Herpetology Notes, volume 11: 1051-1053 (2018) (published online on 29 November 2018)

Hypopigmentation in wild snakes from Uruguay

Victoria Machín1,*, Emilia Rossini1, Carlos Prigioni2, Francisco Kolenc2, Alejandro Crampet1, Claudio Borteiro1,2, and José Manuel Verdes1

Colour patterns can be highly variable in wild 14.8 cm of total length (TL) and 14.0 cm of snout-vent snake populations elsewhere, with several examples length (SVL). Colouration of the specimen fixed in of extreme variation, from complete absence formalin is homogeneously pale cream (Fig. 1A). It was of pigmentation (albinism) to the occurrence of captured along with three other adults that have normal hyperpigmented individuals (Betchel, 1995). Three colouration (MNHN 1626, 2825, 2826; Fig. 1A). The basic types of chromatophore cells are responsible creamish colouration of MNHN 2827 can be caused by for skin colouration in non-mammalian vertebrates, lack of melanin expression or amelanism. Normal colour the melanophores which provide the black and brown pattern of E. munoai include yellowish and greenish colours, the xanthophores that produce red and yellow stains (Fig. 1A, inset) that are usually lost in fixatives, pigments, and the iridophores that variably reflect so we cannot assess whether the studied specimen is colour hues (Bagnara, 1968; Betchel, 1995). Snakes an albino or just amelanistic. To date, this is the only with diminished pigmentation are rare in nature, and known hypopigmentation record in Leptotyphlopidae a few cases were reported for Neotropical species (Sazima and Di-Bernardo, 1991; da Silva et al., 2010; (Sazima and Di-Bernardo, 1991; da Silva et al., 2010; Abegg et al., 2015; de Mira-Mendes et al., 2017). Abegg et al., 2015; de Mira-Mendes et al., 2017). In The new instances of hypopigmented snakes reported this work we present observations about novel cases herein concern a juvenile female of Philodryas of hypopigmentation in wild snakes native to Uruguay, patagoniensis (Girard, 1858) (Dipsadidae) captured and provide a reassessment of previously reported ones in eastern Departament of Treinta y Tres (32º55’S, from this country. 53º42’W), in March 2018. It measured 45 cm TL and 38 The first publication about hypopigmented snakes cm SVL. Ventral and dorsal scales of this specimen are from Uruguay is a brief comment about the finding mainly cream, with orange stains principally along their of an albino Epictia munoai (Orejas-Miranda, 1961) anterior and posterior margins; the eyes are red, with (Leptotyphlopidae), by Orejas-Miranda (1972) who the upper and posterior pupil margins orange and the did not give further description or illustrations. The tongue is reddish and pink (Fig. 1B). A noticeable scar is snake is an adult specimen from Arroyo Salsipuedes present for approximately 2 cm at the end of tail, likely (32º34’ S, 56º35’ W), Departament of Río Negro, due to abnormal shedding. When comparison is made collected on 13 July 1966, housed at the herpetological with the usual brown pattern expected for this species collection of Museo Nacional de Historia Natural de (Fowler and Salomão, 1994), it seems that only dark Montevideo, Uruguay (MNHN 2827). It measures pigmentation is absent. This phenotype corresponds to amelanism or amelanistic albinism (Prüst, 1984; Betchel, 1995). Duarte et al. (2005) mention the finding of two “albino” juveniles of P. patagoniensis from southeastern Brazil, without further detail. The additional new case from Uruguay is a subadult 1 Departamento de Patología, Facultad de Veterinaria, specimen of Bothrops alternatus Duméril, Bibron & Universidad de la República, Alberto Lasplaces 1550, Duméril, 1854 (Viperidae), photographed by local Montevideo 11600, Uruguay. 2 Sección Herpetología, Museo Nacional de Historia Natural, 25 people at Arroyo León, approximately 15 km SW from de Mayo 582, Montevideo 11000, Uruguay. Aiguá (34º17’S, 54º39’W), Department of Maldonado, * Corresponding author. E-mail: [email protected] in January 2014 (not captured). It exhibited the normal 1052 Victoria Machín et al.

