Temporal variation of macrofungal communities in forest stands afforested on former agricultural land
DOI:
https://doi.org/10.15287/afr.2026.4230Keywords:
afforested agricultural land, macromycetes, Picea abies, temporal variabilityAbstract
Our study aimed to assess inter-annual (2016–2020) temporal variability in macromycete species richness, diversity, abundance, and community composition for saprotrophic (SAP) and ectomycorrhizal (ECM) fungi in Norway spruce-dominated stands of different ages (21, 31 and 51 years; a proxy for succession) afforested on former agricultural land (locality Vrchdobroč, central Slovakia). We observed significant inter-annual variability in macromycete species richness, diversity, and abundance, depending on ecotrophic fungal groups. Year had a greater influence than fungal group on all characteristics except species richness, where both factors had similar importance. Stand age affected only macromycete abundance, with differences between ecotrophic groups. The models explained more variability in species richness and abundance than in diversity. Inter-annual variability in fungal community composition exceeded the variability attributable to stand age, with ECM macromycete communities exhibiting greater inter-annual variability than SAP macromycete communities. No direct interaction effects between stand age and sampling year were detected, suggesting that macromycete communities may be shaped by processes operating at broader spatial or temporal scales than those captured by the study plots (416.16 m2) and sampling period. Consequently, in short-term studies, high inter-annual variability in macromycete species richness, diversity, abundance, and community composition could obscure the influence of other factors of interest.
References
Adamczyk J. 2011. Applications of self-organizing map for patterning macrofungal diversity of xerothermic swards. Ecol. Res. 26, 547–554. https://doi.org/10.1007/s11284-011-0812-9
Arnolds E., Downes R. and Somhost I. 2004. Mycologische avonturen in jonge sparrenbosjes op voormalige landbouwgrond. Coolia, 47, 56–64.
Bahram M., Peay K.G. and Tedersoo L. 2015. Local-scale biogeography and spatiotemporal variability in communities of mycorrhizal fungi. New Phytologist, 205, 1454–1463. https://doi.org/10.1111/nph.13206
Bartoń K. 2022. MuMIn: Multi-Model Inference. R package version 1.47.1. https://CRAN.R-project.org/package=MuMIn.Bates et al. 2015
Bates D., Maechler M., Bolker B. and Walker S. 2015. Fitting linear mixed-effects models using lme4. J Stat Soft 67(1), 1–48. https://doi.org/10.48550/arXiv.1406.5823
Bonet J.A., Fischer C.R. and Colinas C. 2004. The relationship between forest age and aspect on the production of sporocarps of ectomycorrhizal fungi in Pinus sylvestris forests of the central Pyrenees. Forest Ecology and Management, 203, 157–175. https://doi.org/10.1016/j.foreco.2004.07.063
Brooks M.E., Kristensen K., Van Benthem K.J., Magnusson A., Berg C.W., Nielsen A., Skaug H.J., Maechler M. and Bolker B.M. 2017. glmmTMB Balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal, 9, 378–400. https://doi.org/10.32614/RJ-2017-066
Buée M., Maurice J.P., Zeller B., Andrianarisoa S., Ranger J., Courtecuisse R., Marcais B. and Le Tacon F. 2011. Influence of tree species on richness and diversity of epigeous fungal communities in a French temperate forest stand. Fungal Ecolopgy, 4, 22–31. https://doi.org/10.1016/j.funeco.2010.07.003
Burke D.J., Lopez-Guttierez J.C., Smemo K.A. and Chan C.R. 2009. Vegetation and soil environment influence the spatial distribution of root associated fungi in a mature beech-maple forest. Applied Environmental Microbiology, 75, 7639–7648.
Cooper J. and Kirk P. 2024). The Index Fungorum Partnership. Retrieved from http://www.indexfungorum.org/Names/Names.asp Accessed 16 February 2024.
De Cáceres M.D. and Legendre P. 2009. Associations between species and groups of sites: indices and statistical inference. Ecology, 90, 3566–3574. https://doi.org/10.1890/08-1823.1
Duncan R.P. and Kefford B.J. 2021. Interactions in statistical models: three things to know. Methods in Ecology and Evolution, 12, 2287–2297. https://doi.org/10.1111/2041-210X.13714
Egli S. 2011. Mycorrhizal mushroom diversity and productivity—an indicator of forest health? Annals of Forest Science, 68, 81–88. https://doi.org/10.1007/s13595-010-0009-3
Fox J. and Weisberg S. 2019. An R companion to applied regression. Sage, Thousand Oaks.
