Reconceptualizing synergism and antagonism among multiple stressors

Abstract

The potential for complex synergistic or antagonistic interactions between multiple stressors presents one of the largest uncertainties when predicting ecological change but, despite common use of the terms in the scientific literature, a consensus on their operational definition is still lacking. The identification of synergism or antagonism is generally straightforward when stressors operate in the same direction, but if individual stressor effects oppose each other, the definition of synergism is paradoxical because what is synergistic to one stressor's effect direction is antagonistic to the others. In their highly cited meta-analysis, Crain et al. (Ecology Letters, 11, 2008: 1304) assumed in situations with opposing individual effects that synergy only occurs when the cumulative effect is more negative than the additive sum of the opposing individual effects. We argue against this and propose a new systematic classification based on an additive effects model that combines the magnitude and response direction of the cumulative effect and the interaction effect. A new class of "mitigating synergism" is identified, where cumulative effects are reversed and enhanced. We applied our directional classification to the dataset compiled by Crain et al. (Ecology Letters, 11, 2008: 1304) to determine the prevalence of synergistic, antagonistic, and additive interactions. Compared to their original analysis, we report differences in the representation of interaction classes by interaction type and we document examples of mitigating synergism, highlighting the importance of incorporating individual stressor effect directions in the determination of synergisms and antagonisms. This is particularly pertinent given a general bias in ecology toward investigating and reporting adverse multiple stressor effects (double negative). We emphasize the need for reconsideration by the ecological community of the interpretation of synergism and antagonism in situations where individual stressor effects oppose each other or where cumulative effects are reversed and enhanced.

Keywords: Antagonism; ecological surprise; interaction; stressor; synergism.

Figure 1

Redrawn from Crain et al. (2008). Conceptual approach to interpreting interaction types from response data presented in factorial studies. Treatments in factorial studies include control (CT), with stressor A (A), with stressor B (B), and with both stressors (A + B). Interaction types are classified as additive, synergistic, and antagonistic, depending on the A + B response compared to the additive sum (AD) of individual effects for stressor A (a), B (b) relative to the control (CT). The three plots show interaction types that have double-negative (i), opposing (ii), and double-positive (iii) individual stressor effects on the response variable of interest.

Figure 2

Our conceptual approach to interpreting interaction types from data presented in factorial studies determined from the magnitude and direction of the cumulative effect and interaction effect in absolute terms. Treatments in factorial studies include control (CT), with stressor A (A), with stressor B (B), and with both stressors (A + B). Directional interaction classes are additive (AD), +synergistic (+S), −synergistic (−S), +antagonistic (+A) and -antagonistic (−A) that vary depending on A + B compared to the additive sum (AD) of individual effects for stressor A (a), B (b) relative to the control (CT). The three plots show interaction types that have double-negative (i), opposing (ii), and double-positive (iii) individual stressors effects on the response variable of interest. (X) indicates that an interaction class is not applicable for the interaction type in question. Figure based on a reanalysis of the database of Crain et al. (2008).