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Taste aversion learning in the bat, Carollia perspicillata
BEHAVIORAL AND NEURAL BIOLOGY 28, 236--242
(1980)
BRIEF REPORT Taste Aversion Learning in the Bat, Carollia perspicillata MARK P. TERK AND LEONARD GREEN L2 Department of Psychology, Washington University, St. Louis, Missouri 63130 Taste aversion learning was studied in a species of frugivorous bat, Carollia perspicillata. Over the course of conditioning, there was a marked reduction in consumption of the test food that was conditionally paired with injections of lithium chloride, and an increase in consumption of the alternative, "safe" food. No significant changes in food consumption were found with bats receiving either saline injections or no treatment. In addition, while all bats decreased their relative consumption of the test food during two-choice postconditioning tests as compared to pretests, the experimental (LiC1) subjects showed a significantly greater decrease. These results thus extend the comparative study of learned taste aversions to a different species of mammal.
The ability of animals to form specific aversions to foods that have been conditionally paired with illness produced by either X-irradiation, drugs, toxins, or rotation has been extensively investigated in the last decade (see Riley & Clarke, 1977, for a complete bibliography). While the overwhelming majority of these studies have been conducted on the laboratory rat, several other species are beginning to attract increasing attention (e.g., hawks: Brett, Hankins, & Garcia, 1976; coyotes and wolves: Gustavson, Kelly, Sweeney, & Garcia, 1976; ferrets: Rusiniak, Gustavson, Hankins, & Garcia, 1976; quail: Wilcoxon, Dragoin, & Kral, 1971; again, see Riley & Clarke, 1977). These studies indicate a species-typical relationship between the animal's food-gathering behaviors and the associability of various cues in such avoidance learning. For example, quail, which rely predominantly on vision in foraging, easily form aversions to visual aspects of food. In fact, such cues are more strongly associated with illness than are taste cues (Wilcoxon et al., 1971). The present i This paper is based upon a Master's thesis submitted by Mark Terk to the Department of Psychology of Washington University. We thank James Banks III who helped in the running of the experiment and Dr. James Simmons who generously provided the bats and the experimental facilities. 2 To whom requests for reprints should be addressed: Department of Psychology, Washington University, St. Louis, Mo. 63130. 236 0163 - 1047/80/020236-07502.00/0 Copyright @ 1980 by Academic Press, Inc. All rights of reproduction in any form reserved.
TASTE AVERSION LEARNING IN THE BAT
237
experiment is the first to demonstrate that a species of bat, Carollia perspicillata, can form an aversion to the taste of a specific food which has been conditionally paired with illness produced by intraperitoneal injection of lithium chloride. While the ability of certain species of bats to learn discriminations has been investigated (e.g,, Eptesicus fuscus, distance discriminations: Simmons, Howell, & Suga, 1975; Phyllostomatidae, olfactory discriminations: Schmidt, 1973; Anoura geoffroyi, visual pattern discriminations: Suthers & Chase, 1969), there is, at present, no published study examining the ability of bats to perform discriminations based on taste. Bats are widely distributed throughout the world. Indeed, they are more widely distributed than any mammalian taxonomic group other than man (Jespen, 1970). Their ecological diversity is high (837 species as of 1970; Jespen, 1970), and they differ considerably in their diets and foodgathering behaviors. The order of mammals comprising bats has been given the name Chiroptera, "wing-handed." The single family comprising the suborder Megachiroptera is the Pteropodidae, the flying foxes and their smaller relatives. These animals possess a keen visual system and feed on fruits and flowers. The other suborder, Microchiroptera, use sonar extensively. Although they have relatively poor vision (Novick, 1969), at least two species of echolocating bats, C. perspicillata and Phyllostomus hastatus, use vision as a passive surveillance system while resting, thus reducing the energy expenditure associated with scanning of the environment for echoes (Chase & Suthers, 1969). Additionally, range limitations of acoustic orientation may make visual detection of familiar landmarks especially useful to these frugivorous bats while finding their way to and from feeding sites. Microchiropterans differ considerably in their diets. Some