ROGER N. JOHNSON,2 MICHAEL J. DESISTO, Jit.,3 AND ALLEN B. KOENIG4. Tufts University. Rats raised in social isolation from weaning showed ...
Journal of Comparative and Physiological Psychology 1972, Vol. 79, No. 2, 237-242
SOCIAL AND DEVELOPMENTAL EXPERIENCE1 AND INTERSPECIFIC AGGRESSION IN RATS ROGER N. JOHNSON,2 MICHAEL J. DESISTO, Jit.,3 AND ALLEN B. KOENIG 4 Tufts
University
Rats raised in social isolation from weaning showed significantly more interspecific aggressive behavior than littermates raised with peers as measured by the proportion initiating a killing attack against frogs in a 20-min. arena test. In six cross-species rearing conditions with frogs and cockroaches, rats failed to form social attachments and when tested individually they killed the alien species as often or more often than did controls. In a final experiment, a significant number of rats became killers only after witnessing aggression in other rats.
Rats raised in isolation fight the same ence has an important effect on adult social way as socially experienced rats (Eibl-Ei- behavior, and that mammals, birds, and besfeldt, 1961), and both wild and labora- even some insects can form strong social tory rats which fail to kill mice cannot be attachments to alien species or inanimate made to do so through starvation, adminis- objects if given appropriate socialization tration of painful electric shock, or allowing (Cairns, 1966a; Scott, 1968). The present experiments are designed to them to watch other rats attack mice (Karli, 1956, 1961). Such findings have test the behavioral effects of (a) social isobeen taken to support the view that aggres- lation, (b) cross-species rearing, and (c) sion in animals and even humans (Lorenz, exposure to killing. Because of the difficulty 1965, 1966) is innate, relatively stereo- of evaluating strength of aggressive motivatyped, and based more on phylogenetic ad- tion, many investigators have concentrated aptation than on learning. A contrasting on mouse killing by rats, however this re(but not mutually exclusive) approach has sponse is relatively weak as evidenced by been to emphasize ontogenetic adaptation the fact that only about 12% of domestiand social experience in the development of cated rats will kill mice, even after hours of adult aggressive behavior, particularly with exposure (Karli, 1956). In the following exregard to the probability of initiating an periments, rats are tested mainly with frogs attack and the choice of a victim. For ex- because (a) frog killing by rats has been ample, lack of peer experience during devel- established as a reliable response which opment frequently increases aggressiveness provides an objective measure of interspein adults, and in monkeys this aggressive- cific aggressive behavior (Bandler, 1969; ness may be directed at other monkeys DeSisto, 1970); (b) nearly all laboratory (Mason, 1960), an alien species (Mason & rats will attack frogs if tested in their home Green, 1962), or even themselves (Harlow cages (DeSisto & Huston, 1970), and the & Harlow, 1962). If cats are raised in a response is strong enough that it will also rat-killing environment, nearly all become take place in a standardized arena, which rat killers, but if they are exposed to rats makes it possible to compare the effects of from weaning to maturity, very few become different rearing conditions; and (c) the unrat killers (Kuo, 1930). Such findings are usual strength of the frog-killing response consistent with the view that early experi- provides a more stringent test for the modifiability of aggressive behavior while also 1 This research was supported by United States examining interspecific fighting between Public Health Service Grant MH-18404. distantly related species. 2 Requests for reprints should be sent to Roger N. Johnson, who is now at Ramapo College, Mahwah, New Jersey 07430. 3 Now at Colby College. 4 Now at the Universitv of Massachusetts.
237
EXPEEIMENT 1 Myer (1969) reported that social isolation from weaning to maturity failed to in-
238
R. N. JOHNSON, M. J. DESISTO, JR., AND A. B. KOENIG
crease interspecific aggression in rats as measured by the proportion of mouse killers. Experiment 1 reexamines this question by testing rats in a neutral arena rather than in home cages, and by using frogs as victims. Method Eighty-seven male Long-Evans rats were weaned at 18-22 days and thereafter maintained ad lib on water and laboratory chow. Fifty-seven rats were raised from weaning in community cages in groups of about 8 while 30 littermates were isolated in individual cages. At 95 days of age, all subjects were individually tested with live grass frogs (Rana pipiens) about 6-8 cm. in trunk length. Testing was carried out in an arena 38 X 18 X 40 cm., which had a hardware-cloth floor resting on a white surface. The walls were also painted white and the ceiling was clear Plexiglas to allow an overhead illumination of 1 ftc. on the floor. The apparatus was placed in a dark room flooded by white noise, and between sessions the floor of the apparatus was wiped down to remove moisture and scents from the previous tests. In general, efforts were made to maximize visibility within the apparatus while minimizing possible distractions by the observer. Testing began by placing a rat in the arena and allowing 30 min. for exploration and adaptation to the apparatus. A frog was then dropped into the apparatus as far from the rat as possible and stop watches were used to measure the latency of the initial attack. If no attack took place after 20 min., the session was arbitrarily terminated and both subjects removed. Considerable rat-frog contact usually took place, even when there were no attacks.
