Mating in the presence of a competitor: audience effects may promote male social tolerance in polyandrous siamang (Symphalangus syndactylus) groups

in Behaviour
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?



Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.



Help

Have Institutional Access?



Access content through your institution. Any other coaching guidance?



Connect

Audience effects on sexual behavior, including changes in copulation frequency and duration in the presence of conspecifics, have been reported in multimale–multifemale groups of several primate species. We examined the interaction of male sexual behavior with group composition and within-group mating pattern in a population of siamangs (Symphalangus syndactylus) containing unimale–unifemale groups and multimale–unifemale groups using mixed models. Aggression in a sexual context was never observed. As predicted, however, copulation rates were lower and copulations were significantly shorter in duration in two-male groups than in unimale groups, even if copulations involving subordinate males were excluded. Dominant males monopolized copulations with the group female in most groups, but copulations were shared among males in three stable two-male groups. When both resident males copulated with the group’s female, there was no evidence that copulating pairs moved to secluded areas, and the duration of copulations did not differ between males. These results are consistent with the hypothesis that male–male tolerance in multimale siamang groups is facilitated by adjustments to sexual behavior in the presence of a sexual competitor.

Sections

References

AdlerN.T. (1969). Effects of the male’s copulatory behavior on successful pregnancy of the female rat. — J. Comp. Physiol. Psychol. 69: 613-622.

AlbertsS.AltmannJ.WilsonM.L. (1996). Mate guarding constrains foraging activity of male baboons. — Anim. Behav. 51: 1269-1277.

AltmannJ. (1974). Observational study of behavior: sampling methods. — Behaviour 49: 227-267.

BarelliC.MatsudairaK.WolfT.RoosC.HeistermannM.HodgesK.IshidaT.MalaivijitnondS.ReichardU.H. (2013). Extra-pair paternity confirmed in wild white-handed gibbons. — Am. J. Primatol. 75: 1185-1195.

BeachF.A. (1976). Sexual attractivity, proceptivity, and receptivity in female mammals. — Horm. Behav. 7: 105-138.

BirkheadT.R.AtkinL.MøllerA.P. (1987). Copulation behavior in birds. — Behaviour 101: 101-138.

BrockelmanW.Y. (2009). Ecology and the social system of gibbons. — In: The gibbons: new perspectives on small ape socioecology and population biology ( LappanS.WhittakerD.J., eds). Springer, New York, NY, p.  211-240.

BruceK.E.EstepD.Q. (1992). Interruption of and harrassment during copulation by stumptailed macaques, Macaca arctoides. — Anim. Behav. 44: 1029-1044.

CampbellC. (2006). Copulation in free-ranging black-handed spider monkeys (Ateles geoffroyi). — Am. J. Primatol. 68: 507-511.

CantJ.JohnstoneR.A. (2000). Power struggles, dominance testing, and reproductive skew. — Am. Nat. 155: 406-417.

ChapaisB. (1983). Reproductive activity in relation to male dominance and the likelihood of ovulation in rhesus monkeys. — Behav. Ecol. Sociobiol. 12: 215-228.

ChiversD.J. (1974). The siamang in Malaya: a field study of a primate in tropical rain forest. — Karger, Basel.

ClayZ.ZuberbühlerK. (2012). Communication during sex among female bonobos: effects of dominance, solicitation, and audience. — Sci. Rep. 2: 291.

Clutton-BrockT.H. (1998). Reproductive skew, concessions and limited control. — Trends Ecol. Evol. 13: 288-292.

DaviesN.B.HartleyI.R.HatchwellB.J.LangmoreN.E. (1996). Female control of copulations to maximize male help: a comparison of polygynandrous alpine accentors, Prunella collaris, and dunnocks, P. modularis. — Anim. Behav. 51: 27-47.

deCatanzaroD.MacNivenE.RucciutiF. (1991). Comparison of the adverse effects of adrenal and ovarian steroids on early pregnancy in mice. — Psychoneuroendocrinology 16: 525-536.

DewsburyD.A. (1972). Patterns of copulatory behavior in male mammals. — Q. Rev. Biol. 47: 1-33.

DickensonJ.L. (2001). Extrapair copulations in western bluebirds (Sialia mexicana): female receptivity favors older males. — Behav. Ecol. Sociobiol. 50: 423-429.

DuboisF.BelzileA. (2012). Audience effect alters male mating preferences in zebra finches (Taeniopygia guttata). — PLoS ONE 7: e43697.

EdvardssonM.CanalD. (2006). The effects of copulation duration in the bruchid beetle Callosobruchus maculatus. — Behav. Ecol. 17: 430-434.

