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Unexpected effects of low doses of a neonicotinoid insecticide on behavioral responses to sex pheromone in a pest insect.

Rabhi KK, Esancy K, Voisin A, Crespin L, Le Corre J, Tricoire-Leignel H, Anton S, Gadenne C - PLoS ONE (2014)

Bottom Line: 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.No clothianidin effect was observed on behavioral responses to plant odor.

View Article: PubMed Central - PubMed

Affiliation: INRA/Université d'Angers, Neuroéthologie-RCIM, UPRES-EA 2647 USC INRA 1330, SFR 4207 QUASAV, 42, rue Georges Morel, F-49071 Beaucouzé, France.

ABSTRACT
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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Effect of low doses of clothianidin on oriented responses of A. ipsilon males towards a 20-ng sex pheromone blend.The percentage of responses of clothianidin-treated males divided by that of DMSO-treated males is represented. The 0.25-ng dose induced a significant decrease in oriented responses whereas the 10-ng dose induced a significant increase in sex pheromone oriented responses. Bars with same letters are not significantly different (G-test, P<0.05). The dashed line represents an equal response of males treated with clothianidine and the corresponding DMSO dose. N>50 for all groups.
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pone-0114411-g002: Effect of low doses of clothianidin on oriented responses of A. ipsilon males towards a 20-ng sex pheromone blend.The percentage of responses of clothianidin-treated males divided by that of DMSO-treated males is represented. The 0.25-ng dose induced a significant decrease in oriented responses whereas the 10-ng dose induced a significant increase in sex pheromone oriented responses. Bars with same letters are not significantly different (G-test, P<0.05). The dashed line represents an equal response of males treated with clothianidine and the corresponding DMSO dose. N>50 for all groups.

Mentions: As there was no significant difference between the oriented responses of control males and males treated with DMSO (see above, File S1), we show the effect of clothianidin on the male oriented response as compared to the corresponding DMSO responses (i.e. the percentage of responses in clothianidin-treated males divided by the percentage of responses of males treated with the corresponding DMSO doses) (Fig. 2). Acute treatment with 2.5 ng, 1 ng, or 0.1 ng clothianidin (<LD0) did not affect the oriented behavioral response to 20 ng of the pheromone (2.5 ng: G = 0.17, df = 1, P = 0.67; 1 ng: G = 0.05, df = 1, P = 0.81; 0.1 ng: G = 0.51, df = 1, P = 0.47) (Fig. 2). However, significantly fewer males responded to the pheromone after treatment with 0.25 ng/moth as compared to DMSO-treated controls (G = 4.34, P = 0.04) (Fig. 2).


Unexpected effects of low doses of a neonicotinoid insecticide on behavioral responses to sex pheromone in a pest insect.

Rabhi KK, Esancy K, Voisin A, Crespin L, Le Corre J, Tricoire-Leignel H, Anton S, Gadenne C - PLoS ONE (2014)

Effect of low doses of clothianidin on oriented responses of A. ipsilon males towards a 20-ng sex pheromone blend.The percentage of responses of clothianidin-treated males divided by that of DMSO-treated males is represented. The 0.25-ng dose induced a significant decrease in oriented responses whereas the 10-ng dose induced a significant increase in sex pheromone oriented responses. Bars with same letters are not significantly different (G-test, P<0.05). The dashed line represents an equal response of males treated with clothianidine and the corresponding DMSO dose. N>50 for all groups.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4269385&req=5

pone-0114411-g002: Effect of low doses of clothianidin on oriented responses of A. ipsilon males towards a 20-ng sex pheromone blend.The percentage of responses of clothianidin-treated males divided by that of DMSO-treated males is represented. The 0.25-ng dose induced a significant decrease in oriented responses whereas the 10-ng dose induced a significant increase in sex pheromone oriented responses. Bars with same letters are not significantly different (G-test, P<0.05). The dashed line represents an equal response of males treated with clothianidine and the corresponding DMSO dose. N>50 for all groups.
Mentions: As there was no significant difference between the oriented responses of control males and males treated with DMSO (see above, File S1), we show the effect of clothianidin on the male oriented response as compared to the corresponding DMSO responses (i.e. the percentage of responses in clothianidin-treated males divided by the percentage of responses of males treated with the corresponding DMSO doses) (Fig. 2). Acute treatment with 2.5 ng, 1 ng, or 0.1 ng clothianidin (<LD0) did not affect the oriented behavioral response to 20 ng of the pheromone (2.5 ng: G = 0.17, df = 1, P = 0.67; 1 ng: G = 0.05, df = 1, P = 0.81; 0.1 ng: G = 0.51, df = 1, P = 0.47) (Fig. 2). However, significantly fewer males responded to the pheromone after treatment with 0.25 ng/moth as compared to DMSO-treated controls (G = 4.34, P = 0.04) (Fig. 2).

Bottom Line: 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.No clothianidin effect was observed on behavioral responses to plant odor.

View Article: PubMed Central - PubMed

Affiliation: INRA/Université d'Angers, Neuroéthologie-RCIM, UPRES-EA 2647 USC INRA 1330, SFR 4207 QUASAV, 42, rue Georges Morel, F-49071 Beaucouzé, France.

ABSTRACT
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.

Show MeSH
Related in: MedlinePlus