The effect of scents on the territorial and aggressive behaviour of laboratory rats

25

Behaviourd Processes, 29(1993)25-36 0 1993 Elsevier Science Publishers B.V. All rights reserved 0376-6357/93/$06.00

BEPROC 00462

The effect of scents on the territorial and aggressive behaviour P.D. Garcia-Brull, Unidad

Docente

de Fisiologia Animal, y Parasitologia,

of laboratory

rats

J. NGtTez and A. Ntiriez Departamento

Universidad

de Biologh

de Valencia,

Animal,

Valencia,

Biologh

Celular

Spain

(Accepted 18 November 1992)

Abstract The

majority

of works found in the literature

mention odours as an important factor in

the development of social lines and the unleashing of aggressive behaviour, but very few authors have studied more deeply the role that these odours play, how they influence behaviour and what importance the variations of these marks of identity may have. In the present work we analyse social relations presented by laboratory rats (Rattus norvegicus, Wistar breed) in seminatural conditions, with special reference to behaviours of dominance, territorialism and aggressiveness, and the importance that these marks of odour play on these behaviours. For this purpose, different individuals (from the established colonies as well as intruders, both males and females and pups) were impregnated with the urine of other individuals and then observed to see whether differences existed in the aggressive behaviour shown towards the intruders by the alpha male of the colony.

Key words:

Aggression; Territory;

Scent-mark;

Odours; Social behaviour

Introduction Unfamiliar male conspecifics are often attacked and killed when entering the established territory of a colony of wild rats (Rat&s norvegicus and R. rattus) (Ewer, 1971; Alberts and Galef, 1973; Blanchard and Blanchard, 1977, 1981; Takahashi and Blanchard, 1982). Likewise, domesticated albino rats (R. norvegicus) from established colonies attacked introduced strangers, although they showed very little agonistic behaviour toward reintroduced members of the same colony (Blanchard et al., 1975, 1977a,b, 1984, 1988a,b;

Correspondence

to:

Biologia

Biologia

Animal,

P.D.

Garcia-Brull, Celular

Unidad

y Parasitologia,

Docente Universidad

de

Fisiologia de Valencia,

Animal,

Departamento

Valencia,

Spain.

de

26 Garcia-Brull rats

et al., 199Oa).

Analysis

and

introduced

strangers

defensive

behaviour

equivalent

1988;

Takahashi

It is well either

secretion

chemical

of particular 1988;

There

sulphate

influence

solution,

Calef,

Flannelly

the intruders

and

Galef

residents Thus,

deprivation

specific

the

intruders

other

declined Sieck

the present

territorial

and aggressive

intruders

with

important

(Birke

its membership

the scent-marking

and Sadler,

of odours

1984;

Maruniak

Lore,

Thor

anosmia reported residents.

interactions

(Alberts

et al.,

virtually

(1975)

that treatment

behaviour with

of

Alberts

by anosmic

with zinc sulphate

anosmia

1976;

eliminates

Although

confronted

peripheral

of a zinc

paradigm

by intact colony

when

aggressive

have investi-

applications

1975;

treated

and

studies

intrusion

peripheral

with

demon-

foreign

males.

may conceivably

and not necessarily

be

to a sensory

of aggression. Thor

(I 976)

residents

reported

as an intact

and aggressive

that

intruder,

zinc

sulphate-treated

and anosmic

residents

behaviours.

have indicated

that zinc

may be more

experiments

territorial

of these

by intranasal and

behaviour

and

effects

on

Most

that residents

in all social

(1974)

Therefore,

and possibly

in rats, therefore,

Luciano

associated

by colony

behavioural

using about

status,

of social-investigatory

found

Flannelly

and Baumbach

and that some

territory,

information

Luciano

However,

to the motivation

in social-investigatory

their

may obtain

role

no diminution

reduction

are attacked

and

1981,

conspecifics

rodents

aggression

Luciano

hand,

1977,

to the

induced

1975;

of aggression

to a general

scent-mark

of rats in the colony

less social-investigatory

the elimination

attributed

the

anosmia,

intruders.

reported

and Blanchard,

According

contradictory.

behaviour

eliminates

intruders,

colony

of attack

and faeces.

