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The enduring effects of sowing legume-rich mixtures on the soil microbial community and soil carbon in semi-arid wood pastures

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Abstract

Aims

Agroforestry systems and legume sowing have been reported as efficient in terms of soil function, gaining momentum as environmentally sustainable agricultural practices. This paper examines how the soil microbial community of Mediterranean pastures responds to legume-enrichment.

Methods

We used phospholipid fatty acids profiling (PLFA) to measure microbial community composition, community-level physiological profiling (CLPP) to measure their activity and functional diversity, and analysed soil labile and bulk organic carbon in four wood pastures. Each site included a triplet of treatments composed of a native pasture (Control) and two native pastures enriched with a legume-rich mixture sowed ≤ 7 (young) and ≥ 11 (old) years ago, and two habitats (under tree canopy vs open pasture). The sites were fertilized with varying amounts of phosphorous.

Results

We found large variations among legume-plot ages and habitats, with microbial biomass, diversity and CLPP-activity higher in the legume-plots than in the control plots, and under tree than in open pastures. The community shift after sowing was driven by increased abundance of gram-negative bacteria and arbuscular mycorrhizal fungi, and decreased saprophytic fungi. Soil bulk and labile C stocks steadily increased after the sowing, and were related to legume abundance, P-fertilization and forage yield, both directly and indirectly, through the positive effect on microbial biomass and CLPP-activity.

Conclusions

The shift in microbial community structure together with the increased soil C stocks, soil P and likely N fixed by legumes form a positive legacy that can help to enhance the productivity and climate-resilience of pastures, although this needs further research.

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References

  • Ahlström A, Raupach MR, Schurgers G, Smith B, Arneth A, Jung M, Reichstein M, Canadell JG, Friedlingstein P, Jain AK, Kato E, Poulter B, Sitch S, Stocker BD, Viovy N, Wang YP, Wiltshire A, Zaehle S, Zeng N (2015) The dominant role of semi-arid ecosystems in the trend and variability of the land CO2 sink. Science 348:895–899

    Article  PubMed  CAS  Google Scholar 

  • Araya YN, Bartelheimer M, Valle CJ, Crujeiras RM, Garcıa-Baquero G (2017) Does functional soil microbial diversity contribute to explain within-site plant β-diversity an alpine grassland and a dehesa meadow in Spain? J Veg Sci 28:1018–1027

    Article  Google Scholar 

  • Bardgett RD, Jones AC, Jones DL, Kemmitt SJ, Cook R, Hobbs PJ (2001) Soil microbial community patterns related to the history and intensity of grazing in sub-montane ecosystems. Soil Biol Biochem 33(12–13):1653–1664

    Article  CAS  Google Scholar 

  • Barneze AS, Whitaker J, McNamara NP, Ostle NJ (2020) Legumes increase grassland productivity with no effect on nitrous oxide emissions. Plant Soil 446:163–177

    Article  CAS  Google Scholar 

  • Ben-David EA, Zaady E, Sher Y, Nejidat A (2011) Assessment of the spatial distribution of soil microbial communities in patchy arid and semi-arid landscapes of the Negev Desert using combined PLFA and DGGE analyses. FEMS Microbiol Ecol 76:492–503

    Article  CAS  PubMed  Google Scholar 

  • Bölscher T, Wadsö L, Börjesson G, Herrmann AM (2016) Differences in substrate use efficiency: impacts of microbial community composition, land use management, and substrate complexity. Biol Fertil Soils 52:547–559

    Article  CAS  Google Scholar 

  • Bond W, Parr C (2010) Beyond the forest edge: Ecology, diversity and conservation of the grassy biomes. Biological Conservervation 143:2395–2404

    Article  Google Scholar 

  • Bondaruk V, Lezama F, Del Pino A, Piñeiro G (2020) Overseeding legumes in natural grasslands: impacts on root biomass and soil organic matter of commercial farms. Sci Total Environ 743:140771

    Article  CAS  PubMed  Google Scholar 

  • Breulmann M, Schulz E, Weißhuhn K, Buscot F (2012) Impact of the plant community composition on labile soil organic carbon, soil microbial activity and community structure in semi-natural grassland ecosystems of different productivity. Plant Soil 352:253–265

