Microbial Ecology

, Volume 78, Issue 3, pp 688–698 | Cite as

Plant Identity Influences Foliar Fungal Symbionts More Than Elevation in the Colorado Rocky Mountains

  • Stephanie N. KivlinEmail author
  • Melanie R. Kazenel
  • Joshua S. Lynn
  • D. Lee Taylor
  • Jennifer A. Rudgers
Plant Microbe Interactions


Despite colonizing nearly every plant on Earth, foliar fungal symbionts have received little attention in studies on the biogeography of host-associated microbes. Evidence from regional scale studies suggests that foliar fungal symbiont distributions are influenced both by plant hosts and environmental variation in climate and soil resources. However, previous surveys have focused on either one plant host across an environmental gradient or one gradient and multiple plant hosts, making it difficult to disentangle the influence of host identity from the influence of the environment on foliar endophyte communities. We used a culture-based approach to survey fungal symbiont composition in the leaves of nine C3 grass species along replicated elevation gradients in grasslands of the Colorado Rocky Mountains. In these ecosystems, the taxonomic richness and composition of foliar fungal symbionts were mostly structured by the taxonomic identity of the plant host rather than by variation in climate. Plant traits related to size (height and leaf length) were the best predictors of foliar fungal symbiont composition and diversity, and composition did not vary predictably with plant evolutionary history. The largest plants had the most diverse and distinctive fungal communities. These results suggest that across the ~ 300 m elevation range that we sampled, foliar fungal symbionts may indirectly experience climate change by tracking the shifting distributions of plant hosts rather than tracking climate directly.


Climate C3 grass Epichloë Foliar endophytes Horizontally transmitted endophytic fungi Microbiome Mountain ecosystems Plant host 



We thank K. Anderson and B. McCormick for help maintaining the foliar endophyte culture collection and A. Chung and J. Bell for assistance with DNA extraction and sequencing.

Funding Information

This work was supported by National Science Foundation grant number DEB1354972 to Rudgers, Taylor and Kivlin and RMBL fellowships to Kivlin, Rudgers, and Lynn.

Supplementary material

248_2019_1336_MOESM1_ESM.docx (192 kb)
ESM 1 (DOCX 192 kb)


