sign in sign up
<<
Home , Hungarian meadow viper, Red tegu, Vipera ammodytes

North-Western Journal of Zoology 2019, vol.15 (2) - Correspondence: Notes 195

Castillo, G.N., González-Rivas C.J., Acosta J.C. (2018b): rufescens Article No.: e197504 (Argentine Red Tegu). Diet. Herpetological Review 49: 539-540. Received: 15. April 2019 / Accepted: 21. April 2019 Castillo, G.N., Acosta, J.C., Blanco, G.M. (2019): Trophic analysis and Available online: 25. April 2019 / Printed: December 2019 parasitological aspects of Liolaemus parvus (Iguania: Liolaemidae) in the Central Andes of Argentina. Turkish Journal of Zoology 43: 277-286. Castillo, G.N., Acosta J.C., Ramallo G., Pizarro J. (2018a): Pattern of infection by Gabriel Natalio CASTILLO1,2,3,*, Parapharyngodon riojensis Ramallo, Bursey, Goldberg 2002 (Nematoda: 1,4 Pharyngodonidae) in the Phymaturus extrilidus from Puna region, Cynthia GONZÁLEZ-RIVAS Argentina. Annals of Parasitology 64: 83-88. and Juan Carlos ACOSTA1,2 Cruz, F.B., Silva, S., Scrocchi, G.J. (1998): Ecology of the lizard Tropidurus etheridgei (: Tropiduridae) from the dry Chaco of Salta, 1. Faculty of Exact, Physical and Natural Sciences, National University Argentina. Herpetological Natural History 6: 23-31. of San Juan, Av. Ignacio de la Roza 590, 5402, San Juan, Argentina. Goldberg, S.R., Bursey, C.R., Morando, M. (2004): Metazoan endoparasites of 12 2. DIBIOVA Research Office (Diversity and Biology of Vertebrates of of from Argentina. Comparative Parasitology 71: 208-214. the Arid), National University of San Juan, Av. Ignacio de la Lamas, M.F., Céspedez, J.A., Ruiz-García, J.A. (2016): Primer registro de Roza 590, 5402, San Juan, Argentina. nematodes parásitos para la culebra Xenodon merremi (Squamata, 3. CONICET (National Council of Scientific and Technical Research), Dipsadidae) en Argentina. Facena 32: 59-67. Av. Ignacio de la Roza 590, 5402, San Juan, Argentina. Lamas, M.F., Zaracho, V.H. (2006): Tropidurus torquatus. Endoparasites. 4. Center for Rehabilitation of Wildlife, Environmental Education Herpetology Review 37: 474-475. and Responsible Recreation, San Juan, Argentina. Márquez, J., Martínez Carretero, E., Dalmasso A. (2016): Provincias * Corresponding author, G. Castillo, E-mail: [email protected] fitogeográficas de la Provincia de San Juan. pp. 187-197. En: Martínez

