Synthesis of plant-soil feedback effects on eastern North American tree species: implications for climate-adaptive forestry

Climate change represents an existential threat to many forest ecosystems because tree populations are often adapted to local climate means and variability. If tree populations cannot migrate or adapt, they risk becoming increasingly maladapted with climate change. This emerging mismatch underscores the need for climate adaptive management techniques, such as assisted migration of tree species, to help mitigate climate change impacts on forest ecosystems. Although biotic and abiotic factors are known to constrain tree establishment success, the extent to which they may determine the success of assisted migration plantings is poorly understood. Thus, defining the extent to which trees affect—and in turn are affected by local soil environments and microbial communities (i.e., plant-soil feedbacks; hereafter PSFs) remains important for guiding effective climate-adaptive forest management. Our objectives were to synthesize the current state of knowledge about the direction and magnitude of PSF effects on temperate tree species of eastern North America, and to identify key hypotheses important for guiding future research. To accomplish these goals, we conducted a meta-analysis of 26 peer-reviewed publications that addressed our criteria. Our compiled database included 61 tree species and was composed primarily of short-term greenhouse experiments that studied PSF effects by manipulating the soil biota in three ways: (1) soil was previously inoculated by a conspecific or heterospecific tree species (i.e., home vs. away), (2) soil was live or sterilized, or (3) soil was untreated or treated with fungicide. We found that PSF had significant effects on tree growth, with the direction and magnitude of PSF strongly dependent on tree mycorrhizal guild. Arbuscular mycorrhizal tree species grown in live or home soils grew 13–33% less than those in sterile or away soils, while ectomycorrhizal tree species grew 11–44% more in live or home than sterile or away soils. PSF effects were associated with several plant functional traits, including specific leaf area, tissue nitrogen, and specific root length. We provide suggestions on incorporating PSFs into assisted migration trials and outline key knowledge gaps for future research. Our synthesis of context-dependent effects of PSFs on tree performance will help inform management decisions involving assisted migration.

[1]  Xugao Wang,et al.  Rhizosphere fungal community assembly varied across functional guilds in a temperate forest , 2023, Ecological Processes.

[2]  G. Decocq,et al.  First report of ectomycorrhizae in Prunus serotina in the exotic range , 2022, Plant and Soil.

[3]  T. Canam,et al.  Plant performance responds to intraspecific variation in soil inocula from individual Solidago clones , 2021, Plant Ecology.

[4]  Liu Xiaoli,et al.  Effects of Slope Aspect and Rainfall on Belowground Deep Fine Root Traits and Aboveground Tree Height , 2021, Frontiers in Plant Science.

[5]  P. Cuijpers,et al.  Meta-Regression , 2021, Doing Meta-Analysis with R.

[6]  M. Umaña,et al.  Tree growth increases through opposing above‐ground and below‐ground resource strategies , 2021, Journal of Ecology.

[7]  M. Bahn,et al.  Relationships between plant–soil feedbacks and functional traits , 2021, Journal of Ecology.

[8]  Warwick J Allen,et al.  Soil sample pooling generates no consistent inference bias: a meta-analysis of 71 plant-soil feedback experiments. , 2021, The New phytologist.

[9]  N. Eisenhauer,et al.  Tree species rather than type of mycorrhizal association drives inorganic and organic nitrogen acquisition in tree-tree interactions. , 2021, Tree physiology.

[10]  P. Kardol,et al.  Multi‐dimensionality as a path forward in plant‐soil feedback research , 2021, Journal of Ecology.

[11]  T. M. Bezemer,et al.  Plant-Soil Feedbacks and Temporal Dynamics of Plant Diversity-Productivity Relationships. , 2021, Trends in ecology & evolution.

[12]  Nico Eisenhauer,et al.  Mixing tree species associated with arbuscular or ectotrophic mycorrhizae reveals dual mycorrhization and interactive effects on the fungal partners , 2021, Ecology and evolution.

[13]  T. M. Bezemer,et al.  Globally, plant‐soil feedbacks are weak predictors of plant abundance , 2021, Ecology and evolution.

[14]  David Ward Shade affects fine-root morphology in range-encroaching eastern redcedars (Juniperus virginiana) more than competition, soil fertility and pH , 2021 .

[15]  M. Friesen,et al.  Microbial Inoculants: Silver Bullet or Microbial Jurassic Park? , 2020, Trends in microbiology.

[16]  D. A. Moeller,et al.  Plant-soil interactions limit lifetime fitness outside a native plant's geographic range margin. , 2020, Ecology.

[17]  D. Orwig,et al.  Seedling survival declines with increasing conspecific density in a common temperate tree , 2020 .

[18]  I. Stehlik,et al.  Assisted species migration and hybridization to conserve cold‐adapted plants under climate change , 2020, Conservation biology : the journal of the Society for Conservation Biology.

