Juggling Priorities: Female Mating Tactics in Phayre's Leaf Monkeys

American Journal of Primatology

Volumn 74, Issue 5, 2012, Pages 471-481

  Lu, Amy ^a,b,c   Beehner, Jacinta C ^c   Czekala, Nancy M ^d   Borries, Carola ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b WILDLIFE CONSERVATION SOCIETY   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d Papoose Conservation Wildlife Foundation   (United States)

Author keywords

Adolescent males; Colobines; Mate choice; Postconceptive mating

Indexed keywords

SEX HORMONE;

FEMALE BEHAVIOR; INFANTICIDE; MATE ATTRACTION; MATE CHOICE; MATING BEHAVIOR; PATERNITY; PREFERENCE BEHAVIOR; PRIMATE; REPRODUCTIVE BIOLOGY; REPRODUCTIVE STATUS; SIGNALING;

AGE DISTRIBUTION; AGGRESSION; ANIMAL; ARTICLE; CHEMISTRY; COLOBINAE; FECES; FEMALE; FERTILITY; MALE; MATE CHOICE; OVULATION; PHYSIOLOGY; RADIOIMMUNOASSAY; THAILAND;

AGE DISTRIBUTION; AGONISTIC BEHAVIOR; ANIMALS; COLOBINAE; FECES; FEMALE; FERTILITY; GONADAL STEROID HORMONES; MALE; MATING PREFERENCE, ANIMAL; OVULATION; RADIOIMMUNOASSAY; THAILAND;

CHAIYAPHUM; NORTHEASTERN REGION; PHU KHIEO WILDLIFE SANCTUARY; THAILAND;

HAPLORHINI; PRIMATES; TRACHYPITHECUS; TRACHYPITHECUS PHAYREI CREPUSCULUS;

EID: 84859911025     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.22004     Document Type: Article

References (70)

