Determinants of within- and among-clutch variation in yolk corticosterone in the European starling

Hormones and Behavior

Volumn 53, Issue 1, 2008, Pages 104-111

  Love, O P ^a   Wynne Edwards, K E ^b   Bond, L ^b   Williams, T D ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

Author keywords

Corticosterone; European starling (Sturnus vulgaris); Laying order; Maternal condition; Maternal effects; Nesting density; Yolk hormones

Indexed keywords

CORTICOSTERONE;

ARTICLE; BIRD; BREEDING; CLUTCH SIZE; CORTICOSTERONE BLOOD LEVEL; EGG YOLK; ENVIRONMENTAL STRESS; EUROPE; NESTING; NONHUMAN; PHENOTYPE; POPULATION; PRIORITY JOURNAL; PROGENY; SOCIAL ISOLATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIRTH ORDER; CLUTCH SIZE; CORTICOSTERONE; EGG PROTEINS; EGG YOLK; EMBRYO, NONMAMMALIAN; FEMALE; POPULATION DENSITY; REPRODUCTION; SOCIAL ENVIRONMENT; STARLINGS; STRESS, PSYCHOLOGICAL;

EID: 37449024073     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2007.09.007     Document Type: Article

References (88)

1. Badyaev A.V., Acevedo-Seaman D., Navara K.J., Hill G.E., and Mendonça M.T. Evolution of sex-biased maternal effects in birds: III. Adjustment of ovulation order can enable sex-specific allocation of hormones, carotenoids, and vitamins. J. Evol. Biol. 19 (2006) 1044-1057
2. Boonstra R., Hik D., Singleton G.R., and Tinnikov A. The impact of predator-induced stress on the snowshoe hare cycle. Ecol. Monogr. 79 (1998) 371-394
3. Breuner C.W., and Orchinik M. Beyond carrier proteins: plasma binding proteins as mediators of corticosteroid action in vertebrates. J. Endocrinol. 175 (2002) 99-112
4. Breuner C.W., and Hahn T.P. Integrating stress physiology, environmental change, and behavior in free-living sparrows. Horm. Behav. 43 (2003) 115-123
5. Cabe, P.R. 1993. European starling (Sturnus vulgaris). The Birds of North America. No 48 (eds. A. Poole and F. Gill), Philadelphia: The Academy of Natural Sciences; Washington, D.C.: The American Ornithologists' Union.
6. Chin E.H., Love O.P., Clark A.M., and Williams T.D. Brood size and environmental conditions sex-specifically affect nestling immune response in the European starling Sturnus vulgaris. J. Avian Biol. 36 (2005) 549-554
7. Christians J.K., Evanson M., and Aiken J.J. Seasonal decline in clutch size in European starlings: a novel randomization test to distinguish between the timing and quality hypotheses. J. Anim. Ecol. 70 (2001) 1080-1087
8. Clinchy M., Zanette L., Boonstra R., Wingfield J.C., and Smith J.N.M. Balancing food and predator pressure induces chronic stress in songbirds. Proc. R. Soc. Lond., B 271 (2004) 2473-2479
9. Cockrem J.F., and Silverin B. Sight of a predator can stimulate a corticosterone response in the great tit (Parus major). Gen. Comp. Endocrinol. 125 (2002) 248-255
10. Creel S., Creel N.M., and Monfort S.L. Social stress and dominance. Nature 379 (1996) 212
11. Creel S., Fox J.E., Hardy A., Sands J., Garrott R., and Peterson R. Snowmobile activity and glucocorticoid stress responses in wild wolves and elk. Conserv. Biol. 16 (2002) 809-814
12. Cree A., Tyrrell C.L., Preest M.R., Thorburn D., and Guillette Jr. L.J. Protecting embryos from stress: corticosterone effects and the corticosterone response to capture and confinement during pregnancy in a live-bearing lizard (Hoplodactylus maculatus). Gen. Comp. Endocrinol. 134 (2003) 316-329
13. Dallman M.F., Strack A.M., Akana S.F., Bradbury M.J., Hanson E.S., Scribner K.A., and Smith M. Feast and famine: critical role of glucocorticoids with insulin in daily energy flow. Front. Neuroendocrinol. 14 (1993) 303-347
14. de Fraipont M., Clobert J., John-Alder H., and Meylan S. Increased pre-natal maternal corticosterone promotes philopatry of offspring in common lizards Lacerta vivipara. J. Anim. Ecol. 69 (2000) 404-413
15. DeVries A.C., Glasper E.R., and Detillion C.E. Social modulation of stress responses. Physiol. Behav. 79 (2003) 399-407
16. Eising C.M., Eikenaar C., Schwabl H., and Groothuis T.G.G. Maternal androgens in Black-headed gulls (Larus ridibundus) eggs: consequences for chick development. Proc. R. Soc. Lond., B 268 (2001) 839-846
