Seasonality, sociality, and reproduction: Long-term stressors of ring-tailed lemurs (Lemur catta)

Hormones and Behavior

Volumn 57, Issue 1, 2010, Pages 76-85

  Starling, Anne P ^a   Charpentier, Marie J E ^a   Fitzpatrick, Courtney ^a   Scordato, Elizabeth S ^a   Drea, Christine M ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

Aggression; Breeding season; Corticosterone; Cortisol; Fecal steroids; Female dominance; Reproduction; Strepsirrhine primate; Stress

Indexed keywords

CORTICOSTERONE; GLUCOCORTICOID;

AGE; ARTICLE; BLOOD SAMPLING; BREEDING; CHRONIC STRESS; CONCEPTION; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEMOGRAPHY; FECES ANALYSIS; FEMALE; FIRST TRIMESTER PREGNANCY; GENETIC ANALYSIS; GESTATION PERIOD; GROUP STRUCTURE; HETEROZYGOSITY; HORMONE DETERMINATION; LACTATION; LEMUR CATTA; MALE; NONHUMAN; ORGANISM SOCIAL GROUP; PHYSIOLOGICAL STRESS; PRIORITY JOURNAL; PROSIMIAN; REPRODUCTION; SEASONAL VARIATION; SECOND TRIMESTER PREGNANCY; SEX DIFFERENCE; SEXUAL BEHAVIOR; SOCIAL DOMINANCE; SOCIAL ENVIRONMENT; THIRD TRIMESTER PREGNANCY;

ANIMALS; CIRCADIAN RHYTHM; CORTICOSTERONE; FECES; FEMALE; GLUCOCORTICOIDS; HYDROCORTISONE; LEMUR; MALE; MATERNAL-FETAL EXCHANGE; MODELS, BIOLOGICAL; PREGNANCY; REPRODUCTION; SEASONS; SEX CHARACTERISTICS; SEX FACTORS; SOCIAL DOMINANCE; SOCIAL ENVIRONMENT; STRESS, PHYSIOLOGICAL;

EID: 73049102075     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2009.09.016     Document Type: Article

References (76)

