Herpetology Notes, volume 14: 873-875 (2021) (published online on 09 June 2021)

Snout and abnormal eyes: a rare case of malformations reported in Dark Spotted deschauenseei Dunn & Conant, 1936 (Serpentes: ) from the Amapá State, northern

Rodrigo Tavares-Pinheiro1, Vinícius A. B. M. de Figueiredo1, Fillipe Pedroso-Santos1, Patrick Ribeiro Sanches1, and Carlos Eduardo Costa-Campos1,*

Malformations are structural abnormalities related to abnormalities in urban environments. the abnormal development of body parts (Frye, 1991; Eunectes deschauenseei is an endemic of Lannoo, 2009; Rothschild et al., 2012; Henle et al., Brazil, occurring only in the states of Amapá and Pará 2017). Accounts of morphological malformations are (Costa and Bérnils, 2018), generally found in large more commonly cited in amphibians than (Gatti and small streams and rivers, swamps, lakes (with and Sannolo, 2014), and the possible causes of these dense vegetation), and flooded forests, with primarily abnormalities are the environmental contaminants, nocturnal habits, and feeding on mammals, birds, radiation and parasitic infections (Wallach, 2007; reptiles and even fish (Strimple, 1993; Pizzatto et al., Johnson et al., 2010). In , dicephaly is the most 2009). reported malformation (Wallach, 2007) among the During a herpetofauna survey at Lagoa dos Índios neotropical species of the families boids, dipsadids and (0.0315ºN, 51.1025ºW; Datum: WGS 84), located in viperids (e.g., Lema, 1994; Albuquerque et al., 2010; the municipality of Macapá, state of Amapá, Brazil, Mcallister and Wallach, 2006; Sant’Anna et al., 2013). on 22 August 2018, around 20:00 h, we found a As in amphibians, snake abnormalities arise during juvenile of E. deschauenseei (snout vent-length = 1.5 embryonic development (Haschek et al., 2010), caused m; tail length = 15 cm) on the ground near the edge by endogenous or exogenous factors, such as genetic of a lagoon. We observed that the , besides and environmental aspects (Droin et al., 1970; Droin, having abnormal snout, also had eyes morphologically 1992; Wallach, 2007). abnormal (Fig. 1). The specimen showed no other Environmental contaminants due to urbanization external physical abnormalities in the rest of the body. are one of the factors that contribute to the population During our approach, the snake threatened to attack us decline of amphibians (McKinneys, 2002; Löfvenhaft and then exhibited a defensive behaviour. We measured, et al., 2004). However, this condition may not be stated photographed and released the snake after our field for snakes since there are no studies of malformations observations. In sum, two sorts of malformations were in snakes in urban environments. Thus, in this identified: (1) snout abnormal: including brachygnathia, paper we report unusual malformations in Eunectes with shortening of the jaw (Fig. 1A,B); and (2) ocular deschauenseei found in an urban area from Amapá malformation: including microphthalmia of the right State, eastern Amazon, Brazil, discuss their possible eye, that exhibited an unusual small size compared to causes, as well as reinforce the importance of studies of left eye (Figure 1B). Left eye also showed abnormal pupil (Fig. 1A). Abnormalities were classified according to Frye (1991) and Rothschild et al. (2012). Several cases of ophthalmic anomalies, including 1 Universidade Federal do Amapá, Departamento de Ciências anophthalmia and microphthalmia, have been reported Biológicas e da Saúde, Laboratório de Herpetologia, Rodovia in different snake species (e.g. Heimes, 1994; Sabater JK, Km 2, Jardim Marco Zero, 68903-419, Macapá, Amapá, and Pérez, 2013; Sant’Anna et al., 2013; Da Silva et Brazil. al., 2015). Likewise, congenital malformations such as * Corresponding author. E-mail: [email protected] shortening of the jaw and dicephalism, are relatively © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. common in snakes, although most frequent in captive 874 Rodrigo Tavares-Pinheiro ������

Figure 1. Snout and abnormal eyes of Eunectes deschauenseei from Amapá State, Eastern Amazon. A) Brachygnathia, with shortening of the jaw and left eye with abnormal pupil. B) Microphthalmia in the right eye. Scale bar = 1cm.

bred than those born in the wild (Bellairs, 1981; potential threats on its range (França et al., 2016). Wallach, 2007). Therefore, further studies testing the prevalence of Abnormalities and their causes are difficulty to malformations in the populations, the influence of clarify and are not fully understood in snakes. Many exogenous factors as potential causes, and how it affects of malformations in tetrapods may be the result of the survivorship of the specimens may help to assess exogenous factors, including environmental pollutants, how E. deschauenseei has been affected by constant parasites, UV radiation or the association of all these fragmentation of their habitats, especially under a factors (Bellairs, 1981; Wallach et al., 2007; Johnson et constant advance of urbanization. al., 2010). The causes of malformations in wild snakes are anecdotal and few studies report environmental Acknowledgments. We would like to thank Paulo Bernarde for factors as possible causes of malformations (Sant’Anna providing the pre-peer review of this manuscript and helpful et al., 2013, Čubrić and Crnobrnja-Isailović, 2017). comments. We thank Instituto Chico Mendes de Conservação da Thus, we suggest the possibility of urbanization (e.g. Biodiversidade (ICMBio) for granting collecting permits (#48102- 2). FPS is grateful to Conselho Nacional de Desenvolvimento fragmentation of habitats, exposure of snakes to Científico e Tecnológico (CNPq) for fellowship (Process exogenous causative agents) as a triggering factor for #134760/2018-2). these malformations and we encourage further studies to clarify this suggestion. References Herein, we report for the first time malformations in E. deschauenseei, reinforcing the importance Albuquerque, N.R.D., Arruda, W.S., Arianna, S. (2010): A of more detailed studies of this species. Eunectes dicephalic yellow anaconda snake, Eunectes notaeus (Serpentes: Boidae), from Southern Pantanal, Brazil. Journal of Natural deschauenseei is classified as Data Deficient in the History 44: 37–41. IUCN Red List of Threatened Species (Dirksen, 2010). Bellairs, A.d´A. (1981): Congenital and developmental diseases. The degree of environmental impact in this species is In: Diseases of the Reptilia. p. 469–485. Cooper, J., Jackson, unknown, although habitat loss and degradation are O.F., Eds., London, UK, Academic press. A rare case of malformations reported in Dark Spotted Anaconda Eunectes 875

