Neonatal body condition, immune responsiveness, and hematocrit predict longevity in a wild bird population

Ecology

Volumn 95, Issue 11, 2014, Pages 3027-3034

  Bowers, E Keith ^a   Hodges, Christine J ^a   Forsman, Anna M ^a,c   Vogel, Laura A ^a   Masters, Brian S ^b   Johnson, Bonnie G P ^b   Johnson, L Scott ^b   Thompson, Charles F ^a   Sakaluk, Scott K ^a  

^a ILLINOIS STATE UNIVERSITY   (United States)

^b TOWSON UNIVERSITY   (United States)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

Fitness; Hematocrit; House Wren; Immune response; Neonatal health; Phytohemagglutinin; Recruitment; Survival; Troglodytes aedon

Indexed keywords

BODY CONDITION; FITNESS; IMMUNE RESPONSE; LIFE HISTORY TRAIT; LONGEVITY; NEONATE; PARENT-OFFSPRING INTERACTION; SONGBIRD; SURVIVAL; WILD POPULATION;

AVES; TROGLODYTES; TROGLODYTES AEDON;

EID: 84911901463     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.1890/14-0418.1     Document Type: Article

References (96)

1. Allison, P. D. 2010. Survival analysis using SAS: a practical guide. Second edition. SAS Institute, Cary, North Carolina, USA.
2. Ardia, D. R. 2005a. Individual quality mediates trade-offs between reproductive effort and immune function in tree swallows. Journal of Animal Ecology 74: 517-524.
3. Ardia, D. R. 2005b. Tree Swallows trade off immune function and reproductive effort differently across their range. Ecology 86: 2040-2046.
4. Ardia, D. R. 2005c. Super size me: an experimental test of the factors affecting lipid content and the ability of residual body mass to predict lipid stores in nestling European starlings. Functional Ecology 19: 414-420.
5. Arriero, E., A. Majewska, and T. E. Martin. 2013. Ontogeny of constitutive immunity: maternal vs. Endogenous influences. Functional Ecology 27: 472-478.
6. Bérubé, C. H., M. Festa-Bianchet, and T. Jorgenson. 1999. Individual differences, longevity, and reproductive senescence in bighorn ewes. Ecology 80: 2555-2565.
7. Birchard, G. F. 1997. Optimal hematocrit: theory, regulation and implications. American Zoologist 37: 65-72.
8. Both, C., M. E. Visser, and N. Verboven. 1999. Densitydependent recruitment rates in great tits: the importance of being heavier. Proceedings of the Royal Society B 266: 465-469.
9. Bowers, E. K., S. K. Sakaluk, and C. F. Thompson. 2011. Adaptive sex allocation in relation to hatching synchrony and offspring quality in house wrens. American Naturalist 177: 617-629.
10. Bowers, E. K., S. K. Sakaluk, and C. F. Thompson. 2013. Sibling cooperation influences the age of nest-leaving in an altricial bird. American Naturalist 181: 775-786.
11. Bowers, E. K., R. A. Smith, C. J. Hodges, L. M. Zimmerman, C. F. Thompson, and S. K. Sakaluk. 2012. Sex-biased terminal investment in offspring induced by maternal immune challenge in the house wren (Troglodytes aedon). Proceedings of the Royal Society B 279: 2891-2898.
12. Cam, E., W. A. Link, E. G. Cooch, J.-Y. Monnat, and E. Danchin. 2002. Individual covariation in life-history traits: seeing the trees despite the forest. American Naturalist 159: 96-105.
13. Casto, J. M., V. Nolan, Jr., and E. D. Ketterson. 2001. Steroid hormones and immune function: experimental studies in wild and captive dark-eyed juncos (Junco hyemalis). American Naturalist 157: 408-420.
14. Cichoń, M., and A. Dubiec. 2005. Cell-mediated immunity predicts the probability of local recruitment in nestling blue tits. Journal of Evolutionary Biology 18: 962-966.
15. Clutton-Brock, T. H., M. Major, S. D. Albon, and F. E. Guinness. 1987. Early development and population dynamics in red deer. I. Density-dependent effects on juvenile survival. Journal of Animal Ecology 56: 53-67.
