Skip to main content Accessibility help
×
Hostname: page-component-76fb5796d-zzh7m Total loading time: 0 Render date: 2024-04-26T21:12:17.136Z Has data issue: false hasContentIssue false

11 - Alternative male reproductive strategies: male bimaturism in orangutans

Published online by Cambridge University Press:  10 August 2009

Suci Utami Atmoko
Affiliation:
Faculty of Biology National University, Jakarta, Indonesia
Jan A. R. A. M. van Hooff
Affiliation:
Ethology and Socio-ecology, Utrecht University, Utrecht, The Netherlands
Peter M. Kappeler
Affiliation:
Deutsches Primatenzentrum, Göttingen, Germany
Carel P. van Schaik
Affiliation:
Duke University, North Carolina
Get access

Summary

INTRODUCTION

An individual's lifetime reproductive success is determined by the degree to which it copes with the various challenges that it faces in the different stages of its life. These challenges change constantly from early juvenility until late adulthood (Setchell & Lee, this volume). They require corresponding adaptive variation in the tactics of survival and reproduction, as the animal passes through the successive phases of its life cycle. This dynamic change takes its most dramatic form in those species where an individual goes through one or several distinct larval stages before becoming a reproductively active adult. Apart from such successive changes, there are also variations in fitness-maximising tactics that coexist side by side. In this chapter we deal specifically with such parallel or alternative fitness trajectories in a primate, the orangutan, a species with two adult, sexually mature male morphs. A recent study by Utami et al. (2002) has shown that these two male morphs exist side by side in a natural population and that each morph can and does produce offspring, suggesting that they represent parallel alternative reproductive tactics. Here we review the pertinent evidence.

It has long been an established fact in ethology that interactions with social partners influence an individual's motivational state and vice versa, and, through interactions, its physiological development and condition. For example, the suppression of reproductive processes by the presence of a same-sex conspecific has been documented for many species, including primates.

Type
Chapter
Information
Sexual Selection in Primates
New and Comparative Perspectives
, pp. 196 - 207
Publisher: Cambridge University Press
Print publication year: 2004

