Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-15T07:23:56.378Z Has data issue: false hasContentIssue false
  • English
  • Français

Community structure of fern-affiliated endophytes in three neotropical forests

Published online by Cambridge University Press:  02 November 2016

Mariana Del Olmo-Ruiz  and
A. Elizabeth Arnold
Mariana Del Olmo-Ruiz
Affiliation:
School of Plant Sciences, The University of Arizona, Tucson, AZ 85721, USA
A. Elizabeth Arnold*
Affiliation:
School of Plant Sciences, The University of Arizona, Tucson, AZ 85721, USA Department of Ecology and Evolutionary Biology, The University of Arizona, Tucson, AZ 85721, USA
*
2 Corresponding author. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract:

From the saprotrophs that decay plant material to the pathogens and mutualists that shape plant demography at local and regional scales, fungi are major drivers of tropical forest dynamics. Although endophytic fungi are abundant and diverse in many biomes, they reach their greatest diversity in tropical forests, where they can influence plant physiology, performance and survival. The number of quantitative studies regarding endophytes has increased dramatically in the past two decades, but general rules have not yet emerged regarding the biogeography, host affiliations, local or regional distributions, or phylogenetic diversity of endophytes in most tropical settings. Here, endophytic fungal communities associated with 18 species of eupolypod fern were compared among forest reserves in Panama, Costa Rica and Mexico. Molecular sequence data for >2000 isolates were used to determine the relationships of host taxonomy, forest (site), and environmental dissimilarity to endophyte community composition. Communities in related ferns differed significantly among forests, reflecting the interplay of geographic distance and environmental dissimilarity. Although the same phyla and classes of fungi were prevalent at each site, they differed in relative abundance. All sites were dominated by the same order (Xylariales), but sites differed in the phylogenetic clustering vs. evenness of their endophyte communities. By addressing the relationship of endophyte communities to host taxonomy, geographic distance and environmental factors, this study complements previous work on angiosperms and contributes to a growing perspective on the factors shaping communities of ecologically important fungi in tropical forests.

Keywords

Ascomycotabiodiversityeupolypodsfungiphylogenetic diversityPteridophytesXylariales
Type
Research Article
Information
Journal of Tropical Ecology , Volume 33 , Issue 1 , January 2017 , pp. 60 - 73
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ALTSCHUL, S., GISH, W., MILLER, W., MYERS, E. & LIPMAN, D. 1990. Basic local alignment search tool. Journal of Molecular Biology 215:403–410.Google Scholar
ARCHER, K. & COLE, A. 1986. Cuticle, cell wall ultrastructure and disease resistance in maidenhair fern. New Phytologist 103:341–348.Google Scholar
ARNOLD, A. E. 2008. Endophytic fungi: hidden components of tropical community ecology. Pp. 254–271 in Schnitzer, S. & Carson, W. (eds). Tropical forest community ecology. Wiley-Blackwell, Oxford.Google Scholar
ARNOLD, A. E. & ENGELBRECHT, B. M. J. 2007. Fungal endophytes nearly double minimum leaf conductance in seedlings of a neotropical tree species. Journal of Tropical Ecology 23:369–372.CrossRefGoogle Scholar
ARNOLD, A. E. & LUTZONI, F. 2007. Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549.Google Scholar
ARNOLD, A. E., GILBERT, G. S., COLEY, P. D., THOMAS, A., MAYNARD, Z., GILBERT, G. S., COLEY, P. D. & KURSAR, T. A. 2000. Are tropical fungal endophytes hyperdiverse? Ecology Letters 3:267–274.Google Scholar
ARNOLD, A. E., MAYNARD, Z. & GILBERT, G. S. 2001. Fungal endophytes in dicotyledonous neotropical trees: patterns of abundance and diversity. Mycological Research 105:1502–1507.Google Scholar
