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The influence of females upon aggression in domesticated male rats (Rattus norvegicus)
Anim . Behav ., 1977, 25, 6 54-659
THE INFLUENCE OF FEMALES UPON AGGRESSION IN DOMESTICATED MALE RATS (RATT US NOR VEGICUS) BY
KEVIN FLANNELLY * & RICHARD LORE
Douglass College, Rutgers-The State University of New Jersey, New Brunswick, New Jersey
Abstract. The aggression of adult male Long-Evans rats (Rattus norvegicus), toward males of the same strain, was tested before and after a 1-week period of cohabitation with a pair of intact females, ovariectomized females, or intact males, comparable to the females in size . Only cohabitation with intact females increased the aggression of resident males against unfamiliar male intruders . Female enhancement of aggression does not appear to be caused by sexual frustration of males, or a function of dominance-subordinance relations, per se . Increased aggression may be mediated by elevated testosterone production associated with mating . Barnett, Evans & Stoddart (1968) reported that cohabitation with females increased the aggression of wild male rats (Rattus norvegicus) against unfamiliar males . Barnett & Stoddart (1969) replicated this finding with wild-trapped males but failed to find female enhancement of male aggression in animals laboratory-bred for several generations . Specifically, laboratoryreared males did not show the increased `threat' posturing and duration of attack against intruders, observed in wild-trapped males housed with females . Similarly, cohabitation with females apparently did little to enhance male aggression against intruders in mixed-sex colonies of albino rats observed by Barnett (1960) . In three of Barnett's albino colonies the display of aggression toward intruders was minimal and males failed to exhibit any threat posturing . An alternative interpretation of Barnett's findings of female enhancement of aggression is possible . Recent work indicates that only dominant members of cohabiting pairs of adult males attack intruders (Flannelly & Lore 1976) . The latter finding suggests that males residing with females are more aggressive simply because they are more likely to dominate smaller females . The increased aggression of a resident male may be the result of his ability to dominate smaller conspecifics regardless of sex . In this study, we compare the aggressive response of resident males toward intruders, after a period of resident cohabitation with either adult females or smaller adult males, comparable to the females in size . If aggression is enhanced specifically by the presence of females, then males residing with females should behave
much more aggressively toward intruders than male residents housed with smaller males, since residents in both living conditions should readily dominate their smaller cagemates. Because the enhancement of male aggression may yet be peculiar to the presence of females but not related to sexual receptivity, a third group of males was tested which were housed with ovariectomized females . Methods A total of 66 male and 24 female Long-Evans rats were purchased from the Marland Breeding Farm, Hewitt, New Jersey. Eighteen older males, weighing 419 to 642 g were designated resident males. The females and remaining males were comparable in size (245 to 379 g) at the start of the experiment . All animals were housed individually in standard Wahman hanging cages from their arrival at the laboratory until used experimentally . Food and water were freely available and a 12 :12 h light-dark cycle maintained during the experiment . Throughout the experiment resident males were housed in 42 x 66 x 26 . 5-cm cages made of galvanized steel with clear Plexiglas fronts and hardware-cloth floors . All testing was done in these cages . A 30 x 20 x 25-cm nesting cage was placed inside and secured to the floor of each test cage . Four 25-W bulbs illuminated the testing room to permit observation during the dark phase of the light cycle . Procedure Twelve randomly chosen females were ovariectomized under ether anaesthesia . A 2-week recovery period was interposed before testing . Aggression tests and colony formation . After 7 to 10 days of habituation to the laboratory
*Present address : Edward R . Johnstone Training and Research Center, Bordentown, New Jersey, 08505, U.S .A . 654
FLANNELLY & LORE : FEMALE INFLUENCE UPON MALE AGGRESSION
environment resident males were transferred to test cages on day 1, where they were housed individually for 7 days . The first aggression test was given on day 8 . A male intruder was placed with each resident and the behaviours of both animals recorded for the next 30 min . Each intruder remained with a resident for 24 h, after which time the intruder was sacrificed, body hair removed with clippers and skin carefully examined for wounds . The method of scoring of wounds is reported elsewhere (Luciano & Lore 1975). On day 13 each resident was removed from its cage and introduced to a different test cage accompanied by either two intact males, two intact females, or two ovariectomized females . In all, 18 colonies were established ; six of each
type. Each resident and its pair of cohabitants were introduced to a test cage simultaneously . The behaviour of all three animals was recorded and for the first 30 min of colony formation (Table I) and the colonies left undisturbed for 7 days . On day 20 an intruder was again placed into the cage of each resident and the second 24-h aggression test begun . Ten minutes before the introduction of an intruder, the two animals cohabiting with a resident were placed into the nesting cage where they were confined for the entire test session . As during the first aggression test, the interaction of resident and intruder was observed for the first 30 min of testing . Intruders were killed and examined for wounds following the 24-h session .
