Dorsal colour pattern variation in Eurasian mountain vipers (genus

Zoologischer Anzeiger 257 (2015) 1–9
Contents lists available at ScienceDirect
Zoologischer Anzeiger
journal homepage: www.elsevier.com/locate/jcz
Dorsal colour pattern variation in Eurasian mountain vipers (genus
Montivipera): A trade-off between thermoregulation and crypsis
Mahdi Rajabizadeh a,b,c,∗ , Dominique Adriaens a , Mohammad Kaboli d , Jaleh Sarafraz e ,
Mohsen Ahmadi d
a
Evolutionary Morphology of Vertebrates, Ghent University, Ghent, Belgium
Department of Biodiversity, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology,
Kerman, Iran
c
Iranian Plateau Herpetology Research Group (IPHRG), Faculty of Science, Razi University, 6714967346 Kermanshah, Iran
d
Department of Fishery and Environment, Faculty of Natural Resources, Tehran University, Tehran, Iran
e
Marine Biology Section, Department of Biology, Ghent University, Ghent, Belgium
b
a r t i c l e
i n f o
Article history:
Received 21 August 2014
Received in revised form 12 March 2015
Accepted 19 March 2015
Available online 4 April 2015
Keywords:
Crypsis
Colour
Pattern
Montivipera
Thermoregulation
a b s t r a c t
Reptile colouration has long been studied as an example of adaptive evolution. Several functions have
been proposed for variety of snake colour and pattern with the most common suggestions being camouflage, aposematism and thermoregulation. Montivipera raddei species complex shows a remarkable
variation in dorsal colour pattern, but so far there has not been a comprehensive study performed on
the adaptive nature of their colour pattern. The dorsal colour pattern of 111 specimens belonging to the
M. raddei species complex, originating from 23 localities across its distribution range, were studied to
explore intra and interspecific variation in the colour pattern. A generalized linear model analysis showed
that there is a significant relationship between the dorsal colour pattern of Montivipera latifii, Montivipera
raddei raddei and Montivipera raddei albicornuta, and the environmental factors of the habitat, including
elevation, average annual temperature, average annual solar radiation, average annual precipitation, vegetation type and substrate colour. The results suggest that the dorsal colour pattern variation in the M.
raddei species complex is affected by a complex trade-off between thermoregulation and crypsis.
© 2015 Elsevier GmbH. All rights reserved.
1. Introduction
Several functions have been proposed for understanding the
variety of snake colour and pattern, with the most common suggestions being camouflage, aposematism and thermoregulation (see
Allen et al., 2013). Among visual effects, crypsis may represent
the major function (and hence selective pressure) explaining the
adaptive nature of colour pattern variation (Vincent, 1982). There
are numerous examples of cryptic colour and pattern in reptiles
(Brodie, 1992; King, 1992; Shine and Harlow, 1998; Wilson et al.,
2006; Farallo and Forstner, 2012; Isaac and Gregory, 2013). Aposematism, the use of bright colours and patterns by noxious animals
to deter predators, is documented in reptiles too (Campbell and
Lamar, 1989; Savage and Slowinski, 1992; Brodie, 1993; Brodie and
∗ Corresponding author at: Ghent University, Evolutionary Morphology of Vertebrates & Zoology Museum, K L Ledeganckstraat 35, B-9000 Gent, Belgium.
Tel.: +98 9388288177.
E-mail address: [email protected] (M. Rajabizadeh).
http://dx.doi.org/10.1016/j.jcz.2015.03.006
0044-5231/© 2015 Elsevier GmbH. All rights reserved.
Janzen, 1995; Valkonen et al., 2011). There are indications that in
ectotherms, colour and thermal physiology are co-adapted, meaning that dark individuals with a lower skin reflectance are at an
advantage under conditions of low temperature thermoregulation
(Gibson and Falls, 1979; Peterson et al., 1993; Lawson and King,
1996; Bittner et al., 2002; Clusella-Trullas et al., 2007, 2009).
The Montivipera raddei species complex (MRC) is a group of
diurnal mountain dwelling vipers, distributed across north, northwestern and western Iran, southern half of Armenia, south of
Azerbaijan, Nakhijavan and adjacent places in eastern Turkey.
(Nilson and Andrén, 1986; Stümpel and Joger, 2009; Stümpel,
2012). These vipers show the typical viper’s zigzag pattern on their
dorsum, in contrast with a dorsal ground colour. The MRC shows
a remarkable variation in dorsal colour pattern, changing from a
light dorsal pattern over a dark ground colour, to a dark pattern
over a light ground colour. There is also variation in the shape of
this dorsal pattern.