1. Bahr NI, Palme R, Mohle U, Hodges JK, Heistermann M. 2000. Comparative aspects of the metabolism and excretion of cortisol in three individual nonhuman primates. Gen Comp Endocrinol 117:427-438.
2. Barelli C, Heistermann M, Boesch C, Reichard UH. 2008. Mating patterns and sexual swellings in pair-living and multimale groups of wild white-handed gibbons, Hylobates lar. Anim Behav 75:991-1001.
3. Beach FA. 1976. Sexual attractivity, proceptivity, and receptivity in female mammals. Horm Behav 7:105-138.
4. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 57:289-300.
5. Borries C, Koenig A, Winkler P. 2001. Variation of life history traits and mating patterns in female langur monkeys (Semnopithecus entellus). Behav Ecol Sociobiol 50:391-402.
6. Borries C, Launhardt K, Epplen C, Epplen JT, Winkler P. 1999. Males as infant protectors in Hanuman langurs (Presbytis entellus) living in multimale groups-defence pattern, paternity and sexual behaviour. Behav Ecol Sociobiol 46:350-356.
7. Brauch K, Pfefferle D, Hodges JK, Mohle U, Fischer J, Heistermann M. 2007. Female sexual behavior and sexual swelling size as potential cues for males to discern the female fertile phase in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Horm Behav 52:375-383.
8. Carnegie SD, Fedigan LM, Ziegler TE. 2004. Behavioral indicators of ovarian phase in white-faced capuchins (Cebus capucinus). Am J Primatol 67:51-68.
9. Carnegie SD, Fedigan LM, Ziegler TE. 2005. Post-conceptive mating in white-faced capuchins, Cebus capucinus: hormonal and sociosexual patterns of cycling, noncycling, and pregnant females. In: Estrada A, Garber PA, Pavelka MSM, Luecke L, editors. New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior, and conservation. New York: Springer. p 387-409.
10. Carosi M, Heistermann M, Visalberghi E. 1999. Display of proceptive behaviors in relation to urinary and fecal progestin levels over the ovarian cycle in female tufted capuchin monkeys. Horm Behav 36:252-265.
11. Cerda-Molina AL, Hernandez-Lopez L, Chavira R, Cardenas M, Paez-Ponce D, Cervantes-De la Luz H, Mondragon-Ceballos R. 2006. Endocrine changes in male stumptailed macaques (Macaca arctoides) as a response to odor stimulation with vaginal secretions. Horm Behav 49:81-87.
12. Clarke PMR, Barrett L, Henzi SP. 2009. What role do olfactory cues play in chacma baboon mating? Am J Primatol 71:493-502.
13. Clutton-Brock TH, McAuliffe K. 2009. Female mate choice in mammals. Q Rev Biol 84:3-27.
14. Conover WJ. 1980. Practical nonparametric statistics. New York: Wiley.
15. Crockett CM, Sekulic R. 1984. Infanticide in red howler monkeys (Alouatta seniculus). In: Hausfater G, Hrdy DB, editors. Infanticide: comparative and evolutionary perspectives. New York: Aldine de Gruyter. p 173-191.
16. Dahl JF. 1986. Cyclic perineal swellings during the intermenstrual intervals of captive female chimpanzees. J Hum Evol 15:369-385.
17. Deag JM. 1980. Interactions between males and unweaned Barbary macaques: testing the agonistic buffering hypothesis. Behaviour 75:54-81.
18. Deschner T, Heistermann M, Hodges JK, Boesch C. 2003. Timing and probability of ovulation in relation to sex skin swelling in wild West African chimpanzees, Pan troglodytes verus. Anim Behav 66:551-560.
19. Deschner T, Heistermann M, Hodges K, Boesch C. 2004. Female sexual swelling size, timing of ovulation, and male behavior in wild West African chimpanzees. Horm Behav 46:204-215.
20. Dixon AF. 1998. Primate sexuality: comparative studies of the prosimians, monkeys, apes, and human beings. Oxford: Oxford University Press.
21. Dubuc C, Brent LJN, Accamando AK, Gerald MS, MacLarnon A, Semple S, ... Engelhardt A. 2009. Sexual skin color contains information about the timing of the fertile phase in free-ranging Macaca mulatta. Int J Primatol 30:777-789.
22. Engelhardt A, Hodges JK, Heistermann M. 2007. Post-conception mating in wild long-tailed macaques (Macaca fascicularis): characterization, endocrine correlates and functional significance. Horm Behav 51:3-10.
23. Engelhardt A, Hodges JK, 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.
24. Engelhardt A, Pfeifer AB, Heistermann M, Niemitz C, van Hooff JARAM, Hodges JK. 2004. Assessment of female reproductive status by male longtailed macaques, Macaca fascicularis, under natural conditions. Anim Behav 67:915-924.
25. France JT. 1981. Overview of the biological aspects of the fertile period. Int J Fertil 26:143-152.
26. Gesquiere LR, Wango EO, Alberts SC, Altmann J. 2007. Mechanisms of sexual selection: sexual swellings and estrogen concentrations as fertility indicators and cues for male consort decisions in baboons. Horm Behav 51:114-125.
27. Gordon TP, Gust DA, Busse CD, Wilson ME. 1991. Hormones and sexual behavior associated with postconception perineal swelling in the sooty mangabey (Cercocebus torquatus atys). Int J Primatol 12:585-597.
28. Gust DA. 1994. Alpha-male sooty mangabeys differentiate between females' fertile and their postconception maximal swellings. Int J Primatol 12:585-597.
29. Hasson O. 1994. Cheating signals. J Theor Biol 167:223-238.
30. Harris TR, Monfort SL. 2006. Mating behavior and endocrine profiles of wild black and white Colobus monkeys (Colobus guereza): toward an understanding of their life history and mating system. Am J Primatol 68:383-396.
31. Heape W. 1900. The "sexual season" of mammals and the relation of the "pro-castrum" to menstruation. Q J Microsc Sci 44:1-70.
32. Heistermann M, Ziegler T, van Schaik CP, Launhardt K, Winkler P, Hodges JK. 2001. Loss of oestrus, concealed ovulation and paternity confusion in free-ranging Hanuman langurs. P Roy Soc Lond B Bio 268:2445-2451.
33. Higham JP, Heistermann M, Ross C, Semple S, MacLarnon AM. 2008a. The timing of ovulation with respect to sexual swelling detumescence in wild olive baboons. Primates 49:295-299.
