Thamnophis Sirtalis Research Articles

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,

Activity Patterns of Garter Snakes, Thamnophis sirtalis, in Relation to Weather Conditions at a Fish Hatchery on Vancouver Island, British Columbia

Activity Patterns of Garter Snakes, Thamnophis sirtalis, in Relation to Weather Conditions at a Fish Hatchery on Vancouver Island, British Columbia

The transvestite serpent: why do male garter snakes court (some) other males?

In large mating aggregations of red-sided garter snakes, Thamnophis sirtalis parietalis, in Manitoba, male courtship is directed not only to females, but also to other males with female-like skin lipids (‘she-males’). We show that ‘she-maleness’ is an intrinsic property of a male rather than an artefact of lipid transfer from females, and that male–male courtship is very common in the field. She-males were distinctive in terms of appearance (they were heavier than other males and more often covered with mud), behaviour (they were inactive and rarely courted females) and performance (they were slow crawlers, ineffective courters and easily outcompeted by other males in mating trials). ‘She-maleness’ was not a characteristic of a particular subset of males, as envisaged in previous work; instead, it was a transitory phase that most (perhaps all) male snakes passed through soon after they first emerged from the winter den. Recently emerged males spent their first day or two relatively inactive, while restoring physiological functions (including locomotor performance and courtship ability). Experimental application of female skin lipids on to males dramatically decreased courtship levels of the recipient snakes. Thus, recently emerged males may derive two kinds of benefit from mimicking female skin lipids. First, female mimicry ‘switches off’ the male's own (energetically expensive) courtship at a time when that courtship would be unproductive. Second, it may disadvantage his rivals by distracting them from females, and increasing their energy expenditure.

THE PROBLEM WITH COURTING A CYLINDRICAL OBJECT: HOW DOES AN AMOROUS MALE SNAKE DETERMINE WHICH END IS WHICH?

[In order to achieve copulation, a male snake must align his body in the same direction as his mate. This may not be a trivial problem in an elongate limbless animal, especially when the male is much smaller than the female (and hence, his head is far from hers) and when she is simultaneously being courted by many other males (so that much of her body is not visible). This is exactly the situation experienced by red-sided gartersnakes ( Thamnophis sirtalis parietalis ) at communal dens in Manitoba. To clarify this question, we modified cues available to males by manipulating various attributes of females (direction of movement, presence of head and tail, concentration of sex pheromones, etc.). Male alignment during courtship does not depend on the visual stimulus provided by the female′s head or tail. Instead, male alignment is influenced by the female′s direction of movement, and by pheromonal stimuli from her skin. We suggest that courting male snakes obtain directional information via their characteristic 'chin-pressing′ behaviour. By pressing firmly on each scale with his chin as he passes over it, a male moving anteriorly (but not posteriorly) along the female′s body will open a small gap between that scale and the next most anterior one. This gap enables his tongue-tips to penetrate more easily towards the scale-hinge area (overlain by the more anterior scale) where sex pheromones are concentrated. Thus, the direction of scale overlap provides pheromonal as well as physical cues that permit males to align correctly for copulation., In order to achieve copulation, a male snake must align his body in the same direction as his mate. This may not be a trivial problem in an elongate limbless animal, especially when the male is much smaller than the female (and hence, his head is far from hers) and when she is simultaneously being courted by many other males (so that much of her body is not visible). This is exactly the situation experienced by red-sided gartersnakes ( Thamnophis sirtalis parietalis ) at communal dens in Manitoba. To clarify this question, we modified cues available to males by manipulating various attributes of females (direction of movement, presence of head and tail, concentration of sex pheromones, etc.). Male alignment during courtship does not depend on the visual stimulus provided by the female′s head or tail. Instead, male alignment is influenced by the female′s direction of movement, and by pheromonal stimuli from her skin. We suggest that courting male snakes obtain directional information via their characteristic 'chin-pressing′ behaviour. By pressing firmly on each scale with his chin as he passes over it, a male moving anteriorly (but not posteriorly) along the female′s body will open a small gap between that scale and the next most anterior one. This gap enables his tongue-tips to penetrate more easily towards the scale-hinge area (overlain by the more anterior scale) where sex pheromones are concentrated. Thus, the direction of scale overlap provides pheromonal as well as physical cues that permit males to align correctly for copulation.]

