Abstract
Soils are the backbone of terrestrial ecosystems, underpinning their biodiversity and functioning. They are also key to agricultural production and ecosystem development. Although focus on effective and profitable food production has led to severely degraded soils, the tools and standards for restoration strategies in agricultural soils are still largely underdeveloped. In this review, we summarize recent developments in ecological restoration practice for soils, evaluate whether these are in line with ecological theory, identify where they could be improved, and contextualize these to agricultural soil restoration. We identify restoration actions and success indicators that may best foster sustainable use of agricultural soils while also increasing their multifunctionality, that is their ability to simultaneously supply multiple ecosystem services including provisioning food and feed. Lastly, we explore actions available to improve soil health and focus on tool and indicator implementation. Calls for reductions in provisioning services, such as yield production, commonly used in ecological restoration practices conflict most directly with wider soil-ecosystem-service-focused restoration actions, including supporting and regulating services. Comprehensive restoration actions harnessing the interdependence of multiple soil properties, including contribution to vegetative yield, appear to be most efficient in agricultural settings with a central role of soil biodiversity in ecosystem service provisioning.
Subject terms: Restoration ecology, Agroecology
This review on soil restoration in agricultural systems suggests comprehensive restoration actions harnessing the interdependence of multiple soil properties, including contribution to vegetative yield, to be most efficient in agricultural settings.
Introduction
Human activities including land use expansion and intensification have degraded ecosystems worldwide. This has threatened their biodiversity and supply of ecosystem services1,2. In response to this, the United Nations recently prioritized the restoration of degraded ecosystems to secure the supply of renewable resources (UN Decade of Restoration 2021–2030, Proposal for an EU Nature Restoration Law)3,4. The targets are ambitious, aiming for restoration of 20% of land and sea area by 2030, and the commitment to restore all ecosystems by 2050. This requires large-scale restoration based on effective restoration strategies.
Traditionally, ecosystem restoration has targeted re-establishment of a ‘pristine’ reference ecosystem according to the definition of ecosystem restoration by the Society for Ecological Restoration5. This reference is often only defined by basic abiotic properties and a few key community indices such as plant species composition. Scientists, stakeholders, and politicians, however, agree that we need broader restoration goals if we are to properly measure restoration success6. This is especially the case for restoration guidelines for ecosystems such as agricultural soils where severe former or continued disturbance disables returning the location to a pristine reference ecosystem7. Therefore, recent restoration guidelines have incorporated wider ecological theory and have begun to integrate other ecosystem properties as targets, including trophic interactions, ecosystem functioning and ecosystem service provisioning8. Such aspects are increasingly recognized as relevant indicators of ecosystem condition (‘ecosystem health’), among scientists, stakeholders, and politicians (e.g. Sustainable Development Goals)4,9–11. However, application of these broader or extended goals is still nascent.
Soils constitute the backbone of all terrestrial ecosystems, and therefore underpin their biodiversity and ecosystem service supply12,13, making them a vital component of any comprehensive ecological restoration programme14–16. Soils are therefore increasingly included into restoration programmes, but a standardized approach based on ecological theory is still largely missing17. This is problematic, particularly in agroecosystems. Since the ‘newest agricultural revolution’, agricultural soils have been vital for optimisation of provisioning services while receiving marginalized soil conservation and restoration measures, which has led to alarming levels of soil degradation globally18,19. There is, thus, an urgent need to develop ecological restoration practices customized to agricultural soils, especially if we are to simultaneously meet the UN Sustainable Development Goals of zero hunger, clean water and sanitation, climate action, and life on land19–21.
Ecological-theory-informed restoration offers a potential to help reverse soil degradation10 and create sustainable agricultural soils that are not only resilient to climate change, but also form part of a robust, healthy landscape19,22. In this article, we provide an overview of how restoration actions informed by ecological theory can be effectively applied in agricultural systems. We further discuss the synergies and trade-offs between restoration for soil sustainability and short-term production and yield and by doing so, aim to pave the way for a more comprehensive approach to ecological restoration, which integrates and acknowledges the multifunctionality of soils and offers solutions and tools to reverse the degradation of soils in agricultural systems.
The broad conclusion our review offers is that many of the reviewed restoration approaches and practices are known (e.g. intercropping or vegetation diversification) and the only change that must be implemented is that the goal of reversing soil degradation should be included as a decision criterion. This will allow the addressing of potential trade-offs between different restoration and production goals, as well as an expansion of understanding towards the combined effects of multiple restoration actions on individual soil properties and functions, and ultimately soil multifunctionality. Further research, however, is needed regarding the combined effects and interactions of single restoration actions23,24, as well as the socio-economic and social factors mediating motivation and acceptance towards soil restoration in agricultural lands25–27.
The need for soil restoration in agricultural systems
Agricultural soil degradation has resulted from a prior focus on one function in these systems: productivity28. This has caused intense soil erosion, soil compaction, soil contamination, and loss of soil biodiversity and soil organic matter21. For example, soil disturbance due to frequent, heavy-machinery tillage and ploughing results in soil physical property changes29, increased soil compaction, disrupted microhabitats, and interrupted organism life cycles, which ultimately all negatively impact soil biodiversity, simplify soil food webs30,31 and lead to soil degradation. Individual causes of soil degradation must be reversed if soil is to be restored. However, we lack standardized strategies for addressing these challenges and tools for assessing the outcomes of restoration on soil quality and soil-based ecosystem services4,9,11.
Successful soil restoration strategies need clear goals to select appropriate restoration actions and indicators to monitor the restoration success4,7. We suggest that concurrently identifying agricultural impacts on soils and soil restoration goals within the ecosystem service framework may be useful here, as it allows us to find synergies and trade-offs between provisioning and other ecosystem services provided by agricultural soils17. Ecosystem services are often linked via shared underlying drivers (e.g.32), and these links should be acknowledged in ecosystem restoration. Ecosystem services are defined as the benefits people obtain from ecosystems and are commonly divided into four groups33. The first group is (i) supporting services such as soil formation, photosynthesis and nutrient cycling that can be understood as ecosystems’ basal capacity to function. Supporting ecosystem services such as nutrient cycling or soil formation reinforce many other ecosystem services32,33. Thus, ecological restoration of agricultural soils should prioritize these supporting services due to their strong links to other services. The three other groups of services, reinforced by supporting services are (ii) regulating services such as climate, water, pest regulation, that can be understood as the capacity of an ecosystem to regulate ecosystem processes and to buffer against environmental changes; (iii) provisioning services such as food, fibre, timber and water that can be understood as ecosystems’ capacity to provide people with resources; and (iv) cultural services such as flower diversity and landscape structural diversity that can be understood as ecosystems’ capacity to provide recreational, aesthetic and spiritual benefits.
