Elsevier

Animal Behaviour

Volume 67, Issue 2, February 2004, Pages 249-259
Animal Behaviour

Male life history and the unusual adult sex ratios of redfronted lemur, Eulemur fulvus rufus, groups

https://doi.org/10.1016/j.anbehav.2003.05.012Get rights and content

Abstract

In group-living species, theoretical considerations indicate the existence of a fundamental conflict of interest between the sexes over the adult sex ratio within groups. Females may derive certain benefits from living with many males. Males, in contrast, should generally try to monopolize access to a group of females. Which sex ultimately controls adult group sex ratio is poorly known. We examined this conflict between the sexes in redfronted lemurs, Malagasy primates characterized by an unusual lack of female-biased adult sex ratios. Using various demographic and behavioural data from several groups collected over 6 years, we examined (1) the proximate determinants of this unusual sex ratio, (2) the temporal distribution of female fertile phases within groups as a determinant of male monopolization potential, (3) sources of between-group variation in the adult sex ratio, and (4) possible social benefits of the relatively high number of males for both sexes. Birth and mortality rates were not sex biased and males migrated considerably more frequently than females, providing no proximate explanation for the unusual sex ratio. However, certain life history traits (fast maturation, short interbirth intervals) may ultimately play a role because they act to facilitate joint group transfers of male coalitions. Despite a relatively small female group size and an associated high monopolization potential, female oestrous synchrony may prevent the formation of single-male groups. Reduced male group size seems to be the main predictor of take-over rate, and, thus, infanticide risk, suggesting that both sexes may benefit from the high number of coresident males, thereby considerably defusing the conflict of interest between the sexes.

Section snippets

Study site and population

The 60-ha study area was in Kirindy Forest, 60 km northeast of Morondava, western Madagascar, within a forestry concession of the Centre de Formation Professionelle Forestière de Morondava and part of the field station of the German Primate Centre (DPZ). For a detailed description of the dry deciduous forest, see Ganzhorn & Sorg (1996). Between 1996 and 2002, 98 individuals from seven groups (A, B, D, F, H, I, J) were captured and individually marked with radiocollars (Biotrack, Wareham,

Results

First, we characterized the adult sex ratio in the lemur groups. The mean female group size was 2.8±0.81 (range 2–4, N=23), whereas male group size was 3.8±1.11 (range 2–7, N=23). The ratio of adult females to males was 1:1.4. There was a significant positive correlation between male and female group size (Spearman correlation by rank: rS=0.532, N=23, P=0.009).

Adult sex ratio is influenced by several factors, such as sex ratio at birth, sex-biased mortality and migration. Of the 45 infants born

Discussion

Our results confirmed that redfronted lemurs live in groups with a male-biased adult sex ratio. Our study suggests that certain life history traits may ultimately play a role in shaping redfronted lemur social organization and that this unusual adult sex ratio may provide benefits for both males and females, thereby considerably defusing the conflict of interest between the sexes.

Acknowledgements

This study was conducted within a collaboration accord between the Laboratoire de Primatologie et de Biologie Evolutive de l'Université d'Antananarivo and the German Primate Centre. We thank Professor Berthe Rakotosamimanana, Dr Rodin Rasoloarison and Léonard Razafimanantsoa for invaluable logistical support throughout this study. Tiana Andrianjanahari, Katrin Böger, Guiseppe Donati, Claudia Fichtel, Roland Hilgartner, Emilien Marc, Carolin Mayer, Nielsen Rabarjiaona, Vero Raharimanantsoa,

References (96)

  • M. Ridley

    The number of males in a primate troop

    Animal Behaviour

    (1986)
  • E.J. Wickings et al.

    Testicular function, secondary sexual development and social status in male mandrills (Mandrillus sphinx)

    Physiology and Behavior

    (1992)
  • B. Wimmer et al.

    The effects of sexual selection and life history on the genetic structure of redfronted lemur, Eulemur fulvus rufus, groups

    Animal Behaviour

    (2002)
  • S.C. Alberts et al.

    Balancing costs and opportunities: dispersal in male baboons

    American Naturalist

    (1995)
  • S.J. Andelman

    Ecological and social determinants of cercopithecine mating patterns

  • C. Borries et al.

