The current decline in global biodiversity is most evident in amphibians with 41% percent of all species worldwide classified as threatened with extinction. Hence, a major challenge in amphibian conservation is the high number of threatened species, leading to a common approach of identifying priority species and regions for conservation efforts. As a part of one of 36 globally designated biodiversity hotspots, Vietnam is considered to be of particular importance for conservation action. To improve amphibian conservation in Vietnam, this study provides an updated species list and assesses their threat status by compiling data from a variety of sources. Furthermore, a Zoological Information Management System (ZIMS) analysis was conducted to determine the representation of extant amphibians from Vietnam in zoos worldwide. The batrachofauna of Vietnam is characterized by a high level of species richness and local endemism as well as a high rate of new discoveries, with more than half of the endemic species reported exclusively from their type locality, making them especially vulnerable to extinction. Up to 18% of all amphibians extant in Vietnam and 28% of endemic species are classified as threatened with extinction by the IUCN. In many cases, the IUCN Red List status is either missing or outdated, highlighting the urgent need of action. Around 14% of endemic amphibian species have been recorded exclusively from unprotected areas, suggesting prioritization for further research and conservation measures. The continuing decline in many species remains an unresolved problem. As a guide for future research and conservation measures, a list of the top 57 species was compiled. In addition, according to the ZIMS analysis, only 8% of threatened and 3% of endemic amphibian taxa from Vietnam are currently kept in zoos worldwide, and a richness analysis revealed that the highest density of husbandries is found in Europe and North America. To achieve maximum outcome for the conservation of threatened species, this study recommends a general shift by zoos towards maintaining species in greater need of captive assurance populations and breeding programs to support integrative strategies that combine in situ and ex situ conservation efforts following the IUCN’s One Plan Approach.

Amphibian conservation, conservation breeding, diversity analysis, endemic species, protected area coverage, threatened with extinction

As a profound consequence of humankind’s global impact on the natural environment, a biodiversity crisis is currently taking place (Wake and Vredenburg 2008; Tollefson 2019; Melville et al. 2021). This rapid biodiversity decline is most evident in amphibians (Gascon et al. 2007; Bishop et al. 2012; Clulow et al. 2014), of which currently more than 40% of all species in the world are under the risk of extinction (IUCN 2021). Amphibians are considered particularly vulnerable to changes, as many species have narrow habitat preferences and restricted geographic ranges (Purvis et al. 2000; Wake and Vredenburg 2008). They also occupy environments that are subject to a multitude of primarily human-caused drivers of decline (Pabijan et al. 2020).

Major threats to the amphibian species are habitat degradation and fragmentation, introduction of invasive species, over-exploitation, and climate change (Gascon et al. 2007; Halliday 2008; Bishop et al. 2012; Hussain and Pandit 2012; Meredith et al. 2016). Additionally, amphibians have been affected by the pathogenic fungi Batrachochytrium dendrobatidis and B. salamandrivorans which can induce chytridiomycosis (Kilpatrick et al. 2010; Martel et al. 2013). This disease has already been linked to the extinction of several amphibian species (Schloegel et al. 2006; Vredenburg et al. 2010). Decreasing amphibian populations are of particular concern because they are indicators of environmental stress and ecosystem health (Blaustein and Wake 1995; Welsh and Ollivier 1998; Bishop et al. 2012). Their precipitous decline serves as a warning that we are in a period of significant environmental degradation (Baillie et al. 2004). Amphibians are integral components of many ecosystems on every continent except Antarctica and may represent an important link between aquatic and terrestrial ecosystems (Whiles et al. 2006). Being predators, prey, or herbivores, and thus contributing to the trophic dynamics of many communities, the loss of amphibians is likely to have cascade impacts on other species (Blaustein 1994; Blaustein and Kiesecker 2002). Therefore, the severe amphibian declines demand urgent and collective actions to prevent another large-scale species extinction (Isaac et al. 2012; Pabijan et al. 2020).