Restoration strategies also require indicators of the degree of soil degradation and restoration success34,35. Soil quality and its associated soil properties might serve as a good indicator36. Soil quality is defined in terms of inherent soil physical, chemical and biological properties, which depend on parental material, topography, climate and hydrology, but also dynamic properties, i.e. those that change over short timescales37–40. This latter dynamic aspect of soil quality is often referred to as soil health and includes the biotic component of the soil41. The concept of soil health is closely related to that of soil multifunctionality (i.e. the simultaneous good functioning of multiple soil functions, or the supply of multiple soil services at different hierarchical scales). In most soils, soil health is largely governed by ecological processes mediated by soil microbial communities (e.g. organic matter decomposition or nutrient cycling). Hence, restoration measures for soil health should capture biotic aspects of soil quality including soil microbial community characteristics (diversity, composition) and microbially mediated ecosystem process rates and trophic interactions36,42 although these are sometimes complex to measure36. However, we also acknowledge that focus on soil quality measures needs to change depending on the restoration goal, i.e. the most appropriate bundle of desired ecosystem properties and services for certain sites or landscapes may not be widely applicable43,44.
Five goals of soil restoration
To foster comprehensive ecosystem restoration strategies that can be applied to agricultural soils, we propose five soil restoration goals. We centre these on soil supporting services as these underpin multiple soil services, making them universal. The goal of restoring soil supporting services requires a wider selection of restoration success indicators beyond the physical and chemical soil properties typically measured in vegetation-centred restoration5 and should also capture biological soil properties42.
Our five proposed restoration goals, each linked to a success indicator and a method to quantify restoration success (Fig. 1, Supplementary Table S1), are:
Fig. 1. Conflicts between goals of soil restoration and agricultural production mediated by restoration actions and their impact on ecosystem properties (i.e. the restoration success indicators).
Restoration goals are i) improve soil quality, ii) improve soil health (i.e. soil multifunctionality), iii) harness the soil biodiversity-ecosystem functioning (BEF) relationship, iv) acknowledge the soil-vegetation interdependence and v) restore soil health at the landscape-scale (i.e. apply all restoration goals the local and landscape-scale). Agricultural goals are the desired ecosystem services i.e. provisioning services (crop & material production), the regulating services (resource-use efficiency) and the supporting services (soil health and the associated stability in production). Cultural services are commonly of less focus and are thus left out here. Impacts of restoration actions on restoration success indicators (i.e. soil and wider ecosystem properties) and their impact on ecosystem services are assumed to act immediately i.e. to be short-term. On the contrary feedback loops between supporting, regulating and provisioning services are assumed to be long-term, as soil formation processes are slow. The selection of listed restoration actions are those suggested by the group of authors (stemming from different disciplines of soil and restoration ecology) and recent publications of the topic to improve the most pressing soil threats suggested by the FAO (OECD FAO21) and reach the restoration goals suggested by this review. The list of restoration actions albeit not exhaustive should reflect the most straightforward and most applied soil restoration actions. Supplementary Table S1 provides a detailed compilation of the underlying statements and references supporting the linkages shown. Created in BioRender. Hannula, E. (2023) BioRender.com/s92u661.
1) Increase soil quality
Restoration actions should aim to improve the physical, chemical, and biological quality of soils45. With respect to physical soil quality, restoration efforts should focus on reduction of soil erosion and compaction46 leading to increase in functions such as water-holding capacity and soil aeration. Soil restoration strategies therefore should include measures to increase (temporal and spatial) vegetation cover and limit heavy agricultural machinery and other soil disturbance (see also for further measures47–49): Vegetation cover and bulk density are often used as indicators of soil restoration despite not representing all the (often more microbial mediated) factors known to be indicative of good soil physical properties, e.g. aggregation and macropore formation42,50. Regarding chemical soil quality, restoration measures should target reduction of mineral fertilizer application and prevention of salinization, e.g. through regulation of nutrient inputs and appropriate water management45,46. Accordingly, nutrient leaching rates could be a good indicator of chemical soil quality. Ecological restoration of biological soil quality should enhance soil organic matter46 and soil biodiversity51. This can be achieved by increasing carbon inputs to soil, improving conditions for soil organisms (e.g. through reducing soil disturbance52), or via inoculation with desired soil organisms51,53. Increasing carbon inputs includes the use of cover crops, adding carbon-dense substrates (biochar, compost) and tree planting in agroforestry systems45. Soil organic matter content is therefore a good indicator of soil biological quality and may also serve as a proxy for biodiversity45,54.
2) Increase soil health
Soil health, possibly measured as soil multifunctionality, encompassing many ecosystem processes should be included as a goal of soil restoration programmes4,9,48,55. Soil functioning, as an indicator of health, can be well-characterized by measuring process rates, such as nutrient and carbon mineralization56,57, rates of enzymatic activities or microbial respiration and carbon use efficiency36,58. A composite measure of these process rates can then serve as an indicator of soil multifunctionality, although the aggregation of process rates into a composite measure needs to be appropriate to the specific restoration context44. For instance, high process rates often accompanied by active microbiome can represent high nutrient cycling rates, but could also correspond to high nutrient leaching and soil carbon losses.
3) Harness the soil biodiversity-functioning (BEF) relationship
Restoration measures should build on the principle and evidence that soil biodiversity enhances many also above-mentioned soil functions including soil structure, water regulation, nutrient cycling, and carbon dynamics31,59–62. This goal can be reached by focusing on restoration of soil biological quality (see restoration goal 1), further underlying the relevance of soil life in ecosystem restoration61. Organic matter content may again serve as a good proxy of both soil biodiversity and functioning, as it promotes soil quality, and biodiversity45,54.
