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Neonicotinoid insecticides alter induced defenses and increase susceptibility to spider mites in distantly related crop plants.

Szczepaniec A, Raupp MJ, Parker RD, Kerns D, Eubanks MD - PLoS ONE (2013)

Bottom Line: Little research, however, has focused on the direct effects of insecticides on plants.Our findings are important because applications of neonicotinoid insecticides have been associated with outbreaks of spider mites in several unrelated plant species.This study adds to growing evidence that bioactive agrochemicals can have unanticipated ecological effects and suggests that the direct effects of insecticides on plant defenses should be considered when the ecological costs of insecticides are evaluated.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, Texas A&M University, College Station, Texas, United States of America. adrianna.szczepaniec@sdstate.edu

ABSTRACT

Background: Chemical suppression of arthropod herbivores is the most common approach to plant protection. Insecticides, however, can cause unintended, adverse consequences for non-target organisms. Previous studies focused on the effects of pesticides on target and non-target pests, predatory arthropods, and concomitant ecological disruptions. Little research, however, has focused on the direct effects of insecticides on plants. Here we demonstrate that applications of neonicotinoid insecticides, one of the most important insecticide classes worldwide, suppress expression of important plant defense genes, alter levels of phytohormones involved in plant defense, and decrease plant resistance to unsusceptible herbivores, spider mites Tetranychus urticae (Acari: Tetranychidae), in multiple, distantly related crop plants.

Methodology/principal findings: Using cotton (Gossypium hirsutum), corn (Zea mays) and tomato (Solanum lycopersicum) plants, we show that transcription of phenylalanine ammonia lyase, coenzyme A ligase, trypsin protease inhibitor and chitinase are suppressed and concentrations of the phytohormone OPDA and salicylic acid were altered by neonicotinoid insecticides. Consequently, the population growth of spider mites increased from 30% to over 100% on neonicotinoid-treated plants in the greenhouse and by nearly 200% in the field experiment.

Conclusions/significance: Our findings are important because applications of neonicotinoid insecticides have been associated with outbreaks of spider mites in several unrelated plant species. More importantly, this is the first study to document insecticide-mediated disruption of plant defenses and link it to increased population growth of a non-target herbivore. This study adds to growing evidence that bioactive agrochemicals can have unanticipated ecological effects and suggests that the direct effects of insecticides on plant defenses should be considered when the ecological costs of insecticides are evaluated.

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Growth rate of spider mite populations on cotton, corn, and tomato plants.Growth rate of spider mite populations was measured on cotton (N = 8), corn (N = 10), and tomato plants (N = 5) treated with the neonicotinoid insecticides in a greenhouse. Population growth rate was calculated by estimating the weekly change in density of spider mites per cm2 of leaf area. Neonicotinoid applications resulted in significantly greater population growth rate of spider mites. Values are means±one standard error. Different letters indicate significant differences (P<0.05; ANOVA, simple effects in mixed model).
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pone-0062620-g005: Growth rate of spider mite populations on cotton, corn, and tomato plants.Growth rate of spider mite populations was measured on cotton (N = 8), corn (N = 10), and tomato plants (N = 5) treated with the neonicotinoid insecticides in a greenhouse. Population growth rate was calculated by estimating the weekly change in density of spider mites per cm2 of leaf area. Neonicotinoid applications resulted in significantly greater population growth rate of spider mites. Values are means±one standard error. Different letters indicate significant differences (P<0.05; ANOVA, simple effects in mixed model).

Mentions: Applications of thiamethoxam to cotton, clothianidin to corn, and imidacloprid to tomato all resulted in increased population growth rates of spider mites. There were nearly 30% more spider mites on thiamethoxam-treated cotton plants than untreated plants at the end of the experiment (F1,14 = 4.23, P = 0.053; Fig. 4A) and nearly 60% more mites on clothianidin treated corn plants (F1,18 = 11.91, P = 0.03; Fig. 4B). We found similar effects in tomato; spider mites were more than twice as abundant on tomato plants treated with imidacloprid than on control plants (F1,8 = 8.16, P = 0.021; Fig. 4C). Because the length of the experiments varied among the three plants (three weeks for cotton and corn and eight weeks for tomato), we calculated the weekly population growth rate of spider mites for our experiments. We found a significant interaction between neonicotinoid treatment and plant species on spider mite growth rate (F4,35.5 = 92.38, P<0.001; Fig. 5). Neonicotinoid applications resulted in significantly higher rates of population growth of spider mites in all three plants, but the strength of this effect varied: neonicotinoids elevated rates of increase by 27% in cotton, and by over 100% in corn and in tomato (Fig. 5).


