Reproductive Ecology of the Montpellier Snake, Malpolon Monspessulanus (Colubridae), and Comparison with Other Sympatric Colubrids in the Iberian Peninsula

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

Mo´nica 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.

LIMATE interacts with many physiological traits, Girons (1982) recorded the isotherm of 22uC of the mean and for this reason it is one of the most important temperature in July as the thermoclimatic limit for several C factors that influence the geographic range of Mediterranean species with vernal spermatogenesis (e.g., species and their life-history strategies (Pither, 2003; Weladji Malpolon monspessulanus and Hemorrhois hippocrepis). In and Holand, 2003). For example, ectothermic vertebrates addition to this physiological constraint on distribution, acquire heat from external sources, and are more sensitive to other reproductive traits may be guided by this particular environmental climatic factors than are endothermic spe- spermatogenetic cycle (e.g., mating, vitellogenesis, egg cies (Pough et al., 2004). Several reproductive qualities of laying, and hatching time). ectotherms are known to be correlated to environmental The evolutionary advantages of each of the spermatogenic temperatures: for females, reproductive frequency, number cycles can be best assessed in the few global regions where of clutches per year, and clutch timing; for males, mainly species with both cycles coexist. One such region is the the spermatogenetic cycle (Zug, 1993). southern Iberian Peninsula. Of seven oviparous snakes in Among ectotherms, snakes show considerable inter- and this region, the aestival cycle is known to occur in Coronella intraspecific plasticity in reproductive traits (Shine, 2003) girondica, Macroprotodon brevis, Rhinechis scalaris, Natrix often related to several climatic factors. Volsøe (1944) maura,andN. natrix (Feriche, 1998; Pleguezuelos and described two spermatogenetic patterns for snakes inhabit- Feriche, 1998; Santos and Llorente, 2001), whereas two ing the temperate region: aestival and vernal cycles (Saint species, M. monspessulanus and H. hippocrepis, are the only Girons, 1982; Seigel and Ford, 1987). The main difference western European snake species with a vernal cycle (Cheylan between these cycles is that in aestival spermatogenesis, et al., 1981; Pleguezuelos and Feriche, 1999). The aims of males produce spermatozoa in summer–autumn, store it this paper are to describe reproductive traits of male and M. monspessulanus during winter, and mate the following spring. In vernal female in the southern Iberian Peninsula, and to compare reproductive cycles of sympatric oviparous cycles, spermatogenesis and mating occur in the same colubrid species subject to similar climatic conditions. calendar year (approximately in early-mid spring and late spring, respectively). Aestival spermatogenesis is common in snakes from temperate and cold regions, whereas vernal MATERIALS AND METHODS cycles are characteristic of species inhabiting the southern belt of the Palaearctic region (e.g., Northern Africa; Saint Study area.—Field studies were carried out in an area of Girons, 1982). Species exhibiting vernal cycles are restricted approx. 3000 km2 in the southeastern Iberian Peninsula to warm regions, where longer activity periods allow the (36u559–37u209N, 3u309–4u159W), centered around the Gran- completion of a complete reproductive cycle within a ada Depression, which spans elevations between 450–900 m calendar year. For this reason, vernal species do not colonize above sea level. During the study period, the mean cold areas, either at high altitude or northern latitude. Saint minimum temperature ranged between 1.9u to 4.4uCin

1 Departamento de Biologı´a 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 Biologı´a 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. F 2008 by the American Society of Ichthyologists and Herpetologists DOI:

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 bodies from some road-killed specimens, or to remove fat between 31.0u to 35.6uC in summer (July), and the mean bodies from museum specimens, we scored fat body level in annual temperature ranged between 12.5u to 14.3uC. five visual categories: zero, no traces of fat; one, small traces Average yearly rainfall ranged between 355.4 and of fat among intestine loops; two, fat bodies covering less 448.0 mm (data from the Cartuja weather station than half of the intestinal surface; three, fat bodies covering [37u129N, 3u369W], representative of the study area). The more than half of the intestinal surface; and four, a area is currently characterized by a mosaic of habitats continuous fat layer in the ventral zone of the abdominal dominated by cultivated land (olive orchards and cereal cavity (Pleguezuelos and Feriche, 1999). Measurements were crops), mixed areas of evergreen forest and scrubland only taken from well-preserved specimens. Therefore, there (Quercus rotundifolia), and, to a lesser extent, pine planta- are some differences in sample size for various measure- tions (Pinus halepensis, P. pinaster). ments. Mean values are followed by 6 1 SD. Variables were tested for normality prior to statistical analysis. Sampling.—Field sampling was conducted from 1993 to 2004, within the framework of a larger study on the snake Data collection for other colubrid species.—We compared fauna of the region (Feriche, 1998). We performed searches reproductive data of M. monspessulanus with data obtained 3–4 days per month (daily searches lasted about six hours), from other colubrids in the study area (Table 1). All data throughout all months of the year. Specimens of M. were obtained in the same area, and during the same period, monspessulanus were collected among those killed by local hence precluding geographic and/or climatic bias. Two people and by traffic. No animals were killed for the colubrid species inhabiting the study area, Coronella aus- purposes of this research. A total of 347 specimens were triaca and Natrix natrix, were removed from comparisons; obtained and preserved in alcohol at the University of the former because it is viviparous, the latter because of its Granada (DBAG). We also hand captured live specimens scarcity and small sample size. when possible (24 individuals), which provided information on morphology, diet, and, to a lesser extent, reproduction. RESULTS Finally, we included specimens collected in the study area from the collections of the Estacio´n Biolo´gica de Don˜ana, Reproductive traits in Malpolon monspessulanus.—Males Seville, Spain (EBD; n 5 13) and Museo Nacional de Ciencias were significantly larger than females, taking into account Naturales, Madrid, Spain (MNCN; n 5 12). In total, we the entire sample of adults (see minimum body size for examined 396 specimens (230 males, 166 females). We adults below; mean SVL: males, 934.6 6 218.9 mm, n 5 160; assume that reproductive cycling remained stable in the females, 750.3 6 83.8 mm, n 5 80; t 5 7.26, df 5 238, P , study area over the 12 years of the study. 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, Data collection for Malpolon monspessulanus.—Snout–vent 896.1 6 50.4 mm, n 5 12; t 5 19.3, df 5 29, P , 0.000001). length (SVL) of specimens was measured with a cord Based on observation of relative TV (residuals), males (61 mm), and they were weighed with an electronic balance matured at 550 mm SVL (Fig. 1A), 37% of the maximum (60.1 g). We determined sex by dissection of preserved male SVL in the study area (1480 mm). In adult males, specimens and by examination of the dorsal pattern and testicular growth started in March, TV peaked in mid June, coloration of living individuals (Pleguezuelos and Moreno, and sharply decreased by the end of June (Fig. 1B), 1988). We checked for recent prey by making a mid-ventral indicating a vernal spermatogenic cycle (Volsøe, 1944). All incision in the stomach of preserved specimens. Live snakes mature males showed enlarged testes during the period of were gently palpated in the fore abdomen to force spermatogenesis (Fig. 1B), suggesting that all adult males regurgitation of recently ingested food, but not in the rear were able to reproduce in consecutive years. Considering abdomen to avoid damage in the reproductive organs. males only during the reproductive period (April–June), We took the following measurements in order to analyze residuals of testis volume decreased with SVL (Fig. 2), reproductive ecology: longest, medium, and shortest axes of indicating that the relative testis volume was smaller for the right testis (60.1 mm) in males; diameter of the largest larger males. follicle or oviductal egg (60.1 mm) in females; fat-body size The smallest mature female measured 634 mm SVL in both sexes. In males, size at maturity and the spermato- (Fig. 3A), so we therefore estimated that females matured genic cycle was determined by relating the testicular volume at 64% of the maximum female SVL in the study area (TV) with spermatogenic activity (Seigel and Ford, 1987). (988 mm). Females with enlarged follicles (.7 mm) were We estimated TV using the formula for the volume of a found from the end of April until mid June, with oviductal flattened ellipsoid (Mayhew, 1963). Adult males showed a eggs during June and early July (Fig. 3B), and with oviductal wide range of body sizes. To remove the effect of SVL on TV, marks, a sign of recent oviposition, during the second half of we calculated residuals from the regression of TV on SVL. June and throughout July. Hence, we deduced that ovipo- Residuals were used to describe seasonal variation in testis sition occurred from mid-June to early July. From Figure 3B, volume (Pleguezuelos and Feriche, 1999, 2006). To analyze we also deduced that the female reproductive cycle was very ontogenetic shift in TV, we correlated the aforementioned synchronous and compressed. No stage of the female cycle residuals with SVL. We limited this analysis to mature males lasted much longer than one month, and the main stages, collected during the spermatogenic period (April to June) to vitellogenesis and oviposition, together lasted only two avoid any effect of spermatogenic inactivity on testis months. volume. We determined timing of vitellogenesis by obser- During the reproductive period, most adult females vation of follicle size in mature females. Clutch size was contained follicles larger than 7 mm in maximum diameter estimated by counting oviductal eggs and enlarged follicles (96.4%, n 5 28; Fig. 3B), indicating that females reproduce (.18 mm). Because we were not able to accurately weigh fat annually. Eight of 22 females with follicles larger than

