Effects of deltamethrin on the specific discrimination of sex pheromones in two sympatric Trichogramma species

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Abstract

The large amounts of insecticides used for crop protection lead to widespread environmental pollution. Determination of the potential impacts induced by this contamination on key species involved in the equilibrium of ecosystems is therefore a necessity. In this study, we tested the effects of a pyrethroid insecticide, deltamethrin, on the capacity of males from two sympatric Trichogramma species to discriminate the sex pheromones emitted by females of their own species (Trichogramma are parasitoids of Lepidopterous). The impact of an acute exposure as could occur at field edges was evaluated using a dose inducing 20% mortality (LD 20). The impact of a low exposure corresponding to diffuse environmental pollution was evaluated by applying an LD 0.1 (a dose inducing no apparent mortality).

For T. semblidis, deltamethrin decreased the specific recognition of sexual pheromones at the higher dose (LD 20) but had no effect on this recognition at the lower dose (LD 0.1). However, deltamethrin decreased the saturation of pheromone receptors at both doses. For T. evanescens, deltamethrin increased the recognition of sexual pheromones at both doses, though not during the same period of observation (at the beginning for the LD 20, at the end for the LD 0.1), but it did not decrease the saturation of the pheromone receptors. These differing results were analyzed considering the behavior of the insects, their level of sensitivity to the insecticide and its mode of action. They provide new insights regarding possible consequences of environmental pollution by insecticides on functional biodiversity.

Highlights

Trichogramma species are parasitoids of numerous Lepidopterous species. ► Deltamethrin impacted the specific recognition of female sexual pheromones by males. ► In T. semblidis, it decreased recognition at an LD 20 but had no effect at an LD 0.1. ► In T. evanescens, deltamethrin increased recognition at an LD 20 and LD 0.1. ► It decreased the saturation of receptors for T. semblidis, but not for T. evanescens

Introduction

When a crop is sprayed with pesticides, studies have shown that 9.5% of the sprayed pesticides enter the atmosphere through drift or volatilization and can therefore be found in all environmental compartments outside treated areas (De Jong et al., 2008). Although this contamination is more pronounced in areas of intensive use of pesticides, such as agricultural crop areas and their peripheries, it can also affect areas much farther away. These more distant areas, which are believed to be uncontaminated because they are not treated, can harbor natural populations with an essential reservoir function that will therefore be exposed to low doses of pesticides (De Jong et al., 2008).

Conventional toxicological screening and testing methods are useful for detecting overt toxic effects of chemicals, but are generally poor with respect to exploring more subtle effects, such as changes in behavioral responses. However, neurotoxic insecticides, by disrupting the transmission of nerve impulses in the nervous system, can lead to the death of insects, but they can also cause many other effects without necessarily being lethal (see Desneux et al., 2007 for a review). These effects will affect the behaviors of insects because of their dependence on their nervous system for perception of stimuli, transmission of this perception to the central nervous system, elaboration of a response to the perceived stimulus, and finally, execution of the behavior chosen according to the perceived stimulus (Vosshall and Stocker, 2007). Therefore, beyond the mortality induced by insecticides, these insecticides may impact wildlife health and the equilibrium of ecosystems through an action at sublethal level (Desneux et al., 2007). Pyrethroids are the second most widely used family of insecticides (organophorus being the first, [EC] European Commission, 2007, [U.S. EPA] U.S. Environmental Protection Agency, 2011). Deltamethrin (Pyr.), the insecticide tested in this study, is used on many crops (e.g., cereal, corn, crucifer, artichoke, asparagus, beet, salad, tomato, pepper, potato, apple, pear, peach, grape, rice, peas, and onion, cf. Couteux and Lejeune, 2009). It is a neurotoxic insecticide that interferes with the transmission of action potentials along neurons (Soderlund, 2012).

In the wild, insects come into contact with a great variety of olfactory signals. It is of vital importance for them to be able to distinguish among all of these signals and to differentiate those associated with their life history traits (Ha and Smith, 2009). Specific discrimination of sex pheromones is one of these vital traits because it is an important step in reproduction (Ayasse et al., 2001). Trichogramma are oophagous parasitoids. They are key species because they control populations of other insects, including numerous pest species, and they play an important role in the equilibrium of ecosystems. Furthermore, they are beneficial insects and are regularly used for biological control. Trichogramma attack over 400 pest species, most of which are Lepidopterous (Li, 1994).

Obtaining a better understanding of the impact of pesticides on beneficial insects, such as parasitoids, is a necessity. This impact must be assessed against a background of acute exposure of beneficial insects that can occur in open fields or field edges, such as during treatment of crops, and that will correspond to exposure to high doses. This impact must also be assessed in the context of the diffuse environmental pollution that can reach ecosystems very distant from treated areas and will, therefore, correspond to exposure to much lower doses that do not necessarily cause any apparent mortality.

In this study, we tested the sublethal effects of deltamethrin on the capacity of males from two sympatric species, Trichogramma semblidis and T. evanescens, to discriminate between sex pheromones emitted by females from these species. Males were tested following exposure to two different doses of insecticide, one of which was relatively high and induced 20% mortality (LD 20) and rather corresponded to possible exposure in the vicinity of treated areas, while the other dose induced no apparent mortality (LD 0.1) and corresponded to diffuse environmental pollution reaching ecosystems distant from treated areas.

Section snippets

Chemicals, equipments and biological material

The insecticide deltamethrin (99% certified purity) was purchased from Cluzeau Info Labo (Sainte-Foy-La-Grande, France). The acetone (99% purity) was purchased from Merck Eurolab (Briare Le Canal, France). The camera (Canon N 50 camera with a 25 mm lens), the video card and the software Cible_p5 were purchased from Secad (Saint Martin du Fresne, France). The detergent Micro-90 was purchased from Bioblock Scientific (Illkirch, France). The Ephestia kuehniella eggs killed by UV radiation were

Lethal doses

The theoretical doses that induce 20 and 0.1% mortality (LD 20 and LD 0.1, respectively) and their 95% confidence intervals are given in Table 1. These doses were used for testing the sublethal effects of deltamethrin on the responses of males to the female sexual pheromones of the two sympatric species.

Specificity of the recognition of sexual pheromones

For both T. semblidis and T. evanescens, the percentage of time spent by males in the area marked by conspecific pheromones was significantly greater than 50% under control conditions (means of

Discussion

The insecticide deltamethrin induced an alteration of the recognition by Trichogramma males of the sexual pheromones of their conspecific females. The effects were different according to the species and dose tested. For T. semblidis, an LD 20 of deltamethrin induced a decrease in the preference of the parasitoid for the sexual pheromones of a conspecific female during a choice situation, whereas an LD 0.1 had no significant effect on this preference. However, both doses induced a decrease in

Acknowledgements

We are thankful to S. Janillon-Martinez and H. Henri for technical assistance and to D. Charif for advices on statistical analyses. We are grateful to B. Pintureau and P. Bolland for determining and providing the two Trichogramma species used in this work. This work was supported by the research program 'Pesticides' (no. PE00/122000/024) of the French Ministry of Environment (Ministère de l'Ecologie, du Développement Durable, du Transport et du Logement).

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