As was to be expected,

against

(1973)

toward

on

are very

Luciano,

also

significantly

On

studies

1976).

aggression

only

strated

1973;

a range

urine

glands

as in other

of peripheral

1971,

among dominant

1990a).

on aggressive

and Thor,

resident

few

or

or social

are no specialized et al.,

relatively

its sexual

of urine,

in the rat, and they

gated the and

drops

Garcia-Brull

are

behaviour

There

using

of species

glands,

deposited,

the scent-mark,

groups.

may be done

patterns rats show

rats (Blanchard

of a variety

by specialized

of the material

from

laboratory

1982).

rodents

produced

composition

the individual

et al.,

that

that

to that of wild

and Blanchard,

known

of attack and defense

indicates

sulphate

properly

were

conducted

behaviour

without

lesions

the urine

of different

donor

in the normal

aggressive

response

treatment

attributed

to investigate

The

rats was used to determine toward

poisoning.

the effect of odours

or manipulations.

of colonies

may be toxic

to systemic

on

scent-marking

whether

odours

of are

male intruders.

Methods Subjects The Wistar from

experiments breed). the

same

experiments. dominant tests.

The (alpha)

(a) The

of introducing (35

cmL),

one which

were

Briefly,

carried

the colonies

litter, colony

and

had

animals

out

been

set

so that a fight takes

colonies

of four 120 150

of albino

days

prior

place for this

to stay on the platform

to

the

days of age during

(Garcia-Brull

into a tank,

rats (Rattus

adult males and four

had been identified

access into pool test”

the males of the colony

manages

60

were about

male of each colony

“restricted

with

consisted

beginning

these

the experiments.

The

on the basis of two dominance et al., 199Ob),

of security.

for the longest

all

of

in the centre of which

position

norve@cus,

adult females,

time

The

which

is a small

dominant

(duration

consists platform

male is the

of test 5 min>.

27

(b) The “access to a female

in oestrous

test”

(Risueno

et al., 19901, which

consists of

placing the males of the colony with an oestrous female. The dominant male is the one which copulates with the female for the longest time, defending this privilege against the other individuals (duration of test 30 min). In both tests we obtained the same results concerning the nature of the dominant male, with a 100% agreement between the two methods. Only two sessions were done with the same colony. In this way, the possible victory experience obtained in previous tests with Flannelly et al., 1984) was eliminated.

placed

strangers

(Blanchard

et al.,

1975;

The introduced strangers used were 64 males and 24 females, with ages and weights equivalent to those of the colony rats at the time of testing. Moreover, 100 pups and 104 reintroduced rats were used. The colony males and females averaged about 420 g and 285 g respectively, and they were between 150 and 200 days old. The intruders used had ages and weights

equivalent

to those of the studied

colony

members

at the time of testing.

Apparatus The colony enclosures were similar 1988). Briefly, these were 75 X 75 x top and flooring of cement covered Food holders and water bottles were were freely available and temperature cycle was maintained. Behaviour was recorded Mitsubitshi

VHS video

Control procedure The tests consisted

to those described in Blanchard et al. (1975, 1977, 100 cm compartments, with plywood walls, Plexiglas with wood shavings which were changed monthly. placed in the centre of each cage. Food and water varied from 22 to 25.7”C. A reversed 12 h light-dark

using a Hitachi

tape recorder

of introducing

(model

video

camera

(model

HV725)

attached

to a

HSE30).

strange males into the colonies

for a period

of 10 min

from the first behavioural interaction. In order to avoid the rats becoming accustomed to attack, as suggested by Blanchard and Blanchard (19771, only two different tests were made with the same colony (introducing different strange males with different treatments in each one). The intruder

animals

were

introduced

to the colonies

by means of a tube

situated

at

ground level, which connected the interior of the receptacle with the exterior. This contact was used only to introduce intruders and remained closed at all other times. Despite this being an artificial way to introduce the intruders, which would not normally occur in the wild, it was, perhaps, the least artificial form of introduction, in that it involved the lowest level of interference by the experimenter. One resident male initiated the majority

of attacks on intruders.

