Deliberate Tail Loss (Pseudoautotomy) in a Viperid Snake
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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 animals 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, 1 Tsar Osvoboditel Blvd, 1000 Sofia, Bulgaria. 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, 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 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 rattlesnake 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 Vipera latastei in northern Portugal. 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. 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