Salamanders of the Old World: The Salamanders of Europe, Asia and Northern Africa 9050114857, 9789050114851

Table of contents :
Salamanders of the Old World
Hynobiidae Cope, 1859
Plethodontidae Gray, 1850
Proteidae Gray, 1825
Proteus Laurenti, 1768
Salamandridae Goldfuss, 1820

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Salamanders of the Old World Max Sparreboom The Salamanders of Europe, Asia and Northern Africa

K N N V P U BL I S H I N G

Colophon Title: Salamanders of the Old World Text: © Max Sparreboom 2014 Maps: © Wouter Beukema 2014; International Union for the Conservation of Nature (IUCN) Artwork: © Bas Teunis 2014 Endpapers: © Bas Teunis 2014. Salamandra salamandra body and head; Lissotriton helveticus male and female from Thiesmeier & Grossenbacher (2004); Triturus cristatus male from Grossenbacher & Thiesmeier (2003); drawings of mouth, skull and skeleton of Salamandra salamandra made for this book. Photos: Photographers are credited in the photo legends and hold copyright of their photos. Photo editing: Bas Teunis. Coverphoto: Hynobius glacialis © You Chung Wei 2014. Photos on back cover: © Max Sparreboom 2014. Salamandra salamandra longirostris; Ommatotriton vittatus; Paradactylodon mustersi; Tylototriton verrucosus larva. Editorial support: Dr Andrew Richford Design: Elske Verharen, Oxedio (cover & innerwork) Layout: Niko Korenhof, Naturalis Biodiversity Center, Leiden © KNNV Publishing, Zeist, the Netherlands First edition 2014

Credits for cited text passages: Beebee, T.J.C. & Griffiths, R.A., (2000). Amphibians and Reptiles. A Natural History of the British Herpetofauna. Harper Collins Publishers, London (summary description of courtship behaviour of Lissotriton vulgaris). Griffiths, R.A., (1996). Newts and Salamanders of Europe. Poyser Natural History, London (passages on eggs, larvae and livebearing, and on threats and conservation in the Introduction). Houck, L.D. & Arnold, S.J., (2003). ‘Courtship and Mating Behavior.’ Pp. 383-424 in: Sever, D.M. (Ed.), (2003). Reproductive Biology and Phylogeny of Urodela. Science Publishers, Inc., Enfield (NH), USA, Plymouth, UK (summaries of reproduction and courtship behaviour in the Introduction). Larson, A., Wake, D. & Devitt, T., (2006). The Tree of Life Project tolweb.org/Caudata/ (passages in genus and family descriptions). Mitchell, J. & Gibbons, W., (2010). Salamanders of the Southeast. The University of Georgia Press, Athens and London (passages on plethodontids, feeding and defence mechanisms in the Introduction). Pasmans, F. Passage on chytridiomycosis in Introduction. Pasmans, F., Bogaerts, S., Janssen, H. & Sparreboom, M., (in press) Schwanzlurche halten und züchten (Captive Husbandry of Salamanders and Newts). Natur und Tierverlag, Münster (passages in the Introduction). Thorn, R., (1969). Les salamandres d’Europe, d’Asie et d’Afrique du Nord. Editions Paul Lechevalier, Paris (translations of species descriptions throughout the book).

This publication was supported by Naturalis Biodiversity Center, Leiden, The Netherlands

Printer: Trento ISBN: 978 90 5011 4851 NUR: 433 www.knnvpublishing.nl Discovering nature and getting close to it KNNV Publishing specialises in unique works on nature and landscape: easily accessible field guides, conservation manuals, distribution atlases and much more. KNNV Publishing also produces chronicles on nature conservation, beautifully illustrated books on natural, cultural and landscape history, travel guides, children’s books and, last but not least, the journal ‘Natura’. All these works help to make valuable knowledge gathered by scientists and amateur researchers available to a broad public. By producing these works, KNNV Publishing contributes to nature conservation and to the enjoyment of nature in the Netherlands. No part of this book may be reproduced in any form by print, photocopy, microfilm or any other means without the written permission from the publisher. 2

Salamanders of the Old World | Colophon

Table of contents Foreword by J.W. Arntzen .......................................................................... 7 Preface ...................................................................................................................... 9 Acknowledgements ..................................................................................... 13 Introduction ...................................................................................................... 14 Cryptobranchidae Fitzinger, 1826 ................................................... 26 Andrias Tschudi, 1837 ...................................................................................... 27 Andrias davidianus (Blanchard, 1871) ................................................. 27 Andrias japonicus (Temminck, 1836) .................................................... 30

Hynobius takedai Matsui & Miyazaki, 1984 ....................................... 92 Hynobius tokyoensis Tago, 1931 .............................................................. 93 Hynobius tsuensis Abé, 1922 ..................................................................... 95 Hynobius turkestanicus Nikolskii, 1910 ............................................... 96 Hynobius yangi Kim, Min & Matsui, 2003 .......................................... 97 Hynobius yatsui Oyama, 1947 .................................................................. 98 Hynobius yiwuensis Cai, 1985 ................................................................... 99 Liua Zhao & Hu, 1983 ..................................................................................... 103 Liua shihi (Liu, 1950) ................................................................................... 103 Liua tsinpaensis (Liu & Hu, 1966) ......................................................... 105 Onychodactylus Tschudi, 1838 ................................................................... 107 Onychodactylus fischeri (Boulenger, 1886) ...................................... 107 Onychodactylus japonicus (Houttuyn, 1782) ................................. 109 Onychodactylus kinneburi Yoshikawa, Matsui, Tanabe & Okayama, 2013 .............................................................................................. 112 Onychodactylus koreanus Min, Poyarkov & Vieites, 2012 ......... 113 Onychodactylus nipponoborealis Kuro-o, Poyarkov & Vieites, 2012 ................................................................................................... 116 Onychodactylus tsukubaensis Yoshikawa & Matsui, 2013 ....... 118 Onychodactylus zhangyapingi Che, Poyarkov, Li & Yan, 2012 119 Onychodactylus zhaoermii Che, Poyarkov & Yan, 2012 ............. 121 Pachyhynobius Fei, Qu & Wu, 1983 .......................................................... 123 Pachyhynobius shangchengensis Fei, Qu & Wu, 1983 .................. 123 Paradactylodon Risch, 1984 ........................................................................ 125 Paradactylodon gorganensis (Clergue-Gazeau & Thorn, 1979) 125 Paradactylodon mustersi (Smith, 1940) ........................................... 126 Paradactylodon persicus (Eiselt & Steiner, 1970) ......................... 128 Pseudohynobius Fei & Ye, 1983 ................................................................... 131 Pseudohynobius flavomaculatus (Hu & Fei, 1978) ......................... 132 Pseudohynobius guizhouensis Li, Tian & Gu, 2010 ........................ 133 Pseudohynobius jinfo Wei, Xiong, Hou & Zeng, 2009 .................. 134 Pseudohynobius kuankuoshuiensis Xu & Zeng, 2007 .................. 135 Pseudohynobius puxiongensis (Fei & Ye, 2000) ............................. 136 Pseudohynobius shuichengensis Tian, Gu, Sun & Li, 1998 ......... 137 Ranodon Kessler, 1866 .................................................................................. 139 Ranodon sibiricus Kessler, 1866 ............................................................ 139 Salamandrella Dybowski, 1870 ................................................................ 142 Salamandrella keyserlingii Dybowski, 1870 ................................... 142 Salamandrella tridactyla (Nikolskii, 1906) ...................................... 145

Hynobiidae Cope, 1859 .............................................................................. 33 Batrachuperus Boulenger, 1878 .................................................................. 39 Batrachuperus karlschmidti Liu, 1950 .................................................. 39 Batrachuperus londongensis Liu & Tian, 1978 .................................. 41 Batrachuperus pinchonii (David, 1872) ................................................ 43 Batrachuperus taibaiensis Song, Zeng, Wu, Liu & Fu, 2001 ...... 45 Batrachuperus tibetanus Schmidt, 1925 ............................................. 46 Batrachuperus yenyuanensis Liu, 1950 ................................................ 49 Hynobius Tschudi, 1838 .................................................................................... 51 Hynobius abei Sato, 1934 ............................................................................. 51 Hynobius amjiensis Gu, 1992 ...................................................................... 53 Hynobius arisanensis Maki, 1922 ............................................................ 54 Hynobius boulengeri (Thompson, 1912) .............................................. 56 Hynobius chinensis Günther, 1889 ......................................................... 57 Hynobius dunni Tago, 1931 ......................................................................... 59 Hynobius formosanus Maki, 1922 ........................................................... 60 Hynobius fuca Lai & Lue, 2008 ................................................................. 62 Hynobius glacialis Lai & Lue, 2008 ......................................................... 63 Hynobius guabangshanensis Shen, 2004 ........................................... 65 Hynobius hidamontanus Matsui, 1987 ................................................. 66 Hynobius hirosei Lantz, 1931 ..................................................................... 68 Hynobius katoi Matsui, Kokuryo, Misawa & Nishikawa, 2004 . 69 Hynobius kimurae Dunn, 1923 ................................................................... 71 Hynobius leechii Boulenger, 1887 ........................................................... 72 Hynobius lichenatus Boulenger, 1883 .................................................... 74 Hynobius maoershanensis Zhou, Jiang & Jiang, 2006 .................. 76 Hynobius naevius (Temminck & Schlegel, 1838) ............................. 77 Hynobius nebulosus (Temminck & Schlegel, 1838) ......................... 79 Plethodontidae Gray, 1850 .................................................................. 147 Hynobius nigrescens Stejneger, 1907 ..................................................... 81 Atylodes Gistel, 1868 ..................................................................................... 148 Hynobius okiensis Sato, 1940 ................................................................... 83 Atylodes genei (Temminck & Schlegel, 1838) ................................. 148 Hynobius quelpaertensis Mori, 1928 ..................................................... 84 Karsenia Min, Yang, Bonett, Vieites, Brandon & Wake, 2005 ... 151 Hynobius retardatus Dunn, 1923 ............................................................ 86 Karsenia koreana Min, Yang, Bonett, Vieites, Brandon & Hynobius sonani (Maki, 1922) ................................................................... 89 Wake, 2005 ..................................................................................................... 151 Hynobius stejnegeri Dunn, 1923 ............................................................... 91 Speleomantes Dubois, 1984 ........................................................................ 153

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Speleomantes ambrosii (Lanza, 1955) ................................................. 153 Speleomantes flavus (Stefani, 1969) .................................................... 156 Speleomantes imperialis (Stefani, 1969) ........................................... 157 Speleomantes italicus (Dunn, 1923) ..................................................... 159 Speleomantes sarrabusensis Lanza, Leo, Forti, Cimmaruta, Caputo & Nascetti, 2001 ......................................................................... 160 Speleomantes strinatii (Aellen, 1958) ................................................. 162 Speleomantes supramontis (Lanza, Nascetti & Bullini, 1986) ................................................................................................... 164

Proteidae Gray, 1825 ................................................................................ 166 Proteus Laurenti, 1768 .................................................................................. 166 Proteus anguinus Laurenti, 1768 .......................................................... 167 Salamandridae Goldfuss, 1820 ....................................................... 170 Calotriton Gray, 1858 ...................................................................................... 171 Calotriton arnoldi Carranza & Amat, 2005 ...................................... 171 Calotriton asper (Dugès, 1852) .............................................................. 172 Chioglossa Bocage, 1864 .............................................................................. 176 Chioglossa lusitanica Bocage, 1864 ..................................................... 176 Cynops Tschudi, 1838 .................................................................................... 180 Cynops chenggongensis Kou & Xing, 1983 ....................................... 180 Cynops cyanurus Liu, Hu & Yang, 1962 ............................................... 181 Cynops ensicauda (Hallowell, 1861) .................................................... 184 Cynops fudingensis Wu, Wang, Jiang & Hanken, 2010 .............. 188 Cynops glaucus Yuan, Jiang, Ding, Zhang & Che, 2013 .............. 190 Cynops orientalis (David, 1873) ............................................................ 190 Cynops orphicus Risch, 1983 .................................................................... 192 Cynops pyrrhogaster (Boie, 1826) ......................................................... 193 Cynops wolterstorffi (Boulenger, 1905) .............................................. 197 Echinotriton Nussbaum & Brodie, 1982 ................................................ 199 Echinotriton andersoni (Boulenger, 1892) ........................................ 199 Echinotriton chinhaiensis (Chang, 1932) .......................................... 202 Euproctus Gené, 1839 ................................................................................... 206 Euproctus montanus (Savi, 1838) ........................................................ 206 Euproctus platycephalus (Gravenhorst, 1829) .............................. 210 Ichthyosaura Sonnini de Manoncourt & Latreille, 1801 ............... 213 Ichthyosaura alpestris (Laurenti, 1768) ............................................ 213 Laotriton Dubois & Raffaëlli, 2009 ........................................................ 218 Laotriton laoensis (Stuart & Papenfuss, 2002) ............................ 218 Lissotriton Bell, 1839 ..................................................................................... 221 Lissotriton boscai (Lataste, 1879) ....................................................... 221 Lissotriton helveticus (Razoumowsky, 1789) ................................. 224 Lissotriton italicus (Peracca, 1898) .................................................... 227 Lissotriton montandoni (Boulenger, 1880) ..................................... 229 Lissotriton vulgaris (Linnaeus, 1758) .................................................. 233 Lyciasalamandra Veith & Steinfartz, 2004 ........................................ 241 Lyciasalamandra antalyana (Basoglu & Baran, 1976) ............... 242 Lyciasalamandra atifi (Basoglu, 1967) ............................................... 243 Lyciasalamandra billae (Franzen & Klewen, 1987) ...................... 244 Lyciasalamandra fazilae (Basoglu & Atatür, 1974) ...................... 245 4

Salamanders of the Old World | Table of contents

Lyciasalamandra flavimembris (Mutz & Steinfartz, 1995) ...... 246 Lyciasalamandra helverseni (Pieper, 1963) ..................................... 247 Lyciasalamandra luschani (Steindachner, 1891) .......................... 249 Mertensiella Wolterstorff, 1925 ............................................................... 252 Mertensiella caucasica (Waga, 1876) ................................................ 252 Neurergus Cope, 1862 .................................................................................. 256 Neurergus crocatus Cope, 1862 ............................................................ 256 Neurergus derjugini (Nesterov, 1916) ............................................... 258 Neurergus kaiseri Schmidt, 1952 ......................................................... 260 Neurergus strauchii (Steindachner, 1887) ....................................... 262 Ommatotriton Gray, 1850 ........................................................................... 266 Ommatotriton ophryticus (Berthold, 1846) ................................... 266 Ommatotriton vittatus (Gray, 1835) ................................................... 269 Pachytriton Boulenger, 1878 ..................................................................... 272 Pachytriton archospotus Shen, Shen & Mo, 2008 ....................... 272 Pachytriton brevipes (Sauvage, 1876) ................................................ 273 Pachytriton changi Nishikawa, Matsui & Jiang, 2012 ................ 275 Pachytriton feii Nishikawa, Jiang & Matsui, 2011 ........................ 277 Pachytriton granulosus Chang, 1933 .................................................. 278 Pachytriton inexpectatus Nishikawa, Jiang, Matsui & Mo, 2011 279 Pachytriton moi Nishikawa, Jiang & Matsui, 2011 ....................... 281 Paramesotriton Chang, 1935 ..................................................................... 283 Paramesotriton caudopunctatus (Liu & Hu,1973) ........................ 283 Paramesotriton chinensis (Gray, 1859) ............................................. 286 Paramesotriton deloustali (Bourret, 1934) ...................................... 288 Paramesotriton fuzhongensis Wen, 1989 ........................................ 290 Paramesotriton guangxiensis (Huang, Tang & Tang, 1983) .... 292 Paramesotriton hongkongensis (Myers & Leviton, 1962) ......... 293 Paramesotriton labiatus (Unterstein, 1930) .................................. 296 Paramesotriton longliensis Li, Tian, Gu & Xiong, 2008 ............. 298 Paramesotriton maolanensis Gu, Chen, Tian, Li & Ran, 2012 299 Paramesotriton wulingensis Wang, Tian & Gu, 2013 .................. 300 Paramesotriton yunwuensis Wu, Jiang & Hanken, 2010 ......... 301 Paramesotriton zhijinensis Li, Tian & Gu, 2008 ............................ 302 Pleurodeles Michahelles, 1830 ................................................................. 304 Pleurodeles nebulosus (Guichenot, 1850) ......................................... 304 Pleurodeles poireti (Gervais, 1835) ...................................................... 305 Pleurodeles waltl Michahelles, 1830 .................................................. 307 Salamandra Garsault, 1764 ......................................................................... 311 Salamandra algira Bedriaga, 1883 ....................................................... 311 Salamandra atra Laurenti, 1768 ........................................................... 314 Salamandra corsica Savi, 1838 ............................................................... 318 Salamandra infraimmaculata (Martens, 1885) ............................ 320 Salamandra lanzai Nascetti, Andreone, Capula & Bullini, 1988 .................................................................................................... 323 Salamandra salamandra (Linnaeus, 1758) ....................................... 325 Salamandrina Fitzinger, 1826 .................................................................... 335 Salamandrina perspicillata (Savi, 1821) ............................................ 335 Salamandrina terdigitata (Bonnaterre, 1789) ................................ 338 Triturus Rafinesque, 1815 ........................................................................... 340 Triturus carnifex (Laurenti, 1768) ........................................................ 340

Triturus cristatus (Laurenti, 1768) ...................................................... 342 Triturus dobrogicus (Kiritzescu, 1903) ............................................... 345 Triturus ivanbureschi Arntzen & Wielstra, 2013 .......................... 346 Triturus karelinii (Strauch, 1870) ......................................................... 348 Triturus macedonicus (Karaman, 1922) ........................................... 350 Triturus marmoratus (Latreille, 1800) .............................................. 351 Triturus pygmaeus (Wolterstorff, 1905) ............................................ 354 Tylototriton Anderson, 1871 ....................................................................... 357 Tylototriton asperrimus Unterstein, 1930 ........................................ 358 Tylototriton broadoridgus Shen, Jiang & Mo, 2012 ...................... 359 Tylototriton dabienicus Chen, Wang & Tao, 2010 ........................ 360 Tylototriton daweishanensis Zhao, Rao, Liu, Li & Yuan, 2012 361 Tylototriton hainanensis Fei, Ye & Yang, 1984 ................................ 361 Tylototriton kweichowensis Fang & Chang, 1932 ......................... 362 Tylototriton lizhenchangi Hou, Zhang, Jiang, Li & Lü, 2012 .... 364 Tylototriton notialis Stuart, Phimmachak, Sivongxay & Robichaud, 2010 ........................................................................................... 365 Tylototriton panhai Nishikawa, Khonsue, Pomchote & Matsui, 2013 .................................................................................................. 366 Tylototriton pseudoverrucosus Hou, Gu, Zhang, Zeng, Li & Lü, 2012 .................................................................................................... 367 Tylototriton shanjing Nussbaum, Brodie & Yang, 1995 ............. 369 Tylototriton taliangensis Liu, 1950 ....................................................... 371

Tylototriton uyenoi Nishikawa, Khonsue, Pomchote & Matsui, 2013 ................................................................................................... 372 Tylototriton verrucosus Anderson, 1871 ............................................ 373 Tylototriton vietnamensis Böhme, Schöttler, Nguyen & Köhler, 2005 .................................................................................................... 378 Tylototriton wenxianensis Fei, Ye & Yang, 1984 ............................ 380 Tylototriton yangi Hou, Zhang, Zhou, Li & Lü, 2012 .................... 381 Tylototriton ziegleri Nishikawa, Matsui & Nguyen, 2013 ......... 382

References ........................................................................................................ 387 Recommended general literature on salamanders ..... 419 Websites ............................................................................................................ 420 Glossary ............................................................................................................. 421 Index of scientific names ................................................................... 424 Maps of Europe and Northern Africa, the Near East, South-East and East Asia ................................................................... 426 About the author ......................................................................................... 431

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Salamanders of the Old World

Foreword This book is about salamanders which, together with frogs, toads and the lesser known ‘worm-salamanders’ form the class Amphibia. Salamanders are an ancient order of amphibians that arose during the Carboniferous period, some 350-300 million years ago, and form a separate group from the frogs and toads. They have a modest, inconspicuous lifestyle, and are seldom seen and seemingly unspectacular. Yet, if you take a closer look, you will find a group that is rich and varied, with wonderful adaptations to life in a variety of habitats in the northern hemisphere and a part of the tropics. Salamanders live and breed in a wide diversity of habitats. Adults of some species gather in ponds and mountain streams while others mate in caves or in high altitude lakes. Some are obliged to inhabit aquatic environments while others have developed morphological features that have freed them from the water and are able to give birth to fully metamorphosed offspring. Salamanders – what fascinating creatures they are! For many of us, capturing a live salamander from a ditch or a pond – an animal that you can actually hold and observe in detail without the need for binoculars or a microscope – may have been the trigger for a wider interest in natural history. Some have gone further and started observing the lives of salamanders in a terrarium. This was indeed the path followed by the author of this book, which at first led him to write a multitude of meticulous publications on the mating behaviour of the species that he observed at home, as well as natural historical accounts of species seen on holidays and during wider travels and surveys in the field. All of these studies have culminated in this complete overview and fully up to date account of all the salamander species that occur in Europe, Asia and Africa north of the Sahara. The species accounts are concise and to the

point and the illustrations … well, look for yourself ! In this book, the author presents a remarkably concise, yet complete, treatise with a more than encyclopedic vision. The scope of the work is impressive – producing not just an identification guide, but also a compendium of data on the distribution, ecology and systematics of these animals, with an emphasis on natural history and reproductive biology. The scientific depth of the book is reflected in the abundance of technical papers that the author has referred to in its preparation. This book fills a long-standing gap. Nearly half a century has passed since Robert Thorn’s naturalist guide ‘Les Salamandres’ (Paris, 1969), and the number of species recognised has increased from about 70 to more than 160 today. We now know more about salamander habitat preferences, behaviour, mating systems, interactions with the environment and their strategies for coping with fluctuating environments, and also about the threats posed to salamander populations and species and the risks of losing them. Recent developments in molecular genetics are also reflected in the book’s coverage through the drastically improved understanding of the geographical variation within species and the amphibian species tree of life. These discoveries allow us to better understand salamander morphology in relation to the environment and the whys and hows of evolutionary change. We can begin to see not just what the different species look like and where they live, but also how they function, and how individual species characteristics have developed – from the vivid colouration of poison glands to the flamboyant crest that the males of some species sport during the mating season. This extraordinary book will serve as a baseline for my continuing passion for salamanders and as an inspiration for new generations of naturalists and students to come. J.W. Arntzen Naturalis Biodiversity Center, Leiden June 2014

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Salamanders of the Old World

Preface The primary purpose of this work is to provide a reference for researchers, naturalists, conservation biologists, biology students, terrarium hobbyists, and others who need a documented introduction to the salamander fauna of Europe, Northern Africa and Asia. This vast area covers the Palearctic Realm, but also ranges across the northern parts of the Indian peninsula and peninsular South-East Asia, into the southern part of China (the Oriental or Indo-Malayan Realm). The title Salamanders of the Old World distinguishes the salamander fauna of this area from the salamanders occurring in the Americas or New World.

History

In 1969 Robert Thorn published his treatise, Les salamandres d’Europe, d’Asie et d’Afrique du Nord. This book – dated to 1968, but actually published in 1969 – has become a classic and served for many years as the primary reference to the salamanders of Europe, Northern Africa and Asia. Many more species have been described in the scientific literature in the meantime, and new insights into salamander phylogeny, taxonomy, ecology and behaviour have been published. Although several books describing the Old World salamander species appeared between 1969 and 2013, none, in my view, have satisfied the need for a comprehensive, up-to-date summary of the published literature, as had Thorn’s book in its day. These days information on salamanders is scattered over a broad range of books and journals in a multitude of languages. This new book sets out to synthesise this widely spread information into a format that is both useful to the scientist and also accessible to the layman. It follows the structure of Thorn’s book and I have used many of his descriptions, translated with minor modifications. Robert Thorn died in November 2012 at the age of 87.

On-line catalogue Distribution of the salamanders of the Old World, covered in this book.

This book started life as an on-line catalogue that could be accessed through the website of the Naturalis Biodiversity Center, Leiden. During the preparation of this catalogue, reactions and comments from peers were

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Robert Thorn in Gersfeld 1995. Photo: Max Sparreboom. ◀◀

Title Page of Les salamandres d’Europe, d’Asie et d’ Afrique du Nord by R. Thorn, published in 1969 (1968). 9

incorporated into the species entries and many friends and colleagues were kind enough to make their photos available for the website, and later for the book. While the book is the result of a joint effort, of course I remain responsible for any errors in it.

Structure

The book is structured as follows. Morphological details of species descriptions, and karyological and genetic analyses are only summarily referred to. The descriptions are mostly limited to external characteristics and should enable identification of most species in the field. Some species are difficult to identify on the basis of external characteristics alone and can only be identified with certainty by using DNA analysis and locality data. This is especially true for plethodontid and hynobiid salamanders. New species are still being described, especially in Asia. Some are entirely unexpected, such as the plethodontid salamander Karsenia koreana, described in 2005 from specimens collected in Korea. I do not discuss the evolutionary history of salamanders, nor the methods used to study it, but refer the reader to the relevant literature. This book does not aspire to making taxonomic statements but takes a conservative approach to proposals for nomenclatural changes and the recognition of new species. The reader is referred to other sources for field identification guides and keys. In this book the emphasis is on natural history and reproductive biology.

Synonyms

Synonyms of species’ names tell the taxonomic history of a given species and many books include lists of synonyms at the beginning of each species entry. I have omitted such lists here and refer the reader to the well-documented lists of synonyms on the website by Frost (Amphibian Species of the World, 2013), whose taxonomic decisions are often followed.

Photographs

Most species are depicted in colour, as far as possible in their natural habitats, although diagnostic characters can often be better shown if the animals are photographed in small aquariums, where they are housed temporarily. Where possible, both sexes and different life stages are illustrated. The photos were taken of living specimens, and the collecting locality of the individual depicted is given wherever this is known.

Description

Taxonomy is the scientific study of the classification and naming of plants, animals, and other organisms. Scientists studying taxonomy name and classify salamanders in ways that reflect ancestral genetic relationships among species. Closely related species are placed within the same genus, and closely related genera are placed within the same family. In this book, the salamander species descriptions are

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Salamanders of the Old World | Preface

ordered systematically, according to the family to which they belong: Cryptobranchidae – giant salamanders; Hynobiidae – a large group of mainly Asiatic, externally fertilising salamanders; Plethodontidae – a large family of lungless salamanders mainly distributed in the Americas, but with some representatives in Europe and Asia; Proteidae – an enigmatic family of neotenic aquatic salamanders; and Salamandridae – a large and diverse family of newts and salamanders. The hierarchy of the taxa commonly used in classification is order – family – genus – species – subspecies. A species comprises individual animals that can interbreed with each other and are distinguished from individuals assigned to other species. In most cases members of a species can be recognised by their outward appearance, but sometimes other characters are used, such as features of internal anatomy or molecular signature, such as distinctive body chemistry, the kinds of proteins present, or the detailed makeup of the DNA that forms their genes. In this book, the species descriptions are ordered within each family in alphabetical order of their Latin names. The first name indicates the genus to which the species belongs; the second name is the species name. The name is followed by the name of the author who first described the animal. If the species has later been transferred to another genus, due to new taxonomic insights, the author’s name is placed in brackets. Usually only one English name is given here, which for many Asiatic species is an arbitrary name anyway. More English names, as well as names used in other languages, are cited on some websites (Amphibian Species of the World; AmphibiaWeb) and are omitted here. Morphological and anatomical details are referred to in a number of species descriptions. The figures on the insides of the cover illustrate the relevant body parts and their names, such as details of the mouth and teeth, and features of the skeleton and external morphology. The technical morphological terms are explained more fully in the glossary.

Colour

The descriptions of colour refer to the colour patterns of living animals. Specimens kept in alcohol usually fade in colour with time.

Length

This refers to the average, or occasionally the maximum, total length of adult animals, measured from snout to tail-tip. The literature often refers to snout-vent length as a measure, because it is more stable than total length. Tails are frequently incomplete or regenerated, thus giving an unreliable measure of total length. However, snout-vent length can be measured in various ways, for example either including or excluding cloaca length, and this can be confusing if the measuring method is not stated explicitly.

Diagnosis

This paragraph summarises the principal characteristics that distinguish this species from other species of the same genus. In a so-called monotypic genus, where the genus contains only one species, the diagnosis refers to the genus (for example Proteus, Chioglossa, Laotriton). Taxonomists consider it useful and practical to coin subspecific names to draw attention to interesting regional variation within a species. Regional variation is particularly common in species with very wide distributions such as the Smooth Newt (Lissotriton vulgaris) and Fire Salamander (Salamandra salamandra) and regionally different forms are conveniently labeled as different subspecies. The nominate subspecies is the form of that species containing the type specimen from which the original species description derives and retains the name of that species in the subspecies part of the Latin name, e.g. Cynops ensicauda ensicauda from the Amami group of the Ryukyu Islands. Cynops ensicauda popei is the subspecies described from specimens collected in the Okinawa island group, and named after the researcher Clifford H. Pope. Early descriptions of new salamander species were based on taxonomists’ knowledge of form and colouration of the animals and recognition that the specimen in question was different enough to receive a new name. Molecular biology has greatly improved our understanding of the relationships between salamander species, genera and families. Modern techniques allow taxonomists to examine the genetic structure of species, leading to a much better understanding of the relationships between populations occurring in different areas. Some salamander species described on the basis of genetic differences are so similar in appearance to other species that they cannot be differentiated by external morphological characters. They can only be discriminated using molecular techniques or their geographic location. Examples include the southern European species of Speleomantes and the Japanese species of Hynobius. Many new species have been described in the last decades and more will doubtless be discovered in the coming years.

Eggs and larvae

Eggs, larvae, and their development into metamorphosed young salamanders are summarised in this section. A typological survey of different types of hynobiid egg sacs is given in the Hynobiidae family description.

Distribution

This paragraph gives the geographical range in which the species is found. It follows the information in the distribution chapters of the IUCN website, on which most of the maps are based. For many species the distribution is poorly known, especially those that are rare or extremely secretive. So far as possible, the shaded areas on species’ range maps are based on sites of documented records. The maps on the

AmphibiaWeb website provide links to the museum catalogue numbers of these voucher specimens. The distribution maps in this book generally follow the latest maps published by the International Union for the Conservation of Nature (IUCN); many of these maps were modified by Wouter Beukema and myself to reflect the most recent information on distribution taken from the literature. We have agreed to share updated maps with the IUCN.

Habitat

This paragraph briefly describes the landscape types in which the species prefers to live. Many species occupy a variety of habitats; those that need a water body for reproduction, such as ponds, small streams or rivers, often move onto land after the breeding season is over and lead a secretive life under stones and logs, or underground. Altitude, climate, soil structure, presence of water and vegetation all determine the character of a habitat.

Behaviour

This paragraph covers a range of behaviour patterns, such as seasonal, diurnal or nocturnal activity patterns, feeding behaviour, reaction to predators, hibernation, aestivation, and reproductive behaviour.

Threats and conservation

The main threats to a species and its habitat are listed here, following the IUCN Red List categories: Not Evaluated, Data Deficient, Least Concern, Near Threatened, Vulnerable, Endangered, Critically Endangered, or Extinct in the wild (IUCN, 2013; Stuart et al., 2008). Many species are protected by local, national or international legislation. For detailed data on protective legislation in European and Asian countries the reader is referred to the national and regional herpetofauna literature.

Observations in captivity

Much of what is known about salamander behaviour stems from observations in captivity made in the labs of professional biologists and the terrariums of hobbyists. Most of our knowledge regarding successful breeding of amphibians comes from the work of dedicated hobbyists. This paragraph summarises reliable first-hand reports of captive breeding in the hobbyist literature where this is relevant to our knowledge of the species’ biology.

Comments

The comments sections cover a variety of different subjects, including evolutionary history, issues under debate, or suggestions for further reading.

References

All references quoted in the species descriptions are cited in full at the back of the book. They do not constitute an exhaustive bibliography but are the sources consulted in gathering the information contained in the species entries. A separate section in the back of this book lists informative and 11

authoritative websites, but because websites are liable to change or may even be discontinued, they are not preferred references and I have therefore made limited use of them. Recommended general literature on salamanders is listed in a separate chapter. Our knowledge of salamanders is increasing rapidly; the present synthesis is intended to be comprehensive up to the end of 2013 and descriptions of new species have been incorporated until 1 December 2013.

Personal

I wish to end this preface on a personal note. My fascination for newts and salamanders dates back to the early 1960s, when I first caught Smooth Newts in ditches, put them in an aquarium and marveled at the lively courtship display of the beautiful, high-crested males. In a way, after half a century, I am still doing this kind of thing. In the 1970s and 1980s it was the ethological work of Timothy R. Halliday on the

12

Salamanders of the Old World | Preface

Smooth Newt and that of Stevan J. Arnold and Paul A. Verrell on other newt species that stimulated me to study the courtship behaviour of salamanders and newts further. Observing and photographing these animals, studying their behaviour patterns, and sharing my interest with like-minded friends has been immensely gratifying. I have learned much about salamanders from herpetologists, students of animal behaviour, and hobbyists, who study these animals in the field or breed them in terrariums in their homes. I hope this book will be a source of inspiration for them and for a new generation of naturalists, much as Robert Thorn’s book of 1969 was for me in the past.

Max Sparreboom Amsterdam, December 2013

Acknowledgements I am indebted to a great many friends and colleagues, who have supported my work on the on-line catalogue, and subsequently the present book, over the past seven years. Their contributions have consisted of making critical comments on draft species entries. Many others have kindly allowed me to use their photos, or helped me to track photos; assisted me in setting up and improving the database; sent and translated literature; made range maps; accompanied me in the field to salamander habitats; offered hospitality, typing and help in organising my material; and done editorial work or provided so many other kinds of support. I gratefully acknowledge their help, which was always unconditional. I list them in alphabetical order. Ahmadzadeh, Faraham; Aljancic, Gregor; Arntzen, Pim (J.W.); Bachhausen, Paul; Bakkers, Mark; Beukema, Wouter; Bogaerts, Sergé; Brakels, Peter; Chan, Bosco (KFBG); Chang, Yu-Hao; Chang, Yuan-Hsian; Che, Jing; Cogalniceanu, Dan; Deban, Stephen; Espallargas, Gustavo; Fei, Liang; Fleck, Jürgen; Fu, Jinzhong; Garcia, Gerardo; Garner, Trenton; Gilbert, Maarten; Gilissen, Tom; Goverse, Edo; Griffiths, Richard; Gu, Xiaoming; Hasumi, Masato; Herder, Jelger; Herrmann, Hans-Joachim; Hou, Mian; Jamin, Arnaud; Janssen, Henry; Jiang, Ke; Johnson, Tim; Kano, Yuichi; Kim, Jong-Bum; Krips, Gerrit; Kühnel, KlausDetlef; Kuwabara, Kazushi; Lau, Michael (KFBG); Leo, Frank; Leung Sze Lun, Alan; Li, Jiatang; Li, Pipeng; Liu, Liuchang; Lou, Xin-quan; Lue, Kuang Yang; Maillet, François; Matsui, Masafumi; Messenger, Kevin; Miller, Jessica; Molenkamp, Ans; Mozaffari, Omid; Nerz, Joachim; Nguyen, Thien Tao; Nishikawa, Kanto; Nöllert, Andreas; Okada, Sumio; Ota, Hidetoshi; Papenfuss, Theodore; Park, Daesik; Pasmans, Frank; Paysant, Franck; Poyarkov, Nick; Pieterse, Sander; Pomchote, Porrawee; Ra, NamYong; Raffaëlli, Jean; Sakuma, Satoshi; Schneider, Willi and Christoph; Schöttler, Thomas; Sejkora, Radek; Sos, Tibor; Stuart, Bryan; Taguchi, Yuki; Teunis, Bas; Thiesmeier, Burkhard; Thorn, Robert; Tochimoto, T.; Trapp, Benny; Voort, Jan van der; Wallays, Henk; Wan, Jay; Wang, Qijun; Wen, Christen; Wielstra, Ben; Wit, Tonny de; Woeltjes, Tonnie; Wu, Yunke; Xie, Feng; Yang, In Shuen; Yang, Weizhao; Ye, Changyuan; Yoshikawa, Natsuhiko; You, Chung Wei; Yuan, Zhiyong; Zeng, Xiao-mao; Zhang, Ming-Wang; Zhang, Xu; Zhao, Haitao; Zhao, Hui; Zhou, Jian-Jun.

Finally, I wish to single out a number of people who have been particularly important for me during the making of this book. In the first place, Pim (J.W.) Arntzen. As researcher at the Department of Terrestrial Zoology – Reptiles and Amphibians, at the Naturalis Biodiversity Center in Leiden, he has facilitated my work on the website catalogue and the book, and has been a great support with advice and critical comments. I owe many thanks to my fellow travelers Sergé Bogaerts, Frank Pasmans and Tonnie Woeltjes, with whom I made trips to Morocco, Vietnam and Turkey, and who allowed me to use their photos, provided literature and critically reviewed several chapters. I wish to thank Xie Feng, Fei Liang and Ye Changyuan (Chengdu) with whom I worked for two seasons on a very rare Chinese salamander, Echinotriton chinhaiensis, and who traveled with me through China to monitor amphibian populations. I wish to thank Hidetoshi Ota for working with me on Cynops ensicauda and for introducing me to the herpetofauna of the Ryukyu islands. I also want to thank Tim Johnson (Tokyo), with whom I saw so many salamanders in Japan during our herping trips. I am much indebted to Wouter Beukema, who has made updated range maps of all the species treated in this book, and who has critically followed my writing of the species chapters. The artwork in this book was made by Bas Teunis. Our collaboration dates back to the 1980s, when he made meticulous pen drawings illustrating my articles on newt courtship behaviour patterns. He kindly agreed to let me use some of his earlier work again and made a number of important new figures for this book. Besides this, he has been an invaluable support by helping me edit the photos. It is my pleasure to acknowledge the editorial assistance of Gerrit Krips, who spent much of his time helping me to get the book manuscript ready. Finally, I should like to express my thanks to Jan Krikken (Naturalis), who agreed that Naturalis should embark on a project such as the website Salamanders of the Old World. I thank KNNV publishers – Paul Kemmeren and Jack Folkers – for their brave decision to start a book project such as this, to Andrew Richford for editing and improving the English text, to Niko Korenhof for making the layout and Jan van Tol, head of the Department of Terrestrial Zoology at Naturalis Biodiversity Center, for facilitating the making of the book. I thank them for their support and co-operation.

13

Introduction Biology of salamanders

Amphibians are a class of ‘coldblooded’ vertebrate animals that have a naked, glandular skin, which is lacking any epidermal covering such as fur, scales or feathers. Salamanders are tailed amphibians with an elongated body, prominent tail, and typically two pairs of limbs that are similar in size. The front legs have four fingers and the hind legs have five or four. Salamanders belong to the order Caudata (‘caudate’ meaning ‘tailed’), which is one of the three orders comprising the class Amphibia. The other amphibian orders are the Anura (frogs and toads which lack tails and have bodies and limbs that are modified for jumping) and the Gymnophiona (caecilians, a group of legless, worm-like animals found in the tropics). Because of their long bodies and tails, salamanders superficially resemble lizards, which are reptiles. But unlike lizards, salamanders do not have scales or claws and have aquatic larvae. Salamanders and lizards are very different animals with different life histories and live in different habitats. Strictly speaking, all tailed amphibians are ‘salamanders’, and ‘newts’ are just a subset of the group. Hence, newts are salamanders, but not every salamander is a newt. ‘Newt’ is the common term generally used for those salamander species in the family Salamandridae that spend at least part of their

A

Caudata

Cryptobranchidae Hynobiidae Sirenidae Salamandridae Ambystomatidae Dicamptodontidae Proteidae Rhyacotritonidae Amphiumidae Plethodontidae

Phylogenetic relationships of extant salamanders based on molecular data. The branches of the tree represent lines of descent of salamander families of the world (A) and of genera in the families Cryptobranchidae, Hynobiidae and Salamandridae (B). Tree topology follows Pyron & Wiens (2011). 14

Salamanders of the Old World | Introduction

adult life in water (e.g. the genera Cynops, Euproctus, Lissotriton, Neurergus, Triturus, and the American Taricha and Notophthalmus). There is however no definitive division between species called either newts or salamanders and the literature is not consistent in its usage of the terms, in particular with regard to the Asian species. In other European languages the situation is similar. Throughout this book the term ‘salamander’ will be used to refer to all species in the family Salamandridae, except for those that have a partly aquatic lifestyle and which are commonly called ‘newt’ in English, ‘Molch’ in German or ‘triton’ in French, which I will refer to as ‘newts’. Currently 652 salamander species are recognised according to Amphibian Species of the World (http://research.amnh.org/vz/ herpetology/amphibia/ accessed on 15 May 2013). They occur in Europe, in North, Central and South America, in Northern Africa, and in Asia. Salamanders vary in length between 3 cm and 150 cm. By far the majority of species (433) belong to the family of lungless salamanders (Plethodontidae). These are found mainly in North, Central and South America, but eight species occur in Europe: the European cave salamanders of the genera Speleomantes and Atylodes. Much to the surprise of the scientific world, a new plethodontid salamander was discovered in South Korea in 2005 and named Karsenia koreana.

B

Andrias Cryptobranchus Onychodactylus Pachyhynobius Salamandrella Hynobius Paradactylodon Ranodon Batrachuperus Liua Pseudohynobius Salamandrina Chioglossa Mertensiella Lyciasalamandra Salamandra Pleurodeles Echinotriton Tylototriton Notophthalmus Taricha Lissotriton Calotriton Triturus Neurergus Ommatotriton Euproctus Ichthyosaura Laotriton Pachytriton Cynops Paramesotriton

Cryptobranchidae

Hynobiidae

Salamandridae

The family Salamandridae is a group of salamanders that occurs mainly in Europe and Asia comprising just over 100 species, as well as two American newt genera, Taricha and Notophthalmus. The typical European and Asian newts (Lissotriton and Cynops) and the Fire Salamander (Salamandra salamandra) belong to this family. Two other salamander families, the mole salamanders, Ambystomatidae (37 species of which the Axolotl, Ambystoma mexicanum, is the best known representative) and the small family Rhyacotritonidae only

‘Salamandra maxima’, the Japanese Giant Salamander © Naturalis Biodiversity Center. Photo: Max Sparreboom.

The most famous illustration of the Japanese Giant Salamander (now called Andrias japonicus) is the lithograph published as plate VII of the Amphibians and Reptiles volume of the Fauna Japonica. The original is a coloured drawing made by Dr S. Mulder from a living specimen and is kept in the library of the Naturalis Biodiversity Center in Leiden. The plate was in a poor state of preservation and was restored in 2004. This photo was made after the restoration. On the original drawing, the salamander is depicted life-size. By positioning the salamander with head and tail bent in an s-shape, the artist could fit it onto a single page, while maintaining enough detail of the skin structure. The illustration is used in many later works on the Giant Salamander and even in logos of Giant Salamander research and education institutions in Japan. This drawing depicts the first living Giant Salamander ever seen outside Japan. The animal was shipped from Nagasaki to Amsterdam in 1830 along with other animals, plants and Japanese utensils. It was collected by Philipp Franz von Siebold (1796-1866),

occur in America and are not part of the Old World salamander fauna. The family of hynobiid salamanders (Hynobiidae) contains 59 species and only occurs in Asia, with the exception of the Siberian Salamander (Salamandrella keyserlingii) which just reaches into Europe. In contrast to the other families, fertilisation in the Hynobiidae and Cryptobranchidae is external, outside the body of the female. In hynobiids the eggs are

the only westerner who was allowed by the Japanese government to collect cultural and biological objects in Japan at that time. Von Siebold was employed as a medical doctor at the VOC (United East-Indian Company) trading post Deshima. In the early 19th century the activities of Von Siebold and his assistant Heinrich Bürger provided the only reliable source of knowledge about Japanese nature and culture. Von Siebold’s notes, the living specimen and a skeleton were used by biologist Coenraad Jacob Temminck to describe the Giant Salamander as a new species. Von Siebold’s notes and collection were the basis of two comprehensive publications about the natural history of Japan. Researchers of the State Museum of Natural History in Leiden published the book series Fauna Japonica, while researchers at the State Herbarium in Leiden wrote the Flora Japonica. Fauna Japonica was published in six volumes between 1833 and 1850 and was produced by C. J. Temminck (1778-1858), Hermann Schlegel (1804-1884) and Willem de Haan (1801-1855). The Japanese Giant Salamander was described in Volume 3 and depicted with the beautiful lithograph shown here. The salamander shown in the picture was actually one of two specimens shipped by Von Siebold. The other ended up in the stomach of the first during the long sea voyage! Upon its arrival in Amsterdam, the salamander was first taken to the State Museum of Natural History in Leiden, where it was kept alive for 10 years. In 1840 it was given to the Amsterdam Zoo, Artis, where it eventually died in 1881. The dead animal was preserved in alcohol in a bottle, but the bottle appears to be lost. Fortunately Von Siebold sent other specimens to the Netherlands. These have been registered as paralectotypes in the scientific collections of the Naturalis Biodiversity Center in Leiden and the zoological museums in Berlin and Paris. References Gassó Miracle et al. (2007); Hoogmoed (1978); Holthuis & Sakai (1970); Schlegel (1842); Temminck (1836); Temminck & Schlegel (1838).

15

The Olm (Proteus anguinus) is an aquatic salamander living in Karstic caves. Planinska jama, Slovenia. Photo: Gregor Aljancic.

deposited in egg sacs, which are clasped and fertilised by the male; in cryptobranchids the eggs are laid in long strings in underwater cavities, where they are fertilised and guarded by the male. The giant salamander family (Cryptobranchidae) consists of only three species, one in North America (the Hellbender, Cryptobranchus alleganiensis) and two in Asia (the Japanese Giant Salamander, Andrias japonicus, and the Chinese Giant Salamander, Andrias davidianus). These are the largest extant salamanders (up to 150 cm in Andrias); they live permanently in water.

branes allow gases and water to pass freely through the egg and also protect it against damage, desiccation, infection and predation. Eggs are most often laid in water bodies or in damp places, where desiccation is unlikely to prevent successful development. After completing the larval stage the juveniles change into miniature versions of the adult form.

Metamorphosis

The process of transformation from the larval to the adult form is called metamorphosis and involves a number of major anatomical and physiological changes.

Three small families, Amphiumidae, Sirenidae and Proteidae, consist of exclusively aquatic salamanders, mostly very long eel-like animals with short legs or front legs only, which retain larval characteristics such as gills. The first two families only occur in America. The Proteidae contains the mudpuppies (Necturus) which occur in America, and the Olm (Proteus anguinus), a species found only in Karstic caves around the Adriatic Sea in Europe.

Development

One of the principal characteristics of amphibians is their biphasic life cycle. The word ‘amphibian’ is derived from the Greek and means ‘both lives’, referring to the free living, aquatic larval stage that most amphibians exhibit before transformation to a form suitable for life on land. The eggs of salamanders, frogs and toads do not have a hard shell but are commonly formed of one or several semi-permeable, gelatinous membranes surrounding the ovum. These mem-

16

Salamanders of the Old World | Introduction

Life cycle of the Alpine Newt (Ichthyosaura alpestris). Top to bottom, left to right: egg, male, female, larva and juvenile. Art: Bas Teunis. From: Griffiths, 1996.

In contrast with frogs and toads, in salamanders the front legs develop first, followed by the hind legs. During metamorphosis the tail-fin is reduced, the external gills are reabsorbed, the glandular adult skin forms and a tongue develops. Juvenile salamanders shift from gill to lung powered respiration. Metamorphosis is mediated by hormones, especially thyroxine which is produced in the thyroid gland located near the throat. Salamander larvae whose thyroids have been surgically removed will not metamorphose unless they are given thyroxine. Iodine is a vital ingredient in thyroxine. If absolutely no iodine is present in the water, the larva will be unable to make any thyroxine and so will be unable to metamorphose. Not all salamanders undergo a metamorphosis. Some species remain in an essentially permanent larval state and never transform. This phenomenon is called neoteny and the metamorphosis is ‘incomplete’. Individuals reach sexual maturity and reproduce while retaining larval characteristics, a phenomenon known as paedomorphosis. A typical example is the Mexican Axolotl (Ambystoma mexicanum) and in this species metamorphosis can be artificially induced by injection of thyroid extract. This phenomenon is called partial neoteny. Species which achieve sexual maturity and breed in the larval stage, and in which metamorphosis cannot be induced artificially, are described as exhibiting total or obligatory neoteny. An example is the Olm (Proteus anguinus). Some other salamander species bypass the free-living larval stage and develop directly to the adult form within the egg. The young hatch, or are born, as tiny replicas of their parents. This is the case in most plethodontid salamanders, including the southern European species of Speleomantes and Atylodes. In other terrestrial salamander genera, partial or entire development takes place inside the female’s body and the young are released as advanced larvae (as in most forms of Salamandra salamandra) or as fullydeveloped small salamanders (as in Salamandra atra, S. lanzai and all Lyciasalamandra species).

European cave salamanders (shown here a female of Speleomantes strinatii, Busalla, Liguria) lay eggs on land and guard them. The young hatch as tiny replicas of the parents. Photo: Frank Pasmans.

serves to force air in and out of the lungs since they do not have an internal diaphragm for this purpose. Fishes use gills to breathe but amphibians can respire using their skin and the lining of the mouth, which enables some species to hibernate under water in winter. They can take in enough oxygen through their skin for respiration in the cold water without having to surface for air. Lungless salamanders, such as the plethodontid salamanders of the genus Speleomantes, Atylodes and Karsenia, the

Skin

Without an external covering of scales, feather or hair, the skin of a salamander is exposed directly to the environment. Possibly because of this, the skin is developed into a complex, highly vascularised, living structure. With its thin skin that is permeable to water, an amphibian’s ability to invade dry environments is restricted. Accordingly, a fair amount of moisture and high air humidity is required for amphibians to be active without risking desiccation. But a thin skin also has advantages: amphibians do not drink through their mouths but can absorb water and also breathe through their skin. Gas exchange in breathing – the uptake of oxygen and the release of carbon dioxide – requires a moist, vascular membrane for the gases to diffuse across. In most land-dwelling vertebrates this occurs in the lungs. The pumping throat of a salamander

Salamander larvae breath through external gills. Here a captive bred larva of Paramesotriton guangxiensis from Shiwan Dashan, Guangxi, China. Photo: Henry Janssen. 17

hynobiid long-tailed salamanders of the genus Onychodactylus, and the salamandrid Corsican Newt (Euproctus montanus) have dispensed with lungs altogether and rely entirely on cutaneous respiration through the skin and buccal respiration through the lining of the mouth. But skin respiration is important in all species, including those with lungs. Salamander larvae and neotenic salamanders breathe through external gills and the skin. Salamanders have a variety of skin glands that help keep the skin moist or help to protect them from enemies. There are two major types of skin glands: mucous and granular, or poison glands. Mucous glands are small and distributed all over the body, and open onto the skin surface through microscopic pores. They secrete fluid mucus that helps lubricate the skin and keep it from drying.

Defence mechanisms

A host of animals – birds, snakes, fish and rats – prey on salamanders. In response, salamanders have developed a variety of ways to avoid being eaten. Most commonly, both aquatic and terrestrial salamanders simply flee but the large salamanders such as giant salamanders (Andrias) can bite hard. Small salamanders, such as some European cave salamanders (Speleomantes), can bite too, but this is effective only against small predators. Many species that live under logs and rocks freeze in place when uncovered, taking advantage of a visual predators tendency to respond to moving prey items; they tend to overlook a camouflaged, motionless salamander.

Small salamanders and newts also defend themselves by being distasteful or toxic and may secrete a powerful toxin from glands in their skin. In many species these poison glands are clustered in certain places on the body, for instance behind the eyes (paratoids), or on the dorsal parts of the body and tail. Skin poisons are only released when the animal is in extreme stress and their main purpose is to render the salamander distasteful and so deter predators. Some species can even actively squirt their poison, such as the Fire Salamander (Salamandra salamandra). Many species, especially those with bright warning colours on some parts of their body and tail, may take up a defensive posture when threatened, displaying the orange or red underside of the body, tail or feet. No amphibian has a poisonous bite or can inflict a poisonous wound. Some species such as the European Cave Salamander (Speleomantes imperialis) can emit a strong smell. Some salamander species escape predation by waving their tail to distract the predator’s attention to that part of the body. A well-known example is the Iberian Golden-striped Salamander (Chioglossa lusitanica). Once a predator grabs its tail, the salamander can ‘autotomise’ or shed it, and the predator is left holding a wriggling tail while the rest of the salamander escapes. A new tail will grow to replace the one lost. A bizarre defence mechanism is shown by the ribbed newts, members of the Mediterranean genus Pleurodeles, and the East-Asian crocodile newts of the genus Echinotriton. When attacked or manipulated roughly, sharp spines on top of the ribs pierce the salamander’s skin and make it an unattractive, painful meal for a predator.

Temperature and activity

Echinotriton chinhaiensis in a defensive posture. Photo: Max Sparreboom. 18

Salamanders of the Old World | Introduction

Amphibians are commonly known as ‘cold-blooded’ animals. This term is a misnomer as the difference between a ‘cold-blooded’ and a ‘warm-blooded’ animal is not simply the temperature of their blood. The important point is whether the body temperature remains constant or varies with ambient temperature, and whether heat to warm the animal is generated metabolically inside its body or must be absorbed from the environment. An amphibian does not produce enough metabolic heat to warm its own body, as birds and mammals do, and body temperature depends upon the temperature of its surroundings. An amphibian can regulate its temperature to a certain extent by actively seeking out spots that have the optimal temperature for a certain activity pattern – feeding, mating or resting motionless avoiding extreme heat or cold in the process. Generally, salamanders prefer relatively low temperatures, usually between 10 and 20°C but can sometimes be active at very low temperatures. A number of Hynobius species start to reproduce in winter at temperatures of 0°C. When temperatures rise and air humidity decreases, such as during Mediterranean summers, most salamanders go underground and aestivate. They remain inactive in cool, humid spots until lower temperatures and

autumn rains bring them to the surface again where they can feed or mate. In northern regions, or at high elevations with long winters, salamanders survive cold winter temperatures by seeking out refugia in forest soils or crevices below the frost line. They remain inactive for months until spring when temperature and humidity start to rise, snow is melting and conditions are favourable for reproductive activity.

Feeding

All larval and adult salamanders are carnivores, their food consisting mainly of living animals. Most salamanders eat a variety of invertebrates such as insects and their larvae, worms, millipedes, centipedes and snails. The larvae eat zooplankton, mosquito larvae and other invertebrates. Some salamanders also eat amphibian eggs and larvae, even of their own kind. Salamanders capture prey in several different ways. They detect potential prey by sight or by smell. The size of the prey they can swallow is in part determined by how wide they can open their mouth (gape). In terrestrial environments salamanders capture their prey by lunging a short distance with the mouth open and on contact quickly extend the tongue forward and downward. The back of the tongue contacts the prey and simultaneously releases a sticky secretion that adheres to it. The tongue – and the insect or worm stuck to it – is quickly withdrawn into the mouth, which closes over it. Plethodontid salamanders can protrude the tongue a short distance. Some species, such as the European cave salamanders of the genus Speleomantes can propel their tongue over a body length distance to catch prey. Feeding in water requires a different method. Salamander larvae and aquatic adult animals vacuum prey into their mouth. As the animal makes a brief lunge at the prey, the floor of the mouth drops and the nostrils close, creating a vacuum that literally sucks the prey into the mouth. Labial folds that develop especially during the aquatic stage enhance the suction effect.

Reproduction and courtship behaviour

Salamanders communicate in a variety of ways. Unlike frogs, which vocalise to attract mates and defend territories, most salamanders lack the ability to make sounds. With a few exceptions (Lyciasalamandra luschani) salamanders are voiceless and when attacked or manipulated roughly, may produce a squeaking sound. Little is known about these sounds, but they may be associated with defence.

Salamanders communicate through chemical, tactile and visual signals. All species produce pheromones – small-molecule, chemical messengers designed to evoke a specific response. For example, the American plethodontid salamanders mark the boundaries of small territories with pheromones produced by glands located posterior to the cloaca. Intruders know from the smell of the pheromone that a certain spot belongs to

Nasolabial grooves on the snout of Speleomantes strinatii (specimen from Genua). Photo: Joachim Nerz.

another salamander. The nasolabial groove on the front of the snout picks up the pheromone informing the salamander that he is on another salamander’s terrain. He will either avoid the territorial male or engage in a fight. Research on American plethodontid species has revealed that the salamanders’ chemical communication system is so sensitive that individuals can recognise other individuals, including their own brothers and sisters. Chemical communication is now also the subject of study in European newts and salamanders. Salamanders reproduce using an amazing variety of behaviour patterns. These range from external fertilisation of the eggs to elaborate courtship rituals in which the male embraces the female or performs a display to persuade her to pick up a packet of his sperm with her cloaca.

Cryptobranchids Although external fertilisation is the usual mode of reproduction among frogs, it is unusual among most salamanders (although it is the rule for the giant salamanders of the Cryptobranchidae family and in the Asian family Hynobiidae).

European cave salamanders (Speleomantes and Atylodes) can shoot out their tongue to catch a distant prey. Art: Bas Teunis. 19

Japanese Giant Salamander (Andrias japonicus) male guarding a clutch of eggs recently laid in his den. Males occupy a breeding site, usually a secluded spot on the bottom, or in the embankment, of a river. Females ready to spawn enter the den to lay eggs and leave the site immediately afterwards. The male subsequently fertilises the eggs and guards them throughout hatching. Art: Bas Teunis from photos of the Andrias breeding programme of Hiroshima City Asa Zoological Park (courtesy Kazushi Kuwabara).

In giant salamanders the male occupies a chamber under a rock in a stream or stream embankment and a female enters it when she is ready to spawn and lays long strands of eggs. The male moves over them and extrudes masses of sperm that fertilise the eggs. The female leaves the nesting den and the male remains with the eggs to protect them from potential predators.

Hynobiids

Oita Salamander (Hynobius dunni). A breeding assemblage of males in captivity. Photo: Henk Wallays. 20

Salamanders of the Old World | Introduction

In the family Hynobiidae the males take up position on a selected egg laying site, such as a twig or rock, and await the arrival of females ready to lay eggs. Strictly speaking, the male does not court the female but focusses his attention primarily on the recently laid eggs. The eggs are housed in two egg sacs, joined together at their bases. The female attaches this common basal portion to a branch or stone. Once this base is secured, the female moves away slowly and the egg sacs are drawn out of each oviduct. Sometimes she is shoved away by the male in his eagerness to fertilise the eggs. He grasps the emerging egg sacs with his fore- and hindlimbs and then releases sperm while arching his body around the egg sac. If rival males come near, the male attempts to monopolise the eggs and their fertilisation

Crested Newt (Triturus cristatus) courtship display. The male shows off his dorsal crest. Art: Bas Teunis.

by maintaining his grasping position. Despite such attempts to keep his paternal monopoly, several males may compete at the same time and actually succeed in fertilising all or some of the eggs. Males may also guard the egg sacs for some time after fertilisation to prevent this from happening.

Plethodontids Courtship in the lungless salamander group, the Plethodontidae, is remarkably uniform among species. The male approaches the female and makes head contact with her. Many plethodontid salamanders have a special gland under the chin (the mental gland) which produces pheromones and is rubbed against the female during courtship. Subsequently, the pair engages in a ‘tail-straddling walk’ in which the female places her chin on the base of the male’s tail while she straddles his tail. The male deposits a spermatophore in front of her snout. The pair moves forward and the female lowers her cloaca over the spermatophore and picks up the sperm packet with her cloacal lips. Subsequent fertilisation is internal. Courtship has rarely been observed in European plethodontids (Speleomantes). They lay their eggs as clutches in damp, cool, hidden places on land, such as in caves, and guard them from predators until they hatch.

special glands in the male cloaca, which influence and stimulate the female. Newts in the genera Triturus and Ommatotriton employ conspicuous visual ornaments, such as dorsal crests. They display in front of the female using both visual and chemical stimuli, with the release of pheromones as the major chemical stimulus. After this display, the male engages the female in a tail-nudging walk (‘creep’) before depositing the spermatophore in front of her snout. The female picks up the sperm cap with her cloaca and insemination occurs. Salamandrids show several types of amplexus as well as courtship without physical contact. In ventral clasping, the male holds the female on his back by hooking both of his fore legs around her fore legs (Tylototriton, Pleurodeles, Salamandra, Lyciasalamandra,

Salamandrids The large family of Salamandridae is characterised by a remarkable diversity among genera in their forms of courtship, amplexus and modes of sperm transfer. In newt species (such as Lissotriton, Triturus, Cynops, Paramesotriton, Neurergus, Pachytriton and some species of Tylototriton) courtship involves an elaborate male display without much physical contact, including various tail-fanning movements in which the male wafts a stream of water containing specific pheromones towards the female’s snout. Courtship pheromones are excreted by

In Lycian salamanders the male carries the female on his back, holding her in an amplexus with his forelegs hooked around hers. Lyciasalamandra fazilae from Dalian-Iztuzu, Turkey. Photo: Frank Pasmans. 21

(Speleomantes). The female curls up, wrapping herself around the small clutch of eggs and defends them against intruders. Other forms of parental care have been observed in some species of Salamandridae (paddle-tailed newts of the genus Pachytriton), in the Corsican Newt (Euproctus montanus), in the giant salamanders of the family Cryptobranchidae, and some species of Hynobiidae (Pachyhynobius).

Eggs, larvae and live-bearing

Direct insemination by the Pyrenean Newt, Calotriton asper. The male lacks an elaborate courtship display and captures the female with his tail when she is close by. In a rapid movement, he raises his tail and coils it up around her body, usually around the pelvic region, thus immobilising her hind legs. Art: Bas Teunis. From: Griffiths, 1996.

Chioglossa, Mertensiella). Dorsal amplexus is also employed, in which the male straddles the female’s back while his forelimbs grasp the female’s pectoral region (Salamandra and the American genus Taricha). In yet other species the male restrains the female in special forms of amplexus, using his tail, hindlimbs and jaws (in mountain stream species of Calotriton and Euproctus) and the sperm is transferred through direct contact between the male and female cloacas.

Generally, free swimming, aquatic larvae emerge from the eggs, which eventually undergo metamorphosis to take on the adult form. Larvae can be divided into two main groups – pond-dwellers (or lentic species) and stream-dwellers (or lotic species). Pond-dwelling larvae, such as those of most newts, hatch at a relatively early stage of development. The front leg buds are still small, the mouth is not yet fully functional, and the larvae remain attached to the egg capsule or adjacent vegetation by two prong-like adhesive organs attached to the head, called balancers. For a few days the larvae are largely immobile and feed on the remaining yolk supply. By the time this is used up the mouth is functional and the balancers have been resorbed, so that the larvae are ready to assume a free-swimming, predatory way of life. Ponds are often stagnant and low in oxygen, and their large, frilly gills provide a large surface area over which oxygen can be absorbed. A deep fin runs along the back and tail which also provides a large surface area for respiration. Stream-dwellers,

When a female has picked up the sperm cap from the spermatophore (a small structure consisting of a gelatinous base that tapers to the top and supports an apical sperm mass) the sperm is stored in a special chamber in the female cloaca (spermatheca). Subsequently – after a few hours, or in some species, anything from a couple of months to over a year after insemination – the eggs are fertilised internally, shortly before they are laid. Eggs are deposited in water or in humid places on land, hidden under rotten foliage. Eggs may be laid either singly (such as in Lissotriton and Pleurodeles) or in clutches on land (such as in terrestrial species like Echinotriton).

Parental care

After laying their eggs, the females usually abandon them and leave the site. Parental care does, however, occur frequently in terrestrial breeders in the family Plethodontidae, and is best known in American species. The eggs are exceptionally large relative to the female body size, and the female ‘broods’ her eggs until they hatch. This behaviour has also been reported for European plethodontids

22

Salamanders of the Old World | Introduction

A young larva of the Palmate Newt (Lissotriton helveticus) with balancers. Photo: Leo Fokus-Natur, courtesy Andreas Nöllert.

such as Euproctus and Neurergus, must be able to cope with flowing water after hatching and so hatch at a more advanced stage of development with functional mouthparts and wellgrown front and hind legs. Life in cool, well-oxygenated, flowing water means that the gills and tail-fin need not be so well-developed as in pond-dwelling species. The body is generally more streamlined with a muscular tail to provide more powerful locomotion in a current of water. The same difference between pond- and stream-dwelling larvae is seen in hynobiids. In most plethodontid salamander species, including the European Speleomantes species, the embryos pass through a gilled stage within the egg capsule and loose their gills just before hatching. They hatch from the eggs as fully developed young salamanders (direct development), but actual observations of hatching in the wild are rare. In a small number of completely terrestrial salamandrid species, fully developed larvae (ovoviviparous as in Salamandra salamandra) or fully metamorphosed juveniles are born (viviparous as in Salamandra atra, S. lanzai and Lyciasalamandra species).

Threats and conservation

Amphibian populations are declining in many parts of the world. There are fewer reports of declines in salamanders than in frogs, but this may reflect the fact that frogs are more widespread and generally better studied. Salamander populations appear to suffer from the same threats as frog populations. They are vulnerable to environmental

change than others. For example, European Smooth Newts (Lissotriton vulgaris) can colonise different breeding waters, and even utilise artificial water bodies such as garden ponds. But many others are highly specialised in their ecological requirements and will decline or disappear when their habitats are disturbed. The main threat to salamander populations is the loss of habitat through human activities. Urban development, agricultural improvement, pond drainage, water abstraction from streams, alterations to stream and river banks, deforestation, dam and road building, the creation of tourist facilities in ecologically sensitive areas, and water pollution – all lead to degradation or destruction of salamander habitats. Habitat destruction leads to smaller areas becoming available for the animals, and worse, to populations becoming fragmented and isolated from each other. When animals cannot migrate and colonise new habitats declines and extinctions can result from local disasters, inbreeding or other unpredictable factors. Global warming and climate change are also expected to have dramatic impacts on the distribution and survival of amphibian species. Salamanders generally cannot survive proximity to predatory fish. When predatory fish are introduced into ponds, lakes or streams, salamander eggs and larvae will quickly become fish food. Over-harvesting of animals for the international pet trade or for use in traditional medicine may pose a serious threat to salamander species with a limited distribution. Although the collecting of many salamander species is illegal in many countries, such as Tylototriton in China, legal control and enforcement is often insufficient to prevent great numbers of protected salamander species from being sold in local markets and the international pet trade.

Amphibians frequently fall victim to road traffic. A sign warning not to crush Fire Salamanders crossing the road in Los Alcornocales, Spain. Photo: Max Sparreboom.

changes that affect their skin and, like frogs, they are affected by changes in both their terrestrial and aquatic habitats. In multispecies amphibian assemblages, salamanders usually decline before frogs and toads and are less successful in dispersing to new habitats. Some species are more adaptable to environmental

Worldwide, especially in mountainous areas, amphibian populations are threatened by a chytrid fungus, Batrachochytrium dendrobatidis. The lethal skin disease caused by this fungus is called chytridiomycosis and is associated with the global decline and extinction of many, mainly anuran, species and poses a real threat to biodiversity. In salamanders, the disease is probably involved in the steep population declines observed in plethodontid salamanders in Central America. The effect of exposure of a salamander to B. dendrobatidis varies, depending on fungal, host and environmental factors. The amphibian host may become resistant to the fungal colonisation leading to the development of healthy and persistent carriers of the fungus or it may develop lethal chytridiomycosis and die as a result. While B. dendrobatidis may well pose a serious threat, its effect on urodelan biodiversity is currently far from clear. 23

In order to assign priorities for conservation action, amphibians have been classified according to their vulnerability in the Red List of the International Union for the Conservation of Nature (IUCN), using the following categories. Extinct: Species for which extensive surveys show there is no reasonable doubt that the last individual has died. Extinct in the Wild: Species that survive only in cultivation, in captivity or as a naturalised population (or populations) well outside the past range. Critically Endangered: Species that are facing an extremely high risk of extinction in the wild. Endangered: Species that are facing a very high risk of extinction in the wild. Vulnerable: Species that are facing a high risk of extinction in the wild. Near Threatened: Species that do not qualify as Critically Endangered, Endangered or Vulnerable now, but are close to qualifying for, or are likely to qualify for, a threatened category in the near future. Least Concern: Species that do not qualify as Critically Endangered, Endangered, Vulnerable or Near Threatened. Widespread and abundant species are included in

Chinese Giant Salamanders (Andrias davidianus) are kept and raised in commercial farms on a large scale. This specimen was 120 cm long and weighed over 40 pounds. Photo: Wang Qijun.

this last category. The criteria are based on observed population reduction, geographic range, population size and quantitative analysis. According to information from 2008, 5% of the Old World salamander species fall in the Critically Endangered category, 14% in the Endangered category and 15% in the Vulnerable category. Nine per cent are considered to be rapidly declining and one species is apparently extinct (Cynops wolterstorffi). Conservation measures can be effective only if the ecological requirements of a species are known. For species to be preserved effectively, all of their habitats have to be protected, both their 24

Salamanders of the Old World | Introduction

aquatic and terrestrial habitats in the case of salamanders. The size of an area to be set aside for a salamander population and what features it should include varies between species. At the least, the area should be large enough for a population to sustain itself within its limits and must be large enough to buffer the natural fluctuations in population size which seem to be a feature of many salamander populations. Breeding amphibians in captivity in order to restock wild populations that have declined to near extinction is occasionally proposed as an ultimate conservation measure. For salamanders, there is no published record of successful interventions of this sort. The Chinese Giant Salamander (Andrias davidianus) is bred in captivity in commercial, state-sponsored farms, but it is impossible to tell whether such farming has led to any scientifically controlled release of captive-bred Giant Salamanders into their natural habitats. No Old World salamander species are included on the list of critically endangered species for which captive breeding is considered an immediately necessary ex-situ conservation action. Because the trade in wild animals and plants crosses the borders between countries, international cooperation is required to regulate and safeguard certain species from over-exploitation. CITES (the Convention on International Trade in Endangered Species of Wild Fauna and Flora) was conceived in the spirit of such cooperation. CITES is an international agreement between governments which aims to ensure that international trade in wild animals and plants, and their products, does not threaten their survival. Today, it accords varying degrees of protection to more than 30,000 species, grouped in Appendices according to how threatened they are by international trade. Presently (2013) CITES offers protection to three Old World salamander species, listed in Appendix 1: the Chinese Giant Salamander (Andrias davidianus), the Japanese Giant Salamander (Andrias japonicus) and the Zagros Mountain Newt (Neurergus kaiseri). Besides international agreements, there is local and national legislation to control the collecting and trading of amphibians, but the main problem is effective implementation of the protection measures and enforcement. Another problem is that once exported from a country where a species is protected, an animal can be imported and kept legally in another country where it is not. This is the case in Europe, for instance, where species of Neurergus from Turkey and Tylototriton from Thailand and China can be legally imported and kept in captivity. The Bern Convention on the Conservation of European Wildlife and Natural Habitats is a binding international legal instrument in the field of nature conservation. Its main aims are to conserve wild flora and fauna and their natural habitats.

Four appendices list particular species for protection. The convention makes recommendations for national conservation action plans, such as for Crested Newts (Triturus cristatus species group) in 2006. The Habitats Directive (more formally known as Council Directive 92/43/EEC on the Conservation of natural habitats and of wild fauna and flora) is a European Union directive adopted in 1992 as a response to the Bern Convention. It aims to protect some 220 habitats and approximately 1,000 species listed in the directive’s Annexes, including almost all European salamander

species, and permits are needed to keep and trade in these species. The directive led to the setting up of a network of Special Areas of Conservation across the European Union called Natura 2000.

References

Altig & McDiarmid (2007); Beebee & Griffiths (2000);

Duellman & Trueb (1986); Frost (2013); Green & Campbell (1992); Griffiths (1996); Heatwole (1994-2013); Houck & Arnold (2003); Larson et al. (2006); Mitchell & Gibbons (2010); Pasmans et al. (in press); Petranka (1998); Sever (2003); Stebbins & Cohen (1995); Stuart et al. (2008); Thorn (1969); Wells (2007).

25

longitudinal skin folds on flanks. There are two genera This family includes the largest living salamanders. in this family, Cryptobranchus, the Hellbender, in Cryptobranchid salamanders are specialised for an eastern North America, and Andrias in China and aquatic habitat comprising cold, fast-flowing, rocky, Japan. There are two extant species of Andrias, one and oxygen rich streams. They are generally found occurring in central China, the other in Japan. living in depressions under stones in streams and rivers. Females lay long, paired strings of several hundred eggs, which are fertilised externally by the In the fossil record, cryptobranchids are well representmale. Males guard the eggs until they hatch 2-3 months ed in the Cenozoic of Eurasia (Vasilyan et al., 2013). after laying. Metamorphosis is partial and the animals Fossils of Andrias are known from the Tertiary of Europe and western North America. For detailed are permanently aquatic. Adults have a number of characteristics of the Cryptobranchidae, see Thorn paedomorphic characters: they have small eyes, lack (1969), Estes (1981), Duellman & Trueb (1986), Larson eyelids and have one pair of gill slits. The gill slits remain open in the American species (Cryptobranchus), et al. (2003), and Browne et al. (2012). but are closed in the Asiatic species (Andrias). Lacrimals and septomaxillae are absent. The palatal teeth form References Browne et al. (2012), Duellman & Trueb (1986), a curved row parallel to the maxillary and premaxillary Estes (1981), Larson et al. (2003), Thorn (1969), Vasilyan teeth. Head large and broad. Head and body flattened; et al. (2013).

Cryptobranchidae Fitzinger, 1826

Chinese Giant Salamander, Andrias davidianus, Xiao Yu Dong (Small Fish Cave), Daba, Wenxian County, Sichuan. Photo: Ted Papenfuss.

26

Salamanders of the Old World | Cryptobranchidae

Andrias Tschudi, 1837 The cryptobranchid genus Andrias contains the largest living salamander species, with adults reaching a total length of more than 100 cm. Vomerine teeth located on anterior margin of vomer, parallel with maxillary tooth row; teeth form a long arc. Nasals in contact with maxilla; frontal does not enter external naris. Pteroid broad, almost in contact with base of maxilla. Hyoid arches cartilaginous. Two pairs of branchial arches. Body large, no spiracle on head. Distance between nostrils less than half the distance between the eyes. Tongue large. Tubercles on highly vascular skin (Zhao & Hu, 1988a).

The genus includes two closely related forms, which likely diverged in the Pliocene (about 4.3 MYA). Despite a small degree of genetic differentiation, they are considered separate species (Matsui et al., 2008a).

Andrias davidianus (Blanchard, 1871) Andrias japonicus (Temminck, 1836)

References

Matsui et al. (2008), Zhao & Hu (1988a).

Andrias davidianus (Blanchard, 1871) | Chinese Giant Salamander Description

Andrias davidianus is a very large, heavily built salamander. Head strongly depressed, snout obtusely truncate; nostrils small, rounded, close to the edge of the upper lip and at the corners of the truncated snout, the internasal space less than half that of the interorbital space. Eyes small, rounded, dorso-lateral in position, and without eyelid. Top of head more or less flat, with a rounded temporal protuberance above and behind each eye. Vomerine teeth in an arched series starting between the choanae, parallel to the maxillary and premaxillary series. A thin lower labial fold, starting about midway between nostril and eye to the angle of the mouth. Trunk less depressed than head, with 12-15 costal grooves, a strong vertebral groove, and strong lateral dermal folds. Legs short and sturdy with skin folds. Tail compressed. Tail length 59-80% of the snout-vent length (Liu, 1950). Dorsal tail-fin extending to the trunk. Skin slippery and porous, with wrinkles, folds and tubercles. Great variation in colour. Most specimens are dark brown, but individuals can be black, dark red, light brown or earth-toned. There are large irregular dark blotches on dorsal and ventral sides. Juveniles often have lighter colouration with small black spots. Albinos have been reported (Fei et al., 2006). No external sexual dimorphism. During the breeding season, cloacal lips are swollen in the male and flat in the female. Total length ca. 100 cm. Chang (1936) quotes a maximum of 180 cm, but most animals found nowadays are considerably smaller (Liu & Liu, 1998). Fei et al. (2006) give sizes of 760-900 mm for adult males and 470-875 mm for females (from Songtao, Guiding, Jiangkou, Leishan, Guizhou). Specimens of 115 cm weigh ca. 25 pounds (11.4 kg, Liu, 1950).

Diagnosis

The Chinese Giant Salamander is very similar to the Japanese Giant Salamander (Andrias japonicus) and differs from it in the arrangement of tubercles on the head and throat. The tubercles of A. davidianus are mostly in pairs, and much smaller and fewer than those of A. japonicus. The tubercles on the throat are characteristic for each species. In A. davidianus, these tubercles are very small and paired and are arranged in rows parallel to the lower jaw. In A. japonicus they are mostly large, single and irregularly scattered. The snout is less rounded and the tail a little longer in the Chinese species, which is also darker in colour with large black patches (Chang, 1936; Liu, 1950; Thorn, 1969). There is substantial genetic variability, but variations correlate poorly with geographical distribution over the three major river systems in which it occurs (Murphy et al., 2000, but see Tao et al., 2005). The genetic patterns discovered in these studies suggest a much higher gene flow between populations of A. davidianus than in A. japonicus (Browne et al., 2012).

Eggs and larvae

Clutch size depends on body weight of the female. A female of 0.5-3 kg can lay 300-600 eggs or more. Eggs are laid in a string in an underwater cavity occupied by a male, and are fertilised externally and guarded by the male until they hatch. Egg diameter is 5-8 mm and capsule diameter is 15-17 mm. Incubation takes 38-40 days at water temperatures of 14-21°C. Hatchlings measure 25-32.5 mm. External gills disappear when total length reaches 170-220 mm (Fei et al., 2006). Haker (1997) reports that eggs measured on average 22×19.2 mm and the diameter of the embryo was 8-9 mm. Reduction of gills began when the larvae were 200-250 mm total length (Haker, 1997). The larvae resemble the adult in shape. 27

Distribution

Andrias davidianus occurs in mountain streams in central China, from Qinghai to Jiangsu and south to Sichuan, Guangxi and Guangdong. It is found in the middle and lower tributaries of Chang Jiang (the Yangtze River), Huang He (the Yellow River) and Zhu Jiang (the Pearl River) (Liu & Liu, 1998). Records from Taiwan may be the result of introductions.

Habitat

Its habitat consists of rocky mountain streams and lakes with cool running water (less than 23°C), at moderate elevations of 100-1,200 m. Chinese giant Salamanders have been found at 4,200 m altitude in Qinghai. The animals inhabit submerged hollows and cavities along river banks and are permanently aquatic (Fei et al., 2006).

Behaviour

28

Adults live singly in deep water and larvae live in groups in crevices at shallower depths. They are mostly nocturnal and feed on aquatic invertebrates, such as crawfish and crabs, as well as on fish and frogs (Fei et al., 2006). Reproductive behaviour has been described for Andrias japonicus (Kawamichi & Ueda, 1998) and is probably similar in A. davidianus. In the reproductive season, May-September, the male occupies a breeding cavity which he aggressively guards against intruders.

The range of Andrias davidianus.

Andrias davidianus, habitat, Zhangjiajie National Forest Park, Hunan. Photo: Max Sparreboom.

Andrias davidianus, habitat, Zhangjiajie National Forest Park, Hunan. Photo: Max Sparreboom.

Salamanders of the Old World | Andrias

Eggs are laid from July to September. Females enter the cavity when they are ready to lay eggs and leave it directly after spawning. The male fertilises the eggs and guards them until they hatch (Fei et al., 2006).

Threats and conservation

Not only have populations become smaller and fragmented, but individuals sampled recently are smaller than formerly, most probably as a result of commercial over-collecting for human consumption (Liu & Liu, 1998; Wang et al., 2004). The Chinese Giant Salamander has also suffered from habitat destruction, for example through the construction of dams, and habitat degradation, such as water pollution from mines (IUCN, 2013). There are no data on abundance published in English. The species is considered Critically Endangered (IUCN, 2013), and is listed in the China Red Data Book of Endangered Animals (Zhao, 1998). It is protected under statute by the State Major Protected Wildlife Grade II (1988) and is listed in CITES Appendix I. Each province has its own local list of protected wildlife species. It is protected in the nature reserves of Fanjing Shan (Jiangkou, Yingjiang, and Songtao counties, Guizhou Province) and Dafengding (Ebian County, Sichuan Province) (Zhao, 1999).

The Chinese Giant Salamander is considered a delicacy and is collected for culinary and commercial purposes and its meat sells for high prices. It is used as a traditional Chinese medicine and supposedly helps to reduce anemia. The skin can be tanned to make leather (Fei et al., 2006). It can be bred in captivity and salamander farms have been founded to supply these markets. Commercial breeding farms were first established in Hunan, Shaanxi, Jiangxi and other provinces in the early 1970s (Liu & Liu, 1998). Salamanders are bred artificially in great numbers, but there are insufficient quantitative data to judge the viability of such farming (Dai et al., 2010). The vast majority of Chinese Giant Salamanders being traded are believed to originate from the wild (IUCN, 2013). In spite of the efforts of commercial farms, it is doubtful if the farming and artificial propagation described by Liu et al. (2000) will be able to alleviate the pressure on natural populations.

Observations in captivity

Outside China, the Chinese Giant Salamander was successfully bred in captivity in Germany by Haker (1997). The history of keeping giant salamanders in Europe is documented by Engelmann (2012) and Engelmann & Dirscherl (2013).

Comments

There is a vast body of literature, much of it in Chinese (cf. Ye et al., 1993 and references therein).

References

Browne et al. (2012); Chang (1936); Dai et al. (2010);

Engelmann (2012); Engelmann & Dirscherl (2013); Fei et al. (1999); Fei et al. (2006); Haker (1997); IUCN (2013); Kawamichi & Ueda (1998); Liu (1950); Liu & Liu (1998); Liu et al. (2000); Murphy et al. (2000); Tao et al. (2005); Thorn (1969); Wang et al. (2004); Ye et al. (1993); Zhao (1998, 1999).

Andrias davidianus, NW Guangxi. Photo: Michael Lau, courtesy Kadoorie Farm and Botanic Garden. 29

Andrias japonicus (Temminck, 1836) | Japanese Giant Salamander Description

Andrias japonicus is a heavily built salamander and one of the two largest extant salamander species. Head broad and flat. Body strongly depressed; terminal two-thirds of tail strongly compressed. Nostrils small, near tip of the snout, their distance from each other less than one-half the distance between the eyes, which are without eyelids and very small. Vomerine teeth in an arched series starting between the choanae, parallel to the maxillary and premaxillary series. Thin lower labial fold starting midway between nostril and eye to angle of mouth. Legs short and flattened. Tail short, slightly more than one-third the total length, with a high dorsal fin beginning at insertion of hind legs, and a lower ventral fin. Skin folds along each side of the body, continuing on to the hind legs (Thorn, 1969). Skin rather smooth and slippery, with wrinkles, folds and tubercles. Colour usually reddish-brown to brownish-yellow, paler below; irregularly blotched and marbled with dusky spots.

Considerable individual variation ranging from completely black to almost yellow. No external sexual dimorphism. During the breeding season, cloacal lips are swollen in the male and flat in the female. Total length of an adult Japanese Giant Salamander ranges from 30 to 150 cm – with a snout-vent length of 20-90 cm – a result of continuous growth after sexual maturity (Kawamichi & Ueda, 1998). Most specimens found in the wild are 60-70 cm in total length (Environment Agency of Japan, 2000). Weight of sexually mature animals ranges between 1.5 and 35 kg (in captivity). The heaviest specimen recorded in the wild was 26.3 kg and measured 136 cm (Tochimoto, pers. comm.). Andrias japonicus exhibits little genetic differentiation. This has been attributed to its polygynous mating system, delayed sexual maturity, longevity, life in a stable aquatic environment, and gigantism as well as bottleneck effects following habitat fragmentation (Matsui & Hayashi, 1992; Matsui et al., 2008a).

Diagnosis

The Japanese Giant Salamander is closely related and very similar to the Chinese Giant Salamander (Andrias davidianus) and differs from the latter in the arrangement of tubercles on the head and throat. These tubercles are larger and more numerous than in A. davidianus and are mostly single and irregularly scattered. The snout is more rounded and the tail a little shorter in the Japanese species.

Eggs and larvae Andrias japonicus, Ichi river, Asago, Hyogo Pref. Photo: Tim Johnson.

Spawning occurs in late August or early September. Eggs are deposited in long strings, containing 400-600 eggs. Diameter of egg 5 mm; diameter of external gelatinous capsule 8-15 mm. At water temperatures between 8 and 18°C embryonic development takes 40-60 days (Kuwabara et al., 1989). Larvae hatch in October-November at a total length of 30 mm and start feeding after absorption of the yolk. One year old larvae measure about 100 mm, three year olds some 200 mm. At this size larvae start losing their gills. Males reach sexual maturity at 30 cm, females at 40 cm. The larval period lasts about 4-5 years, and individuals take another 10 years to reach adulthood (Ministry of the Environment, Japan, 2008).

Distribution

The Japanese Giant Salamander is endemic to Japan, where it is found in the Chubu, Kinki and Chugoku regions of central and western Honshu, in Shikoku and in northeastern Kyushu (Tochimoto, 1996).

Andrias japonicus, Ichi river, Asago, Hyogo Pref. Photo: Max Sparreboom. 30

Salamanders of the Old World | Andrias

Habitat

This salamander occurs in habitats ranging from relatively large rivers (20-50 m wide) to small tributary streams

The animals keep themselves concealed in rocky caverns or in burrows on the water’s edge (Tago, 1927). The altitudinal distribution is 300-1,000 m. Spawning nests and larvae are often found in relatively small lotic habitats, including the upper reaches of tributary streams (Okada et al., 2008).

Behaviour

The range of Andrias japonicus.

(1-4 m wide), with clear, cool water flowing through granite and schist regions. These streams usually have rocky or gravel bottoms, and patches of shallow, quietly running water.

These salamanders are entirely aquatic and nocturnal. They feed on fresh-water crabs, fish, and small amphibians (Tago, 1927), and additionally on aquatic insects and small mammals (Goris & Maeda, 2005). Males and females have overlapping home ranges and are more or less sedentary outside the spawning period. During the breeding season, in AugustSeptember, both sexes congregate at underwater nest sites, consisting of 100-150 cm long burrows into or near the river bank. Nests have a single entrance opening underwater. Favourable nest sites may be used during successive years. Both males and females may occupy more than one nest at a time, with large and heavy males (‘den-masters’) attempting to monopolise occupancy of the nest sites. Nests are guarded from inside by males, attacking other males who try to enter. Males may also patrol around the nest area, chasing and attacking other males. Females enter the nests more than once and lay their eggs in the cavity, where they are fertilised by the male. At this stage several other males may intrude and try to fertilise the eggs. After spawning, den-masters remain at the nests for more than one month and aggressively guard the eggs until

Andrias japonicus, habitat, Hino river, Tottori Pref. Photo: Max Sparreboom. 31

hatching, or late October. Dominance rank of den-masters among males attempting to breed appears to be strong and dead and heavily injured males have often been found during September (Kawamichi & Ueda, 1998).

Threats and conservation

The range of this species is severely fragmented (Ohno, 1981). A continuing decline in the extent and quality of habitat, and in the number of locations where the animal is found has been observed (Matsui & Hayashi, 1992). Weirs, dams and river bank reinforcements constructed for flood and erosion control, agriculture, hydraulic power generation and road construction severely impact a large part of Andrias japonicus’s riverine habitat (Okada et al., 2008). The animal used to be hunted for food and medical purposes. In Japan the species has been fully protected by law since 1952; it is classified as Rare (Kato & Ota, 1993) and considered to be Near Threatened (Environment Agency of Japan, 2000; Ota, 2000a, 2000b; IUCN, 2013). The species is listed under Appendix I of the Convention on International Trade of Endangered Species (CITES) (Ministry of the Environment, Japan, 2008).

Many specimens of A. japonicus were found to be infected by Batrachochytrium dendrobatidis, a chytrid fungus known to be potentially lethal to amphibians, but it is too early to say whether this infection poses a threat to this species (Goka et al., 2009).

Stream habitats are becoming increasingly segmented and isolated by small agricultural dams and sand control dams, thereby inhibiting upstream migration of breeding giant salamanders. Research has shown that if these dams are equipped with uneven or rough surfaces to provide salamander toe-holds, or given gently-sloped detours, A. japonicus could traverse these barriers (Taguchi, 2009; Taguchi & Natuhara, 2009).

Observations in captivity

This species was first bred in captivity in the Amsterdam Zoo (Kerbert, 1905). The Japanese Giant Salamander is extremely long lived and a specimen in the Amsterdam Zoo lived for 52 years (Tago, 1927). The history of keeping giant salamanders in European zoos is described by Engelmann (2012). Hiroshima City Asa Zoological Park has successfully bred A. japonicus since 1979 (Kawata, 2012; Kuwabara et al., 1989). Presently (2010) the third generation is being raised in captivity. Researchers at Asa Zoo study giant salamander reproductive behaviour by observing salamanders breeding in man-made holes in branches of the Shijihara River in Hiroshima Prefecture (Kuwabara & Nakagoshi, 2009).

Comments

There is a vast literature on this species, much of it in Japanese. See Stejneger (1907), Sato (1943), Thorn (1969), and for more recent ecological studies by T. Tochimoto and J. Kobara, see references in Kawamichi & Ueda (1998).

References

Engelmann (2012); Environment Agency of Japan

(2000); Goka et al. (2009); Goris & Maeda (2005); IUCN (2013); Kato & Ota

Eco-friendly works to conserve habitats have begun in some areas and attempts have been made to rebuild spawning places along the Ichi River (Tochimoto, 1995,1996). It is only in recent years that some local governments, at the urging of concerned scientists, have begun flood prevention works that take into account the needs of the giant salamander (Goris & Maeda, 2005).

32

Salamanders of the Old World | Andrias

(1993); Kawamichi & Ueda (1998); Kawata (2012); Kerbert (1905); Kobara (1985); Kuwabara et al. (1989); Kuwabara & Nakagoshi (2009); Matsui & Hayashi (1992); Matsui et al. (2008a); Ministry of the Environment, Japan (2008); Ohno (1981); Okada et al. (2008); Ota (2000a, 2000b); Sato (1943); Stejneger (1907); Tago (1927); Taguchi (2009); Taguchi & Natuhara (2009); Thorn (1969); Tochimoto (1995, 1996).

The Hynobiidae is a monophyletic family, sister to the Cryptobranchidae. Hynobiids are small to moderatesized salamanders, ranging from about 10 to 20 cm total length. Metamorphosis is complete. Adults have eyelids and no gill slits. Larvae have four pairs of gill slits and caudal fins. The palatal dentition pattern is transverse, not paralleling the maxillary and premaxillary teeth. Metamorphosed adults are terrestrial outside the breeding season, except in the genera Batrachuperus, Paradactylodon, Liua and Pachyhynobius, which are found in water all year round. Adults have well-developed lungs except for the genus Onychodactylus, which is lungless. Hynobiids have an angular bone in the lower jaw, and large numbers of microchromosomes. Fertilisation is external. Eggs are laid in two arc-shaped, gelatinous egg sacs, which are

attached to stones or vegetation by a female and are fertilised by the male after deposition. The present distribution of the hynobiids is entirely Asian, ranging from Siberia westward to the Ural Mountains, southwestward to Turkestan, Afghanistan, and Iran, and southward to China, Korea and Japan, where most members of the family occur. The family Hynobiidae contains approximately 60 species assigned to nine genera: Batrachuperus (6 species), Hynobius (32 species), Liua (2 species), Onychodactylus (7 species), Pachyhynobius (1 species), Paradactylodon (3 species), Pseudohynobius (6 species), Ranodon (1 species) and Salamandrella (2 species). For detailed characteristics and evolution of the Hynobiidae, see references in Larson et al. (2003, 2006a), Zhang et al. (2006) and Xia et al. (2012).

Hynobiidae Cope, 1859

Hynobius tokyoensis, males and egg sacs. Hinode Town, Nishitama Dist., Tokyo Metropolis. Photo: Satoshi Sakuma.

33

b a

c

d

e

i

f

h

g

k

j

Egg sacs of hynobiid salamanders. Art: Bas Teunis.

Eggs of hynobiid salamanders

Egg clutches of hynobiid salamanders are deposited as a pair of gelatinous cases, containing a variable number of eggs (ova). Egg sacs are unique to hynobiid salamanders. The egg sac is a turgid, sausageshaped covering formed by the basal portion of the oviduct that encloses all of the ova once the jelly layers around the individual

34

Salamanders of the Old World | Hynobiidae

eggs have been formed by more anterior zones of the oviduct. Females usually extrude two unfused sacs per ovulation event, one from each oviduct. The sac is shaped like a curved or spiral sausage with a pointed distal end, which emerges first and serves as the pedicel (Altig & McDiarmid, 2007). The egg sacs are deposited in streams or ponds, according to species, and are

Egg sacs of hynobiid salamanders: a. Batrachuperus pinchonii. Egg sacs spiral- or C-shaped, ranging from 65-96 mm in length; 5-23 eggs in each egg sac, 3.7 mm in diameter (Fei & Ye, 2001). The drawing is based on photos (Sparreboom) of one egg sac in Wawu Shan Mountain, Sichuan, China, in April 2002 and on a photo in Fei & Ye (2001). b. Batrachuperus taibaiensis. Egg sacs nearly transparent with longitudinal striations; coiled and 15-17 cm long, each containing 27-29 eggs. Egg diameter 5.0-5.5 mm. The description and drawing are based on Li et al. (2008). c. Ranodon sibiricus. Just after deposition, the egg sac is tetrahedral in shape and has a bluish opalescence. Forty-eight hours after spawning the egg sac grows in size to approx. 48-60 mm. Most clutches contain 38-58 eggs. The egg has almost no pigmentation and is 3-5 mm in diameter. The description and drawing are based on Kuzmin & Thiesmeier (2001). d. Salamandrella keyserlingii. The clutch, consisting of two spiraled egg sacs, is attached to twigs and grasses. In the course of development, egg sacs may reach a length of 28 cm and a thickness of 32 mm. One clutch may contain 27-305 eggs, distributed asymmetrically between the two egg sacs. The fertilised egg is grey-brown, a little brighter at the vegetal pole, and measures 1.87-2.38 mm in diameter (Borkin, 1999). The drawing is based on photos in Sato (1993). e. Salamandrella tridactyla. Non-spiraled, banana-shaped egg sacs, belonging to a separate form of Salamandrella, recently recognised as a species (Salamandrella tridactyla) (Berman et al., 2005; Poyarkov & Kuzmin, 2008; Matsui et al., 2008b). The different shaped egg sacs are diagnostic for S. keyserlingii and S. tridactyla. The drawing is based on photos in Sato (1993). f. Onychodactylus koreanus. Two small, paired egg sacs, elliptical in shape with white, semitransparent walls. Mean length 35.7 mm, mean width 15.6 mm. 2-13 eggs in each sac; 10-22 eggs per pair of sacs; egg diameter 4.9-7.2 mm (Park, 2005). The drawing is based on photos in Park (2005) and on photos (Sparreboom) of egg sacs from Hwanseon-gul cave, Samcheok-shi, Kangwon-do, South Korea, August 2009.

attached to stones, twigs or vegetation. Usually, a number of males crowd around the spawning female and the eggs are inseminated as the egg sacs emerge from the female’s cloaca. The basic egg structure consists of an ovum with a vitelline membrane surrounded by several (up to eight) capsules, usually

g. Onychodactylus japonicus. Two small, paired egg sacs, elliptical in shape with white, semitransparent walls. Mean clutch size 11-24 eggs, egg diameter 4.5-5.4 mm (Kuzmin 1995). The drawing is based on a photo in Matsui & Seki (2008). h. Paradactylodon mustersi. Egg sacs 9-15 cm long, attached at the blunt end to the underside of rocks in the current. Egg sacs are at first transparent, becoming more cloudy with age (Reilly, 1983). The drawing is based on photos of one egg sac, deposited in captivity by a female caught in the Paghman valley, Afghanistan, in September 1976. The egg sac was 55 mm long shortly after deposition, containing 14 eggs with a diameter of 3.5 mm (Sparreboom, 1979). Initially the eggs have hardly any pigmentation. In the course of development the amount of pigment increases, as shown in the drawing. i. Paradactylodon gorganensis. Egg sacs contain four rows of eggs per cross section, producing a tetrahedral shape immediately after clutch deposition. Early eggs have a white animal pole and a pigmented, grey vegetal pole. On average 37.4 eggs per egg sac; egg sac length 80-182 mm; egg sac width 31-52 mm; egg diameter 4.1-5.0 mm (Ebrahimi et al., 2004). The drawing represents a reconstruction of what the earliest stage must have looked like, according to Ebrahimi et al., (2004). The description pertains to egg sacs found in Cheshme-ye Manzoulak, Shastkola forest, Iran. j. Liua tsinpaensis. The pair of egg sacs is coiled in a C-shape, the distal end tapering. Length 122-195 mm; 6-11 eggs in each egg sac, 13-20 in each pair. Eggs are oval in shape, 5 mm in diameter and light grey. The drawing is based on photos in Fei et al. (2010). k. Pachyhynobius shangchengensis. A pair of egg sacs is attached to the underside of a stone; length 38-57 mm; width 14-17 mm; each egg sac may contain 18-32 eggs. The egg sac envelopes are dull white with a bluish sheen and are longitudinally striated. Egg diameter on average 3.3 mm. The drawing is based on a photo of one of two pairs of egg sacs produced by captive animals, imported in 2001 and 2008 via the pet trade (Pasmans et al., 2012).

termed jelly layers, of oviductally-produced materials (Salthe, 1963; Altig & McDiarmid, 2007). The ova and capsules are variable in size. The innermost capsule of salamander eggs liquefies soon after deposition. Thus, the ovum, surrounded by the vitelline membrane, floats freely in a capsular chamber (Duellman & Trueb, 1986; Greven, 2003a). The embryo develops into a larva 35

n l m

o

p q

s

r

t u

Cont.: Egg sacs of hynobiid salamanders. Art: Bas Teunis.

inside the chamber. As the embryos approach hatching, the jelly layers and egg sac begin to break down. Hatching larvae break through the egg capsules first and leave the egg sac in the next stage. Suggested functions of egg jelly layers include mechanical support for the ovum, attachment of eggs to each other or a structure in the environment, enhancement or prevention of entry by conspecific and heterospecific sperm respectively, prevention 36

Salamanders of the Old World | Hynobiidae

of polyspermy, sperm capacitation, differential protection from water moulds, protection from contaminants, and protection from predators, pathogens, and environmental stressors such as temperature and UV light. Many of these functions are insufficiently understood and await further study (Greven, 2003a; Altig & McDiarmid, 2007) as is also the case for the egg sacs. The number, size and arrangement of eggs in the egg sacs vary among genera and are used as taxonomic characters for examining

l. Hynobius okiensis. A clutch consists of 20-60 eggs (Goris & Maeda, 2005). Egg sacs of this species have not been described in detail. The drawing is based on a photo of an egg sac laid in captivity (H. Wallays, 2000). m. Hynobius dunni. Egg sacs are 15-30 cm long and 2.5-3 cm in diameter, each containing 18-101 eggs of 2 mm diameter. The drawing is based on a photo of a clutch laid in captivity (K.-D. Kühnel). n. Hynobius quelpaertensis. Each egg sac contains 30-75 eggs. When fully hydrated, the egg sacs reach 8-12 cm in length and 8-10 mm in width. The drawing is based on a photo of a clutch laid in captivity (K.-D. Kühnel). o. Hynobius kimurae. The egg sac typically has a purplish sheen. Clutch size 17-40 eggs, egg diameter 4.2-5 mm (Akita & Miyazaki, 2009). The drawing is based on several photos from Tim Johnson. p. Hynobius boulengeri. The egg sacs have a light blue hue, are banana-shaped – not coiled – and have a distinct whip-like structure on the free end. Egg sacs from Honshu are 15-25 cm long and 13-26 mm in diameter. Clutch size between 32-55. Colour yellowish, animal pole more brownish. The drawing is based on a photo depicting a pair of egg sacs from the Kii Peninsula, Honshu (Nishikawa et al., 2008). q. Hynobius formosanus. The female produces a pair of transparent, string-like egg sacs, containing some 14-15 large eggs (4.25 mm diameter). Colour not uniform, but generally light yellowish with a brown tint, the brown fading with develop-

inter- and intrageneric relationships. Batrachuperus taibaiensis has a relatively long, thick egg sac which is strongly coiled and may contain 27-29 eggs. In contrast, the egg sac of Batrachuperus pinchonii is cylindrical and cayenne-shaped with 7-12 eggs. The egg sac of Batrachuperus yenyuanensis is linear and has 6-13 eggs (Li et al., 2008). Resemblance of egg sac shape may indicate close phylogenetic relationship, but is probably also affected by features of the breeding sites and could be a result of convergent evolution. Further study is required to clarify this issue (Nishikawa et al., 2010).

r.

s.

t.

u.

ment of the embryos (Kakegawa et al., 1989). The drawing is based on photos (Sparreboom) of recently laid egg sacs found in the Taiwan mountains in February 2008. Hynobius tokyoensis. Egg sacs transparent and bananashaped, containing 15-192 eggs, 2.5-3 mm in diameter. Clutch size and egg sac measures are very variable (Kusano, 1986; Ihara, 2002; Goris & Maeda, 2005). The drawing is based on photos (Sparreboom) of egg sacs from Yokosawaire, May 2011. Hynobius nigrescens. The female produces a pair of spindleshaped egg sacs, 9-13 cm long and 5-6 cm wide, whitish and often opaque (Takahashi & Iwasawa, 1989b). The outer envelope of the sac is soft and gelatinous and appears swollen. A clutch contains 40-140 eggs (Goris & Maeda, 2005) with a diameter of 2.5-3 mm, brown with a yellowish vegetal pole. The drawing is based on a photo in Inukai (1932). Pseudohynobius flavomaculatus. Egg sacs coiled in C-shape, the distal end tapering. Length 130-270 mm. 16-26 eggs per sac (Kuzmin & Thiesmeier, 2001). Eggs are round, 5.5 mm in diameter, and pale or light grey. The drawing is made from a photo in Fei et al. (2010). Hynobius retardatus. Egg sacs 5-6 cm long directly after spawning; after absorbing water they may increase in size to 23 cm. Egg diameter 3 mm (Sasaki, 1924; Thorn, 1969). Total clutch size 44-102 eggs (Sato, 1989). The drawing is inspired by the photo in Inukai (1932).

Hynobiids have either stream-type (Onychodactylus, Ranodon, Paradactylodon, Batrachuperus, Pseudohynobius, Liua, Pachyhynobius, and some Hynobius species) or pond-type (Salamandrella and most Hynobius species) life histories. Streamtype salamanders are also called lotic-breeders. They live in mountainous habitats and lay eggs in mountain streams. Pondtype species are so-called lentic-breeders, reproducing in ponds and marshes in lowland habitats (Nishikawa et al., 2010). The colour, shape and size of eggs and egg sacs often appear to be 37

related to the breeding environment. In general, stream-type eggs are large, non-pigmented and small in number. The egg sacs are small and attached to the under surfaces of large stones, or to the stream-bed under or by the sides of large stones, where water flow occurs. Pond-type eggs are usually small and have melanic pigment at the animal pole; the sacs contain a greater number of eggs and are attached to various substrates, in a more exposed environment. Whereas most hynobiid genera are either lotic- or lenticbreeders, the most species-rich genus Hynobius contains both lentic- and lotic-breeding species. Lotic-breeding species of Hynobius only occur in Japan and Taiwan, whereas lenticbreeding Hynobius species are distributed more widely in continental China, Korea and Japan. Lotic-breeders are more or less restricted to mountain streams, but among the lenticbreeding Hynobius there are some species that can occupy lowlands or hills, as well as mountainous regions so long as still waters for breeding are available (Nishikawa et al., 2010). The small-sized Taiwanese lotic-breeding Hynobius species produce small transparent egg sacs with a small number of large whitish eggs. There are differences in the shapes of the egg sacs among lentic-breeding Hynobius species, and also between the two Salamandrella species. For instance, many species produce spiral, string-shaped egg sacs (most Hynobius species from continental China), while others produce spindle- or bananashaped egg sacs (H. guabangshanensis and H. maoershanensis from southern China) (Nishikawa et al., 2010). Salamandrella keyserlingii has spiral, string-shaped sacs, while those of

38

Salamanders of the Old World | Hynobiidae

S. tridactyla are more banana-shaped. Hynobius nigrescens is unique in that it produces spindle-shaped, milky white, opaque egg sacs. Some lotic hynobiids have compact egg sacs with strong longitudinal striations, such as Pachyhynobius shangchengensis and Ranodon sibiricus. Description of hynobiid egg sacs is complicated by the fact that the shape and size of the egg sac change during development. Shortly after deposition the egg sacs begin to swell as they absorb water, resulting in a gradually increasing length and width. The surface of the egg sac also undergoes changes. It may initially become turgid and later turn flabby. Furthermore the surface may be affected by small particles from the pond which stick to the egg sac and render it opaque. The drawings give an idea of the range of different egg sac types, without aiming at completeness. They are based on photos, illustrations in publications and on first hand observation. To facilitate comparison, the egg sacs are depicted in the early stages of development.

References

Akita & Miyazaki (2009), Altig & McDiarmid (2007),

Berman et al. (2005), Borkin (1999), Duellman & Trueb (1986), Ebrahimi et al.(2004), Fei & Ye (2001), Fei et al. (2010), Goris & Maeda (2005), Greven (2003a), Ihara (2002), Inukai (1932), Kakegawa et al. (1989), Kusano (1986), Kuzmin (1995), Kuzmin & Thiesmeier (2001), Larson et al. (2003, 2006), Li et al. (2008), Matsui et al. (2008b), Matsui & Seki (2008), Nishikawa et al. (2008, 2010), Park (2005), Pasmans et al. (2012), Poyarkov & Kuzmin (2008), Reilly (1983), Salthe (1963), Sasaki (1924), Sato (1993), Sparreboom (1979), Takahashi & Iwasawa (1989a, 1989b), Thorn (1969), Xia et al. (2012), Zhang et al. (2006).

Batrachuperus Boulenger, 1878 Batrachuperus is a group of medium-sized, high altitude salamanders. It shares three significant traits with the three species of the genus Paradactylodon, which used to be placed within Batrachuperus: completely aquatic habits; large premaxillary fontanelle; and four toes on the hindlimb (Zhang et al., 2006). Vomerine teeth in two short transverse rows, separated by a more or less wide space. Horny extensions (‘claws’) on tips of toes and digits, sometimes also on other parts of limbs and body. Tail flattened. Lungs present. The genus Batrachuperus presently comprises six described species, all occurring in western China on the eastern border of the Tibetan plateau, where they live in fast-running streams. The current classification and species designation is based on external features. Disagreement among researchers on how many species there are, and which of the named species are synonyms, is due to the lack of consistent morphological characters. The taxonomy of the species belonging to this genus – which contains cryptic species, thus far not described – requires further investigation (Fu et al., 2001; Fu & Zeng, 2008). An undescribed species, distributed in the central and southern Shaluli Mountains, has been referred to as ‘Daocheng species’ and corresponds to B. sp. 2 in Fu & Zeng (2008) (Lu et al., 2012). Batrachuperus karlschmidti and the

Daocheng species occur at high elevations in the west of the genus range (at 3,500-4,300 m) such as the Shaluli and Daxue Mountains, while B. londongensis, B. pinchonii and B. yenyuanensis occur mainly in the eastern lower reaches (at 1,800-3,200 m), such as Emei, Luoji and Bailing mountains (Lu et al., 2012). Batrachuperus tibetanus has a broad central Chinese distribution (Fei et al., 2006).

Batrachuperus karlschmidti Liu, 1950 Batrachuperus londongensis Liu & Tian, 1978 Batrachuperus pinchonii (David, 1872) Batrachuperus taibaiensis Song, Zeng, Wu, Liu & Fu, 2001 Batrachuperus tibetanus Schmidt, 1925 Batrachuperus yenyuanensis Liu, 1950

References

Fei et al. (2006); Fu et al. (2001); Fu & Zeng (2008); Lu et

al. (2012); Zhang et al. (2006).

Batrachuperus karlschmidti Liu, 1950 | Schmidt’s Stream Salamander Description

Body cylindrical and rather stout, with 11 to 13 costal grooves. Snout squarish rather than rounded. Labial folds well-developed. Shape and number of vomerine teeth vary greatly. Limbs short; when adpressed, the tips of the longest digits separated by more than two costal spaces. A large pad between the bases of the first and second fingers and another between the bases of the first and second toes; tips of digits covered with dark brown horny epidermis; no horny epidermis on the palms and soles. Tail strong, a little shorter than snoutvent length, cylindrical at the base, flattened gradually toward the tip; only the posterior part of the dorsal side of the tail-fin is thin, as is the extreme tip of the tail; ventral side of the tail thick and rounded. Vent quadrangular with a groove behind (Liu, 1950). Colour nearly uniform, dark grey or olive-green above and lighter below, normally without spots or marbling. In the male, the vent is a transverse crescent-shaped opening with a large light-coloured papilla in the middle and a longitudinal groove posterior to it. The vent of the female is a

longitudinal opening, without a transverse crescent-shaped opening and no papilla. The vent is more prominently swollen in the female than in the male. Tail relatively longer and body shorter in the male than in the female (Liu, 1950). Total length 18-20 cm (Liu, 1950).

Diagnosis

According to Liu (1950) the species differs from other Batrachuperus species in its total lack of spots and marblings and in the wide separation of vomerine tooth patches, but the diagnostic value of these characteristics is contested (Fu et al., 2001; Fei et al., 2006; Fu & Zeng, 2008). Fu et al. (2001) use mitochondrial DNA data to support the validity of B. karlschmidti.

Eggs and larvae

Egg sacs ranging from 75 to 96 mm in length are attached to the under surfaces of large stones, or to the stream-bed under or by the sides of large stones, where flowing water passes through. They are mostly found in very small brooks, especially near their sources where spring water seeps out of the ground or from under stones. From 7 to 12 eggs, 39

Batrachuperus karlschmidti, Zeduo Mt, Kangding Pref., Ganzi Tibetan Autonomous Region, Sichuan. Photo: Hou Mian, courtesy Zeng Xiaomao.

on average 3.7 mm in diameter, per egg sac; a female may carry more than 45 eggs (Liu, 1950). Larvae hatch at 15-16 mm length. Fully developed larvae are nearly black above, with a lighter underside. Metamorphosis starts when the larvae reach a total length of 8-9 cm. Colour at this stage varies, with indistinct marblings or spots on a dark ground colour. After completion of metamorphosis the animals may be found together with adults in the larger mountain streams (Liu, 1950). According to Liu (1950), who gives an elaborate description of the larva of this species, larvae of Batrachuperus pinchonii and B. karlschmidti differ in size and condition of the gills.

Behaviour

Food consists of aquatic animals, mainly gammarids and stonefly larvae. The breeding season probably lasts from May to the first part of August. Larvae live individually in quiet parts of small streams, while fully metamorphosed juveniles are found together with the adults in the larger mountain streams (Liu, 1950).

Distribution

Batrachuperus karlschmidti is found in Xinduqiao County, Sichuan, China, where it occurs in mountain streams at elevations of 1,800-4,000 m (IUCN, 2013).

Habitat

A largely aquatic species associated with slow-flowing streams in grassland areas (IUCN, 2013). Adult specimens are found under flat stones near the margins of streams, while larvae and small metamorphosed individuals are generally found under stones in the upper reaches of small streams, especially in springs, which are the principal breeding sites (Liu, 1950).

40

Salamanders of the Old World | Batrachuperus

The range of Batrachuperus karlschmidti.

Threats and conservation

Over-collecting for traditional Chinese medicine is a major threat. The species is further threatened by overgrazing of habitat by livestock (IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Current descriptions and classification of species of Batrachuperus are based on morphological features

(Zhao & Jiang, 1988; Fei et al., 2006). However, many morphological traits may be highly variable within species (Fu et al., 2001; Fu & Zeng, 2008) and are therefore not suitable as diagnostic characters. Some authors consider B. karlschmidti to be a junior synonym of B. tibetanus (Fei et al., 2006), but molecular work suggests B. karlschmidti belongs to a separate clade, sister to B. tibetanus (Fu & Zeng, 2008).

References

Fei et al. (2006); Fu et al. (2001); Fu & Zeng (2008); IUCN

(2013); Liu (1950); Zhao & Jiang (1988).

Batrachuperus londongensis Liu & Tian, 1978 | Londong Stream Salamander Description

Batrachuperus londongensis is a large, robust salamander with a flattened head, longer than wide, with short rounded snout. Eyes prominent, projecting laterally. Labial fold well-developed, partly covering lower jaw. It was described on the basis of exceptionally large-bodied individuals in a population on Mt. Omei, which show a tendency to neoteny, many of the adults having remnant gills or open gill slits. The following description is a summary of the species entry in Fei et al. (2006). Body slightly flattened with 12-13 costal grooves; tail thick and cylindrical at the base, flatter towards the tip. Limbs short and thick; when adpressed there are one to four costal grooves between fingers and toes. Dark horny cover on limbs, especially on toes and digits.

Batrachuperus londongensis, Longdong river, Emeishan, Sichuan (type locality). Photo: Hou Mian, courtesy Zeng Xiaomao.

Colour black-brown on the back and sides; some individuals have irregular brown-yellow or orange-yellow spots on the body. Throat light purple-grey, underside purple-grey with irregular black-blue spots.

In the male, the vent is a transverse crescent-shaped opening with a light-coloured papilla in the middle. The vent of the female is a longitudinal opening.

Batrachuperus londongensis, Emeishan, Sichuan. Photo: Max Sparreboom.

Batrachuperus londongensis, Emeishan, Sichuan. Photo: Max Sparreboom. 41

Maximum length males 26 cm, females 23 cm.

Diagnosis

A large salamander with remnants of gills or open gill slits in adults.

Eggs and larvae

One egg sac was found in pieces and recovered. It was around 20 cm long. Largest eggs found in a female’s ovary were 3.5-4.0 mm. According to local observers larvae hatch around April.

Distribution

Previously, only a single population in the Longdong River (Mt. Omei, Sichuan, China, from 1,300 to 1,800 m altitude) was considered to belong to Batrachuperus londongensis (Fei et al., 2006), but a molecular study has identified most populations from Mt. Omei (except those at the summit), Mt. Wawushan in nearby Hongya County, and Mt. Nibashan in Hanyan County as B. londongensis. All of these populations were previously identified as B. pinchonii (Fu & Zeng, 2008).

Habitat

Inhabits deeper parts of the lower section of rivers and springs in forested areas. Stones to hide under and stick egg sacs to are crucial elements in the habitat (Fei et al., 2006).

Behaviour

Salamanders of the type locality are found under stones in the fast-flowing deeper parts of the river.

The range of Batrachuperus londongensis.

Threats and conservation

Over-collecting for traditional Chinese medicine and for food is a major threat. Based on the situation at the type locality the species is listed as Endangered. Some measures have been taken to preserve its habitat, such as a prohibition on the removal of stones in the river for construction work (Fei et al., 2006; IUCN, 2013).

Batrachuperus londongensis, habitat, Longdong river, Emeishan, Sichuan. Photo: Max Sparreboom. 42

Salamanders of the Old World | Batrachuperus

Observations in captivity

There are no reports of this

species being kept in captivity

Comments

Current descriptions and classification of species of Batrachuperus are based on morphological features (Zhao & Jiang, 1988; Fei et al., 2006). Recent work has shown that many morphological traits may be highly variable within

species (Fu et al., 2001; Fu & Zeng, 2008) and therefore not suitable as diagnostic characters. According to Fu & Zeng (2008), populations near Mt. Omei, formerly considered to belong to B. pinchonii should also be assigned to B. londongensis.

References

Fei et al. (2006); Fei & Ye (2001); Fu et al. (2001);

Fu & Zeng (2008); IUCN (2013); Liu (1950); Zhao & Jiang (1988).

Batrachuperus pinchonii (David, 1872) | Stream Salamander Description

Batrachuperus pinchonii is a slender salamander with a flattened head, longer than wide, with short rounded snout. Eyes prominent, projecting laterally. Mouth wide, buccal angle situated below eye; labial fold well-developed, partly covering lower jaw, which also has a fold but less well-developed. Vomerine teeth in two small transverse rows, situated at the middle and on the line of the choanae, separated from each other by a distance equaling half the length of each row. Neck rather long, provided with a fold curved anteriorly. Body cylindrical, of medium length, measuring three times length of head, with 12 costal grooves. Tail shorter than snoutvent length, cylindrical at the base and gradually diminishing toward the end. It shows a straight superior keel that becomes a low crest terminating in a rather obtuse point. Feet flattened;

digits of fore and hindlimbs overlapping or meeting if laid along the body. A soft, cornified sheath under carpus and tarsus, extending to beyond the phalanges like a nail. Cornification of digits extending to palms and soles, lower parts of lower limbs and tip of tail. Most animals have two tubercles on each palm or sole. Skin smooth, with minute pores everywhere except on the throat and under the palms and soles. A vertebral groove; another groove extending from eye to gular fold marks the paratoid; throat exhibits distinct longitudinal folds in front of gular fold. Colour uniform, with light brown background colour on the back and dorsal sides of the limbs and tail; irregularly scattered dark spots and markings on sides of the tail; some specimens

Batrachuperus pinchonii, Erlangshan mountain, Tianquan County, Sichuan. Photo: Hou Mian, courtesy Zeng Xiaomao. 43

have dark spots more concentrated, and arranged more or less in dorso-lateral rows (Chang, 1936; Liu, 1945, 1950). In the male, the vent is a transverse crescent-shaped opening, convex anteriorly, with a light-coloured papilla in the middle of the anterior lip. A shallow longitudinal groove extends backwards from the middle of the transverse opening. The vent of the female is a longitudinal opening, with or without lateral grooves. The vent is more prominently swollen in the female than in the male. Total length males 18-20 cm, females 15-18 cm (Fei & Ye, 2001), but can also be much smaller (males c. 12-14 cm, females 10-13 cm, Fei et al., 2006). According to measurements by Liu (1950) males are on average 13-14 cm and females 14-15 cm.

Diagnosis

A salamander with depressed head and prominent eyes, four fingers and four toes. Light brown epidermis covering palms and soles and extending to lower parts of arms and legs, covering ventral sides of all digits and even extending to dorsal sides of first or second segments of fingers and toes. Batrachuperus pinchonii usually has two small tubercles on

each palm and sole and shares this character only with B. yenyuanensis, but differs from that species in having a shorter and stronger tail, longer and stronger limbs, and large dark spots on the back (Liu, 1950).

Eggs and larvae

The female lays a pair of egg sacs, attaching one end to stones, with 5-23 eggs in each sac. Egg sacs are spiral or C-shaped, ranging from 65 to 96 mm in length. Eggs are oval and 3.7 mm in diameter (Fei & Ye, 2001). The larva is brown or dark grey above, and lighter on the underside. At 30 mm length the tail-fin fold becomes apparent, beginning from the middle of the tail. Three pairs of gills. At 50 mm, coloured spots appear, the gills become shorter and horny extensions of toes and digits become apparent. At around 80 mm length metamorphosis is complete (Fei et al., 2006). According to Liu (1950), larvae of Batrachuperus pinchonii and B. karlschmidti differ in size and form of the gills. Batrachuperus pinchonii has fewer gill filaments, and these are arranged in one row only, except on the third gill, while in B. karlschmidti the gill filaments are in two rows on each gill. The fleshy bases of the gills are welldeveloped in B. karlschmidti and only poorly so in B. pinchonii. Larvae of B. pinchonii are much smaller than B. karlschmidti larvae of the same stage (Liu, 1950).

Distribution

Batrachuperus pinchonii is found in western Sichuan and northwestern Yunnan. It occurs in and near rivers and mountain streams, at elevations of 1,500-3,900 m (Fei & Ye, 2001).

Batrachuperus pinchonii, larva, Wawu Mts, Sichuan. Photo: Max Sparreboom.

Batrachuperus pinchonii, juvenile, Wawu Mts, Sichuan. Photo: Max Sparreboom. 44

Salamanders of the Old World | Batrachuperus

The range of Batrachuperus pinchonii.

Habitat

The species inhabits high-altitude streams and lakes, and surrounding broadleaf and coniferous forests, and sometimes occurs in marshy grassland. Adults live under stones and logs which have fallen into the stream. Some adults stay under roots of vegetation on the bank (Fei et al., 2006). Larvae and recently metamorphosed juveniles are found in the upper reaches of streams or springs (Liu, 1950).

Behaviour

Food consists of larvae of trichopterans, plecopterans and shrimp, and adults may eat their own larvae (Fei et al., 2006). Egg sacs may be found from April to July, at water temperatures of approx. 8°C. Larvae live individually in quiet parts of the stream.

Threats and conservation

Over-collecting for traditional Chinese medicine and for food is a major threat. Harvesting methods include poisoning and electrocution. The species is listed as Vulnerable and the need to implement measures to ensure that harvesting of this species from the wild is managed sustainably is recognised (IUCN, 2013).

Batrachuperus pinchonii, habitat, Wawu Mts, Sichuan. Photo: Max Sparreboom.

Observations in captivity

There is one provisional report of this species being kept in captivity (Fleck, 2011a).

Comments

Batrachuperus pinchonii is introduced here with a detailed description based on Chang (1936) and Liu (1950). It is the taxon from which most other Batrachuperus species have been separated later. Current descriptions and classification of species of Batrachuperus are based on morphological features (Zhao & Jiang, 1988; Fei et al., 2006). Recent work has shown that many morphological traits may be highly variable within species (Fu et al., 2001; Fu & Zeng, 2008) and therefore not suitable as diagnostic characters.

References

Chang (1936); Fei et al. (2006); Fei & Ye (2001); Fleck,

(2011a); Fu et al. (2001); Fu & Zeng (2008); IUCN (2013); Liu (1945,1950); Zhao & Jiang (1988).

Batrachuperus pinchonii, habitat, Wawu Mts, Sichuan. Photo: Max Sparreboom.

Batrachuperus taibaiensis Song, Zeng, Wu, Liu & Fu, 2001 | Taibai Stream Salamander

Description

Batrachuperus taibaiensis is a large, stout salamander. Head moderately depressed, longer than wide; snout short and rounded. Labial folds well-developed, partially covering lower jaw. Eleven costal grooves. Limbs relatively short but strong; when adpressed, tips of digits do not overlap and are always separated by 1-3 costal grooves in adults. Most individuals without palmar and tarsal tubercles. No horny covers on palms, tarsus, and ventral side of fingers and toes. Some individuals have a horny cover on tips of digits. Tail round at the base and

gradually flattening laterally. Tail-fin moderately high. Colour dark or olive-grey on the back, sometimes with small dark spots and light grey on the underside. Snout-vent length a little longer than tail length in males, about the same in females. Total length males 15-22 cm, females 18-22 cm.

Diagnosis

A relatively large, robust salamander, distinguished from other members of the genus by its large size, 45

vomerine teeth arranged in inverted V shape, and lack of horny cover on palms and tarsus. Batrachuperus taibaiensis is distinguished from geographically neighbouring species B. tibetanus by its larger size and the arrangement of vomerine teeth (the description above is a summary of Song et al., 2001), but see comments below.

Eggs and larvae

Egg sacs, coiled and 15-17 cm long, were found attached to the underside of rocks in streams in April, each containing 27-29 eggs. Egg diameter was given as 5.0-5.5 mm. Free swimming larvae were found at stream edges under small stones in the beginning of August. Measurements of larvae are given by Li et al. (2008).

Distribution

Batrachuperus taibaiensis is known from the type locality of the upper stream of the Heihe River, Zhouzhi County, Shaanxi Province, China, at 1,260 m altitude. It is believed to range throughout the Taibeishan Mountains in

Shaanxi (IUCN, 2013), and thought to extend to Gansu and northern Sichuan (Zeng, 2004 in Li et al., 2008). Li et al. (2008) studied the salamanders in the upper part of two rivers and their associated streams on the northern and southern sides of Ping He Liang, from 1,800 to 2,000 m altitude.

Habitat

Like other species of Batrachuperus, B. taibaiensis inhabits fast-flowing streams and can be found under rocks in the stream and on the banks. Subalpine conifers characterise the surrounding habitat, with vegetation often hanging over rivers and streams. Liua tsinpaensis was found in the same streams and B. pinchonii was wide-spread at lower elevations near the Tsinling Mountains, where B. taibaiensis was studied by Li et al. (2008).

Behaviour

The breeding season most likely lasts from April to July, as the youngest larvae with gills and the highest number of juveniles in different stages of development were collected in early August (Li et al., 2008).

Threats and conservation

The main threats are loss of forest habitat surrounding the streams as a result of clear-cutting, and harvesting of animals for medicinal use (IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Current descriptions and classification of species of Batrachuperus are based on morphological features (Zhao & Jiang, 1988; Fei et al., 2006). Many morphological traits may be highly variable within species (Fu et al., 2001; Fu & Zeng, 2008) and therefore not suitable as diagnostic characters. Allozyme data did not support the separation of B. taibaiensis and B. tibetanus (Fu & Zeng, 2008), but the authors suspended synonymising B. taibaiensis with B. tibetanus until more morphological data were available.

References

Fei et al. (2006); Fu et al. (2001); Fu & Zeng (2008); IUCN

(2013); Li et al. (2008); Liu (1950); Song et al. (2001); Zhao & Jiang (1988).

The range of Batrachuperus taibaiensis.

Batrachuperus tibetanus Schmidt, 1925 | Tibetan Stream Salamander Description

Batrachuperus tibetanus is difficult to distinguish from B. pinchonii (Liu, 1950). See under B. pinchonii for a more detailed general description. According to Liu (1950) T. tibetanus can be distinguished from all other species of the genus by its 13 costal grooves and more posteriorly located vomerine teeth, a characteristic not mentioned by Fei et al., who studied a larger number of specimens from more localities and

46

Salamanders of the Old World | Batrachuperus

counted 12 costal grooves (Fei et al., 2006). Batrachuperus tibetanus is separated from B. pinchonii and B. yenyuanensis by the absence of palmar and solar tubercles and its spotted back and tail differ from those of the more or less uniformly coloured karlschmidti (Liu, 1950). According to the key to species of Batrachuperus by Fei et al. (2006): the tail is wide and short, usually shorter than snout-vent length; the tail muscles are

Batrachuperus tibetanus, Ma er-kang Pref., Aba Tibetan & Qiang Autonomous Region, Sichuan. Photo: Hou Mian, courtesy Zeng Xiaomao.

well-developed; the tail-fin fold starts two thirds of the way down the tail; the metacarpal and metatarsal tubercles are not very obvious; the labial folds are well-developed, and the tailfin fold is obvious. Colour dark or olive-grey on the back, sometimes with small dark spots, the underside is light grey. As in B. pinchonii, in the male the vent is a transverse crescentshaped opening, convex anteriorly, with a light-coloured papilla in the middle of the anterior lip. A shallow longitudinal groove extends backwards from the middle of the transverse opening. The vent of the female is a longitudinal opening, with or without lateral grooves. The vent is more prominently swollen in the female than in the male (Liu, 1950). In males tail length exceeds snout-vent length; in females the tail is shorter but snout-vent length is longer than in the male (Fei & Ye, 2001; Fei et al., 2006). Total length males 18-21 cm, females 17-20 cm (Fei & Ye, 2001; Fei et al., 2006).

Diagnosis

Very similar to Batrachuperus pinchonii, from which it is distinguished by: the absence of tubercles and the

horny covering of palms and soles; the weak and low tail; the smaller head; the longer trunk; and the more posteriorly situated vomerine teeth (Liu, 1950). It differs from B. yenyuanensis in having a shorter tail and absence of tubercles on palms and soles. The dorsal tail-fin starts from the tail-base in B. yenyuanensis and only from the posterior two thirds of the tail in B. tibetanus. It differs from B. karlschmidti in having black marblings on the back (Fei et al., 2006).

Eggs and larvae

The female lays a pair of egg sacs, attaching one end to stones, with 16-25 eggs of 3.7 mm diameter in each sac. Egg sacs are 12-22 cm in length. When the larvae approach a length of 33-35 mm, a horny cover develops on fingers and toes and the dorsal fin starts to develop from the back. At a length of 41 mm the dorsal fin begins from the tail-base. At 49 mm the dorsal and ventral tail-fins become lower and the gills become shorter. From 64 mm the gills start to shrivel and metamorphosis begins (Fei et al., 2006). At this stage the larva has all the adult characters and a distinct light-coloured vertebral groove running from behind the head to the tail-base (Liu, 1950).

Distribution

Batrachuperus tibetanus is found in central China, in the provinces of Sichuan, Shaanxi, Qinghai, Xizang 47

(Tibet) and Gansu. It occurs at altitudes from 1,500 to 4,250 m (Fei & Ye, 2001; Fei et al., 2006).

Habitat

This species inhabits the highlands, especially above 3,000 m. It lives in small mountain streams of 1-2 m width, and also in streams of 4 m or more wide, 15-40 cm deep, with many stones on the bottom. During the day adults hide under stones and rotten wood. They are active at night and may occasionally be seen on the banks. Egg sacs, larvae and juveniles are found further upstream (Fei et al., 2006).

Behaviour

Food consists mainly of shrimps and insect larvae. The breeding season lasts from May to early August and most egg sacs are found in May-June at air temperatures between 10 and 24°C and water temperatures between 6 and 13°C (Fei et al., 2006).

Threats and conservation

Over-collecting for traditional Chinese medicine and for food is a major threat to this species. Other threats are habitat loss and water pollution resulting from mining activities. Due to over-exploitation in recent years, its population has declined dramatically. The species is listed as Vulnerable (IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Current descriptions and classification of species of Batrachuperus are based on morphological features (Zhao & Jiang, 1988; Fei et al., 2006). Many morphological traits may be highly variable within species (Fu et al., 2001; Fu & Zeng, 2008) and therefore not suitable as diagnostic characters. Gene tree and allozyme frequency data led Fu & Zeng (2008) to suggest tentatively that B. taibaiensis and B. cochranae are not valid species. Accordingly, B. cochranae has been synonymised with B. pinchonii and eventually B. taibaiensis might have to be synonymised with B. tibetanus.

References

Fei et al. (2006); Fei & Ye (2001); Fu et al. (2001);

Fu & Zeng (2008); IUCN (2013); Liu (1950); Zhao & Jiang (1988).

The range of Batrachuperus tibetanus.

Batrachuperus tibetanus, habitat, Wolong National Natural Reserve, Sichuan. Photo: Max Sparreboom. 48

Salamanders of the Old World | Batrachuperus

Batrachuperus yenyuanensis Liu, 1950 | Yenyuan Stream Salamander having a longer and less muscular tail and a prominent tail-fin fold starting from the tail-base (Liu, 1950; Fei et al., 2006; but see comments).

Eggs and larvae

The female lays a pair of egg sacs, attaching one end to stones in the stream, with 6-13 eggs in each sac, a 12-25 eggs in total. Egg sacs are slightly curled and range from 70 to 125 mm in length (Fei & Ye, 2001; Fei et al., 2006).

Distribution

Batrachuperus yenyuanensis is found in southwestern Sichuan (Yanyuan, Mianning, and Puxiong counties), China, at altitudes of 2,900- 4,400 m, but mostly at 3,200- 3,500 m (Fei & Ye, 2001; IUCN, 2013). The distribution of this species appears to be nested within the range of B. pinchonii (Fu & Zeng, 2008).

Batrachuperus yenyuanensis, Mt. Luoji Lakes, 3,860 m, Sichuan. Photo: Max Sparreboom.

Description

Batrachuperus yenyuanensis is a slender salamander, body dorso-ventrally depressed, with 12 costal grooves. Head greatly depressed; snout rounded; labial folds strongly developed; skin on throat very loose, with many longitudinal folds. Two short, slightly curved patches of vomerine teeth. Limbs well-developed; longest digits meet when limbs are adpressed. Tips of fingers and toes covered with dark, thickened, horny epidermis; two darker cornified tubercles on palm and sole are very distinct. Digits much more flattened and pointed than in any other species of Batrachuperus and exhibit abnormalities in number, shape and size. Tail longer than body, cylindrical at the base, flattened toward the tip; tail-fin thin and high (Liu, 1950). Colour dark brown above, indistinctly stippled with black; light grey below, distinctly stippled with black (Liu, 1950). Fei & Ye (2001) specify: back either dark brown, dirty yellow, or bluishgrey, overlaid with irregular, dark, cloud-like patterns; underside greyish-yellow. The male has a transverse crescent-shaped vent, with a lightcoloured papilla in the middle of the anterior edge. In the female the vent is a longitudinal slit with swollen lips. Total length males 16-21 cm, females 14-18 cm (Fei & Ye, 2001).

Diagnosis

Batrachuperus yenyuanensis usually has two distinct small tubercles on each palm and sole and shares this character only with B. pinchonii, but differs from that species in

The range of Batrachuperus yenyuanensis.

Habitat

Occurs in and near high-altitude streams and lakes and can be found from spring to autumn under rocks, branches and fallen leaves. Inhabited streams are 1-2 m wide and not deeper than about 30 cm, surrounded by coniferous trees, rocks, sand and fallen leaves (Fei et al., 2006).

Behaviour

From October to February hibernating salamanders may be found on land and several individuals have been found under a single stone. Egg sacs are found in great numbers from the end of March to the end of April. Larvae hatch from the end of May to June (Fei et al., 2006). 49

Batrachuperus yenyuanensis, habitat, Mt. Luoji Lakes, 3,860 m, Sichuan. Photo: Max Sparreboom.

