Radiotelemetry reveals variation in fever and sickness behaviours with latitude in a free-living passerine (original) (raw)

Abstract

1. The acute phase immune response, which includes fever and sickness behaviours, carries high costs in energy and time, but enhances pathogen clearance in diverse hosts. Hypotheses based upon pathogen pressures and life-history trade-offs predict that costly immune responses will decrease in strength as latitude increases. However, whether the acute phase response shows latitudinal patterns among free-living, wild populations remains unknown.2. Here, we studied fever and sickness behaviours during the early breeding season in free-living song sparrows (Melospiza melodia) along a latitudinal gradient in southern California (CA), Washington (WA), and Alaska (AK). In 2007 and 2008, we injected males with lipopolysaccharide and assessed sickness behaviour by measuring changes in territorial aggression. In 2008, we monitored fever and sickness behaviour in CA and WA birds using a novel telemetric technique: skin-mounted radiotransmitters with temperature sensors.3. In 2007, territorial defence varied by latitude, with a lower probability of territorial response at 24 h after injection in CA, but not in WA or AK. Radiotelemetry in 2008 revealed that CA birds showed pronounced and prolonged lethargy and fever (c. 2 °C above control males throughout the night), whereas WA birds showed only moderate lethargy and fever (c. 1 °C, returning to control levels during the night).4. This study establishes radiotelemetry as a powerful method for quantifying fever and sickness behaviours in small, free-living vertebrates. Moreover, our data suggest that latitude predicts the strength of these responses. These results can provide insight into disease susceptibility and spread among wild populations.

Loading...

Loading Preview

Sorry, preview is currently unavailable. You can download the paper by clicking the button above.

References (61)