In taxonomic studies of the MRC (e.g. Nilson and Andrén, 1986)
dorsal colour and pattern have been used as important key characters in distinguishing MRC species. Although variation in colour
2
M. Rajabizadeh et al. / Zoologischer Anzeiger 257 (2015) 1–9
Fig. 1. Different populations of the Montivipera raddei species complex and their colour pattern. 1: Montivipera latifii in the central Alborz (D and E), 2: Montivipera raddei
albicornuta in the Zanjan valley (F), 3: populations of Montivipera raddei raddei in the Iran and Turkey bordering mountains in the northwestern Iran and adjacent countries
(referred to NW) (A and B), 4: populations of Montivipera raddei raddei in the isolated mountains in the northwestern Iran (Sahand, Sabalan, Kordestan and Tekab mountains,
briefly referred to SSTK) (C), 5: Montivipera kuhrangica in the central Zagros. Blue markings represent potential distribution of the Montivipera raddei species complex,
generated using Maxent modeling software (M. Yousefi, in lit. 2014). Photos A, B, C and E were taken by M. Rajabizadeh; D was taken by R. Behruz; F was taken by M. Kaboli.
pattern in populations of the MRC could reflect an underlying
level of biodiversity within this group, but reptile colouration has
long been studied as an example of adaptive evolution (e.g. Cott,
1940; Rosenblum et al., 2004). So far there has not been a comprehensive study performed on the adaptive nature of intra- and
inter-population variation in colour pattern of the MRC.
In this paper, we tried to explore to what degree the observed
variation in MRC’s colour pattern could be linked to specific
environmental factors. Answering this question could also reveal
whether colour pattern in the MRC reflects an adaptation to local
environmental conditions.
2. Materials and methods
2.1. Taxonomy and distribution of the Montivipera raddei
species complex
Following Rajabizadeh (2013) small sized species of the MRC
(maximum length 99 cm) consist of four taxa: Montivipera latifii
(Mertens, Darevsky and Klemmer, 1967), Montivipera kuhrangica (Rajabizadeh et al., 2011), Montivipera raddei raddei (Boettger,
1890) and Montivipera raddei albicornuta (Nilson and Andrén,
1985). To look into the colour pattern variation across the MRC,
the dorsal colour pattern in 52 M. raddei raddei, 28 M. raddei albicornuta, 29 M. latifii and two M. kuhrangica from 23 localities across
the distribution range of this species complex were studied (Fig. 1,
Appendices A–C). In summary, the taxonomy, distribution and dorsal colour pattern of the MRC are as follows:
over a light brown or tan dorsal ground colour. A distinct character
of this species is a high level of colour polymorphism in its dorsal
pattern. So far, four different patterns have been identified in M. latifii (Fig. 1D and E, see also Mertens et al., 1967; Nilson and Andrén,
1986; Rajabizadeh et al., 2012).
2.1.2. Montivipera raddei albicornuta
This subspecies inhabits the Zanjan valley (Fig. 1 and Appendix
A). The dorsal ground colour is grey, light grey, greyish brown or
light brown, with a brown or olive (rarely black), black bordered,
zigzag band along the back (Fig. 1F).
2.1.3. Montivipera raddei raddei
This subspecies is distributed across easternmost Turkey, northwestern Iran, Naxcivan, southern Armenia and the adjacent area in
the Azerbaijan Republic (Fig. 1 and Appendix A). It has a blackish,
dark grey, light grey or light brown dorsal ground colour. The dorsal
pattern can be a narrow or broad zigzag band, consists of orange to
yellow, often round blotches that sometimes, and especially on the
lateral side, form a dark edge (Fig. 1A–C).
2.1.4. Montivipera kuhrangica
Only three specimens were reported from a small area in the
central Zagros mountains. The colour and pattern of this species is
similar to that of M. raddei albicornuta (Rajabizadeh et al., 2011).
Supplementry material related to this article found, in the online
version, at http://dx.doi.org/10.1016/j.jcz.2015.03.006.
2.2. Colour pattern data
2.1.1. Montivipera latifii
Current knowledge on the distribution of M. latifii suggests that
this species is restricted to a small area in the central Alborz mountain range (Fig. 1 and Appendix A). It has a brown dorsal pattern
Colour pattern data collected from live specimens were
observed in the field, freshly killed specimens (i.e. road kills), freshly
preserved specimens from museum collections and high quality
M. Rajabizadeh et al. / Zoologischer Anzeiger 257 (2015) 1–9
3
Table 1
Result of ANOVA showing the relationship between the variation of viper’s colour pattern and the variation of normally distributed environmental data. (DGC): dorsal ground
colour, (DPC): dorsal pattern colour and (DPS): shapes of the dorsal pattern.
DGC
Elevation
Temperature
Solar Radiation
Precipitation
DPC
DPS
Sum of squares
df
F
Sig.
Sum of squares
df
F
Sig.
Sum of squares
df
F
Sig.
7375482.67
62.39
830712.68
890807.41
2
2
2
2
39.86
49.42
51.85
101.12
0.00
0.00
0.00
0.00
9150526.73
55.35
939177.95
991922.90
2
2
2
2
60.38
39.66
67.40
143.73
0.00
0.00
0.00
0.00
5690596
51.66132
431038.9
722371.1
2
2
2
2
26.25
35.26
18.18
60.26
0.00
0.00
0.00
0.00
pictures, since 2009. Since preserving solutions (i.e. methanol or
chloroform) could impact the colour of the preserved viper specimens, colour data of older preserved specimens were not taken into
account. To avoid age effect (personal observation) in the analysis,
only adult specimens (defined as specimens with snout-vent length
above 500 mm) were examined. Since these vipers are darker than
usual during shedding, colour data of near to shedding specimens
was not considered. Also, because no sexual dimorphism in the dorsal colour have been observed in the MRC (see Nilson and Andrén,
1986), and we did not observe a visible intersexual difference in the
colour pattern, the colour pattern data of both sexes were pooled
in the analysis.
