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Turkey harbors a high diversity of viperid snakes, many with a high threat level on the International Union for Conservation of Nature (IUCN) Red List, yet perception about even basic topics, such as distributions and conservation statuses, remain poor. We initiated a multi-year project 7 y ago to compensate these shortcomings and present herein dramatically improved information on the status of mountain vipers of central-eastern Anatolia (Asian Turkey): Bolkar Viper (Montivipera b. bulgardaghica), Albizona Viper (M. b. albizona), Wagner’s Viper (M. wagneri), and partly Ottoman Viper (M. xanthina). The data originate from our fieldwork and a comprehensive search of all records available, including information from literature, online resources, locals, and herpetological experts. This resulted in 51 new localities, complemented by 36 published records, which were refined with new information, including four corrected/removed records and two records that were combined with new records due to their proximity. We summarized all records with precise information in a supplemented list of 85 localities, which is compared to current literature and the range maps available on the IUCN Red List of Threatened Species, the global standard reference for consultation on range maps and conservation status of species. Consequently, we report on large range extension of > 100 km in all four mountain viper taxa, increase the extent of occurrence for each viper taxon 4–8 times, reduce the distribution gaps between all pairs of parapatric, related, and ecologically similar mountain vipers, and discuss taxa delimitation, putative contact zones and conservation aspects.
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169
Herpetological Conservation and Biology 15(1):169–187.
Submitted: 8 April 2019; Accepted: 4 February 2020; Published: 30 April 2020.
Copyright © 2020. Konrad Mebert
All Rights Reserved.
Mountain Vipers in Central-eastern turkey:
Huge range extensions for four taxa resHape DeCaDes
of MisleaDing perspeCtiVes
Konrad Mebert1,11, bayraM GöçMen2, Naşit İğci3,4, Mert Kariş2,5,
MehMet aNil Oğuz2, MehMet zülfü Yildiz6, alexaNdre teYNié7, NiKOlaus stüMpel8,
aNd sYlvaiN urseNbacher9,10
1Institute of Development, Ecology, Conservation and Cooperation, Via G. Tomasi di Lampedusa 33, 00144 Rome, Italy
2Department of Biology, Zoology Section, Ege University, Faculty of Science, TR 35100 Bornova-Izmir, Turkey
3Department of Molecular Biology and Genetics, Faculty of Arts and Sciences, Nevşehir Haci Bektaş
Veli University, 50300 Nevşehir, Turkey
4Science and Technology Application and Research Center, Nevşehir Haci Bektaş Veli University, 50300 Nevşehir, Turkey
5Program of Laboratory Technology, Department of Chemistry and Chemical Process Technologies, Acigöl Vocational
School of Technical Sciences, Nevşehir Haci Bektaş Veli University, Nevşehir, Turkey
6Zoology Section, Department of Biology, Faculty of Arts and Sciences, Adiyaman University,
02040 Merkez, Adiyaman, Turkey
7UMR Epidémiologie des Maladies Animales et Zoonotiques, INRA - VetAgro Sup, Centre INRA Auvergne-Rhône-Alpes,
63122 Saint Genès Champanelle, France
8Staatliches Naturhistorisches Museum Braunschweig, Gausstrasse 22, Braunschweig, D-38106, Germany
9Department of Environmental Sciences, Section of Conservation Biology, University of Basel, St. Johanns-Vorstadt 10,
4056 Basel, Switzerland
10Info fauna - CSCF and karch, Avenue de Bellevaux 51, 2000 Neuchâtel, Switzerland
11Corresponding author, e-mail: konradmebert@gmail.com
Abstract.—Turkey harbors a high diversity of viperid snakes, many with a high threat level on the International
Union for Conservation of Nature (IUCN) Red List, yet perception about even basic topics, such as distributions
and conservation statuses, remain poor. We initiated a multi-year project 7 y ago to compensate these shortcomings
and present herein dramatically improved information on the status of mountain vipers of central-eastern Anatolia
(Asian Turkey): Bolkar Viper (Montivipera b. bulgardaghica), Albizona Viper (M. b. albizona), Wagner’s Viper (M.
wagneri), and partly Ottoman Viper (M. xanthina). The data originate from our eldwork and a comprehensive
search of all records available, including information from literature, online resources, locals, and herpetological
experts. This resulted in 51 new localities, complemented by 36 published records, which were rened with new
information, including four corrected/removed records and two records that were combined with new records due
to their proximity. We summarized all records with precise information in a supplemented list of 85 localities,
which is compared to current literature and the range maps available on the IUCN Red List of Threatened Species,
the global standard reference for consultation on range maps and conservation status of species. Consequently, we
report on large range extension of > 100 km in all four mountain viper taxa, increase the extent of occurrence for
each viper taxon 4–8 times, reduce the distribution gaps between all pairs of parapatric, related, and ecologically
similar mountain vipers, and discuss taxa delimitation, putative contact zones and conservation aspects.
Key Words.—Albizona Viper; Anatolia; Bolkar Viper; conservation; IUCN Red List; Montivipera b. albizona; Montivipera
b. bulgardaghica; Montivipera wagneri; Montivipera xanthina; Ottoman Viper; taxa delimitation; Wagner’s Viper
introDuCtion
Turkey has a high viper diversity with at least 11
currently recognized species belonging to the genera
Macrovipera, Montivipera, Daboia, and Vipera (e.g.,
Joger 1984; Mallow et al. 2003; Budak and Göçmen
2008; Mebert et al. 2015a; Göçmen et al. 2018; Freitas
et al. 2020). This unusually high viper diversity for a
Palearctic country likely is the result of its complex
biogeographic history and habitat diversity (Stümpel et
al. 2016); however, taxonomy and phylogeography of
Anatolian vipers is still a controversial issue (Stümpel
and Joger 2009; Mebert et al. 2016). Most of these vipers
received a threat status from the International Union for
Conservation of Nature (IUCN) higher than Vulnerable,
including three of the eight viper species listed globally
as Critically Endangered (IUCN 2020). Unfortunately,
references about distribution and ecology of Anatolian
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Mebert et al.—Range and conservation aspects of Turkish mountain vipers.
vipers are very limited (e.g., Göçmen et al. 2014, 2017;
Mebert et al. 2016), and often portray an unrealistic
situation, as explained herein. This also applies to the
genus Montivipera (mountain or rock vipers), which has
experienced a tumultuous history and was taxonomically
separated from other Palearctic vipers by Nilson et al.
(1999). A few taxa have been described in the last 150 y
(Ottoman Viper, M. xanthina, Radde’s Viper, M. raddei,
Lebanon Viper, M. bornmuelleri, and Lati’s Viper, M.
latii), whereas more recent taxonomic research resulted
in the description of a number of new taxa (Wagners
Viper, M. wagneri, Bolkar Viper, M. bulgardaghica,
Albizona Viper, M. albizona; and Kuhrang Viper, M.
kuhrangica). Species delimitation among these taxa has
remained controversial (e.g., Nilson and Andren 1986,
1992; Schätti et al. 1991; Sindaco et al. 2013), but some
recent studies provided more clarity on relationships
among mountain vipers (Stümpel and Joger 2009;
Stümpel 2012; Stümpel et al. 2016).
Some of the mountain vipers are rather colorful
(raddei, wagneri, albizona) or show a highly variable
and contrasting color pattern (bulgardaghica, xanthina)
that, combined with their putative rarity, led to a
temporary illegal collection frenzy for the pet trade in
the 1980s–90s. Frequent commercial trading, privately
and at reptile expositions, combined with the fear
that the few known populations could be irreversibly
negatively affected, led to the categorization of several
species with a high threat status by the IUCN in the
1990s. A new round of IUCN reassessments in 2008
mainly implemented a higher threat level of mountain
viper species compared to the ones published 15 y earlier
in 1996, yet without any new supporting information
about population aspects and taxonomic clarications.
