Sistrurus Catenatus Research Articles

Demographic Analysis of Imperiled Eastern Massasaugas (Sistrurus catenatus catenatus)

Abstract As quantitative modeling of wildlife populations increases, the need for accurate and precise estimates of demographic rates for these populations also grows. Eastern Massasaugas (Sistrurus catenatus catenatus) are an imperiled rattlesnake species found mainly in the Great Lakes region of North America. We focused on an Eastern Massasauga population found on Beausoleil Island in Georgian Bay that was the subject of a 30-yr mark–recapture study for demographic analysis. We estimated multiple demographic values including annual adult survival, the temporal process variance of survival, population size, and population growth rate. Annual adult survival did not differ significantly between sexes (males 0.74; females 0.73). The process variance of annual adult survival for males was 0.006 and was inestimable for females. This is the first estimate of process variance for Eastern Massasaugas and one of the few such estimates for a snake species. The use of the process variance of survival in population...

To forage, mate, or thermoregulate: Influence of resource manipulation on male rattlesnake behavior.

Male animals should preferentially allocate their time to performing activities that promote enhancing reproductive opportunity, but the need to acquire resources for growth and survival may compete with those behaviors in the short term. Thus, behaviors which require differing movement patterns such as ambushing prey and actively searching for mates can be mutually exclusive. Consequently, males that succeed at foraging could invest greater time and energy into mate searching. We radio‐tracked sixteen male massasauga rattlesnakes (Sistrurus catenatus) and supplemented the diets of half the snakes with mice across an active season. We tested the predictions that reduced foraging needs would allow fed snakes to move (i.e., mate search) more, but that they would consequently be stationary to thermoregulate less, than unfed controls. Contrary to our first prediction, we found no evidence that fed snakes altered their mate searching behavior compared to controls. However, we found controls maintained higher body temperatures than fed snakes during the breeding season, perhaps because fed snakes spent less time in exposed ambush sites. Fed snakes had higher body condition scores than controls when the breeding season ended. Our results suggest the potential costs incurred by devoting time to stationary foraging may be outweighed by the drive to increase mating opportunities. Such instances may be especially valuable for massasaugas and other temperate reptiles that can remain inactive for upwards of half their lives or longer in some cases, and for female rattlesnakes that generally exhibit biennial or more protracted reproductive cycles.

Plasma Vitamin, Mineral and Biochemistry Concentrations in Free-Ranging, Adult Eastern Massasauga (Sistrurus catenatus) During Spring Egress.

Plasma Vitamin, Mineral and Biochemistry Concentrations in Free-Ranging, Adult Eastern Massasauga (Sistrurus catenatus) During Spring Egress.

Plasma Vitamin, Mineral, and Biochemistry Concentrations in Free-Ranging, Adult Eastern Massasauga (Sistrurus catenatus) during Spring Egress

Abstract The purpose of this study was to determine vitamin (A, D, E), mineral (cobalt, copper, molybdenum, manganese, iron, selenium, zinc), and plasma biochemistry concentrations in free-ranging, eastern massasauga rattlesnakes (EMR) (Sistrurus catenatus) in relation to age, sex, reproductive status, and season. Plasma samples were collected from 24 snakes post-brumation (April–May) in Michigan. Significant increases in weight and plasma vitamin E, iron, molybdenum, calcium, phosphorus, triglycerides, and cholesterol were detected in gravid compared to non-gravid females. Vitamin D synthesis from ultraviolet B radiation may be possible in EMR and requires further research. Gravid snakes appear to bioaccumulate molybdenum in tissues. Although the sample size and methodology did not meet ASVCP guidelines for establishing reference ranges, the data provide an important first step in elucidating the role of vitamin and trace minerals in relation to EMR health and reproduction. These data can be used to comp...

Climatic and geographic predictors of life history variation in Eastern Massasauga (Sistrurus catenatus): A range-wide synthesis.

