Behavioral and life history responses of eastern massasauga rattlesnakes (Sistrurus catenatus catenatus) to human disturbance

Parks and nature reserves protect important natural habitats but also provide public opportunities for outdoor recreational activities that may have unintended negative effects on wildlife. We examined the response of eastern massasauga rattlesnakes (Sistrurus catenatus catenatus) to inadvertent disturbance by humans in Killbear Provincial Park, Ontario, Canada. Radio telemetry of 25 adult snakes over two active seasons revealed that, as disturbance increased, gravid females were less visible to observers, but the visibility of non-gravid females and males did not change. Mean distance moved per day decreased and mean time between moves greater than 10 m increased in gravid females, non-gravid females and males with increasing exposure to human disturbance. However, mark-recapture data revealed no differences in the condition or growth rates of snakes, or in the litter size of gravid females, between individuals captured in disturbed and undisturbed study areas. While it is possible that the behavioral responses we observed are not sufficient to have life history consequences, more detailed information on the exposure of individual snakes to human activity is necessary before the conclusion that disturbance is not detrimental to snakes can be accepted. Similarly, other potential negative effects of human disturbance not investigated here remain to be explored.     

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.     

Effects of parasitic infection and radio-transmitters on condition, hematological characteristics and corticosterone concentrations in Texas ratsnakes

Parasites are a health concern of many wildlife species, although their effect on reptiles is poorly studied. Here we examine effects of hemogregarine and external parasites on Texas ratsnake Elaphe obsoleta white blood cell (WBC) concentrations, WBC differentials, heterophil/lymphocyte ratios, packed cell volume (PCV), corticosterone concentrations and body condition. We found little evidence that either ectoparasites or hemogregarines affected the health of Texas ratsnakes. We found a seasonal increase in corticosterone, consistent with glucocorticoids priming the snakes to deal with higher predation risks later in the season. We also examined whether the potential stress of carrying a surgically implanted radio-transmitter compounds any parasitic health effects. We found no effect of transmitters on most aspects of health. We did find equivocal evidence that WBC concentrations were higher in snakes with transmitters and that PCV decreased following transmitter implantation. Although our results generally support the view that data collected using radio-telemetry are unlikely to be biased due to adverse health effects of transmitters, the growing importance of telemetry for studies of snakes and other taxa argues for further research on this topic. When possible, researchers should design telemetry studies in such a way that assessing potential heath effects of transmitters is one of the objectives.     

Kin recognition in rattlesnakes

Snakes are often regarded as the least social of all vertebrate groups, but this assumption stems from the fact that they are secretive and difficult to observe in nature, rather than direct evidence. Recent studies have revealed a surprising degree of social complexity in snakes. Here, I examine the ability of captive-raised timber rattlesnakes (Crotalus horridus) to recognize siblings by measuring the mean separation distance and frequency of contact between pairs of individuals housed together. The results show that female siblings associate more closely with each other than nonsibling pairs. Previous studies have shown that timber rattlesnakes occupying the same hibernacula have higher relatedness than snakes using neighbouring hibernacula, and frequently form social aggregations. Rattlesnakes exhibit other characteristics consistent with advanced sociality, including group defence, conspecific alarm signals and maternal defence of young. These findings reinforce the notion that, rather than being solitary and asocial, some snake species may form family groups.     

Resource selection by the eastern massasauga rattlesnake on managed land in southwestern Michigan

The eastern massasauga rattlesnake (Sistrurus catenatus catenatus) has experienced population declines throughout its range and is now a candidate for federal protection. However, little is known about massasauga habitat selection in Michigan, particularly in actively managed landscapes. Our objectives were to: 1) quantify whether massasaugas in southwestern Michigan select certain vegetation types disproportionately to their availability and 2) quantify whether the vegetation structure associated with snake locations differed between managed (e.g., burning, woody species removal) and unmanaged stands. We implanted radio transmitters in 51 snakes from 2004 to 2005 and 2008 to 2009. We quantified second-order resource selection using compositional analysis, and modeled the effect of habitat management efforts on vegetation using 4 structural variables. All snakes selected cover types disproportionately to their availability (P = 0.001); a ranking matrix ordered the vegetation types, from most to least used, as: early-mid successional deciduous wetland > early-mid successional deciduous upland > developed > late successional mixed lowland forest > late successional deciduous upland forest. We found that snakes in managed areas were associated with greater amounts of dead herbaceous cover (P = 0.005) and less woody stem density (P < 0.001) and tree dominance (P < 0.001) than were snakes in unmanaged areas; however, live herbaceous cover was comparable. Our results can be used by regional managers to provide early and mid successional habitat with structure similar to that selected by snakes in Michigan. © 2011 The Wildlife Society.     

