Effects of late miticide treatments on foraging and colony productivity of European honey bees (Apis mellifera)

Abstract

Chemical miticides are used routinely in honey bee colonies worldwide as treatment for the parasitic mite Varroa destructor, but there have been very few long-term colony-level field studies of the impacts of miticides on the bees themselves. Lab-based studies with individual bees or bees in small groups have highlighted many negative effects of miticides on bee behaviour and physiology; hence, there is an urgent need to better understand the consequences of miticides on honey bee colonies in an apicultural setting. Here we compared effects of commercial treatments of the miticides tau-fluvalinate and thymol, and controls, on honey bee colonies and bee foraging behaviour over five months, from autumn through winter in Sydney, Australia. Since V. destructor does not occur in Sydney, in this study, we could isolate the direct effects of the miticides from indirect effects resulting from reduced mite load. We found the autumn treatment of either miticide caused no significant change in bee adult or brood population or size of food stores. The average temperature in the thymol group differed from the temperature in the control group and was lower during winter. Neither miticide reduced bee longevity. Tau-fluvalinate caused bees to start foraging earlier in life and perform shorter trips, but no other effects on foraging behaviour were documented. To conclude, in Sydney, Australia, limited negative effects of autumn thymol or tau-fluvalinate treatments were observed on bees or bee colony performance.

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Data availability

All data generated or analysed during this study are included in this published article (and its supplementary information files).

References

  1. Adamczyk S., Lázaro R., Pérez-Arquillué C., Conchello P., Herrera A. (2005) Evaluation of residues of essential oil components in honey after different anti-Varroa treatments. J. Agric. Food Chem. 53, 10085–10090.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  2. Alayrangues J., Hotier L., Massou I., Bertrand Y., Armengaud C. (2016) Prolonged effects of in-hive monoterpenoids on the honey bee Apis mellifera. Ecotoxicology 25, 856–862.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  3. Alburaki M., Steckel S. J., Chen D., McDermott E., Weiss M., Skinner J. A., Kelly H., et al. (2017) Landscape and pesticide effects on honey bees: forager survival and expression of acetylcholinesterase and brain oxidative genes. Apidologie 48, 556–571.

    CAS  Article  Google Scholar 

  4. Barron A. B. (2015) Death of the bee hive: understanding the failure of an insect society. Curr. Opin. Insect Sci. 10, 45–50.

    PubMed  Article  PubMed Central  Google Scholar 

  5. Berry J. A., Hood W. M., Pietravalle S., Delaplane K. S. (2013) Field-Level Sublethal Effects of Approved Bee Hive Chemicals on Honey Bees (Apis mellifera L). PLoS One 8.

  6. Beyer M., Junk J., Eickermann M., Clermont A., Kraus F., Georges C., Reichart A., Hoffmann L. (2018) Winter honey bee colony losses, Varroa destructor control strategies, and the role of weather conditions: Results from a survey among beekeepers. Res. Vet. Sci. 118, 52–60.

    PubMed  Article  PubMed Central  Google Scholar 

  7. Boncristiani H., Underwood R., Schwarz R., Evans J. D., Pettis J., Vanengelsdorp D. (2012) Direct effect of acaricides on pathogen loads and gene expression levels in honey bees Apis mellifera. J. Insect Physiol. 58, 613–620.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  8. Bonnafé E., Alayrangues J., Hotier L., Massou I., Renom A., Souesme G., Marty P., Allaoua M., Treilhou M., Armengaud C. (2017) Monoterpenoid-based preparations in beehives affect learning, memory, and gene expression in the bee brain. Environ. Toxicol. Chem. 36, 337–345.

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  9. Bordier C., Conte Y. Le, Klein S., Alaux C., Barron A. B. (2018) Stress decreases pollen foraging performance in honeybees. J. Exp. Biol. 221, jeb171470.

    PubMed  Article  PubMed Central  Google Scholar 

  10. Brodschneider R., Brus J., Danihlík J. (2019) Comparison of apiculture and winter mortality of honey bee colonies (Apis mellifera) in Austria and Czechia. Agric. Ecosyst. Environ. 274, 24–32.

    Article  Google Scholar 

  11. Burley L. M., Fell R. D., Saacke R. G. (2008) Survival of Honey Bee (Hymenoptera: Apidae) Spermatozoa Incubated at Room Temperature from Drones Exposed to Miticides. J. Econ. Entomol. 101, 1081–1087.