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alexander, R. D., Hoogland, J. L., Howard, R. D., Noonan, K. M. & Sherman, P. W. 1979. Sexual dimorphisms and breeding systems in pinnipeds, ungulates, primates and humans. In Evolutionary Biology and Human Social Behaviour: An Anthropological Perspective, ed. N. A. Chagnon & W. A. Irons. Belmont: Wadsworth, pp. 402–603
Andrés, J. A., Sánchez-Guillén, R. A. & Cordero Rivera, A. 2002. Evolution of female colour polymorphism in damselflies: testing the hypotheses. Animal Behaviour, 63, 677–85CrossRefGoogle Scholar
Andrews, P. & Cronin, J. E. 1982. The relationship of Sivapithecus and Ramapithecus and the evolution of the orang-utan. Nature, 297, 541–6CrossRefGoogle Scholar
Andrews, P. & Martin, L. 1987. Cladistic relationships of extant and fossil hominoids. Journal of Human Evolution, 16, 101–18CrossRefGoogle Scholar
Berard, J. D., Nurnberg, P., Epplen, J. T. & Schmidtke, J. 1994. Alternative reproductive tactics and reproductive success in male rhesus macaques. Behaviour, 129, 177–201CrossRefGoogle Scholar
Bercovitch, F. B. 1996. Testicular function and scrotal coloration in patas monkeys. Journal of Zoology, London, 107, 93–100CrossRefGoogle Scholar
Darwin, C. 1871. The Descent of Man and Selection in Relation to Sex. Princeton, NJ: Princeton University Press
Delgado, R. A. & Schaik, C. P. 2000. The behavioral ecology and conservation of the orangutan (Pongo pygmæus): a tale of two islands. Evolutionary Anthropology, 9, 201–183.0.CO;2-Y>CrossRefGoogle Scholar
Dixson, A. F. & Herbert, J. 1974. The effects of testosterone on the sexual skin and genitalia of the male talapoin monkey. Journal of Reproduction and Fertility, 38, 217–19CrossRefGoogle ScholarPubMed
Dixson, A. F., Bossi, T. & Wickings, E. J. 1993. Male dominance and genetically determined reproductive success in mandrills (Mandrillus sphinx). Primates, 34, 525–32CrossRefGoogle Scholar
Fleagle, J. G. 1988. Primate Adaptation and Evolution. New York, NY: Academic Press
Galdikas, B. M. F. 1979. Orangutan adaptation at Tanjung Puting Reserve: mating and ecology. In The Great Apes, ed. D. A. Hamburg & E. R. McCown. New York, NY: Academic Press, pp. 195–233
Galdikas, B. M. F. 1985a. Subadult male orangutan sociality and reproductive behavior at Tanjung Puting. International Journal of Primatology, 8, 87–99CrossRefGoogle Scholar
Galdikas, B. M. F. 1985b. Adult male sociality and reproductive tactics among orangutans at Tanjung Puting Reserve. Folia Primatologica, 45, 9–24CrossRefGoogle Scholar
Galdikas, B. M. F. 1995. Social and reproductive behavior of wild adolescent female orangutans. In The Neglected Ape, ed. R. D. Nadler, B. M. F. Galdikas, L. K. Sheeran & N. Rosen. New York, NY: Plenum Press, pp. 163–82
Goossens, B., Chikhi, L., Utami, S. S., Ruiter, J. & Bruford, M. W. 2000. A multi-samples, multi-extracts approach for microsatellite analysis of faecal samples in an arboreal ape. Conservation Genetics, 1, 157–62CrossRefGoogle Scholar
Graham, C. E. 1988. Reproductive physiology. In Orang-Utan Biology, ed. J. H. Schwartz. New York, NY: Oxford University Press, pp. 91–103
Gross, M. R. 1996. Alternative reproductive strategies and tactics: diversity within sexes. Trends in Ecology and Evolution, 11, 92–8CrossRefGoogle ScholarPubMed
Horr, D. A. 1975. The Borneo orang utan: population structure and dynamics in relationship to ecology and reproductive strategy. In Primate Behavior, ed. L. A. Rosenblum, vol. 4. New York, NY: Academic Press, 307–23
Horr, D. A. 1977. Orang utan maturation: growing up in a female world. In Primate Biosocial Development: Biological, Social and Ecological Determinants, ed. S. Chevalier-Skolnikoff & F. E. Poirer. New York, NY: Garland, pp. 289–322
Isbell, L. A. 1995. Seasonal and social correlates of changes in hair, skin and scrotal condition in vervet monkeys (Cercopithecus æthiops) of Amboseli National Park, Kenya. American Journal of Primatology, 36, 61–70CrossRefGoogle Scholar
