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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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Feeding rate and mobility of S. punctillum and C. rufilabris exposed to imidacloprid through prey.A) Feeding rates (√(mites eaten)/h) of S. punctillum and C. rufilabris were reduced after 3.5 h when mites were reared on foliage from imidacloprid-treated (N = 7) compared to untreated elms (N = 7). (B) Mobility (√mm/s) of S. punctillum and C. rufilabris was significantly reduced after 3.5 h of exposure to spider mites reared on foliage from imidacloprid-treated elms compared to untreated elms. Means±s.e.m. marked with asterisks are significantly different at P<0.05.
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pone-0020018-g002: Feeding rate and mobility of S. punctillum and C. rufilabris exposed to imidacloprid through prey.A) Feeding rates (√(mites eaten)/h) of S. punctillum and C. rufilabris were reduced after 3.5 h when mites were reared on foliage from imidacloprid-treated (N = 7) compared to untreated elms (N = 7). (B) Mobility (√mm/s) of S. punctillum and C. rufilabris was significantly reduced after 3.5 h of exposure to spider mites reared on foliage from imidacloprid-treated elms compared to untreated elms. Means±s.e.m. marked with asterisks are significantly different at P<0.05.

Mentions: Two important taxa of spider mite predators, Coccinellidae in the genus Stethorus and Chrysopidae were collected at both locations in most years of the study. Several previous studies indicate that lady beetles in the genus Stethorus are highly specialized predators of spider mites and are known to exhibit positive density dependence with increasing prey populations [44]–[46]. Green lacewing larvae, Chrysopidae, are also important generalist predators of spider mites [44], [45]. It was not surprising that Stethorus and Chrysopidae were rare on untreated trees in New York and Maryland, where populations of spider mites remained relatively low in all years of the study (Figures 1 and S1). However, the lack of numerical response by either predator to eruptive mite populations at both sites in all years was perplexing and unexpected. This observation and the fact that others have documented debilitating effects of imidacloprid on predatory insects [35], [36], [41], [42] led us to examine the effects of imidacloprid on the behaviour and longevity of two model predators of spider mites, Stethorus punctillum and Chrysoperla rufilabris. We found that feeding rates of adult S. punctillum and larval C. rufilabris were significantly reduced when T. schoenei from elms treated with imidacloprid were offered as prey for 3.5 h (S. punctillum, F1,12 = 56.62, P<0.001; C. rufilabris, F1,12 = 44.09, P<0.001; Figure 2A). While there were significant time by treatment interactions for both predators (S. punctillum, F3,36 = 34.63, P<0.01; C. rufilabris, F3,36 = 17.79, P<0.01), feeding rates differed significantly between treatments after only 1.5 h and differences grew larger as the experiment progressed (Table S5).


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)

Feeding rate and mobility of S. punctillum and C. rufilabris exposed to imidacloprid through prey.A) Feeding rates (√(mites eaten)/h) of S. punctillum and C. rufilabris were reduced after 3.5 h when mites were reared on foliage from imidacloprid-treated (N = 7) compared to untreated elms (N = 7). (B) Mobility (√mm/s) of S. punctillum and C. rufilabris was significantly reduced after 3.5 h of exposure to spider mites reared on foliage from imidacloprid-treated elms compared to untreated elms. 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-g002: Feeding rate and mobility of S. punctillum and C. rufilabris exposed to imidacloprid through prey.A) Feeding rates (√(mites eaten)/h) of S. punctillum and C. rufilabris were reduced after 3.5 h when mites were reared on foliage from imidacloprid-treated (N = 7) compared to untreated elms (N = 7). (B) Mobility (√mm/s) of S. punctillum and C. rufilabris was significantly reduced after 3.5 h of exposure to spider mites reared on foliage from imidacloprid-treated elms compared to untreated elms. Means±s.e.m. marked with asterisks are significantly different at P<0.05.
Mentions: Two important taxa of spider mite predators, Coccinellidae in the genus Stethorus and Chrysopidae were collected at both locations in most years of the study. Several previous studies indicate that lady beetles in the genus Stethorus are highly specialized predators of spider mites and are known to exhibit positive density dependence with increasing prey populations [44]–[46]. Green lacewing larvae, Chrysopidae, are also important generalist predators of spider mites [44], [45]. It was not surprising that Stethorus and Chrysopidae were rare on untreated trees in New York and Maryland, where populations of spider mites remained relatively low in all years of the study (Figures 1 and S1). However, the lack of numerical response by either predator to eruptive mite populations at both sites in all years was perplexing and unexpected. This observation and the fact that others have documented debilitating effects of imidacloprid on predatory insects [35], [36], [41], [42] led us to examine the effects of imidacloprid on the behaviour and longevity of two model predators of spider mites, Stethorus punctillum and Chrysoperla rufilabris. We found that feeding rates of adult S. punctillum and larval C. rufilabris were significantly reduced when T. schoenei from elms treated with imidacloprid were offered as prey for 3.5 h (S. punctillum, F1,12 = 56.62, P<0.001; C. rufilabris, F1,12 = 44.09, P<0.001; Figure 2A). While there were significant time by treatment interactions for both predators (S. punctillum, F3,36 = 34.63, P<0.01; C. rufilabris, F3,36 = 17.79, P<0.01), feeding rates differed significantly between treatments after only 1.5 h and differences grew larger as the experiment progressed (Table S5).

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