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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. Spermatogenesis Vitellogenesis Type Period Type Period vernalvernal March–15aestival June Endaestival March–June 15 June–15 Augustaestival End May–15 Augustaestival April–September prenuptial postnuptial May–August prenuptial postnuptial End 15 April–15 May–early June July May–15 May–early June July postnuptial May–early July postnuptial June–early July July May–June 15 15 June–15 May–June 21 July Aug End May–July 05 Oct 20 Aug This study 25 Sep 15 Aug Pleguezuelos 15 and June–15 Feriche July Pleguezuelos (2006) and Feriche (1999) Feriche 25 (1998) Pleguezuelos Aug and Feriche (1998) Feriche (1998)

Fig. 2. Relationships between the testis volume (standardized by residuals of the testis volume against snout–vent length [SVL]) and Type and Timing of the Main Stages of the Reproductive Cycle in Oviparous Colubrids from the South-Eastern Iberian Peninsula. 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 Malpolon monspessulanus Hemorrhois hippocrepis Coronella girondica Rhinechis scalaris Macroprotodon brevis Natrix maura Species

Table 1. individual.

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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) Fig. 4. Abdominal fat levels of reproductive male (A) and female (B) day of the year (only reproductive individuals, SVL . 630 mm; n 5 64). 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 25 mm had prey in their stomachs, and eight of 19 mature more details). 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. ing period was roughly the same for most species and even 5 6 Clutch size (CS) ranged from three to 11 eggs (mean 6.7 occurred one month earlier in vernal species than in some 5 5 5 2.4, n 18), and increased with female SVL (r 0.52, P aestival species (C. girondica, R. scalaris; Table 1). 0.03, n 5 18; CS 523.96 + 0.0143 * SVL). Neonates were found after active searching from 21 August to 10 Septem- ber; hence, we estimate that egg incubation lasts approxi- DISCUSSION mately 60 days. Neonates measured 205–294 mm SVL Sexual selection has been claimed as one of the evolutionary (mean 5 258.3 6 21.8 mm, n 5 25) and weighed 5.8– driving forces to explain sexual dimorphism in body size in 10.2 g (mean 5 7.5 6 1.2 mm, n 5 13). vertebrates (Simmons and Scheepers, 1996), and particularly During the activity period, fat-body levels were homoge- in snakes (Shine, 1993). Malpolon monspessulanus exhibits neous in sexually mature males (Fig. 4A; Kruskal–Wallis test, the strongest sexual dimorphism in body size among H6,85 5 4.7, P 5 0.583), but not in females (Fig. 4B; Kruskal– western Palaearctic snakes, with males much larger than Wallis test, H6,61 5 22.95, P 5 0.002; in both sexes, females (see a review in Bo¨hme 1993, 1999; Schleich et al., successive winter months were pooled because of small 1996). As male–male combat has been reported in this sample size). Mature females started vitellogenesis with high species (de Haan, 1999), we would expect selection for large fat-body levels, which abruptly declined during this period males, which should have a higher probability of winning (Fig. 3B, 4B). Fat-body levels of males increased with body combat bouts, and thus enjoy greater reproductive success size (rs 5 0.51, P , 0.01, n 5 96). (Gibbons, 1972; Shine 1978, 1993). Male biased sexual dimorphism in body size may also Comparison of reproductive traits.—Within the study area, explain the difference in relative body size at which each sex vernal colubrid species began spermatogenesis one to three attains sexual maturity. Male M. monspessulanus mature at months earlier than species with aestival spermatogenesis shorter absolute and relative body sizes than do females, (Table 1). However, females of species with vernal spermato- attaining maturity at slightly over one third of the genesis underwent vitellogenesis, carried oviductal eggs, and maximum recorded body size. Sexual dimorphism in laid eggs in approximately the same period as did females of maturation is common in snakes (Parker and Plummer, species with aestival spermatogenesis (Table 1). The hatch- 1987). Females mature at larger sizes than males, not only in