  1. Adelman, J.S. & Martin, L.B. (2009) Vertebrate sickness behaviors: adaptive and integrated neuroendocrine immune responses. Integrative and Compara- tive Biology, 49, 202-214.
  2. Arcese, P., Sogge, M.K., Marr, A.B. & Patten, M.A. (2002) Song Sparrow (Melospiza melodia). The Birds of North America, (ed A. Poole). Cornell Lab of Ornithology, Ithaca, NY. Available at http://bna.birds.cornell.edu/bna/ species/704, accessed 4 March 2010.
  3. Ardia, D.R. (2005) Tree swallows trade off immune function and reproductive effort differently across their range. Ecology, 86, 2040-2046.
  4. Aubert, A., Goodall, G., Dantzer, R. & Gheusi, G. (1997) Differential effects of lipopolysaccharide on pup retrieving and nest building in lactating mice. Brain Behavior and Immunity, 11, 107-118.
  5. Bennett, G.F., Montgomerie, R. & Seutin, G. (1992) Scarcity of hematozoa in birds breeding on the arctic tundra of north-america. The Condor, 94, 289- 292.
  6. Bisson, I.A., Butler, L.K., Hayden, T.J., Romero, L.M. & Wikelski, M.C. (2009) No energetic cost of anthropogenic disturbance in a songbird. Pro- ceedings of the Royal Society of London, Series B: Biological Sciences, 276, 961-969.
  7. Bonneaud, C., Mazuc, J., Gonzalez, G., Haussy, C., Chastel, O., Faivre, B. & Sorci, G. (2003) Assessing the cost of mounting an immune response. Ameri- can Naturalist, 161, 367-379.
  8. Buttemer, W.A., Warne, S., Bech, C. & Astheimer, L.B. (2008) Testosterone effects on avian basal metabolic rate and aerobic performance: facts and ar- tefacts. Comparative Biochemistry And Physiology, Part A: Molecular & Inte- grative Physiology, 150, 204-210.
  9. Calisi, R.M. & Bentley, G.E. (2009) Lab and field experiments: are they the same animal? Hormones and Behavior, 56, 1-10.
  10. Catchpole, C.K. & Slater, P.J.B. (1995) Bird Song: Biological Themes and Vari- ations. Cambridge University Press, New York.
  11. Cochran, W.W. & Wikelski, M. (2005) Individual migratory tactics of new world Catharus thrushes: current knowledge and future tracking options from space. Birds of Two Worlds: The Ecology and Evolution of Migration (eds R. Greenberg & P.P. Marra), pp. 274-289. The Johns Hopkins Univer- sity Press, Baltimore, MD.
  12. Exton, M.S. (1997) Infection-induced anorexia: active host defence strategy. Appetite, 29, 369-383.
  13. French, S.S., Denardo, D.F. & Moore, M.C. (2007) Trade-offs between the reproductive and immune systems: facultative responses to resources or obligate responses to reproduction? American Naturalist, 170, 79-89.
  14. French, S.S. & Moore, M.C. (2008) Immune function varies with reproductive stage and context in female and male tree lizards, Urosaurus ornatus. General and Comparative Endocrinology, 155, 148-156.
  15. Gotmark, F. & Post, P. (1996) Prey selection by sparrowhawks, Accipiter nisus: relative predation risk for breeding passerine birds in relation to their size, ecology and behaviour. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences, 351, 1559-1577.
  16. Greiner, E.C., Bennett, G.F., White, E.M. & Coombs, R.F. (1975) Distribution of avian hematozoa of north-america. Canadian Journal of Zoology -Revue Canadienne De Zoologie, 53, 1762-1787.
  17. Grenfell, B.T., Amos, W., Arneberg, P., Bjørnstad, O.N., Greenman, J.V., Harwood, J., Lanfranchi, P., Mclean, A.R., Norman, R.A., Read, A.F. & Skorping, A. (2002) Visions for future research in wildlife epidemiology. Ecology of Wildlife Diseases (eds P.J. Hudson, A. Rizzoli, B.T. Grenfell, J.A.P. Heesterbeek & A.P. Dobson), pp. 151-164. Oxford University Press, Oxford.
  18. Hart, B.L. (1988) Biological basis of the behavior of sick animals. Neuroscience and Biobehavioral Reviews, 12, 123-137.
  19. Hetem, R.S., Mitchell, D., Maloney, S.K., Meyer, L.C.R., Fick, L.G., Kerley, G.I.H. & Fuller, A. (2008) Fever and sickness behavior during an opportu- nistic infection in a free-living antelope, the greater kudu (Tragelaphus strep- siceros). American Journal of Physiology -Regulatory Integrative and Comparative Physiology, 294, R246-R254.
  20. Hiebert, S.M., Stoddard, P.K. & Arcese, P. (1989) Repertoire size, territory acquisition and reproductive success in the song sparrow. Animal Behaviour, 37, 266-273.
  21. Janeway, C.A., Travers, P., Walport, M. & Capra, J.D. (2005) Immunobiology: The Immune System in Health and Disease, 6th edn. Garland, New York.
  22. Johnston, R.F. (1954) Variation in breeding season and clutch size in song spar- rows of the Pacific Coast. The Condor, 56, 268-273.
  23. King, J.R. (1964) Oxygen consumption and body temperature in relation to ambient temperature in the white-crowned sparrow. Comparative Biochemis- try and Physiology, 12, 13-24.
  24. Kjos, C.G. & Cochran, W.W. (1970) Activity of migrant thrushes as deter- mined by radio-telemetry. Wilson Bulletin, 82, 225-226.
  25. Klasing, K.C. (2004) The costs of immunity. Acta Zoologica Sinica, 50, 961- 969.
  26. Kluger, M.J. (1991) Fever: role of pyrogens and cryogens. Physiological Reviews, 71, 93-127.
  27. Kluger, M.J., Kozak, W., Conn, C.A., Leon, L.R. & Soszynski, D. (1998) Role of fever in disease. Annals of the New York Academy of Sciences, 856, 224- 233.
  28. Kroodsma, D.E. (1989) Suggested experimental-designs for song playbacks. Animal Behaviour, 37, 600-609.
  29. Lack, D. (1947) The significance of clutch-size. Ibis, 89, 302-352.
  30. Lambert, T.D., Kays, R.W., Jansen, P.A., Aliaga-Rossel, E. & Wikelski, M. (2009) Nocturnal activity by the primarily diurnal Central Ameri- can agouti (Dasyprocta punctata) in relation to environmental condi- tions, resource abundance and predation risk. Journal of Tropical Ecology, 25, 211-215.
  31. 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.