  1. 1.
    Higgins KL, Arnold AE, Coley PD, Kursar TA (2014) Communities of fungal endophytes in tropical forest grasses: highly diverse host- and habitat generalists characterized by strong spatial structure. Fungal Ecol 8:1–11CrossRefGoogle Scholar
  2. 2.
    Giauque H, Hawkes CV (2013) Climate affects symbiotic fungal endophyte diversity and performance. Am J Bot 100:1435–1444CrossRefGoogle Scholar
  3. 3.
    Malinowski DP, Belesky DB (2000) Adaptations of endophyte-infected cool season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940CrossRefGoogle Scholar
  4. 4.
    Elmi AA, West CP (1995) Endophyte infection effects on stomatal conductance, osmotic adjustment and drought recovery of tall fescue. New Phytol 131:61–67CrossRefGoogle Scholar
  5. 5.
    Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581CrossRefGoogle Scholar
  6. 6.
    Gange AC, Eschen R, Wearn JA, Thawer A, Sutton BC (2012) Differential effects of foliar endophytic fungi on insect herbivores attacking a herbaceous plant. Oecologia 168:1023–1031CrossRefGoogle Scholar
  7. 7.
    Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci U S A 100:15649–15654CrossRefGoogle Scholar
  8. 8.
    Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54:323–342CrossRefGoogle Scholar
  9. 9.
    Kivlin SN, Emery SM, Rudgers JA (2013) Fungal symbionts alter plant responses to global change. Am J Bot 100:1445–1457CrossRefGoogle Scholar
  10. 10.
    Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549CrossRefGoogle Scholar
  11. 11.
    Kivlin SN, Lynn JS, Kazenel MR, Beals KK, Rudgers JA (2017) Biogeography of plant-associated fungal symbionts in mountain ecosystems: a meta-analysis. Divers Distrib 23:1067–1077CrossRefGoogle Scholar
  12. 12.
    Zimmerman NB, Vitousek PM (2012) Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape. Proc Natl Acad Sci U S A 109:13022–13027CrossRefGoogle Scholar
  13. 13.
    Yang T, Weisenhorn P, Gilber JA, Ni Y, Sun R, Shi Y, Chu H (2017) Carbon constrains fungal endophyte assemblages along the timberline. Environ Microbiol 18:2455–2469CrossRefGoogle Scholar
  14. 14.
    Giauque H, Hawkes CV (2016) Historical and current climate drive spatial and temporal patterns in fungal endophyte diversity. Fungal Ecol 20:108–114CrossRefGoogle Scholar
  15. 15.
    Gazis R, Chaverri P (2010) Diversity of fungal endophytes in leaves and stems of wild rubber trees (Hevea brasiliensis) in Peru. Fungal Ecol 3:240–254CrossRefGoogle Scholar
  16. 16.
    Koide RT, Ricks KD, Davis ER (2017) Climate and dispersal influence the structure of leaf fungal endophyte communities of Quercus gambelii in the eastern Great Basin, USA. Fungal Ecol 30:19–28CrossRefGoogle Scholar
  17. 17.
    Christenhusz M, Byng JW (2016) The number of known plant species in the world and its annual increase. Phytotaxa 261:201–217CrossRefGoogle Scholar
  18. 18.
    Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavendar-Barres J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827CrossRefGoogle Scholar
  19. 19.
    Treseder KK, Kivlin SN, Hawkes CV (2011) Evolutionary trade-offs among decomposers determine responses to nitrogen enrichment. Ecol Lett 14:933–938CrossRefGoogle Scholar
  20. 20.
    Martiny AC, Treseder K, Pusch G (2013) Phylogenetic conservation of functional traits in microorganisms. ISME J 7:830–838CrossRefGoogle Scholar
  21. 21.
    Kembel SW, Mueller RC (2014) Plant traits and taxonomy drive host associations in tropical phyllosphere fungal communities. Botany 92:303–311CrossRefGoogle Scholar
  22. 22.
    Van Bael S, Estrada C, Arnold AE (2017) Chapter 6: foliar endophyte communities and leaf traits in tropical trees. In: Dighton J, White JF (eds) The fungal community: its organization and role in the ecosystem. CRC Press, Boca Raton, pp 79–94CrossRefGoogle Scholar
  23. 23.
    Valkama E, Koricheva J, Salminen J-P, Helander M, Saloniemi I, Saikkonen K, Pihlaja K (2005) Leaf surface traits: overlooked determinants of birch resistance to herbivores and foliar micro-fungi? Trees 19:191–197CrossRefGoogle Scholar
  24. 24.
    Giauque H, Connor EW, Hawkes CV (2018) Endophyte traits relevant to stress tolerance, resource use and habitat origin predict effects on host plants. New Phytol.
