The impact of lowbush blueberry (Vaccinium angustifolium Ait.) and cranberry (Vaccinium macrocarpon Ait.) pollination on honey bee (Apis mellifera L.) colony health status

Autoři: Claude Dufour aff001;  Valérie Fournier aff002;  Pierre Giovenazzo aff001
Působiště autorů: Département de biologie, Université Laval, Québec, Québec, Canada aff001;  Centre de recherche et innovation sur les végétaux, Université Laval, Québec, Québec, Canada aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227970


Commercial lowbush blueberry (Vaccinium angustifolium Ait.) and cranberry (Vaccinium macrocarpon Ait.) crops benefit from the presence of honey bee (Apis mellifera L.) for pollination. Unfortunately, beekeepers are observing negative impacts of pollination services on honey bee colonies. In this study, we investigated three beekeeping management strategies (MS) and measured their impact on honey bee colony health and development. Experimental groups (five colonies/MS) were: A) Control farmland honey producing MS (control MS); B) Blueberry pollination MS (blueberry MS); C) Cranberry pollination MS (cranberry MS) and D) Double pollination MS, blueberry followed by cranberry (double MS). Our goals were to 1) compare floral abundance and attractiveness of foraging areas to honey bees between apiaries using a Geographic Information System, and 2) compare honey bee colony health status and population development between MS during a complete beekeeping season. Our results show significantly lower floral abundance and honey bee attractiveness of foraging areas during cranberry pollination compared to the other environments. The blueberry pollination site seemed to significantly reduce brood population in the colonies who provided those services (blueberry MS and double MS). The cranberry pollination site seemed to significantly reduce colony weight gain (cranberry MS and double MS) and induce a significantly higher winter mortality rate (cranberry MS). We also measured significantly higher levels of Black queen cell virus and Sacbrood virus in the MS providing cranberry pollination (cranberry MS and double MS).

Klíčová slova:

Bees – Blueberries – Crops – Foraging – Fruit crops – Honey bees – Pollination – Weight gain


1. Brodschneider R, Crailsheim K. Nutrition and health in honey bees. Apidologie. 2010; 41(3):278–94.

2. Neumann P, Carreck NL. Honey bee colony losses. J Apic Res. 2010; 49(1):1–6.

3. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE. Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol. 2010; 25(6):345–53. doi: 10.1016/j.tree.2010.01.007 20188434

4. Klein A-M, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, et al. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences. 2007; 274(1608):303–13. doi: 10.1098/rspb.2006.3721 17164193

5. Darrach M, Page S. Aperçu statistique de l’industrie apicole canadienne et contribution économique des services de pollinisation rendus par les abeilles domestiques, 2013–2014. In: Agriculture et Agroalimentaire Canada, editor. Ottawa, Ontario: Gouvernement du Canada; 2016. p. 22.

6. Asare E, Hoshide AK, Drummond FA, Criner GK, Chen X. Economic Risk of Bee Pollination in Maine Wild Blueberry, Vaccinium angustifolium. J Econ Entomol. 2017; 110(5):1980–92. doi: 10.1093/jee/tox191 28981673

7. Chagnon M. Causes et effets du déclin mondial des pollinisateurs et les moyens d’y remédier. In: Fédération Canadienne de la Faune. Bureau régional du Québec, editor. 2008. p. 1–70.

8. Chagnon M. Gestion et aménagement des pollinisateurs de la canneberge: vers un rendement accru. Conseil pour le développement de l'agriculture du Québec; 2007 Juin 2007. Report No.: Projet 2216.

9. Cane JH, Schiffhauer D. Dose-response relationships between pollination and fruiting refine pollination comparisons for cranberry (Vaccinium macrocarpon [Ericaceae]). Am J Bot. 2003; 90(10):1425–32. doi: 10.3732/ajb.90.10.1425 21659094

10. Institut de la statistique du Québec. Profil sectoriel de l’industrie bioalimentaire au Québec—Édition 2018.: Gouvernement du Québec; 2019 [Available from:

11. Rioux M-C. Portrait-diagnostic sectoriel de la canneberge au Québec. In: Sous-ministériat à la transformation et aux politiques bioalimentaires, Direction du développement des secteurs agroalimentaires, editors. Quebec, Quebec: MAPAQ; 2018. p. 1–22.

