Skip to main content
Log in

Contact networks and transmission of an intestinal pathogen in bumble bee (Bombus impatiens) colonies

Oecologia Aims and scope Submit manuscript

Abstract

In socially living animals, individuals interact through complex networks of contact that may influence the spread of disease. Whereas traditional epidemiological models typically assume no social structure, network theory suggests that an individual’s location in the network determines its risk of infection. Empirical, especially experimental, studies of disease spread on networks are lacking, however, largely due to a shortage of amenable study systems. We used automated video-tracking to quantify networks of physical contact among individuals within colonies of the social bumble bee Bombus impatiens. We explored the effects of network structure on pathogen transmission in naturally and artificially infected hives. We show for the first time that contact network structure determines the spread of a contagious pathogen (Crithidia bombi) in social insect colonies. Differences in rates of infection among colonies resulted largely from differences in network density among hives. Within colonies, a bee’s rate of contact with infected nestmates emerged as the only significant predictor of infection risk. The activity of bees, in terms of their movement rates and division of labour (e.g., brood care, nest care, foraging), did not influence risk of infection. Our results suggest that contact networks may have an important influence on the transmission of pathogens in social insects and, possibly, other social animals.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Alford DV (1975) Bumblebees. Davis-Poynter, London

    Google Scholar 

  • Anderson RM (1991) Discussion: The Kermack–McKendrick epidemic threshold theorem. Bull Math Biol 53:3–32

    Article  PubMed  CAS  Google Scholar 

  • Anderson RM, May RM (1991) Infectious diseases of humans: dynamics and control. Oxford University Press, Oxford

    Google Scholar 

  • Anderson C, McShea DW (2001) Individual versus social complexity, with particular reference to ant colonies. Biol Rev 76:211–237

    Article  PubMed  CAS  Google Scholar 

  • Birkhead G, Vogt RL (1989) Epidemiologic surveillance for endemic Giardia lamblia infection in Vermont—the roles of waterborne and person-to-person transmission. Am J Epidemiol 129:762–768

    PubMed  CAS  Google Scholar 

  • Borgatti SP, Everett MG, Freeman LC (2002) Ucinet for windows: software for social network analysis. Analytic Technologies, Harvard

    Google Scholar 

  • Bourke AFG (1999) Colony size, social complexity and reproductive conflict in social insects. J Evol Biol 12:245–257

    Article  Google Scholar 

  • Brown MJF, Loosli R, Schmid-Hempel P (2000) Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91:421–427

    Article  Google Scholar 

  • Brown MJF, Schmid-Hempel R, Schmid-Hempel P (2003) Strong context-dependent virulence in a host-parasite system: reconciling genetic evidence with theory. J Anim Ecol 72:994–1002

    Article  Google Scholar 

  • Corner LAL, Pfeiffer DU, Morris RS (2003) Social-network analysis of Mycobacterium bovis transmission among captive brushtail possums (Trichosurus vulpecula). Prev Vet Med 59:147–167

    Article  PubMed  CAS  Google Scholar 

  • Cross PC, Lloyd-Smith JO, Bowers JA, Hay CT, Hofmeyr M, Getz WM (2004) Integrating association data and disease dynamics in a social ungulate: bovine tuberculosis in African buffalo in the Kruger National Park. Ann Zool Fenn 41:879–892

    Google Scholar 

  • Dornhaus A, Chittka L (2001) Food alert in bumblebees (Bombus terrestris): possible mechanisms and evolutionary implications. Behav Ecol Sociobiol 50:570–576

    Article  Google Scholar 

  • Durrer S, Schmid-Hempel P (1994) Shared use of flowers leads to horizontal pathogen transmission. Proc R Soc Lond Ser B 258:299–302

    Article  Google Scholar 

  • Eisenberg JNS, Lei XD, Hubbard AH, Brookhart MA, Colford JM (2005) The role of disease transmission and conferred immunity in outbreaks: analysis of the 1993 Cryptosporidium outbreak in Milwaukee, Wisconsin. Am J Epidemiol 161:62–72

    Article  PubMed  Google Scholar 

  • El Bushra HE, Bin Saeed AA (1999) Intrafamilial person-to-person spread of bacillary dysentery due to Shigella dysenteriae in southwestern Saudi Arabia. East Afr Med J 76:255–259

    PubMed  CAS  Google Scholar 

  • Feldman A, Balch T (2004) Representing honey bee behavior for recognition using human trainable models. Adapt Behav 12:241–250