Figure 1. Hypopygmented wild snakes from Uruguay. A, Epictia munoai, adult fixed specimens with normal pattern (left) and hypopygmented (right). Inset: live normal specimen. B, amelanistic Philodryas patagoniensis, juvenile. Inset: detail of head and tongue. C, hypomelanistic Bothrops alternatus, subadult. D, piebald Boiruna maculata, adult.

pattern of the species, but notoriously less intensely specimens were 122 cm and 97 cm respectively, and the coloured. The usual brown pattern with darker brown colouration was completely white, except for the dorsal stains limited by fine white stripes (Carreira et al., surface of the cephalic region and some small scattered 2005), is replaced by light brown stains but still black stains that partially invade the contiguous ventral contrasting to a creamish background, which account scales (Fig. 1D). Boiruna maculata is usually solid dark for hypomelanism (Fig. 1C). Two observations of grey or black, more intense above, sometimes with extreme hypopigmentation (“albinism”) in B. alternatus whitish spots as depicted from its original description are known from Brazil (Bücherl, in Sazima and Di- (Boulenger, 1896; Scott et al. 2006). Occasionally, Bernardo, 1991; Veiga and Teixeira, 1993). An inverse extensive reticulated white stains are present throughout situation, melanin hyperpigmentation or melanism was the body, and less commonly white colour predominates observed by Hoge (1952) in this species. (Cei, 1993; Giraudo 2001). This last condition, as seen Besides, an adult male of Boiruna maculata in ZVC-R 5459, is known as piebaldism, commonly (Boulenger, 1896) (Dipsasidae) was reported as albino considered among the incomplete albino phenotypes by Carreira et al. (2005). This specimen was found exhibited by snakes (Betchel, 1995). Boiruna maculata dead on km 415 of Route 3 (31º59’ S, 57 º50’ W), and the related species Pseudoboa nigra (Duméril, Departament of Paysandú, and is deposited at the reptile Bibron & Duméril, 1854) are the only two Neotropical collection of Departamento Zoología Vertebrados snakes in which piebaldism occurs naturally (Prado, (ZVC-R 5459), Facultad de Ciencias, Universidad de 1939; Noronha et al., 2013). la República, Montevideo. Total length and SVL of the The rarity of hypopigmentation in wild snakes from Hypopigmentation in wild snakes from Uruguay 1053

