To achieve the pesticide-free goal, several strategies have to be implemented simultaneously. These strategies were developed by considering the fields of knowledge and the scientific disciplines that call for new research fronts. We have thus distinguished what came under (1) agronomy, (2) genetics, (3) biological control, (4) machinery and digital, and (5) economic and social sciences. First, regarding agricultural sciences, cropping systems should be redesigned based on agroecological principles to implement radical change from a curative approach to a prophylactic approach. Second, regarding biological control, biocontrol solutions should be diversified and enhanced to be tailored to a variety of environments and practices. Third, regarding genetics, breeding programs should involve concepts of functional biodiversity and evolutionary ecology. Fourth, regarding machinery and digital, agricultural equipment should be modified to facilitate the transition to pesticide-free agricultural practices, while digital technologies should help optimize pest control and improve epidemiological surveillance. Fifth, regarding economic and social sciences, public policies and private initiatives for the transition toward pesticide-free systems should be implemented.
Redesigning cropping systems to enhance prophylaxis
Studying and designing practices in a variety of situations: from generic to tailored solutions
To date, in developed countries, except for organic agriculture, the technical innovations designed and the way they spread were consistent with dominant high-input systems. For pest control, these solutions were almost only chemical products (except for a few biocontrol solutions) applied either before the occurrence of pests to prevent their emergence (e.g., weeds, fungi) or when they are observed (e.g., mainly insects, but also diseases and weeds to a lesser extent). Pesticide use in agricultural systems cannot be reduced greatly with curative techniques alone; doing so will depend greatly on non-chemical preventive practices that enable prophylaxis (i.e., all technical actions implemented to prevent the occurrence, spread or damage of pests beforehand). In conventional systems, prophylaxis relies on nature-based mechanisms, which can be enhanced by implementing combinations of practices that influence the multiple components of agroecosystems. Prophylaxis not only involves technical actions directly enhancing pest regulations (e.g., flowering strips favoring the development of auxiliaries), but also techniques that slow down the development of pests within the crop (e.g., lower plant densities enhancing a more airy microclimate), or that decrease the pest development/spreading (e.g., a lower and different fertilization management decreasing spore production for aerial fungi-based diseases, or lowering weed growth), or that disrupt the pest cycle (e.g., diversifying the crop sequence). While pest-control solutions consistent with high-pesticide systems are generic and applicable to every situation, nature-based solutions should be adapted to the specific characteristics of the agricultural situation (e.g., soil and climate conditions, value chain, workload) (Meynard et al. 2003; Rusch et al. 2010; Médiène et al. 2011; Duru et al. 2015).
To date, however, the effects of alternative practices have rarely been studied in a wide range of environments or cropping systems since research was used to produce generic rules and recommendations from a few experiments. The kind of tailoring needed would benefit from the initiative and experience of pioneer farmers and experimenters, and from expert knowledge, derived from action in real environments, within an open-innovation process (Chesbrough et al. 2014). Approaches developed recently, such as on-farm innovation tracking (Verret et al. 2020; Salembier et al. 2021), system experiments (Debaeke et al. 2009), hybridization of farmers’ experience and scientific knowledge (Girard and Magda 2020), co-design of farming systems (Le Gal et al. 2011), and support of farmers’ engagement in agroecological practices (Catalogna et al. 2018; Leclère et al. 2018), are emerging methodological bases. They help to identify, analyze, pinpoint, and assess a large set of combinations of practices oriented toward pest regulation. They should be developed specifically to help farmers develop, implement, and improve their practices, thus supporting farmers as designers (Salembier et al. 2018).
Experiments to address multiple stresses in real and situation-specific conditions
Another method is experimentation, specifically comprehensive experiments, which have long been the methods that agronomists used most to produce technical innovations (Salembier et al. 2018). Experiments are usually performed under controlled or mono-stress conditions (e.g., water, or nitrogen, or one pest that decreases growth and yield) to analyze effects of each factor independently and to produce general response laws. For pesticide-free systems, enhanced research should aim to characterize effects of combinations of practices that can address multiple stresses in real and situation-specific conditions. In such a wide range of situations, production of generic knowledge should benefit from hybridizing local scientific knowledge and know-how to deal with the diversity of environments and support locally adapted action. More recently, system experiments were developed; they aim to assess and sometimes gradually improve consistent combinations of practices that target one or more goals (Debaeke et al. 2009; Lechenet et al. 2017). Few system experiments have targeted high performance in pesticide-free systems (Colnenne-David et al. 2014). By identifying the specific processes behind this performance, these experiments help to design and assess prophylaxis-oriented systems and potentially scale out the robustness of their performance, process-based reasoning, and the practices they implement.
Renewing assessment of practices
Since input-intensive agriculture and its related practices were developed mainly to increase yield, innovative agronomic practices are first assessed for their impacts on yield. In contrast, pioneer farmers, who implement innovative low-input practices, often rely on other satisfaction criteria (e.g., maximize the average gross margin calculated over several years, reduce workload). They use such criteria to define the technical changes they progressively implement on their fields, thus building their technical transition toward agroecology (Toffolini et al. 2016; Verret et al. 2020; Salembier et al. 2021). In recent years, numerous multicriteria assessment tools have been developed (Sadok et al. 2009), but they generally assess impacts of entire complex systems, including processes from the “cradle to the grave” (Deytieux et al. 2012; Nemecek et al. 2015). However, these tools do not support farmers in the step-by-step design of their agroecological systems. Indeed, more research should be dedicated to developing indicators aiming to support farmers’ actions in the uncertainty (due to the huge knowledge gaps and the high variability of the impacts of practices depending on the context). In parallel, other tools should be created to enhance, capitalize, and share their learning during the change of their cropping systems toward ambitious challenges.
