Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-26T06:10:03.010Z Has data issue: false hasContentIssue false
  • English
  • Français

Within-host dynamics of an intestinal pathogen of bumble bees

Published online by Cambridge University Press:  04 September 2006

M. C. OTTERSTATTER  and
J. D. THOMSON
M. C. OTTERSTATTER
Affiliation:
Department of Zoology, University of Toronto, 25 Harbord Street, Toronto, Ontario, Canada, M5S 3G5
J. D. THOMSON
Affiliation:
Department of Zoology, University of Toronto, 25 Harbord Street, Toronto, Ontario, Canada, M5S 3G5
Get access Rights & Permissions [Opens in a new window]

Abstract

The success of a pathogen depends not only on its transmission to new hosts, but also on its ability to colonize and persist within its current host. Studies of within-host dynamics have focused on only a few diseases of humans, whereas little is known about the factors that influence pathogen populations as they develop inside non-human hosts. Here, we investigate pathogen dynamics occurring within bumble bees (Bombus impatiens) infected by the gut trypanosome Crithidia bombi. Infection by C. bombi showed several features characteristic of vertebrate diseases, including a rapid initial increase in infection intensity, marked oscillations in parasitaemia, and the stimulation of a systemic immune response in infected bees. Within-host dynamics generated substantial variation in the infectiousness and flower-visiting behaviour of bumble bees. Changes in bee foraging that arise from infection may influence the probability of C. bombi transmission between bees at flowers.

