Aberrant colouration in bats from Poland

NORTH-WESTERN JOURNAL OF ZOOLOGY 13 (2): 303-310 Article No.: e161703 ©NwjZ, Oradea, Romania, 2017 http://biozoojournals.ro/nwjz/index.html Aberrant colouration in bats from Poland Jan CICHOCKI1*, Grzegorz LESIŃSKI2, Krzysztof PIKSA3, Agnieszka WAŻNA1, Marcin WARCHAŁOWSKI1, Anna BATOR1, Iwona GOTTFRIED5, Tomasz GOTTFRIED4, Wojciech GUBAŁA6, Radosław JAROS7, Marek KOWALSKI8, Łukasz PŁOSKOŃ4, Tomasz POSTAWA9, Michał STOPCZYŃSKI10 and Rafał SZKUDLAREK4 1. Department of Zoology, University of Zielona Góra, Szafrana 1, 65-516 Zielona Góra, Poland 2. Faculty of Human Nutrition and Consumer Sciences, Warsaw University of Life Sciences – SGGW, Nowoursynowska 159 C, 02-787 Warszawa, Poland 3. Department of Vertebrate Zoology and Human Biology, Institute of Biology, Pedagogical University of Cracow, Podbrzezie 3, 31-054 Kraków, Poland 4. Polish Society of Wildlife Friends “pro Natura”, Podwale 75, 50-449 Wrocław, Poland 5. Department of Behavioural Ecology, University of Wrocław, Sienkiewicza 21, 50-335 Wrocław, Poland 6. Caves Protection Association „Malinka Group”, Fiedorowska 66, 43-460 Wisła, Poland 7. Polish Society for Nature Conservation "Salamandra", Stolarska 7/3, 60-788 Poznań, Poland 8. Wildlife Society „Stork”, Radomska 22/32, 02-323 Warszawa, Poland 9. Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Sławkowska 17, 31-016 Kraków, Poland 10. Ecologic, Radlińskiej 3/5, 91-848 Łódź, Poland *Corresponding author:, J. Cichocki, E-mail: [email protected] Received: 19. January 2016 / Accepted: 13. August 2016 / Available online: 19. September 2016 / Printed: December 2017 Abstract. During the last 60 years, 34 cases of aberrant colouration in bats of the following species have been recorded in Poland: Rhinolophus hipposideros, Myotis daubentonii, Myotis mystacinus, Myotis nattereri, Myotis myotis, Eptesicus serotinus, Barbastella barbastellus and Plecotus auritus. The largest number of aberrant colouration cases was recorded during the hibernation period in the Nietoperek bat reserve, western Poland (0.016% individuals with albinism). In 2014, five individuals with partial albinism and one flavistic bat were found there. Proportion of individuals with albinism varied from 0.05% in the case of M. nattereri, 0.02% in the case of M. daubentonii and only 0.007% in the case of M. myotis. During the studies on bat swarming in the Tatra Mountains one case of leucistic whiskered bat was recorded which accounts for 0.016% out of over 5,900 representatives of this species that were caught. Aberrant colouration in bats is rarely recorded in Poland and it is not associated with any particular geographical region. Higher probability of observing atypically coloured individuals occurs in large populations of bats. Key words: albinism, flavism, leucism, bats, Chiroptera, Poland. Introduction Aberrant colouration of bat skin and hair is recorded very infrequently. Atypical colouration depending on the level of melanin production deficiency can be classified as albinism, leucism or flavism. Albinism manifests itself by an absolute lack of melanocytes in the skin, fur and eyes. Leucism is characteristic of individuals with just one white part of the body without melanocytes. It is usually a small spot, sometimes it covers larger body areas. Some authors associate leucism with partial albinism (Bowman & Curran 2000, van Grouw 2006, Arriaga-Flores et al. 2016). Flavism manifests itself by yellow or red hair colour, lighter than normal. Flavistic individuals do not demonstrate albinistic features (Červený 1980). Flavism is not clearly defined and is sometimes called „rufous” (Ruprecht 1965), „brown” (van Grouw 2006, van Grouw 2013) or „yellow” (Nedyalkov et al. 2014, Čanády 2016). Another form of aberrant colouration is called melanism and is characterized by an increased content of dark pigment in various parts of the body. Pigmentation disorders are of genetic origin and are a kind of mutation (Červený 1980, Møller et al. 2013, Utzeri et al. 2015). Minor deficiencies in animal pigmentation may result from injuries such as frostbites. It is believed that partial albinism is more often found in small populations (Červený 1980, Bensch et al. 2000). During the recent years, there has been more and more information from all over the world regarding records of albino bats (Buys et al. 2001, Uieda 2001, Obada & Gas 2003, Marín-Vasquez et al. 2010, Sánchez-Hernández et al. 2010, Gaisler et al. 2011, Ramasindrazana