For studying the colour pattern variation in the M. raddei
raddei species complex, the dorsal ground colour (DGC), dorsal
pattern colour (DPC) and dorsal pattern shape (DPS) were documented. To carry out the statistical relationship analysis linked
to environmental conditions, the dorsal ground colour was classified into light, medium and dark categories. To standardize the
colour names, the X11 colour name system was used (available at
http://en.wikipedia.org/wiki/X11 colour names). In this standard
colour naming system, light dorsal ground colour refers to tonalities of tan colour. Dark dorsal ground colour refers to tonalities of
grey, dark grey, cool grey, blackish, as well as greyish brown and
greyish olive. Medium dorsal ground colour refers to light grey,
brown and olive colour. Also the shape of the dorsal blotches was
classified in two types: roundish and triangular (Table 1).
pastures in north and northwestern Iran (characterized by predominant vegetation of cushion shaped bushes, including the genera
Astragalus and Acanthophyllum).
To facilitate the analysis of substrate data, the predominant colour of substrate stones in the habitat was regarded as
the substrate’s colour. We had observed that in high elevation
mountain habitats, with the presence of the MRC, the habitat is
covered by stony outcrops, gravel fields and sandy soil admixed
with differently sized rubble. Because the colour and composition of gravel fields and sandy soils are strongly related to
the colour of parent stones, we used the predominant colour
of substrate stones, as the substrate’s colour. Petrologic data
were extracted from geology maps of Iran (www.ngdir.com),
Turkey (http://www.mta.gov.tr/v2.0/eng/maps.php), Armenia
(http://www.lydianinternational.co.uk/editorimages/documents/
GeologicalMapArmenia.pdf) and Azerbaijan (http://www.azenerji.
com/en/powersystem/maps/geologicalmap.jpg). These stones
were categorized in three colour types (light, medium and dark),
based on the petrologic references and field data. In summary,
dark stones were defined as stones similar in colour or darker
than ophiolite or andesite basalt rocks. Light coloured stones were
defined as stones similar in colour or lighter than tuff stones or
limestone. Medium-coloured stones were separated as all other
stones between dark and light categories, i.e. andesite stones
(Appendix E).
Supplementry material related to this article found, in the online
version, at http://dx.doi.org/10.1016/j.jcz.2015.03.006.
2.3. Environmental factors
2.4. Analysis
To investigate the relationship between colour pattern variation
in the MRC and environmental factors, one biotic factor (vegetation)
and six abiotic factors (elevation, temperature, solar radiation, precipitation and substrate colour), all of which have been proven to
be linked to reptile colour pattern variation, were included in the
analysis.
Vipers of MRC exhibit a diurnal and seasonal movement pattern (Darevsky, 1966; Ettling et al., 2013). Since their minimum
home range for a complete season is 32.3 ha ± 13.8 for males and
18.8 ha ± 4.7 for females (Ettling et al., 2013), we considered the
average of environmental data from 100 ha (1 km2 ) around each
viper’s locality. Data of elevation were extracted from Shuttle
Radar Topography Mission elevation model with cell size of 1 km2 .
Temperature and precipitation data of each viper’s locality were
extracted from the annual mean temperature and annual mean precipitation data, provided by WorldClim (version 1.4, see Hijmans
et al., 2005) with a cell size of 1 km2 . Solar radiation data were generated from annual mean temperature data, using ArcGIS (version
9.3) solar radiation extension, depicting total amount of incoming
solar radiation (WH/m2 year, see Appendix D).
Supplementry material related to this article found, in the online
version, at http://dx.doi.org/10.1016/j.jcz.2015.03.006.
For each viper’s locality, vegetation data was documented. As
the MRC inhabits mountainous pastures or forests with more than
50% density of vegetation, only the vegetation type was considered, grouped in two categories: tree vegetation, referring to forest
or shiblik vegetation, and bush vegetation, referring to mountain
To evaluate the relationship between the viper’s colour pattern and environmental factors, an analysis of variance (ANOVA)
was performed for normally distributed environmental data (elevation, temperature, solar radiation and precipitation) and a
Kruskall–Wallis test was used for categorical data (type of vegetation and substrate colour). If an analysis was significant,
we performed a LSD post-hoc individual one-way ANOVA test
for normally distributed environmental data, and a pairwise
Kruskall–Wallis test for categorical data to determine which factors
were significantly related.
Also, the relationship between viper colour pattern variation
and variation of environmental factors were analysed by employing a generalized lineal model (GLM), using the three colour pattern
variables as dependent (each by each in three different models)
and including elevation, temperature, solar radiation, precipitation, vegetation and substrate colour as independent variables.
The generalized linear model was corrected for dispersion under
a Poisson distribution with a log link function with the variation of
viper colour pattern and environmental factors disturbances as the
response variables.
For a better schematic presentation of the colour pattern and
environmental factors variation across the populations of the MRC,
with respect to the populations of the M. latifii in the central Alborz
and M. raddei albicornuta in the Zanjan valley, populations of the
M. raddei raddei were split into two eastern and western groups.
Populations in Iran and Turkey bordering mountains and adjacent
4
M. Rajabizadeh et al. / Zoologischer Anzeiger 257 (2015) 1–9
countries were referred to NW and populations in the isolated
mountains in the northwestern Iran (Sahand, Sabalan, Kordestan
and Tekab Mountain) referred to SSTK (Fig. 1). M. kuhrangica
was excluded from the statistical analysis because of the low
number of samples (two specimens). Analyses were performed
using SPSS (version 15) statistical software. Pie charts were generated using GraphPad Prism (version 6.05) GraphPad Software
(www.graphpad.com).
