Chronic fertilization and irrigation gradually and increasingly restructure grassland communities

Scientists have known for over a century that resource addition can lead to species loss from plant communities. Recent studies have also shown that resource addition can substantially restructure communities by altering their functional and taxonomic composition—even when species richness remains unchanged. Understanding which aspects of community structure are impacted by different resources and over which timescales will provide insight for management decisions and may also elucidate which measures can act as early warning indicators for subsequent changes in the community. Here, we take advantage of a long‐term factorial experiment to understand how grassland plant communities respond to a decade of nitrogen fertilization (14 g N·m⁻²·yr⁻¹) and irrigation (25 mm water/week during the growing season). After 10 yr, fertilization and irrigation decreased species richness by 22% and 9%, while functional richness decreased by 31% and 41%. Abundance‐weighted functional distance between treatments and controls increased by 55% and 24%, respectively. We expected that abundance‐weighted measures would shift before presence–absence‐based measures, but found limited evidence for this. Instead, our results suggest that species gains, which can occur quickly because they require the addition of only one individual, may serve as early indicators for subsequent community restructuring in the opposite direction. Overall, both chronic nitrogen fertilization and irrigation tended to have gradual and increasing impacts on community structure, but the magnitude of these effects varied greatly depending on the aspect of community structure investigated. Further study will be needed to determine the extent to which our results can be generalized to other resources or sites in order to develop management strategies to maintain both taxonomic and functional trait diversity in the face of chronic resource changes.

[1]  D. Tilman,et al.  Sustainable intensification of high-diversity biomass production for optimal biofuel benefits , 2018, Nature Sustainability.

[2]  P. Reich,et al.  Unexpected reversal of C3 versus C4 grass response to elevated CO2 during a 20-year field experiment , 2018, Science.

[3]  Kerry M. Byrne,et al.  Asymmetric responses of primary productivity to precipitation extremes: A synthesis of grassland precipitation manipulation experiments , 2017, Global change biology.

[4]  M. Cadotte,et al.  Functional traits explain ecosystem function through opposing mechanisms. , 2017, Ecology letters.

[5]  Jens Kattge,et al.  A global Fine-Root Ecology Database to address below-ground challenges in plant ecology. , 2017, The New phytologist.

[6]  R. Kadmon,et al.  Contrasting effects of water and nutrient additions on grassland communities: A global meta‐analysis , 2017 .

[7]  Nathan J B Kraft,et al.  Functional Rarity: The Ecology of Outliers. , 2017, Trends in ecology & evolution.

[8]  Zoltán Botta-Dukát,et al.  New plant trait records of the Hungarian flora. , 2016 .

[9]  E. Borer,et al.  Addition of multiple limiting resources reduces grassland diversity , 2016, Nature.

[10]  K. Zobel,et al.  Plasticity in plant functional traits is shaped by variability in neighbourhood species composition. , 2016, The New phytologist.

[11]  Kate S Boersma,et al.  Linking multidimensional functional diversity to quantitative methods: a graphical hypothesis--evaluation framework. , 2016, Ecology.

[12]  Anthony R. Taylor,et al.  Traits to stay, traits to move: a review of functional traits to assess sensitivity and adaptive capacity of temperate and boreal trees to climate change , 2016 .

[13]  S. Lavorel,et al.  Relative contribution of soil, management and traits to co-variations of multiple ecosystem properties in grasslands , 2016, Oecologia.

[14]  Richard D. Bardgett,et al.  Plant community controls on short‐term ecosystem nitrogen retention , 2016, The New phytologist.

[15]  F. Hartig,et al.  Intraspecific trait variation across scales: implications for understanding global change responses , 2016, Global change biology.

[16]  Christian Wirth,et al.  From pots to plots: hierarchical trait‐based prediction of plant performance in a mesic grassland , 2016 .

[17]  Forest Isbell,et al.  A framework for quantifying the magnitude and variability of community responses to global change drivers , 2015 .