et al. 2014, Romano et. al 2015, Zalapa et al. 2016) or bats demonstrating J. Cichocki et al. 304 partial albinism (Feng et al. 2007, Roncancio & Ramírez-Chaves 2008, Talerico et al. 2008, Boada & Tirira 2010, Satô 2011, Treitler et al. 2013, Muñoz-Romo et. al. 2014, Romano et. al 2015, Zalapa et al. 2016). There are exceptional descriptions of flavistic bats (Krzanowski 1958, Zamolo et al. 2013). In Europe, bats with atypical colouration are rarely observed. After the year 2000, albinism has been recorded for eight species of six genera: Plecotus auritus (Buys et al. 2001, Bator et al. 2008), Eptesicus serotinus (Obada & Gas 2003, Smirnov et al. 2014), Nyctalus noctula (Murariu & Chisamera 2006), Pipistrellus pygmaeus (Baucells et al. 2013), Pipistrellus nathusii (Smirnov et al. 2014), Rhinolophus hipposideros (Godlevska et al. 2005, Bartonička & Buřič 2007, Gaisler et al. 2011, Zamolo et al. 2013), Myotis mystacinus (Smirnov et al. 2014), Myotis myotis (Dietz et al. 2009). Partial albinism of M. myotis was observed in Germany (Haensel 1972) and in the Czech Republic (Červený 1980). Only one record is related to M. nattereri partial albinism (Haensel 1989). So far, atypical colouration of bats has been recorded in Poland several times. Albinism was recorded in the case of M. daubentonii (Uieda 2000, Gólski 2010). Leucism was recorded in the case of M. daubentonii in Nietoperek reserve, however the observations were not thoroughly described (Urbańczyk 1994), as well as in the case of P. auritus (Bator et al. 2008). Flavism was recorded in the case of P. auritus (Krzanowski 1958) and E. serotinus (Ruprecht 1965). The work aims at summarizing all available data on atypical colouration of bats recorded in Poland as well as assessing the frequency of colour aberration in bat populations. Materials and methods The information was collected from the whole territory of Poland during the hibernation period, during the trap capturing as well as the monitoring of breeding colonies. The observations included all bat species occurring in Poland. The analyses contained original data from 19802015. The research also included six observations of abnormal colouration in bats from Poland that were published by: Krzanowski (1958), Ruprecht (1965), Urbańczyk (1994), Uieda (2000), Bator et al. (2008) and Gólski (2010). The following definitions of aberrant colouration have been applied: 1. albino individuals: lack of pigment in the hair and skin, red eyes; 2. leucistic individuals: complete or partial lack of pigment in the hair, irregular white pieces of fur or sig- nificant lack of pigment in the skin, eyes coloured normally; 3. flavistic individuals: yellow or red fur differing from colouration that is typical for the species. This classification was based on Červený (1980), Zamolo et al. (2013) and Tello et al. (2014). Detailed research regarding occurrence of the anomalous colouration was conducted in the Nietoperek reserve. During the years 2013 to 2015 regular counts were conducted in the reserve’s area. The bats were not disturbed during the research and had no direct contact with humans. A detailed photo documentary was prepared. In total, 75,222 individuals from nine species were observed in the reserve during two research seasons. We determined the percentage of individuals with aberrant colouration among the bats hibernating in Nietoperek as well as in other populations for which the data on population numbers was available. The statistical significance of differences in the number of colour aberrations within each species was analyzed using the χ2 test (independent distribution). By using the χ2 test (test compliance with uniform distribution), the frequency of anomalous colouration in individual species was also checked. The differences in proportions in the occurrence of anomalous colouration in the two species in which these aberrations are most often observed (M. myotis and M. nattereri) were tested by using the test of equal proportion. For the calculations, the R program (R Core Team 2014) was used. Results During the past 60 years, 34 cases of atypical bat colouration have been recorded in Poland (Table 1, Fig. 1-3). Aberrant colouration was recorded in the case of eight species from five genera Rhinolophus, Myotis, Eptesicus, Barbastella and Plecotus. The majority of individuals with atypical colouration (67%) demonstrated leucistic features (Fig. 4). Complete albinism was recorded five times. Three individuals