In the upcoming United Nations Decade on Ecosystem Restoration, a global challenge for scientists and practitioners will be to develop a well-functioning seed production sector on the basis of a sound species-selection process1. To balance crop production with biodiversity functions in Mediterranean woody crops, agroecological practices2 suggest the need to move towards the establishment of herbaceous ground covers3,4,5. However, establishing such plants requires a supply of suitable native seeds, which is currently unavailable. Here, we present a comprehensive process for selecting regionally adapted species that also emphasizes considerations for seed production6. Using olive groves as a target system, we found that research on ground covers for regenerative agriculture has largely overlooked native species at the expense of commercial and ill-suited varieties. Our assessment of native annuals showed that 85% of the grasses and forbs evaluated exhibit a suite of ecological and production traits that can be tailored to meet the requirements of farmers, seed producers and environmental agencies. These findings suggest that many native species are neglected in agronomic research, despite being potentially suitable for ground covers and for supporting a nature-based solution7 in restoration practice. The framework used here may be applied in other agroecosystems to follow global greening initiatives and to support native seed production to scale up restoration8,9,10.
Agricultural intensification of Mediterranean woody crops (vineyards, olive groves and fruit trees) has dramatically changed traditional landscapes that were relatively sustainable until the twentieth century11. Olive groves (Olea europaea L.) are a quintessential example of agroecosystems suited for regenerative practices12 because they are perennial cultural systems currently degraded by erosion, desertification and biodiversity loss3. Olive groves range from traditional to intensive and very intensive production systems. In most cases, the use of fertilizers, the suppression of non-crop vegetation and modern irrigation practices have maximized olive production at the cost of soil health, compromising the sustainability of a strategic economic sector in Mediterranean countries13. In turn, the combination of tillage and herbicide use has led to large expanses of bare soil14 through the loss of herbaceous layers that covered olive groves for centuries. These practices increase the dependence on water and the progressive loss of soil organic matter, leading to the need to restore ground covers and balance crop production with the preservation of natural and cultural services15. It has been widely suggested that commercial varieties used for ground covers are ill-suited for the Mediterranean climate and compete with the crop for soil moisture, while native species, especially winter annuals, might provide the benefits of ground covers without the negative aspects of exotic species13,16.
We established an evaluation process to identify native plants with the potential for restoring agroecosystems to meet sustainability targets (Fig. 1). Our framework is based on the untested premise that native plants may be ideal ground covers because they have a better ecological fit with the system, assuming they can be farmed to produce an adequate amount of seeds for establishing and restoring ground covers. As the first step, we reviewed the literature of the last 30 years to assess the use of native plants in agroecological research for restoring the herbaceous cover of olive groves in Mediterranean countries (see ‘State of the art’ in Methods). Of the 50 studies evaluated, 68% focused on ground-cover performance and effects on soil erosion or soil water using commercial species (Fig. 2). These studies analysed 42 forage or domesticated crop varieties (45% Fabaceae, 31% Poaceae, 14% Brassicaceae and 10% other families) from species that are exotic to the regions where they were used (Supplementary Table 1). The other 32% of studies evaluated a total of 20 species native to the study regions, in most cases grasses and forbs (55% Poaceae, 20% Fabaceae, 15% Brassicaceae and 10% other families). While all the studies on native plants assessed ecological traits relevant to their value as ground covers (for example, self-sowing, height development, growth form, herb cover, root development or nitrogen fixation), none of them considered seed-farming potential. This is an important research gap because the need for a seed supply is a priority for establishing ground covers13,16. Indeed, a current global challenge is how to scale up restoration by using large amounts of seeds from native plants to satisfy future demand10, a crucial issue for the upcoming United Nations (UN) Decade on Ecosystem Restoration. In Europe, the whole sector for the production of herbaceous native seeds is underdeveloped for producers and users17, limiting the implementation of agroecological practices.