Ovarian Teratoma in a Garter Snake, Thamnophis sirtalis

ABSTRACT A common garter snake, Thamnophis sirtalis, was presented for coelomic swelling. Exploratory surgery revealed an irregular, lobulated mass approximately 1.75 cm in diameter that was subsequently diagnosed histologically as a teratoma. Teratomata have previously been diagnosed in a variety of species including primates, equines, canines, felines, rodents, birds, amphibians and reptiles. However, teratomata in reptiles have been previously diagnosed only in green iguana, Iguana iguana, and the desert grassland whiptail, Cnemidophorus uniparens. This case report documents the first teratoma diagnosed in a garter snake. Following surgical removal of the neoplasm, the snake made a complete, uneventful recovery.

The genetics of dietary experience in a restricted natural population.

The sources of individual differences in human and non-human animals remain controversial. We demonstrate that diet and genetics interact in determining the ontogenetic trajectory of chemosensory and prey preferences in the common garter snake, Thamnophis sirtalis, a dietary generalist. In litters of neonate snakes from a single small field in an earthworm-ingesting population, initial responses to chemical cues from fish and worm were similar, with zero heritabilities. After 12 meals on fish, however, the heritability of both fish and worm chemosensory responses increased markedly, the change in response to fish but not worm chemicals was heritable, the relative preference for fish versus worm was heritable, and the change in relative preference was heritable. In addition, growth rates on each diet were related to changes in chemoreceptive responses. Such genetic-environment variation that emerges only after equivalent ontogenetic experience may be a factor in responses to environmental change in many species.

Artificial Cover-Objects as a Method for Sampling Snakes (Contia tenuis and Thamnophis spp.) in British Columbia

Artificial cover provides a potentially useful survey method for reptiles, but little quantitative information exists on the relative attractiveness to snakes of cover-objects made of different materials. From March to November 1997 and 1998 we sampled snakes using artificial cover at 5 sites on the southern Gulf Islands, British Columbia. Each station consisted of 3 cover- objects (dimensions: 0.6 X 0.6 m) arranged either along transects or dispersed throughout suit- able habitat. Each cover-object at individual stations was made of a different material: black asphalt roofing; unpainted, corrugated tin roofing; or plywood. We established 30 cover-object stations at 2 primary sites subjected to intensive study and 55 stations at 3 secondary sites in- spected less frequently. Each of the 4 species of snakes known to occur on the islands used our cover-objects: Thamnophis ordinoides and T elegans used cover-objects at all sites, T. sirtalis at 4 sites, and Contia tenuis at 2 sites. We caught 33 individual C. tenuis 89 times under the covers: 67% of the captures took place under asphalt roofing, 28% under tin roofing, and 5% under plywood. Most observations of C. tenuis under both artificial and natural cover-objects occurred from March to early June and from late September to early November in 1997 and 1998. Tham- nophis ordinoides was the most commonly encountered species under artificial cover with 237 captures (114 individuals) at the primary sites and 1413 captures at the secondary sites. The snakes used asphalt and tin roofing most frequently at the secondary sites (43% of captures each), but their pattern of cover use ranged from a preference for asphalt roofing to no apparent preference at the primary sites. Thamnophis sirtalis and T. elegans occurred most frequently under asphalt and tin roofing with only a few captures under plywood (8% and 7%, respectively). Placements of artificial cover provided an efficient method for locating and recapturing snakes, particularly the secretive species C. tenuis. The relatively high heat conductivity of the asphalt and tin roofing most likely enhanced their attractiveness to both C. tenuis and Thamnophis spp. at our study sites.

Optimization of Predator Avoidance by Salamanders Using Chemical Cues: Diet and Diel Effects

The allocation of time and energy to predator defense is a fundamental problem for animals. Predator avoidance may decrease the risk of injury or mortality, but it may also compromise foraging or reproduction, so potential prey should decide whether to avoid a predator based on predation risk. We show that red-backed salamanders (Plethodon cinereus) discriminate between substrates chemically conditioned by garter snakes (Thamnophis sirtalis) that were fed red-backed salamanders, earthworms, or nothing. At night, individuals avoided only the conspecific treatment, and this response was independent of any individual differences between snakes. During the day when garter snakes are much more active, all treatments were avoided. This avoidance appeared to be influenced by a diel rhythm of responsiveness rather than ambient lighting. Avoidance of prey alarm substances released during predation does not explain all these results, nor can simple avoidance of predator scent. A more complex mechanism is proposed that incorporates predator recognition, predator diet discrimination, and risk assessment. These data suggest that terrestrial salamanders may use chemoreception to identify garter snakes and their diets in order to optimize predator avoidance.

