Confirmation of European snow vole Chionomys nivalis (Mammalia: Rodentia: Cricetidae) occurrence in Portugal

Figures & data

Figure 1. (a) Habitat features of the sampling site; (b) the juvenile female snow vole captured; (c) the adult male snow vole captured (this picture was obtained through infrared beam cells).

Table I. Locality and accession numbers of the Chionomys nivalis cyt-b and interphotoreceptor retinoid-binding protein (IRBP) sequences retrieved from GenBank and used in the analysis. Number of sequences is given in parentheses.

Country	Locality	GenBank Acc. No. (n)		References
		cyt-b	IRBP
Andorra	Andorra	JX457754 (1)	JX457672 (1)	Barbosa et al. (2013)
Andorra	Andorra		JX457673 (5)	Barbosa et al. (2013)
Spain	Girona	AY513848 (1)		Jaarola et al. (2004)
Spain	Girona	JX457753 (1)		Barbosa et al. (2013)
Spain	Sierra de Gredos	AM392367 (1)		Galewski et al. (2006)
Spain	Sorpe	JX457752 (1)	JX457671 (1)	Barbosa et al. (2013)
Italy	Duchessa	GQ150802 (1)		Castiglia et al. (2009)
Italy	Gran Sasso	GQ150799 (1)		Castiglia et al. (2009)
Italy	Marta Alpi Liguri	GQ150794 (1)		Castiglia et al. (2009)
Italy	Marta Alpi Liguri	GQ150800 (1)		Castiglia et al. (2009)
Italy	Trento	AY513845 (1)		Jaarola et al. (2004)
Italy	Trento	AY513846 (1)		Jaarola et al. (2004)
Italy	Val Masino	GQ150795 (1)		Castiglia et al. (2009)
Italy	Val Masino	GQ150796 (1)		Castiglia et al. (2009)
Italy	Valle d’Aosta	GQ150797 (1)		Castiglia et al. (2009)
Italy	Valle d’Aosta	GQ150798 (1)		Castiglia et al. (2009)
Italy	Valle d’Aosta	GQ150801 (1)		Castiglia et al. (2009)
Switzerland	Derborence	GU954316 (1)		Fink et al. (2010)
Switzerland	Derborence	GU954317 (1)		Fink et al. (2010)
Slovenia	Mt Sneznik	GQ150792 (1)		Castiglia et al. (2009)
Slovenia	Mt Sneznik	GQ150793 (1)		Castiglia et al. (2009)
Slovakia	West Tatra Mts	AY513847 (1)		Jaarola et al. (2004)
Macedonia	Mt Pelister	GQ150791 (4)		Castiglia et al. (2009)
Bulgaria	Vitosha Mountain	CQ352464 (1)		Bannikova et al. (2013)
Romania	Eastern Carpatians, Breskul Mountain	CQ352465 (1)		Bannikova et al. (2013)
Adygea	Caucasian Reserve, Abago Mountain	JX440342 (2)		Bannikova et al. (2013)
Georgia	Pass of Tskhra-tskharo, Transcaucasia	HQ901803 (2)		Yannic et al. (2012)
Georgia	Pass of Tskhra-tskharo, Transcaucasia	HQ901799 (1)		Yannic et al. (2012)
Georgia	Pass of Tskhra-tskharo, Transcaucasia	HQ901800 (1)		Yannic et al. (2012)
Georgia	Pass of Tskhra-tskharo, Transcaucasia	HQ901801 (1)		Yannic et al. (2012)
Georgia	Bacuriany, Caucasus	HQ901802 (2)		Yannic et al. (2012)
Turkey	Ciglikara	GQ150786 (1)		Castiglia et al. (2009)
Turkey	Ciglikara	GQ150787 (1)		Castiglia et al. (2009)
Turkey	Ciglikara	GQ150788 (1)		Castiglia et al. (2009)
Turkey	Central Taurus	JN244707 (1)		Bannikova et al. (2013)
Syria	Saleh	AY513849 (1)		Jaarola et al. (2004)
Israel	Mt Hermon	GQ150789 (1)		Castiglia et al. (2009)
Israel	Mt Hermon	GQ150790 (1)		Castiglia et al. (2009)
Turkmenistan	Ashabad, Kopet-Dag	HQ901804 (1)		Yannic et al. (2012)
Turkmenistan	Ashabad, Kopet-Dag	HQ901805 (1)		Yannic et al. (2012)
Turkmenistan	Ashabad, Kopet-Dag	HQ901806 (1)		Yannic et al. (2012)
Turkmenistan	Ashabad, Kopet-Dag	HQ901807 (1)		Yannic et al. (2012)

