The oxidative debt of fasting: Evidence for short- to medium-term costs of advanced fasting in adult king penguins

Journal of Experimental Biology

Volumn 219, Issue 20, 2016, Pages 3284-3293

  Schull, Quentin ^a   Viblanc, Vincent A ^a   Stier, Antoine ^a   Saadaoui, Hédi ^a   Lefol, Emilie ^a   Criscuolo, François ^a   Bize, Pierre ^b   Robin, Jean Patrice ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Foraging effort; Hormesis; Oxidative stress; Re feeding signal

Indexed keywords

ANTIOXIDANT; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

AGING; ANIMAL; BLOOD; BODY WEIGHT; DIET RESTRICTION; FEEDING BEHAVIOR; METABOLISM; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PENGUIN; PHYSIOLOGY; SEA; STATISTICAL MODEL;

AGING; ANIMALS; ANTIOXIDANTS; BODY WEIGHT; FASTING; FEEDING BEHAVIOR; LINEAR MODELS; OCEANS AND SEAS; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SPHENISCIDAE; SUPEROXIDE DISMUTASE;

EID: 84992110550     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.145250     Document Type: Article

References (102)

1. Allen, R. and Tresini, M. (2000). Oxidative stress and gene regulation. Free Radic. Biol. Med. 28, 463-499.
2. Andreyev, A. Y., Kushnareva, Y. E. and Starkov, A. A. (2005). Mitochondrial metabolism of reactive oxygen species. Biochemistry 70, 200-214.
3. Angelier, F. and Chastel, O. (2009). Stress, prolactin and parental investment in birds: a review. Gen. Comp. Endocrinol. 163, 142-148.
4. Beckman, K. B. and Ames, B. N. (1998). The free radical theory of aging matures. Physiol. Rev. 78, 547-581.
5. Belkhou, R., Cherel, Y., Heitz, A., Robin, J.-P. and Le Maho, Y. (1991). Energy contribution of proteins and lipids during prolonged fasting in the rat. Nutr. Res. 11, 365-374.
6. Bertile, F., Schaeffer, C., Le Maho, Y., Raclot, T. and Van Dorsselaer, A. (2009). A proteomic approach to identify differentially expressed plasma proteins between the fed and prolonged fasted states. Proteomics 9, 148-158.
7. Bize, P., Devevey, G., Monaghan, P., Doligez, B. and Christe, P. (2008). Fecundity and survival in relation to resistance to oxidative stress in a free-living bird. Ecology 89, 2584-2593.
8. Bost, C. A., Georges, J. Y., Guinet, C., Cherel, Y., Pütz, K., Charrassin, J. B., Handrich, Y., Zorn, T., Lage, J. and Le Maho, Y. (1997). Foraging habitat and food intake of satellite-tracked king penguins during the austral summer at Crozet Archipelago. Mar. Ecol. Prog. Ser. 150, 21-33.
9. Bost, C. A., Handrich, Y., Butler, P. J., Fahlman, A., Halsey, L. G., Woakes, A. J. and Ropert-Coudert, Y. (2007). Changes in dive profiles as an indicator of feeding success in king and Adélie penguins. Deep. Res. Part II Top. Stud. Oceanogr. 54, 248-255.
10. Bretz, F., Hothorn, T. Westfall, P. (2010). Multiple comparisons using R.Boca Raton, FL: CRC Press.
11. Ceriello, A. and Motz, E. (2004). Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler. Thromb. Vasc. Biol. 24, 816-823.
12. Charrassin, J.-B. and Bost, C.-A. (2001). Utilisation of the oceanic habitat by king penguins over the annual cycle. Mar. Ecol. Prog. Ser. 221, 285-298.
13. Chausse, B., Vieira-Lara, M. A., Sanchez, A. B., Medeiros, M. H. G. and Kowaltowski, A. J. (2015). Intermittent fasting results in tissue-specific changes in bioenergetics and redox state. PLoS ONE 10, 1-13.
14. Cherel, Y., Stahl, J. and Le Maho, Y. (1987). Ecology and physiology of fasting in king penguin chicks. Auk 104, 254-262.
15. Cherel, Y., Robin, J. P., Walch, O., Karmann, H., Netchitailo, P. and Le Maho, Y. (1988a). Fasting in king penguin. I. Hormonal and metabolic changes during breeding. Am. J. Physiol. 254, R170-R177.
16. Cherel, Y., Leloup, J. and Le Maho, Y. (1988b). Fasting in king penguin. II. Hormonal and metabolic changes during molt. Am. J. Physiol. 254, R178-R184.
17. Cherel, Y., Mauget, R., Lacroix, A. and Gilles, J. (1994a). Seasonal and fasting-related changes in circulating gonadal steroids and prolactin in king penguins, Aptenodytes patagonicus. Physiol. Zool. 67, 1154-1173.
