Physiological and behavioral responses to an acute-phase response in zebra finches: Immediate and short-term effects

Physiological and Biochemical Zoology

Volumn 87, Issue 2, 2014, Pages 288-298

  Sköld Chiriac, Sandra ^a   Nord, Andreas ^a   ke Nilsson, Jan Å ^a   Hasselquist, Dennis ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; BEHAVIORAL RESPONSE; DOMESTICATION; FITNESS; IMMUNE SYSTEM; MAMMAL; MICROBIAL ACTIVITY; PASSERINE; PATHOGEN; PERSISTENCE; REPRODUCTIVE COST;

IMMUNOGLOBULIN; IMMUNOGLOBULIN Y; LIPOPOLYSACCHARIDE;

ACUTE PHASE RESPONSE; ANIMAL; ARTICLE; BASAL METABOLIC RATE; BLOOD; BODY TEMPERATURE; BODY WEIGHT; FINCH; HUMORAL IMMUNITY; IMMUNOLOGY; INTRAMUSCULAR DRUG ADMINISTRATION; MALE; MOTOR ACTIVITY; PHYSIOLOGY;

ACUTE-PHASE REACTION; ANIMALS; BASAL METABOLISM; BODY TEMPERATURE; BODY WEIGHT; FINCHES; IMMUNITY, HUMORAL; IMMUNOGLOBULINS; INJECTIONS, INTRAMUSCULAR; LIPOPOLYSACCHARIDES; MALE; MOTOR ACTIVITY;

EID: 84896460652     PISSN: 15222152     EISSN: None     Source Type: Journal    
DOI: 10.1086/674789     Document Type: Article

References (67)

