Copeia 2008, No. 2, 279–285
Reproductive Ecology of the Montpellier Snake, Malpolon
monspessulanus (Colubridae), and Comparison with Other
Sympatric Colubrids in the Iberian Peninsula
Mónica Feriche1, Juan M. Pleguezuelos1, and Xavier Santos1,2
Two spermatogenetic cycles, vernal and aestival, have been described in temperate colubrid snakes. In both
cycles, mating occurs in the spring, although vernal species produce spermatozoa in spring, just before mating,
while aestival species use spermatozoa produced the previous summer. In this study, we describe the
reproductive cycles of male and female Malpolon monspessulanus (Colubridae), and compare them to previously
published cycles of five other snake species, four vernal and one aestival, inhabiting the same area. We also
examine the consequences of both spermatogenesis cycles over the entire reproductive processes of male and
female snakes in the south-eastern Iberian Peninsula. Vernal species mate later than do aestival species, as males
must produce spermatozoa just prior to mating. However, vernal species are able to condense spermatogenesis
and vitellogenesis processes, hence undertaking oviposition at the same time as aestival species. Here we discuss
advantages of accomplishing the entire reproductive cycle in one (vernal species) or two (aestival species)
calendar years. We also found that mature male M. monspessulanus exhibit decreased testes volume relative to
body size. Large testes are expected in scenarios of sperm competition. The mating system of M. monspessulanus
(territoriality, mate guarding, male–male combat) does not suggest sperm competition, hence it may be more
advantageous for males of this species to invest in body size than in testes size.
C
LIMATE interacts with many physiological traits,
and for this reason it is one of the most important
factors that influence the geographic range of
species and their life-history strategies (Pither, 2003; Weladji
and Holand, 2003). For example, ectothermic vertebrates
acquire heat from external sources, and are more sensitive to
environmental climatic factors than are endothermic species (Pough et al., 2004). Several reproductive qualities of
ectotherms are known to be correlated to environmental
temperatures: for females, reproductive frequency, number
of clutches per year, and clutch timing; for males, mainly
the spermatogenetic cycle (Zug, 1993).
Among ectotherms, snakes show considerable inter- and
intraspecific plasticity in reproductive traits (Shine, 2003)
often related to several climatic factors. Volsøe (1944)
described two spermatogenetic patterns for snakes inhabiting the temperate region: aestival and vernal cycles (Saint
Girons, 1982; Seigel and Ford, 1987). The main difference
between these cycles is that in aestival spermatogenesis,
males produce spermatozoa in summer–autumn, store it
during winter, and mate the following spring. In vernal
cycles, spermatogenesis and mating occur in the same
calendar year (approximately in early-mid spring and late
spring, respectively). Aestival spermatogenesis is common in
snakes from temperate and cold regions, whereas vernal
cycles are characteristic of species inhabiting the southern
belt of the Palaearctic region (e.g., Northern Africa; Saint
Girons, 1982). Species exhibiting vernal cycles are restricted
to warm regions, where longer activity periods allow the
completion of a complete reproductive cycle within a
calendar year. For this reason, vernal species do not colonize
cold areas, either at high altitude or northern latitude. Saint
1
Girons (1982) recorded the isotherm of 22uC of the mean
temperature in July as the thermoclimatic limit for several
Mediterranean species with vernal spermatogenesis (e.g.,
Malpolon monspessulanus and Hemorrhois hippocrepis). In
addition to this physiological constraint on distribution,
other reproductive traits may be guided by this particular
spermatogenetic cycle (e.g., mating, vitellogenesis, egg
laying, and hatching time).
The evolutionary advantages of each of the spermatogenic
cycles can be best assessed in the few global regions where
species with both cycles coexist. One such region is the
southern Iberian Peninsula. Of seven oviparous snakes in
this region, the aestival cycle is known to occur in Coronella
girondica, Macroprotodon brevis, Rhinechis scalaris, Natrix
maura, and N. natrix (Feriche, 1998; Pleguezuelos and
Feriche, 1998; Santos and Llorente, 2001), whereas two
species, M. monspessulanus and H. hippocrepis, are the only
western European snake species with a vernal cycle (Cheylan
et al., 1981; Pleguezuelos and Feriche, 1999). The aims of
this paper are to describe reproductive traits of male and
female M. monspessulanus in the southern Iberian Peninsula,
and to compare reproductive cycles of sympatric oviparous
colubrid species subject to similar climatic conditions.