17. Eriksen M.S., Haug A., Torjesen P.A., and Bakken M. Prenatal exposure to corticosterone impairs embryonic development and increases fluctuating asymmetry in chickens (Gallus gallus domesticus). Br. Poult. Sci. 44 (2003) 690-697
18. Fowler G.S. Behavioral and hormonal responses of Magellanic penguins (Spheniscus magellanicus) to tourism and nest site visitation. Biol. Conserv. 90 (1999) 143-149
19. 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
20. Groothuis T.G.G., and Schwabl H. Determinants of within- and among-clutch variation in levels of maternal hormones in Black-Headed Gull eggs. Funct. Ecol. 16 (2002) 281-289
21. Groothuis T.G.G., Müller W., Engelhardt von N., Carere C., and Eising C.M. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev. 29 (2005) 329-352
22. Harvey S., Phillips J.G., Rees A., and Hall T.R. Stress and adrenal function. J. Exp. Zool. 232 (1984) 633-645
23. Hayward L.S., and Wingfield J.C. Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. Gen. Comp. Endocrinol. 135 (2004) 365-371
24. Hayward L.S., Satterlee D., and Wingfield J.C. Japanese quail selected for high plasma corticosterone response deposit high levels of corticosterone in their eggs. Physiol. Biochem. Zool. 78 (2005) 1026-1031
25. Hayward L.S., Richardson J.B., Grogan M.N., and Wingfield J.C. Sex differences in the organizational effects of corticosterone in the egg yolk of quail. Gen. Comp. Endocrinol. 146 (2006) 144-148
26. Holberton R.L., Parrish J.D., and Wingfield J.C. Modulation of the adrenocortical stress response in neotropical migrants during autumn migration. Auk 113 (1996) 558-564
27. Janczak A.M., Braastad B.O., and Bakken M. Behavioural effects of embryonic exposure to corticosterone in chickens. Appl. Anim. Behav. Sci. 96 (2006) 69-82
28. Ketterson E.D., and Nolan V. Adaptation, exaptation, and constraint: a hormonal perspective. Am. Nat. 154 (1999) S4-S25
29. Kitaysky A.S., Wingfield J.C., and Piatt J.F. Dynamics of food availability, body condition and physiological stress response in breeding black-legged kittiwakes. Funct. Ecol. 13 (1999) 577-584
30. Kitaysky A.S., Piatt J.F., Wingfield J.C., and Romano M. The adrenocortical stress-response of black-legged kittiwake chicks in relation to dietary restrictions. J. Comp. Physiol. 169 (1999) 303-310
31. Kitaysky A.S., Kitaiskaia E.V., Wingfield J.C., and Piatt J.F. Dietary restriction causes chronic elevation of corticosterone and enhances stress response in red-legged kittiwake chicks. J. Comp. Physiol., B 171 (2001) 701-709
32. Kitaysky A.S., Kitaiskaia E.V., Wingfield J.C., and Piatt J.F. A mechanistic link between chick diet and decline in seabirds?. Proc. R. Soc. Lond., B 273 (2006) 445-450
33. Krebs J.R., and Davies N.B. An Introduction to Behavioural Ecology (1987), Sinauer Associates, Maryland
34. Kullberg C., Houston D.C., and Metcalfe N.B. Impaired flight ability-a cost of reproduction in female blue tits. Behav. Ecol. 13 (2002) 575-579
35. Kullberg C., Jakobsson S., Kaby U., and Lind J. Impaired flight ability prior to egg-laying: a cost of being a capital breeder. Funct. Ecol. 19 (2005) 98-101
36. Lack D. The significance of clutch size. Ibis 89 (1947) 302-352
37. Lack D. The Natural Regulation of Animal Numbers (1954), Clarendon Press, Oxford
38. Lee S.J., Witter M.S., Cuthill I.C., and Goldsmith A.R. Reduction in escape performance as a cost of reproduction in gravid starlings, Sturnus vulgaris. Proc. R. Soc. Lond., B 263 (1996) 619-624
39. Love O.P., Shutt L.J., Silfies J.S., and Bird D.M. Repeated restraint and sampling results in reduced corticosterone levels in developing and adult captive American kestrels (Falco sparverius). Physiol. Biochem. Zool. 76 (2003) 753-761
40. Love O.P., Breuner C.W., Vézina F., and Williams T.D. Mediation of a corticosterone-induced reproductive conflict. Horm. Behav. 46 (2004) 59-65
