Female reproductive strategies in orangutans, evidence for female choice and counterstrategies to infanticide in a species with frequent sexual coercion

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1678, 2010, Pages 105-113

  Knott, Cheryl Denise ^a   Thompson, Melissa Emery ^b   Stumpf, Rebecca M ^c   McIntyre, Matthew H ^d  

^a USA   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d UNIVERSITY OF CENTRAL FLORIDA   (United States)

Author keywords

Female choice; Infanticide avoidance; Orangutan; Paternity certainty; Post conception mating; Sexual coercion

Indexed keywords

EVOLUTIONARY BIOLOGY; FEMALE BEHAVIOR; INFANTICIDE; MATE CHOICE; PATERNITY; PRIMATE; REPRODUCTIVE STRATEGY; SEXUAL CONFLICT; SEXUAL SELECTION;

AGGRESSION; ARTICLE; CONCEPTION; FEMALE; FEMALE GENITAL SYSTEM; INFANTICIDE; MALE; MALE GENITAL SYSTEM; MATE CHOICE; MATING; NONHUMAN; ORANG UTAN; OVULATION; PRIORITY JOURNAL; SEXUAL BEHAVIOR; SPECIES;

MAMMALIA; PONGO PYGMAEUS; PONGO PYGMAEUS PYGMAEUS;

EID: 73949107360     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2009.1552     Document Type: Article

References (64)

