Abstract
For a long time, it has been debated whether the two giant salamanders, Andrias japonicus from Japan and A. davidianus from China, are conspecific or heterospecific. Morphological information about their diagnostic characteristics has been limited, without considering sexual dimorphism and/or body size variation. Recently, A. davidianus, which was introduced into Japan sometime in the past, has been found to hybridize with A. japonicus in situ. Taxonomic identification of individuals involved in this unusual breeding is made based on mitochondrial and nuclear DNA analyses. This identification method is time-consuming and costly. Thus, developing easier methods of identification, such as utilizing external morphological characteristics, is urgently needed. In this study, we verify previous descriptions showing that A. davidianus has a longer relative tail length than A. japonicus, and the tubercles on the lower jaw and throat were present in both sexes of A. davidianus. In addition, many head characteristics were found to be relatively larger in A. davidianus than in A. japonicus, which were new distinguishing characters. These morphological differences help support the idea that these are heterospecific lineages. In hybrids, relative values of head width and tail length were larger than those of A. japonicus, and the tubercles on their lower jaw and throat were present as in A. davidianus, suggesting that the hybrids and A. davidianus are distinguishable from A. japonicus.
References
- Allendorf, F.W., Leary, R.F., Spruell, P. & Wenburg, J.K. (2001) The problems with hybrids: setting conservation guidelines. Trends in Ecology & Evolution, 16, 613–622. https://doi.org/10.1016/S0169-5347(01)02290-X
- Anderson, E.C. & Thompson, E.A. (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics, 160, 1217–1229. https://doi.org/10.1093/genetics/160.3.1217
- Blanchard, É. (1871) Note sur une nouvelle Salamandre gigantesque (Sieboldia Davidiana Blanch.) de la Chine occidentale. Comptes Rendus Hebdomadaires des Séances de l’Académie des Sciences, 73, 79–80.
- Boulenger, E.G. (1924) On a new giant salamander, living in the Society’s gardens. Proceedings of the Zoological Society of London, 1924, 173–174. https://doi.org/10.1111/j.1096-3642.1924.tb01494.x
- Browne, R.K., Li, H., Wang, Z., Okada, S., Hime, P., McMillan, A., Wu, M., Diaz, D., Mcginnity, D. & Briggler, J.T. (2014) The giant salamanders (Cryptobranchidae): Part B. Biogeography, ecology and reproduction. Amphibian and Reptile Conservation, 5, 30–50.
- Chai, J., Lu, C.Q., Yi, M.R., Dai, N.H., Weng, X.D., Di, M.X., Peng, Y., Tang, Y., Shan, Q.H., Wang, K., Liu, H.Z., Zhao, H.P., Jin, J.Q., Cao, R.J., Lu, P., Luo, L.C., Murphy, R.W., Zhang, Y.P. & Che, J. (2022) Discovery of a wild, genetically pure Chinese giant salamander creates new conservation opportunities. Zoological Research, 43, 469−480. https://doi.org/10.24272/j.issn.2095-8137.2022.101
- Chang, M.L.Y. (1935) Sur la salamandre geante de la Chine. Bulletin de la Société Zoologique de France, 60, 347–353.
- Gray, J.E. (1873) On a salamander (Sieboldia) from Shanghai. Journal of Natural History, 12, 188. https://doi.org/10.1080/00222937308680739
- Huxley, J. (1932) Problems of relative growth. Methuen Press, London, 276 pp.
- IUCN SSC Amphibian Specialist Group (2022) Andrias japonicus. The IUCN Red List of Threatened Species, 2022, e.T1273A177177761. Available from: https://doi.org/10.2305/IUCN.UK.2022-2.RLTS.T1273A177177761.en (accessed 18 August 2023)
- Iwama, H. (1955) Notes on the secondary sexual characters of the giant salamander, Megalobatrachus japonicus and Sieboldia davidiana from China. Bulletin of the Biogeographical Society of Japan, 16–19, 360–362. [in Japanese]
- Kaburaki, T. (1932) Some natural monuments of amphibians. Tennen-kinenbutsu Chousa-houkoku, Dobutsu no bu, 3, 92–102. [in Japanese]
- Kobara, J. (1985) O-sansyo-uo (The Japanese giant salamander). Dobutsu-sha, Tokyo, 236 pp. [in Japanese]
- Kuwabara, K. & Nakagoshi, N. (2009) Analysis on reproductive behavior of Japanese giant salamander, Andrias japonicus—Observations on the breeding behavior and notes on the video imagery. Natural History of Nishi-Chugoku Mountains, 14, 11–49. [in Japanese with English abstract]
- Liang, G., Geng, B.R. & Zhao, E.M. (2004) Andrias davidianus. The IUCN Red List of Threatened Species, 2004, e. T1272A3375181. Available from: https://doi.org/10.2305/IUCN.UK.2004.RLTS.T1272A3375181.en (accessed 18 Aug. 2023)
- Liu, C.-C. (1950) Amphibians of western China. Fieldiana, Zoology Memoirs, 2, 1–397.