Developing coupled innovation to enhance diversification
Diversified cropping systems are one of the most powerful ways to reduce pesticide use (Ratnadass et al. 2012), but they may result in products whose characteristics do not correspond to the demand or available processes of agri-food value chains (Magrini et al. 2016; Meynard et al. 2018). Moreover, development of new crops, which is currently rare in research and in the practices, is hampered by a lock-in situation in the entire agri-food system, including a lack of market for agricultural products from these crops and new practices (Magrini et al. 2016; Meynard et al. 2018). In particular, developing intercropping (i.e., growing at least two species partly simultaneously on the same field) raises two questions: on the one hand, the grain sorting from both species, and on the other hand, the valuation of crops with high agronomic interest but low value in the downstream sector, such as legumes (Magrini et al. 2018).
To unlock dominant systems, innovations in the field should be coordinated with innovations at other steps of the value chain, especially downstream with processing innovations. Stimulating such coupled innovation processes, which aims to connect innovation processes in agriculture and food sectors to support healthy and sustainable agri-food systems, calls for specific research (Meynard et al. 2017; Brun et al. 2021). To date, most innovation and design in these sectors have been separated due to specialization of skills, knowledge, and methods. To make coupled innovation possible, methods should be developed to manage these multi-stakeholder systems to increase sharing of knowledge and targets (which are largely disconnected), coordinate design processes, and assess innovations for a variety of criteria that connect agriculture and food, as successfully demonstrated for coupled innovation in cropping systems and machinery (Salembier et al. 2020).
Including the landscape scale in pest management
Pests, such as most insects and many fungi, disperse widely into the environment, sometimes over large distances. Thus, to prevent their spread, practices should be changed not only at the field scale, but also at the landscape scale (i.e., organizing practices at a large scale, which requires the involvement and coordination of many stakeholders). This management complexity is one reason why research on pest management has rarely considered the landscape scale. More generally, there is a lack of information available about the performance of most preventive measures as a function of their degree of adoption at a landscape scale (Benoît et al. 2012). Pesticide-free agriculture thus requires designing pest-suppressing landscapes that combine green infrastructure, landscape mosaics, and related practices (Fig. 2). To develop these landscapes, stakeholders in the territory must be involved in the design process, since they must be coordinated, and assessing consequences of changes in practices at the individual scale is not sufficient (Moreau et al. 2019). Participatory methods with this goal are being developed, and new tools to monitor processes of change at the territory scale should be designed and developed, due to new digital capacities, as developed for water in catchments (Prost et al. 2018). Beyond coordinating stakeholders, strong political will must emerge to reverse the trend of specialization of production, which is largely responsible for the oversimplification of landscapes (Roschewitz et al. 2005).
Diversifying biocontrol strategies and associated business models
For simplicity, we use “biocontrol” to refer to a broad range of pest-control methods. It refers to the four strategies of biocontrol that use living organisms, as defined by Eilenberg et al. (2001): (1) “classical biological control,” which corresponds to introducing an exotic, usually co-evolved, biocontrol agent for permanent establishment and long-term pest control; (2) “inoculation biological control,” which corresponds to releasing a living organism so that its populations become established and control a pest for an extended period, but not permanently; (3) “inundation biological control,” which corresponds to the use of living organisms to control pests when control is achieved exclusively by the released organisms themselves; (4) “conservation biological control,” which corresponds to modifying the environment or existing practices to protect and enhance specific natural enemies to reduce effects of pests. In addition, we also use “biocontrol” to refer to a variety of substances produced by living organisms (but without using these organisms directly): semiochemicals (e.g., pheromones, kairomones), metabolites, plant extracts, and plant-defense stimulators. These substances may be natural extracts or chemically synthesized molecules provided that the latter are identical to natural molecules.
Changing and diversifying business models of the biocontrol sector
Business models currently used by the private biocontrol sector are similar to those of the chemical pesticide sector. These business models are based on selling large quantities of products that are promoted for their short-term measurable efficacy, short-term economic competitiveness, and simplicity of use. By applying this rationale to biocontrol methods, practitioners actually implicitly depreciate these methods because they compare them directly to chemical pesticides based on characteristics that do not correspond to those of most biocontrol modes of action (e.g., mid- or long-term regulation, prophylaxis) and do not promote the overall sustainability of these methods. Practitioners also overlook business models based on services rather than products. The associated value chains and supply chains are also organized to produce, distribute, and use chemical pesticides, not biocontrol products and services (Glare et al. 2012). Analyzing and developing a variety of business models adapted to each type of biocontrol and food chain appears as an interdisciplinary axis of research (e.g., management, sociology, economy, agronomy, biology), which is particularly important for the growth of biocontrol in sustainable pesticide-free agrosystems and food chains (Fig. 3). Such research is extremely rare, although some researchers have occasionally investigated commercialization models (e.g., Harman et al. 2010). This would enable organizational innovations, such as novel or adapted value chains and business models, modifying and diversifying the current industrial sector of biocontrol.
