Behavioral Ecology and Sociobiology

, Volume 69, Issue 11, pp 1785–1794 | Cite as

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

  • Graham L. Banes
  • Biruté M. F. Galdikas
  • Linda Vigilant
Original Article

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.

Keywords

Male bimaturism Sexual selection Secondary sexual characteristics Paternity Reproductive success 

Supplementary material

265_2015_1991_MOESM1_ESM.docx (41 kb)
ESM 1(DOCX 41 kb)

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 402–435Google Scholar
  2. Anderson CM (1986) Female age: male preference and reproductive success in primates. Int J Primatol 7:305–326CrossRefGoogle 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 9:28–36CrossRefPubMedGoogle 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 178–223Google 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 51–60CrossRefGoogle 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 9:201–218CrossRefGoogle Scholar
  7. Di Fiore A (2005) A rapid genetic method for sex assignment in non-human primates. Conserv Genet 6:1053–1058CrossRefGoogle 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 10:12PubMedCentralCrossRefPubMedGoogle Scholar
  9. Emery Thompson M, Zhou A, Knott CD (2012) Low testosterone correlates with delayed development in male orangutans. PLoS One 7, e47282PubMedCentralCrossRefPubMedGoogle Scholar
  10. Fox E (2002) Female tactics to reduce sexual harassment in the Sumatran orangutan (Pongo pygmaeus abelii). Behav Ecol Sociobiol 52:93–101CrossRefGoogle Scholar
  11. Galdikas BMF (1978) Orangutan adaptation at Tanjung Puting Reserve, Central Borneo. PhD thesis, University of California, Los AngelesGoogle Scholar
  12. Galdikas BMF (1981) Orangutan reproduction in the wild. In: Graham CE (ed) Reproductive Biology of the Great Apes. Academic Press, New York, pp 281–300Google Scholar
  13. Galdikas BMF (1983) The orangutan long call and snag crashing at Tanjung Puting Reserve. Primates 24:371–384CrossRefGoogle Scholar
  14. Galdikas BMF (1985a) Orangutan sociality at Tanjung Puting. Am J Primatol 9:101–119CrossRefGoogle Scholar
  15. Galdikas BMF (1985b) Subadult male orangutan sociality and reproductive behavior at Tanjung Puting. Am J Primatol 8:87–99CrossRefGoogle Scholar
  16. Galdikas BMF (1985c) Adult male sociality and reproductive tactics among orangutans at Tanjung Puting. Folia Primatol 45:9–24CrossRefGoogle 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 54:61–72CrossRefPubMedGoogle Scholar
  18. Galdikas BMF, Wood JW (1990) Birth spacing patterns in humans and apes. Am J Phys Anthropol 83:185–191CrossRefPubMedGoogle Scholar
  19. Gerald MS (2001) Primate colour predicts social status and aggressive outcome. Anim Behav 61:559–566CrossRefGoogle 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 15:2577–2588CrossRefPubMedGoogle 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 52:275–293CrossRefPubMedGoogle Scholar
  22. Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555CrossRefPubMedGoogle 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 16:1099–1106CrossRefPubMedGoogle Scholar
  24. Kanthaswamy S, Smith DG (2002) Population subdivision and gene flow among wild orangutans. Primates 43:315–327CrossRefPubMedGoogle 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 215–229Google 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 81–111Google 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 277:105–113CrossRefGoogle 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 53:181–192CrossRefPubMedGoogle Scholar
  29. Leigh SR, Shea BT (1995) Ontogeny and the evolution of adult body size dimorphism in apes. Am J Primatol 36:37–60CrossRefGoogle Scholar
  30. Lewis RJ, van Schaik CP (2007) Bimorphism in male Verreaux’s sifaka in the Kirindy Forest of Madagascar. Int J Primatol 28:159–182CrossRefGoogle Scholar
  31. Locke DP, Hillier LW, Warren WC et al (2011) Comparative and demographic analysis of orang-utan genomes. Nature 469:529–533PubMedCentralCrossRefPubMedGoogle Scholar
  32. MacKinnon JR (1974) The behaviour and ecology of wild orang-utans (Pongo pygmaeus). Anim Behav 22:3–74CrossRefGoogle 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 256–273Google 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 109:19–32CrossRefPubMedGoogle 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 50:67–76CrossRefPubMedGoogle 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 118:25–32CrossRefPubMedGoogle Scholar
  37. Markham R, Groves CP (1990) Weights of wild orang utans. Am J Phys Anthropol 81:1–3CrossRefPubMedGoogle 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 147:966–980CrossRefGoogle 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 78:215–226CrossRefPubMedGoogle 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 10:1835–1844CrossRefPubMedGoogle 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 2:153–158CrossRefGoogle 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 13:2089–2094CrossRefPubMedGoogle Scholar
  43. Porton I (1997) Birth control options. In: Sodaro C (ed) Orangutan species survival plan husbandry manual. Chicago Zoological Society, BrookfieldGoogle Scholar
  44. Robbins MM (1999) Male mating patterns in wild multimale mountain gorilla groups. Anim Behav 57:1013–1020CrossRefPubMedGoogle 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 146–154Google Scholar
  46. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106CrossRefPubMedGoogle 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 269–284Google 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 7:265–287CrossRefGoogle 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 39:177–184CrossRefPubMedGoogle 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 319–341Google 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 ValleyGoogle Scholar
  52. Slate J, Pemberton JM (2007) Admixture and patterns of linkage disequilibrium in a free-living vertebrate population. J Evol Biol 20:1415–1427CrossRefPubMedGoogle 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 196–207CrossRefGoogle 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 235–244Google 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 225–234Google 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 13:643–652CrossRefGoogle 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 9:677–680CrossRefGoogle 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 153–162CrossRefGoogle 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 208–229CrossRefGoogle 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 66:823–834CrossRefGoogle 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 4:535–538CrossRefGoogle 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 3–15CrossRefGoogle Scholar
  63. Waits L, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256CrossRefPubMedGoogle Scholar
  64. Weckerly F (1998) Sexual-size dimorphism: influence of mass and mating systems in the most dimorphic mammals. J Mammal 79:33–52CrossRefGoogle 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 231:563–574CrossRefGoogle Scholar
  66. Yeager CP (1997) Orangutan rehabilitation in Tanjung Puting National Park, Indonesia. Conserv Biol 11:802–805CrossRefGoogle 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 2:391–395CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of AberdeenAberdeenUK
  2. 2.Division of Biological Anthropology, Department of Archaeology and AnthropologyUniversity of CambridgeCambridgeUK
  3. 3.Max Planck Institute for Evolutionary AnthropologyLeipzigGermany
  4. 4.Department of ArchaeologySimon Fraser UniversityBurnabyCanada

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