Radical health: Ecological corollaries of body condition, transport stress and season on plasma antioxidant capacity in the European badger

Journal of Zoology

Volumn 284, Issue 2, 2011, Pages 114-123

  Montes, I ^a   Newman, C ^a   Mian, R ^b   Macdonald, D W ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Oxford MediStress Ltd   (United Kingdom)

Author keywords

Antioxidant; Body condition; European badger; Oxidative stress; ROS; Vitamin E

Indexed keywords

ANTIOXIDANT; BLOOD; BODY CONDITION; CLIMATE CHANGE; DEFENSE MECHANISM; ENVIRONMENTAL STRESS; FAT; FEEDING ECOLOGY; IMMUNOASSAY; INDIVIDUAL VARIATION; MUSTELID; PHYSIOLOGICAL RESPONSE; SEASONAL VARIATION; VITAMIN; WILD POPULATION;

ANIMALIA; MELES MELES; TAXIDIINAE;

EID: 79956123777     PISSN: 09528369     EISSN: 14697998     Source Type: Journal    
DOI: 10.1111/j.1469-7998.2010.00787.x     Document Type: Article

References (100)

1. Anwar, M.A., Knaggs, J., Service, K., Riordan, P., McLaren, G.W., Newman, C., Cheesman, C. & Macdonald, D.W. (2006). The presence of antibodies to Toxoplasma gondii in European badgers (Meles meles). J. Wildl. Dis. 42, 179-181.
2. Anwar, M.A., Newman, C., Macdonald, D.W., Woolhouse, M.E.J. & Kelly, D.W. (2000). Coccidiosis in the European badger (Meles meles) from England, an epidemiological study. Parasitology 120, 255-260.
3. Balaban, R.S., Nemoto, S. & Finkel, T. (2005). Mitochondria, oxidants, and aging. Cell 120, 483-495.
4. Bateson, P. & Bradshaw, E.L. (1997). Physiological effects of hunting red deer (Cervus elaphus). Proc. Roy. Soc. Lond. B Biol. Sci. 264, 1707-1714.
5. Beaulieu, M., Ropert-Coudert, Y., Maho, Y.L., Ancel, A. & Criscuolo, F. (2009). Foraging in an oxidative environment: relationship between δ13C values and oxidative status in Adélie penguins. Proc. Roy. Soc. Lond. B Biol. Sci. 277, 1087-1092.
6. Bevanger, K. & Lindstom, E.K. (1995). Distributional history of the European badger Meles meles in Scandinavia during the 20th century. Ann. Zool. Fenn. 32, 5-9.
7. Bonacic, C. & Macdonald, D.W. (2003). The physiological impact of wool hravesting procedures in vicuñas (Vicugna vicugna). Anim. Welf. 12, 387-402.
8. Bonacic, C., Macdonald, D.W. & Villouta, G. (2003). Adrenocorticotrophin-induced stress response of captive vicuñas (Vicugna vicugna) in the Andes of Chilie. Anim. Welf. 12, 365-387.
9. Bouché, M.B. (1977). Stratégies lombriciennes. In Soil organisms as components of ecosystems. Ecological bulletins (Stockholm) 25, 122-286.
10. Buchner, A., Erdfelde, E. & Faul, F. (1997) How to use G Power. Available at (1 June 2008).
11. Buesching, C.D., Heistermann, M. & Macdonald, D.W. (2009). Seasonal and inter-individual variation in testosterone levels in badgers Meles meles: evidence for the existence of two endocrinological phenotypes. J. Comp. Physiol. A Sens. Neural. Behav. Physiol. 195, 865-871.
12. Cannon, W.B. (1929). Bodily changes in pain, hunger, fear and rage: an account of recent research into the function of emotional excitement, 2nd edn. New York: Appleton-Century-Crofts.
13. Carr, G.M. & Macdonald, D.W. (1986). The sociality of solitary foragers - a model based on resource dispersion. Anim. Behav. 34, 1540-1549.
14. Catoni, C., Peters, A. & Schaefer, H.M. (2008). Life-history trade-offs are influenced by the diversity, availability and interactions of dietary antioxidants. Anim. Behav. 76, 1107-1119.
15. Cleary, G.P., Corner, L.A.L., O'Keeffec, J. & Marples, N.M. (2009). The diet of the badger Meles meles in the republic of Ireland. Mamm. Biol. 74, 438-445.