Table 3
Generalize linear model analysis on three colour pattern variables as dependent and
an interaction of environmental factors as model: Elevation * Temperature * Solar
Radiation * Precipitation * Vegetation Type * Stone Color. AICc: akaiki information
criteria corrected for small sample size.
DGC
DPC
DPS
Pearson chi-square
Log likelihood
AICc
df
Sig.
4.902597
4.51
5.69
−144.763
−136.09
−131.68
345.5741
328.23
319.41
7
5
9
0.00
0.00
0.00
3. Results
Studying the frequency of DPC, DPS and DGC in the MRC populations revealed, that specimens of the M. latifii had a dark and
mainly triangular dorsal pattern, but rarely a mainly light dorsal
ground colour (Fig. 2). At the localities of the Zanjan valley, M. raddei albicornuta had mainly darker dorsal ground colour and lighter
dorsal pattern colour than M. latifii colour patterns (Fig. 2). Populations of the M. raddei raddei in the Iran and Turkey neighbouring
mountains and adjacent countries (NW) had mainly darker dorsal
ground colour and lighter dorsal pattern colour than both the M.
raddei albicornuta colour pattern and M. latifii colour pattern, and
mostly had a roundish shape in their dorsal pattern. M. raddei raddei
in the isolated mountains in the northwestern Iran (SSTK) had both
colour and pattern of M. raddei albicornuta of the Zanjan valley and
M. raddei raddei in the bordering mountains and adjacent countries
of Iran and Turkey (Fig. 2).
In habitats of the MRC in the central Alborz towards the Zanjan
valley and northwestern Iran, generally the elevation, temperature and solar radiation decreased, the precipitation increased. The
pasture vegetation change towards tree vegetation and the predominant medium and light colour stones in the habitat changed
to medium and dark colour stones (Figs. 3 and 4).
There is a significant relationship between the variation of dorsal
pattern colour (DPC), dorsal ground colour (DGC) and shapes of the
dorsal pattern (DPS) of MRC species and the variation of environmental factors including elevation, average annual temperature,
average annual solar radiation and average annual precipitation
(Table 1). The variation of DPC, DGC and DPS in MRC species and
variation of substrate colour and vegetation type in MRC habitat
were significantly interrelated (Table 2). Pairwise analysis revealed
that the variation of all the categories within DGC, DPC and DPS
were significantly related to the variation of environmental factors, except that no significant relation was established between
the variation of colour traits in M. latifii and M. raddei albicornuta, in
relation to variation of vegetation type. No significant relation was
observed between the variation of DPS in M. latifii and M. raddei
albicornuta, in relation to stone colour variation.
Generalized linear model analysis revealed that variation of
colour pattern variables were significantly related to the interaction between elevation, temperature, solar radiation, precipitation,
vegetation and substrate colour of the viper habitat (Table 3).
4. Discussion
The variation of dorsal ground colour (and subsequently dorsal
pattern colour) in the species of the M. raddei complex is related to
the variation of thermal factors, including temperature and solar
radiation. In the MRC distribution range, compared to M. latifii in
the central Alborz, M. raddei raddei occupied a habitat located in
the higher latitudes that is colder and gets lower solar radiation
than central Alborz habitats. The influence of latitude is a major
factor that affect the surface air temperature and solar radiation
(see Fisher, 1986; Fan and Van den Dool, 2008). Darker colouration of the M. raddei raddei allows them to take more advantage of
thermoregulation and radiation absorption, than the lighter M. latifii. A dark colouration in reptiles improves heat absorption over a
shorter time (rapid heat absorption, but see Gibson and Falls, 1979;
Pough et al., 1998; Lawson and King, 1996; Bittner et al., 2002;
Clusella-Trullas et al., 2007, 2009; Norris and Kunz, 2012).
Colour patterns within the M. raddei complex revealed relationships to the predominant colour of substrate stones in the habitats.
The light dorsal ground colour of M. latifii in the central Alborz
mountains is cryptic over the predominant light colour stones in
its habitat. These light stones are mainly consisting of tuffaceous
stones, which are characteristic of old volcanic activities in the
Alborz mountains (Davidson et al., 2004). In the localities of the
M. raddei raddei in the Northwestern Iran and adjacent areas, the
dark ground colour of M. raddei raddei specimens is cryptic over the
predominant dark colour stones. Since the Northwestern Iran localities are close to the closure suture of Tethys Sea ophiolite stones
of the Tethys sea basin and basalt stones of the volcanic activities around the closure suture, are the predominant stones of these
mountainous habitats (see Rögl, 1999).
There are examples of relationships between reptile colour patterns and substrate colour (e.g. Vincent, 1982; Stuart-Fox et al.,
2004; McGaugh, 2008; Micheletti et al., 2012; Farallo and Forstner,
2012). Cryptic colour patterns may help to avoid detection by
predators (Farallo and Forstner, 2012) and by prey (Götmark, 1987).
