Post-conception reproductive competition in cooperatively breeding common marmosets

Hormones and Behavior

Volumn 53, Issue 1, 2008, Pages 274-286

  Saltzman, Wendy ^a,b   Liedl, Kimber J ^b   Salper, Orrie J ^b   Pick, Rebecca R ^b   Abbott, David H ^b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Alloparental care; Biparietal diameter; Chorionic gonadotropin; Estrogen metabolites; Infanticide; Maternal behavior; Pregnancy; Reproductive skew; Reproductive suppression

Indexed keywords

AGGRESSION; ANIMAL EXPERIMENT; ARTICLE; BIPARIETAL DISTANCE; BIRTH; COMPETITION; CONCEPTION; CONTROLLED STUDY; DAUGHTER; FAMILY; FEMALE; HORMONE URINE LEVEL; IMMOBILIZATION STRESS; INCIDENCE; INFANCY; INFANT MORTALITY; INFANTICIDE; LIVE BIRTH; MALE; MARMOSET; MOLECULAR EVOLUTION; MOTHER; NONHUMAN; OVULATION INHIBITION; PREGNANCY; PREGNANCY OUTCOME; PRIORITY JOURNAL; REPRODUCTION; SEXUAL BEHAVIOR; SOCIAL DOMINANCE; SPONTANEOUS ABORTION; STILLBIRTH; SURVIVAL;

AGGRESSION; ANIMALS; BEHAVIOR, ANIMAL; CALLITHRIX; CHORIONIC GONADOTROPIN; COMPETITIVE BEHAVIOR; DOMINANCE-SUBORDINATION; ESTROGENS; FEMALE; INHIBITION (PSYCHOLOGY); MALE; MATERNAL BEHAVIOR; OVULATION INHIBITION; PREGNANCY; PREGNANCY OUTCOME; PREGNANCY, ANIMAL; SOCIAL ENVIRONMENT;

EID: 37349064428     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2007.10.005     Document Type: Article

References (87)