    Article  Google Scholar 

  • Free JB (1955) The division of labour within bumblebee colonies. Insectes Soc 2:195–212

    Article  Google Scholar 

  • Friedman SR et al (1997) Sociometric risk networks and risk for HIV infection. Am J Public Health 87:1289–1296

    Article  PubMed  CAS  Google Scholar 

  • Gegear RJ, Otterstatter MC, Thomson JD (2005) Does infection by an intestinal parasite impair the ability of bumble bees to learn flower handling skills? Anim Behav 70:209–215

    Article  Google Scholar 

  • Gegear RJ, Otterstatter MC, Thomson JD (2006) Bumblebee foragers infected by a gut parasite have an impaired ability to utilize floral information. Proc R Soc Lond Ser B 273:1073–1078

    Article  Google Scholar 

  • Gordon DM, Paul RE, Thorpe K (1993) What is the function of encounter patterns in ant colonies. Anim Behav 45:1083–1100

    Article  Google Scholar 

  • Greene MJ, Gordon DM (2003) Social insects—cuticular hydrocarbons inform task decisions. Nature 423:32–32

    Article  PubMed  CAS  Google Scholar 

  • Heinrich B (1979) Bumblebee economics. Harvard University Press, Cambridge

    Google Scholar 

  • Imhoof B, Schmid-Hempel P (1999) Colony success of the bumble bee, Bombus terrestris, in relation to infections by two protozoan parasites, Crithidia bombi and Nosema bombi. Insectes Soc 46:233–238

    Article  Google Scholar 

  • Keeling MJ, Eames KTD (2005) Networks and epidemic models. J R Soc Interface 2:295–307

    Article  PubMed  Google Scholar 

  • Keystone JS, Krajden S, Warren MR (1978) Person-to-person transmission of Giardia lamblia in day care nurseries. Can Med Assoc J 119:241–242

    PubMed  CAS  Google Scholar 

  • Klovdahl AS (1985) Social networks and the spread of infectious diseases—the AIDS example. Soc Sci Med 21:1203–1216

    Article  PubMed  CAS  Google Scholar 

  • Liljeros F, Edling CR, Amaral LAN (2003) Sexual networks: implications for the transmission of sexually transmitted infections. Microbes Infect 5:189–196

    Article  PubMed  Google Scholar 

  • Logan A, Ruiz-González MX, Brown MJF (2005) The impact of host starvation on parasite development and population dynamics in an intestinal trypanosome parasite of bumble bees. Parasitology 130:637–642

    Article  PubMed  CAS  Google Scholar 

  • Mallon EB, Schmid-Hempel P (2004) Behavioural interactions, kin and disease susceptibility in the bumblebee Bombus terrestris. J Evol Biol 17:829–833

    Article  PubMed  Google Scholar 

  • May RM (2006) Network structure and the biology of populations. Trends Ecol Evol 21:394–399

    Article  PubMed  Google Scholar 

  • Meyers LA (2007) Contact network epidemiology: bond percolation applied to infectious disease prediction and control. Bull Am Math Soc 44:63–86

    Article  Google Scholar 

  • Montoya JM, Pimm SL, Sole RV (2006) Ecological networks and their fragility. Nature 442:259–264

    Article  PubMed  CAS  Google Scholar 

  • Müller CB, Schmid-Hempel P (1992) Variation in life-history pattern in relation to worker mortality in the bumblebee, Bombus lucorum. Funct Ecol 6:48–56

    Article  Google Scholar 

  • Naug D, Camazine S (2002) The role of colony organization on pathogen transmission in social insects. J Theor Biol 215:427–439

    Article  PubMed  Google Scholar 

  • Naug D, Smith B (2006) Experimentally induced change in infectious period affects transmission dynamics in a social group. Proc R Soc B Biol Sci 274:61–65

    Article  Google Scholar 

  • Naumann K, Winston ML, Slessor KN, Prestwich GD, Webster FX (1991) Production and transmission of honey bee queen (Apis mellifera L.) mandibular gland pheromone. Behav Ecol Sociobiol 29:321–332

    Article  Google Scholar 

  • Neaigus A, Friedman SR, Kottiri BJ, Jarlais DCD (2001) HIV risk networks and HIV transmission among injecting drug users. Eval Program Plann 24:221–226

    Article  Google Scholar 

  • Newman MEJ (2003) The structure and function of complex networks. SIAM Rev 45:167–256

    Article  Google Scholar 

  • Newman MEJ, Barabasi AL, Watts DJ (eds) (2006) The structure and dynamics of networks. Princeton University Press, Princeton

