Male orang-utan bimaturism and reproductive success at Camp Leakey in Tanjung Puting National Park, Indonesia

Abstract

Unlike most mammals, male orang-utans exhibit bimaturism, in that mature individuals express one of two distinct morphological forms. Socially subordinate, ‘unflanged’ males are comparable to females in their size and facial morphology, while socially dominant ‘flanged’ males exhibit extreme sexual dimorphism and secondary sexual characteristics, primarily in the form of cheek pads (‘flanges’). Although male ornaments in other species are often phenotypically plastic, such characteristics in orang-utans are irreversible—and, given that both morphs are sexually mature and can father offspring—their adaptive significance remains unclear. We determined paternity of orang-utans at Camp Leakey in Tanjung Puting National Park, within the home range of one long-term dominant male, Kusasi, before, during and after his period of dominance, in comparison with subordinate male conspecifics. We found that Kusasi fathered substantially more offspring conceived during his dominant period than any other male and that socially subordinate, unflanged males only fathered offspring during periods of rank instability. We conclude that orang-utan male bimaturism is consistent with an evolutionarily stable reproductive strategy and that reproduction within the range of a dominant, flanged male is highly skewed in his favour, while unflanged males may largely wait for reproductive opportunities.

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References

  1. Alexander RD, Hoogland JL, Howard RD, Noonan KM, Sherman PW (1979) Sexual dimorphism and breeding systems in pinnipeds, ungulates, primates, and humans. In: Chagnon NA, Irons W (eds) Evolutionary biology and human social behavior: an anthropological perspective. Duxbury Press, North Scituate, pp 402–435

    Google Scholar 

  2. Anderson CM (1986) Female age: male preference and reproductive success in primates. Int J Primatol 7:305–326

    Article  Google Scholar 

  3. Arandjelovic M, Guschanski K, Schubert G, Harris TR, Thalmann O, Siedel H, Vigilant L (2009) Two-step multiplex polymerase chain reaction improves the speed and accuracy of genotyping using DNA from noninvasive and museum samples. Mol Ecol Resour 9:28–36

    CAS  Article  PubMed  Google Scholar 

  4. Brandt EM, Mitchell G (1971) Parturition in primates: behavior related to birth. In: Rosenblum LA (ed) Primate behavior: developments in field and laboratory research, 2. Academic Press, New York, pp 178–223

    Google Scholar 

  5. Clutton-Brock TH (1985) Size, sexual dimorphism, and polygyny in primates. In: Jungers WL (ed) Size and scaling in primate biology. Plenum Press, New York, pp 51–60

    Google Scholar 

  6. Delgado RA, van Schaik CP (2000) The behavioral ecology and conservation of the orangutan (Pongo pygmaeus): a tale of two islands. Evol Anthropol 9:201–218

    Article  Google Scholar 

  7. Di Fiore A (2005) A rapid genetic method for sex assignment in non-human primates. Conserv Genet 6:1053–1058

    Article  Google Scholar 

  8. 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

    PubMed Central  Article  PubMed  Google Scholar 

  9. Emery Thompson M, Zhou A, Knott CD (2012) Low testosterone correlates with delayed development in male orangutans. PLoS One 7, e47282

    PubMed Central  Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  11. Galdikas BMF (1978) Orangutan adaptation at Tanjung Puting Reserve, Central Borneo. PhD thesis, University of California, Los Angeles

  12. Galdikas BMF (1981) Orangutan reproduction in the wild. In: Graham CE (ed) Reproductive Biology of the Great Apes. Academic Press, New York, pp 281–300

    Google Scholar 

  13. Galdikas BMF (1983) The orangutan long call and snag crashing at Tanjung Puting Reserve. Primates 24:371–384

    Article  Google Scholar 

  14. Galdikas BMF (1985a) Orangutan sociality at Tanjung Puting. Am J Primatol 9:101–119

    Article  Google Scholar 

  15. Galdikas BMF (1985b) Subadult male orangutan sociality and reproductive behavior at Tanjung Puting. Am J Primatol 8:87–99

    Article  Google Scholar 

  16. Galdikas BMF (1985c) Adult male sociality and reproductive tactics among orangutans at Tanjung Puting. Folia Primatol 45:9–24

    Article  Google Scholar 

  17. Galdikas BM, Ashbury A (2013) Reproductive parameters of female orangutans (Pongo pygmaeus wurmbii) 1971–2011, a 40-year study at Tanjung Puting National Park, Central Kalimantan, Indonesia. Primates 54:61–72

