Skip to main content

Pervasive Effects of Wildfire on Foliar Endophyte Communities in Montane Forest Trees

Abstract

Plants in all terrestrial ecosystems form symbioses with endophytic fungi that inhabit their healthy tissues. How these foliar endophytes respond to wildfires has not been studied previously, but is important given the increasing frequency and intensity of severe wildfires in many ecosystems, and because endophytes can influence plant growth and responses to stress. The goal of this study was to examine effects of severe wildfires on endophyte communities in forest trees, with a focus on traditionally fire-dominated, montane ecosystems in the southwestern USA. We evaluated the abundance, diversity, and composition of endophytes in foliage of Juniperus deppeana (Cupressaceae) and Quercus spp. (Fagaceae) collected contemporaneously from areas affected by recent wildfire and paired areas not affected by recent fire. Study sites spanned four mountain ranges in central and southern Arizona. Our results revealed significant effects of fires on endophyte communities, including decreases in isolation frequency, increases in diversity, and shifts in community structure and taxonomic composition among endophytes of trees affected by recent fires. Responses to fire were similar in endophytes of each host in these fire-dominated ecosystems and reflect regional fire-return intervals, with endophytes after fire representing subsets of the regional mycoflora. Together, these findings contribute to an emerging perspective on the responses of diverse communities to severe fire, and highlight the importance of considering fire history when estimating endophyte diversity and community structure for focal biomes.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

References

  1. 1.

    Boerner REJ (1982) Fire and nutrient cycling in temperate ecosystems. Bioscience 32(3):187–192

    Article  Google Scholar 

  2. 2.

    DeBano LF, Neary DG, Ffolliott PF (1998) Fire effects on ecosystems. Wiley, New York

    Google Scholar 

  3. 3.

    Falk DA, Heyerdahl EK, Brown PM, Farris C, Fulé PZ, McKenzie D, Swetnam TW, Taylor AH, Van Horne ML (2011) Multi-scale controls of historical forest-fire regimes: new insights from fire-scar networks. Front Ecol Environ 9(8):446–454

    Article  Google Scholar 

  4. 4.

    Overpeck J, Udall B (2010) Dry times ahead. Science 328(5986):1642–1643

    CAS  PubMed  Article  Google Scholar 

  5. 5.

    Swetnam TW, Baisan CH, Kaib J (2001) Forest fire histories of the sky islands of La Frontera: fire-scar reconstructions of fire regimes. In: Webster GL, Bahre CJ (eds) Vegetation and flora of La Frontera: historic vegetation change along the United States/Mexico boundary. University of New Mexico Press, Albuquerque, pp 95–119

    Google Scholar 

  6. 6.

    Westerling AL, Hidalgo HG, Cayan DR, Swetnam TW (2006) Warming and earlier spring increase western U.S. forest wildfire activity. Science 313(5789):940–943

    CAS  PubMed  Article  Google Scholar 

  7. 7.

    Swetnam TW, Baisan CH (1996) Fire histories of montane forests in the Madrean Borderlands. In: Ffolliott PF, DeBano LF, Baker MB, Gottfried GJ, Solis-Garza G, Edminster CB, Neary DG, Allen LS, Hamre RH (eds) Effects of fire on Madrean Province ecosystems. USDA For Serv Gen Tech Rep RM-GTR-289, Fort Collins, pp 15–36

  8. 8.

    Allen LS (1994) Fire management in the sky islands. In: DeBano LF (eds) Biodiversity and management of the Madrean Archipelago: the sky island of Southwestern United States and Northwestern Mexico. Diane, pp 386–388

  9. 9.

    Covington WW, Moore MM (1994) Southwestern ponderosa pine forest structure: changes since Euro-American settlement. J For 92:39–47

    Google Scholar 

  10. 10.

    Kelly AE, Goulden ML (2008) Rapid shifts in plant distribution with recent climate change. Proc Natl Acad Sci U S A 105(33):11823–11826

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  11. 11.

    MacDonald GM (2010) Climate change and water in southwestern North America special feature: water, climate change, and sustainability in the southwest. Proc Natl Acad Sci U S A 107(50):21256–21262

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  12. 12.

    Abella SR (2010) Disturbance and plant succession in the Mojave and Sonoran Deserts of the American southwest. Int J Environ Res Public Health 7(4):1248–1284

    PubMed Central  PubMed  Article  Google Scholar 

  13. 13.

    Ahlstrand GM (1982) Response of Chihuahuan Desert mountain shrub vegetation to burning. J Range Manag 35:62–65

    Article  Google Scholar 

  14. 14.