of M. daubentonii, one R. hipposideros and one E. serotinus were recorded. Partial albinism was recorded in the case of 23 bats. The observed individuals demonstrated the following features: lack of pigment in the skin, lack of pigment in the wing membrane, white wing ends, wings and ears deprived of pigment, distinct white spots or completely white fur with dark wings. Flavism was recorded four times in the case of M. myotis. Three atypically coloured bats of this species were observed in the same hibernaculum. Single flavistic individuals of E. serotinus and P. auritus were recorded (Table 1). Six leucistic individuals of M. nattereri were recorded in the territory of Poland out of which Aberrant colouration in bats in Poland 305 Table 1. Observations of aberrant colourations of bats in Poland in the years 1956-2015. Species Rhinolophus hipposideros Myotis daubentonii Myotis mystacinus Myotis nattereri Myotis myotis Eptesicus serotinus Barbastella barbastellus Plecotus auritus Total Number of individuals 1 1 1 2 1 1 1 1 1 1 1 1 1 1 3 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 34 Locality Period Date Sławniowice1 Adit Barbara1 Jaworki2 Nietoperek3 Warszawa5 Nietoperek3 Nietoperek3 Cave Wielka Litworowa4 Warszawa5 near Nietoperek3 Cave Skamieniała6 Nietoperek3 Nietoperek3 Nietoperek3 near Modlin5 Nietoperek3 Nietoperek3 Rościszów7 Nietoperek3 Nietoperek3 Cave Z Filarami8 Nietoperek3 Nietoperek3 Białowieża12 Warszawa5 Śniaty9 Cave Jasna10 Puławy5 Działdowo13 Cave Diabla Dziura6 Cave Niedźwiedzia11 H H BC H ? H H C H BC C H H H H H H BC H H H H H C H BC C H H C C 2013.02.14 2013.12.17 2014.07.11 1985 1985 before 1994 2014.03.21 2001.08.15 1985 1985 2008.10.22 2012.01.11 2014.01.12 2014.12.06 2011.03.18 11.2013-03.2014 11.2013-03.2014 2014.06.18 2014.11.15 11.2014-03.2015 2015.03.06 2015.11.06 2015.11.26 1962.10.26 1995 2002.08 2008.08.20 1956.03.15 2005.02.06 2006.08.09 2007 Colouration anomaly leucism leucism albinism albinismV albinismVI leucismIII leucism leucism leucism leucism leucism leucism leucism leucism flavism leucism leucism leucism leucism leucism leucism leucism flavism flavismII leucism albinism leucism flavismI leucism leucismIV leucism Abbreviations: H – hibernation, C – capturing, BC – breeding colonies. IKrzanowski 1956, IIRuprecht 1965, IIIUrbańczyk 1994 IVBator et al. 2008, VGólski 2010, VIUieda 2000. Geographical location: 1Sudety Foothills, 2Pieniny Mountains, 3Lubuskie Lakeland, 4Tatra Mountains, 5Mazovian Lowland, 6Ciężkowickie Foothills, 7Sowie Mountains, 8Kamienne Mountains, 9Leszczyńskie Lakeland, 10Dynowskie Foothills, 11Beskidy Mountains, 12Północnopodlaska Lowland, 13Północnomazowiecka Lowland Figure 1. Albino individuals a) Rhinolophus hipposideros (Jaworki, photo by R. Szkudlarek) and b) Eptesicus serotinus (Śniaty, photo by R. Jaros). J. Cichocki et al. 306 Figure 2. Leucistic individuals from Nietoperek Reserve: Myotis nattereri a) photo by I. and T. Gottfried, b) photo by T. Postawa, c) photo by M. Warchałowski, Myotis daubentonii d) photo by M. Warchałowski and Myotis myotis e) photo by J. Cichocki, f) photo by M. Warchałowski. Figure 3. Leucistic individuals: Barbastella barbastellus a) Cave Jasna, photo by W.J. Gubała, Plecotus auritus b) Działdowo, photo by M. Kowalski, Rhinolophus hipposideros c) Adit Barbara, photo by Ł. Płoskoń, f) Sławniowice, photo by R. Szkudlarek. Flavistic individuals Myotis myotis d) near Modlin, photo by G. Lesiński e) Nietoperek, photo by M. Grzelczak. Figure 4. Percentage of recorded aberrant colouration in bats in Poland in the years 1956-2015. four were observed in the Nietoperek reserve. In general, seven leucistic individuals of M. myotis were recorded. Two individuals hibernated in the Nietoperek reserve at the same time as M. nattereri. The third individual was recorded in the breeding colony in the same reserve. Due to the fact that this colony of M. myotis is located in the same area where the bats overwinter, it cannot be ruled out that this one was among the individuals observed during winter. During the research on bat swarming in the Tatra Mountains, one leucistic Aberrant colouration in bats in Poland M. mystacinus was recorded. Atypical colouration was recorded most often during winter bat counts (23 individuals), in the breeding colonies (4 individuals), caught in traps (6 individuals). Aberration was most frequently recorded in the case of M. myotis (11 individuals), M. nattereri (6 individuals), M. daubentonii (5 