Threats and conservation

Over-collecting for traditional Chinese medicine and for food is a major threat. The species is listed as Vulnerable and the need to implement measures to ensure that harvesting of this species from the wild is managed sustainably is recognised (IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Current descriptions and classification of species of Batrachuperus are based on morphological features (Liu, 1950; Zhao & Jiang, 1988; Fei et al., 2006). Many morphological traits may be highly variable within species (Fu et al., 2001; Fu & Zeng, 2008) and therefore not suitable as diagnostic characters. Fu & Zeng (2008) suggest that the long tail and high tail-fins of B. yenyuanensis are possibly variable, habitat-specific characters and may represent a local adaptation to a lentic environment.

Batrachuperus yenyuanensis, Mt. Luoji Lakes, 3,860 m, Sichuan. Photo: Max Sparreboom. 50

Salamanders of the Old World | Batrachuperus

References

Fei et al. (2006); Fei & Ye (2001); Fu et al. (2001);

Fu & Zeng (2008); IUCN (2013); Liu (1950); Zhao & Jiang (1988).

Hynobius Tschudi, 1838 The hynobiid genus Hynobius forms a fairly large, uniform group of salamanders that share many morphological and biological characteristics. Body usually small, tail shorter than snout-vent length; palms and soles without cornified coverings; four fingers and usually five toes. Lungs present. Tongue broad and rounded. Length of egg sac equal to or greater than total length of adult. Vomerine teeth V-shaped; no dorsal fontanelle in skull. They live on land outside the breeding season (Zhao & Hu, 1988b). Most Hynobius species have pond-type life histories (lowland habitats, reproduction in still waters, a large number of small pigmented eggs); but a smaller number have stream-type life histories (hill and mountain habitats, reproduction in streams, a small number of large un-pigmented eggs), but this division is not always clear-cut. The genus is distributed in China, Korea and Japan and presently comprises 32 species (Frost, 2013). Molecular studies have shown a high cryptic diversity among Hynobius populations in Japan and Korea (Baek et al., 2011; Zheng et al. 2012) which will lead to the description of several new species. Hynobius species are hard to distinguish on the basis of morphological features alone. In the following species accounts most of the described external features are only evident in aquatic adults during the breeding season.

Hynobius abei Sato, 1934 Hynobius amjiensis Gu, 1992 Hynobius arisanensis Maki, 1922 Hynobius boulengeri (Thompson, 1912) Hynobius chinensis Günther, 1889 Hynobius dunni Tago, 1931

Hynobius formosanus Maki, 1922 Hynobius fuca Lai & Lue, 2008 Hynobius glacialis Lai & Lue, 2008 Hynobius guabangshanensis Shen, 2004 Hynobius hidamontanus Matsui, 1987 Hynobius hirosei Lantz, 1931 Hynobius katoi Matsui, Kokuryo, Misawa & Nishikawa, 2004 Hynobius kimurae Dunn, 1923 Hynobius leechii Boulenger, 1887 Hynobius lichenatus Boulenger, 1883 Hynobius maoershanensis Zhou, Jiang & Jiang, 2006 Hynobius naevius (Temminck & Schlegel, 1838) Hynobius nebulosus (Temminck & Schlegel, 1838) Hynobius nigrescens Stejneger, 1907 Hynobius okiensis Sato, 1940 Hynobius quelpaertensis Mori, 1928 Hynobius retardatus Dunn, 1923 Hynobius sonani (Maki, 1922) Hynobius stejnegeri Dunn, 1923 Hynobius takedai Matsui & Miyazaki, 1984 Hynobius tokyoensis Tago, 1931 Hynobius tsuensis Abé, 1922 Hynobius turkestanicus Nikolskii, 1910 Hynobius yangi Kim, Min & Matsui, 2003 Hynobius yatsui Oyama, 1947 Hynobius yiwuensis Cai, 1985

References

Baek et al. (2011); Frost (2013); Zhao & Hu (1988b);

Zheng et al. (2012)

Hynobius abei Sato, 1934 | Abe’s Salamander Description

A small, stout salamander. Trunk stocky, with 11-13 costal grooves. Tail shorter than snout-vent length, thick at the base and flattened laterally towards the tip. Vomerine teeth in U-shape (Thorn, 1969). Four fingers and five toes. Limbs relatively short; when laid against the body there is a space of 0.5-3 costal grooves between toes and finger tips.

In males the tail is strongly compressed and very high in the breeding season. Males in the breeding season have a broad triangular head, due to swelling of the jowls (Goris & Maeda, 2005). Upperparts reddish-brown or dark brown with small pale spots on sides and limbs.

Total length approx. 9-11.5 cm (Thorn, 1969).

Diagnosis

A stocky, dark brown salamander with 11-13 costal grooves; similar to Hynobius nebulosus but with a higher and more compressed tail.

Eggs and larvae

The female produces a pair of coiled egg sacs, showing clear longitudinal striations, and containing a total of 26-109 eggs. Matsui & Miyazaki (1984) report a mean clutch size of 71 eggs. Egg sacs are laid hidden beneath the layer of leaves at the bottom of the breeding ponds. Larvae develop slowly underneath the fallen snow, growing faster after the snow melts. Metamorphosis is from June-July to August, some individuals overwintering as larvae (Goris & Maeda, 2005). 51

Hynobius abei. Photo: Hans-Joachim Herrmann. evergreen and deciduous forest and bamboo forest. It breeds in pools, ditches and springs (Stuart et al., 2008). Breeding pools are always situated in shaded places in the forest, where the combination of shade and water seepage maintains a fairly stable year-round temperature, never exceeding 20°C in the summer and never freezing in winter (Goris & Maeda, 2005).

Behaviour

Food consists of snails, spiders and earthworms, probably also insects (Goris & Maeda, 2005). Reproduction starts in November and December, the season of snowfall in its habitat (Goris & Maeda, 2005).

Threats and conservation

The range of Hynobius abei.

Distribution

The species is only known from several disjunct localities on the Tango Peninsula of Kyoto, the Tajima region of Hyogo, and the northern part of Fukui Prefectures, Japan (Environment Agency of Japan, 2000).

Habitat 52

This species inhabits secondary broad-leaved

Salamanders of the Old World | Hynobius

All local populations are small in size and their habitats are becoming seriously degraded (Environment Agency of Japan, 2000). The species is rare and considered highly susceptible to habitat disturbance. It is locally protected and listed as Critically Endangered (Stuart et al., 2008; IUCN, 2013).

Comments

Hynobius abei is sister to a clade containing H. lichenatus, H. tokyoensis, H. takedai and H. nigrescens (Weisrock et al., 2013).

References

Environment Agency of Japan (2000); Goris & Maeda (2005); IUCN (2013); Matsui & Miyazaki (1984); Stuart et al. (2008); Thorn (1969); Weisrock et al. (2013)

Hynobius amjiensis Gu, 1992 | Zhejiang Salamander

Hynobius amjiensis, Longwangshan Mt, Anji County (type locality), Zhejiang. Photo: Hou Mian, courtesy Zeng Xiaomao.

Description

This description is based on the original by Gu (1992) with additional information from Fei et al. (2006). Trunk stocky and somewhat flattened; 13 costal grooves. Head oval and slightly flattened. Head a little longer than wide, snout obtuse and rounded. Distance between nostrils less than or equal to distance between eyes. Eye diameter less than distance between eyes, pupil round. No labial fold. Vomerine teeth in V-shaped pattern. Tongue oval, adhering to bottom of oral cavity. Tail long, a little shorter than snout-vent length. Tail-base almost round, flattened laterally towards the tip. Low dorsal tail-fin, tail-tip obtuse and rounded. Limbs slender, forelimbs shorter and weaker than hindlimbs. Fingers and toes overlap when laid against the body. Skin smooth, central groove running along the dorsum. Colour dusty grey or sepia above, dark grey-brown below. Cloaca of the male is a longitudinal groove with an anterior papilla. Total length 153-166 mm in males, 166 mm in females.

Diagnosis

A stocky salamander, usually with 13 costal grooves. The body of Hynobius amjiensis is rather large compared

The range of Hynobius amjiensis.

with H. chinensis and H. yiwuensis.. Tail length about 92% of snout-vent length (Fei et al., 2006).

Eggs and larvae

The female lays a pair of egg sacs, white and translucent, in spiral form comprising three revolutions. They are attached to aquatic plants, fallen leaves, branches and 53

stones. Length 46-58 mm. A single egg sac contains 43-77 eggs and a female may lay 96-151 eggs in total. Egg diameter 3.5 mm (Fei et al., 2006). Young salamanders reach sexual maturity after three years (Stuart et al., 2008).

Distribution

This species is only known from the type locality, Mt. Longwang Nature Reserve, Anji County, Zhejiang Province, China (Fei et al., 2006; IUCN, 2013).

Habitat

This salamander occurs in a marshy area, covered with sphagnum mosses at 1,300 m altitude. It breeds in a small number of small standing water ponds, surrounded by mosses, grasses, pine and deciduous woods and shrubs. Hynobius amjiensis is terrestrial outside the breeding season and difficult to find. The only known population is believed to comprise 250-300 breeding females (Gu et al., 1999; Stuart et al., 2008).

Behaviour

Hynobius amjiensis feeds on small aquatic invertebrates and earthworms (Gu, 1992). When food is scarce, cannibalism occurs (Fu et al., 2003a). The breeding season is fairly long, extending from mid-November to late May, with a peak period in February. Eggs have been found under ice in December. After reproduction the females leave the water at once, while the males stay on for a while (Fei et al., 2006).

Threats and conservation

The very small range and very small number of breeding sites make this species especially susceptible to habitat alteration. The growing threat of human disturbance at the site, especially from touristic activities, poses increasing risks. The species is considered to be Critically Endangered (Zhao, 1998; Stuart et al., 2008; IUCN, 2013).

Observations in captivity

No reports available.

Comments

Most authors assume that Hynobius amjiensis (with one locality in Zhejiang) and H. yiwuensis (with a wider range in Zhejiang and Fujian Provinces) are separate species and differ from H. chinensis from Hubei. They show considerable genetic divergence and are geographically isolated from all other hynobiid salamanders (Fu et al., 2003b). Hynobius amjiensis is sister to a clade containing H. chinensis, H. guabangshanensis and H. maoershanensis (Xia et al., 2012; Weisrock et al., 2013). In the study of Zheng et al. (2012) H. amjiensis is the sister taxon to Y. yiwuensis.

References

Fei et al. (2006); Fu et al. (2003a, 2003b); Gu et al. (1999);

Gu (1992); IUCN (2013); Stuart et al. (2008); Weisrock et al. (2013); Xia et al. (2012); Zhao (1998); Zheng et al. (2012).

Hynobius arisanensis Maki, 1922 | Alishan Salamander Description

A relatively small salamander. Tail shorter than snout-vent length. Head round, flattened; nostril nearer tip of snout than eye; eyelid almost equal to interorbital space; 11-13 costal grooves. Vomerine tooth row equals 6/7 width of tongue; inner rows well separated. Fifth toe rudimentary, tubercle-like (Maki, 1922; Dunn, 1923). Gular fold present. Large, round black eyes. Paratoids large and flat. Tail cylindrical, slightly compressed toward the tip, which is blunt. Limbs rather short, foreand hindlimbs do not usually touch when laid against the body; in some specimens they overlap (Lai & Lue, 2008). Skin smooth. Colour dark brown, with small yellowish-brown spots, somewhat cream coloured on belly (Maki, 1922; Dunn, 1923). Total length 10-12 cm (Lai & Lue, 2008).

Diagnosis

Short cylindrical tail compressed towards the tip. V-shaped vomerine teeth. When adpressed fore- and hindlimbs do not touch. Five toes, but fifth toe often poorly developed into a protuberance. Uniformly dark brown. Besides genetic characteristics, distribution and colour pattern differences distinguish this species from Hynobius sonani (Lai & Lue, 2008).

54

Salamanders of the Old World | Hynobius

Hynobius arisanensis, Taiwan. Photo: Yang In Shuen.

Eggs and larvae

Egg sacs are attached to stones or twigs in the water. Each egg sac contains only 4-8 eggs. Larvae hatch after two months and reportedly feed on algae and decomposed

plant residue (refs in Hou et al., 2010). Metamorphosis takes place one month later, when snout-vent length is about 14.5 mm (Hou et al., 2011). Metamorphosed juveniles have been found in March (Chen & Lue, 1986a), suggesting a reproductive pattern similar to that of the other Taiwanese Hynobius species.

Distribution

Hynobius arisanensis has a distinct distribution compared with the four other Taiwanese Hynobius species. It occurs in Yushan, Alishan, and the southern Central Mountain Ranges at elevations from 1,800-3,600 m (Lee et al., 2006; Lai & Lue, 2008; Chang, 2010).

predators (see refs in Lee et al., 2006 and Hou et al., 2010). They congregate near creeks during the dry season, from November-April, and disperse in the wet season from MayOctober, generally not venturing more than 5 m from the water. The home range is small (Chen & Lue, 1986a). The breeding season is probably in late winter-early spring. Hou et al. (2010) report a form of parental care in this species, where both sexes guard the eggs and larvae. There is no further information on the breeding behaviour of H. arisanensis.

Threats and conservation

This species is very locally distributed and populations are small. Like the other Taiwanese Hynobius species, is it hence vulnerable to habitat destruction and degradation, due to the development of tourist infrastructure. Hynobius arisanensis is protected within Yushan National Park and Tawushan Nature Preserve, and listed as Vulnerable (Stuart et al., 2008; IUCN, 2013). Currently, all five Taiwanese salamander species are protected by the Wildlife Conservation Law. The effect of concrete constructions on habitat and mobility of salamanders is being monitored (Hou et al., 2010).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

The range of Hynobius arisanensis.

Habitat

Like the other Taiwanese Hynobius species, H. arisanensis occurs in high-elevation montane areas, in woodlands, and broadleaf and coniferous forests, and the transition zone between coniferous forests and alpine bamboo grasslands (Lai & Lue, 2008). These are areas with low temperatures, high annual precipitation, little disturbance, and high humidity. The animals spend most of their lives under logs and rocks near small, cool creeks and seepage areas with a moist substrate. Microhabitat studies indicate that H. arisanensis prefers moist soils under decaying logs on slopes with small creeks and water seepages (Lai, 2009; Lai & Lue, 2013).

Hynobiid salamanders reach the southern boundary of their distribution in Taiwan. The Taiwanese species of Hynobius are endemic to the island and their population sizes are extremely small (Lue et al., 1989). Five species are currently recognised, and are genetically and morphologically distinct (Hynobius sonani, H. formosanus, H. arisanensis, H. fuca and H. glacialis). Hynobius arisanensis is very similar to H. sonani in morphometric and genetic data (Lai & Lue, 2008). Karyology also shows the resemblance between these two species (Iizuka & Kakegawa, 1989). The Taiwanese Hynobius lineage is basal to the other Chinese and Korean Hynobius species as well as to most of the Japanese Hynobius species, except H. kimurae, H. hirosei and H. retardatus (Xia et al., 2012; Zheng et al. 2012; Weisrock et al., 2013).

References

Chang (2010); Chen & Lue (1986a); Dunn (1923); Hou

et al. (2010); Iizuka & Kakegawa (1989); IUCN (2013); Lai (2009); Lai & Lue (2008, 2013); Lee et al. (2006); Lue et al. (1989); Maki (1922); Stuart et al. (2008); Weisrock et al. (2013); Xia et al. (2012); Zheng et al. (2012).

Behaviour

Adult salamanders usually search actively for food at night under debris on the forest floor and prey mainly on sow bugs, earthworms, and other terrestrial invertebrates. Their natural enemies are snakes, pheasants and other 55

Hynobius boulengeri (Thompson, 1912) | Odaigahara Salamander Description

The largest Japanese Hynobius species. Large, flattened head, as long as, or a little longer than wide. Snout rounded; eyes large. Distinct paratoid glands. Gular fold present. Robust and cylindrical body with 13 costal grooves and a clear vertebral depression. Tail a little longer than trunk, flattened laterally; keel absent except near the tail-tip which is rounded. Limbs relatively long and robust. When adpressed fingers and toes barely meet. Four fingers, five toes. Skin smooth.

Male cloaca in the form of an arrow pointing forward, female cloaca is a simple longitudinal fold. Upperparts a uniform brown-black or slate, underparts a little lighter. Juveniles have small grey or bluish dots on upperparts. Total length 11-20 cm. Salamanders from Honshu are larger than those from Amakusa Islands and Osumi Peninsula (Nishikawa et al., 2007). Those from Osumi Peninsula are especially small (Sato, 2003) and form a separate taxon for which a description is pending (see under distribution and comments).

Diagnosis

A large salamander (especially the Honshu specimens), uniformly brown-black or slate coloured.

Eggs and larvae

As in Hynobius hirosei, the egg sacs are light blue in colour, banana-shaped – not coiled, and have a distinct whip-like structure on the free end. Egg sacs from animals from Honshu are 15-25 cm long and 13-26 mm diameter. Clutch size averages between 32-55 (Nishikawa et al., 2008). Eggs are yellowish in colour, animal pole more brownish.

Hynobius boulengeri, Nara Pref. Photo: Kanto Nishikawa.

Larvae hatch at 23-26 mm length, without balancers. At metamorphosis they measure 50-65 mm. Dorso-caudal fin reaches middle of the back. Gills well-developed (Thorn, 1969). Larvae often have black claw-like structures on the tips of their fingers (Nishikawa et al., 2008). There is marked variation in larval development and time of metamorphosis. Larvae may overwinter and reach metamorphosis one or even three years later (Nishikawa & Matsui, 2008; Nishikawa et al., 2008). After metamorphosis juveniles live for a year or two on the slopes of their natal stream, in rock piles or under logs and forest litter (Goris & Maeda, 2005).

Distribution

Hynobius boulengeri occurs in southwestern Honshu on the Kii Peninsula (the type locality is the Odaigahara Mountain in Nara Prefecture). The animals from Kyushu (Sobo-Katamuki Mountains, Amakusa Islands and Osumi Peninsula) form a distinct lineage, thus far unnamed. Their range is disjunct; the species occurs parapatrically with H. stejnegeri which inhabits the Central Kyushu Mountains. The salamander occurring on Shikoku, previously described as a separate species (Lantz, 1931) or a subspecies of H. boulengeri (Sato, 1934), has been returned to full species rank as H. hirosei (Nishikawa et al., 2001, 2003, 2005, 2007).

The range of Hynobius boulengeri. 56

Salamanders of the Old World | Hynobius

The map does not reflect the occurrence of salamanders on the Amakusa Islands and Osumi Peninsula in the southern part of Kyushu (IUCN, 2013).

Habitat

Hynobius boulengeri inhabits deciduous broadleaved, coniferous, or mixed mountain forests, where the species occurs on the slopes, or the bottom of small valleys. Adult salamanders can be found under logs and forest litter, but large numbers remain in the stream for many months after breeding, even overwintering there. Others overwinter under rocks and logs, but some can be seen moving on the forest floor on rainy days in December and January (Goris & Maeda, 2005).

Behaviour

Hynobius boulengeri preys on spiders, insects and large earthworms. Breeding takes place from February to the end of May in medium-sized mountain streams, especially near the headwaters (Goris & Maeda, 2005).

Threats and conservation

The habitat of the Honshu population has deteriorated due to the construction of mountain roads and utilisation for tourism. The Kyushu population is very susceptible to habitat destruction due to its small range, and is considered Vulnerable (Environment Agency of Japan, 2000; Stuart et al., 2008; IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Hynobius boulengeri is the name used for the group of salamanders occurring in the mountainous regions of southern Honshu, Shikoku, and Kyushu. Recent observations show that H. boulengeri from Kyushu comprises three discrete populations from the Sobo-Katamuki Mountains, the Amakusa Islands and the Osumi Peninsula, and that these are genetically closest to H. stejnegeri from the Kyushu Central Mountains. It has been suggested that H. boulengeri sensu stricto should be applied to salamanders from Honshu, the available name H. hirosei to the animals from Shikoku, and that the animals from Kyushu, as long as their formal description is pending, should be retained in H. boulengeri sensu lato (Nishikawa et al., 2007, 2008). Hynobius boulengeri is sister to H. naevius (Weisrock et al., 2013).

References

Environment Agency of Japan (2000); Goris & Maeda

(2005); IUCN (2013); Lantz (1931); Nishikawa & Matsui (2008); Nishikawa et al. (2001, 2003, 2005, 2007, 2008); Sato (1934, 2003); Stuart et al. (2008); Thorn (1969); Weisrock et al. (2013).

Hynobius chinensis Günther, 1889 | Chinese Hynobiid Salamander Description

This description summarises that of the two type specimens by Adler & Zhao (1990). Head large; longer than its width. Tip of snout rounded. Eyes dorsolateral in position, slightly protruding. Diameter of eye shorter than the distance from its anterior corner to the tip of snout; pupil rounded. Nostril between eye and tip of snout, and slightly closer to the latter. Distance between nostrils slightly larger or equal to the distance between eyes. A V-shaped bulge on top of head. No labial fold, gular fold indistinct. Series of vomerine teeth U-shaped. Body short and stout. Limbs well-developed and tips of digits meet when limbs adpressed. 11-12 costal grooves, very prominent and meeting on ventral midline. Four fingers, five toes. Digits flattened, free; without palmar and tarsal tubercles; no cornified covering on palms, tarsus, fingers and toes. Tail length shorter than snout-vent length; tail compressed, but cylindrical at the base and pointed at the end, without crest on ventral edge and only slightly so on its dorsal side. Skin smooth. Colour and size could not be established due to the condition of the specimens. In 2005 specimens were collected from the type locality (Gaojiayan, Yichang, Hubei Province), which largely conformed to the description by Adler & Zhao (1990) except for the shape of the vomerine tooth rows. 12 costal grooves. Colour was not reported, but apparently conforming to the

Hynobius chinensis, male, Gaojiayan, Yichang Pref. (type locality), Hubei. Photo: Hou Mian, courtesy Zeng Xiaomao.

Hynobius chinensis, female, Gaojiayan, Yichang Pref. (type locality), Hubei. Photo: Hou Mian, courtesy Zeng Xiaomao. 57

original description of Günther (1889): uniformly black on upperparts, brownish with dark spots on underside (Wang et al., 2007). Total length was 165-205 mm, tail length a little shorter than snout-vent length.

Diagnosis

A stocky salamander with 11 or 12 costal grooves.

Eggs and larvae

Available descriptions of eggs and larvae relate to specimens from Fujian and Zhejiang, which are now referred to Hynobius yiwuensis (Pope, 1931; Chang, 1936; Zhang & Tang, 1987).

Distribution

The species that was described by Günther in 1889 as Hynobius chinensis was collected in Yichang, Hubei Province (see discussion in Adler & Zhao, 1990). Until it was rediscovered in 2005, no salamanders had been reported from that area (Wang et al., 2007). There is a large gap between the distribution of H. chinensis in Hubei Province and that of the other Hynobius taxa in Zhejiang and Fujian (Fu et al., 2003b). The map indicates its distribution in Gaojiayan, Yichang, Hubei Province, withholding judgement on a possible occurrence in Fujian until more information becomes available. The southeastern population from Fujian Province, currently allocated to H. chinensis, might represent a new species. The Zhejiang records are taken to refer to H. yiwuensis and are not included in the map.

Hynobius chinensis, Gaojiayan, Yichang Pref. (type locality), Hubei. Photo: Hou Mian, courtesy Zeng Xiaomao.

Habitat

This species occurs in forests and arable fields in hilly areas, at altitudes up to 1,400 m. It breeds in pools and small streams (Stuart et al., 2008; IUCN, 2013).

Behaviour

Animals were collected in September and December, suggesting that reproduction takes place during the winter months (Wang et al., 2007).

Threats and conservation

Major threats are habitat destruction and degradation, in particular due to infrastructure development for human settlement. The species is considered to be Endangered (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Most authors assume that Hynobius amjiensis (with one locality in Zhejiang) and H. yiwuensis (with a wider range in Zhejiang and Fujian Provinces) are separate species and differ from H. chinensis from Hubei. They show considerable genetic divergence and are geographically isolated from all other hynobiid salamanders (Fu et al., 2003b), including H. chinensis. According to Weisrock et al. (2013) H. chinensis and H. yiwuensis (referred to as H. chinensis 1, from Zhoushan Island) are sister species, and H. amjiensis is their closest relative. According to the arrangement proposed by Zheng et al. (2012), H. yiwuensis is the sister taxon to H. amjiensis, and this clade is sister to a clade containing the other three mainland Chinese Hynobius species.

References

Adler & Zhao (1990); Chang (1936); Fu et al. (2003b);

Günther (1889); IUCN (2013); Pope (1931); Stuart et al. (2008); Wang et al.

The range of Hynobius chinensis. 58

Salamanders of the Old World | Hynobius

(2007); Weisrock et al. (2013); Zhang & Tang (1987); Zheng et al. (2012).

Hynobius dunni Tago, 1931 | Oita Salamander Description

The following description follows that of Thorn (1969). Head longer than wide, rectangular when viewed from above and snout short and rounded. Gular fold present. Body with 12 costal grooves. Tail shorter than snout-vent length, thick at the base, more flattened towards the tip. Limbs well-developed. Fingers and toes overlap when limbs are adpressed. Four fingers and five long toes. Skin smooth and shiny. Upperparts dark greenish-brown, due to a fine yellowish to greenish speckling on a dark background. Underparts more or less bluish-grey on the belly and lighter on the throat. Underside of tail same colour as upperparts of the body. Females are a little smaller than males, which look heavier. During the breeding season males have an Y-shaped cloaca, while females have a simple longitudinal fold. Head width, tail height and hind legs are enlarged in the male. These characteristics apply to Hynobius species in general. It is difficult to distinguish the sexes after the breeding season, when differences in cloacal fold and tail height are less clear.

Hynobius dunni, male. Photo: Henk Wallays

Total length 12-13 cm (Thorn, 1969), maximum total length of captive animals 16 cm (Wallays, 2002).

Diagnosis

Similar to Hynobius nebulosus but larger in size and longer limbs; toes and fingers overlapping when limbs are adpressed. Vomero-palatine teeth series in U shape. No yellow edges to the tail.

Eggs and larvae

The female produces a pair of egg sacs 15-30 cm long and 2.5-3 cm diameter, each containing 18-101 eggs of 2 mm diameter. Hatchlings measure 13 mm; balancers present; low dorso-caudal fin (Thorn, 1969). Depending on temperature larvae may hatch after some five weeks or later, measuring 14-17 mm. At metamorphosis the larvae have a length of 50-57 mm, or exceptionally 75 mm. Captive animals may reach sexual maturity within three years (Wallays, 2002).

Hynobius dunni, male. Photo: Henk Wallays.

Distribution

This species is restricted to Kyushu – around the cities of Oita, Kumamoto, Miyazaki – and Shikoku – around the city of Kochi (Stuart et al., 2008; IUCN, 2013).

Habitat

This species occurs in paddy fields, secondary forest and bamboo stands in hilly areas. It breeds in pools, ponds and paddy fields at forest edges, ditches and brooks (Stuart et al., 2008).

Hynobius dunni, larva. Photo: Henk Wallays. 59

males was rarely seen. Females enter the water later, approach a male positioned on a branch, and attach the egg sacs to the branch, where they are fertilised by the alerted male or males.

Threats and conservation

The major threat to this species is habitat loss, due in particular to infrastructure development for human settlement. It is also threatened by water pollution and often appears in the pet trade. The species enjoys some local protection (Stuart et al., 2008). It is considered Vulnerable (Environment Agency of Japan, 2000) and Endangered (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

The range of Hynobius dunni.

Behaviour

Behaviour has been studied in captive animals by Wallays (2002), on whose observations the following summary description is based. The breeding season starts in December and may last till the end of April, with a peak in February. Animals are active in water during spring and autumn when temperatures range from 14-16°C. In spring, males enter the water first and assemble near suitable egg laying places, such as branches. They climb up the branches, make waving movements with their tails, and rub their cloacas against certain spots on the branch, possibly marking an individual territory. Aggression among

This species has been bred in captivity over many years from 1998 onwards (Thorn & Raffaëlli, 2001; Raffaëlli, 2007; Wallays, 2002; Pasmans et al., in press). The animals were given a large aquarium furnished with sand, stones and moss, with a humidity gradient. The water part contained branches for egg deposition. Animals were hibernated under temperatures close to 0°C and reproduced at temperatures between 5-16°C. Larvae reached metamorphosis after three months. Adults were fed earth worms and all sorts of insects and their larvae. In captivity animals may reach sexual maturity after three years. It is likely that all the specimens of Hynobius dunni currently held in captivity in Europe originate from the breeding stock of Henk Wallays.

Comments

Hynobius dunni is sister to H. nebulosus (Weisrock et al., 2013).

References

Environment Agency of Japan (2000); IUCN (2013);

Pasmans et al. (in press); Raffaëlli (2007); Stuart et al. (2008); Thorn (1969); Thorn & Raffaëlli (2001); Wallays (2002); Weisrock et al. (2013).

Hynobius formosanus Maki, 1922 | Taiwan Salamander Description

A small salamander. Tail shorter than snoutvent length. Head round, flattened; nostril nearer tip of snout than eye; distance between nostrils greater than between eyelids; eyelid equal to interorbital space; 12 costal grooves. Vomerine tooth row equals 3/4 width of tongue; inner rows close together. Fifth toe smaller than first (Maki, 1922; Dunn, 1923).

irregular, sometimes dense brown spots and patches over body and tail; small dark spots on belly (Fei et al., 2006). Tail is longer in males than in females and more males than females appear to have 11 rather than 12 costal grooves (Lai & Lue, 2008). Total length 9-10 cm (Lai & Lue, 2008).

Gular fold present. Large, round, black eyes. Paratoids large and flat. Tail cylindrical, slightly compressed toward the tip, which is blunt. Limbs rather short, fore- and hindlimbs do not touch when adpressed. Skin smooth. Colour variable, tawny yellow background, mottled with 60

Salamanders of the Old World | Hynobius

Diagnosis

Smaller than other Taiwanese species, except Hynobius fuca. Short cylindrical tail compressed towards the tip. V-shaped vomerine teeth. When adpressed fore- and hindlimbs do not touch. Five toes.

Hynobius formosanus, Taiwan. Photo: You Chung Wei.

Eggs and larvae

The female produces a pair of string-like egg sacs, containing some 14-15 large eggs (4.25 mm diameter). Egg sacs are laid in small slow-moving bodies of water (Lee et al., 2006), where they are attached under stones (Kakegawa et al., 1989). The egg sac is transparent and the outer envelope is not tough as in Hynobius sonani. It has many irregular horizontal grooves and lighter longitudinal stripes than in H. sonani. Colour not uniform, but generally pale yellowish with a brown tint, the brown fading as the embryos develop. Larvae hatch some three months after oviposition at a total length of 19-21 mm, at water temperatures of 7-9°C. They retain a large amount of yolk and have no balancers. Larvae are reported to take almost no food. Metamorphosis takes place about two months after hatching at a length of 25 mm (Kakegawa et al., 1989).

lands, broadleaf and coniferous forests, and the transition zone between coniferous forests and alpine bamboo grasslands (Lai & Lue, 2008). These are areas typified by low temperatures, high annual precipitation, low levels of disturbance and high humidity. The animals spend most of their lives under logs and rocks near small, cool creeks and seepage areas with moist substrate.

Distribution

Hynobius formosanus occurs from the Central Mountain Range to the northern Central Mountains and the Syueshan Mountain ranges of Taiwan, at elevations from 2,3002,900 m. It is partly sympatric with H. sonani (between Mt. Hohuan and Mt. Bilu). Hynobius formosanus and H. glacialis are parapatric, with the former occurring at lower elevations and the latter at greater hights (Lai & Lue, 2008; Chang, 2010).

Habitat

Like the other Taiwanese Hynobius species, H. formosanus occurs in high-elevation montane areas, in wood-

The range of Hynobius formosanus. 61

Behaviour

Adult salamanders usually search actively for food at night under debris on the forest floor, and prey mainly on sow bugs, earthworms, and other terrestrial invertebrates. Their natural enemies are snakes and other predators (Yeh et al., 1988; further refs in Lee et al., 2006). The breeding season ranges from November-January, when the amount of rainfall is small (Kakegawa et al., 1989). Eggs are laid in headwater streams and underground seepages. Male and female adults and freshly laid egg sacs were found in February, under stones in a small water reservoir along a mountain path, water temperature 1°C. Some adults showed bite wounds, probably the result of agonistic encounters (2008, pers. obs.). There is no further information on breeding behaviour.

Threats and conservation

Distribution is very local and populations are small, making this species, like the other Taiwanese Hynobius species, vulnerable to habitat destruction and degradation due to development of infrastructure for tourism (Chen & Lue, 1986a, 1986b). Hynobius sonani and H. formosanus were first protected in 1986 under the Cultural Heritage Preservation Law as precious and rare species, and later by the Wildlife Conservation Law (1989) (Lee et al., 2006). Hynobius formosanus is considered Critically Endangered by Zhao (1998) and listed as Endangered by Stuart et al. (2008) and IUCN (2013).

Observations in captivity

The species has been kept in the laboratory for short periods, where oviposition was induced (Kakegawa et al., 1989), but further documentation regarding captive Hynobius formosanus is lacking.

Comments

Hynobiid salamanders reach the southern boundary of their distribution in Taiwan. The Taiwanese species of Hynobius are endemic to the island and their populations are extremely small in size (Lue et al., 1989). Presently, five Taiwanese species are recognised, which are distinguished genetically and morphologically (Hynobius sonani, H. formosanus, H. arisanensis, H. fuca and H. glacialis). Morphological differences are however subtle and based on a combination of morphometric data, tooth count and colouration (Lai & Lue, 2008). Hynobius formosanus clusters with other Taiwanese Hynobius species in a clade that is sister to all other Hynobius species, except H. retardatus, H. hirosei and H. kimurae (Xia et al., 2012; Zheng et al., 2012; Weisrock et al., 2013).

References

Chang (2010); Chen & Lue (1986a, 1986b); Dunn (1923);

Fei et al. (2006); IUCN (2013); Kakegawa et al. (1989); Lai & Lue (2008); Lee et al. (2006); Lue et al. (1989); Maki (1922); Stuart et al. (2008); Weisrock et al. (2013); Xia et al. (2012); Yeh et al. (1988); Zhao (1998); Zheng et al. (2012).

Hynobius fuca Lai & Lue, 2008 | Taiwan Lesser Salamander Description

The following is summarised from the original description by Lai & Lue (2008). Small-sized species. Head, body and tail are cylindrical, with neck inconspicuous. Head relatively narrow. Interorbital distance is larger than internarial distance. Vomerine teeth are V-shaped. Trunk robust and short. 11-12, normally 11, costal grooves. Tail short and thick, laterally flattened at the tip. Tail shorter than snout-vent length. Limbs are short relative to trunk, with two costal grooves between adpressed limbs. Four hindlimb toes. Dorsal side is blackish-brown in colour, fading toward ventral side. Flank and ventral sides brown. Body marked with white speckles or small blotches. Markings around eyes. Individuals differ in colour only in the amount of white speckles. Total length 7-9 cm.

Diagnosis

A short, robust salamander with short tail. Limbs short, four fingers and four toes. Body blackish-brown with white speckles. Among Taiwanese species, Hynobius fuca is similar to H. formosanus in size, brownish dorsal colour, toe

62

Salamanders of the Old World | Hynobius

number, short limbs and tail, but H. formosanus has yellowishbrown blotches on dorsum while H. fuca has none.

Eggs and larvae

Eggs and larvae have not been described.

Distribution

Hynobius fuca is known from only four locations in the central and northern part of the Syueshan Mountain Range. Altitudinal distribution 1,300-1,720 m above sea level, the lowest among the Taiwanese species (Chang, 2010).

Habitat

Like the other Taiwanese Hynobius species, Hynobius fuca occurs in montane areas with low temperatures, high annual precipitation, low levels of disturbance and high humidity. This species lives on densely shaded, moist forest floors in redwood and mixed coniferous forest, and is found along mountain creeks or under rocks or rotting wood. Its populations appear to be small in size.

Behaviour

There is no information on breeding behaviour. The animals probably reproduce in creeks during the dry season, from November-April.

Hynobius fuca, Taiwan. Photo: Yang In Shuen.

Threats and conservation

Distribution is very local and populations are small, making this species, like the other Taiwanese Hynobius species, vulnerable to habitat destruction and degradation.

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Hynobiid salamanders reach the southern boundary of their distribution in Taiwan. The Taiwanese species of Hynobius are endemic to the island and their population sizes are extremely small (Lue et al., 1989). Presently five

The range of Hynobius fuca.

Taiwanese species are recognised, which are distinguished genetically and morphologically (Hynobius sonani, H. formosanus, H. arisanensis, H. fuca and H. glacialis). Hynobius fuca is the smallest, darkest and most robust of the Taiwanese species and occurs at the lowest elevation. The authors intend to correct the name to Hynobius fucus (pers. comm.).

References

Chang (2010); Lai & Lue (2008); Lue et al. (1989).

Hynobius glacialis Lai & Lue, 2008 | Nanhu Salamander Description

The following is summarised from the original description by Lai & Lue (2008). A medium-sized salamander, the largest among the five Taiwanese species of Hynobius. Head, body and tail are cylindrical, with neck inconspicuous. Interorbital distance is larger than internarial distance. Vomerine teeth are U-shaped. Trunk slimy and long. 12 costal grooves. Tail is long, slender, and flatter laterally near the tip, and a little shorter than snout-vent length. Limbs are long and robust. Tips of fore- and hindlimb digits touch when adpressed. Fifth toe of hindlimb varies from well-developed to rudimentary and is entirely missing in some individuals. Colour of dorsal side is yellowish-brown with deep, black, irregular short stripes, evenly distributed. Ventral side grey, with pale yellow spots on head and pale yellow blotches near flank.

Total length 10-12 cm.

Diagnosis

Largest among the Taiwanese species. Distinctive colouration, with short black stripes on yellowbrown background. Tail relatively long. Limbs relatively long, with fingers and toes touching when adpressed. Five toes. Similar to Hynobius sonani in morphology, but has a relatively narrower head and shorter hindlimbs.

Eggs and larvae

Eggs and larvae have not been described.

Distribution

Hynobius glacialis occurs in the northern Central and Syueshan Mountain Ranges of Taiwan at elevations between 3,200-3,400 m. It is parapatric with H. formosanus, but H. glacialis extends to higher elevations (Chang, 2010). 63

Hynobius glacialis, Taiwan. Photo: You Chung Wei. alpine tundra, usually beside creeks, cold springs, and seepages. During the day, animals normally shelter under rocks on gravel substrates.

Behaviour

There is no information on breeding behaviour of this species. The animals probably reproduce in creeks during the dry season, from November-April.

Threats and conservation

Distribution is very local and populations are small in size, making this species, like the other Taiwanese Hynobius species, vulnerable to habitat destruction and degradation.

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

The range of Hynobius glacialis.

Habitat

Like the other Taiwanese Hynobius species, Hynobius glacialis occurs in high-elevation montane areas with low temperatures, high annual precipitation, low levels of disturbance and high humidity. Hynobius glacialis lives near

64

Salamanders of the Old World | Hynobius

Hynobiid salamanders reach the southern boundary of their distribution in Taiwan. The Taiwanese species of Hynobius are endemic to the island and their populations are extremely small in size (Lue et al., 1989). Presently five Taiwanese species are recognised, which are distinguished genetically and morphologically (Hynobius sonani, H. formosanus, H. arisanensis, H. fuca and H. glacialis). Hynobius glacialis is a relatively slender species, a little longer on average than the other Taiwanese species and occurs at the highest elevations.

References

Chang (2010); Lai & Lue (2008); Lue et al. (1989).

Hynobius guabangshanensis, Guangbangshan forest farm, Qiyang County (type locality), Hunan. Photo: Hou Mian, courtesy Zeng Xiaomao.

Hynobius guabangshanensis Shen, 2004 | Guabang Shan Salamander Description

This is based on the original description by Shen et al. (2004). The species is very similar to Hynobius amjiensis: it is a large-sized salamander with 13 costal grooves, long legs and tips of fingers and toes meeting when adpressed. It differs in the following characters: size smaller than H. amjiensis; vomerine teeth thinner and arranged more closely together; tail length shorter, about 70% of snout-vent length. Total length 125-151 mm.

Diagnosis

A stocky salamander usually with 13 costal grooves. It is slightly smaller than Hynobius amjiensis and its vomerine teeth are arranged more closely together. Tail length shorter than snout-vent length. Gape wider than in other Chinese Hynobius species, the corner of the mouth extending behind the posterior corner of the eye.

Eggs and larvae

The female lays a pair of white, translucent, banana-shaped egg sacs. The egg sacs are attached to aquatic plants or twigs and by absorbing water grow to about 18 cm long. Each egg sac contains about 90 eggs, with a diameter of 2 mm (Guo et al., 2008). Larvae take 1134 hrs to hatch at water temperatures of 6.5-10°C. Newly hatched larvae have an

The range of Hynobius guabangshanensis. average total length of 16.5 mm (Mi et al., 2007).

Distribution

This species is only known from the type locality, Guabang Shan Tree Farm, Qiyang County, Hunan Province, China (Fei et al., 2009; IUCN, 2013). 65

Habitat

This salamander occurs in forest and wetlands such as bogs, marshes, permanent pools and paddy fields. It has been found at 400-720 m altitude (IUCN, 2013).

Behaviour

Hynobius guabangshanensis breeds in winter in standing ponds, bogs and rice fields. Guo et al. (2008) recorded about 100 breeding females each year, from 2003 to 2006. They described their reproductive behaviour as follows. The male grasps an aquatic plant, arches its body into a C-shape and makes shaking movements every 2-20 seconds. The female attaches a pair of egg sacs to the plant and pulls the egg sacs out of her body with her hind legs. The male then grasps the female and the egg sacs and ejects sperm, with his mouth wide open. Both animals wiggle and bend. The process takes 16-26 minutes. The female then swims away and leaves the pond within 12-48 hours. The male stays with the egg sacs and defends them against other males by making shaking movements, opening his mouth and biting.

Threats and conservation

The main threat is habitat loss and degradation due to smallholder farming. There are insufficient data to determine the species’ status (IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Xia et al. (2012) consider Hynobius guabangshanensis and H. maoershanensis to be sister species. Together with H. amjiensis and H. chinensis they form a clade that is sister to H. yiwuensis. According to Zheng et al. (2012), H. guabangshanensis is sister to a group containing H. chinensis and H. maoershanensis.

References

Fei et al. (2009); Guo et al. (2008); IUCN (2013); Mi et al.

(2007); Shen et al. (2004); Xia et al. (2012); Zheng et al. (2012).

Hynobius hidamontanus Matsui, 1987 | Hakuba Salamander Description

Head moderately depressed, distinctly longer than wide. 12, sometimes 13, costal grooves. Limbs short and stout; when adpressed toes and fingers are separated by at least 0.5 costal grooves. Trunk is longer in female. Head width and head length longer in male. Tail vertically oval at base,

gradually flattening to tip, which is obtusely pointed. Posterior half of tail keeled. Males have a relatively longer and higher tail than females, but no tail-fin. Four fingers and four toes. Vomerine teeth in two small, obliquely arched series, nearly touching at midline, and usually forming a shallow V.

Hynobius hidamontanus, gravid female, Hokujo, Hakuba-mura, Nagano Pref. Photo: Masato Hasumi. 66

Salamanders of the Old World | Hynobius

Sexes differ in the number of teeth, and the length and shape of teeth series (Matsui, 1987). Upperparts dark brown, dotted with small silvery and brassy speckles. Speckles tend to fuse on tail. Sides lighter, with many silvery flecks, except around costal grooves. Silvery flecks more prominent in female than in male. Underside lighter, densely covered with silvery dots. Total length approx. 8-11 cm (Goris & Maeda, 2005).

Diagnosis

Most similar to Hynobius lichenatus in appearance, especially in shallow vomerine tooth series and breeding habits, but differs from it in its electrophoretic allozyme profile, in having un-striated egg sac envelopes, a smaller number of vomerine teeth, a relatively short and high tail, short limbs and a long trunk (Matsui, 1987).

Hynobius hidamontanus, Toyama Pref. Photo: Kanto Nishikawa.

Eggs and larvae

The female produces a pair of un-striated egg sacs, the clutch size varying between 30-76 eggs. Egg diameter on average 2.77 mm (Matsui, 1987). Breeding occurs from late April-early May (Matsui, 1987). Eggs hatch in June and most larvae metamorphose in SeptemberNovember, although some wait until the year following ovipo-

sition. Larvae feed on aquatic insects, crustaceans, tubifex worms, and are also cannibalistic (Goris & Maeda, 2005).

Distribution

This species occurs in Gifu and Toyama Prefectures, and Hakuba village, Nagano Prefecture, in central Japan (IUCN, 2013).

Hynobius hidamontanus, six pairs of egg sacs, Hokujo, Hakuba-mura, Nagano Pref. Photo: Masato Hasumi. 67

Behaviour

Little is known about this species’ natural history. Although generally a lentic-breeder, attaching its eggs to plant roots, twigs and branches, egg sacs have also been found under a large stone in a running stream (Hasumi et al., 2002). A large number of non-breeding adults was recorded from those captured on land near a breeding fen during AprilOctober (Hasumi, 2007).

Threats and conservation

Rapid habitat destruction, drying of wetlands, pollution and capture for the pet trade are the main threats. Populations are small and largely isolated from each other, and therefore very vulnerable (Matsui et al., 2002). The species is considered Endangered and enjoys some local protection (Environment Agency of Japan, 2000; Stuart et al., 2008; IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

The range of Hynobius hidamontanus.

Habitat

This species inhabits wetlands in broad-leaved deciduous forest and larch plantations in montane areas. It breeds in slow-flowing streams (Stuart et al., 2008; IUCN, 2013).

Hynobius tenuis Nambu, 1991 is now considered a synonym of H. hidamontanus. Although its external morphology is similar to the eastern lineage of lentic-breeding species, including H. lichenatus, H. hidamontanus appears to be phylogenetically more closely related to H. nebulosus from western Japan (Matsui et al., 2002). Weisrock et al. (2013) regard H. hidamontanus as sister to a clade containing H. boulengeri and H. naevius.

References

Environment Agency of Japan (2000); Goris & Maeda

(2005); Hasumi (2007); Hasumi et al. (2002); IUCN (2013); Matsui (1987); Matsui et al (2002); Stuart et al. (2008); Weisrock et al. (2013).

Hynobius hirosei Lantz, 1931 | Ishizuchi Salamander Description

This summarises the original description by Lantz (1931). Large salamander. Head long, snout rounded. Eyes rather large, not very prominent. Gular fold present. Vomerine teeth in two short series sharply converging backwards. Body long, nearly cylindrical, with 12 or 13 well-marked costal grooves and a distinct vertebral groove extending along the base of the tail. Vent a longitudinal slit. Limbs strong, rather short, just meeting when adpressed. Four fingers, five toes. Tail strong, cylindrical in its proximal third, becoming gradually compressed, with a blunt keel above. Tailtip flattened, sharply keeled above and below, ending bluntly.

Hynobius hirosei, Tokushima Pref. Photo: Kanto Nishikawa. 68

Salamanders of the Old World | Hynobius

Colour uniformly black above, dark grey below, with patchy variations in intensity.

species of H. boulengeri (Sato, 1934), it is now given full species rank again as H. hirosei (Nishikawa et al., 2001, 2003, 2005, 2007). The map indicates the distribution of H. hirosei on Shikoku, but does not reflect the occurrence of a thus far unnamed salamander species on the Amakusa Islands and Osumi Peninsula in the southern part of Kyushu (IUCN, 2013).

Habitat

This species inhabits deciduous broad-leaved, coniferous, or mixed mountain forests, where it lives on the slopes or the bottom of small valleys.

Behaviour

Breeding takes place from early-late May at water temperatures of 8-9°C and the larvae start to hatch three to four weeks later (Sato, 1943; Nishikawa & Matsui, 2008).

Threats and conservation

This species is not immediately threatened (Environment Agency of Japan, 2000) and its conservation status has not been assessed by IUCN.

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments The range of Hynobius hirosei.

Total length 16 cm.

Diagnosis

A large salamander, uniformly black. Hynobius hirosei has a moderate body size, longer head, eyelid, fingers and toes than H. boulengeri from Honshu (Nishikawa et al., 2007).

Eggs and larvae

As in Hynobius boulengeri, the egg sacs have a light blue tint, are banana-shaped – not coiled – and have a distinct whip-like structure on the free end. Clutch size averages between 21-35 and egg sacs are on average 12-23 cm long (Nishikawa et al., 2008).

Distribution

Hynobius hirosei is distributed in Shikoku. Previously described as a separate species (Lantz, 1931) or a sub-

Hynobius hirosei is similar to H. boulengeri. The salamanders occurring in the mountainous regions of southern Honshu, Shikoku, and Kyushu were considered to belong to H. boulengeri. It was recently found that H. boulengeri from Kyushu contains discrete populations from the SoboKatamuki Mountains, the Amakusa Islands and the Osumi Peninsula, and that they are genetically closest to H. stejnegeri from the Kyushu Central Mountains. It was suggested that H. boulengeri sensu stricto should be applied to the salamanders from Honshu, the available name H. hirosei to the animals from Shikoku, and that the animals from Kyushu, as long as their formal description is pending, should be retained in H. boulengeri sensu lato (Nishikawa et al., 2007, 2008). Weisrock et al. (2013) regard H. hirosei as a sister species to H. kimurae.

References

Environment Agency of Japan (2000); IUCN (2013);

Lantz (1931); Nishikawa & Matsui (2008); Nishikawa et al. (2001, 2003, 2005, 2007, 2008); Sato (1934, 1943); Sato (2003); Thorn (1969); Weisrock et al. (2013).

Hynobius katoi Matsui, Kokuryo, Misawa & Nishikawa, 2004 | Kato’s Salamander Description

The following is based on the original description by Matsui et al. (2004). Head moderately depressed, distinctly longer than broad.

Usually 13 costal grooves. Limbs short and stout. Fore- and hindlimbs almost always separated by at least one groove when adpressed. Tail thick and rounded at base, gradually flattening towards the tip; tail-tip obtusely pointed. Tail only slightly 69

keeled. No tail-fin. Four fingers, five toes, but fifth toe very short, rudimentary or absent. Vomerine teeth in two small, obliquely arched series, nearly touching at midline, usually forming a shallow U.

Hynobius katoi, Nagano Pref. Photo: Kanto Nishikawa.

In females the distance between adpressed fore- and hindlimbs is greater than in males. Males have a relatively longer head and shorter trunk than females. Dorsal parts uniformly dark brown, rarely with scattered silvery dots. Silvery dots more common in juveniles. Underside lighter than upperparts, with silvery dots on throat and sometimes on belly. Total length 13-14 cm.

Diagnosis

Most similar to Hynobius naevius in general body proportions, but with a nearly spotless back, narrower head, shorter trunk, fewer vomerine teeth, much more shallowly curved vomerine tooth series and a considerably different electrophoretic allozyme profile. Differs from sympatric H. kimurae in having a much smaller, almost spotless body, longer head, shorter trunk, fewer vomerine teeth, and much shallower vomerine tooth series, as well as in electrophoretic profile.

Eggs and larvae

Although egg sacs of this species have not yet been found they are probably laid in underground streams. Ovarian eggs are large (diameter 4.9 mm), without pigment, and few in number per clutch.

70

Salamanders of the Old World | Hynobius

The range of Hynobius katoi.

Distribution

This species is only known from south central Japan, the montane region of the northwestern part of Shizuoka Prefecture, and the southeastern part of Nagano Prefecture, on the Akaishi Mountains, and along the Oi-gawa and Tenryugawa Rivers. It is found between 500-1,200 m altitude (Matsui et al., 2004; IUCN, 2013).

Habitat

This species inhabits an area where landslides are frequent, suggesting large quantities of underground water. It is presumed to be a larval developer and to breed in streams. Since no breeding sites have yet been found, it probably breeds in underground streams, similar to a morphotype of Hynobius naevius (IUCN, 2013).

Behaviour

The natural history of Hynobius katoi is poorly understood. Females with ripe eggs were collected from late April-early May. Small, recently metamorphosed juveniles have been found in late August.

Threats and conservation

There are insufficient data to assess the species’ conservation status (Matsui et al., 2004; IUCN, 2013).

Observations in captivity species being kept in captivity.

There are no reports of this

Comments

This species is a lotic-breeder and a member of the Hynobius naevius group (Sato, 1943) as evidenced by studies of its karyotype, which corresponds to the chromosome number usually associated with lotic-breeders (Nishikawa et al., 2005a).

References

IUCN (2013); Matsui et al. (2004); Nishikawa et al.

(2005a); Sato (1943).

Hynobius kimurae Dunn, 1923 | Hida Salamander Description

Similar to Hynobius naevius. Stocky trunk with 13-15 costal grooves. Four fingers and usually four instead of five toes (Dunn, 1923; Thorn, 1969). Trunk is a little longer in female than in male. Female cloaca is somewhat swollen, the male cloaca is a longitudinal slit. The tail of the male is higher than that of the female near the tail-tip (illustrated in Akita & Miyazaki, 2009). Upperparts brown black, tending to purple and speckled with numerous yellow spots. Underparts grey brown. Total length 12-14 cm with marked geographical variations in adult body size (Misawa & Matsui, 1997; Akita & Miyazaki, 2009). Animals tend to be larger in populations from the easternmost and westernmost parts of its range compared with those from geographically intermediate populations (Matsui et al., 2009).

Diagnosis

A salamander with a short, fat tail; long vomerine tooth series in U-shape; four toes in many individuals; yellow spots on back.

Eggs and larvae

Egg sacs are laid under rocks in the headwaters or side rivulets of mountain brooks, usually in eddies

Hynobius kimurae, gravid female, Hokujo, Hakuba-mura, Nagano Pref. Photo: Masato Hasumi.

Hynobius kimurae, mass of egg sacs, moved from hidden sites to open site, Hokujo, Hakuba-mura, Nagano Pref. Photo: Masato Hasumi.

Hynobius kimurae, Western Tokyo. Photo: Tim Johnson. 71

where the current is not too strong. The egg sacs are long and straight, with the free tip bent back sharply into a hook. The gelatinous sac typically has a purplish sheen and is very tough (Goris & Maeda, 2005). Clutch size varies from 17-40 eggs, egg diameter ranging from 4.2-5 mm (Akita & Miyazaki, 2009). Older females tend to lay larger eggs (Misawa & Matsui, 1999). Larvae hatch after 37-65 days, depending on water temperature. After hatching they may remain in the egg sac and emerge 14-29 days later (Misawa & Matsui, 1997; Akita & Miyazaki, 2009). Larvae live along the edges of streams where the current is slowest, feeding on mayfly larvae, other aquatic insects and also smaller salamander larvae. In many larvae, fingers and toes have small black claws, which disappear at metamorphosis (Goris & Maeda, 2005). Larval development varies between populations depend-

ing on availability of water and food. In some places larvae metamorphose between late July and late September, in other areas most larvae overwinter and metamorphose between late May and mid-June of the second year (Misawa & Matsui, 1997).

Distribution

This species occurs in montane areas in Kanto, Chubu, Hokuriku, Kinki and Chugoku Districts, Japan (IUCN, 2013).

Habitat

This species inhabits broad-leaved deciduous forest, mixed forest and conifer forest (IUCN, 2013). The animals live in moist places under old logs, large rocks, and in forest litter in seepage areas, etc. (Goris & Maeda, 2005).

Behaviour

Hynobius kimurae forages at night, feeding on earthworms, slugs, spiders, small insects, etc. (Goris & Maeda, 2005). Salamanders migrate to the breeding sites in the headwaters of small streams as early as December, where they spend the winter. Spawning takes place earlier than in other Hynobius species, from early February-April, and larvae hatch from April onward (Misawa & Matsui, 1997).

Threats and conservation

This species is presently not threatened and is listed as of Least Concern (IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Hynobius kimurae varies considerably in ecological traits among populations. Skeletochronological analysis suggests that the minimum maturation age in males is five years in Tokyo and six years in Kyoto, while females of both populations need at least seven years. Older and larger females tend to lay larger eggs. This species usually lives for more than 10 years (Misawa & Matsui, 1999). Weisrock et al. (2013) regard H. hirosei as a sister species to H. kimurae.

References The range of Hynobius kimurae.

Akita & Miyazaki (2009); Dunn (1923); Goris & Maeda (2005); IUCN (2013); Matsui et al. (2009); Misawa & Matsui (1997, 1999); Thorn (1969); Weisrock et al. (2013).

Hynobius leechii Boulenger, 1887 | Leech’s Salamander, Northeastern Salamander Description

A small salamander. Tail shorter than snoutvent length. Head a little longer than wide, slightly depressed; snout short and round, large eyes. Vomerine teeth (31-36) in V-shaped pattern. Labial fold absent. Gular fold present. Body almost cylindrical, with 11-12 (Litvinchuk & Borkin, 2003) or 11-14 (Fei et al., 2006) costal grooves. Limbs of moderate

72

Salamanders of the Old World | Hynobius

length, fingers and toes do not meet when fore- and hindlimbs are adpressed. Prominent tubercles on palms and soles. Base of tail cylindrical, gradually compressed toward the tip and ending in an obtuse tip. Dorsal caudal fin present. Colour olive-brown to blackish-brown above, mottled with irregular grey-brown spots; tail greyish-brown with some dark

Larvae feed on small aquatic invertebrates and, like many salamander species, also eat amphibian larvae, as well as cannibalising conspecifics. Foraging experiments have shown that the frequency of cannibalism was similar between sibling and non-sibling groups, and that small siblings are more vulnerable to cannibalism by large siblings than large ones (Park et al., 2005).

Distribution

Hynobius leechii, Chiak-san National Park, Korea. Photo: Max Sparreboom.

This species ranges from northeastern China (Liaoning, Jilin, Heilongjiang; Fei et al., 2006) southward to North and South Korea. The southern limits of its range are in southern South Korea, where it is replaced by Hynobius quelpaertensis in the southwestern coastal zones and by H. yangi on the southeastern coast (Kim, 2009). Molecular work has revealed substantial diversity in Korean Hynobius populations, suggesting the presence of at least three extra cryptic species (Baek et al., 2011; Zheng et al., 2012).

spotting. Light grey below. Juveniles speckled with small lightcoloured spots. During the breeding season the female can be recognised by her swollen abdomen and cloaca (Kang & Yoon, 1975; Park & Park, 2000), while the male has a higher tail-fin and swollen cloaca (Kim et al., 2009). Females have shorter legs than males, while the legs are proportionately longer in juveniles (Dunn, 1923). Total length 9-14 cm (Zhao, 1998) but more usually 11-12 cm; the female a little larger than the male (Park et al., 1996).

Diagnosis

A small, dark-coloured salamander with slightly flattened tail; irregular dark spots on dorsum and tail; tubercles on palms and soles (Fei et al. (2006).

Eggs and larvae

The female produces a pair of egg sacs, containing 57-125 eggs. When fully hydrated, the egg sacs reach 12-14 cm in length and 12 mm in width, but there is considerable variation in their shape (Song & Koo, 2010). Egg sacs are attached to stones or twigs underwater in streams, ponds and rice fields. Fertilised eggs normally hatch within 3-4 weeks and larvae have an aquatic period of 1-2 years (Park & Park, 2000). Zhao (1998) and Liu et al. (1984) however, record a hatching time of 10-16 days, as a result of keeping eggs at higher temperatures in the laboratory. Upon hatching larvae measure 12-13 mm and have three pairs of external gills and well-developed balancers. When the larvae start to swim the dorsal fin occupies about two thirds of the length of the back, starting from the level where the gills end. At a length of 30-35 mm the balancers disappear. Metamorphosis takes place when the animals have reached a size of approximately 40 mm, and life on land begins (Liu et al., 1984).

The range of Hynobius leechii.

Habitat

This species occurs in hilly, forested terrain, along streams, where it is found in moist places under stones and logs. During the breeding season it lives in the quiet parts of streams, ponds and rice fields.

Behaviour

From October-November to early April the animals hibernate on land, in soft soil under stones and tree roots. Food consists of live prey, such as earthworms, insects and aquatic invertebrates (Yoon et al., 1996). 73

In China the animals enter the water in the beginning of April when water temperatures are 2-5°C. The breeding season extends from mid-April to mid-May when water temperatures range from 4-12°C (Liu et al., 1984). In South Korea they may enter the water earlier, in late February, and the breeding season lasts from early March to early April. Males arrive at a breeding site 2-3 days earlier than females and stay there for approximately 10 days (Sung et al., 2005; Lee & Park, 2008). Males outnumber the females present in the water. This malebiased operational sex ratio implies fierce competition among males to monopolise and fertilise the eggs. In general, three to four males simultaneously mate with a single female. As a result, multiple fertilisations of the egg sacs of one female occur, as the competing males scramble over the egg sacs (Park & Park, 2000; Kim et al., 2009). Sexual behaviour consists of three stages: identification, courtship and fertilisation. The male identifies the female by sniffing and making snout contact. He courts the female using several behaviour patterns, involving rubbing his chin against the female’s head, undulating his body and tail, sniffing, and so-called digging displays, during which the male moves under the female’s body using his head and forelimbs. Shortly before the egg sacs appear, the male clasps the female’s back with foreand hindlimbs. He may then free his fore legs from the female, while keeping his hind legs positioned near the female’s cloaca; he grabs the egg sacs with his fore legs and chin, and pulls them out of the female’s body. When the eggs are separated from the female, the male wraps his body around the egg sacs, holding them between his forelimbs, mouth and hindlimbs, scratches the eggs with his hind feet and releases his sperm over the eggs (Park et al., 1996). After fertilisation the male may keep his body wrapped round the eggs for some time, a posture interpreted as egg guarding behaviour (Park & Park, 2000).

gives two different types of vibration signal, a body undulation as part of the mating display by the male to the female (Kim et al., 2009) and a tail undulation as an aggressive display between rival males. Males often perform aggressive displays in which only the distal part of the tail is waved, before and after attacking other males (Park et al., 2008).

Threats and conservation

This species is still relatively common in Korea. Its habitats are disappearing in China, for instance on Mt. Qian-shan, due to forest clearance and environmental pollution (Zhao, 1998). However, its conservation status, is considered as of Least Concern (IUCN, 2013)

Observations in captivity

This species has been bred in the laboratory (Liu et al., 1984; Park et al., 1996). Animals described as Hynobius leechii in breeding accounts from the Netherlands (Leeuwen & Vos, 1991; Bouwman, 1995) actually originated from Cheju Island and are now known as H. quelpaertensis.

Comments

Hynobius leechii shows a higher genetic variation in the southern part of its range than in the north (Zeng & Fu, 2004). A related species occurs in the southwestern coastal areas and Cheju Island, H. quelpaertensis, and another in the area around Kori in the southeast, H. yangi (Yang et al., 1997; Kim et al., 2003). Kim et al. (2007) argued that the three Korean species were not monophyletic, with H. yangi appearing to be more closely related to the Japanese H. nebulosus than to H. leechii. Weisrock et al. (2013) later decided that they are monophyletic, with their closest relatives in the sister clade containing H. okiensis, H. tsuensis, H. dunni and H. nebulosus.

References

Baek et al. (2011); Bouwman (1995); Dunn (1923); Fei et al.

(2006); IUCN (2013); Kang & Yoon (1975); Kim et al. (2003, 2007, 2009); Lee & Park (2008); Leeuwen van & Vos (1991); Litvinchuk & Borkin (2003); Liu

When two males meet, the encounter may end in one moving away voluntarily, or it may be driven off as the other bites it on the chin and shakes its neck (Park et al., 1996). Hynobius leechii

et al. (1984); Park & Park (2000); Park et al. (1996); Park et al. (2005, 2008); Song & Koo (2010); Sung et al. (2005); Weisrock et al. (2013); Yang et al. (1997); Yoon et al. (1996); Zeng & Fu (2004); Zhao (1998); Zheng et al. (2012).

Hynobius lichenatus Boulenger, 1883 | Northeastern Salamander Description

Large head, as wide as long. Snout short and rounded. Eyes moderately developed but prominent. Gular fold present. Body rather short with 11, occasionally 10-12 costal grooves, excluding an axillary groove (this counting method is commonly used for other hynobiid salamanders). Tail a little shorter than snout-vent length, flattened and ending in a blunt point. Limbs rather long. When adpressed fingers and toes overlap by one or two grooves in males, they meet or are

74

Salamanders of the Old World | Hynobius

separated by one groove in females (Hasumi & Iwasawa, 1987b). This difference is also found in other Hynobius species. Four fingers, five toes; fifth toe sometimes rudimentary. Skin smooth. External morphology shows considerable geographic variation (Hasumi & Iwasawa, 1987a, 1987b, 1988, 1993). Females are a little smaller than males. During the breeding season males have an Y-shaped cloaca, while females have a

simple longitudinal fold. The tail-fin is higher in the male and the fore legs longer than in the female. It is difficult to distinguish the sexes after the breeding season, when differences in cloacal fold and tail height are less clear.

Hynobius lichenatus. Photo: Hans-Joachim Herrmann.

Upperparts blackish, dotted with olive-grey speckles, giving the skin a lichen-like appearance. Whitish spots on the sides of the body. Underparts grey (Stejneger, 1907; Dunn, 1923; Thorn, 1969). Length 10-11 cm (Thorn, 1969).

Diagnosis

A small species with relatively short and flattened tail. Very short series of vomerine teeth in U or V form. When adpressed toes and fingers overlap.

Eggs and larvae

Egg sacs very different from Hynobius nigrescens. A long gelatinous string 12-15 cm in lenght and 1.5-2 cm diameter. 18- 27 eggs per sac, rarely 40-60 (Takahashi & Iwasawa, 1989a, 1990). Matsui & Miyazaki (1984) report a mean total clutch size of 40. Egg diameter 3-3.7 mm. Clutch size and egg size vary with the strength of the water flow in larval habitats: stream-breeding populations deposit larger eggs and pond-breeding populations deposit smaller eggs (Takahashi & Iwasawa, 1989a, 1990). The skin of the sac has a rugose appearance, with strong longitudinal striations (Thorn, 1969; Matsui, 1987). Larvae hatch at 12-14 mm, with balancers present. Larvae are of standing water-type and the dorso-caudal fin begins at the level of the forelimbs. It is lower than in H. nigrescens. Metamorphosis takes place in autumn at ca. 40 mm (Goris & Maeda, 2005)

The range of Hynobius lichenatus.

Distribution

Hynobius lichenatus occurs in the northern parts of Hondo, Japan. It is distributed in Tohoku District and Niigata, Gunma, Tochigi and Ibaragi Prefectures from coastal areas up to 1,500 m altitude (IUCN, 2013). This species’ range overlaps with that of H. nigrescens and occasionally the two species use the same ponds for reproduction (Hasumi & Kakegawa, 1989).

Habitat

This is a lentic-breeding species that occurs in forests in low hills along small streams. Whereas Hynobius nigrescens breeds exclusively in standing water, H. lichenatus reproduces in a variety of habitats such as permanent streams and small, temporary ponds (Takahashi & Iwasawa, 1990).

Behaviour

Breeding takes place from February-June, especially from April-May. Reproductive behaviour is probably similar to that of Hynobius retardatus, but there are no published descriptions of its behaviour.

Threats and conservation

This species is currently not under major threat and it is listed as of Least Concern (IUCN, 2013).

Observations in captivity

The species has been kept and bred in captivity by Wallays (Raffaëlli, 2007). These 75

salamanders should be kept in hibernation for several months each year.

Comments

Molecular work on populations across the species’ distributional range indicates that Hynobius lichenatus is monophyletic and contains three geographically structured clades. The genetic distances between these clades are as large as those seen between different species of Hynobius (Aoki et al., 2013), so descriptions of new species can be expected.

According to Weisrock et al. (2013) Hynobius lichenatus is sister to H. tokyoensis and clusters in a clade that also contains the sister species H. takedai and H. nigrescens.

References

Aoki et al. (2013); Dunn (1923); Goris & Maeda (2005);

Hasumi & Iwasawa (1987a, 1987b, 1988, 1993); Hasumi & Kakegawa (1989); (IUCN (2013); Matsui (1987); Matsui & Miyazaki (1984); Raffaëlli (2007); Stejneger (1907); Takahashi & Iwasawa (1989a, 1990); Thorn (1969); Weisrock et al. (2013).

Hynobius maoershanensis Zhou, Jiang & Jiang, 2006 | Maoer Shan Salamander Description

This is based on the original descriptions of Zhou et al. (2006) and Fei et al. (2009). This is a large salamander similar to Hynobius guabangshanensis. Snout is rounded; distance between nares slightly smaller than between eyelids. Labial fold absent. Gular fold prominent and visible in dorsal view. Angle of jaw far exceeds the posterior margin of the eye. Tongue oval in shape, free at the sides. Trunk is stout and flat with a prominent vertebral groove and 12 costal grooves. Limbs are well-developed. Fingers and toes overlap by 2.5-3 costal grooves when the limbs are adpressed. Four fingers and five toes. Tubercles on palms and soles are absent or inconspicuous. Base of the tail is rounded, posterior part of the tail is gradually laterally compressed. Caudal fin is inconspicuous. Tail about 84% of snout-vent length.

Colour of the dorsum is uniformly black in water and turns yellowish-green on land. Ventral colour is grey with numerous white spots. Total length in males 152-160 mm, 136-155 mm in females.

Diagnosis

A stocky salamander with 12 costal grooves. The unique morphology of chromosome 13 is a distinguishing marker in the karyotype of this species (Qing et al., 2008). Hynobius maoershanensis differs from H. chinensis by having numerous white spots on the ventral side, whereas H. chinensis has dark blotches.

Hynobius maoershanensis, Maoershan Guilin Pref., Guangxi. Photo: Hou Mian, courtesy Zeng Xiaomao. 76

Salamanders of the Old World | Hynobius

Hynobius maoershanensis, North-eastern Guangxi. Photo: Kanto Nishikawa.

Eggs and larvae

The female lays a pair of egg sacs, each containing 37-45 eggs. As in Hynobius guabangshanensis, egg sacs are less than 20 cm long, slightly arched but not forming a helix (Zhou et al., 2006; Fei et al., 2009).

Distribution

Currently known only from the type locality, Maoershan Mountain, in Xingan County, Guangxi Zhuang Autonomous Region, southern China (IUCN, 2013).

Habitat

This species occurs in marshes and surrounding forests at an altitude of ca. 2,000 m. The swamps are surrounded by conifers (Tsuga chinensis) and broad-leaved trees. In the breeding season, the salamander is found in lentic ponds with clear water and a thick layer of silt. Outside the breeding season the species is terrestrial and hard to find (Zhou et al., 2006; IUCN, 2013).

Behaviour

Breeding takes place from early November until the end of February. Males appear to guard the eggs after oviposition (Zhou et al., 2006; IUCN, 2013).

The range of Hynobius maoershanensis.

Threats and conservation

This species is probably adversely affected by human activities in its habitat but insufficient data exist to assess its status (IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Morphologically this species appears to differ from Hynobius guabangshanensis only in relative tail length and number of vomerine teeth. Little is known of the distributions of either species. Their type localities are situated relatively close together. Xia et al. (2012) consider H. guabangshanensis and H. maoershanensis to be sister species. Together with H. amjiensis and H. chinensis they form a clade that is sister to H. yiwuensis. According to the tree proposed by Zheng et al. (2012), H. maoershanensis is sister to H. chinensis.

References

Fei et al. (2009); IUCN (2013); Qing et al. (2008); Xia et al.

(2012); Zheng et al. (2012); Zhou et al. (2006).

Hynobius naevius (Temminck & Schlegel, 1838) | Blotched Salamander Description

Large head, oval when viewed from above. Fairly large eyes. Paratoids flat and distinct. Gular fold present. Stocky trunk with 14 costal grooves. Tail short; shorter than snout-vent length, fat and round, slightly compressed toward the tip and ending in a blunt tip. Limbs short, four fingers, five toes. Skin smooth. Sexes hard to distinguish. During the breed-

ing season the female has a more protruding cloaca, whereas the male simply has a longitudinal fold – the reverse of the sexual dimorphism observed in other Hynobius species. White dots on flanks more pronounced in female than in male. End of tail slightly compressed in the male, lower and more pointed in the female (Thorn, 1972). 77

Hynobius naevius. Photo: Henk Wallays.

Hynobius naevius, larva, Hino County, Tottori Pref. Photo: Max Sparreboom.

Dorsal parts black with a sprinkling of tiny bluish dots. On the flanks the bluish dots are more numerous and dominate the colouration. Underparts pink to bright grey with minute white dots.

and leave the water from the middle of August to the end of September, while others remain in the water until the following spring or summer (Goris & Maeda, 2005).

This species exhibits considerable morphological, allozyme and genetic variation (Tominaga et al., 2003, 2005, 2006; Sakamoto et al., 2005).

Distribution

This species ocurs in montane areas of Chugoku and Kyushu Districts. It is found between 300-1,000 m altitude (IUCN, 2013).

Total length 13-14 cm (Thorn, 1969).

Diagnosis

A stocky salamander with short, fat tail. Long vomerine tooth series in V-shape. Fingers and toes do not touch when adpressed.

Eggs and larvae

Egg sacs are laid under rocks in the headwaters or side rivulets of mountain brooks, usually in eddies where the current is not too strong (Goris & Maeda, 2005). The egg sacs are elongate and spiraled, are approximately 14 cm long, and contain some 20 eggs each. Egg sac diameter 2.5 cm, egg diameter 2.5-3 mm, eggs brown with yellowish-white underside. Larvae measure 16 mm upon hatching. Balancers absent and gills well-developed. Gills are a little smaller than those of Hynobius nebulosus. Dorso-caudal fin on the hind part of back and tail only. Tail-tip pointed. May rarely show weakly developed horny coverings on fingers and toes. Larvae may reach 60 mm total length (Thorn, 1969). The larvae live along the edges of the stream where there is almost no current and feed on aquatic insects and other prey. Some larvae metamorphose

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Salamanders of the Old World | Hynobius

The range of Hynobius naevius.

Habitat

Hynobius naevius is a lotic species, that breeds in streams in broad-leaved evergreen, and mixed forests. (IUCN, 2013).

Behaviour

Hynobius naevius hides under logs and rocks or forest litter, foraging at night and on rainy days. It does not migrate to the breeding sites until the spring thaw, so that breeding occurs from the end of March to the end of May (Goris & Maeda, 2005). For an account of reproductive behaviour see under Observations in Captivity, below.

Threats and conservation

This species is common within its range and presently not threatened. It is listed as of Least Concern (IUCN, 2013).

Observations in captivity

This species has been bred in captivity (Thorn, 1969, 1972; Raffaëlli, 2007) and reproduced at a water temperature of 8°C. Adults were fed earthworms. Eggs and larvae of this species require more care than those of species that reproduce in standing waters. The adults can be kept alive for many years. The following description is based on observations on one pair in captivity (Thorn, 1972). In the water the breeding male frequently makes a rhythmic shivering movement with his body, especially visible in the region of the head and tail. The male moves under the female, makes the shivering movement and moves away

again. While engaged in these movements, the female sometimes sniffs his body. After a while it is the female that approaches the male and tries to move under his body whereupon he makes the shivering movements. She keeps trying to move under him and appears to manoeuvre her body in such a way as to maximise contact between their bodies. The eggs are laid after this preamble, attached to the twig of a water plant. The female creeps under the male once more, then moves to the egg sacs and moves under them. The male follows her to the eggs and then grasps the egg sacs first with his fore legs, then with his hind legs, curling his body, thus rubbing the eggs against his cloaca.

Comments

Hynobius naevius appears to be composed of two distinct groups, one of large size, the other of smaller size (Tominaga & Matsui, 2007). The type series is most similar to specimens from the group of larger animals from Mt. Tara-dake in NW Kyushu, Japan, suggesting that the type locality is in that region (Tominaga & Matsui, 2007). The animals belonging to the second group represent a cryptic species, associated with the subspecies H. naevius yatsui. This taxon is now elevated to full species rank, H. yatsui (Tominaga & Matsui, 2008). According to Weisrock et al. (2013), H. naevius is sister to H. boulengeri and clusters with H. hidamontanus in one clade.

References

Goris & Maeda (2005); IUCN (2013); Raffaëlli (2007);

Sakamoto et al. (2005); Thorn (1969, 1972); Tominaga et al. (2003, 2005, 2006); Tominaga & Matsui (2007, 2008); Weisrock et al. (2013).

Hynobius nebulosus (Temminck & Schlegel, 1838) | Clouded Salamander Misty Salamander

Description

A small stocky salamander. Head small, a little longer than wide; snout short and rounded. Eyes small, paratoid glands inconspicuous. Gular fold present. Trunk stocky, with 13 costal grooves. Tail shorter than snout-vent length, thick at the base and flattened laterally toward the tip. Four fingers and five toes. Montane populations from Hiroshima Prefecture usually have four toes (Okawa & Utsunomiya, 1989). Limbs relatively short; fingers and toes do not touch when adpressed. Skin smooth. Upperparts yellowish-brown, more or less dark, covered with small, fine dark spots. Flanks of juveniles often dotted with small grey-blue speckles. Dorsal part of tail lighter yellow. Underside light yellowish-brown to grey. Colour is variable. In the southeastern part of Hiroshima Prefecture it is yellowish-brown with small dark spots, in the northern montane region of Hiroshima Prefecture it is dark brown with brown spots (Okawa & Utsunomiya, 1989).

in breeding season. After the breeding season it is hard to distinguish the sexes.

In males, tail-fin is higher in the breeding season and more or less undulating; large white spot on throat and swollen cloaca

There is considerable morphological and genetic variation between populations of Hynobius nebulosus (Matsui et al., 2006).

Hynobius nebulosus, Kyoto. Photo: Tim Johnson.

79

Total length approx. 7-12 cm (Okawa & Utsunomiya, 1989). Stejneger (1907) gives a maximum length of 13.5 cm.

Diagnosis

A small, stocky salamander with slightly flattened tail; 13 costal grooves; back ‘misted’ with tiny black dots; dorsal and ventral edges of tail often yellow.

Eggs and larvae

The female produces a pair of spiraled egg sacs, each containing 40-90 eggs in some localities, but only 15-40 at other sites (Okawa & Utsunomiya, 1989). When fully hydrated, the egg sacs reach 20 cm in length and 15 mm in width. Egg diameter 2 mm, brown with a yellowish underside (Thorn, 1969). Egg sacs are attached to dead branches, litter, and so on, a few cm under the water surface, or may be found on the sand at the bottom of slow-flowing streams, or buried in the mud (Okawa & Utsunomiya, 1989). Fertilised eggs normally hatch after 25-30 days. On hatching, larvae measure 12 mm and have three pairs of external gills and well-developed balancers. Metamorphosis takes place at the end of the summer at a larval length of approximately 35 mm, and life on land begins.

Larvae feed on small aquatic invertebrates and, like many salamander species, also eat amphibian larvae, as well as cannibalising conspecifics.

Distribution

This species is widely distributed in southwestern Japan, including Kinki, Chugoku, Shikoku and Kyushu Districts. It is known from coastal to hilly areas up to 300 m altitude (IUCN, 2013) and reaches 1,200 m in Hiroshima Prefecture (Okawa & Utsunomiya, 1989).

Habitat

This species inhabits forests and swamps, where it is found in moist places under stones and logs. It breeds in paddy fields, ditches and springs (IUCN, 2013), but also in slow-flowing mountain streams. In Hiroshima Prefecture it occurs in a variety of habitats, from lowlands to the highlands.

Behaviour

Its food consists of various insects, spiders and earthworms (Ihara & Fujitani, 2005). The majority of males start breeding at the age of 2.8-2.9 years, most females are considered to mature after 4.8-4.9 years (Ento & Matsui, 2002). The male moves to the breeding waters at the end of autumn and develops a white spot on the throat, a darker colouration and higher tail-fin. Reproduction starts

Hynobius nebulosus, larva, Hino County, Tottori Pref. Photo: Max Sparreboom.

Hynobius nebulosus, habitat, area used for research on Kyoto University campus. Photo: Max Sparreboom. 80

Salamanders of the Old World | Hynobius

The range of Hynobius nebulosus.

from December-January in lowland populations, later at higher altitudes, and from mid-April to May in highland populations (Okawa & Utsunomiya, 1989). Larger males come to the breeding site first and establish territories at spots suitable for egg laying. They defend their territories against intruding males and stay longer at the breeding site than non-territorial males. Smaller males arrive a little later. Some establish lower quality territories in unoccupied areas, while others do not form territories but wander around established males, sneaking access to the eggs when females appear. Females appear a little later and more gradually than males. Female arrival and egg laying is spread out over time and may extend over a period of ten weeks (Tanaka, 1989). The male stays on his territory, making undulating movements with his tail and makes rhythmic convulsive jerks with his body when a female approaches. As soon as the female is about to produce the egg sacs, the male grabs one end of the sac between his forelimbs and slightly lowered head. He pulls the egg sac out of the female’s body, and embraces it with fore- and hindlimbs, thus pressing it against his cloaca. At this moment he releases his sperm, fertilising the eggs. After fertilisation the male stays near the egg sacs, his tail making undulating movements, thereby attracting other females while keeping other males away. Females leave the breeding waters immediately after egg laying (Thorn, 1963, 1967, 1969).

Threats and conservation

This species is still relatively common in SW Japan, but its habitats are threatened by house building, road construction, water pollution, invasive species and habitat drainage. The species is also collected for the pet trade. It is ranked as Vulnerable in the Red List of Japan (Yoshikawa et al., 2013a) and is listed as of Least Concern by IUCN (2013).

Observations in captivity

The species has been bred in captivity over many years (Thorn, 1963, 1967, 1969, 1986; Thorn & Raffaëlli, 2001). The animals reproduced at a water temperature of 5-10° C. Adults were fed earthworms. In captivity males may reach sexual maturity after 1-2 years, females after two or three years (Thorn, 1969). One individual lived in captivity for over 20 years (Raffaëlli, 2007). The minimum longevity observed in a natural population is nine years for males and five for females (Ento & Matsui, 2002).

Comments

Hynobius nebulosus is considered a typical lentic-breeder, but also occurs at higher altitudes, where it breeds in high altitude wetlands and small streams (Okawa & Utsunomiya, 1989). Hynobius nebulosus is the sister species of H. dunni (Weisrock et al., 2013).

References

Ento & Matsui (2002); Ihara & Fujitani (2005); IUCN

(2013); Matsui et al. (2006); Okawa & Utsunomiya (1989); Raffaëlli (2007); Stejneger (1907); Tanaka (1989); Thorn (1963, 1967, 1969, 1986); Thorn & Raffaëlli (2001); Weisrock et al. (2013); Yoshikawa et al. (2013a).

Hynobius nigrescens Stejneger, 1907 | Black Salamander Description

A fairly large salamander. Head rectangular when viewed from above. Snout rounded, large, prominent eyes. Gular fold present. Body robust, 11-12 costal grooves extending into transversal folds on underside. Tail thick at the

Hynobius nigrescens. Photo: Klaus-Detlef Kühnel.

base, strongly flattened laterally, ending in an obtuse tip; a little longer than snout-vent length in the male, a little shorter than snout-vent length in the female. Limbs well-developed. Four fingers, five toes. Skin smooth.

Hynobius nigrescens. Photo: Klaus-Detlef Kühnel.

81

Upperparts bluish dark brown in the male, almost black in the female. Underparts pinkish-grey to purple. Females are a little smaller than males. Especially during the breeding season, males have an Y-shaped cloacal opening with a small tubercle at the anterior angle of the vent, while females have a simple longitudinal slit. In a population where breeding occurs in March, this tubercle is present throughout the year, except from May-July, when ventral glands are underdeveloped (Hasumi et al., 1990). In the breeding season, head width, tail height and hind legs are greatly enlarged in the male. These seasonal changes are more pronounced in pond-breeding than in stream-breeding Hynobius species. Females show little seasonal variation in head width or tail height, but exhibit a large increase in body mass, as a result of water absorption during the formation of egg sacs (Hasumi & Iwasawa, 1990). Length 12-19 cm (Goris & Maeda, 2005).

Diagnosis

A large, dark-coloured species with long and strongly flattened tail. Series of vomeral teeth long and in V- or U-shape. Toes and fingers overlap when adpressed.

Eggs and larvae

The female produces a pair of spindleshaped egg sacs, 9-13 cm long and 5-6 cm wide, whitish and often opaque (Takahashi & Iwasawa, 1989b). The outer envelope of the sac is soft and gelatinous and looks swollen. A clutch contains a total of 40-140 eggs (Goris & Maeda, 2005) with a diameter of 2.5-3 mm, brown with a yellowish vegetal pole. Although usually fertilised directly after being laid, egg sacs may remain viable even after three hours in water (Hasumi

The range of Hynobius nigrescens. 82

Salamanders of the Old World | Hynobius

et al., 1993). Upon hatching larvae measure 12-15 mm and have balancers. Larvae are of standing water type. Fairly high dorsocaudal crest beginning at the level of the fore legs. Tail-tip pointed. Gills well-developed (Thorn, 1969). At low altitudes eggs hatch in about one month, but development may take longer at higher elevations. Larvae feed on aquatic insects, frog tadpoles and each other. Metamorphosis takes place from summer to early autumn at a total length of 48-62 mm. Colour is black or dark brown, with numerous white dots on dorsal and lateral surfaces (Iwasawa & Yamashita, 1991). Some larvae overwinter and leave the water the following year (Goris & Maeda, 2005).

Distribution

Hynobius nigrescens is the most widely distributed of the Japanese Hynobius species. It occurs throughout the Tohoku District and parts of the Kanto and Chubu districts of northeastern Honshu. It is also found on Sado island (Matsui et al., 1992).

Habitat

This species occurs from coastal areas to alpine zones in forests and montane grasslands (IUCN, 2013) and can even be found on the edges of craters of extinct volcanos. It has been found at 2,500 m altitude on Mt. Otaki, Nagano Prefecture (Thorn, 1969). Breeding takes place in lakes, ponds, pools, paddie fields and ditches (IUCN, 2013).

Behaviour

These salamanders hide under dead leaves, fallen logs and rocks. They are nocturnal, feeding on millipedes, spiders, small insects, small land crabs and earthworms. Hibernation is on land starting in October. Breeding takes place from February-July, depending on altitude (Goris & Maeda, 2005). Unlike, for instance, Hynobius takedai (Tanaka, 1986) and H. nebulosus (Tanaka, 1989), males of H. nigrescens do not establish real territories. They temporarily take hold of a twig which females visit for oviposition and frequently change position with other males. When a female clings to an occupied twig and rubs her cloaca on it, the male brings his snout close to her cloaca. The female attaches the adhesive tips of the egg sacs to part of the twig and the male then mounts her back and folds his forelimbs around her pelvic region. Immediately after the egg sacs begin to protrude from the female’s cloaca, the male shifts his forelimbs to the egg sacs. The male pushes the female away with his hindlimbs, discharging seminal fluid onto the egg sacs. This action results in the egg sacs being freed from the female’s cloaca. At this time neighbouring males may rush to the spawning pair and also try to fertilise the eggs. With males often outnumbering females at the breeding site, males may scramble-compete for access to the egg sacs, forming mating balls wrapped around the egg sacs (Hasumi, 1994, 2001a).

Threats and conservation

Comments

Observations in captivity

References

This species is still relatively common in northern Japan and listed as of Least Concern (IUCN, 2013).

The species has been kept in captivity and can be housed in the same way as Hynobius retardatus. There are, however, no records of successful captive breeding.

Hynobius sadoensis is considered a synonym of H. nigrescens. Weisrock et al. (2013) cluster H. nigrescens with H. takedai as sister species. Goris & Maeda (2005); Hasumi (1994, 2001a); Hasumi

et al. (1990, 1993); Hasumi & Iwasawa (1990); IUCN (2013); Iwasawa & Yamashita (1991); Matsui et al. (1992); Takahashi & Iwasawa (1989b); Tanaka (1986, 1989); Thorn (1969); Weisrock et al. (2013).

Hynobius okiensis Sato, 1940 | Oki Salamander Description

Morphologically somewhat similar to Hynobius naevius (but see comments). Trunk relatively long and stout with 13 or 14 costal grooves. Tail a little shorter than snout-vent length, thick at the base and vertically compressed posteriorly. Limbs long and robust. Four fingers, five toes. When fore- and hindlimbs are adpressed, toes and fingers overlap by at least one costal groove. Dorsal parts reddish-brown with irregular yellowish spots. Underside is lighter without markings. Total length 12-13 cm (Goris & Maeda, 2005).

Diagnosis

Differs from H. naevius in following characteristics: vomerine tooth series in U-shape. Limbs moderately developed. When limbs are adpressed fingers and toes overlap. Colour is reddish-brown with yellow spots (Thorn, 1969).

brooks. Larvae may have claws, but these are poorly developed in larvae living in slow-moving rivulets (Goris & Maeda, 2005; but see Sato, 1940, in: Matsui et al., 2007, who notes absence of claws). Some larvae metamorphose and leave the water at the end of August to early September, while others overwinter as larvae (Goris & Maeda, 2005).

Distribution

This species only occurs on the island of Dogo in the Oki islands, Shimane Prefecture, Japan. (IUCN, 2013).

Habitat

This species occurs from sea level to the tops of mountains, inhabiting evergreen forest and coniferous plantations. It breeds in streams (IUCN, 2013).

Behaviour

There is no detailed description of the egg sacs. Larvae are abundant in the small tributaries of mountain

In late autumn, many adults gather close to the headwaters of mountain brooks, where they overwinter. The breeding season of Hynobius okiensis is from end February to early April. It is thought that they breed in underground stretches of these brooks (Goris & Maeda, 2005).

Hynobius okiensis. Photo: Henk Wallays.

Hynobius okiensis. Photo: Hans-Joachim Herrmann.

Eggs and larvae

83

It is classified as Critically Endangered (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

This species has been kept in captivity but no details have been published.

Comments

The range of Hynobius okiensis.

Threats and conservation

This species is considered very vulnerable in view of its limited range and several populations have vanished due to habitat destruction. Conservation efforts are needed (Environment Agency of Japan, 2000).

Hynobius okiensis is a lotic-breeding species with characteristics of the lentic-breeding H. nebulosus group, such as the absence of claws on the tips of the digits in larvae, posteriorly compressed tail, long and fragile limbs, presence of a small protuberance at the anterior tip of the vent in the adult male, and diploid chromosome number of 2n=56 (like all species of lentic-breeding Japanese Hynobius) instead of 58 chromosomes (as in the lotic-breeders) (Sato, 1940; Matsui et al., 2007a). Electrophoretic analysis shows that H. okiensis clusters with H. nebulosus and H. dunni and is more closely related to these species than to H. naevius or H. kimurae. This result was confirmed by Weisrock et al. (2013), who found that H. okiensis is sister to a clade containing H. tsuensis, H. dunni and H. nebulosus. This suggests that the lotic-breeding H. okiensis shares a common ancestor with lentic-breeding H. nebulosus and H. dunni, and has secondarily acquired the habit of breeding in streams (Matsui et al., 2007a).

References

Environment Agency of Japan (2000); Goris & Maeda

(2005); IUCN (2013); Matsui et al. (2007a); Sato (1940); Stuart et al. (2008); Thorn (1969); Weisrock et al. (2013).

Hynobius quelpaertensis Mori 1928 | Cheju Salamander Description

A small salamander, closely related to Hynobius leechii, originally described from Cheju Island as a subspecies of H. leechii, but recently elevated to species status on the basis of electrophoretic and morphological analyses (Yang et al., 1997).

Hynobius quelpaertensis. Photo: Klaus-Detlef Kühnel. 84

Salamanders of the Old World | Hynobius

The following summary description largely follows that of H. leechii. Head a little longer than wide, slightly depressed; snout short and large round eyes. Vomerine teeth (37-42) in V-shaped pattern. Gular fold present. Body almost cylindrical

Eggs and larvae

The female produces a pair of egg sacs, each containing 30-75 eggs. When fully hydrated, the egg sacs reach 8-12 cm in length and 8-10 mm in width. Egg sacs are attached to stones or twigs under water in streams and ponds. Larvae hatch after several weeks, measuring 10-11 mm. Metamorphosis follows after 6-8 weeks at a length between 30-48 mm. Hynobius quelpaertensis males and females usually reach sexual maturity at three years of age and can live for up to 10 years (Lee et al., 2010).

Hynobius quelpaertensis, male in breeding season, ventral side. Photo: Klaus-Detlef Kühnel.

Hynobius quelpaertensis, larva. Photo: Klaus-Detlef Kühnel.

with 12-14 costal grooves (Kim et al., 2003). Limbs of moderate length, fingers and toes not meeting when limbs adpressed. Base of tail cylindrical, gradually compressed toward the tip and ending in an obtuse tip. Colour olive-brown to dark brown above, mottled with irregular grey-brown spots; tail greyish-brown with some dark spotting. Light grey below. Juveniles speckled with small lightcoloured spots. During the breeding season the female has a swollen abdomen, the male can be recognised by a higher tail-fin, a swollen cloaca, and heavier and broader head (Leeuwen & Vos, 1991; Bouwman, 1995). Total length 10-12 cm.

Diagnosis

A small, olive-brown salamander with fine black speckles and slightly flattened tail; usually 12-14 costal grooves. Genetically distinct from Hynobius leechii and H. yangi. Morphological differences from H. leechii are subtle and consist mainly of a higher number of vomerine teeth and tailbones in H. quelpaertensis (Yang et al., 1997). H. quelpaertensis is larger than H. yangi (Kim et al., 2003). The colour patterns of H. leechii and H. quelpaertensis are generally similar, H. yangi being light brown dorsally, without fine speckles (Yang et al., 1997).

The range of Hynobius quelpaertensis 85

Distribution

Threats and conservation

Habitat

Observations in captivity

Hynobius quelpaertensis occurs in the southwestern coastal zones of South Korea, including Cheju Island (Quelpart) (Kim, 2009).

The species inhabits hilly, forested terrain and agricultural areas, along streams. It moves to streams and various water bodies to breed.

Behaviour

In Cheju Island egg sacs have been found in December, at temperatures a few degrees above zero. Matings were observed in captivity from November onwards. The animals stayed in the water until early March (Leeuwen & Vos, 1991). The sexual behaviour of animals raised in captivity from eggs collected in Cheju Island was described by Leeuwen & Vos (1991) and Bouwman (1995). These observations are largely in accord with a more detailed description given for Hynobius leechii by Park et al. (1996), except that they also describe a behaviour pattern where males rub their cloacas against certain parts of the tank which are suitable for the attachment of egg sacs. They interpreted this as territorial scent marking using cloacal secretions, which would attract females to these places to deposit their eggs. In the event, females did in fact select these spots for oviposition.

No information available; the data are insufficient to assess the species’ conservation status (IUCN, 2013).

Animals referred to as Hynobius leechii in breeding accounts from the Netherlands (Leeuwen & Vos, 1991; Bouwman, 1995) originate from Cheju Island and are now known as H. quelpaertensis. The species has been bred successfully over several generations and all the animals currently circulating in the pet trade probably derive from this stock. The introduction of a cold period during winter is the key to breeding success of this hardy species, winter being the breeding season of this (and other) Hynobius species. In captivity the primary challenge is to synchronise the breeding behaviour of the two sexes.

Comments

According to Weisrock et al. (2013), the Korean Hynobius species are monophyletic and Hynobius quelpaertensis is sister to a clade containing H. leechii and H. yangi.

References

Bouwman (1995); IUCN (2013); Kim (2009); Kim et al.

(2003); Lee et al. (2010); Leeuwen van & Vos (1991); Park et al. (1996); Weisrock et al. (2013); Yang et al. (1997).

Hynobius retardatus Dunn, 1923 | Hokkaido Salamander Description

A fairly large salamander. Head oval when viewed from above. Snout rounded; large, prominent eyes. Gular fold present. 11, sometimes 12, costal grooves. Tail strongly flattened laterally and with tail-fin on dorsal side. Tail-tip rounded. Tail a little longer than snout-vent length (Adler & Zhao, 1990). Limbs long and well-developed; toes long; four fingers, five toes. Skin smooth. Upperparts uniform greenish-brown. Underparts grey (Thorn, 1969). Females are a little smaller than males. During the breeding season males have an Y-shaped cloaca, while females have a simple longitudinal fold. The tail-fin is higher in the male and the fore legs are longer than in the female. It is difficult to distinguish the sexes after the breeding season, when differences in cloacal fold and tail height are less clear. Maximum length 20 cm, on average 14-18 cm (Sasaki, 1924). There is variation in size among populations (Matsui et al., 1992).

Diagnosis Hynobius retardatus. Photo: Klaus-Detlef Kühnel. 86

Salamanders of the Old World | Hynobius

A large species with long and strongly flattened tail. Typically has 11 costal grooves. Series of vomerine teeth

short and in V-shape. Toes and fingers overlap when limbs adpressed.

Eggs and larvae

The female produces a pair of egg sacs measuring 5-6 cm, directly after spawning, which absorb water and may increase in size to 23 cm and a diameter of 3 cm. Egg diameter 3 mm (Sasaki, 1924; Thorn, 1969). Total clutch size may vary from 44-102 eggs (Sato, 1989). Most egg sacs are found in standing water ca. 3 cm below the water surface, but eggs may also be laid in streaming water (Sato, 1990). Eggs hatch after approximately three weeks, depending on temperature and amount of oxygen (Sasaki, 1924). Upon hatching larvae measure 13 mm and have balancers. Larvae are of standing water type. They have a relatively large head and look like frog tadpoles. The dorsal tail-fin reaches the middle of the back. Colour is dark brown and the tail-fins are more transparent (Thorn, 1969, 1986). Larvae may develop an extra wide mouth and head shape under certain conditions, such as at high densities (Nishihara, 1996). Gape determines the type and size of prey the larva can swallow. Large-headed larval morphs appear to eat more terrestrial invertebrates which have fallen into the water, whereas the small-headed larvae mainly feed on aquatic Diptera larvae (Kohmatsu, 2001a, 2001b). Metamorphosis takes place 40-50 days after hatching (Goris & Maeda, 2005). Normally this is from summer to early autumn at a length of 6-7 cm, but in cold regions at higher altitudes larvae may overwinter and reach a considerable size (Dunn, 1923 cites a specimen of 102 mm). Partial neoteny has been reported from Lake Kuttarush, some specimens reaching a length of 15 cm while retaining gills (Sasaki, 1924). Juveniles are dotted with small, gold-coloured flecks (Thorn, 1986). Experimental studies have shown that larvae grown at the relatively cold temperature of 15°C take significantly longer to reach metamorphosis and that their body size at metamorphosis was significantly larger compared with individuals grown at the relatively warm temperature of 20°C. On the other hand, food type, which is independent of water temperature, also affected the time to metamorphosis and body size at metamorphosis. Hynobius retardatus larvae feeding on conspecifics had a shorter larval period, indicating that cannibalism can incease the rate of development. This accelerated development led to smaller size at metamorphosis (Michimae, 2011).

Distribution

Hynobius retardatus is wide-spread on Hokkaido, Japan. Studies on population structure across the species’ range identified three genetically different groups, which did not overlap spatially (Azuma et al., 2013).

The range of Hynobius retardatus.

Habitat

This species occurs from lowland to alpine zones in forests and grassland. It breeds in lakes, marshes, ponds, pools, and ditches (IUCN, 2013), but also in streams. Egg sacs are attached to twigs, stones, logs, and foliage hanging in the water, and are also found on the bottom and in holes at the pond edge (Sato, 1989, 1990).

Behaviour

Animals emerge from hibernation as soon as the snow melts. Breeding takes place from April-May, (with water temperatures between 3-5°C (Sasaki, 1924) or 6-9°C (Sato, 1989), or as late as July at higher altitudes (Goris & Maeda, 2005). After the breeding season the adult salamanders live a hidden life on land, and often visit the water during non-breeding periods. They feed on insects and their larvae, crustaceans, centipedes, earthworms, and occasionally small fishes (Sasaki, 1924). In the breeding pond, males take position on a twig and become alert if they see a female moving nearby. The female grasps the twig on which the males are waiting and rubs her cloaca over it. The males now bring their snouts close to the female’s cloaca and the female elevates her tail, arching her body. Thereupon the nearest male clasps her pelvic region with his fore legs and the egg sacs begin to protrude from her cloaca. Immediately the male shifts his forelimbs to the egg sacs. The male pushes the female away with his hindlimbs, discharging seminal fluid onto the egg sacs. This action frees the egg sacs from the female’s cloaca. At this time other males rush to the spawning pair and try to fertilise the eggs themselves. The female falls to 87

a

e

h

b

f

i

c

g

j

d Reproductive behaviour sequence in the Hokkaido salamander (Hynobius retardatus). Figs A to F depict behaviour patterns before oviposition: A. Four males (non-shaded) grasp two twigs and one walks around the bottom of the tank; one gravid female (shaded) hides under a leaf. B. Males do not show any interest in the female’s behaviour until she begins to swim and walk actively. C. Males turn their heads towards her. The female grasps the twig which the males had been holding on to. D. Holding onto the twig, the female rubs her vent over it. E. Males approach the female and bring their snouts close to her vent. F. The female arches her body and raises her tail. The male holding the upper position on the twig embraces the female’s waist with his forelimbs, just before oviposition. Figs G to J depict behaviour patterns after oviposition: G. A male grasps the base of the egg sacs with his forelimbs and pushes the female’s vent away with his hindlimbs. H. Four males, except the one looking up from the bottom, begin to scramble for the egg sacs and simultaneously emit their sperm. I. The male looking up from the bottom suddenly begins to swim actively. Having deposited her egg sacs the female leaves the twig. J. The female hides under a leaf on the bottom again. Males grasp the twigs again and no longer pay attention to the egg sacs. Art: Bas Teunis, redrawn from Sato (1992).

88

Salamanders of the Old World | Hynobius

the bottom, remaining motionless for a while, while the males hold on to the egg sacs for some time, after which they take up positions on the twigs again (Sasaki, 1924; Sato, 1992). Males occupying a twig are reported to make repeated shivering, lateral body movements, with the body stiffening intermittently. The precise function of this movement, which is also reported for other species (Hynobius nebulosus, H. naevius), remains unclear, although it may signal excitement (Thorn, 1986; Sato, 1992).

Threats and conservation

This species is still relatively common in Hokkaido and is listed as of Least Concern (IUCN, 2013).

Observations in captivity

The species has been kept and bred in captivity by Thorn (1986) and Wallays (Pasmans et al., 2008). The terrarium should contain some land with numerous hiding places, and an area of water. Temperatures

should preferably not exceed 20°C. The adults should be kept in hibernation (0-6°C) for some months. Changing the water in spring stimulates breeding. Egg sacs should be removed from the tank as male salamanders may make a meal of them.

Comments

Hynobius retardatus differs from all other Hynobius species in that it has a diploid chromosome number of 40 instead of 56, and in that it has shorter vomerine tooth rows. These and several other differences led Adler & Zhao (1990) to propose a new genus Satobius for this species, but it has since been synonymised again with Hynobius. Hynobius retardatus is basal to the genus and sister to the clade holding all other Hynobius species (Weisrock et al., 2013).

References

Adler & Zhao (1990); Azuma et al. (2013); Dunn (1923); Goris & Maeda (2005); IUCN (2013); Komatsu (2001a, 2001b); Matsui et al. (1992); Michimae (2011); Nishihara (1996); Pasmans et al. (2008); Sasaki (1924); Sato (1989, 1990, 1992); Thorn (1969, 1986); Weisrock et al. (2013).

Hynobius sonani (Maki, 1922) | Yushan Salamander Description

A small- to medium-sized salamander. Tail shorter than snout-vent length. Head round, flattened; nostril equidistant between eye and tip of snout; distance between nares greater than between eyelids; eyelid longer than interorbital space. 12-13 costal grooves. Vomerine tooth row equals 4/5 width of tongue; inner rows intermediate between closetogether and well-separated. Fifth toe often reduced or absent (Maki, 1922; Dunn, 1923). Gular fold present. Large, round, black eyes. Paratoids large and flat. Tail cylindrical, slightly compressed toward the tip, which is blunt. Limbs rather short, fore- and hindlimbs do not touch when adpressed. Skin smooth.

Colour variable, pale whitish-yellow overall mottled with brown patches, sometimes forming brown transversal stripes on sides. Small yellow speckles over body and tail. Head is longer in females than in males; internarial distance is a little longer in males than in females; body width is slightly greater in males (Lai & Lue, 2008). Total length 10-12 cm (Lai & Lue, 2008).

Diagnosis

Short cylindrical tail compressed towards the tip. Long series of V-shaped vomerine teeth. When adpressed foreand hindlimbs do not touch. Fifth toe often reduced or absent.

Hynobius sonani, Taiwan. Photo: Yang In Shuen.

Often strong colour contrast between whitish-yellow and brown areas. Eggs and larvae The female produces a pair of string-like egg sacs, containing some 16 large eggs, 5 mm in diameter. Egg sacs are deposited in small, slow-moving bodies of water, under stones (Lee et al., 2006). The egg sac is transparent with a tough, weakly striated envelope. Colour of the eggs light yellowish-white with a green tint. Green fades as development 89

proceeds. At water temperatures of 7-9°C larvae hatch some three months after oviposition, at a total length of ca. 24 mm. They retain a large quantity of yolk and have no balancers (Kakegawa et al., 1989). It is not known whether larvae feed, or how long they take until metamorphosis.

Distribution

Hynobius sonani is restricted to the Central Mountain Range of Taiwan, at elevations from 2,600-3,100 m. It is partly sympatric with H. formosanus (between Mt. Hohuan and Mt. Bilu) (Lai & Lue, 2008; Chang, 2010).

Habitat

Like the other Taiwanese Hynobius species, Hynobius

night. Food consists mainly of insects (Coleoptera) and spiders (Araneae) (Lin et al., 2009). The breeding season ranges from November-January, when the rainfall is low, but may start as early as October (Kakegawa et al., 1989). There is no further information on breeding behaviour.

Threats and conservation

This species is very locally distributed and populations are small, making it vulnerable to habitat destruction and degradation due to development of infrastructure for tourism, like the other Taiwanese Hynobius species. Hynobius sonani and H. formosanus were first protected as precious and rare species under the Cultural Heritage Preservation Law in 1986, and later by the Wildlife Conservation Law (1989) (Lee et al., 2006). Hynobius sonani is considered Critically Endangered by Zhao (1998) and Endangered by Stuart et al. (2008) and IUCN (2013).

Observations in captivity

The species has been kept in the laboratory temporarily, where oviposition was induced (Kakegawa et al., 1989), but there are no further reports on captive H. sonani.

Comments

The range of Hynobius sonani.

sonani inhabits high-elevation montane areas, in woodlands, and broadleaf and coniferous forests, and in the transition zone between coniferous forests and alpine bamboo grasslands (Lai & Lue, 2008). These are areas with low temperatures, high annual precipitation, little disturbance, and high humidity. The animals spend most of their lives under logs and rocks near small, cool creeks and seepage areas with a moist substrate.

Behaviour

90

This species forages actively on the forest floor at

Salamanders of the Old World | Hynobius

Hynobiid salamanders reach the southern boundary of their distribution in Taiwan. The Taiwanese species of Hynobius are endemic to the island and their population sizes are extremely small (Lue et al., 1989). Five species are currently recognised, which are distinguished genetically and morphologically (Hynobius sonani, H. formosanus, H. arisanensis, H. fuca and H. glacialis). Morphological differences are however subtle and based on a combination of morphometric data, tooth count and colouration (Lai & Lue, 2008). Hynobius sonani clusters with other Taiwanese Hynobius species in a clade that is sister to all other Hynobius species, except H. retardatus, H. hirosei and H. kimurae (Zheng et al., 2012; Weisrock et al., 2013).

References

Chang (2010); Dunn (1923); IUCN (2013); Kakegawa et al.

(1989); Lai & Lue (2008); Lee et al. (2006); Lin et al. (2009); Lue et al. (1989); Maki (1922); Stuart et al. (2008); Weisrock et al. (2013); Zhao (1998); Zheng et al. (2012).

Hynobius stejnegeri Dunn, 1923 | Amber-coloured Salamander Description

A large Hynobius species. Head oval when viewed from above. Eyes prominent. Gular fold present. Robust, cylindrical body with 13-14 costal grooves. Tail a little shorter than trunk, thick but a little higher and more flattened than that of H. naevius. Tail-tip blunt. Limbs relatively long and robust. When adpressed fingers and toes do not meet. Four fingers, five toes. Skin smooth. Upperparts brownish-black with large, irregular ambercoloured blotches, that are brighter yellow on the flanks. Underside lighter brown, without blotches (Thorn, 1969; Goris & Maeda, 2005). Total length 13-15 cm, sometimes as large as 20 cm (Goris & Maeda, 2005).

Hynobius stejnegeri. Photo: Tim Johnson.

Diagnosis

A large salamander with amber-coloured blotches on upperside of body and tail. In body proportions similar to Hynobius naevius and H. boulengeri. Similar to H. kimurae in colour, but H. kimurae has only four toes, a longer series of vomerine teeth and a longer body (Dunn, 1923).

Eggs and larvae

Egg sacs are very long, from 17-30 cm, and lack the distinct whip-like structure on the free end as in Hynobius boulengeri. Clutch size is between 21-57 eggs (Nishikawa et al., 2008). Larvae are similar to those of H. naevius but a little more yellowish. Fingers and toes have black claws (Thorn, 1969). Larvae metamorphose in September-October, but many overwinter in the stream as larvae and emerge in spring-summer of the following year (Goris & Maeda, 2005).

Distribution

Hynobius stejnegeri occurs in Kyushu (Kumamoto, Miyazaki and Kagoshima Prefectures), Japan (IUCN, 2013).

Habitat

The range of Hynobius stejnegeri.

Behaviour

Japan, 2000) and Vulnerable (Stuart et al., 2008; IUCN, 2013).

This species inhabits montane broad-leaved, evergreen, and mixed forest. Breeding takes place near the headwaters of mountain streams, from February to mid-May. Interestingly, the female seems to remain near the egg sacs until the eggs hatch (Goris & Maeda, 2005). Hynobius stejnegeri is a loticbreeder. Little is known of its natural history.

Threats and conservation

The quality of this species’ habitat is deteriorating due to construction of roads and water pollution. The species is also harvested for medicine and food, and is considered Near Threatened (Environment Agency of

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Hynobius stejnegeri is genetically and morphometrically very similar to H. boulengeri from Kyushu. It is treated as a distinct species due to its unique colour pattern, the proportions of some body parts, and some distinct alleles (Nishikawa et al., 2005, 2007, 2008). According to Weisrock et al. 91

(2013), H. stejnegeri is basal to a group of Hynobius that includes the species from the Chinese mainland, the H. boulengeri group, the H. nebulosus group and the Korean species.

References

Dunn (1923); Environment Agency of Japan (2000);

Goris & Maeda (2005); IUCN (2013); Nishikawa et al. (2005, 2007, 2008); Stuart et al. (2008); Thorn (1969); Weisrock et al. (2013).

Hynobius takedai Matsui & Miyazaki, 1984 | Hokuriku Salamander developing into tail-fin in breeding males. Tip of tail-fin pointed. Four fingers, usually five toes. Vomerine teeth in two small, obliquely arched series, nearly touching at midline, and forming a shallow U- or V-shape. Upperparts uniformly dark brown or yellowish-brown, females with scattered dark spots. Underside paler, usually with bluishwhite mottling in females. Females and non-breeding males often with small bluish-white spots on sides and limbs. Sexual dimorphism consists of larger head in male, longer trunk in female. Tail is longer and higher in males than in females. Length 10-11 cm. Hynobius takedai. Photo: Tim Johnson.

Description

The following description is based entirely on Matsui & Miyazaki (1984). Head moderately depressed, distinctly longer than broad. Number of costal grooves 12-13, usually 12. Limbs short and stout. When adpressed limbs overlap by 1-2.5 costal grooves. Tail vertically oval at base, gradually flattening to middle part, and increasingly flattened to tip, which is obtusely pointed. Tail moderately keeled above and below, the upper keel originating at the level of the posterior end of vent,

Diagnosis

A small species. Differs from Hynobius nigrescens in its smaller body size, less depressed head, shorter tail and limbs, and transparent egg sacs. Differs from H. lichenatus in its shorter head and limbs, shorter and higher tail, more uniformly dark colour of back, larger clutch size, and in lacking obvious longitudinal striations on egg sacs. Differs from H. abei in having shorter and narrower head, longer limbs, and less keeled lower tail with a more pointed tip, in the presence of dark spots on some females, and in the absence of striations on the egg sac envelope.

Eggs and larvae

Clutch size and egg sacs very different from Hynobius lichenatus and H. abei. Clutch size on average 90 eggs (40 in H. lichenatus and 71 in H. abei). Longitudinal wrinkles on surface of egg sac are weak, whereas the other two species have strong longitudinal striations. The egg sacs are laid coiled around the base of reeds (Goris & Maeda, 2005).

Distribution

Hynobius takedai occurs on the Noto Peninsula of Ishikawa Prefecture and in the adjoining hilly country of Toyama Prefecture, Japan (IUCN, 2013).

Habitat Hynobius takedai. Photo: Hans-Joachim Herrmann. 92

Salamanders of the Old World | Hynobius

This species inhabits broad-leaved deciduous forests and conifer plantations in low hills. Both juveniles and adults live on land in the vicinity of ditches and temporary pools (IUCN, 2013; Goris & Maeda, 2005).

Behaviour

Breeding takes place from January-April in pools of water resulting from melting snow, at the edge of forested areas (Goris & Maeda, 2005). The males that arrive in the water first establish territories and fight off other males. These males are larger and have larger heads than non-territorial males which arrive later (Tanaka, 1986, 1987).

Threats and conservation

This species is threatened by water pollution, predation by introduced predators and destruction of its habitat and is considered Endangered (Environment Agency of Japan, 2000; IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Hynobius takedai is a sister species of H. nigrescens (Weisrock et al. 2013).

References

Environment Agency of Japan (2000); Goris & Maeda

(2005); IUCN (2013); Matsui & Miyazaki (1984); Tanaka (1986, 1987); Weisrock et al. (2013).

The range of Hynobius takedai.

Hynobius tokyoensis Tago, 1931 | Tokyo Salamander Description

Series of vomero-palatine teeth in U-shape and rather short. Trunk normally with 12 costal grooves. Limbs relatively short; when fore- and hindlimbs are adpressed, toes are separated by the space of about one costal groove. Four fingers and five toes (Thorn, 1969; Goris & Maeda, 2005). Ground colour varies from yellowish-brown to blackish-brown, with dark brown individuals predominating. Flanks, cheeks and limbs densely speckled with light blue flecks. On average breeding males are a little smaller than females (Kusano et al., 2006). Total length 8-13 cm (Goris & Maeda, 2005). There is considerable genetic variation in Hynobius tokyoensis. Two groups are recognised within the species, one from northeastern Kanto (Ibaraki) to southern Tohoku (Fukushima), and another from the remaining area south of northern Kanto (Tochigi) (Hayashi & Kusano, 2006; Matsui et al., 2007b). The populations from Aichi Prefecture of the Chubu district of Honshu, formerly considered to belong to H. tokyoensis, are now identified as H. nebulosus (Matsui et al., 2001).

Hynobius tokyoensis, males and egg sacs. Hinode Town, Nishitama Dist., Tokyo Metropolis. Photo: Satoshi Sakuma. 93

Diagnosis

Hynobius tokyoensis differs from H. nebulosus in having 12 costal grooves, while H. nebulosus usually has 13. It lacks the yellow edge to the upper and lower tail-fins, characteristic of H. nebulosus. Vomerine tooth series is U-shaped rather than V-shaped as in H. nebulosus. Hynobius tokyoensis lays eggs in a pair of hard, banana-shaped egg sacs, whereas the egg sacs of H. nubulosus are relatively soft, long and string-shaped (Matsui et al., 2001).

Eggs and larvae

The female lays two transparent bananashaped egg sacs, and attaches them to a twig, leaf or stem of grass. They contain a total of 15-192 eggs, larger females producing more and larger eggs per sac. Eggs measure 2.5-3 mm in diameter. There is considerable variation in egg and clutch sizes (Kusano, 1986; Goris & Maeda, 2005). Eggs may also be deposited in flowing streams in which case the egg sacs are attached to the underside of stones, in the hollows between the stone and the streambed (Ihara, 2002). Kusano (1986) found that this salamander produces a small clutch of large eggs under cool climatic conditions, and a large clutch of small eggs under warm conditions. Eggs hatch by the beginning of May. Larvae that cannibalise other larvae grow faster than those that do not. Metamorphosed

juveniles scatter widely in the forested areas around the breeding site, as do the adults after the breeding season (Goris & Maeda, 2005). Sexual maturity is reached after 4-6 years, in males a little sooner than in females. The oldest male ever found was 21 years (Kusano et al., 2006).

Distribution

This species occurs along the Pacific coast of Fukushima Prefecture and throughout the Kanto District, Honshu, Japan, reaching 300 m altitude (Goris & Maeda, 2005; Stuart et al., 2008).

Habitat

This species occurs in forests from coastal areas to the hills. It breeds in paddy fields, ditches and springs, as well as in small mountain streams, for instance in the Yamanaka District of Miura Peninsula (Ihara, 2002).

Behaviour

The adults are mainly nocturnal, spending their lives in underground tunnels dug by earthworms, moles, mice, and beetle larvae. Hynobius tokyoensis is strictly terrestrial outside the breeding season. It feeds on earthworms, spiders and other arthropods living in the forest litter. Observations in winter indicate that in coastal areas they continue to feed throughout the year (Ihara, 2013). In warm parts of its range, such as the Boso Peninsula, reproduction starts in December-January at water temperatures of 3-5°C, while in colder parts, such as the outskirts of Tokyo, egg sacs do not begin to appear until February. Breeding activity continues for about two months.

The range of Hynobius tokyoensis.

94

Salamanders of the Old World | Hynobius

Hynobius tokyoensis, breeding assemblage, Hinode Town, Nishitama Dist., Tokyo Metropolis. Photo: Satoshi Sakuma.

Males arrive at the breeding site first and select suitable spots for egg laying, which are then defended aggressively against other males. Males cluster in small groups, attracting females by tail waving movements. After a female has made her choice of a particular cluster of males she deposits her eggs. The males grasp the egg sacs and scramble for access to the eggs, each trying to fertilise as many eggs as possible (Goris & Maeda, 2005). In mountain stream habitats single males were frequently found occupying suitable hollows under large stones, most probably defending these potential egg laying spots against other males. Males normally remain in the water for 2-3 weeks (Ihara, 2002, 2013; Kusano, 1980).

Threats and conservation

This species is threatened by habitat loss due to infrastructure development, water pollution, invasive species, drying out of its habitat, and collection

for the pet trade (Stuart et al., 2008). The population around Tokyo is nearing extinction due to habitat destruction (Environment Agency of Japan, 2000). The species is considered Vulnerable (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

Hynobius tokyoensis has been bred in captivity by Henk Wallays (Belgium, 2005) (Raffaëlli, 2007).

Comments

Hynobius tokyoensis is sister to H. lichenatus (Weisrock et al., 2013)

References

Environment Agency of Japan (2000); Goris & Maeda

(2005); Ihara (2002, 2013); IUCN (2013); Kusano (1980, 1986); Kusano et al. (1986); Matsui et al. (2001); Matsui et al. (2007b); Raffaëlli (2007); Stuart et al. (2008); Thorn (1969); Weisrock et al. (2013).

Hynobius tsuensis Abé, 1922 | Tsushima Salamander Description

Similar to Hynobius nebulosus, but with a slightly more slender body and larger in size (Thorn, 1969). 13-14 costal grooves; 1-3 costal grooves between adpressed toes. Tail shorter than or as long as body, cylindrical at base, flattened at tip (Dunn, 1923). Four fingers and five toes. There is sexual dimorphism in colour. Females are dotted with dark brown spots on a yellowish background. Males have purplish spots on a blackish background. The underside of both sexes is lighter in colour, and both sexes have an orange stripe on the upper and lower edges of the tail. The stripe tends to be wider in females (Goris & Maeda, 2005). Total length 11-14 cm (Goris & Maeda, 2005).

Hynobius tsuensis. Photo: Hans-Joachim Herrmann.

Diagnosis

This salamander has a slightly flattened tail; 13 costal grooves; dorsal and ventral edges of tail often yellow as in Hynobius nebulosus.

Eggs and larvae

The female produces a pair of bananashaped egg sacs, containing 25-75 eggs in total, the eggs measuring ca. 3 mm (Goris & Maeda, 2005). Egg sacs are attached to the underside of stones etc., in streams. A high percentage of the eggs, sometimes more than 40%, may be unfertilised (Kuramoto, 1972). Some larvae metamorphose before autumn, but a large proportion overwinter as larvae (Goris & Maeda, 2005).

Distribution

This species only occurs on Tsushima Island, Japan (IUCN, 2013).

Hynobius tsuensis. Photo: Henk Wallays.

95

Behaviour

The natural history of this species is poorly known. It is thought that adults return to the breeding sites in late autumn and early winter, where they overwinter in preparation for the next breeding season (Goris & Maeda, 2005). The breeding season is from February-April (Kuramoto, 1972).

Threats and conservation

This species’ habitat is not under significant threat (IUCN, 2013).

Observations in captivity

The species has been kept in captivity by Henk Wallays (Raffaëlli, 2007).

Comments

The range of Hynobius tsuensis.

Habitat

This species inhabits both mountains and lowlands but is a strictly lotic-breeder (Kim et al., 2007; Matsui et al., 2006).

Despite its close genetic similarity to lentic Hynobius nebulosus populations from Kyushu, and to H. yangi from Korea, H. tsuensis is a purely lotic-breeder with strongly modified egg sacs, unlike the other two species. The steep, montane environments of Tsushima probably forced the ancestral populations to acquire the habit of breeding in flowing water (Kim et al., 2007). According to Weisrock et al. (2013), H. tsuensis is sister to a clade containing H. dunni and H. nebulosus.

References

Dunn (1923); Goris & Maeda (2005); IUCN (2013);

Kim et al. (2007); Kuramoto (1972); Matsui et al. (2006); Raffaëlli (2007); Thorn (1969); Weisrock et al. (2013).

Hynobius turkestanicus Nikolskii, 1910 | Turkestan Salamander Description

All of the collected specimens of Hynobius turkestanicus seem to have been lost. However, based on the description of the holotype, H. turkestanicus seems to be a valid species and not an abnormal individual of any other continental hynobiid species with V-shaped rows of vomerine teeth (Kuzmin, 1999). The following account is an abbreviated rendering of the description by Nikolskii, as given by Kuzmin (1999).

the head. Second, less distinct gular fold between mouth angles. Deep longitudinal groove on side of head from lateral part of gular fold towards snout, ending well behind the eye. Dorsal colouration reddish-brown with small dark brown spots. Flanks and belly yellowish-brown without spots. Total length 9 cm.

Head compressed, longer than broad. Snout rounded, the length equaling interorbital width. Vomerine tooth rows not broader than long. Eyes prominent. Labial folds absent. Body cylindrical, scarcely compressed. Head length 4.5 times snout-vent length. Fingers and toes not touching when adpressed. Fingers and toes long. Tail as long as the distance from gular fold to cloaca. Tail keeled above and below, except on first quarter of tail. Tail-tip tapers to a point. Cloaca a longitudinal slit, without transverse groove, the edges quite swollen. Skin smooth. Deep mid-dorsal groove forking on rear of the skull, longitudinal groove on forepart of the skull. 14 costal grooves, reaching the belly. Paratoids large, flattened, on sides of head behind mouth angles. Gular fold well-developed and extending onto sides of 96

Salamanders of the Old World | Hynobius

Diagnosis

A small hynobiid salamander with 14 costal grooves and V-shaped vomerine teeth. Head relatively short. Five toes.

Eggs and larvae

The larvae in the collection of Nikolskii once attributed to Hynobius turkestanicus, appeared to be Triturus cristatus larvae (Kuzmin, 1999).

Distribution

The type locality is unknown. The female specimen on which Nikolskii based his description was collected ‘between Samarkand and Pamir’ or, according to Kuzmin, in all probability Uzbekistan and Tajikistan.

Habitat

Unknown, but probably as for other Hynobius species, in wet habitats near mountain brooks or semi-flowing waters (Kuzmin, 999).

Threats and conservation

The species has not been found since its description in 1910 and may be extinct.

Comments

There have been doubts about the validity of

H. turkestanicus. All of the specimens have been lost and, in spite of special searches for this species, it has never been found after 1910. Given the description of the holotype and comparison with Salamandrella keyserlingii, it seems likely that H. turkestanicus is not identical to the latter species, with which it might be confused (see discussion in Kuzmin, 1999).

References

Kuzmin (1999).

Hynobius yangi Kim, Min & Matsui 2003 | Kori Salamander Description

A small salamander, related to Hynobius leechii and H. quelpaertensis. Identified earlier as a taxon different from H. leechii (Yang et al., 1997), but only recently described as a separate species on the basis of genetic and morphological analyses (Kim et al., 2003). The following summary is based on this description. Head longer than broad, longer in males than in females. Females with relatively longer trunk than males. 12-14 costal grooves. Limbs short, and when adpressed, mostly do not overlap. Colour olive to light brown above, usually without dark speckles. Underside of body lighter. Separation between toes and fingers is greater in females than in males. Males have longer and higher tails than females. Total length 10-12 cm.

Hynobius yangi, holotype. Photo: Jong-Bum Kim, Mi-Sook Min & Masafumi Matsui.

Diagnosis

Most similar to H. leechii, but distinguished from it by longer and higher tail, greater separation of adpressed limbs, slightly deeper vomerine tooth series, egg sacs coiled, a light brown dorsum, and distinct genetic differences. It has a smaller snout-vent length, relatively longer head, higher tail and shorter trunk, and more costal grooves than H. quelpaertensis from Cheju. Hynobius yangi can be differentiated from H. quelpaertensis from peripheral islands by a relatively longer and higher tail and wider head, and by having more costal grooves and narrower separation of limbs (Kim et al., 2003).

Eggs and larvae

The female produces a pair of egg sacs, which take on a spiral shape, attached to water plants or branches in standing water. The clutch of a single female contained 86 eggs, each ca. 2.7-2.8 mm in diameter (Kim et al., 2003). Larval development is probably similar to that of H. leechii and H. quelpaertensis. Hynobius yangi males and females

The range of Hynobius yangi.

97

become sexually mature at 2-3 years of age, respectively. Both sexes commonly attain a maximum age of 11 years (Lee et al., 2010).

Distribution

This species occurs in clusters around the type locality Hyoam-ri and nearby Gilcheon-ri, both in Jangan-eup, Busan-shi in southeastern South Korea (Kim et al., 2003; Kim, 2009).

Habitat

This species inhabits a river basin, isolated from the other two Hynobius species. It breeds in still waters in ditches and can be considered a lentic-breeder (Kim et al., 2003).

Behaviour

Breeding occurs from late February-late March (Kim et al., 2003). There are no published data on the behaviour of Hynobius yangi, but on-going work at Kangwon National University suggests that its reproductive ecology and mating

behaviour is generally similar to that of H. leechii and H. quelpaertensis (cf. Park et al., 1996).

Threats and conservation

Given its limited range and isolated occurrence, this species must be vulnerable to habitat destruction (Kim et al., 2003). It is listed as Endangered (IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

According to Weisrock et al. (2013), the Korean Hynobius species are monophyletic and H. quelpaertensis is sister to a clade containing H. leechii and H. yangi.

References

IUCN (2013); Kim (2009); Kim et al. (2003); Lee et al.

(2010); Park et al. (1996); Weisrock et al. (2013); Yang et al. (1997).

Hynobius yatsui Oyama, 1947 | Small Blotched Salamander Description

This description is a summary of the description by Tominaga & Matsui (2008). A small salamander belonging to the Hynobius naevius group. Body slender. Head moderately depressed, distinctly longer than broad. 13 costal grooves. Limbs short and stout. Fore- and hindlimbs separated by two costal folds when adpressed. Tail shorter than trunk, vertically oval at base and middle, not keeled, gradually flattened to round tip. Fifth toe very short. Vomerine teeth in two small, obliquely arched series, nearly touching at midline, forming a very deep V-shape. Upperparts reddish-purple with discontinuous brownish-white markings or white dots. Generally the tail is darker with larger markings than on trunk. Ventral ground colour is light grey to light reddish-purple, with relatively small, white markings. Slight sexual dimorphism in body proportions. Males have relatively larger head and longer limbs and tail, while females have a longer trunk. This species exhibits considerable genetic variation (Sakamoto et al., 2009). Total length 9-10 cm.

Diagnosis

Most similar to Hynobius naevius in appearance, but with a smaller body, relatively narrower head, shorter trunk, more cylindrical and shorter tail, relatively longer vomerine tooth series, mottled dorsum, and considerable molecular differences.

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Hynobius yatsui, Nara Pref. Photo: Kanto Nishikawa.

Eggs and larvae

Very few, un-pigmented ova per clutch. Egg sacs are laid in very small, underground streams, where the larvae hatch and metamorphose without feeding. Clutch size varies from 7-19 eggs and egg diameter varies from 4.6-5.0 mm (Tominaga & Matsui, 2008; see also Yoshikawa & Watabe, 2009).

Distribution

This species occurs in the western part of Japan: Chubu District (Gifu and Aichi Prefectures), Kinki District except for Kyoto and Hyogo Prefectures, Shikoku District, and Kyushu District except for Saga and Nagasaki

Behaviour

Hynobius yatsui lives largely underground and its eggs and larvae are rarely found (Yoshikawa & Watabe, 2009). Its natural history is poorly understood. It occurs syntopically with various other species in various localities (including H. naevius, H. kimurae, H. stejnegeri, H. boulengeri). In all these coexisting species, body sizes are larger than in H. yatsui, and oviposition and larval growth occur in relatively wider, more open montane streams (Tominaga & Matsui, 2008).

Threats and conservation

This species is presently not considered threatened and is listed as of Least Concern (IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

The range of Hynobius yatsui.

Prefectures. Its altitudinal range varies between 200-1,800 m (Tominaga & Matsui, 2008; IUCN, 2013).

Habitat

This species inhabits montane forests near the headwaters of streams (IUCN, 2013).

Hynobius naevius was found to comprise two distinct groups, one of larger size, the other one smaller. Comparisons between the type series and specimens of both groups indicated that the type series is most similar to the group of larger animals from Mt. Tara-dake in NW Kyushu, suggesting that the type locality is in that region (Tominaga & Matsui, 2007). The animals belonging to the second group represent a cryptic species, associated to the subspecies H. naevius yatsui, now elevated to full species rank, H. yatsui (Tominaga & Matsui, 2008).

References

IUCN, (2013); Sakamoto et al. (2005, 2009); Tominaga &

Matsui (2007, 2008); Yoshikawa & Watabe (2009).

Hynobius yiwuensis Cai, 1985 | Yiwu Salamander Description

This is based on the original description by Cai (1985). Similar to Hynobius chinensis but less stout. Length of inner branch of vomerine teeth longer than that of H. chinensis. Head oval-shaped with a V-shaped groove, longer than broad. Labial fold absent. Gular fold prominent. 10 costal grooves, occasionally 11. Tips of limbs usually do not touch when adpressed. Tubercles present on palms and soles. Tail shorter than snout-vent length, compressed; males with an obvious tail-fin fold. Dorsal caudal fin continues from tail-base to tail-tip; ventral caudal fin is present at the posterior two thirds of the tail. During breeding season colour changes from dark brown to lighter brown and greenish. Underparts off-white, greyish without speckles (Fei et al., 2006). Total length of 83-136 mm in males and 87-117 mm in females.

Hynobius yiwuensis, captive specimen, Ruiyansi Forest Park, Zhejiang. Photo: Max Sparreboom. 99

Hynobius yiwuensis, captive specimens, Ruiyansi Forest Park, Zhejiang. Photo: Max Sparreboom.

Diagnosis

A stocky salamander usually with 10 costal grooves. The body of Hynobius yiwuensis is smaller compared with H. chinensis and H. amjiensis. Tail length about 60-75% of snout-vent length. Hynobius chinensis has shorter vomerine teeth, 11-12 costal grooves and caudal fins are nearly absent (Fei et al., 2006).

The remnants of the yolk sac were used up after about 10 days (Zhang & Tang, 1987; Fei et al., 2006). Zhang & Tang (1987) provide a table for their embryonic development. In mid-January, with water temperatures between 8-10°C, eggs take about 40 days to hatch, and metamorphosis is completed after 3.5-4 months (Fei et al., 2006). Pope described and depicted Hynobius

Hynobius yiwuensis, female, Xiangshan County, Ningbo City, Zhejiang. Photo: Hou Mian, courtesy Zeng Xiaomao.

Hynobius yiwuensis, juvenile in captivity, Ruiyansi Forest Park, Zhejiang. Photo: Max Sparreboom.

Eggs and larvae

Descriptions of eggs and larvae are derived from descriptions originally given for Hynobius chinensis from Fujian and Zhejiang. Salamanders from these provinces are now considered to belong to H. yiwuensis (Pope, 1931; Chang, 1968; Zhang & Tang, 1987). Zhang & Tang described eggs, larvae and adults from Huantan, Xiaoshan County in Zhejiang Province, China, collected in February 1981. A pair of egg sacs was attached to stems of aquatic plants. The egg sac had a thick anterior part and a thinner caudal end, about 15-17 cm long, containing 33-64 eggs. Egg diameter 2.5-3 mm. On hatching, larvae measured about 15 mm, had a pair of balancers, still contained some yolk, and were almost translucent.

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Salamanders of the Old World | Hynobius

larvae at an advanced stage of development from the Guadun region, Fujian Province. The dorsal fin extended forward past the middle of the back. Body and tail were spotted with grey, the spots being most profuse on the tail-fins where they often tended to run together. The head was uniformly grey and the external gills sparsely speckled with the same colour. Maximum size 62 mm. Larvae were found in May 1926 in pools in a bamboo grove. First metamorphosed juveniles can be found in July (Pope, 1931) or earlier, from May onward (Fei et al., 2006). The colour of recently metamorphosed individuals is dark greyish-black, densely speckled with small bluish spots (pers. obs.).