Table L Means (and Standard Deviations) of Social and Aggressive Measures of Cohabitants and Male Residents During the Initial 30 Min of Colony Formationt Type of colony Resident male with :
Intact females
Ovariectomized females
Intact males
Resident Behaviour toward cohabitants Duration of offensive postures (s)
6.5 (9 .0)
7 .2 (8 . 1)
1512 . 0 (521 . 5)
1295 . 0 (639 .8)
348 .0** (271 . 5)
Frequency of social-investigatory behaviour
98 .2 (43 .5)
78 . 0 (32 . 6)
22 . 0** (18 . 0)
Frequency of ano-genital sniffing
18 . 2 (20 . 8)
11 .7 (26 .8)
4.2 (15 . 3)
Frequency of mounts
14 . 5 (85 . 1)
9.8 (22 . 7)
1 .0 (4 . 5)
Duration of offensive postures (s)
1 .0 (3 . 8)
0.3 (1 .8)
11 .0 (39 . 7)
Duration of defensive postures (s)
9.5 (32 . 7)
27 . 2 (103 . 4)
98 . 3 (153 .2)
Frequency of social-investigatory behaviour
36 .3 (69 . 5)
26 . 0 (56 . 9)
10 .7 (16 . 9)
Frequency of offensive postures
3 .5 (11 . 2)
3 .3 (9 .2)
8 .7 (33 . 2)
Frequency of social-investigatory behaviours
18 . 8 (38 . 8)
20 . 2 (40 .3)
7 .3 (13 . 3)
Latency to fight (s)
655
90 . 8* (93 . 9)
Cohabitants behaviour toward residents
Cohabitants behaviour toward each other
*P<0 .05 . **P<0 . 01 . tSignificance levels represent overall differences between types of colonies .
656
ANIMAL BEHAVIOUR, 25, 3
Behavioural measures . The behaviour patterns recorded were taken principally from Grant & Mackintosh (1963) and are described by them . The total frequency of social-investigatory behaviour of each resident, cohabitant or intruder was recorded individually on digital counters during all observation sessions and a continuous description of all social and aggressive interaction between animals recorded on audio tape . The frequency and duration of each of six offensive and four defensive postures were recorded on an event recorder : `offensive postures' : aggressive groom, attack, offensive sideways, offensive upright, full aggressive, and offensive pinion or pinning ; (defensive postures) defensive upright, defensive sideways, submissive and defensive supine postures . Pinning and defensive supine posture are not described by Grant & Mackintosh (1963) . What the authors term pinning and defensive supine posturing, however, are depicted by Eibl-Eibesfeldt (1961, p. 120, illustration d) . In contrast with the submissive posture, the defensive supine posture is one of active defence, including kicking movements . Frequency of wrestling (see Sales 1972) was also recorded . A fight was defined as a continuous reciprocal sequence of offensive and defensive postures, beginning with the display of an aggressive act and terminating with one animal turning away from the other and engaging in a non-interactive activity . The
frequency and duration of fights and latency to first fight were recorded . Results First Aggression Test Though minimal in some instances, all residents displayed some aggressive behaviour and in no instance did an intruder defeat a resident. No resident exhibited distinctively defensive behaviour . One-way ANOVA's performed on the total duration and frequency of fights, latency to first fight, total duration of offensive posturing by residents, frequency of wrestling and intruder wound scores, revealed no statistically significant differences between the three groups of residents (see Table II) . These analyses were undertaken to confirm the assumption that no differences existed between groups prior to colony formation. Homosexual mounting of intruders was displayed by six of the 18 residents for a total of 14 observed mounts. Fights ranging in duration from 21 to 195 s immediately followed mounting by residents in four instances . Colony Formation Considerable differences between colony types (i .e . types of cohabitants) were observed in the interaction of residents with their cohabitants . during the initial 30 min of colony formation . A one-way ANOVA was performed on each of
Table II. Means (and Standard Deviations) of Aggressive Behaviour of Residents of Each Colony Type on the First and Second Aggression Tests Type of colony Aggression measure
Aggression Resident test male with :
Intact females
Ovariectomized females
Intact males
332 . 0 (108 . 9) 408 . 3 (624 . 7)
365 . 0 (172 . 5) 1004 . 0 (683 . 5)
512 .0 (634 . 8) 1140 .0 (798 .3)
Latency to first fight (s)
First Second
Frequency of fights
First Second
Total fight duration (s)
First Second
75 . 0 (120 . 7) 180 . 2 (171 . 6)*
71 . 8 (60.2) 60 . 7 (82 . 8)
90 .0 (92 . 2) 49 . 3 (97 .6)
Total duration of offensive postures (s)
First Second
85 . 0 (132 . 1) 166 . 5 (141 . 4)
76 . 7 (58 . 6) 66 . 5 (84 . 5)
106 .0 (119 . 0) 58 . 3 (105 . 1)
Frequency of wrestling
First Second
1 . 5 (1 . 1) 7 .0 (6 . 4)**
Intruder wound score
First Second
8 . 5 (8 . 1) 21-7 (47 . 9)**
*P<0 .05 ;