    Article  CAS  Google Scholar 

  • Buyer JS, Sasser M (2012) High throughput phospholipid fatty acid analysis of soils. Appl Soil Ecol 61:127–130

    Article  Google Scholar 

  • Canals RM, Múgica L, Durán M, San Emeterio L (2019) Soil bacterial functional diversity mirrors the loss of plant diversity by the expansion of a native tall-grass in high mountain grasslands. Plant Soil 445:243–257

    Article  CAS  Google Scholar 

  • Cartwright J (2015) Average Well Color Development (AWCD) data based on Community Level Physiological Profiling (CLPP) of soil samples from 120 point locations within limestone cedar glades at Stones River National Battlefield near Murfreesboro, Tennessee, U.S. Geological Survey data release

  • Castellano MJ, Mueller KE, Olk DC, Sawyer JE, Six J (2015) Integrating plant litter quality, soil organic matter stabilization, and the carbon saturation concept. Glob Change Biol 21:3200–3209

    Article  Google Scholar 

  • Chen M, Chen B, Marschner P (2008) Plant growth and soil microbial community structure of legumes and grasses grown in monoculture or mixture. J Environ Sci 20:1231–1237

    Article  CAS  Google Scholar 

  • Collins RP, Lloyd DC, Marshall AH (2017) Strategies for maintaining a functional legume contribution in forage mixtures. Asp Appl Biol 136:245–251

    Google Scholar 

  • Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The microbial efficiency matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Chang Biol 19:988–995

    Article  Google Scholar 

  • Cotrufo MF, Soong JL, Horton AJ, Campbell EE, Haddix ML, Wall DH, Parton WJ (2015) Formation of soil organic matter via biochemical and physical pathways of litter mass loss. Nat Geosci 8:776–779

    Article  CAS  Google Scholar 

  • Cubera E, Moreno G (2007) Effect of single Quercus ilex trees upon spatial and seasonal changes in soil water content in dehesas of central western Spain. Ann for Sci 64:355–364

    Article  Google Scholar 

  • Dassen S, Cortois R, Martens H, de Hollander M, Kowalchuk GA, Van der Putten WH, De Deyn GB (2017) Differential responses of soil bacteria, fungi, archaea and protists to plant species richness and plant functional group identity. Mol Ecol 26:4085–4098

    Article  CAS  PubMed  Google Scholar 

  • De Vries FT, Griffiths RI, Bailey M et al (2018) Soil bacterial networks are less stable under drought than fungal networks. Nat Commun 9:3033

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Vries FT, Shade A (2013) Controls on soil microbial community stability under climate change. Front Microbiol 4:265

    Article  PubMed  PubMed Central  Google Scholar 

  • De Vries FT, Hoffland E, Van Eekeren N, Brussaard L, Bloem J (2006) Fungal/bacterial ratios in grasslands with contrasting nitrogen management. Soil Biol Biochem 38:2092–2103

    Article  CAS  Google Scholar 

  • De Vries FT, Manning P, Tallowin JRB, Mortimer SR, Pilgrim ES, Harrison KA, Hobbs PJ, Quirk H, Shipley B, Cornelissen JHC, Kattge J, Bardgett RD (2012) Abiotic drivers and plant traits explain landscape-scale patterns in soil microbial communities. Ecol Lett 15:1230–1239

    Article  PubMed  Google Scholar 

  • Duchene O, Vian JF, Celette F (2017) Intercropping with legume for agroecological cropping systems: Complementarity and facilitation processes and the importance of soil microorganisms. A review. Agr Ecosyst Environ 240:148–161

    Article  Google Scholar 

  • Fanin N, Kardol P, Farrell M, Nilsson MC, Gundale MJ, Wardle DA (2019) The ratio of Gram-positive to Gram-negative bacterial PLFA markers as an indicator of carbon availability in organic soils. Soil Biol Biochem 128:111–114

    Article  CAS  Google Scholar 

  • Francaviglia R, Renzi G, Ledda L, Benedetti A (2017) Organic carbon pools and soil biological fertility are affected by land use intensity in Mediterranean ecosystems of Sardinia, Italy. Sci Total Environ 599:789–796