    Certini G (2005) Effects of fire on properties of forest soils: a review. Oecologia 143(1):1–10

    PubMed  Article  Google Scholar 

  15. 15.

    Cuevas-Gonzalez M, Gerard F, Balzter H, Riano D (2009) Analysing forest recovery after wildfire disturbance in boreal Siberia using remotely sensed vegetation indices. Glob Chang Biol 15(3):561–577

    Article  Google Scholar 

  16. 16.

    Vázquez FJ, Acea MJ, Carballas T (1993) Soil microbial populations after wildfire. FEMS Microbiol Ecol 13(2):93–103

    Article  Google Scholar 

  17. 17.

    Acea MJ, Carballas T (1996) Changes in physiological groups of microorganisms in soil following wildfire. FEMS Microbiol Ecol 20(1):33–39

    CAS  Article  Google Scholar 

  18. 18.

    Hebel CL, Smith JE, Cromack K Jr (2009) Invasive plant species and soil microbial response to wildfire burn severity in the Cascade Range of Oregon. Appl Soil Ecol 42(2):150–159

    Article  Google Scholar 

  19. 19.

    Xiang X, Shi Y, Yang J, Kong J, Lin X, Zhang H, Zeng J, Chu H (2014) Rapid recovery of soil bacterial communities after wildfire in a Chinese boreal forest. Sci Rep 4:3829

    PubMed Central  PubMed  Google Scholar 

  20. 20.

    Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21(2):51–66

    Article  Google Scholar 

  21. 21.

    Shah MA (2014) Mycorrhizas in extreme environments. In: Shah MA (ed) Mycorrhizas: novel dimensions in the changing world. Springer, New Delhi, pp 53–61

    Chapter  Google Scholar 

  22. 22.

    Singh LP, Gill SS, Tuteja N (2011) Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6(2):175–191

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  23. 23.

    Bellgard SE, Whelan RJ, Muston RM (1994) The impact of wildfire on vesicular-arbuscular mycorrhizal fungi and their potential to influence the reestablishment of postfire plant-communities. Mycorrhiza 4(4):139–146

    Article  Google Scholar 

  24. 24.

    Baynes M, Newcombe G, Dixon L, Castlebury L, O’Donnell K (2012) A novel plant-fungal mutualism associated with fire. Fungal Biol 116(1):133–144

    PubMed  Article  Google Scholar 

  25. 25.

    Baar J, Horton TR, Kretzer A, Bruns TD (1999) Mycorrhizal colonization of Pinus muricata from resistant propagules after a stand‐replacing wildfire. New Phytol 143(2):409–418

    Article  Google Scholar 

  26. 26.

    Trusty PE (2009) Impact of severe fire on ectomycorrhizal fungi of whitebark pine seedlings. Dissertation, Montana State University

  27. 27.

    Peay KG, Garbelotto M, Bruns TD (2009) Spore heat resistance plays an important role in disturbance‐mediated assemblage shift of ectomycorrhizal fungi colonizing Pinus muricata seedlings. J Ecol 97(3):537–547

    Article  Google Scholar 

  28. 28.

    Buscardo E, Rodriguez-Echeverria S, Martin MP, De Angelis P, Pereira JS, Freitas H (2010) Impact of wildfire return interval on the ectomycorrhizal resistant propagules communities of a Mediterranean open forest. Fungal Biol 114(8):628–636

    PubMed  Article  Google Scholar 

  29. 29.

    Bent E, Kiekel P, Brenton R, Taylor DL (2011) Root-associated ectomycorrhizal fungi shared by various boreal forest seedlings naturally regenerating after a fire in interior Alaska and correlation of different fungi with host growth responses. Appl Environ Microb 77(10):3351–3359

    CAS  Article  Google Scholar 

  30. 30.

    Dahlberg A, Schimmel J, Taylor AF, Johannesson H (2001) Post-fire legacy of ectomycorrhizal fungal communities in the Swedish boreal forest in relation to fire severity and logging intensity. Biol Conserv 100(2):151–161

    Article  Google Scholar 

  31. 31.

    Egerton-Warburton L, Podbielski J, Sickel J, Hendrix PF, Sternberg P, Graham R (2005) Mycorrhizal community dynamics following a high intensity wildfire in the California chaparral. Annual Meeting of the Ecological Society of America. Montreal, Canada

  32. 32.

    Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88(3):541–549

    PubMed  Article  Google Scholar 

  33. 33.

    Faeth SH, Hammon KE (1997) Fungal endophytes in oak trees: long-term patterns of abundance and associations with leafminers. Ecology 78(3):810–819

    Article  Google Scholar 

  34. 34.

