NORTH-WESTERN JOURNAL OF ZOOLOGY 14 (1) ©NWJZ, Oradea, Romania, 2018 CORRESPONDENCE - Notes http://biozoojournals.ro/nwjz/index.html

First records of melanism (including in tail bifurcation) of lacertid (Reptilia: ) in

Variations in skin coloration, including complete or partial melanism (a phenotype of increased black pigmentation) have been of interest for at least 130 years in lacertid lizards (Reptilia: Lacertidae) (Camerano 1886). Although widely documented for some lacertids in Europe (see Domeneghetti A. et al. 2016 and citations therein), until now, no published data exist for lizards with partial or complete melanism in Bulgaria. Here we present five unpublished cases from Bulgaria of two widely-distributed lacertid species exhibiting melanism. In Bulgaria, the European Green viridis (Laurenti, 1768) is found in diverse habitats generally up to B.

1,600 m a.s.l.; the Viviparous Lizard Zootoca vivipara (Lich- Figure 1. Partially melanistic female Lacerta viridis meridionalis tenstein, 1823) is a glacial relict at the southern edge of its (A. - left side; B. - right side). range, inhabiting the mountains above 1,400 m a.s.l. 1.) On 16.6.2005, around 10:30h, near Kostilkovo village in the Eastern Rhodopes mountain (41.42441°N, 26.06738°E; 282 m a.s.l.), GP closely observed (without catching or pho- tographing) a completely melanistic adult male L. viridis (likely meridionalis) in a sparse forest of Pubescent Oak Quer- cus pubescens. 2.) On 25.06.2015 NTz and YK were conducting a Figure 2. Partially melanistic Lacerta v. viridis with a bifurcated tail, mentioned in Stojanov et al. (2011). Photographed by Georgi Pop- herpetofaunal survey in the Natura 2000 Site of Community georgiev. Importance (SCI) “Emine - Irakli”, at the central part of the Black Sea coast. At around 13:45h, in a bright deciduous for- est dominated by Q. pubescens with sparse undergrowth, we tern (Brock et al. 2014). Thus, the cause for such extreme observed a basking adult female L. v. meridionalis change in coloration we present here is still to be identified. (42.74139°N, 27.88457°E; 83 m a.s.l.). What looked from a dis- Furthermore, since GP has observed and photographed tance like damaged scales, upon capture of the individual as well the individual from Stojanov et al. (2011) alongside and close inspection was identified as 10–15 irregularly- the authors, here we provide additional information. The shaped spots with black coloration (Fig. 1). Since we could subadult was observed on 2.05.2008, around 10:00h, near not discriminate any mechanical damage to the skin or the Zornitsa village, next to Studen Kladenets Reservoir scales, the spots were at multiple locations, and some scales (41.63081°N, 25.52371°E; 275 m a.s.l.), at the ecotone between had both normal and black coloration, we presume this was a sparse forest (Q. pubescens and Jerusalem thorn Paliurus caused by partial melanism. The coloration (besides the spina-christi) and an open grassland. melanistic spots) was typical for the subspecies. Four other All observations of L. viridis were within the zone where individuals of this taxon that were observed in the same both L. v. viridis, L. v. meridionalis and their hybrids are found survey had normal coloration. (Stojanov et al. 2011; Fig. 403). 3.) We note here a highly intriguing case of L. v. viridis 4., 5.) Additionally, we report two cases of complete with a bifurcated tail (Stojanov et al. 2011, Fig. 402). The au- melanism in Viviparous Lizards Z. vivipara, obtained during thors only mention the bifurcation in the figure caption, but an ongoing mark-recapture study in Vitosha Mountain, we include this observation here as the secondary tail also western Bulgaria. EV captured an adult male on 27.06.2016 bears signs of melanism (Fig. 2). Typically, in lacertids, the (42.59306°N, 23.28899°E; 1,828 m a.s.l.; body length: 48.5 re-growing tail after an autotomy differs from the original mm; tail length: 88.5 mm; weight: 2.72 g; Fig. 3) and a juve- not only in a replacement of the bone with cartilage but in nile on 29.09.2016 (42.60026°N, 23.28257°E; 1,821 m a.s.l.; coloration – ranging from paler to darker than the original body length: 30.0 mm; tail length: 43.5 mm; weight: 0.73 g; and usually with less patterning. We did not observe melan- Fig. 4). Thus, we add additional data on the occurrence of ism on the additional tail upon inspection of published im- melanism of Z. vivipara close to the southern extent of its dis- ages and descriptions of lacertids with bifurcated tails: e.g. a tribution, in addition to a female reported from Montenegro case of a Bosk’s Fringe-fingered Lizard Acanthodactylus (Iković et al. 2014). boskianus asper without a seeming change in coloration Except for the with the bifurcated tail, all other (Tamar et al. 2013); a Sand Lizard L. agilis with no change in individuals had intact tails and seemed in good body condi- color, and a Z. vivipara, with a slight change (Dudek & Ek- tion, with no signs of trauma or injuries. All captured ani- ner-Grzyb 2014); and an Erhard’s Wall Lizard Podarcis mals were released on site after pictures and measurements erhardii with a discolored tail lacking the black striped pat- were taken. Correspondence –Notes 143