Inferring species-level phylogenies and taxonomic distinctiveness using multilocus data in Sistrurus rattlesnakes

Phylogenetic relationships and taxonomic distinctiveness of closely related species and subspecies are most accurately inferred from data derived from multiple independent loci. Here, we apply several approaches for understanding species-level relationships using data from 18 nuclear DNA loci and 1 mitochondrial DNA locus within currently described species and subspecies of Sistrurus rattlesnakes. Collectively, these methods provide evidence that a currently described species, the massasauga rattlesnake (Sistrurus catenatus), consists of two well-supported clades, one composed of the two western subspecies (S. c. tergeminus and S. c. edwardsii) and the other the eastern subspecies (S. c. catenatus). Within pigmy rattlesnakes (S. miliarius), however, there is not strong support across methods for any particular grouping at the subspecific level. Monophyly based tests for taxonomic distinctiveness show evidence for distinctiveness of all subspecies but this support is strongest by far for the S. c. catenatus clade. Because support for the distinctiveness of S. c. catenatus is both strong and consistent across methods, and due to its morphological distinctiveness and allopatric distribution, we suggest that this subspecies be elevated to full species status, which has significant conservation implications. Finally, most divergence time estimates based upon a fossil-calibrated species tree are > 50% younger than those from a concatenated gene tree analysis and suggest that an active period of speciation within Sistrurus occurred within the late Pliocene/Pleistocene eras.     

Effectiveness of Short-Distance Translocation and its Effects on Western Rattlesnakes

ABSTRACT Short-distance translocation (SDT) is commonly used to mitigate snake-human interactions, yet little is known about its effectiveness or its effects on behavior and welfare of snakes. Between April 2004 and October 2005, we evaluated SDT as a conservation and management tool by investigating how 500-m SDT affected spatial ecology, body condition, and behavior of western rattlesnakes (Crotalus oreganus) surgically implanted with radiotransmitters in a field study near Osoyoos, British Columbia, Canada. Of 14 rattlesnakes subjected to SDT, 12 (85.7%) returned on ≥1 occasion (range 1–7 times) to the general area they were removed from. Rattlesnakes that underwent SDT showed an increase in total distance moved over an active season compared to non-translocated snakes, but there was no evidence to suggest SDT had an effect on activity range size. There was no evidence to suggest SDT affected body condition, behavior, or mortality rates. Short-distance translocation to high-quality undisturbed habitats was unsuccessful as a long-term solution to snake-human conflict because most translocated snakes returned to conflict areas within a short time (x̄x = 19.9 ± 8.7 days). However, SDT may be an effective short-term tool to manage snake-human conflict in areas where human presence is seasonal or short-lived if careful attention is paid to species-specific biological needs, habitat quality at the release site, and the location of the release site in relation to conflict areas.     

Abbreviata terrapenis (Nematoda: Physalopteridae): an accidental parasite of the banded rock rattlesnake (Crotalus lepidus klauberi)

The nematode, Abbreviata terrapenis (Physalopteridae) was found in 16 (6%) of 267 banded rock rattlesnakes (Crotalus lepidus klauberi) from Arizona and New Mexico. Abbreviata terrapenis in C. lepidus represents an accidental parasite in that "infection" was acquired by the ingestion of lizard prey. Feeding captive snakes on wild-caught lizards poses a risk of introducing nematodes to the snakes.     