eat insects captured in the air or on the ground, others eat fruit or the nectar from flowers, and still others eat small birds and mammals, including other bats. Since bats possess such ecological diversity they provide an interesting order of animals with which to relate interspecific comparisons. The present research is an initial attempt to demonstrate taste aversion learning in one species of bat as a beginning for the study of such interspecific comparisons. Twenty-nine C. perspicillata, a neotropical frugivorous bat captured in Panama, weighed between 14 and 17 g. Carollia are reportedly the most abundant species of bat in the American tropics. They were chosen since they may be introduced into captivity for prolonged periods of time. Furthermore, Porter (1978) has recently completed an extended behavioral study on this species. In order to prevent stress through heat and humidity loss, the animals were housed in groups in two stainless-steel cages, each measuring 1 x
238
T E R K AND GREEN
0.5 x 0.5 m. They were maintained on a reversed 12-hr dark/light cycle. During the darkness period (from 11:00 AM to 11:00 VM) five 25-W red incandescent lights were on. From 11:00 VM to 11:00 AM fluorescent lights were turned on and the red lights turned off by automatic timers. The temperature in the room fluctuated between 23 and 26°C, and the humidity ranged from 60 to 90%. A mixture of bananas, protein, and bone meal as well as a molasses-based "glop" were made available. The food, water, and glop were placed in plastic trays at the bottom of the cages. The animals were gradually adapted to a feeding schedule in which they were placed in individual cages measuring 25 x 75 x 25 cm, and given 45-min access to food in 5-cm-round by 2.5-cm-deep glass dishes at 1:00 VM daily. In the evening, the bats were fed banana with protein and bone meal in their home cages for 30 min. After the animals had adapted to this feeding regimen, four days of two-substance pretests were administered. The bats were offered a 45-rain simultaneous choice between Gerbers Junior Pears and Junior Apricots. Each food was placed in separate glass dishes and alternated left-right positions daily. Following these pretests, each bat was randomly assigned to one of five groups with an attempt to equalize the groups on the basis of their pretest preference scores. On test days, each bat was offered its more preferred food for 45 rain. On nontest days, bats were given their less preferred, " s a f e " food. Test days were administered 2 to 5 days apart. The number of safe days was randomly varied providing ample time for the bats to recover from the previous test session. Two experimental groups, a high-dose (0.35 M LiC1) Lithium group (N = 6) and a low-dose (0.20 M LiC1) Lithium group (N = 5) received a 2% body wt ip injection of lithium chloride following the feeding session on each test day. The Saline group (N = 8) received an ip injection of physiological (0.9%) saline at 2% body wt on these test days. The NoTreatment control group (N = 5) did not receive any injections but were otherwise subject to the same experimental procedures. A third control group, the Sodium group (N = 5) received an ip injection at 2% body wt of 0.35 M NaC1 after test-day food consumption in an attempt to discern whether any subsequent aversions might be related to the high concentration of salt used rather than to the illness-producing effect of the lithium chloride itself. These procedures were continued for a total of 12 test days. Five days following the final test session, two-choice preference posttests identical to those given as pretests were administered for 4 days. Animals were weighed daily to the nearest 0.1 g and food consumption was measured to the nearest 0.01 g. The relative amount of the test food consumed during conditioning was obtained by dividing the amount of food consumed on the test day by the sum of the amount consumed of the safe food on the previous day plus consumption on the test day. Figure 1 presents the mean relative food
TASTE AVERSION LEARNING IN THE BAT
239