This animal

was the

dominant (alpha) male. The following aggressive behaviours (mostly described by Blanchard and Blanchard, 1977, 1981) were observed and measured (duration). Approaching and investigatory sniffing of the stranger by the alpha male (Fig. la). Piloerection (Fig. 1 b): only when the intruder is not recognized as a member of the colony. Erection of alpha male back hairs. Threat and confrontation (Fig. Ic and d): offensive and defensive upright posture without contact between the two animals. Chase/flight: alpha male chases the intruder biting its back. Boxing posture (Fig. If,): defensive upright posture. The intruder rears on its hind legs, facing its attacker when he makes offensive sideways movements.

28

a) Ano-genital sniffing of

b) Alpha male’s piloerrction

c) Threat

intruder by alpha male.

d) Confrontation

f) 1: Defensive upright posture

e)BoS

or boxing posture (intruder) 2. Lateral attack (alpha male)

gJ 1 Offensive posture (alpha aul.1 2: Submissive poatum (intrudar). Fig, 1, Aggressive(alpha male) and defensive (intruder)

postures observed in territorial behaviour of

rats.

Offensive

sideways movements or lateral attack of alpha male (Fig. If,).

Alpha male

moves lateral to and within 5 cm of the intruder, frequently with its back arched and its head lowered. Aggressive posture or on-top-of posture (Fig. Ig,): alpha male is standing over the intruder, which is lying on its back. Submissive posture (Fig. lg,): The intruder rolls over to lie on its back. Because the data and tables derived are very numerous we present the results in tables alluding to the positive or negative aggressive response of animals (when all these postures were shown or when the intruder was ignored and treated as a colony member respectively). Data were analysed by analysis of variance (ANOVA) and individual comparisons between groups were performed by the Tukey-Kramer test. Each test was repeated four times.

Experimental procedures The intruders were marked

with the urine of different

conspecifics,

and the variation

the resident male’s reactions was analysed. The different tests (64) can be grouped following six experiments. Experiment 1: Stranger introduction (two different tests; see Table 1).

of

in the

29 TABLE

1

Intruder

Reaction 6cu

Experiment

2: Introduction

d

0

+ (Aggression)

(Ignored)

_

of colony

stranger and colony donors respectively Experiment 3: Placement of colony

and

stranger

individual

marked

(28 tests; see Tables 2 and 3). and stranger conspecifics marked

male urine (8 tests; see Table 4). Experiment 4: Removal of alpha male and introduction

with with

urine

of

dominant

of stranger (two tests; see Table

5). Experiment 5: Alpha male removing and colony and stranger animals, marked with urine of stranger and colony donor respectively (16 tests; see Table 61, or with dominant urine (4 tests; see Table 51, placement. Experiment 6: Alpha male, marked

with

urine

of other

colony

members

of stranger

conspecifics, reintroduction (4 tests; see Table 7). Urine donors were enclosed in a 25 x 15 cm stainless steel box floored with a grille. The urine was collected in a graduated cylinder with the help of a funnel. The urine used to mark the intruders was used in the 2 days after its collection to prevent alterations. For the same reason, the urine was stored in hermetically

closed capsules and refrigerated.

Results Experiment 1 First, as control experiment, the strange males (dominant or not) and females were placed, in different tests, in the colony territory. The alpha male always attacked the strange males and never strange females, as described by Blanchard et al. (1984). (See Table

1 and Fig. 2).