ARNOLD, A. E., MEJÍA, L. C., KYLLO, D., ROJAS, E. I., MAYNARD, Z., ROBBINS, N. & HERRE, E. A. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences USA 100:15649–54.CrossRefGoogle Scholar
ARNOLD, A. E., HENK, D. A., EELLS, R. L., LUTZONI, F. & VILGALYS, R. 2007. Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia 99:185–206.Google Scholar
ARNOLD, A. E., MIADLIKOWSKA, J., HIGGINS, K. L., SARVATE, S. D., 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? Systematic Biology 58:283–97.Google Scholar
BAGCHI, R., GALLERY, R. E., GRIPENBERG, S., GURR, S. J., NARAYAN, L., ADDIS, C. E., FRECKLETON, R. P. & LEWIS, O. T. 2014. Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature 506:85–88.Google Scholar
BORCARD, D., GILLET, F. & LEGENDRE, P. 2011. Numerical ecology with R. Use R! series. Springer, New York. 302 pp.Google Scholar
CLARKE, K. R. 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18:117–143.Google Scholar
COLEY, P. D. & BARONE, J. A. 1996. Herbivory and plant defenses in tropical forests. Annual Review of Ecology and Systematics 27:305–335.Google Scholar
CROAT, T. 1978. Flora of Barro Colorado Island. Stanford University Press, Stanford. 943 pp.Google Scholar
DAVIDSE, G., SOUSA, M. & KNAPP, S. (eds). 1995. Flora Mesoamericana. Vol. 1: Psilotaceae a Salvinaceae. Universidad Nacional Autónoma de México/Missouri Botanical Garden/The Natural History Museum, Mexico City. 470 pp.Google Scholar
DEL OLMO-RUIZ, M. & ARNOLD, A. E. 2014. Interannual variation and host affiliations of endophytic fungi associated with ferns at La Selva, Costa Rica. Mycologia 106:8–21.Google Scholar
DIRZO, R., GONZALES-SORIANO, E. & VOGT, R. 1997. Introducción general. Pp. 3–6 in Gonzales-Soriano, E., Dirzo, R. & Vogt, R. (eds). Historia natural de los Tuxtlas. Universidad Nacional Autonoma de Mexico, Mexico City.Google Scholar
ESTRADA, C., DEGNER, E. C., ROJAS, E. I., WCISLO, W. T. & VAN BAEL, S. A. 2015. The role of endophyte diversity in protecting plants from defoliation by leaf-cutting ants. Current Science 109:19–25.Google Scholar
EWING, B. & GREEN, P. 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Research 8:186–194.Google Scholar
EWING, B., HILLIER, L., WENDL, M. & GREEN, P. 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Research 8:175–185.Google Scholar
FISHER, P. J. 1996. Survival and spread of the endophyte Stagonospora pteridiicola in Pteridium aquilinum, other ferns and some flowering plants. New Phytologist 132:119–122.Google Scholar
FISHER, P. J. & PUNITHALINGAM, E. 1993. Stagonospora pteridiicola sp. nov., a new endophytic coelomycete in Pteridium aquilinum . Mycological Research 97:661–664.Google Scholar
GARDES, M. & BRUNS, T. D. 1993. ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Molecular Ecology 2:113–118.Google Scholar
GOSLEE, S. C. & URBAN, D. L. 2007. The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software 22:1–19.Google Scholar
GOTELLI, N. J. 2004. A taxonomic wish-list for community ecology. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 359:585–597.Google Scholar
GRAHAM, C. H. & FINE, P. V. A. 2008. Phylogenetic beta diversity: linking ecological and evolutionary processes across space in time. Ecology Letters 11:1265–1277.Google Scholar
HARPER, D. A. T. (ed.). 1999. Numerical palaeobiology: computer-based modelling and analysis of fossils and their distributions. John Wiley & Sons, Chichester. 468 pp.Google Scholar
HELANDER, M., AHLHOLM, J., SIEBER, T. N., HINNERI, S. & SAIKKONEN, K. 2007. Fragmented environment affects birch leaf endophytes. New Phytologist 175:547–553.Google Scholar
HIGGINBOTHAM, S. J., ARNOLD, A. E., IBAÑEZ, A., SPADAFORA, C., COLEY, P. D. & KURSAR, T. A. 2013. Bioactivity of fungal endophytes as a function of endophyte taxonomy and the taxonomy and distribution of their host plants. PLoS ONE 8:e73192.Google Scholar