18. Cherel, Y., Gilles, J., Handrich, Y. and Maho, Y. (1994b). Nutrient reserve dynamics and energetics during long-term fasting in the king penguin (Aptenodytes patagonicus). J. Zool. 234, 1-12.
19. Chouchani, E. T., Pell, V. R., James, A. M., Work, L. M., Saeb-Parsy, K., Frezza, C., Krieg, T. and Murphy, M. P. (2016). A unifying mechanism for mitochondrial superoxide production during ischemia-reperfusion injury. Cell Metab. 23, 254-263.
20. Costantini, D. (2008). Oxidative stress in ecology and evolution: lessons from avian studies. Ecol. Lett. 11, 1238-1251.
21. Costantini, D. (2011). On the measurement of circulating antioxidant capacity and the nightmare of uric acid. Methods Ecol. Evol. 2, 321-325.
22. Costantini, D. (2014). Oxidative Stress and Hormesis in Evolutionary Ecology and Physiology. A Marriage Between Mechanistic and Evolutionay Approaches. New York: Springer.
23. Costantini, D. (2016). Oxidative stress ecology and the d-ROMs test: facts, misfacts and an appraisal of a decade's work. Behav. Ecol. Sociobiol. 70, 809-820.
24. Costantini, D. and Dell'Omo, G. (2006). Effects of T-cell-mediated immune response on avian oxidative stress. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 145, 137-142.
25. Costantini, D., Marasco, V. and Møller, A. P. (2011). A meta-analysis of glucocorticoids as modulators of oxidative stress in vertebrates. J. Comp. Physiol. B 181, 447-456.
26. Criscuolo, F., Gabrielsen, G. W., Gendner, J. P. and Le Maho, Y. (2002). Body mass regulation during incubation in female common eiders Somateria mollissima. J. Aquat. Ecosyst. Stress Recover. 1, 83-88.
27. Dawson, A., King, V. M., Bentley, G. E. and Ball, G. F. (2001). Photoperiodic control of seasonality in birds. J. Biol. Rhythms 16, 365-380.
28. Finaud, J., Lac, G. and Filaire, E. (2006). Oxidative stress: relationship with exercise and training. Sport. Med. 36, 327-358.
29. Froget, G., Butler, P. J., Woakes, A. J., Fahlman, A., Kuntz, G., Le Maho, Y. and Handrich, Y. (2004). Heart rate and energetics of free-ranging king penguins (Aptenodytes patagonicus). J. Exp. Biol. 207, 3917-3926.
30. Gauthier-Clerc, M., Le Maho, Y., Gendner, J.-P., Durant, J. and Handrich, Y. (2001). State-dependent decisions in long-term fasting king penguins, Aptenodytes patagonicus, during courtship and incubation. Anim. Behav. 62, 661-669.
31. Geiger, S., Kauffmann, M., Le Maho, Y., Robin, J.-P. and Criscuolo, F. (2012). Of the importance of metabolic phases in the understanding of oxidative stress in prolonged fasting and refeeding. Physiol. Biochem. Zool. 85, 415-420.
32. Geiser, F. and Stawski, C. (2011). Hibernation and torpor in tropical and subtropical bats in relation to energetics, extinctions, and the evolution of endothermy. Integr. Comp. Biol. 51, 337-348.
33. Goodman, M. N., McElaney, M. A. and Ruderman, N. B. (1981). Adaptation to prolonged starvation in the rat: curtailment of skeletal muscle proteolysis. Am. J. Physiol. 241, E321-E327.
34. Granger, D. N. (1988). Role of xanthine oxidase and granulocytes in ischemia-reperfusion injury. Am. J. Physiol. 255, H1269-H1275.
35. Groscolas, R. (1990). Metabolic adaptations to fasting in emperor and king penguins. In Penguin Biology (ed. L. S. Davies and J. T. Darby), pp. 269-296. San Diego, CA: Academic Press.
36. Groscolas, R. and Robin, J.-P. (2001). Long-term fasting and re-feeding in penguins. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 128, 643-653.
37. Groscolas, R., Decrock, F., Thil, M. A., Fayolle, C., Boissery, C. and Robin, J. P. (2000). Refeeding signal in fasting-incubating king penguins: changes in behavior and egg temperature. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279, R2104-R2112.
38. Groscolas, R., Lacroix, A. and Robin, J.-P. (2008). Spontaneous egg or chick abandonment in energy-depleted king penguins: a role for corticosterone and prolactin? Horm. Behav. 53, 51-60.