Carretero, E., Garcia A. (eds), San Juan Ambiental, 1º edición. Editorial INCA, Mendoza. Montero, R., Abdala, V., Moro, S., Gallardo, G. (2004): Atlas de rufescens (Squamata: ). Anatomía externa, osteología y bibliografía. Cuadernos de Herpetología 18:17-32. A case of unusual head scalation in O’Grady, S.P., Dearing, M.D. (2006): Isotopic insight into host–endosymbiont ammodytes (Squamata: relationships in Liolaemidae lizards. Oecologia 150: 355-361. Ortlepp, R.J. (1922): The nematode genus Physaloptera Rudolphi. Proceedings of Serpentes: ) the Zoological Society of London 4: 999-1107. in Western Pereira, F.B., Alves, P.V., Rocha, B.M., de Souza Lima, S., Luque, J.L. (2012): A new Physaloptera (Nematoda: Physalopteridae) parasite of Tupinambis merianae (Squamata: Teiidae) from southeastern Brazil. Journal of In squamates, head scalation is often used in taxonomic Parasitology 98: 1227-1235. identification of a species (Ursel 1978; Sanders et al. 2006), as Pereira, F.B., Alves, P.V., Rocha, B.M., de Souza Lima, S., Luque, J.L. (2014): the genes which determine the developmental processes re- Physaloptera bainae n. sp. (Nematoda: Physalopteridae) parasitic in Salvator merianae (Squamata: Teiidae), with a key to Physaloptera species parasitizing lated to scalation could change through the speciation (Mur- from Brazil. Journal of Parasitology 100: 221-227. phy et al. 1987 and references therein). Some studies have Ramallo, G., Bursey, C., Castillo, G., Acosta, J.C. (2016): New species of suggested that the scalation pattern could have genetic Parapharyngodon (Nematoda: Pharyngodonidae) in Phymaturus spp. (Iguania: Liolaemidae) from Argentina. Acta Parasitologica 61: 461-465. (Murphy et al. 1987; King 1997), environmental (Lourdais et Ramallo, G., Bursey, C.H., Goldberg, S., Castillo, G., Acosta, J.C. (2017b): al. 2004), or combined background (Uveges et al. 2012). It is Phymaturus extrilidus. Endoparasites. Herpetological Review 48: 198. therefore important to report any deviation from the “typi- Ramallo, G., Bursey, C.R., Goldberg, S.R. (2002): Spauligodon loboi n. sp. (Nematoda: Pharyngodonidae) parasite of Liolaemus spp. (Iguania: cal” head scalation pattern in a squamate species, as it can be Liolaemidae) from northwestern Argentina. Journal of Parasitology 88: 370- relevant for different evolutionary and ecological studies. 374. Furthermore, some studies suggested that inbreeding (Mur- Ramallo, G., Goldberg, S., Bursey, C., Castillo, G., Acosta, J.C. (2017a): Thubunaea eleodori sp. nov. (Nematoda: Physalopteridae) from Liolaemus phy et al. 1987; Olsson et al. 1996) or abiotic factors such as eleodori (Sauria: Liolaemidae) from Argentina. Parasitology Research 116: temperature (Shine et al. 2005; Idrisova 2018) could contrib- 293-297. ute to the morphological abnormalities such as unusual