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Research article

Selective thinning to enhance soil biodiversity in artificial black pine stands - what happens to mushroom fruiting?

Elena Salerni, Debora Barbato , Cecilia Cazau, Lorenzo Gardin, Gianni Henson, Pamela Leonardi, Antonio Tomao, Claudia Perini

Elena Salerni
University of Siena
Debora Barbato
University of Siena. Email:
Cecilia Cazau
Unione dei Comuni Pratomagno, Via Perugia 2/A, 52024 Loro Ciuffenna, Arezzo, Italy
Lorenzo Gardin
Soil territory environment, Florence
Gianni Henson
University of Siena
Pamela Leonardi
University of Bologna
Antonio Tomao
University of Tuscia
Claudia Perini
University of Siena

Online First: December 31, 2020
Salerni, E., Barbato, D., Cazau, C., Gardin, L., Henson, G., Leonardi, P., Tomao, A., Perini, C. 2020. Selective thinning to enhance soil biodiversity in artificial black pine stands - what happens to mushroom fruiting?. Annals of Forest Research DOI:10.15287/afr.2020.2006

As a man-induced disturbance of forest ecosystems, thinning may affect biodiversity and other related ecological functions including fungal dynamics. In this context, a multidisciplinary EU-Life project was established in 2014 to evaluate the application of selective thinning in two Pinus nigra plantations areas of the Apennines (Monte Amiata and Pratomagno, Tuscany Italy). Selective thinning had the aim to improve stands stability and growth rates, taking also into account the various components of soil biodiversity (flora, fungi, mesofauna, nematodes, microarthropods and bacteria). Here we present mushroom fruiting patterns previous to treatment in 2014 and the effect following the application of forest management (selective thinning and traditional thinning from below) in 2018. Boxplots were used to graphically represent intra and inter annual variations in species richness and abundance, while Principal Coordinates Analyses and multi-response permutation procedures based on Bray-Curtis dissimilarity matrix were applied to evaluate turnover in species composition before the management and after 4 years.

A significant reduction of fungal richness and abundance after 4 years thinning impact was lacking in both study areas, testifying a certain degree of resistance and/or resilience of mushroom fruiting to forest management-related anthropogenic disturbance. Considering each study site separately, Monte Amiata and Pratomagno did not show one uniform trend but differed significantly in their response to management: while in Pratomagno relevant inter-annual differences were present only in a few cases, an underlining significant variation both for species richness and abundance was registered in Monte Amiata for all treatment types among years (inter-annual variation) but not within each year (intra-annual variation). Only in Pratomagno turnover in species composition in selective thinning differed somewhat from the traditional treatment in 2018, showing that a process is underlying but still potentially masked by other variables. Due to the nature of macrofungi, a longer study period (more than 4 years post treatment impact) as well as the application of a more intense forest management, could be necessary to highlight and disentangle any possible trends in fungal fruiting in artificial stands.

Abrego N., Salcedo I., 2014. Response of wood-inhabiting fungal community to fragmentation in a beech forest landscape. Fungal Ecol 8: 18-27.

Ágreda T., Águeda B., Olano JM., Vicente-Serrano SM., Fernández-Toirán M., 2015. Increased evapotranspiration demand in a Mediterranean climate might cause a decline in fungal yields under global warming. Glob Change Biol 21: 3499-3510.

Alday LG., Bonet JA., Oria-de-Rueda JA., Martínez de Aragón J., Aldea J., Martín-Pinto P., de-Miguel S., Hernández-Rodríguez M., Martínez-Peña F., 2017. Record breaking mushroom yields in Spain. Fungal Ecol 26: 144-146.

Anderson JM., 1975. The enigma of soil animal species diversity. In: Vaněk J., (ed.), Progress in Soil Zoology. Proceedings of the 5th International Colloquium on Soil Zoology Held, 17–22 September 1973, Prague, Czech Republick, pp. 51-58.

Andrén O., Balandreau J., 1999. Biodiversity and soil functioning – from black box to can of worms? Appl Soil Ecol 13: 105-108.

Antonín V., Noordeloos ME., 1997. A Monograph of Marasmius, Collybia and related genera in Europa (part 2: Collybia, Gymnopus, Rhodocollybia, Crinipellis, Chaetocalathus and additions to Marasmiellus). IHW-VERLAG, 256 p.

Arnolds E., 1981. Ecology and coenology of macrofungi in grassland and moist heatland in Drenthe the Netherlands. Biblioteca Mycologica, 410 p.

Arnolds E., Kuyper TW., Noordeloos ME., 1995. Overzicht van de paddestoelen in Nederland. Nederlandse Mycologische Vereniging, 872 p.

