Plains Garter Snake Research Articles

Importance of woodland patches as hibernacula for gartersnakes in a prairie river floodplain of central Nebraska

Gartersnakes are common inhabitants along prairie rivers in the Great Plains, but little information is known about hibernacula among diverse floodplain habitats. We radio-tracked Common Gartersnakes (Thamnophis sirtalis) and Plains Gartersnakes (Thamnophis radix) to hibernacula on islands in a braided river system subject to frequent environmental changes along the Platte River in central Nebraska. We further examined capture rates of gartersnakes in floodplain woodland patches from June to November to examine seasonal use of this habitat. In early and mid-September, movements of snakes with transmitters were in grasslands. From late September to mid-October, the farthest movements were documented, and snakes moved from grasslands into woodland patches. From late October to January, movements were minimal in and around hibernacula in wooded or formerly wooded habitats. Capture rates of gartersnakes in woodland trapping arrays also increased in October and November, further demonstrating woodland use during times when snakes travel to and reside at hibernacula. Although grasslands comprised most of the prairie islands at the study area, observations suggested that the limited woodlands on these islands are important for gartersnakes prior to and during hibernation along the Platte River in central Nebraska. Areas with large trees, such as Plains Cottonwoods (Populus deltoides), appeared to provide overwintering sites. In central Nebraska, riparian woodlands continue to be cleared to enhance habitat for endangered and threatened species such as Whooping Cranes (Grus americana), but some of these islands originally contained trees prior to European settlement. Conservation of at least some woodland habitats appears important for overwintering gartersnakes in central Nebraska.

Responses of grassland snakes to tallgrass prairie restoration

Understanding faunal responses to habitat restoration is important in assessing restoration success. We investigated occupancy and abundance of snakes at Nachusa Grasslands, a large‐scale grassland restoration in the midwestern United States. Using artificial cover objects, we sampled within a chronosequence of 12 units converted from row‐crop agriculture 2–25 years before the start of our study. Recaptures of marked snakes revealed that movement distances differed among species in accordance with differences in body size, being least in Dekay's Brownsnakes, intermediate in the Plains Gartersnakes and Common Gartersnakes, and greatest in Eastern Foxsnakes. Consistent with this result, occupancy increased with restoration age in Dekay's Brownsnakes but was unrelated to restoration age in the three larger, more mobile species. Similarly, abundance increased with restoration age in Dekay's Brownsnake but was unrelated to restoration age in other species. The Smooth Greensnake, another small‐bodied snake with limited mobility, and an Illinois species of greatest conservation need, was not detected at Nachusa Grasslands. Given detection probabilities observed during a parallel study at a nearby large grassland‐dominated preserve, we infer that the Smooth Greensnake is truly absent from Nachusa Grasslands. Taken together, our results demonstrate that establishment of faunal components following restoration may be time‐dependent with more sedentary species colonizing only slowly (e.g. Dekay's Brownsnakes) or not at all (e.g. Smooth Greensnakes). These results emphasize the need to clearly identify faunal restoration goals and the means to achieve them.

Reproduction of the Plains Garter Snake,Thamnophis radix, Near Its Northern Range Limit: More Evidence for a “Fast” Life History

Do high-latitude environments constrain life histories of ectotherms? One expectation is that shorter and cooler active seasons at high latitudes limit opportunities for maintenance of optimum body temperature and restrict time for foraging and therefore for growth and reproduction. Thus, under this hypothesis, individuals in high-latitude populations of wide-ranging species would be predicted to grow more slowly, have lower reproductive output, and perhaps reproduce less frequently than lower-latitude conspecifics. However, at Miquelon Lake in central Alberta, the Plains Garter Snake (Thamnophis radix) grows as fast annually as more southerly conspecifics and reaches sexual maturity at the same age. Here, we make a comparable test of latitudinal variation in reproductive traits. Both litter size and offspring size were larger in the Miquelon Lake population than at lower latitudes. Moreover, female snakes could reproduce annually, although the frequency of annual reproduction remains unknown. Litter size...

Systemic Ophidiomyces ophiodiicola Infection in a Free-Ranging Plains Garter Snake (Thamnophis radix)

Abstract A free-ranging plains garter snake (Thamnophis radix) with a brown, encrusted, cutaneous facial lesion presented depressed, emaciated, and dehydrated. It developed respiratory distress and was later euthanized after it failed to respond to antibiotics and supportive treatment. Disseminated granulomatous disease with prominent lung involvement was diagnosed at necropsy. Intralesional hyaline fungal elements, consisting of septate hyphae, were detected histologically among the necrotic core of granulomas and aggregates of epithelioid macrophages. Ophidiomyces ophiodiicola was cultured from tissue specimens and identification was confirmed using 18S rRNA ITS DNA sequencing. Isolation of O. ophiodiicola from lesions that contain morphologically consistent fungal elements strongly incriminates this fungus as the cause of disease in this garter snake.

