Robert T. Mason

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.

Social behavior and pheromonal communication in reptiles.

The role of pheromones in orchestrating social behaviors in reptiles is reviewed. Although all reptile orders are examined, the vast majority of the literature has dealt only with squamates, primarily snakes and lizards. The literature is surprisingly large, but most studies have explored relatively few behaviors. The evolution of chemical signaling in reptiles is discussed along with behaviors governed by pheromones including conspecific trailing, male-male agonistic interactions, sex recognition and sex pheromones, and reptilian predator recognition. Nonreptilian prey recognition by chemical cues was not reviewed. The recent literature has focused on two model systems where extensive chemical ecology studies have been conducted: the reproductive ecology of garter snakes and the behavioral ecology of Iberian lacertid lizards. In these two systems, enough is known about the chemical constituents that mediate behaviors to explore the evolution of chemical signaling mechanisms that affect life history patterns. In addition, these models illuminate natural and sexual selection processes which have lead to complex chemical signals whose different components and concentrations provide essential information about individuals to conspecifics. Reptiles provide excellent candidates for further studies in this regard not only in squamates, but also in the orders where little experimental work has been conducted to date.

Plasma steroid hormone levels of female red-sided garter snakes, Thamnophis sirtalis parietalis: Relationship to mating and gestation

Plasma levels of progesterone (P), testosterone (T), estradiol (E2), and corticosterone (B) of female red-sided garter snakes were measured during the period of ovarian development. Differences in hormone levels were analyzed with respect to three factors: whether the female mated in the spring, ovarian condition, and time after emergence from hibernation. The influence of these three factors on steroid hormone levels of two groups of females were then compared. In experiment I, females were obtained in the fall, subjected to an artificial dormancy period, and placed on warm, summer-like conditions in the laboratory. In experiment II, females were collected in the spring and sampled in the field. They were held in the field on fluctuating conditions for several weeks and then returned to the laboratory for sampling during early vitellogenesis. Females in experiment I had a shortened but otherwise normal ovarian and gestational cycle, whereas females in experiment II had an ovarian and gestational cycle typical of females in the field. In spite of these differences, the steroid hormone levels in relation to the ovarian cycle were remarkably similar for the two groups of females. We confirmed that mating in the spring induces a surge in E2; E2 also was elevated in a single sample obtained from animals collected in the fall. This elevation in plasma levels of E2 in the fall occurs at a time when the majority of females have recently deposited sperm in their oviducts. Plasma levels of T, P, and B were not significantly influenced by mating. Unlike previous reports of other viviparous snakes, plasma levels of P were low and mostly nondetectable, even during late gestation. Plasma T was significantly elevated around the time of late vitellogenesis and ovulation, and there was a tendency for E2 levels to be elevated at this time. In the field, plasma B levels were initially high immediately after capture and declined with time. Plasma B was significantly elevated in all females several weeks after emergence, suggesting that levels of B may vary with other annual cycles.

Relationships between annual cycles of testosterone, corticosterone, and body condition in male red-spotted garter snakes, Thamnophis sirtalis concinnus.

Over a 2‐yr period, we investigated the annual cycles of plasma testosterone and corticosterone and the relationships between these hormones and body condition in a wild population of male red‐spotted garter snakes, Thamnophis sirtalis concinnus. In the 10 mo that were sampled, a peak in testosterone was observed in late summer during gametogenesis and declining through the spring breeding period. Corticosterone and testosterone cycles were positively correlated, in contrast to many vertebrates, suggesting the lack of a direct negative interaction between the two hormones. Body condition, defined as the residual of the regression of mass on snout‐vent length, also cycled annually, with individuals being more robust during the summer than during the spring or fall. Individuals with a positive body condition had significantly lower plasma levels of corticosterone than did individuals with a negative body condition, supporting the energetic role of glucocorticoids. There was no relationship between body condition and testosterone. This study suggests that annual cycles of testosterone, corticosterone, and body condition can be associated with one another, and considering all three simultaneously is necessary to understand their control and function.

Hormonal independence of courtship behavior in the male garter snake

Garter snakes exhibit a dissociated reproductive tactic in which gonadal activity is minimal at the time of mating, increasing only after the breeding season has ended. Experiments are presented demonstrating that neither short-term nor longterm castration affects courtship behavior in adult male red-sided garter snakes (Thamnophis sirtalis parietalis). So long as males have passed through a low-temperature dormancy period (hibernation), castration either shortly after emergence in the spring, or before entering winter dormancy in the fall, does not prevent the display of intense courtship behavior on emergence. Similarly, males castrated during mating activity the previous spring prior to the annual testicular growth phase actively courted females on emergence from hibernation. Males adrenalectomized and castrated during low-temperature dormancy also courted females on emergence. Hypophysectomy during or before low-temperature dormancy did not prevent males from displaying high-intensity courtship behavior on emergence from hibernation. Treatment with sex steroid hormones, as well as hypothalamic and pituitary hormones, and a variety of neural and metabolic affectors also fails to elicit courtship behavior in noncourting males during the summer. It was concluded that causal mechanisms controlling courtship behavior in the red-sided garter snake are fundamentally different, at least at the physiological level, from those mechanisms described for many laboratory and domesticated species.