12. MAPAQ, Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec. Culture du bleuet. 2017 [Available from:

13. APCQ, Association des producteurs de canneberges du Québec. Profil de l'industrie de la canneberge. 2019 [Available from:

14. Institut de la statistique du Québec. Faits saillants de l’enquête sur l’apiculture au Québec—Campagne apicole 2017: Gouvernement du Québec; 2018 [Available from:

15. Morimoto T, Kojima Y, Toki T, Komeda Y, Yoshiyama M, Kimura K, et al. The habitat disruption induces immune-suppression and oxidative stress in honey bees. Ecol Evol. 2011; 1(2):201–17. doi: 10.1002/ece3.21 22393496

16. Simone-Finstrom M, Li-Byarlay H, Huang MH, Strand MK, Rueppell O, Tarpy DR. Migratory management and environmental conditions affect lifespan and oxidative stress in honey bees. Sci Rep. 2016; 6(32023):1–10.

17. Zhu X, Zhou S, Huang ZY. Transportation and pollination service increase abundance and prevalence of Nosema ceranae in honey bees (Apis mellifera). J Apic Res. 2015; 53(4):469–71.

18. Smart M, Pettis J, Rice N, Browning Z, Spivak M. Linking measures of colony and individual honey bee health to survival among apiaries exposed to varying agricultural land use. PLoS ONE. 2016; 11(3):1–28 (e0152685).

19. Donkersley P, Rhodes G, Pickup RW, Jones KC, Wilson K. Honeybee nutrition is linked to landscape composition. Ecol Evol. 2014; 4(21):4195–206. doi: 10.1002/ece3.1293 25505544

20. Winston ML. The biology of the honey bee. Cambridge, Massachusetts: Harvard University Press; 1987.

21. Alaux C, Ducloz F, Crauser D, Le Conte Y. Diet effects on honeybee immunocompetence. Biol Lett. 2010; 6(4):562–5. doi: 10.1098/rsbl.2009.0986 20089536

22. Di Pasquale G, Salignon M, Le Conte Y, Belzunces LP, Decourtye A, Kretzschmar A, et al. Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter? PLoS ONE. 2013; 8(8):e72016. doi: 10.1371/journal.pone.0072016 23940803

23. Di Pasquale G, Alaux C, Le Conte Y, Odoux JF, Pioz M, Vaissière BE, et al. Variations in the availability of pollen resources affect honey bee health. PLoS ONE. 2016; 11(9):e0162818. doi: 10.1371/journal.pone.0162818 27631605

24. Singh RP, Singh PN. Amino acid and lipid spectra of larvae of honey bee (Apis cerana Fabr.) feeding on mustard pollen. Apidologie. 1996; 27:21–8.

25. Myra M, Mackenzie K, Vander Kloet SP. Investigation of a possible sexual function specialization in the lowbush blueberry (Vaccinium angustifolium Aiton. Ericaceae). Small Fruits Rev. 2004; 3(3–4):313–24.

26. Colwell MJ, Williams GR, Evans RC, Shutler D. Honey bee‐collected pollen in agro‐ecosystems reveals diet diversity, diet quality, and pesticide exposure. Ecol Evol. 2017; 7(18):7243–53. doi: 10.1002/ece3.3178 28944014

27. Morrant DS, Schumann R, Petit S. Field methods for sampling and storing nectar from flowers with low nectar volumes. Ann Bot. 2009; 103(3):533–42. doi: 10.1093/aob/mcn241 19074446

28. Starast M, Tasa T, Mänd M, Vool E, Paal T, Karp K, editors. Effect of cultivation area on lowbush blueberry nectar production and pollinator composition. 2014: International Society for Horticultural Science (ISHS), Leuven, Belgium.

29. Cane JH, Schiffhauer D. Nectar production of cranberries: Genotypic differences and insensitivity to soil fertility. J Am Soc Hortic Sci. 1997; 122(5):665–7.

30. Kevan P, Gadawski R, Kevan S, Gadawski S, editors. Pollination of cranberries, Vaccinium macrocarpon, on cultivated marshes in Ontario. Proceedings of the Entomological Society of Ontario; 1983.

31. Girard M, Chagnon M, Fournier V. Pollen diversity collected by honey bees in the vicinity of Vaccinium spp. crops and its importance for colony development. This article is part of a Special Issue entitled “Pollination biology research in Canada: Perspectives on a mutualism at different scales”. Botany. 2012; 90(7):545–55.

32. Winston ML. The honey bee colony: life history. In: Graham EJ, editor. The hive and the honey bee. Hamilton, IL: Dadant and Sons; 1992. p. 73–101.

33. Omar E, Abd-Ella AA, Khodairy MM, Moosbeckhofer R, Crailsheim K, Brodschneider R. Influence of different pollen diets on the development of hypopharyngeal glands and size of acid gland sacs in caged honey bees (Apis mellifera). Apidologie. 2017; 48(4):425–36.