Jarman, P. J. 1983. Mating system and sexual dimorphism in large terrestrial mammalian herbivores. Biological Reviews, 58, 485–520CrossRefGoogle Scholar
Jarman, P. J. & Southwell, C. J. 1986. Grouping, associations, and reproductive strategies in eastern grey kangaroos. In Ecolological Aspects of Social Evolution, ed. D. I. Rubenstein & R. W. Wrangham. Princeton, NJ: Princeton University Press, pp. 399–428
Jolicœur, P. 1985. A flexible 3-parameter curve for limited or unlimited somatic growth. Growth, 49, 271–81Google ScholarPubMed
Kingsley, S. R. 1982. Causes of non-breeding and the development of secondary sexual characteristics in the male orang-utan: a hormonal study. In The Orang-Utan, Its Biology and Conservation, ed. L. E. M. de Boer. Den Haag: Junk, pp. 215–29
Kingsley, S. R. 1988. Physiological development of male orang-utans and gorillas. In Orang-Utan Biology, ed. J. H. Schwartz. New York, NY: Oxford University Press, pp. 123–31
Knott, C. 1998. Orangutans in the wild. National Geographic Society, 194, 30–57Google Scholar
Koolhaas, J. M., de Boer, S. F., Buwalda, B. et al. 2001. How and why coping systems vary among individuals. In Coping with Challenge: Welfare in Animals Including Humans, ed. D. Broom. Dahlem: Dahlem University Press, pp. 199–211
Lank, D. B., Smith, C. M., Hanotte, O., Burke, T. & Cooke, F. 1995. Genetic polymorphism for alternative mating behavior in lekking male ruff Philomachus pugnax. Nature, 378, 59–62CrossRefGoogle Scholar
Leigh, S. R. 1995. Socioecology and the ontogeny of sexual dimorphism in anthropoid primates. American Journal of Physical Anthropology, 97, 339–56CrossRefGoogle ScholarPubMed
Leigh, S. R. & Shea, B. T. 1995. Ontogeny and the evolution of adult body size dimorphism in apes. American Journal of Primatology, 36, 37–60CrossRefGoogle Scholar
Leighton, M., Seal, U. S., Soemarma, K. et al. 1995. Orangutan life history and vortex analysis. In The Neglected Ape, ed. R. D. Nadler, B. M. F. Galdikas, L. K. Sheeran & N. Rosen. New York, NY: Plenum Press, pp. 97–107
MacKinnon, J. R. 1974. The behaviour and ecology of wild orang-utans (Pongo pygmaeus). Animal Behaviour, 22, 3–74CrossRefGoogle Scholar
MacKinnon, J. R. 1979. Reproductive behaviour in wild orangutan populations. In The Great Apes, ed. D. A. Hamburg & E. R. McCown. Menlo Park, CA: Benjamin/Cummings, pp. 256–73
MacKinnon, J. R. 1989. Field studies of wild orang-utans: current state of knowledge. In Perspectives in Primate Biology, Vol. 3, ed. P. K. Seth & S. Seth. New Dehli: Today's and Tomorrow's Publishers, pp. 173–86
Maggioncalda, A. N. 1995. The socioendocrinology of orangutan growth, development, and reproduction – an analysis of endocrine profiles of juvenile, developing adolescent, developmentally arrested adolescent, adult, and aged captive male orangutans. Ph. D. dissertation, Duke University, Durham
Maggioncalda, A. N., Sapolsky, R. M. & Czekala, N. M. 1999. Reproductive hormone profiles in captive male orangutans: implications for understanding developmental arrest. American Journal of Physical Anthropology, 109, 19–323.0.CO;2-3>CrossRefGoogle ScholarPubMed
Maggioncalda, A. N., Czekala, N. M. & Sapolsky, R. M. 2000. Growth hormone and thyroid stimulating hormone concentrations in captive male orangutans: implications for understanding developmental arrest. American Journal of Primatology, 50, 67–763.0.CO;2-V>CrossRefGoogle ScholarPubMed
Maple, T. L., Zucker, E. L. & Dennon, M. B. 1979. Cyclic proceptive behavior in a captive female orang-utan (Pongo pygmæus abelii). Behavioural Processes, 4, 53–9CrossRefGoogle Scholar
Mitani, J. C. 1985a. Sexual selection and adult male orang utan long calls. Animal Behaviour, 33, 272–83CrossRefGoogle Scholar