Experiment 2 (Tables 2 and 3) Colony males and females were

marked

with

strange

male

and

female

urine,

and

strange males and females were marked with urine of colony males and females. Animals (both males and females) marked with female urine (whether strange or not), or with colony male urine, were ignored by the alpha male and treated like a colony member. Only anogenital sniffing (social investigation) was observed. Results show a highly significant difference with the respective control tests (ANOVA P < 0.001 and Tukey-Kramer test P < 0.01). On the other hand, animals (both males and females) marked with strange male urine were always attacked by the alpha male (Table 2). However, when they were colony members marked with strange male urine, aggression was no so fierce (smaller number of bites (7.75 + 1.5) and lesions (I .25 f 0.25)) as in the strange male placement test (12.0 + 2.16 bites, and 3.5 + 0.5 lesions) (only statistical differences in these results), probably because reintroduced colony animals presented submissive postures and did not respond in an aggression elicited manner as an unfamiliar intruder.

EXPERIEIKE:

Nn

MEAN VALUES

( f f SD)

EXPERIEIKE:

Nn

MEAN VALUES

( jf * SD)

Fig. 2. (a) Summary

of the control results of male resident’s aggression against male intruders

defensive scores of intruders (duration in

and

SD). (b) Mean time (s + SD) of each hehaviour shown in

5f

the control experiment by alpha male against female intruders.

in order

to find out whether

due to the postures of these

animals,

some

Strange

pups

were

marked

with

a familiar

were

marked

From

delimitation wise,

results

and killed

odour we

suggest

and distinctive

demonstrated

by individual were

or that of a strange that

of social

both territory

odour

repeated

with

female.

odours

residents

an important

with

and members

that may be due to their

whether

male killed conspecific of the same

own

was

or to the odour

the introduction

If pups,

play

relations

adults

but accepted when

male, the alpha colony

can conclude that

by individual

intruder

by the alpha male,

of a strange

and in the establishment

the outcomes

characteristic

shown

of the experiments

attacked

with the urine

these

the aggressiveness

or confrontations

of pups. they were

strange

or not,

them (Table role

3).

in territory

intruders.

Like-

colony

have a

scent-marking.

31

Experiment 3 Third, we investigated whether odours were related to the hierarchy within the group. We wanted to see if the alpha male would lose its status in the presence of individuals impregnated with alpha male urine. The results (Table 4) show that the intruder males acted submissively before the alpha male, although they were not attacked. The other members of the colony acted submissively in the presence of both the true alpha male and the intruders

marked

with alpha

male urine,

which

they confused

with the true dominant

male. To confirm

(experiments

these observations,

the same tests were done after removal

of the alpha male

4 and 5).

Experiment 4 When a non-marked

strange alpha

male was placed

in the colony

territory

(Table

5),

one of the colony males adopted the role of the new dominant male and attacked the intruder. However, the behaviour of this new alpha male was ambiguous, attacking both intruder and other colony males. There was a significant difference between these attacks (ANOVA P < 0.001 and Tuckey-Kramer test P < 0.01): whereas in the confrontation with an intruder a piloerection could be observed (I 9.0 k 1.63 s>, in the confrontation with the colony animals it was absent. This suggests the existence of hierarchical reorganization in the colony simultaneous with a territorial behaviour (attack against an intruder).

TABLE 2 Intruder

Marked with urine of colony

Colony

6

_

Colony

0

+

6

colony

strange d

0

+ _

+

+ +

Strange 6

+

+

+ _

Strange

+

+

+

_

_

+

P

strange 0

+

Reaction i3u

In this and the following was an aggressive

tables

reaction;

-

+

indicates

indicates

that (1) animals

non-marked

animals

_

were

marked

and absence

with

urine,

and (2) there

of aggressive

behaviour.

