Early exposures to intermale aggression increases the adult aggression of male rats

51

Behavioural Processes, 16 (1988) 57 -66 Elsevier EARLY

EXPOSURES

TO INTERMALE

AGGRESSION

INCREASES

THE ADULT

AGGRESSION OF MALE RATS 2 1 R. Lore , D. Meyerson 1Psychology

Department,

Rutgers

University,

08903 , U.S.A. 2 Psychology Department, University ( Accepted 20 October 1987 )

of Iowa,

New

Brunswick,

Iowa City,

NJ

IA 52240,

U.S.A.

ABSTRACT Lore, R., and Early Meyerson, D. exposure to intermale aggression increases the adult aggression of male rats. Behav. Process., 16 : 57-66 Intact litters of rats were exposed to three brief episodes of intense paternal aggression against an unfamiliar adult conspecific prior to weaning on day 31. Control litters were not exposed to paternal conflict. Male offspring of both groups were given a long-term test of their aggression against an unfamiliar intruder when the subjects were 103-114 days old. During the initial lo-minute observational phase of the aggression test, few animals in either group attacked the intruder, but intruders lost more bodyweight during the 22f-hour test when placed into the cages with the aggression-exposed subjects. Thus, early exposure to aggressive exchanges between adult animals increases the use of an aggressive strategy during subsequent confrontations with unfamiliar conspecifics. Two mechanisms possibly underlying this phenomenon are discussed. INTRODUCTION We

have

known

acquired

during

increases

the

decrease

likelihood

future

Butterworth,

intensity influenced

by

development.

For

membership

changes

to

adulthood

young

comparable

animals

Stipo-Flaherty, intact with Lore,

females

either

example

are

housed

during

more

females

indicates

in

in

that

can

be

during the

from prematurity aggressive groups rats

aggressive

than

or younger

males

males

B.V. (Biomedical

than

(Lore

housed

Division)

&

with housed

(Flannelly

1977).

0376-6357/88/$03.50 0 1988Elsevier Science Publishers

&

the

also

where

groups

&

Scott

experiences

stable male

defeats

Gurney

1958;

rodents

more

adult

while

Scott,

the period

together

Similarly,

experience encounters

Story,

subtle

significantly

reliably

ovariectomized

male

more

rats

housed

1984).

acts,

work

adult far

frequently are

1942;

recent

of

social

aggressive

aggressive

& Allee,

in

number

that in

(Fredericson,

More

aggression a

time

of future

Ginsberg

1951). of

long

successes

aggression

1966;

Fredericson,

a

for

previous

&

58

Even in

during

mice

can

the

be Mouse

environment. present

are more

animals

receiving

Likewise, period

It

the adult

via

male

the

learning

whereby

of

mice

paternal

(1980)

results

aggression

animals

reviewed

in a similar

as a consequence

is,

the

manipulations

of the offspring.

the adult

adult

that

to the young

experimental

one

of

change

in

He interpreted of

an

level

efficient in primates

of early

mouse

peaceful

exposures

a conspecific

to

male brief

was

third that

to nine

brief

the young the cage of

in an identical group

early

was

not

the exposure

to

increased

development

as measured

by the mouse's

latency

in its cage. conducted

rats

would

episodes

of

in

to

provide

with

understanding

male

these of

order

rat

determine preweaning The

aggression.

exposures the

to by

influenced

be adult

designed our

while

in

mice.

within

was exposed

issue

using

placing

a

during

placed

study

present

by

demonstrated

adults,

adulthood,

mice

container

group

on this

phenomenon

just-weaned

wire

DeGhett

aggression during

young

experiment this

aggression

A second

to any adults.

aggressivity

of

a protective

males.

two

group

adult

of

into

to

relevant

(1975) demonstrated

exposed

two aggressive

consistent

the preweaning

grasshopper

modelling;

existence

immediately

episodes

was

than

1972).

aggression.

individually

exposures

of

the

dramatically

he

whether

tests

in an animal's

Chamove

aggression

implicating

Briefly,

The

social fathers

experience

information

that

as

DeGhett

to attack

the their

& Nowell,

throughout

increase

example,

aggression

In the only

fashion

aggression

aggression

mechanism

adult

rodents,

exposed

with

southern

early

be providing

mechanism

to parental

study

learning

of maternal

can be modified

in

(Mugford

in

the

suggesting

findings

adult

that

evidence

the amount

adult

1977).