Keywords

Crithidia bombiBombusbumble beespathogen transmissionwithin-host dynamics
Type
Research Article
Information
Parasitology , Volume 133 , Issue 6 , December 2006 , pp. 749 - 761
Copyright
2006 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Allander, K. and Schmid-Hempel, P. ( 2000). Immune defence reaction in bumble-bee workers after a previous challenge and parasitic coinfection. Functional Ecology 14, 711–717.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. ( 1991). Infectious Diseases of Humans: Dynamics and Control. Oxford University Press, Oxford.
Antia, R., Nowak, M. A. and Anderson, R. M. ( 1996). Antigenic variation and the within-host dynamics of parasites. Proceedings of the National Academy of Sciences, USA 93, 985–989.CrossRefGoogle Scholar
Baer, B. and Schmid-Hempel, P. ( 1999). Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature, London 397, 151–154.CrossRefGoogle Scholar
Brown, M. J. F., Loosli, R. and Schmid-Hempel, P. ( 2000). Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91, 421–427.CrossRefGoogle Scholar
Brown, M. J. F., Moret, Y. and Schmid-Hempel, P. ( 2003). Activation of host constitutive immune defence by an intestinal trypanosome parasite of bumble bees. Parasitology 126, 253–260.CrossRefGoogle Scholar
Colla, S., Otterstatter, M. C., Gegear, R. J. and Thomson, J. D. ( 2006). Plight of the bumble bee: pathogen spillover from commercial to wild populations. Biological Conservation 129, 461–467.CrossRefGoogle Scholar
Costerton, J. W., Cheng, K. J., Geesey, G. G., Ladd, T. I., Nickel, J. C., Dasgupta, M. and Marrie, T. J. ( 1987). Bacterial biofilms in nature and disease. Annual Review of Microbiology 41, 435–464.CrossRefGoogle Scholar
De Roode, J. C., Culleton, R., Cheesman, S. J., Carter, R. and Read, A. F. ( 2004). Host heterogeneity is a determinant of competitive exclusion or coexistence in genetically diverse malaria infections. Proceedings of the Royal Society of London, B 271, 1073–1080.CrossRefGoogle Scholar
Doums, C., Moret, Y., Benelli, E. and Schmid-Hempel, P. ( 2002). Senescence of immune defence in Bombus workers. Ecological Entomology 27, 138–144.CrossRefGoogle Scholar
Druilhe, P., Hagan, P. and Rook, G. A. W. ( 2002). The importance of models of infection in the study of disease resistence. Trends in Microbiology 10, S38–S46.CrossRefGoogle Scholar
Durrer, S. and Schmid-Hempel, P. ( 1994). Shared use of flowers leads to horizontal pathogen transmission. Proceedings of the Royal Society of London, B 258, 299–302.CrossRefGoogle Scholar
Dye, C. and Hasibeder, G. ( 1986). Population dynamics of mosquito-borne disease – Effects of flies which bite some people more frequently than others. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 69–77.CrossRefGoogle Scholar
Ebert, D. ( 1994). Virulence and local adaptation of a horizontally transmitted parasite. Science 265, 1084–1086.CrossRefGoogle Scholar
Ebert, D. and Mangin, K. L. ( 1997). The influence of host demography on the evolution of virulence of a microsporidian gut parasite. Evolution 51, 1828–1837.CrossRefGoogle Scholar
Ebert, D., Zschokke-Rohringer, C. D. and Carius, H. J. ( 1998). Within- and between-population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa. Proceedings of the Royal Society of London, B 265, 2127–2134.CrossRefGoogle Scholar
Ewald, P. W. ( 1983). Host-parasite relations, vectors, and the evolution of disease severity. Annual Review of Ecology and Systematics 14, 465–485.CrossRefGoogle Scholar
Ewald, P. W. ( 1993). The evolution of virulence. Scientific American 268, 86–87.CrossRefGoogle Scholar
Fenner, F. and Ratcliffe, F. ( 1965). Myxomatosis, Cambridge University Press, Cambridge, UK.
Frank, S. A. ( 1996). Models of parasite virulence. Quarterly Review of Biology 71, 37–78.CrossRefGoogle Scholar
Ganusov, V. V., Bergstrom, C. T. and Antia, R. ( 2002). Within-host population dynamics and the evolution of microparasites in a heterogeneous host population. Evolution 56, 213–223.CrossRefGoogle Scholar
Gegear, R. J., Otterstatter, M. C. and Thomson, J. D. ( 2005). Does infection by an intestinal parasite impair the ability of bumble bees to learn flower handling skills? Animal Behaviour 70, 209–215.Google Scholar
Gegear, R. J., Otterstatter, M. C. and Thomson, J. D. ( 2006). Bumblebee foragers infected by a gut parasite have an impaired ability to utilize floral information. Proceedings of the Royal Society of London, B 273, 1073–1078.CrossRefGoogle Scholar
Gegear, R. J. and Thomson, J. D. ( 2004). Does the flower constancy of bumble bees reflect foraging economics? Ethology 110, 793–805.Google Scholar
Gorbunov, P. S. ( 1996). Peculiarities of life cycle in flagellate Crithidia bombi (Protozoa, Trypanosomatidae). Zoologichesky Zhurnal 75, 803–810.Google Scholar
Gravenor, M. B., McLean, A. R. and Kwiatkowski, D. ( 1995). The regulation of malaria parasitaemia – parameter estimates for a population model. Parasitology 110, 115–122.CrossRefGoogle Scholar
Grenfell, B. T. and Anderson, R. M. ( 1985). The estimation of age-related rates of infection from case notifications and serological data. Journal of Hygiene 95, 419–436.CrossRefGoogle Scholar
