Voles and Lemmings (Arvicolinae) of the Palaearctic Region Authors Boris Kryštufek Georgy I. Shenbrot July 2022 Title Voles and Lemmings (Arvicolinae) of the Palaearctic Region Authors Boris Kryštufek (Slovenian Museum of Natural History, Vertebrate Department & Science and Research Centre Koper, Mediterranean Institute for Environmental Studies) Georgy I. Shenbrot (Ben-Gurion University of the Negev, Jacob Blaustein Institutes for Desert Research, Mitrani Department of Desert Ecology & Russian Academy of Sciences, A. N. Severtsov Institute of Ecology and Evolution) Review Boris Krasnov (Ben-Gurion University of the Negev, Jacob Blaustein Institutes for Desert Research) Ivan Horáček (Charles University, Faculty of Science) Language editing Karolyn Close Technical editor Jan Perša (University of Maribor, University Press) Cover designer Jan Perša (University of Maribor, University Press) Cover graphics Kryštufek, Shenbrot, 2022 Published by University of Maribor, University Press Slomškov trg 15, 2000 Maribor, Slovenia https://press.um.si, zalozba@um.si Issued by University of Maribor, Faculty of Natural Sciences and Mathematics Koroška cesta 160, Maribor, Slovenia https://www.fnm.um.si, fnm@um.si Edition 1st Published at Maribor, Slovenia, July 2022 Publication type E-book Available at https://press.um.si/index.php/ump/catalog/book/664 CIP - Kataložni zapis o publikaciji © University of Maribor, University Press Univerzitetna knjižnica Maribor Text © Kryštufek & Shenbrot, 2022 599(0.034.2) This work is licensed under the Creative Commons Attribution 4.0 International License. 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If you would like to reuse any https://press.um.si/index.php/ump/catalog/ third-party material not covered by the book’s Creative book/664 Commons licence, you wil need to obtain permission directly ISBN 978-961-286-611-2 from the copyright holder. doi: 10.18690/um.fnm.2.2022 COBISS.SI-ID 115344131 https://creativecommons.org/licenses/by/4.0 The Book was co-financed by the Slovenian Research Agency ISBN 978-961-286-611-2 (pdf) DOI https://doi.org/10.18690/um.fnm.2.2022 978-961-286-613-6 (hardback) Price Free copy For publisher prof. dr. Zdravko Kačič, rector of University of Maribor Attribution Kryštufek, B. & Shenbrot, G. I. (2022). Voles and Lemmings (Arvicolinae) of the Palaearctic Region. Maribor: University Press. doi: 10.18690/um.fnm.2.2022 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION B. Kryštufek, G. I. Shenbrot Table of Contents Preface............................................................................................................................................1 Acknowledgements ....................................................................................................................... 3 Taxonomy and nomenclature ....................................................................................................... 5 Family-group names ............................................................................................................................................... 5 Genera and Species................................................................................................................................................. 5 Subspecies... ............................................................................................................................................................. 7 Geographic setting ........................................................................................................................ 9 Characteristics of Voles and Lemmings ...................................................................................... 11 External appearance ............................................................................................................................................. 12 Skin derivatives...................................................................................................................................................... 12 Penis and baculum ................................................................................................................................................ 14 Sperm head ............................................................................................................................................................ 14 Skull ..................... ....................................................................................................................................................16 Dentition..... ........................................................................................................................................................... 16 Karyotype... ............................................................................................................................................................ 20 Abbreviations ................................................................................................................................ 21 TRIBE: Pometheomyini Kretzoi, 1955 .........................................................................................25 GENUS: Prometheomys Satunin, 1901 – Long-clawed Mole Voles ................................................................. 25 Prometheomys schaposchnikowi (Satunin, 1901) – Long-clawed Mole Vole ........................................................ 25 TRIBE: Dicrostonychini Kretzoi, 1955 ........................................................................................29 GENUS: Dicrostonyx Gloger, 1841 – Col ared (Varying) Lemmings............................................................. 29 SUBGENUS: Dicrostonyx Gloger, 1841 ............................................................................................................. 32 Dicrostonyx groenlandicus (Traill, 1823) – Nearctic Col ared Lemming............................................................. 32 Dicrostonyx groenlandicus vinogradovi Ognev, 1948 – Vinogradov’s Collard Lemming .................................... 33 SUBGENUS: Myolemmus Pomel, 1852 .............................................................................................................. 33 Dicrostonyx torquatus (Pallas, 1779) – Siberian (Palaearctic) Collared Lemming ............................................ 33 Dicrostonyx torquatus torquatus (Pallas, 1779) ....................................................................................................... 35 Dicrostonyx torquatus pallidus (Middendorff, 1852) ............................................................................................. 36 Dicrostonyx torquatus ungulatus (Baer, 1841) ......................................................................................................... 36 TRIBE: Lemmini Mil er, 1896 ......................................................................................................37 GENUS: Lemmus Link, 1795 – Brown Lemmings .......................................................................................... 38 Lemmus lemmus (Linnæus, 1758) – Palaearctic Brown Lemming .................................................................... 39 ii TABLE OF CONTENTS. Lemmus lemmus lemmus (Linnæus, 1758) .............................................................................................................. 43 Lemmus lemmus chernovi Spitsyn, Bolotov & Kondakov, 2021 ......................................................................... 43 Lemmus lemmus sibiricus (Kerr, 1792) ................................................................................................................... 44 Lemmus lemmus amurensis Vinogradov, 1924 ....................................................................................................... 45 Lemmus lemmus novosibiricus Vinogradov, 1924 ................................................................................................... 46 Lemmus lemmus ognevi Vinogradov, 1933 ............................................................................................................. 46 Lemmus lemmus portenkoi Tchernyavsky, 1967 .................................................................................................... 47 Lemmus lemmus kamchaticus new subspecies ........................................................................................................ 47 Lemmus nigripes (True, 1894) – Beringian Brown Lemming ............................................................................ 48 GENUS: Myopus Miller, 1910 – Wood Lemmings .......................................................................................... 49 Myopus schisticolor (Lilljeborg, 1844) – Wood Lemming ................................................................................... 49 TRIBE: Clethrionomyini Hooper & Hart, 1962 ..........................................................................53 SUBTRIBE: Clethrionomyina Hooper & Hart, 1962 ..................................................................54 GENUS: Clethrionomys Tilesius, 1850 – Red-backed Voles ............................................................................ 54 Clethrionomys glareolus (Schreber, 1780) – Bank Vole......................................................................................... 59 Clethrionomys rutilus (Pallas, 1779) – Siberian Red-backed Vole ...................................................................... 61 Clethrionomys centralis (Miller, 1906) – Tien Shan Red-backed Vole ................................................................ 64 GENUS: Alticola Blanford, 1881 – Mountain Voles ....................................................................................... 65 SUBGENUS: Alticola Blanford, 1881 ................................................................................................................ 68 Alticola roylei (Gray, 1842) – Royle’s Mountain Vole ........................................................................................ 69 Alticola montosus (True, 1894) – Kashmir Mountain Vole ............................................................................... 72 Alticola kohistanicus new species – Kohistan Mountain Vole........................................................................... 72 Alticola argentatus (Severtzov, 1879) – Silver Mountain Vole .......................................................................... 74 Alticola argentatus argentatus (Severtzov, 1879) .................................................................................................... 77 Alticola argentatus blanfordi (Scully, 1880) ............................................................................................................. 78 Alticola argentatus severtzowi (Tikhomirov & Korchagin, 1889) ........................................................................ 78 Alticola argentatus worthingtoni Miller, 1906 .......................................................................................................... 79 Alticola argentatus phasma Miller, 1912 ................................................................................................................. 79 Alticola argentatus subluteus Thomas, 1914 ........................................................................................................... 79 Alticola argentatus tarasovi Rossolimo & Pavlinov, 1992 .................................................................................... 79 Alticola albicauda (True, 1894) – White-tailed Mountain Vole......................................................................... 80 Alticola parvidens Schlitter & Setzer, 1973 – Hindu Kush Mountain Vole .................................................... 81 Alticola stoliczkanus (Blanford, 1875) – Stoliczka’s Mountain Vole ................................................................ 82 Alticola stoliczkanus stoliczkanus (Blanford, 1875) ............................................................................................... 85 Alticola stoliczkanus lama (Barrett-Hamilton, 1900) ........................................................................................... 85 Alticola stoliczkanus bhatnagari Biswas & Khajuria, 1955 ................................................................................... 85 Alticola barakshin Bannikov, 1947 – Gobi Altai Mountain Vole .................................................................... 86 Alticola strelzovi (Kastschenko, 1899) – Strelzov’s Mountain Vole ................................................................. 87 Alticola strelzovi strelzovi (Kastschenko, 1899) ..................................................................................................... 90 Alticola strelzovi desertorum (Kastschenko, 1901) ................................................................................................. 91 Alticola semicanus (G. M. Allen, 1924) – Khangay (Mongolian) Mountain Vole ........................................... 91 Alticola semicanus semicanus (G. M. Allen, 1924) ................................................................................................. 92 Alticola semicanus al eni Argyropulo, 1933 ........................................................................................................... 92 Alticola tuvinicus Ognev, 1950 – Tuva Mountain Vole ..................................................................................... 93 Alticola tuvinicus tuvinicus Ognev, 1950 ................................................................................................................ 94 Alticola tuvinicus khubsugulensis Litvinov, 1973 .................................................................................................... 95 Alticola olchonensis Litvinov, 1960 – Baikal Mountain Vole .............................................................................. 96 SUBGENUS: Aschizomys Miller, 1899 ............................................................................................................... 96 Alticola macrotis (Radde, 1861) – Large-eared Vole ........................................................................................... 97 Alticola macrotis macrotis (Radde, 1861) ................................................................................................................ 99 Alticola macrotis fetisovi (Galkina & Jepifantseva, 1988) ................................................................................... 100 TABLE OF CONTENTS iii. Alticola lemminus (Miller, 1899) – Lemming Vole ............................................................................................. 100 GENUS: Craseomys Miller, 1900 – Grey-sided Voles .................................................................................... 102 SUBGENUS: Craseomys Miller, 1900 ............................................................................................................... 104 Craseomys rufocanus (Sundevall, 1846) – Siberian Grey-sided Vole ................................................................ 104 Craseomys rufocanus rufocanus (Sundevall, 1846) ................................................................................................. 107 Craseomys rufocanus bedfordiae (Thomas, 1905) ................................................................................................... 108 Craseomys rufocanus shanseius Thomas, 1908 ...................................................................................................... 108 Craseomys rex (Imaizumi, 1971) – Dark Grey-sided Vole .............................................................................. 108 SUBGENUS: Phaulomys Thomas, 1905 ........................................................................................................... 109 Craseomys regulus Thomas, 1907 – Korean Grey-sided Vole .......................................................................... 110 Craseomys smithi (Thomas, 1905) – Smith’s Grey-sided Vole ....................................................................... 112 Craseomys andersoni (Thomas, 1905) – Anderson’s Grey-sided Vole ............................................................ 113 SUBTRIBE: Eothenomyina – New Subtribe ............................................................................ 115 GENUS: Caryomys Thomas, 1911 – Brownish Voles .................................................................................... 115 Caryomys inez (Thomas, 1908) – Short-tailed Brownish Vole ....................................................................... 116 Caryomys inez inez (Thomas, 1908) ..................................................................................................................... 118 Caryomys inez nux (Thomas, 1910) ..................................................................................................................... 118 Caryomys eva (Thomas, 1911) – Long-tailed Brownish Vole ......................................................................... 119 Caryomys eva eva (Thomas, 1911) ........................................................................................................................ 