  • Nicolis SC, Theraulaz G, Deneubourg JL (2005) The effects of aggregates on interaction rate in ant colonies. Anim Behav 69:535–540

    Article  Google Scholar 

  • O’Donnell S, Reichardt M, Foster R (2000) Individual and colony factors in bumble bee division of labor (Bombus bifarius nearcticus Handl; Hymenoptera, Apidae). Insectes Soc 47:164–170

    Article  Google Scholar 

  • Otterstatter MC, Thomson JD (2006) Within-host dynamics of an intestinal pathogen of bumble bees. Parasitology 133:749–761

    Article  PubMed  CAS  Google Scholar 

  • Otterstatter MC, Gegear RJ, Colla S, Thomson JD (2005) Effects of parasitic mites and protozoa on the flower constancy and foraging rate of bumble bees. Behav Ecol Sociobiol 58:383–389

    Article  Google Scholar 

  • Pacala SW, Gordon DM, Godfray HCJ (1996) Effects of social group size on information transfer and task allocation. Evol Ecol 10:127–165

    Article  Google Scholar 

  • Padhye NV, Doyle MP (1992) Escherichia coli O157-H7—epidemiology, pathogenesis, and methods for detection in food. J Food Prot 55:555–565

    Google Scholar 

  • Proulx SR, Promislow DEL, Phillips PC (2005) Network thinking in ecology and evolution. Trends Ecol Evol 20:345–353

    Article  PubMed  Google Scholar 

  • Rodd FH, Plowright RC, Owen RE (1980) Mortality rates of adult bumble bee workers (Hymenoptera, Apidae). Can J Zool 58:1718–1721

    Article  Google Scholar 

  • Ryan MJ, Wall PG, Adak GK, Evans HS, Cowden JM (1997) Outbreaks of infectious intestinal disease in residential institutions in England and Wales 1992–1994. J Infect 34:49–54

    Article  PubMed  CAS  Google Scholar 

  • SAS Institute (2006) SAS/STAT 9.1 User’s Guide. SAS Institute, Cary

    Google Scholar 

  • Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton

    Google Scholar 

  • Schmid-Hempel P (2001) On the evolutionary ecology of host-parasite interactions: addressing the question with regard to bumblebees and their parasites. Naturwissenschaften 88:147–158

    Article  PubMed  CAS  Google Scholar 

  • Schmid-Hempel P, Schmid-Hempel R (1993) Transmission of a pathogen in Bombus terrestris, with a note on division of labor in social insects. Behav Ecol Sociobiol 33:319–327

    Article  Google Scholar 

  • Shykoff JA, Schmid-Hempel P (1991) Genetic relatedness and eusociality—parasite-mediated selection on the genetic composition of groups. Behav Ecol Sociobiol 28:371–376

    Article  Google Scholar 

  • van Honk C, Hogeweg P (1981) The ontogeny of the social structure in a captive Bombus terrestris colony. Behav Ecol Sociobiol 9:111–119

    Article  Google Scholar 

  • Veeraraghavan A, Chellappa R (2005) Tracking bees in a hive. In: Snowbird Learning Workshop, Snowbird, Utah

  • Wasserman S, Faust K (1994) Social network analysis: methods and applications. Cambridge University Press, Cambridge

    Google Scholar 

  • Wilson EO (1971) The insect societies. Harvard University Press, Cambridge

    Google Scholar 

  • Wilson EO, Holldobler B (1988) Dense heterarchies and mass communication as the basis of organization in ant colonies. Trends Ecol Evol 3:65–68

    Article  Google Scholar 

  • Wu W (1994) Microevolutionary studies on a host–parasite interaction. PhD dissertation. University of Basel, Basel

Download references

Acknowledgements

We thank T. Day, P. Millson, M.-J. Fortin, P.G. Kevan and two anonymous reviewers for helpful comments on the manuscript. We also thank A. Fung for help with the Ethovision software. Funding for this research was provided by the Natural Sciences and Engineering Research Council of Canada and Ontario Graduate Scholarships to M.C.O.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael C. Otterstatter.

Additional information

Communicated by Nathan Sanders.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Otterstatter, M.C., Thomson, J.D. Contact networks and transmission of an intestinal pathogen in bumble bee (Bombus impatiens) colonies. Oecologia 154, 411–421 (2007). https://doi.org/10.1007/s00442-007-0834-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-007-0834-8

Keywords

Navigation