Starting with a handicap: Phenotypic differences between early- and late-born king penguin chicks and their survival correlates

Functional Ecology

Volumn 28, Issue 3, 2014, Pages 601-611

  Stier, Antoine ^a   Viblanc, Vincent A ^b   Massemin Challet, Sylvie ^a   Handrich, Yves ^a   Zahn, Sandrine ^a   Rojas, Emilio R ^a   Saraux, Claire ^c   Le Vaillant, Maryline ^a   Prud'homme, Onésime ^a   Grosbellet, Edith ^d   Robin, Jean Patrice ^a   Bize, Pierre ^e   Criscuolo, Francois ^a  

^a INSTITUT DE RECHERCHES SUBATOMIQUES   (France)

^b CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^c IFREMER   (France)

^d Hopitaux Universitaires de Strasbourg   (France)

^e UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Corticosterone; Early life conditions; Growth; Individual quality; Oxidative stress; Phenotypic plasticity; Reproductive timing; Telomere

Indexed keywords

ADAPTATION; BIOENERGETICS; BODY MASS; BREEDING SEASON; FLEDGING; GROWTH; HANDICAP PRINCIPLE; INDIVIDUAL VARIATION; MATERNAL EFFECT; MORTALITY; OXIDATION; PHENOTYPIC PLASTICITY; SEABIRD; STEROID; SURVIVAL; WINTER;

APTENODYTES PATAGONICUS; SPHENISCIDAE;

EID: 84900560588     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12204     Document Type: Article

References (71)

