Constitutive immune function in European starlings, Sturnus vulgaris, is decreased immediately after an endurance flight in a wind tunnel

Journal of Experimental Biology

Volumn 215, Issue 2, 2012, Pages 272-278

  Nebel, Silke ^a   Bauchinger, Ulf ^b   Buehler, Deborah M ^c,d   Langlois, Lillie A ^b   Boyles, Michelle ^b   Gerson, Alexander R ^a   Price, Edwin R ^a   McWilliams, Scott R ^b   Guglielmo, Christopher G ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b UNIVERSITY OF RHODE ISLAND   (United States)

^c DEPARTMENT OF NATURAL HISTORY   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Constitutive immune function; European starlings; Life history trade off; Migratory flight; Sturnus vulgaris; Wind tunnel

Indexed keywords

COMPLEMENT; HAPTOGLOBIN;

ANIMAL; ARTICLE; CANADA; FLYING; IMMUNOLOGY; INNATE IMMUNITY; LEUKOCYTE; METABOLISM; MOTOR ACTIVITY; PHYSIOLOGY; POPULATION MIGRATION; SONGBIRD;

ANIMAL MIGRATION; ANIMALS; COMPLEMENT SYSTEM PROTEINS; FLIGHT, ANIMAL; HAPTOGLOBINS; IMMUNITY, INNATE; LEUKOCYTES; MOTOR ACTIVITY; ONTARIO; SONGBIRDS;

ANIMALIA; AVES; STURNUS VULGARIS;

EID: 84856494525     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.057885     Document Type: Article

References (80)

