Flowers as viral hot spots: Honey bees (Apis mellifera) unevenly deposit viruses across plant species
Autoři:
Samantha A. Alger aff001; P. Alexander Burnham aff001; Alison K. Brody aff001
Působiště autorů:
Biology Department, University of Vermont, Burlington, Vermont, United States of America
aff001
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0221800
Souhrn
RNA viruses, once considered specific to honey bees, are suspected of spilling over from managed bees into wild pollinators; however, transmission routes are largely unknown. A widely accepted yet untested hypothesis states that flowers serve as bridges in the transmission of viruses between bees. Here, using a series of controlled experiments with captive bee colonies, we examined the role of flowers in bee virus transmission. We first examined if honey bees deposit viruses on flowers and whether bumble bees become infected after visiting contaminated flowers. We then examined whether plant species differ in their propensity to harbor viruses and if bee visitation rates increase the likelihood of virus deposition on flowers. Our experiment demonstrated, for the first time, that honey bees deposit viruses on flowers. However, the two viruses we examined, black queen cell virus (BQCV) and deformed wing virus (DWV), were not equally distributed across plant species, suggesting that differences in floral traits, virus ecology and/or foraging behavior may mediate the likelihood of deposition. Bumble bees did not become infected after visiting flowers previously visited by honey bees suggesting that transmission via flowers may be a rare occurrence and contingent on multiplicative factors and probabilities such as infectivity of virus strain across bee species, immunocompetence, virus virulence, virus load, and the probability a bumble bee will contact a virus particle on a flower. Our study is among the first to experimentally examine the role of flowers in bee virus transmission and uncovers promising avenues for future research.
Klíčová slova:
Biology and life sciences – Organisms – Eukaryota – Animals – Invertebrates – Arthropoda – Insects – Hymenoptera – Bees – Honey bees – Plants – Flowering plants – Viruses – RNA viruses – Plant science – Plant anatomy – Flowers – Inflorescences – Psychology – Behavior – Animal behavior – Foraging – Zoology – Social sciences
Zdroje
1. Goulson D, Nicholls E, Botías C, Rotheray EL. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Sciencexpress. 2015;2010: 1–16.
2. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE. Global pollinator declines: Trends, impacts and drivers. Trends Ecol Evol. 2010;25: 345–353. doi: 10.1016/j.tree.2010.01.007 20188434
3. Williams PH, Osborne JL. Bumblebee vulnerability and conservation world-wide. Apidologie. 2009;40: 367–387.
4. Evans JD, Schwarz RS. Bees brought to their knees: Microbes affecting honey bee health. Trends Microbiol. Elsevier Ltd; 2011;19: 614–620. doi: 10.1016/j.tim.2011.09.003 22032828
5. McArt SH, Koch H, Irwin RE, Adler LS. Arranging the bouquet of disease: Floral traits and the transmission of plant and animal pathogens. Ecol Lett. 2014;17: 624–636. doi: 10.1111/ele.12257 24528408
6. Levitt AL, Singh R, Cox-Foster DL, Rajotte E, Hoover K, Ostiguy N, et al. Cross-species transmission of honey bee viruses in associated arthropods. Virus Res. 2013;176: 232–240. doi: 10.1016/j.virusres.2013.06.013 23845302
7. Ravoet J, Smet L De, Meeus I, Smagghe G, Wenseleers T, Graaf DC De. Widespread occurrence of honey bee pathogens in solitary bees. J Invertebr Pathol. 2014;122: 55–58. doi: 10.1016/j.jip.2014.08.007 25196470
8. Li J, Peng W, Wu J, Strange JP, Boncristiani H, Chen Y. Cross-species infection of deformed wing virus poses a new threat to pollinator conservation. J Econ Entomol. 2011;104: 732–739. doi: 10.1603/ec10355 21735887
9. Singh R, Levitt AL, Rajotte EG, Holmes EC, Ostiguy N, Vanengelsdorp D, et al. RNA viruses in hymenopteran pollinators: Evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS One. 2010;5: e14357. doi: 10.1371/journal.pone.0014357 21203504
10. Graystock P, Goulson D, Hughes WOH. Parasites in bloom: flowers aid dispersal and transmission of pollinator parasites within and between bee species. Proc R Soc B Biol Sci. 2015;282. Available: http://dx.doi.org/10.1098/rspb.2015.1371
11. Durrer S, Schmid-Hempel P. Shared Use of Flowers Leads to Horizontal Pathogen Transmission. Proc R Soc B Biol Sci. 1994;258: 299–302. doi: 10.1098/rspb.1994.0176
12. Alger SA, Burnham PA, Boncristiani HF, Brody AK. RNA virus spillover from managed honeybees (Apis mellifera) to wild bumblebees (Bombus spp.). PLoS One. 2019;14: e0217822. doi: 10.1371/journal.pone.0217822 31242222