4) Acknowledge the interdependence of vegetation and soil
Soil biodiversity can be influenced by modifying the vegetation, e.g. enhancing or diversifying vegetation cover15. In agroecosystems, this can be done both in spatial (increase in plant species) and temporal scales (widening rotations). Increase in vegetation cover is a powerful measure to prevent soil erosion, increase organic matter content, and improve soil structure63. Diversification of the vegetation is associated with a greater diversity of soil organisms that interact with plants (e.g. mycorrhizal fungi64) and the associated chemical diversity of dead plant residues (e.g. saprotrophic fungi65), and can ultimately lead to higher soil functioning56,65,66. Targeted addition of substrates (wood, manure, plant litter) and soil inoculations with plant-beneficial soil organisms like mycorrhizal fungi can also steer soil communities and their associated functions51,53,67,68. Since plant-soil interactions and impacts on soil functions depend on the environmental context, on surrounding plant and soil community compositions and on co-adaptation forces69, inputs of foreign plant and soil material as restoration measures should be performed with caution (e.g.70), In summary, vegetation cover and vegetation diversity both in time and space might serve a good indicator of the interdependence of vegetation and soil.
5) Restore soil health at the landscape-scale
Intensive land use is one of the major factors degrading soils, and reduced land-use intensity is needed to restore them71. Often the reduced land-use intensity shows a trade-off with provisioning services. However, restoration at the landscape-scale can reduce this trade-off by promoting soil health through suitable land management in the surrounding of the agricultural site. Measures reducing dispersal limitation and enhancing spill-over effects from the surrounding landscape can enhance local soil biodiversity, soil quality and processes underpinning several belowground supporting and regulating ecosystem services (e.g. soil aggregation, carbon storage, nitrogen and phosphorus retention, nitrification, and water recharge)72. Land-use permanency and cover of grasslands and forests at regional scale promote local soil biodiversity and regulating services and thus might serve as a good proxy of landscape-scale support to local soil health at agricultural sites72,73.
Aligning soil restoration with agricultural production goals
The potential for synergies and conflicts between agricultural production and ecological soil restoration (Fig. 1, Supplementary Table S1) requires management. Depending on the prioritized goal(s), specific restoration actions may be chosen. Regardless of the main goal of basic functioning, healthy soils supporting all other desired ecosystem services of interest (ref. 54, Sustainable Development Goals), particular focus on the desired ecosystem services will inevitably lead to specific priorities that then create conflicts (e.g. ref. 43, Fig. 1). The main source of conflict is the focus on provisioning soil services, i.e. the productivity and profit needs of the agricultural sector54 and the restoration focus on broader supporting and regulating services, i.e. ecosystem-centred profits and linked land-use/restoration practices4. This conflict also arises due to different time-scales at work in agriculture and restoration. High levels of agricultural productivity ask for short-term needs and solutions, which conflicts with restoration goals as ecosystems require longer timescales for improved soil supporting services to cascade down to improved provisioning and regulating services74 (Fig. 1). At the same time, spatial and temporal configurations exist where restoration and agricultural management actions can complement each other, e.g. when restoration actions increase soil fertility43,74. We stress that only by assessing the potential synergies and conflicts generated by these underlying goals and associated agricultural-restoration actions, a solution to combine provisioning and ecosystem restoration can be found. Here we present a soil restoration framework that explores the synergies and trade-offs between soil restoration and agricultural production goals and propose associated actions based on available literature (Fig. 1, Supplementary Table S1).
Towards soil restoration goal 1: agricultural restoration for soil quality
Restoration of soil physical quality requires management extensification to reduce soil erosion and compaction through practices like increasing vegetation cover, reducing the use of heavy machinery, and reducing soil disturbance. For example, vegetation cover can be increased by cover cropping and reduced weed management, however, as a trade-off cover-crop management adds extra labour and enhanced weed cover might reduce yield due to crop plant competition with weeds75 (but see ref. 76). Similar increases in extra labour occur when lighter machinery is used or cropping cycles are reduced to limit soil disturbance77. The goal of improved soil quality would, however, benefit from all three aforementioned practices and could have potential indirect positive effects on the agricultural goals of productivity and resource efficiency. Reduced soil management allows for development of stable soils with higher organic matter content, and better capacity to support water- and nutrient cycling (e.g. less demand for mineral fertilizers would arise, due to enhanced nutrient mineralization)47,71,78, increasing profitability of future provisioning services.
Restoration of soil chemical quality requires reduced chemical contamination through reducing current levels and inputs of mineral fertilizers, herbicides, pesticides, heavy metals and if relevant, improved water management. These restoration practices almost always trade off with provisioning services and can influence resource efficiency both positively and negatively on short time scales, while not showing short-term impacts on soil health (Fig. 1, Supplementary Table S1). For example, direct reductions of chemical contamination trade-off with productivity since conventional agriculture heavily relies on mineral fertilizers, herbicides, and pesticides to enhance and stabilize yield79. Resource efficiency, on the contrary, might respond to changes in chemical inputs both positively and negatively; costs are lower due to reduced investment in chemical inputs and microbial nutrient cycling may be more efficient, but there may also be more labour needed for increased weed management75. It is noteworthy that replacement of chemical fertilizers and pest control by biological alternatives offers a solution to diminish these trade-offs with productivity and resource efficiency; this is a strategy already applied in some sustainable agricultural systems (e.g. ref. 78, Fig. 2). Practices like top-soil removal and bioremediation also combat soil contamination through targeted reduction of existing contamination levels. Top-soil removal aims to diminish contamination through removal of the active soil layer and has been successfully applied to restore oligotrophic vegetation5,80. Yet, under certain environmental settings, this may also cause problems like soil erosion10,55, and reduce soil organic carbon content and microbial diversity, which contradicts other soil restoration goals (Fig. 1)53,71,80–82. Bioremediation uses microorganisms and plants to degrade and/or uptake, organic contaminants in soil. Microorganisms break down contaminants by using them as an energy source or co-metabolizing them during energy production, which makes the practice of bioremediation less invasive than other measures, as it only requires a brief period of extra labour and pause of production during the application of microorganisms83. Though quite promising as a new possibility for restoration in active systems, the side effects of this recently implemented practice are not yet fully clear84, e.g. amendments with foreign, mass-produced microorganisms can change the local microbial community and associated soil functions85,86.
