Sibling mice species of the genus Sylvaemus Ognev, 1924 (Mammalia, Rodentia) in the Ukrainian Carpathians
Abstract
Three species of the genus Sylvaemus occur in the region of the Ukrainian Carpathians: the yellow-necked field mouse (S. tauricus), the long-tailed field mouse (S. sylvaticus) and the pygmy field mouse (S. uralensis). Issues of the genus’s taxonomy and identification of species have remained controversial in some parts of the geographic range, while in the Ukrainian Carpathians they have been studied scarcely at all. We studied about 250 mice specimens from the Ukrainian Carpathians belonging to the genus Sylvaemus, among which 216 were analysed morphometrically based on 4 external and 11 cranial characters. Results indicate that by linear body dimension only S. uralensis can be differentiated with high probability. For the pair of species tauricus–sylvaticus, the hind foot length is the least variable among linear body characters, which might be considered diagnostic, although values of this character also tend to overlap. To identify species correctly, it is necessary to use craniometrical characters. For the pair of tauricus–sylvaticus, the least variable among the 11 studied characters are the upper molars length (M13), braincase width (CRB), and braincase height (CRH). Mixed samples of adult specimens of the three species can be differentiated with minimal or practically no overlap by using the relation of the upper molars length to braincase width, condylobasal length, and auditory bulla length. Analysis of characters’ uniformity in adult specimens showed that S. tauricus and S. sylvaticus differ from one another the most by the upper molars length (M13), braincase width (CRB), braincase height (CRH), condylobasal length (CBL), and auditory bulla length (BUL). A similar tendency was revealed for the pair of S. sylvaticus and S. uralensis. A regional identification key was developed for differentiation of adult mice, which allows identifying reliably 93.5% of specimens. Results of the revision of samples suggest that S. tauricus has the widest altitudinal and habitat preferences, S. sylvaticus occurs mainly in humid floodplain biotopes (shrubs, woods) entering far into the mountains along river valleys, while S. uralensis is represented only by few records from lowland floodplain habitats.
Downloads
References
Adamczewska-Andrzejewska K.A. Age reference model for Apodemus flavicollis (Melchior, 1834) // Ekologia Polska – seria A. – 1967. – Vol.15. – P. 787–790.
Balčiauskiené L., Juškaitis R., Mažeikytė R. Identification of shrews and rodents from skull remains according to the length of a tooth row // Acta Zoologica Lituanica. – 2002. – Vol.12, no. 4. – P. 353–361.
Barčiová L., Macholán M. Morphometric key for the discrimination of two wood mice species, Apodemus sylvaticus and A. flavicollis // Acta Zoologica Academiae Scientiarum Hungaricae. – 2009. – Vol.55, no. 1. – P. 31–38.
Barkaszi Z., Zagorodniuk I. The taxonomy of rodents of the Eastern Carpathians // Proceedings of the State Natural History Museum. – 2016. – Vol.32. – P. 137–154.
Bugarski-Stanojević V., Blagojević J., Adnađević T. et al. Molecular phylogeny and distribution of three Apodemus species (Muridae, Rodentia) in Serbia // Journal of Zoological Systematics and Evolutionary Research. – 2008. – Vol.46, no. 3. – P. 278–286.
Čanády A., Mošanský L., Hýbelová M., Pavelková P. Morphometric variability of Apodemus uralensis in Slovakia (Rodentia, Muridae) // Lynx, n. s. (Praha). – 2014. – Vol.45. – P. 5–14.
Čanády A., Mošanský L. Craniometric data of Apodemus sylvaticus in Slovakia // Biologia. – 2015. – Vol.70, no. 7. – P. 974–981.
Chassovnikarova T., Markov G. Wood mice (Apodemus sylvaticus Linnaeus, 1758 and Apodemus flavicollis Melchior, 1834) from Bulgaria: craniometric characteristics and species discrimination // Forest Science. – 2007. – Vol.44, no. 3. – P. 39–52.
Chelomina G.N., Atopkin D.M., Bogdanov A.S. Phylogenetic relationships between species and intraspecific forms of forest mice from the genus Sylvaemus as determined by partial sequencing of the cytochrome b gene of mitochondrial DNA // Doklady Biological Sciences. – 2007. – Vol.416, no. 1. – P. 356–359.
Cichocki J., Ruprecht A. L., Ważna A. Distribution of pygmy field mouse Apodemus uralensis (Pallas, 1811) population in Poland: review of the studies and new data // Fragmenta Faunistica. – 2011. – Vol.54, no. 1. – P. 77–85.
Cranbrook L. Long tailed field mice (Apodemus sp.) from the Channel Islands // Proceedings of the Zoological Society of London. – 1957. – Vol.128, no. 4. – P. 597–600.
Cserkész T. Bagolyköpetekből származó erdeiegér (Sylvaemus subgenus, Rodentia) koponyamaradványok összehasonlító kraniometriai vizsgálata: a fajok elkülönítése és a korcsoportok szerepe // Állattani Közlemények. – 2005. – Vol.90, no. 1. – P. 41–55.