1. Abbott D.H., Keverne E.B., Bercovitch F.B., Shively C.A., Mendoza S.P., Saltzman W., Snowdon C.T., Ziegler T.E., Banjevic M., Garland Jr. T., and Sapolsky R.M. Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm. Behav. 43 (2003) 67-82
2. Allolio B., Hoffman J., Linton E.A., Winkelmann W., Kusche M., and Schulte H.M. Diurnal salivary cortisol patterns during pregnancy and after delivery: relationship to plasma corticotropin-releasing hormone. Clinical Endocrinol. 33 (1990) 279-290
3. Altmann J., Lynch J.W., Nguyen N., Alberts S.C., and Gesquiere L.R. Life-history correlates of steroid concentrations in wild peripartum baboons. Amer. J. Primatol. 64 (2004) 95-106
4. Bales K.L., French J.A., Hostetler C.M., and Dietz J.M. Social and reproductive factors affecting cortisol levels in wild female golden lion tamarins (Leontopithecus rosalia). Am. J. Primatol. 67 (2005) 25-35
5. Bercovitch F.B., and Clarke A.S. Dominance rank, cortisol concentrations, and reproductive maturation in male rhesus macaques. Physiol. Behav. 58 (1995) 215-221
6. Cavigelli S.A. Behavioural patterns associated with faecal cortisol levels in free-ranging female ring-tailed femurs, Lemur catta. Anim. Behav. 57 (1999) 935-944
7. Cavigelli S.A., and Pereira M.E. Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Horm. Behav. 37 (2000) 246-255
8. Cavigelli S.A., Dubovick T., Levash W., Jolly A., and Pitts A. Female dominance status and fecal corticoids in a cooperative breeder with low reproductive skew: ring-tailed lemurs (Lemur catta). Horm. Behav. 43 (2003) 166-179
9. Charpentier M.J.E., Williams C.V., and Drea C.M. Inbreeding depression in ring-tailed lemurs (Lemur catta): genetic diversity predicts parasitism, immunocompetence, and survivorship. Conserv. Genet. 9 (2008) 1605-1615
10. Charpentier M.J.E., Boulet M., and Drea C.M. Smelling right: the scent of male lemurs advertises genetic quality and relatedness. Mol. Ecol. 17 (2008) 3225-3233
11. Charpentier, M.J.E., Crawford, J., Boulet, M., Drea, C.M. submitted for publication. Ring-tailed lemurs (Lemur catta) detect the genetic quality and relatedness of conspecifics via olfactory cues.
12. Coe C.L., and Levine S. Diurnal and annual variation of adrenocortical activity in the squirrel-monkey. Am. J. Primatol. 35 4 (1995) 283-292
13. Creel S. Social dominance and stress hormones. Trends Ecol. Evol. 16 (2001) 491-497
14. Creel S., Creel N.M., and Monfort S.L. Social stress and dominance. Nature 379 6562 (1996) 212
15. Drea C.M. Sex differences and seasonal patterns in steroid secretion in Lemur catta: are socially dominant females hormonally 'masculinized'?. Horm. Behav. 51 (2007) 555-567
16. Drea C.M., and Scordato E.S. Olfactory communication in the ringtailed lemur (Lemur catta): form and function of multimodal signals. In: Hurst J.L., Beynon R.J., Roberts S.C., and Wyatt T. (Eds). Chemical signals in vertebrates 11 (2008), Springer Press, New York 91-102
17. Evans C.S., and Goy R.W. Social behaviour and reproductive cycles in captive ring-tailed lemurs (Lemur catta). J. Zool. 156 (1968) 181-197
18. Fichtel C., Kraus C., Ganswindt A., and Heistermann M. Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux's sifakas (Propithecus verreauxi). Horm. Behav. 51 (2007) 640-648
19. Garner S.R., Madison B.N., Bernier N.J., and Neff B.D. Juvenile growth and aggression in diploid and triploid Chinook salmon Oncorhynchus tshawytscha (Walbaum). J. Fish Biol. 73 (2008) 169-185
20. Gerber P.R., Moisson P.R., and Heistermann M.R. Urinary progestogen and estrogen excretion during pregnancy in Eulemur macaco flavifrons, E. rubriventer, and Hapalemur griseus occidentalis. Int. J. Primatol. 25 (2004) 449-463
21. Gesquière L.R., Altmann J., Khan M.Z., Couret J., Yu J.C., Endres C.S., Lynch J.W., Ogola P., Fox E.A., Alberts S.C., and Wango E.O. Coming of age: steroid hormones of wild immature baboons (Papio cynocephalus). Amer. J. Primatol. 67 (2005) 83-100
22. Gould L., Ziegler T.E., and Wittwer D.J. Effects of reproductive and social variables on fecal glucocorticoid levels in a sample of adult male ring-tailed lemurs (Lemur catta) at the Beza Mahafaly Reserve. Madagascar Am. J. Primatol. 67 (2005) 5-23
23. Goymann W., and Wingfield J.C. Allostatic load, social status and stress hormones: the costs of social status matter. Anim. Behav. 67 (2004) 591-602