The male tail

In many snakes, males have longer tails than females, a characteristic that seems to have arisen early in evolution. From studies of mating red-sided gartersnakes in Manitoba, Canada, it seems that male tail length correlates with copulation success, but the selective force for longer tails remains a matter of surmise.

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.

A Comparative Study of Facial Grooming after Prey Ingestion in Colubrid Snakes

For a comparative study of facial grooming behavior, we selected five species of colubrid snakes (Thamnophis sirtalis, T. butleri, T. melanogaster, Storeria dekayi, and Cyclophiops semicarinatus) based upon their phylogenetic relationships and natural diets. In an initial descriptive study, head-rubbing behavior reliably followed ingestion of earthworms in all five species. Three forms of head rubbing were identified, including two forms of labial rubbing and one form of rostral area rubbing. The latter occurs during foraging as well as grooming. Two additional controlled experiments were then performed. One experiment assessed the effects of multiple feedings with either normal or immobilized earthworms. The second tested the effects of allowing snakes to contact surface secretions of earthworms and purified mucin without physically contacting the worm. The snakes showed a significantly greater number of head rubs when consuming active earthworms than when consuming immobilized worms, and this increased over the five trials. The snakes also head rubbed more frequently in response to earthworm mucus than to either earthworm surface wash or diluted mucin. The physical properties of earthworm mucus (adhesiveness) thus seem to stimulate head-rubbing behavior. Differences in head rubbing among the species are discussed in relation to natural diet and phylogenetic relatedness. Furthermore, mouth gaping often occurred with head rubbing and can be distinguished from yawning. Tactile and kinesthetic cues associated with this gaping behavior may aid in regulating the occurrence of head rubbing. Neonate snakes head rubbed in a species-typical manner.

EVOLUTIONARY RESPONSE OF PREDATORS TO DANGEROUS PREY: PREADAPTATION AND THE EVOLUTION OF TETRODOTOXIN RESISTANCE IN GARTER SNAKES.

Coevolutionary interactions typically involve only a few specialized taxa. The factors that cause some taxa and not others to respond evolutionarily to selection by another species are poorly understood. Preadaptation may render some species predisposed for evolutionary response to new pressures, whereas a lack of genetic variation may limit the evolutionary potential of other taxa. We evaluate these factors in the predator-prey interaction between toxic newts (Taricha granulosa) and their resistant garter snake predators (Thamnophis sirtalis). Using a bioassay of resistance to tetrodotoxin (TTX), the primary toxin in the prey, we examined phenotypic evolution in the genus Thamnophis. Reconstruction of ancestral character states suggests that the entire genus Thamnophis, and possibly natricine snakes in general, has slightly elevated TTX resistance compared to other lineages of snakes. While this suggests that T. sirtalis is indeed predisposed to evolving TTX resistance, it also indicates that the potential exists in sympatric congeners not expressing elevated levels of TTX resistance. We also detected significant family level variation for TTX resistance in a species of Thamnophis that does not exhibit elaborated levels of the trait. This finding suggests that evolutionary response in other taxa is not limited by genetic variability. In this predator-prey system, species and population differences in resistance appear to be largely determined by variation in the selective environment rather than preadaptation or constraint.

Microsatellite markers and multiple paternity in the garter snake thamnophis sirtalis

Data from four microsatellite loci developed for the common garter snake, Thamnophis sirtalis, show that multiple paternity is common in a natural population on Beaver Island, Michigan. Six of eight litters tested, and all litters with five or more neonates, were multiply sired. At least triple paternity was documented in the largest litter examined (n = 13 neonates). Inheritance patterns and genotype frequencies in the wild population indicate the presence of null allele(s) at one of the microsatellite loci. Garter snakes are widely used in quantitative genetics research, and paternity testing is essential in studies that rely on sibling analysis.