    Article  PubMed  CAS  Google Scholar 

  • Frostegård A, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65

    Article  Google Scholar 

  • Frostegård Å, Tunlid A, Bååth E (2011) Use and misuse of PLFA measurements in soil. Soil Biol Biochem 43(8):1621–1625

    Article  CAS  Google Scholar 

  • Gallardo A, Rodriguez-Saucedo JJ, Covelo F, Fernandez-Ales R (2000) Soil nitrogen heterogeneity in a dehesa ecosystem. Plant Soil 222:71–82

    Article  CAS  Google Scholar 

  • Gao Q, Zhu W, Schwartz MW et al (2016) Climatic change controls productivity variation in global grasslands. Sci Rep 6:26958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geertsema W, Rossing WA, Landis DA et al (2016) Actionable knowledge for ecological intensification of agriculture. Front Ecol Environ 14:209–216

    Article  Google Scholar 

  • Geisseler D, Scow KM (2014) Long-term effects of mineral fertilizers on soil microorganisms–a review. Soil Biol Biochem 75:54–63

    Article  CAS  Google Scholar 

  • Grayston SJ, Campbell CD, Bardgett RD, Mawdsley JL, Clegg CD, Ritz K, Griffiths B, Rodwell JS, Edwards SJ, Davies WJ, Elston DJ, Millard P (2004) Assessing shifts in microbial community structure across a range of grasslands of differing management intensity using CLPP, PLFA and community DNA techniques. Appl Soil Ecol 25(1):63–84

    Article  Google Scholar 

  • Guillot E, Hinsinger P, Dufour L, Roy J, Bertrand I (2019) With or without trees: Resistance and resilience of soil microbial communities to drought and heat stress in a Mediterranean agroforestry system. Soil Biol Biochem 129:122–135

    Article  CAS  Google Scholar 

  • Gea-Izquierdo G, Allen-Díaz B, San Miguel A, Cañellas I (2010) How do trees affect spatio-temporal heterogeneity of nutrient cycling in mediterranean annual grasslands? Ann for Sci 67:112

    Article  Google Scholar 

  • Hanan N, Hill M (2012) Savannas in a changing earth system: The NASA Terrestrial Ecology Tree-Grass Project. White Paper for the NASA Terrestrial Ecology Program; Earth Science Division, Washington, DC

  • Herben T, Mayerová H, Skálová H, Hadincová V, Pecháčková S, Krahulec F (2017) Long-term time series of legume cycles in a semi-natural montane grassland: evidence for nitrogen-driven grass dynamics? Funct Ecol 31:1430–1440

    Article  Google Scholar 

  • Hernández-Esteban A, López-Díaz M, Cáceres Y, Moreno G (2019a) Are sown legume-rich pastures effective allies for the profitability and sustainability of Mediterranean dehesas? Agrofor Syst 93:2047–2065

    Article  Google Scholar 

  • Hernández-Esteban A, Rolo V, López-Díaz ML, Moreno G (2019b) Long-term implications of sowing legume-rich mixtures for plant diversity of Mediterranean wood pastures. Agric Ecosyst Environ 286:106686

    Article  CAS  Google Scholar 

  • Herzog S, Wemheuer F, Wemheuer B, Daniel R (2015) Effects of fertilization and sampling time on composition and diversity of entire and active bacterial communities in German grassland soils. PLoS One 10(12):e0145575

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Howlett DS, Moreno G, Losada MRM, Nair PKR, Nair VD (2011) Soil carbon storage as influenced by tree cover in the Dehesa cork oak silvopasture of central-western Spain. J Environ Monit 13(1897):1904

    Google Scholar 

  • Ikoyi I, Fowler A, Schmalenberger A (2018) One-time phosphate fertilizer application to grassland columns modifies the soil microbiota and limits its role in ecosystem services. Sci Total Environ 630:849–858

    Article  CAS  PubMed  Google Scholar 

  • Jin H, Sun OJ, Liu J (2010) Changes in soil microbial biomass and community structure with addition of contrasting types of plant litter in a semiarid grassland ecosystem. Journal of Plant Ecology 3(3):209–217

