Indirect effects of herbicides on biota in terrestrial edge-of-field habitats: A critical review of the literature

This manuscript reviews the current understanding of indirect effects of herbicides in agricultural edge-of-field habitats, with the goal of identifying key uncertainties and critical knowledge gaps. Indirect effects are defined as those observed in animal species as a result of direct effects of exposure to an herbicide on the plant community. Following an extensive search of the literature, the review focuses on 29 studies that specifically addressed some aspect of the indirect effects of herbicides in edge-of-field habitats. The bulk of work has focused on invertebrate and bird species, with few studies investigating small mammals, amphibians, or reptiles (riparian field margins were not included, where amphibians and reptiles are more likely to occur). Key knowledge gaps identified in the review include: (1) a lack of studies incorporating exposures to edge-of-field habitats that would be relevant based on current agronomic practices; (2) few studies attempt to quantify the herbicide exposure within edge-of-field habitats and consider the influence of methods of herbicide application on exposure; (3) few studies incorporate quantitative linkages between direct effects on the plant community, indirect effects on animal species, and population-level effects; and (4) the majority of studies have been conducted in Europe, with a distinct lack of research investigating the indirect effects of herbicides on field margin fauna under agricultural practices in other regions of the world. Of the studies reviewed, many lack one or more key components of a robust experimental design that would be necessary to quantify exposure to and/or effects of herbicides. Adequate quantification of exposure of the plant community is often lacking, including poor representation of exposure scenarios that adequately mimic spray drift. Further, there is a dearth of studies that even attempt to investigate ecologically-relevant linkages between direct effects on plants and associated indirect effects on plant-dependent communities and population-level effects. The state of knowledge pertaining to the indirect effects of herbicides in agricultural field margins is currently insufficient to adequately assess the nature and extent of risks posed by herbicides in these important habitats. There is a strong need for carefully planned and executed field experiments to quantitatively characterize the risks posed by application of herbicides to terrestrial environments. These studies will help to reduce uncertainty and ensure adequate protection of non-target organisms from possible indirect effect of herbicides.