Plant communities as drivers of soil respiration: pathways, mechanisms, and significance for global change

Abstract. Understanding the impacts of plant community characteristics on soil carbon dioxide efflux (R) is a key prerequisite for accurate prediction of the future carbon (C) balance of terrestrial ecosystems under climate change. However, developing a mechanistic understanding of the determinants of R is complicated by the presence of multiple different sources of respiratory C within soil – such as soil microbes, plant roots and their mycorrhizal symbionts – each with their distinct dynamics and drivers. In this review, we synthesize relevant information from a wide spectrum of sources to evaluate the current state of knowledge about plant community effects on R, examine how this information is incorporated into global climate models, and highlight priorities for future research. Despite often large variation amongst studies and methods, several general trends emerge. Mechanisms whereby plants affect R may be grouped into effects on belowground C allocation, aboveground litter properties and microclimate. Within vegetation types, the amount of C diverted belowground, and hence R, may be controlled mainly by the rate of photosynthetic C uptake, while amongst vegetation types this should be more dependent upon the specific C allocation strategies of the plant life form. We make the case that plant community composition, rather than diversity, is usually the dominant control on R in natural systems. Individual species impacts on R may be largest where the species accounts for most of the biomass in the ecosystem, has very distinct traits to the rest of the community and/or modulates the occurrence of major natural disturbances. We show that climate vegetation models incorporate a number of pathways whereby plants can affect R, but that simplifications regarding allocation schemes and drivers of litter decomposition may limit model accuracy. We also suggest that under a warmer future climate, many plant communities may shift towards dominance by fast growing plants which produce large quantities of nutrient rich litter. Where this community shift occurs, it could drive an increase in R beyond that expected from direct climate impacts on soil microbial activity alone. We identify key gaps in knowledge and recommend them as priorities for future work. These include the patterns of photosynthate partitioning amongst belowground components, ecosystem level effects of individual plant traits, and the importance of trophic interactions and species invasions or extinctions for ecosystem processes. A final, overarching challenge is how to link these observations and drivers across spatio-temporal scales to predict regional or global changes in R over long time periods. A more unified approach to understanding R, which integrates information about plant traits and community dynamics, will be essential for better understanding, simulating and predicting patterns of R across terrestrial ecosystems and its role within the earth-climate system.

[1]  Sebastian Schmidtlein,et al.  The role of climate and plant functional trade-offs in shaping global biome and biodiversity patterns , 2011 .

[2]  Sebastian Schmidtlein,et al.  The role of plant functional trade-offs for biodiversity changes and biome shifts under scenarios of global climatic change , 2011 .

[3]  Jin-sheng Xie,et al.  Relationships between carbon allocation and partitioning of soil respiration across world mature forests , 2011, Plant Ecology.

[4]  Y. Malhi,et al.  Changes in the potential distribution of humid tropical forests on a warmer planet , 2011, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[5]  E. Davidson Permafrost and wetland carbon stocks. , 2010, Science.

[6]  D. Metcalfe,et al.  Quantification of effects of season and nitrogen supply on tree below-ground carbon transfer to ectomycorrhizal fungi and other soil organisms in a boreal pine forest. , 2010, The New phytologist.

[7]  A. Thomson,et al.  A global database of soil respiration data , 2010 .

[8]  J. Cornelissen,et al.  Evidence of the ‘plant economics spectrum’ in a subarctic flora , 2010 .

[9]  D. Randall,et al.  Role of deep soil moisture in modulating climate in the Amazon rainforest , 2010 .

[10]  Andrew D. Friend,et al.  Carbon and nitrogen cycle dynamics in the O‐CN land surface model: 1. Model description, site‐scale evaluation, and sensitivity to parameter estimates , 2010 .

[11]  Y. Malhi,et al.  Carbon cost of plant nitrogen acquisition: A mechanistic, globally applicable model of plant nitrogen uptake, retranslocation, and fixation , 2010 .

[12]  F. Berendse,et al.  Plant species richness regulates soil respiration through changes in productivity , 2010, Oecologia.

[13]  G. Lovett,et al.  Effects of biological invasions on forest carbon sequestration , 2010 .