1. Alonso-Alvarez, C. and Telia, J. L. (2001). Effects of experimental food restriction and body mass changes on the avian T-cell-mediated immune response. Can. J. Zool. 79, 101-105. (Pubitemid 32180250)
2. Altizer, S., Bartel, R. and Han, B. A. (2011). Animal migration and infectious disease risk. Science 331, 296-302.
3. Altizer, S. M., Oberhauser, K. S. and Brower, L. P. (2000). Associations between host migration and the prevalence of a protozoan parasite in natural populations of adult monarch butterflies. Ecol. Entom. 25, 125-139. (Pubitemid 30301882)
4. Apanlus, V. (1998). Stress and immune defense. In Stress and Behavior, Vol. 27 (ed A. P. Moller M. Milinski and P. J. B. Slater), pp. 133-153. San Diego: Academic Press.
5. Ardla, D. R. (2005). Tree swallows trade off immune function and reproductive effort differently across their range. Ecology 86, 2040-2046.
6. Ardla, D. R. and Schat, K. A. (2008). Ecoimmunology In Avian Immunology (ed. F Davison, B. Kaspers and K. A. Schat), pp. 421-465. Amsterdam: Academic Press
7. Baj, Z., Kantorskl, J., Majewska, E., Zeman, K., Pokoca, L., Fornalczyke, E., Tchorzewski, H., Sulowska, Z. and Lewlckl, R. (1994). Immunological status of competitive cyclists before and after the training season. Int. J. Sports Med. 15, 319-324. (Pubitemid 24289497)
8. Buehler, D. M. and Piersma, T. (2008). Travelling on a budget: predictions and ecological evidence for bottlenecks in the annual cycle of long-distance migrants Philos. Trans. R. Soc. Lond. B 363, 247-266. (Pubitemid 350249334)
9. Buehler, D. M., Bhola, N., Barjaktarov, D., Goymann, W., Schwabl, I., Tleleman, B. I. and Piersma, T. (2008a). Constitutive immune function responds more slowly to handling stress than corticosterone in a shorebird. Physiol. Biochem. Zool. 81, 673-681.
10. Buehler, D. M., Piersma, T., Matson, K. and Tieleman, B. I. (2008b). Seasonal redistribution of immune function in a migrant shorebird: annual-cycle effects override adjustments to thermal regime. Am. Nat. 172, 783-796.
11. Buehler, D. M., Encinas-Viso, F., Petit, M., Vezina, F., Tieleman, B. I. and Piersma, T. (2009). Limited access to food and physiological trade-offs in a long-distance migrant shorebird. Part II: constitutive immune function and the acute phase response. Physiol. Biochem. Zool. 82, 561-571.
12. Buehler, D. M., Tieleman, B. I. and Piersma, T. (2010a). How do migratory species stay healthy over the annual cycle? A conceptual model for immune function and for resistance to disease. Integr. Comp. Biol. 50, 261-279
13. Buehler, D. M., Tieleman, B. I. and Piersma, T. (2010b). Indices of immune function are lower in red knots (Calidris canutus) recovering protein than in those storing fat during stopover in Delaware Bay. Auk 127, 394-401.
14. Butler, P. J. and Woakes, A. J. (1990). The physiology of bird flight. In Bird Migration: Physiology and Ecophysiology (ed. E. Gwinner), pp. 300-318. Heidelberg, Berlin: Springer.
15. Campbell, T. W. (1995). Avian Hematology and Cytology. Ames, Iowa: Iowa State University Press.
16. Campbell, T. W. and Ellis, C. (2007). Avian and Exotic Animal Hematology and Cytology. Ames, Iowa: Blackwell Publishing.
17. Cardinet, G. H., Littrell, J. F. and Schalm, O. W. (1964). Effects of sustained muscular activity upon blood morphology of the horse. Calif. Vet. 18, 31-35
18. Cooper, C. E., Vollaard, N. B. J., Choueiri, T. and Wilson, M. T. (2002). Exercise free radicals and oxidative stress. Biochem. Soc. Trans. 30, 280-285.
19. Davis, A. K. (2005). Effect of handling time and repeated sampling on avian white blood cell counts. J. Field Ornithol. 76, 334-338. (Pubitemid 41712285)
20. Davis, A. K., Maney, D. L. and Maerz, J. C. (2008). The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Fund. Ecol. 22, 760-772
21. Deerenberg, C., Arpanius, V., Daan, S. and Bos, N. (1997). Reproductive effort decreases antibody responsiveness. Proc. R. Soc. Lond. B 264, 1021-1029 (Pubitemid 27351094)
22. Delers, F., Strecker, G. and Engler, R. (1988). Glycosylation of chicken haptoglobin: isolation and characterization of three molecular variants and studies of their distribution in hen plasma before and after turpentine-induced inflammation Biochem. Cell Biol. 66, 208-217.
23. Dhabhar, F. S. (2002). A hassle a day may keep the doctor away: stress and the augmentation of immune function. Integr. Comp. Biol. 42, 556-564 (Pubitemid 35419990)
24. Dhabhar, F. S., Miller, A. H., McEwen, B. S. and Spencer, R. L. (1995). Effects of stress on immune cell distribution. Dynamics and hormonal mechanisms. J. Immunol. 154, 5511-5527.
25. Dobryszychka, W. (1997). Biological functions of haptoglobin-new pieces to an old puzzle. Eur. J. Clin. Chem. Clin. Biochem. 35, 647-654.
26. Dolbeer, R. A. (1982). Migration patterns for age and sex classes of blackbirds and starlings. J. Field Ornithol. 53, 28-46.