sca- Ramallo, G.R., Díaz, F. (1998): Physaloptera lutzi (Nematoda, Physalopteridae) lation pattern. Sometimes, such malformations could indi- parasite de Liolaemus (Iguania, Tropiduridae) del noroeste Argentino. Boletín Chileno de Parasitología 53: 19-22. cate the need for future conservation assessments or actions Ribas, S.C., Rocha, C.F.D., Teixeira-Filho, P.F., Vicente, J.J. (1995): Helminths on particular population(s) as some malformations can be (Nematoda) of the lizard Cnemidophorus ocellifer (Sauria: Teiidae): Assessing correlated with the ecological performance of the individual the effect of rainfall, body size and sex in the nematode infection rates. Ciencia e Cultura 47: 88-91. (Brown et al. 2017). Here we report a case of atypical head Rudolphi, C.A. (1819): Entozoorum Synopsis, Cui Accedunt Mantissa Duplex et scalation in a nose-horned viper (Vipera ammodytes), as we Indices Locupletissimi. Augusti Rucker, Berlin, Germany. did not detect it in this species in more than thirty years of Skrjabin, K.I., Shikhobalova, N.P., Lagodovskaya, E.A. (1960): Oxyurata of and man. Part one. Oxyuroidea. Essentials of Nematodology, Vol. field work. VIII. Israel Program for Scientific Translations. Moskva, Russia. Vipera ammodytes (Linnaeus, 1758) is venomous Spinelli, C.M., Fiorito de López, L.E., Stiebel, C. (1992): Alteraciones with a distribution range that spans from southern histológicas en el intestino delgado en Tupinambis rufescens (Sauria: teiidae) causadas por Diaphanocephalus galestus (Nematoda: diaphanocephalidae). and northern , through the to Asia Minor Cuadernos de Herpetología 7: 37-40. (Crnobrnja-Isailović & Haxhiu 1997). It is one of the larger Sprehn, C. (1932): Uber einige von Dr. Eisentraut in Bolivien gesammelte European vipers, with the total body length usually up to 1 nematoden. Zoologischer Anzeiger 100: 273-284. m (Arnold & Ovenden 2002). The head is large, triangular, Vicente, J.J., Rodrigues, H.D.O., Gomes, D.C., Pinto, R.M. (1993): Brazilian nematodes. Part III: Nematodes of reptiles. Revista Brasileira de Zoologia 10: with its dorsal side covered by small scales, except for the 19-168. supraoculars (Arnold & Ovenden 2002). Within its range, the Vieira, T.D., Fedatto-Bernardon, F., Müller, G. (2016): Diaphanocephalus galeatus species is easily recognizable by the prominent horn on the (Nematoda: Diaphanocephalidae), parásito de Salvator merianae (Squamata: Teiidae) en el sur del Brasil. Revista Mexicana de Biodiversidad 87: 512-515. top of the viper’s snout. It has 21-23 rows (sometimes 19) of dorsal scales on the mid body and 137-163 ventral scales Key words: Homonota underwoodi, nematodes, Physaloptera retusa, (Tomović 2006; Boulenger 1913). There is a sexual dimor- Pharyngodon, parasites, Salvator rufescens, Teius teyou. phism which is the most prominent in the tail length and

