Raúl Ochoa-Hueso

Dr. Raúl Ochoa-Hueso PhD

Honorary Fellow
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Visiting Address

Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands

About

I study the effects of global change on the biodiversity of terrestrial ecosystems and their functioning. I am also interested in the concept of coupling to understand the myriad of interconnections that allow the maintenance of functional ecosystems.

Biography

I am an ecosystem ecologist with extensive experience researching about the consequences of human impacts on biogeochemical processes, biodiversity, and the assembly of communities in terrestrial ecosystems. Currently, I am a Ramón y Cajal researcher at the University of Cádiz, Spain, where I lead the "Ecosystem Ecology Lab" (https://ecosystemsecology.com/). The laboratory seeks to answer basic questions on how ecosystems function in a context of global change and develop applied nature-based strategies to stop or even reverse impacts, particularly in the context of managed ecosystems such as grasslands and agroecosystems like vineyards. 

Publications

Peer-reviewed publications

  • Science advances
    05-07-2024

    Carbon-phosphorus cycle models overestimate CO 2 enrichment response in a mature Eucalyptus forest

    Mingkai Jiang, Belinda E. Medlyn, David Wårlind, Jürgen Knauer, Katrin Fleischer, Daniel S. Goll, Stefan Olin, Xiaojuan Yang, Lin Yu, Sönke Zaehle, Haicheng Zhang, He Lv, Kristine Y. Crous, Yolima Carrillo, Catriona A. Macdonald, Ian C. Anderson, Matthias M. Boer, Mark Farrell, Andrew N. Gherlenda, Laura Castañeda-Gómez, Shun Hasegawa, Klaus Jarosch, Paul J. Milham, Raul Ochoa-Hueso, Varsha Pathare, Johanna Pihlblad, Juan Piñeiro Nevado, Jeff R. Powell, Sally A. Power, Peter B. Reich, Markus Riegler, David S. Ellsworth, Benjamin Smith
    The importance of phosphorus (P) in regulating ecosystem responses to climate change has fostered P-cycle implementation in land surface models, but their CO2 effects predictions have not been evaluated against measurements. Here, we perform a data-driven model evaluation where simulations of eight widely used P-enabled models were confronted with observations from a long-term free-air CO2 enrichment experiment in a mature, P-limited Eucalyptus forest. We show that most models predicted the correct sign and magnitude of the CO2 effect on ecosystem carbon (C) sequestration, but they generally overestimated the effects on plant C uptake and growth. We identify leaf-to-canopy scaling of photosynthesis, plant tissue stoichiometry, plant belowground C allocation, and the subsequent consequences for plant-microbial interaction as key areas in which models of ecosystem C-P interaction can be improved. Together, this data-model intercomparison reveals data-driven insights into the performance and functionality of P-enabled models and adds to the existing evidence that the global CO2-driven carbon sink is overestimated by models.
    https://doi.org/10.1126/sciadv.adl5822
  • Ecosystems
    12-06-2024

    Plant Multi-element Coupling as an Indicator of Nutritional Mismatches Under Global Change

    Raul Ochoa-Hueso, Juan Piñeiro, Lidia Gómez Morán, Lilia Serrano, Sally A. Power

    Global biogeochemical cycles have been widely altered due to human activities, potentially compromising the ability of plants to regulate their metabolism. We grew experimental herbaceous communities simulating the understory of eucalypt forests from southeastern Australia to evaluate the effects of elevated CO2 (400 vs. 650 ppm) and changes in soil resource availability (high-low water and high-low P) on the concentration of fourteen essential plant macro- and micronutrients, and their degree of coupling. Coupling was based on correlations among all elements in absolute value and a null modeling approach. According to the ancient nature of Australian soils, P addition was the main driver of changes in plant tissue chemistry, increasing the concentrations of P, Mg, Ca, and Mn and reducing the concentrations of C, N, S, Na, and Cu. Most treatment combinations showed coupled patterns of plant elements, particularly under ambient CO2. However, under elevated CO2, elements in plant tissues became more decoupled, which was interpreted as the result of a lack of enough supply of a range of elements to satisfy greater demands. Across treatments, P, Mn, and N were the least coupled elements, while K, Ca, and Fe were the most coupled ones. We provide evidence that plant element coupling was positively related to the concentration and coupling of elements measured in soils worldwide, suggesting that plant element coupling is conserved. Our results provide compelling evidence that evaluating the coupling of a representative range of chemical elements in plant tissues may represent a highly novel and powerful indicator of nutritional mismatches between demand and supply under specific environmental circumstances, including in a resource-altered global change context.

    https://doi.org/10.1007/s10021-024-00914-z
  • Nature
    05-06-2024

    Microbial competition for phosphorus limits the CO2 response of a mature forest

    Mingkai Jiang, Kristine Y. Crous, Yolima Carrillo, Catriona A. Macdonald, Ian C. Anderson, Matthias M. Boer, Mark Farrell, Andrew N. Gherlenda, Laura Castañeda-Gómez, Shun Hasegawa, Klaus Jarosch, Paul J. Milham, Raul Ochoa-Hueso, Varsha Pathare, Johanna Pihlblad, Juan Piñeiro, Jeff R. Powell, Sally A. Power, Peter B. Reich, Markus Riegler, Sönke Zaehle, Benjamin Smith, Belinda E. Medlyn, David S. Ellsworth
    The capacity for terrestrial ecosystems to sequester additional carbon (C) with rising CO2 concentrations depends on soil nutrient availability1,2. Previous evidence suggested that mature forests growing on phosphorus (P)-deprived soils had limited capacity to sequester extra biomass under elevated CO2 (refs. 3,4,5,6), but uncertainty about ecosystem P cycling and its CO2 response represents a crucial bottleneck for mechanistic prediction of the land C sink under climate change7. Here, by compiling the first comprehensive P budget for a P-limited mature forest exposed to elevated CO2, we show a high likelihood that P captured by soil microorganisms constrains ecosystem P recycling and availability for plant uptake. Trees used P efficiently, but microbial pre-emption of mineralized soil P seemed to limit the capacity of trees for increased P uptake and assimilation under elevated CO2 and, therefore, their capacity to sequester extra C. Plant strategies to stimulate microbial P cycling and plant P uptake, such as increasing rhizosphere C release to soil, will probably be necessary for P-limited forests to increase C capture into new biomass. Our results identify the key mechanisms by which P availability limits CO2 fertilization of tree growth and will guide the development of Earth system models to predict future long-term C storage.
    https://doi.org/10.1038/s41586-024-07491-0
  • Agriculture, Ecosystems and Environment
    01-06-2024

    Abandonment of traditional livestock grazing reduces soil fertility and enzyme activity, alters soil microbial communities, and decouples microbial networks, with consequences for forage quality in Mediterranean grasslands

    Antonio Requena Serrano, Begoña Peco, José A. Morillo, Raul Ochoa-Hueso

    Extensive livestock grazing is a global human activity. In the Iberian Peninsula, extensive grazing and seminatural grasslands and open woodlands such as dehesas have co-evolved with human use for millennia. However, social, demographic, and economic factors are now pushing this traditional activity towards both conventional intensification and land abandonment, with consequences for the biodiversity and functioning of these seminatural ecosystems. Soils can be particularly affected by grazing abandonment due to the cessation of inputs of pre-processed organic matter (dungs and urine) and of trampling, with still poorly understood consequences for the composition, network configuration, and activity of soil microbial communities and the capacity of soils to store C. In this work, we used 20 pairs of adjacent plots (40 plots in total) located in seminatural grasslands from central Spain. For each pair, one plot was extensively grazed by livestock and the other one was abandoned. We evaluated the effects of extensive grazing abandonment on soil fertility (C and N contents, and P and K bioavailability), forage quality (fibre and protein content), and soil microbial community composition (amplicon sequencing of 16 S [bacteria] and ITS [fungi]), network coupling, and activity (extracellular hydrolytic enzymes linked to the biogeochemical cycling of C, N, P, and S). Grazing resulted in higher soil fertility in terms of C, N, and P, and grassland forage quality (lower fibre). Grazing also affected soil microbial community composition, but not richness or diversity. These effects occurred primarily through changes in nutrients and soil water availability. Actinobacteria significantly increased in abandoned plots, while Acidobacteria, Verrucomicrobia, and Planctomycetes decreased. Bacterial and, particularly, fungal networks were generally less coupled in abandoned plots. Furthermore, grazing resulted in greater soil enzyme activity via direct effects. These results support the notion that extensive grazing with intermediate stocking rates provides a positive effect on grass quality, soil fertility, nutrient cycling, and microbial network configuration, and thus warn about the potential negative effects of land abandonment.

    https://doi.org/10.1016/j.agee.2024.108932
  • Global Change Biology
    28-05-2024

    Unearthing the soil‐borne microbiome of land plants

    Raul Ochoa-Hueso, David J Eldridge, Miguel Berdugo, Pankaj Trivedi, Blessing Sokoya, Concha Cano‐Díaz, Sebastian Abades, Fernando Alfaro, Adebola R. Bamigboye, Felipe Bastida, José Luis Blanco-Pastor, Asunción de los Rios, Jorge Durán, Stefan Geisen, Tine Grebenc, Javier G. Illán, Yu Rong Liu, Thulani P. Makhalanyane, Steven Mamet, Marco A. Molina‐Montenegro, José L. Moreno, Tina Unuk Nahberger, Gabriel F. Peñaloza‐Bojacá, César Plaza, Ana Rey, Alexandra Rodríguez, Christina Siebe, Brajesh K. Singh, Alberto L. Teixido, Cristian Torres‐Díaz, Ling Wang, Jianyong Wang, Juntao Wang, Eli Zaady, Xiaobing Zhou, Xin‐Quan Zhou, Leho Tedersoo, Manuel Delgado-Baquerizo
    Plant–soil biodiversity interactions are fundamental for the functioning of terrestrial ecosystems. Yet, the existence of a set of globally distributed topsoil microbial and small invertebrate organisms consistently associated with land plants (i.e., their consistent soil-borne microbiome), together with the environmental preferences and functional capabilities of these organisms, remains unknown. We conducted a standardized field survey under 150 species of land plants, including 58 species of bryophytes and 92 of vascular plants, across 124 locations from all continents. We found that, despite the immense biodiversity of soil organisms, the land plants evaluated only shared a small fraction (less than 1%) of all microbial and invertebrate taxa that were present across contrasting climatic and soil conditions and vegetation types. These consistent taxa were dominated by generalist decomposers and phagotrophs and their presence was positively correlated with the abundance of functional genes linked to mineralization. Finally, we showed that crossing environmental thresholds in aridity (aridity index of 0.65, i.e., the transition from mesic to dry ecosystems), soil pH (5.5; i.e., the transition from acidic to strongly acidic soils), and carbon (less than 2%, the lower limit of fertile soils) can result in drastic disruptions in the associations between land plants and soil organisms, with potential implications for the delivery of soil ecosystem processes under ongoing global environmental change.
    https://doi.org/10.1111/gcb.17295
  • Plant and Soil
    05-04-2024

    Soil elemental cycles become more coupled in response to increased nitrogen deposition in a semiarid shrubland

    Cristina Caetano-Sánchez, Juan Piñero, Raul Ochoa-Hueso

    Background and aims: Increased N deposition can break the coupled associations among chemical elements in soil, many of which are essential plant nutrients. We evaluated the effects of four years of N deposition (0, 10, 20, 50 kg N ha−1 yr−1) on the temporal dynamics of the spatial co-variation (i.e., coupling) among ten chemical elements in soils from a semiarid shrubland in central Spain. Methods: Soil element coupling was calculated as the mean of Spearman rank correlation coefficients of all possible pairwise interactions among elemental cycles, in absolute value. We also investigated the role of atomic properties of elements as regulators of coupling. Results: While N deposition impacts on nutrient bioavailability were variable, soil elemental coupling consistently increased in response to N. Coupling responses also varied among elements and N treatments, and four out of ten elemental cycles also responded to N in a season-dependent manner. Atomic properties of elements such as mass, valence orbitals, and electronegativity contributed to explain the spatial coupling of soil elements, most likely due their role on the capacity of elements to interact with one another. Conclusions: The cumulative effects of N deposition can alter the spatial associations among chemical elements in soils, while not having evident consequences on the bioavailability of single elments. These results indicate that considering how multiple elements co-vary in topsoils may provide a useful framework to better understand the simultaneous response of multiple elemental cycles to global change.

    https://doi.org/10.1007/s11104-024-06644-4
  • Global Change Biology
    16-03-2024

    Depth‐dependent responses of soil organic carbon under nitrogen deposition

    Yuanliu Hu, Qi Deng, Thomas Kätterer, Jørgen E. Olesen, Samantha C. Ying, Raul Ochoa-Hueso, Carsten W. Mueller, Michael N. Weintraub, Ji Chen
    Emerging evidence points out that the responses of soil organic carbon (SOC) to nitrogen (N) addition differ along the soil profile, highlighting the importance of synthesizing results from different soil layers. Here, using a global meta-analysis, we found that N addition significantly enhanced topsoil (0–30 cm) SOC by 3.7% (±1.4%) in forests and grasslands. In contrast, SOC in the subsoil (30–100 cm) initially increased with N addition but decreased over time. The model selection analysis revealed that experimental duration and vegetation type are among the most important predictors across a wide range of climatic, environmental, and edaphic variables. The contrasting responses of SOC to N addition indicate the importance of considering deep soil layers, particularly for long-term continuous N deposition. Finally, the lack of depth-dependent SOC responses to N addition in experimental and modeling frameworks has likely resulted in the overestimation of changes in SOC storage under enhanced N deposition.
    https://doi.org/10.1111/gcb.17247
  • Current Biology
    23-10-2023

    Ecosystem consequences of invertebrate decline

    Nico Eisenhauer, Raul Ochoa-Hueso, Yuanyuan Huang, Kathryn E. Barry, Alban Gebler, Carlos A. Guerra, Jes Hines, Malte Jochum, Karl Andraczek, Solveig Franziska Bucher, François Buscot, Marcel Ciobanu, Hongmei Chen, Robert R. Junker, Markus Lange, Anika Lehmann, Matthias C Rillig, Christine Römermann, Josephine Ulrich, Alexandra Weigelt, Anja Schmidt, Manfred Türke

    Human activities cause substantial changes in biodiversity.1,2 Despite ongoing concern about the implications of invertebrate decline,3,4,5,6,7 few empirical studies have examined the ecosystem consequences of invertebrate biomass loss. Here, we test the responses of six ecosystem services informed by 30 above- and belowground ecosystem variables to three levels of aboveground (i.e., vegetation associated) invertebrate community biomass (100%, 36%, and 0% of ambient biomass) in experimental grassland mesocosms in a controlled Ecotron facility. In line with recent reports on invertebrate biomass loss over the last decade, our 36% biomass treatment also represented a decrease in invertebrate abundance (−70%) and richness (−44%). Moreover, we simulated the pronounced change in invertebrate biomass and turnover in community composition across the season. We found that the loss of invertebrate biomass decreases ecosystem multifunctionality, including two critical ecosystem services, aboveground pest control and belowground decomposition, while harvested plant biomass increases, likely because less energy was channeled up the food chain. Moreover, communities and ecosystem functions become decoupled with a lower biomass of invertebrates. Our study shows that invertebrate loss threatens the integrity of grasslands by decoupling ecosystem processes and decreasing ecosystem-service supply.

    https://doi.org/10.1016/j.cub.2023.09.012
  • Global Change Biology
    14-08-2023

    Litter and soil biodiversity jointly drive ecosystem functions

    Shengen Liu, César Plaza, Raul Ochoa-Hueso, Chanda Trivedi, Juntao Wang, Pankaj Trivedi, Guiyao Zhou, Juan Piñeiro, Catarina S. C. Martins, Brajesh K. Singh, Manuel Delgado-Baquerizo
    The decomposition of litter and the supply of nutrients into and from the soil are two fundamental processes through which the above- and belowground world interact. Microbial biodiversity, and especially that of decomposers, plays a key role in these processes by helping litter decomposition. Yet the relative contribution of litter diversity and soil biodiversity in supporting multiple ecosystem services remains virtually unknown. Here we conducted a mesocosm experiment where leaf litter and soil biodiversity were manipulated to investigate their influence on plant productivity, litter decomposition, soil respiration, and enzymatic activity in the littersphere. We showed that both leaf litter diversity and soil microbial diversity (richness and community composition) independently contributed to explain multiple ecosystem functions. Fungal saprobes community composition was especially important for supporting ecosystem multifunctionality (EMF), plant production, litter decomposition, and activity of soil phosphatase when compared with bacteria or other fungal functional groups and litter species richness. Moreover, leaf litter diversity and soil microbial diversity exerted previously undescribed and significantly interactive effects on EMF and multiple individual ecosystem functions, such as litter decomposition and plant production. Together, our work provides experimental evidence supporting the independent and interactive roles of litter and belowground soil biodiversity to maintain ecosystem functions and multiple services.
    https://doi.org/10.1111/gcb.16913
  • Global Biogeochemical Cycles
    06-2023

    Bioavailability of Macro and Micronutrients Across Global Topsoils

    Raul Ochoa-Hueso, Manuel Delgado-Baquerizo, Anita C. Risch, Louise A. Ashton, David Augustine, Nicolas Bélanger, Scott Bridgham, Andrea J. Britton, Viktor J. Bruckman, J. Julio Camarero, Gerard Cornelissen, John A. Crawford, Feike A. Dijkstra, Amanda Diochon, Stevan Earl, James Edgerley, Howard Epstein, Andrew Felton, Julien Fortier, Daniel Gagnon, Ken Greer, Hannah M. Griffiths, Caroline Halde, Hans Martin Hanslin, Lorna I. Harris, Jeremy A. Hartsock, Paul Hendrickson, Knut Anders Hovstad, Jia Hu, Arun D. Jani, Kelcy Kent, Deirdre Kerdraon-Byrne, Sat Darshan S. Khalsa, Derrick Y.F. Lai, France Lambert, Jalene M. LaMontagne, Stéphanie Lavergne, Beth A. Lawrence, Kim Littke, Abigail C. Leeper, Mark A. Licht, Mark A. Liebig, Joshua S. Lynn, Janet E. Maclean, Vegard Martinsen, Marshall D. McDaniel, Anne C.S. McIntosh, Jessica R. Miesel, Jim Miller, Michael J. Mulvaney, Gerardo Moreno, Laura Newstead, Robin J. Pakeman, Jan Pergl, Bradley D. Pinno, Juan Piñeiro, Kathleen Quigley, Troy M. Radtke, Paul Reed, Víctor Rolo, Jennifer Rudgers, P. Michael Rutherford, Emma J. Sayer, Lilia Serrano, Maria Strack, Nicole Sukdeo, Andy F.S. Taylor, Benoit Truax, Leonard J.S. Tsuji, Natasja van Gestel, Brenda M. Vaness, Kevin Van Sundert, Michaela Vítková, Robert Weigel, Meaghan J. Wilton, Yuriko Yano, Ewing Teen, Eric Bremer

    Understanding the chemical composition of our planet's crust was one of the biggest questions of the 20th century. More than 100 years later, we are still far from understanding the global patterns in the bioavailability and spatial coupling of elements in topsoils worldwide, despite their importance for the productivity and functioning of terrestrial ecosystems. Here, we measured the bioavailability and coupling of thirteen macro- and micronutrients and phytotoxic elements in topsoils (3–8 cm) from a range of terrestrial ecosystems across all continents (∼10,000 observations) and in response to global change manipulations (∼5,000 observations). For this, we incubated between 1 and 4 pairs of anionic and cationic exchange membranes per site for a mean period of 53 days. The most bioavailable elements (Ca, Mg, and K) were also amongst the most abundant in the crust. Patterns of bioavailability were biome-dependent and controlled by soil properties such as pH, organic matter content and texture, plant cover, and climate. However, global change simulations resulted in important alterations in the bioavailability of elements. Elements were highly coupled, and coupling was predictable by the atomic properties of elements, particularly mass, mass to charge ratio, and second ionization energy. Deviations from the predictable coupling-atomic mass relationship were attributed to global change and agriculture. Our work illustrates the tight links between the bioavailability and coupling of topsoil elements and environmental context, human activities, and atomic properties of elements, thus deeply enhancing our integrated understanding of the biogeochemical connections that underlie the productivity and functioning of terrestrial ecosystems in a changing world.

    https://doi.org/10.1029/2022GB007680
  • Nature Communications
    07-02-2023

    Globally invariant metabolism but density-diversity mismatch in springtails

    Anton M. Potapov, Carlos A. Guerra, Johan van den Hoogen, Anatoly Babenko, Bruno C. Bellini, Matty P. Berg, Steven L Chown, Louis Deharveng, Ľubomír Kováč, Natalia A. Kuznetsova, Jean-François Ponge, Mikhail B. Potapov, David J. Russell, Douglas Alexandre, Juha M. Alatalo, Javier I. Arbea, Ipsa Bandyopadhyaya, Verónica Bernava, Stef Bokhorst, Thomas Bolger, Gabriela Castaño-Meneses, Matthieu Chauvat, Ting Wen Chen, Mathilde Chomel, Aimée T. Classen, Jerome Cortet, Peter Čuchta, Ana Manuela de la Pedrosa, Susana S.D. Ferreira, Cristina Fiera, Juliane Filser, Oscar Franken, Saori Fujii, Essivi Gagnon Koudji, Meixiang Gao, Benoit Gendreau-Berthiaume, Diego F. Gomez-Pamies, Michelle Greve, I. Tanya Handa, Charlène Heiniger, Martin Holmstrup, Pablo Homet, Mari Ivask, Charlene Janion-Scheepers, Malte Jochum, Sophie Joimel, Bruna Claudia S Jorge, Edite Jucevica, Olga Ferlian, Luís Carlos Iuñes de Oliveira Filho, Osmar Klauberg-Filho, Dilmar Baretta, Eveline J. Krab, Annely Kuu, Estevam C.A. de Lima, Dunmei Lin, Zoë Lindo, Amy Liu, Jing Zhong Lu, María José Luciañez, Michael T. Marx, Matthew A. McCary, Maria A. Minor, Taizo Nakamori, Ilaria Negri, Raul Ochoa-Hueso, José G. Palacios-Vargas, Melanie M. Pollierer, Pascal Querner, Natália Raschmanová, Muhammad Imtiaz Rashid, Laura J. Raymond-Léonard, Laurent Rousseau, Ruslan A. Saifutdinov, Sandrine Salmon, Emma J. Sayer, Nicole Scheunemann, Cornelia Scholz, Julia Seeber, Yulia B. Shveenkova, Sophya K. Stebaeva, Maria Sterzynska, Xin Sun, Winda I. Susanti, Anastasia A. Taskaeva, Maddy Thakur, Maria A. Tsiafouli, Matthew S. Turnbull, Mthokozisi N. Twala, Alexei V. Uvarov, Lisa A. Venier, Lina A. Widenfalk, Bruna R. Winck, Daniel Winkler, Donghui Wu, Zhijing Xie, Rui Yin, Douglas Zeppelini, Tom Crowther, Nico Eisenhauer, Stefan Scheu

    Soil life supports the functioning and biodiversity of terrestrial ecosystems. Springtails (Collembola) are among the most abundant soil arthropods regulating soil fertility and flow of energy through above- and belowground food webs. However, the global distribution of springtail diversity and density, and how these relate to energy fluxes remains unknown. Here, using a global dataset representing 2470 sites, we estimate the total soil springtail biomass at 27.5 megatons carbon, which is threefold higher than wild terrestrial vertebrates, and record peak densities up to 2 million individuals per square meter in the tundra. Despite a 20-fold biomass difference between the tundra and the tropics, springtail energy use (community metabolism) remains similar across the latitudinal gradient, owing to the changes in temperature with latitude. Neither springtail density nor community metabolism is predicted by local species richness, which is high in the tropics, but comparably high in some temperate forests and even tundra. Changes in springtail activity may emerge from latitudinal gradients in temperature, predation and resource limitation in soil communities. Contrasting relationships of biomass, diversity and activity of springtail communities with temperature suggest that climate warming will alter fundamental soil biodiversity metrics in different directions, potentially restructuring terrestrial food webs and affecting soil functioning.

    https://doi.org/10.1038/s41467-023-36216-6
  • Functional Ecology
    2023

    Ecosystem-level decoupling in response to reduced precipitation frequency and degradation in steppe grassland

    Tianxue Yang, Xiaoyue Zhong, Junda Chen, Uffe N Nielsen, Raul Ochoa-Hueso, Yanan Qu, Yushu Sui, Weifeng Gao, Wei Sun

    Grasslands across arid and semi-arid regions are predicted to experience reductions in precipitation frequency. Besides, grassland degradation has become a serious problem in many of these areas. Despite increasing evidence suggesting compound effects of these synchronous alterations on biotic and abiotic ecosystem constituents, we still do not know how they will impact the coupling among ecosystem constituents and its consequences on ecosystem functioning. Here, we assessed the effects of decreased precipitation frequency and grassland degradation on ecosystem coupling, quantified based on the mean strength of pairwise correlations among multispecies communities and their physicochemical environment, individual functions and ecosystem multifunctionality, and reported their relationships within a mechanistic plant–nematode–micro-organism–soil interactions framework. Decreased precipitation frequency led to poorly coupled ecosystems, and reduced aboveground plant biomass, soil water content, soil nutrient levels, soil biota abundance and multifunctionality. By contrast, belowground plant biomass and soil potential enzyme activities increased under decreased precipitation frequency treatment. Severe degradation resulted in decoupled ecosystems and suppressed most of individual functions and multifunctionality. Using structural equation modelling, we showed that coupling had a strong direct positive effect on multifunctionality (standardized total effect: 0.74), while multifunctionality was weakened by greater soil water variation (−0.54) and higher soil pH (−0.53). The great sensitivity of ecosystem coupling to altered precipitation regimes and degradation highlights the importance of considering interactions among biotic and abiotic components when predicting early ecological impacts under changing environments. Moreover, the positive relationship between ecosystem coupling and functioning suggests that restoration of degraded grasslands may be achieved by intensifying ecological interactions.

    https://doi.org/10.1111/1365-2435.14425
  • Agriculture, Ecosystems and Environment
    01-11-2022

    Edaphoclimatic drivers of the effect of extensive vegetation management on ecosystem services and biodiversity in vineyards

    Carmen Chapela-Oliva, Silvia Winter, Raul Ochoa-Hueso

    Vineyards are a very important perennial woody crop globally, but they are also among the most intensively managed agroecosystems. This has resulted in biologically impoverished and highly eroded vineyards. Environmentally-friendly inter-row vegetation management, particularly the use of cover crops, could contribute to avoid erosion and regenerate soil biodiversity in vineyards. In this study, we updated a global meta-analysis on the effects of inter-row extensive vegetation cover management, particularly through the use of cover crops, on ecosystem services, including supporting, regulating and provisioning services, and biodiversity in vineyards. We also analyzed the role of environmental variables (climate, including precipitation- and temperature-related bioclimatic variables and soil properties, including pH and texture) and irrigation in modulating these effects. The presence of extensive vegetation cover consistently increased biodiversity, as well as supporting ecosystem services in irrigated vineyards and regulating services in rainfed vineyards. Provisioning services, which were evaluated as grape yield, were slightly negatively affected in rainfed vineyards, but not in irrigated ones. The effects of vegetation cover on ecosystem services varied depending on the climate and edaphic characteristics of vineyards. For example, supporting ecosystem services were favored in acidic soils and were also positively related to the precipitation of the wettest quarter, whereas regulating services were particularly enhanced in alkaline soils and in locations with lower temperatures of the wettest quarter. Biodiversity was especially favored in locations with lower precipitation seasonality. Taken together, our study indicates the importance of developing strategies for the adaptive management of extensive vegetation covers tailored to the climatic and edaphic conditions of each vineyard. This adaptive management, combined with irrigation and potentially other locally-tailored adaptive strategies, could also contribute to further mitigate potential negative effects of vegetation cover on grape production while maximizing other ecosystem services such as provisioning and supporting services and biodiversity.

    https://doi.org/10.1016/j.agee.2022.108115
  • Journal of Environmental Management
    2022

    Mowing enhances the positive effects of nitrogen addition on ecosystem carbon fluxes and water use efficiency in a semi-arid meadow steppe

    Wenzheng Song, Raul Ochoa-Hueso, Fei Li, Haiying Cui, Shangzhi Zhong, Xuechen Yang, Tianhang Zhao, Wei Sun

    Grasslands are now facing a continuously increasing supply of nitrogen (N) fertilizers, resulting in alterations in ecosystem functioning, including changes in carbon (C) and water cycling. Mowing, one of the most widely used grassland management techniques, has been shown to mitigate the negative impacts of increased N availability on species richness. However, knowledge of how N addition and mowing, alone and/or in combination, affect ecosystem-level C fluxes and water use efficiency (WN) is still limited. We experimentally manipulated N fertilization (0 and 10 g N m−2 yr−1) and mowing (once per year at the end of the growing season) following a randomized block design in a meadow steppe characterized by salinization and alkalinization in northeastern China. We found that, compared to the control plots, N addition, mowing, and their interaction increased net ecosystem CO2 exchange by 65.1%, 14.7%, and 133%, and WN by 40.7%, 18.5%, and 96.1%, respectively. Nitrogen enrichment also decreased soil pH, which resulted in greater aboveground biomass (AGB). Moreover, N addition indirectly increased AGB by inducing changes in species richness. Our results indicate that mowing enhances the positive effects of N addition on ecosystem C fluxes and WN. Therefore, appropriate grassland management practices are essential to improve ecosystem C sequestration, WN, and mitigate future species diversity declines due to ecosystem eutrophication.

    https://doi.org/10.1016/j.jenvman.2022.115889
  • Frontiers in Plant Science
    2022

    Application of biostimulant products and biological control agents in sustainable viticulture

    Keiji Jindo, Travis L. Goron, Paloma Pizarro-Tobías, Miguel Ángel Sánchez-Monedero, Yuki Audette, Ayodeji O. Deolu-Ajayi, Adrie van der Werf, Misghina Goitom Teklu, Moshe Shenker, Cláudia Pombo Sudré, Jader Galba Busato, Raul Ochoa-Hueso, Marco Nocentini, Johan Rippen, Ricardo Aroca, Socorro Mesa, María J. Delgado, Germán Tortosa

    Current and continuing climate change in the Anthropocene epoch requires sustainable agricultural practices. Additionally, due to changing consumer preferences, organic approaches to cultivation are gaining popularity. The global market for organic grapes, grape products, and wine is growing. Biostimulant and biocontrol products are often applied in organic vineyards and can reduce the synthetic fertilizer, pesticide, and fungicide requirements of a vineyard. Plant growth promotion following application is also observed under a variety of challenging conditions associated with global warming. This paper reviews different groups of biostimulants and their effects on viticulture, including microorganisms, protein hydrolysates, humic acids, pyrogenic materials, and seaweed extracts. Of special interest are biostimulants with utility in protecting plants against the effects of climate change, including drought and heat stress. While many beneficial effects have been reported following the application of these materials, most studies lack a mechanistic explanation, and important parameters are often undefined (e.g., soil characteristics and nutrient availability). We recommend an increased study of the underlying mechanisms of these products to enable the selection of proper biostimulants, application methods, and dosage in viticulture. A detailed understanding of processes dictating beneficial effects in vineyards following application may allow for biostimulants with increased efficacy, uptake, and sustainability.

    https://doi.org/10.3389/fpls.2022.932311
  • Plant and Soil
    2022

    Phosphorus and water supply independently control productivity and soil enzyme activity responses to elevated CO2 in an understorey community from a Eucalyptus woodland

    Juan Piñeiro, Raul Ochoa-Hueso, Lilia Serrano, Sally A. Power
    Aims

    While it is well-established that nitrogen (N) availability regulates elevated [CO2] (eCO2) effects on plant growth and soil carbon (C) storage in N-limited environments, there are fewer studies investigating the role of phosphorous (P) supply on such responses in P-limited environments. In this study, we explored whether P fertilization influences the response of plant growth, soil enzyme activity and C fluxes to eCO2, and determined how different levels of water availability regulate these processes.

    Methods

    We used soil collected from a temperate, P-limited Eucalyptus woodland containing the native soil seed bank to grow a potted replica of local understory communities. We exposed the emerging communities to eCO2 under two contrasting water levels and two levels of P fertilization. We assessed plant biomass allocation, the rhizosphere activity of extracellular enzymes related to C, N and P cycles, and pot-level CO2 fluxes.

    Results

    The positive effects of eCO2 on plant production and ecosystem C dynamics were strongly constrained by low levels of P availability. Enhanced water supply increased rhizosphere enzyme activity with minor impacts on plant biomass responses to eCO2. Our data also suggest that plant and microbial mechanisms that increase nutrient release from SOM may not be able to overcome this P limitation.

    Conclusions

    While current Earth System Models predict positive feedback responses of terrestrial ecosystems on C storage under eCO2, here we emphasize the importance of accounting for the widespread phenomenon of P-limitation in such responses.
    https://doi.org/10.1007/s11104-022-05763-0
  • Journal of Applied Ecology
    2022

    Long-term recovery of above- and below-ground interactions in restored grasslands after topsoil removal and seed addition

    Monika Carol Resch, Martin Schütz, Raul Ochoa-Hueso, Nina Buchmann, Beat Frey, Ulrich Graf, Wim H. van der Putten, Stephan Zimmermann, Anita C. Risch

    Evaluation of restoration activities is indispensable to assess the extent to which targets have been reached. Usually, the main goal of ecological restoration is to restore biodiversity and ecosystem functioning, but validation is often based on a single indicator, which may or may not cope with whole-ecosystem dynamics. Network analyses are, however, powerful tools, allowing to examine both the recovery of various biotic and abiotic properties and the integrated response at community and ecosystem level. We used restoration sites where topsoil was removed from former intensively managed grassland and seeds were added. These sites were between 3 and 32 years old. We assessed how plants, soil biota, soil properties and correlation-based interactions between biotic communities and their abiotic environment developed over time and compared the results with (i) intensively managed (not restored), and (ii) well-preserved targeted semi-natural grasslands. Plant, nematode, fungal and prokaryotic diversity and community structures of the restored grasslands revealed clear successional patterns and followed similar trajectories towards targeted semi-natural grasslands. All biotic communities reached targeted diversity levels no later than 18 years post-restoration. Ecological networks of intensively managed and short-term (~4 years) restored grasslands were less tightly connected compared to those found in mid- and long-term (~18–30 years) restored and target grasslands. Restoration specifically enhanced interactions among biotic communities, but reduced interactions between biotic communities and their abiotic environment as well as interactions among abiotic properties in the short- and mid-term. Synthesis and applications: Overall, our study demonstrated that topsoil removal and seed addition were successful in restoring diverse, tightly coupled and well-connected biotic communities above- and below-ground similar to those found in the semi-natural grasslands that were restoration targets. Network analyses proved to be powerful in examining the long-term re-establishment of functionally connected biotic communities in restored ecosystems. Thus, we provide an approach to holistically assess restoration activities by notably considering the complexity of ecosystems, much in contrast to most traditional approaches.

    https://doi.org/10.1111/1365-2664.14145
  • Functional Ecology
    2022

    Nitrogen loading enhances phosphorus limitation in terrestrial ecosystems with implications for soil carbon cycling

    Min Luo, Daryl L. Moorhead, Raul Ochoa-Hueso, Carsten W. Mueller, Samantha C. Ying, Ji Chen

    Increased human-derived nitrogen (N) loading in terrestrial ecosystems has caused widespread ecosystem-level phosphorus (P) limitation. In response, plants and soil micro-organisms adopt a series of P-acquisition strategies to offset N loading-induced P limitation. Many of these strategies impose costs on carbon (C) allocation by plants and soil micro-organisms; however, it remains unclear how P-acquisition strategies affect soil C cycling. Herein, we review the literature on the effects of N loading on P limitation and outline a conceptual overview of how plant and microbial P-acquisition strategies may affect soil organic carbon (SOC) stabilization and decomposition in terrestrial ecosystems. Excessive input of N significantly enhances plant biomass production, soil acidification, and produces plant litterfall with high N/P ratios, which can aggravate ecosystem-level P limitation. Long-term N loading can cause plants and soil micro-organisms to alter their functional traits to increase P acquisition. Plants can release carboxylate exudates and phosphatases, modify root morphological traits, facilitate the formation of symbiotic associations with mycorrhizal fungi and stimulate the abundance of P-mineralizing and P-solubilizing micro-organisms. Releasing carboxylate exudates and phosphatases could accelerate SOC decomposition, whereas changing symbiotic associations and root morphological traits (e.g. an increase in fine root length) may contribute to higher SOC stabilization. Increased relative abundances of P-mineralizing and P-solubilizing bacteria can accelerate P mining and SOC decay, which may decrease microbial C use efficiency and subsequently lower SOC sequestration. The trade-offs between different plant P-acquisition strategies under N loading should be among future research priorities due to their cascading impacts on soil C storage. Quantifying ecosystem thresholds for P adaption to increased N loading is important because P-acquisition strategies are effective when N loading is below the N threshold. Moreover, understanding the response of P-acquisition strategies at different levels of native soil N availability could provide insight to divergent P-acquisition strategies across sites and ecosystems. Altogether, P-acquisition strategies should be explicitly considered in Earth System Models to generate more realistic predictions of the effects of N loading on soil C cycling. Read the free Plain Language Summary for this article on the Journal blog.

    https://doi.org/10.1111/1365-2435.14178
  • Trends in Plant Science
    2022

    Moving towards the ecological intensification of tree plantations

    Susana Gómez-González, Maria Paniw, José Luis Blanco-Pastor, Ana I. García-Cervigón, Oscar Godoy, José M. Herrera, Antonio Lara, Alejandro Miranda, Fernando Ojeda, Raul Ochoa-Hueso

    The growing demand for timber and the boom in massive tree-planting programs could mean the spreading of mismanaged tree plantations worldwide. Here, we apply the concept of ecological intensification to forestry systems as a viable biodiversity-focused strategy that could be critical to develop productive, yet sustainable, tree plantations. Tree plantations can be highly productive if tree species are properly combined to complement their ecological functions. Simultaneously considering soil biodiversity and animal-mediated biocontrol will be critical to minimize the reliance on external inputs. Integrating genetic, functional, and demographic diversity across heterogeneous landscapes should improve resilience under climate change. Designing ecologically intensified plantations will mean breaking the timber productivity versus conservation dichotomy and assuring the maintenance of key ecosystem services at safe levels.

    https://doi.org/10.1016/j.tplants.2021.12.009
  • One Earth
    23-07-2021

    Ecosystem coupling

    Raul Ochoa-Hueso, Manuel Delgado-Baquerizo, Anita C. Risch, Maarten Schrama, Elly Morrien, S. Henrik Barmentlo, Stefan Geisen, Monika Carol Resch, Basten Snoek, Wim H. van der Putten

    Global change frequently disrupts the connections among species, as well as among species and their environment, before the most obvious impacts can be detected. Therefore, we need to develop a unified conceptual framework that allows us to predict early ecological impacts under changing environments. The concept of coupling, defined as the multiple ways in which the biotic and abiotic components of ecosystems are orderly connected across space and/or time, may provide such a framework. Here, we operationally define the coupling of ecosystems based on a combination of correlational matrices and a null modeling approach. Compared with null models, ecosystems can be (1) coupled; (2) decoupled; and (3) anticoupled. Given that more tightly coupled ecosystems displaying higher levels of internal order may be characterized by a more efficient capture, transfer, and storage of energy and matter (i.e., of functioning), understanding the links between coupling and functioning may help us to accelerate the transition to planetary-scale sustainability. This may be achieved by promoting self-organized order.

    https://doi.org/10.1016/j.oneear.2021.06.011
  • Ecological Monographs
    2020

    Links between soil microbial communities, functioning, and plant nutrition under altered rainfall in Australian grassland

    Raul Ochoa-Hueso, Valentina Arca, Manuel Delgado-Baquerizo, Kelly Hamonts, Juan Piñeiro, Lilia Serrano, Julien Shawyer, Sally A. Power
    The size, frequency, and timing of precipitation events are predicted to become more variable worldwide. Despite these predictions, the importance of changes in precipitation in driving multiple above- and belowground ecosystem attributes simultaneously remains largely underexplored. Here, we carried out 3 yr of rainfall manipulations at the DRI-Grass facility, located in a mesic grassland in eastern Australia. Treatments were implemented through automated water reapplication and included +50% and −50% amount, reduced frequency of events, and an extreme summer drought. We evaluated the spatiotemporal responses of multiple ecosystem attributes including microbial biomass, community composition and activity, soil nutrient content and availability, and plant nutritional status to altered rainfall regimes. We found that changing precipitation patterns resulted in multiple direct and indirect changes in microbial communities and soil and plant nutrient content. Main results included greater availability of soil macronutrients and reduced availability of micronutrients under drought, and taxon-specific changes in the composition of soil microbial communities in response to altered rainfall. Moreover, using structural equation modeling, we showed that, in summer 2015, plant macronutrient contents, a widely used ecological indicator of pasture quality, were simultaneously explained by greater soil nutrient availability and the structure of soil microbial communities, and significantly reduced by lower rainfall. Plant micronutrients were also reduced by lower rainfall and explained by changes in microbial attributes. Despite treatment effects on many of the soil, microbial, and plant variables analyzed across the 3 yr of study, many of these ecosystem attributes varied greatly across sampling events. This resulted in many significant interactions between the rainfall treatments and experimental duration, suggesting complex system-level responses to changing rainfall in our grassland, and a high natural buffering capacity of the ecosystem to varying rainfall conditions. Some interactions manifested as changes in the coefficient of variation of ecosystem attributes, particularly in response to changes in the timing of precipitation events and the extreme summer drought. Finally, we posit that a detailed understanding of plant–soil–microbial interactions, and the role of climate in modifying these linkages, will be key for adapting the sustainability of grasslands to a future that will be shaped by climate change.
    https://doi.org/10.1002/ecm.1424

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