Metabolic costs of growth in free‐living Garter Snakes and the energy budgets of ectotherms

1. The metabolic or respiratory cost of growth (RG) is the increase in metabolic rate of a growing animal, and it represents chemical potential energy expended in support of net biosynthesis but not deposited as new tissue. 2. Two statistical methods (multiple non‐linear regression and analysis of regression residuals) were used to calculate RG from data (n = 68) from a doubly labelled water study of free‐ranging Garter Snakes (Thamnophis sirtalis fitchi) in northern California. 3. The sample‐wise (‘ecological’) cost of growth was 2·07 kJ per gram of net growth (equivalent to 8·63 kJ g–1 dry tissue); reanalysis of a subset of efficient growers yielded a more conservative ‘physiological’ estimate of 1·67 kJ g–1. 4. Our empirical estimate of RG, among the first reported for squamate reptiles and free‐living animals of any kind, compares closely with published, laboratory‐derived values for ectotherms. 5. The metabolic costs of growth accounted for an average of 30% of total field metabolic rates for these snakes, which were growing at a mean rate of 3% of body mass per day. However, our method probably underestimated the total ecological cost of growth for large animals, because potential growth costs that covary with body size were not included. 6. Distinction between conceptual and empirical energy budgets clarifies relationships among body size, metabolic rates, and the physiological and ecological costs of growth.

Repeated Injections of TTX Do Not Affect TTX Resistance or Growth in the Garter Snake Thamnophis sirtalis

The garter snake Thamnophis sirtalis is a known predator of the toxic newt Taricha granulosa. Resistance to the primary toxin of the newt, tetrodotoxin (TTX), varies among individuals and has a genetic basis. We investigated the consequences of longterm exposure to this toxin in an experiment designed to determine (1) whether increased tolerance to tetrodotxin occurs following repeated injections of tetrodotoxin in T. sitralis and (2) whether repeated exposure to tetrodotoxin has an effect on the growth of juvenile snakes. We measured resistance to tetrodotoxin for each individual based on reduction in crawl speed. Pairs of neonatal snakes were chosen based on similar resistance and size and randomly split into two groups, control and experimental. Each group received intraperitoneal injections every two weeks of either saline (control) or tetrodotoxin (experimental) for six months. Mass data were collected five times during the year. Length data were collected twice during the year. After one year, resistance was again measured and compared with neonate resistance. Analyses showed that repeated injections of tetrodotoxin had no effect on resistance or growth.

NADPH-diaphorase and NOS enzymatic activities in some neurons of reptilian gut and their relationships with two neuropeptides.

The distribution of neurons containing the enzymes NADPH-diaphorase (NADPH-d) and nitric oxide synthase (NOS) has been studied in the gastrointestinal tract of lizard (Podarcis s. sicula) and snake (Thamnophis sirtalis). The techniques employed were the NADPH-d/nitroblue tetrazolium histochemical method, and the indirect immunofluorescence applied to cryostat sections and to whole-mount preparations. The colocalization of NADPH-d with NOS, with vasoactive intestinal polypeptide (VIP) and with galanin (Gal) was also studied, and a Western blot analysis using an antibody directed against mammalian Gal was performed on lizard stomach extracts. NADPH-d positive nerve cell bodies and fibres were found in the myenteric and submucous plexuses throughout the gastrointestinal tract of both reptiles. These nerve structures were also present in the other intramural nerve plexuses, although in smaller quantities. Both in lizard and snake, the stomach revealed a positive nerve population that was more dense than elsewhere in the gut. The population of the NADPH-d-positive neurons observed in the lizard was larger than that observed in the snake. The distribution of both populations was similar to those that have been described in the gut of several mammalian and non-mammalian vertebrates. Both in lizard and snake, a one-to-one correspondence was noted between NOS- and NADPH-d-containing nerve cell bodies, and the nitrergic neurons containing Gal appeared to be more numerous than those containing VIP. Western blot analysis recognised a single band with a molecular weight (3.4 kDa) very similar to that of porcine Gal. It is hypothesised that at least some of the nitrergic neurons of the lizard and snake gut are inhibitory motor neurons innervating the circular smooth musculature. In addition, the colocalization of NOS and VIP in neurons enhances their inhibitory action. The role of the neurons containing both NOS and Gal remains unknown.