[19]  Jessica A. M. Moore,et al.  Predicting Plant-Soil Feedback in the Field: Meta-Analysis Reveals That Competition and Environmental Stress Differentially Influence PSF , 2020, Frontiers in Ecology and Evolution.

[20]  A. Prasad,et al.  Combining US and Canadian forest inventories to assess habitat suitability and migration potential of 25 tree species under climate change , 2020, Diversity and Distributions.

[21]  M. Cadotte,et al.  Tree mycorrhizal type mediates the strength of negative density dependence in temperate forests , 2020, Journal of Ecology.

[22]  M. Zobel,et al.  How mycorrhizal associations drive plant population and community biology , 2020, Science.

[23]  Julie R. Etterson,et al.  Assisted migration across fixed seed zones detects adaptation lags in two major North American tree species , 2020, Ecological applications : a publication of the Ecological Society of America.

[24]  M. Vellend,et al.  Soil abiotic and biotic properties constrain the establishment of a dominant temperate tree into boreal forests , 2020, Journal of Ecology.

[25]  J. H. Burns,et al.  Individual Plant-Soil Feedback Effects Influence Tree Growth and Rhizosphere Fungal Communities in a Temperate Forest Restoration Experiment , 2020, Frontiers in Ecology and Evolution.

[26]  Denis Bastianelli,et al.  TRY plant trait database - enhanced coverage and open access. , 2019, Global change biology.

[27]  J. Parker,et al.  Tree Diversity Reduces Fungal Endophyte Richness and Diversity in a Large-Scale Temperate Forest Experiment , 2019 .

[28]  R. Kobe,et al.  Site Soil-Fertility and Light Availability Influence Plant-Soil Feedback , 2019, Front. Ecol. Evol..

[29]  R. Standish,et al.  Benefits of mycorrhizal inoculation to ecological restoration depend on plant functional type, restoration context and time , 2019, Fungal Ecology.

[30]  J. Bever,et al.  When and where plant-soil feedback may promote plant coexistence: a meta-analysis. , 2019, Ecology letters.

[31]  Claude A. Garcia,et al.  The global tree restoration potential , 2019, Science.

[32]  J. A. Bennett,et al.  Mechanisms of plant-soil feedback: interactions among biotic and abiotic drivers. , 2018, The New phytologist.

[33]  Ellen L. Fry,et al.  Why are plant–soil feedbacks so unpredictable, and what to do about it? , 2018, Functional Ecology.

[34]  Joel L. Pick,et al.  Reproducible, flexible and high‐throughput data extraction from primary literature: The metaDigitise r package , 2018, Methods in Ecology and Evolution.

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

[36]  J. Alexander,et al.  Do soil biota influence the outcome of novel interactions between plant competitors? , 2018, The Journal of ecology.

[37]  J. Bever,et al.  Relative importance of competition and plant-soil feedback, their synergy, context dependency and implications for coexistence. , 2018, Ecology letters.

[38]  R. Garibay-Orijel,et al.  Ectomycorrhizal fungal communities in high mountain conifer forests in central Mexico and their potential use in the assisted migration of Abies religiosa , 2018, Mycorrhiza.

[39]  C. Talbot,et al.  Information Underload: Ecological Complexity, Incomplete Knowledge, and Data Deficits Create Challenges for the Assisted Migration of Forest Trees , 2018 .

[40]  E. Cardillo,et al.  Topographic effects on dispersal patterns of Phytophthora cinnamomi at a stand scale in a Spanish heathland , 2018, bioRxiv.

[41]  K. Reinhart,et al.  Toward more robust plant-soil feedback research. , 2018, Ecology.

[42]  K. Beard,et al.  Live long and prosper: plant-soil feedback, lifespan, and landscape abundance covary. , 2017, Ecology.

[43]  S. Goetz,et al.  Vulnerability of eastern US tree species to climate change , 2017, Global change biology.

[44]  J. Bever,et al.  Negative plant-phyllosphere feedbacks in native Asteraceae hosts - a novel extension of the plant-soil feedback framework. , 2017, Ecology letters.

[45]  H. Reynolds,et al.  The next frontier of plant–soil feedback research: unraveling context dependence across biotic and abiotic gradients , 2017 .

[46]  S. Fei,et al.  Divergence of species responses to climate change , 2017, Science Advances.

[47]  J. A. Bennett,et al.  Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics , 2017, Science.

[48]  Benjamin L Turner,et al.  PLANT ECOLOGY: Plant‐soil feedback and the maintenance of diversity in Mediterranean‐climate shrublands , 2017 .

[49]  A. Weigelt,et al.  Plant–soil feedbacks: role of plant functional group and plant traits , 2016 .

