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Albinism in Natrix tessellata (Serpentes: Natricidae). The Dice Snake, Natrix tessellata, varies in color and pattern, and has several color morphs. Except for melanism, color aberrations are quite rare in the species. Of the two published records of albinism in N. tessellata, the first, from the mid-19 th century in Italy is dubious; the second is from Israel. Herein, albinism in juvenile N. tessellata from Slovakia is documented, and the occurrence of albinism in all species of European snakes is discussed.
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165
Phyllomedusa - 19(2), December 2020
PROOFS
Received 27 April 2020
Accepted 14 July 2020
Distributed December 2020
Albinism in Natrix tessellata (Serpentes: Natricidae)
Simona Papezikova,1 Milan Oselsky,2 Petr Papezik,1 and Daniel Jablonski1
1 Department of Zoology, Comenius University in Bratislava, Mlynská dolina, Ilkovičova 6, 842 15, Bratislava, Slovakia.
E-mail: daniel.jablonski@balcanica.cz.
2 Košická Belá 274, 044 65 Košická Belá, Slovakia; Herpetolog.sk.
Phyllomedusa 19(2):165–176, 2020
© 2020 Universidade de São Paulo - ESALQ
ISSN 1519-1397 (print) / ISSN 2316-9079 (online)
doi: http://dx.doi.org/10.11606/issn.2316-9079.v19i2p165-176
Abstract
Albinism in Natrix tessellata (Serpentes: Natricidae). The Dice Snake, Natrix tessellata,
varies in color and pattern, and has several color morphs. Except for melanism, color
aberrations are quite rare in the species. Of the two published records of albinism in N.
tessellata, the rst, from the mid–19th century in Italy is dubious; the second is from Israel.
Herein, albinism in juvenile N. tessellata from Slovakia is documented, and the occurrence
of albinism in all species of European snakes is discussed.
Keywords: Central Europe, color aberration, Dice Snake, European snakes, Natricinae.
Resumo
Albinismo em Natrix tessellata (Serpentes: Natricidae). Natrix tessellata varia em cor e padrão e
tem várias formas de cores. Exceto pelo melanismo, as aberrações cromáticas são muito raras na
espécie. Dos dois registros de albinismo publicados para essa espécie, o primeiro, de meados do
século 19 na Itália, é duvidoso; o segundo é de Israel. Documentamos aqui o albinismo em jovens de
N. tessellata da Eslováquia e examinamos o contexto de albinismo observado entre outras serpentes
da Europa.
Palavras-chave: aberração cromática, albinismo, Europa Central, Natricinae, serpentes européias.
Introduction
Natrix tessellata (Laurenti, 1768) comprises
nine mitochondrial evolutionary lineages that
have a rather uniform morphology (Mebert
2011) across the wide range of the species
(Guicking et al. 2009). It is one of the most
common semiaquatic snake species in the
western Palearctic (Gruschwitz et al. 1999)
belonging to the family Natricidae (Zaher et al.
2019); it inhabits watercourses with mostly
rocky shores (Conelli et al. 2011) and feeds
mainly on sh or amphibians (Frotzler et al.
2011, Storm 2018). The species is known for its
color and pattern variation in natural populations
(Sterijovski et al. 2011), including different
color morphs (e.g., uniformly brown or
yellowish), and except for melanism, color
aberrations are rare (e.g., In den Bosch et al.
1998, Sterijovski et al. 2011, Tuniyev et al.
2011).
To date, only two albinotic individuals of
Natrix tessellata have been reported—one from
Italy and one from Israel. The albinotic juvenile
snake from Kfer Netter, Israel, was found alive;
other than a photograph, no further information
166
Phyllomedusa - 19(2), December 2020
Papezikova et al.
was provided by Werner (2016: 268). The snake
from Italy was found by Riccardo Magnani on
09 August 1879 at Cantone delle Tre Miglia,
near Pavia in northern Italy. It is a male with a
snout–vent length of 44.5 cm and tail length of
11.5 cm (total length, 55 cm). The specimen has
two preocular, three postocular, and eight
supralabial scales (Razzetti in litt. 2018). Pirotta
(1879) described it to be pinkish in color with
two darker spots on the scales on the top of the
head, and slight brownish shades on ventral and
subcaudal scales. However, leucism cannot be
excluded in this case as the original author Mr.
Magnani placed the specimen in alcohol,
believing it a venomous species. After a few
hours in alcohol, Pirotta (1879) could not
recognize the color of the iris; this led Pirotta
(1879) to consider the specimen as either
leucistic or albinotic. The snake is deposited in
the zoological collection of the museum in the
Natural History Museum in Pavia, under voucher
number CR0373 (Figure 1).
Figure 1. A potentially albinotic individual of Natrix tessellata found in Pavia in 1879 and deposited in the Natural
History Museum in Pavia, Italy (voucher no. CR0373).
The rst record of albinism in N. tessellata
from Slovakia reported here is important.