- Matsui, M. (1984) Morphometric variation analyses and revision of the Japanese toads (Genus Bufo, Bufonidae). Contributions from the Biological Laboratory of Kyoto University, 26, 209–428.
- Matsui, M. (2005) Habitation confirmation of alien giant salamander species by DNA analysis. River and Watershed Environment Management, 25 pp. [in Japanese]
- Matsui, M. (2017) Effects of introduced Chinese giant salamander on native Japanese congener. Bulletin of Kansai Organization for Nature Conservation, 39, 13–19. [in Japanese with English abstract]
- Matsui, M, Tominaga, A, Liu, W.-Z & Tanaka-Ueno, T. (2008) Reduced genetic variation in the Japanese giant salamander, Andrias japonicus (Amphibia: Caudata). Molecular Phylogenetics and Evolution, 49, 318–326. https://doi.org/10.1016/j.ympev.2008.07.020
- Matsui, M. (2014) Andrias japonicus (Temminck, 1836). In: Ministry of the Environment, Japan (Ed.), Red Data Book 2014—Threatened wildlife of Japan—Reptilia/Amphibia. Gyosei, Tokyo, pp. 130–131.
- Meszoely, C. (1966) North American fossil cryptobranchid salamanders. American Midland Naturalist, 75, 495–515. https://doi.org/10.2307/2423407
- Morescalchi, A., Odierna, G. & Olmo, E. (1977) Karyological relationships between the cryptobranchid salamanders. Experientia, 33, 1579–1581. https://doi.org/10.1007/BF01934008
- National Forestry and Grassland Administration of China (2021) Official release of the updated List of Wild Animals under Special State Protection in China. Available from: http://www.forestry.gov.cn/main/586/20210208/095403793167571.html (accessed 9 April 2023) [in Chinese]
- Nishikawa, K., Matsui, M., Tanabe, S. & Sato, S. (2007) Morphological and allozymic variation in Hynobius boulengeri and H. stejnegeri (Amphibia: Urodera: Hynobiidae). Zoological Science, 24, 752–766. https://doi.org/10.2108/zsj.24.752
- Noble, G.K. (1931) The Biology of the Amphibia. McGraw-Hill Book Company, New York and London, 596 pp.
- R Core Team (2023) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: https://www.R-project.org/ (accessed 9 April 2023)
- Riley, S.P.D., Shaffer, H.B., Voss, S.R. & Fitzpatrick, B.M. (2003) Hybridization between a rare, native tiger salamander (Ambystoma californiense) and its introduced congener. Ecological Applications, 13, 1263–1275. https://doi.org/10.1890/02-5023
- Ryan, M.E., Johnson, J.R. & Fitzpatrick, B.M. (2009) Invasive hybrid tiger salamander genotypes impact native amphibians. Proceedings of the National Academy of Sciences, 106, 11166–11171. https://doi.org/10.1073/pnas.0902252106
- Sessions, S.K. (2008) Evolutionary cytogenetics in salamanders. Chromosome Research, 16, 183–201. https://doi.org/10.1007/s10577-007-1205-3
- Simoons, F.J. (1991) Food in China: A cultural and historical inquiry. CRC Press, Boca Raton, Florida, 596 pp.
- Stejneger, L. (1925) Chinese amphibians and reptiles in the United States National Museum. Proceedings of the United States National Museum, 66, 1–115. https://doi.org/10.5479/si.00963801.66-2562.1
- Tochimoto, T. (1995) Ecological studies on the Japanese giant salamander, Andrias japonicus, in the Ichi River, Hyogo Prefecture. VIII. Reproductive ecology. Part 2. Fighting. Journal of Japanese Association of Zoos and Aquariums, 36, 51–57. [in Japanese]
- Turvey, S.T., Marr, M.M., Barnes, I., Brace, S., Tapley, B., Murphy, R.W., Zhao, E. & Cunningham, A.A. (2019) Historical museum collections clarify the evolutionary history of cryptic species radiation in the world’s largest amphibians. Ecology and Evolution, 9, 10070–10084. https://doi.org/10.1002/ece3.5257
- Yoshikawa, N., Kaneko, S., Kuwabara, K., Okumura, N., Matsui, M. & Isagi, Y. (2011) Development of microsatellite markers for the two giant salamander species (Andrias japonicus and A. davidianus). Current Herpetology, 30, 177–180. https://doi.org/10.5358/hsj.30.177
- Yoshikawa, N., Matsui, M., Hayano, A. & Inoue-Murayama, M. (2012) Development of microsatellite markers for the Japanese giant salamander (Andrias japonicus) through next-generation sequencing, and cross-amplification in its congener. Conservation Genetics Resources, 4, 971–974. https://doi.org/10.1007/s12686-012-9685-7