39. Huang, Z., Huang, P. L., Panahian, N., Dalkara, T., Fishman, M. C. and Moskowitz, M. A. (1994). Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science. 265, 1883-1885.
40. Hulbert, A. J., Pamplona, R., Buffenstein, R. and Buttemer, W. A. (2007). Life and death: metabolic rate, membrane composition, and life span of animals. Am. Physiol. Soc. 1175-1213.
41. Iadecola, C., Zhang, F., Casey, R., Nagayama, M. and Ross, M. E. (1997). Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene. J. Neurosci. 17, 9157-9164.
42. Isaksson, C. and Andersson, S. (2008). Oxidative stress does not influence carotenoid mobilization and plumage pigmentation. Proc. R. Soc. B Biol. Sci. 275, 309-314.
43. Isaksson, C., Sheldon, B. C. and Uller, T. (2011). The challenges of integrating oxidative stress into life-history biology. BioScience 61, 194-202.
44. Kamata, H. and Hirata, H. (1999). Redox regulation of cellular signalling. Cell. Signal. 11, 1-14.
45. Kitaysky, A. S., Wingfield, J. C. and Piatt, J. F. (1999). Dynamics of food availability, body condition and physiological stress response in breeding blacklegged kittiwakes. Funct. Ecol. 13, 577-584.
46. Koch, R. E. and Hill, G. E. (2016). An assessment of techniques to manipulate oxidative stress in animals. Funct. Ecol.
47. Kooyman, G. L., Cherel, Y., Maho, Y. L., Croxall, J. P., Thorson, P. H., Ridoux, V. and Kooyman, C. A. (1992). Diving behavior and energetics during foraging cycles in king penguins. Ecol. Monogr. 62, 143-163.
48. Koubi, H. E., Robin, J. P., Dewasmes, G., Le Maho, Y., Frutoso, J. and Minaire, Y. (1991). Fasting-induced rise in locomotor activity in rats coincides with increased protein utilization. Physiol. Behav. 50, 337-343.
49. Le Maho, Y., Vu Van Kha, V., Koubi, H. E. and Cagnard, M. (1981). Body composition, energy expenditure, and plasma metabolites in long-term fasting geese. Am. J. Physiol. 241, E342-E354.
50. Le Vaillant, M., Viblanc, V. A., Saraux, C., Le Bohec, C., Le Maho, Y., Kato, A., Criscuolo, F. and Ropert-Coudert, Y. (2015). Telomere length reflects individual quality in free-living adult king penguins. Polar Biol. 38, 2059-2067.
51. Lin, H., Decuypere, E. and Buyse, J. (2004). Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus): 1. Chronic exposure. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 139, 737-744.
52. Lindstedt, S. L. and Boyce, M. S. (1985). Seasonality, fasting endurance, and body size in mammals. Am. Nat. 125, 873-878.
53. Mårtensson, J. (1986). The effect of fasting on leukocyte and plasma glutathione and sulfur amino acid concentrations. Metabolism 35, 118-121.
54. McCue, M. D. (2010). Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 156, 1-18.
55. McCue, M. D. (ed.) (2012). Comparative Physiology of Fasting, Starvation, and Food Limitation. New York: Springer.
56. Meir, J. U. and Ponganis, P. J. (2009). High-affinity hemoglobin and blood oxygen saturation in diving emperor penguins. J. Exp. Biol. 212, 3330-3338.
57. Metcalfe, N. B. and Alonso-Alvarez, C. (2010). Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct. Ecol. 24, 984-996.
58. Millar, J. S. and Hickling, G. J. (1990). Fasting endurance and the evolution of mammalian body size. Funct. Ecol. 4, 5-12.
59. Minokoshi, Y., Alquier, T., Furukawa, N., Kim, Y.-B., Lee, A., Xue, B., Mu, J., Foufelle, F., Ferré, P., Birnbaum, M. J. et al. (2004). AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 428, 569-574.
60. Monaghan, P., Metcalfe, N. B. and Torres, R. (2009). Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol. Lett. 12, 75-92.
61. Monternier, P.-A., Marmillot, V., Rouanet, J.-L. and Roussel, D. (2014). Mitochondrial phenotypic flexibility enhances energy savings during winter fast in king penguin chicks. J. Exp. Biol. 217, 2691-2697.