    Arnold AE, Miadlikowska J, Higgins KL, Sarvate SD, Gugger P, Way A, Hofstetter V, Kauff F, Lutzoni F (2009) A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Syst Biol 58(3):283–297

    PubMed  Article  Google Scholar 

  35. 35.

    Gaylord ES, Preszler RW, Boecklen WJ (1996) Interactions between host plants, endophytic fungi, and a phytophagous insect in an oak (Quercus grisea × Q. gambelii) hybrid zone. Oecologia 105(3):336–342

    Article  Google Scholar 

  36. 36.

    Hoffman M, Gunatilaka M, Ong J, Shimabukuro M, Arnold AE (2008) Molecular analysis reveals a distinctive fungal endophyte community associated with foliage of montane oaks in southeastern Arizona. J Ariz Nev Acad Sci 40:91–100

    Article  Google Scholar 

  37. 37.

    Hoffman MT, Arnold AE (2008) Geographic locality and host identity shape fungal endophyte communities in cupressaceous trees. Mycol Res 112(3):331–344

    CAS  PubMed  Article  Google Scholar 

  38. 38.

    Hoffman MT, Arnold AE (2010) Diverse bacteria inhabit living hyphae of phylogenetically diverse fungal endophytes. Appl Environ Microbiol 76(12):4063–4075

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  39. 39.

    U’Ren JM, Lutzoni F, Miadlikowska J, Arnold AE (2010) Community analysis reveals close affinities between endophytic and endolichenic fungi in mosses and lichens. Microb Ecol 60(2):340–353

    PubMed  Article  Google Scholar 

  40. 40.

    Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182(2):314–330

    CAS  PubMed  Article  Google Scholar 

  41. 41.

    Gunatilaka AL (2006) Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity, and implications of their occurrence. J Nat Prod 69(3):509–526

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  42. 42.

    Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67(4):491–502

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  43. 43.

    Preszler RW, Gaylord ES, Boecklen WJ (1996) Reduced parasitism of a leaf-mining moth on trees with high infection frequencies of an endophytic fungus. Oecologia 108(1):159–166

    Article  Google Scholar 

  44. 44.

    Arnold AE, Lewis LC (2005) Ecology and evolution of fungal endophytes, and their roles against insects. In: Vega FE, Blackwell M (eds) Insect-fungal associations: ecology and evolution. Oxford University Press, New York, pp 74–96

    Google Scholar 

  45. 45.

    Niering WA, Lowe CH (1984) Vegetation of the Santa Catalina Mountains—community types and dynamics. Vegetatio 58(1):3–28

    Google Scholar 

  46. 46.

    Davison JE, Breshears DD, van Leeuwen WJD, Casady GM (2011) Remotely sensed vegetation phenology and productivity along a climatic gradient: on the value of incorporating the dimension of woody plant cover. Glob Ecol Biogeogr 20(1):101–113

    Article  Google Scholar 

  47. 47.

    Barton AM (2002) Intense wildfire in southeastern Arizona: transformation of a Madrean oak-pine forest to oak woodland. For Ecol Manag 165(1–3):205–212

    Article  Google Scholar 

  48. 48.

    Baker M (2011) Viability analyses for vascular plant species within Prescott National Forest, Arizona. Draft 4. Unpublished document on file. 108pp

  49. 49.

    Desilets SLE, Nijssen B, Ekwurzel B, Ferre TPA (2007) Post-wildfire changes in suspended sediment rating curves: Sabino Canyon, Arizona. Hydrol Process 21(11):1413–1423

    Article  Google Scholar 

  50. 50.

    USDA Forest Service (2005) Florida Fire Burned Area Emergency Response. http://mbreiding.us/ert/Arizona/Rincons/coronado/www.fs.fed.us/r3/coronado/florida/baer/index.html. Accessed 25 Feb 2015

  51. 51.

    Youberg A, Neary DG, Koestner KA, Koestner PE (2013) Post-wildfire erosion in the Chiricahua Mountains. In: Gottfried GJ, Ffolliott PF, Gebow BS, Eskew LG, Collins LC, comps. (eds) Merging science and management in a rapidly changing world: biodiversity and management of the Madrean Archipelago III, Tucson, AZ, 2012. USDA For Serv, Rocky Mountain Research Station, Fort Collins, CO, pp 357–361

  52. 52.

    InciWeb (2013) Doce Fire. http://inciweb.nwcg.gov/incident/3437/. Accessed 25 Feb 2015

  53. 53.

    McLaughlin SP, Bowers JE (1990) A floristic analysis and checklist for the northern Santa Rita Mountains, Pima Co, Arizona. Southwest Nat 35(1):61–75

    Article  Google Scholar 

  54. 54.

