Elevated corticosterone levels and severe weather conditions decrease parental investment of incubating Adélie penguins

Hormones and Behavior

Volumn 63, Issue 3, 2013, Pages 475-483

  Thierry, Anne Mathilde ^a,b   Massemin, Sylvie ^a,b   Handrich, Yves ^a,b   Raclot, Thierry ^a,b  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b CNRS   (France)

Author keywords

Egg temperature and rotation rate; Glucocorticoids; Incubation behaviour; Pygoscelis adeliae; Seabird; Weather conditions

Indexed keywords

CORTICOSTERONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; ECOPHYSIOLOGY; EGG; HATCHING; HYPOTHERMIA; INCUBATION TEMPERATURE; INCUBATION TIME; LOW TEMPERATURE; MALE; NONHUMAN; PARENTAL BEHAVIOR; PARENTAL INVESTMENT; PENGUIN; POPULATION SIZE; PRIORITY JOURNAL; WEATHER;

ANIMALS; CORTICOSTERONE; DRUG IMPLANTS; MALE; NESTING BEHAVIOR; OVUM; REPRODUCTION; SPHENISCIDAE; TEMPERATURE; TIME FACTORS; WEATHER;

EID: 84875056657     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2012.12.011     Document Type: Article

References (82)

1. Ainley D.G. The Adélie penguin. Bellwether of Climate Change 2002, Columbia University Press, New York.
2. Ainley D.G., LeResche R.E., Sladen W.J.L. Breeding Biology of the Adélie Penguin 1983, University of California Press, Los Angeles, CA.
3. Aldrich T.W., Raveling D.G. Effects of experience and body weight on incubation behavior of Canada geese. Auk 1983, 100:670-679.
4. Angelier F., Clement-Chastel C., Gabrielsen G.W., Chastel O. Corticosterone and time-activity budget: an experiment with black-legged kittiwakes. Horm. Behav. 2007, 52:482-491.
5. Astheimer L.B., Buttemer W.A., Wingfield J.C. Interactions of corticosterone with feeding, activity and metabolism in passerine birds. Ornis Scand. 1992, 355-365.
6. Astheimer L.B., Buttemer W.A., Wingfield J.C. Seasonal and acute changes in adrenocortical responsiveness in an Arctic-breeding bird. Horm. Behav. 1995, 29:442-457.
7. Beaulieu M., Thierry A.-M., Handrich Y., Massemin S., Le Maho Y., Ancel A. Adverse effects of instrumentation in incubating Adélie penguins (Pygoscelis adeliae). Polar Biol. 2010, 33:485-492.
8. Ben-Hur T., Cialic R., Itzik A., Barak O., Yirmiya R., Weidenfeld J. A novel permissive role for glucocorticoids in induction of febrile and behavioral signs of experimental herpes simplex virus encephalitis. Neuroscience 2001, 108:119-127.
9. Bonier F., Martin P.R., Moore I.T., Wingfield J.C. Do baseline glucocorticoids predict fitness?. Trends Ecol. Evol. 2009, 24:634-642.
10. Bourgeon S., Raclot T. Corticosterone selectively decreases humoral immunity in female eiders during incubation. J. Exp. Biol. 2006, 209:4957-4965.
11. Bracegirdle T.J., Connolley W.M., Turner J. Antarctic climate change over the twenty first century. J. Geophys. Res. 2008, 113:D03103.
12. Breuner C.W. Stress and reproduction in birds. Hormones and Reproduction of Vertebrates, Birds 2011, Academic Press. D.O. Norris, K.H. Lopez (Eds.).
13. Breuner C.W., Hahn T.P. Integrating stress physiology, environmental change, and behavior in free-living sparrows. Horm. Behav. 2003, 43:115-123.
14. Buntin J.D. Neural and hormonal control of parental behavior in birds. Advances in the Study of Behavior 1996, 161-213. Academic Press. S.R. Jay, T.S. Charles (Eds.).
15. Chastel O., Weimerskirch H., Jouventin P. High annual variability in reproductive success and survival of an Antarctic seabird, the snow petrel Pagodroma nivea. Oecologia 1993, 94:278-285.
16. Cherel Y., Robin J.-P., Walch O., Karmann H., Netchitailo P., Le Maho Y. Fasting in king penguin. 1. Hormonal and metabolic chances during breeding. Am. J. Physiol. 1988, 254:R170-R177.
