Thermal biology of the common garter snake Thamnophis sirtalis (L.)

Summary The thermoregulatory significance of a striped-melanic colour polymorphism in the common garter snake, Thamnophis sirtalis, was assessed through a combination of labortory experimentation and field study. In experiments with living snakes the melanic morph maintained a higher body temperature than the striped morph, when exposed to natural insolation. Experiments with excised skin showed that this thermal advantage is attributable to some integumental difference between the two morphs. Body temperatures of snakes in the field revealed that, during the colder part of the active season, melanics were able to stay warmer than striped snakes by an amount (1.24 C°) approximating the difference observed in the laboratory. Some evidence and argument is presented to suggest that melanism also may confer protection against overheating in warm periods.     

Thermal correlates of foraging-site selection by Chinese pit-vipers (Gloydius shedaoensis,Viperidae)

• 1.Do thermal factors influence foraging-site selection by ectothermic predators? Snake species that obtain their prey from ambush must remain immobile for long periods, precluding overt behavioural thermoregulation; and some “ambush” snakes use thermal cues to detect endothermic prey. Plausibly, alternative ambush sites might differ either in equilibrial body temperatures available to snakes, or in the thermal “background” against which prey items must be detected.
• 2.We examined this topic with field data on pit-vipers (Gloydius shedaoensis) on a small island in northeastern China. Adult snakes feed only on migrating passerine birds. The snakes ambush birds both from arboreal perches (branches of small trees) and from the ground.
• 3.Arboreal versus terrestrial ambush sites differed both in operative temperatures and thermal “backgrounds” available to the snakes. Operative temperatures inside copper models were lower in trees than on the ground (because of wind), and snakes in arboreal ambush sites were cooler than those in terrestrial sites. Thermal backgrounds from arboreal perches were cooler (and thus, provided more contrast against prey items) than did backgrounds available from terrestrial ambush-sites.
• 4.Thermal factors thus modify the suitability of alternative ambush locations for these pit-vipers, but with a trade-off: a snake in a tree can “see” its prey more clearly, but may not be warm enough (and hence, able to strike fast enough) to capture it. Further work is required to determine whether or not snakes actually use such thermal differences as criteria for the selection of ambush sites.

     

The consistency of individual differences in behaviour: temperature effects on antipredator behaviour in garter snakes

Differences among individuals are necessary for natural selection to occur. The extent and expression of these differences can limit the power of selection to cause evolutionary change. When individuals inconsistently express a trait, selection is less powerful. Labile traits such as behaviour are most likely to be inconsistent in their expression, because of the substantial role of environmental factors in their immediate expression. Previous work has focused on the consistency, or repeatability, of individual behaviour across different environments or within a single environment; little is known about how repeatability within an environment changes across environments. To address this issue, we examined the consistency of antipredator behaviour in juvenile garter snakes in different thermal environments. A group of 59 laboratory-born garter snakes Thamnophis ordinoides, was repeatedly assayed for sprint speed, distance crawled, and number of reversals performed during flight and antipredator display. Antipredator display showed very little variation and could not be analysed. Each individual was tested three times at each of three temperatures chosen to span the range of temperatures that snakes encounter in the field (15, 22.5, 30 degrees C). Temperature had substantial effects on the average expression of each behaviour; snakes crawled more slowly, for shorter distances, and performed fewer reversals at cooler temperatures. Individuals showed significant consistency in their behaviour, and this consistency of expression was not affected by temperature. Copyright 1999 The Association for the Study of Animal Behaviour.     

Species specificity of methyl ketone profiles in the skin lipids of female garter snakes,genus Thamnophis

One of the relatively few vertebrate pheromones to be chemically identified, the female sex pheromone of the red-sided garter snake (Thamnophis sirtalis parietalis) is a series of saturated and monounsaturated methyl ketones contained within female skin lipids. During the breeding season, this pheromone is responsible for eliciting male courtship behaviors and males are able to utilize pheromonal variation to discriminate among females. While the pheromone system of the red-sided garter snake has been the subject of many studies, relatively little is known about the pheromone systems of other garter snakes. Through chemical analyses, we demonstrate that female skin lipids of the red-spotted garter snake (Thamnophis sirtalis concinnus), northwestern garter snake (Thamnophis ordinoides), and plains garter snake (Thamnophis radix) contain similar methyl ketones. The methyl ketone profiles of these snakes differ qualitatively from one another and from the methyl ketone profiles of red-sided garter snakes with differences particularly pronounced between sympatric species. Our results provide evidence that the use of methyl ketones in sexual signaling may be ubiquitous for Thamnophis species and suggest that these compounds could play a role in reproductive isolation between species in this genus.     