Although albinism occurs in all vertebrates, it is
rare in wild populations, especially in adults
(Ferri and Bettiga 1992). The condition is a
genetic anomaly caused by lack of activity of the
enzyme tyrosinase, which is responsible for
formation of melanin (Creel et al. 1974),
resulting in the absence of melanin in the skin,
the iris, and the choroid (Spadola and Di Toro
2007, Krecsák 2008). Estimates of the occurrence
of albinism in the wild vary from 1:10,000 to
1:30,000 (Bechtel 1995).
Materials and Methods
On 16 July 2018 at about 18:00 h, an
anonymous person informed MO of a clutch of
eggs of Natrix tessellata from Šaca, Slovakia
(48°3838.4 N, 21°0946.8 E; 252 m a.s.l.),
where the species is known to occur (Lác and
Lechovič 1964). The clutch of 18 eggs was
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Phyllomedusa - 19(2), December 2020
PROOFS
Albinism in Natrix tessellata
between wooden boards to be used for
construction. Three mold-infested, unfertilized
eggs were removed from the clutch, and the rest
of the eggs were placed in an incubator. During
incubation (moist vermiculite; 26°C; 60–70%
humidity), two eggs started to rot and were
removed on 20 and 23 July 2018. On 11 August
2018, 13 hatchlings, eight normally colored and
ve albinos, hatched after 26 days inside the
incubator. The incubation period for N. tessellata
eggs for Central Europe is 41–72 days (Velenský
et al. 2011). All individuals are kept in plastic
boxes with pine bark. Each box also contains a
large water bowl, a shelter, and a branch of
appropriate size. Photoperiod and heating are
provided by heat lamps with temperatures
reaching up to 28°C in a basking spot and room
temperature in other parts of the enclosure.
Individuals are fed separately every 7–10 days
on aquarium sh provided by local breeders. The
eggs were collected and maintained in captivity
under permit number 10783/2018-6.3 from the
Ministry of Environment of the Slovak
RepublicDirectorate for Nature, Biodiversity
and Landscape Protection. Blood samples were
taken from all individuals and each has its
voucher number (DJ8522–8534), deposited in
the collection of the Department of Zoology,
Comenius University in Bratislava.
Morphometric and meristic data for all
snakes were recorded 1 wk after the snakes
hatched. The following measurements were
taken by SP with a digital caliper to the nearest
0.1 mm: head length (HL), head width (HW),
mouth length (ML). Snout–vent length (SVL),
tail length (TL) and total length (TotL = SVL +
TL) were measured using a tailor´s tape measure.
The following meristic characters were re-
corded: preocular (PREOC), postocular (POSTOC),
supralabial (SUPL), sublabial (SUBL), ventral
(VENT), subcaudal scales (SUBC) and dorsal
scale row (DORS), following the methods of
Moravec (2015). We also documented possible
anomalies in scalation. All individuals were
photographed 30 days after hatching from the
dorsal and ventral sides and close up photographs
of the head from upper, bottom and lateral side
were taken. Detailed photos of ve albino
individuals are presented in Appendix I. Six
individuals [two albinotic (DJ8524, DJ8526) and
four normally colored (DJ8530–8532, DJ8534)],
died independently within 5 mo after hatching.
One year after hatching, the remaining living
individuals were measured (Table 1). We
compared all metric and meristic characters with
results of Laňka (1973) and Opoldusová (2008)
and with our own data for N. tessellata from
Slovakia. At the time of this writing (April
2020), three albinotic and four normal individuals
are being kept in captivity.
To compare rarity of albinism in other
European species of snakes, we reviewed and
summarized published and unpublished (obser-
vations from eld herpetologists supported by a
photo; Appendix II) data about albinotic snakes
(Table 2).
Results
Albinotic individuals from Šaca, Slovakia,
have unpigmented, pinkish skin, and reddish
eyes lacking pigmentation (Figure 2; Appendix
I). Darker pinkish spots are present on cephalic
scales, mainly on the parietal, frontal and
supraocular scales. The inverted V-pattern
behind the head is not as visible as it is in
normally colored individuals, but darker spots
occur on a few scales in that region. There is a
ventral pattern of alternating yellowish and
pinkish spots in each albino snake (Figure 2).
At hatching, all juvenile N. tessellata—both
albinotic and normally colored—had relatively
similar SVL and head measurements (HL, HW,
and ML), but TL differed sexually. Mean SVL
of newly hatched juveniles was 23.27 cm (range
21.40–24.00; SD ± 0.63). Similarly, mean TL
was 6.16 cm (range 5.40–6.80; SD ± 0.46). Of
the13 hatchlings, seven were males and six
females; a total of ve was albinotic—four males
and one female. All metric and meristic data are
summarized in Table 1. There were no anomalies
in the numbers of PREOC and POSTOC scales.
