Temperature-induced Multi-species Cohort Effects in Sympatric Snakes

In reptiles, reproductive maturity is often determined by size rather than age. Consequently, growth early in life may influence population dynamics through effects on generation time and survival to reproduction. Because reproductive phenology and pre- and post-natal growth are temperature-dependent, environmental conditions may induce multi-species cohort effects on body size in sympatric reptiles. I present evidence of this using ten years of neonatal size data for three sympatric viviparous snakes, Dekay’s Brownsnakes (Storeria dekayi), Red-bellied Snakes (S. occipitomaculata) and Common Gartersnakes (Thamnophis sirtalis). End-of-season neonatal size varied in parallel across species such that snout-vent length was 36-61% greater and mass was 65-223% greater in years when gestating females could achieve higher April-May (vs. June-July or August-September) operative temperatures. Thus, temperature had a larger impact during follicular enlargement and ovulation than during gestation or post-natal growth. Multi-species cohort effects like these may affect population dynamics and increase with climate change.

Comparing the population structure of the specialist Butler’s gartersnake (Thamnophis butleri) and the generalist eastern gartersnake (Thamnophis sirtalis sirtalis) in Ontario and Michigan

Species differing in life history attributes vary in their responses to features within a shared landscape. We evaluated genetic structure of sympatric gartersnake species in Southwestern Ontario, Canada and south-east Michigan, U.S.A., where habitat fragmentation is high due to agriculture and urbanization. We surveyed genetic structure of the habitat specialist, Butler’s gartersnake (Thamnophis butleri; Cope, 1889) and habitat generalist, eastern gartersnake (Thamnophis sirtalis sirtalis; Linnaeus, 1758) using DNA microsatellites. Bayesian clustering, Discriminant Analysis of Principal Components, and pairwise population comparisons revealed genetic differentiation among three major regional clusters of Butler’s gartersnake with evidence of further division within one. Genetic clustering of Butler’s gartersnake suggest that inhospitable habitat limits dispersal. Eastern gartersnakes showed less structure, with assignment tests implying a single genetic cluster. We found positive significant Mantel’s r for both species in the smallest distance class (<15 kms), but significant isolation by distance for Thamnophis butleri only. These findings together imply that connectivity for eastern gartersnakes is less impacted by habitat loss and fragmentation or that we were less able to detect their effects. Our study shows the value of multispecies comparisons in studies seeking to understand the underlying causes of genetic structure in natural populations.

Contribution to the special issue on Reptile cognition: Chemically mediated self-recognition in sibling juvenile common gartersnakes (Thamnophis sirtalis) reared on same or different diets: evidence for a chemical mirror?

Although self-recognition or self-awareness has been studied with the visually-based mirror test, passed by several species, primarily apes, the possibility of a chemically-based analogue is controversial. Prior studies suggested that chemical self-recognition may occur in some squamate reptiles. To evaluate this possibility, we studied 24 individually housed gartersnakes, Thamnophis sirtalis, raised from birth on either earthworm or fish diets and tested 12 male and 12 female snakes with cage liners that were either clean, their own, or from same-sex siblings fed their own or the opposite diet. Tongue flicking and activity were recorded in 30-minute video-recorded trials in a balanced design. After initial habituation to the stimuli, male, but not female, snakes discriminated between their own stimuli and those from littermates fed the same diet. Combined with other data and studies, the possibility that a chemical ‘mirror’ form of self-recognition exists in squamate reptiles is supported.

Staying warm is not always the norm: Behavioural differences in thermoregulation of two snake species

Thermal biology research compares field with laboratory data to elucidate the evolution of temperature-sensitive traits in ectotherms. The hidden challenge of many of these studies is discerning whether animals actively thermoregulate, since motivation is not typically assessed. By studying behaviours involved in thermoregulation, we can better understand the mechanisms behind body temperature control. Using an integrative approach, we assess thermoregulatory and thermotactic behaviours of two sympatric snake species with contrasting life histories, the generalist Thamnophis sirtalis sirtalis (Linnaeus, 1758) and the semi-fossorial Storeria occipitomaculata occipitomaculata (Storer, 1839). We expected that thermoregulatory behaviours would be optimised based on life history, in that T. s. sirtalis would show higher evidence for thermally-oriented behaviours than S. o. occipitomaculata due to its active nature. Thamnophis s. sirtalis actively thermoregulated, had higher thermal preferences (29.4 ± 2.5 vs. 25.3 ± 3.6°C), and was more active than S. o. occipitomaculata, which showed relatively low evidence for thermotaxis. Our results build on the notion that evaluating movement patterns and rostral orientation towards a heat-source can help ascertain whether animals make thermally-motivated choices. Our data give insight into the thermoregulatory strategies used by snakes with different life histories, and maximise the information provided by behavioural thermoregulation experiments.

