Experimentally reduced corticosterone release promotes early breeding in blacklegged kittiwakes

Journal of Experimental Biology

Volumn 214, Issue 12, 2011, Pages 2005-2013

  Goutte, Aurélie ^a   Clément Chastel, Céline ^a   Moe, Børge ^b   Bech, Claus ^c   Gabrielsen, Geir Wing ^d   Chastel, Olivier ^a  

^a CNRS   (France)

^b NORWEGIAN INSTITUTE FOR NATURE RESEARCH   (Norway)

^c NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^d NORWEGIAN POLAR INSTITUTE   (Norway)

Author keywords

Arctic seabird; Fitness; Rissa tridactyla; Stress hormones; Timing of breeding

Indexed keywords

CORTICOSTERONE;

ANIMAL; ARTICLE; CHARADRIIFORMES; CLUTCH SIZE; FEMALE; MALE; NORWAY; PHYSIOLOGY; REPRODUCTION; SECRETION; SEX RATIO; TIME;

ANIMALS; CHARADRIIFORMES; CLUTCH SIZE; CORTICOSTERONE; FEMALE; MALE; NORWAY; REPRODUCTION; SEX DISTRIBUTION; TIME FACTORS;

AVES; LARUS; RISSA TRIDACTYLA;

EID: 79957664219     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.051979     Document Type: Article

References (69)