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Phyllomedusa - 19(2), December 2020
Table 1. Basic metric (cm) and meristic characteristics recorded from all hatchling Natrix tessellata from one clutch. Metric data from one-year-old snakes
shown in italics. SVL = snout–vent length; TL = tail length; TotL = total length; HL = head length; HW = head width; ML = mouth length; PREOC =
preocular; POSTOC = postocular; SUPL = supralabial; SUBL = sublabial; VENT ventral = SUBC = subcaudal scales; DORS = dorsal scale row.
No. Sex SVL TL TotL HLHWMLPREOC POSTOC SUPL SUBL VENT SUBC DORS Ventral coloration
8522 M 23.2
28.1
6.4
7.8
29.6
35.9
1.3
1.4
0.6
0.7
1.0
1.1
2/2 3/3 7/7 8/8 174 71 19 many yellow spots on pinkish base
8523 F 23.3
31.3
5.7
8.1
29.0
39.4
1.4
1.7
0.6
0.7
1.0
1.2
2/2 3/3 8/9 9 + 1/9 168 60 19 As above
8524 M 24.0 6.3 30.3 1.4 0.6 1.0 2/2 3/3 8/8 8/8 175 72 19 few yellow spots on pinkish base
8525 M 23.1
29.1
6.2
8.2
29.3
37.3
1.3
1.4
0.6
0.7
1.0
1.1
3/2 3/3 8/8 9/8 178 72 19 many white-yellow spots on
pinkish base
8526 M 23.9 6.5 30.4 1.3 0.6 0.9 2/2 3/3 8/8 9/8 176 69 19 white-yellow spots on pinkish
base
8527 F 23.3
27.4
5.7
7.2
29.0
34.6
1.3
1.5
0.6
0.7
1.0
1.1
2/2 3/3 8/7 9/8 168 + 3 61 19 White-yellow spots on brown base
8528 F 23.3
28.3
5.4
6.7
28.7
35.0
1.3
1.4
0.6
0.6
1.0
1.0
2/2 3/3 8/8 9/8 170 60 19 white spots on brown base
8529 M 23.4
32.0
6.8
9.2
30.2
41.2
1.2
1.5
0.6
0.7
1.0
1.1
2/2 3/4 8/7 8/8 175 69 19 white-yellow spots on brown base
8530 M 23.3 6.5 29.8 1.3 0.6 0.9 2/2 3/3 7/7 8 + 1/9 176 68 19 As above
8531 M 23.2 6.4 29.6 1.2 0.6 1.0 2/2 3/3 7/7 8/8 174 + 2 70 19 As above
8532 F 21.4 5.4 26.8 1.2 0.6 1.0 2/2 3/4 6/7 8/9 169 + 4 58 19 yellow spots on brown base
8533 F 23.7
32.4
6.3
8.6
30.0
41
1.3
1.6
0.6
0.8
1.0
1.3
2/2 3/3 8/7 8/9 171 + 3 62 19 white-yellow spots on brown base
8534 F 23.4 6.5 29.9 1.2 0.5 0.9 2/2 3/3 8/8 8/8 178 71 19 As above
Papezikova et al.
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Phyllomedusa - 19(2), December 2020
PROOFS
Table 2. List of published and unpublished data recording albinotic species of snakes in Europe; *true albinism not
verified. Unpublished observations (in litt. or pers. comm.) are supplemented by photos and presented in
Appendix II.
Species NCountry References
Coronella austriaca 1Austria Happ 1994
2Czech Republic Rehák 1992, B. Trapp (in litt.)
1 Italy Pirotta 1879
1 Netherlands Lenders 2008
1 Slovakia D. Revaj (pers. comm.)
Coronella girondica 1france Geniez and Grillet 1989
1 Spain Martínez-Silvestre et al. 2009
Dolichophis jugularis 1Cyprus Baier et al. 2013
Elaphe sauromates 2Bulgaria Petzold 1975, Jablonski et al. 2019
Hierophis viridiflavus 1Italy Scali 1992
Malpolon monspessulanus 1Spain martínez-Silvestre and Soler 2018
Natrix helvetica 2france Baudin 2003, Varanguin 2012
1 U.K. Boulenger 1913
Natrix maura 5Spain Pérez and Collado 1975, Herrador and Pulido
2006, Alaminos and López 2011, L. Gonzáles
García (in litt.), E.R. Ara (in litt.)
Natrix natrix 1Austria Sackl and Putz 2002
1 Czech Republic Musilová et al. 2006
1 Germany M. Bollhorn (in litt.)
1 Poland T. Krajča (pers. comm.)
Natrix tessellata* 1Italy Pirotta 1879
Natrix tessellata 5Slovakia This study
Vipera ammodytes 1Italy Krecsák 2008
Vipera aspis 3france Bruno 1985, Naulleau 1997, Guiller 2007
Vipera berus 1Bulgaria Stojanov 2014
2 Finland Vainio 1931, Krecsák 2008
1 Germany Buchner 1917
2 Sweden Edelstam 1971, Krecsák 2008
1 Slovakia Gezova et al. 2018
4 U.K. Leighton 1901, Harris 1936, Krecsák 2008
Zamenis longissimus 3Austria Erber 1879, Sochurek 1955, Esterbauer 2014
1 Bosnia & Herzegovina Ćurić 2019
1 Italy Ferri and Bettiga 1992
1 Serbia Radovanović 1941
8 Slovakia Balthasar 1935, Gabzdil 2003, Musilová et al.
2006, Gezova et al. 2018, S. Kl’účiková-Píšová (in
litt.), D. Revaj (pers. comm.), L’ . Magyariová and
Š. Bánovský (in litt.)
