Current Biology recently reported emerging research on the Chinese Giant Salamander in an article titled “The Chinese giant salamander exemplifies the hidden extinction of cryptic species”. This internationally collaborative project was co-lead by Prof. Che Jing at the Kunming Institute of Zoology, Chinese Academy of Sciences (KIZ, CAS), Prof. Zhang Yaping from the Center for Excellence in Animal Evolution and Genetics, CAS, and Prof. Robert Murphy, a senior visiting professor of CAS from the Royal Ontario Museum in Canada.

Che Jing with a Chinese Giant Salamander [Image by Robert Murphy]

Based on genome-level data, the researchers discovered that the Chinese Giant Salamander—Andrias davidianus—consists of at least five and likely eight species. While this is fantastic news in that it increases the endemic species diversity in China, the finding complicates the management and protection of “the salamander” by raising a red flag signaling that the status of each redefined species urgently needs evaluation.

The Chinese Academy of Sciences held a press conference to announce the research achievement. Prof. Zhang Yaping mentioned at the conference that the Chinese Academy of Sciences is the premiere leader of biodiversity research and conservation in China. Indeed, CAS has produced a series of biodiversity inventories along with evaluations of biodiversity losses. Efforts include the creation of a biodiversity inventory database, status assessments and the formation of germplasm resource banks to protect resources against potential environmental disasters. Such research, including that on genetic diversity of the Chinese Giant Salamander and its protection, requires significant cooperation of many large teams owing to huge workloads and arduous field work.

The Chinese Giant Salamander can attain a body size of 2 meters, which makes it the largest existing species of amphibian. Together with the Japanese Giant Salamander and the American Giant Salamander it comprises the small family Cryptobranchidae. The origin of this family can be traced back to the Jurassic Era (160 Mya), and hence the Chinese Giant Salamander is a “living fossil”. Among amphibians, it is “the panda of water”, and as such this iconic species holds a dominant place globally in the protection of the world’s biodiversity resources.

Previously, the Chinese Giant Salamander was widely distributed over 17 provinces through which flow the Yangtze, Yellow and Pearl rivers. Due to the damage of their habitat and overhunting since the 1950s, the densities of populations have decreased rapidly to the extent that some wild populations may have been extirpated. The Chinese Giant Salamander is listed as being a Critically Endangered Species (CE), and it appears in the CITES Convention Appendix I. In China, it has been designated a second-class protected animal species.

MtDNA haplotype clades and genetic structure of wild-caught and farm-bred Chinese giant salamanders Yan et al., 2018

Protection of the Chinese Giant Salamander has been a focal point at home and abroad. Abroad, it is listed in Appendix I of the CITES as being Critically Endangered. At home, the Chinese government has paid great attention to its protection, and invested a lot of manpower and many resources in its in situ conservation. From 1982 until now, China established 48 nature reserves (mostly after the 1980s) that refer to the protection of the Chinese Giant Salamander. Thirty-three of them (three at the national level) exist mainly for that purpose. These nature reserves cover an area of 0.17 million hectares.

In the 1970s, Yang Aisheng and others started exploring the ex situ (captive) breeding of the Chinese Giant Salamander. After decades of research and experience artificial breeding has become very successful. To increase the density of the salamanders in nature, the government frequently organizes releases of ex situ bred offspring. Although records are incomplete, at least 105,918 young salamanders have been released (data from the Internet). Meanwhile, driven by huge economic benefits, artificial breeding thrives. Since the 1990s, the price of a mature Chinese Giant Salamander has occasionally exceeded 10,000 Chinese yuan. Consequently, a large number of wild specimens have been hunted and sold to farms. This practice has created a challenge for protecting the Chinese Giant Salamander; nowadays, wild salamanders are extremely difficult to find, whereas thousands of wild-caught animals are kept in farms.

The Chinese Giant Salamander was assumed to be “one species” and its current protection is based on that view. The distinctiveness of the populations from different places has been neglected. Prof. Murphy firstly reported that the species from the Huangshan (Yellow Mountain) area differed genetically. Considering that suitable habits often isolate amphibians, including the Chinese Giant Salamander, we asked: did the wide distribution and the long history of evolution result in any significant distinctions among the populations from different places? Is the current policy of protection appropriate or effective?

