Exposure to a heat wave under food limitation makes an agricultural insecticide lethal: a mechanistic laboratory experiment

Abstract

Extreme temperatures and exposure to agricultural pesticides are becoming more frequent and intense under global change. Their combination may be especially problematic when animals suffer food limitation. We exposed Coenagrion puella damselfly larvae to a simulated heat wave combined with food limitation and subsequently to a widespread agricultural pesticide (chlorpyrifos) in an indoor laboratory experiment designed to obtain mechanistic insights in the direct effects of these stressors in isolation and when combined. The heat wave reduced immune function (activity of phenoloxidase, PO) and metabolic rate (activity of the electron transport system, ETS). Starvation had both immediate and delayed negative sublethal effects on growth rate and physiology (reductions in Hsp70 levels, total fat content, and activity levels of PO and ETS). Exposure to chlorpyrifos negatively affected all response variables. While the immediate effects of the heat wave were subtle, our results indicate the importance of delayed effects in shaping the total fitness impact of a heat wave when followed by pesticide exposure. Firstly, the combination of delayed negative effects of the heat wave and starvation, and the immediate negative effect of chlorpyrifos considerably (71%) reduced larval growth rate. Secondly and more strikingly, chlorpyrifos only caused considerable (ca. 48%) mortality in larvae that were previously exposed to the combination of the heat wave and starvation. This strong delayed synergism for mortality could be explained by the cumulative metabolic depression caused by each of these stressors. Further studies with increased realism are needed to evaluate the consequences of the here-identified delayed synergisms at the level of populations and communities. This is especially important as this synergism provides a novel explanation for the poorly understood potential of heat waves and of sublethal pesticide concentrations to cause mass mortality.

Temperature-and sex-specific grazing rate of a tropical copepod Pseudodiaptomus annandalei to food availability: Implications for live feed in aquaculture

“…| 3869 (Angilletta, 2009;Angilletta, Niewiarowski, & Navas, 2002;Grote et al, 2015;Hirche, 1987). A strong reduction in the pellet production at 35°C may be a result of physiological depression, that has been observed in aquatic taxa in shallow water bodies exposed to extreme temperatures, for example, damselfly (Dinh, Janssens, & Stoks, 2016), intertidal species (Dong, Yu, Wang, & Dong, 2011;McArley, Hickey, & Herbert, 2017) and copepods (Low et al, 2018…”

Resilience to heat waves in the aquatic snail Lymnaea stagnalis: Additive and interactive effects with micropollutants

“…Moreover, snails exposed to both high temperature and MPs antagonistically reduced their feeding rate. Metabolic imbalance can lead to tradeoffs between important fitness traits (Reznick, Nunney, & Tessier, 2000;Van Noordwijk & de Jong, 1986) or even reduce the rate of all energy-demanding processes due to metabolic depression (Dinh et al, 2016). In fact, the observed discrepancy between resource demand and uptake during the heat wave (and when concurrently exposed to MPs) reduced investment in energydemanding processes (i.e.…”

“…Burton & Metcalfe, ; Mousseau & Fox, ). Moreover, stress effects may also manifest themselves as reduced recovery of individuals from stress after conditions become benign again (Dinh et al., ). Thus, understanding the conjoint and long‐term effects of heat waves on organisms is in high demand when predicting the effects of climate change.…”

“…Przeslawski, Byrne, & Mellin, 2015), predicting stress responses in nature based on individual impacts of different stressors is problematic. Predicting this is especially challenging because conducted work focuses on the immediate impacts of extreme temperatures and their interactions with other stressors (Dinh, Janssens, & Stoks, 2016). However, some environmental stress effects may only become evident after a lag time due to individual level delayed effects (e.g.…”

Simultaneous exposure to a pulsed and a prolonged anthropogenic stressor can alter consumer multifunctionality

“…Heat stress is particularly relevant as aquatic ecosystems are dominated by ectotherms, whose metabolic demands (Vannote andSweeney 1980, Salo et al 2017), growth (Leicht et al 2013) and reproductive output (Salo et al 2017) is largely determined by environmental temperature (Angilletta 2009). At the same time, chemical pollution may further alter organismal performance, such as resource requirements (Dinh et al 2016) and reproduction (Salo et al 2017). Maintaining organismal function at higher temperatures, while simultaneously needing more resources for detoxification of chemical toxicants (Broomhall 2002), can cause energetic conflicts.…”