Hostname: page-component-76fb5796d-vfjqv Total loading time: 0 Render date: 2024-04-26T03:49:51.126Z Has data issue: false hasContentIssue false
  • English
  • Français

Observations of native bumble bees inside of commercial colonies of Bombus impatiens (Hymenoptera: Apidae) and the potential for pathogen spillover

Published online by Cambridge University Press:  07 June 2018

B.J. Hicks ,
B.L. Pilgrim ,
E. Perry  and
H.D. Marshall
B.J. Hicks*
Affiliation:
College of the North Atlantic, 4 Pike’s Lane, Carbonear, Newfoundland and Labrador, A1Y 1A7, Canada Department of Biology, Memorial University, St. John’s, Newfoundland and Labrador, A1B 3X9, Canada
B.L. Pilgrim
Affiliation:
Genomics and Proteomics Facility, Core Research Equipment and Instrument Training (CREAIT) Network, Memorial University, St. John’s, Newfoundland and Labrador, A1C 5S7, Canada
E. Perry
Affiliation:
Genomics and Proteomics Facility, Core Research Equipment and Instrument Training (CREAIT) Network, Memorial University, St. John’s, Newfoundland and Labrador, A1C 5S7, Canada
H.D. Marshall
Affiliation:
Department of Biology, Memorial University, St. John’s, Newfoundland and Labrador, A1B 3X9, Canada
*
1Corresponding author (e-mail: barry.hicks@cna.nl.ca).
Get access Rights & Permissions [Opens in a new window]

Abstract

Many fruit producers use commercial colonies of Bombus impatiens Cresson (Hymenoptera: Apidae) to supplement crop pollination by native bees. A small number of Newfoundland (Newfoundland and Labrador, Canada) farmers forego purchasing new colonies and, instead, purchase previously used colonies from crops in other provinces. This practice has potentially dangerous implications that may adversely affect future native bee diversity in Newfoundland. This study is the first to record the presence of native bumble bee species inside the colonies of new and pre-used commercial B. impatiens and the first to look at diseases in native bumble bees from Newfoundland. Polymerase chain reaction and taxon-specific oligonucleotides were used to screen the commercial and native bumble bee species for pathogens. Crithidia bombi (Lipa and Triggiani), Apicystis bombi (Liu, Macfarlane, and Pengelly), Nosema bombi Fantham and Porter, Nosema ceranae Fries et al., and species of Ascosphaera Olive and Spiltoir, were detected in native bumble bees that were collected from inside the new and pre-used commercial B. impatiens. Crithidia bombi, A. bombi, and N. bombi were also detected among native bees that were collected away from the commercial colonies. Nosema apis (Zander) and Melissococcus plutonius (White) were not detected in any of the bees tested. The mixing of native bumble bees in B. impatiens colonies increases the potential for pathogen spillover and spillback that may threaten the small and vulnerable island bee fauna.

Résumé

De nombreux producteurs de fruits utilisent les colonies commerciales de Bombus impatiens Cresson (Hymenoptera: Apidae) pour compléter la pollinisation des cultures par les abeilles indigènes. Un petit nombre d’agriculteurs de Terre-Neuve (Terre-Neuve-et-Labrador, Canada) renoncent à l’achat de nouvelles colonies et, au lieu de cela, achètent des colonies déjà utilisées dans les cultures d’autres provinces. Cette pratique a des implications potentiellement dangereuses qui pourraient nuire à la diversité future des abeilles indigènes à Terre-Neuve. Cette étude est la première à signaler la présence d’espèces de bourdons indigènes à l’intérieur des colonies de B. impatiens commerciales nouvelles et pré-utilisées et la première à examiner les maladies chez les bourdons indigènes de Terre-Neuve. La réaction en chaîne par polymérase et les oligonucléotides spécifiques du taxon ont été utilisés pour cribler les espèces commerciales de bourdons indigènes et les agents pathogènes. Crithidia bombi (Lipa et Triggiani), Apicystis bombi (Liu, Macfarlane et Pengelly), Nosema bombi Fantham et Porter, Nosema ceranae Fries et al., et les espèces d’Ascosphaera Olive et Spiltoir, ont été détectés chez des bourdons indigènes qui ont été recueillis à l’intérieur du B. impatiens commercial nouveau et pré-utilisé. Crithidia bombi, A. bombi et N. bombi ont également été détectés parmi les abeilles indigènes qui ont été recueillies loin des colonies commerciales. Nosema apis (Zander) et Melissococcus plutonius (White) n’ont été détectés chez aucune des abeilles testées. Le mélange de bourdons indigènes dans les colonies de B. impatiens augmente le risque de débordements et de retombées pathogènes qui pourraient menacer une petite population vulnérable d’abeilles insulaires.