Elucidating how life history traits vary geographically is important to understanding variation in population dynamics. Because many aspects of ectotherm life history are climate-dependent, geographic variation in climate is expected to have a large impact on population dynamics through effects on annual survival, body size, growth rate, age at first reproduction, size–fecundity relationship, and reproductive frequency. The Eastern Massasauga (Sistrurus catenatus) is a small, imperiled North American rattlesnake with a distribution centered on the Great Lakes region, where lake effects strongly influence local conditions. To address Eastern Massasauga life history data gaps, we compiled data from 47 study sites representing 38 counties across the range. We used multimodel inference and general linear models with geographic coordinates and annual climate normals as explanatory variables to clarify patterns of variation in life history traits. We found strong evidence for geographic variation in six of nine life history variables. Adult female snout-vent length and neonate mass increased with increasing mean annual precipitation. Litter size decreased with increasing mean temperature, and the size–fecundity relationship and growth prior to first hibernation both increased with increasing latitude. The proportion of gravid females also increased with increasing latitude, but this relationship may be the result of geographically varying detection bias. Our results provide insights into ectotherm life history variation and fill critical data gaps, which will inform Eastern Massasauga conservation efforts by improving biological realism for models of population viability and climate change.

Mitigation reduces road mortality of a threatened rattlesnake

Context Reducing road mortality is essential to reptile conservation in regions with dense road networks. The Georgian Bay, Ontario population of the eastern massasauga rattlesnake (Sistrurus catenatus) is designated as Threatened, in part because of high road mortality. In Killbear Provincial Park, four ecopassages and barrier fencing were constructed along three busy park roads to reduce road mortality of massasaugas. Aim Although mitigation of road mortality has been widely recommended and in some instances implemented for reptiles, effectiveness of mitigation efforts is often inadequately evaluated. The goals of our study were to use long-term data to quantify the effectiveness of ecopassages and barrier fencing in reducing massasauga fatalities on roads, and to evaluate the potential of these structures to serve as movement corridors for individual snakes. Methods We used five approaches to assess the overall efficacy of mitigation efforts: (1) comparison of pre- and post-mitigation road mortality; (2) camera traps in ecopassages to document massasauga and predator presence; (3) automated tag readers in ecopassage entrances to detect PIT-tagged individuals; (4) an experiment to assess massasauga willingness to enter and travel through ecopassages; and (5) measurement of temperature fluctuations in ecopassages to assess thermal suitability for massasaugas. Key results We found a significant decrease in road mortality of massasaugas on stretches of park roads associated with ecopassages and barrier fencing post construction. Automated tag readers and cameras detected the presence of massasaugas and other animals within the ecopassages, and experimental data showed that massasaugas willingly entered, and in some cases crossed through, ecopassages. Conclusion Our evaluation of mitigation structures determined that they successfully reduce road mortality and provide potential movement corridors between bisected habitats, provided that intense maintenance of the fencing is conducted yearly. We also demonstrated the need to utilise a combination of multiple post-monitoring methods to effectively evaluate mitigation structures. Implications This study provides a template for construction of similar mitigation in other key locations where reptile road mortality occurs.

Demography of a Small and Isolated Population of Eastern Massasauga Rattlesnakes (Sistrurus catenatus) Threatened by Vegetative Succession

Abstract Reforestation of early successional vegetation types has been implicated in the decline and extirpation of snake species dependent on exposed basking sites. Consequently, basking-site improvement measures (e.g., brush clearing) are frequently proposed to conserve threatened and endangered snake populations; however, demographic response of snakes to vegetation manipulation is largely unknown. This study measured changes in reproductive fitness, survival, and abundance of females in an isolated population of endangered Eastern Massasauga Rattlesnakes (Sistrurus catenatus) in years before and after cutting of woody vegetation to create basking opportunities. We marked a total of 181 snakes from 2006 to 2014, over which time substantial vegetation was cleared in key gestation areas to increase availability of basking sites for gravid females. Reproductive cycles of females in this population appeared to be primarily biennial, with parturition dates strongly influenced by maximum daily summer tempera...

Scanning Snakes to Measure Condition: A Validation of Quantitative Magnetic Resonance

Abstract Body composition is a measure of an animal's energetic state that can inform many research fields, yet the analysis traditionally requires individuals to be killed, and chemical analysis is labor intensive. Quantitative magnetic resonance (QMR) measures body composition noninvasively in live and nonanesthetized animals. Our aim was to validate QMR analysis for snakes by comparing it with gravimetric chemical analysis. We collected Northern Watersnakes (Nerodia sipedon sipedon) and Eastern Massasaugas (Sistrurus catenatus catenatus) that were found dead on roads, analyzed their body composition using the QMR scanner, and then by gravimetric chemical analysis. We compared fat mass, wet lean mass, and total water mass between the two methods, and then calculated bias, absolute error (g), and relative error (%) of the QMR analysis. Body composition values from the QMR analyses were highly correlated with the values obtained by gravimetric chemical analysis. Bias and errors were reasonable for wet lea...

