Sexual swellings in wild white-handed gibbon females (Hylobates lar) indicate the probability of ovulation

Hormones and Behavior

Volumn 51, Issue 2, 2007, Pages 221-230

  Barelli, Claudia ^a,b   Heistermann, Michael ^b   Boesch, Christophe ^a   Reichard, Ulrich H ^a,c  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b GERMAN PRIMATE CENTER   (Germany)

^c SOUTHERN ILLINOIS UNIVERSITY   (United States)

Author keywords

Fecal progestogen; Fertility; Genital sexual swelling; Gibbons; Graded signal hypothesis; Hylobates lar; Monogamy; Ovulation; Paternity confusion; Polyandry

Indexed keywords

GESTAGEN;

ARTICLE; CHRONOLOGY; CONTROLLED STUDY; FECES ANALYSIS; FEMALE; FEMALE FERTILITY; FEMALE GENITAL SYSTEM; HAPLORHINI; LACTATION; MATING; MENSTRUAL CYCLE; NONHUMAN; OVULATION; PREDICTION; PREGNANCY; PRIORITY JOURNAL; PROBABILITY; SEX HORMONE DETERMINATION; SEXUAL SWELLING; SOCIAL STRUCTURE; SWELLING; WILD ANIMAL;

ANALYSIS OF VARIANCE; ANIMALS; ESTROUS CYCLE; FECES; FEMALE; HYLOBATES; OVULATION; PROBABILITY; PROGESTERONE; REPRODUCTION; SEASONS; SEX CHARACTERISTICS; STATISTICS, NONPARAMETRIC; VULVA;

EID: 33846046175     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2006.10.008     Document Type: Article

References (78)

