Envenomated Prey Research Articles

Foraging and scavenging behaviour of the prairie rattlesnake (Crotalus viridis): no evidence that envenomation cues facilitate kleptoparasitism of struck prey

Abstract Most viperids are ambush predators that primarily use venom to subdue prey, employing a strike-release-trail hunting strategy whereby snakes follow the unique scent of envenomated prey to locate carcasses they have bitten and released. In addition to killing prey, rattlesnakes (like most carnivores) will also opportunistically scavenge carrion. This scavenging strategy likely includes the occasional consumption of carcasses killed by other snakes (i.e., kleptoparasitism). In areas with high densities of other pitvipers, utilizing the unique scent of animals envenomated by other snakes might be a viable alternative foraging strategy. We evaluated this possibility experimentally using a series of captive behavioural trials on prairie rattlesnakes (Crotalus viridis) to determine whether conspecific or heterospecific (C. scutulatus, C. ornatus) envenomation cues might increase the likelihood of kleptoparasitism. Rattlesnakes did not prefer envenomated prey over nonenvenomated prey, nor did they prefer venom cues of one species over another. Although they did frequently scavenge carcasses, in the absence of striking, snakes generally located carcasses using random searching movements instead of scent trails. Additionally, the amount of time rattlesnakes spent investigating carcass trails did not differ significantly among treatments, suggesting that striking, and the resultant formation of a chemical search image of prey, is more crucial to trailing behaviour than venom cues. Moreover, a high degree of behavioural variation among individuals was observed, suggesting that scavenging and kleptoparasitism in rattlesnakes is more complex than previously realized, and making generalizations about these behaviours is challenging.

Observations on the chemosensory responses of the midget faded rattlesnake (Crotalus oreganus concolor): discrimination of envenomated prey in a type II venom species

Rattlesnakes use prey chemical cues for ambush site selection and for relocating envenomated (E) prey following a predatory strike. The ability to discriminate between E and non-envenomated (NE) prey cues has been widely studied in rattlesnake species that produce type I venoms, which show high levels of snake venom metalloproteinase (SVMP) activity and low lethal toxicity [lethal dose which kills 50% of test animals (LD50) >1.0 µg/g]. However, E vs. NE prey discrimination studies have not been conducted on rattlesnake species that produce a type II venom that consists of low SVMP activity and high lethal toxicity (LD50 <1.0 µg/g). In the current study, long-term captive Crotalus oreganus concolor, which produce a type II venom, were tested for their ability to discriminate between chemical cues of natural (Sceloporus undulatus and Peromyscus maniculatus) and non-natural (Hemidactylus frenatus and Mus musculus) prey cues, as well as for their ability to discriminate between E and NE mouse carcasses, when prey envenomation occurred by a conspecific. Snakes showed significant levels of tongue flicking towards the chemical extracts of P. maniculatus and M. musculus, suggesting that C. oreganus concolor exhibit both innate and experience-based plasticity in response to prey chemical cues. In addition, C. oreganus concolor were able to discriminate between E and NE prey sources, when envenomation occurred by a conspecific, indicating that a type II venomous species can also discriminate between E and NE chemical cues.

Chemosensory response in stunted prairie rattlesnakes Crotalus viridis viridis

Abstract Rattlesnakes use chemical stimuli in ambush site selection and for relocation of envenomated prey through strike-induced chemosensory searching. Shifts in responsiveness to prey chemicals have been documented in many snakes, and often correlate with prey commonly taken as snakes increase in age and size as well as geographical locations of the species. For instance, neonate rattlesnakes that prey primarily on ectotherms responded most strongly to chemical cues of commonly taken lizard prey, whereas adult rattlesnakes that prey primarily on small mammals responded significantly to chemical cues of commonly taken rodents. In the current study, 11 Prairie Rattlesnakes Crotalus viridis viridis which were classified as large neonates based on measures of snout-vent length (SVL) and body mass, yet chronologically were at or near adulthood, were tested for their responsiveness to chemical extracts of natural and non-natural prey items. Although the snakes had eaten only neonate lab mice (Mus musculus), they responded significantly more to chemical cues of natural prey items and particularly to chemical cues of prey normally taken by subadults (Peromyscus mice and Sceloporus lizard). These results suggest that ontogenetic shifts in responsiveness to natural prey chemical cues are innately programmed and are not based on body size or feeding experience in C. v. viridis. This does not imply, however, that growth and experience are without effects, especially with novel prey or rare prey that have experienced recent population expansion.

