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Most conservation efforts are channeled toward highly endangered species. However, snake populations decline rapidly worldwide, and many species that are currently classified as not threatened (e.g. LC - least concern, IUCN Red List) may well rapidly fall into the threatened categories. Yet, common species attract little attention. The principle, that it is more efficient to prevent disasters than to cure effects, is not taken into account. Dice Snakes (Natrix tessellata) offer a typical example of this situation. This species is one of the most widespread and polymorphic snake of the planet. Very large populations occur in the Balkans. On Golem Grad Island (the single island of FYR of Macedonia), a remarkable population of Dice Snakes suffers from recent assaults. Thousands of snakes are killed every year in the nets set by poachers, notably gravid females, raising population viability concerns. Protecting Dice Snakes, other reptiles (e.g. tortoises, vipers, and lizards) and the whole eco-system of Golem Grad Island would require moderate efforts: application of official rules, summer attendance, delivery of official permits to local people (including fishermen), and controlling tourism. In this paper, we addressed a central issue: does illegal fishing represent a potential threat to Dice Snakes? Our data suggest that recent increase of illegal fishing correlates with population decline.
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Herpetological Conservation and Biology 9(3):468−474.
Submitted: 27 April 2014; Accepted: 1 September 2014; Published: 31 December 2014.
468
CONSERVATION THREATS TO DICE SNAKES (NATRIX TESSELLATA) IN
GOLEM GRAD ISLAND (FYR OF MACEDONIA)
BOGOLJUB STERIJOVSKI1, RASTKO AJTIĆ2, LJILJANA TOMOVIĆ3,4,6, AND XAVIER BONNET5
1Macedonian Ecological Society - herpetology group, Vladimir Nazor 10, 1000 Skopje, Macedonia
2Institute for Nature Conservation of Serbia, Dr Ivana Ribara 91, 11070 Belgrade, Serbia
3Institute of Zoology, Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia
4Institute for Biological Research “Siniša Stanković”, University of Belgrade, Bulevar Despota Stefana 142, 11000 Belgrade,
Serbia
5CEBC, UMR-7372, CNRS Université de La Rochelle, 79360, Villiers en Bois, France
6Corresponding author, e-mail: lili@bio.bg.ac.rs
Abstract.—Most conservation efforts are channeled toward highly endangered species. However, snake populations
decline rapidly worldwide, and many species that are currently classified as not threatened (e.g. LC - least concern, IUCN
Red List) may well rapidly fall into the threatened categories. Yet, common species attract little attention. The principle,
that it is more efficient to prevent disasters than to cure effects, is not taken into account. Dice Snakes (Natrix tessellata)
offer a typical example of this situation. This species is one of the most widespread and polymorphic snake of the planet.
Very large populations occur in the Balkans. On Golem Grad Island (the single island of FYR of Macedonia), a
remarkable population of Dice Snakes suffers from recent assaults. Thousands of snakes are killed every year in the nets
set by poachers, notably gravid females, raising population viability concerns. Protecting Dice Snakes, other reptiles (e.g.
tortoises, vipers, and lizards) and the whole eco-system of Golem Grad Island would require moderate efforts:
application of official rules, summer attendance, delivery of official permits to local people (including fishermen), and
controlling tourism. In this paper, we addressed a central issue: does illegal fishing represent a potential threat to Dice
Snakes? Our data suggest that recent increase of illegal fishing correlates with population decline.
Key Words.Balkan Peninsula; conservation; mortality; poaching; tourism
INTRODUCTION
A limited number of flagship organisms, essentially
vertebrates and notably birds and mammals, attract the
attention of media and attract most conservation efforts
(Clark and May 2002; Seddon et al. 2005; Ballouard et
al. 2011; McClenachan et al. 2012). Consequently,
regarding neglected taxa like snakes for instance, only
few highly endangered species benefited from practical
(sometimes successful) conservation programs (Daltry et
al. 2001; Kingsbury and Attum 2009; Read et al. 2011).
However, common species should not be neglected
under the obvious principle that it is more efficient to
prevent disasters rather than to cure their effects
(reviewed by Gaston and Fuller 2008). Overall,
although protecting healthy populations of common
species should be a priority, taxonomic bias for
endothermic vertebrates and for nearly extinct species
represents a discouraging challenge to mobilize
conservation efforts toward not-yet threatened animals.