  32. Lee, K.A., Martin, L.B., Hasselquist, D., Ricklefs, R.E. & Wikelski, M. (2006) Contrasting adaptive immune defenses and blood parasite prevalence in clo- sely related Passer sparrows. Oecologia, 150, 383-392.
  33. Leshchinsky, T.V. & Klasing, K.C. (2001) Divergence of the inflammatory response in two types of chickens. Developmental and Comparative Immunol- ogy, 25, 629-638.
  34. Martin, L.B., Hasselquist, D. & Wikelski, M. (2006) Investment in immune defense is linked to pace of life in house sparrows. Oecologia, 147, 565-575.
  35. Martin, L.B., Weil, Z.M. & Nelson, R.J. (2008) Fever and sickness behaviour vary among congeneric rodents. Functional Ecology, 22, 68-77.
  36. Martin, L.B., Pless, M., Svoboda, J. & Wikelski, M. (2004) Immune activity in temperate and tropical house sparrows: a common-garden experiment. Ecol- ogy, 85, 2323-2331.
  37. Michel, N., Desante, D.F., Kaschube, D.R. & Nott, M.P. (2006) The Monitor- ing Avian Productivity and Survivorship (MAPS) Program Annual Reports, 1989-2003. NBII ⁄ MAPS Avian Demographics Query Interface. Available at: http://www.birdpop.org/nbii/NBIIHome.asp (accessed 12 December 2009).
  38. Møller, A.P., Martin-Vivaldi, M., Merino, S. & Soler, J.J. (2006) Density- dependent and geographical variation in bird immune response. Oikos, 115, 463-474.
  39. Muchlinski, A.E., Baldwin, B.C. & Gramajo, R. (2000) Endotoxin elicits a feb- rile response in laboratory-maintained but not free-living California ground squirrels. Journal of Mammalogy, 81, 701-708.
  40. Nice, M.M. (1937) Studies in the life history of the song sparrow I. Transactions of the Linnaean Society of New York, IV, 1-247.
  41. Norberg, U.M. (1990) Vertebrate Flight. Springer-Verlag, Heidelberg.
  42. Nunn, C.L., Altizer, S.M., Sechrest, W. & Cunningham, A.A. (2005) Latitudi- nal gradients of parasite species richness in primates. Diversity and Distribu- tions, 11, 249-256.
  43. Owen, J.C. & Moore, F.R. (2008a) Relationship between energetic condi- tion and indicators of immune function in thrushes during spring migration. Canadian Journal of Zoology -Revue Canadienne De Zoologie, 86, 638-647.
  44. Owen, J.C. & Moore, F.R. (2008b) Swainson's thrushes in migratory disposition exhibit reduced immune function. Journal of Ethology, 26, 383-388.
  45. Owen-Ashley, N.T. & Wingfield, J.C. (2006) Seasonal modulation of sickness behavior in free-living northwestern song sparrows (Melospiza melodia mor- phna). Journal of Experimental Biology, 209, 3062-3070.
  46. Owen-Ashley, N.T. & Wingfield, J.C. (2007) Acute phase responses of passerine birds: characterization and seasonal variation. Journal of Ornithology, 148, S583-S591.
  47. Owen-Ashley, N.T., Turner, M., Hahn, T.P. & Wingfield, J.C. (2006) Hor- monal, behavioral, and thermoregulatory responses to bacterial lipopolysac- charide in captive and free-living white-crowned sparrows (Zonotrichia leucophrys gambelii). Hormones and Behavior, 49, 15.
  48. Owen-Ashley, N.T., Hasselquist, D., Raberg, L. & Wingfield, J.C. (2008) Lati- tudinal variation of immune defense and sickness behavior in the white- crowned sparrow (Zonotrichia leucophrys). Brain Behavior and Immunity, 22, 614-625.
  49. Peters, A. (2000) Testosterone treatment is immunosuppressive in superb fairy- wrens, yet free-living males with high testosterone are more immunocompe- tent. Proceedings of the Royal Society of London, Series B: Biological Sci- ences, 267, 883-889.
  50. Piersma, T. (1997) Do global patterns of habitat use and migration strategics co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure? Oikos, 80, 623-631.
  51. Pinheiro, J.C. & Bates, D.M. (2000) Mixed-Effects Models in S and S-PLUS. Springer, Berlin.
  52. Pruett, C.L., Arcese, P., Chan, Y.L., Wilson, A.G., Patten, M.A., Keller, L.F. & Winker, K. (2008) Concordant and discordant signals between genetic data and described subspecies of Pacific Coast song sparrows. The Condor, 110, 359-364.
  53. R Development Core Team (2008) R: A Language and Environment for Statisti- cal Computing, Version 2.7.1. Vienna, Austria. Available at: http://www.R- project.org, accessed 31 July 2008.
  54. Roe, C.F. & Kinney, J.M. (1965) Caloric equivalent of fever II. Influence of major trauma. Annals of Surgery, 161, 140-148.
  55. Rohde, K. & Heap, M. (1998) Latitudinal differences in species and com- munity richness and in community structure of metazoan endo-and ectoparasites of marine teleost fish. International Journal for Parasitol- ogy, 28, 461-474.
  56. Smith, J.N.M. (1988) Determinants of lifetime reproductive success in the song sparrow. Reproductive Success (ed. T.H. Clutton-Brock). pp. 154-172. Univeristy of Chicago Press, Chicago.
  57. Tsiouris, J.A., Chauhan, V.P.S., Sheikh, A.M., Chauhan, A., Malik, M. & Vaughan, M.R. (2004) Similarities in acute phase protein response during hibernation in black bears and major depression in humans: a response to underlying metabolic depression? Canadian Journal of Zoology -Revue Canadienne De Zoologie, 82, 1468-1476.
  58. Vaughn, L.K., Bernheim, H.A. & Kluger, M.J. (1974) Fever in the lizard Dipso- saurus dorsalis. Nature, 252, 473-474.
  59. Wingfield, J.C. (1984) Environmental and endocrine control of reproduction in the song sparrow, Melospiza melodia 2. Agonistic interactions as environ- mental information stimulating secretion of testosterone. General and Com- parative Endocrinology, 56, 417-424.
  60. Wingfield, J.C. & Farner, D.S. (1978) The endocrinology of a natural breeding population of the white-crowned sparrow (Zonotrichia leucophrys pugeten- sis). Physiological Zoology, 51, 188-205.
  61. Zar, J.H. (1999) Biostatistical Analysis. Prentice Hall, Upper Saddle River, NJ. Received 8 October 2009; accepted 17 February 2010 Handling Editor: Juan Moreno