24. Goymann W., East M.L., Wachter B., Höner O.P., Möstl E., Van't Hof T.J., and Hofer H. Social, state-dependent and environmental modulation of faecal corticosteroid levels in free-ranging female spotted hyenas. Proc. R. Soc. Lond. B 268 (2001) 2453-2459
25. Goymann W., East M.L., Wachter B., Höner O.P., Möstl E., and Hofer H. Social status does not predict corticosteroid levels in postdispersal male spotted hyenas. Horm. Behav. 43 (2003) 474-479
26. Holekamp K.E., and Smale L. Dispersal status influences hormones and behavior in the male spotted hyena. Horm. Behav. 33 (1998) 205-216
27. Jolly A. Lemur behavior (1966), University of Chicago Press, Chicago
28. Kappeler P.M. Female dominance in Lemur catta: more than just female feeding priority. Folia Primatol. 55 (1990) 92-95
29. Khan M.Z., Altmann J., Isani S.S., and Yu J. A matter of time: evaluating the storage of fecal samples for steroid analysis. Gen. Comp. Endocrinol. 128 (2002) 57-64
30. Kitay J.I. Pituitary-adrenal function in the rat after gonadectomy and gonadal hormone replacement. Endocrinology 73 (1963) 253-260
31. Kosowska B., and Zdrojewicz Z. The role of genetic variability in the hormonal adaptive mechanism. 1. The effect of various homozygosity level on the adrenal-cortex hormone concentrations (corticosterone and aldosterone) in the blood-serum of rats exposed to 2 types of stress. Journal of Animal Breeding and Genetics 108 (1991) 147-153
32. Koyama N. Mating behavior of ring-tailed lemurs (Lemur catta) at Berenty, Madagascar. Primates 29 (1988) 163-175
33. Lockwood C.J., Radunovic N., Nastic D., Petkovic S., Aigner S., and Berkowitz G.S. Corticotropin-releasing hormone and related pituitary-adrenal axis hormones in fetal and maternal blood during the second half of pregnancy. J. Perinatal Medicine 24 (1996) 243-251
34. Lynch J.W., Ziegler T.E., and Strier K.B. Individual and seasonal variation in fecal testosterone and cortisol levels of wild capuchin monkeys, Cebus apella nigritus. Horm. Behav. 41 (2002) 275-287
35. Manogue K.R. Dominance status and adrenocortical reactivity to stress in squirrel monkeys (Saimiri sciureus). Primates 14 (1975) 457-463
36. Mateo J.M. Developmental and geographic variation in stress hormones in wild Belding's ground squirrels (Spermophilus beldingi). Horm. Behav. 50 (2006) 718-725
37. Moberg G.P. Biological response to stress: implications for animal welfare. The biology of animal stress (2000), CABI Publishing, New York 1-21
38. Muller M.N., and Wrangham R.W. Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii). Behav. Ecol. Sociobiol. 55 (2004) 332-340
39. Munck A., Guyre P.M., and Holbrook N.J. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr. Rev. 5 (1984) 25-44
40. Nakamichi M., and Koyama N. Social relationships among ring-tailed lemurs (Lemur catta) in two free-ranging troops at Berenty Reserve, Madagascar. International J. Primatol. 18 (1997) 73-93
41. Nelson, R.J., 2000. An introduction to behavioral endocrinology. Sinauer, Sunderland, MA.
42. 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
43. Ostner J., Kappeler P., and Heistermann M. Androgen and glucocorticoid levels reflect seasonally occurring social challenges in male redfronted lemurs (Eulemur fulvus rufus). Behav. Ecol. Sociobiol. 62 (2008) 627-638
44. Parga J.A., and Lessnau R.G. Female age-specific reproductive rates, birth seasonality, and infant mortality of ring-tailed lemurs on St. Catherines Island: 17-year reproductive history of a free-ranging colony. Zoo Biol. 24 (2005) 295-309
45. Pepe G.J., and Albrecht E.D. Actions of placental and fetal adrenal steroid hormones in primate pregnancy. Endoc. Rev. 16 (1995) 608-648
46. Pereira M.E. Asynchrony within estrous synchrony among ringtailed lemurs (Primates: Lemuridae). Phys. Behav. 49 (1991) 47-52
47. Perret M., and Predine J. Effects of long-term grouping on serum cortisol levels in Microcebus murinus (Prosimii). Horm. Behav. 18 (1984) 346-358
48. Phillips J.G., and Poolsanguan W. A method to study temporal changes in adrenal activity in relation to sexual status in the female laboratory rat. Endocrinology 77 (1978) 283-291
49. Pride R.E. Optimal group size and seasonal stress in ring-tailed lemurs (Lemur catta). Behav. Ecol 16 (2005) 550-560