This is especially true regarding unpopular organisms
such as snakes (Seigel and Mullin 2009). For instance,
millions of snakes are killed for disputable reasons (e.g.
luxury leather industry or recreational purposes;
Fitzgerald and Painter 2000; Brooks et al. 2010) without
triggering public concerns or substantial conservation
actions. Moreover, large populations of common snake
species represent important components in many
ecosystems (Beaupre and Douglas 2009).
Growing evidence suggests that an increasing number
of snake populations (maybe most) are declining
worldwide (Hibbitts et al. 2009; Santos and Llorente
2009; Reading et al. 2010; Godley and Moler 2013;
Goiran and Shine 2013). This negative trend mirrors the
worrying conservation status of reptiles, with more than
20% of the species being under imminent extinction risk
(Böhm et al. 2013), and more generally reflects the
failure of international conventions (e.g. Convention on
Biological Diversity, CBD) to slow down the erosion of
biodiversity (Moyle and Williams 1990; Perfecto et al.
1997). Thus, there is an urgent need to shift away from
a narrow conservation policy focused on few iconic or
nearly extinct species, and instead allocate important
conservation efforts towards common organisms.
In the current study, we identified serious threats to a
population of a common snake species: the amphibious
Dice Snake (Natrix tessellata). Dice Snakes are
distributed over a very large geographic area (Bannikow
et al. 1977; Gruschwitz et al. 1999). This species
exhibits considerable phenotypic variation; each
population displays unique morphological, behavioral,
and physiological characteristics (e. g. Mebert 2011;
Copyright © 2014. Bogoljub Sterijovski. All rights reserved.
Herpetological Conservation and Biology
469
Ajtić et al. 2013; Brischoux and Kornilev 2014).
Although extremely large populations have been
observed (e.g. Carlsson et al. 2011; Ajtić et al. 2013),
information regarding population status is anecdotal
(Luiselli et al. 2007; Ajtić et al. 2013).
We studied such a remarkable population in Golem
Grad Island, a small island of the Galičica National Park
of Macedonia (Former Yugoslavian Republic; FYR).
The absolute number of snakes per hectare is among the
highest documented: an estimated tens of thousands of
sedentary piscivorous snakes live on < 20 ha (Ajtić et al.
2013). Golem Grad Island is a strictly protected area,
tourism is severely restricted, and fire, hunting, and
fishing are prohibited. Unfortunately, field observations
(2007–2013) reveal a different situation: due to recent
inability of law enforcement (border police and rangers
of the National Park Galičica) to patrol the region, many
tourists visit the island freely, fires are regularly lighted,
and illegal hunting and fishing are very frequent
(Sterijovski et al. 2011). Lack of control is a potential
conservation threat for the island and populations, so we
report on the impact of fish poaching on snake
population and we list other threats. Although, huge
numbers of snakes live on the island, suggesting that
mortality caused by poachers is marginal or could be
tolerated, the population status of Dice Snakes is actually
fragile. Preliminary data suggest that the number of
snakes drowned in illegal nets is massive (Sterijovski et
al. 2011; Ajtić et al. 2013). Our goal was to determine if
Dice Snakes are declining on Golem Grad Island and if
they are, to identify the most likely cause of possible
decline. This represents the first steps to raise public
concern, to convince authorities, and hopefully to set up
practical, simple, and efficient long-term conservation
actions.
MATERIAL AND METHODS
We studied Dice Snakes on Golem Grad Island (GGI),
which is located in Prespa Lake (18 ha; N 40°52'; E
20°59') within the Galičica National Park in the Former
Yugoslav Republic (FYR) of Macedonia. It has been
classified as a strictly protected area in 1988. The fact
that it is situated near the tri-junction frontier of FYR of
Macedonia (1.2 km south-west from the island), Greece,
and Albania provides the opportunity for people (tourists
and poachers) from all three countries to access (mostly
illegally) the island.