Fig. 2. Synergies between strategies of sustainable agriculture, improvement of soil threats and soil restoration actions.
Impact strength of sustainable agriculture on soil threats and restoration actions is differentiated as main impacts i.e. those directly addressed by sustainable agricultural strategies, and side impacts i.e. those not directly prioritized by the agricultural strategy and/or occurring indirectly alongside the intended agricultural measures. Intended, direct measures are expected to have generally stronger impact than indirect side impacts. The selection of listed soil threats is based on those published by the FAO (OECD FAO21) and the restoration actions are those suggested by the group of authors (stemming from different disciplines of soil and restoration ecology) and recent publications of the topic to improve these soil threats and reach the restoration goals suggested by this review. The list of restoration actions albeit not exhaustive should reflect the most straightforward and most applied soil restoration actions. Supplementary Table S2 provides the detailed compilation of statements and references. Created in BioRender. Hannula, E. (2024) BioRender.com/f39j113.
Restoration of soil biological quality aims to enhance the functionality of the soil microbial community directly through soil inoculation with beneficial microorganisms or indirectly via diversification of the vegetation cover. These practices can impact the provisioning services either positively or negatively (Fig. 1, Supplementary Table S1). Like for bioremediation, microbial inoculations can have contradictory effects84. For example, inoculation with beneficial microorganisms such as mycorrhizal fungi or N-fixing bacteria benefits plant performance through enhanced nutrient- and water uptake, but also through enhanced resistance to environmental stress53, ultimately promoting productivity and production stability. Yet, at the same time increasing the abundance of few, mass-produced taxon groups (of mycorrhizal fungi—Glomeromycota—or of N-fixing bacteria—Rhizobia, for example) leads to less diverse and less stable soil communities, and in addition, potential suppression of the native soil community85,86 and its associated functions such as pest control and thus productive stability87. Usage or enhancement of native, diverse soil inoculums (i.e. from native well-functioning soils) can reduce the risk of losing soil diversity and production stability but also comes with the risks of co-inoculation with pathogenic soil organisms in the soils and potentially reduced yield88.
To choose the most feasible way to restore a particular soil, risk analysis is recommendable weighing the costs and benefits of each action89. For example, in the case of microbial inoculants, the costs of introducing native pathogens with native inoculum might yet still be lower in terms of yield reduction than those of introducing non-native pests, pathogens, and invasive microbial species, for which tools to control them are still unknown and that can preclude the establishment of the native biodiversity. Famers’ precautions with pest control, however, might limit the acceptance of applying any measures that come with any risk of pest introduction. For example, diversification of vegetation through inter-cropping or reduced weed control enhances pest control through increase in biodiversity87,90, yet competition of crop plants with weeds or intercrops could reduce crop plant performance and productivity49,91 (but see ref. 76 for positive weed effects on yield). Interestingly however, diversification of vegetation on the outskirts of cropland (such as flower strips and hedges) can bring similar benefits to productivity and production stability, which may be promising as a restoration technique in agroecosystems92.
Towards soil restoration goals 2-5: agricultural-restoration of soil health through soil biodiversity-functioning links, soil-vegetation links and landscape-scale drivers
The goal of restoring soil quality focuses on individual soil properties, acknowledging that soil properties are intertwined with each other, albeit implicitly. The other restoration goals, i.e. restoring soil health, soil biodiversity-functioning, soil-vegetation links and soil restoration at the landscape-scale, explicitly combine multiple soil indicators simultaneously as well as consider their interactions. These restoration goals with combined indicators entail the trade-offs and synergies of the specific restoration measures that they combine. All of these restoration measures mainly trade-off with the agricultural goal of productivity, but partly also with the goal of resource-use efficiency (Fig. 1, Supplementary Table S1)28,91. For example, restoring soil health or multifunctionality28, although, as for many soil-quality measures, the resulting multifunctional soils can be, to an extent, more resource-use efficient and stable in productivity as they require fewer external inputs93. Albeit the long history of studies on soil biodiversity and ecosystem functioning in grassland ecosystems10 there is still much room for innovation in this field, especially in agricultural soils (e.g. ref. 94), Lastly, the goal of restoring all the above-mentioned properties, i.e. soil health at the landscape scale focuses on the improvement of soil properties throughout the surrounding landscape. These practices aim at maintaining or increasing the availability of undisturbed ecosystems and soils adjacent to the agricultural site (e.g. hedgerows, flower strips, forest, extensive, permanent grasslands). Overall, this can enhance soil health and ultimately productivity and production stability at the agricultural site through spill-over effects, with little adverse impact on the local agricultural production process, albeit some moderate increases in labour needed due to management of the field-margin habitats55,92,95.
Implications for restoration of agricultural soils
To illustrate the possible implementation and prioritization of restoration goals for agricultural soils, we present the most common restoration activities and apply them to two examples –typical cases of soil degradation in agricultural soils (Boxs 1, 2). Decision on specific restoration activities depends not only on the type and severity of soil degradation (Fig. 2), and the desired restoration goal (Fig. 1), but also on the level of ambition. The Society of Ecological Restoration (SER) suggests in their international standards of ecological restoration a useful framework guiding the decision making around the implementation of restoration activities7.The cornerstones of this framework are a set of measurable ecosystem attributes and a 5-star system of levels of restoration ambition to define the restoration goal as a baseline to measure restoration success. This framework has the advantage to allow measuring restoration success also in cases where defining a pristine reference ecosystem as restoration goal is not feasible, including anthropogenic ecosystems such as agricultural land. Restoration goals should then be selected in correspondence to the environmental conditions (e.g. increasing organic matter content in arid regions should match in quantity and quality those of the surrounding natural ecosystems). The restoration goals developed in this review specify the general ecosystem attributes for soil restoration (Fig. 1) that can be diversified into different levels of ambition from restoring solely basic soil functioning to the restoration of the entire soil ecosystem with its native communities and biotic interactions (Table 1). In agriculture systems, on-site restoration within the site under agricultural use, has typically lower levels of restoration ambition (i.e. provisioning services and soils supporting services, Fig. 1, SER suggestion 1 in Table 1, Boxs 1, 2 non ambitious restoration vision). However, agricultural sites and other ecosystems in the surrounding landscape may have higher levels of ambition, such as restoration of native (soil) communities and species interactions (SER’s suggestion 2–4 in Table 1, Boxs 1, 2 ambitious restoration vision).
