Advertisement

Soil Biota as Drivers of Plant Community Assembly

  • Paul Kardol
  • Jonathan R. De Long
  • Pierre Mariotte
Chapter
Part of the Ecological Studies book series (ECOLSTUD, volume 234)

Abstract

Evidence is accumulating that belowground soil organisms are strong drivers of the aboveground plant community. In this chapter, we examine how soil communities influence plant community assembly through priority effects, soil legacy effects, and niche modification. We discuss how different functional groups of soil organisms drive competitive interactions, species coexistence, and species turnover. We then explore how primary and secondary successional trajectories can be altered by soil communities and delve into the mechanisms by which soil communities can affect ecosystem restoration and biodiversity conservation. Finally, we discuss the role of soil biota in plant invasion and range expansion and how soil biota interact with global environmental changes to affect plant community composition. We conclude by outlining knowledge gaps and propose potential avenues for addressing these gaps via upscaling of measurements, enhanced experimental design, and the utilization of plant and soil organism traits.

Notes

Acknowledgements

We thank Tadashi Fukami and Benjamin Sikes for their helpful comment on an earlier version of the manuscript. Financial support to PK was provided by the Swedish Research Council (Vetenskapsrådet).

References

  1. Allen MF, Crisafulli C, Friese CF et al (1992) Re-formation of mycorrhizal symbiosis on Mount St Helens, 1980–1990 – interaction of rodents and mycorrhizal fungi. Mycol Res 96:447–453CrossRefGoogle Scholar
  2. Aprahamian AM, Lulow ME, Major MR et al (2016) Arbuscular mycorrhizal inoculation in coastal sage scrub restoration. Botany 94:493–499CrossRefGoogle Scholar
  3. Augé RM, Toler HD, Saxton AM (2015) Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza 25:13–24PubMedCrossRefGoogle Scholar
  4. Bais HP, Vepachedu R, Gilroy S et al (2003) Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301:1377–1380PubMedCrossRefGoogle Scholar
  5. Banning NC, Gleeson DB, Grigg AH et al (2011) Soil microbial community successional patterns during forest ecosystem restoration. Appl Environ Microbiol 77:6158–6164PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511CrossRefGoogle Scholar
  7. Bardgett RD, Jones AC, Jones DL et al (2001) Soil microbial community patterns related to the history and intensity of grazing in sub-montane ecosystems. Soil Biol Biochem 33:1653–1664CrossRefGoogle Scholar
  8. Bardgett RD, Richter A, Bol R et al (2007) Heterotrophic microbial communities use ancient carbon following glacial retreat. Biol Lett 3:487–490PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bauman JM, Keiffer CH, Hiremath S et al (2013) Soil preparation methods promoting ectomycorrhizal colonization and American chestnut Castanea dentata establishment in coal mine restoration. J Appl Ecol 50:721–729CrossRefGoogle Scholar
  10. Bennett JA, Cahill JF (2016) Fungal effects on plant-plant interactions contribute to grassland plant abundances: evidence from the field. J Ecol 104:755–764CrossRefGoogle Scholar
  11. Berg MP, Kiers ET, Driessen G et al (2010) Adapt or disperse: understanding species persistence in a changing world. Glob Change Biol 16:587–598CrossRefGoogle Scholar
  12. Bever JD, Mangan SA, Alexander HM (2015) Maintenance of plant species diversity by pathogens. Annu Rev Ecol Evol Syst 46:305–325CrossRefGoogle Scholar
  13. Blomqvist MM, Olff H, Blaauw MB et al (2000) Interactions between above- and belowground biota: importance for small-scale vegetation mosaics in a grassland ecosystem. Oikos 90:582–598CrossRefGoogle Scholar
