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

Abstract

BackgroundRecent 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 FindingsWe 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/SignificanceThe 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.

Honey bee‐collected pollen in agro‐ecosystems reveals diet diversity, diet quality, and pesticide exposure

“…(2010) documented residues in 23 states and one province and reported nearly triple the total residues detected in this study (98 compared to our 39). Eighty‐nine percent of samples in our study had at least one residue detected, similar to 87.7% of samples in the French study (Chauzat et al., 2006), whereas 100% of pollen samples in the American study had at least one residue detected (Mullin et al., 2010). We also observed only 3.9 residues within crop sites compared to 7.1 reported by Mullin et al.…”

“…Testing honey bee foragers themselves, and for presence of residues in honey stomachs, could address this unresolved issue. A related question from this study is how traditionally in‐hive chemicals (i.e., coumaphos, fluvalinate) got in pollen that had been trapped outside of colonies, as has also been reported elsewhere (Chauzat et al., 2006; Mullin et al., 2010). …”

“…Samples were analyzed using a modified popular method for testing food products for residues, called QuEChERS, the quick, easy, cheap, effective, rugged, and safe method, which involves concurrent analysis by gas chromatography/mass spectrometry and liquid chromatography/tandem mass spectrometry (Lehotay, Maštovaká, & Lightfield, 2005; Mullin et al., 2010). …”

“…To illustrate the pesticide problem, one study of honey bee‐collected pollen (hereafter, pollen) in 23 states and one Canadian province found 98 different pesticide residues, with a mean of 7.1 residues per pollen sample (Mullin et al., 2010). A similar survey in France found the neonicotinoid imidacloprid in 49.4% of samples and had from 1 to 5 different residues in positive samples (testing for up to 41 different residues; Chauzat et al., 2006; also see Porrini et al., 2016).…”

Weight of evidence evaluation of a network of adverse outcome pathways linking activation of the nicotinic acetylcholine receptor in honey bees to colony death

“…Over 100 pesticides have been detected in honey bees and hive products, indicating that multiple chemical exposures occur with the potential for numerous interacting effects (Mullin et al, 2010). For example, Palmer et al (2013) described additive adverse effects on neuronal function in Kenyan cells from isolated honey bee brains following combined exposure to both neonicotinoids and an organophosphate.…”