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absolute and relative size, but also in age: males mature at 3– Analyzing ontogenetic variation of testis size relative to 4 years old and females one year later (based on skeleto- body length, we found that relative TV decreased with body chronological data from Hueso [1997] and our data on size size. This can be interpreted as a cue of male senescence, an at maturity). Sexual differences in size and age at maturity aspect rarely considered in reptiles (Finch, 1994). However, can also be explained by the relationship between clutch testes of the largest male M. monspessulanus continue to size and female body size. Females may delay their first produce spermatozoa (unpubl. data of authors). In most reproduction, a decision that always implies risk (Madsen, animals, selection for large testes is expected in scenarios of 1987; Parker and Plummer, 1987), until a body-size sperm competition (Olsson and Madsen, 1998). Neverthe- threshold is reached, hence allowing a theoretical minimum less, the mating system of M. monspessulanus does not clutch size of five eggs in this species (as deduced from the suggest sperm competition, as males are highly territorial, equation of the regression between clutch size and body they practice mate guarding, and they engage in frequent size). male–male combat (de Haan, 1999). This behavior pre- Vernal reproductive cycles are widespread in reptiles cludes, or hampers, access to females by other males. Hence, occurring in warm climatic areas of the southern Palaearctic we expect selection to favor male M. monspessulanus which (Saint Girons, 1982), such as North Africa. On the contrary, invest in body size rather than testes size. Combat is more this cycle is shared with only one of 20 other snake species likely to occur between large males (Madsen et al., 1993), inhabiting Western Europe, Hemorrhois hippocrepis (Plegue- and the larger the male, the greater the possibility of zuelos and Feriche, 1999). This species shares a North winning combat bouts (Andre´n and Nilson, 1981; Schuett African origin with M. monspessulanus (Carranza et al., and Gillingham, 1989), which results in access to more 2006). Thus, we would define this male reproductive cycle copulations (Madsen et al., 1993). Larger males had much in Europe as rare in a strange land. The study of both male more fat stored in fat bodies than did small males, and female reproductive cycles enables us to examine how suggesting that the involution of TV in large males is not the sexes synchronize reproductive timing. In vernal species a consequence of low body condition. like M. monspessulanus, gametogenesis in both sexes is In adult snakes, reproduction in sequential years is an almost synchronous, and constrained to spring (Table 1). indicator of high post-reproductive feeding success and of However, the most interesting analysis is to compare the favorable climatic conditions (Seigel and Ford, 1987; Zuffi et reproductive timing of species exhibiting different sper- al., 1999). Evidently, this must be the case for male as well as matogenic cycles but inhabiting the same region. In so female M. monspessulanus, a rather common terrestrial doing, we observe that vernal species are able to condense colubrid in the southern Iberian Peninsula, inhabiting most their first reproductive stages (spermatogenesis and vitello- thermophilous habitats, and feeding on a wide variety of genesis) with respect to aestival species. Additionally, vernal prey, from insects to