  14. Bokhorst S, Kardol P, Bellingham PJ et al (2017) Responses of communities of soil organisms and plants to soil aging at two contrasting long-term chronosequences. Soil Biol Biochem 106:69–79CrossRefGoogle Scholar
  15. Bradford MA, Jones TH, Bardgett RD, et al (2002) Impacts of soil faunal community composition on model grassland ecosystems. Science 298:615–618PubMedCrossRefGoogle Scholar
  16. Brankatschk R, Towe S, Kleineidam K et al (2011) Abundances and potential activities of nitrogen cycling microbial communities along a chronosequence of a glacier forefield. ISME J 5:1025–1037PubMedCrossRefGoogle Scholar
  17. Bravo-Monasterio P, Pauchard A, Fajardo A (2016) Pinus contorta invasion into treeless steppe reduces species richness and alters species traits of the local community. Biol Invasions 18:1883–1894CrossRefGoogle Scholar
  18. Brinkman EP, Troelstra SR, van der Putten WH (2005) Soil feedback effects to the foredune grass Ammophila arenaria by endoparasitic root-feeding nematodes and whole soil communities. Soil Biol Biochem 37:2077–2087CrossRefGoogle Scholar
  19. Brinkman EP, Duyts H, Karssen G et al (2015) Plant-feeding nematodes in coastal sand dunes: occurrence, host specificity and effects on plant growth. Plant Soil 397:17–30CrossRefGoogle Scholar
  20. Brown VK, Gange AC (1990) Insect herbivory below ground. Adv Ecol Res 20:1–58CrossRefGoogle Scholar
  21. Burkle LA, Belote RT (2015) Soil mutualists modify priority effects on plant productivity, diversity, and composition. Appl Veg Sci 18:332–342CrossRefGoogle Scholar
  22. Callaway RM, Thelen GC, Rodriguez HWE (2004) Soil biota and exotic plant invasion. Nature 427:731–733PubMedPubMedCentralCrossRefGoogle Scholar
  23. Carbajo V, den Braber B, van der Putten WH et al (2011) Enhancement of late successional plants on ex-arable land by soil inoculations. PLoS One 6:e21943PubMedPubMedCentralCrossRefGoogle Scholar
  24. Cavagnaro TR, Bender SF, Asghari HR et al (2015) The role of arbuscular mycorrhizas in reducing soil nutrient loss. Trends Plant Sci 20:283–290PubMedCrossRefGoogle Scholar
  25. Cesarz S, Reich PB, Scheu S et al (2015) Nematode functional guilds, not trophic groups, reflect shifts in soil food webs and processes in response to interacting global change factors. Pedobiologia 58:23–32CrossRefGoogle Scholar
  26. Chan KY (2001) An overview of some tillage impacts on earthworm population abundance and diversity – implications for functioning in soils. Soil Tillage Res 57:179–191CrossRefGoogle Scholar
  27. Chase JM (2003) Community assembly: when should history matter? Oecologia 136:489–498PubMedCrossRefGoogle Scholar
  28. Classen AT, Sundqvist MK, Henning JA et al (2015) Direct and indirect effects of climate change on soil microbial and soil microbial-plant interactions: what lies ahead? Ecosphere 6:1–21CrossRefGoogle Scholar
  29. Collins CG, Carey CJ, Aronson EL et al (2016) Direct and indirect effects of native range expansion on soil microbial community structure and function. J Ecol 104:1271–1283CrossRefGoogle Scholar
  30. Crowther TW, Bradford MA (2013) Thermal acclimation in widespread heterotrophic soil microbes. Ecol Lett 16:469–477PubMedCrossRefPubMedCentralGoogle Scholar
  31. De Deyn GB, Raaijmakers CE, Zoomer HR et al (2003) Soil invertebrate fauna enhances grassland succession and diversity. Nature 422:711–713CrossRefGoogle Scholar
  32. De Deyn GB, Raaijmakers CE, van der Putten WH (2004) Plant community development is affected by nutrients and soil biota. J Ecol 92:824–834CrossRefGoogle Scholar
  33. de Graaff MA, Adkins J, Kardol P et al (2015) A meta-analysis of soil biodiversity impacts on the carbon cycle. SOIL 1:257–271CrossRefGoogle Scholar
  34. de la Peña E, Baeten L, Steel H et al (2016) Beyond plant–soil feedbacks: mechanisms driving plant community shifts due to land-use legacies in post-agricultural forests. Funct Ecol 30:1073–1085CrossRefGoogle Scholar
