Sistrurus Catenatus Research Articles

Measuring Agreement and Discord among Hemagglutination Inhibition Assays Against Different Ophidian Paramyxovirus Strains in the Eastern Massasauga (Sistrurus catenatus catenatus)

At present, the hemagglutination inhibition (HI) assay is the sole commercially available serologic method available to detect exposure to ophidian paramyxovirus (OPMV) in snakes. During 2006, 26 eastern massasaugas (Sistrurus catenatus catenatus) were collected, and blood was sampled to determine their OPMV status. Samples from each snake were divided into 3 aliquots and tested by using commercially available HI assays against the 4 OPMV isolates used in the 3 laboratories that offer the service. All snakes were tested for antibodies by using HI assays against the green tree python (GTP), San Lucan rattlesnake (SLR), and Aruba Island rattlesnake (AIR) isolates. Twenty-five snakes were tested for antibodies against the western diamondback rattlesnake (WDR) isolate. All samples tested against the GTP and SLR were positive (26/26), whereas 56% (14/25) of the WDR assays were positive, and none (0/26) of the AIR assays yielded a positive result. There was 100% agreement between the GTP and SLR assays, and complete disagreement between the SLR and AIR, as well as the GTP and AIR assays. Kappa statistics for the GTP-WDR, SLR-WDR, GTP-AIR, SLR-AIR, and WDR-AIR indicated that the assays had less than chance agreement. The results demonstrate that current HI assays are not reliable as a sole diagnostic assay in the eastern massasauga. Furthermore, HI assays need to be evaluated by using other parameters to determine OPMV exposure in eastern massasaugas.

Roads as barriers to animal movement in fragmented landscapes

AbstractRoads can act as barriers to animal movement through mortality during crossing attempts or behavioral avoidance. This barrier effect has negative demographic and genetic consequences that can ultimately result in local or regional extinction. Here we use radio‐telemetry data on three terrestrial vertebrates (eastern massasaugaSistrurus catenatus, eastern box turtleTerrapene carolinaand ornate box turtleTerrapene ornata) to test whether roads acted as barriers to movement. Specifically, we test whether individuals avoided crossing roads by comparing the number of observed crossings with the number of road crossings predicted by randomizations of individual movement paths. All species crossed roads significantly less often than predicted by chance, indicating strong road avoidance. Results of this study showing behavioral avoidance and previous studies on road mortality indicate that roads are strong barriers to these species. High mortality during crossing attempts would select for road avoidance, reducing the number of individuals killed on roads over time but leading to genetically partitioned subpopulations due to a lack of gene flow. In species that are long‐lived and late‐maturing, negative genetic effects might not be observable over short time‐scales, thus placing populations at high risk of extinction because of a failure to detect an incrementally worsening problem. Formulating successful management strategies for many species in decline will require integrating data on road mortality, animal behavior and population genetics in order to understand more clearly the barrier effect of roads.

Accelerated exchange of exon segments in Viperid three-finger toxin genes (Sistrurus catenatus edwardsii; Desert Massasauga)

BackgroundSnake venoms consist primarily of proteins and peptides showing a myriad of potent biological activities which have been shaped by both adaptive and neutral selective forces. Venom proteins are encoded by multigene families that have evolved through a process of gene duplication followed by accelerated evolution in the protein coding region.ResultsHere we report five gene structures of three-finger toxins from a viperid snake, Sistrurus catenatus edwardsii. These toxin genes are structured similarly to elapid and hydrophiid three-finger toxin genes, with two introns and three exons. Both introns and exons show distinct patterns of segmentation, and the insertion/deletion of segments may define their evolutionary history. The segments in introns, when present, are highly similar to their corresponding segments in other members of the gene family. In contrast, some segments in the exons show high similarity, while others are often distinctly different among corresponding regions of the isoforms.ConclusionOrdered, conserved exon structure strongly suggests that segments in corresponding regions in exons have been exchanged with distinctly different ones during the evolution of these genes. Such a "switching" of segments in exons may result in drastically altering the molecular surface topology and charge, and hence the molecular targets of these three-finger toxins. Thus the phenomenon of accelerated segment switch in exons to alter targeting (ASSET) may play an important role in the evolution of three-finger toxins, resulting in a family of toxins with a highly conserved structural fold but widely varying biological activities.