Although there is some evidence of disruptive colouration function
of the viper zigzag patterns (Edmunds, 1974; Shine and Harlow,
1998), it has been shown that even vipers with an aposematic
colour pattern (see Andrén and Nilson 1981; Forsman, 1995; Lindell
and Forsman, 1996; Wüster et al., 2004; Niskanen and Mappes,
2005; Valkonen et al., 2011; Santos et al., 2014) can appear cryptic against their natural background from a distance (Sherratt and
Beatty 2003; Tullberg et al., 2005). Vipers of the MRC are associated with habitat rocks and during the onset of spring and autumn,
the snakes are mostly observed close to their hibernation sites
between stony outcrops (see Darevsky, 1966; Behruz, 2010). MRC
populations can take advantage from the cryptic colouration, which
resulted from the association between the dorsal ground colour and
the predominant colour of substrate rocks in the habitat. Selective
pressure on the background matching (for a definition, see Stevens
and Merilaita, 2011) resulting from predation pressure, reduce the
Table 2
Result of Kruskall–Wallis analysis showing the relationship between the variation of viper’s colour pattern and the variation of vegetation type and substrate colour categories.
(DPC): dorsal pattern colour, (DGC): dorsal ground colour and (DPS): shapes of the dorsal pattern.
DGC
Vegetation type
Stone Color
DPC
DPS
Chi-square
df
Sig.
Chi-square
df
Sig.
Chi-square
df
Sig.
49.59
58.56
2
2
0.00
0.00
63.63
52.15
2
2
0.00
0.00
60.59
47.39
2
2
0.00
0.00
M. Rajabizadeh et al. / Zoologischer Anzeiger 257 (2015) 1–9
5
Fig. 2. Frequency of the different dorsal colour pattern in the Montivipera raddei species complex and populations.)A): Shapes of the dorsal pattern (DPS), (B): dorsal pattern
colour (DPC) and (C): dorsal ground colour (DGC). Number of examined specimens has been presented in the parentheses.
6
M. Rajabizadeh et al. / Zoologischer Anzeiger 257 (2015) 1–9
Fig. 3. Variation of climatic factors across the habitat of examine specimens of the Montivipera raddei species complex. (A): Elevation, (B): Solar Radiation, (C): Temperature,
(D): Precipitation. The boxplot use the median and 25% quartiles for ends of the box. The lines (or whiskers) extended to the minimum and maximum values within 1.5 times
the spread beyond the quartiles. Number of examined specimens has been presented in the parentheses.
contrast between the substrate’s dominant colour and snake colour
and patterns (Farallo and Forstner, 2012).
The relationship between colour patterns in the species of the
M. raddei complex and vegetation type can have a cryptic function.
Dark colouration in M. raddei raddei which occurs in forested habitats favours crypsis in the cover of trees in contrast to snakes in the
Central Alborz, where bush vegetation offer only limited cover. The
light colouration of M. latifii serves mainly as a cryptic colouration
over the substrate colour. Differences in the habitat sun exposure,
resulting from differences in vegetation type, can affect crypsis as
well (see Kark and Werner, 1993; Macedonia, 2001).
Various environmental factors that are associated with the
colour pattern variation in the MRC include thermal factors, vegetation type and the predominant colour of substrate stones in
the habitat. In summary our results suggest that dorsal colour
pattern variation in the MRC may be the result of a complex tradeoff between thermoregulation and crypsis. This trade-off between
melanistic vs. natural colour pattern is well documented for several snake species (e.g. Gibson and Falls, 1979; Andrén and Nilson,
1981; Lawson and King, 1996; Bittner et al., 2002; Castella et al.,
2013). Although M. raddei raddei takes advantage of its dark ground
colour in terms of crypsis and thermoregulation. However in M.
latifii, selection prefers the light dorsal ground colour that appears
cryptic in light substrates, despite it is not aiding thermoregulation. A pale colouration of ectothermic organisms, such as snakes
is expected to help primarily during unstable weather conditions
such as in early spring when high body temperatures are difficult
to achieve and maintain (e.g. Gibson and Falls, 1988). Recent findings support the hypothesis that thermal physiology and behaviour
are co-adapted (Clusella-Trullas et al., 2007), enabling reptiles to
adjust their behaviour to the thermal condition of the habitat in
order to achieve optimum body temperatures (e.g. Adolph, 1990;
Peterson et al., 1993). It is known that M. raddei raddei leave their
hibernation sites in early spring and start courtship activities at the
end of April or beginning of May (Terent év and Chernov, 1965).
Courtship of M. latifii starts at warmer weather at about the second
half of June (Andrén and Nilson, 1979). Since M. latifii has a pale
colouration in comparison to M. raddei raddei, reproductive activities in late spring may help M. latifii to easily achieve its optimum
body temperature.
Our study confirms previous observations (e.g. Nilson and
Andrén, 1986) that dorsal ground colour and dorsal pattern in
M. Rajabizadeh et al. / Zoologischer Anzeiger 257 (2015) 1–9
7
Fig. 4. Variation of rock colouration (A) and vegetation structure (B) across the habitat of examine specimens of the Montivipera raddei species complex. Number of examined
specimens has been presented in the parentheses.