    Infanticide in Hanuman langurs: social organization, male migration, and weaning age

  • D.K. Brockman et al.

    Reproduction in free-ranging male Propithecus verreauxi: the hormonal correlates of mating and aggression

    American Journal of Physical Anthropology

    (1998)
  • J.D. Bygott et al.

    Male lions in large coalitions gain reproductive advantages

    Nature

    (1979)
  • J. Chism et al.

    Mating and residence patterns of male patas monkeys

    Ethology

    (1986)
  • M. Cords

    Mating systems of forest guenons: a preliminary review

  • C.M. Crockett et al.

    Infanticide in red howlers: female group size, male membership, and a possible link to folivory

  • C.M. Crockett et al.

    Infanticide in red howler monkeys (Alouatta seniculus)

  • J.H. Crook et al.

    Evolution of primate societies

    Nature

    (1966)
  • G. Donati et al.

    Cathemeral activity of red-fronted brown lemurs (Eulemur fulvus rufus) in the Kirindy Forest/CFPF

  • J.F. Eisenberg et al.

    The relationship between ecology and social structure in primates

    Science

    (1972)
  • S.T. Emlen et al.

    Ecology, sexual selection, and the evolution of mating systems

    Science

    (1977)
  • J.U. Ganzhorn et al.

    Ecology and Economy of a Tropical Dry Forest in Madagascar

    (1996)
  • Gerson, J. S. 2000. Social relationships in wild red-fronted brown lemurs (Eulemur fulvus rufus). Ph.D. thesis, Duke...
  • L.R. Godfrey et al.

    Teeth, brains, and primate life histories

    American Journal of Physical Anthropology

    (2001)
  • A.W. Goldizen

    A comparative perspective on the evolution of tamarin and marmoset social systems

    International Journal of Primatology

    (1990)
  • A.H. Harcourt et al.

    Testis weight, body weight and breeding system in primates

    Nature

    (1981)
  • Hilgartner, R. 2001. Wachsamkeitsuntersuchungen an freilebenden Rotstirnmakis (Eulemur fulvus rufus). M.Sc. thesis,...
  • P.N. Hooge et al.

    Animal Movement Extension to ArcView Version 1.1

    (1997)
  • K. Izard et al.

    Reproduction in the collared lemur (Eulemur fulvus collaris)

    American Journal of Primatology

    (1993)
  • C.H. Janson

    Intra-specific food competition and primate social structure: a synthesis

    Behaviour

    (1988)
  • C.H. Janson et al.

    Predicting group size in primates: foraging costs and predation risks

    Behavioral Ecology

    (1995)
  • R.A. Johnstone

    Models of reproductive skew: a review and synthesis

    Ethology

    (2000)
  • A. Jolly et al.

    Infant killing, wounding and predation in Eulemur und Lemur

    International Journal of Primatology

    (2000)
  • K.C. Jones

    Inter-troop transfer of Lemur catta males at Berenty, Madagascar

    Folia Primatologica

    (1983)
  • P.M. Kappeler

    The evolution of sexual size dimorphism in prosimian primates

    American Journal of Primatology

    (1990)
  • P.M. Kappeler

    Intrasexual selection and phylogenetic constraints in the evolution of sexual canine dimorphism in strepsirhine primates

    Journal of Evolutionary Biology

    (1996)
  • P.M. Kappeler

    Primate socioecology: new insights from males

    Naturwissenschaften

    (1999)
  • P.M. Kappeler

    Convergence and nonconvergence in primate social systems

  • P.M. Kappeler

    Primate males: history and theory

  • P.M. Kappeler

    Causes and consequences of unusual sex ratios among lemurs

  • P.M. Kappeler et al.

    On the move around the clock: correlates and determinants of cathemeral activity in wild redfronted lemurs (Eulemur fulvus rufus)

    Behavioral Ecology and Sociobiology

    (2003)
  • P.M. Kappeler et al.

    Evolution of primate social systems

    International Journal of Primatology

    (2002)
  • P.C. Lee

    Comparative ecology of postnatal growth and weaning among haplorhine primates

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    P. M. Kappeler is at the Abteilung soziobiologie, Deutsches Primatenzentrum, Kellnerweg 4, 37077 Göttingen, Germany.

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