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\begin{document}

\title{The First Record of Leucism in the Rhabdophis tigrinus (Boie, 1826)
(Squamata, Colubridae) in South Korea}



\author[1]{Seung-Min Park}%
\author[1]{Seung-Ju Cheon}%
\author[1]{Hye-Rin  Park}%
\author[2]{Na-Yeong Kim}%
\author[1]{Md Mizanur Rahman}%
\author[1]{Ha-Cheol Sung}%
\affil[1]{Chonnam National University}%
\affil[2]{Research Center for Endangered Species, National Institute of Ecology}%


\vspace{-1em}



  
  \date{May 26, 2024}


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\selectlanguage{english}
\begin{abstract}
Leucism, in which pigmentation is lost over part or the entire body of
an animal, has a range of possible genetic causes. Here, we report
leucism in an individual tiger keelback (Rhabdophis tigrinus) found on
Jeung Island, Shinan-gun, Jeollanam-do, South Korea, during a survey of
the distribution of reptiles in the area. The individual was observed
sunbathing in the bushes next to a pond. This individual exhibited
ecdysis, thus it considered that have normal feeding activity. Our
report represents the first observation of leucism in R. tigrinus, and
thus, further analysis is needed of this phenotype to more clearly
understand its impact on the species and its natural history.%
\end{abstract}%



\sloppy


\textbf{Nature notes}

\textbf{The First Record of Leucism in the \emph{Rhabdophis tigrinus}
(Boie, 1826) (Squamata, Colubridae) in South Korea}

Seung-Min Park\textsuperscript{1}, Seung-Ju Cheon\textsuperscript{1},
Hye-Rin Park\textsuperscript{1}, Na-Yeong Kim\textsuperscript{2}, Md
Mizanur Rahman\textsuperscript{3} and Ha-Cheol Sung\textsuperscript{3*}

\textsuperscript{1}Department of Biological Sciences\selectlanguage{ngerman}·Biotechnology,
Chonnam National University, Gwangju 61186, South Korea.

\textsuperscript{2}Research Center for Endangered Species, National
Institute of Ecology, Yeongyang 36531, South Korea.

\textsuperscript{3}Department of Biological Sciences, Chonnam National
University, Gwangju 61186, South Korea.

\textsuperscript{\textbf{*}} Corresponding author.

E-mail address:\emph{shcol2002@chonnam.ac.kr}

Abstract: Leucism, in which pigmentation is lost over part or the entire
body of an animal, has a range of possible genetic causes. Here, we
report leucism in an individual tiger keelback (\emph{Rhabdophis
tigrinus} ) found on Jeung Island, Shinan-gun, Jeollanam-do, South
Korea, during a survey of the distribution of reptiles in the area. The
individual was observed sunbathing in the bushes next to a pond. This
individual exhibited ecdysis, thus it considered that have normal
feeding activity. Our report represents the first observation of leucism
in \emph{R. tigrinus} , and thus, further analysis is needed of this
phenotype to more clearly understand its impact on the species and its
natural history.

Keywords: Tiger keelback; Abnormal color variation; Yellowish snake;
Normal eyes; Ecdysis.

INTRODUCTION

Abnormal color variation on parts or over the entire body of animals has
a variety of genetic causes (Ashaharraza and Lalremsangha, 2020). An
example of this abnormal coloring is leucism, which typically presents
as a partial loss of pigmentation (Lobo and Sreepada, 2016). It appears
similar to albinism, but albino individuals tend to have red eyes due to
a complete lack of pigmentation (Deshmukh et al., 2020), while
individuals with leucism have normal-colored eyes (Acevedo and Aguayo,
2008). Animals with abnormal color variation, such as those with
leucism, can be disadvantaged in nature in various ways to them
(Krecsák, 2008; Bruni, 2017). Because it may encounter an increased risk
of predation (Di Marzio and Rozent\selectlanguage{polish}ā\selectlanguage{english}ls, 2021), or can lead to potential
problems with thermoregulation and visual acuity (Krecs\selectlanguage{ngerman}ák, 2008; Bruni,
2017). Therefore, due to low survival rate, individuals with leucism are
difficult to observe in nature (Lobo and Sreepada, 2016).

The tiger keelback (\emph{Rhabdophis tigrinus} ; Boie, 1826) is a
species of snake found in Russia, Japan (Lee et al., 2011), and
throughout South Korea, including Jeju Island (Jang et al., 2016). This
snake is a venomous snake and has two venom glands, which are used for
digestion and defense (Huthchinson et al., 2007, Lee et al., 2011). The
morphological characteristic of this snake is green with red and black
spots on its neck and keeled on all over the scales (Lee et al., 2011).