The range of Hynobius yiwuensis.

Distribution

This species occurs in Zhejiang Province, China (Zhenghai, Yiwu, Wenling, Jiangshan, Xiaoshan and Zhoushan) (Fei et al., 2006; IUCN, 2013).

Habitat

This species inhabits forests and arable fields in hilly areas, at elevations of 50-200 m. It breeds in pools and small streams (Stuart et al., 2008; IUCN, 2013). Outside the breeding season Hynobius yiwuensis is a terrestrial species, that can be found under stones, logs and rotting leaves in loose and moist soil.

Behaviour

Hynobius yiwuensis feeds on small invertebrates such as earthworms, centipedes and millipedes. With the onset of the breeding season in October, adult salamanders move to ponds, puddles and streams. Spawning is from mid-December to February at temperatures around 0°C, or to May in the Zhoushan islands. After reproduction the adults leave the water (Zhang & Tang, 1987; Fei et al., 2006).

Threats and conservation

Major threats are habitat loss due to clear-cutting and water pollution. The species is considered to be Vulnerable (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

One adult and some juveniles and larvae, collected from Ruiyansi Forest Park, Zhejiang Province in April 1999, were kept and reared in captivity by Max Sparreboom until the end of March 2003. Temperatures were usually kept below 20°C. Larvae metamorphosed at lengths from 4.5-6 cm. Juveniles were entirely covered with bluish speckles and gradually lost the juvenile colouration after two

Hynobius yiwuensis, habitat, Ruiyansi Forest Park, Zhejiang. Photo: Max Sparreboom.

years. The species appears to be sensitive as several individuals died in captivity.

Comments

Adler & Zhao (1990) examined the type specimens of Hynobius chinensis and H. yiwuensis and did not find sufficient differences to warrant species status for H. yiwuensis. However, Fei et al. (1999, 2006) and Fu et al. (2003b) disagree and accept both species. Most other authors also assume that H. amjiensis (with one locality in Zhejiang) and H. yiwuensis (with a wider range in Zhejiang and Fujian Provinces) are separate species and differ from H. chinensis from Hubei. They show considerable genetic divergence and are geographically isolated 101

from all other hynobiid salamanders (Fu et al., 2003b). Xia et al. (2012) consider H. yiwuensis to be sister to the clade that contains the other Chinese mainland Hynobius species H. amjiensis, H. chinensis, H. guabangshanensis and H. maoershanensis). Weisrock et al. (2013) consider H. chinensis and H. yiwuensis (termed H. chinensis 1 from Zhoushan Island) to be sister species, and H. amjiensis to be their closest relative. According to the arrangement proposed by Zheng et al. (2012), H. yiwuensis

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is the sister taxon to H. amjiensis, and this clade is sister to a clade containing the three other mainland Chinese Hynobius species.

References

Adler & Zhao (1990); Cai (1985); Chang (1936); Fei et al. (1999, 2006); Fu et al. (2003b); IUCN (2013); Pope (1931); Stuart et al. (2008); Xia et al. (2012); Zhang & Tang (1987); Zheng et al. (2012).

Liua Zhao & Hu, 1983 This genus comprises two species which are morphologically and ecologically distinct. Liua shihi lives in water all year round, while L. tsinpaensis is only found in water during the breeding season. Liua shihi exhibits several characters associated with an aquatic lifestyle, such as a labial fold and laterally compressed tail. These features are absent in L. tsinpaensis (Zeng et al., 2006). The more terrestrial L. tsinpaensis was referred to Ranodon in its original description. The genus Liua was at first considered monotypic and its diagnosis included the typical aquatic lifestyle characters of L. shihi (Zhao & Hu, 1983; Zhao, 1994). But because tsinpaensis is now included in Liua on the basis of its close genetic relationship to L. shihi, the genus description is no longer adequate. The taxonomy of Ranodon-Liua-Pseudohynobius has long been problematic. Huang et al. (1993) and Fei et al. (2006) do not accept Liua as a separate genus, and place L. tsinpaensis in Pseudohynobius, and L. shihi in Ranodon.

Molecular analysis has shown that the Liua-Pseudohynobius species complex can be divided into two groups, the genus Liua including L. shihi and L. tsinpaensis, and the genus Pseudohynobius (Zeng et al., 2006; Wei et al., 2009). Species now included in the genera Liua and Pseudohynobius are more closely related to mountain stream salamanders of the genus Batrachuperus than to Ranodon (discussion in Zeng et al., 2006 and an overview of the taxonomic implications in Frost, 2013). Liua occurs north and Pseudohynobius south of the Yangtze River.

Liua shihi (Liu, 1950) Liua tsinpaensis (Liu & Hu, 1966)

References

Fei et al. (2006); Frost (2013); Huang et al. (1993);

Wei et al. (2009); Zeng et al. (2006); Zhao (1994); Zhao & Hu (1983).

Liua shihi (Liu, 1950) | Wushan Salamander Description

A robust salamander. Head broad; upper jaw margin flat, rounded and broad. Labial fold present. A long groove extending from posterior angle of eye to temporal area. Tongue elongated and only slightly free at edges. Body cylindrical in shape. 9-11, usually 11, costal grooves. Tail approximately

48% of total length. High caudal fin present. Tail-tip rounded. Four fingers, five toes, flattened. Fingers and toes overlap when limbs are adpressed; in some specimens they just meet or are separated (Fei et al., 2006). Horny brown coverings on palms and soles; finger and toe-tips almost black. Skin smooth.

Liua shihi, Shennongjia, Hubei. Photo: Kevin Messenger. 103

Dorsal colouration yellow-green to olive-brown, dotted with large, light brown patches; ventral side light whitish, sometimes with dark spots (Fei et al., 2006). Males a little larger than females, with a slightly longer tail and head. Cloaca consists of a longitudinal fold; in males a transversal fold in front of cloacal fold (Liu et al., 1960).

found in early spring, indicating that larvae may not reach metamorphosis until at least one year of age (Zhao & Hu, 1983; Liu et al., 1960; Kuzmin & Thiesmeier, 2001; Fei et al., 2006).

Distribution

This species occurs in central China, including southern Henan, southern Shaanxi, eastern Sichuan, north-western Hunan and Hubei Provinces (Kuzmin & Thiesmeier, 2001; IUCN, 2013).

Total length 151-200 mm in males, 133-162 mm in females (Fei et al., 2006)

Diagnosis

A robust salamander. Labial fold well-developed and present all year round. Brown cornified coverings on palms and soles. Vomerine tooth rows in two separated series at an acute or right angle, beginning at level of middle of choanae and extending forward far beyond it (Liu et al., 1960; Zhao & Hu, 1983, 1988b; Zhao, 1994).

Eggs and larvae

The paired egg sacs are coiled in a C-shape, the distal end tapering. The egg sacs are more rounded than in Liua tsinpaensis. Length 65-165 mm, 6-25 eggs per egg sac. Eggs are milk-white in colour and 7 mm in diameter (Liu et al., 1960; Kuzmin & Thiesmeier, 2001). Egg sacs are deposited in streams on the under-surface of stones. Several clutches may be found under one stone. Average size of recently hatched larvae is as large as 25 mm. The newly hatched larvae have three fingers and clearly visible hind leg buds; gills are relatively long; balancers are absent; fin folds are well-developed. They are brownish with small dark spots on the dorsal side and whitish-yellow on ventral side; tail-tip has darker colouration. Larvae grow to about 10 cm before metamorphosis. Large larvae have been The range of Liua shihi.

Habitat

This species inhabits small, low-gradient streams in forested areas at altitudes between 900-2,350 m (Stuart et al., 2008; IUCN, 2013). It is found under stones and in crevices between stones along the streams. In Wushan County, Sichuan, the species is most numerous in mountain brooks at 1,310-1,680 m altitude (Liu et al., 1960). In Shaanxi it is found at 1,950 m altitude in streams with a water temperature of 10-20°C (Song, 1984).

Behaviour

Liua shihi, larva nearing metamorphosis, Shennongjia, Hubei. Photo: Kevin Messenger. 104

Salamanders of the Old World | Liua

Liua shihi feeds on small aquatic and terrestrial invertebrates and their larvae. Larvae of caddisflies and stoneflies have been found in their stomachs (Song, 1984). The breeding season is from the end of March to the beginning of April (Fei et al., 2006), but reproductive behaviour has not been observed. Larvae hatch and leave the egg sacs in June, when water temperatures range from 13-19°C (Liu et al., 1960).

Threats and conservation

This species is still common within its range. Over-exploitation for human consumption and destruction and degradation of its mountain brook habitat pose the greatest threats. The species is considered to be Near Threatened (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

This species has been kept in captivity by Fleck (2010c, 2013a), who kept some animals, obtained from the pet trade, in tanks with flowing water, at water temperatures from 10-12°C in winter and up to 20°C in summer. Higher temperatures were tolerated temporarily. Males grew to 22-25 cm length; their tail length being longer than snout-vent length. Males had broader heads and more muscular forelimbs than females. Captive breeding has not yet been reported.

Comments

Liua shihi has been variously placed in Hynobius, Ranodon, or Liua (Zhao, 1994; Kuzmin & Thiesmeier, 2001; Fei et al., 2006). Molecular analysis has shown that the Liua-Pseudohynobius species complex can be divided into two groups, the genus Liua including Liua shihi and L. tsinpaensis, and the genus Pseudohynobius. Genetically, the two Liua species are more closely related to Batrachuperus than to Ranodon (Zeng et al., 2006). According to Xia et al. (2012), the two Liua species are most closely related to Paradactylodon, according to Weisrock et al. (2013) to Pseudohynobius.

References

Fei et al. (2006); Fleck (2010c, 2013a); IUCN (2013);

Kuzmin & Thiesmeier (2001); Liu et al. (1960); Song (1984); Stuart et al. (2008); Weisrock et al. (2013); Xia et al. (2012); Zeng et al. (2006); Zhao (1994); Zhao & Hu (1983, 1988b).

Liua shihi, habitat, Shennongjia, Hubei. Photo: Kevin Messenger.

Liua tsinpaensis (Liu & Hu, 1966) | Tsinpa Salamander Description

Head round and flat, of equal length and width. Longitudinal groove from posterior part of the eye to occipital region. Labial fold absent. Vomerine teeth arranged in two relatively short, widely separated series between internal nares, with 7-10 teeth in each row. Body cylindrical; 13 costal grooves. Tips of toes and fingers touch when limbs are adpressed. Four fingers, five toes. No cornified coverings on palms and soles, only tips of digits being slightly cornified. Tubercles present on palms and soles but inconspicuous. Tail thick and flattened, of equal length or a little longer than snout-vent length. Dorsal tail-fin thick and starting from tail-base, ventral tail-fin fold only noticeable at tip of the tail (Ye et al., 1993; Fei & Ye, 2001; Kuzmin & Thiesmeier, 2001).

Liua tsinpaensis, Zhouzhi, Shaanxi. Photo: Fei Liang. 105

colour. Larvae have a light brown head and dorsum, with black blotches. Black patches of various sizes on tail-fin fold. Flanks silvery-white, belly completely white. Limbs are light brown. Toes and fingers are black at the tips. Metamorphosis starts when the larvae have reached a length of 60 mm (Fei & Ye, 2001; Kuzmin & Thiesmeier, 2001).

Distribution

This species is restricted to southern Shaanxi (Zhouzhi and Ningshaan Counties) and northeastern Sichuan (Wanyuan County), China (Stuart et al., 2008; IUCN, 2013).

Habitat

This species inhabits small hill streams and riparian habitats, usually in forested areas at altitudes from 1,600-1,860 m (Stuart et al., 2008; IUCN, 2013).

Behaviour

During the day Liua tsinpaensis hides under rocks near mountain streams. It breeds in the mouth of springs. Reproduction takes place in May and June (Fei & Ye, 2001). The reproductive behaviour has not been observed. Outside the breeding period L. tsinpaensis leads a semi-aquatic life. The salamanders often leave the stream sides to forage (Kuzmin & Thiesmeier, 2001).

The range of Liua tsinpaensis.

Threats and conservation

Colour of dorsal side an irregular cloud-like pattern of gold and dark brown. Tail yellowish above. Brown ventral side sporadically marked with tiny white dots (Fei & Ye, 2001; Fei et al., 2010).

Observations in captivity

This species is rare and is known from only three localities. It is threatened by collection for human consumption and medicine as well as habitat loss and degradation due to increased agricultural activities. It is listed as Vulnerable (Stuart et al., 2008; IUCN, 2013). There are no reports of this

species being kept in captivity. Males differ from females in having a broader head, a higher tail with thicker base and a smaller distance between fore- and hindlimbs. Total length 119-142 mm in males, 125-136 mm in females (Fei et al., 2006).

Diagnosis

Smaller in size than Liua shihi. No labial fold, no cornified coverings on palms and soles, not an exclusively aquatic species (Kuzmin & Thiesmeier, 2001).

Eggs and larvae

The paired egg sacs are coiled in a C-shape, the distal end tapering. The egg sacs are less rounded than in Liua shihi. Length 122-195 mm, with 6-11 eggs in each egg sac, and 13-20 in total. Eggs are oval, 5 mm in diameter and light grey in

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Comments

Liua tsinpaensis has been variously placed in Ranodon, Pseudohynobius or Liua (Fei & Ye, 1983c; Zhao, 1994; Kuzmin & Thiesmeier, 2001). Molecular analysis has shown that the Liua-Pseudohynobius species complex can be divided into two groups, the genus Liua including Liua shihi and L. tsinpaensis, and the genus Pseudohynobius. Genetically, the two Liua species are more closely related to Batrachuperus than to Ranodon (Zeng et al., 2006). According to Xia et al. (2012), the two Liua species are most closely related to Paradactylodon, according to Weisrock et al. (2013) to Pseudohynobius.

References

Fei & Ye (1983c, 2001); Fei et al. (2006, 2010); IUCN (2013);

Kuzmin & Thiesmeier (2001); Stuart et al. (2008); Weisrock et al. (2013); Xia et al. (2012); Ye et al. (1993); Zeng et al. (2006); Zhao (1994).

Onychodactylus Tschudi, 1838 The genus Onychodactylus forms a group of closely related, specialised stream-dwelling species, endemic to north-eastern Asia. They are slender salamanders, with a long tail, cylindrical at the base and more compressed at the end. Lungs are absent. Five toes, with distinct blackish cornified claws in adults and developed larvae. The tongue is large and subcircular, free on the sides. Large premaxillary fontanelle. Vomerine teeth in a two-archshaped continuous series. The female lays a pair of short gelatinous egg sacs. Unique among salamanders is a distinct sexual character, consisting of a hypertrophied lateral fold on the posterior surface of the male hind legs, extending from the fifth toe to the tibia. This feature, which effectively increases the surface of the hind legs, is most prominent during the reproductive period. Larvae have a square-shaped head with obtusely blunted snout, which is wider than the body; short gills covered with an opercular skin fold at the base; slightly prominent eyes; all digits bearing black, cone-shaped sharp, horny claws. Characteristic dermal flap develops on outer surfaces of the limbs, and disappears prior to metamorphosis. Dorsal and ventral tail-fins are low. The ground colour in larvae is usually light brownish, ochre, sometimes slightly reddish-brown or orange. With age dark pigment develops as indistinct, clouded or variegated patterns on back and tail, and light areas on the dorsum and tail become brighter (Poyarkov et al., 2012).

The genus Onychodactylus is the most basal lineage within the Hynobiidae and sister taxon to the remaining extant Hynobiidae (Zhang et al., 2006; Zheng et al., 2012; Pyron & Wiens, 2011). Traditionally thought to comprise two species, O. japonicus and O. fischeri, molecular and allozymic work has demonstrated the presence of extensive genetic divergence within the genus, suggesting the existence of several cryptic species (Yoshikawa et al., 2008, 2010a, 2010b, 2012; Poyarkov et al., 2012). At present, eight species are recognised; their descriptions are based on molecular and morphological data.

Onychodactylus fischeri (Boulenger, 1886) Onychodactylus japonicus (Houttuyn, 1782) Onychodactylus kinneburi Yoshikawa, Matsui, Tanabe & Okayama, 2013

Onychodactylus koreanus Min, Poyarkov, & Vieites, 2012 Onychodactylus nipponoborealis Kuro-o, Poyarkov & Vieites, 2012 Onychodactylus tsukubaensis Yoshikawa & Matsui, 2013 Onychodactylus zhangyapingi Che, Poyarkov, Li & Yan, 2012 Onychodactylus zhaoermii Che, Poyarkov & Yan, 2012

References

Poyarkov et al. (2012); Pyron & Wiens (2011); Yoshikawa

et al. (2008, 2010a, 2010b, 2012); Zhang et al. (2006); Zheng et al. (2012).

Onychodactylus fischeri (Boulenger, 1886) | Russian Clawed Salamander Description

Onychodactylus fischeri is a slender, elongate salamander. Tail slightly longer than snout-vent length. Small elongated head with prominent eyes and moderately developed paratoids. The skin is smooth. Colour brown or grey-brown, with dark dots. A dorsal band extends over the body and tail, sometimes divided into large dark spots. Spots may be grouped at the sides, forming two indistinct dorsal stripes.

Males and females show a number of morphometric differences. Males have a relatively longer tail and longer fore legs. Tail of the male ends in a paddle-shaped fin; tail-tip of the female is more pointed. Cloacal slit longer in males than in females (Kuzmin, 1995). Total length of adult animals 13-18 cm (Kuzmin, 1995).

Onychodactylus fischeri, Ussuriisky Reserve, Primorye, Russian Federation. Photo: Burkhard Thiesmeier. 107

Diagnosis

Onychodactylus fischeri differs from other members of this genus by a combination of characters. It has 20-21 presacral trunk vertebrae, 14-15 costal grooves, 11-12 vomerine teeth in each vomerine tooth series. A distinct gap between the vomerine tooth series. In body proportions, O. fischeri differs from congeners by a relatively shorter tail in the males, a relatively narrow head in both sexes and a greater distance between the eyes. The colour of the back is light brown with black blotches and an indistinct dorsal band. In juveniles and adults there is no contrasting spotted colouration (Poyarkov et al., 2012). External sexual differences appear to be manifested to a higher degree in O. japonicus than in O. fischeri (Kuzmin, 1995); the black asperities on the inner surface of the hind legs of both sexes in O. japonicus are not found in O. fischeri (Kuzmin, 1995).

Eggs and larvae

Observations are rare. Most likely, breeding takes place underground between rocks in the streambed, near springs or torrents. Females produce two small, paired egg sacs, elliptical in shape and joined together at the distal end. They are attached to a stone by a mucous stalk. Total length of each sac, including the stalk, is 45 mm, between 1-8 eggs in each sac, egg diameter 5-6 mm (Serbinova & Solkin, 1995). Griffin & Solkin (1995) reported 5-10 eggs in each sac, with a diameter of 6-8 mm.

The pattern of larval development is similar to that of O. japonicus and typical for stream-dwelling salamanders (Regel & Epstein 1977, in Kuzmin, 1995). Larvae spawn and hatch in underground spawning sites. Early larval development is subterranean and the smallest known larvae from the Russian Far East measure 34-39 mm. Larvae complete metamorphosis and move onto land after the third or fourth hibernation at a total length of 7-11 cm. The age of sexual maturation is probably 8-9 years and maximum life-span 16-18 years (Griffin & Solkin, 1995; Smirina et al., 1994, in Kuzmin, 1999).

Distribution

The species is endemic to the Russian Far East. It occurs in the mountainous forest regions of the Sikhote-Alin Mountains (Primorye), southwards from the Zerkalnaya River Valley (Kuzmin, 1999; Poyarkov et al., 2012).

Habitat

Onychodactylus fischeri inhabits moist, cool, shady places in mountainous regions. It occurs from 100-1,700 m altitude. It is associated with the upper reaches of small mountain streams, overgrown by mixed broadleaf and cedar forests. Streambeds should have a thick layer of pebbles and mosscovered rocks, with abundant hiding places, a high humidity and temperatures ranging from 6-11°C. The animals remain close to springs, permanent stream-pools and waterfalls and are found under rocks, stones, fallen trees and logs (Kuzmin, 1995). Stream fidelity has been observed in mature salamanders (Griffin & Solkin, 1995).

Behaviour

This salamander may be locally abundant in suitable habitats, but usually occurs at low density. It feeds on a variable diet of aquatic, but mainly terrestrial, insects, millipedes, etc. (Kuzmin, 1995). Hibernation takes place from about October to late April. The animals appear when temperatures rise to 3-5°C. Breeding takes place in streams, probably mostly underground. Animals in breeding condition have been found from April to mid-July and from August to September. The peak of breeding activity is from mid-May to mid- or end of June, when water temperatures rise from 6-10°C (Serbinova & Solkin, 1995; Griffin & Solkin, 1995).

The range of Onychodactylus fischeri. 108

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Egg deposition and fertilisation were observed in the laboratory by Serbinova & Solkin (1995). Male salamanders seem to seek out females well before spawning and remain in attendance for ca. 10-20 days. The female postures on a stone with the hind part of her body in the water. Male courtship consists of his moving about the female and periodically touching her vent, rubbing his body on hers and staying beside her. When the female slightly arches her tail, the male suddenly extends and bends

his hind legs, and keeps them fixed in that position, unable to use them for locomotion. The female starts spawning by attaching a mucous string with the egg sacs to the stone. The male remains close to the female. When the egg sacs appear, the male starts undulating his body. He nudges the egg sacs and makes excited movements from side to side with his snout, thus dislodging the egg sacs from the female. He grasps the egg sacs with his fore legs, positioning them between his hind legs. While pulling the egg sacs against his vent, he fertilises the eggs. The extended surface of the hind legs of the male probably plays a role in inter-male competition for fertilisations and may be advantageous in the males’ attempts to monopolise egg sacs in assemblages of pairing salamanders by allowing him to grasp and hold the egg sacs more firmly, rub the sperm onto the egg sacs and prevent other males from interfering.

Threats and conservation

Onychodactylus fischeri is a habitat specialist, dependent on undisturbed old growth forest habitat with consistent streams and undisturbed stream substrate. It is mainly threatened by logging in stream headwaters.

This species is listed in the Red Data Books of both the USSR and Russian Federation. Onychodactylus fischeri sensu lato, before its delimitation to the Russian Far East, is listed as of Least Concern by the IUCN (2013). According to researchers, O. fischeri sensu stricto, should be regarded as Vulnerable (Kuzmin & Maslova, 2003; Poyarkov et al., 2012).

Observations in captivity

Experiments have been conducted to breed Onychodactylus fischeri with the help of hormone injections, but few have been successful (Serbinova & Solkin, 1995). In general, attempts to breed the species in captivity have not been very successful (references in Kuzmin, 1995).

Comments

References to Russian literature are given in

Kuzmin (1995).

References

Griffin & Solkin (1995); IUCN (2013); Kuzmin (1995, 1999); Kuzmin & Maslova (2003); Poyarkov et al. (2012); Regel & Epstein (1977); Serbinova & Solkin (1995); Smirina et al. (1994).

Onychodactylus japonicus (Houttuyn, 1782) | Japanese Clawed Salamander Description

Onychodactylus japonicus is a slender, elongate salamander. Tail slightly longer than snout-vent length. Small

elongated head with prominent eyes and moderately developed paratoids. The skin is smooth.

Onychodactylus japonicus, Shiga Pref., west central Honshu. Photo: Max Sparreboom. 109

Colour is brown or grey-brown, with dark dots. A dorsal stripe extends over the body and tail, sometimes divided into large spots. In the western part of its range, the stripe may also be vermillion to orange, contrasting with the sides (Sato, 1943; Goris & Maeda, 2005). Underside pale white, usually with a wedgeshaped dark marking on the neck-chest area (Yoshikawa et al., 2013b). Males and females show a number of morphometric differences. Males are on average longer than females; they have a relatively longer tail and longer fore legs (Akita, 1985, in Kuzmin, 1995). Tail-tip of the female is more pointed than that of the male. The male cloaca is V-shaped, the female cloaca is more rounded. In the breeding season, the male cloaca is somewhat swollen (Sato, 1943; Kuzmin, 1995). Both sexes have black asperities on the inner surface of the hind legs, the males also on the fore legs. Total length of adult animals 15-19 cm in males, 13.5-18 cm in females (Akita, 1985).

Diagnosis

Onychodactylus japonicus differs from other members of the genus by a combination of characters. On average it has 17 presacral vertebrae, 11 costal grooves and 11-12 vomerine teeth in each tooth series (Poyarkov et al., 2012), but counts of numbers of vertebrae, costal grooves and vomerine teeth vary by study (Yoshikawa & Matsui, 2013 found 18-19 presacral vertebrae). There is no gap between the vomerine tooth series. Snout-vent length is relatively small, tail is longer in males; the head is narrower in both sexes, and the distance between the eyes is smaller than in the other Onychodactylus species. Black claws well-developed on both fore- and hindlimbs and may also be present outside the breeding season. Colouration is also distinct: a bright coloured dorsum with a distinct light dorsal band is usually visible in premetamorphic larvae, juveniles and adults (Poyarkov et al., 2012). Usually a dark wedge-shaped marking on the chest (Yoshikawa et al., 2013b). External sexual differences are more evident in O. japonicus than in O. fischeri (Kuzmin, 1995).

Eggs and larvae

Two paired egg sacs, elliptical in shape and joined together at the distal end are attached to a stone by a mucous stalk. Many different sacs may be found attached to a single stone. Mean clutch size is 11-24, egg diameter 4.5-5.4 mm. Size of the egg sac may differ by site and depends on female size and perhaps time of deposition (Kuzmin, 1995 and references therein). The maximum number of ovarian eggs (36) was observed in the largest female (17 cm) (Akita, 1985, in Kuzmin 1995). Hatchlings apparently remain at the oviposition sites at headwaters for several months, then migrate downstream and begin

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The range of Onychodactylus japonicus.

to feed. Iwasawa & Kera (1980, in Kuzmin, 1995) describe the stages in the normal development of egg and larva. Larvae begin metamorphosis and move onto land in their fourth summer at a total length of about 8 cm as described by Hayase & Yamane (1982) for a population from the Tsukuba mountains, which is now regarded as belonging to a separate species, Onychodactylus tsukubaensis (Yoshikawa & Matsui, 2013b).

Distribution

This species is endemic to Japan and is widely distributed on the island of Honshu. Populations with a high degree of genetic differentiation have been found in the Tohoku district, northeastern Honshu (Yoshikawa et al., 2008) and these have now been described as a separate species, Onychodactylus nipponoborealis (Poyarkov et al., 2012). Another cryptic species, O. tsukubaensis, has been described from the Tsukuba mountains, in the Kanto district of eastern Honshu (Yoshikawa & Matsui, 2013). Onychodactylus kinneburi has been described from Shikoku and western Honshu (Yoshikawa et al., 2013b).

Habitat

Onychodactylus japonicus occurs at average altitudes from 300-2,000 m, but can also be found at lower elevations, down to 20 m. It inhabits moist, cool, shady places covered by mixed forests, with streams, moss-covered rocks and stony ground. Preferred habitats are dense woodlands near small rivers and lakes with clear, cool water with temperatures ranging from 9-12°C, usually with a northern exposure. The animals

Onychodactylus japonicus, habitat, north of Kyoto. Photo: Max Sparreboom.

remain close to springs and waterfalls and are found under rocks, stones, fallen trees and logs (Kuzmin, 1995).

Behaviour

Onychodactylus japonicus is a locally abundant species. It feeds on a variety of aquatic, but mainly terrestrial, invertebrates (Kuzmin, 1995). The larval diet consists mainly of mayfly nymphs and caddisfly larvae (Takahara et al., 2011). During migrations in spring or September-December, high concentrations of salamanders may be found, for instance on Hodatsu mountain, Ishikawa prefecture (Akita & Miyazaki, 1991, in Kuzmin, 1995). Depending on altitude and latitude, the breeding period may start in mid-May and last to the end of June (Thorn, 1969), or start in April to June-July and run to early August in the northern part of its range (Ohno, 1982, in Kuzmin, 1995). There may even be two breeding periods each year, in spring and in autumn, at a single site. Males are assumed to be biennial breeders and females possibly triennial (Akita & Miyazaki, 1991, in Kuzmin, 1995). A breeding site on Hodatsu Mountain was described in detail by Akita. Breeding occurred in the underground part of a stream. Pairs of egg sacs were attached to stones in the inside of a small underground cavity where cold springs emerged from under stones to form the headwater of a mountain brook. (Akita, 1982, 1983, in Kuzmin, 1995). This salamander is strongly dependent on cool, permanent water and the availability of hiding places to complete reproduction, and a high density of clutches may be observed in suitable sites.

Egg deposition and fertilisation have not been observed, but are probably similar those recorded for O. fischeri and O. koreanus (Serbinova & Solkin, 1995; Park, 2005).

Threats and conservation

The species is widely distributed throughout Japan, including in several protected areas, and is not uncommon. It is not included in the Red Data Book of Japan. Locally salamanders are collected during their migrations, sold for medicinal purposes or served as a delicacy in restaurants. Onychodactylus japonicus is listed as of Least Concern (IUCN, 2013).

Observations in captivity

Successful experiments have been conducted to breed O. japonicus with the help of hormone injections (references in Kuzmin, 1995).

Comments

References to the Japanese literature are given in Kuzmin (1995), who extensively quotes papers on ecology and reproduction of this species by Y. Akita. An authoritative account of the biology of Onychodactylus japonicus is given by Akita in the Encyclopedia of Animals in Japan by Sengoku et al. (1996).

References

Akita (1982, 1983, 1985, 1996); Akita & Miyazaki (1991);

Goris & Maeda (2005); Hayase & Yamane (1982); IUCN (2013) ; Iwasawa & Kera (1980); Kuzmin (1995); Ohno (1982); Poyarkov et al. (2012); Sato (1943); Sengoku et al. (1996); Serbinova & Solkin (1995); Takahara et al. (2011); Thorn (1969); Yoshikawa et al. (2008, 2013b); Yoshikawa & Matsui (2013).

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Onychodactylus kinneburi Yoshikawa, Matsui, Tanabe & Okayama, 2013 |

Shikoku Clawed Salamander

Onychodactylus kinneburi, male paratype, Mt Takanosu, Kochi Pref. (type locality). Photo: Natsuhiko Yoshikawa.

Description and Diagnosis

Onychodactylus kinneburi is a slender, elongate salamander, similar to the other Japanese Onychodactylus species (O. japonicus, O. nipponoborealis and O. tsukubaensis), to which it is closely related. The following is based on the original description by Yoshikawa et al. (2013b). This species differs from the other Onychodactylus species genetically (Yoshikawa et al., 2008) and by the following combination of morphological features: Sharply defined yellow or yellow-orange dorsal stripe on black background. Body relatively large; tail longer than snout-vent length in both sexes. It lacks a wedge-shaped dark marking on the chest; ventral side pale white with weak pigments; usually 19 presacral vertebrae including atlas; 13 costal grooves; right and left vomerine tooth series usually continuous without gap, series tending to curve in a shallow way; usually 13-16 vomerine teeth on one side. Onychodactylus kinneburi differs from O. japonicus in that females have longer hindlimbs and shorter snout and males have a narrower intercanthal space. It has significantly larger numbers of presacral vertebrae and costal grooves. The species cannot be easily distinguished by dorsal colouration alone. The most reliable character to distinguish O. kinneburi from O. japonicus is the wedge-shaped dark marking on the neckchest area, which is usually present in O. japonicus, but absent in O. kinneburi.

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Eggs and larvae

There is no documented information on egg sacs in the wild, but these are presumably similar to those of O. japonicus. The larvae are ca. 27 mm in total length immediately after hatching, with a large amount of yolk, undeveloped spatulate limbs and a grey dorsum. Larvae of this stage are normally not found in streams. More fully developed larvae come in two colour morphs, one dorsally yellowish-grey with black spots, and the other black with a sharp-edged broad stripe. Larvae found in streams are between 33-105 mm long. Their head is rectangular, snout blunt; eye slightly prominent; three pairs of short external gills; labial fold well-developed at posterior half of upper jaw;

Onychodactylus kinneburi, larva, Mt. Koishiyama, South Shikoku. Photo: Joachim Nerz.

Distribution

This species occurs in the mountains of Shikoku in western Japan and at several localities in the Chugoku Mountains of western Honshu. Onychodactylus kinneburi occurs sympatrically with O. japonicus in the Chugoku Mountains (Yoshikawa et al., 2008, 2010a; 2013b).

Habitat

Onychodactylus kinneburi occurs at altitudes over 700 m (Yoshikawa et al., 2013b). Like the other Onychodactylus species it inhabits cool, humid, well-forested terrain.

Behaviour

The ecology and behaviour of this species are poorly known, but are probably similar to that of Onychodactylus japonicus. Breeding adults of both O. kinneburi and O. japonicus were found around a breeding site, situated near an underground stream. Hatchling larvae and more developed larvae of both species were found in this stream, indicating that breeding site and breeding season are identical in these species, in spite of their clear reproductive and genetic isolation (Yoshikawa et al., 2010a; 2013b).

Threats and conservation The range of Onychodactylus kinneburi.

caudal fin low, but well-developed dorsally and ventrally; dorsal fin higher than ventral fin; dorsal fin starts at the level of posterior hindlimb; ventral fin starts at around posterior half to twothirds of tail; tail-tip moderately rounded; skin fold on posterior edge of limb; surfaces of palm and sole with dark asperities; and digits with acute, recurved claws. A contrast between the orange and black colouration appears in premetamorphic larvae.

Although locally abundant, this species’ range is limited and fragmented. It is recommended that its habitats are monitored, and that Onychodactylus kinneburi is designated as Near Threatened according to IUCN standards (Yoshikawa et al., 2013b).

Observations in captivity

There are no reports of this

species being kept in captivity.

References

Yoshikawa et al. (2008, 2010a, 2013b).

Onychodactylus koreanus Min, Poyarkov & Vieites, 2012 | Korean Clawed Salamander

Description and Diagnosis

Onychodactylus koreanus is a slender, elongate salamander, very similar to O. fischeri sensu stricto, with which it was long considered to be identical. Apart from the genetic differences that distinguish this Korean Onychodactylus species, it can be diagnosed from its congeners by the following combination of characters. 19 presacral trunk vertebrae, 13 costal grooves, 16-17 vomerine teeth in each vomerine tooth series; usually a gap between the tooth series; comparatively larger eyes and relatively narrower head; black claws in both sexes during the breeding season, sometimes absent outside the breeding season.

Colour of the dorsum, head and tail black or brown with numerous small, light, roundish or oval spots and ocelli.

Underside light reddish or brownish. Juveniles have a contrasting spotted colouration (Poyarkov et al., 2012).

Eggs and larvae

Observations are rare. Breeding probably takes place underground between rocks in the stream-bed near springs or torrents. Females produce two small, paired egg sacs, elliptical in shape and joined together at the distal end. They are attached to a stone by a mucous stalk. Assemblages of eggs have been found in Hwansun-gul Cave, Samcheok-shi, Kangwon-do, South Korea. The site is situated inside the cave, where a permanent stream passes through. Park (2005) found a total of 173 pairs of egg sacs at that spot. He counted 2-13 eggs per egg sac and a total clutch size varying from 10-22, with egg diameter ranging from 4.9-7.2 mm. 113

Onychodactylus koreanus, male, Chiak-san National Park, Korea. Photo: Max Sparreboom.

Onychodactylus koreanus, male, Chiak-san National Park, Korea. Photo: Max Sparreboom.

Onychodactylus koreanus, subadult, Chiak-san National Park, Korea. Photo: Max Sparreboom.

Onychodactylus koreanus, larvae, Chuncheon, Korea. Photo: Max Sparreboom.

See below for an account of the reproductive activity observed at this site. The pattern of larval development is similar to that of Onychodactylus fischeri and O. japonicus and typical of streamdwelling salamanders (Regel & Epstein 1977, in Kuzmin, 1995). Larvae between 0-3 years old were found together in streams, and two periods of larval recruitment were observed each year, suggesting that O. koreanus breeds twice yearly (Lee et al., 2008). Metamorphosis takes place in the second or third year, at a total length of 7-10 cm (Lee et al., 2008; Poyarkov et al., 2012). 114

Salamanders of the Old World | Onychodactylus

Distribution

Onychodactylus koreanus has so far only been recorded in South Korea, where it has a wide distribution, inhabiting the mountain ranges of Baekdudaegan and Taebaeksanmaek. Onychodactylus spp. have been recorded from a number of provinces in North Korea, but further study is needed to determine whether these are O. koreanus or another species of Onychodactylus (Poyarkov et al., 2012).

Habitat

Onychodactylus koreanus inhabits moist, cool, shady places in mountainous regions, where it occurs from 10-1,915 m altitude. It is associated with clean, fast-running streams in

Onychodactylus koreanus, egg sacs, Hwansun-gul cave, Korea. Photo: Max Sparreboom.

humidity in the surrounding habitat (Kuzmin, 1995; Poyarkov et al., 2012).

Behaviour

Breeding takes place in streams, probably mostly underground. Observations of breeding are rare. Egg deposition and fertilisation were observed in Onychodactylus fischeri in the laboratory by Serbinova & Solkin (1995). Their findings have been summarised under O. fischeri. Reproduction in O. koreanus is probably generally similar to that of O. fischeri. An extraordinary account is given by Park (2005), who observed sexual behaviour and egg laying in Hwansun-gul cave, Samcheok, Kangwon-do. It appears that under natural circumstances, reproduction is less quiet than in the laboratory. A large assemblage of mating salamanders was observed in the stream running through the cave. For oviposition a female moved to a part of the stream where several males were present and egg sacs were already attached nearby. While she attached her egg sacs to a stone wall some 40 cm under the water surface, many males gathered and attempted to grasp the egg sacs before oviposition was completed. Males formed a mating ball, scrambling for access to the egg sacs. Males outnumbered females by 20/1 (Park, 2005).

Threats and conservation The range of Onychodactylus koreanus.

wooded areas with pine trees or deciduous forests. It is also found in caves. Streambeds where the animals live have a thick layer of pebbles and moss-covered rocks with abundant hiding places, water temperatures ranging from 6-14°C, and high

This species is a habitat specialist, dependent on undisturbed old growth forest habitat with permanent streams and undisturbed stream substrate. Although sensitive to breeding habitat disturbance, Onychodactylus koreanus is common in some areas and regarded as of Least Concern according to IUCN criteria (Poyarkov et al., 2012).

Observations in captivity

Reports of captive maintenance of Onychodactylus koreanus are scarce. In captivity these 115

Onychodactylus koreanus, habitat, Odaesan National Park, Korea. Photo: Max Sparreboom.

salamanders require a winter break of 2-3 months with temperatures of 5-8°C. They become active at temperatures round 12°C. Kept in cool terrariums with a temperature not exceeding 18°C, they thrive on a diet of earthworms. Some captive individuals have lived for 15 years (Arnaud Jamin, Jean Raffaëlli, France, pers. comm., 2013).

Comments

Genetic analyses suggest that this species is sister to Onychodactylus zhaoermii from Liaoning, China, and is more closely related to the Japanese Onychodactylus species than to O. fischeri from Russia (Poyarkov et al., 2012).

References

Kuzmin (1995); Lee et al. (2008); Park (2005); Poyarkov

et al. (2012); Regel & Epstein (1977); Serbinova & Solkin (1995).

Onychodactylus nipponoborealis Kuro-o, Poyarkov & Vieites, 2012 |

Tohoku Clawed Salamander

Description and diagnosis

Onychodactylus nipponoborealis is a slender, elongate salamander, similar to O. japonicus, to which it is most closely related. It was only recently given species status on the basis of the high genetic divergence of salamander populations from Tohoku from O. japonicus populations further south.

This taxon differs from O. japonicus genetically (Yoshikawa et al., 2008) and in the following combination of morphological features: 18 presacral trunk vertebrae, 12 costal grooves and 17-18 vomerine teeth in each vomerine tooth series. Distinctly curved vomerine tooth series usually with a small gap between them; relatively large snout-vent length; short tail in males and relatively longer tail in females; a longer distance between axilla and groin; wider heads in both sexes and relatively greater dis116

Salamanders of the Old World | Onychodactylus

tance between the eyes. Back usually brightly coloured, from yellow-brown to bright red; light dorsal band usually with indistinct borders. Juveniles and larvae with dark ground colour and indistinct dorsal band (Poyarkov et al., 2012).

Eggs and larvae

There are no records of eggs and clutches specifically for this species. Most probably they are similar to those of Onychodactylus japonicus. Larvae appear in streams when they reach a total length of 30-45 mm. Larvae probably metamorphose in their second or third year of life at a total length between 80-90 mm (Poyarkov et al., 2012).

Distribution

This species is endemic to Japan and occurs in the Tohoku district, northeastern Honshu (Yoshikawa et al., 2008; Poyarkov et al., 2012).

Onychodactylus nipponoborealis, Iwate Pref., north-eastern Honshu. Photo: Tim Johnson.

it inhabits mountain coniferous, mixed and broad-leaved deciduous forests, and is found along fast-flowing mountain streams with cool and well-aerated water. Reproduction takes place from late May or June until July to early August (Ohno, 1982 in Poyarkov et al., 2012).

Behaviour

Onychodactylus nipponoborealis is locally abundant. There are no specific records of its behaviour, which is probably similar to that of O. japonicus.

Threats and conservation

This species is widely distributed in the mountains of northern Honshu. It is probably sensitive to habitat destruction and changes in water quality. Poyarkov et al. (2012) suggest that its conservation status should be designated as of Least Concern with regard to IUCN criteria.

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments The range of Onychodactylus nipponoborealis.

Habitat

Onychodactylus nipponoborealis occurs at altitudes from 100-2,000 m. In the Tohoku region in the north of Honshu,

References to the Japanese literature are given in Kuzmin (1995) and Poyarkov et al. (2012). An authoritative account of the biology of Onychodactylus japonicus is given by Akita in the Encyclopedia of Animals in Japan by Sengoku et al. (1996).

References

Akita (1996); Kuzmin (1995); Ohno (1982); Poyarkov

et al. (2012); Sengoku et al. (1996); Yoshikawa et al. (2008).

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Onychodactylus tsukubaensis Yoshikawa & Matsui, 2013 | Tsukuba Clawed Salamander

Description and Diagnosis

Onychodactylus tsukubaensis is a slender, elongate salamander, similar to O. japonicus and O. nipponoborealis, to which it is most closely related. It was only recently described as a species on the basis of the high genetic divergence between populations of this salamander in the Tsukuba mountains and populations of O. japonicus and O. nipponoborealis, and the reproductive isolation that implied (Yoshikawa et al., 2010a; 2012).

This species differs from O. japonicus and O. nipponoborealis genetically (Yoshikawa et al., 2008) and in a combination of morphological features (Yoshikawa & Matsui, 2013). It differs from all other species of Onychodactylus in having a short tail, equal to or only slightly longer in males and shorter in females than snout-vent length. Regarding snout-vent length and head length, O. tsukubaensis differs from O. japonicus in that: in males, O. tsukubaensis has a relatively wider head, shorter tail, longer head, wider chest, larger intercanthal distance and a smaller internarial distance; and in females, O. tsukubaensis has a longer and wider head, wider chest and shorter tail, and smaller intercanthal and internarial distances. Onychodactylus tsukubaensis differs from O. nipponoborealis in having a shorter tail, shorter hindlimbs, a larger intercanthal distance and a smaller interorbital distance. Onychodactylus tsukubaensis has a smaller number of presacral vertebrae (18) than O. nipponoborealis (18-19). The number of vomerine teeth tends

Onychodactylus tsukubaensis, female, (type locality). Photo: Natsuhiko Yoshikawa. 118

Salamanders of the Old World | Onychodactylus

to be higher than in the other two species, but tooth counts differ in different studies and make comparison difficult (Poyarkov et al., 2012). A gap between the vomerine tooth series is rarely present. As in the other two species, colouration is highly variable. Onychodactylus tsukubaensis is more similar to O. nipponoborealis than to O. japonicus, but the occurrence of a distinct broad dorsal stripe and dense silvery dots appears to be more frequent in O. tsukubaensis (Yoshikawa & Matsui, 2013).

Eggs and larvae

Egg sacs are similar to those of Onychodactylus japonicus. They are gelatinous and spindle-shaped, containing a small number of pigmentless, completely yellowish eggs, 5.3 mm in diameter. A clutch may contain some 17 eggs (Yoshikawa & Matsui, 2013). Larvae hatch in February or March at a size of approximately 35 mm. The larvae have a relatively shorter tail and look somewhat stouter than larvae of the other Onychodactylus species. They live in streams for three years before they metamorphose from July-October at a size of 80 mm or more (Hayase & Yamane, 1982; Yoshikawa & Matsui, 2013).

Distribution

This species is endemic to Japan with records in eastern Japan, in the mountains of Tsukuba, Kaba, Ashio, Kinoko, Tsubakuro and the adjacent mountains of Ibaraki Prefecture (Yoshikawa & Matsui, 2013).

The range of Onychodactylus tsukubaensis.

Onychodactylus tsukubaensis, habitat, Mt. Tsukuba from the North. Photo: Natsuhiko Yoshikawa.

Habitat

Onychodactylus tsukubaensis occurs at altitudes from 350-871 m. It inhabits cool, humid, well-forested terrain. The salamanders appear to breed underground in headstreams, where water is always present at a stable temperature of 7.9-9.5°C throughout the year. The breeding season appears to be from May-June or earlier, but is hard to determine due to the secretive, underground lifestyle of these salamanders (Yoshikawa & Matsui, 2013).

Behaviour

The ecology and behaviour of this species are poorly known. There are no specific records of its behaviour, which is probably similar to that of Onychodactylus japonicus.

Threats and conservation

There is no information on

the status of this species.

Observations in captivity

Only one pair of egg sacs of Onychodactylus tsukubaensis has been studied. It was deposited at the end of May in the laboratory (Yoshikawa & Matsui, 2013). There are no published records of this species being bred in captivity.

References

Hayase & Yamane (1982); Poyarkov et al. (2012);

Yoshikawa et al. (2008, 2010a, 2012); Yoshikawa & Matsui (2013).

Onychodactylus zhangyapingi Che, Poyarkov, Li & Yan, 2012 |

Jilin Clawed Salamander

Description and Diagnosis

Onychodactylus zhangyapingi is a slender, elongate salamander, very similar to O. fischeri sensu stricto, with which it was long considered to be identical. In addition to the genetic differences that distinguish this Chinese Onychodactylus species, it can be diagnosed from its congeners by the following combination of characters: 18 presacral trunk vertebrae; 12 costal grooves; usually 16-17 vomerine teeth in each vomerine tooth series; usually no gap between the tooth series; comparatively greater snout-vent length; and narrower head in both sexes. Black claws on fore- and hindlimbs in both sexes during the reproductive period, sometimes also outside the breeding season.

Colour of the dorsum, head and tail black to brown, covered with numerous small light, irregular elongated spots, forming a reticulated or thin marbled pattern. Ventral side is pinkish or yellowish. A light dorsal band is always absent. Juveniles have a contrasting spotted colouration on a dark background (Poyarkov et al., 2012).

Eggs and larvae

There are no documented observations on egg-laying, clutches or embryonic development. Examination of ovaries in females from the type series shows that a female may have 16-21 eggs. The larvae are similar to those of other Onychodactylus species. The smallest known larvae of 119

Onychodactylus zhangyapingi, male, holotype, Heisonggou, Linjiang County, Jilin. Photo: Che Jing.

Distribution

The species is known from the Changbaishan Mountain range in Jilin Province, where it occurs in the Counties of Linjiang, Ji’an and Tonghua. There appears to be a gap between the ranges of Onychodactylus fischeri and O. zhangyapingi. No geographic barrier is known to separate the ranges of O. zhangyapingi and O. zhaoermii (Fei et al., 2006, as O. fischeri; Poyarkov et al., 2012).

Habitat

Onychodactylus zhangyapingi inhabits streams and stream sides in forested, mountainous areas. The type series was collected at 330-560 m altitude. Adults prefer parts of the streams with minimal direct sunlight and abundant hiding places, unfrozen stream pools and underground springs. Streams where the salamanders occur have water temperatures ranging from 6-14° C (Poyarkov et al., 2012).

Behaviour

Breeding takes place in streams, probably mostly underground, as in other Onychodactylus species. Reproduction in this species has not been observed.

The range of Onychodactylus zhangyapingi.

Onychodactylus zhangyapingi appear in streams at a size of 30-40 mm. Metamorphosis is completed at a total length of 80-90 mm, most likely in their second or third year (Poyarkov et al., 2012). 120

Salamanders of the Old World | Onychodactylus

Threats and conservation

This species is a habitat specialist, dependent on persistent streams with an undisturbed substrate, in undisturbed old growth forest. Its distribution is limited and its habitat is under threat of destruction. This species (under the name of Onychodactylus fischeri) was listed as

Endangered in the Red Data Book of China (Zhao, 1998). Researchers recommend including O. zhangyapingi in the China Red Data Book of Endangered Animals and suggest listing it as Vulnerable according to IUCN criteria (Poyarkov et al., 2012).

Observations in captivity

There are no reports of this

Comments

Genetic analyses suggest that this species is sister to Onychodactylus koreanus from Korea, and is more closely related to the Japanese Onychodactylus species than to O. fischeri from the Russian Federation (Poyarkov et al., 2012).

References

Fei et al. (2006); Poyarkov et al. (2012); Zhao (1998).

species being kept in captivity

Onychodactylus zhaoermii Che, Poyarkov & Yan, 2012 | Liaoning

Clawed Salamander

Description and Diagnosis

Onychodactylus zhaoermii is a slender, elongate salamander, very similar to O. fischeri sensu stricto, with which it was long considered to be identical. Apart from the genetic differences that distinguish this Chinese Onychodactylus species, it can be diagnosed from its congeners by the following combination of characters: 17-18 presacral trunk vertebrae; 11-12 costal grooves; usually 13-14 vomerine teeth in each vomerine tooth series; usually a distinct gap between the tooth series; comparatively longer tail in both sexes; smaller eyes in males and relatively narrower heads in both sexes; and black claws on hindlimbs of males and sometimes of females during the breeding season, though claws may be absent in both sexes outside the breeding season.

Colour of the dorsum, head and tail black to violet-brown, covered with numerous small, light, irregular elongated spots, forming a dense reticulated pattern. Light ocelli may be sparsely present, light reddish or orange on the ventral side. Light dorsal band is always absent. Juveniles have a contrasting spotted colouration on a dark background (Poyarkov et al., 2012).

Eggs and larvae

There are no documented observations of egg-laying, clutches or embryonic development. Examination of ovaries in females from the type series shows that a female may have 3-24 eggs. The larvae resemble larvae of Onychodactylus koreanus. They feed on small crustaceans, tubifex worms, small tadpoles and insect larvae (Poyarkov et al., 2012).

The range of Onychodactylus zhaoermii.

Distribution Onychodactylus zhaoermii, Huashan, Anshan, Liaoning. Photo: Peter Brakels.

The species has been recorded in the Qianshan Mountains and the mountainous areas of Liaodong peninsula in Liaoning Province, China. It is unknown where the border 121

lies between the ranges of Onychodactylus zhaoermii and O. koreanus (Fei et al., 2006, as O. fischeri; Poyarkov et al., 2012).

Habitat

Onychodactylus zhaoermii occurs in forested, mountainous areas at elevations ranging from 500-800 m. It inhabits running torrents and permanent streams in valleys under dense forest canopies. Their preferred habitat consists of broad-leaved deciduous forests with dense undergrowth, and lianas, mosses and leaf litter. These salamanders occur in streams with water temperatures ranging from 6-14° C (Kuzmin, 1995; Li, 2004, in Poyarkov et al., 2012).

Behaviour

Breeding takes place in streams, probably mostly underground, as in other Onychodactylus species. The reproductive season is most probably from mid-April to May (Poyarkov et al., 2012).

Threats and conservation

This species is a habitat specialist, dependent on undisturbed old growth forest habitat with persistent streams and undisturbed stream substrates. Its distribution is limited to a few mountain systems in

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Liaoning, and possibly in Jilin Province, in China. Threats include habitat destruction due to intensive logging, farming with herbicides, water pollution and construction work as well as over-collecting for the pet trade. The species (under the name Onychodactylus fischeri) was listed in the Red Data Book of China (Zhao, 1998). Researchers recommend including it in the China Red Data Book of Endangered Animals and suggest listing the species as Vulnerable according to IUCN criteria (Li, 2004, in Poyarkov et al., 2012).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Genetic analyses suggest that this species is sister to Onychodactylus koreanus from Korea, and is more closely related to the Japanese Onychodactylus species than to O. fischeri from Russia (Poyarkov et al., 2012).

References

Fei et al. (2006); Kuzmin (1995); Li (2004); Poyarkov

et al. (2012); Zhao (1998).

Pachyhynobius Fei, Qu & Wu, 1983 Pachyhynobius was diagnosed as a separate group of hynobiid salamanders, differing from Hynobius in the following characteristics: Vomerine teeth arranged in two short arched series (shaped) not connected at the midline; a gap between pterygoid and maxillary; labial folds present; 13 costal grooves; high tail-fin in adults; lacrimal reaching external nares, not the orbits; and a protuberance on inner squamosal (Fei et al., 1983, 1985; Xiong et al., 2007). Different authors arrive at different conclusions regarding the position of Pachyhynobius in recon-

structions of the phylogeny of hynobiids (Zhang et al., 2006; Peng et al., 2010; Xia et al., 2012; Weisrock et al., 2013). The genus comprises only one species:

Pachyhynobius shangchengensis Fei, Qu & Wu, 1983

References

Fei et al. (1983, 1985); Peng et al. (2010);

Weisrock et al. (2013); Xia et al. (2012); Xiong et al. (2007); Zhang et al. (2006).

Pachyhynobius shangchengensis Fei, Qu & Wu, 1983 | Shangcheng Stout Salamander

Description

A stout salamander with cylindrical body. 13 costal grooves. Tail cylindrical at base, laterally compressed near tail-tip; tail shorter than snout-vent length. Limbs short; when adpressed, toes and fingers do not meet. Snout rounded, labial folds present. Gular fold present. Vomerine teeth arranged in two arched series and separated at the midline. Four fingers, five toes, with cornified coverings at tips. Skin smooth. Pachyhynobius shangchengensis is the only hynobiid with a karyotype of 2n=64 (Yang, 1990; Xiong et al., 2007).

Colour of upperparts brownish-black, underside lighter. Juveniles have a blackish background with intensive blue dots all over the body (Pasmans et al., 2012).

Pachyhynobius shangchengensis, male, captive specimen. Photo: Frank Pasmans.

Very conspicuous sexual dimorphism, also visible outside the breeding season: The adult male develops a thick, broad head, to an extent not seen in any other hynobiid. There are further sexual dimorphic traits in dentition and hyobranchium (Clemen & Greven, 2009). Both sexes have high tail-fins. Total length on average 150-184 mm in males, 157-176 in females (Fei et al., 1985, 2006; Ye et al., 1993), but larger sizes have been reported in captive specimens, to a maximum of 196 mm in males and 201 mm in females (Pasmans et al., 2012).

Diagnosis

Vomerine teeth arranged in two separated, arched rows. A stout salamander with short limbs, leaving a distance of four costal grooves between fingers and toes, when limbs are adpressed (Fei et al., 1983, 1985; Xiong et al., 2007). Extremely broad head in adult males.

Eggs and larvae

Egg sacs have been deposited in captivity and were of various sizes: 38-57 mm in length, 14-17 mm in

Pachyhynobius shangchengensis, female, captive specimen. Photo: Frank Pasmans.

width. The females had attached the egg sacs to the underside of flat stones. The larger egg sacs contained 32 and 22 white eggs, the smaller 18 and 20. Egg diameter was 3.3 mm on average. The egg sacs were dull white with a bluish sheen and were 123

longitudinally striated. Larvae hatched after 36-42 days at a temperature of ca. 15°C. The larvae were characterised by the presence of interdigital membranes, the absence of balancers, the presence of a large yolk sac and front- and hindlimb buts, and measured ca. 21 mm. The larvae reached metamorphosis after more than a year (from 441-454 days) at a size of ca. 95 mm. This long larval stage was confirmed by observations in the field. Juveniles tend to be mainly aquatic after metamorphosis (Pasmans et al., 2012).

Distribution

This species occurs in the Dabieshan area (Hubei, Henan, and Anhui Provinces) in central China (Stuart et al., 2008; IUCN, 2013).

Habitat

Pachyhynobius shangchengensis inhabits slow-flowing hill streams in forested areas at altitudes between 380-1,100 m (IUCN, 2013). It prefers small pools along the streams, where the water is clear, about 0.5-1.5 m deep, and the current is slow. Adult salamanders hide in crevices between rocks on the bottom of the stream (Wang et al., 2009).

Behaviour

This species appears to be largely aquatic. It feeds on stream shrimps, small fishes, earthworms and insects (Cai, 2001; Wang et al., 2009). Wounded and scarred specimens have been found. Cai (2001) suggested that stream crabs may have inflicted these wounds, but given the hight levels of aggression observed in captive male specimens, the wounds could well have resulted from fighting amongst the salamanders (Pasmans et al., 2012).

Pachyhynobius shangchengensis, larva, 9 months old. Photo: Frank Pasmans.

Observations of mating behaviour are scarce. In the days preceding the deposition of egg sacs in captivity, males were sometimes seen lining up with the females, undulating their bodies while remaining parallel to the female. No further interactions were observed (Pasmans et al., 2012).

Threats and conservation

This species is uncommon. Over-collecting for human consumption is a major threat (Fei et al., 2006). Habitat destruction and degradation probably also pose threats. It is considered Vulnerable (Stuart et al., 2008; IUCN, 2013). Its habitats are fragmented and there is a need to protect this species from uncontrolled collecting from the wild. Protective measures have been proposed (Cai, 2001; Wang et al., 2009; Xiong et al., 2009).

Observations in captivity

Pachyhynobius shangchengensis has been imported to Europe via the pet trade. This salamander can be fiercely aggressive, but can be kept in large tanks with flowing water and sufficient hiding places. Successful breeding is recorded by Pasmans et al. (2012). The salamanders were kept in large tanks at temperatures usually below 20°C, but incidentally rising to 27°C in summer. Winter temperatures were 2-5°C.

Comments

Fei et al. (2010; 2012) only depict subadult specimens, where the extreme sexual dimorphism in head shape is not yet developed.

References

Cai (2001); Clemen & Greven (2009); Fei et al. (1983,

1985; 2006, 2010, 2012); IUCN (2013); Pasmans et al. (2012); Stuart et al. (2008); Wang et al. (2009); Xiong et al. (2007, 2009); Yang (1990);

The range of Pachyhynobius shangchengensis. 124

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Ye et al. (1993).

Paradactylodon Risch, 1984 Paradactylodon is a group of large-bodied mountain stream salamanders. The three species presently recognised used to be assigned to Batrachuperus, with which they share three significant traits: completely aquatic habits; large premaxillary fontanelle; and four toes on the hindlimb. But recent molecular work found Batrachuperus to be diphyletic. The central and western Asian species are relatives of Ranodon but cannot be assigned to that genus because Ranodon has five toes on the hindlimb and is only semi-aquatic (Zhang et al., 2006). The

genus Paradactylodon, once erected to accommodate Batrachuperus gorganensis (Risch, 1984) but not recognised (Reilly, 1987), has been resurrected to hold three species (Zhang et al., 2006).

Paradactylodon gorganensis (Clergue-Gazeau & Thorn, 1979) Paradactylodon mustersi (Smith, 1940) Paradactylodon persicus (Eiselt & Steiner, 1970)

References

Reilly (1987); Risch (1984); Zhang et al. (2006).

Paradactylodon gorganensis (Clergue-Gazeau & Thorn, 1979) |

Gorgan Mountain Salamander

Description

Paradactylodon gorganensis is a large-bodied salamander, very similar to P. persicus. This description is based on one adult male specimen. Head flattened, eyes well-developed. Large mouth and tongue. Labial folds not well-developed. Vomerine teeth in two arch-shaped rows. Limbs robust, especially hindlimbs. Limbs overlapping when laid against the body. Four toes and four fingers. Tail a little longer than snoutvent length, compressed toward the tip. Upper and lower caudal fins well-developed. Tail-tip has a rounded point. Skin smooth (Thorn & Raffaëlli, 2001). Colour dark olive-brown to yellowish-olive, with yellow spots, less numerous than in P. persicus (Thorn & Raffaëlli, 2001). The belly is lighter than the dorsal parts. Total length 22.6 cm (Thorn & Raffaëlli, 2001).

Diagnosis

A robust, large-bodied salamander with rectangular head and prominent eyes, four fingers and four toes, and tail usually longer than snout-vent length. Yellow spots on back and tail. Differs from Paradactylodon persicus in shape of vomeropalatine teeth series, which form two transverse arched series in a V-shape in P. gorganensis, whereas in P. persicus they are small and scarcely curved. Form of head becomes narrower towards the rear, whereas it remains rectangular in P. persicus. Longer hind legs, relatively longer tail, and bigger eyes than in P. persicus (Clergue-Gazeau & Thorn, 1979; Stöck, 1999).

Eggs and larvae

Egg sacs were found attached to a stone on the bottom of a pond in late January, with water temperature below 10°C. Egg sacs are 80-182 mm long. A single sac may contain 31-52 eggs, 4-5 mm in diameter, in four rows seen in cross section across the egg sac. The first larvae hatch after 40 days, have limb buds, and are 19 mm long. Larvae reach a

Paradactylodon gorganensis, Shirabad Cave near Gorgan, Golestan, Iran. Photo: Omid Mozaffari. total length of 41-50 mm in the first season (Ebrahimi et al., 2004). Young larvae are whitish-yellowish, transparent in appearance, with inconspicuous brownish pigmentation. Larger larvae become darker and a yellow colouration develops. Larvae metamorphose in the second year, ca. 10 cm long, coloured with a contrasting pattern of brown and yellow. 125

In Paradactylodon gorganensis the snout is relatively broader and blunter than in P. persicus. Juveniles live in water and on land (Stöck, 1999).

Distribution

This species occurs in the eastern part of the Elburz Mountains, Golestan Province, Iran, where it was found in the Shirabad Cave and in the Manzoulak spring (Baloutch & Kami, 1995; Stöck, 1999; Ebrahimi et al., 2004; IUCN, 2013).

Habitat

Paradactylodon gorganensis inhabits the Hyrcanean Forest, a temperate rainforest. Adult P. gorganensis have been found in a 200 m long cave, with a spring at the end, at 310 m altitude. Juveniles and adults are hard to find on land (IUCN, 2013).

Behaviour

Analysis of stomach contents showed that this species feeds on aquatic insects and their larvae, but also on salamander larvae of their own kind. The stomach of one individual collected in Shirabad Cave contained two hairless bats (Myotis blythii) (Kami, 2004; Kami refers to P. persicus, but the animals are from the type locality of P. gorganensis). Outside caves, where the difference between night and day is not apparent, the animals are active at night. The life history and ecology of this species are largely unknown.

Threats and conservation

This species is listed as Critically Endangered, because its distribution is limited to a very small area, and the Shirabad Cave suffers from the activities of people visiting it. Nearly all the Hyrcanian forests of Iran are conserved within protected areas, including the range of this species (IUCN, 2013).

Observations in captivity

Larvae and adults of Paradactylodon gorganensis have been kept in captivity on a small scale in Germany. They were kept in a cellar room and were most ac-

Paradactylodon gorganensis, larva, Shirabad Cave near Gorgan, Golestan, Iran. Photo: Omid Mozaffari.

tive at temperatures between 10-16°C at night. Animals reached a size of 20 cm in their fourth year in captivity. There are no accounts of captive breeding as yet (Auer, 2013).

Comments

The taxonomic relationship of Paradactylodon gorganensis to the other Iranian species, P. persicus, is still unclear. Kami (2004) refers to specimens from the type locality of P. gorganensis (Shirabad Cave) as persicus. Paradactylodon gorganensis may be a variant or subspecies of P. persicus, but the species status is best maintained until more data on Iranian Paradactylodon spp. are available (Stöck, 1999; Ebrahimi et al., 2004).

References

Auer (2013); Baloutch & Kami (1995); Clergue-Gazeau &

Thorn (1979); Ebrahimi et al. (2004); IUCN (2013); Kami (2004); Stöck (1999); Thorn & Raffaëlli (2001).

Paradactylodon mustersi (Smith, 1940) | Afghanistan Mountain Salamander Description

Paradactylodon mustersi is a robust salamander with rectangular head and broadly rounded snout. Cylindrical body with 14 costal grooves and a dorsal vertebral groove. Upper and lower jaws have prominent labial folds. Gular fold distinct. Limbs well-developed, with four fingers and four toes. Tips of digits covered with brown horny epidermis, not extending onto soles and palms. Foot and hand each have two tubercles on palmar surface. Vomerine teeth in two small, arched, transverse rows between the choanae, nearly touching at the midline. Tail vertically oval to square at the base, flattening gradually towards the tip, which is obtusely pointed.

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Tail-fin is frequently nicked or jagged. Tail is slightly shorter than snout-vent length. Elongated head with prominent eyes and well-developed paratoids, marking a sharp transition from head to trunk. The skin is smooth. Colour dark olive-brown to yellowish-olive, indistinctly s peckled with tiny pigmented dots. The belly is lighter with fewer pigmented spots. Males are slightly larger than females. The only sexual dimorphism is in the cloaca of mature adults. In males the

Paradactylodon mustersi, Paghman Valley, Afghanistan. Photo: Max Sparreboom.

Paradactylodon mustersi, Paghman Valley, Afghanistan. Photo: Max Sparreboom.

vent is a V-shaped opening pointing posteriorly. A shallow longitudinal groove or fold bisects the V. This pleated fold is the distinguishing feature of the male cloaca. In females the vent is a longitudinal slit that is sometimes puckered or swollen, causing grooves on the lateral lips. The female has a more swollen cloaca than the male.

Paradactylodon mustersi resembles members of Batrachuperus in general appearance, size, diet and habitat. Differences include a reduced tail-fin, ossification of the pterygoid bone and well-developed gills in the larvae.

Total length 16-18 cm.

Diagnosis

A robust salamander with rectangular head and prominent eyes, four fingers and four toes. Horny epidermis on digits does not extend onto the soles and palms as in Batrachuperus pinchonii. Tubercles on palmar surface of foot and hand as in B. karlschmidti and B. yenyuanensis (Liu, 1950).

Eggs and larvae

Eggs are deposited in sacs ca. 9-15 cm long, attached at the blunt end to the underside of rocks in the water current or onto the surface of a bed of watercress. Egg sacs are at first transparent, becoming more cloudy with age. They hold an average of 23 eggs (Nawabi, 1965), each one 3 mm in diameter. A female can produce 40-104 eggs, so probably deposits at least two egg sacs, although observations are lacking. One egg sac deposited in captivity was 55 mm long shortly after deposition, and contained 14 eggs each 3.5 mm in diameter. Larvae were 15 mm long and hatched after about one month (Sparreboom, 1979). Young larvae are mottled brown on the back and light on the belly. A dark line runs down the vertebral groove from the head to the hindlimbs. External gills are well-developed with four gill slits on each side of the head. Paradactylodon mustersi lacks the striking gill reduction found in species inhabiting mountain brooks, such as Batrachuperus. Limbs very thin with four digits on each. Tips of digits have claws as in the adult. Dorsal tail-fin starts where the vertebral groove ends, usually posterior to the level of the vent. Larvae may be found all year round. Metamorphosis takes place in spring after two years. Juveniles probably remain in the water.

Paradactylodon mustersi, Paghman Valley, Afghanistan. Photo: Max Sparreboom.

Distribution

Paradactylodon mustersi is best known from the Paghman mountains on the southern slopes of the Hindu Kush, 127

Afghanistan. Its distribution is not limited to the three tributaries of the Paghman Stream (Reilly, 1983), but extends west of Kabul, where it was reported from Gardan Diwal in the Koh-iBaba Massif (Mertens, 1970). It has also been recorded in the Salang pass north-east of Kabul, in Sanglakh in Maidan Province, south of Kabul, and in Dasht-i-Nawar (Böhme, 1982).

vae. Adults prefer larger prey, whereas larvae eat the smaller insect larvae and elmid beetles. Although mostly feeding in water, adults can also feed on land, where they use the tongue to catch insects (Böhme, 1982). Adults and larvae also eat plant matter, such as clumps of algae. The start of the breeding season coincides with spring thaw. Egg sacs are attached to submerged rocks or plants and have been found from March (Reilly, 1983) to the end of June (Nawabi, 1965).

Threats and conservation

Cultivation near the breeding streams has changed the habitat and irrigation systems divert water, causing the stream flow to vary. Grazing, and pedestrian and animal traffic in and along the streams have had a negative impact on salamander occurrence (Reilly, 1983), but the present situation is unknown. A potential threat is the damming of the stream to provide water for the city of Kabul. The species is very sensitive to habitat disturbance and is listed as Critically Endangered (IUCN, 2013).

Observations in captivity

The range of Paradactylodon mustersi.

Habitat

Paradactylon mustersi inhabits cold (0-14°C) fastrunning streams at altitudes from 2,440-3,750 m, where it can be found all year round. The streams are fed by melting rocky glaciers. Adults are found under rocks in fast moving water, and the larvae in deeper, quieter pools, commonly under floating beds of watercress and duckweed.

Behaviour

Analysis of stomach contents revealed high percentages of trichopterans, gammarids and dipterans in the diet. Food preference of the adults differs from that of the lar-

There are few accounts of Paradactylon mustersi being kept in captivity. They can be kept in tanks with running water, and with water sprayed over flat stones which serve as hiding places. Temperatures should preferably be below 18°C, but temperatures as high as 24°C are tolerated temporarily (Mertens, 1970; Sparreboom, 1977). Deposition of one egg sac was recorded, attached to the underside of a flat stone. An adult was seen upside down under the stone, attending to the place where the egg sac was attached. A few larvae hatched after about a month, but did not live long (Sparreboom, 1979).

Comments

Unless otherwise stated, all data in this species entry are based on Reilly (1983).

References

Böhme (1982); IUCN (2013); Mertens (1970); Nawabi

(1965); Reilly (1983); Sparreboom (1977, 1979).

Paradactylodon persicus (Eiselt & Steiner, 1970) | Persian Mountain Salamander Description

Paradactylodon persicus is a large-bodied salamander. Trunk with 11-14 costal grooves. Dorsal vertebral groove. Gular fold distinct. Limbs well-developed with digits overlapping when adpressed. Four fingers and four toes, with horny asperities on the tips. Tail compressed laterally, with thin upper and lower caudal fins. Tail usually slightly longer than snout-vent length. Head more or less rectangular, in some specimens widening anteriorly.

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Colour dark olive-brown to yellowish-olive, with yellow spots, especially arranged along the vertebral groove. The belly is lighter. Information on cloaca shape and sexual dimorphism is unclear (Kami, 2004). Total length 20- 26 cm (Kami, 2004).

Paradactylodon persicus, Chalus Weyser, Iran. Photo: Faraham Ahmadzadeh.

Diagnosis

A robust, large-bodied salamander with rectangular head and prominent eyes, four fingers and four toes, and tail usually longer than snout-vent length. Yellow spots on back and tail. Differs from Paradactylodon gorganensis in shape of vomero-palatine teeth series, which form two transverse arched series in a V-shape in P. gorganensis, whereas in P. persicus they are small and scarcely curved. The head is rectangular in shape in P. persicus, but becomes narrower posteriorly in P. gorganensis. Paradactylodon persicus has shorter hind legs, relatively shorter

Paradactylodon persicus, Chalus Weyser, Iran. Photo: Faraham Ahmadzadeh. tail and smaller eyes than P. gorganensis (Clergue-Gazeau & Thorn, 1979; Stöck, 1999).

Eggs and larvae

Egg sacs of this species have not been described, but may be similar to those of Paradactylodon gorganensis (Ebrahimi et al., 2004). Paradactylodon persicus was originally described and named from a larval specimen (Eiselt & Steiner, 1970). Larvae have since been described by Schmidtler & Schmidtler (1971) and Kami (2004): Vomerine teeth in two arch-shaped rows; black horny margin on lower jaw; snout rounded, head large; 14-15 costal grooves; four digits on fore- and hindlimbs. In 50 mm long larvae, brownish-black asperities (claws) appear on the tips of the digits, which disappear again in older larvae of ca. 70 mm (Schmidtler & Schmidtler, 1971). Larvae have a distinct upper caudal fin. Young larvae are light yellow without distinct spots. Larger larvae have irregular dark grey spots. Belly is without pattern. Larvae are found all year round and probably metamorphose in their second year (Kami, 2004) at 70-100 mm in length. Juveniles have contrasting yellow-black colouration. Tail length same as snout-vent length. No claws on finger and toe-tips. Longitudinal cloacal fold (Schmidtler & Schmidtler, 1971). Juveniles, like adults, have been found in water and on land.

Distribution

This species occurs on the Caspian slope of the Talysh and Elburz Mountains, in the provinces of Ardabil, Gilan, Golestan and Mazanderan in Iran (Baloutch & Kami, 1995; Kami, 2004; Ahmadzadeh & Kami, 2009; Ahmadzadeh et al., 2011; IUCN, 2013).

Habitat

The ranges of Paradactylodon persicus and P. gorganensis. Shirabad Cave, the type locality of P. gorganensis, is indicated with an arrow.

Although not a strict high altitude salamander such as its Afghan sister species, Paradactylon persicus inhabits cold (normally below 13°C) streams and caves in broadleafed forests with high precipitation, at altitudes up to 1,500 m. Streams are bordered by rich vegetation. Larvae prefer relatively quiet water with rocks. Juveniles and adults are hard to find on land. Adults are probably mainly aquatic, but have also been found in burrows on land (Steiner, 1973; Kami, 2004). 129

Paradactylodon persicus, habitat, Chalus Weyser, Iran. Photo: Faraham Ahmadzadeh.

Behaviour

Analysis of stomach contents revealed a diet of aquatic insects and their larvae, but also salamander larvae of their own kind. The stomach of one salamander collected in a cave contained two hairless bats (Myotis blythii) (Kami, 2004; but Kami refers to animals from the type locality of P. gorganensis). Outside caves, where the difference between night and day is not apparent, the animals are active at night. The life history and ecology of this species are largely unknown.

Threats and conservation

Paradactylodon persicus is threatened by habitat loss due to urban sprawl along the Caspian coast and foothills, agricultural development, logging (with the associated silting of streams and possible changes in ambient temperature), and also by aquatic pollution and by increasing light pollution in some parts of its range. Some populations might also be affected by extended periods of drought. In two localities, populations have declined drastically (Ahmadzadeh & Kami, 2009). The species is protected by wildlife conservation laws in Iran and is listed as Near Threatened (IUCN, 2013).

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Observations in captivity

There are no accounts of this species being kept in captivity, other than that of Schmidtler & Schmidtler (1971), who raised larvae and described the juveniles. See also Auer (2013) for the captive care of Paradactylodon gorganensis.

Comments

The taxonomic relationship of Paradactylodon persicus to the other Iranian species, P. gorganensis, is still unclear. Kami (1999; 2004) refers to specimens from the type locality of P. gorganensis (Shirabad Cave) as persicus. Paradactylodon gorganensis may be a variant or subspecies of P. persicus (Stöck, 1999; Ebrahimi et al., 2004), but the species status is best maintained until more data on Iranian Paradactylodon are available.

References

Ahmadzadeh & Kami (2009); Ahmadzadeh et al. (2011);

Auer (2013); Baloutch & Kami (1995); Ebrahimi et al. (2004); Eiselt & Steiner (1970); IUCN (2013); Kami (1999, 2004); Schmidtler & Schmidtler (1971); Steiner (1973); Stöck (1999).

Pseudohynobius Fei & Ye, 1983 The genus Pseudohynobius was erected by Fei & Ye (1983b). It was diagnosed as a hynobiid salamander having the maxilla oblique, widely separated from the pterygoid; intermaxillary space and interquadrate space nearly equal on the outside; vomerine tooth series short, with 7-17 teeth in shape, the inner branch slightly longer than the outer one; fontanelle between premaxillae and nasal bones large; lacrimal bone touching external nare; no labial folds; 11-13 costal grooves; no cornified coverings on palms and soles. Four fingers, five toes. The validity of the genus has been controversial (Zhao & Hu, 1988b). Molecular work has however supported its validity and appears to have settled the argument (Zeng et al., 2006). According to these and the following authors, the hynobiid Liua-Pseudohynobius species complex can be divided into two groups, the genus Liua including Liua shihi and L. tsinpaensis, and the genus Pseudohynobius (Zeng et al., 2006; Tian et al., 2006; Xu et al., 2007; Wei et al., 2009; Li et al., 2010). Furthermore, Peng

et al. (2010) synonymised Protohynobius Fei & Ye, 2000 with Pseudohynobius. Species now comprising the genera Liua and Pseudohynobius are more closely related to mountain stream salamanders of the genus Batrachuperus than to Ranodon (Zeng et al., 2006; Weisrock et al., 2013 and overview in Frost, 2013). Liua occurs north, and Pseudohynobius south, of the Yangtze River. Both genera are endemic to China.

Pseudohynobius flavomaculatus (Hu & Fei, 1978) Pseudohynobius guizhouensis Li, Tian & Gu, 2010 Pseudohynobius jinfo Wei, Xiong, Hou & Zeng, 2009 Pseudohynobius kuankuoshuiensis Xu & Zeng, 2007 Pseudohynobius puxiongensis (Fei & Ye, 2000) Pseudohynobius shuichengensis Tian, Gu, Sun & Li, 1998

References

Fei & Ye (1983b, 2000); Frost (2013); Li et al. (2010);

Peng et al. (2010); Tian et al. (2006); Wei et al. (2009); Weisrock et al. (2013); Xu et al. (2007); Zeng et al. (2006); Zhao & Hu (1988b).

The distribution of the genus Pseudohynobius. Stars refer to type localities. 1. Pseudohynobius flavomaculatus, 2. P. jinfo, 3. P. kuankuoshuiensis, 4. P. guizhouensis, 5. P. shuichengensis, 6. P. puxiongensis. Further distribution data in text. 131

Pseudohynobius flavomaculatus (Hu & Fei, 1978) | Yellow Spotted Salamander

Description

Head slightly flattened, of equal length and width. No labial fold. Long vomerine tooth rows with 12-17 teeth in each row. On the head, a thin groove runs from the back of the eye to the gular folds, and another groove runs dorsally from the back of the head to the tail-base. Tail length similar to snout-vent length. 11-12 costal grooves. When limbs are adpressed, fingers and toes overlap slightly. Four fingers, five toes. A noticeable but short tail-fin fold is present. Skin smooth. Upperside purple-brown, marked unevenly with irregular yellow or dark yellow blotches. The amount, size and shape of yellow blotches varies individually. Yellow markings are generally smaller on the head, larger on dorsal trunk, and tiny or absent on the tail. Underside light purple. The male has a longer and higher tail than the female. During the reproductive period, the head, back and dorsal side of limbs in the male have tiny white spines (Fei & Ye, 1983b; 2001; Fei et al., 2006; Kuzmin & Thiesmeier, 2001).

Total length 158-189 mm in males, 138-180 mm in females (Fei & Ye, 2001).

Diagnosis

Vomerine tooth series relatively long with 12-17 teeth on each side. Lungs long, reaching the 8th or 9th costal groove posteriorly. No labial folds; no cornified coverings on palms and soles. 11-12 costal grooves. Distinct dorsal colouration, dark purple with irregular yellow blotches (Fei & Ye, 1983b; Kuzmin & Thiesmeier, 2001). Distinct karyotype (2n = 52, Kuzmin & Thiesmeier, 2001; IUCN, 2013). Pseudohynobius flavomaculatus resembles P. kuankuoshuiensis, P. guizhouensis and P. jinfo in the presence of numerous dorsal yellow spots. However, these spots are large and irregularly shaped in P. flavomaculatus, small and oval-shaped in the other species (Wei et al., 2009; Li et al., 2010).

Eggs and larvae

The pair of egg sacs is coiled in a C-shape, the distal end tapering. The egg sacs are similar to those of Liua tsinpaensis. They are 130-270 mm long and contain 16-26 eggs per sac (Kuzmin & Thiesmeier, 2001). Eggs are round, 5.5 mm in

Pseudohynobius flavomaculatus, Hanchi village, Lichuan County, Enshi Tujia and Miao Autonomous Pref., Hubei (type locality). Photo: Hou Mian, courtesy Zeng Xiaomao. 132

Salamanders of the Old World | Pseudohynobius

diameter, and pale or light grey. Larvae are light brown, with upper labial folds. Tail-fin fold is wide, extending to the midpoint of the body (Fei & Ye, 2001; Kuzmin & Thiesmeier, 2001). Larvae feed on insects and small crustaceans, and take up to 1.5-2 years to metamorphose (AmphibiaWeb, 2013).

Distribution

This species occurs in Lichuan County, Hubei Province and Sangzhi County, Hunan Province, China (Zeng et al., 2006).

Habitat

This salamander normally lives on land, hiding under the roots of bamboo or in burrows under mosses and in the soil (Stuart et al., 2008; IUCN, 2013), but also occurs in and around mountain streams with water temperatures between 8-18°C (Ye et al., 1993). It occurs at altitudes from 1,100-1,845 m. The salamanders come out at night and prey on insects and millipedes or enter the stream to catch aquatic arthropods (Fei et al., 2006; Kuzmin & Thiesmeier, 2001).

Behaviour

The breeding season is from mid-April to May. Egg sacs were found in a small pool near a tiny spring seeping

from a small burrow, with a water temperature of 8°C. More egg sacs were found inside the burrow, as well as adults near the egg sacs. Thirty six adult salamanders were dug out of an area of 6 m 2 (Fei et al., 2006). This species’ reproductive behaviour has not been observed.

Threats and conservation

Pseudohynobius flavomaculatus is rare and is principally threatened by habitat destruction and degradation. It is considered Vulnerable (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Morphological and genetic differences between four species of Pseudohynobius are discussed by Wei et al. (2009).

References

AmphibiaWeb (2013); Fei & Ye (1983b, 2001); Fei et al.

(2006); IUCN (2013); Kuzmin & Thiesmeier (2001); Li et al. (2010); Stuart et al. (2008); Wei et al. (2009); Ye et al. (1993).

Pseudohynobius guizhouensis Li, Tian & Gu, 2010 | Guizhou Salamander Description

The following is a summary of the original species description by Li et al., (2010). This species is similar to Pseudohynobius kankuoshuiensis but differs in minor morphological aspects. It has 17 trunk vertebrae instead of 18. Its frontal bones are connected and form a triangle rather than an arc. The gap between frontal and parietal bones is small or absent.

The limits of its range are unknown.

Habitat

Pseudohynobius guizhouensis inhabits montane forest at altitudes of 1,400-1,700 m. The streams in which it breeds are covered with thick bamboo forest and other bushes. Adults normally live on land outside the breeding season and may be found far from streams under thick layers of fallen leaves. Larvae are found in the slow-flowing, shallow parts of streams.

When limbs are adpressed fingers and toes do not overlap.

Behaviour

Dorsum with many small spots; ventral side with many small white spots. Females tend to have more ventral spots than males.

Threats and conservation

Total length approx. 17-20 cm.

Diagnosis

A large salamander with spotted upperside.

Eggs and larvae

Larvae have been found in streams from March-July, with an average length of 67-74 mm.

Distribution

This species is so far only known from its type locality, Mt. Doupeng, at the borders of three counties (Guiding, Duyun and Majiang, Guizhou Province, China).

No published information.

There are insufficient data to make a statement about its status (IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

It is not known how many specimens of Pseudohynobius guizhouensis and P. kuankuoshuiensis were used in the osteological comparison by Li et al. (2010). Molecular work is needed to show if P. guizhouensis is a valid species or not (cf. species accounts of P. flavomaculatus, P. shuichengensis, P. kuankushuiensis and P. jinfo, cf. Zeng et al., 2006).

References

IUCN (2013); Li et al. (2010); Zeng et al. (2006).

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Pseudohynobius jinfo Wei, Xiong, Hou & Zeng, 2009 | Mount Jinfo Salamander Description

This species is similar to Pseudohynobius flavomaculatus, and the population occurring on Mt. Jinfo used to be considered to belong to that species. This is a slender salamander. Tail longer than snout-vent length. Head somewhat depressed and slightly longer than wide. Snout rounded in dorsal view. Large protruding eyes. Gular fold distinct. Vomerine tooth rows with only 8-9 teeth. Distinct groove on back, from back of head to tail-base. 12 costal grooves. Forelimbs slightly shorter than hindlimbs; hindlimbs stronger and twice the width of forelimbs. Tips of fingers and toes touching or slightly overlapping when limbs are adpressed. No horny cover on tips of digits. No tubercles on palms and soles. Dorsal colour purple, mottled with small yellowish spots. Ventral colour pale, flank with small yellowish spots. Total length ca. 20 cm (Wei et al., 2009).

Diagnosis

A salamander with a longer tail than other Pseudohynobius species; 8-9 vomerine teeth on each side; small yellow spots.

Eggs and larvae

Head of the larva is depressed, its width smaller than its length. Limbs slender, fingers and toes flat, with black horny cover at tips. Tail high, smaller than snout-

vent length, tip of tail abruptly peaked. Dorsal fin originating midway down the trunk. Colour light yellow-grey or yellowbrown (Wei et al., 2009).

Distribution

This species is so far only known from two neighbouring mountains, Mt. Jinfo and Mt. Baima, Nanchuan County, southwestern China.

Habitat

Both adult and larval specimens were collected from a clear mountain pond formed by a montane spring, surrounded by grass.

Behaviour

No published information.

Threats and conservation

There are insufficient data to make a statement about its status.

Comments

DNA work has shown that the populations on Mt. Jinfo and Mt. Baima, previously regarded as Pseudohynobius flavomaculatus, belong to a separate, reproductively isolated species (Zeng et al., 2006). Morphological differences between this and the other Pseudohynobius species are given by Wei et al. (2009), whose description forms the basis of the present summary.

References

Wei et al. (2009); Zeng et al. (2006).

Pseudohynobius jinfo, Nanchuan County, Chongqing. Photo: Hou Mian, courtesy Zeng Xiaomao.

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Pseudohynobius kuankuoshuiensis Xu & Zeng, 2007 | Kuankuoshui Salamander

Description

Head oval, slightly flattened. Snout rounded. Distance between nostrils larger than that between eyes. Labial fold absent. Vomerine tooth series have 12-17 teeth on each side. Trunk cylindrical, slightly flattened. Vertebral groove conspicuous. 11 costal grooves. When limbs are adpressed, digits only meet. Dorsal caudal fin starts from tailbase; ventral caudal fin present at the posterior two thirds of the tail. Skin smooth. Small white spots present on head, dorsum and the upperside of limbs. In life, dorsal colouration purplish-brown with scattered oval yellow spots, which are largest on dorsum. This species is similar to Pseudohynobius shuichengensis but its limbs are shorter. When limbs are adpressed fingers and toes touch or overlap slightly. Tail length slightly less than snoutvent length (Wei et al., 2009). This species is also similar to P. flavomaculatus in that it has orange spots on the dorsal side of body, tail and limbs. The spots are, however, smaller, isolated and more rounded. Head dimensions are also different from P. flavomaculatus (Xu et al., 2007; Fei et al., 2010). Dorsal colour greyish-brown with oval yellow spots (Wei et al., 2009).

Total length approx. 20 cm (Xu et al., 2007).

Diagnosis

A large salamander with dark grey, orangespotted upperside.

Eggs and larvae

Measurements of three larvae are given by Xu et al. (2007) and Fei et al. (2009).

Distribution

This species is so far only known from its type locality, Shuiyang, in Guizhou Province, China. The limits of its range are unknown (IUCN, 2013).

Habitat

This salamander inhabits montane areas with dense vegetation at elevations from 1,350-1,500 m. This species shelters in cool, thick, moist layers of fallen leaves from which it may be dug out by locals. Larvae are found in nearby shallow streams, where the water is clear and the current weak. Such streams are covered by the tree canopy. Larvae are also found in small pools fed by springs (Xu et al., 2007). Adults live on land outside the breeding season.

Behaviour

No published information.

Threats and conservation

This species is rare and is threatened by habitat degradation due to human activities. There are insufficient data to make a statement about its status (IUCN, 2013).

Comments

Pseudohynobius kuankuoshuiensis was long considered to be a population of P. flavomaculatus (Fei & Ye, 1983; Fei et al., 2006). However, Zeng et al. (2006) found a fixed allozyme difference between the two species. Mitochondrial sequence data further revealed 14.2% divergence between P. kuankuoshuiensis and P. flavomaculatus. Pseudohynobius kuankuoshuiensis is not closely related to P. flavomaculatus, despite their morphological similarities. Pseudohynobius kuankuoshuiensis is the sister species to P. shuichengensis. Morphological and genetic differences between four species of Pseudohynobius are discussed by Wei et al. (2009).

References

Fei et al. (2006, 2009, 2010); Fei & Ye (1983); IUCN (2013);

Wei et al. (2009); Xu et al. (2007); Zeng et al. (2006).

Pseudohynobius kuankuoshuiensis, Suiyang, Guizhou. Photo: Wei Gang. 135

Pseudohynobius puxiongensis (Fei & Ye, 2000) | Puxiong Salamander

Pseudohynobius puxiongensis, Puxiong town, Yuexi County, Liangshan Yi Autonomous Pref., Sichuan. Photo: Hou Mian, courtesy Zeng Xiaomao.

Description

A relatively small salamander with a slender body form; trunk cylindrical, slightly depressed. Head slightly flattened. No labial fold. Vomerine teeth in two short obliquely arched series, almost meeting in midline. Gular fold distinct. For cranial particulars see Comments below. Tail shorter than snout-vent length. 13 costal grooves (Xiong et al., 2011, recorded only 11 costal grooves). Four fingers, five toes. No horny cover on palms and soles. Dorsal fin fold low. Skin smooth (Fei & Ye, 2000). Upperside uniformly grey-yellow, mottled with yellowish spots, underside grey. A line of distinct dark yellow spots on dorsal side of the tail (Fei & Ye, 2000; Xiong et al., 2011). Total length holotype 133 mm (Fei & Ye, 2000).

Diagnosis

Pseudohynobius puxiongensis differs from other species of the genus in the following combination of features: dorsal colour grey-yellow with yellowish spots; distinct yellow line on dorsal side of the tail; total length smaller than congeners; and a moderate number of vomerine teeth (11-15) (Xiong et al., 2011).

Eggs and larvae

The pair of egg sacs is coiled in a spiral shape. There are transverse striations on the egg sac, which measures 74-121 mm. The eggs are arranged in the egg sac in a single line or interlaced (Peng et al., 2010). On average about

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12 eggs per egg sac, each egg 3.2-3.3 mm in diameter. Larvae have been found in November 2008 and 2009 (Xiong et al., 2011).

Distribution

This species occurs on the Tibetan Plateau. It is only known from the type locality of Puxiong and its immediate surroundings, in Yuexi County, Sichuan Province, China (Fei & Ye, 2000; Peng et al., 2010).

Habitat

This salamander normally lives on land, in and around mountain streams at 2,900 m altitude (Peng et al., 2010) and is only found in water during the breeding season. Lush bamboo and shrubs cover the breeding streams (Xiong et al., 2011). The salamanders are found in the upperparts of small mountain brooks originating from springs.

Behaviour

This species’ breeding season probably lasts from March to the end of April. Egg sacs and adult males near the egg sacs were found at the end of April (Xiong et al., 2011). Their reproductive behaviour has not been observed.

Threats and conservation

Two populations are known and only a very small number of animals have been found. The quality of the habitat appears to be declining due to grazing by livestock. This led Xiong et al. (2011) to regard the species as Critically Endangered although their data have not yet been included in the IUCN assessments.

Comments

Pseudohynobius puxiongensis was originally described as Protohynobius puxiongensis on the basis of a single specimen collected in 1965. Because the specimen had an internasal bone, it was thought to retain a primitive character lost by the common ancestor of all other hynobiid salamanders, and was therefore considered to be not only a new genus, but also a new subfamily, Protohynobiinae (Fei & Ye, 2000). The rediscovery of living individuals of P. puxiongensis near the type locality in 2008-2009 provided specimens that were identical to the original description, except for the presence of the internasal bone, implying that the internasal bone observed in the holotype could just be an individual variation. Investigation of the

complete mitochondrial genome led to the conclusion that P. puxiongensis was nested within the hynobiid family and was most closely related to the group of Pseudohynobius species. Consequently, Peng et al. (2010) included Protohynobius in the synonymy of the genus Pseudohynobius and Xiong et al. (2011) provided a new description. Morphological and genetic differences between four other species of Pseudohynobius are discussed by Wei et al. (2009).

References

Fei & Ye (2000); Fei et al. (2010); Peng et al. (2010);

Wei et al. (2009); Xiong et al. (2011).

Pseudohynobius shuichengensis Tian, Gu, Sun & Li, 1998 | Shuicheng

Salamander

Description

This species is similar to Pseudohynobius flavomaculatus, but is larger in size and its limbs are longer. Fingers and toes overlap when limbs are adpressed. 8-14 vomerine teeth. 12 costal grooves. Horny covers absent from palms and soles. Dorsal caudal fin starts from tail-base; ventral caudal fin starts 1-2 cm after the vent.

Males have higher tail-fins than females. In the male, the cloaca has a longitudinal groove with an anterior papilla; in the female, the cloaca is a simple longitudinal groove. In the breeding season, males develop small white dots on head, dorsum and upperside of limbs and tail; females develop reddish spots around the cloaca (Tian et al., 2006; Wei et al., 2009).

Dorsal colour purplish-brown. Yellow spots, as in P. flavomaculatus, are absent. The ventral colour is lighter.

Total length 177-210 mm in males, 182-213 mm in females (Tian et al., 2006; Fei et al., 2009).

Pseudohynobius shuichengensis, Fenghuang town, Shuicheng Pref., Guizhou (type locality). Photo: Hou Mian, courtesy Zeng Xiaomao. 137

Diagnosis

A large salamander with relatively long limbs. Dorsal colouration uniformly purplish-brown, without yellow spots.

Eggs and larvae

Egg sacs are found in and near burrows where springs emerge and never under stones. They are 163-392 mm long, spiral-shaped and striated. Each egg sac contains 22-54 eggs. Larvae grow to ca. 7-8 cm in size by 150 days after hatching from the egg sacs. Larvae at this stage hibernate and reach metamorphosis during the next spring (Tian et al., 1998).

Distribution

This species is so far only known from its type locality, Shuicheng County, in Guizhou, China. The limits of its range are unknown (IUCN, 2013).

Habitat

This salamander lives in a karstic region. Outside the breeding season adults live on the forest floor near streams at altitudes of 1,910-1,970 m. They hide under thick layers of fallen leaves, in crevices or in karst burrows, 10-20 m away from streams (Tian et al., 2006).

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Salamanders of the Old World | Pseudohynobius

Behaviour

These salamanders are active at night and feed on snails and insects. Breeding takes place in pools near the springs, from early May till the end of June. Their reproductive behaviour has never been observed.

Threats and conservation

This species is rare and threatened by habitat degradation, expanding agriculture, and pollution as a result of of pesticide and herbicide use. It is considered Vulnerable (IUCN, 2013).

Comments

Morphological and genetic differences between four species of Pseudohynobius are discussed by Wei et al. (2009). Mitochondrial DNA data suggest that Pseudohynobius shuichengensis is the sister species to P. kuankuoshuiensis (Zeng et al., 2006). This relationship indicates that the four Pseudohynobius species with bright dorsal spots (P. kuankuoshuiensis, P. flavomaculatus, P. jinfo and P. guizhouensis) are not monophyletic.

References

Fei et al. (2009); IUCN (2013); Tian et al. (1998, 2006);

Wei et al. (2009); Zeng et al. (2006).

Ranodon Kessler, 1866 Ranodon was diagnosed as a separate group of hynobiid salamanders, differing from Hynobius in the following characteristics: vomerine teeth arranged in two transverse, short, widely separated series; premaxillary fontanelle present; lungs present, but reduced; paratoids well-developed; four fingers, five toes; tail compressed laterally, not shorter than body; skin smooth; costal grooves well-developed; full-grown larvae with horny cover on toes; and larvae hibernating (Kuzmin & Thiesmeier, 2001).

In the taxonomic arrangement by Weisrock et al. (2013), Ranodon and Paradactylodon form one clade. The genus contains one species:

Ranodon sibiricus Kessler, 1866

References

Kuzmin & Thiesmeier (2001); Weisrock et al. (2013).

Ranodon sibiricus Kessler, 1866 | Semirechensk Salamander, Xinjiang Salamander Description

A large, robust salamander. Lungs present, but reduced. Vomerine teeth in two short, widely separated series. Premaxillary fontanelle small (Fei et al., 2006). Paratoid glands well-developed. Labial fold often reduced or absent, but welldeveloped in some large individuals. Large, protruding eyes. 11-13 costal grooves. Longitudinal groove running along the vertebral column from occipital region to tail-base. Tail a little longer than body length, or more or less the same length. Tail cylindrical at base, tapering towards the tip. Four fingers, five toes. Dorsal colour yellow-brownish to dark olive and grey-greenish. Some individuals have a dark-spotted pattern on a dark olive background. Colour may change depending on environment. Aquatic adults may be darker than terrestrial individuals. Colour becomes lighter with increase in temperature. Underparts lighter than upperparts.

Ranodon sibiricus, Borokhujir river basin, Junggarian Alatau, Kazakhstan. Photo: Burkhard Thiesmeier.

Males have a higher and longer tail than females. During the breeding season, tail-fin fold has fewer undulations and is higher in males than in females. Limbs and head are more muscular in males. Total length ca. 12-28 cm (Kubykin, 1986, in Kuzmin & Thiesmeier, 2001).

Diagnosis

Vomerine teeth arranged in two short, widely separated series between the internal nares. Tail usually a little longer than body. In adults no cornified covering on palms and soles. Adults not exclusively aquatic outside breeding period (Kuzmin & Thiesmeier, 2001).

Eggs and larvae

Females produce two egg sacs, joined at the distal end by a mucous stalk, and attach them to a stone.

Ranodon sibiricus, captive specimen. Photo: Henk Wallays.

139

Just after deposition, the egg sac is tetrahedral in shape and has a bluish opalescence. Forty-eight hours after spawning the egg sac swells in size to ca. 48-60 mm. Egg sac parameters vary both between individuals and within a given clutch. The majority of clutches contain 38-58 eggs, in Xinjiang clutches of 32-50 eggs have been reported. In general, the number of eggs per clutch seems to depend on female size and, correspondingly, on egg sac size. The eggs have almost no pigmentation and are 3-5 mm in diameter. Larvae hatch at 17-20 mm in length. Given the large amount of yolk in the eggs, larvae have a long endogenous nutrition period. Larvae have no balancers; a long tail; short gills; and cornified coverings on the tips of toes. Metamorphosis usually follows one or two hibernations at a length of 80-104 mm, depending on altitude and time of spawning (Kuzmin & Thiesmeier, 2001). The larvae are of the rheophilous type, but in spite of their adaptations to a life in running-water, the robust body shape of Ranodon sibiricus larvae resembles that of pond-dwelling species (Thiesmeier, 1996). The stages of normal development are illustrated in Kuzmin & Thiesmeier (2001).

Habitat

Ranodon sibiricus inhabits slow-flowing streams with summer water temperatures between 5-18°C, on more or less flat plateaus with a dense network of permanent streams, at altitudes between 2,100-3,200 m (IUCN, 2013). It prefers small, cold, spring-fed mountain streams with a variety of large boulders, stones and gravel substrates, where adults and larvae can find sufficient shelter (Dolmen et al., 1997, 1999).

Behaviour

This species is restricted to the southern and southwestern spurs of the Junggarian Alatau (Altao) Ridge in southern Kazakhstan and Mt. Tianshan in Wenquan County, Xinjiang Uygur Autonomous Region, China. It may also occur in the adjacent Yining, Huocheng and Tacheng Counties of China, and was historically also found in Hergos County. Its range is severely fragmented and suitable habitats are scarce (Stuart et al., 2008; IUCN, 2013).

Hibernation takes place from the end of September or early October to the end of April or early June, depending on altitude (Kuzmin & Thiesmeier, 2001). Adults are mainly nocturnal, and the larvae are also active during the day (Dolmen et al., 1999). These salamanders feed on both aquatic and terrestrial invertebrate prey, spending a considerable part of their life in water. Reproduction begins as soon as the snow and ice melt and extends from the end of April to early August. Ranodon sibiricus tends to breed in small streams at the same site each year. They often attach their egg sacs to the underside of great boulders, but may also attach them to large pebbles, plant stems and the bottom of streams (Dolmen et al., 1997; Greven et al., 1999). They first breed at ca. five years of age and have a lifespan of 15-20 years (or even longer in captivity) (Kuzmin & Thiesmeier, 2001; IUCN, 2013).

The range of Ranodon sibiricus.

Their behaviour before spawning has been described from observations made on captive animals in April 1985, kept in a tank at a water temperature of 11°C (Thorn, 1987, 1994; Kuzmin & Thiesmeier, 2001). The male spent more time in the water than the female. Once both male and female had entered the water, the male was alerted and sniffed the female’s flanks or tail-base. Sometimes he bit her gently. As egg deposition drew near, the female actively approached the male. She seized part of the vegetation with her fore legs, pressed her cloaca against a rocky surface under the water and began to deposit the clutch. On seeing her spawn, the male approached the female, mounted her dorsally and clasped her body with his four limbs. He then proceeded to clasp the emerging egg sac with his fore legs, arched his back, pushed the female away from him and slid the egg sac against his cloaca. Fertilisation probably took place at this point. He curled his body around the egg sac, his snout reaching his cloacal region (termed ball embrace). After about a minute, the male would fall to the bottom, go up for air and then approach the female again, mount her, and the procedure would be repeated for the second egg sac. The entire procedure took about one hour. In the following hour the male was seen sticking his head between the egg sacs, moving them gently

Distribution

140

Its distribution is mainly associated with relic mountain coniferous forests, or areas where forests have existed in the past, adjoining alpine, subalpine, forest-meadow and forestmeadow-steppe belts (Kuzmin et al., 1998).

Salamanders of the Old World | Ranodon

with lateral movements of his head. In the following days the male tended to stay near the egg sacs and the female moved onto land. It is unclear whether this represents a form of clutch guarding (Thorn, 1994; Kuzmin & Thiesmeier, 2001).

Threats and conservation

The range of this species is severely fragmented and its current range continues to shrink. Human activities, including deforestation, fishing and cattle farming pose threats, but also over-exploitation for scientific purposes and the pet trade. A study of the demographic history of the six Chinese populations of Ranodon sibiricus showed that genetic diversity was extremely low, which may be indicative of dramatic population declines in the recent past and make this species particularly vulnerable to changes in its environment (Chen et al., 2012). Existing conservation measures must be taken more seriously to protect this vulnerable animal. It is considered Critically Endangered in China (Zhao, 1998; Wang & Bai, 2000) and Endangered by IUCN standards. It is urgent that effective nature reserves are created to save this species from extinction (Stuart et al., 2008; Chen et al., 2012; IUCN, 2013).

Observations in captivity

The Semirechensk Salamander has been kept in captivity. Thorn (1987, 1994) kept it for some 24-27 years and reported successful breeding over two

generations. Salamanders reared from eggs laid in April 1978 reproduced for the first time in April 1983. He kept the animals in a spacious aquarium with aquatic and terrestrial areas, at temperatures up to 18-20°C in summer and 0-3°C in winter (Raffaëlli, 2007).

Comments

The earlier Russian literature makes reference to a spermatophore deposited by the male (Paraskiv in Kuzmin & Thiesmeier, 2001) but Thorn reports no such behaviour pattern in his descriptions of the species’ sexual behaviour. Ranodon sibiricus reproduces via external fertilisation, similar to that of other Hynobiids. A spermatophore is a structure to effect internal fertilisation, as is the general rule in Salamandrids, so the structure observed by previous authors was probably something else (Thorn, 1994). Kuzmin & Thiesmeier (2001) has been the main source for this chapter. This book usefully summarises the older Russian and Chinese literature.

References

Chen et al. (2012); Dolmen et al. (1997, 1999); Fei et al.

(2006); Greven et al. (1999); IUCN (2013); Kuzmin et al. (1998); Kuzmin & Thiesmeier (2001); Raffaëlli (2007); Thorn (1987, 1994); Stuart et al. (2008); Wang & Bai (2000); Zhao (1998).

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Salamandrella Dybowski, 1870 Vomero-palatine teeth in V-shape, behind the choanae. Short body, total length less than 15 cm, tail shorter than snoutvent length. Four fingers, four toes. Lungs present. Tongue large and rounded. Egg sacs longer than length of the animal. Large number of small-sized eggs. Lives on land outside reproductive season. Pond-type natural history (Vorobyeva & Darevsky, 1994, 1995). Two species, one of them cryptic (Berman

et al., 2005; Poyarkov & Kuzmin, 2008; Matsui et al., 2008b).

Salamandrella keyserlingii Dybowski, 1870 Salamandrella tridactyla (Nikolskii, 1906)

References

Berman et al. (2005); Matsui et al. (2008b); Poyarkov &

Kuzmin (2008); Vorobyeva & Darevsky (1994, 1995).

Salamandrella keyserlingii Dybowski, 1870 | Siberian Newt Description

A moderate-sized, inconspicuous brown salamander. 10-14, exceptionally 15, costal grooves. One fold between digits when limbs adpressed against the body. Head oval; paratoid glands well-developed; gular fold present. Skin smooth. Limbs well-developed; four fingers and (usually) four toes. Tail either longer, equal to, or shorter than snout-vent length. Flattened laterally with a dorsal keel throughout, ventral keel in distal two-thirds. Vent formed by three slits converging with apex forwards, median longest. Vomerine teeth beginning behind inner edge of nares, in V-shaped series. Lungs present (Dunn, 1923; Borkin, 1999; Kuzmin & Maslova, 2003; Litvinchuk & Borkin, 2003).

Colour dull greyish-brown, lighter below; a broad gold-coloured band runs from snout to tip of tail. Inside this band, a thin dark stripe runs from neck to tail-base. The golden band becomes dark and indistinct in males in the breeding season (Goris & Maeda, 2005). Males have relatively longer and higher tails, a larger cloaca (both in length and width), and relatively longer fore legs than females. These differences are more pronounced during the reproductive period (Kuzmin, 1999). In the breeding season males show an increased head width, tail height and body mass and have a yellow pigmented patch on the throat (Hasumi, 2001b). Total length 12-16 cm (Kuzmin, 1999).

Diagnosis

A brown salamander with moderately long flattened tail; usually 13-15 costal grooves (vs usually 11-12 in Salamandrella tridactyla); four toes; a light dorsal band and

Salamandrella keyserlingii, adult male, Darhadyn Wetland, Mongolia. Photo: Masato Hasumi. 142

Salamanders of the Old World | Salamandrella

Salamandrella keyserlingii, near Ekaterinburg, Russian Federation. Photo: Burkhard Thiesmeier.

darker sides (Dunn, 1923). Labial fold absent. A large, longitudinal fontanelle present between frontals and parietals (Fei et al., 2006).

Eggs and larvae

The female produces a pair of egg sacs, connected to one another with a short mucous stalk, by which the clutch is attached to twigs and grasses. One sac of the clutch is spiraled clockwise, the other counter-clockwise. Non-spiraled, banana-shape egg sacs found in the Primorye and Khabarovskii regions belong to a separate form, recently recognised as a species and now named Salamandrella tridactyla (Kuzmin & Maslova, 2003; Berman et al., 2005; Poyarkov & Kuzmin, 2008; Matsui et al., 2008b). The size of the egg sac varies as it ages, becoming larger in the course of embryonic development and reaching a length of 28 cm and a thickness of 32 mm. One clutch may contain 27-305 eggs, distributed asymmetrically between the two egg sacs. Highest numbers of eggs were observed in Manchuria, the lowest in the extreme Northeast and the Amur and Ussuri River areas (Borkin, 1999) (In their analysis of body size / temperature relationship, Hasumi & Borkin (2012) excluded specimens from Manchuria (China) and the Amur River (Russia), so the egg numbers may not accurately reflect the egg numbers of the salamanders occurring there). The fertilised egg is grey-brown, a little brighter at the vegetal pole, and measures 1.87-2.38 mm in diameter (excluding the capsules) (Borkin, 1999). The development of embryo and larva are described and depicted in detail in Sytina et al. (1987). Depending on temperature the larvae hatch after 2-4 weeks, at 9-12 mm length, usually in May-June, and from June to early August in the extreme Northeast (Sato, 1993). Larvae are dark in colour with irregular light spots, and become darker with age. Two balancers are present. Young larvae have a peculiar elongated fin between two of the fingers (Sytina et al., 1987). Larval development up to metamorphosis takes 1.5-3 months, depending on the area. Length at metamorphosis also varies with location from 23-57 mm (Borkin, 1999). These salamanders reach sexual maturity after 5-6 years in cooler areas and after 2-3 years (males) and 3-4 years (females) in warmer areas (Hasumi, 2010; Hasumi & Borkin, 2012).

Distribution

Salamandrella keyserlingii has the widest distribution of all recent amphibian species. It is found in Russia, Kazakhstan, Mongolia, China, North Korea and Japan. Its range extends across the Ural Mountains, well into the European part of Russia, the eastern limit being formed by the Chukotski Mountains near the Bering Strait. The northern limits are the Chaunski Lowlands along the East Siberian Sea in Chukotski and the Kolyma River-Kolyuchinskaya tundra zone.

The ranges of Salamandrella keyserlingii and S. tridactyla (arrow).

The southern limits are northern Kazakhstan, the Altay and Tuva areas of southern Russia, the Hangayn Mountains in northern Mongolia, Inner Mongolia and Heilongjiang Provinces in north-eastern China. The Changbai Mountains in northern North Korea may be home to Salamandrella tridactyla. Salamandrella keyserlingii further occurs on Sakhalin Island, and some of the Kuril Islands: Paramushir, Kunashir and Shikotan Islands, as well as in the Kushiro wetlands in Hokkaido, Japan (Kang & Yoon, 1975; Sato, 1993; Borkin, 1999; Fei et al., 1999, 2006; Kuzmin & Maslova, 2003; Song, 2007). This species is characterised by a high morphological uniformity without distinct geographical variation. Recent molecular work has revealed a cryptic species, now named Salamandrella tridactyla, occurring in the basin of the Ussuri River in Primorye, including Lazovsky, Vladivostok and many other localities, southern Khabarovsk territory, Russia (Berman et al., 2005; Poyarkov & Kuzmin, 2008; Matsui et al., 2008b), as well as in the neighbouring Chinese provinces of Jilin and Heilongjiang (Poyarkov, unpubl. data) and North Korea.

Habitat

This species inhabits a wide range of different habitats, from tundra in the north to forest steppe in the south. It occurs in lowland habitats such as larch forests in river valleys, mixed forests, maritime tundras, grasslands, swamps and wetlands. Reproduction takes place in a broad range of 143

waters, from shallow, temporary puddles to permanent lakes. In tundra regions, reproduction occurs in small lakes and swamps, but in steppe and forest steppe only in large, permanent water bodies located in the flooded parts of river valleys. In taiga, this salamander uses a diverse range of water bodies, including large lakes, permanent and temporary ponds and puddles, as well as man-made ditches. In northern and mountain populations, the species uses open, well-warmed ponds where the ice melts early in spring (Kuzmin, 1999). Microhabitat use by terrestrial animals has been studied by Hasumi et al. (2009).

Behaviour

In general, the species is most numerous in taiga habitats. It is abundant in the permafrost zone and in steppe because of its high thermal tolerance and its use of relatively uniform environments in river valleys (Kuzmin, 1999). On land adults eat invertebrates (Lumbricidae, Mollusca, Aranei, Coleoptera and larval Diptera) and in the water they eat Gastropoda, Daphniidae, Coleoptera and larval Chironomidae. Larvae eat microcrustaceans, small molluscs and insects, and in some streams in the Far East they eat mainly rheophilous crustaceans (Gammaridae) (Kuzmin, 1999). Eggs, larvae and adult newts are preyed upon by a variety of animals. The main predators of eggs and larvae are aquatic insects, while adults are mainly eaten by fish, snakes, birds and mammals (Kuzmin, 1999). Hibernation starts in September-October and in August-early September in the north. This salamander hibernates in rotten (birch) trees, in holes, burrows and under logs, in places where fluctuations in temperature are relatively small. Even so, they

a

b

c

can tolerate very low temperatures in hibernacula, even down to minus 23°C for periods of a few days. In most places hibernation ends in April-May, or from the end of May to early June in the north-eastern part of their range (Kuzmin, 1999). The Siberian Newt is unique among salamanders in its freezetolerance. Adults are able to survive freezing to minus 35-40°C. Sometimes such frozen salamanders, found in the permafrost at a depth of 4-14 m, can be revived after melting. The age of one such specimen excavated from a depth of 11 m was determined as 90±15 years (Kuzmin, 1999). The animals enter the water after hibernation, in mid-April to May in the temperate zone, or at the end of May to mid-June in Arctic and Subarctic zones. In the northern part of its range reproduction may take up to one month, and about 1.5-2 weeks in the main part of its range. Group breeding is typical, the majority of females depositing their eggs within a few days, with dozens of clutches attached to the same substrate (Kuzmin, 1999). In the first stage of breeding behaviour the male moves near to the surface of the water, grasping decaying grasses or branches with its legs and swinging its tail into the water to attract a female. While doing this, it looks out for an egg-bearing female swimming its way. In the second stage, when a female touches the male’s tail, the male attempts to wrap its tail around the female and bring her closer. In the third stage, if the female is ready to lay eggs, she makes no effort to avoid being wrapped up in the male’s tail. In the fourth stage, as the male loosens his grip on the female, the female climbs up decaying grasses or branches to just below the water surface. When the female is ready to lay eggs, she arches her back, raises her tail, and

d

e

f

Reproductive behaviour sequence in the Siberian Salamander (Salamandrella keyserlingii). A. The male (non-shaded) grasps grasses or branches with his legs, near the surface of the water. The female (shaded) approaches from below. B. The male attempts to wrap his tail around the female. C. If the female is ready to lay eggs, she does not resist the male wrapping his tail round her. D. When the female is ready to lay eggs, she arches her back and presses her vent against grasses or branches. E. One or several males rush towards the released egg sacs. F. Males scramble for a position on the egg sacs to fertilise the eggs. Art: Bas Teunis, redrawn from Sato (1993).

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Salamanders of the Old World | Salamandrella

presses her vent against decaying vegetation or some other surface. In the fifth stage, this gesture by the female attracts the attention of other males in the area, which rush towards the released egg sacs. In the sixth stage, the males scramble about the egg sacs in an effort to fertilise the eggs, and the female stops moving and sinks to the bottom. Males may actually pull the egg sacs out of the female’s body. Approximately 30 seconds elapse from the time the female touches the male’s tail to the time that she releases the egg sacs (Sato, 1993). One clutch may be fathered by several males (Fang et al., 1984). After the breeding season, juveniles disperse on land and adults lead a terrestrial life. They live in burrows and under logs. Some surface activity near the breeding waters can be observed in September before the animals migrate to hibernation refugia (Hasumi & Kanda, 2007).

Threats and conservation

There are no major threats to this species. Salamandrella keyserlingii is widespread and common in Russia. It is rare in Kazakhstan, where conservation measures should be considered. The animal receives local protection in some places, such as Kushiro City and Shibecha Town in Japan (Sato, 1993; Hasumi & Kanda, 1998). This species is listed as of Least Concern (IUCN, 2013).

Observations in captivity

Salamandrella can be kept and bred in captivity if offered a long period of hibernation (Herrmann et al., 1988; Kuranova, 1991). According to an account of successful captive breeding (Timofeev & Raffaëlli, 1994), animals were kept at 3-7°C for three months and at 0-2°C during January. Sexual activity started in February at temperatures around 3-5°C. Eggs were laid in March and developed at an average water temperature of 10°C. Larvae hatched in mid-

April at 15 mm long. Metamorphosis took place at the end of July at a length of 4 cm. The juveniles measured 6-7 cm after one year.

Comments

There is a vast literature in Russian. See the volumes edited by Vorobyeva & Darevsky (1994, 1995) and references in Kuzmin (1999), Borkin (1999) and Kuzmin & Maslova (2003). Now that a genetically distinct form from Primorye has been recognised as a new species, Salamandrella tridactyla, the status of animals from neighbouring areas in China and North Korea should be re-investigated (Berman et al., 2005; Poyarkov & Kuzmin, 2008; Matsui et al., 2008b).

Mitochondrial DNA analyses indicate that Salamandrella is the sister clade to the group comprising Liua, Pseudohynobius and Batrachuperus (Peng et al., 2010). According to Pyron & Wiens (2011) Salamandrella and Pachyhynobius form one clade that is basal to all other hynobiids, except Onychodactylus. In the phylogenetic tree proposed by Weisrock et al. (2013), Salamandrella is sister to Pachyhynobius and that clade is sister to a group containing Pseudohynobius, Liua and Batrachuperus.

References

Berman et al. (2005); Borkin (1999); Dunn (1923); Fang

et al. (1984); Fei et al. (1999); Fei et al. (2006); Goris & Maeda (2005); Hasumi (2001b, 2010); Hasumi & Borkin (2012); Hasumi et al. (2009); Hasumi & Kanda (1998, 2007); Hermann et al. (1988); IUCN (2013); Kang & Yoon (1975); Kuranova (1991); Kuzmin (1999); Kuzmin & Maslova (2003); Litvinchuk & Borkin (2003); Matsui et al. (2008b); Peng et al. (2010); Poyarkov & Kuzmin (2008); Pyron & Wiens (2011); Sato (1993); Song (2007); Sytina et al. (1987); Timofeev & Raffaëlli (1994); Vorobyeva & Darevsky (1994, 1995); Weisrock et al. (2013).

Salamandrella tridactyla (Nikolskii, 1906 | Primorye Newt Description

A cryptic species, recently recognised on the basis of DNA analysis (Berman et al., 2005; Poyarkov & Kuzmin, 2008; Matsui et al., 2008b). Cannot be distinguished from Salamandrella keyserlingii on the basis of external characters. For a description see under S. keyserlingii. In populations of S. tridactyla from Primorye the number of costal grooves (11-12) is lower than in S. keyserlingii (11-14/15) and the number of trunk vertebrae is lower also (Litvinchuk & Borkin, 2003).

Diagnosis

A brown salamander with moderately long flattened tail; usually 11-12 costal grooves; four toes; a light dorsal band and darker sides.

Differences between Salamandrella keyserlingii and animals from the Primorye region, now referred to the new species S. tridactyla, concern the shape of the egg sacs, number of eggs, duration of larval development, reproductive habitat, genome size, number of costal grooves and trunk vertrebrae (see references in Litvinchuk & Borkin, 2003) and DNA (Berman et al., 2005; Poyarkov & Kuzmin, 2008; Matsui et al., 2008b).

Eggs and larvae

Females produce a pair of egg sacs, connected to one another with a short mucous stalk, by which the clutch is attached to twigs and grasses. Whereas in Salamandrella keyserlingii the egg sacs are spiraled, the clutches 145

meadows. Reproduction takes place in a broad range of water bodies, from shallow temporary puddles to permanent lakes. Although generally a lowland species breeding in standing water, in Primorye it also breeds in roadside ditches and shallow brooks with running water. It inhabits mountainous terrain up to ca. 900 m altitude (Kuzmin & Maslova, 2003).

Behaviour

Adults enter the water after hibernation. In Khabarovsk and Primorye the breeding season starts in early April and lasts until May-June. Courtship behaviour is probably similar to that of Salamandrella keyserlingii. Egg laying, hatching of the larvae and metamorphosis is earlier than in S. keyserlingii from southern Sakhalin, Zabaykalskiy, central Yakutia and northern Mongolia. Juvenile salamanders of S. tridactyla are much smaller than of S. keyserlingii (Sato, 1993).

Salamandrella tridactyla, Ussuriysk Nature Reserve, Russian Federation. Photo: Burkhard Thiesmeier.

Threats and conservation Observations in captivity

belonging to populations of S. tridactyla in the Primorye and Khabarovsk regions contain egg sacs which are bent in a bananashape (Kuzmin & Maslova, 2003). These egg sacs contain generally fewer eggs than the spiraled ones, with egg sacs from the Khabarovsk area containing 106-131 eggs on average (Sato, 1993).

Distribution

Primorye (Lazovsky, Vladivostok and other localities), southern Khabarovsk area. The precise border between the ranges of Salamandrella tridactyla and S. keyserlingii is not yet known (Matsui et al., 2008b).

Habitat

In the Primorye region this salamander lives in river valleys, groves, bushes, areas with dark-coniferous taiga, and

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Salamanders of the Old World | Salamandrella

There are no major threats

to this species. No published information.

Comments

There is a vast literature in Russian on S. keyserlingii, some of it specifically referring to the salamanders from the Primorye region, which according to various older accounts differed from S. keyserlingii in other parts of its range. See the volumes edited by Vorobyeva & Darevsky (1994, 1995) and references in Kuzmin (1999), Borkin (1999) and Kuzmin & Maslova (2003).

References

Berman et al. (2005); Borkin (1999); Kuzmin (1999);

Kuzmin & Maslova (2003); Litvinchuk & Borkin (2003); Matsui et al. (2008b); Poyarkov &Kuzmin (2008); Sato (1993); Vorobyeva & Darevsky (1994, 1995).

adults hatch directly from the eggs (Larson et al., The family Plethodontidae is by far the largest 2006b). salamander family of the world, with more than 376 recognised species. Salamanders in this family The European lungless salamanders are presently are commonly called ‘lungless salamanders’ and are widely distributed in the Americas, with a small grouped in two genera, Atylodes with one species, and number of species in southeastern France, north and Speleomantes with seven species. Their taxonomic central Italy and Sardinia, and one species in Korea. history is complicated and their classification and All plethodontid salamanders are lungless and nomenclature is subject to debate (Wake et al., 2005; breathe through their moist skin. Fertilisation is Frost, 2013). The Korean genus Karsenia is monotypic internal by means of a spermatophore. Plethodontids and sister to a clade containing the North American are unique among salamanders in having narrow Hydromantes and European Atylodes and Speleomantes grooves between each nostril and the upper lip, called (Min et al., 2005; Vieites et al., 2007). nasolabial grooves. Costal grooves are pronounced. Most plethodontids are completely terrestrial and lay References Frost (2013), Larson et al. (2006b), eggs on land. They lack aquatic larvae and miniature Min et al. (2005), Vieites et al. (2007), Wake et al. (2005).

Plethodontidae Gray, 1850

Speleomantes supramontis, Dorgali, Sardinia. Photo: Max Sparreboom.

147

Atylodes Gistel, 1868 Atylodes was considered a synonym of Hydromantes (sensu lato) prior to its recognition as a subgenus, and subsequently as a genus. See Frost (2013) for a discussion of the intertwined taxonomic histories of Atylodes, Hydromantes and Speleomantes, and Vieites et al. (2007) for theories on the historical biogeography of plethodontids and their colonisation of Eurasia. All the available evidence suggests that the taxon that occurs in southwestern Sardinia, known as Speleomantes genei, is widely divergent from the other European lungless salamanders included in that genus, in their proteins, mitochondrial DNA, sex chromosomes, and to a minor extent in morphology. If these differences justify separation at the genus level, the sister taxon to Speleomantes should be named Atylodes, an old, available name (Wake et al., 2005). Atylodes genei is generally considered to have split off from the ancestral stock well before the other species. This taxon is probably the most basal European plethodontid species, but the question has not yet been resolved with confidence (Carranza et al., 2008; Van der Meijden et al., 2009). Like the Speleomantes species, Atylodes is largely nocturnal. These salamanders are active in the dark, at temperatures

between 5 and 15°C and at air humidity between 70 and 100%. During dry and hot periods they live underground or in caves, often but not exclusively in karstic and calcareous soils. In caves, they frequently occupy areas close to the entrance, where most of the insects on which they prey are found. They eat all sorts of small prey, including molluscs, arthropods, ants and millipedes. The tongue can be projected with great precision and speed. With their large feet, which are partially webbed, and assisted by a prehensile tail, these salamanders are perfectly adapted to climb vertical rock faces and stony walls (Adams & Nistri, 2010). They are protected against predators to some extent by a secretion of the glands in the skin (Brizzi et al., 1991), but may fall victim to, for instance, snakes (Natrix) and slowworms (Anguis fragilis) (Lanza et al., 2007).

Atylodes genei (Temminck & Schlegel, 1838)

References

Adams & Nistri (2010); Brizzi et al. (1991); Carranza

et al. (2008); Frost (2013); Lanza et al. (2007); Van der Meijden et al. (2009); Vieites et al. (2007); Wake et al. (2005).

Atylodes genei (Temminck & Schlegel, 1838) | Gené’s Cave Salamander Description

148

A small salamander, rather robust with moderately broad head. Head flattened, a little longer than wide, and wider than trunk. Snout truncated. Tongue significantly longer than in continental Speleomantes, but shorter than in Sardinian Speleomantes. Eyes large and protruding. In young specimens the nostrils are particularly large, and have a small tentacle under the lower side. Adults have a more or less distinct swelling in the area of the nasolabial groove. Gular fold present. No paratoids and no labial fold. Body short, slender, cylindrical, with 13 trunk vertebrae. Tail cylindrical, approximately same length as snout-vent length or a little shorter, tapering to a sharp point. Limbs well-developed, with four fingers and five toes, clearly truncate and often enlarged at tips. Foot large but significantly smaller than in Sardinian Speleomantes species. Fingers webbed at the base, toes half-webbed. Skin smooth (Thorn, 1969; Lanza et al., 1995, 2007; Lanza, 1999e).

developed dark stippling than in Sardinian Speleomantes species. In young specimens dorsal parts are often more or less extensively greenish, with a metallic sheen (Thorn, 1969; Lanza et al., 1995).

Dorsal parts dark brown to blackish, often with a more or less brown, olive-green or, rarely, ochre-yellow marbling, sprinkled with whitish dots. Ventral side less pigmented, uniformly bright or brown-grey. The purplish aspect of the belly is due to the interior organs that are visible through the skin, which is more or less transparent. Ventral side usually with a more

Total length 115 mm in males and 124 mm in females (Lanza et al., 1995).

Salamanders of the Old World | Atylodes

Sexual dimorphism not pronounced. Premaxillary teeth slightly enlarged in male (Greven et al., 2004). Mental gland under the chin in the male is poorly visible outside the breeding season. No cloacal swelling. Cloacal opening is a longitudinal fold, situated a little more backward in the male than in the female (Thorn, 1969). Two different forms have been described, that may be species or subspecies, based on genetic differences. The two forms cannot be distinguished morphologically (Lanza et al., 2007). Their exact range boundaries are unclear.

Diagnosis

A small, dark-coloured, lungless salamander. Canthus rostralis missing or poorly developed, giving the snout a rounded appearance. Foot large, but smaller than in other

Atylodes genei, Fiuminimaggiore, Sardinia. Photo: Max Sparreboom.

Atylodes genei, Domusnovas, Sardinia. Photo: Max Sparreboom.

Atylodes genei, Fiuminimaggiore, Sardinia. Photo: Max Sparreboom.

Sardinian species. Tongue longer than in continental species of Speleomantes, but shorter than in Sardinian species. Heteromorphic sex chromosomes absent. Genetically well differentiated, showing a higher number of diagnostic loci than in Speleomantes species, from 16- 24 (Lanza et al., 1995).

Eggs

Like species of Speleomantes, Atylodes genei reproduces through direct development of a small number of terrestrial eggs. The female stays with the eggs until they hatch as fully metamorphosed young salamanders. Papinuto (in lit.) has recorded the behaviour of a female and her clutch of ten eggs, from which juveniles hatched in August, 4.5 months after the clutch was discovered in a mine gallery near Domusnovas.

The female sporadically moved away from the eggs. On returning to the clutch she would hold it with a forelimb and keep the clutch raised with her tail. During this time the egg diameter changed from 5-6 to 10 mm. After hatching, the eight newborn salamanders, 20-25 mm long, stayed close to, or even on their mother, leaving the spot about two weeks later (Lanza et al., 2006; 2007).

Distribution

This species is endemic to the region known as Sulcis-Iglesiente, Province of Cagliari, southwestern Sardinia (Lanza et al., 1995). The form provisionally termed form A occurs in the more northern part, and form B in the Carbonia – Barbusi – Monte Tasua area. Specimens belonging to A. genei B 149

Behaviour

Very little is known about the behaviour of this species. In summer, salamanders can be found active on the walls of caves at a temperature of 14°C and an air humidity of 94%. Atylodes genei and Speleomantes species can project their tongue up to a distance of about 4-5 cm to catch prey. Atylodes genei is particularly fast in this respect. During tongue projection towards distant prey, the tongue is shot ballistically and the tongue skeleton leaves the body of the salamander entirely (Deban et al., 2007). This species is able to cast off its tail as a defense against predators (Romano et al., 2010). Courtship has been observed in captivity, but detailed descriptions of the courtship and mating have never been recorded. It appears to be generally similar to that observed in species of Speleomantes. The male mounts the female, clasping her with fore and hind legs. He makes rubbing movements during which he applies his mental gland to the snout of the female. Both partners make undulating movements with their tail but spermatophore transfer was not observed (Lanza et al., 2006).

Threats and conservation The range of Atylodes genei.

In spite of deforestation of its natural habitat, the species has persevered. It is considered Vulnerable given its limited range (Stuart et al., 2008; IUCN, 2013).

Observations in captivity were found at a locality more than 17 km outside its previously known range (Van der Meijden et al., 2009).

Habitat

The species is found in humid outcrops, caves, crevices and forested areas at altitudes between 8 and 650 m, and possibly occurs at higher altitudes (Lanza et al., 2006). It is generally common within its range, except in the Carbonia – Barbusi – Monte Tasua area, where (sub)species B is found (Lanza et al., 2007).

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Salamanders of the Old World | Atylodes

Some observations in captivity have been reported by Lanza et al. (2007). The salamanders are difficult to keep and need a cool and dark terrarium. In exceptional cases captive individuals have lived for over six years. Temperatures above 25°C were lethal (Thorn,1969).

References

Deban et al. (2007); Greven et al. (2004); IUCN (2013);

Lanza (1999e); Lanza et al. (1995, 2006, 2007); Romano et al. (2010); Stuart et al. (2008); Thorn (1969); Van der Meijden et al. (2009); Vieites et al. (2007).

Karsenia Min, Yang, Bonett, Vieites, Brandon & Wake, 2005 Karsenia is a monotypic genus of the family Plethodontidae. It was created to hold the species Karsenia koreana, the first plethodontid salamander species found in Asia. Lungs absent, pterygoid bone in adults absent; large patches of paravomerine teeth, and nasolabial groove. Its discovery in southwestern Korea challenges our understanding of the biogeographic history of the family. Plethodontidae is the largest salamander

family, with the vast majority of genera and species occurring in the Americas, and two genera containing a small number of species in southern Europe (Speleomantes and Atylodes).

Karsenia koreana Min, Yang, Bonett, Vieites, Brandon & Wake, 2005

References

Min et al. (2005).

Karsenia koreana Min, Yang, Bonett, Vieites, Brandon & Wake, 2005 |

Korean Crevice Salamander

Description

This follows the original description by Min et al. (2005). A small salamander, rather robust with moderately broad head. Tail approximately same length as snout-vent length or a little longer. Nasolabial groove in swollen protuberance on upper lip, relatively inconspicuous. Eyes relatively small. Tongue attached at front, but highly protrusible. Snout more or less rounded, nostrils small. Gular fold evident. 14-15 costal grooves. Tail round at the base, slightly laterally compressed towards the posterior, tapering to a sharp point. Limbs and digits short. When adpressed along the body, 3-4 costal folds are left uncovered. Fifth toe shorter than fourth. Digits have slight basal webbing. Approximately 45-50 maxillary teeth and 15-20 vomerine teeth. A large, paired patch of paravomerine teeth (about 150) present on palate.

Colour dark brown along the flanks; frequently a broad dorsal reddish or brownish stripe of varying intensity from tip of snout to tip of tail. Many small silvery dots and flecks on the sides. Venter grey, lighter than flanks, speckled with tiny whitish spots. Females have a more rounded snout than males. Total length 8-9 cm.

Diagnosis

A small, dark-coloured, lungless salamander with short limbs, nasolabial grooves in the male and 14-15 costal grooves.

Karsenia koreana, near Daejeon (type locality), Korea. Photo: Max Sparreboom. 151

Most individuals were found under small rocks or rock flakes scattered among larger boulders on fine-grained soil (IUCN, 2013; AmphibiaWeb, 2013). The species probably uses its solid skull to help it seek refuge in tight spaces between rocks (Buckley et al., 2010).

Behaviour

This species is thought to be exclusively terrestrial. Breeding is presumed to be by direct development, but observations are lacking (IUCN, 2013).

Threats and conservation

This species is common within its range. Even so, little is known about its general biology or conservation status (AmphibiaWeb, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments The range of Karsenia koreana.

Eggs

No Information. It is assumed that eggs are laid on land and develop directly as in other plethodontid salamanders.

Distribution

This species is found at relatively low elevations in southern to mid-western South Korea, where it has been found at more than 20 sites. Type locality is the area near Daejeon, Chungcheongnam-do, Korea, at 210 m (Min et al., 2005; IUCN, 2013; AmphibiaWeb, 2013).

Habitat

This species inhabits damp, mossy talus slopes and limestone rockslides in 15-20 year-old hardwood and mixed hardwood/pine forests. It has even been found in a city park.