50. Pride R.E. High faecal glucocorticoid levels predict mortality in ring-tailed lemurs (Lemur catta). Biol. Lett. 1 (2005) 60-63
51. Pride R.E. Foraging success, agonism, and predator alarms: behavioral predictors of cortisol in Lemur catta. Int. J. Primatol. 26 (2005) 295-319
52. Robbins M.M., and Czekala N.M. A preliminary investigation of urinary testosterone and cortisol levels in wild male mountain gorillas. Am. J. Primatol. 43 (1997) 51-64
53. 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
54. Sands J., and Creel S. Social dominance, aggression and faecal glucocorticoid levels in a wild population of wolves, Canis lupus. Anim. Behav. 67 (2004) 387-396
55. Sapolsky R.M. The endocrine stress-response and social status in the wild baboon. Horm. Behav. 16 (1982) 279-292
56. Sapolsky R.M. Endocrine and behavioral correlates of drought in wild olive baboons (Papio anubis). Am. J. Primatol. 11 (1986) 217-227
57. Sapolsky R.M. Endocrinology of the stress-response. In: Becker J.B., Breedlove S.M., Crews D., and McCarthy M.M. (Eds). Behavioral endocrinology. 2nd ed. (2002), MIT Press, Cambridge, MA 409-450
58. Sapolsky R.M. The influence of social hierarchy on primate health. Science 308 (2005) 648-652
59. Sauther M.L. Reproductive behavior of free-ranging Lemur catta at Beza Mahafaly Special Reserve, Madagascar. Am. J. Phys. Anthropol. 84 (1991) 463-477
60. Scordato E.S., and Drea C.M. Scents and sensibility: information content of olfactory signals in the ringtailed lemur (Lemur catta). Anim. Behav. 73 (2007) 301-314
61. Shideler S.E., Czekala N.M., Benirschke K., and Lasley B.L. Urinary estrogens during pregnancy of the ruffed lemur (Lemur variegatus). Biol. Reprod. 28 (1983) 963-969
62. Smith T.F., and French J.A. Psychosocial stress and urinary cortisol excretion in marmoset monkeys (Callithrix kuhli). Phys. Behav. 62 (1997) 225-232
63. Smith T.F., and French J.A. Social and reproductive conditions modulate urinary cortisol excretion in black tufted-ear marmosets (Callithrix kuhli). Am. J. Primatol. 42 (1997) 253-267
64. Sousa M.B.C., and Ziegler T.E. Diurnal variation on the excretion patterns of fecal steroids in common marmoset (Callithrix jacchus) females. Am. J. Primatol. 46 2 (1998) 105-117
65. Stavisky R.C., Adams M.R., Watson S.L., and Kaplan J.R. Dominance, cortisol, and behavior in small groups of female cynomolgus monkeys (Macaca fascicularis). Horm. Behav. 39 (2001) 232-238
66. Sussman R.W. Demography and social organization of free-ranging Lemur catta in the Beza Mahafaly Reserve, Madagascar. Am. J. Phys. Anthropol. 84 (1991) 43-58
67. Van Horn R.N. Primate breeding season: photoperiodic regulation in captive Lemur catta. Folia Primatol. 24 (1975) 203-220
68. Van Horn R.N., and Resko J.A. The reproductive cycle of the ringtailed lemur (Lemur catta): sex steroid levels and sexual receptivity under controlled photoperiods. Endocrinology 101 (1977) 1579-1586
69. Viau G., and Meaney M.J. Basal and stress hypothalamic-pituitary adrenal activity in cycling and ovariectomized-steroid treated rats. Endocrinology 129 (1991) 2503-2511
70. Vick L.G., and Pereira M.E. Episodic targeting aggression and the histories of Lemur social groups. Behav. Ecol. Sociobiol. 25 (1989) 3-12
71. Wasser S.K., Hunt K.E., Brown J.L., Cooper K., Crockett C.M., Bechert U., Millspaugh J.J., Larson S., and Monfort S.L. A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen. Comp. Endocrinol. 120 (2000) 260-275
72. Weingrill T., Gray D.A., Barrett L., and Henzi S.P. Fecal cortisol levels in free-ranging female chacma baboons: relationship to dominance, reproductive state and environmental factors. Horm. Behav. 45 (2004) 259-269
73. Whitten P.L., Brockman D.K., and Stavisky R.C. Recent advances in noninvasive techniques to monitor hormone-behavior interactions. Yrbk. Phys. Anth. 41 (1998) 1-23
74. Wingfield J.C., and Ramenofsky M. Corticosterone and facultative dispersal in response to unpredictable events. Ardea 85 (1997) 155-166
75. Wingfield J.C., Maney D.L., Breuner C.W., Jacobs J.D., Lynn S., Ramenofsky M., and Richardson R.D. Ecological bases of hormone-behavior interactions: the "emergency life history stage.". Amer. Zool. 38 (1998) 191-206
76. 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