Type
Biodiversity & Evolution
Information
The Canadian Entomologist , Volume 150 , Issue 4 , August 2018 , pp. 520 - 531
Copyright
© Entomological Society of Canada 2018 

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.)

Footnotes

Subject editor: Cory Sheffield

References

Alford, D.V. 1975. Bumblebees. Davis-Poynter, London, United Kingdom.Google Scholar
Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215: 403–410.Google Scholar
Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25: 3389–3402.CrossRefGoogle ScholarPubMed
Arbetman, M.P., Meeus, I., Morales, C.L., Aizen, M.A., and Smagghe, G. 2013. Alien parasite hitchhikes to Patagonia on invasive bumblebee. Biological Invasions, 15: 489–494.Google Scholar
Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemüller, R., Edwards, M., Peeters, T., et al. 2006. Parallel declines in pollinators and insect-pollinated plants in Britain and The Netherlands. Science, 313: 351–354.Google Scholar
Birmingham, A.L., Hoover, S.E., Winston, M.L., and Ydenberg, R.C. 2004. Drifting bumble bee (Hymenoptera: Apidae) workers in commercial greenhouses may be social parasites. Canadian Journal of Zoology, 82: 1843–1853.Google Scholar
Birmingham, A.L. and Winston, M.L. 2004. Orientation and drifting behaviour of bumblebees (Hymenoptera: Apidae) in commercial tomato greenhouses. Canadian Journal of Zoology, 82: 52–59.CrossRefGoogle Scholar
Bommarco, R., Lundin, O., Smith, H. G., and Rundlöf, M. 2012. Drastic historic shifts in bumble-bee community composition in Sweden. Proceedings of the Royal Society B, 279: 309–315.Google Scholar
Breeze, T.D., Bailey, A.P., Balcombe, K.G., and Potts, S.G. 2011. Pollination services in the UK: how important are honeybees? Agriculture, Ecosystems & Environment, 142: 137–143.Google Scholar
Burkle, L.A., Marlin, J.C., and Knight, T.M. 2013. Plant–pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science, 339: 1611–1615.Google Scholar
Bushmann, S.L., Drummond, F.A., Beers, L.A., and Groden, E. 2012. Wild bumblebee (Bombus) diversity and Nosema (Microsporidia: Nosematidae) infection levels associated with lowbush blueberry (Vaccinium angustifolium) production and commercial bumblebee pollinators. Psyche, Article ID 429398. http://dx.doi.org/10.1155/2012/429398.Google Scholar
Cameron, S.A., Lim, H.C., Lozier, J.D., Duennes, M.A., and Thorp, R. 2016. Test of the invasive pathogen hypothesis of bumble bee decline in North America. Proceedings of the National Academy of Science, 113: 4386–4391.CrossRefGoogle ScholarPubMed
Cameron, S.A., Lozier, J.D., Strange, J.P., Koch, J.B., Cordes, N., Solter, L.F., and Griswold, T.L. 2011. Patterns of widespread decline in North American bumble bees. Proceedings of the National Academy of Science, 108: 662–667.CrossRefGoogle ScholarPubMed
Carvalheiro, L.G., Kunin, W.E., Keil, P., Aguirre-Gutiérrez, J., Ellis, W.N., Fox, R., et al. 2013. Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants. Ecology Letters, 16: 870–878.Google Scholar
Colla, S.R., 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.Google Scholar
Colla, S.R. and Packer, L. 2008. Evidence for decline in eastern North American bumblebees (Hymenoptera: Apidae), with special focus on Bombus affinis Cresson. Biodiversity and Conservation, 17: 1379–1391.Google Scholar
Committee on the Status of Endangered Wildlife in Canada. 2010. Assessment and status report on the rusty-patched bumble bee Bombus affinis in Canada [online]. Available from www.registrelep-sararegistry.gc.ca/virtual_sara/files/cosewic/sr%5FRusty%20patched%20Bumble%20Bee%5F0810%5Fe%2Epdf [accessed 25 January 2018].Google Scholar
Committee on the Status of Endangered Wildlife in Canada. 2014a. Assessment and status report on the western bumble bee Bombus occidentalis in Canada [online]. Available from www.registrelep-sararegistry.gc.ca/virtual_sara/files/cosewic/sr%5FWestern%20Bumble%20Bee%5F2014%5Fe%2Epdf [accessed 25 January 2018].Google Scholar