Mitani, J. C. 1985b. Mating behaviour of male orang utans in the Kutai Game Reserve, Indonesia. Animal Behaviour, 33, 392–402CrossRefGoogle Scholar
Mitani, J. C., Grether, G. F., Rodman, P. S. & Priatna, D. 1991. Associations among wild orang-utans: sociality, passive aggregations or chance?Animal Behaviour, 42, 33–46CrossRefGoogle Scholar
Moore, M. C. 1991. Application of organization-activation theory to alternative male reproductive strategies: a review. Hormones and Behavior, 28, 96–115Google Scholar
Moore, M. C., Hews, D. K. & Knapp, R. 1998. Evolution and hormonal control of alternative male phenotypes. American Zoologist, 38, 133–51CrossRefGoogle Scholar
Nadler, R. D. 1977. Sexual behavior of captive orangutans. Archives of Sexual Behavior, 6, 457–75CrossRefGoogle ScholarPubMed
Nadler, R. D. 1981. Laboratory research on sexual behavior of the great apes. In Reproductive Biology of the Great Apes: Biomedical and Comparative Perspectives, ed. C. E. Graham. New York, NY: Academic Press, pp. 191–238
Nadler, R. D. 1995. Sexual behavior of orangutans (Pongo pygmæus). In The Neglected Ape, ed. R. D. Nadler, B. M. F. Galdikas, L. K. Sheeran & N. Rosen. New York, NY: Plenum Press, pp. 223–37
Pilbeam, D., Rose, M. D., Barry, J. C. & Shah, S. M. I. 1990. New Sivapithecus humeri from Pakistan and the relationship of Sivapithecus and Pongo. Nature, 284, 447–8Google Scholar
Plavcan, J. M. 1999. Mating systems, intrasexual competition and sexual dimorphism in primates. In Comparative Primate Socioecology, ed. P. C. Lee. Cambridge: Cambridge University Press, pp. 241–26
Plavcan, J. M. & Schaik, C. P. 1992. Intrasexual competition and canine dimorphism in primates. American Journal of Physical Anthropology, 87, 461–77CrossRefGoogle ScholarPubMed
Rhodes, L., Argersinger, M. E., Gantert, L. T.et al. 1998. Effects of administration of testosterone, dihydrotestosterone, oestrogen and fadrazole, an aromatase inhibitor, on sex skin colour in intact male rhesus macaques. Journal of Reproduction and Fertility, 111, 51–7CrossRefGoogle Scholar
Rijksen, H. D. 1978. A Fieldstudy on Sumatran Orang Utans (Pongo pygmaeus abelii Lesson 1827). Wageningen: H. Veenman & B. V. Zonen
Rodman, P. S. 1973. Population composition and adaptive organisation among orang-utans of the Kutai Reserve. In Comparative Ecology and Behaviour of Primates, ed. H. D. Crook. London: Academic Press, pp. 171–209
Rodman, P. S. 1977. Feeding behaviour of orang-utans in the Kutai Nature Reserve, East Kalimantan. In Primate Ecology, ed. T. H. Clutton Brock. London: Academic Press, pp. 383–413
Rodman, P. S. & Mitani, J. C. 1987. Orangutans: sexual dimorphism in a solitary species. In Primate Societies, ed. B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker. Chicago, IL: University of Chicago Press, pp. 146–54
Ryan, M. J. & Wagner, B. A. 1987. ‘Alternative’ mating behavior in the swordtails Xiphophorus nigrensis and Xiphophorus pygmaeus (Pisces: Poeciliidae). Behavioral Ecology and Sociobiology, 24, 341–8CrossRefGoogle Scholar
Ryan, M. J., Pease, C. M. & Morris, R. M. 1992. A genetic polymorphism is the swordtail Xiphophorus nigrensis: testing the prediction of equal fitness, American Naturalist, 139, 21–31CrossRefGoogle Scholar
Schürmann, C. L. 1982. Courtship and mating behavior of wild orangutans in Sumatra. In Primate Behavior and Sociobiology, ed. A. B. Chiarelli & R. S. Corrucini. Berlin: Springer Verlag, pp. 129–35
Schürmann, C. L. & Hooff, J. A. R. A. M. 1986. Reproductive strategies of the orang-utan: new data and a reconsideration of existing sociosexual models. International Journal of Primatology, 7, 265–87CrossRefGoogle Scholar
Schwartz, J. H. 1984. The evolutionary relationships of man and orang-utans. Nature, 308, 501–5CrossRefGoogle ScholarPubMed
Setchell, J. M. & Dixson, A. F. 2001a. Changes in the secondary sexual adornments of male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status. Hormones and Behavior, 39, 177–84CrossRefGoogle Scholar
