Do temperate tree species diversity and identity influence soil microbial community function and composition?

Abstract Studies of biodiversity–ecosystem function in treed ecosystems have generally focused on aboveground functions. This study investigates intertrophic links between tree diversity and soil microbial community function and composition. We examined how microbial communities in surface mineral soil responded to experimental gradients of tree species richness (SR), functional diversity (FD), community‐weighted mean trait value (CWM), and tree identity. The site was a 4‐year‐old common garden experiment near Montreal, Canada, consisting of deciduous and evergreen tree species mixtures. Microbial community composition, community‐level physiological profiles, and respiration were evaluated using phospholipid fatty acid (PLFA) analysis and the MicroResp™ system, respectively. The relationship between tree species richness and glucose‐induced respiration (GIR), basal respiration (BR), metabolic quotient (qCO 2) followed a positive but saturating shape. Microbial communities associated with species mixtures were more active (basal respiration [BR]), with higher biomass (glucose‐induced respiration [GIR]), and used a greater number of carbon sources than monocultures. Communities associated with deciduous tree species used a greater number of carbon sources than those associated with evergreen species, suggesting a greater soil carbon storage capacity. There were no differences in microbial composition (PLFA) between monocultures and SR mixtures. The FD and the CWM of several functional traits affected both BR and GIR. In general, the CWM of traits had stronger effects than did FD, suggesting that certain traits of dominant species have more effect on ecosystem processes than does FD. Both the functions of GIR and BR were positively related to aboveground tree community productivity. Both tree diversity (SR) and identity (species and functional identity—leaf habit) affected soil microbial community respiration, biomass, and composition. For the first time, we identified functional traits related to life‐history strategy, as well as root traits that influence another trophic level, soil microbial community function, via effects on BR and GIR.

[1]  Christian Messier,et al.  Leaf bacterial diversity mediates plant diversity and ecosystem function relationships , 2017, Nature.

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

[3]  C. L. Reardon,et al.  Soil microbial diversity and activity linked to crop yield and quality in a dryland organic wheat production system , 2016 .

[4]  Filippo Bussotti,et al.  Positive biodiversity-productivity relationship predominant in global forests , 2016, Science.

[5]  P. Reich,et al.  Lack of functional redundancy in the relationship between microbial diversity and ecosystem functioning , 2016 .

[6]  P. Reich,et al.  Functional identity is the main driver of diversity effects in young tree communities. , 2016, Ecology letters.

[7]  Eric Garnier,et al.  Plant Functional Diversity: Organism traits, community structure, and ecosystem properties , 2016 .

[8]  Michel Loreau,et al.  Contributions of a global network of tree diversity experiments to sustainable forest plantations , 2015, Ambio.

[9]  C. Engels,et al.  Plant diversity increases soil microbial activity and soil carbon storage , 2015, Nature Communications.

[10]  P. Reich,et al.  Tree communities rapidly alter soil microbial resistance and resilience to drought , 2015 .

[11]  C. Messier,et al.  Explaining forest productivity using tree functional traits and phylogenetic information: two sides of the same coin over evolutionary scale? , 2015, Ecology and evolution.

[12]  D. Hertel,et al.  Effects of tree identity dominate over tree diversity on the soil microbial community structure , 2015 .

[13]  A. Bérard,et al.  Use of the MicroResp TM method to assess Pollution-Induced Community Tolerance in the context of metal soil contamination , 2014 .

[14]  P. Reich,et al.  Advancing biodiversity–ecosystem functioning science using high-density tree-based experiments over functional diversity gradients , 2013, Oecologia.

[15]  C. Garbe.  Traits fonctionnels des arbres : de la plasticité intraspécifique aux effets de leur diversité sur le fonctionnement de l'écosystème , 2014 .

[16]  G. Gleixner,et al.  Seasonal differences in tree species influence on soil microbial communities , 2013 .

[17]  R. Kadmon,et al.  Functional trade-offs increase species diversity in experimental plant communities. , 2012, Ecology letters.

[18]  M. Lucas‐Borja,et al.  Altitude‐related factors but not Pinus community exert a dominant role over chemical and microbiological properties of a Mediterranean humid soil , 2012 .

[19]  G. Daily,et al.  Biodiversity loss and its impact on humanity , 2012, Nature.

[20]  P. Reich,et al.  Impacts of Biodiversity Loss Escalate Through Time as Redundancy Fades , 2012, Science.

[21]  Jarrett E. K. Byrnes,et al.  A global synthesis reveals biodiversity loss as a major driver of ecosystem change , 2012, Nature.

[22]  P. Reich,et al.  Forest productivity increases with evenness, species richness and trait variation: a global meta‐analysis , 2012 .

[23]  T. Wubet,et al.  Relationships Between Soil Microorganisms, Plant Communities, and Soil Characteristics in Chinese Subtropical Forests , 2012, Ecosystems.

[24]  D. Herman,et al.  Interactions between an arbuscular mycorrhizal fungus and a soil microbial community mediating litter decomposition. , 2012, FEMS microbiology ecology.

[25]  L. Dawson,et al.  Overstory and understory vegetation interact to alter soil community composition and activity , 2012, Plant and Soil.

[26]  B. Elberling,et al.  Soil respiration and rates of soil carbon turnover differ among six common European tree species , 2012 .