41. Love O.P., Chin E.H., Wynne-Edwards K.E., and Williams T.D. Stress hormones: a link between maternal condition and sex-biased reproductive investment. Am. Nat. 166 (2005) 751-766
42. Lucas J.R., Freeberg T.M., Egbert J., and Schwabl H. Fecal corticosterone, body mass, and caching rates of Carolina chickadees (Poecile carolinensis) from disturbed and undisturbed sites. Horm. Behav. 49 (2006) 634-643
43. Macedo R.H.F., Cariello M.O., Pacheco A.M., and Schwabl H.G. Significance of social parameters on differential nutrient investment in guira cuckoo, Guira guira, eggs. Anim. Behav. 68 (2004) 685-694
44. Marra P.P., and Holberton R.L. Corticosterone levels as indicators of habitat quality: effects of habitat segregation in a migratory bird during the non-breeding season. Oecologia 116 (1998) 284-292
45. Mazuc J., Bonneaud C., Chastel O., and Sorci G. Social environment affects female and egg testosterone levels in the house sparrow (Passer domesticus). Ecol. Lett. 6 (2003) 1084-1090
46. McCormick M.I. Behaviorally induced maternal stress in a fish influences progeny quality by a hormonal mechanism. Ecology 79 (1998) 1873-1883
47. McCormick M.I. Experimental test of the effect of maternal hormones on larval quality of a coral reef fish. Oecologia 118 (1999) 412-422
48. Meylan S., and Clobert J. Is corticosterone-mediated phenotype development adaptive? Maternal corticosterone treatment enhances survival in male lizards. Horm. Behav. 48 (2005) 44-52
49. Moore I.T., and Jessop T.S. Stress, reproduction, and adrenocortical modulation in amphibians and reptiles. Horm. Behav. 43 (2003) 39-47
50. Müllner A., Linsenmair K.E., and Wikelski M. Exposure to ecotourism reduces survival and affects stress response in Hoatzin chicks (Opisthocomus hoazin). Biol. Conserv. 118 (2004) 549-558
51. Nager R.G., Monaghan P., Houston D.C., and Genovart M. Parental condition, brood sex ratio and differential young survival: an experimental study in gulls (Larus fuscus). Behav. Ecol. Sociobiol. 48 (2000) 452-457
52. Navara K.J., Siefferman L.M., Hill G.E., and Mendonça M.T. Yolk androgens vary inversely to maternal androgens in Eastern bluebirds: an experimental study. Funct. Ecol. 20 (2006) 449-456
53. Nephew B.C., and Romero L.M. Behavioral, physiological, and endocrine responses of starlings to acute increases in density. Horm. Behav. 44 (2003) 222-232
54. Nilsson J.-A., and Råberg L. The resting metabolic cost of egg laying and nestling feeding in great tits. Oecologia 128 (2001) 187-192
55. Pereira R.J.G., Duarte J.M.B., and Negrão J.A. Effects of environmental conditions, human activity, reproduction, antler cycle and grouping on fecal glucocorticoids of free-ranging Pampas deer stags (Ozotoceros bezoarticus bezoarticus). Horm. Behav. 49 (2006) 114-122
56. Pike T.W., and Petrie M. Potential mechanisms of avian sex manipulation. Biol. Rev. 78 (2003) 553-574
57. Pike T.W., and Petrie M. Maternal body condition and plasma hormones affect offspring sex ratio in peafowl. Anim. Behav. 70 (2005) 745-751
58. Pike T.W., and Petrie M. Offspring sex ratio is related to paternal train elaboration and yolk corticosterone in peafowl. Biol. Lett. 1 (2005) 204-207
59. Pike T.W., and Petrie M. Experimental evidence that corticosterone affects offspring sex ratios in quail. Proc. R. Soc. Lond., B 273 (2006) 1093-1098
60. Pilz K.M., and Smith H.G. Egg yolk androgen levels increase with breeding density in the European starling, Sturnus vulgaris. Funct. Ecol. 18 (2004) 58-66
61. Pilz K.M., Smith H.G., Sandell M.I., and Schwabl H. Interfemale variation in egg yolk androgen allocation in the European starling: do high-quality females invest more?. Anim. Behav. 65 (2003) 841-850
62. Pyle P. Identification Guide to North American Birds-Part 1 (1997), Slate Creek Press, Bolinas, CA USA 732 pp.
63. Remage-Healey L., and Romero L.M. Corticosterone and insulin interact to regulate glucose and triglyceride levels during stress in a bird. Am. J. Physiol., Regul. Integr. Comp. Physiol. 281 (2001) R994-R1003
64. Romero L.M. Physiological stress in ecology: lessons from biomedical research. Trends Ecol. Evol. 19 (2004) 249-255