individuals), P. auritus (4 individuals). One to three single atypically coloured individuals were recorded in the case of R. hipposideros, M. mystacinus, E. serotinus and B. barbastellus (Fig. 5). Relatively high proportion of flavistic individuals occurred in M. myotis while in M. daubentonii, the albinism was recorded relatively frequently – three times (Fig. 6). Figure 5. Records of atypically coloured bats in Poland in the years 1956-2015 (N = 34). During the winter season 2013-2014, in the hibernaculum in Nietoperek reserve, four atypically coloured individuals were recorded (N = 36,628) which accounts for 0.01% of all individuals wintering in the reserve. During the winter season 20142015, three atypically coloured individuals were recorded (N = 38,594) which accounts for 0.008% of all individuals wintering in the reserve. The percentage of atypically coloured individuals is not much different from the aforementioned number in the case of M. myotis, M. daubentonii and M. nattereri (Table 2). The number of reported cases of colour aberration is independent of species (χ2 = 19.7, df = 14, p = 0.14). Therefore, we can assume that the number of different anomalous forms of colouration is proportional to the size of the observed population. Distribution analysis of anomalies in colouring indicates a significantly different frequency of three aberrations (χ2 = 18.1, df = 2, p = 0.0001). Most often occurs leucism. Other aberrations, albinism and flavism, are much rarer. Comparison of the two fractions shows there 307 are no statistically significant differences between the species M. myotis and M. nattereri (Test of proportion χ2 = 1.0, df = 1, p = 0.294). Discussion In the 1980s and 1990s in Europe, many cases of anomalies in bat colouration were recorded. These included both albino individuals and individuals with partial albinism (Červený 1980, Lehnert 1991, Laar 1994, Urbańczyk 1994, Weidner 1994, Zukal et al. 1994, Danko 1995, Uieda 2000). In the recent years, individuals with atypical colouration have been described in Europe less and less often. The only species in the case of which anomaly of colouration can be observed regularly is R. hipposideros (Godlevska et al. 2005, Bartonička & Buřič 2007, Gaisler et al. 2011, Zamolo et al. 2013). In Poland, this species inhabits limited area in the southern part of the country in the mountains and foothills. So far, atypically coloured individuals of M. myotis have not been recorded in Poland. Since the beginning of the 1990s, M. myotis has been the most numerous species wintering in the Nietoperek reserve (Urbańczyk 1994). In January 2014, over 27,000 M. myotis and 3,500 M. nattereri hibernated in the reserve. Low percentage of atypically coloured bats in the small hibernating population decreases the possibility of finding an atypically coloured individual. Similar observations come from the Czech Republic where the participation of individuals with partial albinism concerned only three individuals out of 20,000 (Červený 1980). In the research on Tadarida brasiliensis, it has been stated that one bat in 3-4,000 is leucistic. The frequency of individuals with white fur amounted from 0.25%, in the case of males, to 0.36%, in the case of females (Herreid & Davis 1960). Červený (1980) described the population of B. barbastellus in which the frequency of individuals with partial albinism can be regionally very high, from 2.19% (N = 1,002) to 12.6% (N = 103), which he ascribed mainly to the low total number of bats. In our study, one B. barbastellus with partial albinism has been recorded in southern Poland in the close proximity to the sites described by Červený (1980). Some of the colour aberrations such as melanism may concern almost 4% of the population (Dekeukeleire et al. 2013). Melanism is regarded as a kind of evolutionary adjustment to environmental conditions rather than a consequence of a J. Cichocki et al. 308 Figure 6. Aberrant colouration in bat species in Poland in the years 1956-2015 (N = 34). Table 2. Percentage of atypically coloured individuals in the total number of bats in the years 2013-2015. Species Myotis nattereri Myotis nattereri Myotis daubentonii Myotis myotis Myotis myotis Myotis mystacinus Rhinolophus hipposideros Site Period Nietoperek H1 Nietoperek H2 Nietoperek H1 Nietoperek H1 Nietoperek H2 Tatra Mts C3 Southern Poland BC-H4 Recorded population number (N) 3,560 3,590 4,081 27,669 29,111 5,900 10,000 Number of atypically coloured individuals (N) 1 1 1 2 2 1 3 Percentage of atypically coloured individuals (%) 0.03 0.03 0.02 0.007 0.007 0.017 0.03 Abbreviations: H – hibernation, C – capturing, BC – breeding colonies. 