Uncovering the genomic and metagenomic research potential in old ethanol-preserved snakes

Natural history museum collections worldwide represent a tremendous resource of information on past and present biodiversity. Fish, reptiles, amphibians and many invertebrate collections have often been preserved in ethanol for decades or centuries and our knowledge on the genomic and metagenomic research potential of such material is limited. Here, we use ancient DNA protocols, combined with shotgun sequencing to test the molecular preservation in liver, skin and bone tissue from five old (1842 to 1964) museum specimens of the common garter snake (Thamnophis sirtalis). When mapping reads to a T. sirtalis reference genome, we find that the DNA molecules are highly damaged with short average sequence lengths (38–64 bp) and high C-T deamination, ranging from 9% to 21% at the first position. Despite this, the samples displayed relatively high endogenous DNA content, ranging from 26% to 56%, revealing that genome-scale analyses are indeed possible from all specimens and tissues included here. Of the three tested types of tissue, bone shows marginally but significantly higher DNA quality in these metrics. Though at least one of the snakes had been exposed to formalin, neither the concentration nor the quality of the obtained DNA was affected. Lastly, we demonstrate that these specimens display a diverse and tissue-specific microbial genetic profile, thus offering authentic metagenomic data despite being submerged in ethanol for many years. Our results emphasize that historical museum collections continue to offer an invaluable source of information in the era of genomics.

Effects of Invasive Jumping Worms (Amynthas spp.) On Microhabitat and Trophic Interactions of Native Herpetofauna

Invasive species can affect native communities through multiple mechanisms, including ecosystem engineering and trophic interactions. In North America, invasive jumping worms ( Amynthas spp.) may alter microhabitats used by native herpetofauna or serve as a novel food resource for herpetofauna predators. We investigated effects of Amynthas on leaf litter microhabitat and trophic interactions of native herpetofauna using an outdoor mesocosm experiment, laboratory feeding trials, and field surveys of predator stomach contents in Wisconsin, USA. In mesocosms, Amynthas reduced leaf litter biomass but did not have clear effects on soil conditions (pH, moisture, and temperature) or survival of American toad metamorphs ( Anaxyrus americanus ). In laboratory trials, American toads preyed on Amynthas, though toads were less successful at capturing Amynthas compared with alternative prey, namely European earthworms ( Lumbricus spp.) and crickets ( Acheta domesticus). The differences in prey attack success were likely due to unique defensive behaviors of Amynthas . Amynthas also spent less time moving than Lumbricus , which was associated with later prey detection times by toads. Based on diet surveys, Amynthas are consumed by common garter snakes ( Thamnophis sirtalis ) in southern Wisconsin. We did not find evidence of Amynthas consumption by American toads or red-bellied snakes ( Storeria occipitomaculata ), although additional surveys will be needed to definitively determine whether these taxa are consuming Amynthas . Our findings highlight the importance of studying multiple mechanisms by which invasive species affect native communities and suggest that unique anti-predator behaviors may influence how Amynthas are incorporated into food webs as a novel prey resource.

Stable isotope analysis suggests that tetrodotoxin-resistant Common Gartersnakes (Thamnophis sirtalis) rarely feed on newts in the wild

Toxin-resistant predators may suffer costs from eating chemically-defended prey and do not feed exclusively on toxic prey. Common Gartersnakes (Thamnophis sirtalis) (Linnaeus, 1758) have been considered the drivers of an evolutionary arms race with highly toxic newts (Taricha spp.), which they consume with few or no deleterious effects. However, how frequently newts are consumed in nature is less clear. To address this question, we investigated the diets of T. sirtalis at a site in central Oregon where snakes have high levels of resistance and newts have high levels of tetrodotoxin in the skin. Because snake diets are difficult to quantify using traditional means, we used stable isotopes to estimate the proportion of T. sirtalis diets made up of newts. Our estimate for the proportion of T. sirtalis diet made up of T. granulosa at this site is 3.2%. Ambystoma salamanders were predicted to be the most important prey, followed by slugs, chorus frogs, and mice, with a very minor role for earthworms. Our results demonstrate that even though T. sirtalis are physiologically capable of consuming toxic prey, they do not often do so. Generalist predators can be exposed to very strong selection from, and exert reciprocal selection on even rarely eaten, chemically-defended prey.

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.