  35. de Leon DG, Moora M, Opik M et al (2016) Symbiont dynamics during ecosystem succession: co-occurring plant and arbuscular mycorrhizal fungal communities. FEMS Microbiol Ecol 92:fiw097CrossRefGoogle Scholar
  36. De Long JR, Laudon H, Blume-Werry G et al (2016) Nematode community resistant to deep soil frost in boreal forest soils. Pedobiologia 59:243–251CrossRefGoogle Scholar
  37. de Vries FT, Shade A (2013) Controls on soil microbial community stability under climate change. Front Microbiol 4:265PubMedPubMedCentralCrossRefGoogle Scholar
  38. de Vries FT, Thébault E, Liiri M et al (2013) Soil food web properties explain ecosystem services across European land use systems. Proc Natl Acad Sci USA 110:14296–14301Google Scholar
  39. del Moral R (1983) Initial recovery of subalpine vegetation on Mount St Helens, Washington. Am Midl Nat 109:72–80CrossRefGoogle Scholar
  40. Despain DG (2001) Dispersal ecology of lodgepole pine (Pinus contorta Dougl.) in its native environment as related to Swedish forestry. For Ecol Manage 141:59–68CrossRefGoogle Scholar
  41. Dickie IA, St John MG, Yeates GW et al (2014) Belowground legacies of Pinus contorta invasion and removal result in multiple mechanisms of invasional meltdown. AoB Plants 6:15CrossRefGoogle Scholar
  42. Diez JM, Dickie I, Edwards G et al (2010) Negative soil feedbacks accumulate over time for non-native plant species. Ecol Lett 13:803–809PubMedCrossRefPubMedCentralGoogle Scholar
  43. Engelkes T, Morriën E, Verhoeven KJF et al (2008) Successful range-expanding plants experience less above-ground and below-ground enemy impact. Nature 456:946–948PubMedPubMedCentralCrossRefGoogle Scholar
  44. Eppinga MB, Rietkerk M, Dekker SC et al (2006) Accumulation of local pathogens: a new hypothesis to explain exotic plant invasions. Oikos 114:168–176CrossRefGoogle Scholar
  45. Eschen R, Müller-Schärer H, Schaffner U (2009) Aboveground environment type, soil nutrient content and arbuscular mycorrhizal fungi explain establishment success of Centaurea jacea on ex-arable land and in late-successional grasslands. Plant Soil 322:115–123CrossRefGoogle Scholar
  46. Fraterrigo JM, Balser TC, Turner MG (2006) Microbial community variation and its relationship with nitrogen mineralization in historically altered forests. Ecology 87:570–579PubMedCrossRefPubMedCentralGoogle Scholar
  47. Fukami T (2015) Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu Rev Ecol Evol Syst 46:1–23CrossRefGoogle Scholar
  48. Fukami T, Nakajima M (2013) Complex plant-soil interactions enhance plant species diversity by delaying community convergence. J Ecol 101:316–324CrossRefGoogle Scholar
  49. Gange AC, Brown VK, Farmer LM (1990) A test of mycorrhizal benefit in an early successional plant community. New Phytol 115:85–91CrossRefGoogle Scholar
  50. Gehring CA, Swaty R, Deckert E (2017) Mycorrhizas, drought, and host-plant mortality. In: Johnson NC, Gehring CA, Jansa J (eds) Mycorrhizal mediation of soil. Fertility, structure, and carbon storage. Elsevier, Amsterdam, pp 279–298CrossRefGoogle Scholar
  51. George PBL, Lindo Z (2015) Application of body size spectra to nematode trait-index analyses. Soil Biol Biochem 84:15–20CrossRefGoogle Scholar
  52. Gioria M, Osborne BA (2014) Resource competition in plant invasions: emerging patterns and research needs. Front Plant Sci 5:21CrossRefGoogle Scholar
  53. Gómez-Aparicio L, Ibáñez B, Serrano MS et al (2012) Spatial patterns of soil pathogens in declining Mediterranean forests: implications for tree species regeneration. New Phytol 194:1014–1024PubMedCrossRefPubMedCentralGoogle Scholar
  54. Green PT, O’Dowd DJ, Abbott KL et al (2011) Invasional meltdown: invader-invader mutualism facilitates a secondary invasion. Ecology 92:1758–1768PubMedCrossRefPubMedCentralGoogle Scholar