discuss hypotheses (e.g. Camerano 1886, Werner 1897, Boulenger 1913, Arnold & Ovenden 2002, Korsós & Nagy 2006, Stošić 2014). On the other hand, for various popula- tions of Z. vivipara in Europe, different frequencies of melan- ism have been reported. Frequencies seem higher in males and very low to missing in females, respectively: 0.05% in Pyrenees (San-Jose et al. 2008), 1.13% in the Swiss Alps A. (Cavin 1999), 2.5% in Slovakia (5.9% in males, 0% in females; Jambrich & Jandzik 2012), 8.3% in Czech Republik (15% of all males, but only 2% of females; Gvoždík 1999, but see Boulenger 1917). The hypothesis that melanistic specimens have a thermoregulatory advantage has not been confirmed for the Viviparous Lizard, and decreased crypsis likely is strongly disadvantageous for gravid, slower females (Gvoždík 1999). Thus, the difference of between-population melanism frequencies could be linked either to different lev- B. els of predation pressure or to habitat specifics (e.g. some Figure 3. Adult melanistic Zootoca vivipara. (A. – dorsal view; microhabitats offer better opportunities for melanistic indi- B. – ventral view). viduals to avoid visual predators). Jambrich & Jandzik (2012) also support the idea that the different frequency of melan- ism in Z. vivipara can be linked to habitat quality. However, San-Jose et al. (2008) did not find any evidence of decreased body condition resulting from higher conspicuousness. However, the causes might be more complicated as, in male Z. vivipara, melanin-based ventral colouration may signal an aspect of immune capacity to sexual rivals or potential part- ners (Vroonen et al. 2013). Although we briefly review possible evolutionary driv- ers for melanism in lacertid lizards, due to the low sample size, the proximate causes in Bulgaria are yet to be deter- A. mined. With the increase of the amount and geographic range of the field data being obtained in Bulgaria, we expect that future studies might identify existing populations with higher frequencies of melanism that could be suitable for testing further ecological and genetic question.

Acknowledgements. We thank Borislav Naumov and two anonymous reviewers for suggestions that improved the manuscript. YK, GP, and EV dedicate this publication to NTz, a true friend that will always be with us.