Desert Massasauga Rattlesnakes (Sistrurus catenatus edwardsii) in Southeastern Colorado: Life History, Reproduction, and Communal Hibernation

Abstract We studied Desert Massasauga Rattlesnakes (Sistrurus catenatus edwardsii) in southeastern Colorado in 1998 and 2005–2007. Mark–recapture data for 770 snakes indicated a population size of >3,500 snakes in an area of approximately 4,800 ha. Field growth rates and size class frequency distributions showed that average snake age was 3 yr; 4 yr old snakes were frequently encountered, but less than 4% were 5 yr or older, suggesting low survivorship beyond this age. Conversely, initial growth was rapid; snakes grew an average of 0.57 mm/day in their first full year. Desert Massasaugas mated in fall and spring, producing 2–7 (mean 3.3) young in late August to early September, and reproduction appeared to be biennial. Desert Massasaugas showed maternal attendance for at least 5 days postparturition, and neonate dispersal corresponded with the first shed. Radioed Desert Massasaugas (N = 15) used rodent burrows as hibernacula, and within 50 m of Desert Massasauga hibernacula, eight snake, five anuran, and ...

Origin of a cryptic lineage in a threatened reptile through isolation and historical hybridization.

Identifying phylogenetically distinct lineages and understanding the evolutionary processes by which they have arisen are important goals of phylogeography. This information can also help define conservation units in endangered species. Such analyses are being transformed by the availability of genomic-scale data sets and novel analytical approaches for statistically comparing different historical scenarios as causes of phylogeographic patterns. Here, we use genomic-scale restriction-site-associated DNA sequencing (RADseq) data to test for distinct lineages in the endangered Eastern Massasauga Rattlesnake (Sistrurus catenatus). We then use coalescent-based modeling techniques to identify the evolutionary mechanisms responsible for the origin of the lineages in this species. We find equivocal evidence for distinct phylogenetic lineages within S. catenatus east of the Mississippi River, but strong support for a previously unrecognized lineage on the western edge of the range of this snake, represented by populations from Iowa, USA. Snakes from these populations show patterns of genetic admixture with a nearby non-threatened sister species (Sistrurus tergeminus). Tests of historical demographic models support the hypothesis that the genetic distinctiveness of Iowa snakes is due to a combination of isolation and historical introgression between S. catenatus and S. tergeminus. Our work provides an example of how model-based analysis of genomic-scale data can help identify conservation units in rare species.

Detection of Ophidiomyces, the Causative Agent of Snake Fungal Disease, in the Eastern Massasauga ( Sistrurus catenatus ) in Michigan, USA, 2014.

Snake fungal disease (SFD), caused by Ophidiomyces ophiodiicola, threatens free-ranging snake populations across the US. We assayed 112 swabs from 102 individual eastern massasaugas ( Sistrurus catenatus ) at three locations in Michigan in 2014 for Ophidiomyces using quantitative PCR (qPCR). We observed a 12.7% qPCR prevalence of skin lesions. Individuals at each site had lesions, and occurrence of skin lesions was not significantly different between sites. We detected Ophidiomyces DNA at each of the three sites in five individuals (4.9%). We found no difference in detection probabilities between sites; however, snakes with dermatitis had higher Ophidiomyces DNA detection probabilities (P=0.15±0.08 SE) than snakes without dermatitis (P=0.02±0.01 SE, P=0.026). The emergence of SFD mortalities has potentially serious consequences for the viability of the eastern massasauga in Michigan. Future work should track temporal patterns in vital rates and health parameters, link health data to body condition indices for individual snakes, and conduct a "hotspot" analysis to examine health on a landscape scale.

Microsatellite and major histocompatibility complex variation in an endangered rattlesnake, the Eastern Massasauga (Sistrurus catenatus).