Commonly, \emph{R. tigrinus} is easily found in nearby grasslands,
wetlands, and ponds (Lee et al., 2011). Nevertheless, herein, we report
an individual of \emph{R. tigrinus} with an abnormal color variation.
Additionally, we build on the research review, collect data on leucism
and albinism found in the species and genus.

MATERIALS AND METHODS

On October 10, 2022, we conducted a survey on the distribution of
reptiles in Jeung Island (Shinan-gun, Jeollanam-do, South Korea; Fig.
1). The region contains agricultural land, beaches, two-lane roads,
rivers, and a small pond. We observed reptile species while walking
slowly across the road. We observed 5 species of reptile:\emph{Scincella
vandenburghi} , \emph{Elaphe dione} , \emph{Oocatochus rufodorsatus} ,
\emph{R. tigrinus} , and \emph{Hierophis spinalis} . We observed four
\emph{R. tigrinus} individuals (including one that was dead), but one
had an abnormal color. The unusually colored individual was found near a
small pond (34.971606°N, 126.140892°E, elevation 6 m, Fig. 1). The
individual was sunbathing in the bushes next to the pond. We caught the
snake carefully, measured its body and tail length and after took photos
for identification, released it at the same location.

On online searches, we use Google scholar
(\emph{www.scholar.google.co.kr}) and use the keywords: \emph{Rhabdophis
tigrinus} , leucism, albinism, tiger keelback, abnormal color variation,
snake, Family Colubridae, Genus \emph{Rhabdophis} . Beside English,
consider the distribution of this species, online searches were
conducted in Japanese, Chinses, Russian and Korean.

RESULTS

The observed individual was yellowish overall with no green or black
color (Fig. 2A), its pupils were the same color as those of normal
individuals (Fig. 2B), and it had a pink tongue. Its body length was
39.5 cm, while its tail length was 9.5 cm, for a total of 49 cm.
Especially, we confirmed that the snake was during the process of
ecdysis (Fig. 2B). Based on its body pattern and morphological
characteristic, this abnormal individual was identified as \emph{R.
tigrinus} , while the characteristics of its abnormal color variation
(i.e., body, eyes, and tongue) suggested that it was leucistic (Lobo and
Sreepada, 2016; Urra et al., 2021). Another normal \emph{R.
tigrinus}individual observed in the same location was greenish overall,
with black spots across its entire body and a black tongue (Fig. 2C, D).

Online search results were classified only from Southeast Asia and
Middle East Asia. We found total 11 species of snake of leucism and
albinism and location were mostly India (Table 1). However, we no
reports of leucism and albinism with \emph{R. tigrinus} . On the other
hand, the same genus, we found that albinism of \emph{R. rhodomelas} and
leucism of \emph{R. plumbicolor} in Singapore and India.

DISCUSSION

\emph{R. tigrinus} is very common in South Korea and Japan (Lee et al.,
2011), but reports of leucism have been rare. We searched online to find
reported cases of albino and leucistic \emph{R. tigrinus} but were
unable to find any. We only found the same genus snakes in albinism and
leucism (\emph{R. rhodomelas} and \emph{R. plumbicolor} ). Especially,
most of the albinism and leucism result were from India thus, this
report has a significance as a very rare and important case as Chinese,
Japanese and South Korea. Therefore, this report is the first in all
distribution of this species. In addition, abnormal color individuals
are known to mainly occur in isolated environments (Krecsák, 2008;
Tsuchihashi et al., 2011), so reporting on abnormal individuals to need
to continue for population conservation.

Generally, the size of an adult \emph{R. tigrinus} is 60\selectlanguage{english}-100 cm (Lee et
al., 2011) thus, the observed individual was considered to not yet be
fully mature. In reptiles, feeding and digestion are influenced by body
temperature, and previous studies have suggested that individuals with a
bright body color due to a lack of pigment may have difficulty
regulating this (Kornilios, 2014), with dark colors more efficient in
terms of maintaining the body temperature (Gibon and Falls, 1979). For
this reason, leucistic or albino individuals may experience harmful
consequences for their survival and fitness due to the lack of
thermoregulatory efficiency and camouflage (Krecsak, 2008). However,
this individual seems like leading a normal activity.

