Thamnophis Radix 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.

Cutaneous and Subcutaneous Soft Tissue Tumours in Snakes: A Retrospective Study of 33 Cases

Cutaneous and subcutaneous soft tissue tumours have been rarely described in detail in snakes. Several malignant entities show strikingly similar histological patterns and therefore the term soft tissue sarcoma (STS) has become a standard histopathological diagnosis. The present study characterizes soft tissue tumours in 33 snakes. Samples included 29 surgically excised masses and four carcasses. Additionally, six animals were humanely destroyed and submitted for necropsy examination following tumour recurrence. Benign neoplasms (n=8) were described as lipomas of varying differentiation. Recurrence was observed in two of five snakes in which the clinical course was recorded. Malignant neoplasms (n=25) were diagnosed as STS and graded according to a three-point system previously applied to canine STS. Five (20%) of the primary tumours were classified as grade 1, eleven (44%) as grade 2 and nine (36%) as grade 3 sarcomas. Clinically, recurrence of STS was observed in 11 of 17 cases with available follow-up information. Pathologically, multiple cutaneous metastases were found in one grass snake (Natrix natrix), while visceral metastases were observed in one carpet python (Morelia spilota) and two corn snakes (Pantherophis guttatus). Metastatic risk appears to increase with histological grade. Surgical excision generally represents the current therapy of choice for STS. This study includes the first reports of conventional lipomas in a ribbon snake (Thamnophis radix), angiolipomas in a black-headed python (Aspidites melanocephalus) and a corn snake as well as of STS in a Jamaican boa (Epicrates subflavus), emerald tree boa (Corallus caninus), grass snake (N. natrix), African house snake (Lamprophis fuliginosus), California kingsnake (Lampropeltis getula californiae) and common garter snake (Thamnophis sirtalis).

Heterochrony and early left-right asymmetry in the development of the cardiorespiratory system of snakes.

Snake lungs show a remarkable diversity of organ asymmetries. The right lung is always fully developed, while the left lung is either absent, vestigial, or well-developed (but smaller than the right). A ‘tracheal lung’ is present in some taxa. These asymmetries are reflected in the pulmonary arteries. Lung asymmetry is known to appear at early stages of development in Thamnophis radix and Natrix natrix. Unfortunately, there is no developmental data on snakes with a well-developed or absent left lung. We examine the adult and developmental morphology of the lung and pulmonary arteries in the snakes Python curtus breitensteini, Pantherophis guttata guttata, Elaphe obsoleta spiloides, Calloselasma rhodostoma and Causus rhombeatus using gross dissection, MicroCT scanning and 3D reconstruction. We find that the right and tracheal lung develop similarly in these species. By contrast, the left lung either: (1) fails to develop; (2) elongates more slowly and aborts early without (2a) or with (2b) subsequent development of faveoli; (3) or develops normally. A right pulmonary artery always develops, but the left develops only if the left lung develops. No pulmonary artery develops in relation to the tracheal lung. We conclude that heterochrony in lung bud development contributes to lung asymmetry in several snake taxa. Secondly, the development of the pulmonary arteries is asymmetric at early stages, possibly because the splanchnic plexus fails to develop when the left lung is reduced. Finally, some changes in the topography of the pulmonary arteries are consequent on ontogenetic displacement of the heart down the body. Our findings show that the left-right asymmetry in the cardiorespiratory system of snakes is expressed early in development and may become phenotypically expressed through heterochronic shifts in growth, and changes in axial relations of organs and vessels. We propose a step-wise model for reduction of the left lung during snake evolution.

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.

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.

Post-bite Elevation in Tongue-flick Rate by Neonatal Garter Snakes (Thamnophis radix)

A post-biting elevation in tongue-flicking rate was demonstrated experimentally in neonatal, ingestively naive garter snakes (Thamnophis radix). That the snakes also exhibited apparent searching movements suggests that strike-induced chemosensory searching occurs in nonvenomous snakes lacking previous experience with food or prey chemicals. Two litters of neonates differed in numbers of tongue-flicks emitted, but had similar relative magnitudes of response across experimental conditions. The existence of post-bite elevation in tongue-flick rate (and presumably strike-induced chemosensory searching) argues for a genetic basis for these chemosensory behaviors in a nonvenomous species of snake, extending the recent finding that strike-induced chemosensory searching is fully developed in ingestively naive neonatal rattlesnakes. Possible patterns of evolution of post-bite elevation in tongue-flick rate, and the strike-release-trail strategy of highly venomous snakes are discussed.