Unfortunately, concerns about putative illegal over-
collecting of many vipers have persisted, even though
there is a complete lack of corroborating data over the
last decade aside from anecdotes about illegal export of
a few individuals that would have only a very limited
impact at the population or species threat level. On
the other hand, substantial threats caused by habitat
destruction, e.g., mining activities, valley ooding for
electric power generation, massive livestock grazing, or
plantation sprawl, was strongly underestimated (Mebert
et al. 2016; Zinenko et al. 2016).
Furthermore, competitive interactions among
interested people (professionals and amateurs) have
continued after the last IUCN Red List assessment in
2008 and produced a generally tense climate of distrust,
misinformation, defamations, false assessments and
unrealistic administrative perceptions in relation to
Anatolian vipers. At the same time, a lack of basic
biological studies about distribution, habitat, and
population aspects of Turkish mountain vipers have
prevented a realistic assessment of the extent of
occurrence, population size/densities, and threat levels
of most taxa to this day. To counter the widespread
misunderstanding about these vipers, we initiated a
project 7 y ago to better understand the phylogeny
and biogeography of Anatolian vipers and have
published results on a regular basis (e.g., Mebert et
al. 2014, 2017a; Göçmen et al. 2015a,b; Nalbantsoy
et al. 2016; Stümpel et al. 2019). This study, as well
as the previous ones, represent additional information
for a work in progress, which should culminate in a
much more realistic assessment about the systematic
allocation and true distribution of mountain vipers in
Turkey than is currently presented in publications and
unpublished governmental monitoring reports. Such
documents are often based on the IUCN Red List les
(IUCN 2020), which are regarded as the most inuential
source of information for species conservation in the
world (AGENDA 21. 2010. Understanding NGOs’
[non-government organizations] vision for the 21st
Century. Available from https://agendatwentyone.
wordpress.com/2010/06/28/understanding-ngos-
non-government-organizations/ [Accessed 11 July
2019]; wiseGEEK. 2014. What is IUCN? by Ellis and
Brownyn. Available from https://www.wisegeek.com/
what-is-iucn [Accessed 10 July 2019]; and Saha et al.
2018). Our collection of new and rened information
on the distribution of Anatolian mountain vipers
will inform and guide key national and international
policy and conservation activities and/or regulations.
This information will also be useful for the scientic
community and serve as an important education and
information resource for the public, improve species
identications, help potential funding, and will be
crucial in our goal to overhaul the respective IUCN Red
List les (IUCN 2020).
We restrict our work here to four mountain viper
taxa from south-central to north-eastern Turkey; hence,
excluding Montivipera raddei and most of the core
and western range of M. xanthina. Each species has a
conservation status and current population assessment
according to the IUCN Red List of Threatened Species
(IUCN 2020). Montivipera b. albizona (Albizona
Viper or Central Turkish Mountain Viper) is listed as an
Endangered Turkish endemic, its Extent of Occurrence
is fewer than 5,000 km2, it is known from fewer than
ve locations, and has a continuing population decline
inferred in the number of mature individuals due to the
likely collection for the pet trade and intentional killing.
Montivipera b. bulgardaghica (Bolkar Viper) is listed as
Least Concern because it occurs in an area of extensive
and suitable habitat that appears not under threat, has
a presumed large overall population, and is unlikely to
be declining fast enough to qualify for listing in a more
threatened category. Montivipera wagneri (Wagner's
Viper) is listed as Critically Endangered, is endemic to
Turkey, has experienced a population decline of more
than 80% from exploitation and collection for the
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Herpetological Conservation and Biology
international pet trade over the past three generations
(18 y), and is predicted to have a continued population
decline from over-collection and planned dam
construction in the Aras River Valley, which would
cause a loss of over 80% of suitable habitat for this
species. Montivipera xanthina (Ottoman Viper) is listed
as Least Concern in view of its wide distribution, large
population, and because it is unlikely to be declining
fast enough to qualify for listing in a more threatened
category.
Our primary objective is to initiate a process to
counter the general lack of knowledge about Turkish
mountain vipers, from simple distribution to population
biology and ecology, which is preventing any reliable
assessment of species recognition and conservation
statuses. It is therefore urgent to rapidly improve
our knowledge of the true range limits, population
sizes, species delineation, and relevant environmental
factors that may affect population dynamics. This can
be achieved quickest with a multi-faceted approach
by compiling geographic data on population extent
and habitat occupancy in general and molecular and
morphological data from contact zones or contiguous
(parapatric) populations of two or more viper species
(Mebert et al. 2015b, 2017b). Finally, it is our
overriding objective to provide tools for appropriate
future conservation assessments (Extent of Occurrence,
Population Size/Trend) and actions/management by
publishing herein the massively enlarged distribution
size of Turkish mountain vipers than is ofcially
known.
Material anD MetHoDs
Taxonomic and morphological considerations.
Beginning in 2013, we started to compile a database
on Montivipera, focusing on Turkey. We engaged in a
holistic approach and compiled data from all available
sources, including annual eld excursions and sampling
of representative genetic tissues for species delineation,
searching all literature references, contacting authors of
online photos and reports, questioning locals as well as
herpetologists that have been active in Turkey. We here
largely follow the taxonomic concept of Stümpel et al.
(2016) but expect changes in the future (Freitas et al.
2020).
The Albizona Viper was originally described as
Vipera albizona by Nilson et al. (1990), placed into
the genus Montivipera by Nilson et al. (1999), and
subsequently conrmed by Garrigues et al. (2005).
Recently, M. albizona was suggested as a subspecies of
the Bolkar Viper (M. bulgardaghica) due to molecular
evidence (Stümpel and Joger 2009; Stümpel et al. 2016).
Because the distinction between the two subspecies has
become blurrier with new, often photographic, material,
we apply the subspecies epithet of such specimens listed
herein based on its proximity to the historically known
distribution, and/or topographically linked habitats.
Potential contact (or transition) zones between them are
purely speculative due to lack of data but are suggested
and briey discussed based on geographic proximity of
new material.
The similar and somewhat overlapping color
pattern between M. wagneri and M. b. albizona and the
missing information of a putative contact zone (or most
proximate populations) between them, may render the
taxon allocation of some individual vipers solely based
on photographic and geographic data difcult. Taxon
allocation of such data, however, was decided based on its
proximity to the nearest known mountain viper location,
reecting that no two Montivipera taxa are known to
overlap (Mebert et al. 2016; Stümpel et al. 2016), and a
combination of following features: (1) Morphology: To
be viewed only tentatively because there seems to be a
large overlap of external characters based on published
and our own information. Furthermore, diagnosis
by previous authors (see Table 1) was retrieved from
very small samples, usually representing two to three
populations from the northern range limit of each taxon,
thus missing a more widespread geographic variation
inherent in each taxon. (2) Habitat: Is the habitat linked
to other conspecic populations? We visually evaluated
potential connecting corridor to other known sites of
Montivipera populations at < 5 km distance for suitable
rocky habitat on plateaus or along valleys < 2,200 m
elevation using satellite images from Google Earth
Pro. (3) Molecular: We screened haplotype association
for a few sampled specimens and compared them with
published data. We investigated mitochondrial DNA
following Stümpel et al. (2016) and compared the
obtained sequences to the current published ones in
GenBank using BLAST online. All the evaluation and
Morphological
Character
M. b. albizona M. wagneri
Lateral blotches Blackish spots Dark vertical
stripes
Inner circumoculars ≤ 13 ≥ 12
Ventral scales ≤ 155 ≥ 161
Size mid-dorsal
blotches incl. black
borders
≥ 9 scales wide < 9 scales wide
Contact occipital spots
to rst dorsal blotch
Disconnected Connected up to
50%
Contact occipital spots
to postorbital stripe or
rst lateral blotch
Connected up to
50%
Disconnected
table 1. Differences in morphology between Albizona Viper
(Montivipera bulgardaghica albizona) and Wagner’s Viper (M.
wagneri) both from northern populations, based on Joger et al.
