Abstract
Community-level studies linking plant mycorrhizal status to environment usually do not account for within-plot mycorrhizal status variability; thus, patterns of plant mycorrhizal status diversity are largely unknown. Here, we assessed the relative importance of within- and between-plot variability components in mycorrhizal status and examined how plant mycorrhizal status diversity is related to soil nutrient availability. We hypothesised larger between-plot variability in mycorrhizal status and higher plant mycorrhizal status diversity in P-poor soils. To test these hypotheses, we used plant phylogenies, vegetation, soil and plant mycorrhizal status data from Czech semi-natural grasslands and Scottish coastal habitats. We divided plant mycorrhizal status diversity into divergence and evenness and tested their relations to soil P, K, Ca and Mg. Within-plot variability component of mycorrhizal status was always, on average, at least 2.2 times larger than between-plot variability in our datasets. Plant mycorrhizal status divergence was positively related to Ca (in both datasets) and Mg (only in grasslands and when accounting for phylogeny). In grasslands, the relationship between Mg and plant mycorrhizal status evenness was negative when accounting for phylogeny, while it was positive when not accounting for phylogeny. Plant mycorrhizal status diversity was not linked to P and its relation to K was inconsistent. Our results suggest that high Ca in the soil can promote coexistence of mycorrhizal, facultatively mycorrhizal and non-mycorrhizal plant species. We encourage future studies to also focus on within-plot variability in mycorrhizal status, because it appears to be highly relevant in herbaceous systems.
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All data supporting the results are archived in the Mendeley Data depository (https://data.mendeley.com/datasets/249v8j8vz9/1).
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References
Bergmann J, Weigelt A, van der Plas F, Laughlin DC, Kuyper TW, Guerrero-Ramirez N et al (2020) The fungal collaboration gradient dominates the root economics space in plants. Sci Adv 6:eaba3756. https://doi.org/10.1126/sciadv.aba3756
Bitomský M, Pakeman RJ, Schaefer H, Klimešová J, Rūsiņa S, Lososová Z, Mládková P, Duchoslav M (2021) Mycorrhizal status is a poor predictor of the distribution of herbaceous species along the gradient of soil nutrient availability in coastal and grassland habitats. Mycorrhiza 31:577–587. https://doi.org/10.1007/s00572-021-01047-0
Bitomský M, Schaefer H, Pakeman RJ, Klimešová J, Götzenberger L, Duchoslav M (2022) Data from: Variability in mycorrhizal status of plant species is much larger within than between plots in grassland and coastal habitats. Data Mendeley Depository. https://data.mendeley.com/datasets/249v8j8vz9/1
Bocci G (2015) TR8: an R package for easily retrieving plant species traits. Methods Ecol Evol 6:347–350. https://doi.org/10.1111/2041-210X.12327
Brundrett MC (2021) Auditing data resolves systemic errors in databases and confirms mycorrhizal trait consistency for most genera and families of flowering plants. Mycorrhiza 31:671–683. https://doi.org/10.1007/s00572-021-01051-4
Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220:1108–1115. https://doi.org/10.1111/nph.14976
Brundrett MC, Tedersoo L (2019) Misdiagnosis of mycorrhizas and inappropriate recycling of data can lead to false conclusions. New Phytol 221:1108–1115. https://doi.org/10.1111/nph.15440
Bueno CG, Moora M, Gerz M, Davison J, Öpik M, Pärtel M et al (2017) Plant mycorrhizal status, but not type, shifts with latitude and elevation in Europe. Glob Ecol Biogeogr 26:690–699. https://doi.org/10.1111/geb.12582
Bueno CG, Aldrich-Wolfe L, Chaudhary VB, Gerz M, Helgason T, Hoeksema JD et al (2019a) Misdiagnosis and uncritical use of plant mycorrhizal data are not the only elephants in the room. New Phytol 224:1415–1418. https://doi.org/10.1111/nph.15976
Bueno CG, Gerz M, Zobel M, Moora M (2019b) Conceptual differences lead to divergent trait estimates in empirical and taxonomic approaches to plant mycorrhizal trait assignment. Mycorrhiza 29:1–11. https://doi.org/10.1007/s00572-018-0869-1
Bueno CG, Gerz M, Moora M, Leon D, Gomez-Garcia D, García de Leon D, Font X, Al-Quraishy S, Hozzein WN, Zobel M (2021) Distribution of plant mycorrhizal traits along an elevational gradient does not fully mirror the latitudinal gradient. Mycorrhiza 31:149–159. https://doi.org/10.1007/s00572-020-01012-3