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.

Distinctiveness in the face of gene flow: hybridization between specialist and generalist gartersnakes

Patterns of divergence and polymorphism across hybrid zones can provide important clues as to their origin and maintenance. Unimodal hybrid zones or hybrid swarms are composed predominantly of recombinant individuals whose genomes are patchworks of alleles derived from each parental lineage. In contrast, bimodal hybrid zones contain few identifiable hybrids; most individuals fall within distinct genetic clusters. Distinguishing between hybrid swarms and bimodal hybrid zones can be important for taxonomic and conservation decisions regarding the status and value of hybrid populations. In addition, the causes of bimodality are important in understanding the generation and maintenance of biological diversity. For example, are distinct clusters mostly reproductively isolated and co-adapted gene complexes, or can distinctiveness be maintained by a few 'genomic islands' despite rampant gene flow across much of the genome? Here we focus on three patterns of distinctiveness in the face of gene flow between gartersnake taxa in the Great Lakes region of North America. Bimodality, the persistence of distinct clusters of genotypes, requires strong barriers to gene flow and supports recognition of distinct specialist (Thamnophis butleri) and generalist (Thamnophis radix) taxa. Concordance of DNA-based clusters with morphometrics supports the hypothesis that trophic morphology is a key component of divergence. Finally, disparity in the level of differentiation across molecular markers (amplified fragment length polymorphisms) indicates that distinctiveness is maintained by strong selection on a few traits despite high gene flow currently or in the recent past.

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 neonate and adult snakes

AbstractSex differences in body size and head dimensions are widespread in adult snakes, but because data are scarce for neonates, it is unclear whether differences are present from birth or arise post‐natally. Here we analyse patterns of sexual dimorphism in neonates and adults of four species of natricine snakes, Nerodia sipedon, Storeria dekayi, Thamnophis radix, and T. sirtalis. Two measures of body size (snout–vent length, mass), four measures of head morphology (head length, head width, jaw length, and interocular distance), and tail length were obtained from wild‐caught adults and from offspring born to wild‐caught females. Among neonates, significant sexual dimorphism was found in body size for S. dekayi and T. sirtalis, in head dimensions for S. dekayi, T. radix, and T. sirtalis, and in tail length for all four species. Among adults, significant sexual dimorphism was found in body size, head dimensions, and tail length for all four species. The degree of sexual dimorphism in body size among adults greatly exceeded that among neonates. In contrast, the degree of sexual dimorphism in head dimensions was similar between neonates and adults. The presence of significant sexual dimorphism among neonates suggests that hypotheses regarding the evolutionary significance of sexual dimorphism in snakes should consider newborns as well as adults.

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-

Historical Changes in a Herpetofaunal Assemblage in the Flint Hills of Kansas

-To assess changes in the herpetofauna in the northern Flint Hills of Kansas, we conducted a survey on the Fort Riley Military Reservation (Riley and Geary counties) in 1993 and compared our results with those of C. E. Burt and other early collectors. Of 46 species reported before 1930, 37 were found in 1993. Four species recorded before 1930 and not found in 1993 (Bufo cognatus, Carphophis vermis, Thamnophis radix and Crotalus horridus) are known or believed to persist in Riley and Geary counties. Four other species (Heterodon platirhinos, Nerodia erythrogaster; N. rhombifer and Regina grahamii) have not been reported in over 50 yr and may be extirpated locally. Two additional species (Spea bombifrons and Trachemys scripta) found in 1993 were not reported by early collectors. Changes in relative abundance of species from pre-1930 to 1993 were few, and there was no evidence of decline in amphibian populations. With the exception of declines in species dependent on rare habitats located in the floodplain of major rivers, the herpetological assemblage in the Fort Riley area has changed little during the past 70-100 yr. We attribute this stability to land uses that have maintained large tracts of native vegetation.

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.