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Home , Caudal luring, Ladder snake, Vipera, Vipera ammodytes, Vipera latastei

144 North-Western Journal of Zoology 14(1) / 2018

Pannonian of the common , Zootoca vivipara pannonica long and slender bodies (Costa et al. 2014, Crnobrnja- (Reptilia: Lacertidae). 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 San-Jose, L.M., Gonzales-Jimena, V., Fitze, P.S. (2008): Frequency and : ammodytes (the European nose-horned viper). phenotypic differences of melanistic and normally coloured common th , Lacerta (Zootoca) vivipara of the Southern (). 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 ; 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 (, Lacertidae), in . 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 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, 1 Tsar Osvoboditel Blvd, 1000 Sofia, . complete separation of the tail very close to the individual’s 2. Department of Integrative Zoology, Vienna University, Althanstrasse 14, vent. Immediately after detaching, we observed slow, side- A-1090 Vienna, . to-side movements of the tail for a short amount of time (less 3. Bulgarian Society for the Protection of , 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 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 to aposematic signaling and from 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 ( 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 , 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). , 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 Vipera (bright orange-red or green in the described only in species of three snake families (, case of V. ammodytes, e.g. Fuhn 1969), and despite numerous and Lamprophidae), all generally characterized by population studies having been conducted throughout their Correspondence –Notes 145

In conclusion, our observation shows that deliberate tail loss can occur in shorter bodied and shorter tailed snakes, such as vipers, and suggest that other observations of tail breakage in these snakes may also be the result of pseudoautotomy.

Acknowledgements. The field survey was self-funded by the first two authors. The realization of X-Ray imagery was funded by the Moldavica Herpetological Group. We are grateful to dr. Ș. Strungaru for his help in using the binocular microscope, and to dr. J. Crnobrnja-Isailović for helpful discussions on the topic of pseudoautotomy in snakes prior to writing this manuscript. We also

Figure 1. X-ray image of the broken tail of the thank the two anonymous reviewers for their critical comments on a juvenile Vipera ammodytes. previous draft of this paper.

References

Allf, B.C., Durst, P.A.P., Pfennig, D.W. (2016): Behavioral plasticity and the origin of novelty: The evolution of the rattle. The American Naturalist 188: 475–483. Benton, M.J. (2014): Vertebrate Palaeontology. 4th ed. Oxford: Blackwell Science Ltd. Brito, J.C. (2003): Seasonal and daily activity patterns of in northern . Amphibia-Reptilia 24: 497–508. Brito, J.C., Álvares, F. (2004): Patterns of road mortality in Vipera latastei and V. seoanei from northern Portugal. Amphibia-Reptilia 25: 459–465. Cooper, W.E., Alfieri, K.J. (1993): Caudal autotomy in the Eastern Garter Snake,

