Cross‐Ecosystem Fluxes of Pesticides from Prairie Wetlands Mediated by Aquatic Insect Emergence: Implications for Terrestrial Insectivores

Abstract

Contaminants alter the quantity and quality of insect prey available to terrestrial insectivores. In agricultural regions, the quantity of aquatic insects emerging from freshwaters can be impacted by insecticides originating from surrounding croplands. We hypothesized that, in such regions, adult aquatic insects could also act as vectors of pesticide transfer to terrestrial food webs. To estimate insect-mediated pesticide flux from wetlands embedded in an important agricultural landscape, semipermanetly and temporarily ponded wetlands were surveyed in cropland and grassland landscapes across a natural salinity gradient in the Prairie Pothole Region of North Dakota (USA) during the bird breeding season in 2015 and 2016 (n = 14 and 15 wetlands, respectively). Current-use pesticides, including the herbicide atrazine and the insecticides bifenthrin and imidacloprid, were detected in newly emerged insects. Pesticide detections were similar in insects emerging from agricultural and grassland wetlands. Biomass of emerging aquatic insects decreased 43%, and insectmediated pesticide flux increased 50% along the observed gradient in concentrations of insecticides in emerging aquatic insects (from 3 to 577 ng total insecticide g -1 insect). Overall, adult aquatic insects were estimated to transfer between 2 and 180 µg total pesticide wetland -1 d -1 to the terrestrial ecosystem. In one of the 2 study years, biomass of emerging adult aquatic insects was also 73% lower from agricultural than grassland wetlands and was dependent on salinity. Our results suggest that accumulated insecticides reduce the availability of adult aquatic insect prey for insectivores and potentially increase insectivore exposure to insect-borne pesticides. Adult aquatic insects retain pesticides across metamorphosis and may expose insectivores living near both agricultural and grassland wetlands to dietary sources of toxic chemicals.

Emerging Midges Transport Pesticides from Aquatic to Terrestrial Ecosystems: Importance of Compound- and Organism-Specific Parameters

“…The estimated value is however considerably lower than what has been observed in field studies, where estimates of daily fluxes of insecticides from wetlands are between 0.4 and 26.8 ng/m 2 •d, when also including other aquatic insect orders. 9 The specific contributions of midges in this context are, however, of relevance considering that Chironomidae are the most abundant and have the longest emergence window among the common emerging insect orders, thus making them an important nutrient source in terrestrial food webs. 61,63 Moreover, aquatic insect communities in polluted aquatic environments often show a shift toward dipterans dominating the remaining insect fauna due to their tolerance of a wide range of anthropogenic disturbances, for example, in aquatic environments disturbed by agriculture.…”

“…During their development in freshwater ecosystems impacted by agriculture, industry, or waste water, the aquatic life stages of emerging insects are regularly exposed to a broad range of anthropogenic contaminants. − Contaminants with low toxicities can potentially bioaccumulate in the developing aquatic life stages of emerging insects with minimal effect on emergence success and, when retained by the emerging adult insects after metamorphosis, can be transported into adjacent terrestrial ecosystems . A wide range of contaminants have been observed to be retained by the adult aquatic insects after metamorphosis, for example, some pesticides, metals, metal-based nanoparticles, pharmaceuticals, polychlorinated biphenyls (PCBs), per- and polyfluorinated alkyl substances, and polycyclic aromatic hydrocarbons (PAHs). − After successful emergence, these insects serve as important nutritional sources for spiders, lizards, birds, and bats in adjacent terrestrial food webs . Retention of contaminants by emerging insects therefore has the potential to increase the dietary exposure of terrestrial insectivores, including species of high conservation value .…”

Aquatic‐Terrestrial Insecticide Fluxes: Midges as Neonicotinoid Vectors

“…Neonicotinoid insecticides, however, break away from the trend toward reduced environmental persistence and are found in freshwater ecosystems globally (Morrissey et al, 2015). The ubiquitous presence of insecticides in freshwater ecosystems, even for brief exposure periods during run‐off or spray drift events, has the potential to negatively impact linked aquatic–terrestrial food webs through emerging aquatic insects (Bundschuh et al, 2022; Kraus et al, 2021; Kraus, 2019; Schulz & Liess, 2001; Tooker & Pearsons, 2021).…”

“…Up to now aquatic–terrestrial contaminant transfer has been reported for several classes of contaminants, including metals (Chételat et al, 2008; Wesner et al, 2017), metal‐based nanoparticles (Bundschuh et al, 2019), pharmaceuticals (Previšić et al, 2021), halogenated organic pollutants (Liu et al, 2018), and some fungicides and herbicides (Roodt et al, 2022). In the terrestrial environment, these contaminants can enter the food web and potentially result in detrimental effects on consumers, such as prey avoidance or sublethal effects (Koch et al, 2020; Kraus et al, 2014, 2021; Richmond et al, 2018). Furthermore, exposure to insecticides during the development of emerging aquatic insects can impact the terrestrial recipient food web through changes in insect emergence phenology and productivity.…”

“…Contaminant flux is therefore predicted to decrease with increasing toxicity of a contaminant to aquatic life stages due to decreased survival and emergence (Kraus, 2019). Fluxes of insecticides, including highly toxic neonicotinoids, have recently been reported from contaminated wetlands corresponding with reduced overall insect emergence (Kraus et al, 2021). However, there is a lack of information on the interplay of exposure concentration, toxicity, emergence phenology, and contaminant retention through metamorphosis on the insect‐mediated flux of current‐use insecticides.…”