[14]  Pete Smith,et al.  Integrating plant–soil interactions into global carbon cycle models , 2009 .

[15]  S. Higgins,et al.  Impacts of climate change on the vegetation of Africa: an adaptive dynamic vegetation modelling approach , 2009 .

[16]  M. Huston,et al.  The global distribution of net primary production: resolving the paradox , 2009 .

[17]  Peter J. Bellingham,et al.  Punching above their weight: low‐biomass non‐native plant species alter soil properties during primary succession , 2009 .

[18]  A. Weigelt,et al.  Positive biodiversity–productivity relationship due to increased plant density , 2009 .

[19]  Susan E. Ward,et al.  Plant functional group identity influences short-term peatland ecosystem carbon flux: evidence from a plant removal experiment , 2009 .

[20]  C. Giardina,et al.  Below‐ground carbon flux and partitioning: global patterns and response to temperature , 2008 .

[21]  J. Bascompte,et al.  Global change and species interactions in terrestrial ecosystems. , 2008, Ecology letters.

[22]  D. Wardle,et al.  Context dependency of litter‐mixing effects on decomposition and nutrient release across a long‐term chronosequence , 2008 .

[23]  A. Hodge,et al.  Mycorrhizal respiration: implications for global scaling relationships. , 2008, Trends in plant science.

[24]  Sandra Díaz,et al.  Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. , 2008, Ecology letters.

[25]  A. Nobre,et al.  Nocturnal accumulation of CO2 underneath a tropical forest canopy along a topographical gradient. , 2008, Ecological applications : a publication of the Ecological Society of America.

[26]  J. P. Grime,et al.  Plant community composition, not diversity, regulates soil respiration in grasslands , 2008, Biology Letters.

[27]  Sarah J. Richardson,et al.  Shifts in leaf N : P ratio during resorption reflect soil P in temperate rainforest , 2008 .

[28]  J. Roy,et al.  High variation in foliage and leaf litter chemistry among 45 tree species of a neotropical rainforest community. , 2008, The New phytologist.

[29]  Benjamin Smith,et al.  Representation of vegetation dynamics in the modelling of terrestrial ecosystems: comparing two contrasting approaches within European climate space , 2008 .

[30]  Yiqi Luo,et al.  Rates of litter decomposition in terrestrial ecosystems: global patterns and controlling factors , 2008 .

[31]  J. Cornelissen,et al.  Plant functional traits and soil carbon sequestration in contrasting biomes. , 2008, Ecology letters.

[32]  D. Wardle,et al.  Aboveground and belowground effects of single-tree removals in New Zealand rain forest. , 2008, Ecology.

[33]  W. Kurz,et al.  Mountain pine beetle and forest carbon feedback to climate change , 2008, Nature.

[34]  S. Cordell,et al.  A non‐native invasive grass increases soil carbon flux in a Hawaiian tropical dry forest , 2008 .

[35]  Yiqi Luo,et al.  Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. , 2008, The New phytologist.

[36]  J. Galloway,et al.  An Earth-system perspective of the global nitrogen cycle , 2008, Nature.

[37]  Markus Reichstein,et al.  CO2 balance of boreal, temperate, and tropical forests derived from a global database , 2007 .

[38]  Peter E. Thornton,et al.  Influence of carbon‐nitrogen cycle coupling on land model response to CO2 fertilization and climate variability , 2007 .

[39]  R. Sage,et al.  The temperature response of C(3) and C(4) photosynthesis. , 2007, Plant, cell & environment.

[40]  R. Ceulemans,et al.  How do climate warming and species richness affect CO2 fluxes in experimental grasslands? , 2007, The New phytologist.

[41]  James S. Clark,et al.  Resolving the biodiversity paradox. , 2007, Ecology letters.

[42]  Hisashi Sato,et al.  SEIB–DGVM: A new Dynamic Global Vegetation Model using a spatially explicit individual-based approach , 2007 .

[43]  Mark E. Harmon,et al.  Global-Scale Similarities in Nitrogen Release Patterns During Long-Term Decomposition , 2007, Science.

