Erythrism in the Long-tailed Alpine Garter Snake, Thamnophis

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Erythrism in the Long-tailed Alpine Garter Snake, Thamnophis
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.
Erythrism in the Long-tailed Alpine Garter Snake, Thamnophis
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, Thamnophis
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,
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