Delany M. J., Davis P. E. Observations on the ecology and life history of the Fair Isle field-mouse Apodemus sylvaticus fridariensis (Kinnear) // Proceedings of the Zoological Society of London. – 1961. – Vol.136, no. 3. – P. 439–452.
Demeter A., Lázár P. Morphometric analysis of field mice Apodemus: character selection for routine identification (Mammalia) // Annales Historico-Naturales Musei Nationalis Hungarici. – 1984. – Vol.76. – P. 297–322.
Dzeverin I.I., Lashkova O.I. Rates of divergence for craniometric characters in Sylvaemus species (Muridae, Rodentia) from the Ukrainian fauna // Scientific Bulletin of Uzhgorod University, Series Biology. – 2012. – Vol.32. – P. 131–134. (in Ukrainian)
Fielding D.C. The identification of skulls of the two British species of Apodemus // Journal of Zoology. –1966. – Vol.150, no. 4. – P. 498–500.
Haitlinger R., Ruprecht A.L. The taxonomic value of teeth measurements in the subgenus Sylvaemus Ognev & Vorobiev, 1923 // Acta Theriologica. – 1967. – Vol.12. – P. 180–187.
Herman J.S., Jóhannesdóttir F., Jones E.P. et al. Post-glacial colonization of Europe by the wood mouse, Apodemus sylvaticus: evidence of a northern refugium and dispersal with humans // Biological Journal of the Linnean Society. – 2017. – Vol.120, no. 2. – P. 313–332.
Hoofer S.R., Gaschak S., Dunina-Barkovskaya Ye. et al. New information for systematics, taxonomy, and phylogeography of the rodent genus Apodemus (Sylvaemus) in Ukraine // Journal of Mammalogy. – 2007. – Vol.88, no. 2. – P. 330–342.
Janžekovič F., Kryštufek B. Geometric morphometry of the upper molars in European wood mice Apodemus // Folia Zoologica. – 2004. – Vol.53, no. 1. – P. 47–55.
Jojić V., Bugarski-Stanojević V., Blagojević J., Vujošević M. Discrimination of the sibling species Apodemus flavicollis and A. sylvaticus (Rodentia, Muridae) // Zoologischer Anzeiger. – 2014. – Vol.253. – P. 261–269.
Knitlová M., Horáček I. Late Pleistocene–Holocene paleobiogeography of the genus Apodemus in Central Europe // PLoS ONE. – 2017. – Vol.12, no. 3. – e0173668.
Kolyushev I.I. A brief review of rodents of Transcarpathia // Nauchnye Zapiski UzhGU (Seriya Biologia). – 1953. – Vol.8. – P. 143–158. (in Russian)
Kryštufek B., Sozen M., Bukhnikashvili A. Apodemus uralensis // The IUCN Red List of Threatened Species. – 2008. – e.T1905A8801937.
Kuncová P., Frynta D. Interspecific morphometric variation in the postcranial skeleton in the genus Apodemus // Belgian Journal of Zoology. – 2009. – Vol.139, no. 2. – P. 133–146.
Kyselyuk A.I. Sylvaemus uralensis (Rodentia, Muridae) in the East Carpathians // Vestnik Zoologii. – 1993. – Vol.27, no. 4. – P. 41–47. (in Russian)
Lashkova E.I., Mezhzherin S.V., Dzeverin I.I. Identification of wood mice species of the Ukrainian fauna using external and cranial characters by the multivariate analyses // Vestnik Zoologii. – 2005. – Vol.39, no. 3. – P. 23–28. (in Russian)
Lashkova E.I., Dzeverin I.I., Mezhzherin S.V. Variation of mandible in wood mice species, Sylvaemus (Muridae, Rodentia), from the fauna of Ukraine // Vestnik Zoologii. – 2006. – Vol.40, no. 4. – P. 359–366. (in Russian)
Lashkova E.I., Dzeverin I.I. Odontometric variation and species identification of wood mice Sylvaemus (Muridae, Rodentia) from Ukraine // Vestnik Zoologii. – 2002. – Vol.36, no. 3. – P. 25–33. (in Russian)
Marsh A.C.W., Harris S. Partitioning of woodland habitat resources by two sympatric species of Apodemus: lessons for the conservation of the yellow-necked mouse (A. flavicollis) in Britain // Biological Conservation. – 2000. – Vol.92. – P. 275–283.
Mezhzherin S.V., Lashkova E.I., Tovpinets N.N. Geographic distribution, population densities and habitat preference of the wood mice genus Sylvaemus (Rodentia, Muridae) on the territory of Ukraine // Vestnik Zoologii. – 2002. – Vol.36, no. 6. – P. 39–49. (in Russian)
Mezhzherin S.V., Zagorodniuk I.V. New species of mouse of the genus Apodemus (Rodentia, Muridae) // Vestnik Zoologii. – 1989. – Vol.23, no. 4. – P. 55–59. (in Russian)
Michaux J.R., Magnanou E., Paradis E. et al. Mitochondrial phylogeography of the woodmouse (Apodemus sylvaticus) in the Western Palearctic region // Molecular Ecology. – 2003. – Vol.21. – P. 685–697.