ElderA.A. (2013). Competition among three primate species at Way Canguk, Sumatra, Indonesia. — Unpubl. PhD thesis, Stony Brook University, Stony Brook, NY.

ErskineM.S.KornbergE.CherryJ.A. (1989). Paced copulation in rats: effects of intromission frequency and duration on luteal activation and estrous length. — Physiol. Behav. 45: 33-39.

FuentesA. (2000). Hylobatid communities: changing views on pair bonding and social organization in hominoids. — Yrbk. Phys. Anthropol. 43: 33-60.

GillC.J.RissmanE.F. (1997). Female sexual behavior is inhibited by short- and long-term food restriction. — Physiol. Behav. 61: 387-394.

HimuroC.FujisakiK. (2012). The effects of male harassment on mating duration in the seed bug, Togo hemipterus. — Endomol. Exp. Appl. 142: 53-59.

HohmannG.FruthB. (2003). Intra- and inter-sexual aggression by bonobos in the context of mating. — Behaviour 140: 1389-1413.

HunterF.M.PetrieM.OtronenM.BirkheadT.R.MøllerA.P. (1993). Why do females copulate repeatedly with one male?Trends Ecol. Evol. 8: 21-26.

JansonC. (1984). Female choice and mating system of the brown capuchin monkey Cebus apella (Primates: Cebidae). — Z. Tierpsychol. 65: 177-200.

KaburuS.S.K.InoueS.Newton-FisherN.E. (2013). Death of the alpha: within-community lethal violence among chimpanzees of the Mahale Mountains National Park. — Am. J. Primatol. 75: 789-797.

KinnairdM.F.O’BrienT.G. (1998). Ecological effects of wildfire on lowland rainforest in Sumatra. — Conserv. Biol. 12: 954-956.

LappanS. (2005). Biparental care and male reproductive strategies in siamangs (Symphalangus syndactylus) in southern Sumatra. — Dissertation, New York University, New York, NY.

LappanS. (2007a). Patterns of dispersal in Sumatran siamangs (Symphalangus syndactylus): preliminary mtDNA evidence suggests more frequent male than female dispersal to adjacent groups. — Am. J. Primatol. 69: 692-698.

LappanS. (2007b). Social relationships among males in multi-male siamang groups. — Int. J. Primatol. 28: 369-387.

LindsayD.R.DunsmoreD.G.WilliamsJ.D.SymeG.J. (1976). Audience effects on the mating behaviour of rams. — Anim. Behav. 24: 818-821.

LinklaterW.L.CameronE.Z. (2000). Tests for cooperative behavior between stallions. — Anim. Behav. 60: 731-734.

MansonJ.H. (1994). Male aggression: a cost to female mate choice in Cayo Santiago rhesus macaques. — Anim. Behav. 48: 473-475.

MansonJ.H. (1996). Male dominance and mount series duration in Cayo Santiago rhesus macaques. — Anim. Behav. 51: 1219-1231.

MarlerC.A.MooreM.C. (1989). Time and energy costs of aggression in testosterone-implanted free-living male mountain spiny lizards (Sceloporus jarrovi). — Physiol. Zool. 62: 1334-1350.

MatosR.SchluppI. (2005). Performing in front of an audience: signallers and the social environment. — In: Animal communication networks ( McGregorP.K., ed.). Cambridge University Press, Cambridge.

Matsumoto-OdaA. (1999). Female choice in the opportunistic mating of wild chimpanzees (Pan troglodytes schweinfurthii) at Mahali. — Behav. Ecol. Sociobiol. 46: 258-266.

MitaniJ.C. (1984). The behavioral regulation of monogamy in gibbons (Hylobates muelleri). — Behav. Ecol. Sociobiol. 15: 225-229.

MitaniJ.C. (1987). Territoriality and monogamy among agile gibbons (Hylobates agilis). — Behav. Ecol. Sociobiol. 20: 265-269.

MøllerA.P.BirkheadT.R. (1989). Copulation behaviour in mammals: evidence that sperm competition is widespread. — Biol. J. Linn. Soc. 38: 119-131.

MorinoL. (2009). Monogamy in mammals: expanding the perspective on Hylobatid mating systems. — In: The gibbons: new perspectives on small ape socioecology and population biology ( LappanS.WhittakerD.J., eds). Springer, New York, NY, p.  279-312.

MorinoL. (2012). Behavioral endocrinology of wild male siamangs (Symphalangus syndactylus). — Unpubl. PhD thesis, Rutgers University, New Brunswick, NJ.

MummeR.L.KoenigW.D.PitelkaF.A. (1983). Mate guarding in the Acorn Woodpecker: within-group reproductive competition in a cooperative breeder. — Anim. Behav. 31: 1094-1106.

