[en] Arbuscular mycorrhizal fungi (AMF) are amongst the most studied obligate plant
symbionts and regularly found in terrestrial plants. However, global estimates of AMF
abundance amongst all land plants are difficult because i) the mycorrhizal status of
many non-commercial, wild plant species is still unknown, ii) numerous plant species
engage in facultative symbiosis, meaning that they can, but do not always do, asso-
ciate with mycorrhiza, and iii) mycorrhizal status can vary within families, genera, and
species. To gain deeper insights to the distribution of the plant-AMF symbiosis we
investigated the mycorrhizal status in some of the oldest lineages of extant vascular
plants, Polypodiophytina (ferns) and lycophytes, in one of the hotspots of natural
plant diversification, the tropical rainforest. Providing a new data set of AMF abun-
dance for 82 fern species representing 19 families, we hypothesized that (1) AMF
would be found in 60–80% of the studied plants and (2) plant species with AMF sym-
bionts would be more abundant than non-mycorrhizal species. Both hypotheses were
rejected while the following observations were made: (1) AMF occurred in 30.5% of
studied species, representing 63% of the studied fern families, (2) AMF colonisation
was not correlated with species abundance, (3) a small proportion of AMF-hosting
ferns was epiphytic (6%) and (4) mycorrhization was inconsistent among different
populations of the same species (facultative mycorrhization). While these observa-
tions align with previous studies on ferns, they emphasise that mycorrhization is not
a taxonomic trait and underscore the challenges in estimating the global abundance
of AMF. In addition, the occurrence of AMF in epiphytic plants and no net benefits of
AMF for plant abundance indicate that the mycorrhization observed in this study likely
comprises the commensalism to parasitism range of the symbiosis spectrum.
Smith SE, Read DJ. Mycorrhizal Symbiosis. Academic Press; 2010. https://doi.org/10.1016/b978-0-12-370526-6.x5001-6
Wang B, Qiu Y-L. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza. 2006;16(5):299–363. https://doi.org/10.1007/ s00572-005-0033-6 PMID: 16845554
Strullu-Derrien C, Kenrick P, Pressel S, Duckett JG, Rioult J-P, Strullu D-G. Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 million year old) closely resemble those in extant lower land plants: novel insights into ancestral plant-fungus symbioses. New Phytol. 2014;203(3):964–79. https://doi.org/10.1111/nph.12805 PMID: 24750009
Sportes A, Hériché M, Boussageon R, Noceto P-A, van Tuinen D, Wipf D, et al. A historical perspective on mycorrhizal mutualism emphasizing arbuscular mycorrhizas and their emerging challenges. Mycorrhiza. 2021;31(6):637–53. https://doi.org/10.1007/s00572-021-01053-2 PMID: 34657204
Pires ND, Dolan L. Morphological evolution in land plants: new designs with old genes. Philos Trans R Soc Lond B Biol Sci. 2012;367(1588):508–18. https://doi.org/10.1098/rstb.2011.0252 PMID: 22232763
Landeweert R, Hoffland E, Finlay RD, Kuyper TW, van Breemen N. Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends Ecol Evol. 2001;16(5):248–54. https://doi.org/10.1016/s0169-5347(01)02122-x PMID: 11301154
Cheng L, Booker FL, Tu C, Burkey KO, Zhou L, Shew HD, et al. Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science. 2012;337(6098):1084–7. https://doi.org/10.1126/science.1224304 PMID: 22936776
Finlay RD, Mahmood S, Rosenstock N, Bolou-Bi EB, Köhler SJ, Fahad Z, et al. Reviews and syntheses: Biological weathering and its consequences at different spatial levels – from nanoscale to global scale. Biogeosciences. 2020;17(6):1507–33. https://doi.org/10.5194/bg-17-1507-2020
Encyclopaedia Britannica Eds. Symbiosis. Encyclopaedia Britannica. Accessed 2023 October 24. https://www.britannica.com/science/symbiosis
Johnson NC, Graham J, Smith FA. Functioning of mycorrhizal associations along the mutualism–parasitism continuum*. New Phytologist. 1997;135(4):575–85. https://doi.org/10.1046/j.1469-8137.1997.00729.x