13. Purkiss T, Lach L. Pathogen spillover from Apis mellifera to a stingless bee. Proc R Soc B Biol Sci. 2019;286.
14. Melathopoulos A, Ovinge L, Wolf P, Castillo C, Ostermann D, Hoover S. Viruses of managed alfalfa leafcutting bees (Megachille rotundata Fabricus) and honey bees (Apis mellifera L.) in Western Canada: Incidence, impacts, and prospects of cross-species viral transmission. J Invertebr Pathol. Elsevier; 2017;146: 24–30. doi: 10.1016/j.jip.2017.04.003 28400199
15. Yang X, Cox-Foster DL. Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proc Natl Acad Sci U S A. 2005;102: 7470–7475. doi: 10.1073/pnas.0501860102 15897457
16. Di Prisco G, Cavaliere V, Annoscia D, Varricchio P, Caprio E, Nazzi F. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proc Natl Acad Sci. 2013;110: 18466–18471. doi: 10.1073/pnas.1314923110 24145453
17. Chen Y, Pettis JS, Collins A, Feldlaufer MF. Prevalence and transmission of honeybee viruses. Appl Environ Microbiol. 2006;72: 606–611. doi: 10.1128/AEM.72.1.606-611.2006 16391097
18. Bowen-Walker P, Martin S, Gunn A. The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite varroa jacobsoni Oud. J Invertebr Pathol. 1999;73: 101–106. doi: 10.1006/jipa.1998.4807 9878295
19. Genersch E, Yue C, Fries I, De Miranda JR. Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. J Invertebr Pathol. 2006;91: 61–63. doi: 10.1016/j.jip.2005.10.002 16300785
20. Leat N, Ball B, Govan V, Davison S. Analysis of the complete genome sequence of black queen-cell virus, a picorna-like virus of honey bees. J Gen Virol. 2000;81: 2111–2119. doi: 10.1099/0022-1317-81-8-2111 10900051
21. Otterstatter MC, Thomson JD. Does pathogen spillover from commercially reared bumble bees threaten wild pollinators? PLoS One. 2008;3. doi: 10.1371/journal.pone.0002771 18648661
22. Colla SR, Otterstatter MC, Gegear RJ, Thomson JD. Plight of the bumble bee: Pathogen spillover from commercial to wild populations. Biol Conserv. 2006;129: 461–467. doi: 10.1016/j.biocon.2005.11.013
23. Fürst M a, McMahon DP, Osborne JL, Paxton RJ, Brown MJF. Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature. 2014;506: 364–6. doi: 10.1038/nature12977 24553241
24. Graystock P, Goulson D, Hughes WOH. The relationship between managed bees and the prevalence of parasites in bumblebees. Peer J. 2014; 1–24. doi: 10.7717/peerj.522 25165632
25. McMahon DP, Fürst M a., Caspar J, Theodorou P, Brown MJF, Paxton RJ. A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees. J Anim Ecol. 2015;84: 615–624. doi: 10.1111/1365-2656.12345 25646973
26. Wilfert L, Long G, Leggett HG, Schmid-Hempel P, Butlin R, Martin SJM, et al. Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science (80-). 2016;351: 594–597. doi: 10.1126/science.aac9976 26912700
27. Mazzei M, Carrozza ML, Luisi E, Forzan M, Giusti M, Sagona S, et al. Infectivity of DWV associated to flower pollen: experimental evidence of a horizontal transmission route. PLoS One. 2014;9: e113448. doi: 10.1371/journal.pone.0113448 25419704
28. Chen YP, Higgins JA, Feldlaufer MF. Quantitative real-time reverse transcription-PCR analysis of deformed wing virus infection in the honeybee (Apis mellifera L.). Appl Env Microbiol. 2005;71: 436–441. doi: 10.1128/AEM.71.1.436
29. Adler LS, Michaud KM, Ellner SP, McArt SH, Stevenson PC, Irwin RE. Disease where you dine: Plant species and floral traits associated with pathogen transmission in bumble bees. Ecology. 2018;99: 2535–2545. doi: 10.1002/ecy.2503 30155907
30. Heinrich B. “Majoring” and “minoring” by foraging bumblebees, Bombus vagans: an experimental analysis. Ecology. 1979;60: 246–255. doi: 10.2307/1937652
31. Portlas ZM, Tetlie JR, Prischmann-Voldseth D, Hulke BS, Prasifka JR. Variation in floret size explains differences in wild bee visitation to cultivated sunflowers. Plant Genet Resour Characterisation Util. 2018;16: 498–503. doi: 10.1017/S1479262118000072