34. Scofield HN, Mattila HR. Honey bee workers that are pollen stressed as larvae become poor foragers and waggle dancers as adults. PLoS ONE. 2015; 10(4):e0121731 (1–19). doi: 10.1371/journal.pone.0121731 25853902

35. Herbert EWJ, Hill DA. Honey bee nutrition. In: Graham JM, editor. The hive and the honey bee. Hamilton, Illinois: Dadant and Sons; 2015. p. 237–68.

36. Groff SC, Loftin CS, Drummond F, Bushmann S, McGill B. Parameterization of the InVEST crop pollination model to spatially predict abundance of wild blueberry (Vaccinium angustifolium Aiton) native bee pollinators in Maine, USA. Environ Modell Softw. 2016; 79:1–9.

37. Venturini EM, Drummond FA, Hoshide AK, Dibble AC, Stack LB. Pollination reservoirs in lowbush blueberry (Ericales: Ericaceae). J Econ Entomol. 2017; 110(2):333–46. doi: 10.1093/jee/tow285 28069631

38. Requier F, Odoux J-F, Tamic T, Moreau N, Henry M, Decourtye A, et al. Honey bee diet in intensive farmland habitats reveals an unexpectedly high flower richness and a major role of weeds. Ecol Appl. 2015; 25(4):881–90. doi: 10.1890/14-1011.1 26465030

39. Bizotto LdA, Santos RSS, Boff MIC. Food resources and population pattern in Apis mellifera hives used for apple pollination. Pesqui Agropecu Bras. 2018; 53(4):399–404.

40. Gisder S, Genersch E. Viruses of commercialized insect pollinators. J Invertebr Pathol. 2017; 147:51–9. doi: 10.1016/j.jip.2016.07.010 27498219

41. ESRI. ArcGIS Desktop: Release 10. Redlands, CA: Environmental Systems Research Institute; 2011.

42. Moisan-De Serres J, Bourgouin F, Lebeau M-O. Guide d'identification et de gestion—Pollinisateurs et plantes mellifères. Québec: Centre de référence en agriculture et agroalimentaire du Québec; 2014. 351 p.

43. Delaplane KS, van der Steen J, Guzman-Novoa E. Standard methods for estimating strength parameters of Apis mellifera colonies. J Apic Res. 2013; 52(1):1–12.

44. Giovenazzo P, Dubreuil P. Evaluation of spring organic treatments against Varroa destructor (Acari: Varroidae) in honey bee Apis mellifera (Hymenoptera: Apidae) colonies in eastern Canada. Exp Appl Acarol. 2011; 55(1):65–76. doi: 10.1007/s10493-011-9447-3 21442305

45. vanEngelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, Kim Nguyen B, et al. Colony collapse disorder: A descriptive study. PLoS ONE. 2009; 4(8):1–17 (e0006481).

46. Boncristiani H, Underwood R, Schwarz R, Evans JD, Pettis J, vanEngelsdorp D. Direct effect of acaricides on pathogen loads and gene expression levels in honey bees Apis mellifera. J Insect Physiol. 2012; 58(5):613–20. doi: 10.1016/j.jinsphys.2011.12.011 22212860

47. Gisder S, Genersch E. Molecular differentiation of Nosema apis and Nosema ceranae based on species-specific sequence differences in a protein coding gene. J Invertebr Pathol. 2013; 113(1):1–6. doi: 10.1016/j.jip.2013.01.004 23352902

48. Lee KV, Moon RD, Burkness EC, Hutchison WD, Spivak M. Practical sampling plans for Varroa destructor (Acari: Varroidae) in Apis mellifera (Hymenoptera: Apidae) colonies and apiaries. Journal of Economic Entomology. 2010; 103(4):1039–50. doi: 10.1603/ec10037 20857710

49. Davies GM, Gray A. Don't let spurious accusations of pseudoreplication limit our ability to learn from natural experiments (and other messy kinds of ecological monitoring). Ecol Evol. 2015; 5(22):5295–304. doi: 10.1002/ece3.1782 30151132

50. Hurlbert SH. Pseudoreplication and the design of ecological field experiments. Ecol Monogr. 1984; 54(2):187–211.

51. Couvillon MJ, Riddell Pearce FC, Accleton C, Fensome KA, Quah SKL, Taylor EL, et al. Honey bee foraging distance depends on month and forage type. Apidologie. 2014; 46(1):61–70.