16. Cooke, S. J., J. F. Schreer, D. H. Wahl, and D. P. Philipp. 2010. Cardiovascular performance of six species of field-acclimatized centrarchid sunfish during the parental care period. Journal of Experimental Biology 213: 2332-2342.
17. Dawson, R. D., and G. R. Bortolotti. 1997. Variation in hematocrit and total plasma proteins of nestling American kestrels (Falco sparverius) in the wild. Comparative Biochemistry and Physiology 117A: 383-390.
18. Drilling, N. E., and C. F. Thompson. 1988. Natal and breeding dispersal in House Wrens (Troglodytes aedon). Auk 105: 480-491.
19. Dubiec, A., M. Cichoń, and K. Deptuch. 2006. Sex-specific development of cell-mediated immunity under experimentally altered rearing conditions in blue tit nestlings. Proceedings of the Royal Society B 273: 1759-1764.
20. Fair, J., S. Whitaker, and B. Pearson. 2007. Sources of variation in haematocrit in birds. Ibis 149: 535-552.
21. Forsman, A. M., S. K. Sakaluk, C. F. Thompson, and L. A. Vogel. 2010. Cutaneous immune activity, but not innate immune responsiveness, covaries with mass and environment in nestling house wrens (Troglodytes aedon). Physiological and Biochemical Zoology 83: 512-518.
22. Forsman, A. M., L. A. Vogel, S. K. Sakaluk, B. G. Johnson, B. S. Masters, L. S. Johnson, and C. F. Thompson. 2008. Female house wrens (Troglodytes aedon) increase the size, but not immune responsiveness, of their offspring through extrapair mating. Molecular Ecology 17: 3697-3706.
23. French, S. S., M. D. Dearing, and G. E. Demas. 2011. Leptin as a physiological mediator of energetic trade-offs in ecoimmunology: implications for disease. Integrative and Comparative Biology 51: 505-513.
24. Gaillard, J.-M., M. Festa-Bianchet, D. Delorme, and J. Jorgenson. 2000. Body mass and individual fitness in female ungulates: bigger is not always better. Proceedings of the Royal Society B 267: 471-477.
25. García-Berthou, E. 2001. On the misuse of residuals in ecology: testing regression residuals vs. the analysis of covariance. Journal of Animal Ecology 70: 708-711.
26. Gleeson, D. J., M. W. Blows, and I. P. F. Owens. 2005. Genetic covariance between indices of body condition and immunocompetence in a passerine bird. BMC Evolutionary Biology 5: 61-69.
27. Graham, A. L., A. D. Hayward, K. A. Watt, J. G. Pilkington, J. M. Pemberton, and D. H. Nussey. 2010. Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science 330: 662-665.
28. Green, A. J. 2001. Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82: 1473-1483.
29. Guerreiro, R., A. A. Besson, J. Bellenger, K. Ragot, G. Lizard, B. Faivre, and G. Sorci. 2012. Correlational selection on pro- and anti-inflammatory effectors. Evolution 66: 3615-3623.
30. Hamel, S., S. D. Côté, J.-M. Gaillard, and M. Festa-Bianchet. 2009b. Individual variation in reproductive costs of reproduction: high-quality females always do better. Journal of Animal Ecology 78: 143-151.
31. Hamel, S., J.-M. Gaillard, M. Festa-Bianchet, and S. D. Côté. 2009a. Individual quality, early-life conditions, and reproductive success in contrasted populations of large herbivores. Ecology 90: 1981-1995.
32. Hammond, K. A., M. A. Chappell, R. A. Cardullo, R.-S. Lin, and T. G. Johnsen. 2000. The mechanistic basis of aerobic performance in red junglefowl. Journal of Experimental Biology 203: 2053-2064.
33. Hanson, K. C., and S. J. Cooke. 2009. Nutritional condition and physiology of paternal care in two congeneric species of black bass (Micropterus spp.) relative to stage of offspring development. Journal of Comparative Physiology B 179: 253-266.
34. Hanssen, S. A., D. Hasselquist, I. Folstad, and K. E. Erikstad. 2004. Costs of immunity: immune responsiveness reduces survival in a vertebrate. Proceedings of the Royal Society B 271: 925-930.