MATERIALS AND METHODS
Study area.—Field studies were carried out in an area of
approx. 3000 km2 in the southeastern Iberian Peninsula
(36u559–37u209N, 3u309–4u159W), centered around the Granada Depression, which spans elevations between 450–900 m
above sea level. During the study period, the mean
minimum temperature ranged between 1.9u to 4.4uC in
Departamento de Biologı́a Animal, Facultad de Ciencias, Universidad de Granada, E-18071 Granada, Spain; E-mail: (JMP) [email protected].
Send reprint requests to this address.
2
Departamento de Biologı́a Animal, Facultad de Ciencias, Universidad de Barcelona, Avinguda Diagonal 645, E-28008 Barcelona, Spain.
Submitted: 21 November 2006. Accepted: 29 October 2007. Associate Editor: M. J. Lannoo.
DOI:
F 2008 by the American Society of Ichthyologists and Herpetologists
Copeia cope-08-02-03.3d 21/3/08 17:09:06
279
Cust # CH-06-272
280
Copeia 2008, No. 2
winter (January), the mean maximum temperature ranged
between 31.0u to 35.6uC in summer (July), and the mean
annual temperature ranged between 12.5u to 14.3uC.
Average yearly rainfall ranged between 355.4 and
448.0 mm (data from the Cartuja weather station
[37u129N, 3u369W], representative of the study area). The
area is currently characterized by a mosaic of habitats
dominated by cultivated land (olive orchards and cereal
crops), mixed areas of evergreen forest and scrubland
(Quercus rotundifolia), and, to a lesser extent, pine plantations (Pinus halepensis, P. pinaster).
Sampling.—Field sampling was conducted from 1993 to
2004, within the framework of a larger study on the snake
fauna of the region (Feriche, 1998). We performed searches
3–4 days per month (daily searches lasted about six hours),
throughout all months of the year. Specimens of M.
monspessulanus were collected among those killed by local
people and by traffic. No animals were killed for the
purposes of this research. A total of 347 specimens were
obtained and preserved in alcohol at the University of
Granada (DBAG). We also hand captured live specimens
when possible (24 individuals), which provided information
on morphology, diet, and, to a lesser extent, reproduction.
Finally, we included specimens collected in the study area
from the collections of the Estación Biológica de Doñana,
Seville, Spain (EBD; n 5 13) and Museo Nacional de Ciencias
Naturales, Madrid, Spain (MNCN; n 5 12). In total, we
examined 396 specimens (230 males, 166 females). We
assume that reproductive cycling remained stable in the
study area over the 12 years of the study.
Data collection for Malpolon monspessulanus.—Snout–vent
length (SVL) of specimens was measured with a cord
(61 mm), and they were weighed with an electronic balance
(60.1 g). We determined sex by dissection of preserved
specimens and by examination of the dorsal pattern and
coloration of living individuals (Pleguezuelos and Moreno,
1988). We checked for recent prey by making a mid-ventral
incision in the stomach of preserved specimens. Live snakes
were gently palpated in the fore abdomen to force
regurgitation of recently ingested food, but not in the rear
abdomen to avoid damage in the reproductive organs.
We took the following measurements in order to analyze
reproductive ecology: longest, medium, and shortest axes of
the right testis (60.1 mm) in males; diameter of the largest
follicle or oviductal egg (60.1 mm) in females; fat-body size
in both sexes. In males, size at maturity and the spermatogenic cycle was determined by relating the testicular volume
(TV) with spermatogenic activity (Seigel and Ford, 1987).
We estimated TV using the formula for the volume of a
flattened ellipsoid (Mayhew, 1963). Adult males showed a
wide range of body sizes. To remove the effect of SVL on TV,
we calculated residuals from the regression of TV on SVL.