Defining biocontrol strategies and priorities by anticipating the needs of the most sustainable cropping systems and food chains
Expectations regarding biocontrol are highly unfocused since practitioners want biocontrol solutions to be developed for all target pests that are formerly or currently controlled by broad-spectrum chemical systems. Private and public investment and market analyses are driven without scientifically based criteria and often rely on criteria traditionally used for developing chemical pesticides (e.g., targeting large markets in terms of hectares affected by a pest or niche markets with no current control solution). Analyzing the issues that pests cause in pesticide-free cropping systems while identifying biocontrol solutions adapted to each issue should become a research and innovation activity in itself. It should be based on analyzing (1) pest control issues in a variety of cropping systems and associated agri-food chains with high environmental, economic, and social sustainability (and representative of systems that will become widely used in the future); (2) factors that influence the severity of these pest issues in these systems; and (3) the fit of potential types of biocontrol strategies (e.g., classical, conservation) with the target pest issue, cropping system, and agri-food chain. Doing so would comprehensively identify needs of each type of agri-food chain and geographic area, and would provide insights into the expected role and technical and economic characteristics of potentially relevant biocontrol strategies. This will enable research and innovation investment strategies and market analysis methods to be adjusted for both public and private stakeholders.
Redirecting efforts to focus on interactions of biocontrol with other agroecological practices rather than with pesticides
Research and innovation resources are allocated to studies of the compatibility and interactions of biocontrol with chemical pesticides, while interactions among agroecological practices are currently overlooked. However, farmers’ crop management choices (e.g., plant species, crop treatment, rotation) shape plant health. For example, crop management practices can modify the soil microbiome, which might impact plant health since it is the initial reservoir from which beneficial plant microbes are recruited (Hunter et al. 2014), as shown for fertilization (Zhu et al. 2016). Redirecting efforts to focus on the compatibility and interaction between biocontrol and other agroecological approaches (e.g., agronomic practices, resistant cultivars, digital tools, machinery) is essential to clarify strategies for developing biocontrol for pesticide-free systems. Future research should focus on impacts of (a)biotic factors and agronomic practices applied to biological mechanisms involved in biocontrol. Doing so would enable specific recommendations for using biocontrol methods depending on the characteristics (e.g., environmental factors, practices) of each target cropping system. Likewise, factors that support the success of agronomic practices based on managing biological pest-regulation processes (i.e., conservation biocontrol mediated by agronomic practices) could be identified. The knowledge produced about interactions between biocontrol and other mechanisms will be critical to enable the design of cropping systems that implement genuine IPM. This need, which has been raised for decades, has been inhibited by the dominance of systems based on chemical pesticides (Thomas 1999).
Designing implementation of biocontrol at the landscape scale
Following the pesticide model, biocontrol is used and planned mostly at the field/farm scale, although it often requires thinking at the landscape scale. Despite success stories that combined biocontrol methods at the landscape scale (e.g., mating disruption using pheromones and sterile insects to control Lepidoptera (Thistlewood and Judd 2019)), landscape-scale strategies of pest management are still rarely implemented in practice, perhaps because they appear more complex and less economically favorable in the short term than field applications of chemical pesticide. Research on biocontrol solutions to be implemented at the landscape scale should be highly prioritized. These challenging research activities may require a combination of modeling and experimental work at larger or smaller geographical scales (from a few fields, e.g., for sexual disruption, to large geographical areas, e.g., for landscape management-based conservation biocontrol). In parallel, social and technological sciences must be combined to consider all factors that influence successful implementation of these strategies. In particular, frameworks in social sciences and innovation management should be developed to characterize value chains and territories in which biocontrol is to be used, as should digital tools to ease monitoring and action planning at the landscape scale. These kinds of research activities should lead to the production of knowledge, tools, and policy recommendations that will facilitate implementation of landscape-scale and collective strategies that use biocontrol along with other agroecological practices.
Prioritizing modes of action other than short-term biocides
Methods that do not rely on biocides or organisms are currently overlooked and/or underexploited (e.g., mating disruption, pull–push strategies, plant-defense elicitors, microbiome management). While many research and innovation projects focus on identifying direct antagonists of pests (e.g., predators, parasites, parasitoids), more attention could be paid to other modes of action, particularly if they allow for sustainable approaches based on regulation rather than short-term and localized eradication (Aubertot et al. 2005). A promising area of applied research deals about the management of pest populations by manipulating semiochemicals and odorscapes, which enable a variety of pest control methods with little or no negative impact on local biodiversity, such as trapping, push–pull strategies, and mating disruption (Conchou et al. 2019). Understanding complex interactions between plants and microorganisms is another main research front. Indeed, the microbiome, which is associated with plant leaves, roots, and seeds, has a tremendous and yet untapped potential to improve plant resilience (Trivedi et al. 2017; Hartman et al. 2018). Manipulating plant immune systems is another promising perspective (Pieterse et al. 2014; Romera et al. 2019; Nishad et al. 2020), especially if its timing during plant development can be controlled. Such research would pave the way for developing control methods based on bio-inputs oriented toward greater sustainability. Indeed, these methods impact biodiversity less than biocide (bio-)inputs, and their application is based more on qualitative than quantitative strategies.