Molecular basis for prey relocation in viperid snakes.

BackgroundVertebrate predators use a broad arsenal of behaviors and weaponry for overcoming fractious and potentially dangerous prey. A unique array of predatory strategies occur among snakes, ranging from mechanical modes of constriction and jaw-holding in non-venomous snakes, to a chemical means, venom, for quickly dispatching prey. However, even among venomous snakes, different prey handling strategies are utilized, varying from the strike-and-hold behaviors exhibited by highly toxic elapid snakes to the rapid strike-and-release envenomation seen in viperid snakes. For vipers, this mode of envenomation represents a minimal risk predatory strategy by permitting little contact with or retaliation from prey, but it adds the additional task of relocating envenomated prey which has wandered from the attack site. This task is further confounded by trails of other unstruck conspecific or heterospecific prey. Despite decades of behavioral study, researchers still do not know the molecular mechanism which allows for prey relocation.ResultsDuring behavioral discrimination trials (vomeronasal responsiveness) to euthanized mice injected with size-fractionated venom, Crotalus atrox responded significantly to only one protein peak. Assays for enzymes common in rattlesnake venoms, such as exonuclease, L-amino acid oxidase, metalloproteinase, thrombin-like and kallikrein-like serine proteases and phospholipase A2, showed that vomeronasal responsiveness was not dependent on enzymatic activity. Using mass spectrometry and N-terminal sequencing, we identified the proteins responsible for envenomated prey discrimination as the non-enzymatic disintegrins crotatroxin 1 and 2. Our results demonstrate a novel and critical biological role for venom disintegrins far beyond their well-established role in disruption of cell-cell and cell-extracellular matrix interactions.ConclusionsThese findings reveal the evolutionary significance of free disintegrins in venoms as the molecular mechanism in vipers allowing for effective relocation of envenomated prey. The presence of free disintegrins in turn has led to evolution of a major behavioral adaptation (strike-and-release), characteristic of only rattlesnakes and other vipers, which exploits and refines the efficiency of a pre-existing chemical means of predation and a highly sensitive olfaction system. This system of a predator chemically tagging prey represents a novel trend in the coevolution of predator-prey relationships.

Spider-Venom Peptides: Structure, Pharmacology, and Potential for Control of Insect Pests

Spider venoms are an incredibly rich source of disulfide-rich insecticidal peptides that have been tuned over millions of years to target a wide range of receptors and ion channels in the insect nervous system. These peptides can act individually, or as part of larger toxin cabals, to rapidly immobilize envenomated prey owing to their debilitating effects on nervous system function. Most of these peptides contain a unique arrangement of disulfide bonds that provides them with extreme resistance to proteases. As a result, these peptides are highly stable in the insect gut and hemolymph and many of them are orally active. Thus, spider-venom peptides can be used as stand-alone bioinsecticides, or transgenes encoding these peptides can be used to engineer insect-resistant crops or enhanced entomopathogens. We critically review the potential of spider-venom peptides to control insect pests and highlight their advantages and disadvantages compared with conventional chemical insecticides.

