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Home , Anguis, Iphisa, Legless lizard, Liolaemidae, Mexican blind lizard, Micrablepharus atticolus

Herpetology Notes, volume 13: 961-964 (2020) (published online on 26 November 2020)

The performance of survival: A death-feigning case in graeca Bedriaga, 1881 (: )

Apostolos Christopoulos1,*, Christos Kotselis2, and Theofanis Theofanopoulos3

The Anguis Linnaeus, 1758 (Squamata: anti-predator strategy known in both and Anguidae) comprises five of legless called vertebrates (Cassill et al., 2008; Humphreys and Ruxton, slow , that occur mainly in Europe and western 2018). It was widely reported in (Burghardt Asia. The Greek slow Anguis graeca Bedriaga, and Greene, 1988; Gregory et al., 2007; Vogel and 1881 is a Balkan endemic distributed in the southern Han-Yuen, 2010; Marques et al., 2013; Iiftime and countries of the peninsula (Uetz et al., 2020). In Greece, Iftime, 2014; Sannolo et al., 2014; Muscat et al., 2016; it occurs in many parts of the mainland; Peloponnese; Gomard, 2017; İğci et al., 2017; Golubović et al., 2019), Euboea and Kerkyra Islands (Jablonski et al., 2016). and less frequent in lizards being reported in several Similarly with A. fragilis, A. graeca prefers vegetated families worldwide, including Anelytropsidae (Torres- and humid , with refuges such as stones, leaf Cervantes et al., 2004), Mabuyidae (Ribeiro et al., litter and woody debris (Smith, 1990; Valakos et al., 2010), (Santos et al., 2010), 2008; Speybroeck et al., 2016). Slow worms have (Nunes et al., 2012), Scincidae (Patel et al., 2016; various predators: snakes, birds, frogs, toads, mammals Vergilov, 2017), (Machado-Filho (including domestic cats) (Smith, 1990; Fuke, 2011), et al., 2018; Mesquita et al., 2018). To the best of our while quite recently the large green lizards spp. knowledge, there is no mention of this behaviour in the were also added to the list (Vacher and Wendling, 2019; legless lizards of Anguidae family. The high rates of shed Christopoulos et al., 2020). tails found in the species A. fragilis suggest that these Antipredator traits and behaviours in evolved lizards may suffer a high risk of predation (Stumpel, to both avoid predation risk and to escape capture 1985; Vences, 1993). In addition, it has been found (Humphreys and Ruxton, 2018). Spraying the foe, that antipredator behaviour in the species is induced death-feigning, autohaemorrhaging, caudal autotomy by chemosensory predator recognition (Cabido et al., and blood squirting in Squamata are some of the wide 2004). Here we report another antipredator mechanism variety of behavioural and physiological mechanisms in the genus Anguis. used against predators (Sherbrooke and Middendorf On 16 June 2019 at approximately 15:40 h, at the end of III, 2001; Gregory et al., 2007; Bateman and Fleming, a herpetological survey in the western Othrys Mountain 2009; Santos et al., 2010; Iiftime and Iftime, 2014; İğci range (Fthiotida, Central Greece), we observed an et al., 2017; Humphreys and Ruxton, 2018; Bels and adult A. graeca which seemed to be healthy (total Russell, 2019; Golubović et al., 2019). Death-feigning, length 210 mm), crossing the road. The observation also known as thanatosis and tonic immobility is an point (33.4802oN, 43.2069oE; 742 m a.s.l.) is located in a semi-mountainous zone, SE of the village Palea Giannitsou, and the main consists of pubescent oak (Quercus pubescens) forest with small openings. The day was sunny and the temperature was 29 oC. We stopped, handled the legless , and as we laid it on 1 Department of Zoology and Marine Biology, Faculty of the ground at the edge of the forest, it began to perform Biology, National and Kapodistrian University of Athens, Panepistimioupolis, 15784 Athens, Greece. a -like death-feigning behaviour. We observed the 2 Diagora 24, 11636 Athens, Attika, Greece. whole behaviour carefully and took photographs (Fig. 3 Konstantinoupoleos 4, 35100 Lamia, Fthiotida, Greece. 1). At first, the was spinning around its * Corresponding author. E-mail: [email protected] body vigorously with contractions for one minute (Fig. 962 Apostolos Christopoulos et al.

Figure 1. (A–D) Sequence of death-feigning behaviour in Anguis graeca (adult individual from the western Othrys Mountain); (E) The adult A. graeca in normal standing position, before it left. Photos by Apostolos Christopoulos.

