Mycorrhizal types influence island biogeography of plants
Language English Country Great Britain, England Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't, Research Support, U.S. Gov't, Non-P.H.S.
Grant support
I 3757
Austrian Science Fund FWF - Austria
PubMed
34561537
PubMed Central
PMC8463580
DOI
10.1038/s42003-021-02649-2
PII: 10.1038/s42003-021-02649-2
Knihovny.cz E-resources
- MeSH
- Biodiversity * MeSH
- Plant Dispersal * MeSH
- Plant Physiological Phenomena * MeSH
- Mycorrhizae physiology MeSH
- Plants microbiology MeSH
- Symbiosis * MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
Plant colonization of islands may be limited by the availability of symbionts, particularly arbuscular mycorrhizal (AM) fungi, which have limited dispersal ability compared to ectomycorrhizal and ericoid (EEM) as well as orchid mycorrhizal (ORC) fungi. We tested for such differential island colonization within contemporary angiosperm floras worldwide. We found evidence that AM plants experience a stronger mycorrhizal filter than other mycorrhizal or non-mycorrhizal (NM) plant species, with decreased proportions of native AM plant species on islands relative to mainlands. This effect intensified with island isolation, particularly for non-endemic plant species. The proportion of endemic AM plant species increased with island isolation, consistent with diversification filling niches left open by the mycorrhizal filter. We further found evidence of humans overcoming the initial mycorrhizal filter. Naturalized floras showed higher proportions of AM plant species than native floras, a pattern that increased with increasing isolation and land-use intensity. This work provides evidence that mycorrhizal fungal symbionts shape plant colonization of islands and subsequent diversification.
Czech Academy of Sciences Průhonice Czech Republic
German Centre for Integrative Biodiversity Research Leipzig Germany
University of Durham Durham UK
University of Gottingen Göttingen Germany
University of Kansas Lawrence USA
University of Konstanz Konstanz Germany
See more in PubMed
MacArthur, R. H. & Wilson, E. The theory of Island Biogeography. (Princeton University Press, 1967).
Losos JB, Schluter D. Analysis of an evolutionary species–area relationship. Nature. 2000;408:847. doi: 10.1038/35048558. PubMed DOI
Kisel Y, Barraclough TG. Speciation has a spatial scale that depends on levels of gene flow. Am. Nat. 2010;175:316–334. doi: 10.1086/650369. PubMed DOI
Losos, J. B. & Ricklefs, R. E. The Theory Of Island Biogeography Revisited. (Princeton University Press, 2009).
Onstein RE, et al. Frugivory-related traits promote speciation of tropical palms. Nat. Ecol. Evol. 2017;1:1903. doi: 10.1038/s41559-017-0348-7. PubMed DOI
Bush, M. B. & Whittaker, R. J. Krakatau: colonization patterns and hierarchies. J. Biogeogr.18, 341–356 (1991).
Fukami T. Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu. Rev. Ecol. Evol. Syst. 2015;46:1–23. doi: 10.1146/annurev-ecolsys-110411-160340. DOI
Hoeksema JD, et al. Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism. Commun. Biol. 2018;1:116. doi: 10.1038/s42003-018-0120-9. PubMed DOI PMC
Duchicela J, Bever JD, Schultz PA. Symbionts as filters of plant colonization of islands: tests of expected patterns and environmental consequences in the galapagos. Plants. 2020;9:74. doi: 10.3390/plants9010074. PubMed DOI PMC
Delavaux CS, et al. Mycorrhizal fungi influence global plant biogeography. Nat. Ecol. Evol. 2019;3:424. doi: 10.1038/s41559-019-0823-4. PubMed DOI
Chaudhary, V. B., Nolimal, S., Sosa‐Hernández, M. A., Egan, C. & Kastens, J. Trait‐based aerial dispersal of arbuscular mycorrhizal fungi. New Phytol.228, 238–252 (2020). PubMed
Smith, S. E. & Read, D. J. Mycorrhizal Symbiosis (Academic press, 2008).
