Social odours, sexual arousal and pairbonding in primates

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 361, Issue 1476, 2006, Pages 2079-2089

  Snowdon, Charles T ^a   Ziegler, Toni E ^a,b   Schultz Darken, Nancy J ^b   Ferris, Craig F ^c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Functional magnetic resonance imaging; Neuroendocrine responses; Pairbonds; Primates; Sexual arousal; Social odours

Indexed keywords

ODOR; PAIR BOND; PRIMATE; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR;

PRIMATES;

EID: 33845870974     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2006.1932     Document Type: Review

References (47)

1. Achenbach, G. G. & Snowdon, C. T. 2002 Costs of caregiving: weight loss in captive adult male cotton-top tamarins (Saguinus oedipus) following the birth of infants. Int. J. Primatol. 23, 179-189. (doi:10.1023/A:1013210226793)
2. Anzenberger, G. 1985 How stranger encounters of common marmosets (Callithrix jacchus jacchus) are influenced by family members: the quality of behavior. Fol. Primatol. 45, 204-224.
3. Barrett, J., Abbott, D. H. & George, L. M. 1990 Extension of reproductive suppression by pheromonal cues in subordinate female marmoset monkeys, Callithrix jacchus. J. Reprod. Fert. 90, 411-418.
4. Bensafi, M. et al. 2003 Sex-steroid derived compounds induce sex-specific effects on autonomic nervous system functions in humans. Behav. Neurosci. 117, 1125-1134. (doi:10.1037/0735-7044.117.6.1125)
5. Burley, N. 1979 The evolution of concealed ovulation. Am. Nat. 114, 835-858. (doi:10.1086/283532)
6. Converse, L. J., Carlson, A. A., Ziegler, T. E. & Snowdon, C. T. 1995 Communication of ovulatory state to mates by female pygmy marmosets (Cebuella pygmaea). Anim. Behav. 49, 615-621.
7. Dixson, A. F. & Lloyd, S. A. C. 1988 The hormonal and hypothalamic control of primate sexual behaviour. Symp. Zool. Soc. Lond. 60, 81-117.
8. Epple, G. & Katz, Y. 1984 Social influences on estrogen excretion and ovarian cyclicity in saddleback tamarins (Saguinus fuscicollis). Am. J. Primatol. 6, 215-227. (doi:10. 1002/ajp.1350060309)
9. Epple, G., Belcher, A. M., Kuderling, I., Seller, U., Scolnick, L., Greenfield, K. L. & Smith III, A. B. 1993 Making sense out of scents: species differences in scent glands, scent marking behaviour, and scent mark composition in the Callitrichidae. In Marmosets and tamarins: systematics, behaviour and ecology (ed. A. B. Rylands), pp. 123-151. Oxford, UK: Oxford University Press.
10. Evans, S. 1983 The pair-bond of the common marmoset, (Callithrix jacchus jacchus): an experimental investigation. Anim. Behav. 31, 651-658. (doi:10.1016/S0003-3472(83) 80220-6)
11. Ferris, C. F. & Snowdon, C. T. 2005 Functional magnetic resonance imaging in conscious marmoset monkeys: methods and applications in neuroscience research. In The laboratory primate (ed. S. Wolfe-Coate). Handbook of experimental animals. London, UK: Academic Press.
12. Ferris, C. F. et al. 2001 Functional imaging of brain activity in conscious monkeys responding to sexually arousing cues. NeuroReport 12, 2231-2236. (doi:10.1097/00001756-200107200-00037)
13. Ferris, C. F. et al. 2004 Imaging neural pathways associated with stimuli for sexual arousal in nonhuman primates. J. Mag. Res. Imag. 19, 168-175. (doi:10.1002/jmri.10456)
14. French, J. A. & Cleveland, J. 1984 Scent marking in the tamarin, Saguinus oedipus: sex differences and ontogeny. Anim. Behav. 32, 615-623. (doi:10.1016/S0003-3472(84) 80299-7)