[44]  Bradley J. Cardinale,et al.  Effects of biodiversity on the functioning of trophic groups and ecosystems , 2006, Nature.

[45]  P. Balvanera,et al.  Quantifying the evidence for biodiversity effects on ecosystem functioning and services. , 2006, Ecology letters.

[46]  John F. Mustard,et al.  Invasive grass reduces aboveground carbon stocks in shrublands of the Western US , 2006 .

[47]  R. Schnur,et al.  Climate-carbon cycle feedback analysis: Results from the C , 2006 .

[48]  J. Subke,et al.  Trends and methodological impacts in soil CO2 efflux partitioning: A metaanalytical review , 2006 .

[49]  W. Post,et al.  Plant Respiration in a Warmer World , 2006, Science.

[50]  E. Davidson,et al.  Temperature sensitivity of soil carbon decomposition and feedbacks to climate change , 2006, Nature.

[51]  E. Hobbie Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. , 2006, Ecology.

[52]  Yakov Kuzyakov,et al.  Sources of CO2 efflux from soil and review of partitioning methods , 2006 .

[53]  R. Ceulemans,et al.  Mycorrhizal Hyphal Turnover as a Dominant Process for Carbon Input into Soil Organic Matter , 2006, Plant and Soil.

[54]  S. Scheu,et al.  Biodiversity and Litter Decomposition in Terrestrial Ecosystems , 2005 .

[55]  José M. V. Fragoso,et al.  Forecasting Regional to Global Plant Migration in Response to Climate Change , 2005 .

[56]  David A. Wardle,et al.  Effects of species and functional group loss on island ecosystem properties , 2005, Nature.

[57]  I. C. Prentice,et al.  A dynamic global vegetation model for studies of the coupled atmosphere‐biosphere system , 2005 .

[58]  G. Certini Effects of fire on properties of forest soils: a review , 2005, Oecologia.

[59]  K. Elder,et al.  Carbon limitation of soil respiration under winter snowpacks: potential feedbacks between growing season and winter carbon fluxes , 2005 .

[60]  F. Chapin,et al.  EFFECTS OF BIODIVERSITY ON ECOSYSTEM FUNCTIONING: A CONSENSUS OF CURRENT KNOWLEDGE , 2005 .

[61]  Alan H. Strahler,et al.  MODIS bidirectional reflectance distribution function and albedo Climate Modeling Grid products and the variability of albedo for major global vegetation types , 2005 .

[62]  David M. Richardson,et al.  Conifers as invasive aliens: a global survey and predictive framework , 2004 .

[63]  F. Woodward,et al.  Vegetation dynamics – simulating responses to climatic change , 2004, Biological reviews of the Cambridge Philosophical Society.

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

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

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

[67]  Z. Cardon,et al.  Decomposition dynamics in mixed‐species leaf litter , 2004 .

[68]  Helmut Hillebrand,et al.  On the Generality of the Latitudinal Diversity Gradient , 2004, The American Naturalist.

[69]  D. Wardle,et al.  Herbivore-mediated linkages between aboveground and belowground communities , 2003 .

[70]  Bruce A. Hungate,et al.  MYCORRHIZAL CONTROLS ON BELOWGROUND LITTER QUALITY , 2003 .

[71]  Aaron D. Peacock,et al.  PLANT DIVERSITY, SOIL MICROBIAL COMMUNITIES, AND ECOSYSTEM FUNCTION: ARE THERE ANY LINKS? , 2003 .

[72]  Vivek K. Arora,et al.  A Representation of Variable Root Distribution in Dynamic Vegetation Models , 2003 .

[73]  G. Bending Litter decomposition, ectomycorrhizal roots and the ‘Gadgil’ effect , 2003 .

[74]  F Stuart Chapin,et al.  Effects of plant traits on ecosystem and regional processes: a conceptual framework for predicting the consequences of global change. , 2003, Annals of botany.

[75]  Amy J. Symstad,et al.  Functional diversity revealed by removal experiments , 2003 .

[76]  Yadvinder Malhi,et al.  Increasing dominance of large lianas in Amazonian forests , 2002, Nature.