Results and Discussion Among isolated rats, 80.0% initiated attacks against frogs while only 49.1% of those raised with peers did so, a difference that is statistically significant (x2 = 7.79, p < .01). The effect of rearing conditions is also borne out by the attack latencies, which averaged 86 sec. for the isolates and 341 sec. for subjects housed in groups (rats which did not attack were excluded from latency scores). The failure of Myer (1969) to obtain a difference between isolated- compared to group-reared rats may be due to procedural variables such as the use of mouse killing as a test of aggressiveness, or the isolation of group-reared rats for 10 days before being individually tested with mice.
EXPERIMENT 2 The fact that socially isolated rats were more likely to attack and kill an alien species may be because they were prevented from forming attachments to other animals during development. In Kuo's (1930) experiment, 9 out of 20 isolated cats became rat killers, however no killing took place if cats and rats were raised together and only 3 of 18 of these cats killed other rats. More recently, it has been demonstrated that mouse killing by rats is sharply reduced if both species are raised together (Denenberg, Hudgens, & Zarrow, 1964; Myer, 1969). Experiment 2 was designed to test if crossspecies cohabitation during development reduces interspecific conflict between more distantly related species in which the aggressive response is relatively strong. Method Because of the unique problems involved in providing early experience with distantly related species, six rearing conditions were used with three designed for complete social exposure and three for partial or protected exposure. In the first four conditions the controls were 57 group-reared subjects from Experiment 1. The experimental animals (age, sex, and strain) and testing procedures were the same as those described in Experiment 1. The six rearing conditions were as follows: Group A. Six weanling rat pups were raised on an elevated platform in the middle of a partially filled bathtub containing six frogs. The platform measured 96.5 X 30.0 cm., which provided approximately the same floor space per animal as the control rats reared in group cages. Food and fresh water were available at all times on the platform and the bathtub water was frequently changed. The water level was maintained just below the platform surface so that frogs could easily climb onto it. Group B. Six weanling rats were raised in a group cage (37 X 18 X 38 cm.) that contained a shallow pan of water in which a frog was maintained. Group C. Twenty-four rats were raised from weaning to 95 days in groups of about 6. The community cages were identical to those in Group B except that instead of a pan of water there was an interior hardware-cloth cage 17 X 18 X 15 cm. that contained a frog and a small pan of water. These cages were continuously illuminated so that rats could easily see and smell the frog without touching it. Group D. Seventeen rats were raised in individual cages which contained a closed 2-pt. widemouth jar with a frog inside. In this group the frog
239
EXPERIENCE AND AGGRESSION IN RATS was the only other organism each rat saw from weaning to maturity. Group E. Twenty weanling rats were placed in two group cages along with four cockroaches (Gromphodorina portentosa). These unusually large cockroaches were only slightly smaller than the weanling pups in body length (about 5-6 cm.). Group F. Thirty weanling rats were raised in group cages which contained 2-qt. glass bottles each holding cockroaches (Periplaneta americana). Twenty nine littermate controls were raised in similar cages but without any exposure to cockroaches. At 55-60 days of age all rats were tested in the arena with the American cockroaches.
