Habitat specificity and home-range size as attributes of species vulnerability to extinction: a case study using sympatric rattlesnakes

Large home-range size and habitat specificity are two commonly cited ecological attributes that are believed to contribute to species vulnerability. The eastern diamondback rattlesnake Crotalus adamanteus is a declining species that occurs sympatrically with the more abundant canebrake rattlesnake Crotalus horridus in a portion of the south-eastern Coastal Plain, USA. In this study, we use the ecological similarities of the two species as experimental controls to test the role of home-range size and habitat specificity in the imperilment of the eastern diamondback rattlesnake. We used analysis of variance to investigate differences in home-range size between the two species, and home-range selection was modeled as habitat use versus availability with a case control sampling design using logistic regression. We failed to detect differences in home-range size between the two species; therefore, we could not identify home-range size as an attribute contributing to the imperilment of eastern diamondback rattlesnakes. Eastern diamondback rattlesnakes selected pine savannas to a degree that suggests that the species is a habitat specialist. Of the two factors examined, habitat specificity to the imperiled longleaf pine ecosystem may be a significant contributor to the decline of the eastern diamondback rattlesnake.     

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.     

PCR primers for microsatellite loci in the tiger rattlesnake (Crotalus tigris,Viperidae)

The tiger rattlesnake (Crotalus tigris) is found only in the Sonoran Desert of North America, where it inhabits rocky foothills that are increasingly being affected by urban encroachment. In order to continue a long‐term study of the demography and movements of tiger rattlesnakes around Tucson, Arizona, we identified six novel polymorphic microsatellite loci for this species. All loci exhibited high variability (five to 41 alleles). These markers are useful for studies of paternity, population structure, and assessing appropriate destinations for translocated animals.     

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

I 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.     

Characterization of microsatellite loci isolated in midget faded rattlesnake (Crotalus viridis concolor)

Primers for five polymorphic microsatellite loci were developed for the midget faded rattlesnake (Crotalus viridis concolor), a rare subspecies of western rattlesnake (Crotalus viridus) found only in parts of Wyoming, Colorado, and Utah. Five polymorphic microsatellites were isolated, four of which had relatively high levels of diversity (eight to nine alleles). We found only two departures from Hardy–Weinberg equilibrium and they occurred in different loci, so null alleles are likely not a problem. Moreover, we found that no two loci were linked. These loci will be applicable for population genetic analysis and perhaps analysis of paternity and mating systems.     

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.     

Black Bear Reactions to Venomous and Non‐venomous Snakes in Eastern North America

Bears are often considered ecological equivalents of large primates, but the latter often respond with fear, avoidance, and alarm calls to snakes, both venomous and non‐venomous, there is sparse information on how bears respond to snakes. We videotaped or directly observed natural encounters between black bears (Ursus americanus) and snakes. Inside the range of venomous snakes in Arkansas and West Virginia, adolescent and adult black bears reacted fearfully in seven of seven encounters upon becoming aware of venomous and non‐venomous snakes; but in northern Michigan and Minnesota where venomous snakes have been absent for millennia, black bears showed little or no fear in four encounters with non‐venomous snakes of three species. The possible roles of experience and evolution in bear reactions to snakes and vice versa are discussed. In all areas studied, black bears had difficulty to recognize non‐moving snakes by smell or sight. Bears did not react until snakes moved in 11 of 12 encounters with non‐moving timber rattlesnakes (Crotalus horridus) and four species of harmless snakes. However, in additional tests in this study, bears were repulsed by garter snakes that had excreted pungent anal exudates, which may help explain the absence of snakes, both venomous and harmless, in bear diets reported to date.     