34. Higham JP, Hughes KD, Brent LJN, Dubuc C, Engelhardt A, Heistermann M, ... Stevens M. 2011. Familiarity affects the assessment of female facial signals of fertility by free-ranging male rhesus macaques. P Roy Soc Lond B Bio 278:3452-3458.
35. Higham JP, MacLarnon AM, Ross C, Heistermann M, Semple S. 2008b. Baboon sexual swellings: information content of size and color. Horm Behav 53:452-463.
36. Higham JP, Semple S, MacLarnon AM, Heistermann M, Ross C. 2009. Female reproductive signaling, and male mating behavior, in the olive baboon. Horm Behav 55:60-67.
37. Holm S. 1979. A simple sequentially rejective multiple test procedure. Scand J Stat 6:65-70.
38. Hrdy SB. 1977. The langurs of Abu: female and male strategies of reproduction. Cambridge: Harvard University Press.
39. Hrdy SB. 1979. Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol Sociobiol 1:13-40.
40. Hrdy SB. 2000. The optimal number of fathers: evolution, demography, and history in the shaping of female preferences. Ann NY Acad Sci 907:75-96.
41. 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.
42. Koenig A, Borries C. 2012. Social organization and male residence pattern in Phayre's leaf monkeys. In: Kappeler PM, Watts DP, editors. Long-term field studies of primates. Berlin: Springer. p 217-236.
43. Li BG, Zhao DP. 2007. Copulation behavior within one-male groups of wild Rhinopithecus roxellana in the Qinling Mountains of China. Primates 48:190-196.
44. Lu A, Beehner JC, Czekala NM, Koenig A, Larney E, Borries C. 2011. Phytochemicals and reproductive function in wild Phayre's leaf monkeys (Trachypithecus phayrei crepusculus). Horm Behav 59:28-36.
45. Lu A, Borries C, Czekala NM, Beehner JC. 2010. Reproductive characteristics of wild female Phayre's leaf monkeys. Am J Primatol 72:1073-1081.
46. Lu A, Koenig A, Borries C. 2008. Formal submission, tolerance and socioecological models: a test with female Hanuman langurs. Anim Behav 76:415-428.
47. Maynard Smith J. 1991. Theories of sexual selection. Trends Ecol Evol 6:146-151.
48. Miller SL, Maner JK. 2010. Scent of a woman: men's testosterone responses to olfactory ovulation cues. Psychol Sci 21:276-283.
49. Muller MN, Kahlenberg SM, Emery Thompson M, Wrangham RW. 2007. Male coercion and the costs of promiscuous mating for female chimpanzees. P Roy Soc Lond B Bio 274:1009-1014.
50. Muller MN, Emery Thompson M, Kahlenberg SM, Wrangham RW. 2011. Sexual coercion by male chimpanzees shows that female choice may be more apparent than real. Behav Ecol Sociobiol 65:921-933.
51. Nunn CL. 1999. The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Anim Behav 58:229-246.
52. O'Neill AC, Fedigan LM, Ziegler TE. 2004. Relationship between ovarian cycle phase and sexual behavior in female Japanese macaques (Macaca fuscata). Am J Phys Anthropol 125:352-362.
53. Ostner J, Chalise MK, Koenig A, Launhardt K, Nikolei J, Podzuweit D, Borries C. 2006. What Hanuman langur males know about female reproductive status. Am J Primatol 68:701-712.
54. Ostner J, Nunn CL, Schulke O. 2008. Female reproductive synchrony predicts skewed paternity across primates. Behav Ecol 19:1150-1158.
55. Pagel M. 1994. Evolution of conspicuous oestrous advertisement in old world monkeys. Anim Behav 47:1333-1341.
56. Pawlowski B. 1999. Loss of oestrus and concealed ovulation in human evolution - The case against the sexual-selection hypothesis. Curr Anthropol 40:257-275.
57. Pazol K. 2003. Mating in the Kakamega forest blue monkeys (Cercopithecus mitis): does female sexual behavior function to manipulate paternity assessment? Behavior 140:470-499.
58. Perneger TV. 1998. What's wrong with Bonferroni adjustments. Br Med J 316:1236-1237.
59. Saayman GS. 1975. The influence of hormonal and ecological factors upon sexual behavior and social organization in Old World primates. In: Tuttle RH, editor. Socioecology and psychology of primates. The Hague: Mouton Publishers. p 181-204.
60. Shelmidine N, Borries C, McCann C. 2009. Patterns of reproduction in Malayan silvered leaf monkeys at the Bronx Zoo. Am J Primatol 71:852-859.
61. Sommer V. 1994. Infanticide among the langurs of Jodhpur: testing the sexual selection hypothesis with a long-term record. In: Parmigiani S, vom Saal FS, editors. Infanticide and parental care. Chur: Harwood Academic. p 155-198.
62. Sommer V, Srivastava A, Borries C. 1992. Cycles, sexuality, and conception in free-ranging langurs (Presbytis entellus). Am J Primatol 28:1-27.
63. Stumpf RM, Boesch C. 2005. Does promiscuous mating preclude female choice? Female sexual strategies in chimpanzees (Pan troglodytes verus) of the Tai National Park, Cote d'Ivoire. Behav Ecol Sociobiol 57:511-524.
64. van Belle S, Estrada A, Ziegler TE, Strier KB. 2009. Sexual behavior across ovarian cycles in wild black howler monkeys (Alouatta pigra): male mate guarding and female mate choice. Am J Primatol 71:153-164.
65. van Noordwijk MA, van Schaik CP. 2000. Reproductive patterns in eutherian mammals: adaptations against infanticide? In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press. p 322-360.
66. van Schaik CP. 1994. Predation risk and the number of adult males in a primate group: a comparative test. Behav Ecol Sociobiol 35:261-272.
67. van Schaik CP, Hodges JK, Nunn CL. 2000. Paternity confusion and the ovarian cycles of female primates. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press. p 361-387.
68. Wallen K. 2001. Sex and context: hormones and primate sexual motivation. Horm Behav 40:339-357.
69. Wasser SK, Monfort SL, Southers J, Wildt DE. 1994. Excretion rates and metabolites of oestradiol and progesterone in baboon (Papio cynocephalus cynocephalus) faeces. J Reprod Fertil 101:213-220.
70. Wilcox AJ, Weinberg CR, Baird DD. 1995. Timing of sexual intercourse in relation to ovulation-effects on the probability of conception, survival of the pregnancy, and sex of the baby. N Engl J Med 333:1517-1521.