Table II. Age, sex, number of specimens analysed in each study (N) and biometric measures of Chionomys nivalis (standard errors are given in parentheses when available). According to body weight and hair colour, two age classes, juveniles and adults (body mass > 35 g), were defined (LeLouarn & Janeau 1975; Luque-Larena et al. 2002; Pérez-Aranda et al. 2007b).

Country	Age	Sex	N	Body weight (g)	Head-body length (mm)	Tail length (mm)	Hind foot length (mm)	Ear length (mm)	References
Portugal	A	M	1	49.0	122.4	72.8	22.0	17.3	This study
	J	F	1	27.2	103.1	53.7	19.5	14.5	This study
Spain	A	M	111	50.3 (0.9)	–	–	–	–	Luque-Larena et al. (2004)
	A	F	85	45.4 (0.9)	–	–	–	–
	–	–	NI	35.0–70.0	92.0–140.0	45.0–74.0	17.5–25.0	12.5–21.0	Pérez-Aranda et al. (2007b)
Iran	–	–	4	–	104.0–116.0	58.0–60.0	18.0–19.0	12.0–13.0	Darvish et al. (2005)
Bulgaria	A	M	11	54.8 (11.7)	143.4 (19.6)	61.5 (4.5)	21.6 (1.6)	14.4 (2.8)	Metcheva et al. (2008)
	A	F	13	50.5 (12.2)	128.2 (17.0)	63.4 (9.1)	20.6 (1.3)	14.5 (3.0)

A – adult; J – juvenile; M – male; F – female; NI – no information.

Figure 2. Phylogenetic analysis of the Chionomys nivalis cyt-b gene 855-bp, considering the sequences retrieved from GenBank (see Table I) and the sequences obtained from the captured individuals. (A) Maximum clade credibility tree based on Bayesian coalescence genealogy of the 49 C. nivalis cyt-b sequences with BEAST (Table II). Values on branches indicate posterior probability support for the nodes (≥ 0.8). (B) Median-joining network of the C. nivalis cyt-b haplotypes. Each circle represents one haplotype, and circle size is proportional to the number of sequences of each haplotype. The number of nucleotide differences between haplotypes is indicated on branches. Letters indicate country codes: Adygea (RU-AD), Andorra (AD), Bulgaria (BG), Georgia (GE), Israel (IL), Italy (IT), Macedonia (MK), Portugal (PT; in dark grey), Romania (RO), Slovakia (SK), Slovenia (SI), Spain (ES), Syria (SY), Switzerland (CH), Turkey (TR) and Turkmenistan (TM).

Barbosa S, Paupério J, Searle JB, Alves PC. 2013. Genetic identification of Iberian rodent species using both mitochondrial and nuclear loci: Application to noninvasive sampling. Molecular Ecology Resources 13:43–56. doi:10.1111/1755-0998.12024.

 PubMed Web of Science ®Google Scholar

Jaarola M, Martínková N, Gündüz I, Brunhoff C, Zima J, Nadachowski A, Amori G, Bulatova NS, Chondropoulos B, Fraguedakis-Tsolis S, González-Esteban J, López-Fuster MJ, Kandaurov AS, Kefelioglu H, Luz Mathias M, Villate I, Searle JB. 2004. Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 33:647–663. doi:10.1016/j.ympev.2004.07.015.

