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Striking prey creates a specific chemical search image in rattlesnakes
Anim.
Behav.,
1989,37,477-486
Striking prey creates a specific chemical search image in rattlesnakes Department
TED MELCER & DAVID CHISZAR of Psychology, University of Colorado, Boulder,
CO 80309, U.S.A.
Abstract. Rattlesnakes, Crotalus viridis, struck mouse carcasses misted with water or with diluted perfume. Envenomated carcasses were removed, and later the snakes were presented with a pair of nonenvenomated carcasses, each misted with one of these liquids. Snakes preferred the carcass with the same odour as the prey that was struck, even when the test occurred 60 min after the predatory strike. Under natural circumstances, rodents may acquire distinct chemical identities through their diet. In further tests, snakes preferred carcasses of mice that had been eating the same diet as the mouse that had been struck. These results indicate that rattlesnakes rapidly acquire chemical information from rodent prey during predatory strikes and use this information in subsequent search for prey.
Most species of rattlesnakes specialize upon rodent prey, exhibiting traits that capitalize upon rodent morphology, physiology and behaviour (Greene 1983; Pough & Groves 1983). For example, timber and prairie rattlesnakes wait in ambush along trails habitually used by their prey (Reinert et al. 1984; Duvall et al. 1985; Diller, in press). Also, rattlesnakes typically release adult rodents after the strike, reducing risk of injury from rodent teeth and claws (Klauber 1956; Kardong 1986). Envenomated mice die in 3-8 minutes, and snakes wait about this long before searching for them, suggesting the cadence of the predator’s behaviour has been designed to avoid contact with a rodent still capable of self defence (Estep et al. 1981; Hayes & Galusha 1984). The searching process capitalizes upon chemical cues deposited by prey as they wandered from the site of attack (Brock 1980; Golan et al. 1982; Chiszar et al. 1983a, 1986). Since many rodent trails are likely to be in the snake’s vicinity, selecting the specific trail of the envenomated prey is a crucial task confronting the predator and vipers do this with little difficulty (Baumann 1927; Wiedemann 1932; Naulleau 1965; Duvall et al. 1980; Lee & Chiszar, unpublished data; see Burghardt 1970, for a review of chemical perception in reptiles). Several mechanisms may support trail-following by rattlesnakes. For instance, chemical cues of envenomated rodents are generally attractive to a rattlesnake searching for prey even if the rodent was envenomated by another snake (Duvall et al. 1980). Also, snakes orient toward the prey as it departs from the site of attack, and the subsequent 0003-3472/89/030477
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search begins in that direction (Lee & Chiszar, unpublished data). A previously unexplored possibility is that chemical learning may occur during the strike and later guide the snake in following idiosyncratic chemical cues left by the envenomated prey. The present experiments tested the possibility that rattlesnakes acquire chemical information from prey during the brief contact (0.3 s) made while striking. EXPERIMENT
If prairie rattlesnakes develop preferences for chemical cues acquired during the predatory strike, then the snakes should select carcasses with chemical cues matching those on the envenomated prey. Consequently, rattlesnakes were permitted to strike a mouse carcass misted with either a floral perfume or with water. This carcass was discarded, and snakes then received simultaneous access to two non-envenomated carcasses scented with either water or the perfume. Since neonatal rattlesnakes without prior feeding experience are known to detect and follow chemical cues arising from envenomated mice, it is reasonable to infer an innate perceptual basis for such behaviour (Scudder, Poole, O’Connell & Chiszar, unpublished data). Consequently, to demonstrate that a learning process also contributes to carcass recovery, snakes must demonstrate an ability to use arbitrary chemical cues (not normally associated with prey) as discriminative stimuli (cf. Begun et al. 1988). This is why perfume was applied to mice. Nonenvenomated carcasses were used during the choice
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tests to eliminate any preference effects that might be associated with envenomated mice (Duvall et al. 1978, 1980). Methods
Subjects The subjects were 40 adult prairie rattlesnakes, Crotalus viridis, approximately 70 cm long. Snakes were captured as adults and maintained individually in glass terraria (50 x 27.5 x 30 cm) containing paper floor coverings and stainless steel vessels filled with water. The room was kept at 26-28°C during the photophase (0700-1900 hours) and at 22-24°C during the scotophase. All snakes had been in captivity for several years and had been accepting rodent prey (Mus musculus or preweanling Rattus norvegicus, 20-27 g) on a biweekly schedule. Previously euthanized rodents were fed to snakes, and these carcasses were always suspended into the snakes’ home cages from forceps in order to elicit predatory strikes. Consequently, snakes were accustomed to striking prior to ingesting prey. Snakes were not fed for 2 weeks prior to testing. Although the snakes had been used in previous experiments involving presentation of chemical stimuli, no surgical or pharmacological manipulations had been performed. Therefore, we consider these snakes typical of long-term captive crotalines. Procedure All snakes were observed in their home cages. First, a mouse carcass was misted with about 1 ml of either diluted perfume (2 ml of Jungle Gardenia perfume in 710 ml of tap water) or water. No live rodents were used as stimuli; they were euthanized by cervical dislocation 2 min prior to the experiment. All mice were culls from local breeding facilities and all carcasses were eventually ingested by snakes. For 20 snakes, the lid of a home cage was opened and the misted carcass was suspended from forceps 10 cm above and slightly in front of the snakes’ heads. Within a few seconds snakes oriented to these carcasses, then struck and released them. The envenomated carcass was removed immediately without making contact with any part of the home cage, and the cage lid was closed. Ten snakes struck carcasses misted with water and 10 struck carcasses misted with diluted perfume. The envenomated carcass was discarded and two non-envenomated carcasses were used for the preychoice test, one misted with the diluted perfume
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and one misted with water. Five min after the strike, the new carcasses were placed on the cage floor in dorsal recumbency, 4 cm apart and at the far end of the cage from the snake. The position of perfume- and water-misted carcasses relative to the snake’s head was counterbalanced across snakes. The carcasses remained for 20 min or until the snake ingested one of them. We recorded which carcass was first grasped and swallowed by the snake. These procedures were also applied to 20 additional rattlesnakes that received no-strike presentations of water-misted (N= 10) or perfumedmisted (N= 10) carcasses. In these tests the carcasses were suspended into the home cages but held outside of striking range for 5 s. Results and Discussion All snakes that struck a stimulus mouse carcass swallowed a non-envenomated carcass during the 20-min test, and 16 of these snakes (eight from each subgroup) ingested carcasses that were misted with the same liquid as was present on the prey previously struck (x2 = 7.2, df = 1, P < 0.05). After the no-strike trials, however, snakes either failed to feed within 20 min (N= 11) or they selected randomly among the carcasses. This finding is consistent with previous studies demonstrating that chemosensory searching and trail following occur more intensely and more effectively after predatory strikes (Duvall et al. 1980; Golan et al. 1982; Chiszar et al. 1983a). More importantly, the behaviour of snakes after no-strike presentations strongly suggests that preferences seen after strike presentations are induced, not by mere exposure to chemical cues, but rather by their detection on the prey item during envenomation. It is noteworthy that snakes exhibited equally strong though opposite preferences after they struck water- or perfume-misted carcasses, respectively. That is, snakes showed no greater post-strike preference for familiar, water-misted carcasses than for novel, perfume-misted ones. In fact, we have independent evidence that such prey items are equally acceptable to rattlesnakes as stimuli for envenomation and ingestion (Melter et al., in press). Consequently, the post-strike preferences reported here must have arisen during the strike and we suggest that they are akin to search images (Tinbergen 1960). That is, rattlesnakes acquire a strike-induced preference for specific chemical cues on the prey they have struck.