For

the subsequent

daily

aggression

aggression.

primate

subsequent contact

in a subsequent

may

weaning

of an adult male

possible

may result

aggressivity

in

future

differences

until

no paternal

increases

is

period, by

reared

aggressive

& Southwick,

presence

these

pups

the presence

also

(McCarty

about

preweaning

influenced

in

experiences

a

manner of

rats

59

reared were of

in the wild.

weaned, aggression

potential

with

both

were

changes

Thus,

the exposures

parents

used

to

in the rats'

present. allow

a

occurred

before

the rats

Lastly,

several

measures

more

complete

analysis

of

aggression.

METHODS Subjects Thirteen breeding colonies were established, each consisting of one adult male and one adult female Long-Evans rat, from stock originally supplied by Perfection Breeders, Douqlassville, PA. Seven of the colonies were randomly assigned to the control condition and the remaining six colonies received the experimental treatment (aggression modelling). The male breeders of each colony had been previously used in an aggression study and were selected from a larger group of males based on their readiness to attack an unfamiliar male conspecific introduced into their home cage. Between birth and weaning (at day 31) the litters were housed in 63.5 x 41.5 x 25.5 cm stainless steel maternity cages with solid floors and Plexiglas fronts. Both the male and female breeders were continuously present during the preweaning period. Pine chips were scattered on the floor and changed at weekly intervals. Purina Rat Chow and tap water were available ad libitum, and the animals were maintained on a 12:12 hr light-dzk cycle throughout the study. At weaning, 26 males were randomly selected to serve as Experimental subjects from the six litters exposed to the experimental treatment. An additional 26 males, chosen at random from the seven control litters, served as controls during subsequent aggression testing. Aggression Exposures Each Experimental litter was provided a total of three aggression exposures one each on days 23, 27, and 31. The exposures involved introducing an adult male Long-Evans rat (from the same stock as the colony rats) as an intruder into the maternity cage for a 10 minute period. A total of 18 intruders closely matched in age were used for the aggression exposures, and weight to the resident adult male. The intruders had had no previous experience and were each used only once in the study. each During 10 minute intruder one observer exposure, recorded the frequency and duration of two aggressive behaviors initiated by the (lateral threat display, and fight/attack) resident male toward the intruder. In addition, the defensive during the first, and third intruder reactions of the pups The Experimental exposures were recorded by a second observer. pups were also observed on days 22 and 30 (without an intruder determine rates the present) in order to base for PUPS' The control not presented with colonies were behaviors. room and, since they were maintained in a separate intruders preweaninq period, the aggression-exposure throughout the treatment could not have influenced their behavior. After the third and final exposure (at 31 days of age) the young animals of both groups were weaned into standard laboratory

60

hanging cages (25 x 18 x 18 cm), and thereafter housed together in the same room. Aggression Test and Upon reaching 103-114 days of age, the 26 Experimental 26 Control rats were each given a 224 hour aggression test work in this iaboratory. A similar to that used in previous procedure is available detailed review of this (Lore, During the aggression test, the Nikoletseas, & Takahashi, 1984). duration of three aggressive behaviors (lateral threat display, was recorded during the 10 min on top posture, and fight-attacks) immediately following the intruders' introduction. Body weight of the resident and the intruder were recorded before and after the aggression test. Latency to first attack was also recorded if attack occurred during the initial 10 min observation period. Prior to testing, all 52 subjects w.ere coded and their cages redistributed on the cage rack in order to insure that the testing was done by an observer who was unaware of their previous treatment status. The 26 intruders used in the aggression test were derived from the same Long-Evans stock and had been reared in isolation from weaning. They were younger and their body weight at the test (mean weight = 414.2g) was beginning of the aggression considerably less than that of either the experimental (450.4g) or control (446.1g) animals. Each intruder was used in two aggression tests, once with a control once with an and animal, experimental with presentation the order of intruder counterbalanced between the two treatment groups. In order to minimize the intensity of overt aggression and physical injuries during the aggression test, both the subjects and intruders were much younger than is typical in aggression studies with rats. Previous work indicates that this strain of domesticated rat is only mildly aggressive toward intruders at Also, the use of 100-120 days of age (Takahashi ti Lore, 1982). intruders that are much younger than resident animals seems to As a consequence, we reduce serious fighting during the test. did not anticipate a great deal of measurable aggression during the lo-min observation period. RESULTS Aggression As to the

Exposure

shown

intense

aggressive

intruder.

attack

the

observed

In

the

in which

interactions

only

intruder,

investigating

1, Experimental

in Table

and

pups.

one

of

Also,

the intruder

between

the

in that

subjects

killed

all exposed

male

breeder

18 exposures

incident one

the

were

case

the of

did

the

intruder pup

a pup with

and

female

had

been

mortality

was

a cervical

bite.

