Assessing Honey Bee (Hymenoptera: Apidae) Foraging Populations and the Potential Impact of Pesticides on Eight U.S. Crops.

Beekeepers who use honey bees (Apis mellifera L.) for crop pollination services, or have colonies making honey on or in close proximity to agricultural crops, are concerned about the reductions of colony foragers and ultimate weakening of their colonies. Pesticide exposure is a potential factor in the loss of foragers. During 2009-2010, we assessed changes in the field force populations of 9-10 colonies at one location per crop on each of the eight crops by counting departing foragers leaving colonies at regular intervals during the respective crop blooming periods. The number of frames of adult bees was counted before and after bloom period. For pesticide analysis, we collected dead and dying bees near the hives, returning foragers, crop flowers, trapped pollen, and corn-flowers associated with the cotton crop. The number of departing foragers changed over time in all crops except almonds; general patterns in foraging activity included declines (cotton), noticeable peaks and declines (alfalfa, blueberries, cotton, corn, and pumpkins), and increases (apples and cantaloupes). The number of adult bee frames increased or remained stable in all crops except alfalfa and cotton. A total of 53 different pesticide residues were identified in samples collected across eight crops. Hazard quotients (HQ) were calculated for the combined residues for all crop-associated samples and separately for samples of dead and dying bees. A decrease in the number of departing foragers in cotton was one of the most substantial crop-associated impacts and presented the highest pesticide risk estimated by a summed pesticide residue HQ.

Weighing risk factors associated with bee colony collapse disorder by classification and regression tree analysis.

Colony collapse disorder (CCD), a syndrome whose defining trait is the rapid loss of adult worker honey bees, Apis mellifera L., is thought to be responsible for a minority of the large overwintering losses experienced by U.S. beekeepers since the winter 2006-2007. Using the same data set developed to perform a monofactorial analysis (PloS ONE 4: e6481, 2009), we conducted a classification and regression tree (CART) analysis in an attempt to better understand the relative importance and interrelations among different risk variables in explaining CCD. Fifty-five exploratory variables were used to construct two CART models: one model with and one model without a cost of misclassifying a CCD-diagnosed colony as a non-CCD colony. The resulting model tree that permitted for misclassification had a sensitivity and specificity of 85 and 74%, respectively. Although factors measuring colony stress (e.g., adult bee physiological measures, such as fluctuating asymmetry or mass of head) were important discriminating values, six of the 19 variables having the greatest discriminatory value were pesticide levels in different hive matrices. Notably, coumaphos levels in brood (a miticide commonly used by beekeepers) had the highest discriminatory value and were highest in control (healthy) colonies. Our CART analysis provides evidence that CCD is probably the result of several factors acting in concert, making afflicted colonies more susceptible to disease. This analysis highlights several areas that warrant further attention, including the effect of sublethal pesticide exposure on pathogen prevalence and the role of variability in bee tolerance to pesticides on colony survivorship.

Colony collapse disorder: a descriptive study.

BACKGROUND: Over the last two winters, there have been large-scale, unexplained losses of managed honey bee (Apis mellifera L.) colonies in the United States. In the absence of a known cause, this syndrome was named Colony Collapse Disorder (CCD) because the main trait was a rapid loss of adult worker bees. We initiated a descriptive epizootiological study in order to better characterize CCD and compare risk factor exposure between populations afflicted by and not afflicted by CCD. METHODS AND PRINCIPAL FINDINGS: Of 61 quantified variables (including adult bee physiology, pathogen loads, and pesticide levels), no single measure emerged as a most-likely cause of CCD. Bees in CCD colonies had higher pathogen loads and were co-infected with a greater number of pathogens than control populations, suggesting either an increased exposure to pathogens or a reduced resistance of bees toward pathogens. Levels of the synthetic acaricide coumaphos (used by beekeepers to control the parasitic mite Varroa destructor) were higher in control colonies than CCD-affected colonies. CONCLUSIONS/SIGNIFICANCE: This is the first comprehensive survey of CCD-affected bee populations that suggests CCD involves an interaction between pathogens and other stress factors. We present evidence that this condition is contagious or the result of exposure to a common risk factor. Potentially important areas for future hypothesis-driven research, including the possible legacy effect of mite parasitism and the role of honey bee resistance to pesticides, are highlighted.