Melter EXPERIMENT
& Chiszar: Search images in rattlesnakes 2
We tested whether the strike-induced preferences observed in experiment 1 occur in other taxa of rattlesnakes that exhibit the strike-release-trail strategy described above. Thus, we repeated experiment 1 using six species of rattlesnakes other than C. viridis. Methods Subjects Twenty new adult rattlesnakes (eight C. enyo, four C. horridus, four C. adamanteus, one C. atrox, one C. ruber, two Sistrurus miliaruis) were observed. The history and housing conditions for these snakes were as described for snakes in experiment 1. Procedure The procedures were the same as in experiment 1. Ten snakes struck a water-misted carcass and 10 struck a perfume-misted carcass (same solution as in experiment 1). Where possible, half of the snakes of each species were assigned to each strike condition (water or perfume). All snakes were then permitted to choose between two non-envenomated carcasses, one misted with water and one with perfume. Since no-strike presentations did not result in biased choice behaviour in experiment 1, we did not include such tests here (Golan et al. 1982; Chiszar et al. 1983a). Results and Discussion Seventeen snakes (eight that struck water-misted prey, nine that struck perfume-misted prey) first grasped and swallowed the carcass matching the fragrance of the prey that had been struck (x2 =9.80, df= 1, P< 0.05). Thus, the post-strike preferences seen in experiment 1 also occurred in this group of rattlesnakes, all of which are rodentspecialists. Small sample sizes do not permit comparisons between the individual species, and none was made. The only conclusion we wish to offer is that the phenomenon of experiment I is probably not restricted to C. viridis.
EXPERIMENT
3
If our chemical-learning interpretation of experiments 1 and 2 is correct, then the post-strike
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performance of rattlesnakes should not depend upon the specific chemicals used in those studies (i.e. water and diluted Jungle Gardenia perfume). Therefore, experiment 3 was designed to assess post-strike performance of snakes when different chemicals were applied to mouse carcasses. Methods Subjects The subjects were 20 prairie rattlesnakes that had been tested in experiment 1. Housing and maintenance conditions were as described in experiment 1. Procedure Testing procedures were similar to those described in experiment 1. In experiment 3, snakes struck a carcass misted with either Tea Rose or Jungle Gardenia solution (N= 5 in each condition). These 10 snakes then received prey-choice tests with non-envenomated carcasses misted with Tea Rose and Jungle Gardenia, respectively. The dilution of perfumes in this experiment was the same as reported in experiment 1. An additional 10 snakes struck a carcass misted with either Tea Rose or Halston perfume (N= 5 in each condition). These snakes then received prey-choice tests with nonenvenomated carcasses misted with Tea Rose and Halston, respectively. Tea Rose and Jungle Gardenia are floral scents, whereas Halston is a musk scent. Results and Discussion Fifteen snakes (eight from the Jungle Gardenia versus Tea Rose tests; seven from the Tea Rose versus Halston tests) ingested the carcass bearing the same chemical cues as were encountered during the strike (x2 = 6.66, df= 1, P < 0.05). Thus, snakes were able to discriminate between two floral perfumes, and between a floral and musk scent. This implies that the results of experiments 1 and 2 were not dependent upon specific chemicals used (e.g. choosing between familiar and novel chemical cues). Accordingly, experiment 3 strengthens the conclusions that chemosensory learning occurred during predatory strikes and that some representation of this information was maintained until the prey-choice tests. That floral perfumes could be registered and remembered implies that ophidian chemosensation is not restricted to cues associated with natural prey, mates or enemies. Some receptor
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Animal Behaviour,
macromolecules and associated central nervous system processes must transduce, encode and retain novel chemical information (Arnold 1981; Atema & Derby 1981; Begun et al. 1988). These findings constitute the first systematic evidence of rapidly formed preferences for chemical features of prey (i.e. chemical search images; see also Chiszar et al. 198Sb). Most work on search images has concentrated on visually searching predators (following Tinbergen 1960; see also Curio 1976; Pietrewicz & Kamil 1981). Evidence exists for the development of chemical search images in pea crabs (Pinnotheres maculatus; Derby & Atema 1980), tuna (Thunnus albarcares; Atema et al. 1980), lobsters (Homarus americanus; Atema & Derby 1981) and snails (Acanthina spirata; Murdoch 1969), but extensive experience (2-9 weeks) with novel chemical cues was necessary in all cases. Garter snakes, Thamnophis sirtalis, appear to form chemical search images, but only after 2 weeks of feeding experience (Fuchs & Burghardt 1971). In the most relevant observation, Burghardt (1968) reported that about half of the garter snakes he tested developed preferences for specific prey chemicals (worms or fish) following several predatory strikes. Several other studies have demonstrated changes in reptile food preferences based on early feeding experience (Burghardt & Hess 1966; Burghardt 1967) or on food-aversion conditioning (Burghardt et al. 1973). Animals in these studies may have formed new chemical representations or altered innate ones (as in Begun et al. 1988). However, only in the present case would the term search image have the circumscribed meaning suggested by Dawkins (1971). Since rattlesnakes rapidly formed preferences for novel chemical cues as a consequence of a single predatory strike, the present phenomenon is set apart from such concepts as imprinting, training bias (Bryan 1973) and the other alternatives to specific search images listed by Krebs (1973) and by Guilford & Dawkins (1987).
EXPERIMENT
4
In the above experiments, we established that snakes preferentially ingested mice bearing the same chemical cues as were experienced during predatory strikes. Before speculating further about this phenomenon, it must be established that
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chemoreception (vomeronasal or nasal) is at least correlated with the strike-induced chemical preferences. If either type of chemoreception is involved in post-strike choice behaviour, then snakes should spend more time and direct more tongue flicks at the carcass with matching chemical cues than the carcass with non-matching cues (J. Halpern, E. Erickson & M. Halpern, unpublished data; see also Cowles & Phelan 1959). To measure the rate of tongue flicking it is desirable that the duration of prey-choice tests be controlled by the experimenter, otherwise short trials tend to have high rates of tongue flicking and long trials have low rates. Controlling trial duration eliminates this spurious correlation and also ensures that snakes will sample both stimuli. Accordingly, snakes struck a water- or perfumemisted carcass as in experiments 1-3, then nonenvenomated carcasses were presented simultaneously as before but were confined within wire mesh bags (Duvall et al. 1980). Methods Sulyects The subjects were five adult prairie rattlesnakes, C. viridis, previously tested in experiments 1 and 3. Six months had elapsed before snakes were tested in the present experiment. Housing and maintenance conditions were as described in experiment 1. Materials Mouse carcasses were confined in wire mesh bags (each 13.5 x 9.0 cm). The bags were placed S cm apart and secured on a wooden base (13.5 x 23 x 3.5 cm). Procedure Each snake was allowed to strike a water- or perfume-misted (Jungle Gardenia) mouse as described previously. Five min following the predatory strike snakes received simultaneous access for IO min to non-envenomated perfume- and watermisted mouse carcasses, each contained in a wire mesh bag. We recorded the amount of time the snake’s head was facing and within 2.5 cm of each bag. Also, the number of tongue flicks emitted while snakes were within 2.5 cm of each bag was recorded using hand-held counters. These data were collected during each consecutive 2-min interval of the prey-choice test. Inter-observer agreement for these measures has been uniformly high in
Melter
& Chiszar:
Search
previous experiments (e.g. Duvall et al. 1980; Chiszar et al. 1981, 1983b). Each snake was tested twice. Three snakes struck a water-misted carcass and then received the preychoice test. On the following day, the same snakes struck a perfume-misted carcass and then received the prey-choice test. The remaining two snakes struck a perfume-misted carcass on the first day and a water-misted carcass on the second day. The apparatus was washed after each trial, but it is possible that perfume molecules adhered to the wooden base and/or the mesh bags. Therefore, water- and perfume-misted carcasses were always placed in the same mesh bags, but the apparatus was placed into the snakes’ cages so that these respective bags were equally often on the right and left sides of the snakes’ heads. Data
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T
analysis
Each snake’s scores for investigation (time and number of tongue flicks) of matching and nonmatching carcasses were averaged across perfumeand water-strike trials. These scores were analysed by repeated measures analyses of variance (ANOVAs) to evaluate the effects of matching versus non-matching chemical cues and consecutive 2-min intervals of the prey-choice test. Results and Discussion Figure 1 presents the mean time spent investigating and mean number of tongue flicks directed at each carcass (i.e. the one matching the prey that was struck, and the non-matching one). The means are plotted over successive 2-min blocks of the prey-choice test. The interaction between matching versus non-matching prey and 2-min blocks of testing was significant for both time and tongue flicks (Fsq,r6=4.59 and 3.74, Ps < 0.05). Post-hoc tests (Newman-Kuels) confirmed that means for both measures of investigation were significantly higher for matching carcasses than for non-matching ones during the first 2-min block (PscO.05). There were no significant differences in either measure of investigation between matching and non-matching carcasses after the first 2-min interval. The present experiment extends the effect obtained in experiments 1, 2 and 3 to two new dependent variables. Snakes preferentially investigated the carcass with chemical cues matching those on the carcass that was struck. Since tongue flicking is related to chemosensation (Burghardt
Figure 1. Mean (&SE) time spent investigating and number of tongue flicks directed at matching (m) and non-matching (0) carcasses during consecutive 2-min intervals of the prey-choice test.