Oneto DL, Golan J, Mazzino A, Pringle A, Seminara A. Timing of fungal spore release dictates survival during atmospheric transport. Proc. Natl Acad. Sci. USA. 2020;117:5134–5143. doi: 10.1073/pnas.1913752117. PubMed DOI PMC
Roper M, Pepper RE, Brenner MP, Pringle A. Explosively launched spores of ascomycete fungi have drag-minimizing shapes. Proc. Natl Acad. Sci. USA. 2008;105:20583–20588. doi: 10.1073/pnas.0805017105. PubMed DOI PMC
Shah F, et al. Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors. New Phytol. 2016;209:1705–1719. doi: 10.1111/nph.13722. PubMed DOI PMC
Read DJ, Perez-Moreno J. Mycorrhizas and nutrient cycling in ecosystems- a journey towards relevance? New Phytol. 2003;157:475–492. doi: 10.1046/j.1469-8137.2003.00704.x. PubMed DOI
Martino E, et al. Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists. New Phytol. 2018;217:1213–1229. doi: 10.1111/nph.14974. PubMed DOI
McCORMICK MK, et al. Limitations on orchid recruitment: not a simple picture. Mol. Ecol. 2012;21:1511–1523. doi: 10.1111/j.1365-294X.2012.05468.x. PubMed DOI
Selosse MA, et al. Saprotrophic fungal symbionts in tropical achlorophyllous orchids: finding treasures among the ‘molecular scraps’? Plant Signal. Behav. 2010;5:349–353. doi: 10.4161/psb.5.4.10791. PubMed DOI PMC
Smith GR, Finlay RD, Stenlid J, Vasaitis R, Menkis A. Growing evidence for facultative biotrophy in saprotrophic fungi: data from microcosm tests with 201 species of wood‐decay basidiomycetes. New Phytol. 2017;215:747–755. doi: 10.1111/nph.14551. PubMed DOI
Lindahl BD, Tunlid A. Ectomycorrhizal fungi–potential organic matter decomposers, yet not saprotrophs. New Phytol. 2015;205:1443–1447. doi: 10.1111/nph.13201. PubMed DOI
Peay KG, Schubert MG, Nguyen NH, Bruns TD. Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol. Ecol. 2012;21:4122–4136. doi: 10.1111/j.1365-294X.2012.05666.x. PubMed DOI
Pither J, Pickles BJ, Simard SW, Ordonez A, Williams JW. Below‐ground biotic interactions moderated the postglacial range dynamics of trees. New Phytol. 2018;220:1148–1160. doi: 10.1111/nph.15203. PubMed DOI
van der Heijden MG, Martin FM, Selosse MA, Sanders IR. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol. 2015;205:1406–1423. doi: 10.1111/nph.13288. PubMed DOI
Chaudhary VB, et al. MycoDB, a global database of plant response to mycorrhizal fungi. Sci. Data. 2016;3:160028. doi: 10.1038/sdata.2016.28. PubMed DOI PMC
Pyšek P, et al. Facultative mycorrhizal associations promote plant naturalization worldwide. Ecosphere. 2019;10:e02937. doi: 10.1002/ecs2.2937. DOI
Phillips RP, Brzostek E, Midgley MG. The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. New Phytol. 2013;199:41–51. doi: 10.1111/nph.12221. PubMed DOI
Steidinger B, et al. Climatic controls of decomposition drive the global biogeography of forest-tree symbioses. Nature. 2019;569:404. doi: 10.1038/s41586-019-1128-0. PubMed DOI
Bueno CG, et al. Plant mycorrhizal status, but not type, shifts with latitude and elevation in Europe. Glob. Ecol. Biogeogr. 2017;26:690–699. doi: 10.1111/geb.12582. DOI
Cameron DD, Leake JR, Read DJ. Mutualistic mycorrhiza in orchids: evidence from plant–fungus carbon and nitrogen transfers in the green‐leaved terrestrial orchid Goodyera repens. New Phytol. 2006;171:405–416. doi: 10.1111/j.1469-8137.2006.01767.x. PubMed DOI
Dearnaley JD. Further advances in orchid mycorrhizal research. Mycorrhiza. 2007;17:475–486. doi: 10.1007/s00572-007-0138-1. PubMed DOI
Davison J, et al. Microbial island biogeography: isolation shapes the life history characteristics but not diversity of root-symbiotic fungal communities. ISME J. 2018;12:2211–2224. doi: 10.1038/s41396-018-0196-8. PubMed DOI PMC
Koziol L, Bever JD. Mycorrhizal feedbacks generate positive frequency dependence accelerating grassland succession. J. Ecol. 2019;107:622–632. doi: 10.1111/1365-2745.13063. DOI
Tedersoo L, et al. Global diversity and geography of soil fungi. Science. 2014;346:1256688. doi: 10.1126/science.1256688. PubMed DOI
Koziol, L. et al. The plant microbiome and native plant restoration: the example of native mycorrhizal fungi. BioScience68, 996–1006 (2018).
