Effects of maternal stress on egg characteristics in a cooperatively breeding fish

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 158, Issue 1, 2011, Pages 22-29

  Mileva, Viktoria R ^a   Gilmour, Kathleen M ^b   Balshine, Sigal ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Cichlidae; Cortisol; Egg size; Fecundity; Helper effects; Inter spawn interval; Neolamprologus pulcher; Stress

Indexed keywords

HYDROCORTISONE;

ANIMAL EXPERIMENT; ARTICLE; CHRONIC STRESS; CICHLID; CONTROLLED STUDY; COOPERATIVE BREEDING; DOMINANCE BEHAVIOR; EGG LAYING; EGG SIZE; FEMALE; FERTILITY; FITNESS; HORMONE DETERMINATION; MATERNAL STRESS; NEOLAMPROLOGUS PULCHER; NONHUMAN; REPRODUCTIVE SUCCESS; SPAWNING;

CICHLIDAE; NEOLAMPROLOGUS PULCHER;

EID: 78649633352     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2010.08.017     Document Type: Article

References (66)

1. Alsop D., Vijayan M.M. Development of the corticosteroid stress axis and receptor expression in zebrafish. Am. J. Physiol. 2008, 294:R711-R719.
2. Balshine S., Leach B., Neat F., Reid H., Taborsky M., Werner N. Correlates of group size in a cooperatively breeding cichlid fish (Neolamprologus pulcher). Behav. Ecol. Sociobiol. 2001, 50:134-140.
3. Balshine-Earn S., Neat F.C., Reid H., Taborsky M. Paying to stay or paying to breed? field evidence for direct benefits of helping behavior in a cooperatively breeding fish. Behav. Ecol. 1998, 9:432-438.
4. Barry T.P., Malison J.A., Held J.A., Parrish J.J. Ontogeny of the cortisol stress response in larval rainbow trout. Gen. Comp. Endocrinol. 1995, 97:57-65.
5. Barton B.A., Schreck C.B., Barton L.D. Effects of chronic cortisol administration and daily acute stress on growth, physiological conditions, and stress responses in juvenile rainbow trout. Dis. Aquat. Org. 1987, 2:173-185.
6. Bernier N.J. The corticotropin-releasing factor system as a mediator of the appetite-suppressing effects of stress in fish. Gen. Comp. Endocrinol. 2006, 146:45-55.
7. Bernier N.J., Peter R.E. The hypothalamic-pituitary-interrenal axis and the control of food intake in teleost fish. Comp. Biochem. Physiol. B 2001, 129:639-644.
8. Campbell P.M., Pottinger T.G., Sumpter J.P. Stress reduces the quality of gametes produced by rainbow trout. Biol. Reprod. 1992, 47:1140-1150.
9. Carragher J.F., Sumpter J.P., Pottinger T.G., Pickering A.D. The deleterious effects of cortisol implantation on reproductive function in two species of trout. Salmo trutta L. and Salmo gairdneri Richardson. Gen. Comp. Endocrinol. 1989, 76:310-321.
10. Charmandari E., Tsigos C., Chrousos G. Endocrinology of the stress response. Annu. Rev. Physiol. 2005, 67:259-284.
11. Chrousos G.P. Stressors, stress, and neuroendocrine integration of the adaptive response. The 1997 Hans Selye memorial lecture. Ann. NY Acad. Sci. 1998, 851:311-335.
12. Coleman R.M.,., Galvani A.P. Egg size determines offspring size in neotropical cichlid fishes (teleostei: Cichlidae). Copeia. 1998, 209-213.
13. Contreras-Sanchez W.M., Schreck C.B., Fitzpatrick M.S., Pereira C.B. Effects of stress on the reproductive performance of rainbow trout (Oncorhynchus Mykiss). Biol. Reprod. 1998, 58:439-447.
14. Creel S. Dominance, aggression, and glucocorticoid levels in social carnivores. J. Mammal. 2005, 86:255-264.
15. De Boer S.F., Koopmans S.J., Slangen J.L., Van der Gugten J. Plasma catecholamine, corticosterone and glucose responses to repeated stress in rats: Effect of interstressor interval length. Physiol. Behav. 1990, 47:1117-1124.
16. de Jesus G.E., Hirano T., Inui Y. Changes in cortisol and thyroid hormone concentrations during early development and metamorphosis in the Japanese flounder, Paralichthys Olivaceus. Gen. Comp. Endocrinol. 1991, 82:369-376.
17. Desjardins J.K., Stiver K.A., Fitzpatrick J.L., Balshine S. Differential responses to territory intrusions in a cooperatively breeding fish. Anim. Behav. 2008, 75:595-604.
18. Dobson H., Smith R.F. What is stress, and how does it affect reproduction?. Anim. Reprod. Sci. 2000, 60-61:743-752.
19. Eriksen M.S., Bakken M., Espmark A., Braastad B.O., Salte R. Prespawning stress in farmed atlantic salmon Salmo salar: Maternal cortisol exposure and hyperthermia during embryonic development affect offspring survival, growth and incidence of malformations. J. Fish Biol. 2006, 69:114-129.