Committee on the Status of Endangered Wildlife in Canada. 2014b. Assessment and status report on the gypsy cuckoo bumble bee Bombus bohemicus in Canada [online]. Available from www.registrelep-sararegistry.gc.ca/default.asp?lang=En&n=A6DF8D16-1 [accessed 2 March 2017].Google Scholar
Committee on the Status of Endangered Wildlife in Canada. 2015. Assessment and status report on the yellow-banded bumble bee Bombus terricola in Canada [online]. Available from www.registrelep-sararegistry.gc.ca/default.asp?lang=en&n=177BD170-1#_06 [accessed 2 March 2017].Google Scholar
Djordjevic, S.P., Noone, K., Smith, L., and Hornitzky, M.A.Z. 1998. Development of a hemi-nested PCR assay for the specific detection of Melissococcus plutonius . Journal of Apicultural Research, 37: 165–173.Google Scholar
Evison, S.E.F., Roberts, K.E., Laurenson, L., Pietravalle, S., Hui, J., Biesmeijer, J.C., et al. 2012. Pervasiveness of parasites in pollinators. Public Library of Science One, 7: e30641.Google Scholar
Free, J.B. 1958. The drifting of honey-bees. Journal of Agricultural Science, 51: 294–306.Google Scholar
Fürst, M.A., McMahon, D.P., Osborne, J., Paxton, R.J., and Brown, M.J.F. 2014. Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature, 506: 364–366.Google Scholar
Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R., Aizen, M.A., Bommarco, R., Cunningham, S.A., et al. 2013. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science, 339: 1608–1611.Google Scholar
Genersch, E., Yue, C., Fries, I., and de Miranda, J.R. 2006. Detection of deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. Journal of Invertebrate Pathology, 91: 61–63.Google Scholar
Gillespie, S. 2010. Factors affecting parasite prevalence among wild bumblebees. Ecological Entomology, 35: 737–747.Google Scholar
Gisder, S. and Genersch, E. 2013. Molecular differentiation of Nosema apis and Nosema ceranae based on species–specific sequence differences in a protein coding gene. Journal of Invertebrate Pathology, 113: 1–6.Google Scholar
Goulson, D. and Hughes, W.O.H. 2015. Mitigating the anthropogenic spread of bee parasites to protect wild pollinators. Biological Conservation, 191: 10–19.Google Scholar
Goulson, D., Whitehorn, P., and Fowley, M. 2012. Influence of urbanisation on the prevalence of protozoan parasites of bumblebees. Ecological Entomology, 37: 83–89.Google Scholar
Graystock, P., Goulson, D., and Hughes, W.O.H. 2015. Parasites in bloom: flowers aid dispersal and transmission of pollinator parasites within and between bee species. Proceedings of the Royal Society B: Biological Sciences, 282: 20151371.Google Scholar
Graystock, P., Meeus, I., Smagghe, G., Goulson, D., and Hughes, W.O.H. 2016. The effects of single and mixed infections of Apicystis bombi and deformed wing virus in Bombus terrestris . Parasitology, 143: 358–365.Google Scholar
Graystock, P., Yates, K., Darvill, B., Goulson, D., and Hughes, W.O.H. 2013a. Emerging dangers: deadly effects of an emergent parasite in a new pollinator host. Journal of Invertebrate Pathology, 114: 114–119.Google Scholar
Graystock, P., Yates, K., Evison, S, Darvill, B., Goulson, D., and Hughes, W.O.H. 2013b. The Trojan hives: pollinator pathogens, imported and distributed in bumblebee colonies. Journal of Applied Ecology, 50: 1207–1215.Google Scholar
Grixti, J.C., Wong, L.T., Cameron, S.A., and Favret, C. 2009. Decline of bumble bees (Bombus) in the North American Midwest. Biological Conservation, 142: 75–84.Google Scholar
Hedtke, K., Per Moestrup, J., Jensen, A.B., and Genersch, E. 2011. Evidence for emerging parasites and pathogens influencing outbreaks of stress-related diseases like chalkbrood. Journal of Invertebrate Pathology, 108: 167–173.Google Scholar
Hicks, B.J. 2011. Pollination of lowbush blueberry (Vaccinium angustifolium) in Newfoundland by native and introduced bees. Journal of the Acadian Entomological Society, 7: 108–118.Google Scholar
