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Erythrism in the Smooth Snake, Coronella austriaca (Laurenti, 1768), Recorded from Georgia

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Color aberration are frequently known in snakes, however erythrism is one of the rarest. In this paper, we report the capture of one erythristic male of Coronella austriaca from Georgia and we also present actual knowledge about color aberration in this species.
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ERYTHRISM IN THE SMOOTH SNAKE, Coronella austriaca (LAURENTI, 1768),
Zdenìk Maèát,1David Hegner,2and Daniel Jablonski3
Submitted June 23, 2015.
Color aberration are frequently known in snakes, however erythrism is one of the rarest. In this paper, we report
the capture of one erythristic male of Coronella austriaca from Georgia and we also present actual knowledge
about color aberration in this species.
Keywords: color aberration; Colubridae; Coronella austriaca; Caucasus.
Three classes of chromatophores have impact upon
coloration of reptiles (Bechtel, 1995; Vitt and Caldwell,
2013): melanophores (brown to black pigment cells),
iridiophores (produce the shiny iridescent and reflecting
skin) and xanthophores (yellow and red pigment cells).
Different types of color aberrations are slightly wide-
spread between all animal groups, usually results of gene
mutations in development or uncommon distribution of
chromatophores in the skin (Bechtel, 1995). In reptiles,
eight different types of color aberrations have been de-
scribed; most common are albinism, leucism or mela-
nism and rare are amelanism, axanthism, erythrism, hy-
pomelanism or piebaldism (Bechtel, 1995) although their
nomenclature is not consensual.
One of the most frequent color aberrations is mela-
nism, very common and often referred especially in
snakes (e.g., Andrén and Nilson, 1981; Shine and
Madsen, 1994). It represents a large amount of black col-
oring at the expense of other colors (Majerus, 1998).
The melanistic individuals enjoy a thermal advantage
due to their superior thermoregulatory capabilities
afforded by dark color of body. On the other hand, they
also suffer from higher predation pressure (Andrén and
Nilson, 1981; Tanaka, 2009). In European species of Co-
lubridae, melanism has been recorded in Coronella aus-
triaca (Pernetta and Reading, 2009), Natrix natrix (e.g.,
Opatrný, 1974; Jandzík, 2004; Naumov and Tomoviæ,
2005; Mollov, 2012; Gvozdenoviæ and Schweiger, 2014),
N. tessellata (Laòka, 1978; Gvozdenoviæ and Schweiger,
2014), or Zamenis longissimus (Zadravec and Lauš,
2011). One species, Hierophis carbonarius (also known
as former subspecies of H. viridiflavus in traditional tax-
onomy, see Mezzasalma et al. 2015)), is naturally
melanistic in adult age stage (Arnold and Ovenden,
2002). Cases of albinism and leucism are also common
color anomalies, but survival rate of individuals in nature
is probably low (e.g., Bechtel and Bechtel, 1981;
Krecsák, 2008). It is presenting as a white (yellow-
ish/pinkish) body with red or dark eyes (Bechtel, 1995).
These anomalies have been recorded e.g., in Natrix mau-
ra (Pérez and Collado, 1975), N. natrix (e.g., Boulenger,
1913; Musilová et al., 2006), N. tessellata (Werner, 1898;
Boulenger, 1913), C. austriaca (Werner, 1898; Rehák,
1992, Moravec, 2015), C. girondica (Martínez-Silvestre
et al., 2009), Rhinechis scalaris (Menjón, 2011) or Z. lon-
gissimus (Erber, 1879; Balthasar, 1935; Ferri and Bettiga,
1992). Other types of color aberrations at snakes in
general (axanthism or piebaldism) are probably rare, with
only several recorded reports in available literature
(Stegenga and Mohr, 2012; Kornilios, 2014).