In the second step, we defined the agroecosystem species pool as the set of wild species that is known to occur naturally in the target system, assuming a portion of these species will be suitable for agroecological restoration (Fig. 1, see ‘Species filtering’ in Methods). As a case study, we investigated the agroecosystem species pool of olive groves in the Spanish province of Córdoba (Andalusia), which has a key role in the global olive market18. From a total of 979 taxa of the regional flora reported to occur in traditional olive groves19, we collected life-form traits and species distribution ranges to filter the list to 303 species that are annuals and native to the Mediterranean Basin (see ‘Data availability’). Annual plants are desirable because they will naturally senesce at the onset of the summer dry season and persist as seeds. This reduces competition with the crop for soil moisture and reduces the requirement that farmers actively manage the ground cover, which regenerates from the seed bank at the onset of the autumn rains, when protection from erosion is needed. Nativity to the Mediterranean Basin is also important because not only will the species be adapted to the climate and farming cycles but also the plants will host and support pollinators (for the ground cover and adjacent crops) and beneficial insects as biological pest control20. We compiled up to six ecological traits to assess the suitability of native species for olive farming (see ‘Suitability index’ in Methods) and evaluated these traits in 10 grasses and 30 forbs that passed the above filters and were found in wild populations. Such evaluation (Table 1) showed that most of the species are ecologically suitable (Good, Fair or Excellent) for ecological restoration in the study system.
Our process then looked at production traits to estimate the suitability of species for seed farming (that is, how they respond to the requirements of agronomic practices for producing cost-effective seed lots and generating a commercial seed supply). When we grew them in seed production fields (see ‘Agronomic experiments’ in Methods), we found that 8 grasses and 27 forbs (out of 10 and 30, respectively) showed good establishment and developed to reproductive maturity (Fig. 3). The grasses showed slight differences in phenology, with Cynosurus echinatus, Trachynia distachya and a commercial variety of Lolium multiflorum ripening later than the other grass species. Forbs were more variable in their development, with 13 out of 29 species reaching fruit maturity in July (after 29 weeks), while the other species matured later. These results indicate relatively similar seasonalities and an optimal seed harvest time in early summer (June–July) for grasses and forbs sown in December.
The evaluation of production traits on the basis of the experimental fields showed that most of the species are suitable for seed farming (Table 1). We also looked at fruit height and seed yield, which are critical traits for cost-effective production because they determine the feasibility of mechanical harvesting and the quantity of seeds per area, respectively. We found that all native grasses and 24 forbs produced fruits at a suitable height (taller than 10 cm) for mechanized harvest (for example, with a combine harvester). We found large differences (six orders of magnitude) among the seed yields of grasses, with the highest values for the native grass T. distachya and the lowest for the commercial variety of L. multiflorum. Within forbs, the differences were even larger (18 orders of magnitude), with a clear difference between families with small- and large-seeded species (see ‘Data availability’).
Using the data collected for the selected species, we created a final suitability index that combined ecological and production traits (Table 1). Although both groups of traits may be assessed independently, here we looked at combined suitability for olive farming and seed farming. From a total of 35 species evaluated, 26 were defined as Excellent or Good, 7 were defined as Fair, 1 was Poor and 1 was Fair/Good. The grasses were equally distributed from Fair to Excellent, with the species of Anisantha and Hordeum ranking highest. Although some of the study species have been previously evaluated as ground covers (see Supplementary Table 1), our study demonstrates how the agronomic traits of these species make them suitable for seed farming. Moreover, we identified more than 20 species that have not been used before for greening Mediterranean olive groves, suggesting that many other species from the agroecosystem species pool (not evaluated here) are potentially suitable for ground-cover restoration. Since our seed collection was performed in a relatively dry year (see Methods), it is possible that the evaluated species have specific traits for regeneration with low soil moisture. An ideal follow-up of the evaluation process should therefore repeat field collections to account for the natural dynamics of Mediterranean annual communities in response to interyear climate variability.
