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The effects of single and mixed infections of Apicystis bombi and deformed wing virus in Bombus terrestris

Published online by Cambridge University Press:  08 December 2015

PETER GRAYSTOCK Open the ORCID record for PETER GRAYSTOCK [Opens in a new window] ,
IVAN MEEUS ,
GUY SMAGGHE ,
DAVE GOULSON  and
WILLIAM O. H. HUGHES
PETER GRAYSTOCK*
Affiliation:
Institute of Integrative and Comparative Biology, University of Leeds, Leeds LS2 9JT, UK
IVAN MEEUS
Affiliation:
Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium
GUY SMAGGHE
Affiliation:
Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium
DAVE GOULSON
Affiliation:
School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK
WILLIAM O. H. HUGHES
Affiliation:
School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK
*
*Corresponding author. Institute of Integrative and Comparative Biology, University of Leeds, Leeds LS2 9JT, UK. E-mail: [email protected]
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Summary

Many pollinators are currently suffering from declines, diminishing their gene pool and increasing their vulnerability to parasites. Recently, an increasing diversity of parasites has been recorded in bumblebees, yet for many, knowledge of their virulence and hence the risk their presence poses, is lacking. The deformed wing virus (DWV), known to be ubiquitous in honey bees, has now been detected in bumblebees. In addition, the neogregarine Apicystis bombi has been discovered to be more prevalent than previously thought. Here, we assess for the first time the lethal and sublethal effects of these parasites during single and mixed infections of worker bumblebees (Bombus terrestris). Fifteen days after experimental exposure, 22% of bees exposed to A. bombi, 50% of bees exposed to DWV and 86% of bees exposed to both parasites had died. Bumblebees that had ingested A. bombi had increased sucrose sensitivity (SS) and a lower lipid:body size ratio than control bees. While dual infected bumblebees showed no increase in SS. Overall, we find that A. bombi exhibits both lethal and sublethal effects. DWV causes lethal effect and may reduce the sub lethal effects imposed by A. bombi. The results show that both parasites have significant, negative effects on bumblebee health, making them potentially of conservation concern.

