, Volume 191, Issue 3, pp 493–504 | Cite as

Soil microbes that may accompany climate warming increase alpine plant production

  • Joshua S. LynnEmail author
  • Danielle A. Duarte
  • Jennifer A. Rudgers
Highlighted Student Research


Climate change is causing species with non-overlapping ranges to come in contact, and a key challenge is to predict the consequences of such species re-shuffling. Experiments on plants have focused largely on novel competitive interactions; other species interactions, such as plant–microbe symbioses, while less studied, may also influence plant responses to climate change. In this greenhouse study, we evaluated interactions between soil microbes and alpine-restricted plant species, simulating a warming scenario in which low-elevation microbes migrate upslope into the distribution of alpine plants. We examined three alpine grasses from the Rocky Mountains, CO, USA (Poa alpina, Festuca brachyphylla, and Elymus scribneri). We used soil inocula from within (resident) or below (novel) the plants’ current elevation range and examined responses in plant biomass, plant traits, and fungal colonization of roots. Resident soil inocula from the species’ home range decreased biomass to a greater extent than novel soil inocula. The depressed growth in resident soils suggested that these soils harbor more carbon-demanding microbes, as plant biomass generally declined with greater fungal colonization of roots, especially in resident soil inocula. Although plant traits did not respond to the provenance of soil inocula, specific leaf area declined and root:shoot ratio increased when soil inocula were sterilized, indicating microbial mediation of plant trait expression. Contrary to current predictions, our findings suggest that if upwardly migrating microbes were to displace current soil microbes, alpine plants may benefit from this warming-induced microbial re-shuffling.


Bacteria Fungi Plant microbiome Plant traits Rhizosphere 



We thank the Rudgers-Whitney lab for comments on early analyses for the project and two anonymous reviewers for their helpful comments. Thanks to M. Mann, T. Farkas, and W. Noe for giving up much of a weekend to harvest the experiment. The project was funded by the University of New Mexico Biology Department Grove Summer Scholarship, American Philosophical Society Lewis and Clark Fund, and the United States National Science Foundation Division of Environmental Biology 1701221 awarded to JSL. Additional funding was provided by the United States National Science Foundation Division of Environmental Biology 1354972 to JAR. The experiments comply with USA law. Data associated with this manuscript was deposited in with the following DOI address:

Author contribution statement

JSL and JAR conceived of the study, JSL and DAD collected the data, JSL analyzed the data, and JSL led the writing with contributions from all authors.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

442_2019_4518_MOESM1_ESM.docx (93 kb)
Supplementary material 1 (DOCX 72 kb)