  55. Grigulis K, Lavorel S, Krainer U et al (2013) Relative contributions of plant traits and soil microbial properties to mountain grassland ecosystem services. J Ecol 101:47–57CrossRefGoogle Scholar
  56. Grman E, Suding KN (2010) Within-year soil legacies contribute to strong priority effects of exotics on native California grassland communities. Restor Ecol 18:664–670CrossRefGoogle Scholar
  57. Gundale MJ, Kardol P, Nilsson M-C et al (2014) Interactions with soil biota shift from negative to positive when a tree species is moved outside its native range. New Phytol 202:415–421PubMedCrossRefPubMedCentralGoogle Scholar
  58. Hamel C, Plenchette C (2017) Implications of past, current, and future agricultural practices for mycorrhiza-mediated nutrient flux. In: Johnson NC, Gehring C, Jansa J (eds) Mycorrhizal mediation of soil. Fertility, structure, and carbon storage. Elsevier, Amsterdam, pp 175–186CrossRefGoogle Scholar
  59. Hamman ST, Hawkes CV (2013) Biogeochemical and microbial legacies of non-native grasses can affect restoration success. Restor Ecol 21:58–66CrossRefGoogle Scholar
  60. Hedlund K, Gormsen D (2002) Mycorrhizal colonization of plants in set-aside agricultural land. Appl Soil Ecol 19:71–78CrossRefGoogle Scholar
  61. Helm DJ, Carling DE (1993) Use of soil transfer for reforestation on abandoned mined lands in Alaska. 2. Effects of soil transfer from different successional stages on growth and mycorrhizal formation by Populus balsamifera and Alnus crispa. Mycorrhiza 3:107–114CrossRefGoogle Scholar
  62. Hodkinson ID, Webb NR, Coulson SJ (2002) Primary community assembly on land - the missing stages: why are the heterotrophic organisms always there first? J Ecol 90:569–577CrossRefGoogle Scholar
  63. Hoeksema JD (2005) Plant-plant interactions vary with different mycorrhizal fungus species. Biol Lett 1:439–442PubMedPubMedCentralCrossRefGoogle Scholar
  64. Jangid K, Williams MA, Franzluebbers AJ et al (2011) Land-use history has a stronger impact on soil microbial community composition than aboveground vegetation and soil properties. Soil Biol Biochem 43:2184–2193CrossRefGoogle Scholar
  65. Jassey VE, Chiapusio G, Binet P et al (2013) Above- and belowground linkages in Sphagnum peatland: climate warming affects plant-microbial interactions. Glob Change Biol 19:811–823PubMedCrossRefGoogle Scholar
  66. Kardol P, Bezemer TM, van der Putten WH (2006) Temporal variation in plant-soil feedback controls succession. Ecol Lett 9:1080–1088PubMedPubMedCentralCrossRefGoogle Scholar
  67. Kardol P, Cornips NJ, van Kempen MML et al (2007) Microbe-mediated plant-soil feedback causes historical contingency effects in plant community assembly. Ecol Monogr 77:147–162CrossRefGoogle Scholar
  68. Kardol P, Bezemer TM, van der Putten WH (2009) Soil organism and plant introductions in restoration of species-rich grassland communities. Restor Ecol 17:258–269CrossRefGoogle Scholar
  69. Kardol P, De Long JR, Sundqvist MK (2012) Crossing the threshold: the power of multi-level experiments in identifying global change responses. New Phytol 196:323–326PubMedCrossRefGoogle Scholar
  70. Kardol P, De Deyn GB, Laliberté E et al (2013) Biotic plant-soil feedbacks across temporal scales. J Ecol 101:309–315CrossRefGoogle Scholar
  71. Kaufmann R (2001) Invertebrate succession on an alpine glacier foreland. Ecology 82:2261–2278CrossRefGoogle Scholar
  72. Kazemi S, Hatam I, Lanoil B (2016) Bacterial community succession in a high-altitude subarctic glacier foreland is a three-stage process. Mol Ecol 25:5557–5567PubMedCrossRefGoogle Scholar
  73. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  74. Keller KR (2014) Mutualistic rhizobia reduce plant diversity and alter community composition. Oecologia 176:1101–1109PubMedCrossRefGoogle Scholar
  75. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70PubMedPubMedCentralCrossRefGoogle Scholar