[27]  A. Bérard,et al.  Resilience of soil microbial communities impacted by severe drought and high temperature in the context of Mediterranean heat waves , 2011 .

[28]  Carlo Ricotta,et al.  CWM and Rao’s quadratic diversity: a unified framework for functional ecology , 2011, Oecologia.

[29]  Andrew Gonzalez,et al.  The functional role of producer diversity in ecosystems. , 2011, American journal of botany.

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

[31]  H. Fritze,et al.  Soil organic matter quality as a link between microbial community structure and vegetation composition along a successional gradient in a boreal forest , 2010 .

[32]  G. Gleixner,et al.  Direct and indirect effects of tree diversity drive soil microbial diversity in temperate deciduous forest , 2010 .

[33]  S. Scheu,et al.  Plant diversity effects on soil microorganisms support the singular hypothesis. , 2010, Ecology.

[34]  Todd H. Oakley,et al.  Using Phylogenetic, Functional and Trait Diversity to Understand Patterns of Plant Community Productivity , 2009, PloS one.

[35]  S. Scheu,et al.  Seasonal changes in the soil microbial community in a grassland plant diversity gradient four years after establishment , 2008 .

[36]  T. Hothorn,et al.  Simultaneous Inference in General Parametric Models , 2008, Biometrical journal. Biometrische Zeitschrift.

[37]  M. V. D. van der Heijden,et al.  The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. , 2008, Ecology letters.

[38]  Fabien Quétier,et al.  Assessing functional diversity in the field - methodology matters! , 2007 .

[39]  R. Artz,et al.  Assessing CLPPs using MicroResp™ , 2007 .

[40]  Anne-Béatrice Dufour,et al.  The ade4 Package: Implementing the Duality Diagram for Ecologists , 2007 .

[41]  W. Hendershot,et al.  Ion Exchange and Exchangeable Cations , 2007 .

[42]  Brian J Enquist,et al.  Ecological and evolutionary determinants of a key plant functional trait: wood density and its community-wide variation across latitude and elevation. , 2007, American journal of botany.

[43]  B. McConkey,et al.  Seasonal and long-term resource-related variations in soil microbial communities in wheat-based rotations of the Canadian prairie , 2006 .

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

[45]  S. Zechmeister-Boltenstern,et al.  Composition of the microbial communities in the mineral soil under different types of natural forest , 2005 .

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

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

[48]  A. Ives,et al.  Effects of species diversity on the primary productivity of ecosystems: extending our spatial and temporal scales of inference , 2004 .

[49]  F. Stuart Chapin,et al.  Functional Matrix: A Conceptual Framework for Predicting Multiple Plant Effects on Ecosystem Processes , 2003 .

[50]  T. Anderson.  Microbial eco-physiological indicators to asses soil quality , 2003 .

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

[52]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[53]  J. Potts,et al.  A Rapid Microtiter Plate Method To Measure Carbon Dioxide Evolved from Carbon Substrate Amendments so as To Determine the Physiological Profiles of Soil Microbial Communities by Using Whole Soil , 2003, Applied and Environmental Microbiology.

[54]  P. Hobbs,et al.  Soil microbial community, fertility, vegetation and diversity as targets in the restoration management of a meadow grassland , 2003 .

[55]  R. Bardgett,et al.  Accounting for variability in soil microbial communities of temperate upland grassland ecosystems , 2001 .

[56]  D. White,et al.  Landscape‐Level Patterns of Microbial Community Composition and Substrate Use in Upland Forest Ecosystems , 2001 .

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

[58]  R. Bardgett,et al.  Functional aspects of soil animal diversity in agricultural grasslands , 1998 .

[59]  D. Paré,et al.  Effects of tree species, stand age and soil type on soil microbial biomass and its activity in a southern boreal forest , 1998 .

[60]  Douglas M. Bates,et al.  LINEAR AND NONLINEAR MIXED-EFFECTS MODELS , 1998 .

[61]  B. Degens,et al.  Development of a physiological approach to measuring the catabolic diversity of soil microbial communities , 1997 .

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

[63]  D. Tilman,et al.  Plant diversity and ecosystem productivity: theoretical considerations. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[64]  K. Domsch,et al.  The metabolic quotient for CO2 (qCO2) as a specific activity parameter to assess the effects of environmental conditions, such as ph, on the microbial biomass of forest soils , 1993 .

[65]  K. Domsch,et al.  Determination of ecophysiological maintenance carbon requirements of soil microorganisms in a dormant state , 1985, Biology and Fertility of Soils.

[66]  G. Bouyoucos.  Hydrometer Method Improved for Making Particle Size Analyses of Soils1 , 1962 .

[67]  Patrick L. Thompson,et al.  A general biodiversity–function relationship is mediated by trophic level , 2017 .

[68]  Huimin Wang,et al.  Understory vegetation leads to changes in soil acidity and in microbial communities 27 years after reforestation. , 2015, The Science of the total environment.

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

[70]  C. Prescott,et al.  Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada , 2012 .

[71]  C. Messier,et al.  The effect of biodiversity on tree productivity: from temperate to boreal forests , 2011 .

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

[73]  Jean Thioulouse,et al.  The ade4 package - I : One-table methods , 2004 .

[74]  J. P. E. AND-N.  A PHYSIOLOGICAL METHOD FOR THE QUANTITATIVE MEASUREMENT OF MICROBIAL BIOMASS IN SOILS , 2022 .