The role of vision in the predatory behaviour of natricine snakes

Early workers concluded that ingestively naive garter snakes (Thamnophis) recognize chemical cues from their normal prey, and that such cues are sufficient to elicit prey attack, whereas visual prey cues are not sufficient. In the light of recent observations on how garter and water snakes (Nerodia) forage, new tests were made of the role of visual stimuli in the aquatic predation of several natricine species. Both experienced and ingestively naive snakes oriented to and attacked a fish model in plain water, although they made more orientations and attacks when diffuse fish odour was present in the water. Fish odour in water also elicited increased aquatic searching behaviour. Early views on the role of vision in the predation of newborn natricine snakes require modification, and there is a need for investigation of the properties of effective visual stimuli and the ontogeny of responsiveness to them.     

Family, sex and testosterone effects on garter snake behaviour

To better understand how genes and hormones interact to affect behaviour in nature, I used a factorial design to test for effects of family membership, sex and testosterone level on activity and defensive behaviour of the common garter snake, Thamnophis sirtalis. Behaviours (latency to move, defensive strikes, response distance) were scored prior to hormone manipulation (when snakes were 39 days of age), while sham or testosterone-containing implants were in place (190 days), following implant removal and simulated hibernation (284 days), and when snakes were 428 days of age. Family membership had pervasive effects on all three behaviours and on their ontogenetic trajectories, suggesting strong genetic or maternal components to behavioural variation. Sex had a significant effect on the number of defensive strikes; females struck more frequently than males, but ontogenetic trajectories were similar between the sexes. Testosterone manipulation also had an effect on strikes: snakes in the elevated-testosterone treatment group struck less frequently than shams while implants were in place. Sex and treatment effects on latency to move and response distance were lacking. Family*treatment interaction effects were lacking for latency to move and number of defensive strikes but were present for response distance. Possibly, genetic or maternally induced variation in strikes is mediated through variation in circulating hormone levels, whereas variation in response distance is mediated through receptor-level phenomena. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Conflicts between courtship and thermoregulation: the thermal ecology of amorous male garter snakes (Thamnophis sirtalis parietalis, colubridae)

Thermoregulatory behavior is an important component of daily activities for many reptiles, especially for small heliothermic (sun-basking) species that inhabit cold climates. However, the relative costs and benefits of thermoregulation depend on numerous factors, such that reptiles may sometimes accord a low priority to precise control of body temperatures. We observed and radio tracked garter snakes (Thamnophis sirtalis parietalis) in central Manitoba during the mating season (spring). Previous studies on this species have documented precise behavioral regulation of body temperatures during summer. In contrast, the courting snakes that we studied in springtime spent little time in overt thermoregulatory behavior. Body temperatures were extremely variable (both in outdoor enclosures and in the field) despite abundant opportunities for more precise thermal control. These small elongate reptiles cool so quickly (relative to the time periods needed for effective courtship) that any benefit to higher body temperatures would be transitory at best. Experiments show that hotter males are no better at obtaining matings or at detecting predators. Thus, male garter snakes concentrate on courtship rather than on basking. In the face of conflicting priorities, reptiles may often forgo precise thermoregulation because its benefits are too low, and its costs too high, compared with alternative behaviors.     

The ecological consequences of unpalatable prey: phytoplankton response to nutrient and predator additions

Thermoregulation is thought to be the most important factor influencing habitat selection by terrestrial ectotherms, at least in temperate climates. The cost-benefit model of thermoregulation predicts that ectotherms should invest more in thermoregulation when the costs of doing so are low (when the thermal quality of the habitat is high). However, the extent to which ectotherms vary their thermoregulatory behaviour according to the thermal quality of habitats is currently unknown. We studied the relationship between habitat use and thermoregulation in 53 black rat snakes using temperature-sensitive radio-transmitters. Among the habitats available to black rat snakes, edges had the highest thermal quality, retreat sites and forest were intermediate, and open habitats had the lowest thermal quality. Black rat snakes experienced more favourable body temperatures while in barns (retreat sites) than in edges, and in edges than in forest. During the day, the effectiveness and the extent of thermoregulation by the snakes were equal in barns and forest, but much lower in edges. In fact, black rat snakes selected thermally favourable microhabitats less than their availability while in edges. Therefore, more favourable body temperatures were not necessarily achieved in thermally superior habitats by increased thermoregulation, but simply because favourable temperatures were encountered more often in those habitats. This result is contrary to the central prediction of the cost-benefit model of thermoregulation and we suggest that this model should be modified to put more emphasis on other costs of thermoregulation, such as increased predation risk or lost foraging opportunities.     