As one of the rarest aberration at Palaearctic snakes is
erythrism. It is defined as naturally occurring color con-
dition of animals with excessive production and deposi-
tion of red and orange pigments (erythrophores) with var-
ious shades and degrees of intensity (Gilhen, 2010;
Moore and Ouellet, 2014). Among the European snakes
population, erythrism is very rare. However, in vipers are
known reddish or orange populations; Vipera berus,so
called aberration chersea Linnaeus, 1758 or V. ammody-
tes from Montenegro and northern Albania (Kreiner,
2007; Fric and Moravec, 2015). The one old record of
erythristic Z. longissimus from Slovakia is also known
(Lác, 1970).
1026-2296/2016/2301-0073 © 2016 Folium Publishing Company
Russian Journal of Herpetology Vol. 23, No. 1, 2016, pp. 73 – 76
1Department of Ecology and Environmental Sciences, Palacký Uni-
versity in Olomouc, Šlechtitelù 27, 783 71, Olomouc, Czech Repub-
lic; e-mail:
2Mšenská 3938/26, 466 04 Jablonec nad Nisou, Czech Republic.
3Department of Zoology, Comenius University in Bratislava, Mlynská
dolina B-1, 842 15, Bratislava, Slovakia;
The smooth snake (Coronella austriaca) is western
Palaearctic colubrid species, commonly widespread from
Portugal, Spain on a west to Iran, Kazakhstan and central
Russia to the east (Arnold and Ovenden, 2002; Sindaco et
al., 2013) with several independent phylogenetic lineages
occurring there (Galarza et al., 2015; Sztencel-Jab³onka
et al., 2015). According to Arnold and Ovenden (2002),
coloration in C. austriaca is considerably variable, but
usually grayish, brownish and pinkish. Males are usually
brighter than females and color pattern in adults occa-
sionally shows some correlation with habitat. Back is
colored with small dark spots, head with dark blotch
often crossing to two short dark stripes on the neck. Dark
stripe from side of neck through eye to nostril is also
present. Belly is usually darkish (red, orange or gray).
Juveniles are more contrast than the adults, abdomen is
often in brick red color.
One adult male of erythristic C. austriaca (Fig. 1)
was captured on 30 April 2013 in surroundings of village
Meneso (Mccheta-Mtianetie, Georgia; 42°15¢11¢¢ N
44°40¢26¢¢ E, 1003 m a.s.l.) in Agravi river valley. Indi-
vidual was found during cloudy weather without rain on
river rocky shore terrain. The animal dorsal surface was
reddish/brownish (Fig. 1a). Usual coloration patterns
(head blotch and stripes, nostril-neck stripes) were only
slightly visible. All these structures were reddish and
darker than rest of body. Belly was slightly orange. Other
recorded reptilian species at the locality were Lacerta
strigata Eichwald, 1831 and Darevskia rudis (Bedriaga,
1886). No other records of erythristic individuals of
C. austriaca are known from literature, however Rehák
(1992) referred about numerous reddish specimens of
C. austriaca (without any details) recorded in northeast-
ern Turkey and Azerbaijan. Besides erythrism, several
other color aberrations have been recorded in C. austria-
ca (see Table 1).
To our best knowledge, this is probably the first pub-
lished and photographed record of erythrism in C. aus-
triaca from Georgia, overall uncommon phenomenon in
snakes. There are no more data about benefits in selective
mechanisms or thermoregulation of erythrism in snakes
(Mooi et al., 2011). Red coloration could serve as an
aposematic coloration (Gotmark, 1994) or option of
defensive behavior like Batesian mimicry (Cassell and
Jones, 2005). However, there is number of snake species
that use red coloration as easily recognizable characteris-
tic and as a result they deceive a potential predator (e.g.,
Diadophis,Lampropeltis). Red coloration brings certain
advantages; e.g., experiments with salamanders (Pletho-
don cinereus) showed that birds selectively avoid attack-
ing erythristic individuals than normally colored (Tilley
et al., 1982). Similar results were confirmed in red-
striped morph of P. cinereus (Venesky and Anthony,
2007). Therefore, a single but significant evolutionary
event as predation pressure could probably evolve the
matching colors or patterns in common ancestor of some
group of snakes. Indeed, many snake species with red
coloration of its body (some members of genus Atractus,
Cylindrophis,Helicops,Oxyrhopus,Tripanurgos, juve-
nile of Clelia clelia,Oreocryptophis, etc.) live in the
tropics where the predation pressure is potentially higher.
