Wildlife ecotoxicology of plant protection products: knowns and unknowns about the impacts of currently used pesticides on terrestrial vertebrate biodiversity.

Agricultural practices are a major cause of the current loss of biodiversity. Among postwar agricultural intensification practices, the use of plant protection products (PPPs) might be one of the prominent drivers of the loss of wildlife diversity in agroecosystems. A collective scientific assessment was performed upon the request of the French Ministries responsible for the Environment, for Agriculture and for Research to review the impacts of PPPs on biodiversity and ecosystem services based on the scientific literature. While the effects of legacy banned PPPs on ecosystems and the underlying mechanisms are well documented, the impacts of current use pesticides (CUPs) on biodiversity have rarely been reviewed. Here, we provide an overview of the available knowledge related to the impacts of PPPs, including biopesticides, on terrestrial vertebrates (i.e. herptiles, birds including raptors, bats and small and large mammals). We focused essentially on CUPs and on endpoints at the subindividual, individual, population and community levels, which ultimately linked with effects on biodiversity. We address both direct toxic effects and indirect effects related to ecological processes and review the existing knowledge about wildlife exposure to PPPs. The effects of PPPs on ecological functions and ecosystem services are discussed, as are the aggravating or mitigating factors. Finally, a synthesis of knowns and unknowns is provided, and we identify priorities to fill gaps in knowledge and perspectives for research and wildlife conservation.

Effects of plant protection products on ecosystem functions provided by terrestrial invertebrates.

Plant protection products (PPP) are extensively used to protect plants against harmful organisms, but they also have unintended effects on non-target organisms, especially terrestrial invertebrates. The impact of PPP on ecosystem functions provided by these non-target invertebrates remains, however, unclear. The objectives of this article were to review PPP impacts on the ecosystem functions provided by pollinators, predators and parasitoids, and soil organisms, and to identify the factors that aggravate or mitigate PPP effects. The literature highlights that PPP alter several ecosystem functions: provision and maintenance of biodiversity, pollination, biotic interactions and habitat completeness in terrestrial ecosystems, and organic matter and soil structure dynamics. However, there are still a few studies dealing with ecosystem functions, with sometimes contradictory results, and consequences on agricultural provisioning services remain unclear. The model organisms used to assess PPP ecotoxicological effects are still limited, and should be expanded to better cover the wide functional diversity of terrestrial invertebrates. Data are lacking on PPP sublethal, transgenerational, and "cocktail" effects, and on their multitrophic consequences. In empirical assessments, studies on PPP unintended effects should consider agricultural-pedoclimatic contexts because they influence the responses of non-target organisms and associated ecosystem functions to PPP. Modeling might be a promising way to account for the complex interactions among PPP mixtures, biodiversity, and ecosystem functioning.

Regulatory framework for the assessment of the impacts of plant protection products on biodiversity: review of strengths and limits.

The placing of plant protection products (PPPs) on the market in the European Union is governed by numerous regulations. These regulations are among the most stringent in the world, however they have been the subject of criticisms especially because of the decline in biodiversity. The objectives of this work were to review (1) the functioning and actors involved in the PPP framework processes, (2) the construction of the environmental risk assessment focused on biodiversity, and (3) the suggested ways to respond to the identified limits. Both literature from social sciences and ecotoxicology were examined. Despite the protective nature of the European regulation on PPPs, the very imperfect consideration of biodiversity in the evaluation process was underlined. The main limits are the multiplicity of applicable rules, the routinization of the evaluation procedures, the lack of consideration of social data, and the lack of independence of the evaluation. Strengths of the regulation are the decision to integrate a systemic approach in the evaluation of PPPs, the development of modeling tools, and the phytopharmacovigilance systems. The avenues for improvement concern the realism of the risk assessment (species used, cocktail effects…), a greater transparency and independence in the conduct of evaluations, and the opening of the evaluation and decision-making processes to actors such as beekeepers or NGOs. Truly interdisciplinary reflections crossing the functioning of the living world, its alteration by PPPs, and how these elements question the users of PPPs would allow to specify social actions, public policies, and their regulation to better protect biodiversity.

Natural products for biocontrol: review of their fate in the environment and impacts on biodiversity.

Biocontrol solutions (macroorganisms, microorganisms, natural substances, semiochemicals) are presented as potential alternatives to conventional plant protection products (PPPs) because they are supposed to have lower impacts on ecosystems and human health. However, to ensure the sustainability of biocontrol solutions, it is necessary to document the unintended effects of their use. Thus, the objectives of this work were to review (1) the available biocontrol solutions and their regulation, (2) the contamination of the environment (soil, water, air) by biocontrol solutions, (3) the fate of biocontrol solutions in the environment, (4) their ecotoxicological impacts on biodiversity, and (5) the impacts of biocontrol solutions compared to those of conventional PPPs. Very few studies concern the presence of biocontrol solutions in the environment, their fate, and their impacts on biodiversity. The most important number of results were found for the organisms that have been used the longest, and most often from the angle of their interactions with other biocontrol agents. However, the use of living organisms (microorganisms and macroorganisms) in biocontrol brings a specific dimension compared to conventional PPPs because they can survive, multiply, move, and colonize other environments. The questioning of regulation stems from this specific dimension of the use of living organisms. Concerning natural substances, the few existing results indicate that while most of them have low ecotoxicity, others have a toxicity equivalent to or greater than that of the conventional PPPs. There are almost no result regarding semiochemicals. Knowledge of the unintended effects of biocontrol solutions has proved to be very incomplete. Research remains necessary to ensure their sustainability.

Collective scientific assessment as a relevant tool to inform public debate and policymaking: an illustration about the effects of plant protection products on biodiversity and ecosystem services.

Several sustainable development goals cannot be achieved without implementing a new generation of environmental measures to better preserve or restore biodiversity and ecosystem services. However, understanding and addressing biodiversity loss and ecosystem degradation is a challenging problem that is not solvable without integrating the best and latest science. It is crucial to enhance the legibility of this knowledge for decision-makers and policymakers following good-practice standards of scientific assessment. This is the main objective of collective scientific assessments (CSAs), as carried out by the French National Research Institute for Agriculture, Food and the Environment (INRAE) since the early 2000s following a documented procedure to inform public policy and foster public debate on complex interdisciplinary issues. This article describes the main steps of the CSA procedure designed by INRAE's Directorate for Collective Scientific Assessment, Foresight and Advanced Studies, from formulation of the initial question asked by public or para-public bodies (typically ministry divisions or environmental agencies) to wider dissemination of the results and conclusions. This process description is then illustrated through the example of a CSA recently commissioned by three French Ministries (for Ecology, for Research, and for Agriculture) regarding (i) contamination of terrestrial, freshwater, and marine ecosystems by plant protection products (PPPs); (ii) the resulting effects on biodiversity and ecosystem services; and (iii) possible prevention and mitigation strategies. The capacity of this kind of CSA to inform public debate and policymaking is then exemplified through a description of the main outcomes generated by the latest CSA dealing with the adverse effects of PPPs. We also provide a short overview of some key expectations from the current CSA, with a focus on the recent development of the ecosystem service approach in ecological risk assessments of PPPs in the European Union. This illustration demonstrates that CSAs, which are applicable to a wide variety of complex interdisciplinary questions that are not limited to environmental issues, are a relevant tool to inform public debate and policymaking.