Advertisement

Plant and Soil

, Volume 444, Issue 1–2, pp 71–85 | Cite as

Litter-driven feedbacks influence plant colonization of a high elevation early successional ecosystem

  • Clifton P. Bueno de MesquitaEmail author
  • Steven K. Schmidt
  • Katharine N. Suding
Regular Article
First Online:
  • 200 Downloads

Abstract

Aims

Plant-microbe interactions are crucial components of ecosystem development but are understudied during early succession. The goal of this study was to investigate species-specific effects of plants on unvegetated soils being colonized by plants as climate changes, and assess how plant-soil feedbacks influence plant succession.

Methods

We used lab and field litter additions in an early successional unvegetated ecosystem in the Front Range of the Colorado Rocky Mountains to examine litter-driven changes in soil bacterial and fungal communities. We then used plant litter-trained soil as inocula in a greenhouse experiment to test plant-soil feedbacks.

Results

We found species-specific effects of litter additions on bacterial and fungal communities in unvegetated soils, which are likely due to both differences in tissue litter chemistry and differences in the litter microbiome. We identified a negative effect of soil trained by litter from the conservative forb Silene acaulis on the growth of the fast-growing bunchgrass Deschampsia cespitosa, likely due to changes in microbial communities that resulted in lowered nitrification rates or to a litter-driven increase in N-immobilization.

Conclusions

Our study demonstrates the importance of plant specificity and potential negative litter-driven feedbacks in primary succession, which could lead to patchy distribution of plant colonists as climate change allows colonization of these areas.

Keywords

Plant-microbe interactions Succession Plant-soil feedback Litter 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

We thank Elise Castle for help in the greenhouse, Piper Dumont for help in the lab, Anna Wright for help in the field, and Sam Sartwell for help in the lab and field. Marko Spasojevic and Sören Weber provided foliar C:N data. We thank Bill Bowman, Noah Fierer and Dan Doak for feedback on this experiment. Logistical support was provided by the Niwot Ridge LTER program (NSF DEB 1637686) and CU Mountain Research Station. Funding was provided by NSF grant DEB 1457827 to KNS and SKS. We would also like to acknowledge the suggestions of two anonymous reviewers, whose input greatly improved this manuscript.

Supplementary material

11104_2019_4242_MOESM1_ESM.docx (1.5 mb)
ESM 1 (DOCX 1.50 mb)