Developing biocontrol based on mid-/long-term management of pest populations
Given the dominant use of curative chemical pesticides and associated value chains, biocontrol activities that rely on long-term services tend to be marginalized. In particular, conservation biocontrol and classical biocontrol have been particularly neglected despite their history of success and their often outstanding cost–benefit ratios (e.g., from 1:50 to > 1:3000 for classical biocontrol programs performed in New Zealand and Australia in the past few decades) (Page et al. 2006; Hardwick et al. 2016). In addition, the diversity and density of resident natural enemies, as well as the pest-control services they provide, are rarely the target of routine detection and surveillance by or for practitioners. This strongly limits the potential for sound implementation of conservation biocontrol or inoculation biocontrol adjusted to the needs of cropping systems. Research needs to be reoriented to develop biocontrol strategies based on long-term regulation of pest densities. It could consist in studying factors that influence regulation of pests by resident organisms (i.e., conservation biocontrol) and their large-scale implementation by practitioners, as well as the use of dedicated sensors and tools to perform this monitoring. It would also be relevant to analyze factors that drive the success of strategies that rely on inoculation and temporary or permanent establishment of beneficial organisms (i.e., inoculation and classical biocontrol). Greater investment in these research axes should provide practitioners with a range of methods and strategies for conservation, inoculation, and classical biocontrol that enable mid-/long-term pest regulation, accompanied by business models and tools that facilitate their establishment and adoption.
Broadening the scope of breeding programs to include functional biodiversity and evolutionary ecology concepts
Enhancing functional biodiversity at multiple scales
Plant breeding is a vibrant science with cutting-edge technologies that provide new solutions to increase food security, but breeding programs still require several years to decades to obtain new crop varieties (Tester and Langridge 2010). To decrease the cost associated with releasing new varieties, breeding programs have progressively focused on a few crops, such as those in the Poaceae family (e.g., maize, rice, wheat). By doing so, they restrict the options for benefitting from genetic diversity in fields or the landscape, even though this diversity is an important way to regulate crop pests. Indeed, genetic uniformity promotes strong and directional selection pressure on pathogens. To limit this pressure, breeders can develop deployment strategies that include new varieties to foster diversification and new cultivars with different resistance genes as well as the ability to coexist (intercropping) without negative interactions such as competition for resources (Fig. 4). However, doing so has a cost that should be balanced by its side benefits on the environment and health. These strategies based on managing host (i.e., crop) genetic diversity can be introduced in time (i.e., rotations) or space (e.g., plant mixtures, landscape mosaics) (Veres et al. 2013; Snyder et al. 2021). Beyond the benefits of implementing more complex rotations with new species, intra-field genetic heterogeneity can generate countless ecological interactions. Indeed, coexisting species or genotypes can achieve synergies when they consume different resources or have different natural enemies, or when their resources or enemies vary in time and/or space. Some of these combinations protect plants effectively (Johnson et al. 2015), while enhancing soil quality and its connections to ecosystem services (Cong et al. 2015; Zhou et al. 2019). However, progress remains to be made to identify new complementary combinations of species and to select mixtures of varieties and populations that show increased resistance; they should include new cultivars but not ignore underused or forgotten species and cultivars (Chable et al. 2020). In parallel, targeting pesticide-free agriculture argues for including classic and emerging ecological theories about functional biodiversity and evolutionary ecology in plant breeding programs to capture benefits of genetic diversity (Gaudio et al. 2019). Some European programs as DIVERSIFY or REMIX on cropped species (refer also to the European initiative “Crop Diversification Cluster”) pointed out some results that support this assertion (Annicchiarico et al. 2019; Jäck et al. 2021). Genetic diversity could indeed promote species diversity in plant communities (Prieto et al. 2015; Meilhac et al. 2019), through genetic and ecological mechanisms (Meilhac et al. 2020). Thus, increasing diversity requires considering jointly multiple levels of biodiversity (i.e., genes, population, or community). To date, breeding programs have had difficulty deriving value from the benefits of inter- or intra-crop mixtures due to the few traits that they consider (Litrico and Violle 2015). In contrast, breeding programs have aimed for the standardization required by the food supply chain.
The genetic basis of “ability to co-exist” traits for all major crops requires renewing methods and criteria in selection programs (Sampoux et al. 2020). Co-existence traits are crucial to breeding programs that aim to foster diversification since they enable plants to share and adapt to the environment (Hill 1990; Hinsinger et al. 2011). However, cultivar performances in pure stands are rarely identical to their performances in plant mixtures because demand for a particular resource can outstrip the supply, thus leading to a shortage of resources. This difference is sometimes observed under agroecological practices such as direct drilling or conservation agriculture (Peltonen-Sainio et al. 2009; Sampoux et al. 2020). Thus, combinations of specific ecological activities, as close as possible to agroecological systems, should be considered as breeding criteria, even though they complicate the design of experiments and related statistical methods (Hill 1990). Emerging translational biology, comparative biology, and plant community ecology can provide new insights into target plant traits that must be implemented to cultivate species in diversified and pesticide-free agroecosystems.