**P<0.01 .
2 .2 4.5
(1 . 2) (3 . 3)*
2.0 1 .7
2 .7 1-7
(1 . 3) (1 . 9)
1 .5 0.9
(0 . 8) (1 . 1)
(1 .9) (1 . 9)
3-3 1 .0
(2-8) (1 . 8)
7 . 3 (8-4) 8 . 0 (33 .4)
5 .0 1 .7
(5 . 3) (6 . 4)
FLANNELLY & LORE : FEMALE INFLUENCE UPON MALE AGGRESSION
the measures of social and aggressive behaviour of colony members presented in Table I . If no fighting occurred during the 30-min observation period fight latency was considered to be 1800 s . Latency to the first fight (F = 7. 61 ; df = 2, 15 ; P < 0 .01) resident total duration of offensive postures (F=3-94 ; df = 2, 15 ; P<0-05) and frequency of social-investigatory behaviour of residents toward cohabitants (F = 7 . 11 ; df = 2, 15 ; P < 0. 01) differed significantly across colonies . Five of the six residents which received intact females exhibited mounting toward one or both cohabitants. Intact females were housed individually, after the completion of the experiment to determine if they had become pregnant during cohabitation . Females from four of the six colonies (seven of the 12 intact females) gave birth . Second Aggression Test Differences between the aggression score of each resident on the first and second test were calculated and one-way ANO VA's performed on these difference scores for various measures . Table II presents the means and standard deviations of several measures of resident aggression on the first and second tests . All residents housed with intact females displayed increases over their first test scores on most aggression measures . Few animals housed with intact males or ovariectomized females increased, and most decreased in aggressiveness toward intruders . Frequency of wrestling with intruders differed significantly across types of colonies (F = 6 .82 ; df= 2, 15 ; P < 0.01) . Comparisons between colony types revealed that residents housed with intact females showed significantly greater increases in total fight duration (F = 5 . 17 ; df = 1, 15 ; P < 0 . 05) and frequency of fights (F = 6 . 98 ; df = 1, 15 ; P < 0 . 05) than residents housed with males or ovariectomized females . Although differences in resident total duration of offensive postures were not significant, residents housed with intact females showed a significant increase in duration of full aggressive (F = 5 . 86 ; df = 1, I5 ; P < 0 .05) and offensive sideways postures (F= 13 . 48 ; df = 1, 15 ; P < 0. 01), in comparison with residents of the other two types of colonies . A single intruder exposed to a resident housed with females was killed and extensively cannabalized. Wound scores were therefore analysed non-parametrically (Kruskal-Wallis analysis of variance by ranks) . Intruder wound scores were found to differ significantly across types of
657
colonies (H = 39 .6, df = 2, P < 0.01) . Resident mounting of intruders was observed in only one instance, by a resident housed with males . Discussion The results demonstrate that female cohabitation with males enhances male aggression against intruders in domesticated rats . Residents housed with intact females fought intruders significantly more frequently, and with greater intensity and severity than residents housed with intact males or ovariectomized females (see Table II) . Enhancement of male aggression is specific to the presence of females and does not appear to be only a function of dominance-subordinance relations among colony members . Residents housed with ovariectomized females or smaller intact males did not display increased aggression . Flannelly & Lore (1976) have previously suggested that the achievement of dominance within a colony might increase the aggression of the dominant colony member against intruders. Therefore, female enhancement of male aggression, as reported by Barnett et al . (1968, 1969), might be due to the fact that colony males were dominant over female cohabitants. Here the selection of comparably sized male and female cohabitants, which were considerably smaller than resident males, was intended to insure the dominance status of residents within both like-sex and mixed-sex colonies . Though residents substantially dominated male cohabitants during colony formation (see Table I), resident aggression against intruders was not increased by cohabitation with males. The results of the present study are in accord with the findings of Barnett et al . (1968, 1969) that cohabitation with females enhances male aggression . The present study, moreover, extends the generality of this finding to include domesticated rats . An earlier study by Thor & Flannelly (1976) failed to find increased male aggression following cohabitation with females . In that study, however, pre-cohabitation aggression scores of male colony members were extremely low . Apparently, exposure of males to females in adulthood does not necessarily enhance aggression unless sufficiently high aggression levels are already present . Taylor (1975) has reported that very brief exposure of a male to an inaccessible receptive female produces an immediate tendency to approach a submissive male . This finding need not, however, represent the active seeking of a
658
ANIMAL BEHAVIOUR, 25, 3