Arboreal ambush site selection by pit-vipers Gloydius shedaoensis

For a sit-and-wait predator, the choice of ambush site may be a crucial determinant of foraging success. During fieldwork on a small island in northeastern China, we explored the availability and use of arboreal ambush sites (tree branches) selected by Shedao pit-vipers, Gloydius shedaoensis. The snakes were highly selective at a variety of spatial scales. For example, they displayed strong biases in terms of which tree species were used, which individual trees within each species were used and which branches were used within a tree. Snakes disproportionately used trees that were on the edge rather than the interior of thickets, and branches that faced out towards the clearing rather than back towards the thicket. Branches at an angle slightly above horizontal were preferred. The snakes used branches visited at high rates by potential prey, that provided effective camouflage, and with thermal and visual backgrounds (cool, bright) that contrasted strongly with avian prey items (hot, dark). The snakes used perches close to the ground (the area of greatest bird activity) despite suboptimal visual and thermal backgrounds. Use of thicker branches by larger snakes, and by snakes containing recently ingested prey items, may contribute to effective camouflage. Thermoregulation did not appear to influence foraging site selection.     

A novel mechanism regulating a sexual signal: The testosterone-based inhibition of female sex pheromone expression in garter snakes

Vertebrates communicate their sex to conspecifics through the use of sexually dimorphic signals, such as ornaments, behaviors and scents. Furthermore, the physiological connection between hormones and secondary sexual signal expression is key to understanding their dimorphism, seasonality and evolution. The red-sided garter snake (Thamnophis sirtalis parietalis) is the only reptile for which a described pheromone currently exists, and because garter snakes rely completely on the sexual attractiveness pheromone for species identification and mate choice, they constitute a unique model species for exploring the relationship between pheromones and the endocrine system. We recently demonstrated that estrogen can activate female pheromone production in male garter snakes. The purpose of this study was to determine the mechanism(s) acting to prevent female pheromone production in males. We found that castrated males (GX) are courted by wild males in the field and produce appreciable amounts of female sex pheromone. Furthermore, pheromone production is inhibited in castrates given testosterone implants (GX + T), suggesting that pheromone production is actively inhibited by the presence of testosterone. Lastly, testosterone supplementation alone (T) increased the production of several saturated methyl ketones in the pheromone but not the unsaturated ketones; this may indicate that saturated ketones are testosterone-activated components of the garter snake's skin lipid milieu. Collectively, our research has shown that pheromone expression in snakes results from two processes: activation by the feminizing steroid estradiol and inhibition by testosterone. We suggest that basal birds and garter snakes share common pathways of activation that modulate crucial intraspecific signals that originate from skin.     

Temperature-limited Activity in the Garter Snake Thamnophis melanogaster (Colubridae)

Many garter snakes, Thamnophis melanogaster, at a desert pond first started foraging for tadpoles when mean water surface temperature was about 20 °C (at 0945–1015 h), and the number of snakes tripled when water temperature reached about 24 °C (at 1100–1130 h). In two years, snakes foraged in April and May, but not in March when water never reached 23 °C and only exceeded 20 °C for a few hours after the usual foraging hours. Snakes in the laboratory dedicated increasing amounts of time to underwater foraging as air and water temperatures increased from 9 °C to 29 °C, and their rate of attacks on fish increased steeply and progressively above an apparent threshold lying between roughly 19 °C and 24 °C, up to at least 29 °C. Temperature may limit T. melanogaster's foraging at the pond to the hours after roughly 0900 h and to the period after roughly March, despite evidence that prey abundance is maximal in March.     