We note that some of the evaluated species can be considered weeds by farmers21 and may have been subjected to eradication in olive groves in the Mediterranean Basin. Since many farmers may be reluctant to re-establish wild species22, the adoption of native species as ground covers will require outreach and education activities to meet global policy on restoration (Fig. 1). As a proof of concept, a pilot study conducted on a conventional olive grove in our study region showed that a subset of the species predicted as potentially suitable in this study performed well during the following growing season, developing a soil seed bank with the potential for plant regeneration23. Nevertheless, the performance of specific monocultures or seed mixtures may change under different environmental conditions or restoration aims (for example, when a given function is prioritized). Although our study provides a set of species that are potentially suitable for ground cover as a commercially viable alternative to commercial varieties, further investigation is needed to test the performance of those species in a target agroecosystem.
Overall, this study demonstrates how the agroecosystem species pool may provide a set of native plants with suitable characteristics to meet the requirements of seed producers and ecological restoration of Mediterranean woody crops. This study also includes production traits of native plants in a comprehensive assessment of species selection, thus combining ecological and agronomical targets. The evaluation steps presented here can be adapted to any agroecosystem for establishing large quantities of suitable seeds (or the restoration species pool17) that maximizes cost-effectiveness in seed production areas6. Similar approaches between academia and conservation agencies will be essential in restoration programmes developed by private and public partnerships to develop nature-based solutions on the basis of native seed markets10. Such programmes also will need to deal with issues related to policy targets (for example, investing research efforts on priority systems by considering regional or national regulations)10 and restoration practices (for example, designing seed provenance for selected species and developing infrastructures to scale up restoration projects)1. Our evaluation process also provides a link between agronomic research and seed producers, which is one of the major limitations of seed-based restoration17,24. The evaluation of agronomic traits will further complement the research agenda of seed-trait ecology25. Although the specific traits to be used and the way they are combined may diverge depending on the target habitats and on-site experiments, implementing a process like the one presented here is a necessary step in identifying and producing commercial native seed supplies for agroecosystem restoration.
State of the art
Olive groves are one of the most important agroecosystems in the Mediterranean region owing to their great socioeconomic impact and the large surface area they cover, with 10,527,502 ha of land under production in 2017 (97% of the global area used for this crop)26. However, the use of unsustainable soil-management practices over recent decades threatens the sustainability of these agroecosystems27. One of the most important threats is soil erosion by water, which leads to land degradation and desertification28. To ameliorate this situation, ground cover is the best method to control erosion by covering the soil with either inert matter or live plants29. While grasses are expected to provide the root structure and surface cover to protect soil from erosion and drought28, forbs (depending on the species) promote nitrogen fixation and additional functions such as interactions with pollinators, beneficial insects and other wildlife13,30.
When an olive farmer wishes to sow and establish ground covers, the species available in the market are commercial forage varieties that were not selected for this system. Wild native species are expected to provide more benefits to the farmer and the agroecosystem, but they are rarely used owing to the scarcity of seeds in the market. To address the extent of this problem, we searched for publications focusing on ground covers in olive groves of the Mediterranean region. In May 2015, we queried the Google Scholar database with the following search criteria: ‘ground covers’ AND ‘cover crops’ AND ‘olive’ AND ‘Mediterranean’ AND ‘Europe’ since 1985. From about 17,000 articles, we manually checked the titles of the publications and selected those that clearly referred to the topic. We then compiled a list of taxa used as ground cover, which were split into: (1) commercial species of any geographical distribution that are available in the market as (mostly undefined) varieties and (2) wild species that are native to the Mediterranean regions where olive trees are cultivated. We also looked at reports and proceedings cited in the selected articles, since most of the studies were useless or did not mention the species used. This resulted in 50 publications focused on olive groves from Albania, France, Italy, Portugal and Spain (Supplementary Table 1). The aims of the studies were grouped into 11 major research topics. We then summarized the numbers of commercial and native species used for each topic, and the proportions of the plant families represented in each group (Fig. 2).