(1988), Nilson et al. (1990), and Mulder (1994).
172
Mebert et al.—Range and conservation aspects of Turkish mountain vipers.
taxon allocations, in particular those that originate from
photos only, should be seen as provisional until ner
analysis (i.e., a more complete genetic and morphological
analysis) is available. We summarized and listed most
relevant and available locality data of Montivipera
wagneri, M. b. bulgardaghica, and M. b. albizona, but
also the south-eastern range segment of M. xanthina
which is most proximate to other mountain viper taxa
(see Locality List in Supplemental Information).
results
The updated range of the four mountain viper taxa
(Fig. 1) generally shows a rather continuous range of
Montivipera taxa from west to east, much different from
the general perception of isolated populations or as
presented in IUCN Red List les. Listed numbers in the
distribution maps (Fig. 2 and subsequent maps presented
for each taxon below) correspond to locality numbers in
the specimen/habitat photographs and Locality List in
the Supplemental Information.
Wagner’s Viper (Montivipera wagneri).—We
provisionally assign all Montivipera specimens,
including those based on photographs, that originate
from south of the Munzur Mountains in the provinces
Tunceli and Erzincan, and from east of the Euphrates
River Valley in provinces farther south, to M. wagneri.
figure 1. Updated distribution of mountain vipers in Turkey. Points represent locality records (see Locality List in Supplemental
Information) for Ottoman Viper, Montivipera xanthina (black), Albizona Viper, M. b. albizona (green), Bolkar Viper, M. b. bulgardaghica
(light blue), Wagner’s Viper, M. wagneri (yellow), and Radde’s Viper, M. raddei (red). Locality marks for western and inland Ottoman
Viper (M. xanthina) are not complete, but sufciently representative, as they are not the focus in this study. Black interrupted lines
represent country borders. A larger version of this map is accessible in Supplemental Information.
figure 2. Updated distribution of Wagner’s Viper (Montivipera wagneri) and adjacent locations of Radde’s Viper (M. raddei) in Turkey.
Numbers refer to the Locality List in the Supplemental Information, but only for M. wagneri, as M. raddei is not the focus of this study.
Several samples used for genetic analysis originate from Aras Valley (circled locality-1) and other single locations that are indicated with
a black center. Question marks indicate areas where further Montivipera populations are expected but require conrmation. A larger
version of this map is accessible in Supplemental Information.
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Herpetological Conservation and Biology
The range extends about 250 km west of the previously
known western limit near Horasan (locality-2 in Fig.
2; Kumlutas et al. 2015) and includes also recently
discovered published (Göçmen et al. 2014; Yildiz et
al. 2018) and unpublished sites in the provinces Kars,
Ağri, Muş, Erzurum, Bingöl, Elazığ, and Tunceli
(Figs. 3 and 4, plus Supplemental Information Figs.
S1–S7). Complementary to these allocations, all
Montivipera records from northwest of the Munzur
Mountains and west of Euphrates River are assigned
to M. b. albizona.
Albizona Viper or Central Turkish Mountain Viper
(Montivipera bulgardaghica albizona).—Correction
of Terra Typica: the terra typica of albizona was
originally given as Kulmac Daglari (Nilson et al. 1990),
a mountain chain that begins in the west just north of the
villages Harmandali and Kürkçüyurt, district Altinyayla/
Sivas, and ends in the east at Yilanli Mountain, district
Kangal/Sivas. The entire 70 km mountain chain appears
to provide some suitable habitat for Montivipera vipers,
but not as extensive as the Tecer Mountains parallel
to the north, a well-known site for M. b. albizona
(localities 25-28 in Fig. 5 and Supplemental Information
Figs. S7E, S9). Recent discussions with the senior
author of the description and provision of coordinates,
however, revealed that the terra typica lies 100 km
farther east near the Karaşar Geçidi (= K. pass), district
Divriği/Sivas (see locality-23 below). We also present
new and rened localities in the provinces Erzincan,
Malatya, Kayseri, Sivas, Kahramanmaraş, and Hatay
(Supplemental Information Figs. S7–S12), as well as
a large southeastern extension into province Adiyaman
(locality-45 in Fig. 5, photographs in Fig. 6, and more
specimens depicted in Supplemental Information Fig.
S13) about 145 km south and 195 km east of previously
known sites (Göçmen et al. 2014). The distribution
map in Fig. 5 also replaces the one presented in Çiçek
et al. (2017), which is based on previous literature and
photographic records, all presented herein with more
precision and corrections, where appropriate. No
vouchers could be located for the presence of M. b.
albizona in Sivas-province districts Gemerek, Yildizeli
and Zara (Çiçek et al. 2018; Kerim Cicek, pers.
comm.), but see discussion appended to locality-34 in
Supplemental Information.
figure 3. Range extensions of Wagner’s Viper (Montivipera wagneri) in Turkey. (A) Individual from Günindi, district Kağizman/Kars,
near eastern end of encircled locality-1, respectively contact zone with M. raddei (Mebert et al. 2016); (B) Individual from locality-4a,
Dereköy, district Tutak/Agri; (C) locality-8, habitat and two Wagner’s Viper from the area between Bostancilar and Akçakaynak, district
Bulanik/Muş. (A, C, and insert photographed by Konrad Mebert and B by Naşit İğci).
174
Mebert et al.—Range and conservation aspects of Turkish mountain vipers.
figure 5. Updated distribution of Albizona Viper (Montivipera bulgardaghica albizona) and nearest record of the Bolkar Viper
(Montivipera b. bulgardaghica) in Turkey. Numbers refer to the Locality List in the Supplemental Information. Samples used for genetic
analysis are indicated with a black center, except for locality-40 from Başkonuş, Merkez/Kahramanmaraṣ, which refers to an albumin
analysis by Göçmen et al. (2009). Question marks indicate regions where further Montivipera populations are expected but require
conrmation. An enlarged version of this map is in Supplemental Information.
figure 4. First conrmed presence of Wagner’s Viper (Montivipera wagneri) in Tunceli Province, Turkey. Habitat and a Wagner’s Viper
from locality-14, Tahkini Yaylasi-Pohoz Mevki, northeast of Turnayolu, district Nazimiye/Tunceli. (Photographed by Konrad Mebert).
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Herpetological Conservation and Biology
Bolkar Viper (Montivipera b. bulgardaghica).—
We extend the range about 13 km west within province
Mersin and 130 km east in province Adana (Fig. 7). We
include photographic vouchers (Fig. 8 and Supplemental
Information Figs. S14–S16) of this species. Information
about the records is given in the Locality List in the
Supplemental Information.
Ottoman Viper (Montivipera xanthina).—Only
south-eastern records are mapped herein (Fig. 9; but
see wider view in Fig. 1). In the Locality List (see
Supplemental Information), we summarize new and
rened (from previously published, mainly primary
sources) records of the Ottoman Viper from its
southeastern-most range, adjacent and as close as 11
km from Montivipera bulgardaghica ssp. We include
photographic vouchers (Fig. 10 and Supplemental
Information Figs. S17 and S18), including the rst
documentation of M. xanthina from the province of
Mersin.