Baral S., Thapa-Magar KB., Karki G., Devkota S., Shrestha BB., 2015. Macrofungal diversity in community-managed sal (Shorea robusta) forests in central Nepal. Mycology 6(3-4): 151-157.

Barbato D., Perini C., Mocali S., Bacaro G., Tordoni E., Maccherini S., Marchi M., Cantiani P., De Meo I., Bianchetto E., Landi S., Bruschini S., Bettini G., Gardin L., Salerni E., 2019. Teamwork makes the dream work: disentangling cross-taxon congruence across soil biota in black pine plantations. Sci Total Environ 656: 659-669.

Beker JH., Eberhardt U., Vesterholt J., 2016. Hebeloma (Fr.) P. Kumm. (Vol. 14 - Fungi Europaei). Edizioni Tecnografica, 1218 p.

Boddy L., Büntgen U., Egli S., Gange A., Heegaard E., Kirk P., Mohammad A., Kauserud H., 2014. Climate variation effects on fungal fruiting. Fungal Ecol 10: 20-33.

Boncina A., Kadunc A., Robic D., 2007. Effects of selective thinning on growth and development of beech (Fagus sylvatica L.) forest stands in south-eastern Slovenia. Ann For Sci 64(1): 47-57.

Bonet JA., Fischer CR., 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 Ecol Manag 203: 157-175.

Bonet JA., De-Miguel S., de Aragón JM., Pukkala T., Palahí M., 2012. Immediate effect of thinning on the yield of Lactarius group deliciosus in Pinus pinaster forests in Northeastern Spain. Forest Ecol Manag 265: 211-217.

Bonet JA., González-Olabarria JR., Martínez de Aragón J., 2014. Mushroom production as an alternative for rural development in a forested mountainous area. J Mt Sci 11(2): 535-543.

Brussaard L., Kuyper TW., Didden WAM., de Goede RGM., Bloem J., 2004. Biological soil quality from biomass to biodiversity – Importance and resilience to management stress and disturbance. In: SchjØnning P., Elmholt S., Christensen BT., (eds.), Chapter: 9 Managing Soil Quality: Challenges in Modern Agriculture”. CABI Publishing, pp.139-161.

Brussaard L., de Ruiter PC., Brown GG., 2007. Soil biodiversity for agricultural sustainability. Agr Ecosyst Environ 121: 233-244.

Candusso M., Lanzoni G., 1990. Lepiota s.l. (Vol. 4 - Fungi Europaei). Libreria Editrice Giovanna Biella, 743 p.

Cantiani P., 2016. Il diradamento selettivo. Accrescere stabilità e biodiversità in boschi artificiali di pino nero. Manuale tecnico SelPiBioLife [LIFE13 BIO/IT/000282]. Compagnia delle Foreste, Arezzo, Italy, 62 p.

Cantiani P, Marchi M., 2017. A spatial dataset of forest mensuration collected in black pine plantations in central Italy. Ann For Sci 74(3): 50.

Castaño C., Alday JG., Lindahl BD., Martínez de Aragón J., de-Miguel S., Colinas C., Parladé J., Pera J., Bonet JA., 2018. Lack of thinning effects over inter-annual changes in soil fungal community and diversity in a Mediterranean pine forest. Forest Ecol Manag 424: 420-427.

Costantini EAC., 2007. Linee guida dei metodi di rilevamento e informatizzazione dei dati pedologici. CRA-ABP, Firenze, Italy, 296 p.

Dejene T., Oria-de-Rueda JA, Martín-Pinto P., 2017. Fungal diversity and succession following stand development in Pinus patula Schiede ex Schltdl. & Cham. plantations in Ethiopia. Forest Ecol Manag, 395: 9-18.

Di Salvatore U.; Ferretti F.; Cantiani P.; Paletto A.; De Meo I.; Chiavetta U., 2013. Multifunctionality assessment in forest planning at landscape level. The study case of Matese Mountain Community (Italy). Ann Silvic Res 37: 45–54.

Dove NC., Keeton WS., 2015. Structural complexity enhancement increases fungal species richness in northern hardwood forests. Fungal Ecol 13: 181-192.

Egli S., Ayer F., Chatelain F., 1990. Der einfluss des pilzsammelns auf die pilzflora. Mycologia Helvetica 3(4): 417–428.

Egli S., Peter M., Buser C., Stahel W., Ayer F., 2006. Mushroom picking does not impair future harvests–results of a long-term study in Switzerland. Biol Conserv 129(2): 271-276.

Egli S., Ayer F., Peter M., Eilmann B., Rigling A., 2010 Is forest mushroom productivity driven by tree growth? Results from a thinning experiment. Ann Forest Sci 67: 509.

