The dark side of the red ape: male-mediated lethal female competition in Bornean orangutans

Abstract

Female Bornean orangutans (Pongo pygmaeus wurmbii) are mainly solitary and philopatric, leading to adult female relatives sharing adjacent and overlapping home ranges. Females tend to be intolerant of unrelated females, with whom they also may have overlapping home ranges. However, fights that lead to injuries are extremely rare and lethal aggression had never been observed. Here, we report the first case of lethal female-female aggression during over 26,000 h of focal data collected on adult females at Tuanan, Central Kalimantan: A young female, who had recently lost her infant, attacked an old resident female. The interaction’s unique feature was that the attacking female was supported by an unflanged male, who had been in consort with her during the week preceding the attack and was responsible for the lethal injuries to the victim. The victim received protection from a flanged male who was probably attracted to the noise generated by the fight. We conclude that even in a species in which coercion is frequently observed in male-female interactions, female leverage over males can coax males into providing services, such as coalitionary support.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2

References

  1. Arora N, van Noordwijk MA, Ackermann C et al (2012) Parentage-based pedigree reconstruction reveals female matrilineal clusters and male-biased dispersal in nongregarious Asian great apes, the Bornean orang-utans (Pongo pygmaeus). Mol Ecol 21:3352–3362

    CAS  Article  PubMed  Google Scholar 

  2. Ashbury A (2013) Not all who wander are lost: the socio-spatial dynamics of home range establishment among young female orangutans (Pongo pygmaeus wurmbii) at Tuanan. MSc Thesis, University of Zurich

  3. Ashbury AM, Posa MRC, Dunkel LP, Spillmann B, Utami Atmoko SS, van Schaik CP, van Noordwijk MA (2015) Why do orangutans leave the trees? Terrestrial behavior among wild Bornean orangutans (Pongo pygmaeus wurmbii) at Tuanan, Central Kalimantan. Am J Primatol 77:1216–1229

    Article  PubMed  Google Scholar 

  4. Campbell CJ (2006) Lethal intragroup aggression by adult male spider monkeys (Ateles geoffroyi). Am J Primatol 68:1197–1201

    Article  PubMed  Google Scholar 

  5. Dunkel LP, Arora N, van Noordwijk MA, Utami Atmoko SS, Putra AP, Krützen M, van Schaik CP (2013) Variation in developmental arrest among male orangutans: a comparison between a Sumatran and a Bornean population. Front Zool 10:12

    Article  PubMed  PubMed Central  Google Scholar 

  6. Edwards SD, Snowdon CT (1980) Social behavior of captive, group-living orangutans. Int J Primatol 1:39–62

    CAS  Article  Google Scholar 

  7. Fox EA (2002) Female tactics to reduce sexual harassment in the Sumatran orangutan (Pongo pygmaeus abelii). Behav Ecol Sociobiol 52:93–101

    Article  Google Scholar 

  8. Goodall J (1986) The chimpanzees of gombe. Harvard University Press, Cambridge

    Google Scholar 

  9. Gouzoules H (1980) A description of genealogical rank changes in a troop of Japanese monkeys (Macaca fuscata). Primates 21:262–267

    Article  Google Scholar 

  10. Gros-Louis J, Perry S, Manson J (2003) Violent coalitionary attacks and intraspecific killing in wild white-faced capuchin monkeys (Cebus capucinus). Primates 44:341–346

    Article  PubMed  Google Scholar 

  11. Husson SJ, Wich SA, Marshall AJ et al (2009) Orangutan distribution, density, abundance and impacts of disturbance. In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, New York, pp 77–96

    Google Scholar 

  12. Knott CD (1998) Orangutans in the wild. National Geographic, http://ngm.nationalgeographic.com/2008/11/orangutans/knott-text. Accessed 14 Aug 2015

  13. Knott CD, Beaudrot L, Snaith T, White S, Tschauner H, Planansky G (2008) Female-female competition in Bornean orangutans. Int J Primatol 29:975–997

    Article  Google Scholar 

  14. Knott CD, Thompson E, Stumpf MR, McIntyre MH (2010) Female reproductive strategies in orangutans, evidence for female choice and counterstrategies to infanticide in a species with frequent sexual coercion. Proc R Soc Lond B 277:105–113