1. Akana, S. F., Scribner, K. A., Bradbury, M. J., Strack, A. M., Walker, C. D. and Dallman, M. F. (1992). Feedback sensitivity of the rat hypothalamo-pituitary-adrenal axis and its capacity to adjust to exogenous corticosterone. Endocrinology 131, 585- 594.
2. Angelier, F., Shaffer, S. A., Weimerskirch, H., Trouvé, C. and Chastel, O. (2007). Corticosterone and foraging behavior in a pelagic seabird. Physiol. Biochem. Zool. 80, 283-292. (Pubitemid 46581368)
3. Angelier, F., Clément-Chastel, C., Welcker, J., Gabrielsen, G. W. and Chastel, O. (2009). How does corticosterone affect parental behaviour and reproductive success? A study of prolactin in black-legged kittiwakes. Funct. Ecol. 23, 784-793.
4. Ball, G. F. (1993). The neural integration of environmental information by seasonally breeding birds. Am. Zool. 33, 185-199.
5. Ball, G. F. and Ketterson, E. D. (2008). Sex differences in the response to environmental cues regulating seasonal reproduction in birds. Philos. Trans. R. Soc. Lond. B 363, 231-246. (Pubitemid 350249338)
6. Blas, J. and Hiraldo, F. (2010). Proximate and ultimate factors explaining floating behavior in long-lived birds. Horm. Behav. 57, 169-175.
7. Bokony, V., Lendvai, A. Z., Liker, A., Angelier, F., Wingfield, J. C. and Chastel, O. (2009). Stress response and the value of reproduction: are birds prudent parents? Am. Nat. 173, 589-598.
8. Bonier, F., Martin, P. R., Moore, I. T. and Wingfield, J. C. (2009). Do baseline glucocorticoids predict fitness? Trends Ecol. Evol. 24, 634-642.
9. Breuner, C. W. and Orchinik, M. (2002). Plasma binding proteins as mediators of corticosteroid action in vertebrates. J. Endocrinol. 175, 99-112. (Pubitemid 35276590)
10. Breuner, C. W., Wada, H., Shyu, J. and Love, O. P. (2003). Corticosteroid binding globulin capacity responds to chronic hormone treatment but not acute stressors. Integr. Comp. Biol. 46, 1013.
11. Breuner, C. W., Patterson, S. H. and Hahn, T. P. (2008). In search of relationships between the acute adrenocortical response and fitness. Gen. Comp. Endocr. 157, 288- 295. (Pubitemid 351899058)
12. Brinkhof, M. W. G., Cave, A. J., Daan, S. and Perdeck, A. C. (2002). Timing of current reproduction directly affects future reproductive output in European coots. Evolution 56, 400-411. (Pubitemid 34253409)
13. Busch, D. S., Sperry, T. S., Wingfield, J. C. and Boyd, E. H. (2008). Effects of repeated, short-term, corticosterone administration on the hypothalamo-pituitaryadrenal axis of the white-crowned sparrow (Zonotrichia leucophrys gambelii). Gen. Comp. Endocr. 158, 211-223.
14. Byrd, G. V., Sydeman, W. J., Renner, H. M. and Minobe, S. (2008). Responses of piscivorous seabirds at the Pribilof Islands to ocean climate, Deep-Sea Res. II 55, 1856-1867.
15. Chastel, O., Lacroix, A., Weimerskirch, H. and Gabrielsen, G. W. (2005). Modulation of prolactin but not corticosterone responses to stress in relation to parental effort in a long-lived bird. Horm. Behav. 47, 459-466. (Pubitemid 40385095)
16. Dawson, A. (2008). Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability. Philos. Trans. R. Soc. Lond. B 363, 1621-1633. (Pubitemid 351441049)
17. Dawson, A., King, V. M., Bentley, G. E. and Ball, G. F. (2001). Photoperiodic control of seasonality in birds. J. Biol. Rhythm. 16, 366-381.
18. DeForest, L. N. and Gaston, A. J. (1996). The effect of age on timing of breeding and reproductive success in the thick-billed Murre. Ecology 77, 1501-1511.
19. Drent, R. H. and Daan, S. (1980). The prudent parent - energetic adjustments in avian breeding. Ardea 68, 225-252.
20. Durant, J. M., Hjermann, D. O., Anker-Nilssen, T., Beaugrand, G., Mysterud, A., Pettorelli, N. and Stenseth, N. C. (2005). Timing and abundance as key mechanisms affecting trophic interactions in variable environments. Ecol. Lett. 8, 952-958. (Pubitemid 41258116)
21. Durant, J. M., Hjermann, D. O., Ottersen, G. and Stenseth, N. C. (2007). Climate and the match or mismatch between predator requirements and resource availability. Clim. Res. 33, 271-283. (Pubitemid 351728296)
22. Feldman, D., Mondon, C. E., Horner, J. A. and Weiser, J. N. (1979). Glucocorticoid and estrogen regulation of corticosteroid-binding globulin production by rat liver. Am. J. Physiol. Endocrinol. Metab. 237, E493-E499. (Pubitemid 10174518)
23. Frederiksen, M., Harris, M. P., Daunt, F., Rothery, P. and Wanless, S. (2004). Scaledependent climate signals drive breeding phenology of three seabird species. Glob. Change Biol. 10, 1214-1221. (Pubitemid 38964513)
24. Golet, G. H., Schmutz, J. A., Irons, D. B. and Estes, J. A. (2004). Determinants of reproductive costs in the long-lived black-legged kittiwake: a multiyear experiment. Ecol. Monog. 74, 353-372. (Pubitemid 39182899)