We defined the agroecosystem species pool as the set of species reported to occur and persist naturally (that is, without direct human intervention) in our target system. The species pool was restricted to olive groves of Córdoba Province, Andalusia, Spain, for which there is a complete inventory of vascular plants and their habitat preferences19. We reduced the initial list to those species recorded in cultivated areas (managed crops) and ruderal areas (borders or other disturbed spots near or within fields) and applied a series of filters using information from regional and Spanish floras. Because seeds will be used as the propagule and because we are interested in herbaceous plants, we removed ferns and woody vascular plants (mainly from Equisetaceae, Salicaceae, Fagaceae, Ulmaceae, Moraceae, Santalaceae, Simaroubaceae, Anacardiaceae, Rhamnaceae, Thymelaeaceae, Tamaricaceae, Oleaceae and Arecaceae). In the next filtering step, we removed taxa whose native range is outside the Mediterranean Basin. Our definition of native plants includes archaeophytes (that is, species that might have been introduced before ad 1500 and are now naturalized). These taxa are adapted to the regional climate, and they are presumed to have the most potential for trophic interactions (with pollinators, for example). We then filtered out taxa to keep winter annuals, because they persist and regenerate in seasonally dry and disturbed habitats31 and because they have short life cycles and naturally senesce in spring. Winter annuals will therefore be self-sowing and won’t compete for water with the olive trees during the dry summer season. Some of the selected species can function as biennials or short-lived perennials, but they were included in the evaluation because they behave mostly as therophytes in the study system. Some of them (for example, Anthyllis vulneraria, Antirrhinum bellidifolium, Salvia verbenaca and Scabiosa atropurpurea) also have been identified as hosts for beneficial insects32.
In 2015, we conducted a field survey to collect seeds from wild populations of any of the preselected species in the Spanish province of Córdoba and ecologically similar environments in the nearby province of Jaén. According to data from the Spanish Agency of Meteorology (www.aemet.es) for the Córdoba airport in 2015, this year was about 50% drier than the average of the last decade. We prioritized the collection of different taxonomic families but defined between 20% and 25% of target taxa to be grasses (Poaceae) because of their structural importance as ground covers. After several field campaigns looking for any of the selected species, we had collected a sufficient number of seeds for 10 grasses and 30 forbs in a total of 66 sites. We sampled a minimum of two populations for each species with a minimum of 500 individuals per population, and we collected seeds from at least 100 haphazardly selected individuals per population, following the standards of the ENSCONET protocol33. In the study region, the natural populations available for the initial collection of foundation seeds are not threatened or legally protected, and they are relatively abundant. In a set of germination experiments, we confirmed that all the study species behave as winter annuals, and they are expected to germinate in autumn34,35, a desired condition for avoiding water competition with olive trees in summer. The remaining seeds were stored under ambient conditions until the field experiments started.
To evaluate production traits for seed farming, we conducted a field experiment on grasses and forbs from November 2015 to June 2016 on farmland southwest of Córdoba (Spain) near the Guadalquivir River (37.829741° N, 4.905091° W). The site is part of an agricultural area for the production of herbaceous crops and orange orchards. The field trials were conducted in a flat, uniform field with a single soil type (sandy loam). The plots were arranged as randomized blocks with three repetitions for each species (Supplementary Fig. 1). The sowing of grasses and forbs took place on three consecutive days starting on 30 November 2015. A lawn roller was used to increase the soil–seed contact. For comparative purposes, we also sowed a commercial variety of Italian ryegrass (Lolium multiflorum Lam. var. westerwoldicum Wittm), which is widely available in the seed market of Mediterranean countries and one of the first choices of olive farmers for ground cover. To assess traits important to mechanized seed farming, we monitored the development and seedling establishment of the recruits every two weeks. We also monitored plant development and provided supplemental irrigation (~20 l m−2) two times during spring 2016 to ensure that the plants completed their cycle in dry periods. This is a common practice in rain-fed agriculture, and it is also the regular procedure for seed farming in the study area.