1. Abbott, D.H., 1979. The sexual development of the common marmoset monkey Callithrix jacchus jacchus. Ph.D. thesis, University of Edinburgh.
2. Abbott D.H., and Hearn J.P. Physical, hormonal and behavioural aspects of sexual development in the marmoset monkey, Callithrix jacchus. J. Reprod. Fertil. 53 (1979) 155-166
3. Abbott D.H., Saltzman W., Schultz-Darken N.J., and Smith T.E. Specific neuroendocrine mechanisms not involving generalized stress mediate social regulation of female reproduction in cooperatively breeding marmoset monkeys. Ann. N.Y. Acad. Sci. 807 (1997) 219-238
4. Abbott, D.H., Digby, L.J., Saltzman, W., in press. Reproductive skew in female common marmosets: contributions of infanticide and subordinate self-restraint. In: R. Hager, C.B. Jones (Eds.), Reproductive Skew in Vertebrates: Proximate and Ultimate Causes. Cambridge University Press.
5. Albuquerque A.C.S.R., Sousa M.B.C., Santos H.M., and Ziegler T.E. Behavioral and hormonal analysis of social relationships between oldest females in a wild monogamous group of common marmosets (Callithrix jacchus). Int. J. Primatol. 22 (2001) 631-645
6. Alonso C. Fracasso na inibição da reprodução de uma fêmea subordinada e troca de hierarquia em um grupo familiar de Callithrix jacchus jacchus. A Primatologia No Brasil - 2: An 2° Congr Bras Primatologia, Campinas, 1985 (1986) 203
7. Arruda M.F., Araûjo A., Sousa M.B.C., Albuquerque F.S., Albuquerque A.C.S.R., and Yamamoto M.E. Two breeding females within free-living groups may not always indicate polygyny: alternative subordinate female strategies in common marmosets (Callithrix jacchus). Folia Primatol. 76 (2005) 10-20
8. Baker J.V., Abbott D.H., and Saltzman W. Social determinants of reproductive failure in male common marmosets housed with their natal family. Anim. Behav. 58 (1999) 501-513
9. Bales K., French J.A., and Dietz J. Explaining variation in maternal care in a cooperatively breeding species. Anim. Behav. 63 (2002) 453-561
10. Bardi M., and Petto A.J. Parental failure in captive common marmosets (Callithrix jacchus): a comparison with tamarins. Folia Primatol. 73 (2002) 46-48
11. Bezerra B.M., Da Silva Souta A., and Schiel N. Infanticide and cannibalism in a free-ranging plurally breeding group of common marmosets (Callithrix jacchus). Am. J. Primatol. 69 (2007) 1-8
12. Chambers P.L., and Hearn J.P. Peripheral plasma levels of progesterone, oestradiol-17β, oestrone, testosterone, androstenedione and chorionic gonadotrophin during pregnancy in the marmoset monkey, Callithrix jacchus. J. Reprod. Fertil. 56 (1979) 23-32
13. Chetty M., and Elson J. Biochemistry in the diagnosis and management of abnormal early pregnancy. Clin. Obstet. Gynecol. 50 (2007) 55-66
14. Clutton-Brock T.H., Brotherton P.N.M., Smith R., McIlrath G.M., Kansky R., Gainor D., O'Riain M.J., and Skinner J.D. Infanticide and expulsion of females in a cooperative mammals. Proc. R. Soc. Lond., Ser. B 265 (1998) 2291-2295
15. Converse L.J., Carlson A.A., Ziegler T.E., and Snowdon C.T. Communication of ovulatory state to mates by female pygmy marmosets, Cebuella pygmaea. Anim. Behav. 49 (1995) 615-621
16. Corbett L.K. Social dynamics of a captive dingo pack: population regulation by dominant female infanticide. Ethology 78 (1988) 177-198
17. Crespi B.J., and Ragsdale J.E. A skew model for the evolution of sociality via manipulation: why it is better to be feared than loved. Proc. R. Soc. Lond., B 267 (2000) 821-828
18. de Waal F.B.M. Dynamics of social relationships. In: Smuts B.B., Cheney D.L., Seyfarth R.M., Wrangham R.W., and Struhsaker T.T. (Eds). Primate Societies (1987), University of Chicago Press, Chicago 421-429
19. Digby L. Infant care, infanticide, and female reproductive strategies in polygynous groups of common marmosets (Callithrix jacchus). Behav. Ecol. Sociobiol. 37 (1995) 51-61
20. Digby L.J. Social organization in a wild population of Callithrix jacchus: II. Intragroup social behavior. Primates 36 (1995) 361-375