1. Anderson C.M., and Bielert C.F. Adolescent exaggeration in female catarrhine primates. Primates 35 (1994) 283-300
2. Aranda J.D., Brindle E., Carey K.D., Rice K., Tatar M., and O'Connor K.A. Sexual swelling relative to occurrence and timing of ovulation in Papio sp. Am. J. Phys. Anthropol. 42 (2006) 57 (S)
3. Barelli, C., Heistermann, M., in press. Monitoring female reproductive status using fecal hormone analysis and preliminary data on patterns of genital swellings in relation to female cycle stage in captive and wild white-handed gibbons (Hylobates lar). In: Lappan, S.M., Whittaker, D., Geissmann T. (Eds.), The Gibbons: New Perspectives on Small Ape Socioecology and Population Biology. Springer, Berlin.
4. Bettinger T., Wallis J., and Morris A. Reproductive parameters of mandrills at the Tulsa Zoo. Zoo Biol. 14 (1995) 115-121
5. Breznock A.W., Harrold J.B., and Kawakami T.G. Successful breeding of the laboratory-housed gibbon (Hylobates lar). Lab. Anim. Sci. 27 (1977) 222-228
6. Brockelman W.Y., Reichard U., Treesucon U., and Raemakers J.J. Dispersal, pair formation, and social structure in gibbons (Hylobates lar). Behav. Ecol. Sociobiol. 42 (1998) 329-339
7. Campbell C.J. Primate sexuality and reproduction. In: Campbell C.J., Fuentes A., MacKinnon K.C., Panger M., and Bearder S. (Eds). Primates in Perspective (2006), Oxford Univ. Press, Oxford 423-437
8. Carpenter C.R. The menstrual cycle and body temperature in two gibbons (Hylobates lar). Anat. Rec. 79 (1941) 291-296
9. Cheyne S.M., and Chivers D.J. Sexual swellings of female gibbons. Folia Primatol. 77 (2006) 345-352
10. Chivers D.J. The siamang in Malaya. Contrib. Primatol. 4 (1974) 1-335
11. Chivers D.J. Sexual behaviour of wild siamang. In: Chivers D.J., and Herbert J. (Eds). Recent Advances in Primatology (1978), Academic Press, London 609-610
12. Clutton-Brock T.H., and Harvey P.H. Evolutionary rules and primates societies. In: Bateson P.P.G., and Hinde R.A. (Eds). Growing Points in Ethology (1976), Cambridge Univ. Press, Cambridge 195-237
13. Cooper W.E., and Crews D. Hormonal induction of secondary sexual coloration and rejection behaviour in female keeled earless lizards, Holbrookia propinqua. Anim. Behav. 35 (1987) 1177-1187
14. Dahl J.F., and Nadler R.D. Genital swelling in females of the monogamous gibbon, Hylobates lar. Am. J. Phys. Anthropol. 89 (1992) 101-108
15. Dahl J.F., and Nadler R.D. The external genitalia of female gibbons, Hylobates (H.) lar. Anat. Rec. 232 (1992) 572-578
16. Davies N.B., Hartley I.R., Hatchwell B.J., and Langmore N.E. Female control of copulations to maximize male help: a comparison of polygynandrous alpine accentors, Prunella collaris, and dunnocks, P. modularis. Anim. Behav. 51 (1996) 27-47
17. Deschner T., Heistermann M., Hodges J.K., and Boesch C. Timing and probability of ovulation in relation to sex ski swelling in wild West African chimpanzees, Pan troglodytes verus. Anim. Behav. 66 (2003) 551-560
18. Dixson A.F. Observations on the displays, menstrual cycles and sexual behaviour of the "Black ape" of Celebes (Macaca nigra). J. Zool. (London) 182 (1977) 63-84
19. Dixson A.F. Observations on the evolution and behavioral significance of "sexual skin" in female primates. Adv. Study Behav. 13 (1983) 63-106
20. Dixson A.F. Primate Sexuality (1998), Oxford Univ. Press, Oxford
21. Dixson A.F., and Herbert J. Gonadal hormones and sexual behavior in groups of adult talapoin monkeys (Miopithecus talapoin). Horm. Behav. 8 (1977) 141-154
22. Dukelow W.R., Grauwiler J., and Brüggemann S. Characteristics of the menstrual cycle in nonhuman primates: I. Similarities and dissimilarities between Macaca fascicularis and Macaca arctoides. J. Med. Primatol. 8 (1979) 39-47
23. Emery M.A., and Whitten P.L. Size of sexual swellings reflects ovarian function in chimpanzees (Pan troglodytes). Behav. Ecol. Sociobiol. 54 (2003) 340-351
24. Engelhardt A., Hodges J.K., Niemitz C., and Heistermann M. Female sexual behaviour, but not sex skin swelling, reliably indicates the timing of the fertile phase in wild long-tailed macaques (Macaca fascicularis). Horm. Behav. 47 (2005) 195-204
25. Engelhardt A., Heistermann M., Hodges J.K., Nuernberg P., and Niemitz C. Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis)-male monopolisation, female mate choice or post-copulatory mechanisms?. Behav. Ecol. Sociobiol. 59 (2006) 740-752
26. Ferguson G.W. Color change and reproductive cycling in female collared lizards (Crotaphytus collaris). Copeia 3 (1976) 491-494
27. France J.T. Overview of the biological aspects of the fertile period. Int. J. Fertil. 26 (1981) 143-152