119 Caryomys eva alcinous (Thomas, 1911) ................................................................................................................ 120 GENUS: Eothenomys Miller, 1900 – Oriental Voles ....................................................................................... 120 Eothenomys melanogaster (A. Milne Edwards, 1871) – Père David’s Oriental Vole ...................................... 121 Eothenomys colurnus (Thomas, 1911) – Fujian Oriental Vole .......................................................................... 122 Eothenomys colurnus colurnus (Thomas, 1911) ..................................................................................................... 124 Eothenomys colurnus kanoi Tokuda, 1937 ............................................................................................................ 124 Eothenomys eleusis (Thomas, 1911) – Yunnan Oriental Vole .......................................................................... 125 Eothenomys eleusis eleusis (Thomas, 1911) ........................................................................................................... 128 Eothenomys eleusis miletus (Thomas, 1914) .......................................................................................................... 128 Eothenomys eleusis fidelis Hinton, 1923 ................................................................................................................ 129 Eothenomys eleusis cachinus (Thomas, 1921) ........................................................................................................ 129 Eothenomys eleusis shimianensis Liu, 2018 ............................................................................................................. 130 GENUS: Anteliomys Miller, 1896 – Chinese Voles ......................................................................................... 130 SUBGENUS: Anteliomys Miller, 1896 .............................................................................................................. 131 Anteliomys chinensis (Thomas, 1891) – Long-tailed Chinese Vole.................................................................. 131 Anteliomys olitor (Thomas, 1911) – Dwarf Chinese Vole................................................................................ 132 Anteliomys olitor olitor (Thomas, 1911) ............................................................................................................... 132 Anteliomys olitor hypolitor (Wang & Li, 2000) ..................................................................................................... 135 Anteliomys proditor (Hinton, 1923) – Yulungshan Chinese Vole.................................................................... 135 Anteliomys wardi (Thomas, 1912) – Ward’s Chinese Vole .............................................................................. 136 Anteliomys custos (Thomas, 1912) – Mountain Chinese Vole ......................................................................... 138 Anteliomys custos custos (Thomas, 1912) .............................................................................................................. 138 Anteliomys custos rubel us (G. M. Allen, 1924) .................................................................................................... 139 Anteliomys custos ninglangensis (Wang & Li, 2000).............................................................................................. 139 Anteliomys custos changsanensis (Wang & Yang, 2000) ....................................................................................... 139 SUBGENUS: Ermites S. Liu, Y. Liu, Guo et al., 2012 ................................................................................... 139 Anteliomys tarquinius (Thomas, 1912) – Sichuan Chinese Vole ..................................................................... 139 Anteliomys hintoni Osgood, 1932 – Hinton’s Chinese Vole ............................................................................ 141 Anteliomys hintoni hintoni (Osgood, 1932) .......................................................................................................... 142 Anteliomys hintoni jinyangensis (Liu, 2018) ........................................................................................................... 142 Anteliomys hintoni meiguensis (Liu, 2018) ............................................................................................................. 143 Anteliomys hintoni luojishanensis (Liu, 2018) ........................................................................................................ 143 iv TABLE OF CONTENTS. TRIBE: Arvicolini Gray, 1821 ..................................................................................................... 145 SUBTRIBE: Bramina Mil er & Gidley, 1918 .............................................................................. 145 GENUS: Ellobius Fischer, 1814 – Northern Mole Voles ............................................................................. 149 Ellobius talpinus (Pallas, 1770) – Common Mole Vole ................................................................................... 150 Ellobius talpinus talpinus (Pallas, 1770) ............................................................................................................... 151 El obius talpinus rufescens (Eversmann, 1870) .................................................................................................... 152 El obius talpinus kashtchenkoi Thomas, 1912 ...................................................................................................... 152 El obius talpinus transcaspiae Thomas, 1912........................................................................................................ 153 Ellobius talpinus orientalis G. M. Allen, 1924 ..................................................................................................... 153 El obius tancrei W. Blasius, 1884 – Eastern Mole Vole ................................................................................... 153 El obius tancrei tancrei W. Blasius, 1884 .............................................................................................................. 154 El obius tancrei fuscipes Thomas, 1909 ................................................................................................................. 155 Ellobius tancrei albicatus Thomas, 1912 ............................................................................................................... 155 El obius tancrei coenosus Thomas, 1912 ............................................................................................................... 155 Ellobius tancrei larvatus G. M. Allen, 1924 ......................................................................................................... 155 El obius tancrei alaicus Vorontsov, Liapunova, Zakarjan & Ivanov, 1969 ..................................................... 156 GENUS: Bramus Pomel, 1892 – Southern Mole Voles ................................................................................. 156 Bramus fuscocapil us (Blyth, 1843) – Afghan Mole Vole ................................................................................... 157 Bramus lutescens (Thomas, 1897) – Transcaucasian Mole Vole ...................................................................... 158 SUBTRIBE: Pliomyina Kretzoi, 1969 ........................................................................................ 161 GENUS: Dinaromys Kretzoi, 1955 – Dinaric Voles ....................................................................................... 161 Dinaromys bogdanovi (V. Martino & E. Martino, 1922) – Martino’s Dinaric Vole....................................... 166 Dinaromys bogdanovi bogdanovi (V. Martino & E. Martino, 1922) .................................................................... 166 Dinaromys bogdanovi grebenscikovi (V. Martino, 1934) ........................................................................................ 166 Dinaromys longipedis (Đulić & Vidinić, 1967) – Western Dinaric Vole ......................................................... 167 SUBTRIBE: Lagurina Kretzoi, 1955 .......................................................................................... 169 GENUS: Lagurus Gloger, 1841 – Steppe Lemmings..................................................................................... 170 Lagurus lagurus (Pallas, 1773) – Steppe Lemming ........................................................................................... 170 Lagurus lagurus lagurus (Pallas, 1773) .................................................................................................................. 173 Lagurus lagurus altorum Thomas, 1912 ............................................................................................................... 174 Lagurus lagurus aggressus Serebrennikov, 1929 .................................................................................................. 174 Lagurus lagurus abacanicus Serebrennikov, 1929 ................................................................................................ 175 Genus: Eolagurus Argyropulo, 1946 – Desert Lemmings .............................................................................. 175 Eolagurus luteus (Eversmann, 1840) – Yel ow Desert Lemming ................................................................... 176 Eolagurus przewalskii (Büchner, 1889) – Przewalski’s Desert Lemming ....................................................... 177 SUBTRIBE: Hyperacrina New Subtribe ................................................................................... 179 GENUS: Hyperacrius Miller, 1896 – Kashmir Voles ...................................................................................... 179 Hyperacrius wynnei (Blanford, 1881) – Murree Kashmir Vole ........................................................................ 181 Hyperacrius wynnei wynnei (Blanford, 1881) ........................................................................................................ 182 Hyperacrius wynnei traubi Phillips, 1969 .............................................................................................................. 182 Hyperacrius fertilis (True, 1894) – True's Kashmir Vole .................................................................................. 182 Hyperacrius fertilis fertilis (True, 1894) ................................................................................................................. 183 Hyperacrius fertilis brachelix (Miller, 1899) ........................................................................................................... 183 Hyperacrius fertilis zygomaticus Phillips, 1969 ....................................................................................................... 184 SUBTRIBE: Arvicolina Gray, 1821 ............................................................................................. 185 GENUS: Arvicola Lacépède, 1799 – Water Voles .......................................................................................... 185 TABLE OF CONTENTS v. Arvicola sapidus Miller, 1908 – Iberian Water Vole ......................................................................................... 187 Arvicola sapidus sapidus Miller, 1908 ................................................................................................................... 188 Arvicola sapidus tenebricus Miller, 1908 ................................................................................................................ 188 Arvicola persicus Filippi, 1865 – Persian Water Vole ........................................................................................ 188 Arvicola italicus Savi, 1838 – Italian Water Vole .............................................................................................. 191 Arvicola italicus italicus Savi, 1838 ........................................................................................................................ 193 Arvicola italicus destructor Savi, 1838 .................................................................................................................... 193 Arvicola amphibius (Linnæus, 1758) – Eurasian Water Vole ........................................................................... 193 SUBTRIBE: Microtina Rhoads, 1895......................................................................................... 199 GENUS: Chionomys Miller, 1908 – Snow Voles ............................................................................................. 200 SUBGENUS: Chionomys Miller, 1908 ............................................................................................................... 202 Chionomys nivalis (Martins 1842) – European Snow Vole .............................................................................. 202 SUBGENUS: Protochionomys new subgenus .................................................................................................... 205 Chionomys gud (Satunin, 1909) – Gudaur Snow Vole ...................................................................................... 206 Chionomys lasistanius (Neuhäuser, 1936) – Lazistan Snow Vole .................................................................... 208 Chionomys roberti (Thomas, 1906) – Robert’s Snow Vole ............................................................................... 209 GENUS: Proedromys Thomas, 1911 –Groove-toothed Voles ....................................................................... 211 Proedromys bedfordi Thomas, 1911 – Groove-toothed Vole ............................................................................ 211 GENUS: Mictomicrotus, new genus – Liangshan Voles .................................................................................. 213 Mictomicrotus liangshanensis (Liu, Sun, Zeng & Zhao, 2007) – Liangshan Vole ............................................ 213 GENUS: Volemys Zagorodnjuk, 1990 – Sichuan Voles ................................................................................ 215 Volemys mil icens (Thomas, 1911) – Common Sichuan Vole ......................................................................... 217 Volemys musseri (Lawrence, 1982) – Marie’s Sichuan Vole ............................................................................ 218 GENUS: Neodon Hodgson, 1849 – Scrub Voles ............................................................................................ 219 SUBGENUS: Nedon Hodgson, 1849 – Himalayan Scrub Voles ................................................................. 221 Neodon sikimensis Hodgson, 1849 – Sikkim Scrub Vole ................................................................................. 221 Neodon nepalensis Pradhan, Sharma, Sherchan et al., 2019 – Nepalese Scrub Vole....... ............................. 224 SUBGENUS: Phaiomys Blyth, 1862 – Thibetan Scrub Voles ....................................................................... 225 Neodon leucurus (Blyth, 1862) – Blyth’s Scrub Vole ......................................................................................... 227 Neodon fuscus (Büchner 1889) – Büchner’s Scrub Vole .................................................................................. 229 Neodon irene (Thomas, 1911) – Chinese Scrub Vole ....................................................................................... 230 Neodon irene irene (Thomas, 1911) ...................................................................................................................... 232 Neodon irene oniscus (Thomas, 1911) ................................................................................................................... 233 Neodon forresti Hinton, 1923 – Forrest’s Scrub Vole ....................................................................................... 233 Neodon linzhiensis Liu, Sun, Liu, Wang, Guo & Murphy, 2012 – Linzhi Scrub Vole ................................. 234 Neodon clarkei (Hinton, 1923) – Clarke’s Scrub Vole ..................................................................................... 235 Neodon medogensis Liu, Jin, Liu et al., 2017 – Medog Scrub Vole .................................................................. 237 Neodon nyalamensis Liu, Jin, Liu et al., 2017 – Nyalam Scrub Vole ............................................................... 238 GENUS: Alexandromys Ognev, 1914 – Grass Voles ...................................................................................... 239 SUBGENUS: Alexandromys Ognev, 1914 ....................................................................................................... 242 Alexandromys fortis (Büchner, 1889) – Reed Vole ............................................................................................ 242 Alexandromys fortis fortis (Büchner, 1889) .......................................................................................................... 245 Alexandromys fortis calamorum (Thomas, 1902) .................................................................................................. 246 Alexandromys fortis michnoi (Kastchenko, 1910) ................................................................................................ 