Reptile Road Mortality around an Oasis in the Illinois Corn Desert with Emphasis on the Endangered Eastern Massasauga

Roads have numerous negative ecological effects on terrestrial fauna, and vehicular mortality can have significant demographic consequences for some species. We studied road mortality of reptiles around Carlyle Lake, Clinton County, Illinois, USA, from April 2000 through November 2002, to assess the impact of vehicular traffic and identify influential factors. Carlyle Lake, a popular tourism/recreation area, is situated in a larger agricultural landscape and is home to the largest Illinois population of the endangered Eastern Massasauga (Sistrurus catenatus). We documented 321 cases of reptile road mortality (84 individuals of six turtle species and 237 individuals of nine snake species) while driving our approx. 46 km study route roundtrip daily. Turtle road mortality was highest in May and June, and positively associated with precipitation and minimum daily temperature. Colubrid snake road mortality was highest in April and October, and positively associated with minimum daily temperature. We recorded 42 cases of road mortality of S. catenatus with the highest number occurring from mid-August to mid-September. Road mortality in S. catenatus was biased toward adult males, which show an increase in movement in August, coinciding with the peak of the mating season and a period of high tourist visitation. The traffic intensity on a road segment did not significantly affect the level of road mortality, but segments through high quality habitats had higher levels of mortality than segments through lower quality habitats. Based on our study on the ecology of S. catenatus, we make recommendations to reduce road mortality that should aid in the conservation of the Carlyle Lake population.

The Type Localities of Sistrurus catenatus and Crotalus viridis (Serpentes: Viperidae), with the Unraveling of a Most Unfortunate Tangle of Names

Abstract The broad and imprecise type localities of Crotalinus catenatus Rafinesque, 1818 (now Sistrurus catenatus) and Crotalinus viridis Rafinesque, 1818 (now Crotalus viridis) are re-identified based on a published account of the collector's travels as well as an examination of the relationship and contacts between the collector and the author of the type description. Both type specimens are lost. Unfortunately, enhanced resolution of the type locality of S. catenatus places it within the range of S. c. tergeminus Say, 1823 (a subsequently described subspecies). Thus, the name S. c. catenatus incontrovertibly applies to the form currently recognized as S. c. tergeminus, which in turn renders the latter as a subjective junior synonym of the former, leaving the eastern form with an unfamiliar name (Crotalus messasaugus Kirtland, 1838). To conserve prevailing usage, we are preparing an appeal to the International Commission of Zoological Nomenclature (ICZN) to allow a neotype of Sistrurus catenatus to be ...

Massasauga Home Range Patterns in the Midwest

Abstract: The massasauga (Sistrurus catenatus) has drastically declined throughout its range mainly due to habitat loss and human persecution. Populations of the massasauga that occur north and east of the Missouri River, USA, are currently candidates for listing under the United States Endangered Species Act. In areas where land managers wish to improve habitat for existing populations or create habitat for repatriation efforts, an understanding of massasauga spatial ecology is necessary to ensure that adequate sized blocks of habitat are created and properly managed. We studied spatial ecology of massasaugas at 2 sites in Wisconsin and 3 sites in Missouri over an 11‐year period. Our results indicated that male massasaugas had larger spatial requirements than all other cohorts. Our study sites supporting viable populations indicated that managers interested in restoring or enhancing massasauga habitat should use 100 ha as a minimum restoration or management target. (JOURNAL OF WILDLIFE MANAGEMENT 72(3):754–759; 2008)

Assessment of Allelic Variation Among Massasauga Rattlesnake Populations via Microsatellite Analysis