Gáper J. 1992. Changes in occurrence ofmycorrhizal fungi during spruce forest stand development. In: Forest – Wood - Ecology, Proceedings, TU Zvolen, pp. 199–203.
Gáper J. 1994. Temporal dynamics of macrofungi during Norway spruce stand development. Acta Facultatis Ecologiae Zvolen, 1, 99–108.
Gáper J. and Lizoň P. 1995. Sporocarp succession of mycorrhizal fungi in Norway spruce plantations in formerly agricultural land. In: Baluška F. (ed.) Structure and function of roots. Proceedings of the Fourth International Symposium on Structure and Function of Roots. Kluwer, Dordrecht, Boston, pp. 349–352.
Gáper J. and Lizoň P. 1997. Colonisation of Norway spruce plantations by ectomycorrhizal macrofungi. Ekologia (Bratislava), 16, 337–344.
Gáper J. and Mihál I. 2008. Ectomycorrhizal potential and rot in man–made forests. Acta Faultatis Ecologiae Zvolen, 18, 21–25.
Gere R., Kočiš M., Židó J., Gömöry D. and Gömöryová E. 2022. Differential Effects of Tree Species on Soil Microbiota 45 Years after Afforestation of Former Pastures. Diversity, 14, 515. https://doi.org/10.3390/d14070515
Gryndler M., Baláž M., Hršelová H., Jansa J. and Vosátka M. 2004. Mycorrhizal symbiosis – the coexistence of fungi with plant roots. Academia, Praha, 366 pp.
Gulden G., Hoilnad K., Bendiksen K., Brandrund T.E., Foss B.E., Jensenn H.B. and Laber D. 1992. Macromycetes and air pollution. Bibliotheca Mycologica, 144, 1–71.
Halme P. and Kotiaho J.S. 2012. The importance of timing and number of surveys in fungal biodiversity research. Biodiversity Conservation, 21, 205–219. https://doi.org/10.1007/s10531-011-0176-z
Hartig F. 2022. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level / Mixed Regression Models. R package version 0.4.6. http://florianhartig.github.io/DHARMa/ (accessed 31 March 2023).
Hill M.O. 1973. Diversity and evenness: a unifying notation and its consequences. Ecology 54, 427–432.
Hofmeister J., Hošek J., Brabec M., Dvořák D., Beran M., Deckerová H., Burel J., Kříž M., Borovička J., Běťák J. and Vašutová M. 2014. Richness of ancient forest plant species indicates suitable habitats for macrofungi. Biodiversity Conservation, 23, 2015–2031. https://doi.org/10.1007/s10531-014-0701-y
Jonsson L., Dahlberg A. and Brandrud E. 2000. Spatiotemporal distribution of an ectomycorrhizal community in an oligotrophic Swedish Picea abies forest subjected to experimental nitrogen addition: aboveand below ground views. Forest Ecology and Management, 132, 143–156. https://doi.org/10.1016/S0378-1127(99)00220-0
Kałucka I.L. 2009. Macrofungi in the secondary succession on the abandoned farmland near the Białowieża old- growth forest. Monografia Botanica, 99, 1–155.
