The stress response of the highly social African cichlid Neolamprologus pulcher

Physiological and Biochemical Zoology

Volumn 82, Issue 6, 2009, Pages 720-729

  Mileva, Viktoria R ^a   Fitzpatrick, John L ^a   Marsh Rollo, Susan ^a   Gilmour, Kathleen M ^b   Wood, Chris M ^a   Balshine, Sigal ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROCORTISONE;

AGGRESSION; BEHAVIORAL RESPONSE; CICHLID; COOPERATIVE BREEDING; FITNESS; STEROL;

AIR AND AIR RELATED PHENOMENA; ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; BLOOD; CICHLID; COMPARATIVE STUDY; FEMALE; MALE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SEXUAL BEHAVIOR; SOCIAL DOMINANCE;

ANALYSIS OF VARIANCE; ANIMALS; CICHLIDS; CONFINED SPACES; FEMALE; HYDROCORTISONE; MALE; SEXUAL BEHAVIOR, ANIMAL; SOCIAL DOMINANCE; STRESS, PHYSIOLOGICAL;

AFRICAN CICHLIDS; CICHLIDAE; NEOLAMPROLOGUS PULCHER;

EID: 73449132584     PISSN: 15222152     EISSN: None     Source Type: Journal    
DOI: 10.1086/605937     Document Type: Article

References (63)