246 Alexandromys fortis dolichocephalus (Mori, 1930) ................................................................................................. 246 Alexandromys fortis uliginosus (Jones & Jonson, 1955) ...................................................................................... 247 Alexandromys fortis fujianensis (Hong, 1981) ....................................................................................................... 247 Alexandromys sachalinensis (Vasin, 1955) – Sakhalin Grass Vole .................................................................... 247 Alexandromys maximowiczi (Schrenck, 1859) – Maximowicz’s Grass Vole ................................................. 248 Alexandromys maximowiczi maximowiczii (Schrenck, 1859) .............................................................................. 252 Alexandromys maximowiczi ungurensis (Kastschenko, 1913)............................................................................. 252 vi TABLE OF CONTENTS. Alexandromys mujanensis (Orlov & Kovalskaya, 1978) – Muya Grass Vole ................................................. 252 Alexandromys evoronensis (Kovalskaja & Sokolov, 1980) – Evoron Grass Vole ........................................... 253 Alexandromys mongolicus (Radde, 1861) – Mongolian Grass Vole .................................................................. 255 Alexandromys alpinus Lissovsky, Yatsentyuk, Petrova & Abramson, 2017 – Khangai Grass Vole .......... 257 Alexandromys middendorffii (Polyakov, 1881) – Middendorf’s Grass Vole .................................................... 258 Alexandromys middendorffii middendorffii (Poljakov, 1881) ................................................................................. 261 Alexandromys middendorffii ryphaeus (Heptner, 1948) ........................................................................................ 261 Alexandromys middendorffii hyperboreus (Vinogradov, 1933) .............................................................................. 261 Alexandromys shantaricus (Ognev 1929) – Gromov’s Grass Vole .................................................................. 262 Alexandromys shantaricus shantaricus Ognev, 1929 ............................................................................................. 263 Alexandromys shantaricus gromovi Vorontsov, Boeskorov, Lyapunova & Revin, 1988 ................................. 263 SUBGENUS: Oecomicrotus Rabeder, 1981 ....................................................................................................... 263 Alexandromys oeconomus (Pallas, 1776) –Tundra Grass Vole, Root Vole ...................................................... 263 Alexandromys limnophilus (Büchner, 1889) – Lacustrine Grass Vole ............................................................. 267 Alexandromys limnophilus limnophilus (Büchner, 1889) ...................................................................................... 269 Alexandromys limnophilus malygini (Courant et al., 1999) .................................................................................. 269 SUBGENUS: Yushanomys new subgenus ........................................................................................................ 269 Alexandromys kikuchi (Kuroda, 1920) – Taiwan Grass Vole ........................................................................ 270 Alexandromys montebel i (A. Milne Edwards, 1872) – Japanese Grass Vole ................................................. 272 GENUS: Lasiopodomys Lataste, 1887 – Hairy-footed Voles.......................................................................... 274 SUBGENUS: Lasiopodomys Lataste, 1887 ........................................................................................................ 276 Lasiopodomys brandti (Radde, 1861) – Yel ow (Brandt’s) Hairy-footed Vole .............................................. 276 Lasiopodomys brandti brandti (Radde, 1861) ...................................................................................................... 277 Lasiopodomys brandti hangaicus (Bannikov, 1948).............................................................................................. 278 SUBGENUS: Lemmimicrotus Tokuda, 1941 ..................................................................................................... 278 Lasiopodomys mandarinus (A. Milne Edwards, 1871) – Mandarin Hairy-footed Vole ................................. 278 Lasiopodomys mandarinus mandarinus (A. Milne-Edwards, 1871) ..................................................................... 279 Lasiopodomys mandarinus johannes (Thomas, 1910) ............................................................................................ 280 Lasiopodomys mandarinus faeceus (G. Allen, I924) ............................................................................................... 280 Lasiopodomys mandarinus kishidai (Mori, 1930) .................................................................................................. 280 Lasiopodomys mandarinus vinogradovi (Fetisov, 1936) ......................................................................................... 281 GENUS: Stenocranius Kashchenko, 1901 – Narrow-headed Voles ............................................................. 281 Stenocranius gregalis (Pallas, 1779) – Common Narrow-headed Vole ............................................................ 283 Stenocranius raddei (Polyakov, 1881) – Radde’s Narrow-headed Vole .......................................................... 288 GENUS: Microtus Schrank, 1798 – Grey Voles .............................................................................................. 288 SUBGENUS: Blanfordimys Argyropulo, 1933 ................................................................................................. 289 Microtus afghanus Thomas, 1912 – Afghan Vole .............................................................................................. 290 Microtus afghanus afghanus Thomas, 1912 ........................................................................................................... 292 Microtus afghanus balchanensis Heptner & Shukurov, 1950 .............................................................................. 293 Microtus afghanus dangarinensis Golenishchev & Sablina, 1991 ........................................................................ 293 Microtus bucharensis Vinogradov, 1930 – Bucharian Vole ............................................................................... 293 Microtus bucharensis bucharensis Vinogradov, 1930............................................................................................. 293 Microtus bucharensis davydovi Golenishchev & Sablina, 1991 ........................................................................... 294 Microtus yuldaschi (Severtsov, 1879) – Juniper Vole ......................................................................................... 295 Microtus yuldaschi yuldaschi (Severtsov, 1879) ..................................................................................................... 296 Microtus yuldaschi carruthersi Thomas, 1909 ........................................................................................................ 297 SUBGENUS: Euarvicola Acloque, 1900 – Field Voles .................................................................................. 297 Microtus agrestis (Linnæus, 1761) – Common Field Vole ................................................................................ 299 Microtus lavernedi (Crespon, 1844) – Mediterranean Field Vole ................................................................... 303 Microtus rozianus (Bocage, 1865) – Portugese Field Vole ............................................................................... 304 SUBGENUS: Iberomys Chaline, 1972 – Cabrera’s Voles ............................................................................... 305 Microtus cabrerae Thomas, 1906 – Cabrera’s Vole ............................................................................................ 305 TABLE OF CONTENTS vii. SUBGENUS: Terricola Fatio, 1867 – Pine voles ............................................................................................ 309 Microtus majori (Thomas, 1906) – Major’s Pine Vole ...................................................................................... 313 Microtus subterraneus (Sélys, 1836) – European Pine Vole .............................................................................. 315 Microtus fingeri (Neuhäuser, 1936) – Anatolian Pine Vole .............................................................................. 319 Microtus daghestanicus (Shidlovskiy, 1919) – Dagestan Pine Vole................................................................... 320 Microtus savi (Selys, 1838) – Common Savi’s Vole ......................................................................................... 323 Microtus savii savii (Selys, 1838) ........................................................................................................................... 324 Microtus savii tolfetanus Contoli, 2003 ................................................................................................................. 324 Microtus brachycercus (Lehmann, 1961) – Short-tailed Savi’s Vole .................................................................. 325 Microtus brachycercus brachycercus (Lehmann, 1961) ............................................................................................ 325 Microtus brachycercus niethammericus Contoli, 2003 ............................................................................................. 325 Microtus nebrodensis ( Minà-Palumbo, 1868) – Sicilian Savi’s Vole .................................................................. 325 Microtus duodecimcostatus (Sélys, 1839) – Mediterranean Pine Vole ................................................................ 328 Microtus lusitanicus Gerbe, 1879 – Lusitanian Pine Vole ................................................................................. 330 Microtus pyrenaicus (Sélys, 1847) – Pyrenean Pine Vole ................................................................................... 331 Microtus multiplex (Fatio, 1905) – Alpine Pine Vole ........................................................................................ 334 Microtus liechtensteini (Wettstein, 1927) – Liechtenstein’s Pine Vole ............................................................. 336 Microtus tatricus (Kratochvíl, 1952) – Carpathian Pine Vole .......................................................................... 337 Microtus tatricus tatricus (Kratochvíl, 1952) ........................................................................................................ 338 Microtus tatricus zykovi (Zagorodnyuk, 1989) .................................................................................................... 339 Microtus thomasi (Barrett-Hamilton, 1903) – Thomas’ Pine Vole.................................................................. 339 Microtus felteni ( Malec & Storch, 1963) – Balkan Pine Vole ........................................................................... 342 SUBGENUS: Microtus Schrank, 1798 – Grey Voles ..................................................................................... 343 Microtus arvalis (Pallas, 1779) – Common Grey Vole (Common Vole) ....................................................... 346 Microtus obscurus (Eversmann, 1841) – Altai Grey Vole ................................................................................. 351 Microtus rossiaemeridionalis Ognev, 1924 – East-European Grey Vole .......................................................... 354 Microtus mystacinus (Filippi, 1865) – Caspian Grey Vole ................................................................................. 358 Microtus kermanensis Roguin, 1988 – Kerman Grey Vole ............................................................................... 359 Microtus transcaspicus Satunin, 1905 – Transcaspian Grey Vole ..................................................................... 360 Microtus ilaeus Thomas, 1912 – Kyrgyz Grey Vole ......................................................................................... 363 Microtus ilaeus ilaeus Thomas, 1912 .................................................................................................................... 364 Microtus ilaeus igromovi Meyer & Golenishchev, 1996 ...................................................................................... 365 Microtus socialis (Pallas, 1773) – Common Social Vole ................................................................................... 368 Microtus socialis socialis (Pallas, 1773) .................................................................................................................. 369 Microtus socialis parvus Satunin, 1901 .................................................................................................................. 370 Microtus socialis satunini (Ognev, 1924) .............................................................................................................. 371 Microtus socialis gravesi Goodwin, 1934 .............................................................................................................. 371 Microtus socialis nikolajevi Ognev, 1950 ............................................................................................................... 372 Microtus socialis bogdoensis Wang & Ma, 1981 .................................................................................................... 372 Microtus socialis aristovi Golenishchev, 2002 ...................................................................................................... 372 Microtus socialis zaitsevi Golenishchev, 2002 ...................................................................................................... 373 Microtus anatolicus Kryštufek & Kefelioğlu, 2001 – Anatolian Social Vole .................................................. 373 Microtus irani Thomas, 1921 – Iranian Social Vole ......................................................................................... 374 Microtus irani irani Thomas, 1921 ....................................................................................................................... 377 Microtus irani schidlovskii Argyropulo, 1933 ....................................................................................................... 377 Microtus irani bateae Kretzoi, 1962 ...................................................................................................................... 377 Microtus irani karamani Kryštufek, Vohralík, Zima, Koubínová & Bužan, 2010 ........................................ 378 Microtus paradoxus (Ogneff & Heptner, 1928) – Khorasan (Kopetdag) Social Vole ................................. 378 Microtus guentheri (Danford & Alston, 1880) – Levant (Guenther’s) Social Vole ....................................... 379 Microtus mustersi Hinton, 1926 – Muster’s Social Vole ................................................................................... 382 Microtus hartingi Barrett-Hamilton, 1903 – Harting’s Social Vole ................................................................. 383 Microtus dogramacii Kefelioğlu & Kryštufek, 1999 – Dogramaci’s Social Vole ............................................ 386 viii TABLE OF CONTENTS. Microtus schelkovnikovi Satunin, 1907 – Schelkovnikov’s Vole ....................................................................... 388 Bibliographic list ........................................................................................................................ 391 Transliteration ..................................................................................................................................................... 391 Abbreviations ...................................................................................................................................................... 391 References .................................................................................................................................. 393 Appendix .....................................................................................................................................423 Zoobank registrations ................................................................................................................ 425 Index to the technical names ..................................................................................................... 