DisCussion
Distribution and conservation aspects.—Among
snakes, vipers are perceived as disproportionately
threatened with extinction, and thus, acquiring
information on their distribution, ecological niche, and
natural history is fundamental to better understand their
biology and assess their conservation status (Maritz et
al. 2016; Alencar et al. 2018; Saha et al. 2018). This has
also become evident to us since the start of this project
in 2013, because the biology of vipers in Turkey has
remained poorly studied to this day, including studies
on their distributions and population statuses with only
fragmentary or misleading information. This lack of
good data is reected in the IUCN Red List les in three
of four Montivipera taxa treated herein (M. wagneri, M.
b. bulgardaghica, M. [b.] albizona) and in most recent
scientic publications (Kumlutaş et al. 2015; Tok et al.
2015; Gül et al. 2016; Tuniyev 2016; Kurnaz et al. 2018;
Ahmadi et al. 2019), Turkish provincial governmental
reports (e.g., Çiçek et al. 2017; Avci et al. 2018), and in
virtually all books that include chapters on vipers from
Anatolia (e.g., Phelps 2010; Sindaco et al. 2013; Geniez
2015).
By using a combination of published results,
satellite images from Google Earth Pro, as well as the
increasing provision of open online landscape photos,
we conclude that suitable habitat for most viper species
appears relatively extensive across much of Anatolia.
When combining key factors, such as southern aspect,
elevation, and coarse-rocky surface structure (no ne
sediments) to provide shelter for night, hibernation, and
prey, potential new locations can often be pinpointed
on satellite images. We have also extended the habitats
of Montivipera spp. from rocky mountain slopes
with bushes (e.g., Aras Valley in Kars, locality-1,
Supplemental Information Fig. S1) and light forests
figure 6. The new, currently most southeastern, locality of Albizona Viper (Montivipera bulgardaghica albizona) in Turkey at the
Nemrut Archaeological site, district Kahta/Adiyaman, locality-45. Depicted is one of the treeless areas near the peak and one of the
Albizona Vipers found there (see more examples in Supplemental Information Fig. S13). (Photograhed by Mehmet Zülfü Yildiz).
176
Mebert et al.—Range and conservation aspects of Turkish mountain vipers.
(e.g., Kar Boğaz Valley in Fig. 8, from localities-50–52,
and Göller in Adana, locality-46), to wet riparian
habitats (e.g., Ovacik/Sivas locality-25, Supplemental
Information Fig. S9), dry steppe-like stony hills (e.g.,
Otluca/Ağri locality-5 and Dolabaş/Muş locality-7 and
Supplemental Information Figs. S2 and S3), treeless
rocky mountain summits (e.g., Bozdağ Tepesi/Hatay
locality-43 and Mt. Nemrut/Adiyaman locality-45,
Fig. 6), agricultural elds at about 1,000 m elevation
(Bostanli/Kahramanmaraş locality-41, Supplemental
Information Fig. S11), and hilly-rocky high elevation
plateaus around 1,800–2,200 m elevation (e.g.,
Karakuyu/Sivas locality-36, Yilanhöyük locality-31,
Masman Basi/Erzincan locality-21, Hisarlik Plateau/
Konya locality-78, Mağara-Kirobasi/Mersin locality-72,
Supplemental Information Fig. S17). In particular, the
extensive bush and grassland on at, rocky plateaus are
rarely listed as habitat for Montivipera spp. in surveys
and the general literature (see example in Supplemental
Information Fig. S4). Yet, these plateaus are common
and extensive in eastern Anatolia and likely constitute
a largely neglected habitat for mountain viper surveys
with the potential for many overlooked populations.
Hence, lack of nding vipers results from insufcient
eld exploration and coordination with good weather
conditions for surface activities of these generally
secretive snakes, particularly those living in semi-arid
climates across most of inner Anatolia. In only seven
figure 7. Updated distribution of Bolkar Viper (Montivipera b. bulgardaghica) in Turkey. Inset map repeats the same sites overlaid
by a light blue shading but enlarged to show the two eastern-most sites (localities-46 and -47, see vouchers in Fig. 8). Numbers refer to
the Locality List in the Supplemental Information. Samples used for genetic analysis are indicated with a black center. Question marks
indicate areas where further Montivipera populations are expected but require conrmation. A newly discovered Ottoman Viper (M.
xanthina (black dot-70) near bulgardaghica-locality-62 indicates a potential contact zone between them. An enlarged version of this map
is in Supplemental Information.
years, we tried to compensate for those insufciencies by
systematically optimizing eld and desk work, including
networking, with a pioneering focus on new regions
and addressing all available sources of recent locality
data on vipers. This resulted in a rapid accumulation of
distribution knowledge for some mountain vipers (other
Turkish viper taxa show a similar trend and are currently
being analyzed as well). Compared to the range maps
published on the IUCN Red List of Threatened Species
(IUCN 2019), the Extent of Occurrence for Montivipera
b. bulgardaghica was enlarged by more than four
times (from 1,300 to 6,000 km2), with extensions of
about 13 km in western (locality-62, Fig. 7) and 130
km in northeastern (locality-46, Fig. 7) directions
from the corresponding IUCN range (see Fig. 11).
The distribution area for Montivipera b. albizona was
enlarged by about eight times (from < 5,000 km2 to
38,500 km2; see Fig. 11), with extensions of about 145
km to the south (locality-43, Fig. 5) and 160 km to the east
(locality-45, Fig. 5); similarly the extent of occurrence
for M. wagneri was enlarged about eight times (from
2,500 to 21,000 km2; see Fig. 11), with extensions of
about 226 km in southwestern (locality-15, Fig. 2), and
30 km in eastern directions to Günindi, Kars (locality-1,
the eastern-most of the wagneri-localities shown in Fig.
2), whereas the range of M. xanthina was extended by
150 km east (locality-70, Fig. 9) across the vast highland
plateau from its nearest previously published record in
177
Herpetological Conservation and Biology
Kumlutaş et al. (2004). We can safely assume that these
large range extensions will concomitantly increase the
total population size of each taxon, even though the
many mountain valleys with suitable habitat between
the listed localities have not been explored thus far.
Yet, with the core of Montivipera diversity contained
in Anatolia, it remains with the Turkish government
to safeguard existing populations and implement any
necessary conservation measures against threats from
habitat destruction and climate warming (Mebert et al.
2016; Ahmadi et al. 2019).
We anticipate that many viper species of Anatolia will
follow a similar path of revelations as was experienced
with Orsini’s Viper Vipera ursinii in France, which once
was estimated to consist of six to nine populations with a
total of 200–300 animals by the late 1980s (Corbett 1989;
Stumpel et al. 1992), but surveys up to 2008 corrected
those numbers to 21 populations with a potential
carrying capacity of 168,000 vipers (Lyet et al. 2013).
Similarly, there has been rapidly increasing distribution
knowledge for Karst Viper Vipera u. macrops (Jelić et
al. 2013) and Greek Meadow Viper, V. graeca (Mizsei
et al. 2016, 2018). Not unexpectedly, the biogeographic
situation of vipers in Anatolia is increasingly resembling
other Palearctic vipers occurring in southern Europe,
where every mountain/valley has (or had, if the habitat
has since become too degraded or lost) its population
of vipers, a situation already quite well predicted by
Schätti et al. (1991).
The often-cited major threat through illegal collection
by Baran and Atatür (1998) or IUCN (2020) appears
outdated for Turkey, except for very small and isolated
populations that could be quickly overexploited. Yet such
specic cases are not known for Turkey. Indeed, neither
reports by the Turkish authority, nor recent workshops
with our attendance as viper experts at the Viper
Specialist Group-IUCN meetings in Greece (2014) and
Morocco (2017) revealed any large-scale sampling or
smuggling of vipers out of Turkey. Similarly, no illegal
snake smuggling aside from single specimens, which
itself is biologically irrelevant for the survival of a
population and much less that of a species, have been
found by a governmental compilation of smuggling
cases from 2007–2017 (General Directorate of Nature
Conservation and National Parks, Turkey. 2018. Ofcial
statistics on the number of biosmuggling cases in
Turkey from 2007–2017. Available from http://www.
milliparklar.gov.tr/resmiistatistikleryeni [Accessed
5 March 2019]), or by a new summary study on bio-
smuggling in Turkey (Birben and Gençay 2019),
inquiries from NGOs, commercial markets, breeders
or other scientists, as well as our own experience
(Mebert et al. 2016). According to the Convention on
Biological Diversity (https://www.cbd.int), however, in
which Turkey participates, countries have the right to
their biological diversity and should control the access
to their biological resources to secure sustainable use.