References

  1. Abarenkov K, Nilsson RH, Larsson KH et al (2010) The UNITE database for molecular identification of fungi - recent updates and future perspectives. New Phytol 186:281–285CrossRefGoogle Scholar
  2. Amaral-Zettler LA, McCliment EA, Ducklow HW, Huse SM (2009) A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS One 4.  https://doi.org/10.1371/journal.pone.0006372 CrossRefGoogle Scholar
  3. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  4. Austin AT, Vivanco L (2006) Plant litter decomposition in a semi-arid ecosystem controlled by photodegradation. Nature 442:555–558.  https://doi.org/10.1038/nature05038 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bais HP, Vepachedu R, Gilroy S (2003) Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301(80):1377–1380CrossRefGoogle Scholar
  6. Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20:634–641.  https://doi.org/10.1016/j.tree.2005.08.005 CrossRefGoogle Scholar
  7. Bellemain E, Carlsen T, Brochmann C, Coissac E, Taberlet P, Kauserud H (2010) ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiol 10:189.  https://doi.org/10.1186/1471-2180-10-189 CrossRefPubMedCentralGoogle Scholar
  8. Berendse F (1990) Organic matter accumulation and nitrogen mineralization during secondary succession in heathland ecosystems. J Ecol 78:413–427CrossRefGoogle Scholar
  9. Berendse F (1998) Effects of dominant plant species on soils during succession in nutrient-poor ecosystems. Biogeochemistry 42:73–88CrossRefGoogle Scholar
  10. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microb Ecol 68:1–13.  https://doi.org/10.1111/j.1574-6941.2009.00654.x CrossRefGoogle Scholar
  11. Bever JD (2002) Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proc R Soc B Biol Sci 269:2595–2601.  https://doi.org/10.1098/rspb.2002.2162 CrossRefGoogle Scholar
  12. Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85:561–573CrossRefGoogle Scholar
  13. Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, Rillig MC, Stock WD, Tibbett M, Zobel M (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478.  https://doi.org/10.1016/j.tree.2010.05.004 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bueno de Mesquita CP, Knelman JE, King AJ, Farrer EC, Porazinska DL, Schmidt SK, Suding KN (2017) Plant colonization of moss-dominated soils in the alpine: microbial and biogeochemical implications. Soil Biol Biochem 111:135–142.  https://doi.org/10.1016/j.soilbio.2017.04.008 CrossRefGoogle Scholar
  15. Bueno de Mesquita CP, Tillmann LS, Bernard CD, Rosemond KC, Molotch NP, Suding KN (2018) Topographic heterogeneity explains patterns of vegetation response to climate change (1972–2008) across a mountain landscape, Niwot ridge, Colorado. Arct Antarct Alp Res 50:e1504492.  https://doi.org/10.1080/15230430.2018.1504492 CrossRefGoogle Scholar
  16. Caine N (2010) Recent hydrologic change in a Colorado alpine basin: an indicator of permafrost thaw? Ann Glaciol 51:130–134CrossRefGoogle Scholar
  17. Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive. Front Ecol Environ 2:436–443CrossRefGoogle Scholar
  18. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high- throughput community sequencing data. Nature 7:335–336.  https://doi.org/10.1038/nmeth0510-335 CrossRefGoogle Scholar
  19. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624.  https://doi.org/10.1038/ismej.2012.8 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Cázares E, Trappe JM, Jumpponen A (2005) Mycorrhiza-plant colonization patterns on a subalpine glacier forefront as a model system of primary succession. Mycorrhiza 15:405–416.  https://doi.org/10.1007/s00572-004-0342-1 CrossRefPubMedGoogle Scholar
  21. Chapin FS, Walker LR, Fastie CL, Sharman LC (1994) Mechanisms of Primary Succession Following Deglaciation at Glacier Bay, AlaskaGoogle Scholar
  22. Corti G, Ugolini FC, Agnelli A, Certini G, Cuniglio R, Berna F, Fernández Sanjurjo MJ (2002) The soil skeleton, a forgotten pool of carbon and nitrogen in soil. Eur J Soil Sci 53:283–298.  https://doi.org/10.1046/j.1365-2389.2002.00442.x CrossRefGoogle Scholar
