Erythrism in the Long-tailed Alpine Garter Snake, Thamnophis
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Herpetology Notes, volume 16: 175-177 (2023) (published online on 26 February 2023) Erythrism in the Long-tailed Alpine Garter Snake, Thamnophis scalaris (Squamata: Colubridae), from Puebla and Tlaxcala, México Luis F. Hidalgo-Licona1,2,*, Antonio Y. Cisneros-Bernal1,2,3, Gonzalo Medina-Rangel1,3, and Carlos A. Hernández-Jiménez4 Colour variation has been extensively studied in and strongly contrast with the ventral colouration. reptiles at the inter- and intra-populational level, as it is The supralabial scales are cream coloured with black an attribute with ecological, evolutionary, and taxonomic anterior and posterior highlights. Nuchal blotches are implications (Brodie, 1993; Mooi et al. 2011; Isaac usually interrupted by a vertebral stripe that is either and Gregory, 2013). In some cases, colour variation cream-coloured (Fig. 1A) or yellow (Fig. 1B), and they represents a non-adaptive trait that has resulted from are either partially or completely separated from the an anomaly in the expression of pigmentation in certain parietal to each side by a thin vertical line. The lateral individuals, and can lead to albinism (Stephenson and stripe is the same colour as the vertebral stripe is found Drace, 2014), melanism (King, 2003), and erythrism on either side of the body. (Jablonski et al., 2022). Erythrism is characterised by the unusual increase in pheomelanin in the skin of some vertebrates, producing an overall reddish pigmentation that can vary in tone and/or intensity (Moore and Ouellet, 2014). Thamnophis scalaris Cope, 1861 is a moderately sized natricine colubrid species (snout-vent length 600 mm) that inhabits the mountainous regions of south-central México within an elevational range of 2100–4270 m (Ramírez-Bautista et al., 2009). Rossman (1996) and Rossman and Gongora (1997) described the species’ colouration as predominately brown, with shades that range from lighter (Fig. 1A) to darker (Fig. 1B), and a series of small blotches with brown or black stripes on either side of the body. The venter is generally brownish grey, occasionally with slight black stippling throughout. The mental and the throat are white, cream, or yellow, 1 Museo de Zoología “Alfonso L. Herrera”, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, CDMX 04510, México. 2 Ciudad Universitaria, Universidad Nacional Autónoma de México, Cuidad de México, CDMX 04510, México. 3 Totlok A. C., Ciudad de México, CDMX 04350, México. 4 Facultad de Ciencias Biológicas, Benemérita Universidad Figure 1. The typical appearance of Thamnophis scalaris. (A) Autónoma de Puebla, Av. San Claudio s/n Edif. 112, Puebla, Adult male from Apatlaco in Parque Nacional Iztaccíhuatl- 72570 Puebla, México. Popocatépetl, México. (B) Adult male from La Venta in Parque * Corresponding author. E-mail: fernandohlicona@outlook.com Nacional Iztaccíhuatl-Popocatépetl, México. Photographs by © 2023 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. Luis F. Hidalgo-Licona.
176 Luis F. Hidalgo-Licona et al. Despite being in a subsequent search, we identify two Burnt Orange (10), with Sepia (286) highlights on the other cases of erythrism in the Long-tailed Alpine Garter anterior and posterior margins (Fig. 2A). The venter is Snake (see below), this is the first time it is reported and of Burnt Orange (10) colouration in the anterior region, described in detail. At 17:00 h, on 26 May 2022, we degrading into a Light Buff (2) colouration posteriorly collected an individual of Thamnophis scalaris in the (Fig. 2B). The mental is Pale Buff (1) with slight Burnt municipality of San José Chiapa in the Mexican state Orange (10) stippling anteriorly that becomes more of Puebla (19.2705°N, -97.7058°E; 2393 m elevation) uniform and intense closer to the throat, in a notable (Fig. 2). The specimen MZFC 36449 was a juvenile contrast with the ventral colouration (Fig. 2C). The female (snout-vent length: 285 mm; tail length: 90 mm) nuchal blotches are completely separated from the found within a rock crevice situated on the margin of parietal by the vertebral stripe, which is a Warm Buff an irrigation canal. The specimen was euthanised with (4) colour (Fig. 2D). a pentobarbital solution following the specific protocol Other cases of erythrism in colubrids have been for reptiles by the AVMA guidelines for the Euthanasia registered in Natrix natrix (Linnaeus, 1758) (Jablonsky of Animals (Underwood et al., 2013). Finally, the et al., 2022), Coronella austriaca Laurenti, 1768 (Macat specimen was preserved in 96% ethanol and deposited et al., 2016), and Thamnophis sirtalis (Linnaeus, 1758) in the Museo de Zoología “Alfonso L. Herrera” at (Gilhen, 2010). It the case of the latter, Fitch (2001) the Facultad de Ciencias of the Universidad Nacional and Mooi et al. (2011) report that in two populations, Autónoma de México. one from Kansas, USA and the other from Manitoba, Based on the Colour Catalogue for Field Biologists Canada, that a greater proportion of erythrism is (Köhler, 2012), the specimen MZFC 36449 possesses observed in females with respect to males, a pattern a lateral stripe on either side of the body coloured that could be related to antipredator behaviour. Even Spectrum Orange (9), contrasting with a dorsal though it is not possible to compare such findings colouration of Sepia (286) on a Vandyke Brown (282) with the single specimen reported herein, another background (Fig. 2A). Supralabial scales are uniform unpublished record exists of a specimen of T. scalaris Figure 2. An erythristic individual of Thamnophis scalaris (MZFC36449) from San José Chiapa, Puebla, México, in different views: lateral (A), ventral (B), gular (C), and dorsal (D). Photographs by Gonzalo Medina Rangel.