21. Digby L.J. Infanticide by female mammals: implications for the evolution of social systems. In: van Schaik C.P., and Janson C.H. (Eds). Infanticide by Males and its Implications (2000), Cambridge University Press, Cambridge 423-446
22. Digby L.J., Ferrari S.F., and Saltzman W. Callitrichines: the role of competition in cooperatively breeding species. In: Campbell C.J., Fuentes A., MacKinnon K.C., Panger M., and Bearder S.K. (Eds). Primates in Perspective (2007), Oxford University Press, New York 85-106
23. Eastman S.-A.K., Makawiti D.W., Collins W.P., and Hodges J.K. Pattern of excretion of urinary steroid metabolites during the ovarian cycle and pregnancy in the marmoset monkey. J. Endocrinol. 102 (1984) 19-26
24. Eggert A.-K., and Müller J.K. Timing of oviposition and reproductive skew in cobreeding female burying beetles (Nicrophorus vespilloides). Behav. Ecol. 11 (2000) 357-366
25. Elwood R.W. Changes in the responses of male and female gerbils (Meriones unguiculatus) towards test pups during the pregnancy of the female. Anim. Behav. 25 (1977) 46-51
26. Elwood R.W. The development, inhibition and disinhibition of pup-cannibalism in the Mongolian gerbil. Anim. Behav. 28 (1980) 1188-1194
27. Elwood R.W. Postparturitional reestablishment of pup cannibalism in female gerbils. Dev. Psychobiol. 14 (1981) 209-212
28. Faulkes C.G., Arruda M.F., and Monteiro da Cruz M.A.O. Matrilineal genetic structure within and among populations of the cooperatively breeding common marmoset, Callithrix jacchus. Mol. Ecol. 12 (2003) 1101-1108
29. Ferrari S.F., and Digby L.J. Wild Callithrix groups: stable extended families?. Am. J. Primatol. 38 (1996) 19-27
30. Fite J.E., and French J.A. Pre- and postpartum sex steroids in female marmosets (Callithrix kuhlii): is there a link with infant survivorship and maternal behavior?. Horm. Behav. 38 (2000) 1-12
31. French J.A. Proximate regulation of singular breeding in callitrichid primates. In: Solomon N.G., and French J.A. (Eds). Cooperative Breeding in Mammals (1997), Cambridge University Press, New York 34-75
32. French J.A., Bales K.L., Baker A.J., and Dietz J.M. Endocrine monitoring of wild dominant and subordinate female Leontopithecus rosalia. Int. J. Primatol. 24 (2003) 1281-1300
33. Hackländer K., Möstl E., and Arnold W. Reproductive suppression in female Alpine marmots, Marmota marmota. Anim. Behav. 65 (2003) 1133-1140
34. Hager R., and Johnstone R.A. Infanticide and control of reproduction in cooperative and communal breeders. Anim. Behav. 67 (2004) 941-949
35. Hamilton I.M. A commitment model of reproductive inhibition in cooperatively breeding groups. Behav. Ecol. 15 (2004) 585-591
36. Harlow C.R., Gems S., Hodges J.K., and Hearn J.P. The relationship between plasma progesterone and the timing of ovulation and early embryonic development in the marmoset monkey (Callithrix jacchus). J. Zool. 201 (1983) 273-282
37. Hearn J.P. Restraining device for small monkeys. Lab. Anim. 11 (1977) 261-262
38. Heger W., Merker H.-J., and Neubert D. Frequency of prenatal loss in marmoset monkeys (Callithrix jacchus). In: Neubert D., Merker H.-J., and Hendrickx A.G. (Eds). Nonhuman Primates - Developmental Biology and Toxicology (1988), Ueberreuter Wissenschraft, Vienna 129-140
39. Hrdy S.B. Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol. Sociobiol. 1 (1979) 13-40
40. Huck U.W., Bracken A., and Lisk R.D. Female-induced pregnancy block in the golden hamster. Behav. Neural Biol. 38 (1983) 190-193
41. Jaquish C.E., Gage T.B., and Tardif S.D. Reproductive factors affecting survivorship in captive Callitrichidae. Am. J. Phys. Anthropol. 84 (1991) 291-305
42. Jaquish C.E., Tardif S.D., Toal R.L., and Carson R.L. Patterns of prenatal survival in the common marmoset (Callithrix jacchus). J. Med. Primatol. 25 (1996) 57-63
43. Johnson E.O., Kamilaris T.C., Carter S., Gold P.W., and Chrousos G.P. "Environmental stress" and reproductive success in the common marmoset (Callithrix jacchus). Am. J. Primatol. 25 (1991) 191-201