The spectacular discovery of a plethodontid salamander in Asia has led to new hypotheses concerning the colonisation of Eurasia by plethodontids (Vieites et al., 2007). A specimen of this species was discovered in the collection of the Institute for Amphibian Biology, Hiroshima University, Japan. It was collected in 1971 from Mt. Gyeryong by a joint Korean-Japanese research team, but had gone previously unnoticed (Nishikawa, 2009). The genome size of Karsenia is relatively large (karyotype 2N=28), and resembles that of the geographically closest plethodontids from western North America, especially species of the genus Hydromantes (Sessions et al., 2008).

References

AmphibiaWeb (2013); Buckley et al. (2010); IUCN (2013);

Min et al. (2005); Nishikawa (2009); Sessions et al. (2008); Vieites et al. (2007).

Karsenia koreana, habitat near Daejeon (type locality), Korea. Photo: Max Sparreboom. 152

Salamanders of the Old World | Karsenia

Speleomantes Dubois, 1984 The European plethodontid salamanders are contained in the genera Speleomantes and Atylodes. They are closely related to the salamanders of the American genus Hydromantes, to which they were previously assigned. The intertwined taxonomic histories of Atylodes, Hydromantes and Speleomantes are complicated (Wake et al., 2005; Frost, 2013). The relationships among European cave salamanders and their historical biogeography are not yet fully resolved, but Atylodes (formerly placed in Hydromantes or Speleomantes) genei appears to be basal to the other European plethodontid salamanders, and the eastern Sardinian species appear to be more closely related to the mainland species Speleomantes strinatii, S. ambrosii and S. italicus (Carranza et al., 2008; Vieites et al., 2007; Van der Meijden et al., 2009). In spite of their morphological similarities, there is a deep genetic divergence among all Sardinian cave salamander species, which can largely be attributed to the effects of mountains and cave systems that act as barriers to gene flow (Chiari et al., 2012). The European cave salamanders are similar in general appearance, and are most reliably distinguished using biochemical techniques. They are characterised by a slender body with a cylindrical tail, just under half the total length. The head is broad and rounded and the eyes are large. The tongue can be protruded with great precision and speed to catch prey up to a distance of about 40-50 mm, further than any other European salamander. Toes stubby and partially webbed on the hind feet. Sexes similar in appearance, but males have an oval-shaped glandular swelling on the chin, the mental gland, and slightly enlarged premaxillary teeth. A pair of small sensory tentacles may also be visible on the upper lip. These are associated with a shallow groove running from the nostril to the lip (the nasolabial groove) (Griffiths, 1996; Lanza, 1999a, 1999c; Lanza et al., 1995; 2006).

These salamanders are active in the dark, at temperatures between 5-15°C and at humidities between 70-100%. During dry, hot periods they live underground or in caves, often but not exclusively in calcareous soil. In caves they frequently occupy areas close to the entrance, where most insects are found on which they prey. They eat all sorts of small prey including molluscs, arthropods, ants and millipedes. With their large feet, which are partially webbed, and assisted by a prehensile tail, these salamanders are perfectly adapted to climb vertical rock faces, rock crevices and stony walls (Adams & Nistri, 2010). They are protected against predators to some extent by a secretion of the glands in the skin (Brizzi et al., 1991), but may fall victim to, for instance, snakes (Natrix) and slow worms (Anguis fragilis) (Lanza et al., 2007). Fungicidal skin secretions appear to confer resistance to Chytridiomycosis (Pasmans et al., 2013).

Speleomantes ambrosii (Lanza, 1955) Speleomantes flavus (Stefani, 1969) Speleomantes imperialis (Stefani, 1969) Speleomantes italicus (Dunn, 1923) Speleomantes sarrabusensis Lanza, Leo, Forti, Cimmaruta, Caputo & Nascetti, 2001

Speleomantes strinatii (Aellen, 1958) Speleomantes supramontis (Lanza, Nascetti & Bullini, 1986)

References

Adams & Nistri (2010); Brizzi et al. (1991); Carranza

et al. (2008); Chiari et al. (2012); Frost (2013); Griffiths (1996); Lanza (1999a, 1999c); Lanza et al. (1995, 2006, 2007); Pasmans et al. (2013); Van der Meijden et al. (2009); Vieites et al. (2007); Wake et al. (2005).

Speleomantes ambrosii (Lanza, 1955) | Ambrosi’s Cave Salamander Description

A moderately stout salamander. Head flattened and oval in dorsal view. Snout more or less truncate to rounded, projecting over the mouth, especially in the male. Nostrils closer to snout tip than to the eye. Tongue longer than in Speleomantes italicus and shorter than in the large Sardinian species. Tail oval in cross section, slightly less than half the total length but a little shorter in females than in males, gradually tapering. Moderately bulging eyes. Gular fold present. No paratoids and no labial fold. Body short, subquadrangular in cross section, with usually 11 costal grooves. Limbs short, but well-developed, with four fingers and five toes. Fingers and toes more or less flattened, overlapping in adult males when appressed,

separated by a short gap in adult females. Finger and toe-tips hardly enlarged distally, more or less truncated. Vestigial webbing between toes. Skin smooth (Lanza et al., 1995, 2007; Lanza, 1999b). Colouration highly variable. Dark ground colour on back; occasionally two dorsolateral stripes or blotches on trunk and tail, or a reticulated design; spots present or absent. Dorsal pattern from monochrome to polychrome with different colours and colour nuances. Sometimes a more or less irregular dark V- or X-shaped mark behind the eyes. Ventral colour nutbrown to dark bistre, with small white spots (Lanza et al., 1995, 153

Speleomantes ambrosii ambrosii, north of La Spezia. Photo: Joachim Nerz.

2007; Lanza, 1999b). In young specimens dorsal parts are often more or less extensively greenish, with a metallic sheen. Newborn animals have much larger nostrils than older animals (Lanza et al., 1995). Sexual dimorphism not pronounced. Premaxillary teeth slightly enlarged in male (Greven et al., 2004). Mental gland under the chin in the male is also visible outside the breeding season. Cloacal swelling present in male, much less so in female.

Genetic research has revealed the existence of two subspecies: Speleomantes ambrosii ambrosii and S. a. bianchii, which are in part parapatric. The two forms cannot be distinguished morphologically with certainty. Speleomantes a. ambrosii occurs west of the Magra River; the populations parapatric with S. a. bianchii almost always have a brown to black back, apart from two light, more or less discontinuous dorsolateral stripes. Speleomantes a. bianchii occurs east of the Magra River; when parapatric with S. a. ambrosii it usually lacks the typical S. a. ambrosii colour

Speleomantes ambrosii bianchii, Upper Frigido River. Photo: Joachim Nerz. 154

Salamanders of the Old World | Speleomantes

pattern (Lanza et al., 2007). However, genetic research suggests that this subspecies may actually belong to S. italicus, rather than to S. ambrosii (Carranza et al., 2008). Total length 116 mm in males and females (Lanza et al., 2007; females 124 mm according to Lanza et al., 1995). On average adult females are 10% longer than males (Salvidio & Bruce, 2006).

Diagnosis

A small dark-coloured, lungless salamander. Colour highly variable. Somewhat blunt canthus rostralis almost always present. Speleomantes ambrosii cannot be distinguished from S. strinatii on morphological characteristics alone (Lanza, 1999b; Lanza et al., 1995).

Eggs

Like other species of Speleomantes, S. ambrosii reproduces through direct development of a small number of terrestrial eggs. Most reports actually refer to other species, especially S. strinatii (Lanza, 1999b). Despite the lack of direct evidence, it has been inferred that continental Speleomantes lay their eggs underground, presumably in holes safe from dangerous environmental extremes (Lanza et al., 2006). Speleomantes ambrosii bianchii, habitat, Upper Frigido River. Photo: Joachim Nerz.

sea level to around 2,300 m (IUCN, 2013). Like the other Speleomantes species, it can be found in various habitats, from forest to semi-barren rocky sites, on the surface as well as in caves.

Behaviour

Very little is known of the behaviour of this species. It is most probably similar to that of the other Speleomantes and Atylodes species, especially Speloeomantes strinatii (Lanza et al., 1995; 2007). Continental Speleomantes lead an active life between 2.6-22.0°C and at a relative humidity between 67-100%, whereas Sardinian species probably tolerate slightly higher temperatures. In summer the highest activity was observed inside caves, and in winter outside caves (Lanza et al., 2006).

Threats and conservation The range of Speleomantes ambrosii.

Distribution

This species is restricted to scattered localities in La Spezia Province, northwestern Italy (Lanza et al., 2007; IUCN, 2013).

Habitat

This species inhabits humid outcrops, caves, crevices and forested areas in the vicinity of streams, at altitudes from

Although relatively common, this species is considered Near Threatened due to its restricted range (IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

References

Carranza et al. (2008); Greven et al. (2004); IUCN (2013);

Lanza (1999b); Lanza et al. (2007); Lanza et al. (1995); Lanza et al. (2006); Salvidio & Bruce (2006).

155

Speleomantes flavus (Stefani, 1969) | Monte Albo Cave Salamander Description

A moderately stout salamander. Head flattened and oval in dorsal view. Snout more or less truncate to rounded, projecting over the mouth, especially in the male. Nostrils closer to snout tip than to the eye. Tongue significantly longer than in all other Speleomantes, except Speleomantes supramontis. Tail oval in cross section, slightly less than half the total length but a little shorter in females than in males, gradually tapering. Moderately bulging eyes. Gular fold present. No paratoids and no labial fold. Limbs well-developed, with four fingers and five toes. Finger and toe-tips more or less truncate and often enlarged at tips. Vestigial webbing between toes. Skin smooth (Lanza et al., 1995, 2007; Lanza, 1999d). Colour of upperparts extremely variable: ground colour dark brown to blackish with blotches or marblings which are yellowish, ochre, or sometimes greenish. Some individuals are yellow above. Ventral parts usually bright, sometimes translucent. Underside usually plain, sometimes with brown spots. In young specimens dorsal parts are often more or less extensively greenish, with a metallic sheen. Newborn animals have much larger nostrils than older animals (Lanza et al., 1995).

Diagnosis

Sexual dimorphism not pronounced. Premaxillary teeth slightly enlarged in male (Greven et al., 2004). Mental gland under the chin in the male is also visible outside the breeding season. Cloacal swelling present in male, much less so in female.

Eggs

The range of Speleomantes flavus.

A fairly large lungless salamander. No canthus rostralis. Tongue longer than in other Speleomantes species, but shorter than in Speleomantes supramontis. Foot large (Lanza et al., 1995, 2007).

Total length 127 mm in males and 146 mm in females (Lanza et al., 1995; 2007).

Speleomantes flavus, Monte Albo, Sardinia. Photo: Max Sparreboom. 156

Salamanders of the Old World | Speleomantes

Like other species of Speleomantes, Speleomantes flavus probably reproduces through direct development of a small number of terrestrial eggs, but definitive observations are lacking.

Distribution

Threats and conservation

Habitat

Observations in captivity

This species is endemic to northeastern Sardinia, the Monte Albo chain and hills between Siniscola and the Posada River, Province of Nuoro (Lanza et al., 2007; IUCN, 2013).

This species inhabits a variety of habitats, prefering those with only minor fluctuations in temperature and humidity such as rocky outcrops, caves, crevices and forested areas between 40-1,050 m altitude. It has been found active in caves at temperatures of 11-18°C and a humidity of 75-94% (Lanza et al., 2007).

Behaviour

This species is entirely terrestrial and nocturnal. There is very little information on its life history and behaviour. It is assumed to be similar to other Speleomantes species (Lanza, 1999d; Lanza et al., 2007).

Speleomantes flavus is not endangered but considered Vulnerable given its limited range (IUCN, 2013).

There is no information regarding the behavior of this species.

Comments

Speleomantes flavus, S. supramontis and S. imperialis are often attacked by leeches (Batracobdella algira, Lanza et al., 2006, 2007).

References

Greven et al. (2004); IUCN (2013); Lanza (1999d);

Lanza et al. (1995, 2006, 2007).

Speleomantes imperialis (Stefani, 1969) | Odorous Cave Salamander Description

A moderately stout salamander. Head flattened and oval in dorsal view. Snout more or less truncate to rounded, projecting over the mouth, especially in the male. Nostrils closer to snout tip than to the eye. Tongue significantly longer than in continental Speleomantes, significantly shorter than in Speleomantes supramontis and S. flavus. Tail oval in cross section, slightly less than half the total length; a little shorter in females than in males, and gradually tapering. Moderately bulging eyes. Gular fold present. No paratoids and no labial fold. Limbs well-developed, with four fingers and five toes. Finger and toe-tips more or less truncate and often enlarged at tips. Vestigial webbing between toes. Skin smooth (Lanza et al., 1995, 2007; Lanza, 1999f).

Colour of upperparts moderately variable: ground colour dark brown to blackish with blotches or marblings which are yellowish, ochre, or sometimes greenish. Ventral parts usually bright with brown spots. Spotting on underside more pronounced than in S. flavus. As in the latter species, there may be a dark V-, inverted V- or X-shaped mark on the neck. In young specimens dorsal parts are often more or less extensively greenish, with a metallic sheen. Newborn animals have much larger nostrils than older animals (Lanza et al., 1995). Sexual dimorphism not pronounced. Premaxillary teeth slightly enlarged in the male (Greven et al., 2004). Mental gland under the chin in the male is also visible outside the breeding season. Cloacal swelling present in male, much less so in female.

Speleomantes imperialis, Villasalto, Sardinia. Photo: Max Sparreboom. 157

Total length 133 mm in males and 150 mm in females (Lanza et al., 1995; 2007).

Diagnosis

A fairly large lungless salamander. No canthus rostralis. Tongue longer than in continental Speleomantes species, but shorter than in Speleomantes supramontis and S. flavus. Foot large, but smaller than in S. flavus and S. supramontis. Emits strong scent when handled; scent emission absent in populations close to Lake Omodeo (Lanza et al., 1995, 2007).

Eggs

Like other Speleomantes species, Speleomantes imperialis reproduces through direct development of a small number of terrestrial eggs. A clutch laid in January, consisting of 6 eggs, 5-6 mm in diameter, was described by Mutz (1998), who bred this species in captivity at temperatures of 8-12°C in winter and up to 15°C in summer. The female stayed close to the eggs all the time except for brief excursions to find food. Two eggs were eaten by the female and four juveniles hatched in July at total lengths of 26.0-28.2 mm. The juveniles and their mother stayed close together at the nest site until two weeks after hatching.

areas between 7-1,170 m altitude. The species has been found active in caves at temperatures of 14-18°C and humidities of 94-95% (Lanza et al., 2007).

Behaviour

This species is entirely terrestrial and nocturnal. Like other Speleomantes species, Speleomantes imperialis projects its tongue to capture prey up to 6 cm away. During tongue projection to a distant prey, the tongue is shot ballistically and the tongue skeleton leaves the body of the salamander entirely (Deban & Dicke, 2004). Mating and egg-laying certainly take place in winter and spring, but probably all year round as well. In some populations the animals were observed at high densities (Lanza, 1999f; Lanza et al., 2007). Courtship and spermatophore deposition have not been observed.

Threats and conservation

Speleomantes imperialis is abundant in its range and not endangered. It is considered Near Threatened given its limited range (IUCN, 2013).

Observations in captivity

Detailed observations on the development of the eggs and parental care were made on animals kept in a terrarium placed in a refrigerator (Mutz, 1998).

Comments

Speleomantes flavus, S. supramontis and S. imperialis are often attacked by leeches (Batracobdella algira, Lanza et al., 2006, 2007).

References

Deban & Dicke (2004); Greven et al. (2004); IUCN (2013);

Lanza (1999f); Lanza et al. (1995, 2006, 2007); Mutz (1998).

Speleomantes imperialis, juvenile, near Ulassai, Sardinia. Photo: Sergé Bogaerts.

Distribution

This species is endemic to central, centraleastern and southeastern Sardinia, in the provinces of Nuoro, Oristano and Cagliari (Lanza et al., 2007; IUCN, 2013).

Habitat

This species occurs in a variety of habitats, as long as temperatures are moderate and humidity is high. It prefers habitats with only minor fluctuations in temperature and humidity such as humid outcrops, caves, crevices and forested

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Salamanders of the Old World | Speleomantes

The range of Speleomantes imperialis.

Speleomantes italicus (Dunn, 1923) | Italian Cave Salamander Description

A moderately stout salamander. Head flattened and oval in dorsal view. Snout more or less truncate to rounded, projecting over the mouth, especially in the male. Nostrils closer to snout tip than to the eye. Tongue shorter than in Speleomantes strinatii and the large Sardinian species. Tail oval in cross section, slightly less than half the total length but a little shorter in females than in males, and gradually tapering. Moderately bulging eyes. Gular fold present. No paratoids and no labial fold. Body short, subquadrangular in cross section, usually with 11 costal grooves. Limbs short, but well-developed, with four fingers and five toes. Fingers and toes more or less flattened, overlapping in adult males when appressed, separated by a short gap in adult females. Finger and toe-tips hardly enlarged distally, more or less truncated. Vestigial webbing between toes. Skin smooth (Lanza et al., 1995, 2007; Lanza, 1999g).

Total length 112 mm in males and 120 mm in females (Lanza et al., 2007).

Diagnosis

A small dark-coloured, lungless salamander. Somewhat blunt canthus rostralis usually present. Tongue shorter than in other species. Digits bluntly pointed to moderately truncate at tips. Foot usually a little smaller than in Speleomantes ambrosii and S. strinatii (Lanza et al., 1995).

Eggs

Like other Speleomantes species, Speleomantes italicus reproduces through direct development of a small number of terrestrial eggs. Despite the lack of direct evidence from field observations, it has been inferred that continental Speleomantes lay their eggs underground, presumably in holes safe from dangerous environmental extremes (Lanza et al., 2006).

Colour highly variable as in all Speleomantes, especially in the northwestern part of its range where there is genetic introgression with S. ambrosii bianchii (Lanza et al., 2007). Back light brown to black, often with spotted, blotched, striped or reticulated pattern; spots and marble pattern often more pronounced on tail. Ventral side more or less dark brown, dotted with grey spots. Different patterns can occur together in the same population. In young specimens dorsal parts are often more or less extensively greenish, with a metallic sheen. Newborn animals have much larger nostrils than older animals (Lanza et al., 1995). Sexual dimorphism not pronounced. Premaxillary teeth slightly enlarged in male (Greven et al., 2004). Mental gland under the chin in the male is also visible outside the breeding season. Cloacal swelling present in male, much less so in female.

The range of Speleomantes italicus.

Distribution

Speleomantes italicus is a northern and central Apennine endemic, ranging from the province of Reggio Emilia (Emilia-Romagna) and Lucca (Tuscany) southwards to the province of Pescara (Abruzzi) (Lanza et al., 1995; IUCN, 2013).

Habitat

Speleomantes italicus, east of Cardoso. Photo: Joachim Nerz.

The species occurs in a variety of habitats, as long as temperatures are moderate and humidity is high. It prefers habitats with only minor fluctuations in temperature and humidity such as humid outcrops, caves, crevices and forested areas between 80-1,598 m altitude. It is not limited to calcareous 159

soils, but to the kind of rocky ground that permits a subterranean life during the warm, dry season. In some areas these salamanders will even climb trees up to 3.5 m high (Casali et al., 2005; Lanza et al., 2007).

at temperatures between 2.6-17.5°C and relative humidities of 67-100% (Lanza et al., 2007). Activity peaks during spring and autumn after rainfall, at temperatures between 13-15°C, and drops off in winter and summer. They feed on a variety of invertebrate prey such as small Gasteropoda, Coleoptera, and the larvae of Lepidoptera and Isopoda. They can detect prey by smell in total darkness, but usually prefer areas in caves that receive some light and where they can see their prey directly (Lanza et al., 1995). There are some fragmentary observations of courtship behaviour (Lanza et al., 2006), but detailed descriptions of courtship and mating are lacking. Their behaviour appears to be generally similar to the Sardinian species of Speleomantes. The male mounts the female, clasping her with fore and hind legs. He makes rubbing movements during which he applies his mental gland to the snout of the female. Both partners make undulating movements with their tail. Spermatophore transfer has not been observed.

Threats and conservation

Speleomantes strinatii is common within its range though less so in the southernmost part, and is not endangered. It is considered Near Threatened given its limited range (IUCN, 2013).

Observations in captivity

Speleomantes italicus, habitat, south-east of Massa. Photo: Joachim Nerz.

There are no reports of this

species being kept in captivity.

Behaviour

These salamanders are entirely terrestrial, nocturnal and active practically all year round. They are active

References

Casali et al. (2005); Greven et al. (2005); IUCN (2013);

Lanza (1999g); Lanza et al. (1995, 2006, 2007).

Speleomantes sarrabusensis Lanza, Leo, Forti, Cimmaruta, Caputo &

Nascetti, 2001 | Sarrabus Cave Salamander

Description

A moderately stout salamander. Head flattened and oval in dorsal view. Snout more or less truncate to rounded, projecting over the mouth, especially in the male. Nostrils closer to snout tip than to the eye. Tongue significantly longer than in continental Speleomantes, and significantly shorter than in Speleomantes supramontis and S. flavus. Tail oval in cross section, slightly less than half the total length but a little shorter in females than in males, and gradually tapering. Moderately bulging eyes. Gular fold present. No paratoids and no labial fold. Limbs well-developed, with four fingers and five toes. Finger and toe-tips more or less truncate and often enlarged at tips. Vestigial webbing between toes. Skin smooth (Lanza et al., 1995, 2007; Lanza, 1999f). Colour of upperparts variable as in S. imperialis: ground colour brown to blackish with blotches or marblings which are

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Salamanders of the Old World | Speleomantes

yellowish, ochre, or sometimes greenish. Ventral parts usually lighter with brown spots. In young specimens dorsal parts are often more or less extensively greenish, with a metallic sheen. Newborn animals have much larger nostrils than older animals (Lanza et al., 1995). Sexual dimorphism not pronounced. Premaxillary teeth slightly enlarged in male (Greven et al., 2004). Mental gland under the chin in the male is also visible outside the breeding season. Cloacal swelling present in male, much less so in female. Total length 111 mm in males and 123 mm in females (Lanza et al., 2007).

Diagnosis

Smaller than Speleomantes imperialis. Scent emission, such as in S. imperialis, absent (Lanza et al., 2007).

Originally described as a subspecies of S. imperialis, it was later elevated to species status (Carranza et al., 2008) on the basis of genetic and allozymic analyses. It cannot be distinguished from S. imperialis on external morphological characteristics.

appeared that males reached sexual maturity after the second year of life and females after the second or third year. Males were between 4-10 and females between 4-7 years old (Tessa et al., 2008).

Speleomantes sarrabusensis, Sarrabus, near the type locality, Sardinia. Photo: Max Sparreboom.

Speleomantes sarrabusensis, habitat of type locality, Sarrabus, Sardinia. Photo: Max Sparreboom.

Eggs

Eggs have not yet been observed. Although one would expect that this species would reproduce through direct development of a small number of terrestrial eggs, like other Speleomantes species, there is some evidence that it might be the only viviparous lineage of Speleomantes described to date (discussion in Lanza et al., 2006, 2007). Thus far females have not been examined as to whether they carry developing young.

Threats and conservation

Speleomantes sarrabusensis has a very limited range. It does not appear to be endangered, but is listed as Vulnerable (IUCN, 2013).

Distribution

This species is endemic to southeastern Sardinia, where it occurs in the Sette Fratelli Mountain range, Sarrabus, Cagliari Province (Lanza et al., 2007; IUCN, 2013).

Habitat

This species inhabits a granitic almost caveless area, living in humid rocky outcrops, crevices and forested areas at altitudes between 200-850 m (Lanza et al., 2007; IUCN, 2013).

Behaviour

Practically nothing is known about the ecology and behaviour of Speleomantes sarrabusensis and reports of possible viviparity need confirmation. Fragments of courtship and a male mounting a female have been depicted in Lanza et al. (2006). From a study of longevity and population dynamics it The range of Speleomantes sarrabusensis. 161

Observations in captivity

No published observations.

References

Carranza et al. (2008); Greven et al. (2004); IUCN (2013);

Lanza (1999f); Lanza et al. (1995, 2006, 2007); Tessa et al. (2008).

Speleomantes strinatii (Aellen, 1958) | French Cave Salamander Description

A moderately stout salamander. Head flattened and oval in dorsal view. Snout more or less truncate to rounded, projecting over the mouth, especially in the male. Nostrils closer to snout tip than to the eye. Tongue longer than in Speleomantes italicus, but shorter than in the large Sardinian species. Tail oval in cross section, slightly less than half the total length but a little shorter in females than in males, and

gradually tapering. Moderately bulging eyes. Gular fold present. No paratoids and no labial fold. Body short, subquadrangular in cross section, usually with 11 costal grooves. Limbs short, but well-developed, with four fingers and five toes. Fingers and toes more or less flattened, overlapping in adult males when adpressed, separated by a short gap in adult females. Finger and toe-tips hardly enlarged distally, more or less truncated. Vestigial webbing between toes. Skin smooth (Lanza et al., 1995, 2007; Lanza, 1999b). Colour highly variable as in all Speleomantes. Dorsal parts light to dark brown, often with a more or less brown, yellow, orange or greenish marbling. Spots and marble pattern often more pronounced on tail. Ventral side more or less dark brown, dotted with grey spots, especially on the throat. In young specimens dorsal parts are often more or less extensively greenish, with a metallic sheen. Newborn animals have much larger nostrils than older animals (Lanza et al., 1995).

Speleomantes strinatii, east of Genua. Photo: Joachim Nerz.

Sexual dimorphism not pronounced. Premaxillary teeth slightly enlarged in male (Greven et al., 2004). Mental gland under the chin in the male is also visible outside the breeding season. Cloacal swelling present in male, much less so in female. On average adult females are 7% longer than males (Salvidio & Bruce, 2006). Total length 116 mm in males and 128 mm in females (Lanza et al., 2007).

Diagnosis

A small dark-coloured, lungless salamander. Somewhat blunt canthus rostralis usually present. Tongue shorter than in Sardinian species but longer than in Speleomantes italicus. Speleomantes strinatii and S. ambrosii cannot be distinguished on external morphological characters.

Eggs

Speleomantes strinatii, Roquebilliere, France. Photo: Sergé Bogaerts. 162

Salamanders of the Old World | Speleomantes

Like other species of Speleomantes, Speleomantes strinatii reproduces through direct development of a small number of terrestrial eggs. A clutch consists of 6-14 ivory white eggs 5-6 mm in diameter, connected by a transparent mucous string, deposited on a humid substrate, in rock crevices or on moss. Egg deposition was observed in captive specimens between September-February (Durand, 1967a, 1967b, 1970, 1973). Other clutches were obtained in December, also under captive conditions. The female coils around the clutch and defends it

against predators (such as conspecific females and rats: Oneto et al., 2010). Brooding females have been observed eating their eggs, possibly those that did not develop properly (Salvidio et al., 1994). Despite the lack of direct evidence from field observations, it has been inferred that continental Speleomantes lay their eggs underground, presumably in holes safe from dangerous environmental extremes (Lanza et al., 2006). In captive conditions at a temperature of 12°C the eggs reached a diameter of 10 mm after eight months and hatching was observed after 10 months. Development is probably faster at higher temperatures. Recently hatched juveniles measured 22-24 mm (Durand, 1967b; 1970, 1973). Interestingly, juveniles have been reported to remain at the nest site for some weeks after hatching, with the mother in attendance (Oneto et al., 2010). Males become sexually mature in their third year, females one year later (Salvidio & Bruce, 2006).

Distribution

This species is restricted to south-eastern France and north-western Italy. It occurs from Alpes-de-HautesProvence to the Province of La Spezia, eastern Liguria (Duguet & Melki, 2003; Lanza et al., 2007; Lescure & de Massary, 2012; IUCN, 2013).

Habitat

This species occurs in a variety of habitats, as long as temperatures are moderate and humidity is high. It prefers

The range of Speleomantes strinatii.

habitats with only minor fluctuations in temperature and humidity such as humid outcrops, caves with wet walls, crevices and forested areas from sea level to 2,400 m altitude. It is not limited to calcareous soils, but to the kind of rocky ground that permits a subterranean life during the warm, dry season (Ficetola et al., 2012; Lanza et al., 2007). There is some degree of microhabitat segregation between adults and juveniles, with juveniles occupying microhabitats that are more exposed to environmental hazards such as predation and desiccation (Salvidio & Pastorino, 2002).

Behaviour

This species is entirely terrestrial, nocturnal and active practically all year round. Individuals are active at temperatures between 5-22°C and relative humidities of 74-100% (Lanza et al., 2007). There is a peak of activity in spring and autumn after rainfall, at temperatures between 13-15°C, and a dip in winter and summer. In winter Speleomantes strinatii remains active at altitudes below 500 m, and above 900 m in summer. It feeds on a variety of invertebrate prey, especially arthropods and dipterans (Limonia nubeculosa), which are captured using the long ballistic tongue. Juveniles prey upon coleopterans, myriapods and other small insects and have a broader trophic niche than adults (Salvidio et al., 1994). Long term studies of a population suggest that males may constantly outnumber females (Salvidio, 2008). Mating certainly takes

Speleomantes strinatii, habitat east of Genua. Photo: Joachim Nerz. 163

place in winter and spring, but probably all year round as well (Lanza, 1999b; Duguet & Melki, 2003; Lanza et al., 2007). Fragmentary observations of courtship have been made in captivity (Lanza, 1999b, Lanza et al., 2006, quoting observations by Mertens, Rehberg and Durand), but detailed descriptions of courtship and mating are lacking. This species’ behaviour appears to be generally similar to that of Sardinian Speleomantes species. The male mounts the female, clasping her with fore and hind legs. He makes rubbing movements during which he applies his mental gland to the snout of the female. Both partners make undulating movements with their tail. Spermatophore transfer has not been observed.

Threats and conservation

protected as a rare species. It is considered Near Threatened given its limited range (IUCN, 2013).

Observations in captivity

Most observations of mating, egg laying and parental care have been made on captive specimens (Mertens, 1923; Rehberg, 1960; Durand, 1967ab, 1970, 1973; Oneto et al., 2010).

References

Duguet & Melki (2003); Durand (1967a, 1967b, 1970,

1973); Ficetola et al. (2012); Greven et al. (2004); IUCN (2013); Lanza (1999b); Lanza et al. (1995, 2006, 2007); Lescure & de Massary (2012); Mertens (1923); Oneto et al. (2010); Rehberg (1960); Salvidio (2008); Salvidio & Bruce (2006); Salvidio et al. (1994); Salvidio & Pastorino (2002).

Speleomantes strinatii is abundant in its range and not endangered. In France it is

Speleomantes supramontis (Lanza, Nascetti & Bullini, 1986) | Supramonte Cave Salamander

Description

A moderately stout salamander, the adult female especially somewhat stockier than its congeners. Head flattened and oval in dorsal view. Snout more or less truncate to rounded, projecting over the mouth, especially in the male. Nostrils closer to snout tip than to the eye. Tongue significantly longer than in other species of Speleomantes. Tail oval in cross section, slightly less than half the total length but a little shorter in females than in males, and gradually tapering. Moderately bulging eyes. Gular fold present. No paratoids and no labial fold. Limbs well-developed, with four fingers and five toes. Finger and toe-tips more or less truncate and often enlarged at tips. Vestigial webbing between toes. Skin smooth (Lanza, 1999h; Lanza et al., 1995, 2007). Colour of upperparts highly variable: ground colour dark brown to blackish with blotches or marblings which are yellowish, ochre, or sometimes olive-green. Ventral parts bright as in Speleomantes flavus, but usually more or less dotted or marbled with dark spots. In young specimens dorsal parts are often more or less extensively greenish, with a metallic sheen. Newborn animals have much larger nostrils than older animals (Lanza et al., 1995).

Speleomantes supramontis, Dorgali, Sardinia. Photo: Max Sparreboom.

Sexual dimorphism not pronounced. Premaxillary teeth slightly enlarged in male (Greven et al., 2004). Mental gland under the chin in the male is also visible outside the breeding season. Cloacal swelling present in male, much less pronounced in female. Total length to 135 mm in males and up to 143 mm in females (Lanza et al., 2007). 164

Salamanders of the Old World | Speleomantes

Speleomantes supramontis, Dorgali, Sardinia. Photo: Max Sparreboom.

Diagnosis

A fairly large lungless salamander. No canthus rostralis. Tongue longer than in other Speleomantes species. Foot large. Does not emit an unpleasant scent (Lanza et al., 2007).

Eggs

Like other species of Speleomantes, Speleomantes supramontis reproduces through direct development of a small number of terrestrial eggs, but detailed observations in the wild are lacking. Rehberg (1960) found five eggs in the left and seven eggs in the right oviduct of a female S. supramontis which died in captivity, each with a diameter of 5.5 mm.

Distribution

This species is endemic to central-eastern Sardinia, around the Gulf of Orosei, occurring roughly between the Rio di Oliena-Cedrino Valley and 40° N latitude in the province of Nuoro (Lanza et al., 2007; IUCN, 2013).

altitude. It has been found active in caves at temperatures of 11-19°C and humidities of 86-98% (Lanza et al., 2007).

Behaviour

This species is entirely terrestrial and nocturnal. Speleomantes species are specialists at capturing prey with their tongues. They launch the tongue and the entire tongue skeleton out of the mouth ballistically, not simply by protrusion. The tongue skeleton fires out well past the point where the protractor muscles are able to exert force, thus becoming a projectile. Speleomantes supramontis is able to extrude its tongue up to 60 mm (80% of its body length) in less than 20 milliseconds. The cartilaginous tongue skeleton shoots completely out of the mouth and sets a record among plethodontids (Deban et al., 1997; 2007).

Courtship appears to be generally similar to that observed in Atylodes genei and other species of Speleomantes. The male mounts the female, clasping her with fore and hind legs. He makes rubbing movements during which he applies his mental gland to the snout of the female. Both partners make undulating movements with their tail. Spermatophore transfer has not been observed (Rehberg, 1960; Lanza et al., 2006).

Threats and conservation

Speleomantes supramontis, although considered common within its range, is recently reported to have suffered population declines and is hence considered Endangered given its limited range. Threats include habitat loss and illegal collection for the pet trade (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

Observations on behaviour and development of captive animals have been reported by Mertens (1923) and Rehberg (1960), but it is unclear if the specimens were of Speleomantes supramontis or S. imperialis (Lanza et al., 2007).

The range of Speleomantes supramontis.

Habitat

This species occurs in a variety of habitats, as long as temperatures are moderate and humidity is high. It prefers habitats with only minor fluctuations in temperature and humidity such as humid outcrops, caves, crevices and forested areas with a good growth of moss, between 100 m-1,400 m

Comments

Speleomantes flavus, S. supramontis and S. imperialis are often attacked by leeches (Batracobdella algira, Lanza et al., 2006, 2007).

References

Deban et al. (1997, 2007); Greven et al. (2004); IUCN

(2013); Lanza (1999h); Lanza et al. (1995, 2006, 2007); Mertens (1923); Rehberg (1960); Stuart et al. (2008).

165

Salamanders of the family Proteidae are permanently Proteus Laurenti, 1768 aquatic and retain the large, filamentous gills and caudal fins characteristic of larvae throughout life. The Proteus is a European, subterranean salamander, family Proteidae contains two genera, the European which has degenerate eyes. The body is slender and genus Proteus and Necturus. Necturus is an eastern the number of toes is reduced on both fore- and North American genus with normal pigmentation, hindlimbs. The genus Proteus may consist of several functioning eyes and four digits on each foot. The cryptic species (Sket, 1997). grouping of the genera Proteus and Necturus into a single family is controversial and should be considered Proteus anguinus Laurenti, 1768 tentative. The shared features by which these genera are grouped together taxonomically are possibly a reReferences Frost (2013), Larson (2006), Sket (1997). sult of parallel, paedomorphic evolutionary trends and not strongly indicative of common ancestry (Larson, 2006; Frost, 2013).

Proteidae Gray, 1825

Proteus anguinus, south­west of Ljubljana, Slovenia. Photo: Joachim Nerz.

166

Salamanders of the Old World | Proteidae

Proteus anguinus Laurenti, 1768 | Olm Description

Proteus anguinus is an eel-like, elongate salamander with small legs. This aquatic salamander is the only cave-adapted vertebrate in Europe, and exhibits troglomorphic characteristics such as skin depigmentation, eye degeneration and neoteny. The head is elongated and trapezoidal when viewed from above, with a duckbill-shaped snout. Eyes are poorly developed and covered by skin. Three pink coloured external gills on each side of the head. Tail about one third of total length, flattened laterally and with a tail-fin above and below. Fore legs have three fingers, hind legs two. In its natural habitat the Olm is yellow-pinkish to flesh-coloured. When kept

artificially in lighter surroundings for several months, pigmentation can develop and its colour changes to black. Melanin is present to some degree and this species is not truly albinistic. Males are a little shorter than females. Due to the translucency of the skin, internal organs are visible on the ventral side and sexually mature females can be distinguished by the presence of eggs visible in the ovaries. During the breeding season males have a larger and more elongated, swollen cloaca than females (Parzefall et al., 1999).

Proteus anguinus, south of Grosuplje, Slovenia. Photo: Joachim Nerz.

Proteus anguinus, south-west of Ljubljana, Slovenia. Photo: Joachim Nerz.

Proteus anguinus parkelj, Jelsevnik, Slovenia. Photo: Gregor Aljancic.

167

Total length 23-25 cm, exceptionally 35 cm (Parzefall et al., 1999).

Diagnosis

An eel-like salamander with small, thin legs. Head elongate with elongated, truncated snout. A pair of three external gills. Tail much shorter than trunk.

Historical reports of viviparity have not been confirmed by rigorous observations. Development time of eggs and larvae is temperature dependent. At 10°C eggs develop in 140 days and at this temperature it takes 14 years for these salamanders to reach sexual maturity. There is no clear metamorphosis – Proteus is a largely neotenic salamander that maintains external gills, tailfin and other juvenile characteristics throughout its life, but the skeletal organisation of the skull does not point to a fully neotenic development (Parzefall et al., 1999).

Distribution

Proteus anguinus is restricted to the subterranean Karst streams of the Dinaric Alps. Its range extends from the Isonzo-Soca River in southeastern Venezia Giulia in Italy through the southern half of Slovenia, southern Croatia, and parts of Bosnia and Herzegovina to the Trebisnjica River in eastern Herzegovina (Parzefall et al., 1999). It has been introduced to the Grotto Parolini, Vicenza, northern Italy (Lanza et al., 2007) and Tular near Kranj in Slovenia. Its occurrence in Montenegro remains unconfirmed (AmphibiaWeb, 2013). The black Proteus is found in Bela Krajina, southeastern Slovenia (Sket & Arntzen, 1994).

Habitat

The range of Proteus anguinus.

A morphologically distinct cavernicolous form (black Proteus) from southeastern Slovenia (Bela Krajina) has been described as a subspecies (Proteus anguinus parkelj, Sket & Arntzen, 1994). It differs from P. a. anguinus (white Proteus) in having dark pigmentation, fully developed eyes, a skull with broader and shorter bones and fewer teeth, a voluminous jaw musculature that gives the head a bulky appearance (Ivanovic et al., 2013), a proportionally longer trunk with a higher number of vertebrae, shorter extremities, and a shorter tail. Some significant morphometric differences are also found between white Proteus populations from Planina and Sticna (Sket & Arntzen, 1994). Black Proteus can reach a length of 40 cm or more (AmphibiaWeb, 2013).

Eggs and larvae

A female establishes an egg-laying territory. After 2-3 days the female starts attaching eggs to the underside of large stone slabs. She may continue laying eggs for up to 25 days, laying a total of up to 70 eggs. The female stays with the eggs and defends them against conspecifics. Eggs are 4-5 mm in diameter and absorb water to swell to 8-9 mm.

168

Salamanders of the Old World | Proteus

This species generally occurs in large subterranean aquatic Karst systems formed in limestone and dolomite rocks, and may be found in cave entrances (especially during episodes of high rainfall and flooding) and abandoned mine workings. Many of the caves where the species occurs are connected to rivers that run above ground for the first 50-100 km before disappearing underground. Populations may be found close to the surface or as much as 300 m underground depending on the thickness of the Karstic formation. The species is found in waters ranging from 5-15°C. Proteus a. parkelj is found in warmer surface waters (Stuart et al., 2008; IUCN, 2013). The Olm sometimes leaves the water and crawls about on humid surfaces underground, probably searching for food (Parzefall et al., 1999).

Behaviour

Proteus is a highly specialised, troglomorphic species that is normally blind and has developed highly specialised non-visual sensory systems to orient in permanently dark habitats, to find food and mates (Uiblein et al., 1992; Parzefall et al., 1999; Schlegel et al., 2006). Adult animals are rarely seen and are probably restricted to deep subterranean waters. (The black form has eyes and is probably less restricted to subterranean total darkness). Most observed individuals were not yet sexually mature (Briegleb, 1962; Parzefall et al., 1999). Important observations on the life history and behaviour of this animal have been made in captivity, in a breeding colony kept in a CNRS laboratory at Moulis in the French Pyrenees. Animals usually sit still in small groups under stones and appear to be chemically attracted to the company of conspe-

cifics (Guillaume, 2000). Individuals leave the assemblage for foraging and reproduction. They feed on small crustacaeans, gastropods and other invertebrates, including terrestrial species (Lanza et al., 2007). Prey items are detected using chemical cues. In the laboratory, breeding activity takes place all year round. The breeding male stakes out a territory by fanning its tail and chasing away conspecifics. Breeding males fight each other fiercely by pushing, biting and beating their tails. The male commences courtship when a sexually mature female enters his territory. He circles around the female while making tailfanning movements in the direction of her head. The male touches the body of the female and picks up chemical cues from her cloacal region. When responsive, the female touches the male’s cloaca with her snout. The male creeps ahead of the female and the female follows. The pair moves forward for 5-10 cm. The male deposits a spermatophore while making shivering movements with the base of his tail. The spermatophore is glued to the substrate by a translucent peduncle covered with a white globular sperm cap (Guillaume et al., 1999). The pair continues to creep forward and the female stops with her cloaca situated over the spermatophore. While staying in this position for about a minute the sperms move up into the cloaca. This courtship sequence may be repeated several times within a couple of hours (Parzefall et al., 1999). After being inseminated, a female leaves the male’s territory and establishes an egg-laying territory. After 2-3 days she starts attaching eggs to the underside of large stone slabs.

Threats and conservation

The main threats to this species come from changes in the forested and pastoral land above the subterranean systems, largely through tourism, economic changes, and increasing water pollution, all of which have a direct influence on habitat. The species is highly dependent on clean water, and is therefore very susceptible to pollution. Other localised threats might include water abstraction and hydroelectric schemes. There is some illegal

collection for the pet trade, but the extent of this is unknown (Stuart et al., 2008; IUCN, 2013). The species is protected by national legislation in Italy and Slovenia and also through international legislation. It is considered Vulnerable. The black form is limited to a few holes connected to subterranean networks in a very small geographic area and is especially in need of protection (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

A captive breeding colony of 400 individuals has been established in the Subterranean Laboratory of the CNRS, in the French Pyrenees at Moulis, where the species has been studied for more than 50 years since 1955. Long-term studies show that Proteus anguinus has evolved an extreme life-history strategy with a predicted maximum lifespan of over 100 years, an adult average lifespan of 68.5 years, an age at sexual maturity of 15.6 years and that it lays an average of 35 eggs every 12.5 years (Voituron et al., 2011).

Comments

The taxonomic status of different populations of Proteus – including the black form provisionally described as a subspecies on the basis of distinctive morphological characteristics – has not yet been settled (Sket & Arntzen, 1994; Grillitsch & Tiedemann, 1994; Arntzen & Sket, 1996, 1997). Phylogenetic analysis reveals that the white olm (P. a. anguinus) represents several deeply diverged, cryptic lineages (six clades, based on mitochondrial DNA sequence data) and that the black olm lineage (P. a. parkelj) is deeply nested within white olm lineages (Sket & Arntzen, 1994; Goricˇki & Trontelj, 2006; Trontelj et al., 2009; Goricˇ ki et al., 2012; Ivanovic et al., 2013).

References

AmphibiaWeb (2013); Arntzen & Sket (1996, 1997);

Briegleb (1962); Goricˇ ki & Trontelj (2006); Goricˇ ki et al. (2012); Grillitsch & Tiedemann (1994); Guillaume (2000); Guillaume et al. (1999); IUCN (2013); Ivanovic et al. (2013); Lanza et al. (2007); Parzefall et al. (1999); Schlegel et al. (2006); Sket & Arntzen (1994); Stuart et al. (2008); Trontelj et al. (2009); Uiblein et al. (1992); Voituron et al. (2011).

169

This family includes the species regarded as typical newts and salamanders. It is a diverse family, including both large- and small-bodied, terrestrial and – at least partly – aquatic species. Some are strictly terrestrial (for instance Salamandra in Europe and the Middle East, Echinotriton in China and Japan) and some are permanently aquatic (such as Pachytriton in China). The largely terrestrial salamanders (Chioglossa, Lyciasalamandra, Mertensiella, Salamandra) are smooth-skinned while most of the other genera have a rough skin. Most species have aquatic larvae except for some viviparous salamanders that give birth to fully metamorphosed offspring (for instance Lyciasalamandra). No single feature uniquely characterises all salamandrids as a monophyletic group, but a combined analysis of morphological and molecular characters strongly supports the monophyletic view (Titus & Larson, 1995; Zhang et al., 2008). The family Salamandridae has a holarctic distribution and is represented in Europe, north-western Africa, Asia, and North America.

triton), on its dorsal surface (as in the American species of Notophthalmus and Taricha), by its tail (Euproctus and Calotriton), or make no physical contact with the female at all (Cynops, Neurergus, Paramesotriton, Laotriton, Pachytriton, Lissotriton, Ommatotriton, Ichthyosaura, Echinotriton, Triturus and Salamandrina). The presence of well-developed lungs is ancestral for salamandrids with five evolutionarily independent reductions or losses of lungs in the genera Calotriton, Chioglossa, Euproctus, Pachytriton, and Salamandrina. The family Salamandridae contains some 93 species assigned to the following genera: Calotriton (2 species), Chioglossa (1 species), Cynops (9 species), Echinotriton (2 species), Euproctus (2 species), Ichthyosaura (1 species), Laotriton (1 species), Lissotriton (5 species), Lyciasalamandra (7 species), Mertensiella (1 species), Neurergus (4 species), Ommatotriton (2 species), Pachytriton (7 species), Paramesotriton (12 species), Pleurodeles (3 species), Salamandra (6 species), Salamandrina (2 species), Triturus (8 species) and Tylototriton (18 species). For a detailed review of the biology, reproduction and diversity of salamandrids, see Griffiths (1996), Zhao et al. (1988) and Larson et al. (2007). Steinfartz et al. (2007), Weisrock et al. (2006) and Zhang et al. (2008) have analysed the phylogenetic relationships within the family Salamandridae.

Fertilisation is internal. A male inseminates a female using a spermatophore that he deposits in front of her. The female picks up the sperm with her cloaca. The eggs are fertilised before they are laid. Courtship in salamandrids can be classified into four general types based on the degree of contact between the male and female (Houck & Arnold, 2003). Male salamandrids may actively References Griffiths (1996), Houck & Arnold (2003), Larson capture the female on its ventral surface (Mertensiella, et al. (2007), Steinfartz et al. (2007), Titus & Larson (1995), Lyciasalamandra, Salamandra, Pleurodeles, and TylotoWeisrock et al. (2006), Zhang et al. (2008), Zhao et al. (1988).

Salamandridae Goldfuss, 1820

Salamandra corsica. Vizzavona. Photo: Max Sparreboom. 170

Salamanders of the Old World | Salamandridae

Calotriton Gray, 1858 This genus was resurrected to comprise two species of Pyrenean mountain brook newts formerly included in the genus Euproctus (Carranza & Amat, 2005; Frost, 2013). They are small- to mediumsized newts. Head depressed and fairly robust. Prominent swellings on posterior sides of the head. Paratoid glands absent. Gular fold present. Skin covered with tubercles bearing horny tips. Tips of fingers and toes covered by a black corneous, naillike sheath. No dorsal and caudal crest during breeding season.

Their distribution is restricted to the Pyrenees. The genus Calotriton is sister to Triturus (Pyron & Wiens, 2011).

Calotriton arnoldi Carranza & Amat, 2005 Calotriton asper (Dugès, 1852)

References

Carranza & Amat (2005); Frost (2013); Pyron & Wiens

(2011).

Calotriton arnoldi Carranza & Amat, 2005 | Montseny Newt Description

A rough-skinned newt without paratoid glands. Head relatively flat, longer than wide, snout more or less rounded and slightly truncated; upper jaw reaching over the edge of lower jaw; eyes small. Labial folds present. Gular fold present. Tail ending in obtuse point and shorter than snout-vent length. First three to four caudosacral vertebrae with short transverse processes, not elongate as in Calotriton asper. Four fingers, five toes, all depressed and free, with tips covered by black claw-like sheath. Skin rough, but much smoother than in C. asper. The colour is chocolate brown, sometimes with light, silverygold stippling on the sides. Adult and young specimens uniform dorsally, with a light and very thin brownish-orange stripe from the base to the tip of the tail. Complete absence in both adults and young of the broad light-coloured vertebral stripe common in C. asper. Throat very light, largely unspotted.

Calotriton arnoldi, Montseny. Photo: Frank Pasmans.

Venter translucid, light ochre-brown, with dark markings most developed at the sides (Carranza & Amat, 2005). Males are not significantly smaller than females. Cloaca rounded and with a vertical slit in the male, and cylindrical in the female, relatively narrow and of a contrasting bright reddish-orange colour at the tip. Total length ca. 10 cm.

Diagnosis

Similar to Calotriton asper, but differs in its mitochondrial DNA and various other features: first caudosacral vertebrae have short transverse processes directed obliquely backwards; dorsal skin is smoother; no tubercles on underside; smaller than C. asper; lack of vertebral stripe (Carranza & Amat, 2005).

Calotriton arnoldi, Montseny. Photo: Frank Pasmans. 171

Threats and conservation

Large amounts of water are extracted from El Montseny for commercial purposes and the main threat to this species is the resultant lowering of the water table, rendering upperparts of the inhabited streams unsuitable. Population densities are estimated to be low (Carranza & Amat, 2005; IUCN, 2013). The Montseny Newt is considered Critically Endangered (IUCN, 2013). Within Calotriton arnoldi, two distinct groups of populations can be clearly differentiated, with an absence of gene flow between those situated on the eastern and western sides of the river valley that acts as a barrier. This is important for their management and for conservation measures (Valbuena-Ureña et al., 2013).

Calotriton arnoldi subadult, Montseny. Photo: Jan van der Voort.

Eggs and larvae

There are no data on its reproductive biology, which probably resembles that of Calotriton asper. The larva is similar to that of C. asper and shows the typical chocolate-brown colouration (Amat & Carranza, 2006).

Distribution

Calotriton arnoldi is known from only seven streams in two separate localities within the boundaries of El Montseny Natural Park in northeastern Spain (Amat & Carranza, 2006; IUCN, 2013).

Habitat

This is a largely aquatic, montane species that inhabits oligotrophic, fast-running waters with temperatures below 15°C, in beech and holm oak forests at altitudes between 600 and 1,200 m. Neither adults nor juveniles have ever been found on land (Carranza & Amat, 2005).

Behaviour

This species is almost totally nocturnal. There are no data on its behaviour.

Observations in captivity

A captive breeding programme started in 2007, carried out by the Departament de Medi Ambien of the Generalitat de Catalunya (IUCN, 2013).

Comments

Good Spanish accounts of the biology of Calotriton asper and C. arnoldi are García-París et al. (2004) and Montori & Llorente (2009), and Amat & Carranza (2006) respectively. It has been argued that the speciation separating C. asper and C. arnoldi is of relatively recent occurrence, approx. 1.1 Mya. This may have been caused by a geographical barrier or the climatic fluctuations frequent in the Western Palearctic during the Pleistocene (Carranza & Amat, 2005). In spite of having originated recently, and their being ecologically similar and geographically very close, there is no evidence of hybridisation between C. arnoldi and C. asper (Valbuena-Ureña et al., 2013).

References

Amat & Carranza (2006); Carranza & Amat (2005);

García-París et al. (2004); IUCN (2013); Montori & Llorente (2009); Valbuena-Ureña et al. (2013).

Calotriton asper (Dugès, 1852) | Pyrenean Newt Description

A rough-skinned newt without paratoid glands. Head relatively flat, longer than wide, snout more or less rounded, and slightly truncated; upper jaw reaching over the edge of lower jaw; eyes small. Labial folds present. Gular fold present. Tail ending in obtuse point and about as long as snout-vent length. First three to four caudosacral vertebrae have prominent transverse processes. Four fingers, five toes, all depressed and free, with tips covered by black claw-like sheath. Skin very rough, covered with tubercles bearing horny tips. The colour is variable, from grey and olive-green to brown and blackish above, uniform or with light, yellowish spots, which often merge into a broad vertebral line, especially in younger

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Salamanders of the Old World | Calotriton

animals. Venter opaque with a yellow, orange or red central band (Clergue-Gazeau, 1999; Carranza & Amat, 2005). Males are smaller than females, with the tail a little shorter and higher, and head more robust. Cloaca rounded and with a vertical slit in the male, and conical or cylindrical in the female, in the form of a small tube directed backwards. Total length usually 11-14 cm (female) and 10-12 cm (male).

Diagnosis

A rough-skinned newt with variable colour and a broad yellow vertebral line in subadults. Three to four caudosacral vertebrae with prominent transverse processes at

Calotriton asper, Olot, Catalunya, Spain. Photo: Frank Pasmans.

Calotriton asper, north of Benasque, Spain. Photo: Burkhard Thiesmeier.

approx. 90° to vertebral axis. Cloaca bulbous-conical in female, broad at the base (Carranza & Amat, 2005). There is a high degree of geographic variation in skin rugosity and colour patterns, but this has not led to the recognition of subspecies status between populations (Clergue-Gazeau, 1999).

Eggs and larvae

The female lays 20-30 eggs annually, or considerably more, depending on the size of the female.

Eggs are whitish. Diameter (without taking account of the gelatinous envelope) is 3.5-5 mm. Eggs are deposited singly against or between stones. The extended female cloaca enables the female to press the eggs into crevices (Clergue-Gazeau, 1999). Duration of embryonic development depends on temperature. At a water temperature of 12°C eggs take 45 days to hatch, and only 19 days at 19°C (Clergue-Gazeau, 1999; Thiesmeier & Hornberg, 1986). The larva has no balancers, measures 11-14 mm and is bright grey, speckled with dark dots. It becomes darker with age. Caudal fin extends only slightly onto the back. Toe-tips have a horny cover. Depending on altitude, the larval stage may take around 14 months (at 1,000 m) or longer at higher altitudes, where metamorphosis takes place in the third summer. At this stage the juveniles measure 45- 60 mm. Giant larvae of 95 mm have been recorded, including neotenic specimens. Metamorphosis itself may be prolonged. It takes about one month at 12°C, but may take much longer, for instance in subterranean habitats. At metamorphosis the juveniles are very dark-coloured. They reach sexual maturity after 2-3 years. In captivity males were sexually mature after 2.5-3 years, and females at the age of four years (Thiesmeier & Hornberg, 1990; Clergue-Gazeau, 1999).

Distribution

Calotriton asper is restricted to the Pyrenean mountain range of France and Spain, where it occurs at altitudes from 175 m to over 3,000 m on the northern slopes. The average range is 700-2,500 m. It occurs as far as the Corbières mountains 20 km south-east of Carcassonne in southeastern France (Lescure & de Massary, 2012; IUCN, 2013). 173

cycle is reversed. There, the animals stay in water during the winter and disappear during the summer months when water temperatures reach 18-22°C. When temperatures fall to below 12°C in September the animals appear again (Clergue-Gazeau, 1999). Cave-dwelling animals may stay in water all year round and their reproductive periodicity differs due to the lack of light stimulation and senses other than vision are activated to orient themselves in the darkness (Hervant et al., 2000; Schlegel et al., 2006). Their food consists of insect larvae, molluscs and worms and varies according to season and availability (Clergue-Gazeau, 1999).

The ranges of Calotriton asper and C. arnoldi (arrow).

Habitat

This is a largely, but not exclusively, aquatic, montane species that inhabits cold mountain lakes, torrents, oxygenrich streams, and occasionally cave systems. It prefers rocky substrates and avoids muddy waters (Clergue-Gazeau, 1999). Males occur predominantly in shaded areas with little aquatic vegetation and females in areas without sand and with high canopy cover. Both sexes avoid open and sunny sections and prefer parts of the stream with sufficient canopy cover. Under stable habitat conditions, the newts are fairly sedentary and do not move far up- or downstream. Except during catastrophic floods, larvae can avoid being washed away downstream if sufficient shelter is available. They can be abundant in shallow areas in stream beds with sufficient aquatic vegetation and a weak current (Montori et al., 2008). Extreme rainfall and strong currents can cause dramatic declines and produce natural population fluctuations (Montori et al., 2012). Genetic studies confirmed that C. asper shows marked geographic isolation, small population sizes and very limited dispersal (Milá et al., 2010).

Behaviour

The species is found in streams once water temperatures reach 6°C in spring. They leave the stream in autumn when water temperatures fall below 5-6°C and seek refuge in shelters in the embankment in winter. At low altitudes the

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Salamanders of the Old World | Calotriton

These newts are mainly nocturnal and hide under stones in the quieter, often deeper parts of the stream. They walk over the bottom and rarely swim. Reproduction takes place in water and starts shortly after the snow melts. Mating behaviour starts either with a male actively searching for a mate, or by the male taking up a signalling position during which he straightens his tail and raises it to a near-vertical position. A female shows interest by approaching the male and sniffing his cloaca. Thereupon the male captures the female with his tail and holds on to her, but does not hold her tail in his mouth. The position the animals assume varies. Mating may take place with the partners in a parallel position, or with male and female facing in opposite directions. The male makes slow rhythmic movements with his hind legs, stimulating the female’s cloaca and facilitating sperm transfer. The hind legs of the male are held in such a position as to catch the spermatophores, which are subsequently maneuvered into the female’s cloaca. Mating may take more than 30 hrs and up to four spermatophores may be deposited in one mating sequence. After mating, the male releases the female (Thiesmeier & Hornberg, 1990; Guillaume, 1999).

Threats and conservation

Although not directly threatened over most of its range, in certain peripheral localities these newts are scarce and several populations have disappeared. The main threats are loss of and damage to the species’ aquatic habitats. Introduction of salmonids and other fish can lead to population extinctions, especially in mountain lakes. Pesticides, accumulating in the newt’s body tissues, pose another threat. The Pyrenean Newt is considered Near Threatened (Stuart et al., 2008; Lescure & de Massary, 2012; IUCN, 2013).

Observations in captivity

Calotriton asper has been regularly bred in captivity as far as the fourth generation (Maillet & Schultschik, 2013a). Reproductive behaviour and development of larvae and juveniles has been described from

detailed observations on captive animals. In captivity this species requires water temperatures from 11-18°C and can be kept in water all year round. Observation tanks should be spacious (100×40 cm), with water levels at 10-20 cm. A water pump is useful to keep the water moving and gammarids may be provided as food. The animal is long-lived and may reach an age of at least 20 years (Thiesmeier & Hornberg, 1986, 1990).

Comments

Good Spanish accounts of the biology of Calotriton asper and C. arnoldi are García-París et al. (2004) and

Montori & Llorente (2009), and Amat & Carranza (2006), respectively.

References

Amat & Carranza (2006); Carranza & Amat (2005);

Clergue-Gazeau (1999); García-París et al. (2004); Guillaume (1999); Hervant et al. (2000); IUCN (2013); Lescure & de Massary 2012); Maillet & Schultschik (2013a); Milá et al. (2010); Montori & Llorente (2009); Montori et al. (2008, 2012); Schlegel et al. (2006); Stuart et al. (2008); Thiesmeier & Hornberg (1986, 1990); Wolterstorff (1901).

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Chioglossa Bocage, 1864 Premaxillary paired with short backward extensions. Nasals large and in contact. Frontosquamosal arch absent. Two series of vomerine teeth in S-shape. Tongue oval, free at the sides and protractile. Tail cylindrical and long. The male has no dorsal tail tubercle such as in Lyciasalamandra and Mertensiella. Insemination preceded by ventral amplexus similar to that of Pleurodeles and Salamandra (Thorn, 1969). The distribution is restricted to the Iberian Peninsula. Chioglossa lusitanica is the single extant representative of the genus Chioglossa that forms

a monophyletic group with Mertensiella, another monotypic genus for Mertensiella caucasica (Waga, 1876) from the Caucasus. Both species are streamside salamanders characterised by a slender build with short appendages and a long tail (Arntzen et al., 2007b).

Chioglossa lusitanica Bocage, 1864

References

Arntzen et al. (2007b); Thorn (1969).

Chioglossa lusitanica Bocage, 1864 | Golden-striped Salamander Description

A slender, long-tailed salamander. Tail about twice as long as snout-vent length. Head depressed, longer than wide, rounded snout and large protruding eyes. Tongue oval, free at the sides and protractile. Paratoids small. Body and tail cylindrical. Tail gradually laterally compressed towards the tip. Usually 11 costal grooves. Feet small, but well-developed with four fingers and five toes. Inner toes very small. Gular fold present. Lungs present, but sometimes reduced in size. Skin smooth.

176

Females are a little longer than males. In the breeding season males have thicker forelimbs (‘muscles’) that play a role in clasping the female during courtship. Total maximum length 156 mm for males, 164 mm for females, on average 128 mm (Arntzen, 1999).

Diagnosis

A very slender salamander with tail twice as long as snout-vent length. Large protruding eyes. No dorsal tail tubercle in male.

Ground colour black with two broad copper-coloured bands along the back, fusing into one at the tail-base and continuing to the tail-tip. Copper colour fades towards head and towards tail-tip. Dark-coloured parts of body and tail sprinkled with tiny blue spots, giving the animal an almost metallic sheen.

The subspecies Chioglossa lusitanica longipes (Arntzen & Alexandrino, 2007) has longer arms and fingers, legs and toes than the nominotypical subspecies. The nominate race occurs south of the Mondego River in central Portugal and the subspecies C. l. longipes north of the river, but there is a substantial

Chioglossa lusitanica longipes, Valongo, Portugal. Photo: Sergé Bogaerts.

Chioglossa lusitanica lusitanica, Lousã, Portugal. Photo: Frank Pasmans.

Salamanders of the Old World | Chioglossa

Chioglossa lusitanica longipes, Valongo, Portugal. Photo: Edo Goverse.

zone of overlap. The colour pattern of the salamander tends to a clinal variation, with the dorsal golden-stripe becoming more strongly marked from south to north. An ecological analysis suggests slightly different habitat characteristics for the two forms, with a harsher regime of lower temperature and lower humidity for the more mountainous southern form C. l. lusitanica (Arntzen et al., 2007b).

Larvae are whitish in colour upon hatching and become darker with age. They are slender, with short gills and short extremities and the paddle-shaped tail and trunk are of approximately the same length. Larvae live in both quiet waters and in

Eggs and larvae

Females normally lay 10-17 eggs – exceptionally more – in submerged holes in stream banks (Sequeira et al., 2003). Eggs are also found under stones and against rocks in stagnant or slow-flowing water. Eggs are laid singly but are often found as small clusters or large assemblages of several clutches. A well-known breeding site occupies some ancient mine galleries. Such spots are favourite refuges for salamanders in hot and dry periods and are characterised by near-constant temperatures all year round. Egg diameter is approximately 4 mm. The gelatinous egg capsule is 5-8 to 11 mm in diameter. Eggs are unpigmented and yellow-white in colour. The eggs are relatively large, but hatchling larvae are small. After six to nine weeks, or ten weeks at lower temperatures, the larvae hatch at a size of 12-13 mm (Arntzen, 1981, 1999; Vences, 1990).

Chioglossa lusitanica eggs, Valongo, Portugal. Photo: Max Sparreboom. 177

may reach a snout-vent length of 29 mm, total length 70 mm, before metamorphosis (Arntzen, 1999). Juvenile salamanders are found in the same habitat as adults but stay closer to the stream and may even be active during the day. Sexual maturity is reached after 4.5-6 years, males generally a year earlier than females (Lima et al., 2001). In captivity animals may live for more than 10 years, but in the wild there are no records of animals older than eight years (Arntzen, 1999; Thorn & Raffaëlli, 2001).

Distribution

Chioglossa lusitanica larva, Rio Tendi, Asturias, Spain. Photo: Frank Pasmans.

Chioglossa lusitanica is endemic to the Iberian Peninsula, where it occurs in northern and central Portugal and north-western Spain. Rainfall and altitude determine its range. The species is largely restricted to areas of low and medium altitude, under 1,000 m, and of high rainfall, with annual precipitation over 1000 mm (Arntzen, 1981; Teixeira et al., 2001; Arntzen & Teixeira, 2006; IUCN, 2013).

Habitat

The species inhabits streamside habitats, mostly in humid mountain areas. It is associated with clear, well-oxygenated, small- to medium-sized, slightly acidic streams (although in Portugal it has been found in water with pH 7-8), with dense surrounding vegetation. It has also been recorded in caves and abandoned, flooded mine galleries. It is associated with broadleaved oak forest, and occurs in secondary vegetation, but only rarely in commercial plantations. Animals have been recorded from eucalypt plantations, pine forests and even shrubland (Taxus or Erica) (IUCN, 2013). Optimal temperatures for adults range between 9 and 19°C and they prefer breeding habitats with little fluctuation in temperature, such as the deserted mine galleries in Valongo in northern Portugal where water temperatures range between 10 and 14°C (Arntzen, 1981, 1999; Vences, 1990; García-París et al., 2004). Males, females and juveniles differ in habitat utilisation (Sequeira et al., 2001).

Behaviour

The range of Chioglossa lusitanica.

parts of the stream with a stronger current. The larvae hatched in autumn hardly grow over winter and metamorphose the following summer at a snout-vent length of 22 mm (total length approximately 45-50 mm). Others overwinter and metamorphose at a snout-vent length of 24 mm. Some older individuals 178

Salamanders of the Old World | Chioglossa

Adults usually remain in hiding during summer. In the wet season, from autumn to spring, they become active, mainly at night. Juveniles are also active in summer and are less nocturnal than adults. Larvae are strictly nocturnal. Individual salamanders may be sedentary for long periods, but others migrate over long distances (more than 700 m) at high speed (more than 350 m in a single night) (Arntzen, 1994b). Migration takes place along the stream and in dry and hot periods, animals seek hiding places in deeper refuges, in stream banks and in dams. Hibernation is less evident than aestivation. Salamanders have been found active at temperatures just over 0°C (Arntzen, 1999). Food consists mainly of spiders, beetles, flies, and fly larvae 2-4 mm in size, varying between habitats and depending on the abundance of particular prey species. Food items are usually captured with the tongue, which is shot at the prey in a particular manner, over a distance of up to 1 cm

(Vences, 1990). Adult salamanders generally do not feed during the reproductive period in summer and autumn (Vences, 1990; Arntzen, 1999). This species may adopt several different anti-predator postures. It may stretch the tail forward and hide its head under it, or may feign death by remaining motionless and laying the front legs against the body (Vences, 1990). A specific form of anti-predator response is tail autotomy. The salamander may break off its tail when attacked or handled with force. The shed tail end keeps wriggling for some time, thus attracting the predator’s attention and allowing the animal to escape. The tail can regenerate completely, but tail loss comes at a cost. Fat reserves are stored in the tail and losing it appears to reduce fecundity in females (Arntzen, 1981, 1994a, 1999). Reproduction usually takes place in late summer and autumn, and exceptionally in early summer in some localities. The timing of reproductive activity differs within and between populations (Vences, 1990; Sequeira et al., 2003). Mating normally takes place on land or in shallow water (Arntzen, 1999). A sexually active male salamander stands in an alert posture on extended forelimbs and rapidly pursues any moving salamander. Upon reaching a female, the male nudges her briefly with his snout. He moves to the female’s head and then shoves his head under her axilla. He pushes forward under the female’s body, raising both arms as he nears the female’s head. When his up-raised forelimbs contact the female’s forelimbs, he clamps them downward and holds the female in amplexus. During amplexus the male shifts his body, swings his upraised head under the female’s chin, and vigorously flexes his body from side to side. The male then displaces his sacrum several times before he begins to deliver a spermatophore. He deposits the spermatophore on the substrate under the female’s cloaca. In displacing his sacrum, the female falls upon the spermatophore and thus picks up the sperm cap in her cloaca. The male may deposit further spermatophores without interrupting amplexus (Arnold, 1987).

to rocks in slow-moving water, as well as on land. Large assemblages of eggs (more than 100 or even 1000) are often found in the mine galleries – the result of many females selecting the same spot. Parental care, as seen in species with similar egg-laying habits, such as Euproctus montanus, has not been observed in Chioglossa lusitanica (Arntzen, 1999).

Threats and conservation

Major threats to this species are pollution of streams with agrochemicals, canalisation, water extraction from streams for agricultural purposes, and the loss of terrestrial streamside habitat through conversion to forestry plantations (Eucalyptus and Pinus). In Portugal the habitat is at risk from fire. Eastern Spanish populations exhibit lower population densities, and there have been reports of declines and extinctions in Galicia. In Portugal populations are widespread and abundant (4-5 adults per metre of brook habitat) and under no immediate danger, but they are considered vulnerable because of their specialised habitat requirements. Chioglossa lusitanica is protected by national legislation in both Portugal and Spain and listed as Vulnerable (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

Chioglossa lusitanica has been kept in captivity and its reproductive behaviour has been described on the basis of detailed observations of captive animals (Thorn, 1966; Arnold, 1987). It is a delicate species that can be kept in a humid, cold environment, with temperatures around 15°C and a short winter rest period at temperatures below 5°C. Tanks should have a portion of shallow water 5-10 cm deep. It has lived in captivity for over 10 years (Thorn & Raffaëlli, 2001).

Comments

Good Spanish accounts of the Golden-striped salamander with extensive documentation are given by GarcíaParís et al. (2004) and Vences (2009).

References

Arnold (1987); Arntzen (1981, 1994a, 1994b, 1999);

Arntzen et al. (2007b); Arntzen & Teixeira (2006); García-París et al. (2004); IUCN (2013); Lima et al. (2001); Sequeira et al. (2001, 2003); Stuart

Egg clutches are found in well-hidden places such as in deep, eroded holes on the stream floor, under stones or attached

et al. (2008); Teixeira et al. (2001); Thorn (1966); Thorn & Raffaëlli (2001); Vences (1990, 2009).

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Cynops Tschudi, 1839 The species of the genus Cynops are morphologically similar overall. All are smaller-bodied than either Paramesotriton or Pachytriton. They have a vertebral ridge, and almost all individuals lack lateral ridges. The tail is laterally compressed, and the skin is granular, except in C. wolterstorffi. Some individuals have parietal ridges, although these are generally not as prominent as in Paramesotriton (Chan et al., 2001). Nine species are currently recognised in the genus Cynops. Cynops wolterstorffi was long placed in a separate genus Hypselotriton on the basis of studies on skull morphology (Herre, 1939; Pope & Boring, 1940; Thorn, 1969). Cladistic studies, based on molecular and morphological characters, had suggested that Cynops might be paraphyletic, with C. pyrrhogaster possibly being more closely related to Paramesotriton than to C. cyanurus (Chan et al., 2001), but recent work confirms the monophyly of Cynops (Wu et al., 2010c). Cynops orientalis, C. fudingensis, C. orphicus and C. glaucus form a species group that is distributed along the coastline of south-

eastern China. These species differ from the Yunnan-Guizhou Plateau species group (C. chenggongensis, C. cyanurus and C. wolterstorffi) and the Japanese species group (C. pyrrhogaster and C. ensicauda), both morphologically and genetically (Zhao & Hu, 1988a; Weisrock et al., 2006).

Cynops chenggongensis Kou & Xing, 1983 Cynops cyanurus Liu, Hu & Yang, 1962 Cynops ensicauda (Hallowell, 1861) Cynops fudingensis Wu, Wang, Jiang & Hanken, 2010 Cynops glaucus Yuan, Jiang, Ding, Zhang & Che, 2013 Cynops orientalis (David, 1873) Cynops orphicus Risch, 1983 Cynops pyrrhogaster (Boie, 1826) Cynops wolterstorffi (Boulenger, 1905)

References

Chan et al. (2001); Herre (1939); Pope & Boring (1940);

Thorn (1969); Weisrock et al. (2006); Wu et al. (2010c); Zhao & Hu (1988a).

Cynops chenggongensis Kou & Xing, 1983 | Chenggong Newt Description

This description follows Kou & Xing (1983). A relatively small newt. Head slightly flattened; snout rounded and slightly protruding beyond mandibles. Nostrils situated at snout tip. Labial fold very conspicuous, covering two-thirds of the mandibles. Gular fold present. Paratoids and vertebral ridge inconspicuous. When limbs are adpressed, digits do not, or hardly meet. Tail shorter than snout-vent length and laterally compressed. Skin very smooth in life, but becomes slightly granulated after preservation.

Cynops chenggongensis, from Fei, Ye & Jiang, 2010. 180

Salamanders of the Old World | Cynops

Distinct yellow or orange spot below the eye. Dorsal colouration greenish-yellow with dark spots or blotches. In most specimens, orange spots form two dorsolateral lines (1-10 or more spots on each side). Ventral colouration is bright orange with irregular black blotches. Conspicuous black spots on the tail of females. Tail of males develops a blue sheen during the breeding season. Male cloaca is swollen with papillae on inner wall. Total length 78.5-95.5 mm in males, 90-106.2 mm in females.

Diagnosis

Cynops chenggongensis resembles C. cyanurus, but is recognised as a separate species (Zhao & Adler, 1993; Fei et al., 1999). It differs from C. cyanurus by its smoother skin and less conspicuous vertebral ridge, and frequently has two dorsolateral rows of orange-yellow spots from shoulder to tail-base. The original description claims that the two species can be further distinguished by the presence of conspicuous black spots on the tail of female C. chenggongensis (Kou & Xing, 1983), but black caudal spots are also observed in female C. cyanurus (Fei et al., 2006).

Eggs and larvae

The breeding season probably starts late March to early April. One female may lay 200-300 eggs per year. The diameter of the egg capsule is 2.8-3.6 mm and the diameter

of the embryo is 1.7-1.8 mm. Dissection revealed that females smaller than 82.5 mm in total length are not sexually mature (Kou & Xing, 1983).

Distribution

Known only from the type locality of Shuitang, Chenggong County, Yunnan, China, at 1,940 m altitude.

Habitat

This species is found in small ponds, rice fields and ditches near rice fields at ca. 2,000 m altitude. The type specimens were collected in March and April 1982. Hibernation starts in October and takes place underground, where specimens have been found at depths of less than 10 cm.

Behaviour

There is no information regarding the behaviour of this species.

Threats and conservation

At the type locality, the species appears to be threatened by loss of wetland habitats and water pollution. It has not been observed in recent years. There are no data to assess its conservation status (IUCN, 2013).

Comments

Based on the presence of a distinct orange spot below the eye, Cynops chenggongensis is most probably closely related to C. cyanurus and C. wolterstorffi, all of which are known from the Yunnan-Guizhou Plateau, the eastern extension of the Tibetan Plateau. However, no molecular data are available for this species, so its relationship to other Cynops remains to be settled. Occasionally, newts similar to C. cyanurus are imported to Europe through the pet trade, under the name of C. chenggongensis, but with unknown collecting locality. Such identifications should be treated with caution.

References The range of Cynops chenggongensis.

Fei et al. (2006); Fei et al. (1999); Fei et al. (2010);

IUCN (2013); Kou & Xing (1983); Zhao & Adler (1993).

Cynops cyanurus Liu, Hu & Yang, 1962 | Blue-tailed Fire-bellied Newt, Chuxiong Fire-bellied Newt

Description

Cynops cyanurus is generally similar in appearance to C. orientalis, but differs from it in the following respects: Paratoid glands inconspicuous, noticeable vertebral ridge, orange-red spot at the corners of the mouth, skin rather granulated; occipital V-shaped ridge connected to vertebral ridge, vertebral ridge and limbs brownish; distinct inner and outer metacarpal and metatarsal tubercles, of which the outer ones are conical (Liu et al., 1962; Zhao & Hu, 1988a). Tail is shorter than snout-vent length and tapers gradually towards the tip; tail-tip rounded or ending in a blunt tip.

Colour is dark brown above, occasionally lighter and may change to lighter olive-brown or yellow during the night. Individual colour change is also clearly visible in larvae and juveniles. The vertebral ridge is often lighter than the colour of the back. The vent is covered with an irregular pattern of red or orange spots on a dark blue to black background; the orange colour may predominate, marbled or dotted with irregular black patches. Black spots on the tail of the male. Male smaller than female. In the reproductive season the male has a distinct blue sheen along the tail, which sometimes extends over the flanks. The male cloaca is swollen. 181

Cynops cyanurus, Kunming Municipality, Yunnan. Photos: Hou Mian.

Cynops cyanurus, Shuicheng Pref., Guizhou (type locality). Photo: Hou Mian.

Cynops cyanurus, Shuicheng Pref., Guizhou (type locality). Photo: Hou Mian.

Total length 73-85 mm in males, 75-100 mm in females (Fei et al., 2006).

The ecological data published by Fei & Ye (1988, 1990), referred to below, apply to this subspecies.

One subspecies, Cynops c. yunnanensis Yang, 1983 is recognised (according to Zhao & Adler, 1993, Yang’s paper was published prior to the paper by Fei and Ye, 1983a, who named the same animal C.c. chuxiongensis). This form occurs in Chuxiong and Jingdong counties in north-eastern Yunnan at altitudes between 2,400 and 2,600 m. It differs from the nominate form in its larger size (males 82-96 mm, females 97-115 mm) and the uniform, dark colour of the upper parts of limbs, body and muscular part of the tail. Anterior half of the cloaca is orangered, posterior part greyish-black, inferior caudal fin fold orange-red, bordered with a dark wavy line (Fei & Ye, 1983a). 182

Salamanders of the Old World | Cynops

Diagnosis

Vertebral ridge and red-orange spot below the eye distinguish Cynops cyanurus from C. orientalis. Blue tail in the male in nuptial dress.

Eggs and larvae

Eggs are laid individually, wrapped in leaves, from 1 to 24 per day up to 226 on average per season per female. The soft leaves of water plants are chosen for egg-deposition at a depth of 2-6 cm below the water surface (Fei & Ye, 1988). Eggs are laid from April to early October, with a peak in the breeding season in May and June, when water temperatures range from 18 to 27°C (Fei & Ye, 1990). Various differences in

Cynops cyanurus, male in captivity. Photo: Max Sparreboom.

ponds close to Kunming (IUCN, 2013). In October, after the reproductive season, the animals move onto land. They never stray far from water and live in secondary coniferous and broadleaf forest (Fei & Ye, 1990).

Behaviour

These newts hibernate in damp caves or stony crevices near their breeding waters from October to April. Reproduction takes place in calm water at water temperatures of 18-27°C, especially in the shallows at depths of 10-20 cm where the water warms up easily. The peak of breeding activity is in May and June (Fei & Ye, 1990).

The range of Cynops cyanurus.

reproductive ecology between Cynops orientalis and C. cyanurus have been observed. Whereas female C. cyanurus can produce eggs fertilised by a single insemination for up to two weeks afterwards, a female C. orientalis can apparently store sperm for longer and lay fertilised eggs for several months following a single insemination (Yang & Shen, 1993). At water temperatures between 18 and 29°C, eggs hatch after about 17 days and metamorphosis takes place 147 days later (Fei & Ye, 1988). Yang & Shen (1993) report that metamorphosis in C. cyanurus takes longer than in C. orientalis. Larvae are dark brown to yellow and may change colour. In the final larval stages the light spots at the corners of the mouth are already visible. Total length at metamorphosis is 47 mm on average (Yang & Shen, 1993) and the animals reach sexual maturity after about two years (Fei & Ye, 1988).

Distribution

This species is known from Guizhou and Yunnan from altitudes between 1,790 and 2,400 m. It is common on the Yunnan plateau (Yang, 1991; Fei et al., 1999).

Habitat

The habitat consists of ponds in mixed forest and paddy fields. Breeding takes place in shallow waters such as irrigated paddy fields, ponds in the forest, and also in artificial

Their sexual behaviour was first studied in the laboratory and published by Fei and Ye (1988). The male follows the female and tries to block her path. When the female stops moving, the male will touch her with his snout and occasionally bite her. He fans his tail in front of her snout, in bouts lasting 2-5 seconds at 3 second intervals, and may continue in this way for about 20 minutes. Once responsive, a female moves forwards and touches the male with her snout or bites him 5-10 times. The male turns round 180 degrees and starts creeping ahead of her, his tail making snake-like movements. The female follows him and continuously touches or nibbles at his undulating tail. After creeping 10-20 cm, the male raises his tail and deposits a spermatophore. The sperm cap is 3.5-6.5 mm long and 0.5-0.8 mm in diameter and it attaches to the female cloaca and is absorbed in 25-40 minutes. If the sperm is picked up, the female usually loses interest and stops responding. If the sperm cap is missed, the female keeps on creeping and the male may deposit one or two more spermatophores. This behaviour is similar to that observed in other Cynops species (Sparreboom & Faria, 1997; Sparreboom, 1998).

Threats and conservation

The species has a relatively wide distribution. Its populations are presumably large and it appears to tolerate some degree of habitat modification. It is not presently considered endangered (IUCN, 2013). 183

Cynops species. In captivity, as in the wild, C. cyanurus starts breeding later in the season than other Cynops species and at higher temperatures, an unexpected observation for a mountain species (Sparreboom, 1998; Fleck, 2000).

Comments

Cynops cyanurus, female in captivity. Photo: Max Sparreboom.

Observations in captivity

Cynops cyanurus has been captive-bred, but for unknown reasons (water quality, temperature regime?) it does not breed so easily in captivity as other

Cynops cyanurus have appeared in the pet trade from time to time, as well as newts that are more or less similar to it. Collecting localities are usually not known. Variation in colour, size, blue colouration of the tail, smoothness or granulation of the skin and presence of a dorsal ridge, suggest that some imported specimens might belong to different but related taxa.

References

Fei & Ye (1983a, 1988, 1990); Fei et al. (1999, 2006); Fleck

(2000); IUCN (2013); Liu et al. (1962); Sparreboom (1998); Sparreboom & Faria (1997); Yang & Shen (1993); Yang (1983, 1991); Zhao & Adler (1993); Zhao & Hu (1988a).

Cynops ensicauda (Hallowell, 1861) | Sword-Tailed Newt Description

The Sword-Tailed Newt is the largest species of the genus Cynops. Head larger and paratoid glands less prominent than in the other Japanese Cynops species, C. pyrrhogaster. Vertebral ridge clearly present, lateral glandular ridges not distinct. Tail vertically flattened and ending in an obtuse, tapering tip, hence the scientific and English name. Limbs, toes and fingers shorter than in C. pyrrhogaster. Skin rather granulated. Two subspecies are recognised: the nominate form C. e. ensicauda, occurring in the Amami island Group, and C. e. popei, occurring in the Okinawa Island Group (Inger, 1947). The validity of these subspecies has been confirmed in a study using mitochondrial DNA sequences (Tominaga et al., 2010).

The colour is dark to olive-brown above, with occasionally lighter coloured lateral and dorsal stripes (in C. e. ensicauda) or black to dark brown, with occasionally brown or light green patches or stripes (in C. e. popei). Colour of the underside is variable, from yellow to orange or red, with an irregular pattern of black lines or patches. Occasionally the belly has no spots and is uniformly orange, or may be predominantly black with little orange colouration. Individuals with exceptional whitegreen and orange-red patterns occur. Tail longer than head and body in the female, a little shorter or the same length as the rest of the body in the male. In the breeding season the male of the subspecies C. e. ensicauda has a silver-blue sheen along the tail (similar to that in males of e.g. Triturus cristatus or Paramesotriton hongkongensis). Total maximum length 13 (male) to 15 cm (female).

Diagnosis

A rather large size and long tail distinguish this newt from other Cynops species. Belly and soles of feet are yellow to orange, glandular system weakly developed. The two subspecies differ in colouration and the stripe on the tail of C. e. ensicauda in the breeding season.

Cynops ensicauda ensicauda, male, right, courting female, Amami. Photo: Tim Johnson. 184

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Cynops ensicauda is genetically well differentiated from C. pyrrhogaster from the main Japanese islands (Hayashi & Matsui, 1988), but settling the relationship between these two species requires further study (Tominaga et al., 2010).

Breeding assemblage of Cynops ensicauda ensicauda, Amami. Photos: Max Sparreboom.

Eggs and larvae

Eggs are laid individually, under and between leaves, folded in a leaf, or inside reeds and grasses. They are usually laid in water, but in some populations may also be deposited in damp areas out of the water (Tanaka, 2003 in: Johnson, 2004; pers. obs.). Size of jelly mass 4-5 mm, egg diameter approx. 3 mm, brown above and yellow-white below. A female can lay from several dozens up to several hundreds of eggs per season (Franzen & Franzen, 2005). Egg-laying extends over several months. The reproductive cycle may begin in late October at lower elevations and extend to June-July (Sparreboom & Ota, 1995). Sato (1943) reports that in the natural habitat eggs are laid from March to July-August. Larvae hatch after some three to four weeks at a length of 12-15 mm – depending on water temper-

ature – and reach a total length of 40-45 mm at metamorphosis, after 3-4 months. They are dark brown to black in colour. Larvae of various sizes are present in breeding waters, indicating that reproduction occurs over much of the year (Sparreboom & Ota, 1995). The juvenile newts move onto the land where they normally live until reaching sexual maturity after at least 2-3 years.

Distribution

The distribution of Cynops ensicauda is limited to the Japanese Ryukyu archipelago. Cynops e. ensicauda occurs on Amami-Oshima, Kakeroma, Uke and Yoro, and C. e. popei is distributed on Okinawa, Sesoko, Hamahiga, Tonaki, Tokashiki, Zamami, Geruma, Fukaji and Aka (Hayashi & Matsui, 1988; Johnson, 2004; Ota, 2005; Tominaga et al., 2010). 185

Cynops ensicauda popei, female, southern Okinawa. Photo: Max Sparreboom.

Cynops ensicauda popei, female laying an egg, southern Okinawa. Photo: Max Sparreboom.

Cynops ensicauda popei, juvenile, captive bred. Photo: Max Sparreboom.

Habitat

This newt occurs in both forests and meadows. A variety of water bodies serve as breeding habitats: Rice paddies, marshy meadows with holes and puddles, roadside and irrigation ditches, cattle drinking waterholes, and occasionally also streams (Inger, 1947; Sparreboom & Ota, 1995).

Behaviour

Terrestrial animals, both adults and juveniles, can be found at night, and also during the daytime when it is raining, wandering through leaf litter and crossing roads. Food consists of small snails, water insects, earth worms, eggs of their own kind, small dead fish, and even juvenile salamanders (Sparreboom & Ota, 1995; Katayama, 2011).

The range of Cynops ensicauda. 186

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Breeding activity is stimulated by the onset of cooler weather and the rains. Males tend to be present at breeding sites earlier than females and remain in the water longer. Males approach females entering the breeding pond and start displaying by fanning their tails in the direction of the female’s snout. Once the female stays still and turns her head towards the courting male, the male turns around and starts creeping ahead of her.

Cynops ensicauda and Echinotriton andersoni, habitat, Amami. Photo: Max Sparreboom.

If the female follows the male and touches his tail, the male deposits a spermatophore on the substrate. By following the male, the female is led over the spermatophore and picks up the sperm cap with her cloaca. A male may deposit several spermatophores during one mating sequence (Sparreboom, 1994).

In the natural habitat a successful sperm transfer was accomplished in only 2% of observed courtships (Sparreboom & Ota, 1995). Males compete for matings by actively interfering in on-going courtships and thus profit from the preceding courtship efforts of a rival male (Sparreboom, 1996).

Sexual interference in the Sword-tailed Newt (Cynops ensicauda). After having displayed to the female with tail-fanning, the male turns around and begins to creep ahead of her. The female is receptive and follows him. A second male moves between the tail of the creeping male and the snout of the female. He rapidly swings his head on a horizontal level, touching the male’s tail and shoving the female away. The effect of this ‘female mimicry’ interference is twofold: the first courting male is led to deposit a spermatophore by the tail-touches of the interfering male. This spermatophore is wasted. Second, the intruder manages to divert the attention of the female. She continues creeping but now behind the intruder who may obtain a ‘sneaky’ insemination. Art: Bas Teunis. From: Sparreboom, 1996. 187

Threats and conservation

Although seemingly abundant in some localities at certain times of the year, Cynops ensicauda populations are in fact in decline and the number of animals observed is dwindling. Habitats are disappearing due to pressure from human activities and newts die in great

numbers in concrete gutters along the roadside (Sparreboom & Ota, 1995; Ota, 2000a, 2000b; Johnson, 2004). The pet trade via Tokyo and Hong Kong probably takes a heavy toll (Johnson, 2004). The species is presently considered Endangered (IUCN, 2013).

Observations in captivity

Cynops ensicauda has frequently been kept in aquariums and may be kept in water all year round. In captivity this species requires temperatures from 20° to 30° C in summer and 12° to 15° C in winter. Juveniles especially require these relatively high temperatures if they are to reach adulthood, an observation noted by Gerlach who was the first to breed this newt in captivity (Gerlach, 1934). The animal is long-lived (20-25 years is not exceptional) and will breed without problems. There is a large body of literature on the captive breeding of this species (Sparreboom, 1998; Franzen & Franzen, 2005; Bachhausen, 2013a).

References

Bachhausen (2013a); Franzen & Franzen (2005);

Gerlach (1934); Hayashi & Matsui (1988); Inger (1947); IUCN (2013); Johnson (2004); Katayama (2011); Ota (2000a, 2000b, 2005); Sato (1943);

Cynops ensicauda ensicauda, second generation (F2) captive bred juvenile. Photo: Max Sparreboom.

Sparreboom (1994, 1996, 1998); Sparreboom & Ota (1995); Tominaga et al. (2010).

Cynops fudingensis Wu, Wang, Jiang & Hanken, 2010 | Fuding Fire-bellied Newt Description

The Fuding Fire-bellied Newt is a recently described species of Cynops belonging to the group of Cynops species that occurs in the foothills and mountainous regions of southeastern China (C. orientalis and C. orphicus). The following description summarises the species description by Wu et al. (2010c).

A small newt. Head shape oval in dorsal view. Snout truncate, projecting slightly beyond mandible. Nostril on snout tip; eye large. Labial fold well-developed. Inconspicuous longitudinal

ridge posterior to each eye. Skull relatively narrow. Paratoid gland poorly developed. Gular fold usually absent. Skin finely granulated, venter and underside of limbs smooth. Vertebral ridge elevated and conspicuous. Four fingers and five toes, no webbing. Tail laterally compressed, tapering posteriorly; caudal fin distinct; tail-tip bluntly pointed in female, rounded in male. Colour dark brown to lighter brown above; obscure black flecks on head and back. Vertebral ridge dark orange. Ventral colour

Cynops fudingensis, male, type specimen, Mt. Taimu region, Fuding, Fujian. Photo: Yunke Wu. 188

Salamanders of the Old World | Cynops

Cynops fudingensis, female, Mt. Taimu region, Fuding, Fujian. Photo: Yunke Wu.

ranges from yellowish-orange to reddish-orange. Number and position of ventral black dots vary among individuals; some specimens have black dots on the chin. The holotype has an orange dot on the dorsal side of the forelimb base, which is not present in all individuals; base of first digits of fore- and hindlimbs light orange. Orange red on cloaca, continuing to underside of tail. Posterior limit of cloaca may be black. Male smaller than female; the tail in particular is shorter in the male than in the female. In the reproductive season, males have a wider and more swollen cloaca. Total length 72-77 mm in males, 80-95 mm in females (Wu et al., 2010c; Fei et al., 2012).

Diagnosis

Similar to Cynops orientalis and C. orphicus but differs from these species both genetically and morphologically. Morphological differences compared with C. orientalis include a proportionately shorter trunk, longer tail, longer head and longer limbs. It resembles C. orphicus morphologically in having a finely granulated skin, a conspicuous vertebral ridge, and black spots on the tail, but differs in its proportionately larger head, longer limbs and shorter trunk. Venter and chin bright orange without dark blotches, but a few small black dots may be present; two dark ventral spots on the shoulder and axilla of each side, but spots from opposite sides do not connect at the midline; transverse black gular stripe absent; irregular spots on tail.

Eggs and larvae

Distribution

Cynops fudingensis is thus far only known from the Mt. Taimu region in Fuding, a coastal mountain in northeastern Fujian Province, China (Wu et al., 2010c). Its range is situated between the southernmost occurrences of C. orientalis and the northernmost locality of C. orphicus.

Habitat

This species’ habitat at the type locality is described as small, still-water puddles and ditches in a deserted agricultural field on a hillside, about 1 km from Mt. Taimu. The water is shallow and clear, with abundant aquatic plants and arthropods. The aquatic substrate is composed of soft earth and decomposing vegetation. Weeds grow densely in the field (Wu et al., 2010c).

Behaviour

These newts were found to be active during daytime, crawling on the bottom of the puddles and ditches. No further information to date.

Threats and conservation

Given this species’ isolated occurrence, it is probably vulnerable to habitat destruction associated with tourism, introduction of invasive predators and collection by hobbyists (Wu et al., 2010c).

Comments

Cynops fudingensis is the sister species of C. orientalis. The two species together form the sister clade to C. orphicus (Wu et al., 2010c).

References

Fei et al. (2012); Wu et al. (2010c).

No information to date.

189

Cynops glaucus Yuan, Jiang, Ding, Zhang & Che, 2013 | Bluish Grey Fire-bellied Newt Description and diagnosis

The Bluish Grey Fire-bellied Newt is a recently described species of Cynops belonging to the group of Cynops species that occurs in the foothills and mountainous regions of southeastern China (C. orientalis, C. fudingensis, and C. orphicus). Morphological and molecular analyses suggest this new species forms a highly diverged lineage within this group. The following description summarises the species description by Yuan et al. (2013).

possessing an inconspicuous vertebral ridge and having poorly developed paratoid glands. It differs from C. cyanurus and C. chenggongensis by absence of a postocular orange spot. It differs from C. orphicus by having an inconspicuous vertebral ridge. It differs from C. fudingensis by the following characteristics: an irregular bright orange stripe in the middle of the venter; bright orange blotches on the chin, the sides of the venter and around the cloaca; two bright orange blotches on the ventral sides of the limbs. It differs from C. orientalis by having a rough skin and an inconspicuous vertebral ridge. Male smaller than female; the tail in particular is shorter and wider in the male. In the reproductive season, males have a wider and more swollen cloaca. Total length 65-75 mm in males, 83-96 mm in females (Yuan et al., 2013).

Eggs and larvae

No information to date.

Distribution

Cynops glaucus is thus far only known from the region near Mt. Lianhua in Wuhua County in northeastern Guangdong, China (Yuan et al., 2013).

Cynops glaucus, type locality, Wuhua, Guangdong. Photo: Zhiyong Yuan.

A small newt, broadly similar to C. orphicus and C. fudingensis. It is distinguished from other species of Cynops by having irregular bluish-grey spots on dorsal sides of head, body, limbs and tail. It differs from C. pyrrhogaster and C. ensicauda by

Habitat

This species’ habitat at the type locality is described as small, still-water wetlands on the hillside. These are covered with tall shrubs and grasses, with scattered, shallow puddles, mostly around 20 cm deep, sometimes deeper. The aquatic substrate is composed of soft earth and decomposing vegetation (Yuan et al., 2013).

References

Yuan et al. (2013).

Cynops orientalis (David, 1873) | Chinese Fire-bellied Newt Description

The Chinese Fire-bellied Newt is the smallest species of the East Asian salamandrid genus Cynops and is morphologically distinct from other taxa in this genus. Head relatively large, a little longer than broad; snout rounded. Palatine teeth in two longitudinal series, commencing from front of choanae, meeting anteriorly and gradually diverging posteriorly. Tongue small, practically free at the sides. Paratoids moderately developed, their posterior borders demarcating head from neck. Faint vertebral ridge. Tail rather short, approximately the length of the body. Margins of dorsal and ventral tail-fins nearly parallel in breeding male, ending rather abruptly in a blunt,

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rounded tip. Skin rather smooth, especially in aquatic individuals (Chang, 1933). Lateral line organs clearly visible in water. Colour is dark brown to black above, occasionally greyish. Colour of belly and throat lively red or orange with many rounded black spots. The base of each limb, anterior part of the cloaca and ventral tail-fin are orange, posterior part of cloaca is black (Fei et al., 2006). Male smaller than female; the tail in particular is shorter in the male than in the female. In the reproductive season, males have

oviposition and early development there are differences between C. orientalis and C. cyanurus (Yang & Shen, 1993). Hatching larvae are 10-12 mm. Larvae are uniformly dark brown to black, a little lighter on the ventral side, and take approximately 50-80 days to metamorphose. After metamorphosis, at a length of 30-35 mm (Yang & Shen, 1993; Bogaerts, 1999), juveniles live on land.

Distribution

Cynops orientalis, male, captive specimen. Photo: Max Sparreboom.

Cynops orientalis is widely distributed in the lower reaches of the Yangtze River and adjacent areas, in the hilly plains of central and southeastern China at 30-1,500 m altitude (the provinces of Henan, southern Hubei, southern Anhui, Jiangsu, Zhejiang, Guangxi, Fujian, and Hunan, Zhao & Hu, 1988a; Fei et al., 2006).

well-developed dorsal and ventral tail-fins, and a swollen cloaca. Total length 61-77 mm for males, 64-98 mm for females (Fei et al., 2006).

Subspecies

One subspecies, Cynops orientalis qianshan, has been described from Anhui, Henan and Hubei Provinces (type locality Qianshan, Anhui) (Fei et al., 2012). On average it is smaller than the nominate form. The ventral fin fold of the male is thinner and more distinct than in the nominate form. Dorsal parts of body and limbs uniformly black. Belly bright orange red with black short bars or round spots. It occurs in shallow, well vegetated waters, in rice fields and puddles and also in slow-flowing mountain streams (Fei et al., 2012).

Diagnosis

The small size, dark-coloured back and red venter with black patches distinguish Cynops orientalis from other Cynops species. Unlike C. cyanurus and C. chenggongensis, this species has no orange spot behind the eye and no blue sheen along the tail of the male during the breeding season. Vertebral ridge is less pronounced than in C. fudingensis (Wu et al., 2010c).

Eggs and larvae

Eggs are laid singly, under and between leaves, folded in a leaf, and in floating roots and grasses. Size of oval-shaped jelly mass 4-2.5 mm, egg rounded, 2 mm in diameter. A female can lay a little over 100 eggs per season on average (Kung et al., 1960; Yang & Shen, 1993), from March to mid-June. Optimal water temperature for egg deposition is 15-23° C. Eggs laid in water at 18-25°C hatch in 11-17 days. At lower temperatures hatching takes considerably longer (Kung et al., 1960; Yang & Shen, 1993). One insemination is sufficient for a female to lay fertilised eggs over a period of two months; in this and other features of

The ranges of eastern Chinese species of Cynops.

Habitat

This species’ habitat is described as consisting of all suitable water bodies at various altitudes, mountain ponds, seepages and paddy fields in hilly areas, small brooks, flooded fields in mountain valleys, in forests and degraded areas. Locally it may be very abundant. ‘Always the water is cold and quiet, in the shade of grass, with a mud bottom free from stones’ (Chang & Boring, 1935). For egg deposition Cynops orientalis often chooses lentic water bodies such as ponds, wells and farmland ditches (Yang & Shen, 1993). 191

Behaviour

There are no studies in western languages on the natural history and ecology of this species. Although these newts are often aquatic, they also live on land outside the breeding season. In Zhejiang, where winters are mild, Cynops orientalis does not hibernate and is active all year round (Fei et al., 2006). According to observations by Yang & Shen in Hunan (1993), males enter the breeding pond first in January and February, resulting in an initial sex-ratio skewed towards males. Fei et al. (2006) refer to a peak in the breeding season from late April to mid-May. Males and females leave the breeding waters from July to September. Reproduction and courtship behaviour is similar to that of other Cynops species, but shows temporal differences. The male identifies a female by sniffing her body. He positions himself in front of her, and rapidly vibrates the distal part of his tail, fanning towards her snout. If the female is responsive, she stays still or moves towards the male. The male then turns round, creeping ahead of the female. He deposits a spermatophore on the substrate and the female picks it up with her cloaca. The male’s tail-fanning courtship display and creep movements ahead of the female are of relatively short duration and one spermatophore is deposited a few seconds after the male starts to creep ahead of the female. The female looses interest in the male soon after the first spermatophore is deposited. The male may bite and hold onto the female for a short while afterwards (Sparreboom & Faria, 1997).

Threats and conservation

Due to the local abundance of this species and its wide distribution, the Chinese Firebellied Newt is not immediately endangered. But habitat destruction and degradation are potential major threats to this species, as well as the use of herbicides and insecticides on rice terraces (IUCN, 2013). The animals are sold by the thousands in pet-markets in China and Europe. The species is used for educational and research purposes. In traditional Chinese medicine it is used to cure skin itching or burning (Fei et al., 2006).

Observations in captivity

This species has been successfully kept and bred in captivity. It can be kept in water all year round. Most observations on its behaviour were made in aquariums (Koepernik & Herrmann, 1991; Bachhausen, 1998; Sparreboom, 1998; Bogaerts, 1999). It prefers dense vegetation and still water and takes all sorts of living and dead food items. In captivity juveniles can be persuaded to live in water, where they grow faster than on land (Bogaerts, 1999).

Comments

Cynops orientalis is the sister species to C. fudingensis (Wu et al., 2010c).

References

Bachhausen (1998); Bogaerts (1999); Chang (1933);

Chang & Boring (1935); Fei et al. (2006, 2012); IUCN (2013); Koepernik & Herrmann (1991); Kung et al. (1960); Sparreboom (1998); Sparreboom & Faria (1997); Wu et al. (2010c); Yang & Shen (1993); Zhao & Hu (1988a).

Cynops orphicus Risch, 1983 | Dayang Newt Description

A medium-sized Cynops. Paratoids poorly developed. Dorsal surface of head smooth, flat, slightly concave, with a posteriorly pointing, slightly raised V behind middle, its apex joining vertebral line, which is slightly concave, becoming raised before base of tail. Limbs are small, forelimbs a little longer and only half as thick as hindlimbs.

Cynops orphicus, male, Tian Chi Lake, Chao’an County, Guangdong. Photo: Max Sparreboom. 192

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Tail nearly as long as head and body length, ending in an acute tip. Skin smooth; sides almost without wrinkles; about fourteen indistinct costal grooves discernible on upperparts. Gula and throat almost without longitudinal or transverse grooves. Colour brown to blackish above, bright orange below. Four large irregular blotches on gula. Irregular median stripe on belly, with a row of irregular blotches on each side. A spot near

Cynops orphicus, female, Tian Chi Lake, Chao’an County, Guangdong. Photo: Max Sparreboom.

palm and base of undersides of arms and legs. Cloacal lips orange, black posteriorly. Tail bright reddish-orange on basal three-fourths of ventral fin, entire apical half becoming pale orange-brown, more orange on both fins, dotted with black blotches (excerpted from description of Gressitt in Risch, 1983). Sexual dimorphism is well-developed. The male has a swollen cloaca, a well-developed dorsal tail crest, and is smaller than the female. Maximum total length 87 mm (male) to 116 mm (female) (David Wake, pers. comm. in Bachhausen, 2006).

Diagnosis

Distinguished from other Cynops species by the following combination of characters: Head flattened, with a fairly prominent canthus rostralis; skin very finely granulated; tail with small blackish dots and moderate dorsal and ventral fins; bright spots constantly present on palm and base of the underside of each fore- and hindlimb; ventral pattern consisting of an irregular light median longitudinal stripe and dark spots arranged in lateral rows (Risch, 1983). Closely related to, but distinguished from, C. orientalis by presence of conspicuous vertebral ridge and a bright ventral longitudinal stripe (Fei et al., 2006).

Eggs and larvae

Eggs and larvae were reared in the laboratory in Chengdu. They resemble those of C. orientalis.

Distribution

Until recently, Cynops orphicus was only known from its type locality near Dayang, at an altitude of 640 m in northeastern Guangdong, where it was collected as long ago as 1936. In 2001 some specimens were collected from Tian Chi Lake, Chao’an County, some 160 km NE of the type locality at 1,325 m altitude, and brought back alive to the Institute of Biology in Chengdu and the Museum of Vertebrate Zoology, Berkeley. Recently, however, a population of C. orientalis from Mt. Daiyun, Dehua, in central Fujian Province was reassigned

to C. orphicus (Fei et al., 2006), and this taxonomic change was confirmed by molecular analysis (Weisrock et al., 2006). As a result, the documented range of C. orphicus expanded northward to more closely approach the southern limit of C. orientalis (Wu et al., 2010c).

Habitat

This species’ habitat in Dayang was described as located in a cultivated mountain valley, encircled by partly wooded mountains. The specimens were probably caught in pools connected to a small stream in the valley (Risch, 1983). In Mt. Daiyun, Dehua, Fujian, animals were found in swamps at elevations of 1,400-1,600 m (Fei et al., 2006). The swamps are about 1 m deep and have dense aquatic vegetation.

Behaviour

In water these newts prey on earthworms, crustaceans, mites, and insects and their larvae (Gressitt in Risch, 1983). The species inhabits and breeds in pools and small lakes. It hibernates in terrestrial habitats, including forest and somewhat degraded areas (IUCN, 2013). The reproductive behaviour was observed in the laboratory in Chengdu and resembles that of Cynops orientalis (Sparreboom & Faria, 1997; Xie Feng, Max Sparreboom, pers. obs.)

Threats and conservation

Cynops orphicus is a rare species that appears to be in decline. Its habitat is probably being impacted by tourist development and it is listed as Endangered (IUCN, 2013).

Observations in captivity

The species was bred in captivity in 2002 at the Institute of Biology in Chengdu. It has not yet been kept in private aquariums (Reinartz, 2013).

References

Bachhausen (2006); Fei et al. (2006); IUCN (2013); Reinartz (2013); Risch (1983); Sparreboom & Faria (1997); Weisrock et al. (2006); Wu et al. (2010c); Zhao & Hu (1988a).

Cynops pyrrhogaster (Boie, 1826) | Japanese Fire-bellied Newt Description

A dark coloured newt, stoutly built, with vivid colours on the belly. Skin granular. Paratoid glands large, compressed, and almost continuous with a dorso-lateral glandular ridge, which is cut by transverse grooves into a series of bead-like glands. Ventro-lateral glandular ridge present from axilla to groin. A large globular gland on each side of the neck, and a smaller, round scapular gland above the insertion of the fore-leg. The colour is dark brown to black above, incidentally dotted with small reddish spots and stripes in the shoulder region and

along the flanks. Colour of the underside is variable, from pale yellow to orange or deep red, with an irregular pattern of black lines or patches; occasionally the belly has no spots and is uniformly orange, or is predominantly black with little orange or red colouration. Individuals with exceptional red dorsal colouration are known (Matsui et al., 2003). The tail-tip of the male becomes rounded during the breeding season, ending in a short filament, or tapers into a pointed tip with a long tail filament. The glandular system of the male 193

becomes very prominent, with large flap-like paratoid glands. A grey to purple sheen appears on the sides of body and tail and the surface of the skin becomes smooth and slimy to the touch. Occasionally dark patches form on the side of the tail. Total length usually 8-10 cm (male) to 10-12 cm (female).

Diagnosis

A small, dark brown newt with rugose skin and bright belly colouration. Limbs, toes and fingers longer than in Cynops ensicauda. Soles of the feet are brown to black in C. pyrrhogaster, not yellow to orange as in C. ensicauda, and the glandular system is strongly developed. C. pyrrhogaster is genetically well differentiated from C. ensicauda from the Ryukyu islands (Hayashi & Matsui, 1988).

Subspecies and variation Cynops pyrrhogaster, male, Yubara, Okayama Pref. Photo: Max Sparreboom.

Cynops pyrrhogaster, female egg-laying, Yubara, Okayama Pref. Photo: Max Sparreboom.

Cynops pyrrhogaster, male in breeding season, Yubara, Okayama Pref. Photo: Max Sparreboom. 194

Salamanders of the Old World | Cynops

There is a great deal of geographic variation in body-proportions and colour patterns. One subspecies has been described, Triturus (= Cynops) p. sasayamae (Mertens, 1969), based solely on the pattern of the colours on the belly, leaving the very heterogeneous majority of individuals within the nominate form, C. p. pyrrhogaster. However, the distinct subspecific status of C. p. sasayamae has subsequently been rejected by mitochondrial DNA data and allozyme studies (Tominaga et al., 2013; Hayashi & Matsui, 1988). The different geographical forms, described by Kawamura & Sawada (1959) and Sawada (1963a; 1963b) on the basis of the ventral marking patterns and body proportions have no formal subspecific status. The various forms are usually referred to as the Atsumi, Sasayama, Hiroshima, Tohoku, Kanto and Intermediate ‘races’. But atypical forms also occur within populations, making it impossible to assign single specimens to a particular ‘race’ if the collecting locality is unknown. The results of Sawada’s work have been summarised in Thorn (1969), Sparreboom (1982), Hayashi & Matsui (1988, 1990), and Franzen & Franzen (2005). Analysis of mitochondrial DNA sequences (Tominaga et al., 2013) showed that four major clades could be recognised in C. pyrrhogaster , which only partly correlate to the geographic ranges found by Sawada (1963ab) on the basis of morphological and behavioural traits, and by Hayashi & Matsui (1988, 1990) on the basis of allozymes. A northern clade occurs in Tohoku and Kanto districts, and a central clade is distributed in Chubu, northern Kinki, and eastern Chugoku districts. The northern and central clades were completely parapatric, without geographical overlap. A western clade occurs in southern Kinki, western Chugoku, Shikoku, and northeastern to central Kyushu districts. The central and western clades were found to be largely parapatric. Furthermore, a southern clade is distributed in southern and western Kyushu, and was found to be almost totally parapatric with the western clade. Tominaga et al. (2013) found that the degree of genetic differentiation was very large compared with the usual range of

intraspecific variation, and suggested that C. pyrrhogaster was composed of four species lineages that replace each other geographically. The taxonomic relationships among these lineages are the subject of further study. In a new arrangement, the name C. pyrrhogaster will be used for the western lineage, since the terra typica of Molge pyrrhogaster Boie, 1826 was restricted to Nagasaki by Hoogmoed (1978).

Eggs and larvae

Eggs are laid singly, folded in and between leaves, and are always laid in the shallow parts of water bodies. The jelly mass is 3 mm diameter, and the egg diameter ca. 2 mm, brown above and yellow-white below. A female can lay from several dozens up to several hundreds of eggs per season (Tsutsui, 1931; Franzen & Franzen, 2005). Larvae hatch at a length of 10 mm after some three to four weeks – depending on water temperature – and after 3-4 months reach a total length of 40-45 mm at metamorphosis. The juveniles are dark brown to black in colour, initially with a pale yellow belly. Some forms have a yellow-orange stripe over the body and dorsal and ventral sides of the tail. They eat mainly Collembola and Acari and develop the red colouration of the ventral skin as they mature (Matsui et al., 2003a; 2003b). Juvenile newts normally live on land until they reach sexual maturity after three years.

The range of Cynops pyrrhogaster.

Distribution

Cynops pyrrhogaster inhabits the Japanese main islands Honshu, Kyushu and Shikoku; the smaller islands Sado, Awaji, Iki and Naga; the Goto and Koshikijima archipelagos; and the Oki and Amakusa island groups (Hayashi & Matsui, 1988; Goris & Maeda, 2005; Tominaga et al., 2013).

Habitat

This newt occurs in various habitat types, such as forests and meadows, as well as cultivated land. A wide variety of water bodies may serve as breeding habitats including rice paddies, marshy meadows with holes and puddles, roadside and irrigation ditches, and ponds and lakes, but occasionally also streams, at altitudes between 120 and 1,140 m (Marunouchi et al., 2000).

Behaviour

Hibernation may take place on land or in the mud on the bottom of a pond. At water temperatures of 7-8°C in March, animals inhabit breeding ponds, where they lead a mainly nocturnal life, and start breeding immediately after hibernation (Tsutsui, 1931). Depending on altitude and geographical region, the breeding season extends to early June, with a peak in April at water temperatures between 8-15°C. At this time mating can also be observed during the day. Egg laying starts soon after mating and continues until July at water temperatures between 14-20° C (Tsutsui, 1931).

Cynops pyrrhogaster, breeding habitat near Kyoto. Photo: Max Sparreboom. 195

As in C. ensicauda, food may consist of small snails, aquatic insects, earthworms, eggs of their own kind, rotten meat, rotten plants, and rice (Sato, 1943). Cynops pyrrhogaster may be protected from predation to some extent by its skin venom, but nevertheless falls victim to snakes (Atobe et al., 2011). Reproduction is similar in all species of Cynops, and takes place after a more or less elaborated courtship display in the breeding pond. The male tries to persuade the female to accept his sperm by courting her. As soon as he is aware of her presence, he approaches her and smells her body by keeping his snout close to hers or to her cloacal region. He follows her and tries to block her path by moving in front of her and presenting her with the side of his head. He bends his tail along the side of his body and starts making fanning movements in the direction of her snout. When the female is responsive she will stand still and approach the male. This signals to the male that he can stop fanning and proceed to the next phase. He turns around and moves ahead of her, his tail undulating harmonically, the female following him, touching or nibbling at his tail while she walks behind. The male raises his tail and deposits a spermatophore. He may put down several spermatophores within the same courtship sequence. If the female is still responsive, she moves ahead, her cloaca moving over the spermatophore and picks up the sperm cap. The courtship behaviour patterns are

described by Tsutsui (1931), Kawamura & Sawada (1959) and Arnold (1972). Behaviour patterns may vary between populations. In the Sasayama form, for instance, the male has particularly prominent glands at the side of his head and body. During fanning he places a hind leg on the neck or back of the female, places a fore leg in font of her snout and attempts to press the side of his head against the female’s snout. In other forms, the female bites the male rather vigorously as a sign that she is responsive. Kawamura & Sawada (1959) and Sawada (1963a, 1963b) found that the sexes do not always recognise the courtship displays of individuals from different populations. A male from one population may not accept the bite of a female from another population, or a female from certain neighbouring populations may not accept the hind leg on her back from a Sasayama male, and will move away. In such cases individuals will not mate and their populations may become reproductively isolated and thus be on their way to forming separate species.

Threats and conservation

Although once common and still seemingly abundant in some localities at certain times of the year, many populations are in decline and the number of animals observed is dwindling, especially in the lowlands. Habitats are disappearing due to pressure from human activities and the pet trade probably takes a heavy toll. Nonetheless, the species is presently regarded as of Least Concern (IUCN, 2013).

Observations in captivity

Cynops pyrrhogaster has frequently been kept in aquariums and may be kept in water all year round. In captivity this species requires temperatures from 15-20°C in summer and 5-10°C in winter. The animal is long-lived and 20-25 years is not exceptional with some records of individuals over 40 years of age (Bogaerts, 2013b). The species will breed successfully if pairs come from the same collecting localities. There is a large body of literature on captive breeding of this species (Sparreboom, 1998; Franzen & Franzen, 2005).

References

Arnold (1972); Atobe et al. (2011); Bogaerts (2013b);

Franzen & Franzen (2005); Goris & Maeda (2005); Hayashi & Matsui (1988, 1990); Hoogmoed (1978); IUCN (2013); Kawamura & Sawada (1959); Marunouchi et al. (2000); Matsui et al. (2003a, 2003b); Mertens (1969);

Cynops pyrrhogaster, courtship, male on the right. Photo: Max Sparreboom.

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Sato (1943); Sawada (1963a, 1963b); Sparreboom (1982, 1998); Thorn (1969); Tominaga et al. (2013); Tsutsui (1931).

Cynops wolterstorffi (Boulenger, 1905) Description

Head a little longer than wide, and high in the occipital region. The snout is short and rounded, reaching over the lower jaw. Distinct labial lobe. Eye big, situated dorso-laterally. Paratoid glands small. Gular fold more or less well-developed. Stout body, a little higher than wide, no dorso-lateral ridges. Tail a little shorter than head and body, compressed at the base and high, featuring a crest on dorsal and ventral sides. Tail end rather pointed. Limbs slender, with four digits on forelimbs and five on hindlimbs. Digits do not have claws and are not webbed. Skin smooth, but rougher than, for instance, in C. orientalis. Colour is black on the back, with a distinct orange-coloured vertebral ridge extending onto the tail. Occasionally orange spots on head and sides of the body. Colour of ventral side red or orange with irregular dark spots, sometimes forming longitudinal rows (Chang, 1936). A noticeable orange-red spot behind the eye, at the corner of the mouth.

The male has a deep blue tail in the breeding season (Zhao, 1998). The male cloaca is rounded but not very prominent, the female cloaca forms a short fold. Many mature specimens have gill vestiges of various lengths. Individuals of 119 mm long have been found with complete gills and gill filaments (Fei et al., 2006). One of the type specimens has gills and contains ripe ova (Pope & Boring, 1940). A good illustration is published with the original description (Boulenger, 1905, plate 17; copied in smaller format in Wolterstorff, 1926). Photos of preserved specimens are published in Wolterstorff (1934, plate 1), who remarked that this newt had a fish-like appearance, adapted to an entirely aquatic life. There are no photos of living specimens. Total length 107-128 mm for males, 111-152 mm for females (Fei et al., 2006).

Cynops wolterstorffi, illustrations of the type description by Boulenger (1905). The species is considered extinct. 197

Diagnosis

A fairly large newt compared with other Cynops species, with a strong tendency to neoteny. Red spot at the corner of the mouth, an arched back, inconspicuous paratoid glands and bluish colour of the tail in the male, similar to C. cyanurus (Zhao & Hu, 1988a). Eggs and larvae have not been described.

Distribution

The species’ known distribution is limited to Kunming Lake (Yunnan-fu, Yunnan Lake), in the Chinese province of Yunnan, situated on a plateau at approx. 1,800 m altitude (Fei et al., 1999).

During the breeding season in April and May, thousands of animals were reported swimming among aquatic plants in the shallow parts of the lake’s shores. It was still reported as abundant in 1950 but none have been found since 1979 (Zhao, 1998).

Threats and conservation

Anecdotal records of newts coming to the surface for fish bait held out by fishermen date back to the 1970s and 1984. However, authoritative surveys in the area have not yielded any newts since 1979. The species is considered to be Extinct (Zhao, 1998).

Three factors are held responsible for the presumed extinction of the species: 1. pollution of Kunming Lake, due to the growth of Kunming city and increased disposal of industrial waste and domestic sewage into the lake; 2. decrease of suitable lake habitat due to land reclamation, especially in the northern part of the lake; and 3. increased presence of natural enemies such as Grass Carp and duck, and possibly the introduction of Bull Frogs (Rana catesbeiana, now also named Lithobates catesbeianus) (Zhao, 1998).

Observations in captivity

There are no reports of this species being maintained in captivity.

Comments

Cynops wolterstorffi was long placed in a separate genus Hypselotriton on the basis of studies on skull morphology (Herre, 1939; Pope & Boring, 1940; Thorn, 1969), but Chang (1936) and Zhao & Hu (1988a) considered the species morphologically very similar to C. cyanurus and placed it in Cynops. Fei et al. (2012) placed it in Hypselotriton once more.

The range of Cynops wolterstorffi.

Habitat

This newt used to be found in shallow waters along the northern part of Kunming Lake, and also in irrigation canals, ponds and swamps. Hibernation would take place in deeper waters of the lake (Zhao, 1998). The population was large before the 1960s, with more than one newt per ten square meters of water surface (Fei et al., 2006).

Behaviour

The Kunming Lake Newt was most probably entirely aquatic but little is known of its natural history.

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Local knowledge of this newt is now restricted to the reports of a few older fishermen, who were questioned about its occurrence in the lake (Zhao, 1998). No molecular data are available for this species. DNA extraction from museum specimens may settle its relationship to C. cyanurus and other Cynops species.

References

Boulenger (1905); Chang (1936); Fei et al. (2006); Fei

et al. (2012); Herre (1939); Pope & Boring (1940); Thorn (1969); Wolterstorff (1926, 1934); Zhao (1998); Zhao & Hu (1988a).

Echinotriton Nussbaum & Brodie, 1982 Echinotriton is unique among amphibian genera in having an anteriorly curved spine on the posterolateral surface of each quadrate. Echinotriton is most similar to Tylototriton, but differs in a number of significant morphological and life history features (Nussbaum & Brodie Jr, 1982; Zhao & Hu, 1988a). The ribs of the middle trunk region are long and curved; the distal tips of the ribs have no muscular attachment, are sharptipped, and often penetrate the skin through the primary warts. Echinotriton has a stockier body than Tylototriton, with shorter limbs, digits and tail. The adults are completely terrestrial and lay their eggs on land; the eggs measure over

3.0 mm in diameter (Zhao & Hu, 1988a). The southern and south-eastern Asian genera Echinotriton and Tylototriton are placed in a clade with the European and North African genus Pleurodeles (Hayashi & Matsui, 1989; Weisrock et al., 2006).

Echinotriton andersoni (Boulenger, 1892) Echinotriton chinhaiensis (Chang, 1932)

References

Hayashi & Matsui (1989); Nussbaum & Brodie Jr (1982);

Weisrock et al. (2006); Zhao & Hu (1988a).

Echinotriton andersoni (Boulenger, 1892) | Anderson’s Salamander Description

Echinotriton andersoni is a stout, flat salamander with a series of 12-15 conspicuous, knob-like lateral glands. Vomero-palatine teeth in V-shape, arranged in two longitudinal series, meeting in front (Stejneger, 1907). Body broad and flattened; head broad and triangular in shape.

Colour is uniformly dark brown or black on the dorsal and ventral sides, with only the underside of the tail, the cloacal region, and the soles of the feet yellow-orange in colour. Animals from Tokunoshima often have a prominent orange colouration on the lateral warts.

Echinotriton andersoni, northern Okinawa. Photo: Max Sparreboom.

Echinotriton andersoni, Tokunoshima. Photo: Max Sparreboom.

Echinotriton andersoni, Amami. Photo: Max Sparreboom. 199

There is no obvious morphological distinction between the sexes (Inger, 1947; Nussbaum & Brodie Jr, 1982). In both sexes the cloacal opening consists of a longitudinal slit. When slightly opened, the cloaca of the female is smooth on the inside, whereas that of the male is more rugose. Females with eggs have a distended abdomen. Total length 13-16 cm (Inger, 1947; Thorn, 1969); tail usually shorter than snout-vent length. Levels of genetic variability within samples from island populations are within the intrapopulational range previously reported for other salamandrids (Hayashi et al., 1992). There is substantial genetic divergence between populations from the Okinawa and Amami Island Groups. Populations from the southern part of Okinawa Island are more closely related to those from Tokashiki Island than to those from the northern and central parts of Okinawa (Honda et al., 2012).

The female lays large, single eggs on land, in one or several clutches (Utsunomiya et al., 1978). The egg capsule measures ca. 7 mm in diameter and consists of three layers, the egg proper being 3.0-3.2 mm in diameter. It is almost white, lacking brown pigments (Sato, 1943). Larvae are flushed out of their terrestrial oviposition sites by heavy rain and are capable of finding their way to water by crawling and leaping through the mud (Utsunomiya et al., 1978). The larvae hatch when they are approx. 20 days old; they are without balancers, ca. 17 mm in size, and still have yolk (Igawa et al., 2013). They have a pair of bushy gills and a broad head. The colour is yellow-green, darkening with age.

Distribution

Echinotriton andersoni is closely related to, and very similar to the Chinese sister species E. chinhaiensis, but differs from it in having rows of secondary warts running along each side of the vertebral crest, between the vertebral column, and in the row of primary warts, supported by the ribs.

This species is distributed on seven islands of the Ryukyu archipelago, including Amami-o-shima, Yorojima, Tokunoshima and Ukejima of the Amami group, and Okinawajima, Sesokojima, and Tokashikijima of the Okinawa group (Hayashi et al., 1992; Honda et al., 2011; IUCN, 2013). There are old records of it occurring on Mt. Kuanyinshan north of Taipei in Taiwan, but its presence there has not been confirmed in recent years (Zhao & Adler, 1993; Zhao, 1999; pers. obs., 2008). The species is presently considered extinct in Taiwan (Zhao, 1998; IUCN, 2013). On Okinawa, the species is rare and occurs in isolated patches of forest (Hayashi et al., 1992;

Echinotriton andersoni, hatchling larva, Tokunoshima. Photo: Max Sparreboom.

Echinotriton andersoni, developed larva, Tokunoshima. Photo: Max Sparreboom.

Echinotriton andersoni, young larva, Tokunoshima. Photo: Max Sparreboom.

Echinotriton andersoni, juvenile, Tokunoshima. Photo: Max Sparreboom.

Diagnosis

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Eggs and larvae

Salamanders of the Old World | Echinotriton

Echinotriton andersoni, habitat along roadside gutter, Tokunoshima. Larvae at different stages of development were found in the gutter. Photo: Max Sparreboom.

Kato & Ota, 1993). On Tokunoshima the species occurs in and near sugar cane fields, at altitudes of 100-200 m, in areas which were covered by forest until the mid-1960s. Their occurrence in the remaining patches of forest on that island is doubtful (Utsunomiya et al., 1978).

Habitat

This species inhabits vegetated areas with constantly humid substrates in broad-leaved evergreen forest, secondary forest, grassland and swamp (IUCN, 2013). Adults live in leaf litter, in rocky crevices, and under rocks and logs. They may even appear in or near cultivated fields (Goris & Maeda, 2005).

Behaviour

Both male and female Echinotriton andersoni lead a largely hidden terrestrial life and are difficult to observe outside the breeding season. Food consists of terrestrial Isopoda and Coleoptera, earthworms and spiders (Sato, 1943).

The range of Echinotriton andersoni.

The reproductive season may start as early as October-November, depending on the rainfall pattern (Goris & Maeda, 2005), but more usually extends from early February to late June, with a peak between the middle of March and early April (Utsunomiya 201

et al., 1978). Only the females move to the oviposition sites. Males are far less commonly found. Mating takes place on land and has only been observed in the laboratory. The male approaches the female and sniffs at her body. The couple makes a circular movement, in the course of which the male excretes a thread of mucous from his cloaca, surrounding the female by a spiderweb-like string of mucous attached to the substrate (Utsunomiya, 1982; Utsunomiya & Matsui, 2002). The male then deposits several spermatophores. Sperm pick-up by the female has not yet been observed, but probably the female is led over the spermatophore, in a similar way to E. chinhaiensis (Sparreboom et al., 2001a). Sperm may be stored in the female cloaca for at least four months (Utsunomiya, 1982). Both egg-laying and hatching of the larvae appear to be related to rainfall. Eggs are laid in humus or under rotting leaves in sites close to ponds, puddles and springs. Eggs may also be laid before the pond fills with water. Echinotriton andersoni exhibits a stereotypic, rigid antipredator posture, during which the body is flattened and curled up and the hands and tail are raised. The species has sharp, elongated, ribs with sharp epipleural processes, capable of piercing through the lateral warts (Brodie Jr et al., 1984).

Threats and conservation

It is difficult to detect population trends in this species due to its secretive habits. It is not a common species and not many populations have been followed systematically. Utsunomiya et al. (1978) found dialect names for the species’ localities in Tokunoshima, suggesting that people were familiar with it in the past, when it must have been more common. Being secretive, it is not often noticed by local people.

Suitable habitats combining features such as sufficient cover for the eggs and suitable water bodies for the development of larvae are becoming rare. It is impossible to know the extent of damage to population numbers caused by clearing original forest to make room for sugar cane plantations (Utsunomiya et al., 1978). Road and drainage ditch construction, and deforestation further contribute to fragmentation of the species’ scarce habitats and cause decreases in the number and size of its populations. The species also falls victim to the Java Mongoose, an invasive species known for its negative impact on native wildlife in Japan. The species is classified as Rare by Kato & Ota (1993) and listed as Vulnerable in the Red Data Book (Environment Agency of Japan, 2000; Ota, 2000a, 2000b; Ota & Toda, 2000). The species is designated as a natural monument in both Okinawa and Kagoshima Prefectures, but wild-caught specimens continue to appear in the overseas pet trade (Igawa et al., 2013). It is listed as Endangered by IUCN (2013).

Observations in captivity

Echinotriton andersoni has been captive-bred on a small scale (Nussbaum & Brodie Jr, 1982; Utsunomiya, 1982; Snider & Zippel, 2000; Fleck, 2006). In Nago (Okinawa), three breeding colonies, originating from three different islands, have been set up to help preserve this species and conserve the genetic diversity of natural populations. Breeding was successful and simple to achieve at temperatures between 20-25°C (Igawa et al., 2013).

References

Brodie et al. (1984); Environment Agency of Japan

(2000); Fleck (2006); Goris & Maeda (2005); Hayashi et al. (1992); Honda et al. (2011, 2012); Igawa et al. (2013); Inger (1947); IUCN (2013); Kato & Ota (1993); Nussbaum & Brodie Jr (1982); Ota (2000a, 2000b); Ota & Toda (2000); Sato (1943); Snider & Zippel (2000); Sparreboom et al. (2001a); Stejneger (1907); Thorn (1969); Utsunomiya (1982); Utsunomiya & Matsui (2002); Utsunomiya et al. (1978); Zhao (1998,1999); Zhao & Adler (1993).

Echinotriton chinhaiensis (Chang, 1932) | Chinhai Salamander Description

Echinotriton chinhaiensis is a stout salamander with flattened body and head, and a series of ca. 12 conspicuous knoblike, porous lateral glands. Head broad and triangular in shape. Bony ridges on the head not prominent. A triangular projection posterior to the mouth corresponds to the unique quadrate hook on the skull (Fei et al., 2006). Skin granular. Vomeropalatine teeth in V-shape, arranged in two longitudinal series, meeting in front. Tail shorter than snout-vent length. Colour uniformly dark brown or black on the dorsal and ventral sides, with only the posterior margin of the paratoid gland, the

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projection behind the mouth, the underside of the tail, the cloacal region, and the palms and soles coloured yellow-orange. In some individuals the knob-like lateral warts are orange in colour (Fei et al., 2006). No obvious morphological distinction between the sexes. In both sexes the cloacal opening consists of a longitudinal slit. When slightly opened, the cloaca of the female is smooth on the inside, whereas that of the male is more rugose. Females with eggs have a distended abdomen. In the male the vent is swollen during the mating season.

Echinotriton chinhaiensis, female with recently laid eggs, Ruiyansi Forest Park, Beilun, Zhejiang. Photo: Max Sparreboom.

Echinotriton chinhaiensis, female, Ruiyansi Forest Park, Beilun, Zhejiang. Photo: Liuchang Liu.

Eggs and larvae

The female lays 72-94 large, single eggs on land, in one or several clutches (Cal & Fei, 1984). Communal nesting sites may contain several superimposed layers of eggs (Xie et al., 2000). The egg capsule measures from 7.2-10.5 mm in diameter and consists of three layers; the egg proper is 3.2-3.8 mm in diameter. It is light yellow, lacking brown pigments (Cai & Fei, 1984). The female does not attend to the eggs and moves away from the breeding site immediately after

Echinotriton chinhaiensis, male, Ruiyansi Forest Park, Beilun, Zhejiang. Photo: Max Sparreboom.

Total length 109-139 mm in males and 124-151 mm in females (Chang, 1932, 1936; Cai & Fei, 1984; Ye et al., 1993; Fei et al., 2006).

Diagnosis

Echinotriton chinhaiensis is closely related to, and very similar to its Japanese sister species E. andersoni (Zhao & Hu, 1988a), but differs in lacking the rows of secondary warts running along each side of the vertebral crest, between the vertebral column, and in the row of primary warts, supported by the ribs. It has only one epipleural process on each of ribs 2-4. The fifth toe is normally developed; it has 5 metatarsals and 9 tarsals (Cai & Fei, 1984). Genetic diversity is low, but not significantly so (Xie, 1999).

The range of Echinotriton chinhaiensis. 203

egg laying. After about 3-4 weeks, in May, the larvae are flushed out of the terrestrial oviposition sites by heavy rain and can find their way to water by wriggling and leaping several centimetres above the ground (Xie, 1999; Xie et al., 2000). Balancers may be observed in the embryo 4-5 days after oviposition. Larvae hatch without balancers and measure ca. 20 mm. They can survive 3-4 days on land. Metamorphosis follows after 58-88 days (Xie et al., 2001). From egg to metamorphosis takes ca. 110 days. Newly metamorphosed salamanders with a total length of 34-40 mm climb onto land in August (Cai & Fei, 1984; Xie, 1999). The salamanders attain sexual maturity in their third or fourth year. Only females were found and most were 5-6 years old (Yang et al., 2011).

Distribution

Echinotriton chinhaiensis is only known from its type locality and two nearby valleys east of the city of Ningbo (i.e. Chengwan, Ruiyansi and Qiushan, district of Beilun, province of Zhejiang, China, respectively). Over the last 20 years, the species has only been reported occasionally from the type locality where it inhabits a forested area 100-200 m above sea level (Fei et al., 1999).

Habitat

Typical spawning habitats around the ponds to which the females migrate are characterised by a combination of features: dense plant cover around the ponds and vegetation comprising an upper layer of evergreen broad-leaved trees, a

middle layer of shrubs, and a lower layer of grasses, creating a dark, humid habitat. The ponds are semipermanent with a pH value of 6-7. The water bodies are small and shallow, and fed mainly by rain water. The only three ponds left after 2008 are 6-9 m 2 with a maximum water depth of 30-40 cm (Liu et al., 2010). The eggs are laid on slopes and flat ground directly bordering the ponds, with a surface consisting of loose soil and stones and invariably covered by a thick layer of leaf litter (Xie et al., 2000, 2002)

Behaviour

In 1999, the population of this salamander in Ruiyansi Forest Park probably consisted of no more than ca. 370 adult animals (Xie, 1999). Both males and females lead a largely hidden terrestrial life and are difficult to observe outside the breeding season. They are inactive during the day and very slow-moving and inconspicuous when active. Hibernation takes place from November-March. Food consists of earthworms, snails and Scolopendridae (Cai & Fei, 1984). In the reproductive season, only the females move to the oviposition sites. Males are rarely found. Mating takes place on land and has only been observed in captivity (Sparreboom et al., 2001a). The male approaches the female on land and deposits several spermatophores. The couple makes a circular movement, during which the female maintains orientation towards the cloaca of the male. The male excretes a thin mucous thread from his cloaca onto the substrate. In the course of the circular

Echinotriton chinhaiensis, habitat, Ruiyansi Forest Park, Beilun, Zhejiang. Photo: Max Sparreboom. 204

Salamanders of the Old World | Echinotriton

Diagrammatic representation of reproductive behaviour in the Chinhai Salamander, Echinotriton chinhaiensis. Female is shaded, male is non-shaded. Solid arrows indicate direction of movement; thin arrows indicate small-amplitude movements with sacral region (vent-swinging). The triangle represents a spermatophore. Red lines represent mucous thread excreted by the male. A. Male approaches female. B. Male nudges female and female turns towards him. Male starts marking a trail and deposits a spermatophore. C. Male and female orient to each other; the male retreats; the couple forms an elliptical circle. The male excretes a thin string of mucous substance, mounting it on the substrate, and moves away sideways from the spermatophore. D. While standing still during a pause in the circling movement, both animals perform vent-swinging. E. The couple continues to move slowly in the circle. F. The female is led over the spermatophore; she moves her hind-body sideways, her cloaca placed over the spot where the spermatophore was deposited; she performs vent-swinging and picks up the spermatophore in her cloaca (indicated by the arrow). The male resumes marking a trail and is on the point of depositing a second spermatophore. G. An intruding female (left) approaches a courting pair during circling behaviour. H. Inner animal in the circle is the intruding female, who attempts to sneak the courtship from the first courting female (sexual interference). Art: Bas Teunis, redrawn from Sparreboom et al. (2001a).

movements the female is led over the spermatophore. Eggs are laid in the humus or under rotting leaves close to ponds, puddles and springs. The breeding season extends from late March to late April (Xie et al., 2000). Migration to the oviposition site and hatching of the larvae both appear to be related to rainfall. Echinotriton chinhaiensis exhibits a stereotyped, rigid antipredator posture, during which the body is flattened and curled up and the hands and tail are raised. The species has sharp, elongated ribs with sharp epipleural processes, capable of piercing through the lateral warts (Brodie et al., 1984; Cai & Fei, 1984).

Threats and conservation

The only population that has been followed over the years is in Ruiyansi Forest Park, near the city of Ningbo in the province of Zhejiang. Suitable habitats with the correct combination of characteristics such as sufficient cover for the eggs and appropriate water bodies for the development of larvae, are rare. Road construction and deforestation contribute to fragment these scarce habitats and to lead to a decrease in the size and number of populations.

a

e

b

f

c

g

d

h

Pollution of the breeding habitat is also a serious threat (Xie et al., 2000). Cai & Fei (1984) and Fei (1992) noted a rapid decrease in suitable habitat in the valley, with the growth in tea plantations, orange orchards and other small scale agriculture. The one population that was known, that of Ruiyansi, still looked relatively healthy but was isolated and vulnerable, and was considered endangered. As a consequence, in 1988 Echinotriton chinhaiensis was listed in the grade 2 category of major state protected wildlife (Zhao, 1998), meaning that capture and handling of this salamander were henceforth licensed by the state government. The species is protected by law in Zhejiang (Huang et al., 1990). In 1999, artificial ponds were created near the known breeding ponds in Ruiyansi Forest Park and attempts were made to prevent farmers from dumping pollutants and cleaning their equipment in the ponds. The artificial ponds were colonised by salamanders one year later (Sparreboom et al., 2001b), but this did not prevent further decline in the population’s reproductive output each year. A survey in 2008 revealed that one of the four breeding ponds had been destroyed, and that the total number of females that came and laid eggs near the ponds had fallen to 47, less than 205

half the number found in 1998-2000 (Liu et al., 2010). This decrease is probably due to construction work, tourism and two heavy typhoons in 2007. Echinotriton chinhaiensis is amongst the rarest and most threatened salamander species on earth and is considered Critically Endangered (IUCN, 2013).

Observations in captivity

The Chinhai Salamander has been captive-bred on a small scale in an outdoor enclosure at the Chengdu Institute of Biology and its care is, in principle, easy. At present there is no stable ex-situ breeding group.

Comments

During a vertebrate survey in Zhejiang, held in 1999, a new locality was discovered in Qiushan valley: Two

female salamanders were found at the edge of a small puddle, entirely covered with terrestrial vegetation. The species has not been reported from the terra typica (Chengwan) for many years and could not be found during a survey in April 1999. The animal is not generally noticed by local inhabitants, except incidentally while digging up bamboo sprouts. It must be considered extremely rare.

References

Brodie Jr et al. (1984); Cai & Fei (1984); Chang (1932,

1936); Fei (1992); Fei et al. (1999, 2006); Huang et al. (1990); IUCN (2013); Liu et al. (2010); Sparreboom et al. (2001a, 2001b); Xie (1999); Xie et al. (2000, 2001, 2002); Yang et al. (2011); Ye et al. (1993); Zhao (1998); Zhao & Hu (1988a).

Echinotriton chinhaiensis, female, Ruiyansi Forest Park, Beilun, Zhejiang. Photo: Max Sparreboom.

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Salamanders of the Old World | Echinotriton

Euproctus Gené, 1839 A genus of small- to medium-sized newts (7-15 cm). Caudosacral vertebrae with short transverse processes directed obliquely backwards. Head rather large, depressed, longer than broad. Upper jaw extending over lower jaw. Gular fold absent. Limbs moderate in size; four fingers, five toes, all without webbing. Skin finely tubercular on flanks and head, smooth ventrally. Body relatively flat or slightly rounded in cross section; no dorsal crest. Tail about as long as head and body and compressed laterally. Lungs absent or much reduced. Males have spurs on hind legs (Carranza & Amat, 2005). Their distri-

bution is restricted to the Mediterranean Islands of Corsica and Sardinia. The genus Euproctus is basal to a clade containing Ichthyosaura, Laotriton, Pachytriton, Cynops and Paramesotriton (Pyron & Wiens, 2011).

Euproctus montanus (Savi, 1838) Euproctus platycephalus (Gravenhorst, 1829)

References

Carranza & Amat (2005); Pyron & Wiens (2011);

Wolterstorff (1901).

Mountain brook newts, Calotriton asper (Triton asper, fig. I abc), Euproctus montanus (Triton montanus, fig. II abc) and Euproctus platycephalus (Triton Rusconii, fig. III abc), painted from living specimens by Lorenz Müller. Plate V in Wolterstorff, 1901.

Euproctus montanus (Savi, 1838) | Corsican Newt Description

A small to medium-sized newt with welldefined paratoid glands. Snout rounded, upper jaw slightly extending over lower jaw. Tongue rather large and protractile. Labial folds and gular fold absent. Tail a little shorter than snout-vent length, compressed laterally and pointed. Body

relatively flat. Dorsal skin smooth in aquatic phase and finely tubercular in terrestrial phase, ventral skin smooth in both aquatic and terrestrial phases. Fingers and toes short and depressed. Spurs on hind legs of males laterally flattened and not strongly protruding (Carranza & Amat, 2005). 207

Eggs and larvae

Euproctus montanus, female, Corsica. Photo: Burkhard Thiesmeier.

Euproctus montanus, male, Corsica. Photo: Burkhard Thiesmeier.

Colour brown or olive above, sometimes with lighter, yellowish, reddish or greenish markings that may form a thin vertebral line. Venter yellowish, grey or brown, speckled with whitish dots. Male cloaca conical and projecting backwards. Cloacal chamber contains a pseudopenis which may protrude from the cloaca during amplexus (Brizzi et al., 1995a). Female cloaca hemispherical with a vertical slit. Total length usually 8-10 cm, max. 13 cm.

Diagnosis

A small-sized, brownish newt; smooth-skinned in water, rough-skinned on land. Lungs absent. Male with broad head and spurs on hind legs. No dorsal crest in breeding season.

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Eggs are found between mid-April and end September. Eggs are usually laid as a clutch, attached underneath stones, or to a partly submerged a rock which is sprayed by water, but also occasionally among water plants. Several clutches may be found together under a single stone. A female lays a clutch of 20-35 eggs or more each year. One female was reported to lay 54 eggs within a two week period (Alcher, 1981b). Miaud & Muratet (2004) report clutches of 10-120 eggs. Eggs measure 2.6-4.1 mm in diameter, not including the gelatinous capsule. At a water temperature of 15°C embryonic development takes about 40-50 days. Upon hatching larvae measure either 13.3 mm on average (Alcher, 1988), or 16-18 mm (Thiesmeier et al., 1996). Developing larvae are light brown and can be recognised by their elongated, rectangular head (Bedriaga, 1897). They have a rounded tail-tip and can be distinguished from larvae of the Fire Salamander (Salamandra corsica) by the absence of a bright spot at the base of the legs. The caudal fin extends only slightly onto the back (Miaud & Muratet, 2004). Larval development may take 244-280 days, depending on water temperature. Higher temperatures result in much faster development: 90-120 days at temperatures between 15-19°C (Thiesmeier et al., 1996). Larvae live hidden under stones, away from the current. At metamorphosis juveniles measure between 36-55.5 mm, with smaller sizes recorded in animals from lower altitudes and larger sizes in animals from higher altitudes. Larvae from higher altitudes may take one or two winters to reach metamorphosis. Larvae may be found all year round (Miaud & Muratet, 2004). Juvenile Euproctus montanus have a green to yellow pattern of spots on a dark brown background and a thin orange, yellow or brownish vertebral stripe (Rimpp & Thiesmeier, 1999). Juveniles reach sexual maturity at an age of 4-5 years (Maillet & Schultschik, 2013b).

Distribution

Euproctus montanus is endemic to the Mediterranean island of Corsica, France, where it is widely distributed from Cap Corse in the north to Montagne de Cagne in the south, and from Golfe de Girolata in the west to the start of the lowlands in the east (Delaugerre & Cheylan, 1992). It occurs from sea level up to 2,289 m altitude in the Lac du Cinto (Lescure & de Massary, 2012).

Habitat

The species inhabits streams in forested or overgrown areas, where it prefers quieter, deeper parts downstream from waterfalls, and where cover is provided by flat stones. It also occurs in mountain lakes. On land this salamander uses spaces underground between roots of trees and shrubs, and under logs and stones. They can be found especially between the roots of sweet chestnut trees along stream banks (Rimpp & Thiesmeier, 1999a).

Behaviour

Animals become active at temperatures above 5°C. Adults eat invertebrates found on stream bottoms, such as stoneflies, ephemerids, caddisflies and to a lesser degree, salamander larvae, and the eggs and young of its own species and of Discoglossus frogs (Duguet & Melki, 2003; Lanza et al., 2007).

Reproduction takes place in water when temperatures range between 10-15°C. Matings may also occur on land at the water’s edge. The breeding season is dependent on climate and altitude. At lower altitudes, reproduction may take place in March-June as well as in September-October, and at higher altitudes in JulyAugust. Animals in captivity reproduce between November and April. In summer, after reproduction, the animals move onto land and lead a terrestrial life, hidden underground. Following rainfall in September-October, they return to the water (Rimpp & Thiesmeier, 1999a). In the breeding season, usually spring, the male actively searches for a female. He grasps her by clasping her pelvic region with his tail, at the same time grabbing her tail with his mouth and pulling it straight. During this amplexus the male’s body is placed diametrically over that of the female and the male’s cloaca is pressed onto that of the female. Of all salamandrids, E. montanus appears to have the most direct, intimate contact between male and female. It is unclear if the hind leg

spurs massage the male’s own cloaca or play a role in sperm transfer or stimulation of the female cloaca (Thiesmeier & Hornberg, 1990; Rimpp & Thiesmeier, 1999a). The reduced cloacal glands of the male probably relate to the direct transfer of sperm, for which no spermatophore structure is needed (Brizzi et al., 1995a). Copulation may take up to four hours and a male may deposit two sperm packages. The female usually lays her eggs as a clutch, attached to the underside of a flat stone in the stream. Observations in captivity have shown that the female stays with the eggs, guarding them until they hatch, a form of maternal care that is rare among salamandrids (Alcher, 1981b, 1985; Thiesmeier et al., 1996; Rimpp & Thiesmeier, 1999a).

Threats and conservation

Although not directly threatened in most of its range, in certain localities these salamanders are threatened by habitat fragmentation, introduction of predatory fishes (e.g. trout), water pollution and over extraction of water for agriculture and tourism. The conservation status of this species is presently considered as of Least Concern (IUCN, 2013).

Observations in captivity

Euproctus montanus has been bred in captivity on several occasions and the reproductive behaviour and development of larvae and juveniles has been described from detailed observations. In captivity this species requires water temperatures between 12-18°C and a rest period of several months at temperatures between 4-7° C (Alcher, 1980a). Ideally, tanks should have a water and a land section, although the animals can often be kept in water all year round. A water pump is useful to keep the water moving slowly. Captive animals should be given small insects and their larvae, since worms are often refused. Euproctus montanus has lived in captivity for 5-7 years (Rimpp & Thiesmeier, 1999a), but is more difficult to breed than E. platycephalus. Details of captive maintenance of the two Euproctus species and Calotriton asper are provided in Alcher (1980a), Thiesmeier & Hornberg (2002) and Maillet & Schultschik (2013b).

References

Alcher (1980a, 1981b, 1985, 1988); Bedriaga (1897); Brizzi

et al. (1995a); Carranza & Amat (2005); Delaugerre & Cheylan (1992); Duguet & Melki (2003); IUCN (2013); Lanza et al. (2007); Lescure & de Massary (2012); Maillet & Schultschik (2013b); Miaud & Muratet (2004); Rimpp & Thiesmeier (1999a); Thiesmeier & Hornberg (1990,

The range of Euproctus montanus.

2002); Thiesmeier et al. (1996).

209

Euproctus platycephalus (Gravenhorst, 1829) | Sardinian Newt

Euproctus platycephalus, Villasalto, Sardinia. Photo: Max Sparreboom.

Euproctus platycephalus, juvenile, Villasalto, Sardinia. Photo: Max Sparreboom.

Description

A small to medium-sized newt with relatively flat body. Paratoid glands not well-defined. Head depressed, much longer than broad, snout semi-elliptical, upper jaw extending over lower jaw, upper lips with well-developed labial folds. Paratoid glands present, but not conspicuous. No gular fold. Tongue small, sub-elliptical, free at the sides. Lungs rudimentary. Tail about as long as snout-vent length, broad at the base and increasingly compressed laterally, ending in an obtuse point, with small upper and lower crests, the latter beginning half way along the tail. Fingers rather elongate and slender. Dorsal skin smooth or finely tubercular above, venter completely

210

Salamanders of the Old World | Euproctus

Euproctus platycephalus, terrestrial stage with dry skin, Rio Fluminaddu, Sardinia. Photo: Max Sparreboom.

smooth. Spurs on hind legs of males strongly protruding, especially in older specimens (Carranza & Amat, 2005). Colour brown or olive above, variegated with greenish, yellowish or light grey areas and an orange-reddish vertebral stripe. Venter is whitish on the sides and yellowish or reddish along the centre, with irregularly distributed black spots on belly and throat (Carranza & Amat, 2005). Male cloaca-hook extended backwards with opening directed upwards; female cloaca slightly protruding or conical with opening directed backwards and downwards (Rimpp & Thiesmeier, 1999b). Males

are longer and heavier than females and have proportionally longer and heavier head, shorter cloaca, longer tail and longer hindlimbs (Bovero et al., 2003).

tree bark in a forest close to the breeding stream. They are dark in colour with a red vertebral stripe, bright green spots behind the eyes and on the body and tail, and with brown-grey limbs (Rimpp & Thiesmeier, 1999b).

Total length 11-12 cm, max. 15 cm.

Diagnosis

A small-sized, brownish newt, smooth-skinned in water, slightly rough-skinned on land. Head long. Male with spurs on hind legs. No dorsal crest in breeding season.

Eggs and larvae

Sexual maturity is attained 2-5 years after metamorphosis and adults from four populations studied lived from 3-4 years (Angelini et al., 2008b). In captivity animals reached adulthood in the third year after egg deposition (Rimpp & Thiesmeier, 1999b; Maillet & Schultschik, 2013c).

The female lays the eggs individually under rocks and in cracks with the help of her tubular, extended cloaca, in captivity also on gravel substrate and hidden in the sand. A female may lay between 57-221 eggs per season, extending over a period of several months. Eggs measure 3-3.3 mm in diameter, 4-5 mm including the gelatinous capsule. Embryonic development takes 37.6 days on average at a water temperature of 15°C and 12.7 days at 24.5°C. Larvae are 8.8-14.5 mm on hatching. Duration of larval development also depends on temperature. At 15°C it takes 376-453 days, and 184-260 days at 20.5°C. Juveniles are fairly large, 43.8-64.0 mm in total length, at metamorphosis (Alcher, 1980a, 1980b; Rimpp & Thiesmeier, 1999b). Developing larvae are light brown and can be recognised by their elongated, rectangular head. They have a rounded tail-tip and are similar to the larvae of Euproctus montanus, except for the dorsal fin, which extends further onto the back (Bedriaga, 1897; Miaud & Muratet, 2004). Euproctus platycephalus shows a tendency to paedomorphosis and almost sexually mature specimens with gill vestiges have been reported. Juvenile newts have been found on land under

The range of Euproctus platycephalus.

Euproctus platycephalus, habitat, Villasalto, Sardinia. Photo: Max Sparreboom. 211

Distribution

Endemic to the Mediterranean island of Sardinia, Italy, where it is restricted to the eastern part of the island, from the Limbara mountains in the North, via Gennargentu in the centre, to the Sarrabus mountains in the South, and between Baunei in the east and Monte Linas in the west (Lecis & Norris, 2003; Lanza et al., 2007; IUCN, 2013).

Habitat

Euproctus platycephalus is a montane species. Its aquatic habitat consists of permanent and temporary stagnant pools, mountain streams, calm parts of rivers and small mountain lakes. Its terrestrial habitat is riverine scrub or woodland close to the water and animals are found under stones and among the roots of bushes and trees in wasteland. The species occurs between 50-1,800 m, with most records from 400-900 m (Rimpp & Thiesmeier, 1999b; Lanza et al., 2007; IUCN, 2013).

Behaviour

Most animals are active at water temperatures between 9-14°C, generally after dark (Pieroni et al., 2008). In harsh periods in winter and summer they may hide under logs and stones on land, but some individuals may live in water all year round. Food consists of aquatic invertebrates such as adult and larval arthropods, worms and molluscs. They have a preference for chironomid larvae and also eat eggs of their own species (Sotgiu et al., 2008). Potential predators are birds, small mammals, salmonid fish and water snakes (Natrix) (Lanza et al., 2007). Reproduction takes place in water in spring, in April-May, with water temperatures ranging from 9-14°C, but has also been observed following aestivation in autumn (October-November). These newts are less active in winter and mid-summer (Pieroni et al., 2008). In captivity they reproduce all year round except in July-August (Rimpp & Thiesmeier, 1999b). The male searches actively for a female with its mouth open. If he hits upon a female, he grabs her with his jaws and holds onto her body between the neck and cloaca. His tail is laid loosely over the cloacal region of the female, his body arched over that of the female during copulation, and sperm transfer takes place via direct contact between the male and female cloacas. The spurs on the male’s hind legs are used to massage the male’s own cloaca and bring about sperm transfer. Copulation can take between one and three hours, during which one sperm package

212

Salamanders of the Old World | Euproctus

is delivered. There is no tight amplexus using the tail as in Euproctus montanus and Calotriton asper (Bedriaga, 1883, 1893, 1897; Thiesmeier & Hornberg, 1990; Rimpp & Thiesmeier, 1999b). The female usually lays her eggs singly and not as a clutch, as in Euproctus montanus. There is no female parental care in E. platycephalus, such as observed in E. montanus.

Threats and conservation

Major threats to the species are pollution of water bodies, habitat fragmentation, predation by introduced trout, and prolonged drought. Its decline is not well understood. Chytridiomycosis has been detected in a population in the Sette Fratelli area (Bovero et al., 2008). It is listed as Endangered (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

Euproctus platycephalus has been bred in captivity as far as the fifth generation (Maillet & Schultschik, 2013c) and reproductive behaviour and development of larvae and juveniles has been described from detailed observations. In captivity this species prefers water temperatures below 18°C and a rest period of several months at temperatures between 6-13°C (Alcher, 1980a, 1981a). Tanks should ideally have a water and a land section, although the animals can most easily be kept in water all year round. A water pump is useful to keep the water moving slowly. Captive animals should be given small insects and their larvae. Euproctus platycephalus has lived in captivity for many years and captive breeding is straightforward. Details of captive maintenance of the two Euproctus species and Calotriton asper are provided in Alcher (1980a), Thiesmeier & Hornberg (2002) and Maillet & Schultschik (2013c) respectively.

Comments

The rarity and apparent sensitivity of Euproctus platycephalus to environmental threats is in striking contrast with the ease of breeding this species in captivity.

References

Alcher (1980a, 1980b, 1981a); Angelini et al. (2008b);

Bedriaga (1883, 1893, 1897); Bovero et al. (2003, 2008); Carranza & Amat (2005); IUCN (2013); Lanza et al. (2007); Lecis & Norris (2003); Maillet & Schultschik (2013c); Miaud & Muratet (2004); Pieroni et al. (2008); Rimpp & Thiesmeier (1999b); Sotgiu et al. (2008); Stuart et al. (2008); Thiesmeier & Hornberg (1990, 2002).

Ichthyosaura Sonnini de Manoncourt & Latreille, 1801 After it had become obvious from genetic studies that the European newt genus Triturus was not monophyletic (Weisrock et al., 2006; Steinfartz et al., 2007), new genus names have been introduced for the taxa formerly included in Triturus. The Alpine Newt was placed in a monotypic genus, which eventually received the available name Ichthyosaura (Schmidtler, 2009; Thiesmeier & Schulte (2010) discuss the nomenclatural history). In phylogenetic reconstructions, the Alpine Newt has variously been placed as sister to the Lissotriton vulgaris group (Weisrock

et al., 2006; Zhang et al., 2008) or as sister to the Asian newt genera Cynops, Paramesotriton, Laotriton and Pachytriton (Steinfartz et al., 2007; Pyron & Wiens, 2011).

Ichthyosaura alpestris (Laurenti, 1768)

References

Pyron & Wiens (2011); Schmidtler (2009); Steinfartz

et al. (2007); Thiesmeier & Schulte (2010); Weisrock et al. (2006); Zhang et al. (2008).

Ichthyosaura alpestris (Laurenti, 1768) | Alpine Newt Description

A medium-sized newt. Head a little longer than wide, snout broad and rounded. Labial folds only on posterior part of upper lip during the breeding season. Gular fold distinct. Body stocky; trunk almost quadrangular in the male in breeding condition, more rounded in the female. Tail approximately the same length as or a little shorter than the rest of the body, laterally compressed and ending in a pointed tip. In the reproductive season the male has a low, smooth-edged crest which runs along the back and continues, without interruption, onto the tail. The tail also has a ventral fin, but less high than the dorsal crest. The female only has the caudal fin. After the breeding season the dorsal crest, caudal fins and labial folds become reduced in the male. In aquatic animals the caudal fins remain present all year round. Fingers and toes short, flattened and without webbing. Skin is smooth during the breeding season or granulated outside the breeding season, and velvety during life on land (Thorn, 1969).

Background colour is dark grey, blackish or bluish, with a bright orange or reddish belly and throat. The belly is unspotted, but there may be a few small dark spots on the throat. Males have a whitish band with distinctive dark spots running from the cheeks, along the lower flanks, and onto the cloaca and tail. Between this and the orange belly, a light blue flash runs between the fore- and hindlimbs. The crest is whitish with regular dark spots which give it a zigzag or checkerboard effect along the back. Females are slightly drabber than males, and may have a greenish-blue mottled appearance. They also have the black-spotted and bluish flashes along the side, but these are less distinctive than in the male (Thorn, 1969; Griffiths, 1996). As in most newt species, the cloaca of the male is swollen in the breeding season. The male is usually 8-10 cm, the female 10-12 cm long (Thorn, 1969).

Ichthyosaura alpestris, male (left) courting female. Photo: Max Sparreboom. 213

Ichthyosaura alpestris, couple, male right. Photo: Jelger Herder.

A great number of subspecies and varieties have been described, especially from the Balkans, mainly on the basis of external morphology and colour patterns. The validity of these subspecies has been contested and it is hard to find diagnostic morphological differences between populations. Only four subspecies are recognised in a critical summary by Rocˇek et al. (2003). Analysis of mitochondrial DNA from animals sampled over the entire species’ range shows substantial genetic differentiation and suggests that there are five genetic lineages which roughly correspond to the subspecies described thus far (Sotiropoulos et al., 2007). A western lineage group (alpestris, apuana and cyreni) and an eastern lineage group (alpestris and veluchiensis) can be distinguished. The relationships within the entire group have not yet been satisfactorily resolved. Ichthyosaura alpestris alpestris: The nominotypical subspecies occurs in central Europe, reaches its northeastern limit in the western part of Ukraine, and its southern limit in the Rodope Mountains in northern Greece. The eastern lineage includes the paedomorphic forms montenegrina, piperiana and serdara from Montenegro. The western lineage includes the subspecies I. a. cyreni (Sotiropoulos et al., 2007). 214

Salamanders of the Old World | Ichthyosaura

Ichthyosaura alpestris apuana: In this Italian subspecies, the throat is more often covered with many small dark spots than in other forms. It is genetically distinct from the nominate form and occurs in the northern and central Apennine Mountains. Towards the South its distribution is more patchy, with the southernmost populations found in Calabria (Sotiropoulos et al., 2007). Ichthyosaura alpestris cyreni: This subspecies is more difficult to differentiate from the nominate form. The skull is generally more rounded in shape and there are karyological differences between cyreni and alpestris (Arano & Arntzen, 1987; Herrero et al., 1989; Sotiropoulos et al., 2007). It occurs in the Cantabrian Mountains in north-west Spain. Ichthyosaura alpestris veluchiensis: The southern limit of the Alpine Newt’s distribution is located in Greece, where the subspecies I. a. veluchiensis occurs on the central mainland and the Peloponnese, and another – thus far unnamed – lineage inhabits northern Pindus extending to southern Serbia. The morphological description of this Greek subspecies is based on some traits observed in the female: olive-greenish colour on the dorsal side; presence of black spots on the belly; skin flaps

of the upper jaw not reaching the lower jaw; snout narrow and convex viewed from above; distinct colour pattern on the flank; and sparse dark spots on the lower edge of the tail (Sotiropoulos et al., 2001). The general validity of these minor morphological differences has been questioned (Thiesmeier & Schulte, 2010). However, molecular studies have clearly established this form as a genetically distinct subspecies (Sotiropoulos et al., 2007). Apart from the genetic differences, the number of trunk vertebrae is on average higher (13) in specimens from the Vlasina and Greek lineages than in the Balkan lineage (Vukov et al., 2011). Within Greece, there are two lineages, one from the Greek mainland and the other from the Peloponnese peninsula. Individuals of the former are more blue in colour, while newts from the Peloponnese are more conspicuously spotted (Sotiropoulos et al., 2007; 2008b).

Diagnosis

A medium-sized newt with unspotted orange underparts; occasionally with some spots on the throat. Small black spots on the flanks.

Eggs and larvae

The female attaches her eggs singly by wrapping a leaf or other object around her cloaca with her hind legs and pressing the egg into it. A clutch usually consists of 70-390 eggs. Ovum is 1.5-1.7 mm in diameter and clear greybrown in colour. The diameter of the egg capsule is 2.5-3 mm (Rocˇek et al., 2003). Depending on temperature, most larvae hatch between 2-4 weeks after egg deposition. At a water temperature of 20-22°C larvae hatch after 8-9 days at a length of 7-8 mm (Rocˇek et al., 2003). A fully developed larva has a dorsal tail-fin starting at the level of the forelimbs, a ventral tail-fin and 12-13 costal grooves. Tail-tip moderately pointed with a very small, sharp pointed filament (Thorn, 1969). The colour varies greatly but is generally pale brownish-yellow becoming darker towards the tail. Larvae metamorphose after about three months at a total length of 40-50 mm, sometimes smaller, sometimes larger. Some larvae may overwinter and metamorphose the following year. The speed of growth depends on temperature and altitude. In lowland populations sexual maturity is reached after three years in males, 4-5 years in females, while at higher altitudes 9-11 years is common. Adults may reach an age of 10 years in lowland populations (Rocˇek et al., 2003), and over 30 years in mountain populations (Wagner et al., 2011). Neoteny or paedomorphosis is a regular phenomenon in I. alpestris (where individual animals reach sexual maturity without metamorphosis and retain juvenile characters into adulthood). Paedomorphosis is widespread in newts and salamanders and is believed to perhaps play an important role in evolution. Its cause has been much debated. Many authors

The range of Ichthyosaura alpestris.

believe it may be environmentally induced and connected to a relatively stable aquatic habitat or a combination of ecological factors, but a single cause has not been identified and the mechanism whereby some individuals in the same population are paedomorphic and others metamorphic remains poorly understood (Rocˇek et al., 2003; Thiesmeier & Schulte, 2010). There is some evidence that paedomorphic and metamorphic newts eat different prey (Denoël & Joly, 2001a, 2001b). The syntopic existence of the two forms allows resource partitioning, earlier reproduction in terms of age and season in paedomorphs, and differences in breeding frequency between the two forms. Although the degree of development of secondary sexual traits is very different in the two morphs, they are not sexually isolated. Indeed, they are sexually compatible and will interbreed (Denoël et al., 2001a; Denoël, 2003).

Distribution

This species occurs in central Europe, from Denmark in the north to Greece in the south. It is largely absent from the Pannonian plain and its distribution is patchy and fragmented in the southern parts of its range. The Alpine Newt is especially at home in mountain habitats, where it may occur above 2,000 m, but in spite of its name, it also occurs in lowlands (Rocˇek et al., 2003; Thiesmeier & Schulte, 2010). 215

Habitat

The Alpine Newt is a widespread and ecologically highly flexible newt, especially in terms of its choice of breeding sites. It inhabits a wide variety of water bodies: ponds, shallow temporary puddles, larger water reservoirs, and quiet parts of streams. It is especially frequent in forested areas or areas which have recently been cleared of forest. It is fairly tolerant of eutrophication and temperature changes. Ichthyosaura alpestris is the only newt species that occurs above 1,500 m altitude (Rocˇek et al., 2003). In the terrestrial phase it lives a secretive life on and under the forest floor, in the burrows of small mammals, and under logs and stones.

Behaviour

In the parts of its range where water bodies are frozen in winter, the aquatic phase and reproductive activity starts as soon as the ice disappears; in lowlands in midFebruary, and in the summer at higher altitudes. Above 2,000 m activity is limited to June-July to September. Egg laying starts in April-May and may continue until July or August (Rocˇek et al., 2003). Alpine Newts show a high degree of site fidelity (Joly & Miaud, 1989). They are active at dusk and dawn and during the morning, when sexual activity takes place. Feeding is mainly nocturnal (Martin et al., 1989). They eat chironomid larvae and pupae, larvae of crane flies (Tipulidae), mayflies (Ephemeroptera) and isopods, but also caterpillars, earthworms, and amphibian eggs and larvae. In mountain lakes, where benthic prey is rare, they eat plankton and small insects which have fallen onto the water surface (Rocˇek et al., 2003). Alpine Newts may be taken by a range of predators, such as snakes and birds, but direct observations are few. The presence of fish poses a potential danger for a populations’ survival (Rocˇek et al., 2003). Courtship and mating take place in water and have been the subject of scientific study for many years (starting with Gasco, 1881; full description in Denoël, 1996). The male performs a courtship display, which differs in some respects from that of, for instance, the Smooth Newt (Lissotriton vulgaris). The repertoire of courtship behaviours of Ichthyosaura alpestris is more limited than in L. vulgaris. Following a period of orientation, during which the male attempts to assume a position in front of the female, there is a long period of static display, more prolonged than in L. vulgaris (Halliday, 1977). The male remains stationary in front of the female, his tail flexed close to his body, beating rapidly and producing a steady stream of water which carries pheromones from the male’s cloaca to the female’s snout. In addition to chemical stimulation, the fan display provides vibrational and visual stimuli and is the most frequent element of the sexual display of this species (Denoël,

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1998). After a male has been fanning for some time, he combines a new behaviour with this display, the lean-in. In between fanning bouts he raises his body by extending his legs and leans towards the female so that his flank or tail touches her snout (Halliday, 1977; Arntzen & Sparreboom, 1989). Provided the female does not flee during the fanning display, the male then turns away from her and commences spermatophore deposition behaviour. The male creeps in front of the female, quivering his tail, and after a few seconds, deposits a spermatophore on the substrate in front of her. The female follows and nudges the base of the male’s tail with her snout, thereby eliciting spermatophore deposition. The male then creeps on, away from the female for a distance of about one body-length and turns to block her path as she follows him. The sperm mass may or may not be picked up by the female’s cloaca at this time. The male may then creep again, thus initiating a second sequence of spermatophore deposition. As many as six spermatophores may be deposited during a single courtship encounter (Hoeck & Garner, 2007). When a male encounters a female already engaged in courtship, he may interfere with the courting male’s attempts to inseminate her. The rival displays to the female and may inseminate her himself (Verrell, 1988). During the spermatophore transfer phase the male may perform various wiggling movements with his tail and tail-tip. These appear to be alternative tactics, intended to lure a nonresponsive female to the male, the wormlike movements acting as a bait-mimic. When the female is attracted to these movements she may approach the male and bite on his tail. Once the male has won her attention again, he can continue his courtship (Arntzen & Sparreboom, 1989; Denoël et al., 2001b).

Threats and conservation

There are no specific threats endangering this species more than other newts. Chemical pollution of wetlands, as well as destruction of habitat has led to extinction of the species in some localities. Introduction of fish, especially salmonids, into newt habitat poses a serious threat (Thiesmeier & Schulte, 2010). Newt habitat in the Montenegrin holokarst region has been steadily declining over the past decades, as many ponds originally created to hold water for cattle and human consumption have been abandoned. Human activities seem to have contributed to the genetic impoverishment of the southernmost, marginal populations (Sotiropoulos et al., 2008a). Given its vast distribution, the species is generally considered to be of Least Concern (AmphibiaWeb, 2013).

Observations in captivity

The Alpine Newt is easily kept and bred in captivity. It can be persuaded to live entirely in water all year round. Temperatures of 2-5°C in winter are necessary to bring the animals into breeding condition.

Juveniles live on land but can be returned to the water after one year. Individuals have lived in captivity for 15-20 years (Thorn, 1969; Raffaëlli, 2007).

Comments

Extensive documentation, critical evaluation of data and good photos of animals from different localities are given by Thiesmeier & Schulte (2010). Ambrogio & Gilli (1998) devoted a small monograph to the Italian Alpine Newts. The Alpine Newt is even the main character in a children’s book (Meissner, 1985).

References

Ambrogio & Gilli (1998); AmphibiaWeb (2013); Arano

& Arntzen (1987); Arntzen & Sparreboom (1989); Denoël (1996, 1998, 2003); Denoël & Joly (2001a, 2001b); Denoël et al. (2001a, 2001b); Gasco (1881); Griffiths (1996); Halliday (1977); Herrero et al. (1989); Hoeck & Garner (2007); Joly & Miaud (1989); Martin et al. (1989); Meissner (1985); Raffaëlli (2007); Rocˇek et al. (2003); Sotiropoulos et al. (2001, 2007, 2008a, 2008b); Thiesmeier & Schulte (2010); Thorn (1969); Verrell (1988); Vukov et al. (2011); Wagner et al. (2011).

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Laotriton Dubois & Raffaëlli, 2009 This genus was created to hold a species of newt originally described under the name Paramesotriton laoensis. This large salamander is morphologically distinct from species of the genus Paramesotriton, in which it was originally placed. There are differences in skin colouration, distribution of warts and glands on the skin, and in its having an undifferentiated tongue pad, similar to that of Pachytriton (Stuart & Papenfuss, 2002). It has been confirmed that P. laoensis constitutes a

different lineage (Weisrock et al., 2006; Zhang et al., 2008) and a new monotypic genus Laotriton was coined for this species (Dubois & Raffaëlli, 2009).

Laotriton laoensis (Stuart & Papenfuss, 2002)

References

Dubois & Raffaëlli (2009); Stuart & Papenfuss (2002);

Weisrock et al. (2006); Zhang et al. (2008).

Laotriton laoensis (Stuart & Papenfuss, 2002) | Laos Warty Newt Description

A robust, large-bodied newt. Head equal in width to body, and strongly sloping in profile. Snout short, truncate, rounded in profile, and protruding beyond lower jaw. Tongue small with tongue pad lacking a free posterior margin. Three tubercular dorsal ridges, one midline and two lateral, extending from top of head to base of tail. Dorsal and ventral surfaces largely covered with glands and warts. Paratoids enlarged, projecting backwards. Tail laterally compressed. Dorsal tail-fin and indistinct ventral tail-fin. Tail-tip rounded (Stuart & Papenfuss, 2002). Colour black. Tubercular dorsal ridges and dorsum of paratoid glands tan. Tan spot on dorsum of snout, dorsum of forelimbs at junction with body, and extending somewhat obliquely from posterior corner of eye to near corner of mouth. The iris is

Laotriton laoensis, Ban Le, Phoukhout Dist., Prov. Xiang Khouang, Laos. Photo: Henry Janssen. 218

Salamanders of the Old World | Laotriton

brown. Large, irregular, orange-red spots on underside, orangered on underside of tail-base (Stuart & Papenfuss, 2002). Striped pattern of bluish-white spots on the tail of the male, especially prominent during the breeding season. The female develops a protruding cloaca during the oviposition period (Bachhausen, 2013b). Total length 17-19 cm (Stuart & Papenfuss, 2002). Larger sizes have been reported for captive animals; 19 cm for males, 23 cm for females (Bachhausen, 2008, 2009).

Diagnosis

A large newt with distinct tan dorsal stripes. Dorsal and ventral surfaces covered with glands and warts. Reduced tongue pad. Large, orange-red spots on ventral side.

Laotriton laoensis, Ban Le, Phoukhout Dist., Prov. Xiang Khouang, Laos. Photo: Henry Janssen.

Laotriton laoensis, F1 male, parents from Ban Nyot Phae, Phoukhout Dist., Prov. Xiang Khouang, Laos. Photo: Max Sparreboom, courtesy Paul Bachhausen.

Eggs and larvae

The eggs are attached singly, or mounted singly in rows between leaves that have fallen into the stream and accumulated in leaf packs on the bottom. Within a stream pool, multiple females oviposited on leaves in the same leaf pack. The eggs are sticky, oval, and ca. 2.5×3 mm (3.5×5 mm including the jelly capsule) (Phimmachak et al., 2012). In captive animals, egg laying was recorded from mid-November- end February, at water temperature of 16°C. One female laid 445 eggs (90% fertilised) in one year and 125 and 170 in the two following years. Larvae hatch after five weeks at a size of ca. 14 mm, when kept at a water temperature of 18-19°C. In contrast to the larvae of Paramesotriton spp, those of Laotriton laoensis are entirely black and do not have a yellow patch on the tip of the snout or a white iris. They only develop pink-coloured stripes down the back during metamorphosis (Bachhausen, 2013b). Metamorphosis takes place after ca. 3.5 months at a size of ca. 45 mm. One year old juveniles measure ca. 10 cm (Bachhausen, 2008, 2009). Captive newts reach sexual maturity after 3-4 years (Bachhausen, 2012)

The range of Laotriton laoensis.

Distribution

The geographic range of this species is restricted to a small area in northern Laos, where it has been recorded from Xaysamboun district in Vientiane Province, Pek and Phoukhout districts in Xiangkhouang Province, and Phoukoun district in Louangphabang Province (Phimmachak et al., 2012).

Habitat

Aquatic adults inhabit the pools of small, cold, slightly acidic, flowing streams that traverse a variety of vegetation types, such as evergreen forests, shrubs, grassland, and rice fields, at elevations between 1,160-1,430 m. The streams have a substrate of silt, gravel, rocks, and submerged rock faces.

Laotriton laoensis, habitat, Phoukhout District, Prov. Xiang Khouang, Laos. Photo: Gustavo Espallargas. 219

that described for Paramesotriton hongkongensis and other Paramesotriton species. The male takes up position in front of the female, bends his tail and makes fanning movements with the distal part of his tail in the direction of the female’s snout. The male then turns around and creeps ahead of the female, who follows and regularly touches his undulating tail. The male may deposit 1-5 spermatophores. The female picks up the sperm with her cloaca. After sperm pick-up, the male may bite the female, usually at the tail-base, but also on other parts of her body, and hold onto her for up to 30 minutes, while the female stays more or less calm. Interestingly, and unlike observations on Paramesotriton species, intraspecific aggressive behaviour has not been observed in Laotriton (Bachhausen, 2008, 2009, 2013b).

Threats and conservation

Laotriton laoensis, habitat, Phoukhout District, Prov. Xiang Khouang, Laos. Photo: Gustavo Espallargas.

Stream temperatures range from 13-25°C (Phimmachak et al., 2012).

Behaviour

This species is found in pools within the streams, and is active during the day, at least during November (Stuart & Papenfuss, 2002). Laotriton laoensis is largely aquatic but has also been observed moving overland during and after heavy rain. It eats a wide variety of invertebrates and vertebrates, including large prey (crab appendages, frogs), and females eat the eggs of conspecifics. Mayfly larvae (Ephemeroptera) were the most abundant prey found in the stomachs of L. laoensis. Courtship was observed underwater in the wild in December and January. The male was seen placing his snout on the female’s head, body, cloaca and tail, and fanning her with his tail (Phimmachak et al., 2012). Adults were mostly active at dusk and at night in captivity. Courtship was observed in captivity from September-January at a water temperature of 16°C. Courtship behaviour resembles

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The primary threat to this species is overharvesting for the international pet trade and for medicine and food. In 2008 the species was nationally listed as a Category I species in the Lao Wildlife and Aquatic (Animal) Law, thereby prohibiting all commercial trade in the species. Phimmachak et al. (2012) proposed that this species’ status should be upgraded to Endangered in the IUCN Red List of Threatened Species on the basis of its restricted range and suspected reduction in its population size due to overexploitation (IUCN, 2013). Species distribution models have shown that the amount of suitable habitat for this species in northern Laos is small, emphasising the urgent need for increased protection efforts (Chunco et al., 2013).

Observations in captivity

Some animals were imported into Germany in 2005 by Thomas Schöttler (Bad Schwalbsch, Germany). The species has been bred in captivity up to the second generation. Mating was observed from SeptemberJanuary at 16°C. Eggs were laid at temperatures between 15-18°C. Larvae and juveniles were raised successfully at temperatures between 18-19°C and 20-22°C, respectively. Animals were kept in large aquariums with running water. The water was changed frequently and the tanks were kept spotlessly clean (detailed accounts in Bachhausen, 2008, 2009, 2012, 2013b; Pasmans et al., in press).

Comments

Laotriton laoensis is sister to a clade containing Pachytriton, Cynops and Paramesotriton (Pyron & Wiens, 2011).

References

Bachhausen (2008, 2009, 2012, 2013b); Chunco et al.

(2013); IUCN (2013); Pasmans et al. (in press); Phimmachak et al. (2012); Pyron & Wiens (2011); Stuart & Papenfuss (2002).

Lissotriton Bell, 1839 Following genetic studies showing that the European newt genus Triturus was not monophyletic (Weisrock et al., 2006; Steinfartz et al., 2007), new genus names have been introduced for the taxa formerly included in Triturus. The Alpine Newt was placed in the monotypic genus Ichthyosaura (Schmidtler, 2009; Thiesmeier & Schulte, 2010, discuss the nomenclatural history), the small-bodied newts were placed in Lissotriton and the largebodied newts remained in Triturus. Steinfartz et al. (2007) consider Lissotriton to be the sister taxon of Neurergus + Ommatotriton and Calotriton + Triturus. There is no consensus among researchers regarding the taxonomic status of the different forms contained in Lissotriton vulgaris (Frost, 2013 raises many of them to species status). Despite a high level of mitochondrial DNA divergence, and

evidence of ancient diversification events between some subspecies, the available data do not allow definitive conclusions regarding their taxonomic status. The following species list adopts the more conservative arrangement of Speybroeck et al. (2010), in which regional forms of L. vulgaris are maintained as subspecies.

Lissotriton boscai (Lataste, 1879) Lissotriton helveticus (Razoumowsky, 1789) Lissotriton italicus (Peracca, 1898) Lissotriton montandoni (Boulenger, 1880) Lissotriton vulgaris (Linnaeus, 1758)

References

Frost (2013); Schmidtler (2009); Speybroeck et al. (2010);

Steinfartz et al. (2007); Thiesmeier & Schulte (2010); Weisrock et al. (2006).

Lissotriton boscai (Lataste, 1879) | Bosca’s Newt, Iberian Newt Description

A small-bodied newt. Head longer than wide, snout large, rounded and with a single longitudinal groove on top. Eyes rather small. Labial folds well-developed in the breeding season. Gular fold present. Distinct paratoids. Body slightly quadrangular in cross section in the male, more rounded in the female. Tail low, longer than the rest of the body, compressed and with low dorsal and ventral tail-fins, a little higher in the male. Tail tapering to a pointed tip, sometimes with a short, whitish tail filament. No dorsal crest. Dorso-lateral ridges moderately developed. Extremities rather frail. No toe webbing or skin flaps on the toes. Skin smooth.

a few black spots, often forming a row along each side of the belly. Underside of the tail orange with black spots in the male and without spots in the female (Thorn, 1969). Male cloaca rounded with a longitudinal fold. Female cloaca conical-shaped, directed backwards with a small opening on the top. 7-10 cm total length (Thorn, 1969), females slightly larger than males. For specimens from Portugal: females, from 51.5-92 mm; males, from 50-85 mm (Caetano, 2003). Animals from Doñana are smaller than from Galicia (García-París et al., 2004).

Dorsal colouration yellowish-brown in the male, darker in the female, sometimes olive-brown with more or less distinct dark patches. Underside yellowish-orange to a lively orange-red with

Lissotriton boscai was generally considered to be a morphologically and genetically uniform species (García-París et al., 2004),

Lissotriton boscai, male, Algarve, Portugal. Photo: Sergé Bogaerts.

Lissotriton boscai, female, Algarve, Portugal. Photo: Sergé Bogaerts. 221

but mitochondrial DNA analyses have revealed deep levels of geographical variation. Two principal, genetically divergent, evolutionary lineages have been identified, one consisting of populations from central south-western coastal Portugal and the other comprising all the remaining populations (MartínezSolano et al., 2006). The question of whether these lineages represent distinct species has yet to be determined.

Diagnosis

A small-bodied newt with orange underside, lined with some dark spots on the sides of the belly. Absence of dark stripe through the eye. A single longitudinal groove on the snout. No dorsal crest in the male (Thorn, 1969).

Eggs and larvae

Females attach their eggs singly to leaves and stalks of submersed aquatic plants. Egg-laying may take 2-3 months (Caetano, 2003) and occurs between OctoberNovember and May-June, depending on locality and altitude (Malkmus, 2004). A clutch may consist of 100-250 eggs (Malkmus, 2004). The eggs are oval-shaped and 1.5-2 mm in diameter. The egg is brown above and whitish below. Depending on temperature most larvae hatch after 2-3 weeks, at a size of about 10 mm (Caetano, 2003). A fully developed larva 30 mm long has a well-developed dorsocaudal fin. The tail-tip is pointed and ends in a small filament. Gills are long (Thorn, 1969). The head is longer than wide and the colour of the back varies between yellowish-brown and olive-brown with irregular small black dots. Larvae metamorphose after some three months at a total length of 30-35 mm. In juvenile newts the underside of the tail is often orange and there may be red spots on the back. Some larvae overwinter and metamorphose the following year. Sexual maturity is reached after about three years, longevity varying with latitude. Animals from Galicia may live up to 10 years, while in Doñana females live up to nine years and males up to six years (DíazPaniagua, 2009).

ditches, quarries, lagoons, and deep still waters (Malkmus, 2004; IUCN, 2013).

Behaviour

The adults spend much of the year in the water bodies where they reproduce. At elevations above 1,200 m they spend the winter months on land, where they hibernate (Malkmus, 2004). At lower altitudes they may aestivate on land for a couple of months during summer (Thorn, 1969). The adult diet consists largely of insects and crustaceans (Díaz-Paniagua, 2009). Small larvae eat copepods and ostracods, while older larvae feed on chironomid larvae, nematodes and small molluscs (Caetano, 2003). They may be taken by a wide range of predators, such as snakes and birds, but also Marbled Newts (Triturus marmoratus) (Díaz-Paniagua, 2009). Rising air humidity is a major factor that stimulates the newts to enter the water and start breeding. The males enter the water first and are also the first to leave at the end of the breeding season. Reproductive activity takes place largely during the day (Caetano, 2003). The courtship display of male Lissotriton boscai is generally similar to the suite of behaviours described for other Lissotriton species (Halliday, 1974, 1977; Arntzen &

Distribution

Lissotriton boscai is restricted to the western part of the Iberian Peninsula. It occurs from sea level to elevations approaching 1,870 m, but prefers elevations between 400-1,000 m (IUCN, 2013).

Habitat

Lissotriton boscai inhabits a broad range of terrestrial habitats, including eucalyptus plantations, pine groves, open oak (Quercus) woodland, scrub and sandy coastal areas. It is also found in traditionally farmed areas. At lower altitudes, adult specimens may remain in water from October-May, but some are aquatic all year round. Suitable aquatic habitat includes slow-flowing to moderately rapid streams with gravel or rock bottoms, irrigation channels, and also small stagnant water bodies, such as vegetated shallow ponds, cattle troughs, road

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The range of Lissotriton boscai.

Sparreboom, 1989). The male approaches and sniffs the female. He makes rapid tail movements in the direction of her snout, the most evident being the fanning of his tail. After the female has shown an interest, the male turns around and creeps ahead of the female. The female follows the creeping male and touches his tail-base, prompting the male to depositit a spermatophore on the substrate, right in front of the female’s snout. The female creeps on and picks up the spermatophore with her cloaca while walking over it. But the courtship behaviour of L. boscai differs from that of other species of Lissotriton in several respects. During courtship there is a more direct physical contact between male and female, the snout of the female touching the neck of the male during the tail-fanning display. The fanning bouts last much longer than in other species, except L. italicus, and the male remains more static. During courtship the male performs certain particular displays, such as wiggling movements with the tail-tip, and another movement of the tail termed ‘flamenco’, whereby he raises his tail almost vertically and makes slow worm-like movements with the tail-tip. These behaviours have long been known for L. boscai, but have subsequently been observed in other newt species as well (Krefft, 1937; Giacoma & Sparreboom, 1987; Arntzen & Sparreboom, 1989; Rafinski & Pecio, 1992; Bernardini, 1992; Faria, 1993, 1995). The wiggling movements appear to act as a bait mimic, or lure, to attract a female’s attention. Apart from visual cues, chemical communication plays an important role in the sexual behaviour of newts. The animals use chemical information to find breeding ponds and mates, and to detect the presence of potential rivals. Research has shown that L. boscai males modify their courtship

on the basis of chemical cues, for instance to detect and cope with competing males (Aragón et al., 2000; Aragón, 2009; 2011).

Threats and conservation

This species is mostly threatened by the loss of its breeding waters, caused by drainage for agriculture and urbanisation. Some mortality has been observed as a result of diseases. Introduced predators such as fish, crayfish and mink also threaten Lissotriton boscai. Over much of its range, however, the species is resistant, its populations are stable and its status is generally considered to be of Least Concern (IUCN, 2013).

Observations in captivity

Lissotriton boscai can be kept and bred in captivity. It is possible to persuade the animals to stay in water all year round, which makes it easier to care for them. They should be fed on small living prey and the water should be kept particularly clean and fresh (Thorn, 1969; Eijsden, 1981).

Comments

Excellent chapters on the biology of Lissotriton boscai are found in the Fauna Iberica (García-París et al., 2004) and on the website on the Iberian Vertebrates (Díaz-Paniagua, 2009).

References

Aragón (2009, 2011); Aragón et al. (2000); Arntzen &

Sparreboom (1989); Bernardini (1992); Caetano (2003); Díaz-Paniagua (2009); Eijsden (1981); Faria (1993, 1995); García-París et al. (2004); Giacoma & Sparreboom (1987); Halliday (1974, 1977); IUCN (2013); Krefft (1937); Malkmus (2004); Martínez-Solano et al. (2006); Rafinski & Pecio (1992); Thorn (1969).

Lissotriton boscai, male (left) courting female. Photo: Max Sparreboom. 223

Lissotriton helveticus (Razoumowsky, 1789) | Palmate Newt Description

A small-bodied newt. Head a little longer than wide, snout fairly large and marked with three longitudinal grooves. Labial folds well-developed during the breeding season. Gular fold quite indistinct. Body fairly stout. Tail flattened laterally and a little longer than snout-vent length. Breeding males develop a low, smooth-edged crest along the back and tail. A fin is present on the ventral side of the tail. In the male two dorso-lateral ridges, giving the body a square appearance in cross section. After the breeding season many of these

characters are lost. The female’s body becomes more rounded in cross section and shows an indistinct vertebral ridge; in the breeding season she has low fins on upper- and underside of the tail. In the breeding season, the male’s tail-tip is truncated and ends in a filament 4-7 mm long. Toes of his hind feet are webbed. Skin smooth in the aquatic stage, and dry, finely granulated and velvety during the terrestrial stage. Distinct pores visible on head and paratoid region. Colour brown or olive-brown above, with small dark spots. In females the black spots on the upper side of the body are small and sometimes aggregate into two irregular lines that run down the back. A short, narrow eye-stripe runs along each side of the head. Head of the male is mottled dark brown. In the male, the hind legs, cloaca, foot webbing, and sometimes the caudal crest are blackish. Ventral tail-fin blue-grey in the male, orange in the female. Two longitudinal rows of dark greenish spots on either side of the tail, bordering a pale orange flash. Middle zone of the underside yellow or light orange, lateral sides whitish, throat un-pigmented. Sometimes some black spots on the belly. The female sometimes has a reddish vertebral stripe during the terrestrial stage (Thorn, 1969). Female Lissotriton helveticus are drabber in appearance than the male and lack the crest, conspicuous colour patterns, swollen cloaca and toe webbing (Beebee & Griffiths, 2000). The cloaca of the breeding male is bulbous and rounded and similar to that of L. vulgaris, but the thread-like papillae are less distinct. The female cloaca is less protruding, oval-shaped and with a short cloacal slit (Thorn, 1969).

Lissotriton helveticus, couple, Unterwirbach, Thüringen. Photo: Frank Leo Fokus-Natur, courtesy Andreas Nöllert. 224

Salamanders of the Old World | Lissotriton

Lissotriton helveticus, male in breeding dress. Photo: Franck Paysant.

Geographic variation is limited. Various forms have been described as subspecies on the basis of differences in size and colouration (L. h. alonsoi, L. h. sequeirai and L. h. punctillatus), but more comparative work, including genetic analysis, remains to be done to resolve their relative taxonomic status (Schlüpmann & Van Gelder, 2004). Usually, the male is 50-80 mm, the female 55-95 mm long (Duguet & Melki, 2003).

Diagnosis

A small-bodied newt with underside coloured yellow in the middle, whitish at the sides. At the side of the head a dark longitudinal stripe passing through the eye. Snout marked by three longitudinal grooves. Few or no spots on the belly, and throat always spotless in both sexes (Thorn, 1969). Lissotriton helveticus males have a caudal filament, a smooth-edged caudal crest and hind foot webs, whereas males of the nominate form of L. vulgaris have a denticulate dorsal and caudal crest, narrow skin extensions on hind foot toes and no caudal filament. Head, ventral and tail colour patterns are different, L. vulgaris being overall more colourful and contrasting. Females of the two species are much more similar than males but can be distinguished by the short caudal tail filament in L. helveticus and a pointed tail-tip and marbled throat in L. vulgaris (Secondi et al., 2010).

The immature newts remain on land until ready to breed. This can occur at two years of age in some populations, although females usually reach sexual maturity one year later than males (Beebee & Griffiths, 2000). A mid-altitude population (830 m) of L. helveticus in the Jura Mountains was composed of adults 4-11 years old (Guyétant et al., 1991; Amat et al., 2010).

Distribution

Lissotriton helveticus is a west-European species and ranges from northern Portugal and Spain, where populations are often very fragmented, across most of France to northern Germany (IUCN, 2013). In the Netherlands and Belgium, it is rare and largely confined to soft-water pools (Beebee & Griffiths, 2000).

Habitat

Lissotriton helveticus is usually very common where habitat is suitable. It is present in a variety of habitats including marshes, heath-land, moorlands, forests, pastures, and agricultural land (IUCN, 2013). Like L. vulgaris, it inhabits a wide variety of pond-types preferring fish-free pools and ditches. Across its range it most often occurs at altitudes between 100-500 m, but reaches 1,200 m in the Vosges and Jura, 1,600 in the Massif Central, and ascends to 2,500 m in the Pyrenees (Duguet & Melki, 2003). Over much of its range, L. helveticus occurs in sympatry with L. vulgaris, but hybridisation is rare

Eggs and larvae

Females attach the eggs singly by wrapping a leaf or other object around their cloaca with the hind legs and pressing the egg between it (Norris & Hosie, 2005). A clutch may consist of hundreds of eggs. Clutches of 200-300 have been recorded in England (Beebee & Griffiths, 2000). The eggs are light brown to greenish-grey and are 1.3-1.8 mm in diameter and egg capsules are 2.2-3.0 mm in diameter (Schlüpmann & Van Gelder, 2004). Depending on temperature, most larvae hatch after 2-3 weeks at 6-12 mm in length. On average, Lissotriton helveticus eggs take 1-2 days longer to complete development than those of L. vulgaris, resulting in their hatchlings being marginally larger. In L. helveticus larvae the distance from the nostril to the eye is smaller than the longitudinal diameter of the eye (Thorn, 1969), but in practice, L. helveticus larvae cannot be distinguished from L. vulgaris larvae with certainty (Beebee & Griffiths, 2000). Recently hatched larvae have balancers and are yellow-brown in colour with two conspicuous, black longitudinal stripes along the sides. At a size of 9.5 mm the balancers are absorbed and the colour becomes more cryptic (Thorn, 1969). Larvae metamorphose after 3-3.5 months at a total length of 30-40 mm. Some larvae may overwinter and metamorphose the following year. Partial neoteny occurs regularly and entirely neotenic populations are known, for instance, from the plateau du Lazarc (Aveyron, France; Thorn & Raffaëlli, 2001).

The range of Lissotriton helveticus. 225

(Arntzen et al., 1998; Johanet et al., 2010). In France, the two species exhibit different habitat preferences, L. vulgaris preferring ponds in open habitats, while L. helveticus also breeds in forest ponds (Secondi et al., 2012).

Behaviour

Lissotriton helveticus is ecologically similar to L. vulgaris. It usually overwinters on land and commences activity in December-January, when the adult newts migrate to water to breed. Breeding usually starts in February and extends to JuneJuly, depending on altitude (Duguet & Melki, 2003).

The reproductive biology of L. helveticus is also similar to that of L. vulgaris. The male uses an elaborate courtship display to persuade the female to receive his spermatophore and there are only subtle differences in courtship behaviour between the two species (Halliday, 1975; Wambreuse & Bels, 1984). In both species courtship starts with the male pursuing a female and displaying to her using a combination of tail movements, including fanning and waving as well as the more violent whip in which the male lashes his tail against the side of his body. In L. helveticus, the waves are less conspicuous and the whips less violent than in L. vulgaris. Moreover, L. helveticus males fan their tails about twice as fast as L. vulgaris and the fanning bouts last longer (Halliday, 1975; 1977; Beebee & Griffiths, 2000). Laboratory experiments have shown that female L. helveticus use multiple traits to assess the attractiveness of a male, including both morphological ornaments and courtship behaviours (Cornuau et al., 2012). The tail filament plays a role during the fanning display and females prefer males with longer tail filaments (Haerty et al., 2007). The spermatophore transfer phase is similar to that of L. vulgaris. Lissotriton helveticus from southeast France have been observed performing a curious behaviour after spermatophore transfer. The male sniffs the female’s cloaca and attempts to scratch at it with circular movements of his front legs (Joly, 1995). The function of this behaviour is unknown.

Threats and conservation

There is no particular threat that endangers this species more than other newts. It is locally

threatened by general drainage, pollution and eutrophication of breeding pools, abandonment of traditional farming practices, and the introduction of predatory fish and crayfish (Procambarus clarkii) (García-París et al., 2004). Desertification is a threat in southern parts of its range. However, through most of its range, populations are stable and abundant and the species’ conservation status is considered as of Least Concern (IUCN, 2013).

Observations in captivity

The Palmate Newt can be kept and bred in captivity. After the breeding period, the animals usually leave the water and should be given the option to live on land. Low temperatures in winter are necessary to bring them into breeding condition. Juveniles live on land and only enter the water once they are sexually mature. Individuals have lived in captivity for up to 12, exceptionally 18 years (Thorn, 1969).

Comments

Analysis of large samples has confirmed that hybridisation between Lissotriton helveticus and L. vulgaris is extremely rare (Arntzen et al., 1998). As there is very little ecological isolation between the two species when they occur in the same pond, the subtle differences in behaviour and morphology must be enough to maintain this almost complete reproductive isolation (Beebee & Griffiths, 2000). Laboratory experiments have shown that female L. helveticus can detect the presence of conspecifics from a distance using chemical cues (Secondi et al., 2005). The natural history of L. helveticus is thoroughly reviewed in Die Amphibien und Reptilien Deutschlands (Schlüpmann et al., 1996), the Handbuch der Reptilien und Amphibien Europas (Schlüpmann & Van Gelder, 2004), Fauna Iberica (García-París et al., 2004) and on the website on Iberian vertebrates (Diego-Rasilla, 2011).

References

Amat et al. (2010); Arntzen et al. (1998); Beebee &

Griffiths (2000); Cornuau et al. (2012); Diego-Rasilla (2011); Duguet & Melki (2003); García-París et al. (2004); Guyétant et al. (1991); Haerty et al. (2007); Halliday (1975, 1977); IUCN (2013); Johanet et al. (2010); Joly (1995); Norris & Hosie (2005); Schlüpmann et al. (1996); Schlüpmann & Van Gelder (2004); Secondi et al. (2005, 2010, 2012); Thorn (1969); Thorn & Raffaëlli (2001); Wambreuse & Bels (1984).

Lissotriton helveticus, courting pair, Mayenne, France. The female (left) has just picked up sperm in her cloaca. Photo: Max Sparreboom. 226

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Lissotriton italicus (Peracca, 1898) | Italian Newt Description

A small-bodied newt. Head almost as wide as long. Snout thick, short, obtuse. Eyes slightly prominent. Labial folds well-developed during the breeding season. Gular fold present. Tail low and compressed, about as long as the rest of the body. Tail-tip rounded; in the breeding season the male has a little thorn at the tail-tip. Dorsal and ventral caudal fins low.

Dorsal colouration similar to Lissotriton helveticus, but small black spots always present on the belly and often on the throat. Throat yellow to orange. Spots on the sides of the body have a metallic shine in the breeding season. In the breeding season both sexes have a golden-yellow patch on the temporal region, behind the eyes. This spot is always visible in juvenile Italian Newts (Peracca, 1898; Thorn, 1969). No dorsal crest in the male, but a distinct median dorsal groove in both sexes. The male has dorso-lateral ridges, giving the body a slightly quadrangular shape. No skin flaps on the toes. Male cloaca half-rounded, female cloaca more conical. Males 4.5-6.5 cm, females 5.5-7.5 cm, max. 8 cm (Thorn, 1969). This is the smallest newt species in Europe.

Lissotriton italicus is a fairly morphologically uniform species, but karyological and mitochondrial DNA analyses have revealed strong geographical variation (Lanza et al., 2007; Canestrelli et al., 2012). Two main genetically divergent, evolutionary lineages have been identified, one comprising populations from the Calabrian peninsula and the other containing all the remaining populations.

Diagnosis

A small-bodied newt with yellow to orange underside, the throat darker than the belly. Small dark spots on the belly, few or no spots on the throat. Brown stripes on the head absent. The male does not have a dorsal crest. Both sexes have a golden-yellow patch behind the eyes (Thorn, 1969; Sparreboom, 2003).

Eggs and larvae

Females lay 200-300 eggs, attaching them to leaves with their hind legs. The greyish-yellow eggs are ovalshaped and 1.3-1.8 mm in diameter. Larvae take 3-4 months to reach metamorphosis at a temperature of 20°C. Larvae are ca. 7 mm at hatching and metamorphose at 26-31 mm (Thorn, 1969; Lanza et al., 2007). They are light yellowish-brown to dark brown in colour. In the later larval stages the tail is pigmented

Lissotriton italicus, male, Fasana, Calabria. Photo: Frank Leo Fokus-Natur, courtesy Andreas Nöllert. 227

Habitat

Lissotriton italicus inhabits all sorts of ponds and temporary pools, water tanks and cisterns, quarries, wells and slow-moving streams. In cooler habitats it may be found in water all year round, but normally leads a terrestrial life after the breeding period which, depending on the local climate, may end between April and October (Sparreboom, 2003).

Behaviour Lissotriton italicus larva. Art: Bas Teunis.

as in Ichthyosaura alpestris. Larger larvae may be distinguished from those of Lissotriton vulgaris by the blunt tail-tip and the presence of spots behind the eyes (Lanza, 1983). Overwintering larvae grow larger and paedomorphosis is common. Adults reach sexual maturity in their third year. Maximum age is between 8-11 years (Sparreboom, 2003).

Distribution

Lissotriton italicus is endemic to central and southern Italy. It is most common at altitudes below 800 m, but reaches altitudes round 1,500 m in the Pollino Massif and above Lago Remmo (Sparreboom, 2003).

Adult Lissotriton italicus may remain in the water after the end of the breeding period. In warm regions they aestivate on land, in cold regions they hibernate. The highest densities of newts in the water were recorded from DecemberFebruary. Lissotriton italicus appears to show strong site fidelity (Lanza et al., 2007). The adult diet consists of both aquatic and terrestrial invertebrates. Males, which are often smaller than females, eat mostly chironomid larvae and copepods, whereas females swallow ostracods, cladocerans and terrestrial insects (Lanza et al., 2007). Reproductive activity largely takes place during the day. The courtship display of male L. italicus is generally similar to the suite of behaviours described for other newt species, especially L. boscai (Giacoma & Sparreboom, 1987; Arntzen & Sparreboom, 1989; Rafinski & Pecio, 1992; Bernardini, 1992; Faria, 1993, 1995). The male makes rapid tail movements in the direction of the female’s snout, the most prominent being the fanning of his tail. After the female has shown an interest, the male turns around and creeps ahead of her. The female follows the creeping male and touches his tail-base prompting the male to deposit a spermatophore onto the substrate, right in front of the female’s snout. The female creeps on and picks up the spermatophore with her cloaca while walking over it. In some respects the courtship behaviour of L. italicus differs from that of other Lissotriton species. The static display phase is extended; the frequency of tail beats during the fanning display is higher than in other species; and the time spent fanning is much longer than in the courtship of the other newt species. Apart from tail-fanning, the male may employ other behaviour patterns to attract a female, for example by making wiggling movements with his tail, while the tail is bent or kept upright (Giacoma & Sparreboom, 1987). As in other newt species, rival males will attempt to interfere with on-going courtship encounters and have been observed pushing away courting males and thus sneaking a mating opportunity (Giacoma & Crusco, 1987).

Threats and conservation

The range of Lissotriton italicus. 228

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The species is mostly threatened by drainage of wetlands. Pollution and eutrophication of aquatic habitat, and the introduction of predatory fish may also pose problems. A decline has been observed in many areas in which cases the species appears to be Vulnerable (Scillitani et al., 2004). Its status is on the whole considered to be of Least Concern (IUCN, 2013).

Lissotriton italicus, pair, near Benevento. Photo: Max Sparreboom.

Observations in captivity

Lissotriton italicus can be kept and bred in captivity. Animals can be persuaded to remain in water all year round, making it easier to care for them. They are mainly active in winter at water temperatures slightly above 10°C (Thorn, 1969). To breed them in captivity, it is best to hibernate them for 8-10 weeks at temperatures between 5-10°C (Kühnel & Schwarzer, 1987; Bouwman, 1999).

Comments

A good chapter on the biology of Lissotriton italicus is contained in Lanza et al. (2007).

References

Arntzen & Sparreboom (1989); Bernardini (1992);

Bouwman (1999); Canestrelli et al. (2012); Faria (1993, 1995); Giacoma & Crusco (1987); Giacoma & Sparreboom (1987); IUCN (2013); Kühnel & Schwarzer (1987); Lanza (1983); Lanza et al. (2007); Peracca (1898); Rafinski & Pecio (1992); Scillitani et al. (2004); Sparreboom (2003); Thorn (1969).

Lissotriton montandoni (Boulenger, 1880) | Carpathian Newt Description

A small-bodied newt. Rounded snout; head relatively flat and wide, with three grooves. Eyes fairly big, slightly protruding and laterally placed. Labial folds welldeveloped in the aquatic stage. Gular fold distinct. Body square in cross section in the breeding male, more rounded in the female. Tail flattened, as long as or a little shorter than the rest of the body; tail-tip blunt with a filamentous extension of 3-4 mm in the breeding male. Sometimes a rudimentary tail filament in the female. The breeding male has a low, smooth dorsal ridge and a low, smooth-edged crest on the tail and welldeveloped dorso-lateral ridges. These characteristics disappear after the breeding season. The female is similar to that of Lissotriton vulgaris. She has no dorsal fin, but has poorlydeveloped dorso-lateral ridges and tail-fins. Limbs are welldeveloped, with fingers and toes flat and free. In the terrestrial phase the skin is velvety and finely granulated, especially in the female. In the aquatic stage the skin is smoother. Dorsal parts are coloured olive-brown to greenish with marbled mottling or more or less numerous dark spots. Lower parts

uniformly yellow or orange, rarely with some small black dots, and grading to a paler shade on the throat. Hind legs and cloacal region of the male brown black. Lower edge of the tail of the male orange, with a whitish or bluish flash. Lower edge of the tail of the female orange and lined with a row of black spots on either side (Thorn, 1969). In the terrestrial phase the colours become darker, sometimes reddish (Necˇas et al., 1997). In the breeding male the cloacal region is bulbous, similar to that of L. helveticus. Usually, the male is 7-8 cm, the female 7.5-10 cm long (Thorn, 1969). The species is morphologically uniform over its entire range. No subspecies are recognised.

Diagnosis

A small-bodied newt resembling Lissotriton vulgaris and L. helveticus, but distinct from these species in having three longitudinal grooves on the snout. Instead of a 229

Lissotriton montandoni, male, Carpathian Mts, Romania. Photo: Benny Trapp.

Lissotriton montandoni, female, Carpathian Mts, Romania. Photo: Benny Trapp.

denticulated dorsal crest, the breeding male has a low, smoothedged ridge, a blackish cloaca, feet with almost no webbing, and a tail filament. Lissotriton montandoni is uniform yellow or orange on the ventral side. Very few black spots on the sides (Thorn, 1969). Lissotriton montandoni and L. vulgaris are two genetically related species which produce fertile hybrids where their ranges meet. Lissotriton montandoni lives in sympatry with L. vulgaris in many aquatic habitats over its entire range, especially along small rivers in the mountains or in the hilly areas of the Subcarpathians. Hybrids show characteristics of both parent species (Mikulicek & Zavadil, 2008; Gherghel et al., 2012).

Eggs and larvae

Females attach their eggs, singly or in groups of 2-5, to leaves or other objects, or on the bottom of the water body. A clutch may consist of between 35-460 eggs (Zavadil et al., 2003). The eggs are brownish above, ochre-white below and 1.6-1.8 mm

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in diameter. The egg capsule is 2.2-2.8 to 2.8-4 mm in diameter. Most larvae hatch after an average of 15 days depending on temperature and measure 5-7 mm. The larvae are similar to those of Lissotriton vulgaris and L. helveticus but have been described as smaller and more robust than those of L. vulgaris and Ichthyosaura alpestris. When fully developed, the larvae have a dorsal tail-fin starting in the neck region and a ventral tail-fin. The dorsal fin is lower than in L. vulgaris. The head is blunt and rounded with a wide gape and the tail-fin has a pointed, often filamentous tip. Metamorphosis takes place after 2-3 months at 20-45 mm in lenght. Juveniles often have a bright vertebral stripe that remains until sexual maturity (Zavadil et al., 2003). Some larvae overwinter and metamorphose the following year. It is unknown at what age the animals reach sexual maturity.

Distribution

Lissotriton montandoni is endemic to the east Carpathian and easternmost Sudetes Mountains (Czech Republic, Poland, Romania, Slovakia and Ukraine). It has been introduced into the Bavarian Forest, Germany (IUCN, 2013).

The range of Lissotriton montandoni.

Habitat

Lissotriton montandoni inhabits wet and shaded coniferous, mixed and deciduous forests, their edges, and meadow glades, as well as sub-alpine areas. It is generally regarded as a montane species, but it occurs at altitudes between 120-2,000 m. Reproduction and larval development take place in almost any temporary or permanent water body in the Carpathians, including lakes, ponds, swamps, springs, puddles, ditches, overgrown stream pools, and even wheel ruts in country roads (IUCN, 2013). Populations attain maximum densities at elevations of 500-750 m, locally as high as 18-20 specimens per 1 m 2 (Kuzmin, 1999).

Behaviour

Lissotriton montandoni usually overwinters on land, and rarely in water. Male and female newts leave their terrestrial winter refuges in spring and congregate in ponds in order to breed. This may start as early as March in lower areas but in higher regions the aquatic phase shifts to the summer. Males arrive some two weeks before the females and may already be active at temperatures just above 1°C. The activity period can be relatively long, lasting until October (Necˇas et al., 1997; Zavadil et al., 2003).

Lissotriton montandoni, habitat, Bistra, Mures County, Romania. Photo: Tibor Sos. In the aquatic stage the diet consists of a variety of small invertebrates, especially crustaceans, and amphibian eggs and larvae. During the terrestrial stage L. montandoni feeds on ants, beetles, annelids, molluscs, etc. (Necˇas et al., 1997; Kuzmin, 1999). During the terrestrial stage the animals are active mainly at night. In the aquatic phase they are active both day and night. Courtship and mating take place during the day, and feeding mostly at night (Zavadil et al., 2003). These newts and their larvae are taken by a wide range of predators, such as fish, snakes and birds, but also by beetles, and the larvae of Crested Newts (Triturus cristatus) and Fire Salamanders (Salamandra salamandra) (Kuzmin, 1999; Zavadil et al., 2003). In its general pattern, the sexual behaviour of L. montandoni most resembles that of L. helveticus. The male courtship repertoire consists of three phases: orientation, static display and retreat 231

structure development, introduction of predatory fish, and pollution of habitats by domestic sewage. Collection of newts for education, science and the pet trade has negatively impacted some populations. Lissotriton montandoni is further affected by hybridisation with L. vulgaris, whose range is generally encroaching onto that of L. montandoni as a result of ongoing deforestation. It is listed on appendix II of the Bern Convention and is protected by national legislations. Its status is on the whole considered to be of Least Concern (IUCN, 2013).

Observations in captivity

Lissotriton montandoni, female laying eggs, Maramures Mts, Romania. Photo: Dan Cogalniceanu.

display, followed by the spermatophore transfer phase. During courtship display the male performs three tail movements: fanning; the whip – a forceful lash with the tail ; and the wave – where the male takes a side-on position in front of the female and shows her the side of his body and tail. The main differences between the display of L. montandoni, L. helveticus and L. vulgaris consist in the relative frequencies of these tail movements and the duration of fanning bouts (Pecio & Rafinski, 1985; Arntzen & Sparreboom, 1989).

Threats and conservation

Some populations have declined due to habitat destruction, such as logging and infra-

The Carpathian Newt can be kept and bred in captivity, but is more sensitive to its environment and fussier in its diet than L. vulgaris. It prefers small crustaceans, insects and spiders over earthworms (Thorn, 1969). After the breeding period, the animals always leave the water and should be allowed to live on land. Temperatures of 3-6°C for 2-3 months in winter are necessary to bring the animals into breeding condition. The aquatic stage can be prolonged to 4-5 months if the water temperature is kept low, preferably around 15°C (Obst, 1975).

Comments

The natural history of Lissotriton montandoni is the subject of a thorough review in the Handbuch der Reptilien und Amphibien Europas (Zavadil et al., 2003). The relationship between L. montandoni and its sister species L.vulgaris is complicated. Morphologically the species are clearly distinct but genetically they are hard to distinguish (Babik et al., 2005; Nadachowska & Babik, 2009; Nadachowska-Brzyska et al., 2012). Extensive range-wide sampling has shown that the mitochondrial, but not the nuclear, DNA of L. montandoni has been totally replaced by the mitochondrial DNA of L. vulgaris. This introgression has probably occurred via multiple, spatially and temporally separated episodes of hybridisation (Zielinski et al., 2013). Natural hybridisation is of interest as it represents a unique source of information about the mechanisms of reproductive isolation, which can lead to speciation. The courtship behaviour of L. montandoni is more similar to that of L. helveticus than is that of L. vulgaris. Even so, hybridisation between L. helveticus and L. vulgaris, species that are sympatric over much of their range, is rare, whereas hybridisation between L. vulgaris and L. montandoni is common. This indicates that in spite of the morphological and behavioural differences between these two species, these differences are not sufficient to effectively isolate them (Pecio & Rafinski, 1985; Osikowski, 2012).

References Lissotriton montandoni, courtship, Bistra, Mures County, Romania. The male (left) holds his tail folded against his body, braking the forward movement of the female. The spermatophore is situated under the female’s body. Photo: Tibor Sos. 232

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Arntzen & Sparreboom (1989); Babik et al. (2005);

Gherghel et al. (2012); Kuzmin (1999); Mikulicek & Zavadil (2008); Nadachowska & Babik (2009); Nadachowska-Brzyska et al. (2012); Necˇas et al. (1997); Obst (1975); Osikowski (2012); Pecio & Rafinski (1985); Thorn (1969); Zavadil et al. (2003); Zielinski et al. (2013).

Lissotriton vulgaris (Linnaeus, 1758) | Smooth Newt Description

A small-bodied newt. Head longer than wide, snout elongated, truncated in the male and rounded in the female, with three longitudinal grooves. Eyes slightly protruding. Labial folds well-developed during the breeding season. Gular fold absent or only slightly evident. Slender body with rounded trunk. Tail flattened laterally and a little longer than snout-vent length. The adult male in nuptial dress shows a high denticulated crest, extending without interruption from the the back of the head onto the tail. A fin is present on the ventral side of the tail. After the breeding season the crest is reduced to an indistinct skin fold and the tail-fins disappear entirely. Tail-tip pointed, in some forms ending in a short filament. Toes of the hind feet are lined with a skin fold in breeding males. The cloaca of the breeding male is swollen and rounded, always with black pigmentation. The cloacal slit is elongated with thread-like papillae on the hind part (Thorn, 1969).

Female Lissotriton vulgaris are much drabber in appearance and lack the crest, conspicuous colour patterns, swollen cloaca and toe-flaps of males (Beebee & Griffiths, 2000). The female shows an indistinct vertebral ridge; in the breeding season she has rather low, straight fins on upper- and underside of the tail. In both sexes the skin is smooth in the aquatic stage, and dry, finely granulated, and velvety during the terrestrial stage. Distinct pores visible on head and paratoid region.

Lissotriton vulgaris vulgaris, couple, male above, the Netherlands. Photo: Jelger Herder.

Colour brown or olive-brown above, often yellow-brown in the female. Fairly large rounded brown spots in the male. In females the black spots on the upper side of the body are

small and sometimes aggregated into two or more irregular lines that run down the back. Five to seven dark longitudinal stripes on the head, especially conspicuous in the male. The crest of the male often shows bright and dark vertical bands. Ventral side orange, whitish at the sides, speckled with small,

Lissotriton v. vulgaris, male, The Hague, Netherlands. Photo: Max Sparreboom.

Lissotriton v. vulgaris, female, The Hague, Netherlands. Photo: Max Sparreboom. 233

dark, round dots. Ventral side of the female is lighter with smaller dark dots. In the male, the lower edge of the tail is tinged red, with triangular black spots, and a silver-blue flash during the breeding season. After the aquatic stage the nuptial dress fades, the dark, round spots become smaller, and the male becomes similar to the female, although the spots on the male always remain larger than those on the females. Usually, the male is 9-11 cm, the female 8-9.5 cm long (Thorn, 1969). The degree of variation in the secondary sexual characters of the regional forms is greater than that found in other newts. This has resulted in the description of many subspecies, mainly based on external morphological features of the males in breeding condition, including crest, tail-tip, toe-flaps, body cross section, dorso-lateral folds, and pigmentation. The validity of these subspecies is disputed. According to recent reviews (Raxworthy, 1990; Schmidtler & Franzen, 2004; Ivanovic et al., 2011; Grosse, 2011) at least eight subspecies are considered to be valid. Lissotriton vulgaris ampelensis (Fuhn, 1951) The dorsal crest is of medium height (>1.0 mm at mid-body) and weakly denticulated with rounded serrations. The tail gradually tapers to a fine thread (but there is no tail filament). There are no dorso-lateral folds. The body cross section is slightly square dorsally. The toe-flaps are large and well-developed (Raxworthy, 1990). This subspecies occurs in the Ukrainian Carpathians and the Danube delta in northern Romania (Kuzmin, 1999).

Lissotriton vulgaris graecus, male, Olympos Mt, Greece. Photo: Benny Trapp.

Lissotriton vulgaris graecus, female, Olympos Mt, Greece. Photo: Benny Trapp.

Lissotriton vulgaris graecus (Wolterstorff, 1905) The dorsal crest is low (1.0 mm at mid-body) and deeply notched with rounded denticulations. There is no tail filament, the tail usually tapering to a blunt end. There are no dorso-lateral folds. The body cross section is rounded. The toe-flaps are moderately or poorly developed (Raxworthy, 1990). The nominate subspecies is distributed in much of northwest, central and eastern Europe, and the western part of Asia Minor (Schmidtler & Franzen, 2004). Other subspecies have been described from Croatia and BosniaHerzegovina (L. v. dalmaticus), from southern Bosnia-Herzegovina, south-western and southern Montenegro (L. v. tomasini), and from the area round Drnis and Sinj (T. v. intermedia). These are difficult to characterise and their taxonomic status remains unsettled (Schmidtler & Franzen, 2004; Grosse, 2011).

Diagnosis

A small-bodied newt with orange underside, lined with white, and dark spots on body and tail in the male.

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Development of the Smooth Newt (Lissotriton vulgaris) from egg to adult. Watercolour executed by J. Hans (photo and collection: Bibliothèque nationale et universitaire de Strasbourg, ms. 441). Signed on the left: observed and painted by Rösel of Nuremberg, and on the right: copied by Hans under the supervision of J. Hermann. The original by Rösel is missing. See comments by M. Niekisch (2009) in his Introduction to the Reprint of August Johann Rösel von Rosenhof, Historia naturalis ranarum nostratium / Die natürliche Historie der Frösche hiesigen Landes. Nuremberg, 1758. Courtesy Bibliothèque Nationale et Universitaire de Strasbourg.

The female has smaller dark spots and a higher density of small, dark spots on the throat, although these can be sparse or even absent in some females. Sides of the head with brown longitudinal stripes. The male of the nominate form has a high, wavy, denticulated crest along the back. In the southern forms, breeding males develop a number of anatomical features that resemble those shown by males of Lissotriton helveticus, rather than those of the nominate subspecies L. v. vulgaris. These include a low, smooth-edged crest, a distal tail filament, and prominent dorso-lateral ridges.

Eggs and larvae

Females attach their eggs singly by wrapping a leaf or other object around the cloaca using the hind legs and pressing the egg into it. A clutch may consist of hundreds of eggs. In England, clutches of 100-500 eggs have been recorded (Schmidtler & Franzen, 2004). Clutch size is highly variable and correlated with the size of the female. The eggs are light brown to greenish-grey and are 1.3-1.7 mm in diameter. The egg capsule is 2.7-3.5 mm in diameter and reaches a size of 4 mm during the course of embryonic development (Schmidtler & Franzen, 2004).

The gills are red. Larvae metamorphose after some three months at a total length of 30-40 mm. Some larvae may overwinter and metamorphose the following year. Partial neoteny occurs regularly. Growth is dependent on latitude and altitude. In the northern and eastern parts of its range growth is slower than in more south-westerly areas. Sexual maturity is reached after 2-3 years, sometimes later. Lissotriton vulgaris may reach an age of 6-14 years in the wild (Schmidtler & Franzen, 2004).

Distribution

Lissotriton vulgaris is the most ubiquitous and widely-distributed newt of the Old World. It occurs across north-west, central and eastern Europe including central and southern Scandinavia and western Asia around the Black Sea, with an outpost on the Caspian Sea. It is absent from the Iberian Peninsula and south-west France. Its range extends deep into Siberia in the east. In the south-eastern parts of its range the

Depending on temperature, most larvae hatch after 10-20 days at a length of 6.5-7 mm (Beebee & Griffiths, 2000; Schmidtler & Franzen, 2004). Recently hatched larvae have balancers and are coloured yellow-brown with two conspicuous, black, longitudinal stripes along the sides. At 9.5 mm length the balancers are absorbed and the colour becomes more cryptic. Fully developed larvae have a dorsal tail-fin starting in the neck region and a ventral tail-fin. The head is blunt and rounded with a wide gape; the tail-fin has a pointed but non-filamentous tip (Schmidtler & Franzen, 2004; Thorn, 1969). The colour varies from yellowishto greenish-brown with small brown speckles and small goldcoloured dots along the sides. Underside whitish to golden.

The range of Lissotriton vulgaris.

Lissotriton vulgaris graecus, habitat, Olympos Mt, Greece. Photo: Benny Trapp.

Lissotriton vulgaris schmidtlerorum, habitat, South of Izmir, Turkey. Photo: Max Sparreboom. 237

distribution is fragmented (Schmidtler & Franzen, 2004; Grosse, 2011).

Habitat

Lissotriton vulgaris is a common and ecologically highly flexible species, both in terms of breeding site and terrestrial habitat characteristics. It inhabits a wide variety of water bodies with stagnant or semi-flowing water: ponds, shallow temporary puddles, larger water reservoirs, and quiet parts of streams. It also colonises garden ponds and parks within cities. In the terrestrial phase this newt lives a secretive life, mostly underground, in the burrows of small mammals,

move to the front

sniff

whip wave

ORIENTATION

follow

STATIC DISPLAY fan

fan RETREAT DISPLAY

retreat & whip

creep & follow quiver SPERMATOPHORE TRANSFER PHASE

touch tail deposition

creep on

brake & touch tail wiggle tail bent

push back

Diagram of courtship behaviour sequence in the Smooth Newt (Lissotriton vulgaris). Female is shaded, male is non-shaded. Art: Bas Teunis, redrawn from Arntzen & Sparreboom (1989), based on Halliday (1974). 238

Salamanders of the Old World | Lissotriton

and under logs and stones, and can often be found in gardens. The nominate subspecies L. v. vulgaris is generally considered a lowland species, although it does occur at altitudes above 1,000 m, for instance in central Europe. The southern subspecies also occurs at higher altitude (Beebee & Griffiths, 2000; Schmidtler & Franzen, 2004). Lissotriton vulgaris cannot survive in completely barren habitats that are totally devoid of water and hiding places, such as in dry steppe regions.

Behaviour

Lissotriton vulgaris usually overwinters on land, under logs, in burrows, and in rotten trees, often in groups. Male and female newts leave their terrestrial winter refuges in spring and congregate in ponds to breed. They are ready to mate soon after they enter the water. Mating may commence in midFebruary, although in higher and more northerly regions the aquatic phase shifts to the summer. In some areas the newts enter water in the autumn (Kuzmin, 1999). The hibernation period is longer in the northern and north-eastern parts of the species’ range, while in the southern parts of its range hibernation may be skipped entirely. During the terrestrial stage, the animals are active mainly at night. In the aquatic phase they show a crepuscular daily rhythm with activity peaks around dawn and dusk and higher levels of activity at night than during the day. Lissotriton vulgaris is a relatively unselective feeder, preying on a wide range of invertebrates. The food spectrum on land includes Lumbricidae, Gastropoda, Acarina, Aranei, Collembola, Coleoptera, Lepidoptera and Diptera. In the aquatic phase adults prey on invertebrates of the same size as large-sized larvae: aquatic molluscs (Bivalvia, Gastropoda) and insects (larval Ephemenoptera and Chironomidae, larval and imago Coleoptera). Cannibalism occurs, mainly in the form of oophagy (AmphibiaWeb, 2013). These newts are taken by a wide range of predators, such as snakes and birds, but also frogs and Crested Newts (Triturus cristatus) (Kuzmin, 1999). The presence of fish in a breeding pond may pose a danger, but does not always exclude the successful breeding of L. vulgaris (Schmidtler & Franzen, 2004). The reproductive biology of L. vulgaris, especially of the nominate subspecies L. v. vulgaris, has been extensively studied, both in the laboratory (Halliday, 1974, 1977, 1990) and, to a lesser extent, in the field (Verrell & McCabe, 1988). The male uses an elaborate courtship display to persuade the female to receive his spermatophore. The description by Tim Halliday has served as a model for the study of many other newt species (Arntzen & Sparreboom, 1989). The following account of the courtship display is based upon the studies carried out by Halliday and co-workers (as summarised by Beebee & Griffiths, 2000).

‘Smooth Newts develop their full set of breeding characters only after entering the water and it may take several weeks for the male crest to reach its full height.’(...) ‘Courtship starts with the male newt making initial overtures towards a prospective 1

mate. In this orientation phase the male tries to attract the attention of a female by following her, sniffing her cloaca and swimming in front of her to block her way. In some cases the female simply swims off and the courtship sequence ends 2

4 3

6 5

8 7

9

11

10

Lissotriton vulgaris courtship sequence. Photos: Max Sparreboom. 1. Male tail-fanning. 2. Building up a tail-lash (whip). 3. Whip. 4. Showing off the side of his body (wave). 5. Creeping ahead of the female. 6. Female orients to the male’s tail, creeping behind him. 7. Female follows the creeping male. 8. Female touches tail-base of the male; male deposits spermatophore. 9. Male turns side-on while female moves over the spermatophore. 10. Female picks up sperm cap from spermatophore. 11. After sperm pick-up the male turns around and nudges female’s cloaca. 239

there. If she is interested in her suitor, however, she remains in one place and turns to face him. Having secured her attention, the male then starts a long and frenetic courtship display. He first faces the female and vibrates the tail rapidly against his own body. This fanning wafts secretions from his cloaca towards the female, thereby stimulating her further. Episodes of fanning can go on for half a minute or more, but may be interspersed by two other display behaviours. The wave involves the male presenting a full side-on view of his body and tail to the female, showing off his breeding characters to best effect. The whip is a more violent movement in which his tail is lashed powerfully against his own flank, often causing a current of water that drives the female backwards. The three behaviours used in the display are initially conducted while the male is stationary, but if the female continues to show interest he starts to move backwards, continuing his display as he goes, but with fewer fans and more whips and waves. This leads into the final phase of courtship where the relationship is consummated by the transfer of a packet of sperm called the spermatophore. The male turns away from the female and leads her on by creeping in front of her, quivering his tail to maintain attention. If still interested she follows and touches his tail with her snout. In response to this signal he lifts and folds his tail, and deposits a spermatophore on the substrate. He must now delicately manipulate his partner over the spermatophore so that it is absorbed into her cloaca. After moving forward by about half a body length he turns to one side so that he is now at right angles to his mate, thereby blocking her progress. The female presses forward and touches the male’s tail which is now turned against his own flank. This contact stimulates the male to unbend his tail, thereby pushing the female back slightly so that her hindquarters rub against the spermatophore. By this time the female’s cloaca has opened and extended and if the male has orchestrated his display accurately the top of the spermatophore will adhere to the cloaca and be absorbed into the female’s body so that the sperm can fertilize her eggs. At any time during this sequence the female may lose interest and swim away. In fact the whole repertoire is often repeated several times in one encounter, with a new spermatophore being deposited on each occasion.’ (...) ‘Males often outnumber females and competition for females is intense. Smooth Newts do not display any direct aggression towards each other and are not territorial, and males wander widely within a pond in search of prospective mates. However, male Smooth Newts have adopted a sneaky strategy to obtain successful matings at the expense of their competitors. This is achieved by interfering with another male’s courtship during a crucial phase. Having allowed the first male to carry out initial displays and arouse the female, a sneaky male will move in at the spermatophore transfer stage and touch the tail of his rival. This stimulates the leading male to deposit a spermatophore as if his tail was touched by the female. The sneaky male then leads away the receptive female and completes the court-

ship sequence by depositing his own spermatophore which she then picks up (Verrell, 1984).’ Interestingly, sexual interference has also been observed in females, in situations where receptive females outnumbered males and had to compete for them (Waights, 1996). Female Smooth Newts have a preference for males with large crests (Green, 1991).

Threats and conservation

There is no specific threat that endangers this newt more than other newt species. In some regions populations are declining or have gone extinct due to anthropogenic causes. Populations appear to be especially vulnerable at the margins of their range. Some forms (L. v. schreiberi) have a very small distributional range and are affected by loss of breeding habitat (Schmidtler & Franzen, 2004). Lissotriton v. lantzi is considered threatened in Georgia and Azerbaijan and its status is indeterminate in Russia (Kuzmin, 1999). Given the vast distribution of the nominate form, and its high abundance in many places, its status is on the whole considered to be of Least Concern (IUCN, 2013).

Observations in captivity

The Smooth Newt can be kept and bred in captivity. After the breeding period, the animals always leave the water and should be allowed to live on land. Temperatures of 2-5°C in winter are necessary to bring the animals into breeding condition. Juveniles live on land and only enter the water once they are sexually mature. Individuals have lived in captivity for 4-8 years, and exceptionally for 18-20 years (Thorn, 1969).

Comments

The natural history of Lissotriton vulgaris is the subject of a thorough review in the Handbuch der Reptilien und Amphibien Europas (Schmidtler & Franzen, 2004). An informative monograph on this species has been written by Grosse (2011) and good pictures are published in Nöllert et al. (2010). The evolution of the male dorsal crest, such a typical feature in the various forms of L. vulgaris, is addressed by Wiens et al. (2011).

Lissotriton v. vulgaris lives in sympatry with L. helveticus over a vast area. Hybridisation, however, is rare (see under L. helveticus). Lissotriton montandoni occurs together with L. vulgaris over much of L. montandoni’s range and here hybridisation is common (see under L. montandoni).

References

AmphibiaWeb (2013); Arntzen & Sparreboom (1989);

Babik et al. (2005); Beebee & Griffiths (2000); Green (1991); Grosse (2011) ; Halliday (1974, 1977, 1990); IUCN (2013); Ivanovic et al. (2011); Kuzmin (1999); Lanza et al. (2007); Nadachowska & Babik (2009); NadachowskaBrzyska et al. (2012); Nöllert et al. (2010); Olgun et al. (1999); Raxworthy (1988, 1990); Schmidtler & Franzen (2004); Sparreboom & Arntzen (1987); Tarkhnishvili & Gokhelashvili (1999); Thorn (1969); Trapp (2007); Valakos et al. (2008) ; Verrell (1984); Verrell & McCabe (1988); Waights (1996); Wiens et al. (2011).

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Salamanders of the Old World | Lissotriton

Lyciasalamandra Veith & Steinfartz, 2004 Lycian salamanders of the genus Lyciasalamandra are slender, terrestrial, viviparous salamanders, with most species less than 14 cm in total length. Lyciasalamandra can be distinguished from Salamandra and Chioglossa by an additional phalange at the first toe/finger of the fore- and hindlimbs. The genus can be distinguished from Chioglossa by its normal lungs, which are reduced in Chioglossa, and by the absence of a tongue projection mechanism such as is present in Chioglossa. It differs from Salamandra in skull characteristics (Özeti, 1967). Furthermore, unlike Chioglossa and most species of Salamandra, males of Lyciasalamandra have keratinized epidermal projections covering the back. The tail is much shorter than in Mertensiella (80-90% of snout-vent length, cf. 120-200% in Mertensiella caucasica) (Franzen & Steinfartz, 1999; Veith & Steinfartz, 2004). The male has a dorsal tail tubercle similar to that of Mertensiella (Sever et al., 1997). Insemination of the female is preceded by a ventral amplexus similar to that of Pleurodeles, Salamandra, Chioglossa and Mertensiella (Thorn, 1969). The tubercle plays a role during courtship and mating and is a unique feature in salamanders. It has long been regarded as a synapomorphic trait of Mertensiella caucasica and the species then known under the name of Mertensiella luschani, hence the previous inclusion of both taxa in a single genus Mertensiella. However, mitochondrial and nuclear DNA sequence data have shown that M. luschani is the sister taxon to Salamandra and that Mertensiella is sister to Chioglossa (Veith & Steinfartz, 2004; Pyron & Wiens,

The range of the genus Lyciasalamandra in Turkey and Greece.

2011), a conclusion long anticipated by Özeti (1967). The dorsal tail tubercle must have either evolved twice independently as a result of convergent evolution, or have been present in the ancestor of the four genera and subsequently lost in Chioglossa and Salamandra. The genus Lyciasalamandra consists of nine genetically and morphologically distinct taxa – seven species, one of them comprising three subspecies – distributed allopatrically along the southwestern coast of Turkey and several of the Aegean islands. These lineages diverged nearly simultaneously in the Late Miocene, ca. 6-8 million years ago, when extensive uplifting of Anatolia occurred in response to the Arabian collision (Weisrock et al., 2001). Lyciasalamandra species are restricted to karstic limestone areas. Most localities are below 500 m, with a maximum altitude of 1,340 m. The typical habitat is pine forest on northerly exposed slopes (Veith et al., 2001). Several other forms of Lyciasalamandra have recently been described as new species under the names L. arikani, irfani and jehudahi (Göçmen et al., 2011; Göçmen & Akman, 2012; cf. Frost, 2013). More data, especially molecular data, are needed before salamanders from these populations can be convincingly distinguished from neighbouring forms and recognised as separate species.

The range of western Lyciasalamandra species.

The range of eastern Lyciasalamandra species.

241

Lyciasalamandra antalyana (Basoglu & Baran, 1976) Lyciasalamandra atifi (Basoglu, 1967) Lyciasalamandra billae (Franzen & Klewen, 1987) Lyciasalamandra fazilae (Basoglu & Atatür, 1974) Lyciasalamandra flavimembris (Mutz & Steinfartz, 1995) Lyciasalamandra helverseni (Pieper, 1963) Lyciasalamandra luschani (Steindachner, 1891)

References

Franzen & Steinfartz (1999); Frost (2013); Göçmen et al.

(2011); Göçmen & Akman (2012); Özeti (1967); Pyron & Wiens (2011); Sever et al. (1997); Steinfartz & Mutz (1999); Thorn (1969); Veith et al. (2001); Veith & Steinfartz (2004); Weisrock et al. (2001).

Lyciasalamandra antalyana (Basoglu & Baran, 1976) | Antalya Salamander Description

A slender salamander with delicate limbs. Generally similar in appearance to Lyciasalamandra luschani. Dorsal tail tubercle in males is relatively small (Steinfartz & Mutz, 1999).

Parturition

Colour varies greatly among individuals. Ground colouration yellow with dark spots, or dark with yellow spots. Dark ground colour generally predominates. Contrasting dark yellow colour pattern on head is striking. Paratoids and upperside of eyeballs are always bright yellow. Lateral stripe yellowish with undefined edges. Ventral side uniformly yellow (Steinfartz & Mutz, 1999).

Distribution

Total maximum length 13.4 cm (Franzen et al., 2008).

Diagnosis

A slender, terrestrial salamander with delicate limbs and large protruding eyes. Colour pattern highly variable. Can be distinguished from other Lyciasalamandra species by clearly contrasting yellow colouration on paratoids and eyes. Tail tubercle in male relatively small.

Lyciasalamandra antalyana, Hurma. Photo: Frank Pasmans. 242

Salamanders of the Old World | Lyciasalamandra

Like the other Lyciasalamandra species, this species is viviparous. A female usually gives birth to two fully metamorphosed young, 47-71 mm in length (Steinfartz & Mutz, 1999) (see Lyciasalamandra luschani). This species occurs in the eastern Taurus range, from southwest of Antalya northwards. Its known range has been extended further north to localities in Burdur Province, up to 750 m altitude (Akman et al., 2013), since the distribution previously described by Franzen et al. (2008). Some hybrids have been found in a narrow contact zone with L. billae (Johannesen et al., 2006).

Habitat

All Lyciasalamandra species typically inhabit pine forest and maquis shrublands on slopes with a northern exposure. Lyciasalamandra antalyana occurs at altitudes from 120-750 m (Franzen et al., 2008; Akman et al., 2013). Its habitat requirements are similar to L. luschani.

Lyciasalamandra antalyana, inland form, Thermessos. Photo: Frank Pasmans.

Behaviour

This species activity pattern and behaviour is similar to that described for L. luschani (Steinfartz & Mutz, 1999; Franzen et al., 2008).

Threats and conservation

Eight adjacent populations are known and the species can be abundant within this restricted range. Given its small range it is considered Endangered (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

Lyciasalamandra species have been kept in captivity. Its reproductive behaviour and develop-

ment of the juveniles have been described largely on the basis of detailed observations of captive animals (Steinfartz & Mutz, 1999). This species is easy to keep (see under L. luschani), but breeding in captivity is rare (Steinfartz & Mutz, 1999; Raffaëlli, 2007).

Comments

The life history of all Lyciasalamandra species is

similar.

References

Akman et al. (2013); Franzen et al. (2008); IUCN (2013);

Johannesen et al. (2006); Raffaëlli (2007); Steinfartz & Mutz (1999); Stuart et al. (2008).

Lyciasalamandra atifi (Basoglu, 1967) | Atif’s Salamander Description

A slender salamander with delicate limbs. Generally similar in appearance to Lyciasalamandra luschani. Dorsal tail tubercle relatively small (Steinfartz & Mutz, 1999). Colour varies greatly among individuals. Ground colour of dorsal side dark brown with numerous small, silvery-white speckles. Unspotted individuals are also found. Dense white spotting on sides, fusing into larger patches. Limbs and tail orange to reddish-brown with darker shades and partly silverywhite spots. Ventral side uniformly yellow-orange (Steinfartz & Mutz, 1999). Total maximum length 18.1 cm (Franzen et al., 2008).

Diagnosis

A slender, terrestrial salamander with delicate

limbs and large protruding eyes. Dark ground colour. Largest Lyciasalamandra species. Can be distinguished from other Lyciasalamandra species by irregular silvery-white colouration of the flanks (Franzen et al., 2008).

Parturition

This species is viviparous like the other Lyciasalamandra species. A female usually gives birth to two fully metamorphosed young (Steinfartz & Mutz, 1999) (see Lyciasalamandra luschani). A female of 150 mm total length was observed giving birth to two young of ca. 78 mm length in November. Their colour was similar to that of the female (Göçmen et al., 2013a).

Distribution

Southern Taurus range, from Selge (ca. 60 km north-east of Antalya) in the west to the area north of Alanya in

Lyciasalamandra atifi, male, Selge. Photo: Frank Pasmans.

243

the east, a west-east distance of around 110 km (Franzen et al., 2008).

Habitat

All Lyciasalamandra species typically inhabit pine forest and maquis shrublands on slopes with a northern exposure. Lyciasalamandra atifi occurs at altitudes from 190-1,300 m (Franzen et al., 2008). Its habitat requirements are similar to L. luschani.

Behaviour

This species activity pattern and behaviour are similar to that described for L. luschani (Steinfartz & Mutz, 1999; Franzen et al., 2008).

Threats and conservation

The species can be abundant

within its restricted range. Given its very small range Lyciasalamandra atifi is considered Endangered (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

Lyciasalamandra species have been kept in captivity. They are easy to keep (see under L. luschani), but breeding in captivity is rare (Steinfartz & Mutz, 1999; Raffaëlli, 2007).

Comments

The life history of all Lyciasalamandra species is

similar.

References

Franzen et al. (2008); Göçmen et al. (2013a); IUCN (2013);

Raffaëlli (2007); Steinfartz & Mutz (1999); Stuart et al. (2008).

Lyciasalamandra billae (Franzen & Klewen, 1987) | Bille’s Salamander Description

A slender salamander with delicate limbs. Generally similar in appearance to Lyciasalamandra luschani. Dorsal tail tubercle in males very small (Steinfartz & Mutz, 1999). Colour varies greatly among individuals. Eyeballs dark. Ground colour varies from salmon-orange or reddish, to black. Small silvery-white spots, often regularly distributed over the back, sometimes arranged in two dorsolateral stripes. Gland openings on paratoids, dorsum and tail are black, contrasting with lighter ground colour. Lateral white band always well-defined and extending to beneath the eyes (Steinfartz & Mutz, 1999). Ventral side translucent flesh-coloured.

Lyciasalamandra billae, male, south of Antalya. Photo: Frank Pasmans. 244

Salamanders of the Old World | Lyciasalamandra

Total maximum length 13.6 cm (Franzen et al., 2008).

Diagnosis

A slender, terrestrial salamander with delicate limbs and large protruding eyes. Colour pattern variable. Can be distinguished from other Lyciasalamandra species by clearly contrasting white lateral band, orange to salmon ground colour and lack of conspicuous yellow colouration on paratoids and eyeballs (Franzen et al., 2008).

Parturition

This species is viviparous like the other Lyciasalamandra species.. A female usually gives birth to two fully metamorphosed young (Steinfartz & Mutz, 1999) (see Lyciasalamandra luschani).

Lyciasalamandra billae, female, Goynuk. Photo: Frank Pasmans.

Distribution

Eastern Taurus range, southwest of Antalya, between Kedetler and Beldibi, a north-south distance of only 15 km (Franzen et al., 2008). Occasional hybrids have been found in a narrow contact zone with L. antalyana (Johannesen et al., 2006).

Habitat

All Lyciasalamandra species typically inhabit pine forest and maquis shrublands on slopes with a northern exposure. Lyciasalamandra billae occurs at altitudes from 15-230 m (Franzen et al., 2008). Its habitat requirements are similar to L. luschani.

Behaviour

This species activity pattern and behaviour are similar to that described for L. luschani (Steinfartz & Mutz, 1999; Franzen et al., 2008).

Threats and conservation

This species can be abundant within its restricted range. Given its very small range it is considered Critically Endangered (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

Lyciasalamandra species have been kept in captivity. They are easy to keep (see under L. luschani), but breeding in captivity is rare (Steinfartz & Mutz, 1999; Raffaëlli, 2007).

Comments

The life history of all Lyciasalamandra species is

similar.

References

Franzen et al. (2008); IUCN (2013); Johannesen et al.

(2006); Raffaëlli (2007); Steinfartz & Mutz (1999); Stuart et al. (2008).

Lyciasalamandra fazilae (Basoglu & Atatür, 1974) | Fazila’s Salamander Description

A slender salamander with delicate limbs. Generally similar in appearance to Lyciasalamandra luschani. Dorsal tail tubercle small (Steinfartz & Mutz, 1999). Ground colour of dorsum, head, tail and limbs orange-red, a colour only found on the tails of other Lyciasalamandra species. Laterally, a conspicuous silvery-white band sharply separates the bright dorsal side from the more weakly pigmented ventral side. Brown to black isolated spots on the back may cluster together above the white lateral band. On the middle of the back the borders of these spots are not so uniformly structured and may form a contrasting marbled pattern or even obscure most of the red dorsal colour (Steinfartz & Mutz, 1999). Ventral side bright orange-red, often translucent.

Lyciasalamandra fazilae, male, Iztuzu. Photo: Max Sparreboom.

Total maximum length 14.1 cm (Franzen et al., 2008).

Diagnosis

A slender, terrestrial salamander with delicate limbs and large protruding eyes. Can be distinguished from other Lyciasalamandra species by the intense orange-red colouration, contrasting with deep black (Franzen et al., 2008).

Parturition

This species is viviparous like the other Lyciasalamandra species. A female usually gives birth to two fully metamorphosed young (Steinfartz & Mutz, 1999) (see Lyciasalamandra luschani). Skeletochronological research on a population of Lyciasalamandra fazilae from Dalyan has shown that juveniles reach sexual maturity after three years. Males may reach a maximum age of eight years, and females 10 years (Olgun et al., 2001).

Lyciasalamandra fazilae, male, Iztuzu. Photo: Max Sparreboom. 245

Lyciasalamandra fazilae, habitat, Candir near Sultanye. Photo: Max Sparreboom.

Distribution

This species’ range extends from the hills around the Köycegiz valley in a south-eastern direction to the area around Üzümlü (north of Fethiye), a west-east distance of about 60 km (Franzen et al., 2008).

Habitat

All Lyciasalamandra species typically inhabit pine forest and maquis shrublands on slopes with a northern exposure. Lyciasalamandra fazilae occurs from sea level to altitudes around 1,000 m (Franzen et al., 2008). Its habitat requirements are similar to L. luschani.

Behaviour

This species’ activity pattern and behaviour are similar to that described for L. luschani (Steinfartz & Mutz, 1999; Franzen et al., 2008).

Threats and conservation

This species can be abundant within its restricted range. Given its very small range L. fazilae is considered Endangered (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

Lyciasalamandra species have been kept in captivity. They are easy to keep (see under L. luschani), but breeding in captivity is rare (Steinfartz & Mutz, 1999; Raffaëlli, 2007).

Comments

The life history of all Lyciasalamandra species is

similar.

References

Franzen et al. (2008); IUCN (2013); Olgun et al. (2001);

Raffaëlli (2007); Steinfartz & Mutz (1999); Stuart et al. (2008).

Lyciasalamandra flavimembris (Mutz & Steinfartz, 1995) | Marmaris

Salamander

Description

A slender salamander with delicate limbs. Generally similar to Lyciasalamandra luschani. Dorsal tail tubercle very small (Steinfartz & Mutz, 1999). Ground colour of dorsal side dark brown with an irregular pattern of tiny silvery-white dots. On head dark colour contrasts with yellow eyeballs and paratoids. Ventral

246

Salamanders of the Old World | Lyciasalamandra

colouration sharply separated from dorsal colouration by an unpigmented line along the flanks. Ventral side translucent. Limbs and tail yellow to light brown-orange, with whitish spots. Colour separation between dorsal and ventral sides continuing on tail, but with lighter dorsal side. Black glandular openings on paratoids clearly visible (Steinfartz & Mutz, 1999).

Lyciasalamandra flavimembris, male, near Marmaris. Photo: Max Sparreboom.

Lyciasalamandra flavimembris, female, near Marmaris. Photo: Max Sparreboom.

Total maximum length 15.0 cm (Franzen et al., 2008).

80-620 m (Franzen et al., 2008). Its habitat requirements are similar to L. luschani.

Diagnosis

A slender, terrestrial salamander with delicate limbs and large protruding eyes. Can be distinguished from other Lyciasalamandra species by the combination of dark dorsal colour, yellow paratoids and eyeballs, and unpigmented flanks (Franzen et al., 2008).

Parturition

This species is viviparous like the other Lyciasalamandra species. A female usually gives birth to two fully metamorphosed young (Steinfartz & Mutz, 1999) (see Lyciasalamandra luschani).

Distribution

This species’ range extends from Marmaris in a north-eastern direction to the area near Ula, a north-south distance of around 30 km (Franzen et al., 2008).

Habitat

All Lyciasalamandra species typically inhabit pine forest and maquis shrublands on slopes with a northern exposure. Lyciasalamandra flavimembris occurs at altitudes from

Behaviour

This species’ activity pattern and behaviour are similar to that described for L. luschani (Steinfartz & Mutz, 1999; Franzen et al., 2008).

Threats and conservation

Given its very small range L. flavimembris is considered Endangered (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

Lyciasalamandra species have been kept in captivity. They are easy to keep (see under L. luschani), but breeding in captivity is rare (Steinfartz & Mutz, 1999; Raffaëlli, 2007).

Comments

The life history of all Lyciasalamandra species is

similar.

References

Franzen et al. (2008); IUCN (2013); Raffaëlli (2007);

Steinfartz & Mutz (1999); Stuart et al. (2008).

Lyciasalamandra helverseni (Pieper, 1963) | Helversen’s Salamander Description

A slender salamander with delicate limbs. Generally similar in appearance to Lyciasalamandra luschani. Dorsal tail tubercle relatively large, up to 4-5 mm long (Steinfartz & Mutz, 1999). Ground colour of dorsal side dark brown, sometimes with a

purplish sheen. Paratoids dark, sometimes yellow. Limbs and tail lighter coloured than the back. Small yellow spots on the back. The flanks are yellow. Ventral side flesh-coloured to orange-red, marbled with white and light bluish, translucent. Underside of tail orange-yellow, throat yellowish-pink. Females on average slightly larger than males, with relatively longer tail. 247

Lyciasalamandra helverseni, female, Karpathos, Greece. Photo: Frank Pasmans.

Total maximum length 14.8 cm (Steinfartz & Mutz, 1999).

Diagnosis

A slender, terrestrial salamander with delicate limbs and large protruding eyes. Can be distinguished from other Lyciasalamandra species by fairly large size, large dorsal tail tubercle, and rather uniform brown colour, speckled with yellow dots (Steinfartz & Mutz, 1999).

Parturition

This species is viviparous like the other Lyciasalamandra species. A female usually gives birth to two fully metamorphosed young (Steinfartz & Mutz, 1999) (see Lyciasalamandra luschani).

Distribution

This species is endemic to the Greek islands of Karpathos, Kassos and Saria, in the south-east Aegean Sea (Steinfartz & Mutz, 1999).

Habitat

All Lyciasalamandra species typically inhabit pine forest and maquis shrublands on slopes with a northern exposure. Lyciasalamandra helverseni is found in rocky, shrubby habitats and loose rock walls and ruins.

Behaviour

This species’ activity pattern and behaviour are similar to that described for L. luschani (Steinfartz & Mutz, 1999; Franzen et al., 2008).

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Lyciasalamandra helverseni, male, Karpathos, Greece. Photo: Frank Pasmans.

Threats and conservation

The species is fairly common and abundant within its range, and can also be found near human settlements. Given its small range Lyciasalamandra helverseni is considered Vulnerable (Stuart et al., 2008; IUCN, 2013). It is protected by national legislation (Valakos et al., 2008).

Observations in captivity

Lyciasalamandra species have been kept in captivity. They are easy to keep (see under L. luschani), but breeding in captivity is rare (Steinfartz & Mutz, 1999; Raffaëlli, 2007).

Comments

The relative position of Lyciasalamandra helverseni within the phylogeny of Lyciasalamandra is obscured by a striking discord between nuclear and mitochondrial markers. In the mitochondrial analyses of Weisrock et al. (2006) and Veith et al. (2008) the mitochondrial DNA tree links L. helverseni to the L. billae / L. antalyana group that lives geographically distant from Karpathos. It has been suggested that L. billae may have reached Karpathos by floating on ocean-borne vegetation rafts (Veith et al., 2008).

References

IUCN (2013); Raffaëlli (2007); Steinfartz & Mutz (1999);

Stuart et al. (2008); Valakos et al. (2008); Veith et al. (2008); Weisrock et al. (2006)..

Lyciasalamandra luschani (Steindachner, 1891) | Luschan’s Salamander Description

A slender salamander with delicate limbs. Head broad and flat, only slightly longer than wide. Snout rounded. Eyes large and protruding. Paratoids long, narrow and protruding, with clearly visible, dark-coloured gland openings. Gular fold well-developed. Body cylindrical with 11-13 weakly defined costal grooves. Tail length shorter than snout-vent length. Tail roughly oval in cross section and slightly laterally compressed. Conspicuous dorsal tail tubercle, 3-4 mm long, at the base of the tail in males. The projection is finger-like and is inclined anteriorly. Limbs with four fingers and five toes without webbing. Lungs well-developed. Skin is not entirely smooth in males. Dorsal skin, throat and forelimbs are covered with minute spiny rugosities (Özeti, 1967). Males have slightly thicker forelimbs than females. Older females sometimes have a slight

elevation on the part of the tail-base where males have the dorsal tubercle (Steinfartz & Mutz, 1999). So females, too, have a kind of dorsal tail tubercle. It contains hypertrophied granular and mucous glands (Staub et al., 2005). Colour varies between individuals and differs between subspecies. Three subspecies are recognised on the basis of colour and genetic differences. Lyciasalamandra luschani basoglui (Baran & Atatür, 1980). Ground colour of dorsal side brownish to reddish with a variable pattern of brownish or blackish spots. In females brown pattern more extensive than in males. Ground colour of paratoids lighter. Head, tail and sides of limbs red to pink with a few brown spots (Steinfartz & Mutz, 1999). Up to 14.2 cm total length. Distributed between Kas and the island of Kekova, to Akuyu Mevki, Turkey, on the mainland. Also on the Greek island of Kastellorizon (Franzen et al., 2008; Valakos et al., 2008). Lyciasalamandra luschani finikensis (Basoglu & Atatür, 1975). Ground colour of dorsal side brownish-black with a variable pattern of silvery-white spots. Red and yellow colours lacking. Sides pigmented whitish (Steinfartz & Mutz, 1999). In animals from Finike light dorsal spots small and isolated; in animals from Catalar and Arif marbled spots more extensive and brighter. Total length up to 14 cm. Ranges from Finike on the coast, north to Catalar and Arif, and east to Alakir Baraji and Catal Tepesi, Turkey (Franzen et al., 2008; Beukema et al., 2009).

Lyciasalamandra luschani basoglui, male, Kekova. Photo: Max Sparreboom.

Lyciasalamandra luschani basoglui, female, Kekova. Photo: Max Sparreboom.

Lyciasalamandra luschani luschani (Steindachner, 1891). Ground colour of dorsal side yellow to silver, covered with a

Lyciasalamandra luschani finikensis, female, Finike. Photo: Frank Pasmans. 249

Lyciasalamandra luschani luschani, male, north of Dodurga. Photo: Max Sparreboom.

pattern of dark brown to black spots that may predominate over the ground colour. Paratoids mostly yellow, sides yellowish, limbs and tail reddish to light brown. Ventral side less pigmented, often flesh-coloured (Steinfartz & Mutz, 1999). Total length up to 13.0 cm. Occurs in a few localities between Esen and Letoon (ruined city between Fethiye and Patara), Turkey (Franzen et al., 2008)

Diagnosis

A slender, terrestrial salamander with delicate limbs and large protruding eyes. Colour pattern highly variable. Prominent dorsal tail tubercle in male.

Parturition

This species is viviparous like the other Lyciasalamandra species. A female usually gives birth to two fully metamorphosed young of 6.35 cm average lenght. The larvae feed on the other eggs within the uterus. Young salamanders are born from October to the end February. No gravid females were found in the field from the end of February onwards. Most observations of births have been made in captivity. Gestation time is rather short, probably from 5-8 months (Steinfartz & Mutz, 1999). Skeletochronological research on a population of Lyciasalamandra fazilae from Dalyan has shown that juveniles reach sexual maturity after three years. Males may attain a maximum age of eight years, females 10 years (Olgun et al., 2001).

Distribution

The three subspecies of Lyciasalamandra luschani occur in an area covering little more than 100 km, from Fethiye southwards to Finike, Turkey, including the islands of Kastellorizon, Greece, and Kekova, Turkey (Franzen et al., 2008). The ranges of the known subspecies of L. luschani are almost contiguous (Göçmen et al., 2013b).

Habitat The range of Lyciasalamandra luschani. 250

Salamanders of the Old World | Lyciasalamandra

All Lyciasalamandra species typically inhabit pine forest and maquis shrublands on slopes with a northern aspect. Lyciasalamandra luschani occurs at altitudes from 60-840 m

(Franzen et al., 2008). Habitat requirements include an average annual rainfall between 800-1000 mm, an average January temperature above 0°C, and a soil structure with crevices. The crevices provide crucial survival refuges during the hot, dry summer months (Klewen, 1988; Steinfartz & Mutz, 1999; Veith et al., 2001).

Behaviour

These alamanders have been found active from early November to mid-April following rain. In the dry season they shun the surface and live a secretive life underground, many individuals often aggregating to share a single shelter (Gautier et al., 2006). The animals are active at night and occasionally in the morning (Steinfartz & Mutz, 1999). This species is a generalist and opportunist feeder. It seems to prefer arthropods but also takes earthworms and slugs. Coleopterans, gastropods and spiders have also been found in their stomachs (Dusen et al., 2004; Cicek et al., 2007; Polymeni et al., 2011). Natural enemies are invertebrates (scorpions), birds, hedgehogs and rats. In the face of danger, they may adopt a defensive position with the trunk raised above the substrate and arched. A distress call has been described for individuals of Lyciasalamandra luschani finikensis from the Arif, and several other, populations and appears to be typical for this subspecies (Franzen & Glaw, 1999; Beukema et al., 2009).

The onset of activity is determined by air temperature (13-14°C), rainfall, and air humidity in autumn and reproductive activity probably starts at that time too. In ideal weather conditions animals may be found in great numbers. Courtship generally resembles that of Chioglossa and Salamandra (Arnold, 1987), and especially Mertensiella (Schultschik, 1994a). The male makes a sudden approach to a female, pushes himself forward under the female’s body and hooks his forelimbs over hers. While the male is carrying the female on his back in this ventral amplexus, the pair makes body movements during which the male rubs the caudal tubercle on the cloacal orifice of the female and eventually inserts it. This pseudo-coitus takes place shortly before the male deposits a spermatophore. It may serve to ascertain whether the female is ready for sperm transfer.

The apparent effect is that it stabilises the female precisely over the spot where the spermatophore will be dropped so that it can be picked up successfully (Schultschik, 1994a; Sever et al., 1997). Both sexes make wriggling and snake-like movements with their bodies and a whitish substance is secreted by the male from glands on the dorsum. The male then deposits a spermatophore on the substrate, under the female’s cloaca and displaces his sacrum laterally to one side. By displacing his sacrum, the female falls upon the spermatophore with her cloaca opened and picks up the sperm cap in her cloaca (Rehberg, 1981; Schultschik, 1994ab; Steinfartz & Mutz, 1999).

Threats and conservation

Within its naturally restricted range, this species is potentially threatened by habitat loss caused by forest fires, and over-collection for scientific purposes. It is listed as Endangered by Stuart et al. (2008) and Vulnerable by IUCN (2013).

Observations in captivity

Lyciasalamandra species have been kept in captivity. Their reproductive behaviour has been described largely on the basis of detailed observations of captive animals (Rehberg, 1981; Klewen, 1988; Steinfartz & Mutz, 1999). The terrarium should be rather dry and provided with rocks and hiding places. Temperatures should not exceed 20-22°C in summer, and should be lowered to 8°C for several weeks during winter. They are easy to keep, but breeding in captivity is rare (Raffaëlli, 2007).

Comments

The life history of all Lyciasalamandra species is similar. Interestingly, the distress call is only known of Lyciasalamandra l. finikensis.

References

Arnold (1987); Beukema et al. (2009); Cicek et al. (2007);

Dusen et al. (2004); Franzen et al. (2008); Franzen & Glaw (1999); Gautier et al. (2006); Göçmen et al. (2013b); IUCN (2013); Olgun et al. (2001); Özeti (1967); Polymeni et al. (2011); Raffaëlli (2007); Rehberg (1981) ; Schultschik (1994a, 1994b); Sever et al. (1997); Staub et al. (2005); Steinfartz & Mutz (1999); Stuart et al. (2008); Valakos et al. (2008); Veith et al. (2001).

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Mertensiella Wolterstorff, 1925 Premaxillary paired with short backward extensions. Nasals large and in contact. Frontosquamosal arch absent. Two series of vomerine teeth in S-shape. Tongue rounded, free at the sides. Tail almost cylindrical and slightly compressed. The male has a dorsal tail tubercle similar to that of Lyciasalamandra (Sever et al., 1997). Insemination of the female is preceded by a ventral amplexus similar to that of Pleurodeles and Salamandra (Thorn, 1969). The tubercle plays a role during courtship and mating and is a unique feature in salamanders. It has long been regarded as a synapomorphic trait of Mertensiella caucasica and M. luschani, hence the former inclusion of both taxa in a single genus Mertensiella.

Distribution is restricted to the Caucasus and north-eastern Turkey. Mertensiella caucasica is the single extant representative of the genus. Mertensiella is sister to Chioglossa, another monotypic genus with Chioglossa lusitanica Bocage, 1864, from the Iberian Peninsula. Both species are streamside salamanders characterised by a slender build with short appendages and a long tail (Arntzen et al., 2007b).

Mertensiella caucasica (Waga, 1876)

References

Arntzen et al. (2007b); Sever et al. (1997); Thorn (1969).

Mertensiella caucasica (Waga, 1876) | Caucasian Salamander Description

A slender, long-tailed salamander. Tail about 60% of total length. Head depressed, a little longer than wide, rounded snout and large protruding eyes. Paratoids elongated. Tongue round and free at the sides. Body slightly flattened; tail almost cylindrical. Tail gradually laterally compressed towards

tail end. Usually 12-13 costal grooves. V-shaped depression on the hind side of the head, continuing as a vertebral depression along the back. Limbs rather short, with four fingers and five toes, moderately developed and without webbing. Gular fold present. Lungs well-developed (Thorn, 1969). Ground colour dark brown to black, speckled with yellow or yellow-orange spots, rounded or elongate and arranged in two more or less longitudinal rows along the back. Small yellow spots also on sides and limbs. Underside dark red-brown to grey-brown, sometimes with small whitish speckles on throat, venter and sides.

Mertensiella caucasica, male, NE Turkey. Photo: Max Sparreboom. 252

Salamanders of the Old World | Mertensiella

Mertensiella caucasica, female, NE Turkey. Photo: Max Sparreboom.

The adult male has a conspicuous tubercle projecting from the skin of the dorsal surface of the tail-base; 2-4 mm long and slightly bent anteriorly. This tail tubercle is permanent and independent of breeding condition. Males have longer, thicker forelimbs (‘muscles’) that play a role in clasping the female during courtship. The dorsal skin of the male is covered with minute rugosities, small sharp tubercles that make the skin less smooth than that of the female (Schultschik, 1994a; Franzen, 1999; Sever et al., 1997). Total maximum length 18-20 cm (Thorn, 1969). Mertensiella caucasica, as currently defined, represents two evolutionary lineages that evolved independently, perhaps splitting during the lower Pliocene. These lineages represent different taxa, possibly soon to be described as separate species, distributed in the Borjomi area in central Georgia, and in southwestern Georgia and north-eastern Turkey, respectively. The two forms can only be distinguished genetically (Tarkhnishvili et al., 2000). Their isolation has been explained as a result of different climatic requirements (Tarkhnishvili et al., 2008).

Diagnosis

A slender salamander with a long tail, about 60% of the total length. Small yellow spots and stripes. Large protruding eyes. Prominent dorsal tail tubercle in male.

Eggs are 4.5-6 mm in diameter. The gelatinous egg capsule is 9-10 mm in diameter. The relatively large eggs are unpigmented and yellow-white in colour. Embryonic development is extremely slow. The larvae hatch at a size of 17-20 mm after 7-13 weeks, or even as long as 4.5 months at low water temperatures of ca. 12°C. Larger larvae, from 24-26 mm, have been recorded in captive animals (Schultschik, 1994ab; Franzen, 1999). Newly hatched larvae have well-developed external gills and a tail-fin that extends to the back of the head. In later stages the tail-fin is much reduced. Developed larvae have a slender, elongated body with a large hammer-shaped head, short external gills and a low tail-fin, rounded at the tip. Body is grey in colour with rows of round, light spots on the flanks. The yellow spots appear during metamorphosis. Metamorphosis takes place after two to four winters at a size of 28-46 mm snout-vent length. In a population from Borjomi Canyon, Georgia, males reached sexual maturity after 12 years, females after 16 years. Skeletochronological analysis indicated that the oldest animals were 22-23 years old (Tarkhnishvilli & Gokhelashvili, 1999). These findings may be extreme and require confirmation. In an Anatolian population (Kümbet Plateau, Turkey, 1,575 m altitude) the age at maturity was 4-5 years in both sexes and the maximum age was 10 years in males and nine years in females (Üzüm, 2009).

Eggs and larvae

A female normally lays between 11-24 eggs, deposited singly or in small clusters. They are laid in hidden places in streams or may be attached to plants and leaves. Eggs are rarely found, probably because they are often laid in underground parts of springs and stream beds (Schultschik, 1994ab, Franzen, 1999).

Mertensiella caucasica, larva, NE Turkey. Photo: Max Sparreboom.

The range of Mertensiella caucasica.

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Mertensiella caucasica, habitat, NE Turkey. Photo: Max Sparreboom.

Distribution

Mertensiella caucasica is restricted to north-east Anatolia and the western spurs of the Trialeti mountain ridge, Turkey, and the Meskhetian and Lazistanian ridges, Georgia. It occurs at altitudes from sea level to 2,800 m (Franzen, 1999). The presence or absence of this salamander depends on the level of rainfall, temperature and ruggedness of the terrain (Tarkhnishvili et al., 2008).

Habitat

This species inhabits streamside habitats in forests in the subalpine belt, and in alpine meadows. It lives mainly in small streams less than 1-1.5 m wide and about 20-30 cm deep in spring. The banks are covered with dense vegetation and contain a thick layer of leaf and branch litter, moss and grass (Franzen, 1999; IUCN, 2013).

Behaviour

These salamanders are active from April-October and are strictly nocturnal. Activity patterns differ depending on the region. In Georgia, at altitudes of 1,000-1,300 m, animals were active from May-August, whereas in Turkey, at altitudes between 25-100 m, active animals could not be found in summer. This species is probably inactive in the winter, even in frost free areas (Franzen, 1999). Adult salamanders feed on both aquatic and terrestrial prey including crustaceans of the family

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Oniscidae, Arachnida, and insect larvae. Juveniles feed on very small soil invertebrates, mainly Collembola (Tarkhnishvili & Gokhelashvili, 1999). Their principal natural enemy is the Grass Snake (Natrix natrix). This species may adopt several different anti-predator postures: it may curl up, stretch the tail forward and hide its head under it; it may feign death by remaining motionless and laying the fore legs against the body; or on further irritation it may suddenly flip its curled-up body and thus displace itself. Tail autotomy, as in Chioglossa, has not been observed (Franzen, 1999). The timing of breeding is determined by air and water temperature (13-15°C). Breeding usually occurs in spring and early summer. In Georgia the breeding period starts in May, reaches a peak in the second half of June, and continues until mid-July. Males appear at the breeding sites before females (Tarkhnishvili & Serbinova, 1993; Tarkhnishvili & Gokhelashvili, 1999). Reproduction takes place at the streamsides, partly in water, partly on land. Several reproductive behaviour patterns have been described. Courtship generally resembles that of Chioglossa and Salamandra (Arnold, 1987). Males await the arrival of females in or near the stream (pers. obs. in NE Turkey). When in water, the

male searches for a mate by swimming round, with forelimbs slightly raised. On bumping into a female, he attempts to creep under her and first clasp her hind legs from below. The male then pushes further forward under the female’s body and hooks his forelimbs over hers. While the male is carrying the female on his back in this ventral amplexus, the pair makes body movements during which the male rubs his caudal tubercle on the cloacal orifice of the female and eventually inserts it. This pseudo-coitus takes place shortly before the male deposits a spermatophore and may serve to ascertain whether the female is ready for sperm transfer. The apparent effect is that it stabilises the female precisely over the spot where the spermatophore will be dropped and can be picked up successfully (Schultschik, 1994a; Sever et al., 1997). The male then deposits a spermatophore on the substrate, under the female’s cloaca and displaces his sacrum laterally to one side. By displacing his sacrum, the female falls upon the spermatophore and picks up the sperm cap in her cloaca (Schultschik, 1994ab). Egg laying may start three days after mating, but as much as two months may pass between mating and first egg laying (Schultschik, 1994ab; Tarkhnishvili & Gokhelashvili, 1999).

Threats and conservation

Habitat destruction is a major threat across this species’ range. In Georgia, illegal logging, use of brooks as roads for the transportation of cut trees, and destruction of habitats by cattle are known causes of population declines. In Turkey, road construction and summer house tourism in the Black Sea Mountains pose a threat. The species is also collected for the pet trade. It is listed in the Red Data Book of Georgia and listed as Vulnerable by IUCN (Stuart et al., 2008; Tarkhnishvili & Kaya, 2009; IUCN, 2013).

Observations in captivity

Mertensiella caucasica has been kept in captivity and its reproductive behaviour and the devel-

Mertensiella caucasica, female. NE Turkey. Photo: Max Sparreboom.

opment of larvae and juveniles have been described on the basis of detailed observations of captive animals (Schultschik, 1994ab; 2013a). It is a delicate species that should be kept in a cold, humid environment, with water temperatures around 12-14°C, and a short winter rest period at temperatures of 4°C. Air temperature should be kept higher, up to 20°C. Tanks should have a shallow water part and the water should be aerated. Animals have lived in captivity for more than 16 years and a second generation in captivity has been obtained by Schultschik.

References

Arnold (1987); Franzen (1999); IUCN (2013); Schultschik

(1994a, 1994b, 2013a); Sever et al. (1997); Stuart et al. (2008); Tarkhnishvili et al. (2000, 2008); Tarkhnishvili & Gokhelashvili (1999); Tarkhnishvili & Kaya (2009); Tarkhnishvili & Serbinova (1993); Thorn (1969); Üzüm (2009).