  25. 25.
    Higgins KL, Arnold AE, Miadlikowska J, Sarvate SD, Lutzoni F (2007) Phylogenetic relationships, host affinity, and geographic structure of boreal and arctic endophytes from three major plant lineages. Mol Phylogenet Evol 42:543–555CrossRefGoogle Scholar
  26. 26.
    Massimo NC, Devan MN, Arendt KR, Wilch MH, Riddle JM, Furr SH, Steen C, U’Ren JM, Sandberg DC, Arnold AE (2015) Fungal endophytes in aboveground tissues of desert plants: infrequent in culture, but highly diverse and distinctive symbionts. Microb Ecol 70:61–76CrossRefGoogle Scholar
  27. 27.
    Del Olmo-Ruiz M, Arnold AE (2014) Interannual variation and host affiliations of endophytic fungi associated with ferns at La Selva, Costa Rica. Mycologia 106:8–21CrossRefGoogle Scholar
  28. 28.
    Suryanarayanan TS, Wittlinger SK, Faeth SH (2005) Endophytic fungi associated with cacti in Arizona. Mycol Res 109:635–639CrossRefGoogle Scholar
  29. 29.
    Kittel TGF, Thornton PE, Royle JA, Chase TN (2002) Climates of the Rocky Mountains: historical and future patterns. In: Baron JS (ed) Rocky Mountain futures: an ecological perspective. Island Press, Covelo, pp 59–82Google Scholar
  30. 30.
    Dunne JA, Harte J, Taylor KJ (2003) Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol Monogr 73:69–86CrossRefGoogle Scholar
  31. 31.
    Pepin N, Losleben M (2002) Climate change in the Colorado Rocky Mountains: free air versus surface temperature trends. Int J Climatol 22(3):311–329CrossRefGoogle Scholar
  32. 32.
    Rangwala I, Miller JR (2012) Climate change in mountains a review of elevation-dependent warming and its possible causes. Clim Chang 114:527–547CrossRefGoogle Scholar
  33. 33.
    Lynn JS, Canfield S, Conover RR, Keene J, Rudgers JA (in press) Pocket gopher (Thomomys talpoides) soil disturbance peaks at mid elevation and is associated with air temperature, forb cover, and plant diversity. Arctic, Antarctic, and Alpine Research.Google Scholar
  34. 34.
    Shaw RB (2008) Grasses of Colorado. University Press of Colorado, BoulderGoogle Scholar
  35. 35.
    USDA NRCS (2018) The PLANTS Database (, 21 January 2018). National Plant Data Team, Greensboro, NC 27401–4901 USA
  36. 36.
    Paine CET, Norden N, Chave J, Forget P-M, Fortunel C, Dexter KG, Baraloto C (2012) Phylogenetic density dependence and environmental filtering predict seedling mortality in a tropical forest. Ecol Lett 15:34–41CrossRefGoogle Scholar
  37. 37.
    Vincent JB, Weiblen GD, May G (2016) Host associations and beta diversity of fungal endophyte communities in New Guinea rainforest trees. Mol Ecol 25:825–841CrossRefGoogle Scholar
  38. 38.
    Taylor DL, Booth MG, McFarland JW, Herriott IC, Lennon NJ, Nusbaum C, Marr TG (2008) Increasing ecological inference from high throughput sequencing of fungi in the environmental through a tagging approach. Mol Ecol Resour 8:742–752CrossRefGoogle Scholar
  39. 39.
    Caparaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Gonzalez Pena A, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevensky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefGoogle Scholar
  40. 40.
    Glassman SI, Martiny JBH (2018) Broadscale ecological patterns are robust to use of exact sequence variants versus operational taxonomic units. mSphere 3:e00148–e00118CrossRefGoogle Scholar
  41. 41.
    Corradi N, Croll D, Colard A, Kuhn G, Ehinger M, Sanders IR (2007) Gene copy number polymorphisms in an arbuscular mycorrhizal fungal population. Appl Environ Microbiol 73:366–369CrossRefGoogle Scholar
  42. 42.
    Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, Frei dit Frey N, Gianinazzi-Pearson V, Gilbert LB, Handa Y, Herr JR, Hijri M, Koul R, Kawaguchi M, Krajinski F, Lammers PJ, Masclaux FG, Murat C, Morin E, Nedikumana S, Pagni M, Petitpierre D, Requena N, Rosikiewicz P, Riley R, Saito K, San Clemente H, Shapiro H, van Tuinen D, Becard G, Bonfante P, Paszkowski U, Shachar-Hill YY, Tuskan GA, JPW Y, Sanders IR, Henrissat B, Rensing SA, Grigoriev IV, Corradi N, Roux C, Martin F (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci U S A 110:20117–20122CrossRefGoogle Scholar
  43. 43.
