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Neonicotinoid insecticide imidacloprid causes outbreaks of spider mites on elm trees in urban landscapes.

Szczepaniec A, Creary SF, Laskowski KL, Nyrop JP, Raupp MJ - PLoS ONE (2011)

Bottom Line: Imidacloprid's systemic activity and mode of entry via roots or trunk injections reduce risk of environmental contamination and limit exposure of non-target organisms to pesticide residues.This is the first study to report the effects of pesticide applications on the arthropod communities in urban landscapes and demonstrate that imidacloprid increases spider mite fecundity through a plant-mediated mechanism.Widespread use of neonicotinoid insecticides, however, can disrupt ecosystems tipping the ecological balance in favor of herbivores and creating pest outbreaks.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, University of Maryland, College Park, Maryland, United States of America. ada.s@tamu.edu

ABSTRACT

Background: Attempts to eradicate alien arthropods often require pesticide applications. An effort to remove an alien beetle from Central Park in New York City, USA, resulted in widespread treatments of trees with the neonicotinoid insecticide imidacloprid. Imidacloprid's systemic activity and mode of entry via roots or trunk injections reduce risk of environmental contamination and limit exposure of non-target organisms to pesticide residues. However, unexpected outbreaks of a formerly innocuous herbivore, Tetranychus schoenei (Acari: Tetranychidae), followed imidacloprid applications to elms in Central Park. This undesirable outcome necessitated an assessment of imidacloprid's impact on communities of arthropods, its effects on predators, and enhancement of the performance of T. schoenei.

Methodology/principal findings: By sampling arthropods in elm canopies over three years in two locations, we document changes in the structure of communities following applications of imidacloprid. Differences in community structure were mostly attributable to increases in the abundance of T. schoenei on elms treated with imidacloprid. In laboratory experiments, predators of T. schoenei were poisoned through ingestion of prey exposed to imidacloprid. Imidacloprid's proclivity to elevate fecundity of T. schoenei also contributed to their elevated densities on treated elms.

Conclusions/significance: This is the first study to report the effects of pesticide applications on the arthropod communities in urban landscapes and demonstrate that imidacloprid increases spider mite fecundity through a plant-mediated mechanism. Laboratory experiments provide evidence that imidacloprid debilitates insect predators of spider mites suggesting that relaxation of top-down regulation combined with enhanced reproduction promoted a non-target herbivore to pest status. With global commerce accelerating the incidence of arthropod invasions, prophylactic applications of pesticides play a major role in eradication attempts. Widespread use of neonicotinoid insecticides, however, can disrupt ecosystems tipping the ecological balance in favor of herbivores and creating pest outbreaks.

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Effect of imidacloprid on elm leaf area in New York (A) and Maryland (B).Figure depicts area of leaves (√cm2) used in surveys of arthropod community presented in Figure 1. Elms (treated: N = 10; untreated: N = 10) in New York had a significantly greater leaf area following exposure to imidacloprid in all sampling years, while trees in Maryland (treated: N = 10; untreated: N = 10) were larger in the last year of the study. Means±s.e.m. marked with asterisks are significantly different at P<0.05.
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pone-0020018-g004: Effect of imidacloprid on elm leaf area in New York (A) and Maryland (B).Figure depicts area of leaves (√cm2) used in surveys of arthropod community presented in Figure 1. Elms (treated: N = 10; untreated: N = 10) in New York had a significantly greater leaf area following exposure to imidacloprid in all sampling years, while trees in Maryland (treated: N = 10; untreated: N = 10) were larger in the last year of the study. Means±s.e.m. marked with asterisks are significantly different at P<0.05.

Mentions: Imidacloprid clearly affected reproduction of T. schoenei thereby revealing another deleterious consequence of its use. In microcosms containing leaves, imidacloprid directly enhanced fecundity of T. schoenei. Adult T. schoenei fed foliage from elms treated with imidacloprid laid more eggs than T. schoenei that consumed leaves from untreated elms (F1,15 = 4.93, P = 0.042; Figure 3A). While fecundity was enhanced by almost 40%, longevity was not affected (F1,15 = 1.54, P = 0.23; Figure 3A). Conversely, a direct stimulatory effect of imidacloprid on T. schoenei fecundity was absent when mites were directly sprayed with the pesticide and then offered foliage from elms free of imidacloprid (F1,58 = 0.52, P = 0.49; Figure 3B). The longevity of T. schoenei was similarly unaffected by dermal exposure to imidacloprid (F1,58 = 1.45, P = 0.23; Figure 3B). Females sprayed directly with imidacloprid may have been exposed to lower doses of the pesticide than T. schoenei feeding on imidacloprid-treated foliage for extended period of time, thus explaining lack of effect of dermal sprays on T. schoenei fecundity and longevity. Stimulation of T. schoenei's reproductive performance, however, could also be mediated through a physiological response of elms to imidacloprid. Evidence for altered plant physiology was evident in comparisons of leaf areas of treated and untreated elms. Despite housing greater numbers of spider mites, imidacloprid-treated trees had significantly larger leaves in New York each year (2005, F1,89 = 17.89, P<0.001; 2006, F1,54 = 6.83, P = 0.009; 2007, F1,72 = 4.57, P = 0.033), and in 2007 in Maryland (F1,54 = 5.54, P = 0.02; Figure 4). The interaction between time and treatment did not have significant effects on leaf sizes (New York: 2005, F4,89 = 0.15, P = 0.963; 2006, F2,54 = 0.09, P = 0.915; 2007, F3,72 = 0.13, P = 0.944; Maryland: 2007, F2,54 = 1.2, P = 0.303). Contrary to an earlier report [14], we found that increased leaf size was not accompanied by increased nitrogen content (Table S7).