[77]  L. Comas,et al.  Linking root traits to potential growth rate in six temperate tree species , 2002, Oecologia.

[78]  P. Reich,et al.  The response of soil CO2 flux to changes in atmospheric CO2, nitrogen supply and plant diversity , 2001 .

[79]  S. Pacala,et al.  A METHOD FOR SCALING VEGETATION DYNAMICS: THE ECOSYSTEM DEMOGRAPHY MODEL (ED) , 2001 .

[80]  Katherine L. Gross,et al.  WHAT IS THE OBSERVED RELATIONSHIP BETWEEN SPECIES RICHNESS AND PRODUCTIVITY , 2001 .

[81]  T. Näsholm,et al.  Amino acid uptake: a widespread ability among boreal forest plants , 2001 .

[82]  N. Buchmann,et al.  Large-scale forest girdling shows that current photosynthesis drives soil respiration , 2001, Nature.

[83]  G. González,et al.  SOIL FAUNA AND PLANT LITTER DECOMPOSITION IN TROPICAL AND SUBALPINE FORESTS , 2001 .

[84]  F. Woodward,et al.  Global response of terrestrial ecosystem structure and function to CO2 and climate change: results from six dynamic global vegetation models , 2001 .

[85]  Ü. Rannik,et al.  Productivity overshadows temperature in determining soil and ecosystem respiration across European forests , 2001 .

[86]  J. Lawton,et al.  Consequences of the reduction of plant diversity for litter decomposition: effects through litter quality and microenvironment , 2000 .

[87]  R. B. Jackson,et al.  Global patterns of root turnover for terrestrial ecosystems , 2000 .

[88]  P. Vitousek,et al.  The role of polyphenols in terrestrial ecosystem nutrient cycling. , 2000, Trends in ecology & evolution.

[89]  K. Gaston Global patterns in biodiversity , 2000, Nature.

[90]  D. Wardle,et al.  PLANT REMOVALS IN PERENNIAL GRASSLAND: VEGETATION DYNAMICS, DECOMPOSERS, SOIL BIODIVERSITY, AND ECOSYSTEM PROPERTIES , 1999 .

[91]  Jonathan M. Levine,et al.  Elton revisited: a review of evidence linking diversity and invasibility , 1999 .

[92]  R. Bardgett,et al.  Linkages between plant litter diversity, soil microbial biomass and ecosystem function in temperate grasslands , 1999 .

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

[94]  Christopher E. Heil,et al.  Effects of Woody Plants on Microclimate in a Semiarid Woodland: Soil Temperature and Evaporation in Canopy and Intercanopy Patches , 1998, International Journal of Plant Sciences.

[95]  M. Mack,et al.  Impacts of biological invasions on disturbance regimes. , 1998, Trends in ecology & evolution.

[96]  Peter M. Vitousek,et al.  Effects of plant composition and diversity on nutrient cycling , 1998 .

[97]  F. J. Barnes,et al.  OVERSTORY-IMPOSED HETEROGENEITY IN SOLAR RADIATION AND SOIL MOISTURE IN A SEMIARID WOODLAND , 1997 .

[98]  R. Aerts,et al.  Initial litter respiration as indicator for long-term leaf litter decomposition of Carex species , 1997 .

[99]  Jean-Francois Lamarque,et al.  Variations in the predicted spatial distribution of atmospheric nitrogen deposition and their impact on carbon uptake by terrestrial ecosystems , 1997 .

[100]  Eileen H. Helmer,et al.  Root biomass allocation in the world's upland forests , 1997, Oecologia.

[101]  J. A. Barone,et al.  HERBIVORY AND PLANT DEFENSES IN TROPICAL FORESTS , 1996 .

[102]  Martin T. Sykes,et al.  Climate change, tree species distributions and forest dynamics: A case study in the mixed conifer/northern hardwoods zone of northern Europe , 1996 .

[103]  R. Ruess,et al.  Contributions of fine root production and turnover to the carbon and nitrogen cycling in taiga forests of the Alaskan interior , 1996 .