NakamuraM. (1998). Multiple mating and cooperative breeding in polygynandrous alpine accentors I. Competition among females. — Anim. Behav. 56: 259-275.

NicholsonA.J. (1954). An outline of the dynamics of animal populations. — Aust. J. Zool. 2: 9-65.

NurcahyoA. (1999). Studi perilaku harian siamang (Hylobates syndactylus) di taman nasional Bukit Barisan Selatan, Lampung. — Unpubl. BSc thesis, Universitas Gadjah Mada, Yogyakarta.

O’BrienT.G.KinnairdM.F.AntonN.PrasetyaningrumM.D.P.IqbalM. (2003). Fire, demography and the persistence of siamang (Symphalangus syndactylus: Hylobatidae) in a Sumatran rainforest. — Anim. Conserv. 6: 115-121.

Overduin-de VriesA.M.MaassenJ.J.M.SpruijtB.M.SterckE.H.M. (2012). Sneaky monkeys: an audience effect of male rhesus macaques (Macaca mulatta) on sexual behavior. — Am. J. Primatol. 74: 217-228.

PadurL.WedekindJ.ÖztürkO.StreitB.TiedemannR.PlathM. (2009). Do audience effects lead to relaxed male sexual harassment?Behaviour 146: 1739-1758.

PalombitR.A. (1993). Lethal territorial aggression in a monogamous primate. — Am. J. Primatol. 31: 311-318.

PalombitR.A. (1994). Dynamic pair bonds in hylobatids: implications regarding monogamous social systems. — Behaviour 128: 65-101.

ParkerG.A. (1974). Courtship persistence and female guarding as male time investment strategies. — Behaviour 48: 157-184.

PetrieM. (1992). Copulation frequency in birds: why do females copulate more than once with the same male. — Anim. Behav. 44: 790-792.

PilastroA.MandelliM.GaspariniC.DaddaM.BisazzaA. (2007). Copulation duration, insemination efficiency and male attractiveness in guppies. — Anim. Behav. 74: 321-328.

RaemaekersJ.J.RaemaekersP.M. (1985). Field playback of loud calls to gibbons (Hylobates lar): territorial, sex-specific and species-specific responses. — Anim. Behav. 33: 481-493.

Ruiz de ElviraM.HerndonJ.G. (1986). Disruption of sexual behaviour by high ranking rhesus monkeys (Macaca mulatta). — Behaviour 96: 227-240.

SapolskyR.M. (2005). The influence of social hierarchy on primate health. — Science 308: 648-652.

SilkJ.B. (2002). Kin selection in primate groups. — Int. J. Primatol. 23: 849-875.

TonerJ.P.AdlerN.T. (1986). The pre-ejaculatory behavior of male and female rats affects the number of sperm in the vagina and uterus. — Physiol. Behav. 36: 363-367.

TownsendC.R.DeschnerT.ZuberbühlerK. (2008). Female chimpanzees use copulation calls flexibly to prevent social competition. — PLoS ONE 3, DOI:10.1371/journal.pone.0002431.

TownsendC.R.ZuberbühlerK. (2009). Audience effects in chimpanzee copulation calls. — Common Integr. Biol. 2: 282-289.

WattsD.P. (1998). Coalitionary mate guarding by male chimpanzees at Ngogo, Kibale National Park, Uganda. — Behav. Ecol. Sociobiol. 44: 43-55.

Figures

  • Comparison of estimated mean copulation rates (copulations/month) in unimale and multimale groups from the GLMM analyses. Error bars represent 95% confidence intervals of the estimated means. (A) All copulations involving the adult female and male group members. (B) Copulations involving dominant male–female dyads only. p<0.01, ∗∗p<0.001.

    View in gallery
  • Mean duration of copulations by males in stable one-male groups and two-male groups, and an unstable three-male grouping. Means are calculated as means of group means. Error bars represent 95% confidence intervals. (A) All copulations involving the adult female and male group members. (B) Copulations involving dominant male–female dyads only. The three-male group was not included in the LMM analysis. p<0.01, ∗∗p<0.001.

    View in gallery
  • Mean duration of copulations in multimale groups where copulations were monopolized by the dominant male (‘Monopolized’) vs. groups where copulations were shared between two males (‘Shared’). Means were calculated as means of individual means for all individuals for which at least two copulations were observed. Error bars represent 95% confidence intervals. p<0.01, ∗∗p<0.001.

    View in gallery

Information

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 17 17 8
Full Text Views 6 6 6
PDF Downloads 1 1 1
EPUB Downloads 0 0 0