Michael P. LeMaster

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.

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

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.

Body size enhances mating success in male garter snakes

n many kinds of animals, larger males tend to defeatsmaller rivals in bouts of physical combat and maythereby enhance their mating opportunities. Does largerbody size also enhance male mating success in speciesthat do not display overt male–male combat? The onlydetailed evidence on this topic for snakes comes from astudy on red-sided garter snakes,

REPRODUCTIVE ISOLATING MECHANISMS BETWEEN TWO SYMPATRIC SIBLING SPECIES OF SEA SNAKES

Abstract Mechanisms that maintain species isolation within sympatric congeners have attracted analysis in many kinds of organisms, but not in snakes. We studied two sibling species of amphibious sea snakes (Laticauda colubrina and L. frontalis) on the island of Efate, in the Pacific Ocean republic of Vanuatu. The two taxa are almost identical morphologically, except that L. colubrina grows much larger than L. frontalis. No natural hybrids have been reported, and geographic distributions of the two taxa suggest the possibility of sympatric speciation. Our fieldwork shows that the two taxa are often syntopic and overlap in breeding seasons. Behavioral studies in outdoor arenas show that the separation between these two taxa is maintained by species‐specific cues that control male courtship. Males of both species courted conspecific females but not heterospecific females. The proximate mechanism driving this separation involves chemical cues. Adult females of both taxa possess distinctive lipids in the skin. Males directed courtship behavior (chin‐pressing) to hexane‐extracted samples of lipids from conspecific but not heterospecific females. Males of the dwarf species (L. frontalis) were more selective courters than were those of the larger taxon (L. colubrina), perhaps because a preference for courting larger females means that L. colubrina males would be unlikely to court L. frontalis—sized (i.e., small) females even in the absence of pheromonal barriers.

Why do male snakes have longer tails than females

In most snake species, males have longer tails than females of the same body length. The adaptive significance of this widespread dimorphism has attracted much speculation, but few tests. We took advantage of huge mating aggregations of red–sided gartersnakes (Thamnophis sirtalis parietalis) in southern Manitoba to test two (non–exclusive) hypotheses about the selective forces responsible for this dimorphism. Our data support both hypotheses. First, relative tail length affects the size of the male copulatory organs (hemipenes). Males with longer tails relative to body length have longer hemipenes, presumably because of the additional space available (the hemipenes are housed inside the tail base). Second, relative tail length affects male mating success. Males with partial tail loss (due to predation or misadventure) experienced a threefold reduction in mating success. Among males with intact tails, we detected strong stabilizing selection on relative tail length in one of the two years of our study. Thus, our data support the notion that sex divergence in tail length relative to body length in snakes reflects the action of sexual selection for male mating success.

Chemosensory cues allow courting male garter snakes to assess body length and body condition of potential mates

When choosing between two potential mates, a male may benefit by picking a larger (longer and/or more heavy-bodied) female because she is likely to produce more or larger offspring. Males of many species use visual cues to evaluate the sizes of their mates, but in some situations (at night or in a crowded mating swarm), vision may be useless. Potentially, males may be able to use chemical cues that convey information about female body size. We manipulated cues available to free-ranging male garter snakes (Thamnophis sirtalis parietalis) in large courting aggregations near communal dens in Manitoba, Canada. Males not only directed disproportionate courtship to longer and heavier-bodied females, but also courted most vigorously in response to lipids extracted from the skins of such females. Our data show that with a flick of his tongue, a male garter snake can identify not only a females body length, but also her body condition.

Conspecific trailing behaviour of red-sided garter snakes, Thamnophis sirtalis parietalis, in the natural environment

The ability of animals to orient based on pheromonal cues in the environment can have significant consequences to their reproductive success and survival. For example, it is hypothesized that snakes use pheromone trails to locate potential mates during the breeding season and to locate winter hibernacula. Numerous studies have demonstrated that snakes are capable of detecting and following pheromone trails in the laboratory, but it has yet to be shown experimentally whether snakes use such behaviour in their natural environment. In this study, we conducted trailing experiments to test the response of adult red-sided garter snakes to pheromone trails on the natural substrate under naturally occurring conditions during two periods, the spring breeding season and the autumn migration back to the hibernacula. Male snakes detected and followed female trails in the spring, while neither sex displayed trailing behaviour during the period of autumn migration. Our results suggest that adult garter snakes use pheromone trails for locating potential mates during the breeding season and most likely rely on other mechanisms (e.g. visual cues) for navigation to overwintering hibernacula.

PHEROMONALLY MEDIATED SEXUAL ISOLATION AMONG DENNING POPULATIONS OF RED-SIDED GARTER SNAKES, Thamnophis sirtalis parietalis

Utilizing behavioral experiments and chemical analyses, we examined whether pheromonally mediated sexual isolation exists between denning populations of red-sided garter snakes (Thamnophis sirtalis parietalis) in Manitoba, Canada. Simultaneous choice tests conducted during the breeding season revealed that adult males from a hibernaculum in central Manitoba displayed a strong courtship preference for females from their own population over females from a hibernaculum in western Manitoba, whereas males from the western Manitoba hibernaculum showed no such preference. In addition, trailing experiments testing the response of males from the two hibernacula to familiar and unfamiliar female trails showed similar results, demonstrating that the observed male preference is mediated through chemical cues. Subsequent chemical analysis of the female sexual attractiveness pheromone, a homologous series of long-chain saturated and ω-9 cis-unsaturated methyl ketones responsible for eliciting male courtship behavior and trailing behavior in garter snakes, showed significant variation in the composition of the pheromone between the two populations. Specifically, the two populations varied in the relative concentrations of individual unsaturated methyl ketones expressed by females. These results suggest that sexual isolation exists to a degree among denning populations of red-sided garter snakes due to variation in the expression of the female sexual attractiveness pheromone.