17. Cockrem J.F., Silverin B. Sight of a predator can stimulate a corticosterone response in the great tit (Parus major). Gen. Comp. Endocrinol. 2002, 125:248-255.
18. Cockrem J.F., Potter M.A., Candy E.J. Corticosterone in relation to body mass in Adelie penguins (Pygoscelis adeliae) affected by unusual sea ice conditions at Ross Island, Antarctica. Gen. Comp. Endocrinol. 2006, 149:244-252.
19. Cockrem J.F., Potter M.A., Barrett D.P., Candy E.J. Corticosterone responses to capture and restraint in emperor and Adélie penguins in Antarctica. Zool. Sci. 2008, 25:291-298.
20. Conway C.J., Martin T.E. Evolution of passerine incubation behavior: influence of food, temperature, and nest predation. Evolution 2000, 54:670-685.
21. Criscuolo F., Chastel O., Bertile F., Gabrielsen G.W., Le Maho Y., Raclot T. Corticosterone alone does not trigger a short term behavioural shift in incubating female common eiders Somateria mollissima, but does modify long term reproductive success. J. Avian Biol. 2005, 36:306-312.
22. Dallman M.F., Akana S.F., Levin N., Walker C.D., Bradbury M.J., Suemaru S., Scribner K.S. Corticosteroids and the control of function in the hypothalamo-pituitary-adrenal (HPA) axis. Ann. N. Y. Acad. Sci. 1994, 746:22-31.
23. Davis L.S., McCaffrey F.T. Survival analysis of eggs and chicks of Adélie penguins (Pygoscelis adeliae). Auk 1986, 103:379-388.
24. Derksen D.V. Quantitative-analysis of incubation behavior of Adélie penguin. Auk 1977, 94:552-566.
25. R Development Core Team R: a Language and Environment for Statistical Computing 2011, R Foundation for Statistical Computing, Vienna, Austria.
26. Drent R., Daan S. The prudent parent: energetic adjustments in avian breeding. Ardea 1980, 68:225-252.
27. DuRant S.E., Hepp G.R., Moore I.T., Hopkins B.C., Hopkins W.A. Slight differences in incubation temperature affect early growth and stress endocrinology of wood duck (Aix sponsa) ducklings. J. Exp. Biol. 2010, 213:45-51.
28. Emmerson L., Pike R., Southwell C. Reproductive consequences of environment-driven variation in Adélie penguin breeding phenology. Mar. Ecol. Prog. Ser. 2011, 440:203-216.
29. Fisher R.J., Poulin R.G., Todd L.D., Brigham R.M. Nest stage, wind speed, and air temperature affect the nest defence behaviours of burrowing owls. Can. J. Zool. 2004, 82:707-713.
30. Fontaine J.J., Martin T.E. Parent birds assess nest predation risk and adjust their reproductive strategies. Ecol. Lett. 2006, 9:428-434.
31. Fowler G.S. Behavioral and hormonal responses of Magellanic penguins (Spheniscus magellanicus) to tourism and nest site visitation. Biol. Conserv. 1999, 90:143-149.
32. Goutte A., Angelier F., Welcker J., Moe B., Clement-Chastel C., Gabrielsen G.W., Bech C., Chastel O. Long-term survival effect of corticosterone manipulation in black-legged kittiwakes. Gen. Comp. Endocrinol. 2010, 167:246-251.
33. Groscolas R., Robin J.-P. Long-term fasting and re-feeding in penguins. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2001, 128:643-653.
34. Groscolas R., Decrock F., Thil M.A., Fayolle C., Boissery C., Robin J.-P. Refeeding signal in fasting-incubating king penguins: changes in behavior and egg temperature. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2000, 279:R2104-R2112.
35. Groscolas R., Lacroix A., Robin J.-P. Spontaneous egg or chick abandonment in energy-depleted king penguins: a role for corticosterone and prolactin?. Horm. Behav. 2008, 53:51-60.
36. Handrich Y. Incubation water loss in King Penguin egg. II. Does the brood patch interfere with eggshell conductance?. Physiol. Zool. 1989, 62:119-132.
37. Hardin J.W., Hilbe J.M. Generalized estimating equations. Wiley Encyclopedia of Clinical Trials 2007, John Wiley & Sons, Inc.