    Baumgartner KH, Fulé PZ (2007) Survival and sprouting responses of Chihuahua pine after the Rodeo-Chediski fire on the Mogollon Rim, Arizona. West N Am Nat 67(1):51–56

    Article  Google Scholar 

  55. 55.

    Caprio AC, Zwolinski MJ (1995) Fire and vegetation in a Madrean oak woodland, Santa Catalina Mountains, southeastern Arizona. In: DeBano L, Gottfried GJ, Hamre RH, Edminster CB, Ffolliott PF, and Ortega-Rubio A (eds) Biodiversity and management of the Madrean Archipelago: the sky islands of the southwestern United States and northwest Mexico. USDA For Serv Gen Tech Rep RM-GTR-264, Fort Collins, pp 389–398

  56. 56.

    Maghran LA (2014) Recovery and changes in plant communities from two large fires in the Santa Catalina Mountains, Arizona, USA. Dissertation, The University of Arizona

  57. 57.

    Higgins KL, Coley PD, Kursar TA, Arnold AE (2011) Culturing and direct PCR suggest prevalent host generalism among diverse fungal endophytes of tropical forest grasses. Mycologia 103(2):247–260

    PubMed  Article  Google Scholar 

  58. 58.

    Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8(3):186–194

    CAS  PubMed  Article  Google Scholar 

  59. 59.

    Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8(3):175–185

    CAS  PubMed  Article  Google Scholar 

  60. 60.

    Maddison WP, Maddison DR (2015) Mesquite: a modular system for evolutionary analysis. Ver 3.02 http://mesquiteproject.org

  61. 61.

    Monacell JT, Carbone I (2014) Mobyle SNAP Workbench: a web-based analysis portal for population genetics and evolutionary genomics. Bioinformatics 30(10):1488–1490

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  62. 62.

    U’Ren JM, Riddle JM, Monacell JT, Carbone I, Miadlikowska J, Arnold AE (2014) Tissue storage and primer selection influence pyrosequencing‐based inferences of diversity and community composition of endolichenic and endophytic fungi. Mol Ecol Resour 14:1032–1048

    PubMed  Google Scholar 

  63. 63.

    U’Ren JM, Lutzoni F, Miadlikowska J, Laetsch AD, Arnold AE (2012) Host and geographic structure of endophytic and endolichenic fungi at a continental scale. Am J Bot 99(5):898–914

    PubMed  Article  Google Scholar 

  64. 64.

    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  65. 65.

    Nilsson RH, Veldre V, Hartmann M, Unterseher M, Amend A, Bergsten J, Kristiansson E, Ryberg M, Jumpponen A, Abarenkov K (2010) An open source software package for automated extraction of ITS1 and ITS2 from fungal ITS sequences for use in high-throughput community assays and molecular ecology. Fungal Ecol 3(4):284–287

    Article  Google Scholar 

  66. 66.

    Sun Y, Cai Y, Liu L, Yu F, Farrell ML, McKendree W, Farmerie W (2009) ESPRIT: estimating species richness using large collections of 16S rRNA pyrosequences. Nucleic Acids Res 37(10):e76

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  67. 67.

    Schloss PD (2010) The effects of alignment quality, distance calculation method, sequence filtering, and region on the analysis of 16S rRNA gene-based studies. PLoS Comput Biol 6(7):e1000844

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  68. 68.

    Schloss PD (2009) A high-throughput DNA sequence aligner for microbial ecology studies. PLoS ONE 4(12):e8230

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  69. 69.

    White JR, Navlakha S, Nagarajan N, Ghodsi M-R, Kingsford C, Pop M (2010) Alignment and clustering of phylogenetic markers—implications for microbial diversity studies. BMC Bioinforma 11(1):152

    Article  CAS  Google Scholar 

  70. 70.

    U’Ren JM, Dalling JW, Gallery RE, Maddison DR, Davis EC, Gibson CM, Arnold AE (2009) Diversity and evolutionary origins of fungi associated with seeds of a neotropical pioneer tree: a case study for analysing fungal environmental samples. Mycol Res 113(4):432–449

    PubMed  Article  CAS  Google Scholar 

  71. 71.

    Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):9

    Google Scholar 

  72. 72.

    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410

    CAS  PubMed  Article  Google Scholar 

  73. 73.

    Huson DH, Auch AF, Qi J, Schuster SC (2007) MEGAN analysis of metagenomic data. Genome Res 17(3):377–386

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  74. 74.

