Hormonal and Experiential Predictors of Infant Survivorship and Maternal Behavior in a Monogamous Primate (Callicebus cupreus)

American Journal of Primatology

Volumn 74, Issue 5, 2012, Pages 462-470

  Jarcho, Michael R ^a   Mendoza, Sally P ^a,b   Bales, Karen L ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Infant survival; Maternal behavior; Maternal parity; Steroid hormones

Indexed keywords

ESTRONE; PREGNANEDIOL;

AGE CLASS; FUNCTIONAL ROLE; HORMONE; MATERNAL CARE; MATERNAL EFFECT; PARTURITION; PREGNANCY; PRIMATE; STEROID; SURVIVORSHIP;

AGE; ANIMAL; ARTICLE; BIRTH; BREEDING; ENZYME IMMUNOASSAY; FEMALE; LIVE BIRTH; MATERNAL BEHAVIOR; PARITY; PHYSIOLOGY; PITHECIIDAE; PREGNANCY; URINE;

AGE FACTORS; ANIMALS; ESTRONE; FEMALE; IMMUNOENZYME TECHNIQUES; LIVE BIRTH; MATERNAL BEHAVIOR; PARITY; PARTURITION; PITHECIIDAE; PREGNANCY; PREGNANCY, ANIMAL; PREGNANEDIOL;

CALLICEBUS; CALLICEBUS CUPREUS; PRIMATES;

EID: 84859912737     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.22003     Document Type: Article

References (60)

