Patterns of parasite infection in bumble bees (Bombus spp.) of Northern Virginia

Ecological Entomology

Volumn 39, Issue 1, 2014, Pages 17-29

  Malfi, Rosemary L ^a   Roulston, T'Ai H ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Bombus; Bumble bee; Conopidae; Crithidia; Nosema; Parasitism

Indexed keywords

BODY SIZE; DISEASE INCIDENCE; DISEASE PREVALENCE; FLY; GRASSLAND; INFECTIOUS DISEASE; MEADOW; PARASITISM; PATHOGENICITY; POPULATION DECLINE; SEASONAL VARIATION;

UNITED STATES; VIRGINIA;

APOIDEA; BOMBUS (GENUS); BOMBUS FERVIDUS; CONOPIDAE; CRITHIDIA; NOSEMA;

EID: 84891827640     PISSN: 03076946     EISSN: 13652311     Source Type: Journal    
DOI: 10.1111/een.12069     Document Type: Article

References (65)

1. Ascher, J.S. & Pickering, J. (2013) Discover Life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila) [Access Online] [WWW document]. URL http://www.discoverlife.org [accessed on 15 January 2013].
2. Bartomeus, I., Ascher, J.S., Gibbs, J., Danforth, B.N., Wagner, D.L., Hedtke, S.M. et al. (2013) Historical changes in northeastern US bee pollinators related to shared ecological traits. Proceedings of the National Academy of Sciences, 110, 4656-4660.
3. Brown, M.J.F. (2011) The trouble with bumblebees. Nature, 469, 169-170.
4. Brown, M.J.F., Loosli, R. & Schmid-Hempel, P. (2000) Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos, 91, 421-427.
5. Brown, M.J.F., Schmid-Hempel, R. & Schmid-Hempel, P. (2003) Strong context-dependent virulence in a host-parasite system: reconciling genetic evidence with theory. Journal of Animal Ecology, 72, 994-1002.
6. Cameron, S.A., Lozier, J.D., Strange, J. P., Koch, J.B., Cordes, N., Solter, L. F. & Griswold, T.L. (2011) Patterns of widespread decline in North American bumble bees. Proceedings of the National Academy of Sciences, 108, 662-667.
7. Colla, S.R. & Dumesh, S. (2010) The bumble bees of southern Ontario: notes on natural history and distribution. Journal of the Entomological Society of Ontario, 141, 38-67.
8. Colla, S.R. & Packer, L. (2008) Evidence for decline in eastern North American bumblebees (Hymenoptera: Apidae), with special focus on Bombus affinis Cresson. Biodiversity Conservation, 17, 1379-1391.
9. Colla, S.R., Otterstatter, M.C., Gegear, R.J. & Thomson, J.D. (2006) Plight of the bumble bee: pathogen spillover from commercial to wild populations. Biological Conservation, 129, 461-467.
10. Colla, S.R., Gadallah, F., Richardson, L.F., Wagner, D. & Gall, L. (2012) Assessing declines of North American bumble bees (Bombus spp.) using museum specimens. Biodiversity and Conservation, 21, 3585-3595.
11. Cordes, N., Huang, W., Strange, J.P., Cameron, S.A., Griswold, T.L., Lozier, J.D. et al. (2012) Interspecific geographic distribution and variation of the pathogens Nosema bombi and Crithidia species in the United States bumble bee populations. Journal of Invertebrate Pathology, 109, 206-216.
12. Couvillion, M.J., Jandt, J.M., Duong, N.H.I. & Dornhaus, A. (2010) Ontogency of worker body size distribution in bumble bee (Bombus impatiens) colonies. Ecological Entomology, 35, 424-435.
13. 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, 299-302.
14. Evans, E., Thorp, R.W., Jepsen, S. & Black, S.H. (2008) Status Review of Three Formerly Common Species of Bumble Bee in the Subgenus Bombus. Xerces Society, Portland, Oregon.
15. Fisher, R.M. (1989) Incipient colony manipulation, Nosema incidence and colony productivity of the bumble bee Bombus terrestris (Hymenoptera, Apidae). Journal of the Kansas Entomological Society, 62, 581-589.
16. Gegear, R.J., Otterstatter, M.C. & Thomson, J.D. (2005) Does parasitic infection impair the ability of bumblebees to learn flower-handling techniques? Animal Behaviour, 70, 209-215.
17. Gegear, R.J., Otterstatter, M.C. & Thomson, J.D. (2006) Bumble-bee foragers infected by a gut parasite have an impaired ability to utilize floral information. Proceedings of the Royal Society B, 273, 1073-1078.
18. Gillespie, S. (2010) Factors affecting parasite prevalence among wild bumblebees. Ecological Entomology, 35, 737-747.
19. Goulson, D. (2010) Bumblebees: Behavior, Ecology, and Conservation. Oxford University Press, Oxford, U.K.