1 Slovenia Krofel 2004
1 Switzerland Bruno and Maugeri 1990
Zamenis scalaris 4Spain Rollinat 1934, Lesparre 2001, Manjón 2011, D.
Lerena and R.C. Zárate (in litt.)
Albinism in Natrix tessellata
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Phyllomedusa - 19(2), December 2020
Papezikova et al.
Figure 2. Comparison of normally colored and albinotic
hatchlings of Natrix tessellata from Šaca,
Košice, Slovakia: frontal (A), dorsal (B), and
ventral (C) views.
A
B
C
However, the following anomalies in scalation
were observed in 11 of the 13 individuals: fused
SUPL in DJ8522; fused SUBL in DJ8533;
inserted SUBL in DJ8523 and DJ8530; fused
SUBC in DJ8522–8524, DJ8526, DJ8529, and
DJ8531; inserted VENT in DJ8527 and DJ8531–
8533; and split VENT in DJ8528 (numbers listed
in Table 1).
We found records of a total of 65 truly
albinotic snakes representing four families and
eight genera in Europe (Table 2); this total
includes the ve juveniles from Šaca, Slovakia,
as a new record for Europe. The total excludes
the dubious record of N. tessellata (CR0373)
from Pavia, Italy, as well as the albinotic Israelic
snake (Werner 2016). Among the albinotic
snakes recorded in Europe, the genus Zamenis
contains the most albinos (20 individuals,
representing ~ 33% of the total; the ve
individuals from Šaca were excluded from this
calculation because they were found as eggs and
hatched in captivity), which were found in eight
countries. Only one albino snake is recorded for
each of the genera Dolichophis (Cyprus),
Hierophis (Italy), and Malpolon (Spain). Spain
has the greatest number of albinotic snakes; a
total of 11 individuals of four species is known—
Coronella girondica (Daudin, 1803), Malpolon
monspessulanus (Hermann, 1804), Natrix maura
(Linnaeus, 1758), and Zamenis scalaris (Schinz,
1822). Each of the following countries has only
one record of an albino snake: the Netherlands,
Bosnia and Herzegovina, Cyprus, Poland, Serbia,
Slovenia, and Switzerland. In the genus Natrix,
albino individuals occur in almost all species
[viz., N. natrix (Linnaeus, 1758), N. helvetica
(Lacépède, 1789), N. maura, and N. tessellata]
with the exception of N. astreptophora (Seoane,
1885). Four albino N. natrix were found in each
of four countries (Austria, Czech Republic,
Germany, and Poland), three N. helvetica in two
countries (France and the United Kingdom), and
ve N. maura in one country (Spain; Table 2).
Six truly albinotic N. tessellata individuals occur
in two countries—one in Israel and ve described
here from Slovakia (excluding the dubious
record from Italy).
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Phyllomedusa - 19(2), December 2020
PROOFS
Discussion
Albinism in snakes is considered to be a rare,
autosomal recessive mutation with an expected
ratio of normally colored to albinotics of 3:1 if
mating two heterozygotes (Clay 1935, Bechtel
and Bechtel 1985). When mating heterozygotes
and homozygotes, the probability of albinotic
juveniles is approximately 50% (Bechtel and
Bechtel 1985). When two homozygotes mate
then 100% of offspring will be of the albino
phenotype. However, without information on the
coloration of unhatched N. tessellata, we can
only estimate the genotype of the parents; most
likely one was a heterozygote and the other a
recessive homozygote. The frequency of
recessive alleles is greater in small, fragmented
populations (Laikre 1999) and that could be the
case in this study. The population in eastern
Slovakia is at the northern edge of the range of
the species (Gezova and Jablonski 2018) and one
might assume that populations occurring near
the range limits have lower densities and
effective population sizes (Vucetich and Waite
2003). The occurrence and survival of albinotic
individuals also may be related to abiotic
environmental features such as elevation and
temperature (Kehas et al. 2005). Moreover,
environmental pollution (Kolenda et al. 2017)
that may occur in an urban area, such as the one
where the egg clutch was found, may be
correlated abnormal scutelation in reptiles, but
the relationship has not been well studied
(Mulder 1995, Cruz-da-Silva et al. 2018 and
literature therein). However, anomalous scalation
in N. tessellata is not unusual in central Europe
(e.g., Laňka 1978, Rehák 1989, Baruš et al.
1992).