44. Johnstone R.A., and Cant M.A. Reproductive skew and the threat of eviction: a new perspective. Proc. R. Soc. Lond., B 266 (1999) 275-279
45. Keeping M.G. Social organization and division of labour in colonies of the polistine wasp, Belonogaster petiolata. Behav. Ecol. Sociobiol. 31 (1992) 211-224
46. Keller L., and Reeve H.K. Partitioning of reproduction in animal societies. TREE 9 (1994) 98-102
47. Kirkpatrick-Tanner M., Aeschlimann C., and Anzenberger G. Occurrence of an infanticide within a captive polygynous group of common marmosets, Callithrix jacchus. Folia Primatol. 67 (1996) 52-58
48. Lazaro-Perea C., Castro C.S.S., Harrison R., Araujo A., Arruda M.F., and Snowdon C.T. Behavioral and demographic changes following the loss of the breeding female in cooperatively breeding marmosets. Behav. Ecol. Sociobiol. 48 (2000) 137-146
49. Livesey J.H., Roud H.K., Metcalf M.G., and Donald R.A. Glycerol prevents loss of immunoreactive follicle-stimulating hormone and luteinizing hormone from frozen urine. J. Endocrinol. 98 (1983) 381-384
50. Melo L., Mendes Pontes A.R., and Monteiro da Cruz M.A.O. Infanticide and cannibalism in wild common marmosets. Folia Primatol. 74 (2003) 48-50
51. Mumme R.L., Koenig W.D., and Pitelka F.A. Reproductive competition in the communal acorn woodpecker: sisters destroy each other's eggs. Nature 306 (1983) 583-584
52. Nievergelt C.M., and Martin R.D. Energy intake during reproduction in captive common marmosets (Callithrix jacchus). Physiol. Behav. 65 (1999) 849-854
53. Nievergelt C.M., Digby L.J., Ramakrishnan U., and Woodruff D.S. Genetic analysis of group composition and breeding system in a wild common marmoset (Callithrix jacchus) population. Int. J. Primatol. 21 (2000) 1-20
54. Oerke A.-K., Einspanier A., and Hodges J.K. Detection of pregnancy and monitoring patterns of uterine and fetal growth in the marmoset monkey (Callithrix jacchus) by real-time ultrasonography. Am. J. Primatol. 36 (1995) 1-13
55. Packer C., and Pusey A.E. Infanticide in carnivores. In: Hausfater G., and Hrdy S.B. (Eds). Infanticide (1984), Aldine, New York 31-42
56. Pryce C.R., Abbott D.H., Hodges J.K., and Martin R.D. Maternal behavior is related to prepartum urinary estradiol levels in red-bellied tamarin monkeys. Physiol. Behav. 44 (1988) 717-726
57. Rasa O.A.E. The dwarf mongoose: a study of behavior and social structure in relation to ecology in a small social carnivore. In: Rosenblatt J. (Ed). Advances in the Study of Behavior (1987), Academic Press, New York 121-163
58. Ratnieks F.L.W., and Visscher P.K. Worker policing in the honeybee. Nature 342 (1989) 796-797
59. Rico Hernández G., and Parás Garcia A. Retrospective study of the causes of infant death in a common marmoset (Callithrix jacchus jacchus) colony. Lab. Primate Newsl. 40 (2001) 1-5
60. Roda S.A., and Mendes Pontes A.R. Polygyny and infanticide in common marmosets in a fragment of the Atlantic forest of Brazil. Folia Primatol. 69 (1998) 372-376
61. Rothe H., Darms K., and Koenig A. Sex ratio and mortality in a laboratory colony of the common marmoset (Callithrix jacchus). Lab Anim. 26 (1992) 88-99
62. Rowell T.E. The concept of social dominance. Behav. Biol. 11 (1974) 131-154
63. Saltzman W. Reproductive competition among female common marmosets (Callithrix jacchus): proximate and ultimate causes. In: Jones C.B. (Ed). Sexual Selection and Reproductive Competition in Primates: New Perspectives and Directions (2003), American Society of Primatologists, Norman, OK 197-229
64. Saltzman W., and Abbott D.H. Diminished maternal responsiveness during pregnancy in multiparous female common marmosets. Horm. Behav. 47 (2005) 151-163
65. Saltzman W., Schultz-Darken N.J., Scheffler G., Wegner F.H., and Abbott D.H. Social and reproductive influences on plasma cortisol in female marmoset monkeys. Physiol. Behav. 56 (1994) 801-810
66. Saltzman W., Schultz-Darken N.J., Severin J.M., and Abbott D.H. Escape from social suppression of sexual behavior and of ovulation in female common marmosets. Ann. N.Y. Acad. Sci. 807 (1997) 567-570