8
M. Rajabizadeh et al. / Zoologischer Anzeiger 257 (2015) 1–9
Fig. 5. Phylogenetic distribution of different colour pattern morphs in the Montivipera raddei species complex. The figure shows variation of the colour pattern, parallel to
dispersal of the Montivipera raddei species complex into central Alborz and in the direction of the northwestern Iran and adjacent area in Armenia and Turkey. Figure shows
that dorsal colour pattern of Montivipera raddei populations in Sahand, Sabalan, Kordestan and Tekab mountain, referred to SSTK is a combination of both colour patterns of
M. raddei albicornuta of the Zanjan valley and M. raddei raddei of northwestern Iran and adjacent area. Schematic pictures, light, medium and dark dorsal ground colour and
dorsal pattern colour are presented as white, grey and dark grey colour. Also, variation of the shape of dorsal pattern is presented similar to natural pattern. Dorsal ground
colour, dorsal pattern colour and the shape of dorsal pattern agree with data of Table 1. Phylogenetic tree modified from ‘Stümpel (2012)’. For the map legends, see Fig. 1.
the MRC are mainly in contrasting colour with each other. Colour
patterns represent a balance between the need for signalling (e.g.
aposematic signalling) and the need for crypsis to avoid predation
(Stuart-Fox et al., 2004). Hence, although dorsal ground colour in
the MRC have thermoregulatory or cryptic functions, dorsal blotch
colour serves as a contrasting colour in combination with a dorsal
ground colour to keep a signalling function.
In a phylogenetic context (following Stümpel, 2012), populations of M. raddei ssp. form a monophyletic lineage, showing
different local adaptation and trade-offs with environmental factors leading to different colour pattern morphs (Fig. 5).
The occurrence of both colour pattern morphs of M. raddei
albicornuta and M. raddei raddei, within populations of the SSTK
mountains (Fig. 1) is not accompanied by occurrence of both environmental condition of the Northwestern Iran and the Zanjan valley
in the SSTK mountains. We hypothesize that the observed diversity within the colour and pattern of SSTK’s populations can be
explained by occurrence of gene flow between the M. raddei ssp.
populations, caused by Pleistocene climate oscillations (see Hewitt,
2004). The temperature decreased during Pleistocene cooling periods causing descending elevation shift in the habitat of mountain
dwelling species. The SSTK mountains are adjacent to the Zanjan valley and Montivipera populations inhabiting these mountain
ranges are isolated by a dry, intra-mountainous plain, named the
Ghezel-Ozan basin.
Although, at present the basin is not suitable habitat for M. raddei
ssp., maybe because Pleistocene cold seasons altered the climate,
it was a historical suitable habitat for M. raddei ssp. and mediated
connection between Montivipera populations of the Zanjan valley
and SSTK mountains.
Species of M. raddei complex are an interesting model for studying local adaptation of colour and pattern traits, in response to
different environmental factors and trade-off between thermoregulatory, cryptic and signalling function of colour pattern characters.
Further studies are needed to determine thermal preferences and
thermoregulatory behaviour of M. raddei ssp. and M. latifii to test
whether thermoregulation and behaviour or co-adapted in these
vipers.
Acknowledgements
No official funding was used for this research. We greatly thank
Hasan Poudineh, Mohsen Ranjbaran, Nikolaus Stümpel, Ruzbeh
Behruz, Maoud Yousefi, Benny Trapp, Göran Nilson and Jeff Ettling
for their kind cooperation. We would like to thank Alexander
Kupfer, Marco Zuffi and an anonymous referee for commenting on
earlier manuscript versions.
References
Adolph, S.C., 1990. Influence of behavioral thermoregulation on microhabitat use
by two Sceloporus lizards. Ecology 71, 315–327.
Allen, W.L., Baddeley, R., Scott-Samuel, N.E., Cuthill, I.C., 2013. The evolution and
function of pattern diversity in snakes. Behav. Ecol. 24, 1237–1250.
Andrén, C., Nilson, G., 1979. Vipera latifii (Reptilia, Serpentes, Viperidae) an
endangered viper from Lar Valley, Iran, and remarks on the sympatric
herpetofauna Vipera latifii (Reptilia, Serpentes, Viperidae) an endangered viper
from Lar Valley, Iran, and remarks on the sympatric herpetofauna. J. Herpetol.
13, 335–341.
Andrén, C., Nilson, G., 1981. Reproductive success and risk of predation in normal
and melanistic colour morphs of the adder, Vipera berus. Biol. J. Linn. Soc. 15,
235–246.
Behruz, R., 2010. Ecology of Latifi’s Viper (Montivipera latifii) in the Lar National
Park, Master Thesis. Tehran University, Iran.
Bittner, T.D., King, R.B., Kerfin, J.M., 2002. Effects of body size and melanism on the
thermal biology of garter snakes (Thamnophis sirtalis). Copeia 2002, 477–482.
Boettger, O., 1890. Eine neue viper aus Armenien. Zool. Anz. 13, 62–64.
Brodie, E., 1992. Correlational selection for color pattern and antipredator behavior
in the garter snake Thamnophis ordinoides. Evolution 46, 1284–1298.
Brodie, E., 1993. Differential avoidance of coral snake banded patterns by
free-ranging avian predators in Costa Rica. Evolution 47, 227–235.
Brodie, E., Janzen, F., 1995. Experimental studies of coral snake mimicry:
generalized avoidance of ringed snake patterns by free-ranging avian
predators. Funct. Ecol. 9, 186–190.
Campbell, J.A., Lamar, W.W., 1989. The Venomous Reptiles of Latin America.
