Activation of the immune system incurs energetic costs but has no effect on the thermogenic performance of house sparrows during acute cold challenge

Journal of Experimental Biology

Volumn 216, Issue 11, 2013, Pages 2097-2102

  King, Marisa O ^a   Swanson, David L ^a  

^a University of South Dakota   (United States)

Author keywords

Immune; Life history; Lipopolysaccharide; Thermogenic capacity; Trade off

Indexed keywords

LIPOPOLYSACCHARIDE;

ACUTE PHASE RESPONSE; ANIMAL; ARTICLE; COLD; ENERGY METABOLISM; IMMUNE; IMMUNE SYSTEM; IMMUNOLOGY; LIFE HISTORY; METABOLISM; PHYSIOLOGY; SPARROW; THERMOGENIC CAPACITY; THERMOREGULATION; TRADE-OFF;

IMMUNE; LIFE HISTORY; LIPOPOLYSACCHARIDE; THERMOGENIC CAPACITY; TRADE-OFF;

ACUTE-PHASE REACTION; ANIMALS; BODY TEMPERATURE REGULATION; COLD TEMPERATURE; ENERGY METABOLISM; IMMUNE SYSTEM; LIPOPOLYSACCHARIDES; SPARROWS;

EID: 84878102694     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.079574     Document Type: Article

References (49)