The decline in populations of the eastern massasauga rattlesnake (Sistrurus catenatus catenatus) across its range is of concern to conservation managers and the species is currently a candidate for federal listing. Because only four eastern massasauga populations are known to occur in Missouri, the species is on the Missouri Endangered Species List. We sought to produce a molecular genetic data set that could be used to inform conservation management decisions about three of these populations. Our method was to collect and analyze data from three microsatellites sites in an effort to provide insight into the genetic health of the populations and into relationships between them. Our method was controlled by inclusion of two populations of the western massasauga (Sistrurus catenatus tergeminus) from southeastern Nebraska. The final data set included 111 individuals from Missouri and Nebraska populations. Although a significant portion (92%) of alleles were shared between each population, low levels of heterozygosity were detected, indicating local inbreeding. Tests of population differentiation suggested that little to no gene flow between these populations has occurred, giving rise to unique allele frequencies and combinations which may be of high conservation value. Most notably, significant differentiation was observed between putative subpopulations at the Squaw Creek National Wildlife Refuge that are in close proximity to one another. Our results illustrate the value of molecular genetics analysis in conservation management and have important implications for the management of Missouri massasauga populations.

Movement and Growth of Neonate Eastern Massasaugas (Sistrurus catenatus)

Throughout the geographic range, adult Eastern Massasaugas (Sistrurus catenatus) exhibit plasticity in movement, fecundity, diet, and activity range size; however, the ecology of subadults remains unknown. We attached radio transmitters to 16 free-ranging neonate S. catenatus and monitored their movements and growth for up to 56 days prior to their initial hibernation. Neonate movement frequency (70%) was consistent with values reported for adults throughout the geographic range, but activity range size (0.36 ha) and mean daily distance moved (5.3 m) were smaller. Males gained significantly more mass than females over the first 50 days, but no difference in length was detected. Neonate S. catenatus returned to their general birthing area to overwinter. Because of ontogenetic shifts and differences in the spatial distribution of resources, regionally-specific management plans based on data for all age classes are essential in providing effective conservation measures.

Male Movement and Body Size Affect Mate Acquisition in the Eastern Massasauga (Sistrurus Catenatus)

Knowledge of mating system characteristics can elucidate forces driving sexual selection. In male pitvipers, both male movement tactics and body size are predicted to be important determinants of reproductive success. We used radio telemetry to monitor free-ranging Sistrurus catenatus (Eastern Massasauga) from 2000 through 2002 to determine whether male movement tactics and body size affect mate acquisition. Reproductive behaviors peaked in late July to early August. Females were accompanied by multiple males per season (up to seven); however, male mate acquisition varied considerably with only three of 17 (18%) males located more than one female during a single mating season. During the mating season, male mean daily distance moved (21.8 m) and movement frequency (77%) were higher than during the nonmating season (13.3 m, 63%). Male movement rate and body mass were positively related to the number of females acquired, and heavier males were observed accompanying females as the mating season progressed. Our results indicate that both movement tactics and body size are important in the mating system of S. catenatus; however, direct measures of reproductive success will be necessary before assessing the intensity of sexual selection.

English

Since the enactment of the Surface Mining Control and Reclamation Act (SMCRA) thousands of grassland habitats have been created in eastern North America. In western Pennsylvania over 50 species of birds including, eleven species that are either listed as threatened, endangered or as special concern, have been observed using grasslands and wetlands on reclaimed mines. In addition to these bird species, the endangered Massasauga (Sistrurus catenatus catenatus) has been observed foraging on grasslands on two mine sites in western Pennsylvania. Although the development of wildlife habitats can be incorporated into the reclamation of mine lands, the specific habitats for threatened and endangered species are generally not a defined objective of the reclamation of mine lands. Because threatened and endangered species nest and forage on grasslands and wetlands on mine lands, they should be given consideration during the reclamation of mine lands.

The venom gland transcriptome of the Desert Massasauga Rattlesnake (Sistrurus catenatus edwardsii): towards an understanding of venom composition among advanced snakes (Superfamily Colubroidea)