1970, 1980; Kubie & Halpern 1979; Halpern & Kubie 1980, 1983; Gillingham & Clark 1981), the present results suggest that the selection of matching carcasses in experiments 1,2 and 3 was based on the vomeronasal and/or nasal systems. The transient preference for the matching carcass was probably related to the inability of snakes to ingest this prey, thereby inducing the predators to explore the alternative, non-matching, item. It seems likely that, under natural circumstances, snakes would begin to grasp and swallow prey shortly after locating it. Thus, there may not have been selective pressure for a strike-induced preference to endure beyond recognition and location of prey. Alternatively, the strike-induced chemical preference may be a short-lived phenomenon that influences the predator’s searching behaviour only for a few minutes. This second interpretation suggests that the chemical preferences observed in these experiments may not last long enough to guide the trailing behaviour of rattlesnakes under natural conditions. The following experiment attempts to resolve this issue.
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Animal EXPERIMENT
Behaviour,
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The process of trailing an envenomated rodent requires considerable time; 20 min is not uncommon in laboratory tests, and snakes remain alert to trails for as long as 2 h following a predatory strike (Chiszar et al. 1982, 1985a; Golan et al. 1982). Thus, it is important to learn how long snakes retain the chemical preference reported in experiments 1 through 4. Does the disappearance of the preference after the first 2-min block (see Fig. 1) depend on the testing procedure that prevents grasping and swallowing, or does it indicate that the preference is retained only for several minutes? If the first view is correct, then snakes should prefer the matching carcass when a longer delay (e.g. 60 min) is introduced between the predatory strike and the prey-choice test. Methods Subjects The subjects were eight adult prairie rattlesnakes (four from experiment 4 and four naive snakes). Housing and deprivation conditions were as described in experiment 1. Procedure The strike and prey-choice procedures were the same as described in experiment 4. Each snake was tested twice, once on each of 2 consecutive days. One prey-choice test occurred 5 mm following predatory strike and the other test occurred 60 min after the strike. Four snakes (two naive and two from experiment 4) received the 5-min test on the first day and the 60-min test on the second day, whereas the remaining four snakes received the delay conditions in the reverse order. Four snakes struck a water-misted carcass and four struck a perfume-misted (Jungle Gardenia) carcass prior to each prey-choice test. The duration of the prey-choice test and the dependent variables recorded were the same as in experiment 4. Results and Discussion Figure 2 shows the mean time and mean number of tongue flicks directed at matching and nonmatching carcasses during the first 2 min of the prey-choice test. Performance after the 5- and 60min delays was similar; snakes investigated the matching carcass significantly more than the nonmatching carcass after both delays. Repeated
5-min
60-min Delay
time
Figure 2. Mean (t-SE) time spent investigating and number of tongue flicks directed at matching (m) and non-matching (0) carcasses during prey-choice tests conducted 5- and 60-min after predatory strike. Data represent performance during the first 2-min interval of the test. measures ANOVAs performed on the effects of matching versus non-matching prey and test delay (5 or 60-min) revealed main effects of type of carcass on time and tongue flicks, (Fs,,~ = 7.48 and 6.3 1, Ps < 0.05). There were no significant interactions between test delay and carcass type in either analysis. As in experiment 4, preference for the matching carcass disappeared after the first 2-min block. Therefore, only performance during the first 2-min interval is shown in Fig. 2. Snakes retained the strike-induced chemical preference over a substantial delay, and the preference observed after 60 min was as robust as the preferences observed in tests conducted only a few minutes after the predatory strike. It is also important to note that the absolute levels of investigation (time and tongue flicks) were similar after both delays. These findings indicate that chemical preferences acquired by snakes during predatory strike are retained long enough to guide extended trailing of prey under natural circumstances. Retention of the chemical preference after 60 min also suggests that peripheral after-effects of the
Melter
& Chiszar: Search images in rattlesnakes
strike (e.g. residuation of chemical cues in the vomeronasal or nasal organs) probably do not mediate the snakes’ ability to recognize the matching carcass. Such peripheral after-effects would be expected to dissipate within 5510 min after the strike (Meredith 1980; Chiszaret al. 1985b). Hence, we are probably dealing with a central nervous system representation that is created consequent to the predatory strike. Most important, occurrence of the strike-induced preference in the 60-min test suggests that disappearance of the preference after the first 2 min during both 5- and 60-min tests is a function of test procedure (i.e. since snakes could not grasp the preferred item, they were induced to investigate the alternative).
EXPERIMENT
6
Various species of rattlesnakes show elevated levels of tongue flicking until about 2 h following predatory strikes (Chiszar et al. 1982, 1985a). Thus, it is of interest to know if retention of the chemical learning observed in the above experiments also dissipates 2 h following the strike. Methods Subjects Eight prairie rattlesnakes (all from experiment 5) were subjects. One snake failed to respond during the prey-choice test and was dropped from the experiment. Housing and deprivation conditions were as described previously. Procedure The procedures were the same as in experiment 5 with the following exceptions. Each snake was tested once; four snakes struck a water-misted carcass and three snakes struck a perfume-misted carcass. All snakes received the prey-choice test 120 min after the strike. We recorded the same dependent variables as in experiments 4 and 5 (time spent over the tongue flicks directed at matching and non-matching carcasses). Results and Discussion There were no significant differences between investigation of matching and non-matching carcasses at any point during the prey-choice test after the 2-h delay. The combined mean number of seconds spent investigating the carcasses (s match-
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ing+ s non-matching/2) during the first 2-min block was 28.9 and the combined mean number of tongue flicks directed at the carcasses was 21.3. Thus, the absolute level of investigation observed 120 min after the strike was comparable to the absolute level of investigation observed in the 5and 60-min tests (see Fig. 2). This finding indicates that snakes were as motivated to investigate prey after the 2-h delay as they were in the shorter delay tests; they simply did not exhibit a preference for the matching carcass 2 h after the strike. We suggest that the specific chemical search image decays between 60 and 120 min following the strike.
EXPERIMENT
7
The above experiments show that rattlesnakes acquire chemical cues from rodents during predatory strikes and retain such information as long as 1 h after the strike. Admittedly, our application of chemical cues to rodents was artificial in that carcasses were misted with various perfume solutions to induce distinctive chemical cues on the rodents. It is important to attempt to simulate more natural circumstances by which rodents might acquire distinctive aromas. One way that rodents might acquire idiosyncratic chemical cues is through their diets, since different foods should leave different chemical cues in their mouths and/or on their integuments as a consequence of feedingrelated activities such as grooming. Galef and his colleagues have shown that laboratory rats can transmit chemical cues arising from their diets through various social interactions with conspecifits naive to the same diets (Galef & Wigmore 1983; Galef et al. 1985; Galef & Stein 1985). In the present experiment we investigated the possibility that, during predatory strikes, snakes might acquire chemical cues associated with the rodent’s diet and use such information in subsequent search for prey. If snakes can discriminate between mice based on their diets, then they should prefer carcasses of mice that ate the same diet as the mouse struck. Methods Subjects The subjects were six prairie rattlesnakes that had experience in the above experiments. Snakes
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Behaviour,
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had not been tested for about 30 days prior to the present experiment. Housing and maintenance conditions were as described previously.