38. Hébert P.N. Ecological factors affecting initiation of incubation behaviour. Avian Incubation: Behaviour, Environment, and Evolution 2002, 270-279. Oxford University Press. D.C. Deeming (Ed.).
39. Hepp G.R., Kennamer R.A., Johnson M.H. Maternal effects in wood ducks: incubation temperature influences incubation period and neonate phenotype. Funct. Ecol. 2006, 20:308-314.
40. Højsgaard S., Halekoh U., Yan J. The R package geepack for generalized estimating equations. J. Stat. Softw. 2006, 15:1-11.
41. Jacobs J.D., Wingfield J.C. Endocrine control of life-cycle stages: a constraint on response to the environment?. Condor 2000, 102:35-51.
42. Jönsson K.I. Capital and income breeding as alternative tactics of resource use in reproduction. Oikos 1997, 78:57-66.
43. Kitaysky A.S., Piatt J.F., Wingfield J.C., Romano M. The adrenocortical stress-response of black-legged kittiwake chicks in relation to dietary restrictions. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 1999, 169:303-310.
44. Kitaysky A.S., Wingfield J.C., Piatt J.F. Corticosterone facilitates begging and affects resource allocation in the black-legged kittiwake. Behav. Ecol. 2001, 12:619-625.
45. Kluger M.J. Fever: role of pyrogens and cryogens. Physiol. Rev. 1991, 71:93-127.
46. Landys M.M., Ramenofsky M., Wingfield J.C. Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen. Comp. Endocrinol. 2006, 148:132-149.
47. Lea R.W., Klandorf H. The brood patch. Avian Incubation: Behaviour, Environment, and Evolution 2002, 100-118. Oxford University Press. D.C. Deeming (Ed.).
48. Liang K.-Y., Zeger S.L. Longitudinal data analysis using generalized linear models. Biometrika 1986, 73:13-22.
49. Love O.P., Williams T.D. The adaptive value of stress-induced phenotypes: effects of maternally derived corticosterone on sex-biased investment, cost of reproduction, and maternal fitness. Am. Nat. 2008, 172:E135-E149.
50. Love O.P., Breuner C.W., Vezina F., Williams T.D. Mediation of a corticosterone-induced reproductive conflict. Horm. Behav. 2004, 46:59-65.
51. McNamara J.M., Houston A.I. State-dependent life histories. Nature 1996, 380:215-221.
52. Müller C., Almasi B., Roulin A., Breuner C.W., Jenni-Eiermann S., Jenni L. Effects of corticosterone pellets on baseline and stress-induced corticosterone and corticosteroid-binding-globulin. Gen. Comp. Endocrinol. 2009, 160:59-66.
53. Ouyang J.Q., Quetting M., Hau M. Corticosterone and brood abandonment in a passerine bird. Anim. Behav. 2012, 84:261-268.
54. Peig J., Green A.J. New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 2009, 118:1883-1891.
55. Piersma T., Lindström Å., Drent R.H., Tulp I., Jukema J., Morrison R.I.G., Reneerkens J., Schekkerman H., Visser G.H. High daily energy expenditure of incubating shorebirds on High Arctic tundra: a circumpolar study. Funct. Ecol. 2003, 17:356-362.
56. Robin J.-P., Boucontet L., Chillet P., Groscolas R. Behavioral changes in fasting emperor penguins: evidence for a "refeeding signal" linked to a metabolic shift. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1998, 43:R746-R753.
57. Rogers C.M., Ramenofsky M., Ketterson E.D., Val Nolan J., Wingfield J.C. Plasma corticosterone, adrenal mass, winter weather, and season in nonbreeding populations of dark-eyed juncos (Junco hyemalis hyemalis). Auk 1993, 110:279-285.
58. Romero L.M., Remage-Healey L. Daily and seasonal variation in response to stress in captive starlings (Sturnus vulgaris): corticosterone. Gen. Comp. Endocrinol. 2000, 119:52-59.
59. Romero L.M., Reed J.M., Wingfield J.C. Effects of weather on corticosterone responses in wild free-living passerine birds. Gen. Comp. Endocrinol. 2000, 118:113-122.