BackgroundSnake venoms are complex mixtures of pharmacologically active proteins and peptides which belong to a small number of superfamilies. Global cataloguing of the venom transcriptome facilitates the identification of new families of toxins as well as helps in understanding the evolution of venom proteomes.ResultsWe have constructed a cDNA library of the venom gland of a threatened rattlesnake (a pitviper), Sistrurus catenatus edwardsii (Desert Massasauga), and sequenced 576 ESTs. Our results demonstrate a high abundance of serine proteinase and metalloproteinase transcripts, indicating that the disruption of hemostasis is a principle mechanism of action of the venom. In addition to the transcripts encoding common venom proteins, we detected two varieties of low abundance unique transcripts in the library; these encode for three-finger toxins and a novel toxin possibly generated from the fusion of two genes. We also observed polyadenylated ribosomal RNAs in the venom gland library, an interesting preliminary obsevation of this unusual phenomenon in a reptilian system.ConclusionThe three-finger toxins are characteristic of most elapid venoms but are rare in viperid venoms. We detected several ESTs encoding this group of toxins in this study. We also observed the presence of a transcript encoding a fused protein of two well-characterized toxins (Kunitz/BPTI and Waprins), and this is the first report of this kind of fusion in a snake toxin transcriptome. We propose that these new venom proteins may have ancillary functions for envenomation. The presence of a fused toxin indicates that in addition to gene duplication and accelerated evolution, exon shuffling or transcriptional splicing may also contribute to generating the diversity of toxins and toxin isoforms observed among snake venoms. The detection of low abundance toxins, as observed in this and other studies, indicates a greater compositional similarity of venoms (though potency will differ) among advanced snakes than has been previously recognized.

Spatial Ecology and Multi-scale Habitat Selection by a Threatened Rattlesnake: The Eastern Massasauga (Sistrurus Catenatus Catenatus)

Using radio telemetry and geographic information systems (GIS), we investigated movement patterns, home ranges, and habitat selection by Eastern Massasauga rattlesnakes from 2003 to 2004 at an 815-ha fen preserve located in southeastern Michigan, USA. We tested habitat selection on three different scales: microhabitat (by modeling differences in climatic and structural variables between snake-selected sites and random sites, using logistic regression), macrohabitat, and landscape-scale (both by compositional analysis comparing proportions of habitat types used versus proportions available). One hundred percent minimum convex polygon (MCP) home ranges averaged 1.3 ha, and daily movement rates averaged 6.9 m/d. Models predicted that snakes exhibit complex microhabitat selection based on multiple climatic and structural variables including soil temperatures, relative humidity, canopy cover, litter depth, and various vegetation parameters. Snakes actively establish home ranges in the broader landscape by selecting areas with disproportionate quantities of emergent wetland, scrub/shrub wetland, and lowland hardwood habitats. Upland hardwood and all human-altered landscapes were rarely used, even though they were available. This has potentially serious conservation implications. Encroachment of these types of landscapes into areas of suitable habitat could severely restrict movement and home range sizes of these snakes. Potential disruption of movement patterns and gene flow of remaining populations could be extremely detrimental to this species.

Venom Proteomes of Closely RelatedSistrurusRattlesnakes with Divergent Diets

The protein composition of the venoms of the three subspecies of Sistrurus catenatus (S. c. catenatus, tergeminus, and edwardsii) and a basal species, Sistrurus miliarius barbouri, were analyzed by RP-HPLC, N-terminal sequencing, MALDI-TOF peptide mass fingerprinting, and CID-MS/MS. The venoms of the four Sistrurus taxa contain proteins from 11 families. The protein family profile and the relative abundance of each protein group in the different venoms are not conserved. Myotoxins and 2-chain PLA2s were detected only in S.c. catenatus and S.c. tergeminus, whereas C-type BPP and Kunitz-type inhibitors were exclusively found in S.c. edwardsii and Sistrurus miliarius barbouri. Among major protein families, taxa were most similar in their metalloproteases (protein similarity coefficient value: 34%) and most divergent in PLA2s (12%), with values for disintegrins and serine proteases lying between these extremes (25 and 20%, respectively). The patterns of venom diversity points to either a gain in complexity in S. catenatus taxa or a loss of venom diversity occurring early on in the evolution of the group involving the lineage connecting S. milarius to the other taxa. The high degree of differentiation in the venom proteome among recently evolved congeneric taxa emphasizes the uniqueness of the venom composition of even closely related species that have different diets. Comparative proteomic analysis of Sistrurus venoms provides a comprehensive catalog of secreted proteins, which may contribute to a deeper understanding of the biology and ecology of these North American snakes and may also serve as a starting point for studying structure-function correlations of individual toxins.

