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Mammalia

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Volume 81, Issue 6

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Anomalous coat colour in the fat dormouse (Glis glis): a review with new records

Anežka Holcová-Gazárková
  • Corresponding author
  • Department of Zoology, Faculty of Science, Palacký University, tř. 17. listopadu 50, Olomouc, CZ-771 46, Czech Republic
  • Department of Biology, Faculty of Education, Palacký University, Purkrabská 2, Olomouc, CZ-771 40, Czech Republic
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/ Boris Kryštufek / Peter Adamík
  • Department of Zoology, Faculty of Science, Palacký University, tř. 17. listopadu 50, Olomouc, CZ-771 46, Czech Republic
  • Museum of Natural History, nám. Republiky 5, Olomouc, CZ-771 73, Czech Republic
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Published Online: 2016-12-08 | DOI: https://doi.org/10.1515/mammalia-2016-0122

Abstract

We reviewed the available records on aberrantly coloured fat dormice Glis glis and are reporting on two recent cases of flavistic males. We identified five colour variants among nearly 11,000 dormice from throughout their range in Europe and Asia (of these 6174 from Slovenia and Croatia, and 3493 from the Czech Republic). Flavistic dormice come from Slovenia and Czechia (two cases each) while all the remaining colour variants were recorded in Slovenia between 1860 and 2012: melanistic (20 inds.), albino (7 inds.), isabellinus (4 inds.), and individuals with white tail stripes (five cases). The two flavistic individuals from Czechia were captured during a demographic study. Interestingly, the aberrant pelage was gained by both males later in life as in the years of first encounter they had the typical greyish coat colouration.

Keywords: albinism; edible dormouse; flavism; melanism; small mammal

Introduction

Pelage colour provides a series of functions for mammals and is likely to be under strong selection pressure. Colouration is caused by the presence or absence of melanin pigment in hairs, the skin and an iris of the eye (Searle 1968). Melanin is synthesised in melanocytes and its synthesis is controlled by several genes. Their mutation causes decreased function of the tyrosinase enzyme, which catalyses the first step necessary in melanin synthesis, oxidation of tyrosine to dopaquinone. This mutation of the tyrosinase gene is associated with albinism (Barsh 2001). There are three different types of albinotic phenotype – complete albinism with red eyes and pink skin, leucism with unchanged colour of eyes and white skin, and partial albinism. The red or yellow hair colouration, known as flavism, is associated with the production of pheomelanin. The appearance of a dark phenotype with an increased quantity of eumelanin in melanocytes is determined as melanistic (Kingsley et al. 2009; Barsh 2001). Melanocytes could switch between the synthesis of the two types of pigments.

The reason for the low prevalence of albinotic, flavistic or melanistic phenotypes in natural populations is caused by an autosomal recessive pattern of inheritance. The probability of the expression of recessive alleles is higher in small, isolated, inbred populations with low genetic variability and in populations restricted in size after a bottleneck or founder effect (Stangl et al. 1995, Bensch et al. 2000). Some authors claim, for example, that in water voles Arvicola Lacepede 1799 or in common hamsters Cricetus cricetus Linnaeus 1758 the frequency of pelage anomalies is linked to stressful conditions or population abundance (Potapov et al. 1998, Kayser and Stubbe 2000). Animals with aberrant pelage are likely to be under strong pressure from predators (Jehl 1985, Brewer et al. 1993). For example, albinotic fat dormice Glis glis Linnaeus 1766 do not survive their first year, which contrasts with survival in naturally coloured individuals (Kryštufek and Flajšman 2007, Lebl et al. 2011). Typical fat dormouse pelage is grey to greyish-brown on upperparts including the head and the tail, while the underparts and the inner surface of legs are whitish (Kryštufek 2010). The iris of the eye is black. Here we review cases of colour aberrations in fat dormice and report on two recent cases of flavism from the east Czech Republic.