427 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION B. Kryštufek & G. I. Shenbrot Preface Voles and lemmings (subfamily Arvicolinae) are the many other biological subdisciplines who work on a most specious and widely distributed rodents across the daily basis with various arvicoline species are frequently immense Palaearctic region, provided there is at least baffled by the taxonomic changes and discordant some available vegetation cover. They are keystone classifications used in different sources. The aim of this members and engineers of temperate, boreal and arctic review is to provide an up-to-date taxonomic review of ecosystems. Through their digging arvicolines aerate the group within the Palaearctic borders. In particular soil, increase groundwater recharge, and impact we are attempting to ensure continuity between the nutrient cycling, plant productivity and species earlier morphology-based taxonomies, karyology-based composition. These effects are further emphasised species delimitations and the current DNA-aided through grazing which promotes ecological succession phylogenetic reconstructions. and creates habitats for other species. By transmitting ample amounts of cel ulose and starch into proteins, This work provides a complete and independent list of arvicolines control the abundance of prey and predator Palaearctic voles and lemmings with descriptions, keys species. Although smal in size, they are large in the for identification, detailed distributional maps and basic transfer of energy between the trophic levels. taxonomic details al owing the user “to interpret intelligently and cautiously the results of taxonomists As one would have thought, arvicolines are frequently labour” (Corbet 1978:1). Although several recent used in various research endeavours of fundamental compilations have addressed the topic, we still believe and applied significance, including research on small- that the present work provides novel views. Truly, it is mammal population dynamics, reconstruction of the compilation but as we hope, a critical one, based on our impact of glacial-interglacial climatic dynamics on first-hand experiences with various arvicoline species, biodiversity and its survival in refugia, study of the assemblages and faunas throughout Europe and Asia evolution of metabolic rate and life-history strategies, gained during the last half century of our professional and understanding the neuroscience of social work. In 31 museums and collections across Europe, behaviour. Arvicolines are of interest as reservoirs of Asia and the USA, we examined well over 20,000 infectious disease and as pests to agriculture and voucher specimens, including 302 name bearing types forestry. As they are ubiquitous in many fossil and 43 syntypes representing a further 13 nominal taxa. assemblages, their fossilised remnants provide accurate Of the 128 species recognised in this review, we saw al biochronological information and are widely used as a except 4. Maps were derived from an expanded earlier proxy of environmental change. basis (Shenbrot & Krasnov 2005) which now contains 117,350 locality points. We studied literature on the The majority of arvicolines are r-selected, have a short topic, including original publications for nearly every generation time and high population turnover rate. taxonomic name published since 1758. And last, but They furthermore show high rates of mutation change not least, we discussed various issues of arvicoline and chromosomal rearrangements, evolve promptly taxonomy, zoogeography and biology with experts who and abound with cryptic species. The number of actively study particular groups. We have received recognised species nearly doubled in the last half- invaluable assistance from many experts and their century and has still not stabilised. Experts engaged in comments and suggestions were most helpful, though, medical zoology, epidemiology, biostratigraphy, as usual, the opinions and mistakes remain our own zooarchaeology, population ecology, biodiversity responsibility. conservation, museum collection management and 2 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION B. Kryštufek & G. I. Shenbrot Acknowledgements For access to specimens and help in collections, B. Herzegovina), Milan Paunović (Natural History Kryštufek thanks (abc): Oleg Akseev (Laboratory for Museum Belgrade, Serbia), Svetozar Petkovski Biomonitoring, Academy of Sciencies of Tatarstan (Macedonian Museum of Natural History, Skopje, Republic, Kazan, Russia), Hermann Ansorge North Macedonia), Alexandr A. Pozdnyakov (Institute (Senckenberg Museum für Naturkunde Görlitz, for Systematics and Ecology of Animals, Novosibirsk, Germany), †Kurt Bauer, Frank Zachos and Katharina Russia), Klara Stefen (Museum für Tierkunde, Dresden, Spreitzer (Natural History Museum, Vienna), Petr Germany), †Gerhard Storch, †Dieter Kock, Irina Ruf Benda (National Museum, Prague), Gábor Csorba and and Katrin Krohmann (Forschungsinstitut und Natur-Tamás Görföl (Hungarian Natural History Museum, Museum Senckenberg, Frankfurt am Main, Germany), Budapest), Aleksandra Davydova and Leonid L. Voyta Nikola Tvrtković (Mammal collection, Zagreb (Zoological Museum, St. Petersburg, Russia), Linda University, Croatia), Vladimir Vohralík (Department of Gordon, Darrin Lunde and Esther M. Langan Zoology, Charles University, Prague), and †Jan Zima (Smithsonian National Museum of Natural History, (Institute of Vertebrate Biology, Brno, Czech Washington D.C.), Paula Jenkins and Roberto Portela Republic). Mrs. Mojca Jernejc Kodrič provided Miguez (Natural History Museum, London), Rainer invaluable help with vouchers in the Slovenian Museum Hutterer (Zoologisches Forschungsinstitut und of Natural History. Museum Alexander Koenig, Bonn), Haluk Kefelioğlu (Ondokuz Myıs University, Samsun, Turkey), Richard We were fortunate to benefit from the experience of Kraft and Anneke van Heteren (Zoologische many who generously gave their time, provided Staatssammlung München, Germany), Irina additional information and helped with literature (abc): Kuznetsova (Institute of Plant and Animal Ecology, Erik Åhlander, Giovanni Amori, Natalya Abramson, Yekatarinburg, Russia), Shin-Ichiro Kawada (National Irina Bakloushinskaya, Anna Bannikova, Marina Museum of Nature and Science, Tokyo), Vladimir Baskevich, †Kurt Bauer, Gabriel Chişamera, Normand Lebedev and Nataliya Spasskaya (Zoological Museum Davis, Yulia Davydova, Maria Chiara Deflorian, of Moscow State Unievrsity, Moscow), Liang-Kong Lin Chistiane Denys, Nikolai E. Dokuchaiev, Feodor N. (National Museum of Natural Science, Taichung, Golenishchev, Barbara Herzig, Ivan Horáček, Masahiro Taiwan), Ahmad Mahmoudi (Rodentology Centre, A. Iwasa, Yakibumi Kaneko, †Dieter Kock, Dražen Ferdovsi University of Mashad, Pasteur Institute of Kotrošan, Irina Kuznetsova, Vladimir Lebedev, Iran, Akanlu Station and Urmia University, Urmia, Ahmad Mahmoudi, Vasily Malygin, Maria Mathias, Igor Iran), Verity L. Mathis (Florida Museum of Natural Pavlinov, Alexandr Pozdnyakov, Jeremy B. Searle, History, University of Florida, Gainesville, USA), Lutz †Gerhard Storch, Boris Sheftel, Katharina Spreitzer, Maul (Research Station of Quaternary Palaeontology Alexey Tesakov, Vladimir Vohralík, Igor Zagorodnyuk, Weimar, Germany), Frieder Mayer and Steffen Bock †Jan Zima, Tanya Zorenko, and Alexandr Zykov. (Zoologisches Museum, Humboldt Universität, Berlin), George Mitsainas (Zoological Museum, University of For translations from Japanese we thank Paul Patras, Greece), †Guy Musser and Eric Brothers Callomon, Masaharu Motokawa, and Takashi Yato. (American Museum of Natural History, New York), Some of the Chinese texts were translated by Shih-Wei Adam Nadachowski (Institute of Systematics and Chang and Kai He. We thank photographers who Experimental Zoology, Krakow, Poland), †Svetoslav generously al owed us to reproduce their photographs; Obratil (National Museum, Sarajevo, Bosnia and they are named in the figure captions. For arrangements 4 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. with photographers we thank Irina Bakloushinskaya, Vohralík (Prague), and Irena and †Jan Zima (Brno). At Yulia Davydova, Yulia Kropacheva, Nataliya V. various critical phases of this project, Franc Janžekovič Lopatina, Alexandr Pozdnyakov, Ole Jakob Sørensen, (University in Maribor) provided much needed support Johan Thissen, and Viktoria Vekhnik. Jan Hošek is to B.K. Particular thanks are to Rainer Hutterer for his gratefully acknowledged for the original drawings of continuing interest and support of this work. lemmings provided specifically for this book. This research received support from the SYNTHESYS During his protracted stays in collections abroad, B.K. Project http://www.synthesys.info/ (to B.K.) which enjoyed the warm hospitality of Yulia Davydova was financed by European Community Research (Yekaterinburg), Rainer Hutterer and Inge Bischoff Infrastructure Action under the FP7 Integrating (Bonn), Carol and †Gordon Kirkland (Shipensburg), Activities Programme. Further funding was provided Vasily Malygin (Moscow), Mary and Pat Morris (Ascot), by Slovenian Research Agency through research core Natalya and Alexandr Pozdnyakov (Novosibirsk), funding no. P1-0255 (B.K.). Masaharu and Mrs. Motokawa (Kyoto), Vladimir VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION B. Kryštufek & G. I. Shenbrot Taxonomy and nomenclature Taxonomy is usual y defined as the theory and practice additional information is in square brackets. References of identifying, describing, and arranging (classifying) to the original naming are provided for valid names, but organisms into taxonomic groups on the basis of their not for their junior synonyms and invalid names. Type relationships. A taxonomic system reflects, or should localities for all available names are shown on the reflect the evolutionary history of the group under species maps. study, which in turn is imperfectly known. Systems are based on the existing scientific facts, other hypotheses Family-group names and even intuition and are not the final truth. They are hypotheses of genuine evolutionary relationships and as Prior to 1990, the name Microtinae Miller, 1896, was such are subject to further testing, modification or usually used for voles and lemmings (Figure 1) but has rejection. Taxonomic systems are continuously now been replaced by Arvicolinae Gray, 1821, which changing as our understanding of phylogenetics has absolute seniority. Some authors ranked the group advances. as a family in its own right (Arvicolidae; Kretzoi 1955, Chaline et al. 1977, Honacki et al. 1982, Panteleyev An integral part of taxonomy is nomenclature, the 1998, Martin 2007). arrangement of principles regarding creating and using scientific names to promote their stability and In the late 19th century, Miller (1896) proposed a universality. The usage of a particular Linnean name is division of the subfamily into two supergeneric groups the consequence of the nomenclatural history of the (Lemmi and Microti), and shortly afterwards Méhely name and regulations available through the (1914) advocated an alternative dichotomy into International Code on Zoological Nomenclature Fibrinae and Microtinae. Simpson (1945) proposed (hereinafter referred to as the Code). Within arvicolines, three such groups (Lemmini, Microtini and Ellobiini) one is confronted with names at three hierarchical while Musser & Carleton (2005) recognised ten tribes ranks: the species group names (species and of which eight have Palaearctic representatives. Relying subspecies), the genus-group names (genera and on recent phylogenetic reconstructions (particularly subgenera), and the family-group names (the subfamily, Steppan & Schenk 2017) we classify voles and tribes and subtribes). The nomenclature at each of these lemmings into five tribes (see below). Main sources for ranks was regulated by the 4th edition of the Code the family-group names are McKenna & Bell (1997) and (ICZN 1999) to which we strictly adhere. Musser & Carleton (2005). Family-group names are created from generic names by adding an extension: - Authorities for taxonomic names with the year of idea (family), -inae (subfamily), -ini (tribe), and –ina publication are given for all Palaearctic taxa, regardless (subtribe). of their rank. Contrary to reference quotes in the text which have no comma between the author(s) name(s) Genera and Species and the year of publication (e.g. Ognev 1929), the name (or names) of a taxonomic authority (authorities) and the year are separated by a comma (e.g. Alexandromys In the Linnean taxonomy and nomenclature, the generic Ognev, 1914). Type localities are provided for all valid (genus) name is the first name of a binominal name species and subspecies. If quoted from the original (binomen). DNA-based phylogenetics brought much source, the type locality is in quotation marks and any clarity into generic classification, however, molecular 6 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. clusters which are ranked as distinct genera are not makeups and occupy different niches. A hypothesis as always definable morphological y. We have recognised to whether two sister lineages are conspecific or not can 26 genera, which is a higher number compared to other be tested in parts of their overlapping (sympatric) revisions over the last century. Various authors writing ranges. The confusion begins with the extension of the on the topic after 1904 classified Palaearctic Arvicolinae small-scale reality over space and evolutionary time, i.e. in 14–23 genera (median=17; Figure 1). We frequently with the al ochronic and al opatric populations. When in use a subgeneric rank which was avoided in some earlier doubt, we compared data from the same marker reviews (e.g. Corbet 1978) but is gaining attention since between different pairs of sister species and the advent of molecular phylogenetics (Teta 2019). extrapolated taxonomic inferences from better-studied cases. We have made every attempt to examine al the Species is the central category in the majority of available information from different operational criteria. biological sub-disciplines. It therefore comes as a Further issues in species delimitation are posed by the surprise that biologists frequently disagree on how to limited hybridisation in overlapping (parapatric) parts of define a species and how to delimit two closely related species’ ranges. Documented cases of parapatric species (de Queiroz 2007). In our pragmatic view, hybridisation are few in arvicolines, the zone of range species are lineages which maintain their unique genetic overlap is usually narrow and the gene flow is frequently Figure 1: Number of species (∆) and genera (▲) of voles and lemmings (subfamily Arvicolinae) recognised in the Palaearctic region by various authors since 1904. Bold upper case letters indicate the family-group name used by the authors: M – Microtinae, A – Arvicolinae (asterisk indicates a family rank Arvicolidae). Sources: 1–Trouessart (1904), 2–El erman (1941), 3–El erman & Morrison-Scott (1951), 4–Gromov & Polyakov (1977), 5–Corbet (1978), 6–Corbet & Hil (1980), 7–Honacki et al. (1982), 8–Corbet & Hil (1986), 9–Musser & Carleton (1993), 10–Pavlinov et al. (1995), 11–Panteleyev (1998), 12–Pavlinov (2003), 13–Musser & Carleton (2005), 14–Shenbrot & Krasnov (2005), 15–Pavlinov (2006), 16–Pardiñas et al. (2017), 17–Burgin et al. (2020), 18–this review. Taxonomy and nomenclature 7. restricted or nil. Most of our current knowledge on that the deficiencies attributed to the subspecies system species diversity in Arvicolinae relies on morphological, are more a matter of excess and misuse in the chromosomal and mitochondrial (mt) DNA variation, application of the concept, rather than of the concept and on cross-breeding trials. Phylogenetic itself. In any case, subspecies remains in use as the reconstructions using nuclear DNA are sorely needed lowest category recognised in formal taxonomy and is for testing the validity of recently recognised cryptic sanctioned by the International Code of Zoological species. Nomenclature. At least 16 taxonomic lists of Palaearctic arvicolines As was common with mammals in general, subspecies have been published since Trouessart (1904) which in arvicolines were also erected on morphological recognised between 69 and 165 (median=100) species. evidence, frequently from a single population and The Nearctic muskrat Ondatra zibethicus which since diagnosed by a smal number of traits. Variation was 1905 has repeatedly been introduced from North only exceptional y quantified and mapped to discern the America and is now widespread in Europe and boreal pattern for subsequent classification. Various Asia (Pardiñas et al. 2017) is not considered. As evident subspecific forms are based on slight differences with from Figure 1, compilations were rare during the first no proof of discontinuity (cf. the purported subspecific half of the 20th century and the number of recognised diagnoses in Niethammer & Krapp 1982, and Gromov species varied dramatical y between sources. El erman & & Erbajeva 1995). DNA-based phylogeographic Morrison-Scott (1951), who strictly adhered to a assessments on the other hand repeatedly retrieved polytypic species concept, recognised less species than geographic structuring similar to the one stipulated by any other review. Although they are frequently blamed the advocates of a polytypic species concept evidencing for the “taxonomic inertia” which followed during the that subspecies are potential y real and meaningful. second half of the 20th century, their species list laid the Little has been done in Palaearctic arvicolines to link groundwork for the steady taxonomic progress