Precautions against bio-smuggling is important in this
context even for single specimens. Although a variety
of viper species were exported from Turkey in the past
without permission, and illegal collection has been cited
as a threat issue for all four Montivipera taxa treated
herein (see respective les in IUCN 2020), this activity
has signicantly reduced in the past 20 y. This has been
due to regulations and governmental projects on this
subject and the increasing risk of illegally exporting bio-
goods out of Turkey, and also due to the saturation of the
pet market with captive-bred specimens. Fortunately,
today, anyone from Turkey or abroad can conduct
studies after receiving appropriate and collaborative
permits from the governmental bodies.
Another aspect that grew out of the non-representative
fear about illegal collecting relates to non-academic
herpetologists and naturalists that post their new viper
figure 8. Distribution updates of the Bolkar Viper (Montivipera
b. bulgardaghica) in Turkey. (A) locality-46, Göller Yaylasi,
district Kozan/Adana (Photographed by Şensu Küçükateş); (B)
locality-47, Kizildam, district Aladağ/Adana, specimen with a
color pattern more typical for albizona (Photographed by Karim
Amri); (C) locality-51, Kar Boğaz Valley, district Pozanti/Adana
(Photographed by Mehmet Zülfü Yildiz); (D) male and female
vipers (Photographed by Bayram Göçmen); (E) male and female
vipers from nearby locality-50 (Photographed by Fabien Bettex; (F)
male and (G) female vipers from western-most locality-62, Ünlük
Tepesi, Gavuruçtuğu, district Erdemli/Mersin (Photographed by
Mert Kariş).
178
Mebert et al.—Range and conservation aspects of Turkish mountain vipers.
ndings on social media. We have contacted most
authors of such posts, yet a few were still unwilling to
share their locality information to prevent population-
damaging sampling. Such fear, however, is not realistic
based on the extensive habitat and distribution that
vipers occupy in Turkey today, as we demonstrate in
this paper. On the contrary, locality data could be more
usefully applied to conservation needs by assessing the
extent of occurrence, habitat constituents, population
sizes and immediate local threats to certain species that
otherwise may risk extinctions of entire populations
with 100s to several 1,000s of specimens. It was
recently concluded that the most prevalent threats facing
more than 8,000 threatened or near-threatened species
on the IUCN Red List of Threatened Species (IUCN
2020) are agriculture and overexploitation (Maxwell
et al. 2016; Grooten and Almond 2018). Habitat
degradation through agriculture, but also through over-
grazing, urban sprawl, and plantations poses massive
structural landscape changes with often severe negative
effects on susceptible terrestrial species such as vipers.
Substantive information on the conservation status of a
threatened species, such as range, population size, and
its ecological context, will depend on comprehensive
local data to better promote its survival in the future.
Concerning conservation aspects, we strongly
argue that there are stronger and more realistic threats
to viper populations than illegal collection for the
international pet trade. The principal threats for
Anatolian mountain vipers are likely posed by wide-
scale habitat degradation and destruction, mainly
through overgrazing by domestic livestock (goats,
sheep, cattle), agriculture and plantations, suburban
sprawl, and valley ooding through dam construction
(Ettling et al. 2015; Maxwell et al. 2016; Mizsei et al.
2016; Çiçek et al. 2018; Grooten and Almond 2018). In
particular, Palaearctic steppes have become one of the
most endangered terrestrial biomes of the world through
high rates of conversion and widespread degradation
(Török et al. 2016). In Turkey alone, more than 44%
of the natural steppe and steppe forest area has been
lost due to conversion to cropland, afforestation, and
overgrazing, putting Anatolian mountain vipers that
depend on rocky montane grassland under increased
conservation risk (Ambarli et al. 2016; Wesche et al.
2016; Mebert et al. 2016). Because livestock changes
figure 9. Southeastern distribution of Ottoman Vipers (Montivipera xanthina) in Turkey. Numbers refer to the Locality List in the
Supplemental Information. The corresponding International Union for Conservation of Nature (IUCN) map also includes an area for M.
xanthina near where Adana, Niğde and Kayseri provinces meet. Because none of the literature in the IUCN assessment (IUCN 2020)
includes such a reference, we presume that area may represent district Ulukişla/Niğde and relates to the listing of M. xanthina for Bolkar
Daği Ulukişla in Başoğlu and Baran (1980), which later was described as M. bulgardaghica (Nilson and Andren 1985). Samples used for
genetic analysis are indicated with a white center dot and are either listed in Table S1 (Supplemental Information), except for locality-65
from south Ercyies Mt., Develi/Konya, which refers to an albumin analysis by Göçmen et al. (2009). Question marks indicate areas
where further Montivipera populations are expected but require conrmation of taxon allocation. An enlarged version of this map is in
Supplemental Information
179
Herpetological Conservation and Biology
vegetation structure and cover in ways important to
small mammals, community-level total abundance of
small mammals typically declines with grazing (Schieltz
and Rubenstein 2016), which in turn negatively affects
the food base of snakes. Similarly, Rotem et al. (2016)
found that reptile diversity decreased with grazing at
arid sites. To maintain viper diversity in Turkey, as well
as most other fauna and ora, it is necessary to consider
those threats and publicly address them in the future.
Taxa delimitation.—Because the IUCN Red List
assesses threat levels primarily at the species level
(IUCN 2020), delimitation of species becomes relevant;
however, insufcient geographic data often hampers
the biologically meaningful categorization of taxa
into species, subspecies, or local populations. This
partly applies also to Montivipera species for which
traditional species classication has been the standard
in the IUCN Red List. This standard is increasingly
challenged by means of expanding geographic sampling
and delimiting species using molecular methods. In
the most recent study, Stümpel et al. (2016) assessed
roughly a low 2–3% sequence divergence of three
mt-genes (CYTB, COX1, ND5) among Montivipera
wagneri, M. b. bulgardaghica, and M. b. albizona, a
situation asking for systematic re-evaluations in the
future (Freitas et al. 2020). Comparativley, a new study
on the Transcaucasian Ratsnake, Zamenis hohenackeri,
largely sympatric with our Montivipera spp. herein,
showed a broad intergradation zone (gene ow) between
subspecies that diverged at around 5% cyt b (Hofmann
et al. 2018), higher than in aformentioned Montivipera
taxa. Bradley and Baker (2001) suggested that cyt b
divergence by < 2% between small mammal taxa is
indicative of subspecies level, whereas divergence from
2%–11% requires more methodological evaluation
(morphological, genetic, ecological, etc.), and divergence
of > 11% can be considered a species. Even though one
may expect that snake genera delimit by different levels
of cyt b divergence and might not be comparable to small
mammals, various studies that include closely related
snake species in sympatry, where species integrity is
figure 10. Updated distribution of Ottoman Vipers (Montivipera xanthina) from its southeastern range borders in Turkey. (A) Individual
from locality-66, west of Erciyes Mt., Subaşi, district Incesu/Kayseri (Photographed by Johan Nylander); (B) Viper from locality-68,
Azatli Dam, Çiftlik/Niğde (Photographed by Mert Kariş); (C) and (D) locality-70, M. xanthina and habitat, northwest Kuşluca (Toros),
district Erdemli/Mersin (Photographed by Fabien Bettex); (E) Viper from locality-71, northwest Akpinar, district Erdemli/Mersin
(Photographed by Konrad Mebert).
