Elsevier

Chemosphere

Volume 128, June 2015, Pages 148-154
Chemosphere

Combined effects of larval exposure to a heat wave and chlorpyrifos in northern and southern populations of the damselfly Ischnura elegans

https://doi.org/10.1016/j.chemosphere.2015.01.044Get rights and content

Highlights

  • Damselfly larvae were sequentially exposed to a heat wave and chlorpyrifos.

  • Surprisingly, the heat wave positively affected fat storage and immune function.

  • Chlorpyrifos had strong negative effects on survival, growth and fat storage.

  • The AChE inhibition by chlorpyrifos was magnified by the heat wave.

  • Delayed effects of heat waves may make damselflies more vulnerable to pesticides.

Abstract

Heat waves are generally associated with an increased energy consumption and could thus increase the vulnerability to subsequent pesticide exposure. We investigated the combined effect of a heat wave and subsequent exposure to the pesticide chlorpyrifos in Ischnura elegans damselfly larvae. To assess local thermal adaptation to heat waves, we applied these combined stressors on replicated low- and high-latitude populations in Europe. Unexpectedly, we observed positive sublethal effects of the heat wave: fat content and phenoloxidase activity increased. Chlorpyrifos had strong negative effects on survival, growth rate, and fat content, while phenoloxidase activity increased; these effects between latitudes were found similar. We found little indication of a higher ability to withstand a heat wave in southern larvae. We did detect a synergistic negative effect on AChE activity. This result highlights the importance of considering delayed effects of extreme temperature events when assessing the impact of pesticides under climate change.

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.

References (51)

  • P.D. Noyes et al.

    The toxicology of climate change: environmental contaminants in a warming world

    Environ. Int.

    (2009)
  • T.J. Reilly et al.

    Occurrence of boscalid and other selected fungicides in surface water and groundwater in three targeted use areas in the United States

    Chemosphere

    (2012)
  • H. Segner

    Moving beyond a descriptive aquatic toxicology: the value of biological process and trait information

    Aquat. Toxicol.

    (2011)
  • S.A. Adamo et al.

    Some like it hot: the effects of climate change on reproduction, immune function and disease resistance in the cricket Gryllus texensis

    J. Exp. Biol.

    (2011)
  • M.A. Beketov et al.

    Pesticides reduce regional biodiversity of stream invertebrates

    Proc. Natl. Acad. Sci. U.S.A.

    (2013)
  • S.K. Brewer et al.

    The effects of chlorpyrifos on cholinesterase activity and foraging behavior in the dragonfly, Anax junius (Odonata)

    Hydrobiologia

    (1999)
  • M. Campero et al.

    Sublethal pesticide concentrations and predation jointly shape life history: behavioral and physiological mechanisms

    Ecol. Appl.

    (2007)
  • M. Campero et al.

    Metamorphosis offsets the link between larval stress, adult asymmetry and individual quality

    Funct. Ecol.

    (2008)
  • M.J. Crawley

    Mixed-effects models

  • K.E. Day et al.

    Use of acetylcholinesterase activity to detect sublethal toxicity in stream invertebrates exposed to low concentrations of organophosphate insecticides

    Aquat. Toxicol.

    (1990)
  • M. De Block et al.

    Short-term larval food stress and associated compensatory growth reduce adult immune function in a damselfly

    Ecol. Entomol.

    (2008)
  • K.D.B. Dijkstra

    Field Guide to the Dragonflies of Britain and Europe

    (2006)
  • K. Dinh Van et al.

    Susceptibility to a metal under global warming is shaped by thermal adaptation along a latitudinal gradient

    Global Change Biol.

    (2013)
  • K. Dinh Van et al.

    Temperature and latitude-specific life history shape the vulnerability to a widespread pesticide in damselfly larvae

    J. Appl. Ecol.

    (2014)
  • C.L. Folt et al.

    Synergism and antagonism among multiple stressors

    Limnol. Oceanogr.

    (1999)
  • Cited by (31)

    • How will climatic warming affect insect pollinators?

      2023, Advances in Insect Physiology
    • Genetic variation of the interaction type between two stressors in a single population: From antagonism to synergism when combining a heat spike and a pesticide

      2022, Environmental Pollution
      Citation Excerpt :

      Additive and synergistic effects between a heat extreme (such as heat waves and heat spikes) and subsequent exposure to a pesticide have been observed before, but never for the same trait among genotypes of the same species. An additive effect between a heat wave and a pesticide (in current study found in one genotype for survival and in four genotypes for time to maturation), has been detected for survival and growth rate after sequential exposure to a heat wave and the organophophate chorpyrifos in the larvae of the damselfly Ischnura elegans (Arambourou and Stoks, 2015; Dinh Van et al., 2016). In the latter study, however, there was a synergistic interaction between the heat wave and chlorpyrifos for mortality, but only when combined with starvation (Dinh Van et al., 2016).

    • The complexity of global change and its effects on insects

      2021, Current Opinion in Insect Science
    View all citing articles on Scopus
    View full text