However, also other explanations in connection of
red color may be discussed. For instance, Fitch (2001)
proposed a link between red color and aggressive behav-
ior. According to Thurow (1955), rather genetics is
involved in erythristic form than environmental factors.
This phenotype could result from the action of mutant
allele that quantitatively inhibits the development of
melanin (Thurow, 1955). Other explanation offer Mooi et
al. (2011), who suggested that color aberration is influ-
enced by local evolutionary forces like position of glacial
refuges of the species. According to current results based
on mtDNA analysis (Galarza et al., 2015; Sztencel-
74 Zdenìk Maèát et al.
Fig. 1. The erythristic Coronella austriaca:a, dorsal side; b, ventral
Jab³onka et al., 2015), independent phylogenetic lineage
of C. austriaca occurs in region of Caucasus what may
speculatively correspond with specific morphological
characteristics of the local population. In any event, an
adaptive evolution of color aberrations in snakes as well
as facts about red coloration phenomenon are underesti-
mated and other experimental research is needed.
Acknowledgments. We are grateful to Martin Rulík
(Olomouc, Czech Republic) for revision of first version of the
manuscript draft and to Boris Lauš (Zagreb, Croatia) and
Xavier Santos Santiró (Barcelona, Spain) for providing lite-
rature. Zdenìk Maèát was supported by IGA PøF UPOL:
No. IGA_PrF_2015_008.
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76 Zdenìk Maèát et al.
... The taxonomic breadth across which erythrism occurs in reptiles and amphibians is likely greater in nature than currently recognized in the literature. For example, erythristic Smooth Snakes (Coronella austriaca) have been recorded from elsewhere in their range(Maèát et al. 2016), but not yet from the British Isles. ...
Full-text available
Over the years, the terminology in regards to the abnormal coloration of reptiles and amphibians has become more complex with not all authors agreeing on the same terms. This, combined with the diversity of chromatic abnormalities, has led to some confusion, particularly between hobbyists and biologists who tend to use different jargon. In this review, we aim to address this issue by explaining how color within the skin of amphibians and reptiles arises, and evaluating which terminology should be used. This information is then used to explore each of the known chromatic abnormalities observed in amphibians and reptiles before summarizing the known cases from the British Isles. Finally, we also present a number of previously unrecorded instances of color abnormalities in the hope that it promotes further examples to be recorded. Given their rarity in nature, color abnormalities are likely to have a significant impact on the fitness of animals displaying them. Despite our efforts to summarize all the available information on color abnormalities in the herpetofauna of the British Isles, there are still gaps in our knowledge. These could be filled through the effort of a national recording scheme aimed at abnormally colored individuals.
... Other cases of erythrism in colubrids have been registered in Natrix natrix (Linnaeus, 1758) (Jablonsky et al., 2022), Coronella austriaca Laurenti, 1768 (Macat et al., 2016), and Thamnophis sirtalis (Linnaeus, 1758) (Gilhen, 2010). It the case of the latter, Fitch (2001) and Mooi et al. (2011) report that in two populations, one from Kansas, USA and the other from Manitoba, Canada, that a greater proportion of erythrism is observed in females with respect to males, a pattern that could be related to antipredator behaviour. ...
... Yet, it remains, that we can only speculate about the biological significance that is behind such reddish phenotypes and their rare manifestations in wild snake popula- tions (cf. Mačát et al. 2016;Zúñiga-Baos 2020;Borteiro et al. 2021). Thus, due to the rarity of this colour morph in Grass Snakes, we would like to encourage more field herpetologists and naturalists to present their unusual observations of Grass Snakes with reddish colouration. ...