  23. Darcy JL, Schmidt SK, Knelman JE et al (2018) Phosphorus, not nitrogen, limits plants and microbial primary producers following glacial retreat. Sci Adv 4:eaaq0942CrossRefGoogle Scholar
  24. DeSantis TZ, Hugenholtz P, Larsen N et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072.  https://doi.org/10.1128/AEM.03006-05 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Di Marino E, Scattolin L, Bodensteiner P, Agerer R (2008) Sistotrema is a genus with ectomycorrhizal species - confirmation of what sequence studies already suggested. Mycol Prog 7:169–176.  https://doi.org/10.1007/s11557-008-0562-4 CrossRefGoogle Scholar
  26. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998.  https://doi.org/10.1038/nmeth.2604 CrossRefGoogle Scholar
  27. Edwards IP, Bürgmann H, Miniaci C, Zeyer J (2006) Variation in microbial community composition and culturability in the rhizosphere of Leucanthemopsis alpina (L.) Heywood and adjacent bare soil along an alpine chronosequence. Microb Ecol 52:679–692.  https://doi.org/10.1007/s00248-006-9097-x CrossRefPubMedGoogle Scholar
  28. Engelkes T, Morriën E, Verhoeven KJF, Bezemer TM, Biere A, Harvey JA, McIntyre LM, Tamis WLM, van der Putten WH (2008) Successful range-expanding plants experience less above-ground and below-ground enemy impact. Nature 456:946–948.  https://doi.org/10.1038/nature07474 CrossRefPubMedGoogle Scholar
  29. Enríquez AS, Duarte CM, Url S (1993) Patterns in decomposition rates among photosynthetic organisms: the importance of detritus C:N:P content. Ecology 94:457–471Google Scholar
  30. Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017.  https://doi.org/10.1038/ismej.2011.159 CrossRefPubMedGoogle Scholar
  31. Fisk MC, Schmidt SK, Seastedt TR (1998) Topographic patterns of above- and belowground production and nitrogen cycling in alpine tundra. Ecology 79:2253–2266.  https://doi.org/10.1890/0012-9658(1998)079[2253:TPOAAB]2.0.CO;2 CrossRefGoogle Scholar
  32. Fox J, Weisberg S (2011) An {R} companion to applied regression, Second EditionGoogle Scholar
  33. Freeman KR, Martin AP, Karki D, Lynch RC, Mitter MS, Meyer AF, Longcore JE, Simmons DR, Schmidt SK (2009a) Evidence that chytrids dominate fungal communities in high-elevation soils. Proc Natl Acad Sci U S A 106:18315–18320CrossRefGoogle Scholar
  34. Freeman KR, Pescador MY, Reed SC, Costello EK, Robeson MS, Schmidt SK (2009b) Soil CO2 flux and photoautotrophic community composition in high-elevation, “barren” soil. Environ Microbiol 11:674–686.  https://doi.org/10.1111/j.1462-2920.2008.01844.x CrossRefPubMedGoogle Scholar
  35. Grayston SJ, Wang S, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378.  https://doi.org/10.1016/S0038-0717(97)00124-7 CrossRefGoogle Scholar
  36. Hervé M (2019) RVAideMemoire: testing and plotting procedures for biostatistics. R package version 0.9–71Google Scholar
  37. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363.  https://doi.org/10.1002/bimj.200810425 CrossRefGoogle Scholar
  38. Inderjit, Wardle DA, Karban R, Callaway RM (2011) The ecosystem and evolutionary contexts of allelopathy. Trends Ecol Evol 26:655–662.  https://doi.org/10.1016/j.tree.2011.08.003 CrossRefPubMedGoogle Scholar
  39. Janos DP (1980) Mycorrhizae influence tropical succession. Biotropica 12:56–64CrossRefGoogle Scholar
  40. Kardol P, Martijn Bezemer T, van der Putten WH (2006) Temporal variation in plant-soil feedback controls succession. Ecol Lett 9:1080–1088.  https://doi.org/10.1111/j.1461-0248.2006.00953.x CrossRefPubMedGoogle Scholar
  41. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  42. King AJ, Meyer AF, Schmidt SK (2008) High levels of microbial biomass and activity in unvegetated tropical and temperate alpine soils. Soil Biol Biochem 40:2605–2610.  https://doi.org/10.1016/j.soilbio.2008.06.026 CrossRefGoogle Scholar