We adapted the Biologische Bundesanstalt, Bundessortenamt und Chemische Industrie system36 to code the phenological growth stages of both forbs and grasses. We then recorded growth habits to determine the suitability for mechanized harvest and measured two quantitative traits that cannot be inferred from the literature: (1) minimum fruit height above the soil when the seeds are about to disperse, which determines the feasibility of mechanical harvesting, and (2) seed yield as the seed number per m2. For the grasses, the number of seeds was calculated from the number of spikes counted in 1 m2 and the average number of seeds per spike found in 10 single spikes for each species and each replicate. For the forbs, we estimated the number of seeds from the total weight per lot and species, using the 1,000-seed-weight ratio provided by the Seed Information Database37. Three forb species (Anarrhinum bellidifolium, Helianthemum ledifolium and Tuberaria guttata) and two grass species (Aegilops geniculata and A. triuncialis) did not grow well for measuring agronomic traits; therefore, they were not further evaluated.
Scoring native plants on the basis of seed collection or biological attributes is a method to optimize the use of seed lots for restoration38. Here we used the free software DEXi v.5.00 (ref. 39) to estimate the potential suitability of the 40 evaluated grasses and forbs for both olive farming and seed farming, on the basis of ecological and production traits, respectively. DEXi has been used to support complex decision-making where factors may be competing, including agroecological applications40. The program uses the following as fundamental terms: options, attributes, values, functions and evaluations. Options are the possible selections; in this case, each native species. An attribute is a characteristic of interest. For each attribute, an option has a value, which is organized as a qualitative scale: low, medium and high. We first defined and organized 16 attributes on the basis of the existing literature (see Supplementary Table 1 and references) for both grasses and forbs, namely: (1) trafficability (plant height), (2) seasonal growth, (3) growth habit, (4) non-competitive for water, (5) non-competitive for nitrogen, (6) non-host for the Verticillium pathogen, (7) seed size, (8) seed shape, (9) fruit height, (10) harvest window, (11) seed dehiscence (separation from fruits), (12) seed separation (from inert material), (13) fruit shattering, (14) dispersal window, (15) seed yield and (16) demand in the market. We then input these to DEXi to build a hierarchy of base attributes (which we input data values for) and aggregated attributes (traits) in two major functions: suitability for olive farming (on the basis of ecological traits, 1–6) and suitability for seed farming (on the basis of production traits, 7–16). Once the branch structure was defined, we created a scale for each attribute (for example, Poor, Fair, Good, Excellent) and input the values for each option. The attributes were assigned on the basis of data from the literature or from our laboratory and agricultural experiments (see ‘Data availability’). For each aggregate attribute, we defined a matrix of function rules, which DEXi uses to calculate the value of the aggregate attribute using the default parameters. Although DEXi is based on qualitative attributes, it calculates indirect weights for setting a utility function to find a multicriteria solution. We ran the software to generate the suitability index for olive farming, seed farming and their combination.
Further information on research design is available in the Nature Research Reporting Summary linked to this article.
The data for species pools, production traits (numerical) and species assessments and a copy of the DEXi evaluation file are archived at https://doi.org/10.5281/zenodo.3460431.
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We thank M. Hernández González for his support on the review of ground cover species and on lab and field work. This research was funded by the PEOPLE/Marie Curie Actions of the European Union’s Seventh Framework Programme FP7/2007-2013 under REA grant agreement number 607785 through the ITN project NASSTEC (www.nasstec.eu). B.J.-A. was further supported by the Marie Curie Clarín-COFUND programme of the Principality of Asturias and the European Union (ACB17-26) and the Asturias regional grant number FC-GRUPIN-IDI/2018/000151.
C.G.-R. is the head of a private company producing native seeds for ecological restoration.
Peer review information Nature Plants thanks Michael Perring and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
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Jiménez-Alfaro, B., Frischie, S., Stolz, J. et al. Native plants for greening Mediterranean agroecosystems. Nat. Plants 6, 209–214 (2020). https://doi.org/10.1038/s41477-020-0617-3
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