Figure 2. Stereo microscope photographs of the last vertebrae from Thamnophis s. sirtalis. Amphibia-Reptilia 14: 86–89. Costa, H.C., Moura, M.R., Feio, R.N. (2014): A tale of lost tails: Pseudoautotomy the broken tail of the juvenile Vipera ammodytes, at the separation in the Neotropical snake genus Drymoluber (Serpentes: Colubridae). point, showing intervertebral breakage: A – frontal view of the first Canadian Journal of Zoology 92: 811–816. vertebra; B – dorsal view of the first two vertebrae. Crnobrnja-Isailović, J., Ajtić, R., Tomović, L. (2007): Activity patterns of the sand viper (Vipera ammodytes) from the central . Amphibia-Reptilia 28: 582–589. ranges (e.g. and V. ursinii – Luiselli et al. 2007; V. Crnobrnja-Isailović, J., Ćorović, J., Halpern, B. (2016): Deliberate tail loss in ammodytes - Crnobrnja-Isailović et al. 2007; V. berus – Phelps Dolichophis caspius and tessellata (Serpentes: Colubridae) with a brief review of pseudoautotomy in contemporary snake families. North-Western 2004; Madsen et al. 2004; Strugariu et al. 2014; V. latastei and Journal of Zoology 12: 367–372. V. seoanei – Brito 2003, Brito & Álvares 2004), caudal luring Fuhn, I.E. (1969): Broaște, șerpi, șopârle. Bucharest, Romania: Editura Științifică, has been observed in free-ranging individuals only on very Romania. [in Romanian] Glaudas, X., Alexander, G.J. (2017): A lure at both ends: aggressive visual rare occasions (e.g. Parellada & Santos 2002). We thus mimicry signals and prey-specific luring behaviour in an ambush-foraging suspect that pseudoautotomy may not be adaptively snake. and 71: 2. hindered in this group of snakes, as there is no evidence to Jagnandan, K., Russell, A.P., Higham, T.E. (2014): Tail autotomy and firmly link caudal displays to fitness. We hypothesize that subsequent regeneration alter the mechanics of locomotion in lizards. The Journal of Experimental Biology 217: 3891–3897. deliberate tail loss may be a more common phenomenon in Kaufman, G.A., Gibbons, J.W. (1975): Weight–length relationships in thirteen younger individuals, for which tail loss may represent a species of snakes in the southeastern United States. Herpetologica 31: 31–37. better survival strategy than defensive strikes, under more Lazić, M.M., Carretero, M.A., Krstev, M.T., Macanović, M.L., Krstić, N., Crnobrnja-Isailović, J. (2012): Incidence patterns of ectodermic lesions in extreme situations, such as the one perceived by the viper wild populations of Common Wall Lizard (Podarcis muralis). Amphibia- during measurement. Nevertheless, these assumptions Reptilia 33: 327–336. should be inspected in future, more detailed studies into this Lima, S.L., Dill, L.M. (1990): Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 68: 619– subject. 640. Pseudoautotomy has been reported quite frequently in Luiselli, L., Filippi, E., Di Lena, E. (2007): Ecological relationships between slender and long-tailed snake species of three families: sympatric Vipera aspis and Vipera ursinii in high-altitude habitats of Central . Journal of Herpetology 41: 378–384. Colubridae, Lamprophiidae and Elapidae (see review in Madsen, T., Ujvari, B., Olsson, M. (2004): Novel genes continue to enhance Crnobrnja-Isailović et al. 2016). For some species, the population growth in adders (). Biological Conservation 120: frequency of tail breakage in a population was strongly 145–147. linked to predation rates (e.g. Pleguezuelos et al. 2010, Marco, A. (2002): Coluber hippocrepis (horseshoe whip snake): Caudal autotomy. Herpetological Review 33: 210. Santos et al. 2011). Previous reports of pseudoautotomy Meyrt, J.R., Kassen, R. (2007): The effects of competition and predation on describe the snakes exhibiting a circular body movement diversification in a model adaptive radiation. Nature 446: 432–435. along the longitudinal axis while being handled by the tail Parellada, X., Santos, X. (2002): Caudal luring in free-ranging adult Vipera latasti. Amphibia-Reptilia 23: 343–347. (e.g. Sharma 1980, Cooper & Alfieri 1993, Marco 2002, Costa Phelps, T. (2004): Population dynamics and spatial distribution of the adder et al. 2014, Crnobrnja-Isailović et al. 2016). In the juvenile V. Vipera berus in southern Dorset, England. Mertensiella 15: 241–258. ammodytes, the only movements displayed prior to the tail Pleguezuelos, J.M., Feriche, M., Reguero, S., Santos, X. (2010): Patterns of tail breakage in the ladder snake (Rhinechis scalaris) reflect differential predation loss were similar to the longitudinal contractions that snakes pressure according to body size. Zoology 113: 269–274. frequently exhibit during measurements (personal Santos, X., Feriche, M., Leon, R., Filippakopoulou, A., Vidal-Garcia, M., observation). After separation, the tail only moved slowly Llorente, G.A., Pleguezuelos, J.M. (2011): Tail breakage frequency as an indicator of predation risk for the aquatic snake Natrix maura. Amphibia- side-to-side for a brief period, unlike the vigorous twitches Reptilia 32: 375–383. reported in Thamophis sauritus (Todd & Wassersug 2010). Sharma, B.D. (1980): A rare case autotomy seen in Amphiesma stolata (Linn., 146 North-Western Journal of Zoology 14(1) / 2018