62. Morales, A. E., Pérez-Jiménez, A., Carmen Hidalgo, M., Abellán, E. and Cardenete, G. (2004). Oxidative stress and antioxidant defenses after prolonged starvation in Dentex dentex liver. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 139, 153-161.
63. Muggeo, V. M. R. (2008). segmented: an {R} package to fit regression models with broken-line relationships. R News 8, 20-25.
64. Nakagawa, S. and Cuthill, I. C. (2007). Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol. Rev. 82, 591-605.
65. Nordøy, E. S., Ingebretsen, O. C. and Blix, A. S. (1990). Depressed metabolism and low protein catabolism in fasting grey seal pups. Acta Physiol. Scand. 139, 361-369.
66. Olsson, O. (1996). Seasonal effects of timing and reproduction in the king penguin: a unique breeding cycle. J. Avian Biol. 27, 7.
67. Olsson, O. (1997). Clutch abandonment: a state-dependent decision in king penguins. J. Avian Biol. 28, 264.
68. Phillips, R. A. and Hamer, K. C. (1999). Lipid reserves, fasting capability and the evolution of nestling obesity in procellariiform seabirds. Proc. R. Soc. B Biol. Sci. 266, 1329.
69. Rey, B., Halsey, L. G., Dolmazon, V., Rouanet, J.-L., Roussel, D., Handrich, Y., Butler, P. J. and Duchamp, C. (2008). Long-term fasting decreases mitochondrial avian UCP-mediated oxygen consumption in hypometabolic king penguins. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R92-R100.
70. Richter, T. and Von Zglinicki, T. (2007). A continuous correlation between oxidative stress and telomere shortening in fibroblasts. Exp. Gerontol. 42, 1039-1042.
71. Ristow, M. and Zarse, K. (2010). How increased oxidative stress promotes longevity and metabolic health: The concept of mitochondrial hormesis (mitohormesis). Exp. Gerontol. 45, 410-418.
72. Robin, J. P., Frain, M., Sardet, C., Groscolas, R. and Le Maho, Y. (1988). Protein and lipid utilization during long-term fasting in emperor penguins. Am. J. Physiol. Regul. Integr. Comp. Physiol. 254, R61-R68.
73. Robin, J. P., Boucontet, L., Chillet, P. and Groscolas, R. (1998). Behavioral changes in fasting emperor penguins: evidence for a 'refeeding signal' linked to a metabolic shift. Am. Physiol. Soc. 274, 746-753.
74. Robin, J.-P., Fayolle, C., Decrock, F., Thil, M.-A., Côté, S. D., Bernard, S. and Groscolas, R. (2001). Restoration of body mass in king penguins after egg abandonment at a critical energy depletion stage: early vs late breeders. J. Avian Biol. 32, 303-310.
75. Robin, J. P., Decrock, F., Herzberg, G., Mioskowski, E., Le Maho, Y., Bach, A. and Groscolas, R. (2008). Restoration of body energy reserves during refeeding in rats is dependent on both the intensity of energy restriction and the metabolic status at the onset of refeeding. J. Nutr. 138, 861-866.
76. Romero, L. M. and Romero, R. C. (2002). Corticosterone responses in wild birds: the importance of rapid initial sampling. Condor 104, 129.
77. Secor, S. M. and Carey, H. V. (2016). Integrative physiology of fasting. Compr. Physiol. 6, 773-825.
78. Selman, C., Blount, J. D., Nussey, D. H. and Speakman, J. R. (2012). Oxidative damage, ageing, and life-history evolution: where now? Trends Ecol. Evol. 27, 570-577.
79. Sorensen, M., Sanz, A., Gómez, J., Pamplona, R., Portero-Otín, M., Gredilla, R. and Barja, G. (2006). Effects of fasting on oxidative stress in rat liver mitochondria. Free Radic. Res. 40, 339-347.
80. Souza Rocha, G., Fonseca, A., Rodrigues, M., Dantas, F., Caldeira-de-Araujo, A. and Santos, R. (2008). Comet assay to determine DNA damage induced by food deprivation in rats. Acta Biol. Hung. 59, 315-325.
81. Speakman, J. R. and Selman, C. (2011). The free-radical damage theory: accumulating evidence against a simple link of oxidative stress to ageing and lifespan. Bioessays 33, 255-259.
82. Spée, M., Beaulieu, M., Dervaux, A., Chastel, O., Le, Y. and Raclot, T. (2010). Hormones and behavior should I stay or should I go? Hormonal control of nest abandonment in a long-lived bird, the Adélie penguin. Horm. Behav. 58, 762-768.