Residuals were used to describe seasonal variation in testis
volume (Pleguezuelos and Feriche, 1999, 2006). To analyze
ontogenetic shift in TV, we correlated the aforementioned
residuals with SVL. We limited this analysis to mature males
collected during the spermatogenic period (April to June) to
avoid any effect of spermatogenic inactivity on testis
volume. We determined timing of vitellogenesis by observation of follicle size in mature females. Clutch size was
estimated by counting oviductal eggs and enlarged follicles
(.18 mm). Because we were not able to accurately weigh fat
Copeia cope-08-02-03.3d 21/3/08 17:09:07
280
bodies from some road-killed specimens, or to remove fat
bodies from museum specimens, we scored fat body level in
five visual categories: zero, no traces of fat; one, small traces
of fat among intestine loops; two, fat bodies covering less
than half of the intestinal surface; three, fat bodies covering
more than half of the intestinal surface; and four, a
continuous fat layer in the ventral zone of the abdominal
cavity (Pleguezuelos and Feriche, 1999). Measurements were
only taken from well-preserved specimens. Therefore, there
are some differences in sample size for various measurements. Mean values are followed by 6 1 SD. Variables were
tested for normality prior to statistical analysis.
Data collection for other colubrid species.—We compared
reproductive data of M. monspessulanus with data obtained
from other colubrids in the study area (Table 1). All data
were obtained in the same area, and during the same period,
hence precluding geographic and/or climatic bias. Two
colubrid species inhabiting the study area, Coronella austriaca and Natrix natrix, were removed from comparisons;
the former because it is viviparous, the latter because of its
scarcity and small sample size.
RESULTS
Reproductive traits in Malpolon monspessulanus.—Males
were significantly larger than females, taking into account
the entire sample of adults (see minimum body size for
adults below; mean SVL: males, 934.6 6 218.9 mm, n 5 160;
females, 750.3 6 83.8 mm, n 5 80; t 5 7.26, df 5 238, P ,
0.000001) and only the upper decile of individuals of each
sex (mean SVL: males, 1323.5 6 65.4 mm, n 5 19; females,
896.1 6 50.4 mm, n 5 12; t 5 19.3, df 5 29, P , 0.000001).
Based on observation of relative TV (residuals), males
matured at 550 mm SVL (Fig. 1A), 37% of the maximum
male SVL in the study area (1480 mm). In adult males,
testicular growth started in March, TV peaked in mid June,
and sharply decreased by the end of June (Fig. 1B),
indicating a vernal spermatogenic cycle (Volsøe, 1944). All
mature males showed enlarged testes during the period of
spermatogenesis (Fig. 1B), suggesting that all adult males
were able to reproduce in consecutive years. Considering
males only during the reproductive period (April–June),
residuals of testis volume decreased with SVL (Fig. 2),
indicating that the relative testis volume was smaller for
larger males.
The smallest mature female measured 634 mm SVL
(Fig. 3A), so we therefore estimated that females matured
at 64% of the maximum female SVL in the study area
(988 mm). Females with enlarged follicles (.7 mm) were
found from the end of April until mid June, with oviductal
eggs during June and early July (Fig. 3B), and with oviductal
marks, a sign of recent oviposition, during the second half of
June and throughout July. Hence, we deduced that oviposition occurred from mid-June to early July. From Figure 3B,
we also deduced that the female reproductive cycle was very
synchronous and compressed. No stage of the female cycle
lasted much longer than one month, and the main stages,
vitellogenesis and oviposition, together lasted only two
months.
During the reproductive period, most adult females
contained follicles larger than 7 mm in maximum diameter
(96.4%, n 5 28; Fig. 3B), indicating that females reproduce
annually. Eight of 22 females with follicles larger than
Cust # CH-06-272
Period
March–15 June
End March–June
15 June–15 August
End May–15 August
April–September
May–August
Type
vernal
vernal
aestival
aestival
aestival
aestival
Species
Malpolon monspessulanus
Hemorrhois hippocrepis
Coronella girondica
Rhinechis scalaris
Macroprotodon brevis
Natrix maura
Spermatogenesis
prenuptial
prenuptial
postnuptial
postnuptial
postnuptial
postnuptial
Type
Period of
oviductal eggs
June–early July
15 May–June
July
15 June–15 July
End May–July
15 June–15 July
Period
End April–15 June
May–15 June
15 May–early July
May–early July
May–early July
May–June
Vitellogenesis
Table 1. Type and Timing of the Main Stages of the Reproductive Cycle in Oviparous Colubrids from the South-Eastern Iberian Peninsula.