[18]  D. Ciccarelli Mediterranean coastal dune vegetation: Are disturbance and stress the key selective forces that drive the psammophilous succession? , 2015 .

[19]  Akira Mori,et al.  Functional redundancy of multiple forest taxa along an elevational gradient: predicting the consequences of non‐random species loss , 2015 .

[20]  Ian J. Wright,et al.  Global effects of soil and climate on leaf photosynthetic traits and rates , 2015 .

[21]  Eric Justes,et al.  A Functional Characterisation of a Wide Range of Cover Crop Species: Growth and Nitrogen Acquisition Rates, Leaf Traits and Ecological Strategies , 2015, PloS one.

[22]  S. Frey,et al.  Global environmental change and the nature of aboveground net primary productivity responses: insights from long-term experiments , 2015, Oecologia.

[23]  Melinda D. Smith,et al.  Functional trait expression of grassland species shift with short- and long-term nutrient additions , 2015, Plant Ecology.

[24]  H. Peter Linder,et al.  Diversification rate shifts in the Cape Floristic Region: The right traits in the right place at the right time , 2014 .

[25]  Jason D. Fridley,et al.  Community Functional Responses to Soil and Climate at Multiple Spatial Scales: When Does Intraspecific Variation Matter? , 2014, PloS one.

[26]  F. Woodward,et al.  A Global Data Set of Leaf Photosynthetic Rates, Leaf N and P, and Specific Leaf Area , 2014 .

[27]  Ellen L. Fry,et al.  Seasonal Variation in the Capacity for Plant Trait Measures to Predict Grassland Carbon and Water Fluxes , 2014, Ecosystems.

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

[29]  Peter B. Adler,et al.  Functional traits explain variation in plant life history strategies , 2013, Proceedings of the National Academy of Sciences.

[30]  S. Levin,et al.  Resource limitation in a competitive context determines complex plant responses to experimental resource additions. , 2013, Ecology.

[31]  David A. Wardle,et al.  Contrasting effects of plant inter‐ and intraspecific variation on community‐level trait measures along an environmental gradient , 2013 .

[32]  S. Dray,et al.  A guide for using functional diversity indices to reveal changes in assembly processes along ecological gradients , 2013 .

[33]  David A. Norton,et al.  Contrasting effects of productivity and disturbance on plant functional diversity at local and metacommunity scales , 2013 .

[34]  Laura Turnbull,et al.  Sensitivity of grassland plant community composition to spatial vs. temporal variation in precipitation. , 2013, Ecology.

[35]  S. Polasky,et al.  Nutrient enrichment, biodiversity loss, and consequent declines in ecosystem productivity , 2013, Proceedings of the National Academy of Sciences.

[36]  Bill Shipley,et al.  Inter‐specific and intra‐specific trait variation along short environmental gradients in an old‐growth temperate forest , 2013 .

[37]  Wilfried Thuiller,et al.  Rare Species Support Vulnerable Functions in High-Diversity Ecosystems , 2013, PLoS biology.

[38]  S. Polasky,et al.  Low biodiversity state persists two decades after cessation of nutrient enrichment. , 2013, Ecology letters.

[39]  Eric G. Lamb,et al.  Limited effects of simulated acidic deposition on seedling survivorship and root morphology of endemic plant taxa of the Athabasca Sand Dunes in well-watered greenhouse trials , 2013 .

[40]  David Mouillot,et al.  A functional approach reveals community responses to disturbances. , 2013, Trends in ecology & evolution.

[41]  Justin P. Wright,et al.  Does the leaf economic spectrum hold within local species pools across varying environmental conditions , 2012 .

[42]  B. Enquist,et al.  The leaf-area shrinkage effect can bias paleoclimate and ecology research. , 2012, American journal of botany.

[43]  R. B. Jackson,et al.  A Global Database of Carbon and Nutrient Concentrations of Green and Senesced Leaves , 2012 .

[44]  A. Siefert,et al.  Spatial patterns of functional divergence in old‐field plant communities , 2012 .

[45]  E. Schulze,et al.  Using Plant Functional Traits to Explain Diversity–Productivity Relationships , 2012, PloS one.

