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Morphological Variation of the Five Vole Species of the Genus Microtus

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Morphological Variation of the Five Vole Species of the Genus Microtus Acta Zoologica (Stockholm) 90: 254–264 (July 2009) doi: 10.1111/j.1463-6395.2008.00348.x MorphologicalBlackwell Publishing Ltd variation of the five vole species of the genus Microtus (Mammalia, Rodentia, Arvicolinae) occurring in Greece Stella E. Fraguedakis-Tsolis, Basil P. Chondropoulos, Costas V. Stamatopoulos and Sinos Giokas Abstract Section of Animal Biology, Department of Fraguedakis-Tsolis, S.E., Chondropoulos, B.P., Stamatopoulos, C.V. and Biology, University of Patras, GR-26500 Giokas, S. 2009. Morphological variation of the five vole species of the genus Patras, Greece Microtus (Mammalia, Rodentia, Arvicolinae) occurring in Greece. — Acta Zoologica (Stockholm) 90: 254–264 Keywords: Greece, Microtus, morphometrics, Morphometric data for the five vole species of the genus Microtus living in Rodentia, Terricola Greece are old, sparse, poor and insufficiently analysed. This work aims to give the first comprehensive morphometric analysis of body and skull inter- Accepted for publication: and intraspecific variation for M. (M.) guentheri, M. (M.) rossiaemeridionalis, 13 June 2008 M. (Terricola) subterraneus, M. (T.) felteni and M. (T.) thomasi, applying multivariate statistics to 28 linear morphometric variables. It was based on ample material (202 adult individuals) using samples from localities that adequately cover the entire distributional range of each species in Greece. The five species and the two subgenera (Microtus and Terricola) were morphometrically clearly distinguished and discriminating variables were revealed. However, morphometrics did not provide robust criteria to infer phylogenetic relations among species. Furthermore, three species, M. (M.) guentheri, M. (M.) rossiaemeridionalis and M. (T.) thomasi, exhibited considerable intraspecific size or shape variation, which was mostly random and not associated with geographical proximity. Comparisons with data in the literature, mainly concerning populations of these species from adjacent areas, indicate that the Greek M. (M.) guentheri, M. (M.) rossiaemeridionalis and M. (T.) thomasi tend to be smaller than their conspecifics, while M. (T.) subterraneus and M. (T.) felteni are about equal in size to their Balkan relatives. Sinos Giokas, Section of Animal Biology, Department of Biology, University of Patras, GR-26500 Patras, Greece. E-mail: [email protected] makes it ideal for evolutionary studies examining inter/ Introduction intraspecific geographical variability, adaptive convergence Microtus Schrank 1798 is one of the most speciose, differentiated and divergence, and identification of sibling species. and widespread mammalian genera (Mitchell-Jones et al. According to recent knowledge (Mitchell-Jones et al. 1999; Musser and Carleton 2005). However, the phylogenetic 1999), five vole species of the genus Microtus live in Greece relationships within Microtus and its closest relatives, based belonging to the European subgenera Microtus and Terricola initially on dental and skull morphology and karyotypes, are (although there are objections to the status of Terricola – uncertain and some difficulties remain both in delimiting Kryßtufek et al. 1996); these are Microtus (Microtus) guentheri species and in defining subgenera even with the use of mole- (Danford & Alston 1880), M. (M.) rossiaemeridionalis Ognev cular approaches (Jaarola et al. 2004). Yet, it is noteworthy 1924, M. (Terricola) subterraneus (de Sélys-Longchamps 1836), that the genus Microtus displays a number of features that M. (T.) felteni Malec & Storch 1963 and M. (T.) thomasi © 2008 The Authors 254 Journal compilation © 2008 The Royal Swedish Academy of Sciences Acta Zoologica (Stockholm) 90: 254–264 (July 2009) Fraguedakis-Tsolis et al. • Morphometrics of the Greek Microtus voles previous morphometric attempts did not partition efficiently size from shape components. The present work aims to give the first comprehensive morphometric analysis of body and skull variation for these five vole species in Greece. This analysis, using multivariate statistics, is based on ample material consisting of samples from localities that adequately cover the entire distributional range of each species in Greece. An effort was also made to compare our morphometric data with those available in the literature. This approach allows us not only to investigate the morphometric and geographical variation of these Microtus species in Greece, and to examine if such morphometrics are sufficient in providing a reliable identity for each species or population, but also to identify possible morphological size and shape adaptations, useful in understanding the diversifica- tion processes of these small mammals. Fig. 1—Map