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      Unexpected Effects of Low Doses of a Neonicotinoid Insecticide on Behavioral Responses to Sex Pheromone in a Pest Insect


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          In moths, which include many agricultural pest species, males are attracted by female-emitted sex pheromones. Although integrated pest management strategies are increasingly developed, most insect pest treatments rely on widespread use of neurotoxic chemicals, including neonicotinoid insecticides. Residual accumulation of low concentrations of these insecticides in the environment is known to be harmful to beneficial insects such as honey bees. This environmental stress probably acts as an “info-disruptor” by modifying the chemical communication system, and therefore decreases chances of reproduction in target insects that largely rely on olfactory communication. However, low doses of pollutants could on the contrary induce adaptive processes in the olfactory pathway, thus enhancing reproduction. Here we tested the effects of acute oral treatments with different low doses of the neonicotinoid clothianidin on the behavioral responses to sex pheromone in the moth Agrotis ipsilon using wind tunnel experiments. We show that low doses of clothianidin induce a biphasic effect on pheromone-guided behavior. Surprisingly, we found a hormetic-like effect, improving orientation behavior at the LD20 dose corresponding to 10 ng clothianidin. On the contrary, a negative effect, disturbing orientation behavior, was elicited by a treatment with a dose below the LD0 dose corresponding to 0.25 ng clothianidin. No clothianidin effect was observed on behavioral responses to plant odor. Our results indicate that risk assessment has to include unexpected effects of residues on the life history traits of pest insects, which could then lead to their adaptation to environmental stress.

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          Diversity of vertebrate nicotinic acetylcholine receptors.

          Nicotinic acetylcholine receptors (nAChRs) are pentameric neurotransmitter receptors. They are members of the Cys-loop family of ligand-gated ion channels which also include ionotropic receptors for 5-hydroxytryptamine (5-HT), gamma-aminobutyric acid (GABA) and glycine. Nicotinic receptors are expressed in both the nervous system and at the neuromuscular junction and have been implicated in several neurological and neuromuscular disorders. In vertebrates, seventeen nAChR subunits have been identified (alpha1-alpha10, beta1-beta4, gamma, delta and epsilon) which can co-assemble to generate a diverse family of nAChR subtypes. This review will focus on vertebrate nAChRs and will provide an overview of the extent of nAChR diversity based on studies of both native and recombinant nAChRs.
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            Subchronic exposure of honeybees to sublethal doses of pesticides: effects on behavior.

            Laboratory bioassays were conducted to evaluate the effects on honeybee behavior of sublethal doses of insecticides chronically administered orally or by contact. Emergent honeybees received a daily dose of insecticide ranging from one-fifth to one-five-hundredth of the median lethal dose (LD50) during 11 d. After exposure to fipronil (0.1 and 0.01 ng/bee), acetamiprid (1 and 0.1 microg/bee), or thiamethoxam (1 and 0.1 ng/bee), behavioral functions of honeybees were tested on day 12. Fipronil, used at the dose of 0.1 ng/bee, induced mortality of all honeybees after one week of treatment. As a result of contact treatment at 0.01 ng/bee, honeybees spent significantly more time immobile in an open-field apparatus and ingested significantly more water. In the olfactory conditioning paradigm, fipronil-treated honeybees failed to discriminate between a known and an unknown odorant. Thiamethoxam by contact induced either a significant decrease of olfactory memory 24 h after learning at 0.1 ng/bee or a significant impairment of learning performance with no effect on memory at 1 ng/bee. Responsiveness to antennal sucrose stimulation was significantly decreased for high sucrose concentrations in honeybees treated orally with thiamethoxam (1 ng/bee). The only significant effect of acetamiprid (administered orally, 0.1 microg/bee) was an increase in responsiveness to water. The neonicotinoids acetamiprid and thiamethoxam tested at the highest dose (one-tenth and one-fifth of their oral LD50, respectively) and fipronil at one-five-hundredth of LD50 have limited effects on the motor, sensory, and cognitive functions of the honeybee. Our data on the intrinsic toxicity of the compounds after chronic exposure have to be taken into account for evaluation of risk to honeybees in field conditions.
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              Sublethal effects of neurotoxic insecticides on insect behavior.

              K. Haynes (1987)

                Author and article information

                Role: Editor
                PLoS One
                PLoS ONE
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                17 December 2014
                : 9
                : 12
                : e114411
                [1]INRA/Université d'Angers, Neuroéthologie-RCIM, UPRES-EA 2647 USC INRA 1330, SFR 4207 QUASAV, 42, rue Georges Morel, F-49071 Beaucouzé, France
                United States Department of Agriculture, Beltsville Agricultural Research Center, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: KKR HT-L SA CG. Performed the experiments: KKR KE AV LC JLC CG. Analyzed the data: KKR KE AV LC JLC CG. Contributed reagents/materials/analysis tools: KKR HT-L SA CG. Wrote the paper: KKR KE HT-L SA CG.

                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                : 9 September 2014
                : 10 November 2014
                Page count
                Pages: 15
                This work was supported by French National Funding Agency grant ANR-12 ADAP-0012-01 to H.T.-L., S.A., C.G. and a PhD grant to K.K.R., by the « Région Pays de la Loire » to S.A. and C.G. and by a Fulbright grant to K.E.
                Research Article
                Biology and Life Sciences
                Insect Pheromones
                Sex Pheromones
                Animal Behavior
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.



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