Table 1.
Possible levels of ambitions for restoration projects detailed for different ecosystem attributes recommended by the SER
Ecosystem attribute (soil restoration goal) | * | ** | *** | **** | ***** |
---|---|---|---|---|---|
Absence of threats (no separate restoration goal, but implied as restoration activity) |
Further deterioration discontinued, and site has tenure and management secured | Threats from adjacent areas beginning to be managed or mitigated | All adjacent threats managed or mitigated to a low extent | All adjacent threats managed or mitigated to an intermediate extent | All threats managed or mitigated to high extent |
Physical conditions (Improve soil physical and chemical quality) | Gross physical and chemical problems remediated (e.g. excess nitrogen, altered pH, biochemical contamination) | Soil chemical and physical properties on track to stabilize within range of the reference system | Soil stabilized within range of the reference system and supporting growth of native biota | Soil securely maintaining conditions suitable for ongoing recruitment of native biota | Soil exhibiting physical and chemical characteristics highly similar to that of the reference ecosystem with evidence they can indefinitely sustain species and processes |
Species composition (Improve soil biological quality) | Some colonizing beneficial symbiotic and decomposing species present (ca. 2% of reference system). Moderate onsite threat from pathogenic species. Regeneration niches available. | A small subset of characteristic beneficial symbiotic and decomposing species establishing (e.g. ca. 10% of reference). Low to moderate onsite threat from pathogenic species | A subset of characteristic beneficial symbiotic and decomposing species establishing (e.g. ca. 25% of reference) over substantial proportions of the site. Very low onsite threat from pathogenic species. | Substantial diversity of beneficial symbiotic and decomposing species establishing (e.g. ca. 60% of reference) present across the site and representing a wide diversity of groups. Very low onsite threat from pathogenic species | High diversity of characteristic beneficial symbiotic and decomposing species establishing (e.g. ca. 80% of reference) with high similarity to the reference system; improved potential for colonization of more beneficial species over time. No onsite threat from pathogenic species |
Structural diversity (Harness soil vegetation interdependence) | One or fewer biological strata present and no spatial patterning or community trophic complexity relative to the reference ecosystem. | More strata present but low spatial patterning and trophic complexity relative to reference. | Most strata present and some spatial patterning and trophic complexity relative to reference. | All strata present and substantial spatial patterning and trophic complexity developing relative to reference. | All strata present and high spatial patterning and trophic complexity relative to reference. Further patterning and complexity able to self-organize to highly resemble the reference. |
Ecosystem function (Improve soil health, harness soil BEF relationship, harness soil vegetation interdependence) | Substrates and hydrology are at a foundational stage only, capable of future development of functions similar to the reference. | Substrates and hydrology show increased potential for a wide range of functions including nutrient cycling, and provision of habitats and resources for other species. | Evidence of functions commencing (e.g. nutrient cycling, water filtration, and provision of habitat and resources for a range of species). | Substantial evidence of functions and processes commencing including reproduction, dispersal, and recruitment of native species. | Considerable evidence of functions and processes on a secure trajectory towards that of the reference and evidence of ecosystem resilience tested by reinstatement of appropriate disturbance regimes. |
External changes (Restore soil health at the landscape-scale) | Potential for exchanges (e.g. of species, genes, water, fire) with surrounding landscape or aquatic environment identified. | Connectivity for enhanced positive (and minimized negative) exchanges arranged through cooperation with stakeholders. Linkages being reinstated. | Positive exchanges between site and external environment becoming evident (e.g. more species, more gene-flow) | High level of positive exchanges with other native ecosystems established; control of undesirable species and disturbances. | Evidence that external exchanges are highly similar to reference, and long-term integrated management arrangements with broader landscape in place and operative. |
The table is based on the current international standards for ecological restoration (Gann et al. 7) with some adaptations to soil restoration and additionally aligning the defined soil restoration goals of this review with the recommended ecosystem attributes and highlighting the restoration goals suggested for implementation for different scenarios of restoration of agricultural land by Gann et al. 7 (see footnote). The stars indicate the levels of ambition (* - low to ***** - highest possible) according to the SER´s 5-star system presented in Gann et al. 7.
SER´s restoration suggestions for agricultural and horticulture lands:
Full Restoration: Native ecosystem recovery (out of use) (complete 5-star column - *****)
Rehabilitation/passive restoration: Recovery of agricultural productivity/ecological agriculture adjacent to native ecosystems (complete 3-star column - ***)
Partial Restoration: Native ecosystem with potential for only partial recovery (2-star column, at least for biological attributes i.e. species composition, structural diversity, ecosystem function and external changes - **)
Rehabilitation: Recovery of agricultural capacity for ecosystem services (2-star column for ecosystem function - **)
Below we describe a broad collection of the most common restoration activities for soils used in food production and in landscape-scale soil restoration as an inspiration how soil restoration in agriculture could be applied. As ecosystems vary in environmental conditions, and restoration goals, (levels of ambition) depend on individual farm management, this compilation of activities is not exhaustive but is a starting point to define actions adapted to the environmental context, economic feasibility and ambition of soil restoration (as illustrated in Boxs 1, 2).
Box 1 Hypothetical agricultural soil restoration example for reversing degradation of agricultural soils due to eutrophication/over-fertilization including restoration goals, levels of ambition for each goal and suitable restoration activities.
Problem:
Soil eutrophication and nutrient leaching into the groundwater and thus to adjacent ecosystems due to over-fertilization. See photograph as illustration.
