Date Published: March 23, 2017
Publisher: Public Library of Science
Author(s): Jesse C. Miles, Jessica Hua, Maria S. Sepulveda, Christian H. Krupke, Jason T. Hoverman, Nicolas Desneux.
The widespread usage of neonicotinoid insecticides has sparked concern over their effects on non-target organisms. While research has largely focused on terrestrial systems, the low soil binding and high water solubility of neonicotinoids, paired with their extensive use on the landscape, puts aquatic environments at high risk for contamination via runoff events. We assessed the potential threat of these compounds to wetland communities using a combination of field surveys and experimental exposures including concentrations that are representative of what invertebrates experience in the field. In laboratory toxicity experiments, LC50 values ranged from 0.002 ppm to 1.2 ppm for aquatic invertebrates exposed to clothianidin. However, freshwater snails and amphibian larvae showed high tolerance to the chemical with no mortality observed at the highest dissolvable concentration of the insecticide. We also observed behavioral effects of clothianidin. Water bugs, Belostoma flumineum, displayed a dose-dependent reduction in feeding rate following exposure to clothianidin. Similarly, crayfish, Orconectes propinquus, exhibited reduced responsiveness to stimulus with increasing clothianidin concentration. Using a semi-natural mesocosm experiment, we manipulated clothianidin concentration (0.6, 5, and 352 ppb) and the presence of predatory invertebrates to explore community-level effects. We observed high invertebrate predator mortality with increases in clothianidin concentration. With increased predator mortality, prey survival increased by 50% at the highest clothianidin concentration. Thus, clothianidin contamination can result in a top-down trophic cascade in a community dominated by invertebrate predators. In our Indiana field study, we detected clothianidin (max = 176 ppb), imidacloprid (max = 141 ppb), and acetamiprid (max = 7 ppb) in soil samples. In water samples, we detected clothianidin (max = 0.67 ppb), imidacloprid (max = 0.18 ppb), and thiamethoxam (max = 2,568 ppb). Neonicotinoids were detected in >56% of soil samples and >90% of the water samples, which reflects a growing understanding that neonicotinoids are ubiquitous environmental contaminants. Collectively, our results underscore the need for additional research into the effects of neonicotinoids on aquatic communities and ecosystems.
Neonicotinoid insecticides, which account for 26% of the global insecticide market, have recently become the most widely used insecticide class worldwide . Developed in the 1980s, neonicotinoids first came into regular use with imidacloprid starting in the early 1990s. Since that time additional active ingredients have been developed and classified into three groups: N-nitroguanidines (imidacloprid, thiamethoxam, clothianidin, dinotefuran), nitromethylenes (nitenpyram), and N-cyanoamidines (acetamiprid and thiacloprid) . Currently, thiamethoxam and its breakdown product clothianidin dominate usage in North American cropping systems . The increasing usage of neonicotinoids has been fueled by their relatively low toxicity to vertebrate species . Neonicotinoids target the post-synaptic nicotinic acetylcholine receptor, causing paralysis and death. Because neonicotinoids bind more strongly to insect receptors than vertebrate receptors and invertebrates have a higher ratio of nicotinic receptors, they generally have low toxicity to vertebrate species . A key driver of rapid neonicotinoid adoption in North America is the ability to apply them prophylactically as a seed dressing to some of the most widely grown annual crops . As seeds germinate, the insecticide is incorporated into the plant and distributed systemically during growth. This process is facilitated by the high water solubility of neonicotinoids . Although neonicotinoids can be used as spray applications, approximately 60% of applications are as seed dressings . The prophylactic application of neonicotinoids to virtually all seeds of corn, soybeans and other annual crops without prior knowledge of the season’s pest populations has raised concern over the environmental risks associated with their use .
Neonicotinoids pose a risk to aquatic systems due to their low soil binding, high soil persistence, and high water solubility . Using controlled laboratory experiments, we documented that the neonicotinoid clothianidin has lethal and sublethal effects on wetland invertebrates at field relevant concentrations. Using a community-level mesocosm experiment, we found that clothianidin can reduce the abundance of predatory invertebrates, which indirectly benefits clothianidin-tolerant herbivores in the community. Additionally, we detected four neonicotinoids in the vast majority of soil and water samples at field sites in close proximity to agricultural lands.