Snake venomics of Crotalus tigris: the minimalist toxin arsenal of the deadliest Neartic rattlesnake venom. Evolutionary Clues for generating a pan-specific antivenom against crotalid type II venoms

We report the proteomic and antivenomic characterization of Crotalus tigris venom. This venom exhibits the highest lethality for mice among rattlesnakes and the simplest toxin proteome reported to date. The venom proteome of C. tigris comprises 7-8 gene products from 6 toxin families; the presynaptic β-neurotoxic heterodimeric PLA(2), Mojave toxin, and two serine proteinases comprise, respectively, 66 and 27% of the C. tigris toxin arsenal, whereas a VEGF-like protein, a CRISP molecule, a medium-sized disintegrin, and 1-2 PIII-SVMPs each represent 0.1-5% of the total venom proteome. This toxin profile really explains the systemic neuro- and myotoxic effects observed in envenomated animals. In addition, we found that venom lethality of C. tigris and other North American rattlesnake type II venoms correlates with the concentration of Mojave toxin A-subunit, supporting the view that the neurotoxic venom phenotype of crotalid type II venoms may be described as a single-allele adaptation. Our data suggest that the evolutionary trend toward neurotoxicity, which has been also reported for the South American rattlesnakes, may have resulted by pedomorphism. The ability of an experimental antivenom to effectively immunodeplete proteins from the type II venoms of C. tigris, Crotalus horridus , Crotalus oreganus helleri, Crotalus scutulatus scutulatus, and Sistrurus catenatus catenatus indicated the feasibility of generating a pan-American anti-Crotalus type II antivenom, suggested by the identification of shared evolutionary trends among South and North American Crotalus species.     

AN INTRAPERITONEAL RADIO TRANSMITTER FOR SEA OTTERS

A small intraperitoneal radio transmitter was developed and used successfully in California sea otters. The transmitter weighs about 120 g and has an internal antenna. Thirty-five implanted transmitters were located for an average of 526 d. The carcasses of five animals that died were recovered; there were no complications associated with the transmitters in these individuals. Reproductive performance of the adult females with implanted transmitters appeared normal. The main advantages of this transmitter are its reliability and long life. It has enabled the collection of significant new information on California sea otters.     

Genetic identity of endangered massasauga rattlesnakes (Sistrurus sp.) in Missouri

An important application of DNA-based genetic techniques in conservation genetics is to establish the taxonomic identity of individuals whose ancestry is uncertain, especially those from declining populations. Massasauga rattlesnakes (Sistrurus catenatus) in Missouri currently persist in three isolated populations and have been classified as eastern massasauga rattlesnakes (S. c. catenatus), which is a candidate for listing as a Federally Threatened or Endangered species. However, previous morphological evidence has suggested that these snakes are either hybrids between the eastern massasauga (S. c. catenatus) and the non-threatened western massasauga (S. c. tergeminus) or are pure S. c. tergeminus. Here, we analyze microsatellite DNA and mtDNA variation to assess the taxonomic identity of individuals from two of the three populations specifically those found in Holt and Linn Counties, Missouri. Population and phylogenetic analyses strongly support the conclusion that snakes in both populations are genetically most similar to reference S. c. tergeminus individuals from Kansas and are not related to S. c. catenatus individuals from Illinois and Ohio. These results argue that the current classification of these snakes as endangered S. c. catenatus is unwarranted and hence that the overall range-wide numbers of S. c. catenatus are less than previously estimated. Nonetheless the Missouri populations, while not part of the federally listed taxon, are strongly deserving of protected status at the state level because of their rarity within the state.     

Probing,Assessment, and Management during Interactions between Ground Squirrels and Rattlesnakes

The predator-prey relationship between California ground squirrels (Spermophilus beecheyi) and northern Pacific rattlesnakes (Crotalus viridis) is a useful system for exploring conflict and assessment. Rattlesnakes are major predators of ground squirrel pups, but pose a less significant threat to adult squirrels. Adults approach, harass, and even attack rattlesnakes in defense of their pups. Two factors that may influence risk to both squirrel and snake during encounters are the size and body temperature of the rattlesnake. We used high-speed video to analyze the strikes of rattlesnakes of various sizes tested at different body temperatures. Results indicate that warmer snakes are more dangerous because they strike with higher velocity, greater accuracy, and less hesitation. Similarly, larger snakes are more dangerous because they can strike farther and at higher speeds, and keep their fangs embedded longer. Thus, ground squirrels would benefit from extracting information about a rattlesnake's size and temperature. The converse of our results is that cooler, smaller rattlesnakes may be more vulnerable. These snakes could mitigate their risk by avoiding dangerous adversaries and minimizing cues that divulge their weaknesses. Such tactics might explain the active probing that squirrels direct at rattlesnakes, which may function to overcome a snake's resistance to disclosing its vulnerability.     