    Article  PubMed  Google Scholar 

  18. Galdikas BMF, Wood JW (1990) Birth spacing patterns in humans and apes. Am J Phys Anthropol 83:185–191

    CAS  Article  PubMed  Google Scholar 

  19. Gerald MS (2001) Primate colour predicts social status and aggressive outcome. Anim Behav 61:559–566

    Article  Google Scholar 

  20. Goossens B, Setchell JM, James SS, Funk SM, Chikhi L, Abulani A, Ancrenaz M, Lackman-Ancrenaz I, Bruford MW (2006) Philopatry and reproductive success in Bornean orang-utans (Pongo pygmaeus). Mol Ecol 15:2577–2588

    CAS  Article  PubMed  Google Scholar 

  21. Harrison ME, Chivers DJ (2007) The orang-utan mating system and the unflanged male: a product of increased food stress during the late Miocene and Pliocene? J Hum Evol 52:275–293

    Article  PubMed  Google Scholar 

  22. Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555

    Article  PubMed  Google Scholar 

  23. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  24. Kanthaswamy S, Smith DG (2002) Population subdivision and gene flow among wild orangutans. Primates 43:315–327

    Article  PubMed  Google Scholar 

  25. Kingsley S (1982) Causes of non-breeding and the development of secondary sexual characteristics in the male orang-utan: a hormonal study. In: de Boer LM (ed) The orang-utan, its biology and conservation. Junk, Den Haag, pp 215–229

    Google Scholar 

  26. Knott CD (2009) Orangutans: sexual coercion without sexual violence. In: Muller MN, Wrangham RW (eds) Sexual coercion in primates: an evolutionary perspective on male aggression against females. Harvard University Press, Cambridge, pp 81–111

    Google Scholar 

  27. Knott CD, Emery Thompson M, Stumpf RM, 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 

  28. Kuze N, Dellatore D, Banes GL, Pratje P, Tajima T, Russon AE (2012) Factors affecting reproduction in rehabilitant female orangutans: young age at first birth and short inter-birth interval. Primates 53:181–192

    Article  PubMed  Google Scholar 

  29. Leigh SR, Shea BT (1995) Ontogeny and the evolution of adult body size dimorphism in apes. Am J Primatol 36:37–60

    Article  Google Scholar 

  30. Lewis RJ, van Schaik CP (2007) Bimorphism in male Verreaux’s sifaka in the Kirindy Forest of Madagascar. Int J Primatol 28:159–182

    Article  Google Scholar 

  31. Locke DP, Hillier LW, Warren WC et al (2011) Comparative and demographic analysis of orang-utan genomes. Nature 469:529–533

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  32. MacKinnon JR (1974) The behaviour and ecology of wild orang-utans (Pongo pygmaeus). Anim Behav 22:3–74

    Article  Google Scholar 

  33. MacKinnon JR (1979) Reproductive behavior in wild orangutan populations. In: Hamburg DA, McCown ER (eds) The great apes. Benjamin/Cummings, Menlo Park, pp 256–273

    Google Scholar 

  34. Maggioncalda AN, Sapolsky RM, Czekala NM (1999) Reproductive hormone profiles in captive male orangutans: implications for understanding developmental arrest. Am J Phys Anthropol 109:19–32

    CAS  Article  PubMed  Google Scholar 

  35. Maggioncalda AN, Czekala NM, Sapolsky RM (2000) Growth hormone and thyroid stimulating hormone concentrations in captive male orangutans: implications for understanding developmental arrest. Am J Primatol 50:67–76

    CAS  Article  PubMed  Google Scholar 

  36. Maggioncalda AN, Czekala NM, Sapolsky RM (2002) Male orangutan subadulthood: a new twist on the relationship between chronic stress and developmental arrest. Am J Phys Anthropol 118:25–32

    Article  PubMed  Google Scholar 

  37. Markham R, Groves CP (1990) Weights of wild orang utans. Am J Phys Anthropol 81:1–3

    CAS  Article  PubMed  Google Scholar 

  38. Mitani JC, Gros-Louis J, Richards AF (1996) Sexual dimorphism, the operational sex ratio, and the intensity of male competition in polygynous primates. Am Nat 147:966–980

    Article  Google Scholar 

  39. Mitra Setia T, van Schaik CP (2007) The response of adult orang-utans to flanged male long calls: inferences about their function. Folia Primatol 78:215–226