Klavina D., Tedersoo L., Agan A., Adamson K., Bitenieks K., Gaitnieks T. and Drenkhan R. 2022. Soil fungal communities in young Norway spruce-dominant stands: footprints of former land use and selective thinning. European Journal of Forest Research, 141, 503–516. https://doi.org/10.1007/s10342-022-01454-8
Kuo M. 2024. Mushroomexpert.com homepage. Retrieved from www.mushroomexpert.com/index.html. Accessed 16 February 2024
Kwon T. and Tsuyuzaki S. 2016. Differences in nitrogen redistribution between early and late plant colonizers through ectomycorrhizal fungi on the volcano Mount Koma. Ecological Research, 31, 557–567. https://doi.org/10.1007/s11284-016-1364-9
Lagana A., Angiolini C., Loppi S., Salerni E., Perini C., Barluzzi C. and De Dominicis V. 2002. Periodicity, fluctuations and successions of macrofungi in fir forests (Abies alba Miller) in Tuscany, Italy. Forest Ecology and Management, 169, 187–202. https://doi.org/10.1016/S0378-1127(01)00672-7
Lenth R. 2023. emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.8.6, https://CRAN.R-project.org/package=emmeans
Lepš J. and Šmilauer P. 2003. Multivariate analysis of ecological data using Canoco. Cambridge University Press
Li D.W. 1996. The effects of Laccaria proxima and fibrous pulp waste on the growth of nine container-grown conifer seedling species. Mycorrhiza, 6, 137–143. https://doi.org/10.1007/s005720050118
Luptáková E. and Mihál I. 2018. Ectomycorrhizal macromycetes in monoculture spruce stands of different age on former agricultural land based on 2016 data. Zprávy lesnického výzkumu, 63, 195–205.
Luptáková E. Parák M. and Mihál I. 2018. Structure of fungal communities (Ascomycota, Basidiomycota) in Western Carpathians submontane forest stands under different managements. Mycosphere, 9, 1053–1072.
Luptáková E. and Mihál I. 2020. Dynamics of ectomycorrhizal mycobiota (Basidiomycota) communities on a former agricultural land (West Carpathians). Mycological Progress, 19, 845–857. https://doi.org/10.1007/s11557-020-01597-1
Mihál I.1998. Production of fruiting bodies of saprophytic fungi in spruce monocultures planted on former arable land. Ekologia (Bratislava), 17, 152–161.
Mihál I. 2005. Macrofungi succession in differently aged Norway spruce monocultures. Folia Oecologica, 32, 103–109.
Mihál I. 2011. Contribution to the knowledge of mycoflora of the Poľana Mts (Central Slovakia). Natura Carpatica, 52, 7–16.
Mihál I. 2023. Structure of symbiotic and saprotrophic mycobiota in cultivated spruce stands. Ekologické Štúdie, 14, 52–66.
Mihál I. and Gáper J. 1995. Epigeous sporocarp production in Poľana Biosphere Reserve Norway spruce stands. Ekologia (Bratislava), suppl. 2/1995, 59–68.
Mihál I. and Luptáková E. 2016. Monitoring of the mycoflora of spruce monocultures on former non-forest soils and perspectives for further research. Životné prostredie, 50, 108–117.
Mihál I. and Luptáková E. 2018. Contribution to the knowledge of mycoflora of two forest stands with different representation of the spruce trees in the Protected Landscape Area – Biosphere Reserve Poľana Mt (central Slovakia). Natura Carpatica, 59, 25–33.
Mihál I. and Luptáková E. 2020. Dynamic of biomass production of epigeic sporocarps in monoculture spruce stands (Western Carpathians). Zprávy lesnického výzkumu, 65, 197–207.
Miyamoto T., Igarashi T. and Tkahashi K. 2000. Lignin-degrading ability of litter-decomposing basidiomycetes from Picea forests of Hokkaido. Mycoscience, 41, 105–110. https://doi.org/10.1007/BF0246431
Mueller G.M. 1992. Systematics of Laccaria (Agaricales) in the continental United States and Canada, with discussions on extralimital taxa and descriptions of extant types. Fieldiana Botany, 30, 1–158.
Oksanen J., Simpson G., Blanchet F., Kindt R., Legendre P., … and Weedon J. 2022. Vegan: community ecology package. R package version 2.6–4. https://CRAN.R-project.org/package=vegan
Peršoh D., Stolle N., Brachmann A., Begerow D. and Rambold G. 2018. Fungal guilds are evently distributed along a vertical spruce forest soil profile while individual fungi show pronounced niche partitioning. Mycological Progress, 17, 925–939. https://doi.org/10.1007/s11557-018-1405-6
Pešková V., Soukup F., Landa J. 2009. Comparison of mycobiota of diverse aged spruce stands o former agricultural soil. J For Sci 55, 452–460.