Prey‐driven behavioral habitat use in a low‐energy ambush predator

Food acquisition is an important modulator of animal behavior and habitat selection that can affect fitness. Optimal foraging theory predicts that predators should select habitat patches to maximize their foraging success and net energy gain, likely achieved by targeting areas with high prey availability. However, it is debated whether prey availability drives fine‐scale habitat selection for predators. We assessed whether an ambush predator, the timber rattlesnake (Crotalus horridus), exhibits optimal foraging site selection based on the spatial distribution and availability of prey. We used passive infrared camera trap detections of potential small mammal prey (Peromyscus spp., Tamias striatus, and Sciurus spp.) to generate variables of prey availability across the study area and used whether a snake was observed in a foraging location or not to model optimal foraging in timber rattlesnakes. Our models of small mammal spatial distributions broadly predicted that prey availability was greatest in mature deciduous forests, but T. striatus and Sciurus spp. exhibited greater spatial heterogeneity compared with Peromyscus spp. We found the spatial distribution of cumulative small mammal encounters (i.e., overall prey availability), rather than the distribution of any one species, to be highly predictive of snake foraging. Timber rattlesnakes appear to forage where the probability of encountering prey is greatest. Our study provides evidence for fine‐scale optimal foraging in a low‐energy, ambush predator and offers new insights into drivers of snake foraging and habitat selection.     

Evaluating Basking-Habitat Deficiency in the Threatened Eastern Massasauga Rattlesnake

ABSTRACT Woody plant succession is hypothesized to threaten many reptile populations by reducing the amount of solar energy available for thermoregulation. Mitigation via vegetation management is often recommended; however, the need for such management practices rarely has been evaluated. We examined the need for basking-site enhancement for the eastern massasauga rattlesnake (Sistrurus c. catenatus; hereafter EMR) in New York, USA, where only 2 populations remain: one at an open-canopy site and another at a closed-canopy site. Microhabitat temperatures were substantially lower at the closed-canopy site, where EMRs selected the warmest available basking sites. Eastern massasauga rattlesnakes in the open-canopy population selected basking sites that afforded greater cryptic cover. We recommend experimental reduction of shrub cover to improve EMR basking habitat at the closed-canopy site. More generally, we caution that management efforts to reduce shrub cover for basking EMRs should maintain adequate cryptic cover.     

Fossils and phylogeny uncover the evolutionary history of a unique antipredator behaviour

Recently, two squirrel species (Spermophilus spp.) were discovered to anoint their bodies with rattlesnake scent as a means of concealing their odour from these chemosensory predators. In this study, we tested multiple species with predator scents (rattlesnake and weasel) to determine the prevalence of scent application across the squirrel phylogeny. We reconstructed the evolutionary history of the behaviour using a phylogenetic analysis and fossil records of historic predator co‐occurrence. Squirrels with historical and current rattlesnake co‐occurrence all applied rattlesnake scent, whereas no relationship existed between weasel scent application and either weasel or rattlesnake co‐occurrence. This was surprising because experimental tests confirmed rattlesnake and weasel scent were both effective at masking prey odour from hunting rattlesnakes (the primary predator of squirrels). Ancestral reconstructions and fossil data suggest predator scent application in squirrels is ancient in origin, arising before co‐occurrences with rattlesnakes or weasels in response to some other, now extinct, chemosensory predator.     

Does rattling deter? The case of domestic dogs

Although the rattling of rattlesnakes (Crotalus and Sistrurus) is widely accepted as being aposematic, the hypothesis that rattling deters approach from the snake's potentially dangerous adversaries has not been well tested. In a controlled study using rattling recorded from captive rattlesnakes (C. oreganus helleri) and a variety of comparison sounds or no-sound controls, domestic dogs (Canis familiaris) showed no hesitation to approach camouflaged speakers projecting the recorded rattles. The dogs were equally likely to approach speakers projecting rattling as they were to approach speakers playing control sounds, or speakers that were silent. Furthermore, the dogs spent no less time in front of the speakers projecting the rattles than they did in front of speakers projecting control sounds or no sound. The dogs' reactions may not be representative of other species with whom rattlesnakes come into contact, but the data suggest a need for some circumspection about the role of rattling in the rattlesnake's defensive repertoire. Our results also suggest that dogs may be vulnerable to envenomation because they fail to react to the sound of rattling with avoidance.     