15. French, J. A. & Snowdon, C. T. 1981 Sexual dimorphism in responses to unfamiliar intruders in the tamarin (Saguinus oedipus). Anim. Behav. 29, 822-829. (doi:10.1016/S0003-3472(81)80016-4)
16. French, J. A., Abbott, D. H. & Snowdon, C. T. 1984 The effect of social environment on estrogen secretion, scent marking and sociosexual behavior in tamarins (Saguinus oedipus). Am. J. Primatol. 6, 155-167. (doi:10.1002/ajp. 1350060304)
17. Heymann, E. W. 2003 Scent marking paternal care and sexual selection in Callitrichines. In Sexual selection and reproductive competition in primates; new perspectives and directions (ed. C. Jones), pp. 305-325. New York, NY: Wiley Liss.
18. Hrdy, S. 1999 Mother nature, maternal instincts and how they shape the human species. New York, NY: Ballantine.
19. Lazaro-Perea, C. 2001 Intergroup interactions in wild common marmosets, Callithrix jacchus; territorial defence and assessment of neighbours. Anim. Behav. 62, 11-21. (doi:10.1006/anbe.2000.1726)
20. Lazaro-Perea, C., Snowdon, C. T. & Arruda, M. F. 1999 Scent-marking behavior in wild groups of common marmosets (Callithrix jacchus). Behav. Ecol. Sociobiol. 46, 313-324. (doi:10.1007/s002650050625)
21. Lazaro-Perea, C., Castro, C. S. S., Harrison, R., Araujo, A., Arruda, M. F. & Snowdon, C. T. 2000 Behavioral and demographic changes following the loss of the breeding female in cooperatively breeding marmosets. Behav. Ecol. Sociobiol. 48, 137-146. (doi:10.1007/s002650000215)
22. Lloyd, S. A. C. & Dixson, A. F. 1988 Effects of hypothalamic lesions upon the sexual and social behaviour of the male common marmoset (Callithrix jacchus). Brain Res. 463, 317-329. (doi:10.1016/0006-8993(88) 90405-2)
23. Paredes, R. G. & Baum, M. J. 1995 Altered sexual partner preference in male ferrets given excitotoxic lesions of the preoptic area/anterior hypothalamus. J. Neurosci. 15, 6619-6630.
24. Paredes, R. G., Tzschentke, T. & Nakach, N. 1998 Lesions of the medial preoptic area/anterior hypothalamus (MPOA/AH) modify partner preference in male rats. Brain Res. 813, 1-8. (doi:10.1016/S0006-8993(98) 00914-7)
25. Preti, G., Wysocki, C. J., Barnhart, K. T., Sondheimer, S. J. & Leyden, J. L. 2003 Male axillary extracts contain pheromones that affect pulsatile secretion of luteinizing hormone and mood in women recipients. Biol. Reprod. 68, 2107-2113. (doi:10.1095/biolreprod.102.008268)
26. Sanchez, S., Peleaz, F., Gil-Burmann, C. & Kaumanns, W. 1999 Costs of infant carrying in the cotton-top tamarin. Am. J. Primatol. 48, 99-111. (doi:10.1002/(SICI)1098-2345(1999)48:2〈99::AID-AJP2〉3.0.CO;2- 6)
27. Savic, I., Berglund, P., Gulyas, B. & Roland, P. 2001 Smelling of odorous sex hormone-like compounds causes sex differentiated hypothalamic activations in humans. Neuron 31, 661-668. (doi:10.1016/S0896- 6273(01)00390-7)
28. Savic, I., Berglund, H. & Lindstrom, P. 2005 Brain responses to putative pheromones in homosexual men. Proc. Natl Acad. Sci. USA 102, 7356-7361. (doi:10.1073/pnas. 0407998102)
29. Savage, A., Ziegler, T. E. & Snowdon, C. T. 1988 Sociosexual development, pairbond formation and mechanisms of fertility suppression in female cotton-top tamarins (Saguinus oedipus oedipus). Am. J. Primatol. 14, 345-359. (doi:10.1002/ajp.1350140404)
30. Singh, D. & Bronstad, P. M. 2001 Female body odour is a potential cue for ovulation. Proc. R. Soc. B 268, 797-801. (doi:10.1098/rspb. 2001.1589)
31. Smith, T. E. & Abbott, D. H. 1998 Behavioral discrimination between circumgenital odor from periovulatory dominant and anovulatory female common marmosets (Callithrix jacchus). Am. J. Primatol. 46, 265-284. (doi:10.1002/(SICI) 1098-2345(1998)46:4〈265::AID-AJP1〉3.0. CO;2-D)