1. Abbas A. K. and A. H. Lichtman. 2011. Basic immunology: functions and disorders of the immune system. Updated ed. Saunders-Elsevier, Philadelphia.
2. Adelman J. S., G. E. Bentley, J. C. Wingfield, L. B. Martin, and M. Hau. 2010a. Population differences in fever and sickness behaviors in a wild passerine: a role for cytokines. J Exp Biol 213: 4099-4109.
3. Adelman J. S., S. Córdoba-Córdoba, K. Spoelstra, M. Wikelski, and M. Hau. 2010b. Radiotelemetry reveals variation in fever and sickness behaviours with latitude in a free-living passerine. Funct Ecol 24: 813-823.
4. Ashley N. T. and J. C. Wingfield. 2012. Sickness behavior in vertebrates. Pp. 45-91 in G. E. Demas and R. J. Nelson, eds. Ecoimmunology. Oxford University Press, New York.
5. Baumann H. and J. Gauldie. 1994. The acute phase response. Immunol Today 15: 74-80.
6. Bech C., I. Langseth, and G. W. Gabrielsen. 1999. Repeatability of basal metabolism in breeding female kittiwakes Rissa tridactyla. Proc R Soc B 266: 2161-2167.
7. Bonneaud C., J. Mazuc, G. Gonzalez, C. Haussy, O. Chastel, B. Faivre, and G. Sorci. 2003. Assessing the cost of mounting an immune response. Am Nat 161: 367-379.
8. Bozinovic F. and P. Sabat. 2010. On the intraspecific variability in basal metabolism and the food habits hypothesis in birds. Curr Zool 56: 759-766.
9. Broggi J., E. Hohtola, K. Koivula, M. Orell, and J.-Å. Nilsson. 2009. Long-term repeatability of winter basal metabolic rate and mass in a wild passerine. Funct Ecol 23: 768-773.
10. Burness G., C. Armstrong, T. Fee, and E. Tilman-Schindel. 2010. Is there an energetic-based trade-off between thermoregulation and the acute phase response in zebra finches? J Exp Biol 213: 1386-1394.
11. Calder W. A. 1964. Gaseous metabolism and water relations of the zebra finch, Taeniopygia castanotis. Physiol Zool 37: 400-413.
12. Coon C. A. C., R. W. Warne, and L. B. Martin. 2011. Acute-phase responses vary with pathogen identity in house sparrows (Passer domesticus). Am J Physiol Regul Integr Comp Physiol 300: R1418-R1425.
13. Deak T., C. Bellamy, and K. A. Bordner. 2005. Protracted increases in core body temperature and interleukin-1 following acute administration of lipopolysaccharide: implications for the stress response. Physiol Behav 85: 296-307.
14. Eraud C., A. Jacquet, and B. Faivre. 2009. Survival cost of an early immune soliciting in nature. Evolution 63: 1036-1043.
15. Gray D. A., M. Marais, and S. K. Maloney. 2013. A review of the physiology of fever in birds. J Comp Physiol B 183: 297-312.
16. Gregory N. G., S. R. Payne, C. D. Devine, and C. J. Cook. 2009. Effect of lipopolysaccharide on sickness behaviour in hens kept in cage and free range environments. Res Vet Sci 87: 167-170.
17. Grindstaff J. L., D. Hasselquist, J.-Å. Nilsson, M. Sandell, H. G. Smith, and M. Stjernman. 2006. Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity. Proc R Soc B 273: 2551-2557.
18. Gutierrez J. S., J. A. Masero, J. M. Abad-Gomez, A. Villegas, and J. M. Sanchez-Guzman. 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.
19. Hanssen S. A., D. Hasselquist, I. Folstad, and K. E. Erikstad. 2004. Costs of immunity: immune responsiveness reduces survival in a vertebrate. Proc R Soc B 271: 925-930.
20. Harden L. M., I. du Plessis, S. Poole, and H. P. Laburn. 2006. Interleukin-6 and leptin mediate lipopolysaccharide-induced fever and sickness behavior. Physiol Behav 89: 146-155.
21. Hart B. L. 1988. Biological basis of the behavior of sick animals. Neurosci Biobehav Rev 12: 123-138.
22. Hasselquist D., J. A. Marsh, P. W. Sherman, and J. C. Wingfield. 1999. Is avian humoral immunocompetence suppressed by testosterone? Behav Ecol Sociobiol 45: 167-175.
23. Hasselquist, D. and J.-Å. Nilsson. 2012. Physiological mechanisms mediating costs of immune responses: what can we learn from studies of birds? Anim Behav 83: 1303-1312.
24. Hawley D. M., S. E. DuRant, A. F. Wilson, J. S. Adelman, andW. A. Hopkins. 2012. Additive metabolic costs of thermoregulation and pathogen infection. Funct Ecol 26: 701-710.
25. Hegemann, A., K. D. Matson, M. A. Versteegh, and B. I. Tieleman. 2012. Wild skylarks seasonally modulate energy budgets but maintain energetically costly inflammatory immune responses throughout the annual cycle. PLoS ONE 7: e36358.
26. Hill R. W. 1972. Determination of oxygen consumption by use of the paramagnetic oxygen analyzer. J Appl Physiol 33: 261-263.
27. Holm S. 1979. A simple sequentially rejective multiple test procedure. Scand J Stat 6: 65-70.
28. Ilmonen P., T. Taarna, and D. Hasselquist. 2000. Experimentally activated immune defense in female pied flycatchers results in reduced breeding success. Proc R Soc B 267: 665-670.
29. Klasing K. C. 2004. The costs of immunity. Acta Zool Sin 50: 961-969.
30. Koutsos E. A. and K. C. Klasing. 2001. The acute phase response in Japanese quail (Coturnix coturnix japonica). Comp Biochem Physiol C 128: 255-263.
31. Lee K. A., L. B. Martin II, and M. C. Wikelski. 2005. Responding to inflammatory challenges is less costly for a successful avian invader, the house sparrow (Passer domesticus), than its lessinvasive congener. Oecologia 145: 244-251.
32. Lessells C. M. and P. T. Boag. 1987. Unrepeatable repeatabilities: a common mistake. Auk 104: 116-121.