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Neurergus Cope, 1862 Salamanders of the Middle Eastern genus Neurergus are moderately slender animals, dark brown to black above, with a pattern of yellow spots. Only Neurergus kaiseri has a different colour pattern and is smaller than the other three species. Neurergus species are stream-dwelling. Premaxillary bone single; frontosquamosal arch incomplete; maxilla in contact with pterygoid (Leviton et al., 1992). Tongue rounded, small, free on the sides and largely free behind. Palatal teeth arranged in two straight rows which converge anteriorly and diverge posteriorly. Paratoid glands present, poorly defined. Five toes on hindlimbs. Tail long, compressed. Molecular work has shown that the genus Neurergus is monophyletic (Steinfartz et al., 2002) and sister to Ommatotriton (Pyron & Wiens, 2011). Four species are currently recognised.

Neurergus crocatus Cope, 1862 Neurergus derjugini (Nesterov, 1916) Neurergus kaiseri Schmidt, 1952 Neurergus strauchii (Steindachner, 1887)

References

Leviton et al. (1992); Pyron & Wiens (2011);

Steinfartz et al. (2002).

The ranges of Neurergus species.

Neurergus crocatus Cope, 1862 | Lake Urmia Newt Description

256

A large-bodied newt. Head flattened, longer than wide. Snout rounded. Paratoids not prominent; gular fold present. Trunk almost round, rather slender, without dorsal ridge, but with slight vertebral depression. Lungs reduced. Tail longer than snout-vent length, rounded at the base, compressed lateral-

ly toward the tip. Tail-tip blunt. Moderately developed tail-fins on dorsal and ventral sides; dorsal tail-fin a little higher, especially in the breeding season. Limbs well-developed and broadly overlapping when adpressed. Hindlimbs thicker than frontlimbs in both sexes. Toes and fingers thick and flat (Freytag, 1957).

Neurergus crocatus, Choman Prov., Iraq. Photo: W. and C. Schneider.

Neurergus crocatus, Choman Prov., Iraq. Photo: W. and C. Schneider.

Salamanders of the Old World | Neurergus

Skin of dorsal side granulated and wrinkled, with scattered small warts. In terrestrial phase, the skin is dry and rough, not shiny as in Salamandra. Ventral side smooth. Dorsal colour dark brown to black with yellow, rounded, irregular blotches. Similar spots on the sides of the tail. Ventral surface orange-red in the male, yellowish in the female. Cloaca half rounded in the male, swollen in the breeding season, with a longitudinal slit. Cloaca conical in the female with a rounded opening and protruding (Schmidtler & Schmidtler, 1975; Fleck, 2011c). Spots along the tail do not develop a silver-blue colour in males, as in Neurergus strauchii. However, N. crocatus has its own sexual dimorphism in colour pattern during the breeding season: males may have a few large, intensely white and shiny dots on the tail, arranged in a single line (Schneider & Schneider, 2010; Fleck, 2010d). No subspecies are currently recognised but three clearly distinct colour morphs do exist, whose taxonomic status remains to be clarified (Schneider & Schneider, 2011; Fleck, 2011c; Schultschik, 2013b). Total length between 16-18 cm (Schmidtler & Schmidtler, 1975).

Eggs are joined in a jelly string. Occasionally there are more eggs in one capsule than the other. At water temperatures averaging 16°C, larvae hatch after 25-27 days at a length of 11 mm (Steinfartz, 1995) or 13-14 mm (Schultschik, 2013b). Larvae have a slender body-shape. The dorsal tail-fin reaches well onto the middle of the body. Tail-tip rounded. Short gills. Younger larvae are bright grey with irregular black spots, older larvae have irregular, large, bright blotches. Ventral colour uniformly light. Tail of older larvae more or less clearly pigmented. For comparative larval morphology of Neurergus crocatus and N. strauchii see Schmidtler & Schmidtler (1975) and Steinfartz (1995). Metamorphosis takes place after four or 5-6 months at a length of 60-70 mm (Timofeev, 1997). Growth is slow and sexual maturity is reached after 4-5 years in captive animals (Schultschik, 2013b; Thorn & Raffaëlli, 2001). In a study of the age structure of a breeding population in Turkey, ages ranged from 5-14 years for males and from 8-17 years for females (Üzüm et al., 2011).

Distribution

The Lake Urmia Newt occurs in the mountains west of Lake Urmia in northwestern Iran (Najafi-Majd & Kaya, 2013; Al-Sheikhly et al., 2013), in southeast Anatolia, Turkey, and in the Kurdish region of northern Iraq (Schneider & Schneider, 2010, 2011; IUCN, 2013).

Diagnosis

Yellow dorsal blotches often larger than in Neurergus strauchii; ventral side orange-red in males, yellowish in females. Female cloaca slightly protruding in breeding season.

Eggs and larvae

Oviposition occurs in March-April. Eggs are laid in clutches of 150-200 on the lower surface of flat stones in mountain streams. Fleck (2012) reports an instance of 350 eggs. Jelly capsule ca. 6-9 mm in diameter and the embryo diameter is 1.5-2.0 mm (Steinfartz, 1995; Timofeev, 1997).

The range of Neurergus crocatus.

Habitat Neurergus crocatus, larva. Photo: Sergé Bogaerts.

This species inhabits spring-fed pools and mountain brooks in valleys with or without shade cast by vegetation, between 500-1,500 m altitude (Schmidtler & Schmidtler, 1975). Baran and Atatür (1998) cite a vertical distribution of 1,500- 2,000 m. 257

touching his tail. The male deposits a spermatophore, moves forward and makes a 90º turn, bringing him back into a position perpendicular to the female’s body. He stops (‘brakes’) the female in her progress at a point when her cloaca is situated above the place where the spermatophore was deposited. This behaviour is similar in Neurergus crocatus, N. strauchii, and N. kaiseri. The observations on N. derjugini are unclear. This courtship behaviour is generally similar to that of the small European pond-breeding newts and of Asian Cynops, Pachytriton and Paramesotriton (Sparreboom et al., 2000).

Threats and conservation Courtship behaviour in the Lake Urmia Newt (Neurergus crocatus). The male (left) takes up a position almost opposite the female’s body. He bends his tail back against the side nearest to the female, the tail-tip reaching his flank. The tail-fanning movements begin at the tail-base and run up to the tail-tip. With every beat of the tail-base the distal part makes an outward slapping movement. Art: Bas Teunis. From: Sparreboom et al., 2000.

Behaviour

Hibernation probably lasts from December to the end of February. The start and duration of the breeding season varies with altitude, water level, and streamwater temperature and can begin at any time between mid-April and early June (Schneider & Schneider, 2010, 2011). Newts leave the water for the surrounding areas after breeding, but their terrestrial habitat remains unknown. The adults probably stay under rocks during winter (IUCN, 2013). Reproductive behaviour was studied in captive specimens originating from Aqrah in northern Iraq. The male takes up a position in front of the female, from where he starts a tailfanning display, fanning his tail in the direction of her snout. The female signals that she is responsive by moving forward towards the male. The male takes a few steps backward, then turns away from the female and creeps ahead of her, his tail making undulating movements. The female follows him,

This species is considered to be relatively susceptible to habitat change, habitat loss, pollution, drought and collection. Neurergus crocatus is protected by national legislation in Turkey and Iran and is listed as Vulnerable (IUCN, 2013).

Observations in captivity

Neurergus crocatus has been bred in captivity on several occasions (up to the fourth generation, Pasmans et al., in press), but keeping the animals alive for longer periods and rearing the juveniles, has proved to be difficult (Steinfartz, 1995; Timofeev, 1997; Wallays, 2002; Schultschik, 2013b). These newts should be kept in tanks with cool, running water, and with enough hiding places under flat stones, and so on. These animals can be kept in water almost all year round in captivity, but for successful breeding a terrestrial phase and hibernation period is recommended. The data on eggs and larvae, and the observations on courtship and oviposition reported above were made on captive animals.

Comments

For Iranian references see Baloutch & Kami (1995). For earlier literature see Freytag (1957).

References

Al-Sheikhly et al. (2013); Baloutch & Kami (1995);

Baran & Atatür (1998); Fleck (2010d, 2011c, 2012); Freytag (1957); IUCN (2013); Leviton et al. (1992); Najafi-Majd & Kaya (2013); Schmidtler (1994); Schmidtler & Schmidtler (1970, 1975); Schneider & Schneider (2010, 2011); Schultschik (2013b); Sparreboom et al. (2000); Steinfartz (1995); Thorn & Raffaëlli (2001); Timofeev (1997); Üzüm et al. (2011); Wallays (2002).

Neurergus derjugini (Nesterov, 1916) | Kurdistan Newt Description

A medium- to large-bodied, slender salamander. Head flattened, longer than wide. Snout rounded. Paratoids not prominent; gular fold present. Trunk almost round, rather slender, without dorsal ridge, but with slight vertebral depression. Lungs reduced. Tail-length about the same as snout-vent length. Tail rounded at the base, compressed laterally toward

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the tip. Tail-tip blunt. Moderately developed tail-fins on dorsal and ventral sides; dorsal tail-fin a little higher, especially in the breeding season. Limbs broadly overlap when adpressed (Leviton et al., 1992). Skin of dorsal side granular and wrinkled, with small, scattered, warts. In terrestrial phase, the skin is dry and rough, not shiny as in Salamandra. Ventral side smooth.

Neurergus derjugini, Hawraman Mountains, Iraq (type locality). Photo: W. and C. Schneider.

Neurergus derjugini, Surkew Mountains, Penjwin District, Iraq. Photo: W. and C. Schneider.

Dorsal colour dark brown to black with many small yelloworange, rounded, irregular spots. Similar spots on the sides of the tail. The black colour of the sides partly extends onto the belly. Ventral surface carmine-red. Throat and ventral surface of limbs often speckled with back spots (Schmidtler & Schmidtler, 1975).

middle of the body. They have two rows of light spots along the back, and two interrupted rows of black spots along the sides of the belly. Tail-fin mottled black-brown (Schmidtler & Schmidtler, 1975). Larvae still possess gills in early autumn. Many larvae may not complete metamorphosis until the following year (Sharifi & Assadian, 2005). Captive animals reached metamorphosis after 4-5 months at a length of 45-55 mm (Schultschik, 2013c). For comparative larval morphology of the four Neurergus species, see Schmidtler & Schmidtler (1975). Juveniles have a characteristic colour pattern that distinguishes them from juveniles of the other Neurergus species: black with

Cloaca of the male semi-spherical and protruding during the breeding season, with a longitudinal slit. Female cloaca tubular during the breeding season with a rounded opening, protruding 3 mm (Schmidtler & Schmidtler, 1975). Male Neurergus derjugini do not develop silver-blue spots along the tail. Total length between 15-17 cm (Schmidtler & Schmidtler, 1975), females a little larger than males (Torki, 2012).

Diagnosis

A newt with numerous yellow dorsal blotches. Ventral surface carmine-red. Limbs broadly overlap when adpressed (Leviton et al., 1992). Ventral colouration as in Neurergus crocatus. Breeding male has no silver-blue spots along the tail, as in N. strauchii. Smaller than N. crocatus and N. strauchii.

Eggs and larvae

Oviposition starts in April and may continue to mid-June. Approximately 100 eggs are laid singly or in small clumps on vegetation or on rocks in mountain streams (Sharifi & Assadian, 2005). Eggs laid in captivity were preferentially attached to stones in concealed spots. The diameter of their jelly was 6 mm, and that of the embryo ca. 2.5 mm. The yolk is whitish-grey in colour (Schultschik, 2013c). Larvae hatch at a length of 13-14 mm, after about 25 days at a temperature of 16C° and start feeding 12 days later (Schultschik, 2013c). In older larvae the well-developed dorsal tail-fin reaches to just over the

The range of Neurergus derjugini. 259

six bright orange markings on the sides of the head and the insertion points of the limbs (Schultschik, 2013c).

Distribution

Neurergus derjugini occurs in the Surkev and Avroman Mountains on the borders of Iran, Iraq and Turkey. The species is known from a number of streams along the road from Quri-Qaleh to Paveh in Iran. The number of known populations given by Iranian authors varies from four to eight (Sharifi & Assadian, 2004; Torki, 2012; further references in Fleck, 2011b and Schultschik, 2013c). They are distributed over a range of ca. 200 km from north to south (Schneider & Schneider, 2013).

Habitat

This species inhabits rocky mountain streams, with gravel and pebble substrates, at altitudes between 1,000-1,800 m, in the oak forest zone of the Zagros Mountains. Inhabited streams are usually shaded by bushes and have a water temperature of 13.7-16°C (Schneider & Schneider, 2011). The terrestrial habitat bordering the streams includes diverse types of open woodland. The high-altitude streams on the western Iranian Plateau are cooler than the lower elevation streams in the north-eastern part of the range (Sharifi & Asadian, 2004).

Behaviour

Animals move from their wintering sites to breeding streams as soon as the spring thaw occurs, from late January to early March. Breeding is recorded from late March onward (Sharifi & Assadian, 2005). Reproductive behaviour was studied in captive specimens of Neurergus derjugini originating from the area around Quri-Qaleh (Kermanshahan), Iran. Typically the male takes up a position high on a stone in the water, from where he surveys the tank. He starts tail-fanning at every object that comes near. After he has approached a female he starts a tail-fanning display in the direction of her snout. When the female is responsive, the male turns away from her and deposits a number of spermatophores. The female is led over the spermatophores and picks up the

sperm cap from one of them. This behaviour is similar in the four Neurergus species although observations on N. derjugini courtship are fragmentary (Sparreboom et al., 2000).

Threats and conservation

This species may be locally common, where suitable habitat is present. Habitat loss through diversion of streams for irrigation is probably the most important factor threatening the species in its Iranian range (Sharifi & Assadian, 2004). It is difficult to judge just how endangered this species is. It is listed as Critically Endangered (IUCN, 2013), but Schneider & Schneider (2013) were unable to identify specific threats and consider the species Not Endangered.

Observations in captivity

Neurergus derjugini has been bred to the second generation by Schultschik (2013c), but rearing the second generation juveniles failed. The observations on larvae and courtship reported above were made on captive animals.

Comments

For earlier literature see Freytag (1957), Schmidtler & Schmidtler (1975) and Frost (2013). Two subspecies were described by Nesterov (1916): Neurergus d. derjugini, described from the Surkev Mountains in Iraq; and N. d. microspilotus, described from the Avroman Mountains in Iraq (Schneider & Schneider, 2011; Schultschik, 2013c). Neurergus d. derjugini is characterised by a few large yellow spots, and N. d. microspilotus, by numerous small spots. Closer examination of specimens of both forms showed that variation in the dorsal spot pattern was not sufficient to differentiate the two forms as subspecies (Schneider & Schneider, 2013).

References

Fleck (2011b); Freytag (1957); Frost (2013); IUCN (2013);

Leviton et al. (1992); Nesterov (1916); Schmidtler & Schmidtler (1975); Schneider & Schneider (2011, 2013); Schultschik (2013c) ; Sharifi & Assadian (2004, 2005); Sparreboom et al. (2000); Torki (2012).

Neurergus kaiseri Schmidt, 1952 | Luristan Newt Description

A small colourful newt. Head flattened, longer than wide. Snout rounded. Paratoids not prominent. Trunk almost round, rather slender, without dorsal ridge, but with slight vertebral depression. Tail almost as long as snout-vent length, rounded at the base, compressed laterally toward the tip. Skin of dorsal side rather smooth with small warts. Ventral side smooth.

Colour black with irregular-shaped white blotches covering head, back and sides of body and tail. White blotches sometimes 260

Salamanders of the Old World | Neurergus

forming white bands on the sides. Yellow-orange stripe along the back, bordered with irregular white spots, forming a wave pattern. Sometimes orange spots on white patches in paratoid region. Limbs white or orange with black patches. Ventral surface of head, body, limbs and tail orange. Male cloaca swollen in the breeding season. Female cloaca extended in tubular shape 5-6 mm long, much longer than in other Neurergus species (Schmidtler & Schmidtler, 1975). Body measurements have shown differences between the sexes

Neurergus kaiseri, Haft-tanan, near Dezful, Khuzestan, Iran. Photo: Omid Mozaffari.

The range of Neurergus kaiseri.

(Sharifi et al., 2012) and while a light blue colouration can sometimes be observed on the sides of the male’s tail (Schneider & Schneider, 2013), the best criterion to distinguish the sexes in the field is the form of the cloaca in the breeding season.

place after 3.5 months at a length of 45-55 mm. The newts become sexually mature after 3-4 years on reaching a total length of some 110 mm (Schultschik, 2013d; Pasmans et al., in press).

Total length between 11-14 cm (Schmidtler & Schmidtler, 1975), females a little larger than males (Torki, 2012; Sharifi et al., 2013).

Diagnosis

A small newt with spectacular black, white and orange colouration. Yellow-orange stripe on the back and uniformly orange on ventral side. Female with strongly extended cloaca in breeding season.

Eggs and larvae

Oviposition takes place in March-April, depending on altitude. Captive females have laid up to 160 eggs (Pasmans et al., in press). Eggs are pressed singly into small cracks and crevices in rocks. Jelly capsule 4 mm in diameter, the embryo 1.5-2 mm in diameter (Schmidtler & Schmidtler, 1975). Larvae hatch after ca. 17 days at a length of 13-14 mm (Steinfartz & Schultschik, 1997; Schultschik, 2013d). Young larvae were found at the type locality in mid-April. Schmidtler & Schmidtler (1975) found larvae nearing metamorphosis at the end of May in a water body with water exceeding 20°C in temperature. High temperatures lead to rapid metamorphosis. The dorsal tail-fin of the larva reaches well past the middle of the body, which is a characteristic of pond-type larvae. Younger larvae are yellow with minute black dots. Older larvae have light spots along the back, often forming median rows. Belly uniformly lightcoloured. Tail almost invariably without dark pigment. For comparative larval morphology of Neurergus, see Schmidtler & Schmidtler (1975). In captive animals, metamorphosis takes

Distribution

Neurergus kaiseri occurs in the southern Zagros range in Iran. It is known from Shahbazan and Talehzang, Ahoo-Burad, and in the Shahzade Ahmad and Hajbarikab River valleys (Sharifi et al., 2008; Schultschik, 2013d) as well as in the drainage area of the Karkheh River (Schneider & Schneider, 2013). One population has been reported as extinct (RastegarPouyani et al., 2005; IUCN, 2013).

Habitat

This species inhabits spring-fed streams, pools and stone troughs at 500-1,430 m altitude. The streams are mostly surrounded by arid scrubland (Schultschik & Steinfartz, 1996; IUCN, 2013). It is unclear where the animals spend the summer and winter months (Schmidtler & Schmidtler, 1975). There is an extensive cave system below the mountain range and Schultschik (2013d) suggested that the newts spend the greater part of the year there. The data are insufficient to support this assumption in general (Torki, 2012; Schneider & Schneider, 2013).

Behaviour

Activity probably starts in December-January, when the rain is falling. Adults disappear from the streams after reproduction in March-April when the temperature rises and water bodies dry up. At higher altitudes with cooler climatic conditions, the reproductive cycle starts and ends later. Reproductive behaviour was studied in captive specimens of Neurergus kaiseri originating from Shahbazan, Iran. The male takes up position in front of the female, from where he starts a 261

tail-fanning display, fanning his tail in the direction of her snout. If the female is responsive and approaches the male, he turns away and creeps ahead of her, his tail making undulating movements. The female follows him, touching his tail. The male deposits a spermatophore, moves forward and makes a 90° turn, bringing him back into a position perpendicular to the female’s body. He stops (‘brakes’) the female in her progress at a point when her cloaca is situated above the place where the spermatophore was deposited. This behaviour is similar in N. strauchii, N. crocatus and N. kaiseri. Observations on N. derjugini are fragmentary. This courtship behaviour is generally similar to that of the small European pond-breeding newts and of Asian Cynops, Pachytriton and Paramesotriton (Sparreboom et al., 2000).

Threats and conservation

Habitat loss resulting from timber extraction for small-scale subsistence use, coupled with the effects of severe droughts, are the major threats to this species. Given its rarity, collection for the pet trade could in principle be a serious threat. It is listed as Critically Endangered (IUCN, 2013), but the degree of endangerment is debatable (Torki, 2012; Schneider & Schneider, 2013). The Zagros Newt was added to Appendix 1 of CITES in 2010 (Schultschik, 2013d).

Observations in captivity

Neurergus kaiseri has been bred in captivity up to the fourth generation (Steinfartz & Schultschik, 1997; Schultschik, 2013d; Pasmans et al., in press)

but it is sensitive, and rearing the juveniles has proved difficult. This species requires higher water temperatures than other Neurergus species. The newts stop feeding and remain in their hiding places at temperatures below 18°C. Temperatures around 24°C prompt oviposition. The newts are strictly nocturnal and shy away from light., They live partly in water, partly on land throughout the year. The observations on courtship, oviposition and larval development reported above were obtained from captive animals.

Comments

An enigmatic species, much of whose natural history is still unknown. Neurergus kaiseri larvae, with their long and relatively high tail-fin, seem to be more adapted to still water than the larvae of the other, stream-dwelling, Neurergus species. The eggs are smaller than in the other species, which may also indicate pond-breeding habits. For this reason N. kaiseri has been termed a pond-breeder (Steinfartz et al., 2002), but observations in the wild are lacking. The elongated form of the female cloaca is most likely an adaptation to egglaying in running water, similar to Euproctus platycephalus and Paramesotriton caudopunctatus.

References

IUCN (2013); Pasmans et al. (in press); Rastegar-Pouyani

et al. (2005); Schmidtler & Schmidtler (1975); Schneider & Schneider (2013); Schultschik (2013d); Schultschik & Steinfartz (1996); Sharifi et al. (2008, 2012, 2013); Sparreboom et al. (2000); Steinfartz et al. (2002); Steinfartz & Schultschik (1997), Torki (2012).

Neurergus strauchii (Steindachner, 1887) | Anatolia Newt Description

A slender, large-bodied newt. Head flattened, longer than wide. Snout rounded. Paratoids not prominent; gular fold present. Trunk almost round, rather slender, without dorsal ridge, but with slight vertebral depression. Lungs reduced. Tail almost as long as snout-vent length, rounded at the base, compressed laterally toward the tip (Schmidtler & Schmidtler, 1970). The tail is relatively shorter in the male than in the female (Pasmans et al., 2006). Tail-tip blunt. Moderately developed tail-fins on dorsal and ventral sides; dorsal tail-fin a little higher, especially in the breeding season. Limbs welldeveloped and only just touching when adpressed (Schmidtler & Schmidtler, 1970). Skin of dorsal side granular and wrinkled, with small, scattered warts. In the terrestrial phase, the skin is dry and rough, not shiny as in Salamandra. Ventral side smooth.

Neurergus strauchii, Malatya Prov. Photo: Max Sparreboom. 262

Salamanders of the Old World | Neurergus

Dorsal colour dark brown to black with many small, yelloworange, rounded, irregular spots. Similar spots on the sides of

Neurergus strauchii, larva. Photo: Sergé Bogaerts.

Diagnosis Neurergus strauchii, adults and subadults found under a stone on land, Malatya Prov. Photo: Max Sparreboom.

Smaller and more numerous yellow dorsal spots than in Neurergus crocatus; on ventral side a continuous or interrupted orange line. Male with silver-blue spots along the tail in breeding season.

Eggs and larvae the tail. Black colour of the sides partly extends onto the belly, reducing the orange-red colouration of the vent to a narrow line. Throat black with orange lining and often yellow spots. Ventral surface of the limbs grey-black. Cloaca half rounded in the male, swollen in the breeding season, with a longitudinal slit. Cloaca slightly conical in the female with a rounded opening, less protruding than in Neurergus crocatus (Schmidtler & Schmidtler, 1975). Male N. strauchii develop silver-blue spots along the tail, sometimes forming a stripe. Total length 16-19 cm (Schmidtler & Schmidtler, 1975). Two subspecies have been described: Neurergus s. strauchii (Steindachner, 1887) from the Lake Van area (Schmidtler & Schmidtler, 1970); and N. s. barani Öz, 1994, from the mountains near the city of Malatya (Öz, 1994), this form being characterised by a lower number of dorsal yellow spots. The number of spots in N. strauchii follows a west-east cline, with specimens from populations of N. s. barani having the lowest number of spots, followed by a steady increase in the more eastern populations of N. s. strauchii. No differences were noted in belly patterns between the two forms: both show either a continuous or interrupted orange ventral line (Pasmans et al., 2006). Genetically the two forms appear not to be differentiated enough to represent distinct evolutionary lineages (Özdemir et al., 2009).

Oviposition starts end April, continuing until May, sometimes later (Schmidtler, 1994; Steinfartz & Schultschik, 1997; Pasmans et al., 2006). Eggs are laid in clutches of 70-110 on the lower surface of stones in mountain streams. Bogaerts et al. (2012) report a maximum of 285 eggs. Jelly capsule is 5-6 mm in diameter, embryo diameter 2.5 mm (Schmidtler & Schmidtler, 1970). Eggs are joined in a jelly string. Larvae hatch after about one month, at a length of 13-15 mm, at water temperatures between 12-18°C (Fleck, 1984). Larvae have a slender body-form, but are stockier than larvae of Neurergus crocatus. The dorsal tail-fin reaches almost onto the middle of the body. Tail-tip rounded. Short gills. Younger larvae are grey with a dense cover of tiny black dots, while older larvae have light spots in two rows along the back and two irregular rows of grey-black spots on the belly. Tail of older larvae densely pigmented black-brown. For comparative larval morphology of N. crocatus and N. strauchii, see Schmidtler & Schmidtler (1975) and Steinfartz (1995). Metamorphosis takes place after 7-8 months at a length of 60-70 mm (Steinfartz, 1995) or after 4-5 months at a length of 50-55 mm (Fleck, 1984). Metamorphosis may be postponed till after winter (Schmidtler, 1994). In captive-bred animals sexual maturity is reached after two or 3-4 years (Haker, 1986; Schultschik, 2013e).

Distribution

Neurergus s. strauchii occurs in the Lake Van area and localities west of Lake Van, Turkey (Pasmans et al., 2006). Neurergus s. barani is only known from the Kubbe Mountains near the city of Malatya (Öz, 1994). New discoveries 263

of this species are gradually filling the gap between the eastern and western localities (Özdemir et al., 2009).

Habitat

This species inhabits perennial, rocky mountain streams, with stretches of calmer water, at altitudes between 950-1,800 m. The borders of the streams may or may not have some vegetation. Terrestrial habitats are always situated in rocky areas with a modest shrub layer and a few trees (Bogaerts et al., 2006).

Behaviour

These animals spend the winter months on land under stones and in burrows (Schmidtler & Schmidtler, 1970), probably from October to the end of March. Breeding takes place in mountain streams, starting at the end of April when the snow is melting (Steinfartz & Schultschik, 1997; Bogaerts et al., 2010). Their diet consists of soft-bodied invertebrates, and aquatic and terrestrial insects (Baran & Atatür, 1998).

The range of Neurergus strauchii.

Reproductive behaviour was studied in captive specimens of Neurergus s. barani, originating from the type locality near Malatya, central Anatolia. The male takes up a position in front of the female, from where he starts a tail-fanning display, fanning his tail in the direction of her snout. By moving forward towards the male the female signals that she is responsive. The male makes a few steps backward, then turns away from the female and creeps ahead of her, his tail making undulating

Neurergus strauchii, breeding habitat, Kubbe Mountain, Malatya Prov. Photo: Max Sparreboom.

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Salamanders of the Old World | Neurergus

Neurergus strauchii, two males, Kubbe Mt, Malatya Prov. Photo: Max Sparreboom.

movements. The female follows him, touching his tail. The male deposits a spermatophore, moves forward and makes a 90° turn, bringing him back into a position perpendicular to the female’s body. He stops (brakes) the female in her progress at a point when her cloaca is situated above the place where the spermatophore was deposited. This behaviour is similar in N. strauchii, N. crocatus and N. kaiseri. Observations of N. derjugini are fragmentary. This courtship behaviour is generally similar to that of the small European pond-breeding newts and of Asian Cynops, Pachytriton and Paramesotriton (Sparreboom et al., 2000).

Threats and conservation

This species may be locally common where suitable habitat is present. It is considered to be relatively susceptible to habitat change, habitat loss, pollution, drought and collection for the pet trade. Although strictly protected by the Convention on the Conservation of European Wildlife and Natural Habitats (the Bern Convention), the status of Neurergus strauchii in Turkey is not clear (Bogaerts et al., 2006; Pasmans et al., 2006). It is listed as Vulnerable (IUCN, 2013).

Observations in captivity

Neurergus strauchii has been successfully bred in captivity (Fleck, 1984; Haker, 1986;

Courtship behaviour in the Anatolia Newt (Neurergus strauchii barani) in the spermatophore transfer phase. After depositing a spermatophore on the substrate in front of the female, the male creeps on approximately one body length ahead of the female. He pivots about one fore leg, making a 90° turn so that he comes to stand in a position perpendicular to the female’s body with his tail folded back and making slow worm-like movements. Art: Bas Teunis, from Sparreboom et al., 2000.

Stein fartz, 1995; Bogaerts et al., 2012; Schultschik, 2013e). The newts should be kept in tanks with cool (12-16°C in the egg-laying season) and running water, providing enough hiding places with flat stones. In captivity the animals can be kept in water all year round but allowing a terrestrial phase is more natural, although both strategies have led to successful breeding. The data on eggs and larvae, and the observations on courtship and oviposition reported above were obtained mainly from captive animals. Neurergus strauchii has been captive-bred to the F5 generation. The results of several longterm breeding projects have been usefully summarised by Bogaerts et al. (2012).

Comments

For earlier literature see Freytag (1957) and Schmidtler & Schmidtler (1970).

References

Baran & Atatür (1998); Bogaerts et al. (2006, 2010, 2012);

Fleck (1984); Freytag (1957); Haker (1986); IUCN (2013); Öz (1994); Özdemir et al. (2009); Pasmans et al. (2006); Schmidtler (1994); Schmidtler & Schmidtler (1970, 1975); Schultschik (2013e); Sparreboom et al. (2000); Steinfartz (1995); Steinfartz & Schultschik (1997).

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Ommatotriton Gray, 1850 After genetic studies had shown that the European newt genus Triturus was not monophyletic (Weisrock et al., 2006; Steinfartz et al., 2007), new genus names have been introduced to cover the newt taxa formerly included in it. The Banded Newt (Triturus vittatus) was placed in the genus Ommatotriton (Gray, 1850) by Litvinchuk et al., (2005), the small-bodied newts were placed in Lissotriton, and the large-bodied newts remained in Triturus. Ommatotriton is the sister taxon of Neurergus (Steinfartz et al., 2007; Pyron &

Wiens, 2011). The genus contains two closely related and morphologically similar species, with widely divergent distributions.

Ommatotriton ophryticus (Berthold, 1846) Ommatotriton vittatus (Gray, 1835)

References

Litvinchuk et al. (2005); Pyron & Wiens (2011) ;

Steinfartz et al. (2007); Weisrock et al. (2006).

Ommatotriton ophryticus (Berthold, 1846) | Northern Banded Newt Description

266

A medium- to large-bodied newt. Head longer than wide, snout rounded. Large eyes. Labial folds well-developed during the aquatic stage. Paratoid glands lacking. Gular fold present, sometimes indistinct. Body rather robust, trunk rounded, more slender in the male. Tail flattened, a little longer or as long as the rest of the body and with pointed tip. Male in breeding condition has a high, denticulated dorsal crest, measuring up to 45 mm high. It begins on the head and is separated from the tail crest by a deep indentation. There is a crest on both the upper- and underside of the tail. Spikes on the tail crests are less high and pointed than on dorsal crest. The female lacks crests, but has a low, straight vertebral ridge and caudal ridges. Toes and fingers are flattened, elongated in the male and without webbing. On the hindlimb the male has a well-developed metatarsal skin fold. The cloaca of the breeding male is swollen and rounded (Thorn, 1969).

In both sexes the skin is smooth in the aquatic stage, and dry, finely granulated, and velvety during the terrestrial stage.

Ommatotriton ophryticus nesterovi, male, Adapazari, Turkey. Photo: Max Sparreboom.

Ommatotriton ophryticus ophryticus, female, NE Turkey. Photo: Max Sparreboom.

Female Ommatotriton ophryticus are much drabber in appearance and lack the crest, conspicuous colour patterns, swollen cloaca, metatarsal skin folds and toe-flaps of males.

spots, the sides are sometimes slightly spotted. Throat and chest have dark grey spots. Young individuals have a yellowish vertebral line (Thorn, 1969).

Salamanders of the Old World | Ommatotriton

Upperparts of the male in breeding dress brown to greenish with numerous dark spots; colour of the female and male outside breeding season olive-green or brown with small dark spots. Dorsal crest of the male with alternating light- and darkcoloured vertical bars. On the sides a longitudinal, silver-white band, bordered on both sides with a black line. The sides of the tail of the breeding male have a whitish or greenish-blue flash. Underside orange to red-orange, in the middle often without

Total length 12-14.5 cm. Males are larger than females and may reach a maximum length of 17-18 cm (Arntzen & Olgun, 2000; Borkin et al., 2003). The western form (O. o. nesterovi) is smaller than the eastern form (O. o. ophryticus) (Cicek et al., 2011). Two subspecies are recognised within O. ophryticus, a western group of populations from northwestern Anatolia (O. o. nesterovi Litvinchuk, Zuiderwijk, Borkin & Rosanov, 2005) and an eastern group, occurring in the remaining part of Pontic Turkey and western Caucasus (O. o. ophryticus (Berthold, 1846 and Litvinchuk et al., 2005, respectively). They differ in genome size and the number of trunk vertebrae (modal number of 12 in the western and 13 in the eastern group) and show geographic variation in allozymes (Arntzen & Olgun, 2000; Litvinchuk et al., 2005; Lanza et al., 2010).

(maximum 10) in a lowland population and eight (maximum 16) in a population at higher elevation. According to Tarkhnishvili & Gokhelashvili (1999), in the Caucasus sexual maturity may be reached after three (males) or four years (females), most males maturing after five, and females after six, hibernations. The oldest males recorded were 12 years old, and the oldest females 21 years.

Diagnosis

A medium- to large-bodied newt. Straight white band along the flanks, lined with black, underside often without spots. Males with high, conspicuously spiked dorsal and caudal crest in the breeding season. The male has long, thin toes with thin flaps of skin surrounding them.

Eggs and larvae

Females attach their eggs singly to leaves or other objects at a water depth of 5-30 cm, with the highest density of eggs found at a depth of 20-30 cm. A clutch may consist of hundreds of eggs; between 9-221 (Tarkhnishvili & Gokhelashvili, 1999) per female with an average of 90-100 (Borkin et al., 2003). Each egg measures 3-4 mm in diameter including capsule, and 1.5-1.8 mm in diameter without capsule. Larvae measure 7-8 mm at hatching, and newly metamorphosed juveniles are 29-44 mm. The larva is similar to that of Lissotriton vulgaris, but differs in having a smaller eye in relation to the distance between the nostrils, light spots behind the eyes, and irregularly-shaped, light dorsal spots (Kuzmin, 1999). Embryonic development takes 12-30 days, depending on temperature, and metamorphosis is completed in July-September, after 70-150 days (Kuzmin, 1999). At higher temperatures larvae can complete metamorphosis in 1.5 months (Borkin et al., 2003). Growth rates of Ommatotriton ophryticus larvae are more susceptible to change in environmental conditions than those of other newt species. In unfavourable conditions, they grow much more slowly than either L. vulgaris or Triturus karelinii larvae, whereas in optimal conditions growth is much faster. Larvae may occasionally overwinter in slow-running mountain streams and metamorphose in the following spring. Neoteny has not been observed in the Caucasus (Tarkhnishvili & Gokhelashvili, 1999), but paedomorphic newts have been recorded in Turkish populations (Kaya et al., 2008; Baskale et al., 2011, 2013). Kutrup et al. (2005) found that the mean age of breeding newts in two populations in northeastern Turkey was four years

The range of Ommatotriton ophryticus.

Distribution

The range of Ommatotriton ophryticus extends from north-western Anatolian Turkey, along the southern Black Sea coast, to the western part of the Caucasus, reaching eastern Georgia and Krasnodar Territory in Russia (Tarkhnishvili & Gokhelashvili, 1999; Borkin et al., 2003; Litvinchuk et al., 2005; Cicek et al., 2011).

Habitat

Ommatotriton ophryticus inhabits forest landscapes, from dry Oriental Hornbeam (Carpinus orientalis) forests in eastern Georgia, to humid, mixed and deciduous forests at the Black Sea coast. It is found from sea level up to 2,743 m, its optimal elevation range being 600-1,700 m. These newts are most abundant in small lakes and ponds on grassland patches surrounded by forest. They are also found in slow-running water bodies on subalpine meadows and in slow-running forest 267

pools. Their distribution is limited by the 600 mm annual rainfall isoline. This species appears to be more closely associated with humidity than its sister species, O. vittatus, which can also be found in xeric habitats (Tarkhnishvili & Gokhelashvili, 1999).

Ommatotriton ophryticus nesterovi, habitat, Adapazari, Turkey. Photo: J.W. Arntzen.

Behaviour

Ommatotriton ophryticus usually overwinters on land, under logs, in burrows and rotten trees, often in groups. Hibernation may also take place in water in small springs, especially in the western Caucasus. Along the Black Sea coast, these newts can remain active throughout the winter and appear at the breeding waters at the end of November. In eastern Georgia, the first male newts appear at breeding sites in late March. Mass migration occurs at the beginning of April, during the first April rains. They are mainly active at night during the terrestrial stage. In the aquatic phase, both larvae and adults are active day and night, although the larvae are most active during the first three hours of the morning, when temperatures drop to around 14°C (Tarkhnishvili & Gokhelashvili, 1999). Adult newts in the aquatic phase eat both benthic organisms and invertebrates living among aquatic plants. The main component of the diet of males is aquatic snails (family Planorbidae). The eggs of amphibians comprise about 50% of the diet of adult females, including those of conspecifics. On land, insect larvae predominate in the diet (Tarkhnishvili & Gokhelashvili, 1999).

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These newts are taken by a wide range of predators, such as Grass Snakes (Natrix natrix) and Marsh Frogs (Pelophylax ridibundus). Males enter the breeding waters first and develop their breeding dress over a period of one week to one month, after which reproductive activity starts (Borkin et al., 2003). Females enter the breeding sites later than males and leave the water 2-3 weeks after spawning. Males in breeding condition space themselves out over the breeding pond. If an individual male comes too close, and within sight of another male, a fierce territorial combat results, in which legs may be bitten off, wounds may be inflicted in the cloacal region, and one of the rivals may even be killed (Raxworthy, 1989; Arntzen & Sparreboom, 1989; Tarkhnishvili & Gokhelashvili, 1999). This kind of aggression is only shown towards conspecific males. The following description is derived from Raxworthy (1989). When a female comes within sight of a male, he slowly waves his tail, and then rushes forward to the front of the female by rapid swimming to take up a display posture. The body of the male is arched dorso-ventrally in what has been named a cat buckle display and the body is leaned in towards the female so that sometimes his crest may flap partly over her. The tail is bent towards the female and rapidly vibrated at the tip in what has been termed the flurry display. This vibration involves only the tail-tip, which is vibrated while turned away from the female. During this flurry the male raises his hind legs off the substrate and pivots on the inner front leg, the one closest to the female, so that his body and tail lean in and swing slowly towards the female. Each bout of tail-flurry is terminated by a strong lash of the tail, named the whip. The force of the whip is so strong that it often displaces both the male and the female. After performing the whip the male quickly returns to his display posture in front of the female and repeats his courtship movements. If the female is responsive she first remains motionless. Once she has been subjected to several flurry/whip bouts she starts moving towards the cloaca of the male and her cloaca starts to evert downwards. The male turns round and goes into sperm transfer phase. He deposits a spermatophore in front of the female and creeps on ahead of her. After proceeding about one body length he pivots through 90° to block the path of the following female in a posture called ‘brake’. If the sperm cap of the spermatophore makes contact with the cloaca lips, it adheres and is drawn into the cloaca. Following the ‘brake’, the male may then either make a breathing ascent or start to display again to this or another female (Raxworthy, 1989). The female can start laying eggs within several hours after mating (Tarkhnishvili & Gokhelashvili, 1999).

Threats and conservation

Populations of Ommatotriton ophryticus suffer anthropogenic pressure through deforestation

and uncontrolled introduction of fish into their breeding sites. In the western Caucasus the species is threatened by predation from the introduced raccoon (Procyon lotor). In the sub-alpine belt, an important threat is overgrazing by cattle, which accelerates eutrophication of small water bodies (Tarkhnishvili & Gokhelashvili, 1999). In the Caucasus it is also threatened by collection for the pet trade. The species is listed in the Red Data Books of the USSR, Russia and Georgia and described as Near Threatened (IUCN, 2013).

Observations in captivity

The Banded Newt has been kept and bred in captivity for years (Lantz, 1912; Oeser, 1951; Thorn, 1969; Haker, 1974; Schmidtler, 1977; Diesener, 1982; Golovanov & Raffaëlli, 1983; Raffaëlli, 2007; Pasmans et al., 2008). After the breeding period, the animals always leave the water and should be offered the opportunity to live on land. Terrestrial refuges should be relatively dry, not wet or soggy. Temperatures of 5-6°C in winter are necessary to bring the animals into breeding condition. Juveniles live on land and only enter the water

once they are sexually mature. The species is sensitive to stress and unfavourable conditions. In particular, care should be taken to keep only one male in an aquarium. Males in breeding condition are extremely aggressive and will fight to the death.

Comments

The natural history of Ommatotriton ophryticus is the subject of a thorough review in the Handbuch der Reptilien und Amphibien Europas (Borkin et al., 2003) and in The Amphibians of the Caucasus (Tarkhnishvili & Gokhelashvili, 1999). The evolution of the male dorsal crest, such a spectacular feature of this species, is addressed by Wiens et al. (2011).

References

Arntzen & Olgun (2000); Arntzen & Sparreboom

(1989); Baskale et al. (2011, 2013); Borkin et al. (2003); Cicek et al. (2011); Diesener (1982); Golovanov & Raffaëlli (1983); Haker (1974); IUCN (2013); Kaya et al. (2008); Kutrup et al. (2005); Kuzmin (1999); Lantz (1912); Lanza et al. (2010); Litvinchuk et al. (2005); Oeser (1951); Pasmans et al. (2008); Raffaëlli (2007); Raxworthy (1989); Schmidtler (1977); Tarkhnishvili & Gokhelashvili (1999); Thorn (1969); Wiens et al. (2011).

Ommatotriton vittatus (Gray, 1835) | Southern Banded Newt Description

A small-bodied newt. Very similar to Ommatotriton ophryticus, which has long been considered a subspecies of O. vittatus. White band along the body is relatively broad. Often small dark spots on ventral side (Thorn, 1969). Total length 8-10 cm, up to 12-13 cm maximum (Thorn, 1969).

Several subspecies have been named within O. vittatus, but there is no consensus on their validity. The debate has focused

on the differences between the form described as O. v. cilicensis, from the region round Adana, Turkey, and the nominate form O. v. vittatus from more southern parts of the species’ range. Ommatotriton v. cilicensis is supposed to have 14 or more spikes in the male dorsal crest and a discontinuous lower dark lateral stripe, while the upper lateral stripe may also be interrupted. It occurs from the province of Icel, Turkey, on the Mediterranean coast, to the area round Ceyianplnar on the Mesopotamian plain in south-eastern Turkey (Franzen, 2001). The nominate

Ommatotriton vittatus, male, W of Al Qadmus, Syria. Photo: Max Sparreboom. 269

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Ommatotriton vittatus, female, W of Al Qadmus, Syria. Photo: Max Sparreboom. ◀

Ommatotriton vitattus, male, E of Al Haffah, Syria. Photo: Max Sparreboom.

form, O. v. vittatus, typically has 14 or fewer spikes in the crest and a continuous upper dark lateral stripe, while the lower lateral stripe may be interrupted (Franzen & Schmidtler, 1997; Olgun et al., 1997). The nominate form occurs from Gaziantep Province in Turkey, east of the Amanus mountain range, down to Israel. The genetic differentiation between the two forms is similar to that between the two forms of O. ophryticus (Arntzen & Olgun, 2000), which has been divided into two subspecies. Borkin et al. (2003) list some more morphological differences but leave the question of subspecific status open.

Distribution

Ommatotriton vittatus occurs from southeastern Turkey, through western Syria, Lebanon, north-western Jordan to Israel (the southern limit being the southern Coastal Plain of Ashkelon) and parts of the Palestine Territories (IUCN, 2013; Borkin et al., 2003). This distribution is mainly shaped by levels of precipitation, both in summer and in winter (Bogaerts et al., 2013).

Diagnosis

A small-sized newt. Straight white band along the flanks, lined with a black, continuous or interrupted, stripe. Underside sometimes spotted. Males with conspicuously spiked, high dorsal and caudal crests in the breeding season. The male has long, thin toes. Ommatotriton vittatus is smaller in body size than the eastern form of its sister species, O. ophryticus. The dorsal crest of a male in full breeding condition can be as high and spiked as in O. ophryticus.

Eggs and larvae

Females attach their eggs singly to leaves, grasses or other objects. In populations in Israel, where the species has been studied for years, a clutch may consist of 18-68 eggs. Most eggs are laid near the sides of a pond at water depths of 5-30 cm. The egg including capsule is 3-4.1 mm in diameter, and 1.5-1.9 mm in diameter without capsules. The larvae are 7.3-12.0 mm at hatching and newly metamorphosed juveniles are 17.8-44.8 mm long. In Israeli populations larvae may grow considerably larger, up to 69 mm (Borkin et al., 2003). Larval development has been documented by StettinerKallner (1962). Variation in larval growth and timing of metamorphosis allows Ommatotriton vittatus to adapt to fluctuating breeding conditions (Pearlson & Degani, 2011).

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Salamanders of the Old World | Ommatotriton

The range of Ommatotriton vittatus.

Habitat

Ommatotriton vittatus inhabits coniferous, mixed and deciduous forests up to sub-alpine meadows. Breeding sites consist of lakes, ponds, temporary puddles, drainage canals, roadside ditches in meadows, slow-flowing streams and stream pools in open areas (IUCN, 2013). In the breeding season, the species occurs in rainpools in the central coastal plain of Israel and in Upper Galilee (Geffen et al., 1987) and in rain-flooded areas, temporary and permanent ponds, small springs, concrete basins and ditches in Syria (Bogaerts et al., 2013).

It is found from 200 m below sea level up to 2,750 m altitude (IUCN, 2013). It appears to be more closely associated with xeric habitats than its sister species, O. ophryticus, which is more often found in humid habitats (Tarkhnishvili & Gokhelashvili, 1999).

Behaviour

Ommatotriton vittatus usually spends the hot summer on land and underground. In the central coastal plain of Israel they appear on land in November-December following the November rains. As pools fill up, the animals enter the water, where they breed in February. Most leave the water by the end of February. In more northern populations the aquatic stage may last longer and females may remain in the pools until early summer (Degani & Mendelssohn, 1983; Geffen et al., 1987). In western Syria the newts were in full breeding condition in February 2009, and freshly laid eggs were found (Bogaerts et al., 2013). Adult newts in the terrestrial phase prey on snails, isopods, arachnids, myriapods and coleopterans, with land snails being the most important food item. In rainwater pools the predominant food item is ostracods (Geffen et al., 1987). The newts are taken by a wide range of predators, such as grasssnakes (Natrix natrix), Marsh Frogs (Pelophylax ridibundus), crows and ravens (Borkin et al., 2003). Males enter the breeding waters first and develop their crests, colouration and hind leg extensions, after which reproductive activity starts (Borkin et al., 2003). The reproductive behaviour of the sister species O. ophryticus has been studied (Raxworthy, 1989; Arntzen & Sparreboom, 1989). Observations of the courtship of O. vittatus in the wild suggest that its sexual and aggressive behaviour is similar to that of O. ophryticus. Sometimes several males could be seen posturing on the bottom of a pond, carefully seeing to it that a particular distance to their neighbours was maintained. Close encounters resulted in fierce struggles (Bogaerts et al., 2013).

Ommatotriton vittatus, habitat, E of Al Haffah, Syria. Photo: Max Sparreboom.

Threats and conservation

This species is sensitive to habitat loss through forest destruction, destruction of wetlands, overgrazing by cattle, urbanisation, industrial and agrochemical pollution throughout its range. In Israel it is threatened by collection for the pet trade and spraying of pesticides to combat mosquitoes. It is protected by national legislation in Israel. The species is listed as of Least Concern (IUCN, 2013).

Observations in captivity

The Banded Newt has been kept and bred in captivity. Although most reports pertain to Ommatotriton ophryticus, the care of O. vittatus is similar (Pasmans et al., 2008).

Comments

The natural history of Ommatotriton vittatus is the subject of a thorough review in the Handbuch der Reptilien und Amphibien Europas (Borkin et al., 2003). The evolution of the male dorsal crest, such a spectacular feature of this species, is addressed by Wiens et al. (2011).

References

Arntzen & Olgun (2000); Arntzen & Sparreboom

(1989); Bogaerts et al. (2013); Borkin et al. (2003); Degani & Mendelssohn (1983); Franzen (2001); Franzen & Schmidtler (2000); Geffen et al. (1986-87); IUCN (2013); Olgun et al. (1997); Pasmans et al. (2008); Pearlson & Degani (2011); Raxworthy (1989); Stettiner-Kallner (1962); Tarkhnishvili & Gokhelashvili (1999); Thorn (1969); Wiens et al. (2011).

271

Pachytriton Boulenger, 1878 The genus Pachytriton is the most aquatic in the family Salamandridae. Adult Pachytriton live permanently in small, shallow, clean, cold water montane streams and have morphological and osteological specialisations associated with their aquatic habitat (Wu et al., 2012a; 2013). Salamanders of this genus have a smooth skin, a slender body lacking a vertebral ridge, and a tail that is compressed laterally to varying degrees. Skull long and narrow. Where the long maxillary bones approach the pterygoids, the elements form approximately straight lines. Frontosquamosal arch is rarely complete and attenuate if formed. The frontal process of the premaxilla, which is both long and broad, separates the nasals. The hyobranchial apparatus of Pachytriton is unique with the stout, bony epibranchials flaring dorsolaterally and wrapping round the neck, and is highly specialised for aquatic “gape and suck” feeding (Özeti & Wake, 1969). In adult Pachytriton, the tongue is fully attached to the floor of the mouth, as an adaptation for suction feeding, whereas in juveniles the tongue is protrusive and adapted for catching terrestrial prey (Nishikawa et al., 2009). Most specimens have 12 trunk vertebrae (Chan et al., 2001). The genus Pachytriton was previously thought to be related to Calotriton (then Euproctus) asper, sharing anatomical adaptations to life in flowing streams with that species (Herre, 1933; Freytag, 1982b). Molecular studies have now grouped Pachytriton with Laotriton, Cynops and Paramesotriton. It is considered monophyletic (Chan et al., 2001; Weisrock et al., 2006) and most closely related to Laotriton (Zhang et al., 2008). Several

undescribed froms have been reported from the pet trade which on the basis of morphological similarities appeared to belong to Pachytriton (Thiesmeier & Hornberg, 1997; Scholz, 1998). Formerly believed to contain just two species (P. brevipes and P. labiatus), recent molecular work has shown that the genus contains at least seven species. These are hard to distinguish on morphological grounds alone and colouration is not a reliable character for delimiting species boundaries (Wu et al., 2010b). The relationship among the different forms and their distributions is not yet clear. Population- and species-level analysis suggests that monsoon activity and global warming may have played a critical role in shaping the genetic diversity and distributional pattern in Pachytriton (Wu et al., 2013).

Pachytriton archospotus Shen, Shen & Mo, 2008 Pachytriton brevipes (Sauvage, 1876) Pachytriton changi Nishikawa, Matsui & Jiang, 2012 Pachytriton feii Nishikawa, Jiang & Matsui, 2011 Pachytriton granulosus Chang, 1933 Pachytriton inexpectatus Nishikawa, Jiang, Matsui & Mo, 2011 Pachytriton moi Nishikawa, Jiang & Matsui, 2011

References

Chan et al. (2001); Freytag (1982b); Herre (1933);

Nishikawa et al. (2009); Özeti & Wake (1969); Scholz (1998); Thiesmeier & Hornberg (1997); Weisrock et al. (2006); Wu et al. (2010b, 2012a, 2013); Zhang et al. (2008).

Pachytriton archospotus Shen, Shen & Mo, 2008 | Guidong Paddle-Tailed Newt, Guidong Stout Newt

Description

The following description is largely based on Shen et al., (2008). Pachytriton archospotus is a fairly large, slender salamander, similar to P. brevipes. Body stout with smooth skin. Head longer than wide and slightly flattened. Snout blunt. Eyes small. Labial fold prominent. Gular fold present. Osteological features include the presence of a frontosquamosal arch and short straight epibranchial bones. Vertebral ridge absent. When limbs are adpressed, digits do not meet. Tail strong and laterally compressed at the posterior half. Dorsal caudal fin starts from the base of the tail, the ventral caudal fin is only visible at the end of the tail. Dorsal colour is blackish-brown to light brown and the colour may change gradually. Ventral colour is bright orange to pale yellow with dark blotches. Small rounded black spots are scattered around the body; some individuals have few or no black spots.

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Pachytriton archospotus, Guidong County (type locality), SE Hunan. Photo: Zhang Xu.

Total length 144-184 mm in males, 161-211 mm in females.

Diagnosis

Spotted on the back like Pachytriton brevipes, but differs from it in having frontosquamosal arches (although the frontosquamosal arch is also observed in some P. brevipes populations (salamandersofchina.lifedesks.org)). The most striking characteristic that distinguishes P. archospotus from its congeners is the morphology of the hyobranchial apparatus. In P. archospotus, the ceratohyal is placed more anteriorly than it is in other Pachytriton. First and second ceratobranchials are also greatly enlarged such that their distal ends are visible posterior to the skull in dorsal view. Unlike the strongly bowed and flared epibranchial that is characteristic of other Pachytriton, the epibranchial of P. archospotus is straight and rod-like, resembling that of Paramesotriton and Cynops species. Furthermore, P. archospotus lacks the distinct epibranchial flange that is typical of other members of the genus (Wu et al., 2012a). Snout length shorter than interocular space, instead of longer such as in P. brevipes. Head longer than wide. Cloacal area in male is not swollen in breeding season; cloacal papillae are longer than in the other species.

Eggs and larvae

No published information.

The range of Pachytriton archospotus.

Distribution

Apart from the type locality, Qiyunshan, Guidong County, in the southeastern part of Hunan Province, China at 1,250 m altitude, this species has been found in Wugongshan, Jinggangshan and Guanyindong (Wu et al., 2013). Its distributional range was until recently considered to form a part of the range of P. brevipes (Fei et al., 2006). All Pachytriton populations occurring in the Luoxiao mountain range (southeastern Hunan, southwestern Jiangxi and northern Guangdong) are probably P. archospotus (salamandersofchina. lifedesks.org).

Habitat

This species inhabits mountain streams, ranging from 1,000-1,600 m. In Mt. Jinggang it also occurs at approximately 800 m. It lives in streams surrounded by bushes and grassland, and by broad-leaved evergreen and coniferous forest.

Behaviour

The climax of the reproductive period occurs in May. Long term observation by Shen et al. (2008) suggests that two and three year old individuals are too young to reproduce.

Threats and conservation

Populations of this species are probably shrinking due to the disappearance of streams and to deforestation. Local people occasionally put the animals in liquor, thinking this promotes good health.

Observations in captivity

No published information.

Comments

Originally described as a new species on the basis of unique phenotypic features in a geographically distinct population of spotted Pachytriton individuals, the validity of P. archospotus as a distinct species was later confirmed by molecular analyses. Analysis of mitochondrial DNA sequences suggests that P. archospotus is sister to P. brevipes (Wu et al., 2010b).

References

Fei et al. (2006); salamandersofchina.lifedesks.org;

Shen et al. (2008); Wu et al. (2010b, 2012a, 2013).

Pachytriton brevipes (Sauvage, 1876) | Paddle-Tailed Newt,

Black-spotted Stout Newt

Description

A medium- to large-bodied newt. Head flat and large, longer than wide, snout truncated, conspicuous labial folds. Eyes rather small, located at or anterior to the jaw angle.

Paratoid region prominent, another gland situated behind the paratoid. Distinct gular fold. No vertebral ridge, but a slight vertebral groove on the trunk. Two rows of vomerine teeth in 273

coloured animals, spots are more clearly visible than in darker specimens. Ventral side lighter than dorsal and lateral sides, mottled with an irregular mix of red, pink and whitish colours (Thiesmeier & Hornberg, 1997). Size and density of the spots vary among individuals. Some newts lack black spots on the ventral side, and some are entirely spotless (Fei et al., 2006). Sexual dimorphism not pronounced. Cloacal region not much different between the sexes, slightly swollen in the breeding male, with papillae protruding from the cloaca. Breeding males develop one or several bluish-white spots on the distal part of the tail. Total length 155-193 mm in males, 160-185 mm in females (Fei et al., 2006). Pachytriton brevipes, Wuyishan mountain, Fujian. Photo: Hou Mian.

Diagnosis

A stout-bodied newt with smooth skin. Epibranchial bones are elongated and curved, wrapped around the neck. Most literature distinguishes Pachytriton brevipes from P. inexpectatus (formerly named P. labiatus) by the presence of numerous small black spots over the entire body, but spotless populations of P. brevipes are common (Wu et al., 2010b).

Eggs and larvae

Females lay 30-60 eggs, attached to the lower surface of rocks in a stream. Eggs are milky white and form a compact clutch. The ovum is ca. 4.5 mm in diameter and the entire egg, including jelly capsule, reaches a diameter of 7.5 mm (Fei et al., 2006).

Pachytriton brevipes, Wuyishan mountain, Fujian. Photo: Hou Mian.

inverted V-shape, converging anteriorly. Tail strong, a little shorter than snout-vent length, round at the base and compressed at the end with a rounded tip. Caudal fin on upperside of last two thirds of the tail and a low keel on underpart of the entire tail. Fore and hind legs short, with digits not touching when adpressed to the body. Fingers and toes are short and stubby, their tips flat and rounded. Webbing is present at the base of digits in some animals, whereas in others digits are nearly half-webbed. Skin smooth and covered with mucus. Vertical wrinkles on the sides of the body and cross-wrinkles on the vent. Colour different shades of light brown, tan to reddish. Usually small black spots covering entire body, head and tail. In lighter274

Salamanders of the Old World | Pachytriton

The range of Pachytriton brevipes.

Distribution

Pachytriton brevipes occurs in the mountains of southeastern China (Jiangxi, Fujian, Guangdong) (Wu et al., 2013). The precise borders of its range are unknown.

Habitat

This species is associated with montane broadleaf and mixed forests at elevations ranging from 800-1,700 m (Fei et al., 2006). It inhabits streams which may be as small as 1 m wide and 20 cm deep. Large numbers of animals are found in ponds with slow-running water, deeper than 1 m.

Behaviour

The animals are most active at night. During the day the newts rest at the bottom of the stream or hide in crevices. They feed on small prey such as frog tadpoles (Pope, 1931). Pachytriton has a gape and suck feeeding habit specialised for foraging in flowing streamwater. Pachytriton brevipes is aggressive and territorial. The breeding season is from May-August (Fei et al., 2006). Its reproductive behaviour is similar to that described for the species previously named P. labiatus (Thiesmeier & Hornberg, 1997; Sparreboom & Thiesmeier, 1999).

Threats and conservation

This species is collected for human consumption in parts of its range and exported for the international pet market (Fei et al., 2006). Populations are threatened when people poison an entire stream to catch fish. Habitat destruction and degradation also pose threats, but the species is relatively common and presently listed as of Least Concern (IUCN, 2013).

Observations in captivity

Mudrack (1984) reports breeding of this species in an aquarium. Prior to laying eggs, the male was seen biting the female and holding on to her, with vents apposed. This was interpreted as mating behaviour, but other interpretations cannot be excluded. Sixteen eggs, 5 mm in diameter, were laid under a flat stone (Mudrack, 1984). Successful captive breeding of Pachytriton brevipes has not been reported.

In general, aquariums for Pachytriton should have flowing water. Due to this species’ extremely aggressive behaviour, a tank can accommodate only one or two animals and should

contain many hiding places where animals can sit in isolation (Thiesmeier & Hornberg, 1997; Reilley, 2005).

Comments

Pachytriton species of unknown provenance are regularly imported via the pet trade. Various different phenotypes have been recognised among these imported animals. The first, provisionally named Pachytriton A, is characterised by its striking sexual dimorphism. The breeding male has whiteblue colours covering the entire lateral sides of the tail. This form has been bred in captivity and its eggs and larvae have been described (Thiesmeier, 1997; Thiesmeier & Hornberg, 1997, 2000). A single clutch of 84-85 eggs is laid under stones, where the female stays in attendance under the eggs, protecting them against intruders, produces dorsal excretions, and eats any eggs that go bad. After metamorphosis the juvenile newts move onto land. The granular skin and the pronounced belly colouration of the juvenile newt are striking, and resemble juvenile Cynops. Another phenotype, named Pachytriton B, lacks the small black spots on dorsal and lateral sides. Instead it has minute light speckles on a uniform brown colour; orange spots that may form dorso-lateral bands; and a belly with large orange patches. This form was later described as P. xanthospilos from Mt. Mang, near the border between Hunan and Guangdong Provinces (Wu et al., 2012b) and subsequently synonymised with P. changi, which was described only slightly earlier on the basis of two specimens from the pet trade (Nishikawa et al., 2012, 2013b). A third form was described provisionally as Pachytriton C on the basis of its skeletal features (Scholz, 1998). This form is characterised by a rough leathery skin and clouded colouration. This animal was later identified as a thus far unknown species of Paramesotriton and was described as a new species, Paramesotriton ermizhaoi from the Guangxi Zhuang Autonomous Region (Wu et al., 2009). This species was later synonymised with Paramesotriton labiatus (Nishikawa et al., 2011b). It was captive-bred by Henk Wallays.

References

Fei et al. (2006); IUCN (2013); Mudrack (1984); Nishikawa

et al. (2011b, 2012, 2013b); Pope (1931); Reilley (2005); Scholz (1998); Sparreboom & Thiesmeier (1999); Thiesmeier (1997); Thiesmeier & Hornberg (1997, 2000); Wu et al. (2009, 2010b, 2012b, 2013).

Pachytriton changi Nishikawa, Matsui & Jiang, 2012 | Chang’s Stout Newt Description

The following account is based on two recent descriptions, which appeared almost simultaneously. Wu et al., 2012b described this new species as Pachytriton xanthospilos on the basis of specimens from Mt. Mang, Mangshan National Forest Park, near the border between Hunan and Guangdong Provinces, China. Nishikawa et al., 2012 described the species as

Pachytriton changi, on the basis of two specimens from the pet trade. Using genetic and morphological evidence, Nishikawa et al. (2013b) concluded that the animals belonged to the same species and decided that P. xanthospilos was a subjective junior synonym of Pachytriton changi, and that the latter name should be formally recognised. 275

choanae and extend posteriorly into the oral cavity. Paratoids prominent. Gular fold present but inconspicuous. Skin very smooth. Vertebral groove present along the dorsal midline. A few longitudinal wrinkles on throat, and numerous transverse wrinkles on flanks and venter. Limbs very short; digits remain well separated when fore- and hindlimbs are adpressed against flank. Four fingers and five toes, with limited webbing at base of digits. Tail highly laterally compressed. Prominent dorsal caudal fin extends from tail-base to tail-tip. Ventral caudal fin conspicuous. Tail-tip rounded. Cloaca small and not swollen. In life, the colour of the dorsum is uniformly dark brown, venter lighter brown with large, irregular, orange blotches. Orange spots present along dorsolateral flanks, most conspicuous near pectoral and pelvic regions. Underside of tail and cloaca light orange. Total length 16- 17 cm.

Diagnosis

This species can be diagnosed from congeners by the following combination of characters: body size large and very robust; dorsal colour uniformly brown to light brown; large bright-orange spots or blotches extend ribbon-like dorsolaterally in most specimens; and orange blotches sometimes present on head and dorsum. It lacks the black spots of Pachytriton archospotus and P. brevipes; it has a longer series of upper jaw and vomerine teeth compared with P. feii; and it is larger than P. granulosus and has a longer snout. It differs from P. inexpectatus and P. moi by having a smaller body, narrower head, and longer, thinner tail.

Pachytriton changi, from Mangshan National Forest Park, near the border between Hunan and Guangdong (type locality of P. xanthospilos, synonym of P. changi). Photos: Hou Mian.

A moderate-sized newt. Head flat and oval to rectangular. Head width measured at the posterior angle of the jaw almost equals width measured at the paratoid gland. Head much longer than wide. Snout truncate, projecting slightly beyond mandible. Nostril at snout tip. Eyes very small and not bulging. Labial fold prominent on upper jaw. Tongue pad elliptical, poorly differentiated from the mouth floor. Posterior tip of maxillary bone contacts pterygoid lobe; the two bones are arrayed in an approximately straight line. Vomerine teeth inverted V-shaped. Tooth rows converge anteriorly at the anterior limit of the internal 276

Salamanders of the Old World | Pachytriton

The range of Pachytriton changi.

Eggs and larvae

No published information.

Distribution

Pachytriton changi is known from Mt. Mang in the Mangshan National Forest Park, China and very likely also occurs in the nearby mountains of the Guangdong Nanling National Forest Park. Those mountains are located in the middle-to-eastern section of the Nanling Mountain Range. The precise borders of its range are unknown.

Habitat

This species occurs in montane streams at elevations above 800 m. These streams are covered by canopies of lush broadleaf forest, with a flourishing understorey of dense bushes and bamboos. Tall grasses grow along the adjacent stream banks. Streams are about 2-3 m wide and 0.5-1 m in depth, with cold, clear water. Large boulders are scattered in the streams or

on the banks. The salamanders are usually found in pools along the stream, where the water current is slow (Wu et al., 2012b).

Behaviour

This species is most active at night, but can be seen resting at the bottom of pools during the day.

Threats and conservation

Pachytriton changi is frequently collected illegally and has recently suffered from habitat destruction due to tourism. Wu et al. (2012b) regard the species as Near Threatened.

Observations in captivity

There are no reports of this

species being kept in captivity.

References

Nishikawa et al. (2012, 2013b); Wu et al. (2012b).

Pachytriton feii Nishikawa, Jiang & Matsui, 2011 | Fei’s Stout Newt Description

This is a summary of the original description by Nishikawa et al. (2011a). Pachytriton feii is a relatively small-sized Pachytriton with a flat, slender body. Skin smooth. Head oval in shape, depressed and nearly flat in profile. Snout truncate, slightly extending over lower jaw. Nostrils close to snout tip. Labial fold evident. Skull narrow. Maxillary connecting with pterygoid, forming a nearly straight line. Fronto-squamosal arch complete, but not robust. Epibranchial relatively short, wrapping the neck dorsolaterally. Vomerine tooth series long, with an inverted V-shape, tooth rows converging anteriorly, slightly exceeding anterior limit of choanae. Tongue fully attached to mouth floor. Paratoids evident. Gular fold present but weak. No vertebral or dorsolateral ridges. 11 costal grooves between axilla and groin. Adpressed limbs separated by 1.5 costal folds. Number of trunk

vertebrae 12. Fingers and toes without webbing. Tail laterally compressed, dorsal fin evident posteriorly. Colour of the back uniformly dark brown. Venter lighter, with reddish-orange markings. Markings diffuse in adults but brighter and more sharply delineated in juveniles. Underside of tail and cloaca light orange. Total length on average 17-18 cm, with males slightly smaller than females. Fei et al. (2012) give 16.7-19.8 cm for females, 14.7-19.0 cm for males.

Diagnosis

A moderate-sized Pachytriton, uniformly dark brown above, usually without bright orange dots along dorso-

Pachytriton feii, living specimen from type series. Photo: Masafumi Matsui. 277

lateral region in adults; no black spots over the body. Most similar to P. granulosus, but with wider head, longer snout and limbs, larger eyes, thinner tail, and wider vomerine tooth series.

Eggs and larvae

No published information.

Distribution

Pachytriton feii is known from Mt. Huang in southern Anhui Province, China. The precise borders of its range are unknown.

Habitat

This species is common in streams and their branches on Mt. Huang above ca. 600 m altitude.

Behaviour

This species is mainly nocturnal, but can also be found in daytime during cloudy or rainy weather. The breeding season is from late spring to early summer.

References

Fei et al. (2012); Nishikawa et al. (2011a).

The range of Pachytriton feii.

Pachytriton granulosus Chang, 1933 | Northeastern Paddle-Tailed Newt, Spotless Stout Newt

Description

A moderately large, slender salamander. Similar to Pachytriton inexpectatus, with which it was formerly considered identical, and long known as P. labiatus. See comments section of P. inexpectatus.

brown, sometimes with red spots or dorso-lateral orange stripes. No small black spots on body, head and tail. Distinct red and black colouration on the belly. Similar to Pachytriton inexpectatus, but smaller and with narrower head (Nishikawa et al., 2011b). The original description applies to a juvenile male, total length 87 mm, from a stream in Jietouzhen, Tiantai City, Zhejiang Province, China. External characteristics were noted as: no dorsal ridge; numerous minute granules on skin; and orangered spots along the body sides (Chang, 1933).

Eggs and larvae

Probably similar to Pachytriton

inexpectatus.

Distribution

This species occurs in Zhejiang, southern Anhui, southern Jiangsu, northern Jiangxi and Fujian Provinces, China. (Nishikawa et al., 2011b; Fei et al., 2012; Wu et al., 2013).

Habitat Pachytriton granulosus. Photo: Kanto Nishikawa.

Diagnosis

A moderately large-bodied newt with smooth skin and rectangular-shaped head. Colour of the back uniform

278

Salamanders of the Old World | Pachytriton

Pachytriton granulosus inhabits mountain streams of varying sizes, where it lives a mainly aquatic life. Small juveniles are probably terrestrial (Nishikawa et al., 2011b; Thiesmeier & Hornberg, 1998, 2000).

Behaviour

Probably similar to Pachytriton inexpectatus.

pose threats, but the species appears to be relatively common (IUCN, 2013 information for Pachytriton labiatus).

Observations in captivity

See under Pachytriton

inexpectatus.

Comments

The range of Pachytriton granulosus.

Threats and conservation

The species is collected for use in traditional Chinese medicine and exported for the international pet market. Habitat destruction and degradation also

This is a taxonomically problematic species. A small salamander from Zhejiang Province was described by Chang (1933) as a new species Pachytriton granulosus and so named because of its rough, granular skin. It took a long time before this animal was recognised as the juvenile of another species, with a smooth-skin adult (Cai, 1985; Thiesmeier, 1997; Thiesmeier & Hornberg, 1997; Nishikawa et al., 2009). It was assumed that this other species must be P. labiatus, until Nishikawa et al. (2011b) found that the type specimen and paratypes of P. labiatus were in fact a Paramesotriton species (which in the meantime had been described as Paramesotriton ermizhaoi by Wu et al., 2009). This species was then given the available name P. granulosus, to distinguish it from the south-western group of Pachytriton, which was named P. inexpectatus by Nishikawa et al. (2011b). All literature prior to 2011 should be used with great caution because of these confusions.

References

Cai (1985); Chang (1933); Fei et al. (2006, 2012); IUCN

(2013); Nishikawa et al. (2009, 2011b); Thiesmeier (1997); Thiesmeier & Hornberg (1997, 1998, 2000); Wu et al. (2009, 2013).

Pachytriton inexpectatus Nishikawa, Jiang, Matsui & Mo, 2011 | Yaoshan

Stout Newt

Description

A fairly large but slender salamander. Head flat and large, longer than wide, snout truncated, conspicuous

Pachytriton inexpectatus, Dayaoshan mountain, Jinxiu County, Guangxi Zhuang Autonomous Region (type locality). Photos: Hou Mian.

labial folds. Eyes rather small. Paratoid glands prominent, another gland behind the paratoid gland. Distinct gular fold. No vertebral ridge, but a slight vertebral groove on the trunk (Fei et al., 2006). Tail strong, same length as snout-vent length, round at the base and compressed at the end with a rounded tip. Caudal fin on upper side of last two-thirds of the tail and a low keel on underpart of the entire tail. Fore and hind legs short, not touching when adpressed to the body. Fingers and digits short and stubby. Skin smooth with vertical wrinkles on the sides of the body and cross-wrinkles on the vent. Colour of back and sides mostly uniform dark or pale brown, usually without black spots or bright orange dorso-lateral dots; ventral side coloured vivid red and black, without dark spotting, reddish marks forming two longitudinal lines. Red and black ratio can differ greatly, from nearly completely red to almost entirely black. Ventral orange markings tend to be brighter in juveniles and diffused in larger adults (Wu et al., 2010b; Nishikawa et al., 2011b; Thiesmeier, 1997).

279

Sexual dimorphism not pronounced. Cloacal region broadly similar in the sexes, slightly swollen in the breeding male. Villi 2 mm long protruding from cloaca of breeding male. Breeding males develop one or several bluish-white spots on the distal part of the tail. Total length on average 164 mm in males, 176 mm in females (Nishikawa et al., 2011b); Ye et al. (1993) give 15-19 cm total length.

Diagnosis

A large-bodied newt with smooth skin and rectangular-shaped head. Colour of the back uniform brown, sometimes with red spots or dorso-lateral orange stripes. No small black spots on body, head and tail. Distinct red and black colouration on the belly. Similar to Pachytriton granulosus, but larger and more robust, with a wider head (Nishikawa et al., 2011b).

Eggs and larvae

Eggs and larvae are rarely found. Fei et al. (2006) reported developed embryos from Leishan, Guizhou Province, China, in June. Eggs found in ovaries ranged from 32-89 in number and were 3.4-4.7 mm in diameter (Nishikawa et al., 2011). Egg deposition in captivity was reported by Thiesmeier & Hornberg (1998, 2000). In two consecutive years a female of unknown provenance, and probably belonging to this species, laid a clutch of 42 eggs on the ceiling of the hiding place where she normally sat. Water temperature was 9.5°C. The eggs were large, the diameter of the embryo varying between 4.7-5.3 mm. The larvae were 15.1-17.6 mm long at hatching, the yolk was still present, and the legs were not yet formed. Embryonic development took ca. 57 days in water at

The range of Pachytriton inexpectatus. 280

Salamanders of the Old World | Pachytriton

an average temperature of 13.5°C. Metamorphosis occurred after about three months, at a water temperature of 16-17°C. Metamorphosed newts were small, ca. 35-42 mm long, and had a granulated skin. Juveniles are thought to live on land for the first few years of life, before reaching sexual maturity and returning to the water.

Distribution

This species occurs in western Guizhou Province, south-western Henan Province, north-western Guangdong Province, and northern and western Guangxi Zhuang Autonomous Region, China (Nishikawa et al., 2011b)

Habitat

Pachytriton inexpectatus inhabits mountain streams of varying sizes, where it lives a mainly aquatic life. Small juveniles are probably terrestrial (Nishikawa et al., 2011b; Thiesmeier & Hornberg, 1998, 2000).

Behaviour

Pachytriton inexpectatus has a gape and suck feeding habit specialised for foraging in flowing water. Its diet includes various species of annelids, molluscs and insects (Xu et al., 2002). Little is known about its ecology and natural history. In Guangdong the breeding season is reportedly in SeptemberOctober (Xu et al., 2002), but females collected with ripe eggs in May and June suggest that breeding can start earlier (Nishikawa et al., 2011b). The following information on reproductive behaviour is based on observations of captive specimens collected from an unknown locality. Both sexes are aggressive and fiercely attack animals coming within sight of, or near their hiding place, especially during the reproductive season. The female exhibits a form of parental care. Eggs are deposited in assemblages on the lower surface of stones or in hollows. The female sits under the eggs and does not leave while the eggs develop. She fends off other animals by biting. She may eat some of her eggs, possibly the mouldy or unfertilised ones (Thiesmeier & Hornberg, 1998; Sparreboom & Thiesmeier, 1999). The courtship of Pachytriton resembles that of other tailfanning, aquatic salamandrids that lack amplexus (Cynops, Paramesotriton). The male folds his tail back and makes fanning movements with the distal part of his tail, fanning roughly in the direction of the female’s snout. If the female is responsive and moves towards the male, the male turns around and starts creeping ahead of the female. The female probably orients to the male’s undulating tail and touches his tail with her snout. After a number of such tail-touches, the male deposits a spermatophore and creeps on, the female following him. The female moves over the spermatophore and picks up the sperm cap in her cloaca (Sparreboom & Thiesmeier, 1999).

Tail-fanning is not always associated with courtship. Any form of excitement, such as disturbance or the approach of a conspecific newt, may prompt bouts of tail-fanning in both male and female.

Threats and conservation

The species is collected for use in traditional Chinese medicine and is exported for the international pet market. Habitat destruction and degradation also pose threats, but the species appears to be relatively common (IUCN, 2013 information for P. labiatus).

Observations in captivity

Aquariums for Pachytriton must be spacious and should have flowing water. Due to this species’ extremely aggressive behaviour, a tank can accommodate only one or two animals and should contain many hiding places where they can sit in isolation (Thiesmeier & Hornberg, 1997, 1998, 2000; Reilley, 2005).

Comments

According to Frost (2013) ‘Nishikawa et al. (2011b) describe a confusing situation, where most of the animals previously referred to as the north-eastern population of Pachytriton labiatus were actually Pachytriton granulosus. The south-western population of the former Pachytriton labiatus was a distinct species, which they named Pachytriton inexpectatus, and the nominal types of Pachytriton labiatus were conspecific with what had been named Paramesotriton ermizhaoi, and not with the populations that had for so long been termed Pachytriton labiatus. All literature prior to 2011 should be used with great caution because of these confusions’.

References

Fei et al. (2006); Frost (2013); IUCN (2013); Nishikawa et

al. (2011b); Reilley (2005); Sparreboom & Thiesmeier (1999); Thiesmeier (1997); Thiesmeier & Hornberg (1997, 1998, 2000); Wu et al. (2010b); Xu et al. (2002).

Pachytriton moi Nishikawa, Jiang & Matsui, 2011 | Mo’s Stout Newt Description

The following is a summary of the holotype description by Nishikawa et al. (2011a). Pachytriton moi is a relatively large, stout-bodied Pachytriton. Skin smooth. Head squarish oval in shape, depressed and nearly flat in profile. Snout long and truncate, slightly extending over lower jaw. Nostrils close to snout tip. Labial fold evident. Skull wide. Maxillary connecting with pterygoid, forming an almost straight line. Fronto-squamosal arch complete and very robust. Epibranchial very long, wrapping the neck dorsolaterally. Vomerine tooth series long, inverted V-shaped, tooth rows

converging anteriorly, greatly exceeding anterior limit of choanae. Tongue fully attached to mouth floor. Paratoids evident. Gular fold present but weak. No vertebral or dorsolateral ridges. 10 costal grooves between axilla and groin. Adpressed limbs separated by one costal fold. Number of trunk vertebrae 12. Fingers and toes without webbing. Tail laterally compressed, posterior dorsal fin evident. Colour of the back uniformly dark brown. Venter light brown with several small orange spots in adults. Underside of tail partly light orange. Total length 19 cm.

Diagnosis

A relatively large, stout-bodied Pachytriton, uniformly dark brown above, without bright orange dots along dorsolateral region; no black spots over the body. Most similar to P. inexpectatus, but with larger body, longer snout and wider head. In juveniles, snout longer and ventral markings more finely scattered than in P. inexpectatus.

Eggs and larvae

No published information.

Distribution

Pachytriton moi. Photo: Kanto Nishikawa.

Pachytriton moi is known only from Mt. Mao’er, Ziyuan County and the Huaping National Nature Reserve, Longsheng Gezu Autonomous County, China. The precise borders of its range are unknown. In northern Guangxi, this species is distributed sympatrically with P. inexpectatus, but is much less abundant. 281

Habitat

The adult holotype was collected at an altitude of ca. 2,200 m in a montane stream.

Behaviour

This species is mainly nocturnal. Its breeding ecology and life history are unknown.

Comments

Phylogenetic relationships within the genus Pachytriton have not been resolved. Wu et al. (2012b) recognise two major clades on the basis of mitochondrial sequence data. The first clade includes P. inexpectatus and P. moi. The latter species is regarded as a third major clade in Pachytriton by Nishikawa et al. (2011a), but the data of Wu et al. (2012b) strongly support a sister relationship between P. inexpectatus and P. moi. Interestingly, the geographic range of P. moi lies within that of P. inexpectatus and the two species occur in sympatry at some locations. Nuclear gene and ecological data are necessary to further elucidate relationships between these two species.

The range of Pachytriton moi.

282

Salamanders of the Old World | Pachytriton

References

Nishikawa et al. (2011a); Wu et al. (2012b).

Paramesotriton Chang, 1935 Newts of the genus Paramesotriton resemble Cynops, but are generally larger. All species have a more or less rough skin and a prominent vertebral ridge, often with a lateral ridge along each side of the back. The parietal ridges of the skull are prominent and the tail is high and laterally compressed. Several morphological characters distinguish P. caudopunctatus from the other Paramesotriton species (Bischoff & Böhme, 1980; Sparreboom, 1981; Freytag, 1983). It is less robust, and its skull is longer and narrower compared with the broader skulls of the other Paramesotriton species. Molecular studies have shown that Paramesotriton is monophyletic, and sister to Cynops (Pang et al., 1992; Chan et al., 2001; Lu et al., 2004; Weisrock et al., 2006; Pyron & Wiens, 2011) or to Laotriton (Gu et al., 2012b). Paramesotriton species live in and around mountain streams. Paramesotriton is endemic to China and northern Vietnam. The distribution ranges of most of the species are poorly known.

Paramesotriton caudopunctatus (Liu & Hu, 1973) Paramesotriton chinensis (Gray, 1859) Paramesotriton deloustali (Bourret, 1934) Paramesotriton fuzhongensis Wen, 1989 Paramesotriton guangxiensis (Huang, Tang & Tang, 1983) Paramesotriton hongkongensis (Myers & Leviton, 1962) Paramesotriton labiatus (Unterstein, 1930) Paramesotriton longliensis Li, Tian, Gu & Xiong, 2008 Paramesotriton maolanensis Gu, Chen, Tian, Li & Ran, 2012 Paramesotriton wulingensis Wang, Tian & Gu, 2013 Paramesotriton yunwuensis Wu, Jiang & Hanken, 2010 Paramesotriton zhijinensis Li, Tian & Gu, 2008

References

Bischoff & Böhme (1980); Chan et al. (2001); Freytag

(1983); Gu et al. (2012b); Lu et al. (2004); Pang et al. (1992); Pyron & Wiens (2011); Sparreboom (1981); Weisrock et al. (2006).

Distribution of the genus Paramesotriton. Stars refer to the type localities. Only the ranges of P. chinensis, P. hongkongensis and P. deloustali are shaded. 1. Paramesotriton chinensis, 2. P. hongkongensis, 3. P. yunwuensis, 4. P. fuzhongensis, 5. P. labiatus, 6. P. caudopunctatus, 7. P. maolanensis, 8. P. longliensis, 9. P. zhijinensis, 10. P. wulingensis, 11. P. guangxiensis, 12. P. deloustali. Further distribution data in text.

Paramesotriton caudopunctatus (Liu & Hu, 1973) | Spot-tailed Warty Newt Description

A slender warty newt. Head flat and longer than wide. Prominent upper lip. Fore legs thinner and longer than hind legs. Toes and fingers short, broad and flattened, tips blunt and rounded. Tail shorter than snout-vent length. Dorsal and ventral tail-fins straight. Tail-tip blunt and rounded. Skin rough, but smoother than in other species of Paramesotriton. Prominent dorsal ridge.

tail. Ventral side of chin and throat grey-green, with incidentally a tinge of purple and cream-coloured spots. On the sides the colour changes from light green to orange-red, with small black spots (Hu et al., 1973; Sparreboom, 1981). The specimens described by Bischoff & Böhme (1980) have an ochre-coloured back, a ventral side mottled with green, grey and brown, and a red line running from throat to tail.

Dorsal and dorso-lateral ridges orange to ochre-coloured. Sides of head and body greenish, changing to light ochre towards the

The male has a light, round or elongate, pink spot on each side of the tail end, surrounded by black lines, except on the side of 283

Total length 122-146 mm in males, 131-154 mm in females (Fei et al., 2006). Variation between individuals is considerable, as is also apparent from the descriptions of Hu et al. (1973) and Bischoff & Böhme (1980). The type description is based on animals from Leishan, in Guizhou, and the specimens described by Bischoff & Böhme probably come from Quangxi.

Diagnosis

Paramesotriton caudopunctatus, male, Leigongshan Mountain, Guizhou (type locality). Photos: Hou Mian.

A slender, warty newt with a more elongated snout than other Paramesotriton species, and with a smoother skin and prominent orange dorsal ridge. Fingers and toes flattened. Black and conspicuous pink to orange spots, bordered with black, on the tail of the male. Belly colour variable, ranging from a pattern mottled with green, grey and brown with a red line running from throat to tail, to bright orange-red, with a small number of black spots placed in longitudinal rows.

Eggs and larvae

Eggs are normally placed in stone crevices, between stones and in fissures, either singly or as small clutches, rather than laid between the leaves of water plants. At the time of oviposition the female cloaca becomes thick and cone-shaped, allowing her to press the eggs between

284

Paramesotriton caudopunctatus, female, Leigongshan Mountain, Guizhou (type locality). Photos: Hou Mian.

Paramesotriton caudopunctatus, larva. Photo: Klaus-Detlef Kühnel.

the tail-tip. There are some more smaller and irregular pink spots, arranged in a longitudinal line at the base of the tail, surrounded by black, and a number of small black spots. In the breeding season, these pink spots become more conspicuous and turn bright purple, surrounded by dark purple to black linings. The body becomes light ochre-yellow. The female lacks these spots, but in older females a similar spot at the end of the tail may be vaguely visible. The male, as in most newt species, develops a swollen cloaca in the breeding season, with protruding papillae. Shortly before the female starts laying eggs, her cloaca becomes enlarged and cone-shaped, exceeding the size of the male cloaca (Sparreboom, 1983).

stones and into crevices. Eggs are laid in April-May and measure 4×3 mm in diameter, and 5×3.5 mm including the jelly capsule. A female may lay some 64 eggs on average (Henry Janssen, pers. comm.). Larvae hatch after 17-40 days, and measure 9-11 mm (Sparreboom, 1983; Henry Janssen, pers. comm.). Body colour black with small yellow-white spots arranged in longitudinal rows; pale yellow to reddish gills; iris yellow; dorsal tail-fin with a thin white edge; an orange-red dorsal stripe. After metamorphosis at a size of 45-55 mm, the animals are dark brown to black with light spots forming dorsolateral lines as well as ventro-lateral lines and have a prominent reddish dorsal ridge running from the head to the tail-tip. Juveniles move onto land. After a couple of months the body

Salamanders of the Old World | Paramesotriton

colour gradually changes to the ochre of the adult newt. The black sides of the back between the dorsal and dorso-lateral ridges contrast sharply with the red ridges and ochre sides and limbs, and may remain visible until adulthood.

Distribution

Paramesotriton caudopunctatus occurs in southwestern Hunan, southeastern Guizhou, and Fuchuan in eastern Guangxi in central China. It probably also occurs in areas between these known sites (Fei et al., 2012; IUCN, 2013). In Quangxi, P. caudopunctatus is sympatric with P. fuzhongensis (Wen, 1989; Zhang & Wen, 2000).

Habitat

This species inhabits mountain streams of varying sizes and the surrounding habitats in forested areas at altitudes from 800-1,800 m (Fei et al., 2006). It prefers pools along the stream, with a slow current and water depths between 10-100 cm. Paramesotriton caudopunctatus often forages near the edges of pools, under leaves fallen into the water. Some animals may be found in grassland, up to 15 cm away from the water.

Paramesotriton caudopunctatus, courtship. The male (left) creeps ahead of the female and is about to deposit a spermatophore. Photo: Max Sparreboom.

Behaviour

Mainly active in the evening, this species preys on insect larvae, arthropods, snails, frog eggs and earthworms (Fei et al., 2006). Knowledge of this species’ behaviour is based on observations of captive animals. Males establish territories and attack intruders. Both males and females are aggressive. If bitten an animal may curl up around the body of its attacker and remain motionless until the aggressor releases his grip.

Reproductive activity has been observed from November- April. The male takes up an alert posture, his fore legs stretched and his tail bent sideways. When he has identified a female, he orients in front of her and starts fanning his tail, producing a water stream directed to her snout. He keeps his head level with hers. If the female remains still, the male continues tailfanning. When responsive, the female moves towards the male. The male turns around, away from the female and moves forward, ahead of the female, making undulating movements with his tail. The female orients to the spot on the male’s tail and follows him. At this stage, the male may raise his tail and stretch it, keeping only the tip bent, so that the bright-coloured spotted tail-tip acts as a flag, moving to left and right and attracting the female (Sparreboom, 1983). This behaviour has not been observed in other Paramesotriton species, which all lack the tail spot. It resembles the luring tail movements of some European newt species (e.g. Lissotriton boscai, Triturus pygmaeus). The male then deposits a spermatophore in front of the female. When correctly aligned, the female moves over it and picks it up in her cloaca. A male may deposit several spermatophores in succession.

Paramesotriton caudopunctatus, courtship. The female’s viewpoint. The male creeps ahead of the female, making harmonica-like movements with his tail. Photo: Henry Janssen.

After egg-laying, females often remain close to the oviposition site and stay near the eggs. This behaviour has been observed on several occasions and may represent a form of parental care (Henry Janssen pers. comm.)

Threats and conservation

Although reportedly a very common species, Paramesotriton caudopunctatus is affected by habitat degradation (e.g., due to dam construction and the collection of wood) and by harvesting for use in traditional Chinese medicine and the international pet trade (IUCN, 2013). It is listed as Near Threatened. 285

Observations in captivity

The data on reproductive behaviour are all derived from observations on captive newts. Henry Janssen (Bruges, Belgium) has kept a detailed, long-term account of his observations on courtship and other behaviour patterns, including egg-laying, growth of larvae, and rearing of juveniles. Although popular among salamander enthusiasts, this species has proved difficult to breed. Large tanks with many flat stones and hiding places, aerated water, cool temperatures,

and limiting the collection to only a small group of animals, appear necessary requirements. Larvae and juveniles may be sensitive to stress, and prone to cannibalism, so are best kept in separate containers. Observations on the behaviour patterns of this species in the reproductive season suggest complex social interactions, which are not yet fully understood (Sparreboom, 1983; Henry Janssen, pers. comm.).

Comments

The taxonomic position of Paramesotriton caudopunctatus has been a subject of debate. Paramesotriton caudopunctatus differs from all other species of Paramesotriton in several respects. Its elongate snout, different sexual dimorphism, and unique egg-laying behaviour, led to it being placed in a (sub)genus of its own (Allomesotriton) by Freytag (1983). Molecular studies based on mitochondrial DNA suggest that Paramesotriton may be divided into two clades: one including P. caudopunctatus, P. longliensis, P. zhijinensis, P. maolanensis and P. wulingensis, and the other containing the remaining Paramesotriton species (Zhao et al., 2008; Wu et al., 2010a; Pyron & Wiens, 2011; Gu et al., 2012a, 2012b).

References Paramesotriton caudopunctatus, captive F1 males fighting. The bitten animal curls up around the head of the biting male. Photo: Henry Janssen.

Bischoff & Böhme (1980); Fei et al. (2006, 2012); Freytag

(1983); Gu et al. (2012a, 2012b); Hu et al. (1973); IUCN (2013); Pyron & Wiens (2011); Sparreboom (1981, 1983); Wen (1989); Wu et al. (2010a); Zhang & Wen (2000); Zhao et al. (2008).

Paramesotriton chinensis (Gray, 1859) | Chinese Warty Newt Description

A robust newt with very granular skin and less prominent vertebral ridge. Warts are largest on head and dorsum. Head a little longer than wide, snout truncated. Labial fold is conspicuous. Gular fold is absent or inconspicuous. Limbs well-developed; digits overlap when limbs are adpressed. Tail longer than snout-vent length, high and laterally compressed, with fins on upper- and undersides and ending in a blunt tip. Dorsal colour is uniform dark olive-green or grey to dark brown, occasionally with darker patches on body and tail, and small orange dots irregularly scattered on the sides. In the terrestrial form the dorsal colour is uniformly black (Chang & Boring, 1935). Ventral side bluish-black, with small, unequal, irregular yellow-orange spots on the chin, neck, belly and underside of the legs. Underside of the tail is reddish-yellow, interrupted with dark patches.

Paramesotriton chinensis, male, Zhejiang. Photos: Hou Mian. 286

Salamanders of the Old World | Paramesotriton

In the breeding season, the male has a silver-white stripe along the tail and a swollen cloaca with protruding papillae. Males are smaller than females.

Eggs and larvae

Eggs are laid singly between leaves, but many eggs may be laid on a single leaf. Eggs large, as in other Paramesotriton species. Larvae are uniformly black and juveniles are black with yellow spots (Thorn & Raffaëlli, 2001). Captive-bred animals reached sexual maturity between 3-7 years (Pasmans et al., in press).

Distribution

This species occurs in eastern China, including the provinces of Anhui, Zhejiang and Fujian. Its distribution was formerly believed to be wider, including Chongqing, Hunan, Guangdong and Guangxi in central China (Fei et al., 2006; IUCN, 2013), but the Paramesotriton forms in those areas actually represent new species (see under P. longliensis, P. yunwuensis, P. fuzhongensis, P. labiatus) (Wu et al., 2009, 2010a).

Habitat Paramesotriton chinensis, female, Zhejiang. Photos: Hou Mian.

Total length 126-141 mm in males, 133-151 mm in females (Fei et al., 2006). Females in captivity may reach a length of 18.5 cm (Pasmans et al., in press).

Diagnosis

A robust newt with very rough skin. Paramesotriton chinensis resembles Cynops pyrrhogaster in the form of the head and paratoid glands, but differs from it in its larger size and the colour pattern on the belly: small yellow-orange spots on a bluish-black background, rather than a black pattern on a red background colour (Gray, 1859). Dorsal side far more granular than in P. hongkongensis; no cranial ridges and less prominent dorso-lateral ridges than in P. hongkongensis. Tail of the female higher than in P. fuzhongensis and the tail end of the female very dark to black, unlike P. fuzhongensis (Thorn & Raffaëlli, 2001).

The species’ aquatic habitat consists of wide stony streams with swift-running water, at the base of mountains at elevations between 200-1,200 m. Stream substrates include gravel and sand, and the streams are bordered by trees and shrubs. The newts hide under stones in the water and also live partly on land, where they are found under grass were the ground is damp and covered with decaying leaves (Chang & Boring, 1935).

Behaviour

Paramesotriton chinensis preys on earthworms, insects and snails (Fei et al., 2006). It is most active at night from 7 pm to 2 am (Lv & Shen, 1998). Observations in captivity indicate that P. chinensis is aggressive during the breeding season, when it lives in water. This behaviour, which possibly serves to defend a territory, has been observed in all species of Paramesotriton (Sparreboom, 1984b; Raffaëlli, 2007; Pasmans et al., in press). Courtship behaviour has not been described in detail but is probably similar to that of other Paramesotriton species (Romer, 1951; Arnold, 1972; Rehák, 1984; Sparreboom, 1984abc, 1986, 1991).

Threats and conservation

The Chinese Warty Newt is frequently found for sale in Chinese pet markets, along with Cynops orientalis and Pachytriton species. Although this suggests that this species is abundant, the effect of such harvesting on natural populations has not been studied and is hence unknown. The species is presently considered to be of Least Concern (IUCN, 2013).

Observations in captivity

Paramesotriton chinensis. Illustration in the original description by Gray, 1859.

Most examples of Paramesotriton chinensis circulating among hobbyists are obtained through the pet trade and their precise collecting locality is unknown. The species has been known among hobbyists for many years (Freytag 1963), but factual information on captive breeding remains limited. Like other Paramesotriton species, it is problematic in captivity, probably due to its sensitivity to 287

stress. Aquariums should be spacious and have enough hiding places to allow the animals to escape from aggressive conspecifics. A detailed account is given in Pasmans et al. (in press).

Comments

Species descriptions of Paramesotriton provide little comparative detail and identification is often difficult. Before P. fuzhongensis was described (Wen, 1989), Chinese newts obtained via the pet trade were often labeled P. chinensis, being the form most similar to the animal at hand. Observations

made on P. chinensis in earlier papers, probably relate to P. fuzhongensis (such as in Sparreboom, 1984abc) or to P. hongkongensis, (such as in Romer, 1951), before the Hong Kong Newt was described as a separate species (Myers & Leviton, 1963).

References

Arnold (1972); Chang & Boring (1935); Fei et al. (2006);

Freytag (1963); Gray (1859); IUCN (2013); Lv & Shen (1998); Myers & Leviton (1963); Pasmans et al. (in press); Raffaëlli (2007); Rehák (1984); Romer (1951); Sparreboom (1984a, 1984b, 1984c, 1986, 1991); Thorn & Raffaëlli (2001); Wen (1989); Wu et al. (2009); Wu et al. (2010a).

Paramesotriton deloustali (Bourret, 1934) | Tam Dao Warty Newt Description

A large, heavy newt with very granular skin and large head. Head as long as or a little longer than broad, with truncated or square snout. Bony ridges on each side of the head extending from snout to paratoid glands and median ridge on parietal part of the head. Stout body with high vertebral ridge and two dorso-lateral series of glandular warts extending onto the first part of the tail. Tail a little shorter than snout-vent length with high undulating fin above and straight caudal fin below. Tail end rounded or blunt. Skin of head and body very rough with numerous wrinkles.

The tail a little shorter in the male than in the female. In the breeding season the male develops a swollen cloaca and an irregular, bright purple stripe on the tail. This stripe may also be faintly present in some females. Dorsal colour deep olive-brown with orange spots on the dorsolateral ridges. Tail end lighter in colour. Ventral colour deep orange-red with a network of black lines, sometimes interrupted, forming large, irregular, orange blotches. Underside of the tail orange at the base and darker at the end (Freytag & Petzold, 1961). Animals kept in captivity for many years showed a gradual change in ventral colouration, from large orange patches to a more mottled pattern with black becoming more prominent (Henry Janssen, pers. comm.). Total average length 16-17 cm in males and 18-20 cm in females (Rehák, 1984). Larger specimens have been recorded.

Diagnosis Paramesotriton deloustali, male F1, parents from Tam Dao. Photo: Henry Janssen.

A large newt with warty skin and large head. Bright orange colouration on belly, throat and chin, covered with a typical network of black lines.

Eggs and larvae

Paramesotriton deloustali, female F1, parents from Tam Dao. Photo: Henry Janssen. 288

Salamanders of the Old World | Paramesotriton

Egg deposition has been observed from January-April. The female uses her hind feet to press the leaves of aquatic plants together against the eggs as they are laid. Eggs are laid singly, or sometimes in a chain of several eggs. A female may lay between 30-256 eggs (Rehák, 1984, 1990). Eggs are large, the jelly capsule measuring 7 or 8×5 or 6 mm, and the eggs are 3 mm in diameter. At temperatures between 17-27°C, larvae hatch after 28-37 days at a length of 12-16 mm, at various stages of development. Larvae hatching after 28 days are 12 mm long and exhibit the initial phase of digital growth on the forefeet and bud-shaped hind-feet. Larvae hatching after 37 days are 16 mm long and have four digits present on welldeveloped fore- and hind-feet (Rehák, 1984).

Vietnam. It occurs from ca. 200-1,300 m altitude (Nguyen et al., 2003; IUCN, 2013).

Habitat

This species inhabits small and medium-sized streams in lower montane, evergreen forest, including small pools and man-made basins. Water temperature in winter and early spring is fairly constant at around 11°C.

Behaviour Paramesotriton deloustali, female, Tam Dao. Photo: Max Sparreboom.

Paramesotriton deloustali appears to have no hibernation or aestivation period. Adults may be found in water all year round and it is unclear whether some adult individuals may also live partly on land. This species has been recorded eating the larvae of Odonata and small gastropods (Rehák, 1990). These newts are mainly nocturnal. The reproductive season starts at the end of November, when water temperatures fall from 19°C to 14°C (Rehák, 1990). Their reproductive behaviour is similar to that described for P. fuzhongensis and P. hongkongensis (Romer, 1951; Arnold, 1972; Sparreboom, 1984abc). The males are aggressive towards individuals of either sex, especially during the breeding period. They defend territories, as do other species of Paramesotriton, and are solicitous of certain individuals that are tolerated and mated, while other are bitten or driven away (Rehák, 1984, 1990).

Paramesotriton deloustali, female, ventral side. Tam Dao. Photo: Max Sparreboom.

Larvae have three pairs of gills. Body is black, upper margin of tail-fin and posterior part of bottom margin are white, and the gills are pink. Nostrils white. Eye prominent, iris light, pupil horizontal. Light spots appear on ventral side of the body of the larva at the age of two months. If larvae are kept in the dark, the black colour changes to greyish. After 4-12 months, larvae undergo metamorphosis at a size of about 5 cm and live on land until they reach sexual maturity. In captivity, several juveniles returned to the water after 17 months, at a length of 9-10 cm. The orange spots on the belly are small in juveniles and become larger with age. The metamorphosed juvenile is dark brown to black and has a smooth skin. One to two months after metamorphosis the dorsal and dorso-lateral ridges appear (Rehák, 1984, 1986).

Distribution

This species was originally known only from the Tam Dao mountain ridge in northern Vietnam. It has now been found in more than ten localities in Bac Kan, Ha Giang, Yen Bai, Tuyen Quang, Tay Nguyen and Lao Cai Provinces, all in

Observations on sexual behaviour of captive animals were made from December-February, at water temperatures between 16-18°C. When faced with a female to which he is ‘well-disposed’, the male approaches her and lightly nudges her body with his snout. He approaches alongside her, turns in front of her head, stops and performs a lateral display consisting of rapid fanning movements of the tail, folded against his body. If the female stops and stands still, the male continues to perform bouts of tail-fanning. If receptive, the female moves forward and nudges the male’s cheek, sometimes biting his head delicately. At this point the male turns away from her and pauses just in front of her snout with his tail in an S-shape. When the female nudges his tail with her snout, the male creeps forward and the female follows. The male stops and deposits a spermatophore. If followed by the female, he creeps on and may release several more spermatophores in succession (Rehák, 1984).

Threats and conservation

Paramesotriton deloustali is kept as an exotic pet in some Hanoi homes and its habitat, at least in Tam Dao, is under pressure (McRae, 1999; Martens, 2003). The main threats are habitat loss, water pollution, poisoning of water due to fishing, and collecting. It is considered Endangered in the Vietnam Red Data Book (Tran et al., 1992) and has 289

been protected by legislation in Vietnam since 1992. The species is considered Vulnerable (IUCN, 2013). Measures are being taken to conserve its habitat (Nguyen et al., 2003).

Observations in captivity

Paramesotriton deloustali has been bred in captivity on several occasions (Rehák, 1984; Henry Janssen, in Thorn & Raffaëlli, 2001) and is the subject of research and breeding attempts in Vietnam (Nguyen, 2000). The observations on courtship and oviposition reported above were made on captive animals. These newts should be given enough space and hiding places to avoid aggressive encounters. Water temperature should be maintained between 15-25°C and the water should preferably be aerated. The Tam Dao Warty Newt has proved delicate in captivity and sensitive to stress, and is best kept as

a pair in a large tank. Rearing the young newts is difficult, especially in the stage directly following metamorphosis. Newts born in captivity reproduced for the first time in their sixth or seventh year, at a length of 125-140 mm (Rehák, 1990).

Comments

Although there appears to be local variation in size and colour patterns among the different populations, all the animals from the mentioned localities are thus far attributed to P. deloustali.

References

Arnold (1972); Freytag & Petzold (1961); IUCN (2013);

Martens (2003); McRae (1999); Nguyen (2000); Nguyen et al. (2003); Rehák (1984, 1986, 1990); Romer (1951); Sparreboom, M., (1984a, 1984b, 1984c); Thorn & Raffaëlli (2001); Tran et al. (1992).

Paramesotriton fuzhongensis Wen, 1989 | Fuzhong Warty Newt Description

A large, robust newt with very warty skin. Head longer than wide. Upper labial fold prominent and more developed under the eyes. Fore- and hindlimbs of nearly equal length, with hindlimbs stouter and tip of forelimb reaching midway between nostril and eye. Adpressed fore- and hindlimbs overlap. Toes with blunt, round tips. Tail shorter than snout-vent length, thick at the base and gradually becoming laterally compressed.

Skin very rough with prominent dorsal ridge. Entire body, from head to anterior part of tail and dorsal surface of limbs covered

with warts. Large dorso-lateral warts form two ridges. Underside smooth from labial fold to belly, as are the fore- and hindlimbs. Colour of dorsal side dark to olive-brown, occasionally mixed with a lighter or darker colour. Sometimes small dark spots on back. Sides may have greyish-white stripes or various black spots. A light dorsal stripe in some specimens. Belly pattern consisting of large, disconnected orange or red blotches extending onto throat and chin. The male normally has a shorter and higher tail than the female. Orange spots on throat smaller than in female. During the breeding season the male has a silver-blue sheen along the tail. Total length 133-166 mm for males, 134-159 mm for females (Wen, 1989). The largest (captive) female on record measured 21 cm (Sparreboom, 1991).

Diagnosis

A large, stout newt, the skin densely covered with warts. Similar to Paramesotriton chinensis but larger and covered with more and larger warts, and no black tail end in the female (Thorn & Raffaëlli, 2001). Similar to P. guangxiensis, but with a more warty skin, longer and narrower head, longer and lower tail, and with black mottling on the back in many individuals, which is rare in P. guangxiensis. Forelimbs of P. fuzhongensis reaching between the eye and nostril when drawn forward, while those of P. guangxiensis do not reach as far (Wen, 1989).

Eggs and larvae Paramesotriton fuzhongensis, Zhongshan County, Guangxi Zhuang Autonomous Region (type locality). Photos: Hou Mian. 290

Salamanders of the Old World | Paramesotriton

Egg deposition was observed in captivity, taking place from March-May. Eggs are large, the jelly mass measuring 5-6 mm, the egg diameter 2.5-3 mm. Eggs are laid

Distribution

Paramesotriton fuzhongensis is only known from northeastern Guangxi (Zhongshan, Fuchuan and Gongchen Counties) in China, where it lives at altitudes from 400-1,200 m (IUCN, 2013). Paramesotriton guangxiensis occurs in Mingjiang, in the extreme southwestern part of the Guangxi Autonomous Region. The two areas are separated by the Xi River system (Wen, 1989).

Habitat

This newt inhabits low-gradient montane streams surrounded by broadleaf forests. It prefers pools under waterfalls (Yunke Wu, pers. comm.). Adult animals may be found under rocks and sometimes on land. Reproduction takes place in the water. In Fuchuan County, Paramesotriton fuzhongensis is sympatric with P. caudopunctatus (Wen, 1989).

Paramesotriton fuzhongensis, male. Photo: Henry Janssen.

Paramesotriton fuzhongensis, male. Photo: Henry Janssen.

Paramesotriton fuzhongensis, female. Photo: Henry Janssen.

between leaves, but the leaves are not folded around the egg as occurs in Cynops. Larvae hatch at various stages of development after 3-5 weeks, depending on water temperature, and measure 10-12 mm. Larvae black or dark brown, some with cream coloured dots on back and belly, gills reddish, iris white, and a white spot on the snout. They measure approximately 40 mm at metamorphosis (Sparreboom, 1984c). Juveniles are dark brown, sometimes with orange dots and stripes on the back (Thorn & Raffaëlli, 2001).

Behaviour

There is very little information about the ecology and life history of this species (Zhang & Wen, 2000). Reproductive behaviour was observed in captivity in February-March. Courtship patterns of animals labeled Paramesotriton chinensis have been described in part, but these individuals probably belonged to the form later described as P. fuzhongensis (Sparreboom, 1984abc, 1986, 1991). Aquarium observations have shown that the male defends a territory, normally near a hiding place or at a spot where he can oversee his surroundings. He approaches and attacks intruding newts – males and occasionally also females. When the intruding animal flees, the resident male returns to his spot. If the attacker bites, for instance on a leg or tail, he may hold on for several minutes and make jerking movements with his head. A bitten animal assumes a characteristic position. It curls up sideways around the head and neck of the attacker, eyes closed, and remains motionless until the attacker loosens its grip and lets go. Both males and females are subject to attacks, and females may also be aggressive. This aggression probably serves to maintain a kind of territory, and could be interpreted as a mechanism to monopolise suitable mating sites on the bottom of streams. Courtship takes place at night and follows the pattern described for P. hongkongensis (Romer, 1951; Arnold, 1972) and P. deloustali (Rehák, 1984). The male stands at the alert with his fore legs stretched and his head raised a little. He approaches a female, and after he has identified her as such, starts fanning his tail, creating a stream of water directed toward her snout. A responsive female remains standing motionless. At a certain moment the male turns around and walks ahead a few paces. The female orients herself towards the silver stripe on the male’s tail and touches it with her snout. The male creeps on and deposits a spermatophore on the substrate. The female follows the male, moves over the spermatophore and, if all goes well, picks up the sperm cap with her cloaca. The male may deposit several spermatophores in one sequence (Sparreboom, 1991). 291

Threats and conservation

Most newts circulating among hobbyists are obtained through the pet trade and, accordingly, their precise collecting locality is either unknown or unreliable. There may be further, undescribed forms in addition to those known at present.

Observations in captivity

Identification of members of the genus Paramesotriton is therefore often problematic. The taxonomic information in the original species descriptions is very limited, and scientists disagree about the taxonomic status of the various forms. Pang et al. (1992) suggested that P. fuzhongensis was very similar to P. chinensis based on morphology, osteology and morphometric data, except that P. fuzhongensis was larger and had higher caudal fins. However, molecular phylogenetic analyses indicate a close relationship between P. fuzhongensis, P. guangxiensis and P. yunwuensis (Weisrock et al., 2006; Wu et al., 2010a; Pyron & Wiens, 2011). The specific status of P. fuzhongensis is no longer contested.

This species is listed as Vulnerable. Fewer than ten locations are known and the extent and quality of its habitat are in decline, as are the number of mature animals found (IUCN, 2013).

Observations in captivity indicate that Paramesotriton fuzhongensis is aggressive in the breeding season, when it lives in water, as is the case to some degree in all species of Paramesotriton. The reproductive behaviour described above was observed in aquariums of 80×40×40 cm provided with numerous hiding places (Sparreboom, 1984abc). The species is difficult to keep and appears sensitive to stress, such as disturbances in the aquarium or exposure to other newts.

Comments

Before Paramesotriton fuzhongensis was described, Chinese newts obtained via the pet trade were often labeled P. chinensis, being the species most similar to the animal at hand. Observations made on P. chinensis in earlier papers, may in fact relate to P. fuzhongensis (such as in Sparreboom, 1984abc). The animals on which these articles reported were imported from Hong Kong in the late 1970’s and early 1980’s.

References

Arnold (1972); IUCN (2013); Pang et al. (1992); Pyron &

Wiens (2011); Rehák (1984); Romer (1951); Sparreboom (1984a, 1984b, 1984c, 1986, 1991); Thorn & Raffaëlli (2001); Weisrock et al. (2006); Wen (1989); Wu et al. (2010a); Zhang & Wen (2000).

Paramesotriton guangxiensis (Huang, Tang & Tang, 1983) | Guangxi

Warty Newt

Description

A moderately small-sized warty newt. Flat, triangular head, longer than wide. Flat, stout body. Snout truncated. Labial fold well-developed. When fore- and hindlimbs are adpressed, digits just meet. Skin rugose with small wrinkles, a high vertebral ridge extending onto the tail. Tail length shorter than snout-vent length, ending in a thin tip. Cloaca swollen and with papillae visible in the male during the reproductive season.

292

Paramesotriton guangxiensis, F1, 2 yrs old, ventral side, Shiwan Dashan, Guangxi. Photo: Henry Janssen.

Colour of upperside dark brown; underside black with large, irregular yellow to orange blotches. Lower tail-fin orange, fading towards the tip. Colour is lighter in the female.

Paramesotriton guangxiensis, F1, 2 yrs old, Shiwan Dashan, Guangxi. Photo: Henry Janssen.

Morphologically, Paramesotriton guangxiensis resembles, but is nevertheless distinct from, P. deloustali, P. yunwuensis and P. fuzhongensis. In P. guangxiensis and P. yunwuensis the extended forelimb does not reach the posterior margin of the eye. In P. deloustali the extended forelimb reaches the midpoint of the eye and in P. fuzhongensis it reaches even further anteriorly to a point midway between the eye and the nostril. Compared with P. yunwuensis, P. guangxiensis is smaller and more gracile: the trunk is relatively flat in cross section, not square or round as in P. yunwuensis. Its tail is shorter and deeper (Wu et al. 2010a).

Salamanders of the Old World | Paramesotriton

Total length 125-140 mm in males, ca. 134 mm in females (Huang et al., 1983).

Diagnosis

Similar to Paramesotriton chinensis, notably in its granular skin, but it differs from that species in having a snout length longer than the eye diameter, a flatter body, entirely dark brown colour of the back, short fore legs, prominent dorsal ridge, and high, compressed tail (Huang et al., 1983).

Threats and conservation

Due to its vulnerable habitat and the limited extent of its currently known occurrence it is listed as Endangered (IUCN, 2013).

Observations in captivity

Larvae of this species have been successfully raised to adulthood by Henry Janssen (Bruges, Belgium).

Paramesotriton guangxiensis, larva. Photo: Henry Janssen.

Eggs and larvae

The larva is black with golden-yellow gills, tail-fin lined with white, and the tip of the nose and iris yellowish-white. Underside black with whitish patches.

Distribution

Apart from the type locality, Paiyang shan, Ningming County in Guangxi, China, where it occurs at 470 m altitude (Huang et al., 1983; Zhang & Wen, 2000), this species has also been reported from Shiwan Dashan National Forest Park (Guangxi, China, Arnaud Jamin, pers. comm.) and neighbouring areas in northern Vietnam (Nguyen Thien Tao, pers. comm.)

Habitat

Paramesotriton guangxiensis inhabits low gradient streams and their surrounding habitats under dense forest and bushes. They hide under rocks in the stream or in grasses near the stream edge and are often found on land after heavy rains, up to 0.5-1 m away from the stream (Fei et al., 2006).

Behaviour

The species is mostly nocturnal and preys on small insects and earthworms.

Paramesotriton guangxiensis, habitat, Shiwan Dashan, Guangxi. Photo: Arnaud Jamin.

Comments

The large head and distinctive colour pattern give this species the look of a small-sized Paramesotriton deloustali. However, molecular studies suggest that P. guangxiensis is more closely related to P. yunwuensis and P. fuzhongensis than to P. deloustali (Wu et al., 2010a; Pyron & Wiens, 2011).

References

Fei et al. (2006); Huang et al. (1983); IUCN (2013);

Pyron &Wiens (2011); Wu et al. (2010a); Zhang & Wen (2000).

Paramesotriton hongkongensis (Myers & Leviton, 1962) | Hong Kong

Warty Newt

Description

A stocky newt with a dorsal ridge and clearly demarcated dorso-lateral ridges consisting of glandular warts. Head a little longer than wide with truncated snout. Cranial ridge from tip of snout to paratoid region; bony median parietal

ridge. In transverse section the trunk is pentagonal, rather than round as in Paramesotriton chinensis. Tail a little shorter than head and body, compressed laterally and a little higher than in P. chinensis. Tail-tip blunt. Skin less warty than in P. chinensis. 293

Paramesotriton hongkongensis, male, Hongkong. Photo: Bosco Chan, courtesy KCC.

Paramesotriton hongkongensis, Wutong Hill, border between Hongkong and Shenzhen. Photos: Hou Mian.

Dorsal colour uniform dark olive to dark brown, the vertebral ridge faintly or distinctly orange in some individuals. Ventral colouration bluish-black with irregular, unequal, orange spots, small in some specimens and larger in others. Lower edge of tail orange, fading towards tail-tip. Tail dark like dorsal colour or lighter, sometimes mottled with orange and a darker colour (Romer, 1951). Males are smaller than females. In the breeding season males have a swollen cloaca and a greyish-white stripe on the tail. Fewer and larger orange spots on the belly of the male than of the female. In the male, the orange spots are surrounded by black on a greyish-blue base; in the female the background colour is more evenly dark, covered with more and smaller orange spots; the male has one larger orange patch just before the cloacal opening, whereas this is lacking in the female (Martens, 1999). Total length 104-125 mm in males, 118-143 mm in females (Fei et al., 2006). In captivity, females may exceptionally reach a length of 16 cm (Pasmans et al., in press).

Diagnosis

A robust newt with relatively smooth skin. Differs from Paramesotriton chinensis in: the smoother, less tuberculated skin of its head and trunk; the presence of a distinct median parietal ridge; the presence of large orange-red spots on the gular region; the presence of an uninterrupted light streak

294

Salamanders of the Old World | Paramesotriton

Paramesotriton hongkongensis, adult female F1. Photo: Henry Janssen.

along the inferior midline of the basal part of the tail; and much stronger dorso-lateral ridges (Myers & Leviton, 1962).

Eggs and larvae

Eggs are laid in February-March. The female presses the leaves of aquatic plants together with her hind feet around the eggs as they are laid. Eggs are laid singly, sometimes forming a series, sandwiched between a single leaf. A female may lay ca. 115 eggs (Romer, 1951). Eggs are larger than in many other salamanders, the jelly capsule measuring 6×4.5 mm, and the egg diameter being 2.9 mm (Kong & Tong, 1986). Larvae hatch after 3-4 weeks at a length of 10-14 mm and at various stages of development. Hatching is normally after 25 days, at a water temperature of 20°C, with hind-limb development at stage 5 of 39 stages, with the fourth digit and second toe appearing, and at a total larval length of 13 mm (Kong & Tong, 1986). Larvae are black, with pink gills, golden iris and a whitish patch on the snout between the nostrils. The belly is black with irregular pale yellow spots.

Breeding occurs primarily during the cool, dry season, but the breeding season may extend over eight months. Seasonal migration patterns differ among populations, males usually entering and leaving the breeding pools earlier and staying longer than females (Fu et al., 2013).

Paramesotriton hongkongensis, larva. Photo: Christen Wen.

Paramesotriton hongkongensis, females laying eggs. Photo: Christen Wen.

Most larvae reach metamorphosis before the next cold season at a length of 40-44 mm, and then move onto land (Romer, 1951). It takes them three years to reach sexual maturity (Kong & Tong, 1986).

Adult Paramesotriton hongkongensis feed mainly on snails, shrimps, newt eggs, beatid mayflies and calamoceratid caddisflies. Cannibalised eggs are more important as food for females than for males. The diet of adult newts on land comprises mainly earthworms and isopods (Fu et al., 2013).

Distribution

The Hong Kong Warty Newt occurs from coastal Guangdong, including Hong Kong, at altitudes from 30-940 m (IUCN, 2013). It is widely distributed in the New Territories, and more localised on Lantau Island and Hong Kong Island (Karsen et al., 1998). It also occurs in central Guangdong, where a population has been found on Mt. Nankun (Gu et al., 2007; Wu et al., 2010a).

Habitat

Aquatic habitats serve as important breeding and feeding grounds for Paramesotriton hongkongensis, while the adjacent terrestrial habitats are crucial for feeding and growth during the extended non-breeding period which is spent on land (Fu et al., 2013). The aquatic habitat consists of slow-flowing, shallow streams, and deep stream pools, with numerous pebbles and boulders providing cover. Aquatic and terrestrial vegetation overhanging the water’s edge provide suitable habitat for the newts and their prey.

Behaviour

There is no hibernation period. Adults may be found in water all year round. The water temperature of the streams does not normally fall below 12.5°C. They are mainly nocturnal but can also be observed during the day. Recent ecological work showed that individual newts remain in the breeding pools for 45 days on average, suggesting that populations in pools were changing throughout the breeding season and that most adult individuals had a 10 month terrestrial phase. The main reproductive season is from November-April.

Reproductive behaviour is similar to that described for P. fuzhongensis (observations on animals sourced from the pet trade, at the time still identified as P. chinensis) and P. deloustali (Rehák, 1984; Sparreboom, 1984abc). The males may be aggressive and appear to defend territories, as in other Paramesotriton species. When first faced with a female, the male approaches her slowly and nudges her body lightly with his snout. He moves rapidly forward alongside her, turns in front of her head and immediately stops and performs a lateral display. This display consists of fanning movements of the tail, folded against his body. If the female stops and remains stationary, the male continues to perform bouts of tail-fanning. If the female moves forward and nudges the male’s cheek during the lateral display, the male immediately turns away from her and pauses just in front of her snout with his tail in an S-shape. When the female nudges his tail with her snout, the male creeps forward and the female follows. The male stops and deposits a spermatophore (Arnold, 1972).

Threats and conservation

Significant numbers of newts are collected for the pet trade and this species is considered Near Threatened. It is protected by local legislation in Hong Kong (IUCN, 2013).

Observations in captivity

The Hong Kong Warty Newt has been bred in captivity on several occasions (Romer, 1951; 295

Sparreboom, 1984c; Pasmans et al., in press) and the observations on courtship and oviposition reported above were made on captive animals. In the aquarium, these newts should be given enough space and hiding places to space themselves out, so that they can avoid aggressive encounters. Water temperature should be maintained between 15-25º C and the water should preferably be aerated (Thorn & Raffaëlli, 2001). The Hong Kong Warty Newt has proved to be hardy in captivity and can live for many years. Rearing the young newts is more difficult, especially in the stage directly following metamorphosis, when they are very specific in their humidity requirements. Paramesotriton hongkongensis has been captive bred to the third generation (F3) by Henry Janssen (Bruges, Belgium).

Comments

Our knowledge of the ecology and life-history of this species has long been based mainly on the report by Romer (1951). The recent work of Fu et al. (2013) addresses the ecology of this species and sets an example for further work on other Paramesotriton species.

References

Arnold (1972); Fei et al. (2006); Fu et al. (2013); Gu et al.

(2007); IUCN (2013); Karsen et al. (1998); Kong & Tong (1986); Martens (1999); Myers & Leviton (1962); Pasmans et al. (in press); Rehák (1984); Romer (1951); Sparreboom (1984a, 1984b, 1984c, 1986); Thorn & Raffaëlli (2001); Wu et al. (2010a).

Paramesotriton labiatus (Unterstein, 1830) | Spotless Smooth Warty Newt Description

The following account is based on the description of this species under the name Paramesotriton ermizhaoi by Wu et al. (2009; see under comments below).

No toe webbing. Tail laterally compressed; posterior dorsal fin evident, ventral caudal fin indistinct; tail-tip round in profile.

Paramesotriton labiatus, Dayaoshan, Guangxi. Photo: Hou Mian.

Paramesotriton labiatus, Dayaoshan, Guangxi (type locality). Photo: Li Jiatang.

A slender, flat-bodied newt. Head oval in shape, depressed and nearly flat in profile. Snout truncate and slightly projecting beyond lower mandible. Nostrils close to snout tip. Labial folds evident. Skull relatively narrow. Paratoid region evident, not enlarged. Gill filaments absent, gular fold present. Skin relatively smooth on head and body, with small transverse wrinkles. Vertebral ridge thin, slightly elevated. Lateral dorsal ridge absent. About half of the animals studied had thirteen, rather than the usual twelve trunk vertebrae. Limbs short. 296

Salamanders of the Old World | Paramesotriton

Paramesotriton labiatus, ventral view, Dayaoshan, Guangxi. Photo: Hou Mian.

pools with a very slow current. Fishes and small aquatic invertebrates coexist with this newt.

Dorsal colour olive-brown with irregular black flecks. Vertebral ridge with orange tint. Ventral side paler brown with orange-red irregularly shaped blotches. Orange-red on underside of tail.

Behaviour

Total length 92-128 mm in males, 94-138 mm in females; males on average slightly smaller and with shorter tail than females.

Threats and conservation

During the day Paramesotriton labiatus is usually found in water, hiding under rocks or between crevices. No published information.

Observations in captivity

Paramesotriton labiatus, Dayaoshan, Guangxi (type locality). Photo: Yunke Wu.

Diagnosis

Skin relatively smooth; granular warts absent on head and body; vertebral ridge not prominent; head depressed and nearly flat in profile; habitus slender and depressed. When limbs are adpressed, fingers and toes hardly meet.

Eggs and larvae

No published information, but see under observations in captivity and comments.

Distribution

This species was described by Unterstein (1930) as Molge labiatum from ‘Yaoshan, Kwangsi, China.’ This area is currently known as Mt. Dayao, Jinxiu Yao Autonomous County, Guangxi Zhuang Autonomous Region, China (Wu et al., 2009; Nishikawa et al., 2011b; Fei et al., 2012). It may occur more widely, as it is sometimes misidentified as P. chinensis.

Habitat

Paramesotriton labiatus inhabits a single stream in broadleaf forest with a ground cover of herbaceous plants and vines. The stream is in a valley and is slow-flowing, 3-4 m wide, and shallow. The substrate consists of gravel, scattered small rocks, and semi-submerged, larger rocks. Along the stream are

If Paramesotriton labiatus is the same species as Pachytriton C (see comments below), there is some experience in keeping this animal in captivity (Scholz, 1998). It was captive bred by Henk Wallays in 1994-95. Animals were secretive and strictly nocturnal when kept in an aquarium with a water temperature of 10-17°C. Both sexes were aggressive during the breeding period, but would aggregate under stones without casualties. During this period the male had white spots on the sides of the tail. Tail-fanning was part of the courtship behaviour. Eggs of 5-6 mm diameter were laid singly, in small groups against rocks and in crevices, apparently guarded by a female. The larvae resemble other Paramesotriton larvae in that the edge of the dorsal fin is white, but they lack the white pigmentation on snout and gills of their congeners. Recently metamorphosed juveniles have a granulated skin, red cheeks and a red dorsal stripe, similar to some Cynops pyrrhogaster, and large red areas on the underside (Raffaëlli, 2007).

Comments

Descriptions of morphology, colour and behaviour of a newt species, imported via the pet trade and provisionally named Pachytriton C (Scholz, 1998), match with Paramesotriton labiatus. Most probably the two names refer to the same species. The newt described by Wu et al. (2009) as Paramesotriton ermizhaoi, was relegated to the synonymy of Paramesotriton labiatus by Nishikawa et al. (2011b). These authors ‘found a confusing situation, where most of what had been referred to as the northeastern population of Pachytriton labiatus should have the name Pachytriton granulosus applied; the southwestern population of former Pachytriton labiatus was a distinct species, which they name Pachytriton inexpectatus, and the types of nominal Pachytriton labiatus were conspecific with what had been named Paramesotriton ermizhaoi and not with the populations that had had the name Pachytriton labiatus applied for so long. All literature prior to 2011 should be used with great caution because of this’ (Frost, 2013, quote).

References

Fei et al. (2012); Frost (2013); Nishikawa et al. (2011b);

Raffaëlli (2007); Scholz (1998); Unterstein (1930); Wu et al. (2009).

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Paramesotriton longliensis Li, Tian, Gu & Xiong, 2008 | Longli Warty Newt

Paramesotriton longliensis, female, western Hubei. Photo: Yunke Wu.

Description

The following account is based on the original description by Li et al. (2008b), supplemented with a new record on the species’ occurrence further north (Wu et al., 2010a). A robust newt with granular skin and prominent vertebral ridge; dorso-lateral ridges vaguely present. Head flattened, longer than wide, snout truncated. Tail longer than snout-vent length, high and laterally compressed, with fins on upper- and undersides and ending in a blunt tip. Legs well-developed, hindlimbs a little longer than forelimbs. When adpressed, hindlimbs and forelimbs meet. No toe webbing or fringes, but black sheath at toe-tips.

Paramesotriton longliensis, (uncertain identification; locality unknown). Photo: Henry Janssen.

Wu et al. (2010a) described specimens from a population in western Hubei and noted that the cloaca is prominent in females and conical in shape. These authors also found light coloured lateral stripes in the tail of both males and females, more conspicuous in males than in females. Dorsal colour light brown, occasionally taking on the yellow colour of the substrate; dorsal ridge yellow. Ventral side black, with scattered, irregular, orange-red spots, including one on the underside of the base of each leg. Total length 102-131 mm for males, 105-140 mm for females (Li et al., 2008b). Specimens from the population in western Hubei are larger, males measuring about 14 cm, females 15 cm (Wu et al., 2010a).

Diagnosis

Hind part of upper branchial bone points upwards, resulting in a clearly visible protrusion on both sides of

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Paramesotriton longliensis, (uncertain identification; locality unknown). Photo: Henry Janssen.

the gill vestiges. Skin very rough, warts densely covering much of dorsal and lateral surfaces. Warts on dorso-lateral ridge with yellow or orange tint and sometimes forming discontinuous dorso-lateral stripes. Black cuticle at tip of the toes. Prominent dorsal ridge.

Eggs and larvae

No published information.

Distribution

Paramesotriton longliensis is known from the type locality Shuichang village, Longli County, Guizhou Province, China, at 1,142 m altitude (Li et al., 2008b) and from a river near Shizilu village, Xianfeng County, Hubei, at 787 m elevation (Wu et al., 2010a; Fei et al., 2012). Specimens from southeastern Chongqing, which is geographically intermediate between western Hubei and the type locality in central Guizhou, were initially identified as P. chinensis (Xie et al., 2004). These animals are morphologically similar to those from western Hubei and may belong to the same species. Therefore, the geographic range of P. longliensis probably extends from central Guizhou to western Hubei (Wu et al., 2010a).

Habitat

Paramesotriton longliensis inhabits quiet parts of large reservoirs and the outflows of underground water reservoirs at elevations of 700-1,200 m where the water is clear, and the substrate contains stones, mud and some vegetation (Li et al., 2008b). The population in western Hubei inhabits a large river, ca. 10-20 m wide and 1-2 m deep, in a narrow valley (Wu et al., 2010a). In Hubei, this newt prefers silty substrates and can also be found near river banks after rains. It is often caught with fishes in seine-nets.

Behaviour

Paramesotriton longliensis is usually inactive during the day, hiding under stones, fallen leaves, in the sand or between weeds. It feeds at night, sitting still on the bottom of the water and catching insects, earthworms, shrimp, small fish and snails.

The breeding season extends from mid-April to late June.

Threats and conservation

No published Information.

Observations in captivity

This species can be kept in captivity using similar methods to the other Paramesotriton species (Pasmans et al., in press).

Comments

Despite the large geographic distance between sampling localities (ca. 400 km), the two known populations are genetically similar and are hence considered to belong to the same species. Paramesotriton longliensis is similar to P. zhijinensis, the two species being separated by only a modest genetic distance (Wu et al., 2010a).

Molecular studies based on mitochondrial DNA suggest that Paramesotriton may be divided into two clades: one including P. caudopunctatus, P. longliensis, P. zhijinensis, P. maolanensis and P. wulingensis, the other containing the remaining species of Paramesotriton (Zhao et al., 2008; Wu et al., 2010a; Pyron & Wiens, 2011; Gu et al., 2012a, 2012b).

References

Fei et al. (2012); Freytag (1983); Gu et al. (2012a, 2012b);

Li et al. (2008b); Pasmans et al. (in press); Pyron & Wiens (2011); Wang et al. (2013); Wu et al. (2010a); Xie et al. (2004); Zhao et al. (2008).

Paramesotriton maolanensis Gu, Chen, Tian, Li & Ran, 2012 | Maolan

Warty Newt

Description

A large-bodied species of Paramesotriton, with smooth skin, short limbs and degenerate external eyes, with vestigial lenses. The following is based on the original species description (Gu et al., 2012a). Head longer than wide, elongated snout. Head strongly oblique in profile. Skull broad, snout short and truncated, extending beyond lower jaw. Limbs frail, hindlimbs longer and thicker than forelimbs. Mid-dorsal ridge present, extending into a caudal fin. Hyoid apparatus differs from congeners: the ceratobranchial is bony, rather than cartilaginous; the epibranchial bone diverges, forming a Y-shape; the two ends of the Y-shape join the first and second ceratobranchial bones. Male cloaca a 6-7 mm long slit, with a pair of glands visible inside; female cloaca small and oval-shaped without glands visible.

Colour is brown-black; dorsal ridge with non-continuous yellow mottling. Venter and chin with large, irregular orangered spots; smaller, yellow spots on the sides of venter and chin. Total length 177-192 mm in males, 197-208 mm in females (Gu et al., 2012a).

Diagnosis

Paramesotriton maolanensis can be distinguished from other Paramesotriton species by the following combination of characteristics: large body-size; smooth skin without granular warts; external eyes degenerate; prominent mid-dorsal ridge; head broad and long; very long horny protuberances behind the head.

Eggs and larvae

No published information. 299

Paramesotriton maolanensis, Maolan National Nature Reserve, Libo County, Guizhou (type locality). Photo: Gu Xiaoming.

Distribution

Paramesotriton maolanensis has been described from the Maolan Natural Nature Reserve, Libo County, Guizhou Province, China.

Habitat

This species has so far only been found in a 60 m² deep pool, surrounded by vegetation, situated in a karstic forest. The pool is fed by water from springs and caves, connected to an underground river. The water is clear and about 17°C year-round. The newts usually stay on the bottom of the pool and are hard to find. The pool supports large quantities of hexapods, shrimps, crabs and fishes.