To answer these questions and better protect the iconic salamander, Che Jing, Zhang Yaping and Robert Murphy and their team initiated research in 2007. After 10 years of investigation and research, and collaborations with international research units, they collected 70 wild samples and 1034 tissue samples from farms (mostly from shed skin and mouths). This allowed for further research on the genetic structure of wild and farmed populations.

Researchers visit one of Andrias davidianus farms. [Image from Chen Hongman]

As the genome of the Chinese Giant Salamander is about 50Gb in size—which is huge—the research group applied a reduced genome method to conduct a genetic analysis of the wild population. Combined with mitochondrial gene analysis, it turns out that the Chinese Giant Salamander is not a single species. The distributions of the five newly discovered species (the Shaanxi, Sichuan, Guangxi, Guizhou, and Anhui species) are closely associated with aquatic systems, and generally correspond with watersheds of the Yangtze, Yellow, Pearl and Qiantang rivers. Conservative estimations suggest that speciation occurred about 4.71 to 10.25 million years ago; each species has a long evolutionary history. Further, two additional species were found in farms only, and together with the recorded population on the Tibet Plateau (at 4000 meters) it is possible that at least eight species of Chinese Giant Salamander exist, but this conclusion requires further study. The discovery of such vast diversity, made possible by new genomic technologies, is astounding especially in an already well-studied giant amphibian.

Species are the basic unit for protection and management initiatives. Based on past experience and the assumption of one species, ex situ breeding and releasing occurred in nature reserves without considering the geographic origins of the breeding stock. This approach risked the possible genetic mixing of species, and even the substitution of one locally adapted species for another. Such actions can lead to the loss of genetic resources or even species extinction as well as ineffective protection of the native species. A random sampling of the farm population found that 78.82% of the individuals originated from Shaanxi. From 2013 to 2016, the Zoological Society of London launched a conservation program for Chinese giant salamanders. The ZSL supported and cooperated with local Chinese scientists to conduct field and questionnaire surveys in China. The Kunming Institute of Zoology, Chinese Academy of Sciences undertook the genetics analysis of the collected samples, and found that the maternal line of the 12 wild-caught individuals from Shaanxi, Guizhou and Guangxi all originated from Shaanxi. Further, taking Guizhou as an example, analysis of microsatellite DNA indicated that although the randomly sampled 100 farmed individuals originated from different matrilines, they had been blended into one species at the nuclear gene level. In another words, uninformed efforts to protect the species may have accelerated extinction via genetic homogenization.

The new genetic technologies efficiently yield invaluable insights into the Chinese Giant Salamanders. Now it is urgently necessary to apply data from these technologies to the formation of a new policy for protection and management of the species. Researchers must comprehensively analyze the population size of each clade species, noting its native genetic diversity, history and structure, and area of distribution. Further, it is necessary to establish a standard technology for genetic assessments and set guidelines for farming. The release of animals without genetic verification and disease assessments should be banned; released disease-free Chinese Giant Salamanders should be identified genetically. The researchers hope that collaborative efforts can pave the way to protection of other endangered species.

Yan Fang from the Kunming Institute of Zoology, Chinese Academy of Sciences is the first author. Che Jing, Zhang Yaping and Robert Murphy are the joint corresponding authors. This work is supported by the programs of the Strategic Priority Research Program, CAS (XDPB020406), State Key Laboratory of Genetic Resources and Evolution, the Kunming Institute of Zoology, CAS (GREKF15-10), the National Natural Science Foundation of China (NSFC 31090250, 31360144), the Darwin Initiative (Project No. 19-003) and EDGE programme from the Zoological Society of London, the Ocean Park Conservation Foundation of Hong Kong, China's Biodiversity Observation Network CAS, the Animal Branch of the Germplasm Bank of Wild Species, CAS (Large Research Infrastructure Funding), and the Natural Science Foundation of Anhui Provincial Bureau of Education (KJ2014A244). JC is supported by the NSFC (31622052) and the Youth Innovation Promotion Association CAS. FY is supported by the NSFC (31401958) and the West Light Project of CAS. RWM is supported by the CAS President's International Fellowship Initiative (PIFI) and the ROM foundation.

Source: Kunming Institute of Zoology, Chinese Academy of Sciences

For more information, please contact:

Dr. Che Jing

E-mail: chej@mail.kiz.ac.cn