1. Anderson, T. R. (2006). Biology of the Ubiquitous House Sparrow: From Genes to Populations. New York, NY: Oxford University Press.
2. Arens, J. R. and Cooper, S. J. (2005). Metabolic and ventilatory acclimatization to cold stress in house sparrows (Passer domesticus). Physiol. Biochem. Zool. 78, 5799-589.
3. Barsig, J., Küsters, S., Vogt, K., Volk, H.-D., Tiegs, G. and Wendel, A. (1995). Lipopolysaccharide-induced interleukin-10 in mice: role of endogenous tumor necrosis factor-α. Eur. J. Immunol. 25, 2888-2893.
4. Bartholomew, G. A., Vleck, D. and Vleck, C. M. (1981). Instantaneous measurements of oxygen consumption during pre-flight warm-up and postflight cooling in sphingid and saturniid moths. J. Exp. Biol. 90, 17-32.
5. Blatteis, C. M. (2006). Endotoxic fever: new concepts of its regulation suggest new approaches to its management. Pharmacol. Ther. 111, 194-223.
6. Bonneaud, C., Mazuc, J., Gonzalez, G., Haussy, C., Chastel, O., Faivre, B. and Sorci, G. (2003). Assessing the cost of mounting an immune response. Am. Nat. 161, 367-379.
7. Burness, G., Armstrong, C., Fee, T. and Tilman-Schindel, E. (2010). Is there an energetic-based trade-off between thermoregulation and the acute phase response in zebra finches? J. Exp. Biol. 213, 1386-1394.
8. Cheng, H. W., Freire, R. and Pajor, E. A. (2004). Endotoxin stress responses in chickens from different genetic lines. I. Sickness, behavioral, and physical responses. Poult. Sci. 83, 707-715.
9. Coon, C. A. C., Warne, R. W. and Martin, L. B. (2011). Acute-phase responses vary with pathogen identity in house sparrows (Passer domesticus). Am. J. Physiol. 300, R1418-R1425.
10. Cooper, S. J. and Swanson, D. L. (1994). Seasonal acclimatization of thermoregulation in the black-capped chickadee. Condor 96, 638-646.
11. Dabbert, C. B., Lochmiller, R. L. and Teeter, R. G. (1997). Effects of acute thermal stress on the immune system of the Northern Bobwhite (Colinus virginianus). Auk 114, 103-109.
12. Dawson, W. R. and Smith, B. K. (1986). Metabolic Acclimatization in the American Goldfinch (Carduelis tristis). New York, NY: Elsevier.
13. French, S. S., Moore, M. C. and Demas, G. E. (2009). Ecological immunology: the organism in context. Integr. Comp. Biol. 49, 246-253.
14. Gutiérrez, J. S., Masero, J. A., Abad-Gomez, J. M., Villegas, A. and Sanchez-Guzman, J. M. (2011). Metabolic consequences of overlapping food restriction and cell-mediated immune response in a long-distance migratory shorebird, the little ringed plover Charadrius dubius. J. Avian Biol. 42, 259-265.
15. Hangalapura, B. N., Nieuwland, M. G. B., de Vries Reilingh, G., Heetkamp, M. J. W., 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.
16. Hangalapura, B. N., Nieuwland, M. G. B., Buyse, J., Kemp, B. and Parmentier, H. K. (2004a). Effect of duration of cold stress on plasma adrenal and thyroid hormone levels and immune responses in chicken lines divergently selected for antibody responses. Poult. Sci. 83, 1644-1649.
17. Hangalapura, B. N., Nieuwland, M. G. B., de Vries Reilingh, G., van den Brand, H., Kemp, B. and Parmentier, H. K. (2004b). Durations of cold stress modulates overall immunity of chicken lines divergently selected for antibody responses. Poult. Sci. 83, 765-775.
18. Hart, B. L. (1988). Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev. 12, 123-137.
19. Hawley, D. M., DuRant, S. E., Wilson, A. F., Adelman, J. S. and Hopkins, W. A. (2012). Additive metabolic costs of thermoregulation and pathogen infection. Funct. Ecol. 26, 701-710.
20. Hayes, J. P. and O'Connor, C. S. (1999). Natural selection on thermogenic capacity of high-Altitude deer mice. Evolution 53, 1280-1287.
21. Hudson, J. W. and Kimzey, S. L. (1966). Temperature regulation and metabolic rhythms in populations of the house sparrow, Passer domesticus. Comp. Biochem. Physiol. 17A, 203-217.
22. Kent, S., Bluthé, R. M., Kelley, K. W. and Dantzer, R. (1992). Sickness behavior as a new target for drug development. Trends Pharmacol. Sci. 13, 24-28.
23. Kluger, M. J., Kozak, W., Conn, C. A., Leon, L. R. and Soszynski, D. (1998). Role of fever in disease. Ann. New York Acad. Sci. 856, 224-233.
24. Lee, K. A., Martin, L. B., II and Wikelski, M. C. (2005). Responding to inflammatory challenges is less costly for a successful avian invader, the house sparrow (Passer domesticus), than its less-invasive congener. Oecologia 145, 243-250.