MOVEMENT AND MACROHABITAT SELECTION OF THE EASTERN MASSASAUGA IN A FEN HABITAT

The eastern massasauga, Sistrurus c. catenatus, is a small rattlesnake threatened with extirpation throughout its range. Massasaugas occur in a variety of habitats and adequate knowledge of their natural history at local scales is essential for effective management. We used radiotelemetry to document patterns of movement and macrohabitat selection of massasaugas in a fen environment, an important, but understudied, habitat. Based on both 100% minimum convex polygons and 95% kernel density, seasonal home ranges of males were larger than those of nongravid females which, in turn, were larger than those of gravid females. Activity center estimations followed the same trend as the seasonal range estimations. Similarly, activity centers (50% kernel density) of males were larger than those of nongravid females which were larger than those of gravid females. Nongravid females and gravid females differed in their mean frequency of daily movement, distance moved per day and total distance moved in a season. Males also differed from gravid females in these three regards, but only differed from nongravid females in distance moved per day. Compositional analysis of both 100% MCPs and 95% kernel densities indicated a preference for emergent wetland vegetation by all individuals; however, wooded areas and meadows were used to a lesser extent.

Effects of Mowing and Summer Burning on the Massasauga (Sistrurus catenatus)

Prescribed fire is used to reduce coverage of woody vegetation in early successional habitats, but burning may also result in direct and indirect mortality of reptiles inhabiting the burn site. Mowing prior to burning has been hypothesized to render grassland habitats unsuitable for the massasauga (Sistrurus catenatus), thereby reducing the number of individuals that may be affected in the management unit at the time of burning. I evaluated the impact of mowing prior to summer burning on massasaugas at Squaw Creek National Wildlife Refuge, in northwestern Missouri, during the summer of 2003 using radiomarked snakes. Pre-burn mowing resulted in the direct mortality of three (43%) of seven radiomarked massasaugas present in the treatment area. Prescribed fire resulted in a mortality of one of two remaining individuals. Pre-burn mowing did not reduce mortalities as hypothesized and likely added to the overall snake mortality rate. Management alternatives other than mowing and prescribed fire when snakes are active should be considered when managing massasauga habitat.

Utility of a set of microsatellite primers developed for the massasauga rattlesnake (Sistrurus catenatus) for population genetic studies of the timber rattlesnake (Crotalus horridus)

AbstractI tested six microsatellite DNA primer pairs developed for the massasauga rattlesnake (Sistrurus catenatus) on a sample population of the timber rattlesnake (Crotalus horridus). It had been speculated in a previous publication that cross‐species amplification would not be worthwhile across the two rattlesnake genera. However, for this primer set (the only one currently published for the genus Sistrurus), successful amplification at each locus was accomplished for all loci with an annealing temperature of 57 °C and locus‐specific buffer conditions. Each locus was polymorphic, with the number of alleles per locus ranging from two to 12. Significant heterozygote deficits were detected for three loci (Scu01, Scu05 and Scu07). For Scu01, all individuals were homozygous for the same allele except one female who was homozygous for a different allele. This same female was also homozygous for a rare allele at Scu07. When this female was removed from the data set, the number of observed heterozygotes at Scu01 and Scu07 did not differ significantly from random expectations. However, a large heterozygote deficit persisted at Scu05 (despite subsampling), suggesting that this locus may not be useful for population genetic studies of timber rattlesnakes. Despite some limitations, this set of primers may be a useful complement to those already developed for the genus Crotalus. Moreover, the results of this study seem to provide new justification for further studies of cross‐species amplification of microsatellite loci across the two rattlesnake genera.

Hibernation Site Selection by Eastern Massasauga Rattlesnakes (Sistrurus catenatus catenatus) near Their Northern Range Limit

Abstract Hibernation sites at higher latitudes must protect snakes from colder conditions for longer periods of time. Because fewer locations are likely to be suitable, hibernation site availability may restrict the northern distribution of snakes. We considered overwinter mortality, hibernation site fidelity, and the abundance of suitable hibernation sites based on surface features to assess whether Massasauga Rattlesnakes are likely to be limited by hibernation site availability on the Bruce Peninsula, Ontario, Canada. We used three years of radio telemetry to locate 46 hibernation sites of 32 individual snakes. Snakes hibernated individually in old root systems, rodent burrows, and rock crevices in forested areas. Hibernation sites could be differentiated from forested areas generally available to snakes but not from locations with holes and crevices in the immediate vicinity of hibernation sites. Few snakes hibernated in the same location in consecutive years, although most (>70%) hibernated within 10...

