Behavioral Ecology and Sociobiology

, Volume 58, Issue 4, pp 383–389 | Cite as

Effects of parasitic mites and protozoa on the flower constancy and foraging rate of bumble bees

  • Michael C. OtterstatterEmail author
  • Robert J. Gegear
  • Sheila R. Colla
  • James D. Thomson
Original Article


Parasites can affect host behavior in subtle but ecologically important ways. In the laboratory, we conducted experiments to determine whether parasitic infection by the intestinal protozoan Crithidia bombi or the tracheal mite Locustacarus buchneri alters the foraging behavior of the bumble bee Bombus impatiens. Using an array of equally rewarding yellow and blue artificial flowers, we measured the foraging rate (flowers visited per minute, flower handling time, and flight time between flowers) and flower constancy (tendency to sequentially visit flowers of the same type) of bees with varying intensities of infection. Bumble bee workers infected with tracheal mites foraged as rapidly as uninfected workers, but were considerably more constant to a single flower type (yellow or blue). In contrast, workers infected with intestinal protozoa showed similar levels of flower constancy, but visited 12% fewer flowers per minute on average than uninfected bees. By altering the foraging behavior of bees, such parasites may influence interactions between plants and pollinators, as well as the reproductive output of bumble bee colonies. Our study is the first to investigate the effects of parasitic protozoa and tracheal mites on the foraging behavior of bumble bees, and provides the first report of Crithidia bombi in commercial bumble bees in North America.