Full-text available
We describe the unusual case of erythrism in the Eastern Grass Snake, Natrix natrix. This colour morph is very rare and has not been reported in the literature before. Despite having observed thousands of N. natrix in the field, we personally detected this morph in only three individuals originating from Slovakia, Romania, and mainland Greece, while photos of a fourth individual from a Greek island were provided to us. In addition, a recent study with a large data set from citizen scientists was unable to produce a single reddish Eastern Grass Snake. Such colouration is likewise uncommon in the western members of Grass Snakes (N. helvetica, N. astreptophora), with two examples provided herein. Because the potential biological importance of erythristic colouration is unclear, we encourage other field herpetologists and naturalists to publish their observations of reddish Grass Snakes in the printed literature.
... Erythrism (from the Greek eruthrós meaning red) has been recorded in birds (Hudon and Mulvihill 2017), mammals (Schwarz 1927), reptiles (Maèát et al. 2016) and amphibians (Tilley 1982), and apparently is caused either by genetic or dietary means (Hudon and Mulvihill 2017). Chromatophores (pigment-containing cells) are usually grouped based on the color they reflect under white light, in this case an increased number of erythrophores that reflect red light (Matsumoto 1965). ...
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The morphological characteristics of Coronella austriaca Laurenti, 1768 in the Samara region are presented. The proportion of melanists in the total sample (n = 147) was 2.04%. In wild-caught individuals of different ages and in calves obtained under laboratory conditions which were not in a state of molting, five variants of belly coloration (n = 140) were recorded, namely: black (17.1%), gray (5.0%), brown (17.9%), beige (2.9 %), and orange (57.1%). The first variant of coloration prevailed in mature snakes (48.6%, n = 37), while the latter did in newborns (72.5%, n = 58). The gray and beige shades of the belly began to appear after the second wintering, not occurring in newborns, underyearlings and yearlings. Individuals of both sexes in the total sample showed differences in the change rate of body weight with age, namely: longer and thinner individuals were observed among immature females (L.corp. ˂ 475 mm) than among males of the same size; after reaching sexual maturity (L.corp. > 475 mm) females weighed more than males (on average). The proportion of underyearlings caught in nature in the total sample was 8.8%. The female underyearlings (n = 8) had, on average, a greater body length with the head (L.corp.) and a smaller tail length ( as compared to males (n = 5), as well as they were slightly larger than males by total length ( on average. The average value of the L.corp. / index was higher in female underyearlings than in males (5.5 and 4.9, respectively). The ranges of its variability (4.9–5.9 for females and 4.2–4.9 for males, respectively) intersected in heterosexual underyearlings by only one value, 4.9. Sexually mature females (n = 37), compared to males (n = 35), had higher average and maximum values of L.corp. but lower average values of The L.corp. / index was less, on average, in adult males than in females; the ranges of its variability (3.1–4.4 and 4.5–7.5, respectively) did not overlap. Males had a lower mean value of Ventr. and more Scd. as compared with females (170.6 and 56.2 versus 184.0 and 49.5, respectively). The variability ranges of the first trait did not overlap and could be used to determine the sex of young individuals. The CAPO index in males (n = 61) was 0.62, which was somewhat higher than that in females (n = 45), 0.42. The proportion of asymmetric individuals of both sexes (n = 106) according to bilateral characteristics (Lab., Temp.I L/R, Temp.II, and L/R) was 54%.
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We used a multidisciplinary approach to infer the taxonomy and historical biogeography of Hierophis viridiflavus and H. gemonensis, performing molecular analyses of mitochondrial (16S, Cyt-b, ND4) and nuclear markers (PRLR), a landmark-based morphometric study and a cytogenetic analysis. Our data distinguished three main groups in the studied species, corresponding to H. gemonensis and to two monophyletic clades (E and W) within H. viridiflavus. Clades E and W display a significant genetic (about 4% for Cyt-b and ND4) and morphological divergence and a different morphology of the W sex chromosome (submetacentric in clade E and telocentric in clade W). Taking into account the existing divergence, these clades appear to represent independent phylogenetic units, deserving elevation to species status. Specific names should be H. viridiflavus (Lacépède, 1789) and H. carbonarius (Bonaparte 1833) for clades W and E, respectively. The phylogeography of the studied species is only partially concordant with a general pattern of ‘southern richness and northern purity’ of genetic diversity, whereas H. gemonensis exhibits high genetic diversity at low latitudes (especially in the Peloponnese), H. carbonarius shows a number of different haplotypes both at low (along the southern Italian Apennines and in Sicily) and high latitudes in Italy. Furthermore, a relaxed clock model hypothesizes the differentiation between H. gemonensis and H. viridiflavus sensu lato at about 7 Mya, in the Messinian. Subsequently, the speciation involving H. viridiflavus sensu stricto and H. carbonarius took place in the Quaternary, probably as a result of Pleistocene climatic oscillations. Furthermore, our results are consistent with the existence of several ‘refugia within refugia’ in Italy and in the Balkans and depict the major cladogenesis as allopatric events, mainly driven by paleoclimatic and geographical factors.