Integrating the variety of pesticide-free practices and the environment in breeding
Current breeding programs create productive cultivars, but their productivity remains conditioned by agricultural practices. Indeed, the expression of genetic potential, which defines the genetic yield potential, depends on pesticide, water, and nutrient inputs, especially since breeding is performed for standardized cropping systems. Therefore, when the availability of water or nutrient is not synchronized with the plant needs, the genetic yield potential can be reduced, making observed yield lower than potential yield. This yield gap can sometimes be observed when certain agroecological practices, such as direct drilling or conservation agriculture, are implemented (Peltonen-Sainio et al. 2009; Voss-Fels et al. 2019). Developing new practices to eliminate pesticides can also lead to this situation; thus, more research is needed to include these new practices in breeding. However, beyond the practices, a crop’s direct environment should be considered when breeding new varieties. Indeed, the genotype × environment × management (G × E × M) equation of the breeder’s objective is to derive value from genetic resources in the face of environmental heterogeneity (Prieto et al. 2015; Litrico and Violle 2015; Meilhac et al. 2019). Following this perspective, participative breeding should be developed. Indeed, farmers could be part of the breeding innovation (Berthet et al. 2020). First, participative breeding help preserve in situ genetic resources under climate change and innovative practices and then address evolving genetic capacities in addition to ex situ approaches (Hawtin et al. 1996). The reproduction and selection on farm allow for a continuous evolution and adaptation of crop populations in response to natural selection and selection performed based on desired characteristics defined by site-specific conditions or practices. Second, through seed exchanges, crosses, or mixtures, participatory breeding could foster genetic diversity. Accordingly, innovative programs combining breeder’s and farmer’s selection approach can contribute to the release of new varieties to solve the (G × E × M) equation (Dawson and Goldberger 2008). While promising, such new approach of breeding raises new issues dealing with evolutionary processes and organization leading to a certain unpredictability that can be overcome with an efficient dialogue with all tenants (stakeholders, farmers, researchers). In particular, developing predictive models based on data-driven approaches, assisted by new mathematical and statistical learning methods, and on crop models may provide credible genotype responses to the environment and management practices (Messina et al. 2020; Cooper et al. 2021). This modeling approach, or in silico trials, can also benefit from innovations in agricultural machinery by including data captured by sensors and digital agriculture mapping to broaden analysis to a wider range of soil and climate conditions.
Broadening the scope of breeding by integrating interactions with soil and microorganisms
In addition, little research on lasting effects of plant legacies through complex plant–soil feedback has been performed, even though plant ecology has demonstrated the latter’s benefits for crop protection (Putten 2003; Wang et al. 2017). Plants influence soil biota, including pathogens, directly through root exudation or by modifying nutrient and water availability, and indirectly through litter fall. These organisms in turn can influence plant performance either positively or negatively. Domestication and breeding select the most productive species with resource-acquisition traits, thus neglecting other plant functional traits. Extending plant-trait approaches to soil biota and including them in breeding programs is a promising research front, especially since agricultural systems make it possible to choose crop species and varieties (Mariotte et al. 2018). Accordingly, unexpected benefits could be included in farmers’ assessments of new diversification crops, especially when improvements in soil quality (e.g., soil structure) are observed with fewer external resources or a smaller workforce. Dedicated research should address such complex plant–soil feedback. In particular, it would be interesting to distinguish individual drivers induced by plants and their interaction with nutrients, exogenous inputs, and pests. To do so, experiments under both controlled and field conditions are needed. Finally, interfaces between plants and their environment must be monitored to take advantage of this progress. Accordingly, sensors or new indicators that complement soil quality and fertility indicators (e.g., plant rhizosphere indicators) must be developed.
Future plant-breeding programs should focus on plants’ ability to steer their microbial communities as a heritable trait to deliver the next generation of microbe-improved plants (Gopal and Gupta 2016). Indeed, promising research consists of considering a plant as a super organism, a holobiont, composed of the plant itself and its microbiome (Vandenkoornhuyse et al. 2015; Agnolucci et al. 2019; Bailly et al. 2019). Doing so would enable simultaneously breeding crops and their associated microorganisms and/or plant traits that promote beneficial microorganism interactions. Considering microbe genes in addition to a host plant’s genome would thus increase the plant's ability to cope with abiotic and biotic stress (Berendsen et al. 2012; Liu et al. 2020) and changing environments (Classen et al. 2015). To address these objectives, the discrete interplay between plants and microbes must be understood better. In particular, research should focus on distinguishing function versus microbial diversity relationships, as well as the influence of rare taxa or strains that define the satellite microbiome in addition to the core microbiome (Jousset et al. 2017).
Beyond the technical aspects of multi-trait phenotyping, registering microbe-improved plants is a burden for breeders according to current mandatory criteria, such as distinctness, uniformity, and stability, that define the concept of a variety (Louwaars 2018; Jamali et al. 2020). International and national policies for registering new varieties based on performance in high-input systems should be renewed by initiating research on new criteria. Beyond microbe-improved plants, this change could also enable value to be derived from participatory breeding and consideration of a crop’s direct environment in breeding. However, this would not be possible without the engagement of policy makers and relevant stakeholders (e.g., research centers, breeding companies, farmers’ unions).
In addition, breeding programs have inadvertently selected plant traits that impair the ability of plant communication to recruit and select beneficial microbes compared to that of wild types or wild relatives (Berendsen et al. 2012; Pérez-Jaramillo et al. 2016, 2018). One known example is the inability of elite wheat varieties to develop interactions with several mycorrhizal fungi of great importance in capturing potassium or phosphorus and fostering healthy plant growth. Because these genetic abilities were present in ancient cultivars, they could be reintroduced into modern varieties (Jacott et al. 2017; Sawers et al. 2018). Finally, facilitating effective interdisciplinary research among plant geneticists, ecologists, and agronomists in charge of cropping system design is crucial to reveal de novo solutions for agriculture. This kind of holistic approach is essential due to the complex multi-trophic and aboveground–belowground relationships in agroecosystems (Kostenko et al. 2012; Dias et al. 2015; Wurst and Ohgushi 2015; Mariotte et al. 2018; Li et al. 2019). Altogether, managing the plant microbiota through appropriate management practices and crop management design can be considered to influence agroecosystem health (i.e., “One Health”) and, by extension, socio-ecological systems (i.e., “EcoHealth”, as defined by Mi et al. 2016).