Materials and methods

The review of cases of coat colour anomalies was based on checking museum skins (see Acknowledgements for museum collections) and catalogues of the Slovenian Museum of Natural History (hereafter PMS), examinations of dormice captured by traditional hunters in hunting areas south of Ljubljana in Slovenia and adjacent Croatia, their records and private collections of taxidermic mounts, and dormice individually marked during population monitoring in montane forests of European beech (Fagus sylvatica) and fir (Abies alba) in the area around Kočevje, Slovenia (1998–2015; n=1256) and in a deciduous forest on the Island of Cres, Croatia (2011–2013; n=298). Whenever possible, individuals were classified into one of two age categories: juvenile (before the first hibernation) and adult (after the first hibernation). We supplement these records with two recent cases recorded in the Czech Republic. Since 2005 we have been intensively studying fat dormice occupying nest boxes near Dlouhá Loučka, Nízký Jeseník (49°49′N, 17°12′E) in NE Czechia. The study site represents a managed mixed deciduous forest with the dominant tree species being sessile oak (Quercus petraea) and European beech. All newly captured dormice were individually marked with subcutaneously injected passive integrated transponders (Trovan, ID 162 Isonorm). For details on field procedures see Lebl et al. (2011), Kukalová et al. (2013), and Holcová Gazárková and Adamík (2016).

Results

In total we checked nearly 11,000 edible dormice: 127 samples from Western Europe (England, France, Spain, Switzerland), 3798 from Central Europe (Austria, Czech Republic, Germany, Hungary, Moldova, Poland, Romania, Slovakia), 53 from Eastern Europe (Ukraine, Russia), 7147 samples from southeastern Europe (Bosnia and Herzegovina, Bulgaria, Croatia, Greece, Kosovo, Macedonia, Montenegro, Serbia, Slovenia, European part of Turkey), and 68 from southwestern Asia, including the Caucasus (Armenia, Azerbaijan, Daghestan, Georgia, Iran, Turkey in Asia, Kabardino-Balkaria in Russia). Aberrant pelage in dormice was found in samples from Slovenia and the Czech Republic. There are 20 records of melanistic individuals, seven records of albinos, four records of issabelinus dormice (Figure 1), four flavistic records and five cases of individuals with ordinary pelage but white tail stripes. Melanistic dormice were captured between 1860 and 2012 in south-central Slovenia. Four individuals originate from the 19th century, and the remaining were obtained during and after the 1990s. We saw 14 skins, seven of which are deposited in PMS (collection # 18441, 18775, 19183, 21954, 21955, 22001, 24369). The dorsal side is typically the darkest, and the belly is greyish black. Ears are light grey, the snout, lips, manus and fingers of the hind foot are whitish. Typically, there was a white chin strike of variable size (Figure 1A). The body mass of eight melanistic dormice was 70–189 g, hence the material includes both the juveniles in their first year and the individuals which overwintered at least once. All melanistic individuals are from beech and fir forests from an area of <2000 km2; the exact origins of the two individuals collected before 1860 (documented in PMS) and another pelt from a fur market is not known with certainty.

(A) Museum skin of a melanistic fat dormouse in dorsal and ventral view. Juvenile female (body mass=133 g), captured on 2 October 2011 in Mt. Hrušica, Slovenia (45°52′ N, 14°11′ E). Slovenian Museum of Natural History PMS 19183. Photo courtesy of Ciril Mlinar. (B) Taxidermic mount of an albinistic dormouse. Juvenile male (body mass=52 g), captured 24 September 1999 in Polom, Slovenia (45°44′ N, 14°51′ E). The patch on the hip is due to dirt. Private collection. Photo courtesy of Alenka Kryštufek. (C) Taxidermic mount of an isabelline dormouse. Juvenile male (body mass=109.5 g) capture in autumn 1999 in south-central Slovenia. Exposed to light, photographed in 2016. Private collection. Photo courtesy of Alenka Kryštufek.
Figure 1:

(A) Museum skin of a melanistic fat dormouse in dorsal and ventral view.

Juvenile female (body mass=133 g), captured on 2 October 2011 in Mt. Hrušica, Slovenia (45°52′ N, 14°11′ E). Slovenian Museum of Natural History PMS 19183. Photo courtesy of Ciril Mlinar. (B) Taxidermic mount of an albinistic dormouse. Juvenile male (body mass=52 g), captured 24 September 1999 in Polom, Slovenia (45°44′ N, 14°51′ E). The patch on the hip is due to dirt. Private collection. Photo courtesy of Alenka Kryštufek. (C) Taxidermic mount of an isabelline dormouse. Juvenile male (body mass=109.5 g) capture in autumn 1999 in south-central Slovenia. Exposed to light, photographed in 2016. Private collection. Photo courtesy of Alenka Kryštufek.

Albinistic dormice were obtained between 1861 and 2011 from the same area as the melanistic animals. Six albinos were seen, four of them before they were skinned, and they all had pink eyes. All animals were entirely white (Figure 1B). The body mass of two individuals was 52 and 118 g, respectively, suggesting that they were both less than a year old. The remaining albinos were also classified with certainty as juveniles.