EFFECTS OF SEX, ENVIRONMENT, AND CONDITION ON THE MUSKING BEHAVIOR OF SYMPATRIC GARTERSNAKES (THAMNOPHIS SPP.)

Despite an abundance of studies documenting antipredator and defensive behaviors of gartersnakes (genus Thamnophis), few have quantitatively examined musking, a widely utilized antipredator tactic. In this study we quantify musking behaviors in the Terrestrial Gartersnake (Thamnophis elegans) and the Plains Gartersnake (T. radix) when hand-captured at four sites in and near Denver, Colorado, USA. Overall, Plains Gartersnakes musked significantly more often than Terrestrial Gartersnakes. Female Terrestrial Gartersnakes musked more frequently than males, a pattern not evident in the Plains Gartersnake. Additionally, we observed a positive correlation in body condition and musking propensity in Terrestrial Gartersnakes, suggesting resource-dependent behavior in this species. Musking behavior was consistent across variations in predation pressure, environmental conditions, and snake body size, all factors shown to influence other gartersnake defensive behaviors. These results corroborate other research which demonstrates that snake antipredator behaviors are determined by complex interactions of abiotic and biotic factors.

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.

Seasonal, Condition-Dependent, and Individual Variation in Testosterone in a Natricine Snake

Abstract We collected plasma samples from adult males in a natural population of Plains Gartersnakes (Thamnophis radix) to characterize seasonal variation in testosterone. As in other New World temperate zone natricines, testosterone was high during spring emergence, declined as courtship and mating progressed, and then increased in late summer and fall. Based on patterns seen in this and other studies, we suggest that the rapidity with which testosterone decreases following spring emergence may be associated with the length of the mating season; and that it decreases rapidly in species and populations in which the mating season is brief and more slowly in species and populations in which mating occurs over an extended period. Testosterone showed a clear, positive association with body condition in adult male Plains Gartersnakes. Whether this association translates into greater reproductive success warrants further investigation. Because we collected blood samples multiple times from individual males with...

Ontogenetic Effects on Snake Hemipenial Morphology

Abstract In this study we investigate hemipenial variation through ontogeny by preparing specimens of known-aged individuals from captive-bred Plains Gartersnakes, Thamnophis radix, descended from a wild population in northern Illinois, USA. We examined males at two different ages (215–254 days, N = 9) and (829–867 days, N = 12) to compare both juvenile and adult morphologies. Hemipenis length increased isometrically with tail length, and there were no significant differences detected between right and left hemipenis length or width. In addition, this study is the first to explore variation in hemipenial morphology within and among litters. We found significant litter effects on hemipenis length, on the elevation (but not the slope) of the relationship between hemipenis length and tail length, and on number of basal hooks, suggesting a possible genetic basis to these characteristics. These results highlight the importance of examining multiple males through ontogeny, as well as reporting body-size measure...

Growth and maturity of a terrestrial ectotherm near its northern distributional limit: does latitude matter?

High-latitude environments are challenging for terrestrial ectotherms because short and cool active seasons generally limit the time available for foraging and growth, thereby negatively influencing life-history variables such as growth rate and age at maturity and ultimately, via fitness differences, their evolution. Many species show latitudinal clines in life-history traits, including growth rate and body size. We estimated growth curves of Plains Garter Snakes ( Thamnophis radix (Baird and Girard, 1853)) near the northern limit of the species’ range in central Alberta and compared our findings to similar estimates for more southerly populations. Despite a short growing season, female T. radix at Miquelon Lake grew rapidly, reaching maturity in 1 or 2 years, similar to southern populations, and attained greater maximum sizes than snakes in southern populations. Overall, growth in this high-latitude population is comparable with what is seen in other conspecific populations. Possible reasons for lack of marked latitudinal effect include longer days at high latitudes, highly productive aquatic habitats for foraging, effective thermoregulation, reduced competition, and (or) countergradient variation in growth rate.

Hybridization between two gartersnake species (Thamnophis) of conservation concern: a threat or an important natural interaction?