21
20
25
05
15
25
Aug
Aug
Sep
Oct
Aug
Aug
First
hatchling
This study
Pleguezuelos and Feriche (1999)
Feriche (1998)
Pleguezuelos and Feriche (2006)
Pleguezuelos and Feriche (1998)
Feriche (1998)
References
Feriche et al.—Reproduction of the montpellier snake
Copeia cope-08-02-03.3d 21/3/08 17:09:07
281
Cust # CH-06-272
281
Fig. 1. Testicular growth in male Montpellier Snake (Malpolon
monspessulanus) in the Depression of Granada (south-eastern Iberian
Peninsula). Residual scores of the right testis volume plotted against (A)
body size (snout–vent length [SVL]; all individuals considered; n 5 118)
and (B) day of the year (only reproductive individuals, SVL . 550 mm;
n 5 81). Each data point represents one individual.
Fig. 2. Relationships between the testis volume (standardized by
residuals of the testis volume against snout–vent length [SVL]) and
the SVL of male Malpolon monspessulanus collected during the
spermatogenic period (April–June) in the Depression of Granada
(south-eastern Iberian Peninsula). Each data point represents one
individual.
282
Copeia 2008, No. 2
Fig. 3. Length of the largest follicle or oviductal egg in female
Montpellier Snake (Malpolon monspessulanus) in the Depression of
Granada (south-eastern Iberian Peninsula) plotted against (A) body size
(snout–vent length [SVL]; all individuals considered; n 5 95) and (B)
day of the year (only reproductive individuals, SVL . 630 mm; n 5 64).
25 mm had prey in their stomachs, and eight of 19 mature
females collected outside of the vitellogenic and oogenic
periods had prey in their stomachs (2 3 2 Table, x2 5 0.14, P
5 0.7), suggesting that gravid females do not stop feeding.
Clutch size (CS) ranged from three to 11 eggs (mean 5 6.7 6
2.4, n 5 18), and increased with female SVL (r 5 0.52, P 5
0.03, n 5 18; CS 5 23.96 + 0.0143 * SVL). Neonates were
found after active searching from 21 August to 10 September; hence, we estimate that egg incubation lasts approximately 60 days. Neonates measured 205–294 mm SVL
(mean 5 258.3 6 21.8 mm, n 5 25) and weighed 5.8–
10.2 g (mean 5 7.5 6 1.2 mm, n 5 13).
During the activity period, fat-body levels were homogeneous in sexually mature males (Fig. 4A; Kruskal–Wallis test,
H6,85 5 4.7, P 5 0.583), but not in females (Fig. 4B; Kruskal–
Wallis test, H6,61 5 22.95, P 5 0.002; in both sexes,
successive winter months were pooled because of small
sample size). Mature females started vitellogenesis with high
fat-body levels, which abruptly declined during this period
(Fig. 3B, 4B). Fat-body levels of males increased with body
size (rs 5 0.51, P , 0.01, n 5 96).
Comparison of reproductive traits.—Within the study area,
vernal colubrid species began spermatogenesis one to three
months earlier than species with aestival spermatogenesis
(Table 1). However, females of species with vernal spermatogenesis underwent vitellogenesis, carried oviductal eggs, and
laid eggs in approximately the same period as did females of
species with aestival spermatogenesis (Table 1). The hatchCopeia cope-08-02-03.3d 21/3/08 17:09:09
282
Fig. 4. Abdominal fat levels of reproductive male (A) and female (B)
Montpellier Snakes (Malpolon monspessulanus) in the Depression of
Granada (south-eastern Iberian Peninsula). Fat-body level is scored in
five categories, from zero to four (see the Materials and Methods for
more details).
ing period was roughly the same for most species and even
occurred one month earlier in vernal species than in some
aestival species (C. girondica, R. scalaris; Table 1).