consumption for each group for each test session. Values below 0.50 indicate less test-food consumption than safe-food consumption. Both Lithium groups showed a steady decline in relative test-food consumption throughout the test sessions. In addition, there appears to be little difference in the rate of decline between the two Lithium groups. Due to the high mortality rate in the Sodium group it is discarded from all subsequent statistical analyses. Furthermore, the high-dose Lithium group (0.35 M LiC1) also suffered a high mortality rate and the remaining two animals were combined with the low-dose lithium group (0.20 M LiC1) for further analyses. An autopsy was performed on one of the bats which died prior to receiving an injection. Cause of death was attributed to stress arising from changes in its environment. These bats are quite sensitive to lowering of temperature which would arise from their transfer from the group cage to individual testing chambers. An overall split-plot analysis of variance was performed on the relative food consumption with groups as the between factor and trial blocks the within factor. For purposes of a linear trend analysis, test d'ays were grouped into four trial blocks of 3 days each. The analysis revealed a significant main effect for groups (F(3,16) = 34.09, p < .0001) and trial blocks (F(3,48) = 19.89, p < .001) and a significant linear trend only in the Lithium group (F(1,3) = 49.96, p < .01) with no other reliable trends in any of the other groups. Clearly, only the Lithium (Illness) group showed a reliable decrease in relative consumption of the test food over the course of conditioning. Figure 2 shows the absolute amount of food consumed on test and safe days for each treatment group. A reliable three-way interaction of groups by absolute amount of safe/test food consumed by trial blocks was obtained. The Lithium groups showed a significant positive linear trend (F(1,16) = 20.87, p < .001) in amount of safe food consumed across blocks of trials and, of course, a significant downward linear trend (F(1,16) = 66.52, p < .0001) was obtained for the amount of test food O-O Saline iN:B) No Treatment(N:5) Sodium (N :2) O--O High-Dose Lithium N~2) t.-Q Low-Dose Lithium N=4}
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FIG. 1. Mean relative consumption of the test food during conditioning for each group of bats.
240
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FIG. 2. Mean absolute amount of test food consumed on each of the test sessions (solid line) and safe food consumed on the previous safe day (dotted line) for each of the groups. c o n s u m e d across sessions. No reliable trends were obtained for the absolute a m o u n t of safe or test food c o n s u m e d in the Saline or N o - T r e a t m e n t control group. Two-choice, 45-min simultaneous preference tests between the two foods were conducted for 4 days prior to and following the experimental test sessions. Relative preference was obtained by dividing the amount c o n s u m e d of the test food by the total amount of the test plus safe foods c o n s u m e d on each preference test day. One high-dose lithium animal died 1 day prior to the start of the post-tests. The a u t o p s y revealed no evidence of pathology in the blood or in any of the organs examined. It was suggested that a spider bite might have been the possible cause of death. Thus, only five experimental animals were available for post-test scores. Figure 3 shows the m e a n relative preference scores for each group on both the preexperimental and postexperimental preference tests. All Z.8 _o
8.4
'~,2 PRE POST Lithium (N:5)
PRE POST Sahne (N:8)
PRE POST No-Treatment (N:5)
PRE POST Sodium (N:2)
FI6. 3. Meanrelative consumption of the test food during pre- and postpreference tests for each group.
TASTE AVERSION LEARNING IN THE BAT
241
groups showed a decrease in post-test relative consumption of the initially preferred food. Much more striking, however, is the dramatic reversal in relative preference for the Lithium group. A split-plot analysis of variance with groups as the between factor and pre/post-test preference scores as the within factor yielded a reliable overall effect (F(1,15) = 5.68,p < .05). Simple main effects tests revealed that the groups did not differ from each other on pretest scores (F < 1) but did, however, differ from each other on the postexperimental test scores (F(1,15) = 7.18, p < .025). A reliable difference between the Saline vs No-Treatment groups in their postexperimental test scores was obtained (F(1,15) = 5.50, p < .05). The significant difference found between preand postexperimental preference scores across all groups in part reflects the differential experience the subjects had with the safe food. The bats were given 2 to 5 safe days followed by 1 test day, and this schedule was repeated 12 times. The greater experience with the safe food might thus account for this change in preference. In addition, the fact that the saline-injected animals showed a higher relative preference for the test food than did the No-Treatment group indicates that the injection, per se, cannot account for the markedly decreased