Feeding Experience Modifies the Assessment of Ambush Sites by the Timber Rattlesnake, a Sit-and-Wait Predator

To effectively ambush prey, sit‐and‐wait predators must locate sites where profitable prey are likely to return. One means by which predators evaluate potential ambush sites is by recognizing high‐use areas through chemical cues deposited inadvertently by their prey. However, it is unknown whether ambush predators can use chemical cues associated with past prey items in the assessment of potential ambush sites. I examined selection of ambush sites by timber rattlesnakes (Crotalus horridus) exposed to trails made from chemical extracts of the integument of various prey species. I evaluated the role of feeding experience in ambush site selection by comparing the behavior of timber rattlesnakes before and after feeding experience with different sized prey items. Timber rattlesnakes are more likely to select ambush sites adjacent to chemical trails from prey with which they have had feeding experience, but only those fed relatively large prey showed an increase in responsiveness. Increased responsiveness after feeding experience was exhibited in experiments using integumentary extracts of mammals (the natural prey of timber rattlesnakes), but not in those using extracts of fish. These results indicate that ambush predators may learn to recognize chemicals on the integument of profitable food items, and use that experience when subsequently selecting ambush sites. Additionally, these findings provide evidence that size‐dependent predation by snakes may be, in some species, a result of active prey selection.     

Snake venom dipeptidyl peptidase IV: taxonomic distribution and quantitative variation

The present study examined the taxonomic distribution of dipeptidyl peptidase IV (DPP IV) activity in venoms of 59 ophidian taxa, representing seven subfamilies of the Families Elapidae and Viperidae. DPP IV activity is extremely variable at all taxonomic levels. It ranged from essentially none in laticaudine, hydrophiine, and some bungarine and elapine venoms, to 10.72 μmol 4-methoxy-β-naphthylamine liberated per min per 200 μg venom, for Ophiophagus hannah. Intra- and interpopulational variation were examined among eight populations of prairie rattlesnakes (Crotalus viridis viridis), Great Basin rattlesnakes (Crotalus viridis lutosus) and southern Pacific rattlesnakes (Crotalus viridis helleri). Among these populations, the mean weighted range of variation was 4.9-fold, and even among litter mates of C. v. lutosus, DPP IV activity varied as much as 5.6-fold. The two most salient findings, the near ubiquity of DPP IV in snake venoms and its great quantitative variability, even among full siblings, are paradoxical. The widespread distribution of the enzyme suggests an important role in envenomation, while the variable activity levels suggest that DPP IV and by extension, other individual enzymatic constituents, may not be under much individual selective pressure.     

Public information for solitary foragers: timber rattlesnakes use conspecific chemical cues to select ambush sites

Many animals use public information (PI) gathered from conspecificsto assess the quality of potential foraging locations. To date,research on this phenomenon has focused almost exclusively onsocial foragers that live in groups and monitor nearby individuals.PI is potentially available to solitary foragers as well, inthe form of cues (such as chemical cues) that persist in theenvironment after conspecifics are no longer present. In thisstudy, I examined the response of a solitary sit-and-wait predator,the timber rattlesnake (Crotalus horridus), to chemical cuesfrom conspecifics that had recently fed as opposed to thosethat had been deprived of food. Experiments with a T-maze indicatedthat timber rattlesnakes always follow conspecific chemicaltrails out of the maze, regardless of whether or not the individualleaving the trail had recently fed. However, an enclosure choicetest found that individuals are more likely to select ambushsites in areas with chemical cues from conspecifics that hadrecently fed. These results indicate that snakes may use conspecificchemical cues not only to find mates, shelter sites, and hibernaculabut also profitable food patches. Additionally, this study highlightsthe possibility that other solitary foragers may use PI to guidetheir foraging behavior.     