    Article  Google Scholar 

  15. Kunz JA (2015) Ontogeny and variability of play behaviour in wild, immature Bornean (Pongo pygmaeus wurmbii) and Sumatran orangutans (Pongo abelii). MSc Thesis, University of Zurich

  16. Lewis RJ (2002) Beyond dominance: the importance of leverage. Q Rev Biol 77:149–164

    Article  PubMed  Google Scholar 

  17. Marty PR, Cadilek M, Dunkel LP, Agil M, Heistermann M, Willems EP, van Noordwijk MA, Weingrill T (2015) Endocrinological morrelates of male bimaturism in wild Bornean orangutans. Am J Primatol 77:1170–1178

    CAS  Article  PubMed  Google Scholar 

  18. Miller L (1998) Fatal attack among wedge-capped bapuchins. Folia Primatol 69:89–92

    CAS  Article  PubMed  Google Scholar 

  19. Mitani JC, Watts DP, Amsler SJ (2010) Lethal intergroup aggression leads to territorial expansion in wild chimpanzees. Curr Biol 20:R507–R508

    CAS  Article  PubMed  Google Scholar 

  20. Mitra Setia T, Delgado RA, Utami Atmoko SS, Singleton I, van Schaik CP (2009) Social organization and male-female relationships. In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, New York, pp 235–244

    Google Scholar 

  21. Morrogh-Bernard H, Morf N, Chivers D, Krützen M (2011) Dispersal patterns of orang-utans (Pongo spp.) in a Bornean peat-swamp forest. Int J Primatol 32:362–376

    Article  Google Scholar 

  22. Palombit RA (1993) Lethal territorial aggression in a white-handed gibbon. Am J Primatol 31:311–318

    Article  Google Scholar 

  23. Scarry CJ, Tujague MP (2012) Consequences of lethal intragroup aggression and alpha male replacement on intergroup relations and home range use in tufted capuchin monkeys (Cebus apella nigritus). Am J Primatol 74:804–810

    Article  PubMed  Google Scholar 

  24. Seyfarth RM (1978) Social relationships among adult male and female baboons. I. Behaviour during sexual consortship. Behaviour 64:204–226

    Article  Google Scholar 

  25. Singleton I, van Schaik CP (2002) The social organisation of a population of Sumatran orang-utans. Folia Primatol 73:1–20

    Article  PubMed  Google Scholar 

  26. Starin ED (1994) Philopatry and affiliation among red colobus. Behaviour 130:253–270

    Article  Google Scholar 

  27. Tajima T, Kurotori H (2010) Nonaggressive interventions by third parties in conflicts among captive Bornean orangutans (Pongo pygmaeus). Primates 51:179–182

    Article  PubMed  Google Scholar 

  28. Talebi MG, Beltrão-Mendes R, Lee PC (2009) Intra-community coalitionary lethal attack of an adult male southern muriqui (Brachyteles arachnoides). Am J Primatol 71:860–867

    CAS  Article  PubMed  Google Scholar 

  29. Utami Atmoko SS, Singleton I, van Noordwijk MA, van Schaik CP, Mitra Setia T (2009) Male-male relationships in orangutans. In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, New York, pp 225–233

    Google Scholar 

  30. Valero A, Schaffner CM, Vick LG, Aureli F, Ramos-Fernandez G (2006) Intragroup lethal aggression in wild spider monkeys. Am J Primatol 68:732–737

    Article  PubMed  Google Scholar 

  31. van Noordwijk MA, van Schaik CP (2009) Intersexual food transfer among orangutans: do females test males for coercive tendency? Behav Ecol Sociobiol 63:883–890

    Article  Google Scholar 

  32. van Noordwijk MA, Arora N, Willems EP, Dunkel LP, Amda RN, Mardianah N, Ackermann C, Krützen M, Schaik CP (2012) Female philopatry and its social benefits among Bornean orangutans. Behav Ecol Sociobiol 66:823–834

    Article  Google Scholar 

  33. van Noordwijk MA, Willems EP, Utami Atmoko SS, Kuzawa C, van Schaik CP (2013) Multi-year lactation and its consequences in Bornean orangutans (Pongo pygmaeus wurmbii). Behav Ecol Sociobiol 67:805–814

    Article  Google Scholar 

  34. van Schaik CP (1999) The socioecology of fission-fusion sociality in orangutans. Primates 40:69–86

