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Fungicides

Certain fungicides are emerging as being harmful to bee health. As of Sept 15, 2015, there are 184 fungicide products registered for use in New York. While foraging, bees can come in contact with fungicides that are sprayed on orchards and in other landscapes. To date, fungicide residues have been detected in pollen, bee bread, wax, and honey in bee hives and nests [1-4]. In fact, next to miticides applied by beekeepers to control varroa, residues in hive materials are predominantly fungicides [5]. Despite the prevalence of fungicide use in conventional agriculture, scientific research is only beginning to uncover how they may affect wild and managed bees. This section provides an overview of what is currently known. For specific details on which fungicides have been researched, as well as other additional information, please consult the articles referenced in this summary. Only a handful of currently used fungicides have been investigated for their impact on bee health, and not all of these have had negative implications.

Laboratory Studies

Very few laboratory studies have examined the effects of fungicides on bees, and the only bee species that have been investigated are honey bees [6-10], bumble bees [11, 12], and blue orchard bees [9]. The majority of honey bee laboratory studies investigate fungicide impacts on mortality [6, 7, 9]. There is evidence for honey bee mortality as a result of fungicide exposure, but this is variable depending on which are used [6], illustrating that some pose more risk than others. Studies that examine the effects of fungicides on physiology and development find they can destroy cells that line the mid-gut [8] and prevent maturation [6]. Similarly, some studies on bumble bees show certain fungicides cause mortality [13], while others report no negative effects [11, 12, 14]. Again, some fungicides cause mortality to blue orchard bees in the lab, while others do not [9]. The fungicides tested that do exhibit negative effects on bees in the lab are Preston-Mix, Signum, Rovral, Captan, Ziram, Neem oil, and propiconazole. It must be noted that fungicide exposure in the lab does not necessarily reflect what bees encounter in the field. Dosages, concentrations, and exposure can be amplified in laboratory settings.

Field Studies

Compared to laboratory studies, there are even fewer field studies that have examined the effects of fungicides on bees. Some fungicides increase honey bee mortality and alter foraging behavior [15], while others do not [7, 16]. In addition, fungicides applied to orchards during or even prior to bloom can alter the beneficial fungi in the honey bee colony and lead to reduced production of bee bread (larval food) [17]. Bumble bees exposed to the fungicide Manzate experience altered behavior [18]. Alternatively, blue orchard bees exposed to a variety of different fungicides (Manzate excluded), experience no lethal or sublethal effects [19].

Other field studies find population or colony declines as a result of fungicide exposure, but the exact mechanism of action is unknown. For instance, wild bee abundance in New York apple orchards decreases with increasing pesticide use, and this relationship is largely driven by fungicides [20]. Additionally, a positive correlation exists between the presence of fungicide residues in honey bee hives and the occurrence of colony disorders (weakness, queen loss, brood problems, etc.) [2]. The fungicide chlorothalonil has also been detected at elevated levels in the entombed pollen of dying honey bee colonies [21]. Recently, this same fungicide has been found to impair colony growth and queen body size in bumble bees [22]. These associations of fungicides with bee declines warrant further investigation. To date, the fungicides that elicit negative responses in these mentioned field studies are metalaxyl-M, fludioxonil, chlorothalonil and Manzate.

Interaction Effects

Fungicide-pesticide

Laboratory studies have shown that several fungicides interact synergistically with pyrethroid insecticides to increase their toxicity. The risk of toxicity is high for honey bees and moderate for bumble bees when these combinations are present in pollen [4]. Applying these fungicide-insecticide combinations directly on honey bees leads to increased mortality [23-25] and reduced ability to regulate body temperature [26]. Of course, synergism between insecticides and fungicides depends on the pesticides in question [27], as not all combinations may cause increased risk.

