SUMMARY: We investigated the mechanisms by which temperature induces seasonal reproductive behavior in red-sided garter snakes (Thamnophis sirtalis parietalis). Specifically, we addressed whether elevated temperatures during winter dormancy influence (1) diel melatonin and corticosterone rhythms; (2) sex steroid hormone and corticosterone profiles; and (3) the expression of reproductive behavior following emergence. Elevated hibernation temperatures (i.e. 10°C versus 5°C) significantly increased overall melatonin and decreased corticosterone concentrations of snakes. The temperature-induced differences in melatonin rhythms between the 5°C and 10°C treatment groups persisted even after both groups were again acclimated to 10°C, indicating that cold temperature exposure has a lasting influence on melatonin rhythms. Elevated hibernation temperatures also significantly altered androgen and corticosterone profiles of snakes,providing a potential mechanism to explain reported annual variation in steroid hormones. Although previous studies indicate that male red-sided garter snakes exhibit a dissociated reproductive strategy, we demonstrate the presence of intersexual variation in sex steroid hormone profiles, as estradiol concentrations of female snakes increased significantly prior to spring mating activity. Importantly, the percentage change in body mass did not differ significantly between snakes in the hibernation treatments,indicating that the observed changes in hormone profiles are indeed temperature induced and not simply an indirect result of significant changes in the energy balance of snakes. Finally, in males maintained at 10°C during winter dormancy the onset of courtship behavior following emergence was delayed. Our results suggest that environmental temperatures induce reproductive behavior, in part, via changes in diel melatonin and/or corticosterone rhythms in this seasonally breeding reptile.

Red-sided garter snakes (Thamnophis sirtalis parietalis) court and mate in early spring around large communal overwintering dens in central Manitoba. Emerging females are immediately covered by dozens or hundreds of vigorously-courting males, potentially imposing significant costs to the female. By manipulating numbers of courting males (both directly and by applying anticourtship pheromones), we quantified the degree to which female dispersal from the den is hindered by courtship. Courted females dispersed only about half as fast as did solitary females. Blood lactate levels were higher in mating than in courting or noncourting snakes of both sexes; the high levels of lactate in mating females support the idea that courtship is physiologically stressful to these animals, perhaps via constraints to female respiration. In arena trials, females that were exercised to exhaustion before courtship mated with smaller males than did control females. The spatial distribution of snakes around the den exhibits substantial heterogeneity, with densities often varying markedly between adjacent areas. Arena trials mimicking this heterogeneity showed that unmated females avoided parts of the enclosure containing scent cues from males. Our data support the hypothesis that courtship in T. s. parietalis confers significant costs to females, and that female behaviors have evolved to reduce those costs.

Red-sided garter snakes ( Thamnophis sirtalis parietalis (Say in James, 1823)) in Manitoba, Canada, undergo 8 months of continuous winter dormancy prior to spring emergence. As in other ectothermic species, increases in ground temperature may be the cue for emergence from winter dormancy in these populations. To test this hypothesis, we measured body temperatures during winter dormancy by surgically implanting small temperature loggers into 32 female red-sided garter snakes before they entered their native hibernaculum. The following spring, we recaptured seven of the snakes implanted with temperature loggers. Body temperature declined gradually from mid-September (14.7 ± 0.24 °C, mean ± SE) to early April (1.1 ± 0.16 °C, mean ± SE) during winter dormancy, reaching minimal values approximately 1 month prior to spring emergence. Body temperatures of emerging snakes ranged from 0.5 °C during early spring to 6.3 °C during late spring (3.4 ± 0.84 °C, mean ± SE). These results do not support the hypothesis that an increase in ground temperature (and hence body temperature) is necessary for emergence from winter dormancy. We suggest that critically low temperatures (i.e., 0.5–1 °C) are a Zeitgeber entraining an endogenous circannual cycle that regulates snake emergence. These results offer new insight into the mechanisms regulating seasonal emergence from winter dormancy.