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

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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.
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