61

TOTAL FREQUENCY DIRECTED TOWARDS

Table 1 OF ADULT MALE RESIDENT AGGRESSIVE BEHAVIORS THE INTRUDERS DURING THE THREE EARLY EXPOSURES

Litter Number 2 3 5 6 7 8

Lateral Threat 24 39 42 33 21 72

Observations

of

exposures

indicate

defensive

behaviors

motionless periods

that

litters

the

without

the

were

behaviors

which

aggression

exposures.

with

exposures,

or without but

for

never

Most the

pups

most

with

the

female the

and

third

exclusively

in

the observational

in

the

Experimental

feeding,

part

commonly, resident

huddled

almost

resting,

the

first

of the cage or clinging During

present,

nursing,

were

the

engaged

in a corner

cage wall).

intruder

observed

during

pups

(huddling

to the wire mesh

condition

corner

the

Fight-attack 12 14 42 41 15 56

and

absent young

huddled

during

resident

playing,

during

the male

in

the the

aggression breeder

or

intruder. Aggression As first

10

threats,

acts

min

serious

of

the

exhibited

animals

eight

Test

expected,

of

a

aggression

Aggression total

2 on top postures, the

26

(17 lateral

Experimental threats,

of

was

Test. 25

infrequent Six

of

aggressive

15 attacks) subjects

toward

the acts

26

the

control

(8

lateral

intruders

whereas

displayed

5 on top postures,

during

43

aggressive

21 attacks).

Table 2 PERCENT BODY WEIGHT LOSS AND STANDARD DEVIATION OF INTRUDERS AND RESIDENTS DURING THE 224 HOUR AGGRESSION TEST Resident

Treatment

Aggression Exposed Animals (N=26) Control Animals (N=26)

Percent Body Weiqht Intruders 8.41 (2.51) 6.16 (3.351

LOSS (SD) Residents 6.78 (2.66) 6.28 (3.16)

62

Table during

2

presents

the

224

experimental

tested

order

first)

was

nor

than

exposed

suffered

these

c 1.0

were

trial or

with

aggression

larger

with

control

and

Resident

also

with

(intruder

treatment

cases.

this

animals

tested

order

tested

between

but

all

tested

a significantly

first

in both

residents

of

When

Neither

subjects

E

loss

same animals

interaction

to early

control

significance

test.

,.005.

the

significant,

that had been weight

weight

than when

F(1,24)=9.84, E with experimental

subjects

percent

aggression intruders

subjects,

loss of body weight controls

the

hour

trial

animals

lost slightly

effect

did

not

at an early

age

more

approach

(F c 1.0).

DISCUSSION In this brief

study,

episodes

conspecific toward

of

young

exhibited

intruders

a

than

aggression-exposure. not

exhibit

during

the

when

an

immediate minutes

exposed Weight

is

often

reaction during work of

a to

body

to these

meaningful

during

the

colonies

intruders

were

socially

the

reared

of

stay.

adult

intolerance early

animals in

test,

did

aggression

intruders

entire

many

long-term

of

the

degree

223

lost

hour

of

test

were

and

was recorded

than

their

more wounds

intruders

placed

Isolation-reared

When,

after

fighting

24 hours

however, 24-hour

&

occurs

in previous

into the cages the

during

reared

colony's the first were

not

intruders

the

isolation-reared

stay

in the colonies,

and lost much

(Luciano

that

intruders

socially

tests

aggressive

For example,

intruders for

aggression

resident's

rats

severity

hour.

removed

they had suffered

to three an

received

increase

the

during

to the intruder

greater

first

during

of the test.

lab, unfamiliar

with

not

aggression

index

than

minutes

hour of the intruder's attacked

social

had

dramatic

the

intruders

intruders

response

of

against

animals.

more

in this

degree that

weight

of

established

aggression

the aggression-exposed

and of

loss

the initial

aggressive

greater

Although

more

exposed

paternal

controls

first

significantly

rats

intense

Lore,

more weight 1975).