1. Abrams, P., Leimar, O., Nylin, S. & Wiklund, C. (1996) The effect of flexible growth rates on optimal sizes and development times in a seasonal environment. The American Naturalist, 147, 381-395.
2. Alonso-Alvarez, C., Bertrand, S., Faivre, B. & Sorci, G. (2007) Increased susceptibility to oxidative damage as a cost of accelerated somatic growth in zebra finches. Functional Ecology, 21, 873-879.
3. Angelier, F., Weimerskirch, H., Dano, S. & Chastel, O. (2007) Age, experience and reproductive performance in a long-lived bird: a hormonal perspective. Behavioral Ecology and Sociobiology, 61, 611-621.
4. Arendt, J.D. (1997) Adaptive intrinsic growth rates: an integration across taxa. Quarterly Review of Biology, 72, 149-177.
5. Bauch, C., Becker, P.H. & Verhulst, S. (2013) Telomere length reflects phenotypic quality and costs of reproduction in a long-lived seabird. Proceedings of the Royal Society of London. Series B: Biological Sciences, 280, 20122540.
6. Beaulieu, M., Reichert, S., Le Maho, Y., Ancel, A. & Criscuolo, F. (2011) Oxidative status and telomere length in a long-lived bird facing a costly reproductive event. Functional Ecology, 25, 577-585.
7. Benowitz Fredericks, Z.M. & Kitaysky, A.S. (2005) Benefits and costs of rapid growth in common murre chicks Uria aalge. Journal of Avian Biology, 36, 287-294.
8. Bize, P., Metcalfe, N.B. & Roulin, A. (2006) Catch-up growth strategies differ between body structures: interactions between age and structure-specific growth in wild nestling Alpine Swifts. Functional Ecology, 20, 857-864.
9. Bize, P., Devevey, G., Monaghan, P., Doligez, B. & Christe, P. (2008) Fecundity and survival in relation to resistance to oxidative stress in a free-living bird. Ecology, 89, 2584-2593.
10. Bize, P., Criscuolo, F., Metcalfe, N., Nasir, L. & Monaghan, P. (2009) Telomere dynamics rather than age predict life expectancy in the wild. Proceedings of the Royal Society of London. Series B, Biological Sciences, 276, 1679-1683.
11. Bonier, F., Martin, P.R., Moore, I.T. & Wingfield, J.C. (2009) Do baseline glucocorticoids predict fitness? Trends in Ecology & Evolution, 24, 634-642.
12. Brinkhof, M.W. (1997) Seasonal decline in body size of Coot chicks. Journal of Avian Biology, 28, 117-131.
13. Brinkhof, M.W. & Cavé, A.J. (1997) Food supply and seasonal variation in breeding success: an experiment in the European coot. Proceedings of the Royal Society of London Series B: Biological Sciences, 264, 291-296.
14. Cherel, Y. & Le Maho, Y. (1985) Five months of fasting in king penguin chicks: body mass loss and fuel metabolism. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 249, R387-R392.
15. Cherel, Y., Stahl, J.-C. & Le Maho, Y. (1987) Ecology and physiology of fasting in king penguin chicks. The Auk, 104, 254-262.
16. Corbel, H., Geiger, S. & Groscolas, R. (2010) Preparing to fledge: the adrenocortical and metabolic responses to stress in king penguin chicks. Functional Ecology, 24, 82-92.
17. Corbel, H., Morlon, F., Geiger, S. & Groscolas, R. (2009) State-dependent decisions during the fledging process of king penguin chicks. Animal Behaviour, 78, 829-838.
18. Cote, J., Clobert, J., Meylan, S. & Fitze, P.S. (2006) Experimental enhancement of corticosterone levels positively affects subsequent male survival. Hormones and Behavior, 49, 320-327.
19. Criscuolo, F., Bize, P., Nasir, L., Metcalfe, N.B., Foote, C.G., Griffiths, K. et al. (2009) Real-time quantitative PCR assay for measurement of avian telomeres. Journal of Avian Biology, 40, 342-347.
20. Daan, S., Dijkstra, C., Drent, R. & Meijer, T. (1988) Food supply and the annual timing of avian reproduction. Proceedings XIXth Ornithological Congress, Ottawa, 1986, 392-407.
21. Dantzer, B., Newman, A.E.M., Boonstra, R., Palme, R., Boutin, S., Humphries, M.M. et al. (2013) Density triggers maternal hormones that increase adaptive offspring growth in a wild mammal. Science, 340, 1215-1217.
22. Daunt, F., Wanless, S., Harris, M.P. & Monaghan, P. (1999) Experimental evidence that age-specific reproductive success is independent of environmental effects. Proceedings of the Royal Society of London Series B: Biological Sciences, 266, 1489-1493.
23. Descamps, S., Gauthier-Clerc, M., Gendner, J.-P. & Le Maho, Y. (2002) The annual breeding cycle of unbanded king penguins Aptenodytes patagonicus on Possession Island (Crozet). Avian Science, 2, 87-98.