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Procedure
The strike and prey-choice procedures were the same as described in experiment 4. Snakes struck either the carcass of a mouse that had been eating cinnamon chow (see below, N = 3) or the carcass of a mouse that ate cocoa chow (see below, N= 3). All prey-choice tests were conducted 10 min after snakes struck prey; the envenomated mouse was discarded as before and snakes received a choice between a cinnamon carcass and a cocoa carcass (described below) confined in wire mesh bags as in experiment 4. Adult mice, Mus musculus, were used as stimuli and were housed four or five to a cage. They were provided with access to water and glass bowls containing powdered laboratory chow adulterated with either ground cinnamon (I % by weight) or Hershey’s cocoa (2% by weight). Each cage was supplied with 100 g of the appropriate diet on each of 2 consecutive days. Mice ate most of their chow but some of it was found distributed widely in the cages. On the afternoon of their second day with the cinnamon or cocoa diets, mice were killed and the carcasses were used as stimuli in either the strike or prey-choice procedures. The experimenter could detect cinnamon or cocoa odour on each carcass. Results and Discussion Figure 3 shows mean investigation scores (time and tongue flicks) for matching and non-matching carcasses during the prey-choice tests. Snakes spent significantly more time over the matching carcass than the non-matching one during the first 2-min interval (F,,s= 35.24, P~0.02). There was also a greater number of tongue flicks over the matching carcass than the non-matching carcass during the first 2 min (FI.s= 14.81, P~0.02). As in previous experiments, the preference for the matching carcass disappeared after the first 2 min of testing. The present experiment indicates that rodents acquired distinctive chemical cues from their diets. Mice may have acquired chemical cues from diets as a consequence of ingestion and/or through residual particles of food left on their integuments. Most importantly, rattlesnakes detected this chemical information during predatory strikes and used it during subsequent search for the prey. This
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Figure 3. Mean (&SE) time spent investigating and number of tongue flicks directed at matching (m) and non-matching (0) carcasses during consecutive 2-min intervals of the prey-choice test. finding suggests a natural mechanism by which rodents might develop individual chemical identities that rattlesnakes could use during post-strike trail following. GENERAL
DISCUSSION
Rodent-specializing rattlesnakes rapidly formed chemical search images. The predatory strike provided initial access to the chemical cues, and the snakes retained some representation of this information for at least 60 min. Retention of the chemical preference over this delay presumably could facilitate location of the wounded rodent’s trail and eventual location of the carcass. It remains unclear how the chemical learning observed in the present experiments might interact with other mechanisms that support post-strike location of envenomated prey (Duvall et al. 1980; Lee & Chiszar, unpublished data). Rattlesnakes probably use several different cues at their disposal to trail prey following predatory strikes. Our data also show that rattlesnakes acquired strike-induced preferences for chemical cues of
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rodents feeding on different diets. Thus, it is conceivable that rattlesnakes make use of their chemical learning ability under natural circumstances. Rodents feeding on different materials probably possess different chemical cues that may be acquired and used by snakes during predation. We propose that the phenomenon reported in experiment 7 would also occur with rodents feeding on diets containing more natural fragrances (e.g. sage). The strike-release-trail strategy is an aspect of specialization upon rodent prey by rattlesnakes. Indeed, some researchers regard this behaviour as a sign of rodent specialization when it is seen in other taxa of venomous snakes (Shine & Covacevich 1983). Accordingly, until comparative data become available, we are hesitant to generalize our conclusions about chemical search images to taxa other than those practising the strike-release-trail strategy. Perhaps this chemical memory system is unique to these species.
ACKNOWLEDGMENTS
We thank the animal care facility of the Department of Psychology for the rodents used in these experiments. We also thank Dr B. G. Galef, Jr for several lively conversations that led to this line of work. Indeed, we have referred to these studies as demonstrating a capitalization upon the Galef effect by rattlesnakes (e.g. such terminology was used at the winter conference on Current Issues in Developmental Psychobiology, 1986). We thank Karl Kandler, Mary Jen and Oakland Salavea for help in gathering the data.
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Baumann, F. 1927. Experimente uber den Geruchssin der Viper. Revue suisse Zool., 34, 173-184. Begun, D., Kubie, J. L., O’Keefe, M. P. & Halpern, M. 1988. Conditioned discrimination of an airborne odorant by garter snakes (Thamnophis radix and T. sirtalis sirtalis.). J. camp. PsychoI., 102, 3543. Brock, 0. G. 1980. Predatory behavior of eastern diamondback rattlesnakes (Crotalus adamanteus): field enclosure and Y-maze laboratory studies, emphasizing prey-trailing behavior. Ph.D. thesis, Florida State University. Bryan, J. E. 1973. Feeding history, parental stock, and food selection in rainbow trout. Behaviour, 45, 123% 153. Burghardt, G. M. 1967. The primacy effect of the first feeding experience in the snapping turtle. Psychonom. Sci., 7, 383-384. Burghardt, G. M. 1968. The reinforcement potential of the consummatory act in the modification of chemicalcue preferences. Am. Zool., 8, 745. Burghardt, G. M. 1970. Chemical perception in reptiles. In: Communication by Chemical Signals (Ed. by J. S. Johnston, Jr, D. G. Moulton&A. Turk), pp. 241-308, New York: Appleton-Century-Crofts. Burghardt, G. M. 1980. Behavioral and stimulus correlates of vomeronasal functioning in reptiles: feeding, grouping, sex and tongue use. In: Chemical Signals. Vertebrates and Aquatic Invertebrates. (Ed. by D. Muller-Schwarze & R. Silverstein), pp. 275-301. New York: Plenum Press. Burghardt, G. M. & Hess, E. H. 1966. Food imprinting in the snapping turtle, Chelydra serpentina. Science, N. Y., 151,
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Burghardt, G. M., Wilcoxin, H. C. & Czaplicki, J. A. 1973. Conditioning in garter snakes: aversion to palatable prey induced by delayed illness. Anim. Learn. Behav., I, 317-320. Chiszar, D., O’Connell, B., Greenlee, R., Demeter, B., Walsh T., Chiszar, J., Moran, K. & Smith, H. M. 1985a. Duration of strike-induced chemosensory searching in long term captive rattlesnakes at National Zoo, Audobon Zoo and San Diego Zoo. Zoo biol., 4, 291-294. Chiszar, D., Radcliffe, C. W. & Feiler, F. 1986. Trailing behavior in banded rock rattlesnakes (Crotalus lepidus klauberi) and prairie rattlesnakes (C. viridis viridis). J. camp. PsychoI., 100, 368-371. Chiszar, D., Radcliffe, C. W., O’Connell, B. & Smith, H. M. 1981. Strike-induced chemosensory searching in rattlesnakes (Crotalus viridis) as a function of disturbance prior to presentation of rodent prey. Psycho/. Rec., 32, 57-62. Chiszar, D., Radcliffe, C. W., O’Connell, B. & Smith, H. M. 1982. Analysis of the behavioral sequence emitted by rattlesnakes during feeding episodes.: 2. Duration of strike-induced chemosensory searching in rattlesnakes (Crotalus viridis, C. enyo). Behav. Neur. Biol., 34, 261270. Chiszar, D., Radcliffe, C. W., Overstreet, R. & Poole, T. 1985b. Duration of strike-induced chemosensory searching in the cottonmouth (Agkistrodonpisciuorous) and a test of the hypothesis that striking prey creates a specific search image. Can. J. Zool., 63, 1057~1061. Chiszar, D., Radcliffe, C. W., Scudder, K. M. & Duvall,
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Halpern, M. & Kubie, J. L. 1980. Chemical access to the vomeronasal organs of garter snakes. Physiol. Eehav., 24, 3677371. Halpern, M. & Kubie, J. L. 1983. Snake tongue flicking behavior: clues to vomeronasal system functions. In: Chemical Signals in Vertebrates 3 (Ed. by D. MullerSchwarze & R. M. Silverstein), pp. 45-72. New York: Plenum Press. Hayes, W. K. & Galusha, J. A. 1984. Effects of rattlesnake (Crotalus viridis oreganus) envenomation on mobility of male wild and laboratory mice (Mus musculus).