Purin S, Rillig MC. Parasitism of arbuscular mycorrhizal fungi: reviewing the evidence. FEMS Microbiol Lett. 2008;279(1):8–14. https://doi.org/10.1111/j.1574-6968.2007.01007.x PMID: 18070075
Ramírez-Flores MR, Perez-Limon S, Li M, Barrales-Gamez B, Albinsky D, Paszkowski U, et al. The genetic architecture of host response reveals the importance of arbuscular mycorrhizae to maize cultivation. Elife. 2020;9:e61701. https://doi.org/10.7554/eLife.61701 PMID: 33211006
Neuhauser C, Fargione JE. A mutualism–parasitism continuum model and its application to plant–mycorrhizae interactions. Ecol Model. 2004;177(3–4):337–52. https://doi.org/10.1016/j.ecolmodel.2004.02.010
Neubauer A, Aros-Mualin D, Mariscal V, Szövényi P. Challenging the term symbiosis in plant-microbe associations to create an understanding across sciences. J Integr Plant Biol. 2024;66(1):7–11. https://doi.org/10.1111/jipb.13588 PMID: 38038369
Karst J, Jones MD, Hoeksema JD. Positive citation bias and overinterpreted results lead to misinformation on common mycorrhizal networks in forests. Nat Ecol Evol. 2023;7(4):501–11. https://doi.org/10.1038/s41559-023-01986-1 PMID: 36782032
Ryan MH, Graham JH. Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops. New Phytol. 2018;220(4):1092–107. https://doi.org/10.1111/nph.15308 PMID: 29987890
Bennett AE, Classen AT. Climate change influences mycorrhizal fungal-plant interactions, but conclusions are limited by geographical study bias. Ecology. 2020;101(4):e02978. https://doi.org/10.1002/ecy.2978 PMID: 31953955
Albornoz FE, Dixon KW, Lambers H. Revisiting mycorrhizal dogmas: Are mycorrhizas really functioning as they are widely believed to do? Soil Ecol Lett. 2020;3(1):73–82. https://doi.org/10.1007/s42832-020-0070-2
Corlett RT. Plant diversity in a changing world: Status, trends, and conservation needs. Plant Divers. 2016;38(1):10–6. https://doi.org/10.1016/j.pld.2016.01.001 PMID: 30159445
Sabatini FM, Jiménez-Alfaro B, Jandt U, Chytrý M, Field R, Kessler M, et al. Global patterns of vascular plant alpha diversity. Nat Commun. 2022;13(1):4683. https://doi.org/10.1038/s41467-022-32063-z PMID: 36050293
Dudhane M, Borde M, Thomas S. Advances in AMF research: isolation, histochemical staining, enumeration, morphological and molecular techniques. In: Parihar M, Rakshit A, Adholeya A, Chen Y, ed. Arbuscular Mycorrhizal Fungi in Sustainable Agriculture: Inoculum Production and Application. Springer Nature Singapore; 2024: 37–55. https://doi.org/10.1007/978-981-97-0296-1_2
Formenti L, Iwanycki Ahlstrand N, Hassemer G, Glauser G, van den Hoogen J, Rønsted N, et al. Macroevolutionary decline in mycorrhizal colonization and chemical defense responsiveness to mycorrhization. iScience. 2023;26(5):106632. https://doi.org/10.1016/j.isci.2023.106632 PMID: 37168575
Lara-Pérez LA, Valdés-Baizabal MD, Noa-Carrazana JC, Zulueta-Rodríguez R, Lara-Capistrán L, Andrade-Torres A. Mycorrhizal associations of ferns and lycopods of central Veracruz, Mexico. Symbiosis. 2015;65(2):85–92. https://doi.org/10.1007/s13199-015-0320-8
Lehnert M, Krug M, Kessler M. A review of symbiotic fungal endophytes in lycophytes and ferns – a global phylogenetic and ecological perspective. Symbiosis. 2016;71(2):77–89. https://doi.org/10.1007/s13199-016-0436-5
Mulder C, Sand-Jensen K. The functional role of mycorrhiza in plants and the implications for ecology and conservation. J Appl Ecol. 2007;45(1):361–70. https://doi.org/10.1111/j.1365-2664.2007.01402.x
Brundrett MC, Tedersoo L. Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol. 2018;220(4):1108–15. https://doi.org/10.1111/nph.14976 PMID: 29355963
Michel J, Lehnert M, Quandt D. Elevation and cation exchange capacity determine diversity of ferns in a low-montane tropical rainforest in Ecuador. J Trop Ecol. 2023;39. https://doi.org/10.1017/s0266467423000081
Berry C. The middle Devonian plant collections of Francois Stockman reconsidered. Geologica Belgica. 2009;12(1–2):25–30.