  1. Alexander JM, Diez JM, Levine JM (2015) Novel competitors shape species’ responses to climate change. Nature 525:515–518. CrossRefPubMedGoogle Scholar
  2. Alexander JM, Diez JM, Hart SP, Levine JM (2016) When climate reshuffles competitors: a call for experimental macroecology. Trends Ecol Evol 31:831–841. CrossRefPubMedPubMedCentralGoogle Scholar
  3. Allsup C, Lankau R (2019) Migration of soil microbes may promote tree seedling tolerance to drying conditions. Ecology 100:e02729. CrossRefPubMedGoogle Scholar
  4. Anderson DR (2008) Model based inference in the life sciences: a primer on evidence. Springer, New York, LondonCrossRefGoogle Scholar
  5. Antunes PM, Koch AM, Morton JB et al (2011) Evidence for functional divergence in arbuscular mycorrhizal fungi from contrasting climatic origins. New Phytol 189:507–514. CrossRefPubMedGoogle Scholar
  6. Bartoń K (2018) MuMIn: multi-model inference. Accessed 15 May 2019
  7. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. CrossRefGoogle Scholar
  8. Beckstead J, Parker IM (2003) Invasiveness of Ammophila arenaria: release from soil-borne pathogens? Ecology 84:2824–2831. CrossRefGoogle Scholar
  9. Bilton MC, Whitlock R, Grime JP et al (2010) Intraspecific trait variation in grassland plant species reveals fine-scale strategy trade-offs and size differentiation that underpins performance in ecological communities. Botany 88:939–952. CrossRefGoogle Scholar
  10. Chung YA, Rudgers JA (2016) Plant–soil feedbacks promote negative frequency dependence in the coexistence of two aridland grasses. Proc R Soc B Biol Sci 283:20160608. CrossRefGoogle Scholar
  11. 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:art130. CrossRefGoogle Scholar
  12. Compant S, Van Der Heijden MGA, Sessitsch A (2010) Climate change effects on beneficial plant-microorganism interactions: climate change and beneficial plant-microorganism interactions. FEMS Microbiol Ecol 73:197–214. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Conti G, Díaz S (2013) Plant functional diversity and carbon storage—an empirical test in semi-arid forest ecosystems. J Ecol 101:18–28. CrossRefGoogle Scholar
  14. Crawford KM, Bauer JT, Comita LS et al (2019) When and where plant-soil feedback may promote plant coexistence: a meta-analysis. Ecol Lett 22:1274–1284. CrossRefPubMedGoogle Scholar
  15. Dobzhansky T (1950) Evolution in the tropics. Am Sci 38:208–221Google Scholar
  16. Fierer N, McCain CM, Meir P et al (2011) Microbes do not follow the elevational diversity patterns of plants and animals. Ecology 92:797–804. CrossRefPubMedGoogle Scholar
  17. Fridley JD, Lynn JS, Grime JP, Askew AP (2016) Longer growing seasons shift grassland vegetation towards more-productive species. Nat Clim Change 6:865–868. CrossRefGoogle Scholar
  18. Friesen ML, Porter SS, Stark SC et al (2011) Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 42:23–46. CrossRefGoogle Scholar
  19. Givnish TJ (1999) On the causes of gradients in tropical tree diversity. J Ecol 87:193–210. CrossRefGoogle Scholar
  20. 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 101:47–57. CrossRefGoogle Scholar
  21. Hendershot JN, Read QD, Henning JA et al (2017) Consistently inconsistent drivers of microbial diversity and abundance at macroecological scales. Ecology 98:1757–1763. CrossRefPubMedGoogle Scholar
  22. Henning JA, Weston DJ, Pelletier DA et al (2016) Root bacterial endophytes alter plant phenotype, but not physiology. PeerJ 4:e2606. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kivlin SN, Emery SM, Rudgers JA (2013) Fungal symbionts alter plant responses to global change. Am J Bot 100:1445–1457. CrossRefPubMedGoogle Scholar
  24. Kivlin SN, Lynn JS, Kazenel MR et al (2017a) Biogeography of plant-associated fungal symbionts in mountain ecosystems: a meta-analysis. Divers Distrib 23:1067–1077. CrossRefGoogle Scholar
  25. Kivlin SN, Muscarella R, Hawkes CV, Treseder KK (2017b) The predictive power of ecological niche modeling for global arbuscular mycorrhizal fungal biogeography. In: Tedersoo L (ed) Biogeography of mycorrhizal symbiosis. Springer International Publishing, Cham, pp 143–158CrossRefGoogle Scholar
  26. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70. CrossRefPubMedGoogle Scholar
  27. Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301. CrossRefGoogle Scholar
  28. Körner C (2007) The use of ‘altitude’ in ecological research. Trends Ecol Evol 22:569–574. CrossRefPubMedGoogle Scholar
  29. Kraft NJB, Crutsinger GM, Forrestel EJ, Emery NC (2014) Functional trait differences and the outcome of community assembly: an experimental test with vernal pool annual plants. Oikos 123:1391–1399. CrossRefGoogle Scholar
  30. Ladau J, Shi Y, Jing X et al (2018) Existing climate change will lead to pronounced shifts in the diversity of soil prokaryotes. mSystems 3:e00167-18. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Lau JA, Lennon JT (2011) Evolutionary ecology of plant–microbe interactions: soil microbial structure alters selection on plant traits. New Phytol 192:215–224. CrossRefPubMedGoogle Scholar
  32. Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc Natl Acad Sci 109:14058–14062. CrossRefPubMedGoogle Scholar
  33. Lenoir J, Gégout J-C, Marquet P et al (2008) A significant upward shift in plant species optimum elevation during the 20th century. Science 320:1768–1771. CrossRefPubMedGoogle Scholar
  34. Lynn JS, Kazenel MR, Kivlin SN, Rudgers JA (2019) Context-dependent biotic interactions predict plant abundance across altitudinal environmental gradients. Ecography 42:1600–1612. CrossRefGoogle Scholar
  35. Mangan SA, Schnitzer SA, Herre EA et al (2010) Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–755. CrossRefPubMedGoogle Scholar
  36. 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. CrossRefGoogle Scholar
  37. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Miller RM, Miller SP, Jastrow JD, Rivetta CB (2002) Mycorrhizal mediated feedbacks influence net carbon gain and nutrient uptake in Andropogon gerardii. New Phytol 155:149–162. CrossRefGoogle Scholar
