No evidence for avoidance of visibly diseased conspecifics in the highly social banded mongoose (Mungos mungo)

Abstract

Individual host behavior may be influenced by infectious disease in ways that can alter population-level disease dynamics. A novel pathogen in the Mycobacterium tuberculosis complex, Mycobacterium mungi, has emerged among banded mongooses (Mungos mungo) in Northeastern Botswana. This host–pathogen system provides an opportunity to study how individual behavior and social interactions in a group-living species might respond to infectious disease. We used repeated focal observations of known individuals with an extensive ethogram to identify behavioral differences and social interactions between healthy individuals and those with clinical signs of tuberculosis (TB). Clinically diseased banded mongooses exhibited a significantly smaller proportion of time active and alert, a larger proportion of time resting, and a slower behavioral transition rate compared to healthy individuals. They also showed lower reciprocation of allogrooming by approximately 50 %. Despite these strong behavioral differences that may serve as visible cues for healthy mongooses to avoid diseased conspecifics, we found no evidence for avoidance of clinically diseased mongooses by healthy individuals or vice versa: Clinically diseased individuals did not have lower levels of social behaviors than healthy individuals, and clinically diseased mongooses were allogroomed at the expected level despite their decreased reciprocation. Our results show that in contrast to prior studies of other species, avoidance of diseased conspecifics did not occur in this highly social species. We discuss hypotheses for this lack of avoidance and potential implications for pathogen transmission.

This is a preview of subscription content, access via your institution.

Fig. 1

References

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

    CAS  PubMed  Article  Google Scholar 

  2. Alexander KA, Laver PN, Michel A, Williams M, van Helden PD, Warren RM, van Pittius NCG (2010) Novel Mycobacterium tuberculosis complex pathogen, M. mungi. Emerg Infect Dis 16:1296–1299

    PubMed Central  PubMed  Article  Google Scholar 

  3. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267

    CAS  PubMed  Article  Google Scholar 

  4. Arakawa H, Arakawa K, Deak T (2010) Sickness-related odor communication signals as determinants of social behavior in rat: a role for inflammatory processes. Horm Behav 57:330–341

    CAS  PubMed  Article  Google Scholar 

  5. Behringer DC, Butler MMJ, Shields JJD (2006) Avoidance of disease by social lobsters. Nature 441:421

    CAS  PubMed  Article  Google Scholar 

  6. Behringer DC, Butler MJ, Shields JD (2008) Ecological and physiological effects of PaV1 infection on the Caribbean spiny lobster (Panulirus argus Latreille). J Exp Mar Biol Ecol 359:26–33

    Article  Google Scholar 

  7. Bell MB, Nichols HJ, Gilchrist JS, Cant MA, Hodge SJ (2012) The cost of dominance: suppressing subordinate reproduction affects the reproductive success of dominant female banded mongooses. Proc R Soc Lond B 279:619–624

    CAS  Article  Google Scholar 

  8. Bouwman KM, Hawley DM (2010) Sickness behaviour acting as an evolutionary trap? Male house finches preferentially feed near diseased conspecifics. Biol Lett 6:462–465

    PubMed Central  PubMed  Article  Google Scholar 

  9. Cant MA (2013) Demography and social evolution of banded mongooses. Adv Stud Behav 45:407–445

    Article  Google Scholar 

  10. Cant MA, Otali E, Mwanguhya F (2002) Fighting and mating between groups in a cooperatively breeding mammal, the banded mongoose. Ethology 108:541–555

    Article  Google Scholar 

  11. De Luca D, Ginsberg J (2001) Dominance, reproduction and survival in banded mongooses: towards an egalitarian social system? Anim Behav 61:17–30

    PubMed  Article  Google Scholar 

  12. Dolinsky ZS, Hardy CA, Burright RG, Donovick PJ (1985) The progression of behavioral and pathological effects of the parasite Toxocara canis in the mouse. Physiol Behav 35:33–42