1. Arnqvist, G. & Rowe, L. 2005 Sexual conflict. Princeton, NJ: Princeton University Press.
2. Bailey, D. & Alimadhi, F. 2007 logit.mixed: mixed effects logistic model. In Zelig: everyone's statistical software (eds K. Imai, G. King & O. Lav). http://gking.harvard.edu/zelig.
3. Beaudrot, L. H., Kahlenberg, S. M. & Marshall, A. J. 2009 Why male orangutans do not kill infants. Behav. Ecol. Sociobiol. 63, 1549-1562. (doi:10.1007/s00265-009-0827-1)
4. Chapman, T., Arnqvist, G., Bangham, J. & Rowe, L. 2003 Sexual conflict. Trends Ecol. Evol. 18, 41-47. (doi:10.1016/S0169- 5347(02)00004-6)
5. Connor, R. C., Richards, A. F., Smolker, R. A. & Mann, J. 1996 Patterns of female attractiveness in Indian Ocean bottlenose dolphins. Behaviour 133, 1-109.
6. Czekala, N. M., Shideler, S. E. & Lasley, B. L. 1988 Comparisons of reproductive hormone patterns in the hominoids. In Orang-utan biology (ed. J. H. Schwartz), pp. 117-132. Oxford, UK: Oxford University Press.
7. Delgado, R. A. 2003. The function of adult male long calls in wild orangutans (Pongo pygmaeus). PhD dissertation, Duke University, Durham, NC.
8. Delgado, R. A. 2006 Sexual selection in the loud calls of male primates: signal content and function. Int. J. Primatol. 27, 5-25. (doi:10.1007/s10764-005-9001-4)
9. Dickemann, M. 1979 Female infanticide, reproductive strategies and social stratification. In Evolutionary biology and human social behavior (eds N. Chagnon & W. Irons), pp. 321-367. Duxbury, MA: North Scituate.
10. Emery Thompson, M. 2005 Reproductive endocrinology of wild female chimpanzees (Pan troglodytes schweinfurthii): methodological considerations and the role of hormones in sex and conception. Am. J. Primatol. 67, 137-158. (doi:10.1002/ajp.20174)
11. Engelhardt, A., Hodges, J. K., Niemitz, C. & Heistermann, M. 2005 Female sexual behavior, but not sex skin swelling, reliably indicates the timing of the fertile phase in wild long-tailed macaques (Macaca fascicularis). Horm. Behav. 47, 195-204. (doi:10.1016/j.yhbeh.2004.09.007)
12. Engelhardt, A., Hodges, J. K. & Heistermann, M. 2007 Post-conception mating in wild long-tailed macaques (Macaca fascicularis): characterization, endocrine correlates and functional significance. Horm. Behav. 51, 3-10. (doi:10.1016/j.yhbeh.2006.06.009)
13. Fox, E. A. 1998 The function of female mate choice in the Sumatran orangutan (Pongo pygmaeus abelii). PhD dissertation, Duke University, Durham, NC.
14. Fox, E. 2002 Female tactics to reduce sexual harassment in the Sumatran orangutan (Pongo pygmaeus abelii). Behav. Ecol. Sociobiol. 52, 93-101. (doi:10.1007/s00265-002-0495-x)
15. Galdikas, B. M. F. 1981 Orangutan reproduction in the wild. In Reproductive biology of the great apes (ed. C. E. Graham), pp. 281-300. New York, NY: Academic Press.
16. Galdikas, B. M. F. 1985a Adult male sociality and reproductive tactics among orangutans at Tanjung Puting. Folia Primatol. 45, 9-24. (doi:10.1159/000156188)
17. Galdikas, B. M. F. 1985b Subadult male orangutan sociality and reproductive behavior at Tanjung Puting. Am. J. Primatol. 8, 87-99. (doi:10.1002/ajp.1350080202)
18. Galdikas, B. M. F. & Wood, J. W. 1990 Birth spacing patterns in humans and apes. Am. J. Phys. Anthropol. 83, 185-191. (doi:10.1002/ajpa.1330830207)
19. Gavrilets, S., Arnqvist, G. & Friberg, U. 2001 The evolution of female mate choice by sexual conflict. Proc. R. Soc. Lond. B 268, 531-539. (doi:10.1098/rspb.2000.1382)
20. Goossens, B., Setchell, J. M., James, S. S., Funk, S. M., Chikhi, L., Abulani, A., Ancrenaz, M., Lackman-Ancrenaz, I. & Bruford, M. W. 2006 Philopatry and reproductive success in Bornean orang-utans (Pongo pygmaeus). Mol. Ecol. 15, 2577-2588. (doi:10.1111/j.1365-294X.2006.02952.x)
21. Graham, C. 1988 Reproductive physiology. In Orang-utan biology (ed. J. H. Schwartz), pp. 91-103. Oxford, UK: Oxford University Press.
22. Hestermann, M., Ziegler, T., van Schaik, C. P., Launhardt, K., Winkler, P. & Hodges, J. K. 2001 Loss of oestrus, concealed ovulation, and paternity confusion in free-ranging Hanuman langurs. Proc. R. Soc. Lond. B 268, 2445-2451. (doi:10.1098/rspb.2001.1833)