The disappearance of amphibians is perhaps the most significant taxon-specific extinction event that conservationists are facing (Zippel et al. 2011). A major challenge in amphibian conservation is the high number of species facing extinction worldwide, as it far exceeds the resources available (Mittermeier et al. 1998; Myers et al. 2000; Mittermeier et al. 2011). Therefore, scientists are facing hurdles in determining the best approach to save the maximum number of species with the available resources and identifying which species should be prioritized initially (Myers et al. 2000). Since habitat loss is a key threat to nine out of ten threatened amphibian species (Baillie et al. 2004), it is important to identify, safeguard, and possibly extend protection, especially for sites where high rates of threatened species occur (Semlitsch 2003). Furthermore, endemic species with restricted ranges are more at risk of extinction than those with larger ranges (Meiri et al. 2017). Thus, biodiversity hotspots with high concentrations of endemic and threatened species need to be identified (Myers 1990; Mittermeier et al. 1998; Eken et al. 2004). Additionally, in cases where over-exploitation, habitat loss or pollution is the clear driver of extinction, captive assurance colonies need to be held in suitable programs, such as in zoos or conservation breeding stations, so that habitat restoration efforts and reintroductions can be a viable conservation strategy (Clulow et al. 2014).

Vietnam is located in the Indo-Burma region, one of the 36 global biodiversity hotspots, which constitute focal points for conservation efforts (Myers et al. 2000; Stork and Habel 2014; Noss et al. 2015). Due to an excessive rate of habitat loss and a large number of endemic species, Vietnam is regarded as an important area with high biodiversity conservation priority (Myers et al. 2000). In terms of biodiversity, the country is recognized as one of the top nations in the world with high species richness (Sterling et al. 2006), particularly the herpetofauna (Adler 2009). An extraordinarily large number of new species has been described from Vietnam in the last decades, in particular amphibians and reptiles (e.g., Ziegler and Nguyen 2019, see below).

The first major herpetological summary was published by Morice (1875), listing 13 amphibian species for Vietnam. From 1947, Rene Bourret published a series of papers and books on the herpetofauna of Vietnam, Laos, and Cambodia, documenting a total of 171 amphibians for the Indochinese region (Nguyen 2006). Because of the Indochinese Wars, biodiversity exploration was interrupted during the period from 1954 to 1975. Since 1975, a surge in herpetological studies of Vietnam has resulted in an enormous increase of our knowledge in this group of vertebrates (Nguyen 2006). The most recent herpetological list for Vietnam by Nguyen et al. (2009) reported 174 species of amphibians. Moreover, a large number of new amphibian discoveries from Vietnam in the last three decades also highlighted the mega-diversity of the country (Ziegler and Nguyen 2019). The outcomes of the studies and the resulting greater knowledge of the batrachofauna of Vietnam are essential for species conservation, as these data form a foundation for developing effective conservation programs.

In terms of nature conservation, the most important policy of Vietnam was the establishment of a protected area network. In 1962, the first Vietnamese National Park (NP), Cuc Phuong NP, was established in northern Vietnam. Three decades later, in 1995 with the ongoing loss of habitat and over-exploitation of the fauna and flora, the government decided to counteract by expanding the network of existing NPs and protected areas (PAs) (Sterling et al. 2006). Since then, the number of PAs has increased to a total of 33 NPs, 59 nature reserves, and 13 habitat and species conservation areas in Vietnam, including two world heritage sites (Stolton et al. 2004; Le et al. 2018, VEA 2020). With 1,077,236 ha in total, the NPs cover about 3% of the country’s area and there are plans to increase this number even further. Of the current 33 NPs, 24 are managed by provincial authorities, while the Vietnam Administration of Forestry (VNFOREST) is responsible for the other six (Le et al. 2018).

As there is no conservation assessment of endemic and threatened terrestrial vertebrate species in Vietnam available, this study focuses on amphibians. As a basis for improved conservation of Vietnamese amphibians, we analyzed the species diversity of amphibians in the country, their threat status according to IUCN (2021), national legislations as well as their distribution with particular focus on endemic and micro-endemic species. Considering the One Plan Approach, supported by the IUCN, that aims to develop integrative strategies to combine in situ and ex situ measures with groups of experts for the purpose of improved species conservation, another goal of this study was to analyze the representation of extant amphibian species from Vietnam in zoos worldwide. Such an approach has already been performed for amphibians globally (Jacken et al. 2020), but not yet for a particular region in Southeast Asia. As this study presents a topical review of the amphibian fauna of Vietnam, the first objective was to provide an updated species list for all amphibian species extant in Vietnam. We further identified hotspots based on species-level metrics (e.g., species richness, endemism, and extinction vulnerability). We assessed the proportion of endemic and threatened species, and the coverage of their distribution areas by protected areas to compile a list of the taxa, which face the greatest risk of extinction and hence are in highest need of attention in conservation work.