    CAS  PubMed  Article  Google Scholar 

  13. Drewe JA, Eames KTD, Madden JR, Pearce GP (2011) Integrating contact network structure into tuberculosis epidemiology in meerkats in South Africa: implications for control. Prev Vet Med 101:113–120

    PubMed  Article  Google Scholar 

  14. Edwards J (1988) The effects of Trichinella spiralis infection on social interactions in mixed groups of infected and uninfected male mice. Anim Behav 36:529–540

    Article  Google Scholar 

  15. Fagen R (1981) Animal play behavior. Oxford University Press, New York

    Google Scholar 

  16. Fischbacher M (1993) Resolution of social conflicts in banded mongooses (Mungos mongo) with a game theoretical model for the evolution of egalitarian relationships. Dissertation, University of Zurich

  17. Gilchrist JS (2006) Reproductive success in a low skew, communal breeding mammal: the banded mongoose, Mungos mungo. Behav Ecol Sociobiol 60:854–863

    Article  Google Scholar 

  18. Gilchrist JS, Otali E, Mwanguhya F (2004) Why breed communally? Factors affecting fecundity in a communal breeding mammal: the banded mongoose (Mungos mungo). Behav Ecol Sociobiol 57:119–131

    Article  Google Scholar 

  19. Graham KL, Burghardt GM (2010) Current perspectives on the biological study of play: signs of progress. Q Rev Biol 85:393–418

    PubMed  Article  Google Scholar 

  20. Hart BL (1988) Biological basis of the behavior of sick animals. Neurosci Biobehav Rev 12:123–137

    CAS  PubMed  Article  Google Scholar 

  21. Hart BL (1990) Behavioral adaptations to pathogens and parasites: five strategies. Neurosci Biobehav Rev 14:273–294

    CAS  PubMed  Article  Google Scholar 

  22. Hawley DM, Etienne RS, Ezenwa VO, Jolles AE (2011) Does animal behavior underlie covariation between hosts’ exposure to infectious agents and susceptibility to infection? Implications for disease dynamics. Integr Comp Biol 51:528–539

    PubMed  Article  Google Scholar 

  23. Johnson R (2002) The concept of sickness behavior: a brief chronological account of four key discoveries. Vet Immunol Immunopathol 87:443–450

    CAS  PubMed  Article  Google Scholar 

  24. Kavaliers M, Colwell DD (1995) Odours of parasitized males induce aversive responses in female mice. Anim Behav 50:1161–1169

    Article  Google Scholar 

  25. Kavaliers M, Choleris E, Agmo A, Pfaff DW (2004) Olfactory-mediated parasite recognition and avoidance: linking genes to behavior. Horm Behav 46:272–283

    PubMed  Article  Google Scholar 

  26. Kiernan K, Tao J, Gibbs P (2012) Tips and strategies for mixed modeling with SAS/STAT® procedures. SAS Global Forum 2012:332–2012

    Google Scholar 

  27. Kiesecker JM, Skelly DK, Beard KH, Preisser E (1999) Behavioral reduction of infection risk. P Natl Acad Sci USA 96:9165–9168

    CAS  Article  Google Scholar 

  28. Kimball BA, Yamazaki K, Kohler D, Bowen RA, Muth JP, Opiekun M, Beauchamp GK (2013) Avian influenza infection alters fecal odor in mallards. PLoS One 8:e75411

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  29. Laver PN (2013) The foraging ecology of banded mongooses (Mungos mungo): epidemiological and human-wildlife conflict implications. Dissertation, Virginia Tech

  30. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  31. Lloyd-Smith JO, Getz WM, Westerhoff HV (2004) Frequency-dependent incidence in models of sexually transmitted diseases: portrayal of pair-based transmission and effects of illness on contact behaviour. Proc R Soc Lond B 271:625–634