Setchell, J. M. & Dixson, A. F. 2001b. Circannual changes in the secondary sexual adornments of semifree-ranging male and female mandrills (Mandrillus sphinx). American Journal of Primatology, 53, 109–213.0.CO;2-I>CrossRefGoogle Scholar
Setchell, J. M. & Dixson, A. F. 2002. Developmental variables and dominance rank in adolescent male mandrills (Mandrillus sphinx). American Journal of Primatology, 56, 9–25CrossRefGoogle Scholar
Shuster, S. M. & Wade, M. J. 1991. Equal mating success among male reproductive strategies in a marine isopod. Nature, 350, 608–10CrossRefGoogle Scholar
Smuts, B. B. 1985. Sex and Friendship in Baboons. New York, NY: Aldine
Sugardjito, J. 1986. Ecological constraints on the behaviour of Sumatran orang-utans (Pongo pygmæus abelii) in the Gunung Leuser National Park, Indonesia. Ph. D. thesis, University of Utrecht
Sugardjito, J., Boekhorst, I. J. A. & Hooff, J. A. R. A. M. 1987. Ecological constraints on the grouping of wild orang-utans (Pongo pygmaeus) in the Gunung Leuser National Park, Sumatra, Indonesia. International Journal of Primatology, 8, 17–41CrossRefGoogle Scholar
te Boekhorst, I. J. A., Schürmann, C. L. & Sugardjito, J. 1990. Residential status and seasonal movements of wild orang-utans in the Gunung Leuser Reserve (Sumatra, Indonesia). Animal Behaviour, 39, 1098–109CrossRefGoogle Scholar
Uchida, A. 1996. Craniodental variation among the great apes. Peabody Museum Bulletin, 4, 1–186Google Scholar
Utami Atmoko, S. 2000. Bimaturism in orang-utan males: reproductive and ecological strategies. Ph. D. thesis, University of Utrecht
Utami, S. & Mitra Setia, T. 1995. Behavioral changes in wild male and female Sumatran orangutans (Pongo pygmaeus abelii) during and following a resident male take-over. In The Neglected Ape, ed. R. D. Nadler, B. M. F. Galdikas, L. K. Sheeran & N. Rosen. New York, NY: Plenum Press, pp. 183–90
Utami, S. S., Wich, S. A., Sterck, E. H. M. & Hooff, J. A. R. A. M. 1997. Food competition between wild orangutans in large fig trees. International Journal of Primatology, 18, 909–27CrossRefGoogle Scholar
Utami, S. S., Goossens, B., Bruford, M. W., Ruiter, J. R. & Hooff, J. A. R. A. M. 2002. Male bimaturism and reproductive success in Sumatran orang-utans. Behavioral Ecology, 13, 643–52CrossRefGoogle Scholar
Vandenburgh, J. G. 1965. Hormonal basis of the sex skin in male rhesus monkeys. General and Comparative Endocrinology, 5, 31–4CrossRefGoogle Scholar
van Hooff, J. A. R. A. M. 1995. The orangutan: a social outsider and a social-ecology test case. In The Neglected Ape, ed. R. D. Nadler, B. M. F. Galdikas, L. K. Sheeran & N. Rosen. New York, NY: Plenum Press, pp. 153–62
van Hooff, J. A. R. A. M. 2000. Relationships among non-human primate males: a deductive framework. In Primate Males, ed. P. M. Kappeler. Cambridge University Press: Cambridge, pp. 183–91
Hooff, J. A. R. A. M. & Schaik, C. P. 1994. Male bonds: affiliative relationships among nonhuman primate males. Behaviour, 130, 143–51Google Scholar
Rhijn, J. G. 1973. Behavioural dimorphism in male ruffs, Philomachus pugnax (L.). Behaviour, 47, 153–229CrossRefGoogle Scholar
van Schaik, C. P. & van Hooff, J. A. R. A. M. 1996. Toward an understanding of the orangutan's social system. In Great Ape Societies, ed. W. C. McGrew, L. F. Marchant & T. Nishida. Chicago, IL: University of Chicago Press, pp. 3–15
Weckerly, F. 1998. Sexual-size dimorphism: influence of mass and mating systems in the most dimorphic mammals. Journal of Mammalogy, 79, 33–52CrossRefGoogle Scholar
Wickings, E. J., Bossi, T. & Dixson, A. F. 1993. Reproductive success in the mandrill, Mandrillus sphinx: correlations of male dominance and mating success with paternity, as determined by DNA fingerprinting. Journal of Zoology, London, 231, 563–74CrossRefGoogle Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×