TABLE 1 RESULTS OF ARENA TESTS WITH COCKROACHEI (GBOUP F) AND WITH FROGS (ALL OTHER GROUPS) Rat rearing condition after weaning
% killers
Complete social isolation Raised with peers Group A: Raised with peers and with frogs on platform Group B: Raised with peers and with frogs in large cages Group C: Raised with peers and frogs with frogs protected Group D: Isolated rats raised with protected frogs Group F: Raised with peers and protected cockroaches Group F: Raised with peers, no exposure to cockroaches
80.0 49.1 80.0 100.0
76.9
Results and Discussion 84.1 Cohabitation became impossible in Groups A, B, and E because rats killed the 60.0 alien species. In Group E, weanling rats 82.8 killed and ate their cockroach cagemates during the first 24 hr. In Group A, the rats E was discontinued when weanand frogs initially coexisted and both spe- lingNote.—Group rats killed their cockroach cagemates during cies were often observed next to each other the first day. on the platform. When the rats were 50 days old, however, a frog skeleton was dis- .01). When individual rats were raised with covered and thereafter the frogs stayed in individual frogs (Group D), 16 out of 17 or the water. Rats began to patrol the edge of 94.1% attacked with a mean latency of 58 the platform in an effort to snare passing sec. Compared to subjects in Experiment 1 frogs, and they became so skillful that re- raised in individual cages with no exposure placement frogs were quickly captured and to frogs, a higher proportion (94.1% comdevoured (one rat drowned, apparently pared to 80.0%) became killers; however2 from falling off the platform while trying this difference fails to reach significance (x to catch a frog). After 75 days of age, frogs = 1.71, p > .10). In Group F, 24 of 29 rats which had were no longer replaced and rats did not see a frog again until 95 days when they were never seen cockroaches attacked them in individually tested in the arena. All but one the arena compared to 18 of 30 which had visual exposure from Days 20 to 55. The quickly (M = 85 sec.) attacked. 2 Similar results were obtained with Group difference, however, is not significant (x = B. Rats explored the frog but did not harm 3.72, p < .10). A summary of the results of it until they were 52 days old when they the first two experiments is presented in were observed chasing the frog through the Table 1. water pan after which they killed it. ReEXPERIMENT 3 placement frogs were also attacked and this It is clear from Experiment 2 that crossattempt at cross-species rearing had to be species cohabitation failed to reduce interabandoned. When later individually tested specific aggression and in one condition in the arena, all subjects were frog killers. (Group C) led to an increase. Experiment 3 In Group C, cohabitation from weaning was designed to test further whether social to maturity was assured by protecting the experience can modify aggressiveness and in frogs with an interior enclosure, but when particular what effect killer rats have on tested in the arena 19 of 24 or 76.9% atnonkiller rats. tacked with a mean latency of 25 sec. This is a significantly higher proportion of killers Method than the 49.1% of group-reared animals Adult male Long-Evans rats were screened for that had never seen frogs (x2 = 7.21, p < failure to attack frogs in two successive arena tests
240
R. N. JOHNSON, M. J. DESISTO, JR., AND A. B. KOENIG
on different days. These "pacifist" rats were assigned to either an experimental group (26 subjects) or a control group (13 subjects). The control rats were simply retested an additional four times on different days to see if repeated testing increased the proportion of killers. The experimental animals were placed in group cages where they could observe through a wire screen frogs being attacked by an established killer rat. After watching one or two attacks per day for a week, each rat was individually tested in the arena, and if no attack resulted the procedure was repeated a second week.
Results and Discussion Of the 13 control animals only 3 or 23.1% eventually attacked after a total of six sessions. Among the 26 experimental rats, 7 killed after the first week and another 8 after the second week for a total of 15 of 26 or 57.7% (x2 = 4.18, p < .05). The fact that observing killing significantly increased the proportion of killers was further supported by a final test with some of the remaining rats in both groups which still had not attacked a frog. Each was tested when 24-hr, food deprived, and again when satiated. Five out of six experimental subjects killed when hungry, and then continued to kill when satiated. Among the control animals, only 2 of 10 killed when hungry, and only these 2 continued to kill after satiation (x2 = 6.11, p < .02). GENERAL DISCUSSION Perhaps the most significant finding is the failure of rats to form social attachments to alien species with which they were raised from weaning. The absence of social bonds was demonstrated by a variety of conditions in Experiment 2 where most rats quickly attacked and killed species with which they had extensive social experience during development. These results are inconsistent with the conclusions of much previous research from which it has been concluded that social attachments are commonly found in many mammals, birds, and even insects, and that such attachments may take place to whatever is present in the environment whether it is rewarding, punishing, or indifferent (Scott, 1968; Scott & Fuller, 1965). Cross-species attachments have been demonstrated between many species including rats and cats (Kuo, 1930;
