Herein, we report the first observation of two different coloration patterns in Chilean snakes. Based on the alteration of wild coloration patterns, a juvenile specimen of Tachymenis chilensis coronellina Werner, 1898 was diagnosed with albinism and a juvenile specimen of Tachymenis chilensis chilensis (Schlegel, 1837) was diagnosed with leucism. The existence of color variations in wild snake populations and the implications of these for fitness are discussed.

phenotype, reptiles, short-tailed snake, skin coloration, South American snakes

Snake species have evolved numerous coloration patterns with functions that aid in thermoregulation, camouflage, warning, and mimicry (Bechtel 1978, Krecsák 2008). However, inherited color defects, such as albinism and leucism, are well documented in many species of snakes (Bechtel 1991).

Leucistic animals present eyes normally pigmented, usually black, or blue (Wareham 2005) whereas the skin has either reduced coloration or lacks it entirely (Sage 1962, Bechtel 1995). Leucistic snakes have a diminished number of iridophores and probably an exceptionally low number of melanophores and xanthophores or none at all (Bechtel 1991), and lack eumelanin and phaeomelanin (Bechtel 1995, Van Grouw 2006). On the other hand, albinism is generally defined as the absence of the black and brown pigmentation usually provided by melanophore cells, but the other two types, xanthophores, and iridophores are functional, which results in skin with a pattern of yellow, orange, and red pigments, and red eyes (Bechtel 1991). Nevertheless, albinism relies on defects to several biochemical pathways caused by different genetic defects and producing partial and total albinism (Bechtel 1991, 1995). Although there are numerous reports of total albinism, partial albinism, and leucism in snakes worldwide, some of them require detailed revision if the diagnoses were incorrectly made. Recently, Devkota et al. (2020) showed a list of snake species with leucism, which were verified with a photograph or description that specifically mentioned the coloration of the eyes. Remarkably, leucism has also been confused with albinism in snakes (e.g., Sazima and Di-Bernardo 1991, Vyas 2009, Thombre and Dhande Abhishek 2015).

The genus Tachymenis is distributed through Peru, Bolivia, Argentina, and Chile, with six species currently recognized. In Chile, Tachymenis comprises T. peruviana Wiegmann, 1834 and T. chilensis (Schlegel, 1837), the latter species containing two subspecies T. c. coronellina Werner, 1898 and T. c. chilensis (Schlegel, 1837), fide Ruiz de Gamboa 2020. Tachymenis c. coronellina is distributed from San Fernando in the south to Antofagasta in the north (Valenzuela-Dellarossa et al. 2010). Tachymenis c. chilensis is a small snake distributed from Monte Lorenzo and Toquihua (O´Higgins Region) to Chiloé Island, further south in the Los Lagos Region of Chile (Ortiz 1973, Simonetti 2001, Valenzuela-Dellarossa et al. 2010) (Fig. 1A). In Argentina, T. c. chilensis is recorded from Neuquén, Chubut and Río Negro provinces (Cei 1986, Avila et al. 2012, Giraudo et al. 2012, Nenda et al. 2017), where it inhabits riverbanks with rocks and forests of Nothofagus and Araucaria (Giraudo et al. 2012). T. chilensis exhibits considerable variability of color and dorsal pattern, including reduction of the dorsal lines and melanism in the Chilean southern populations (Hellmich 1937, Donoso-Barros 1966, Flores 2018); however, no formal studies on color variations and their relevance to geographic distribution or natural history have been conducted. Herein, we describe the first observations of leucism and albinism in specimens of Tachymenis chilensis.

Figure 1. 

A. Distribution of Tachymenis species in Chile based in Valenzuela-Dellarrossa et al. (2010). The location of the specimens with albinism and leucism are represented in green and purple stars, respectively. Map was done using ARCGIS v10.7 (ESRI) software; B. T. c. coronellina with albinism; C. T. c. chilensis with leucism.

In November 2018, in the vicinity of Totoralillo (30°03'54"S, 71°22'10"W), a specimen of Tachymenis chilensis coronellina with abnormal coloration was found between low bushes near an old and abandoned house at 13.21 h (GMT-4). The specimen was measured and photographed (Fig. 1B and Table 1). This snake exhibited a dorsal pattern of white and yellow and possessed red eyes, so it was diagnosed as albino.

In February 2014, during fieldwork in the vicinity of Segundo Corral, Los Lagos Region, Chile (42°04'33"S, 71°51'49"W), an abnormally patterned specimen Tachymenis chilensis chilensis was found crossing a path between Nothofagus and Drymis forests at 12.00 h (GMT-4). The specimen was measured and photographed (Fig. 1C and Table 2) and released where it was found. This snake lacked any dorsal patterning, being fully white while its eyes were gray with black vertical pupils. Leucism was diagnosed based on these characteristics.