    PubMed  Article  PubMed Central  Google Scholar 

  12. Calatayud-Vernich P., Calatayud F., Simó E., Picó Y. (2018) Pesticide residues in honey bees, pollen and beeswax: Assessing beehive exposure. Environ. Pollut. 241, 106–114.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  13. Carayon J. L., Téné N., Bonnafé E., Alayrangues J., Hotier L., Armengaud C., Treilhou M. (2014) Thymol as an alternative to pesticides: Persistence and effects of Apilife Var on the phototactic behavior of the honeybee Apis mellifera. Environ. Sci. Pollut. Res. 21, 4934–4939.

    CAS  Article  Google Scholar 

  14. Carroll M. J., Meikle W. G., McFrederick Q. S., Rothman J. A., Brown N., Weiss M., Ruetz Z., Chang E. (2018) Pre-almond supplemental forage improves colony survival and alters queen pheromone signaling in overwintering honey bee colonies. Apidologie 49, 827–837.

    CAS  Article  Google Scholar 

  15. Coffey M. F., Breen J. (2016) The efficacy and tolerability of Api-Bioxal as a winter varroacide in a cool temperate climate climate. J. Apic. Res. 8839, 1–9.

    Google Scholar 

  16. Colin T., Bruce J., Meikle W. G., Barron A. B. (2018) The development of honey bee colonies assessed using a new semi-automated brood counting method: Combcount. PLoS One 13, 1–14.

    Article  CAS  Google Scholar 

  17. Colin T., Lim M. Y., Quarrell S. R., Allen G. R., Barron A. B. (2019a) Effects of thymol on European honey bee hygienic behaviour. Apidologie 50, 141–152.

    CAS  Article  Google Scholar 

  18. Colin T., Meikle W. G., Paten A. M., Barron A. B. (2019b) Long-term dynamics of honey bee colonies following exposure to chemical stress. Sci. Total Environ. 677, 660–670.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  19. Colin T., Meikle W. G., Wu X., Barron A. B. (2019c) Traces of a Neonicotinoid Induce Precocious Foraging and Reduce Foraging Performance in Honey Bees. Environ. Sci. Technol. 53, 8252–8261.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  20. Colin T., Plath J. A., Klein S., Vine P., Devaud J.-M., Lihoreau M., Meikle W. G., Barron A. B. (2020) The miticide thymol in combination with trace levels of the neonicotinoid imidacloprid reduces visual learning performance in honey bees (Apis mellifera). Apidologie, 1–11.

  21. Dietemann V., Pflugfelder J., Anderson D., Charrière J.-D., Chejanovsky N., Dainat B., Miranda J. de, et al. (2012) Varroa destructor : research avenues towards sustainable control. J. Apic. Res. 51, 125–132.

    Article  Google Scholar 

  22. Frost E. H., Shutler D., Hillier N. K. (2013) Effects of fluvalinate on honey bee learning, memory, responsiveness to sucrose, and survival. J. Exp. Biol. 216, 2931–8.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  23. Fukuda H., Sekiguchi K. (1966) Seasonal change of the honeybee worker longevity in Sapporo, North Japan, with notes on some factors affecting the life-span. Japanese J. Ecol. 16, 206–212.

    Google Scholar 

  24. Giusti M., Sabelli C., Donato A. Di, Lamberti D., Paturzo C. E., Polignano V., Lazzari R., Felicioli A. (2017) Efficacy and safety of Varterminator, a new formic acid medicine against the varroa mite. J. Apic. Res. 56, 162–167.

    Article  Google Scholar 

  25. Gregorc A., Evans J. D., Scharf M., Ellis J. D. (2012) Gene expression in honey bee (Apis mellifera) larvae exposed to pesticides and Varroa mites (Varroa destructor). J. Insect Physiol. 58, 1042–1049.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  26. Haarmann T., Spivak M., Weaver D., Weaver B., Glenn T. (2002) Effects of Fluvalinate and Coumaphos on Queen Honey Bees (Hymenoptera: Apidae) in Two Commercial Queen Rearing Operations. J. Econ. Entomol. 95, 28–35.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  27. Hatjina F., Haristos L. (2005) Indirect effects of oxalic acid administered by trickling method on honey bee brood. J. Apic. Res. 44, 172–174.

    CAS  Article  Google Scholar 

  28. He X., Wang W., Qin Q., Zeng Z., Zhang S., Barron A. B. (2013) Assessment of flight activity and homing ability in Asian and European honey bee species, Apis cerana and Apis mellifera, measured with radio frequency tags. Apidologie 44, 38–51.

    Article  Google Scholar 

  29. Henry M., Cerrutti N., Aupinel P., Decourtye A., Gayrard M., Odoux J.-F., Pissard A., Rüger C., Bretagnolle V. (2015) Reconciling laboratory and field assessments of neonicotinoid toxicity to honeybees. Proc. R. Soc. B Biol. Sci. 282, 20152110.