Although mostly up to date, the data of this study unlikely reflects the actual species number of Vietnam’s amphibian fauna. Since the cut-off date for our species list (June 2021), another six new species were described from Vietnam and are not included in this study: Gracixalus ziegleri Le, Do, Tran, Nguyen, Orlov, Ninh & Nguyen, 2021, Vietnamophryne cuongi Nguyen, Hoang, Jianping, Orlov, Ninh, Nguyen, Nguyen & Ziegler, 2021, Leptobrachella graminicola Nguyen, Tapley, Nguyen, Luong & Rowley, 2021, Boulenophrys frigida (Tapley, Cutajar, Nguyen, Portway, Mahony, Nguyen, Harding, Luong & Rowley, 2021), Micryletta melanops Poyarkov, Nguyen, Yang & Gorin, 2021, and Theloderma khoii Ninh, Nguyen, Nguyen, Hoang, Siliyavong, Nguyen, Le, Le & Ziegler, 2022. The new species discovery rate of amphibians from Vietnam is still high, as indicated by the 88 newly described species in the last decade, highlighting the outstanding amphibian diversity of the country. In addition, since the publication of the amphibian checklist by Nguyen et al. (2009), a total of 33 new country records have been documented from Vietnam, and there are an additional 12 amphibian species found in localities near the border between neighboring countries and Vietnam that are expected to occur in Vietnam. It is thus certain that additional new species will be described or recorded from Vietnam in the near future. On the other hand, taxonomic revisions, which are warranted for some of the existing taxa, may also alter the number of currently recognized amphibians in the country. For example, based on studies undertaken over the last decade, 20 of the 174 amphibian species listed by Nguyen et al. (2009) have been excluded from Vietnam, while 48 were reassigned to other genera. Moreover, the distribution data presented herein reliably reflect current scientific knowledge, but certainly do not represent the actual distribution of many species, in particular those only recently described and so far, only known from their type localities. Additionally, some of the endemic species occurring close to border areas are expected to be distributed in adjacent countries and therefore not endemic after all, such as Limnonectes nguyenorum McLeod, Kurlbaum & Hoang, 2015 which has recently been reported from China as well (Liu et al. 2022).

Amphibian endemism is not distributed evenly across the landscape of Vietnam with highest numbers of endemic species found in the Central Highlands (26 species endemic to this region), Northeast (14 species), and Northwest (11 species). The data are relatively consistent with the high species richness recorded in the regions. Specifically, the Central Highlands should be prioritized for amphibian conservation as most provincial and local endemic species are located in this region (n = 22) as well as most species classified as threatened by the IUCN Red List (n = 11). More than half of the 95 endemic species (n = 54, 57%) are only known from their type localities, emphasizing the importance of establishing local protected areas and strengthening the already existing protected area network particularly the tropical montane forests in the provinces of Kon Tum, Lam Dong and Lao Cai, for which high numbers of endemic species were recorded.

Only 73.8% of amphibians extant in Vietnam have been assigned an IUCN Red List category and not all the amphibians classified as threatened by the IUCN are protected by national legislations, highlighting the possibility of more far-reaching measures for species protection and conservation. It is noted that Decree No. 64/2019 did not include any amphibian species in the high conservation priority list. Re-evaluation and possible inclusion of endemic and threatened amphibians is highly recommended. More than half of all available threat statuses are outdated and there are differences in quality of the respective reports between previous and more recent reports (IUCN 2021), thus reaffirming the importance of re-evaluations. Further research is especially needed for 33 species classified as DD since DD species are more likely to become extinct than assessed species (Howard and Bickford 2014; Bland et al. 2015). According to the IUCN Standards and Petitions Committee (2019), the species classified as DD should be prioritized by the scientific community to generate data that will allow their proper classification into a threat category. Continued collection of basic biological and ecological information is also particularly relevant for the 51 endemic species that have not yet been evaluated by the IUCN, so that their threat status can be properly assessed.

As only four amphibian species endemic to Vietnam are listed on CITES Appendices, the other 91 endemic species are recommended to be monitored for negative impacts from the trade. In addition, an updated version of the Vietnam Red Data Book is urgently required because conservation statuses of many species from Vietnam have changed substantially since its publication in 2007.

A total of 13 endemic species (14% of all endemics) are recorded exclusively from unprotected areas. Of these species, only Amolops minutus (EN) and Theloderma ryabovi (EN), have been classified by the IUCN as threatened and should be prioritized for further research into their distribution and threats to design appropriate conservation actions, including protected area coverage.