Distinguishing between hybrid zones formed by secondary contact versus parapatric divergence-with-gene-flow is an important challenge for understanding the interplay of geographic isolation and local adaptation in the origin of species. Similarly, distinguishing between natural hybrid zones and those that formed as a consequence of recent human activities has important conservation implications. Recent work has demonstrated the existence of a narrow hybrid zone between the plains gartersnake (Thamnophis radix) and Butler’s gartersnake (T. butleri) in the Great Lakes region of North America, raising questions about the history and conservation value of genetically admixed populations. Both taxa are of conservation concern, and it is not clear whether to regard hybridization as a threat or a natural interaction. Here we use phylogeographic and population genetic methods to assess the timescales of divergence and hybridization, and test for evidence that the hybrid zone is of recent origin. We assayed AFLP markers and ND2 mitochondrial DNA (mtDNA) sequences from T. radix, T. butleri, and the closely related short-headed gartersnake (T. brachystoma) throughout their North American ranges. We find shallow mtDNA divergence overall and high levels of variation within the contact zone. These patterns are inconsistent with recent contact of long-diverged taxa. It is not possible to distinguish true divergence-with-gene-flow from a long-term secondary contact zone, but we infer that the hybrid zone is a long-standing, natural interaction.

Partial hepatectomy in a Plains garter snake (Thamnophis sirtalis radix) with biliary cystadenoma: case report

A four-year-old, captive-bred, female Plains garter snake (Thamnophis sirtalis radix) was presented with a large midbody distension (5 cm × 3 cm × 3 cm) in the second third of the body length (total body length 123 cm). Contrast radiography technique excluded an envolvement of the oesophagus or stomach. Aspiration of 8 ml of acellular straw coloured fluid negative for presence of bacteria, fungi or parasites, reduced the swelling to a third of its original size. Surgical exploration revealed a pathologically changed central part of the liver with multiple different sized cysts. Histopathologically the diagnosis was defined as biliary cystadenoma. As the liver had a physiological appearance cranial and caudal to the central area, a partial hepatectomy was performed. The snake recovered well and started to feed spontaneously two days after surgery. During the check up two, four and seven months after hepatectomy, the snake was active and in a good condition. Hypoproteinaemia and altered activity of lactate dehydrogenase were present two months after surgery, azurophilia and hyperuricaemia were present in the blood sampled four months after hepatectomy. Except for azurophilia, the other values of the blood profile were within the expected range for a healthy snake seven months after surgery, indicating full recovery. This is the first detailed report of a successful central resection of a large pathologically changed part of the liver in snakes which was diagnosed as biliary cystadenoma.

Novel microsatellite loci for studies of Thamnophis Gartersnake genetic identity and hybridization

Butler’s Gartersnakes (BGS; Thamnophis butleri) are confined to open and semi-open canopy wetlands and adjacent uplands, habitats under threat of development in Wisconsin. To address issues of species identity and putative hybridization with congeneric snakes, a suite of 18 microsatellite loci capable of cross-species amplification of Plains Gartersnakes (T. radix) and Common Gartersnakes (T. sirtalis) was developed. All loci were polymorphic in BGS with mean number of alleles per locus of 16.11 (range = 3–41) and mean observed heterozygosity of 0.659 (range = 0.311–0.978). Loci amplified efficiently in the congeneric species with high levels of intra- and inter-specific variation. These loci will aid ongoing efforts to effectively identify and manage BGS in Wisconsin.

Behavioural correlates with hemipenis morphology in New World natricine snakes

Copulatory organs (hemipenes) of male snakes vary markedly among species in shape and ornamentation. We suggest that sexual conflict over copulation duration may have shaped the evolution of hemipenis morphology, favouring more elaborate organs in species in which a long duration of copulation is especially beneficial to males, despite the associated costs to females. To test this proposition, we compare mating behaviour between two species of gartersnakes differing in hemipenis morphology. In addition, we review data on copulation duration and hemipenis morphology and relate hemipenis morphology to phylogeny among of New World natricines. As predicted, copulation duration was significantly shorter in the common gartersnake (Thamnophis sirtalis), a species with simple subcylindrical hemipenes, than in the plains gartersnake (Thamnophis radix), a species with more complex, bilobed organs. Furthermore, female T. radix frequently exhibited vigorous body rolls during copulation, a behaviour associated with copulation termination, whereas female T. sirtalis never exhibited this behaviour. Copulations were of shorter duration when female T. radix (but not T. sirtalis) more greatly exceeded males in body size, suggesting that females can more easily disengage from small males. Our review of New World natricines provides only weak evidence for an association between copulation duration and hemipenis morphology. Our mapping of hemipenis morphology onto the New World natricine phylogeny suggests that hemipenis morphology is evolutionarily plastic; both simple and bilobed hemipenes occur in all three major natricine clades, as well as in two of three gartersnake subclades and several sister-species pairs.