20. Fitzpatrick J.L., Desjardins J.K., Stiver K.A., Montgomerie R., Balshine S. Male reproductive suppression in the cooperatively breeding fish Neolamprologus pulcher. Behav. Ecol. 2006, 17:25-33.
21. Fitzpatrick J.L., Desjardins J.K., Milligan N., Stiver K.A., Montgomerie R., Balshine S. Female-mediated causes and consequences of status change in a cooperatively breeding fish. Proc. R. Soc. Lond. B Biol. Sci. 2008, 275:929-936.
22. Gaglinano M., McCormick M.I. Hormonally mediated maternal effect shape offspring survival potential in stressful environments. Oecologia 2009, 160:657-665.
23. Gamperl A.K., Vijayan M.M., Boutilier R.G. Experimental control of stress hormone levels in fishes: Techniques and applications. Rev. Fish Biol. Fish. 1994, 4:215-255.
24. Gilmour K.M., DiBattista J.D., Thomas J.B. Physiological causes and consequences of social status in salmonid fish. Integr. Comp. Biol. 2005, 45:263-273.
25. Goymann W., Wingfield J.C. Allostatic load, social status and stress hormones: the costs of social status matter. Anim. Behav. 2004, 67:591-602.
26. Hayward L.S., Wingfield J.C. Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. Gen. Comp. Endocrinol. 2004, 135:365-371.
27. Heg D., Brouwer L., Bachar Z., Taborsky M. Large group size yields group stability in the cooperatively breeding cichlid Neolamprologus pulcher. Behaviour 2005, 142:1615-1641.
28. Jentoft S., Aastveit A.H., Torjesen P.A., Andersen Ø. Effects of stress on growth, cortisol and glucose levels in non-domesticated eurasian perch (Perca fluviatilis) and domesticated rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2005, 141:353-358.
29. Marsh E. Effects of egg size on offspring fitness and maternal fecundity in the orangethroat darter Etheostoma pectabile (Pisces: Percidae). Copeia 1986, 1986:18-30.
30. McCormick M.I. Behaviorally induced maternal stress in a fish influences progeny quality by a hormonal mechanism. Ecology 1998, 79:1873-1883.
31. McCormick M.I. Experimental test of the effect of maternal hormones on larval quality of a coral reef fish. Oecologia 1999, 118:412-422.
32. McCormick M.I. Mother matter: Crowding leads to stressed mothers and smaller offspring in marine fish. Ecology 2006, 87:1104-1109.
33. McCormick S.D.S., Shrimpton J.M., Carey J.B., O'Dea M.F., Sloan K.E., Moriyama S., Björnsson B.T. Repeated acute stress reduces growth rate of Atlantic salmon parr and alters plasma levels of growth hormone, insulin-like growth factor I and cortisol. Aquaculture 1998, 168:221-235.
34. Mileva V.R., Fitzpatrick J.L., Marsh-Rollo S., Gilmour K.M., Wood C.M., Balshine S. The stress response of the highly social African cichlid Neolamprologus pulcher. Physiol. Biochem. Zool. 2009, 82:720-729.
35. Montero D., Izquierdo M.S., Tort L., Robaina L., Vergara J.M. High stocking density produces crowding stress altering some physiological and biochemical parameters in gilthead seabream, Sparus aurata, juveniles. Fish Physiol. Biochem. 1999, 20:53-60.
36. Ostrand K.G., Cooke S.J., Wahl D.H. Effects of stress on largemouth bass reproduction. N. Am. J. Fish. Manage. 2004, 24:1038-1045.
37. Øverli Ø., Sørensen C., Kiessling A., Pottinger T.G., Gjøen H.M. Selection for improved stress tolerance in rainbow trout (Oncorhynchus mykiss) leads to reduced feed waste. Aquaculture 2006, 261:776-781.
38. Pankhurst N.W., Van Der Kraak G. Effects of stress on reproduction and growth of fish. Fish Stress and Health in Aquaculture 1997, 73-93. Cambridge University Press, Cambridge. G.K. Iwama, A.D. Pickering, J.P. Sumpter, C.B. Schreck (Eds.).
39. Pankhurst N.W., Van Der Kraak G. Evidence that acute stress inhibits ovarian steroidogenesis in rainbow trout in vivo, through the action of cortisol. Gen. Comp. Endocrinol. 2000, 117:225-237.
40. Perry S.F., Bernier N.J. The acute humoral adrenergic stress response in fish: Facts and fiction. Aquaculture 1999, 177:285-295.
41. Perry S.F., Reid S.G., Salama A. The effects of repeated physical stress on the b-adrenergic response of the rainbow trout red blood cell. J. Exp. Biol. 1996, 199:549-562.