1. Abbott D. H., E. B. Keverne, F. B. Bercovitch, C. A. Shively, S. P. Mendoza, W. Saltzman, C. T. Snowdon, T. E. Ziegler, M. Banjevic, and T. Garland. 2003. Are subordinates always stressed? a comparative analysis of rank differences in cortisol levels among primates. Horm Behav 43:67-82.
2. Alderman S. and N. J. Bernier. 2009. Ontogeny of the corticotropin- releasing factor system in zebrafish. Gen Comp Endocrinol 164:61-69.
3. Aubin-Horth N., J. K. Desjardins, Y. M. Martei, S. Balshine, and H. A. Hofmann. 2007. Masculinized dominant females in a cooperatively breeding species. Mol Ecol 16:1349-1358.
4. Balshine S. and P. M. Buston. 2008. Cooperative behaviour in fishes. Pp. 437-484 in C. Magnhagen, V. Braithwaite, E. Forsgren, and B. G. Kapoor, eds. Fish Behaviour. Science, Enfield, NH.
5. Balshine S., B. Leach, F. Neat, H. Reid, M. Taborsky, and N. Werner. 2001. Correlates of group size in a cooperatively breeding cichlid fish (Neolamprologus pulcher). Behav Ecol Sociobiol 50:134-140.
6. Balshine-Earn S., F. C. Neat, H. Reid, and M. Taborsky. 1998. Paying to stay or paying to breed? field evidence for direct benefits of helping behavior in a cooperatively breeding fish. Behav Ecol 9:432-438.
7. Barton B. A. 2002. Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517-525.
8. Barton B. A., C. B. Schreck, and L. A. Sigismondi. 1986. Multiple acute disturbances evoke cumulative physiological stress responses in juvenile chinook salmon. Trans Am Fish Soc 115:245-251.
9. Bender N., D. Heg, I. M. Hamilton, Z. Bachar, M. Taborsky, and R. F. Oliveira. 2006. The relationship between social status, behavior, growth and steroids in male helpers and breeders of a cooperatively breeding cichlid. Horm Behav 50:173-182.
10. Bergmüller R., D. Heg, K. Peer, and M. Taborsky. 2005. Extended safe havens and between-group dispersal of helpers in a cooperatively breeding cichlid. Behavior 142:1643-1667.
11. Bilbo S. D. and R. J. Nelson. 2003. Sex differences in photoperiodic and stress-induced enhancement of immune function in Siberian hamsters. Brain Behav Immun 17:462-472.
12. Brouwer L., D. Heg, and M. Taborsky. 2005. Experimental evidence for helper effects in a cooperatively breeding cichlid. Behav Ecol 16:667-673.
13. Buchner A. S., K. A. Sloman, and S. Balshine. 2004. The physiological effects of social status in the cooperatively breeding cichlid Neolamprologus pulcher. J Fish Biol 65:1080-1095.
14. Carlson A. A., A. J. Young, A. F. Russell, N. C. Bennett, A. S. McNeilly, and T. Clutton-Brock. 2004. Hormonal correlates of dominance in meerkats (Suricata suricatta). Horm Behav 46:141-150.
15. Chrousos G. P. 1998. Stressors, stress, and neuroendocrine integration of the adaptive response: the 1997 Hans Selye memorial lecture. Ann NY Acad Sci 851:311-335.
16. Creel S. 2001. Social dominance and stress hormones. Trends Ecol Evol 16:491-497.
17. -. 2005. Dominance, aggression, and glucocorticoid levels in social carnivores. J Mammal 86:255-264.
18. Creel S., N. M. Creel, and S. L. Monfort. 1996. Social stress and dominance. Nature 379:212.
19. Critchlow V., R. A. Liebelt, M. Bar-Sela, W. Mountcastle, and H. S. Lipscomb. 1963. Sex difference in resting pituitaryadrenal function in the rat. Am J Physiol 205:807-815.
20. Davis K. B., M. A. Suttle, and N. C. Parker. 1984. Biotic and abiotic influences on corticosteroid hormone rhythms in channel catfish. Trans Am Fish Soc 113:414-421.
21. Desjardins J. K., K. A. Stiver, J. L. Fitzpatrick, and S. Balshine. 2008. Differential responses to territory intrusions in cooperatively breeding fish. Anim Behav 75:595-604.
22. Dierkes P., D. Heg, M. Taborsky, E. Skubic, and R. Achmann. 2005. Genetic relatedness in groups is sex-specific and declines with age of helpers in a cooperatively breeding cichlid. Ecol Lett 8:968-975.
23. Dierkes P., M. Taborsky, and U. Kohler. 1999. Reproductive parasitism of broodcare helpers in a cooperatively breeding fish. Behav Ecol 10:510-515.
24. Fitzpatrick J. L., J. K. Desjardins, N. Milligan, K. A. Stiver, R. Montgomerie, and S. Balshine. 2008. Female-mediated causes and consequences of status change in a cooperatively breeding fish. Proc R Soc B 275:929-936.
25. Fitzpatrick J. L., J. K. Desjardins, K. A. Stiver, R. Montgomerie, and S. Balshine. 2006. Male reproductive suppression in the cooperatively breeding fish Neolamprologus pulcher. Behav Ecol 17:25-33.
26. Fox H. E., S. A. White, M. F. Kao, and R. D. Fernald. 1997. Stress and dominance in a social fish. J Neurosci 17:6463-6469.
27. Gamperl A. K., M. M. Vijayan, and R. G. Boutilier. 1994. Experimental control of stress hormone levels in fishes: techniques and applications. Rev Fish Biol Fish 4:215-255.
28. Goymann W. and J. C. Wingfield. 2004. Allostatic load, social status and stress hormones: the costs of social status matter. Anim Behav 67:591-602.
29. Hartman F. A., F. F. Shelden, and E. L. Green. 1943. Weights of interrenal glands of elasmobranchs. Anat Rec 87:371-378.
30. Heg D., R. Bergmüller, D. Bonfils, O. Otti, Z. Bachar, R. Burri, G. Heckel, and M. Taborsky. 2006. Cichlids do not adjust reproductive skew to the availability of independent breeding options. Behav Ecol 17:419-429.
31. Heg D., L. Brouwer, Z. Bachar, and M. Taborsky. 2005. Large group size yields group stability in the cooperatively breeding cichlid Neolamprologus pulcher. Behavior 142:1615-1641.
32. Hontela A. 1998. Interrenal dysfunction in fish from contaminated sites: in vivo and in vitro assessment. Environ Toxicol Chem 17:44-48.