24. Descamps, S., Gauthier-Clerc, M., Le Bohec, C., Gendner, J.-P. & Le Maho, Y. (2005) Impact of predation on king penguin Aptenodytes patagonicus in Crozet Archipelago. Polar Biology, 28, 303-310.
25. Dmitriew, C.M. (2011) The evolution of growth trajectories: what limits growth rate? Biological Reviews, 86, 97-116.
26. Forchhammer, M.C., Clutton Brock, T.H., Lindström, J. & Albon, S.D. (2001) Climate and population density induce long-term cohort variation in a northern ungulate. Journal of Animal Ecology, 70, 721-729.
27. Forslund, P. & Pärt, T. (1995) Age and reproduction in birds - hypotheses and tests. Trends in Ecology & Evolution, 10, 374-378.
28. Gauthier-Clerc, M., Le Maho, Y., Clerquin, Y., Bost, C.-A. & Handrich, Y. (2002) Seabird reproduction in an unpredictable environment: how king penguins provide their young chicks with food. Marine Ecology Progress Series, 237, 291-300.
29. Geiger, S., Le Vaillant, M., Lebard, T., Reichert, S., Stier, A., Le Maho, Y. et al. (2012) Catching-up but telomere loss: half-opening the black box of growth and ageing trade-off in wild king penguin chicks. Molecular Ecology, 21, 1500-1510.
30. Griffiths, R., Double, M.C., Orr, K. & Dawson, R.J. (2002) A DNA test to sex most birds. Molecular Ecology, 7, 1071-1075.
31. Groothuis, T.G.G., Müller, W., von Engelhardt, N., Carere, C. & Eising, C. (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neuroscience & Biobehavioral Reviews, 29, 329-352.
32. Halliwell, B. & Gutteridge, J. M. C. (2007) Free Radicals in Biology and Medicine. URL (accessed 1 March 2013).
33. Haussmann, M.F., Longenecker, A.S., Marchetto, N.M., Juliano, S.A. & Bowden, R.M. (2012) Embryonic exposure to corticosterone modifies the juvenile stress response, oxidative stress and telomere length. Proceedings of the Royal Society of London. Series B, Biological Sciences, 279, 1447-1456.
34. Hayward, L.S. & Wingfield, J.C. (2004) Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. General and Comparative Endocrinology, 135, 365-371.
35. Heezik, Y.V., Seddon, P.J., Cooper, J. & Plös, A.L. (1994) Interrelationships between breeding frequency, timing and outcome in king penguins Aptenodytes patagonicus: are king penguins biennial breeders? Ibis, 136, 279-284.
36. Heidinger, B.J., Blount, J.D., Boner, W., Griffiths, K., Metcalfe, N.B. & Monaghan, P. (2012) Telomere length in early life predicts lifespan. Proceedings of the National Academy of Sciences of the United States of America, 109, 1743-1748.
37. Honarmand, M., Goymann, W. & Naguib, M. (2010) Stressful dieting: nutritional conditions but not compensatory growth elevate corticosterone levels in zebra finch nestlings and fledglings (ed C Kullberg). PLoS One, 5, e12930.
38. Horn, T., Robertson, B.C., Will, M., Eason, D.K., Elliott, G.P. & Gemmell, N.J. (2011) Inheritance of telomere length in a bird. PLoS One, 6, e17199.
39. Kitaysky, A.S., Wingfield, J.C. & Piatt, J.F. (2001) Corticosterone facilitates begging and affects resource allocation in the black-legged kittiwake. Behavioral Ecology, 12, 619-625.
40. Kitaysky, A., Kitaiskaia, E., Piatt, J. & Wingfield, J. (2003) Benefits and costs of increased levels of corticosterone in seabird chicks. Hormones and Behavior, 43, 140-149.
41. Lecomte, V.J., Sorci, G., Cornet, S., Jaeger, A., Faivre, B., Arnoux, E. et al. (2010) Patterns of aging in the long-lived wandering albatross. Proceedings of the National Academy of Sciences of the United States of America, 107, 6370-6375.
42. Lindström, J. (1999) Early development and fitness in birds and mammals. Trends in Ecology & Evolution, 14, 343-348.
43. Metcalfe, N. & Monaghan, P. (2001) Compensation for a bad start: grow now, pay later? Trends in Ecology & Evolution, 16, 254-260.
44. Monaghan, P. (2008) Early growth conditions, phenotypic development and environmental change. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 363, 1635-1645.
45. Monaghan, P. & Haussmann, M. (2006) Do telomere dynamics link lifestyle and lifespan? Trends in Ecology & Evolution, 21, 47-53.
46. Mousseau, T.A. & Fox, C.W. (1998) The adaptive significance of maternal effects. Trends in Ecology & Evolution, 13, 403-407.
47. Muller, M. & Groothuis, T.G. (2013) Within-clutch variation in yolk testosterone as an adaptive maternal effect to modulate avian sibling competition: evidence from a comparative study. The American Naturalist, 181, 125-136.
48. Nylin, S. & Gotthard, K. (1998) Plasticity in life-history traits. Annual Review of Entomology, 43, 63-83.
