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

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  • Podyjí National Park , Znojmo, Czech Republic

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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),
RECORDED FROM GEORGIA
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: zdenek.macat@gmail.com
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;
e-mail: daniel.jablonski@balcanica.cz
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.
a
b
Fig. 1. The erythristic Coronella austriaca:a, dorsal side; b, ventral
side.
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.
... 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 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.
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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.