    Article  Google Scholar 

  • Jing X, Yang X, Ren F, Zhou H, Zhu B, He JS (2016) Neutral effect of nitrogen addition and negative effect of phosphorus addition on topsoil extracellular enzymatic activities in an alpine grassland ecosystem. Appl Soil Ecol 107:205–213

    Article  Google Scholar 

  • Joffre R (1990) Plant and soil nitrogen dynamics in Mediterranean grasslands: a comparison of annual and perennial grasses. Oecologia 85:142–149

    Article  CAS  PubMed  Google Scholar 

  • Kaiser K, Wemheuer B, Korolkow V, Wemheuer F, Nacke H, Schöning I, Schrumpf M, Daniel R (2016) Driving forces of soil bacterial community structure, diversity, and function in temperate grasslands and forests. Sci Rep 6:1–12

    Article  CAS  Google Scholar 

  • Kallenbach CM, Frey SD, Grandy AS (2016) Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat Commun 7:13630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kotroczó Z, Veres Z, Fekete I, Krakomperger Z, Tóth JA, Lajtha K, Tóthmérész B (2014) Soil enzyme activity in response to long-term organic matter manipulation. Soil Biol Biochem 70:237–243

    Article  CAS  Google Scholar 

  • Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371

    Article  CAS  Google Scholar 

  • Lama S, Kuhn T, Lehmann MF, Müller C, Gonzalez O, Eisenhauer N, Lange M, Scheu S, Olemann Y, Wilcke W (2020) The biodiversity-N cycle relationship: a 15 N tracer experiment with soil from plant mixtures of varying diversity to model N pool sizes and transformation rates. Biol Fertil Soils 56(1047):1061

    Google Scholar 

  • Lange M, Eisenhauer N, Sierra CA et al (2015) Plant diversity increases soil microbial activity and soil carbon storage. Nat Commun 6:1–8

    Article  Google Scholar 

  • Lefcheck JS (2016) piecewiseSEM: Piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579

    Article  Google Scholar 

  • Leifeld J, Kögel-Knabner I (2005) Soil organic matter fractions as early indicators for carbon stock changes under different land-use? Geoderma 124:143–155

    Article  CAS  Google Scholar 

  • Li J, Jiao S, Gao R, Bardgett R (2012) Differential effects of legume species on the recovery of soil microbial communities, and carbon and nitrogen contents, in abandoned fields of the Loess Plateau, China. Environ Manage 50:1193–1203

    Article  PubMed  Google Scholar 

  • Li F, Sørensen P, Li X, Olesen JE (2020) Carbon and nitrogen mineralization differ between incorporated shoots and roots of legume versus non-legume based cover crops. Plant Soil 446:243–257

    Article  CAS  Google Scholar 

  • Li H, Xu Z, Yan Q et al (2018a) Soil microbial beta-diversity is linked with compositional variation in aboveground plant biomass in a semi-arid grassland. Plant Soil 423:465–480

    Article  CAS  Google Scholar 

  • Li Y, Liu Y, Wu S, Nie C, Lorenz N, Lee NR, Dick RP (2018b) Composition and carbon utilization of soil microbial communities subjected to long-term nitrogen fertilization in a temperate grassland in northern China. Appl Soil Ecol 124:252–261

    Article  Google Scholar 

  • Lopez-Sangil L, Rousk J, Wallander H, Casals P (2011) Microbial growth rate measurements reveal that land-use abandonment promotes a fungal dominance of SOM decomposition in grazed Mediterranean ecosystems. Biol Fertil Soils 47:129–138

    Article  Google Scholar 

  • Luo X, Fu X, Yang Y, Cai P, Peng S, Chen W (2016) Microbial communities play important roles in modulating paddy soil fertility. Sci Rep 6:20326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo R, Fan J, Wang W, Luo J, Kuzyakov Y, He JS, Chu H, Ding W (2019) Nitrogen and phosphorus enrichment accelerates soil organic carbon loss in alpine grassland on the Qinghai-Tibetan Plateau. Sci Total Environ 650:303–312