consumption by the Illness group. Thus, the aversion was specific to the taste and not attributable to the injection as such. Most important, however, the Lithium group, which received pairings of the test food with LiC1 injections, showed a significantly greater reduction in post-test preference scores than did the average of the two control groups (F(1,15) = 8.76, p < .01). The present results thus demonstrate that bats of the species C. perspicillata are capable of forming a conditioned taste aversion to a specific food which has been conditionally associated with illness induced by lithium chloride injections. In addition, these results extend the comparative study of conditioned taste aversions to another, more esoteric mammal, and the parameters established throughout the course of this experiment may be of use in studies concerned with interspecific comparisons of food aversion learning. Rozin and Kalat (1971) have stressed the importance of regarding behavior within an adaptive-evolutionary framework: We propose to treat learning and memory as any other biological characteristic, subject to natural selection and therefore adapted to handle specific types of problems. Insofar as an important environmental problem (e.g., obtaining adequate foods) presents unique demands or contingencies, we would expect to find appropriate modifications of learning and memory abilities, closely articulated with one another and with the natural behavior of the organism. (pp. 459-460)
The heuristic value of such a perspective can best be highlighted by considering the types of predictions that might be made with regard to whether the relative associability of various food cues (e.g., taste, color, sound, odor) varies with the natural foraging behavior of different species
242
TERK AND GREEN
of bat. For example, since Carollia use vision as a passive surveillance system and can visually detect and avoid obstacles in their flight path when deafened (Chase & Suthers, 1969), it would be of interest to assess the relative saliency of visual and auditory cues in their food-avoidance behaviors. For comparative purposes, it would also be valuable to investigate these parameters in another well-studied, but ecologically distinct bat, the insectivorous E. fuscus which relies upon echolocation in its food-gathering (Simmons, Fenton, & O'Farrell, 1979). Accordingly, one might predict that the more salient cue for Carollia would be visual whereas auditory cues would assume overriding importance for Eptesicus. Finally, these results suggest a possible approach in attenuating vampire bat attack upon resting cattle and the concomitant spread of rabies in this important food source. REFERENCES Brett, L. P., Hankins, W. G., & Garcia, J. (1976). Prey-lithium aversions III: Bueto hawks. Behavioral Biology, 17, 87-98. Chase, J., & Suthers, R. A. (1969). Visual obstacle avoidance by echolocating bats. Animal Behavior, 17, 201-207. Gustavson, C. R., Kelly, D. L., Sweeney, M., & Garcia, J. (1976). Prey-lithium aversions I: Coyotes and wolves. Behavioral Biology, 17, 61-72. Jespen, G. L. (1970). Bat origins and evolution. In W. A. Wimsatt (Ed.), Biology of Bats, Vol. I, pp. 1-64. New York: Academic Press. Novick, A. (1969). The Worm of Bats. New York: Holt, Rinehart & Winston. Porter, F. L. (1978). Social Behavior and Acoustic Communication in the Bat, Carollia perspicillata. Unpublished doctoral dissertation, Washington University. Riley, A. L., & Clarke, C. M. (1977). Conditioned taste aversions: A bibliography. In L. M. Barker, M. R. Best, & M. Domjan (Eds.), Learning Mechanisms in Food Selection, pp. 592-616. Waco, Texas: Baylor Univ. Press. Rozin, P., & Kalat, J. W. (1971). Specific hungers and poison avoidance as adaptive specializations of learning. Psychological Review, 78, 459-486. Rusiniak, K. W., Gustavson, C. R., Hankins, W. G., & Garcia, J. (1976). Prey-lithium aversions II: Laboratory rats and ferrets. Behavioral Biology, 17, 73-85. Schmidt, U. (1973). Olfactory threshold and odour discrimination of the vampire bat (Desmodus rotundus). Periodicum Biologorum, 75, 89-93. Simmons, J. A., Howell, D., & Suga, N. (1975). Information content of bat sonar echoes. American Scientist, 63, 204-215. Simmons, J. A., Fenton, M. G., & O'Farrell, M. J. (1979). Echolocation and pursuit of prey by bats. Science, 203, 16-21. Suthers, R. A., & Chase, J. (1969). Visual form discrimination by echolocating bats. The Biological Bulletin, 137, 535-546. Wilcoxon, H. C., Dragoin, W. B., & Kral, P. A. (1971). Illness-induced aversions in rat and quail: Relative salience of visual and gustatory cues. Science, 171, 826-828.