Cosme M, Fernández I, van der Heijden MGA, Pieterse CMJ (2018) Non-mycorrhizal plants: the exceptions that prove the rule. Trends Plant Sci 23:577–587. https://doi.org/10.1016/j.tplants.2018.04.004
Craine JM (2009) Resource strategies of wild plants. Princeton, New Jersey, USA. https://doi.org/10.1515/9781400830640
de Bello F, Carmona CP, Lepš J, Szava-Kovats R, Pärtel M (2016) Functional diversity through the mean trait dissimilarity: resolving shortcomings with existing paradigms and algorithms. Oecologia 180:933–940. https://doi.org/10.1007/s00442-016-3546-0
de Bello F, Šmilauer P, Diniz-Filho JAF, Carmona CP, Lososová Z, Herben T, Götzenberger L (2017) Decoupling phylogenetic and functional diversity to reveal hidden signals in community assembly. Methods Ecol Evol 8:1200–1211. https://doi.org/10.1111/2041-210X.12735
Duarte LDS, Debastiani VJ, Carlucci MB, Diniz-Filho JAF (2018) Analyzing community-weighted trait means across environmental gradients: should phylogeny stay or should it go? Ecology 99:385–398. https://doi.org/10.1002/ecy.2081
Fritz SA, Purvis A (2010) Selectivity in mammalian extinction risk and threat types: a new measure of phylogenetic signal strength in binary traits. Conserv Biol 24:1042–1051. https://doi.org/10.1111/j.1523-1739.2010.01455.x
Gallagher RV, Leishman MR (2012) Contrasting patterns of trait-based community assembly in lianas and trees from temperate Australia. Oikos 121:2026–2035. https://doi.org/10.1111/j.1600-0706.2012.20025.x
Garcia K, Zimmermann SD (2014) The role of mycorrhizal associations in plant potassium nutrition. Front Plant Sci 5:337. https://doi.org/10.3389/fpls.2014.00337
Gerz M, Bueno CG, Zobel M, Moora M (2016) Plant community mycorrhization in temperate forests and grasslands: relations with edaphic properties and plant diversity. J Veg Sci 27:89–99. https://doi.org/10.1111/jvs.12338
Gerz M, Bueno CG, Ozinga WA, Zobel M, Moora M (2019) Responses of plant community mycorrhization to anthropogenic influence depend on the habitat and mycorrhizal type. Oikos 128:1565–1575. https://doi.org/10.1111/oik.06272
Hartnett DC, Wilson GWT (2002) The role of mycorrhizas in plant community structure and dynamics: lessons from grasslands. Plant Soil 244:319–331. https://doi.org/10.1023/A:1020287726382
Hempel S, Götzenberger L, Kühn I, Michalski SG, Rillig MC, Zobel M, Moora M (2013) Mycorrhizas in the Central European flora: relationships with plant life history traits and ecology. Ecology 94:1389–1399
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. https://doi.org/10.1093/bioinformatics/btq166
Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103. https://doi.org/10.1016/j.tree.2007.10.008
Lambers H, Albornoz F, Kotula L, Laliberté E, Ranathunge K, Teste FP, Zemunik G (2018) How belowground interactions contribute to the coexistence of mycorrhizal and non-mycorrhizal species in severely phosphorus-impoverished hyperdiverse ecosystems. Plant Soil 424:11–33. https://doi.org/10.1007/s11104-017-3427-2
Lavorel S, Grigulis K, McIntyre S, Williams NSG, Garden D, Dorrough J et al (2008) Assessing functional diversity in the field – methodology matters! Funct Ecol 22:134–147. https://doi.org/10.1111/j.1365-2435.2007.01339.x
Li L, Tilman D, Zhang F (2014) Plant diversity and over yielding: insights from belowground facilitation of intercropping in agriculture. New Phytol 203:63–69. https://doi.org/10.1111/nph.12778
Mason NWH, Mouillot D, Lee WG, Wilson B (2005) Functional richness, functional evenness and functional divergence: the primary components of functional diversity. Oikos 111:112–118. https://doi.org/10.1111/j.0030-1299.2005.13886.x
Mehlich A (1984) Mehlich no 3 soil test extractant: A modification of Mehlich no 2 extractant. Commun Soil Sci Plant Anal 15:1409–1416
Menzel A, Hempel S, Manceur AM, Götzenberger L, Moora M, Rillig MC, Zobel M, Kühn I (2016) Distribution patterns of arbuscular mycorrhizal and non-mycorrhizal plant species in Germany. Perspect Plant Ecol, Evol Syst 21:78–88. https://doi.org/10.1016/j.ppees.2016.06.002
Moora M (2014) Mycorrhizal traits and plant communities: perspectives for integration. J Veg Sci 25:1126–1132. https://doi.org/10.1111/jvs.12177
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D et al. (2019) Vegan: community ecology package. R package version 2.5–6. https://CRAN.R-project.org/package=vegan
Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W (2018) Caper: Comparative analyses of phylogenetics and evolution in R. R package version 1.0.1. https://CRAN.R-project.org/package=caper