  43. Kittel TGF, Williams MW, Chowanski K, Hartman M, Ackerman T, Losleben M, Blanken PD (2015) Contrasting long-term alpine and subalpine precipitation trends in a mid-latitude north American mountain system, Colorado front range, USA. Plant Ecol Divers 8:607–624.  https://doi.org/10.1080/17550874.2016.1143536 CrossRefGoogle Scholar
  44. Knelman JE, Legg TM, O’Neill SP, Washenberger CL, González A, Cleveland CC, Nemergut DR (2012) Bacterial community structure and function change in association with colonizer plants during early primary succession in a glacier forefield. Soil Biol Biochem 46:172–180.  https://doi.org/10.1016/j.soilbio.2011.12.001 CrossRefGoogle Scholar
  45. Knelman JE, Schmidt SK, Lynch RC, Darcy JL, Castle SC, Cleveland CC, Nemergut DR (2014) Nutrient addition dramatically accelerates microbial community succession. PLoS One 9:e102609.  https://doi.org/10.1371/journal.pone.0102609 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Knelman JE, Graham EB, Prevéy JS, Robeson MS, Kelly P, Hood E, Schmidt SK (2018) Interspecific plant interactions reflected in soil bacterial community structure and nitrogen cycling in primary succession. Front Microbiol 9:2611–2642.  https://doi.org/10.3389/fmicb.2018.00128 CrossRefGoogle Scholar
  47. Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–488.  https://doi.org/10.1016/S0953-7562(89)80195-9 CrossRefGoogle Scholar
  48. Kowalchuk GA, Buma DS, De Boer W et al (2002) Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Antonie van Leeuwenhoek, Int J Gen Mol Microbiol 81:509–520.  https://doi.org/10.1023/A:1020565523615 CrossRefGoogle Scholar
  49. Lau JA, Puliafico KP, Kopshever JA, Steltzer H, Jarvis EP, Schwarzländer M, Strauss SY, Hufbauer RA (2008) Inference of allelopathy is complicated by effects of activated carbon on plant growth. New Phytol 178:412–423.  https://doi.org/10.1111/j.1469-8137.2007.02360.x CrossRefGoogle Scholar
  50. Leff JW, Bardgett RD, Wilkinson A, Jackson BG, Pritchard WJ, de Long JR, Oakley S, Mason KE, Ostle NJ, Johnson D, Baggs EM, Fierer N (2018) Predicting the structure of soil communities from plant community taxonomy, phylogeny, and traits. ISME J 12:1794–1805.  https://doi.org/10.1038/s41396-018-0089-x CrossRefPubMedPubMedCentralGoogle Scholar
  51. Losleben M (2017) Air temperature data for D1 chart recorder from 1952/10/1 - ongoing, daily. http://niwot.colorado.edu/index.php/data/data/air-temperature-data-for-d1-chart-recorder-1952-ongoing. Accessed 18 Mar 2019
  52. McGonigle TP, Miller MH, Evans DG et al (1990) A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytol 115:495–501.  https://doi.org/10.1111/j.1469-8137.1990.tb00476.x CrossRefGoogle Scholar
  53. McGuire CR, Nufio CR, Bowers MD, Guralnick RP (2012) Elevation-dependent temperature trends in the Rocky Mountain front range: changes over a 56- and 20-year record. PLoS One 7:e44370.  https://doi.org/10.1371/journal.pone.0044370 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Miller RM (1979) Some occurrences of vesicular–arbuscular mycorrhiza in natural and disturbed ecosystems of the Red Desert. Can J Bot 57:619–623.  https://doi.org/10.1139/b79-079 CrossRefGoogle Scholar
  55. Miniaci C, Bunge M, Duc L, Edwards I, Bürgmann H, Zeyer J (2007) Effects of pioneering plants on microbial structures and functions in a glacier forefield. Biol Fertil Soils 44:289–297.  https://doi.org/10.1007/s00374-007-0203-0 CrossRefGoogle Scholar
  56. Mitchell CE, Power AO (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627.  https://doi.org/10.1038/nature01317 CrossRefPubMedGoogle Scholar
  57. Mladenov N, Williams MW, Schmidt SK, Cawley K (2012) Atmospheric deposition as a source of carbon and nutrients to an alpine catchment of the Colorado Rocky Mountains. Biogeosciences 9:3337–3355.  https://doi.org/10.5194/bg-9-3337-2012 CrossRefGoogle Scholar
  58. Morriën E, van der Putten WH (2013) Soil microbial community structure of range-expanding plant species differs from co-occurring natives. J Ecol 101:1093–1102.  https://doi.org/10.1111/1365-2745.12117 CrossRefGoogle Scholar