    Article  CAS  PubMed  Google Scholar 

  • Lüscher A, Huguenin-Elie O, Suter M, Finn JA, Suter D (2017) From research to practice: grass-legume mixtures as a pillar for sustainable intensification. Asp Appl Biol 136:103–106

    Google Scholar 

  • Maestre FT, Escolar C, Bardgett RD, Dungait JA, Gozalo B, Ochoa V (2015) Warming reduces the cover and diversity of biocrust-forming mosses and lichens, and increases the physiological stress of soil microbial communities in a semi-arid Pinus halepensis plantation. Front Microbiol 6:865

    Article  PubMed  PubMed Central  Google Scholar 

  • Marschner P, Yang C-H, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33:1437–1445

    Article  CAS  Google Scholar 

  • Massey PA, Creamer RE, Whelan MJ, Ritz K (2016) Insensitivity of soil biological communities to phosphorus fertilization in intensively managed grassland systems. Grass Forage Sci 71:139–152

  • Miki T, Yokokawa T, Ke P-J, Hsieh I-F, Hsieh C, Kume T, Yoneya K, Matsui K (2018) Statistical recipe for quantifying microbial functional diversity from EcoPlate metabolic profiling. Ecol Res 33:249–260

    Article  CAS  Google Scholar 

  • Milcu A, Partsch S, Scherber C, Weisser WW, Scheu S (2008) Earthworms and legumes control litter decomposition in a plant diversity gradient. Ecology 89:1872e1882

    Article  Google Scholar 

  • Morais T, Teixeira R, Domingos T (2018) The Effects on greenhouse gas emissions of ecological intensification of meat production with rainfed sown biodiverse pastures. Sustainability 10:4184

    Article  CAS  Google Scholar 

  • Moreno G, Gonzalez-Bornay G, Pulido F, Lopez-Diaz ML, Bertomeu M, Juárez E, Diaz M (2016) Exploring the causes of high biodiversity of Iberian dehesas: the importance of wood pastures and marginal habitats. Agrofor Syst 90:87–105

    Article  Google Scholar 

  • Moreno G, Aviron S, Berg S et al (2018) Agroforestry systems of high nature and cultural value in Europe: provision of commercial goods and other ecosystem services. Agrofor Syst 92:877–891

    Article  Google Scholar 

  • Moreno G, Bartolome JW, Gea-Izquierdo G, Cañellas I (2013) Overstory-understory relationships. Mediterranean oak woodland working landscapes. Springer, Dordrecht, pp 145–179

    Chapter  Google Scholar 

  • Orwin KH, Dickie IA, Holdaway R, Wood JR (2018) A comparison of the ability of PLFA and 16S rRNA gene metabarcoding to resolve soil community change and predict ecosystem functions. Soil Biol Biochem 117:27–35

    Article  CAS  Google Scholar 

  • Paracchini ML, Petersen JE, Hoogeveen Y, Bamps C, Burfield I, Van Swaay C (2008) High nature value farmland in Europe. An estimate of the distribution patterns on the basis of land cover and biodiversity data. Luxemburg

  • Piton G, Legay N, Arnoldi C, Lavorel S, Clément JC, Foulquier A (2019) Using proxies of microbial community-weighted means traits to explain the cascading effect of management intensity, soil and plant traits on ecosystem resilience in mountain grasslands. J Ecol 108:876–893

    Article  CAS  Google Scholar 

  • Prudent M, Dequiedt S, Sorin C, Girodet S, Nowak V, Duc G, Salon C, Maron PA (2020) The diversity of soil microbial communities matters when legumes face drought. Plant Cell Environ 43(4):1023–1035

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2018) A language and environment for statistical computing

  • Rasmussen C, Heckman K, Wieder WR, Keiluweit M, Lawrence CR, Berhe AA,  Blankinship JC, Crow SE, Druhan JL, Hicks Pries CE, Marin-Spiotta E, Plante AF, Schädel C, Schimel JP, Sierra CA, Thompson A, Wagai R (2018) Beyond clay: towards an improved set of variables for predicting soil organic matter content. Biogeochemistry 137:297–306

  • Reed SC, Seastedt TR, Mann CM, Suding KN, Townsend AR, Cherwin KL (2007) Phosphorus fertilization stimulates nitrogen fixation and increases inorganic nitrogen concentrations in a restored prairie. Appl Soil Ecol 36:238–242

