Postrestoration colonization suggests slow regeneration, plant translocation barriers, and other host/symbiont lessons during the United Nations' Decade on Ecosystem Restoration

Mycorrhizal restoration benefits are widely acknowledged, yet factors underpinning this success remain unclear. To illuminate when natural regeneration might be sufficient, we investigated the degree mycorrhizal fungi would colonize Populus fremontii (Fremont cottonwood) 2 years after the restoration of a riparian corridor, in the presence of an adjacent source. We compared colonization levels across plant populations and ecotypes, and from trees in the planted area to those in natural source populations. Four findings contribute to the theory and application of host–symbiont interactions. (1) Median ectomycorrhizal colonization of trees in the planted area was less than one‐tenth of that within natural source populations (p < 0.05), suggesting that even with adjacent intact habitat, sluggish regeneration would make proactive mycorrhizal restoration beneficial. (2) Within the planted area, median ectomycorrhizal and arbuscule colonization of trees sourced from greater distances were less than one‐third of that for trees sourced locally (p < 0.05), suggesting translocation poses barriers to symbioses. (3) Changes in colonization did not align with plant ecotypes, suggesting that geographic scales of selection for plants and fungi differ. (4) Slight increases in median mycorrhizal colonization (from 0% to 5%) were strongly correlated with increased survival for the plant provenance with lowest survival (r2 = 46% and rs = 48%, p < 0.05), suggesting mycorrhizae are particularly beneficial when plants are under stress (including translocation‐induced stress). This study is novel in demonstrating that mycorrhizal regeneration is slow even in the presence of adjacent intact habitat, and that when colonization could seem negligible, it may still have biological significance.

[1]  T. May,et al.  What Do the First 597 Global Fungal Red List Assessments Tell Us about the Threat Status of Fungi? , 2022, Diversity.

[2]  M. Bowker,et al.  Sympatric soil biota mitigate a warmer‐drier climate for Bouteloua gracilis , 2022, Global change biology.

[3]  M. Rillig,et al.  Arbuscular mycorrhizal root colonization depends on the spatial distribution of the host plants , 2022, Mycorrhiza.

[4]  G. D. De Deyn,et al.  Soil microbiota as game-changers in restoration of degraded lands , 2022, Science.

[5]  K. Hultine,et al.  Tradeoffs between leaf cooling and hydraulic safety in a dominant arid land riparian tree species. , 2022, Plant, cell & environment.

[6]  F. Pope,et al.  ‘Can't see the forest for the trees’: The importance of fungi in the context of UK tree planting , 2022, Food and Energy Security.

[7]  R. Weinberg Restoration , 2021, Canadian Medical Association Journal.

[8]  Arvind A. R. Bhuta,et al.  Challenges to the Reforestation Pipeline in the United States , 2021, Frontiers in Forests and Global Change.

[9]  C. Sáenz-Romero,et al.  Assisted Migration Field Tests in Canada and Mexico: Lessons, Limitations, and Challenges , 2020, Forests.

[10]  J. Abatzoglou,et al.  Warmer and Drier Fire Seasons Contribute to Increases in Area Burned at High Severity in Western US Forests From 1985 to 2017 , 2020, Geophysical Research Letters.

[11]  S. Shuster,et al.  Intraspecific Genetic Variation and Species Interactions Contribute to Community Evolution , 2020 .

[12]  K. Hultine,et al.  Adaptive trait syndromes along multiple economic spectra define cold and warm adapted ecotypes in a widely distributed foundation tree species , 2020, Journal of Ecology.

[13]  Jennifer M. Bhatnagar,et al.  Back to Roots: The Role of Ectomycorrhizal Fungi in Boreal and Temperate Forest Restoration , 2020, Frontiers in Forests and Global Change.

[14]  D. Gömöry,et al.  Assisted migration vs. close-to-nature forestry: what are the prospects for tree populations under climate change? , 2020, Central European Forestry Journal.

[15]  T. Kolb,et al.  Familiar soil conditions help Pinus ponderosa seedlings cope with warming and drying climate , 2020, Restoration Ecology.

[16]  Mark A. White,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.

[17]  C. Doughty,et al.  Adaptive capacity in the foundation tree species Populus fremontii: implications for resilience to climate change and non-native species invasion in the American Southwest , 2020, Conservation physiology.

[18]  Manuel R. Guariguata,et al.  International principles and standards for the practice of ecological restoration. Second edition , 2019, Restoration Ecology.

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

[20]  C. Guerra,et al.  Global mismatches in aboveground and belowground biodiversity , 2019, Conservation biology : the journal of the Society for Conservation Biology.

[21]  K. Grady,et al.  Genotypic variation in phenological plasticity: Reciprocal common gardens reveal adaptive responses to warmer springs but not to fall frost , 2018, Global change biology.

[22]  K. Saikkonen,et al.  Glyphosate decreases mycorrhizal colonization and affects plant-soil feedback. , 2018, The Science of the total environment.

[23]  M. Schwartz,et al.  Amplifying plant disease risk through assisted migration , 2018, Conservation Letters.

[24]  C. Azcón-Aguilar,et al.  Root metabolic plasticity underlies functional diversity in mycorrhiza-enhanced stress tolerance in tomato. , 2018, The New phytologist.

[25]  Z. Münzbergová,et al.  Slow recovery of arbuscular mycorrhizal fungi and plant community after fungicide application: An eight‐year experiment , 2018, Journal of Vegetation Science.

[26]  H. Spiecker,et al.  Cold adaptation recorded in tree rings highlights risks associated with climate change and assisted migration , 2018, Nature Communications.

[27]  C. Doughty,et al.  Mycorrhizal symbioses influence the trophic structure of the Serengeti , 2018 .

