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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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Abundance of spider mites in a cotton field exposed to treatments of thiamethoxam.The total abundance of spider mites summed over the entire sampling period was significantly affected by the treatments (A). Spider mites were more abundant in plots (N = 8) assigned to Foliar and Seed+Foliar treatments compared to untreated plots (Kruskal-Wallis multiple comparison test, P<0.05). Similarly, over the course of the experiment, spider mites increased in numbers in field plots treated with thiamethoxam delivered as foliar sprays (Foliar) and combination of seed treatments and foliar sprays (Seed+Foliar) (B). Seed treatments (Seed) alone did not affect populations of T. cinnabarinus, whereas abundance of spider mites in plots that received foliar applications of thiamethoxam or combination of seed and foliar treatments was significantly increased in late May and June compared to untreated plots (Tukey’s test, P<0.05). Values are means of spider mite numbers per cm2 of leaf area±one standard error, letters (A) and asterisks (B) mark significantly different means.
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pone-0062620-g006: Abundance of spider mites in a cotton field exposed to treatments of thiamethoxam.The total abundance of spider mites summed over the entire sampling period was significantly affected by the treatments (A). Spider mites were more abundant in plots (N = 8) assigned to Foliar and Seed+Foliar treatments compared to untreated plots (Kruskal-Wallis multiple comparison test, P<0.05). Similarly, over the course of the experiment, spider mites increased in numbers in field plots treated with thiamethoxam delivered as foliar sprays (Foliar) and combination of seed treatments and foliar sprays (Seed+Foliar) (B). Seed treatments (Seed) alone did not affect populations of T. cinnabarinus, whereas abundance of spider mites in plots that received foliar applications of thiamethoxam or combination of seed and foliar treatments was significantly increased in late May and June compared to untreated plots (Tukey’s test, P<0.05). Values are means of spider mite numbers per cm2 of leaf area±one standard error, letters (A) and asterisks (B) mark significantly different means.

Mentions: The average number of spider mites (T. cinnabarinus) was significantly greater in thiamethoxam-treated cotton plots than in untreated plots in our field experiment (Kruskal-Wallis test: Χ2 = 23.05, df = 3, P<0.001; Fig. 6A). Over the eight-week sampling period, spider mites were, on average, twice as abundant on cotton plants treated with thiamethoxam (Friedman test: Χ2 = 11.94, df = 3; P = 0.008; Fig. 6B). Foliar sprays and a combination of foliar and seed treatments significantly increased spider mite abundance on two out of the five sampling dates (Fig. 6B). Because seed treatments alone had no effect on the abundance of spider mites, the increase in spider mites was likely driven by foliar applications of thiamethoxam. Moreover, the insecticide applications had no effect on the abundance of predators of spider mites (Χ2 = 1.32, df = 3; P = 0.724); the average number of predators per cm2 of leaf area was comparable among treatments (Untreated: 0.06±0.01 s.e.m.; Seed: 0.05±0.02 s.e.m.; Foliar: 0.04±0.01 s.em.; Seed+Foliar: 0.04±0.01 s.e.m.). Predators that were collected from field plots included lacewings (Chrysopidae), predaceous bugs (Anthocoridae), and predatory mites (Phytoseiidae).


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)

Abundance of spider mites in a cotton field exposed to treatments of thiamethoxam.The total abundance of spider mites summed over the entire sampling period was significantly affected by the treatments (A). Spider mites were more abundant in plots (N = 8) assigned to Foliar and Seed+Foliar treatments compared to untreated plots (Kruskal-Wallis multiple comparison test, P<0.05). Similarly, over the course of the experiment, spider mites increased in numbers in field plots treated with thiamethoxam delivered as foliar sprays (Foliar) and combination of seed treatments and foliar sprays (Seed+Foliar) (B). Seed treatments (Seed) alone did not affect populations of T. cinnabarinus, whereas abundance of spider mites in plots that received foliar applications of thiamethoxam or combination of seed and foliar treatments was significantly increased in late May and June compared to untreated plots (Tukey’s test, P<0.05). Values are means of spider mite numbers per cm2 of leaf area±one standard error, letters (A) and asterisks (B) mark significantly different means.
© Copyright Policy
Related In: Results  -  Collection

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pone-0062620-g006: Abundance of spider mites in a cotton field exposed to treatments of thiamethoxam.The total abundance of spider mites summed over the entire sampling period was significantly affected by the treatments (A). Spider mites were more abundant in plots (N = 8) assigned to Foliar and Seed+Foliar treatments compared to untreated plots (Kruskal-Wallis multiple comparison test, P<0.05). Similarly, over the course of the experiment, spider mites increased in numbers in field plots treated with thiamethoxam delivered as foliar sprays (Foliar) and combination of seed treatments and foliar sprays (Seed+Foliar) (B). Seed treatments (Seed) alone did not affect populations of T. cinnabarinus, whereas abundance of spider mites in plots that received foliar applications of thiamethoxam or combination of seed and foliar treatments was significantly increased in late May and June compared to untreated plots (Tukey’s test, P<0.05). Values are means of spider mite numbers per cm2 of leaf area±one standard error, letters (A) and asterisks (B) mark significantly different means.
Mentions: The average number of spider mites (T. cinnabarinus) was significantly greater in thiamethoxam-treated cotton plots than in untreated plots in our field experiment (Kruskal-Wallis test: Χ2 = 23.05, df = 3, P<0.001; Fig. 6A). Over the eight-week sampling period, spider mites were, on average, twice as abundant on cotton plants treated with thiamethoxam (Friedman test: Χ2 = 11.94, df = 3; P = 0.008; Fig. 6B). Foliar sprays and a combination of foliar and seed treatments significantly increased spider mite abundance on two out of the five sampling dates (Fig. 6B). Because seed treatments alone had no effect on the abundance of spider mites, the increase in spider mites was likely driven by foliar applications of thiamethoxam. Moreover, the insecticide applications had no effect on the abundance of predators of spider mites (Χ2 = 1.32, df = 3; P = 0.724); the average number of predators per cm2 of leaf area was comparable among treatments (Untreated: 0.06±0.01 s.e.m.; Seed: 0.05±0.02 s.e.m.; Foliar: 0.04±0.01 s.em.; Seed+Foliar: 0.04±0.01 s.e.m.). Predators that were collected from field plots included lacewings (Chrysopidae), predaceous bugs (Anthocoridae), and predatory mites (Phytoseiidae).

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