  76. Kostenko O, van de Voorde TFJ, Mulder PPJ et al (2012) Legacy effects of aboveground-belowground interactions. Ecol Lett 15:813–821CrossRefPubMedPubMedCentralGoogle Scholar
  77. Koziol L, Bever JD (2015) Mycorrhizal response trades off with plant growth rate and increases with plant successional status. Ecology 96:1768–1774PubMedCrossRefGoogle Scholar
  78. Koziol L, Bever JD (2016) AMF, phylogeny, and succession: specificity of response to mycorrhizal fungi increases for late-successional plants. Ecosphere 7(11):e01555CrossRefGoogle Scholar
  79. Kranabetter JM (2004) Ectomycorrhizal community effects on hybrid spruce seedling growth and nutrition in clearcuts. Can J Bot 82:983–991CrossRefGoogle Scholar
  80. Kuebbing SE, Patterson CM, Classen AT et al (2016) Co-occurring nonnative woody shrubs have additive and non-additive soil legacies. Ecol Appl 26:1896–1906PubMedCrossRefGoogle Scholar
  81. Kulmatiski A, Beard KH, Stark JM (2006) Soil history as a primary control on plant invasion in abandoned agricultural fields. J Appl Ecol 43:868–876CrossRefGoogle Scholar
  82. Kulmatiski A, Hines J, Eisenhauer N (2014) Soil organism effects on grassland production and diversity. In: Mariotte P, Kardol P (eds) Grassland biodiversity and conservation in a changing world. Nova Science Publishers Inc., New York, pp 27–49Google Scholar
  83. Laflower DM, Hurteau MD, Koch GW et al (2016) Climate-driven changes in forest succession and the influence of management on forest carbon dynamics in the Puget Lowlands of Washington State, USA. For Ecol Manage 362:194–204CrossRefGoogle Scholar
  84. Laliberté E, Turner BL, Costes T et al (2012) Experimental assessment of nutrient limitation along a 2-million-year dune chronosequence in the south-western Australia biodiversity hotspot. J Ecol 100:631–642CrossRefGoogle Scholar
  85. Lankau RA, Nuzzo V, Spyreas G et al (2009) Evolutionary limits ameliorate the negative impact of an invasive plant. Proc Natl Acad Sci USA 106:15362–15367PubMedCrossRefGoogle Scholar
  86. Lankau RA, Zhu K, Ordonez A (2015) Mycorrhizal strategies of tree species correlate with trailing range edge responses to current and past climate change. Ecology 96:1451–1458CrossRefGoogle Scholar
  87. Lavelle P, Bignell A, Lepage M et al (1997) Soil function in a changing world: the role of invertebrate ecosystem engineers. Eur J Soil Biol 33:159–193Google Scholar
  88. Liao CZ, Peng RM, Luo YQ et al (2008) Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–714PubMedCrossRefGoogle Scholar
  89. Mangan SA, Schnitzer SA, Herre EA et al (2010) Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–755CrossRefGoogle Scholar
  90. Mariotte P, Le Bayon R-C, Eisenhauer GC et al (2016) Subordinate plant species moderate drought effects on earthworm communities in grasslands. Soil Biol Biochem 96:119–127CrossRefGoogle Scholar
  91. Mariotte P, Canarini A, Dijkstra FA (2017) Stoichiometric N:P flexibility and mycorrhizal symbiosis favor plant resistance against drought. J Ecol 105:958–967CrossRefGoogle Scholar
  92. Maron JL, Vila M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373CrossRefGoogle Scholar
  93. Maron JL, Klironomos J, Waller L et al (2014) Invasive plants escape from suppressive soil biota at regional scales. J Ecol 102:19–27CrossRefGoogle Scholar
  94. Maron JL, Smith AL, Ortega YK et al (2016) Negative plant-soil feedbacks increase with plant abundance, and are unchanged by competition. Ecology 97:2055–2063PubMedCrossRefGoogle Scholar
  95. McDonald BA, Stukenbrock EH (2016) Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security. Philos Trans R Soc B 371:20160026CrossRefGoogle Scholar
  96. McGeoch MA, Butchart SHM, Spear D et al (2010) Global indicators of biological invasion: species numbers, biodiversity impact and policy responses. Divers Distrib 16:95–108CrossRefGoogle Scholar
