Biodiversity and services provided by nature: what is known about the impact of pesticides?

A look at the context, the results and the leads opened up by this wide-ranging work.

Why this collective scientific expertise?

To have an up-to-date overview of scientific knowledge

The decline in biodiversity in France and the rest of the world has been documented in an increasing number of publications over the past twenty years, a warning reinforced by the publication of the 2019 IPBES report¹. Environmental contamination by pesticides has been identified as one of the causes of this situation. Ambitious public policies are now in place in France and Europe to regulate the use of plant protection products - in other words, pesticides used on crops, gardens, green spaces and infrastructures - and to encourage alternatives to synthetic pesticides. However, the use of these substances remains high: 55,000 to 70,000 tonnes are still used in France, depending on the year. Public authorities, farmers, environmental protection associations, water agencies, scientists, industrialists, citizens... all are concerned by this issue which affects our environment and our food. In order to have an updated inventory of scientific knowledge, the ministries in charge of the Environment, Agriculture and Research asked INRAE and Ifremer for a collective scientific expertise on the impacts of plant protection products on biodiversity and ecosystem services. The results of this multidisciplinary and collective exercise, which mobilised 46 experts from 19 research organisations over a period of 2 years, were shared at a feedback symposium attended by over 600 participants on 5 May.

In 2005, the public authorities commissioned INRA and Cemagref (now merged into INRAE) to carry out a first collective scientific expertise on pesticides and their impact on agriculture and the environment, with the effects on human health being assessed by INSERM. In 2008, INRA delivered another expertise on the consequences of agriculture on biodiversity. These expertises helped to better integrate pesticide reduction into research orientations and were decisive in building the first French plan for pesticide reduction in agriculture. Launched in 2008 following the Grenelle de l'Environnement (a national consultative process), the Ecophyto 2018 plan had an ambitious and quantified objective: to reduce the use of pesticides by half within 10 years. Since then, the regulations governing the marketing of pesticides have evolved: withdrawal of substances with the highest persistence in the environment or the highest toxic effects, recognition and prioritisation of biocontrol, and the introduction of phytopharmacovigilance² to monitor the effects of pesticides during their use. In addition, the European Union has adopted the Water Framework Directive and the Marine Strategy Framework Directive as well as the Pesticides Package in order to better protect human health and the environment against the risks associated with chemical substances. Agricultural practices are changing, with more emphasis on biocontrol solutions, organic farming and agroecology. Scientific knowledge and analytical techniques have been strengthened to better characterise the effects of substances and the contamination of ecosystems. They also mobilise new concepts like ecosystem services, i.e. services that nature provides to society (such as pollination or biological pest control), holobiont (formed by an organism, e.g. a plant, and the communities of microorganisms that are closely associated with it, called its microbiota) and exposome (all the chemical, physical and biological exposures to which we are subjected).

Based on a bibliographic analysis of more than 4,000 international scientific publications, the expertise delivered on 5 May by INRAE and Ifremer updates the current state of knowledge and identifies what is solid, needs to be consolidated or has not been sufficiently explored since the preceding expertises. These data are essential for the French and European public authorities in terms of regulations and research strategy. In addition to this INRAE-Ifremer expertise, Inserm has updated its expertise on the impacts of pesticides on human health in 2021 and INRAE has been commissioned to carry out an expertise on the management of plant covers to promote the natural regulation of pests (results to be delivered on 20 October).

What insights have been gained on the impacts?

On land and at sea: plant protection products are present everywhere

The picture drawn in 2022 is much more accurate than those from 2005 and 2008 owing to the densification of the monitoring network and the improvement of analysis techniques that focus on plant protection products and certain products resulting from their degradation (or transformation). Glyphosate - by far the most widely used herbicide in the world - and its main transformation product (AMPA) are among the most widespread substances in the soil. All environments are affected by the contamination of mixtures of plant protection products, but agricultural areas close to the application sites are the most contaminated. This contamination then affects soils and watercourses to the seas and oceans, with generally decreasing concentrations along this continuum. Some pollutants that are very persistent in the environment, such as DDT, lindane and hexachlorobenzene, which have been banned for years, are found as far as the deep sea and the polar zones. Everywhere, mixtures of pollutants are found: phytopharmaceutical products, themselves in mixtures, are present alongside pharmaceuticals and microplastics....