Comstock Pub. Associates, Ithaca, NY.
Castella, B., Golay, J., Monney, J.C., Golay, P., Mebert, K., Dubey, S., 2013. Melanism,
body condition and elevational distribution in the asp viper. J. Zool. 290,
273–280.
Clusella-Trullas, S., van Wyk, J.H., Spotila, J.R., 2007. Thermal melanism in
ectotherms. J. Therm. Biol. 32, 235–245.
Clusella-Trullas, S., Wyk, J.H., Spotila, J.R., 2009. Thermal benefits of melanism in
cordylid lizards: a theoretical and field test. Ecology 90, 2297–2312.
Cott, H.B., 1940. Adaptive Coloration in Animals. Methuen and Co., London.
M. Rajabizadeh et al. / Zoologischer Anzeiger 257 (2015) 1–9
Darevsky, I.S., 1966. Ecology of stone-viper (Vipera xanthina raddei Boettger) in the
natural surroundings of Armenia. Mem. Inst. Butantan Simp. Int. 33, 81–83.
Davidson, J., Hassanzadeh, J., Berzins, R., Stockli, D.F., Bashukooh, B., Turrin, B.,
Pandamouz, A., 2004. The geology of Damavand volcano, Alborz Mountains,
northern Iran. Geol. Soc. Am. Bull. 116 (1/2), 16–29.
Edmunds, M.E., 1974. Defence in Animals: A Survey of Anti-predator Defences.
Longman, Harlow, Essex.
Ettling, J.A., Aghasyan, L.A., Aghasyan, A.L., Parker, P.G., 2013. Spatial ecology of
Armenian vipers, Montivipera raddei, in a human-modified landscape. Copeia
2013, 64–71.
Fan, Y., Van den Dool, H., 2008. A global monthly land surface air temperature
analysis for 1948–present. J. Geophys. Res. 113, 1–18.
Farallo, V.R., Forstner, M.R., 2012. Predation and the maintenance of colour
polymorphism in a habitat specialist squamate. PLoS One 7, 1–12.
Fisher, W.B., 1986. The Cambridge history of Iran. The Land of Iran, vol. 1.
Cambridge University Press, Cambridge.
Forsman, A., 1995. Opposing fitness consequences of colour pattern in male and
female snakes. J. Evol. Biol. 8, 53–70.
Gibson, A.R., Falls, J.B., 1979. Thermal biology of the common garter snake
Thamnophis sirtalis (L.). II. The effects of melanism. Oecologia 43, 99–109.
Gibson, A.R., Falls, B., 1988. Melanism in the common garter snake: a Lake Erie
phenomenon. In: Downhower, J.F. (Ed.), The Biogeography of the Island Region
of Western Lake Erie. Ohio State University Press, Columbus, pp. 233–245.
Götmark, F., 1987. White underparts in gulls function as hunting camouflage.
Anim. Behav. 35, 1786–1792.
Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G., Jarvis, A., 2005. Very high
resolution interpolated climate surfaces for global land areas. Int. J. Climatol.
25, 1965–1978.
Hewitt, G.M., 2004. Genetic consequences of climatic oscillations in the
Quaternary. Philos. Trans. R. Soc. B 359, 183–195.
Isaac, L.A., Gregory, P.T., 2013. Can snakes hide in plain view? Chromatic and
achromatic crypsis of two color forms of the western terrestrial Garter snake
(Thamnophis elegans). Biol. J. Linn. Soc. 108, 756–772.
Kark, S., Werner, Y.L., 1993. Polymorphism of Psammophis schokari (Ophidia:
Colubridae) in Israel and Sinai. Israel J. Zool. 39, 64.
King, R.B., 1992. Lake Erie water snakes revisited: morph-and age-specific
variation in relative crypsis. Evol. Ecol. 6, 115–124.
Lawson, R., King, R.B., 1996. Gene flow and melanism in Lake Erie garter snake
populations. Biol. J. Linn. Soc. 59, 1–19.
Lindell, L.E., Forsman, A., 1996. Sexual dichromatism in snakes: support for the
flicker-fusion hypothesis. Can. J. Zool. 74, 2254–2256.
Macedonia, J.M., 2001. Habitat light, colour variation, and ultraviolet reflectance in
the Grand Cayman anole, Anolis conspersus. Biol. J. Linn. Soc. 73, 299–320.
McGaugh, S.E., 2008. Colour variation among habitat types in the spiny softshell
turtles (Trionychidae: Apalone) of Cuatrociénegas, Coahuila, Mexico. J.
Herpetol. 42, 347–353.
Mertens, R., Darevsky, I.S., Klemmer, K., 1967. Vipera latifii, eine neue giftschlange
aus dem Iran. Senck. Biol. 48, 161–168.
Micheletti, S., Parra, E., Routman, E.J., 2012. Adaptive Colour polymorphism and
unusually high local genetic diversity in the side-blotched lizard, Uta
stansburiana. PLoS One 7, 476–494.
Nilson, G., Andrén, C., 1985. Systematics of the Vipera xanthina complex (Reptilia:
Viperidae). I. A new Iranian viper in the raddei species-group.
Amphibia–Reptilia 6, 207–214.
Nilson, G., Andrén, C., 1986. The mountain vipers of the Middle East: the Vipera
Xanthina complex (Reptilia, Viperidae). Bonner Zool. Monographien 20, 1–90.