35. Hochachka, W., and J. N. M. Smith. 1991. Determinants and consequences of nestling condition in song sparrows. Journal of Animal Ecology 60: 995-1008.
36. Ilmonen, P., T. Taarna, and D. Hasselquist. 2000. Experimentally activated immune defence in female pied flycatchers results in reduced breeding success. Proceedings of the Royal Society B 267: 665-670.
37. Johnson, L. S. 2014. House Wren (Troglodytes aedon). Number 380 in A. Poole, editor. The birds of North America Online. Version 2. Cornell Lab of Ornithology and American Ornithologists' Union, Ithaca, New York, USA.
38. Kilgas, P., V. Tilgar, and R. Mänd. 2006. Hematological health state indices predict local survival in a small passerine bird, the great tit (Parus major). Physiological and Biochemical Zoology 79: 565-572.
39. Knowles, S. C. L., S. Nakagawa, and B. C. Sheldon. 2009. Elevated reproductive effort increases blood parasitaemia and decreases immune function in birds: a meta-regression approach. Functional Ecology 23: 405-415.
40. Lambrechts, M. M., et al. 2010. The design of artificial nestboxes for the study of secondary hole-nesting birds: a review of methodological inconsistencies and potential biases. Acta Ornithologica 45: 1-26.
41. Lee, K. A. 2006. Linking immune defenses and life history at the levels of the individual and the species. Integrative and Comparative Biology 46: 1000-1015.
42. Lee, K. A., M. Wikelski, W. D. Robinson, T. R. Robinson, and K. C. Klasing. 2008. Constitutive immune defences correlated with life-history variables in tropical birds. Journal of Animal Ecology 77: 356-363.
43. Lindén, M., L. Gustafsson, and T. Pärt. 1992. Selection on fledging mass in the Collared Flycatcher and the Great Tit. Ecology 73: 336-343.
44. Lindström, J. 1999. Early development and fitness in birds and mammals. Trends in Ecology and Evolution 14: 343-348.
45. Lochmiller, R. L., and C. Deerenberg. 2000. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88: 87-98.
46. López-Rull, I., P. Celis, C. Salaberria, M. Puerta, and D. Gil. 2011. Post-fledging recruitment in relation to nestling plasma testosterone and immune responsiveness in the spotless starling. Functional Ecology 25: 500-508.
47. Love, O. P., K. G. Salvante, J. Dale, and T. D. Williams. 2008. Sex-specific variability in the immune system across lifehistory stages. American Naturalist 172: E99-E112.
48. Martin, L. B., II, P. Han, J. Kwong, and M. Hau. 2006a. Cutaneous immune activity varies with physiological state in female house sparrows (Passer domesticus). Physiological and Biochemical Zoology 79: 775-783.
49. Martin, L. B., II, P. Han, J. Lewittes, J. R. Kuhlman, K. C. Klasing, and M. Wikelski. 2006b. Phytohemagglutinininduced skin swelling in birds: histological support for a classic immunoecological technique. Functional Ecology 20: 290-299.
50. Martin, L. B., II, A. Scheuerlein, and M. Wikelski. 2003. Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proceedings of the Royal Society B 270: 153-158.
51. Martin, L. B., II, Z. M. Weil, and R. J. Nelson. 2007. Immune defense and reproductive pace of life in Peromyscus mice. Ecology 88: 2516-2528.
52. Martin, L. B., Z. M. Weil, and R. J. Nelson. 2008. Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philosophical Transactions of the Royal Society B 363: 321-339.
53. Martin, T. E., A. P. Moller, S. Merino, and J. Clobert. 2001. Does clutch size evolve in response to parasites and immunocompetence? Proceedings of the National Academy of Sciences USA 98: 2071-2076.
54. Mauck, R. A., K. D. Matson, J. Philipsborn, and R. E. Ricklefs. 2005. Increase in the constitutive innate humoral immune system in Leach's Storm-Petrel (Oceanodroma leucorhoa) chicks is negatively correlated with growth rate. Functional Ecology 19: 1001-1007.