65. Romero L.M., and Remage-Healey L. Daily and seasonal variation in response to stress in captive starlings (Sturnus vulgaris): corticosterone. Gen. Comp. Endocrinol. 119 (2000) 52-59
66. Romero L.M., and Romero R.C. Corticosterone responses in wild birds: the importance of rapid initial sampling. Condor 104 (2002) 129-135
67. Romero L.M., and Wikelski M. Exposure to tourism reduces stress-induced corticosterone levels in Galápagos marine iguanas. Biol. Conserv. 108 (2002) 371-374
68. Romero L.M., Reed J.M., and Wingfield J.C. Effects of weather on corticosterone responses in wild, free-living passerine birds. Gen. Comp. Endocrinol. 118 (2000) 113-122
69. Rubolini D., Romano M., Boncoraglio G., Ferrari R.P., Martinelli R., Galeoti P., Fasola M., and Saino N. Effects of elevated egg corticosterone levels on behavior, growth, and immunity of yellow-legged gull (Larus michahellisi) chicks. Horm. Behav. 47 (2005) 592-605
70. Saino N., Romano M., Ferrari R.P., Martinelli R., and Møller A.P. Stressed mothers lay eggs with high corticosterone levels which produce low-quality offspring. J. Exp. Zool. 303 (2005) 998-1006
71. Sapolsky R.M., Romero L.M., and Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21 (2000) 55-89
72. Schwabl H. Yolk is a source of maternal testosterone for developing birds. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 11446-11450
73. Schwabl H. Maternal steroid hormones in the egg. In: Harvey S., and Etches R.J. (Eds). Perspectives in Avian Endocrinology (1997), Journal of Endocrinology Limited, Bristol 3-13
74. Seckl J.R. Glucocorticoid programming of the fetus; adult phenotypes and molecular mechanisms. Mol. Cell. Endocrinol. 185 (2001) 61-71
75. Sinervo B., and DeNardo D.F. Costs of reproduction in the wild: path analysis of natural selection and experimental tests of causation. Evolution 50 (1996) 1299-1313
76. Smith H.G. Selection for synchronous breeding in the European starling. Oikos 105 (2004) 301-311
77. Suorsa P., Helle H., Huhta E., Jäntti A., Nikula A., and Hakkarainen H. Forest fragmentation is associated with primary brood sex ratio in the treecreeper (Certhia familiaris). Proc. R. Soc. Lond., B 270 (2003) 2215-2222
78. Uller T., and Olsson M. Direct exposure to corticosterone during embryonic development influences behaviour in an ovoviviparous lizard. Ethology 112 (2006) 390-397
79. Verboven N., Evans N.P., D'Alba L., Nager R.G., Blount J.D., Surai P.F., and Monaghan P. Intra-specific interactions influence egg composition in the lesser black-backed gull (Larus fuscus). Behav. Ecol. Sociobiol. 57 (2005) 357-365
80. Vézina F., and Williams T.D. Metabolic costs of egg production in the European starling (Sturnus vulgaris). Physiol. Biochem. Zool. 75 (2002) 377-385
81. Vézina F., Salvante K.G., and Williams T.D. The metabolic cost of avian egg formation: possible impact of yolk precursor production?. J. Exp. Biol. 206 (2003) 4443-4451
82. Walker B.G., Boersma P.D., and Wingfield J.C. Physiological and behavioral differences in Magellanic penguin chicks in undisturbed and tourist-visited locations of a colony. Conserv. Biol. 19 (2005) 1571-1577
83. Walker B.G., Boersma P.D., and Wingfield J.C. Habituation of adult Magellanic penguins to human visitation as expressed through behavior and corticosterone secretion. Conserv. Biol. 20 (2006) 146-154
84. Williams T.D. Mechanisms underlying the costs of reproduction. Bioscience 55 (2005) 39-48
85. Wingfield J.C. The concept of allostasis: coping with a capricious environment. J. Mammal. 86 (2005) 248-254
86. Wingfield J.C., Bruener C., and Jacobs J. Corticosterone and behavioral responses to unpredictable events. In: Harvey S., and Etches R.J. (Eds). Perspectives in Avian Endocrinology (1997), Journal of Endocrinology Ltd., Bristol, UK 267-278
87. 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". Am. Zool. 38 (1998) 191-206
88. Wittingham L.A., and Schwabl H. Maternal testosterone in tree swallow eggs varies with female aggression. Anim. Behav. 63 (2002) 63-67