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Melter. T.. Kandler. K. & Chiszar. D. In mess. Effects of nova1 chemical cues on predatory responses of rodentspecializing rattlesnakes. Bull. Ps.whonom. Sot. Meredith. M. 1980. The vomeronasal organ and accessory olfactory systems in hamster. In: Chemical Signals. Vertebrate and Aquatic Invertebrates (Ed. by D. Muller-Schwarze & R. M. Silverstein). pp. 3033326. New York: Plenum Press. Murdoch, W. W. 1969. Switching in general predators: experiments on predator specificity and stability of prey populations. Ecol. Monogr., 39, 335 354. Naulleau, G. 1965. La biologie et le comportement predateur de Vipera aspis au laboratoire ct dans la nature. Bull. Biol. Fr. Belg., 99, 395--524. Pietrewicz, A. T. & Kamil, A. C. 198 1. Search images and detection of cryptic prey: an operant approach. In: Foraging Behavior: logical Approaches
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(Ed. by A. C. Kamil & T. D. Sargeant). pp. 3 1 I-33 I New York: Garland STPM. Pough. F. H. &Groves, J. E. 1983. Specializations of the body form and food habits of snakes. .4n7. Zool., 23, 443 454. Reinert, H. K., Cundall, D. & Busher, L. M. 1984. Foraging behavior of the timber rattlesnake. Crotalus horridus. Copeia, 1984,976 -98 I. Shine. R. & Covacevich, J. 1983. Ecology of highly venomous snakes: the Australian genus 0s.wrnnu.s (Elapidae). .I. Herpetol., 17, 60-69. Tinbergen, L. 1960. The natural control of insects in pinewoods. I. Factors influencing the intensity of predation of songbirds. Archs N&er Zool., 13,265- 343. Wiedemann, E. 1932. Zur Biologie der Nahrungsaufnahme der Kreuzotter. Vineraberur L. Zoo/. Anz., 97, 278 286.
(Received
7 March 1988; MS. number:
revised A5251
16 MU!,
I
I98R,
Behav.,
1989,37,477-486
Striking prey creates a specific chemical search image in rattlesnakes Department
TED MELCER & DAVID CHISZAR of Psychology, University of Colorado, Boulder,
CO 80309, U.S.A.
Abstract. Rattlesnakes, Crotalus viridis, struck mouse carcasses misted with water or with diluted perfume. Envenomated carcasses were removed, and later the snakes were presented with a pair of nonenvenomated carcasses, each misted with one of these liquids. Snakes preferred the carcass with the same odour as the prey that was struck, even when the test occurred 60 min after the predatory strike. Under natural circumstances, rodents may acquire distinct chemical identities through their diet. In further tests, snakes preferred carcasses of mice that had been eating the same diet as the mouse that had been struck. These results indicate that rattlesnakes rapidly acquire chemical information from rodent prey during predatory strikes and use this information in subsequent search for prey.
Most species of rattlesnakes specialize upon rodent prey, exhibiting traits that capitalize upon rodent morphology, physiology and behaviour (Greene 1983; Pough & Groves 1983). For example, timber and prairie rattlesnakes wait in ambush along trails habitually used by their prey (Reinert et al. 1984; Duvall et al. 1985; Diller, in press). Also, rattlesnakes typically release adult rodents after the strike, reducing risk of injury from rodent teeth and claws (Klauber 1956; Kardong 1986). Envenomated mice die in 3-8 minutes, and snakes wait about this long before searching for them, suggesting the cadence of the predator’s behaviour has been designed to avoid contact with a rodent still capable of self defence (Estep et al. 1981; Hayes & Galusha 1984). The searching process capitalizes upon chemical cues deposited by prey as they wandered from the site of attack (Brock 1980; Golan et al. 1982; Chiszar et al. 1983a, 1986). Since many rodent trails are likely to be in the snake’s vicinity, selecting the specific trail of the envenomated prey is a crucial task confronting the predator and vipers do this with little difficulty (Baumann 1927; Wiedemann 1932; Naulleau 1965; Duvall et al. 1980; Lee & Chiszar, unpublished data; see Burghardt 1970, for a review of chemical perception in reptiles). Several mechanisms may support trail-following by rattlesnakes. For instance, chemical cues of envenomated rodents are generally attractive to a rattlesnake searching for prey even if the rodent was envenomated by another snake (Duvall et al. 1980). Also, snakes orient toward the prey as it departs from the site of attack, and the subsequent 0003-3472/89/030477
+ 10$03.00/O
search begins in that direction (Lee & Chiszar, unpublished data). A previously unexplored possibility is that chemical learning may occur during the strike and later guide the snake in following idiosyncratic chemical cues left by the envenomated prey. The present experiments tested the possibility that rattlesnakes acquire chemical information from prey during the brief contact (0.3 s) made while striking. EXPERIMENT
If prairie rattlesnakes develop preferences for chemical cues acquired during the predatory strike, then the snakes should select carcasses with chemical cues matching those on the envenomated prey. Consequently, rattlesnakes were permitted to strike a mouse carcass misted with either a floral perfume or with water. This carcass was discarded, and snakes then received simultaneous access to two non-envenomated carcasses scented with either water or the perfume. Since neonatal rattlesnakes without prior feeding experience are known to detect and follow chemical cues arising from envenomated mice, it is reasonable to infer an innate perceptual basis for such behaviour (Scudder, Poole, O’Connell & Chiszar, unpublished data). Consequently, to demonstrate that a learning process also contributes to carcass recovery, snakes must demonstrate an ability to use arbitrary chemical cues (not normally associated with prey) as discriminative stimuli (cf. Begun et al. 1988). This is why perfume was applied to mice. Nonenvenomated carcasses were used during the choice
01989
477
1
The Association for the Study of Animal Behaviour
478
Animal Behaviour,
tests to eliminate any preference effects that might be associated with envenomated mice (Duvall et al. 1978, 1980). Methods
Subjects The subjects were 40 adult prairie rattlesnakes, Crotalus viridis, approximately 70 cm long. Snakes were captured as adults and maintained individually in glass terraria (50 x 27.5 x 30 cm) containing paper floor coverings and stainless steel vessels filled with water. The room was kept at 26-28°C during the photophase (0700-1900 hours) and at 22-24°C during the scotophase. All snakes had been in captivity for several years and had been accepting rodent prey (Mus musculus or preweanling Rattus norvegicus, 20-27 g) on a biweekly schedule. Previously euthanized rodents were fed to snakes, and these carcasses were always suspended into the snakes’ home cages from forceps in order to elicit predatory strikes. Consequently, snakes were accustomed to striking prior to ingesting prey. Snakes were not fed for 2 weeks prior to testing. Although the snakes had been used in previous experiments involving presentation of chemical stimuli, no surgical or pharmacological manipulations had been performed. Therefore, we consider these snakes typical of long-term captive crotalines. Procedure All snakes were observed in their home cages. First, a mouse carcass was misted with about 1 ml of either diluted perfume (2 ml of Jungle Gardenia perfume in 710 ml of tap water) or water. No live rodents were used as stimuli; they were euthanized by cervical dislocation 2 min prior to the experiment. All mice were culls from local breeding facilities and all carcasses were eventually ingested by snakes. For 20 snakes, the lid of a home cage was opened and the misted carcass was suspended from forceps 10 cm above and slightly in front of the snakes’ heads. Within a few seconds snakes oriented to these carcasses, then struck and released them. The envenomated carcass was removed immediately without making contact with any part of the home cage, and the cage lid was closed. Ten snakes struck carcasses misted with water and 10 struck carcasses misted with diluted perfume. The envenomated carcass was discarded and two non-envenomated carcasses were used for the preychoice test, one misted with the diluted perfume
37, 3