[50]  T. M. Bezemer,et al.  Soil inoculation steers restoration of terrestrial ecosystems , 2016, Nature Plants.

[51]  Benjamin L Turner,et al.  An ectomycorrhizal nitrogen economy facilitates monodominance in a neotropical forest. , 2016, Ecology letters.

[52]  J. Bever,et al.  Maintenance of Plant Species Diversity by Pathogens , 2015 .

[53]  K. Treseder,et al.  Sources of inocula influence mycorrhizal colonization of plants in restoration projects: a meta‐analysis , 2015 .

[54]  Keenan M. L. Mack,et al.  Plant‐soil feedbacks as drivers of succession: evidence from remnant and restored tallgrass prairies , 2015 .

[55]  J. Bever,et al.  Mycorrhizal response trades off with plant growth rate and increases with plant successional status. , 2015, Ecology.

[56]  W. Dawson,et al.  Testing the Plant Growth-Defense Hypothesis Belowground: Do Faster-Growing Herbaceous Plant Species Suffer More Negative Effects from Soil Biota than Slower-Growing Ones? , 2015, The American Naturalist.

[57]  H. Lambers,et al.  Phosphorus limitation, soil-borne pathogens and the coexistence of plant species in hyperdiverse forests and shrublands. , 2015, The New phytologist.

[58]  E. Kiers,et al.  Partner selection in the mycorrhizal mutualism. , 2015, The New phytologist.

[59]  R. Bardgett,et al.  Are plant-soil feedback responses explained by plant traits? , 2014, The New phytologist.

[60]  P. Midford,et al.  Patterns in root traits of woody species hosting arbuscular and ectomycorrhizas: implications for the evolution of belowground strategies , 2014, Ecology and evolution.

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

[62]  M. Whitlock,et al.  Assisted Gene Flow to Facilitate Local Adaptation to Climate Change , 2013 .

[63]  E. Siemann,et al.  Plant-soil biota interactions of an invasive species in its native and introduced ranges: implications for invasion success. , 2013 .

[64]  C. Messier,et al.  Interspecific coordination and intraspecific plasticity of fine root traits in North American temperate tree species , 2013, Front. Plant Sci..

[65]  I. Ibáñez,et al.  Plant–soil feedback links negative distance dependence and light gradient partitioning during seedling establishment , 2013 .

[66]  Katherine N. Suding,et al.  Plant–soil feedbacks: the past, the present and future challenges , 2013 .

[67]  T. Fukami,et al.  Consequences of plant–soil feedbacks in invasion , 2013 .

[68]  W. H. van der Putten,et al.  Climate Change, Aboveground-Belowground Interactions, and Species' Range Shifts , 2012 .

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

[70]  R. Vilgalys,et al.  Evaluating the impacts of multiple generalist fungal pathogens on temperate tree seedling survival. , 2012, Ecology.

[71]  J. Kranabetter,et al.  Divergence in ectomycorrhizal communities with foreign Douglas-fir populations and implications for assisted migration. , 2012, Ecological applications : a publication of the Ecological Society of America.

[72]  C. Vriesendorp,et al.  Conspecific density dependence in seedlings varies with species shade tolerance in a wet tropical forest. , 2011, Ecology letters.

[73]  B. Kaplin,et al.  Seed Germination of Habenaria repens (Orchidaceae) in situ Beyond its Range, and its Potential for Assisted Migration Imposed by Climate Change , 2011 .

[74]  Spyros Konstantopoulos,et al.  Fixed effects and variance components estimation in three‐level meta‐analysis , 2011, Research synthesis methods.

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

[76]  Keenan M. L. Mack,et al.  Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest , 2010, Nature.

[77]  Wolfgang Viechtbauer,et al.  Conducting Meta-Analyses in R with the metafor Package , 2010 .

[78]  Matthias C. Rillig,et al.  Does herbivory really suppress mycorrhiza? A meta‐analysis , 2010 .

[79]  Jason D. Hoeksema,et al.  A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. , 2010, Ecology letters.

[80]  R. Miller,et al.  Resource limitation is a driver of local adaptation in mycorrhizal symbioses , 2010, Proceedings of the National Academy of Sciences.

[81]  E. Veenendaal,et al.  Plant–soil interactions in the expansion and native range of a poleward shifting plant species , 2010 .

[82]  C. Field,et al.  The velocity of climate change , 2009, Nature.

[83]  J. Zimmerman,et al.  Abiotic and biotic drivers of seedling survival in a hurricane‐impacted tropical forest , 2009 .

[84]  K. Beard,et al.  Plant-soil feedbacks: a meta-analytical review. , 2008, Ecology letters.

[85]  H P Possingham,et al.  Assisted Colonization and Rapid Climate Change , 2008, Science.