Setting new goals for agricultural machinery and digital technologies
Developing equipment adapted to agroecological practices
Currently, most agricultural machines are adapted to cropping systems that rely on pesticide use. This choice has influenced field size and has ultimately shaped landscapes (Jepsen et al. 2015). Current machines are thus adapted to large fields and were designed to optimize pesticide use (e.g., precision of application, high speed to benefit from periods when pesticides can be applied) (Smith 2018; Berenstein and Edan 2018). Most machines are designed to have curative action against pests, in particular as a substitute for herbicides, but they do not use much data, which allows for targeted and automated action. The development of precision agriculture opens up the possibility of managing pests and diseases by mechanical actions. However, the vast majority of precision farming applications consists of optimizing the use of pesticides, and this is therefore part of the current paradigm relying on pesticides (Gossen and McDonald 2020). Overall, development of mechanized prophylaxis remains limited. More research on big data and machine learning would improve pest detection, monitoring practices, and crop health (Ip et al. 2018; Korres et al. 2019). It would advance the design of equipment and thus enable non-chemical agricultural management decisions to be tailored in time and space (Bongiovanni and Lowenberg-Deboer 2004; Finger et al. 2020). In particular, new technologies enable knowing exactly where crops are located within a field in order to spare them, while controlling the rest of the cultivated space (Liu et al. 2019). For example, at the field scale, controlling the location of seeds precisely using GPS makes it possible to hoe between rows and within each row, thus eliminating the need for herbicides (Griepentrog et al. 2005). Intercropping is a highly effective technical lever for managing pests without pesticides (Stomph et al. 2020), with several biological and ecological processes involved in this control (Ratnadass et al. 2012). Yet they often require specific machinery to sow (as diverse as alternating rows of each species, sometimes at different depths, mixed rows or relay-cropping) or to sort the harvested products, thus limiting their extension. In addition, robotics is a tool to replace human labor for the most tedious tasks, such as weeding, or to perform actions to combat pests (Fig. 5). For example, aphids can be vacuumed up not only to monitor their populations but to help maintain them at low densities (Belding et al. 1991; Schmidt et al. 2012). Indeed, development of preventive robotics may solve several limits of the present situation, in particular the slowness of robots: if the robot’s objective is to decrease pest pressure by removing contaminated plant parts, high speed is not essential. At another stage of the value chain, innovations should improve sorting abilities in order to facilitate processing of grain harvested from intercrops (Meynard et al. 2018). This is also relevant when crops are interlocked on the same field (e.g., living mulch) without being intended for harvest (Wortman et al. 2012). Overall, the equipment of these innovations must cover the needs of main crops and diversified crops at low cost.
Promoting the adaptability of the equipment to a variety of environments
Current equipment is highly standardized and lacks adaptability: it is designed to cover the needs of farmers with large farms, which tends to increase machine size and power (Kutzbach 2000). This trend has contributed to the intensification and standardization of agroecosystems, characterized by the same dominant crops around the world. To benefit from natural regulation, however, pesticide-free agriculture will require developing smaller machines, adapted to smaller fields and local conditions. Research on the adaptability of equipment must thus be developed. This can be done in two ways, which can coexist. Smart machines should be developed that self-adapt to local conditions using embedded sensors (Berducat et al. 2009). This self-adaptation could relate to navigation, speed, or the precision of action (Tisseyre 2013). In comparison, self-built machines should be designed from open-access knowledge to provide new opportunities for farmers (Joly 2017). Indeed, in addition to limiting individual purchases of high-tech but expensive equipment, some machinery cooperatives have developed their own equipment or provided “fablabs” in which farmers can make their own modifications. By doing so, they can simultaneously redesign their cropping system and equipment, which therefore become adapted to the local context and the farmers’ specific needs (Salembier et al. 2020). In parallel, research should focus on economic models that would support production of small series of equipment by small and medium enterprises.
Improving in-field epidemiological surveillance through innovative monitoring tools
Current decision-making tools are dedicated mainly to supporting curative rather than preventive agronomic practices. In particular, information about the risk of crop loss delivered to farmers is based mostly on the weather forecast only and is not influenced by preventive actions that farmers could have taken. More research should be developed on combining monitoring and prediction tools that consider and support preventive agronomic practices (Rossi et al. 2019). Indeed, efforts are currently underway to adapt decision-making support to the specific characteristics of biocontrol (Giles et al. 2017), but other innovative tools should also be developed. Technological advances in sensors, the “Internet of Things” and big data processing could together provide the ability to quantify and consider subjective or measured probabilities of pest occurrence or crop loss. Doing so could reduce farmer uncertainty, particularly by developing systemic decision-support and design-support tools that ease strategic decisions built on preventive practices. Decision-making tools could also be improved by combining farmer perceptions of risk and economic utility (Gent et al. 2010).