HIGGINS, K. L., COLEY, P. D., KURSAR, T. A. & ARNOLD, A. E. 2011. Culturing and direct PCR suggest prevalent host generalism among diverse fungal endophytes of tropical forest grasses. Mycologia 103:247–260.Google Scholar
HIGGINS, K., ARNOLD, A., COLEY, P. & KURSAR, T. 2014. Communities of fungal endophytes in tropical forest grasses: highly diverse host- and habitat generalists characterized by strong spatial structure. Fungal Ecology 8:1–11.Google Scholar
HOFFMAN, M. T. & ARNOLD, A. E. 2008. Geographic locality and host identity shape fungal endophyte communities in cupressaceous trees. Mycological Research 112:331–44.Google Scholar
JOHNSON, M. T. J. & STINCHCOMBE, J. R. 2007. An emerging synthesis between community ecology and evolutionary biology. Trends in Ecology and Evolution 22:250–257.Google Scholar
KATOH, K. & STANDLEY, D. M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30:772–780.Google Scholar
KEMBEL, S. W., COWAN, P. D., HELMUS, M. R., CORNWELL, W. K., MORLON, H., ACKERLY, D. D., BLOMBERG, S. P. & WEBB, C. O. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464.CrossRefGoogle ScholarPubMed
KINDT, R. & COE, R. 2005. Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre (ICRAF), Nairobi. 207 pp.Google Scholar
KREFT, H., JETZ, W., MUTKE, J. & BARTHLOTT, W. 2010. Contrasting environmental and regional effects on global pteridophyte and seed plant diversity. Ecography 33:408–419.Google Scholar
LEGENDRE, P. & FORTIN, M. 1989. Spatial pattern and ecological analysis. Vegetatio 80:107–138.Google Scholar
MARKHAM, K., CHALK, T. & STEWARD, C. N. 2006. Evaluation of fern and moss protein-based defenses against phytophagous insects. International Journal of Plant Science 167:111–117.Google Scholar
MCDADE, L. A., BAWA, K. S., HESPENHEIDE, H. A. & HARTSHORN, G. S. 1994. (eds). La Selva: ecology and natural history of a Neotropical rain forest. University of Chicago Press, Chicago. 493 pp.Google Scholar
MICKEL, J. & SMITH, A. 2004. The pteridophytes of Mexico. Memoirs of the New York Botanical Garden 88:1–1054.Google Scholar
MURALI, T. S., SURYANARAYANAN, T. S. & VENKATESAN, G. 2007. Fungal endophyte communities in two tropical forests of southern India: diversity and host affiliation. Mycological Progress 6:191–199.Google Scholar
PETRINI, O., FISHER, P. J. & PETRINI, L. E. 1992. Fungal endophytes of bracken (Pteridium aquilinum), with some reflections on their use in biological control. Sydowia 44:282–293.Google Scholar
RIBA, R. & PEREZ-GARCIA, B. 1997. Pteridofitas. Pp. 175–181 in Gonzales-Soriano, E., Dirzo, R. & Vogt, R. (eds). Historia natural de los Tuxtlas. Universidad Nacional Autonoma de Mexico, Mexico City.Google Scholar
RICHARDSON, K. A. & CURRAH, R. S. 1995. The fungal community associated with the roots of some rainforest epiphytes of Costa Rica. Selbyana 16:49–73.Google Scholar
RODRIGUEZ, R. J., WHITE, J. F., ARNOLD, A. E. & REDMAN, R. S. 2009. Fungal endophytes: diversity and functional roles. The New Phytologist 182:314–330.Google Scholar
SAIKKONEN, K. 2007. Forest structure and fungal endophytes. Fungal Biology Reviews 21:67–74.CrossRefGoogle Scholar
SCHMID, E., OBERWINKLER, F. & GÓMEZ, L. D. 1995. Light and electron microscopy of a host-fungus interaction in the roots of some epiphytic ferns from Costa Rica. Canadian Journal of Botany 73:991–996.Google Scholar
SCHUETTPELZ, E. & PRYER, K. 2009. Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. Proceedings of the National Academy of Sciences USA 106:11200–11205.Google Scholar
SIEBER, T. N. 2007. Endophytic fungi in forest trees: are they mutualists? Fungal Biology Reviews 21:75–89.Google Scholar
SMITH, A. R., PRYER, K. M., SCHUETTPELZ, E., KORALL, P., SCHNEIDER, H. & WOLF, P. G. 2006. A classification for extant ferns. Taxon 55:705–731.Google Scholar
STAMATAKIS, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313.Google Scholar