[46]  Cyrille Violle,et al.  The return of the variance: intraspecific variability in community ecology. , 2012, Trends in ecology & evolution.

[47]  Fusuo Zhang,et al.  Floral, climatic and soil pH controls on leaf ash content in China's terrestrial plants , 2012 .

[48]  F. C. Pillsbury,et al.  Analysis of abrupt transitions in ecological systems , 2011 .

[49]  J. Fargione,et al.  Patterns of trait convergence and divergence among native and exotic species in herbaceous plant communities are not modified by nitrogen enrichment , 2011 .

[50]  F. Bello,et al.  Community trait response to environment: disentangling species turnover vs intraspecific trait variability effects , 2011 .

[51]  P. Reich,et al.  High plant diversity is needed to maintain ecosystem services , 2011, Nature.

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

[53]  I. C. Prentice,et al.  Evidence of a universal scaling relationship for leaf CO2 drawdown along an aridity gradient. , 2011, The New phytologist.

[54]  Brody Sandel,et al.  Using plant functional traits to guide restoration: A case study in California coastal grassland , 2011 .

[55]  Brody Sandel,et al.  Contrasting trait responses in plant communities to experimental and geographic variation in precipitation. , 2010, The New phytologist.

[56]  Lucien Hoffmann,et al.  Intraspecific variability and trait‐based community assembly , 2010 .

[57]  P. Vesk,et al.  What does species richness tell us about functional trait diversity? Predictions and evidence for responses of species and functional trait diversity to land-use change , 2010 .

[58]  Carolyn Hull Sieg,et al.  A multi‐trait test of the leaf‐height‐seed plant strategy scheme with 133 species from a pine forest flora , 2010 .

[59]  Wilfried Thuiller,et al.  Intraspecific functional variability: extent, structure and sources of variation , 2010 .

[60]  Guido Brusa,et al.  Can CSR classification be generally applied outside Britain? , 2010, Plant Ecology.

[61]  Jarrod D. Hadfield,et al.  MCMC methods for multi-response generalized linear mixed models , 2010 .

[62]  J. Bullock,et al.  Nitrogen deposition causes widespread loss of species richness in British habitats , 2010 .

[63]  Peter M van Bodegom,et al.  Plant Strategies in Relation to Resource Supply in Mesic to Wet Environments: Does Theory Mirror Nature? , 2009, The American Naturalist.

[64]  Marta Halina,et al.  Phylogenetic community structure in Minnesota oak savanna is influenced by spatial extent and environmental variation , 2009 .

[65]  S. Collins,et al.  A framework for assessing ecosystem dynamics in response to chronic resource alterations induced by global change. , 2009, Ecology.

[66]  S. Vicente‐Serrano,et al.  A Multiscalar Drought Index Sensitive to Global Warming: The Standardized Precipitation Evapotranspiration Index , 2009 .

[67]  W. Knorr,et al.  Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global‐scale terrestrial biosphere models , 2009 .

[68]  Luca Bragazza,et al.  Conservation priority of Italian Alpine habitats: a floristic approach based on potential distribution of vascular plant species , 2009, Biodiversity and Conservation.

[69]  Ian J. Wright,et al.  Leaf phosphorus influences the photosynthesis–nitrogen relation: a cross-biome analysis of 314 species , 2009, Oecologia.

[70]  Martin Hermy,et al.  The LEDA Traitbase: a database of life‐history traits of the Northwest European flora , 2008 .

[71]  Peter B Reich,et al.  Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants. , 2008, Ecology letters.

[72]  D. Mouillot,et al.  New multidimensional functional diversity indices for a multifaceted framework in functional ecology. , 2008, Ecology.

[73]  H. Reynolds,et al.  Perturbations alter community convergence, divergence, and formation of multiple community states. , 2008, Ecology.

[74]  M. Cadotte,et al.  Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. , 2008, Ecology.

[75]  David Tilman,et al.  Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands , 2008, Nature.