55. Maxwell, M. H., G. W. Robertson, and C. C. McCorquodale. 1992. Whole blood and plasma viscosity values in normal and ascitic broiler chickens. British Poultry Science 33: 871-877.
56. McCleery, R. H., R. A. Pettifor, P. Armbruster, K. Meyer, B. C. Sheldon, and C. M. Perrins. 2004. Components of variance underlying fitness in a natural population of the great tit Parus major. American Naturalist 164: E62-E72.
57. McCorkle, F., I. Olah, and B. Glick. 1980. Morphology of the phytohaemagglutinin-induced cell response in the chicken's wattle. Poultry Science 59: 616-623.
58. McGraw, J. B., and H. Caswell. 1995. Estimation of individual fitness from life-history data. American Naturalist 147: 47-64.
59. Merilä, J., L. E. B. Kruuk, and B. C. Sheldon. 2001. Natural selection on the genetical component of variance in body condition in a wild bird population. Journal of Evolutionary Biology 14: 918-929.
60. Merilä, J., and B. C. Sheldon. 2000. Lifetime reproductive success and heritability in nature. American Naturalist 155: 301-310.
61. Mitchell, G. W., C. G. Guglielmo, N. T. Wheelwright, C. R. Freeman-Gallant, and D. R. Norris. 2011. Early life events carry over to influence pre-migratory condition in a freeliving songbird. PLoS One 6: e28838.
62. Moller, A. P., and N. Saino. 2004. Immune response and survival. Oikos 104: 299-304.
63. Moreno, J., S. Merino, J. J. Sanz, E. Arriero, J. Morales, and G. Tomás. 2005. Nestling cell-mediated immune response, body mass and hatching date as predictors of local recruitment in the pied flycatcher Ficedula hypoleuca. Journal of Avian Biology 36: 251-260.
64. Naef-Daenzer, B., F. Widmer, and M. Nuber. 2001. Differential post-fledging survival of great and coal tits in relation to their condition and fledging date. Journal of Animal Ecology 70: 730-738.
65. Norris, K., and M. R. Evans. 2000. Ecological immunology: life-history trade-offs and immune defense in birds. Behavioral Ecology 11: 19-26.
66. Norte, A. C., J. A. Ramos, P. M. Araújo, J. P. Sousa, and B. C. Sheldon. 2008. Health-state variables and enzymatic biomarkers as survival predictors in nestling Great Tits (Parus major): effects of environmental conditions. Auk 125: 943-952.
67. Nussey, D. H., K. A. Watt, A. Clark, J. G. Pilkington, J. M. Pemberton, A. L. Graham, and T. N. McNeilly. 2014. Multivariate immune defences and fitness in the wild: complex but ecologically important associations among plasma antibodies, health and survival. Proceedings of the Royal Society B 281: 20132931.
68. Ots, I., A. Murumägi, and P. Hõrak. 1998. Haematological health state indices of reproducing great tits: methodology and sources of natural variation. Functional Ecology 12: 700-707.
69. Packard, G. C., and T. J. Boardman. 1988. The misuse of ratios, indices, and percentages in ecophysiological research. Physiological Zoology 61: 1-9.
70. Pirsig, R. M. 1974. Zen and the art of motorcycle maintenance. Bantam Books, New York, New York, USA.
71. Potti, J., J. Moreno, S. Merino, O. Frías, and R. Rodríguez. 1999. Environmental and genetic variation in the haematocrit of fledgling pied flycatchers Ficedula hypoleuca. Oecologia 120: 1-8.
72. Richner, H., A. Oppliger, and P. Christe. 1993. Effect of an ectoparasite on reproduction in great tits. Journal of Animal Ecology 62: 703-710.
73. Ricklefs, R. E., and M. Wikelski. 2002. The physiology/lifehistory nexus. Trends in Ecology and Evolution 17: 462-468.
74. Sadd, B. M., and M. T. Siva-Jothy. 2006. Self-harm caused by an insect's innate immunity. Proceedings of the Royal Society B 273: 2571-2574.
75. SAS Institute. 2011. SAS 9.3. SAS Institute, Cary, North Carolina, USA.