Comments

Molecular studies based on mitochondrial DNA suggest that Paramesotriton may be divided into two

Paramesotriton maolanensis, ventral side, Maolan National Nature Reserve, Libo County, Guizhou (type locality). Photo: Gu Xiaoming.

clades: one including P. caudopunctatus, P. longliensis, P. zhijinensis, P. maolanensis and P. wulingensis, the other containing the remaining species of Paramesotriton (Zhao et al., 2008; Wu et al., 2010a; Pyron & Wiens, 2011; Gu et al., 2012a, 2012b; Wang et al., 2013). Paramesotriton maolanensis is a bizarre-looking animal. Like the species most closely related to it, P. zhijinensis and P. longliensis, P. maolanensis lives in an environment of karst caves and underground rivers. Of these species, P. maolanensis is most associated with a subterranean life. It has probably lost the ability to see and shows several paedomorphic characteristics.

References

Gu et al. (2012a, 2012b); Pyron & Wiens (2011); Wang

et al. (2013); Wu et al. (2010a); Zhao et al. (2008).

Paramesotriton wulingensis Wang, Tian & Gu, 2013 | Wuling Warty Newt Description and diagnosis

A slender warty newt, most similar to Paramesotriton caudopunctatus. It has been described as a distinct species on the basis of molecular data and a number of anatomical differences (Wang et al., 2013). Body colour is a deeper dark brown, dorsal tubercles are larger, and dorsal ridges are lower than in P. caudopunctatus from Leishan (type locality). The skull differs from that of P. caudopunctatus: the suture in the middle of the nose is deeper, the suture lines between prefrontal and nasal have a different shape, and the frontosquamosal arc is structured differently in the two species. The frontal branch of the pterygoid is relatively longer in P. wulingensis than in P. caudopunctatus.

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Total length 124-139 mm in males, 113-137 in females (Wang et al., 2013).

Eggs and larvae

Probably similar to Paramesotriton

caudopunctatus.

Distribution

This species is described from the Wuling Mountains: Youyang in Southern Chongqing and Jiankou in northeastern Guizhou (Wang et al., 2013), areas formerly regarded as the northern part of the range of Paramesotriton caudopunctatus (Fei et al., 2012).

Paramesotriton wulingensis, holotype, Youyang, Chongqing. Photo: Gu Xiaoming.

Paramesotriton wulingensis, holotype, ventral side, Youyang, Chongqing. Photo: Gu Xiaoming.

Habitat

Comments

Behaviour

References

Like Paramesotriton caudopunctatus, this species inhabits mountain streams of varying sizes and the surrounding habitats in forested areas. No published information. Probably similar to P. caudopunctatus.

Paramesotriton wulingensis is closely related to Paramesotriton caudopunctatus. See comments section under that species for a note on the taxonomic position. Fei et al. (2012); Wang et al. (2013).

Paramesotriton yunwuensis Wu, Jiang & Hanken, 2010 | Yunwu Warty Newt Description

A large, robust newt. Head longer than broad, wider than neck. Snout truncate, projecting beyond mandible. Head slopes steeply downward anteriorly in lateral view. Labial fold welldeveloped. Vomerine tooth patch-shaped. Paratoids prominent.

Gular fold present, numerous longitudinal wrinkles on throat. Vertebral ridge flat and inconspicuous. Numerous transverse wrinkles on flanks, venter and lateral sides of tail-base. Large warts on head and dorso-lateral ridges. Four fingers and five toes, no webbing. Tail laterally compressed; dorsal caudal fin evident on posterior half of tail; ventral caudal fin inconspicuous. Tail-tip rounded. Cloaca with transverse wrinkles.

Paramesotriton yunwuensis, male paratype, Luoding, Guangdong. Photo: Yunke Wu.

Paramesotriton yunwuensis, male paratype, ventral side, Luoding, Guangdong. Photo: Yunke Wu.

The following account is based on the original description by Wu et al. (2010a).

301

Dorsal colouration ranges from reddish-brown to olive-brown. Ventral colour pattern varies from black background with a few orange blotches to orange background with numerous small black flecks. Bright ventral blotches irregular without a network of black lines. Males have a bluish-white caudal stripe on the posterior half of the tail during the breeding season, and few papillae on the cloacal wall. Adult females have a more conspicuous vertebral ridge, a smaller and shorter cloacal opening, and no papillae on the cloacal wall. Total length 165-186 mm in males, 145-161 mm in females. Males on average larger than females.

Diagnosis

A large, robust newt with flat or low vertebral ridge, lightly granular warts, long and shallow tail and short limbs. When extended rostrally, the forelimb barely reaches the posterior margin of the eye. When forelimb and hindlimb are adpressed, tips of digits just meet. Paramesotriton yunwuensis is similar to P. guangxiensis in having short limbs, but differs from it in its much larger body size and long, narrow tail.

Eggs and larvae

No published information.

Distribution

This species is described from Nanchong village, Fuhe, Luoding city, Guangdong Province, China. It probably occurs more widely in the streams in the Yunwu Mountains, located in the southwestern corner of Guangdong.

Habitat

Paramesotriton yunwuensis inhabits large pools (4×4 m) along a montane stream at mid-elevation in the Yunwu Mountains. Water depth reaches about 3 m. The pool substrate comprises submerged boulders, small rocks and coarse gravel. Pools are connected by currents of cold, clear, slow-moving water. Broadleaf forests grow along the site, but the stream is not covered by the canopy. Several species of fish coexist with this newt.

Behaviour

During the day Paramesotriton yunwuensis can be seen crawling actively on the deep pool bottom. At night they can be found at the shallower pool edges. The breeding season is probably around May.

Threats and conservation

No detailed published information. This species is caught and sold to tourists, an activity that is probably not sustainable. Conservation measures are required.

Comments

Based on mitochondrial DNA sequence data, Paramesotriton yunwuensis is the sister species of P. guangxiensis (Wu et al., 2010a). Together they form the sister lineage to P. fuzhongensis (Pyron & Wiens, 2011). In conjunction with the three species’ geographic distributions, the Pearl River may act as a geographic barrier to speciation.

References

Pyron & Wiens (2011); Wu et al. (2010a).

Paramesotriton zhijinensis Li, Tian & Gu, 2008 | Zhijin Warty Newt Description

The following is based on the description by Zhao et al. (2008), which was published one month after what appears to be the original description in Chinese (Li et al., 2008a). A fairly large, robust salamander. Head moderately sloping in profile, relatively large and flat; skull broad with maxillaries oriented at an angle to the body axis; head length distinctly longer than head width. Snout short, truncate, extending beyond lower lip. Nostrils located on the tip of the snout. Gular fold present. Eyes are relatively large and round. Upper lips thick, fleshy and overlapping lower lip from eye to snout. Three tubercular dorsal ridges, one midline and two lateral, extending from behind the head to the tail-base. Glands and warts cover much of the dorsal and ventral surfaces. No webbing on fingers and toes. Tail slender, laterally compressed; dorsal tail-fin and indistinct ventral tail-fin present; posterior end of tail rounded in lateral profile, not pointed.

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Salamanders of the Old World | Paramesotriton

Dorsal colour is brown-black. Three tubercular dorsal ridges with non-continuous yellow mottling. Dorsal stripes are variable, sometimes indistinct and with tiny light yellow spots. Large, irregular orange-red spots on venter, chin, underside of axillae, cloaca and tail; some weak, smaller spots interspersed on venter. Orange-red spots diminish in size posteriorly on underside of tail-base. Distinct yellow postocular stripe located near corner of mouth. Most adult animals have vestiges of gills or gill filaments. The original description does not record morphological differences between male and female. Total length 103-127 mm for males, 102-125 mm for females (Li et al., 2008a).

Li et al. (2008a) also reported this newt from slow-flowing, shallow streams at elevations of 1,300-1,400 m.

Habitat

The pond in which the animals were found has clear water at 16°C year-round. The pond has large quantities of algae and fishes.

Behaviour

Given its tendency to neoteny, Paramesotriton zhijinensis is probably mainly aquatic. In the daytime the animals move to the bottom of the pond, in the evening they move to the littoral region to feed. The breeding season extends from mid-April to late June.

Threats and conservation

Until more is known about salamander populations in the neighbourhood, the type locality is the only known locality where the species occurs. For this reason alone it probably is very vulnerable.

Comments

Paramesotriton zhijinensis, Zhijin County, Guizhou (type locality). Photo: Che Jing.

Diagnosis

This species can be distinguished from other Paramesotriton species by the following combination of characters: Distinct yellow postocular stripe and two noncontinuous, dorsolateral stripes on dorsolateral ridges. Neoteny is common with most adult specimens having vestigial gills and gill filaments (Zhao et al., 2008).

Eggs and larvae

Eggs have not been described. According to Zhao et al. (2008) colouration of the larvae is similar to adults except that the spots are fewer in number and larger (unlike other Paramesotriton species). A 61.8 mm long larva, collected in May, was uniformly black on the upperside.

Distribution

All specimens were found in an artificial pond (Shuangyan Pond), fed by an underground spring, surrounded by mountains, at an altitude of 1,310 m in Zhijin County, located on the Guizhou Plateau, China (Li et al., 2008a; Zhao et al., 2008).

Zhao et al. (2008) described lines of scent glands on the snout, along the back and along the ventral surface. The glands emitted a small amount of white, malodorous secretion when touched. According to Zhao et al. (2008) the function of these glands remains unknown. It seems unlikely that the glandular system of this species is different from that of other Paramesotriton species and similar pits are also present in other Paramesotriton species. Although the authors do not describe the odour, it may well be similar to the pungent smell that many newt species – including species of Paramesotriton – are known to secrete when handled. The scent emitted by newts in distress has been likened to that of Parsley root.

Molecular studies based on mitochondrial DNA suggest that Paramesotriton may be divided into two clades: one including P. caudopunctatus, P. longliensis, P. zhijinensis, P. maolanensis and P. wulingensis, the other containing the remaining species of Paramesotriton (Zhao et al., 2008; Wu et al., 2010a; Pyron & Wiens, 2011; Gu et al., 2012a, 2012b; Wang et al., 2013). Paramesotriton zhijinensis and P. longliensis look similar and are sister species, and the genetic divergence between them is small (Wu et al., 2010a). More data are needed to assess the relationship between these two species.

References

Fei et al. (2012); Freytag (1983); Gu et al. (2012a, 2012b);

Li et al. (2008a); Pyron & Wiens (2011); Wang et al. (2013); Wu et al. (2010a); Zhao et al. (2008).

303

Pleurodeles Michahelles, 1830 Two premaxillae, fronto-squamosal arch completely ossified. Vomerine teeth in two longitudinal rows, diverging in a V- or U-shape. Tongue small and round, free at the sides. Tail long and compressed laterally. Head broad, large and flattened. Skin rough, with small warts. Pleurodeles is adapted to life in standing water (Thorn, 1969; García-París et al., 2004). The genus Pleurodeles is distributed in southern Europe and North Africa and is most closely related to the East-Asian genera Echinotriton

and Tylototriton (Hayashi & Matsui, 1989; Weisrock et al., 2006).

Pleurodeles nebulosus (Guichenot, 1850) Pleurodeles poireti (Gervais, 1835) Pleurodeles waltl Michahelles, 1830

References

García-París et al. (2004); Hayashi & Matsui (1989);

Thorn (1969); Weisrock et al. (2006).

Pleurodeles nebulosus (Guichenot, 1850) | Algerian Ribbed Newt Description

Pleurodeles nebulosus is a medium-sized Pleurodeles. Head strongly flattened, about as wide as long, with rounded snout. Eyes rather small. Body somewhat flattened. It usually has 14 presacral vertebrae, and lacks the sharp rib tips that project through the skin as in P. waltl. Hind legs somewhat stronger than front legs. During the breeding season, when in water, dorsal and ventral tail-fins develop. Males have longer tails and longer forelimbs than females (Schleich et al., 1996). Most P. nebulosus have a U-shaped row of palatine teeth (Carranza & Wade, 2004). Skin very granular. Colour brown with a greenish or yellowish tinge. Irregular dark patches without distinct borders. Head, back and tail with very small yellow or brown dots. Sides yellowish, but without the 8-10 yellowish spots as in P. waltl. Dorsal tail-fin and upperside of digits yellow to orange or pale; underside of limbs and body pale grey, belly often with round, dark brown spots.

In the breeding season males have a swollen cloaca and reddishbrown nuptial pads on the inner side of the forelimbs. Males are a little smaller than females. Tail longer than snout-vent length in adult males, shorter in females and juveniles (Schleich et al., 1996). Total length up to 180 mm, exceptionally reaching 230 mm (Carranza & Wade, 2004). Animals occurring south of the Medjerda Mountains tend to be larger in size than more northerly specimens (Pasmans et al., 2002; Carranza & Arnold, 2004).

Diagnosis

A medium-sized Pleurodeles lacking the 8-10 yellowish glandular swellings along the sides of the body that are characteristic of Pleurodeles waltl. It is genetically differentiated from the closely related P. poireti and P. waltl and is also recognisable by several morphological characteristics.

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Salamanders of the Old World | Pleurodeles

Pleurodeles nebulosus, Tabarka, Tunisia. Photo: Frank Pasmans.

It is smaller than P. waltl and larger than P. poireti. It differs from P. waltl in usually having 14 instead of 15 presacral vertebrae, in lacking sharp rib tips that project through the skin, and in the presence of a tubercular process on rib 3 and often traces of this structure on ribs 1 and 2. Sexual dimorphism in P. nebulosus is less pronounced than in P. poireti. Most P. nebulosus have a U-shaped row of palatine teeth, unlike P. poireti which usually have a V-shaped row of palatine teeth. The general shape of the skull, snout and contour of the jaws differs between P. nebulosus and P. poireti (Carranza & Wade, 2004).

Eggs and larvae

Eggs and larvae are similar to those of Pleurodeles waltl. In Tunisia, larvae were found from the beginning of December to the first half of April (Sicilia et al., 2009).

Distribution

This species occurs across northern Tunisia and Algeria, but is absent from the Edough Peninsula in north-

piles near breeding habitat (Pasmans et al., 2002). Adults and larvae were observed in water bodies with temperatures ranging from 10-26.8°C (Sicilia et al., 2009). Interestingly, the defensive posture is different from that observed in P. waltl. It does not bend its back so that the sharp tips of the ribs pierce the skin. It just flattens its body and curls its tail, and no skin secretions have been observed (Pasmans et al., 2002). The reproductive behaviour is similar to that of Pleurodeles waltl, although Schleich et al. (1996) reported a slight difference in the behaviour pattern leading to spermatophore transfer. The rotation of the mating pair with forelimbs locked and heads pointing in opposite directions, which these authors consider typical for P. nebulosus has however also been observed in P. waltl (Arnold, 1977; Houck & Arnold, 2003; pers. obs.).

Threats and conservation

The range of Pleurodeles nebulosus.

ern Algeria, which is home to P. poireti (Carranza & Wade, 2004; Veith et al., 2004; IUCN, 2013). Its distribution is fragmented due to the scarcity of suitable habitat.

Habitat

Pleurodeles nebulosus habitats are mainly found in flood plains (Pasmans et al., 2002). Reproductive sites mostly consist of wetlands with a temporary hydroperiod such as swamps, marshes, ponds, flooded fields, pools and road ditches. It occurs at altitudes ranging from sea level up to 457 m in the Medjerda Mountains (Sicilia et al., 2009). The highest altitude known in Tunisia is 689 m, near Forêt des Chênes, where Pasmans et al. (2002) found a juvenile specimen.

Behaviour

Little is known about the ecology and behaviour of this species. Individuals were found under stones and in clay

There is no direct information on threats to this species. Locally it may be common (Pasmans et al., 2002), but suitable habitats are disappearing or deteriorating due to urbanisation, the building of hotels, and infilling of cattle watering holes (Ben Hassine, 2011). Further survey work is necessary to assess its current population status. Pleurodeles nebulosus is considered Vulnerable (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

Pleurodeles nebulosus has been bred in captivity and, like P. waltl, can be kept in water all year round (Thorn, 1969; Raffaëlli, 2007).

Comments

Most of the specimens from North Africa previously referred to as P. poireti belong to P. nebulosus, true P. poireti being restricted to the Edough Peninsula in northern Algeria (Carranza & Wade, 2004).

References

Arnold (1977); Ben Hassine (2011); Carranza &

Arnold (2004); Carranza & Wade (2004); Houck & Arnold (2003); IUCN (2013); Pasmans et al. (2002); Raffaëlli (2007); Schleich et al. (1996); Sicilia et al. (2009); Stuart et al. (2008); Thorn (1969); Veith et al. (2004).

Pleurodeles poireti (Gervais, 1835) | Edough Ribbed Newt Description

Pleurodeles poireti is a dwarf form of Pleurodeles, that is genetically differentiated from the closely related P. nebulosus and P. waltl and is also morphologically recognisable by its smaller overall size. It differs from P. waltl in usually having 14 instead of 15 presacral vertebrae, in lacking sharp rib tips that project through a row of glandular swellings on the flanks, and in having a tubercular process on rib 3 and often traces of this structure on ribs 1 and 2.

Total length not exceeding 129 mm, but captive animals can grow larger (Henry Janssen, pers. comm.). Males significantly smaller than females (Carranza & Wade, 2004).

Diagnosis

A dwarf Pleurodeles lacking the 8-10 yellowish glandular swellings along the sides of the body that are characteristic of Pleurodeles waltl. Differs from P. waltl in the number of presacral vertebrae, usually 15 in P. waltl and 14 in 305

Pleurodeles poireti, captive specimen. Photo: Henry Janssen.

P. poireti. Sexual dimorphism in P. poireti is more pronounced than in P. nebulosus. Most P. nebulosus have a U-shaped row of palatine teeth, unlike P. poireti which usually have a V-shaped row of palatine teeth. Pleurodeles poireti differs from P. nebulosus in the general shape of the skull, snout and contour of the jaws (Carranza & Wade, 2004).

Eggs and larvae

Eggs and larvae are similar to those of Pleurodeles waltl (Rafaëlli, 2007).

Distribution

This species is restricted to the Edough Peninsula and surrounding lowland areas in Algeria, but the

The range of Pleurodeles poireti.

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precise extent of its distribution is unknown (Carranza & Wade, 2004; Samraoui et al., 2012).

Habitat

Pleurodeles poireti is probably largely aquatic and dependent upon cisterns, ponds, swamps and other wetlands (IUCN, 2013).

Behaviour

This species has a similar breeding strategy to P. nebulosus, depositing eggs, and completing its larval development in water (Raffaëlli, 2007). Its reproductive behaviour has not been described, but is thought to be similar to that of P. waltl and P. nebulosus (Henry Janssen, pers. comm.).

Pleurodeles poireti, captive specimens in amplexus. The male carries the female on his back, hooking his forelimbs around hers. Photo: Henry Janssen.

Threats and conservation

From 2006 onward a poorly understood strong decline of the species has been observed in localities where it was previously abundant. Other amphibian species in the area have not shown a similar decline (Samraoui et al., 2012). Further survey work is necessary to assess its current population status. It is considered Endangered (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

Pleurodeles poireti from Annaba have been bred in captivity by Raffaëlli (2007). Raised from larvae hatched in the Lacroix laboratory (Jussieu, France) the first amplexus was observed in nine month old animals kept at 22°C. Eggs were laid in several batches around plants and on the bottom of the tank at 16°C after replacing half the tank volume with fresh water.

Comments

Most of the animals from North Africa previously referred to as Pleurodeles poireti actually belong to P. nebulosus, true P. poireti being restricted to the Edough Peninsula in northern Algeria (Carranza & Wade, 2004). Unless accompanied by locality data, descriptions of habitat and behaviour such as in Thorn (1969) and Schleich et al. (1996) cannot be assigned to P. poireti sensu stricto with certainty (Carranza & Wade, 2004).

References

Carranza & Wade (2004); IUCN (2013); Raffaëlli (2007);

Schleich et al. (1996); Samraoui et al. (2012); Stuart et al. (2008); Thorn (1969).

Pleurodeles waltl Michahelles, 1830 | Ribbed Newt Description

A very large, stockily built salamander. Head strongly flattened, a little longer than wide. Snout rounded. Eyes small and situated high on the head. Vomerine tooth rows diverging backward, usually in inverted V- or U-shape. Gular fold present. Body strong and stout, without distinct neck, trunk slightly flattened and no dorsal crest. 15 presacral vertebrae; tubular process on rib 3 and traces of this structure on ribs 1 and 2 (Carranza & Arnold, 2004). There is a longitudinal row of 8-10 yellowish glandular warts on each side

of the body corresponding to the position of the directly underlying ribs. Tail strongly laterally compressed. Tail length equals snout-vent length in young individuals, but is longer than snout-vent length in adults, and proportionally longer in males than females. Dorsal and ventral tail-fins low, but higher in males during the reproductive season. Tail ends in a blunt tail-tip. Limbs are short and stocky. Digits long, without webbing. Skin granulated, except on the middle part of the belly.

Pleurodeles waltl, north of Chefchaouen, Morocco. Photo: Max Sparreboom.

307

Pleurodeles waltl, subadult, south of Kenitra, Morocco. Photo: Max Sparreboom.

Dorsal side is greyish-yellow to olive-green with dark brown blotches and small black dots covering the warts. Older animals are darker. Males may tend to be more reddish, and females brownish. The glandular warts along the flanks may be whitish or yellow-orange. Ventral side very light coloured, whitish or yellowish, generally with black spots or marblings. Underside of the tail yellow or orange (Thorn, 1969). In males the forelimbs are stronger than the hindlimbs. In the breeding season males develop dark brown, strongly keratinized nuptial pads on the inner sides of the front legs. Most conspicuous difference between the sexes is the size and shape of the forelimbs, which are also stronger in males than in females outside the breeding season. Usually between 17-30 cm long (Thorn, 1969). Total maximum length 312 mm for males, 286 mm for females (Salvador & García-París, 1999).

Diagnosis

A very large salamander with 8-10 yellowish rounded spots along the sides of the body. Differs from Pleurodeles nebulosus, which occurs in northern Tunisia and Algeria in the number of presacral vertebrae, usually 15 in P. waltl and 14 in P. nebulosus. Pleurodeles nebulosus lacks the rounded yellow spots and the ability to pierce its skin with the rib tips. Pleurodeles poireti resembles P. nebulosus in this respect and is the smallest species in the genus (Carranza & Wade, 2004).

Eggs and larvae

A female may lay a clutch of ca. 150 eggs in her first year of sexual maturity, while a four year old female may deposit a clutch of some 700-800 eggs, although higher numbers (800-2,000) have been recorded (Schleich et al., 1996;

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Pleurodeles waltl, male in breeding season with rugosities (nuptial pads) on forelimbs. Nisa, Portugal. Photo: Max Sparreboom.

IUCN, 2013). The female may deposit her entire clutch in 2-3 days. Eggs are attached to plants or stones in small groups of about a dozen eggs and are produced at about 10-15 min intervals. Ovum diameter is very small: 1.7-2 mm, the animal pole being dark, and the vegetal pole light in colour. The diameter of the entire egg is 5-7 mm (Thorn, 1969; Salvador & García-París, 1999). Larvae hatch after ca. 13 days at a length of 11 mm (at a water temperature of 18°C). On the 20th day the balancers start to reduce in size, and by the 40th day have almost disappeared. A fully developed larva has a high dorsal fin starting directly behind the head. Head relatively large. Irregular grey spots on body and fin. The tail ends in a fine tip. The development time from egg to metamorphosis is extremely variable. At temperatures between 7-27°C larvae of 6.5-8 mm long were reported to hatch after 3-26 days (Salvador & García-París, 1999). After 3-4.5 months the larvae metamorphose at sizes varying from 53-110 mm, probably depending on density of larvae, availability of food and water in the breeding pond, and temperature (Salvador, 2009). Some larvae overwinter and may reach a considerable size. Giant larvae have been documented and neoteny occurs, both in the wild and in the laboratory. The development of eggs and larvae is well-documented (Gallien & Durocher, 1957; Shi & Boucaut, 1995) because P. waltl is often used in cellular and molecular embryological studies, and has even been used for experiments in space. After one year the metamorphosed juveniles measure 14 cm, and reach 17.5 cm after two years (Salvador & García-París, 1999). Animals of 16 months old are capable of reproducing. Pleurodeles waltl normally reaches an age of 8-12 years, but in captivity may exceptionally live for 20 or even 25 years (Thorn, 1969; Salvador & García-París, 1999).

found 30-50 cm deep underground (Salvador & García-París, 1999).

Behaviour

In the parts of its range where waters are frozen in winter, such as around Leon, reproductive activity starts as soon as the ice disappears in mid-February. In more southwestern parts of its range breeding takes place from OctoberMay with the onset of the autumn rains, and in Catalonia from October-March (Salvador & García-París, 1999). In Morocco animals could be found in January, in ponds that were partly frozen at night (pers. obs.). They are active mostly at night. Pleurodeles waltl is a voracious salamander that will eat any prey that can be overwhelmed, including insects and their larvae, worms, crustaceans, and amphibian larvae, including conspecific eggs and larvae. The salamander itself is taken by a range of predators, such as many species of birds of prey, herons, storks, snakes (Natrix maura), rats and wild boar (Salvador & García-París, 1999).

The range of Pleurodeles waltl.

Distribution

This species occurs in central and southern Iberia, and in the coastal plain of northern and north-western Morocco. It is essentially a lowland species becoming rare above 900 m altitude, although it has been found at 1,565 m in the Sierra de Loja, Granada, Spain (IUCN, 2013) and 1,100 m in Oulmès, Morocco (Schleich et al., 1996). The close resemblance of Moroccan P. waltl populations to those from south-eastern and east Iberia indicates that their ancestors reached Africa comparatively recently and long after the disappearance of the land connection associated with the Messinian Salinity Crisis (5.96-5.33 million years ago). Because amphibians are very unlikely to cross salt water, the Moroccan populations may result from anthropogenic introductions that could have been accidental (Carranza & Arnold, 2004; Veith et al., 2004).

When threatened or harassed by a predator (or by man), P. waltl releases a viscous milky, poisonous secretion onto its skin surface. In addition it assumes an immobile defensive posture, arching its body and thereby stretching the skin of the lateral orange warts. In this posture the skin is contracted towards the mid-dorsum and the ribs are rotated so as to point backwards. As a result, the exceptionally long and sharply pointed rib tips pierce the body wall and project freely from the sides of the

Habitat

Pleurodeles waltl is a highly aquatic species of Mediterranean-type habitats including scrub, open woodland and cultivated land. It occurs in a range of different water bodies such as ponds, dayas, wadis, lakes, ditches and slowmoving streams, often temporary in nature, with or without vegetation cover. The adults are mostly found under stones or in mud in their aquatic habitats, or sheltering under cover on land if the wetland dries up. They may occur in slightly modified aquatic and terrestrial habitats (Salvador & García-París, 1999; IUCN, 2013). In summer, when the water dries up, they take refuge in the muddy soil of the pond, or under stones, in caves, or in artificial walls away from the pond. In Morocco, animals have been

Pleurodeles waltl, habitat, south of Kenitra, Morocco. Photo: Max Sparreboom. 309

trunk as spines. The skin in the penetrated areas lacks permanent pores through which the ribs can project and is pierced anew every time this antipredator posturing is assumed (Heiss et al., 2009). The exposed tips of the ribs may wound any predator that tries to grab the wriggling salamander, making it more vulnerable to the poisonous secretions. There are no reports of direct observations of this behaviour in the wild. Courtship and mating take place in water. A sexually active male holds his forelimbs up and slightly bent, while swimming towards a female. He captures the female by rushing beneath her and clasping her forelimbs with his forelimbs. While hooked onto the female in this ventral amplexus, a male can transport the female by swimming with his tail and walking with his hindlimbs, and thus monopolise his access to the female. An intruding rival male may attempt to dislodge the male by grappling for possession of the female and thus interfere with his courtship. Irrespective of the presence of rival males, the pair may stay in amplexus for hours or even days. During amplexus the male’s everted cloaca is sometimes placed on the

female’s snout and sometimes the male wraps his tail around the female. As a prelude or alternative to amplexus the male may perform a tail-fanning display in front of the female. For spermatophore transfer the male releases one forelimb and restrains the female using the other forelimb. The male swings his sacrum through an arc of 180° or more by pivoting about the contralateral forelimb. Sperm transfer is accomplished as the pair pivots about their interlocked forelimbs while facing each other head to head (Arnold, 1977; Houck & Arnold, 2003). The male deposits a spermatophore on the substrate and the female picks up the sperm cap with her cloaca. A male may deposit up to seven spermatophores during a single mating (Salvador & García-París, 1999). Males tend to stay in water much longer than females (Salvador, 2009).

Threats and conservation

This species is generally threatened by loss of aquatic habitats through drainage, agrochemical pollution, the impact of livestock (in North African dayas), eutrophication, domestic and industrial contamination, and infrastructure development. It has largely disappeared from coastal areas in Iberia and Morocco close to tourist developments and other densely populated areas, such as Madrid. Introduced fish and crayfish (Procambarus clarkii) are known to prey on eggs and larvae of Pleurodeles, and are implicated in its decline. Mortality on roads has been reported to be a serious threat to some populations. The species is listed as Near Threatened (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

The Ribbed Newt can be kept and bred in captivity. It is best kept entirely aquatic all year round, in large tanks with vegetation at temperatures of 6-8°C in winter and 18-25°C in summer. Breeding often follows the addition of fresh water to the tank (Raffaëlli, 2007).

Comments

Good Spanish accounts of the Ribbed Newt with extensive documentation are given by García-París et al. (2004) and Salvador (2009). Beukema et al. (2013) discuss the distribution of Pleurodeles in Northern Africa.

References Pleurodeles waltl courtship. After release of the female from ventral amplexus, the pair pivots around their right forelimbs, which are still hooked. This stage precedes the deposition of the spermatophore by the male and sperm pick-up by the female. Captive animals from Cadiz, Spain. Photo: Max Sparreboom.

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Arnold (1977); Beukema et al. (2013); Carranza & Arnold

(2004); Carranza & Wade (2004); Gallien & Durocher (1957); García-París et al. (2004); Heiss et al. (2009); Houck & Arnold (2003); IUCN (2013); Raffaëlli (2007); Salvador (2009); Salvador & García-París (1999); Schleich et al. (1996); Shi & Boucaut (1995); Stuart et al. (2008); Thorn (1969); Veith et al. (2004).

Salamandra Garsault, 1764 Salamanders belonging to this genus are robust, terrestrial animals with a smooth, shiny skin, well-defined paratoids and a relatively short tail, usually shorter than snout-vent length. Premaxillaries paired, each with a long posterior projection separating the small nasals. Bony frontosquamosal arch absent. Vomeropalatine teeth in two longitudinal S-shaped curves beginning ahead of the choanae. Tongue oval, almost round, free at the sides. Tail almost cylindrical and slightly compressed (Thorn, 1969). Colours predominantly black and yellow, and very variable between and within populations of the same species or subspecies. There are no seasonal differences in body shape or colouration. The salamanders do not enter water, except for the females when depositing larvae. Some forms do not enter water at all and give birth to fully metamorphosed young. Salamandra species are moderate- to large-sized with total lengths varying from 13-30 cm. The genus Salamandra is sister to Lyciasalamandra (Özeti, 1967; Steinfartz, 2004). Unlike Lyciasalamandra and Mertensiella, males of Salamandra do not have keratinized epidermal projections covering the back (with the exception of some forms of Salamandra algira). Lungs are normally developed. The tongue does not have a projection mechanism. Limbs robust with four fingers and five toes, no toe-webbing (except vestigial webbing in S. lanzai). Males are often smaller than females and have a swollen cloaca in the breeding season. Mating takes place on land. Insemination of the female is preceded by a ventral amplexus similar to that of Chioglossa, Lyciasalamandra and Mertensiella (Thorn, 1969). The genus Salamandra occurs mainly in Europe, with some species reaching northern Africa, Turkey and the Middle East.

The genus Salamandra consists of at least six morphologically and genetically distinct species, which split between 5-13 million years ago (Steinfartz et al., 2000; Pyron & Wiens, 2011; Frost, 2013). Several subspecies are also recognised, most of them in Salamandra salamandra. The evolutionary history of Salamandra is complex and the taxonomic status of a number of these forms is under debate. Several taxa formerly recognised as subspecies of the Fire Salamander (Salamandra salamandra) on the basis of morphological criteria have been raised to full species rank, mainly on the basis of genetic analysis, but supported by morphological and distributional data. Fire Salamanders generally have a contrasting yellow-black colour. The two Alpine Salamander species are entirely black, with the exception of two subspecies of Salamandra atra, which have a pattern of yellowish-white patches on the back. These species are smaller than most Fire Salamanders (Steinfartz, 2004). Viviparity occurs in several lineages of Salamandra salamandra and S. algira. It is the sole mode of reproduction in Salamandra atra and S. lanzai, and most probably developed independently as an adaptation to habitats unsuitable for larval development (Velo-Antón et al., 2007).

Salamandra algira Bedriaga, 1883 Salamandra atra Laurenti, 1768 Salamandra corsica Savi, 1838 Salamandra infraimmaculata (Martens, 1885) Salamandra lanzai Nascetti, Andreone, Capula & Bullini, 1988 Salamandra salamandra (Linnaeus, 1758)

References

Frost (2013); Özeti (1967); Pyron & Wiens (2011); Stein-

fartz (2004); Steinfartz et al. (2000); Thorn (1969); Velo-Antón et al. (2007).

Salamandra algira Bedriaga, 1883 | North African Fire Salamander Description

Characterised by a more slender body form than the central European Fire Salamander (Salamandra salamandra) with a relatively long tail. Tail laterally somewhat flattened. Relatively long fore legs and flatter toes than European Salamandra species. Yellow spots few in number and arranged irregularly (Bons & Geniez, 1996; Schleich et al., 1996). Almost no yellow spots on ventral side. Four subspecies have been named on the basis of morphological, molecular and ecological differences (Beukema et al., 2010; 2013).

Salamandra algira algira Bedriaga, 1883 A fairly large salamander, reaching 24 cm, with alternating yellow blotches and small red spots along head, body and tail.

Short head with rounded snout and small paratoids. Formerly thought to occur from the Rif Mountains and Middle Atlas in Morocco in the west to the Edough peninsula in Algeria (the type locality), the range of the nominate subspecies is now tentatively restricted to the Algerian populations (Escoriza & Comas, 2007; Beukema et al., 2013). Salamandra algira spelaea Escoriza & Comas, 2007 A slender salamander, moderately sized (ca. 17-23 cm). Head flat, longer than wide with prominent eyes. Snout round, long limbs, long fingers and toes. Tail a little shorter than snout-vent length. Background colour jet black with scattered rounded or elongated yellow blotches, not arranged in bands. Small red spots 311

Salamandra algira splendens, Taza. Photo: Max Sparreboom.

around paratoids, eyes, flanks and on limbs and tail. Occasional white spots on lateral and ventral sides. Ventral side black. This form is restricted to the Beni Snassen mountain range, north-eastern Morocco, where it has been observed near water bodies on limestone outcrops and granite soils at altitudes between 600-1,300 m (Escoriza et al., 2006; Escoriza & Comas, 2007). Salamandra algira splendens Beukema, de Pous, Donaire-Barroso, Bogaerts, Garcia-Porta, Escoriza, Arribas, El Mouden & Carranza, 2013 A large, slender salamander, (215 mm total length). Head flat and elongated, 1.5 times longer than wide; long limbs, fingers and tail; black colouration with rounded or elongated yellow markings and red discolouration. It deposits larvae in small water bodies, from October-May. The range of S. a. splendens is restricted to the western and central Rif Mountains and the north-eastern Middle Atlas Mountains (Beukema et al., 2013).

Salamandra algira tingitana, Taghramt. Photo: Max Sparreboom. 312

Salamanders of the Old World | Salamandra

Salamandra algira tingitana Donaire-Barroso & Bogaerts, 2003 Characterised by relatively small total length (21 cm for males, 18 cm for females). Colouration usually dull with a background showing shades of seal-brown. Yellow on tail reduced, four spots on the head, sometimes two. The yellow blotches can disappear and turn a dull shade of grey-white (hypoluteism). Absence of red colouration and tendency to melanism (dark brown instead of jet black colouration). Males of S. a. tingitana are unique in having a very high number of small glandular protuberances on the skin during the breeding period and a distinct swelling of the inner part of the brachial region of the fore legs, comparable to the swellings in Mertensiella caucasica and Chioglossa lusitanica (Donaire-Barroso & Bogaerts, 2003). Salamandra algira tingitana is restricted to the Tangitana peninsula in northwestern Morocco. Viviparous populations are known from the area north of Oued Martil, and ovoviviparous populations from the area south of Martil (Donaire-Barroso et al., 2001; Beukema et al., 2010; 2013).

Diagnosis

A slender, moderate-sized, terrestrial salamander with smooth, shiny skin, prominent paratoids and conspicuous black and yellow colouration with red spots (except in S. a. tingitana). Tail relatively long. Colour pattern highly variable, especially in S. a. tingitana which shows a strong reduction in the number of yellow spots.

Reproduction

Salamandra algira females are usually ovoviviparous (larviparous). They release relatively advanced larvae directly into streams and ponds. Both permanent and temporary water bodies are used. A female may produce 19-22 larvae (Bogaerts, pers. com.) similar in appearance to those of Salamandra salamandra. A yellow spot at the insertion of each limb characterises all Fire Salamander larvae. They measure about 35 mm at birth and metamorphose at 67.5 mm on average. Larvae can be found from November-April (Donaire-Barroso & Bogaerts, 2001).

Salamandra algira splendens, larvae, Taza. Photo: Max Sparreboom.

Salamandra algira splendens, larvae near to metamorphosis, Taza. Photo: Max Sparreboom.

Females of S. a. tingitana from the area north of Oued Martil produce fully developed young. Captive females gave birth to 5-17 metamorphosed young at an average size of ca. 33 mm (Donaire-Barroso & Bogaerts, 2001; Donaire-Barroso et al., 2001). The two reproductive types are associated with environmental differences. The viviparous form occurs in areas with little or no surface water, lower temperatures and less rainfall (Beukema et al., 2010).

The range of Salamandra algira.

eastern Morocco. Its aquatic biotope – if available – includes all sorts of water bodies: cisterns, cattle watering sites, man-made springs and small shaded pools (Escoriza & Comas, 2007). The species occurs at altitudes from ca. 80-2,450 m (IUCN, 2013).

Behaviour

Salamandra algira aestivates during the hot summer months. They are nocturnal and crepuscular and may be found especially on rainy nights during the breeding season,

Salamandra algira tingitana, habitat, Ceutat. Photo: Max Sparreboom.

Distribution

Salamandra algira has a patchy distribution and is restricted to north-west Africa, with a fragmented range in parts of northern Morocco (Rif Mountains and Middle Atlas), Ceuta (Spanish enclave in Morocco), and the coastal mountain ranges of northern Algeria. There is no confirmation of its possible occurrence in Tunisia. The southernmost record is from the southern slopes of the Jebel Bou Iblane in Morocco (Bogaerts et al., 2007).

Habitat

The terrestrial habitat of Salamandra algira varies across its range. It is generally restricted to diverse types of humid montane forest, where it is found under stones and beneath tree roots in Cedar (Cedrus) and Oak (Quercus) woodland (IUCN, 2013). It has also been observed in caves in Beni Snassen,

Salamandra algira splendens, habitat, Taza. Photo: Max Sparreboom. 313

which extends from November-April. They are entirely terrestrial. Only the female makes a brief visit to the water to deposit the larvae. The onset of the active period is determined by the autumn rains. This species’ courtship behaviour has not been described in detail, but is probably similar to that of Salamandra salamandra (Arnold, 1987). The male engages the female in a ventral amplexus and makes undulating and shifting movements with his body and tail. Sperm transfer is accomplished during ventral clasping. The male deposits one spermatophore. He lifts his vent off the spermatophore and moves his sacrum and tail to the side and so out from under the female. Her vent drops partway towards the spermatophore. The male then draws his sacrum and tail forward under the female’s femur without causing her to move her leg so that the female settles onto the spermatophore, inserting the entire structure into her cloaca (pers. obs.). On rare occasions a form of rival combat was observed between two captive males, similar to that observed in Salamandra

salamandra in the wild (Kästle, 1986). The males embrace and temporarily stand up belly to belly, rubbing their chins against one another, climbing over each other’s back, turning around and pushing one another downwards. This behaviour was interpreted as territorial defence by a resident male. The winning male stayed in the area while the loser escaped and found shelter (Bogaerts & Donaire-Barroso, 2005). Several such male interactions in European Salamandra salamandra have been filmed recently and posted on YouTube.

Threats and conservation

This species occurs in small relic populations around water sources, making it sensitive to any alterations in the habitat, especially any human activities that directly or indirectly increase aridity, such as channelisation of water sources for irrigation. This is a particularly serious threat in the case of Salamandra a. spelaea (Escoriza et al., 2006; Escoriza & Comas, 2007). This species is also threatened by deforestation and overgrazing by domestic livestock and is classified as Vulnerable (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

Salamandra algira is easy to keep in captivity (Bogaerts, 2012, 2013a) and is occasionally captive-bred. The viviparous reproduction of S. a. tingitana was discovered in captive animals (Donaire-Barroso & Bogaerts, 2001). A suitable terrarium is similar to that described for Salamandra salamandra (Schorn & Kwet, 2010).

Comments

A taxonomic revision of Salamandra algira awaits the analysis of molecular and morphological data of all known populations. Phylogenetically, Salamandra algira is basal to all other Salamandra species (Weisrock et al., 2006).

References

Arnold (1987); Beukema et al. (2010, 2013); Bogaerts

(2012, 2013a); Bogaerts & Donaire-Barroso (2005); Bogaerts et al. (2007); Donaire-Barroso & Bogaerts (2001, 2003); Donaire-Barroso et al. (2001); Escoriza et al. (2006); Escoriza & Comas (2007); IUCN (2013); Kästle

Salamandra algira splendens, couple in amplexus, the male carrying the female on his back. Taza. Photo: Max Sparreboom.

(1986); Schleich et al. (1996); Schorn & Kwet (2010); Stuart et al. (2008); Weisrock et al. (2006).

Salamandra atra Laurenti, 1768 | Alpine Salamander Description

A moderate-sized salamander. Head moderately flattened, almost as long as wide. Snout rounded. No labial folds. Eyes protruding. Large and conspicuous paratoids with gland openings visible. Gular fold present. Body rather slender. Trunk rounded, slightly flattened, with 11-13 prominent vertical costal grooves. Tail almost cylindrical in cross section, usually shorter than snout-vent length, and marked with grooves that form a series of rings. Tail-tip

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pointed. Limbs well-developed but thinner than in the Fire Salamander (Salamandra salamandra). Four fingers and five toes without webbing. Lungs well-developed. Skin smooth. A prominent longitudinal row of glandular protuberances on either side of the vertebral column. The male is slimmer than the female. Cloacal opening is a simple longitudinal fold, slightly swollen in the male during the reproductive season (Thorn, 1969).

Total length 9-13 cm (Steinfartz, 2004). Three subspecies are usually recognised on the basis of colouration, body measurements and genetic differences. The validity of a fourth subspecies, S. a. prenjensis, which was found near Serajevo, is not accepted by most authors. Salamandra atra atra Laurenti, 1768. A fully melanistic form, uniformly black in colour. This species occurs in the European Alps, with isolated populations in the Balkan Dinaric Alps in Slovenia, Croatia, Bosnia-Herzegovina, Serbia-Montenegro and northern Albania. It occurs at altitudes between 400-2,800 m and is most frequent between 800-2,000 m (IUCN, 2013). Salamandra atra aurorae Trevisan, 1982. Somewhat more slender than the nominate form. Black ground colour, but with a dorsal pattern of largely coalescent bright coloured patches varying in colour from whitish or yellow to greenish or grey (Guex & Grossenbacher, 2004). Its range is by and large restricted to the Bosco del Dosso and Val Rensola in north-east Italy, with some populations further to the east

Salamandra atra pasubiensis, Pasubio, Italy. Photo: Wouter Beukema.

Salamandra atra pasubiensis Bonato & Steinfartz, 2005. This is another genetically distinct lineage. Colour pattern variable among individuals within a population, from uniformly black (as in S. a. atra) to yellow-patched (as in S. a. aurorae). Patches mainly straw-yellow but also brownish, only on dorsal surface, most often on proximal parts of limbs, also on head and trunk. Patches more limited than in S. a. aurora. This form is restricted to the Monte Pasubio massif in the Venetian Prealps in north-eastern Italy, where it occurs at altitudes between 1,450-1,900 m (Bonato & Steinfartz, 2005; Lanza et al., 2007).

Diagnosis

A moderate-sized, slender terrestrial salamander with smooth, shiny skin and prominent paratoids. Entirely melanistic in most populations across its range. Two subspecies with limited distributions in north-eastern Italy have a variable colouration, with the dorsal side to some degree covered with yellow patches.

Salamandra atra aurorae, Asiago, Italy. Photo: Wouter Beukema.

(IUCN, 2013). It occurs at altitudes between 1,250-1,800 m (Lanza et al., 2007). Although molecular analyses have revealed that S. a. aurorae is genetically distinct from S. a. atra, the taxonomic status of S. a. aurorae remains uncertain (Joger, 1996; Veith et al., 1998; Ribéron et al., 2004; Bonato & Steinfartz, 2005; Speybroeck et al., 2010; Frost, 2013).

Salamandra atra differs from the other melanistic salamander species, S. lanzai, in the following aspects: no webbing between fingers and toes; on average 3 cm smaller than S. lanzai, tail-tip pointed, not rounded (only in adult animals); the cone-shaped glands on the dorsal surface are arranged in a double row along either side of the vertebral column, with one glandular opening on each. Salamandra lanzai lacks these cone-shaped glands along the vertebral column, instead having a series of elongated glands with several openings each (Grossenbacher, 1994). 315

Salamandra atra atra, Belluno, Italy. Photo: Wouter Beukema.

Reproduction

Salamandra atra females do not deposit larvae, like the Fire Salamander (S. salamandra). Instead they give birth to one or two fully developed young. The term pueripary has been proposed for this phenomenon, to replace the term vivipary (Greven, 2003b). This pattern of development appears to be an adaptation to the high altitudes where this salamander lives, because the growing season is too short to allow a freeliving larval stage in streams in such extreme environments. The female ovulates over 100 eggs, 40-60 for each uterus – the caudal portion of the oviduct. Generally only one egg in each uterus becomes enveloped by a full set of jelly layers, is fertilized and develops into a larva. The remaining eggs disintegrate to form a nutrient yolk mass. The gestation period is 2-4 years, depending on climatic conditions related to the altitude at which individuals are living. During this period the embryo lives for 1-2 years on the food provided by the degenerate eggs, after which it lives in a special part of the uterus, termed the zona trophica, which continuously provides the young with a cellular material that serves as food (Guex & Greven, 1994; Greven, 2003a). The terrestrial, fully metamorphosed young are 40-50 mm total length at birth, which usually takes place in June-July (Thorn, 1969; Guex & Grossenbacher, 2004). Sexual maturity is attained after 4-5 years. Longevity is at least 10 years and maximum age has been estimated as 14-15 years (Guex & Grossenbacher, 2004; Lanza et al., 2007). In captivity animals have lived for eight years on exceptional occasions (Thorn, 1969).

Distribution

The species occurs in the European Alps (from the Haute-Savoie in France, to southern Germany, Switzerland, Austria and northern Italy), with isolated populations in the

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The ranges of Salamandra atra and S. lanzai (arrow).

Balkan Dinaric Alps in Slovenia, Croatia, Bosnia-Herzegovina, Serbia-Montenegro and northern Albania (Duguet & Melki, 2003; Lanza et al., 2007; IUCN, 2013).

Habitat

Salamandra atra inhabits cool, damp alpine meadows, stony pastures, dwarf heath and mixed, broadleaf and coniferous woodland. It occurs at altitudes between 400-2,800 m (IUCN, 2013). The optimal habitat is a combination of alpine meadows, dwarf heath and a soil structure with plentiful hiding places, such as stones, logs and rodent burrows. Estimates of population densities vary from 97 (dense woodland) and 475 (open woodland) salamanders (S. a. aurorae) per hectare (Bonato & Fracasso, 2003) to a maximum of 2000-3000 (S. a. atra) per ha (Klewen, 1988; Guex & Grossenbacher, 2004).

Behaviour

Salamandra atra is nocturnal and exclusively terrestrial. Its seasonal activity pattern depends on climatic conditions at different altitudes. Hibernation at higher altitudes may take as long as eight months (Klewen, 1988). The onset of the active period is determined by rainfall and air humidity, bringing the Alpine Salamanders out, sometimes in great numbers. After rain salamanders can sometimes be found during the day. Activity starts when the snow has disappeared and, depending on altitude, may extend from late April to early October, with a peak in July-August. Optimal temperature is 8-15°C and optimal air humidity 89- 97%. The main activities – foraging, mating – take place in the early morning hours (Klewen, 1988; Guex & Grossenbacher, 2004).

During the day the salamanders hide under stones and logs and in crevices in the ground. Like Fire Salamanders (S. salamandra), Alpine Salamanders (S. atra and S. lanzai) show a high degree of site fidelity. There appears to be a difference in shelter use between Fire Salamanders and Alpine Salamanders. In the former, each adult individual always uses the same refuge. In the latter, each adult uses the same refuge for a few days before moving to another (Bonato & Fracasso, 2003). Faecal pellets allow intruders to identify the residents and serve as a kind of territorial warning (Gautier & Miaud, 2003). It is mainly the males that disperse to other habitats, females showing a higher level of philopatry (Helfer et al., 2012). This species is a generalist feeder, eating beetles, spiders, slugs and earthworms (Guex & Grossenbacher, 2004). Natural enemies are Magpies, Jays, Alpine Choughs and Ravens, Adders (Vipera berus), Grass Snakes (Natrix natrix), Slow Worms (Anguis fragilis) and hedgehogs. Predation at higher altitudes is probably limited, a prerequisite for a species that only produces two young every 4-5 years (Guex & Grossenbacher, 2004). Reproductive behaviour generally resembles that of S. salamandra (Himstedt, 1965; Joly, 1966; Arnold, 1987). It has been described in most detail by Häfeli (1971). A sexually active male stands in an alert posture, with forelimbs extended and head raised. He rapidly pursues a moving female. When the male reaches the female he nudges her, sometimes partly straddling her dorsum in the process. The male may clasp the female’s dorsum with his forelimbs while nudging her. Such dorsal clasping is relatively rare in S. salamandra but in S. atra the male invariably clasps the female’s dorsum before sliding beneath her to begin ventral clasping. In the dorsal clasping position the male presses his head downward and rhythmically swings it back and forth, so that his chin rubs the female’s dorsum (Häfeli, 1971; Arnold, 1987). Salmandra atra is more similar to S. salamandra in its other breeding behaviour patterns. Sperm transfer is accomplished during ventral clasping. The male deposits one spermatophore at a time (but may deposit three spermatophores at 10 minute intervals according to Häfeli, 1971). He moves his sacrum and tail to the side, out from under the female. Her vent drops partway towards the spermatophore. The male then draws his sacrum and tail forward under the female’s femur without causing her to move her leg so that the female settles onto the spermatophore, inserting the entire structure into her cloaca (Arnold, 1987).

A number of behaviour patterns – chasing, mounting and head rubbing – have been observed, particularly among males. Several interpretations have been proposed for this ‘pseudomating behaviour’, such as sex recognition and territorial conflicts (Guex & Grossenbacher, 2004). Similar male-male interactions have been observed in S. salamandra and S. algira and were interpreted as rival combat (Kästle, 1986; Bogaerts & Donaire-Barroso, 2005).

Threats and conservation

This species can be abundant in some parts of its range (Switzerland, Austria, Italy), but is rarer in the Dinaric Alps in Slovenia, Croatia, Bosnia-Herzegovina, Serbia-Montenegro and northern Albania. Some local populations in Switzerland are threatened by road mortality and populations in the Dinaric Alps are threatened by localised habitat destruction due to intensification of farming methods, tourism and infrastructure development. Populations in Serbia-Montenegro are small, fragmented and threatened by over-collecting for the pet trade and possibly climatic changes. The subspecies Salamandra a. aurorae is threatened by collection for scientific purposes and the pet trade, and general habitat alteration. It qualifies for listing as Critically Endangered (IUCN, 2013). Salamandra atra is listed on Appendix II of the Bern Convention, S. a. aurorae is listed on Annex II of the EU Habitats Directive. The species is protected by national legislation over much of its range. It is considered as of Least Concern (IUCN, 2013).

Observations in captivity

Alpine Salamanders are difficult to keep in captivity, but there is one record of their being maintained in captivity for 15 years (Raffaëlli, 2007). Useful observations on captive animals, supplementing field research, were made in large outdoor enclosures (Klewen, 1986; 1988).

Comments

Salamandra atra is the sister species to S. corsica (Weisrock et al., 2006).

References

Arnold (1987); Bogaerts & Donaire-Barroso (2005);

Bonato & Fracasso (2003); Bonato & Steinfartz (2005); Duguet & Melki (2003); Frost (2013); Greven (2003a, 2003b); Gautier & Miaud (2003); Grossenbacher (1994a); Guex & Greven (1994); Guex & Grossenbacher (2004); Häfeli (1971); Helfer et al. (2012); Himstedt (1965); IUCN (2013); Joger (1986); Kästle (1986); Klewen (1986, 1988); Lanza et al. (2007); Raffaëlli (2007); Ribéron et al. (2004); Speybroeck et al. (2010); Steinfartz (2004); Thorn (1969); Veith et al. (1998); Weisrock et al. (2006).

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Salamandra corsica Savi, 1838 | Corsican Fire Salamander Description

A large, stocky Fire Salamander. Head wider than long with rounded snout. Upper jaw slightly extending over lower jaw. No labial folds. Eyes large and protruding. Small triangular paratoids. Distinct gular fold. Tail almost cylindrical in cross section, about one third the total length. Limbs thick, with short fingers and toes. Lungs well-developed. Skin smooth and shiny. A longitudinal series of glandular openings on either side of the vertebral column, arranged in two irregular rows on the tail. More or less clear, vertical costal grooves. Colour of dorsum and sides deep shiny black with many irregular, small to moderately large, yellow or orange patches, rarely arranged in longitudinal rows. The colour pattern differs individually. Often four yellow spots on the head, sometimes giving the head a predominantly yellow colour. The colour pattern changes during development, with yellow patches increasing and changing to more irregular shapes (Beukema, 2011). Underside black, usually with small irregular pale yellow or brownish spots. Cloacal opening is a simple longitudinal fold, slightly swollen in the male during the reproductive season (Thorn, 1969; Duguet & Melki, 2003; Mutz, 2004). Total length ca. 18 cm in males, 19 cm in females (Duguet & Melki, 2003).

Reproduction

Salamandra corsica females, like S. salamandra females, do not lay eggs. Instead they release small, relatively advanced, larvae directly into streams and ponds. There are no data on the number of larvae a female can deposit. Larvae of sizes varying from 2.65-4.24 cm were collected in May at ca. 900 m altitude (Mutz, 2004). Larvae are similar to those of S. salamandra. They have moderately long gills; the tail crest starts in the middle of the body; the tail-tip is blunt. Colour is grey-brown mottled with black and metallic dots. Ventral parts whitish. A yellow spot at the insertion of each limb characterises all Fire Salamander larvae. Larvae raised in captivity at 15°C took between 75-95 days to reach metamorphosis (Mutz, 2004). There are only a few records regarding the timing of larval deposition. At higher elevations larvae are probably released in spring and in warmer areas at lower altitudes probably during the winter months. Females have been observed releasing larvae in March and April, and wandering over the forest floor, even during the day (Bille, 2012). Fire Salamanders are flexible and adapt their long breeding season to seasonal and geographical circumstances (Mutz, 2004). Recently metamorphosed individuals are hard to find and immature animals of 5-11 cm may be found close to the streams where they lived as larvae. The juveniles grow to 9-10 cm long after two years (Duguet & Melki, 2003). In captivity Corsican Fire Salamanders took more than five years to reach sexual maturity (Mutz, 2004).

Salamandra corsica, Vizzavona. Photo: Max Sparreboom.

Diagnosis

A stocky Fire Salamander with smooth, shiny skin, relatively small paratoids and short digits. Conspicuous black and yellow colouration. Colour pattern highly variable.

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The range of Salamandra corsica.

There is one record of a female from the Restonica valley giving birth to four fully developed young (Mertens, 1957), but there are no further observations of viviparity in this species.

Distribution

This species is endemic to the French Mediterranean island of Corsica. It occurs across the island from Cap Corse in the North to the Cagne Mountains in the South. It is rare in the littoral regions below 500 m altitude and is not found in the eastern plain or in the area of Bonifacio (Delaugerre & Cheylan, 1992; Duguet & Melki, 2003).

Habitat

Salamandra corsica inhabits moist deciduous, mixed forests with well shaded streams. It is especially associated with beech, Sweet Chestnut and pine forests, but also occurs in lower maquis landscapes and in subalpine regions (Delaugerre & Cheylan, 1992; IUCN, 2013). It prefers microhabitats around large boulders in forests, covered with dense leaf-litter and moss. It occurs at elevations from 50-1,890 m, with a preference for altitudes between 500-1,300 m (Duguet & Melki, 2003; Lescure & de Massary, 2012).

Behaviour

Fire Salamanders are active in seasons with high levels of moisture and without frost, snow, draught and summer heat. Consequently in southern Europe most salamanders are hard to find in the summer months. Rains in March-April and September-October bring them out in great numbers. They are nocturnal and crepuscular and may be found especially on rainy nights with little wind. They are entirely terrestrial. Only the females make a brief visit to the water to release the larvae.

During the day the salamanders hide under stones and logs and in rodent holes in the ground. They are generalist feeders eating snails and slugs, spiders, centipedes, beetles and earthworms (Duguet & Melki, 2003). The reproductive behaviour of Salamandra corsica is identical to that of S. salamandra (Mutz, 2004). After engaging the female in a ventral amplexus, the male deposits a spermatophore on the substrate and moves his hind body out from under the female. The female thus settles onto the spermatophore, inserting the entire spermatophore into her cloaca (Arnold, 1987).

Threats and conservation

This species is not threatened as long as forests, streams and other water bodies are properly managed. Forest fires are a potential threat, especially in the mountains (Duguet & Melki, 2003). The species is listed on Appendix III of the Bern Convention and is protected by national legislation. It is considered as of Least Concern by IUCN (2013).

Observations in captivity

Fire Salamanders have often been kept in captivity. Their reproductive behaviour has been described largely on the basis of detailed observations of captive animals (Arnold, 1987). They are easy to keep and Salamandra corsica has been successfully bred in captivity (Mutz, 2004).

Comments

The biology of Salamandra corsica appears to be generally similar to that of S. salamandra, of which is was long considered a subspecies, but detailed information on its life

Salamandra corsica, habitat, Vizzavona. Photo: Max Sparreboom. 319

history is lacking. Salamandra corsica was elevated to full species status on the basis of mitochondrial DNA analysis. Its closest relative is not the continental Fire Salamander (S. salamandra), but the Alpine Salamander (S. atra), from which it split about five million years ago (Steinfartz et al, 2000; Steinfartz, 2004).

References

Arnold (1987); Beukema (2011); Bille (2012); Delaugerre

& Cheylan (1992); Duguet & Melki (2003); IUCN (2013); Lescure & de Massary (2012); Mertens (1957); Mutz (2004); Steinfartz (2004); Steinfartz et al. (2000); Thorn (1969).

Salamandra infraimmaculata (Martens, 1885) | Near-Eastern

Fire Salamander

Description

The largest Fire Salamander, in general appearance most similar to the central European Salamandra salamandra. Head broad and large. Underside black, without spots except on the throat. Cloaca a simple longitudinal fold as in the other Fire Salamanders, but the male cloaca is distinctly swollen and protrudes more clearly than in other Fire Salamanders, both inside and outside the breeding season. Three subspecies have been named mainly on the basis of different colouration and body measurements. Their status is not yet settled. For summary descriptions and pictures of the distinct phenotypes see Schorn & Kwet (2010).

Salamandra infraimmaculata infraimmaculata Martens, 1885 A very large salamander, tail shorter than snout-vent length, round 40% of total length. One row of generally rounded spots along the back. Four round yellow blotches on the head, arranged symmetrically. Ventral side entirely black and unspot-

ted. The largest specimen measured was a female of 32.4 cm from Galilee (Degani, 1986). It occurs from southern Turkey, through north-western Syria and Lebanon to northern Israel. Salamandra infraimmaculata orientalis Wolterstorff, 1925 Difficult to distinguish from the nominal form on morphological grounds. Genetically only slightly different from S. i. semenovi (Böhme et al., 2013). Compared with S. i. semenovi slightly longer, broader head and shorter tail. Described from south-eastern Turkey around Adana (Steinfartz et al., 2000). Salamandra infraimmaculata semenovi Nesterov, 1916 Stocky body, head moderately broad, snout slightly rounded. Salamandra i. semenovi shows a distinct colour pattern and has small yellow spots on the ventral side. Black colour predominates on dorsum. Covered with many small, yellow arabesquelike spots or rosettes. The yellow blotches appear as broken

Salamandra infraimmaculata, Ferunluk, Syria. Photo: Max Sparreboom. 320

Salamanders of the Old World | Salamandra

Salamandra infraimmaculata semenovi, Kemaliye, Turkey. Photo: Sergé Bogaerts.

Salamandra infraimmaculata semenovi, Ilic, Turkey. Photo: Max Sparreboom.

rings with black spots in the middle. The yellow blotches are highly variable between and within populations (Fleck, 2013e). Patchy distribution, ranging from eastern Turkey and northern Iraq to western Iran.

Diagnosis

A large-sized terrestrial salamander with smooth, shiny skin, prominent paratoids and conspicuous black and yellow colouration. Four round blotches on the head, underside unspotted. Colour pattern highly variable, especially in S. i. semenovi.

Reproduction

Salamandra infraimmaculata females are ovoviviparous (larviparous). They release relatively advanced larvae directly into streams and ponds. Both permanent and temporary water bodies are used. Litter size is 15-105 larvae (Degani & Mendelssohn, 1982). Large females may give birth to more than 100 larvae, but the number of larvae does not seem to be correlated with the mother’s age or mass (Warburg, 2009). The larvae may be released all at once, or over several nights and into several water bodies. The larvae are similar to those of S. salamandra. A yellow spot at the insertion of each limb characterises all Fire Salamander larvae. They measure 29.0-34.5 mm at birth and metamorphosis takes place after 2-4 months at a size of approximately 5-7 cm. Cannibalism is frequent and cannibalistic larvae are larger than other, non-cannibalistic larvae (Degani, 1993; Cohen et al., 2005). Interestingly, cannibalistic larvae appear to be able to assess the degree of their genetic relatedness to conspecifics and vary their behavioural responses depending on the degree of similarity between them (Markman et al., 2009). The salamanders reach maturity at 3-4 years of age, but growth continues thereafter. Longevity in the southernmost population of Mt. Carmel is at least 20 years (Warburg, 2009).

The range of Salamandra infraimmaculata.

Distribution

This species occurs in south-eastern and eastern parts of Anatolia, Turkey; a small area in north-western Iran; northern Iraq; Lebanon; Syria and northern Israel (Tel Dan, upper and western Galilee, and Mt. Carmel) (IUCN, 2013; Bogaerts et al., 2013).

Habitat

The terrestrial habitat of Salamandra infraimmaculata varies across its range. In Iran it is known from an area of arid sparse cork forest. In Turkey and Lebanon it inhabits damp forests and groves in mountains or hilly regions, taking shelter under leaves, roots or stones near water sources. It also occurs 321

Salamandra infraimmaculata, habitat, also of larval and adult Ommatotriton vittatus, west of Qadmus, Syria. Photo: Max Sparreboom.

around artificial water basins fed by winter rains or springs (Hraoui-Bloquet et al., 2001; 2002). In Israel isolated populations are found around pools, often temporary in nature, and slowflowing spring-fed streams. It occurs at altitudes from approximately 180-2,000 m (IUCN, 2013).

Behaviour

Salamandra infraimmaculata aestivates in the hottest summer months, at least in its Mediterranean range. It is nocturnal and crepuscular and may be found especially on rainy nights during the breeding season, which extends from November-March in the Mediterranean parts of its range. Populations from higher elevations hibernate and start activity in March-April. They are entirely terrestrial. Only the females make brief visits to water to deposit their larvae. Whenever they can choose between pools of different depths to deposit their larvae, gravid females spread the larvae both spatially and temporally, and deposit more larvae into deeper pools (Segev et al., 2011). Fire Salamanders show a high degree of site fidelity. Individuals return to the same hiding places and breeding sites and can be found there over several years. Individuals can be easily recognised by their colour patterns and this has enabled researchers to follow a population through several years (Warburg, 1994; 2006; 2009). Although Fire Salamanders are often portrayed as extreme examples of an animal with a strong and specific site fidelity, recent ecological studies have challenged this view and

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showed that the emigration rate can be high and home ranges much larger than previously assumed (Warburg, 2006; Bar-David et al., 2007). The onset of activity is determined by air temperature and humidity. In a moist habitat at Tel Dan, Israel, where water is available throughout the year and temperature relatively constant, activity commenced during or shortly after the rain, at an air humidity of 80-100% and at temperatures of 6-16°C (Degani & Mendelssohn, 1982). The courtship behaviour of this species has not been described in detail, but in all likelihood is similar to that of S. salamandra (Arnold, 1987; Degani, 1996). The male engages the female in a ventral amplexus and makes undulating and shifting movements with his body and tail. Sperm transfer is accomplished during ventral clasping. The male deposits one spermatophore. He lifts his vent off the spermatophore and moves his sacrum and tail to the side and so out from under the female so that her vent drops partway towards the spermatophore. The male then draws his sacrum and tail forward under the female’s femur without causing her to move her leg so that she settles onto the spermatophore, inserting the entire structure into her cloaca.

Threats and conservation

This species is threatened in parts of its range, such as Israel and Lebanon, by infrastructure development and aquatic pollution due to pesticides. Introduc-

tion of predatory fish into the breeding ponds poses a threat. Introduced Mosquitofish (Gambusia affinis) are especially harmful to larval growth and survival (Segev et al., 2009a; 2009b). Adults killed on the roads may pose a threat in some parts of its range. In Israel, the species is considered Endangered and is protected by national legislation. This species is quite wellspread in Lebanon but there is little information on its status (Hraoui-Bloquet et al., 2001; 2002). It is vulnerable in Syria, since its habitats are threatened by water abstraction from springs and by aquatic and terrestrial pollution (Bogaerts et al., 2013). The Near-Eastern Fire Salamander is considered as Near Threatened (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

Near-Eastern Fire Salamanders are easy to keep and are occasionally bred in captivity. A 26.5 cm long female, imported from Lebanon as a larva in 1996, successfully reproduced in captivity. In 2007 she produced a litter of 79 larvae (including some unfertilised eggs and malformed larvae). In 2011 she produced a second litter of 102 larvae (Sergé Bogaerts, pers. comm.). A suitable terrarium

for this species would be similar to that described for Salamandra salamandra (Schorn & Kwet, 2010).

Comments

There is a substantial body of literature on Salamandra infraimmaculata from Israel, where it reaches its southernmost border. The population at Mt. Carmel has been the subject of a long-term study (Degani, 1996; Warburg, 1994; 2006; 2009). Ecological studies have addressed population structure, migration, reproductive strategies, larval development and threats in several populations in Israel (Segev et al., 2009a; 2009b; 2010; 2011). There is very little information on the populations in Iraq, Syria and Iran.

References

Arnold (1987); Bar-David et al. (2007); Bogaerts et al.

(2013); Böhme et al. (2013); Cohen et al. (2005); Degani (1986, 1993, 1996); Degani & Mendelssohn (1982); Fleck (2013e); Hraoui-Bloquet et al. (2001, 2002); IUCN (2013); Markman et al. (2009); Schorn & Kwet (2010); Segev et al. (2009a, 2009b, 2010, 2011); Steinfartz et al. (2000); Stuart et al. (2008); Warburg (1994, 2006, 2009).

Salamandra lanzai Nascetti, Andreone, Capula & Bullini, 1988 | Lanza’s Alpine Salamander

Description

Salamandra lanzai is a high altitude species. It is generally similar in appearance to the other black alpine salamander (Salamandra atra atra), but differs from it genetically and morphologically. It is more stoutly built and the head is more flattened than in S. atra. Upperside rather smooth, without the longitudinal row of glandular protuberances on either side of the vertebral column. 12 costal grooves. Tail-tip not pointed as in S. atra, but rounded (only in adult specimens). Limbs very long, overlapping when adpressed. Toes long, slightly flattened. Small web-like skin structures between digits. Colour uniformly black. Paratoids smaller in male than in female (Grossenbacher, 2004). Males have a more prominent cloaca and are more slender than females (Andreone et al., 2004). Males in the breeding season show minute rugosities on the upperside (Duguet & Melki, 2003).

between fingers and toes; on average 3 cm larger, tail-tip rounded, not pointed; in S. atra cone-shaped glands on the dorsal surface are arranged in a double row along either side of the vertebral column, with one glandular opening on each. Salamandra lanzai does not have these cone-shaped glands along the vertebral column, but instead has a series of elongated glands with several openings on each (Grossenbacher, 1994).

Total maximum length 17 cm (Grossenbacher, 2004; Steinfartz, 2004). Salamandra lanzai is surprisingly homogeneous; no genetic variation was observed either within or among populations (Steinfartz et al., 2000; Ribéron et al., 2002).

Diagnosis

A moderate-sized, terrestrial salamander. Salamandra lanzai differs from the other melanistic salamander species, S. atra atra, in the following aspects: slight webbing

Salamandra lanzai, Italy. Photo: Wouter Beukema. 323

Reproduction

Like Salamandra atra, female S. lanzai give birth to fully developed young. One female may produce 1-6 young after a gestation of 2-4 years, depending on climatic conditions related to altitude (Miaud et al., 2001; Grossenbacher, 2004). Juveniles usually measure 40-50 mm at birth, minimally 37-42 mm (Grossenbacher, 2004). There is considerable variation in age, size at maturity and gestation among populations. In the Guil population both sexes reach maturity at eight years of age, while in the Po population males and females mature at three and six years of age respectively (Miaud et al., 2001; Andreone et al., 2004). Maximum age in nature is 30 years for a female (Duguet & Melki, 2003).

Distribution

This species occurs only in a very small area of the western Alps, around the Viso Massif, on the border of north-western Italy and south-eastern France. It is distributed in the valleys of the Po, Pellice and Germanasca in Italy, and in the Guil Valley in France. An isolated population occurs in the Chisone valley, Italy (Duguet & Melki, 2003; Lanza et al., 2007; IUCN, 2013). The north-eastern limit of the species’ distribution is in the Upper Sangone valley, Turin Province, in north-western Italy (Tessa et al., 2007).

Habitat

Salamandra lanzai inhabits rocky alpine meadows and scree slopes, often close to small streams, usually above the tree line. The lowest localities are situated in mixed and coniferous forest. It occurs at altitudes between ca. 1,200- 2,600 m (IUCN, 2013). Estimates of population densities vary from 297 specimens per hectare in the Guil Valley at 2,200 m to 733 individuals per hectare in the Germanasca valley at 1,550 m (Ribéron & Guyétant, 1996; Andreone et al., 2001; Grossenbacher, 2004).

Behaviour

Salamandra lanzai is nocturnal and terrestrial. Its seasonal activity pattern depends on climatic conditions at different altitudes. The activity period is brief: five months at 1,550 m and three months at 2,200 m altitude (Andreone et al., 2004). The onset of the active period is determined by rainfall and air humidity, bringing the salamanders out, sometimes in great numbers. After rain, salamanders can sometimes be found during the day. Activity starts when the snow disappears and may extend from early June (occasionally as soon as the end of April in mild springs) to September, with a peak at the end of July (Grossenbacher, 2004). Salamanders are active at air temperatures between 1.5-19°C, substrate temperatures between 3- 20°C (Grossenbacher, 2004) and at air humidities above 80% (Duguet & Melki, 2003). They hide under stones and logs during the day, in former rodent burrows and in crevices in the ground (Ribéron & Miaud, 2000). Like S. atra, S. lanza shows a high degree of site fidelity. Interestingly, olfactory communication plays a role in shelter selection. Older juvenile salamanders

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appear to scent mark their shelters and adult females avoid signs of these older juveniles but not of younger juveniles (Gautier et al., 2004). Faecal pellets allow intruders to identify the residents and may serve as a kind of territorial warning (Gautier & Miaud, 2003). This species is an opportunist feeder and eats a wide range of terrestrial invertebrates (mainly arthropods), but also captures prey in mountain streams, such as trichopteran larvae (Grossenbacher, 2004). The breeding season is most probably in late summer (Andreone, 1992). As in other Salamandra species, S. lanzai includes a ventral amplexus as part of its courtship repertoire, with the male carrying the female on his back, his forelimbs hooked over hers. The reproductive behaviour generally resembles that of S. atra, described in detail by Häfeli (1971). Sexually active males stand in an alert posture, with forelimbs extended and head raised, so as to survey the surroundings from an elevated position. There are no descriptions of the entire mating behaviour. A number of behaviour patterns – chasing, embracing and head rubbing – have been observed among males. This has been interpreted as part of the species’ sexual and territorial behaviour (Andreone, 1992). Similar male-male interactions have been observed in S. salamandra and S. algira (Kästle, 1986; Bogaerts & DonaireBarroso, 2005).

Threats and conservation

While there are no major threats to this species, some localised developments for tourism might disturb its habitat. In some populations many individuals are killed by traffic. Salamandra lanzai is listed on Annex IV of the EU Habitats Directive and on Appendix II of the Bern Convention under Salamandra atra. It is important to maintain traditional forest and alpine management within the species’ range and raise awareness of this vulnerable alpine endemic species among a wide public (Duguet & Melki, 2003; Andreone et al., 2007). It is considered Vulnerable (Stuart et al., 2008; IUCN, 2013).

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Salamandra lanzai is sister to a clade that contains S. atra and S. corsica (Weisrock et al., 2006).

References

Andreone (1992); Andreone et al. (2004, 2007); Bogaerts

& Donaire-Barroso (2005); Duguet & Melki (2003); Gautier et al. (2004) ; Gautier & Miaud (2003); Grossenbacher (1994, 2004); Häfeli (1971); IUCN (2013); Kästle (1986); Lanza et al. (2007); Miaud et al. (2001); Ribéron et al. (2002); Ribéron & Guyétant (1996); Ribéron & Miaud (2000); Steinfartz (2004) ; Steinfartz et al. (2000); Stuart et al. (2008); Tessa et al. (2007); Weisrock et al. (2006).

Salamandra salamandra (Linnaeus, 1758) | Fire Salamander Description

A robust, stout-bodied salamander. Head moderately flattened, almost as long as wide. Snout rounded. Upper jaw slightly extending over lower jaw. No labial folds. Eyes large and protruding. Large and conspicuous paratoids with gland openings visible. Distinct gular fold. Trunk robust and slightly flattened. Tail almost cylindrical in cross section, usually shorter than snout-vent length. Tail-tip blunt. No crests or ridges. Limbs short but strong, with four fingers and five toes without webbing. Lungs well-developed. Skin smooth and shiny. A longitudinal series of glandular openings on either side of the vertebral column. More or less clear, vertical costal grooves. Colour of dorsum and sides deep shiny black with irregular yellow or orange patches, sometimes arranged in longitudinal rows. In some subspecies a scattering of reddish spots. The colour pattern differs individually. Underside grey-black, sometimes brownish or bluish, sometimes with yellowish spots. In males fore- and hindlimbs slightly overlap when adpressed against the body, in females fore- and hindlimbs merely touch one another (Thorn, 1969). Cloacal opening a simple longitudinal fold, slightly swollen in the male during the reproductive season. The subspecies differ in certain morphological features and colour patterns. Some 13 subspecies are recognised mainly on

the basis of different colouration and body measurements. There is no consensus as to whether each taxon deserves species or subspecies status. The distribution ranges are not sharply separated, intergradation occurs, and genetic data do not provide unambiguous evidence in every case (Steinfartz et al., 2000). Subspecific status of some taxa is unclear. Salamandra s. albanica, S. s. carpathica and S. s. beschkovi are not usually recognised, while S. s. werneri is (Thiesmeier, 2004). For summary descriptions and pictures of the distinct phenotypes see Schorn & Kwet (2010). Salamandra salamandra alfredschmidti Köhler & Steinfartz, 2006 Tendi Salamander A small salamander, reaching a size of 9-12 cm. Extremely variable in colour pattern. It is not usually bright black and yellow but dirty grey-yellow, grey, brown, orange-brown or olive-green. It closely resembles Salamandra s. bernardezi. Distributed between Cangas de Onis and Mieres, Asturias (Beukema, 2006). Salamandra salamandra almanzoris Müller & Hellmich, 1935 Gredos Salamander A relatively small Fire Salamander. The black ground colour predominates and the yellow colour pattern is reduced. Larval features are sometimes retained in adult animals. Restricted to the Sierra de Gredos and Sierra de Guadarrama, central Spain, where it occurs at altitudes around 2,000 m (Thiesmeier, 2004; Kwet, 2011).

Salamandra salamandra alfredschmidti, Rio Marea, Spain. Photo: Frank Pasmans. 325

Salamandra salamandra almanzoris, male, Sierra de Gredos. Photo: Andreas Nöllert.

Salamandra salamandra bejarae, La Alberca. Photo: Wouter Beukema.

Salamandra salamandra bernardezi, colour variants, Sierra de Cuera. Photos: Wouter Beukema. 326

Salamanders of the Old World | Salamandra

Salamandra salamandra bejarae Wolterstorff, 1934 Spanish Fire Salamander A small, stocky salamander with short, high tail and pointed snout. Irregular yellow spots on predominantly black background. Sometimes red spots on head and paratoids. It occurs in the dry highlands of the central and central-eastern Meseta areas in Spain (Thiesmeier, 2004). Salamandra salamandra bernardezi Wolterstorff, 1928 Oviedo Fire Salamander A small, elegant salamander. Upperside mainly yellow. A narrow or broad black longitudinal band running from head to tail. The female gives birth to fully developed young, but it is not unique in this respect, as populations of live-bearing Salamandra s. fastuosa have also been described. It occurs in Asturia, western Cantabria and north-eastern Galicia, Spain. The border between the ranges of this form and S. s. fastuosa is unclear (Thiesmeier, 2004).

Salamandra salamandra crespoi, near Monchique. Photo: Sergé Bogaerts.

Salamandra salamandra fastuosa, Selva da Irati. Photo: Frank Pasmans.

Salamandra salamandra crespoi Malkmus, 1983 Monchique Fire Salamander A large, slender salamander, reaching a length of 19-25 cm. Long tail and very long limbs with long fingers and toes, relatively small paratoids and prominent eyes; head flattened and long. Many small yellow spots on black ground colour; similar to Salamandra s. gallaica but lacking red components in yellow parts. It occurs in the Serra de Monchique in southern Portugal (Thiesmeier, 2004) and extends eastward to the Spanish border (Guadiana River) and northward to the Serra de Grandola (Reis et al., 2011). Salamandra salamandra fastuosa Schreiber, 1912 Small and slender salamander, characterised by two bright yellow longitudinal bands on the back. Tail relatively long and low. Head small, snout short and rounded, paratoids small. Similar to Salamandra s. bernardezi but is larger in size, up to approx. 20 cm. It is impossible to distinguish S. s. fastuosa from S. s. bernardezi in eastern Asturia and western Cantabria, where their ranges meet or overlap. Salamandra s. fastuosa may be either ovoviviparous or viviparous (García-París et al., 2003). This subspecies occurs in the Basque country, in the North of Navarra and in the western and central Pyrenees (Thiesmeier, 2004). Salamandra salamandra gallaica Seoane, 1885 Portuguese Fire Salamander A large, robust salamander. Variable yellow spots on black background, often in horse-shoe, comma or ring-shaped patterns. Often red spots on head, more rarely also on other body parts. It occurs in Portugal, except in the South, and neighbouring areas in northwestern Spain (Thiesmeier, 2004). Viviparous populations of Salamandra s. gallaica have been found on two small Atlantic islands off the northwestern coast of Spain (San Martiño and Ons) (Velo-Antón et al., 2011).

Salamandra salamandra gallaica, Serra de Lousã, Portugal. Photo: Sergé Bogaerts. 327

Salamandra salamandra gigliolii Eiselt & Lanza, 1956 Italian Fire salamander An elegant, relatively long-bodied salamander with long, high tail and long extremities, may reach a length of 20 cm or more. Head broad and flattened and often almost entirely yellow. The yellow spots form larger patches, often obscuring the black ground colour. Most individuals have red colouration on the throat and ventral side. It occurs in south and central Italy, in the northwards to Liguria (Thiesmeier, 2004). Salamandra salamandra longirostris Joger & Steinfartz, 1994 Long-snout Fire Salamander A large salamander, reaching a length of more than 22 cm. It has a conspicuously long, pointed snout, with upper jaw

extending clearly over lower jaw. Roundish or quadrangular lemon-yellow spots on a black background, often in horse-shoe or comma shape. No red spots as in Salamandra s. morenica. It is further characterised by a pattern of four large yellow spots on the head and two more spots above the corner of the mouth. Isolated from other forms, it occurs in the southern Spanish provinces of Cadiz and Malaga (Thiesmeier, 2004). It is genetically well-differentiated from the other Fire Salamanders and is considered a full species by some authors (Frost, 2013). Salamandra salamandra morenica Joger & Steinfartz, 1994 Morena Fire Salamander A large salamander, up to 20 cm total length. Extensive red colouration, especially on paratoids and other parts of the head,

Salamandra salamandra morenica, Sierra de Aracena, Alajar. Photo: Andreas Nöllert. Salamandra salamandra gigliolii, Calabria. Photo: Mark Bakkers.

Salamandra salamandra longirostris, Andalusia. Photo: Max Sparreboom. 328

Salamanders of the Old World | Salamandra

Salamandra salamandra salamandra, male, Thüringen, Germany. Photo: Andreas Nöllert.

Title pages of the first monograph on the Fire Salamander, by J.P. Wurffbainius, 1683.

but also on rest of body. Back predominantly black with a few small yellow spots. It occurs in the Sierra Morena, where its range extends from the Portuguese border in the East to the Sierra de Alcaraz and Sierra de Espuña (Murcia, Spain) in the West (Thiesmeier, 2004). Salamandra salamandra salamandra (Linnaeus, 1758) Spotted Salamander The nominate form reaches a length of 14-20 cm in central Europe, 18-28 cm in southeastern Europe. Stocky body form with broad head, relatively long tail and extremities. Variable, irregular pattern of yellow spots, sometimes arranged in longitudinal bands. It is widely distributed, from northern and central Italy to southern Switzerland, Austria, southeastern Germany, Czech Republic and southern Poland to the Carpathians. In extends southeastwards to the Balkan Peninsula.

Salamandra salamandra salamandra, male, ventral side, Thüringen, Germany. Photo: Andreas Nöllert.

Salamandra salamandra terrestris Lacépède, 1788 Striped Fire Salamander A moderate-sized, stocky salamander, mostly smaller than 329

Salamandra salamandra terrestris, Dontreix, France. Photo: Max Sparreboom.

20 cm. Variable colour patterns, but usually two, continuous or interrupted yellow stripes along the back. Specimens with irregular spots without stripes are common, and also occur within populations of striped specimens. Individuals with red colouration are occasionally found (Thiesmeier, 2004). GarcíaParís et al. (2004) refer to the Pyrenean populations of this taxon by the name Salamandra salamandra europaea Bedriaga, 1883. Salamandra salamandra werneri Sochurek & Gayda, 1941 Greek Fire Salamander A fairly large form with a broad snout, extending over the lower jaw. Irregular small yellow spots, few in number, sometimes forming longitudinal rows. Often small reddish spots within the yellow spots, especially on the head. It occurs in southern and central Greece, including the Peloponnese and Euboia.

Salamandra salamandra werneri, Chania, Pilion Mountains, Greece. Photo: Frank Pasmans. 330

Salamanders of the Old World | Salamandra

The exact range in the North is not known (Thiesmeier, 2004; Kwet, 2011).

Diagnosis

A moderate- to large-sized terrestrial salamander with smooth, shiny skin, prominent paratoids and conspicuous black and yellow colouration. Colour pattern highly variable.

Reproduction

Salamandra salamandra females do not lay eggs. Instead they release relatively advanced, but small, larvae directly into streams and ponds. The term larvipary has been proposed for this phenomenon, to replace the term ovovivipary (Greven, 2003b). The female enters the water, usually only immersing her hind-body, and releases 10-50 larvae, usually round 30. The larvae may be released all at once, or spread out over several nights. Under natural conditions S. salamandra females may produce larvae fathered by several males (Steinfartz et al., 2006). Paternity analysis has shown that females can store sperm from different males for several months, and larvae are deposited in the order of fertilisation. Female reproductive success appears to increase with the number of sires (Caspers et al., 2013). Larvae have moderately long gills; the tail crest starts in the middle of the body; the tail-tip is blunt. They are grey-brown in colour mottled with black and metallic dots and the ventral parts are whitish. A yellow spot at the insertion of each limb characterises Fire Salamander larvae. They measure 20-30 mm at birth and reach metamorphosis after 2-3 months, at a size of 55-65 mm (Thorn, 1969). The duration of larval development is strongly dependent on water temperature and habitat. Different development times have been reported for populations in central Europe and in Spain. In Germany larval development

took 120 days in a stream at water temperatures of 10°C. Higher water temperatures generally lead to more rapid development. In some forms (S. s. almanzoris) larvae may stay in the water longer and develop their yellow-black colour pattern at an advanced stage of development, but before metamorphosis. Larvae may be deposited in spring, but as late as winter or autumn in some areas. In central Europe, larvae can be found from February-October (Thiesmeier & Grossenbacher, 2004).

The range of Salamandra salamandra.

The reproductive biology of S. salamandra in northern Spain is extraordinary. Populations of S. s. bernardezi, S. s. alfredschmidti and S. s. fastuosa in the Cantabrian Mountains either give birth to terrestrial, fully metamorphosed individuals or display a mixed strategy, with some females giving birth to relatively large larvae in late developmental stages and others producing fully metamorphosed, terrestrial juveniles. (The term juvipary has been proposed for this phenomenon as a replacement for the general term vivipary, and as opposed to larvipary for the production of advanced larvae, Greven, 2003b). Viviparous populations of S. s. gallaica have been found on two small

Salamandra salamandra alfredschmidti, habitat, Rio Tendi. Photo: Andreas Nöllert.

Salamandra salamandra almanzoris, habitat, Sierra de Gredos 1977. Photo: Max Sparreboom.

Salamandra salamandra morenica, habitat, Sierra de Aracena, Alajar. Photo: Andreas Nöllert. 331

Atlantic islands off the north-western coast of Spain (San Martiño and Ons). Transitions from ovoviviparity to viviparity have occurred repeatedly in amphibians. Viviparity is a derived reproductive mode in salamanders. The current discussion focuses on the origin of viviparity in Fire Salamanders (Buckley et al., 2007). Viviparity either arose only once within S. salamandra and then spread across the various Fire Salamander populations (García-París et al., 2003) or – more probably – evolved independently, and rapidly in different lineages (Velo-Antón et al., 2011).

Distribution

This species is present across much of central, eastern and southern Europe. In the former Soviet Union, it is known only from the mountains and foothills of the Ukrainian Carpathians. The populations of some of the Iberian subspecies are fragmented (IUCN, 2013).

Habitat

Salamandra salamandra inhabits mixed, moist deciduous forests with well-shaded streams. Within the mountain forest belt, it can be found in woodlands, glades and forest edges, rocky slopes, dense bush, and herbaceous vegetation. The occurrence of Fire Salamanders on woodless mountain pastures and within hayfields possibly indicates the existence of forests in the past. In the Iberian Peninsula the species may be found in upland Mediterranean type forest and associated habitats. It prefers microhabitats covered with dense leaf-litter and moss and occurs from lowland areas up to 2,500 m in central Spain (IUCN, 2013).

Behaviour

Fire Salamanders are active in seasons with high levels of moisture and the absence of frost, snow, draught and summer heat. Consequently in central and western Europe most salamanders hibernate in the winter months and in southern Europe most salamanders aestivate in the hottest summer months. The animals are nocturnal and crepuscular and may be found especially on rainy nights with little wind. They are entirely terrestrial. Only the female makes a brief visit water to deposit the larvae. During the day the salamanders hide under stones and logs and in rodent holes in the ground. Fire Salamanders show a high degree of site fidelity and return to the same hiding places where they can be found over several years. Individuals can be easily recognised by their colour patterns, enabling researchers to trace a large number of animals through the years (Joly, 1968; Feldmann, 1987; Thiesmeier & Grossenbacher, 2004). Although Fire Salamanders are often portrayed as extreme examples of animals with a strong and specific site fidelity, recent ecological studies have challenged this view and shown that emigration rates can be high and home ranges much larger than previously assumed (Schulte et al., 2007; Schmidt et al., 2007).

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This species is a generalist feeder and eats snails and slugs, spiders, centipedes, beetles and earthworms (Thiesmeier & Grossenbacher, 2004). Larvae are also opportunistic in their food choice and may adapt their foraging strategy to suit the environment, such as when living in caves or streams (Manenti et al., 2013). Potential natural enemies of adult Fire Salamanders are hedgehogs, badgers, wild boar and rats, but specific records are rare (Thiesmeier & Grossenbacher, 2004). In the face of danger, they may adopt a defensive posture with the trunk slightly raised and the head pressed down, thus presenting the attacker with the paratoids, where poison glands are located. The skin poison, which contains neurotoxins, may be an efficient deterrent to most predators. Fire Salamanders are capable of actively spraying poison from their mid-dorsal glands as a defensive measure when attacked, a unique phenomenon in salamanders (Freytag, 1982a; Brodie & Smatresk, 1990). The onset of the active period is determined by air temperature (above 3°C, ideally between 8-12°C), rainfall and air humidity (75-80%, ideally above 96%). Reproductive activity probably starts at that time too. In ideal weather conditions animals may be found in great numbers. How do salamanders locate potential mating partners? There is experimental evidence that Fire Salamanders can discriminate the sex of conspecifics based on substrate-borne chemical cues while they are active in humid conditions at night (Caspers & Steinfartz, 2011). Courtship generally resembles that of Chioglossa (Arnold, 1987), Lyciasalamandra and Mertensiella (Schultschik, 1994a). It has been described and depicted by Himstedt (1965) and Joly (1966), and in greatest detail by Arnold (1987). A sexually active male stands in an alert posture, with forelimbs extended and head raised. He rapidly pursues a moving female. When the male reaches the female he nudges her, sometimes partly straddling her dorsum in the process. In some cases the male may clasp the female’s dorsum with his forelimbs while nudging her. Such dorsal clasping is relatively rare in Salamandra salamandra. More often the male simply nudges the female and then attempts to clasp her from the ventral side by pushing himself under her body and hooking his forelimbs around hers. Once the male has engaged the female in ventral amplexus, he begins making undulating and shifting movements with his body and tail, a behaviour pattern termed body-shifting. The male slightly raises his head, swings his head laterally back and forth, rubbing the upper side of his head on the female’s chin. The onset of spermatophore deposition is marked by the cessation of body-shifting. The female increasingly presses her vent against the base of the male’s tail,

Salamandra salamandra bernardezi, couple in ventral amplexus, San Miguel de Arroes, Gijón, Asturias. Photo: Frank Pasmans.

predatory species (salmonids and crayfish), and population fragmentation. Mortality of adults killed on roads may pose a threat in some parts of its range. Chytridiomycosis has been reported in some Spanish populations (Bosch & MartínezSolano, 2006). A new chytrid fungus, lethal to Fire Salamanders, has been found in the Netherlands (Batrachochytrium salamandrivorans, Martel et al., 2013). The Fire Salamander is listed on Appendix III of the Bern Convention and is protected by national legislation over much of its range. It is considered as of Least Concern by IUCN (2013).

so that the distal part of her tail arches slightly upwards. Sperm transfer is accomplished during ventral clasping. The male deposits one spermatophore. He lifts his vent off the spermatophore and moves his sacrum and tail to the side and so out from under the female. Her vent drops partway towards the spermatophore. The male then draws his sacrum and tail forward under the female’s femur without causing her to move her leg so that the female settles onto the spermatophore, inserting the entire structure into her cloaca. Sometimes the female drops down beside the spermatophore and may lift up and settle onto it, apparently orienting tactually to it (Arnold, 1987).

Observations in captivity

On rare occasions a form of rival combat was observed between two Salamandra males. Kästle (1986) reported 36 observations of an aggressive form of interaction between male Fire Salamanders in the Bavarian Alps. The males embraced and temporarily stood up belly to belly, rubbing their chins against one another, climbing over one another’s back, turning round and pushing one another downwards. This behaviour was interpreted as the defence of a territory by a resident male. The winning male stayed in the area and the loser left. Several such Fire Salamander male interactions have now been described (Bogaerts & DonaireBarroso, 2005; Velo-Antón et al., 2012), or filmed and posted on YouTube.

Comments

Threats and conservation

The main threats to this species include localised general habitat destruction, improper forest management, pollution of breeding sites by agrochemicals, collection for commercial purposes, introduction of

Fire Salamanders have often been kept in captivity and their reproductive behaviour has been described largely on the basis of detailed observations on captive animals (Arnold, 1987). A terrarium for Fire Salamanders should be moist but not wet, and should be provided with sufficient hiding places. Temperatures should preferably not exceed 20-22°C in summer, and should be reduced to 8°C for several weeks during winter. They are easy to keep in captivity and several forms have been successfully bred over several generations. There are reports of captive Fire Salamanders reaching over 40 years of age (Böhme, 1979; Raffaëlli, 2007; Schorn & Kwet, 2010).

Salamandra salamandra is phylogenetically basal to a clade containing S. infraimmaculata, S. lanzai, S. corsica and S. atra (Weisrock et al., 2006). There is a vast literature on the Fire Salamander. It was first mentioned by the Greek philosopher Aristotle and the earliest 333

monograph was written in 1683 by the Nurnberg physician Wurffbain (Wurffbainius, 1683). For a discussion of the earliest knowledge of this salamander, its folklore and cultural history see Orbán (1985) and Hohorst et al. (1997).

References

Arnold (1987); Beukema (2006); Bogaerts & Donaire-

Barroso (2005); Böhme (1979); Bosch & Martínez-Solano (2006); Brodie & Smatresk (1990); Buckley et al. (2007); Caspers & Steinfartz (2011); Caspers et al. (2013); Feldmann (1987); Francis (1934); Freytag (1982a); Frost (2013); García-París et al. (2003, 2004); Greven (2003b); Himstedt

For specific information the reader is referred to the books which were the main sources used for this entry (Thiesmeier & Grossenbacher, 2004; Thiesmeier, 2004). For the Iberian Fire Salamanders see García-París et al. (2003; 2004), for the Italian salamanders Lanza et al. (2007), for Greece and the Balkan countries see Trapp (2007), Valakos et al. (2008), Stojanov et al. (2011). The book by Francis (1934) describing the anatomy of the Fire Salamander is still a classic text.

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(1965); Hohorst et al. (1997); IUCN (2013); Joly (1966, 1968); Kästle (1986); Kwet (2011); Lanza et al. (2007); Manenti et al. (2013); Martel et al. (2013); Orbán (1985); Özeti (1967); Raffaëlli (2007); Reis et al. (2011); Schmidt et al. (2007); Schorn & Kwet (2010); Schulte et al. (2007); Schultschik (1994a); Steinfartz (2004); Steinfartz et al. (2000, 2006); Stojanov et al. (2011); Thiesmeier (2004); Thiesmeier & Grossenbacher (2004); Thorn (1969); Trapp (2007) ; Valakos et al. (2008); Veith et al. (1998); Velo-Antón et al. (2011, 2012); Weisrock et al. (2006); Wurffbainius (1683).

Salamandrina Fitzinger, 1826 Very small salamanders. Premaxillary paired. Nasals separated by internasal cavity. Bony fronto-squamosal arch present. Two series of vomeropalatine teeth beginning at the level of the choanae, parallel on the front and diverging backwards. Triangular tongue free at the sides and at the back side. Paratoids absent. Tail slightly compressed. Four fingers, four toes. Lungs reduced (Thorn, 1969). The genus Salamandrina is

considered an ancient lineage representing the most basal split within the family Salamandridae which took place approximately 90 million years ago (Steinfartz et al., 2007). Accordingly, Salamandrina is sister to the group of all remaining salamandrids (Zhang et al., 2008). Until 2005, Salamandrina was believed to be a monotypic genus, composed of a single species, Salamandrina terdigitata (Zuffi, 1999), which was discontinuously distributed from the northern Apennines to the tip of Calabria in Italy. Genetic studies, using both mitochondrial and nuclear DNA markers, revealed that Salamandrina is actually composed of two well-differentiated, largely parapatric species (Mattoccia et al., 2005; Nascetti et al., 2005; Canestrelli et al., 2006). The genetic divergence is among the highest exhibited between congeneric species within the salamandrid family. The two species can also be identified on the basis of morphology (Romano et al., 2009a; Angelini et al., 2010b). There is a small area of sympatry between them and hybridisation occurs where their ranges meet (Hauswaldt et al., 2011; Mattoccia et al., 2011). A multimarker study of the demographic histories of the two species led to an estimate that they diverged approx. 2.25 million years ago (Hauswaldt et al., 2014).

Salamandrina perspicillata (Savi, 1821) Salamandrina terdigitata (Bonnaterre, 1789)

References

Angelini et al. (2010b); Canestrelli et al. (2006);

Hauswaldt et al. (2011, 2014); Mattoccia et al. (2011); Mattoccia et al.

The ranges of Salamandrina perspicillata (north) and S. terdigitata (south).

(2005); Nascetti et al. (2005); Romano et al. (2009a); Steinfartz et al. (2007); Thorn (1969); Zhang et al. (2008); Zuffi (1999).

Salamandrina perspicillata (Savi, 1821) | Northern Spectacled Salamander Description

A very small salamander. Head a little longer than wide. Snout short and rounded, large mouth. Large, prominent eyes in lateral position. Gular fold absent. Paratoids absent. Trunk almost quadrangular and dorsoventrally flattened, ribs and vertebrae visible under the skin, giving the animal a very skinny appearance. No crests. Tail longer than rest of the body and slightly compressed. Vertebral ridge distinct on front part of the tail. Tail-tip pointed. Limbs long and thin. Four toes, four fingers without webbing. Skin mat, finely granulated and dry. Lungs reduced. Colour of upperside of body and tail black or deep brown. Upperside of tail gradually lighter toward the tip. A yellow or white V-shaped spot between the eyes, pointed backwards.

The underside of tail, cloaca and feet, and frequently the distal part of the belly, are bright red. The rest of the ventral region is white or grey with irregular dark spots (Thorn, 1969). Sexual dimorphism is difficult to perceive (Vanni, 1980; Zuffi, 1999). On average the male is a little smaller than the female, his body is shorter and his tail longer. Males have a longer cloacal slit and wider head. By manipulating the cloacal lips, the lateral walls of the cloacal chamber are extruded, showing knifebladeshaped ridges in the male, whereas they are smooth in the female (Romano et al., 2009b). Total length 80-90 mm (Zuffi, 1999); the largest males measure 92 mm, the largest females up to 134 mm (Lanza et al., 2007). 335

Salamandrina perspicillata, Stazzema, Tuscany. Photo: Frank Pasmans.

Diagnosis

A very small salamander, terrestrial (except for females that enter water to lay eggs), coloured black to brown on dorsal side. Tail partly reddish dorsally, ventral side of body white, ventral side of cloaca, tail and limbs, frequently also distal part of the belly, bright red. A whitish or yellowish V-shaped spot between the eyes (‘spectacles’, hence its scientific and vernacular names). The Northern Spectacled Salamander largely resembles its southern Italian sister species, Salamandrina terdigitata. Apart from genetic differences in both mitochondrial and nuclear DNA, the species can be differentiated morphologically. Salamandrina perspicillata is larger in size, the red colouration on the tail is less extensive, and the median reddish dorsal line is less commonly expressed than in S. terdigitata (Romano et al., 2009a). Ventral colouration is also different, in particular on the anterior part of the head and the pectoral girdle (Angelini et al., 2010b). However, the species cannot be discriminated with 100% certainty on morphological traits alone.

Salamandrina perspicillata, Bradia Prataglia, Tuscany. Photo: Frank Pasmans.

Development of the eggs takes 20-22 days at water temperatures around 14°C and longer at lower temperatures. Larvae hatch at a length of 7-13 mm (Lanza et al., 2007) and have balancers at this stage. The larvae are slender, with short gills with a small number of short filaments. Colour yellow to brown above, with dark spots. Ventral colour whitish or yellow. Dorsal tail-fin is high and starts at the beginning of the dorsum. Tail-tip rounded. Larvae can easily be identified by the possession of four toes (Thorn, 1969). They reach metamorphosis after 2-5 months at a length of 20-35 mm and measure 35-40 mm after one year. Females reach sexual maturity in 4-5 years. Longevity was recorded as 10-12 years (Zuffi, 1999; Angelini et al., 2010b; AmphibiaWeb, 2013).

Eggs and larvae

Females enter the water for the sole purpose of laying eggs and usually leave the water within 7-9 days. They lay 30-60 eggs and attach them individually to submerged objects, each egg being glued to the substrate by a peduncle. Egg masses are the result of adhesion of several eggs to one another, laid by one or more females. The yolk is 1.5-3.7 mm in diameter (Lanza et al., 2007) and the gelatinous envelope is 5 mm in diameter (Thorn, 1969). Eggs are heavily predated by aquatic invertebrates. Egg-laying females have been observed chasing caddisfly larvae away from freshly laid eggs using a variety of body movements which create a water current that causes the caddisfly larva to fall to the bottom, or by physically pushing them away with the body and tail (Boscherini & Romano, 2011).

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The range of Salamandrina perspicillata.

Distribution

This species is endemic to central and northern peninsular Italy in the Apennine Mountains and other hilly areas, down to Caserta Province (Campania) in the south. The northern limit of its range is near Brallo di Pregola in the Lombardia region. The eastern limit is in northern Apulia (Romano et al., 2009a). The western border of the Apulia region is probably the south-eastern outpost for both species of Salamandrina (Liuzzi et al., 2011).

Habitat

Salamandrina perspicillata inhabits forest with dense undergrowth in hilly and mountainous areas, also Mediterranean bush vegetation, usually at elevations between 200-900 m, but also at lower and higher altitudes. Breeding sites are generally well-oxygenated waters, slow-running streams with rocky beds, springs, drinking troughs and small ponds (Zuffi, 1999; IUCN, 2013).

Behaviour

Salamandrina has been found underground during summer and winter, but there is on the whole little information about its terrestrial hiding places. It is mainly crepuscular and nocturnal, but in humid places on leaf litter individuals may sometimes also be observed active during the day (Bruni & Romano, 2011). Oviposition takes place from MarchApril, but may start after rainfall in winter, or continue until August, depending on the locality and climatic conditions. In some sites egg-laying has been observed in September (Lanza et al., 2007). Only females enter the water, males are completely terrestrial. Females display strong site fidelity, returning to the same breeding site every year (Angelini et al., 2008). Experiments have shown that salamanders use smell to find terrestrial sheltering places and are able to discriminate between shelters previously used by conspecifics and those previously unused (Romano & Ruggiero, 2008; Vignoli et al., 2010). These salamanders prey on all sorts of small invertebrates, especially arthropods, with a preference for Acarina (AmphibiaWeb, 2013). There are few reports of predation on adult salamanders which are probably unpalatable to predators. If distressed, this salamander may assume a defensive posture, similar to the so-called Unken-reflex: the salamander curls its body dorsally to a variable degree, even so far as to form a loop. In doing so, it partly displays the ventral colour pattern of its body and the bright red pattern on the underside of its tail and limbs. It can hold this position for up to a few minutes (Utzeri et al., 2005). The breeding season is most probably prolonged. Sperm can be stored in the female cloaca for some months and has been found in the spermatheca from autumn to spring (Brizzi et al., 1995). All reproductive activity takes place on land. Until 2011, the courtship was poorly known from fragmentary observations (Strötgen, 1927; Houck & Arnold, 2003). Observations in the

natural habitat have confirmed and supplemented these earlier reports and can be summarised as follows (Bruni & Romano, 2011). A male assumes an alert posture, climbing onto a higher vantage point that enables him to watch his surroundings, and may even stand on his hind legs using the tail as a support. He may mark a trail on the substrate by excreting a mucous substance from his cloaca. When the male sees another salamander he quickly approaches it, attempting to bar its way by positioning himself in front of it. Keeping his head raised, his snout touches the lateral part of the other individual’s body or tail-base, thus presumably confirming that it is a female. If the female is responsive and stands still, the male positions himself in front of her and starts undulating his tail in a horizontal plane. The female puts her snout near the male’s pelvis and the pair slowly moves around in an elliptical circle, while keeping a distance of 2-4 cm from each other and making undulating movements with their tails. During this circling the male deposits a spermatophore of some 4 mm high on the substrate. The pair continues to circle around in such a way that the female eventually moves over the spermatophore with her cloaca and picks it up. Rival males may interfere with the courtship. The courting male attempts to repel them with head raised and sideward tail movements. If the intruding male does not go away, the courting male may chase the intruder away by biting him, holding onto him as the intruder moves away (Bruni & Romano, 2011). Salamandrina perspicillata appears to have a remarkable repertoire of aggressive behaviour patterns, in one of which the male attempts to turn his opponent upside down by jerks and twists of his body (Utzeri et al., 2005). The courtship behaviour patterns of Salamandrina have more in common with representatives of the Asian genus Echinotriton than with Salamandra and other European salamandrids, but show some elements, such as standing up on the hind legs, that are unique among terrestrial salamanders.

Threats and conservation

There are some local population declines in parts of the species’ range caused by habitat loss and water pollution, but overall it is not significantly threatened. Introduced trout (Salmo trutta) have a detrimental effect on the reproductive output of Salamandrina perspicillata (Piazzini et al., 2011). The species is protected by regional legislation. It is considered as of Least Concern by IUCN (2013).

Observations in captivity

Spectacled Salamanders have been kept and bred in captivity on several occasions but are delicate subjects. Adults can be kept in small terrariums with a humidity gradient and temperatures preferably not exceeding 23°C. Raising larvae is not problematic but rearing juveniles is difficult. The best results have been obtained in outdoor terrariums and small sterile boxes furnished with paper tissue (Bogaerts & Pasmans, 2002). 337

Comments

Until 2005, Salamandrina terdigitata was considered the only species within the monotypic genus Salamandrina. After the split into two well-differentiated species, the name perspicillata – previously considered a junior synonym of S. terdigitata – was available for the northern species (type locality Mugello in Tuscany). The name terdigitata became restricted to what is now considered the southern species (type locality Vesuvius). Prior to 2005 the name S. terdigitata in the literature refers to the single, taxonomically undivided species. Most studies have been conducted on what is now the northern species, S. perspicillata. A brief monograph is dedicated to S. perspicillata in the area around Rome, and

summarises our knowledge of its biology, emphasising the importance of its conservation (Rocca & Vignoli, 2009). An excellent summary of information on both species is given in Lanza et al. (2007).

References

AmphibiaWeb (2013); Angelini et al. (2008a, 2010a,

2010b); Bogaerts & Pasmans (2002); Boscherini & Romano (2011); Brizzi et al. (1995b); Bruni & Romano (2011); Houck & Arnold (2003); IUCN (2013); Lanza et al. (2007); Liuzzi et al. (2011); Piazzini et al. (2011); Rocca della & Vignoli (2009); Romano et al. (2009a, 2009b); Romano & Ruggiero (2008); Strötgen (1927); Thorn (1969) ; Utzeri et al. (2005); Vanni (1980); Vignoli et al. (2010); Zuffi (1999).

Salamandrina terdigitata (Bonnaterre, 1789) | Southern

Spectacled Salamander

Description

The Southern Spectacled Salamander largely resembles its northern Italian sister species, Salamandrina perspicillata. Apart from mitochondrial and nuclear genetic differences, the species are morphologically distinct. Salamandrina terdigitata has a smaller body size, more extensive red colouration on the tail, and more often shows a median reddish dorsal line than does S. perspicillata (Romano et al., 2009a). Ventral colouration is also different, in particular on the anterior part of the head and the pectoral girdle (Angelini et al., 2010b). However, the species cannot be discriminated with certainty by morphological traits alone.

Salamandrina terdigitata, Sant’ Eufemia d’Aspromonte, Calabria. Photo: Frank Pasmans. 338

Salamanders of the Old World | Salamandrina

Total length of females (captured in the water during spawning activity) averages 8.1 cm, compared with 8.6 cm on average for S. perspicillata. The males are generally a little smaller than females (Romano et al., 2009a).

Diagnosis

A very small salamander, terrestrial (except for females that enter water to lay eggs), coloured black or brown on dorsal side. Tail partly reddish dorsally, ventral side of body white, ventral side of tail and limbs, frequently also distal part of the belly, bright red. A whitish or yellowish V-shaped spot between the eyes (‘spectacles’, hence its vernacular name). Very

similar to, but a little smaller than Salamandrina perspicillata, but cannot be diagnosed with 100% certainty on the basis of morphological traits alone.

Eggs and larvae

Little information is available on the ecology and reproductive biology of this species. Its reproductive biology is most probably similar to that of the northern species Salamandrina perspicillata, for which more observations are available. The spawning season extends from April-June. Larvae can overwinter in water bodies (AmphibiaWeb, 2013).

Distribution

This species is endemic to southern peninsular Italy in the Apennine Mountains and other hilly areas, south of Caserta Province (Campania). The northern limit of its range is in the province of Benevento (Campania), in a small area which overlaps with the range of Salamandrina perspicillata. The southern limit is in the province of Reggio Calabria, and the eastern limit the province of Cosenza (Calabria) (Romano et al., 2009a). The western border of the Apulia region is probably the south-eastern outpost for both species of Salamandrina (Liuzzi et al., 2011).

Habitat

Salamandrina terdigitata inhabits forest with dense undergrowth in hilly and mountainous areas, also Mediterranean bush vegetation, usually at elevations between 200-900 m, but also at lower and higher altitudes. Breeding sites are generally well-oxygenated waters, slow-running streams with rocky beds, springs, drinking troughs and small ponds (Zuffi, 1999; IUCN, 2013).

Behaviour

Most probably similar to the behaviour of Salamandrina perspicillata.

Threats and conservation

This species is not threatened and is protected by regional legislation. Its status is considered as of Least Concern by IUCN (2013).

Observations in captivity

Spectacled Salamanders have been kept and bred in captivity on several occasions but are delicate subjects. Adults can be kept in small terrariums with a humidity gradient and with temperatures preferably not exceeding 23°C. Raising larvae is not problematic but rearing juveniles is difficult. The best results have been obtained in outdoor terrariums and small sterile boxes furnished with paper tissue (Bogaerts & Pasmans, 2002).

Comments

Until 2005, Salamandrina terdigitata was considered the only species within the monotypic genus Salamandrina. After the split into two well-differentiated species, the name perspicillata – previously considered a junior synonym of S. terdigitata – was available for the northern species (type locality Mugello in Tuscany). The name terdigitata became restricted to what is now considered the southern species (type locality Vesuvius). Prior to 2005 the name S. terdigitata in the literature refers to the single, taxonomically undivided species. Most studies have been conducted on what is now the northern species, S. perspicillata. Until more detailed information becomes available the assumption must be that the life histories of S. terdigitata and S. perspicillata are similar.

References

AmphibiaWeb (2013); Angelini et al. (2010b); Bogaerts

& Pasmans (2002); IUCN (2013); Liuzzi et al. (2011); Romano et al. (2009a);

The range of Salamandrina terdigitata.

Zuffi (1999).

339

Triturus Rafinesque, 1815 The genus Triturus comprises the large-bodied Eurasian Newts. Triturus was once a larger genus, containing not only the largebodied species, but also other medium- and small-sized European newts. After genetic studies had shown that the European newt genus Triturus was polyphyletic (Weisrock et al., 2006; Steinfartz et al., 2007), new genus names have been introduced for the majority of taxa formerly included in Triturus (Ichthyosaura, Lissotriton and Ommatotriton) (García-París et al., 2004) and only the crested newts and marbled newts remained in Triturus. Members of the crested newt group – the Triturus cristatus superspecies – were long considered subspecies of Triturus cristatus (Arntzen & Wallis, 1999; Wielstra et al., 2013a), and the Pygmy Marbled Newt, Triturus pygmaeus) was until recently considered a subspecies of T. marmoratus (García-París et al., 2001). What distinguishes Triturus from the other European newts is its fairly large body-size, the size and whitegreenish colour of the eggs, and the shape of the larvae. Larvae have a high tail-fin with black spots and very long, thin fingers and toes. Triturus larvae occupy different spatial niches than other newt larvae. They are more nektonic than, for instance, the benthic, bottom-dwelling larvae of Lissotriton vulgaris, and are more often found foraging higher up in the water column (Grosse, 1994). A further feature that distinguishes Triturus from all other newts is their so-called ‘developmental arrest syndrome’. Due to a peculiar genetic defect, only half of all the eggs laid by a female develop properly. The remainder stop developing and die. This phenomenon is hard to explain (Horner & Macgregor, 1985; Jehle et al., 2011). It is difficult to distinguish the various crested newt species on external characters alone, but the throat-belly colour pattern gives an indication. The modal count of the number of rib-bearing pre-sacral vertebrae can be used to discriminate between the crested newt species. Overall body shape appears to reflect ecology, with a gradient running from the more terrestrial species with a short, sturdy body and a low vertebrae count (13) as in T. karelinii, to the more

aquatic species with a long, slender body and a high vertebrae count (16 or 17) as in T. dobrogicus (Arntzen & Wallis, 1999). The marbled newts, T. marmoratus and T. pygmaeus, which make up the crested newts’ sister group, have the heaviest body build in the genus and have a typical vertebrae count of 12. Species of Triturus are distributed across most of Europe and adjacent Asia. They are found in regions generally regarded as important glacial refugia, such as the Iberian, Italian and Balkan Peninsulas, Anatolia, Caucasia and the southern Caspian Sea shore (Wielstra et al., 2013b). The Triturus species have largely parapatric ranges, which sometimes overlap in narrow contact zones. Delineating precise geographic range borders of adjacent crested newt species is difficult. In some regions, three or four species are in contact with one another, resulting in hybridisation and partially fertile hybrids. In central France the ranges of T. cristatus and T. marmoratus overlap to a considerable extent. In the area of syntopy, these species do sometimes hybridise and produce fertile offspring (refs in Arntzen, 2003). Triturus is monophyletic and sister to the genus Calotriton (Steinfartz et al., 2007; Zhang et al., 2008; Pyron & Wiens, 2011).

Triturus carnifex (Laurenti, 1768) Triturus cristatus (Laurenti, 1768) Triturus dobrogicus (Kiritzescu, 1903) Triturus ivanbureschi Arntzen & Wielstra, 2013 Triturus karelinii (Strauch, 1870) Triturus macedonicus (Karaman, 1922) Triturus marmoratus (Latreille, 1800) Triturus pygmaeus (Wolterstorff, 1905)

References

Arntzen (2003); Arntzen & Wallis (1999); García-París

et al. (2001, 2004); Grosse (1994); Horner & Macgregor (1985); Jehle et al. (2011); Pyron & Wiens (2011); Steinfartz et al. (2007); Weisrock et al. (2006); Wielstra et al.(2013a, 2013b); Zhang et al. (2008).

Triturus carnifex (Laurenti, 1768) | Italian Crested Newt Description

A large-bodied newt. Similar to Triturus cristatus, but the Italian Crested Newt has a somewhat stouter body, larger head and stronger limbs. The dorsal colouration varies from light brown and dark grey to dark brown, with large black blotches. The throat colour varies from yellow with black spots to black, but always has many small white dots. The ventral side is orange with large, dark grey to black blotches and spots. Unlike T. cristatus, the margins of these blotches and

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Salamanders of the Old World | Triturus

spots are blurred. Females and juveniles often have a distinct yellow-greenish dorsal line. The male crest is slightly lower and less serrated than that of T. cristatus and T. dobrogicus (Arntzen, 2003; Jehle et al., 2011). Total length between 10-15 cm, the females on average larger than the males (Lanza et al., 2007).

Triturus carnifex, male, Ucka Istra, Croatia. Photo: Benny Trapp.

Diagnosis

A large, dark coloured newt with rough skin. A high dorsal crest in the breeding male, strongly indented at the tail-base. Compared with the other crested newt species it has a medium stocky build and little or no white stippling on the sides. Throat colour variable with white stipples. Ventral surface yellow-orange with a few large, roundish, ill-defined and muddy-grey to black spots (Arntzen, 2003; Wielstra et al., 2013c).

Triturus carnifex, female, Ucka Istra, Croatia. Photo: Benny Trapp.

description is given under Triturus cristatus. Larvae measure 50-80 mm at metamorphosis and sometimes giant larvae of up to 105 mm are found, which have probably overwintered (Lanza et al., 2007). The Italian Crested Newt reaches an average age of 8-9 years, but a maximum age of 18 years has been recorded (Lanza et al., 2007).

Distribution

Eggs and larvae of the crested newt species cannot be distinguished morphologically and a

Triturus carnifex occurs in Italy, a large part of Austria and a small area of southern Switzerland. To the east, it reaches the northern Balkans, the western tip of Hungary, Slovenia, Croatia and the northwest of Bosnia-Herzegovina

Triturus carnifex larva. Art: Bas Teunis. From: Griffiths, 1996.

The range of Triturus carnifex.

Eggs and larvae

341

(Arntzen, 2003; Jehle et al., 2011). There are introduced populations in western Switzerland, southern Germany, the Azores island of São Miguel, the Netherlands, and the UK (Arntzen, 2003; IUCN, 2013).

Habitat

Triturus carnifex inhabits a broad variety of terrestrial habitats from beech woodlands to arid Mediterranean areas. The Italian Crested Newt breeds in all sorts of water bodies from artificial ponds, densely vegetated pools, and large quarries, to small drinking troughs. Among the crested newt species, T. carnifex is the species with the widest ecological range (Arntzen, 2003).

Behaviour

Adult newts arrive at the breeding waters between early March and early April, and leave the water at the end of July. They overwinter in some ponds and can be found all year round (Arntzen, 2003). Triturus carnifex is a voracious, opportunistic feeder. Both adults and larvae feed on the larvae of Odonata, Ephemeroptera and Diptera. Cladocera, Copepoda and Ostracoda are eaten by larvae while adult insects, and amphibian eggs and larvae are eaten more by adults (Arntzen, 2003). The reproductive biology and courtship behaviour repertoire of crested newt species are by and large the same (Arnold, 1972

provides a description of the behaviour repertoire of T. carnifex) and are described under T. cristatus.

Threats and conservation

Although locally still abundant in the south of its range, this species has disappeared in some places in the Po Plain. It is hardy and survives in a variety of habitats, including man-made water bodies, but is sensitive to changes in water quality, such as those caused by industrial pollution and destruction or drainage of ponds. In some areas, introduced predatory fish have caused population declines. The species is protected by national legislation in most countries and it is listed on Appendix II of the Bern Convention. It is listed on annex IV of the EU Natural Habitats Directive. Its status is considered to be of Least Concern (IUCN, 2013).

Observations in captivity

The Italian Crested Newt can be kept and bred in captivity and can often be persuaded to live in water all year round.

Comments

References to summary chapters and books are given under T. cristatus. A good synthesis of the biology of this species is given by Arntzen (2003) and Lanza et al. (2007).

References

Arnold (1972); Arntzen (2003); IUCN (2013); Jehle et al.

(2011); Lanza et al. (2007); Wielstra (2013c).

Triturus cristatus (Laurenti, 1768) | Northern Crested Newt Description

A large-bodied newt. Head as long as or a little longer than wide and snout rounded. Eyes fairly prominent. Labial folds well-developed in the aquatic stage. Gular fold present. Body stout with rounded trunk. Tail a little shorter or as long as the rest of the body, strongly compressed and with pointed tip. The adult male in breeding condition has a high denticulated dorsal crest, interrupted just above the tail-base. It has a similar crest on the tail, but less indented. A straight crest on the underside of the tail. The female does not have a dorsal crest but a vertebral groove. Her tail has both a dorsal and ventral fin. Limbs well-developed. Fingers and toes flattened, rather long in the male and without webbing. During the terrestrial phase, the skin remains moist. After the breeding season the crest is reduced to an indistinct skin fold. The cloaca of the breeding male is strongly swollen and rounded. The cloacal slit is elongated. The female cloaca is less prominent, oval in shape and with a short cloacal slit (Thorn, 1969). Upperparts dark brown to grey with more or less distinct large black patches. The sides of body and head are sprinkled with

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small white spots. Underside yellow to orange with irregular shaped black spots. The female has a yellow or orange line along the lower edge of the tail. Toes are marked with fine black and yellow bands. In breeding condition, the male has a whitish, mother-of-pearl coloured flash running along the middle of the tail. The male is usually ca. 13.5 cm, the female 16 cm, maximum 18 cm (Thorn, 1969).

Diagnosis

A large, dark coloured newt with rough skin. A high dorsal crest in the male, strongly indented above the tail-base. Compared with the other crested newt species Triturus cristatus has a slender build (only T. dobrogicus has a more slender body form) and heavily white-stippled sides. Throat a muddied mix of black and yellow with fine white stippling. Ventral surface yellow-orange with irregular black spots (Arntzen, 2003; Wielstra et al., 2013c).

Eggs and larvae

A female deposits her eggs singly by wrapping them in aquatic plants, preferably close to the

Triturus cristatus, male (right) and female, the Netherlands. Photo: Jelger Herder.

water surface (Arntzen & Hedlund, 1990), and may lay ca. 200-400 eggs per season. The embryos of crested newts are white, light yellow or very light green, 1.9-2.4 mm in diameter, and surrounded by a transparent, gelatinous capsule about 5 mm in diameter (Arntzen, 2003). Temperature determines the speed of embryonic development. The time from egg laying to hatching is normally between 15-20 days. At hatching larvae measure 10.5-11.5 mm and have a pair of balancers. Fully developed larvae have a conspicuous tail-fin which tapers to a fine point, and elongate, slender digits. There are dark spots on the body and tail. The head is rounded and flattened and has three pairs of bushy gills behind it (Griffiths, 1996). Larvae of Triturus cristatus have 13-14 costal grooves (T. dobrogicus also 13-14; T. karelinii 9-10; Kuzmin, 1999).

reaches the Ural Mountains and Western Siberia (Litvinchuk & Borkin, 2010). The southern border extends from central France, north of the Alps to the Balkans.

Habitat

Triturus cristatus inhabits a broad range of water bodies with permanent stagnant or semi-flowing water such as ponds with aquatic vegetation and without fish, flooded quarries, swampy areas along rivers, and irrigation channels and ditches. Crested newts usually prefer more open, larger and deeper water bodies than other newt species (Jehle et al., 2011). The surrounding terrestrial habitat may consist of coniferous, mixed, and deciduous forests, and bush lands, pastures, meadows, parks and gardens (Arntzen, 2003). In the terrestrial phase the newt lives a secretive life, mostly underground in

Larvae metamorphose at a total length of 52-90 mm (Kupfer, 1997). Some larvae may overwinter and metamorphose the following year. Partial neoteny occurs regularly. Growth is dependent on altitude. In the northern parts of the range, growth is slower than in more south-westerly areas. Sexual maturity is reached after 2-3 years and after 3-4 years in Scandinavia. Males reach sexual maturity earlier than females. The maximum age so far recorded for free-ranging T. cristatus is 13-18 years (Arntzen, 2003).

Distribution

Triturus cristatus occupies the largest range of all Triturus species, occurring in most parts of the Western Palearctic. In the west its range extends to central France, the Benelux countries and Great Britain. In northern Europe, the species occurs in Scandinavia. In the eastern part of its range it

The range of Triturus cristatus. 343

rodent burrows and crevices beneath tree stumps. Triturus cristatus is generally considered a lowland species, although it occurs up to 1,750 m in the Alps (IUCN, 2013). Crested newts tend to be more aquatic than marbled newts and the smallbodied European newt species. Immature newts can sometimes be found in water.

Behaviour

Triturus cristatus usually overwinters on land, under logs, in burrows and in rotten trees, but often also in water. Male and female newts leave their terrestrial winter refuges in spring and then congregate in ponds in order to breed. Males arrive around a week before the females. They are ready to mate soon after entering the water. In an Atlantic climate, the migration to the breeding ponds takes place between the end of February and early May and the animals leave the water between mid-July and October (Arntzen, 2003). During the terrestrial stage, the animals are mainly active at night. In the aquatic phase they show a crepuscular daily rhythm with peaks of activity in the late evening and early dawn (Arntzen, 2003).

Triturus cristatus is a voracious, unselective feeder, preying on a wide range of water fauna. Besides aquatic insects, the food spectrum includes leeches (Erpobdella), snails, freshwater shrimp (Gammarus), small-bodied newts and their larvae, and frog spawn and tadpoles. They may also cannibalise their own smaller congeners (Arntzen, 2003). Crested newts are preyed upon by a wide range of predators, such as fish, snakes and birds. The reproductive biology and courtship behaviour repertoire of T. cristatus has been described from observations in captivity (Arnold, 1972 for T. carnifex; Halliday, 1977; Green, 1989) and in the field (Zuiderwijk & Sparreboom, 1986; Arntzen & Sparreboom, 1989; Hedlund, 1990; Zuiderwijk, 1990). When darkness falls, breeding males move to open spots and space themselves out over the bottom of the pond. Males interact actively and are aggressive towards each other, a feature also seen in T. marmoratus and the two Ommatotriton species, but not in the small-bodied European newts. During male-male encounters the aggressive display consists of pushing the other away, arching the back into a ‘cat-buckle’ and making tail lashes. A male may also raise himself on his fore legs, with tail and hind body waving over the body of his opponent. Such intermale encounters are more frequent than male-female encounters (Zuiderwijk & Sparreboom, 1986; Hedlund, 1990) and can be interpreted as a form of territorial behaviour, intended to monopolise places suitable for courtship. When a female approaches a male that has taken up position on a suitable spot, the male will start displaying to her. He arches his back and 344

Salamanders of the Old World | Triturus

leans in over her snout and body while standing on his fore legs. He beats his tail in the direction of the female and while displaying rocks his body rhythmically from side to side. The tail beats are interrupted by a more violent action whereby the tail is lashed rapidly in the direction of the female, often slapping her on the head or flank. These tail lashes produce a current of water that is often strong enough to displace both male and female. After the male has convinced the female of his qualities and once she is receptive, he turns around and creeps ahead of her, his tail folded harmonica-wise and making undulating movements. The female touches his tail with her snout and the male deposits a spermatophore on the substrate and leads the female over it. As the female continues to creep behind him, the spermatophore will adhere to the lips of her everted cloaca and be absorbed into her body. Most courtship sequences are not successfully completed as rival males constantly interfere with ongoing courtships. This mating system, where males congregate in a communal display area for the purpose of attracting and courting females, and where females come to choose a mate, is called a lek. It is common in birds and chorusing frogs, but was an unexpected finding in newts (Zuiderwijk & Sparreboom, 1986; Hedlund & Robertson, 1989). Crested newt females prefer males with high crests over males with lower crests and make the assessment visually (Malmgren & Enghag, 2008).

Threats and conservation

Triturus cristatus is sensitive to changes in water quality, for instance those caused by industrial water pollution and destruction or drainage of ponds. In some areas, introduced predatory fish lead to population declines and in other parts of its range, such as the countries of the former Soviet Union, there is substantial commercial collecting of this species for the pet trade. It is protected in many countries and is listed on annexes II and IV of the EU Natural Habitats Directive. Given its vast distribution, this species status is on the whole considered to be of Least Concern (IUCN, 2013).

Observations in captivity

Triturus cristatus can be kept and bred in captivity (Kühnel, 1983). Individuals have lived in captivity for many years and Thorn (1969) cites a record of a captive specimen reaching 27 years of age.

Comments

State-of-the-art knowledge of the Triturus cristatus species group is found in the Handbuch der Reptilien und Amphibien Europas (Arntzen, 2003). An informative monograph has been produced by Burkhard Thiesmeier (Laurenti Verlag), first authored by Thiesmeier & Kupfer in German (2000) and followed by a second German edition (Thiesmeier, Kupfer & Jehle, 2009) and a third edition in English (Jehle, Thiesmeier & Foster, 2011). Another recent synthesis on

crested newts is the book by Litvinchuk & Borkin (2010, in Russian). The evolution of the male dorsal crest in newts, such a typical feature of T. cristatus, is addressed by Wiens et al. (2011).

References

Griffiths (1996); Halliday (1977); Hedlund (1990); Hedlund & Robertson (1989); IUCN (2013); Jehle et al. (2011); Kupfer (1997); Kühnel (1983); Kuzmin (1999); Litvinchuk & Borkin (2010); Malmgren & Enghag (2008); Thiesmeier & Kupfer (2000); Thiesmeier et al. (2009); Thorn (1969);

Arnold (1972); Arntzen (2003); Arntzen & Sparreboom

(1989); Arntzen & Wallis (1999); Beebee & Griffiths (2000); Green (1989);

Wielstra et al. (2013c); Wiens et al. (2011); Zuiderwijk (1990); Zuiderwijk & Sparreboom (1986).

Triturus dobrogicus (Kiritzescu, 1903) | Danube Crested Newt

Triturus dobrogicus, male. Photo: Max Sparreboom.

Description

A medium- to large-bodied newt with long, narrow head. It is the smallest and most slender of the crested newt species, with relatively short limbs and a long body. The dorsal side is black or dark brown. The flanks are dotted with small white spots. The throat is black or grey, and spotted with white. Some females have a yellow dorsal stripe as in Triturus carnifex. The colour of the ventral side is orange to red, with small to medium-sized, sharply delineated black blotches. In the breeding season, the male has a high, deeply serrated dorsal crest, the highest of all crested newt species.

Eggs and larvae

A full description is given under Triturus cristatus. Triturus dobrogicus has the smallest egg size, the smallest larval size, the longest embryonic and larval periods and the largest metamorphosed juveniles of all the European

The male attains a maximum size of 120-140 mm, the female 130-184 mm (Arntzen, 2003).

Diagnosis

A large, dark coloured newt with rough skin. The male has a very high dorsal crest, strongly indented at the tail-base. It has a very slender build compared with other crested newt species; heavily white-stippled sides; black throat with large angular white spots, especially in the male; and a deep orange coloured ventral surface with many sharp, roundish black spots (Arntzen, 2003; Wielstra et al., 2013c).

Triturus dobrogicus, pair. Photo: Max Sparreboom. 345

crested newt species (Vörös & Arntzen, 2010; Cvijanovic et al., 2009; Furtula et al., 2009). Larvae of T. dobrogicus have 13-14 costal grooves, more than the other crested newt species. Larvae smaller than 20 mm are coloured black, and larger larvae are light brown (Kuzmin, 1999; Arntzen, 2003). Sexual maturity is reached after 2-3 years. Adults may live for up to 8 years or more (Thonke et al., 1994).

Romania, northern Bulgaria, southern Moldova and southwest Ukraine, and in Hungary, eastern Austria, Slovakia, Slovenia, extreme northern Bosnia-Herzegovina, northern Serbia and northern Croatia. It is generally found in lowland areas below 300 m (Arntzen et al., 1997; IUCN, 2013).

Habitat

Triturus dobrogicus inhabits open habitats with mixed deciduous forests, bushlands, flooded lowlands with lakes and oxbows, and also agricultural landscapes and villages, and riparian groves in steppe regions. It is strictly aquatic in some instances. Reproduction takes place in small ponds with stagnant water, or in channels, ditches and flooded areas (Griffiths, 1996; IUCN, 2013).

Behaviour

The behaviour patterns of Triturus dobrogicus resemble those of the other crested newt species and are described under T. cristatus. The long duration of the aquatic stage is typical of this species’ behaviour.

Threats and conservation

This species is sensitive to changes in water quality, for example those caused by industrial water pollution and destruction or drainage of ponds. The main cause of its decline is habitat destruction through the conversion of wetlands, (semi-)natural land and pasture into arable fields. Given its small range, relative rarity and the rapid loss of its habitat, Arntzen et al. (1997) describe the conservation status of Triturus dobrogicus as Vulnerable. The species is listed as Near Threatened by IUCN (2013).

Observations in captivity The range of Triturus dobrogicus.

Distribution

The distribution of Triturus dobrogicus is restricted to the Pannonian and Dobrogean lowlands of central and Eastern Europe. It covers the floodplains of the Danube, Tisza, Drava and Sava Rivers and is bounded by the mountains occupied by other crested newt species. It occurs in western

The Danube Crested Newt has frequently been kept and bred in captivity (Schultschik, 2013f).

References

Arntzen (2003); Arntzen et al. (1997); Cvijanovic et al.

(2009); Furtula et al. (2009); Griffiths (1996); IUCN (2013); Jehle et al. (2011); Kuzmin (1999); Schultschik (2013f); Thiesmeier & Kupfer (2000); Thiesmeier et al. (2009); Thonke et al. (1994); Vörös & Arntzen (2010); Wielstra et al. (2013c).

Triturus ivanbureschi Arntzen & Wielstra, 2013 | Balkan-Anatolian Crested Newt Description and diagnosis

A large-bodied newt with strong limbs, a sturdy roller-shaped body, a large head and a relatively short, flattened tail. This species and Triturus karelinii can only be separated using molecular genetic data and diagnostic morphological features have not yet been documented (Wielstra et al. 2013c). The description is given under T. cristatus and T. karelinii.

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Total length of newts from southwest Turkey maximum 15 cm, from Greece 16 cm (Franzen et al., 2008; Trapp, 2007; Valakos et al., 2008).

Eggs and larvae

Eggs and larvae of the crested newt species cannot be distinguished morphologically. A full description is given under Triturus cristatus.

Triturus ivanbureschi, male, Thrace, Greece. Photo: Benny Trapp.

Triturus ivanbureschi, female, Thrace, Greece. Photo: Benny Trapp.

Triturus ivanbureschi, male on land, SW Turkey. Photo: Max Sparreboom.