Evidence for Scavenging Behavior in the Western Diamondback Rattlesnake (Crotalus atrox)

The use of dead and decaying animals for food appears often as an adaptive strategy in birds and mammals but is apparently rare within the reptiles. Scanty evidence exists for the utilization of such a scavenging strategy by rattlesnakes but convincing data gathered under properly controlled circumstances in this regard have not been forthcoming. Western diamondback rattlesnakes (Crotalus atrox) were cage and arena tested for putrescent mouse preference and putrescent mouse location ability. Adults and neonates readily accepted mice that had been aged up to 48 h while black rat snakes (Elaphe obsoleta) failed to accept putrescent mice and would accept fresh-killed rodents only if the latter were moving. Adult rattlesnakes could locate putrescent mice buried in gravel but failed to find fresh-killed animals. The results were used to document strong evidence for a scavenging feeding strategy for this species and perhaps for the viperids as a whole.     

Rattlesnakes Create a Context for Localizing Their Search for Potential Prey

This paper presents systematically collected field data on what transpires between free-living rattlesnakes (Crotalus viridis oreganus) and individuals of an important prey species, California ground squirrels (Spermophilus beecheyi). In the course of two field seasons we discovered that rattlesnakes and California ground squirrels can engage in at least six different episode classes: snake watching, snake following, inspecting/probing coiled snakes, interaction, rattlesnake approaching squirrel and envenomation. If a rattlesnake is moving directly toward a squirrel and is within 3 m of its burrow an interaction may develop, but more commonly it does not. Instead of engaging the snake, the squirrels seemed to try to remain stationary in the face of the snake's advance, as if to minimize affording the snake information about the nursery burrow location. The rattlesnakes in turn behaved as though they were using the location of the squirrels that resisted moving away from their advance as the hub of a radial search pattern. We argue that if the squirrel engages the snake before it discovers the burrow, the location of the nursery burrow may be revealed and the pups' vulnerability actually increased.     

Integrating individual behaviour and landscape genetics: the population structure of timber rattlesnake hibernacula

Individuals of many species show high levels of fidelity to natal populations, often due to reliance on patchily distributed habitat features. In many of these species, the negative impacts of inbreeding are mitigated through specialized behaviours such as seasonal mating dispersal. Quantifying population structure for species with these characteristics can potentially elucidate social and environmental factors that interact to affect mating behaviour and population connectivity. In the northern part of their range, timber rattlesnakes are communal hibernators with high natal philopatry. Individuals generally recruit to the same hibernaculum as their mother and remain faithful to that hibernaculum throughout their lives. We examined the genetic structure of Crotalus horridus hibernacula in the northeastern USA using microsatellite loci. Sampled hibernacula exhibited only modest levels of differentiation, indicating a significant level of gene flow among them. We found no significant correlation between genetic differentiation and geographical distance, but did find significant positive correlation between genetic differentiation and a cost-based distance metric adjusted to include the amount of potential basking habitat between hibernacula. Therefore, thermoregulation sites may increase gene flow by increasing the potential for contact among individuals from different populations. Parentage analyses confirmed high levels of philopatry of both sexes to their maternal hibernaculum; however, approximately one-third of paternity assignments involved individuals between hibernacula, confirming that gene flow among hibernacula occurs largely through seasonal male mating dispersal. Our results underscore the importance of integrating individual-level behaviours and landscape features with studies of fine-scale population genetics in species with high fidelity to patchily distributed habitats.     

Donning your enemy's cloak: ground squirrels exploit rattlesnake scent to reduce predation risk

Ground squirrels (Spermophilus spp.) have evolved a battery of defences against the rattlesnakes (Crotalus spp.) that have preyed on them for millions of years. The distinctive behavioural reactions by these squirrels to rattlesnakes have recently been shown to include self-application of rattlesnake scent-squirrels apply scent by vigorously licking their fur after chewing on shed rattlesnake skins. Here, we present evidence that this behaviour is a novel antipredator defence founded on exploitation of a foreign scent. We tested three functional hypotheses for snake scent application--antipredator, conspecific deterrence and ectoparasite defence--by examining reactions to rattlesnake scent by rattlesnakes, ground squirrels and ectoparasites (fleas). Rattlesnakes were more attracted to ground squirrel scent than to ground squirrel scent mixed with rattlesnake scent or rattlesnake scent alone. However, ground squirrel behaviour and flea host choice were not affected by rattlesnake scent. Thus, ground squirrels can reduce the risk of rattlesnake predation by applying rattlesnake scent to their bodies, potentially as a form of olfactory camouflage. Opportunistic exploitation of heterospecific scents may be widespread; many species self-apply foreign odours, but few such cases have been demonstrated to serve in antipredator defence.     