[76]  B. Wilsey,et al.  Dominant Species Constrain Effects of Species Diversity on Temporal Variability in Biomass Production of Tallgrass Prairie , 2007 .

[77]  T. McMahon,et al.  Updated world map of the Köppen-Geiger climate classification , 2007 .

[78]  Maria Lundmark,et al.  Acclimation of photosynthesis and respiration is asynchronous in response to changes in temperature regardless of plant functional group. , 2007, The New phytologist.

[79]  G. Hegerl,et al.  Detection of human influence on twentieth-century precipitation trends , 2007, Nature.

[80]  D. Tilman,et al.  Resource Use Patterns Predict Long‐Term Outcomes of Plant Competition for Nutrients and Light , 2007, The American Naturalist.

[81]  Charles A Price,et al.  Scaling mass and morphology in leaves: an extension of the WBE model. , 2007, Ecology.

[82]  Eric Garnier,et al.  Assessing the effects of land-use change on plant traits, communities and ecosystem functioning in grasslands: a standardized methodology and lessons from an application to 11 European sites. , 2007, Annals of botany.

[83]  Michel Loreau,et al.  From selection to complementarity: shifts in the causes of biodiversity–productivity relationships in a long-term biodiversity experiment , 2007, Proceedings of the Royal Society B: Biological Sciences.

[84]  William F. Fagan,et al.  Phylogenetic and Growth Form Variation in the Scaling of Nitrogen and Phosphorus in the Seed Plants , 2006, The American Naturalist.

[85]  D. Ackerly,et al.  A trait-based test for habitat filtering: convex hull volume. , 2006, Ecology.

[86]  T. Huntington Evidence for intensification of the global water cycle: Review and synthesis , 2006 .

[87]  Dali Guo,et al.  Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. , 2005, The New phytologist.

[88]  William G. Lee,et al.  Functional richness, functional evenness and functional divergence: the primary components of functional diversity , 2005 .

[89]  P. Reich,et al.  Assessing the generality of global leaf trait relationships. , 2005, The New phytologist.

[90]  Begoña Peco,et al.  The effect of grazing abandonment on species composition and functional traits: the case of dehesa grasslands , 2005 .

[91]  Christopher J. Lortie,et al.  The importance of importance , 2005 .

[92]  Sophie Gachet,et al.  BASECO: a floristic and ecological database of Mediterranean French flora , 2005, Biodiversity & Conservation.

[93]  K. Gross,et al.  Functional- and abundance-based mechanisms explain diversity loss due to N fertilization. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[94]  Terry V. Callaghan,et al.  Leaf digestibility and litter decomposability are related in a wide range of subarctic plant species and types , 2004 .

[95]  G. Asner,et al.  Nitrogen Cycles: Past, Present, and Future , 2004 .

[96]  Daniel G. Milchunas,et al.  Functional traits of graminoids in semi-arid steppes: a test of grazing histories , 2004 .

[97]  P. Reich,et al.  Species and functional group diversity independently influence biomass accumulation and its response to CO2 and N. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[98]  J. P. Grime,et al.  The plant traits that drive ecosystems: Evidence from three continents , 2004 .

[99]  Sean C. Thomas,et al.  The worldwide leaf economics spectrum , 2004, Nature.

[100]  C. Stevens,et al.  Impact of Nitrogen Deposition on the Species Richness of Grasslands , 2004, Science.

[101]  Terry V. Callaghan,et al.  DECOMPOSITION OF SUB‐ARCTIC PLANTS WITH DIFFERING NITROGEN ECONOMIES: A FUNCTIONAL ROLE FOR HEMIPARASITES , 2003 .

[102]  Alastair Fitter,et al.  Thermal acclimation of leaf and root respiration: An investigation comparing inherently fast- and slow-growing plant species , 2003 .

[103]  Bill Shipley,et al.  Trade‐offs between net assimilation rate and specific leaf area in determining relative growth rate: relationship with daily irradiance , 2002 .

[104]  P. Reich,et al.  Functional traits, productivity and effects on nitrogen cycling of 33 grassland species , 2002 .

