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Seasonal Variation in Reproductive Traits of the Oviparous Water Snake, Natrix maura, in the Ebro Delta of Northeastern Spain

2001; The Society for the Study of Amphibians and Reptiles; Volume: 35; Issue: 4 Linguagem: Inglês

10.2307/1565905

1937-2418

Xavier Santos, Gustavo A. Llorente,

Wildlife Ecology and Conservation

-We describe the reproductive cycle of a population of the viperine snake (Natrix maura) in the Ebro Delta rice fields. This area is characterized by seasonal changes in water levels that strongly affect seasonal aquatic prey availability. Vilperine snakes emerged from hibernation in March and mating occurred from April to June, using sperm stored by males overwinter. Spermatogenesis was postnuptial and sperm mobilization from testes to spermiducts occurred in August. Variation in the lipid content of fat bodies suggests that both mating and spermatogesis are energetically costly. 'lVitellogenesis was prenuptial as follicular growth occurred after emergence from hibernation. Gravid females were found in July and August Clutch size was similar to other viperine snake populations, but spermatogenesis and vitellogenesis were delayed in the Ebro Delta population. These interpopulational differences may be related to variation in prey availability. Variation in the lipid content of fat bodies supports this hypothesis. In April, both males and females showed few lipid reserves, and vitellogenesis was delayed to the extent that females were gravid in August. In contrast to other snake species, variation in food availability did not affect the proportion of reproductive females or clutch size. In temperate regions, females invest lipids from fat bodies in oogenesis (Seigel and Ford, 1987), and therefore, variation in fat body mass has been used as a measure of the energetic costs of female reproduction. Most studies of males have considered energetic costs of mating behavior (Krohmer and Aldridge, 1985; Aldridge et al., 1990; Bonnet and Naulleau, 1996), and only recent studies have focused on the cost of producing sperm (Olsson et al., 1997). For both sexes, it is assumed that reproductive activities involve the ability to store energy, which should be linked to resource availability. Food availability is considered the proximate factor that causes variation in life-history traits (e.g., Seigel and Ford, 1991) and has been analyzed by experimental manipulation of diet (Ford and Seigel, 1989; Seigel and Ford, 1991, 1992). Field studies have also suggested that energy intake can constrain reproductive output. Shine and Madsen (1997) demonstrated that the proportion of reproductive females in a given year is correlated with food availability in the previous year, and Ford and Seigel (1994) suggested that short-term variation in resource availability also causes changes in reproductive output. It is generally accepted that there is a threshold of stored fat required before the onset of vitellogenesis in some species (Saint Girons, 1957; Blem, 1981, 1997; Scott et al., 1995; Naulleau and Bonnet, 1996). Female snakes exhibit phenotypic plasticity in 1 Corresponding Author. E-mail: herpetologia@ porthos.bio.ub.es life-history traits when exposed to periods of low foraging success prior to vitellogenesis (Ford and Seigel,1994). In natural populations, this reproductive plasticity can result in a reduction in the proportion of reproductive females (Saint Girons, 1957; Andren and Nilson, 1983; Naulleau and Bonnet, 1996; Shine and Madsen, 1997; Shine et al., 1998) or the production of small clutch sizes or small eggs (Plummer, 1984; Seigel and Fitch, 1985). Plummer (1983) suggested that vitellogenesis in the snake Opheodrys aestivus could be delayed until fat stores were increased by feeding, similar to Smith's (1968) observations of Ameiva. In the Mediterranean region, rice fields exhibit short-term fluctuations: they are temporary, highly dynamic aquatic ecosystems and are characterized by a rapid development of their biological communities (For6s and Comfn, 1992). In Ebro Delta Natural Park in northeastern Spain, rice fields are flooded from mid-April through September and become dry plains after harvesting (October) and remain so until the following spring. Aquatic animal biomass exhibits sharp monthly variation throughout the rice cycle (Gonzalez-Solis et al., 1996). In this paper, we describe the reproductive cycle of a viperine snake population, Natrix maura, from the Ebro Delta rice fields. This oviparous water snake is widely distributed in western Europe and northwestern Africa and is the most abundant snake in the Iberian Peninsula (Santos et al., 1997) and in the Ebro Delta (Llorente et al., 1991). Previous studies from other localities reported that N. maura is characterized by prenuptial vitellogenesis and postnuptial spermatogenThis content downloaded from 207.46.13.101 on Sat, 08 Oct 2016 05:37:08 UTC All use subject to http://about.jstor.org/terms X. SANTOS AND G. A. LLORENTE esis with sperm overwintering in spermiducts (Duguy and Saint Girons, 1966; Hailey and Davies, 1987a; Ja6n, 1988; Brafa, 1998). Thus, in the Ebro Delta, we expected that the onset of vitellogenesis would coincide with low aquatic prey availability during drought conditions. The aim of this paper is to analyze the reproductive phenotypic plasticity of this oviparous snake in this scenario. MATERIALS AND METHODS Fieldwork was carried out in the canals and rice fields of Ebro Delta Natural Park, a wetland area located on the Mediterranean coast of the northeastern Iberian Peninsula. Two researchers covered the study area at monthly intervals from March 1990 to November 1991, searching for viperine snakes in standarized transects over two days. Specimens were collected by hand, measured (snout-vent length, SVL in mm), weighed (to the nearest 0.1 g) and sexed using external characteristics (Feriche et al., 1993). In females, cloacal fluid smears were obtained to analyze the presence of spermatozoa as a means of establishing the mating period (see Hailey and Davies, 1987b). For analysis of reproductive tissues, a subsample of at least three males and three females was collected each month, killed by inducing cold torpor and frozen in dry ice. To increase monthly samples, snakes recently killed on roads or killed by country people were also collected (for monthly sample sizes, see Fig. 1). Abdominal fat bodies were removed from each snake and oven dried at 60?C until constant weight was achieved. Lipids were extracted from the dry tissue, using the Soxhlet method for four hours. N-hexane was used as organic solvent. After extraction, fat bodies were weighed again to determine lipid content. In males, both testes were measured (length and maximum width; + 0.1 mm) and weighed (+ 0.01 g). We obtained smears from the testes and spermiducts. In females, oviducts were removed, weighed (+ 0.01 g) and a smear of the oviductal fluid analyzed. Both ovaries were weighed, and follicles were counted and measured (length and width, +0.1 mm). Follicle volume was estimated by V = 4/3 Xr a/2 (b/2)2 where a corresponds to the length and b to the width of the follicle. Smears from the cloaca, testes, spermiducts, and oviducts were stained with hematoxylin-eosin (dift-quick method), and observed at 400X. Because smears were homogeneous, the sample was divided in three blocks, and the spermatogenic cell abundance was counted in a haphazard area within each block. Size at maturity was determined in males by the presence of spermatozoa in testes or sper0.10