16. Cohen, A.A. & McGraw, K.J. (2009). No simple measures for antioxidant status in birds: complexity in inter- and intraspecific correlations among circulating antioxidant types. Funct. Ecol. 23, 210-220.
17. Cohen, A.A., McGraw, K.J. & Robinson, W.D. (2009). Serum antioxidant levels in wild birds vary in relation to diet, season, life history strategy, and species. Oecologia (Heidelb.) 161, 673-683.
18. Cook, C.J., Mellor, D.J., Harris, P.J., Ingram, J.R. & Mathews, L.R. (2000). Hands-on and hands-off measurement of stress. In The Biology of animal stress principles and implications for animal welfare: 123-146. Moberg, G.P. & Mench, J.A. (Eds). Oxfordshire: CABI Publishing.
19. Costantini, D. (2008). Oxidative stress in ecology and evolution: lessons from avian studies. Ecol. Lett. 11, 1231-1258.
20. Costantini, D., Cardinale, M. & Carere, C. (2007). Oxidative damage and anti-oxidant capacity in two migratory bird species at a stop-over site. Comp. Biochem. Physiol. C 144, 363-371.
21. Costantini, D., Dell'Ariccia, G. & Lipp, H-P. (2008). Long flights and age affect oxidative status of homing pigeons (Columba livia). J. Exp. Biol. 211, 377-381.
22. Costantini, D., Rowe, M., Butler, M.W. & McGraw, K.J. (2010). From molecules to living systems: historical and contemporary issues in oxidative stress and antioxidant ecology. Funct. Ecol. 24, 950-959.
23. Davies, K. (1995). Oxidative stress: the paradox of aerobic life. Biochem. Soc. Symp. 61, 1-31.
24. Davies, M.J., Forni, L.G. & Willson, R.L. (1988). Vitamin E analogue Trolox C. E.s.r. and pulse-radiolysis studies of free-radical reactions. Biochem. J. 255, 513-522.
25. Dawkins, M.S. (2004). Using behaviour to assess animal welfare. Anim. Welf. 13, S3-S7.
26. De Kloet, E.R., Joëls, M. & Holsboer, F. (2005). Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 6, 463-475.
27. Domingo-Roura, X., Newman, C., Calafell, F. & Macdonald, D.W. (2001). Blood biochemistry reflects seasonal nutritional and reproductive constraints in the Eurasian badger (Meles meles). Physiol. Biochem. Zool. 74, 450-460.
28. Edwards, C.A. & Bohlen, P.J. (1996). Biology and ecology of earthworms, 3rd edn. London: Chapman & Hall.
29. Faul, F. & Erdfelder, E. (1992). GPOWER: A priori-, post hoc-, and compromise power analyses for MS-DOS [computer program]. Bonn: Bonn University.
30. Fearon, D.T. & Locksley, R.M. (1996). The instructive role of innate immunity in the acquired immune response. Science 272, 50-54.
31. Flajnik, M.F. & Du Plasquier, L. (2004). Evolution of innate and adaptive immunity: can we draw a line? Trend Immunol. 25, 640-644.
32. Fontagne, S., Lataillade, E., Breque, J. & Kaushik, S. (2008). Lipid peroxidative stress and antioxidant defence status during ontogeny of rainbow trout (Oncorhynchas mykiss). Br. J. Nutr. 100, 102-111.
33. Fowler, P.A. & Racey, P.A. (1988). Overwintering strategies of the badger, Meles meles, at 57-degrees-n. J. Zool. (Lond.) 214, 635-651.
34. Fragoso, C. & Lavelle, P. (1992). Earthworm communities of tropical rain forests. Soil Biol. Biochem. 24, 1397-1408.
35. Gelling, M., Montes, I., Moorhouse, T.P. & Macdonald, D.W. (2010). Captive housing during water vole (Arvicola terrestris) reintroduction: does short-term social stress impact on animal welfare? PLoS ONE 5, e9791, doi:DOI: 10.1371/journal.pone.0009791.
36. Gerard, B.M. (1967). Factors affecting earthworms in pastures. J. Anim. Ecol. 36, 235-252.
37. Grandin, T. (1997). Assessment of stress during handling and transport. J. Anim. Sci. 75, 249-257.
38. Hofer, H. (1988). Variation in resource presence, utilization and reproductive success within a population of European badgers (Meles meles). Mammal. Rev. 18, 25-36.