    Huson DH, Mitra S, Ruscheweyh H-J, Weber N, Schuster SC (2011) Integrative analysis of environmental sequences using MEGAN4. Genome Res 21(9):1552–1560

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  75. 75.

    Baisan C, Swetnam TW (1990) Fire history on a desert mountain range: Rincon Mountain Wilderness, Arizona, U.S.A. Can J For Res 20:1559–1569

    Article  Google Scholar 

  76. 76.

    Swetnam TW, Baisan CH, Caprio AC, Brown PM (1992) Fire history in a Mexican oak-pine woodland and adjacent montane conifer gallery forest in southeastern Arizona. In: Ffolliott PF, Gottfried GJ, Bennett DA, Hernandez C, Victor M, Ortega-Rubio A, Hamre RH (eds) Ecology and management of oaks and associated woodlands: perspectives in the southwestern United States and northern Mexico. USDA For Serv Gen Tech Rep RM-GTR-218. Fort Collins, pp 165–173

  77. 77.

    Seklecki MT, Grissino-Mayer HD, Swetnam TW (1996) Fire history and the possible role of Apache-set fires in the Chiricahua Mountains of southeastern Arizona. In: Ffolliott PF, DeBano LF, Baker MB, Gottfried GJ, Solis-Garza S, Edminster CB, Neary DG, Hamre RH (eds) Effects of fire on Madrean province ecosystems. USDA For Serv Gen Tech Rep RM-GTR-289. Fort Collins, pp 238–246

  78. 78.

    Swetnam TW (2005) Fire histories from pine-dominant forest in the Madrean Archipelago. In: Gottfried GJ, Gebow BS, Eskew LG, Edminster CB (eds) Connecting mountain islands and desert seas: biodiversity and management of the Madrean Archipelago II. USDA For Serv RMRS-P-36. Fort Collins, pp 35–43

  79. 79.

    Kaib M, Baisan CH, Grissino-Mayer HD, Swetnam TW (1996) Fire history in the gallery pine-oak forests and adjacent grasslands of the Chiricahua mountains of Arizona. In: Ffolliott PF, DeBano LF, Baker MB, Gottfried GJ, Solis-Garza S, Edminster CB, Neary DG, Hamre RH (eds) Effects of fire on Madrean province ecosystems. USDA For Serv Gen Tech Rep RM-GTR-289. Fort Collins, pp 253–264

  80. 80.

    Kaib M, Swetnam TW, Baisan CH (1999) Fire history in canyon pine-oak forests, intervening desert grasslands, and higher-elevation mixed-conifer forests of the southwest borderlands. In: Gottfried GJ, Curtin CG (eds) Toward integrated research, land management, and ecosystem protection in the Malpai Borderlands. USDA For Serv RMRS-P-10. Fort Collins, pp 57–64

  81. 81.

    Swetnam TW, Baisan CH (1996) Historical fire regime patterns in the southwestern United States since AD 1700. In: Allen CD (ed) Fire effects in southwestern forest. USDA For Serv Gen Tech Rep RM-GTR-286. Fort Collins, pp 11–32

  82. 82.

    Dooley S, Treseder K (2012) The effect of fire on microbial biomass: a meta-analysis of field studies. Biogeochemistry 109(1–3):49–61

    Article  Google Scholar 

  83. 83.

    Parker TJ, Clancy KM, Mathiasen RL (2006) Interactions among fire, insects and pathogens in coniferous forests of the interior western United States and Canada. Agric For Entomol 8(3):167–189

    Article  Google Scholar 

  84. 84.

    Rieske LK (2002) Wildfire alters oak growth, foliar chemistry, and herbivory. For Ecol Manag 168(1–3):91–99

    Article  Google Scholar 

  85. 85.

    Rieske LK, Housman HH, Arthur MA (2002) Effects of prescribed fire on canopy foliar chemistry and suitability for an insect herbivore. For Ecol Manag 160(1–3):177–187

    Article  Google Scholar 

  86. 86.

    Ferwerda JG, Siderius W, Van Wieren SE, Grant CC, Peel M, Skidmore AK, Prins HHT (2006) Parent material and fire as principle drivers of foliage quality in woody plants. For Ecol Manag 231(1–3):178–183

    Article  Google Scholar 

  87. 87.

    Wiersma GB, Elvir JA, Eckhoff JD (2007) Forest vegetation monitoring and foliar chemistry of red spruce and red maple at Acadia National Park in Maine. Environ Monit Assess 126(1–3):27–37

    CAS  PubMed  Article  Google Scholar 

  88. 88.

    Pausas JG, Bradstock RA, Keith DA, Keeley JE (2004) Plant functional traits in relation to fire in crown-fire ecosystems. Ecology 85(4):1085–1100

    Article  Google Scholar 

  89. 89.