1. Albrecht ED, Pepe GJ. 1999. Central integrative role of oestrogen in modulating the communication between the placenta and fetus that results in primate fecal-placental development. Placenta 20:129-139.
2. Amico JA, Thomas A, Hollingshead DJ. 1997. The duration of estradiol and progesterone exposure prior to progesterone withdrawal regulates oxytocin mRNA levels in the paraventricular nucleus of the rat. Endocr Res 23:141-156.
3. Bardi M, French JA, Ramirez SM, Brent L. 2004. The role of the endocrine system in baboon maternal behavior. Biol Psychiatry 55:724-732.
4. Bardi M, Shimizu K, Barrett GM, Borgognini-Tarli SM, Huffman MA. 2003. Peripartum sex steroid changes and maternal style in rhesus and Japanese macaques. Gen Comp Endocrinol 133:323-331.
5. Bardi M, Shimizu K, Fujita S, Borgognini-Tarli SM, Huffman MA. 2001. Hormonal correlates of maternal style in captive macaques (Macaca fuscata, M. mulatta). Int J Primatol 22:647-662.
6. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:12.
7. Blyth BJ, Hollingshead DJ, Amico JA. 1997. Time course of induction of oxytocin messenger ribonucleic acid levels in the hypothalamic paraventricular nucleus of ovariectomized rats following gonadal steroid administration. Life Sci 60:2427-2433.
8. Brown AG, Leite RS, Strauss III JF. 2006. Mechanisms underlying "functional" progesterone withdrawal at parturition. Ann N Y Acad Sci 1034:36-49.
9. Cameron EZ, Linklater WL, Stafford KJ, Minot EO. 2000. Aging and improving reproductive success in horses: declining residual reproductive value or just older and wiser? Behav Ecol Sociobiol 47:243-249.
10. Caraty A, Skinner DC. 1999. Progesterone priming is essential for the full expression of the positive feedback effect of estradiol in inducing preovulatory gonadotropin-releasing hormone surge in the ewe. Endocrinology 140:165-170.
11. Chambers PL, Hearn JP. 1985. Embryonic, foetal, placental development in the common marmoset (Callithrix jacchus). J Zool 207:545-561.
12. Champagne FA. 2008. Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 29:386-397.
13. Chiesa C, Osborn JF, Haass C, Natale F, Spinelli M, Scapillati E, Spinelli A, Pacifico L. 2008. Ghrelin, leptin, IGF-1, IGFBP-3, and insulin concentrations at birth: is there a relationship with fetal growth and neonatal anthropometry? Clin Chem 54:550-558.
14. Dwyer CM, Smith LA. 2008. Parity effects on maternal behaviour are not related to circulating oestradiol concentrations in two breeds of sheep. Physiol Behav 93:148-154.
15. Epple G. 1978. Reproductive and social behavior of marmosets with special reference to captive breeding. Primates Med 10:50-62.
16. Fairbanks LA. 1996. Individual differences in maternal style: causes and consequences for mothers and offspring. Adv Study Behav 25:579-611.
17. Feldman R, Gordon I, Schneiderman I, Weisman O, Zagoory-Sharon O. 2010. Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent-infant contact. Psychoneuroendocrinology 35:1133-1141.
18. Fragaszy DM, Schwarz S, Shimosaka D. 1982. Longitudinal observations of care and development of infant titi monkeys (Callicebus moloch). Am J Primatol 2:191-200.
19. Fuentes A. 1998. Re-evaluating primate monogamy. Am Anthropol 100:890-907.
20. Godfrey K. 2002. The role of the placenta in fetal programming - a review. Placenta 23:S20-S27.
21. Goedhart G, Vrijkotte TG, Roseboom TJ, van der Wal MF, Cuijpers P, Bonsel GJ. 2010. Maternal cortisol and offspring birthweight: results from a large prospective cohort study. Psychoneuroendocrinology 35:644-652.
22. Green WCH. 1990. Reproductive effort and associated costs in bison (Bison bison): do older mothers try harder? Behav Ecol 1:148-160.
23. Haig D. 1996. Placental hormones, genomic imprinting, and maternal-fetal communication. J Evol Biol 9:357-380.
24. Hauser H, Gandelman R. 1985. Lever pressing for pups: evidence for hormonal influence upon maternal behavior of mice. Horm Behav 19:454-468.
25. Hoffman KA, Mendoza SP, Hennessy MB, Mason WA. 1995. Responses of infant titi monkeys, Callicebus moloch, to removal of one or both parents: evidence for paternal attachment. Dev Psychobiol 28:399-407.
26. Hrdy SB. 1999. Mother nature. New York: Pantheon.
27. Insel TR, Young LJ. 2001. The neurobiology of attachment. Nat Neurosci Rev 2:129-136.
28. Jaffe M. 1886. Measurement of creatinine using picric acid. Z Physiol Chem 10:391-400.
29. Kallen CB. 2004. Steroid hormone synthesis in pregnancy. Obstet Gynecol Clin North Am 31:795-816.
30. Kendrick KM, Keverne EB. 1991. Importance of progesterone and estrogen priming for the induction of maternal behavior by vaginocervical stimulation in sheep: effects of maternal experience. Physiol Behav 49:745-750.
31. Kendrick KM, Keverne EB, Baldwin BA. 1987. Intracerebroventricular oxytocin stimulates maternal behavior in sheep. Neuroendocrinology 46:56-61.
32. Keverne EB. 1996. Psychopharmacology of maternal behavior. J Psychopharmacol 10:16-22.
33. Kleemann DO, Walker SK, Seamark RF. 1994. Enhanced fetal growth in sheep administered progesterone during the first three days of pregnancy. J Reprod Fertil 102:411-417.