Genetic diversity is fundamental to maintaining the long‐term viability of populations, yet reduced genetic variation is often associated with small, isolated populations. To examine the relationship between demography and genetic variation, variation at hypervariable loci (e.g., microsatellite DNA loci) is often measured. However, these loci are selectively neutral (or near neutral) and may not accurately reflect genomewide variation. Variation at functional trait loci, such as the major histocompatibility complex (MHC), can provide a better assessment of adaptive genetic variation in fragmented populations. We compared patterns of microsatellite and MHC variation across three Eastern Massasauga (Sistrurus catenatus) populations representing a gradient of demographic histories to assess the relative roles of natural selection and genetic drift. Using 454 deep amplicon sequencing, we identified 24 putatively functional MHC IIB exon 2 alleles belonging to a minimum of six loci. Analysis of synonymous and nonsynonymous substitution rates provided evidence of historical positive selection at the nucleotide level, and Tajima's D provided support for balancing selection in each population. As predicted, estimates of microsatellite allelic richness, observed, heterozygosity, and expected heterozygosity varied among populations in a pattern qualitatively consistent with demographic history and abundance. While MHC allelic richness at the population and individual levels revealed similar trends, MHC nucleotide diversity was unexpectedly high in the smallest population. Overall, these results suggest that genetic variation in the Eastern Massasauga populations in Illinois has been shaped by multiple evolutionary mechanisms. Thus, conservation efforts should consider both neutral and functional genetic variation when managing captive and wild Eastern Massasauga populations.

Manipulation of basking sites for endangered eastern massasauga rattlesnakes

Generating open-canopy basking sites via manipulation of vegetative cover has been proposed as a conservation strategy for snakes and other reptiles. We assessed how endangered eastern massasauga rattlesnakes (Sistrurus catenatus) responded to 2 types of manipulations at a wetland site in New York, USA: 1) cutting shrubs to create ≤100-m2 plots within known gestation areas in 2008, 2011, and 2012, and 2) cutting tree and shrub cover in the adjacent forest to create a 4-ha forest clearing in 2011. Based on systematic visual surveys from June to August in 2011 and 2012, we estimated snake presence among manipulated and unmanipulated plots in response to plot treatment date. We observed massasaugas selecting newly manipulated plots more often than unmanipulated plots within known gestation areas in both 2011 and 2012, but we detected no increase in massasauga activity within the adjacent forest clearing in either year. The effectiveness of vegetation cutting appeared to decline after 3 years because of vegetation re-growth. We suggest that cutting shrubs to ≤0.25 m in height can benefit this population of rare snakes, which faces limited availability of basking sites because of vegetative succession. © 2016 The Wildlife Society.

HEMATOLOGY IN AN EASTERN MASSASAUGA (SISTRURUS CATENATUS) POPULATION AND THE EMERGENCE OF OPHIDIOMYCES IN ILLINOIS, USA.

Disease events are threatening wildlife populations across North America. Specifically, mortality events due to Ophidiomyces (snake fungal disease; SFD) have been observed recently in snakes in Illinois, US. We investigated the health of a population of eastern massasaugas ( Sistrurus catenatus ) in south-central Illinois using 1) a meta-analysis of hematologic findings from 2004, 2011, 2013, and 2014; 2) a determination of the prevalence of SFD in snakes examined in 2013 and 2014; and 3) the examination of 184 museum specimens collected from 1999-2013 for signs and presence of SFD. For the meta-analysis and prevalence of SFD, hematologic analytes were reduced to three principle components that explained 67.5% of the cumulative variance. There were significant differences among one principle component (total white blood cell counts, monocytes, lymphocytes, and basophils) across years when it was highest in 2004 and 2014. The top general linear model explaining the difference in principle components included the main effects of year and stage, body condition index (BCI), and the interaction between stage and BCI. The prevalence of SFD was 18% (n=7) in 2013 and 24% (n=11) in 2014, and no hematologic analytes were associated with SFD. In museum specimens, Ophidiomyces DNA was first detected from an individual collected in 2000. Studies such as these, integrating multiple modalities of health, can elucidate the epidemiology of diseases that may pose conservation threats.