  97. Middleton EL, Bever JD (2012) Inoculation with a native soil community advances succession in a grassland restoration. Restor Ecol 20:218–226CrossRefGoogle Scholar
  98. Milcu A, Paul S, Lukac M (2011) Belowground interactive effects of elevated CO2, plant diversity and earthworms in grassland microcosms. Basic Appl Ecol 12:600–608CrossRefGoogle Scholar
  99. Molina-Montenegro MA, Oses R, Torres-Diaz C et al (2015) Fungal endophytes associated with roots of nurse cushion species have positive effects on native and invasive beneficiary plants in an alpine ecosystem. Perspect Plant Ecol Evol Syst 17:218–226CrossRefGoogle Scholar
  100. Montesinos-Navarro A, Segarra-Moragues JG, Valiente-Banuet A et al (2016) Fungal phylogenetic diversity drives plant facilitation. Oecologia 181:533–541PubMedCrossRefGoogle Scholar
  101. Moora M, Zobel M (2009) Arbuscular mycorrhiza and plant-plant interactions – impact of invisible world on visible patterns. In: Pugnaire FI (ed) Positive interactions and plant community dynamic. CRC Press, Boca Ration, pp 79–98Google Scholar
  102. Morriën E, van der Putten WH (2013) Soil microbial community structure of range-expanding plant species differs from co-occurring natives. J Ecol 101:1093–1102CrossRefGoogle Scholar
  103. Nara K (2006) Pioneer dwarf willow may facilitate tree succession by providing late colonizers with compatible ectomycorrhizal fungi in a primary successional volcanic desert. New Phytol 171:187–198PubMedCrossRefGoogle Scholar
  104. Nielsen UN, Ayres E, Wall DH et al (2011) Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity-function relationships. Eur J Soil Sci 62:105–116CrossRefGoogle Scholar
  105. O’Dowd DJ, Green PT, Lake PS (2003) Invasional ‘meltdown’ on an oceanic island. Ecol Lett 6:812–817CrossRefGoogle Scholar
  106. Obase K, Tamai Y, Yajima T et al (2008) Mycorrhizal colonization status of plant species established in an exposed area following the 2000 eruption of Mt. Usu, Hokkaido, Japan. Landsc Ecol Eng 4:57–61CrossRefGoogle Scholar
  107. Paudel S, Wilson GWT, MacDonald B et al (2016) Predicting spatial extent of invasive earthworms on an oceanic island. Divers Distrib 22:1013–1023CrossRefGoogle Scholar
  108. Pellegrino E, Bedini A (2014) Enhancing ecosystem services in sustainable agriculture: biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biol Biochem 68:429–439CrossRefGoogle Scholar
  109. Pendergast TH, Burke DJ, Carson WP (2013) Belowground biotic complexity drives aboveground dynamics: a test of the soil community feedback model. New Phytol 197:1300–1310PubMedCrossRefPubMedCentralGoogle Scholar
  110. Perring MP, Standish RJ, Price JN et al (2015) Advances in restoration ecology: rising to the challenges of the coming decades. Ecosphere 6:25CrossRefGoogle Scholar
  111. Pieterse CMJ, Zamioudis C, Berendsen RL et al (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375CrossRefGoogle Scholar
  112. Pineiro J, Maestre FT, Bartolome L et al (2013) Ecotechnology as a tool for restoring degraded drylands: a meta-analysis of field experiments. Ecol Eng 61:133–144CrossRefGoogle Scholar
  113. Polley HW, Johnson HB, Derner JD (2003) Increasing CO2 from subambient to superambient concentrations alters species composition and increases above-ground biomass in a C3/C4 grassland. New Phytol 160:319–327CrossRefGoogle Scholar
  114. Reynolds HL, Packer A, Bever JD et al (2003) Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291CrossRefGoogle Scholar
  115. Rodriguez-Echeverria S, Armas A, Piston N et al (2013) A role for below-ground biota in plant-plant facilitation. J Ecol 101:1420–1428CrossRefGoogle Scholar
  116. Schmidt SK, Reed SC, Nemergut DR et al (2008) The earliest stages of ecosystem succession in high-elevation (5000 metres above sea level), recently deglaciated soils. Proc R Soc Lond B Biol Sci 275:2793–2802PubMedCrossRefGoogle Scholar