The island of Golem Grad is recognized as an unique
ecosystem due to the abundance of numerous rare plant
and fungi species and a high density of reptile and bird
species (Melovski 1998). Vegetation has not been
managed for more than two centuries, resulting in a
climax forest where most of the trees, Juniperus excelsa,
are taller than 10 m. The lack of domestic and feral
mammals (e.g. cats, dogs, rats, goats) that can cause
major damage to the native fauna and European island
ecosystems (Loss et al. 2013) likely explains the marked
abundance of many species, notably predators belonging
to various taxa: centipedes, snakes, otters, and raptors
occur in large numbers for instance. The herpetofauna
of GGI is remarkable. This small island is inhabited by
dense populations of Dice Snakes, Nose-horned Vipers
(Vipera ammodytes), and Hermann’s Tortoises (Testudo
hermanni) that are of particular interest for behavioral
and ecological studies (Ajtić et al. 2013; Djordjević et al.
2013; Golubović et al. 2013; Arsovski et al. 2014).
From 2008 to 2013, we visited the study site each
spring and summer (except in 2013), and occasionally in
autumn (total 13 field trips). On average, the duration of
each field survey was of 10 d and 1–12 people
participated in each survey (Table 1). The total field
effort was of 875 person-days. Most snakes we used in
the analyses were captured and permanently marked
using the classical scale-clipping (plus superficial
burning) method (Ajtić et al. 2013). We palpated,
measured body size and mass, and carefully described
each snake (see Ajtić et al. 2013 for details). Processing
each snake required approximately 15 min. We assessed
the relationship between consecutive field trips and
snake searching success (number of snakes searched,
captured, and processed/day/people) using Spearman’s
Rank Correlation (α = 0.05).
We estimated the impact of illegal hunting on Dice
Snakes using the information provided by police
TABLE 1. Summary of the field effort (capture/mark/recapture
studies) to monitor reptiles on Golem Grad Island, in Prespa Lake
within the Galičica National Park in the Former Yugoslavian
Republic of Macedonia.
Year
Season
No. of
people
No.
of
days
Searching
effort
(person-
days)
2008 Spring 4 10 40
Summer 3 8 24
2009 Spring 6 16 96
Summer 7 15 105
2010 Spring 4 10 40
Summer 6 20 120
Fall 3 3 9
2011 Spring 8 12 96
Summer 12 22 264
2012 Spring 5 10 50
Summer 2 4 8
Fall 1 3 3
2013 Spring 4 5 20
Total 65 138 875

Sterijovski et al.—Threats to Dice Snakes in Macedonia.
470
officers, official reports of the State Inspectorate, as well
as using our own counting efforts. During a single
random survey performed at night in early August 2011,
police collected 50 illegal nets. They estimated that the
maximum number of nets set per night was close to this
value, and provided an estimate ranging between 30 and
40 nets per night. Each net measured 50 m long with 2.5
cm mesh. In each net, police found 10–30 dead snakes
(and many fish). They also estimated that the nets were
set around GGI every 2–3 nights on average, from mid
of June to the end of July. Two years later (22 May
2013), police collected 238 fishing nets: 10 nets were
directly taken from the water and were full of fish and
some nets contained 205 kg of fish (e.g. Cyrpinus
carpio, Barbus prespensis). On average, in each net, the
poachers collected 10–15 kg of Belvica (Alburnus
belvica) a relatively small endemic species. These data
enabled us to estimate the amount of fish collected
during the main Belvica fish-poaching period, which
coincides exactly with the main foraging season in Dice
Snakes (Ajtić et al. 2013).
To crudely estimate the impact of fish poaching on
dice snakes, we used various combinations of the main
parameters above, and calculated possible total numbers
of snakes killed per year. We set the range of variation
of the main parameters as follow: poaching season 15,
30 or 45 d; poaching frequency 1 d/week, 3 d/week, or
every 3 d; number of nets set per night 5, 10, 15, 20, 30
or 40 nets; number of snakes drowned per net 5, 10, 15
or 20. We used these settings to take into account
variations of the poaching pressure due to changing
weather conditions; for instance, likely poachers work in
large numbers only under very favorable conditions
(e.g., no wind).