Perceptions and Attitudes of Urucum Settlement Residents about Local Wildlife

This study aimed to evaluate perceptions and attitudes of local people about wild fauna and was carried out in the Urucum settlement, in the Brazilian Pantanal. We sought to: (1) identify which species of wild animals were most frequently chosen by residents of the Urucum settlement based on their familiarity; (2) identify the values associated with this fauna and the implications for conservation; and (3) test the effect of gender, age, and level of education of the residents on their attitudes. We used a structured questionnaire with open and closed questions to interview the residents. Distributions of responses about perceptions were analyzed using the chi-square test, and differences between the values associated with each species were analyzed using the Kruskal-Wallis test. The effect of gender, age, and level of education on attitudes toward the most chosen species was tested using generalized linear models (GLM). Among 61 residents interviewed, we found that the nine-banded armadillo (Dasypus novemcinctus), toucan (Ramphastos toco), monk parakeet (Myiopsitta monachus), rhea (Rhea Americana), and rattlesnake (Crotalus durissus) were the most frequently chosen species. These species were followed by tropical freshwater fish (a fish of the genus Astyanax sp.) and the blue morpho butterfly (Morpho sp.), both chosen with equal frequency. Most perceptions and attitudes were positive apart from those for the rattlesnake. Attitudes toward the rattlesnake were associated with the age of respondents, and the most common value associated with conserving the selected animals was “Anthropocentric.” As demonstrated by other studies, contact with environmental education activities could help to promote tolerance to rattlesnakes. Likewise, this tool can also broaden our understanding of the ecological importance of wild species, facilitating their conservation.     

Phylogeographic patterns of trans-Amazonian vicariants and Amazonian biogeography: the Neotropical rattlesnake (Crotalus durissus complex) as an example

Aim To investigate the phylogeography and execute a historical‐demographic analysis of the Neotropical rattlesnake, Crotalus durissus, thereby testing the hypothesis of a Pleistocene central Amazon corridor of dry forest or savanna that partitioned the Amazonian rain forest into western and eastern portions. Location South America. Methods Using sequences of three mitochondrial genes, we estimated the phylogeography, gene and nucleotide diversity across the South American range of C. durissus. Tree topology tests were used to test alternative biogeographical hypotheses, and tests of population genetic structure and statistical parsimony networks and nested clade phylogeographic analysis (NCPA) were used to infer connectivity and historical population processes on both sides of the Amazon basin. Results Tree topology tests rejected the hypothesis of a coastal dispersal in favour of a central corridor scenario. Gene diversity was similar on both sides of the Amazon basin. Nucleotide diversity indicated that the populations from north of the Amazon basin represented ancestral populations. Analysis of molecular variance (amova ) showed that intra‐population molecular variation was greater than between regions. Historical‐demographic statistics showed significant population expansion south of the Amazon, and little differentiation in the north, indicating moderate past gene flow between north and south of the Amazon. The parsimony network connected clades from the Roraima and Guyana populations with Mato Grosso, suggesting an Amazonian central corridor, and NCPA supported allopatric fragmentation between north and south of the Amazon. Main conclusions The distribution of C. durissus on both sides of the Amazon basin is evidence of changes in the distribution of rain forest vegetation during the Pleistocene. Our results suggest a formerly continuous distribution of this rattlesnake along a central Amazonian corridor during the middle Pleistocene. Allopatric fragmentation inferred from NCPA is consistent with vicariance resulting from a subsequent closure of this habitat corridor. This study emphasizes the potential of trans‐Amazonian open formation species to inform the debate on the past distribution of rain forests in the Amazon Basin.