Abnormally colored species of snakes may
be subject to higher predation pressure by
visually oriented predators, and thus, be
negatively affected by the lack of pigmentation
because they are more easily visible. In addition,
reproductive tness of albino snakes is reduced
(Krecsák 2008, McCardle 2012). The lack of
pigment in the eyes adversely affects vision;
thus, it is more difcult for albino snakes to nd
suitable prey, avoid danger, and perceive visual
signals during mating season (Miller 2005,
Krecsák 2008). These facts may partially account
for the fact that more albino juveniles were
encountered in the wild than adults (e.g.,
Alaminos and López 2011, Gezova et al. 2018,
Martínez-Silvestre and Soler 2018). Nevertheless,
albinotic adults of several genera of European
snakes, including the genus Natrix, have been
observed in the wild (e.g., Sackl and Putz 2002,
Krecsák 2008, Alaminos and López 2011, Bruni
2017, Jablonski et al. 2019). Krecsák (2008)
posits that there are more aberrant European
Viperinae snakes in northern regions than in
southern regions; however, we observed the
opposite in our review in which the most albinos
occurred in central Europe and the Iberian
Peninsula with the greatest number of albinos
recorded in the genera Zamenis, Vipera, and
Natrix. We suggest that there is no clear pattern
in albinism in European snakes and that albinotic
individuals seem to be distributed randomly in
the natural populations. However, ecological,
and environmental factors need to be investigated
more thoroughly.
Acknowledgments
We thank Edoardo Razzetti for providing
assistance and information about the specimen
deposited in the Natural History Museum in
Pavia and Alessandra Pandol for providing
photos of this snake. We also thank E. R. Ara, Š.
Bánovský, M. Bollhorn, L. Gonzáles García, D.
Jandzík, S. Kľúčiková-Píšová, T. Krajča, D.
Lerena, M. Lukanová, Ľ. Magyariová, D. Revaj,
B. Trapp, and R. C. Zárate for notes and photos
of albinotic snake species recorded in Europe.
The Ministry of Environment of Slovak
Republic, Directorate for Nature Biodiversity
and Landscape Protection granted permission to
keep individuals from Šaca. We are also grateful
to L. Trueb and R. Morgan for English
corrections, and associate editor Ross D.
MacCulloch and two anonymous reviewers for
Albinism in Natrix tessellata
172
Phyllomedusa - 19(2), December 2020
comments which improved the rst version of
the manuscript. This work was supported by the
Slovak Research and Development agency,
contracts no. APVV-15-0147 and APVV-19-
0076.
References
Alaminos, E. A. and J. J. L. López. 2011. Un caso de
albinismo en Natrix maura en el sur de la Península
Ibérica. Boletín de la Asociación Herpetológica
Española 22: 8182.
Baier, F., D. J. Sparrow, and H. J. Wiedl (eds.). 2013. The
Amphibians and Reptiles of Cyprus. Frankfurt am Main.
Edition Chimaira. 362 pp.
Balthasar, V. 1935. Několik pozurohodných objektů
herpetologické sbírky Slovenského vlastivědného muzea
v Bratislavě. Vědy přírodní 16: 67–68.
Baruš, V., M. Kminiak, B. Král, O. Oliva, E. Opatrný, I.
Rehák, P. Roth, Z. Špinar, and L. Vojtková (eds.). 1992.
Plazi - Reptilia. Praha. Fauna ČSFR 26, Academia. 224
pp.
Baudin, B. 2003 Observation en Mayenne d’une couleuvre à
collier albinos (Natrix natrix helvetica). Biotopes
21: 39–40.
Bechtel, H. B. (ed.). 1995. Reptile and Amphibian
Variants: Colors, Patterns and Scales. Malabar. Krieger
Publishing Company. 206 pp.
Bechtel, H. B. and E. Bechtel. 1985. Genetics of color
mutations in the snake, Elaphe obsoleta. Journal of
Heredity 76: 7–11.
Boulenger, G. A. (ed.). 1913. The Snakes of Europe. London.
Methusen & Co. Ltd. 350 pp.
Bruni, G. 2017. A leucistic grass snake Natrix natrix
(Linnaeus, 1758) (Serpentes: Natricidae) from Tuscany,
Central Italy. Herpetology Notes 10: 313–316.
Bruno, S. (ed.). 1985. Le Vipere d´Italia e d´Europa.
Bologna. Edagricole. 270 pp.
Bruno, S. and S. Maugeri (eds.). 1990. Serpenti d’Italia e
d’Europa. Milano. Giorgio Mondadori Editore. 207 pp.
Buchner, O. 1917. Über besonders merkvürdige
Färbungsvarietäten der Kreuzotter nebst ergänzenden
Mitteilungen über das Vorkommen und die Verbreitung
derselben Würtemberg, sowie über das Naturell der
Giftschlangen. Jahreshefte des Vereins für
Vaterländische Naturkunde in Württemberg 1917: 10–
22.
Papezikova et al.
Clay, W. 1935. The Occurrence of albinos in a brood of the
Common Water Snake, Natrix sipedon sipedon (L.).
