Covert Deformed Wing Virus Infections Have Long-term Deleterious Effects on Honeybee Foraging and Survival

Overview

Journal Proc Biol Sci

Specialty Biology

Date 2017 Feb 3

PMID 28148747

Citations 63

Authors

Kristof Benaets

Anneleen Van Geystelen

Dries Cardoen

Lina De Smet

Dirk C de Graaf

Liliane Schoofs

Maarten H D Larmuseau

Laura E Brettell

Stephen J Martin

Tom Wenseleers

Affiliations

Soon will be listed here.

Abstract

Several studies have suggested that covert stressors can contribute to bee colony declines. Here we provide a novel case study and show using radiofrequency identification tracking technology that covert deformed wing virus (DWV) infections in adult honeybee workers seriously impact long-term foraging and survival under natural foraging conditions. In particular, our experiments show that adult workers injected with low doses of DWV experienced increased mortality rates, that DWV caused workers to start foraging at a premature age, and that the virus reduced the workers' total activity span as foragers. Altogether, these results demonstrate that covert DWV infections have strongly deleterious effects on honeybee foraging and survival. These results are consistent with previous studies that suggested DWV to be an important contributor to the ongoing bee declines in Europe and the USA. Overall, our study underlines the strong impact that covert pathogen infections can have on individual and group-level performance in bees.

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References

Whitehorn P, OConnor S, Wackers F, Goulson D . Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science. 2012; 336(6079):351-2. DOI: 10.1126/science.1215025. View

Shen M, Yang X, Cox-Foster D, Cui L . The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees. Virology. 2005; 342(1):141-9. DOI: 10.1016/j.virol.2005.07.012. View

Ravoet J, Smet L, Meeus I, Smagghe G, Wenseleers T, de Graaf D . Widespread occurrence of honey bee pathogens in solitary bees. J Invertebr Pathol. 2014; 122:55-8. DOI: 10.1016/j.jip.2014.08.007. View

Maori E, Paldi N, Shafir S, Kalev H, Tsur E, Glick E . IAPV, a bee-affecting virus associated with Colony Collapse Disorder can be silenced by dsRNA ingestion. Insect Mol Biol. 2009; 18(1):55-60. DOI: 10.1111/j.1365-2583.2009.00847.x. View

Wolf S, McMahon D, Lim K, Pull C, Clark S, Paxton R . So near and yet so far: harmonic radar reveals reduced homing ability of Nosema infected honeybees. PLoS One. 2014; 9(8):e103989. PMC: 4123971. DOI: 10.1371/journal.pone.0103989. View

Cardoen D, Ernst U, Boerjan B, Bogaerts A, Formesyn E, de Graaf D . Worker honeybee sterility: a proteomic analysis of suppressed ovary activation. J Proteome Res. 2012; 11(5):2838-50. DOI: 10.1021/pr201222s. View

Li Z, Chen Y, Zhang S, Chen S, Li W, Yan L . Viral infection affects sucrose responsiveness and homing ability of forager honey bees, Apis mellifera L. PLoS One. 2013; 8(10):e77354. PMC: 3795060. DOI: 10.1371/journal.pone.0077354. View

Smet L, Ravoet J, de Miranda J, Wenseleers T, Mueller M, Moritz R . BeeDoctor, a versatile MLPA-based diagnostic tool for screening bee viruses. PLoS One. 2012; 7(10):e47953. PMC: 3483297. DOI: 10.1371/journal.pone.0047953. View

Natsopoulou M, McMahon D, Paxton R . Parasites modulate within-colony activity and accelerate the temporal polyethism schedule of a social insect, the honey bee. Behav Ecol Sociobiol. 2016; 70:1019-1031. PMC: 4917585. DOI: 10.1007/s00265-015-2019-5. View

10.

Mockel N, Gisder S, Genersch E . Horizontal transmission of deformed wing virus: pathological consequences in adult bees (Apis mellifera) depend on the transmission route. J Gen Virol. 2010; 92(Pt 2):370-7. DOI: 10.1099/vir.0.025940-0. View

11.

Mayack C, Naug D . Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. J Invertebr Pathol. 2009; 100(3):185-8. DOI: 10.1016/j.jip.2008.12.001. View

12.

Dainat B, Evans J, Chen Y, Gauthier L, Neumann P . Predictive markers of honey bee colony collapse. PLoS One. 2012; 7(2):e32151. PMC: 3285648. DOI: 10.1371/journal.pone.0032151. View

13.

McMenamin A, Genersch E . Honey bee colony losses and associated viruses. Curr Opin Insect Sci. 2020; 8:121-129. DOI: 10.1016/j.cois.2015.01.015. View

14.

Hunter W, Ellis J, vanEngelsdorp D, Hayes J, Westervelt D, Glick E . Large-scale field application of RNAi technology reducing Israeli acute paralysis virus disease in honey bees (Apis mellifera, Hymenoptera: Apidae). PLoS Pathog. 2011; 6(12):e1001160. PMC: 3009593. DOI: 10.1371/journal.ppat.1001160. View

15.

Wells T, Wolf S, Nicholls E, Groll H, Lim K, Clark S . Flight performance of actively foraging honey bees is reduced by a common pathogen. Environ Microbiol Rep. 2016; 8(5):728-737. PMC: 5091639. DOI: 10.1111/1758-2229.12434. View

16.

de Miranda J, Fries I . Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). J Invertebr Pathol. 2008; 98(2):184-9. DOI: 10.1016/j.jip.2008.02.004. View

17.

Perry C, Sovik E, Myerscough M, Barron A . Rapid behavioral maturation accelerates failure of stressed honey bee colonies. Proc Natl Acad Sci U S A. 2015; 112(11):3427-32. PMC: 4371971. DOI: 10.1073/pnas.1422089112. View

18.

Iqbal J, Mueller U . Virus infection causes specific learning deficits in honeybee foragers. Proc Biol Sci. 2007; 274(1617):1517-21. PMC: 2176156. DOI: 10.1098/rspb.2007.0022. View

19.

McMahon D, Natsopoulou M, Doublet V, Furst M, Weging S, Brown M . Elevated virulence of an emerging viral genotype as a driver of honeybee loss. Proc Biol Sci. 2016; 283(1833). PMC: 4936039. DOI: 10.1098/rspb.2016.0811. View

20.

Goulson D, Nicholls E, Botias C, Rotheray E . Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science. 2015; 347(6229):1255957. DOI: 10.1126/science.1255957. View