    Article  Google Scholar 

  • Rivest D, Lorente M, Olivier A, Messier C (2013) Soil biochemical properties and microbial resilience in agroforestry systems: Effects on wheat growth under controlled drought and flooding conditions. Sci Total Environ 463–464:51–60

  • Rolo V, López-Díaz ML, Moreno G (2012) Shrubs affect soil nutrients availability with contrasting consequences for pasture understory and tree overstory production and nutrient status in Mediterranean grazed open woodlands. Nutr Cycl Agroecosyst 93:89–102

    Article  Google Scholar 

  • Rooney DC, Clipson NJW (2009) Phosphate addition and plant species alters microbial community structure in acidic upland grassland soil. Microb Ecol 57:4–13

  • Rousk J, Brookes PC, Bååth E (2011) Fungal and bacterial growth responses to N fertilization and pH in the 150-year ‘Park Grass’ Uk grassland experiment. FEMS Microbiol Ecol 76:89–99

    Article  CAS  PubMed  Google Scholar 

  • Saar S, Semchenko M, Barel JM, De Deyn GB (2016) Legume presence reduces the decomposition rate of non-legume roots. Soil Biol Biochem 94:88–93

    Article  CAS  Google Scholar 

  • Sayer EJ, Oliver AE, Fridley JD, Askew AP, Mills RT, Grime JP (2017) Links between soil microbial communities and plant traits in a species-rich grassland under long-term climate change. Ecol Evol 7:855–862

    Article  PubMed  PubMed Central  Google Scholar 

  • Schleuss PM, Widdig M, Heintz-Buschart A, Guhr A, Martin S, Kirkman K, Spohn M (2019) Stoichiometric controls of soil carbon and nitrogen cycling after long-term nitrogen and phosphorus addition in a mesic grassland in South Africa. Soil Biol Biochem 135:294–303

    Article  CAS  Google Scholar 

  • Schloter M, Nannipieri P, Sørensen SJ, Van Elsas JD (2018) Microbial indicators for soil quality. Biol Fertil Soils 54:1–10

    Article  CAS  Google Scholar 

  • Seddaiu G, Porcu G, Ledda L, Roggero PP, Agnelli A, Corti G (2013) Soil organic matter content and composition as influenced by soil management in a semi-arid Mediterranean agro-silvo-pastoral system. Agr Ecosyst Environ 167:1–11

    Article  Google Scholar 

  • Shi Y, Ziadi N, Hamel C, Bélanger G, Abdi D, Lajeunesse J, Lafond J, Lalande R, Shang J (2020) Soil microbial biomass, activity and community structure as affected by mineral phosphorus fertilization in grasslands. Appl Soil Ecol 146:103391

    Article  Google Scholar 

  • Simón N, Montes F, Díaz-Pinés E, Benavides R, Roig S, Rubio A (2013) Spatial distribution of the soil organic carbon pool in a Holm oak dehesa in Spain. Plant Soil 366:537–549

    Article  CAS  Google Scholar 

  • Sofo A, Ricciuti P (2019) A standardized method for estimating the functional diversity of soil bacterial community by Biolog® EcoPlatesTM assay - the case study of a sustainable olive orchard. Appl Sci 9:4035

    Article  CAS  Google Scholar 

  • Soussana J-F, Lemaire G (2014) Coupling carbon and nitrogen cycles for environmentally sustainable intensification of grasslands and crop-livestock systems. Agr Ecosyst Environ 190:9–17

    Article  CAS  Google Scholar 

  • Spohn M, Pötsch EM, Eichorst SA, Woebken D, Wanek W, Richter A (2016) Soil microbial carbon use efficiency and biomass turnover in a long-term fertilization experiment in a temperate grassland. Soil Biol Biochem 97:168–175

    Article  CAS  Google Scholar 

  • Stolbovoy V, Montanarella L, Filippi N, Jones A, Gallego J, Grassi G (2005) Soil sampling protocol to certify the changes of organic carbon stock in mineral soil of the European Union. Version 2. EUR 21576 EN/2. 56 pp. Office for Official Publications of the European Communities, Luxembourg

