Whether warming magnifies the toxicity of a pesticide is strongly dependent on the concentration and the null model

Abstract

How global warming changes the toxicity of contaminants is a research priority at the intersection of global change biology and ecotoxicology. While many pesticides are more toxic at higher temperatures this is not always detected. We studied whether deviations from this general pattern can be explained by concentration-dependent interaction effects and by testing the interaction against the inappropriate null model. We exposed larvae of the mosquito Culex pipiens to three concentrations of the pesticide chlorpyrifos (absence, low and high) in the absence and presence of 4°C warming. Both the low and high chlorpyrifos concentration were lethal and generated negative sublethal effects: activity of acetylcholinesterase (AChE) and total fat content decreased, and oxidative damage to lipids increased, yet growth rate increased. Warming was slightly lethal, yet had positive sublethal effects: growth rate, total fat content and metabolic rate increased, and oxidative damage decreased. For four out of seven response variables the independent action model identified the expected synergistic interaction between chlorpyrifos and warming. Notably, for three variables (survival, AChE and fat content) this was strongly dependent on the chlorpyrifos concentration, and for two of these (AChE and fat content) not associated with a significant interaction in the general(ized) linear models. For survival and fat content, warming only potentiated chlorpyrifos (CPF) toxicity at the low CPF concentration, while the opposite was true for AChE. Our results highlight that taking into account concentration-dependence and appropriate null model testing is crucial to improve our understanding of the toxicity of contaminants in a warming world.

Reduced stress defence responses contribute to the higher toxicity of a pesticide under warming

“…The relevance of studying the impact of chlorpyrifos under warming is shown by several studies in which chlorpyrifos was more toxic at higher temperatures in aquatic insects (e.g., Dinh Van et al, 2014; Janssens & Stoks, 2013; Lydy et al., 1999; Tran et al., 2018). In a companion study (Delnat et al., 2019), we documented for mortality a synergistic interaction (combined effect: ~18%) between a low‐effect chlorpyrifos concentration (single effect: ~11%) and warming (single effect: ~1%). Yet, there was an additive effect (combined effect: ~57%) between a high‐effect chlorpyrifos concentration (single effect: ~53%) and warming (single effect: ~1%) based on the IA model.…”

“…The clean reads were visually inspected with fastqc version 0.11.8 (Andrews, 2010). RNA sequence reads have been deposited in the NCBI Sequence Read Archive (SRA) under accession PRJNA637105 (Delnat et al, 2020a).…”

“…This synergism between toxicants and warming is known as the “climate‐induced toxicant sensitivity” (CITS) concept (Hooper et al., 2013; Moe et al., 2013; Noyes & Lema, 2015). Nevertheless, even within contaminant groups that typically follow the CITS pattern, support for it is not always present or may be concentration‐dependent (e.g., Delnat et al., 2019; Table 1 in Holmstrup et al., 2010). To improve our insights into the CITS concept and, in general, the combined effects of multiple stressors, a better mechanistic understanding is needed (Camp & Buchwalter, 2016; Griffen et al., 2016; Kaunisto et al., 2016; Song et al., 2018).…”

“…The IA model assumes additivity of two effects in terms of the probabilistic sum, which accounts for the probability that an individual that is killed by one stressor cannot be killed by the other stressor by subtracting the product of their effect (Bliss, 1939; Schäfer & Piggott, 2018; see Supplementaries , including Figure S1 and Table S1). Several studies have successfully applied the IA model to study the interactive effects at the organismal level between contaminants and natural stressors such as predation and parasitism (e.g., Coors & De Meester, 2008; Pestana et al., 2009), UV radiation (Korkaric et al., 2015; Yu et al., 2015) and warming (Delnat et al., 2019). The IA model has only recently been successfully applied at the molecular level for assessing the combined effects of the contaminant uranium and gamma radiation (Song et al., 2018).…”

“…Yet, there was an additive effect (combined effect: ~57%) between a high‐effect chlorpyrifos concentration (single effect: ~53%) and warming (single effect: ~1%) based on the IA model. In this companion study, we studied, next to survival, effects on growth rate, and physiology (acetylcholinesterase activity, total fat content, metabolic rate and oxidative stress; Delnat et al., 2019). We complemented the current study with an in‐depth analysis of the gene expression patterns using RNA‐sequencing (RNA‐seq).…”