The Exposure Order Strongly Modifies How a Heat Spike Increases Pesticide Toxicity

Abstract

The exposure order may strongly affect the impact of stressors, yet is largely ignored for the frequently occurring combinations of toxicants with natural stressors. We tested how exposure order shaped the interactive effects of serial exposure to the pesticide chlorpyrifos and to a heat spike in the larvae of the mosquito Culex pipiens. Notably, the chlorpyrifos-induced mortality was much more magnified by the heat spike and a synergism was already detected at the low concentration when exposure to chlorpyrifos followed the heat spike. This suggests that the preceding heat spike weakened the larvae as reflected in their lower net energy budget, moreover the chlorpyrifos-induced inhibition of its target enzyme (acetylcholinesterase) was only magnified by the heat spike when it was the first stressor. Also the chlorpyrifos-induced reduction in heat tolerance was stronger when the pesticide pulse followed the heat spike, and was buffered by the heat spike when this was the second stressor. Our results provide the first evidence that the exposure order can strongly change the magnifying effect of an important climate change factor on the toxicity of a pesticide. This highlights the importance of exposure order in ecological risk assessment of toxicants under realistic combinations with natural stressors.

Thermal plasticity and sensitivity to insecticides in populations of an invasive beetle: Cyfluthrin increases vulnerability to extreme temperature

“…The authors also showed that the reduction in heat tolerance was smaller when the animals had been pre exposed to higher temperatures, a finding that is in line with our study. In addition, Delnat et al (2019) found that pesticide exposure decreased temperature tolerance in mosquito larvae and males, and Meng, Delnat, and Stoks (2020) showed that pesticide J o u r n a l P r e -p r o o f exposure prior to experiencing a heat spike reduced heat tolerance of mosquito larvae. This reduction in temperature tolerance following pesticide exposure is also true for other taxa, as critical thermal maximum was also reduced in fishes after exposure to endosulfan and chlorpyrifos (Heath et al 1994;Patra et al 2007).…”

“…However, the higher inhibition of acetylcholine esterase suggested that heat waves may increase the sensitivity of damselflies to this chemical. More recent studies have examined the effects of successive heat spikes and pesticide exposure (Meng, Delnat, and Stoks 2020), and the delayed effects of pesticide exposures on life histories of insects (Dinh, Janssens, and Stoks 2016).…”

“…Moreover, all but one of these studies used insect larvae, and all investigations were based on aquatic species, meaning that terrestrial insect species and adult life stages are severely underrepresented from this research. Likewise, some studies have investigated the thermal tolerance of insects after they were exposed to pesticides (Op de Beeck, Verheyen, andStoks 2017, 2018;Delnat et al 2019;Meng, Delnat, and Stoks 2020). Yet again, all of these investigations have focused on aquatic larvae, and used the organophosphate chlorpyrifos.…”

“…Insects preexposed to daily heat spikes were expected to recover faster from heat shock, but slower from cold shock treatments, compared to insects kept at constant temperature. Furthermore, insects exposed to insecticides were hypothesized to be characterized by a lower ability to cope with temperature stress, either due to an increased toxicity of the chemical with daily heat spikes or decreased ability to cope with heat shock after chemical stress (Op de Beeck, Verheyen, and Stoks 2017;Delnat et al 2019;Meng, Delnat, and Stoks 2020).…”

Exposure order effects of consecutive stressors on communities: the role of co‐tolerance

“…However, the importance of temporal factors (i.e. order and timing of exposures) affecting communities remains relatively unexplored (Thompson et al 2018, Brooks and Crowe 2019, Jackson et al 2021) compared to those affecting single species (Cheng et al 2015, Boyd et al 2018, Meng et al 2020. Instead, most empirical evidence of community responses to combined stressors has been derived from simultaneous, rather than sequential, exposures (Gunderson et al 2016).…”