Combined effects of larval exposure to a heat wave and chlorpyrifos in northern and southern populations of the damselfly Ischnura elegans
Introduction
There is a surge of interest in the impact of pesticides under global climate change, mainly because many pesticides are more toxic at higher temperatures (Noyes et al., 2009, Moe et al., 2013) and a strong increase in pesticide exposure is expected (Kattwinkel et al., 2011). Extreme aspects of global warming, such as heat waves (Meehl and Tebaldi, 2004), may be especially relevant to study. This is because strong synergistic effects with pesticides generally occur when the natural stressor induces a strong physiological response (Holmstrup et al., 2010), which is the case for heat waves (Pörtner and Farrell, 2008).
Despite the many studies looking at the combined exposure to pesticides and heat stress (Holmstrup et al., 2010), potential delayed effects of a heat wave on vulnerability to pesticides have been ignored. With short heat waves and pesticide pulses being frequent, situations where pesticide pulses are succeeding heat waves should be common. Under this scenario, animals will be exposed to the pesticide at the ambient temperature. Therefore, the increased metabolic activity caused by the heat wave and associated lowered energy storage could increase vulnerability to the pesticide (Sokolova and Lanning, 2008).
An added complexity in the study of contaminants under global warming is that local thermal adaptation may mediate the effects of pesticides under higher temperatures (Moe et al., 2013, Dinh Van et al., 2013). Given that populations at lower latitudes experience a higher frequency of heat waves they are likely adapted to heat waves (Orlowski and Seneviratne, 2012). The study of the combined effects of heat waves and pesticide exposure therefore demands for a spatially explicit approach at different latitudes (Fukami and Wardle, 2005).
As ‘test-of-principle’ we investigated whether a heat wave makes damselfly larvae more vulnerable to a subsequent exposure to the chlorpyrifos (CPF) and whether this differs between high- and low-latitude populations. Damselfly larvae are particularly sensitive to global warming (Hassall and Thompson, 2008) and to organic toxicants (Liess and Von der Ohe, 2005). We chose to study Ischnura elegans (odonata, Coenagrionidae) as this is a very common damselfly species in Europe showing a broad latitudinal range (Dijkstra, 2006) and its response to CPF has been well studied (e.g. Dinh Van et al., 2014, Janssens et al., 2014). CPF, an organophosphate insecticide, is an important pesticide to study in this context as it is a priority pollutant in the European Water Framework Directive (2000/60/EC) which has been approved under the European plant protection products regulation (1107/2009). Note that it is not our aim to explicitly test the validity of the safe concentrations according to current legislation, instead we want to provide ‘proof-of-principle’ of delayed pesticide effects of exposure to a heat wave. Previous investigation studied the effect of a heat wave in the adult stage after pre-exposure to CPF in the larval stage (Janssens et al., 2014). In this research we inverted the methodology in order to assess the delayed effect of a heat wave on CPF sensitivity within the larval stage. As both stressors are in current study not separated by metamorphosis, stronger synergistic effects may be expected (Campero et al., 2008).
We measured effects on two life-history traits (mortality and growth rate) and four fitness-related biochemical markers: fat content, the level of the heat shock protein Hsp70, and the activities of the enzymes acetylcholinesterase (AChE) and phenoloxidase (PO). Because organophosphate insecticides act as AChE inhibitors, AChE activity has been widely used as a biomarker of CPF exposure (Fulton and Key, 2001). The levels of Hsp70, proteins involved in maintaining cellular homeostasis, have been shown to increase in response to pesticide and heat stress (Sorensen et al., 2003). As detoxification is energetically costly, the fat content can be reduced by pesticide exposure (Janssens and Stoks, 2013a). Because pesticide exposure can suppress the immune response (Galloway and Depledge, 2001), we measured PO activity, a key enzyme of the insect immune system (González-Santoyo and Córdoba-Aguilar, 2012).
Section snippets
Test animals and rearing conditions
I. elegans populations were collected at the low-latitude and the high-latitude parts of the species’ range in Europe (Dijkstra, 2006). At the northern latitude, two Swedish populations were sampled: Eriksö (SWER, 58°39′N, 17°34′E) and Lund (SWLU, 55°40′N, 13°03′E). At the southern latitude, one population was sampled in north-eastern Spain, Ferrol (SP, 43°29′N, 8°18′W) and one population was sampled in south France, Saint-Martin-de-Crau (FR, 43°38′N, 4°49′E). The north–south distance between
Pesticide effects
Exposure to CPF significantly reduced survival to ca. 90% (Fig. 1b and Table 1). Similarly, the growth rate was reduced in the presence of CPF (Fig. 1d and Table 1).
Overall, we observed a moderate, but not significant, decrease of AChE activity in CPF-exposed groups (Fig. 2a and Table 2). CPF exposure had no main effect on Hsp70 levels (Fig. 2b and Table 2). The fat content was significantly reduced in groups exposed to CPF (Fig. 2c and Table 2). Instead, PO activity was approximately two times
Discussion
We investigated whether a heat wave makes I. elegans damselfly larvae more sensitive to subsequent CPF exposure. Furthermore, testing this hypothesis in from two different latitudes, allowed us to assess whether local thermal adaptation may mitigate heat wave effects.
Acknowledgments
We thank Bert Deruyck, Frank Johansson, Philippe Lambret and Iago Sanmartin-Villar for collecting damselfly eggs and Ria Van Houdt and Rony Van Aerschot for assistance during the experiment. Comments by two anonymous reviewers considerably improved the manuscript. Financial support came from the French Ministry of Ecology, Sustainable Development and Energy, FWO Grant G.0610.11, the Belspo project Speedy, and the KU Leuven Centre of Excellence program PF/2010/07.
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