Ekschmitt K., Griffiths BS., 1998. Soil biodiversity and its implications for ecosystem functioning in a heterogeneous and variable environment. Appl Soil Ecol 10: 201-215.

Giller PS., 1996. The diversity of soil communities the poor man’s tropical rainforest. Biodivers Conserv 5: 135-168.

Hawksworth DL., Lücking R., 2017. Fungal diversity revisited: 2.2 to 3.8 million species. In: Heitman J., Howlett B., Crous P., Stukenbrock E., James T., Gow NAR., (eds), The Fungal Kingdom. ASM Press, Washington DC, USA, pp. 79-95.

Karavani A., De Cáceres M., Martínez de Aragón J., Bonet JA., de-Miguel S., 2018. Effect of climatic and soil moisture conditions on mushroom productivity and related ecosystem services in Mediterranean pine stands facing climate change. Agr Forest Meteorol 248: 432-440.

Kim MS., Klopfenstein NB., McDonald GI., 2010. Effects of forest management practices and environment on occurrence of Armillaria Species. Journal of Korean Forest Society 99(2): 251-257.

Kranabetter JM., Friesen J., Gamiet S., Kroeger P., 2005. Ectomycorrhizal mushroom distribution by stand age in western hemlock–lodgepole pine forests of northwestern British Columbia. Can. J. For. Res. 35(7): 1527-1539.

Kucuker DM., Baskent EZ., 2017. Impact of forest management intensity on mushroom occurrence and yield with a simulation-based decision support system. Forest Ecol Manag 389: 240-248.

Leonardi P., Graziosi S., Zambonelli A., Salerni E., 2017. The economic potential of mushrooms in an artificial Pinus nigra forest. Italian Journal of Mycology 46: 48-59.

Lin WR., Chen WC., Wang PH., 2011. Effects of forest thinning on diversity and function of macrofungi and soil microbes. Sydowia 63(1): 67-77.

Lin WR., Wang PH., Chen MC., Kuo YL., Chiang PN., Wang MK., 2015. The impacts of thinning on the fruiting of saprophytic fungi in Cryptomeria japonica plantations in central Taiwan. Forest Ecol Manag 336: 183-193.

Maghnia FZ., Sanguin H., Abbas Y., Verdinelli M., Kerdouh B., El Ghachtouli N., Lancellotti E., Bakkali Yakhlef SE., Duponnois R., 2017. Impact du mode de gestion de la subéraie de la Maâmora (Maroc) sur la diversité des champignons ectomycorhiziens associés à Quercus suber. C R Biol 340(5): 298–305.

Manetti MC., Becagli C., Bertini G., Cantiani P., Marchi M., Pelleri F., Sansone D., Fabbio G., 2020. The conversion into high forest of Turkey oak coppice stands: methods, silviculture and perspectives. iForest 13: 309-317. – doi: 10.3832/ifor3483-013

Marchi M., Paletto A., Cantiani P., Bianchetto E., De Meo I., 2018. Comparing thinning system effects on ecosystem services provision in artificial black pine (Pinus nigra JF Arnold) forests. Forests, 9(4): 188.

Martínez-Peña F., de-Miguel S., Pukkala T., Bonet JA., Ortega-Martínez P., Aldea J., Martínez de Aragón J., 2012. Yield models for ectomycorrhizal mushrooms in Pinus sylvestris forests with special focus on Boletus edulis and Lactarius group deliciosus. Forest Ecol Manag 282: 63-69.

Martínez de Aragón J., Bonet JA., Fischer CR., Colinas C., 2007. Productivity of ectomycorrhizal and selected edible saprotrophic fungi in pine forests of the pre-Pyrenees mountains Spain: Predictive equations for forest management of mycological resources. Forest Ecol Manag 252: 239-256.

Mello A., Murat C., Bonfante P., 2006. Truffles: much more than a prized and local fungal delicacy. FEMS Microbiol Lett, 260(1): 1-8.

Müller J., Engel H., Blaschke M., 2007. Assemblages of wood-inhabiting fungi related to silvicultural management intensity in beech forests in southern Germany. Eur J For Res 126: 513-527.

Nielsen UN., Ayres E., Wall DH., Bardgett RD., 2011. Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity – function relationships. Eur J Soil Sci 62: 105-116.

Norvell L., 1995. Loving the chanterelle to death? The ten-year Oregon chanterelle project. McIlvainea 12(1): 6-25.

Oria-de-Rueda JA., Hernández-Rodríguez M., Martín-Pinto P., Pando V., Olaizola J., 2010. Could artificial reforestations provide as much production and diversity of fungal species as natural forest stands in marginal Mediterranean areas? Forest Ecol Manag 260(2): 171-180.