32. Braman SK, Quick JC. Differential bee attraction among crape myrtle cultivars (Lagerstroemia spp.: Myrtales: Lythraceae). Environ Entomol. 2018;47: 1203–1208. doi: 10.1093/ee/nvy117 30085015
33. Hernández IG, Palottini F, Macri I, Galmarini CR, Farina WM. Appetitive behavior of the honey bee Apis mellifera in response to phenolic compounds naturally found in nectars. J Exp Biol. 2019;222. doi: 10.1242/jeb.189910 30559301
34. Arenas A, Kohlmaier MG. Nectar source profitability influences individual foraging preferences for pollen and pollen-foraging activity of honeybee colonies. Behav Ecol Sociobiol. Behavioral Ecology and Sociobiology; 2019;73. doi: 10.1007/s00265-019-2644-5
35. Ghazoul J. Floral diversity and the facilitation of pollination. J Ecol. 2006;94: 295–304. doi: 10.1111/j.1365-2745.2006.01098.x
36. Hegland SJ, Boeke L. Relationships between the density and diversity of floral resources and flower visitor activity in a temperate grassland community. Ecol Entomol. 2006;31: 532–538. doi: 10.1111/j.1365-2311.2006.00812.x
37. Manley R, Boots M, Wilfert L. Emerging viral disease risk to pollinating insects: ecological, evolutionary and anthropogenic factors. J Appl Ecol. 2015; doi: 10.1111/1365-2664.12385 25954053
38. Graham, James M. Interaction Effects: Their Nature and Some Post Hoc Exploration Strategies. Annual Meeting of the Southwest Educational Research Association. 2000.
39. Bates D, Maechler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw. 2015;67: 1–48. doi: 10.18637/jss.v067.i01
40. Hothorn T, Bretz F, Westfall P, Heiberger RM, Schuetzenmeister A, Scheibe S. simultaneous inference in general parametric models. Biometrical J. 2008;50: 346–363. Available: https://cran.r-project.org/web/packages/multcomp/citation.html
41. R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2016.
42. Richardson LL, Bowers MD, Irwin RE. Nectar chemistry mediates the behavior of parasitized bees: Consequences for plant fitness. Ecology. 2016;97: 325–337. doi: 10.1890/15-0263.1 27145608
43. Manson JS, Otterstatter MC, Thomson JD. Consumption of a nectar alkaloid reduces pathogen load in bumble bees. Oecologia. 2010;162: 81–89. doi: 10.1007/s00442-009-1431-9 19711104
44. Simone-Finstrom MD, Spivak M. Increased resin collection after parasite challenge: A case of self-medication in honey bees? PLoS One. 2012;7: 17–21. doi: 10.1371/journal.pone.0034601 22479650
45. Richardson LL, Adler LS, Leonard AS, Andicoechea J, Regan KH, Anthony WE, et al. Secondary metabolites in floral nectar reduce parasite infections in bumblebees. Proc R Soc London B Biol Sci. 2015;282: 20142471. doi: 10.1098/rspb.2014.2471 25694627
46. Annoscia D, Zanni V, Galbraith D, Quirici A, Grozinger C, Bortolomeazzi R, et al. Elucidating the mechanisms underlying the beneficial health effects of dietary pollen on honey bees (Apis mellifera) infested by Varroa mite ectoparasites. Sci Rep. Springer US; 2017;7: 1–13. doi: 10.1038/s41598-016-0028-x
47. Chang CF, Suzuki A, Kumai S, Tamura S. Chemical Studies on “Clover Sickness”: Part II. Biological functions of isoflavonoids and their related compounds. Agric Biol Chem. 1969;33: 398–408. doi: 10.1080/00021369.1969.10859325
48. Andres A, Donovan SM, Kuhlenschmidt MS. Soy isoflavones and virus infections. J Nutr Biochem. Elsevier Inc.; 2009;20: 563–569. doi: 10.1016/j.jnutbio.2009.04.004 19596314
49. Graystock P, Blane EJ, Mcfrederick QS, Goulson D, Hughes WOH. Parasites and Wildlife Do managed bees drive parasite spread and emergence in wild bees ? Int J Parasitol Parasites Wildl. Elsevier Ltd; 2016;5: 64–75. doi: 10.1016/j.ijppaw.2015.10.001 28560161
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