Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae

Abstract

Recent declines in honey bee populations and increasing demand for insect-pollinated crops raise concerns about pollinator shortages. Pesticide exposure and pathogens may interact to have strong negative effects on managed honey bee colonies. Such findings are of great concern given the large numbers and high levels of pesticides found in honey bee colonies. Thus it is crucial to determine how field-relevant combinations and loads of pesticides affect bee health. We collected pollen from bee hives in seven major crops to determine 1) what types of pesticides bees are exposed to when rented for pollination of various crops and 2) how field-relevant pesticide blends affect bees' susceptibility to the gut parasite Nosema ceranae. Our samples represent pollen collected by foragers for use by the colony, and do not necessarily indicate foragers' roles as pollinators. In blueberry, cranberry, cucumber, pumpkin and watermelon bees collected pollen almost exclusively from weeds and wildflowers during our sampling. Thus more attention must be paid to how honey bees are exposed to pesticides outside of the field in which they are placed. We detected 35 different pesticides in the sampled pollen, and found high fungicide loads. The insecticides esfenvalerate and phosmet were at a concentration higher than their median lethal dose in at least one pollen sample. While fungicides are typically seen as fairly safe for honey bees, we found an increased probability of Nosema infection in bees that consumed pollen with a higher fungicide load. Our results highlight a need for research on sub-lethal effects of fungicides and other chemicals that bees placed in an agricultural setting are exposed to.

Figure 1. Pollen collection from the crop where a hive was located was low for most crops.

Bars show mean ± se. Letters indicate statistically significant differences (p<0.05).

Figure 2. Pesticide diversity found in pollen samples, but not pesticide load, varied by crop.

White bars show pesticide diversity, gray bars show pesticide load (mean ± se). Post-hoc testing found the following groups, where letters indicate statistically significant differences: apple a, b; blueberry c; cranberry_early d; cranberry_late b, d, e, f; cucumber e; pumpkin c, d, f; and watermelon d.

Figure 3. Fungicide and neonicotinoid diversities varied by crop.

Bars show the total number of pesticides in each category found in each crop. Kruskal-Wallis test statistics comparing pesticide diversity between crops are: fungicides, H₆ = 16.1, p = 0.01; cyclodienes, H₆ = 6.9, p = 0.33; neonicotinoids, H₆ = 17.9, p = 0.007; organophosphates, H₆ = 14.3, p = 0.03; pyrethroids, H₆ = 7.8, p = 0.26. We only compared pesticide diversities for categories containing at least three chemicals. Sequential Bonferroni adjusted critical values are: 0.01, 0.0125, 0.0167, 0.025, 0.05. A * indicates that the total number of pesticides varied between crops within that pesticide category.

Figure 4. Load varied by pesticide category.

Letters indicate statistically significant differences. The total load for each category is weighted by the number of chemicals in that category, to facilitate comparison across categories.

Figure 5. Probability of Nosema infection increased with fungicide load in consumed pollen.

Histograms show the number of bees with (top) and without (bottom) Nosema spores as a function of the fungicide load in the pollen they were fed. The curve shows the predicted probability of Nosema infection.