Helminth infracommunity structure of the sympatric garter snakes Thamnophis eques and Thamnophis melanogaster from the Mesa Central of Mexico

Seventy-two Mexican garter snakes (Thamnophis eques) and 126 black-bellied garter snakes (T. melanogaster) were collected from 4 localities of the Mesa Central of Mexico between July 1996 and February 1998 and examined for helminths. Both species of garter snakes occurred sympatrically in every locality except in Lake Cuitzeo. Both species of snakes shared 9 helminth species, and in general, T. melanogaster hosted a larger number of species than T. eques. In each locality, a different helminth species showed the highest levels of prevalence and abundance (Spiroxys susanae in Ciénaga de Lerma, Telorchis corti in Lago de Pátzcuaro, Proteocephalus variabilis in Lago de Cuitzeo, and Contracaecum sp. in Lago de Chapala). Helminth communities in garter snakes of the Mesa Central are depauperate and dominated by a single parasite species. In those localities where the snakes occurred in sympatry, helminth communities were, in general, more diverse and species-rich in T. melanogaster. Differences in the ecology and physiology of these species of garter snakes may explain this pattern because black-bellied garter snakes (T. melanogaster) are more aquatic than Mexican garter snakes (T. eques) and primarily eat aquatic prey, potentially exposing themselves to a larger number of helminths transmitted by predator-prey infection. The helminth infracommunities of garter snakes in the Mesa Central of Mexico show a strong Nearctic influence because most of the species infecting these hosts have been recorded in other Nearctic colubrid snakes. However, the helminth infracommunities of these garter snakes are less species-rich and less diverse than those in colubrid snakes in more temperate latitudes. The widespread ecological perturbation of sampling sites in the Mesa Central because of human activity, and geographic differences in foraging ecology of the hosts and, thus, exposure to parasites transmitted by intermediate hosts may help to explain these patterns.     

A test of the thermal coadaptation hypothesis with black rat snakes (Elaphe obsoleta) and northern water snakes (Nerodia sipedon)

• 1.The thermal coadaptation hypothesis predicts that (1) ectotherms experiencing a narrow range of body temperatures in the wild will evolve to perform well over a narrow range of body temperatures and that (2) the optimal temperature for performance will be equal to the preferred body temperature of the species.
• 2.We tested the predictions of the thermal coadaptation hypothesis with black rat snakes (Elaphe obsoleta) and northern water snakes (Nerodia sipedon) because black rat snakes experience lower and more variable body temperatures than northern water snakes at our study site.
• 3.We measured swimming speed, tongue-flicking speed, and striking speed in black rat snakes, and swimming speed and tongue-flicking speed in northern water snakes.
• 4.Adult water snakes generally had narrower performance breadths and higher optimum performance temperatures than adult black rat snakes.
• 5.Performance breadths were the same for swimming, tongue flicking, and striking within adult black rat snakes, but performance optima for these behaviours differed significantly. Performance breadths differed and performance optima were the same for swimming and tongue flicking within adult northern water snakes.
• 6.The relative swimming performance of neonates of the two species was similar in breadth to that of adults, but the thermal optimum for neonate black rat snakes was higher than that of adults.
• 7.Overall, our results provided support for the thermal coadaptation hypothesis.

     

Behavioural variation in natural populations. III: Antipredator displays in the garter snake Thamnophis radix

Recently born garter snakes (Thamnophis radix) were subjected to a variety of threatening stimuli. The would crawl away from the investigator until high levels of lactate were attained, and then adopt one of a variety antipredator displays. These antipredator behaviours were surprisingly variable between individuals of a single population, but behaviours of individuals were consistent in replicate trials and in response to different stimuli. Snakes became more defensive when simulated predator attacks were more severe, but they became more offensive when tested at a lower temperature. Analysis of behavioural variation within and between 15 litters of full-sibling (172) snakes gave heritability estimates of 0.37 for single trials and 0.45 for the average of two replicate trials. This is the first study to examine the heritability of antipredator behaviour in any terrestrial vertebrate species.     

Testing an Adaptive Hypothesis Through Context-Dependence: Effects of Water Depth on Foraging Behaviour in Three Species of Garter Snakes