39. Huang, D., Ou, B. & Prior, R. (2005). The chemistry behind antioxidant capacity assays. J. Agric. Food Chem. 53, 1841-1856.
40. IPCC. (2007). Climate change 2007: synthesis report. Contribution of working groups I, II and III to the fourth assessment report of the intergovernmental panel on climate change. Geneva: IPCC.
41. Johnson, D.D.P., Jetz, W. & Macdonald, D.W. (2002a). Environmental correlates of badger social spacing across Europe. J. Biogeogr. 29, 411-425.
42. Johnson, D.D.P., Kays, R., Blackwell, P.G. & Macdonald, D.W. (2002b). Does the resource dispersion hypothesis explain group living? Trends Ecol. Evol. 17, 563-570.
43. Kauhala, K. (1995a). Mayran levinneisyys ja runsaus Suomessa. Suom. Riista 41, 85-94.
44. Kauhala, K. (1995b). Distributional history of the European badger Meles meles in Scandinavia during the 20th Century. Ann. Zool. Fenn. 32, 183-191.
45. Kruuk, H. (1978a). Foraging and spatial organisation of the European badger, Meles meles L. Behav. Ecol. Sociobiol. 4, 75-89.
46. Kruuk, H. (1978b). Spatial-organization and territorial behavior of European badger Meles meles. J. Zool. (Lond.) 184, 1-19.
47. Kruuk, H. (1989). The social badger: ecology and behaviour of a group-living carnivore (Meles meles). Oxford: Oxford University Press.
48. Kruuk, H. & Parish, T. (1981). Feeding specialization of the European badger Meles meles in Scotland. J. Anim. Ecol. 50, 773-788.
49. Kruuk, H. & Parish, T. (1985). Food, food availability and weight of badgers (Meles meles) in relation to agricultural changes. J. Appl. Ecol. 22, 705-715.
50. Laugero, K.D. & Moberg, G.P. (2000). Energetic response to repeated stress in rapidly growing mice. Am J Physiol - Endocrinol. Metab. 279, E33-E43.
51. Lester, P. (2001). Molecular aspects of α-tocotrienol antioxidant action and cell signalling. J. Nutr. 131, 369-373.
52. Macdonald, D.W. (1980). The red fox, Vulpes vulpes, as a predator upon earthworms, Lumbricus terrestris. Z. Tierpsychol. 52, 171-200.
53. Macdonald, D.W. (1983). Predation on earthworms by terrestrial carnivores. In Earthworm ecology: 393-414. Satchell, J.E. (Ed.) London: Chapman & Hall.
54. Macdonald, D.W., Anwar, M., Newman, C., Woodroffe, R. & Johnson, P.J. (1999). Inter-annual differences in the age-related prevalences of Babesia and Trypanosoma parasites of European badgers (Meles meles). J. Zool. (Lond.) 247, 65-70.
55. Macdonald, D.W. & Newman, C. (2002). Population dynamics of badgers (Meles meles) in Oxfordshire, UK: numbers, density and cohort life histories, and a possible role of climate change in population growth. J. Zool. (Lond.) 256, 121-138.
56. Macdonald, D.W., Newman, C., Buesching, C.D. & Johnson, P.J. (2008). Male-biased movement in a high-density population of the Eurasian badger (Meles meles). J. Mammal. 89, 1077-1086.
57. Macdonald, D.W., Newman, C., Buesching, C.D. & Nouvellet, P. (2010). Are badgers 'under the weather'? Direct and indirect impacts of weather variability on European badgers (Meles meles) population dynamics. Glob. Change Biol. 16, 2913-2922.
58. Macdonald, D.W., Newman, C., Dean, J., Buesching, C.D. & Johnson, P.J. (2004). The distribution of Eurasian badger, Meles meles, setts in a high-density area: field observations contradict the sett dispersion hypothesis. Oikos 106, 295-307.
59. Macdonald, D.W., Newman, C., Nouvellet, P. & Buesching, C.D. (2009). Mechanisms for population regulation and the role of density-dependence in the demographics of the Eurasian badger, Meles meles: matrix models applied to a long-term population study. J. Mammal. 90, 1392-1403.