which phylogeographic lineages with traditional subspecies in has followed from the 1950s right up to now. order to build robust subspecific taxonomies. In this review we did not entirely reject the subspecies but were Main sources for the genus- and species-group names still cautious in formalising subspecies. are Trouessart (1897, 1904, 1910), Palmer (1904), Miller (1912a), Allen (1940), Ellerman (1941), Ognev (1948, 1950), Ellerman & Morrison-Scott (1951), Corbet (1978), Pavlinov & Rossolimo (1987), Kretzoi & Kretzoi (2000), and Musser & Carleton (2005). Subspecies Since the late 19th century mammalogists have applied subspecies names to define infraspecific geographic variation. The practice gained popularity with the acceptance of the polytypic species concept but ever since the 1950s was subject to repeated attack. At present, the situation with trinomial taxonomy is ambiguous. Subspecies are rejected by many claiming that the rank is imaginary and, as such inefficient and superfluous for reference purposes. Opponents argue 8 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION B. Kryštufek & G. I. Shenbrot Geographic setting Voles and lemmings are a Holarctic group. Of the 161 in their entirety. A single vole is endemic to the species listed in Pardiñas et al. (2017), only four are Palaearctic Africa. Transberingian, while the remaining are exclusively Nearctic (38 species) or Palaearctic endemics (119 Distributional ranges of 128 Palaearctic arvicolines species). In the past, the Transberingian species were cover surface areas between 334–17.5 million km2, i.e. believed to be more numerous and at some stage the a difference of more than four orders of magnitude. fol owing species pairs were considered as Frequency distribution is heavily skewed towards conspecifics: Microtus arvalis (Palaearctic) – M. montanus small areas (mean=1,088,561 km2, median=97,719 (Ellerman 1941), M. agrestis – M. pennsylvanicus, km2) and half of all ranges measure 26,000–517,000 Stenocranius gregalis – Microtus miurus, and Clethrionomys km2. glareolus – C. gapperi. Arvicolines transgress the southern Holarctic border in both continents and Arvicolines are better at conserving heat than in several genera are predominantly or exclusively dissipating it, hence they are poorly equipped to Oriental ( Hyperacrius, Caryomys, Eothenomys, Anteliomys). thermoregulate at high ambient temperatures. Despite this, we covered the Euro-Asiatic arvicolines Unsurprisingly, throughout the Holarctic they are the Figure 2: Species density of Palaearctic voles and lemmings. The darker the colour, the higher the number of species per unit area. 10 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. most abundant in terms of species and individuals in patches and frequently occupy high elevations. Along boreal and northern temperate regions. Few species the elevational gradient they range from below sea occupy semideserts and the eastern Palaearctic true level (–20 m) to 6,140 m, i.e. they ascend higher than deserts; voles are however absent from deserts in the any other rodent. One half of all ranges are at an west (Figure 2). Along the southern distributional altitude of 545–2,322 m. border, arvicolines search for shaded or wet (marshy) VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION B. Kryštufek & G. I. Shenbrot Characteristics of Voles and Lemmings Figure 3: Representative genera of Palaearctic voles and lemmings. Art Jan Hošek. Used with permission of the Science and Research Centre Koper. 12 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. External appearance The majority of arvicolines are of smal size. Body form is robust and short-tailed. Tail is usually shorter than ½ of head and body and tapers towards the pointed tip; its cross section is circular. Head is large with a bluntly rounded muzzle; eyes are small. Limbs are powerful and although moderately long, they are hidden in the integument of the trunk, hence giving a short-legged appearance (Figure 3). Hind feet are plantigrade and usual y longer than the digitigrade fore feet which in turn tend to be broader. The feet each have 5 digits but the thumb is always distinctly smaller and usually reduced to a mere vestige. Figure 4: The diastemal palate in Microtus arvalis as viewed from below. Skin derivatives The auricle is typically small to moderately large, rounded and rather concealed in the fur. The lateral The rhinarium, a hairless and specialised skin facies is usually structured with helicis, plica principalis surrounding the external openings of the nostrils (pinna), and antitragus; the prominence of the tragus (external nares), is of general murine type. The dorsal varies (Figure 5). In Dicrostonyx and Bramina, the ear is and ventral margins of nares are swollen forming the reduced to a small projection around the meatus (Figure dorsum (above the nostrils), the infranarial region 118g). (below each nostril), the paired alae nasi (on the flanks of nostrils), and the internarial area (between nostrils); the internarial region is medially divided by a shallow sulcus (Figures 13c & 119). Some authors (Ognev 1948, Gromov & Polyakov 1977) denote the dorsum and the infranarial area as upper (superior) and lower (inferior) allae nasi (nasalis), respectively. Towards the upper lip, the infranarial area continues as the medial cleft (philtrum). Rhinarium is situated on the tip of the snout and comparatively high above the upper incisors but the distance is shorter in fossorial voles (Vinogradov 1926a, Brown 1972). The lips are furred and their lobes, Figure 5: Left auricle in Clethrionomys glareolus (left) and along with the medio-ventral infoldings fill the oral Microtus hartingi (right). Not to scale. cavity between the incisors and molars. The hypertrophied incisors are seen from the outside (cf. Digits are equipped with curved and laterally Figure 118h) however the entrance to the cavity is compressed claws; the thumb has a smal claw or its tightly closed by the labial lobes (Figure 4). The lobes rudiment, a flat nail. The claws are narrower, longer and are comparatively poorly developed in lemmings sharper in climbing voles (e.g. Clethrionoyms, Chionomys, (Dicrostonychini and Lemmini) and in Clethrionomyini Dinaromys) and broader, shorter and blunter in fossorial but come close together or even meet in Prometheomys species. The front claws are frequently longer and may and in the majority of Arvicolini. In Bramina the lobes undergo various changes. They are much elongated in fuse to each other across the mid-line (Vinogradov Prometheomys (Figure 14), and peculiarly modified in 1926a,b). The palate is covered by a mucous membrane Dicrostonyx (Figure 19). The fore feet have 5 palmar pads which forms transverse ridges. Usual y, there are 3 in nearly al species; pads are reduced to 4 in Myopus and diastemal and 4–6 inter-molar ridges. are effectively absent in Dicrostonyx, Lemmus, and Characteristics of Voles and Lemmings 13. Eolagurus. Typicaly, there are 6 plantar pads on the hind winter (Figures 24 & 81). Moult is of sublateral type, feet (e.g. Figure 49) but the lateral metatarsal pad is with replacement of hair starting ventro-laterally and frequently absent, hence giving a count of 5 pads (e.g. progressing medio-ventrally and dorsally (Kryltzov Figure 204). Number of pads frequently varies between 1964). 5 and 6 even within the same species although one or the other count strongly prevails. In species which have On the head are long and coarse tactile hairs, the been studied more in detail, asymmetry was detected in whiskers (vibrissae). Mystacial vibrissae ( vibrissae the same individual with different counts of pads on the mystaciales) as the longest and most prominent are left and right soles (e.g. Alexandromys). Lagurus has only arranged in several rows on the snout. Further clusters 4 small plantar pads (Figure 138a) and in Dicrostonyx, of vibrissae are positioned around mouth and on the Lemmus and Eolagurus the vestiges of pads are entirely chin (Sokolov & Kulikov 1987). Whiskers are the concealed under dense hairs (Figures 25a & 138b). longest in voles living among rocks and the shortest in fossorial species. All voles are furred. The hair densely covers the entire body except the auricle, the nasal pad, the distal portion Voles and lemmings have sebaceous glands which are of limbs and the tail. The tail is covered with scaly distributed al over the body and connect to hair annulations that are partly or ful y concealed by stiff fol icles. Larger sebaceous glands are organised as pads hairs; terminal hairs normally form a tuft (pencil) of situated on the cheeks (cheek gland) and in the variable length and density (Figures 28, 48 & 241). The posterior part of the body (postero-lateral glands). fur is of a simple structure. It consists of dense and Position of the postero-lateral glands is group-shorter underfur and of longer and stiffer contour characteristic and was used in taxonomy as far back as (guard) hairs. Fossorial voles normally have a mole-like Miller (1896). These glands produce a waxy (oily) pelage of short and dense fur with guard hairs not much excretion and are frequently sparsely haired or entirely longer than the underfur. Guard hairs are coarse and devoid of hair (Wallin 1967, Clarke & Frearson 1972). protruding on the posterior back of aquatic voles. Hair Postero-lateral glands can be present in one or both bases are nearly invariably slate and the fur is general y sexes (usually in old males) and are not seen at all times a shade of brown with blackish, buff, rusty, or yel owish (Quay 1968). There can be a single gland (caudal and tints. Light or black tips of longer stiff hairs give a rump glands) situated in the sagittal plane, or two grizzled appearance which is characteristic for many symmetrical and laterally placed glands (flank and hip species. Voles from humid habitats tend to be darker glands; Figure 6a) (Quay 1968). The caudal gland is and those from arid regions are more buff. A high present in Dicrostonyx, the rump gland in Lemmus and proportion of black individuals is typical of certain Myopus, the hip glands in Microtus (reported in the riparian populations of Arvicola amphibius and for subgenera Microtus, Terricola, and Euarvicola), fossorial voles. Voles occupying rocky environments Alexandromys, and Lasiopodomys, and the flank glands in ( Alticola, Dinaromys, Chionomys) are frequently grey. Clethrionomys, Alticola, Craseomys, Eothenomys, Eolagurs, Pelage is monochromatic and the bel y is lighter and Dinaromys, Arvicola, Neodon, Stenocranius, and Chionomys greyer than the back; clear demarcation along the flanks (Quay 1968, Lehmann 1969, Claussen 1975). is rare. Some voles ( Lemmus, Dicrostonyx, Lagurus, Posterolateral glands are absent in Lagurus (Kratochvíl Stenocranius) have a black spinal (mid-dorsal) stripe. 1962) and Bramina (Quay 1968). Subspecies of Lemmus lemmus display blotches of bright and dull fur (Figures 26a & 33), matching certain Tarsal (Meibomian) glands are modified sebaceous environments at certain times, e.g. birch woods in glands situated in both eyelids of many mammals, spring and subalpine tundra during autumn. The rich including arvicolines. Although still imperfectly known, colouration can be aposematic (in combination with variation in their numbers associates with taxonomy. aggressive behaviour), protective (cryptic), or a mixture The combined number of tarsal glands in the upper and of both (Andersson 2015). Dicrostonyx and Aschizomys lower eyelids is high in Dicrostonychini (14–29), show seasonal polyphenism having white pelage during Lemmini (18–27), Clethrionomyini (6–25; usually >15) and Lagurina (21–26), but low in Arvicolina (3–11) and 14 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. Microtina (1–14; usually <10) (Quay 1954, Dearden El obius). A shal ow terminal crater frequently has 1959, Hrabě 1977, 1978, 1979). fingerlike processes. When not erect the penis is folded caudad and the glans is turned backward. Situated in the glans penis is a heterotopic bone cal ed the baculum ( os penis or os priapi). Its development is highly variable among species and its adaptive value is controversial. Because its morphology general y varies considerably between species but remains fairly constant within species, the baculum was frequently included in taxonomic studies. The arvicoline baculum is approximately 0.8–1.2-times as long as the glans and consists of a proximal shaft (proximal baculum, stalk) and a distal baculum (trident). The proximal baculum is dorsoventral y flattened and has an expanded base (Figures 62, 130, 159 & 265). The trident consists of three-pronged finger-like processes (digits) attached to the distal end of the proximal bone. The distal baculum Figure 6: Schematic depiction of integumental structures in voles and lemmings: a–position of different types of the can either be cartilaginous or osseous. Osseous postero-lateral glands (nomenclature fol ows Quay 1968); b–a processes consist of dorso-ventral y flattened medial complete set of mammary glands. process and two lateral processes which are joined by cartilage. Distal processes are ankylosed to the distal Female Palaearctic voles and lemmings have 4, 6 or 8 end of the shaft, either firmly or loosely. Shape of the nipples. Niethammer (1972) interpreted 8 nipples (2 baculum changes with age (Anderson 1960, Hooper & inguinal and 2 pectoral pairs; Figure 6b) as the primitive Hart 1962, Liu et al. 2017, Yato & Motokawa 2021). condition in the subfamily. Eight nipples are present in all Palaearctic tribes; Clethrionomyini and Arvicolini Sperm head also have 4 or 6 nipples. In such cases, both inguinal pairs are always present, except in Bramina. Bramina (6 Morphology of the sperm head proved useful in nipples) are unique for retaining both pectoral pairs but distinguishing sibling species of voles, hence we include losing an inguinal pair; an identical situation is known this information when available. The head is one of the in the Nearctic Microtus guatemalensis and M. ochrogaster two component parts of the mammalian gamete (Niethammer 1972). Liu et al. (2018) report 1 pectoral (spermatozoon); the other one is the tail. The head is and 1 inguinal pair for Eothenomys (4 nipples) which flattened and asymmetrical. It contains a nucleus contradicts Hinton (1923:147); this is typical of the (postacrosomal region sensu Fawcett 1975) with a Nearctic Microtus mexicanus. Further combinations of haploid set of chromosomes. Overlying the nucleus is nipples were observed in Nearctic voles, along with up the acrosome (acrosomal cap or apical segment) of to 10 nipples in Ondatra (Niethammer 1972). Ognev variable shape. Aksenova (1978) distinguished three (1950) reported 10 nipples for Lasiopodomys (as Phaiomys) main types of sperm head in arvicolines: (i) the but this is likely erroneous (cf. Allen 1940). Number of acrosome is hook-shaped and caudal y flexed (the head nipples can vary intraspecifically (e.g. in Craseomys smithi is falciform); (ii) the acrosome is conical and placed on and some Terricola) and is rarely asymmetric in the same the apex (the head is semi-oval); (iii) the acrosome is individual (cf. Meyer et al. 1996). apical and submerged into the nucleus. Penis and baculum Voles have a simple barrel-shaped glans with a diameter accounting for 50–75% of the length (broader in Characteristics of Voles and Lemmings 15. Figure 7: Lateral views of arvicoline skul (top) and mandible (bottom). Abbreviations: infraorb.–infraorbital; for.–foramen; M–molar; proc.–process; temp.–temporal. Figure 8: Arvicoline skul in dorsal (left) and ventral (right) views. Only half of the skul is shown. 