196 North-Western Journal of Zoology 2019, vol.15 (2) - Correspondence: Notes number of subcaudal scales (males have longer tail and more subcaudal scales) (Tomović 2002). During a survey carried out on October 11th 2018 in western Serbia, we encountered a juvenile nose-horned vi- per (total length L =248 mm) which had large dorsal head scales on the central part of the head, besides the normal large supraoculars and other small scales (Fig.1). The large scales could be considered as one scale incompletely sepa- rated or as two large scales with the smaller one in between (Fig.1). We did not record any other unusual morphological trait on this viper. The individual had 2 supraoculars, 12 small scales surrounding the eyes, 6 midorbitals, 1 supraros- tral and the eyes were separated with two rows of scales from the supralabials. The head length was 17,98 mm, the head width was 11,74 mm, the rostral height was 2,06 mm, the rostral width was 2,00 mm and the horn height was 3,60 Figure 1. Nose-horned viper with large head scales. mm. All these measurements of morphometric characters are within the usual range of values previously published for V. ammodytes (for example see Tomović 2006; Tok & Kumluts 1996). The snake’s behaviour was the same as in other en- countered nose-horned vipers. All the examinations were done in situ and the was marked and released after- wards. In the same local population, this viper was the only one among the 18 measured individuals which had large head scales. Fig. 2 represents a typical head scalation in V. ammodytes from the same local population. Furthermore, the observed juvenile individual was the only one with this type of head scalation among 74 examined nose-horned vipers in the year of 2018 in Serbia. To the best of our knowledge, this type of head scalation in V. ammodytes has never been re- ported. Regarding other snake species, authors have re- Figure 2. Nose-horned viper with typical head scalation. ported a fragmentation of head scales (for example: Stoy- anov & Tzankov 2017 for V. berus; Brown et al. 2017 for Ste- early embryogenesis and produce head scale abnormalities gonotus cucullatus). in S. cucullatus, and they correlated those abnormalities with The presence of large scales on the dorsal side of the the ecological performance of the individuals. Other than head of the nose-horned viper reported individual could be this, Brown et al. (2017) have also found that scale abnor- explained from several points of view: Ursel (1978) proposed malities are not limited to small isolated, disturbed popula- that presence of small scales on the dorsal side of the viperid tions. head is the result of the fragmentation of large scales Furthermore, considering that the reported nose-horned into smaller ones, which happened secondary in the course viper is a juvenile individual, maybe postnatal changes in of evolution. If true, then this atypical scalation could be the scalation can happen as reported for V. ursinii (Tomović et case of simple atavism. In their study on V. aspis, Lorioux et al. 2008). However, this possibility has to be taken with cau- al. (2013), concluded that the formation of head scales hap- tion as recent results of Bauwens et al. (2018) study con- pens during late embryogenesis and it can be influenced by firmed ontogenetic stability of individual head scalation pat- temperature. So, the presence of large head scales could also tern in a large population of V. berus. be the result of environmental impact on the embryogenesis In conclusion, this unusual head scalation in V. ammo- of this individual. Murphy et al. (1987) concluded that dytes can be considered very rare as it was not previously snakes scalation abnormalities could be either determined by published elsewhere. To answer the question whether the the polygenes or by a large influence of the genetic back- cause is genetic, environmental or combined, more evidence ground against which a mutant gene is expressed, implying and further studies (both genetic and ecological) are needed. that scalation abnormalities in Crotalus atrox, which they ob- served, could be the result of inbreeding. Based on our in- Acknowledgements. The fieldwork was kindly funded by The terviews with the local inhabitants, some years ago, the vi- Rufford Foundation (grants no: 19578-1 and 23392-2) for TČ and by pers were deliberately killed in large numbers during the Ministry of Education, Science and Technological Development of mating season in the area where the reported juvenile nose- Republic of Serbia (grant no 173025), for both JCI and TČ. TČ is very horned viper individual was found. Also, the habitat where grateful to Nikola Vuletić for logistic help. the reported individual was found, is intersected with roads References and agricultural land. Having this in mind, the presence of Arnold, E.N., Ovenden, D., Burton, J. A. (2002): Reptiles and of large scales on the head could also be the result of inbreed- Britain and . Collins, London. ing in the small, disturbed population. Brown et al. (2017) Bauwens, D., Claus, K., Mergeay, J. (2018): Genotyping validates photo- identification by the head scale pattern in a large population of the European found that both genetic and environmental factors influence adder (). Ecology and Evolution 8(5): 2985-2992. North-Western Journal of Zoology 2019, vol.15 (2) - Correspondence: Notes 197