and one misted with water. Five min after the strike, the new carcasses were placed on the cage floor in dorsal recumbency, 4 cm apart and at the far end of the cage from the snake. The position of perfume- and water-misted carcasses relative to the snake’s head was counterbalanced across snakes. The carcasses remained for 20 min or until the snake ingested one of them. We recorded which carcass was first grasped and swallowed by the snake. These procedures were also applied to 20 additional rattlesnakes that received no-strike presentations of water-misted (N= 10) or perfumedmisted (N= 10) carcasses. In these tests the carcasses were suspended into the home cages but held outside of striking range for 5 s. Results and Discussion All snakes that struck a stimulus mouse carcass swallowed a non-envenomated carcass during the 20-min test, and 16 of these snakes (eight from each subgroup) ingested carcasses that were misted with the same liquid as was present on the prey previously struck (x2 = 7.2, df = 1, P < 0.05). After the no-strike trials, however, snakes either failed to feed within 20 min (N= 11) or they selected randomly among the carcasses. This finding is consistent with previous studies demonstrating that chemosensory searching and trail following occur more intensely and more effectively after predatory strikes (Duvall et al. 1980; Golan et al. 1982; Chiszar et al. 1983a). More importantly, the behaviour of snakes after no-strike presentations strongly suggests that preferences seen after strike presentations are induced, not by mere exposure to chemical cues, but rather by their detection on the prey item during envenomation. It is noteworthy that snakes exhibited equally strong though opposite preferences after they struck water- or perfume-misted carcasses, respectively. That is, snakes showed no greater post-strike preference for familiar, water-misted carcasses than for novel, perfume-misted ones. In fact, we have independent evidence that such prey items are equally acceptable to rattlesnakes as stimuli for envenomation and ingestion (Melter et al., in press). Consequently, the post-strike preferences reported here must have arisen during the strike and we suggest that they are akin to search images (Tinbergen 1960). That is, rattlesnakes acquire a strike-induced preference for specific chemical cues on the prey they have struck.
Melter EXPERIMENT
& Chiszar: Search images in rattlesnakes 2
We tested whether the strike-induced preferences observed in experiment 1 occur in other taxa of rattlesnakes that exhibit the strike-release-trail strategy described above. Thus, we repeated experiment 1 using six species of rattlesnakes other than C. viridis. Methods Subjects Twenty new adult rattlesnakes (eight C. enyo, four C. horridus, four C. adamanteus, one C. atrox, one C. ruber, two Sistrurus miliaruis) were observed. The history and housing conditions for these snakes were as described for snakes in experiment 1. Procedure The procedures were the same as in experiment 1. Ten snakes struck a water-misted carcass and 10 struck a perfume-misted carcass (same solution as in experiment 1). Where possible, half of the snakes of each species were assigned to each strike condition (water or perfume). All snakes were then permitted to choose between two non-envenomated carcasses, one misted with water and one with perfume. Since no-strike presentations did not result in biased choice behaviour in experiment 1, we did not include such tests here (Golan et al. 1982; Chiszar et al. 1983a). Results and Discussion Seventeen snakes (eight that struck water-misted prey, nine that struck perfume-misted prey) first grasped and swallowed the carcass matching the fragrance of the prey that had been struck (x2 =9.80, df= 1, P< 0.05). Thus, the post-strike preferences seen in experiment 1 also occurred in this group of rattlesnakes, all of which are rodentspecialists. Small sample sizes do not permit comparisons between the individual species, and none was made. The only conclusion we wish to offer is that the phenomenon of experiment I is probably not restricted to C. viridis.
EXPERIMENT
3
If our chemical-learning interpretation of experiments 1 and 2 is correct, then the post-strike
479
performance of rattlesnakes should not depend upon the specific chemicals used in those studies (i.e. water and diluted Jungle Gardenia perfume). Therefore, experiment 3 was designed to assess post-strike performance of snakes when different chemicals were applied to mouse carcasses. Methods Subjects The subjects were 20 prairie rattlesnakes that had been tested in experiment 1. Housing and maintenance conditions were as described in experiment 1. Procedure Testing procedures were similar to those described in experiment 1. In experiment 3, snakes struck a carcass misted with either Tea Rose or Jungle Gardenia solution (N= 5 in each condition). These 10 snakes then received prey-choice tests with non-envenomated carcasses misted with Tea Rose and Jungle Gardenia, respectively. The dilution of perfumes in this experiment was the same as reported in experiment 1. An additional 10 snakes struck a carcass misted with either Tea Rose or Halston perfume (N= 5 in each condition). These snakes then received prey-choice tests with nonenvenomated carcasses misted with Tea Rose and Halston, respectively. Tea Rose and Jungle Gardenia are floral scents, whereas Halston is a musk scent. Results and Discussion Fifteen snakes (eight from the Jungle Gardenia versus Tea Rose tests; seven from the Tea Rose versus Halston tests) ingested the carcass bearing the same chemical cues as were encountered during the strike (x2 = 6.66, df= 1, P < 0.05). Thus, snakes were able to discriminate between two floral perfumes, and between a floral and musk scent. This implies that the results of experiments 1 and 2 were not dependent upon specific chemicals used (e.g. choosing between familiar and novel chemical cues). Accordingly, experiment 3 strengthens the conclusions that chemosensory learning occurred during predatory strikes and that some representation of this information was maintained until the prey-choice tests. That floral perfumes could be registered and remembered implies that ophidian chemosensation is not restricted to cues associated with natural prey, mates or enemies. Some receptor
480
Animal Behaviour,
macromolecules and associated central nervous system processes must transduce, encode and retain novel chemical information (Arnold 1981; Atema & Derby 1981; Begun et al. 1988). These findings constitute the first systematic evidence of rapidly formed preferences for chemical features of prey (i.e. chemical search images; see also Chiszar et al. 198Sb). Most work on search images has concentrated on visually searching predators (following Tinbergen 1960; see also Curio 1976; Pietrewicz & Kamil 1981). Evidence exists for the development of chemical search images in pea crabs (Pinnotheres maculatus; Derby & Atema 1980), tuna (Thunnus albarcares; Atema et al. 1980), lobsters (Homarus americanus; Atema & Derby 1981) and snails (Acanthina spirata; Murdoch 1969), but extensive experience (2-9 weeks) with novel chemical cues was necessary in all cases. Garter snakes, Thamnophis sirtalis, appear to form chemical search images, but only after 2 weeks of feeding experience (Fuchs & Burghardt 1971). In the most relevant observation, Burghardt (1968) reported that about half of the garter snakes he tested developed preferences for specific prey chemicals (worms or fish) following several predatory strikes. Several other studies have demonstrated changes in reptile food preferences based on early feeding experience (Burghardt & Hess 1966; Burghardt 1967) or on food-aversion conditioning (Burghardt et al. 1973). Animals in these studies may have formed new chemical representations or altered innate ones (as in Begun et al. 1988). However, only in the present case would the term search image have the circumscribed meaning suggested by Dawkins (1971). Since rattlesnakes rapidly formed preferences for novel chemical cues as a consequence of a single predatory strike, the present phenomenon is set apart from such concepts as imprinting, training bias (Bryan 1973) and the other alternatives to specific search images listed by Krebs (1973) and by Guilford & Dawkins (1987).