 PubMed Web of Science ®Google Scholar

Galewski T, Tilak M, Sanchez S, Chevret P, Paradis E, Douzery EJP. 2006. The evolutionary radiation of Arvicolinae rodents (voles and lemmings): Relative contribution of nuclear and mitochondrial DNA phylogenies. BMC Evolutionary Biology 6:80. doi:10.1186/1471-2148-6-80.

 PubMed Web of Science ®Google Scholar

Castiglia R, Annesi F, Kryštufek B, Filippucci MG, Amori G. 2009. The evolutionary history of a mammal species with a highly fragment range: The phylogeography of the European snow vole. Journal of Zoology 279:243–250. doi:10.1111/j.1469-7998.2009.00612.x.

 Web of Science ®Google Scholar

Fink S, Fischer MC, Excoffier L, Heckel G. 2010. Genomic scans support repetitive continental colonization events during the rapid radiation of voles (Rodentia: Microtus): The utility of AFLPs versus mitochondrial and nuclear sequence markers. Systematic Biology 59:548–572. doi:10.1093/sysbio/syq042.

 PubMed Web of Science ®Google Scholar

Bannikova AA, Sighazeva AM, MAlikov VG, Golenishev FN, Dzuev RI. 2013. Genetic diversity of Chionomys genus (Mammalia, Arvicolinae) and comparative phylogeography of snow voles. Animal Genetics 49:561–575. doi:10.1134/S1022795413050025.

 Web of Science ®Google Scholar

Yannic G, Burri R, Malikov VG, Vogel P. 2012. Systematics of snow voles (Chionomys, Arvicolinae) revisited. Molecular Phylogenetics and Evolution 62:806–815. doi:10.1016/j.ympev.2011.12.004.

 PubMed Web of Science ®Google Scholar

LeLouarn H, Janeau G. 1975. Répartition et biologie du campagnol des neiges Microtus nivalis Martins dans la région de Briançon. Mammalia 39:589–604. doi:10.1515/mamm.1980.44.1.1.

 PubMed Web of Science ®Google Scholar

Luque-Larena JJ, López P, Gosálbez J. 2002. Microhabitat use by the snow vole Chionomys nivalis in alpine environments reflects rock-dwelling preferences. Canadian Journal of Zoology 80:36–41. doi:10.1139/z01-197.

 Web of Science ®Google Scholar

Pérez-Aranda D, Garrido García JA, Soriguer R. 2007b. Chionomys nivalis (Martins, 1842). Ficha Libro Rojo. In: Palomo LJ, Gisbert J, Blanco JC, editors. Atlas y Libro Rojo de los Mamíferos terrestres de España. Madrid: Dirección General de Conservación de la Biodiversidad-SECEM-SECEMU. pp. 410–414.

 Google Scholar

Luque-Larena JJ, López P, Gosálbez J. 2004. Spacing behaviour and morphology predict promiscuous mating strategies in the rock-dwelling snow vole, Chionomys nivalis. Canadian Journal of Zoology 82:1051–1060. doi:10.1139/z04-083.

 Web of Science ®Google Scholar

Darvish J, Siahsarvie R, Javidkar M, Mirshamsi O. 2005. New records of the snow vole Chionomys nivalis (Rodentia: Arvicolinae) from the Binaloud and Elburz Mountains of Iran. Acta Zoologica Cracoviensia 48:67–70. doi:10.3409/173491505783995716.

 Google Scholar

Metcheva R, Beltcheva M, Chassovnikarova T. 2008. The snow vole (Chionomys nivalis) as an appropriate environmental bioindicator in alpine ecosystems. Science of the Total Environment 391:278–283. doi:10.1016/j.scitotenv.2007.10.007.

 PubMed Web of Science ®Google Scholar