In

than still

63

another reared of

the

study,

caged-reared

aggression animals

of

controls

during

in

the

greater

20

and

weight

animals

minutes

intruders

environment

burrowing

wounding

first

hours,

by

less than that

had

loss

of

the

exposed

to

experienced

(Nikoletseas

&

1981). In

the

present

experienced

any

animals

were

test.

Although

amounts

serious

in good

of body

lesioning

physical

nearly weight

were

more

matched

closely

(Nikoletseas

& Lore,

short-term

behavioral

expose

intruders

acquire

a

not require

in Given

the

to residents

for

of older, are

it

does

to

were

animals

seem

aggressive

to

in order

to

animals's

the

test

resident

high

the

necessary

resident

however,

of

in

periods

a

as

that

unreliability

time

elicit

the

not

intruders

the

cases,

highly

likely

after

appreciable

aggression

of

In most

all of the

resident

frequent

long

appraisal

and

losses and

the

of

test,

that

these

to

intruders

lost

animals

age

nor

examined

animals

older

aggression

the use

intruders

the

indices

intolerance.

the test when

the test,

using

1981).

realistic

aggressive

during

of

during

work

residents

condition

all

as in previous

intruder-elicited

neither

study,

great

or

the

24

displayed

significantly

was

after

Yet,

reared

aggression

environments

test.

significantly Lore,

amount

in burrowing

level

does

animals of

overt

aggression. Our previous

findings results

aggressive

of

A

mediated?

information

these

as

the

may be transmitted

Experimental

work

learning

modelling,

via

stimulus

(Lore,

acquiring

an

has

are

later

might

posits

as

that

that

Suedfeld,

response

(Corson,

1971) 1967;

young

solely

Note

rats to

effect

the

behavior

and

be rat

as

that

a

the

modalities.

are

avoid

to the

confronted

this

conflicts.

learning

(1975)

animals

increase

via any of the sensory

such &

How

aggressive adult

demonstrated

Blanc,

operant

animals

adults.

about

DeGhett's

of young

conspecifics

interpretations

observing

with

exposures

adult

when

information

of

consistent

Early

intruders

learning

some

consequence

are

between

aggression

unfamiliar

acquires

rats mice.

exchanges

intensity with

with with

capable

of

an

aversive

more

rapidly

Powell,

1968)

by

64

exposure Since

to

an

young

to aperiodic Bovet,

this

intense

about

learning

adulthood

as

compared

the

could

the

system

thereby

and

stress.

relatively

evidence

Early

&

acquire and

that

aggressivity

exposure

to

that

mediates

in the

presently

in

the

parallel distressed

in

rats.

be

aimed

The

handled

well

acquisition (1980)

periods,

of

the

parental

review

Interestingly,

these

of

staged

conflicts

between

specifying

of subsequent

eachother

& Zahn-Waxler, the

aggression.

during

1985).

mechanism

aggression the

animal

observing

towards

rather

mechanism

primate

(DeGhett,

become

at

animals

and attempted

represent

in mice

Iannotti,

these

1962, p. 245).

demonstrated

aggression

a more

one group

housed

children

more

limited

(1962) handled

controls

of

their

stressful

even

that

(Cummings,

in

can produce

then

even

handling

to

is

developmental

Chamove's

that

changes

and

to that

effectively

reactions

controls.

might

as that

more

observation

while

exhibit

period

may

neuroendocrine

periodic

stressors

and Morton

critical

nongenetic

as well

early

stress

evidence

There

the nonhandled

experiences, the

as

1968).

and Morton,

during

cope

which

exposure

early

animal's

to

behavioral

nonhandled with

of

long-lasting

preweaning

with

illustrated

literature,

and

early

abundant

such

Levine,

(Denenberg

modelling

adult

mechanism

the

young

produced

Denenberg

stress

than

the

that form

the

produce

to wrestle

to nip them"

of

that these

the

together

alteration

a

work

&

animal: during

episodes

represent

could

indicating

rats

should

increased

not incompatible,

treatments

(Newton

"attempted

also

rats

experiences

lacking

is

physiological

aggressive

and

young

the

these

phenomenon

enables

Earlier

rodents

situations

levels

task.