DISCUSSION
Sexual selection has been claimed as one of the evolutionary
driving forces to explain sexual dimorphism in body size in
vertebrates (Simmons and Scheepers, 1996), and particularly
in snakes (Shine, 1993). Malpolon monspessulanus exhibits
the strongest sexual dimorphism in body size among
western Palaearctic snakes, with males much larger than
females (see a review in Böhme 1993, 1999; Schleich et al.,
1996). As male–male combat has been reported in this
species (de Haan, 1999), we would expect selection for large
males, which should have a higher probability of winning
combat bouts, and thus enjoy greater reproductive success
(Gibbons, 1972; Shine 1978, 1993).
Male biased sexual dimorphism in body size may also
explain the difference in relative body size at which each sex
attains sexual maturity. Male M. monspessulanus mature at
shorter absolute and relative body sizes than do females,
attaining maturity at slightly over one third of the
maximum recorded body size. Sexual dimorphism in
maturation is common in snakes (Parker and Plummer,
1987). Females mature at larger sizes than males, not only in
Cust # CH-06-272
Feriche et al.—Reproduction of the montpellier snake
absolute and relative size, but also in age: males mature at 3–
4 years old and females one year later (based on skeletochronological data from Hueso [1997] and our data on size
at maturity). Sexual differences in size and age at maturity
can also be explained by the relationship between clutch
size and female body size. Females may delay their first
reproduction, a decision that always implies risk (Madsen,
1987; Parker and Plummer, 1987), until a body-size
threshold is reached, hence allowing a theoretical minimum
clutch size of five eggs in this species (as deduced from the
equation of the regression between clutch size and body
size).
Vernal reproductive cycles are widespread in reptiles
occurring in warm climatic areas of the southern Palaearctic
(Saint Girons, 1982), such as North Africa. On the contrary,
this cycle is shared with only one of 20 other snake species
inhabiting Western Europe, Hemorrhois hippocrepis (Pleguezuelos and Feriche, 1999). This species shares a North
African origin with M. monspessulanus (Carranza et al.,
2006). Thus, we would define this male reproductive cycle
in Europe as rare in a strange land. The study of both male
and female reproductive cycles enables us to examine how
the sexes synchronize reproductive timing. In vernal species
like M. monspessulanus, gametogenesis in both sexes is
almost synchronous, and constrained to spring (Table 1).
However, the most interesting analysis is to compare the
reproductive timing of species exhibiting different spermatogenic cycles but inhabiting the same region. In so
doing, we observe that vernal species are able to condense
their first reproductive stages (spermatogenesis and vitellogenesis) with respect to aestival species. Additionally, vernal
species delay the mating period one to two months, thus
causing vitellogenesis to become prenuptial (postnuptial in
aestival species). Because of condensed vitellogenic and
oogenic periods, vernal species and aestival species undertake oviposition at the same time. In all snake species of the
study area, oviposition is timed to coincide with the start of
the warmest period of the year (Table 1), as this stage is
seasonally constrained by the high thermal requirements of
embryogenesis in reptiles (Saint Girons, 1982; Peterson et
al., 1993; Mathies and Andrews, 1995). In ectotherms,
timing of reproduction arises not from selection on
reproducing adults, but mainly through selection on
incubating eggs and neonates (Zug, 1993).
Does a shorter reproductive cycle provide vernal species
any evolutionary advantage over aestival species in areas
where these species coexist? Our data suggest that it does.
Currently, there is ample evidence for global warming
(Intergovernmental Panel on Climate Change, 1994; Jones
et al., 2001). In this scenario, vernal species in temperate
areas such as Europe may benefit. The vernal spermatogenic
cycle has strong thermal requirements that constrain its
northern border to approximately the 22uC mean isotherm
in July (Cheylan et al., 1981; Saint Girons, 1982). If
temperatures are increasing, we would expect an expansion
of northern and altitudinal limits of these species (Walther
et al., 2002). Although it is still hypothetical, some
evidences exist. Within the study area the mean annual
temperature increased 1.54uC in the last 22 years. In
parallel, M. monspessulanus increased its seasonal activity
period at a rate of 2–3 days/year (Moreno-Rueda and
Pleguezuelos, in press) and its dominance in the snake
community, from 27% to close to 50% of snake captures (C.