All environments are affected by the contamination of mixtures of plant protection products, but agricultural areas close to the application sites are the most contaminated. This contamination then affects soils and watercourses to the seas and oceans.

On the other hand, little scientific data are available on the contamination of the overseas regions, which have specific features linked to particular regulations. One exception to this observation concerns chlordecone, which was authorised in a derogatory manner until 1993 (after being banned in 1990) in the banana plantations of the French West Indies. It has been the subject of numerous studies in Guadeloupe and Martinique, where it is present throughout the land-sea continuum, although it becomes more diluted the further one moves away from the spraying zones.

Biodiversity is affected, as well as the services it provides

Chemical pollution - to which plant protection products contribute - is the third or fourth most important factor in the destruction of biodiversity worldwide, after the change or destruction of natural habitats, resource exploitation and climate change. Current knowledge concerning more specifically the effects of plant protection products is mainly generated in agricultural contexts, the main products studied being synthetic pesticides and copper. Very little knowledge is available on biocontrol products. Specific to French regulations, they include macro-organisms (like insects and nematodes) and micro-organisms (like viruses, bacteria, fungi and yeasts) released into crops to control their pests, chemical mediators (such as pheromones or kairomones) that trap, divert and disturb attackers, as well as natural substances. The latter are of mineral, plant or animal origin and have various uses (e.g. fungicides, insecticides or herbicides).

There is strong evidence that plant protection products are one of the main causes of the decline of terrestrial invertebrates in agricultural areas, including pollinating insects and pest predators (ladybirds, carabids, etc.) as well as birds. In seed-eating birds, direct effects are predominant due to the toxicity of ingested seeds. For insectivorous birds, the indirect effects are considerable: they lose their food supply because of the reduction in the number of insects. Aquatic organisms are also affected. Macroinvertebrate populations could decrease by 40% in the most polluted agricultural rivers. For all these terrestrial and aquatic organisms, the direct and indirect non-lethal effects are considerable, something that was not studied to the same extent 15 years ago. These effects can take the form of loss of orientation or flight ability in insects and birds, reduced reproductive efficiency or immune deficiencies.  Some of these effects are because of damage to the microbiota, i.e. all the microorganisms present in these organisms (as is, for example, the case with the intestinal flora in humans). Some of these products also affect the endocrine system, which are mainly studied in mammalian and fish model species and whose consequences on populations have yet to be assessed.

Plant protection products are also responsible for the decline of amphibians (25% of their populations are threatened in Europe) and bats. In addition to these findings by type of organism, the study also focused on the ecological role they play. Microorganisms, which are present in abundance in all environments, are mainly affected in agricultural soils and nearby waterways contaminated by plant protection products. Their capacity to degrade organic matter and supply nutrients to ecosystems is diminished.

The expertise highlights the importance of landscape management for biodiversity resilience

The expertise highlights the importance of landscape management for biodiversity resilience; it is essential to create refuge areas (terrestrial and aquatic vegetation) that are interconnected: they are reservoirs for species that can then recolonise neighbouring environments. However, these refuge areas, and more generally natural habitats, are threatened by the simplification of agricultural landscapes (larger plots with less varied borders) and by soil artificialisation, with plant protection products playing an aggravating role.

The three ecosystem services for which the impacts of pesticides have been most studied to date are cultivated plant production (protected from pests and diseases by plant protection products), pollination (negatively affected, mainly by neonicotinoids and pyrethroids) and the control of pests by natural predators (also negatively affected). However, the latter two services are useful to the first: plant production will therefore also be negatively impacted in the long term. There are many knowledge gaps regarding the other services.

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What levers can be used to limit these impacts?

In addition to reducing the use of pesticides, which remains the primary lever for preserving biodiversity, the expertise identifies three main types of action levers: mitigation of effects, regulation and the use of less persistent and impacting products such as biocontrol products.

Mitigation of effects

A need to combine different levers for better effectiveness

Mitigation can be achieved by limiting the drift (off target) of plant protection products during application and their immediate transfer to soil and water, which implies intervening when the weather is favourable (now regulated). Adapted agricultural equipment and products with heavier formulations make it possible to limit drift. It is important to cover the soil with vegetation: 40% less polluted in this case. Phytoremediation - or depollution by plants - can help reduce the presence of pesticides in the soil by 10%. Landscape management also plays a major role in creating buffer zones that limit runoff to neighbouring soils and watercourses: ponds can reduce runoff by 60%, and hedges and grass strips by 40%.