25. Liknes, E. T., Scott, S. M. and Swanson, D. L. (2002). Seasonal acclimatization in the American goldfinch revisited: to what extent do metabolic rates vary seasonally? Condor 104, 548-557.
26. Marais, M., Maloney, S. K. and Gray, D. A. (2011). The metabolic cost of fever in Pekin ducks. J. Therm. Biol. 36, 116-120.
27. Marsh, R. L. and Dawson, W. R. (1989). Avian adjustments to cold. In Animal Adaptation to Cold. Advances in Comparative and Environmental Physiology, Vol. 4 (ed. L. C. H. Wang), pp. 205-253. Berlin: Springer-Verlag.
28. Martin, L. B., II, Scheuerlein, A. and Wikelski, M. (2003). Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc. Biol. Sci. 270, 153-158.
29. McKechnie, A. E. (2008). Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review. J. Comp. Physiol. B 178, 235-247.
30. Ots, I., Kerimov, A. B., Ivankina, E. V., Ilyina, T. A. and Hõrak, P. (2001). Immune challenge affects basal metabolic activity in wintering great tits. Proc. R. Soc. B 268, 1175-1181.
31. Owen-Ashley, N. T. and Wingfield, J. C. (2007). Acute phase responses of passerine birds: characterization and seasonal variation. J. Ornithol. 148, S583-S591.
32. Owen-Ashley, N. T., Turner, M., Hahn, T. P. and Wingfield, J. C. (2006). Hormonal, behavioral, and thermoregulatory responses to bacterial lipopolysaccharide in captive and free-living white-crowned sparrows (Zonotrichia leucophrys gambelii). Horm. Behav. 49, 15-29.
33. Pantin-Jackwood, M. J., Smith, D. M., Wasilenko, J. L., Cagle, C., Shepherd, E., Sarmento, L., Kapczynski, D. R. and Afonso, C. L. (2012). Effect of age on the pathogenesis and innate immune responses in Pekin ducks infected with different H5N1 highly pathogenic avian influenza viruses. Virus Res. 167, 196-206.
34. Qin, L., Wu, X., Block, M. L., Liu, Y., Breese, G. R., Hong, J. S., Knapp, D. J. and Crews, F. T. (2007). Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55, 453-462.
35. Rudaya, A. Y., Steiner, A. A., Robbins, J. R., Dragic, A. S. and Romanovsky, A. A. (2005). Thermoregulatory responses to lipopolysaccharide in the mouse: dependence on the dose and ambient temperature. Am. J. Physiol. 289, R12449-R1252.
36. Saarela, S., Klapper, B. and Heldmaier, G. (1989). Thermogenic capacity of greenfinches and siskins in winter and summer. In Physiology of Cold Adaptation in Birds (ed. C. Bech and R. E. Reinertsen), pp. 115-122. New York: Plenum Press.
37. Schmidt-Nielsen, K. (1984). Scaling: Why is Animal Size so Important? Cambridge: Cambridge University Press.
38. Sears, M. W., Hayes, J. P., O'Connor, C. S., Geluso, K. and Sedinger, J. S. (2006). Individual variation in thermogenic capacity affects above ground activity of high altitude deer mice. Funct. Ecol. 20, 97-104.
39. Stearns, S. C. (1989). Trade-offs in life-history evolution. Funct. Ecol. 3, 259-268.
40. Svensson, E., Raberg, L., Koch, C. and Hasselquist, D. (1998). Energetic stress, immunosuppression and the costs of an antibody response. Funct. Ecol. 12, 9129-919.
41. Swanson, D. L. (2001). Are summit metabolism and thermogenic endurance correlated in winter-Acclimatized passerine birds? J. Comp. Physiol. B 171, 475-481.
42. Swanson, D. L. (2010). Seasonal metabolic variation in birds: functional and mechanistic correlates. Curr. Ornithol. 17, 75-129.
43. Swanson, D. L. and Liknes, E. T. (2006). A comparative analysis of thermogenic capacity and cold tolerance in small birds. J. Exp. Biol. 209, 466-474.
44. Swanson, D. L., Drymalski, M. W. and Brown, J. R. (1996). Sliding vs static cold exposure and the measurement of summit metabolism in birds. J. Therm. Biol. 21, 221-226.
45. Swanson, D. L., Thomas, N. E., Liknes, E. T. and Cooper, S. J. (2012). Intraspecific correlations of basal and maximal metabolic rates in birds and the aerobic capacity model for the evolution of endothermy. PLoS ONE 7, e34271.
46. Verbeek, E., Oliver, M. H., Waas, J. R., McLeay, L. M., Blache, D. and Matthews, L. R. (2012). Reduced cortisol and metabolic responses of thin ewes to an acute cold challenge in mid-pregnancy: implications for animal physiology and welfare. PLoS ONE 7, e37315.
47. Wiersma, P., Chappell, M. A. and Williams, J. B. (2007). Cold-And exercise-induced peak metabolic rates in tropical birds. Proc. Natl. Acad. Sci. USA 104, 20866-20871.
48. Withers, P. C. (1977). Measurement of VO2, VCO2, and evaporative water loss with a flow-through mask. J. Appl. Physiol. 42, 120-123.
49. Zuk, M. and Stoehr, A. M. (2002). Immune defense and host life history. Am. Nat. 160 Suppl. 4, S9-S22.