Abstract
Fungicides are found in agricultural areas to protect crops from fungal diseases. When sprayed in areas where honey bee colonies are placed for pollination, bees can collect or otherwise be exposed to these compounds. While labeled safe for bees by the manufacturers, our research found that pollen containing fungicides had a negative effect on the beneficial fungi found in bee colonies that help converting the pollen into bee bread and can end up in the bees themselves. As a result, pathogenic fungi (that cause chalkbrood and stonebrood diseases) were not kept in check by the beneficial fungi, including Aspergillus, Penicillium, Cladosporium, and Rhizopus, which were compromised by the presence of fungicides in the hive. Colonies were found to be weakened by the persistent presence of fungicides. Steps to help protect colonies are outlined.
References
Alarcón R, DeGrandi-Hoffman G, Wardell G (2009) Fungicides can reduce, hinder pollination potential of honey bees. Western Farm Press 31:17–21
Anderson KE, Carroll MJ, Sheehan T, Mott BM, Maes P, Corby-Harris V (2014) Hive-stored pollen of honey bees: many lines of evidence are consistent with pollen preservation, not nutrient conversion. Mol Ecol 23:5904–5917
Aronstein KA, Murray KD (2010) Chalkbrood in honey bees. J Invert Pathol 103:S20–S29
Barnett HL, Hunter BB (2003) Illustrated genera of imperfect fungi, 4th edn. APS Press, St. Paul
Bernauer OM, Gaines-Day HR, Steffan SA (2015) Colonies of bumble bees (Bombus impatiens) produce fewer workers, less bee biomass, and have smaller mother queens following fungicide exposure. Insects 6:478–488
Bernert AC, Sagili RR, Johnson KB (2012) Evaluating pesticide sensitivity of the honey bee (Apis mellifera) microbiome. ESA Annual Meeting Online, Knoxville
Brown AE (2007) Benson’s microbiological applications: laboratory manual in general microbiology. McGraw-Hill, New York
Carlton AJA, Jones A (2007) Determination of imidazole and triazole fungicide residues in honeybees using gas chromatography-mass spectrometry. J Chromatogr A 1141:117–122
Chiesa F, Milani N, D’Agaro M (1989) Observations of the reproductive behavior of Varroa jacobsoni Oud.: techniques and preliminary results. In: Cavalloro R (ed) Proceeding of the meeting of the EC-Experts’ Group, Udine 1988, pp 213–222
Cooper B (1980) Fluctuating broodnest temperature rhythm. Br Isles Bee Breeders News 18:12–16
Foley K, Fazio G, Jensen AB, Hughes WOH (2014) The distribution of Aspergillus spp. opportunistic parasites in hives and their pathogenicity to honey bees. Vet Microbiol 169:203–210
Gilliam M (1979) Microbiology of pollen and bee bread: the yeasts. Apidologie 10:43–53
Gilliam M (1997) Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiol Lett 155:1–10
Gilliam M, Vandenberg JD (1997) Fungi. In: Morse RA, Flottum PK (eds) Honey bee pests, predators and diseases, 79–112
Gilliam M, Taber S III, Lorenz B et al (1988) Factors affecting development of chalkbrood disease in colonies of honey bees, Apis mellifera, fed pollen contaminated with Ascosphaera apis. J Invert Pathol 52:314–325
Gilliam M, Prest DB, Lorenz BJ (1989) Microbiology of pollen and bee bread: taxonomy and enzymology of molds. Apidologie 20:53–68
Jennings DH, Lysek G (1999) Fungal biology: understanding the fungal lifestyle. Springer-Verlag, New York
Johnson RM, Ellis MD, Mullin CA, Frazier M (2010) Pesticides and honey bee toxicity—USA. Apidologie 41:312–331
Johnson RM, Dahlgren L, Siegfried BD et al (2013) Acaricide, fungicide and drug interaction in honey bees (Apis mellifera). PLoS ONE doi:10.1371/journal.pone.0054092
Kubik M, Nowacki J, Pidek A, Warakomska Z, Michalczuk L, Goszczyñski W (1999) Pesticide residues in bee products collected from cherry trees protected during blooming period with contact and systemic fungicides. Apidologie 30:521–532
Kubik M, Nowacki J, Pidek A, Warakomska Z, Michalczuk L, Goszczyñski W, Dwuznik B (2000) Residues of captan (contact) and difenoconazole (systemic) fungicides in bee products from an apple orchard. Apidologie 31:531–541
Mattila HR, Rios D, Walker-Sperling VE, Roeselers G, Newton ILG (2012) Characterization of the active microbiotas associated with honey bees reveals healthier and broader communities when colonies are genetically diverse. PLoS ONE 7:e32962
Morse R (1984) Research review: How far will bees fly? Gleanings in Bee Culture September: 474
Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, vanEnglesdorp D, Pettis JS (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS ONE 5:e9754
Mussen E (2008) Fungicides toxic to bees? Apiculture Newsletter Nov/Dec 2008
Naug D (2009) Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biol Conserv 142:2369–2372
Osintseva LA, Chekryga GP (2008) Fungi of melliferous bees pollenload. Mikol Fitopatol 42:464–469
Pettis JS, Lichtenberg EM, Andree M et al (2013) Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLoS ONE 8(7):1–9. doi:10.1371/journalpone.0070182
Royce L, Yoder J, Nelson B et al (2015) Tree hive colonies: increased quantity of beneficial fungi in bee bread from the trees and its antifungal properties against chalkbrood. Bee Culture March: 59–63
Škerl MIS, Velikonja Bolta S, Baša Česnik H, Gregorc A (2009) Residues of pesticides in honeybee (Apis mellifera carnica) bee bread and in pollen loads from treated apple orchards. Bull Environ Contam Toxicol 83:374–377
Vásquez A, Olofsson T (2009) The lactic acid bacteria involved in the production of bee pollen and bee bread. J Apic Res 48:189–195
West SA, Diggle SP, Buckling A et al (2007) The social lives of microbes. Ann Rev Ecol Evol Syst 38:53–57
Wood M (1998) Microbes help bees battle chalkbrood. Agric Res 46:16–17
Yoder JA, Hedges BZ, Heydinger DJ et al (2012a) Differences among fungicides targeting beneficial fungi associated with honey bee colony. In: Sammataro D, Yoder JA (eds) Honey bee colony health: challenges and sustainable solutions, 181–192
Yoder JA, Heydinger DJ, Hedges BZ et al (2012b) Fungicides reduce symbiotic fungi in bee bread and the beneficial fungi in colonies. In: Sammataro D, Yoder JA (eds) Honey bee colony health: challenges and sustainable solutions, 193–214
Yoder JA, Jajack AJ, Rosselot AE, Smith TJ, Yerke MC, Sammataro D (2013) Fungicide contamination reduces beneficial fungi in bee bread based on an area-wide field study in honey bee, Apis mellifera, colonies. J Tox Environ Health A 76:587–600
Acknowledgements
Special thanks to Dr. Michael A. Senich (Midland, TX) for funding to BWN (Wittenberg University, Springfield, OH).
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Yoder, J.A., Nelson, B.W., Jajack, A.J., Sammataro, D. (2017). Fungi and the Effects of Fungicides on the Honey Bee Colony. In: Vreeland, R., Sammataro, D. (eds) Beekeeping – From Science to Practice. Springer, Cham. https://doi.org/10.1007/978-3-319-60637-8_5
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