Common measures of immune function vary with time of day and sampling protocol in five passerine species

Journal of Experimental Biology

Volumn 218, Issue 5, 2015, Pages 757-766

  Zylberberg, Maxine ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Complement; Ecological immunology; Innate immune function; Lysozyme acute phase protein; Natural antibodies; Passerines; PIT54 acute phase protein

Indexed keywords

ANTIBODY; LYSOZYME;

ADAPTATION; ANIMAL; BLOOD; CIRCADIAN RHYTHM; HEMOLYSIS; IMMUNOLOGY; INNATE IMMUNITY; PASSERIFORMES; PHYSIOLOGICAL STRESS; SPECIES DIFFERENCE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTIBODIES; BLOOD; CIRCADIAN RHYTHM; HEMOLYSIS; IMMUNITY, INNATE; IMMUNOLOGY; MURAMIDASE; PASSERIFORMES; SPECIES SPECIFICITY; STRESS, PHYSIOLOGICAL;

PASSERIFORMES;

EID: 84964253063     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.111716     Document Type: Article

References (48)

1. Ardia, D. R., Schat, K. A. and Winkler, D. W. (2003). Reproductive effort reduces long-term immune function in breeding tree swallows (Tachycineta bicolor). Proc. R. Soc. Lond. B Biol. Sci. 270, 1679-1683.
2. Boughton, R. K., Joop, G. and Armitage, S. A. O. (2011). Outdoor immunology: methodological considerations for ecologists. Funct. Ecol. 25, 81-100.
3. Braude, S., Tang-Martinez, Z. and Taylor, G. T. (1999). Stress, testosterone, and the immunoredistribution hypothesis. Behav. Ecol. 10, 345-350.
4. Breuner, C. W., Wingfield, J. C. and Romero, L. M. (1999). Diel rhythms of basal and stress-induced corticosterone in a wild, seasonal vertebrate, Gambels whitecrowned sparrow. J. Exp. Zool. A Comp. Exp. Biol. 284, 334-342.
5. Buehler, D. M., Bhola, N., Barjaktarov, D., Goymann,W., Schwabl, I., Tieleman, I. and Piersma, T. (2008). Constitutive immune function responds more slowly to handling stress than corticosterone in a shorebird. Physiol. Biochem. Zool. 81, 673-681.
6. Caroll, M. C. and Prodeus, A. P. (1998). Linkages of innate and adaptive immunity. Curr. Opin. Immunol. 10, 36-40.
7. Casali, P. and Schettino, E.W. (1996). Structure and function of natural antibodies. Curr. Top. Microbiol. Immunol. 210, 167-179.
8. Davis, A. K. (2005). Effect of handling time and repeated sampling on avian white blood cell counts. J. Field Ornithol. 76, 334-338.
9. Day, T., Graham, A. L. and Read, A. F. (2007). Evolution of parasite virulence when host responses cause disease. Proc. R. Soc. B Biol. Sci. 274, 2685-2692.
10. Dhabhar, F. S. and McEwen, B. S. (1997). Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leukocyte trafficking. Brain Behav. Immun. 11, 286-306.
11. Dickstein, G., Shechner, C., Nicholson,W. E., Rosner, I., Shen-Orr, Z., Adawi, F. and Lahav, M. (1991). Adrenocorticotropin stimulation test: effects of basal cortisol level, time of day, and suggested new sensitive low dose test. J. Clin. Endocrinol. Metabol. 72, 773-778.
12. Fratto, M., Ezenwa, V. O. and Davis, A. K. (2014). Infection with mycoplasma gallisepticum buffers the effects of acute stress on innate immunity in house finches. Physiol. Biochem. Zool. 87, 257-264.
13. Haine, E. R., Moret, Y., Siva-Jothy, M. T. and Rolff, J. (2008). Antimicrobial defense and persistent infection in insects. Science 322, 1257-1259.
14. Hangalapura, B. N., Nieuwland, M. G., Reilingh, G. D. V., Heetkamp, M. J., van den Brand, H., Kemp, B. and Parmentier, H. K. (2003). Effects of cold stress on immune responses and body weight of chicken lines divergently selected for antibody responses to sheep red blood cells. Poult. Sci. 82, 1692-1700.
15. Hangalapura, B. N., Nieuwland, M. G., Reilingh, G. D. V., Buyse, J., Van Den Brand, H., Kemp, B. and Parmentier, H. K. (2005). Severe feed restriction enhances innate immunity but suppresses cellular immunity in chicken lines divergently selected for antibody responses. Poult. Sci. 84, 1520-1529.
16. Hawley, D. M., Lindström, K. and Wikelski, M. (2006). Experimentally increased social competition compromises humoral immune responses in house finches. Horm. Behav. 49, 417-424.
17. Hirsch, R. L. (1982). The complement system: its importance in the host response to viral infection. Microbiol. Mol. Biol. Rev. 46, 71-85.
18. Hoye, B. J. (2012). Variation in postsampling treatment of avian blood affects ecophysiological interpretations. Methods Ecol. Evol. 3, 162-167.
19. Janeway, C. A., Travers, P., Walport, M. and Shlomchik, M. (2001). Immunobiology. New York: Garland Science.
20. Janssens, C. J. J. G., Helmond, F. A. and Weigant, V. M. (1995). The effect of chronic stress on plasma cortisol concentrations in cyclic female pigs depends on the time of day. Domest. Anim. Endocrinol. 12, 167-177.