49. Olsson, O. (1996) Seasonal effects of timing and reproduction in the king penguin: a unique breeding cycle. Journal of Avian Biology, 27, 7-14.
50. Olsson, O. (1997) Clutch abandonment: a state-dependent decision in king penguins. Journal of Avian Biology, 28, 264-267.
51. Perrins, C.M. (1970) The timing of birds 'breeding seasons. Ibis, 112, 242-255.
52. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29, 2003-2007.
53. Roff, D. (1980) Optimizing development time in a seasonal environment: the 'ups and downs' of clinal variation. Oecologia, 45, 202-208.
54. Salomons, H.M., Mulder, G.A., van de Zande, L., Haussmann, M.F., Linskens, M.H.K. & Verhulst, S. (2009) Telomere shortening and survival in free-living corvids. Proceedings of the Royal Society of London. Series B, Biological Sciences, 276, 3157-3165.
55. Saraux, C., Viblanc, V.A., Hanuise, N., Le Maho, Y. & Le Bohec, C. (2011) Effects of individual pre-fledging traits and environmental conditions on return patterns in juvenile king penguins (ed S Thrush). PLoS One, 6, e20407.
56. Sepp, T., Sild, E., Blount, J.D., Männiste, M., Karu, U. & Hõrak, P. (2012) Individual consistency and covariation of measures of oxidative status in greenfinches. Physiological and Biochemical Zoology, 85, 299-307.
57. Sies, H. (2007) Total antioxidant capacity: appraisal of a concept. The Journal of Nutrition, 137, 1493-1495.
58. Smith, S., Turbill, C. & Penn, D.J. (2011) Chasing telomeres, not red herrings, in evolutionary ecology. Heredity, 107, 372-373.
59. Spencer, K.A., Evans, N.P. & Monaghan, P. (2009) Postnatal stress in birds: a novel model of glucocorticoid programming of the hypothalamic-pituitary-adrenal axis. Endocrinology, 150, 1931-1934.
60. Stier, A., Reichert, S., Massemin, S., Bize, P. & Criscuolo, F. (2012) Constraint and cost of oxidative stress on reproduction: correlative evidence in laboratory mice and review of the literature. Frontiers in Zoology, 9, 37.
61. Stonehouse, B. (1960) The king penguin: Aptenodytes patagonica, of South Georgia. Scientific Report of the Falkland Islands Dependencies Survey, 1-81.
62. Tarry-Adkins, J.L., Martin-Gronert, M.S., Chen, J.H., Cripps, R.L. & Ozanne, S.E. (2008) Maternal diet influences DNA damage, aortic telomere length, oxidative stress, and antioxidant defense capacity in rats. The FASEB Journal, 22, 2037-2044.
63. Tarry-Adkins, J.L., Chen, J.H., Smith, N.S., Jones, R.H., Cherif, H. & Ozanne, S.E. (2009) Poor maternal nutrition followed by accelerated postnatal growth leads to telomere shortening and increased markers of cell senescence in rat islets. The FASEB Journal, 23, 1521-1528.
64. Tarry-Adkins, J.L., Martin-Gronert, M.S., Fernandez-Twinn, D.S., Hargreaves, I., Alfaradhi, M.Z., Land, J.M. et al. (2013) Poor maternal nutrition followed by accelerated postnatal growth leads to alterations in DNA damage and repair, oxidative and nitrosative stress, and oxidative defense capacity in rat heart. The FASEB Journal, 27, 379-390.
65. Verhulst, S. & Tinbergen, J.M. (1991) Experimental evidence for a causal relationship between timing and success of reproduction in the great tit Parus m. major. The Journal of Animal Ecology, 60, 269-282.
66. Viblanc, V.A.V. (2011) Coping with energy limitation, social constraints and stress in a colonial breeder, the king penguin (Aptenodytes patagonicus). PhD thesis, University of Strasbourg, Strasbourg, France.
67. Voillemot, M., Hine, K., Zahn, S., Criscuolo, F., Gustafsson, L., Doligez, B. et al. (2012) Effects of brood size manipulation and common origin on phenotype and telomere length in nestling collared flycatchers. BMC Ecology, 12, 17.
68. Weimerskirch, H., Stahl, J.C. & Jouventin, P. (1992) The breeding biology and population dynamics of king penguins Aptenodytes patagonica on the Crozet Islands. Ibis, 134, 107-117.
69. Wingfield, J.C., Williams, T.D. & Visser, M.E. (2008) Introduction. Integration of ecology and endocrinology in avian reproduction: a new synthesis. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 363, 1581-1588.
70. Wingfield, J.C., Maney, D.L., Breuner, C.W., Jacobs, J.D., Lynn, S., Ramenofsky, M. et al. (1998) Ecological bases of hormone - behavior interactions: the 'emergency life history stage'. Integrative and Comparative Biology, 38, 191-206.
71. Wolf, J.B. & Wade, M.J. (2009) What are maternal effects (and what are they not)? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 364, 1107-1115.