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.
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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.
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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). b–e 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)
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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
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DOI: https://doi.org/10.1007/s00248-015-0664-x