Neonicotinoid insecticides alter induced defenses and increase susceptibility to spider mites in distantly related crop plants.

Szczepaniec A, Raupp MJ, Parker RD, Kerns D, Eubanks MD - PLoS ONE (2013)

Growth rate of spider mite populations on cotton, corn, and tomato plants.Growth rate of spider mite populations was measured on cotton (N = 8), corn (N = 10), and tomato plants (N = 5) treated with the neonicotinoid insecticides in a greenhouse. Population growth rate was calculated by estimating the weekly change in density of spider mites per cm2 of leaf area. Neonicotinoid applications resulted in significantly greater population growth rate of spider mites. Values are means±one standard error. Different letters indicate significant differences (P<0.05; ANOVA, simple effects in mixed model).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3643937&req=5

pone-0062620-g005: Growth rate of spider mite populations on cotton, corn, and tomato plants.Growth rate of spider mite populations was measured on cotton (N = 8), corn (N = 10), and tomato plants (N = 5) treated with the neonicotinoid insecticides in a greenhouse. Population growth rate was calculated by estimating the weekly change in density of spider mites per cm2 of leaf area. Neonicotinoid applications resulted in significantly greater population growth rate of spider mites. Values are means±one standard error. Different letters indicate significant differences (P<0.05; ANOVA, simple effects in mixed model).
Mentions: Applications of thiamethoxam to cotton, clothianidin to corn, and imidacloprid to tomato all resulted in increased population growth rates of spider mites. There were nearly 30% more spider mites on thiamethoxam-treated cotton plants than untreated plants at the end of the experiment (F1,14 = 4.23, P = 0.053; Fig. 4A) and nearly 60% more mites on clothianidin treated corn plants (F1,18 = 11.91, P = 0.03; Fig. 4B). We found similar effects in tomato; spider mites were more than twice as abundant on tomato plants treated with imidacloprid than on control plants (F1,8 = 8.16, P = 0.021; Fig. 4C). Because the length of the experiments varied among the three plants (three weeks for cotton and corn and eight weeks for tomato), we calculated the weekly population growth rate of spider mites for our experiments. We found a significant interaction between neonicotinoid treatment and plant species on spider mite growth rate (F4,35.5 = 92.38, P<0.001; Fig. 5). Neonicotinoid applications resulted in significantly higher rates of population growth of spider mites in all three plants, but the strength of this effect varied: neonicotinoids elevated rates of increase by 27% in cotton, and by over 100% in corn and in tomato (Fig. 5).

Bottom Line: Little research, however, has focused on the direct effects of insecticides on plants.Our findings are important because applications of neonicotinoid insecticides have been associated with outbreaks of spider mites in several unrelated plant species.This study adds to growing evidence that bioactive agrochemicals can have unanticipated ecological effects and suggests that the direct effects of insecticides on plant defenses should be considered when the ecological costs of insecticides are evaluated.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, Texas A&M University, College Station, Texas, United States of America. adrianna.szczepaniec@sdstate.edu

ABSTRACT

Background: Chemical suppression of arthropod herbivores is the most common approach to plant protection. Insecticides, however, can cause unintended, adverse consequences for non-target organisms. Previous studies focused on the effects of pesticides on target and non-target pests, predatory arthropods, and concomitant ecological disruptions. Little research, however, has focused on the direct effects of insecticides on plants. Here we demonstrate that applications of neonicotinoid insecticides, one of the most important insecticide classes worldwide, suppress expression of important plant defense genes, alter levels of phytohormones involved in plant defense, and decrease plant resistance to unsusceptible herbivores, spider mites Tetranychus urticae (Acari: Tetranychidae), in multiple, distantly related crop plants.

Methodology/principal findings: Using cotton (Gossypium hirsutum), corn (Zea mays) and tomato (Solanum lycopersicum) plants, we show that transcription of phenylalanine ammonia lyase, coenzyme A ligase, trypsin protease inhibitor and chitinase are suppressed and concentrations of the phytohormone OPDA and salicylic acid were altered by neonicotinoid insecticides. Consequently, the population growth of spider mites increased from 30% to over 100% on neonicotinoid-treated plants in the greenhouse and by nearly 200% in the field experiment.

Conclusions/significance: Our findings are important because applications of neonicotinoid insecticides have been associated with outbreaks of spider mites in several unrelated plant species. More importantly, this is the first study to document insecticide-mediated disruption of plant defenses and link it to increased population growth of a non-target herbivore. This study adds to growing evidence that bioactive agrochemicals can have unanticipated ecological effects and suggests that the direct effects of insecticides on plant defenses should be considered when the ecological costs of insecticides are evaluated.

Show MeSH
Related in: MedlinePlus