Boulenger, G.A. (1913): On the geographical races of Vipera ammodytes. Journal An observation of the nectar- / feeding of Natural History 11(63): 283-287. Brown, G.P., Madsen, T., Dubey, S., Shine, R. (2017): The causes and ecological hair-crested drongo (Dicrurus hottentottus) correlates of head scale asymmetry and fragmentation in a tropical snake. Scientific reports 7(1): 11363. eats a lizard as a novel food source Crnobrnja-Isailović, J., Haxhiu, I. (1997): Vipera ammodytes. pp. 384-385. In: Gasc, J.P. et al. (eds.), Atlas of Amphibians and Reptiles in Europe. Societas The hair-crested drongo (Dicrurus hottentottus) is a common Europaea Herpetologica and Muséum National d' Histoire Naturelle, Paris. migratory passerine , which breeds in central and south- Idrisova, L.A. (2018): The Effect of Incubation Temperature on Deviations of Pholidosis and Malformations in Grass Snake natrix (L. 1758) and ern China and typically heads to tropical Indochina to over- Sand Lizard Lacerta agilis (L. 1758). KnE Life Sciences 4(3): 70-74. winter (Rocamora & Yeatman-Berthelot 2009). While it is King, R.B. (1997): Variation in brown snake (Storeria dekayi) morphology and well established that drongos utilize diverse habitat, their scalation: sex, family, and microgeographic differences. Journal of Herpetology, 31(3): 335-346. diet is poorly understood. Previous observation has identi- Lorioux, S., Vaugoyeau, M., DeNardo, D.F., Clobert, J., Guillon, M., Lourdais, fied that, in tropical overwintering areas, the hair-crested O. (2013): Stage dependence of phenotypical and phenological maternal drongo feeds primarily on nectar (Pandey 1991), whereas in effects: insight into squamate reproductive strategies. The American Naturalist 182(2): 223-233. subtropical and temperate breeding areas it appears to Lourdais, O., Shine, R., Bonnet, X., Guillon, M., Naulleau, G. (2004): Climate mainly eat (Wang & Qian 1989, Zhao 2001). Zhao affects embryonic development in a viviparous snake, Vipera aspis. Oikos (2001) claims that hair-crested drongos may eat snakes in 104: 551-560. Murphy, J.B., Rehg, J.E., Maderson, P.F., McCrady, W.B. (1987): Scutellation high latitude areas, and Rocamora & Yeatman-Berthelot and pigmentation defects in a laboratory colony of Western diamondback (2009) provide an anecdotal report that this species may eat rattlesnakes (Crotalus atrox): mode of inheritance. Herpetologica 43(3): 292- small lizards. However, to-date, there has been no firm evi- 300. dence corroborating that this nectar-insect eating bird con- Olsson, M., Gullberg, A., Tegelström, H. (1996): Malformed offspring, sibling matings, and selection against inbreeding in the sand lizard (Lacerta agilis). sumes vertebrates. Journal of Evolutionary Biology 9(2): 229-242. Sanders, K.L., Malhotra, A., Thorpe, R.S. (2006): Combining molecular, Over 3 days (17, 18, 21) in June 2017, we observed a hair-crested morphological and ecological data to infer species boundaries in a cryptic drongo nest, built in an empress tree (Paulownia tomentosa), ap- tropical . Biological Journal of the Linnean Society 87: 343-364. proximately 15 meters in front of a local residential house in Yangri Shine, R., Langkilde, T., Wall, M., Mason, R. T. (2005): The fitness correlates of scalation asymmetry in garter snakes Thamnophis sirtalis parietalis. Functional town (478m a.s.l., 110.81°E, 31.74°N) in Shennongjia, Hubei province, Ecology 19(2): 306-314. China. Stoyanov, A., Tzankov, N. (2017): Individual variation of pileus scalation characteristics in Vipera berus bosniensis Boettger, 1889 (Reptilia: Sqaumata: Using a single-lens reflex camera (Canon 7D2, 100-400 mm Viperidae). North-Western Journal of Zoology 13(1): 186-191. lens), with 0.31 magnification, we observed that on June 18, Tomović, L., Radojičić, J., Dzukić, G., Kalezić, M.L. (2002): Sexual dimorphism of the sand viper (Vipera ammodytes L.) from the central part of Balkan at 17: 32, an adult female drongo flew back to its nest, carry- Peninsula. Russian journal of herpetology 9(1): 69-76. ing a small lizard of the species Szechwan japalure (Japalura Tomović, Lj. (2006): Systematics of the nose-horned viper (Vipera ammodytes, flaviceps), that it fed to one of its nestlings (Fig. 1). Although Linnaeus, 1758). The Herpetological Journal 16(2): 191-201. Tomović, L., Carretero, M.A., Ajtic, R., Crnobrnja-Isailovic, J. (2008): Evidence for post-natal instability of head scalation in the meadow viper () – patterns and taxonomic implications. Amphibia-Reptilia 29(1): 61- 70. Tok, C.V., Kumlutş, Y. (1996): On Vipera ammodytes transcaucasiana (Viperidae) from Perşembe, Black Sea region of . Zoology in the 13(1): 47-50. Ursel, F. (1978): Der Pileus der Squamata. Stuttgarter Beiträge zur Naturkunde Serie A Üveges, B., Halpern, B., Péchy, T., Posta, J., Komlósi, I. (2012): Characteristics and heritability analysis of head scales of the Hungarian meadow viper (Vipera ursinii rakosiensis, Méhely 1893). Amphibia-Reptilia 33(3-4): 393-400.

Key words: head scales, scale oligomerization, Vipera ammodytes, vi- per, Serbia.

Article No.: e197505 Received: 02. February 2019 / Accepted: 04. September 2019 Available online: 10. September 2019 / Printed: December 2019

Tijana ČUBRIĆ1 and Jelka CRNOBRNJA-ISAILOVIĆ1,2

1. Department of Biology and Ecology, Faculty of Science and Mathematics, University of Niš, Višegradska 33, 18 000 Niš, Serbia. 2. Department of Evolutionary Biology, Institute for Biological Research “Siniša Stanković”, University of Belgrade, Despota Stefana 142, 11000 Belgrade, Serbia. * Corresponding author, T. Čubrić, E-mail: [email protected]