1A,B). In a second phase, it stayed in tonic immobility standing position and remained in immobility for in inverted position for approx. 1.5 minutes (Fig. 1C). approx. two minutes (Fig. 1E). Finally, the slow worm Then, it moved part of its body and kept standing moved slowly towards the forest and hid in the leaf almost in immobility in the same position, while the litter. This is the first reported record of death-feigning sliding motion was almost imperceptible; this behaviour behaviour in the Greek slow worm. lasted for two minutes (Fig. 1D). After this successful Caudal autotomy is the only known defensive short performance, the slow worm regained its normal mechanism of genus Anguis until now. Here we report The performance of survival: A death-feigning case in Anguis graeca 963 a case of death-feigning as a second antipredator (L., 1758) and Natrix tessellata (Laurenti, 1768) from Turkey. behaviour in a species of genus Anguis. Furthermore, A. Commagene Journal of Biology 1(1): 63–64. graeca is a poorly studied species, thus many biological Iiftime, A., Iftime, O. (2014): Thanatosis and autohaemorrhaging in the Aesculapian Snake Zamenis longissimus (Laurenti, 1768). and ecological aspects remain unknown. Every natural Herpetozoa 26(3/4): 173–174. history note about the Greek slow worm’s life is Jablonski, D., Jandzik, D., Mikulíček, P., Džukić, G., Ljubisavljević, important so that we get to know more about its cryptic K., Tzankov, N., et al. (2016): Contrasting evolutionary life traits. histories of the legless lizards slow worms (Anguis) shaped by the topography of the Balkan Peninsula. BioMed Central Acknowledgements. We thank Petros Lymberakis (Natural History Evolutionary Biology 16(1): 99. Museum of Crete, University of Crete) for the pre-peer review of Machado-Filho, P.R., Moya, G.M., Maffei, F. (2018): Death- the manuscript. feigning behaviour in Iphisa elegans: the second reported case in the Family Gymnophthalmidae (Reptilia: Squamata). Acta Amazonica 48(2): 151–153. References Marques, O.A., Banci, K.R., Strüssmann, C. (2013): Death- Bateman, P.W., Fleming, P.A. (2009): To cut a long tail short: a feigning behaviour in water snakes of the genus Hydrodynastes review of lizard caudal autotomy studies carried out over the last (Dipsadidae) from South America. Amphibia-Reptilia 25: 178– 20 years. Journal of Zoology 277(1): 1–14. 184. Bels, V., Russell, A. (2019): Behavior of Lizards: Evolutionary and Mesquita, G.S., Ferraz, D., Ramalho, W.P., Machado, I.F., Vaz- Mechanistic Perspectives. Boca Raton, CRC Press. Silva, W. (2018): Death-feigning as defensive behavior in blue- Burghardt, G.M., Greene, H.W. (1988): Predator simulation and tailed microteiid lizard Micrablepharus atticolus Rodrigues, duration of death feigning in neonate hognose snakes. 1996. Herpetology Notes 11: 1065–1067. Behaviour 36(6): 1842–1844. Muscat, E., Rotenberg, E.L., Machado, I.F. (2016): Death-feigning Cabido, C., Gonzalo, A., Galán, P., Martín, J., López, P. (2004): behaviour in an Erythrolamprus miliaris (Linnaeus, 1758) Chemosensory predator recognition induces defensive behavior () water snake in Ubatuba, São Paulo, southeastern in the slow-worm (Anguis fragilis). Canadian Journal of Zoology Brazil. Herpetology Notes 9: 95–97. 82(3): 510–515. Nunes, J.V., Elisei, T., de Sousa, B.M. (2012): Anti-predator Cassill, D.L., Vo, K., Becker, B. (2008): Young fire ant workers feign behaviour in the Brazilian lizard itambere death and survive aggressive neighbors. Naturwissenschaften (Tropiduridae) on a rocky outcrop. Herpetological Bulletin 120: 95(7): 617–624. 22–28. Christopoulos, A., Zogaris, D., Karaouzas, I., Zogaris, S. (2020): Patel, H., Naik, V., Tank, S.K. (2016): Death-feigning behavior A predation case of Anguis graeca Bedriaga, 1881 (Squamata: in two species of Lygosoma (Squamata: Scincidae) from Anguidae) by Lacerta trilineata Bedriaga, 1886 (Squamata: India. Phyllomedusa 15(2): 191–194. ) from Central Greece. Herpetology Notes 13: 105– Ribeiro, S.C., Sousa, J.G.G., Teles, D.A, Almeida, W.O., Guarnieri, 107. M.C. (2010): Mabuya arajara (NCN). Death-feigning. Fuke, C. (2011): A study of a translocated population of Anguis Herpetological Review 41(4): 494–495. fragilis in Cornwall, UK. The Plymouth Student Scientist 4(2): Sannolo, M., Gatti, F., Scali, S. (2014): First record of thanatosis 181–221. behaviour in Malpolon monspessulanus (Squamata: Golubović, A., Andjelković, M., Gvozdenović, S., Šukalo, G., Colubridae). Herpetology Notes 7: 323. Tomović, L., Bonnet, X. (2019): Oscar deserving performance: Santos, M.B.D., de Oliveira, M.C.L.M., Verrastro, L., Tozetti, A.M. death-feigning in dice snakes. In: Ficetola, G.F., Sacchi, R., (2010): Playing dead to stay alive: death-feigning in Scali, S., Manenti, R., Coladonato, A., Melotto, A., et al. occipitalis (Squamata: Liolaemidae). Biota Neotropica 10(4): (editors). XX European Congress of Herpetology, Milan, 2-6 361–364. September 2019. Program and Abstracts. Societas Europaea Sherbrooke, W.C., Middendorf III, G.A. (2001): Blood-squirting Herpetologica, Milano. variability in horned lizards (Phrynosoma). Copeia 2001(4): Gomard, G. (2017): Hierophis viridiflavus (Lacépède, 1789) 1114–1122. feigning death when handled. The Herpetological Bulletin 142: Smith, N. (1990): The ecology of the slow-worm (Anguis fragilis 50–51. L.) in southern England. PhD thesis, University of Southampton, Gregory, P.T., Isaac, L.A., Griffiths, R.A. (2007): Death feigning by Southampton, UK, 229 pp. grass snakes (Natrix natrix) in response to handling by human Speybroeck, J., Beukema, W., Bok, B., Voort, J.V. (2016): Field “predators”. Journal of Comparative Psychology 121(2): 123– Guide to the Amphibians & Reptiles of Britain and Europe. 129. London, United Kingdom, Bloomsbury, 320 pp. Humphreys, R.K., Ruxton, G.D. (2018): A review of thanatosis Stumpel, A.H.P. (1985): Biometrical and ecological data from a (death feigning) as an anti-predator behaviour. Behavioral Netherlands population of Anguis fragilis (Reptilia, Sauria, Ecology and Sociobiology 72(2): 22. Anguidae). Amphibia-Reptilia 6: 181–194. İğci, N., Göçmen, B., Kariş, M., Akman, B. (2017): Observation Torres-Cervantes, R.J., Hernandez-Ibarra, X., Ramirez-Bautista, A. of Autohemorrhage as a Defensive Behavior of Natrix natrix (2004): Anelytropsis papillosus (Mexican blind lizard). Death 964 Apostolos Christopoulos et al.