Road Mortality of Reptiles and Other Wildlife at the Ojibway Prairie Complex and Greater Park Ecosystem in Southern Ontario

The Ojibway Prairie Complex in Windsor contains the largest protected tallgrass prairie ecosystem in Ontario and supports numerous species at risk. Despite its ecological significance, it is crossed by multiple high-traffic roads. Road mortality is a major threat to endangered species in Canada, particularly reptiles. The main goal of this study was to describe the nature and extent of vertebrate road mortality, with a focus on reptiles, on roads bisecting the Ojibway Prairie Complex, and the Greater Park Ecosystem, in Windsor and Lasalle, Ontario. A systematic road mortality survey was conducted by bicycle along seven roads (12.5 km) in 2010, 2012, and 2013. Also, opportunistic observations (n = 103) spanning over 30 years were assembled from a variety of sources. In total, 2083 vertebrates (49 species), including 446 reptiles (11 species), were recorded “dead onroad” during systematic surveys. The highest diversity of reptiles was recorded on Matchette Road, whereas the highest rate of reptile mortality was recorded on Malden Road. Reptile species at risk were killed on all roads surveyed. Combining systematic and opportunistic data, we found seven reptile species at risk: Butler’s Gartersnake (Thamnophis butleri), Eastern Foxsnake (Pantherophis vulpinus), Eastern Massasauga (Sistrurus catenatus catenatus), Blanding’s Turtle (Emydoidea blandingii),Eastern Musk Turtle (Sternotherus odoratus), Northern Map Turtle (Graptemys geographica), and Snapping Turtle (Chelydra serpentina). Reptile road mortality “hotspots” occurred where each road is intersected by a naturalized utility right-of-way. Our results can be used to focus mitigation efforts in space and time to reduce mortality rates and enhance connectivity in the Ojibway Prairie Complex and Greater Park Ecosystem.

PLASMA ELECTROPHORETIC PROFILES IN THE EASTERN MASSASAUGA (SISTRURUS CATENATUS) AND INFLUENCES OF AGE, SEX, YEAR, LOCATION, AND SNAKE FUNGAL DISEASE.

The purpose of this study was to establish reference intervals of the protein electrophoretic fractions and the acute-phase proteins hemoglobin binding protein (as determined by the haptoglobin assay) and C-reactive protein (CRP) and assess any possible correlations between varying age class, sex, location (Illinois or Michigan), year, or presence of snake fungal disease (SFD). Banked plasma samples were assayed from 130 eastern massasaugas from 2009 to 2014 in Illinois and Michigan. Snakes from Michigan had higher total protein (mean: 5.50 g/dl), albumin/globulin ratio (0.42), albumin (1.59 g/dl), and gamma globulins (0.55 g/dl) than from snakes in Illinois (4.72 g/dl, 0.29, 1.03 g/dl, 0.38 g/dl, respectively). Snakes in Illinois (22.19 g/ml) had higher CRP than snakes in Michigan (10.89 mg/ml). Adults had higher gamma globulins (0.47 g/dl) than juveniles (0.28 g/dl). Males had higher alpha-2 globulins (0.98 g/dl) and CRP (21.4 mg/ml) than females (0.85, 11.6, respectively). There were no significant differences in absolute plasma proteins in SFD-positive snakes, but the percentage of gamma globulins was significantly higher in positive snakes. Future research in this area can now build on this data to determine changes in population health over time or due to specific environmental or disease threats.

Genetic Structure of Western Massasauga Rattlesnakes (Sistrurus catenatus tergeminus)

Abstract Understanding how habitat heterogeneity influences the genetic structure of populations is an important goal of conservation genetics. Species with different evolutionary histories may respond differently to contemporary habitat loss and fragmentation. Recent genetic analyses have shown high levels of genetic structure in two subspecies of Massasauga Rattlesnakes of conservation concern (Eastern Massasaugas, Sistrurus catenatus catenatus and Desert Massasaugas, Sistrurus catenatus edwardsii) living in highly fragmented habitats. Here, we complement those results with an analysis of the genetic structure of the third subspecies (Western Massasaugas, Sistrurus catenatus tergeminus), which has a largely continuous distribution in Kansas but with some isolated populations in Missouri. We found no evidence of genetic structure among the Kansas populations of Western Massasaugas, though our STRUCTURE analysis did identify the two Missouri populations as distinct clusters from each other and from the Ka...

