Charles W. Radcliffe

Analysis of the behavioral sequence emitted by rattlesnakes during feeding episodes: I. Striking and chemosensory searching

Rattlesnakes exhibited an elevated rate of tongue flicking after striking a mouse. This chemosensory searching process probably aids the snake in locating its dead or dying prey when movement cues are no longer produced. Seeing, smelling, and detecting thermal cues arising from a live mouse were not sufficient to produce the increase in the tongue-flick rate; the mouse must be struck. After striking a mouse, rattlesnakes also showed some degree of inhibition against striking a second mouse for as long as 20 min. Hence, “switching on” the chemosensory searching process involves “switching off” (at least partially) the striking system.

Strike-Induced Chemosensory Searching by Rattlesnakes: The Role of Envenomation-Related Chemical Cues in the Post-Strike Environment

Rattlesnakes and many other viperids typically strike and release adult rodent prey (Gans, 1966; O’Connell et al., 1982; Radcliffe et al., 1980), allowing the envenomated rodent to wander up to 600 cm before succumbing to the venom (Estep et al., 1981). The snakes then follow the chemical trail left by the envenomated prey. Although this predatory strategy risks losing the prey, it avoids tissue damage that could result from rodent teeth and claws if the snake attempted to hold the struggling prey after the strike. Even some of the deadliest elapids exhibit this strategy when they prey upon rodents (Chiszar et al., under review; Radcliffe et al., 1982; Shine & Covacevich, 1982), indicating that rodents are formidable prey and that the strike-release-trail system probably appeared very early in the evolution of venomous snakes (see Marx & Rabb, 1965, for a discussion of viperid evolution).

Effects of Chemical and Visual Stimuli Upon Chemosensory Searching by Garter Snakes and Rattlesnakes

Many studies indicate that chemical cues activate garter snake feeding behavior whereas visual and/or thermal stimuli do so for rattlesnakes. However, no experiments have factorially combined chemical and visual cues for either of these taxa. The present work explored possible interactive effects of these stimuli on rate of tongue flicking (RTF) in garter snakes (Thamnophis radix haydeni) and rattlesnakes (Crotalus e. enyo, C. v. viridis, and Sistrurus catenatus tergeminus). In Experiments 1 and 2 snakes were exposed to four conditions represent- ing an orthogonal combination of presence vs. absence of visual and chemical stimuli arising from prey. RTF was recorded for 5 min under each condition. Garter snakes exhibited a significant elevation in RTF in the presence of chemical cues whether or not visual cues were present. There was also an effect of visual cues but no interaction between visual and chemical cues. Rattlesnakes did not respond to chemical cues; these snakes showed only an effect of visual cues. In Experiment 3, rattlesnakes were again observed as above, with the exception that test sessions were of 10 min duration. Behavior during the first 5 min was identical to that seen in Experiment 2, but during min 6-10 the snakes responded more in the condition containing visual plus chemical cues than in any other condition. Visual stimuli alerted rattlesnakes to the presence of potential prey and gave rise to elevated RTF which subsequently allowed these predators to utilize chemical cues that happened to be available. Hence, garter snakes and rattlesnakes use both chemical and visual information but differ in the sequence in which these stimuli are used.

Trailing Behavior in Prairie Rattlesnakes (Crotalus viridis)

Six rattlesnakes (Crotalus v. viridis) were observed in four experimental conditions designed to assess ability to follow odoriferous mouse trails. If snakes had not struck mice just prior to being exposed to the trails, then no trailing behavior was observed, whereas trails were followed with precision if the snakes struck mice prior to the tests. Striking led to pronounced elevations in rate of tongue flicking, and the magnitude of this effect did not depend upon presence vs absence of mouse trails in the post-strike environment. However, when a trail was present, the high rate of tongue flicking facilitated locating the trail and following it to the mouse carcass positioned at its end. Once a trail was located, the snake confined its head to within 2 cm of the odoriferous cues, and 75% of the tongue flicks were directed to the trail.