In addition, epidemiological surveillance must be expanded by generalizing monitoring methods (Sankaran et al. 2010). Indeed, epidemiological surveillance seldom provides information about the potential of natural regulations to control outbreaks of a given pest, which would thus allow farmers to avoid a pesticide treatment. In pesticide-free agriculture, epidemiological surveillance should include a wide variety of organisms, from pests to auxiliary organisms, to provide valuable information about potential natural regulation at a large scale. Research should thus focus on monitoring methods to improve and extend in-field epidemiological surveillance. In particular, the next generation of networked sensors should be designed using molecular assessment to model epidemiological risk and share metadata with stakeholders (Mahlein 2015). For example, sensors based on insect pheromone receptors are promising tools that could provide early warning of invasive insect pests (Tewari et al. 2014). Other types of sensors include molecular assessment that uses nanotechnology systems such as lab-on-a-chip devices: they could provide a promising option for effective detection and analysis of diseases caused by microorganisms (Martinelli et al. 2015; Kashyap et al. 2017). To do so, breakthrough innovations in biocontrol are expected to provide detection and recognition of insect pheromones, as mentioned (Sect. 3.2) (Conchou et al. 2019). Beyond sensors, development of big data will increase transparency of production processes by enabling traceability, in particular of input use (Finger et al. 2020; Fielke et al. 2020). By doing so, policies may become more effective due to lower transaction costs between farmers and authorities (OECD 2019). It can also lead to the development of dedicated agri-food chains that derive value from low-input farming through price bonuses and thus pay farmers for using more sustainable practices (Choe et al. 2009).
Expanding monitoring areas by including non-agricultural reservoirs
Finally, epidemiological surveillance is still limited in space (i.e., cultivated fields), time (i.e., short term), and purpose (i.e., pests). Indeed, current epidemiological surveillance relies on direct observation of pests and specific data from relatively short-term events within or next to cropped fields. It therefore does not consider inoculum reservoirs or the presence of auxiliary organisms in non-agricultural areas. However, the recent concept of One Health asserts that most new animal and human diseases come from disturbed natural environments that are reservoirs of disease vectors (Cunningham et al. 2017). Research on expanding the One Health paradigm to crop production is thus an interesting option. Expanding this concept of plant disease epidemics would involve monitoring risk factors for the proliferation of pests by including non-agricultural reservoirs within epidemiological surveillance (Morris et al. 2009) to detect pests as early as possible and thus optimize the preventive approach necessary for prophylaxis. In addition, it would be interesting for epidemiological surveillance of plants, animals, and humans to share at least some of the technology to compare their results and improve prevention and forecasting abilities (Zinsstag 2012; Davis et al. 2017). Effectively integrating the plethora of potential indicators from smart sensors, social networks, digital maps, and remotely sensed imagery would enable the next generation of epidemiological models to be developed and innovative tools that support decision-making by farmers and other stakeholders to be created (Rapport et al. 1998). Overall, the next generation of agricultural equipment should facilitate implementation of preventive actions: in an integrative way, sensors and the sensor-machine interface must work on connecting epidemiological risk and the actions of machines designed to decrease risks due to pests.
Implementing public policies and private initiatives for the transition toward pesticide-free systems
Improving the effectiveness and acceptance of public policies
To date, pesticide-reduction policies have fallen short of expectations, and reasons why more effective ones have not been developed must be determined. One explanation is that most policies are designed independently of each other, especially environmental and agri-food policies. Some policies target pesticide reduction while others still support current production systems. Furthermore, agricultural policies do not address food issues, even though the agroecological transition should involve the entire food chain. This is clearly the case of the EU’s Common Agricultural Policy, which has failed to include pesticide issues in its instruments and to connect food issues to agri-environmental issues (Guyomard et al. 2020). Several studies confirm that policies must be combined to achieve convincing results (Lee et al. 2019; Guyomard et al. 2020; Möhring et al. 2020b). Thus, research should focus on cross-effects to combine policies, including food policies, more effectively and to identify potential synergies (Pedersen et al. 2020). Progress should also be made to combine more effectively the types of public policy instruments that can be implemented to reduce pesticide use: regulatory, economic, and informational (Vedung 1998).
To encourage implementation of these policies, one fundamental rationale is the hidden costs of pesticides. Indeed, impacts of pesticide use on the environment and health lie at the source of costs (e.g., health costs, pollution-control costs) borne by private and public stakeholders. These costs can be associated with “negative externalities.” They are difficult to assess, and only a few studies on this issue are available (Bourguet and Guillemaud 2016). New methods should be developed to ease and standardize this assessment. Specific research projects should focus on this issue by developing a multi-disciplinary framework that integrates epidemiology, ecology, and toxicology, in particular. These research projects should be closely related to the practices currently used in the field, in particular how farmers apply pesticides (e.g., climate conditions, equipment) and protect themselves (e.g., protective equipment) (Garrigou et al. 2020). Such research would ease the social acceptance of policies while potentially accelerating changes.
Fostering collective actions at the landscape scale
The limited impact of agri-environmental policies can be explained by their focus on individual farmers. Recent studies showed that changes in practices depend not only on individual actions but on the wider context (Schoonhoven and Runhaar 2018). In particular, adoption of innovative practices to reduce pesticide use can be encouraged by collective approaches in which the sharing of experience with peers (i.e., other farmers perceived to be like-minded) is essential (Chantre et al. 2015; Bakker et al. 2021). Thus, research on spatial and collective mechanisms is needed to drive transition to pesticide-free agriculture. Innovative instruments should be designed to target not only individual farmers but also groups (e.g., farmers, other stakeholders involved in territorial initiatives), while addressing the issue of “free riders” who may defect from the common strategy. Among these instruments, “nudging” is a promising tool that uses various types of psychological bias to favor targeted decisions. For example, nudging implemented through a conditional collective bonus can create a pro-environmental social norm that encourages farmers to reduce pesticide use (Kuhfuss et al. 2016). Nonetheless, further research should better define the characteristics of such policies to ensure their effectiveness and foster their implementation.