Four individuals were light grey washed buffy and are classified as isabellinus (Figure 1C). They were all captured in the last decades of the 20th century in the same area as the melanistic animals. Three of them were juveniles while the age of the remaining animal could not be ascertained. Five male skulls in PMS (collection nos. 11866, 11872, 12125, 12126, 12299) bear a label note that tails had oblique white stripes on the tail. At least some of them were adults (body mass 120.5–184.2 g). These animals were from the same area as the melanistic ones.

Four dormice are classified as flavistic, although they were not of exactly the same colour. Two flavistic dormice from Mt. Krim, central Slovenia (45°55′ N, 14°28′ E) were examined in August 2000 after being exposed to light for decades. They were yellowish but lacked the grey tone of the isabellinus type. Both specimens were in a private collection and could no longer be traced as of 2016. In any case, they were lighter in colour than the two Czech animals. Two additional cases of flavism were recorded in Czechia during long-term population monitoring of the fat dormouse. Between 2005 and 2015 we marked 3493 individual dormice (juvenile numbers not included). Only two of the captured dormice had aberrant colouration. Both individuals showed signs of flavism when the entire coat was golden (Figure 2). Skin and eye colouration were the same as in typical fat dormice. The first male was captured as a juvenile in 2011. In 2012 it was recaptured with ordinary grey pelage. In 2013 it was again recaptured but this time with aberrant pelage (Table 1). The second male was first captured in 2014 with ordinary grey pelage after its first hibernation. It was in the next year when this individual was found in aberrant gold pelage. Interestingly both individuals were caught in the same nest box.

Two aberrantly coloured fat dormice males found in Nízký Jeseník, Czech Republic. The upper two figures are of a male recorded in 2013 (photo courtesy of Igor Magál), the lower two figures are for a male recorded in 2015 (photo courtesy of Vladislav Holec).
Figure 2:

Two aberrantly coloured fat dormice males found in Nízký Jeseník, Czech Republic.

The upper two figures are of a male recorded in 2013 (photo courtesy of Igor Magál), the lower two figures are for a male recorded in 2015 (photo courtesy of Vladislav Holec).

Table 1:

Capture histories of the two fat dormice with aberrant colour.

In conclusion, all colour variants were recorded among 6310 dormice from Slovenia and 3493 dormice from Czechia. No variants were observed among the 1313 dormice from the rest of Europe and 68 skins from southwestern Asia. This material also included insular dormice, specifically 401 individuals from the small Adriatic islands of Croatia, 16 from Sicily and Sardinia, and 41 from England. We also asked colleagues who ran field studies on dormice in Austria, Germany and Lithuania for records of aberrantly coloured individuals (C. Bieber, J. Fietz, and R. Juškaitis, pers comm) but none of them recorded any such cases.

Discussion

Aberrantly coloured individuals were observed in a wide range of mammalian taxa such as rodents, insectivores, bats and carnivores (e.g. Little 1958, Pucek 1964, Borowski 1973, Michalak 1986, Baláž et al. 2007, Acevedo et al. 2009, Lopucki and Mróz 2010). Across the different species of mammals such as bats, insectivores, rodents or seals, the most commonly observed colouration anomalies were partial albinism or leucism (Pucek 1964, Michalak 1986, Acevedo et al. 2009, Lopucki and Mróz 2010, Abreu et al. 2013, Nedyalkov et al. 2014). For example, leucism in common hamsters Cricetus cricetus (Kayser and Stubbe 2000), and in field mice Apodemus flavicollis Melchior 1834 and Apodemus agrarius Pallas 1771 (Lopucki and Mróz 2010), or partial albinism in mice (Čanády 2015) were observed most often. Abreu et al. (2013) recorded 198 cases of pelage anomalies in their review of Neotropical mammals. Among them albinos or partial albinos (piebaldism) were reported most often. The most common records of melanistic individuals were reported for common hamsters, bank vole Myodes glareolus Schreber 1780, common vole Microtus arvalis Pallas 1778 (Bobek and Bartke 1967, Mäkelä and Viro 1980, Kocian and Žiak 1992, Baláž et al. 2007, Lopucki and Mróz 2010, Kryštufek et al. 2016), and rarely for the bicoloured white-toothed shrew Crocidura leucodon Hermann 1780 (Baláž et al. 2007). Interestingly, in the common hamster some populations were reported to have an unusually high proportion of melanistic individuals – up to 50% in Thuringia (Zimmermann 1969) and around 80% in Ukraine and Bashkortostan, Russia (Berdyugin and Bolshakov 1998). Albinism seems to be less often reported than melanism. Frequent reports on albinism occur in moles Talpa europea Linnaeus 1758 (Lopucki and Mróz 2010, Nedyalkov et al. 2014). Judging from the scarcity of reports on flavistic individuals it seems that this anomaly is probably least frequent in nature. The few observations, for example, report on one case each of a lesser horseshoe bat Rhinolophus hipposideros Bechstein 1800 (Zamolo et al. 2013) stripped field mouse A. agrarius (Čanády 2016), and steppe mouse Mus spicilegus Petényi 1882 (Čanády et al. 2008). In the common Muscardinus avellanarius Linnaeus 1758 and forest dormouse Dryomys nitedula Pallas 1778 only melanistic individuals were observed, but with unknown frequencies (Pilyavskii and Abelentsev 1979, Juškaitis and Büchner 2013, Augustin 2016). In addition, in common dormouse individuals with white-tipped tails occur in low frequency but across multiple sites in Europe (Juškaitis 2014). At one Lithuanian site up to 19% of common dormice had white tail tips (Juškaitis 2001). Lang et al. (2016) recorded one partial albino common dormouse in Hesse, Germany.