Lu M, Hedin LO. Global plant–symbiont organization and emergence of biogeochemical cycles resolved by evolution-based trait modelling. Nat. Ecol. Evol. 2019;3:239. doi: 10.1038/s41559-018-0759-0. PubMed DOI
Zotz G. The systematic distribution of vascular epiphytes–a critical update. Bot. J. Linn. Soc. 2013;171:453–481. doi: 10.1111/boj.12010. DOI
Zotz G. Vascular epiphytes in the temperate zones–a review. Plant Ecol. 2005;176:173–183. doi: 10.1007/s11258-004-0066-5. DOI
Taylor A, Weigelt P, König C, Zotz G, Kreft H. Island disharmony revisited using orchids as a model group. New Phytol. 2019;223:597–606. doi: 10.1111/nph.15776. PubMed DOI
Razanajatovo M, et al. Autofertility and self‐compatibility moderately benefit island colonization of plants. Glob. Ecol. Biogeogr. 2019;28:341–352. doi: 10.1111/geb.12854. DOI
van Kleunen M, et al. The Global Naturalized Alien Flora (Glo NAF) database. Ecology. 2019;100:e02542. doi: 10.1002/ecy.2542. PubMed DOI
Pysek P, et al. Naturalized alien flora of the world: species diversity, taxonomic and phylogenetic patterns, geographic distribution and global hotspots of plant invasion. Preslia. 2017;89:203–274. doi: 10.23855/preslia.2017.203. DOI
Weigelt P, König C, Kreft H. GIFT–A global inventory of floras and traits for macroecology and biogeography. J. Biogeogr. 2020;47:16–43. doi: 10.1111/jbi.13623. DOI
Kalwij JM. Review of ‘The Plant List, a working list of all plant species’. J. Veg. Sci. 2012;23:998–1002. doi: 10.1111/j.1654-1103.2012.01407.x. DOI
Byng JW, et al. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot. J. Linn. Soc. 2016;181:1–20. doi: 10.1111/boj.12385. DOI
Maherali H, et al. Mutualism persistence and abandonment during the evolution of the mycorrhizal symbiosis. Am. Nat. 2016;188:E113–E125. doi: 10.1086/688675. PubMed DOI
Brundrett MC. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil. 2009;320:37–77. doi: 10.1007/s11104-008-9877-9. DOI
Gerdemann J. Vesicular-arbuscular mycorrhiza and plant growth. Annu. Rev. Phytopathol. 1968;6:397–418. doi: 10.1146/annurev.py.06.090168.002145. DOI
Bueno CG, Gerz M, Zobel M, Moora M. Conceptual differences lead to divergent trait estimates in empirical and taxonomic approaches to plant mycorrhizal trait assignment. Mycorrhiza. 2018;29:1–11. doi: 10.1007/s00572-018-0869-1. PubMed DOI
Brundrett, M. C. & Tedersoo, L. Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol.220, 1108–1115(2018). PubMed
Vrålstad, T. Are ericoid and ectomycorrhizal fungi part of a common guild? New Phytol. 164, 7–10 (2004). PubMed
Vrålstad T, Fossheim T, Schumacher T. Piceirhiza bicolorata–the ectomycorrhizal expression of the Hymenoscyphus ericae aggregate? New Phytol. 2000;145:549–563. doi: 10.1046/j.1469-8137.2000.00605.x. PubMed DOI
Karger DN, et al. Climatologies at high resolution for the earth’s land surface areas. Sci. Data. 2017;4:170122. doi: 10.1038/sdata.2017.122. PubMed DOI PMC
Danielson, J. J. & Gesch, D. B. Global multi-resolution terrain elevation data 2010 (GMTED2010). Report No. 2331-1258, (US Geological Survey, 2011).
Center for International Earth Science Information Network - CIESIN - Columbia University, U. N. F. a. A. P.-F., and Centro Internacional de Agricultura Tropical - CIAT. Gridded Population of the World, Version 3 (GPWv3): Population Count Grid. Palisades, NY: NASA Socioeconomic Data and Applications Center (SEDAC). (2005).
Tuanmu MN, Jetz W. A global 1‐km consensus land‐cover product for biodiversity and ecosystem modelling. Glob. Ecol. Biogeogr. 2014;23:1031–1045. doi: 10.1111/geb.12182. DOI
Weigelt P, Kreft H. Quantifying island isolation–insights from global patterns of insular plant species richness. Ecography. 2013;36:417–429. doi: 10.1111/j.1600-0587.2012.07669.x. DOI
Kreft H, Jetz W, Mutke J, Kier G, Barthlott W. Global diversity of island floras from a macroecological perspective. Ecol. Lett. 2008;11:116–127. PubMed
Triantis KA, Economo EP, Guilhaumon F, Ricklefs RE. Diversity regulation at macro‐scales: species richness on oceanic archipelagos. Glob. Ecol. Biogeogr. 2015;24:594–605. doi: 10.1111/geb.12301. DOI
Crase B, Liedloff AC, Wintle BA. A new method for dealing with residual spatial autocorrelation in species distribution models. Ecography. 2012;35:879–888. doi: 10.1111/j.1600-0587.2011.07138.x. DOI
Bivand RS, Wong DWS. Comparing implementations of global and local indicators of spatial association. TEST. 2018;27:716–748. doi: 10.1007/s11749-018-0599-x. DOI
R Core Team. R: A Language And Environment For Statistical Computing (R Foundation for Statistical Computing, 2019).
Bates D, Maechler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 2015;67:1–48. doi: 10.18637/jss.v067.i01. DOI
Delavaux, C. et al. Mycorrhizal Types Influence Island Biogeography of Plants: associated data. Zenodo10.5281/zenodo.5179626 (2021). PubMed PMC
Mycorrhizal types influence island biogeography of plants