Copeia 1935: 115–118.
Conelli, A. E., M. Nembrini, and K. Mebert. 2011. Different
habitat use of Dice Snakes, Natrix tessellata, among
three populations in Canton Ticino, Switzerland. A
radiotelemetry study. Mertensiella 18: 100–116.
Creel, D., C. J. Witkop, and R. A. King. 1974. Asymmetric
visually evoked potentials in human albinos: evidence
for visual system anomalies. Investigaitive Ophthalmology
13: 430–440.
Cruz-da-Silva, R. C., M. A. de Freitas, and A. D. Abegg.
2018. A remarkable specimen of the genus Anilius
(Serpentes: Aniliidae): rare colour aberration or a new
species? Herpetology Notes 11: 161–165.
Ćurić, A. 2019. Albinism of Aesculapian snake Zamenis
longissimus (Laurenti, 1768) in situ: rst record for
Bosnia and Herzegovina. Natura Sloveniae 21: 31–33.
Edelstam, C. 1971. White adders. Animals: The International
Wildlife Magazin 13: 896–897.
Erber, J. 1879. Einen Albino der Aesculapnatter (Elaphis
aesculapii). Verhandlungen der Zoologisch-Botanischen
Gesellschaft in Wien 29: 39–40.
Esterbauer, H. 2014. Die Äskulapnatter, Zamenis longissimus
(Laurenti, 1768). Erstnachweis einer amelanistischen
Farbmutation in Österreich. Ein Porträt der Äskulapnatter
in Verbindung mit dem Erstnachweis einer „weißen“
Farbvariante in Österreich liefert der Reptilienfachmann.
ÖKO·L 36: 711.
Ferri, V. and M. Bettiga. 1992. Un caso di albinismo nel
Colubro di Esculapio, Elaphe l. longissima (Laurenti,
1768). Il Naturalista Valtellinese. Atti del Museo Civico
di Storia Naturale di Morbegno 3: 91–96.
Frotzler, N., N. Davitashvili, and K. Mebert. 2011.
Distribution of the Dice Snake (Natrix tessellata) in
Georgia (Transcaucasia) and comparative notes on the
genus Natrix. Mertensiella 18: 357364.
Gabzdil, R. 2003. Svetový unikát na výstave. Extra Zemplín,
Nezávislý týždenník občanov okresov Michalovce,
Trebišov a Sobrance 10: 2.
Geniez, P. and P. Grillet (eds.). 1989. Les Couleuvres et Les
Viperes. Lausanne. Editions Payot. 64 pp.
Gezova, S. and D. Jablonski. 2018. Range extension and
highest elevational populations of Natrix tessellata
in Slovakia. Amphibian and Reptile Conservation 12:
98– 105.
Gezova, S., P. Drugac, A. Purkart, and D. Jablonski. 2018.
Albinism in two snake species recorded from Slovakia.
Russian Journal of Herpetology 25: 79–82.
173
Phyllomedusa - 19(2), December 2020
PROOFS
Gruschwitz, M., S. Lenz, K. Mebert, and V. Laňka. 1999.
Natrix tessellata (Laurenti, 1768) – Wurfelnatter. Pp.
581–644 in W. Böhme (ed.), Handbuch der Reptilien
und Amphibien Europas. Band 3/IIA: Schlangen II.
Wiesbaden. AULA-Verlag.
Guicking, D., U. Joger, and M. Wink. 2009. Cryptic diversity
in a Eurasian water snake (Natrix tessellata,
Serpentes: Colubridae): evidence from mitochondrial
sequence data and nuclear ISSR PCR ngerprinting.
Organisms, Diversity and Evolution 9: 201–214.
Guiller, G. 2007. Un spécimen albinos de Vipera aspis
(Linnaeus, 1758) découvert dans l´Ouest de la France.
Bulletin de la Société des Sciences naturelles de l´Ouest
de la France 29: 1–6.
Happ, F. 1994. Fund einer Albino-Schlingnatter (Coronella
austriaca austriaca Laurenti, 1768) auf dem
Magdalensberg in Kärnten. Carinthia II 184: 123–129.
Harris, G. T. (ed.). 1936. Albino adder. Axminster. Report
and Transactions of the Devonshire Association for the
Advancement of Science, Literature and Art. 134 pp.
Herrador, F. C. and L. P. Pulido. 2006. Albinismo e
hipomelanismo en Culebra viperina. Butlletí de la
Societat Catalana d’Herpetologia 17: 53–55.
In den Bosch, H., W. Bischoff, and J. F. Schmidtler. 1998.
Bemerkenswerte Reptilienfunde im Libanon.
Herpetofauna 20: 19–32.
Jablonski, D., J. Jankov, K. Bedev, and N. Natchev. 2019.
Albinism in Elaphe sauromates. Herpetological Bulletin
149: 46.