  • Sun F, Pan K, Olatunji OA et al (2019) Specific legumes allay drought effects on soil microbial food web activities of the focal species in agroecosystem. Plant Soil 437:455–471

    Article  CAS  Google Scholar 

  • Tang M, Cheng W, Zeng H, Zhu B (2019) Light intensity controls rhizosphere respiration rate and rhizosphere priming effect of soybean and sunflower. Rhizosphere 9:97–105

    Article  Google Scholar 

  • Tardy V, Spor A, Mathieu O, Lévèque J, Terrat S, Plassart P, Regnier T, Bardgett RD, Van der Putten WH, Roggero PP, Seddaiu G, Bagella S, Lemanceau P, Ranjard L, Maron PA (2015) Shifts in microbial diversity through land use intensity as drivers of carbon mineralization in soil. Soil Biol Biochem 90:204–213

    Article  CAS  Google Scholar 

  • Thomson BC, Tisserant E, Plassart P, Uroz S, Griffiths RI, Hannula SE, Bu M, Mougel C, Rankard L, Van Veen JA, Matin F, Bailey MJ, Lemanceau P (2015) Soil conditions and land use intensification effects on soil microbial communities across a range of European field sites. Soil Biol Biochem 88:403–413

    Article  CAS  Google Scholar 

  • Tubiello FN, Soussana JF, Howden SM (2007) Crop and pasture response to climate change. PNAS 104:19686–19690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van der Wal A, de Boer W (2017) Dinner in the dark: illuminating drivers of soil organic matter decomposition. Soil Biol Biochem 105:45–48

    Article  CAS  Google Scholar 

  • Van Eekeren N, Van Liere D, De Vries FT, Rutgers M, de Goede RGM, Brussaard L (2009) A mixture of grass and clover combines the positive effects of both plant species on selected soil biota. Appl Soil Ecol 42:254–263

    Article  Google Scholar 

  • Van Zanten HH, Herrero M, Van Hal O et al (2018) Defining a land boundary for sustainable livestock consumption. Glob Change Biol 24:4185–4194

    Article  Google Scholar 

  • Vázquez de Aldana BR, Petisco C, GarcíaCriado B (2008) Interannual variations in phosphorus content of semiarid grasslands over a long time period. In: Hopkins A, Gustafsson T, Bertilsson J, Dalin G, Nilsdotter-Linde N, Spörndly E (eds) Biodiversity and animal feed. Future challenges for grassland production. Grassland Science in Europe, 13. European Grassland Federation, Uppsala, pp 634–636

    Google Scholar 

  • Waldrop MP, Firestone MK (2006) Seasonal dynamics of microbial community composition and function in oak canopy and open grassland soils. Microb Ecol 52:470–479

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Chapman SJ, Yao H (2016) Incorporation of 13C-labelled rice rhizodeposition into soil microbial communities under different fertilizer applications. Appl Soil Ecol 101:11–19

    Article  Google Scholar 

  • Weil RR, Islam KR, Stine MA, Gruver JB, Samson-Liebig SE (2003) Estimating active carbon for soil quality assessment: A simplified method for laboratory and field use. Am J Altern Agric 18:3–17

    Article  Google Scholar 

  • Weiner T, Gross A, Moreno G, Migliavacca M, Schrumpf M, Reichstein M, Carrara A, Angert A (2018) Following the turnover of soil bioavailable phosphate in Mediterranean savanna by oxygen stable isotopes. J Geophys Res Biogeosci 123:1850–1862

    Article  CAS  Google Scholar 

  • Whalen JK (2014) Managing soil biota-mediated decomposition and nutrient mineralization in sustainable agroecosystems. Advances in Agriculture 2014: Article ID 384604, 13 pages

  • Widdig M, Schleuss PM, Biederman LA, Borer ET, Crawley MJ, Kirkman KP, Seablom EW, Wragg PD, Spohn M (2020) Microbial carbon use efficiency in grassland soils subjected to nitrogen and phosphorus additions. Soil Biol Biochem 146:107815