    Lindner DL, Banik MT (2011) Intragenomic variation in the ITS rDNA region obscures phylogenetic relationships and inflates estimates of operational taxonomic units in genus Laetiporus. Mycologia 103:731–740CrossRefGoogle Scholar
  44. 44.
    Thiery O, Vasar M, Jairus T, Davison J, Roux C, Kivistik PA, Metspalu A, Milani L, Saks U, Moora M, Zobel M (2016) Sequence variation in nuclear ribosomal small subunit, internal transcribed spacer and large subunit regions of Rhizophagus irregularis and Gigaspora margarita is high and isolate-dependent. Mol Ecol 25:2816–2832CrossRefGoogle Scholar
  45. 45.
    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefGoogle Scholar
  46. 46.
    Nhuyen 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 20:241–248CrossRefGoogle Scholar
  47. 47.
    Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Steves MHH, Szoecs E, Wagner H (2017) Vegan: community ecology package. R package version 2.4–5.
  48. 48.
    R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  49. 49.
    Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423CrossRefGoogle Scholar
  50. 50.
    Bates S, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  51. 51.
    Clarke KR, Gorley RN (2009) Primer version 6.1.10 user manual and tutorial. Primer-E, PlymouthGoogle Scholar
  52. 52.
    Anderson MJ, Walsh DCI (2013) PERMANOVA, ANOSIM, and the mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol Monogr 83:557–574CrossRefGoogle Scholar
  53. 53.
    Roberts DW (2007) Labdsv: ordination and multivariate analysis for ecology. R Package Version 1.8–0Google Scholar
  54. 54.
    Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14CrossRefGoogle Scholar
  55. 55.
    Ranelli LB, Hendricks WQ, Lynn JS, Kivlin SN, Rudgers JA (2015) Biotic and abiotic predictors of fungal colonization in grasses of the Colorado Rockies. Divers Distrib 21:962–976CrossRefGoogle Scholar
  56. 56.
    Classen AT, Sundqvist MK, Henning JA, Newman GS, Moore JAM, Cregger MA, Moorhead LC, Patterson CM (2015) Direct and indirect effects of climate change on soil microbial-plant interactions: what lies ahead? Ecosphere 6:1–21CrossRefGoogle Scholar
  57. 57.
    Langenheim JH (1962) Vegetation and environmental patterns in the Crested Butte area, Gunnison County, Colorado. Ecol Monogr 32:249–285CrossRefGoogle Scholar
  58. 58.
    Zorio SD, Williams CF, Aho KA (2016) Sixty-five years of change in montane plant communities in Western Colorado, USA. Arct Antarct Alp Res 48:703–722CrossRefGoogle Scholar
  59. 59.
    Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330CrossRefGoogle Scholar
  60. 60.
    Ravnskov S, Jensen B, Knudsen IMB, Bodker L, Jensen DF, Karlinski L, Larsen J (2006) Soil inoculation with the biocontrol agent Clonostachys rosea and the mycorrhizal fungus Glomus intraradices results in mutual inhibition, plant growth promotion and alteration of soil microbial communities. Soil Biol Biochem 38:3452–3462CrossRefGoogle Scholar
  61. 61.
    Buckley H, Young CA, Charlton ND, Hendricks WQ, Haley B, Nagabhyru P, Rudgers JA (in revision) Leaf endophytes mediate fertilizer effects on plant yield and traits in northern oat grass (Trisetum spicatum). Plant SoilGoogle Scholar
  62. 62.
    Mack KML, Rudgers JA (2008) Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos 117:310–320CrossRefGoogle Scholar
  63. 63.
    Bond BJ (2000) Age-related changes in photosynthesis of woody plants. Trends Plant Sci 8:349–353CrossRefGoogle Scholar
  64. 64.
    Kivlin SN, Winston GC, Goulden ML, Treseder KK (2014) Environmental filtering affects soil fungal community composition more than dispersal limitation at regional scales. Fungal Ecol 12:14–25CrossRefGoogle Scholar
  65. 65.
    Musick HB, Trujillo SM, Truman CR (1996) Wind-tunnel modeling of the influence of vegetation structure on saltation threshold. Earth Surf Process Landf 21:589–605CrossRefGoogle Scholar
  66. 66.
    Kazenel MR 2016. Altitudinal gradients do not predict plant-symbiont response to experimental warming.

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of BiologyUniversity of New MexicoAlbuquerqueUSA
  2. 2.Rocky Mountain Biological LaboratoryCrested ButteUSA
  3. 3.Department of Ecology and Evolutionary BiologyUniversity of TennesseeKnoxvilleUSA

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