28. Gauthier C. Reproductive parameters and paracallosal skin color changes in captive female guinea baboons, Papio papio. Am. J. Primatol. 47 (1999) 67-74
29. Glander K.E. Reproduction and population growth in free-ranging mantled howling monkeys. Am. J. Phys. Anthropol. 53 (1980) 25-36
30. Gordon T.P., Gust D.A., Busse C.D., and Wilson M.E. Hormones and sexual behavior associated with postconception perineal swelling in the sooty mangabey (Cercocebus torquatus atys). Int. J. Primatol. 12 (1991) 585-597
31. Hadidian J., and Bernstein I.S. Female reproductive cycles and birth data from an Old World monkey colony. Primates 20 (1979) 429-442
32. Hamilton W.J. Significance of paternal investment by primates to the evolution of adult male-female associations. In: Taub D.M. (Ed). Primate Paternalism (1984), van Nostrand Reinhold, New York 309-335
33. Heistermann M., Möhle U., Vervaecke H., van Elsacker L., and Hodges J.K. Application of urinary and fecal steroid measurements for monitoring ovarian function and pregnancy in the bonobo (Pan paniscus) and evaluation of perineal swelling patterns in relation to endocrine events. Biol. Reprod. 55 (1996) 844-853
34. Heistermann M., Uhrigshardt J., Husung A., Kaumanns W., and Hodges J.K. Measurement of faecal steroid metabolites in the lion-tailed macaque (Macaca silenus): a non-invasive tool for assessing female ovarian function. Primate Rep. 59 (2001) 27-42
35. Hodges J.K., Heistermann M., Beard A., and van Aarde R.J. Concentrations of progesterone and the 5α-reduced progestins, 5α-pregnane-3,20-dione and 5α-pregnane-3α-ol-20-one in luteal tissue and circulating blood and their relationship to luteal function in the African elephant, Loxodonta africana. Biol. Reprod. 56 (1997) 640-646
36. Hrdy S.B. The Women that Never Evolved (1981), Harvard Univ. Press, Cambridge, MA
37. Hrdy S.B., and Whitten P.L. Pattering of sexual activity. In: Smuts B.B., Cheney D.L., Seyfarth R.M., Wrangham R.W., and Struhsaker T.T. (Eds). Primate Societies (1987), Univ. of Chicago Press, Chicago 370-384
38. Kappeler P.M., and van Schaik C.P. Evolution of primate social systems. Int. J. Primatol. 23 4 (2002) 707-740
39. Lappan, S., 2005. Biparental care and male reproductive strategies in siamangs (Symphalangus syndactilus) in southern Sumatra. PhD thesis, University of New York.
40. Matthews L.H. Notes on the genital anatomy and physiology of the gibbon (Hylobates). Proc. Zool. Soc. Lond. 116 (1946) 339-364
41. Möhle U., Heistermann M., Dittami J., Reinberg V., Wallner B., and Hodges J.K. Patterns of anogenital swelling size and their endocrine correlates during ovulatory cycles and early pregnancy in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Am. J. Primatol. 66 (2005) 351-368
42. Mundry R. Testing related samples with missing values: a permutation approach. Anim. Behav. 58 (1999) 1143-1153
43. Mundry R., and Fischer J. Use of statistical programs for nonparametric tests of small samples often leads to incorrect P values: examples from animal behaviour. Anim. Behav. 56 (1998) 246-259
44. Nadler R.D. Cyclicity in tumescence of the perineal labia of female lowland gorillas. Anat. Rec. 181 (1975) 791-798
45. Nadler R.D., Dahl J.F., and Collins D.C. Serum and urinary concentration of sex hormones and genital swelling during the menstrual cycle of the gibbon. J. Endocrinol. 136 (1993) 447-455
46. Nunn C.L. The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Anim. Behav. 58 (1999) 229-246
47. Nunn C.L., van Schaik C.P., and Zinner D. Do exaggerated sexual swellings function in female mating competition in primates? A comparative test of the reliable indicator hypothesis. Behav. Ecol. 12 (2001) 646-654
48. Oates J.F., Davies A.G., and Delson E. The diversity of living colobines. In: Oates J.F., and Davies A.G. (Eds). Colobine Monkeys (1994), Cambridge Univ. Press, Cambridge 45-73
49. Ostner J., and Heistermann M. Endocrine characterization of female reproductive status in wild redfronted lemurs (Eulemur fulvus rufus). Gen. Comp. Endocrinol. 131 (2003) 274-283
50. Pagel M. The evolution of conspicuous oestrous advertisement in Old World monkeys. Anim. Behav. 27 (1994) 1-36
51. Palombit R.A. Extra-pair copulations in a monogamous ape. Anim. Behav. 47 3 (1994) 721-723
52. Raemaekers J.J., and Raemaekers P.M. Field playback of loud calls to gibbons (Hylobates lar): territorial, sex-specific and species-specific responses. Anim. Behav. 33 (1985) 481-493
53. Reichard U. Extra-pair copulation in a monogamous gibbons (Hylobates lar). Ethology 100 2 (1995) 99-112