Segura, pers. comm.).
Copeia cope-08-02-03.3d 21/3/08 17:09:09
283
Cust # CH-06-272
283
Analyzing ontogenetic variation of testis size relative to
body length, we found that relative TV decreased with body
size. This can be interpreted as a cue of male senescence, an
aspect rarely considered in reptiles (Finch, 1994). However,
testes of the largest male M. monspessulanus continue to
produce spermatozoa (unpubl. data of authors). In most
animals, selection for large testes is expected in scenarios of
sperm competition (Olsson and Madsen, 1998). Nevertheless, the mating system of M. monspessulanus does not
suggest sperm competition, as males are highly territorial,
they practice mate guarding, and they engage in frequent
male–male combat (de Haan, 1999). This behavior precludes, or hampers, access to females by other males. Hence,
we expect selection to favor male M. monspessulanus which
invest in body size rather than testes size. Combat is more
likely to occur between large males (Madsen et al., 1993),
and the larger the male, the greater the possibility of
winning combat bouts (Andrén and Nilson, 1981; Schuett
and Gillingham, 1989), which results in access to more
copulations (Madsen et al., 1993). Larger males had much
more fat stored in fat bodies than did small males,
suggesting that the involution of TV in large males is not
a consequence of low body condition.
In adult snakes, reproduction in sequential years is an
indicator of high post-reproductive feeding success and of
favorable climatic conditions (Seigel and Ford, 1987; Zuffi et
al., 1999). Evidently, this must be the case for male as well as
female M. monspessulanus, a rather common terrestrial
colubrid in the southern Iberian Peninsula, inhabiting most
thermophilous habitats, and feeding on a wide variety of
prey, from insects to medium-sized birds and mammals
(Valverde, 1967; Pleguezuelos, 1998). In this species, all
adult males reproduced in sequential years, and spermatogenic processes apparently did not deplete fat-body levels.
Most adult females also reproduced in sequential years;
however, fat-body cycling was tied to the timing of the
reproductive cycle. Fat-body cycling suggests that stored
lipids must contribute to the energy needed for follicular
maturation and egg yolking, hence classifying female M.
monspessulanus as a ‘‘capital breeder,’’ as is typical of most
ectotherms (Bonnet et al., 1998). However, females continue
to feed during the vitellogenic period at a similar rate as
adult females outside this period. This suggests a certain
degree of ‘‘income breeding.’’ Accordingly, this species
provides an additional argument against using a simplistic
dichotomy (capital vs. income) to describe the strategy of
female ectotherms for fueling reproduction. Many snakes
appear to rely on an intermediate strategy defined as
‘‘facultative income’’ (Lourdais et al., 2002), as has recently
been reported for some colubrids (Reading, 2004; Santos and
Llorente, 2004; Pleguezuelos and Feriche, 2006).
ACKNOWLEDGMENTS
We thank S. Honrubia, M. Moreno, and J. FernándezCardenete for field assistance. J. Cabot (EBD) and J. González
(MNCN) provided facilities for studying specimens from
museums. K. Setser improved the style of the manuscript.
The last stage of this study was supported by the Research
Award REN2000-1376 GLO from the Spanish MCYT.
LITERATURE CITED
Andren, C., and G. Nilson. 1981. Reproductive success and
risk of predation in normal and melanistic colour morphs
284
Copeia 2008, No. 2
of the adder, Vipera berus. Biological Journal of the
Linnean Society 15:235–246.
Böhme, W. 1993, 1999. Handbuch der Reptilien und
Amphibien Europas. Schlangen (Serpentes). Aula–Verlag,
Wiesbaden. Vol. I:1–480; Vol. II:481–815.
Bonnet, X., S. D. Bradshaw, and R. Shine. 1998. Capital
versus income breeding: an ectothermic perspective.
Oikos 83:333–341.
Carranza, S., E. N. Arnold, and J. M. Pleguezuelos. 2006.
Mitochondrial DNA indicates the Mediterranean snakes,
Malpolon monspessulanus and Hemorrhois hippocrepis (Squamata, Colubridae), are recent colonizers of the Iberian
Peninsula. Molecular Phylogenetics and Evolution
40:532–546.