medium-sized birds and mammals species delay the mating period one to two months, thus (Valverde, 1967; Pleguezuelos, 1998). In this species, all causing vitellogenesis to become prenuptial (postnuptial in adult males reproduced in sequential years, and spermato- aestival species). Because of condensed vitellogenic and genic processes apparently did not deplete fat-body levels. oogenic periods, vernal species and aestival species under- Most adult females also reproduced in sequential years; take oviposition at the same time. In all snake species of the however, fat-body cycling was tied to the timing of the study area, oviposition is timed to coincide with the start of reproductive cycle. Fat-body cycling suggests that stored the warmest period of the year (Table 1), as this stage is lipids must contribute to the energy needed for follicular seasonally constrained by the high thermal requirements of maturation and egg yolking, hence classifying female M. embryogenesis in reptiles (Saint Girons, 1982; Peterson et monspessulanus as a ‘‘capital breeder,’’ as is typical of most al., 1993; Mathies and Andrews, 1995). In ectotherms, ectotherms (Bonnet et al., 1998). However, females continue timing of reproduction arises not from selection on to feed during the vitellogenic period at a similar rate as reproducing adults, but mainly through selection on adult females outside this period. This suggests a certain incubating eggs and neonates (Zug, 1993). degree of ‘‘income breeding.’’ Accordingly, this species Does a shorter reproductive cycle provide vernal species provides an additional argument against using a simplistic any evolutionary advantage over aestival species in areas dichotomy (capital vs. income) to describe the strategy of where these species coexist? Our data suggest that it does. female ectotherms for fueling reproduction. Many snakes Currently, there is ample evidence for global warming appear to rely on an intermediate strategy defined as (Intergovernmental Panel on Climate Change, 1994; Jones ‘‘facultative income’’ (Lourdais et al., 2002), as has recently et al., 2001). In this scenario, vernal species in temperate been reported for some colubrids (Reading, 2004; Santos and areas such as Europe may benefit. The vernal spermatogenic Llorente, 2004; Pleguezuelos and Feriche, 2006). cycle has strong thermal requirements that constrain its northern border to approximately the 22uC mean isotherm ACKNOWLEDGMENTS in July (Cheylan et al., 1981; Saint Girons, 1982). If We thank S. Honrubia, M. Moreno, and J. Ferna´ndez- temperatures are increasing, we would expect an expansion Cardenete for field assistance. J. Cabot (EBD) and J. Gonza´lez of northern and altitudinal limits of these species (Walther (MNCN) provided facilities for studying specimens from et al., 2002). Although it is still hypothetical, some museums. K. Setser improved the style of the manuscript. evidences exist. Within the study area the mean annual The last stage of this study was supported by the Research temperature increased 1.54uC in the last 22 years. In Award REN2000-1376 GLO from the Spanish MCYT. parallel, M. monspessulanus increased its seasonal activity period at a rate of 2–3 days/year (Moreno-Rueda and LITERATURE CITED Pleguezuelos, in press) and its dominance in the snake community, from 27% to close to 50% of snake captures (C. Andren, C., and G. Nilson. 1981. Reproductive success and Segura, pers. comm.). risk of predation in normal and melanistic colour morphs

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