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The present study considers the genetic structure and phylogeography of the smooth snake (Coronella austriaca) in Central Europe, as analyzed on the basis of 14 microsatellite markers and a 284-bp fragment of cytochrome b. We found deep divergence between western and south-eastern Poland, suggesting at least two different colonization routes for Central Europe, originating in at least two different refugia. The west/south-east divide was reflected in the haplotype distribution and topology of phylogenetic trees as defined by mitochondrial DNA, and in population structuring seen in the admixture analysis of microsatellite data. The well supported western European clade suggests that another refugium might have existed. We also note the isolation-by-distance and moderate-topronounced structuring in the examined geographical demes. Our data fit the assumption of the recently suggested sex-biased dispersal, in that we found a strong divide in the maternal line, as well as evidence for a small but existent gene flow based on biparentally inherited microsatellite markers. All studied populations were very similar in respect of allelic richness, observed and expected heterozygosities, and inbreeding coefficients. However, some genetic characteristics were different from those expected compared to a similar fine-scale study of C. austriaca from Great Britain. In the present study, we observed heterozygosity deficit, high inbreeding, and low Garza–Williamson indices, suggesting a reduction in population size. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, ADDITIONAL KEYWORDS: biogeography – genetic diveristy – microsatellites – mtDNA – refugium.
The fourth edition of the textbook Herpetology covers the basic biology of amphibians and reptiles, with updates in nearly every conceptual area. Not only does it serve as a solid foundation for modern herpetology courses, but it is also relevant to courses in ecology, behavior, evolution, systematics, and morphology. Examples taken from amphibians and reptiles throughout the world make this book a useful herpetology textbook in several countries. Naturalists, amateur herpetologists, herpetoculturists, zoo professionals, and many others will find this book readable and full of relevant natural history and distributional information. Amphibians and reptiles have assumed a central role in research because of the diversity of ecological, physiological, morphological, behavioral, and evolutionary patterns they exhibit. This fully revised edition brings the latest research to the reader, ranging over topics in evolution, reproduction, behavior and more, allowing students and professionals to keep current with a quickly moving field.
The Eastern Red-backed Salamander (Plethodon cinereus) is the most abundant salamander species in many forests of northeastern North America. It is well-known for its colour polymorphism, which includes eight colour phenotypes: the red-backed (striped), lead-backed (unstriped) and erythristic morphs, as well as the iridistic, albino, leucistic, amelanistic and melanistic anomalies. Here we review the various colorations of P. cinereus, with the objective of facilitating the identification of these different phenotypes and of generating interest among field herpetologists and scientists reporting on this species. We also list six previously unpublished occurrences of colour variants in this species (1 case of erythrism, 3 of iridism, 1 of leucism, and 1 of partial leucism). To our knowledge, these cases include the first documented occurrence of iridism in the red-backed morph of P. cinereus, and the first two mentions of this colour anomaly in the lead-backed morph from Canada.
The Maritime Garter Snake, Thamnophis sirtalis pallidulus, is highly variable in pattern and colour. Although this subspecies is largely defined on the basis of colour, four colour morphs have previously been described for the subspecies, including a melanistic form. Based on specimens from Nova Scotia, Canada, a fifth, uncommon erythristic variant is added to the complex colour variation known for the Maritime Garter Snake.