Ecological immunology in a fluctuating environment: An integrative analysis of tree swallow nestling immune defense

Ecology and Evolution

Volumn 3, Issue 4, 2013, Pages 1091-1103

  Pigeon, Gabriel ^a   Bélisle, Marc ^a   Garant, Dany ^a   Cohen, Alan A ^a   Pelletier, Fanie ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

Agricultural intensification; Bird; Ecological immunology; Integrated immune score; Performance; Tree swallow

Indexed keywords

EID: 84886286654     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.504     Document Type: Article

References (67)

1. Ardia, D. R. 2007. The ability to mount multiple immune responses simultaneously varies across the range of the tree swallow. Ecography 30:23-30.
2. Arriero, E. 2009. Rearing environment effects on immune defence in blue tit Cyanistes caeruleus nestlings. Oecologia 159:697-704.
3. Baeta, R., M. Bélisle, and D. Garant 2012. Agricultural intensification exacerbates female-biased primary brood sex-ratio in tree swallows. Landscape Ecol. 27:1395-1405.
4. Bates, D., M. Maechler, and B. Bolker 2011. lme4: linear mixed-effects models using S4 classes. R package version 0.999999-0. Available at:http://CRAN.R-project.org/package=lme4.
5. Beldomenico, P. M., S. Telfer, S. Gebert, L. Lukomski, M. Bennett, and M. Begon 2008. The dynamics of health in wild field vole populations: a haematological perspective. J. Anim. Ecol. 77:984-997.
6. Benton, T. G., D. M. Bryant, L. Cole, and H. Q. P. Crick 2002. Linking agricultural practice to insect and bird populations: a historical study over three decades. J. Appl. Ecol. 39:673-687.
7. Blancher, P. J., R. D. Phoenix, D. S. Badzinski, M. D. Cadman, T. L. Crewe, C. M. Downes, et al. 2009. Population trend status of Ontario 's forest birds. Forestry Chronicle 85:184-201.
8. Boughton, R. K., G. Joop, and S. A. O. Armitage 2011. Outdoor immunology: methodological considerations for ecologists. Funct. Ecol. 25:81-100.
9. Buehler, D. M., T., Piersma & B. I., Tieleman 2008. Captive and free-living red knots Calidris canutus exhibit differences in non-induced immunity that suggest different immune strategies in different environments. J. Avian Biol. 39:560-566.
10. Buehler, D. M., M. A. Versteegh, K. D. Matson, and B. I. Tieleman 2011. One problem, many solutions: simple statistical approaches help unravel the complexity of the immune system in an ecological context. PLoS ONE 6:e18592.
11. Chamberlain, D. E., R. J. Fuller, R. G. H. Bunce, J. C. Duckworth, and M. Shrubb 2000. Changes in the abundance of farmland birds in relation to the timing of agricultural intensification in England and Wales. J. Appl. Ecol. 37:771-788.
12. Christe, P., A. P. Møller, and F. de Lope 1998. Immunocompetence and nestling survival in the house martin: the tasty chick hypothesis. Oikos 83:175-179.
13. Cichon, M., and A. Dubiec 2005. Cell-mediated immunity predicts the probability of local recruitment in nestling blue tits. J. Evol. Biol. 18:962-966.
14. Clark, P., W. Boardman, and S. Raidal 2009. Atlas of Clinical Avian Hematology. Oxford, Wiley-Blackwell, Iowa, Ames.
15. Daoust, S. P., J. Savage, T. L. Whitworth, M. Bélisle, and J. Brodeur 2012. Diversity and Abundance of Ectoparasitic Blow FliesProtocalliphora(Diptera: Calliphoridae) and theirNasonia(Hymenoptera: Pteromalidae) Parasitoids in Tree Swallow Nests within Agricultural Lands of Southern Québec, Canada. Ann. Entomol. Soc. Am. 105:471-478.
16. Davis, M. M. 2008. A prescription for human immunology. Immunity 29:835-838.
17. Davis, A. K., D. L. Maney, and J. C. Maerz 2008. The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct. Ecol. 22:760-772.
18. Donald, P. F., F. J. Sanderson, I. J. Burfield, and F. P. J. van Bommel 2006. Further evidence of continent-wide impacts of agricultural intensification on European farmland birds, 1990-2000. Agric. Ecosyst. Environ. 116:189-196.
19. Dray, S. 2007. The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22:1-20.
20. Ghilain, A., and M. Bélisle 2008. Breeding success of tree swallows along a gradient of agricultural intensification. Ecol. Appl. 18:1140-1154.
21. Graham, A. L., J. E. Allen, and A. F. Read 2005. Evolutionary Causes and Consequences of Immunopathology. Annu. Rev. Ecol. Syst. 36:373-397.