    Article  CAS  Google Scholar 

  30. Holst N., Meikle W. (2018) Breakfast Canyon Discovered in Honeybee Hive Weight Curves. Insects 9, 176.

    PubMed Central  Article  Google Scholar 

  31. Johnson R. M., Dahlgren L., Siegfried B. D., Ellis M. D. (2013) Acaricide, fungicide and drug interactions in honey bees (Apis mellifera). PLoS One 8, e54092.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  32. Jones J. C., Myerscough M. R., Graham S., Oldroyd B. P. (2004) Honey bee nest thermoregulation: diversity promotes stability. Science 305, 402–4.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  33. Jones J. C., Oldroyd B. P. (2006) Nest Thermoregulation in Social Insects.

  34. Jong D. De, Morse R. A., Eickwort G. C. (1982) Mite pests of honey bees. Annu. Rev. Entomol. 27, 229–252.

    Article  Google Scholar 

  35. Kasiotis K. M., Tzouganaki Z. D., Machera K. (2018) Chromatographic determination of monoterpenes and other acaricides in honeybees: Prevalence and possible synergies. Sci. Total Environ. 625, 96–105.

    CAS  PubMed  Article  Google Scholar 

  36. Kassambara A., Kosinski M. (2018) survminer: Drawing Survival Curves using “ggplot2”.

  37. Klein S., Cabirol A., Devaud J. M., Barron A. B., Lihoreau M. (2017) Why bees are so vulnerable to environmental stressors. Trends Ecol. Evol. 32, 268–278.

    PubMed  Article  PubMed Central  Google Scholar 

  38. Kunert K., Crailsheim K. (1988) Seasonal changes in carbohydrate, lipid and protein content in emerging worker honeybees and their mortality. J. Apic. Res. 27, 13–21.

    CAS  Article  Google Scholar 

  39. Lenth R., Singmann H., Love J., Buerkner P., Herve M. (2018) Package “emmeans.”

  40. Martel A. C., Zeggane S. (2002) Determination of acaricides in honey by high-performance liquid chromatography with photodiode array detection. J. Chromatogr. A 954, 173–180.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  41. Meikle W. G., Adamczyk J. J., Weiss M., Gregorc A., Johnson D. R., Stewart S. D., Zawislak J., Carroll M. J., Lorenz G. M. (2016a) Sublethal Effects of Imidacloprid on Honey Bee Colony Growth and Activity at Three Sites in the U.S. PLoS One 11, e0168603.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  42. Meikle W. G., Corby-Harris V., Carroll M. J., Weiss M., Snyder L. A., Meador C. A. D., Beren E., Brown N. (2019) Exposure to sublethal concentrations of methoxyfenozide disrupts honey bee colony activity and thermoregulation. PLoS One 14, 1–21.

    Article  CAS  Google Scholar 

  43. Meikle W. G., Holst N., Colin T., Weiss M., Carroll M. J., McFrederick Q. S., Barron A. B. (2018) Using within-day hive weight changes to measure environmental effects on honey bee colonies. PLoS One 13, e0197589.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  44. Meikle W. G., Weiss M. (2017) Monitoring Colony-level Effects of Sublethal Pesticide Exposure on Honey Bees. J. Vis. Exp. 129, 1–10.

    Google Scholar 

  45. Meikle W. G., Weiss M., Beren E. (2020) Landscape factors influencing honey bee colony behavior in Southern California commercial apiaries. Sci. Rep. 10, 1–16.

    Article  CAS  Google Scholar 

  46. Meikle W. G., Weiss M., Stilwell A. R. (2016b) Monitoring colony phenology using within-day variability in continuous weight and temperature of honey bee hives. Apidologie 47, 1–14.

    Article  Google Scholar 

  47. Milani N. (1999) The resistance of Varroa jacobsoni Oud. to acaricides. Apidologie 30, 229–234.

    CAS  Article  Google Scholar 

  48. Muggeo V. R. M. (2008) segmented: An R Package to Fit Regression Models with Broken-Line Relationships.

  49. Mullin C. A., Frazier M., Frazier J. L., Ashcraft S., Simonds R., vanEngelsdorp D., Pettis J. S. (2010) High Levels of Miticides and Agrochemicals in North American Apiaries: Implications for Honey Bee Health. PLoS One 5.

  50. Odemer R., Rosenkranz P. (2018) Chronic exposure to a neonicotinoid pesticide and a synthetic pyrethroid in full-sized honey bee colonies. bioRxiv, 293167.

  51. Odemer R., Rosenkranz P. (2020) Chronic exposure to a neonicotinoid pesticide and a synthetic pyrethroid in full-sized honey bee colonies. J. Apic. Res. 59, 2–11.