Chastity belts in gartersnakes: the functional significance of mating plugs

Male red-sided gartersnakes (Thamnophis sirtalis parietalis) deposit a thick gelatinous plug that occludes the female cloaca after copulation. Previous workers have interpreted the plug as a sexually-selected adaptation to (1) physically prevent re-mating by the female, and/or (2) provide pheromonal cues to discourage courtship by rival males or to decrease receptivity by females. Our data support the former hypothesis, but not the latter. Plugs serve as effective physical barriers to additional copulation for <72 h, but this is long enough for most females to become unreceptive, and/or disperse from the mating aggregation. Experimental removal of plugs immediately after copulation results in some re-mating by females, but plug removal several hours later does not rekindle sexual receptivity. Contrary to previous work, our experiments show that fluids associated with copulation (rather than the plug per se) are responsible for the rapid decline of male interest in mated females. Thus, the plug’s primary function is to physically prevent matings rather than as a source of pheromonal cues to manipulate the behaviour of females or rival males. Plug mass is determined not only by a male’s body size, but by his prior mating history (plug mass decreases with repeated mating) and by the size of his partner (males allocate larger plugs to larger females). Gartersnakes are unusual not only in their production of mating plugs, but also in their brief duration of copulation compared to other snakes. Mating plugs may have evolved in gartersnakes to reduce mating times, because of the extremely high ‘opportunity cost’ of prolonged mating to a male gartersnake in a mating aggregation.

Pick on someone your own size: ontogenetic shifts in mate choice by male garter snakes result in size-assortative mating

Data on over 950 natural matings of red-sided garter snakes, Thamnophis sirtalis parietalis, in Manitoba revealed size-assortative pairing: large males tended to mate with large females, and small males with small females. Unlike previously reported cases of size-assortative mating, the causal mechanism in these snakes involved a size-related shift in active mate selection by males. In the field, courtship as well as mating was size assortative (albeit, with considerable scatter around the trend line). Staged trials in outdoor arenas showed that males of all sizes preferred to court large rather than small females, but this preference was stronger in large males. Males adjusted their courtship intensity in response to the numbers and sizes of females and competing males, but did not change their preferences with respect to female body size. Thus, size-assortative mating was not a direct consequence of large males excluding their smaller rivals from large females. Males may be selective courters in this species because they have a limited supply of sperm and mating plugs, and hence can copulate effectively only a few times within the mating season. Given intense competition from large males (which primarily court large females), small males may benefit from focusing on small females. Alternatively, small males may be less capable of inducing sexual receptivity from large females. Mark–recapture data confirmed that males grow rapidly from one year to the next. Thus, the size-related shift in male mate choice was due to an ontogenetic change rather than the existence of multiple male morphs differing in both body size and courtship preference.  2001 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.

VARIATION IN A FEMALE SEXUAL ATTRACTIVENESS PHEROMONE CONTROLS MALE MATE CHOICE IN GARTER SNAKES

Male red-sided garter snakes (Thamnophis sirtalis parietalis) display a courtship preference for larger females during the breeding season. Utilizing behavioral experiments and chemical analyses, we tested the hypothesis that males can discriminate among females of varying size solely by means of the sexual attractiveness pheromone, a previously characterized sex pheromone composed of a homologous series of long-chain saturated and ω-9 cis-unsaturated methyl ketones contained in the skin lipids of females. When presented with skin lipid extracts from large and small females, a greater proportion of males displayed courtship behaviors to large female extracts. This demonstrates that there is an intrinsic property of the female skin lipids that allows males to differentiate among large and small females. Analysis of the sexual attractiveness pheromone revealed that the necessary variation exists for this pheromone to function as a reliable indicator to males of female body size. Specifically, we observed a strong correlation between female snout–vent length and the relative concentration of saturated and ω-9 cis-unsaturated methyl ketones composing the pheromone; smaller females expressed pheromone profiles higher in saturated methyl ketones, while larger females expressed pheromone profiles dominated by unsaturated methyl ketones. The results of this study suggest that male red-sided garter snakes utilize compositional variation in the female sexual attractiveness pheromone to differentiate among potential mates of varying size.

Why Did the Snake Cross the Road? Effects of Roads on Movement and Location of Mates by Garter Snakes (Thamnophis sirtalis parietalis)

If animals avoid road surfaces or are unable to follow conspecific trails across such surfaces, previously continuous populations may be fragmented. We gathered data on the effects of a small (4-m wide) gravel road on the behavior and trail-following abilities of garter snakes (Thamnophis sirtalis parietalis) in Manitoba, central Canada. As expected, the road surface had less vegetation cover, a more open canopy and, thus, higher incident radiation than did the surrounding grassland. Contrary to expectations, however, substrate temperatures were lower on the road than in its surrounds, because of the higher reflectivity of the roads surface. On a nearby asphalt road, substrate temperatures were relatively high on the road surface only in the evening, as surrounding areas cooled. Focal sampling showed that snakes avoided the gravel road, typically changing direction when they encountered it. If they crossed the road, they did so by the shortest possible route (straight across). Mate-searching male snakes were less able to follow substrate-deposited pheromonal trails left by females if those trails crossed a road than if the trails were entirely within the surrounding grassland. Thus, roads may significantly modify snake movement patterns, as well as the ability of males to locate reproductive females. Our study provides the first detailed information on the effects of roads on snake behavior.