Adaptive hypotheses based on interspecific comparisons can be tested by evaluating the context‐dependence of the behaviour of individual organisms. Drummond (Behaviour, 86, 1983, 1) categorized garter snake species (Thamnophis) as terrestrial–aquatic generalists or aquatic specialists based on diet and aquatic foraging behaviour. He hypothesized that the characteristic foraging behaviours of aquatic specialists – including frequent crawling on the underwater substrate and a high rate of underwater predatory strikes – are adaptations for feeding on relatively widely dispersed aquatic prey. Drummond's hypothesis based on interspecific comparisons suggests that individual snakes might change their foraging in the direction of aquatic specialist behaviour with an increase in water depth (which increases prey dispersion). I tested this prediction through laboratory observations of Mexican Pacific lowlands garter snakes (T. validus) feeding on minnows in shallow (2 cm) and deep (3–7 cm) water. Members of this species are appropriate subjects because they are ecologically intermediate between the generalists and aquatic specialists studied by Drummond, and thus might be expected to show more variation in aquatic foraging behaviour than those species. T. validus showed significantly higher frequencies of crawling on the underwater substrate and of underwater strikes in the deep water than in the shallow water; i.e. increased water depth shifted the behaviour of these snakes toward that of aquatic specialists, thus supporting Drummond's hypothesis. Individuals of an aquatic specialist species, the narrow‐headed garter snake (T. rufipunctatus), showed less pronounced changes in behaviour with increased water depth. Western ribbon snakes (T. proximus), which feed primarily at the land–water interface (and are expected to act like terrestrial–aquatic generalists), typically refused to feed in deep water. Interspecific differences in underwater visual acuity may underly the behavioural differences among the three species by determining whether changes in foraging behaviour with water depth are advantageous. Information on phylogenetic relationships suggests that the facultative behaviour of T. validus may represent an intermediate stage in the evolution of aquatic specialization.     

Hibernation in garter snakes (Thamnophis sirtalis parietalis): seasonal cycles of cold tolerance

1. The red-sided garter snake hibernates for about six months each year in Manitoba, Canada, where winter temperatures are often as low as -40 degrees C. Mammalian hibernators typically undergo profound changes in preparation for hibernation, but little is known about corresponding changes in reptiles. 2. We tested the importance of seasonal changes in the ability of red-sided garter snakes to hibernate successfully by exposing them to winter conditions at different times of year. 3. Animals that began hibernation in the fall were more likely to survive hibernation than animals that began hibernation in either early or late summer, despite the fact that the animals were kept on seasonally constant conditions prior to hibernation. 4. We suggest that these changes are derived from endogenous components of the yearly hibernation cycle of red-sided garter snakes but that only part of the cycle proceeds endogenously, i.e. it is not a completely endogenous circannual cycle.     

Behavioural and hormonal responses to capture stress in the male red-sided garter snake, Thamnophis sirtalis parietalis

We measured the behavioural and hormonal responses to capture stress in male red-sided garter snakes. Four hours of capture stress resulted in no suppression of mating behaviour relative to control individuals. In contrast, the same stress resulted in a significant increase in plasma levels of corticosterone and a significant decrease in plasma levels of testosterone. There was a significant negative correlation between plasma levels of corticosterone and testosterone in both control and capture-stress groups, suggesting that the increase in corticosterone directly drives the decrease in testosterone. While there was no relation between body size and initial plasma levels of the two steroids, longer individuals had a significantly greater increase in corticosterone following capture stress than did shorter individuals. Snakes display indeterminate growth, suggesting that older individuals have decreased sensitivity to negative feedback in the hypothalamic-pituitary-adrenal axis and thus hypersecrete glucocorticoids. These results suggest that male red-sided garter snakes have uncoupled their behavioural stress response from their hormonal stress response to maximize reproductive opportunities. Copyright 2000 The Association for the Study of Animal Behaviour.     

Environmental and seasonal adaptations of the adrenocortical and gonadal responses to capture stress in two populations of the male garter snake, Thamnophis sirtalis

Stress and reproduction are generally thought to work in opposition to one another. This is often manifested as reciprocal relationships between glucocorticoid stress hormones and sex steroid hormones. However, seasonal differences in how animals respond to stressors have been described in extreme environments. We tested the hypothesis that garter snakes, Thamnophis sirtalis, with limited reproductive opportunities will suppress their hormonal stress response during the breeding season relative to conspecifics with an extended breeding season. The red-sided garter snake, T.s. parietalis, of Manitoba, Canada, has a brief breeding season during which males displayed no change in either plasma levels of testosterone or corticosterone, which were both elevated above basal levels, in response to capture stress. During the summer, capture stress resulted in increased plasma corticosterone and decreased testosterone. During the fall, when mating can also occur, males exhibited a significant decrease in testosterone but no increase in corticosterone in response to capture stress. The red-spotted garter snake, T.s. concinnus, of western Oregon, has an extended breeding season during which males displayed a stress response of increased plasma corticosterone and decreased testosterone levels. The corticosterone response to capture stress was similar during the spring, summer, and fall. In contrast, the testosterone response was suppressed during the summer and fall when gametogenesis was occurring. These data suggest that male garter snakes, in both populations, seasonally adapt their stress response but for different reasons and by potentially different mechanisms. J. Exp. Zool. 289:99-108, 2001.