Hicks, B.J. and Sircom, J. 2016. Pollination of commercial cranberry (Vaccinium macrocarpon Ait.) by native and introduced managed bees in Newfoundland. Journal of the Acadian Entomological Society, 12: 22–30.Google Scholar
Higes, M., Martín-Hernández, R., Botías, C., Bailón, E.G., González-Porto, A.V., Barrios, L., et al. 2008. How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology, 10: 2659–2669.Google Scholar
Hobbs, G.A. 1966. Ecology of species of Bombus Latr. (Hymenoptera: Apidae) in southern Alberta. V. Subgenus Subterraneobombus Vogt. The Canadian Entomologist, 98: 288–294.Google Scholar
Hobbs, G.A. 1967. Ecology of species of Bombus (Hymenoptera: Apidae) in southern Alberta, vi. subgenus Pyrobombus . The Canadian Entomologist, 99: 1271–1292.Google Scholar
James, R.R. and Skinner, J.S. 2005. PCR diagnostic methods for Ascosphaera infections in bees. Journal of Invertebrate Pathology, 90: 98–103.Google Scholar
Jay, S.C. 1966. Drifting of honeybees in commercial apiaries III. Effect of apiary layout. Journal of Apicultural Research, 5: 103–112.CrossRefGoogle Scholar
Klee, J., Tay, W.T., and Paxton, R.J. 2006. Specific and sensitive detection of Nosema bombi (Microsporidia: Nosematidae) in bumble bees (Bombus spp.; Hymenoptera: Apidae) by PCR of partial rRNA gene sequences. Journal of Invertebrate Pathology, 91: 98–104.Google Scholar
Klein, A.M., Vaissière, B.E, Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C., and Tscharntke, T. 2007. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B, 274: 303–313.Google Scholar
Koh, I., Lonsdorf, E.V., Williams, N.M., Brittain, C., Isaacs, R., Gibbs, J., and Ricketts, T.H. 2016. Modeling the status, trends, and impacts of wild bee abundance in the United States. Proceedings of the National Academy of Science of the United States of America, 113: 140–145.Google Scholar
Lauro, F.M., Favaretoo, M., Covolo, L., Rassau, M., and Bertoloni, G. 2003. Rapid detection of Paenibacillus larvae from honey and hive samples with a novel nested PCR protocol. International. Journal of Microbiology, 81: 195–201.Google Scholar
Laverty, T.M. and Harder, L.D. 1988. The bumble bees of eastern Canada. The Canadian Entomologist, 120: 965–987.Google Scholar
Lefebvre, D. and Pierre, J. 2007. Demographic consequences of drift in contiguous hives of Bombus terrestris . Journal of Economic Entomology, 100: 1756–1763.Google Scholar
Lipa, J.J. and Triggiani, O. 1996. Apicystis gen nov and Apicystis bombi (Liu, Macfarlane & Pengelly) comb nov (Protozoa: Neogregarinida), a cosmopolitan parasite of Bombus and Apis (Hymenoptera: Apidae). Apidologie, 27: 29–34.Google Scholar
Lopez-Vaamonde, C., Koning, J.W., Brown, R.M., Jordan, W.C., and Bourke, A.F.G. 2004. Social parasitism by male-producing reproductive workers in a eusocial insect. Nature, 430: 557–560.Google Scholar
Malfi, R. and Roulston, T.H. 2014. Patterns of parasite infection in bumble bees (Bombus spp.) of northern Virginia. Ecological Entomology, 39: 17–29.Google Scholar
Mallinger, R.E. and Gratton, C. 2015. Species richness of wild bees, but not the use of managed honeybees, increases fruit set of a pollinator-dependent crop. Journal of Applied Ecology, 52: 323–330.Google Scholar
Maxfield-Taylor, S.A., Mujic, A.B., and Rao, S. 2015. First detection of the larval chalkbrood disease pathogen Ascosphaera apis (Ascomycota: Eurotiomycetes: Ascosphaerales) in adult bumble bees. Public Library of Science One, 10: e0124868.Google Scholar
Meeus, I., Smagghe, G., Siede, R., Jans, K., and de Graaf, D.C. 2010. Multiplex RT-PCR with broad-range primers and an exogenous internal amplification control for the detection of honeybee viruses in bumblebees. Journal of Invertebrate Pathology, 105: 200–203.Google Scholar