Nevertheless, this individual appeared to be engaged in normal feeding
activity because it was undergoing ecdysis (King and Turmo, 1997). As in
this report, about the normal activity of individuals with leucism,
Krecsak (2008) argued that this was possibly due to partially hidden the
body as the trade-off thermoregulation. Furthermore, Bruni (2017)
suggested that they were mainly active around stagnant water with a
temperature higher than the surrounding temperature at night. In fact,
our observed individual was also found near a stagnant pond. However,
the implications of these rare phenotypes for the metabolism,
thermoregulation, and environmental fitness of affected individuals
remain largely unknown (Urra et al., 2021). Therefore, further studies
are needed to understand the impact of these abnormal phenotypes on the
species and their natural history.

\textbf{FUNDING INFORMATION}

This study was carried out with the support of NIE -Entrusted
Research-2022-56, 2022 National Distribution Survey of Endangered
Wildlife (6th Phase 1st Year).

\textbf{DATA AVAILABILITY STATEMENT}

We confirm that the Data Availability Statement is included in the
manuscript, and that access to all necessary data files is provided to
editors and reviewers.



\textbf{REFERENCES}

Acevedo, J., \& Aguayo, M. (2008). Leucistic South American sea lion in
Chile, with a review of anomalously color in otariids.~\emph{Revista de
Biologia marina y Oceanografia} ,~\emph{43} (2), 413-417.

Ashaharraza, K., \& Lalremsangha, H. (2020). A leucistic Checkered
Keelback, \emph{Fowlea piscator} (Serpentes: Natricidae), from Mizoram,
India.~\emph{Reptiles \& Amphibians} ,~\emph{27} (1), 42-43.

Bruni, G. (2017). A leucistic grass snake \emph{Natrix natrix}(Linnaeus,
1758)(Serpentes: Natricidae) from Tuscany, central
Italy.~\emph{Herpetology Notes} ,~\emph{10} , 313-316.

Deshmukh, R. V., Deshmukh, S. A., Badhekar, S. A., Rewatkar, J.,
Pachare, V. P., \& Kawale, S. B. (2020). First records of albinism or
leucism in six species of snakes from central India.~\emph{Reptiles \&
Amphibians} ,~\emph{26} (3), 174-179.

Di Marzio, A., \& Rozent\selectlanguage{polish}ā\selectlanguage{english}ls, R. (2021). First report of a leucistic
Common Adder, \emph{Vipera berus} (Linnaeus, 1758) in Latvia (Squamata:
Viperidae).~\emph{Herpetology Notes} ,~\emph{14} , 73-76.

Gibson, A. R., \& Falls, J. B. (1979). Thermal biology of the common
garter snake \emph{Thamnophis sirtalis} (L.). II. The effects of
melanism.~\emph{Oecologia} , 99-109.

Hutchinson, D. A., Mori, A., Savitzky, A. H., Burghardt, G. M., Wu, X.,
Meinwald, J., \& Schroeder, F. C. (2007). Dietary sequestration of
defensive steroids in nuchal glands of the Asian snake \emph{Rhabdophis
tigrinus} .~\emph{Proceedings of the National Academy of Sciences}
,~\emph{104} (7), 2265-2270.

Jang, H. J., Kim, D. I., \& Jang, M. H. (2016). Distribution of reptiles
in South Korea: based on the 3rd National Ecosystem Survey.~\emph{Korean
J. Herpetol} ,~\emph{7} , 30-35.

King, R. B., \& Turmo, J. R. (1997). The effects of ecdysis on feeding
frequency and behavior of the common garter snake (Thamnophis
sirtalis).~\emph{Journal of Herpetology} ,~\emph{31} (2), 310-312.

Krecs\selectlanguage{ngerman}ák, L. (2008). Albinism and leucism among European Viperinae: a
review.~\emph{Russian journal of Herpetology} ,~\emph{15} (2), 97-102.

Lee, J. H., Jang, H. J., \& Suh, J. H. (2011). Ecological guide book of
herpetofauna in Korea.~\emph{National Institute of Environmental
Research, Incheon, South Korea} . 197pp.

Lobo, J. V., \& Sreepada, K. S. (2016). First report of leucism in
Python \emph{molurus molurus} (Serpentes: Pythonidae) from Mangalore,
Karnataka, India.~\emph{Phyllomedusa: Journal of Herpetology}
,~\emph{15} (2), 199-200.