[105]  Bill Shipley,et al.  Dry matter content as a measure of dry matter concentration in plants and their parts , 2002 .

[106]  Michel Loreau,et al.  Partitioning selection and complementarity in biodiversity experiments , 2001, Nature.

[107]  Fumito Koike,et al.  Plant traits as predictors of woody species dominance in climax forest communities , 2001 .

[108]  Jacob McC. Overton,et al.  Shifts in trait‐combinations along rainfall and phosphorus gradients , 2000 .

[109]  J. P. Grime,et al.  The effects of trophic structure and soil fertility on the assembly of plant communities: a microcosm experiment , 2000 .

[110]  M. Lechowicz,et al.  The functional co-ordination of leaf morphology, nitrogen concentration, and gas exchange in40 wetland species , 2000 .

[111]  Sandra Díaz,et al.  Leaf structure and defence control litter decomposition rate across species and life forms in regional floras on two continents , 1999 .

[112]  Bill Shipley,et al.  Interacting determinants of specific leaf area in 22 herbaceous species: effects of irradiance and nutrient availability , 1999 .

[113]  Paul A. Keddy,et al.  Community Assembly Rules, Morphological Dispersion, and the Coexistence of Plant Species , 1998 .

[114]  Mark Westoby,et al.  A leaf-height-seed (LHS) plant ecology strategy scheme , 1998, Plant and Soil.

[115]  P. Reich,et al.  The Influence of Functional Diversity and Composition on Ecosystem Processes , 1997 .

[116]  H. Lambers,et al.  Leaf Respiration in Light and Darkness (A Comparison of Slow- and Fast-Growing Poa Species) , 1997, Plant physiology.

[117]  D. Tilman,et al.  Convergence and divergence of old-field vegetation after 11 yr of nitrogen addition , 1995 .

[118]  Bill Shipley,et al.  Structured interspecific determinants of specific leaf area in 34 species of herbaceous angiosperms , 1995 .

[119]  Alastair H. Fitter,et al.  The ecological flora database. , 1994 .

[120]  R. Peet,et al.  Changes in chalk-grassland structure and species richness resulting from selective nutrient additions , 1993 .

[121]  David Tilman,et al.  CONVERGENCE AND DIVERGENCE OF OLD-FIELD PLANT COMMUNITIES ALONG EXPERIMENTAL NITROGEN GRADIENTS' , 1988 .

[122]  David Tilman,et al.  Secondary Succession and the Pattern of Plant Dominance Along Experimental Nitrogen Gradients , 1987 .

[123]  Peter Manning,et al.  Trait?based classification and manipulation of plant functional groups for biodiversity?ecosystem function experiments , 2014 .

[124]  P. Legendre,et al.  A distance-based framework for measuring functional diversity from multiple traits. , 2010, Ecology.

[125]  Jeremy W. Lichstein,et al.  The Imprint of Species Turnover on Old-Growth Forest Carbon Balances - Insights From a Trait-Based Model of Forest Dynamics , 2009 .

[126]  Denis Vile Significations fonctionnelle et écologique des traits des espèces végétales exemple dans une succession post-culturale méditerranéenne et généralisations , 2005 .

[127]  J. Soussana,et al.  Plant traits and functional types in response to reduced disturbance in a semi-natural grassland , 2005 .

[128]  D. Roy,et al.  PLANTATT - attributes of British and Irish plants: status, size, life history, geography and habitats , 2004 .

[129]  S. Schneider,et al.  Climate Change 2001: Synthesis Report: A contribution of Working Groups I, II, and III to the Third Assessment Report of the Intergovernmental Panel on Climate Change , 2001 .

[130]  E. H. Simpson Measurement of Diversity , 1949, Nature.

[131]  John Bennet Lawes,et al.  XXVIII. Agricultural, botanical, and chemical results of experiments on the mixed herbage of permanent meadow, conducted for more than twenty years in succession on the same land. — Part. II. The botanical results , 1882, Philosophical Transactions of the Royal Society of London.