  59. Nemergut DR, Anderson SP, Cleveland CC, Martin AP, Miller AE, Seimon A, Schmidt SK (2007) Microbial community succession in an unvegetated, recently deglaciated soil. Microb Ecol 53:110–122.  https://doi.org/10.1007/s00248-006-9144-7 CrossRefPubMedGoogle Scholar
  60. Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248.  https://doi.org/10.1016/j.funeco.2015.06.006 CrossRefGoogle Scholar
  61. Ohtonen R, Fritze H, Pennanen T, Jumpponen A, Trappe J (1999) Ecosystem properties and microbial community changes in primary succession on a glacier forefront. Oecologia 119:239–246.  https://doi.org/10.1007/s004420050782 CrossRefPubMedGoogle Scholar
  62. Oksanen J, Blanchet FG, Kindt R, et al (2013) Package ‘vegan.’ R Packag ver 20–8 254.  https://doi.org/10.4135/9781412971874.n145
  63. Padhy B, Patnaik PK, Tripathy AK (2000) Allelopathic potential of Eucalyptus leaf litter leachates on germination and seedling growth of fingermillet. Allelopath J 7:69–78Google Scholar
  64. Petrýdesová J, Kučera J, Bacigálová K, Vadkertiová R, Lopandic K, Vďačný P, Slovák M (2016) Disentangling identity of species of the genus taphrina parasitizing herbaceous rosaceae, with proposal of taphrina gei-montani sp. Nov. Int J Syst Evol Microbiol 66:2540–2549.  https://doi.org/10.1099/ijsem.0.001095 CrossRefPubMedGoogle Scholar
  65. Pinheiro J, Bates D, DebRoy S, Sarkar D (2014) Package “nlme.” In: R vignetteGoogle Scholar
  66. Pohlert T (2014) The pairwise multiple comparison of mean ranks package (PMCMR). R package. 27. http://cran.ms.unimelb.edu.au/web/packages/PMCMR/vignettes/PMCMR.pdf
  67. Porazinska DL, Farrer EC, Spasojevic MJ, Bueno de Mesquita CP, Sartwell SA, Smith JG, White CT, King AJ, Suding KN, Schmidt SK (2018) Plant diversity and density predict belowground diversity and function in an early successional alpine ecosystem. Ecology 99:1942–1952.  https://doi.org/10.1002/ecy.2420 CrossRefPubMedGoogle Scholar
  68. Preston DL, Caine N, Mcknight DM et al (2016) Climate regulates alpine lake ice cover phenology and aquatic ecosystem structure. Geophys Res Lett 43:5353–5360.  https://doi.org/10.1002/2016GL069036 CrossRefGoogle Scholar
  69. R Core Team (2018) R: A Language and Environment for Statistical Computing. R Found. Stat. Comput. {ISBN} 3–900051–07-0Google Scholar
  70. Reynolds HL, Packer A, Bever JD, Clay K (2003) Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291CrossRefGoogle Scholar
  71. Sattin SR, Cleveland CC, Hood E, Reed SC, King AJ, Schmidt SK, Robeson MS, Ascarrunz N, Nemergut DR (2010) Functional shifts in unvegetated, perhumid, recently-deglaciated soils do not correlate with shifts in soil bacterial community composition. J Microbiol 47:673–681.  https://doi.org/10.1007/s12275-009-0194-7 CrossRefGoogle Scholar
  72. Schiltz S, Gaillard I, Pawlicki-Jullian N, Thiombiano B, Mesnard F, Gontier E (2015) A review: what is the spermosphere and how can it be studied? J Appl Microbiol 119:1467–1481.  https://doi.org/10.1111/jam.12946 CrossRefPubMedGoogle Scholar
  73. Schmidt SK, Reed SC, Nemergut DR, Stuart Grandy A, Cleveland CC, Weintraub MN, Hill AW, Costello EK, Meyer AF, Neff JC, Martin AM (2008a) The earliest stages of ecosystem succession in high-elevation (5000 metres above sea level), recently deglaciated soils. Proc R Soc B 275:2793–2802.  https://doi.org/10.1098/rspb.2008.0808 CrossRefPubMedGoogle Scholar
  74. Schmidt SK, Sobieniak-Wiseman LC, Kageyama SA, Halloy SRP, Schadt CW (2008b) Mycorrhizal and dark-septate Fungi in plant roots above 4270 meters elevation in the Andes and Rocky Mountains. Arct Antarct Alp Res 40:576–583.  https://doi.org/10.1657/1523-0430(07-068) CrossRefGoogle Scholar
  75. Schmidt SK, Porazinska D, Concienne BL, Darcy JL, King AJ, Nemergut DR (2016) Biogeochemical stoichiometry reveals P and N limitation across the post-glacial landscape of Denali National Park, Alaska. Ecosystems 19:1164–1177.  https://doi.org/10.1007/s10021-016-9992-z CrossRefGoogle Scholar
  76. Suding KN, Ashton IW, Bechtold H, Bowman WD, Mobley ML, Winkleman R (2008) Plant and microbe contribution to community resilience in a directionally changing environment. Ecol Monogr 78:313–329.  https://doi.org/10.1890/07-1092.1 CrossRefGoogle Scholar