Keywords

pollinatoremerging diseasepathogenneogregarineDWV
Type
Research Article
Information
Parasitology , Volume 143 , Issue 3 , March 2016 , pp. 358 - 365
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Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Alizon, S., de Roode, J. C. and Michalakis, Y. (2013). Multiple infections and the evolution of virulence. Ecology Letters 16, 556–567.Google Scholar
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
Arrese, E. L. and Soulages, J. L. (2010). Insect fat body: energy, metabolism, and regulation. Annual Review of Entomology 55, 207–25.Google 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.Google Scholar
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 Sciences of the United States of America 108, 662–7.Google Scholar
Chen, Y., Higgins, J. and Feldlaufer, M. (2005). Quantitative real-time reverse transcription-PCR analysis of deformed wing virus infection in the honeybee (Apis mellifera L.). Applied and Environmental Microbiology 71, 436.CrossRefGoogle ScholarPubMed
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
Doublet, V., Natsopoulou, M. E., Zschiesche, L. and Paxton, R. J. (2015). Within-host competition among the honey bees pathogens Nosema ceranae and Deformed wing virus is asymmetric and to the disadvantage of the virus. Journal of Invertebrate Pathology 124, 31–34.CrossRefGoogle Scholar
Evison, S. E. F., Roberts, K. E., Laurenson, L., Pietravalle, S., Hui, J., Biesmeijer, J. C., Smith, J. E., Budge, G. and Hughes, W. O. H. (2012). Pervasiveness of parasites in pollinators. PloS ONE 7, e30641.Google Scholar
Fürst, M. A., McMahon, D. P., Osborne, J. L., Paxton, R. J. and Brown, M. J. F. (2014). Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506, 364–6.CrossRefGoogle ScholarPubMed
Goulson, D. (2010). Bumblebees: Behaviour, Ecology, and Conservation. Oxford University Press, Oxford.Google Scholar
Graystock, P., Yates, K., Evison, S. E. F., Darvill, B., Goulson, D. and Hughes, W. O. H. (2013 a). The Trojan hives: Pollinator pathogens, imported and distributed in bumblebee colonies. Journal of Applied Ecology 50, 1207–1215.CrossRefGoogle Scholar
Graystock, P., Yates, K., Darvill, B., Goulson, D. and Hughes, W. O. H. (2013 b). Emerging dangers: deadly effects of an emergent parasite in a new pollinator host. Journal of Invertebrate Pathology 114, 114–119.Google Scholar
Graystock, P., Goulson, D. and Hughes, W. O. H. (2014). The relationship between managed bees and the prevalence of parasites in bumblebees. PeerJ 2, e522.Google Scholar
Graystock, P., Blane, J. E., McFrederick, Q. S., Goulson, D. and Hughes, W. O. H. (2015 a). Do managed bees drive parasite spread and emergence in wild bees? International Journal for Parasitology: Parasites and Wildlife. doi: 10.1016/j.ijppaw.2015.10.001.Google Scholar
Graystock, P., Goulson, D. and Hughes, W. O. H. (2015 b). 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. doi: 10.1098/rspb.2015.1371.Google Scholar
Iqbal, J. and Mueller, U. (2007). Virus infection causes specific learning deficits in honeybee foragers. Proceedings of the Royal Society B: Biological Sciences 274, 1517–1521.Google Scholar
Jones, C. M. and Brown, M. J. F. (2014). Parasites and genetic diversity in an invasive bumblebee. Journal of Animal Ecology 83, 1428–1440.Google Scholar
Klee, J., Tek Tay, W. 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
Kosior, A., Celary, W., Olejniczak, P., Fijal, J., Król, W., Solarz, W. and Plonka, P. (2007). The decline of the bumble bees and cuckoo bees (Hymenoptera: Apidae: Bombini) of Western and Central Europe. Oryx 41, 79–88. doi: 10.1017/S0030605307001597.CrossRefGoogle Scholar
Li, J., Peng, W., Wu, J., Strange, J. P., Boncristiani, H. and Chen, Y. (2011). Cross-species infection of deformed wing virus poses a new threat to pollinator conservation. Journal of Economic Entomology 104, 732–739.CrossRefGoogle ScholarPubMed
Lipa, J. J. and Triggiani, O. (1992). A newly recorded neogregarine (Protozoa, Apicomplexa), parasite in honey bees (Apis mellifera) and bumble bees (Bombus spp). Apidologie 23, 533–536.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.CrossRefGoogle Scholar
Liu, H. J., Macfarlane, R. P. and Pengelly, D. H. (1974). Mattesia bombi n. sp. (Neogregarinida: Ophrocystidae), a parasite of Bombus (Hymenoptera: Apidae). Journal of Invertebrate Pathology 23, 225–231.Google Scholar
Macfarlane, R. P., Lipa, J. J. and Liu, H. J. (1995). Bumble bee pathogens and internal enemies. Bee World 76, 130–148.Google Scholar
Maharramov, J., Meeus, I., Maebe, K., Arbetman, M., Morales, C., Graystock, P., Hughes, W. O. H., Plischuk, S., Lange, C. E., de Graaf, D. C., Zapata, N., de la Rosa, J. J. P., Murray, T. E., Brown, M. J. F. and Smagghe, G. (2013). Genetic variability of the neogregarine Apicystis bombi, an etiological agent of an emergent bumblebee disease. PloS ONE 8, e81475.Google Scholar
Manley, R., Boots, M. and Wilfert, L. (2015). Emerging viral disease risk to pollinating insects: ecological, evolutionary and anthropogenic factors. Journal of Applied Ecology 52, 331–340.Google Scholar