In addition to certain pyrethroids, lab experiments have found the toxic effects of neonicotinoids to be increased when combined with fungicides. For instance, Thiacloprid is more toxic when combined with fungicides in the lab, but this effect was not seen in semi-field trials [4, 28]. Negative effects from combinations with imidacloprid have been documented in both honey bees and managed Osmia cornifrons[29] as well. One lab study using Osmia cornifrons examined fungicide interactions in tank mixes – which can contain multiple pesticides and other chemicals – but found no differences in mortality or behavior [19]. Lastly, fungicides have been shown to also increase the toxicity of miticides to honey bees when they are present together [30].

Fungicide-disease

Fungicide-disease interactions have been documented in the honey bee, where these chemicals have been found to increase honey bees’ susceptibility to Nosema ceranae infection [3]. Interestingly, low levels of fumagillin can also increase Nosema infection [31]. Fumagillin is the only registered treatment to control the fungal parasite Nosema. At high dosages it kills Nosema effectively, but at lower doses (for instance, when fumagillin begins to degrade naturally in the hive) Nosema persists. This has important implications for controlling Nosema and suggests the development of alternative treatments is needed. More research overall is needed to untangle the role that fungicides may be playing in bee health at both the individual and population level.

References

  1. Kubik, M., et al., 2000. Residues of captan (contact) and difenoconazole (systemic) fungicides in bee products from an apple orchard. Apidologie,  31(4): p. 531-541.
  2. Simon-Delso, N., et al., 2014. Honeybee Colony Disorder in Crop Areas: The Role of Pesticides and Viruses. Plos One,  9(7).
  3. Pettis, J.S., et al., 2013. Crop Pollination Exposes Honey Bees to Pesticides Which Alters Their Susceptibility to the Gut Pathogen Nosema ceranae. Plos One,  8(7).
  4. Sanchez-Bayo, F. and K. Goka, 2014. Pesticide Residues and Bees - A Risk Assessment. Plos One,  9(4).
  5. Mullin, C., et al., 2010. High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS One,  5: p. e9754.
  6. Mussen, E.C., J.E. Lopez, and C.Y.S. Peng, 2004. Effects of selected fungicides on growth and development of larval honey bees, Apis mellifera L. (Hymenoptera: Apidae). Environmental Entomology,  33: p. 1151-1154.
  7. Mayer, D.F. and J.D. Lunden, 1986. Toxicity of fungicides and an acaricide to honey bees (Hymenoptera, Apidae) and their effects on bee foraging behavior and pollen viability on blooming apples and pears. Environmental Entomology,  15(5): p. 1047-1049.
  8. Gregorc, A. and J.D. Ellis, 2011. Cell death localization in situ in laboratory reared honey bee (Apis mellifera L.) larvae treated with pesticides. Pesticide Biochemistry and Physiology,  99(2): p. 200-207.
  9. Ladurner, E., et al., 2005. Assessing delayed and acute toxicity of five formulated fungicides to Osmia lignaria Say and Apis mellifera. Apidologie,  36(3): p. 449-460.
  10. Papaefthimiou, C. and G. Theophilidis, 2001. The cardiotoxic action of the pyrethroid insecticide deltamethrin, the azole fungicide prochloraz, and their synergy on the semi-isolated heart of the bee Apis mellifera macedonica. Pesticide Biochemistry and Physiology,  69(2): p. 77-91.
  11. Malone, L.A., et al., 2007. No sub-lethal toxicity to bumblebees, Bombus terrestris, exposed to Bt-corn pollen, captan and novaluron. New Zealand Journal of Crop and Horticultural Science,  35(4): p. 435-439.
  12. Mommaerts, V., et al., 2008. Trichoderma-based biological control agents are compatible with the pollinator Bombus terrestris: A laboratory study. Biological Control,  46(3): p. 463-466.