Chemical cues used by prairie rattlesnakes (Crotalus viridis) to follow trails of rodent prey

Each of 10 prairie rattlesnakes (Crotalus viridis) was exposed to three types of trails after striking rodent prey (Mus musculus). One trail was made with mouse urine, another was made with tap water, and the third consisted of materials from mouse integument. The snakes exhibited trailing behavior only when integumentary trails were available. It was concluded that prairie rattlesnakes do not utilize urinary cues; instead they attend to materials associated with rodent skin and fur.

Strike-induced chemosensory searching in Old World vipers and New World pit vipers

It is known that striking rodent prey induces a sustained, high rate of tongue flicking in rattlesnakes. The present study shows this phenomenon (called strike-induced chemosensory searching, SICS) to occur in species of rattlesnakes not previously investigated and in two species ofAgkistrodon. SICS occurs in Old World vipers (Eristocophis, Vipera, Bitis), including species which normally hold their prey after striking. A hypothesis is offered which (1) accounts for the occurrence of SICS in these latter species and (2) suggests that SICS in some viperids may have arisen through paedomorphic evolution. More generally, it is concluded that SICS is probably a homologous trait in vipers and pit vipers and that the trait may have first appeared in elapid ancestors of the viperidae.

Effects of prey size on poststrike behavior in rattlesnakes (Crotalus durissus, C. enyo, and C. viridis)

Rattlesnakes of three taxa (Crotalus durissus, C. enyo, and C. viridis) struck and released large rodent prey but held smaller rodents in their jaws after striking. The specimens of C. enyo were clearest in this regard; almost all large prey were released, and all small prey were held. This finding is consistent with the fact that large rodents are more dangerous to rattlesnakes than are small rodents. Accordingly, it appears that rattlesnakes have evolved differential predatory strategies for dealing with prey of varying size. Speculation is offered about the manner in which these respective strategies are activated or selected during predatory episodes.

Preference for envenomated rodent prey by rattlesnakes

Adult specimens of several rattlesnake species which struck and envenomated a mouse or which did not have an opportunity to strike were allowed to choose between an envenomated mouse and one manually killed by the experimenter. Only rattlesnakes that struck a mouse made a choice, and the envenomated mouse was selected most frequently. Odor cues emanating from the envenomated mouse and/or remembrance of taste or odor cues briefly experienced during the strike probably mediated eventual selection of the envenomated mouse, and may represent important components of the stimulus configuration releasing swallowing once dead prey are located.

Distance traveled by mice after envenomation by a rattlesnake (C. viridis)

Adult mice (Mus musculus, C3H) envenomated by adult prairie rattlesnakes (Crotalus viridis) traveled an average of 185.6 cm in an open field prior to becoming immobilized (78 sec). The range of distances traveled by the 20 envenomated mice in this study was 0-676.5 cm. These distances give an indication of the extent of the trailing task that confronts a prairie rattlesnake under natural conditions. Hence, laboratory studies of trailing behavior in rattle-snakes should use trails of at least 180-200 cm if results are to have ecological validity. Of course, data from additional strains of rodents envenomated by additional species of rattlesnakes should be accumulated in order to supplement the information provided here.

Rate of tongue flicking by rattlesnakes during successive stages of feeding on rodent prey

Specimens of each of three species of rattlesnakes (Crotalus enyo enyo, C. durissus culminatus, and Crotalus vegrandis) exhibited no tongue flicking prior to striking live mice during a regular feeding session. All snakes flicked their tongues at high rates (more than 20 flicks/minute) between striking and commencement of swallowing. Also, frequent tongue flicking (10 to 15 flicks/minute) was seen for about 15 min after swallowing. These data indicate that well-acclimated, captive rattlesnakes do not rely upon the Jacobson’s organ to detect prey or to guide the predatory attack, but that they do use this sensory system to locate prey after striking. Since an envenomated rodent may wander several meters prior to dying, Jacobson’s organ may be very important in finding such prey. It is also of interest that renewed tongue flicking occurs after swallowing. A hypothesis is offered concerning the role of the latter behavior.