STAMATAKIS, A., BLAGOJEVIC, F., NIKOLOPOULOS, D. S. & ANTONOPOULOS, C. D. 2007. Exploring new search algorithms and hardware for phylogenetics: RAxML meets the IBM Cell. Journal of VLSI Signal Processing Systems for Signal, Image, and Video Technology 48:271–286.Google Scholar
SURYANARAYANAN, T. S., MURALI, T. S. & VENKATESAN, G. 2002. Occurrence and distribution of fungal endophytes in tropical forests across a rainfall gradient. Canadian Journal of Botany 80:818–826.Google Scholar
SURYANARAYANAN, T. S., VENKATESAN, G. & MURALI, T. S. 2003. Endophytic fungal communities in leaves of tropical forest trees: diversity and distribution patterns. Current Science 85:489–493.Google Scholar
TAVARE, S. 1986. Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences 17:57–86.Google Scholar
U'REN, J. M., DALLING, J. W., GALLERY, R. E., MADDISON, D. R., DAVIS, E. C., GIBSON, C. M. & ARNOLD, A. E. 2009. Diversity and evolutionary origins of fungi associated with seeds of a Neotropical pioneer tree: a case study for analysing fungal environmental samples. Mycological Research 113:432–449.Google Scholar
U'REN, J. M., LUTZONI, F., MIADLIKOWSKA, J. & ARNOLD, A. E. 2010. Community analysis reveals close affinities between endophytic and endolichenic fungi in mosses and lichens. Microbial Ecology 60:340–353.Google Scholar
U'REN, J. M., LUTZONI, F., MIADLIKOWSKA, J., LAETSCH, A. D. & ARNOLD, A. E. 2012. Host and geographic structure of endophytic and endolichenic fungi at a continental scale. American Journal of Botany 99:898–914.Google Scholar
U'REN, J. M., RIDDLE, J. M., MONACELL, J. T., CARBONE, I., MIADLIKOWSKA, J. & ARNOLD, A. E. 2014. Tissue storage and primer selection influence pyrosequencing-based inferences of diversity and community composition of endolichenic and endophytic fungi. Molecular Ecology Resources 14:1032–1048.Google Scholar
URS, R. R., ROBERTS, P. D. & SCHULTZ, D. C. 2006. Localisation of hydrogen peroxide and peroxidase in gametophytes of Ceratopteris richardii (C-fern) grown in the presence of pathogenic fungi in a gnotobiotic system. Annals of Applied Biology 149:327–336.Google Scholar
VAN BAEL, S. A., FERNÁNDEZ-MARÍN, H., VALENCIA, M. C., ROJAS, E. I., WCISLO, W. T. & HERRE, E. A. 2009. Two fungal symbioses collide: endophytic fungi are not welcome in leaf-cutting ant gardens. Proceedings of the Royal Society B 276:2419–2426.Google Scholar
VASCO, A., MORAN, R. C. & AMBROSE, B. A. 2013. The evolution, morphology, and development of fern leaves. Frontiers in Plant Science 4:345.Google Scholar
VEGA, F., POSADA, F., AIME, M., PAVA-RIPOLL, M., INFANTE, F. & REHNER, S. 2008. Entomopathogenic fungal endophytes. Biological Control 46:72–82.Google Scholar
VILGALYS, R. & HESTER, M. 1990. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172:4238–4246.Google Scholar
VINCENT, J. B., WEIBLEN, G. D. & MAY, G. 2016. Host associations and beta diversity of fungal endophyte communities in New Guinea rainforest trees. Molecular Ecology 25:825–841.Google Scholar
WEBB, C. 2000. Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. American Naturalist 156:145–155.Google Scholar
WEBB, C. O., ACKERLY, D. D., MCPEEK, M. A. & DONOGHUE, M. J. 2002. Phylogenies and community ecology. Annual Review of Ecology and Systematics 33:475–505.Google Scholar
WHITE, T. J., BRUNS, T., LEE, S. B. & TAYLOR, J. W. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Pp. 315–322 in Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J. (eds). PCR protocols: a guide to methods and application. Academic Press, San Diego.Google Scholar
ZHANG, S. B., SUN, M., CAO, K. F., HU, H. & ZHANG, J. L. 2014. Leaf photosynthetic rate of tropical ferns is evolutionarily linked to water transport capacity. PLoS ONE 9.Google Scholar
ZUBEK, S., PIATEK, K., NAKS, P., HEISE, W., WAYDA, M. & MLECZKO, P. 2010. Fungal root endophyte colonization of fern and lycophyte species from the Celaque National Park in Honduras. American Fern Journal 100:126–136.Google Scholar