Removal of nestling radio-transmitters by adult Sprague’s Pipit (Anthus spragueii)

Fledgling birds are notoriously difficult to find and capture because of their cryptic behavior. As a result, researchers usually affix transmitters to nestlings to study aspects of post-fledging ecology. However, parents may attempt to remove nestling transmitters, which could negatively impact nestlings. We attached radio-transmitters to 95 Sprague’s Pipit (Anthus spragueii) nestlings using a modified Rappole and Tipton leg harness. Within 1–2 days after transmitter attachment, we recorded six cases of parents removing transmitters from nestlings and depositing the transmitters outside the nest. At one of these nests, we videotaped parents pecking and pulling at nestlings that had transmitters and also dragging a nestling out of the nest by the transmitter. Of 12 video-monitored nests where we attached transmitters to nestlings, 33% had cases of parents attempting to remove transmitters by pecking and pulling at nestlings. Our observations highlight the need to closely monitor nestlings with transmitters so that researchers have the opportunity to reattach transmitters should parents remove them and to monitor the health of nestlings. Video-monitoring nests could also help to identify any unseen, negative impacts on nestlings due to transmitter attachment.     

Stimulus control of predatory behaviour in red spitting cobras (Naja mossambica pallida) and prairie rattlesnakes (Crotalus v. viridis)

Two experiments examined the responses of red spitting cobras (Naja mossambica pallida) to stimulus properties of rodent prey. In experiment 1 cobras exhibited elevated rates of tongue flicking (RTF) and trail-following behaviour after striking mice and after 15-s presentations of visual-chemical-thermal cues arising from mice held just out of striking range. Disturbance with a clean snake hook did not produce similar effects. In experiment 2 these cobras were compared with prairie rattlesnakes (Crotalus v. viridis). All snakes were exposed to five stimulus conditions in their home cages: (1) 3 s of disturbance (D) with a clean snake hook; (2) 15 s of D; (3) 3 s inspection of a live mouse held out of striking range (NS); (4) 15 s of NS; and (5) a presentation of a live mouse inside striking range (S). The snakes always struck in the latter condition, usually within 3 s. Rattlesnakes exhibited elevated RTF only after S, whereas cobras did so after 15 s of both NS and S. The performance of rattlesnakes was consistent with the assumption that these animals are ambushers; that of cobras was consistent with the assumption that these animals are active hunters which will chase and catch visually detected prey.     

Use of Implanted Radiotransmitters to Estimate Survival of Greater Sage-Grouse Chicks

ABSTRACT Reduced chick survival has been implicated in declines of greater sage-grouse (Centrocercus urophasianus) populations. Because monitoring survival of unmarked sage-grouse chicks is difficult, radiotelemetry may be an effective technique to estimate survival rates, identify causes of mortality, and collect ecological data. Previous studies have used subcutaneous implants to attach radiotransmitters to hatchlings of several species of birds with precocial young. Previous researchers who used subcutaneous implants in free-ranging populations removed chicks from the capture location and implanted transmitters at an alternate site. Because logistics precluded removing newly hatched greater sage-grouse chicks from the field, we evaluated a method for implanting transmitters at capture locations. We captured 288 chicks from 52 broods and monitored 286 radiomarked chicks daily for 28 days following capture during May and June 2001–2002. Two (>1%) chicks died during surgery and we did not radiomark them. At the end of the monitoring period, 26 chicks were alive and 212 were dead. Most (98%, 207/212) radiomarked chick mortality occurred < 21 days posthatch and predation (82%, 174/212) was the primary cause of death. Necropsies of 22 radiomarked chicks did not indicate inflammation or infection from implants, and they were not implicated in the death of any chicks. Fate of 48 chicks was unknown because of transmitter loss (n = 16), radio failure (n = 29), and brood mixing (n = 3). Overall, the 28-day chick survival rate was 0.220 (SE = 0.028). We found that mortalities related to the implant procedure and transmitter loss were similar to rates reported by previous researchers who removed chicks from capture sites and implanted transmitters at an alternate location. Subcutaneous implants may be a useful method for attaching transmitters to newly hatched sage-grouse chicks to estimate survival rates, identify causes of mortality, and collect ecological data.     