Uruguay seems to be also the case of other Neotropical 38‒39. snakes, as only a few cases have been reported from large Carreira, S., Meneghel, M., Achaval, F. (2005): Reptiles de regions with species-rich snake assemblages (Sazima Uruguay. Montevideo, Facultad de Ciencias, Universidad de la República, 637 pp. and Di-Bernardo, 1991). Recently, hypopigmentation Cei, J.M. (1993): Reptiles del noroeste, nordeste y este de la in the fossorial snake Phalotris lemniscatus (Duméril, Argentina: Herpetofauna de las selvas subtropicales, Puna y Bibron and Duméril, 1854) from Uruguay was reported Pampas. Monografie XIV. Torino, Italy, Museo Regionale di by Abegg et al. (2015). Most reports of partial and total Scienze Naturali, 949 pp. albinism in Neotropical wild snakes involve species Choate, L.D. (1963): An albino population of Elaphe climacophora with fossorial or mainly nocturnal habits, like E. from Iwakuni, Japan. Herpetologica 18:� 260� 62. munoai, and B. alternatus and B. maculata respectively da Silva, F.A., de Assis, C.L., Quintela, F.M. (2010): Albinism in a Liophis miliaris (Linnaeus, 1758) (Serpentes: Dipsadidae) (Sazima and Di-Bernardo, 1991; Cardoso and Parpinelli, from Minas Gerais State, southern Brazil. Herpetology Notes 2006; Abegg et al., 2015; de Mira-Mendes et al., 3: 171‒172. 2017). However, P. patagoniensis has diurnal activity de Mira-Mendes, C.V., Rios, C.H.V., Martins, R.A., Medeiros, (Hartmann and Marques, 2005). Albino snakes with T., Solé, M., Argôlo, A.J.S. (2017): A case of albinism in nocturnal habits may have a greater change to avoid Amerotyphlops brongersmianus (Vanzolini, 1976) (Serpentes: mortality by visually oriented predators, particularly Typhlopidae) from southern Bahia, northeaestern Brazil. birds (Sazima and Di-Bernardo, 1991). As expected, Herpetology Notes 10: 131‒132. albino phenotypes are not commonly seen in wild snake Duarte, M.R., Franco, F.L., Oliveira, A.L. (2005): New records of albinism in neotropical snakes. Memórias do Instituto Butantan populations. An exception is a population of Elaphe 61: 66. climacophora (Boie, 1826) from Iwakuni, Japan, Fowler, I.R., Salomão, M.G. (1994): A study of sexual dimorphism with a high frequency of albinos. This phenomenon in six species from the colubrid genus Philodryas. The Snake is apparently strongly influenced by human pressure 26: 117‒122. because of governmental protection of the population, Giraudo, A. (2001): Serpientes de la Selva Paranaense y del Chaco combined with geographic isolation and elimination of Húmedo. Buenos Aires, LOLA, 289 pp. other phenotypes and snakes species by local people Hartmann, P.A., Marques, O.A.V. (2005): Diet and habitat use of two sympatric species (Choate, 1963). Further studies about the presentation of Philodryas (Colubridae), in south Brazil. Amphibia-Reptilia 26: of hypopigmented phenotypes in different ecological 25‒31. traits, inheritance mechanisms and their relevance to Hoge, A.R. (1952): Anomalia na lepidose e pigmentação das survival in wild populations are needed. escamas dorsais em B. jararaca e B. alternata. Memórias do Instituto Butantan 24: 237‒240. Acknowledgements. The authors are grateful to Diego Arrieta Noronha, J. da C., Barros, A.B., de Miranda, R.M., Almeida, E.J., (MNHN), and Melitta Meneghel and Raúl Maneyro (ZVC-R) Rodrigues, D.J. (2013): Record of leucism in Pseudoboa nigra for allowing working space at their institutions, to Lucy Fros (Serpentes: Dipsadidae). Herpetology Notes 6: 81‒82. for loaning the specimen of P. patagoniensis, and Alejandro Orejas-Miranda, B. (1972): Observaciones sobre un caso de Fernández for information regarding B. alternatus. Carlos Piña albinismo de Leptotyphlops munoai. Boletín de la Sociedad kindly reviewed an early version of the manuscript. CB, FK Zoológica del Uruguay 2: 36. and JMV acknowledge Agencia Nacional de Investigación e Prado, A. (1939): Notas ofiológicas 3. Mais um caso de albinismo Innovación (ANII/SNI). em serpente. Memórias do Instituto Butantan 13: 1‒5. Prüst, E. (1984): Albinism in snakes. Litteratura Serpentium 4: References 6‒15. Sazima, I., Di-Bernardo, M. (1991): Albinismo em serpentes Abegg, A.D., Entiauspe Neto, O.M., de Lema, T. (2015): First neotropicais. Memórias do Instituto Butantan 53: 167‒173. record of albinism in the Elapomorphini tribe (Serpentes: Scott, N.J., Giraudo, A.R., Scrocchi, G., Aquino, A.L., Cacciali, P., Dipsadidae). Herpetology Notes 8: 503‒505. Motte, M. (2006): The genera Boiruna and Clelia (Serpentes: Bagnara, J.T., Taylor, J.D., Hadley, M.E. (1968): The dermal Pseudoboini) in Paraguay and Argentina. Papéis Avulsos de chromatophore unit. Journal of Cell Biology 38: 67‒79. Zoologia 46: 77‒105. Betchel, H.B. (1995): Reptile and amphibian variants. Color, Veiga, L. A., Teixeira, A. (1993): Albinismo em Bothrops pattern, and scales. Malabar, Florida, USA, Krieger Publishing alternatus Dm. � Bibr., 1854 (Ophidia, Viperidae). Arquivos Co., 206 pp. de Biologia e Tecnologia 36: 521‒524. Boulenger, G.A. (1896): Catalogue of the snakes in the British Museum. Vol. III. Trustee of the British Museum, London, 727 pp. Accepted by Seyyed Saeed Hosseinian Yousefkhani Cardoso, S.R.T., Parpinelli, C. (2006): Crotalus durissus terrificus (Rattlesnake): a case of xanthism. Herpetological Bulletin 97: