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Understanding the combined effects of soil amendments and inoculation of mycorrhizal fungi on the response of different plant species during the phytostabilization process of trace elements contaminated soils is a challenge. This task is more difficult, but more realistic, when the study is carried out under field conditions.

A research team of the IRNAS-CSIC, in collaboration with researchers from EEZ-CSIC, has assessed the combined effects of two amendment doses (high and low doses) and mycorrhizal inoculation on the response of saplings of wild olive and stone pine, planted in a contaminated field site. The amendments were a mix of sugarbeet lime and biosolid compost. The inoculation treatments were made with a commercial inoculum of arbuscular mycorrhizal fungi for wild olive, while we used ectomycorrhizal fungi for stone pine. The experimental plot was located at the Guadiamar Green Corridor (Sevilla).

Results showed a weak or null effect of the mycorrhizal inoculation on plant growth, survival and trace element accumulation. There was only a significant increase on P nutrition for stone pine, growing on non-amended conditions. In general, the positive effect of mycorrhizal colonization on P nutrition is more evident under stress conditions and it can disappear under more favourable soil conditions.

The soil amendments were very effective reducing trace elements availability and their accumulation in both plant species, especially in roots. However, the effects on plant biomass were species-dependent and contrasted; low-dose amendments (30 T ha-1) increased the biomass of wild olive by 33.3%, but reduced by 28% that of pine. On the other hand, the high doses of amendments (60 T ha-1) produced some negative effects on plant growth and nutrition, probably related to the increase of soil salinity.

Both plant species, stone pine and wild olive, have been proved to be adequate for phytostabilization of contaminated soils under Mediterranean climate, due to their tolerance to drought and metals, and the low transfer of trace elements from root to shoot, thus reducing toxicity for the food web.

As a conclusion of this study, we highlight the importance of implementing microbial-assisted phytoremediation approaches, for which a better understanding of the diversity and ecology of plant-associated microorganisms is needed. The use of indigenous mycorrhizal fungi, locally adapted and tolerant to contamination, will favour to reach the phytostabilization purposes.

This study has been published in the Science of the Total Environment:

Madejón, P., Navarro-Fernández, C.M., Madejón, E., López-García, A., Marañón, T. (2021). Plant response to mycorrhizal inoculation and amendments on a contaminated soil, Science of the Total Environment, vol. 789, art. 147943.

The different plant strategies in the use of resources can be aligned on an economics spectrum, resulting from the trade-off between maximizing growth and resource capture (acquisitive strategy) versus the conservative strategy, with more protected organs of longer life span. Within this context, it is of great relevance to know the amount of photosynthate inverted by the plant on the construction of fine roots to explore the soil and uptake water and nutrients.

          A research team from the University of Cordoba, in collaboration with IRNAS-CSIC, CEBAS-CSIC and the University of Brandenburg-Cottbus, has studied the components of the construction costs (carbon, minerals and nitrogen concentrations) of the fine roots (< 2mm diameter) for 60 Mediterranean woody species.           The type of association with symbiotic microbes influenced on the contribution of different components in the root construction costs. Thus, the concentration of minerals was more important for the roots of plants associated with ectomycorrhizal fungi (EcM), while the organic nitrogen was dominant in roots associated with rhizobial N-fixing species. Therefore, the specific resource-use strategy associated to each type of symbiont modulate the trade-off between structural and metabolic compounds, during the building of roots.

Environmental conditions also influenced on the root construction costs. In nutrient-poor soils the energy spent per unit of root mass by plants was greater than the root cost in more fertile and favourable conditions. Plant species able to tolerate stress caused by water and nutrient scarcity often have a conservative strategy in the use of resources, with more costly roots of longer life span.   

In conclusion, the root construction cost is a key functional trait for terrestrial plants, related with their strategies in the use of resources, the type of associations with symbiotic microorganisms, and with the availability of soil water and nutrients.

This study has been published on line the 7 February 2021 in the Journal of Ecology:

de la Riva EG, Prieto I, Marañón T, Pérez‐Ramos IM, Olmo M, Villar R (2021). Root economics spectrum and construction costs in Mediterranean woody plants: The role of symbiotic associations and the environment. Journal of Ecology , 109: 1873-1885.‐2745.13612

The restoration of old mining areas, in particular if they are located near towns or villages, is essential to reduce their potential risks for human health and to minimize their visual impacts.

In this study, a research team of the IRNAS-CSIC, in collaboration with researchers from the University of Seville and the Environmental and Water Agency of the Regional Government of Andalusia (AMAYA), has assessed the effectiveness of the rehabilitation of an old waste rock pile (named Cabezo de los Gatos), derived from the mining activity, adjacent to the town of Tharsis (SW Spain).

The rehabilitation process, carried out twelve years ago, consisted in the reshape of the rock pile slope, followed by the application of limestone amendments and subsequent application of a topsoil layer. Finally, the revegetation of the area was implemented planting native shrubs and trees; in addition, a mixture of native grasses and shrubs was hydroseeded onto the remediated area.

In general, the applied measures were successful, covering with woody vegetation the upper part of the waste rock pile, and providing a greening visual landscape for the inhabitants of the town nearby. Moreover, the levels of trace elements contents in the aerial part of the vegetation growing in the upper of the slope were below the toxicity thresholds for the livestock potentially consuming them. In contrast, the lower part of the slope was almost devoid of vegetation. In addition, some plants, like the gum rose (Cistus ladanifer), growing at the base of the rock pile, had concentrations of Cd above the maximum tolerable level for animals, therefore representing a toxicity risk.

We interpret that partial failure in the rehabilitation process as due to the acid mine drainage, which caused downslope a decrease of soil pH and the consequent increased availability of trace elements, resulting in the accumulation of potentially toxic elements in the aerial parts of the plants. This contamination reduced the growth and establishment of plants, diminishing the vegetation cover.

To cope with the problem of acid mine drainage we propose an alternative approach to restore waste rock piles. We suggest to select extractive wastes and to place the non-acid generating ones around the periphery of the rock pile, as a protective cover. Thus, reducing infiltration rates, seepages and the negative effect of the acid mine drainage.

This study has been published in the Journal of Environmental Management:

Madejón, P., Caro-Moreno, D., Navarro-Fernández, C.M., Rossini-Oliva, S., Marañón, T. (2021) Rehabilitation of waste rock piles: Impact of acid drainage on potential toxicity by trace elements in plants and soil. Journal of Environmental Management, 280, art. no. 111848.

Fungi are a fundamental component of the soil microbiome, with essential ecosystem functions. They contribute to the nutrient cycling, through the organic matter decomposition; forming symbiotic associations with plants (mycorrhizas) they allow to explore a greater volume of soil to capture water and nutrients; on the other hand, pathogen fungi regulate plant populations.

A research team of the IRNAS-CSIC, in collaboration with researchers from the universities of Seville, Jaén and Copenhagen, has studied the soil fungal diversity and its relations with tree species in the Guadiamar Green Corridor (Seville, Spain). This area was remediated and afforested after a mine-spill contamination episode in 1998.   

Using high-throughput sequencing of environmental DNA allowed to identify more than 9,000 different fungal “species” (OTUs, operational taxonomic units) in 50 soil samples from two contrasted sites in the Green Corridor. In the South site (Quema), the highest fungal diversity was found under white poplar (Populus alba), with average of 1,168 species per tree, belonging to 141 different families. While under wild olives (Olea europaea var. sylvestris), the average diversity was 599 species of 95 families. In contrast, non-remediated soils, where the mine sludge was not cleaned up, and were not remediated neither afforested, had a low fungal diversity: average of only 51 species per sample and 20 families. Although these fungal species have interest due to their tolerance to extreme conditions of soil acidity and high concentration of potentially toxic elements.       

Venn diagram with fungal diversity in each habitat type.

We start to discover the magnitude of the soil biodiversity: hundreds or thousands of species in each sample, but we still ignore the functionality of all those species. The comparison with the existing database -FUNguild- allowed to assign the functional group for a 13.6% of the species recorded in the Green Corridor study. Within this representative sample (1,283 species), the dominant functional group was the saprothrophs fungi, which decompose organic matter and contribute to nutrient cycling, and were more tied to wild olive and grassland soils. The second most abundant group was the plant pathogens, mainly found in non-remediated soils. The third group, ectomycorrhizal fungi, was especially abundant in soils under trees, like pines and poplars, forming symbiotic associations with them.     

Tree planting to recover contaminated soils (phytoremediation) increases soil fungal diversity, in particular of ectomycorrhizal fungi. Restoring with different tree species, so forming a mixed forest, increases the spatial heterogeneity of environmental conditions; in consequence, the soil fungal biodiversity will be higher and the ecosystem services in the phytoremediated area will be promoted.

The study has been published in the journal Soil Biology and Biochemistry:

Gil-Martínez M, López-García Á, Domínguez MT, Kjøller R, Navarro-Fernández CM, Rosendahl S, Marañón T (2021). Soil fungal diversity and functionality are driven by plant species used in phytoremediation. Soil Biology and Biochemistry, 153: 108102.

Root functions are multiple and essential for plant growth and survival. They include nutrient and water acquisition, resource storage, support of symbiotic soil microbes and anchorage. At the ecosystem level, they contribute to soil structure and to the carbon and nutrient cycles.

Researchers of the IRNAS-CSIC, in collaboration with the University of Seville and the University of Cordoba, have studied the variation of 27 root traits (morphological, chemical and isotopic) in seven tree species planted in the Guadiamar Green Corridor (Seville, Spain). Three of the species are deciduous: white poplar (Populus alba), narrow-leafed ash (Fraxinus angustifolia) and hackberry (Celtis autralis). While the other four species are evergreen: stone pine (Pinus pinea), holm oak (Quercus ilex), wild olive (Olea europaea) and carob (Ceratonia siliqua).

The main variation trend observed in the root traits supports the “root economics spectrum” hypothesis. There is a trade-off between tree species having lighter roots and higher length per mass unit, which maximizes soil resource acquisition and thus they grow faster on favourable conditions. On the contrary, tree species with denser roots and lower specific length tend to have resource conservation and slower growth, on adverse conditions.

Besides the main trend, there are other dimensions reflecting the root multifunctionality. 1) The root carbon concentration was not correlated with the morphological variables. 2) the ability to bind trace elements (for example, Pb and Cd) to root cells tends to be associated with the plant tolerance to soil contamination by metals. 3) The fractionation of 15N in roots is a time-integrated trait of mycorrhizal mediated nutrition.

In general, roots and leaves are functionally coordinated. The fast acquisition and processing of water and nutrients by the roots must be coupled with fast acquisition and processing of carbon by leaves. However, there was strong discordance between roots and leaves, with regards to the accumulation of several trace elements.

Soil conditions, and metal contamination in particular, affect morphological and chemical traits of tree roots. There are reciprocal interactions and feedback processes between soil and tree roots.

A remarkable physiological trait for these tree roots is the capacity to diminish the availability of trace elements into the soil, in special of those potentially toxic (Cd, Pb, As). We recommend planting trees with high “phytostabilisation” potential to remediate metal-contaminated soils.

This study has been published in the April issue of the journal Plant and Soil:

Marañón, T., Navarro-Fernández, C. M., Gil-Martínez, M., Domínguez, M. T., Madejón, P., Villar, R. (2020). Variation in morphological and chemical traits of Mediterranean tree roots: linkage with leaf traits and soil conditions. Plant and Soil, 449: 389-403.

The assessment and evaluation of ecosystem services is a valuable tool to support and justify sustainble soil management.

Researchers of IRNAS, CSIC have contributed to the development of a methodology to quantify changes in ecosystem services induced by soil management measures, as part of the European RECARE consortium.

A comparative analysis of the results for 26 measures applied to remediate degraded soils, in 16 case studies across Europe, has been carried out. In particular, IRNAS´s researchers have evaluated the results of amendments (biosolid compost) and tree planting (wild olive) in contaminated and remediated soils of the Guadiamar Green Corridor.

The new methodology was applied to evaluate the impacts of each 26 measures on different ecosystem services. The most relevant 15 ecosystem services were selected, grouped in provisioning, regulation and cultural services. In general, the applied soil remediation measures produced positive changes in ecosystem services. Within the regulation services, “mediation of flows” (protection from erosion) and “mediation of waste, toxics and other nuisances” (stabilization of contaminants) showed the most important positive impacts.

The methodology also detected synergies and trade-offs among ecosystem services. This holistic approach may be the base for a valuation of the benefits from each ecosystem service and the integrated management of the evaluated land.

The results have been published in the December issue of the open access journal Sustainability:

Gudrun Schwilch, Tatenda Lemann, Örjan Berglund, Carlo Camarotto, Artemi Cerdà, Ioannis N. Daliakopoulos, Silvia Kohnová, Dominika Krzeminska, Teodoro Marañón, René Rietra, Grzegorz Siebielec, Johann Thorsson, Mark Tibbett, Sandra Valente, Hedwig van Delden, Jan van den Akker, Simone Verzandvoort, Nicoleta Olimpia Vrînceanu, Christos Zoumides, Rudi Hessel (2018), Assessing impacts of soil management measures on Ecosystem Services. Sustainability, 10 (12), 4416, doi:10.3390/su10124416.

Soil abiotic properties, such as texture, nutrient availability and water, are essential in the development of terrestrial plants. Mycorrhizal fungi, which are fungi living in symbiosis with plants roots, are also key for plant growing. This symbiosis enhances a trade-off of carbohydrates and nutrients beneficial for both plant and fungi. Therefore, it is expected that different mycorrhizal fungal communities (in terms of species and their morphological traits) would affect plant development (in terms of plant chemical and morphological traits) in different ways.

In order to understand this mycorrhizal fungi-plant relationship, researchers from IRNAS-CSIC and Universidad de Sevilla (Spain), in collaboration with researchers from the University of Copenhagen (Denmark) and the University of Reading (United Kingdom), developed a study on holm oak trees and their symbiotic ectomycorrhizal fungi. The area selected for this study, known as the Guadiamar Green Corridor (Seville), suffered a mine spill leaving behind hectares of land contaminated by trace elements. Twenty years after the accident and the phytoremediation of the affected area, trace elements are still present and the role of ectomycorrhizal fungi might be especially important in this stressful environment.

In this study, we found that ectomycorrhizal fungi explained more than soil abiotic properties for most of the measured plant traits, especially root functional traits. The symbiosis with abundant species of ectomycorrhizal fungi (Hebeloma cavipes and Thelephora terrestris) was related to conservative positions into the root economics spectrum. Conservative traits, like denser roots and higher dry matter content, allow tree survival under adverse conditions. Hebeloma cavipes and Thelephora terrestris were characterised with a high rhizomorph formation, a fungal trait that enhances water and phosphate uptake through a long-distance exploration mechanism. It may be possible that this specific tree-fungi symbiosis was established as a consequence of resource limitations.

Trace element mobility through the soil-root-leaf continuum was analysed and despite soil trace elements concentrations in our environmental gradient was relatively large, accumulation of trace elements in oak leaves was relatively low. This confirms that holm oak is a suitable species for the phytostabilisation of contaminated soils, given its ability to prevent trace element accumulation into aboveground biomass. However, it is not the role of the tree alone, as trace element transfer was highly explained by its associated ectomycorrhizal fungal communities, which suggests that interactions with fungi play an important role at determining the capacity of this tree species to retain trace elements into its roots.

These findings support that ectomycorrhizal fungal community composition and their functional traits mediate plant performance in trace element contaminated soils, and have a high influence on plant capacity for phytoremediation of contaminants.

The study has been published in the journal Frontiers in Plant Science:

Gil-Martínez, M., López-García, Á., Domínguez, M. T., Navarro-Fernández, C. M., Kjøller, R., Tibbett, M., & Marañón, T. (2018). Ectomycorrhizal Fungal Communities and Their Functional Traits Mediate Plant–Soil Interactions in Trace Element Contaminated Soils. Frontiers in Plant Science, 9, 1682.