32. Smith, A. B., Yarger, R. G. & Epple, G. 1976 The major volatile constituents of the marmoset (Saguinus fuscicollis) scent mark. Tetrahedron Lett. 17, 983-986. (doi:10.1016/ S0040-4039(00)77984- 6)
33. Smith, T. E., Abbott, D. H., Tomlinson, A. J. & Mlotkewicz, J. A. 1997 Differential display of investigative behavior permits discrimination of scent signatures from familiar and unfamiliar socially dominant female marmoset monkeys (Callithrix jacchus). J. Chem. Ecol. 23, 2523-2546. (doi:10. 1023/B:JOEC.0000006664.38169.e5)
34. Snowdon, C. T. 1996 Parental care in cooperatively breeding species. In Parental care: evolution, mechanisms and adaptive significance (ed. J. S. Rosenblatt & C. T. Snowdon), pp. 643-689. San Diego, CA: Academic Press.
35. Snowdon, C. T. 2001 Sexe, attachement et monogamie chez les primates (sex, pairbonds and monogamy in primates). Primatologie 3, 387-420.
36. Sobel, N., Prabhakaran, V., Hartley, C. A., Desmond, J. E., Glover, G. H., Sullivan, E. V. & Gabrielli, J. D. E. 1999 Blind smell: brain activation induced by an undetected airborne chemical. Brain 122, 209-217. (doi:10.1093/brain/ 122.2.209)
37. Stern, K. & McClintick, M. K. 1998 Regulation of ovulation by human pheromones. Nature 392, 177-179. (doi:10. 1038/32408)
38. Trotier, D., Eliot, C., Wassef, M., Talman, G., Bensimon, J. L., Doving, K. B. & Ferrand, J. 2000 The vomeronasal cavity in adult humans. Chem. Senses 25, 369-380. (doi:10.1093/chemse/25.4.369)
39. Wallen, K. 1982 Influence of female hormonal state on rhesus sexual behavior varies with space for social interactions. Science 217, 375-377. (doi:10.1126/science.7201164)
40. Washabaugh, K. & Snowdon, C. T. 1998 Chemical communication of reproductive status in female cotton-top tamarins (Saguinus o. oedipus). Am. J. Primat. 45, 337-349. (doi:10. 1002/(SICI)1098-2345(1998)45: 4〈337::AID-AJP2〉3.0. CO;2-X)
41. Wyatt, T. D. 2003 Pheromones and animal behaviour, communication by smell and taste. Cambridge, UK: Cambridge University Press.
42. Ziegler, T. E., Bridson, W. E., Snowdon, C. T. & Eman, S. 1987 Urinary gonadotropin and estrogen excretion during the post-partum estrous, conception and pregnancy in the cotton-top tamarin. Am. J. Primatol. 12, 127-140. (doi:10. 1002/ajp.1350120202)
43. Ziegler, T. E., Epple, G., Snowdon, C. T., Porter, T. A., Belcher, A. & Kuederling, I. 1993 Detection of the chemical signals of ovulation in the cotton-top tamarin, Saguinus oedipus. Anim. Behav. 45, 313-322. (doi:10. 1006/anbe.1993.1036)
44. Ziegler, T. E., Washabaugh, K. F. & Snowdon, C. T. 2004a Responsiveness of expectant male cotton-top tamarins, Saguinus oedipus, to mate's pregnancy. Horm. Behav. 45, 84-92. (doi:10.1016/j.yhbeh. 2003.09.003)
45. Ziegler, T. E., Jacoris, S. & Snowdon, C. T. 2004b Sexual communication between breeding male and female cotton-top tamarins (Saguinus oedipus) and its relationship to infant care. Am. J. Primatol. 64, 57-69. (doi:10.1002/ ajp.20061)
46. Ziegler, T. E., Schultz-Darken, N. J., Scott, J. J., Snowdon, C. T. & Ferris, C. F. 2005 Neuroendocrine response to female ovulatory odors depends upon social condition in male common marmosets, Callithrix jacchus. Horm. Behav. 47, 56-64. (doi:10.1016/j.yhbeh.2004.08.009)
47. Zinner, D. P., Nunn, C. L., Van Schaik, C. & Kappeler, P. 2004 Sexual selection and exaggerated sexual swelling in female primates. In Sexual selection in primates: new and comparative perspectives (ed. P. Kappeler & C. Van Schaik), pp. 71-89. Cambridge, UK: Cambridge University Press.