Ultrasound and aggressive behaviour in rats and other small mammals

doi:10.1016/S0003-3472(72)80177-5

Animal Behaviour

Volume 20, Issue 1, February 1972, Pages 88-100

https://doi.org/10.1016/S0003-3472(72)80177-5 Get rights and content

Abstract

Aggressive behaviour has been observed in rats, Rattus norvegicus, and fourteen other species of small mammals. Ultrasounds were detected during aggressive behaviour in at least seven of these species, and in rats two distinct types of signal were recorded. Short ultrasounds of 3 to 65 ms duration and at frequencies of about 50 kHz were produced in aggressive situations, while long pulses up to 3400 ms duration and at about 25 kHz appeared to be synchronous with the long exhalations of submissive rats. Aggressive behaviour was reduced in encounters where long pulses were emitted. The physical characteristics of the ultrasounds produced by the different species are described and the importance of these signals in the establishment and maintenance of social relationships in small mammals is discussed.

References (35)

AndersonJ.W.
The production of ultrasonic sounds by laboratory rats and other mammals
Science, N.Y.
(1954)
BaileyN.T.J.
BarnettS.A.
BarnettS.A.
Rats. Scient. Am.
(1967)
BroughtonW.B.
Method in bio-acoustic terminology
BrownA.M.
Bimodal cochlear response curves in rodents
Nature, Lond.
(1970)
BrownA.M.
High frequency responsiveness in rodents at the level of the inferior colliculus
Nature, Lond.
(1971)
BrownL.E.
Home range and movement of small mammals
Symp. zool. Soc. Lond.
(1966)
ChanceM.R.A.
An interpretation of some agonistic postures: the role of ‘cut off’ acts and postures
Symp. zool. Soc. Lond.
(1962)
ClarkeJ.E.
The aggressive behaviour of the vole
Behaviour
(1965)

ColliasN.E.

Aggressive behaviour among vertebrate animals

Physiol. Zool.

(1944)

CrowcroftP.

Notes on the behaviour of shrews

Behaviour

(1955)

CrowcroftP.

Social organization and territorial behaviour in the wild house mouse (Mus musculus L.)

Proc. zool. Soc. Lond.

(1963)

Eibl-EibesfeldtI.

Gefangenschaftsbeobachtungen an der Wüstenmaus (Meriones persicus persicus Blanford): Ein Beitrag zur vergleichenden Ethologie der Nager

Z. Tierpsychol.

(1951)

EisenburgJ.F.

Studies on the behaviour of Peromyscus maniculatus gambelii and Peromyscus californicus parasiticus

Behaviour

(1962)

GrantE.C.

An analysis of the social behaviour of male laboratory rat

Behaviour

(1963)

GrantE.C. et al.

A comparison of the social postures of some common laboratory rodents

Behaviour

(1963)

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Ultrasound and aggressive behaviour in rats and other small mammals

Abstract

The production of ultrasonic sounds by laboratory rats and other mammals

Science, N.Y.

Rats. Scient. Am.

Method in bio-acoustic terminology

Bimodal cochlear response curves in rodents

Nature, Lond.

High frequency responsiveness in rodents at the level of the inferior colliculus

Nature, Lond.

Home range and movement of small mammals

Symp. zool. Soc. Lond.

An interpretation of some agonistic postures: the role of ‘cut off’ acts and postures

Symp. zool. Soc. Lond.

The aggressive behaviour of the vole

Behaviour

Aggressive behaviour among vertebrate animals

Physiol. Zool.

Notes on the behaviour of shrews

Behaviour

Social organization and territorial behaviour in the wild house mouse (Mus musculus L.)

Proc. zool. Soc. Lond.

Gefangenschaftsbeobachtungen an der Wüstenmaus (Meriones persicus persicus Blanford): Ein Beitrag zur vergleichenden Ethologie der Nager

Z. Tierpsychol.

Studies on the behaviour of Peromyscus maniculatus gambelii and Peromyscus californicus parasiticus

Behaviour

An analysis of the social behaviour of male laboratory rat

Behaviour

A comparison of the social postures of some common laboratory rodents

Behaviour