    Article  Google Scholar 

  52. Perry C. J., Søvik E., Myerscough M. R., Barron A. B. (2015) Rapid behavioral maturation accelerates failure of stressed honey bee colonies. Proc. Natl. Acad. Sci. 112, 3427–3432.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  53. Pettis J. S., Collins A. M., Wilbanks R., Feldlaufer M. F. (2004) Effects of coumaphos on queen rearing in the honey bee, Apis mellifera. Apidologie 35, 605–610.

    CAS  Article  Google Scholar 

  54. Pinheiro J., Bates D., DebRoy S., Sarkar D. (2019) nlme: Linear and Nonlinear Mixed Effects Models.

  55. Prado A., Pioz M., Vidau C., Requier F., Jury M., Crauser D., Brunet J. L., Conte Y. Le, Alaux C. (2019) Exposure to pollen-bound pesticide mixtures induces longer-lived but less efficient honey bees. Sci. Total Environ. 650, 1250–1260.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  56. R Core Team R. (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria.

    Google Scholar 

  57. Rosenkranz P., Aumeier P., Ziegelmann B. (2010) Biology and control of Varroa destructor. J. Invertebr. Pathol. 103, S96–S119.

    PubMed  Article  PubMed Central  Google Scholar 

  58. Serra Bonvehí J., Ventura Coll F., Ruiz Martínez J. A. (2016) Residues of essential oils in honey after treatments to control Varroa destructor. J. Essent. Oil Res. 28, 22–28.

    Article  CAS  Google Scholar 

  59. Søvik E., Perry C. J., LaMora A., Barron A. B., Ben-Shahar Y. (2015) Negative impact of manganese on honeybee foraging. Biol. Lett. 11, 1–4.

    Article  CAS  Google Scholar 

  60. Straub L., Williams G. R., Pettis J., Fries I., Neumann P. (2015) ScienceDirect Superorganism resilience : eusociality and susceptibility of ecosystem service providing insects to stressors. Curr. Opin. Insect Sci. 12, 109–112.

    Article  Google Scholar 

  61. Therneau T. M. (2015) A Package for Survival Analysis in S.

  62. Tihelka E. (2018) Effects of synthetic and organic acaricides on honey bee health: A review. Slov. Vet. Res. 55, 114–140.

    Google Scholar 

  63. Toomemaa K., Martin A., Williams I. H. (2010) The effect of different concentrations of oxalic acid in aqueous and sucrose solution on Varroa mites and honey bees. Apidologie 41, 643–653.

    CAS  Article  Google Scholar 

  64. Tsigouri A. D., Menkissoglu-Spiroudi U., Thrasyvoulou A. (2001) Study of tau-fluvalinate persistence in honey. Pest Manag. Sci. 57, 467–471.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  65. Underwood R. M., Traver B. E., López-Uribe M. M. (2019) Beekeeping Management Practices Are Associated with Operation Size and Beekeepers’ Philosophy towards in-Hive Chemicals. Insects 10, 10.

    PubMed Central  Article  Google Scholar 

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Acknowledgements

We thank Shaun Garvey for his help with hive maintenance.

Funding

TC received an iMQRES scholarship from Macquarie University. ABB is funded by the Australian Research Council (ARC Future Fellowship no. 140100452) and by the Lord Mayor’s Charitable Foundation through the Eldon & Anne Foot Trust. ABB and WGM are funded by the United States Department of Agriculture ARS agreement no: 58-5342-3-004F.

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Authors

Contributions

Designed study: TC, ABB, WGM. Gathered data: TC, JW, CF, XW. Analysed data: TC. Wrote manuscript: TC, ABB. Developed manuscript: all authors.

Corresponding author

Correspondence to Théotime Colin.

Additional information

Effets des traitements miticides tardifs sur le butinage et la productivité des colonies d’abeilles européennes ( Apis mellifera ).

miticides / acaricides / Varroa destructor / RFID / mesure du poids en continu.

Auswirkungen einer späten Akarizidbehandlung auf die Sammelaktivität und Produktivität europäischer Honigbienen ( Apis mellifera ).

Milbenbehandlung / Akarizide / Varroa destructor / RFID / kontinuierliche Gewichtsmessung.

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Manuscript Editor: Peter Rosenkranz

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Colin, T., Forster, C.C., Westacott, J. et al. Effects of late miticide treatments on foraging and colony productivity of European honey bees (Apis mellifera). Apidologie (2021). https://doi.org/10.1007/s13592-020-00837-3

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Keywords

  • miticides
  • acaricides
  • Varroa destructor
  • RFID
  • continuous weight measurement