  117. Sikes BA, Hawkes CV, Fukami T (2016) Plant and root endophyte assembly history: interactive effects on native and exotic plants. Ecology 97:484–493PubMedCrossRefGoogle Scholar
  118. Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919PubMedCrossRefGoogle Scholar
  119. Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32CrossRefGoogle Scholar
  120. Sonnemann I, Hempel S, Beutel M et al (2013) The root herbivore history of the soil affects the productivity of a grassland plant community and determines plant response to new root herbivore attack. Plos One 8:e56524.  https://doi.org/10.1371/journal.pone.0056524PubMedPubMedCentralCrossRefGoogle Scholar
  121. Staddon PL, Gregersen R, Jakobsen I (2004) The response of two Glomus mycorrhizal fungi and a fine endophyte to elevated atmospheric CO2, soil warming and drought. Glob Change Biol 10:1909–1921CrossRefGoogle Scholar
  122. Stinson KA, Campbell SA, Powell JR et al (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:727–731CrossRefGoogle Scholar
  123. Stuble KL, Souza L (2016) Priority effects: natives, but not exotics, pay to arrive late. J Ecol 104:987–993CrossRefGoogle Scholar
  124. Taylor DL, Hollingsworth TN, McFarland JW et al (2014) A first comprehensive census of fungi in soil reveals both hyperdiversity and fine-scale niche partitioning. Ecol Monogr 84:3–20CrossRefGoogle Scholar
  125. Teste FP, Kardol P, Turner BL et al (2017) Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Science 355:173–176CrossRefGoogle Scholar
  126. Thébault A, Mariotte P, Lortie CJ et al (2014) Land management trumps the effects of climate change and elevated CO2 on grassland functioning. J Ecol 102:896–904CrossRefGoogle Scholar
  127. Titus JH, del Moral R (1998) Seedling establishment in different microsites on Mount St. Helens, Washington, USA. Plant Ecol 134:13–26CrossRefGoogle Scholar
  128. van de Voorde TFJ, van der Putten WH, Bezemer TM (2011) Intra- and interspecific plant-soil interactions, soil legacies and priority effects during old-field succession. J Ecol 99:945–953CrossRefGoogle Scholar
  129. van der Heijden MGA (2010) Mycorrhizal fungi reduce nutrient loss from model grassland ecosystems. Ecology 91:1163–1171PubMedCrossRefPubMedCentralGoogle Scholar
  130. van der Heijden MGA, Horton TR (2009) Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol 97:1139–1150CrossRefGoogle Scholar
  131. van der Heijden MGA, Klironomos JN, Ursic M et al (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72CrossRefGoogle Scholar
  132. van der Putten WH (2012) Climate change, aboveground-belowground interactions, and species’ range shifts. Annu Rev Ecol Evol Syst 43:365–383CrossRefGoogle Scholar
  133. van der Putten WH, van Dijk C, Peters BAM (1993) Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 362:53–56CrossRefGoogle Scholar
  134. van der Putten WH, Macel M, Visser ME (2010) Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Philos Trans R Soc B 365:2025–2034CrossRefGoogle Scholar
  135. van der Putten WH, Bardgett RD, Bever JD et al (2013) Plant-soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276CrossRefGoogle Scholar
  136. van der Stoel CD, van der Putten WH, Duyts H (2002) Development of a negative plant-soil feedback in the expansion zone of the clonal grass Ammophila arenaria following root formation and nematode colonization. J Ecol 90:978–988CrossRefGoogle Scholar
  137. van der Wal A, van Veen JA, Smant W et al (2006) Fungal biomass development in a chronosequence of land abandonment. Soil Biol Biochem 38:51–60CrossRefGoogle Scholar
  138. van Groenigen JW, Lubbers IM, Vos HMJ et al (2014) Earthworms increase plant production: a meta-analysis. Sci Rep-UK 4:6365.  https://doi.org/10.1038/srep06365