Context:
Typical cornfield in central, temperate Europe with high soil fertility and moisture as well as small-scale landscape structure. Picture taken in Münster, (Germany) by © Lena Neuenkamp.
Intensively managed corn field (10 ha) in Münster (Northwest Germany) on highly fertilized sandy-loamy soils with sufficient precipitation throughout the year (870 mm per year); the landscape surrounding the field contains many structural elements such as hedgerows, tree lines, ditches and small forests typical of the so-called park-like landscape of the Münsterland region (Landwirtschaftskammer NRW113).
Typical cornfield in central, temperate Europe with high soil fertility and moisture as well as small-scale landscape structure. Picture taken in Münster, (Germany) by © Lena Neuenkamp.
Current condition:
Corn is cultivated on the tilled fields during late spring and early summer and treated with large quantities of slurry and NPK fertilizer (ca. 300 kg N per ha and year) as well as pesticides for pest and weed control. After the harvest from August to October the corn field is tilled again and cultivated with intercrops or winter wheat, including further fertilization using slurry and additional pesticide application. High fertilizer and pesticide concentrations together with year-round excess water through precipitation can lead to substantial leaching of nutrients and pesticides to the groundwater. Chemical and mechanical weed management further lead to periods of very low vegetation cover favouring leaching of nutrients and occasional soil erosion in between the crop rows during heavy rains. Weed management by herbicides in conjunction with high nutrient levels finally result in low plant and subsequently low soil diversity in the field and field margins. Wind erosion risk of soil is low due to moderate wind speeds and the structural landscape elements surrounding the field acting as wind breakers. Example based on governmental agricultural information for central Germany from Landwirtschaftskammer NRW (2022) and Deutsches Maiskomitee114.
Vision (moderately ambitious): Corn production and yield remains stable, but with aim to reduce negative impacts on the surrounding ecosystems and the groundwater by preventing leaching and with lower risk of soil erosion. | Vision (more ambitious): The vision is the same as the moderately ambitious vision but adding the aim to increase plant and soil biodiversity and ultimately those of other trophic groups (e.g. pollinating insects) and biotic interaction among them. |
Soil restoration goals: 1. Increase soil chemical quality 2. Increase soil health (i.e. stabilize soil functioning) | Soil restoration goals (in addition to 1-2): 3. Improve soil biological quality (soil biodiversity) 4. Acknowledge the soil-vegetation interdependence 5. Harness the soil biodiversity-ecosystem functioning relationship 6. Increase soil health at the landscape scale |
Restoration activities: 1. Reduce slurry, mineral fertilizer and pesticide inputs and reduce subsequent leaching, e.g. corn´s high nutrient-use efficiency allows it to take up 130 kg/ha residual N after cultivation of wheat (Deutsches Maiskomitee114). 2. Add legumes or other catch crops to the cropping cycle or as under-sown species to assure soil cover at all times, reducing leaching risks and to recover soil nutrients. Moreover, add C-rich material to restore soil stoichiometry and promote C-storage of microorganism (Clocciatti et al.67). | Restoration activities (in addition to 1-2): 1.3. Reducing tillage frequency as much as possible to lower soil disturbance and allow soil microbial communities and species interactions to develop, as diversity and functioning increase over time. 4. Diversify mixtures of under-sown 5. and cover crop species (i.e. further diversification of the cropping cycle), with expected positive effects on soil microbial diversity and biotic interactions Same activities as 4. as diversified soil biodiversity and biotic interactions amplify soil functioning/health. 6. (Partial) restoration of ecosystems surrounding the corn field as much as feasible, especially with the focus on enhancing native community diversity and biotic interactions. |
Box 2 Hypothetical agricultural soil restoration example for reversing degradation of agricultural soils due to soil erosion including restoration goals, levels of ambition for each goal and suitable restoration activities.
Problem:
Loss of the organic and fertile humus layer by accelerated mineralisation and wind erosion due to tillage, lack of vegetation cover and spatial landscape structures stopping the wind. See photograph as illustration.
Context:
Typical harvested wheat field with stubbles in the steppe of Northern Kazakhstan with moderately high soil fertility but low moisture, high wind speeds, and little landscape structure. Picture taken close to Astana (Kazakhstan) by © Johannes Kamp.
Extensively managed summer wheat field (400 ha) near Astana (Northern Kazakhstan) on moderately productive loamy-sandy Kastanozem soils with little annual precipitation (350 mm per year). The landscape surrounding the field contains few structural elements besides other large agricultural fields or small remnants of steppe vegetation.
Typical harvested wheat field with stubbles in the steppe of Northern Kazakhstan with moderately high soil fertility but low moisture, high wind speeds, and little landscape structure. Picture taken close to Astana (Kazakhstan) by © Johannes Kamp.
Current condition:
Summer wheat is sown in May after tillage with no or very sparse mineral NPK fertilizer and weed management if applied by spraying from airplanes. After the harvest in August/September, the summer wheat field is left fallow until the next tillage in May before sowing. Tillage, lack of vegetation cover, high wind speeds, low precipitation and a sandy soil structure favour the loss and degradation of humus-rich topsoil through mineralisation of organic matter and wind erosion during the fallow times but also during cultivation, as vegetation cover between crop rows is low due to dry environmental conditions and weed management. Wind erosion risk is enhanced by large field sizes and the lack of trees in the naturally open steppe landscape. Continued tillage and biomass extraction through harvest lead to considerable losses in nutrients and humus followed by lowered soil water potential and declining soil fertility. Example based on agricultural research from Northern Kazakhstan (Koza et al.115).