Martins, A. and Melo, G. (2010). Has the bumblebee Bombus bellicosus gone extinct in the northern portion of its distribution range in Brazil? Journal of Insect Conservation 14, 207–210.Google Scholar
McMahon, D. P., Fürst, M. a., Caspar, J., Theodorou, P., Brown, M. J. F. and Paxton, R. J. (2015). A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees. Journal of Animal Ecology 84, 615–624.Google Scholar
Meeus, I., de Graaf, D. C., Jans, K. and Smagghe, G. (2010). Multiplex PCR detection of slowly-evolving trypanosomatids and neogregarines in bumblebees using broad-range primers. Journal of Applied Microbiology 109, 107–115.Google Scholar
Meeus, I., Brown, M. J. F., de Graaf, D. C. and Smagghe, G. (2011). Effects of invasive parasites on bumble bee declines. Conservation Biology 25, 662–71.Google Scholar
Meeus, I., Mosallanejad, H., Niu, J., de Graaf, D. C., Wäckers, F. and Smagghe, G. (2014). Gamma irradiation of pollen and eradication of Israeli acute paralysis virus. Journal of Invertebrate Pathology 121, 10–13.Google Scholar
Morimoto, T., Kojima, Y., Yoshiyama, M., Kimura, K., Yang, B., Peng, G. and Kadowaki, T. (2013). Molecular detection of protozoan parasites infecting Apis mellifera colonies in Japan. Environmental Microbiology Reports 5, 74–77.CrossRefGoogle ScholarPubMed
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
Naug, D. and Gibbs, A. (2009). Behavioral changes mediated by hunger in honeybees infected with Nosema ceranae . Apidologie 40, 595–599.Google Scholar
Plischuk, S. and Lange, C. E. (2009). Invasive Bombus terrestris (Hymenoptera: Apidae) parasitized by a flagellate (Euglenozoa: Kinetoplastea) and a neogregarine (Apicomplexa: Neogregarinorida). Journal of Invertebrate Pathology 102, 263–265.Google Scholar
Plischuk, S., Martín-Hernández, R., Prieto, L., Lucía, M., Botías, C., Meana, A., Abrahamovich, A. H., Lange, C. and Higes, M. (2009). South American native bumblebees (Hymenoptera: Apidae) infected by Nosema ceranae (Microsporidia), an emerging pathogen of honeybees (Apis mellifera). Environmental Microbiology Reports 1, 131–135.Google Scholar
Plischuk, S., Meeus, I., Smagghe, G. and Lange, C. E. (2011). Apicystis bombi (Apicomplexa: Neogregarinorida) parasitizing Apis mellifera and Bombus terrestris (Hymenoptera: Apidae) in Argentina. Environmental Microbiology Reports 3, 565–568.Google Scholar
Plischuk, S., Sanscrainte, N. D., Becnel, J. J., Estep, A. S. and Lange, C. E. (2015). Tubulinosema pampeana sp. n. (Microsporidia, Tubulinosematidae), a pathogen of the South American bumble bee Bombus atratus . Journal of Invertebrate Pathology 126, 31–42.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
Ravoet, J., Maharramov, J., Meeus, I., De Smet, L., Wenseleers, T., Smagghe, G. and de Graaf, D. C. (2013). Comprehensive Bee Pathogen Screening in Belgium Reveals Crithidia mellificae as a New Contributory Factor to Winter Mortality. PloS ONE 8, e72443.CrossRefGoogle ScholarPubMed
Riveros, A. J. and Gronenberg, W. (2009). Olfactory learning and memory in the bumblebee Bombus occidentalis . Naturwissenschaften 96, 851–6.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Ryabov, E. V., Wood, G. R., Fannon, J. M., Moore, J. D., Bull, J. C., Chandler, D., Mead, A., Burroughs, N. and Evans, D. J. (2014). A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission. PLoS Pathogens 10, e1004230. doi: 10.1371/journal.ppat.1004230.Google Scholar
Scheiner, R., Page, R. E. and Erber, J. (2001). Responsiveness to sucrose affects tactile and olfactory learning in preforaging honey bees of two genetic strains. Behavioural Brain Research 120, 67–73.Google Scholar
Schmid-Hempel, P. (1998). Parasites in Social Insects. Princeton University Press.Google Scholar
Singh, R., Levitt, A. L., Rajotte, E. G., Holmes, E. C., Ostiguy, N., VanEngelsdorp, D., Lipkin, W. I., Depamphilis, C. W., Toth, A. L. and Cox-Foster, D. (2010). RNA viruses in hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PloS ONE 5, e14357.CrossRefGoogle ScholarPubMed
Tentcheva, D., Gauthier, L., Zappulla, N., Dainat, B., Cousserans, F., Colin, M. E. and Bergoin, M. (2004). Prevalence and Seasonal Variations of Six Bee Viruses in Apis mellifera L. and Varroa destructor Mite Populations in France. Applied and Environmental Microbiology 70, 7185–7191.Google Scholar
Whitehorn, P. R., Tinsley, M. C., Brown, M. J. F., Darvill, B. and Goulson, D. (2011). Genetic diversity, parasite prevalence and immunity in wild bumblebees. Proceedings of the Royal Society B: Biological Sciences 278, 1195–202.CrossRefGoogle ScholarPubMed
Williams, P. H. and Osborne, J. L. (2009). Bumblebee vulnerability and conservation world-wide. Apidologie 40, 367–387.Google Scholar
Xie, Z., Williams, P. H. and Tang, Y. (2008). The effect of grazing on bumblebees in the high rangelands of the eastern Tibetan Plateau of Sichuan. Journal of Insect Conservation 12, 695–703.Google Scholar
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