Kehas, A. J., K. Theoharides, and J. Gilbert. 2005. Effect of
sunlight intensity and albinism on the covering response
of the Caribbean Sea urchin Tripneustes ventricosus.
Marine Biology 146: 11111117.
Krecsák, L. 2008. Albinism and leucism among European
Viperinae: a review. Russian Journal of Herpetology
15: 97–102.
Kolenda, K., B. Najbar, A. Najbar, P. Kaczmarek, M.
Kaczmarski, and T. Skawiński. 2017. Rare colour
aberrations and anomalies of amphibians and reptiles
recorded in Poland. Herpetology Notes 10: 103109.
Krofel, M. 2004. First record of albino Aesculapian Snake
(Elaphe longissima) in Slovenia. Natura Sloveniae
6: 53–56.
Lác, J. and A. Lechovič. 1964. Historický prehľad výskumu
plazov na území Slovenska do roku 1963. Acta Rerum
Naturalium Musei Nationalis Slovaci 10: 124–154.
Laikre, L. 1999. Hereditery defects and conservation genetic
management of captive populations. Zoo Biology
18: 81–99.
Laňka, V. 1973. Variabilita a biologie užovky podplamaté,
Natrix tessellata Laurenti, 1768. Unpublished M.Sc.
Dissertation. Charles University, Praha, Czech Republic.
Laňka, V. 1978. Variabilität und Biologie der Würfelnatter
(Natrix tessellata). Acta Universitatis Carolinae
Biologica 1975-1976: 167–207.
Leighton, G. R. (ed.). 1901. The Life History of British
Serpents and Their Local Distribution in the British
Isles. Edinburgh and London. William Blackwood and
Sons. 448 pp.
Lenders, A. J. W. 2008. Opnieuw een albino Gladde slang in
de Meinweg. Natuurhistorisch Maandblad 97: 139.
Lesparre, D. 2001. Un caso de albinismo en culebra de
escalera (Elaphe scalaris). Boletín de la Asociación
Herpetologica Espańola 12: 1718.
Manjón, N. 2011. Caso de albinismo total en Rhinechis
scalaris. Boletín de la Asociación Herpetológica
Española 22: 7778.
Martínez-Silvestre, A. and J. Soler. 2018. Caso de albinismo
en Malpolon monspessulanus (Hermann, 1804). Boletín
de la Asociación Herpetológica Española 29: 31–33.
Martínez-Silvestre, A., J. Soler, J. M. Ş. Gener, M. García,
and C. Martí. 2009. Albinismo total de Coronella
girondica en la Península Ibérica. Boletín de la
Asociación Herpetológica Española 20: 44–45.
McCardle, H. 2012. Albinism in wild vertebrates.
Unpublished M.Sc. Dissertation. University of San
Marcos, Texas, USA.
Mebert, K. 2011. Geographic variation of morphological
characters in the Dice Snake (Natrix tessellata).
Mertensiella 18: 11–19.
Miller, J. D. 2005. All about albinism. Missouri
Conservationist 66: 4–7.
Moravec, J. 2015. Natrix tessellata (Laurenti, 1768) - užovka
podplamatá. Pp. 364–395 in J. Moravec (ed.), Fauna
ČR. Plazi - Reptilia. Praha. Academia.
Mulder, J. 1995. Congenital anomalies in morphology and
colour in captive-bred Vipers (Reptilia, Serpentes,
Viperidae). Deinsea 2: 41–50.
Musilová, R., V. Zavadil, and P. Kotlík. 2006. Albinismus
užovky obojkové. Živa 5: 228–229.
Naulleau, G. (ed.). 1997. La Vipére Aspic. Saint Yrieix. Éveil
Nature. 72 pp.
Opoldusová, Z. 2008. Sexuálny dimorzmus Natrix tessellata
(Colubridae, Reptilia). Unpublished M.Sc. Dissertation.
Comenius University, Bratislava, Slovakia.
Albinism in Natrix tessellata
174
Phyllomedusa - 19(2), December 2020
Pérez, M. and E. Collado. 1975. Hallazgo de Natrix maura
albina. Acta Vertebrata 2: 271–272.
Petzold, H. G. 1975. Eine albinotische Vierstreifennatter,
Elaphe quatuorlineata sauromates, aus Bulgarien.
Salamandra 11: 113–118.
Pirotta, R. 1879. Di alcuni casi di albinismo nei Rettili. Atti
della Societa Italiana di Scienze Naturali 21: 1–4.
Radovanović, M. 1941. Zur Kenntnis der Herpetofauna des
Balkans. Zoologischer Anzeiger 136: 145–159.
Rehák, I. 1989. Revize fauny hadů Československa.
Unpublished Ph.D Thesis. Charles University, Prague,
Czech Republic.
Rehák, I. 1992. Coronella austriaca Laurenti, 1768 - Užovka
hladká. Pp. 134–140 in V. Baruš, O. Oliva, M. Kminiak,
B. Král, E. Opatrný, I. Rehák, P. Roth, Z. Špinar, and L.
Vojtková (eds.), Fauna ČSFR. sv. 26. Plazi - Reptilia.