RESULTS
We captured 6,921 Dice Snakes on GGI: 6,329
captures and 592 recaptures. We fully processed snakes
at capture and recapture (e.g. measurements, palpation,
color description). Although population size could not
be accurately estimated, the very high number of snakes
processed revealed that a very large population of snakes
inhabits GGI (Table 2).
Considering a main poaching period of 45 days (mid
of June - end of July), around 5,500 kg of Belvica fish
were taken from the waters surrounding GGI during the
main period of Belvica fish poaching. In June 2010, we
counted 49 Dice Snakes drowned in two nets set near the
shore from late afternoon until the next morning (Fig. 1).
We found 32 adult males and 17 adult females, including
nine gravid females in the nets. On average, each gravid
female carried nine well developed eggs.
Given our assumptions, we estimate that 2,440 ±
2,764 (SD) snakes are killed every year. However, the
range of incertitude is very wide, ranging from 54 to
18,000 snakes killed per year (95% confidence interval:
2,526–3,053). Approximately 18% of the drowned
snakes were gravid females. Thus we estimated that on
average 439 ± 498 of gravid females are killed each year
(range 10–3,240 females). Each female was carrying
nine eggs on average, which leads to an additional loss
of 3,954 ± 4,478 eggs per year (range 87–29,160).
Using the mean body mass of Dice Snakes (0.15 kg;
FIGURE 1. Dice Snakes (Natrix tessellata), both sexes and three color
morphs, found drowned in fishing net illegally set on the near shore of
Golem Grad Island, Prespa Lake, in the Former Yugoslavian Republic
of Macedonia in June 2010. (Photographed by Rastko Ajtić).
TABLE 2. Summary of captures and recaptures of Dice Snakes
(Natrix tessellata) on Golem Grad Island, Prespa Lake, in the
Former Yugoslavian Republic of Macedonia. Note that recaptures
included snakes recaptured both within (i.e., recently marked
snakes) and among session (snakes marked during previous
sessions).
Year
Season
No. of
snakes
Recaptures
% of recaptures
2008 Spring 361 1 0.28%
Summer 241 2 0.83%
2009 Spring 643 6 0.94%
Summer 519 23 4.43%
2010 Spring 764 29 4.98%
Summer 1,281 151 11.79%
Fall 41 2 4.88%
2011 Spring 684 66 9.78%
Summer 1,252 233 18.41%
2012 Spring 388 64 16.49%
Summer 18 2 6.06%
Fall 56 0 0.00%
2013 Spring 81 13 16.05%
Total 6,329 592
Herpetological Conservation and Biology
471
F
IGURE
2. Relationship between time (session number, n = 13 from
spring 2008 to spring 2013, see Table 1) and snake searching success.
In autumn, most potential field sessions were not conducted and are
indicated with grey circles on the X-axis. Note that one fall-session
with a very low field effort (i.e., snakes were not fully processed but
simply weighted and counted) was discarded (autumn 2012, grey
circle).
unpubl. data), we estimated that 366 ± 415 kg of snakes
are destroyed each year. We found a negative
correlation between searching success and successive
field trips (r
s
= -0.59, P < 0.05; Fig. 2).
D
ISCUSSION
At the beginning of the mark/recapture study, our
capacity to process snakes was the main limiting factor;
we could catch hundreds of snakes in a short period of
time (e.g., about 100 snakes for one person in a half an
hour search time). Considering broad field efforts, the
number of snakes that we captured, measured, and
marked increased rapidly over time: on average, we
collected about 1,100 snakes per year (ranging from
approximately 100 to 2,300). In summer 2011, however,
despite greater than twice the number of person days in
the field, we only caught about the same number of
snakes that we caught the year before. In fact, capturing
even 100 animals per day required a considerable search
effort. The total number of snakes processed reflected
searching success, and was less limited by our capacity
to process them.
Our results suggest that the impact of illegal fishing on
Dice Snakes around GGI is important. The high
variability of snakes drowned in the nets that we
estimated are not the best way to determine the effect of
poaching because this range corresponds to extreme
combinations of all four factors set at their minimal or
maximal levels during the whole poaching season.