INFLUENCE OF PREY ODOR CONCENTRATION ON THE POSTSTRIKE TRAILING BEHAVIOR OF THE NORTHERN PACIFIC RATTLESNAKE

Rattlesnake predatory behavior is defined by a strike and then release of rodent prey. Poststrike, the released envenomated prey dashes off and dies. Therefore, the snake must relocate the prey relying largely upon chemosensory cues emitted by the struck prey. Assessing these poststrike chemosensory cues is important to the snake as these cues may contain significant information about the effectiveness of the preceding strike and hence the likelihood that trailing the odor left by the envenomated prey will allow successful recovery of the prey. One possible cue in this scent trail is concentration of the distinctive odor generated in the prey during envenomation. To test this, we presented snakes with different poststrike choices of low and high prey-odor concentrations. We found that although rattlesnakes could trail each concentration level, they preferred the high odor concentrations. These results imply that rattlesnakes respond to concentration levels, not just to a threshold level of prey odor. This adjustment to different odor concentrations is not accomplished by varying rate of tongue flicks (RTFs). Based on this study and previous work, we propose a behavioral mechanism by which rattlesnakes assess the chemosensory quality of a poststrike prey odor trail.

The influence of prey-scent stimuli on predatory behavior of the North American copperhead Agkistrodon contortrix (Serpentes: Viperidae)

Viperid snakes strike, envenomate, and release mammalian prey to prevent being harmed by the prey; snakes must then track prey in the process of strike-induced chemosensory searching. Because rattlesnakes prefer to track and consume envenomated prey, it would seem that the scent of envenomated tissue is key to the tracking process. After striking rodents, rattlesnakes also retain a specific chemical search image of prey items. I examined this behavioral pattern in copperheads (Agkistrodon contortrix) from three US populations with documented dietary biases toward mammals (Kansas), lepidopteran larvae (Texas), and amphibians (Louisiana), respectively. Experiments were conducted to assess whether copperheads form a specific search image of nonenvenomated mouse, hornworm, and frog prey items. Additional experiments tested the relative importance of envenomated tissue to prey scent. Results indicate that copperheads do not form a specific search image of prey items. Preference for nonenvenomated prey items is in the order mouse . hornworm . frog for all three populations; therefore, the innate behavioral preference for types of prey does not match the dietary biases noted in the literature. Envenomated mice and hornworms were preferred to all nonenvenomated prey items, but most trials involving envenomated frogs did not suggest envenomated prey preference. Overall, these results suggest that when the snakes search for prey, envenomated tissue stimuli are more important to snakes than scents arising from the prey itself. Searching and consumption behaviors seem to be independent, suggesting that strike-induced chemosensory searching and consumption are more complicated behavioral processes than previously recognized.

Venom variation and chemoreception of the viperid Agkistrodon contortrix: evidence for adaptation?

Previous studies of chemoreceptive behavior in vipers suggest that snakes focus on the scent of envenomated tissue to track their prey following envenomation. Other studies have indicated a correlation between qualitative differences in venom biochemistry and geographic variation in diet. The North American copperhead (Agkistrodon contortrix) varies geographically in diet and venom biochemistry; snakes were collected from three populations (Kansas, Texas, and Louisiana) that are known to have different prey preferences. Behavioral experiments were conducted to assess whether copperheads preferred envenomated prey more than nonenvenomated prey, as do other species of vipers studied thus far. Additional experiments tested the ability of copperheads to distinguish between envenomated prey from different geographic populations, and between geographic populations of copperheads and two other species of viper. Results indicated that copperheads prefer envenomated prey to nonenvenomated prey. In envenomated-prey discrimination experiments, copperheads distinguished between envenomated prey from different geographic populations, and some snakes distinguished envenomated prey of A. contortrix from those of A. piscivorns and Sistrurus catenatus. Sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) was used to study the variation of venom biochemistry in this species and two other taxa (A. piscivorus and S. catenatus), and confirmed intraspecific and interspecific variation of venom proteins. Relative potency of the venom from different populations as indicated by time to immobilization experiments was in the order: Louisiana > Texas > Kansas. The relative potency of the venom from each population matched the order of preference in the chemoreception experiments. These results suggest that chemoreception is sensitive to subtle differences in venom biochemistry and may reflect adaptation to improve efficiency of finding envenomated prey.