Pakeman RJ, Alexander J, Beaton J, Brooker R, Cummins R, Eastwood A et al (2015) Species composition of coastal dune vegetation in Scotland has proved resistant to climate change over a third of a century. Glob Change Biol 21:3738–3747. https://doi.org/10.1111/gcb.12999
Pakeman RJ, Hewison RL, Lewis RJ (2017) Drivers of species richness and compositional change in Scottish coastal vegetation. Appl Veg Sci 20:183–193. https://doi.org/10.1111/avsc.12283
Park DS, Worthington S, Xi Z (2018) Taxon sampling effects on the quantification and comparison of community phylogenetic diversity. Mol Ecol 27:1296–1308. https://doi.org/10.1111/mec.14520
Peat HJ, Fitter AH (1993) The distribution of arbuscular mycorrhizas in the British flora. New Phytol 125:845–854. https://doi.org/10.1111/j.1469-8137.1993.tb03933.x
Peres-Neto PR, Dray S, ter Braak JF (2017) Linking trait variability to the environment: critical issues with community-weighted mean correlation resolved by the fourth-corner approach. Ecography 40:806–816. https://doi.org/10.1111/ecog.02302
Pescador DS, de Bello F, Valladares F, Escudero A (2015) Plant trait variability along an altitudinal gradient in Mediterranean high mountain grasslands: controlling the species turnover effect. PLoS ONE 10:e0118876. https://doi.org/10.1371/journal.pone.0118876
Peterson BG, Carl P (2020). Performance analytics: econometric tools for performance and risk analysis. R package version 2.0.4. https://CRAN.Rproject.org/package=PerformanceAnalytics
R Core Team (2019) R: A language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria. https://www.R-project.org/
Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391
Scheloske S, Maetz M, Schneider T, Hildebrandt U, Bothe H, Povh B (2004) Element distribution in mycorrhizal and nonmycorrhizal roots of the halophyte Aster tripolium determined by proton induced X-ray emission. Protoplasma 223:183–189. https://doi.org/10.1007/s00709-003-0027-1
Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, London, UK
Soudzilovskaia NA, Vaessen S, Barcelo M, He J, Rahimlou S, Abarenkov K et al (2020) Fungal root: global online database of plant mycorrhizal associations. New Phytol 227:955–966. https://doi.org/10.1111/nph.16569
Swenson NG (2014) Functional and phylogenetic ecology in R. Springer, New York, USA
van der Heijden MGA, Scheublin TR (2007) Functional traits in mycorrhizal ecology: their use for predicting the impact of arbuscular mycorrhizal fungal communities on plant growth and ecosystem functioning. New Phytol 174:244–250. https://doi.org/10.1111/j.1469-8137.2007.02041.x
Wang Y, Naumann U, Wright ST, Warton DI (2012) mvabund – an R package for model-based analysis of multivariate abundance data. Methods Ecol Evol 3:471–474. https://doi.org/10.1111/j.2041-210X.2012.00190.x
Zemunik G, Turner BL, Lambers H, Laliberté E (2015) Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nat Plants 1:15050. https://doi.org/10.1038/NPLANTS.2015.50
Acknowledgements
We are grateful to Pavla Mládková, Kamil Maralík and Clémence Chaudron for their help with data collecting. The clarity of the manuscript was substantially improved thanks to the suggestions of two anonymous reviewers.
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This work was supported by Ministry of Education, Youth and Sports of the Czech Republic (INTER-EXCELLENCE, LTC18056, COST action 16212), Palacký University in Olomouc (IGA_PrF_2020_020) and long-term research development project of the Czech Academy of Sciences (RVO 67985939). MB was supported by the Scholarship of the city of Ostrava. RJP was supported by the Strategic Research Programme of the Scottish Government’s Rural and Environment Science and Analytical Services Division.
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MB conceived the ideas and led writing of the manuscript. MB and RJP designed the study and collected the data. MB analysed the data with help from HS. All authors discussed the results, contributed critically to the drafts and gave final approval for publication.
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Communicated by Melinda D. Smith.
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Bitomský, M., Schaefer, H., Pakeman, R.J. et al. Variability in mycorrhizal status of plant species is much larger within than between plots in grassland and coastal habitats. Oecologia 200, 209–219 (2022). https://doi.org/10.1007/s00442-022-05262-0
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DOI: https://doi.org/10.1007/s00442-022-05262-0