(1980)
BRIEF REPORT Taste Aversion Learning in the Bat, Carollia perspicillata MARK P. TERK AND LEONARD GREEN L2 Department of Psychology, Washington University, St. Louis, Missouri 63130 Taste aversion learning was studied in a species of frugivorous bat, Carollia perspicillata. Over the course of conditioning, there was a marked reduction in consumption of the test food that was conditionally paired with injections of lithium chloride, and an increase in consumption of the alternative, "safe" food. No significant changes in food consumption were found with bats receiving either saline injections or no treatment. In addition, while all bats decreased their relative consumption of the test food during two-choice postconditioning tests as compared to pretests, the experimental (LiC1) subjects showed a significantly greater decrease. These results thus extend the comparative study of learned taste aversions to a different species of mammal.
The ability of animals to form specific aversions to foods that have been conditionally paired with illness produced by either X-irradiation, drugs, toxins, or rotation has been extensively investigated in the last decade (see Riley & Clarke, 1977, for a complete bibliography). While the overwhelming majority of these studies have been conducted on the laboratory rat, several other species are beginning to attract increasing attention (e.g., hawks: Brett, Hankins, & Garcia, 1976; coyotes and wolves: Gustavson, Kelly, Sweeney, & Garcia, 1976; ferrets: Rusiniak, Gustavson, Hankins, & Garcia, 1976; quail: Wilcoxon, Dragoin, & Kral, 1971; again, see Riley & Clarke, 1977). These studies indicate a species-typical relationship between the animal's food-gathering behaviors and the associability of various cues in such avoidance learning. For example, quail, which rely predominantly on vision in foraging, easily form aversions to visual aspects of food. In fact, such cues are more strongly associated with illness than are taste cues (Wilcoxon et al., 1971). The present i This paper is based upon a Master's thesis submitted by Mark Terk to the Department of Psychology of Washington University. We thank James Banks III who helped in the running of the experiment and Dr. James Simmons who generously provided the bats and the experimental facilities. 2 To whom requests for reprints should be addressed: Department of Psychology, Washington University, St. Louis, Mo. 63130. 236 0163 - 1047/80/020236-07502.00/0 Copyright @ 1980 by Academic Press, Inc. All rights of reproduction in any form reserved.
TASTE AVERSION LEARNING IN THE BAT
237
experiment is the first to demonstrate that a species of bat, Carollia perspicillata, can form an aversion to the taste of a specific food which has been conditionally paired with illness produced by intraperitoneal injection of lithium chloride. While the ability of certain species of bats to learn discriminations has been investigated (e.g,, Eptesicus fuscus, distance discriminations: Simmons, Howell, & Suga, 1975; Phyllostomatidae, olfactory discriminations: Schmidt, 1973; Anoura geoffroyi, visual pattern discriminations: Suthers & Chase, 1969), there is, at present, no published study examining the ability of bats to perform discriminations based on taste. Bats are widely distributed throughout the world. Indeed, they are more widely distributed than any mammalian taxonomic group other than man (Jespen, 1970). Their ecological diversity is high (837 species as of 1970; Jespen, 1970), and they differ considerably in their diets and foodgathering behaviors. The order of mammals comprising bats has been given the name Chiroptera, "wing-handed." The single family comprising the suborder Megachiroptera is the Pteropodidae, the flying foxes and their smaller relatives. These animals possess a keen visual system and feed on fruits and flowers. The other suborder, Microchiroptera, use sonar extensively. Although they have relatively poor vision (Novick, 1969), at least two species of echolocating bats, C. perspicillata and Phyllostomus hastatus, use vision as a passive surveillance system while resting, thus reducing the energy expenditure associated with scanning of the environment for echoes (Chase & Suthers, 1969). Additionally, range limitations of acoustic orientation may make visual detection of familiar landmarks especially useful to these frugivorous bats while finding their way to and from feeding sites. Microchiropterans differ considerably in their diets. Some eat insects captured in the air or on the ground, others eat fruit or the nectar from flowers, and still others eat small