25. Goutte, A., Antoine, E., Weimerskirch, H. and Chastel, O. (2010a). Age and the timing of breeding in a long-lived bird: a role for stress hormones? Funct. Ecol. 24, 1007-1016.
26. Goutte, A., Angelier, F., Welcker, J., Moe, B., Clément-Chastel, C., Gabrielsen, G. W., Bech, C. and Chastel, O. (2010b). Long-term survival effect of corticosterone manipulation in black-legged kittiwakes. Gen. Comp. Endocr. 167, 246-251.
27. Goutte, A., Angelier, F., Clément-Chastel, C., Trouvé, C., Moe, B., Bech, C., Gabrielsen, G. W. and Chastel, O. (2010c). Stress and the timing of breeding: glucocorticoid- luteinizing hormones relationships in an arctic seabird. Gen. Comp. Endocr. 169, 108-116.
28. Hipfner, J. M., McFarlane-Tranquilla, L. A. and Addison, B. (2008). Do marine birds use environmental cues to optimize egg production? An experimental test based on relaying propensity. J. Avian Biol. 39, 611-618.
29. Kempenaers, B., Lanctot, R. B., Gill, V. A., Hatch, S. A. and Valcu, M. (2007). Do females trade copulations for food? An experimental study in Black-legged Kittiwakes. Behav. Ecol. 18, 345-353. (Pubitemid 46363257)
30. Kitaysky, A. S., Wingfield, J. C. and Piatt, J. F. (1999). Dynamics of food availability, body condition and physiological stress response in breeding Black-legged Kittiwakes. Funct. Ecol. 13, 577-584.
31. Kitaysky, A. S., Wingfield, J. C. and Piatt, J. F. (2001). Corticosterone facilitates begging and affects resource allocation in the Black-legged kittiwake. Behav. Ecol. 12, 619-625. (Pubitemid 32882193)
32. Kitaysky, A. S., Piatt, J. F. and Wingfield, J. C. (2007). Stress hormones link food availability and population processes in seabirds. Mar. Ecol. Prog. Ser. 352, 245-258. (Pubitemid 351211791)
33. Kitaysky, A. S., Piatt, J. F., Hatch, S. A., Kitaiskaia, E. V., Benowitz-Fredericks, Z. M., Shultz, M. T. and Wingfield, J. C. (2010). Food availability and population processes: severity of nutritional stress during reproduction predicts survival of longlived seabirds. Funct. Ecol. 24, 625-637.
34. Lack, D. (1968). Ecological Adaptations for Breeding in Birds. London: Methuen.
35. Lanctot, R. B., Hatch, S. A., Gill, V. A. and Eens, M. (2003). Are corticosterone levels a good indicator of food availability and reproductive performance in a kittiwake colony? Horm. Behav. 43, 489-502. (Pubitemid 36683027)
36. Landys, M. M., Ramenofsky, M. and Wingfield, J. C. (2006). Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen. Comp. Endocr. 148, 132-149. (Pubitemid 44142500)
37. Lendvai, A. Z., Giraudeau, M. and Chastel, O. (2007). Reproduction and modulation of the stress response: an experimental test in the house sparrow. Proc. Roy. Soc. B. Biol. 274, 391-397. (Pubitemid 47055463)
38. Lormée, H., Jouventin, P., Trouve, C. and Chastel, O. (2003). Sex-specific patterns in baseline corticosterone and body condition changes in breeding Red-footed Boobies Sula sula. Ibis 145, 212-219. (Pubitemid 36429721)
39. Love, O. P., Breuner, C. W., Vézina, F. and Williams, T. D. (2004). Mediation of a corticosterone-induced reproductive conflict. Horm. Behav. 46, 59-65. (Pubitemid 38822938)
40. Lyon, B. E., Chaine, A. S. and Winkler, D. W. (2008). Ecology: a matter of timing. Science 321, 1051-1052.
41. McNamara, J. M. and Houston, A. I. (2008). Optimal annual routines: behaviour in the context of physiology and ecology. Philos. T. R. Soc. B. 363, 301-319. (Pubitemid 350253041)
42. Moe, B., Langseth, I., Fyhn, M., Gabrielsen, G. W. and Bech, C. (2002). Changes in body condition in breeding kittiwakes Rissa tridactyla. J. Avian Biol. 33, 225-234.
43. Moe, B., Stempniewicz, L., Jakubas, D., Angelier, F., Chastel, O., Dinessen, F., Gabrielsen, G. W., Hanssen, F., Karnovsky, N. J., Ronning, B., Welcker, J., Wojczulanis-Jakubas, K. and Bech, C. (2009). Climate change and phenological responses of two seabird species breeding in the high-Arctic. Mar. Ecol. Prog. Ser. 393, 235-246.
44. Müller, C., Almasi, B., Roulin, A., Breuner, C. W., Jenni-Eiermann, S. and Jenni, L. (2009). Effects of corticosterone pellets on baseline and stress-induced corticosterone and corticosteroid-binding-globulin. Gen. Comp. Endocr. 160, 59-66.
45. Naves, L. C., Monnat, J. Y. and Cam, E. (2006). Breeding performance, mate fidelity, and nest site fidelity in a long-lived seabird: behaving against the current? Oikos 115, 263-276. (Pubitemid 44581370)
46. Nilsson, J. A. and Svensson, E. (1996). The cost of reproduction: a new link between current reproductive effort and future reproductive success. Proc. R. Soc. Lond. B 263, 711-714. (Pubitemid 27048012)