Vision (moderately ambitious): Summer wheat production and yield remaining stable, while the risk of soil erosion is lowered, and soil organic carbon and nutrient stocks are maintained. | Vision (more ambitious): The vision is the same as the moderately ambitious vision but adding the aim to increase structural diversity at the landscape scape to elevate plant diversity and subsequently soil biodiversity, those of other trophic groups (e.g. pollinating insects) and biotic interaction among them and ultimately ecosystem functioning and resilience. |
Soil restoration goals: 1. Increase soil health (i.e. stabilize soil functioning) | Soil restoration goals: 2. Acknowledge the soil-vegetation interdependence 3. Harness the soil biodiversity-ecosystem functioning relationship 4. Increase soil health at the landscape scale |
Restoration activities: 1.a. Reduce tillage to increase soil aggregate stability and decrease erosion risk 1.b. Avoid fallow times with bare soil by adding legumes or other catch crops to the cropping cycle or as under-sown species to assure soil cover, increase soil moisture, and to recover soil nutrients. | Restoration activities: 2. Diversified mixtures of under-sown species and cover crop species (i.e. further diversification of the cropping cycle), with expected positive effects on soil microbial diversity and biotic interactions. 3. Same activities as 2. as diversified soil biodiversity and biotic interactions amplify soil functioning/health. 4. Diversify landscape structure in the surrounding of the wheat field by restoring/re-installing stretches of native steppe grassland ecosystems and reduce field sizes as much as practicable to lower wind-speed and wind erosion. Moreover, restoring native steppe grassland provides grazing opportunities for local livestock and comes with the benefit of enhancing native community diversity and biotic interactions above- and belowground. |
On-site restoration (within the agricultural site)
Restoration practices to halt degradation of agricultural soils that are being applied on sites currently under agricultural production mostly encompass measures of management extensification that reduce land-use impact, which often imply reducing land-use intensity and the application of resource-conserving practices96. These measures should aim at maintaining productivity to minimize divergence between restoration and agricultural goals. Invasive measures such as abandoning site from production71, are hence less suitable, as they hamper the provisioning services. Under the umbrella of suitable on-site restoration practices for agricultural soils fall most concepts of sustainable agriculture, such as organic farming, regenerative agriculture97, and sustainable intensification usually termed conservation agriculture98. Sustainable intensification and regenerative agriculture serve best in combining soil restoration and agriculture as they focus on soil biodiversity and ecosystem functioning99 (Fig. 2, Supplementary Table S2). The level of ambition for on-site soil restoration is commonly limited to the recovery and stability of provisioning (Fig. 1), and few basic soil ecosystem functions such as minimizing the negative impacts on surrounding ecosystems such as nutrient leaching7 (Table 1).
More specifically, the concepts of sustainable management are covered in three soil restoration practices (Fig. 2). 1) In organic farming, only organic fertilizers are used which maintains soil fertility and increased activity of native microbes can lead to soils being resilient to plant pathogens and promote nutrient mobilization52,100. It is also a resource-conserving practice and hence minimizes the effects of external inputs promoting biodiversity52,100. Therefore, organic farming benefits several restoration goals and protects against various threats including i) reducing chemical and fertilizer inputs and thus soil contamination, and ii) reducing soil disturbance and increase diversity of vegetation cover, thus increasing soil biodiversity and reducing carbon loss, and ultimately ensuring soil fertility and pathogen protection77,101 (Fig. 2). 2) Regenerative agriculture follows a similar approach than organic farming to conserve the soil but puts soil conservation more comprehensively into focus beyond reduction of artificial external inputs. The approach of regenerative agriculture entails various adaptive, resource-conserving agricultural practices aiming to minimize soil disturbance, keep soils covered and leave living roots inside the soil, encourage diversity, and integrate livestock97,102 (Fig. 2). The practices applied in regenerative agriculture align well with a subset of our soil restoration goals (Fig. 2), namely: improved soil carbon and soil water-holding capacity, enhanced microbial functions, nutrient cycling, and increased resilience to diseases and pests (Fig. 2). 3) Sustainable intensification adds the use of biodiversity‐ecosystem functioning mechanisms as a new aspect99, i.e. the enhancing of functional benefits that bring about biodiversity, such as pest-control87 (Fig. 2).
The three presented approaches of sustainable agriculture entail yield trade-offs (Fig. 1). However, recent research has proposed solutions to minimize these trade-offs, allowing them to emerge as promising agricultural restoration strategies. One solution is the targeted application of sustainable agricultural practices. Yield loss with biodiversity gain under no-tillage in organic farming systems seems to be taxon- and crop-type-dependent with non-cereal crops showing much more positive yield responses77. Increased application of organic fertilizer under no-tillage can partly compensate for the lower yield stability induced in organic farming no-tillage systems79. Another solution is incorporating time flexibility for long-term restoration to take effect. The regeneration of soils under regenerative and conservation agricultural practices often takes years after starting the practices to regain lost soil functions (e.g. soil carbon content) and this often coincides with a period of reduced yields (yield gap; Fig. 1)100,103. Inoculations with microbes offer a possibility to decrease the yield gap increasing plant productivity but this potentially has only short-term effects and can negatively affect native soil biodiversity53, especially when using foreign or mass-produced instead of native inoculum85,86. A final solution is diversifying agricultural production systems. New business models for agricultural producers are emerging where not only yield is considered but also other verifiable functions such as increase in nutrient use efficiency and carbon retention61. We further stress that all agricultural restoration measures should be tested for their feasibility and success of effects with local communities that include farmers. The establishment of ‘living labs’ and ‘lighthouse farms’ where farmers co-create together with scientist solutions to improving the soils is a definite way forward104.
Landscape-scale restoration
To maximize soil restoration potential, since ecosystems within a landscape are connected and restoration measures might be compromised by the necessity of profit in terms of on-site restoration efforts in active agricultural systems, distribution of restoration measures in the landscape and non-agricultural sites can be an option to reverse soil degradation45,55,72,73. This approach follows the concept of land sparing vs. land sharing105 and of passive restoration i.e. the positive impact of intact (restored) ecosystems to their surrounding ones7. Such landscape approaches include restoration of matrix ecosystems surrounding agricultural production sites to create buffer and connection patches, or at an even larger hierarchical scale, aiming for the restoration of multifunctional landscapes55,106. The level of restoration ambition for landscape-scale restoration can vary between full and partial restoration of the surrounding ecosystems but compared to only rehabilitation of ecosystem functions of on-site restoration activities should also focus on the biotic ecosystem elements such as restoration of native community composition and interactions7 (Table 1).