23. Horr, D. A. 1975 The Borneo orangutan: population structure and dynamics in relationship to ecology and reproductive strategy. In Primate behavior: developments in field and laboratory research, vol. 4 (ed. L. A. Rosenblum), pp. 307-323. New York, NY: Academic Press.
24. Hrdy, S. B. 1979 Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol. Sociobiol. 1, 13-40.
25. Johnson, A., Knott, C., Pamungkas, B., Pasaribu, M. & Marshall, A. 2005 A survey of the orangutan Pongo pygmaeus pygmaeus population in and around Gunung Palung National Park, West Kalimantan, Indonesia based on nest counts. Biol. Conserv. 121, 495-507. (doi:10.1016/j.biocon.2004. 06.002)
26. Kingsley, S. 1982 Causes of non-breeding and the development of the secondary sexual characteristics in the male orang utan: a hormonal study. In The orang utan: its biology and conservation. The Hague, The Netherlands: Dr W. Junk.
27. Knott, C. D. 1996 Field collection and preservation of urine in orangutans and chimpanzees. Tropic Biodivers. 4, 95-102.
28. Knott, C. D. 1998 Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating fruit availability. Int. J. Primatol. 19, 1061-1079. (doi:10.1023/A:1020330404983)
29. Knott, C. D. 1999. Reproductive, physiological and behavioral responses of orangutans in Borneo to fluctuations in food availability. PhD dissertation, Harvard University, Cambridge, MA.
30. Knott, C. D. 2001 Female reproductive ecology of the apes: implications for human evolution. In Reproductive ecology and human evolution (ed. P. Ellison), pp. 429-463. New York, NY: Aldine de Gruyter.
31. Knott, C. D. 2005 Radioimmunoassay of estrone conjugates from urine dried on filter paper. Am. J. Primatol. 67, 121-135. (doi:10.1002/ajp.20173)
32. Knott, C. D. 2009 Orangutans: sexual coercion without sexual violence. In Sexual coercion in primates: an evolutionary perspective on male aggression against females (eds M. N. Muller & R. W. Wrangham), pp. 81-111. Cambridge, MA: Harvard University Press.
33. Knott, C. D. & Kahlenberg, S. 2007 Orangutans in perspective: forced copulations and female mating resistance. In Primates in perspective (eds S. Bearder, C. J. Campbell, A. Fuentes, K. C. MacKinnon & M. Panger), pp. 290-305. Oxford, UK: Oxford University Press.
34. Knott, C., Beaudrot, L., Snaith, T., White, S., Tschauner, H. & Planansky, G. 2008 Female-female competition in Bornean orangutans. Int J Primatol 29, 975-997. (doi:10.1007/s10764-008-9278-1)
35. Kokko, H. 2005 Treat 'em mean, keep 'em (sometimes) keen: evolution of female preferences for dominant and coercive males. Evol Ecol 19, 123-135. (doi:10.1007/s10682-004-7919-1)
36. Kokko, H., Brooks, R., Jenions, M. & Morley, J. 2003 The evolution of mate choice and mating biases. Proc. R. Soc. Lond. B 270, 653-664. (doi:10.1098/rspb.2002.2235)
37. MacKinnon, J. R. 1974 The behaviour and ecology of wild orang-utans (Pongo pygmaeus). Anim. Behav. 22, 3-74. (doi:10.1016/S0003- 3472(74)80054-0)
38. Maggioncalda, A. N., Sapolsky, R. M. & Czekala, N. M. 1999 Reproductive hormone profiles in captive male orangutans: implications for understanding developmental arrest. Am. J. Phys. Anthropol. 109, 19-32. (doi:10.1002/(SICI)1096-8644(199905)109:1〈19::AID-AJPA3〉3.0. CO;2-3)
39. Mallinson, J. 1984 Breeding of great apes at the Jersey Wildlife Preservation Trust and a look into the future. Zoo Biol. 3, 1-11. (doi:10.1002/zoo.1430030102)
40. Mitani, J. 1985 Mating behaviour of male orangutans in the Kutai Game Reserve, Indonesia. Anim. Behav. 33, 391-402.
41. Mitra Setia, T. & van Schaik, C. P. 2007 The response of adult orang-utans to flanged male long calls: inferences about their function. Folia Primatol. 78, 215-226. (doi:10.1159/000102317)
42. Morrogh-Bernard, H. C. et al. 2009 Orangutan activity budgets and diet. In Orangutans: geographic variation in behavioral ecology and conservation (eds A. Wich, S. S. Utami & T. Mitra Setia & C. van Schaik), pp. 119-134. Oxford, UK: Oxford University Press.
43. Nadler, R. D. 1988 Sexual and reproductive behavior. In Orang-utan biology (ed. J. H. Schwartz), pp. 31-51. Oxford, UK: Oxford University Press.
44. Nunn, C. L. 1999 The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Anim. Behav. 58, 229-246. (doi:10.1006/anbe.1999.1159)