McDougall & McDougall, 1927), rats and monkeys (Mason & Green, 1962), rats and mice (Denenberg et al., 1964; Myer, 1969), cats and birds (Kuo, 1967), and lambs and dogs (Cairns, 1964). Several possibilities might be offered to help explain the lack of attachment behavior in Experiment 2. It could be argued that cohabitation after weaning misses the period of primary socialization when bonds are most easily formed. But attachments can be formed in later stages (Scott, 1962), and cohabitation following weaning has been successful in other experiments with rats (Myer, 1969). Another possibility is that social attachments may not take place when species are separated by barriers. For example, there is evidence that the adrenocortical response of mice reared with rats does not take place if the species are separated by a wire-mesh barrier (Denenberg, Paschke, Zarrow, & Rosenberg, 1969). But it has also been reported (King, 1957) that mice isolated from each other by wire screens do not differ in agonistic behavior from group-reared mice, and that attachments can be formed even if there is no physical contact (Gray, 1960). In Experiment 2, wire and glass barriers were used only because killing, not attachments, resulted from direct social contact. Finally, it may be argued that social attachments are facilitated by emotional arousal (Scott, 1962), and that such arousal in turn is influenced by stimulus similarity. It is not that dissimilar species fail to attend to each other, but rather that they fail to get emotionally involved. Many animals quickly detect and attack an alien species, but often this is better characterized as predation. In acquiring a meal there may be a minimum of emotional involvement, as was the case with rats which had extensive social experience with frogs. When finally allowed access to frogs they displayed little emotionality and often began eating their victim without bothering to kill it first. Whether killing is predatory or aggressive may depend on developmental experience as well as on the species involved, for either type of killing may be intraspecific or interspecific (Johnson, 1972). This is evidenced by the fact that isolated rats be-
EXPERIENCE AND AGGRESSION IN RATS
came highly emotional (i.e., freezing, crouching, defecating) when confronted with a frog, and their attacks were usually frenzied pursuits consumated with a deadly bite on the neck. Following the kill, many of the isolates retreated to a corner and made no attempt to eat their victim. It might be hypothesized that highly dissimilar animals tend to ignore each other or else engage in predatory behavior, and in either case emotional involvement is minimal which reduces the likelihood of attachment formation. Nonpredatory social fighting does involve emotionality, but in general this type of agonistic behavior tends to decrease the more dissimilar the species (Fisher, 1964). But the lack of stimulus similarity and emotional arousal between rats and frogs cannot be a complete explanation for the absence of attachment behavior, for there is considerable evidence that attachments can take place with stationary and inanimate objects. This has been demonstrated in monkeys (Harlow, 1958), dogs (Igel & Calvin, 1960), lambs (Cairns, 1966b), and chicks (Gray, 1960). While social experience had little effect in Experiment 2, it did modify aggressive behavior in Experiments 1 and 3. It is well known that isolated rats are more vicious and difficult to handle than group-reared rats (Hatch, Balazs, Wiberg, & Grice, 1963), and Experiment 1 showed that they are also more likely to attack an alien species (although Myer, 1969, did not obtain this effect between rats and mice). Social restriction during development also increases intraspecific fighting in many animals including cats, dogs, birds, fish (Kuo, 1967), and monkeys (Harlow & Harlow, 1962; Mason, 1960). But lack of peer experience may also reduce aggressiveness, particularly in genetically aggressive strains of mice (King & Gurney, 1954) and dogs (Fisher, 1955; Fuller & Clark, 1966; Scott & Fuller, 1965). It, therefore, appears that social isolation may either increase or decrease aggressiveness, and the exact effect depends in part on the genetically determined social behavior of the species. Experiment 3 found that observing killing increases the likelihood that some normally peaceful rats will become killers.
241
These findings are different from those of Karli (1961), who reported that adult rats which failed to kill mice did not become killers after watching killing. Karli (1956) also reported that most wild and domesticated rats which normally do not kill mice will starve to death rather than kill. In the present experiment, hunger induced frog killing in established nonkillers mainly if subjects had previously witnessed frog killing. These results are similar to those of Kuo (1930) who found that observing killing had a much stronger effect than hunger alone. It should be noted that the present findings as well as those of Kuo and others fail to explain all individual differences, for some rats become killers even if they have never witnessed killing, and others never kill, even if they have observed killing. In conclusion, it appears that some aspects of interspecific aggressive behavior can be modified by social and developmental experience while others cannot. No sweeping generalizations can be made, for the exact effect depends on a combination of social and genetic factors along with the particular species being tested. REFERENCES HANDLER, R. J., JR. Facilitation of aggressive behavior in the rat by direct cholinergic stimulation of the hypothalamus. Nature, 1969, 224, 1035-1036. CAIRNS, R. B. Social behavior changes by crossspecies rearing. American Psychologist, 1964, 19, 484. (Abstract) CAIRNS, R. B. Attachment behavior of mammals. Psychological Review, 1966, 73, 409-426. (a) CAIRNS, R. B. Development, maintenance, and extinction of social attachment behavior in sheep. Journal of Comparative and Physiological Psychology, 1966/62,298-306. (b) DENENBERQ, V. H., HTJDGENS, G. A., & ZARROW, M. X. Mice reared with rats: Modification of behavior by early experience with another species. Science, 1964, 143, 380-381. DENENBERG, V. H., PASCHKE, R., ZAHROW, M. X., & ROSENBERG, K. M. Mice reared with rats: Elimination of odors, vision, and audition as significant stimulus sources. Developmental Psychobiology, 1969, 2, 26-28. DsSisTO, M. J., JR. Hypothalamic mechanisms of killing behavior in the laboratory rat. Unpublished doctoral dissertation, Tufts University, 1970. DESISTO, M. J., JR., & HUSTON, J. P. Effect of territory on frog-killing by rats. Journal of General Psychology, 1970, 83, 179-184.