Common restoration practices to restore ecosystems in the agricultural matrix or the landscape work through adding diversifying landscape elements such as hedge rows107,108 or flower strips92. These practices are vegetation-based, with effects of higher vegetation diversity and complexity acting on the soil via plant-soil interactions; soil focused practices could further enhance the soil restoration potential of these landscape-scale approaches. Establishment of hedgerows in an agricultural landscape increase soil-based functions and services such as diversity of arbuscular mycorrhizal fungi108, organic matter and nutrient accumulation107 (Fig. 2). These effects come with positive feedback with the vegetation through enhancing flowering plant diversity, establishment, and persistence64,73 and ultimately, pollination and crop yield92,109 (Fig. 2). Positive effects increase with permanency of the matrix ecosystems and the development of the soils therein, calling beyond the establishment of matrix ecosystems also for the conservation of existing natural ecosystems within the agricultural landscape such as grasslands and forests72,73.
As direct soil restoration practice, soil inoculation with native soil from the surroundings could be applied to enhance soil diversity steering hedgerows and other matrix elements towards the favourable conditions that allow them to increase crop yield and pollination53. However, direct effects of flower strips on soils are less studied92. Their potential to control aboveground pests92 might give rise to similar effects belowground, where high plant diversity also controls microbial pathogen loads90. Yet, reduced soil disturbance caused by flower strips seems to be the most relevant factor causing the final mediation of below-ground pest control, through the enhancing of native, beneficial soil microbes such as mycorrhizal fungi110. Thus, agricultural matrix and landscape elements are a promising measures to improve soils within a nearby agricultural landscape and alleviate negative soil impacts on those agricultural sites, especially when integrated long-term into the surrounding ecosystems.
Future directions
Current rates of ecosystem degradation in the face of ongoing climate-change have boosted research and development to find strategies combating these trends. The formation of international incentives and regulations such as the Sustainable Development Goals or the UN Decade of Ecological Restoration underlines the relevance of these topics. From an agricultural point of view, that means enabling food security while combining profitable production with sustainability, ideally while also integrating local and scientific knowledge111. Considering this, the immense potential of soils in supporting this task is in the focus of attention (e.g. Soils and the Sustainable Development Goals112). This review revealed many approaches to restore soil and foster sustainable agricultural production, while also revealing remaining research gaps.
First, many of the reviewed restoration approaches and practices are known (e.g. intercropping or vegetation diversification) and the only change that must be implemented is that the goal of reversing soil degradation should be included as a decision criterion. This will allow the addressing of potential trade-offs between different restoration and production goals, as well as an expansion of understanding towards the combined effects of multiple restoration actions on individual soil properties and functions, and ultimately soil multifunctionality. In other words, though we know the effects of single restoration actions—as described in this review—their combined effects and interaction are still a matter of recent research23,24 that should explicitly integrate soil restoration strategies.
Second, this review touched upon the environmental aspects of soil restoration in agriculture, screening potential methods of soil restoration that can be integrated into agricultural landscapes. The implementation of these methods has a political and economic consideration, regardless of the range of the strategy from fully organic to modifications made in molecular mechanisms. This brings up questions of how to motivate the adoption of soil restoration methods by agricultural producers and monitor their efficiency25 in view of the public eye. Piñeiro et al.25 demonstrated in a recent review that political incentives for adoption of sustainable agricultural practices are partly successful. Yet, more data needs to be collected on the specific environmental and socio-economic conditions of the agricultural production site as well as the effects of the incentives on ecosystem services.
Finally, an aspect that has not been explicitly focused on in this review but that we emphasized as important to consider in the introduction, is the social aspect of ecological restoration, i.e. the inclusion of diverse stakeholders and diverse sources of knowledge, including traditional ecological knowledge, into restoration projects. This is not a new idea; it has been put forward as a strategy to enhance restoration success and acceptance of restoration projects within the populations most closely affected by these very measures26,27.
Reporting summary
Further information on research design is available in the Nature Portfolio Reporting Summary linked to this article.
Supplementary information
Acknowledgements
All authors thank the editorial team of Communications Biology and Professor Li for inviting us to contribute to the Restoration and Rewilding Collection. They also thank Fernando Maestre, Marcel van der Heijden and Pete Manning, as well as the three anonymous reviewers for their very valuable comments on earlier drafts of this manuscript. L.N. thanks the European Union for funding of the MYFUN project (835472) through the Marie Skłodowska-Curie Individual Fellowship. D.G.L. thanks the Regional Government of Madrid and The University of Alcalá for project [CM/JIN/2019-023] and the talent research grant 2018-T2/BIO-10995, and the European Union NextGenerationEU/PRTR for project TED2021-130908B-C44, funded by MCIN/AEI/10.13039/501100011033.
Author contributions
L.N. developed the outline and first draft of the manuscript. L.N., D.G.L., E.G., U.H., N.H., and E.H. edited the outline and the first and following drafts regarding their expertise: L.N.—multifunctionality, mycorrhizal fungi, comprehensive restoration goals; D.G.L.—landscape-scale restoration; E.G.—stakeholder participation and soil biodiversity; U.H.—soil quality indicators; N.H.—implementation of restoration strategies; E.H.—soil biodiversity and soil organic carbon. L.N. finalized the manuscript, and L.N. and E.H. drafted the illustrations, which E.H. finalized. L.N. and N.H. drafted the restoration examples, which L.N. and E.H. finalized.
Peer review
Peer review information
Communications Biology thanks David Eldridge, Lisa Markovchick, and Jimmy Morales-Márquez for their contribution to the peer review of this work. Primary Handling Editors: Shouli Li and Manuel Breuer. A peer review file is available.
Data availability
The authors declare that all data and code in this data is made publicly available. As the manuscript presents a literature review, with no data analysis applied, no code has been used. All literature that forms the basis of this review is listed in the reference of the main text and supplementary material. The latter contains the literature used for creating the figures and strategies of literature search are detailed in the figure captions.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
The online version contains supplementary material available at 10.1038/s42003-024-07275-2.
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Data Availability Statement
The authors declare that all data and code in this data is made publicly available. As the manuscript presents a literature review, with no data analysis applied, no code has been used. All literature that forms the basis of this review is listed in the reference of the main text and supplementary material. The latter contains the literature used for creating the figures and strategies of literature search are detailed in the figure captions.