Plant functional trait shifts explain concurrent changes in the structure and function of grassland soil microbial communities

Land‐use intensification drives changes in microbial communities and the soil functions they regulate, but the mechanisms underlying these changes are poorly understood as land use can affect soil communities both directly (e.g. via changes in soil fertility) and indirectly (e.g. via changes in plant inputs). The speed of microbial responses is also poorly understood. For instance, whether it is long‐term legacies or short‐term changes in land‐use intensity that drive changes in microbial communities. To address these topics, we measured multiple microbial functions, bacterial and fungal biomass and abiotic soil properties at two time intervals 3 years apart. This was performed in 150 grassland sites differing greatly in management intensity across three German regions. Observed changes in microbial soil properties were related to both long‐term means and short‐term changes in: abiotic soil properties, land‐use intensity, community abundance‐weighted means of plant functional traits and plant biomass properties in regression and structural equation models. Plant traits, particularly leaf phosphorus, and soil pH were the best predictors of change in soil microbial function, as well as fungal and bacterial biomass, while land‐use intensity showed weaker effects. Indirect legacy effects, in which microbial change was explained by the effects of long‐term land‐use intensity on plant traits, were important, thus indicating a time lag between plant community and microbial change. Whenever the effects of short‐term changes in land‐use intensity were present, they acted directly on soil microorganisms. Synthesis. The results provide new evidence that soil communities and their functioning respond to short‐term changes in land‐use intensity, but that both rapid and longer time‐scale responses to changes in plant functional traits are at least of equal importance. This suggests that management which shapes plant communities may be an effective means of managing soil communities and the functions and services they provide.

[1]  N. Fierer,et al.  Fungal diversity regulates plant-soil feedbacks in temperate grassland , 2018, Science Advances.

[2]  C. Nock,et al.  Biodiversity and ecosystem functioning relations in European forests depend on environmental context. , 2017, Ecology letters.

[3]  M. Schloter,et al.  Spatial and temporal dynamics of nitrogen fixing, nitrifying and denitrifying microbes in an unfertilized grassland soil , 2017 .

[4]  S. Scheu,et al.  Root biomass and exudates link plant diversity with soil bacterial and fungal biomass , 2017, Scientific Reports.

[5]  M. Schloter,et al.  Biodiversity at multiple trophic levels is needed for ecosystem multifunctionality , 2016, Nature.

[6]  S. Marhan,et al.  Temporal and small-scale spatial variation in grassland productivity, biomass quality, and nutrient limitation , 2016, Plant Ecology.

[7]  M. Perring,et al.  Global environmental change effects on ecosystems: the importance of land‐use legacies , 2016, Global change biology.

[8]  S. Marhan,et al.  Carbon transfer from maize roots and litter into bacteria and fungi depends on soil depth and time , 2016 .

[9]  S. Wright,et al.  The global spectrum of plant form and function , 2015, Nature.

[10]  V. Acosta‐Martínez,et al.  Phosphorus Cycle Enzymes , 2015 .

[11]  C. Poll,et al.  Nitrogen Cycle Enzymes , 2015 .

[12]  S. Marhan,et al.  Do general spatial relationships for microbial biomass and soil enzyme activities exist in temperate grassland soils , 2015 .

[13]  Noah Fierer,et al.  Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe , 2015, Proceedings of the National Academy of Sciences.

[14]  J. Kattge,et al.  Simple measures of climate, soil properties and plant traits predict national-scale grassland soil carbon stocks , 2015 .

[15]  S. Marhan,et al.  Effects of warming and drought on potential N2O emissions and denitrifying bacteria abundance in grasslands with different land-use. , 2015, FEMS Microbiology Ecology.

[16]  Martin Schaefer,et al.  Land use intensification alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition , 2015, Ecology letters.

[17]  P. Reich The world‐wide ‘fast–slow’ plant economics spectrum: a traits manifesto , 2014 .