[86]  R. Kobe,et al.  Tolerance of soil pathogens co-varies with shade tolerance across species of tropical tree seedlings. , 2008, Ecology.

[87]  J. Malcolm,et al.  Canopy cover mediates interactions between a specialist caterpillar and seedlings of a neotropical tree , 2007 .

[88]  C. Augspurger,et al.  Host Specificity of Pathogenic Pythium Species: Implications for Tree Species Diversity , 2007 .

[89]  B. Casper,et al.  Evaluating plant-soil feedback together with competition in a serpentine grassland. , 2007, Ecology letters.

[90]  Ü. Niinemets,et al.  Tolerance to shade, drought, and waterlogging of temperate northern hemisphere trees and shrubs , 2006 .

[91]  Paul Kardol,et al.  Temporal variation in plant-soil feedback controls succession. , 2006, Ecology letters.

[92]  J. Ehrenfeld,et al.  FEEDBACK IN THE PLANT-SOIL SYSTEM , 2005 .

[93]  W. H. van der Putten,et al.  Soil feedback and pathogen activity in Prunus serotina throughout its native range , 2005 .

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

[95]  P. Adler,et al.  A meta‐analysis of biotic resistance to exotic plant invasions , 2004 .

[96]  P. A. Mason,et al.  The influence of spatial patterns of damping‐off disease and arbuscular mycorrhizal colonization on tree seedling establishment in Ghanaian tropical forest soil , 2004 .

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

[98]  Alex C Rodriguez,et al.  Soil biota and exotic plant invasion , 2004, Nature.

[99]  J. Bever,et al.  Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. , 2003, The New phytologist.

[100]  G. Yohe,et al.  A globally coherent fingerprint of climate change impacts across natural systems , 2003, Nature.

[101]  David A. Wardle,et al.  Communities and Ecosystems: Linking the Aboveground and Belowground Components , 2002 .

[102]  J. Klironomos Feedback with soil biota contributes to plant rarity and invasiveness in communities , 2002, Nature.

[103]  J. Lovett-Doust,et al.  Plant strategies, vegetation processes, and ecosystem properties , 2002 .

[104]  R. Shaw,et al.  Range shifts and adaptive responses to Quaternary climate change. , 2001, Science.

[105]  A. Packer,et al.  Soil pathogens and spatial patterns of seedling mortality in a temperate tree , 2000, Nature.

[106]  Jessica Gurevitch,et al.  THE META‐ANALYSIS OF RESPONSE RATIOS IN EXPERIMENTAL ECOLOGY , 1999 .

[107]  Mark G. Tjoelker,et al.  Close association of RGR, leaf and root morphology, seed mass and shade tolerance in seedlings of nine boreal tree species grown in high and low light , 1998 .

[108]  James D. Bever,et al.  INCORPORATING THE SOIL COMMUNITY INTO PLANT POPULATION DYNAMICS : THE UTILITY OF THE FEEDBACK APPROACH , 1997 .

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

[110]  S. Pacala,et al.  Forest models defined by field measurements : Estimation, error analysis and dynamics , 1996 .

[111]  J. Bever Feeback between Plants and Their Soil Communities in an Old Field Community , 1994 .

[112]  B. Ellis,et al.  The time-course of disease suppression and antibiosis by the ectomycorrhizal fungus Paxillus involutus. , 1989, The New phytologist.

[113]  F. Stuart Chapin,et al.  Resource Availability and Plant Antiherbivore Defense , 1985, Science.

[114]  C. Augspurger,et al.  Pathogen mortality of tropical tree seedlings: experimental studies of the effects of dispersal distance, seedling density, and light conditions , 1984, Oecologia.

[115]  David B. Pillemer,et al.  Summing Up: The Science of Reviewing Research , 1984 .

[116]  W. G. Cochran The combination of estimates from different experiments. , 1954 .

[117]  P. Antunes,et al.  Fungal inoculants in the field: Is the reward greater than the risk? , 2018 .

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

[119]  S. LeDuc,et al.  Ectomycorrhizal inoculum potential of northeastern US forest soils for American chestnut restoration: results from field and laboratory bioassays , 2013, Mycorrhiza.

[120]  J. Maron,et al.  Soil fungal pathogens and the relationship between plant diversity and productivity. , 2011, Ecology letters.

[121]  E. Leigh,et al.  Challenges Associated With Testing And Falsifying The Janzen–Connell Hypothesis: A Review and Critique , 2008 .

[122]  D. J. Shure,et al.  PATCH-SIZE EFFECTS ON PLANT PHENOLICS IN SUCCESSIONAL OPENINGS OF THE SOUTHERN APPALACHIANS' , 1993 .

[123]  J. Connell On the role of the natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees , 1971 .