meagre opponent or aggressive target by a dominant male, as suggested by Taylor. More reasonably, Taylor's males may have been actively seeking the briefly presented oestrous female. Exposure to an oestrous female also significantly increased the mean number of aggressive acts displayed toward submissive males . The inclusion of homosexual mounting in Taylor's aggression score, however, begs the question whether the increased aggression reported actually represents increased sexual behaviour. Even if mounts per se, were not sufficient to elevate aggression scores, mounting might elicit aggression from even the most submissive males, especially when testing is conducted in an essentially neutral arena, and thus inflate aggression scores . Barnett (1958) suggested that the heightened aggressivity of males exposed to females may represent a displacement activity . Taylor (1975) proposed that increased male aggression following exposure to receptive but inaccessible females may be the consequence of sexual frustation or general arousal mediated by olfactory cues. Other evidence indicates that increased male aggression in sexually active animals is mediated by hormonal changes associated with increased sexual activity . Folman & Drori (1966) found that prolonged (7 to 17 weeks) adult cohabitation with a pair of normally cycling female rats increased male accessory reproductive organ size in comparison with cohabitation with pairs of ovariectomized females or intact males . Increased testes size and testosterone production found following cohabitation with gonadally intact females appeared to be the direct consequence of mating (Folman & Drori 1969) since cohabitation with castrated female and exposure to the odour of intact females did not prevent atrophy of the accessory organs (Folman & Drori 1966) . Thomas & Thomas (1973) reported that limited copulatory opportunities (allowing only three intromissions every fourth day) over a 6-week period are sufficient to significantly increase testes and seminal vesicle size of adult male rats above unmated levels . In the present study, males housed with intact females presumably had between two and four opportunities to copulate fully with receptive females . Only one male in this group failed to show mounting during the brief observation period at colony formation, and females of four of the six colonies became pregnant . This limited copulatory experience, therefore, may have
been sufficient to elevate aggression through increased testosterone production . The enhancement of male aggression found in the present experiment may represent only one aspect of a complex relationship between sexual and aggressive behaviour . While reflexive fighting by rats in response to electric shock was first observed in 1939 (O'Kelly & Steckle 1939) only more recently was it reported that intermittent shock administration also facilitated copulatory performance in rats (Barfield & Sachs 1968 ; Caggiula & Eibergen 1969) . The close correspondence between sexual and aggressive behaviour in rats has since been further demonstrated (Caggiula 1972) using tail shock as an arousing stimulus . Both copulation and aggression are readily elicited by shock with the frequency of occurrence of each depending in part, on size of test cage and sex of target animal . Examination of the possible interaction of sexual and aggressive behaviour using a more naturalistic approach should disclose to what extent these two classes of behaviour exert mutual influence upon one another. Acknowledgments This paper is based upon a thesis submitted by the first author to The Graduate School of Rutgers University in partial fulfilment of the requirements for the degree of Master of Science . The authors would like to thank Dr Donald H . Thor for his critical reading of the manuscript and helpful suggestions . Financial assistance from the Rutgers Research Council is gratefully acknowledged . REFERENCES Barfield, R. J. & Sachs, B . D . 1968. Sexual behavior : Stimulation by painful electric shock to the skin in male rats. Science, N. Y.,161, 392-394. Barnett, S. A. 1958. An analysis of social behaviour in wild rats . Proc. zool. Soc . Land., 130, 107-152. Barnett, S . A . 1960. Social behaviour among tame rats and among wild-white hybrids . Proc. zool. Soc . Lond., 134, 611-621 .
Barnett, S . A ., Evans, C. S. & Stoddart, R. C . 1968 . Influence of females on conflict among wild rats . J. Zool. Lond., 154, 391-396. Barnett, S . A . & Stoddart, R . C. 1969 . Effects of breeding in captivity on conflict among wild rats . J. Mammal ., 50, 321-325 . Caggiula, A . R . 1972. Shock-elicited copulation and aggression in male rats . J. comp . physiol. Psychol ., 80, 393-397 .
Caggiula, A . R. & Eibergen, R. 1969 . Copulation of virgin male rats evoked by painful peripheral stimulation. J. comp. physiol. Psychol., 69,414-419 . Eibl-Eibesfeldt, I . 1961 . The fighting behavior of animals . Scient . Am ., 205, 112-122 .
FLANNELLY & LORE : FEMALE INFLUENCE UPON MALE AGGRESSION Flannelly, K. & Lore, R . 1976 . Dominance-subordinance in cohabiting pairs of adult rats : Effects on aggressive behavior. Aggress. Behav ., 1, 331-340 . Folman, Y. & Drori, D . 1966 . Effects of social isolation and of female odours on the reproductive system, kidneys and adrenals of unmated male rats . J. Reprod. & Fert ., 11, 43-50 . Folman, Y. & Drori, D . 1969 . The testosterone content of the testes of mated and unmated rats . J. Endocrinol., 44, 127-128 . Grant, E. C . & Mackintosh, J . H. 1963 . A comparison of the social postures of some common laboratory rodents . Behaviour, 21, 246-259 . Luciano, D. & Lore, R. 1975 . Aggression and social experience in domesticated rats . J. comp. physio! Psycho!., 88, 917-923 . O'Kelly, L . E . & Steckle, L . C . 1939 . A note on long-
659
enduring emotional responses in the rat . J. Psycho!., 8, 125-131 . Sales, G. D . 1972 . Ultrasound and aggressive behaviour in rats and other small mammals . Anim . Behav ., 20, 88-100 . Taylor, G . T . 1975 . Male aggression in the presence of an estrous female. J. comp . physio!. Psycho!., 89, 246-252 . Thomas, T. R . & Thomas, C . N. 1973 . Mediation of mating induced increase in accessory reprodutive organ size of male rats . Physiol. Behav., 10, 13-17. Thor, D . H . & Flannelly, K. J. 1976 . Exposure to females as a variable in territorial aggression of the laboratory rat . Psycho!. Rep., 38, 749-750 . (Received 21 November 1975 ; revised 22 March 1976 ; MS. number : A1791)
