Comparative toxicities of organophosphate and pyrethroid insecticides to aquatic macroarthropods

Highlights

• We exposed crayfish and water bugs to pyrethroid and organophosphate insecticides.

• Insecticide class was a significant predictor of risk of mortality during the study.

• Pyrethroid insecticides were consistently more toxic than organophosphates.

• Malathion was the only insecticide identified as posing low risk to macroarthropods.

• Identifying low-risk insecticides is critical to minimize adverse ecosystem effects.

Abstract

As agricultural expansion and intensification increase to meet the growing global food demand, so too will insecticide use and thus the risk of non-target effects. Insecticide pollution poses a particular threat to aquatic macroarthropods, which play important functional roles in freshwater ecosystems. Thus, understanding the relative toxicities of insecticides to non-target functional groups is critical for predicting effects on ecosystem functions. We exposed two common macroarthropod predators, the crayfish Procambarus alleni and the water bug Belostoma flumineum, to three insecticides in each of two insecticide classes (three organophosphates: chlorpyrifos, malathion, and terbufos; and three pyrethroids: esfenvalerate, λ-cyhalothrin, and permethrin) to assess their toxicities. We generated 150 simulated environmental exposures using the US EPA Surface Water Contamination Calculator to determine the proportion of estimated peak environmental concentrations (EECs) that exceeded the US EPA level of concern (0.5 × LC₅₀) for non-endangered aquatic invertebrates. Organophosphate insecticides generated consistently low-risk exposure scenarios (EECs < 0.5 × LC₅₀) for both P. alleni and B. flumineum. Pyrethroid exposure scenarios presented consistently high risk (EECs > 0.5 × LC₅₀) to P. alleni, but not to B. flumineum, where only λ-cyhalothrin produced consistently high-risk exposures. Survival analyses demonstrated that insecticide class accounted for 55.7% and 91.1% of explained variance in P. alleni and B. flumineum survival, respectively. Thus, risk to non-target organisms is well predicted by pesticide class. Identifying insecticides that pose low risk to aquatic macroarthropods might help meet increased demands for food while mitigating against potential negative effects on ecosystem functions.

Introduction

Global sales of insecticides have increased over the past several decades (Grube et al., 2011). Insecticide use is positively correlated with cropland (Meehan et al., 2011) and is almost certain to increase with the agricultural expansion necessary to feed the increasing global human population (Tilman et al., 2011, Tilman et al., 2001). Pyrethroid use in particular has increased worldwide, especially to control vector-borne diseases (van den Berg et al., 2012). Additionally, the organophosphate insecticides chlorpyrifos and malathion remain among the most-frequently detected insecticides in surface waters of the United States (Gilliom, 2007), even as agricultural use of organophosphates in the United States has stagnated (Grube et al., 2011, Thelin and Stone, 2013).

Agrochemical pollution from insecticide run-off can have important negative consequences for non-target taxa (Brock et al., 2000, McMahon et al., 2012, Rohr et al., 2013, Rohr et al., 2008b). Insecticides can adversely impact aquatic macroarthropods (Brock et al., 2000, Van Wijngaarden et al., 2006), which play many important functional roles in wetland ecosystems (Wallace and Webster, 1996), including as predators of aquatic herbivores (Kesler and Munns, 1989, Weber and Lodge, 1990) and as prey for vertebrate predators (Jordan et al., 1996). Because they occupy intermediate trophic levels, macroinvertebrates can mediate the effects of both top-down and bottom-up pressures on ecosystems (Wallace and Webster, 1996). Thus, changes in the abundances of macroarthropod predators can indirectly affect aquatic community composition and ecosystem properties (Halstead et al., 2014, Rohr and Crumrine, 2005).

As new pesticides are developed and approved for use, it is important that risk assessors can predict the risk these chemicals pose to non-target wildlife. Pesticides may vary both in their toxicity to organisms and in their estimated environmental exposures, the latter of which is based on recommended application rates and the physicochemical properties of the pesticide. Insecticides with similar modes of action often have similar safe threshold values in terms of toxic units (concentrations of different pesticides that are standardized by dividing by the geometric mean of reported EC₅₀ values of the most sensitive standard test species (typically Daphnia magna); Brock et al., 2000). Therefore, pesticides of the same class (i.e., organophosphate vs. pyrethroid insecticides) might be expected to pose similar risk to focal species even though individual pesticides within a class might vary in their relative estimated environmental exposures and toxicities.

The United States Environmental Protection Agency (US EPA) has developed standardized methods for assessing risk to non-target organisms. Environmental exposure scenarios can be generated using the US EPA’s Surface Water Contamination Calculator software (SWCC v1.106), which incorporates recommended pesticide application rates for a given crop, local weather and soil characteristics, and the physicochemical properties of the pesticide to generate a 30-year series of peak estimated environmental concentrations (EECs) for a standardized wetland (US EPA, Washington, DC, USA). The ratio of the EEC for a given pesticide relative to its median lethal concentration (LC₅₀) for an organism of concern is then used to determine a risk quotient for that organism (RQ = EEC/LC₅₀; US EPA, 2014). The US EPA considers RQ values of 0.5 or greater as representing acute high risk to aquatic organisms (US EPA, 2014a).

Here we compare the relative toxicities of three insecticides in each of two classes of compounds (three organophosphates: chlorpyrifos, malathion, and terbufos; and three pyrethroids: esfenvalerate, λ-cyhalothrin, and permethrin) for two important macroarthropod predators of snails: the crayfish Procambarus alleni and the water bug Belostoma flumineum. Additionally, as an exploration of relative environmental risk within and between insecticide classes, we compared simulated peak environmental exposures for each insecticide to the US EPA level of concern (0.5 × LC50) for each species. Both classes of these insecticides affect the nervous systems of target organisms; organophosphates inhibit acetylcholinesterase activity (Newman and Unger, 2002) and pyrethroid insecticides act on voltage-sensitive ion channels in the axonal membranes of neurons to prevent repolarization of action potentials (Soderlund et al., 2002). Our goals were to determine if individual insecticides within a chemical class pose similar threats to these arthropods, and if there are individual chemicals or classes that might pose a lower risk to these taxa if runoff events occur.