Praha. Academia.
Rollinat, R (ed.). 1934. La Vie des Reptiles de la France
Centrale. Paris. Delegrave. 343 pp.
Sackl, P. and J. Putz. 2002. Eine albinotische Ringelnatter,
Natrix natrix (L.), im steirischen Ennstal, Österreich
(Reptilia, Squamata, Colubridae). Joannea Zoologie
4: 11–13.
Scali, S. 1992. Caso di colorazione anomala nel Biacco
(Coluber viridiavus Lacepede, 1789). Atti della Società
Italiana di Scienze Naturali e del Museo Civico di Storia
Naturale di Milano 133: 294–295.
Sochurek, E. 1955. Die Äskulapnatter Elaphe l. longissima
Laurentus 1768 - in Niderösterreich. Unsere Heimat
26: 180–182.
Spadola, F. and F. Di Toro. 2007. Complete albinism in a
Podarcis muralis newborn. Acta Herpetologica 2: 49–
51.
Sterijovski, B., R. Ajtić, L. Tomović, S. Djordjević, M.
Djurakić, A. Golubović, J. Crnobrnja-Isailović, J. M.
Ballouard, D. Desmont, F. Groumpf, and X. Bonnet.
2011. Natrix tessellata on Golem Grad, FYR of
Macedonia: a natural fortress shelters a prosperous
snake population. Mertensiella 18: 298301.
Stojanov, A. J. 2014. First record of amelanism of Vipera
berus bosniensis Boettger, 1889, in Bulgaria. Herpetozoa
26: 180–182.
Storm, P. 2018. European water snakes and the competitive
exclusion principle. Litteratura Serpentium. Jaargang
38: 5987.
Tuniyev, B., S. Tuniyev, T. Kirschey, and K. Mebert. 2011.
Notes on the Dice Snake (Natrix tessellata) from the
Caucasian Isthmus. Mertensiella 18: 343–356.
Vainio, I. 1931. Zur verbreitung und biologie der Kreuzotter,
Vipera berus (L.) in Finnland. Annales Societatis
Zoologicæ Botanicæ Fennicæ Vanamo 12: 3–19.
Varanguin, N. 2012. Couleuvre à collier - Natrix natrix
(Linnaeus, 1758), Ouvrage. Atlas des Reptiles de
Bourgogne, Bourgogne Nature, Hors - Série 12: 257–272.
Velenský, M., P. Velenský, and K. Mebert. 2011. Ecology
and ethology of Dice Snakes (Natrix tessellata) in the
city district Troja, Prague. Mertensiella 18: 157–176.
Vucetich, J. A. and T. A. Waite. 2003. Spatial patterns of
demography and genetic processes across the species’
range: null hypotheses for landscape conservation
genetics. Conservation Genetics 4: 639–645.
Werner, Y. L. (ed.). 2016. Reptile Life in the Land of Israel
with Comments on Adjacent Regions. Frankfurt am
Main. Edition Chimaira. 494 pp.
Zaher, H., R. W. Murphy, J. C. Arredondo, R. Graboski, P.
R. Machado-Filho, K. Mahlow, G. G. Montingelli, A. B.
Quadros, N. L. Orlov, M. Wilkinson, Y-P. Zhang, and F.
G. Grazziotin. 2019. Large-scale molecular phylogeny,
morphology, divergence-time estimation, and the fossil
record of advanced caenophidian snakes (Squamata:
Serpentes). PLoS ONE 14: e0217959.
Editor: Ross D. MacCulloch
Papezikova et al.
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PROOFS
Appendix I. Albinotic individuals No. 8522–8526 from Šaca, Košice. Head in lateral (A, B), dorsal (C)
and ventral (D) views. Dorsal (E) and ventral (F) views of body. Numbers of individuals written
below correspond to the numbers listed in Table 1.
A
A A
C
C C
E
E E
B
B B
D
D D
F
F F
8522
8524 8525
A
C
E
B
D
F
8523
A
C
E
B
D
F
8526
Albinism in Natrix tessellata
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Phyllomedusa - 19(2), December 2020
Appendix II. Previously unpublished photographs of albinotic snakes from Europe. (A) Coronella austriaca, Czech Republic
(B. Trapp); (B) C. austriaca, Slovakia (D. Revaj); (C) Natrix maura, Spain (L. Gonzáles García); (D) N. maura, Spain
(E.R. Ara); (E) Natrix natrix, Germany (M. Bollhorn); (F) N. natrix, Poland (T. Krajča); (G) Zamenis longissimus,
Slovakia (S. Kľúčiková-Píšová); (H) Z. longissimus, Slovakia (Ľ. Magyariová and Š. Bánovský);
(I) Z. longissimus, Slovakia (D. Revaj); (J) Zamenis scalaris, Spain (D. Lerena and R.C. Zárate).
A
C
E
G
I
B
D
F
H
J
Papezikova et al.
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