To achieve the goals of the One Plan Approach, the integration of ex situ populations into global species conservation planning and implementation must be strengthened. According to the Convention on Biological Diversity, ex situ efforts are recommended to function as a supporting measure to in situ efforts and ideally enable reintroductions of captive populations into the wild when it is possible. Since the exact origin of most of the kept amphibian populations is not evident in ZIMS, genetic analyses are recommended to determine their provenance or priority should be placed on species or their populations with known geographic origins and endemic species from Vietnam, respectively. As zoos and other husbandry facilities only have limited resources, the selection of species should be well planned and ideally focused on species with a greater need of captive assurance populations and breeding programs. It is also important to further investigate and determine which species would benefit the most from ex situ efforts on a species-by-species basis; as a starting point, range-restricted species could be prioritized. As a specific recommendation resulting from the data compiled herein, a list of top 50 species which might profit most from research and/or conservation efforts was compiled. A ranking scheme was used to generate the list, with points given for 1) Level of endemism, 2) IUCN Red List status, and 3) Not recorded in any protected area. An additional seven species were added because they received the same scores as those ranked from 26 to 50 (Suppl. material 1: Table S13).

Although the data from ZIMS and ZTL are not complete, it is apparent from these zoo databases that only a few amphibian species from Vietnam are present in zoos worldwide. Of the species held in zoos, only a small fraction is kept in more than a hundred individuals each. Overall, a majority of held species are not a priority for conservation (listed as LC) and threatened taxa are underrepresented in zoos. We therefore recommend a general shift from common, non-threatened display species towards establishing ex situ populations of threatened species to address the amphibian crisis. In addition, nearly two-thirds of the held species are only present in one or two institutions. For the maintenance of healthy ex situ populations, a network of keeping facilities is recommended (e.g., Ziegler et al. 2020). It is also important to maintain multiple safeguard populations against unforeseen events (such as disease outbreaks or natural catastrophes) (e.g., Jacken et al. 2020). Only 11 out of 29 held amphibian species exceed the criterion of at least four holding institutions suggested by Jacken et al. (2020). Of the five threatened species (according to IUCN 2021) kept in zoos, only two, Theloderma bicolor and Tylototriton vietnamensis, are currently held in four or more institutions. Of the 13 endemic amphibian species from Vietnam which are recorded exclusively from unprotected areas, only a single species, Theloderma ryabovi (EN), is present in zoos with very few individuals in a single institution according to ZIMS. However, it can be assumed that more amphibian species and a larger number of individuals are kept and bred in captive-breeding centers in the country of origin (Harding et al. 2015) or elsewhere. Local holdings such as in the Me Linh Station for Biodiversity in Vinh Phuc Province, which also include amphibian populations (Ziegler et al. 2016), are not listed in either the ZIMS or the ZTL database. These in country facilities play a special role in developing conservation breeding programs for threatened amphibian species. The map showing the distribution of regional endemic or even micro-endemic amphibians in Vietnam underlines the necessity of scientific institutions and stations in the respective regions to consider conservation of these taxa a top priority, as they are the only ones on site and able to implement effective conservation breeding projects. As an additional measure, co-operation with zoos worldwide is recommended.

Conservation of amphibians in Vietnam could be further improved through continued field research, as well as more targeted support for the highly threatened endemic species analyzed in this study. Monitoring programs are considered especially important for 28 threatened species endemic to Vietnam to assess their population status. Further research is also crucial for the 63 endemic species not yet evaluated by the IUCN or classified as DD and the 13 endemic species exclusively recorded from unprotected areas. Besides threat status assessment, strengthening or establishing new protected areas should be considered, where required. Captive facilities in Vietnam in concert with international zoos should consider shifting their focus towards threatened amphibian species. In particular, regional stations and captive facilities can play a critical role in improving amphibian conservation through making the establishment of husbandry and breeding programs for threatened and microendemic amphibian species a top priority, following the IUCN’s One Plan Approach.

We thank Prof. Dr. Lee Grismer (Riverside) and Dr. Arne Schulze (Landau) for kindly reviewing and commenting on a previous version of the manuscript. Many thanks to our colleagues for providing photographs and the map. This research was partially supported by the Vietnam Academy of Science and Technology (Project Code: ĐLSĐ00.01/20-23).