Genetic Structure is Inconsistent with Subspecies Designations in the Western Massasauga Sistrurus tergeminus

Abstract The massasauga Sistrurus catenatus was historically divided into three subspecies, but this long-standing taxonomy has recently been called into question. Genetic research now recognizes a split of the species into the eastern massasauga S. catenatus and western massasauga S. tergeminus, with the latter split into two subspecies, the desert massasauga S. t. edwardsii and the prairie massasauga S. t. tergeminus. Although the distinction between geographically isolated populations of S. catenatus and S. tergeminus is well-supported genetically, the geographic relationships among populations of S. t. tergeminus and S. t. edwardsii remain unresolved because of incomplete sampling throughout the species’ range. This poses a difficult challenge for conservation and management of this species. Sistrurus t. tergeminus does not have state or federal conservation status, but S. t. edwardsii has been petitioned for listing under the U.S. Endangered Species Act. In this study, we used nuclear and mitochondrial DNA from 52 individuals from 7 states to explore the taxonomic and geographic relationships between S. t. tergeminus and S. t. edwardsii populations. Maximum likelihood and Bayesian inference frameworks for both nuclear and mtDNA genes indicated that S. t. tergeminus and S. t. edwardsii populations were genetically indistinguishable. However, at the species level, we did find eight well-supported mtDNA clades within S. tergeminus, including individuals from five peripheral populations in 1) Arizona and western New Mexico, 2) Colorado and Kansas, 3) Missouri, 4) Oklahoma, and 5) southern Texas. These peripherally isolated populations surrounded a larger population of individuals from north-central Texas, New Mexico, and Oklahoma that was contiguous with three additional genetically distinct populations. We conclude that the putative subspecies S. t. tergeminus and S. t. edwardsii, as currently defined, most likely represent polytypic phenotypes of S. tergeminus rather than discrete taxonomic entities. Instead, we suggest that S. tergeminus existed historically as a large, contiguous collection of populations that only recently became fragmented into several, as opposed to two, potentially discrete taxonomic entities.

Interrogating the Venom of the Viperid Snake Sistrurus catenatus edwardsii by a Combined Approach of Electrospray and MALDI Mass Spectrometry.

The complete sequence characterization of snake venom proteins by mass spectrometry is rather challenging due to the presence of multiple isoforms from different protein families. In the present study, we investigated the tryptic digest of the venom of the viperid snake Sistrurus catenatus edwardsii by a combined approach of liquid chromatography coupled to either electrospray (online) or MALDI (offline) mass spectrometry. These different ionization techniques proved to be complementary allowing the identification a great variety of isoforms of diverse snake venom protein families, as evidenced by the detection of the corresponding unique peptides. For example, ten out of eleven predicted isoforms of serine proteinases of the venom of S. c. edwardsii were distinguished using this approach. Moreover, snake venom protein families not encountered in a previous transcriptome study of the venom gland of this snake were identified. In essence, our results support the notion that complementary ionization techniques of mass spectrometry allow for the detection of even subtle sequence differences of snake venom proteins, which is fundamental for future structure-function relationship and possible drug design studies.

Multi-scale Responses of Eastern Massasauga Rattlesnakes (Sistrurus catenatus) to Prescribed Fire

The eastern massasauga rattlesnake (Sistrurus catenatus) is a threatened species that occurs in habitats frequently targeted by prescribed burns. There have been reports of massasauga mortality as a result of prescribed fires, but little is known regarding the indirect effects of fire on this species. The objective of this study was to monitor massasaugas during a prescribed fire to assess direct and indirect effects. We initially implanted radio transmitters in 13 massasaugas inhabiting an area targeted for periodic prescribed fires and tracked them following a prescribed fire to determine burn-related mortality and behavioral influences. Data loggers, temperature sensitive paint, and measuring posts were used to record detailed fire data. Of the five snakes on the burn unit at the time, two died as a result of the fire. No differences were observed in daily movements and home range sizes between burn categories (in the burn, same site not in the burn and at a nearby unburned site). Snakes on and off the burn unit at the same site exhibited the same habitat preference for wetland habitats, whereas snakes at the control site preferred herbaceous areas. Slight differences were observed in microhabitat selection related to litter depth, surface light intensity, distance to water, and surface temperature. The snakes did not appear to alter their seasonal activities as a result of the prescribed fire. The results of this study suggest ways to minimize impacts from prescribed fires on massasauga populations.