52. Beekman M, Ratnieks FLW. Long-range foraging by the honey bee, Apis mellifera L. Funct Ecol. 2000; 14(4):490–6.

53. Visscher PK, Seeley TD. Foraging strategy of honeybee colonies in a temperate deciduous forest. Ecology. 1982; 63(6):1790–801.

54. von Frisch K. Vie et moeurs des abeilles. Paris, France: Albin Michel; 2011. 251 p.

55. SAS Institute Inc. SAS® University Edition Quick start guide for students with visual impairments. Version 2.7 9.4 M5 ed. Cary, NC: SAS Institute Inc.; 2018.

56. Pettis JS, Lichtenberg EM, Andree M, Stitzinger J, Rose R, Vanengelsdorp D. Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLoS ONE. 2013; 8(7):e70182. doi: 10.1371/journal.pone.0070182 23894612

57. Requier F, Odoux J-F, Henry M, Bretagnolle V. The carry-over effects of pollen shortage decrease the survival of honeybee colonies in farmlands. J Appl Ecol. 2017; 54(4):1161–70.

58. Martin G. Influence d’un supplément alimentaire sur le développement des colonies d’abeilles domestiques (Apis mellifera, Linnaeus 1758) au Québec: Université de Montréal; 2009.

59. Fewell JH, Winston ML. Colony state and regulation of pollen foraging in the honey bee, Apis mellifera L. Behav Ecol Sociobiol. 1992; 30(6):387–93.

60. DeGrandi-Hoffman G, Wardell G, Ahumada-Segura F, Rinderer T, Danka R, Pettis J. Comparisons of pollen substitute diets for honey bees: consumption rates by colonies and effects on brood and adult populations. J Apic Res. 2015; 47(4):265–70.

61. Kleinschmidt GJ, Kondos AC, Harden J, Turner JW. Colony management for eucalypt honey flows. Aust Beekeep. 1974; 75(11):261–4.

62. Li JH, Evans JD, Li WF, Zhao YZ, DeGrandi-Hoffman G, Huang SK, et al. New evidence showing that the destruction of gut bacteria by antibiotic treatment could increase the honey bee's vulnerability to Nosema infection. PLoS ONE. 2017; 12(11):1–18 (e0187505).

63. Tritschler M, Vollmann JJ, Yanez O, Chejanovsky N, Crailsheim K, Neumann P. Protein nutrition governs within-host race of honey bee pathogens. Sci Rep. 2017; 7(1):14988. doi: 10.1038/s41598-017-15358-w 29118416

64. Erler S, Denner A, Bobis O, Forsgren E, Moritz RF. Diversity of honey stores and their impact on pathogenic bacteria of the honeybee, Apis mellifera. Ecol Evol. 2014; 4(20):3960–7. doi: 10.1002/ece3.1252 25505523

65. Chen YP, Siede R. Honey bee viruses. Adv Virus Res. 70: Academic Press; 2007. p. 33–80. doi: 10.1016/S0065-3527(07)70002-7 17765703

66. Mondet F, de Miranda JR, Kretzschmar A, Le Conte Y, Mercer AR. On the front line: quantitative virus dynamics in honeybee (Apis mellifera L.) colonies along a new expansion front of the parasite Varroa destructor. PLoS Pathog. 2014; 10(8):1–15 (e1004323).

67. Nazzi F, Brown SP, Annoscia D, Del Piccolo F, Di Prisco G, Varricchio P, et al. Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog. 2012; 8(6):1–16 (e1002735).

68. DeGrandi-Hoffman G, Chen Y. Nutrition, immunity and viral infections in honey bees. Curr Opin Insect Sci. 2015; 10:170–6. doi: 10.1016/j.cois.2015.05.007 29588005

69. Glenny W, Cavigli I, Daughenbaugh KF, Radford R, Kegley SE, Flenniken ML. Honey bee (Apis mellifera) colony health and pathogen composition in migratory beekeeping operations involved in California almond pollination. PLoS ONE. 2017; 12(8):e0182814. doi: 10.1371/journal.pone.0182814 28817641

70. Welch A, Drummond F, Tewari S, Averill A, Burand JP. Presence and prevalence of viruses in local and migratory honeybees (Apis mellifera) in Massachusetts. Applied and Environmental Microbiology. 2009; 75(24):7862. doi: 10.1128/AEM.01319-09 19854916

71. Arien Y, Dag A, Shafir S. Omega-6:3 ratio more than absolute lipid level in diet affects associative learning in honey bees. Front Psychol. 2018; 9:1001. doi: 10.3389/fpsyg.2018.01001 29971031

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