A test of the hierarchical model of habitat selection using eastern massasauga rattlesnakes ( Sistrurus c. catenatus)

Understanding the process animals follow to select habitat, rather than just documenting the habitat they use, will improve our ability to predict how the animals use habitat in other locations and how they will respond to changes in habitat. Animals are usually assumed to select habitats hierarchically, preferentially using specific macrohabitats at a landscape scale and specific microhabitats within the preferred macrohabitats. We used four years of telemetry data from 34 individuals to test this hierarchical model of habitat selection with eastern massasauga rattlesnakes ( Sistrurus c. catenatus) in Ontario. Snakes were selective at the microhabitat scale, preferentially using locations with closer retreat sites and shrubs than random. Gravid females were most selective, using sites with more rock cover and less canopy closure than sites used by males and nongravid females. Snakes preferred forested habitats for hibernation and steadily increased their use of open, wetland, and edge habitats to a peak in mid-summer. Landscape-scale habitat preferences were generally mild and could be explained by the relative availability of suitable microhabitat within habitats, suggesting habitat selection was primarily driven by microhabitat preferences. The lack of selectivity at the landscape scale may be a consequence of fine-grained differences between habitats that allow massasauga rattlesnakes to find suitable microhabitats in all available macrohabitats. For species that select habitat primarily at the microhabitat scale (e.g., the rattlesnakes we studied), landscape-scale modeling of habitat use will only be effective to the extent habitats reflect the availability of suitable microhabitat within.

HEMATOLOGY, PLASMA BIOCHEMISTRY, AND ANTIBODIES TO SELECT VIRUSES IN WILD-CAUGHT EASTERN MASSASAUGA RATTLESNAKES (SISTRURUS CATENATUS CATENATUS) FROM ILLINOIS

During the 2004 field season, blood was collected from Eastern massasauga rattlesnakes (Sistrurus catenatus catenatus) in the Carlyle Lake (Carlyle, Illinois, USA) and Allerton Park (Monticello, Illinois, USA) populations to derive baseline complete blood count and plasma biochemistry data and to assess the prevalence of antibodies to West Nile virus (WNV) and ophidian paramyxovirus (OPMV). Massasaugas were located for sampling through visual encounter surveys. Body weight, snout-vent length, total protein, globulins, sodium, and potassium were normally distributed among the survey population. Aspartate aminotransferase, creatine kinase, albumin, calcium, uric acid, white blood cell count, heterophils, lymphocytes, monocytes, eosinophils, and basophils were non-normally distributed within these animals. Female snakes had significantly shorter tail lengths; lower blood glucose, packed cell volumes, and absolute azurophil counts; and higher plasma calcium and phosphorus concentrations than did males. None of the snakes tested (n=21) were seropositive for WNV, whereas all (n=20) were seropositive for OPMV.

A REPATRIATION STUDY OF THE EASTERN MASSASAUGA (SISTRURUS CATENATUS CATENATUS) IN WISCONSIN

The use of relocations, repatriations, and translocations as amphibian and reptile conservation strategies has received much debate. In the case of endangered species, their use may outweigh the potential negative consequences. We performed an experimental repatriation of the eastern massasauga (Sistrurus catenatus catenatus), which has experienced range-wide population declines and extirpations. The experiment included measures to minimize negative conspecific effects to the donor populations as well as inter-species effects on the release and donor sites. Snakes released during late July had lower mortality rates, larger home ranges, and gained more mass than snakes released in early September. The July release cohort also successfully reproduced, while no breeding activity was observed with September release snakes. Results of this study suggest that repatriation may be a viable method of restoring eastern massasauga populations. We hope the methods and conservation measures used in this experiment wil...