76. Schamber, J. L., D. Esler, and P. L. Flint. 2009. Evaluating the validity of using unverified indices of body condition. Journal of Avian Biology 40: 49-56.
77. Schuler, B., M. Arras, S. Keller, A. Rettich, C. Lundby, J. Vogel, and M. Gassmann. 2010. Optimal hematocrit for maximal exercise performance in acute and chronic erythropoietin- treated mice. Proceedings of the National Academy of Sciences USA 107: 419-423.
78. Schulte-Hostedde, A. I., B. Zinner, J. S. Millar, and G. J. Hickling. 2005. Restitution of mass-size residuals: validating body condition indices. Ecology 86: 155-163.
79. Sheldon, B. C., and S. Verhulst. 1996. Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11: 317-321.
80. Tarwater, C. E., R. E. Ricklefs, J. D. Maddox, and J. D. Brawn. 2011. Pre-reproductive survival in a tropical bird and its implications for avian life histories. Ecology 92: 1271-1281.
81. Tella, J. L., A. Scheuerlein, and R. E. Ricklefs. 2002. Is cellmediated immunity related to the evolution of life-history strategies in birds? Proceedings of the Royal Society B 269: 1059-1066.
82. Thompson, C. F., J. E. C. Flux, and V. T. Tetzlaff. 1993. The heaviest nestlings are not necessarily the fattest nestlings. Journal of Field Ornithology 64: 426-432.
83. Tieleman, I. B., J. B. Williams, R. E. Ricklefs, and K. C. Klasing. 2005. Constitutive innate immunity is a component of the pace-of-life syndrome in tropical birds. Proceedings of the Royal Society B 272: 1715-1720.
84. Tinbergen, J. M., and M. C. Boerlijst. 1990. Nestling weight and survival in individual great tits (Parus major). Journal of Animal Ecology 59: 1113-1127.
85. Tschirren, B., P. S. Fitze, and H. Richner. 2003. Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings. Journal of Animal Ecology 72: 839-845.
86. van Noordwijk, A. J., and G. de Jong. 1986. Acquisition and allocation of resources: their influence on variation in life history tactics. American Naturalist 128: 137-142.
87. Viney, M. E., E. M. Riley, and K. L. Buchanan. 2005. Optimal immune responses: immunocompetence revisited. Trends in Ecology and Evolution 20: 665-669.
88. Vinkler, M., J. Svobodová, B. Gabrielová, H. Bainová, and A. Bryjová. 2014. Cytokine expression in phytohaemagglutinininduced skin inflammation in a galliform bird. Journal of Avian Biology 45: 43-50.
89. Wagner, E. C., C. A. Stables, and T. D. Williams. 2008. Hematological changes associated with egg production: direct evidence for changes in erythropoiesis but a lack of resource dependence? Journal of Experimental Biology 211: 2960-2968.
90. Westneat, D. F., J. Weiskittle, R. Edenfield, T. B. Kinnard, and J. P. Poston. 2004. Correlates of cell-mediated immunity in nestling house sparrows. Oecologia 141: 17-23.
91. Wilcoxen, T. E., R. K. Boughton, and S. J. Schoech. 2010. Selection on innate immunity and body condition in Florida scrub-jays throughout an epidemic. Biology Letters 6: 552-554.
92. Williams, T. D. 2012. Physiological adaptations for breeding in birds. Princeton University Press, Princeton, New Jersey, USA.
93. Williams, T. D., W. O. Challenger, J. K. Christians, M. Evanson, O. Love, and F. Vezina. 2004. What causes the decrease in haematocrit during egg production? Functional Ecology 18: 330-336.
94. Williams, T. D., J. K. Christians, J. J. Aiken, and M. Evanson. 1999. Enhanced immune function does not depress reproductive output. Proceedings of the Royal Society B 266: 753-757.
95. Wilson, A. J., and D. H. Nussey. 2010. What is individual quality? An evolutionary perspective. Trends in Ecology and Evolution 25: 207-214.
96. Young, B. E. 1996. An experimental analysis of small clutch size in tropical house wrens. Ecology 77: 472-488.