High Levels of Miticides and Agrochemicals in North American Apiaries: Implications for Honey Bee Health

By C. Mullin, M. Frazier, J. Frazier, S. Ashcraft, R. Simonds, D. vanEngelsdorp, J. Pettis. PLoS ONE, 2010

1,418 citations recorded by the source corpus.

Background Recent declines in honey bees for crop pollination threaten fruit, nut, vegetable and seed production in the United States. A broad survey of pesticide residues was conducted on samples from migratory and other beekeepers across 23 states, one Canadian province and several agricultural cropping systems during the 2007–08 growing seasons. Methodology/Principal Findings We have used LC/MS-MS and GC/MS to analyze bees and hive matrices for pesticide residues utilizing a modified QuEChERS method. We have found 121 different pesticides and metabolites within 887 wax, pollen, bee and associated hive samples. Almost 60% of the 259 wax and 350 pollen samples contained at least one systemic pesticide, and over 47% had both in-hive acaricides fluvalinate and coumaphos, and chlorothalonil, a widely-used fungicide. In bee pollen were found chlorothalonil at levels up to 99 ppm and the insecticides aldicarb, carbaryl, chlorpyrifos and imidacloprid, fungicides boscalid, captan and myclobutanil, and herbicide pendimethalin at 1 ppm levels. Almost all comb and foundation wax samples (98%) were contaminated with up to 204 and 94 ppm, respectively, of fluvalinate and coumaphos, and lower amounts of amitraz degradates and chlorothalonil, with an average of 6 pesticide detections per sample and a high of 39. There were fewer pesticides found in adults and brood except for those linked with bee kills by permethrin (20 ppm) and fipronil (3.1 ppm). Conclusions/Significance The 98 pesticides and metabolites detected in mixtures up to 214 ppm in bee pollen alone represents a remarkably high level for toxicants in the brood and adult food of this primary pollinator. This represents over half of the maximum individual pesticide incidences ever reported for apiaries. While exposure to many of these neurotoxicants elicits acute and sublethal reductions in honey bee fitness, the effects of these materials in combinations and their direct association with CCD or declining bee health remains to be determined.

Subfields: Ecology, Evolution, Behavior and Systematics, Food Science, Insect Science

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Citations in the corpus

Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment (2012, background): “In some studies, a wide range of pesticides was measured in different bee-related products (Bernal et al. 2010; Chauzat et al. 2009; Mullin et al. 2010; Genersch et al. 2010), while others solely focused on neonicotinoid pesticides.”
Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure (2014, background): “Indeed, recent studies report more than 30 different pesticides inside individual honeybee (Apis mellifera) colonies (Johnson et al. 2010; Mullin et al. 2010) and neonicotinoid residues in the nectar stores of bumblebee (Bombus terrestris) colonies placed in the field next to oilseed rape fields gro”
Quo vadis Aethina tumida? Biology and control of small hive beetles (2016, background): “…pest because they are mostly easy to use and effective, but there are reported problems, for example with the residues of coumaphos pres-ent in wax (Mullin et al. 2010), which can contaminate honey and besides the product does not seem to work well in cooler temperatures (Mostafa and Williams…”
Standard methods for artificial rearing of Apis mellifera larvae (2013, background): “Therefore, the effects of these handicaps and the combination of two or more sublethal effects are extensively investigated (Mullin et al., 2010; Moritz et al., 2010; Genersch et al., 2010).”
The puzzle of honey bee losses: a brief review. (2010, background): “Mullin et al. (2010) indicates that: “frequent coincidence in pollen of high levels of the non-systemic fungicide chlorothalonil with lower levels of systemic pesticides including fungicides is another probable synergistic combination that needs further exploration concerning bee decline”.”
Nosema ceranae disease of the honey bee (Apis mellifera) (2018, background): “Residues of over 100 different pesticides and their metabolites have been detected on bees or in pollen, honey, wax, and equipment (Bogdanov 2006; Chauzat and Faucon 2007; Frazier et al. 2008; Chauzat et al. 2009; Mullin et al. 2010; Lambert et al. 2013; Pettis et al. 2013).”
Standard methods for maintaining adult Apis mellifera in cages under in vitro laboratory conditions (2013, background): “…and environmental contaminants found in bee products All bee products, including honey, corbicular pollen, and bee bread, can contain pathogens, environmental contaminants, and agro-chemical residues (e.g. Bromenshenk et al., 1985; Higes et al., 2008; Chauzat et al., 2009; Mullin et al., 2010).”
Neonicotinoids, bee disorders and the sustainability of pollinator services (2013, neutral): “after the sowing or during the flowering period [89,91,96].”
Impacts of Pesticides on Honey Bees (2016, background): “In recent years, a number of studies have reported the residue levels of agricultural pesticides found in pollen [66, 67] and nectar of flowers [68, 69], in water bodies of agricultural areas [28], as well as in beehive matrices, such as beebread, honey and wax [70, 71].”
Multiple Routes of Pesticide Exposure for Honey Bees Living Near Agricultural Fields (2012, background): “Pesticide exposure has received significant attention and recently-published analyses of pollen from managed bees located near agricultural environments demonstrated that many agricultural chemicals (including insecticides, miticides, fungicides and herbicides) are detectable in honey bee wax and po”