54. Reichard U.H. Monogamy in gibbons: the male perspective. In: Reichard U.H., and Boesch C. (Eds). Monogamy: Mating Strategies and Partnerships in Birds, Humans and other Mammals (2003), Cambridge Univ. Press, Cambridge 190-213
55. Reichert K.E., Heistermann M., Hodges J.K., Boesh C., and Hohmann G. What females tell males about their reproductive status: are morphological cues reliable signals of ovulation in bonobos (Pan paniscus)?. Ethology 108 (2002) 583-600
56. Roberts S.C., Havlicek J., Flegr J., Hruskova M., Little A.C., Jones B.C., Perrett D.I., and Petrie M. Female facial attractiveness increases during the fertile phase of the menstrual cycle. Proc. R. Soc. London, B 271 (2004) 270-272 (Suppl.)
57. Rowell T.E., and Chalmers N.R. Reproductive cycles of the mangabey Cercocebus albigena. Folia Primatol. 12 (1970) 264-272
58. Saayman G.S. Effects of ovarian hormones on the sexual skin and behavior of ovariectomized baboons (Papio ursinus) under free-ranging conditions. In: Phoenix C.H. (Ed). Proc. IVth Int. Congr. Primatol. vol. 2 (1973), Karger, Basel 64-98
59. Setchell J.M., and Wickings E.W. Social and seasonal influences on the reproductive cycle in female mandrills (Mandrillus sphinx). Am. J. Phys. Anthropol. 125 (2004) 73-84
60. Sicchar L.A., and Heymann E.W. Preliminary observations on external signs of estrus in moustached tamarins, Saguinus mystax (Callitrichidae). Lab. Primate Newsl. 31 (1992) 4-6
61. Siegel S., and Castellan N.J. Nonparametric Statistics for the Behavioral Sciences (1988), McGraw-Hill, New York
62. Sillén-Tullberg B., and Møller A.P. The relationship between concealed ovulation and mating systems in anthropoid primates: a phylogenetic analysis. Am. Nat. 141 (1993) 1-25
63. Stallmann R.R., and Froehlich J.W. Primate sexual swellings as coevolved signal systems. Primates 41 (2000) 1-16
64. Struhsaker T.T., and Leland L. Socioecology of five sympatric monkey species in the Kibale Forest, Uganda. Adv. Study Behav. 9 (1979) 159-228
65. Taub D.M. Female choice and mating strategies among wild Barbary macaques (Macaca sylvanus). In: Lindburg D.G. (Ed). The Macaques: Studies in Ecology, Behavior and Evolution (1980), van Nostrand Reinhold, New York 287-344
66. Tenaza R.R. Female sexual swellings in the Asian colobine Simias concolor. Am. J. Primatol. 17 (1989) 81-86
67. Thierry B., Heistermann M., Aujard F., and Hodges J.K. Long-term data on basic reproductive parameters and evaluation of endocrine, morphological, and behavioral measures for monitoring reproductive status in a group of semifree-ranging tonkean macaques (Macaca tonkeana). Am. J. Primatol. 39 (1996) 47-62
68. van Horn R.N., and Eaton G.G. Reproductive physiology and behavior in prosimians. In: Doyle G.A., and Martin R.D. (Eds). The Study of Prosimians Behavior (1979), Academic Press, New York 79-122
69. van Noordwijk M.A., and van Schaik C.P. Reproductive patterns in eutherian mammals: adaptations against infanticide?. In: van Schaik C.P., and Janson C.H. (Eds). Infanticide by Males and its Implications (2000), Cambridge Univ. Press, Cambridge 322-360
70. van Schaik C.P., van Noordwijk M.A., and Nunn C.L. Sex and social evolution in primates. In: Lee P.C. (Ed). Comparative Primate Socioecology (1999), Cambridge Univ. Press, Cambridge 204-231
71. van Schaik C.P., Hodges J.K., and Nunn C.L. Paternity confusion and the ovarian cycles of female primates. In: van Schaik C.P., and Janson C.H. (Eds). Infanticide by Males and its Implications (2000), Cambridge Univ. Press, Cambridge 361-387
72. Wallis J. Sexual behavior of captive chimpanzees (Pan troglodytes): pregnant versus cycling females. Am. J. Primatol. 3 (1982) 77-88
73. Wilcox A.J., Weinberg C.R., and Baird D.D. Timing of sexual intercourse in relation to ovulation. N. Engl. J. Med. 333 (1995) 1517-1522
74. Wright P.C., Toyama T.M., and Simons E.I. Courtship and copulation in Tarsius bancanus. Folia Primatol. 46 (1986) 142-148
75. Zar J.H. Biostatistical Analysis. 4th ed. (1999), Prentice Hall, Upper Saddle River, NJ
76. Ziegler T., Hodges J.K., Winkler P., and Heistermann M. Hormonal correlates of reproductive seasonality in wild female Hanuman langurs (Presbytis entellus). Am. J. Primatol. 51 (2000) 119-134
77. Zinner D., and Deschner T. Sexual swellings in female hamadryas baboons after male take-overs: "deceptive" swellings as a possible female counter-strategy against infanticide. Am. J. Primatol. 52 (2000) 157-168
78. Zinner D.P., Nunn C.L., van Schaik C.P., and Kappeler P.M. Sexual selection and exaggerated sexual swellings of female primates. In: Kappeler P.M., and van Schaik C. (Eds). Sexual Selection in Primates: New and Comparative Perspectives (2004), Cambridge Univ. Press, New York 71-89