Pešková V., Lorenc F., Modlinger R. and Pokorná V. 2015. Impact of drought and stand edge on mycorrhizal density on the fine roots of Norway spruce. Annals of Forest Research, 58, 245–257. https://doi.org/10.15287/afr.2015.364
Power S.A. and Ashmore M.R. 1996. Nutrient relations and root mycorrhizal status of healthy and declining beech (Fagus sylvatica L.) in southern Britain. Water Air Soil Pollution, 86, 317–333. https://doi.org/10.1007/BF00279164
R Core Team. 2023. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Retrieved from - https://www.R-project.org/
Roswell M., Dushoff J. and Winfree R. 2021. A conceptual guide to measuring species diversity. Oikos, 130, 321–338. https://doi.org/10.1111/oik.07202
RStudio. 2023. RStudio: Integrated development for R. Version 2023.03.1-446. Retrieved from http://www.rstudio.com
Rudawska M., Leski T., Stasinska M., Karlinski L., Wilgan R. and Kujawska M. 2022. The contribution of forest reserves and managed forests to the diversity of macrofungi of different trophic groups in European mixed coniferous forest ecosystem. Forest Ecology and Management, 518, 120274, https://doi.org/10.1016/j.foreco.2022.120274
Rudolph S., Maciá-Vicente L.G., Lotz-Winter H., Shleuning M. and Piepenbring M. 2018. Temporal variation of fungal diversity in a mosaic landscape in Germany. Studies in Mycology, 89, 95–104. https://doi.org/10.1016/j.simyco.2018.01.001
Salerni E., Barbato D., Cazau C., Gardin L., Henson G., Leonardi P., Tomao A. and Perini C. 2020. Selective thinning to enhance soil biodiversity in artificial black pine stands - what happens to mushroom fruiting? Annals of Forest Research, 63, 75–90. https://doi.org/10.15287/afr.2020.2006
SHMÚ. 2019. Slovak Hydrometeorological institute, Banská Bystrica – Meteorological Station Detvianska Huta - internal data, retrieved from www.shmu.sk, accessed 20 January 2019
Stankevičiené D. and Kasparavičius J. 2007. Studies on ectomycorrhizal basidiomycete in pine forest on the Lithuania – Poland transboundary region. Acta Mycologica, 42, 59–68.
Štefančík I. and Kamenský M. 2009. Vývoj zalesňování nelesních půd na Slovensku (Development of afforestation of non-forest soils in Slovakia). In: Vacek S. et al.: Zakládání a stabilizace lesních porostů na bývalých zemědělských a degradovaných půdách (Establishment and stabilization of forest stands on former agricultural and degraded soils). Kostelec nad Černými lesy, Lesnická práce, 88, 1–784.
Tedersoo L. and Smith M.E. 2013. Lineages of ectomycorrhizal fungi revisited: Foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biology, 27, 83–99. https://doi.org/10.1016/j.fbr.2013.09.001
Ujházy K., Ujházyová M., Bučinová K., Čiliak M., Glejdura S. and Mihál I. 2018. Response of fungal and plant communities to management induced overstorey changes in montane forests of the Western Carpathians. European Journal of Forest Resarch, 137, 169–183.
Unterseher M., Westphal B., Amelang N. and Jansen F. 2012. 3,000 species and no end – species richness and community pattern of woodland macrofungi in Mecklenburg-Western Pomerania, Germany. Mycological Progress, 11, 543–554. https://doi.org/10.1007/s11557-011-0769-7
Vašutová M. 2004. Macromycetes of permanent plots in cultural forests in the Moravskoslezské Beskydy Mts. and Vsetínské vrchy hills (Czech Republic). Czech Mycology, 56, 259–289. https://doi.org/10.33585/cmy.56309
Wickham H. 2016. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York
Wiklund K., Nilsson L.O. and Jacobson S. 1995. Effect of irrigation, fertilisation and artificial drought on basidioma production in a Norway spruce stand. Canadian Journal of Botany, 73, 200–208. https://doi.org/10.1139/b95-023
Wu Y.T., Wubet T., Trogisch S., Both S., Scholten T., Bruelheide H. and Buscot F. 2013. Forest age and plant species composition determine the soil fungal community composition in a Chinese subtropical forest. PLoS One 8: e6682. https://doi.org/10.1371/journal.pone.0066829
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