83. Spée, M., Marchal, L., Thierry, A.-M., Chastel, O., Enstipp, M., Le Maho, Y., Beaulieu, M. and Raclot, T. (2011). Exogenous corticosterone mimics a late fasting stage in captive Adélie penguins (Pygoscelis adeliae). Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R1241-R1249.
84. Speijer, D., Manjeri, G. R. and Szklarczyk, R. (2014). How to deal with oxygen radicals stemming from mitochondrial fatty acid oxidation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130446.
85. Staples, J. F. (2016). Metabolic flexibility: hibernation, torpor, and estivation. Compr. Physiol. 6, 737-771.
86. Stier, A., Reichert, S., Massemin, S., Bize, P. and Criscuolo, F. (2012). Constraint and cost of oxidative stress on reproduction: correlative evidence in laboratory mice and review of the literature. Front. Zool. 9, 37.
87. Stier, A., Bize, P., Schull, Q., Zoll, J., Singh, F., Geny, B., Gros, F., Royer, C., Massemin, S. and Criscuolo, F. (2013). Avian erythrocytes have functional mitochondria, opening novel perspectives for birds as animal models in the study of ageing. Front. Zool. 10, 33.
88. Stier, A., Bize, P., Habold, C., Bouillaud, F., Massemin, S. and Criscuolo, F. (2014a). Mitochondrial uncoupling prevents cold-induced oxidative stress: a case study using UCP1 knockout mice. J. Exp. Biol. 217, 624-630.
89. Stier, A., Massemin, S. and Criscuolo, F. (2014b). Chronic mitochondrial uncoupling treatment prevents acute cold-induced oxidative stress in birds. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 184, 1021-1029.
90. Stonehouse, B. (1960). The king penguin, Aptenodytes patagonica of South Georgia. Sci. Rep. Falkl. Isl. Dep. Surv. 23, 1-81.
91. Szkudelski, T., Okulicz, M., Bialik, I. and Szkudelska, K. (2004). The influence of fasting on liver sulfhydryl groups, glutathione peroxidase and glutathione-S-transferase activities in the rat. J. Physiol. Biochem. 60, 1-6.
92. Vázquez-Medina, J. P., Crocker, D. E., Forman, H. J. and Ortiz, R. M. (2010). Prolonged fasting does not increase oxidative damage or inflammation in postweaned northern elephant seal pups. J. Exp. Biol. 213, 2524-2530.
93. Vázquez-Medina, J. P., Zenteno-Savín, T., Forman, H. J., Crocker, D. E. and Ortiz, R. M. (2011). Prolonged fasting increases glutathione biosynthesis in postweaned northern elephant seals. J. Exp. Biol. 214, 1294-1299.
94. Vázquez-Medina, J. P., Zenteno-Savín, T., Elsner, R. and Ortiz, R. M. (2012). Coping with physiological oxidative stress: a review of antioxidant strategies in seals. J. Comp. Physiol. B 182, 741-750.
95. Viblanc, V. A., Bize, P., Criscuolo, F., Le Vaillant, M., Saraux, C., Pardonnet, S., Gineste, B., Kauffmann, M., Prud'homme, O., Handrich, Y. et al. (2012). Body girth as an alternative to body mass for establishing condition indexes in field studies: a validation in the king penguin. Physiol. Biochem. Zool. 85, 533-542.
96. Von Zglinicki, T. (2000). Role of oxidative stress in telomere length regulation and replicative senescence. Ann. N. Y. Acad. Sci. 908, 99-110.
97. Von Zglinicki, T. (2002). Oxidative stress shortens telomeres. Trends Biochem. Sci. 27, 339-344.
98. Wasselin, T., Zahn, S., Le Maho, Y., Van Dorsselaer, A., Raclot, T. and Bertile, F. (2014). Exacerbated oxidative stress in the fasting liver according to fuel partitioning. Proteomics 14, 1905-1921.
99. Weimerskirch, H., Stahlt, J. C. and Jouventin, P. (1992). The breeding biology and population dynamics of king penguins (Aptenodytes patagonica) on the Crozet Islands. Ibis 134, 107-117.
100. Yun, J. and Finkel, T. (2014). Mitohormesis. Cell Metab. 19, 757-766.
101. Zenteno-Savín, T., Clayton-Hernández, E. and Elsner, R. (2002). Diving seals: are they a model for coping with oxidative stress? Comp. Biochem. Physiol. C Toxicol. Pharmacol. 133, 527-536.
102. Zenteno-Savin, T., St. Leger, J. and Ponganis, P. J. (2010). Hypoxemic and ischemic tolerance in emperor penguins. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 152, 18-23.