Our review of cases shows that it is most likely that melanistic fat dormice occur with the highest frequency. No colour variants were observed among 458 insular dormice. Our results therefore do not support the generalisation on the higher probability of the expression of the recessive alleles responsible for colour variants in a population which has lost genetic variability due to the founder effect (cf. Stangl et al. 1995, Bensch et al. 2000). However, we have a lack of samples for other colour variants in this species. It is perhaps not surprising that nearly all the cases of colour variants originate from the area of traditional dormice hunting in south-central Slovenia, where tens of thousands animals are trapped during years when dormice reproduce (Kryštufek and Flajšman 2007). Similarly, our knowledge of colour polymorphism in the common hamster also benefited from pelt markets which were annually supplied by hundreds of thousands of skins (cf. Kryštufek et al. 2016).

Our two cases of flavistic individuals which changed their pelage later during their life add to the diversity of pelage types. To date such a change in pelage was described in fruit bats Artibeus jamaicensis Leach 1821 from Yucatan, Mexico (Macswiney et al. 2012). We do not know whether in our case the dormice fed on a particular diet that could have led to a change in pelage after moult as was the case in fruit bats.

Acknowledgements

We wish to thank Igor Magál, Márie Mozgová, Stanislav Chlebus, Monika Kukalová, Vladislav Holec and Michaela Pupíková for their help with field work in Czechia and to Andrej Hudoklin, Stane Kumelj, Marjan Zavodnik, Andrej Zavodnik, and other traditional dormice hunters in Slovenia for providing information and specimens. Claudia Bieber, Joanna Fietz, and Rimvydas Juškaitis kindly shared their observations on pelage in their study populations. Access to museum collections was granted by (abc) Petr Benda (National Museum, Prague, Czech Republic), Alexandra N. Davydova (Zoological Institute and Zoological Museum, Russian Academy of Sciences, St. Petersburg, Russia), Linda Gordon (National Museum of Natural History, Washington DC, USA), Barbara Herzig-Straschil (Naturhistorisches Museum Wien, Vienna, Austria), Rainer Hutterer (Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany), Paula Jenkins (Natural History Museum London, UK), Richard Kraft (Zoologisches Staatssammlung München, Munich, Germany), Katrin Krohmann (Senckenberg Forschungsinstitut und Naturmuseum Frankfurt a. M., Germany), Milan Paunović (Natural History Museum of Serbia, Belgrade, Serbia), and †William Stanley (Field Museum of Natural History, Chicago, USA). Karolyn Close improved English and style. This study was partly supported by grant scheme for graduate students (IGA PrF) of Palacký University.

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About the article

Received: 2016-08-30

Accepted: 2016-10-25

Published Online: 2016-12-08

Published in Print: 2017-10-26


Citation Information: Mammalia, Volume 81, Issue 6, Pages 595–600, ISSN (Online) 1864-1547, ISSN (Print) 0025-1461, DOI: https://doi.org/10.1515/mammalia-2016-0122.

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