    Article  PubMed  Google Scholar 

  40. Morin PA, Chambers KE, Boesch C, Vigilant L (2001) Quantitative polymerase chain reaction analysis of DNA from noninvasive samples for accurate microsatellite genotyping of wild chimpanzees (Pan troglodytes verus). Mol Ecol 10:1835–1844

    CAS  Article  PubMed  Google Scholar 

  41. Nietlisbach P, Nater A, Greminger MP, Arora N, Krützen M (2010) A multiplex-system to target 16 male-specific and 15 autosomal genetic markers for orangutans (genus: Pongo). Conserv Genet Res 2:153–158

    Article  Google Scholar 

  42. Nsubuga AM, Robbins MM, Roeder AD, Morin PA, Boesch C, Vigilant L (2004) Factors affecting the amount of genomic DNA extracted from ape faeces and the identification of an improved sample storage method. Mol Ecol 13:2089–2094

    CAS  Article  PubMed  Google Scholar 

  43. Porton I (1997) Birth control options. In: Sodaro C (ed) Orangutan species survival plan husbandry manual. Chicago Zoological Society, Brookfield

    Google Scholar 

  44. Robbins MM (1999) Male mating patterns in wild multimale mountain gorilla groups. Anim Behav 57:1013–1020

    Article  PubMed  Google Scholar 

  45. Rodman PS, Mitani JC (1987) Orangutans: sexual dimorphism in a solitary species. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 146–154

    Google Scholar 

  46. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  47. Schürmann CL (1982) Mating behaviour of wild orang utans. In: de Boer LM (ed) The orang-utan, its biology and conservation. Junk, Den Haag, pp 269–284

    Google Scholar 

  48. Schürmann CL, van Hooff JARAM (1986) Reproductive strategies of the orang-utan: new data and a reconsideration of existing sociosexual models. Int J Primatol 7:265–287

    Article  Google Scholar 

  49. Setchell JM, Dixson AF (2001) Changes in the secondary sexual adornments of male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status. Horm Behav 39:177–184

    CAS  Article  PubMed  Google Scholar 

  50. Short RV (1981) Sexual selection in man and the great apes. In: Graham CE (ed) Reproductive Biology of the Great Apes. Academic, London, pp 319–341

    Google Scholar 

  51. Singleton I, Wich SA, Husson S, Stephens S, Utami-Atmoko SS, Leighton M, Rosen N, Traylor-Holzer K, Lacy R, Byers O (2004) Orangutan population and habitat viability assessment: final report. IUCN SSC Conservation Breeding Specialist Group, Apple Valley

  52. Slate J, Pemberton JM (2007) Admixture and patterns of linkage disequilibrium in a free-living vertebrate population. J Evol Biol 20:1415–1427

    CAS  Article  PubMed  Google Scholar 

  53. Utami Atmoko S, van Hooff JARAM (2004) Alternative male reproductive strategies: male bimaturism in orangutans. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, Cambridge, pp 196–207

    Google Scholar 

  54. Utami Atmoko SS, Mitra Setia T, Goossens B, James SS, Knott CD, Morrogh-Bernard HC, van Schaik CP, van Noordwijk MA (2009a) Orangutan mating behavior and strategies. In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, Oxford, pp 235–244

    Google Scholar 

  55. Utami Atmoko SS, Singleton I, van Noordwijk MA, van Schaik CP, Mitra Setia T (2009b) 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, Oxford, pp 225–234

    Google Scholar 

  56. Utami SS, Goossens B, Bruford MW, de Ruiter JR, van Hooff JARAM (2002) Male bimaturism and reproductive success in Sumatran orang-utans. Behav Ecol 13:643–652

    Article  Google Scholar 

  57. Vallet D, Petit E, Gatti S, Levréro F, Ménard N (2008) A new 2CTAB/PCI method improves DNA amplification success from faeces of Mediterranean (Barbary macaques) and tropical (lowland gorillas) primates. Conserv Genet 9:677–680

    CAS  Article  Google Scholar 

  58. van Hooff JARAM (1995) The orangutan: a social outsider and a social-ecology test case. In: Nadler RD, Galdikas BMF, Sheeran LK, Rosen N (eds) The neglected ape. Plenum Press, New York, pp 153–162

    Google Scholar 

  59. van Noordwijk MA, van Schaik CP (2004) Sexual selection and the careers of primate males: paternity concentration, dominance acquisition tactics and transfer decisions. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: a comparative perspective. Cambridge University Press, Cambridge, pp 208–229