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Mebert et al.—Range and conservation aspects of Turkish mountain vipers.
naturally tested (Harrison 1993), show cyt b divergence
at an equivalent magnitude and range. For example, the
Southern and Northern watersnakes (Nerodia fasciata
and N. sipedon, respectively), diverge by 9% cyt b, but
produce very wide hybrid zones (20–100 km) that align
(are constrained) along environmental factors (Mebert
2008, 2010); Western and Eastern grass snakes (Natrix
helvetica and N. natrix, respectively), differ by 6.9%
with limited unidirectional nuclear gene ow across a
narrow contact zone between taxa (Kindler et al. 2017);
a divergence of 5.2% exists between partly sympatric
Mexican and Checkered gartersnakes (Thamnophis
eques and T. marcianus, respectively), or 5.5% between
Western Aquatic and Coast gartersnakes (T. couchii and
T. elegans, respectively; de Queiroz and Lawson 1994);
and sympatric North American brown snakes (Storeria
spp.) differ by 8% (Alfaro and Arnold 2001). Within the
Anatolian mountain vipers, a 9% difference separates
Montivipera wagneri and M. raddei with no sign of
introgression along a sharp parapatry line, consisting of
a 5–10 m wide shallow stream separating them north of
Kağızman, Turkey (Mebert et al. 2016; Stümpel et al.
2016).
In contrast, taxa with incomplete speciation and/or
hybridization tend to show levels of cyt b divergence <
5%, such as indicated by the complete fusion of ratsnake
lineages in southern Canada, classied as species
by Burbrink et al. (2000) that differ by 3.5% and are
regarded as conspecic (Gibbs et al. 2006), or the Plains
and Butler’s gartersnakes (Thamnophis radix and T.
butleri, respectively), that differ in Wisconsin by < 1%
(de Queiroz and Lawson 1994; Alfaro and Arnold 2001)
or < 2% in the more variable ND4 (Placyk et al. 2012),
likely as a result of ancient and long-standing mtDNA-
introgression reecting incomplete speciation (Placyk et
al. 2012; McVay et al. 2015).
In Palearctic vipers, there are currently several
recognized species with < 5% cyt b divergence, yet they
all relate to allopatric populations or taxa for which no
natural test (i.e., integrity in sympatry) is available, thus,
they may as well represent temporarily isolated and
locally variable subspecies, e.g., Armenian Steppe Viper
Vipera eriwanensis, Iranian Steppe Viper (V. ebneri),
Baran’s Viper (V. barani), Dinnik’s Viper (V. dinniki),
Lotiev’s Viper (V. lotievi), or some of the Montivipera
indicated in the text (Freitas et al. 2020). Hence, one
needs to compile more data from different lines of
evidence (integrative approach) to show that there is a
coherent pattern of distinct morphology, genetics, and
geographic structure. Adequate sampling is the basis
to compensate for the lack of required information
with proximate populations or even contact zones
between two taxa investigated for free gene ow today
or in the past by molecular means (Mebert 2008, 2010;
figure 11. Updated distribution of mountain vipers in south-central to north-eastern Anatolia, Turkey, with known localities as colored
circles on top of same color shaded areas representing their interpolated ranges: dark grey Ottoman Viper (Montivipera xanthina), light
blue Bolkar Viper (M. b. bulgardaghica), green Albizona Viper (M. b. albizona), yellow Wagner’s Viper (M. wagneri). For the latter three
taxa, the smaller, white-bordered, and color-saturated polygons represent the approximate and much smaller distribution maps as depicted
in the respective les of the International Union for Conservation of Nature (IUCN) Red List of Threatened Species (IUCN 2020). The
red transparent band over the Euphrates River leading north to a red-bordered area encircling the Munzur-Mercan Mountains indicates
the prominent landscape feature separating most proximate populations between M. b. albizona and M. wagneri or may represent their
potential contact zone. Similarly, the red-hatched circle near the Ceyhan River reects a potential contact or transition zone between
the subspecies of M. b. bulgardaghica and M. b. albizona. Question marks indicate areas where additional Montivipera populations are
expected but require conrmation. An enlarged version of the map is placed in Supplemental Information.
181
Herpetological Conservation and Biology
Hillis 2019). We strive to improve our knowledge in
locating these contact zones or proximate populations
by molecular means, and if otherwise not possible, by
consensus of color pattern variation.
Because some frequent color pattern variations
between Montivipera b. albizona and M. wagneri are
quite similar, taxon-allocation based on photographs of
specimens from proximate populations between them
presents some challenges. This convergence in color
pattern might be the result of similar environmental
pressure or gene ow in the past (Rajabizadeh et al.
2015), but with the knowledge that there is generally no
large sympatry between two Montivipera taxa (Stümpel
et al. 2016) save some narrow contact zones (Mebert
et al. 2016), we can at least approach the delimitations
or current separation between these Montivipera taxa
based on consensus in color pattern. Indeed, there are
two prominent topographic features producing a large
(up to 100 km) longitudinal gap with vast stretches of
unsuitable or qualitatively reduced habitat, potentially
separating the ranges of the two mountain viper taxa:
the huge Munzur-Mercan mountain ranges with a nearly
100 km stretch of > 2,700 m elevation along the border
between the provinces Erzincan and Tunceli and the
mighty Euphrates River with a hot-dry landscape of at
terrain or ne-sedimented hills and mountains < 1,000
m elevation reaching far inland from the river along the
border of Malatya and Elazığ provinces. This unsuitable
area is bordered in the south by the Malatya Mountain
range west of the Euphrates and includes locality-45
(Montivipera b. albizona) in Adiyaman Province. From
the eastern side of the Euphrates in southern Elazığ
(Hazar Mountains) and Diyarbakir (Maden Mountains)
provinces, we received credible, local reports of
mountain vipers with yellow dorsal blochtes resembling
Wagners Viper. These mountain ranges on both sides
of the Euphrates likely constitute the southern border
for regional mountain vipers, as a atter and lower arid
landscape continues from there southwards towards
Syria.
In respect to the Munzur Mountains, our current
information assigns all specimens without genetic data
from the western end of these mountains, Erzincan
Province, to M. b. albizona, and predict their presence
in the northwestern corner of Tunceli Province, with
only 25 km continuous habitat from nearby albizona
populations in Kabataş/Erzincan (localities-17 and -18),
but additional albizona vouchers have been conrmed
with genetic samples from nearby Erzincan and Sivas
localities (e.g., localities-20 and -23, Supplemental
Information Table S1). Regarding the occurrence of M.
b. albizona north of the Munzur Mountains, however,
only one shed skin of M. b. albizona has been reported
(locality-16; Mulder 1995). The nearest populations
of M. wagneri are found in the eastern part of Tunceli
Province (photo voucher of Hengirvan, locality-15, and
new specimen/molecular vouchers from 18 km distant
Tahkini Yaylasi, locality-14, Fig. 4, Supplemental
Information Table S1). These M. wagneri show virtually
no cyt b genetic divergence (0–2 mutations over 700bp)
to M. wagneri from 250 km farther east in Aras Valley,
Kars Province, whereas there are 13–15 mutations to
the currently nearest M. b. albizona 128 km farther west
at Sandik, locality-20. The distance would be reduced
to 78 km taking untested records between Hengirvan
and Ziyaret Tepesi, respectively, localities-15–16. It
becomes evident that the southern slopes and valleys
of the Munzur Mountains need to be evaluated for a
potential contact and/or transition zone between these
two Montivipera taxa.