THE INFLUENCE OF FEMALES UPON AGGRESSION IN DOMESTICATED MALE RATS (RATT US NOR VEGICUS) BY
KEVIN FLANNELLY * & RICHARD LORE
Douglass College, Rutgers-The State University of New Jersey, New Brunswick, New Jersey
Abstract. The aggression of adult male Long-Evans rats (Rattus norvegicus), toward males of the same strain, was tested before and after a 1-week period of cohabitation with a pair of intact females, ovariectomized females, or intact males, comparable to the females in size . Only cohabitation with intact females increased the aggression of resident males against unfamiliar male intruders . Female enhancement of aggression does not appear to be caused by sexual frustration of males, or a function of dominance-subordinance relations, per se . Increased aggression may be mediated by elevated testosterone production associated with mating . Barnett, Evans & Stoddart (1968) reported that cohabitation with females increased the aggression of wild male rats (Rattus norvegicus) against unfamiliar males . Barnett & Stoddart (1969) replicated this finding with wild-trapped males but failed to find female enhancement of male aggression in animals laboratory-bred for several generations . Specifically, laboratoryreared males did not show the increased `threat' posturing and duration of attack against intruders, observed in wild-trapped males housed with females . Similarly, cohabitation with females apparently did little to enhance male aggression against intruders in mixed-sex colonies of albino rats observed by Barnett (1960) . In three of Barnett's albino colonies the display of aggression toward intruders was minimal and males failed to exhibit any threat posturing . An alternative interpretation of Barnett's findings of female enhancement of aggression is possible . Recent work indicates that only dominant members of cohabiting pairs of adult males attack intruders (Flannelly & Lore 1976) . The latter finding suggests that males residing with females are more aggressive simply because they are more likely to dominate smaller females . The increased aggression of a resident male may be the result of his ability to dominate smaller conspecifics regardless of sex . In this study, we compare the aggressive response of resident males toward intruders, after a period of resident cohabitation with either adult females or smaller adult males, comparable to the females in size . If aggression is enhanced specifically by the presence of females, then males residing with females should behave
much more aggressively toward intruders than male residents housed with smaller males, since residents in both living conditions should readily dominate their smaller cagemates. Because the enhancement of male aggression may yet be peculiar to the presence of females but not related to sexual receptivity, a third group of males was tested which were housed with ovariectomized females . Methods A total of 66 male and 24 female Long-Evans rats were purchased from the Marland Breeding Farm, Hewitt, New Jersey. Eighteen older males, weighing 419 to 642 g were designated resident males. The females and remaining males were comparable in size (245 to 379 g) at the start of the experiment . All animals were housed individually in standard Wahman hanging cages from their arrival at the laboratory until used experimentally . Food and water were freely available and a 12 :12 h light-dark cycle maintained during the experiment . Throughout the experiment resident males were housed in 42 x 66 x 26 . 5-cm cages made of galvanized steel with clear Plexiglas fronts and hardware-cloth floors . All testing was done in these cages . A 30 x 20 x 25-cm nesting cage was placed inside and secured to the floor of each test cage . Four 25-W bulbs illuminated the testing room to permit observation during the dark phase of the light cycle . Procedure Twelve randomly chosen females were ovariectomized under ether anaesthesia . A 2-week recovery period was interposed before testing . Aggression tests and colony formation . After 7 to 10 days of habituation to the laboratory
*Present address : Edward R . Johnstone Training and Research Center, Bordentown, New Jersey, 08505, U.S .A . 654
FLANNELLY & LORE : FEMALE INFLUENCE UPON MALE AGGRESSION
environment resident males were transferred to test cages on day 1, where they were housed individually for 7 days . The first aggression test was given on day 8 . A male intruder was placed with each resident and the behaviours of both animals recorded for the next 30 min . Each intruder remained with a resident for 24 h, after which time the intruder was sacrificed, body hair removed with clippers and skin carefully examined for wounds . The method of scoring of wounds is reported elsewhere (Luciano & Lore 1975). On day 13 each resident was removed from its cage and introduced to a different test cage accompanied by either two intact males, two intact females, or two ovariectomized females . In all, 18 colonies were established ; six of each
type. Each resident and its pair of cohabitants were introduced to a test cage simultaneously . The behaviour of all three animals was recorded and for the first 30 min of colony formation (Table I) and the colonies left undisturbed for 7 days . On day 20 an intruder was again placed into the cage of each resident and the second 24-h aggression test begun . Ten minutes before the introduction of an intruder, the two animals cohabiting with a resident were placed into the nesting cage where they were confined for the entire test session . As during the first aggression test, the interaction of resident and intruder was observed for the first 30 min of testing . Intruders were killed and examined for wounds following the 24-h session .