Haydon, D. T., Matthews, L., Timms, R. and Colegrave, N. ( 2003). Top-down or bottom-up regulation of intra-host blood-stage malaria: Do malaria parasites most resemble the dynamics of prey or predator? Proceedings of the Royal Society of London, B 270, 289–298.Google Scholar
Hellriegel, B. ( 1992). Modeling the immune response to malaria with ecological concepts – short-term behavior against long-term equilibrium. Proceedings of the Royal Society of London, B 250, 249–256.CrossRefGoogle Scholar
Herre, E. A. ( 1993). Population structure and the evolution of virulence in nematode parasites of fig wasps. Science 259, 1442–1445.CrossRefGoogle Scholar
Hetzel, C. and Anderson, R. M. ( 1996). The within-host cellular dynamics of bloodstage malaria: theoretical and experimental studies. Parasitology 113, 25–38.CrossRefGoogle Scholar
Hoshen, M. B., Heinrich, R., Stein, W. D. and Ginsburg, H. ( 2000). Mathematical modelling of the within-host dynamics of Plasmodium falciparum. Parasitology 121, 227–235.CrossRefGoogle Scholar
Imhoof, B. and Schmid-Hempel, P. ( 1998). Single-clone and mixed-clone infections versus host environment in Crithidia bombi infecting bumblebees. Parasitology 117, 331–336.CrossRefGoogle Scholar
Imhoof, B. and 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 Sociaux 46, 233–238.CrossRefGoogle Scholar
Kermack, W. O. and McKendrick, A. G. ( 1927). A contribution to the mathematical theory of epidemics. Proceedings of the Royal Society of London, A 115, 700–721.CrossRefGoogle Scholar
Klinkenberg, D. and Heesterbeek, J. A. P. ( 2005). A simple model for the within-host dynamics of a protozoan parasite. Proceedings of the Royal Society of London, B 272, 593–600.CrossRefGoogle Scholar
Kollien, A. H. and Schaub, G. A. ( 2000). The development of Trypanosoma cruzi in triatominae. Parasitology Today 16, 381–387.CrossRefGoogle Scholar
Kollien, A. H. and Schaub, G. A. ( 2002). The development of Blastocrithidia triatomae (Trypanosomatidae) in the reduviid bug Triatoma infestans (Insecta): influence of starvation. Parasitology Research 88, 804–809.CrossRefGoogle Scholar
Kollien, A. H. and Schaub, G. A. ( 2003). The development of Blastocrithidia triatomae (Trypanosomatidae) in the reduviid bug Triatoma infestans (Insecta): influence of feeding. Parasitology Research 89, 430–436.Google Scholar
Laverty, T. M. ( 1994). Bumble bee learning and flower morphology. Animal Behaviour 47, 531–545.CrossRefGoogle Scholar
Lehane, M. J., Wu, D. and Lehane, S. M. ( 1997). Midgut-specific immune molecules are produced by the blood-sucking insect Stomoxys calcitrans. Proceedings of the National Academy of Sciences, USA 94, 11502–11507.CrossRefGoogle Scholar
Lenski, R. E. ( 1988). Evolution of plague virulence. Nature, London 334, 473–474.CrossRefGoogle Scholar
Lipsitch, M. and Moxon, E. R. ( 1997). Virulence and transmissibility of pathogens: What is the relationship? Trends in Microbiology 5, 31–37.Google Scholar
Lloyd-Smith, J. O., Getz, W. M. and Westerhoff, H. V. ( 2004). Frequency-dependent incidence in models of sexually transmitted diseases: portrayal of pair-based transmission and effects of illness on contact behaviour. Proceedings of the Royal Society of London, B 271, 625–634.CrossRefGoogle Scholar
Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. and Getz, W. M. ( 2005). Superspreading and the effect of individual variation on disease emergence. Nature, London 438, 355–359.CrossRefGoogle Scholar
Logan, A., Ruiz-Gonzalez, M. X. and Brown, M. J. F. ( 2005). The impact of host starvation on parasite development and population dynamics in an intestinal trypanosome parasite of bumble bees. Parasitology 130, 637–642.CrossRefGoogle Scholar
MacKinnon, M. J. and Read, A. F. ( 2004). Virulence in malaria: an evolutionary viewpoint. Philosophical Transactions of the Royal Society of London, B 359, 965–986.CrossRefGoogle Scholar
Matthews, L., Low, J. C., Gally, D. L., Pearce, M. C., Mellor, D. J., Heesterbeek, J. A. P., Chase-Topping, M., Naylor, S. W., Shaw, D. J., Reid, S. W. J., Gunn, G. J. and Woolhouse, M. E. J. ( 2006). Heterogeneous shedding of Escherichia coli O157 in cattle and its implications for control. Proceedings of the National Academy of Sciences, USA 103, 547–552.CrossRefGoogle Scholar
May, R. M. and Anderson, R. M. ( 1987). Transmission dynamics of HIV infection. Nature, London 326, 137–142.CrossRefGoogle Scholar
Molineaux, L. and Dietz, K. ( 1999). Review of intra-host models of malaria. Parassitologica 41, 221–231.Google Scholar
Myers, J. H. and Rothman, L. E. ( 1995). Virulence and transmission of infectious diseases in humans and insects – evolutionary and demographic patterns. Trends in Ecology and Evolution 10, 194–198.CrossRefGoogle Scholar
Nakajima, Y., Saido-Sakanaka, H., Gihara, K., Taylor, D. and Yamakawa, M. ( 2005). Antibacterial peptides are secreted into the midgut lumen to provide antibacterial midgut defense in the soft tick, Ornithodoros moubata (Acari: Argasidae). Applied Entomology and Zoology 40, 391–397.CrossRefGoogle Scholar