16 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. Skul can be distinguished (Figure 9), despite various intermediary stages (Hinton 1926a, Pozdnyakov 2008) Skull is massive with a short rostrum and straight dorsal (Figure 10). In the Clethrionomyini type, the palate profile (Figures 7,8). Nasals are short and do not usually terminates posteriorly as a simple shelf. The postero-overtop the anterior-most point of the rostrum. lateral pits lie below (in fact, dorsal to) the palate level Masseteric (zygomatic) plate is broad, situated and open directly to choanae. The medial edges of pits transversely or obliquely to the sagittal plane; usual y do not communicate with the shelf and its infraorbital foramen is widened above for transmission medial spine (“nasal spine” of Hinton 1926a), when the of the enlarged medial masseter; its ventral portion is latter is present. In the Arvicolini type, the medial spine slit-like and obliterates in Bramina. Zygomatic arches extends posteriorly and merges with the medial edges are heavy and conspicuously broad in the jugal region. of pits to form a sloping septum on each side of the Zygomatic width usually accounts for 55–60% of the mesopterygoid vacuity. The septum can be broad, short skull length and extreme shapes are rare. The skull is and ill-defined or long, narrow and prominent, or may excessively narrowed in Stenocranius and widened in assume an intermediate structure. Messopterygoid fossa Bramina. The braincase, which is commonly rather extends between the last molars, while the postpalatine deep, is flattened in some rock-dwelling voles, reaching and parapterygoid fossae are absent in the majority of the extreme in Alticola strelzovi. The interorbital region is species. narrow and the supratemporal ridges merge and form an interorbital crest in adults of some species. The mandible consists of a horizontal corpus Anterolateral margin of squamosal bone has a (horizontal ramus; corpus mandibulae) and vertical ramus prominent postorbital crest or process for attachment ( ramus mandibulae) with 3 processes: coronoid, articular, of anterior temporal muscle. Parietal and interparietal and angular processes (Figure 8). The articular process bones are typical y large, but powerful temporal ridges is usually set at an angle of 125–130o against the may restrict them. The ridges usually diverge from horizontal ramus. Two prominent ridges on the labial behind the interorbital region and reach the maximal surface of the mandible serve as attachments for major lateral expansion at the plane of glenoid fossa; masseteric muscle and are consequently known as posteriorly, they may converge, turning outwardly again masseteric ridges (crests). They converge on the corpus at the level of the interparietal bone. The occipital at the level of M1. region is either truncated or sharply sloped. Auditory bul ae tend to be smal in fossorial and amphibious Dentition voles and large in open-terrain species. The mastoid portion is sometimes inflated. The wal s of the bul ae Al arvicolines have 1 incisor and 3 molars on both the are thin with no spongy tissues in Clethrionomyini, left and right side of the upper and lower jaws (Figure Pliomyina, and Hyperactina. In the majority of voles the 8), hence the total number of teeth is 16. The dentition wal s of the bul ae are spongy and the middle ear cavity is monophyodont. Incisors and molars are separated by is filled to varying degrees with ossified threads. diastema which in Palaearctic taxa is always longer than Anterior palatal (incisive) foramina are moderately long the molar row. Incisors grow from persistent pulps and (not reaching the level of M1); in fossorial forms, have the front surface coated with enamel. This leaves foramina are frequently shortened and narrowed into a the dentine naked behind, resulting in markedly unequal slit. A well-marked groove extends from the posterior wear between the two surfaces which preserves a chisel end of each incisive foramen back to the maxil o- point to the crown of the incisors. Typical y, they are palatine suture or beyond, pass under the postero- broad and smooth with a faint groove in some genera. lateral bridges and reach the postero-lateral pit (post- The enamel on the front surface is usual y stained palatine foramen; fossa palatina lateralis). yel ow to orange. The upper incisors are proodont in several fossorial representatives but are orthodont in The structure of the posterior palate demonstrates a the majority of species. The upper incisors are strongly significant taxonomic character. The two main palates curved and pass backward into the maxillary to Characteristics of Voles and Lemmings 17. terminate in front of M1. The alveolar sheath of the surrounded by transverse loops in which dentine fields upper incisors extends further back in El obius, extend across the tooth (Figure 11). Each lobe, cap or terminating on the hard palate mesial to molars. The triangle is formed by dentine which is bounded lower incisors are longer and less curved. With respect external y by a sheet of enamel. The occlusal surface to their length and position in the mandibular corpus, 2 dentine shows shal ow concavities representing sites of main types can be distinguished. In the lemming type, morphologically irregular dentine (reparative dentine) the alveolar portion of the incisor is positioned lingually formed in response to irritations (Phillips & Oxberry with respect to the molar row and terminates at the 1972). The enamel-covered sides of the crown form a alveolar capsule below M3. In the vole type, the incisor series of anticlines (salient angles) with the synclines (re-passes under M2–M3 from the lingual side to the labial entrant folds, infoldings) lying in-between. Although side and ascends into the condylar process where it lingual and buccal re-entrants are roughly equal in terminates in a wel -marked bulge ( processus alveolaris) depth, the outer (labial) triangles are smaller than the (Hinton 1926a). This dissimilarity results from different inner (lingual) in many genera. Terminal angles on M3 timing in the development of the lower incisor and M3. and M1 are either acute or obtuse. In most voles, In the lemming type, the development of M3 is cement is present in the synclines. Triangles are accelerated and blocks the protrusion of the incisor classified as either opened (enamel of a re-entrant angle towards the articular process. In the vole type, the nearly or completely meets the opposing re-entrant growth of the incisor is advanced with respect to M3, angle) or closed (the two re-entrant angles are separate). causing a lingual shift of the molar alveolus (Štĕrba & Míšek 1982, Borodin 2014). Upper molars consist of the anterior lobe (AL) and variable number of triangles (T). There are usually 4 Molars are extremel y hypsodont, attaining arhizodont triangles on the 1st upper molar (M1) and 3 triangles on hypselodoncy (Renvoisé & Michon 2014) in most the 2nd upper molar (M2). The 3rd upper molar (M3) has clades. They are mesiodistal y long, angular and consist a variable number of triangles and terminates with the of multiple prismatic elements. The 1st molar is always posterior cap (PC; posterior prism or heel). The 1st the longest and the remaining molars are of lower molar (M1) is the most complex and most approximately the same length. Length proportions in frequently used in taxonomy. Its posterior part is a the great majority of arvicolines (M2/M1=0.70; trigonid-talonid complex (TTC) which consists of the M3/M1=0.26) differ from those in remaining Muroidea. posterior lobe (PL) and 3 triangles. Except for few (Renvoisé et al. 2009). exceptions ( Prometheomys, Ellobius), the TTC is invariant across the subfamily. The anteroconid complex (ACC) The pulp cavities remain open (arhizodont molars) for is positioned anterior to the TTC and carries the the whole lifespan in the majority extant clades except anterior cap (AC) and a variable number of triangles. for Prometheomys, Dinaromys, Bramina, and some The 2nd (M2) and the 3rd (M3) lower molars are of a Clethrionomyina which retain rhizodont condition and simple structure, each consisting of a PL and four develop roots with advanced age. Development of triangles which frequently merge into transverse loops. roots can be highly variable even within the species (see Outer triangles on M3 are usually rudimentary (Meulen introduction to Clethrionomyini). Weekly rate of molar 1973, Semken & Wallace 2002). The most variable growth is 0.4–0.5 mm in Lagurus lagurus, 0.5–0.6 mm in sections of dentition are the posterior part in M3 and Alexandromys fortis, 0.6–0.7 mm in Lasiopodomys the anterior part of M1. Molar pattern is conveniently mandarinus, 0.8–0.9 mm in Dicrostonys torquatus and 1.0– used in taxonomy and distinct morphotypes may have 1.1 mm in Alticola argentatus. The entire molar crown is diagnostic value. On the other hand, there is wide rebuilt between 6–12 months, depending on the group occurrence of homologous variability across species (Koenigswald & Golenishev 1979). The grinding (Angermann 1974). Asymmetry is also common; e.g. in surfaces are flat, composed of alternating dental 10 species of Arvicolini, Kovaleva et al. (2019) found triangles which are arranged in two paral el series and 27.7% of individuals with an asymmetric M1. 18 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. Figure 9: The main types of the palate in Arvicolinae rodents: a–Clethrionomyini type (Alticola albicauda); b–Arvicolini type (Microtus montebelli). Figure 10: Posterior hard palate in main groups of Arvicolinae: a–Prometheomys schaposchnikowi (tribe Prometheomyini); b–Dicrostonyx torquatus (tribe Dicrostonychini); c–Lemmus nigripes (tribe Lemmini); d– Caryomys inez (Eothenomyina new subtribe, tribe Clethrionomyini); e–El obius tancrei (subtribe Bramina); f– Hyperacrius wynnei (Hyperacrina new subtribe); g–Eolagurus luteus (subtribe Lagurina); h–Dinaromys bogdanovi (subtribe Pliomyina). Subtribes e–h are classified into the tribe Arvicolini. Morphological structures are explained in Figure 9; o.f.–oval foramen. Characteristics of Voles and Lemmings 19. The molars assume an adult pattern early in postnatal Upper molars consist of the anterior lobe (AL) and ontogenesis, e.g. in Stenocranius gregalis at the age of 1 variable number of triangles (T). There are usually 4 month (Markova et al. 2013). triangles on the 1st upper molar (M1) and 3 triangles on the 2nd upper molar (M2). The 3rd upper molar (M3) has Molars are extremel y hypsodont, attaining arhizodont a variable number of triangles and terminates with the hypselodoncy (Renvoisé & Michon 2014) in most posterior cap (PC; posterior prism or heel). The 1st clades. They are mesiodistal y long, angular and consist lower molar (M1) is the most complex and most of multiple prismatic elements. The 1st molar is always frequently used in taxonomy. Its posterior part is a the longest and the remaining molars are of trigonid-talonid complex (TTC) which consists of the approximately the same length. Length proportions in posterior lobe (PL) and 3 triangles. Except for few the great majority of arvicolines (M2/M1=0.70; exceptions ( Prometheomys, Ellobius), the TTC is invariant M3/M1=0.26) differ from those in remaining Muroidea. across the subfamily. The anteroconid complex (ACC) (Renvoisé et al. 2009). is positioned anterior to the TTC and carries the anterior cap (AC) and a variable number of triangles. The pulp cavities remain open (arhizodont molars) for The 2nd (M2) and the 3rd (M3) lower molars are of a the whole lifespan in the majority extant clades except simple structure, each consisting of a PL and four for Prometheomys, Dinaromys, Bramina, and some triangles which frequently merge into transverse loops. Clethrionomyina which retain rhizodont condition and Outer triangles on M3 are usually rudimentary (Meulen develop roots with advanced age. Development of 1973, Semken & Wallace 2002). The most variable roots can be highly variable even within the species (see sections of dentition are the posterior part in M3 and introduction to Clethrionomyini). Weekly rate of molar the anterior part of M1. Molar pattern is conveniently growth is 0.4–0.5 mm in Lagurus lagurus, 0.5–0.6 mm in used in taxonomy and distinct morphotypes may have Alexandromys fortis, 0.6–0.7 mm in Lasiopodomys diagnostic value. On the other hand, there is wide mandarinus, 0.8–0.9 mm in Dicrostonys torquatus and 1.0– occurrence of homologous variability across species 1.1 mm in Alticola argentatus. The entire molar crown is (Angermann 1974). Asymmetry is also common; e.g. in rebuilt between 6–12 months, depending on the group 10 species of Arvicolini, Kovaleva et al. (2019) found (Koenigswald & Golenishev 1979). The grinding 27.7% of individuals with an asymmetric M1. The surfaces are flat, composed of alternating dental molars assume an adult pattern early in postnatal triangles which are arranged in two parallel series and ontogenesis, e.g. in Stenocranius gregalis at the age of 1 surrounded by transverse loops in which dentine fields month (Markova et al. 2013). extend across the tooth (Figure 11). Each lobe, cap or triangle is formed by dentine which is bounded The enamel layer that binds each tooth acts as a cutting external y by a sheet of enamel. The occlusal surface edge during mastication. In primitive voles, the enamel dentine shows shallow concavities representing sites of is continuous, rather thick, and equally developed morphologically irregular dentine (reparative dentine) (undifferentiated) although the enamel becomes thicker formed in response to irritations (Phil ips & Oxberry in those portions exposed to higher abrasion during 1972). The enamel-covered sides of the crown form a chewing. In arhizodont molars, the enamel plates are series of anticlines (salient angles) with the synclines (re- commonly thin or discontinuous at the apices of each entrant folds, infoldings) lying in-between. Although salient angle. Because the two edges of the triangles lingual and buccal re-entrants are roughly equal in assume different roles in mastication, they differentiate depth, the outer (labial) triangles are smal er than the and vary in thickness in the majority of recent inner (lingual) in many genera. Terminal angles on M3 arvicolines. The convex edges (anterior edges of upper and M1 are either acute or obtuse. In most voles, molars and posterior edges of lower molars) are defined cement is present in the synclines. Triangles are as trailing (lee) edges, while the concave edges (anterior classified as either opened (enamel of a re-entrant angle edges of lower molars and posterior edges of upper nearly or completely meets the opposing re-entrant molars) are leading (luff) edges. Molars display negative angle) or closed (the two re-entrant angles are separate). differentiation when trailing edges are thicker than the 20 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. leading edges and positive differentiation when the interprismatic matrix running paral el to the occlusal leading edges are thicker (Martin 2007). surface. Lamellar enamel consists of bands (lamellae) that run parallel to the occlusal surface while the sequential layers are orthogonal. The interprismatic matrix strengthens the enamel in the third dimension. The radial type is presumably the most primitive and gave origin to the tangential type by turning the entire structure from 450 (primitive tangential enamel) to 900 (Koenigswald 1980, Koenigswald & Martin 1984). Karyotype Chromosomes are highly condensed parts of the genetic material and proteins which assume a threadlike structure during the metaphase of the cel division. Their number in a somatic cell is usually stable for a population and is reported as a diploid number (2n). Chromosomes of the same cel differ in size and shape. The shape is defined by the position of the centromere. When it is apical, the chromosome is acrocentric, Figure 11: Dental nomenclature of arvicoline molars (after otherwise it is bi-armed (meta- or submetacentric). The Meulen 1973). Occlusal surfaces are of left upper (maxil ary) number of chromosomal arms (NF) gives a simple series (in Chionomys) and of right lower (mandibular) molar series (in Dinaromys). Lingual (inner) side is to the left and metrics of a conventional y stained set of chromosomes buccal (labial, outer) side is to the right. Anterior is to the top. within the cel (karyotype). The name of chromosomes AC–anterior cap; ACC–anteroconid complex; AL–anterior and their shape may vary within a single population or loop; BR–buccal re-entrant angle; BS–buccal salient angle; between them (polymorphism). Some polymorphic LR–lingual re-entrant angle; LS–lingual salient angle; PC– posterior cap (heel); PCC–posteroconid complex; PL– species show fixed differences between populations posterior lobe; T–dental triangle; TTC–trigonid-talonid (polytypy) which usual y originate from pericentric complex. inversions or fusions/fissions of acrocentric/bi-armed elements. The enamel consists of ~96% inorganic material (apatite prisms or crystals) and the rest is surrounding Chromosomal evidence started to enter taxonomic interprismatic matrix. Differences in the orientation of research in the 1950s and resulted in considerable prisms (schmelztype) define the enamel banding advances. By now, the vast majority of Palaearctic voles pattern (schmelzmuster) which differs among major and lemmings have been karyotyped. Compared to taxonomic groups. Three major types occur in other mammals the rate of chromosomal evolution is arvicolines. The basic type is radial enamel with prisms high in arvicolines in general and some lineages show a rising against the outer surface of the tooth; the particularly accelerated tempo of change. This makes interprismatic substance takes orthogonal orientation arvicoline rodents karyotypical y one of the most against the prisms and is therefore oriented radially. polymorphic groups of mammals. Tangential enamel is typified by prisms and the 21 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. Abbreviations External and cranial measurements: Other abbreviations: BWt–body mass (weight); 2n – diploid number of chromosomes HTL–total length (H&B+TL) NF – fundamental number of chromosomal arms H&B–length of head and body; NFa – fundamental number of autosomal arms TL–length of tail; mt – mitochondrial (genome, DNA) HF–length of hind foot; Cyt b – cytochrome b EL–length of ear. K2P – genetic distance calculated using the Kimura 2- CbL–condylobasal length of skull (occipital condyle to parameter model the anterior-most point of the premaxil ary); TMRCA – the most recent common ancestor OnL –occipitonasal length of skull (occipital condyle to sp/spp. – species (singular/plural) the anterior-most point of the nasals); ssp/sspp. – subspecies (singular/plural) ZgW–zygomatic width; ky/My (kya/Mya)–thousand/mil ion years (ago) MxT–length of molar row. a.s.l. – [elevation] above sea level s. str. – sensu stricto (in a narrow sense) Ratios (quotiens) are indicated by a slash (/); e.g. x̄ – arithmetic mean TL/H&B denotes a ratio of tail length against the length SD – standard deviation of head and body. CI – confidence interval ~ approximately Molars are abbreviated by the upper case letter “M” with ≈ almost equal to numbers 1–3 indicating their position in the row; < / > less than / more than superscript/subscript denotes upper (maxil ary)/lower ≤ / ≥ less than or equal / more than or equal (mandibular) molars. E.g. M2 is the 2nd upper molar. For further abbreviations of molar morphology see Figure 11. 