60. Silverin B. Corticosterone-binding proteins and behavioral effects of high plasma lavels of corticosterone during the breeding period of the pied flycatcher. Gen. Comp. Endocrinol. 1986, 64:67-74.
61. Sladen W.J.L. The pygoscelid penguins, scientific reports. Falkland Islands Dependencies Survey, London 1958.
62. Spée M., Beaulieu M., Dervaux A., Chastel O., Le Maho Y., Raclot T. Should I stay (prolactin) or should I go (corticosterone): hormonal control of nest abandonment in a long-lived bird, the Adélie penguin. Horm. Behav. 2010, 58:762-768.
63. Spée M., Marchal L., Lazin D., Le Maho Y., Chastel O., Beaulieu M., Raclot T. Exogenous corticosterone and nest abandonment: a study in a long-lived bird, the Adélie penguin. Horm. Behav. 2011, 60:362-370.
64. Spée M., Marchal L., Thierry A.-M., Chastel O., Enstipp M., Le Maho Y., Beaulieu M., Raclot T. Exogenous corticosterone mimics a late fasting stage in captive Adélie penguins (Pygoscelis adeliae). Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 300:R1241-R1249.
65. Stearns S.C. The Evolution of Life-Histories 1992, Oxford University Press.
66. Tinbergen J.M., Williams J.B. Energetics of Incubation, Avian Incubation: Behaviour, Environment, and Evolution 2002, 299-313.
67. Ullian M.E. The role of corticosteroids in the regulation of vascular tone. Cardiovasc. Res. 1999, 41:55-64.
68. Vleck C.M., Ross L.L., Vleck D., Bucher T.L. Prolactin and parental behavior in Adelie penguins: effects of absence from nest, incubation length, and nest failure. Horm. Behav. 2000, 38:149-158.
69. Weimerskirch H., Zimmermann L., Prince P.A. Influence of environmental variability on breeding effort in a long-lived seabird, the yellow-nosed albatross. Behav. Ecol. 2001, 12:22-30.
70. Weinrich J.A., Baker J.R. Adelie penguin (Pygoscelis adeliae) embryonic development at different temperatures. Auk 1978, 95:569-576.
71. Williams G.C. Natural selection, the costs of reproduction, and a refinement of lack's principle. Am. Nat. 1966, 100:687.
72. Wingfield J.C. Control of behavioural strategies for capricious environments. Anim. Behav. 2003, 66:807-815.
73. Wingfield J.C., Kitaysky A.S. Endocrine responses to unpredictable environmental events: stress or anti-stress hormones?. Integr. Comp. Biol. 2002, 42:600-609.
74. Wingfield J.C., Ramenofsky M. Corticosterone and facultative dispersal in response to unpredictable events. Ardea 1997, 85:155-166.
75. Wingfield J.C., Sapolsky R.M. Reproduction and resistance to stress: when and how. J. Neuroendocrinol. 2003, 15:711-724.
76. Wingfield J.C., Silverin B. Ecophysiological studies of hormone-behavior relations in birds. Hormones, Brain and Behavior 2009, 817-854. Academic, San Diego, CA. D.W. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach, R.T. Rubin (Eds.).
77. Wingfield J.C., Moore M.C., Farner D.S. Endocrine responses to inclement weather in naturally breeding populations of white-crowned sparrows (Zonotrichia leucophrys pugetensis). Auk 1983, 100:56-62.
78. Wingfield J.C., Maney D.L., Breuner C.W., Jacobs J.D., Lynn S., Ramenofsky M., Richardson R.D. Ecological bases of hormone-behavior interactions: the "emergency life history stage". Am. Zool. 1998, 38:191-206.
79. Wingfield J.C., Patrick Kelley J., Angelier F., Chastel O., Lei F., Lynn S., Miner B., Davis J., Li D., Wang G. Organism-environment interactions in a changing world: a mechanistic approach. J. Ornithol. 2011, 152:279-288.
80. Yan J. Geepack: yet another package for generalized estimating equations. R-News 2002, 2(3):12-14.
81. Yan J., Fine J.P. Estimating equations for association structures. Stat. Med. 2004, 23:859-880.
82. Zuur A., Ieno E., Walker N., Saveliev A., Smith G. Mixed Effects Models and Extensions in Ecology with R 2009, Springer.