  13. Mommaerts, V., et al., 2012. Miniature-dispenser-based bioassay to evaluate the compatibility of powder formulations used in an entomovectoring approach. Pest Management Science,  68(6): p. 922-927.
  14. Gradish, A.E., et al., 2010. Effect of reduced risk pesticides for use in greenhouse vegetable production on Bombus impatiens (Hymenoptera: Apidae). Pest Management Science,  66: p. 142-146.
  15. Tremolada, P., et al., 2010. Field Trial for Evaluating the Effects on Honeybees of Corn Sown Using Cruiser(A (R)) and Celest xl(A (R)) Treated Seeds. Bulletin of Environmental Contamination and Toxicology,  85(3): p. 229-234.
  16. Fell, R.D., E.G. Rajotte, and K.S. Yoder, 1983. Effects of fungicide sprays during apple bloom on pollen viability and honey bee foraging. Environmental Entomology,  12(5): p. 1572-1575.
  17. Yoder, J.A., et al., 2013. Fungicide Contamination Reduces Beneficial Fungi in Bee Bread Based on an Area-Wide Field Study in Honey Bee, Apis mellifera, Colonies. Journal of Toxicology and Environmental Health-Part a-Current Issues,  76(10): p. 587-600.
  18. Sprayberry, J.D.H., K.A. Ritter, and J.A. Riffell, 2013. The Effect of Olfactory Exposure to Non-Insecticidal Agrochemicals on Bumblebee Foraging Behavior. Plos One,  8(10).
  19. Ladurner, E., et al., 2008. Foraging and nesting behavior of Osmia lignaria (Hymenoptera : megachilidae) in the presence of fungicides: Cage studies. Journal of Economic Entomology,  101(3): p. 647-653.
  20. Park, M.G., et al., 2015. Negative effects of pesticides on wild bee communities can be buffered by landscape context. Proceedings of the Royal Society B-Biological Sciences,  282: p. 20150299.
  21. vanEngelsdorp, D., et al., 2009. "Entombed Pollen": A new condition in honey bee colonies associated with increased risk of colony mortality. Journal of Invertebrate Pathology,  101(2): p. 147-149.
  22. Bernauer, O.M., H.R. Gaines-Day, and S.A. Steffan, 2015. Colonies of Bumble Bees (Bombus impatiens) Produce Fewer Workers, Less Bee Biomass, and Have Smaller Mother Queens Following Fungicide Exposure. Insects,  6: p. 478-488.
  23. Pilling, E.D., et al., 1995. Mechanism of synergism between the pyrethroid insecticide lambda-cyhalothrin and the imiazole fungicide prochloraz, in the honeybee (Apis mellifera L). Pesticide Biochemistry and Physiology,  51: p. 1-11.
  24. Pilling, E.D. and P.C. Jepson, 1993. Synergism between EBI fungicides and a pyrethroid insecticide in the honey bee (Apis mellifera). Pesticide Science,  39(4): p. 293-297.
  25. Meled, M., A. Thrasyvoulou, and L.P. Belzunces, 1998. Seasonal variations in susceptibility of Apis mellifera to the synergistic action of prochloraz and deltamethrin. Environmental Toxicology and Chemistry,  17(12): p. 2517-2520.
  26. Vandame, R. and L.P. Belzunces, 1998. Joint actions of deltamethrin and azole fungicides on honey bee thermoregulation. Neuroscience Letters,  251: p. 57-60.
  27. Thompson, H.M. and H. Folkard-Ward, 2001. Toxicity of realistic combinations of pyrethroids and fungicides to honeybees, in Hazards of Pesticides to Bees, L.P. Belzunces, C. Pelissier, and G.B. Lewis, Editors. p. 83-89.
  28. Schmuck, R., T. Stadler, and H.W. Schmidt, 2003. Field relevance of a synergistic effect observed in the laboratory between an EBI fungicide and a chloronicotinyl insecticide in the honeybee (Apis mellifera L, Hymenoptera). Pest Management Science,  59(3): p. 279-286.
  29. Biddinger, D.J., et al., 2013. Comparative toxicities and synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski). PLoS One,  8(9): p. e72587.
  30. Johnson, R.M., et al., 2013. Acaricide, fungicide and drug interactions in honey bees (Apis mellifera). PLoS One,  8(1): p. e54092.
  31. Huang, W.-F., et al., 2013. Nosema ceranae Escapes Fumagillin Control in Honey Bees. Plos Pathogens,  9(3): p. e1003185.