42. Pickering A.D., Stewart A. Acclimation of the interrenal tissue of the brown trout, Salmo trutta L., to chronic crowding stress. J. Fish Biol. 1984, 24:731-740.
43. Pickering A.D., Pottinger T.G., Christie P. Recovery of the brown trout, Salmo trutta L., from acute handling stress: A time-course study. J. Fish Biol. 1982, 20:229-244.
44. Ramsay J.M., Feist G.W., Varga Z.M., Westerfield M., Kent M.L., Schreck C.B. Whole-body cortisol is an indicator of crowding stress in adult zebrafish, Danio rerio. Aquaculture 2006, 258:565-574.
45. Räsänen K., Laurila A., Merilä J. Maternal investment in egg size: Environment-and population-specific effects on offspring performance. Oecologia 2005, 142:546-553.
46. Reid S.G., Furimsky M., Perry S.F. The effects of repeated physical stress or fasting on catecholamine storage and release in the rainbow trout, Oncorhynchus mykiss. J. Fish Biol. 1994, 45:365-378.
47. Reid S.G., Bernier N.J., Perry S.F. The adrenergic stress response in fish: Control of catecholamine storage and release. Comp. Biochem. Physiol. C 1998, 120:1-27.
48. Reynard M., Savory C.J. Stress-induced oviposition delays in laying hens: Duration and consequences for eggshell quality. Br. Poult. Sci. 1999, 40:585-591.
49. Rondó P.H.C., Ferreira R.F., Nogueira F., Ribeiro M.C.N., Lobert H., Artes R. Maternal psychological stress and distress as predictors of low birth weight, prematurity and intrauterine growth retardation. Eur. J. Clin. Nutr. 2003, 57:266-272.
50. Salvante K.G., Williams T.D. Effects of corticosterone on the proportion of breeding females, reproductive output and yolk precursor levels. Gen. Comp. Endocrinol. 2003, 130:205-214.
51. Schoech S.J., Rensel M.A., Bridge E.S., Boughton R.K., Wilcoxen T.E. Environment, glucocorticoids, and the timing of reproduction. Gen. Comp. Endocrinol. 2009, 163:201-207.
52. Schreck C.B. Accumulation and long-term effects of stress in fish. The biology of animal stress. Basic principles and implications for animal welfare. CABI 2000, 147-158.
53. Schreck C.B. Stress and fish reproduction: The roles of allostatis and hormesis. Gen. Comp. Endocrinol. 2010, 165:549-556.
54. Schreck C.B., Contreras-Sanchez W., Fitzpatrick M. Effects of stress on fish reproduction, gamete quality, and progeny. Aquaculture 2001, 1997:3-24.
55. Sloman K.A. Exposure of ova to cortisol pre-fertilisation affects subsequent behaviour and physiology of brown trout 2010.
56. Stiver K.A., Dierkes P., Taborsky M., Balshine S. Dispersal patterns and status change in a co-operatively breeding cichlid Neolamprologus pulcher: Evidence from microsatellite analyses and behavioural observations. J. Fish Biol. 2004, 65:91-105.
57. Stiver K.A., Fitzpatrick J., Desjardins J.K., Balshine S. Sex differences in rates of territory joining and inheritance in a cooperatively breeding cichlid fish. Anim. Behav. 2006, 71:449-456.
58. Stiver K.A., Fitzpatrick J.L., Desjardins J.K., Neff B.D., Quinn J.S., Balshine S. The role of genetic relatedness among social mates in a cooperative breeder. Behav. Ecol. 2008, 19:816-823.
59. Stiver K.A., Fitzpatrick J.L., Desjardins J.K., Balshine S. Mixed parentage in Neolamprologus pulcher groups. J. Fish Biol. 2009, 74:1129-1135.
60. Stratholt M.L., Donaldson E.M., Liley N.R. Stress induced elevation of plasma cortisol in adult female coho salmon (Oncorhynchus kisutch), is reflected in egg cortisol content, but does not appear to affect early development. Aquaculture 1997, 158:141-153.
61. Taborsky M. Broodcare helpers in the cichlid fish Lamprologus brichardi: their costs and benefits. Anim. Behav. 1984, 32:1236-1252.
62. Taborsky M., Limberger D. Helpers in fish. Behav. Ecol. Sociobiol. 1981, 8:143-145.
63. Taborsky B., Skubic E., Bruintjes R. Mothers adjust egg size to helper number in a cooperatively breeding cichlid. Behav. Ecol. 2007, 18:652-657.
64. Wendelaar Bonga S.E. The stress response in fish. Physiol. Revs. 1997, 77:591-625.
65. Williams T.D. Intraspecific variation in egg size and egg composition in birds: Effects on offspring fitness. Biol. Rev. 1994, 68:35-59.
66. Young A.J., Carlson A.A., Monfort S.L., Russell A.F., Bennett N.C., Clutton-Brock T. Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proc. Natl Acad. Sci. USA 2006, 103:12005-12010.