    Article  Google Scholar 

  32. Loehle C (1995) Social barriers to pathogen transmission in wild animal populations. Ecology 76:326–335

    Article  Google Scholar 

  33. Martin LB II, Weil ZM, Nelson RJ (2007) Fever and sickness behaviour vary among congeneric rodents. Funct Ecol 22:68–77

    Google Scholar 

  34. Moore J (2002) Parasites and the behavior of animals. Oxford University Press, Oxford

    Google Scholar 

  35. Muller CA, Manser MB, Mu CA (2008) Scent-marking and intrasexual competition in a cooperative carnivore with low reproductive skew. Ethology 114:174–185

    Article  Google Scholar 

  36. Neal E (1970) The banded mongoose, Mungos mungo Gmelin. East African Wildl J 8:63–71

    Article  Google Scholar 

  37. Nichols HJ, Jordan NR, Jamie GA et al (2012) Fine-scale spatiotemporal patterns of genetic variation reflect budding dispersal coupled with strong natal philopatry in a cooperatively breeding mammal. Mol Ecol 21:5348–5362

    PubMed  Article  Google Scholar 

  38. Owen-Ashley NT, Turner M, Hahn TP, Wingfield JC (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

    CAS  PubMed  Article  Google Scholar 

  39. Parsons SDC, Drewe JA, Van Pittius NCG, Warren RM, van Helden PD (2013) Novel cause of tuberculosis. Emerg Infect Dis 19:2004–2007

    PubMed Central  PubMed  Article  Google Scholar 

  40. Penn D, Potts WK (1998) Chemical signals and parasite-mediated sexual selection. Trends Ecol Evol 13:391–396

    CAS  PubMed  Article  Google Scholar 

  41. Rood JP (1975) Population dynamics and food habits of the banded mongoose. East African Wildl J 13:89–111

    Article  Google Scholar 

  42. Tobler M, Schlupp I (2008) Influence of black spot disease on shoaling behaviour in female western mosquitofish, Gambusia affinis (Poeciliidae, Teleostei). Environ Biol Fish 81:29–34

    Article  Google Scholar 

  43. Weary DM, Huzzey JM, von Keyserlingk MAG (2009) Board-invited review: using behavior to predict and identify ill health in animals. J Anim Sci 87:770–777

    CAS  PubMed  Article  Google Scholar 

  44. Weber N, Bearhop S, Dall SRX, Delahay RJ, Ra MD, Carter SP (2013a) Denning behaviour of the European badger (Meles meles) correlates with bovine tuberculosis infection status. Behav Ecol Sociobiol 67:471–479

    Article  Google Scholar 

  45. Weber N, Carter SP, Dall SRX, Delahay RJ, McDonald JL, Bearhop S, McDonald RA (2013b) Badger social networks correlate with tuberculosis infection. Curr Biol 23:R915–R916

    CAS  PubMed  Article  Google Scholar 

  46. Zylberberg M, Klasing KC, Hahn TP (2012) House finches (Carpodacus mexicanus) balance investment in behavioural and immunological defences against pathogens. Biol Lett 9:20120856

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

We thank Peter Laver and Mark Vandewalle for field assistance, Jeff Walters for statistical assistance and comments on the manuscript, and Bill Hopkins and Ignacio Moore for comments on the manuscript.

Ethical standards

This study was conducted under a permit from the Botswana Ministry of Environment, Wildlife, and Tourism and approval of the Virginia Tech’s Institutional Animal Care and Use Committee (Protocol number 07-146-FIW).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Bonnie M. Fairbanks.

Additional information

Communicated by A. I. Schulte-Hostedde

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Fairbanks, B.M., Hawley, D.M. & Alexander, K.A. No evidence for avoidance of visibly diseased conspecifics in the highly social banded mongoose (Mungos mungo). Behav Ecol Sociobiol 69, 371–381 (2015). https://doi.org/10.1007/s00265-014-1849-x

Download citation

Keywords

  • Behavior
  • Disease
  • Disease avoidance
  • Banded mongoose
  • Tuberculosis