Cheylan, M., J. Bons, and H. Saint Girons. 1981. Existence
d’un cycle spermatogénétique vernal et prénuptial chez
un serpent méditerranéen, la couleuvre de Montpellier
Malpolon monspessulanus. Comptes Rendus de la Académie
des Sciences, Paris 292:1207–1209.
de Haan, C. 1999. Malpolon monspessulanus, p. 661–756. In:
Handbuch der Reptilien und Amphibien Europas. W.
Böhme (ed.). Band 3/IIA: Schlangen 2. Aula–Verlag,
Wiesbaden.
Feriche, M. 1998. Ecologı́a reproductora de los colúbridos
del sureste de la Penı́nsula Ibérica. Unpubl. Ph.D. diss.,
Universidad de Granada, Granada.
Finch, C. E. 1994. Longevity, Senescence and the Genome.
The University of Chicago Press, Chicago.
Gibbons, J. W. 1972. Reproduction, growth and sexual
dimorphism in the canebrake rattlesnake (Crotalus horridus atricaudatus). Copeia 1972:222–226.
Hueso, F. A. 1997. Biometrı́a, folidosis y esqueletocronologı́a de la Culebra bastarda Malpolon monspessulanus
Hermann, 1804 en Extremadura. Tes. Lic., Universidad
de Extremadura, Badajoz, Spain.
Intergovernmental Panel on Climate Change. 1994.
Climate Change. Cambridge University Press, Cambridge.
Jones, P. D., T. J. Osborne, and K. R. Briffa. 2001. The
evolution of the climate over the last millenium. Science
292:662–667.
Lourdais, O., X. Bonnet, R. Shine, D. Denardo, G.
Naulleau, and M. Guillon. 2002. Capital-breeding and
reproductive effort in a variable environment: a longitudinal study of a viviparous snake. Journal of Animal
Ecology 71:470–479.
Madsen, T. 1987. Natural and sexual selection in grass
snakes, Natrix natrix, and adders, Vipera berus. Unpubl.
Ph.D. diss., University of Lund, Lund, Sweden.
Madsen, T., R. Shine, J. Loman, and T. Hakansson. 1993.
Determinants of mating success in male adders. Animal
Behaviour 45:491–499.
Mathies, T., and R. M. Andrews. 1995. Thermal
and reproductive biology of high and low elevation
populations of the lizard Sceloporus scalaris: implications for the evolution of viviparity. Oecologia 104:
101–111.
Mayhew, W. W. 1963. Reproduction in the Granite Spiny
Lizard, Sceloporus orcutti. Copeia 1963:144–152.
Moreno-Rueda, G., and J. M. Pleguezuelos. In press. Longterm and short-term effects of temperature on snake
abundance in the wild: a case study with Malpolon
monspessulanus. Herpetological Journal.
Olsson, M., and T. Madsen. 1998. Sexual selection and
sperm competition in reptiles, p. 503–577. In: Sperm
Copeia cope-08-02-03.3d 21/3/08 17:09:09
284
Competition and Sexual Selection. T. R. Birkhead and A. P.
Moller (eds.). Academic Press, London.
Parker, W. S., and M. V. Plummer. 1987. Population
biology, p. 253–301. In: Snakes: Ecology and Evolutionary
Biology. R. A. Seigel, J. T. Collins, and S. S. Novak (eds.).
McGraw-Hill, New York.
Peterson, C. R., A. R. Gibson, and M. E. Dorcas. 1993.
Snake thermal ecology: the causes and consequences of
body-temperature variation, p. 241–314. In: Snakes Ecology and Behavior. R. A. Seigel and J. T. Collins (eds.).
McGraw-Hill, New York.
Pither, J. 2003. Climate tolerance and interspecific variation
in geographic range size. Proceedings of the Royal Society
of London 270:475–481.
Pleguezuelos, J. M. 1998. Malpolon monspessulanus (Hermann, 1804), p. 408–427. In: Fauna Ibérica 10. M. A.
Ramos (ed.). MNCN, C.S.I.C., Madrid.
Pleguezuelos, J. M., and M. Feriche. 1998. Reproductive
biology of the secretive Mediterranean colubrid Macroprotodon cucullatus in the southern Iberian Peninsula.
