Social context modulates sickness behavior

Abstract

Sickness behaviors constitute an array of symptoms exhibited by an animal during the course of an infection, including reduced activity, reduced food and water intake, and reduced social interactions. It is hypothesized that these symptoms enable reallocation of finite energy resources to fight infection. In this way, by focusing energy on healing, available resources are being removed from other activities, potentially reducing adaptive opportunities, such as mating. Hence, to achieve increased reproductive success, animals might be able to adjust the expression of sickness behaviors to their environmental circumstances. While abiotic conditions such as temperature and season can modulate sickness behaviors, no studies in passerines have linked modulation of sickness behaviors to social settings. Here, it is demonstrated that social surroundings affect the extent to which animals exhibit symptoms of sickness. After an immune challenge, zebra finches kept in isolation markedly reduced activity, but those kept in a colony setting did not. The same trend is verified when looking at the time they spent resting. Additionally, a proinflammatory cytokine (interleukin-6) was quantified in plasma samples and all animals that had been immune challenged showed increased levels of this marker, showing that the physiological response was similar. Hence, birds in a social context were able to overcome the behavioral, but not physiological, symptoms usually associated with an inflammatory response. These findings suggest a trade-off between allowing the body to respond to an infection and taking advantage of being in a social situation.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Adelman JS, Martin LB (2009) Vertebrate sickness behaviors: adaptive and integrated neuroendocrine immune responses. Integr Comp Biol 49:202–214

    PubMed  Article  CAS  Google Scholar 

  2. Adelman JS, Bentley GE, Wingfield JC, Martin LB, Hau M (2010) Population differences in fever and sickness behaviors in a wild passerine: a role for cytokines. J Exp Biol 213:4099–4109

    PubMed  Article  Google Scholar 

  3. Alexander C, Rietschel E (2001) Bacterial lipopolysaccharides and innate immunity. J Endotoxin Res 7:167–202

    PubMed  CAS  Google Scholar 

  4. Aubert A, Goodall G, Dantzer R, Gheusi G (1997) Differential effects of lipopolysaccharide on pup retrieving and nest building in lactating mice. Brain Behav Immun 11:107–118

    PubMed  Article  CAS  Google Scholar 

  5. Avitsur R, Yirmiya R (1999) The immunobiology of sexual behavior: gender differences in the suppression of sexual activity during illness. Pharmacol Biochem Be 64:787–796

    Article  CAS  Google Scholar 

  6. Burness G, Armstrong C, Fee T, 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

    PubMed  Article  Google Scholar 

  7. Cohn D, de Sa-Rocha L (2006) Differential effects of lipopolysaccharide in the social behavior of dominant and submissive mice. Physiol Behav 87:932–937

    PubMed  Article  CAS  Google Scholar 

  8. Dantzer R (2004) Cytokine-induced sickness behaviour: a neuroimmune response to activation of innate immunity. Eur J Pharmacol 500:399–411

    PubMed  Article  CAS  Google Scholar 

  9. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  10. Eisenberger NI, Inagaki TK, Mashal NM, Irvin MR (2010) Inflammation and social experience: an inflammatory challenge induces feelings of social disconnection in addition to depressed mood. Brain Behav Immun 24:558–563

    PubMed  Article  Google Scholar 

  11. Elmquist J, Scammell T, Saper C (1997) Mechanisms of CNS response to systemic immune challenge: the febrile response. Trends Neurosci 20:565–570

    PubMed  Article  CAS  Google Scholar 

  12. Fishkin R, Winslow J (1997) Endotoxin-induced reduction of social investigation by mice: interaction with amphetamine and anti-inflammatory drugs. Psychopharmacology 132:335–341

    PubMed  Article  CAS  Google Scholar 

  13. Hart B (1988) Biological basis of the behavior of sick animals. Neurosci Biobehav R 12:123–137

    Article  CAS  Google Scholar 

  14. Hawley DM, DuRant SE, Wilson AF, Adelman JS, Hopkins WA (2012) Additive metabolic costs of thermoregulation and pathogen infection. Funct Ecol 26:701–710

    Article  Google Scholar 

  15. Johnson R, Vonborell E (1994) Lipopolysaccharide-induced sickness behavior in pigs is inhibited by pretreatment with indomethacin. J Anim Sci 72:309–314

    PubMed  CAS  Google Scholar 

  16. Johnson RW, Curtis SE, Dantzer R, Kelley KW (1993) Central and peripheral prostaglandins are involved in sickness behavior in birds. Physiol Behav 53:127–131

    PubMed  Article  CAS  Google Scholar 

  17. Kavaliers M, Choleris E, Agmo A, Braun WJ, Colwell DD, Muglia LJ, Ogawa S, Pfaff DW (2006) Inadvertent social information and the avoidance of parasitized male mice: a role for oxytocin. Proc Natl Acad Sci U S A 103:4293–4298