Distribution

Triturus ivanbureschi occurs on the south-eastern Balkan Peninsula, covering most of Bulgaria, the eastern parts of Greece, Macedonia and Serbia, as well as European Turkey. The Asian distribution is restricted to Asiatic Turkey, along the coast of the Aegean Sea, the Sea of Marmara and the Black Sea, extending to ca. 300 km inland (Wielstra et al., 2013c).

Habitat

Triturus ivanbureschi inhabits all kinds of water bodies such as ponds with and without vegetation, ditches, cisterns, quarries, lakes and flooded riversides. The altitudinal range in western Turkey is up to 1,200 m, and in Bulgaria up to 1,700 (Franzen et al., 2008; Stojanov et al., 2011).

Behaviour

Triturus ivanbureschi enters the water after hibernation or may hibernate on the bottom of the breeding pond.

The range of Triturus ivanbureschi.

In Bulgaria the breeding season starts in May (Stojanov et al., 2011). In Turkey the aquatic phase starts with the onset of the winter rains in December (Franzen et al., 2008). The species’ reproductive behaviour appears to be similar to that of T. cristatus and has been described under that species.

Threats and conservation

This species is sensitive to changes in water quality, for instance those caused by industrial water pollution and destruction or drainage of ponds. 347

Observations in captivity

The Balkan-Anatolian Crested Newt can be kept and bred in captivity (Kühnel, 1983).

Comments

The traditional species Triturus karelinii comprises three geographically structured, genetically divergent lineages, an eastern, central and western lineage. These forms are sufficiently separated to be regarded as distinct species. The name T. karelinii is now restricted to the eastern lineage; a new name T. ivanbureschi has been given to the central / western lineage; and a formal description of the third lineage awaits further data analysis. The name T. arntzeni, previously

used for the crested newts in the southeast Balkans, has been placed in the synonymy of T. macedonicus (Wielstra et al., 2013c). A thorough state-of-the-art review of the crested newt species is found in the Handbuch der Reptilien und Amphibien Europas (Arntzen, 2003).

References

Arntzen (2003); Franzen et al. (2008); Kühnel (1983);

Stojanov et al. (2011); Trapp (2007); Valakos et al. (2008) ; Wielstra et al. (2013c).

Triturus karelinii (Strauch, 1870) | Caucasian Crested Newt Description

A large-bodied newt with strong limbs, a sturdy roller-shaped body, a large head and a relatively short, flattened tail (Tarkhnishvili & Gokhelashvili, 1999). Upperparts olive or dark brown, with white spots on the flanks. The ventral blotches are rather small and often angular in shape, and the

Individuals can attain a size of 18-19 cm, but populations with much smaller individuals are known (Jehle et al., 2011).

Diagnosis

A large newt with strong limbs. A moderately indented dorsal crest in the male. It is the most stockily built of

Triturus karelinii, male, northern Turkey. Photo: Max Sparreboom.

Triturus karelinii, courting pair. Photo: Max Sparreboom.

colour pattern on the throat resembles that on the belly. The skin is smooth. Juveniles have a yellow dorsal stripe that remains visible in adult females. The dorsal crest of the breeding male is moderately indented. It extends along the whole body and tail, frequently without interruption at the tailbase. The black dorsal spots can turn greenish-blue in breeding males (Arntzen, 2003). 348

Salamanders of the Old World | Triturus

the crested newt species. Sides are densely covered with small white dots. Ventral surface is yellow-orange with many small to medium-sized spots, frequently angular in shape and continuing onto the throat (Arntzen, 2003; Wielstra et al., 2013c).

Eggs and larvae

Eggs and larvae of the crested newt species cannot be distinguished morphologically and a full description is given under Triturus cristatus. Larvae of T. karelinii have 9-10 costal grooves in contrast to the other crested newt species, which have a higher number. A clutch contains 150-190 eggs. Larvae metamorphose from August-

October at an age of 3-5 months. Sexual maturity is reached at an age of 5-6 years and maximum longevity has been estimated at 10-15 years (Kuzmin, 1999).

Behaviour

Triturus karelinii enters the water after hibernation. Spawning occurs in March-May and from MayJuly in the highlands. After reproduction, newts generally remain in the water until August. Larvae feed on microcrustaceans, molluscs and insects. Planktonic Daphniidae are a favoured food item, which corresponds to the nektonic habits of the well-developed newt larvae. Adults feed on all sorts of limnophilous organisms, such as Gastropoda, Ostracoda and Isopoda. On land they eat worms, slugs, spiders and insects (Kuzmin, 1999). Their reproductive behaviour appears to be similar to that of T. cristatus and is described under that species.

Threats and conservation

This species is sensitive to changes in water quality, for instance those caused by industrial water pollution and destruction or drainage of ponds. In the former Soviet Union there is significant commercial collecting for the pet trade. The status of Triturus karelinii in the Caucasus is not clear. The species is considered Rare in Georgia and Azerbaijan, and Vulnerable in Russia and Ukraine. It is listed as of Least Concern (Tarkhnishvili & Gokhelashvili, 1999; Kuzmin, 1999; IUCN, 2013).

Observations in captivity

The Caucasian Crested Newt can be kept and bred in captivity (Kühnel, 1983).

The range of Triturus karelinii.

Distribution

Triturus karelinii occupies an area extending from the tip of northeast Turkey to the Caucasus and the southern Caspian Sea coast in Iran. Formerly, the distribution of T. karelinii was thought to include the north and west of Turkey and the Balkans. The crested newts occurring in that area have now been assigned to a different species, T. ivanbureschi (Wielstra et al., 2013c).

Habitat

Triturus karelinii inhabits mountain forests, forest steppes and even true steppes. They are found on slopes and plateaus covered with meadows or xerophytic vegetation and containing small, stagnant swamps and ponds. Such habitats are found in the Crimea and southern Azerbaijan. The species tolerates drier habitats than other Triturus species. Reproduction takes place in slow-moving stream pools, ponds and occasionally drainage ditches. The altitudinal range extends from 50-2,200 m (Kuzmin, 1999; IUCN, 2013).

Comments

Triturus karelinii comprises three geographically structured, genetically divergent lineages, an eastern, central and western lineage. These forms are sufficiently separated to be regarded as distinct species. The name T. karelinii is restricted to the eastern lineage; a new name T. ivanbureschi has been given to the western lineage; a formal description of the third lineage awaits further data analysis. The name T. arntzeni, previously used for the crested newts in the south-east Balkans, has been placed in the synonymy of T. macedonicus (Wielstra et al., 2013c). Informative chapters on T. karelinii are found in Kuzmin (1999) and Tarkhnishvili & Gokhelashvili (1999). A recent synthesis of the crested newts is presented in the book by Litvinchuk & Borkin (2010, in Russian).

References

Arntzen (2003); IUCN (2013); Jehle et al. (2011); Kühnel

(1983); Kuzmin (1999); Litvinchuk & Borkin (2010); Tarkhnishvili & Gokhelashvili (1999); Wielstra et al. (2013c).

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Triturus macedonicus (Karaman, 1922) | Macedonian Crested Newt Description

A large-bodied newt. Similar to Triturus carnifex, but identification is difficult as some specimens may resemble any of the other crested newt species. Formerly considered a subspecies of T. carnifex, this taxon was elevated to species status because it forms an old and separate lineage (Arntzen et al., 2007a). The Macedonian Crested Newt differs in colour from T. carnifex. It has small, unblurred, black ventral blotches and spots, and a yellow rather than orange ventral colouration. The dorsal yellow stripe is mostly missing, and the white dots on the flanks are more numerous (Arntzen, 2003). Total length 13-15 cm (Valakos et al., 2008; Stojanov et al., 2011), sometimes up to 20 cm (Trapp, 2007).

Diagnosis

A large, dark coloured newt with rough skin. A high dorsal crest in the male, strongly indented at the tail-base. It has a medium, stocky build compared with the other crested newt species and sides are densely white-stippled. Throat is dark black or a muddied mix of black and yellow with many medium sized white stipples. Ventral surface yellow to orange-yellow with a dense pattern of small, irregular spots (Wielstra et al., 2013c).

Eggs and larvae

Eggs and larvae are similar in all crested newt species and are described in the Triturus cristatus species

entry. As in T. carnifex, giant larvae of more than 10 cm long have been recorded (Trapp, 2007).

Distribution

Triturus macedonicus was previously considered a subspecies of T. carnifex but their distribution ranges have been separated for more than five million years. Triturus macedonicus occupies the southern Balkans. It occurs in the south-east of Bosnia-Herzegovina, in Montenegro, southern Serbia and in Albania, Macedonia and north-western Greece (Arntzen, 2003; Jehle et al., 2001). It reaches the Slavjanka mountains in the extreme south-western tip of Bulgaria (Stojanov et al., 2011).

Habitat

Triturus macedonicus inhabits a wide variety of terrestrial and aquatic habitats comparable to T. carnifex. Records in Greece are mainly from higher elevations, up to 1,725 m on Mt. Arenes. Here the newts inhabit medium-sized mountain lakes without fish, and melt-water ponds, but also smaller pools, quarries and cattle drinking troughs (Trapp, 2007).

Behaviour

The aquatic phase extends from February to October-November. Reproduction takes place in March-June. A second breeding period has been observed during the autumn in southern populations (Valakos et al., 2008).

Triturus macedonicus, male, Pindos mountains, Greece. Photo: Benny Trapp. 350

Salamanders of the Old World | Triturus

Adult newts arrive at the breeding waters between early March and early April, and leave the water at the end of July. The reproductive biology and courtship behaviour repertoire of crested newt species are by and large the same (Arnold, 1972 provides a description of the behaviour repertoire of Triturus carnifex) and have been described under T. cristatus.

Threats and conservation

The threats to habitats of this species are similar to those applying to Triturus carnifex. Its conservation status has not yet been assessed (IUCN, 2013).

Observations in captivity

Like the other crested newt species, the Macedonian Crested Newt can be kept and bred in captivity.

Comments

References to summary chapters and books are given under Triturus cristatus.

References

Arnold (1972); Arntzen (2003); Arntzen et al. (2007a);

IUCN (2013); Jehle et al. (2011); Stojanov et al. (2011); Trapp (2007); Valakos et al. (2008) ; Wielstra et al. (2013c).

The range of Triturus macedonicus.

Triturus marmoratus (Latreille, 1800) | Northern Marbled Newt Description

A relatively stocky, large-bodied newt. Head as long as wide and snout flattened, large and rounded. Labial folds well-developed in the aquatic stage. Gular fold present. Body stout with rounded trunk. Tail strongly compressed, as long as or a little longer than the rest of the body and terminating in a pointed tip. The adult male in breeding condition shows a high dorsal, lightly undulating crest, extending onto the tail. The crest is often lower but not interrupted above the tail-base. There is a straight crest on the underside of the tail. The female does not have a dorsal crest but a vertebral groove,

often coloured yellow or orange. Her tail has both a dorsal and ventral fin. Limbs well-developed. Fingers and toes without webbing, flattened and longer in the male. The skin of the upperside is more or less granulated, a little smoother on the underside. The cloaca of the breeding male is strongly swollen and rounded, as in Triturus cristatus (Thorn, 1969).

Triturus marmoratus, male, Creuse, France. Photo: Max Sparreboom.

Triturus marmoratus, female, Creuse, France. Photo: Max Sparreboom.

Upperparts lively green, olive or yellow-green with an irregular design of large black patches. The male dorsal crest has vertical bars, coloured black and whitish or greenish. The female shows

351

2004). Eggs are attached to the leaves of submersed aquatic plants, between October-July, depending on altitude. Eggs and larvae cannot be distinguished from those of Triturus pygmaeus and T. cristatus, except by analysis of enzymes (Espregueira Themudo & Arntzen, 2007a). Older larvae have a greenish sheen and 12-13 costal grooves on each side of the body (Thorn, 1969). Larvae metamorphose at a total length of 40-70 mm (Herrero et al., 2003a). Sexual maturity is reached after 3-5 years. The maximum recorded life span for T. marmoratus is 14 years in France and 15 years in Portugal (Francillon-Vieillot et al., 1990).

Distribution

Triturus marmoratus inhabits much of northern Spain and Portugal, and central, southern and western France. In France, there is a broad region of overlap between T. marmoratus and T. cristatus. These two species differ in many respects and show a different habitat preference, but hybridisation does occur (Schoorl & Zuiderwijk, 1981; Arntzen et al., 2009). Triturus marmoratus and T. pygmaeus share a parapatric range border from coastal Portugal to central Spain. The two species occasionally hybridise (Espregueira Themudo & Arntzen, 2007a).

Habitat The range of Triturus marmoratus.

an orange vertebral stripe; juveniles of both sexes have a bright orange dorsal stripe running over the back and tail. The male in breeding condition has a silvery flash on the tail. In terrestrial condition the green colour is brighter and the skin is dry and granulated. Underside grey, brown, pink or blackish with white dots, sometimes marbled with indistinct black or white and black patches. Average total length 130-148 mm, rarely round 160 mm, females a little larger than males (Herrero et al., 2003a).

Diagnosis

A large, stocky newt with rough skin. A high dorsal crest in the male in breeding condition, a little lower but not indented above the tail-base. Dorsal colour marbled green; underside without yellow or orange colouration (Thorn, 1969). Triturus marmoratus differs from T. pygmaeus in the following respects. Triturus pygmaeus is a small to medium-sized newt with rough skin and a relatively low dorsal crest in the male in breeding condition, extending onto the tail without interruption at the tail-base. Dorsal colour marbled green, underside yellow or orange, transparent with white dots and black spots.

Eggs and larvae

A female lays hundreds of eggs, up to an estimated 416 (Arntzen & Hedlund, 1990) or 500 (Malkmus,

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Salamanders of the Old World | Triturus

Triturus marmoratus is the most terrestrial Triturus species, spending more time on land than the others. The terrestrial habitat generally comprises the area close to the breeding pond (Jehle, 2000). Aquatic habitats of T. marmoratus include well-vegetated ponds, pools, ditches and streams, generally in dry woodlands, heathland, fields and rough grassland, including traditional farmland (IUCN, 2013). Triturus marmoratus is found from sea level up to 1,930 m, with a preference for altitudes between 500-900 m (Malkmus, 2004). In Spain it has been recorded at 2,100 m (García-París et al., 2004; Montori, 2010). Habitat separation appears to exist in areas of range overlap with T. cristatus. Triturus marmoratus favours hilly and wooded environments with many terrestrial hiding places while T. cristatus generally inhabits flat, open places (Schoorl & Zuiderwijk, 1981). In the Iberian Peninsula, in the contact zone with T. pygmaeus, T. marmoratus thrives in more permanent water bodies with regular but low annual recruitment, whereas T. pygmaeus thrives in ephemeral ponds with fluctuating breeding populations (Espregueira Themudo & Arntzen, 2007a).

Behaviour

Triturus marmoratus usually overwinters on land. In the southern part of its range, migration to the breeding sites follows the onset of autumn rains. Part of the population overwinters in water. As temperatures rise from January onward, another part of the population moves to the breeding ponds. Breeding and egg laying starts in February (in southern France, Jakob et al., 2002; Duguet & Melki, 2003). In the northern parts of its range, reproduction starts in March. The aquatic stage

lasts about three months, which is about two months shorter than in T. cristatus (Jehle, 2000). Like T. cristatus, T. marmoratus is a voracious, unselective feeder, preying on a wide range of aquatic fauna. Larvae feed on Cladocera, Ostracoda and Copepoda, while adults prey on crustacaeans, larvae of Diptera, Trichoptera and Ephemeroptera,

and amphibian eggs and larvae, including their own species. On land they eat mainly Gasteropoda, larvae of Lepidoptera, small insects and worms (Montori, 2010). The reproductive behaviour of T. marmoratus has been described on the basis of observations in the natural habitat and in the laboratory (Zuiderwijk & Sparreboom, 1986;

A

D

B

E

C

F

Courtship behaviour sequence in the Northern Marbled Newt (Triturus marmoratus). A. The male (left) begins courtship by taking up position in front of the female (right); he bends his tail in her direction and slightly arches his back. B. The male, his body arched in a catbuckle, his head held parallel to that of the female, raises his hind body and lifts his hind legs off the substrate. The tail may be kept still or make irregular waving movements. C. The male, viewed from behind, stands on his hands and delivers a forceful tail-lash in the direction of the female, thereby occasionally touching her head and body. D. The male has turned round and creeps ahead of the female (right), his cloaca fully opened; the female touches his tail; the male deposits a spermatophore. E. After depositing a spermatophore, the male turns 90° and assumes a side-on position. The female follows and presses her snout against the male’s tail or cloacal region. The male may push her slightly back. F. After spermatophore deposition and – in this case – successful sperm pick-up, the male may occasionally bite the female, holding on to her for some seconds. Art: Bas Teunis. From: Sparreboom & Teunis, 1990. 353

Sparreboom & Teunis, 1990; Zuiderwijk, 1990). When darkness falls, breeding males move to open spots and space themselves out over the bottom of the pond. Males actively interact and show aggression towards each other, a feature also seen in T. cristatus and the two Ommatotriton species, but not in the small-bodied European newts. This behaviour is described in more detail under T. cristatus. Triturus marmoratus uses more physical effort in male-male encounters than does T. cristatus under the same circumstances. A male that occupies a territory may push and bite an intruder and make vigorous tail-lashes in his direction, thus chasing him away from his temporary territory (Zuiderwijk, 1990). The sexual behaviour of T. marmoratus is similar to that of T. cristatus, but differs from it in the temporal patterns of a number of display behaviours. Furthermore, there are differences in frequency and intensity of certain displays. ‘Rocking’ behaviour is virtually absent in T. marmoratus, whereas in T. cristatus this is the most developed form of courtship movement. T. marmoratus shows a less extreme ‘cat-buckle’ display than T. cristatus and a higher frequency of ‘tail-lashes’ (Sparreboom & Teunis, 1990). Behaviour patterns may vary between different parts of a species’ range. The courtship of T. marmoratus shows clear differences from that of T. pygmaeus, its closest relative. These are described under T. pygmaeus (Hidalgo-Vila et al., 2002).

Threats and conservation

This species is threatened by agricultural intensification, drainage, pollution and

eutrophication of water bodies. Introduced diseases, as well as introduced predatory fish and crayfish, pose threats in parts of the species’ range. It is protected by national legislation throughout its range and listed on Annex IV of the EU Habitats Directive and on Annex III of the Bern Convention. Its status is considered to be of Least Concern by IUCN (2013).

Observations in captivity

Both species of marbled newt can be kept and bred in captivity (Diesener, 1982). Captive individuals may live for many years and Thorn (1969) cites a record of one reaching over 25 years of age.

Comments

A thorough state-of-the-art review of Triturus marmoratus is found in the Handbuch der Reptilien und Amphibien Europas (Herrero et al., 2003a). Good syntheses are given in the Amphibia volume of the Fauna Iberica (GarcíaParís et al., 2004) and the virtual encyclopaedia on the Spanish vertebrates (Montori, 2010).

References

Arntzen & Hedlund (1990); Arntzen et al. (2009);

Diesener (1982); Duguet & Melki (2003); Espregueira Themudo & Arntzen (2007a); Francillon-Vieillot et al. (1990); García-París et al. (2004); Herrero et al. (2003a); Hidalgo-Vila et al. (2002); IUCN (2013); Jakob et al. (2002); Jehle (2000); Malkmus (2004); Montori (2010); Schoorl & Zuiderwijk (1981); Sparreboom & Teunis (1990); Thorn (1969); Zuiderwijk (1990); Zuiderwijk & Sparreboom (1986).

Triturus pygmaeus (Wolterstorff, 1905) | Southern Marbled Newt, Pygmy Newt Description

Triturus pygmaeus is the smallest of the largebodied newts in the genus Triturus. It is similar in colouration to the Northern Marbled Newt, Triturus marmoratus, of which it was long considered to be a subspecies. The two forms are genetically isolated and are both now regarded as full species (Espregueira Themudo & Arntzen, 2007a).

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well-developed in the aquatic stage. Tail compressed near the tip and relatively short. The crest is similar to that of T. marmoratus, but lower and straighter, without a dip at the tail-base. Bronze-coloured spots may appear in breeding males (García-París et al., 1993, 2001; Herrero et al., 2003b).

Head a little longer than wide with rounded snout and big eyes. Gular fold present and paratoids clearly visible. Labial folds

In the terrestrial phase the dorsal colour pattern shows irregular black patches on a green background. These patches may form a single row along the flanks, with green the dominant colour.

Triturus pygmaeus, male, Nisa, Portugal. Photo: Max Sparreboom.

Triturus pygmaeus, female, Nisa, Portugal. Photo: Max Sparreboom.

Salamanders of the Old World | Triturus

In females the dorsal mid-line is orange and continuous, in the males it is blotched with black. The ventral side is mostly un-pigmented, yellow or pink and transparent. It is covered on the sides with black dots and small white dots, which may be clustered to form larger white blotches. The black spots on the underside are larger and more rounded in the male than in the female (García-París et al., 1993, 2001; Herrero et al., 2003b). Average total length between 90-125 mm, usually not exceeding 140 mm (García-París et al., 2004). Populations with very smallsized newts (75-77 mm) are described from Doñana (DíazPaniagua et al., 1996).

Diagnosis

Small to medium-sized newt with rough skin. A relatively low dorsal crest in the male in breeding condition, extending onto the tail without interruption at the tail-base. Dorsal colour marbled green, underside yellow or orange, transparent with white dots and black spots. Triturus pygmaeus differs from T. marmoratus in the following respects: Triturus marmoratus is a larger, stocky newt with rough skin and a high dorsal crest in the male in breeding condition, a little lower but not indented above the tail-base. Dorsal colour marbled green, underside without yellow or orange colouration (Thorn, 1969).

Eggs and larvae

The range of Triturus pygmaeus.

Eggs and larvae cannot be distinguished from T. marmoratus morphologically. A female lays hundreds of eggs, various reports claiming numbers between 148-382. Larval development takes 3.5 months. Larvae measure 37-56 mm at metamorphosis. Recently metamorphosed newts have been observed from May onwards (Herrero et al., 2003b). Pygmy Newts from Doñana mature at the age of two years, with a small number maturing at the age of one year. Longevity was reported as 9-10 years (Díaz-Paniagua, 1998). In populations from southern Portugal, sexual maturity is attained in the fourth year and maximum age is estimated to be 11-12 years (Herrero et al., 2003b)

Distribution

Triturus pygmaeus occurs on the Iberian Peninsula, where it is distributed in central and southern Portugal and the southern half of Spain. It occurs from sea level to 1,450 m altitude (IUCN, 2013). Triturus marmoratus and T. pygmaeus share a parapatric range border from coastal Portugal to central Spain. The two species are largely parapatric, but occasionally hybridise. Triturus pygmaeus appears to be expanding its range northwards and replacing T. marmoratus, which can only persist in areas where ecological conditions are relatively favourable (Espregueira Themudo & Arntzen, 2007a, 2007b).

Habitat

Triturus pygmaeus inhabits broadleaf woodland. It is found in traditional farmland areas and other lightly modified

Triturus pygmaeus, habitat, also of Lissotriton boscai, Olhos de Agua, Marvao, Portugal. Photo: Max Sparreboom. 355

habitats. Aquatic habitats used for reproduction include temporary or permanent ponds, lagoons, abandoned quarries and wells, drinking troughs, irrigation ponds, ditches and other water bodies (Malkmus, 2012; IUCN, 2013). In the contact zone with T. pygmaeus, T. marmoratus thrives in more permanent water bodies with regular but low annual recruitment, whereas T. pygmaeus thrives in ephemeral ponds with a fluctuating breeding population (Espregueira Themudo & Arntzen, 2007b).

Behaviour

The reproduction period varies greatly from one region to another. In the southern part of its range, migration to the breeding sites follows the onset of the autumn rains. In Doñana the newts are aquatic from November-May. A long period of draught and high temperatures between the end of spring and autumn drives the animals to inactivity (Herrero et al., 2003b). The larvae of Triturus pygmaeus actively forage in the water column, feeding on zooplankton and insect larvae. Adults feed mainly on insect larvae, crustaceans, worms and spiders (Reques, 2009). The courtship behaviour of T. pygmaeus has been described on the basis of observations of animals from Doñana (Hidalgo-Vila et al., 2002). Although broadly similar to that of T. marmoratus (Zuiderwijk & Sparreboom, 1986; Sparreboom & Teunis, 1990; Zuiderwijk, 1990), its courtship behaviour differs in some important aspects. One typical feature is the slow regular fanning movement of the tail, termed ‘slow-fan.’ During this behaviour, which is the most frequent movement in a courtship sequence of this species, the abdomen is curved slightly upwards in the centre and the head held up. Males perform this movement on the side facing the female. In contrast to the forceful tail-lashes of the large Triturus species, the tail only incidentally beats against the male’s flank and never touches the female. Furthermore, the male also tries to attract an initially unresponsive female with bait mimic tail movements, such as a movement

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with the tail held straight up, called ‘flamenco’ (Hidalgo-Vila et al., 2002). This behaviour was described earlier for Lissotriton boscai and L. italicus and also occurs in other species (Arntzen & Sparreboom, 1989). Aggressive male interactions, such as in T. marmoratus, have not been reported.

Threats and conservation

The species is threatened by habitat loss, especially the loss of temporary ponds. In the west of Spain and southern Portugal it is eaten by introduced nonnative crayfish and predatory fish. Many populations around Madrid have disappeared. Over-exploitation of groundwater, agrochemical pollution and loss of traditional breeding sites have led to a decline in southern and eastern Spain. Drainage of ponds, straightening of streams, increasing traffic and intensification of agriculture, all affect the species in Portugal also (Malkmus, 2004; IUCN, 2013). The species is listed on Annex III of the Bern Convention, and is protected by legislation in Spain. Its status is considered Vulnerable on the Spanish Red List and Near Threatened by IUCN (2013).

Observations in captivity

Pygmy newts can be kept and bred in captivity (Bogaerts, 2002, 2013c).

Comments

Good syntheses on Triturus pygmaeus are given in the Handbuch der Reptilien und Amphibien Europas (Herrero et al., 2003b), in the Amphibia volume of the Fauna Iberica (García-París et al., 2004) and in the virtual encyclopaedia on the Spanish vertebrates (Reques, 2009).

References

Arntzen & Sparreboom (1989); Bogaerts (2002, 2013c);

Díaz-Paniagua (1998); Díaz-Paniagua et al. (1996); Espregueira Themudo & Arntzen (2007a, 2007b); García-París et al. (1993, 2001, 2004); Herrero et al. (2003b); Hidalgo-Vila et al. (2002); IUCN (2013); Malkmus (2004, 2012); Reques (2009); Sparreboom & Teunis (1990); Zuiderwijk (1990); Zuiderwijk & Sparreboom (1986).

Tylototriton Anderson, 1871 The salamandrid genus Tylototriton is widely distributed from the eastern Himalayas, South-East Asia, to southern and central China. It is characterised by a combination of characteristics: two premaxillae; short nasal processes, not reaching the frontal; nasals broad, in contact with each other; frontosquamosal arch stout and ridged; maxilla long, in contact with the quadrate; vomerine teeth Λ-shaped. 13-15 trunk vertebrae; neural spines high and large; postsacral ribs on caudosacral vertrebrae. Head broad and large; labial folds inconspicuous; skin very rough, with warts and tubercles; vertebral ridge noticeable; limbs long, tips of fingers and toes overlap when adpressed; tongue small, free on both sides. The genus Tylototriton is distinct from Echinotriton in morphology, geographic distribution, and life history (Nussbaum & Brodie Jr, 1982; Zhao & Hu, 1988a). In Tylototriton the ribs of the middle trunk region are short and only slightly curved; all ribs are approximately the same length; the distal tips of the ribs are attached to trunk musculature and do not penetrate the skin. The skull is characterised by well-developed bony crests. Eggs have a diameter of less than 2.5 mm and are usually deposited in water (Zhao & Hu, 1988a). The genera Echinotriton and Tylototriton are placed in a clade with the European and North African genus Pleurodeles (Hayashi & Matsui, 1989; Weisrock et al., 2006; Pyron & Wiens, 2011). Taxonomic subdivision of the genus Tylototriton is a subject of debate. Most authors recognise two groups or subgenera, the T. verrucosus group and the T. asperrimus group. The first includes T. daweishanensis, T. kweichowensis, T. pseudoverrucosus, T. shanjing, T. taliangensis, T. uyenoi, T. verrucosus and T. yangi; the second includes T. asperrimus, T. broadoridgus, T. dabienicus, T. hainanensis, T. lizhenchangi, T. notialis, T. panhai, T. vietnamensis, T. wenxianensis, and T. ziegleri (Nishikawa et al., 2013c). Many new species have been described in recent years, and there are probably more to follow.

Tylototriton asperrimus Unterstein, 1930 Tylototriton broadoridgus Shen, Jiang & Mo, 2012 Tylototriton dabienicus Chen, Wang & Tao, 2010 Tylototriton daweishanensis Zhao, Rao, Liu, Li & Yuan, 2012 Tylototriton hainanensis Fei, Ye & Yang, 1984 Tylototriton kweichowensis Fang & Chang, 1932 Tylototriton lizhenchangi Hou, Zhang, Jiang, Li & Lü, 2012 Tylototriton notialis

Tylototriton taliangensis Liu, 1950 Tylototriton uyenoi Nishikawa, Khonsue, Pomchote & Matsui, 2013 Tylototriton verrucosus Anderson, 1871 Tylototriton vietnamensis Böhme, Schöttler, Nguyen & Köhler, 2005. Tylototriton wenxianensis Fei, Ye & Yang, 1984 Tylototriton yangi Hou, Zhang, Zhou, Li & Lü, 2012 Tylototriton ziegleri Nishikawa, Matsui & Nguyen, 2013

Distribution of the genus Tylototriton. Shaded areas indicate distribution of T. verrucosus. Stars refer to type localities. 1. T. wenxianensis, 2. T. dabienicus, 3. T. broadoridgus, 4. T. taliangensis, 5. T. pseudoverrucosus, 6. T. kweichowensis, 7. T. lizhengchangi, 8. T. asperrimus, 9. T. vietnamensis, 10. T. ziegleri, 11. T. daweishanensis, 12. T. yangi, 13. T. shanjing, 14. T. verrucosus, 15. T. hainanensis, 16. T. notialis, 17. T. panhai, 18. T. uyenoi. Further distribution data in text.

Stuart, Phimmachak, Sivongxay & Robichaud, 2010

Tylototriton panhai Nishikawa, Khonsue, Pomchote & Matsui, 2013 Tylototriton pseudoverrucosus Hou, Gu, Zhang, Zeng, Li & Lü, 2012 Tylototriton shanjing Nussbaum, Brodie & Yang, 1995

References

Hayashi & Matsui (1989); Nishikawa et al. (2013c);

Nussbaum & Brodie Jr (1982); Pyron & Wiens (2011); Weisrock et al. (2006); Zhao & Hu (1988a).

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Tylototriton asperrimus Unterstein, 1930 | Black Knobby Newt Description

A medium-sized Tylototriton. Head flat and oval, with prominent bony ridges. Head width slightly larger than head length. Rounded snout. No labial fold. Gular fold conspicuous. Body slender and flattened. When limbs are adpressed, digits meet or slightly overlap. Dorsal ridge distinct but low and segmented; dorso-lateral warts prominent. Skin rough, with fine granules. Small transverse wrinkles present on venter. Tail compressed laterally and ending in a pointed tip. Tail shorter than snout-vent length (Zhao, 1998). Colour uniformly greyish-black. Ventral side lighter. Tips of digits, cloaca and lower margin of tail orange-red (Fei et al., 1984; Fei et al., 2005). Some individuals from the type locality have a few orange-tinted dorso-lateral warts (Yunke Wu, pers. com.). In the breeding season, small papillae are visible in the males’ cloaca (Fei et al., 2006).

Eggs and larvae

Clutches of 30-52 eggs are laid under dead leaves on the slopes of a breeding pond. Egg diameter 3.0-3.4 mm, diameter of gelatinous envelope after fully absorbing water is 10 mm (Ye et al., 1993; Zhao, 1998; Xie, 1999). Larvae develop in water.

Distribution

This species is widely distributed in central and southern China (Guangxi, Guangdong, Guizhou, Hunan and Anhui Provinces) at altitudes of 400-1,700 m. Localities reported for northern Vietnam may actually refer to T. ziegleri or T. vietnamensis (Schöttler, 2003; Bain & Nguyen, 2004; Böhme et al., 2005; Nishikawa et al., 2013a). The precise boundary of the species’ distribution is unclear.

Habitat

Tylototriton asperrimus lives under dead leaves or in root holes near water in heavily shaded forest in the mountains (Zhao, 1998). It breeds in small temporary ponds in bamboo and primary forest (IUCN, 2013).

Total length 115-144 mm for males (Fei et al., 2006).

Tylototriton asperrimus, Yaoshan, Guangxi (type locality). Photo: Yunke Wu.

Diagnosis

A medium-sized black Tylototriton, with 13-16 black dorso-lateral warts on each side. Separation between warts is clear (Fei et al., 2006). Snout more rounded and bony ridges on head more prominent than in Tylototriton vietnamensis (Böhme et al., 2005). The species resembles T. wenxianensis and T. hainanensis, but differs from T. wenxianensis by clearly separated large dorso-lateral warts and from T. hainanensis by a relatively narrower head and smaller body size.

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Salamanders of the Old World | Tylototriton

Tylototriton asperrimus, in natural habitat, Yaoshan, Guangxi. Photo: Yunke Wu.

Behaviour

This species lives on land outside the breeding season, where it feeds on insects and their larvae, earthworms, spiders, slugs and other small invertebrates (Zhao, 1998). Breeding season is in April-May. Males have been seen entering the water, but reproductive behaviour has not yet been observed. Females lay egg clutches on land under dead leaves, like Echinotriton chinhaiensis (Ye et al., 1993; Xie, 1999; Bain & Nguyen, 2004).

Threats and conservation

The major threat to this species in China is harvesting for use in traditional Chinese medicine. Habitat is being lost and degraded as a result of agricultural practices and collection of wood (IUCN, 2013). Illegal collection for the pet trade may pose another threat (Yunke Wu, pers. comm.). Tylototriton asperrimus is listed as Near Threatened (IUCN, 2013).

Observations in captivity

Captive observations of animals sold through the pet trade as Tylototriton asperrimus have been published by Fleck, who reports successful captive breeding. The animals were kept on land during winter. From March onward they were housed in aquaterrariums with water 10 cm deep. Eggs were laid in water, attached to cork bark. Larvae hatched at the end of May-early June. Fully developed larvae had conspicuously long, flag-like tails. Metamorphosis took place in September at 49 mm length (Fleck, 2003, 2010a; Fleck & Schultschik, 2013).

Comments

Tylototriton asperrimus shares some external characters with Echinotriton, such as its pointed ribs which pierce the skin, and its reproductive habits, such as laying large eggs on land. This species was placed in Echinotriton by some authors (Zhao & Hu, 1988a) but molecular work suggests that T. asperrimus is better placed in Tylototriton (Larson et al., 2003; Weisrock et al., 2006; Zhang et al., 2008). The relationships among T. asperrimus, T. wenxianensis, T. hainanensis, T. vietnamensis and T. notialis are unclear due to their high degree of morphological similarity. Molecular work based on mitochondrial and nuclear DNA revealed moderate to large genetic divergence among these species, which form a monophyletic group (Weisrock et al., 2006; Stuart et al., 2010).

References

Bain & Nguyen (2004); Böhme et al. (2005); Fei et al.

(1984, 2005, 2006); Fleck (2003, 2010a); Fleck & Schultschik (2013); IUCN (2013); Larson et al. (2003); Nishikawa et al. (2013a); Schöttler (2003); Stuart et al. (2010); Weisrock et al. (2006); Xie (1999); Ye et al. (1993); Zhang et al. (2008); Zhao (1998); Zhao & Hu (1988a).

Tylototriton broadoridgus Shen, Jiang & Mo, 2012 | Sangzhi Knobby Newt Description and diagnosis

A medium-sized Tylototriton. This species is very similar to Tylototriton wenxianensis, but differs from it in the following characteristics: comparatively broad dorsal ridge, its width almost equal to the diameter of the

eye. The tail is higher than wide at the tail-base. Males do not have papillae on the inner surface of the cloaca. Warts on body sides are rough and protruding, with thin, transverse striae between them.

Tylototriton broadoridgus, captive specimen in Chengdu. Photo: Max Sparreboom. 359

Total length 110-140 mm for males, 139-163 for females (Shen et al., 2012).

Eggs and larvae

Larvae of ca. 34 mm total length were collected in June (1986) and estimated to be 1-1.5 months old. External gills are fully developed and lateral lines begin to appear when larvae reach ca. 58 mm. The body is black, except for the orange ventral fin and digit tips. At 62 mm long the gills begin to atrophy, the dorsal ridge becomes more prominent and metamorphosis sets in. Most larvae complete metamorphosis before the winter although some individuals overwinter at the bottom of the pond (Shen et al., 2012).

Distribution

This species occurs in the Tianping Mountains in Shangzhi County of Hunan Province, China.

Habitat

Tylototriton broadoridgus inhabits a mountainous area at an elevation of 1,000-1,600 m in bamboo groves or areas covered with thick, dry branches and fallen leaves. The species is mainly terrestrial, but enters pools in the breeding season, especially ponds with murky water and a thick layer of humus at the bottom.

Behaviour

Little is known of this species’ natural history and behaviour. The breeding season starts in early May, with males entering the ponds first. After the breeding season, the animals generally leave the pond, but some males can be found active on the pond bottom as late as July.

Threats and conservation

There are no data with

which to assess its status.

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Before 2012 this species was identified as Tylototriton asperrimus or T. wenxianensis. Mitochondrial DNA sequence data show that T. broadoridgus is sister to a clade containing T. wenxianensis and T. dabienicus and make up one lineage within the T. asperrimus group (Shen et al., 2012). For photos of adults and larvae and a distribution map, see Fei et al. (2012).

Tylototriton broadoridgus, habitat, Tianping Mt., border Hunan, Hubei. Photo: Max Sparreboom.

References

Fei et al. (2012); Shen et al. (2012).

Tylototriton dabienicus Shen, Wang & Tao, 2010 | Dabie Knobby Newt Description and diagnosis

A medium-sized Tylototriton. This species is very similar to Tylototriton wenxianensis, of which it was earlier considered to be a subspecies. Tylototriton dabienicus can be distinguished from all the other black species of the T. asperrimus group by a combination of the following

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characteristics: head much longer than wide; limbs short; tips of fingers and toes do not touch when fore- and hindlimbs are adpressed; tips of fingers reach the orbital region when forelimbs are stretched forward; the cloacal lips are coloured orange (Chen et al., 2010).

Total length normally 135-156 mm for females (Chen et al., 2010).

Eggs and larvae

Threats and conservation

There are no data with

which to assess its status. Eggs are laid as a clutch on land.

Distribution

This species occurs in the Dabie Mountains. It has been described from the Huangbaishan National Forest Park of Henan Province, China.

Habitat

Tylototriton dabienicus lives in a forested, mountainous area at an elevation of 698-767 m.

Behaviour

Little is known of this species’ natural history and behaviour.

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Before 2012 this species was considered a subspecies of T. wenxianensis. Mitochondrial DNA sequence data show that T. broadoridgus is sister to a clade containing T. wenxianensis and T. dabienicus and make up one lineage within the T. asperrimus group (Shen et al., 2012). For photos of adults, eggs, larvae, habitat and a distribution map, see Fei et al. (2012).

References

Chen et al. (2010); Fei et al. (2012); Shen et al. (2012).

Tylototriton daweishanensis Zhao, Rao, Liu, Li & Yuan, 2012 | Dawei

Knobby Newt

Description and diagnosis

A medium-sized Tylototriton. This species belongs to the Tylototriton verrucosus group and is most closely related to T. shanjing. The interspecific genetic distance between T. shanjing and this species is considered high enough to warrant its description at the species level (Zhao et al., 2012). It can be distinguished from its congeners by forelimbs that are longer than hindlimbs, brown-black overall colouration, and the orange colour of undersides of fingers and toes, cloacal region and underside of the tail. Total length normally 133-136 mm, type specimen measuring 152 mm (Zhao et al., 2012).

Distribution

This species has been described from Dawei Mountain, Pingbian County, Yunnan. There is no information on this species’ natural history.

Comments

The original description contains a small photo of the preserved type specimen. The diagnosis presented here was based on the short English summary of the type description and the pictured type specimen. Mitochondrial DNA sequence data suggest that Tylototriton daweishanensis is sister to T. shanjing (Zhao et al., 2012).

References

Zhao et al. (2012).

Tylototriton hainanensis Fei, Ye & Yang, 1984 | Hainan Knobby Newt Description

A medium-sized Tylototriton. Slightly larger than Tylototriton asperrimus and T. wenxianensis. Head flat and

wider than long, with weakly developed bony ridges. Rounded snout. Gular fold present. Body slender and flattened. Dorsal ridge distinct but low and segmented; 14-16 large dorso-lateral warts prominent with clear boundaries. Skin rough, with fine granules. Small transverse wrinkles on venter. Tail compressed laterally and ending in a pointed tip. Tail shorter than snoutvent length. Colour entirely black or brownish-black. Tips of digits, cloacal region and lower margin of tail orange-red. Some specimens have orange-tinted dorso-lateral warts (Fei et al., 1984; Fei et al., 2005).

Tylototriton hainanensis, Hainan. Photo: Bosco Chan, courtesy KCC.

Total length 137-148 mm for males, 125-140 for females (Fei et al., 1984; Ye et al., 1993). 361

Diagnosis

A medium-sized, black Tylototriton, similar to but a little larger than Tylototriton asperrimus. Skull much broader than in T. asperrimus and limbs rather short. When a forelimb is stretched forward, finger tips only reach the eye, whereas they reach the nostril in T. asperrimus and T. wenxianensis (Fei et al., 1984). Snout more rounded and head wider than in T. vietnamensis (Böhme et al., 2005).

Distribution

This species is known from Wuzhishan, Diaoluoshan and Jianfengling in Hainan, China, from altitudes between 770-950 m (IUCN, 2013).

Habitat

Tylototriton hainanensis lives under dead leaves or in root holes in heavily shaded forest in the mountains (Fei et al., 1984).

Behaviour

No direct observations available.

Threats and conservation

This species is threatened by habitat loss and degradation due to agriculture, clear-cutting and infrastructure development for tourism. The species is not common. In Jianfengling National Nature Reserve, population density is estimated as ca. 30 individuals per km 2 (Wang et al., 2008). It is listed as Endangered (IUCN, 2013).

Observations in captivity

There are no recorded obser-

vations in captivity (Fleck, 2013b).

Comments Tylototriton hainanensis, young larva. Photo: Christen Wen.

Eggs and larvae

Eggs are laid in clutches on land, under dead leaves, in April-May. A clutch contains 58-90 eggs (Fei et al., 1984; Xie, 1999).

Molecular phylogeny derived from mitochondrial DNA sequence data recognised Tylototriton hainanensis as the likely sister species to T. notialis from Laos (Stuart et al., 2010).

References

Böhme et al. (2005); Fei et al. (1984, 2005); Fleck (2013b);

IUCN (2013); Stuart et al. (2010); Wang et al. (2008); Xie (1999); Ye et al. (1993).

Tylototriton kweichowensis Fang & Chang, 1932 | Guizhou Crocodile Newt Description

A large, robust salamander. Head oval, with distinct bony ridges along the sides. Nostrils close to the tip of the broad and rounded snout. Prominent glandular vertebral ridge. Dorso-lateral ridges less prominent than in Tylototriton

shanjing. Fingers and toes not webbed. Skin of body and tail granular. Paratoids large and distinct. Gular fold prominent. Limbs are strong and moderately long, the tip of the longest finger reaching beyond the nostril to the tip of the snout.

Tylototriton kweichowensis, Shuicheng County, Guizhou. Photo: Hou Mian. 362

Salamanders of the Old World | Tylototriton

When limbs are adpressed, palm and sole overlap (Liu, 1950). Tail compressed laterally, with well-developed fin fold, a little shorter than snout-vent length. Dorso-lateral warts not round and widely separated as in T. shanjing, but square, indistinct and almost fused (Thorn & Raffaëlli, 2001; Nussbaum et al., 1995). Colour black, with bright orange pigment on the temporal region of the head. Three broad longitudinal orange stripes on the back. Tail and tips of digits orange-yellow. Sexual dimorphism is poorly developed. The cloaca of the male is characterised by a small longitudinal slit, that of the female by a small rounded opening. Total length 155-195 mm in males, 177-210 mm in females (Fei et al., 2006).

Diagnosis

A large, robust salamander with orange pigment on the head, except the snout, and on vertebral ridge, dorsolateral body and tail warts, on an otherwise dark brown ground colour. Tail and digits orange. Dorso-lateral warts not round and widely separated as in Tylototriton shanjing, but square, almost fused or only separated by narrow grooves (Nussbaum et al., 1995).

Eggs and larvae

Eggs are laid singly, or two to three at a time, and disperse on the bottom of the pond. Some are laid on land, on moist soil, or under large stones near the pond. The entire clutch is laid within 1-3 days after insemination of the female. Clutch size averages 121 (Tian et al., 1995) or 141 on (Tian et al., 1997) and is positively correlated to snout-vent length of the female. Egg diameter is 2.3-3.4 mm, diameter of egg including gelatinous envelope is 6.2-6.5 mm. Larvae hatch after 21 days at water temperatures of 16-22°C. Hatching rate is higher in June than in May, and is related to rainfall and air temperature. Larvae hatch at 12 mm length, with remains of

yolk still present. Metamorphosis takes place after 105 days at a total length of ca. 62 mm. The orange colour of mid-dorsal stripe and tail appears and the juveniles move onto land (Tian et al., 1997).

Distribution

This species is recorded from Bijie, Dafang, Hezhang, Nayong, Shuicheng, Weining, and Zhijin in western Guizhou and from Yiliang and Yongshan in northeastern Yunnan, China (Zhao, 1998).

Habitat

This species inhabits small ponds, slow-flowing streams and their surroundings in mountainous regions of 1,800-2,300 m altitude. The preferred terrestrial habitat is moist, shady grassy slopes, with many hiding places. Tylototriton kweichowensis prefers to reproduce in ponds with algae and aquatic plants, and a water depth of less than one metre (Tian et al., 1997; Zhao, 1998).

Behaviour

Tylototriton kweichowensis lives mainly on land outside the breeding season. It forages both on land and in water. Prey includes insects (mostly beetles), centipedes, shrimps, snails, earthworms and frogs. This newt is most active in the morning and at night (Gu & Shang, 1994). The reproductive season is from early May-early July, which coincides with the rainy season. The sex ratio in the breeding ponds varies by month, with males usually outnumbering the females, especially in June and July (Hu et al., 1996; Tian et al., 1997). An incomplete courtship sequence was observed by Tian et al. (1997) and included ventral amplexus. The male grasped the female from below, hooking his fore legs around the fore legs of the female. During amplexus, the couple moved about using movements of the tail and the fore legs of the female and hind legs of the male. Amplexus could last 1-2 days. The male was seen bending his tail, a trembling movement passing along the distal one third of his tail, after which he deposited a spermatophore on the floor before the pair separated. The female did not pick up the spermatophore during amplexus (Tian et al., 1997). There are also reports of courtship consisting of a pair slowly turning around in circles, face to face, the male fanning his tail. During this rotating movement, the male deposited several spermatophores. The female was led over the spermatophores and picked one up in her cloaca. Ventral amplexus was not observed (Fleck, 1992).

Threats and conservation

Tylototriton kweichowensis. Photo: Sergé Bogaerts.

This species is threatened by habitat destruction and degradation caused by brick factories and mining. It is also collected for use in traditional Chinese medicine and the pet trade. It is listed as Vulnerable (Zhao, 1998; IUCN, 2013). 363

Observations in captivity

The reproductive behaviour patterns of this species were observed in captive animals (Tian et al., 1997; Fleck, 1992). Tylototriton kweichowensis has regularly been bred in captivity. When kept in tanks it prefers dry spots, but with sufficiently high air humidity. Individuals have lived and reproduced in captivity for 24 years (Fleck, 1992, 2013c).

Comments

Tylototriton kweichowensis forms a well-supported clade with T. shanjing and T. verrucosus in mitochondrial phy-

logeny (Weisrock et al., 2006; Pyron & Wiens, 2011). Phylogenetic analysis of twelve populations of T. kweichowensis from across its range, showed that there was very little geographic structure among populations (Xiao et al., 2010; Zhang et al., 2013).

References

Fei et al. (2006); Fleck (1992, 2013c); Gu & Shang (1994);

Hu et al. (1996); IUCN (2013); Liu (1950); Nussbaum et al. (1995); Pyron & Wiens (2011); Thorn & Raffaëlli (2001); Tian et al. (1995, 1997); Weisrock et al. (2006); Xiao et al. (2010); Zhang et al. (2013); Zhao (1998).

Tylototriton lizhenchangi Hou, Zhang, Jiang, Li & Lü 2012 | Mangshan

Crocodile Newt

Description and diagnosis

This description is summarised from an unpublished English manuscript, made available for this purpose by Hou Mian.

Tylototriton lizhenchangi, female, Yizhang, Hunan. Photo: Hou Mian.

A large, robust salamander, similar to Tylototriton asperrimus but larger. Head longer than wide. 16-17 rib nodules on each side of the trunk, forming a sharp-edged, distinctly raised dorsolateral ridge. Tail a little longer than snout-vent length. Skin finely granulated. Forelimbs, when stretched forward, reach the tip of the snout or slightly beyond. Colour of the entire body black. Only the tips of fingers and toes, the cloacal region and underside of the tail are red. In the male the hind parts of the paratoids are also red. Total length 146-173 mm for males, 150-157 mm for females (Fei et al., 2012). 364

Salamanders of the Old World | Tylototriton

Tylototriton lizhenchangi, adult in breeding habitat, Yizhang, Hunan. Photo: Hou Mian.

Eggs and larvae

No published information available.

Distribution

This species is known from Yizhang, in the southern part of Hunan Province, possibly also in Ruyuan, Guangdong Province, China.

Threats and conservation

This species is used as a drug in Chinese traditional medicine and thousands are exported via the illegal pet trade under the name T. asperrimus. Researchers have observed a rapid decline and consider the species Endangered (Hou Mian, pers. comm.).

Habitat

Observations in captivity

Behaviour

Comments

This species inhabits forested, karstic highlands at elevations between 952-1,200 m. In the breeding season it is found in puddles, ponds or quiet streams. Tylototriton lizhenchangi forages in water and on land, and feeds on small water insects (Caridina) and molluscs. The reproductive season is from May-June. Animals congregate in small pools, streams and marshes to mate and lay eggs.

This species has probably been kept in captivity as T. asperrimus. Published reports are not available.

Phylogenetic analysis of mitochondrial DNA sequences and morphological features confirm this species’ placement in the T. asperrimus species group. Photos of adults, habitat and a range map are shown in Fei et al. (2012).

References

Fei et al. (2012); Hou et al. (2012).

Tylototriton notialis Stuart, Phimmachak, Sivongxay & Robichaud, 2010 |

Laos Knobby Newt

Description

The following is a summary of the original description by Stuart et al., (2010). A moderately stout salamander. Head broader than body, longer than wide, slightly sloping in profile. Snout short, truncate in dorsal view, rounded in profile, projecting beyond lower jaw. Nostrils close to snout tip. Vomeropalatine teeth in two rows, anteriorly in contact and beginning posterior to the anterior margin of the choanae, converging into two parallel rows briefly, before diverging from one another. Glandular ridge on midline of crown from above anterior edge of eye to middle of head. Glandular ridge on outer margin of crown from above eye to base of paratoid. Paratoids enlarged, projecting backward.

Glandular patch on skin of nape. Distinct vertebral tubercular ridge from posterior end of crown to base of tail, separated from ridge on midline of crown. Dorso-lateral row of approximately 14 large glandular warts (rib nodules) on each side from level of axilla to base of tail, distinctly knob-like anteriorly, becoming smaller posteriorly, merging at level of groin. Smaller, glandular warts on most of remaining dorsal and ventral surfaces, warts on crown, nape, and back with clusters of sometimes conical glands; those on throat granular and widely spaced, those on belly arranged in striations perpendicular to body axis, with a smooth, glandular, ovoid patch of skin on chest. Gular fold weak. Four fingers, five toes, all without webbing. Tail a little shorter than snout-vent length, laterally compressed, with narrow dorsal fin, smooth ventral ridge, tip acuminate in profile. Colour of dorsal and ventral surfaces dark brown. Margin of upper and lower lip, posterior end of paratoid, rib nodules, dorsal

Tylototriton notialis, paratype, Boualapha District, Khammouan Prov., Laos. Photo: Brian Stuart.

margin of tail, outer margin of upper surface of hand and finger tips, lower surface of hand, except centre of palm, dorsal surface of toe-tips, ventral surface of toes and extending from fifth toe to base of foot, cloacal region continuing to ventral ridge of tail, all bright orange. Anterior surface of forelimb from axilla to base of first finger with narrow, broken, yellow stripe. Anterior and ventral surfaces of hindlimbs with small, scattered yellow spots. Iris dark brown, pupil black. Animals on land are almost black, and darker than animals caught in water. Total length 10-14 cm. 365

some T. notialis from Vietnam lack this colour (Nishikawa et al., 2013a; pers. obs.).

Eggs and larvae

Eggs have not yet been described. Two size classes of larvae were collected in May, living in syntopy with the holotype. One specimen was 33.1 mm length, and larvae in the other group measured 17.9-20.9 mm.

Distribution Tylototriton notialis, holotype, Boualapha District, Khammouan Prov., Laos. Photo: Brian Stuart.

The species is currently known from only a few localities. The type locality is Nakai-Nam Theun National Protected Area, Boualapha District, Khammouan Province, Laos. It has also been reported from Nghe An, Vietnam (Nishikawa et al., 2013a).

Habitat

Tylototriton notialis inhabits a mixed evergreen, deciduous, and pine forest at approximately 1,000 m altitude. The holotype and larvae were found in a 3 m wide stream with a slow current and sand and bedrock substrate, including leaf litter-filled potholes, just upstream from a 3 m high chute over bedrock. Water temperature was 19.5°C. Two paratypes were found on land.

Behaviour

These animals apparently enter the stream to reproduce. No other data are available.

Tylototriton notialis, holotype, ventral side, Boualapha District, Khammouan Prov., Laos. Photo: Brian Stuart.

Diagnosis

A Tylototriton with a broad, flattened head and truncated snout. It has a combination of distinct, knob-like rib nodules; glandular warts on most of remaining dorsal and ventral surfaces; very dark brown to black colouration on dorsum and venter and bright orange colouration on rib nodules. The bright orange colouration on the posterior end of paratoids (Stuart et al., 2010) cannot be used as a diagnostic characteristic for Tylototriton notialis, since various other species in the T. asperrimus group also show this colouration, and

Threats and conservation

No information available to

date.

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Tylototriton notialis is distinctive both genetically and morphologically compared with other members of the T. asperrimus group. It is nested in a clade containing T. hainanensis from Hainan and Tylototriton species from Cao Bang, Vietnam (Stuart et al., 2010).

References

Nishikawa et al. (2013a); Stuart et al. (2010).

Tylototriton panhai Nishikawa, Khonsue, Pomchote & Matsui, 2013 |

Panha’s Knobby Newt

Description and diagnosis

This is based on the original description by Nishikawa et al. (2013c). A medium-sized Tylototriton with rough, granulated skin, knob-like warts in dorso-lateral rows and prominent, wide dorso-lateral bony ridges on the head. Small but distinct paratoids; gular fold present. 14 trunk vertebrae. The vertebral ridge is distinct and not segmented. Rib nodules prominent and large, limbs long and thin, tips of fore- and hindlimbs

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overlapping when limbs are adpressed. Tail thin and laterally compressed. Dorsal side of the head, upper and lower lips, paratoids, vertebral ridge, rib nodules, tips of fingers and toes, margin of vent slit, and dorsal and ventral edges of tail are yellow, orange, to reddish-brown.

dark brown and the remaining area dark cream in colour. Clutch size is unknown.

Distribution

This species is known from Phu Hin Rong Kla National Park, Phitsanulok Province, and Phu Luang Wildlife Sanctuary and Phu Suan Sai National Park, Loei Province, Thailand.

Habitat

Tylototriton panhai is found in moist forest with bamboo bushes and a variety of water bodies, such as rain puddles and streams.

Behaviour

Adults are found in water during the breeding season, from May- July.

Threats and conservation

No published data available.

Observations in captivity

There are no reports of this

species being kept in captivity.

Comments

Tylototriton panhai, Phu Luang, Thailand. Photo: Porrawee Pomchote.

Tylototriton panhai is similar to T. shanjing, T. pseudoverrucosus and T. uyenoi but differs from them in having well-developed, broad bony ridges on the head, and black limbs and tail, except for the ridges. Total length 135 mm (holotype).

Eggs and larvae

Eggs are found attached to wet grass and plants overhanging the water or under wood debris on land near small streams and ponds. Mean diameter of ripe ova found in an ovary of the holotype was 1.5-2.7 mm. The animal pole was

Several geographically separated colour variants of Tylototriton have been recorded from Thailand (Wongratana, 1984; Chan-Ard et al., 1999; Chuaynkern et al., 2008; Pomchote et al., 2008), giving rise to the expectation that these forms constitute different taxa. On the basis of molecular data, Nishikawa et al. (2013c) discerned three groups of Tylototriton, considered to belong to T. shanjing, as undescribed species. Two of these were described as T. uyenoi resp. T. panhai. These species match the observed morphological differences. One group from Doi Lahnga, Chang Rai Province, awaits description. See also comments under T. verrucosus and T. shanjing.

References

Chan-Ard et al. (1999); Chuaynkern et al. (2008);

Nishikawa et al. (2013c); Pomchote et al. (2008); Wongratana (1984).

Tylototriton pseudoverrucosus Hou, Gu, Zhang, Zeng, Li & Lü, 2012 |

Southern Sichuan or Chuannan Knobby Newt

Description and diagnosis

This description is summarised from an unpublished English manuscript, made available for this purpose by Hou Mian.

A large, slender salamander. Head longer than wide. Crown smooth, without ridges. 15-16 roundish rib nodules on each side of the trunk, well separated, forming distinctly raised dorsolateral ridges. Tail much longer than snout-vent length. Skin finely granulated. Limbs thin and long. Ground colour of dorsum dark brown to black. Ventral side,

vertebral tubercular ridge, dorso-lateral glands, paratoids, fingers and toes, cloaca and tail are brownish-red. Maximum total length 187 mm for males, 200 mm for females (Hou et al., 2012).

Eggs and larvae

No description available.

Distribution

This species is known from Ningnan County, in the southern part of Sichuan, China. 367

Tylototriton pseudoverrucosus, female, Ningnan County, Sichuan. Photo: Hou Mian.

Habitat

This species inhabits high mountains at elevations between 2,300-2,800 m in secondary forest, and also in areas where forests have been cut or burnt. It is found in marsh puddles and pools during the breeding season.

Behaviour

Tylototriton pseudoverrucosus forages in water and on land, and feeds on small water insects and molluscs. The breeding season is in June and July. Animals can then be found by day and night congregating in small pools and marshes to mate and lay eggs.

Threats and conservation

This species’ habitat is impacted by human activities, such as reclamation of land for agriculture and hydropower development, as well as by natural disasters. Researchers have observed a

Tylototriton pseudoverrucosus, male, Ningnan County, Sichuan. Photo: Hou Mian.

rapid decline in numbers and consider the species Endangered (Hou Mian, pers. comm.).

Observations in captivity Comments

Phylogenetic analysis of mitochondrial DNA sequences confirm this species’ placement in the Tylototriton verrucosus species group. Its closest relative is T. taliangensis. Photos of adults, habitat and a range map are shown in Fei et al. (2012).

References

Fei et al. (2012); Hou et al. (2012).

Tylototriton pseudoverrucosus, habitat, Ningnan County, Sichuan. Photo: Zhang Ming-Wang. 368

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There are no reports of this

species being kept in captivity.

Tylototriton shanjing Nussbaum, Brodie & Yang, 1995 | Yunnan Newt,

Mandarin Salamander

Description

A large, robust salamander. Head flat and oval, with strongly developed cranial crests and cranial boss. Nostrils close to the tip of the broad and rounded snout. Prominent glandular vertebral ridge. Dorso-lateral row of 15 nodules on each side of body and anterior part of the tail. Fingers and toes not webbed. Skin of body and tail granular. Paratoids large and distinct, slightly concave. Gular fold present. Tail compressed laterally, with well-developed fin fold, a little shorter than snout-vent length. Tylototriton shanjing has ossified structures on the median part of the frontals and differs from T. verrucosus in this and various other skull and vertebrae characters (Haller-Probst, 1998). Colour dark brown on dorsum, with bright orange or yellow pigment on the head, vertebral ridge, and dorso-lateral body and tail warts. Most of the venter, tail and limbs also orangeyellow. Ventral ground colour dark brown with dominant orange-yellow suffusion on chin, throat and belly. Dorso-lateral warts round and widely separated (Nussbaum et al., 1995).

Tylototriton shanjing, captive specimen. Photo: Frank Pasmans.

Sexual dimorphism is poorly developed, and variable among populations (Nussbaum et al., 1995). The cloaca of the male is characterised by a small longitudinal slit, that of the female by a small rounded opening. Total length 136-150 mm for males, 147-170 for females (Fei et al., 2006). In captive animals of unknown provenance, maximum lengths of 20 cm have been recorded.

Diagnosis

A dark brown salamander with orange or yellow pigment on the head, vertebral ridge, and dorso-lateral warts on body and tail. Most of the venter, tail and limbs also orangeyellow (Nussbaum et al., 1995). Strongly developed cranial crests and cranial boss. Skull surface is covered with prominent dorso-lateral bony crests and a median crest on the parietalia. Differs from Tylototriton verrucosus in having a bright orange head, tail and dorso-lateral nodules, and in having ossified structures on the median part of the frontals (Haller-Probst, 1998).

Eggs and larvae

Eggs are deposited singly or in strings on aquatic plants in ponds and measure 2.5-3 mm in diameter (Zhao, 1998). Permanent ponds are generally used for eggdeposition, but eggs may also be laid in clutches on land near the pond edge (Xie, 1999; Li & Li, 2000). Diameter of egg including jelly envelope is 7 mm (Rehberg, 1986). Clutch sizes of 30-100 (Snider, 1998), 122 (Xie, 1999), 291 and 240 eggs (Rehberg, 1986) have been recorded. Larvae hatch after about

Tylototriton shanjing, captive specimens, pet market, Shanghai. Photo: Max Sparreboom.

two weeks, at different stages of development. Larvae with remains of yolk are 13 mm long, and larvae hatching with developed fore legs are a little longer (Rehberg, 1986). The fully grown larva has a tail as long as, or a little shorter than, the head and body, its tip obtusely pointed. Colour olive-brownish, thickly speckled with darker markings. Upper crest of tail not reaching the head. Skin finely or coarsely granular. Light-coloured dorso-lateral lines appear in the maturing larva and the light colour becomes concentrated in a row of light spots during metamorphosis (Ziegler et al., 2008). 369

Tylototriton shanjing, Nam Lieng, Laos (identification uncertain). Photo: Gustavo Espallargas.

Tylototriton shanjing, habitat, Nam Lieng, Laos. Photo: Gustavo Espallargas.

Metamorphosis occurs ca. 10 weeks after hatching, at a total length of 49-58 mm (Rehberg, 1986). Specimens are sexually mature at 3-4 years of age with a snout-vent length of 70-75 mm (Snider, 1998).

in the direction of the female’s snout. Several observers have observed the male depositing a spermatophore during this ‘love-waltz’, choosing a stone or other firm piece of substrate to attach it to. Continuing the rotating movement, the female was led over the spermatophore, which she picked up with her extended cloaca (Sparreboom, 1999). This courtship behaviour can be performed both in water and on land. Ventral amplexus, during which the male hooks his fore legs round the fore legs of the female from below, such as in T. verrucosus and Pleurodeles, has not so far been observed.

Distribution

This species is known from central, western and southern Yunnan, China, where it occurs along the Nu, Lancang and Yuan Rivers, at altitudes of 1,000-2,500 m (Zhao, 1998; IUCN, 2013). Tylototriton shanjing is also known from northeastern Laos, where it has been collected in Phu Pan, Xam Neua (Nishikawa et al., 2013c) and was also observed 140 km further south (Gustavo Espallargas, pers. comm.). The boundary between T. shanjing and T. verrucosus is not clear.

Habitat

Tylototriton shanjing inhabits hill forests and secondary forest and can be found in shady, moist places near rice-fields, ponds and irrigation canals (Zhao, 1998).

Behaviour

The breeding season is from May-August (Zhao, 1998). Reproduction takes place in water, but there are no direct field observations, so possible mating on land cannot be excluded. Courtship behaviour was described in captive animals by Rehberg (1986) and Schultschik et al. (2013). Males and females entered the water during the first week of May, at a water temperature of 23ºC. The couple moved cheek-to-cheek opposite each other, performing a typical roundabout dance without direct bodily contact. Their heads at the centre, the outer sides of their bent tails formed the edge of a circle, in an image resembling a spiral. The male slowly fanned his bent tail

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Threats and conservation

Tylototriton shanjing is common in central, western and southern Yunnan, but less common in the northern part of its range. It is collected for use in traditional Chinese medicine and for the international pet trade. Suitable habitat is reduced or degraded by infrastructure development. The species is listed as Near Threatened (Zhao, 1998; IUCN, 2013).

Observations in captivity

This species is more difficult to keep and breed than Tylototriton verrucosus, with temperature and humidity being the crucial factors (Thorn & Raffaëlli, 2001), but has nonetheless frequently been captive-bred. Tylototriton shanjing is more terrestrial than T. verrucosus (Ziegler et al., 2008; Schultschik et al., 2013).

Comments

The systematics of Tylototriton shanjing and T. verrucosus remain unclear. Frost (2013) follows Zhang et al. (2007) and Yang & Rao (2008) in considering T. shanjing a

subspecies of T. verrucosus. Stuart et al. (2010) found a level of divergence between T. verrucosus and T. shanjing, that was similar to the interspecific differences in the T. asperrimus species group, and consider T. shanjing a valid species. See further comments under T. verrucosus.

References

Fei et al. (2006); Frost (2013); Haller-Probst (1998); IUCN

(2013); Li & Li (2000); Nishikawa et al. (2013c); Nussbaum et al. (1995); Rehberg (1986); Schultschik et al. (2013); Snider (1998); Sparreboom (1999); Stuart et al. (2010); Thorn & Raffaëlli (2001); Yang & Rao (2008); Xie (1999); Zhang et al. (2007); Zhao (1998); Ziegler et al. (2008).

Tylototriton taliangensis Liu, 1950 | Taliang Knobby Newt Description

A long-tailed, robust salamander; the largest species of Tylototriton. Head flat and longer than wide. Cranial ridges less prominent than in other Tylototriton species. Paratoids distinct. Entire head, body and tail covered with small tubercles, rough when living on land and smoother in water, during the breeding season. Dorsal ridge distinct. Dorso-lateral warts indistinct and somewhat rectangular. Forelimb long, the tip of the longest finger reaching beyond the snout. When limbs

are adpressed, digits overlap. Tail compressed laterally, with well-developed fin fold, a little longer than snout-vent length. Colour uniform black, a little lighter on belly. Edges of paratoids red-orange. Cloaca, ventral margin of tail, first part of digits orange. Cloaca in female pointed cone-shaped, in male half coneshaped. On inner side of fore legs the male has an oval, orange spot, which becomes more prominent during the breeding season (Kabisch et al., 1994; Fleck, 1997). Total length 186-220 mm in males, 194-230 mm in females (Fei & Ye, 2001; Fei et al., 2006).

Diagnosis

A slender Tylototriton, entirely black, with edges of paratoids, toe-tips, cloaca and underside of tail red-orange. Dorso-lateral glandular ridges inconspicuous.

Eggs and larvae Tylototriton taliangensis, Jinhua Lake, Liziping, Shimian County, Sichuan. Photo: Max Sparreboom.

Eggs are deposited singly on water plants in water. Diameter 2-2.2 mm. Clutch size 250-280 (Fei & Ye, 2001). The developed larva has a broad head, rounded snout and long gills. Colour brown, mottled with dark markings, extending onto fins. Dorsal tail-fin low, beginning on first quarter of the back. Dorsal and ventral tail-fins running almost parallel; tail-tip blunt and rounded. Larvae overwinter and metamorphose the following year at lengths between 59-72 mm (Kühnel et al., 1999).

Distribution

The species is distributed in Hanyuan, Mianning, Shimian, Meigu, Zhaojue and E’bianand Mabian in south-western Sichuan, China.

Habitat

This species’ habitat consists of densely vegetated forested valleys, where it lives in grass near ponds or in ponds, in the mountains at elevations of 1,390-3,000 m (Fei & Ye, 2001). At the highest elevations the habitat may consist of ponds in grassland plateaus (Kabisch et al., 1994).

Tylototriton taliangensis, in breeding pond, Jinhua Lake, Liziping, Shimian County, Sichuan. Photo: Max Sparreboom.

Behaviour

Breeding season from June-August (Xie, 1999). Adults assemble in the ponds to breed. Courtship behaviour 371

Tylototriton taliangensis, breeding habitat, Jinhua Lake, Liziping, Shimian County, Sichuan. Photo: Max Sparreboom.

was observed in captive animals. First the male makes tailfanning movements in the direction of the female. Then the male moves under the female and grasps her forelimbs with his forelimbs from behind, swimming around with the female on his back. During this amplexus the male may deposit several spermatophores on the floor. While maintaining amplexus, the male moves his hind body sideways from under the female so that she hits a spermatophore with her cloaca and picks it up (Fleck, 1997; Kühnel et al., 1999). Animals in amplexus may also be found on land (Ye et al., 1993).

Threats and conservation

This species is threatened by over-collection for traditional Chinese medicine and the pet trade. It is listed as Near Threatened (Zhao, 1998; IUCN, 2013).

Tylototriton taliangensis, habitat, Pusagang, Sichuan. Photo: Max Sparreboom.

Observations in captivity

Tylototriton taliangensis has been bred in captivity. The best results were obtained by keeping them cool in spring at water temperatures between 10-15°C. A female deposited an entire clutch of 200 eggs within 24 hours when water temperatures were raised to 24-27°C in early June (Fleck, 1997, 2013d; Kühnel et al., 1999).

Comments

Tylototriton taliangensis is the sister species of a clade containing T. shanjing, T. verrucosus and T. kweichowensis (Weisrock et al., 2006; Pyron & Wiens, 2011).

References

Fei et al. (2006); Fei & Ye (2001); Fleck (1997, 2013d); IUCN (2013); Kabisch et al. (1994); Kühnel et al. (1999); Pyron & Wiens (2011); Weisrock et al. (2006); Xie (1999); Ye et al. (1993); Zhao (1998).

Tylototriton uyenoi Nishikawa, Khonsue, Pomchote & Matsui, 2013 |

Uéno’s Knobby Newt

Description and diagnosis

This is based on the original description by Nishikawa et al. (2013c). A medium-sized Tylototriton with rough, granulated skin, knob-like warts in dorso-lateral rows and prominent, narrow dorso-lateral bony ridges on the head. Small but distinct paratoids; gular fold present. 14 trunk vertebrae. The vertebral ridge is distinct and slightly segmented. Rib nodules prominent, limbs long and thin, tips of fore- and hindlimbs overlapping when limbs are adpressed. Tail thin and laterally compressed.

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Dorsal side of the head, upper and lower lips, vertebral ridge, rib nodules, limbs, vent region and entire tail orange to reddish-brown. Males have a relatively longer tail and vent slit than females. Tylototriton uyenoi is similar to T. shanjing, but differs from it in having darker markings, relatively wider head, longer and higher tail, and wider and longer vomerine tooth series.

Head triangular with short and rounded snout. Caudal and dorsal fins nearly absorbed. Tail-tip rounded. Dorsum yellowish-brown; venter paler.

Distribution

This species is known from Doi Ang Khang, Doi Chang Kien, Doi Inthanon, Doi Pui and Doi Suthep, Chang Mai Province, Thailand.

Habitat

Tylototriton uyenoi inhabits natural and artificial ponds, farm ditches, and slow-running streams. Adults may be found in water outside the breeding period.

Behaviour

The breeding season is from May-July.

Threats and conservation

No published data available.

Observations in captivity

There are no reports of this

species being kept in captivity. Tylototriton uyenoi, Doi Inthanon, Chiang Mai. Photo: Porrawee Pomchote.

It differs from T. panhai in having orange to reddish-brown limbs and tail, and narrow dorso-lateral ridges on the head. Total length 156 mm (holotype).

Eggs and larvae

Mean diameter of ripe ova in ovaries of the paratype was 1.9-2.8 mm. The animal pole was dark brown and the remaining area dark cream in colour. Clutch size is unknown. Larvae are found in water bodies from August-December. A fully developed larva of 66 mm was collected in early September.

Comments

Several geographically separated colour variations of Tylototriton have been recorded from Thailand (Wongratana, 1984; Chan-Ard et al., 1999; Chuaynkern et al., 2008; Pomchote et al., 2008), giving rise to the expectation that these forms constitute different taxa. On the basis of molecular data, Nishikawa et al. (2013c) discerned three groups of Tylototriton, until then considered to belong to T. shanjing, and described two of these as T. uyenoi resp. T. panhai. These species match the observed morphological differences. One group from Doi Lahnga, Chang Rai Province, awaits description. See also comments under T. verrucosus and T. shanjing.

References

Chan-Ard et al. (1999); Chuaynkern et al. (2008); Nishikawa et al. (2013c); Pomchote et al. (2008); Wongratana (1984);

Tylototriton verrucosus Anderson, 1871 | Himalayan Salamander, Crocodile Newt

Description

A large, robust salamander. Head flat and oval, with strongly developed cranial crests and cranial boss. Nostrils close to the tip of the broad and rounded snout. Eyes of moderate size with large, granular upper eyelid. Prominent glandular vertebral ridge. Dorso-lateral row of 15 nodules on each side of body and anterior part of the tail. Fingers and toes not webbed. Skin of body and tail granular. Paratoids large and distinct, slightly concave. Gular fold present. Tail compressed laterally, with welldeveloped fin fold, a little shorter than snout-vent length. Colour uniformly dark brown on dorsum, sides and venter. Tail and soles of hands and feet lighter brown than body.

Underside of tail lighter, sometimes yellow or orange. This description applies to animals from Nepal (Anders et al., 1998) and largely conforms to the original description (Anderson, 1871, based on specimens from western Yunnan) and the descriptions of specimens from Taunggyi in Burma (ThantShima et al., 1979) and the Darjeeling area in India (Kuzmin et al., 1994). There is regional variation in the prominence of the vertebral and dorso-lateral ridges. There is also variation in contrast between the cranial ridges, paratoids, and dorso-lateral nodules, coloured in different shades of light brown to yellow, and the dorsum which varies from dark chocolate-brown to black. The light brown to black contrast in the colour of body, 373

T. shanjing from Yunnan, Nishikawa et al. (2013c) synonymise T. v. pulcherrima with T. shanjing. Sexual dimorphism is poorly developed. Females are larger than males; they have a larger head and longer limbs, but smaller cloaca and lower tail (Seglie, 2002; Seglie et al., 2010). The cloaca of the male is characterised by a small longitudinal slit, that of the female by a small rounded opening. In the breeding season the female cloaca is more conical in shape than that of the male (Anders et al., 1998).

Tylototriton verrucosus pulcherrimus, male, Luchun County, Yunnan. Photo: Hou Mian.

Average total length of animals from Darjeeling is 17.5 cm for females and 15.4 cm for males (Seglie, 2002). In captive animals of unknown provenance, lengths of 24 cm have been recorded (Clare, 2004).

Diagnosis

A dark brown salamander with vertebral ridge and dorso-lateral rows of warts. Strongly developed cranial crests and cranial boss. Skull surface is covered with prominent dorso-lateral bony crests and a median crest on the parietalia. Differs from Tylototriton shanjing genetically (Stuart et al., 2010), in lacking the bright orange head and dorso-lateral nodules, and in having no ossified structures on the median part of the frontals (Haller-Probst, 1998).

Eggs and larvae

Tylototriton verrucosus, eggs. Photo: Max Sparreboom.

head, limbs and tail is more pronounced in terrestrial than in aquatic individuals. One subspecies has been described under the name Tylototriton verrucosus pulcherrima Hou, Zhang, Li & Lu, 2012. (The authors probably intended to name it pulcherrimus, masc.) This form occurs in the Huanglian Mountains and is characterised by having a row of 16 distinct dorso-lateral knobs. These knobs are relatively uniform in size, not enlarged on the middle of the trunk. Red ground colour, paratoids yellow-orange. Its range is separated from that of the nominate T. verrucosus and extends from Yunnan Province to north-western Vietnam, presumably also in north-eastern Laos (Hou et al., 2012; Hou Mian, pers. comm.). This newt occurs in thick vegetation in warm and humid habitats in rain forests at 1,450-1,550 m altitude. The newts assemble in puddles and pools, where they mate and lay eggs from May-June. Based on small genetic differences with 374

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Eggs are laid onto submerged vegetation and directly onto the bottom of a pond, or rarely on land. Records of clutch size vary from 26-60 (Kuzmin, 1999) to 30-400 eggs (Thant-Shima et al., 1979). When the gelatinous envelope is fully distended, the egg measures between 6-10 mm in diameter (Smith, 1924), and the embryo 2 mm (Sparreboom, 1999). Larvae hatch after 7-20 days, ca. 11 mm long. The fully grown larva has a tail as long as, or a little shorter than snoutvent length, its tip obtusely pointed. Upper crest of tail not reaching the head. Skin finely or coarsely granular. The prominent ridges on the sides of the head, characteristic of the adult, are just apparent. Knob-like projections on flanks visible as elongated vertical folds of skin. Colour olive-brownish, thickly speckled with darker markings. Metamorphosis takes place between summer and autumn at a total length between 37-75 mm (Smith, 1924; Schleich & Kästle, 2002). Larvae of late clutches are known to overwinter. The age of sexual maturation is around 3-5 years, and maximum recorded longevity is 11 years (Kuzmin et al., 1994; Kuzmin, 1999; Seglie et al., 2010).

Distribution

This species occurs from India (West Bengal, and smaller, isolated populations in Manipur and Arunachal Pradesh), Sikkim, Bhutan and eastern Nepal through the Kachin and Shan Hills of Myanmar to south-western Yunnan (Longchuan County and its vicinity), China, and in scattered mountains in northern Thailand. It has recently been recorded

from Lai Chau and Lao Cai Provinces in Vietnam. The boundary between this species and Tylototriton shanjing is not clear (Yang & Rao, 2008; Wanglial & Gurung, 2012; IUCN, 2013).

Habitat

Tylototriton verrucosus, larva. Photo: Max Sparreboom.

The terrestrial habitat is largely moist forest, or sites where mountain forests previously existed, such as rice fields, tea plantations, meadows covering the shores of mountain ponds and lakes, forest edges, etc. The animals generally remain close to water (Kuzmin, 1999). Aquatic habitats include various freshwaters including permanent pools and forest streams, natural and artificial ponds, rain puddles and swamps (Seglie, 2002). Breeding occurs in the shallow areas of these water bodies. In the southern part of its range it is generally an upland species occurring at elevations between 1,000-3,000 m. In the northern part of its range T. verrucosus is reported from low hills below 1,000 m (IUCN, 2013).

Behaviour

Although the species is not usually common, population density in the breeding waters may locally be very high, from 71-101 per 100 m 2 (Seglie, 2002). It feeds on aquatic and terrestrial insects, bivalves, cannibalised eggs of Tylototriton verrucosus and plant material (Anders et al., 1998). Young larvae feed on mosquito larvae, microcrustaceans, chironomids and various other benthic prey. Later stage larvae prey on aquatic insects and small crabs and after metamorphosis the diet consists of small bivalves and terrestrial food such as Collembola, larval Lepidoptera, larval Diptera and isopods. The adult diet consists of Lumbricidae, larval Diptera, Coleoptera, Lepidoptera, and Odonata, adult dytiscid beetles, larvae of frogs and cannibalised eggs (Dasgupta, 1996).

Tylototriton verrucosus, larva. Photo: Max Sparreboom. Reproduction starts soon after the adult emerges from hibernation. Over a large part of its range, reproduction coincides with the start of the monsoon season (late March-early April). Males enter the breeding pond first and may stay longer than females, resulting in seasonal fluctuations in sex ratio. Spawning occurs from March-May (in May in the Darjeeling district, Seglie et al., 2010), and may continue throughout the rainy season (as late as September). Females leave the water soon after laying eggs (Seglie, 2002). Most adults have left the water by October (AmphibiaWeb, 2013; Kuzmin, 1999).

Tylototriton verrucosus, giant larva, captive bred. Photo: Max Sparreboom.

Courtship behaviour was first observed in specimens from upper Burma (Boulenger, 1920). Boulenger observed that the male clasped the female from below, with his forelimbs hooked over the fore legs of the female, similar to Pleurodeles waltl. Several fragmentary descriptions are given in the literature. The following account is based on observation of one pair of T. verrucosus from Burma (Myanmar), placed in an aquarium by Thant-Shima et al. (1979). The aquarium was filled with fresh water at 24-25°C. After 1-2 days the male grasped the female 375

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Tylototriton verrucosus, courtship in a captive pair of unknown provenance. The male performs tail-fanning in the direction of the female’s snout. The pair slowly moves around, pivoting around their forelimbs, their heads held cheek to cheek. Ventral amplexus was not observed in this courtship sequence. Photos: Max Sparreboom.

from below, hooking his forelimbs around her fore legs as described by Thorn (1969) and swam around with her in the tank. After 6-12 hours, the pair moved to the bottom and started making a rotating movement around each other, their heads turned towards each other. This lasted for a few hours or the whole night. During this performance, the cloaca of both sexes was wide open. The male deposited several spermatophores onto pebbles by rubbing over them with his cloaca. The spermatophores were conical in shape and transparent, apart from the white part on the top, from which microscopically small sperm were seen diffusing into the water. 376

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Apparently the female caught the sperms in her cloaca by rubbing her cloaca over them during the rotating movement. Several hours later, the female started to lay eggs.

Threats and conservation

Habitat loss from infrastructure development and regular human-induced forest fires (in South-East Asia) pose threats to this species. Water pollution from agrochemicals and domestic detergents, and the extraction of water for irrigation also degrade its habitat. The species is considered a bad omen and is therefore killed in certain areas in Myanmar (Gyi, 1969). It is used as bait for fishing in Myanmar

and is in demand for the domestic and international pet trade. It is also harvested for use as a traditional medicine in India (IUCN, 2013). In the Darjeeling District the principal problem is the high rate of habitat loss due to human activities, draining of ponds, and the introduction of fish (Seglie, 2002; Seglie et al., 2003). The species or its habitat is protected by legislation in Nepal, India, China and Thailand. Initiatives for conservation have been taken in India and Thailand (Humphrey & Bain, 1990; Seglie, 2002). The species is listed as of Least Concern (IUCN, 2013).

Observations in captivity

Tylototriton verrucosus has been studied in captivity since the beginning of the 20th century and much of our knowledge of its reproductive behaviour stems from observations of captive animals. It can be easily bred in aquariums with clean water (20-27°C) and plant cover and will then often lead a mainly aquatic life (Mudrack, 1972; Sparreboom, 1999; Novarini, 2000; Clare, 2004). Most animals imported via the pet trade are of unknown provenance. They vary in size, colour pattern and behaviour, making it difficult to attribute observations of reproductive activity made in aquariums. Observations made before 1995, when T. shanjing was described (Nussbaum et al., 1995), may in fact refer to that species (such as in Rehberg, 1986).

Comments

There are various, partly contradictory, accounts of this species’ reproductive behaviour. There are references to: direct apposition of the cloacas of male and female (Mudrack, 1972); spermatophore transfer during amplexus and mating partly on land similar to Salamandra (Dasgupta, 1994); floating sperm sacs sucked up by the female with her cloaca (Roy & Mushahidunnabi, 2001); egg guarding by the female (Dasgupta, 1984); partial external fertilisation of eggs squeezed out of the female during amplexus; and juvenile newts climbing onto their mother’s back to enjoy maternal care (Shrestha, 2001). Most of these descriptions are incomplete, inaccurate or fictitious. There is a challenge for further study. For a good summary of our knowledge of T. verrucosus see Schleich & Kästle (2002).

Tylototriton verrucosus, illustration of the type description by Anderson, 1871.

When Anderson (1871) published the description of T. verrucosus, he described the species as a uniformly blackish-brown newt. He did not designate a type series. Only later did he designate 16 syntypes, of which 12 have since been located (Chanda et al., 2000). One of these is in the British Museum of Natural History. These syntypes had been collected from a broad area in Yunnan and did not match the black colouration of the original description, but showed a vivid orange colour pattern (Fei et al., 2012). Nussbaum et al. (1995) recognised the orange colour morph as a new species, T. shanjing, based on colouration and morphometric analyses. They designated a neotype from Longchuan, Yunnan, for T. verrucosus, which now represents the brown colour morph. But given the existence of the syntypes, the neotype may loose validity. Consequently, a nomenclatural problem with the description of T. verrucosus may arise in future. First a lectotype will have to be described on the basis of the syntypes. Depending on the colour patterns and body measures of the syntypes, the new holotype arising may well have the characteristics of what is now T. shanjing, resulting eventually in the name shanjing becoming a synonym of verrucosus.

References

AmphibiaWeb (2013); Anders et al. (1998); Anderson

(1871); Boulenger (1920); Chanda et al. (2000); Clare (2004); Dasgupta

Authors disagree as to whether T. verrucosus and T. shanjing represent two colour morphs of the same species or two separate species (Zhang et al., 2007; Frost, 2013). Stuart et al. (2010) found a relatively large mitochondrial DNA divergence between them, supporting the view that they are separate species (cf. Pyron &Wiens, 2011).

(1984, 1994, 1996); Fei et al. (2012); Frost (2013); Gyi (1969); Haller-Probst (1998); Hou et al. (2012); Humphrey & Bain (1990); IUCN (2013); Kuzmin (1999); Kuzmin et al. (1994); Mudrack (1972); Nishikawa et al. (2013c); Novarini (2000); Nussbaum et al. (1995); Pyron & Wiens (2011); Rehberg (1986); Roy & Mushahidunnabi (2001); Schleich & Kästle (2002); Seglie (2002); Seglie et al. (2003, 2010); Shrestha (2001); Smith (1924); Sparreboom (1999); Stuart et al. (2010); Thant-Shima et al. (1979); Thorn (1969); Wangyal & Gurung (2012); Zhang et al. (2007)

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Tylototriton vietnamensis Böhme, Schöttler, Nguyen & Köhler, 2005 |

Vietnamese Knobby Newt, Vietnamese Crocodile Newt

Description

A small-sized Tylototriton. Head broader than body and slightly sloping in profile. Snout short, truncate in dorsal view, rounded in profile and protruding beyond lower jaw. Nostrils close to snout tip. Upper lips thick, fleshy and overlapping lower lip under eye region. A low vertebral tubercular ridge, extending from top of head to base of tail. Two lateral rows of larger warts, extending from insertion of forelimbs to base of tail. Glands and warts relatively small,

covering most of dorsal surfaces; venter almost smooth. Paratoids greatly enlarged, slightly projecting backwards. Gular fold absent. Fingers without webbing, toes with basal webbing. Tail laterally compressed; dorsal and ventral tail-fin moderately developed; tail-tip acuminate in profile. Tail longer than snout-vent length (Böhme et al., 2005). Colour of dorsal and ventral surfaces greyish-brown in animals caught in water; animals caught on land are much darker. Finger and toe-tips orange-yellow. Tail brownish-tan with ventral tail-fin orange-yellow. Cloacal region bordered with orange-yellow (Böhme et al., 2005). Total length 122 mm for males; with a maximum snout-vent length of 84 mm, females are larger than males, which have a snout-vent length of 75 mm (Bernardes et al., 2011).

Diagnosis

Tylototriton vietnamensis, Mau Son, Vietnam. Photo: Max Sparreboom.

A small-sized Tylototriton, with broad, flattened head and truncated snout. Paratoids large, elongated; dorsal skin covered with small warts and glands; three tubercular dorsal ridges; slightly flattened rib nodules. Colour of animals in water greyish-tan or brownish. In external characters most similar to Tylototriton asperrimus, T. hainanensis and T. wenxianensis, but different from T. wenxianensis in lighter body colouration, truncated rather than rounded snout and more prominent dorso-lateral ridges. It differs from T. asperrimus in having lighter dorsal colour, less prominent rib nodules, truncated rather than rounded snout, and less prominent bony ridges on head. It differs from T. hainanensis in its smaller size, head-shape not wider than long, and snout truncated rather than rounded (Böhme et al., 2005).

Eggs and larvae

Eggs are laid in clutches on land, close to the water. Larvae of 45 mm length have been found in June-July

Tylototriton vietnamensis, Ha Giang, Vietnam. Photo: Max Sparreboom. 378

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Tylototriton vietnamensis, larva, parents from type locality. Photo: Frank Pasmans.

in ponds in secondary forest. Larvae nearing metamorphosis have been found in October (Böhme et al. 2005).

Distribution

This species is known from four provinces in northern and north-central Vietnam: Cao Bang, Lang Son, Bac Giang and Phu Tho (Nguyen et al., 2009) and may also occur in adjacent southern China and eastern Laos. The precise boundary of the species’ distribution is unclear.

Habitat

Tylototriton vietnamensis occurs in and near muddy ponds within dense bamboo vegetation in secondary forest (Schöttler, 2003; Bernardes et al., 2013). The holotype was described from Bac Giang Province in northern Vietnam, where it was found at an altitude of 250-300 m (Böhme et al., 2005). In the Tay Yen To Nature Reserve, in the north-east of Vietnam, this newt was found at altitudes between 180-580 m (Bernardes et al., 2011).

Behaviour

This species depends on the availability of small muddy pools in the shadow of trees for reproduction (Bernardes et al., 2012). Adults enter the ponds during the rainy season and leave again before October (Böhme et al., 2005). Most individuals found in the ponds are males and females are hard to find. Reproductive behaviour has not yet been described. Probably, females are at the breeding site for a very short period and mainly live on land. In captivity, a male has been observed

attempting to clasp a subadult female in the water in a ventral amplexus (pers. obs.).

Threats and conservation

The status of Tylototriton vietnamensis is still poorly known. It is listed as Endangered in the Vietnam Red Book (2007) and Near Threatened in the IUCN Red List of Threatened Species (IUCN, 2013).

Observations in captivity

Tylototriton vietnamensis has been kept in captivity in Europe (Fleck, 2010b). The species appears to be sensitive to diseases and not easy to keep alive. Captive breeding has not yet been reported. Some specimens are being reared from eggs collected at the type locality in 2010 (Pasmans, Sparreboom, pers. obs.)

Comments

Northern Vietnam and its neighbouring regions are home to several taxa of Tylototriton (T. vietnamensis, T. asperrimus, T. ziegleri, T. verrucosus, T. notialis) whose taxonomic status remains the subject of debate. Their relationships are unclear and their distribution ranges in Vietnam largely unknown. Records of T. asperrimus before 2005 may well refer to T. vietnamensis or other species, described at a later date (Bain & Nguyen, 2004).

References

Bain & Nguyen (2004); Bernardes et al. (2011, 2012,

2013); Böhme et al. (2005); Fleck (2010b); IUCN (2013); Nguyen et al. (2009); Schöttler (2003).

Tylototriton, breeding habitat, Ha Giang, Vietnam. Photo: Max Sparreboom. 379

Tylototriton wenxianensis Fei, Ye & Yang, 1984 | Wenxian Knobby Newt Description

A medium-sized Tylototriton. Head flat and oval, with prominent bony ridges. Head width equals head length. Rounded snout; no labial fold. Gular fold present. When forelimb is stretched forward, digits reach nostril. When limbs are adpressed, digits meet or slightly overlap. Dorsal ridge low and segmented; dorso-lateral warts are connected, forming a dorso-lateral ridge; boundary between warts is indistinct. Skin rough, size of warts nearly uniform on dorsum and venter. Tail compressed laterally and ending in a pointed tip. Tail shorter than snout-vent length.

development are only known from observations on captive animals (Fleck, 2013f). Clutches vary in size from 56-81 eggs and were laid partly underwater, partly in a transition zone between water and land, or partly on land (Pasmans et al., in press). The outer diameter of a single egg was 7-8 mm, and that of the yolk 3 mm. The embryo was pure white in colour and had a small brown polar cap. Eggs stored at 20°C hatched after 3-4 weeks. Metamorphosis followed some three months after oviposition.

Distribution

This species has a disjunct distribution. It is found in Wenxian in southern Gansu, Pingwu and Qingchuan in northern Sichuan, Leishan in eastern Guizhou, and in Zhongxian, Yunyang, Fengjie Counties of Chongqing, China, from 650-2,500 m altitude (Fei et al., 2006; IUCN, 2013). The population from the Tianping Mountains in Shangzhi County of Hunan Province has been described as a separate species, T. broadoridgus (Shen et al., 2012).

Habitat

Tylototriton wenxianensis inhabits forests near streams, and pools in hilly areas (IUCN, 2013). It hides under rocks near small ponds, surrounded by dense grassland (Li et al., 2008).

Behaviour Tylototriton wenxianensis, Guangyuan Pref., Sichuan. Photo: Hou Mian.

Dorsal colour entirely black; ventral colour brownish-black. Tips of digits and lower margin of tail orange. Cloacal region black in most specimens; only a few have yellow cloacal lips (Fei et al., 1984; Fei & Ye, 2001; Fei et al., 2005; Fei et al., 2006). Total length 125-141 mm for males (Fei et al., 1984).

Diagnosis

A medium-sized black Tylototriton, with warts the same colour as the back. Snout more rounded and bony ridges on head more prominent than in Tylototriton vietnamensis (Böhme et al., 2005). Differs from T. asperrimus by indistinct boundaries between the dorso-lateral warts and darker coloured cloacal region (Fei et al., 2005; Fei et al., 2006).

Eggs and larvae

Egg clutches are laid on land (Ye et al., 1993; Xie, 1999). Larvae develop in water. The reproductive season is in May-June (Xie, 1999). Egg and clutch size, and larval

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Little is known of this species’ natural history and behaviour. Observations on captive animals show that males enter the water before the females. A ventral amplexus, as in T. verrucosus and T. taliangensis, apparently forms part of the courtship, as well as a rotating courtship movement with heads directed at one another, but without physical contact (Fleck, 2013f; Pasmans et al., in press). Females lay clutches of eggs on land under dead leaves as do Echinotriton chinhaiensis (Ye et al., 1993; Xie, 1999). Like Echinotriton, hatchling larvae can reach the pond using leaping and wriggling movements (Pasmans et al., in press).

Threats and conservation

The distribution area of this species is shrinking due to cultivation of the species’ favourite habitat: moist forest with shallow, muddy, vegetated pools (Li et al., 2008). It is listed as Vulnerable (IUCN, 2013).

Observations in captivity

Tylototriton wenxianensis has been bred in captivity on several occasions (Fleck, 2010b, 2013f; Pasmans et al., in press).

Comments

The relationships between Tylototriton wenxianensis and similar species (T. asperrimus, T. hainanensis, T. vietnamensis, T. notialis) are unclear. In external characters

this species is most similar to T. asperrimus, of which it was originally considered to be a subspecies (Fei et al., 1984). Molecular work shows that genetic divergence between T. wenxianensis and T. asperrimus is moderate (Zhang et al., 2008; Stuart et al., 2010). There are reports of courtship behaviour observed in the wild (Gong et al., 2008a, 2008b), but it is unclear what observation methods were used. Some parts of these reports appear to have been copied uncritically from the existing literature – especially the articles on Echinotriton chinhaiensis – which raises doubts about their scientific value.

References

Böhme et al. (2005); Fei & Ye (2001); Fei et al. (1984, 2005,

2006); Fleck (2010b, 2013f); Gong et al. (2008a, 2008b); IUCN (2013);

Tylototriton wenxianensis, captive bred subadult. Photo: Frank Pasmans.

Li et al. (2008); Pasmans et al. (in press); Shen et al. (2012); Stuart et al. (2010); Xie (1999); Ye et al. (1993); Zhang et al. (2008).

Tylototriton yangi Hou, Zhang, Zhou, Li & Lü, 2012 | Tiannan Crocodile Newt

Tylototriton yangi, Gejiu City, Yunnan. Photo: Hou Mian.

Description

Snout short, slightly truncate in dorsal view, round in profile, exceeding beyond lower jaw. Glandular ridge on midline of crown from above anterior edge of the eye to middle of the head. Paratoids large. Distinct vertebral tubercular ridge from posterior end of crown to base of tail. Dorso-lateral row of ca. 16 large rib nodules on each side, from level of axilla to base of tail, distinctly knob-like at the axilla, becoming smaller towards the tail. Gular fold not prominent. Limbs stout and short, hindlimbs longer than forelimbs. Forelimbs, when stretched forward, reach the tip of the snout or slightly beyond. Tail laterally compressed, tip acuminate in profile.

This description is summarised from two unpublished English manuscripts, made available for this purpose by Hou Mian.

Colour dark brown to black. Bright orange-red colouration on corners of the mouth, dorso-lateral glands, paratoids, tail, fingers, toes and cloacal region.

A large, robust salamander, similar to Tylototriton kweichowensis. Head wider than body, longer than broad and sloping in profile.

Total length 127-158 mm in males, 145-172 in females (Fei et al., 2012; Hou et al., 2012).

Tylototriton yangi, female, Yunnan. Photo: Hou Mian.

Tylototriton yangi, female, ventral side, Yunnan. Photo: Hou Mian. 381

Diagnosis

A large, robust salamander with orange-red pigment on the corners of the mouth, paratoids, dorsal and dorso-lateral ridges, tail and digits. Similar to Tylototriton kweichowensis, but differs in the arrangement and form of dorso-lateral warts. In T. kweichowensis these are less knobby, square, smoother and more or less fused into orange rows, in T. yangi they are very prominent, round and separated from each other.

Eggs and larvae

Larvae are of the pond-type. Head is flat, the dorsal fin starts just behind the head. Colour from light yellow to tannish-grey with irregular light spots over the entire body that become more prominent when the larva reaches metamorphosis after some two months.

Distribution

This species is recorded from the region east of Yuan Chiang Red River. All known localities are on the YunnanGuizhou plateau. The easternmost site is in Wenshan National Nature Reserve, Laojunshan Mountain area, Wenshan County, Wenshan Autonomous Region, Yunnan. The southernmost locality is in Daweishan National Nature Reserve, Pingbian County, Honghe Autonomous Region, Yunnan.

Habitat

This species inhabits forested, karstic highlands at elevations above 1,200 m. In the breeding season the adult is found in paddy fields, ponds or quiet streams with water plants.

Behaviour

Tylototriton yangi forages in water and on land, and feeds on earthworms, tadpoles, water insects and crickets. The reproductive season is from May-June. Animals congregate in small pools, streams and marshes to mate and lay eggs.

Threats and conservation

This species is used as a drug in Chinese traditional medicine and thousands are exported via the illegal pet trade. Another threat is the use of pesticides and fertilisers in areas where agricultural fields are close to the breeding habitats. Researchers have observed a rapid decline in numbers and consider the species as Endangered (Hou Mian, pers. comm.).

Observations in captivity

This species has probably been kept in captivity as T. verrucosus, T. kweichowensis or T. shanjing. Reports are not available.

Comments

Phylogenetic analysis of mitochondrial DNA sequences and morphological features confirm this species’ placement in the T. verrucosus species group. Photos of adults, larvae, habitat and a range map are shown in Fei et al. (2012).

References

Fei et al. (2012); Hou et al. (2012).

Tylototriton ziegleri Nishikawa, Matsui & Nguyen, 2013 | Zieglers Knobby Newt Description

A medium-sized Tylototriton. Tylototriton ziegleri is distinguishable from the other species by molecular as well as morphological characteristics. It differs from other

species in the T. asperrimus group in having prominent bony ridges on head, denser granules on body, distinct tubercular vertebral ridge, and prominent knob-like warts (vs smoother skin, less developed ridges on head, slightly tubercular to smooth vertebral ridge, and slightly flattened to nearly indistinct warts in T. asperrimus, T. broadoridgus, T. hainanensis, T. lizhenchangi, T. notialis, T. vietnamensis, and T. wenxianensis) (Nishikawa et al., 2013a). Dorsum uniformly black; venter slightly lighter than dorsum. Warts, finger and toe-tips, parts of soles and palms, anterior end of vent, and ventral ridge of tail bright orange. Females a little larger than males, with shorter vent slit than males. Total length 110-142 mm for males, 142-145 mm for females (Nishikawa et al., 2013a; pers. obs.).

Diagnosis Tylototriton ziegleri, male, Pia Oac, Vietnam. Photo: Max Sparreboom. 382

Salamanders of the Old World | Tylototriton

A medium-sized black Tylototriton with rough, finely granulated skin; distinct bony ridges on head; segmented prominent vertebral ridge, forming a row of tubercles; rib

Tylototriton ziegleri, eggs found under a stone, Pia Oac, Vietnam. Photo: Max Sparreboom.

Tylototriton ziegleri, eggs and larva, Pia Oac, Vietnam. Photo: Max Sparreboom.

Tylototriton ziegleri, larvae, June 2009, Pia Oac, Vietnam. Photo: Nguyen Thien Tao.

Tylototriton ziegleri, larva, Pia Oac, Vietnam. Photo: Max Sparreboom.

Tylototriton ziegleri, fully developed larva, Pia Oac, Vietnam. Photo: Max Sparreboom.

Tylototriton ziegleri, just after metamorphosis, Pia Oac, Vietnam. Photo: Max Sparreboom.

Tylototriton ziegleri, juvenile, Pia Oac, Vietnam. Photo: Max Sparreboom. 383

nodules prominent; limbs long and thin; tips of forelimbs and hindlimbs greatly overlapping when adpressed; tail thin (Nishikawa et al., 2013a).

Eggs and larvae

Eggs are laid in clutches on land. In midMay 2010 two egg assemblages were found under a stone near a puddle in moist soil. The two assemblages totalled 123 eggs, possibly forming one clutch. Diameter of the egg capsule was 10-11 mm (Sparreboom et al., 2011). Two further clutches of 131 and 134 eggs were obtained from a captive female from Pia Oac, Cao Bang, in 2011 and 2012. Larvae hatch after 6-7 weeks at a length of 21-22 mm. On hatching the larvae have a long pigmented tail, no yolk remains, no balancers, and four well-developed legs. They are washed into the nearby water by the rains, or make their way to water using active leaping or wriggling movements (Sparreboom et al., 2011). Head of the larva is nearly trapezoidal, depressed and sloping in profile; snout short and slightly truncate; labial fold distinct; caudal fin higher than head; dorsal fin higher than ventral fin; dorsal fin starts at the middle of the trunk; tail-tip rounded. Colour yellowish-brown, becoming darker with age, until they are black shortly before metamorphosis. Venter whitish and transparent; golden spots scattered on dorsal head and trunk, lateral body, tail-fin, and axilla to throat. Fingers and toes yellow (Nishikawa et al., 2013a; pers. obs.). The larvae metamorphose some 3-4 months after oviposition, at a size varying from 43-62 mm, and move onto land. In the first weeks their skin is smooth, then it becomes more granular and warty (pers. obs.).

Distribution

The species is distributed in Ha Giang and Cao Bang Provinces, possibly also in Lao Cai Province, in northern Vietnam (Nishikawa et al., 2013a). The precise boundary of the species’ distribution is unclear.

Habitat

Tylototriton ziegleri is basically terrestrial and leads a secretive life on and under the forest floor.

Behaviour

The breeding season is from April-May (Nishikawa et al., 2013a). Reproduction occurs in both temporary and permanent ponds as well as in puddles in bamboo and primary forest. Males enter the water, but reproductive behaviour has not yet been observed.

Threats and conservation

Habitat loss and degradation, especially around the breeding ponds, appear to pose threats to the few known populations of this species (Nishikawa et al., 2013a).

Observations in captivity

Observations on eggs and larval development have been made on a small number of captive animals collected at Pia Oac, Cao Bang, in 2010. These specimens were then still identified as Tylototriton asperrimus. The animals were kept in terrariums with moss and cork bark at temperatures between 20-25°C. In spring they were housed in aquaterrariums with a land part and a water part some 3 cm deep. Egg clutches were deposited on land, hidden between cork bark and mosses (pers. obs.).

Tylototriton ziegleri, female with clutch, laid in captivity. Specimen from Pia Oac, Vietnam. Photo: Max Sparreboom.

Comments

Northern Vietnam hosts quite a number of Tylototriton species; their distribution ranges are largely unknown and their relationships unclear.

Tylototriton ziegleri, habitat, Pia Oac, Vietnam. Photo: Max Sparreboom. 384

Salamanders of the Old World | Tylototriton

References

Nishikawa et al. (2013a); Sparreboom et al. (2011).

Tylototriton breeding habitat, northern Vietnam. Photo: Max Sparreboom. 385

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Recommended general literature on salamanders Duellman, W.E. & Trueb, L., (1986). Biology of Amphibians. McGraw-Hill Book Company, New York, St Louis, San Francisco. Fei, L., Ye, C., Huang, Y. et al., (2006). Fauna Sinica, Amphibia Vol. 1. General Accounts of Amphibia, Gymnophiona and Urodela. Science Press, Beijing, China (in Chinese). Fei, L., Ye, C. & Jiang, J., (2012). Colored Atlas of Chinese Amphibians and their Distributions. Sichuan Publishing House of Science and Technology, Chengdu (in Chinese). Griffiths, R.A., (1996). Newts and Salamanders of Europe. T. & A.D. Poyser Natural History, London. Grossenbacher, K. & Thiesmeier, B. (Eds), (1999). Handbuch der Reptilien und Amphibien Europas. Band 4 Schwanzlurche (Urodela) I. Aula-Verlag, Wiesbaden. Grossenbacher, K. & Thiesmeier, B. (Eds), (2003). Handbuch der Reptilien und Amphibien Europas. Band 4 Schwanzlurche (Urodela) IIa. Aula-Verlag, Wiesbaden. Heatwole, H. (Ed. & co-editors), (1994-> ). Amphibian Biology. Surrey Beatty & Sons Pty Limited, Chipping Norton > Baulkham Hills, Australia. 1994 vol. 1 The Integument, 1995 vol. 2 Social Behaviour, 1998 vol. 3 Sensory

Ecological Aspects, Effect of Humans, and Management, 2013 vol. 11 part 3 Status of Conservation and Decline of Amphibians: Eastern Hemisphere: Western Europe. Nöllert, A. & Nöllert, C., (1992). Die Amphibien Europas. Franckh-Kosmos Verlags-GmbH & Co, Stuttgart. Pasmans, F., Bogaerts, S., Janssen, H. & Sparreboom, M., (in press). Schwanzlurche halten und züchten / Captive Husbandry of Salamanders and Newts. Natur und Tierverlag, Münster. Petranka, J.W., (1998). Salamanders of the United States and Canada. Smithsonian Institution Press, Washington, London. Raffaëlli, J., (2007). Les urodèles du monde. Penclen édition Schultschik, G. & Grosse, W.-R. (Eds), (2013). Threatened Newts and Salamanders – Guidelines for Conservation Breeding. Mertensiella 20e. Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V., Mannheim. Sever, D.M. (Ed.), (2003). Reproductive Biology and Phylogeny of Urodela. Science Publishers, Inc., Enfield (NH), USA, Plymouth, UK. Stebbins, R.C. & Cohen, N.W., (1995). A Natural History of Amphibians. Princeton University Press, Princeton, New Jersey. Thiesmeier, B. & Grossenbacher, K. (Eds), (2004). Handbuch der Reptilien

Perception, 2000 vol. 4 Palaeontology, 2003 vol. 5 Osteology, 2005 vol. 6

und Amphibien Europas. Band 4 Schwanzlurche (Urodela) IIb. Aula-Verlag,

Endocrinology, 2007 vol. 7 Systematics, 2009 vol. 8 Decline: Diseases, Para-

Wiesbaden.

sites, Maladies Pollution, 2010 vol. 9 part 1 Status of Decline of Amphibians: Western Hemisphere – Paraguay, Chile and Argentina, 2011 vol. 9 part 2 Status of Decline of Amphibians: Western Hemisphere – Uruguay, Brazil, Colombia and Ecuador, 2012 vol. 10 Conservation and Decline of Amphibians:

Thorn, R., (1969). Les salamandres d’Europe, d’Asie et d’Afrique du Nord. Éditions Paul Lechevalier, Paris. Wells, K.D., (2007). The Ecology and Behavior of Amphibians. The University of Chicago Press, Chicago, London.

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Websites Salamanders of the Old World started as an online catalogue allowing free access to information on the natural history of the newts and salamanders of Europe, Asia and Northern Africa (science.naturalis.nl/salamanders). From 2007 onward this website was hosted by the Naturalis Natural History Museum, since 2010 renamed the Naturalis Biodiversity Center, in Leiden. This catalogue was built up gradually until 2013, inspired by, and sharing data with the following websites: amphibiaweb.org/ AmphibiaWeb is an online system enabling anyone to search and retrieve information relating to amphibian biology and conservation. It aims at establishing a ‘home page’ for every species of amphibian in the world. AmphibiaWeb was created in conjunction with the Digital Library Project at the University of California, Berkeley, USA. iucnredlist.org/ This is the website of the International Union for Conservation of Nature and Natural Resources. The IUCN Red List presents a comprehensive assessment of the conservation status of the world’s known species of amphibians. The first assessment was completed as the Global Amphibian Assessment (GAA) in 2004 and was updated in 2006 and 2008. The latest version to date is The IUCN Red List of Threatened Species. Version 2013.1.

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Salamanders of the Old World | Websites

salamandersofchina.lifedesks.org. This is a lifedesk focusing on all of the Chinese salamander species. It is maintained by Yunke Wu, Harvard University, USA with species entries written by Max Sparreboom and Yunke Wu. tolweb.org/Caudata/ The website of The Tree of Life (ToL) Project provides a basic source of information regarding the evolutionary history of all organisms on Earth, including the major amphibian taxa. The salamander chapters are authored by Allan Larson, David Wake & Tom Devitt, 2006. The ToL Project is hosted by The University of Arizona College of Agriculture and Life Sciences and The University of Arizona Library. research.amnh.org/herpetology/amphibia/index.html Amphibian Species of the World is a fully searchable online reference of amphibian taxonomy referred to as Frost, Darrel R. 2013. Amphibian Species of the World: an Online Reference. Version 5.6 (9 January 2013). American Museum of Natural History, New York, USA. For care-sheets of species kept in captivity, and details on captive breeding, see caudata.org/ and ag-urodela.de. These sites provide links to other sites on captive maintenance of newts and salamanders.

Glossary Adpress to press closely against. With salamanders, the relative length of the limbs can be assessed by holding them closely against the side of the body and measuring the overlap or distance separating them Aestivation a period of inactivity during dry or hot periods in which animals await the return of conditions suitable for feeding and other activities Allopatric referring to two or more species or other groups that have non-overlapping ranges and are geographically isolated from one another Amphibians group of vertebrates that includes lissamphibians (Anura, composed of frogs and toads; Caudata, which includes salamanders and newts; and Gymnophiona, limbless amphibians also known as caecilians or apodans) and several extinct taxa that are more closely related to lissamphibians than to amniotes. Amphibians include aquatic, amphibious and terrestrial species Amplexus mating embrace of the female by the male; there are several types of amplexus (ventral and dorsal clasping, with limbs or with tail) Anterior referring to the front side of an animal, towards the head Aposematic colouration bright colouration or contrasting colour pattern serving as a warning signal to deter predators Axilla region formed by the posterior surfaces of the insertion of the forelimbs and the adjacent surfaces of the body; colloquially the ‘armpit’ Balancers these organs are small, fleshy, rod-like lateral appendages with slightly bulbous tips that project from the region of the jaw joint of salamander larvae in their early stages, before limbs develop; they disappear after a few days; typically – but not exclusively – associated with species that are pond-breeding as opposed to stream-breeding Benthic pertaining to the bottom of a body of water; opposite of nektonic Canthus rostralis a raised, dorsolateral, bony ridge that extends from the eye to the tip of the snout Caudal pertaining to the tail Caudata “tailed amphibians”; taxon that includes salamanders and newts; also called Urodela, one of the three main lissamphibian groups Choanae internal nares that open into the mouth cavity Cloaca the common chamber of the body that receives the products of the reproductive, digestive and excretory systems; it opens to the outside via the vent Conspecific belonging to the same species Costal grooves parallel, vertical folds on the side of the body, corresponding to the location of the ribs. There are several ways

of counting costal grooves. The method usually followed is to recognise only the lateral grooves between the fore- and hindlimbs, which do not touch the limb’s posterior and anterior margins, i.e. excluding axillary and inguinal grooves Courtship a series of behaviour patterns that precedes mating Dentition arrangement of the teeth Dimorphism the existence of two different morphologies; for instance between the sexes Distal away from the base or point of attachment (body); the outermost parts of limbs or tail; as opposed to proximal (near to) Diurnal active during the day Dorsal pertaining to the back side of the body (dorsum) Dorso-lateral the area between dorsal and lateral sides of the body; the area where many salamanders have glandular ridges or warts Dorsum the upper surface of the body Egg sac a turgid, sausage-shaped covering formed by the basal portion of the oviduct that encloses all the ova once the gelatinous layers around the individual eggs have been formed by more anterior zones of the oviduct. Egg sacs are unique to hynobiid salamanders. Females usually extrude two unfused sacs per ovulation event, one from the ovisac of each oviduct Endemic of unique occurrence in a specific country or area Gular fold an external flap or fold of tissue that extends across the lower throat region Herpetology the scientific study of amphibians and reptiles Hibernation a period of inactivity during cold periods Holotype the single specimen designated or otherwise fixed as the name-bearing type of a nominal species or subspecies when the nominal taxon is established Hyobranchium the tongue-gill apparatus in salamanders; has a dual role as a buccal pump mechanism in respiration and as the main mechanism for tongue protrusion Intercanthal distance minimum distance between anterior corners of the eyes Internarial distance minimum distance between external nares Juviparous giving birth to fully developed, metamorphosed young (as in Salamandra salamandra bernardezi); also viviparous Karst a typical landscape that is formed when limestone is exposed to high precipitation. Limestone easily dissolves in water, which causes gullies, cracks, caves, dolines and a variety of other features. Examples are the Sierras of western Andalusia in Spain, rock formations in Sardinia (Italy), the Dinaric Alps in the Balkan countries, and the mountain ranges along the southwestern Turkish coast. Karst landscape is home to a large number of amphibians and other fauna as it offers them a refuge underground in hot and dry summers 421

Labial fold a fold of tissue extending the upperlip, serving to suck prey into the mouth cavity; often found in salamanders in the aquatic stage Larva an immature form of an animal that radically differs in appearance from the adult Larviparous depositing larvae with legs and gills (as in Salamandra salamandra); also ovoviviparous Lateral pertaining to the side of the body Lectotype a syntype designated as the single name-bearing type specimen subsequent to the establishment of a nominal species or subspecies Lentic pertaining to standing or slow-moving, plankton-rich water bodies, such as ponds, lakes, swamps and bogs Lotic pertaining to fast-moving, plankton-poor water bodies, such as springs, headwater streams, and rivers Maxillary teeth teeth on the maxillary bones, located along the sides of the upper jaw Mental gland gland on the chin region of the male of some salamander species, serving to stimulate females during courtship; often organized into patches, which are visible with the naked eye Metamorphosis the transformation from a gilled larva to a juvenile salamander that lacks gills Monophyletic forming a category descended from a common ancestor Monotypic referring to a taxonomic group that contains only one taxon of the immediately lower rank; e.g. a monotypic genus contains only one species Nasolabial grooves a pair of shallow slit-like channels between nostril and upper jaw in males of all lungless salamanders of the family Plethodontidae. During the breeding season the margin of the lip encompassing the terminus of each groove becomes elongated into a fleshy extension called a cirrus. Presumably the enlarged sensory tracts facilitate olfactory trailing of females by males and avoidance of tracks left by other males Nektonic moving actively by themselves in the water column, as opposed to benthic Neotenic animals in a state of neoteny; i.e. they are sexually mature in the larval stage Neoteny retention of larval features and delay of metamorphosis; partial neoteny is when the larva fails to metamorphose and continues growing; total neoteny occurs when the animal actually achieves sexual maturity and breeds in the larval stage; see also paedomorphosis. Neoteny is sometimes understood as only referring to delayed metamorphosis, in contrast to paedomorphosis which refers to retention of juvenile features in the adult animal. The phenomenon is especially common in the Alpine Newt, Ichthyosaura alpestris Neotype the single specimen designated as the name-bearing type of a nominal species or subspecies when there is a need to define the nominal taxon objectively and no name-bearing type is believed to be extant 422

Salamanders of the Old World | Glossary

Nocturnal active at night Oophagy eating of eggs of the same species; observed in many species of newts during the aquatic stage Oviparous egg-laying Oviposit to deposit eggs Ovoviviparous bearing live young from eggs; the young develop within the fertilised eggs in the womb, and hatch at or shortly after egg laying (for instance in most forms of Salamandra salamandra); also larviparous Paedomorphosis retention of juvenile features in the adult; see neoteny Parapatric referring to two or more species or groups with adjoining but non-overlapping geographic ranges; opposite of sympatric Paratoids also parotoids, parotids or paratoid glands swollen, glandular structures behind the eyes, secreting a toxic white substance that deters predators Paratype each specimen of a type series other than the holotype Pheromones chemicals that provide scent information left by one animal to another individual of the same species Phylogeny diagram that represents the evolutionary relationships between organisms. It includes a topology (which indicates only a nested or hierarchical pattern of relationships) and branch lengths (representing the evolutionary distances between taxa) Polyphyletic forming a category descended from different ancestors Posterior referring to the back side of an animal, towards the tail Premaxillary teeth teeth on the premaxillary bone, located in the anterior medial portion of the upper jaw Proximal near the base or point of attachment (body); as opposed to distal (away from) Rheophilous adapted to life in streams Rostral on the anterior tip of the upper jaw Rugose possessing a rough surface, creased or wrinkled Sacrum bone in the pelvis Species an identifiable and distinct group of organisms whose members breed and produce viable offspring under natural conditions Spermatheca a chamber leading off the internal lining of the female cloaca that is used to store sperm Spermatophore a structure comprising a sperm-filled capsule resting upon an elaborately shaped gelatinous base, deposited during courtship by the male Subspecies a taxonomic unit, or ‘race’ within a species, usually defined as morphologically distinct and occupying a geographic range that does not overlap with that of other races of the species. Subspecies may interbreed naturally in areas of geographic contact

Sympatric referring to two or more species or groups that have overlapping ranges and occur in the same geographic region; opposite of parapatric Synapomorphic referring to a shared character inherited from a direct common ancestor Syntopic referring to two or more species or groups that occur together locally in the same habitat Syntype each specimen of a type series from which neither a holotype nor a lectotype has been designated. The syntypes collectively constitute the name-bearing type Systematics science that studies the diversity and evolution of biological organisms. It includes taxonomy Tail filament the region of the tail-tip which is devoid of tail-fin and shows a distinct transition from the rest of the tail (as in Lissotriton helveticus and L. vulgaris kosswigi) Taxon (plural taxa) the taxonomic name applied to a group of organisms, such as a family, genus, species or subspecies Taxonomy the study of the systematic classification and naming of organisms

Terra typica or type locality the geographical place of capture, collection, or observation of the name-bearing type of a nominal species or subspecies Tubercle a small raised bump on the skin Type a term to denote a particular kind of specimen or taxon Type locality or terra typica the geographical place of capture, collection, or observation of the name-bearing type of a nominal species or subspecies Urodela taxon (whose members are called ‘urodeles’) that includes salamanders and newts; also called Caudata, ‘tailed amphibians’, one of the three main lissamphibian groups Vent external cloacal opening; see cloaca Venter the lower surface of the body Ventral pertaining to the underside of the body Vertebral along the dorsal midline of the body Vertebrates animals that possess a backbone such as fish, amphibians, reptiles, birds, and mammals Viviparous live-bearing, giving birth to fully developed young (as in Lyciasalamandra); also juviparous Vomerine teeth tooth patches or tooth rows located on paired bones on the roof of the mouth Xeric dry; said of landscapes such as deserts

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Index of scientific names Ambystoma mexicanum ............................ 15, 17 Ambystomatidae ....................................... 14, 15 Amphibia ......................................................... 7, 14 Amphiumidae ............................................ 14, 16 Andrias ................................................................... 27 Andrias davidianus ........................................... 27 Andrias japonicus ................................ 15, 20, 30 Anura ..................................................................... 14 Atylodes ............................................................... 148 Atylodes genei .................................................... 148 Batrachochytrium dendrobatidis ......... 23, 32 Batrachochytrium salamandrivorans ..... 333 Batrachuperus ..................................................... 39 Batrachuperus karlschmidti .......................... 39 Batrachuperus londongensis ......................... 41 Batrachuperus pinchonii .......................... 35, 43 Batrachuperus taibaiensis ....................... 35, 45 Batrachuperus tibetanus ................................ 46 Batrachuperus yenyuanensis ....................... 49 Batracobdella algira ....................... 157, 158, 165 Calotriton ............................................................. 171 Calotriton arnoldi ............................................. 171 Calotriton asper ................................................ 172 Caudata ................................................................. 14 Chioglossa ............................................................ 176 Chioglossa lusitanica ...................................... 176 Chioglossa lusitanica longipes ..................... 176 Chioglossa lusitanica lusitanica ................. 176 Cryptobranchidae .............................. 14, 16, 19 Cryptobranchus ........................................... 14, 16 Cryptobranchus alleganiensis ....................... 16 Cynops .................................................................. 180 Cynops chenggongensis ................................. 180 Cynops cyanurus ............................................... 181 Cynops cyanurus chuxiongensis ................ 182 Cynops cyanurus cyanurus .......................... 182 Cynops ensicauda ............................................. 184 Cynops ensicauda ensicauda ....................... 184 Cynops ensicauda popei ................................. 184 Cynops fudingensis ......................................... 188 Cynops glaucus ................................................. 190 Cynops orientalis .............................................. 190 Cynops orientalis orientalis .......................... 191 Cynops orientalis qianshan ........................... 191 Cynops orphicus ............................................... 192 Cynops pyrrhogaster ...................................... 193 Cynops pyrrhogaster pyrrhogaster ........... 194 Cynops pyrrhogaster sasayamae ............... 194 424

Salamanders of the Old World | Index

Cynops wolterstorffi ........................................ 197 Dicamptodontidae ......................................... 14 Echinotriton ....................................................... 199 Echinotriton andersoni .................................. 199 Echinotriton chinhaiensis ............................ 202 Euproctus ........................................................... 207 Euproctus montanus ...................................... 207 Euproctus platycephalus ............................... 210 Gymnophiona ................................................... 14 Hynobiidae ........................................... 15, 20, 33 Hynobius ................................................................ 51 Hynobius abei ...................................................... 51 Hynobius amjiensis ........................................... 53 Hynobius arisanensis ....................................... 54 Hynobius boulengeri .................................. 37, 56 Hynobius chinensis ............................................ 57 Hynobius dunni ............................................ 37, 59 Hynobius formosanus ................................ 37, 60 Hynobius fuca ...................................................... 62 Hynobius glacialis .............................................. 63 Hynobius guabangshanensis ......................... 65 Hynobius hidamontanus ................................ 66 Hynobius hirosei ................................................. 68 Hynobius katoi ................................................... 69 Hynobius kimurae ........................................ 37, 71 Hynobius leechii .................................................. 72 Hynobius lichenatus ......................................... 74 Hynobius maoershanensis .............................. 76 Hynobius naevius ............................................... 77 Hynobius nebulosus .......................................... 79 Hynobius nigrescens .................................... 37, 81 Hynobius okiensis ........................................ 37, 83 Hynobius quelpaertensis .......................... 37, 84 Hynobius retardatus .................................. 37, 86 Hynobius sonani ................................................. 89 Hynobius stejnegeri ........................................... 91 Hynobius takedai ............................................... 92 Hynobius tokyoensis .................................. 37, 93 Hynobius tsuensis .............................................. 95 Hynobius turkestanicus .................................. 96 Hynobius yangi ................................................... 97 Hynobius yatsui .................................................. 98 Hynobius yiwuensis ......................................... 99 Ichthyosaura ....................................................... 213 Ichthyosaura alpestris .................................... 213 Ichthyosaura alpestris alpestris ................. 214 Ichthyosaura alpestris apuana .................... 214 Ichthyosaura alpestris cyreni ...................... 214

Ichthyosaura alpestris veluchiensis .......... 214 Karsenia ................................................................ 151 Karsenia koreana ........................................ 14, 151 Laotriton .............................................................. 218 Laotriton laoensis ............................................ 218 Lissotriton ........................................................... 221 Lissotriton boscai .............................................. 221 Lissotriton helveticus ..................................... 224 Lissotriton italicus ........................................... 227 Lissotriton montandoni ................................ 229 Lissotriton vulgaris ......................................... 233 Lissotriton vulgaris ampelensis ................. 234 Lissotriton vulgaris dalmaticus ................. 236 Lissotriton vulgaris graecus ......................... 234 Lissotriton vulgaris intermedia .................. 236 Lissotriton vulgaris kosswigi ...................... 234 Lissotriton vulgaris lantzi ............................ 235 Lissotriton vulgaris meridionalis .............. 235 Lissotriton vulgaris schmidtlerorum ........ 235 Lissotriton vulgaris schreiberi .................... 236 Lissotriton vulgaris tomasini ...................... 236 Lissotriton vulgaris vulgaris ....................... 236 Liua ........................................................................ 103 Liua shihi ............................................................. 103 Liua tsinpaensis ......................................... 35, 105 Lyciasalamandra .............................................. 241 Lyciasalamandra antalyana ....................... 242 Lyciasalamandra arkani ............................... 241 Lyciasalamandra atifi ................................... 243 Lyciasalamandra billae ................................ 244 Lyciasalamandra fazilae .............................. 245 Lyciasalamandra flavimembris ................ 246 Lyciasalamandra helverseni ....................... 247 Lyciasalamandra irfani ................................. 241 Lyciasalamandra jehudai ............................. 241 Lyciasalamandra luschani .......................... 249 Lyciasalamandra luschani basoglui ........ 249 Lyciasalamandra luschani finikensis ...... 249 Lyciasalamandra luschani luschani ........ 249 Mertensiella ........................................................ 252 Mertensiella caucasica ................................... 252 Natrix ........... 148, 153, 212, 254, 268, 271, 309 Necturus ................................................................ 16 Neurergus ............................................................ 256 Neurergus crocatus .......................................... 256 Neurergus derjugini ........................................ 258 Neurergus kaiseri ............................................ 260 Neurergus strauchii ........................................ 262

Neurergus strauchii barani ........................... 263 Neurergus strauchii strauchii ...................... 263 Notophthalmus ............................................. 14, 15 Ommatotriton .................................................. 266 Ommatotriton ophryticus ........................... 266 Ommatotriton ophryticus nesterovi ........ 267 Ommatoriton ophryticus ophryticus ...... 267 Ommatotriton vittatus ................................. 269 Ommatotriton vittatus cilicensis ............. 269 Ommatotriton vittatus vittatus ............... 270 Onychodactylus ................................................ 107 Onychodactylus fischeri ................................ 107 Onychodactylus japonicus .................... 35, 109 Onychodactylus kinneburi ............................ 112 Onychodactylus koreanus ...................... 35, 113 Onychodactylus nipponoborealis .............. 116 Onychodactylus tsukubaensis ..................... 118 Onychodactylus zhangyapingi .................... 119 Onychodactylus zhaoermii ........................... 121 Pachyhynobius .................................................. 123 Pachyhynobius shangchengensis ........ 35, 123 Pachytriton ............................................... 272, 297 Pachytriton archospotus ............................... 272 Pachytriton brevipes ....................................... 273 Pachytriton changi .......................................... 275 Pachytriton feii .................................................. 277 Pachytriton granulosus .................................. 278 Pachytriton inexpectatus .............................. 279 Pachytriton labiatus .............................. 279, 281 Pachytriton moi ................................................ 281 Pachytriton xanthospilos .............................. 275 Paradactylodon ................................................. 125 Paradactylodon gorganensis ................. 35, 125 Paradactylodon mustersi ....................... 35, 126 Paradactylodon persicus ............................... 128 Paramesotriton .................................................. 283 Paramesotriton caudopunctatus ................ 283 Paramesotriton chinensis ............................. 286 Paramesotriton deloustali ........................... 288 Paramesotriton fuzhongensis ..................... 290 Paramesotriton guangxiensis ..................... 292 Paramesotriton hongkongensis .................. 293 Paramesotriton labiatus ............................... 296 Paramesotriton longliensis .......................... 298 Paramesotriton maolanensis ...................... 299 Paramesotriton wulingensis ....................... 300 Paramesotriton yunwuensis ........................ 301 Paramesotriton zhijinensis .......................... 302 Plethodontidae ........................................ 21, 147 Pleurodeles ......................................................... 304 Pleurodeles nebulosus .................................... 304

Pleurodeles poireti .............................................. 305 Pleurodeles waltl .............................................. 307 Procyon lotor ..................................................... 269 Proteidae ..................................................... 16, 166 Proteus .................................................................. 166 Proteus anguinus .............................................. 167 Proteus anguinus anguinus .......................... 168 Proteus anguinus parkelj ............................... 168 Protohynobius .................................................... 131 Pseudohynobius ................................................. 131 Pseudohynobius flavomaculatus ......... 37, 132 Pseudohynobius guizhouensis ...................... 133 Pseudohynobius jinfo ...................................... 134 Pseudohynobius kuankuoshuiensis ........... 135 Pseudohynobius puxiongensis .................... 136 Pseudohynobius shuichengensis .................. 137 Ranodon ............................................................... 139 Ranodon sibiricus ..................................... 35, 139 Rhyacotritonidae ...................................... 14, 15 Salamandra ......................................................... 311 Salamandra algira ............................................ 311 Salamandra algira algira ............................... 311 Salamandra algira spelaea ............................ 311 Salamandra algira splendens ...................... 312 Salamandra algira tingitana ....................... 312 Salamandra atra ............................................... 314 Salamandra atra aurorae .............................. 315 Salamandra atra pasubiensis ...................... 315 Salamandra atra prenjensis ......................... 315 Salamandra corsica ......................................... 318 Salamandra infraimmaculata ................... 320 Salamandra infraimmaculata infraimmaculata ............................................. 320 Salamandra infraimmaculata orientalis 320 Salamandra infraimmaculata semenovi 320 Salamandra lanzai .......................................... 323 Salamandra maxima ......................................... 15 Salamandra salamandra ............................... 325 Salamandra salamandra albanica ............ 325 Salamandra salamandra alfredschmidti 325 Salamandra salamandra almanzoris ....... 325 Salamandra salamandra bejarae ............... 327 Salamandra salamandra bernardezi ........ 327 Salamandra salamandra beschkovi .......... 325 Salamandra salamandra carpathica ........ 325 Salamandra salamandra crespoi ................ 327 Salamandra salamandra fastuosa ............. 327 Salamandra salamandra gallaica .............. 327 Salamandra salamandra gigliolii .............. 328 Salamandra salamandra longirostris ...... 328 Salamandra salamandra morenica ........... 328

Salamandra salamandra salamandra ......... 329 Salamandra salamandra terrestris ........... 329 Salamandra salamandra werneri ............. 330 Salamandrella ................................................... 142 Salamandrella keyserlingii .................... 35, 142 Salamandrella tridactyla ...................... 35, 145 Salamandridae ........................................ 21, 170 Salamandrina .................................................... 335 Salamandrina perspicillata ......................... 335 Salamandrina terdigitata ............................. 338 Sirenidae .............................................................. 16 Speleomantes ...................................................... 153 Speleomantes ambrosii ................................... 153 Speleomantes ambrosii ambrosii ................ 154 Speleomantes ambrosii bianchii ................. 154 Speleomantes flavus ........................................ 156 Speleomantes imperialis ................................ 157 Speleomantes italicus ..................................... 159 Speleomantes sarrabusensis ......................... 160 Speleomantes strinatii ................................... 162 Speleomantes supramontis ........................... 164 Taricha ............................................................. 14, 15 Triturus ............................................................... 340 Triturus carnifex ............................................. 340 Triturus cristatus ........................................... 342 Triturus dobrogicus ........................................ 345 Triturus ivanbureschi ................................... 346 Triturus karelinii ............................................ 348 Triturus macedonicus ................................... 350 Triturus marmoratus ..................................... 351 Triturus pygmaeus .......................................... 354 Tylototriton ........................................................ 357 Tylototriton asperrimus ............................... 358 Tylototriton broadoridgus ............................ 359 Tylototriton dabienicus ................................ 360 Tylototriton daweishanensis ...................... 361 Tylototriton hainanensis .............................. 361 Tylototriton kweichowensis ........................ 362 Tylototriton lizhenchangi ............................ 364 Tylototriton notialis ....................................... 365 Tylototriton panhai ....................................... 366 Tylototriton pseudoverrucosus .................. 367 Tylototriton shanjing .................................... 369 Tylototriton taliangensis .............................. 371 Tylototriton uyenoi ......................................... 372 Tylototriton verrucosus ................................. 373 Tylototriton vietnamensis ........................... 378 Tylototriton wenxianensis .......................... 380 Tylototriton yangi ........................................... 381 Tylototriton ziegleri ........................................ 382 Urodela ............................................................... 423 425

Maps of Europe and Northern Africa, the Near East, South-East and East Asia

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Salamanders of the Old World

About the author Max Sparreboom is a research associate of the Naturalis Biodiversity Center, Leiden, with a long-standing interest in the amphibian fauna of Europe and Asia. He is also director of the Praemium Erasmianum Foundation in Amsterdam.

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