20. Goulson, D. & Darvill, B. (2004) Niche overlap and diet breadth in bumblebees; are rare species more specialized in their choice of flowers? Apidologie, 35, 55-63.
21. Goulson, D., Hanley, M.E., Darvill, B., Ellis, J.S. & Knight, M.E. (2005) Causes of rarity in bumblebees. Biological Conservation, 122, 1-8.
22. Goulson, D., Lye, G.C. & Darvill, B. (2008) Decline and conservation of bumble bees. Annual Review of Entomology, 53, 191-208.
23. Greenleaf, S. & Kremen, C. (2006) Wild bee species increase tomato production and respond differently to surrounding land use in Northern California. Biological Conservation, 133, 81-87.
24. Grixti, J.C., Wong, L.T., Cameron, S.A. & Favret, C. (2009) Decline of bumble bees (Bombus) in the North American Midwest. Biological Conservation, 142, 75-84.
25. 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, 233-238.
26. Kearns, C. & Thomson, J.D. (2001) The Natural History of Bumblebees: A Sourcebook for Investigations. University Press of Colorado, Boulder, Colorado.
27. Kissinger, C.N., Cameron, S.A., Thorp, R.W., White, B. & Solter, L.F. (2011) Survey of bumble bee (Bombus) pathogens and parasites in Illinois and selected areas of northern California and southern Oregon. Journal of Invertebrate Pathology, 107, 220-224.
28. Knee, W.J. & Medler, J.T. (1965) The seasonal size increase of bumblebee workers (Hymenoptera: Bombus). The Canadian Entomologist, 97, 1149-1155.
29. Korner, P. & Schmid-Hempel, P. (2005) Correlates of parasite load in bumblebees in an Alpine habitat. Entomological Science, 8, 151-160.
30. Kremen, C., Williams, N.M., Bugg, R.L., Fay, J.P. & Thorp, R.W. (2004) The area requirements of an ecosystem service: crop pollination by native bee communities in California. Ecology Letters, 7, 1109-1119.
31. Li, J., Chen, W., Wu, J., Peng, W., An, J., Schmid-Hempel, P. & Schmid-Hempel, R. (2012) Diversity of Nosema associated with bumblebees (Bombus spp.) from China. International Journal of Parasitology 42(): 49-61.
32. Lozier, J.D. & Cameron, S.A. (2009) Comparative genetic analyses of historical and contemporary collections highlight contrasting geographic histories for the bumble bees Bombus pensylvanicus and B. impatiens in Illinois. Molecular Ecology, 18, 1875-1886.
33. MacFarlane, R.P. & Pengelly, D.H. (1974) Conopidae and Sarcophidae (Diptera) as parasites of adult Bombinae (Hymenoptera) in Ontario. Proceedings of the Entomological Society of Ontario, 105, 55-59.
34. Maeta, Y. & MacFarlane, R.P. (1993) Japanese Conopidae (Diptera): their biology, overall distribution, and role as parasites of bumble bees (Hymenoptera, Apidae). Japanese Journal of Entomology, 61, 493-509.
35. Memmott, J., Waser, N.M. & Price, M.V. (2004) Tolerance of pollination networks to species extinctions. Proceedings of the Royal Society of London Series B, 271, 2605-2611.
36. Mitchell, T.B. (1962) Bees of the Eastern United States, Vol. II. Technical Bulletin No. 152. The North Carolina Agricultural Experiment Station, Raleigh, North Carolina.
37. Muller, C.B. & Schmid-Hempel, P. (1992) Correlates of reproductive success among field colonies of Bombus lucorum: the importance of growth and parasites. Ecological Entomology, 17, 343-353.
38. Muller, C.B., Blackburn, T.M. & Schmid-Hempel, P. (1996) Field evidence that host selection by conopid parasitoids is related to host body size. Insectes Sociaux, 43, 227-233.
39. Otterstatter, M.C. (2004) Patterns of parasitism among conopid flies parasitizing bumblebees. Entomologia Experimentalis et Applicata, 11, 135-139.
40. Otterstatter, M.C. & Thomson, J.D. (2008) Does pathogen spillover from commercially reared bumble bees threaten wild pollinators. PLoS One, 3, e2771.
41. Otterstatter, M.C., Whidden, T.L. & Owen, R.E. (2002) Contrasting frequencies of parasitism and host mortality among phorid and conopid parasitoids of bumble-bees. Ecological Entomology, 27, 229-237.
42. Otterstatter, M.C., Gegear, R.J., Colla, S.R. & Thomson, J.D. (2005) Effects of parasitic mites and protozoa on the flower constancy and foraging rates of bumble bees. Behavioral Ecology and Sociobiology, 58, 383-389.