Murray, T.E., Coffey, M.F., Kehoe, E., and Horgan, F.G. 2013. Pathogen prevalence in commercially reared bumble bees and evidence of spillover in conspecific populations. Biological Conservation, 159: 269–276.Google Scholar
Neumann, P., Moritz, R.F.A., and Mautz, D. 2000. Colony evaluation is not affected by drifting of drone and worker honeybees (Apis mellifera L.) at a performance testing apiary. Apidologie, 31: 67–79.CrossRefGoogle Scholar
Niwa, S., Iwano, H., Asada, S., Matsuura, M., and Goka, K. 2004. A microsporidian pathogen isolated from a colony of the European bumblebee, Bombus terrestris, and infectivity on Japanese bumblebee. Japanese Journal of Applied Entomology and Zoology, 48: 60–64.Google Scholar
O’Connor, S., Park, K.J., and Goulson, D. 2013. Worker drift and egg dumping by queens in wild Bombus terrestris colonies. Behavioral Ecology and Sociobiology, 67: 621–627.Google Scholar
Otterstatter, M.C. and Thomson, J.D. 2008. Does pathogen spillover from commercially reared bumble bees threaten wild pollinators? Public Library of Science One, 3: e2771.Google Scholar
Otti, O. and Schmid-Hempel, P. 2007. Nosema bombi: a pollinator parasite with detrimental fitness effects. Journal of Invertebrate Pathology, 96: 118–124.CrossRefGoogle ScholarPubMed
Otti, O. and 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.Google Scholar
Pfeiffer, K.J. and Crailsheim, K. 1998. Drifting of honeybees. Insectes Sociaux, 45: 151–167.Google Scholar
Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O., and Kunin, W.E. 2010. Global pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution, 25: 345–353.Google Scholar
Potts, S.G., Imperatriz-Fonseca, V., Ngo, H.T., Aizen, M.A., Biesmeijer, J.C., Breeze, T.D., et al. 2016. Safeguarding pollinators and their values to human well-being. Nature, 540: 220–229.Google Scholar
Rutrecht, S.T. and Brown, M.J.F. 2008. The life-history impact and implications of multiple parasites for bumble bee queens. International Journal for Parasitology, 38: 799–808.Google Scholar
Sachman-Ruiz, B., Narváez-Padilla, N., and Reynaud, E. 2015. Commercial Bombus impatiens as reservoirs of emerging infectious diseases in central México. Biological Invasions, 17: 2043–2053.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.Google Scholar
Schmid-Hempel, R. and Tognazzo, M. 2010. Molecular divergence defines two distinct lineages of Crithidia bombi (Trypanosomatidae), parasites of bumblebees. Journal of Eukaryotic Microbiology, 57: 337–345.Google Scholar
Sheffield, C.S., Heron, J., Gibbs, J., Onuferko, T.M., Oram, R., Best, L., et al. 2017. Contribution of DNA barcoding to the study of the bees (Hymenoptera: Apoidea) of Canada: progress to date. The Canadian Entomologist, 149: 736–754.Google Scholar
Shutler, D., Head, K., Burgher-MacLellan, K.L., Colwell, M.J., Levitt, A.L., Ostiguy, N., and Williams, G.R. 2014. Honey bee Apis mellifera parasites in the absence of Nosema ceranae fungi and Varroa destructor mites. Public Library of Science One, 9: e98599.Google Scholar
Stephen, W.P., Vandenberg, J.D., and Fichter, B.L. 1981. Etiology and epizootiology of chalkbrood in the leafcutting bee, Megachile rotundata (Fabricius), with notes on Ascosphaera species. Technical report. Oregon State University Agricultural Experimental Station Bulletin, 653: 1–10.Google Scholar
Szabo, N.D., Colla, S.R., Wagner, D.L., Gall, L.F., and Kerr, J.T. 2012. Do pathogen spillover, pesticide use, or habitat loss explain recent North American bumblebee declines. Conservation Letters, 5: 232–239.Google Scholar
Takahashi, J., Martin, S.J., Ono, M., and Shimizu, I. 2010. Male production by non-natal workers in the bumblebee, Bombus deuteronymus (Hymenoptera: Apidae). Journal of Ethology, 28: 61–66.Google Scholar
Wynns, A.A., Jensen, A.B., and Eilenberg, J. 2013. Ascosphaera callicarpa, a new species of bee-loving fungus, with a key to the genus for Europe. Public Library of Science One, 8: e73419.Google Scholar