A complementary approach is to favour biocontrol over synthetic pesticides. However, there is a need for research and data on environmental contamination and its impacts. Moreover, the difficulty is that some biocontrol products and organisms are already present in the environment and it is difficult to quantify the contribution made by pest control. Biocontrol solutions are generally less persistent and have lower ecotoxicity than conventionally used pesticides, but there are exceptions, such as Bacillus thuringiensis, spinosad and pyrethrins.

There is no single solution to reduce the impacts of pesticides, but a need to combine different levers for better efficiency.

Regulation

The current regulations, although very ambitious and restrictive, as highlighted by the scientific literature, could be improved to better achieve their protection objectives. At present, routine risk assessment does not take into account the complexity of living organisms (and interactions between species) nor cocktail or multi-stress effects. Improvements could also be achieved by more extensive integration of epidemiological monitoring data. The species (e.g. seed-eating birds to better assess indirect effects) and the environments studied should also be better targeted.

Research needs

François Houllier: We need to know more about the sea. The Blue Chair set up by Ifremer will enable us to better study the impact of pollution on the microbiota of marine organisms. Greater success will be sought in submitting projects to the French Priority Research Programme "Ocean &Climate", the French Priority Research Programme and Infrastructure "One Water", as well as the projects of the European mission for the restoration of seas and oceans. But a large part of the levers is on land.

In conclusion of this expertise, François Houllier, CEO of Ifremer, affirmed his institute's commitment to pursue research to better shed light on the gaps: "Most of the levers are on land, but we need to know more about the sea: The Blue Chair set up by Ifremer in Nantes will study the impact of pollution on the microbiota of marine organisms; I also hope that ambitious projects will be submitted on the marine exposome in the French Priority Research Programme "Ocean-Climate", on the land-sea continuum in the French Priority Research Programme and Infrastructure "One Water" or in the context of the European mission for the restoration of oceans and waters.” For his part, Philippe Mauguin, CEO of INRAE, insisted on the need to strengthen the expertise and the development of alternative approaches. "The One Health concept, a single human, animal and environmental health, could thus be further mobilised in research with the concepts of exposome, eco-exposome and microbiota.” It is necessary to make progress in the qualitative and quantitative characterisation of biodiversity and ecosystem services, in attributing the multiple causes of decline like chemical pollution, climate change and soil artificialisation. It will also be necessary to correct the magnifying effect created by the focus of research on particular molecules or chemical groups and the reverberation effect whereby a result can only be obtained if it is present in the area “illuminated” by the research programme.

Philippe Mauguin: The One Health concept, a single human, animal and environmental health, could thus be further mobilised in research with the concepts of exposome, eco-exposome and microbiota.

The French public authorities have mobilised significant resources to support alternatives to pesticides, in particular led by INRAE: the French Priority Research Programme Growing and protecting crops differently, the French Priority Research Programme and Infrastructure (PEPR) on varietal selection and the major challenges biocontrol and robotics. Agroecology and alternatives to pesticides are a priority in INRAE's 2030 roadmap, and INRAE has also been the driving force behind a European alliance to move away from pesticides involving 34 research institutes from 20 European countries. A symposium organised by INRAE in Dijon on 2 and 3 June, under the aegis of the French Presidency of the European Union, will be an opportunity to share progress and research in this field. In addition to the French public authorities, Philippe Mauguin pointed out the need to raise awareness among the European public authorities and to share this expertise in an operational manner; this was carried out on 11-12 May at a ministerial conference organised by the Ministry of the Environment. On this occasion, Anses presented the European Partnership for the Assessment of Risks from Chemicals (PARC), which it coordinates. The Partnership has the ambition of designing a new generation of more protective assessment. In December 2022, INRAE will also deliver a forecast on the exit from pesticides at the European level.

Notes:

1. IPBES: Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services
2. Phytopharmacovigilance: System that aims to monitor the undesirable effects of plant protection products available on the market and covers the contamination of the environment, exposure and impacts on living organisms - including humans - and ecosystems as well as the emergence of resistance (Anses).