Multiple Stress Reduces the Advantage of Pesticide Adaptation

Abstract

Under global change scenarios, multistress conditions may occur regularly and require adaptation. However, the adaptation to one stressor might be associated with the increased sensitivity to another stressor. Here, we investigated the ecological consequences of such trade-off under multiple stress. We compared the pesticide tolerance of the crustacean Gammarus pulex from agricultural streams with populations from reference streams. Under optimum temperature, G. pulex from agricultural streams were considerably more tolerant to pesticides as compared to the reference populations. Here, we assume that the increased tolerance in agricultural populations is the combination of acclimation, epigenetic effect, and genetic evolution. After experimental pre-exposure to very low concentration (LC50/1000), reference populations showed increased pesticide tolerance. In contrast, pre-exposure did not further increase the tolerance of agricultural populations. Moreover, these populations were more sensitive to elevated temperature alone due to the hypothesized fitness cost of genetic adaptation to pesticides. However, both reference and agricultural populations showed a similar tolerance to the combined stress of pesticides and warming due to stronger synergistic effects in adapted populations. As a result, pesticide adaptation loses its advantage. The combined effect was predicted well using the stress addition model, developed for predicting the synergistic interaction of independent stressors. We conclude that under multistress conditions, adaptation to pesticides reduces the general stress capacity of individuals and trade-off processes increase the sensitivity to additional stressors. This causes strong synergistic effects of additional stressors on pesticide-adapted individuals.

Neglected impacts of plant protection products on invertebrate aquatic biodiversity: a focus on eco-evolutionary processes

“…Temporal fluctuations in tolerance levels were recorded in the field, with an unexpected pattern of negative correlation with exposure levels along the seasons, explained as a reduction in potential variability of sensitivities within populations at the maximum of the cultural treatments, which may induce high lethal stress in streams (Becker et al 2020). The genetic or plastic nature of tolerance seems here again not totally exclusive depending on the exposure history of populations (Siddique et al 2021).…”

“…Pyrethroid resistance in Hyalella has hence been associated to fitness costs for tolerant organisms with increased susceptibility to thermal stress and lower reproductive capacities (Heim et al 2018). Neonicotinoid tolerance in Gammarus pulex population from agricultural areas goes with reduced demographic growth when populations are cultured under PPP-free conditions in the laboratory (Siddique et al 2020), and increased susceptibility to elevated temperature (Siddique et al 2021). These observations highlight a major challenge in the context of ongoing global change, characterized by multiple stress situations in the future aquatic environment.…”

“…One classical example in ecotoxicology for phenotypic flexibility is the acclimation during pre-exposure to chronic concentrations of a toxicant that increases the acute tolerance in case of subsequent exposure to the same chemical. Although studies addressing the contribution of phenotypic plasticity to PPP tolerance remain extremely rare in comparison for instance with a growing number of studies documenting this mechanism for metallic contaminants, a recent illustration was reported for the tolerance of the freshwater crustacean Gammarus pulex preexposed in the laboratory to the neonicotinoid insecticide clothianidin(Siddique et al 2021). The response is moreover considered «…”

Uncovering the Grinnellian niche space of the cryptic species complex Gammarus roeselii

“…In recent years, Gammarus spp. have increasingly been used as test organisms for studying adaptation processes to various anthropogenic stressors ( Schulz & Liess, 1999 ; Bundschuh & Schulz, 2011 ; Shahid et al, 2018a , 2018b ; Siddique et al, 2020 ; Siddique, Shahid & Liess, 2021 ; Grethlein et al, 2022 ). So far, mostly intraspecific differences between populations in anthropogenically stressed regions were compared with pristine regions.…”

The spatiotemporal profile and adaptation determine the joint effects and interactions of multiple stressors

“…Consequently, future stress of similar intensity may have a lower effect on adapted individuals, populations, and communities, respectively [6,31]. Moreover, adaptation can determine the response to additional stressors, for instance, through co-tolerance [45], tradeoffs [46], or maladaptation [47].…”