Food Habits of the Plains Garter Snake (Thamnophis radix) at the Northern Limit of Its Range

The North American genus Thamnophis is a widely distributed and abundant group of snakes. Previous research has indicated that most garter snakes are generalist predators that largely consume anurans, with some degree of geographic and temporal plasticity in response to resource variation. We studied the dietary habits of the Plains Garter Snake, Thamnophis radix, based on stomach contents from 548 animals collected in the field from 1995-2006 at the northern limit of the species' range in central Alberta, Canada. Feeding frequency overall was low (22%) and was highest in spring and early summer. Diet was composed mainly of anurans (85%), especially Wood Frogs (Rana sylvatica) and Boreal Chorus Frogs (Pseudacris maculata), and occasionally invertebrates (10%) and small mammals (5%). Small snakes (<200 mm) began feeding shortly after birth and consumed mainly smaller frogs. Larger snakes ate a wider range of prey sizes and types, but frogs still constituted the majority of prey consumed. Despite sexual size dimorphism, males and females ate prey of the same size and type; however, gravid females contained food less frequently than both males and nongravid females. This study adds to the growing number of dietary studies on T. radix and provides additional evidence for the ecological plasticity of Thamnophis species. Further studies are needed to examine how important these snakes are as components of wetland food chains.

HEADSTARTING AS A MANAGEMENT TOOL: A CASE STUDY OF THE PLAINS GARTERSNAKE

The use of headstarting and related techniques as management tools for threatened and endangered species remains controversial, due in part to a lack of empirical data on their effectiveness. Here, we present data on pre-natal mortality, growth, and survival during headstarting as well as growth, survival, and reproduction following release for an unprotected population of plains gartersnakes. We combine these data with data on growth and survival of comparably sized wild-caught snakes to provide an overall evaluation of the potential effectiveness of headstarting. Depending on rearing conditions, proportions of live births varied from 0.79 (‘worst-case’) to 0.94 (‘best-case’), survival during headstarting ranged from 0.74 (‘worst-case’) to 0.88 (‘best-case’), and second-year survival following release ranged from 0.11 (‘worst-case’) to 0.40 (‘best-case’). In comparison, survival of free-ranging snakes was 0.16 in their first year and 0.40 in their second year. Assuming the proportion of live births in nature is close to 1, expected survival to reproductive maturity among free-ranging snakes is 0.06, whereas that for headstarted snakes ranges from 0.07 (‘worst-case’) to 0.33 (‘best-case’). The growth rate of headstarted snakes following release was similar to that of similar-sized free-ranging snakes, and headstarted snakes were successful at reproduction. Together, these results suggest that, if carefully implemented, headstarting may be an effective management tool for endangered plains gartersnake populations in Ohio and for other natricine snakes with similar demographic characteristics.

Growth, Survival, and Reproduction in a Northern Illinois Population of the Plains Gartersnake, Thamnophis radix

A six-year mark-recapture study, consisting of 567 captures of 216 individually marked snakes, and the birth of 889 young in 53 litters born to 39 wild-caught females were used to estimate demographic and life-history parameters of a Northern Illinois population of Thamnophis radix. Using the von Bertalanffy growth model, males were found to differ from females in asymptotic size but not in the rate at which they approached this size. Size of known age individuals together with growth rate estimates were used to assign age at first capture. Age and sex were then used as grouping variables to obtain age- and sex-specific survival using program MARK. The results suggest that males and females have approximately equal survival in the 0 and 1 age classes but that females have higher survival than males as adults (0.45 vs 0.35). Population estimates calculated using Schumacher-Eschmeyer and Jolly-Seber methods indicate an adult population size of 64 and 172 adults, respectively, corresponding to densities of 40 and 107 adults per hectare. Average female fertility increased from 6.4 in one-year-old females to 21 among six-year-old females. Detailed demographic studies such as this have utility in development of management strategies and theories concerning life-history evolution.

Species-isolating mechanisms in a mating system with male mate choice (garter snakes, Thamnophis spp.)

Reproductive isolation between sympatric taxa can be maintained by specific mate-recognition behaviours or by ecological divergence that reduces interspecific contact during reproduction. Common garter snakes, Thamnophis sirtalis (L., 1758), and plains garter snakes, Thamnophis radix (Baird and Girard, 1853), are sympatric over large areas, but morphological data suggest that the prezygotic isolation between these two species partially breaks down in a severely cold part of their joint range in Manitoba. Courtship trials show that male T. radix court intensely over a narrower range of (higher) ambient temperatures than do male T. sirtalis. Males selectively court females of their own species, but male T. radix are less choosy than male T. sirtalis. Hexane extracts of female skin lipids also elicited species-specific courtship. Although this male preference for species-specific pheromones contributes to species isolation, it is not strong enough to completely separate the two taxa. The absence of hybridization over most of the sympatric range may depend on the timing of mating (early spring, near the hibernation den). Differences between the species in hibernation-site selection and the timing of spring emergence break down in central Manitoba because severely cold winter temperatures force both species together into the few available hibernation (and thus, mating) sites, and the short warm season reduces temporal separation in emergence (and thus, mating) seasons.