Table L Means (and Standard Deviations) of Social and Aggressive Measures of Cohabitants and Male Residents During the Initial 30 Min of Colony Formationt Type of colony Resident male with :
Intact females
Ovariectomized females
Intact males
Resident Behaviour toward cohabitants Duration of offensive postures (s)
6.5 (9 .0)
7 .2 (8 . 1)
1512 . 0 (521 . 5)
1295 . 0 (639 .8)
348 .0** (271 . 5)
Frequency of social-investigatory behaviour
98 .2 (43 .5)
78 . 0 (32 . 6)
22 . 0** (18 . 0)
Frequency of ano-genital sniffing
18 . 2 (20 . 8)
11 .7 (26 .8)
4.2 (15 . 3)
Frequency of mounts
14 . 5 (85 . 1)
9.8 (22 . 7)
1 .0 (4 . 5)
Duration of offensive postures (s)
1 .0 (3 . 8)
0.3 (1 .8)
11 .0 (39 . 7)
Duration of defensive postures (s)
9.5 (32 . 7)
27 . 2 (103 . 4)
98 . 3 (153 .2)
Frequency of social-investigatory behaviour
36 .3 (69 . 5)
26 . 0 (56 . 9)
10 .7 (16 . 9)
Frequency of offensive postures
3 .5 (11 . 2)
3 .3 (9 .2)
8 .7 (33 . 2)
Frequency of social-investigatory behaviours
18 . 8 (38 . 8)
20 . 2 (40 .3)
7 .3 (13 . 3)
Latency to fight (s)
655
90 . 8* (93 . 9)
Cohabitants behaviour toward residents
Cohabitants behaviour toward each other
*P<0 .05 . **P<0 . 01 . tSignificance levels represent overall differences between types of colonies .
656
ANIMAL BEHAVIOUR, 25, 3
Behavioural measures . The behaviour patterns recorded were taken principally from Grant & Mackintosh (1963) and are described by them . The total frequency of social-investigatory behaviour of each resident, cohabitant or intruder was recorded individually on digital counters during all observation sessions and a continuous description of all social and aggressive interaction between animals recorded on audio tape . The frequency and duration of each of six offensive and four defensive postures were recorded on an event recorder : `offensive postures' : aggressive groom, attack, offensive sideways, offensive upright, full aggressive, and offensive pinion or pinning ; (defensive postures) defensive upright, defensive sideways, submissive and defensive supine postures . Pinning and defensive supine posture are not described by Grant & Mackintosh (1963) . What the authors term pinning and defensive supine posturing, however, are depicted by Eibl-Eibesfeldt (1961, p. 120, illustration d) . In contrast with the submissive posture, the defensive supine posture is one of active defence, including kicking movements . Frequency of wrestling (see Sales 1972) was also recorded . A fight was defined as a continuous reciprocal sequence of offensive and defensive postures, beginning with the display of an aggressive act and terminating with one animal turning away from the other and engaging in a non-interactive activity . The
frequency and duration of fights and latency to first fight were recorded . Results First Aggression Test Though minimal in some instances, all residents displayed some aggressive behaviour and in no instance did an intruder defeat a resident. No resident exhibited distinctively defensive behaviour . One-way ANOVA's performed on the total duration and frequency of fights, latency to first fight, total duration of offensive posturing by residents, frequency of wrestling and intruder wound scores, revealed no statistically significant differences between the three groups of residents (see Table II) . These analyses were undertaken to confirm the assumption that no differences existed between groups prior to colony formation. Homosexual mounting of intruders was displayed by six of the 18 residents for a total of 14 observed mounts. Fights ranging in duration from 21 to 195 s immediately followed mounting by residents in four instances . Colony Formation Considerable differences between colony types (i .e . types of cohabitants) were observed in the interaction of residents with their cohabitants . during the initial 30 min of colony formation . A one-way ANOVA was performed on each of
Table II. Means (and Standard Deviations) of Aggressive Behaviour of Residents of Each Colony Type on the First and Second Aggression Tests Type of colony Aggression measure
Aggression Resident test male with :
Intact females
Ovariectomized females
Intact males
332 . 0 (108 . 9) 408 . 3 (624 . 7)
365 . 0 (172 . 5) 1004 . 0 (683 . 5)
512 .0 (634 . 8) 1140 .0 (798 .3)
Latency to first fight (s)
First Second
Frequency of fights
First Second
Total fight duration (s)
First Second
75 . 0 (120 . 7) 180 . 2 (171 . 6)*
71 . 8 (60.2) 60 . 7 (82 . 8)
90 .0 (92 . 2) 49 . 3 (97 .6)
Total duration of offensive postures (s)
First Second
85 . 0 (132 . 1) 166 . 5 (141 . 4)
76 . 7 (58 . 6) 66 . 5 (84 . 5)
106 .0 (119 . 0) 58 . 3 (105 . 1)
Frequency of wrestling
First Second
1 . 5 (1 . 1) 7 .0 (6 . 4)**
Intruder wound score
First Second
8 . 5 (8 . 1) 21-7 (47 . 9)**
*P<0 .05 ;