References

Arnold, N., Ovenden, D. (2002): A field guide to the and amphibians of Britain and Europe. Harper Collins Publishers, London. Boulenger, E.G. (1913): Exhibition of a living melanistic specimen of the Green Lizard. Proceedings of the Zoological Society of London 1913: 546. Boulenger, G.A. (1917): On the variation of the common lizard, Lacerta vivipara. B. Journal of Zoological Research 2: 1–16. Brock, K.M., Belasen, A., Foufopoulos, J. (2014): Podarcis erhardii (Erhard’s Wall Figure 4. Juvenile melanistic Zootoca vivipara. (A. – dorsal Lizard). Bifurcated tail, post-autotomy. Herpetological Review 45: 332. view; B. – ventral view). Camerano, L. (1886): Descrizione di una Lacerta viridis (Laur.) melanica. Bollettino dei Musei di Zoologia e Anatomia Comparata della Regia Università di Torino I. The observations presented here are the only ones of Cavin, L. (1999): Obsérvations d’individus mélaniques chez le lézard vivipare. complete or partial melanism of lacertids that we know of in Bulletin de la Société Herpetologique de France 65–66: 76–78. Domeneghetti, D., Mondini, S., Bruni, G. (2016): Melanism and pseudo- Bulgaria. Based on our personal unpublished data, we pre- melanism in the Common Wall Lizard, Podarcis muralis Laurenti, 1768 sume that, in general, the frequencies of melanism in lacertid (Reptilia: Lacertidae) in central Italy. Herpetology Notes 9: 307–309. lizards in Bulgaria are very low (<0.01%): we have over 9,000 Dudek, K., Ekner-Grzyb, A. (2014): Field observation of two-tailed sand lizard Lacerta agilis Linnaeus, 1758 and a common lizard Zootoca vivipara (Jacquin, records of L. viridis from diverse locations, and 723 of Z. vi- 1787) in Poland. Natura Sloveniae 16: 65–66. vipara (including 329 from Vitosha). Gvoždík, L. (1999): Colour polymorphism in a population of the common The evolutionary significance of melanism in reptiles, lizard, Zootoca vivipara (: Lacertidae). Folia Zoologica 48: 131–136. and especially lacertids, still remains controversial and is Iković, V., Krasić, M., Gvozdenović, S. (2014): A record of melanistic viviparous lizard Zootoca vivipara (Lichtenstein, 1823 (Squamata, Lacertidae) on subject to debate. Observations of melanistic L. viridis are Prokletije Mountain, Montenegro. Hyla 2014: 41–44. few, mostly incidental and provide limited possibilities to Jambrich, A., Jandzik, D. (2012): Melanism in the topotypic population of the 144 North-Western Journal of Zoology 14(1) / 2018

Pannonian subspecies of the common lizard, Zootoca vivipara pannonica long and slender bodies (Costa et al. 2014, Crnobrnja- (Reptilia: Lacertidae). Herpetology Notes 5: 219–221. Isailović et al. 2016). Korsós, Z., Nagy, Z.T. (2006): Kurzbericht über ein vollständig melanotisches Exemplar der Smaragdeidechse, Lacerta viridis (Laurenti, 1768) in Ungarn. Here we describe the first observation of deliberate tail Die Eidechse 17: 42–46. loss, in the form of pseudoautotomy, in a viperid snake San-Jose, L.M., Gonzales-Jimena, V., Fitze, P.S. (2008): Frequency and species: Vipera ammodytes (the European nose-horned viper). phenotypic differences of melanistic and normally coloured common th lizards, Lacerta (Zootoca) vivipara of the Southern Pyrenees (Spain). The observation was made on the 13 of June, 2013, Herpetological Review 39: 422–425. during a survey of the herpetofauna from the Cerna river Stojanov, A., Tzankov, N.D., Naumov, B. (2011): Die Amphibien und Reptilien valley (south-western Romania; coordinates: 44.890 N, Bulgariens. Chimaira, Frankfurt am Main. Stošić, J. (2014): The first record of a melanistic Eastern Green Lizard, Lacerta 22.425 E) conducted by two of the authors (AS and PCD). viridis Laurenti, 1768 (Squamata, Lacertidae), in Croatia. Hyla 2014: 47–50. The habitat in which the observation took place comprises a Tamar, K., Maza, E., Meiri, S. (2013): Acanthodactylus boskianus (Bosk’s Fringe- westerly exposed slope with deciduous forest along a busy Fingered Lizard). Bifurcation. Herpetological Review 44: 135–136. Vroonen, J., Vervust, B., Van Damme, R. (2013): Melanin-based colouration as a road with rock reinforced sides. For all snake individuals potential indicator of male quality in the lizard Zootoca vivipara (Squamata: captured, we recorded their sex, age (adult or immature) as Lacertidae). Amphibia-Reptilia 34: 539–549. well as several morphometric traits (including body mass Werner, F. (1897): Die Reptilien und Amphibien Österreich-Ungarns und der [BM] and snout-vent length [SVL]). All measurments were Occupationsländer. Pichler's Witwe & Sohn, Wien. performed on site by the first author and all were Key words: Sauria, Lacerta viridis, Zootoca vivipara, color variations. released in their habitat of origin immediatly after processing. Article No.: e177501 One of the captured Vipera ammodytes indviduals was a Received: 30. January 2017 / Accepted: 08. October 2017 juvenile female (SVL= 210 mm, BM=13.8 g) that exhibited Available online: 09. February 2018 / Printed: June 2018 deliberate tail loss during handling. The snake was being held behind the head with one hand, and by the tail with the Yurii V. KORNILEV1,2,3,*, Georgi POPGEORGIEV1,3, other hand, without being stretched, when the viper Emiliya VACHEVA1 and Nikolay TZANKOV1,† exhibited a brief (ca. 1-2 seconds) series of strong contractions of the entire body, followed by a rapid and 1. Vertebrates Department, National Museum of Natural History, complete separation of the tail very close to the individual’s 1 Tsar Osvoboditel Blvd, 1000 Sofia, Bulgaria. 2. Department of Integrative Zoology, Vienna University, Althanstrasse 14, vent. Immediately after detaching, we observed slow, side- A-1090 Vienna, Austria. to-side movements of the tail for a short amount of time (less 3. Bulgarian Society for the Protection of Birds, PO Box 50, 1111 Sofia, Bulgaria. than a minute). No bleeding was observed. The detached tail * Corresponding author, Y. Kornilev, E-mail: [email protected] section, measuring 23.6 mm was preserved in 99.6% ethanol for further investigations. We determined the type of urotomy using X-ray imagery