  77. Sweetingham MW, Cruickshank RH, Wong DH (2009) Pectic zymograms and taxonomy and pathogenicity of the Ceratobasidiaceae. Trans Br Mycol Soc 86:305–311.  https://doi.org/10.1016/s0007-1536(86)80161-9 CrossRefGoogle Scholar
  78. Titus JH, Del Moral R (1998) Seedling establishment in different microsites on Mount St. Helens, Washington, USA. Plant Ecol 134:13–26.  https://doi.org/10.1023/A:1009765502741 CrossRefGoogle Scholar
  79. Tscherko D, Hammesfahr U, Zeltner G, Kandeler E, Böcker R (2005) Plant succession and rhizosphere microbial communities in a recently deglaciated alpine terrain. Basic Appl Ecol 6:367–383.  https://doi.org/10.1016/j.baae.2005.02.004 CrossRefGoogle Scholar
  80. van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310.  https://doi.org/10.1111/j.1461-0248.2007.01139.x CrossRefPubMedGoogle Scholar
  81. van der Putten WH (2012) Climate change, aboveground-belowground interactions, and species’ range shifts. Annu Rev Ecol Evol Syst 43:365–383.  https://doi.org/10.1146/annurev-ecolsys-110411-160423 CrossRefGoogle Scholar
  82. van der Putten WH, Troelstra SR (1990) Harmful soil organisms in coastal foredunes involved in degeneration of Ammophila arenaria and Calammophila baltica. Can J Bot 68:1560–1568.  https://doi.org/10.1139/b90-200 CrossRefGoogle Scholar
  83. van der Putten WH, van Dijk C, Troelstra SR (1988) Biotic soil factors affecting the growth and development of Ammophila arenaria. Oecologia 76:313–320.  https://doi.org/10.1007/BF00379970 CrossRefPubMedGoogle Scholar
  84. van der Putten WH, Maas PWT, Van Gulik WJM, Brinkman H (1990) Characterization of soil organisms involved in the degeneration of Ammophila arenaria. Soil Biol Biochem 22:845–852.  https://doi.org/10.1016/0038-0717(90)90166-W CrossRefGoogle Scholar
  85. van der Putten WH, Van Dijk C, Peters BAM (1993) Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 362:53–56.  https://doi.org/10.1038/362053a0 CrossRefGoogle Scholar
  86. 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 Lond Ser B Biol Sci 365:2025–2034.  https://doi.org/10.1098/rstb.2010.0037 CrossRefGoogle Scholar
  87. van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, van de Voorde TFJ, Wardle DA (2013) Plant-soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276.  https://doi.org/10.1111/1365-2745.12054 CrossRefGoogle Scholar
  88. van der Putten WH, Bradford MA, Pernilla Brinkman E, van de Voorde TFJ, Veen GF (2016) Where, when and how plant-soil feedback matters in a changing world. Funct Ecol 30:1109–1121.  https://doi.org/10.1111/1365-2435.12657 CrossRefGoogle Scholar
  89. 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 95:1050–1057.  https://doi.org/10.1111/j.1365-2745.2007.01282.x CrossRefGoogle Scholar
  90. Vivanco JM, Bais HP, Stermitz FR, Thelen GC, Callaway RM (2004) Biogeographical variation in community response to root allelochemistry: novel weapons and exotic invasion. Ecol Lett 7:285–292.  https://doi.org/10.1111/j.1461-0248.2004.00576.x CrossRefGoogle Scholar
  91. Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840.  https://doi.org/10.1038/nrmicro2910 CrossRefPubMedGoogle Scholar
  92. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T (eds) PCR Protocols. Academic Press, New York, pp 315–322Google Scholar
  93. Yang Q, Carrillo J, Jin H, Shang L, Hovick SM, Nijjer S, Gabler CA, Li B, Siemann E (2013) Plant–soil biota interactions of an invasive species in its native and introduced ranges: implications for invasion success. Soil Biol Biochem 65:78–85.  https://doi.org/10.1016/j.soilbio.2013.05.004 CrossRefGoogle Scholar
  94. Yang J-W, Yeh Y-H, Kirschner R (2016) A new endophytic species of Neostagonospora (Pleosporales) from the coastal grass Spinifex littoreus in Taiwan. Botany 94:593–598.  https://doi.org/10.1139/cjb-2015-0246 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA
  2. 2.Institute of Arctic and Alpine ResearchUniversity of ColoradoBoulderUSA

Personalised recommendations

Cite article

Buy options