34. Maestripieri D. 1999. Changes in social behavior and their hormonal correlates during pregnancy in pig-tail macaques. Int J Primatol 20:707-718.
35. Maestripieri D, Wallen K, Carroll KA. 1997. Infant abuse runs in families of group-living pigtail macaques. Child Abuse Negl 21:465-571.
36. Meddle SL, Bishop VR, Gkoumassi E, van Leeuwen FW, Douglas AJ. 2007. Dynamic changes in oxytocin receptor expression and activation at parturition in the rat brain. Endocrinology 148:5095-5104.
37. Mendoza SP. 1999. Squirrel monkeys. In: Poole T, editor. The UFAW handbook on the care and management of laboratory animals, 7th ed. Oxford: Blackwell Science Ltd. p 591-600.
38. Mendoza SP, Mason WA. 1986. Parental division of labour and differentiation of attachments in a monogamous primate (Callicebus moloch). Anim Behav 34:1336-1347.
39. Moltz H, Lubin M, Leon M, Numan M. 1970. Hormonal induction of maternal behavior in the ovariectomized nulliparous rat. Physiol Behav 5:1373-1377.
40. Monro CJ, Stabenfeldt GH, Cragun JR, Addiego LA, Overstreet JW, Lasley BL. 1991. Relationship of serum estradiol and progesterone concentrations to the excretion profiles of their major urinary metabolites as measured by enzyme immunoassay and radioimmunoassay. Clin Chem 37:838-844.
41. Power ML, Schulkin J. 2006. Functions of corticotropin-releasing hormone in anthropoid primates: from brain to placenta. Am J Hum Biol 18:431-447.
42. Pryce CR. 1993. The regulation of maternal behavior in marmosets and tamarins. Behav Processes 30:201-224.
43. Rainey WE, Rehman KS, Carr BR. 2004. The human fetal adrenal: making adrenal androgens for placental estrogens. Semin Reprod Med 22:327-336.
44. Ramirez SM, Bardi M, French JA, Brent L. 2004. Hormonal correlates of changes in interest in unrelated infants across the peripartum period in female baboons (Papio hamadryas anubis sp.). Horm Behav 46:520-528.
45. Rosenblatt JS, Siegel HI. 1981. Factors governing the onset and maintenance of maternal behavior among nonprimate mammals: the role of hormonal and non-hormonal factors. In: Gubernick DJ, Klopfer PH, editors. Parental care in mammals. New York: Plenum. p 13-76.
46. Rutherford JN. 2009. Fetal signaling through placental structure and endocrine function: illustrations and implications from a nonhuman primate model. Am J Hum Biol 21:745-753.
47. Saltzman W, Maestripieri D. 2011. The neuroendocrinology of primate maternal behavior. Prog Neuropsychopharmacol Biol Psychiatry 35:1192-1204.
48. Shideler SE, Monro CJ, Tell L, Owiti G, Laughlin L, Chatterton Jr RT, Lasley BL. 1990. The relationship of serum estradiol and progesterone concentrations to the enzyme immunoassay measurements of urinary estrone conjugates and immunoreactive pregnanediol-3-glucuronide in Macaca mulatta. Am J Primatol 22:113-122.
49. Shively CA, Wood CE, Register TC, Willard SL, Lees CJ, Chen H, ... Cline JM. 2007. Hormone therapy effects on social behavior and activity levels of surgically postmenopausal cynomolgus monkeys. Psychoneuroendocrinology 32:981-990.
50. Siegel HI, Rosenblatt JS. 1975a. Estrogen induced maternal behavior in hysterectomized-ovariectomized virgin rats. Physiol Behav 14:465-471.
51. Siegel HI, Rosenblatt JS. 1975b. Progesterone inhibition of estrogen-induced maternal behavior in hysterectomized-ovariectomized virgin rats. Horm Behav 6:223-230.
52. Smith R, Mesiano S, Nicholson R, Clifton V, Zakar T. 2005. The regulation of human parturition. In: Power ML, Schulkin J, editors. Birth, distress and disease: placenta-brain interactions. Cambridge: Cambridge University Press. p 74-87.
53. Tardif SD, Richter CB, Carson RL. 1984. Effects of sibling-rearing experience on future reproductive success in two species of Callitrichidae. Am J Primatol 6:377-380.
54. Terkel J, Rosenblatt JS. 1972. Humoral factors underlying maternal behavior at parturition: cross transfusion between freely moving rats. J Comp Physiol Psychol 3:365-371.
55. Thomas A, Shughrue PJ, Merchenthaler I, Amico JA. 1999. The effects of progesterone on oxytocin mRNA levels in the paraventricular nucleus of the female rat can be altered by the administration of diazepam or ru486. J Neuroendocrinol 11:137-144.
56. Valeggia CR. 1996. Social influences on the development of sexual physiology and behavior in titi monkey females (Callicebus cupreus) [Dissertation]. Davis: University of California.
57. Valeggia CR, Mendoza SP, Fernandez-Duque E, Mason WA, Lasley B. 1999. Reproductive biology of female titi monkeys (Callicebus moloch) in captivity. Am J Primatol 47:183-195.
58. Wang MW, Crombie DL, Hayes JS, Heap RB. 1995. Aberrant maternal behaviour in mice treated with a progesterone receptor antagonist during pregnancy. J Endocrinol 145:371-377.
59. Wilson ME, Legendre A, Pazol K, Fisher J, Chikazawa K. 2005. Gonadal steroid modulation of the limbic-hypothalamic-pituitary-adrenal (LHPA) axis is influenced by social status in female rhesus monkeys. Endocrine 26:89-97.
60. Yoshinaga K, Hawkins RA, Stocker JF. 1969. Estrogen secretion by the rat ovary in vivo during the estrous cycle and pregnancy. Endocrinology 85:103-112.