Whereas the Munzur Mountains might act as a
potential topographic obstacle for exchange between
northern populations of Montivipera b. albizona and
M. wagneri, the Euphrates River is a potential barrier
between these vipers farther south. The Euphrates
River already ows through the Munzur Mountains
in Erzincan Province where it is remarkably narrow
and anked by a steep valley, though only the Blunt-
nosed Viper (Macrovipera lebetina) is known from its
hot and dry riparian area < 1,500 m elevation (unpubl.
data). Similarly, large portions of semi-arid southern
and central Tunceli Province including mountains up to
2,000 m elevation appear void of Montivipera spp., but
are inhabited by Macrovipera lebetina according to an
experienced national park ranger with more than 30 y of
province-wide service (Murat Özel, pers. comm.).
Farther south in Elazığ and Malatya provinces, the
Euphrates River system widens substantially. Beginning
at the northern end of the massive Keban Reservoir
Lake (ooded Euphrates Valley and tributaries), the
Euphrates River is anked by alluvial plains with ne
sediments on plateaus and gentle hills mostly < 1,100
m elevation, and leaving some rocky habitats in lower,
drier, and warmer climate (Barry 2008), a semi-arid
landscape that is less suitable for M. wagneri and M. b.
albizona, but rather preferred by the larger Macrovipera
lebetina, a potential competitor (Schätti et al. 1991).
This remains speculative, however, without further
eld investigations and local data, and as the recently
discovered contact zone between M. wagneri and M.
raddei exemplied, such taxon divisions do not need to
be accompanied by major landscape features (Mebert
et al. 2015a, 2016). Nonetheless, there are two regions
alongside the southern Euphrates River that potentially
provide conditions suitable for Montivipera populations:
between Keban and the Karakaya Reservoir Lake (40 km
river course), and the outow of this reservoir lake and
the northern end of the huge Bayat-Atatürk Reservoir
Lake, where the Euphrates River meanders through the
eastern portion of the Malatya and Adiyaman Mountain
182
Mebert et al.—Range and conservation aspects of Turkish mountain vipers.
ranges anked by steeper slopes and mountains >
1,000 m elevation, (e.g., see photographic vouchers
from localities-22 and -45 in Fig. 8 and Supplemental
Information Figs. S8, 13). These regions along the
Euphrates River and the adjacent southern versant of the
Munzur Mountains possibly constitute a non-continuous,
rst contact zone between Montivipera taxa. Indeed,
preliminary cyt b analysis (750bp) shows that northern
M. b. albizona from Sivas and Erzincan provinces show
less genetic distance to populations 150–250 km farther
south than to M. wagneri 130 km east across Euphrates
(Supplemental Information Table S1).
A second contact may exist between M. b.
bulgardaghica and M. b. albizona in Adana Province,
previously thought to be separated by ca. 160 km between
locality-48 at Elmali Bogazi (bulgardaghica) and
locality-40 at Başkonuş Plateau (albizona). The contact
zone is provisionally placed between the bulgardaghica-
like specimen from Göller/Adana (locality-46 and
Fig. 8A) and the more albizona-like specimens from
about 38 km farther east at Başkonuş Plateau and
Bostanli, Kahramanmaraṣ Province (localities-40 and
-41, Supplemental Information Figs. S7G, S10, S11).
This contact region has a low elevation, and thus less
suitable habitat leading to reduced gene ow, of mostly
< 1,000 m (red-hatched circle in Fig. 11), and begins at
the city of Osmaniye in the south, forming a western
border along Keşiş River north to Kadirli-Kesiksuyu
Reservoir-Çağlayan Deresi-Çiçeklidere-Bağdaş Yaylasi
(Y. = plateau) and Savrun Çayi (Ç. = river), and shows
an eastern border with a line following Osmaniye-
Aslantaş Reservoir Lake-Andirin-Köprüağzi Deresi. A
high mountain, Ağaca Dağ at about 2,200 m elevation,
borders this relatively lower region near the junction
of the provinces Kayseri, Adana, Kahramanmaraṣ,
and Osmaniye. The color pattern in south-eastern
Montivipera populations from Kahramanmaraṣ and
Adiyaman provinces show extreme variation, however,
with large- to small-blotched specimens, with spotted
to vertical-lined anks, with round to rectangular
blotches, often losing the light colored center posteriorly
and with irregularly-formed borders reminiscent of
bulgardaghica (Fig. 6 and Supplemental Information
Figs. S10–S13). This large color pattern variation in the
potential contact zone possibly reect an intergradation
between M. b. bulgardaghica and M. b. albizona, as it
can be expected between these two conspecic clades
(Stümpel et al. 2016); thus, the geographic transition
might be much larger and gradual between these taxa.
This is supported by an increasing genetic divergence
by distance. For example, beginning with typical M.
b. bulgardaghica at Kar Boğaz/Adana (locality-48),
there are ve mutations across 150 km east to M. b.
albizona at Bostanli/Kahramanmaras (locality-41), but
eight mutations across 360 km east to M. b. albizona at
Adiyaman (locality-45). Yet, many more samples from
the entire region are required to elucidate the genetic
character of any contact or transition zone.
New information points to a third contact zone
that exists between Montivipera xanthina and M.
bulgardaghica in Erdemli district, Mersin Province.
Previously published data showed a shortest distance
of 150 km between these mountain vipers species, i.e.
between type locality-53 of bulgardaghica (Nilson and
Andren 1985) at Bolkar Daği, border Niğde-Mersin
provinces, to the xanthina-locality-63 at Erciyes
Mountain, Kayseri Province (Nilson et al. 1988). A
consensus of cyt b data (Supplemental Information Table
S1) and/or color pattern reduces the distance between
the western-most M. b. bulgardaghica at Gavuruçtuğu
(locality-62) to M. xanthina near Akpinar to 16 km
(locality-71, Fig. 10E) and 11 km near Kuşluca (only
xanthina color pattern, locality-70, Fig. 10C, D). The
habitat between these localities consists of continuous
rock formation along high-elevation plateaus and
southern versants of the Bolkar Mountains with two
north-south valleys passing through Toros and Sungur
at primarily > 1,400 m elevation, that may represent the
contact zone.
In summary, the distances between the distribution
areas of the different Montivipera taxa discussed herein
have been reduced dramatically: between Montivipera
wagneri and M. b. albizona from 280 km down to 78 km;
between M. b. albizona and M. b. bulgardaghica from
160 km down to 38 km and for M. b. bulgardaghica and
M. xanthina from about 150 km down to 11 km. Yet, for
all the suggested contact zones or region of proximate
populations, vouchers are missing to pinpoint precise
areas of species delimitation or contact zones between
these clades. Hence, much sampling, in particular
for molecular data, is still needed for a ne-scaled
phylogeographic analysis of these mountain vipers.
Conclusion.—This study revealed dramatic changes
in the distribution of central-eastern Anatolian mountain
vipers compared to what was ofcially perceived for
decades by published and governmental information.
With many new localities, but also rened-published
(improved precision) ones, and increased habitat
variation shown in gures and/or described for some
localities in Supplemental Information, it becomes
obvious that all four Montivipera taxa treated herein
have not only much greater ranges but also larger
population sizes. This updated information will have
effects on the conservation statuses and facilitate new
and more realistic assessments for the IUCN Red List
of Threatened Species (IUCN 2020), including the shift
of perceived threats from overcollection to overgrazing.
The results from this paper will help to locate
proximate or parapatric populations or even nd contact
183
Herpetological Conservation and Biology
zones between two Montivpera taxa. Consequently,
we hope to stimulate new studies to investigate
gene ow across species ranges and test for species
integrity and relevant environmental correlates that
could be incorporated into effective conservation
measurements and specic action plans. Finally, we
urge the conservation and scientic community to
seek collaborative work with Turkish authorities and
researchers, raise public awareness and understanding,
and thus improve tools for the conservation of these
valuable species and their habitat as national treasures.
