Pesticide-Virus Interactions in Honey Bees: Challenges and Opportunities for Understanding Drivers of Bee Declines

Abstract

Honey bees are key agricultural pollinators, but beekeepers continually suffer high annual colony losses owing to a number of environmental stressors, including inadequate nutrition, pressures from parasites and pathogens, and exposure to a wide variety of pesticides. In this review, we examine how two such stressors, pesticides and viruses, may interact in additive or synergistic ways to affect honey bee health. Despite what appears to be a straightforward comparison, there is a dearth of studies examining this issue likely owing to the complexity of such interactions. Such complexities include the wide array of pesticide chemical classes with different modes of actions, the coupling of many bee viruses with ectoparasitic Varroa mites, and the intricate social structure of honey bee colonies. Together, these issues pose a challenge to researchers examining the effects pesticide-virus interactions at both the individual and colony level.

Keywords: honey bee virus; insecticide–virus synergism; pesticide resistance; toxicology; virus tolerance/resistance.

Figure 1

(A) Pesticide × virus interactions require integration of many potential scenarios, and there are many challenges in understanding the relevance of potential interactions. Pesticide considerations: Honey bees can and have been exposed to many different pesticide types (insecticides, fungicides, herbicides, etc.), each containing multiple classes with different modes of action. Product formulations also contain adjuvants and “inert” chemicals that can interact with active ingredients to alter pesticide sensitivity in bees. One must also consider how application methods might affect how bees are exposed to the pesticides. Virus considerations: honey bees can be infected with more than 20 different types of viruses, often at the same time, and there are likely coinfection interactions (DWV: deformed wing virus; SBV: sacbrood virus; IAPV: Israeli acute paralysis virus; LSV: Lake Sinai virus; BQCV: black queen cell virus; ABPV: acute bee paralysis virus). At the same time, variable pressure from Varroa mites and other pathogens can affect these dynamics. The route of exposure to these viruses is likely to cause different responses in the infected bees. Overall considerations: for both pesticide and virus experiments, the context of investigation can also yield variable responses. Bees of different caste (queen vs. worker), developmental stage (egg, larva, pupa, and adult), and age can all experience these stressors differently. Further, most experimental manipulations of pesticide and virus stress are done outside of the colony context; honey bee colony units can respond differently than individuals or small groups in experimental settings. Thus, studying pesticide/virus interactions in honey bees sounds deceptively simple; however, the potential interactions make investigation a significant challenge. (B) Pesticide exposure can negatively impact many components and pathways of the immune system. Phagocytosis: pro-hemocyte differentiation can be impaired, resulting in fewer phagocytosing immune cells. The process of phagocytosis itself can also be affected; autophagy: Regulation of autophagy can be disrupted, potentially leading to apoptosis in cells; receptor activity: some insecticides target receptors that are also involved in antiviral defenses; gene expression: pesticides can alter expression of immune and detoxification genes. This includes upregulating inhibitors of the important immune system transcription factor, NF-κB; heat shock proteins: some pesticides downregulate expression of genes coding for heat shock proteins. These proteins can reduce viral load and also have functions in the RNAi antiviral pathway; gut bacteria: pesticides can also disrupt gut microbial communities, which are known to play roles in honey bee health and immunity.