Herpetological Journal 8:195–200.
Pleguezuelos, J. M., and M. Feriche. 1999. Reproductive
ecology of the Hoseshoe Whip Snake, Coluber hippocrepis,
in the Southeast of the Iberian Peninsula. Journal of
Herpetology 33:202–207.
Pleguezuelos, J. M., and M. Feriche. 2006. Reproductive
ecology of a Mediterranean ratsnake, the ladder snake
Rhinechis scalaris (Schinz, 1822). Herpetological Journal
16:177–182.
Pleguezuelos, J. M., and M. Moreno. 1988. Folidosis,
Biometrı́a y Coloración de Ofidios en el SE de la Penı́nsula
Ibérica: Malpolon monspessulanus (Hermann). Revista
Española de Herpetologı́a 3:183–196.
Pough, F. H., J. R. Heiser, and C. M. Janis. 2004. Vertebrate
Life. Prentice Hall, Upper Saddle River, New Jersey.
Reading, C. J. 2004. The influence of body condition and
prey availability on female breeding success in the smooth
snake, Coronella austriaca Laurenti. Journal of Zoology
264:61–67.
Saint Girons, H. 1982. Reproductive cycles of male snakes
and their relationships with climate and female reproductive cycles. Herpetologica 38:5–16.
Santos, X., and G. A. Llorente. 2001. Seasonal variation in
reproductive traits of the oviparous water snake, Natrix
maura, in the Ebro Delta of northeastern Spain. Journal of
Herpetology 35:653–660.
Santos, X., and G. A. Llorente. 2004. Lipid dynamics in the
viperine snake Natrix maura from the Ebro Delta. Oikos
105:132–140.
Schleich, H. H., W. Kästle, and K. Kabisch. 1996.
Amphibians and Reptiles of North Africa. Koeltz Scientific
Books, Koenigstein, Germany.
Schuett, G. W., and J. C. Gillingham. 1989. Male–male
agonistic behaviour of the copperhead, Agkistrodon contortrix. Amphibia–Repilia 10:243–266.
Seigel, R. A., and N. B. Ford. 1987. Reproductive ecology,
p. 210–252. In: Snakes: Ecology and Evolutionary Biology.
R. A. Seigel, J. T. Collins, and S. S. Novak (eds.). McGrawHill, New York.
Shine, R. 1978. Sexual size dimorphism and male combat in
snakes. Oecologia 33:269–278.
Shine, R. 1993. Sexual dimorphism in snakes, p. 49–86. In:
Snakes: Ecology and Behavior. R. A. Seigel and J. T. Collins
(eds.). McGraw-Hill, New York.
Cust # CH-06-272
Feriche et al.—Reproduction of the montpellier snake
Shine, R. 2003. Reproductive strategies in snakes. Proceedings of the Royal Society of London B 270:995–1004.
Simmons, R. E., and L. Scheepers. 1996. Winning by a
neck: sexual selection in the evolution of giraffe. American Naturalist 148:771–786.
Valverde, J. A. 1967. Estructura de una comunidad de
vertebrados terrestres. Monografı́as de la Estación Biológica de Doñana 1:1–218.
Volsøe, H. 1944. Structure and seasonal variation of the
male reproductive organs of Vipera berus (L.). Spolia
Zoologica Musei Hauniensis 5:1–157.
Copeia cope-08-02-03.3d 21/3/08 17:09:10
285
Cust # CH-06-272
285
Walther, G. R., E. Post, P. Convey, A. Menzel, C.
Parmesan, T. J. C. Beebee, J. M. Fromentin, O. HoeghGuldberg, and F. Bairlen. 2002. Ecological responses to
recent climate change. Nature 416:389–395.
Weladji, R. B., and O. Holand. 2003. Global climate change
and reindeer: effects of winter weather on the autumn
weight and growth of calves. Oecologia 136:317–323.
Zuffi, M. A. L., F. Giudici, and P. Ioalè. 1999. Frequency
and effort of reproduction in female Vipera aspis from a
southern population. Acta Oecologica 20:633–638.
Zug, G. R. 1993. Herpetology. Academic Press, San Diego.