(Fig. 1) and, subsequently, by exposing the first two Deliberate tail loss (pseudoautotomy) vertebrae from the separation point under a stereo in a viperid snake microscope (Carl Zeiss V.8; Fig. 2). Both techniques revealed intervertebral separation, thus characterizing Predation is one of the most powerful agents of selection and pseudoautotomy. Furthermore, X-ray imagery enabled us to animals have evolved a broad and diverse array of determine that the detached tail had 28 vertebrae (Fig. 1). adaptations for predator deterrence or avoidance (e.g. Lima To the best of our knowledge, our observation represents & Dill 1990, Meyer & Kassen 2007). These can range from the first comprehensive description of deliberate tail loss in a crypsis to aposematic signaling and from mimicry to viperid snake, in the form of pseudoautotomy. Although thanatosis or chemical defense (e.g. Stilling 2001). One more Kaufman & Gibbons (1975) mention individuals of North extreme adaptation is generally referred to as autotomy and American pit-vipers (Agkistrodon and Crotalus) and we have involves the deliberate loss of an appendage as a survival previously observed adult individuals of other Eurasian strategy, with the aim of distracting or confusing predators. viper species (Vipera ursinii and V. berus; unpublished data) This is a widespread phenomenon that was recorded both with incomplete tails, the exact circumstances responsible among invertebrates and vertebrates (Jagnandan et al. 2014). for tail loss remain unknown. Many viper species exhibit tail In reptiles, deliberate tail loss (known as urotomy) is a display behaviours, especially in the form of “caudal luring” common predator escape tactic, especially in the for attracting prey (e.g. Glaudas & Alexander 2017 and Rhynchocephalia and Squamata (Benton 2014, Crnobrnja- references therein), as well as tail vibrations that produce Isailović et al. 2016). Many groups of lizards are known to audible warnings for deterring potential predators, with (in exhibit deliberate tail loss, including in the form of Crotalus and Sistrurus) or without a specialized “rattle” (Allf autotomy, i.e. intravertebral breakage along specialized et al. 2016), and these behaviours can potentially lead to tail rupture plates, followed by regeneration of the tail (e.g. breakage (e.g. Crnobrnja-Isailović et al. 2016 & references Lazić et al. 2012). Snakes, on the other hand, are known to therein). On the other hand, these displays are potentially of exhibit only pseudoautotomy, i.e. intervertebral rupture of a highly important adaptive value, and tail loss might result the tail, not followed by regeneration, although observations in higher costs to individual fitness. However, although are far less frequent compared to lizards (Crnobrnja-Isailović brightly coloured tail tips are characteristic of Eurasian et al. 2016). Furthermore, deliberate tail loss was previously vipers of the genus Vipera (bright orange-red or green in the described only in species of three snake families (Colubridae, case of V. ammodytes, e.g. Fuhn 1969), and despite numerous Elapidae and Lamprophidae), all generally characterized by population studies having been conducted throughout their