Supporting farmers’ innovation networks
In the EU, farms’ economic structures are increasingly capital-intensive. This issue is closely related to demographic changes in the agricultural sector: the number of farmers is decreasing, which tends to increase the size of farms and encourages simplification of crop management and the search for increasing productivity per worker (European Commission 2017b). At the same time, the outsourcing of agricultural activities to dedicated companies is increasing, and these companies are more inclined to use conventional practices that do not lead to a reduction in pesticide use (Nguyen et al. 2020). More research on economic models of farms and their pesticide use is needed, in particular regarding workload and their compatibility with transition to pesticide-free agriculture. Indeed, practices that tend to reduce pesticide use are generally considered to be more labor intensive and to require more complex work organization and more skilled labor (Bowman and Zilberman 2013). Since some authors disagree with this assertion (Lechenet et al. 2014), it is necessary to investigate this problem and better understand the constraint of work organization in pesticide-free cropping systems.
In contrast, some farms have already started transitioning toward a strong reduction in pesticides. These farms represent examples to follow, and dissemination of their innovative practices, or of the knowledge derived from these innovations, must be facilitated. To do so, it would be appropriate to support innovation networks and web platforms that foster information exchange and innovative tools between farmers (Sacchettini and Calliera 2017). These innovation networks can focus on specific local conditions, for example through living labs, or be designed to reach a wider audience by relying on digital tools such as dedicated forums (Maria et al. 2021). Indeed, innovation to achieve pesticide-free agriculture cannot be restricted to top-down processes, from research to farmers, but should also enhance the knowledge and discoveries of those working in the field (Fig. 6).
Renewing extension services and training
Extension services to farmers have been largely privatized and fragmented in the past decade (Wuepper et al. 2020), and this tends to encourage pesticide use instead of developing preventive measures (Pedersen et al. 2019). Furthermore, extension services, both public and private, provide generic tactical advice at the field scale rather than strategic advice that is co-produced with farmers for specific needs and conditions (Labarthe and Laurent 2013). Thus, research should provide knowledge and innovative organizations to support extension services so they can provide strategic advice at the scale of the entire cropping system, or even at the territory scale, while facilitating exchanges between farmers to promote participatory innovation (MacMillan and Benton 2014). Beyond training farmers, the education of young people who wish to pursue a career in agriculture must be revised. Whether in high schools or universities, training is often disconnected from the latest systemic innovations. A stronger connection between research and teaching is therefore necessary, as is a more interdisciplinary curriculum, mixing for example crop sciences, animal sciences, ecology, and economics (Hilimire et al. 2014).
Paying farmers for pesticide-free practices
Beyond the effectiveness of current policies, more ambitious policies to eliminate pesticides must be developed, in particular by paying farmers who use pesticide-free practices. Indeed, the expected redesign and innovations described previously may not be effective immediately after they are implemented: crop yields may decrease due to the removal of pesticides and costs may increase, in particular labor costs. This phenomenon could be temporary, lasting only during a transition period during which natural regulations are not yet established, or more permanent. Payment should thus be offered to farmers who lose income. If the decrease in productivity is permanent, farmers should receive compensation that corresponds to the public goods produced by pesticide-free agriculture (e.g., increased biodiversity), through subsidies or a better added value of products thanks to a specific label implemented by downstream stakeholders. In addition, other types of subsidies could help farmers invest in new equipment for their fields or in landscape infrastructure.
Large-scale transition to pesticide-free systems will, however, require significant public spending to fund these subsidies. Financial resources could come from taxing pesticides, which economists often mention as the most effective tool to decrease pesticide use (Finger et al. 2017). However, several studies have shown that the tax rate must be high for taxation to have a substantial influence (Skevas et al. 2012; Femenia and Letort 2016). These taxes would burden farmers economically, but redistributing tax revenues could increase the acceptability of taxes and effectively support the transition toward pesticide-free practices (Finger et al. 2017). Taxation would be a valuable tool to decrease the loss of profitability for farmers, foster political acceptability, and thus guarantee a smoother transition to pesticide-free agriculture.
Promoting the coordination of stakeholders to foster pesticide-free food chains
The market can contribute to offset the lower profitability of pesticide-free practices by increasing the added value of agricultural products and considering consumers’ willingness to pay. Indeed, shifting toward pesticide-free food chains requires implementing new strategies and reorganizing agri-food chains, from raw production to consumption, including downstream sector (e.g., marketing and processing) (Meynard et al. 2017). Beyond the well-known issue of diversifying crops in agri-food chains (Magrini et al. 2016; Meynard et al. 2018), research on relevant differentiation strategies for food products is needed to foster transition. Several studies show coordinating private stakeholders by fostering contracts between farmers and retailers can help these chains and products to develop. To ensure that they are effective, however, it is necessary to (1) provide long-term commitment (Möhring et al. 2020b), (2) provide technical advice to support the transition (Cholez et al. 2020), and (3) develop a marketing approach that informs consumers (Bazoche et al. 2014). In parallel, developing traceability and tracking tools for consumers will enable labeled products to be developed. By doing so, private stakeholders could become drivers of change: such tools take advantage of consumers’ greater willingness to pay for pesticide-free products and provide a price bonus to farmers who meet these specifications (Florax et al. 2005).
Public and private initiatives to support farmers’ income are particularly important since farmers do not consider positive externalities of pesticide-free practices, whether internal (e.g., that influence management of beneficial organisms on their farm) or external (e.g., on bees or aquatic organisms), in their decision-making. To consider these elements better, research should also help develop indicators and methods that can help farmers and their advisors consider ecosystem services. In particular, developing new economic accounting tools that include innovative indicators that highlight ecosystem services and consider multi-year practices is a promising research area.