Acknowledgments.—We dedicate this article to
our beloved and esteemed co-author, contributor
and collaborator, Dr. Bayram Göçmen, who passed
away during the nal steps of this study. Field work
permits focusing on vipers (permission numbers 20210,
183897 and 101792) were issued by the Republic of
Turkey Ministry of Agriculture and Forestry, General
Directorate of Nature Conservation and National
Parks. This work was partly supported by the Wilhelm
Peters Fund 2013 administered by the main body of the
German Herpetological Society, respectively, Deutsche
Gesellschaft für Herpetologie und Terrarienkunde
(DGHT), and also DGHT-Zürich, Switzerland, the
JCE private funding, and in particular the Mohamed
bin Zayed Species Conservation Fund, project nos.
13057971 (2014), 150510677 (2015), 160513040
(2016), 170516395 (2017/18). The authors thank
Şevket Gültekin, Adem Adakul, Mücahit Çakmak,
Çağatay Altin, Mehmet Akif Bozkurt, Burhan Sarikaya,
Thomas Ott, Murat Özel, Mert Elverici, Mahmut
Aydoğdu, Özer Camci, and Osman Özkan for their
assistance during our eld surveys. We also thank all
the persons providing valuable material, such as photos
and locality information, which are explicitly named for
their respective provisions in the locality list and gures.
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187
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konraD Mebert is an independent researcher and International Project Coordinator based in
Switzerland, conducting studies globally on amphibians and reptiles with an emphasis on vipers.
After completing a Master's degree at the University of Zürich, Switzerland, on geographic variation
and the effects of inbreeding on the Dice Snake (Natrix tessellata), and a doctoral degree on hybrid
zones in North American watersnakes (Nerodia fasciata and N. sipedon) at Old Dominion University,
Norfolk, Virginia, he currently is associated with the State University of Santa Cruz, Ilhéus,
Bahia, Brazil, and the Institute of Development, Ecology, Conservation and Cooperation (IDECC) in
Rome, Italy. His work volume produced more than 130 professional and popular publications/reports
and two books on water snakes including topics on evolution, ecology, biodiversity and conservation.
Many expeditions and a passion for photography has led him to all relevant continents. Current
(2020) principal study sites are located in Turkey, Panama, Ecuador, Brazil, Slovenia, Italy, Georgia,
and China. (Photographed by Marco Sassoe).
Naşit İğci obtained his B.Sc. degree in zoology from Ege University Department of Biology, Izmir,
Turkey, in 2008. He received his M.Sc. and Ph.D. from Ankara University Biotechnology Institute,
Turkey, in 2009 and 2015, respectively, and is currently an Associate Professor in Nevşehir Haci
Bektaş Veli University Department of Molecular Biology and Genetics, Nevşehir, Turkey, since
2016. His research includes biochemistry and pharmacology of snake venoms, and the ecology
and systematics of amphibians and reptiles of Turkey. He worked as a reptile specialist in several
projects related to biodiversity monitoring and conservation supported by the Government of Turkey.
(Photographed by Konrad Mebert).
Mert Kariş is a Lecturer at the Acigöl Vocational High School of Technical Sciences, Nevşehir
Haci Bektaş Veli University, Cappadocia, Turkey. He received his Zoology B.Sc. degree from the
Department of Biology, Faculty of Science, Ege University, Izmir, and M.Sc. and Ph.D. degrees in
Biology/Zoology from the Institute of Natural and Applied Sciences, Ege University, Izmir, Turkey.
His research focuses on systematics (taxonomy), ecology and diversity of amphibians and reptiles
of Turkey. He also works on biochemical and pharmacological properties of snake venoms and
amphibian skin secretions. (Photographed by Kürşat Bal).
MeHMet Zülfü yilDiZ is an Associate Professor at the Department of Biology in Adiyaman
University (Turkey) and has extensive experience of east and southeast Anatolia. He received his
university education at Harran University in Şanliurfa (B.S. and M.S. degrees) and Ege University in
İzmir, Turkey. His interests cover biodiversity, ecology, systematics, molecular phylogeny of reptile
and amphibians, and venom studies of vipers. Mehmet contributes regularly to the Amphibians and
Reptiles Monitoring & Photography Society in Turkey. He has authored or co-authored over 40 peer-
reviewed papers on herpetology and is editor for Biharean Biologist, Commagene Journal of Biology,
and Acta Biologica Turcica. (Photographed by Konrad Mebert).
... HerpNet, n = 10), and scientific publications (n = 143). Particularly, the study by Mebert et al. [55] has noticeably provided improved distribution data of the Montivipera of central-eastern Anatolia. Overall, we obtained 320 presence points covering the entire distribution of mountain vipers' (Fig. 1) and ranging from 12 occurrences for M. kuhrangica to 51 localities for M. albizona. ...
Article
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Background The orogeny of the eastern Mediterranean region has substantially affected ecological speciation patterns, particularly of mountain-dwelling species. Mountain vipers of the genus Montivipera are among the paramount examples of Mediterranean neo-endemism, with restricted ranges in the mountains of Anatolia, the Levant, Caucasus, Alborz, and Zagros. Here we explore the phylogenetic and ecological diversification of Montivipera to reconstruct its ecological niche evolution and biogeographic history. Using 177 sequences of three mitochondrial genes, a dated molecular phylogeny of mountain vipers was reconstructed. Based on 320 occurrence points within the entire range of the genus and six climatic variables, ecological niches were modelled and used to infer ancestral niche occupancy. In addition, the biogeographic history and ancestral states of the species were reconstructed across climate gradients. Results Dated phylogenetic reconstruction revealed that the ancestor of mountain vipers split into two major clades at around 12.18 Mya followed by multiple vicariance events due to rapid orogeny. Montivipera colonised coastal regions from a mountain-dwelling ancestor. We detected a highly complex ecological niche evolution of mountain vipers to temperature seasonality, a variable that also showed a strong phylogenetic signal and high contribution in niche occupation. Conclusion Raising mountain belts in the Eastern Mediterranean region and subsequent remarkable changes in temperature seasonality have led to the formation of important centres of diversification and endemism in this biodiversity hotspot. High rates of niche conservatism, low genetic diversity, and segregation of ranges into the endemic distribution negatively influenced the adaptive capacity of mountain vipers. We suggest that these species should be considered as evolutionary significant units and priority species for conservation in Mediterranean mountain ecosystems.
... In brief, distributional ranges were constructed (at a resolution of 10′) taking into account distinct sources, such as International Union for Conservation of Nature distribution polygons, maps and occurrences from publications (e.g. Ursenbacher et al., 2008;Martínez-Freiría et al., 2017;Freitas et al., 2018;Mebert et al., 2020), or occurrences from public databases (e.g. Global Biodiversity Information Facility, www.gbif.org). ...
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... edlis t.org/) and publications (e.g. [44][45][46], and occurrences obtained from public databases (e.g. Global Biodiversity Information Facility, https ://www. ...
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... This applies even to introns and other fast-evolving single copy nuclear genes (e.g., NT3, PRLR, Townsend et al., 2008). Consequently, other molecular approaches such as even faster evolving markers (e.g., Kindler and Fritz, 2018;Pöschel et al., 2018), phylogenomic methods (e.g., Blair et al., 2019;Heinicke et al., 2018), and increased sampling to evaluate current or past gene flow between most-proximate populations or contact zones of two or more closely related species (Mebert, 2008(Mebert, , 2015a(Mebert, , b, 2020Hillis, 2019) should be favoured to infer evolutionary histories and resolve species limits among these taxa. ...
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