[28]  M. Lucas‐Borja,et al.  Lack of local adaptation to the establishment conditions limits assisted migration to adapt drought-prone Pinus nigra populations to climate change , 2018 .

[29]  Evan Bolton,et al.  Database resources of the National Center for Biotechnology Information , 2017, Nucleic Acids Res..

[30]  B. Lindahl,et al.  Retention of seed trees fails to lifeboat ectomycorrhizal fungal diversity in harvested Scots pine forests , 2017, FEMS microbiology ecology.

[31]  Dana H. Ikeda,et al.  Genetically informed ecological niche models improve climate change predictions , 2017, Global change biology.

[32]  A. Bucharova Assisted migration within species range ignores biotic interactions and lacks evidence , 2017 .

[33]  L. J. Lamit,et al.  Tree genotype influences ectomycorrhizal fungal community structure: Ecological and evolutionary implications , 2016 .

[34]  J. Bever,et al.  AMF, phylogeny, and succession: specificity of response to mycorrhizal fungi increases for late‐successional plants , 2016 .

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

[36]  Jason D. Hoeksema,et al.  Home-field advantage? evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis , 2016, BMC Evolutionary Biology.

[37]  John H. Werren,et al.  Holes in the Hologenome: Why Host-Microbe Symbioses Are Not Holobionts , 2016, mBio.

[38]  J. Cahill,et al.  Ectomycorrhizal fungi mediate indirect effects of a bark beetle outbreak on secondary chemistry and establishment of pine seedlings. , 2015, The New phytologist.

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

[40]  David B. Neale,et al.  The Evolution of Forest Genetics and Tree Improvement Research in the United States , 2015 .

[41]  K. Theis,et al.  Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes , 2015, PLoS biology.

[42]  R. Miller,et al.  Mycorrhizal phenotypes and the Law of the Minimum. , 2015, The New phytologist.

[43]  N. Johnson,et al.  Uncoupling the effects of phosphorus and precipitation on arbuscular mycorrhizas in the Serengeti , 2015, Plant and Soil.

[44]  Stephanie N. Kivlin,et al.  Fungal Symbionts Alter Plant Drought Response , 2013, Microbial Ecology.

[45]  C. Gehring,et al.  Disrupting mycorrhizal mutualisms: a potential mechanism by which exotic tamarisk outcompetes native cottonwoods. , 2012, Ecological applications : a publication of the Ecological Society of America.

[46]  T. Kolb,et al.  Genetic variation in productivity of foundation riparian species at the edge of their distribution: implications for restoration and assisted migration in a warming climate , 2011 .

[47]  R. Azcón,et al.  Azospirillum and arbuscular mycorrhizal colonization enhance rice growth and physiological traits under well-watered and drought conditions. , 2011, Journal of plant physiology.

[48]  M. Garbelotto,et al.  Evidence of dispersal limitation in soil microorganisms: isolation reduces species richness on mycorrhizal tree islands. , 2010, Ecology.

[49]  Ian M. Fingerman,et al.  Database resources of the National Center for Biotechnology Information , 2010, Nucleic Acids Res..

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

[51]  J. Frank,et al.  Mycorrhizas on nursery and field seedlings of Quercus garryana , 2009, Mycorrhiza.

[52]  E. Rosenberg,et al.  Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. , 2008, FEMS microbiology reviews.

[53]  M. Allen,et al.  Efflux of hydraulically lifted water from mycorrhizal fungal hyphae during imposed drought , 2008, Plant signaling & behavior.

[54]  K. Ineichen,et al.  The cultivation bias: different communities of arbuscular mycorrhizal fungi detected in roots from the field, from bait plants transplanted to the field, and from a greenhouse trap experiment , 2007, Mycorrhiza.

[55]  M. Rillig,et al.  Mycorrhizas and soil structure , 2006 .

[56]  T. Whitham,et al.  Environmental and genetic effects on the formation of ectomycorrhizal and arbuscular mycorrhizal associations in cottonwoods , 2006, Oecologia.

[57]  J. Cairney,et al.  Ectomycorrhizal fungal communities in young forest stands regenerating after clearcut logging. , 2003, The New phytologist.

[58]  E. Allen,et al.  SHIFTS IN ARBUSCULAR MYCORRHIZAL COMMUNITIES ALONG AN ANTHROPOGENIC NITROGEN DEPOSITION GRADIENT , 2000 .

[59]  T. Grove,et al.  Working with Mycorrhizas in Forestry and Agriculture , 1996 .

[60]  N. Dickinson,et al.  Metal resistance in trees: the role of mycorrhizae , 1995 .

[61]  Steven L. Miller,et al.  Root-gap dynamics in a lodgepole pine forest: ectomycorrhizal and nonmycorrhizal fine root activity after experimental gap formation , 1994 .

[62]  D. Tilman,et al.  Plant and Soil Controls on Mycorrhizal Fungal Communities , 1992 .

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

[64]  A. Saxton,et al.  Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis , 2014, Mycorrhiza.

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

[66]  C. Raghavender,et al.  Approach for enhancing mycorrhiza - mediated disease resistance of tomato damping-off , 2012 .

[67]  Karen A. Koestner,et al.  Threats to Western United States Riparian Ecosystems: A Bibliography , 2012 .

[68]  T. Whitham,et al.  Ecological Communities: Biodiversity is related to indirect interactions among species of large effect , 2007 .

[69]  David J. Buttler,et al.  Second Edition , 2007 .

[70]  M. Allen,et al.  Differential modulation of host plant δ13C and δ18O by native and nonnative arbuscular mycorrhizal fungi in a semiarid environment , 2006 .

[71]  K. Nara Ectomycorrhizal networks and seedling establishment during early primary succession. , 2006, The New phytologist.