67. Saltzman W., Severin J.M., Schultz-Darken N.J., and Abbott D.H. Behavioral and social correlates of escape from suppression of ovulation in female common marmosets housed with the natal family. Am. J. Primatol. 41 (1997) 1-21
68. Saltzman W., Schultz-Darken N.J., Wegner F.H., Wittwer D.J., and Abbott D.H. Suppression of cortisol levels in subordinate female marmosets: reproductive and social contributions. Horm. Behav. 33 (1998) 58-74
69. Saltzman W., Pick R.R., Salper O.J., Liedl K.J., and Abbott D.H. Onset of plural cooperative breeding in common marmoset families following replacement of the breeding male. Anim. Behav. 68 (2004) 59-73
70. Snowdon C.T. Infant care in cooperatively breeding species. Adv. Study Behav. 25 (1996) 643-689
71. Sousa M.B.C., Albuquerque A.C.S.R., Albuquerque F.S., Araujo A., Yamamoto M.E., and Arruda M.F. Behavioral strategies and hormonal profiles of dominant and subordinate common marmoset (Callithrix jacchus) females in wild monogamous groups. Am. J. Primatol. 67 (2005) 37-50
72. Tardif S.D. The bioenergetics of parental behavior and the evolllution of alloparental care in marmosets and tamarins. In: Solomon N.G., and French J.A. (Eds). Cooperative Breeding in Mammals (1997), Cambridge University Press, New York 11-33
73. Tardif S.D., and Bales K.L. Relations among birth condition, maternal condition, and postnatal growth in captive common marmoset monkeys (Callithrix jacchus). Am. J. Primatol. 62 (2004) 83-94
74. Tardif S.D., Smucny D.A., Abbott D.H., Mansfield K., Schultz-Darken N., and Yamamoto M.E. Reproduction in captive common marmosets (Callithrix jacchus). Comp. Med. 53 (2003) 364-368
75. Tardif S.D., Ziegler T.E., Power M., and Layne D.G. Endocrine changes in full-term pregnancies and pregnancy loss due to energy restriction in the common marmoset (Callithrix jacchus). J. Clin. Endocrinol. Metab. 90 (2005) 335-339
76. Torii R., Nigi H., Koizumi H., and Tanioka Y. Serum chorionic gonadotropin, progesterone, and estradiol-17beta levels during pregnancy in the common marmoset, Callithrix jacchus. Primates 30 (1989) 207-215
77. Tuomi J., Agrell J., and Mappes T. On the evolutionary stability of female infanticide. Behav. Ecol. Sociobiol. 40 (1997) 227-233
78. Vehrencamp S.L. Relative fecundity and parental effort in communally nesting anis, Crotophaga sulcirostris. Science 197 (1977) 403-405
79. Vehrencamp S.L. A model for the evolution of despotic versus egalitarian societies. Anim. Behav. 31 (1983) 667-682
80. Wasser S.K., and Starling A.K. Proximate and ultimate causes of reproductive suppression among female yellow baboons at Mikumi National Park, Tanzania. Am. J. Primatol. 16 (1988) 97-121
81. Webley G.E., and Hearn J.P. Embryo-maternal interactions during the establishment of pregnancy in primates. Oxf. Rev. Reprod. Biol. 16 (1994) 1-32
82. Windle C.P., Baker H.F., Ridley R.M., Oerke A.-K., and Martin R.D. Unrearable litters and prenatal reduction of litter size in the common marmoset (Callithrix jacchus). J. Med. Primatol. 28 (1999) 73-83
83. Yamamoto, M.E., Arruda, M.M.F., Alencar, A.I., Sousa, M.B.C., Araújo, A., in press. Mating systems and female-female competition in the common marmosets, Callithrix jacchus. In: L.C. Davis, S.M. Ford, L.M. Porter (Eds.), The Smallest Anthropoids: the Marmoset/Callimico Radiation. Springer-Verlag.
84. Young A.J., Carlson A.A., Monfort S.L., Russell A.F., Bennett N.C., and Clutton-Brock T. Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 12005-12010
85. Zar J.H. Biostatistical Analysis. 4th ed. (1999), Prentice Hall, Upper Saddle River, NJ
86. Ziegler T.E., Matteri R.L., and Wegner F.H. Detection of urinary gonadotropins in callitrichid monkeys with a sensitive immunoassay based upon a unique monoclonal antibody. Am. J. Primatol. 31 (1993) 181-188
87. Ziegler T.E., Scheffler G., and Snowdon C.T. The relationship of cortisol levels to social environment and reproductive functioning in female cotton-top tamarins, Saguinus oedipus. Horm. Behav. 29 (1995) 407-424