27. Earle, R. A. and Underhill, L. G. (1993). Absence of haematozoa in some charadriiformes breeding in the Taimyr Peninsula, Russia. Ardea 81, 21-24
28. Exton, M. S. (1997). Infection-induced anorexia: active host defence strategy. Appetite 29, 369-383. (Pubitemid 28041135)
29. Folstad, I., Nilssen, A. C. and Andersen, J. (1991). Parasite avoidance: the cause of post-calving migrations in Rangifer? Can. J. Zool. 69, 2423-2429
30. Gerson, A. R. and Guglielmo, C. G. (2011). Flight at low ambient humidity increases protein catabolism in migratory birds. Science 333, 1434-1436.
31. Gleeson, M. (2007). Immune function in sport and exercise. J. Appl. Physiol. 103, 693-699. (Pubitemid 47204989)
32. Gleeson, M., McDonald, W. A., Cripps, A. W., Pyne, D. B., Clancy, R. L. and Fricker, P. A. (1995). The effect of immunity of long-term intensive training in elite swimmers. Clin. Exp. Immunol. 102, 210-216.
33. Graham, A. L., Hayward, A. D., Watt, K. A., Pilkington, J. G., Pemberton, J. M. and Nussey, D. H. (2010). Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science 330, 662-665.
34. Gross, W. B. and Siegel, H. S. (1983). Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens. Avian Dis. 27, 972-979.
35. Gutteridge, J. M. C. (1987). The antioxidant activity of haptoglobin towards haemoglobin-stimulated lipid peroxidation Biochim. Biophys. Acta 917, 219-223 (Pubitemid 17004970)
36. Hasselquist, D., Lindstrom, A., Jenni-Eiermann, S., Koolhaas, A. and Piersma, T. (2007). Long flights do not influence immune responses of a long-distance migrant bird: a wind-tunnel experiment. J. Exp. Biol. 210, 1123-1131. (Pubitemid 46759226)
37. Hoffmann, D., Wolfarth, B., Hörterer, H. G., Halle, M., Reichhuber, C., Nadas, K. Tora, C., Erfle, V., Protzer, U. and Schatzl, H. M. (2010). Elevated epstein-barr virus loads and lower antibody titers in competetivie athletes. J. Med. Virol. 82, 446-451.
38. Johnson, C. R. and Field, C. C. (1993). Using fixed-effects model multivariate analysis of variance in marine biology and ecology. Oceanogr. Mar. Biol. Annu. Rev. 31, 177-221.
39. Juul-Madsen, H. R., Viertlboeck, B., Smith, A. L. and Göbel, T. W. F. (2008). Avian innate immune resonses. In Avian Immunology (ed. F. Davison, B. Kaspers and K A. Schat), pp. 129-158. Amsterdam: Academic Press.
40. King, J. R. (1974). Seasonal allocation of time and energy resources in birds. In Avian Energetics, Vol. 15 (ed. R. A. J. Paynter), pp. 4-85. Cambridge, MA: Nuttall Ornithological Club.
41. Klasing, K. C. (1998). Avian macrophages: regulators of local and systemic immune responses. Poultry Sci. 77, 983-989. (Pubitemid 128525111)
42. Klasing, K. C. (2004). The costs of immunity. Acta Zool. Sinica 50, 961-969.
43. Kraaijeveld, A. R., Limentani, E. C. and Godfray, H. C. J. (2001). Basis of the tradeoff between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Proc. R. Soc. Lond. B 268, 259-261. (Pubitemid 32154504)
44. Landys-Ciannelli Jukema, J. and Piersma, T. (2002). Blood parameter changes during stopover in a long-distance migratory shorebird, the bar-tailed godwit Limosa lapponica taymyrensis. J. Avian Biol. 33, 451-455. (Pubitemid 36080435)
45. Lee, K. A. (2006). Linking immune defenses and life history at the levels of the individual and the species. Integr. Comp. Biol. 46, 1000-1015 (Pubitemid 44736435)
46. Lim, Y. K., Jenner, A., Am, A. B., Wang, Y., Hsu, S. I.-H., Chong, S. M., Baumman, H., Halliwell, B. and Lim, S.-K. (2000). Haptoglobin reduces renal oxidative DNA and tissue damage during phenylhydrazine-induced hemolysis. Kidney Int. 58, 1033-1044.
47. Liu, J., Xiao, H., Lei, F., Zhu, Q., Qin, K., Zhang, X.-w., Zhang, X.-I., Zhao, D., Wang, G., Feng, Y. et al. (2005). Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 309, 1206. (Pubitemid 41170907)
48. Lochmiller, R. L. and Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87-98. (Pubitemid 30121291)
49. Lopez, P. and Martin, J. (2005). Female Iberian wall lizards prefer male scents that signal a better cell-mediated immune response. Biol. Lett. 1, 404-406 (Pubitemid 41796580)
50. Marra, P. P., Griffing, S., Caffrey, C., Kilpatrick, A. M., McLean, R., Brand, C., Saito, E., Dupuis, A. P., Kramer, L. and Novak, R. (2004). West Nile Virus and wildlife. Bioscience 54, 393-402. (Pubitemid 38641532)
51. Martin, L. B., Weil, Z. M. and Nelson, R. J. (2008). Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philos. Trans. R. Soc. Lond. B 363, 321-339. (Pubitemid 350249337)
52. Martin, L. B. I. (2005). Trade-offs between molt and immune activity in two populations of house sparrows (Passer domesticus). Can. J. Zool. 83, 780-787.
53. Matson, K. D. (2006). Are there differences in immune function between continental and insular birds? Proc. R. Soc. Lond. B 273, 2267-2274. (Pubitemid 44387332)