22 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. SUBFAMILY: ARVICOLINAE GRAY, 1821 VOLES AND LEMMINGS The context of voles and lemmings within the classis Mammalia is as follows: Class Mammalia Linnaeus, 1758 Subclass Theria Parker & Haswell, 1897 Infraclass Eutheria Gill, 1872 Magnorder Boreoeutheria Springer & de Jong, 2001 Superorder Euarchantoglires Murphy, Eizirik, O’Brien et al., 2001 Order Rodentia Bowdich, 1821 Suborder Myomorpha Brandt, 1855 Superfamily Muroidea Illiger, 1811 Family Cricetidae Fischer, 1817 Subfamily Arvicolinae Gray, 1821 Arvicolinae are in a sister position against true Palaearctic hamsters Cricetinae. Diversification of arvicolines started between 5.7±0.6 Mya (Conroy & Cook 1999) in Late Miocene (Fejfar et al. 2011) and 7.0 Mya (Steppan & Schenk 2017) and the group appeared in the fossil record some 5.5 Mya (Chaline et al. 1999). Modern classification and nomenclature of voles and lemmings is based on Miller (1896), Hinton (1926a) and Ellerman (1941). Key to tribes and subtribes 1a) Lower incisors are short and positioned lingual y with respect to molar row; they terminate below M3 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 1b) Lower incisors pass under M2-M3 from the lingual side to the labial side and ascend into condylar process; they terminate posterior to M3. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 2a) Pelage colour does not depend on the season; ears short but normal y developed; front claws of normal size; skull is low with flat dorsal profile; re-entrant angles fil ed with cement; M1 consists of TTC and AC (5 closed dental fields); M1–2 with 5 closed dental fields; triangles of M3 form transverse laminas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Lemmini 2b) Pelage is brown in summer, white in winter; ears are reduced to a low fold of integument; front claws of digits III and IV much larger during winter; skull is deep with evenly convex dorsal profile; re-entrant angles without cement; M1 has 4 alternating triangles and AC anterior to TTC (9–10 closed dental fields); M1–2 with 7 closed dental fields; triangles of M3 alternate . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Dicrostonychini 3a) Palms and soles are thickly hairy; lingual re-entrant angle LR2 of M2–3 with additional small salient angle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Lagurina 24 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. 3b) Palms and soles at least partly nude; lingual re-entrant angle LR2 of M2–3 without additional salient angle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .4 4a) Molar pattern simplified; dental fields confluent; enamel band of molars is wide and not differentiated; re-entrant angles without cement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .5 4b) Molar pattern not simplified; dental fields usually alternate; enamel band of molars is differentiated; re-entrant angles have cement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .6 5a) Front claws grossly enlarged; 8 nipples; interparietal is remarkably small; pterygoid with oval foramen; upper incisors are orthodont . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Prometheomyini 5b) Front claws of normal size; 6 nipples; interparietal not reduced; pterygoid without oval foramen; upper incisors strongly proodont . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Bramina 6a) Palate terminates as a simple shelf; postero-lateral pits open directly to choanae . . . . .Clethrionomyini 6b) Medial spine extends posteriorly and merges with the medial edges of pits to form a sloping septum on each side of the mesopterygoid vacuity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 7a) Walls of auditory bullae without spongy tissue; M3: T2 is confluent with AL . . . . . . . . . . . . . . . . . . . . . . . . 8 7b) Walls of auditory bullae filled with spongy tissue; M3: T2 is separated from AL. . . . .Arvicolina, Microtina* 8a) TL/H&B>0.55; mystacial vibrissae >50 mm; 6 plantar pads; re-entrant folds with cement; dental fields on M1–3 alternate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Pliomyina 8b) TL/H&B<0.55; mystacial vibrissae <30 mm; 5 plantar pads; re-entrant folds lack cement; dental fields on M1–3 confluent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Hyperacrina new subtribe * Arvicolina and Microtina differ in a combination of several traits. Arvicolina are large (CbL>30 mm) and have a simple M1 (T4 communicates with T5 and AC). Those Microtina, which are of large size, always have a more complex M1 (T4 isolated from T5 and AC); if T4 is confluent with T5 and optional y with AC, then size is smal er (CbL<30 mm). VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION B. Kryštufek & G. I. Shenbrot TRIBE: Prometheomyini Kretzoi, 1955 Prometheomyinae Kretzoi, 1955:355. Type genus is Prometheomys Satunin. Taxonomy. An ancient lineage which may hold a basal position in Arvicolinae (Steppen & Schenk 2017). The tribe contains a single monospecific genus. GENUS: Prometheomys Satunin, 1901 and rocky substrate (Vereshchagin 1959, Kryštufek & – Long-clawed Mole Voles Vohralìk 2005). Altitudinal range is 1,500–3,000 m a.s.l. with an outlier at 723 m. Prometheomys Satunin, 1901a:572. Type species is Characteristics. A medium-sized fossorial vole which Prometheomys schaposchnikowi Satunin. digs using enlarged front claws. Dimensions: Prometheomys schaposchnikowi BWt=52.5–101 g, H&B=125–169 mm, TL=36–57 mm, HF=20.8–25.0 mm, EL=10.5–14.2 mm, CbL=29.8– (Satunin, 1901) – Long-clawed Mole 34.4 mm, ZgW=17.4–20.0 mm, MxT=7.0–8.7 mm. The Vole eyes are smal (diameter=2.1 mm) and the ears are conspicuous and sparsely covered by fur; they are Prometheomys schaposchnikowi Satunin, 1901a:573. Type rounded and equipped with barely detectable antitragus. locality is “a [high mountain] Pass on the Georgian Rhinarium shows no peculiarities; mystacial vibrissae are Military Road”, and “not far from Kreuzberges short and light (Figure 13). Feet have 5 toes each, [Krestoviy Pass above Gudaur] on the Georgian Military equipped with long, slender claws; the claws are longer Road in the main chain of the Caucasus, ca. 6500’ [1,980 on the front feet (6.2–7.2 mm) than on the hind feet (<4 m] high”, Georgia. mm). Palms and soles are nude with 5 and 5–6 pads, respectively. Some pads (lateral metatarsal and palmar Distribution (Figure 12). Endemic to the Caucasus. interdigital) may be reduced (Figure 14). Tail is Distribution area of 58,566 km2 is in 3 main fragments: moderately long (TL/H&B=0.27–0.43) and tapers (i) Western Caucasus in Krasnodar Krai, Adygeya, and gradually from a thick (~5.5 mm) base (Figure 15). Tail likely also south-western Karachay-Cherkessia (Russian is densely haired and terminates into a pencil (length≈6 Federation) and Abkhazia; (ii) Central Caucasus in mm). Fur is up to 15 mm long, soft and moderately North Ossetia (Russia) and Georgia; and (ii ) Lesser dense. Upper parts are dul grey-brown to cinnamon and Caucasus in south-western Georgia and north-eastern the bel y is greyish and shaded cinnamon; cheeks are Turkey. Main habitats are humid meadows with snow usually buff. Hair bases are slate-grey and shade the cover lasting for >200 days/year. Long-clawed mole- ventral side. Juveniles are more greyish. Tail is uniformly voles also occupy forest clearings, birch stands, orchards brown with a white tip in ~½ of voles (51.4%, n=214). and arable land but avoid steep (inclination >250) slopes Feet and ears are dark brown. Females have 8 nipples. 26 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. Figure 12: Distribution of long-clawed mole vole Prometheomys schaposchnikowi. Figure 13: Head (a), ear (b) and the rhinarium (c) of Prometheomys schaposchnikowi from Gudauri, Central Caucasus. Note the small eye, relatively large ear, and short whiskers (inset a). Abbreviations in inset c: Isup–upper incisor; a.n. – ala nasi; d–dorsum; g–gum between the upper incisors in.p. –internarial portion; if.p. –infranarial portion; l.l. –labial lobe; n–nares (external nostrils); ph–philtrum. Tribe: Prometheomyini Kretzoi, 1955 27. age. Temporals are narrow but squamosals are very large. Incisive foramina are of moderate size. The posterior margin of the hard palate is unique in showing broad and complete postero-lateral bridges and shallow pits behind, each with a large oval foramen (Figure 10a). Medial spine is broad but does not merge with the medial edges of pits; hence there is no sloping septum on each side of the mesopterygoid vacuity. Bullae show no peculiarities and the porus acusticus is of normal size. The mandible has wel -developed processes. Upper incisors are orthodont with shal ow longitudinal grooves. The root of the lower incisors passes onto the lingual side between the roots of M2–M3 and forms a Figure: 14: Left palm (left) and sole (right) in Prometheomys bulge on the labial side of the articular process. Molars schaposchnikowi from Gudauri, Greater Caucasus, Georgia. are rooted with 2 roots each; M1 occasional y has 3 roots. In young voles, the alveolar capsules of the molars Glans penis is simple and oval, 15.9 mm long and bulge in the floors of the orbit. Molar enamel is thick covered with spines. The baculum is composed of a (0.14 mm), mainly of radial type but salient angles proximal corpus (length=3.74 mm) and distal trident. contain small amount of discrete lamellar enamel Medial process (length=1.51 mm) is larger and more (Koenigswald 1980). The grinding pattern is simple with ossified than the lateral processes (Çolak et al. 1999). no sharp salient angles and dental fields of alternating triangles are frequently confluent; re-entrant folds lack The skull is robust with squarish brain-case, parallel cement (Figure 17). Anterior molars show al elements zygomatic arches, and vertical y truncated occiput seen in other arvicolines. The anteroconid complex of (Figure 16). Rostrum is broad and moderately long, the M interorbital constriction is wel pronounced. Temporal 1 consists of 2 triangles (T4–5) merging with the anterior loop. Posterior molars are the most reduced ridges fuse into sagittal crest which extends from mid- with only 2 lobes present in older individuals. M3 is interorbital region to the occiput. The sagittal suture made of 2 loops and a single triangle (T2); a rudiment of from the nasals back to the interparietal bone does not T3 is visible in young voles. Unworn M obliterate but persists into advanced age; the 3 shows 2 re- entrant angles on each side but LR3 is obliterated with interparietal is remarkably small and diminishes with age. Figure: 15: Carcass of Prometheomys schaposchnikowi from Gudauri, Central Caucasus, Georgia. Photo F. Janžekovič. 28 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. Figure 16: Skull in Prometheomys schaposchnikowi from northern Caucasus in Russia. Figure 17: Molar pattern in Prometheomys schaposchnikowi: upper (a) and lower row (a’–Çam Geçidi near Ardahan, Turkey); isolated M3 (b; northern Caucasus, Russian Federation); isolated M1 (c’) and M3 (d’–Gudauri, Georgia). Karyotype (2N=56) consists of 11 bi-armed pairs while Variation and subspecies. Monotypic species the remaining autosomes are acrocentric. All (Gromov & Erbajeva 1995). A melanistic population acrocentrics have short arms except for 4 pairs, which is was reported from the western part of the range (Turov the source of various opinions on the number of single- 1934); in the Upper Laba and Belaya Rivers, the and bi-armed chromosomes. Two fundamental proportion of black individuals is ~50% (Vereshchagin numbers are therefore reported: NFa=70 (Zima & Kràl 1959). 1984) and NFa=100 (Çolak et al. (1999). The Y chromosome is either metacentric or acrocentric. VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION B. Kryštufek & G. I. Shenbrot TRIBE: Dicrostonychini Kretzoi, 1955 Dicrostonychini Kretzoi, 1955:355. Type genus is Dicrostonyx Gloger. Taxonomy. An ancient lineage originating from the first pulse of Arvicolinae radiation. The only Palaearctic representative is Dicrostonyx. GENUS: Dicrostonyx Gloger, 1841 – eyes are of moderate size (Figure 18). Tail is cylindrical, Col ared (Varying) Lemmings approximately the same length as the hind foot (TL/H&B=0.10–0.16), and the terminal pencil of bristle-like hair is as long as the tail itself (9–20 mm in Distribution. Circumpolar Arctic tundra, usually north torquatus). Hind foot is unusual y large and strong; palms of 55° northern latitude (Shenbrot & Krasnov 2005). are short and exceptional y broad. Feet are densely The centre of species richness is North America with 6 furred on both sides; pads are entirely absent on palms extant species (Pardiñas et al. 1997). Figure 18: Col ared lemmings with summer pelage: a– Dicrostonyx torquatus (Taymir, Russia); b– D. groenlandicus (Groenland). Photo courtesy: Gerard Müskens (a) and Sven Büchner (b). Characteristics. Arvicoline rodents highly adapted to and those on the soles are vestigial remnants at the base the extreme conditions of the Arctic tundra. Among of the toes (Miller 1896). The thumb is barely others, they are unique in several seasonal adaptations perceptible with a tiny nail. Claws of manual digits III as a response to the short photoperiod: whitening of and IV are of normal size during summer (in D. torquatus pelage, increasing of size, modifying body shape to the length of the claw on digit III is 6–10 mm; height become rounder (Reynolds 1993), and developing large ≤2.5 mm) but grow much larger in winter (length=11– “winter claws” with bifurcate apex. Body is short and 15.5 mm, height 5–5.7 mm; Ognev 1948). The winter thick and the head is disproportional y large. Ears are claw is the result of the fusion of the summer claw with reduced to a low fold of integument around the meatus; the outward growth of the distal end of a toe pad which 30 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. cornifies. The boundary between the two parts is Skull is lightly built but deep (depth behind denoted by a deepened lateral groove; differential wear M3/CbL=0.35–0.42) and broad with widely expanded during digging results in a notch at the groove between zygomatic arches (ZgW/CbL=0.64–0.67); profile is the dorsal summer claw and the hypertophied toe pad evenly convex. Rostrum and nasals are rather narrow (Figure 19). Winter claws are partly lost during the and long, masseteric plate is high. Interorbital region is spring moult and also worn down to normal-sized constricted and supraorbital ridges remain separated by summer claws (Hansen, 1957). Summer fur in D. a groove. Each squamosal develops a conspicuous peg-torquatus is 7–8.5 mm long on the bel y and 10–11.5 mm like postorbital process. Braincase is approximately as on the mid-back; winter fur is softer and longer (9 mm wide as it is long, while the interparietal is longer than it and 12.5–17.5 mm on the ventral and the dorsal side, is wide. Incisive foramina are narrow and long but do respectively). Summer pelage is greyish to brownish; not reach the level of M1. Posterior edge of hard palate cheeks are grey, front flanks and shoulders are rusty; is essentially like in Clethrionomyini. The shelf belly is white to yel owish white with a broad buff or terminates in a short median spine and incompletely rusty col ar on the throat. Winter pelage is white, rarely covers post-palatal pits (Figure 10b). Interpterygoid cinnamon-straw, pinkish or smoky grey, occasionally vacuity is broad. Bullae are of modest size and the with blackish spots on the nose and between the eyes, mastoid portion is somewhat inflated. The walls of the or with buff patches on the shoulders and behind the bullae are spongy; spongy bone also partly fills the cavity ears. Some lemmings can be of intermediate colour of the middle ear (Hooper & Hart 1962). Mandible is (Dunaeva & Kucheruk 1941, Hansen 1959). Hair bases slender and coronoid process is short and blunt (Figure are slate regardless of the season and heavily cloud the 20). colour of the fur. In D. torquatus the moult occurs in early April–May (white to brown pelage) and October Lower incisor is of lemming type, i.e. short and with (brown summer to white winter fur; Ognev 1948). Adult lingual position of its alveolar portion relative to molar females have 8 nipples. Glans penis is highly distinctive row. Molars are rootless and lack cement in re-entrant due to the absence of dorsal papil a and the entire folds. Enamel is positively differentiated with leading configuration of the baculum. The distal trident is edge thicker than the trailing one; schmelzmuster cartilaginous or only partly ossified. The basal stalk is consists of lamellar and radial elements (Koenigswald ≤3.1 mm long in Nearctic species (Anderson 1960, 1980). The enamel band is interrupted by dentine tracks Ognev 1948). at the vertices of all salient angles on all molars (Borodin 2014). Folding pattern is complex (Figure 21). M1 and M2 have 6 and 5 closed triangles posterior to the anterior loop, respectively; posterior triangles T6 and T7 are invariably small. M3 has 3 re-entrant folds on each side and a short posterior lobe. M1 is longer than M2+M3 combined in the lower jaw with 5 lingual and 4 labial deep re-entrant angles; anterior cap is confluent with triangles T8–T9. Posteriorly, M2 and M3 each have 4 closed triangles between the posterior lobe and the anterior vestigial loops T5–T6. Molars gradually became more complex throughout the Holarctic over the last 35 ka (Smirnov & Fedorov 2003). However, some modern Figure 19: Right front foot in Dicrostonyx torquatus (from the populations retained the simple archaic pattern Bolshezemelyskaya tundra, Russian Federation) with winter (Agadjanyan 1976). The archaic type lacks postero-claws on toes III and IV. Abbreviations: s.c, –summer claw; lingual loop T7 on M1–M 2, and antero-labial T6 on M1 l.g. –lateral groove; t.p. –cornified outward growth of the distal (Figure 21a–b’). end of a toe pad; I, II–1st (thumb) and 2nd toes, respectively. Photo: B. Kryštufek. Tribe: Dicrostonychini Kretzoi, 1955 31. Figure 20: Skul and mandible in col ared lemmings: top–Dicrostonyx torquatus (from Taimyrski Zapovednik, Krasnoyarsk Krai, Russian Federation); bottom–D. groenlandicus vinogradovi from Wrangel Island, Chukotka Autonomous Okrug, Russian Federation. Figure 21: Occlusal molar pattern in col ared lemmings. Dicrostonyx torquatus from Taimyrski Zapovednik, Krasnoyarsk Krai, Russian Federation: upper (a) and lower row (a’); isolated M3 (b’). D. groenlandicus vinogradovi from Wrangel Island, Chukotka Autonomous Okrug, Russian Federation: upper (c) and lower row (c’); isolated M1 (d’). 