    Kruger FJ (1983) Plant community diversity and dynamics in relation to fire. In: Kruger FJ, Mitchell DT, Jarvis JUM (eds) Mediterranean-type ecosystems. Springer, Berlin, pp 446–472

    Chapter  Google Scholar 

  90. 90.

    Hart SC, DeLuca TH, Newman GS, MacKenzie MD, Boyle SI (2005) Post-fire vegetative dynamics as drivers of microbial community structure and function in forest soils. For Ecol Manag 220(1–3):166–184

    Article  Google Scholar 

  91. 91.

    Egger KN (1986) Substrate hydrolysis patterns of post-fire Ascomycetes (Pezizales). Mycologia 78(5):771–780

    CAS  Article  Google Scholar 

  92. 92.

    Tedersoo L, Arnold AE, Hansen K (2013) Novel aspects in the life cycle and biotrophic interactions in Pezizomycetes (Ascomycota, Fungi). Mol Ecol 22(6):1488–1493

    PubMed  Article  Google Scholar 

  93. 93.

    Rincón A, Santamaría BP, Ocaña L, Verdú M (2014) Structure and phylogenetic diversity of post-fire ectomycorrhizal communities of maritime pine. Mycorrhiza 24(2):131–141

    PubMed  Article  Google Scholar 

  94. 94.

    Longo S, Nouhra E, Goto BT, Berbara RL, Urcelay C (2014) Effects of fire on arbuscular mycorrhizal fungi in the Mountain Chaco Forest. For Ecol Manag 315:86–94

    Article  Google Scholar 

  95. 95.

    Kipfer T, Moser B, Egli S, Wohlgemuth T, Ghazoul J (2011) Ectomycorrhiza succession patterns in Pinus sylvestris forests after stand-replacing fire in the Central Alps. Oecologia 167(1):219–228

    PubMed  Article  Google Scholar 

  96. 96.

    Kutorga E, Adamonytė G, Iršėnaitė R, Juzėnas S, Kasparavičius J, Markovskaja S, Motiejūnaitė J, Treigienė A (2012) Wildfire and post-fire management effects on early fungal succession in Pinus mugo plantations, located in Curonian Spit (Lithuania). Geoderma 191:70–79

    Article  Google Scholar 

  97. 97.

    Motiejūnaitė J, Adamonytė G, Iršėnaitė R, Juzėnas S, Kasparavičius J, Kutorga E, Markovskaja S (2014) Early fungal community succession following crown fire in Pinus mugo stands and surface fire in Pinus sylvestris stands. Eur J For Res 133(4):745–756

    Article  Google Scholar 

  98. 98.

    Rajala T, Velmala SM, Tuomivirta T, Haapanen M, Müller M, Pennanen T (2013) Endophyte communities vary in the needles of Norway spruce clones. Fungal Biol 117(3):182–190

    PubMed  Article  Google Scholar 

  99. 99.

    Shubin L, Juan H, Renchao Z, ShiRu X, YuanXiao J (2014) Fungal endophytes of Alpinia officinarum rhizomes: insights on diversity and variation across growth years, growth sites, and the inner active chemical concentration. PLoS ONE 9(12):e115289

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  100. 100.

    Rajala T, Velmala SM, Vesala R, Smolander A, Pennanen T (2014) The community of needle endophytes reflects the current physiological state of Norway spruce. Fungal Biol 118(3):309–315

    PubMed  Article  Google Scholar 

  101. 101.

    Zimmerman NB, Vitousek PM (2012) Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape. Proc Natl Acad Sci U S A 109(32):13022–13027

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  102. 102.

    U’Ren JM, Lutzoni F, Miadlikowska J, Gleason T, Leo A, Monacell JT, Arendt K, Lefevre E, Ball B, Chen K-H, May G, Carbone I, Arnold AE (2015) Geographic and temporal structure of endophytic and endolichenic fungal communities of the boreal biome. 28th Fungal Genetics Conference, Pacific Grove

  103. 103.

    Begerow D, Nilsson H, Unterseher M, Maier W (2010) Current state and perspectives of fungal DNA barcoding and rapid identification procedures. Appl Microbiol Biotechnol 87(1):99–108

    CAS  PubMed  Article  Google Scholar 

  104. 104.

    Jumpponen A, Jones KL (2009) Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytol 184(2):438–448

    CAS  PubMed  Article  Google Scholar 

  105. 105.

    Bailey JK, Deckert R, Schweitzer JA, Rehill BJ, Lindroth RL, Gehring C, Whitham TG (2005) Host plant genetics affect hidden ecological players: links among Populus, condensed tannins, and fungal endophyte infection. Can J Bot 83(4):356–361

    Article  Google Scholar 

  106. 106.

    Moricca S, Ginetti B, Ragazzi A (2012) Species- and organ-specificity in endophytes colonizing healthy and declining Mediterranean oaks. Phytopathol Mediterr 51(3):587–598

    Google Scholar 

  107. 107.

    Collado J, Platas G, González I, Peláez F (1999) Geographical and seasonal influences on the distribution of fungal endophytes in Quercus ilex. New Phytol 144(3):525–532

    Article  Google Scholar 

  108. 108.

    Sahashi N, Kubono T, Miyasawa Y, Si I (1999) Temporal variations in isolation frequency of endophytic fungi of Japanese beech. Can J Bot 77(2):197–202

    Article  Google Scholar 

  109. 109.

    Guo L-D, Huang G-R, Wang Y (2008) Seasonal and tissue age influences on endophytic fungi of Pinus tabulaeformis (Pinaceae) in the Dongling Mountains, Beijing. J Integr Plant Biol 50(8):997–1003

    PubMed  Article  Google Scholar 

  110. 110.

    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(1):8–21

    PubMed  Article  Google Scholar 

  111. 111.

    Carroll G (1995) Forest endophytes: pattern and process. Can J Bot 73(S1):1316–1324

    Article  Google Scholar 

  112. 112.

    Matsumura E, Fukuda K (2013) A comparison of fungal endophytic community diversity in tree leaves of rural and urban temperate forests of Kanto district, eastern Japan. Fungal Biol 117(3):191–201

    PubMed  Article  Google Scholar 

  113. 113.

    Arnold AE, Herre EA (2003) Canopy cover and leaf age affect colonization by tropical fungal endophytes: ecological pattern and process in Theobroma cacao (Malvaceae). Mycologia 95(3):388–398

    PubMed  Article  Google Scholar 

  114. 114.

    Carroll G (1988) Fungal endophytes in stems and leaves—from latent pathogen to mutualistic symbiont. Ecology 69(1):2–9

    Article  Google Scholar 

  115. 115.

    Arnold AE, Mejía 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(26):15649–15654

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  116. 116.

    Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343

    Article  Google Scholar 

  117. 117.

    Schulz B, Römmert A-K, Dammann U, Aust H-J, Strack D (1999) The endophyte–host interaction: a balanced antagonism? Mycol Res 103(10):1275–1283

    Article  Google Scholar 

  118. 118.

    Jiang H, Shi Y-T, Zhou Z-X, Yang C, Chen Y-J, Chen L-M, Yang M-Z, Zhang H-B (2011) Leaf chemistry and co-occurring species interactions affecting the endophytic fungal composition of Eupatorium adenophorum. Ann Microbiol 61(3):655–662

    Article  Google Scholar 

  119. 119.

    Estrada C, Rojas EI, Wcislo WT, Van Bael SA (2014) Fungal endophyte effects on leaf chemistry alter the in vitro growth rates of leaf-cutting ants’ fungal mutualist, Leucocoprinus gongylophorus. Fungal Ecol 8:37–45

    Article  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge financial support from NIH R01-CA90265 to AAL Gunatilaka and AEA; NSF DEB-0640996, DEB-072825, and DEB-1045766 to AEA; NIFA ARZT-1259370-S25-200 and ARZT-1360230-H25-218 to AEA; the Arizona Biomedical and Biological Sciences Graduate Program (YLH); and the College of Agriculture and Life Sciences and School of Plant Sciences at The University of Arizona (AEA and YLH). We thank M. del Olmo Ruiz and M. Gunatilaka for logistical support; D. Falk for providing information on fire history; S. Araldi, E. Bowman, N. Garber, J. Shaffer, and N. Zimmerman for reviewing the manuscript; C. Khambholja for editorial assistance; A. Ray-Maitra, M. Amistadi and Motzz Laboratories for chemical analyses; J. DeVore, A. Ndobegang and J.P. Toledo for assistance in laboratory work; and members of the Arnold lab at the University of Arizona for helpful discussion. This paper represents a portion of the doctoral dissertation research of YLH in School of Plant Sciences at The University of Arizona, and guidance from R.E. Gallery, J. Bronstein, M. McMahon, and M. Orbach is gratefully acknowledged in this context.

Author information

Affiliations

Authors

Corresponding author

Correspondence to A. Elizabeth Arnold.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table 1

Sample sites, collection information, burn status, microsite, and isolation frequency of culturable endophytes for each tree. Individuals sampled more than once are listed separately by sampling event. JD: J. deppeana, QH: Q. hypoleucoides, QT: Q. turbinella. (XLSX 16 kb)

Supplementary Table 2

Top BLAST hits of 1298 sequences. (XLSX 96 kb)

Supplementary Table 3

Ca, K, Mg, and N content in mature, symptomless leaves of J. deppeana and Q. hypoleucoides. Values indicate percentage of leaf dry weight. JD: J. deppeana, QH: Q. hypoleucoides. (PDF 99 kb)

Supplementary Table 4

Occurrence of 95 OTU as a function of host taxon and burn status, and class-level taxonomic placement of each OTU. Data represent isolates for which both ITS1 and ITS2 were sequenced (see Methods). (XLSX 18 kb)

Supplementary Table 5

PERMANOVA shows that community structure differed significantly as a function of host taxon and fire age class, but did not differ as a function of the host taxon X fire age class interaction. * indicates significant results (PDF 171 kb)

Supplementary Fig. 1

Regression analyses with least-squares contrast for endophyte isolation frequency and diversity in the Santa Rita Mountains reveal differences between fire age classes defined by ≤6 and 7–18 years, providing a basis for delineating very recent (≤6 years since fire) and recent (7–18 years since fire) age classes. a log-transformed isolation frequency, with season and host species set as random factors and fire age class as the explanatory variable (F 1, 19.82 = 10.96, P = 0.0035). b log-transformed Fisher's alpha, with host species set as a random factor and fire age class as the explanatory variable (F 1, 11.04 = 5.60, P = 0.0374). Different letters represent significant differences between fire age classes. Season was not included in the latter analysis because it was not associated with differences in diversity (see Methods) (DOCX 90 kb)

Supplementary Fig. 2

Herbivory and pathogen damage scores for mature leaves of Quercus spp., and their relationship to fire age class, endophyte isolation frequency, and diversity. a Herbivory damage was significantly lower (*) in the very recent fire age class (≤6 years; ANOVA, F 2, 148 = 8.4947, P = 0.0003) relative to the other fire age classes. Pathogen damage did not differ as a function of fire age class (ANOVA, F 2, 148 = 0.5559, P = 0.5747). be Herbivory and pathogen damage scores were not related to endophyte isolation frequency and diversity. (DOCX 158 kb)

Supplementary Fig. 3

In vitro fungal growth on leaf extracts prepared from healthy foliage of J. deppeana or Q. hypoleucoides. Colony radius was compared for four endophyte isolates grown on extracts from the host species from which they were isolated (i.e., same host), vs. the other host species (i.e., different host). Different letters indicate significant differences. Data show the colony radius of YLH0024 after 18 days (t 22 = −1.21, P = 0.2389), YLH0063 after 10 days (t 21 = 2.53, P = 0.0193), YLH0084 after 8 days (t 22 = −0.97, P = 0.3419), and YLH0112 after 20 days (t 22 = −3.07, P = 0.0057) (DOCX 97 kb)

Supplementary Fig. 4

Linear regression of a isolation frequency and b diversity of endophytes vs. foliar Ca, K, Mg, and N content in J. deppeana (DOCX 200 kb)

Supplementary Fig. 5

Linear regression of a isolation frequency and b diversity of endophytes vs. foliar Ca, K, Mg, and N content in Q. hypoleucoides (DOCX 201 kb)

Supplementary Fig. 6

Leaf Ca, K, Mg and N content did not differ significantly among fire age classes in a J. deppeana (Ca: F 2, 30 = 1.38, P = 0.2679; K: F 2, 30 = 1.50, P = 0.2401; Mg: F 2, 30 = 0.82, P = 0.4486; N: F 2, 30 = 2.47, P = 0.1019) or b Q. hypoleucoides (Ca: F 2, 20 = 1.49, P = 0.2496; K: F 2, 20 = 0.60, P = 0.5591; Mg: F 2, 20 = 0.31, P = 0.7387; N: F 2, 20 = 0.02, P = 0.9851) (DOCX 33 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Huang, YL., Devan, M.M.N., U’Ren, J.M. et al. Pervasive Effects of Wildfire on Foliar Endophyte Communities in Montane Forest Trees. Microb Ecol 71, 452–468 (2016). https://doi.org/10.1007/s00248-015-0664-x

Download citation

Keywords

  • Ascomycota
  • Diversity
  • Dothideomycetes
  • Eurotiomycetes
  • Fire history
  • Forest management
  • Leotiomycetes
  • Pezizomycetes
  • Phenology
  • Sordariomycetes
  • Symbiosis