feigning and autotomy. Herpetological Review 35: 384. Uetz, P., Freed, P., Hošek, J., eds. (2020): Anguis species. The Database. Available at: http://www.reptile-database.org. Accessed on 10 February 2020. Vacher, J.P., Wendling, T. (2019): An unusual case of predation of the western green lizard Lacerta bilineata Daudin, 1802 (Reptilia: Lacertidae) on the slow worm Anguis fragilis Linnaeus, 1758 (Reptilia: Anguidae). Herpetology Notes 12: 1201–1202. Valakos, E.D., Pafilis, P., Sotiropoulos, K., Lymberakis, P., Maragou, P., Foufopoulos, J. (2008): The Amphibians and Reptiles of Greece. Frankfurt am Main, , Chimaira, 463 pp. Vences, M. (1993): Beobachtungen an einer isolierten population der blindschleiche (Anguis fragilis) in nordwestspanien. Salamandra 29: 265–268. Vergilov, V. (2017): Notes on the defensive behavior and activity of Ablepharus kitaibelii (Bibron & Bory de Saint-Vincent, 1833) in Bulgaria. ZooNotes 116: 1–4. Vogel, G., Han-Yuen, H.K. (2010): Death feigning behavior in three colubrid species of tropical Asia. Russian Journal of Herpetology 17(1): 15–21.

Accepted by Florina Stanescu