47. Perrins, C. M. (1970). Timing of birds breeding seasons. Ibis 112, 242-255.
48. R Development Core Team (2008). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051- 07-0, URL http://www.R-project.org.
49. Ricklefs, R. E. and Wikelski, M. (2002). The physiology/life-history nexus. Trends Ecol. Evol. 17, 462-468. (Pubitemid 35249995)
50. Romero, L. M. and Reed, J. M. (2005). Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp. Biochem. Physiol. 140A, 73-79. (Pubitemid 40139157)
51. Romero, L. M., Strochlic, D. and Wingfield, J. C. (2005). Corticosterone inhibits feather growth: potential mechanism explaining seasonal down regulation of corticosterone during molt. Comp. Biochem. Physiol. 142A, 65-73. (Pubitemid 41265916)
52. Salvante, K. G. and Williams, T. D. (2003). Effects of corticosterone on the proportion of breeding females, reproductive output and yolk precursor levels. Gen. Comp. Endocr. 130, 205-214. (Pubitemid 36207603)
53. Schoech, S., J., Bowman, R., Bridge, E., S., Morgan, G., M., Rensel, M., A., Wilcoxen, T., E. and Boughton, R. K. (2007). Corticosterone administration does not affect timing of breeding in Florida scrub-jays (Aphelocoma coerulescens). Horm. Behav. 52, 191-196. (Pubitemid 47088446)
54. Schoech, S. J., Rensel, M. A., Bridge, E. S., Boughton, R. K. and Wilcoxen, T. E. (2009). Environment, glucocorticoids, and the timing of reproduction. Gen. Comp. Endocr. 163, 201-207.
55. Shultz, M. T. and Kitaysky, A. S. (2008). Spatial and temporal dynamics of corticosterone and corticosterone binding globulin are driven by environmental heterogeneity, Gen. Comp. Endocr. 155, 717-728.
56. Shultz, M. T., Piatt, J. F., Harding, A. M. A., Kettle, A. B. and Van Pelt, T. I. (2009). Timing of breeding and reproductive performance in murres and kittiwakes reflect mismatched seasonal prey dynamics. Mar. Ecol. Prog. Ser. 393, 247-258.
57. Stenseth, N. C. and Mysterud, A. (2002). Climate, changing phenology, and other life history and traits: Nonlinearity and match-mismatch to the environment. Proc. Natl. Acad. Sci. USA 99, 13379-13381. (Pubitemid 35215388)
58. Vandenborne, K., De Groef, B., Geelissen, S., Kühn, E., Darras, V. and Van der Geyten, S. (2005). Corticosterone-induced negative feedback mechanisms within the hypothalamo-pituitary-adrenal axis of the chicken. J. Endocrinol. 185, 383-391. (Pubitemid 40883383)
59. Verhulst, S. and Nilsson, J. A. (2008). The timing of birds' breeding seasons: a review of experiments that manipulated timing of breeding. Philos. Trans. R. Soc. Lond. B 363, 399-410. (Pubitemid 350253040)
60. Visser, M. E. and Both, C. (2005). Shifts in phenology due to global climate change: the need for a yardstick. Proc. R. Soc. Lond. B 272, 2561-2569. (Pubitemid 41796558)
61. Visser, M. E., van Noordwijk, A. J., Tinbergen, J. M. and Lessells, C. M. (1998). Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc. R. Soc. Lond. B 265, 1867-1870. (Pubitemid 28477374)
62. Weimerskirch, H., Lallemand, J. and Martin, J. (2005). Population sex ratio variation in a monogamous long-lived bird, the wandering albatross. J. Anim. Ecol. 74, 285-291. (Pubitemid 40451981)
63. Wingfield, J. C. (1980). Fine temporal adjustment of reproductive functions. In Avian Endocrinology (ed. A. Epple and M. H. Stetson), pp. 367-389. New York, NY
64. Wingfield, J. C. (2008). Comparative endocrinology, environment and global change. Gen. Comp. Endocr. 157, 207-216.
65. Wingfield, J. C. and Kenagy, G. J. (1991). Natural regulation of reproductive cycles. In Vertebrate Endocrinology: Fundamentals and Biomedical Implications (ed. P. K. T. Pang and M. P. Schreibman), pp. 181-241. San Diego, CA: Academic Press.
66. Wingfield, J. C. and Sapolsky, R. M. (2003). Reproduction and resistance to stress: when and how? J. Neuroendocr. 15, 711-724. (Pubitemid 36874367)
67. Wingfield, J. C., Hahn, T. P., Maney, D. L., Schoech, S. J., Wada, M. and Morton, M. L. (2003). Effects of temperature on photoperiodically induced reproductive development, circulating plasma luteinizing hormone and thyroid hormones, body mass, fat deposition and molt in mountain white-crowned sparrows, Zonotrichia leucophrys oriantha. Gen. Comp. Endocr. 131, 143-158. (Pubitemid 36390115)
68. Wolkowitz, O., M. (1994). Prospective controlled-studies of the behavioral and biological effects of exogenous corticosteroids. Psychoneuroendocrino. 19, 233-255. (Pubitemid 24137796)
69. Zhao, X. F., Scrocchi, L. A. and Hammond, G. L. (1997). Glucocorticoids induce corticosteroid-binding globulin biosynthesis by immature mouse liver and kidney. J. Steroid Biochem. 60, 163-169. (Pubitemid 27229770)