43. Otti, O. & Schmid-Hempel, P. (2007) Nosema bombi: a pollinator parasite with detrimental fitness effects. Journal of Invertebrate Pathology, 96, 118-124.
44. Otti, O. & Schmid-Hempel, P. (2008) A field experiment on the effect of Nosema bombi in colonies of the bumblebee Bombus terrestris. Ecological Entomology, 33, 577-582.
45. Plischuk, S., Martín-Hernández, R., Prieto, L., Lucía, M., Botías, C., Meana, A. et al. (2009) South American native bumblebees (Hymenoptera: Apidae) infected by Nosema ceranae, an emerging pathogen of honeybees (Apis mellifera). Environmental Microbiology, 1, 131-135.
46. Reed, D.A., Luhring, K.A., Stafford, C.A., Hansen, A.K., Millar, J.G., Hanks, L.M. et al. (2007) Host defensive response against an egg parasitoid involves cellular encapsulation and melanization. Biological Control, 41, 214-222.
47. Rutrecht, S.T. & Brown, M.J.F. (2009) Differential virulence in a multiple-host parasite of bumble bees: resolving the paradox of parasite survival? Oikos, 118, 941-949.
48. SAS Institute Inc. (2008) SAS/STAT 9.2 User's Guide. SAS Institute Inc, Cary, NC.
49. Schmid-Hempel, P. & Durrer, S. (1991) Parasites, floral resources, and reproduction in natural-populations of bumblebees. Oikos, 62, 342-350.
50. Schmid-Hempel, P. & Schmid-Hempel, R. (1988) Parasitic flies (Conopidae, Diptera) may be important stress factors for the ergonomics of their bumblebee hosts. Ecological Entomology, 13, 469-472.
51. Schmid-Hempel, R. & Schmid-Hempel, P. (1989) Superparasitism and larval competition in conopid flies (Dipt., Conopidae), parasitizing bumblebees (Hym., Apidae). Mitteilungen der Schweizerischen entomologischen Gesellschaft, 62, 279-289.
52. Schmid-Hempel, P. & Schmid-Hempel, R. (1990) Endoparasitic larvae of conopid flies alter pollination behavior of bumblebees. Naturwissenschaften, 77, 450-452.
53. Schmid-Hempel, R. & Schmid-Hempel, P. (1991) Endoparasitic flies, pollen-collection by bumblebees, and a potential host-parasite conflict. Oecologia, 87, 227-232.
54. Schmid-Hempel, R. & Schmid-Hempel, P. (1996) Host choice and fitness correlates for conopid flies parasitizing bumblebees. Oecologia, 107, 71-78.
55. Schmid-Hempel, P. & Stauffer, H. (1998) Parasites and flower choice of bumblebees. Animal Behavior, 55, 819-825.
56. Schmid-Hempel, R. & Tognazzo, M. (2010) Molecular divergence defines two distinct lineages of Crithidia bombi (Trypanosomatidae), parasites of bumblebees. Journal of Eukaryotic Microbiology, 57, 337-345.
57. Schmid-Hempel, P., Muller, C., Schmid-Hempel, R. & Shykoff, J.A. (1990) Frequency and ecological correlates of parasitism by conopid flies (Conopidae, Diptera) in populations of bumblebees. Insectes Sociaux, 37, 14-30.
58. Shykoff, J.A. & Schmid-Hempel, P. (1991a) Parasites delay worker reproduction in bumblebees-consequences for eusociality. Behavioral Ecology, 2, 242-248.
59. Shykoff, J.A. & Schmid-Hempel, P. (1991b) Incidence and effects of four parasites in populations of bumble bees in Switzerland. Apidologie, 2, 242-248.
60. Smilanich, A.M., Mason, P.A., Sprung, L., Chase, T.R. & Singer, M.S. (2011) Complex effects of parasitoids on pharmacophagy and diet choice of a polyphagous caterpillar. Oecologia, 165, 995-1005.
61. Solter, L.F., Becnel, J.J., & Vavra, J. (2012) Research methods for entomopathogenic microsporidia and other protists Manual of Techniques in Invertebrate Pathology, 2nd edn (ed. by Lacy, L.A.). Academic Press, London, U.K.
62. Stanghellini, M.S., Ambrose, J.T. & Schultheis, J.R. (1997) The effects of honey bee and bumble bee pollination on fruit set and abortion of cucumber and watermelon. American Bee Journal, 137, 386-391.
63. Szabo, N.D., Colla, S.R., Wagner, D.L., Gall, L.F. & Kerr, J.T. (2012) Do pathogen spillover, pesticide use, or habitat loss explain recent North American bumblebee declines? Conservation Letters, 5, 232-239.
64. USDA (2007) Census of Agriculture. United States Department of Agriculture, Washington, District of Columbia.
65. Williams, P.H., Colla, S. & Zhenghua, X. (2009) Bumblebee vulnerability: common correlates of winners and losers across three continents. Conservation Biology, 23, 931-940.