33. Lochmiller R. L. and C. Deerenberg. 2000. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88: 87-98.
34. Maloney S. K. and D. A. Gray. 1998. Characteristics of the febrile response in Pekin ducks. J Comp Physiol B 168: 177-182.
35. Marais M., S. K. Maloney, and D. A. Gray. 2011. The metabolic cost of fever in Pekin ducks. J Therm Biol 36: 116-120.
36. Martin L. B., D. M. Hawley, and D. R. Ardia. 2011. An introduction to ecological immunology. Funct Ecol 25: 1-4.
37. Martin L. B., A. Scheuerlein, and M. Wikelski. 2003. Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc R Soc B 270: 153-158.
38. Marzal A., M. Reviriego, F. de Lope, and A. P. Møller. 2007. Fitness costs of an immune response in the house martin (Delichon urbica). Behav Ecol Sociobiol 61: 1573-1580.
39. 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.
40. Mendes L., T. Piersma, D. Piersma, and D. Hasselquist. 2006. Two estimates of the metabolic costs of antibody production in migratory shorebirds: low costs, internal reallocation, or both? J Ornithol 147: 274-280.
41. Moe B., B. Rønning, S. Verhulst, and C. Bech. 2009. Metabolic ageing in individual zebra finches. Biol Lett 5: 86-89.
42. Nilsson J.-Å. 2003. Ectoparasitism in marsh tits: costs and functional explanations. Behav Ecol 14: 175-181.
43. Nilsson J.-Å., M. Å kesson, and J. F. Nilsson. 2009. Heritability of resting metabolic rate in a wild population of blue tits. J Evol Biol 22: 1867-1874.
44. Nilsson J.-Å., M. Granbom, and L. Råberg. 2007. Does the strength of an immune response reflect its energetic cost? J Avian Biol 38: 488-494.
45. Nilsson J.-Å. and L. Råberg. 2001. The resting metabolic cost of egg laying and nestling feeding in great tits. Oecologia 128: 187-192.
46. Nomoto S. 1996. Diurnal variations in fever induced by intravenous LPS injection in pigeons. Pfluegers Arch Eur J Physiol 431: 987-989.
47. Nord A., S. Chiriac, D. Hasselquist, and J.-Å. Nilsson. 2013. Endotoxin injection attenuates rest-phase hypothermia in wintering great tits through the onset of fever. Funct Ecol 27: 236-244.
48. Nord A. and J.-Å. Nilsson. 2011. Incubation temperature affects growth and energy metabolism in blue tit nestlings. Am Nat 178: 639-651.
49. Norris K. and M. R. Evans. 2000. Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11: 19-26.
50. Ots I., A. B. Kerimov, E. V. Ivankina, T. A. Ilyina, and P. Hõrak. 2001. Immune challenge affects basal metabolic activity in wintering great tits. Proc R Soc B 268: 1175-1181.
51. Owen-Ashley N. T., M. Turner, T. P. Hahn, and J. C. Wingfield. 2006. Hormonal, behavioral, and thermoregulatory responses to bacterial lipopolysaccharide in captive and freeliving white-crowned sparrows (Zonotrichia leucophrys gambelii). Horm Behav 49: 15-29.
52. Owen-Ashley N. T. and J. C. Wingfield. 2007. Acute phase responses of passerine birds: characterization and seasonal variation. J Ornithol 148: 583-591.
53. 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.
54. Piersma T., N. Cadee, and S. Daan. 1995. Seasonality in basal metabolic rate and thermal conductance in a long-distance migrant shorebird, the knot (Calidris canutus). J Comp Physiol B 165: 37-45.
55. Råberg L., M. Grahn, D. Hasselquist, and E. Svensson. 1998. On the adaptive significance of stress-induced immunosuppression. Proc R Soc B 265: 1637-1641.
56. Råberg L., J.-Å. Nilsson, P. Ilmonen, M. Stjernman, and D. Hasselquist. 2000. The cost of an immune response: vaccination reduces parental effort. Ecol Lett 3: 382-386.
57. Råberg L., M. Stjernman, and D. Hasselquist. 2003. Immune responsiveness in adult blue tits: heritability and effects of nutritional status during ontogeny. Oecologia 136: 360-364.
58. Sheldon B. C. and S. Verhulst. 1996. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11: 317-321.
59. Soler J. J., L. De Neve, T. Perez-Contreras, M. Soler, and G. Sorci. 2003. Trade-off between immunocompetence and growth in magpies: an experimental study. Proc R Soc B 270: 241-248.
60. Sorci G. and B. Faivre. 2009. Inflammation and oxidative stress in vertebrate host-parasite systems. Philos Trans R Soc B 364: 71-83.
61. Svensson E., L. Råberg, C. Koch, and D. Hasselquist. 1998. Energetic stress, immunosuppression and the costs of an antibody response. Funct Ecol 12: 912-919.
62. Tizard I. 2008. Sickness behavior, its mechanisms and significance. Anim Health Res Rev 9: 87-99.
63. Tobler M., D. Hasselquist, H. G. Smith, and M. I. Sandell. 2010. Short-and long-term consequences of prenatal testosterone for immune function: an experimental study in the zebra finch. Behav Ecol Sociobiol 64: 717-727.
64. Toomey M. B., M. W. Butler, and K. J. McGraw. 2010. Immunesystem activation depletes retinal carotenoids in house finches (Carpodacus mexicanus). J Exp Biol 213: 1709-1716.
65. Tschirren B. and H. Richner. 2006. Parasites shape the optimal investment in immunity. Proc R Soc B 273: 1773-1777.
66. von Schantz T., S. Bensch, M. Grahn, D. Hasselquist, and H. Wittzell. 1999. Good genes, oxidative stress and conditiondependent sexual signals. Proc R Soc B 266: 1-12.
67. Zuk M. and A. M. Stoehr. 2002. Immune defense and host life history. Am Nat 160: 9-22.