54. 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, 275-286. (Pubitemid 39575125)
55. Mauck, R. A., Matson, K. D., Philipsborn, J. and Ricklefs, R. E. (2005). Increase in the constitutive innate humoral immune system in Leach's storm-petrel (Oceanodroma leucorhoa) chicks is negatively correlated with growth rate. Funct Ecol. 19, 1001-1007. (Pubitemid 44922252)
56. Mendes, L., Piersma, T., Lecoq, M., Spaans, B. and Ricklefs, R. E. (2005). Disease-limited distributions? Contrasts in the prevalence of avian malaria in shorebird species using marine and freshwater habitats. Oikos 109, 396-404 (Pubitemid 40518638)
57. Moreno, J., Sanz, J. J. and Arriero, E. (1999). Reproductive effort and T-lymphocyte cell-mediated immunocompetence in female pied Flycatchers Ficedula hypoleuca Proc. R. Soc. Lond. B 266, 1105-1109. (Pubitemid 29290253)
58. Nieman, D. C. (1997). Exercise immunology: practical applications. Int. J. Sports Med. 18, S91-S100.
59. Nieman, D. C. and Pedersen, B. K. (1999). Exercise and immune function: recent developments. Sports Med. 27, 73-80. (Pubitemid 29123579)
60. Nieman, D. C., Buckley, K. S., Henson, D. A., Warren, B. J., Suttles, J., Ahle, J. C. Simandle, S., Fagoaga, O. R. and Nehlsen-Cannarella, S. L. (1995). Immune function in marathon runners versus sedentary controls. Med. Sci. Sports Exerc. 27, 986992.
61. Norris, K. and Evans, M. R. (2000). Ecological immunology: life history trade-offs and immune defense in birds. Behav. Ecol. 11, 19-26. (Pubitemid 30146972)
62. Ochsenbein, A. F. and Zinkernagel, R. M. (2000). Natural antibodies and complement link innate and acquired immunity. Immunol. Today 21, 624-630 (Pubitemid 32044019)
63. Olson, C. L. (1976). On choosing a test statistic in multivariate analysis of variance Psychol. Bull. 83, 579-586.
64. Pedersen, B. K. and Hoffmann-Goetz, L. (2000). Exercise and the immune system regulation, integration, and adaptation. Physiol. Rev. 80, 1055-1081. (Pubitemid 30452011)
65. Peirce, M. A. (1981). Distribution and host-parasite check-list of the haematozoa of birds in western Europe. J. Nat. Hist. 15, 419-458
66. Piersma, T., Everaarts, J. M. and Jukema, J. (1996). Build-up of red blood cells in refuelling bar-tailed godwits in relation to individual migratory quality. Condor 98, 363370.
67. Reed, K. D., Meece, J. K., Henkel, J. S. and Shukla, S. K. (2003). Birds, migration and emerging zoonoses: West Nile virus, Lyme disease, influenza A and enteropathogens. Clin. Med. Res. 1, 5-12.
68. Rolff, J. and Siva-Jothy, M. T. (2003). Invertebrate ecological immunology. Science 301, 472-475. (Pubitemid 36900296)
69. Sanz, J. J., Moreno, J., Merino, S. and Tomás, G. (2004). A trade-off between two resource-demanding functions: post-nuptial moult and immunity during reproduction in male pied flycatchers. J. Anim. Ecol. 73, 441-447. (Pubitemid 38583740)
70. Schmid-Hempel, P. and Ebert, D. (2003). On the evolutionary ecology of specific immune defence. Trends Ecol. Evol. 18, 27-32. (Pubitemid 36048850)
71. Sentiirk, U. K., Gündüz, F., Kuru, O., Kocer, G., Ozkaya, Y. G., Yesilkaya, A., Bor-Kücükatay, M., Uyüklü, M., Yalçin, O. and Baskurt, O. K. (2005). Exerciseinduced oxidative stress leads hemolysis in sedentary but not trained humans. J. Appl. Physiol. 99, 1434-1441. (Pubitemid 43014351)
72. Sheldon, B. C. and Verhulst, S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317-321
73. Sokal, R. R. and Rohlf, F. J. (1995). Biometry. New York: W. H. Freeman and Company.
74. Telia, J. L., Scheuerlein, A. and Ricklefs, R. E. (2002). Is cell-mediated immunity related to the evolution of life-history strategies in birds? Proc. R. Soc. Lond. B 269, 1059-1066. (Pubitemid 34553549)
75. Tvede, N., Steensberg, J., Baslund, B., Halkjaer Kristensen, J. and Pedersen, B. K. (1991). Cellular immunity in highly trained elite racing cyclists during periods of training with high and low intensity. Scand. J. Med. Sci. Sportsl, 163-166
76. van Gils, J. A., Munster, V. J., Radersma, R., Liefhebber, D., Fouchier, R. A. M. and Klaassen, M. (2007). Hampered foraging and migratory performance in swans infected with low-pathogenic avian influenza A virus. PLoS ONE 2, e184
77. Willmer, P., Stone, G. and Johnston, I. (2000). Environmental Physiology of Animals. Oxford: Blackwell Science.
78. Wolach, B., Eliakim, A., Gavrieli, R., Kodesh, E., Yarom, Y., Schlesinger, M. and Falk, B. (1998). Aspects of leukocyte function and the complement system following aerobic exercise in young female gymnasts. Scand. J. Med. Sci. Sports 8, 9197.
79. Zar, J. H. (1999). Biostatistical Analysis. New Jersey: Prentice Hall
80. Zuur, A. F., leno, E. N., Walker, N. J., Saveliev, A. A. and Smith, G. M. (2009) Mixed Effects Models and Extensions in Ecology with R. New York: Springer.