[104]  F. Stuart Chapin,et al.  Responses of Arctic Tundra to Experimental and Observed Changes in Climate , 1995 .

[105]  C. Potter,et al.  Global patterns of carbon dioxide emissions from soils on a 0.5-degree-grid-cell basis , 1995 .

[106]  Roderick C. Dewar,et al.  Carbon Allocation in Trees: a Review of Concepts for Modelling , 1994 .

[107]  David Tilman,et al.  Limiting Similarity in Mechanistic and Spatial Models of Plant Competition in Heterogeneous Environments , 1994, The American Naturalist.

[108]  V. Meentemeyer,et al.  Litter mass loss rates in pine forests of Europe and Eastern United States: some relationships with climate and litter quality , 1993 .

[109]  A. McGuire,et al.  Global climate change and terrestrial net primary production , 1993, Nature.

[110]  P. Vitousek,et al.  Biological invasions by exotic grasses, the grass/fire cycle, and global change , 1992 .

[111]  W. Schlesinger,et al.  The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate , 1992 .

[112]  F. Pierson,et al.  Variability of near-surface soil temperature on sagebrush rangeland. , 1991 .

[113]  D. M. Gates,et al.  Soil respiration of five aspen stands in northern lower Michigan , 1991 .

[114]  P. Matson Plant-soil interactions in primary succession at Hawaii Volcanoes National Park , 1990, Oecologia.

[115]  S. McNaughton,et al.  Ecosystem-level patterns of primary productivity and herbivory in terrestrial habitats , 1989, Nature.

[116]  Richard H. Waring,et al.  Forest Ecosystems: Concepts and Management , 1985 .

[117]  J. Aber,et al.  Fine Roots, Net Primary Production, and Soil Nitrogen Availability: A New Hypothesis , 1985 .

[118]  Sandra Brown,et al.  The Storage and Production of Organic Matter in Tropical Forests and Their Role in the Global Carbon Cycle , 1982 .

[119]  C. C. Grier,et al.  Above- and below-ground net production in 40-year-old Douglas-fir stands on low and high productivity sites , 1981 .

[120]  J. P. Grime Vegetation classification by reference to strategies , 1974, Nature.

[121]  I. Hiscock Communities and Ecosystems , 1970, The Yale Journal of Biology and Medicine.

[122]  J. Randerson,et al.  Technical Description of version 4.0 of the Community Land Model (CLM) , 2010 .

[123]  J. O H A N N E,et al.  Scaling environmental change through the community-level: a trait-based response-and-effect framework for plants , 2008 .

[124]  M. I C H A E,et al.  Carbon allocation in forest ecosystems , 2007 .

[125]  Millenium Ecosystem Assessment Ecosystems and human well-being: synthesis , 2005 .

[126]  Ian J. Wright,et al.  World-wide leaf economics spectrum , 2004 .

[127]  Inderjit,et al.  Root Exudates: an Overview , 2003 .

[128]  Peter M. Cox,et al.  Description of the "TRIFFID" Dynamic Global Vegetation Model , 2001 .

[129]  J. Raich,et al.  Vegetation and soil respiration: Correlations and controls , 2000 .

[130]  E. Schulze,et al.  Biomass allocation and water use under arid conditions , 1997 .

[131]  M. Lerdau,et al.  Allocation theory and chemical defense , 1997 .

[132]  S. Grayston,et al.  Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability , 1997 .

[133]  R. F. Doren,et al.  Effects of fire on different size individuals of Schinus terebinthifolius. , 1990 .

[134]  W. Lonsdale,et al.  Alien vegetation and native biota in tropical Australia: the impact of Mimosa pigra , 1989 .

[135]  Robert L. Sanford,et al.  Nutrient Cycling in Moist Tropical Forest , 1986 .

[136]  S S I T C H,et al.  Evaluation of Ecosystem Dynamics, Plant Geography and Terrestrial Carbon Cycling in the Lpj Dynamic Global Vegetation Model , 2022 .

[137]  M. P.R.,et al.  A METHOD FOR SCALING VEGETATION DYNAMICS: THE ECOSYSTEM DEMOGRAPHY MODEL (ED) , 2022 .