birds and mammals, including other bats. Since bats possess such ecological diversity they provide an interesting order of animals with which to relate interspecific comparisons. The present research is an initial attempt to demonstrate taste aversion learning in one species of bat as a beginning for the study of such interspecific comparisons. Twenty-nine C. perspicillata, a neotropical frugivorous bat captured in Panama, weighed between 14 and 17 g. Carollia are reportedly the most abundant species of bat in the American tropics. They were chosen since they may be introduced into captivity for prolonged periods of time. Furthermore, Porter (1978) has recently completed an extended behavioral study on this species. In order to prevent stress through heat and humidity loss, the animals were housed in groups in two stainless-steel cages, each measuring 1 x
238
T E R K AND GREEN
0.5 x 0.5 m. They were maintained on a reversed 12-hr dark/light cycle. During the darkness period (from 11:00 AM to 11:00 VM) five 25-W red incandescent lights were on. From 11:00 VM to 11:00 AM fluorescent lights were turned on and the red lights turned off by automatic timers. The temperature in the room fluctuated between 23 and 26°C, and the humidity ranged from 60 to 90%. A mixture of bananas, protein, and bone meal as well as a molasses-based "glop" were made available. The food, water, and glop were placed in plastic trays at the bottom of the cages. The animals were gradually adapted to a feeding schedule in which they were placed in individual cages measuring 25 x 75 x 25 cm, and given 45-min access to food in 5-cm-round by 2.5-cm-deep glass dishes at 1:00 VM daily. In the evening, the bats were fed banana with protein and bone meal in their home cages for 30 min. After the animals had adapted to this feeding regimen, four days of two-substance pretests were administered. The bats were offered a 45-rain simultaneous choice between Gerbers Junior Pears and Junior Apricots. Each food was placed in separate glass dishes and alternated left-right positions daily. Following these pretests, each bat was randomly assigned to one of five groups with an attempt to equalize the groups on the basis of their pretest preference scores. On test days, each bat was offered its more preferred food for 45 rain. On nontest days, bats were given their less preferred, " s a f e " food. Test days were administered 2 to 5 days apart. The number of safe days was randomly varied providing ample time for the bats to recover from the previous test session. Two experimental groups, a high-dose (0.35 M LiC1) Lithium group (N = 6) and a low-dose (0.20 M LiC1) Lithium group (N = 5) received a 2% body wt ip injection of lithium chloride following the feeding session on each test day. The Saline group (N = 8) received an ip injection of physiological (0.9%) saline at 2% body wt on these test days. The NoTreatment control group (N = 5) did not receive any injections but were otherwise subject to the same experimental procedures. A third control group, the Sodium group (N = 5) received an ip injection at 2% body wt of 0.35 M NaC1 after test-day food consumption in an attempt to discern whether any subsequent aversions might be related to the high concentration of salt used rather than to the illness-producing effect of the lithium chloride itself. These procedures were continued for a total of 12 test days. Five days following the final test session, two-choice preference posttests identical to those given as pretests were administered for 4 days. Animals were weighed daily to the nearest 0.1 g and food consumption was measured to the nearest 0.01 g. The relative amount of the test food consumed during conditioning was obtained by dividing the amount of food consumed on the test day by the sum of the amount consumed of the safe food on the previous day plus consumption on the test day. Figure 1 presents the mean relative food
TASTE AVERSION LEARNING IN THE BAT
239