[18]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[19]  Y. Kuzyakov,et al.  Microbial gross organic phosphorus mineralization can be stimulated by root exudates – A 33P isotopic dilution study , 2013 .

[20]  M. Schloter,et al.  Different Land Use Intensities in Grassland Ecosystems Drive Ecology of Microbial Communities Involved in Nitrogen Turnover in Soil , 2013, PloS one.

[21]  I. Schöning,et al.  Community mean traits as additional indicators to monitor effects of land-use intensity On grassland plant diversity , 2013 .

[22]  Shinichi Nakagawa,et al.  A general and simple method for obtaining R2 from generalized linear mixed‐effects models , 2013 .

[23]  Michael Bahn,et al.  Relative contributions of plant traits and soil microbial properties to mountain grassland ecosystem services , 2013 .

[24]  Bill Shipley,et al.  Abiotic drivers and plant traits explain landscape-scale patterns in soil microbial communities. , 2012, Ecology letters.

[25]  Yves Rosseel,et al.  lavaan: An R Package for Structural Equation Modeling , 2012 .

[26]  Carsten F. Dormann,et al.  A quantitative index of land-use intensity in grasslands: Integrating mowing, grazing and fertilization , 2012 .

[27]  Vladimir G. Onipchenko,et al.  A rediscovered treasure: mycorrhizal intensity database for 3000 vascular plant species across the former Soviet Union , 2012 .

[28]  N. Hölzel,et al.  Reducing Sample Quantity and Maintaining High Prediction Quality of Grassland Biomass Properties with near Infrared Reflectance Spectroscopy , 2011 .

[29]  S. Marhan,et al.  Land-use intensity modifies spatial distribution and function of soil microorganisms in grasslands , 2011 .

[30]  S. Higgins,et al.  TRY – a global database of plant traits , 2011, Global Change Biology.

[31]  M. Schloter,et al.  Influence of land-use intensity on the spatial distribution of N-cycling microorganisms in grassland soils. , 2011, FEMS microbiology ecology.

[32]  Thomas Bell,et al.  The bacterial biogeography of British soils. , 2011, Environmental microbiology.

[33]  S. Oakley,et al.  Increases in soil organic carbon sequestration can reduce the global warming potential of long‐term liming to permanent grassland , 2011 .

[34]  M. Schrumpf,et al.  Phosphorus partitioning in grassland and forest soils of Germany as related to land-use type, management intensity, and land use–related pH , 2011 .

[35]  M. Lange,et al.  Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment , 2010, Nature.

[36]  L. Ruess,et al.  The fat that matters: Soil food web analysis using fatty acids and their carbon stable isotope signature , 2010 .

[37]  Benjamin L Turner,et al.  Linkages of plant traits to soil properties and the functioning of temperate grassland , 2010 .

[38]  Jens Nieschulze,et al.  Implementing large-scale and long-term functional biodiversity research: The Biodiversity Exploratories , 2010 .

[39]  Charles J. Marsh,et al.  A global comparison of grassland biomass responses to CO2 and nitrogen enrichment , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[40]  A. Varma,et al.  Role of Enzymes in Maintaining Soil Health , 2010 .

[41]  A. Vogel,et al.  Changes in wet meadow vegetation after 20 years of different management in a field experiment (North-West Germany) , 2009 .

[42]  P. Brookes,et al.  Contrasting Soil pH Effects on Fungal and Bacterial Growth Suggest Functional Redundancy in Carbon Mineralization , 2009, Applied and Environmental Microbiology.

[43]  K. Beard,et al.  Decoupling Plant-Growth From Land-Use Legacies in Soil Microbial Communities , 2008 .

[44]  S. Lavorel,et al.  Incorporating plant functional diversity effects in ecosystem service assessments , 2007, Proceedings of the National Academy of Sciences.

[45]  Mark Rees,et al.  Decoupling the direct and indirect effects of nitrogen deposition on ecosystem function. , 2006, Ecology letters.

[46]  Hon Keung Tony Ng,et al.  Statistics: An Introduction Using R , 2006, Technometrics.