33. Hontela A., P. Dumont, D. Duclos, and R. Fortin. 1995. Endocrine and metabolic dysfunction in yellow perch, Perca flavescens, exposed to organic contaminants and heavy metals in the St. Lawrence River. Environ Toxicol Chem 14:725-731.
34. Jarvis J. U. 1981. Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212:571-573.
35. Komdeur J. 1994. Experimental evidence for helping and hindering by previous offspring in the cooperative-breeding Seychelles warbler Acrocephalus sechellensis. Behav Ecol Sociobiol 34:175-186.
36. Kudielka B. M. and C. Kirschbaum. 2005. Sex differences in HPA axis responses to stress: a review. Biol Psychol 69:113-132.
37. Lamba V. J., S. V. Goswami, and B. I. Sundararaj. 1983. Circannual and circadian variations in plasma levels of steroids (cortisol, estradiol-17 beta, estrone, and testosterone) correlated with the annual gonadal cycle in the catfish, Heteropneustes fossilis (Bloch). Gen Comp Endocrinol 50:205-225.
38. Pickering A. D. and P. Christie. 1981. Changes in the concentrations of plasma cortisol and thyroxine during sexual maturation of the hatchery-reared brown trout, Salmo trutta L. Gen Comp Endocrinol 44:487-496.
39. Pickering A. D. and T. G. Pottinger. 1989. Stress responses and disease resistance in salmonid fish: effects of chronic elevation of plasma cortisol. Fish Physiol Biochem 7:253-258.
40. Pottinger T. G., T. R. Carrick, S. E. Hughes, and P. H. M. Balm. 1996. Testosterone, 11-ketotestosterone, and estradiol-17β modify baseline and stress-induced interrenal and corticotropic activity in trout. Gen Comp Endocrinol 104:284-295.
41. Reeder D. M., T. H. Kunz, and E. P. Widmaier. 2004. Baseline and stress-induced glucocorticoids during reproduction in the variable flying fox, Pteropus hypomelanus (Chiroptera: Pteropodidae). J Exp Zool 301:682-690.
42. Rice W. R. 1989. Analyzing tables of statistical tests. Evolution 43:223-225.
43. Rotllant J., R. J. Arends, J. M. Mancera, G. Flik, S. E. Wendelaar Bonga, and L. Tort. 2000. Inhibition of HPI axis response to stress in gilthead sea bream (Sparus aurata) with physiological plasma levels of cortisol. Fish Physiol Biochem 23:13-22.
44. Rubenstein D. R. 2007. Stress hormones and sociality: integrating social and environmental stressors. Proc R Soc B 274:967-975.
45. Rubenstein D. R. and S.-F. Shen. 2009. Reproductive conflict and the costs of social status in cooperatively breeding vertebrates. Am Nat 173:650-661.
46. Schoech S. J., R. Bowman, E. S. Bridge, and R. K. Boughton. 2007. Baseline and acute levels of corticosterone in Florida scrubjays (Aphelocoma coerulescens): effects of food supplementation, suburban habitat, and year. Gen Comp Endocrinol 154:150-160.
47. Schoech S. J., R. L. Mumme, and M. C. Moore. 1991. Reproductive endocrinology and mechanisms of breeding inhibition in cooperatively breeding Florida scrub jays (Aphelocoma c. coerulescens). Condor 93:354-364.
48. Schoech S. J., R. L. Mumme, and J. C. Wingfield. 1997. Corticosterone, reproductive status, and body mass in a cooperative breeder, the Florida scrub-jay (Aphelocoma coerulescens). Physiol Biol 70:68-73.
49. Schradin C. 2008. Seasonal changes in testosterone and corticosterone levels in four social classes of a desert dwelling sociable rodent. Horm Behav 53:573-579.
50. Sloman K. A., N. B. Metcalfe, A. C. Taylor, and K. M. Gilmour. 2001. Plasma cortisol concentrations before and after social stress in rainbow trout and brown trout. Physiol Biochem Zool 74:383-389.
51. Sokal R. R. and F. J. Rohlf. 1995. Biometry. W. H. Freeman, San Francisco.
52. Sopinka N. M., J. L. Fitzpatrick, J. K. Desjardins, K. A. Stiver, S. E. Marsh-Rollo, and S. Balshine. 2009. Liver size as an indicator of social status in an African cichlid fish. J Fish Biol 75:1-16.
53. Stiver K. A., J. K. Desjardins, J. L. Fitzpatrick, B. Neff, J. S. Quinn, and S. Balshine. 2007. Evidence for size and sex-specific dispersal in a cooperatively breeding cichlid fish. Mol Ecol 16:2974-2984.
54. Stiver K. A., P. Dierkes, M. Taborsky, and S. Balshine. 2004. Dispersal patterns and status change in a co-operatively breeding cichlid Neolamprologus pulcher: evidence from microsatellite analyses and behavioral observations. J Fish Biol 65:91-105.
55. Stiver K. A., J. Fitzpatrick, J. K. Desjardins, and S. Balshine. 2006. Sex differences in rates of territory joining and inheritance in a cooperatively breeding cichlid fish. Anim Behav 71:449-456.
56. -. 2009. Mixed parentage in Neolamprologus pulcher groups. J Fish Biol 74:1129-1135.
57. Stiver K. A., J. L. Fitzpatrick, J. K. Desjardins, B. D. Neff, J. S. Quinn, and S. Balshine. 2008. The role of genetic relatedness among social mates in a cooperative breeder. Behav Ecol 19:816-823.
58. Taborsky M. 1984. Broodcare helpers in the cichlid fish Lamprologus brichardi: their costs and benefits. Anim Behav 32:1236-1252.
59. Taborsky M. and D. Limberger 1981. Helpers in fish. Behav Ecol Sociobiol 8:143-145.
60. Taves M. D., J. K. Desjardins, S. Mishra, and S. Balshine. 2009. Androgens and dominance: sex-specific patterns in a highly social fish (Neolamprologus pulcher). Gen Comp Endocrinol 161:202-207.
61. Touma C. and R. Palme. 2005. Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Ann NY Acad Sci 1046:54-74.
62. Virgin C. E., Jr., and R. M. Sapolsky. 1997. Styles of male social behavior and their endocrine correlates among low-ranking baboons. Am J Primatol 42:25-39.
63. Wendelaar Bonga S. E. 1997. The stress response in fish. Physiol Rev 77:591-625.