consumption for each group for each test session. Values below 0.50 indicate less test-food consumption than safe-food consumption. Both Lithium groups showed a steady decline in relative test-food consumption throughout the test sessions. In addition, there appears to be little difference in the rate of decline between the two Lithium groups. Due to the high mortality rate in the Sodium group it is discarded from all subsequent statistical analyses. Furthermore, the high-dose Lithium group (0.35 M LiC1) also suffered a high mortality rate and the remaining two animals were combined with the low-dose lithium group (0.20 M LiC1) for further analyses. An autopsy was performed on one of the bats which died prior to receiving an injection. Cause of death was attributed to stress arising from changes in its environment. These bats are quite sensitive to lowering of temperature which would arise from their transfer from the group cage to individual testing chambers. An overall split-plot analysis of variance was performed on the relative food consumption with groups as the between factor and trial blocks the within factor. For purposes of a linear trend analysis, test d'ays were grouped into four trial blocks of 3 days each. The analysis revealed a significant main effect for groups (F(3,16) = 34.09, p < .0001) and trial blocks (F(3,48) = 19.89, p < .001) and a significant linear trend only in the Lithium group (F(1,3) = 49.96, p < .01) with no other reliable trends in any of the other groups. Clearly, only the Lithium (Illness) group showed a reliable decrease in relative consumption of the test food over the course of conditioning. Figure 2 shows the absolute amount of food consumed on test and safe days for each treatment group. A reliable three-way interaction of groups by absolute amount of safe/test food consumed by trial blocks was obtained. The Lithium groups showed a significant positive linear trend (F(1,16) = 20.87, p < .001) in amount of safe food consumed across blocks of trials and, of course, a significant downward linear trend (F(1,16) = 66.52, p < .0001) was obtained for the amount of test food O-O Saline iN:B) No Treatment(N:5) Sodium (N :2) O--O High-Dose Lithium N~2) t.-Q Low-Dose Lithium N=4}
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FIG. 1. Mean relative consumption of the test food during conditioning for each group of bats.
240
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FIG. 2. Mean absolute amount of test food consumed on each of the test sessions (solid line) and safe food consumed on the previous safe day (dotted line) for each of the groups. c o n s u m e d across sessions. No reliable trends were obtained for the absolute a m o u n t of safe or test food c o n s u m e d in the Saline or N o - T r e a t m e n t control group. Two-choice, 45-min simultaneous preference tests between the two foods were conducted for 4 days prior to and following the experimental test sessions. Relative preference was obtained by dividing the amount c o n s u m e d of the test food by the total amount of the test plus safe foods c o n s u m e d on each preference test day. One high-dose lithium animal died 1 day prior to the start of the post-tests. The a u t o p s y revealed no evidence of pathology in the blood or in any of the organs examined. It was suggested that a spider bite might have been the possible cause of death. Thus, only five experimental animals were available for post-test scores. Figure 3 shows the m e a n relative preference scores for each group on both the preexperimental and postexperimental preference tests. All Z.8 _o
8.4
'~,2 PRE POST Lithium (N:5)
PRE POST Sahne (N:8)
PRE POST No-Treatment (N:5)
PRE POST Sodium (N:2)
FI6. 3. Meanrelative consumption of the test food during pre- and postpreference tests for each group.
TASTE AVERSION LEARNING IN THE BAT
241
groups showed a decrease in post-test relative consumption of the initially preferred food. Much more striking, however, is the dramatic reversal in relative preference for the Lithium group. A split-plot analysis of variance with groups as the between factor and pre/post-test preference scores as the within factor yielded a reliable overall effect (F(1,15) = 5.68,p < .05). Simple main effects tests revealed that the groups did not differ from each other on pretest scores (F < 1) but did, however, differ from each other on the postexperimental test scores (F(1,15) = 7.18, p < .025). A reliable difference between the Saline vs No-Treatment groups in their postexperimental test scores was obtained (F(1,15) = 5.50, p < .05). The significant difference found between preand postexperimental preference scores across all groups in part reflects the differential experience the subjects had with the safe food. The bats were given 2 to 5 safe days followed by 1 test day, and this schedule was repeated 12 times. The greater experience with the safe food might thus account for this change in preference. In addition, the fact that the saline-injected animals showed a higher relative preference for the test food than did the No-Treatment group indicates that the injection, per se, cannot account for the markedly decreased consumption by the Illness group. Thus, the aversion was specific