TABLE 3 Intruder

Marked colony

with urine of 6

colony

0

strange d

strange

0

colony

strange

PUPS

PUPS

+ _

pups

+

+

+

+

_

Strange pups

+

+

+

+

+

Reaction

~

Colony

6cu

+ zlled

killed

32 TABLE

4

Intruder colony

6

colony

9

strange ~7

strange 0

Marked with ~7cy urine

+

+

+

+

Reaction 0 cy

_

_

_

_

_

_

_

submissive

submissive

submissive

submissive

posture

posture

posture

posture

Other colony d reaction

TABLE

5

Alpha male removed Intruder colony 6

colony 9

strange 6

strange 0

+

+

+

i

_

_

Marked with ~3cy urine New alpha d reaction

’

’ Hierarchical

Experiment The

5

mentioned)

reactions when

the

reorganizational urine

of the

members,

TABLE Alpha

could

be observed

an animal,

male (whether

When

+

reorganization.

same

strange

_

+

strange

(no

statistical

or a subordinated

male

with

was

marked

could be observed.

alpha

male

having all the ensuing

differences

or not to the group,

that of a dominant

disputes colony

belonging

it was benefits

urine

However,

considered (Table

strange

of a colony when the

with

was marked

only

male

by the

6).

male removed Marked colony

with 8

urine

of colony

0

strange

+ +

+

+ _

+

+

_

+

d

Colony

0

+

+ _

Strange

8

+

Strange

P

+

New alpha

’ Hierarchical

’ reorganization.

strange

+

Colony

6 reaction

d

+ _

0

test of a

5). internal

was marked

6

Intruder

last

urine

male) (Table animal,

the intruder

dominant

the

with

with

colony

33 TABLE

7

Reintroduction

Marked with urine of colony d

colony 0

strange 8

strange 0

Colony 8 LY

+

+

+

+

Other colony d reaction’

-

-

+

_

Final status

6 N recoveredits status after combats

I Social reorganization.

Experiment 6 In a last group of tests the colony alpha male, marked with the urine of a colony subordinated male or that of a strange male, was reintroduced (Table 7). In the first case, the alpha male needed to regain its status. It is remarkable that no piloerection, confrontations or lateral attacks were observed. Only a short fight was observed between some colony males and the alpha male (31.5 _t 4.31 s of offensive posture, 1.75 k 0.35 bites and 0.25 t_ 0.5 lesions from the alpha male toward the other colony males). In the second case, the alpha male was attacked as intruder by one of the colony males, but generally the alpha male recovered its status after a few fights. Nevertheless, some important differences with the control experiment could be observed. For example, duration of postures of threat, confrontation, boxing and chase/flight was shorter than that of the control test. Besides, while in the first test only the alpha male adopted offensive postures, in this case both individuals did so, though males from the colony assumed submissive postures as soon as the alpha male attacked them furiously (8.75 k 0.96 bites and 3.25 f 0.5 lesions). It is noteworthy that no lateral attack appeared at all as opposed to the control test in which it lasted 123.75 + 7.89 s. These results make the statistical differences great (ANOVA P < 0.001 and Tukey-Kramer test P < O.Ol), which seems to be due to the fact that the alpha male was not known as such due to the odour with which it was impregnated. So then it was attacked as a strange male by other males from the colony it had to regain its status as dominant with typical fights of social reorganization (different to those shown in fights against intruders).

Discussion Of all the tests done, the maximum number of bites and lesions were observed in the cases in which the intruder presented a strange male odour. The results show that odours also play an important role in the establishment of social relations between members of the same familiar group, and that such odours differentiate one animal from another in the colony. The results also suggest the existence of a “family component” in odours, typical and exclusive to each colony, which serves to the differentiate territory and members of a

34 colony

from

unique

and exclusive

the other the

the

group). The

Probably,

(19711,

(1976).

to

manner. such

(1975)

with

aggression odours

results

a strange

Hurst

(1989),

investigating

the test odour

familiar

odours

measured

were

time

accepting the possibility tioned

odours

were

family

marks

the

spent

lack

this

encounters.

marks

social

aggressive

behaviour

the other

subordinate

marks

that

results

suggest

reason,

delimit

classic In

towards males. a territory

that

the

is confirmed

when

they

in

were

preceding

of continued suggest,

and

territory.