Serpentes: Colubridae). Snake 12: 60. 16 individuals and some of them are deposited in the Na- th Stilling, P. (2001): Ecology: theories and applications. 4 edition. Prentice Hall, tional Natural History Museum of B&H. However, Ljubis- New Jersey. Strugariu, A., Gherghel, I., Zamfirescu, Ș.R. (2014): Annual reproduction in avljević et al. (2015) mentions a possible second locality, near female adders (Vipera berus) from a montane environment. Journal of Bijeljina, for B&H quoting unpublished Bsc thesis of Aleksić Herpetology 48: 552–555. (1954), but without any voucher photographs or specimens. Todd, J., Wassersug, R. (2010): Caudal pseudoautotomy in the Eastern Ribbon Snake Thamnophis sauritus. Amphibia-Reptilia 31: 213–215. None of the localities was ever reconfirmed since the original records and existence of viable population were doubted. Key words: antipredator tactic, intervertebral tail breakage, In this paper we describe the re-discovered population urotomy, Vipera ammodytes. given in Sofradžija (1978) in locality Lozje (Cvilin, Ustiko- lina; 43°34' 18°49'). A total of 21 individuals were observed Article No.: e177503 Received: 08. May 2017 / Accepted: 30. November 2017 and 13 of them were caught (Fig. 1; Table 1). All caught indi- Available online: 11. December 2017 / Printed: June 2018 viduals were measured with calliper (1 mm) and digital weight (0,01g) and released afterwards at the site of capture.

The weather was warm but cloudy (22 °C) and variable Alexandru STRUGARIU1,*, Paul C. DINCĂ2 windy (from 0 to 2,3 m/s). Humidity was 35,2 % with soil and Ștefan R. ZAMFIRESCU2 temperature of 9 °C.

1. Research Department, Faculty of Biology, “Alexandru Ioan Cuza”

University of Iași, Iași, Romania. Figure 1. Caught individuals of Ablepharus kitaibelii – numbers corre- 2. Faculty of Biology, “Alexandru Ioan Cuza” University of Iași, Iași, Romania. spond to those in Table 1. *Corresponding author, A. Strugariu, E-mail: [email protected]

Figure 2. Habitat of Ablepharus kitaibelii from Bosnia and Herzego- The Snake-eyed skink, Ablepharus kitaibelii vina during the summer (left) and early spring (right) (photo: A. Zimić). Bibron & Bory, 1833 (Reptilia, Squamata: Scincidae) viable population re-discovered in - with morphological, The vegetation of the snake-eyed skink's habitat in this locality at the time of capture was a meadow with remnants ecological and conservation notes of last year's vegetation in which individuals very skilfully managed to hide (Fig. 1b). The meadow is extremely small The snake-eyed skink, Ablepharus kitaibelii Bibron & Bory, (20x15 m) and very steep (45°) with southwestern exposure 1833 is the only representative of its genus in , and from 429 to 433 m a.s.l. The habitat of the A. kitaibelii is south the northernmost European species of the Scincidae bordered with an old orchard (plum and cherry), while the (Herczeg et al. 2004). In Europe it is known from the south- north-east borders with light forest dominated by Quercus ern part of , , most of , southern and cerris forests with Fraxinus ornus (Fig. 1a). The meadow’s eastern parts of Romania, Bulgaria, , , and western border is represented by urban landscapes and cul- , including the Aegean and the Ionian Islands, and tivated surfaces and the Drina River. (Szövényi & Jelić 2011; Speybroeck et al. 2016). It No individuals were found in the nearby areas: (1) lives on wide variety of dry habitats with sufficient cover of where the grass is intensively cut, (2) in the forests or low vegetation or leaf litter, offering hiding places. Found in meadows, grassy slopes and forest edges (Speybroeck et al. 2016). The first official data of A. kitaibelii from Bosnia and Her- zegovina (B&H) was given by Sofradžija (1978) for eastern Bosnia (locality “Ustikolina”). The author collected