to the taste and not attributable to the injection as such. Most important, however, the Lithium group, which received pairings of the test food with LiC1 injections, showed a significantly greater reduction in post-test preference scores than did the average of the two control groups (F(1,15) = 8.76, p < .01). The present results thus demonstrate that bats of the species C. perspicillata are capable of forming a conditioned taste aversion to a specific food which has been conditionally associated with illness induced by lithium chloride injections. In addition, these results extend the comparative study of conditioned taste aversions to another, more esoteric mammal, and the parameters established throughout the course of this experiment may be of use in studies concerned with interspecific comparisons of food aversion learning. Rozin and Kalat (1971) have stressed the importance of regarding behavior within an adaptive-evolutionary framework: We propose to treat learning and memory as any other biological characteristic, subject to natural selection and therefore adapted to handle specific types of problems. Insofar as an important environmental problem (e.g., obtaining adequate foods) presents unique demands or contingencies, we would expect to find appropriate modifications of learning and memory abilities, closely articulated with one another and with the natural behavior of the organism. (pp. 459-460)
The heuristic value of such a perspective can best be highlighted by considering the types of predictions that might be made with regard to whether the relative associability of various food cues (e.g., taste, color, sound, odor) varies with the natural foraging behavior of different species
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of bat. For example, since Carollia use vision as a passive surveillance system and can visually detect and avoid obstacles in their flight path when deafened (Chase & Suthers, 1969), it would be of interest to assess the relative saliency of visual and auditory cues in their food-avoidance behaviors. For comparative purposes, it would also be valuable to investigate these parameters in another well-studied, but ecologically distinct bat, the insectivorous E. fuscus which relies upon echolocation in its food-gathering (Simmons, Fenton, & O'Farrell, 1979). Accordingly, one might predict that the more salient cue for Carollia would be visual whereas auditory cues would assume overriding importance for Eptesicus. Finally, these results suggest a possible approach in attenuating vampire bat attack upon resting cattle and the concomitant spread of rabies in this important food source. REFERENCES Brett, L. P., Hankins, W. G., & Garcia, J. (1976). Prey-lithium aversions III: Bueto hawks. Behavioral Biology, 17, 87-98. Chase, J., & Suthers, R. A. (1969). Visual obstacle avoidance by echolocating bats. Animal Behavior, 17, 201-207. Gustavson, C. R., Kelly, D. L., Sweeney, M., & Garcia, J. (1976). Prey-lithium aversions I: Coyotes and wolves. Behavioral Biology, 17, 61-72. Jespen, G. L. (1970). Bat origins and evolution. In W. A. Wimsatt (Ed.), Biology of Bats, Vol. I, pp. 1-64. New York: Academic Press. Novick, A. (1969). The Worm of Bats. New York: Holt, Rinehart & Winston. Porter, F. L. (1978). Social Behavior and Acoustic Communication in the Bat, Carollia perspicillata. Unpublished doctoral dissertation, Washington University. Riley, A. L., & Clarke, C. M. (1977). Conditioned taste aversions: A bibliography. In L. M. Barker, M. R. Best, & M. Domjan (Eds.), Learning Mechanisms in Food Selection, pp. 592-616. Waco, Texas: Baylor Univ. Press. Rozin, P., & Kalat, J. W. (1971). Specific hungers and poison avoidance as adaptive specializations of learning. Psychological Review, 78, 459-486. Rusiniak, K. W., Gustavson, C. R., Hankins, W. G., & Garcia, J. (1976). Prey-lithium aversions II: Laboratory rats and ferrets. Behavioral Biology, 17, 73-85. Schmidt, U. (1973). Olfactory threshold and odour discrimination of the vampire bat (Desmodus rotundus). Periodicum Biologorum, 75, 89-93. Simmons, J. A., Howell, D., & Suga, N. (1975). Information content of bat sonar echoes. American Scientist, 63, 204-215. Simmons, J. A., Fenton, M. G., & O'Farrell, M. J. (1979). Echolocation and pursuit of prey by bats. Science, 203, 16-21. Suthers, R. A., & Chase, J. (1969). Visual form discrimination by echolocating bats. The Biological Bulletin, 137, 535-546. Wilcoxon, H. C., Dragoin, W. B., & Kral, P. A. (1971). Illness-induced aversions in rat and quail: Relative salience of visual and gustatory cues. Science, 171, 826-828.