**P<0.01 .
2 .2 4.5
(1 . 2) (3 . 3)*
2.0 1 .7
2 .7 1-7
(1 . 3) (1 . 9)
1 .5 0.9
(0 . 8) (1 . 1)
(1 .9) (1 . 9)
3-3 1 .0
(2-8) (1 . 8)
7 . 3 (8-4) 8 . 0 (33 .4)
5 .0 1 .7
(5 . 3) (6 . 4)
FLANNELLY & LORE : FEMALE INFLUENCE UPON MALE AGGRESSION
the measures of social and aggressive behaviour of colony members presented in Table I . If no fighting occurred during the 30-min observation period fight latency was considered to be 1800 s . Latency to the first fight (F = 7. 61 ; df = 2, 15 ; P < 0 .01) resident total duration of offensive postures (F=3-94 ; df = 2, 15 ; P<0-05) and frequency of social-investigatory behaviour of residents toward cohabitants (F = 7 . 11 ; df = 2, 15 ; P < 0. 01) differed significantly across colonies . Five of the six residents which received intact females exhibited mounting toward one or both cohabitants. Intact females were housed individually, after the completion of the experiment to determine if they had become pregnant during cohabitation . Females from four of the six colonies (seven of the 12 intact females) gave birth . Second Aggression Test Differences between the aggression score of each resident on the first and second test were calculated and one-way ANO VA's performed on these difference scores for various measures . Table II presents the means and standard deviations of several measures of resident aggression on the first and second tests . All residents housed with intact females displayed increases over their first test scores on most aggression measures . Few animals housed with intact males or ovariectomized females increased, and most decreased in aggressiveness toward intruders . Frequency of wrestling with intruders differed significantly across types of colonies (F = 6 .82 ; df= 2, 15 ; P < 0.01) . Comparisons between colony types revealed that residents housed with intact females showed significantly greater increases in total fight duration (F = 5 . 17 ; df = 1, 15 ; P < 0 . 05) and frequency of fights (F = 6 . 98 ; df = 1, 15 ; P < 0 . 05) than residents housed with males or ovariectomized females . Although differences in resident total duration of offensive postures were not significant, residents housed with intact females showed a significant increase in duration of full aggressive (F = 5 . 86 ; df = 1, I5 ; P < 0 .05) and offensive sideways postures (F= 13 . 48 ; df = 1, 15 ; P < 0. 01), in comparison with residents of the other two types of colonies . A single intruder exposed to a resident housed with females was killed and extensively cannabalized. Wound scores were therefore analysed non-parametrically (Kruskal-Wallis analysis of variance by ranks) . Intruder wound scores were found to differ significantly across types of
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colonies (H = 39 .6, df = 2, P < 0.01) . Resident mounting of intruders was observed in only one instance, by a resident housed with males . Discussion The results demonstrate that female cohabitation with males enhances male aggression against intruders in domesticated rats . Residents housed with intact females fought intruders significantly more frequently, and with greater intensity and severity than residents housed with intact males or ovariectomized females (see Table II) . Enhancement of male aggression is specific to the presence of females and does not appear to be only a function of dominance-subordinance relations among colony members . Residents housed with ovariectomized females or smaller intact males did not display increased aggression . Flannelly & Lore (1976) have previously suggested that the achievement of dominance within a colony might increase the aggression of the dominant colony member against intruders. Therefore, female enhancement of male aggression, as reported by Barnett et al . (1968, 1969), might be due to the fact that colony males were dominant over female cohabitants. Here the selection of comparably sized male and female cohabitants, which were considerably smaller than resident males, was intended to insure the dominance status of residents within both like-sex and mixed-sex colonies . Though residents substantially dominated male cohabitants during colony formation (see Table I), resident aggression against intruders was not increased by cohabitation with males. The results of the present study are in accord with the findings of Barnett et al . (1968, 1969) that cohabitation with females enhances male aggression . The present study, moreover, extends the generality of this finding to include domesticated rats . An earlier study by Thor & Flannelly (1976) failed to find increased male aggression following cohabitation with females . In that study, however, pre-cohabitation aggression scores of male colony members were extremely low . Apparently, exposure of males to females in adulthood does not necessarily enhance aggression unless sufficiently high aggression levels are already present . Taylor (1975) has reported that very brief exposure of a male to an inaccessible receptive female produces an immediate tendency to approach a submissive male . This finding need not, however, represent the active seeking of a
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ANIMAL BEHAVIOUR, 25, 3