PERSISTENCE OF TRAILING BEHAVIOR: CUES INVOLVED IN POSTSTRIKE BEHAVIOR BY THE RATTLESNAKE (CROTALUS VIRIDIS OREGANUS)

Following the release of envenomated prey, a rattlesnake exhibits a series of poststrike behaviors, involving largely chemosensory cues that lead to recovery and swallowing of the dead prey. Unlike prestrike chemosensory activity that may help the snake place itself generally in the vicinity of prey, this poststrike trailing is more specific and selective. The rattlesnake discriminates the particular poststrike trail of the envenomated mouse from odor trails of other unstruck mice. But an envenomated prey may dash significant distances over complicated terrain. Consequently, poststrike trailing by the rattlesnake may take hours during which it is exposed to its own predators. If the odor trail ages significantly, losing its perceptibility, then poststrike trailing eventually becomes futile. To examine this, each rattlesnake was permitted to strike prey, but allowed to follow the placed scent trails only at six fixed intervals poststrike, t = 0, 2, 4, 6, 12, and 24 hours. Our results indicate that in the absence of an envenomating strike, rattlesnakes did not exhibit successful trailing of prey odors, whether those scent trails were from an unstruck mouse or a mouse struck independently by another snake. However, allowed to strike, snakes maintained an interest in selective trailing up to 24 hours from the time of envenomation, although with decreasing frequency. Therefore, the strike must precede the specific and selective poststrike trailing behavior, characterized by an ability to discriminate and track the scent of the particular mouse envenomated. These results imply that the strike itself is a releaser of selective chemosensory trailing and that snakes can retain for extended periods of time a 'memory′ of the unique chemical cues of the particular mouse struck.

Discrimination between Envenomated and Nonenvenomated Prey by Western Diamondback Rattlesnakes (Crotalus atrox): Chemosensory Consequences of Venom

Snake venoms have multiple consequences on prey, ranging from immobilizing and digestive effects to enhancing the salience of envenomated prey and their chemical trails. Although the toxic and lytic effects are reasonably well understood, the chemosensory effects have been little studied. Experiment 1 showed that western diamondback rattlesnakes (Crotalus atrox) preferred envenomated (E) over nonenvenomated (NE) prey in a standardized choice situation, as other species have done in previous studies. In Experiment 2, E prey were prepared by injecting reconstituted lyophilized venom, so that dosage could be controlled, something not possible when snakes envenomated prey as in Experiment 1 and in most previous studies of rattlesnake response to E and NE prey. Prey injected with 10 mg of lyophilized venom were reliably discriminated from NE prey by C. atrox. A dose-response curve was established in Experiment 3 to assess the lowest dose to produce E prey that were preferred over NE prey. Two statistical techniques were used to estimate minimum perceptible dose (MPD), giving values of 6.0 and 7.1 mg, respectively. These values were compared with the amount of venom snakes actually injected during predatory strikes and with various measures of lethality. Chemosensory effects of venom probably facilitate rattlesnake predatory behavior in that adult rodents are usually released after envenomation, requiring that the snake follow the prey's trail to recover the carcass. This trail-following task depends upon the snake's ability to discriminate trails of E prey from those deposited in the vicinity by other (NE) rodents as they engaged in foraging activities.

Post-prandial chemosensory searching in black rat snakes

In a laboratory experiment, black rat snakes, Elaphe o. obsoleta, increased rates of tongue flicking following ingestion of prey. This post-prandial tongue-flick increase, in combination with searching behaviour, represented post-prandial chemosensory searching (PPCS). Such chemosensory searching enabled rat snakes to locate subsequent prey more quickly than initial prey, which may prove beneficial in the wild. Single snakes of five other colubrid species also showed post-prandial tongue flick increases in similar experiments. Field observations are described that support inferences drawn from experimental results. Strike-induced chemosensory searching (SICS) is well known in venomous snakes, and was thought to have evolved as an adaptation for chemically trailing envenomated prey after voluntary release. This study adds to a growing list of non-venomous squamates that appear to show SICS, suggesting that the trait may instead be widespread and ancestral. The data are consistent with the view that SICS arose in a snake–lizard ancestor and may now serve different functions in different lineages. The emerging scenario for the evolution of chemosensory searching is a complex mix of adaptation and exaptation, underscoring the need to distinguish historical origin from current utility in the study of behavioural traits.