[47]  R. B. Jackson,et al.  The diversity and biogeography of soil bacterial communities. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[48]  K. Treseder A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. , 2004, The New phytologist.

[49]  Eric Garnier,et al.  PLANT FUNCTIONAL MARKERS CAPTURE ECOSYSTEM PROPERTIES DURING SECONDARY SUCCESSION , 2004 .

[50]  C. D. Clegg,et al.  Spatial structure in soil chemical and microbiological properties in an upland grassland. , 2004, FEMS microbiology ecology.

[51]  D. Wardle,et al.  Ecological Linkages Between Aboveground and Belowground Biota , 2004, Science.

[52]  R. Joergensen,et al.  Ergosterol and microbial biomass relationship in soil , 1996, Biology and Fertility of Soils.

[53]  R. Bardgett,et al.  The short-term effects of cessation of fertiliser applications, liming, and grazing on microbial biomass and activity in a reseeded upland grassland soil , 1995, Biology and Fertility of Soils.

[54]  E. Kandeler,et al.  Effect of cattle slurry in grassland on microbial biomass and on activities of various enzymes , 1993, Biology and Fertility of Soils.

[55]  E. Kandeler,et al.  Short-term assay of soil urease activity using colorimetric determination of ammonium , 1988, Biology and Fertility of Soils.

[56]  D. Tilman,et al.  The Importance of Land-Use Legacies to Ecology and Conservation , 2003 .

[57]  M. Wood,et al.  A microplate fluorimetric assay for the study of enzyme diversity in soils , 2001 .

[58]  K. Tian,et al.  Legacies of agriculture and forest regrowth in the nitrogen of old-field soils , 2000 .

[59]  P. Hobbs,et al.  Management influences on soil microbial communities and their function in botanically diverse haymeadows of northern England and Wales , 2000 .

[60]  P. Hobbs,et al.  Plant species and nitrogen effects on soil biological properties of temperate upland grasslands , 1999 .

[61]  R. Bardgett,et al.  The measurement of soil fungal:bacterial biomass ratios as an indicator of ecosystem self-regulation in temperate meadow grasslands , 1999, Biology and Fertility of Soils.

[62]  D. Wardle,et al.  Linking above-ground and below-ground interactions: How plant responses to foliar herbivory influence soil organisms , 1998 .

[63]  J. P. Grime,et al.  Benefits of plant diversity to ecosystems: immediate, filter and founder effects , 1998 .

[64]  D. Bossio,et al.  Determinants of Soil Microbial Communities: Effects of Agricultural Management, Season, and Soil Type on Phospholipid Fatty Acid Profiles , 1998, Microbial Ecology.

[65]  David A. Wardle,et al.  Can comparative approaches based on plant ecophysiological traits predict the nature of biotic interactions and individual plant species effects in ecosystems? , 1998 .

[66]  T. Ando,et al.  Measurement of soil microbial biomass phosphorus by an anion exchange membrane method , 1995 .

[67]  J. A. Veen,et al.  Carbon fluxes in the rhizosphere of winter wheat and spring barley with conventional vs integrated farming , 1995 .

[68]  S. Rushton,et al.  The effects of grazing management on the vegetation of mesotrophic (meadow) grassland in Northern England , 1994 .

[69]  E. Bååth,et al.  Microbial biomass measured as total lipid phosphate in soils of different organic content , 1991 .

[70]  P. Brookes,et al.  AN EXTRACTION METHOD FOR MEASURING SOIL MICROBIAL BIOMASS C , 1987 .

[71]  F. Widdel,et al.  Phospholipid Ester-linked Fatty Acid Biomarkers of Acetate-oxidizing Sulphate-reducers and Other Sulphide-forming Bacteria , 1986 .

[72]  J. K. Martin,et al.  Measurement of phosphorus in the soil microbial biomass:A modified procedure for field soils , 1986 .

[73]  J. Tiedje,et al.  Phases of denitrification following oxygen depletion in soil , 1979 .