Erythrism in the Long-tailed Alpine Garter Snake, from Puebla and Tlaxcala, México 177 with similar colouration as the one presented here (Fig. 3). A juvenile female was photographed by Alan Emir Díaz Félix on 11 November 2021 from Nativitas, Tlaxcala (19.2447°N, -98.3699°E; 2215 m elevation), 69.77 km in straight-line distance from our collected specimen. An online search on iNaturalist revealed an additional record of erythrism in T. scalaris from the Xaloztoc municipality in Tlaxcala, México (19.4368°N, -98.0178°E; 2489 m; 20 November 2014; www. inaturalist.org/observations/1094338), published by Juan Carlos López Domínguez. This record is situated 37.75 km in straight-line distance from the collected specimen MZFC 36449. These findings are interesting given that the three reports from which we have photographic confirmation Figure 3. An erythristic individual of Thamnophis scalaris all pertain to a region between the states of Puebla and from Nativitas, Tlaxcala, México. Photograph by Alan Emir Tlaxcala, two are females, and were found at the lower Díaz-Félix. limits of the species’ known elevational range (Ramírez- Bautista et al., 2009). Future projects are necessary to King, R.B. (2003): Mendelian inheritance of melanism in the garter evaluate if this colour variation can be attributed to some snake Thamnophis sirtalis. Herpetologica 59(4): 484–489. intersexual, inter-populational, or ecological factor, or Köhler, G. (2012): Colour catalogue for field biologists. Herpeton, if they represent isolated cases of intra-populational Offenbach, 49 p. variation. Macat, Z., Hegner, D., Jablonski, D. (2016): Erythrism in the smooth snake, Coronella austriaca (Laurenti, 1768), recorded Acknowledgments. We thank Alan Emir Díaz-Félix for providing from Georgia. Russian Journal of Herpetology 23(1): 73–76. us with information and photographs of the specimen found Mooi, R.D., Wiens J.P., Casper, G.S. (2011): Extreme colour in Nativitas, Tlaxcala (Fig. 3). We also thank Ricardo Palacios variation within populations of the Common Gartersnake, Aguilar for comments on a draft of the manuscript. The first Thamnophis sirtalis, in central North America, with implications author LFHL, is grateful to the Posgrado en Ciencias Biologicas for subspecies status. Copeia 2011: 187–200. at UNAM, as well as the Consejo Nacional de Ciencias y Moore, J.D., Ouellet, M. (2014): “A review of colour phenotypes Tecnología (CONACyT) for supported by a scholarship (grant of the Eastern Red-backed Salamander, Plethodon cinereus, in number 850195). North America,” The Canadian Field-Naturalist 128: 250–259. Ramírez-Bautista, A., Hernández-Salinas, U., García-Vázquez, References U.O., Leyte-Manrique, A., Canseco-Márquez, L. (2009): Herpetofauna del Valle de México: diversidad y conservación. Brodie III, E.D. (1993): Differential avoidance of coral snake Universidad Autónoma del Estado de Hidalgo, 213 pp. banded patterns by free-ranging avian predators in Costa Rica. Rossman, D.A. (1996): The garter snakes: evolution and ecology. Evolution 47: 227–235. University of Oklahoma Press. 254 pp. Fitch, H.S. (2001): Further study of the garter snake, Thamnophis Rossman, D.A., Gongora, G.L. (1997): Variation in the Mexican sirtalis, in northeastern Kansas. Scientific Papers of the garter snake Thamnophis scalaris Cope and the taxonomic University of Kansas Natural History Museum 19: 1–6. status of T. scaliger (Jan). Occasional Papers of the Museum of Gilhen, J. (2010): Erythrism in the Maritime Garter Snake, Natural Science, Louisiana State University 1: 1. Thamnophis sirtalis pallidulus, in Nova Scotia. The Canadian Stephenson, B.P., Drace, K.M. (2014): A new report of albinism in Field-Naturalist 124(2): 99–103. the Common Garter Snake (Thamnophis sirtalis), and a review INaturalist (2022): Comisión Nacional para el Conocimiento y of existing records: Is there a geographic bias in observations? Uso de la Biodiversidad. Available at https://www.inaturalist. Herpetological Review 45: 569–577. org/observations/1094338https://www.inaturalist.org/ Underwood, W., Anthony, R., Cartner, S., Corey, D., Grandin, observations/1094338. Accessed on 7 Novembrer 2022. T., Greenacre, C.B., et al. (2013): AVMA guidelines for the Isaac, L.A., Gregory, P.T. (2013): Can snakes hide in plain view? euthanasia of animals: 2013 edition. Schaumburg, IL: American Chromatic and achromatic crypsis of two colour forms of Veterinary Medical Association. the Western Terrestrial Garter Snake (Thamnophis elegans). Biological Journal of the Linnean Society 108: 756–772. Jablonski, D., Trapp, B., Tzoras, E., Mebert, K. (2022): Erythrism Accepted by Michael Jowers in the Eastern Grass Snake, Natrix natrix (Linnaeus, 1758). Herpetozoa 35: 213–217.
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