that

animals

maturation

innocous

subsequent

animals

the

to Fe exposed Robitaille

for their

although

observed

accelerates

of

likely 1962;

during

to

performing are

(Calhoun,

plausible

is responsible

conflict

infant

aggression

aggression

An alternate,

with

conditions

situations.

underlie adult

field

it is quite

1976),

modelling

under

but

information

conspecific

experienced

rats

1975)

reports obviously

adults the Future

underlying

and anger work this

65

REFERENCES The Ecology and Sociology of the Norway Calhoun, J.B., 1962. USPHS Publication No. 1008. Washington, DC, U.S. Rat. Government Printings Office. Nongenetic induction of acquired levels of Chamove, A.S., 1980. J. Abnorm. Psychol., 89: 469-488. aggression. Observational learning of a lever pressing Corson, J.A., 1967. 197-198. response. Psychon. Sci., 7: Cummings, E.M., Iannotti, R.J. & Zahn-Waxler, C. 1985. Influence of conflict between adults on the emotions and aggression of young children. Devel. Psychol., 21: 495-507. DeGhett, V.J., 1975. A factor influencing aggression in adult Witnessing aggression when young. mice: Behav. Biol., 13: 291-300. Denenberg, V., & Morton, J.R., 1962. Effects of environmental complexity and social groupings upon modification of emotional Physiol. Psychol., 55: behavior. J. Comp. 242-246. Flannelly, K., & Lore, R., 1977. The influence of females upon aggression in domesticated male rats (Rattus norvegicus). Anim. Behav., 25: 654-659. Fredericson, E., Story, A.W., Gurney, N.L., & Butterworth, K., 1955. The relationships between heredity, sex, and aggression in two inbred mouse strains. J Genet. Psychol., 78: 121-130. Ginsburg, B., & Allee, W.C. 1942. Some effects of conditioning on social dominance and subordination in inbred strains of mice. Physiol. Zool., 15: 485-506. Lore, R., Blanc, A., & Suedfeld, P., 1971. Empathic learning of a passive-avoidance response in domesticated Rattus norvegicus. Anim. Behav., 19: 112-114. M., & Takahashi, L., 1984. Lore, R., Nikoletseas, Colony aggression in laboratory rats, A review and some recommendations. Aggress. Behav., 10: 59-71. A., 1984. Postweaning social Lore, R., & Stipo-Flaherty, experience and adult aggression in rats. Physiol. & Behav., 571-574. 33: Postnatal influences on Lore, R., & Takahashi, L., 1984. intermale aggression in rodents. In Flannelly, R. J. (Editors) Biological perspectives Blanchard, & D. C. Blanchard on aggression, Liss, New York, pp. 189-206. Aggression and social experience Luciano, D., & Lore, R., 1975. J Comp. Physiol. Psychol., 88: in domesticated rats. 743-745. Paternal care and the McCarty, R., & Southwick, C.H., 1977. development of behavior in the southern grasshopper mouse, 476-482. Behav. Biol., 19: Onychomys torridus. Paternal stimulation during Mugford, R.A., & Nowell, N.W., 1972. Effects upon aggression and open-field testing of infancy: 30-36. J. Comp. Physiol. Psychol., 79: mice. Early experience and behavior, Newton, G., & Levine, S., 1968. Charles Thomas, Springfield. Aggression in domesticated Nikoletseas, M., & Lore, R., 1981. Aggress. Behav., rats reared in a burrow-digging environment. 245-252. 7:

66

Field observations on the Robitaille, J.A., & Bovet, J., 1976. social behaviour of the Norway rat, Rattus norvegicus (Berkenhout). Biol. Behav., 1: 289-208. Aggression. University of Chicago Press, Scott, J.P., 1958. Chicago. E., 1951. The causes of Scott, J-P., & Fredericson, fighting in mice and rats. Physiol. Zool., 26: 273-309. Takahashi, L., & Lore, R., 1982. Intermale and maternal aggression in adult rats tested at different ages. Physiol. & Behav., 29: 1013-1018. Footnotes 1.

2.

Requests for reprints should be sent to Richard Department of Psychology, Busch Campus, Rutgers New Brunswick, NJ 08903 This research was supported by a grant from the Research Council, Rutgers University. We thank Goldberger for her assistance in the study.

Lore, University, Rutgers Susan