Response of timber rattlesnakes to commercial logging operations

Forest management practices in the eastern United States directly impact large parcels of land that serve as habitat for timber rattlesnakes (Crotalus horridus). We assessed the behavioral response of timber rattlesnakes to commercial logging activities and the impact of such activities on a timber rattlesnake population in northcentral Pennsylvania. We radiotelemetrically monitored 67 individual snakes over periods of up to 4 years, marked and recaptured 306 snakes, and conducted search and survey efforts before, during, and after commercial logging operations on 3 timber sale parcels (totaling 154.2 ha). Location and timing of timber sales created the maximum opportunity for interaction of snakes with logging operations and with altered habitat. Observed logging-related mortality of snakes was low (<2% of the population/yr), but potential mortality could have reached 7%. Logging activity and resulting habitat changes did not alter behavior or movement patterns of telemetrically monitored snakes. Snakes with established activity ranges in timber sale areas continued to use these areas both during and after logging operations. Similarly, snakes with activity patterns that did not include timber sale areas did not alter their movement patterns to include such sites in the short-term. Timbering increased structural diversity of the habitat and, concurrently, diversity of habitat used by timber rattlesnakes increased. Our results suggest that the opportunity exists to develop forest management practices that provide timber products while limiting impacts on behavior and habitat use of timber rattlesnakes. To further reduce impacts to timber rattlesnake populations we recommend that management agencies require commercial logging contractors, sub-contractors, and field employees to adhere strictly to a policy that prohibits the intentional killing of rattlesnakes encountered during logging activities. © 2010 The Wildlife Society.     

Venom proteomes of closely related Sistrurus rattlesnakes 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.     

Rattling Behavior of Prairie Rattlesnakes (Crotalus viridis viridis,Viperidae) in Relation to Sex,Reproductive Status,Body Size,and Body Temperature

We examined whether sex, reproductive status, body size, or body temperature of prairie rattlesnakes (Crotalus viridis viridis) was related to when snakes rattled in response to an approaching observer. We found that gravid females allowed significantly closer approaches than males, suggesting that females relied on crypsis to avoid predation, possibly because pregnancy constrained their locomotive ability. Smaller snakes allowed significantly closer approaches than did larger snakes. Smaller snakes may be more cryptic or slower, which may influence their waiting to rattle until the observer was close. Overall, we found no consistent relationship between the distance from the observer that a snake rattled and its body temperature. However, cooler gravid females allowed closer approaches by the observer than did warmer gravid females. In summary, reproductive status, body size, and body temperature appear to influence the costs and benefits of crypsis vs. active defense of rattlesnakes.     

Effects of external and surgically implanted dummy radio transmitters on mortality, swimming performance and physiological status of juvenile masu salmon Oncorhynchus masou

The effects of external and surgically implanted radio transmitters on juvenile masu salmon Oncorhynchus masou were examined. External attachment of transmitters significantly decreased the survival of fish and caused a decreased critical swimming speed compared with surgical implantation. Although plasma cortisol, plasma glucose and haematocrit values did not differ significantly among groups, it appeared that the most suitable transmitter attachment method for juvenile O. masou may be surgical implantation.     

Rattlesnake predatory behaviour: Mediation of prey discrimination and release of swallowing by cues arising from envenomated mice

Responses of rattlesnakes to envenomated mice were examined in five experiments. In experiment 1 rattlesnakes (Crotalus durissus terrificus and C. viridis viridis) discriminated mice that they had envenomated, as indexed by number of tongue flicks and accumulated investigation time, when these prey items were paired with control mice killed by the experimenter. Experiment 2 demonstrated that rattlesnakes also exhibited this discrimination when presented with mice envenomated by a conspecific and controls killed by the experimenter. In experiments 1 and 2, we observed that rattlesnakes delivered a large number of tongue flicks to exudates associated with nasal-oral tissues of envenomated mice. It has commonly been noted that rattlesnakes typically swallow envenomated, dead mice head first. In experiment 3 this observation was statistically verified. Evidence obtained in experiment 4 indicated that nasal-oral tissues of envenomated, dead mice were discriminated from anogenital tissues by rattlesnakes. Cues arising from the nasal-oral tissues probably (1) assisted the snakes in locating the head-end of the rodent, and (2) released the swallowing modal-action pattern, the final phase of the predatory sequence. In experiment 5, rattlesnakes exhibited no discrimination between nasal-oral and anogenital tissues of non-envenomated, dead mice, indicating that the results of experiment 4 were probably dependent upon effects of envenomation.