  139. van Grunsven RHA, van der Putten WH, Bezemer TM et al (2007) Reduced plant-soil feedback of plant species expanding their range as compared to natives. J Ecol 95:1050–1057CrossRefGoogle Scholar
  140. van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245PubMedCrossRefGoogle Scholar
  141. van Kleunen M, Dawson W, Essl F et al (2015) Global exchange and accumulation of non-native plants. Nature 525:100–103PubMedCrossRefPubMedCentralGoogle Scholar
  142. Vitousek PM, Walker LR, Whiteaker LD et al (1987) Biological invasions by Myrica faya alters ecosystem development in Hawaii. Science 238:802–804PubMedCrossRefPubMedCentralGoogle Scholar
  143. Vitousek PM, Walker LR, Whiteaker LD et al (1993) Nutrient limitations to plant growth during primary succession in Hawaii Volcanos National Park. Biogeochemistry 23:197–215CrossRefGoogle Scholar
  144. Wagg C, Jansa J, Schmid B et al (2011) Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol Lett 14:1001–1009PubMedCrossRefGoogle Scholar
  145. Wagg C, Bender SF, Widmer F et al (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci USA 111:5266–5270PubMedPubMedCentralCrossRefGoogle Scholar
  146. Wang D, Yang SM, Tang F et al (2012) Symbiosis specificity in the legume – rhizobial mutualism. Cell Microbiol 14:334–342PubMedCrossRefGoogle Scholar
  147. Wanner M, Elmer M, Sommer M et al (2015) Testate amoebae colonizing a newly exposed land surface are of airborne origin. Ecol Indic 48:55–62CrossRefGoogle Scholar
  148. Wardle DA, Bardgett RD, Klironomos JN et al (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633CrossRefGoogle Scholar
  149. Weller DM, Raaijmakers JM, Gardener BBM et al (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348PubMedCrossRefGoogle Scholar
  150. Widenfalk LA, Malmström A, Berg MP et al (2016) Small-scale Collembola community composition in a pine forest soil – overdispersion in functional traits indicates the importance of species interactions. Soil Biol Biochem 103:52–62CrossRefGoogle Scholar
  151. Wilschut RA, Geisen S, ten Hooven FC et al (2016) Interspecific differences in nematode control between range-expanding plant species and their congeneric natives. Soil Biol Biochem 100:233–241CrossRefGoogle Scholar
  152. Wubs ERJ, van der Putten WH, Bosch M et al (2016) Soil inoculation steers restoration of terrestrial ecosystems. Nat Plants 2:16107Google Scholar
  153. Wurst S, Ohgushi T (2015) Do plant- and soil-mediated legacy effects impact future biotic interactions? Funct Ecol 29:1373–1382CrossRefGoogle Scholar
  154. Wurst S, Langel R, Scheu S (2005) Do endogeic earthworms change plant competition? A microcosm study. Plant Soil 271:123–130CrossRefGoogle Scholar
  155. Yuste JC, Penuelas J, Estiarte M et al (2011) Drought-resistant fungi control soil organic matter decomposition and its response to temperature. Glob Change Biol 17:1475–1486CrossRefGoogle Scholar
  156. Zhang NL, van der Putten WH, Veen GF (2016) Effects of root decomposition on plant-soil feedback of early- and mid-successional plant species. New Phytol 212:220–231PubMedCrossRefPubMedCentralGoogle Scholar
  157. Zobel M, Opik M (2014) Plant and arbuscular mycorrhizal fungal (AMF) communities - which drives which? J Veg Sci 25:1133–1140CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Paul Kardol
    • 1
  • Jonathan R. De Long
    • 2
  • Pierre Mariotte
    • 3
    • 4
  1. 1.Department of Forest Ecology and ManagementSwedish University of Agricultural SciencesUmeåSweden
  2. 2.Department of Terrestrial EcologyNetherlands Institute of EcologyWageningenThe Netherlands
  3. 3.Ecole Polytechnique Fédérale de Lausanne (EPFL)School of Architecture, Civil and Environmental Engineering (ENAC), Laboratory of Ecological Systems (ECOS)LausanneSwitzerland
  4. 4.Swiss Federal Institute for Forest, Snow and Landscape Research (WSL)LausanneSwitzerland

Personalised recommendations