Bomfleur B, McLoughlin S, Vajda V. Fossilized nuclei and chromosomes reveal 180 million years of genomic stasis in royal ferns. Science. 2014;343(6177):1376–7. https://doi.org/10.1126/science.1249884 PMID: 24653037
Linares-Palomino R, Cardona V, Hennig EI, Hensen I, Hoffmann D, Lendzion J. Non-woody life-form contribution to vascular plant species richness in a tropical American forest. Forest Ecol. 2009:87–99.
Chater CCC. Light in the darkness: how ferns flourished in the ancestral angiosperm forest. New Phytol. 2021;230(3):886–8. https://doi.org/10.1111/nph.17273
Pouteau R, Meyer J-Y, Blanchard P, Nitta JH, Terorotua M, Taputuarai R. Fern species richness and abundance are indicators of climate change on high-elevation islands: evidence from an elevational gradient on Tahiti (French Polynesia). Climatic Change. 2016;138(1–2):143–56. https://doi.org/10.1007/s10584-016-1734-x
Da Silva VL, Mehltreter K, Schmitt JL. Ferns as potential ecological indicators of edge effects in two types of Mexican forests. Ecol Indic. 2018;93:669–76. https://www.sciencedirect.com/science/article/abs/pii/S1470160X18303704?via%3Dihub
Richter DD, Babbar LI. Soil Diversity in the Tropics. In: Begon M, Fitter AH, Macfadyen A. Advances in Ecological Research. Academic Press; 1991: 315–89. https://doi.org/10.1016/s0065-2504(08)60100-2
Jobbágy EG, Jackson RB. The distribution of soil nutrients with depth: global patterns and the imprint of plants. Biogeochemistry. 2001;53(1):51–77. https://doi.org/10.1023/a:1010760720215
Moreno-Jiménez E, Maestre FT, Flagmeier M, Guirado E, Berdugo M, Bastida F, et al. Soils in warmer and less developed countries have less micronutrients globally. Glob Chang Biol. 2023;29(2):522–32. https://doi.org/10.1111/gcb.16478 PMID: 36305858
Hawkins BA, Field R, Cornell HV, Currie DJ, Guégan J-F, Kaufman DM, et al. Energy, water, and broad-scale geographic patterns of species richness. Ecology. 2003;84(12):3105–17. https://doi.org/10.1890/03-8006
Richter M, Diertl K-H, Emck P, Peters T, Beck E. Reasons for an outstanding plant diversity in the tropical Andes of Southern Ecuador. LO. 2009;12:1–35. https://doi.org/10.3097/lo.200912
USGS EROS. U.S. Geological Survey Earth Resources Observatory and Science (EROS) Center (public domain). 2025 [Accessed 2025 June 6]. http://eros.usgs.gov/#
PPGI. A community‐derived classification for extant lycophytes and ferns. J Syt Evol. 2016;54(6):563–603. https://doi.org/10.1111/jse.12229
Hassler M. Checklist of ferns and lycophytes of the world. In: Bánki O, Roskov Y, Döring M, Ower G, Vandepitte L, Hobern D, ed. Cat Life Checklist 14.3. 2022. https://doi.org/10.48580/dfqj-3dc
Grace C, Stribley DP. A safer procedure for routine staining of vesicular-arbuscular mycorrhizal fungi. Mycol Res. 1991;95(10):1160–2. https://doi.org/10.1016/s0953-7562(09)80005-1
R Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2024. https://www.R-project.org
Fox J, Weisberg S. An R companion to applied regression. 3 ed. Thousand Oaks CA: Sage; 2019. https://www.john-fox.ca/Companion
Wickham H. ggplot2: elegant graphics for data analysis. New York: Springer-Verlag; 2016.
Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biom J. 2008;50(3):346–63.
Smith FA, Grace EJ, Smith SE. More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol. 2009;182(2):347–58. https://doi.org/10.1111/j.1469-8137.2008.02753.x PMID: 19207688
Zeng K, Huang D, Zhang X, Liu S, Huang X, Xin G. Fern species and seasonal variation alter arbuscular mycorrhizal fungal colonization and co-occurrence patterns in the Heishiding Natural Reserve, South China. Appl Soil Ecol. 2024;193:105172. https://doi.org/10.1016/j.apsoil.2023.105172
Tedersoo L, Nilsson RH, Abarenkov K, Jairus T, Sadam A, Saar I, et al. 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytol. 2010;188(1):291–301. https://doi.org/10.1111/j.14698137.2010.03373.x PMID: 20636324
Troudet J, Grandcolas P, Blin A, Vignes-Lebbe R, Legendre F. Taxonomic bias in biodiversity data and societal preferences. Sci Rep. 2017;7(1):9132. https://doi.org/10.1038/s41598-017-09084-6 PMID: 28831097
Lehnert M, Kessler M. Mycorrhizal relationships in Lycophytes and ferns. Fern Gaz. 2016;20(3):101–16.
Lehnert M, Kottke I, Setaro S, Pazmiño LF, Suárez JP, Kessler M. Mycorrhizal Associations in Ferns from Southern Ecuador. Am Fern J. 2009;99(4):292–306. https://doi.org/10.1640/0002-8444-99.4.292
Watkins JE Jr, Cardelús CL. Ferns in an Angiosperm World: Cretaceous Radiation into the Epiphytic Niche and Diversification on the Forest Floor. Int J Plant Sci. 2012;173(6):695–710. https://doi.org/10.1086/665974
Guillen-Otero T, Lee S-J, Hertel D, Kessler M. Facultative mycorrhization in a fern (Struthiopteris spicant L. Weiss) is bound to light intensity. BMC Plant Biol. 2024;24(1):103. https://doi.org/10.1186/s12870-024-04782-6 PMID: 38331718
West B, Brandt J, Holstien K, Hill A, Hill M. Fern-associated arbuscular mycorrhizal fungi are represented by multiple Glomus spp.: do environmental factors influence partner identity? Mycorrhiza. 2009;19(5):295–304. https://doi.org/10.1007/s00572-009-0234-5 PMID: 19242733
Lee E-H, Eo J-K, Ka K-H, Eom A-H. Diversity of arbuscular mycorrhizal fungi and their roles in ecosystems. Mycobiology. 2013;41(3):121–5. https://doi.org/10.5941/MYCO.2013.41.3.121 PMID: 24198665
Guillen T, Kessler M, Homeier J. Fern mycorrhizae do not respond to fertilization in a tropical montane forest. Plant Environ Interact. 2024;5(2):e10139. https://doi.org/10.1002/pei3.10139 PMID: 38560414
Kessler M, Jonas R, Strasberg D, Lehnert M. Mycorrhizal colonizations of ferns and lycophytes on the island of La Réunion in relation to nutrient availability. Basic Appl Ecol. 2010;11(4):329–36. https://doi.org/10.1016/j.baae.2010.01.002
Nadkarni NM, Matelson TJ. Fine litter dynamics within the tree canopy of a tropical cloud forest. Ecology. 1991;72(6):2071–82. https://doi.org/10.2307/1941560
Bothe H, Turnau K, Regvar M. The potential role of arbuscular mycorrhizal fungi in protecting endangered plants and habitats. Mycorrhiza. 2010;20(7):445–57. https://doi.org/10.1007/s00572-010-0332-4 PMID: 20652364