behaviour

behaviour

the behaviour intruders On

the other

intruders

that

of cases intruders

depends

for this

intruders

an unknown of Williams

differ-

measured

to show

by the data of

the assertion

et al. (1990)

the

spent

between

animal

invading resident

in

the time

the

area do so fearfully. with

we have

lines

differentiating

with

from

of

to which

In our work, marking

without

to an

on the closeness

of the individual

territory

we disagree

and

area, the alpha male

has been masked

lose confrontations

by the investigations

area

the aforemen-

explanation

Hurst

of all males,

hand,

marking we have

familiar

of the alpha male (the only

discourage enter

low

that when

is displayed. the

in our experiments)

do not

in the

If the presence

He

of a new area. The

not attach great importance

that this

assessed

closely

more than

in our work

in the aforementioned

we think

having

or marked

invasion

One

In his

spent

on the test odour.

comparatively

demonstrate

families

families.

of time

Even though

does

mice to urine

of whole

unfamiliar

deposited

the intruder.

aggressive

house

marks

investigated

is that in his experiments,

Therefore

in the majority

conclusion

although

and the marking

positions.

present

male of the colony

possibility

and

of odours

our results

towards

without

of wild

did not deter from

investigation

of the defended point,

Another

investigating their

the results,

is also detected,

final

of marks

not generally

male urine.

on

in its territory,

belongs

aggression-elicited did not respond

probability

due to the amount

unfamiliar

be that the alpha

measured

an killed

the natural

investigation

ence could

the mark

of

and Thor

but, as our results

responses

of

to an individual

the mark to the centre

the findings

of the victims

the

1976),

resident

were

stimuli

and reacts aggressively

mark found

and Thor,

with

Flannelly

Pups

movement

by

in aggressiveness

not attacked because,

in

dnd

reduces

from

to odours

is provoked odour

attacked

the behavioural

of Hurst’s

belong

were

respond Luciano’s.

home area, including

males towards

the

pheromones,

to the mechanism and

and

intruders

with

which

Flannelly

(1975)

not

were

and to the frequency

odour

findings

of adult

relevant relations

are in agreement

a decreased

factor

mice collected

and unfamiliar

curious

response

their

in response

that unfamiliar

most

1973;

of individual

suggests

likely

be one

investigated

within

the differences

did

of diverse

to

outside

of aggressiveness.

1990)

urine

they

to exist,

is not recognized

result

in social

that anosmic

seems

sex and status

composition.

Mackintosh

but they

Most

may

and Galef,

encountered

and the work

(Alberts

role

and

odour,

manner

the

of information

are in disagreement

odour.

an attack

are

in their

in rats. They

Dixon

resident’s

are the releasers

odours

not

behaviour)

an aggression-elicited

marked

items

component”

to communicate

at least, status

variations

has emphasized

the

serves

components

several

(1974a,b),

a “personal

which

play a significant

(territorial

present

and following

time,

(because,

subtle

provide

odours

detect The

odour

through

Payne

Luciano

failing

these

results

conspecific

against an intruder Rails

same

of the same colony

individualism

present

At the

to each individual,

members

obtaining which

intruder.

that the area. For

Our this

individuals.

This

not to mention

other

studies. his

work,

non-pregnant

Hurst

females

also

argues

was observed,

fact has also been confirmed

that

prolonged

investigation

of

both by the males and the females

in our experiments.

urine

coming

in the colony.

from This

35

References Alberts,

J.R. and Calef, B.C.,

1971.

Acute anosmia in the rat: A behavioural test of a peripherally

induced olfactory deficit. Physiol. Alberts,

J.R. and Galef, B.G.,

Behav., 6: 619-621.

1973.

Olfactory

cues and movement:

aggression in the wild Norway rat. J. Comp. Physiol. Birke, L.I.A.

and Sadler, D., 1984.

Scent-marking

Psychol.,

Stimuli

mediating intraspecific

85: 2333242.

behaviour in response to conspecific odours by the

rat, Rattus norvegicus. Anim. Behav., 32: 493-500. Blanchard,

R.J. and Blanchard,

D.C.,

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