Neonicotinoid insecticide imidacloprid causes outbreaks of spider mites on elm trees in urban landscapes.

Szczepaniec A, Creary SF, Laskowski KL, Nyrop JP, Raupp MJ - PLoS ONE (2011)

Effect of imidacloprid on elm leaf area in New York (A) and Maryland (B).Figure depicts area of leaves (√cm2) used in surveys of arthropod community presented in Figure 1. Elms (treated: N = 10; untreated: N = 10) in New York had a significantly greater leaf area following exposure to imidacloprid in all sampling years, while trees in Maryland (treated: N = 10; untreated: N = 10) were larger in the last year of the study. Means±s.e.m. marked with asterisks are significantly different at P<0.05.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3104998&req=5

pone-0020018-g004: Effect of imidacloprid on elm leaf area in New York (A) and Maryland (B).Figure depicts area of leaves (√cm2) used in surveys of arthropod community presented in Figure 1. Elms (treated: N = 10; untreated: N = 10) in New York had a significantly greater leaf area following exposure to imidacloprid in all sampling years, while trees in Maryland (treated: N = 10; untreated: N = 10) were larger in the last year of the study. Means±s.e.m. marked with asterisks are significantly different at P<0.05.
Mentions: Imidacloprid clearly affected reproduction of T. schoenei thereby revealing another deleterious consequence of its use. In microcosms containing leaves, imidacloprid directly enhanced fecundity of T. schoenei. Adult T. schoenei fed foliage from elms treated with imidacloprid laid more eggs than T. schoenei that consumed leaves from untreated elms (F1,15 = 4.93, P = 0.042; Figure 3A). While fecundity was enhanced by almost 40%, longevity was not affected (F1,15 = 1.54, P = 0.23; Figure 3A). Conversely, a direct stimulatory effect of imidacloprid on T. schoenei fecundity was absent when mites were directly sprayed with the pesticide and then offered foliage from elms free of imidacloprid (F1,58 = 0.52, P = 0.49; Figure 3B). The longevity of T. schoenei was similarly unaffected by dermal exposure to imidacloprid (F1,58 = 1.45, P = 0.23; Figure 3B). Females sprayed directly with imidacloprid may have been exposed to lower doses of the pesticide than T. schoenei feeding on imidacloprid-treated foliage for extended period of time, thus explaining lack of effect of dermal sprays on T. schoenei fecundity and longevity. Stimulation of T. schoenei's reproductive performance, however, could also be mediated through a physiological response of elms to imidacloprid. Evidence for altered plant physiology was evident in comparisons of leaf areas of treated and untreated elms. Despite housing greater numbers of spider mites, imidacloprid-treated trees had significantly larger leaves in New York each year (2005, F1,89 = 17.89, P<0.001; 2006, F1,54 = 6.83, P = 0.009; 2007, F1,72 = 4.57, P = 0.033), and in 2007 in Maryland (F1,54 = 5.54, P = 0.02; Figure 4). The interaction between time and treatment did not have significant effects on leaf sizes (New York: 2005, F4,89 = 0.15, P = 0.963; 2006, F2,54 = 0.09, P = 0.915; 2007, F3,72 = 0.13, P = 0.944; Maryland: 2007, F2,54 = 1.2, P = 0.303). Contrary to an earlier report [14], we found that increased leaf size was not accompanied by increased nitrogen content (Table S7).

Bottom Line: Imidacloprid's systemic activity and mode of entry via roots or trunk injections reduce risk of environmental contamination and limit exposure of non-target organisms to pesticide residues.This is the first study to report the effects of pesticide applications on the arthropod communities in urban landscapes and demonstrate that imidacloprid increases spider mite fecundity through a plant-mediated mechanism.Widespread use of neonicotinoid insecticides, however, can disrupt ecosystems tipping the ecological balance in favor of herbivores and creating pest outbreaks.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, University of Maryland, College Park, Maryland, United States of America. ada.s@tamu.edu

ABSTRACT

Background: Attempts to eradicate alien arthropods often require pesticide applications. An effort to remove an alien beetle from Central Park in New York City, USA, resulted in widespread treatments of trees with the neonicotinoid insecticide imidacloprid. Imidacloprid's systemic activity and mode of entry via roots or trunk injections reduce risk of environmental contamination and limit exposure of non-target organisms to pesticide residues. However, unexpected outbreaks of a formerly innocuous herbivore, Tetranychus schoenei (Acari: Tetranychidae), followed imidacloprid applications to elms in Central Park. This undesirable outcome necessitated an assessment of imidacloprid's impact on communities of arthropods, its effects on predators, and enhancement of the performance of T. schoenei.

Methodology/principal findings: By sampling arthropods in elm canopies over three years in two locations, we document changes in the structure of communities following applications of imidacloprid. Differences in community structure were mostly attributable to increases in the abundance of T. schoenei on elms treated with imidacloprid. In laboratory experiments, predators of T. schoenei were poisoned through ingestion of prey exposed to imidacloprid. Imidacloprid's proclivity to elevate fecundity of T. schoenei also contributed to their elevated densities on treated elms.

Conclusions/significance: This is the first study to report the effects of pesticide applications on the arthropod communities in urban landscapes and demonstrate that imidacloprid increases spider mite fecundity through a plant-mediated mechanism. Laboratory experiments provide evidence that imidacloprid debilitates insect predators of spider mites suggesting that relaxation of top-down regulation combined with enhanced reproduction promoted a non-target herbivore to pest status. With global commerce accelerating the incidence of arthropod invasions, prophylactic applications of pesticides play a major role in eradication attempts. Widespread use of neonicotinoid insecticides, however, can disrupt ecosystems tipping the ecological balance in favor of herbivores and creating pest outbreaks.

Show MeSH
Related in: MedlinePlus