Effects of deltamethrin on the specific discrimination of sex pheromones in two sympatric Trichogramma species
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).
References (36)
- et al.
Estimated nationwide effects of pesticide spray drift on terrestrial habitats in the Netherlands
J. Environ. Manage.
(2008) - et al.
Sublethal effects of the insecticide chlorpyrifos on the sex pheromonal communication of Trichogramma brassicae
Chemosphere
(1998) - et al.
Partial compensation of the sublethal effect of delthamethrin on the sex pheromonal communication of Trichogramma brassicae
Chemosphere
(2001) - et al.
Modifications of the sex pheromonal communication of Trichogramma brassicae by a sublethal dose of deltamethrin
Chemosphere
(1999) - et al.
Dose-response relationship in lethal and behavioural effects of different insecticides on the parasitic wasp Aphidius ervi
Chemosphere
(2004) - et al.
Disruptive sublethal effects of insecticides on biological control: altered foraging ability and life span of a parasitoid after feeding on extrafloral nectar of cotton treated with systemic insecticides
Biol. Control
(2000) - Al Dabel, F., 2004. Etude des comportements et des molécules impliquées dans la rencontre des sexes chez les...
- et al.
Mating behavior and chemical communication in the order Hymenoptera
Ann. Rev. Entomol.
(2001) - et al.
Spermatogeny as a life-history index in parasitoid wasps
Oecologia
(2005) - et al.
Effects of pesticides on Colpoclypeus florus (Hymenoptera: Eulophidae) and Trichogramma platneri (Hymenoptera: Trichogrammatidae), parasitoids of leafrollers in Washington
J. Econ. Entomol.
(2001)
Insect olfaction from model systems to disease control
Proc. Nat. Acad. Sci. U.S.A.
Sex determination in the Hymenoptera: A review of models and evidence
Heredity
Index Phytosanitaire ACTA 2010
Increase of the behavioral response to kairomones by the parasitoid wasp Leptopilina heterotoma surviving insecticides
Arch. Environ. Contam. Toxicol.
Decrease in fecundity induced by interspecific mating between two Trichogramma parasitoid species
J. Econ. Entomol.
Inhibition of sex pheromone communications of Trichogramma brassicae (Hymenoptera) by the insecticide chlorpyrifos
Environ. Toxicol. Chem.
Modification of Trichogramma behaviors during the exploitation of host patches induced by the insecticide chlorpyrifos
EcoHealth
Reduction in the sex ratio of the progeny of a parasitoid wasp (Trichogramma brassicae) surviving the insecticide chlorpyrifos
Arch. Environ. Contam. Toxicol.
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