From antagonism to synergism: Extreme differences in stressor interactions in one species

Abstract

Interactions between stressors are involved in the decline of wild species and losses of managed ones. Those interactions are often assumed to be synergistic, and per se of the same nature, even though susceptibility can vary within a single species. However, empirical measures of interaction effects across levels of susceptibility remain scarce. Here, we show clear evidence for extreme differences in stressor interactions ranging from antagonism to synergism within honeybees, Apis mellifera. While female honeybee workers exposed to both malnutrition and the pathogen Nosema ceranae showed synergistic interactions and increased stress, male drones showed antagonistic interactions and decreased stress. Most likely sex and division of labour in the social insects underlie these findings. It appears inevitable to empirically test the actual nature of stressor interactions across a range of susceptibility factors within a single species, before drawing general conclusions.

Figure 1

Honeybee drone and worker cage mortality and Nosema ceranae spore loads. (A, B) Survival curves (Kaplan-Meier) indicate the cumulative survival [%] of honeybees over the 14-day experiment for each treatment. In drones, the Pathogen treatment had significantly lower survival when compared to the remaining treatments. In workers, the Combined treatment had the lowest survival, and the Malnutrition treatment was significantly lower than the Control and Pathogen. Different letters indicate a significant difference between treatments. (C,  D) N. ceranae spore loads of individual honeybee drones and workers for each treatment group. For drones, the Pathogen and Combined had significantly higher spore counts than the remaining treatments, but did not differ themselves. For workers, Pathogen had significantly higher spore counts than all other treatments. The boxplots show the inter-quartile range (box), the median (line within box), data range (horizontal lines from box), and outliers (black dots). Different letters indicate a significant difference between treatments.

Figure 2

Honeybee drone and worker cage mortality. Survival curves (Kaplan-Meier) compare the cumulative survival [%] of honeybee (Apis mellifera) workers (grey line) and drones (black line) over the 14-day experiment for each individual treatment: (A) Control, (B) Malnutrition, (C) Pathogen, (D) Combined. The data revealed that workers and drones receiving pollen (A & C) did not significantly differ from one another, whereas workers deprived of pollen (B & D) showed significantly lower survival rates then pollen deprived drones.