60. Macdonald, D.W., Newman, C., Stewart, P.D., Domingo-Roura, X. & Johnson, P.J. (2002). Density-dependent regulation of body mass and condition in badgers (Meles meles) from Wytham woods. Ecology 83, 2056-2061.
61. Matés, J.M. & Sánchez-Jiménez, F. (1999). Antioxidant enzymes and their implications in pathophysiologic processes. Front. Biosci. 4, 339-345.
62. Mathews, F., Lovett, L., Rushton, S. & Macdonald, D.W. (2006a). Bovine tuberculosis in cattle: reduced risk on wildlife-friendly farms. Biol. Lett. 2, 271-274.
63. Mathews, F., Macdonald, D.W., Taylor, G.M., Gelling, M., Norman, R.A., Honess, P.E., Foster, R., Gower, C.M., Varley, S., Harris, A., Palmer, S., Hewinson, G. & Webster, J.P. (2006b). Bovine tuberculosis (Mycobacterium bovis) in British farmland wildlife: the importance to agriculture. Proc. Roy. Soc. Lond. B Biol. Sci. 273, 357-365.
64. McGraw, K.J., Cohen, A.A., Costantini, D. & Hõrak, P. (2010). The ecological significance of antioxidants and oxidative stress: a marriage between mechanistic and functional perspectives. Funct. Ecol. 24, 947-949.
65. McGraw, K.J., Hill, G.E. & Parker, R.S. (2005). The physiological costs of being colourful: nutritional control of carotenoid utilization in the American goldfinch, Carduelis tristis. Anim. Behav. 69, 653-660.
66. McLaren, G., Bonacic, C. & Rowan, A. (2007). Animal welfare and conservation. In Key topics in conservation biology: 120-133. Macdonald, D. & Service, K. (Eds). Oxford: Blackwells Publishing Ltd.
67. McLaren, G.W., Macdonald, D.W., Georgiou, C., Mathews, F., Newman, C. & Mian, R. (2003). Leukocyte coping capacity: a novel technique for measuring the stress response in vertebrates. Exp. Physiol. 88, 541-546.
68. McLaren, G.W., Mathews, F., Fell, R., Gelling, M. & Macdonald, D.W. (2004). Body weight change as a measure of stress: a practical test. Anim. Welf. 13, 337-341.
69. Moberg, G.P. (2000). Suffering from stress: an approach for evaluating the welfare of an animal. Acta Agric. Scand. Sect. A - Anim. Sci. 27, 46-49.
70. Monaghan, P., Metcalfe, N.B. & Torres, R. (2009). Oxidative stress as a mediator of life history trade-offs: mechanisms, measurement and interpretation. Ecol. Lett. 12, 75-92.
71. Montero, D., Tor, L., Robaina, L., Vergara, J.M. & Izquierdo, M.S. (2001). Low vitamin E in diet reduces stress resistance of gilthead seabream Sparus aurata juveniles. Fish Shellfish Immunol. 11, 473-490.
72. Montes, I., McLaren, G.W., Macdonald, D.W. & Mian, R. (2003). The effects of acute stress on leukocyte activation. J. Physiol. 54P, 88P.
73. Montes, I., Mclaren, G.W., Macdonald, D.W. & Mian, R. (2004). The effect of transport stress on leukocyte activation in wild badgers. Anim. Welf. 13, 355-359.
74. Neal, E.G. & Cheeseman, C.L. (1996). Badgers. London: Poyser.
75. Newman, C., Buesching, C.D. & Macdonald, D.W. (2004). First report of Cheyletiella parasitovorax infestation in the Eurasian badger. Vet. Rec. 155, 180-181.
76. Newman, C., Macdonald, D.W. & Anwar, M.A. (2001). Coccidiosis in the European badger, Meles meles in Wytham woods: infection and consequences for growth and survival. Parasitology 123, 133-142.
77. Nourooz-Zadeh, J., Ziegler, D., Sohr, C., Betteridge, JD., Knight, J. & Hothersall, J. (2006). The use of pholasin as a probe for the determination of plasma total antioxidant capacity. Clin. Biochem. 39, 55-61.
78. Nutrient Data Laboratory. (2007). Oxygen Radical Absorbance Capacity (ORAC) of selected foods - 2007. Washington, DC: Agriculture Research Service, US Department of Agriculture.
