Parasites and pesticides act antagonistically on honey bee health

Abstract

Pesticides and parasites have each been linked to increased mortality in western honey bees (Apis mellifera). Currently, it is uncertain if one makes the other worse; several studies have tested for potential synergistic stressor effects, but results have been mixed. Here, we use a hierarchical meta‐analysis of 63 experiments from 26 studies to gain a clearer view of the combined effects of parasites and pesticides on honey bee health. We found that combined pesticide–parasite treatments do tend to be deadlier than uncombined treatments but are significantly less deadly than predicted additive or multiplicative effects. In other words, combined treatment effects are not synergistic, but antagonistic. Much of the previous uncertainty about the combined effects of pesticides and parasites on honey bee health can be attributed to a bias in the previous research against stressor antagonism; many researchers have excluded the possibility of antagonism a priori. Synthesis and applications. Meta‐analysis shows that when honey bees are stressed by a combination of pesticides and parasites, the combined stress effect is antagonistic, that is, less than the sum of its parts. A better understanding of the mechanisms underlying this antagonism could prove critical for effective management of honey bee health.

Varying impact of neonicotinoid insecticide and acute bee paralysis virus across castes and colonies of black garden ants, Lasius niger (Hymenoptera: Formicidae)

“…In contrast to our expectations, the colony strength (number of workers and brood) of the combined treatment was not different from the neonicotinoid and virus treatment. Thus, at colony level, the two stressors interact antagonistically, meaning that co-exposed colonies are doing better than expected if the individual effects of viruses and neonicotinoids are summed up 36 , 37 , 81 . These findings are in line with studies in bees suggesting that interactions between pesticides and pathogens are often antagonistic, particularly interactive effects on proxies of fitness such as behaviour, parasite load and immune responses 36 , 37 .…”

“…Thus, at colony level, the two stressors interact antagonistically, meaning that co-exposed colonies are doing better than expected if the individual effects of viruses and neonicotinoids are summed up 36 , 37 , 81 . These findings are in line with studies in bees suggesting that interactions between pesticides and pathogens are often antagonistic, particularly interactive effects on proxies of fitness such as behaviour, parasite load and immune responses 36 , 37 . Overall, these results highlight that the nature of stressor impacts and interactions strongly depends on the variable and effect level looked at.…”

“…Furthermore, long-term exposure inevitably leads to co-exposure and potential interactions with other stressors. Although interactions amongst stressors are often assumed to be synergistic per se, they may be additive or even antagonistic depending on the nature of the stressors and susceptibility of an organism 36 , 37 , which in turn underlies inter- and intra-species specific variability 31 . Factors such as age, developmental stage or sex influence stressor susceptibility leading to within-species differences 31 , 38 .…”

Synergistic and Antagonistic Interactions Between Varroa destructor Mites and Neonicotinoid Insecticides in Male Apis mellifera Honey Bees

“…Individually, they can elicit a range of negative consequences on honey bees, ranging from sub-lethal physiological and behavioral effects to lethal ones that result in reduced survival (Havard et al, 2020). When acting in concert, diverse effects are observed, ranging from antagonistic parasitic-pesticide interactions to synergistic pesticide-pesticide ones (Straub et al, 2020;Bird et al, 2021;Siviter et al, 2021).…”

“…Despite V. destructor and neonicotinoids considered to ubiquitous stressors to honey bees (Little et al, 2015;Wilfert et al, 2016;Colwell et al, 2017;Mitchell et al, 2017), little is known about their potential interactive effects in honey bees. A handful of studies on non-reproductive honey bee females, the workers, have yielded conflicting results, ranging from no interaction to synergism (Straub et al, 2016;Siede et al, 2018;Morfin et al, 2020;Bird et al, 2021); however, no such work has investigated possible effects on honey bee drones, despite their predicted greater susceptibility to environmental stressors as proposed by the haploid susceptibility hypothesis (O' Donnell and Beshers, 2004), which suggests that drones are likely less resilient to environmental stressors than their worker counterparts due to a lack in allelic variation at important immune related genes (Hamilton, 1964;O'Donnell and Beshers, 2004;Retschnig et al, 2014;Friedli et al, 2020). The availability of high quality drones to mate with reproductive honey bee females, the queens, is crucial for the fitness of those queens and their colonies (Koeniger and Koeniger, 2007), since genetic variation confers benefits such as increased resilience to biotic risk factors (Tarpy, 2003;Tarpy and Seeley, 2006;Delaplane et al, 2015;Simone-Finstrom et al, 2016).…”