Sexual Dimorphism in Size of Cloacal Glands of the Garter Snake, Thamnophis radix haydeni

A pair of cloacal glands lie at the base of the tail in snakes. These glands are elongate and sausageshaped and exude a thick tan-colored liquid that is often malodorous (Fitch, 1965). Because of their often malodorous secretion, these glands have been referred to as 'musk glands' or 'scent glands' (Whiting, 1969). Cloacal glands are dorsal to the hemipenes in males and are located in a corresponding position in females (Whiting, 1969). Whiting (1969) reported that cloacal glands of females were frequently larger than those of males, but provided no quantitative evidence. Thorpe (1989) found that cloacal glands of female grass snakes (Natrix natrix) were significantly longer than those of males. He suggested that smaller gland size in males was a consequence of crowding by the hemipenes. The function of these glands has been a subject of controversy for many years (Mason, 1992). Before Noble and Claussen (1936) demonstrated that the source of the female sex attractant was in the dorsal skin, many authors suggested that the glands served as its source (Whiting, 1969; Mason, 1992). More recently, authors have suggested that the secretions may be used as an alarm pheromone (Brisbain, 1968; Graves and Duvall, 1988) or for marking territory (Andren, 1986). Most often, a defensive function has been attributed to the glands because the malodorous fluid is commonly secreted after a snake has been captured and handled (Mason, 1992). Klauber (1956) speculated that the secretion may make a snake less attractive or less palatable as a prey item. We measured both length and width of cloacal glands of western plains garter snakes (Thamnophis radix haydeni) to determine whether sexual dimorphism occurs in gland size. We show that females have significantly larger glands than males and we suggest that crowding of the glands by the hemipenes may not be sufficient to explain this sexual dimorphism. We also speculate as to why females may require larger glands than males based on potential sex differences in threat of predation. Eight nongravid females, four gravid females, and 11 males were examined. These snakes were part of a group of snakes kept in captivity for approximately four months for use in an experimental study of locomotory performance and defensive behavior (Kiss-

Juvenile toads avoid chemical cues from snake predators

Chemical senses mediate several anuran behaviours, including predator avoidance by larval frogs. Predation by garter snakes is an important influence on the survival of post-metamorphic, juvenile toads (Bufosp.). Studies have shown that visual, rather than chemical, cues are important for predator avoidance in post-metamorphic juvenile bufonids. This study investigated the ability of post-metamorphic, juvenile great plains toads,B.cognatusand southwestern toads,B.microscaphusto detect and avoid chemical cues from their respective predators, the eastern plains garter snake,Thamnophis radixand the wandering garter snake,T.elegansJuvenileB.cognatuscollected in South Dakota were observed on unmarked paper towels significantly more than on similar towels treated with chemical cues fromT.radixSimilarly, juvenileB.microscaphusfrom Arizona were observed on unmarked towels significantly more than on towels marked with chemical cues fromT.elegansToad avoidance of snake odour was apparently not a generalized response to reptile chemical cues: juvenileB.microscaphuscontinued to avoid snake odours when these were simultaneously presented with odours from sympatric lizards,Sceloporus undulatusHence, juvenileB.cognatusandB.microscaphusapparently detect and avoid chemical cues from snake species that prey on them.

Population and sex differences in antipredator responses of breeding fathead minnows (Pimephales promelas) to chemical stimuli from garter snakes (Thamnophis radix andT. sirtalis)

We conducted a predator bite survey on a population of fathead minnows (Pimephales promelas) considered to be under substantial predation pressure by western plains garter snakes (Thamnophis radix). Scarring, due to failed predation attempts by garter snakes and crayfish (Orconectes virilis), was observed significantly more often in breeding males than in breeding females and nonbreeding minnows. Likely, territorial nest defense under the edges of rocks along the water's edge, a habitat occupied by crayfish and frequented by snakes, caused the breeding males to be differentially vulnerable to predation. Under controlled laboratory conditions, breeding males from this population exhibited an antipredator response to chemical stimuli from live snakes (T. sirtalis andT. radix) significantly more often than breeding female minnows from the same population and breeding minnows of both sexes from a population that was presumed to be under lower predation pressure from snakes.