    Article  PubMed  Google Scholar 

  35. van Schaik CP (2000) Infanticide by male primates: the sexual selection hypothesis revisited. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 27–60

    Google Scholar 

  36. van Schaik CP, Wich SA, Utami SS, Odom K (2005) A simple alternative to line transects of nests for estimating orangutan densities. Primates 46:249–254

    Article  PubMed  Google Scholar 

  37. Wartmann FM, Purves RS, van Schaik CP (2010) Modelling ranging behaviour of female orang-utans: a case study in Tuanan, Central Kalimantan, Indonesia. Primates 51:119–130

    Article  PubMed  Google Scholar 

  38. Wich S, Sterck E (2007) Familiarity and threat of opponents determine variation in Thomas langur (Presbytis thomasi) male behaviour during between-group encounters. Behaviour 144:1583–1598

    Article  Google Scholar 

  39. Wich SA, de Vries H, Ancrenaz M, Perkins L, Shumaker RW, Suzuki A, van Schaik CP (2009) Orangutan life history variation. In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, New York, pp 65–75

    Google Scholar 

  40. Wilson EO (1975) Sociobiology. Belknap, Cambridge

    Google Scholar 

  41. Wilson ML, Boesch C, Fruth B et al (2014) Lethal aggression in Pan is better explained by adaptive strategies than human impacts. Nature 513:414–417

    CAS  Article  PubMed  Google Scholar 

  42. Wrangham RW (1999) Evolution of coalitionary killing. Yearb Phys Anthropol 42:1–30

    Article  Google Scholar 

  43. Wrangham RW, Glowacki L (2012) Intergroup aggression in chimpanzees and war in Nomadic hunter-gatherers. Evaluating the chimpanzee model. Hum Nat 23:5–29

    Article  PubMed  Google Scholar 

  44. Zucker EL (1987) Control of intragroup aggression by a captive male orangutan. Zoo Biol 6:219–223

    Article  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the Indonesian Institute of Science (LIPI), the Indonesian State Ministry for Research and Technology (RISTEK), the Director General Departemen Kehutanan (PHKA), Departamen Dalam Negri, the local government in Central Kalimantan, the BKSDA Palangkaraya, the Bornean Orangutan Survival Foundation (BOSF), and the MAWAS in Palangkaraya for their permission and support to conduct this research. We also thank the Fakultas Biologi Universitas Nasional (UNAS) in Jakarta for their collaboration and support for the Tuanan project and in particular Dr. Tatang Mitra Setia. We are indebted to the Tuanan field team for their contribution to data collection, in particular Pak Rahmatd, Pak Yandi, Tono, Idun, Kumpo, Suwi, Abuk, and Wilhelm Osterman as well as many local and foreign students and their financial supporters. For major financial support, we thank the University of Zurich, the A.H. Schultz Stiftung, Philadelphia Zoo, as well as USAID (APS-497-11-000001 to E.R.V.). This research complied with the current national laws of Indonesia. We also thank the two anonymous reviewers for their helpful feedback.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Anna M. Marzec.

Ethics declarations

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Funding

This study was funded by the University of Zurich (grant number not available), A.H. Schultz-Stiftung zur Förderung Primatologischer Forschung (grant number not available), United States Agency for International Development (USA) (APS-497-11-000001), and Philadelphia Zoo (grant number not available).

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Significance statement

In this paper, we report the first observed case of female-female lethal aggression in orangutans. This case was extraordinary because the attacking young female recruited the help of a male, who caused the injuries that eventually killed the old, resident female. The old female that was attacked subsequently received protection from a male. The males were thus in effect acting as hired guns. The effective recruitment of males into conflicts between females is novel and unique among apes. It shows an unsuspected degree of leverage of sexually attractive females over unrelated males and can coax males into providing services, such as coalitionary support, in a species otherwise better known for their sexual coercion by males.

Communicated by R. Noë

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 35 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Marzec, A.M., Kunz, J.A., Falkner, S. et al. The dark side of the red ape: male-mediated lethal female competition in Bornean orangutans. Behav Ecol Sociobiol 70, 459–466 (2016). https://doi.org/10.1007/s00265-015-2053-3

Download citation

Keywords

  • Orangutan
  • Lethal aggression
  • Coalitionary attack
  • Female-female competition
  • Male support