Male Barbary macaques eavesdrop on mating outcome: a playback study

doi:10.1016/j.anbehav.2007.12.003

Animal Behaviour

Volume 75, Issue 6, June 2008, Pages 1885-1891

https://doi.org/10.1016/j.anbehav.2007.12.003 Get rights and content

Female copulation calls have been viewed as being addressed to the mating partner, to ensure male protection and mate guarding or, alternatively, to other males, to incite male competition. In a previous study, we found that copulation calls of female Barbary macaques, Macaca sylvanus; given during ejaculatory matings differed from those given during nonejaculatory matings and hence provided potential information about mating outcome to listeners. In this playback study, we tested whether this variation is salient to male listeners. In addition, we assessed the influence of cues from other modalities that are related to female receptivity on male responses to copulation calls. The study was conducted on Barbary macaques living in the enclosure ‘La Forêt des Singes’, at Rocamadour, France. Males responded more rapidly and more strongly, and spent more time walking and in the vicinity of females, after playbacks of calls given during ejaculatory copulations than after those given during nonejaculatory copulations. Responses, however, were not influenced by the cycle stage of the female whose calls were played back. The results suggest that male Barbary macaques appear to discount contextual information in favour of information related to mating outcome when allocating their mating effort.

Section snippets

Study Site and Subjects

The study was conducted during the mating seasons of 2005–2006 and 2006–2007 in the outdoor enclosure ‘La Forêt des Singes’ in Rocamadour, France (size: 20 ha), a visitor park where monkeys range freely, while visitors are restricted to a path. Study subjects belonged to three social groups (‘Petit Bassin’: 25 adult females, 18 adult males; ‘Grand Bassin’: 21 adult females, 8 adult males; ‘Volerie’: 19 adult females, 15 adult males) and were individually recognizable by tattoos and individual

Playback

The presentation of ejaculatory and nonejaculatory copulation calls resulted in different male responses. All males tested reacted when presented with an ejaculatory copulation call; 14 looked and four approached the speaker. In contrast, after the presentation of nonejaculatory calls three of the males showed no response, 14 looked and one approached the speaker. The type of copulation call (ejaculatory versus nonejaculatory) tended to influence the category of male response, although this was

Discussion

After playback of female copulation calls that were originally given during ejaculatory matings, males spent more time looking, walking and in the close vicinity of other females than after the presentation of calls given during nonejaculatory matings. Note that we did not expect males to spend more time in the vicinity of the particular female whose calls were played back as we ensured that this female was nowhere near the male subject. Also in terms of response categories (rise, approach),

Acknowledgments

We thank Ellen Merz for permission to conduct this study in ‘La Forêt des Singes’ at Rocamadour, and Géròme Lagarrigue and George Martins for support in the field. We are grateful to Dani Hönig and Matthis Drolet who helped carry out the playback experiments and Andrea Heistermann and Kornelius Kimmich for support in hormone analyses.

References (36)

K. Brauch et al.
Female sexual behavior and sexual swelling size as potential cues for males to discern the female fertile phase in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar
Hormones and Behavior
(2007)
A. Engelhardt et al.
Assessment of female reproductive status by male longtailed macaques, Macaca fascicularis, under natural conditions
Animal Behaviour
(2004)
J. Fischer et al.
Baboon responses to graded bark variants
Animal Behaviour
(2001)
S.B. Hrdy
Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females
Ethology and Sociobiology
(1979)
A. Leitao et al.
Within-song complexity in a songbird is meaningful to both male and female receivers
Animal Behaviour
(2006)
S. Semple
Individuality and male discrimination of female copulation calls in the yellow baboon
Animal Behaviour
(2001)
J.O. Wolff et al.
Promiscuous females protect their offspring
Trends in Ecology & Evolution
(2004)
J. Altmann
Observational study of behavior: sampling methods
Behaviour
(1974)
E. Behboodi et al.
The use of a urinary estrone conjugates assay for detection of optimal mating time in the cynomolgus macaque (Macaca fascicularis)
Journal of Medical Primatology
(1991)
Brauch, K. 2007. Male and female reproductive strategies in relation to paternity outcome in Barbary macaques (Macaca...

C. Darwin

The Descent of Man, and Selection in Relation to Sex

(1871)

G. De Turckheim et al.

Breeding Barbary macaques in outdoor open enclosures

Deag, J. M. 1974. A study of the social behaviour and ecology of the wild Barbary macaque, Macaca sylvanus L. Ph.D....

C.M. Drea

Bateman revisted: the reproductive tactics of female primates

Integrative and Comparative Biology

(2005)

J. Fischer et al.

Development of infant baboons' responses to graded bark variants

Proceedings of the Royal Society of London, Series B

(2000)

P. Haccou et al.

Statistical Analyses of Behavioural Data

(1994)

K. Hammerschmidt et al.

Maternal discrimination of offspring vocalizations in Barbary macaques (Macaca sylvanus)

Primates

(1998)

M. Heistermann et al.

Female ovarian cycle phase affects the timing of male sexual activity in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar

American Journal of Primatology

(2007)

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Male Barbary macaques eavesdrop on mating outcome: a playback study

Section snippets

Study Site and Subjects

Playback

Discussion

Acknowledgments

Hormones and Behavior

Animal Behaviour

Animal Behaviour

Ethology and Sociobiology

Animal Behaviour

Animal Behaviour

Trends in Ecology & Evolution

Observational study of behavior: sampling methods

Behaviour

The use of a urinary estrone conjugates assay for detection of optimal mating time in the cynomolgus macaque (Macaca fascicularis)

Journal of Medical Primatology

The Descent of Man, and Selection in Relation to Sex

Breeding Barbary macaques in outdoor open enclosures

Bateman revisted: the reproductive tactics of female primates

Integrative and Comparative Biology

Development of infant baboons' responses to graded bark variants

Proceedings of the Royal Society of London, Series B

Statistical Analyses of Behavioural Data

Maternal discrimination of offspring vocalizations in Barbary macaques (Macaca sylvanus)

Primates

Female ovarian cycle phase affects the timing of male sexual activity in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar

American Journal of Primatology