Nigam, Y., Maudlin, I., Welburn, S. and Ratcliffe, N. A. ( 1997). Detection of phenoloxidase activity in the hemolymph of tsetse flies, refractory and susceptible to infection with Trypanosoma brucei rhodesiense. Journal of Invertebrate Pathology 69, 279–281.CrossRefGoogle Scholar
O'Donnell, S., Reichardt, M. and Foster, R. ( 2000). Individual and colony factors in bumble bee division of labor (Bombus bifarius nearcticus Handl; Hymenoptera, Apidae). Insectes Sociaux 47, 164–170.CrossRefGoogle Scholar
Otterstatter, M. C., Gegear, R. J., Colla, S. and Thomson, J. D. ( 2005). Effects of parasitic mites and protozoa on the flower constancy and foraging rate of bumble bees. Behavioral Ecology and Sociobiology 58, 383–389.CrossRefGoogle Scholar
Roberts, M. G. and Heesterbeek, J. A. P. ( 1998). A simple parasite model with complicated dynamics. Journal of Mathematical Biology 37, 272–290.CrossRefGoogle Scholar
Rodd, F. H., Plowright, R. C. and Owen, R. E. ( 1980). Mortality rates of adult bumble bee workers (Hymenoptera, Apidae). Canadian Journal of Zoology 58, 1718–1721.CrossRefGoogle Scholar
SAS INSTITUTE ( 1999). SAS User's Guide, SAS Institute, Cary, North Carolina.
Schiestl, F. P. and Barrows, E. M. ( 1999). Queen and forager sizes of Bombus affinis cresson (Hymenoptera: Apidae). Proceedings of the Entomological Society of Washington 101, 880–886.Google Scholar
Schmid-Hempel, P. ( 1998). Parasites in Social Insects, Princeton University Press, Princeton, New Jersey.
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.CrossRefGoogle Scholar
Schmid-Hempel, P. ( 2005). Natural insect host-parasite systems show immune priming and specificity: puzzles to be solved. Bioessays 27, 1026–1034.CrossRefGoogle Scholar
Schmid-Hempel, P., Puhr, K., Kruger, N., Reber, C. and Schmid-Hempel, R. ( 1999). Dynamic and genetic consequences of variation in horizontal transmission for a microparasitic infection. Evolution 53, 426–434.CrossRefGoogle Scholar
Schmid-Hempel, P. and Schmid-Hempel, R. ( 1993). Transmission of a pathogen in Bombus terrestris, with a note on division of labor in social insects. Behavioral Ecology and Sociobiology 33, 319–327.Google Scholar
Sheldon, B. C. and Verhulst, S. ( 1996). Ecological immunology: Costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317–321.CrossRefGoogle Scholar
Shykoff, J. A. and Schmid-Hempel, P. ( 1991 a). Genetic relatedness and eusociality – parasite-mediated selection on the genetic composition of groups. Behavioral Ecology and Sociobiology 28, 371–376.Google Scholar
Shykoff, J. A. and Schmid-Hempel, P. ( 1991 b). Parasites and the advantage of genetic-variability within social insect colonies. Proceedings of the Royal Society of London, B 243, 55–58.Google Scholar
Siva-Jothy, M. T. and Plaistow, S. J. ( 1999). A fitness cost of eugregarine parasitism in a damselfly. Ecological Entomology 24, 465–470.CrossRefGoogle Scholar
Sokal, R. R. and Rohlf, F. J. ( 1995). Biometry, 3rd Edn. W.H. Freeman and Company, New York.
Taylor, L. H., Walliker, D. and Read, A. F. ( 1997). Mixed-genotype infections of malaria parasites: Within-host dynamics and transmission success of competing clones. Proceedings of the Royal Society of London, B 264, 927–935.CrossRefGoogle Scholar
Teitelbaum, J. E. and Walker, W. A. ( 2005). The development of mucosal immunity. European Journal of Gastroenterology and Hepatology 17, 1273–1278.CrossRefGoogle Scholar
Tyler, K. M., Higgs, P. G., Matthews, K. R. and Gull, K. ( 2001). Limitation of Trypanosoma brucei parasitaemia results from density-dependent parasite differentiation and parasite killing by the host immune response. Proceedings of the Royal Society of London, B 268, 2235–2243.CrossRefGoogle Scholar
Vizoso, D. B. and Ebert, D. ( 2004). Within-host dynamics of a microsporidium with horizontal and vertical transmission: Octosporea bayeri in Daphnia magna. Parasitology 128, 31–38.CrossRefGoogle Scholar
Williams, R. B. ( 1998). Epidemiological aspects of the use of live anticoccidial vaccines for chickens. International Journal for Parasitology 28, 1089–1098.CrossRefGoogle Scholar
Williams, R. B. ( 2001). Quantification of the crowding effect during infections with the seven Eimeria species of the domesticated fowl: its importance for experimental designs and the production of oocyst stocks. International Journal for Parasitology 31, 1056–1069.CrossRefGoogle Scholar
Wodarz, D. ( 2006). Ecological and evolutionary principles in immunology. Ecology Letters 9, 694–705.CrossRefGoogle Scholar
Woolhouse, M. E. J., Dye, C., Etard, J. F., Smith, T., Charlwood, J. D., Garnett, G. P., Hagan, P., Hii, J. L. K., Ndhlovu, P. D., Quinnell, R. J., Watts, C. H., Chandiwana, S. K. and Anderson, R. M. ( 1997). Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proceedings of the National Academy of Sciences, USA 94, 338–342.CrossRefGoogle Scholar
Woolhouse, M. E. J., Watts, C. H. and Chandiwana, S. K. ( 1991). Heterogeneities in transmission rates and the epidemiology of schistosome infection. Proceedings of the Royal Society of London, B 245, 109–114.CrossRefGoogle Scholar