Costa, H.C., Bérnils, R.S. (2018): Répteis do Brasil e suas Lannoo, M.J. (2009): Malformed frogs: the collapse of aquatic Unidades Federativas: Lista de espécies. Herpetologia Brasileira ecosystems. Berkeley and Los Angeles, University of California 7: 11–58. Press. Čubrić, T., Crnobrnja-Isailović, J. (2017): Malformation of eye Lema, T. (1994): Descrição de um exemplar com bifurcação pupil in nose-horned viper (Vipera ammodytes) from a wild axial de Echinanthera cyanopleura (Cope, 1885) (Serpentes, population. Herpetology Notes 10: 229–231. Colubridae, Xenodontinae). Acta Biologica Leopoldensia 16: Da Silva, M.A.O., Bertelsen, M.F., Wang, T., Pedersen, M., 113–117. Lauridsen, H., Heegaard, S. (2015): Unilateral microphthalmia Löfvenhaft, K., Runborga, S., Sjögren-Gulveb, P. (2004): Biotope or anophthalmia in eight pythons (Pythonidae). Veterinary patterns and amphibian distribution as assessment tools in urban ophthalmology 18: 23–29. landscape planning. Landscape Urban Plan 68: 403–427. Dirksen, L. (2010): Eunectes deschauenseei. The IUCN Red List Mcallister, C.T., Wallach, V. (2006): Discovery of a dicephalic of Threatened Species 2010. http://dx.doi.org/10.2305/IUCN. western diamondback rattlesnake, Crotalus atrox (Serpentes: UK.2010-4.RLTS.T176262A7207195.en. Acessed on 26 Viperidae), from Texas, with a summary of dicephalism among September 2018. members of the genus Crotalus. Journal of the Arkansas Droin, A. (1992): The developmental mutants of Xenopus. The Academy of Science 60: 67–73. International Journal of Developmental Biology 36: 455–464. McKinney, M.L. (2002): Urbanization, biodiversity, and Droin, D., Uehling, V., Reynaud, J. (1970): Une mutation letale, conservation. Bioscience 52: 883–890. recessive, “bt” (bent tail) chez Xenopus laevis. Revue Suisse de Pizzatto, L., Marques, O., Facure, K. (2009): Food habits of Zoologie 77: 596–602. Brazilian boid snakes: Overview and new data, with special Franca, F.G.R., Mesquita, D.O., Colli, G.R. (2006): A checklist reference to Corallus hortulanus. Amphibia-Reptilia 30: 533– of snakes from Amazonian Savannas in Brazil, housed in the 544. colecao herpetologica da universidade de Brasilia, with new Rothschild, B.M., Schultze, H., Pellegrini, R. (2012): Herpetological distribution records. Occasional Papers of the Oklahoma Osteopathology: Annotated Bibliography of Amphibians and Museum of Natural History 17: 1–13. Reptiles. New York, Springer. Frye, F.L. (1991): Care: An Atlas of Diseases and Sabater, M., Pérez, M. (2013): Congenital ocular and adnexal Treatments. TFH Publications, Neptune City. disorders in reptiles. Veterinary Ophthalmology 16: 47–55. Gatti, F., Sannolo, M. (2014): Two cases of polydactyly in the Sant’Anna, S.S., Grego, K.F., Lorigados, C.A.B., Fonseca-Pinto, Italian crested newt, Triturus carnifex. Herpetology Notes 7: A.C.B.C., Fernandes, W., Sá-Rocha, L.C., Catão-Dias, J.L. 477–478. (2013): Malformations in Neotropical Viperids: Qualitative and Haschek, W.M., Rousseaux, C.G., Wallig, M.A. (2010): Quantitative Analysis. Journal of Comparative Pathology 149: Fundamentals of Toxicologic Pathology, Second Edition. 503–508. London, Academic Press. Strimple, P. (1993): The Green Anaconda Eunectes murinus Heimes, P. (1994): Morphologische Anomalien bei Äskulapnattern (Linnaeus). Liyyeratura Serpentium 13: 46–50. (Elaphe longissima) im Rheingau-Taunus. Salamandra 30: Wallach, V. (2007): Axial bifurcation and duplication in snakes. 268–271. Part I. A synopsis of authentic and anecdotal cases. Bulletin of Henle, K., Dubois, A., Vershinin, V. (2017): Commented glossary, the Maryland Herpetological Society 43: 57–95. terminology and synonymies of anomalies in natural populations Wallach, V. (2007): Axial bifurcation and duplication in snakes. of amphibians. Mertensiella 25: 9–48. Part I. A synopsis of authentic and anecdotal cases. Bulletin of Johnson, P.T.J., Reeves, M.K., Krest, S.K., Pinkney, A.E. (2010): the Maryland Herpetological Society 43: 57–95. A decade of deformities: advances in our understanding of amphibian malformations and their implications. In: Ecotoxicology of Amphibians and Reptiles. p. 511–536. Sparling, D.W., Linder, G., Bishop, C.A., Krest, S.K., Eds., Pensacola, Society of Environmental Toxicology and Chemistry.

Accepted by Clarissa Canedo