1winter 2013-2014; 2winter 2014-2015; 31999-2005; 42014-2015 disease (Maierus & Mundy 2003). During our observations no melanistic individuals were recorded. Similarly, it is very rare to observe flavistic individuals. It may also be a result of difficulties in observing atypically coloured individuals. Changeability of colouration in the case of M. myotis is quite high, especially in relation to young and older individuals. A yellow individual in a cave with artificial light is difficult to spot. We had similar problems while describing M. daubentonii which looks like covered with water drops. This is a common phenomenon observed in hibernating bats of this species. It is not until a closer look that one can see that the fur colour is not the result of water drops. In the 1980s, individual cases of atypically coloured, creamy individuals of M. daubentonii were recorded in the Nietoperek reserve (Urbańczyk 1994). In the case of individuals with albinism or partial albinism such problems usually do not occur. It seems that predators are more interested in white-coloured animals (Slavik et al. 2015). Kestrel's Falco tinnunculus attack on an albino bank vole Myodes glareolus was observed (Steen & Sonerud 2012). However, in the case of bats some of the species choose hideouts that are hard to access. The information about the albino Myotis sodalis which lived seven years is well known (Brack & Johnson 1990). Other authors share observations according to which albino bats live about three years (Caire & Thies 1988). Some of the tropical bat species such as ghost bats Diclidurus are completely white. According to Uieda (2000), light colouration in the case of bats inhabiting rainforests increases the chance of survival. One of the two leucistic individuals of M. myotis was observed during two hibernating periods in the Nietoperek reserve. There is no complete certainty whether or not this was the same individual. E. serotinus was also observed in the breeding colony for two seasons. Atypically coloured bats demonstrate certain common features in colour anomalies. M. nattereri from Warsaw lacked pigment in its ears and wings. Similar case was described for M. daubentonii from Holland at the end of the 1980s (Bekker 1989). There is also one known individual of Myotis frater from Japan with reduced pigmentation in ears and skin of wings and tail (Satô 2011). Similarly, the described P. auritus was character- Aberrant colouration in bats in Poland ized by the lack of pigmentation in the skin. The observations of lack of pigmentation in the skin are less frequent because they cannot be seen during the hibernation. The awakening of an individual would have been necessary. The recording of bats with complete or partial albinism and their frequency may have significant meaning for examining the population condition. The presented comparison shows a very small participation of albino individuals in bat populations. Bats are long-lived animals and some species usually inhabit limited areas. It is relatively easy to survey winter colonies. Greater participation of individuals with partial albinism may be a motivation for more detailed research on habitat of bats, e.g. water pollution. Within the area around Chernobyl, an increased partial albinism of birds was recorded (Møller et al. 2013). Bats belong to a group of mammals that are particularly prone to carcinogenic factors due to the selection of hiding places, e.g. wintering sites in the uranium mines, sites with polluted water. Basements, old forts or mines in central Europe were often used in the 1980s and 1990s as waste dumps. The increased number of observations in the 1970s and 1980s might have been directly linked to environmental pollution. It could have been also influenced by significant decrease in the population number of bats and formation of smaller isolated populations (Červený 1980). It is also possible that such observations were not published as they were regarded uninteresting and had a local importance. However, the lack of more precise research does not allow drawing more accurate conclusions in that matter. Acknowledgments. We are grateful to Prof. W. Bogdanowicz, M. Grzelczak, J. Gulatowska, M. Ignaczak, A. Kościelska, L. Koziróg, S. Menderski, G. 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