    Article  CAS  Google Scholar 

  • Will C et al (2010) Horizon-specific bacterial community composition of German grassland soils, as revealed by pyrosequencing-based analysis of 16S rRNA genes. Appl Environ Microbiol 76:6751–6759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willers C, Van Rensburg PJJ, Claassens S (2015) Phospholipid fatty acid profiling of microbial communities – a review of interpretations and recent applications. J Appl Microbiol 119:1207–1218

    Article  CAS  PubMed  Google Scholar 

  • Wilson MH, Lovell ST (2016) Agroforestry - the next step in sustainable and resilient agriculture. Sustainability 8:574

    Article  Google Scholar 

  • Wu GL, Liu Y, Tian FP, Shi ZH (2017) Legumes functional group promotes soil organic carbon and nitrogen storage by increasing plant diversity. Land Degrad Dev 28:1336–1344

    Article  Google Scholar 

  • Xi N, Chu C, Bloor JM (2018) Plant drought resistance is mediated by soil microbial community structure and soil-plant feedbacks in a savanna tree species. Environ Exp Bot 155:695–701

    Article  Google Scholar 

  • Yang Y, Wu L, Lin Q, Yuan M, Xu D, Yu H, Hu Y, Duan J, Li X, He Z, Xue K, Van Nostrand J, Wang S, Zhou J (2013) Responses of the functional structure of soil microbial community to livestock grazing in the Tibetan alpine grassland. Glob Chang Biol 19(2):637–648

    Article  PubMed  Google Scholar 

  • Yang Y, Tilman D, Furey G, Lehman C (2019) Soil carbon sequestration accelerated by restoration of grassland biodiversity. Nat Commun 10:718

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Young A (1997) Agroforestry for soil management, 2nd edn. CAB International, Wallingford (320 pp)

    Book  Google Scholar 

  • Zhao F, Ren C, Shelton S, Wang Z, Pang G, Chen J, Wang J (2017) Grazing intensity influence soil microbial communities and their implications for soil respiration. Agr Ecosyst Environ 249:50–56

    Article  CAS  Google Scholar 

  • Zhou J, Zhang F, Huo Y et al (2019) Following legume establishment, microbial and chemical associations facilitate improved productivity in degraded grasslands. Plant Soil 443:273–292

    Article  CAS  Google Scholar 

  • Zhou Z, Wang C, Zheng M, Jiang L, Luo Y (2017) Patterns and mechanisms of responses by soil microbial communities to nitrogen addition. Soil Biol Biochem 115:433–441

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Virginia Gascón (IRNASA-CSIC) for her valuable task in laboratory analyses. This paper was developed as part of the project PID2019-108313RB-C31/AEI/10.13039/501100011033 funded by the Spanish State Research Agency. A. Hernández-Esteban was supported by a fellowship from Fundación Tatiana Pérez de Guzmán el Bueno, Madrid (Spain). V. Rolo was supported by a “Talento” fellowship (TA18022) funded by the regional government of Extremadura (Spain). José M. Igual was supported by project “CLU-2019-05 – IRNASA/CSIC Unit of Excellence”, funded by the Junta de Castilla y León and co-financed by the European Union (ERDF “Europe drives our growth”).

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Authors and Affiliations

  1. INDEHESA Research Institute, Forestry School, University of Extremadura, 10600, Plasencia, Spain

    Gerardo Moreno, Ana Hernández-Esteban & Víctor Rolo

  2. Instituto de Recursos Naturales y Agrobiología de Salamanca, CSIC, Salamanca, Spain

    José Mariano Igual

  3. Unidad Asociada Grupo de Interacción Planta-Microorganismo, Universidad de Salamanca-IRNASA-CSIC, Salamanca, Spain

    José Mariano Igual

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  1. Gerardo Moreno
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  2. Ana Hernández-Esteban
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  3. Víctor Rolo
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  4. José Mariano Igual
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Correspondence to Gerardo Moreno.

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Moreno, G., Hernández-Esteban, A., Rolo, V. et al. The enduring effects of sowing legume-rich mixtures on the soil microbial community and soil carbon in semi-arid wood pastures. Plant Soil 465, 563–582 (2021). https://doi.org/10.1007/s11104-021-05023-7

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