  39. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142CrossRefGoogle Scholar
  40. Olsson PA, Rahm J, Aliasgharzad N (2010) Carbon dynamics in mycorrhizal symbioses is linked to carbon costs and phosphorus benefits. FEMS Microbiol Ecol 72:125–131. CrossRefPubMedGoogle Scholar
  41. Pepin N, Losleben M (2002) Climate change in the Colorado Rocky Mountains: free air versus surface temperature trends. Int J Climatol 22:311–329. CrossRefGoogle Scholar
  42. Perez-Harguindeguy N, Diaz S, Garnier E et al (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 61:167–234. CrossRefGoogle Scholar
  43. Perrine-Walker FM, Gartner E, Hocart CH et al (2007) Rhizobium -initiated rice growth inhibition caused by nitric oxide accumulation. Mol Plant Microbe Interact 20:283–292. CrossRefPubMedGoogle Scholar
  44. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  45. Ranelli LB, Hendricks WQ, Lynn JS et al (2015) Biotic and abiotic predictors of fungal colonization in grasses of the Colorado Rockies. Divers Distrib 21:962–976. CrossRefGoogle Scholar
  46. Rangwala I, Miller JR (2012) Climate change in mountains: a review of elevation-dependent warming and its possible causes. Clim Change 114:527–547. CrossRefGoogle Scholar
  47. Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170:445–457. CrossRefPubMedGoogle Scholar
  48. Reinhart KO, Rinella MJ (2016) A common soil handling technique can generate incorrect estimates of soil biota effects on plants. New Phytol 210:786–789. CrossRefPubMedGoogle Scholar
  49. Revillini D, Gehring CA, Johnson NC (2016) The role of locally adapted mycorrhizas and rhizobacteria in plant–soil feedback systems. Funct Ecol 30:1086–1098. CrossRefGoogle Scholar
  50. Reynolds HL, Packer A, Bever JD, Clay K (2003) Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291. CrossRefGoogle Scholar
  51. Rinella MJ, Reinhart KO (2017) Mixing soil samples across experimental units ignores uncertainty and generates incorrect estimates of soil biota effects on plants: response to Cahill et al. (2017) ‘No silver bullet: different soil handling techniques are useful for different research questions, exhibit differential type I and II error rates, and are sensitive to sampling intensity’. New Phytol 216:15–17. CrossRefPubMedGoogle Scholar
  52. Rinella MJ, Reinhart KO (2018) Toward more robust plant-soil feedback research. Ecology 99:550–556. CrossRefPubMedGoogle Scholar
  53. Rudgers JA, Miller TEX, Ziegler SM, Craven KD (2012) There are many ways to be a mutualist: endophytic fungus reduces plant survival but increases population growth. Ecology 93:565–574. CrossRefPubMedGoogle Scholar
  54. Rudgers JA, Kivlin SN, Whitney KD et al (2014) Responses of high-altitude graminoids and soil fungi to 20 years of experimental warming. Ecology 95:1918–1928. CrossRefPubMedGoogle Scholar
  55. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to imagej: 25 years of image analysis. Nat Methods 9:671–675. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Sheik CS, Beasley WH, Elshahed MS et al (2011) Effect of warming and drought on grassland microbial communities. ISME J 5:1692–1700. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Siles JA, Margesin R (2016) Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: what are the driving factors? Microb Ecol 72:207–220CrossRefGoogle Scholar
  58. Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic press, CambridgeGoogle Scholar
  59. Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses: research review. New Phytol 182:347–358. CrossRefPubMedGoogle Scholar
  60. terHorst CP, Zee PC (2016) Eco-evolutionary dynamics in plant-soil feedbacks. Funct Ecol 30:1062–1072. CrossRefGoogle Scholar
  61. Thomas CD, Cameron A, Green RE et al (2004) Extinction risk from climate change. Nature 427:145–148. CrossRefPubMedGoogle Scholar
  62. Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363. CrossRefPubMedGoogle Scholar
  63. Van der Putten WH (2012) Climate change, aboveground-belowground interactions, and species’ range shifts. Annu Rev Ecol Evol Syst 43:365–383. CrossRefGoogle Scholar
  64. Van der Putten WH, Bradford MA, Pernilla Brinkman E et al (2016) Where, when and how plant-soil feedback matters in a changing world. Funct Ecol 30:1109–1121. CrossRefGoogle Scholar
  65. Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007PubMedPubMedCentralGoogle Scholar
  66. Walther G-R, Post E, Convey P et al (2002) Ecological responses to recent climate change. Nature 416:389. CrossRefPubMedGoogle Scholar
  67. Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10. CrossRefPubMedPubMedCentralGoogle Scholar
  68. Westoby M (1998) A leaf-height-seed (LHS) plant ecology strategy scheme. Plant Soil 199:213–227. CrossRefGoogle Scholar
  69. Wolfe BE, Parrent JL, Koch AM et al (2009) Spatial heterogeneity in mycorrhizal populations and communities: scales and mechanisms. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas—functional processes and ecological impact. Springer, Berlin, Heidelberg, pp 167–185CrossRefGoogle Scholar
  70. Wright DP, Scholes JD, Read DJ (1998) Effects of VA mycorrhizal colonization on photosynthesis and biomass production of Trifolium repens L. Plant Cell Environ 21:209–216. CrossRefGoogle Scholar
  71. Yang J, Kloepper JW, Ryu C-M (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4. CrossRefPubMedGoogle Scholar
  72. Zhou Z, Wang C, Luo Y (2018) Response of soil microbial communities to altered precipitation: a global synthesis. Glob Ecol Biogeogr 27:1121–1136. CrossRefGoogle Scholar
  73. Zorio SD, Williams CF, Aho KA (2016) Sixty-five years of change in montane plant communities in Western Colorado, USA. Arct Antarct Alp Res 48:703–722. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of BiologyUniversity of New MexicoAlbuquerqueUSA
  2. 2.The Rocky Mountain Biological LaboratoryGothicUSA
  3. 3.Department of Biological ScienceUniversity of BergenBergenNorway

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