32 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. Despite the distinctive grinding structure, the molar Dicrostonyx groenlandicus (Traill, proportions in Dicrostonyx resemble the pattern seen in 1823) – Nearctic Col ared Lemming the majority of arvicolines, except for Lemmini which have relatively longer M 2 and M3 (Renvoisé et al. 2009). Mus Grœnlandicus Traill, 1823 (in: Scoresby 1823:390). Type locality: “Jameson’s Land”, Greenland. Key to species For Nearctic synonyms see Hall (1981). 1a) Karyotype 2n=37–48 (supernumerary B Taxonomy. Collared lemmings from Wrangel Island chromosomes usual y numerous) …………….torquatus were described as a subspecies ( vinogradovi) of torquatus 1b) Karyotype 2n=28 (supernumerary B chromosomes (Ognev 1948) but began to be treated as a species in its never present)………………….. groenlandicus vinogradovi own right on the basis of karyological evidence (Kozlovsky 1974) and cross-breeding trials (Kuznetzova & Novokshanova 1988). Molecular analysis by Fedorov SUBGENUS: Dicrostonyx Gloger, 1841 et al. (1999) provided further evidence for classification of vinogradovi in groenlandicus. Dicrostŏnyx Gloger, 1841:97. Type species by subsequent designation is “an American species, probably Mus Distribution (Figure 22). Range (=3,343,830 km2) hudsonius Pallas” (Miller 1896:38). extends from Alaska to Hudson Bay, encompassing the high arctic islands of northern Canada; also northern Figure 22: Distribution of the Nearctic col ared lemming Dicrostonyx groenlandicus. Note that the only Palaearctic population is confined to Wrangel Island in the Arctic Ocean offshore Chukotka Autonomous Okrug of the Russian Federation. Tribe: Dicrostonychini Kretzoi, 1955 33. and north-eastern coast of Greenland. Present on in torquatus. Molars are more complex with an additional several Aleutian Islands and on the Bering Sea islands postero-lingual vestigial angle T7 on M1 and M2, and a (MacDonald & Cook 2009). Altitudinal range is 0–1,800 high frequency of the antero-labial vestigial angle (T5) m. on M3 (Figure 21c–d). The karyotype (2n=28, NFa=50) consists mainly of bi-armed chromosomes and is of the Characteristics. See under vinogradovi. Beringian (=Nearctic) type (Kozlovsky 1974, Zima & Král 1984). Females have either XX or XY heterosomes Variation and Subspecies. In addition to the (Fredga et al. 1999). Palaearctic vinogradovi, between 5 (Pardiñas et al. 2017) and 11 subspecies (Hall 1981) are recognised in the SUBGENUS: Myolemmus Pomel, 1852 Nearctic part of the range. Myolemmus Pomel, 1852:363. Type species: Arvicola Dicrostonyx groenlandicus vinogradovi (Myolemmus) ambiguus Pomel, 1852 [= Dicrostonyx Ognev, 1948 – Vinogradov’s Collard torquatus; Trouessart 1897:547]; based on fossil material. Lemming Synonyms. Cuniculus Wagler, 1830 [preoccupied]; Misothermus Hensel, 1855; Borioikon Polyakov, 1881; Dicrostonyx torquatus vinogradovi Ognev, 1948:509. Type Tylonyx Schulze, 1897. locality: “Wrangel Island”, Arctic Ocean, East-Siberian Sea, Far Eastern District, Chukotka Autonomous Taxonomy. The subgenus is general y known as Okrug, Russian Federation. Misothermus but the name is predated by Myolemmus. Contains a single polytypic species. Distribution. Endemic to Wrangel Island (Figure 22). The island is a distance of 140 km from the closest point Characteristics. In addition to the nucleotide on the Siberian mainland and has a surface area of 7,600 sequences (Fedorov et al., 2022), karyology provides the km2. Lemmings occupy dry and upland tundra on slopes most distinguishing characteristic between subgenera: and riverine and coastal terraces up to 400–500 m a.s.l. diploid number is high in Myolemmus and frequently (Chernyavskiy 1984). contains additional B chromosomes. Characteristics. Slightly larger but otherwise similar to torquatus. Dimensions: BWt=52–114 g, H&B=113–151 Dicrostonyx torquatus (Pallas, 1779) – mm, TL=11–22 mm, HF=15.0–18.6 mm, CbL=28.0– Siberian (Palaearctic) Col ared 32.7 mm, ZgW=18.3–21.0 mm, MxT=7.0–8.8 mm. Lemming Back is ash grey to grey-brown with a variable extent of buff or dull rusty wash; admixture of hairs with grey, Taxonomy. In the past torquatus was frequently black dull rusty tips gives a speckled appearance. regarded as the only representative of the genus (Mil er Shoulders and front flanks are rusty to chestnut brown. 1896, Ognev 1948). The rump and head usually remain grey; fur is reddish around pinnae. Belly is whitish or light-grey, heavily Distribution (Figure 23). Endemic to the polar regions clouded with slate underfur and of a cream or yel owish of the Russian Federation, from Mezen' River and the shade in some animals. Spinal stripe is most obvious in Kanin Peninsula (NE Arkhangelsk Oblast, European young individuals and in summer pelage and is Russia) to Chukotka, the Bering Sea coast, and frequently obscured in adults who have more dense Kamchatka. Range covers 1,922,845 km2 and extends in black hairs. When present, the spine is usually restricted a narrow belt along the Arctic coast with southward to mid-back and the rump. Winter fur is cream-white expansions along the River Yenisey, in the north-eastern but hair bases remain slate; the head is darker than the coast of the Sea of Okhotsk and in Kamchatka, reaching back and a grey spinal stripe may be present. Feet and the southernmost point at 530N latitude. Occurs on 7 tail are grey. Skull is on average heavier and deeper than islands (or island groups): Vaygach Island, Novaya 34 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. Zemlya (the Southern and Northern Islands), Belyy back is rarely plain (beige or ash-grey). Cheeks are buff, [=White] Island (near the northern end of the Yamal reddish-brown or grey; fur in front of pinnae is usual y Peninsula), Severnaya Zemlya (Oktyabr’skoy Revolutsii bright rusty and sharply contrasts a transverse light [=Zemlya Imperatora Nikolaya II] and Bolshevik stripe behind the ears. Black spinal stripe is common but Islands), islands in the Lena River delta (Mostakh, fades or disappears in the east. Bel y is white and heavily Sagastyr and others), New Siberian Islands (quoted for washed by slate-grey undercolour; some animals show a the entire archipelago by Ognev 1948, but museum buff tint. Tail is light grey above, whitish below; paws vouchers known only from Stolbovoy Island), and the are whitish. Skull is essentially like in vinogradovi. Molar Bear [=Medvezhyi] Islands (Chetyrekhstolbovoy pattern is less complex and normally lacks vestigial Island). Possibly 70% of habitat was lost since the LGM angles T7 (on M1–M2), T6 (M2) and T5 on M3 (Figure (Fedorov et al. 2020). Major habitat is upland and well- 21a–a’). drained treeless tundra and rocky alpine tundra; permafrost is frequently only 30–40 cm below the D. torquatus is polymorphic for a B chromosome system, surface. Along the southern range margin, collared hence the number of chromosomes in somatic cel s lemmings occupy sparse larch stands of the varies from 46 to >80. Diploid complement (2n, northernmost taiga belt but do not enter dark, closed- without Bs) contains 45–48 mostly acrocentric canopy taiga (Popov 1977). Recorded up to 1,400 m chromosomes (NF=51–52; Gileva 1983), and the a.s.l. in the northern Ural Mts. and till 500–700 m in remaining 0–15 (possibly >30) elements are Bs. The Kamchatka and Koryak Highland (Kostenko 1984). presumed basic karyotype contains 48 ordinary autosomes and two heterosomes; translocations Characteristics. General characteristics are the same as between autosomes led to a stepwise decrease in the for the genus. Dorsal pelage is usual y chestnut-brown, diploid number (Fredga et al. 1999). Heterosomes are reddish-brown or with rich rusty shades on the anterior unusual since females possess either XX or XY back, shoulders and front flanks; the combined effect of complements and males have XY. Heterozygous variously coloured hairs is a speckled pattern of blackish, females have X-linked mutation that supresses the Y light and rusty spots and patches (Figure 24a,b). The chromosome (designated as X*) and converts such Figure 23: Distribution of the Siberian col ared lemming Dicrostonyx torquatus. Tribe: Dicrostonychini Kretzoi, 1955 35. individuals to females. Individuals from Chukotka and Mt- DNA. Mt-diversity is low between and within Polar Urals have 1 chromosome less in XY males and lineages (Fedorov et al. 1999) and becomes high to the X*Y females than in XX and X*X females, the result of east of Kolyma (West-Beringian lineage). Recent translocations between the Y and certain autosomes Siberian collared lemmings evolved from the West- (Gileva 1983, Zima & Král 1984, Fredga 1988). Beringian lineage during the last 77 ky (CI=54–107 ky); the westernmost lineages (Pechora and Yamal) are <6.5 ka old (Fedorov et al. 2020). Over the last ~50 ky at least 4 different lineages succeeded each other across Europe and western Russia (Palkopoulou et al. 2016). Traditional taxonomy recognised 1 island ( ungulatus) and 2 mainland subspecies (Gromov et al. 1963, Gromov & Erbajeva 1985). Lemmings from Bolshevik Is. may represent another yet unnamed form (Gromov & Polyakov 1977). Colour varies clinally; in a west-to-east direction the rusty hues are replaced by a chestnut colour and the dark spinal stripe is gradually lost (Gromov & Polyakov 1977). Dicrostonyx torquatus torquatus (Pallas, 1779) Mus (torquatus) Pallas, 1779:77 + Table XI B. Type locality: “Novum hune praecedentis in Sibiria conterraneum postia notiorem faciam” and “hujus Sibirica fere minorem e regionibus ad Obum sitis arcticis accepi” (p. 206). Restricted to “Subarctic region of the Ob’ estuary” (Ognev 1948:504), Siberia, Russian Federation. Figure 24: Individual and seasonal variation in fur colour of Distribution. Arctic coast between the Kanin Dicrostonyx torquatus. Note the difference between dark Peninsula and Yenisey. summer (a,b–from the Timansky tundra) and white winter skins (c,d–Chukotka). Note the white “col ar” behind the ears Characteristics. Smaller than pallidus; skull is and the mid-spinal stripe in summer skins. Top winter skin (c) displays brown patches on shoulders and on sides of back; the moderately deep. Dimensions: BWt=40–158 g, individual on the extreme bottom (d) is plain white. Photo: B. H&B=101–153 mm, TL=11–21 mm, HF=13–17 mm, Kryštufek. EL=4–8 mm, CbL=27.2–23.7 mm, ZgW=17.6–22.6 mm, MxT=7.2–9.2 mm. Upper side is grey-brown, Variation and subspecies. Dicrostonyx exhibits washed with rusty or buff shades; shoulders are the same extensive chromosomal polymorphism with 4 races colour as the back, flanks are reddish-brown, cheeks which are characterised by the morphology of buff or reddish-brown; black spinal stripe is prominent. heterosomes, by reduced chromosome numbers due to Contains 2 al opatric Mt- DNA sublineages (Fedorov et Robertsonian translocations and by the presence of al. 1999) and a single chromosomal race (Race I; 2n=45– supernumerary (B) chromosomes. These chromosomal 46 + 2–9 Bs; Fredga et al. 1999). races are congruent with the phylogeographic pattern of 36 VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION. Dicrostonyx torquatus palidus blackish than those from Sakha and Chukotka (Middendorff, 1852) (Chernyavskiy 1984). Karyotype: 2n=46, 47, 48 (Stenseth & Ims 1993). Contains 3 allopatric Mt- DNA sublineages centred in Taimyr, and in the deltas of Yana [Myodes torquatus] var. pallida Middendorff, 1852:93 (not and Kolyma, respectively (Fedorov et al. 1999), and 3 1867; Ognev 1948:506). Syntypes were captured in chromosomal races (Fredga et al. 1999): Race II (2n=46 “Taimyrlande” (Taymyr Peninsula) and “Nówaja- + 5–13 Bs), Race III (2n=37–39; without Bs), and Race Semljá” (Novaya Zemlya, Arctic Ocean, Russian IV (2n=47–48 + 3–6 Bs). Federation). Syntypes belong to two subspecies (the nominal and ungulatus). We therefore restrict the type locality to: Taymyr Peninsula, northern Krasnoyarsk Dicrostonyx torquatus ungulatus Krai, Russian Federation. (Baer, 1841) Synonyms. Mus lenae Kerr, 1792; Mus lenensis Pallas, Lemmus ungulatus Baer, 1841:283. Type locality: Island of 1811; Dicrostonyx chionopaes G. M. Allen, 1914. Novaya Zemlya, Russia. Distribution. From Taymyr Peninsula till Chukotka Distribution. Endemic to the Severny and Yuzhny and Kamchatka. Islands (Novaya Zemlya archipelagos, Arkhangelsk Oblast). Characteristics. Size large; skull shallow. Dimensions: BWt=47–153 g, H&B=109–155 mm, TL=14–22 mm, Characteristics. Cranially the most distinct subspecies HF=14.5–17.0 mm, EL=4–7 mm, CbL=27.1–32.5 mm, with a deep skul and short nasals. Dimensions: ZgW=16.7–21.6 mm, MxT=7.3–8.8 mm. In captivity, H&B=131 mm, TL=25 mm, HF=15.5 mm, chionopaes grow faster than the nominal subspecies CbL=28.8–29.1 mm, ZgW=19.1–20.1 mm, MxT=4.6– (Prushinskaya et al. 1992). Size is stable among 7.8 mm. Externally similar to mainland lemmings. populations; CbL ( x̄ ±SD; mm) varies from 29.0±0.32 Pelage is ash-grey with a light brown shade and black (lowlands along the Lena River) to 29.8±034 (Yamal) spots; shoulders and front flanks are rusty-buff to and 29.8±0.29 (Chukotka; Chernyavskiy 1984). Back is chestnut-brown. A single Mt- haplotype is known which more variegated than in nominal subspecies; shoulders differs from the remaining conspecific sequences by are richly rusty, cheeks grey, spinal stripe frequently ill- 0.7–1.2% (Spitsyn et al. 2021b). Karyotype is not defined or absent. Animals from Taimyr are more known. VOLES AND LEMMINGS (ARVICOLINAE) OF THE PALAEARCTIC REGION B. Kryštufek & G. I. Shenbrot TRIBE: Lemmini Mil er, 1896 Lemmi Miller, 1896:8. Type genus is Lemmus Link. short. Although reduced in the majority of arvicolines, the thumb carries a large, blunt and flattened nail (Figure Synonyms. Hypudaei Fitzinger, 1867. 25). The fur is long and dense. There are 8 mammae in Lemmus and Myopus; Synpatomys has 6–8 nipples. Glans Taxonomy. The tribe contains 3 genera: Lemmus, penis is cylindrical; baculum consists of a relatively short Myopus and Synaptomys; the last holds a basal position in and robust proximal stalk and distal trident. The sperm phylogenetic trees (Robovský et al. 2008). head is falciform (Retzius 1909). Distribution. The range of the tribe is circumpolar, also The skull is broad and low with powerful zygomatic encompassing boreal and temperate zones as far south arches which expand abruptly. Rostrum is relatively as 450 north in Eurasia, and 350 north in North America short, nasals are bottle-shaped. Interorbtital region is (Shenbrot & Krasnov 2005). Of the 3 genera, Lemmus is narrow with a prominent ridge which expands Holarctic, Myopus is Palaearctic, and Synaptomys is posteriorly across temporals, reaching the lambdal crest. Nearctic. Post-orbital process on the squamosal is evident but less prominent than in Dicrostonyx. Maxillary tooth-rows Characteristics. In the Palaearctic representatives the rapidly diverge posteriorly. Incisive foramina are rather body is either vole-like ( Myopus) or more chunky and short and wide; the lateral palatal grooves are wel - robust ( Lemmus); the tail is perpetually short (TL