Effects of a community restoration fire on small mammals and herpetofauna in the southern Appalachians

As part of the Wine Spring Creek ecosystem management project on the Nantahala National forest, North Carolina, we assessed effects of a community restoration fire on small mammals and herpetofauna in the upper slope pitch pine ( Pinus rigida) stands, neighboring midslope oak ( Quercus spp.) stands and rhododendron ( Rhododendron maximum) dominated riparian areas during 1995 and 1996. Using drift-fence arrays with pitfalls and snap-trapping, we collected these small mammals: masked shrew ( Sorex cinereus), smoky shrew ( S. fumeus), water shrew ( S. palustris), pygmy shrew ( S. hoyi), northern short-tailed shrew ( Blarina brevicauda), deer mouse ( Peromyscus maniculatus), white-footed mouse ( P. leucopus), golden mouse ( Ochrotomys nuttalli), southern red-backed vole ( Clethrionomys gapperi), pine vole ( Microtus pinetorum) and woodland jumping mouse ( Napaeozapus insignis). Herpetofauna collected from drift-fence arrays and time-constrained searches included: eastern newt ( Notophtalmus viridescens), seepage salamander ( Desmognathus aeneus), mountain dusky salamander ( D. ochrophaeus), Blue Ridge two-lined salamander ( Eurycea wilderae), spring salamander ( Gyrinophilus porphyriticus), Jordan's salamander ( Plethodon jordani), wood frog ( Rana sylvatica), five-lined skink ( Eumeces fasciatus), eastern garter snake ( Thamnophis sirtalis), and northern ringneck snake ( Diadophis punctatus). Prior to the prescribed community restoration fire in the spring of 1995, there were no significant differences in small mammal or herpetofauna collections between burned and control areas. Post-treatment in 1995 and 1996, showed no significant differences among collections of most species between burned and control areas. Slope position accounted for more variation among the species of greatest abundance than did burning. Concern for the effects of prescribed fire as a management tool on small mammals and herpetofauna in the southern Appalachians seems unwarranted.

Perceived predation risk as a function of predator dietary cues in terrestrial salamanders

Prey often avoid predator chemical cues, and in aquatic systems, prey may even appraise predation risk via cues associated with the predator’s diet. However, this relationship has not been shown for terrestrial predator–prey systems, where the proximity of predators and prey, and the intensity of predator chemical cues in the environment, may be less than in aquatic systems. In the laboratory, we tested behavioural responses (avoidance, habituation and activity) of terrestrial red-backed salamanders,Plethodon cinereus, to chemical cues from garter snakes,Thamnophis sirtalis, fed either red-backed salamanders or earthworms (Lumbricusspp.). We placed salamanders in arenas lined with paper towels pretreated with snake chemicals, and monitored salamander movements during 120min. Salamanders avoided substrates preconditioned by earthworm-fed (avoidanceX±SE=91.1±2.5%,N=25) and salamander-fed (95.2±2.5%,N=25) snakes, when tested against untreated substrate (control). Salamanders avoided cues from salamander-fed snakes more strongly (75.2±5.5%,N=25) than earthworm-fed snakes when subjected to both treatments simultaneously, implying that salamanders were sensitive to predator diet. Salamanders tended to avoid snake substrate more strongly during the last 60min of a trial, but activity patterns were similar between salamanders exposed exclusively to control substrate versus those subject to snake cues. In another experiment, salamanders failed to avoid cues from dead conspecifics, suggesting that the stronger avoidance of salamander-fed snakes in the previous experiment was not directly due to chemical cues emitted by predator-killed salamanders. Salamanders also did not discriminate between cues from a salamander-fed snake versus a salamander-fed snake that was recently switched (i.e. <14 days) to an earthworm diet. Our results imply that terrestrial salamanders are sensitive to perceived predation risk via by-products of predator diet, and that snake predators rather than dead salamanders may be largely responsible for the release of such chemicals.

Plasticity of foraging behavior in garter snakes (Thamnophis sirtalis) reared on different diets.

Plasticity of foraging behavior in garter snakes (Thamnophis sirtalis) reared on different diets.

Plasticity of foraging behavior in garter snakes (Thamnophis sirtalis) reared on different diets.

Plasticity of foraging behavior in garter snakes (Thamnophis sirtalis) reared on different diets.