Behavior Bombus Crithidia bombi Foraging Locustacarus buchneri Parasites 


  1. Brodeur J, McNeil JN (1992) Host behavior modification by the endoparasitoid Aphidius nigripes—a strategy to reduce hyperparasitism. Ecol Entomol 17:97–104Google Scholar
  2. Brown MJF, Loosli R, Schmid-Hempel P (2000) Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91:421–427CrossRefGoogle Scholar
  3. 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 72:994–1002CrossRefGoogle Scholar
  4. Chittka L, Thomson JD, Waser NM (1999) Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86:361–377CrossRefGoogle Scholar
  5. Durrer S, Schmid-Hempel P (1994) Shared use of flowers leads to horizontal pathogen transmission. Proceedings of the Royal Society of London Series B 258:299–302Google Scholar
  6. Feore SM, Bennett M, Chantrey J, Jones T, Baxby D, Begon M (1997) The effect of cowpox virus infection on fecundity in bank voles and wood mice. Proceedings of the Royal Society of London Series B 264:1457–1461CrossRefPubMedGoogle Scholar
  7. Gegear RJ, Laverty TM (1998) How many flower types can bumble bees work at the same time? Can J Zool 76:1358–1365CrossRefGoogle Scholar
  8. Gegear RJ, Otterstatter MC, Thomson JD(in press) Does infection by an intestinal parasite impair the ability of bumble bees to learn flower handling skills? Anim Behav, in pressGoogle Scholar
  9. Gegear RJ, Thomson JD (2004) Does the flower constancy of bumble bees reflect foraging economics? Ethology 110:793–805CrossRefGoogle Scholar
  10. Goka K, Okabe K, Niwa S, Yoneda M (2000) Parasitic mite infestation in introduced colonies of European bumblebees, Bombus terrestris. Jap J Appl Entomol Zool 44:47–50CrossRefGoogle Scholar
  11. Goulson D (1999) Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution. Perspec Plant Ecol, Syst Evol 2:185–209Google Scholar
  12. Goulson D (2003) Bumblebees: their behaviour and ecology. Oxford University Press, OxfordGoogle Scholar
  13. Gunn A, Irvine RJ (2003) Subclinical parasitism and ruminant foraging strategies—a review. Wildlife Soc Bull 31:117–126Google Scholar
  14. Harrison JF, Camazine S, Marden JH, Kirkton SD, Rozo A, Yang XL (2001) Mite not make it home: Tracheal mites reduce the safety margin for oxygen delivery of flying honeybees. J Exper Biol 204:805–814Google Scholar
  15. Heinrich B (1979) Bumblebee economics. Harvard University Press, CambridgeGoogle Scholar
  16. Holmes JC, Zohar S (1990) Pathology and host behaviour. In: Behnke JM (ed) Parasitism and host behaviour. Taylor and Francis, London, pp 34–63Google Scholar
  17. Husband RW, Sinha RN (1970) A revision of genus Locustacarus with a key to genera of family Podapolipidae (Acarina). Ann Entomol Soc Am 63:1152–1162Google Scholar
  18. 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 Sociaux 46:233–238CrossRefGoogle Scholar
  19. SAS Institute (1999) SAS User’s Guide. SAS Institute, Cary, North CarolinaGoogle Scholar
  20. Ives AR, Murray DL (1997) Can sublethal parasitism destabilize predator-prey population dynamics? A model of snowshoe hares, predators and parasites. J Anim Ecol 66:265–278Google Scholar
  21. Karban R, English-Loeb G (1997) Tachinid parasitoids affect host plant choice by caterpillars to increase caterpillar survival. Ecology 78:603–611Google Scholar
  22. Laverty TM (1994) Bumble Bee Learning and Flower Morphology. Anim Behav 47:531–545CrossRefGoogle Scholar
  23. Lipa JJ, Triggiani O (1980) Crithidia bombi sp n. A flagellated parasite of a bumble-bee Bombus terrestris L. (Hymenoptera, Apidae). Acta Protozoologica 27:287–290Google Scholar
  24. Moore J (2002) Parasites and the behaviour of animals. Oxford University Press, OxfordGoogle Scholar
  25. Muller CB, Schmid-Hempel P (1992a) Correlates of reproductive success among field colonies of Bombus lucorum - the importance of growth and parasites. Ecol Entomol 17:343–353Google Scholar
  26. Muller CB, Schmid-Hempel P (1992b) Variation in life-history pattern in relation to worker mortality in the bumblebee, Bombus lucorum. Functional Ecol 6:48–56Google Scholar
  27. Otterstatter MC, Whidden TL (2004) Patterns of parasitism by tracheal mites (Locustacarus buchneri) in natural bumble bee populations. Apidologie 35:351–357CrossRefGoogle Scholar
  28. Poulin R, Brodeur J, Moore J (1994) Parasite manipulation of host behavior—should hosts always lose? Oikos 70:479–484Google Scholar
  29. Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton, NJGoogle Scholar
  30. Schmid-Hempel P (2001) On the evolutionary ecology of host-parasite interactions: addressing the question with regard to bumblebees and their parasites. Naturwissenschaften 88:147–158CrossRefPubMedGoogle Scholar
  31. Schmid-Hempel P, Schmid-Hempel R (1990) Endoparasitic larvae of conopid flies alter pollination behavior of bumblebees. Naturwissenschaften 77:450–452CrossRefGoogle Scholar
  32. Schmid-Hempel P, Stauffer HP (1998) Parasites and flower choice of bumblebees. Anim Behav 55:819–825CrossRefPubMedGoogle Scholar
  33. Schmid-Hempel R, Schmid-Hempel P (1991) Endoparasitic flies, pollen-collection by bumblebees and a potential host-parasite conflict. Oecologia 87:227–232CrossRefGoogle Scholar
  34. Shykoff JA, Schmid-Hempel P (1991) Incidence and effects of four parasites in natural populations of bumble bees in Switzerland. Apidologie 22:117–125Google Scholar
  35. Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W.H. Freeman and Company, New YorkGoogle Scholar
  36. Stamp NE (1981) Behavior of parasitized aposematic caterpillars: advantages to the parasitoid or the host? Am Naturalist 118:715–725CrossRefGoogle Scholar
  37. Sutcliffe GH, Plowright RC (1988) The Effects of food supply on adult size in the bumble bee Bombus terricola Kirby (Hymenoptera, Apidae). Can Entomol 120:1051–1058Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Michael C. Otterstatter
    • 1
    Email author
  • Robert J. Gegear
    • 1
  • Sheila R. Colla
    • 1
  • James D. Thomson
    • 1
  1. 1.Department of ZoologyUniversity of TorontoTorontoCanada

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