Pagliai M., 1997. Metodi di analisi fisica del suolo. Franco Angeli, Milano. 400 p.

Perini C., Barbato D., Bianchetto E., Mocali S., De Meo I., Cantiani P., Salerni E., 2017. Soil biota and innovative forest management: a Life Project. In: Proceedings of the “European Council for Conservation of Fungi and International Mycological Association”. 1-6 October 2017 Ohrid, Republic of Macedonia, pp. 48-49.

Pilz D., Molina R., 2002. Commercial harvests of edible mushrooms from the forests of the Pacific Northwest United States: issues management and monitoring for sustainability. Forest Ecol Manag 155(1): 3-16.

Pilz D., Molina R., Mayo J., 2006. Effects of thinning young forests on chanterelle mushroom production. J Forest 104: 9-14.

Ponce RA., Ágreda T., Águeda B., Aldea J., Martínez-Peña F., Modrego MP., 2014. Soil physical properties influence “black truffle” fructification in plantations. Mycorrhiza 24:55-64

R Development Core Team., 2018. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL: http://cran.

Robinson RM., Williams MR., 2011. Forestcheck: the response of epigeous macrofungi to silviculture in jarrah (Eucalyptus marginata) forest. Aust Forestry 74(4): 288-302.

Salerni E., Perini C., 2004. Experimental study for increasing productivity of Boletus edulis s.l. in Italy. Forest Ecol Manag 201: 161-170.

Salerni E., Perini C., 2010. Macrofungal communities in Italian fir woods – short term effects of silviculture and its implications for conservation. Cryptogamie Mycol 31: 251-283.

Salerni E., Baglioni F., Perini C., 2011. Valorizzazione della produzione di Tuber aestivum Vittad. in tartufaie naturali presenti nel Monte Amiata e nel Monte Cetona. Micologia Italiana 40(1): 44-62.

Santos-Silva C., Goncalves A., Louro R., 2011. Canopy cover influence on macrofungal richness and sporocarp production in montado ecosystems. Agroforest Syst 82: 149-159.

Savoie JM., Largeteau ML., 2011. Production of edible mushrooms in forests: trends in development of a mycosilviculture. Applied Microbiol Biot 89: 971-979.

Shaw PJA., Kibby G., Mayes J., 2003. Effects of thinning treatment on an ectomycorrhizal succession under Scots pine. Mycol Res 107(3): 317–328.

Smith SE., Read DJ., 2008. Mycorrhizal Symbiosis 3rd edn. Academic Press, London, 800 p.

Soil Survey Staff., 2014. Keys to soil taxonomy. 12th ed. USDA - Natural Resources Conservation Service, Washington, DC.

Suominen M., Junninen K., Kouki J., 2019. Diversity of fungi in harvested forests 10 years after logging and burning: Polypore assemblages on different woody substrates. Forest Ecol Manag 446: 63-70.

Tahvanainen V., Miina J., Kurttila M., Salo K., 2016. Modelling the yields of marketed mushrooms in Picea abies stands in eastern Finland. Forest EcolManag 362: 79-88.

Tedersoo L., Bahram M., Põlme S., Kõljalg U., Yorou NS., Wijesundera R., ... & Smith ME., 2014. Global diversity and geography of soil fungi. Science, 346(6213).

Tomao A., Bonet JA., Martínez de Aragón J., de-Miguel S., 2017. Is silviculture able to enhance wild forest mushroom resources? Current knowledge and future perspectives. Forest Ecol Manag 402: 102-114.

Tomao A., Bonet JA., Castaño C., de-Miguel S., 2020. How does forest management affect fungal diversity and community composition? Current knowledge and future perspectives for the conservation of forest fungi. Forest Ecol Manag 457: 117678.

Usher MB., Davis P., Harris J., Longstaff B., 1979. A profusion of species? Approaches towards understanding the dynamics of the populations of microarthropods in decomposer communities. In: Anderson RM., Turner BD., Taylor LR., (eds.), Population Dynamics. Blackwell Scientific Publications, pp. 359-384.

Waltert B., Wiemken V., Rusterholz HP., Boller T., Baur B., 2002. Disturbance of forest by trampling: Effects on mycorrhizal roots of seedlings and mature trees of Fagus sylvatica. Plant Soil 243: 143-154.

Whitford WG., 1996. The importance of the biodiversity of soil biota in arid ecosystems. Biodivers Conserv 5: 185-195.

Summary of the mushroom sampling performed in the 27 plots in Monte Amiata study site (A) before (2014) and after (2018) management practices
Summary of the mushroom sampling performed in the 27 plots in Pratomagno study site (P) before (2014) and after (2018) management practices
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