showing the distributional borders of the five Materials and Methods Microtus species in Greece. ....... M. (M.) guentheri, ------ M. (M.) rossiaemeridionalis, __ __M. (Terricola) subterraneus, Sampling and variables ___M. (T.) felteni and ___.. M. (T.) thomasi. A total of 202 adult individuals of the five Microtus species studied were collected from 40 localities, in an effort to adequately cover their variation. Because of the small sample (Barrett-Hamilton 1903). The geographical distribution size of M. (M.) rossiaemeridionalis and M. (T.) thomasi of these species in mainland Greece shows considerable collected from some of these localities, we pooled the material differences in the extent of their distribution and sympatry coming from the same physiographic/geographical unit to (Fig. 1). Specifically, M. (T.) thomasi is the most common form larger groups for the purposes of the statistical analysis. and widespread species, living from Western Makedonia in Information about the location (geographical and regional the north to the southernmost part of Peloponnisos; origin) and the size of each sample are presented in Table 1. M. (M.) guentheri occurs in most parts of the northern The following 28 linear morphometric variables (four and eastern Greek mainland except Peloponnisos; M. (M.) external and 24 cranial) were analysed: head and body length rossiaemeridionalis is distributed in the northern parts of the (HB), tail length (TL), ear length (EL), hind foot length country (Ipeiros, Makedonia, Thraki); the remaining two (HFL), condylobasal length (CBL), basal length (BL), species, M. (T.) subterraneus and M. (T.) felteni, have a condyloincisive (condylobasilar) length (CIL), occipitonasal restricted range confined to the mountainous north-central length (ONL), upper diastema length (UDL), incisive continental part of Greece (Ondrias 1966; Niethammer foramen length (IFL), nasal length (NL), upper molar row 1982a,b,c,d; Petrov and RuΩic 1982; Vohralík and Sofianidou length (at the alveoli level) (UMR), upper molar row length 1987, 1992; Sofianidou and Vohralík 1991; Mitchell-Jones (at the crowns level) (UMRc), tympanic bulla length (TBL), et al. 1999). The only Greek islands inhabited by voles are interorbital width (interorbital constriction) (IOW), occipital Lesvos, where M. (M.) guentheri is known to occur (Stam- width (OW), palatal length (PL), zygomatic width (ZW), atopoulos and Ondrias 1995; Mitchell-Jones et al. 1999), brain-case height (from the tympanic bulla) (BCHb), brain-case and Evvoia, where M. (T.) thomasi is distributed (Niethammer height (from the foramen of the tympanic bulla) (BCHf), 1982d; Mitchell-Jones et al. 1999). It is noteworthy that the brain-case width (BCW), rostral height (at the alveolus of the southernmost distributional borders of these five Microtus M1 (ROH1), rostral height (at the middle of the upper species are found in Greece. Furthermore, M. (T.) felteni molars) (ROH), mastoid width (MW), mandibular length and M. (T.) thomasi are endemic to the southern Balkans (ML), lower molar row length (at the alveoli level) (LMR), (Niethammer 1982c,d; Mitchell-Jones et al. 1999). lower molar row (at the molar crowns) (LMRc) and articular The morphometric data for these vole species in Greece height (AH). The above variables are commonly used in are rather old, sparse, limited and insufficiently analysed morphometric analyses of voles and are illustrated in (Ondrias 1965, 1966; Spitz 1978; Niethammer and Krapp Niethammer and Krapp (1978) and Ventura and Gosálbez 1982; Brunet-Lecomte and Nadachowski 1994; Tsekoura (1989). The four external variables were measured with a et al. 2002), mainly because of the small numbers of specimens ruler to the nearest 0.5 mm while the remaining variables examined and variables measured, and the few populations were measured using a digital vernier calliper (Mitutoyo Ltd, sampled within each species range. Furthermore, these UK) to the nearest 0.01 mm. All measurements for our © 2008 The Authors Journal compilation © 2008 The Royal Swedish Academy of Sciences 255 Morphometrics of the Greek Microtus voles • Fraguedakis-Tsolis et al. Acta Zoologica (Stockholm) 90: 254–264 (July 2009) Table 1 Sampling localities and the respective number of individuals examined for each Microtus species Species Sampling localities and number of individuals (in parentheses) M. (M.) guentheri Paranesti (Drama Pref.), Eastern Makedonia (4); Amyntaio (Florina Pref.), Western Makedonia (7); Sykourio (Larisa Pref.), Thessaly (8); Gravia (Fokida Pref.), Sterea Ellada (15). M. (M.) rossiaemeridionalis Protokklisi (Evros Pref.) and Kremasti (Xanthi Pref.), Thrace (8); Lagkadikia (Thessaloniki Pref.) and Olynthos (Chalkidiki Pref.), Central Makedonia (6); Sevastiana (Pella Pref.) and Kopanos (Imathia Pref.), Western Makedonia (27); Arnissa (Pella Pref.) and Kato Vermio (Imathia Pref.), Western
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