22. Hegemann, A., K. D. Matson, C. Both, and B. I. Tieleman 2012. Immune function in a free-living bird varies over the annual cycle, but seasonal patterns differ between years. Oecologia 170:605-618.
23. Hellgren, O., and B. C. Sheldon 2011. Locus-specific protocol for nine different innate immune genes (antimicrobial peptides: beta-defensins) across passerine bird species reveals within-species coding variation and a case of trans-species polymorphisms. Mol. Ecol. Resour. 11:686-692.
24. Johnsen, T. S., and M. Zuk 1999. Parasites and tradeoffs in the immune response of female red jungle fowl. Oikos 86:487-492.
25. Legendre, P., and L., Legendre 1998. Numerical Ecology. 2nd English ed. Elsevier Science, Amsterdam.
26. Legendre, P., J. Oksanen, and C. J. F. ter Braak 2011. Testing the significance of canonical axes in redundancy analysis. Methods Ecol. Evol. 2:269-277.
27. Lochmiller, R. L., and C. Deerenberg 2000. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87-98.
28. Lochmiller, R. L., M. R. Vestey, and J. C. Boren 1993. Relationships between protein nutritional status and immunocompetence in northern bobwhite chicks. Auk 110:503-510.
29. Martin, L. B., P. Han, J. Lewittes, J. R. Kuhlman, K. C. Klasing, and M. Wikelski 2006. Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct. Ecol. 20:290-299.
30. Martin, L. B., D. M. Hawley, and D. R. Ardia 2011. An introduction to ecological immunology. Funct. Ecol. 25:1-4.
31. Matson, K. D., R. E. Ricklefs, and K. C. Klasing 2005. A hemolysis-hemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Dev. Comp. Immunol. 29:275-286.
32. Matson, K. D., A. A. Cohen, K. C. Klasing, R. E. Ricklefs, and A. Scheuerlein 2006a. No simple answers for ecological immunology: relationships among immune indices at the individual level break down at the species level in waterfowl. Proc. Roy. Soc. Lon. Ser. B Biol. Sci. 273:815-822.
33. Matson, K. D., B. I. Tieleman, and K. C. Klasing 2006b. Capture stress and the bactericidal competence of blood and plasma in five species of tropical birds. Physiol. Biochem. Zool. 79:556-564.
34. Maxwell, M. H., and G. W. Robertson 1998. The avian heterophil leucocyte: A review. World Poultry Sci J 54:155-178.
35. McCarty, J. P. 2001. Variation in growth of nestling tree swallows across multiple temporal and spatial scales. Auk 118:176.
36. McCoy, M. W., B. M. Bolker, C. W. Osenberg, B. G. Miner, and J. R. Vonesh 2006. Size correction: comparing morphological traits among populations and environments. Oecologia 148:547-554.
37. Monros, J. S., E. J. Belda, and E. Barba 2002. Post-fledging survival of individual great tits: the effect of hatching date and fledging mass. Oikos 99:481-488.
38. Morrison, E. S., D. R. Ardia, and E. D. Clotfelter 2009. Cross-fostering reveals sources of variation in innate immunity and hematocrit in nestling tree swallows Tachycineta bicolor. J. Avian Biol. 40:573-578.
39. Murphy, M. T. 2003. Avian Population Trends within the Evolving Agricultural Landscape of Eastern and Central United States. Auk 120:20.
40. Nakagawa, S., and R. P. Freckleton 2008. Missing inaction: the dangers of ignoring missing data. Trends Ecol. Evol. 23:592-596.
41. Nebel, S., Mills, A., J. D, McCracken, and P. D. Taylor 2010. Declines of Aerial Insectivores in North America Follow a Geographic Gradient. Avian Conserv. Ecol. 5:1.
42. Neve, L. D., J. J. Soler, M. Ruiz-Rodríguez, D. Martín-Gálvez, T. Pérez-Contreras, and M. Soler 2007. Habitat-specific effects of a food supplementation experiment on immunocompetence in Eurasian Magpie Pica pica nestlings. Ibis 149:763-773.
43. Oksanen, J., F. G., Blanchet, R., Kindt, P., Legendre, P. R., Minchin, R. B., O'Hara, et al. 2012. vegan: community Ecology Package. R package version 2.0-3. http://CRAN.R-project.org/package=vegan.R. package version 2.0-3.
44. Palacios, M. G., J. E. Cunnick, D. Vleck, and C. M. Vleck 2009. Ontogeny of innate and adaptive immune defense components in free-living tree swallows, Tachycineta bicolor. Dev. Comp. Immunol. 33:456-463.
45. Palacios, M. G., J. E. Cunnick, D. W. Winkler, and C. M. Vleck 2012. Interrelations among immune defense indexes reflect major components of the immune system in a free-living vertebrate. Physiol. Biochem. Zool. 85:1-10.