    PubMed  Article  CAS  Google Scholar 

  18. Kelley K, Bluthe R, Dantzer R, Zhou J, Shen W, Johnson R, Broussard S (2003) Cytokine-induced sickness behavior. Brain Behav Immun 17:S112–S118

    PubMed  Article  CAS  Google Scholar 

  19. Klein SL, Nelson RJ (1999) Activation of the immune-endocrine system with lipopolysaccharide reduces affiliative behaviors in voles. Behav Neurosci 113:1042–1048

    PubMed  Article  CAS  Google Scholar 

  20. Kluger M (1986) Is fever beneficial. Yale J Biol Med 59:89–95

    PubMed  CAS  Google Scholar 

  21. Kluger M (1991) Fever—role of pyrogens and cryogens. Physiol Rev 71:93–127

    PubMed  CAS  Google Scholar 

  22. Lenczowski MJ, Bluthé RM, Roth J, Rees GS, Rushforth DA, van Dam AM, Tilders FJ, Dantzer R, Rothwell NJ, Luheshi GN (1999) Central administration of rat IL-6 induces HPA activation and fever but not sickness behavior in rats. Am J Physiol 276:R652–R658

    PubMed  CAS  Google Scholar 

  23. Leshchinsky T, Klasing K (2001) Divergence of the inflammatory response in two types of chickens. Dev Comp Immunol 25:629–638

    PubMed  Article  CAS  Google Scholar 

  24. Murray M, Murray AB (1979) Anorexia of infection as a mechanism of host defense. Am J Cli Nutr 32:593–596

    CAS  Google Scholar 

  25. Nakano K, Suzuki S, Oh C (1987) Significance of increased secretion of glucocorticoids in mice and rats injected with bacterial endotoxin. Brain Behav Immun 1:159–172

    PubMed  Article  CAS  Google Scholar 

  26. Nelson RJ (2004) Seasonal immune function and sickness responses. Trends Immunol 25:187–192

    PubMed  Article  CAS  Google Scholar 

  27. Owen-Ashley NT, Wingfield JC (2006) Seasonal modulation of sickness behavior in free-living northwestern song sparrows (Melospiza melodia morphna). J Exp Biol 209:3062–3070

    PubMed  Article  Google Scholar 

  28. Owen-Ashley N, Turner M, Hahn T, Wingfield J (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

    PubMed  Article  CAS  Google Scholar 

  29. Pinheiro JC, Bates DC (2000) Mixed-effects models in S and S-PLUS. Springer, Berlin

    Google Scholar 

  30. Rivier C, Chizzonite R, Vale W (1989) In the mouse, the activation of the hypothalamic–pituitary–adrenal axis by a lipopolysaccharide (endotoxin) is mediated through interleukin-1. Endocrinology 125:2800–2805

    PubMed  Article  CAS  Google Scholar 

  31. Vanoers M, Vanderheyden A, Aarden L (1988) Interleukin 6 (Il-6) in serum and urine of renal-transplant recipients. Clin Exp Immunol 71:314–319

    CAS  Google Scholar 

  32. Wingfield JC, Vleck CM, Moore MC (1992) Seasonal changes of the adrenocortical-response to stress in birds of the Sonoran desert. J Exp Zool 264:419–428

    PubMed  Article  CAS  Google Scholar 

  33. Yee JR, Prendergast BJ (2010) Sex-specific social regulation of inflammatory responses and sickness behaviors. Brain Behav Immun 24:942–951

    PubMed  Article  CAS  Google Scholar 

  34. Yirmiya R, Rosen H, Donchin O, Ovadia H (1994) Behavioral-effects of lipopolysaccharide in rats—involvement of endogenous opioids. Brain Res 648:80–86

    PubMed  Article  CAS  Google Scholar 

  35. Yirmiya R, Avitsur R, Donchin O, Cohen E (1995) Interleukin-1 inhibits sexual behavior in female but not in male rats. Brain Behav Immun 9:220–233

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the staff at the FSSBER, Sean Liu, Eric Mendez, Alan Chen, and Sarah Fong for hours of behavioral observations and Gregory Goldsmith, Nicole Perfito, Lance Kriegsfeld, and Eileen Lacey for help with statistical analysis and comments on the manuscript.

Funding

The authors would like to thank Ministério para Ciência, Tecnologia e Ensino Superior (MCTES-Lisbon, Portugal) for financial support through doctoral grant [SFRH/BD/33251/2007 to P.C.L.] and support from the National Science Foundation [0920753 and 0956338 to G.E.B. and IOS-0750540 to J.C.W.].

Ethical standards

The authors declare that the present study complies with the current laws of the United States of America.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Patrícia C. Lopes.

Additional information

Communicated by D. Rubenstein

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lopes, P.C., Adelman, J., Wingfield, J.C. et al. Social context modulates sickness behavior. Behav Ecol Sociobiol 66, 1421–1428 (2012). https://doi.org/10.1007/s00265-012-1397-1

Download citation

Keywords

  • LPS
  • Trade-off
  • IL-6
  • Isolation
  • Group