Urra, F. A., Zúñiga, A., Melero, N., Reyes, N., Herrera, Y.,
Miranda-Calle, A. B., \& Ortiz, J. C. (2021). Leucism and albinism in
the rear-fanged snakes \emph{Tachymenis chilensis chilensis} (Schlegel,
1837) and Tachymenis chilensis coronellina Werner, 1898 (Serpentes,
Dipsadidae).~\emph{Herpetozoa} ,~\emph{34} , 125-129.

Tsuchihashi, A., Tamate, H., \& Yokohata, Y. (2011). Frequent occurrence
of partial albinism in lesser Japanese moles (\emph{Mogera imaizumii} )
on Kinkazan Island, Miyagi Prefecture, northeastern Japan.~\emph{Mammal
study} ,~\emph{36} (3), 141-146.

Foenander, J., \& Charlton, T. (2023). First report of albinism in the
Blue-necked Keelback,(\emph{Rhabdophis rhodomelas} )(Boie 1827), from
Singapore.~\emph{Reptiles \& Amphibians} ,~\emph{30} (1), e20042-e20042.

Mukherjee, S., \& Mohan, R. (2021). Albinism and leucism in free-ranging
snakes rescued in Gujarat and Tamil Nadu, India.~\emph{Reptiles \&
Amphibians} ,~\emph{28} (3), 485-487.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image1/image1}

\end{center}
\end{figure}

FIG. 1. Location of the observed leucistic \emph{Rhabdophis
tigrinus}individual. A, Satellite view. The red circle indicates where
the individual was found, surrounded by agricultural land, a beach, a
two-lane road, a river, and a small pond. B, Foreground photo of A. The
white arrow indicates the point of found.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image2/image2}

\end{center}
\end{figure}

FIG. 2. Leucistic and normal \emph{Rhabdophis tigrinus} individuals
observed in the survey. A, Leucistic \emph{R. tigrinus} individual
showing an overall yellowish body color. B, Close-up of the head,
showing that the originally black spots appear pink and that the eye
color is normal. C, Normal \emph{R. tigrinus} individual exhibiting a
greenish overall body color. D, Close-up of the head, showing red and
black spots on the neck and a black tongue (The red coloring of the lips
appears to be the result of injury and scarring). Photos by Seung-Min
Park.\selectlanguage{english}
\begin{longtable}[]{@{}llllll@{}}
\toprule
\textbf{No.} & \textbf{Species} & \textbf{Type} & \textbf{Location} &
\textbf{Year} & \textbf{Reference}\tabularnewline
\midrule
\endhead
1 & \emph{Rhabdophis rhodomelas} & Albinism & Singapore & 2023 &
Foenander and Charlton, 2023\tabularnewline
2 & \emph{Rhabdophis plumbicolor} & Leucistic & India & 2014 & Deshmukh
et al., 2020\tabularnewline
3 & \emph{Fowlea piscator} & Leucistic; Albinism & India & 2019; 2017 &
Ashaharraza and Lalremsangha, 2020; Deshmukh et al., 2020\tabularnewline
4 & \emph{Python molurus molurus} & Leucistic & India & 2016 & Lobo and
Sreepada, 2016\tabularnewline
5 & \emph{Bungarus caeruleus} & Leucistic; Albinism & India & 2007,
2012, 2015, 2018; 2017 & Mukherjee and Mohan, 2021, Chaudhuri et al.,
2018; Deshmukh et al., 2020\tabularnewline
6 & \emph{Eryx conicus} & Albinism & India & 2017, 2019; 2018 &
Mukherjee and Mohan, 2021; Deshmukh et al., 2020\tabularnewline
7 & \emph{Naja naja} & Albinism & India & 2016, 2019 & Mukherjee and
Mohan, 2021\tabularnewline
8 & \emph{Lycodon aulicus} & Albinism; Leucistic & India & 2016; 2018 &
Mukherjee and Mohan, 2021; Deshmukh et al., 2020\tabularnewline
9 & \emph{Coelognathus helena} & Albinism & India & 2011 & Mukherjee and
Mohan, 2021\tabularnewline
10 & \emph{Ptyas mucosa} & Albinism & India & 2019 & Mukherjee and
Mohan, 2021\tabularnewline
11 & \emph{Oligodon arnensis} & Albinism & India & 2017 & Deshmukh et
al., 2020\tabularnewline
\bottomrule
\end{longtable}

Table 1. List of data recording albinism and leucistic snakes in
Southeast Asia and Middle East Asia.

\selectlanguage{english}
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