EXPERIMENT
4
In the above experiments, we established that snakes preferentially ingested mice bearing the same chemical cues as were experienced during predatory strikes. Before speculating further about this phenomenon, it must be established that
37,3
chemoreception (vomeronasal or nasal) is at least correlated with the strike-induced chemical preferences. If either type of chemoreception is involved in post-strike choice behaviour, then snakes should spend more time and direct more tongue flicks at the carcass with matching chemical cues than the carcass with non-matching cues (J. Halpern, E. Erickson & M. Halpern, unpublished data; see also Cowles & Phelan 1959). To measure the rate of tongue flicking it is desirable that the duration of prey-choice tests be controlled by the experimenter, otherwise short trials tend to have high rates of tongue flicking and long trials have low rates. Controlling trial duration eliminates this spurious correlation and also ensures that snakes will sample both stimuli. Accordingly, snakes struck a water- or perfumemisted carcass as in experiments 1-3, then nonenvenomated carcasses were presented simultaneously as before but were confined within wire mesh bags (Duvall et al. 1980). Methods Sulyects The subjects were five adult prairie rattlesnakes, C. viridis, previously tested in experiments 1 and 3. Six months had elapsed before snakes were tested in the present experiment. Housing and maintenance conditions were as described in experiment 1. Materials Mouse carcasses were confined in wire mesh bags (each 13.5 x 9.0 cm). The bags were placed S cm apart and secured on a wooden base (13.5 x 23 x 3.5 cm). Procedure Each snake was allowed to strike a water- or perfume-misted (Jungle Gardenia) mouse as described previously. Five min following the predatory strike snakes received simultaneous access for IO min to non-envenomated perfume- and watermisted mouse carcasses, each contained in a wire mesh bag. We recorded the amount of time the snake’s head was facing and within 2.5 cm of each bag. Also, the number of tongue flicks emitted while snakes were within 2.5 cm of each bag was recorded using hand-held counters. These data were collected during each consecutive 2-min interval of the prey-choice test. Inter-observer agreement for these measures has been uniformly high in
Melter
& Chiszar:
Search
previous experiments (e.g. Duvall et al. 1980; Chiszar et al. 1981, 1983b). Each snake was tested twice. Three snakes struck a water-misted carcass and then received the preychoice test. On the following day, the same snakes struck a perfume-misted carcass and then received the prey-choice test. The remaining two snakes struck a perfume-misted carcass on the first day and a water-misted carcass on the second day. The apparatus was washed after each trial, but it is possible that perfume molecules adhered to the wooden base and/or the mesh bags. Therefore, water- and perfume-misted carcasses were always placed in the same mesh bags, but the apparatus was placed into the snakes’ cages so that these respective bags were equally often on the right and left sides of the snakes’ heads. Data
images
in rattlesnakes
I
481
T
analysis
Each snake’s scores for investigation (time and number of tongue flicks) of matching and nonmatching carcasses were averaged across perfumeand water-strike trials. These scores were analysed by repeated measures analyses of variance (ANOVAs) to evaluate the effects of matching versus non-matching chemical cues and consecutive 2-min intervals of the prey-choice test. Results and Discussion Figure 1 presents the mean time spent investigating and mean number of tongue flicks directed at each carcass (i.e. the one matching the prey that was struck, and the non-matching one). The means are plotted over successive 2-min blocks of the prey-choice test. The interaction between matching versus non-matching prey and 2-min blocks of testing was significant for both time and tongue flicks (Fsq,r6=4.59 and 3.74, Ps < 0.05). Post-hoc tests (Newman-Kuels) confirmed that means for both measures of investigation were significantly higher for matching carcasses than for non-matching ones during the first 2-min block (PscO.05). There were no significant differences in either measure of investigation between matching and non-matching carcasses after the first 2-min interval. The present experiment extends the effect obtained in experiments 1, 2 and 3 to two new dependent variables. Snakes preferentially investigated the carcass with chemical cues matching those on the carcass that was struck. Since tongue flicking is related to chemosensation (Burghardt
Figure 1. Mean (&SE) time spent investigating and number of tongue flicks directed at matching (m) and non-matching (0) carcasses during consecutive 2-min intervals of the prey-choice test.
1970, 1980; Kubie & Halpern 1979; Halpern & Kubie 1980, 1983; Gillingham & Clark 1981), the present results suggest that the selection of matching carcasses in experiments 1,2 and 3 was based on the vomeronasal and/or nasal systems. The transient preference for the matching carcass was probably related to the inability of snakes to ingest this prey, thereby inducing the predators to explore the alternative, non-matching, item. It seems likely that, under natural circumstances, snakes would begin to grasp and swallow prey shortly after locating it. Thus, there may not have been selective pressure for a strike-induced preference to endure beyond recognition and location of prey. Alternatively, the strike-induced chemical preference may be a short-lived phenomenon that influences the predator’s searching behaviour only for a few minutes. This second interpretation suggests that the chemical preferences observed in these experiments may not last long enough to guide the trailing behaviour of rattlesnakes under natural conditions. The following experiment attempts to resolve this issue.
482
Animal EXPERIMENT
Behaviour,
37, 3
5
The process of trailing an envenomated rodent requires considerable time; 20 min is not uncommon in laboratory tests, and snakes remain alert to trails for as long as 2 h following a predatory strike (Chiszar et al. 1982, 1985a; Golan et al. 1982). Thus, it is important to learn how long snakes retain the chemical preference reported in experiments 1 through 4. Does the disappearance of the preference after the first 2-min block (see Fig. 1) depend on the testing procedure that prevents grasping and swallowing, or does it indicate that the preference is retained only for several minutes? If the first view is correct, then snakes should prefer the matching carcass when a longer delay (e.g. 60 min) is introduced between the predatory strike and the prey-choice test. Methods Subjects The subjects were eight adult prairie rattlesnakes (four from experiment 4 and four naive snakes). Housing and deprivation conditions were as described in experiment 1. Procedure The strike and prey-choice procedures were the same as described in experiment 4. Each snake was tested twice, once on each of 2 consecutive days. One prey-choice test occurred 5 mm following predatory strike and the other test occurred 60 min after the strike. Four snakes (two naive and two from experiment 4) received the 5-min test on the first day and the 60-min test on the second day, whereas the remaining four snakes received the delay conditions in the reverse order. Four snakes struck a water-misted carcass and four struck a perfume-misted (Jungle Gardenia) carcass prior to each prey-choice test. The duration of the prey-choice test and the dependent variables recorded were the same as in experiment 4. Results and Discussion Figure 2 shows the mean time and mean number of tongue flicks directed at matching and nonmatching carcasses during the first 2 min of the prey-choice test. Performance after the 5- and 60min delays was similar; snakes investigated the matching carcass significantly more than the nonmatching carcass after both delays. Repeated
5-min
60-min Delay
time
Figure 2. Mean (t-SE) time spent investigating and number of tongue flicks directed at matching (m) and non-matching (0) carcasses during prey-choice tests conducted 5- and 60-min after predatory strike. Data represent performance during the first 2-min interval of the test. measures ANOVAs performed on the effects of matching versus non-matching prey and test delay (5 or 60-min) revealed main effects of type of carcass on time and tongue flicks, (Fs,,~ = 7.48 and 6.3 1, Ps < 0.05). There were no significant interactions between test delay and carcass type in either analysis. As in experiment 4, preference for the matching carcass disappeared after the first 2-min block. Therefore, only performance during the first 2-min interval is shown in Fig. 2. Snakes retained the strike-induced chemical preference over a substantial delay, and the preference observed after 60 min was as robust as the preferences observed in tests conducted only a few minutes after the predatory strike. It is also important to note that the absolute levels of investigation (time and tongue flicks) were similar after both delays. These findings indicate that chemical preferences acquired by snakes during predatory strike are retained long enough to guide extended trailing of prey under natural circumstances. Retention of the chemical preference after 60 min also suggests that peripheral after-effects of the
Melter
& Chiszar: Search images in rattlesnakes
strike (e.g. residuation of chemical cues in the vomeronasal or nasal organs) probably do not mediate the snakes’ ability to recognize the matching carcass. Such peripheral after-effects would be expected to dissipate within 5510 min after the strike (Meredith 1980; Chiszaret al. 1985b). Hence, we are probably dealing with a central nervous system representation that is created consequent to the predatory strike. Most important, occurrence of the strike-induced preference in the 60-min test suggests that disappearance of the preference after the first 2 min during both 5- and 60-min tests is a function of test procedure (i.e. since snakes could not grasp the preferred item, they were induced to investigate the alternative).
