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Non-target effects on aquatic decomposer organisms of imidacloprid as a systemic insecticide to control emerald ash borer in riparian trees

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Abstract

Imidacloprid is effective against emerald ash borer when applied as a systemic insecticide. Following stem or soil injections to trees in riparian areas, imidacloprid residues could be indirectly introduced to aquatic systems via leaf fall or leaching. Either route of exposure may affect non-target, aquatic decomposer organisms. Leaves from ash trees treated with imidacloprid at two field rates and an intentionally-high concentration were added to aquatic microcosms. Leaves from trees treated at the two field rates contained imidacloprid concentrations of 0.8–1.3 ppm, and did not significantly affect leaf-shredding insect survival, microbial respiration or microbial decomposition rates. Insect feeding rates were significantly inhibited at foliar concentrations of 1.3 ppm but not at 0.8 ppm. Leaves from intentionally high-dose trees contained concentrations of about 80 ppm, and resulted in 89–91% mortality of leaf-shredding insects, but no adverse effects on microbial respiration and decomposition rates. Imidacloprid applied directly to aquatic microcosms to simulate leaching from soils was at least 10 times more toxic to aquatic insects than the foliar concentrations, with high mortality at 0.13 ppm and significant feeding inhibition at 0.012 ppm.

Introduction

The emerald ash borer (EAB) (Agrilus planipennis) is an invasive, exotic insect pest that has recently been responsible for widespread mortality of ash trees (Fraxinus spp.) in northeastern North American. The EAB has the potential to cause economic and ecological impacts on a scale similar to those of previous invasive pests on American chestnut (Castanea dentata) and white elm (Ulmus americana) (Liebhold et al., 1995; Cappaert et al., 2005; Poland and McCullough, 2006). Wood-boring insect pests like the EAB provide unique challenges to forest pest managers because the most damaging life stages of the insects are the phloem-feeding larvae which are difficult to target by conventional foliar applications of insecticides. In addition, conventional insect control methods are often not considered appropriate or publicly acceptable in many urban or recreational environments.

In response to the need for effective and safe pest control strategies to address these types of pest problems, there have been concerted efforts in developing and testing pesticides with reduced risk to human or environmental health (Thompson and Kreutzweiser, 2007). One alternative strategy to reduce environmental exposure and provide effective control of problematic insect pests such as wood-boring insects is the application of selective, systemic insecticides to trees through stem- or soil-injections (e.g., Helson et al., 2001, Wanner et al., 2002). Systemic insecticides are not applicable to all forest pest management situations but they may be well suited for exotic species within a restricted area before the species becomes widely distributed. They may also be well suited to smaller-scale situations in which an infestation occurs or threatens an environmentally sensitive area where broad-scale pesticide applications or tree-removal approaches are not acceptable. This would include, for example, riparian forests of municipal watersheds or agricultural irrigation streams, shoreline areas of “cottage country”, public parks and other high-profile recreational areas, high-value stands, and conservation areas.

Imidacloprid (1-(6-chloro-3-pyridinylmethyl)-N-nitroimidaolidin-2-ylideneamine) is a systemic, chloro-neonicotinyl insecticide, that specifically blocks the nicotinergic neuronal pathway. This pathway is more abundant in insects than in warm-blooded animals accounting for its selective toxicity. The properties, efficacy, toxicology, and environmental profile of imidacloprid have been previously reviewed (Elbert et al., 1991; Felsot, 2001; Sheets, 2001). While imidacloprid is most widely used as an agricultural or horticultural insecticide, it has recently been demonstrated to be highly effective as a systemic insecticide or prophylactic treatment against EAB in ash trees of northern Michigan, USA (McCullough et al., 2003) and southern Ontario, Canada (Helson and Thompson, unpublished data). Stem injections of imidacloprid have also been used successfully to affect control over wood-boring Asian longhorned beetle (Anoplophora glabripennis) infestations near Chicago, IL, USA (Poland et al., 2006), and recent studies have indicated that it is effective against the brown spruce longhorned beetle (Tetropium fuscum) in eastern Canada as well (Thompson et al., unpublished data). In exploiting its systemic properties, imidacloprid may be applied by direct stem injection into tree trunks, or by soil drench or soil injections around the drip-lines of tree canopies.

When applied as stem injections to riparian trees, foliar residues of imidacloprid can enter water bodies when trees lose their leaves in autumn. When applied to soils, imidacloprid concentrations can leach to nearby water bodies. Field studies on the leaching potential of imidacloprid provide variable results with some studies reporting little or no movement below 30 cm depth (Rouchaud et al., 1996; Kalpana et al., 2002) while others indicate significant mobility in soil column (Gupta et al., 2002; Vollner and Klotz, 1997) and field (Felsot et al., 1998) studies. Imidacloprid is most susceptible to leaching in soils with low organic content, coarse texture, high rock or gravel component, and in those which are saturated or near-saturated or with significant macropore content (Felsot et al., 1998). The Canadian Pest Management Regulatory Agency considers imidacloprid to have high potential for surface water contamination, leaching to groundwater and persistence in soils (PMRA, 2001).

Imidacloprid concentrations in leaves from treated trees or from soil applications leaching to receiving waters may pose a risk of harm to non-target, aquatic decomposer organisms. The objective of our study was to determine if leaves that fall from riparian ash trees treated with imidacloprid to control EAB pose a risk of harm to natural decomposer organisms and processes in nearby waterbodies. We then compared that to the risk of harm posed by direct exposure to imidacloprid concentrations in water that might arise from ground applications and leaching to nearby aquatic systems.

Section snippets

Experimental treatments and design

The fate and effects of imidacloprid were determined in aquatic microcosms in two separate experiments. In the first experiment, leaves from imidacloprid-treated ash trees were added to replicate microcosms to mimic an autumn leaf-fall scenario in which leaves from treated riparian trees would fall into nearby waterbodies. The second experiment was conducted immediately after and included untreated leaves as well as the direct application of imidacloprid to the microcosms to mimic a leaching

Water quality

Over the coarse of the first experiment, water temperatures ranged from 18.7 to 19.3 °C, with average daily temperatures of 18.9 to 19.1 °C. DO concentrations remained at or near saturation, ranging from 8.85 to 9.42 mg/L. Conductivity gradually increased over the 14-day period ranging from 53 to 80 μS/cm, and pH ranged from 6.2 to 6.8. During the second experiment, water temperatures ranged from 18.9 to 20.4 °C, with average daily temperatures of 19.1 to 20.0 °C. DO ranged from 8.52 to 10.56 mg/L, pH

Water quality

Water quality parameters (DO, pH, conductivity) for both experiments were maintained at conditions similar to those of regional forest water bodies (Kreutzweiser et al., unpublished data), and would not have caused the observed insect mortality or sublethal effects. There were no concentration-dependent patterns among water quality parameters measured, indicating no treatment effects on these water quality parameters. Conductivity tended to increase over time in all microcosms and may have been

Conclusion

The results from these microcosm experiments indicate that imidacloprid concentrations in ash leaves that fall into water bodies from trees treated at typical field rates to control EAB will pose little risk of harm to aquatic leaf-shredding insects or to aquatic microbial communities. At the upper end of the range of typical field concentrations in leaves, there may be feeding-inhibition effects on leaf-shredding insects but the ecological implications of this will depend on the mode of action

Acknowledgments

We are grateful to Scott Capell, Kara Herridge, Elisa Sturgeon, and Korrie Young for technical assistance. Blair Helson treated the potted ash trees with imidacloprid.

Funding sources: The project was funded in part by the Enhanced Pest Management Methods S&T Program of Natural Resources Canada.

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