46. Pap, P. L., G. A. Czirjak, C. I. Vagasi, Z. Barta, and D. Hasselquist 2010. Sexual dimorphism in immune function changes during the annual cycle in house sparrows. Naturwissenschaften 97:891-901.
47. Pap, P. L., C. I. Vágási, G. Á. Czirják, A. Titilincu, A. Pintea, G. Osváth, et al. 2011. The Effect of Coccidians on The Condition and Immune profile of Molting House Sparrows (Passer Domesticus). Auk 128:330-339.
48. Piertney, S. B., and M. K. Oliver 2006. The evolutionary ecology of the major histocompatibility complex. Heredity 96:7-21.
49. Pigeon, G., R. Baeta, M. Bélisle, D. Garant, and F. Pelletier In press. Effects of agricultural intensification and temperature on immune response to phytohemagglutinin in tree swallows (Tachycineta bicolor). Can. J. Zool. 56-63.
50. Porlier, M., M. Bélisle, and D. Garant 2009. Non-random distribution of individual genetic diversity along an environmental gradient. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364:1543-1554.
51. R Development Core Team. 2012. R: A Language and Environment for Statistical Computing. 2.15.0 ed. R Foundation for Statistical Computing, Vienna, Austria.
52. Raberg, L., and M. Stjernman 2003. Natural selection on immune responsiveness in blue tits Parus caeruleus. Evolution 57:1670-1678.
53. Rioux Paquette, S., D. Garant, F. Pelletier, and M. Bélisle In press. Seasonal patterns in tree swallow prey (Diptera) abundance are affected by agricultural intensification. Ecol. Appl.
54. Robillard, A., D. Garant, and M. Bélisle 2012. The Swallow and the Sparrow: how agricultural intensification affects abundance, nest site selection and competitive interactions. Landscape Ecol. 1-15.
55. Sadd, B. M., and M. T. Siva-Jothy 2006. Self-harm caused by an insect's innate immunity. Proc. Roy. Soc. Lon. Ser. B Biol. Sci. 273:2571-2574.
56. Saino, N., M. Romano, R. Ambrosini, R. P. Ferrari, and A. P. Moller 2004. Timing of reproduction and egg quality covary with temperature in the insectivorous Barn Swallow, Hirundo rustica. Funct. Ecol. 18:50-57.
57. Segel, L. A., and I. R. Cohen 2001. Design principles for the immune system and other distributed autonomous systems. Oxford University Press, New York.
58. Siva-Jothy, M. T., and J. J. W. Thompson 2002. Short-term nutrient deprivation affects immune function. Physiol. Entomol. 27:206-212.
59. Sokal, R. R., and F. J. Rohlf 1994. Biometry: The Principles and Practice of Statistics in Biological Research. W.H. Freeman & Company, New York.
60. Soler, J. J., J. M. Peralta-Sanchez, E. Flensted-Jensen, A. M. Martin-Platero, and A. P. Moller 2011. Innate humoural immunity is related to eggshell bacterial load of European birds: a comparative analysis. Naturwissenschaften 98:807-813.
61. Thomas, D. W., B. Shipley, J. Blondel, P. Perret, A. Simon, and M. M. Lambrechts 2007. Common paths link food abundance and ectoparasite loads to physiological performance and recruitment in nestling blue tits. Funct. Ecol. 21:947-955.
62. Tieri, P., A. Grignolio, A. Zaikin, M. Mishto, D. Remondini, G. C. Castellani, et al. 2010. Network, degeneracy and bow tie integrating paradigms and architectures to grasp the complexity of the immune system. Theor. Biol. Med. Model. 7:32.
63. Toma, S., L. Cornegliani, P. Persico, and C. Noli 2006. Comparison of 4 fixation and staining methods for the cytologic evaluation of ear canals with clinical evidence of ceruminous otitis externa. Vet. Clin. Path. J 35:194-198.
64. Viney, M. E., E. M. Riley, and K. L. Buchanan 2005. Optimal immune responses: immunocompetence revisited. Trends Ecol. Evol. 20:665-669.
65. Vinkler, M., H. Bainová, and T. Albrecht 2010. Functional analysis of the skin-swelling response to phytohaemagglutinin. Funct. Ecol. 24:1081-1086.
66. Winkler, D. W., K. K. Hallinger, D. R. Ardia, R. J. Robertson, B. J. Stutchbury, and R. R. Cohen 2011. Tree Swallow (Tachycineta bicolor). in A. Poole, ed. The birds of North America online. Cornell lab of ornithology, Ithaca, New York. Available at:http://bna.birds.cornell.edu/bna/species/011.
67. Wolak, M. E., D. J. Fairbairn, and Y. R. Paulsen 2012. Guidelines for estimating repeatability. Methods Ecol. Evol. 3:129-137.