To compare the morphological characteristics and coloration of T. chilensis specimens, we reviewed 361 specimens of Tachymenis c. coronellina and T. c. chilensis deposited between 1947 until 2020 in Museo Nacional de Historia Natural de Chile (MNHNC; 39 specimens), Colección de Flora y Fauna Profesor Patricio Sánchez Reyes of Pontificia Universidad Católica de Chile (SSUC; 3 specimens), Museo de Zoología of Universidad de Concepción (MZUC; 316 specimens), and Museo Regional de Historia Natural de Concepción (MHNC; 3 specimens). Measurements of head length (HL), head width (HW), head high (HH), and total length (TL) were taken with a hardened stainless steel digital Vernier caliper (0.01 mm precision). These morphological data were obtained only for neonates from herpetological collections to be used for comparisons with specimens reported in this study with leucism and albinism (Table 1 and 2).

Substantial differences in dorsal patterning and coloration were observed during the review of the specimens of T. chilensis included in the four Chilean herpetological collections. Specimens of T. chilensis exhibited yellow or gray coloration with dorsal black stripes, which can be separated or in contact with the following stripe (Fig. 2A, B). Some specimens had an extension of black coloration of dorsal stripe on their yellow background, predominating the black as dorsal and ventral coloration (Fig. 2C). This suggests a pseudo-melanistic phenotype in which occurs an unusual enlargement of the pattern of dark spots of the animal as has been reported for other snakes (Fernández-Guiberteau et al. 2015). Melanism, which is due to excessive dark pigmentation of the integument by mutations, also has been observed (Fig. 2D) as previously described by Donoso-Barros (1966). None of the museum voucher specimens exhibited leucism or albinism. Taking into consideration the current dearth of studies about the abundance of leucism and albinism in Chilean snakes, we calculated the prevalence and incidence of these phenotypes using the specimens collected over 73 years of fieldwork plus our two observations. We determine a low prevalence (0.27%, i.e. 1 specimen observed with albinism or leucism in 363 specimens) and low incidence (1.37%, i.e. 1 specimen identified with albinism or leucism in 73 years of fieldwork) for these alterations in coloration in T. chilensis.

Figure 2. 

Variations of the coloration in Tachymenis c. coronellina and T. ch. chilensis. A–C. Variations in black stripes in T. c. coronellina (MZUC 25351, SSUC-Re 440, SSUC-Re 023); D. Total melanism in T. c. chilensis (FMNH 3871); E, F. Neonates of Tachymenis c. coronellina. The red arrowheads show dorsal pattern (MZUC11512, MZUC44953); G. Dorsal view (MZUC45033) of neonate of Tachymenis c. chilensis.

The reproductive biology of Chilean snake species is poorly known (Donoso-Barros and Rubio 1962, Cabeza et al. 2019). To determine if the specimens with leucism and albinism observed may be neonates, we studied two series of neonates collected from females of T. c. coronellina and T. c. chilensis, during January 1961 Polpaico, Metropolitan Region, and March 1971 in Laraquete, BioBio Region, respectively. All neonates exhibited the normal phenotype comprised of a gray or brown background with black vertebral lines or stripes (Fig. 2E–G, arrowheads). No differences in coloration or pattern were found between neonates and adults with normal phenotype. On the other hand, morphological measurements of neonates of T. c. coronellina and T. c. chilensis, and the specimens with albinism and leucism described in this work exhibited similar size and length to the normal phenotype (Table 1 and 2), suggesting that the specimens with abnormal coloration were of early ontogenetic age. In this report, we described the first cases of both albinism and leucism in the genus Tachymenis. Our review of 73 years of collection in the field shows that adults and neonates exhibit normal phenotype with variations in the extension of dorsal stripes, and some specimens acquiring more black coloration as previously described (Donoso-Barros 1966). In contrast, with reports that in some populations of Japanese Elaphe climacophora, where albino and leucistic adults are common (Fukada 1978, Iwanishi et al. 2018), leucism and albinism have apparently low prevalence and incidence for T. chilensis. Notably, the implications of these rare phenotypes on metabolism and thermoregulation in these specimens as well as their fitness in the environment remain largely unknown. Further studies are required to understand the relevance of these abnormalities of coloration and their implications for the natural history of Tachymenis species.

This work was supported by CONICYT PCI-Biotechnology #Redbio0027, FONDECYT #11201322, and U-Inicia UI-024/20.