EXPERIMENT
6
Various species of rattlesnakes show elevated levels of tongue flicking until about 2 h following predatory strikes (Chiszar et al. 1982, 1985a). Thus, it is of interest to know if retention of the chemical learning observed in the above experiments also dissipates 2 h following the strike. Methods Subjects Eight prairie rattlesnakes (all from experiment 5) were subjects. One snake failed to respond during the prey-choice test and was dropped from the experiment. Housing and deprivation conditions were as described previously. Procedure The procedures were the same as in experiment 5 with the following exceptions. Each snake was tested once; four snakes struck a water-misted carcass and three snakes struck a perfume-misted carcass. All snakes received the prey-choice test 120 min after the strike. We recorded the same dependent variables as in experiments 4 and 5 (time spent over the tongue flicks directed at matching and non-matching carcasses). Results and Discussion There were no significant differences between investigation of matching and non-matching carcasses at any point during the prey-choice test after the 2-h delay. The combined mean number of seconds spent investigating the carcasses (s match-
483
ing+ s non-matching/2) during the first 2-min block was 28.9 and the combined mean number of tongue flicks directed at the carcasses was 21.3. Thus, the absolute level of investigation observed 120 min after the strike was comparable to the absolute level of investigation observed in the 5and 60-min tests (see Fig. 2). This finding indicates that snakes were as motivated to investigate prey after the 2-h delay as they were in the shorter delay tests; they simply did not exhibit a preference for the matching carcass 2 h after the strike. We suggest that the specific chemical search image decays between 60 and 120 min following the strike.
EXPERIMENT
7
The above experiments show that rattlesnakes acquire chemical cues from rodents during predatory strikes and retain such information as long as 1 h after the strike. Admittedly, our application of chemical cues to rodents was artificial in that carcasses were misted with various perfume solutions to induce distinctive chemical cues on the rodents. It is important to attempt to simulate more natural circumstances by which rodents might acquire distinctive aromas. One way that rodents might acquire idiosyncratic chemical cues is through their diets, since different foods should leave different chemical cues in their mouths and/or on their integuments as a consequence of feedingrelated activities such as grooming. Galef and his colleagues have shown that laboratory rats can transmit chemical cues arising from their diets through various social interactions with conspecifits naive to the same diets (Galef & Wigmore 1983; Galef et al. 1985; Galef & Stein 1985). In the present experiment we investigated the possibility that, during predatory strikes, snakes might acquire chemical cues associated with the rodent’s diet and use such information in subsequent search for prey. If snakes can discriminate between mice based on their diets, then they should prefer carcasses of mice that ate the same diet as the mouse struck. Methods Subjects The subjects were six prairie rattlesnakes that had experience in the above experiments. Snakes
484
Animal
Behaviour,
00, 0
had not been tested for about 30 days prior to the present experiment. Housing and maintenance conditions were as described previously.
60
Procedure
The strike and prey-choice procedures were the same as described in experiment 4. Snakes struck either the carcass of a mouse that had been eating cinnamon chow (see below, N = 3) or the carcass of a mouse that ate cocoa chow (see below, N= 3). All prey-choice tests were conducted 10 min after snakes struck prey; the envenomated mouse was discarded as before and snakes received a choice between a cinnamon carcass and a cocoa carcass (described below) confined in wire mesh bags as in experiment 4. Adult mice, Mus musculus, were used as stimuli and were housed four or five to a cage. They were provided with access to water and glass bowls containing powdered laboratory chow adulterated with either ground cinnamon (I % by weight) or Hershey’s cocoa (2% by weight). Each cage was supplied with 100 g of the appropriate diet on each of 2 consecutive days. Mice ate most of their chow but some of it was found distributed widely in the cages. On the afternoon of their second day with the cinnamon or cocoa diets, mice were killed and the carcasses were used as stimuli in either the strike or prey-choice procedures. The experimenter could detect cinnamon or cocoa odour on each carcass. Results and Discussion Figure 3 shows mean investigation scores (time and tongue flicks) for matching and non-matching carcasses during the prey-choice tests. Snakes spent significantly more time over the matching carcass than the non-matching one during the first 2-min interval (F,,s= 35.24, P~0.02). There was also a greater number of tongue flicks over the matching carcass than the non-matching carcass during the first 2 min (FI.s= 14.81, P~0.02). As in previous experiments, the preference for the matching carcass disappeared after the first 2 min of testing. The present experiment indicates that rodents acquired distinctive chemical cues from their diets. Mice may have acquired chemical cues from diets as a consequence of ingestion and/or through residual particles of food left on their integuments. Most importantly, rattlesnakes detected this chemical information during predatory strikes and used it during subsequent search for the prey. This
50 2 .2 =
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20& IO I
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3
2-min
intervals
4
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5
b
6
Figure 3. Mean (&SE) time spent investigating and number of tongue flicks directed at matching (m) and non-matching (0) carcasses during consecutive 2-min intervals of the prey-choice test. finding suggests a natural mechanism by which rodents might develop individual chemical identities that rattlesnakes could use during post-strike trail following. GENERAL
DISCUSSION
Rodent-specializing rattlesnakes rapidly formed chemical search images. The predatory strike provided initial access to the chemical cues, and the snakes retained some representation of this information for at least 60 min. Retention of the chemical preference over this delay presumably could facilitate location of the wounded rodent’s trail and eventual location of the carcass. It remains unclear how the chemical learning observed in the present experiments might interact with other mechanisms that support post-strike location of envenomated prey (Duvall et al. 1980; Lee & Chiszar, unpublished data). Rattlesnakes probably use several different cues at their disposal to trail prey following predatory strikes. Our data also show that rattlesnakes acquired strike-induced preferences for chemical cues of
Melter
& Chiszar:
Search
rodents feeding on different diets. Thus, it is conceivable that rattlesnakes make use of their chemical learning ability under natural circumstances. Rodents feeding on different materials probably possess different chemical cues that may be acquired and used by snakes during predation. We propose that the phenomenon reported in experiment 7 would also occur with rodents feeding on diets containing more natural fragrances (e.g. sage). The strike-release-trail strategy is an aspect of specialization upon rodent prey by rattlesnakes. Indeed, some researchers regard this behaviour as a sign of rodent specialization when it is seen in other taxa of venomous snakes (Shine & Covacevich 1983). Accordingly, until comparative data become available, we are hesitant to generalize our conclusions about chemical search images to taxa other than those practising the strike-release-trail strategy. Perhaps this chemical memory system is unique to these species.
ACKNOWLEDGMENTS
We thank the animal care facility of the Department of Psychology for the rodents used in these experiments. We also thank Dr B. G. Galef, Jr for several lively conversations that led to this line of work. Indeed, we have referred to these studies as demonstrating a capitalization upon the Galef effect by rattlesnakes (e.g. such terminology was used at the winter conference on Current Issues in Developmental Psychobiology, 1986). We thank Karl Kandler, Mary Jen and Oakland Salavea for help in gathering the data.
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(Received
7 March 1988; MS. number:
revised A5251
16 MU!,
I
I98R,