meagre opponent or aggressive target by a dominant male, as suggested by Taylor. More reasonably, Taylor's males may have been actively seeking the briefly presented oestrous female. Exposure to an oestrous female also significantly increased the mean number of aggressive acts displayed toward submissive males . The inclusion of homosexual mounting in Taylor's aggression score, however, begs the question whether the increased aggression reported actually represents increased sexual behaviour. Even if mounts per se, were not sufficient to elevate aggression scores, mounting might elicit aggression from even the most submissive males, especially when testing is conducted in an essentially neutral arena, and thus inflate aggression scores . Barnett (1958) suggested that the heightened aggressivity of males exposed to females may represent a displacement activity . Taylor (1975) proposed that increased male aggression following exposure to receptive but inaccessible females may be the consequence of sexual frustation or general arousal mediated by olfactory cues. Other evidence indicates that increased male aggression in sexually active animals is mediated by hormonal changes associated with increased sexual activity . Folman & Drori (1966) found that prolonged (7 to 17 weeks) adult cohabitation with a pair of normally cycling female rats increased male accessory reproductive organ size in comparison with cohabitation with pairs of ovariectomized females or intact males . Increased testes size and testosterone production found following cohabitation with gonadally intact females appeared to be the direct consequence of mating (Folman & Drori 1969) since cohabitation with castrated female and exposure to the odour of intact females did not prevent atrophy of the accessory organs (Folman & Drori 1966) . Thomas & Thomas (1973) reported that limited copulatory opportunities (allowing only three intromissions every fourth day) over a 6-week period are sufficient to significantly increase testes and seminal vesicle size of adult male rats above unmated levels . In the present study, males housed with intact females presumably had between two and four opportunities to copulate fully with receptive females . Only one male in this group failed to show mounting during the brief observation period at colony formation, and females of four of the six colonies became pregnant . This limited copulatory experience, therefore, may have
been sufficient to elevate aggression through increased testosterone production . The enhancement of male aggression found in the present experiment may represent only one aspect of a complex relationship between sexual and aggressive behaviour . While reflexive fighting by rats in response to electric shock was first observed in 1939 (O'Kelly & Steckle 1939) only more recently was it reported that intermittent shock administration also facilitated copulatory performance in rats (Barfield & Sachs 1968 ; Caggiula & Eibergen 1969) . The close correspondence between sexual and aggressive behaviour in rats has since been further demonstrated (Caggiula 1972) using tail shock as an arousing stimulus . Both copulation and aggression are readily elicited by shock with the frequency of occurrence of each depending in part, on size of test cage and sex of target animal . Examination of the possible interaction of sexual and aggressive behaviour using a more naturalistic approach should disclose to what extent these two classes of behaviour exert mutual influence upon one another. Acknowledgments This paper is based upon a thesis submitted by the first author to The Graduate School of Rutgers University in partial fulfilment of the requirements for the degree of Master of Science . The authors would like to thank Dr Donald H . Thor for his critical reading of the manuscript and helpful suggestions . Financial assistance from the Rutgers Research Council is gratefully acknowledged . REFERENCES Barfield, R. J. & Sachs, B . D . 1968. Sexual behavior : Stimulation by painful electric shock to the skin in male rats. Science, N. Y.,161, 392-394. Barnett, S. A. 1958. An analysis of social behaviour in wild rats . Proc. zool. Soc . Land., 130, 107-152. Barnett, S . A . 1960. Social behaviour among tame rats and among wild-white hybrids . Proc. zool. Soc . Lond., 134, 611-621 .
Barnett, S . A ., Evans, C. S. & Stoddart, R. C . 1968 . Influence of females on conflict among wild rats . J. Zool. Lond., 154, 391-396. Barnett, S . A . & Stoddart, R . C. 1969 . Effects of breeding in captivity on conflict among wild rats . J. Mammal ., 50, 321-325 . Caggiula, A . R . 1972. Shock-elicited copulation and aggression in male rats . J. comp . physiol. Psychol ., 80, 393-397 .
Caggiula, A . R. & Eibergen, R. 1969 . Copulation of virgin male rats evoked by painful peripheral stimulation. J. comp. physiol. Psychol., 69,414-419 . Eibl-Eibesfeldt, I . 1961 . The fighting behavior of animals . Scient . Am ., 205, 112-122 .
FLANNELLY & LORE : FEMALE INFLUENCE UPON MALE AGGRESSION Flannelly, K. & Lore, R . 1976 . Dominance-subordinance in cohabiting pairs of adult rats : Effects on aggressive behavior. Aggress. Behav ., 1, 331-340 . Folman, Y. & Drori, D . 1966 . Effects of social isolation and of female odours on the reproductive system, kidneys and adrenals of unmated male rats . J. Reprod. & Fert ., 11, 43-50 . Folman, Y. & Drori, D . 1969 . The testosterone content of the testes of mated and unmated rats . J. Endocrinol., 44, 127-128 . Grant, E. C . & Mackintosh, J . H. 1963 . A comparison of the social postures of some common laboratory rodents . Behaviour, 21, 246-259 . Luciano, D. & Lore, R. 1975 . Aggression and social experience in domesticated rats . J. comp. physio! Psycho!., 88, 917-923 . O'Kelly, L . E . & Steckle, L . C . 1939 . A note on long-
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enduring emotional responses in the rat . J. Psycho!., 8, 125-131 . Sales, G. D . 1972 . Ultrasound and aggressive behaviour in rats and other small mammals . Anim . Behav ., 20, 88-100 . Taylor, G . T . 1975 . Male aggression in the presence of an estrous female. J. comp . physio!. Psycho!., 89, 246-252 . Thomas, T. R . & Thomas, C . N. 1973 . Mediation of mating induced increase in accessory reprodutive organ size of male rats . Physiol. Behav., 10, 13-17. Thor, D . H . & Flannelly, K. J. 1976 . Exposure to females as a variable in territorial aggression of the laboratory rat . Psycho!. Rep., 38, 749-750 . (Received 21 November 1975 ; revised 22 March 1976 ; MS. number : A1791)