45. Pazol, K. 2003 Mating in the Kakamega Forest blue monkeys (Cercopithecus mitis): does female sexual behavior function to manipulate paternity assessment? Behaviour 140, 473-499. (doi:10.1163/156853903322127940)
46. Rijksen, H. D. 1978 A field study on Sumatran orang-utans (Pongo pygmaeus abelii, Lesson 1827): ecology, behaviour, and conservation. Wageningen, The Netherlands: H. Veenman & Zonen B.V.
47. Rodman, P. S. 1979 Individual activity patterns and the solitary nature of orangutans. In The great apes, vol. 5 (eds D. L. Hamburg & E. R. McCown), pp. 234-255. London, UK: W. A. Benjamin.
48. Saayman, G. 1975 The influence of hormonal and ecological factors upon sexual behavior and social organization in Old World primates. In Socioecology and psychology of primates (ed. R. H. Tuttle). The Hague, The Netherlands: Mouton.
49. Schürmann, C. 1982 Mating behaviour of wild orangutans. In The orang utan: its biology and conservation (ed. L. de Boer). The Hague, The Netherlands: W. Junk.
50. Schürmann, C. L. & van Hooff, J. A. R. A. M. 1986 Reproductive strategies of the orang-utan: new data and a reconsideration of existing sociosexual models. Int. J. Primatol. 7, 265-287. (doi:10.1007/BF02736392)
51. Semple, S. & McComb, K. 2000 Perception of female reproductive state from vocal cues in a mammal species. Proc. R. Soc. Lond. B 267, 707-712. (doi:10.1098/rspb.2000.1060)
52. Smuts, B. B. & Smuts, R. W. 1993 Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Adv. Study Behav. 22, 1-63. (doi:10.1016/S0065- 3454(08)60404-0)
53. Stumpf, R. M. & Boesch, C. 2005 Does promiscuous mating preclude female choice? Female sexual strategies in chimpanzees (Pan troglodytes verus) of the Tai National Park, Côte d'Ivoire. Behav. Ecol. Sociobiol. 57, 511-524. (doi:10.1007/s00265-004-0868-4)
54. Stumpf, R. M., Emery Thompson, M. & Knott, C. 2008 A comparison of female mating strategies in Pan troglodytes and Pongo spp. Int. J. Primatol. 29, 865-884. (doi:10.1007/s10764-008-9284-3)
55. Trivers, R. M. 1972 Parental investment and sexual selection. In Sexual selection and the descent of man, 1871-1971 (ed. B. Campbell), pp. 136-179. Chicago, IL: Aldine.
56. Utami, S. & Setia, T. M. 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 (eds R. D. Nadler, B. F. M. Galdikas, L. K. Sheeran & N. Rosen), pp. 183-190. New York, NY: Plenum Press.
57. Utami, S. S., Goossens, B., Bruford, M. W., de Ruiter J. R. & van Hooff, J. A. R. A. M. 2002 Male bimaturism and reproductive success in Sumatran orangutans. Behav. Ecol. 13, 643-652. (doi:10.1093/beheco/13.5. 643)
58. van Noordwijk, M. A. & van Schaik, C. P. 2000 Reproductive patterns in eutherian mammals: adaptations against infanticide? In Infanticide by males (eds C. P. van Schaik & C. H. Janson), pp. 322-360. Cambridge, UK: Cambridge University Press.
59. van Schaik, C. P. 2000a Infanticide by male primates: the sexual selection hypothesis revisited. In Infanticide by males (eds C. P. van Schaik & C. H. Janson), pp. 27-60. Cambridge, UK: Cambridge University Press.
60. van Schaik, C. P. 2000b Vulnerability to infanticide by males: patterns among mammals. In Infanticide by males (eds C. P. van Schaik & C. H. Janson), pp. 61-71. Cambridge, UK: Cambridge University Press.
61. van Schaik, C. P., Pradhan, G. R. & van Noordwijk, M. A. 2004 Mating conflict in primates: infanticide, sexual harassment and female sexuality. In Sexual selection in primates: new and comparative perspectives (eds P. M. Kappeler & C. P. van Schaik), pp. 131-150. Cambridge, UK: Cambridge University Press.
62. Wallen, K. 2001 Sex and context: hormones and primate sexual motivation. Horm. Behav. 40, 339-357. (doi:10.1006/hbeh.2001.1696)
63. Wich, S. A., Utami-Atmoko, S. S., Setia, T. M., Rijksen, H. D., Schürmann, C., van Hooff, J. A. R. A. M. & van Schaik, C. P. 2004 Life history of wild Sumatran orangutans (Pongo abelii). J. Hum. Evol. 47, 385-398. (doi:10.1016/j.jhevol.2004.08.006)
64. Ziegler, T. E. 2007 Female sexual motivation during non-fertile periods: a primate phenomenon. Horm. Behav. 51, 1-2. (doi:10.1016/j.yhbeh. 2006.09.002)