Michaux J.R., Libois R., Filipucci M.-G. So close and so different: comparative phylogeography of two small mammal species, the yellow-necked fieldmouse (Apodemus flavicollis) and the woodmouse (Apodemus sylvaticus) in the Western Palearctic region // Heredity. – 2005. – Vol.94. – P. 52–63.
Naglov B.A. Distribution and population density of Sylvaemus sylvaticus (Rodentia, Muridae) in Kharkov Oblast // Vestnik Zoologii. – 1995. – Vol.29, no. 5–6. – P. 87–89. (in Russian)
Niethammer Von J. Zur frage der introgression bei den waldmäusen Apodemus sylvaticus und Apodemus flavicollis (Mammalia, Rodentia) // Journal of Zoological Systematics and Evolutionary Research. –1969. — Vol.7, no. 1. – P. 77–127.
Orlov V.N., Bulatova N.Sh., Nadjafova R.S., Kozlovsky A.I. Evolutionary classification of European wood mice of the subgenus Sylvaemus based on allozyme and chromosome data // Bonner Zoologische Beiträge. – 1996. – Vol.46. – P. 191–202.
Panzironi C., Cerone G., Cristaldi M., Amori G. A method for the morphometric identification of southern Italian populations of Apodemus (Sylvaemus) // Hystrix. – 1993. – Vol. 5, no. 1–2. – P. 1–16.
Polushina N.A., Voznyuk M.N. New data on Apodemus microps Krat. et Ros. in the territory of the USSR // Rodents. Book of Abstracts of the V All-Union Conference on Rodents. – Moscow, 1980. – P. 37–38. (in Russian)
Popov V.V. Discriminant criteria and comparative study on morphology and habitat selection of Apodemus sylvaticus (Linnaeus, 1758) and Apodemus flavicollis (Melchior, 1834) (Mammalia, Rodentia, Muridae) in Bulgaria // Acta Zoologica Bulgaria. – 1993. – Vol.46. – P. 100–111.
Shnarevich I.D. Mammals of the Soviet Bukovina // Animals of the Soviet Bukovina. – Chernivtsi, 1959. –P. 5–65. (in Russian)
Sokur I.T. Mammals of the Soviet Carpathians and their economic use. – Kyiv: Publishing House of AN UkrSSR, 1952. – 68p. (in Ukrainian)
Stetsula N. Age variation as the factor influencing on the exactness of identification of morphologically close species of mouse-like rodents // Proceedings of the Theriological School. – 2012. – Vol.11. – P. 41–49. (in Ukrainian)
Tatarinov K.A. Mammals of the western regions of Ukraine. – Lviv, 1956. – 257p. (in Ukrainian)
Tchernov E. Polymorphism, size trends and Pleistocene paleoclimatic response of the subgenus Sylvaemus (Mammalia: Rodentia) in Israel // Israel Journal of Zoology. – 1979. – Vol.28. – P. 131–159.
Turyanin I.I. Fauna, economic and epidemiologic importance of rodents of Transcarpathia // Nauchnye Zapiski UzhGU (Seriya Biologia). – 1959. – Vol.40. – P. 21–28. (in Russian)
Vohralík V. Distribution, skull morphometrics and systematic status of an isolated population of Apodemus microps (Mammalia, Rodentia) in NW Bohemia, Czech Republic // Acta Societatis Zoologicae Bohemicae. – 2002. – Vol.66. – P. 67–80.
Vorontsov N.N., Boyeskorov G.G., Mezhzherin S.V. et al. Systematics of the Caucasian wood mice of the subgenus Sylvaemus (Mammalia, Rodentia, Apodemus) // Zoologicheskii Zhurnal. – 1992. – Vol.71, no. 2. – P. 119–131. (in Russian)
Zagorodniuk I.V. Sibling species of mice from Eastern Europe: taxonomy, diagnostics and distribution // Reports of the National Academy of Sciences of Ukraine. – 1996. – No. 12. – P. 166–173.
Zagorodniuk I.V., Kavun K.Yu. Age-related variation as basis for emergence of interspecific differences in rodents (Muriformes) // Reports of the National Academy of Sciences of Ukraine. – 2000. – No. 3. – P. 174–180. (in Ukrainian)
Zimmermann K. Die Untergattungen der gattung Apodemus Kaup. // Bonner Zoologische Beiträge. – 1962. – Vol.13, no. 1–3. – P. 198–208.
Authors retain copyright of their work and grant the journal the right of its first publication under the terms of the Creative Commons Attribution License 4.0 International (CC BY 4.0), that allows others to share the work with an acknowledgement of the work's authorship.