Niskanen, M., Mappes, J., 2005. Significance of the dorsal zigzag pattern of Vipera
latastei gaditana against avian predators. J. Anim. Ecol. 74, 1091–1101.
Norris, A.L., Kunz, T.H., 2012. Effects of solar radiation on animal thermoregulation.
In: Babatunde, E.B. (Ed.), Solar raditation. INTECH Open Access Publisher, pp.
195–220, 484 pages.
9
Peterson, C.R., Gibson, A.R., Dorcas, M.E., 1993. Snake thermal ecology: the causes
and consequences of body-temperature variation. In: Seigel, R.A., Collins, J.T.
(Eds.), Snakes: Ecology and Behavior. McGraw Hill, New York, pp. 241–314.
Pough, F.H., Andrews, R.M., Cadle, J.E., Crump, M.L., Savitzky, A.H., Wells, K.D.,
1998. Herpetology. Benjamin Cummings Press, New York, pp. 577p–$9.
Rajabizadeh, M., 2013. Biodiversity of the Snakes in Southern and Western
Mountains of Iran, with Special Emphasis on Biodiversity in Colubroids. PhD
Thesis. Ghent University, Belgium.
Rajabizadeh, M., Nilson, G., Kami, H.G., 2011. A new species of mountain viper
(Serpentes: Viperidae) from the Central Zagros Mountains, Iran. Russ. J.
Herpetol. 18, 235–240.
Rajabizadeh, M., Yazdanpanah, A., Ursenbacher, S., 2012. Dorsal pattern variation
and sexual dimorphism in Montivipera latifii (Mertens, Darevsky and Klemmer,
1967) (Serpentes: Viperidae). Acta Herpetol. 7, 121.
Rosenblum, E.B., Hoekstra, H.E., Nachman, M.W., 2004. Adaptive reptile color
variation and the evolution of the MCIR gene. Evolution 58, 1794–1808.
Rögl, F., 1999. Mediterranean and paratethys: facts and hypotheses of an oligocene
to miocene paleogeography (short overview). Geol. Carpath. 50,
339–349.
Santos, X., Vidal-García, M., Brito, J.C., Fahd, S., Llorente, G.A., Martínez-Freiría, F.,
Parellada, X., Pleguezuelos, J.M., Sillero, N., 2014. Phylogeographic and
environmental correlates support the cryptic function of the zigzag pattern in
a European viper. Evol. Ecol. 28, 611–626.
Savage, J.M., Slowinski, J.B., 1992. The colouration of the venomous coral snakes
(family Elapidae) and their mimics (families Aniliidae and Colubridae). Biol. J.
Linn. Soc. 45, 235–254.
Sherratt, T.N., Beatty, C.D., 2003. The evolution of warning signals as reliable
indicators of prey defense. Am. Nat. 162, 377–389.
Shine, R., Harlow, P.S., 1998. Ecological divergence among sympatric colour
morphs in blood pythons, Python brongersmai. Oecologia 116, 11119.
Stevens, M., Merilaita, S., 2011. Animal Camouflage: Mechanisms and Function.
Cambridge University Press, Cambridge.
Stuart-Fox, D.M., Moussalli, A., Johnston, G.R., Owens, J.R., 2004. Evolution of colour
variation in dragon lizards: quantitative tests of the role of crypsis and local
adaptation. Evolution 58, 1549–1559.
Stümpel, N., 2012. Phylogenie und Phylogeographie Eurasischer Viperinae unter
Besonderer Berücksichtigung der Orientalischen Vipern der Gattungen
Montivipera und Macrovipera. PhD Thesis. Technische Universität
Braunschweig.
Stümpel, N., Joger, U., 2009. Recent advances in phylogeny and taxonomy of near
and Middle Eastern vipers – an update. ZooKeys 31, 179–191.
Terent év, P.V., Chernov, S.A., 1965. Key to Amphibian and Reptiles. Israel Program
for Scientific translation, Jerusalem, V + 313 pp., 122 figs, [English translation
of Terent év & Chernov, 1949].
Tullberg, B.S., Merilaita, S., Wiklund, C., 2005. Aposematism and crypsis combined
as a result of distance dependence: functional versatility of the colour pattern
in the swallowtail butterfly larva. Proc. R. Soc. B: Biol. Sci. 272, 1315–1321.
Valkonen, J., Niskanen, M., Björklund, M., Mappes, J., 2011. Disruption or
aposematism? Significance of dorsal zigzag pattern of European vipers. Evol.
Ecol. 25, 1047–1063.
Vincent, J.W., 1982. Colour pattern variation in Crotalus lepidus lepidus (Viperidae)
in southwestern Texas. Southwest. Nat. 27, 263–272.
Wilson, D., Heinsohn, R., Wood, J., 2006. Life-history traits and ontogenetic colour
change in an arboreal tropical python, Morelia viridis. J. Zool. 270, 399–407.
Wüster, W., Allum, C.S., Bjargardóttir, I.B., Bailey, K.L., Dawson, K.J., Guenioui, J.,
Lewis, J., McGurk, J., Moore, A.G., Niskanen, M., Pollard, C.P., 2004. Do
aposematism and Batesian mimicry require bright colours? A test, using
European viper markings. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 271,
2495–2499.