21. Klasing, K. C. (1998). Nutritional modulation of resistance to infectious diseases. Poult. Sci. 77, 1119-1125.
22. Koenen, M. E., Boonstra-Blom, A. G. and Jeurissen, S. H. M. (2002). Immunological differences between layer- and broiler-type chickens. Vet. Immunol. Immunopathol. 89, 47-56.
23. Korner, P. and Schmid-Hempel, P. (2004). In vivo dynamics of an immune response in the bumble bee Bombus terrestris. J. Invertebr. Pathol. 87, 59-66.
24. Lee, K. A. and Klasing, K. C. (2004). A role for immunology in invasion biology. Trends Ecol. Evol. 19, 523-529.
25. Lee, K. P., Cory, J. S., Wilson, K., Raubenheimer, D. and Simpson, S. J. (2006). Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc. R. Soc. B Biol. Sci. 273, 823-829.
26. Martin, L. B. (2009). Stress and immunity in wild vertebrates: timing is everything. Gen. Comp. Endocrinol. 163, 70-76.
27. Martin, L. B., Scheuerlein, A. and Wikelski, M. (2003). Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc. R. Soc. Biol. Sci. Ser. B 270, 153-158.
28. Matson, K. D., Ricklefs, R. E. and Klasing, K. C. (2005). A hemolysishemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Dev. Comp. Immunol. 29, 275.
29. Matson, K. D., Tieleman, B. I. and Klasing, K. C. (2006). Capture stress and the bactericidal competence of blood and plasma in five species of tropical birds. Physiol. Biochem. Zool. 79, 556-564.
30. Millet, S., Bennett, J., Lee, K. A., Hau, M. and Klasing, K. C. (2007). Quantifying and comparing constitutive immunity across avian species. Dev. Comp. Immunol. 31, 188-201.
31. Norris, K. and Evans, M. R. (2000). Ecological immunology: life history trade-offs and immune defense in birds. Behav. Ecol. 11, 19-26.
32. Owen-Ashley, N. T. and Wingfield, J. C. (2007). Acute phase responses of passerine birds: characterization and seasonal variation. J. Ornithol. 148, 583-591.
33. Quaye, I. K. (2008). Haptoglobin, inflammation and disease. Trans. R. Soc. Trop. Med. Hyg. 102, 735-742.
34. R Core Team. (2014). R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing
35. Raberg, L., Grahn, M., Hasselquist, D. and Svensson, E. (1998). On the adaptive significance of stress-induced immunosuppression. Proc. R. Soc. Lond. B Biol. Sci. 265, 1637-1641.
36. Rich, E. L. and Romero, L.M. (2001). Daily and photoperiod variations of basal and stress-induced corticosterone concentrations in house sparrows (Passer domesticus). J. Comp. Physiol. B 171, 543-547.
37. Ricklefs, R. E. and Wikelski, M. (2002). The physiology/life-history nexus. Trends Ecol. Evol. 17, 462-468.
38. Romero, L. M. and Reed, J. M. (2005). Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp. Biochem. Physiol. A Mol. Integr. Physiol. 140, 73-79.
39. Sadd, B. M. and Siva-Jothy, M. T. (2006). Self-harm caused by an insects innate immunity. Proc. R. Soc. B Biol. Sci. 273, 2571-2574.
40. Wicher, K. B. and Fries, E. (2006). Haptoglobin, a hemoglobin-binding plasma protein, is present in bony fish and mammals but not in frog and chicken. Proc. Natl. Acad. Sci. USA 103, 4168-4173.
41. Wickham, H. (2009). Ggplot2: Elegant Graphics for Data Analysis. New York: Springer.
42. Wingfield, J. C., OReilly, K. M. and Astheimer, L. B. (1995). Modulation of the adrenocortical responses to acute stress in arctic birds: a possible ecological basis. Am. Zool. 35, 285-294.
43. Wingfield, J. C., Maney, D. L., Breuner, C. W., Jacobs, J. D., Lynn, S., Ramenofsky, M. and Richardson, R. D. (1998). Ecological bases of hormone- behavior interactions: the emergency life history stage. Am. Zool. 38, 191-206.
44. Zylberberg, M. (2014). Galapagos ground finches balance investment in behavioural and immunological pathogen defences. Ibis 156, 615-626.
45. Zylberberg, M., Lee, K. A., Klasing, K. C. and Wikelski, M. (2012). Increasing avian pox prevalence varies by species, and with immune function, in Galápagos finches. Biol. Conserv. 153, 72-79.
46. Zylberberg, M., Klasing, K. C. and Hahn, T. P. (2013a). House finches (Carpodacus mexicanus) balance investment in behavioural and immunological defences against pathogens. Biol. Lett. 9, 20120856.
47. Zylberberg, M., Lee, K. A., Klasing, K. C. and Wikelski, M. (2013b). Variation with land use of immune function and prevalence of avian pox in Galapagos finches. Conserv. Biol. 27, 103-112.
48. Zylberberg, M., Klasing, K. C. and Hahn, T. P. (2014). In house finches, Haemorhous mexicanus, risk takers invest more in innate immune function. Anim. Behav. 89, 115-122.