The role of the vomeronasal organ in rattlesnake (Crotalus viridis oreganus) predatory behavior.

During predatory behavior, rattlesnakes depend primarily upon thermal and visual cues to initially aim a strike. However, it has been hypothesized that prey-related odors sensed by the vomeronasal system act as releasing stimuli of the strike and that such vomodors are primary stimuli during poststrike trailing and swallowing of the envenomated rodent. To test this, northern Pacific rattlesnakes were rendered avomic by bilateral lesions of the vomeronasal nerves, and their vomic and avomic predatory behaviors were compared. Avomic rattlesnakes exhibited fewer strikes and complete elimination of trailing and swallowing behavior. These results support the hypothesis that vomodors sensed via the vomeronasal organ are capable of acting as releasing stimuli of selected rattlesnake predatory behaviors. Sensory input via the vomeronasal organ is important during prestrike/strike behavior, and it is a major route of sensory input during poststrike trailing and ingestion of envenomated prey.

Post-strike orientation of the prairie rattlesnake facilitates location of envenomated prey

Prairie rattlesnakes (Crotalus viridis) typically release adult rodent prey after envenomation. The post-strike head orientation of the snake may facilitate location of the trail left by the rodent. To examine this possibility, mice were presented using a pair of tongs so that no chemical cues were deposited on any surfaces. Snakes exhibited a change in head orientation after predatory strikes, bringing them closer to the departure bearing of the prey. In addition, when trail searching began snakes contacted the departure bearing of the prey first rather than the entry bearing. When rodent trails are available, we expect this initial contact to bias the snake towards selecting the post-envenomation trail.

Strike‐induced chemosensory searching in old world vipers and new world pit vipers at San Diego Zoo

AbstractRattlesnakes (Crotalus unicolor, C vegrandis) and Russell's vipers (Vipera russelli) at San Diego Zoo exhibited sustained high rates of tongue flicking after striking mice (Mus musculus) but not after seeing, smelling, and/or detecting thermal cues arising from mice. Called strike‐induced chemosensory searching (SICS), this phenomenon contributes to poststrike trailing of envenomated prey. Because these zoo‐raised snakes had always been offered dead rodents, and because these prey were usually ingested without first being struck, the present snakes had rarely exercised their innate predatory repertoire (ie, ambush tactics including striking, releasing, and trailing). Indeed, most specimens had never before struck a mouse and, hence, had never exhibited SICS. The occurrence of SICS in the present study clearly indicates that this important aspect of the predatory repertoire had not been degraded as a consequence of long‐term captive husbandry.

Strike-Induced Chemosensory Searching in Rattlesnakes (Crotalus Viridis) as a Function of Disturbance Prior to Presentation of Rodent Prey

Prairie rattlesnakes (Crotalus viridis) exhibited higher rates of tongue flicking after striking and envenomating a mouse than after seeing, smelling, or detecting the warmth of a mouse. Thus, as in several previous studies, chemosensory searching subserved by the vomeronasal system was activated consequent to the delivery of a successful predatory strike. This effect, however, was not observed when the snakes were disturbed (by handling or transportation to a new environment) just prior to being exposed to mice. The same kinds of disturbance did not interfere with strike-induced chemosensory searching in specimens of C. enyo, which are characteristically less likely than C. viridis to exhibit ritualized defensive patterns (Rdps) consequent to disturbance. Thus, for C. enyo the predatory reaction chain appears to be immune or closed to at least some disturbing influences and runs to completion once initiated by a strike. For C. viridis, on the other hand, the chain is vulnerable to interference, probably because cues which elicit Rdps receive attentional priority. It is now interesting to ask if C. viridis eventually will exhibit chemosensory searching after the Rdps subside (usually 10-15 min are required for this); that is, do the animals have a memory system which will cause them to begin searching for the en-venomated prey after the hiatus (retention interval) created by RDPs.