79. Papas, A.M. (1999). Antioxidant status, diet and health. Boca Raton: CRC Press.
80. Podmore, I.D., Griffiths, H.R., Herbert, K.E., Mistry, N., Mistry, P. & Lunec, J. (1998). Vitamin C exhibits pro-oxidant properties. Nature 392, 559-559.
81. Prakash, M., Balamurgan, M., Parthasarath, K., Gunasekaren, G., Coper, E.L. & Ranganathan, L.S. (2007). Anti-ulceral and anti-oxidative properties of earthworm paste of Lampito mauritii Kinberg on Rattus norvegicus. Eur. Rev. Med. Pharmacol. Sci. 11, 9-15.
82. Prakash, M., Gunasekaran, G. & Elumalai, K. (2008). Effect of earthworm powder on antioxidant enzymes in alcohol induced hepatotoxic rats. Eur. Rev. Med. Pharmacol. Sci. 12, 237-243.
83. Punchard, N.A. & Kelly, F.J. (Eds) (1996). Free radicals a practical approach. Oxford: IRL Press.
84. Re, R., Pellegrini, N., Pannala, A., Yang, M. & Rice-Evans, C. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic. Biol. Med. 26, 1231-1237.
85. Reiter, R.J., Tan, D-X., Osuna, C. & Gitto, E. (2005). Actions of melatonin in the reduction of oxidative stress: a review. J. Biomed. Sci. 7, 444-458.
86. Rogers, L.M., Cheeseman, C.L. & Langton, S. (1997). Body weight as an indication of density-dependent regulation in badgers (Meles meles) at Woodchester Park, Gloucestershire. J. Zool. (Lond.) 242, 597-604.
87. Rhee, S.G. (2006). Cell signaling. H2O2, a necessary evil for cell signaling. Science 312, 1882-1883.
88. Savill, P.S., Perrins, C.M. & Fisher, N. (Eds) (2010). Wytham Woods: Oxford's Ecological Laboratory. Oxford: Oxford University Press.
89. Selman, C., McLaren, J.S., Meyer, C., Duncan, J.S., Redman, P. & Collins, A.R., et al. (2006). Life-long vitamin C supplementation in combination with cold exposure does not affect oxidative damage or lifespan in mice, but decreases expression of antioxidant protection genes. Mech. Ageing Dev. 127, 897-904.
90. Seyle, H. (1936). A syndrome produced by diverse nocuous agents. Nature 138, 32.
91. Sies, H. (1997). Oxidative stress: oxidants and antioxidants. Exp. Physiol. 82, 291-295.
92. Shelton-Rayner, G., Mian, R., Chandler, S., Robertso, D. & Macdonald, D.W. (2010). Quantitative physiological assessment of mental loading via altered immune functioning following interaction with differing automotive interface technologies. Cell Immunol. 263, 22-30.
93. da Silva, J., Woodroffe, R. & Macdonald, D.W. (1993). Habitat, food availability and group territoriality in the European badger, Meles meles. Oecologia (Hiedlb.) 95, 558-564.
94. Speedy, A.W. & Clark, C.F. (1981). Lowland sheep: the nutrition and management cycle. Vet. Rec. 108, 493-496.
95. Stanner, S.A., Hughes, J., Kell, C.N. & Buttriss, J. (2004). A review of the epidemiological evidence for the 'antioxidant hypothesis'. Public Health Nutr. 7, 407-422.
96. Surai, P.F. (2002). Natural antioxidants in avian nutrition and reproduction. Nottingham: Nottingham University Press.
97. Trites, A.W. & Donnelly, C.P. (2003). The decline of Steller sea lions Eumetopias jubatus in Alaska: a review of the nutritional stress hypothesis. Mammal. Rev. 33, 3-28.
98. Tuyttens, F.A.M., Macdonald, D.W. & Roddam, A.W. (2002). Effects of radio-collars on European badgers (Meles meles). J. Zool. (Lond.) 257, 37-42.
99. Woodroffe, R., Macdonald, D.W. & Cheeseman, C.L. (1997). Endocrine correlates of contrasting male mating strategies in the European badger, Meles meles. J. Zool. (Lond.) 241, 291-300.
100. Zhou, J., Yan, X.L., Ryan, D.H. & Harris, R.B.S. (1999). Sustained effects of repeated restraint stress on muscle and adipocyte metabolism in high-fat-fed rats. Am. J. Physiol. - Regul. Integr. Comp. Physiol. 277, R757-R766.