Using averages provides more realistic values, and
indicates that thousands (about 2,500) of adult snakes
likely are drowned in the nets during summers of low
F
IGURE
3. Klepto-foraging between two Dice Snakes (Natrix
tessellata) at Golem Grad Island, Prespa Lake, in the Former
Yugoslavian Republic of Macedonia. One snake caught a Belvica
fish (top, larger grey snake) whereas a second snake (bottom, smaller
dice-pattern snake) attempts to steal the prey. (Photographed by
Xavier Bonnet).
Police attendance, and that thousands of eggs of snakes
are lost. Indeed, since 2011, poachers regularly deploy
an intensive network of nets to capture Belvica fish.
Golem Grad Island is easily accessible because the mean
distance from Albanian and Macedonian harbors to GGI
is 4.3 ± 0.7 km. Illegal fishing concentrates on the near
shore because Belvica shelter in the narrow area of
partly submerged boulders that surrounds GGI. Because
Dice Snakes from GGI feed predominately on Belvica
(Ajtić et al. 2013), the local concentration of Belvica
may well explain the high numbers of resident Dice
Snakes and certainly justifies the attractiveness of the
area for poachers. In addition, snakes holding a fish in
their mouth are frequently pursued by other snakes (Fig.
3); klepto-foraging is common in GGI and we found that
roughly 10% of the snakes use this strategy when
Belvica concentrate near the shore. We believe that fish
trapped in the nets represent appealing prey, explaining
the very high number of drowned individuals in the nets
primarily designed to catch Belvica.
Consequently, the impact of poaching on Belvica and
Dice Snakes is intensive, highly localized, and it
increased suddenly in 2011 due to logistical difficulties
faced by the Macedonian police to patrol the area. The
destruction of thousands of snakes every year represents
a serious threat to the population of the Dice Snakes.
The low number of recaptures relative to the total
number of individuals captured per season precluded
performing robust analyses to estimate population size.
The total number of snakes inhabiting GGI was
estimated to more than 10,000 individuals in 2008–2010
(Ajtić et al. 2013); therefore an estimated 24% (95%
confidence interval: 25–31%) of the population may
have been destroyed during the last years of heavy
poaching. This proportion might be lower considering
that it is likely that > 10,000 snakes inhabited GGI
Sterijovski et al.—Threats to Dice Snakes in Macedonia.
472
before 2011. Whatever the case, a high proportion of the
Dice Snake population has been taken by the poachers
since 2011. Furthermore, the impact of illegal fishing
around GGI may have an influence on the entire
population of Dice Snakes in the Prespa Lake region. In
spring 2012, we inspected the three other islands of the
lake (Agios Achilleos and Vidronisi in Greece and Mal
Grad in Albania) and none of them sheltered dense or
large population of Dice Snakes as observed on GGI.
We note that no snakes marked on GGI were later
captured on any of the three other islands of the lake, or
in the shore populations of the mainland, suggesting that
migrations from Golem to other sites, if any, are limited.
Thus, there is little option for inter-population
compensation if the colony of GGI is severely impacted.
In addition to the direct effect of poaching, indirect
threats should be considered. Over-fishing may cause a
depletion of the main prey consumed by Dice Snakes
and by other predators (e.g. cormorants, otters). Dice
Snakes represent an important food source for various
birds (diurnal and nocturnal raptors, herons), otters, and
vipers, that all feed regularly or intensively on Dice
Snakes (Ajtić et al. 2013). The collapse of Dice Snakes
may well perturb the trophic relationships and the
population dynamics of different species. Finally, many
tourists (transported by fishermen or poachers) freely
and illegally visit GGI. In the absence of official guides,
they impact the wildlife by killing snakes and illegally
collecting tortoises and sometimes they light fires (forest
fires were a major hazard in July 2012). Possible
impacts of tourism will increase in the near future. For
instance a major project for the development of tourism
in the Prespa Lake was signed between the Macedonian
government and the Portuguese company Aquapura
International (SeeNews. 2007. Portuguese Aquapura
Invests 50M€ in Hotel and Spa Centre in Macedonia.
Available from http://wire.seenews.com/news/portu
guese-aquapura-invests-50-mln-euro-in-hotel-and-spa-
centre-in-macedonia-217972. [Accessed 15 July 2014]).