Snäll T, Ehrlén J, Rydin H. Colonization–extinction dynamics of an epiphyte metapopulation in a dynamic landscape. Ecology. 2005;86(1):106–15. https://doi.org/10.1890/04-0531
Dubuisson J-Y, Schneider H, Hennequin S. Epiphytism in ferns: diversity and history. C R Biol. 2009;332(2–3):120–8. https://doi.org/10.1016/j.crvi.2008.08.018 PMID: 19281945
Querejeta JI, Egerton-Warburton LM, Allen MF. Direct nocturnal water transfer from oaks to their mycorrhizal symbionts during severe soil drying. Oecologia. 2003;134(1):55–64. https://doi.org/10.1007/s00442-002-1078-2 PMID: 12647179
Hammer EC, Pallon J, Wallander H, Olsson PA. Tit for tat? A mycorrhizal fungus accumulates phosphorus under low plant carbon availability. FEMS Microbiol Ecol. 2011;76(2):236–44. https://doi.org/10.1111/j.1574-6941.2011.01043.x PMID: 21223336
Säle V, Palenzuela J, Azcón-Aguilar C, Sánchez-Castro I, da Silva GA, Seitz B, et al. Ancient lineages of arbuscular mycorrhizal fungi provide little plant benefit. Mycorrhiza. 2021;31(5):559–76. https://doi.org/10.1007/s00572-021-01042-5 PMID: 34327560
Engelmoer DJP, Behm JE, Toby Kiers E. Intense competition between arbuscular mycorrhizal mutualists in an in vitro root microbiome negatively affects total fungal abundance. Mol Ecol. 2014;23(6):1584–93. https://doi.org/10.1111/mec.12451 PMID: 24050702
Drigo B, Pijl AS, Duyts H, Kielak AM, Gamper HA, Houtekamer MJ, et al. Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc Natl Acad Sci U S A. 2010;107(24):10938–42. https://doi.org/10.1073/pnas.0912421107 PMID: 20534474
Barbosa MV, Pedroso D de F, Curi N, Carneiro MAC. Do different arbuscular mycorrhizal fungi affect the formation and stability of soil aggregates? Ciênc Agrotec. 2019;43. https://doi.org/10.1590/1413-7054201943003519
Camenzind T, Mason-Jones K, Mansour I, Rillig MC, Lehmann J. Formation of necromass-derived soil organic carbon determined by microbial death pathways. Nat Geosci. 2023;16(2):115–22. https://doi.org/10.1038/s41561-022-01100-3
Shabtai IA, Wilhelm RC, Schweizer SA, Höschen C, Buckley DH, Lehmann J. Calcium promotes persistent soil organic matter by altering microbial transformation of plant litter. Nat Commun. 2023;14(1):6609. https://doi.org/10.1038/s41467-023-42291-6 PMID: 37857604
McCully ME. ROOTS IN SOIL: unearthing the complexities of roots and their rhizospheres. Annu Rev Plant Physiol Plant Mol Biol. 1999;50:695–718. https://doi.org/10.1146/annurev.arplant.50.1.695 PMID: 15012224
Lekberg Y, Rosendahl S, Michelsen A, Olsson PA. Seasonal carbon allocation to arbuscular mycorrhizal fungi assessed by microscopic examination, stable isotope probing and fatty acid analysis. Plant Soil. 2012;368(1–2):547–55. https://doi.org/10.1007/s11104-012-1534-7
Nuccio EE, Blazewicz SJ, Lafler M, Campbell AN, Kakouridis A, Kimbrel JA, et al. HT-SIP: a semi-automated stable isotope probing pipeline identifies cross-kingdom interactions in the hyphosphere of arbuscular mycorrhizal fungi. Microbiome. 2022;10(1):199. https://doi.org/10.1186/s40168-022-01391-z PMID: 36434737