242
R. N. JOHNSON, M. J. DeSISTO, JR., AND A. B. KOENIG
EiBL-EiBESFELDT, I. The fighting behavior of animals. Scientific American, 1961, 205, 112-122. FISHEB, A. E. The effects of differential early treatment on the social and exploratory behavior of puppies. Unpublished doctoral dissertation, Pennsylvania State University, 1955. FISHER, J. Interspecific aggression. In J. D. Carthy & F. J. Ebling (Eds.), The natural history oj aggression. New York: Academic Press, 1964. FULLEB, J. L., & CLARK, L. D. Genetic and treatment factors modifying the postisolation syndrome in dogs. Journal oj Comparative and Physiological Psychology, 1966, 61, 251-257. GRAY, P. H. Evidence that retinal flicker is not a necessary condition of imprinting. Science, 1960,132,1834-1835. HATCH, A., BALAZS, T., WIBEHQ, G. S., & GBICE, H. C. Long-term isolation stress in rats. Science, 1963,142, 507. HARLOW, H. F. The nature of love. American Psychologist, 1958,13, 673-685. HABLOW, H. F., & HARLOW, M. K. Social deprivation in monkeys. Scientific American, 1962, 207, 136-146. IQEL, G. J., & CALVIN, A. D. The development of affectional responses in infant dogs. Journal oj Comparative and Physiological Psychology, 1960, 53, 302-305. JOHNSON, R. N. Aggression in man and animals. Philadelphia: W. B. Saunders, 1972. KARLI, P. The Norway rat's killing response to the white mouse: An experimental analysis. Behaviour, 1956, 10, 81-103. KARLI, P. Nouvelles donnees experimentales sur le comportement d'aggression interspecifique Rat-Souris. Journal de Physiologic, 1961, 53, 383-384. KING, J. A. Relationship between early social experience and adult aggressive behavior in inbred mice. Journal of Genetic Psychology, 1957, 90, 151-166.
KINO, J. A., & GTJBNEY, N. L. Effect of early social experience on adult aggressive behavior in C 57 BL/10 mice. Journal of Comparative and Physiological Psychology, 1954, 47, 326-330. Kuo, Z. Y. The genesis of the cat's response toward the rat. Journal of Comparative Psychology, 1930,11,1-35. Kuo, Z. Y. The dynamics of behavior development. New York: Random House, 1967. LORENZ, K. Evolution and modification of behavior. Chicago: University of Chicago Press, 1965. LOBENZ, K. On aggression. New York: Harcourt, Brace, & World, 1966. MASON, W. A. The effect of social restriction on the behavior of rhesus monkeys: I. Free social behavior. Journal of Comparative and Physiological Psychology, 1960, 53, 582-587. MASON, W. A., & GREEN, P. C. The effects of social restriction on the behavior of rhesus monkeys: IV. Responses to a novel environment and to an alien species. Journal of Comparative and Physiological Psychology, 1962, 55, 363-368. McDouGALL, W., & McDouGALL, K. Notes on instinct and intelligence in rats and cats. Journal of Comparative Psychology, 1927, 7, 145-175. MYEB, J. S. Early experience and the development of mouse killing by rats. Journal of Comparative and Physiological Psychology, 1969, 67, 46-49. SCOTT, J. P. Critical periods in behavioral development. Science, 1962, 138, 949-958. SCOTT, J. P. The process of primary socialization in the dog. In G. Newton & S. Levine (Eds.), Early experience and behavior. Springfield, 111.: Charles C Thomas, 1968. SCOTT, J. P., & FULLER, J. L. Genetics and the social behavior of the dog. Chicago: University of Chicago Press, 1965. (Received February 12, 1971)