    Google Scholar 

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

    Article  Google Scholar 

  61. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  62. van Schaik CP, van Hooff JARAM (1996) Toward an understanding of the orangutan’s social system. In: McGrew W, Nishida T (eds) Great Ape Societies. Cambridge University Press, Cambridge, pp 3–15

    Google Scholar 

  63. Waits L, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256

    CAS  Article  PubMed  Google Scholar 

  64. Weckerly F (1998) Sexual-size dimorphism: influence of mass and mating systems in the most dimorphic mammals. J Mammal 79:33–52

    Article  Google Scholar 

  65. Wickings EJ, Bossi T, Dixson AF (1993) Reproductive success in the mandrill, Mandrillus sphinx: correlations of male dominance and mating success with paternity, as determined by DNA fingerprinting. J Zool 231:563–574

    Article  Google Scholar 

  66. Yeager CP (1997) Orangutan rehabilitation in Tanjung Puting National Park, Indonesia. Conserv Biol 11:802–805

    Article  Google Scholar 

  67. Zhang Y, Morin PA, Ryder OA, Zhang Y (2001) A set of human tri-and tetra nucleotide microsatellite loci useful for population analyses in gorillas (Gorilla gorilla gorilla) and orangutans (Pongo pygmaeus). Conserv Genet 2:391–395

    Article  Google Scholar 

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Acknowledgments

We thank the Indonesian State Ministry of Research and Technology (RISTEK), the Indonesian State Ministry of Forestry (PHKA), the Indonesian Institute of Sciences (LIPI), the Indonesian Natural Resource Conservation Agency (BKSDA) and the Tanjung Puting National Park Office (BTNTP) for granting their permission to undertake this research and to our formal counterpart, S. H. Limin of CIMTROP at Universitas Palangka Raya, for his generous support of this work. We are indebted to A. E. Leiman OBE, S. Brend, P. A. Racey, S. B. Piertney and L. Howe who were instrumental to facilitating this research; to D. Rachmawan, J. R. Houslay, L. E. Koslowski, E. Tan and the Indonesian assistants who assisted with sample collection; to G. L. Shapiro, A. E. Russon and R. Garriga for their data on Kusasi’s history and to R. J. Turton, M. Arandjelovic and V. Städele for assistance with analyses. We thank the Los Angeles Zoo and Botanical Gardens, Como Park Zoo and Conservatory and Henry Vilas Zoo (all USA) for providing biomaterials from their orang-utans for use in developing the multiplex procedure, following approval by recommendation from the Orangutan Species Survival Plan (SSP). We are grateful for the comments of M. A. van Noordwijk and two anonymous reviewers, which greatly improved this manuscript.

Funding

This work was supported by the University of Aberdeen (UoA) Expedition Fund; UoA Small Grants Fund; UoA Alumni Annual Fund; the John Reid Trust; the Royal Geographical Society with Institute of British Geographers; the Royal Scottish Geographical Society; the Gilchrist Educational Trust; the Orangutan Foundation UK; the North of England Zoological Society at Chester Zoo; Darwin College, University of Cambridge; the Primate Society of Great Britain Charles A Lockwood Memorial Grant; the ARCUS Foundation; the Leverhulme Centre for Human Evolutionary Studies, University of Cambridge; the Miss Millie Foundation; Henry Vilas Zoo; The Orang-utan Conservation Genetics Trust and the Max Planck Society. GLB was supported by the Orang Utan Republik Foundation through the 2012 LP Jenkins Memorial Fellowship and by the German Academic Exchange Service (DAAD). The long-term research conducted at Camp Leakey, which facilitated this genetic study, was primarily funded by the Orangutan Foundation International.

Compliance with ethical standards

All applicable international, national and/or institutional guidelines for the care and use of animals were followed. Biological samples were exported from the Republic of Indonesia and from the United States of America to the European Union, via the United Kingdom, with permits 14459/IV/SATS-LN/2008, 00459/IV/SATS-LN/2011, 11US49805A/9 and 477248/01-27 under the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). All experiments described herein comply with the current laws of the countries in which they were performed. The authors declare that they have no conflict of interest.

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Communicated by M. A. van Noordwijk

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Banes, G.L., Galdikas, B.M.F. & Vigilant, L. Male orang-utan bimaturism and reproductive success at Camp Leakey in Tanjung Puting National Park, Indonesia. Behav Ecol Sociobiol 69, 1785–1794 (2015). https://doi.org/10.1007/s00265-015-1991-0

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Keywords

  • Male bimaturism
  • Sexual selection
  • Secondary sexual characteristics
  • Paternity
  • Reproductive success