Toad Strauchbufo raddei in East Asia. Evolutionary Ecology. In press. DOI: 10.1007/s10682-022-10206-4