We do not know if and how this project will be
achieved, but the Macedonian Tourism Office is
promoting GGI as a major tourist site (Macedonian
Tourism Office. 2014. Lake Prespa. Available from
http://makedonskibiser.com.mk/index.php?option=com_
content&view=article&id=601%3A2009-11-06-16-43-
18&catid=142%3A2009-08-22-23-37-48&Itemid=393&
lang=en. [Accessed 25 November 2014]).
Overall, although accurate size estimates of Dice
Snake or Belvica fish populations are not available, the
crude calculations we performed are supported by a
large data set and by the long term monitoring of the
study site. Regardless of the accuracy of our estimates,
illegal fishing and tourism should be better regulated
before irreversible damages occur to a remarkable and
prosperous population of Dice Snakes and to a whole
ecosystem that shelters very dense populations of
various species, notably reptiles. Paradoxically, the tri-
junction frontier between the FYR of Macedonia,
Greece, and Albania situated only 1.2 km south-west of
GGI is poorly attended by authorities. Thus, illegal
fishing is rapidly developing and large numbers of
people visit GGI without official permit and without risk
of sanction. Clearly, official regulations are not
respected and consequently a very large snake
population of Europe is in danger. Unfortunately, the
conservation status of the Dice Snake (Least Concern;
Agasyan et al. 2014) is not particularly helpful to launch
conservation actions. A practical solution would be to
involve local fishermen and students. Official permits
should be delivered to selected people to organize boat
transport and visits on GGI. Fees from these permits
could provide an important income. Appropriate
publicity may attract sufficient (albeit, limited) numbers
of visitors to see the unique and fascinating reptilian
fauna of the island. Providing unambiguous scientific
information regarding the extraordinary ecological value
of not-yet threatened reptilian species, and about major
threats to them, represents the first step to convince
authorities and to set up such practical conservation
actions.
Acknowledgments.We are grateful to many people
from several countries who participated in the field
research. Special thanks to the authorities of the
National Park Galičica who issued the official permits
and to Mitko Tasevski who immensely contributed to
logistic support. Ljiljana Tomović was partly financed
by the Ministry of Education, Science and Technological
Development of Republic of Serbia (Grant No. 173043).
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B
OGOLJUB
S
TERIJOVSKI
started with batracho-herpetology within the Research Society of the
Biology Students from Skopje, Macedonia in 1999. He was involved in many projects concerning
distribution mapping, EIA studies, and valorization on protected areas. He is a member of
IUCN/SSC Amphibian Specialist Group, Societas Europaea Herpetologica, Macedonian
Ecological Society, and Serbian Herpetological Society. His expertises are faunistics, project
management, and population ecology. (Photographed by Xavier Bonnet).
R
ASTKO
A
JTIĆ
works as an expert Herpetologist at the Institute for Nature Conservation of the
Republic of Serbia. He has been studying vipers (Vipera ammodytes, V. berus, and V. ursinii) in
the central part of the Balkan Peninsula since 1997. His specialties are herpetology, field
research, conservation of amphibians and reptiles, and population ecology. Rastko is one of the
founders of the Serbian Herpetological Society, Milutin Radovanović. (Photographed by Rastko
Ajtić).
L
JILJANA
T
OMOVIĆ
works as an Associate Professor of Vertebrate Morphology, Systematics,
and Phylogeny at the University of Belgrade, Faculty of Biology. She has been studying vipers
(Vipera ammodytes, V. berus, and V. ursinii) in the central part of the Balkan Peninsula since
1993. Her specialties are herpetology, morphology, systematics, population ecology, and
ethology. Ljiljana is a member and one of the founders of the Serbian Herpetological Society,
Milutin Radovanović. (Photographed by Metodija Velevski).
X
AVIER
B
ONNET
is a Senior Researcher at the Centre d’Etudes Biologiques de Chizé (UMR
CNRS-Université de la Rochelle) in France. During the past 23 y, he studied snakes and tortoises
in different places (France, Morocco, Togo, Australia, New Caledonia, China) and more recently
in Macedonia. Interested in ecology, evolution, conservation, and environmental education, his
specialty is to set up long-term field studies and to use eco-physiological investigative methods.
(Photographed by Jean-Marie Ballouard).
Thesis
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