Substrate properties, forest structure and climate influences wood-inhabiting fungal diversity in broadleaved and mixed forests from Northeastern Romania
Abstract
Aim of the study: The main objective of this study was to find the factors which best explains the wood-inhabiting fungal species’ richness in beech and oak-dominated forests.
Area of study: We focused on broadleaved and mixed forests found in Northeastern Romania.
Materials and methods: 59 plots were randomly set up in broadleaved and mixed forest stands, in which vegetation structure, composition, and topoclimatic factors were quantified along with wood-inhabiting fungal richness. Generalized linear models were used to characterize relationship between fungal diversity and biotic and abiotic factors.
Main results: 374 taxa were identified, with numerous species found to cohabitate, the highest sharing being between Fine Woody Debris and Downed Coarse Woody Debris. The best predictors of total diversity were related to the substrate, management, stand structure, and macroclimate. Higher volumes of logs and large branches in various decay stages increased fungal richness. The same effect was found in diverse forests, with large snags. Macroclimate and topoclimate positively influenced diversity, through De Martonne Aridity Index and snow cover length, both indicating macrofungi preferences for higher moisture of substrate. Silvicultural interventions had an ambivalent effect to fungal diversity, phenomenon observed through stump numbers and proportion.
Research highlights: Particular environmental characteristics proved significantly important in explaining different wood-inhabiting fungal richness patterns. Substrate-related variables were the most common ones found, but they were closely linked to climate and forest stand variables.
Keywords: Wood-inhabiting fungi; oak, beech and coniferous forests; substrate diversity; dead wood types; coarse woody debris; fine woody debris; climatic variables.
Abbreviations used:
ALT, elevation; ASPI, Aspect Index; BIO1, mean annual temperature; BIO4, temperature seasonality; BIO7, annual temperature range; BIO12, annual precipitation; BIO15, precipitation seasonality; CWD, coarse woody debris; DBH, diameter at breast height; DCWD, downed coarse woody debris; DCWD_DECAY, DCWD decay diversity; DCWD_DIV, DCWD taxonomic diversity; DCWD_SV, surface-volume ratio of DCWD; DCWD_VOL, DCWD volume; DMAI, De Martonne Aridity Index; DMAI_AU, Autumn DMAI; DMAI_SP, Spring DMAI; DMAI_SU, Summer DMAI; DMAI_WI, Winter DMAI; FAI, Forestry Aridity Index; FWD, fine woody debris; L_SNAG_BA, large snag basal area; OLD_BA, basal area of old trees; POI, Positive Openness Index; RAI, Recent Activity Index; SCL, snow cover length; SLOPE, slope; SNAG_N, snag density; STUMP_N, stump density; TPI, Topographic Position Index; TREE_BA, mean basal area of trees; TREE_DIV, tree' Shannon diversity.Downloads
References
Abrego N, Salcedo I, 2011. How does fungal diversity change based on woody debris type? A case study in Northern Spain. Ekologija 57(3): 109-119. https://doi.org/10.6001/ekologija.v57i3.1916
AbregoN, Halme P, Purhonen J, Ovaskainen O, 2016. Fruit body based inventories in wood-inhabiting fungi: Should we replicate in space or time? Fungal Ecol 20: 225-232. https://doi.org/10.1016/j.funeco.2016.01.007
Administrația Națională de Meteorologie, 2008. Clima României. Academia Română, București, Romania. 316 pp.
Andronache I, Fensholt R, Ahammer H, Ciobotaru A-M, Pintilii R-D, Peptenatu D, Drăghici C-C, Diaconu DC, Radulović M, Pulighe G, et al., 2017. Assessment of textural differentiations in forest resources in Romania using fractal analysis. Forests 8(3): 54-74. https://doi.org/10.3390/f8030054
Balboa-Murias MA, Rojo A, Álvarez JG, Merino A, 2006. Carbon and nutrient stocks in mature Quercus robur L. stands in NW Spain. Ann Forest Sci 63(5): 557-565. https://doi.org/10.1051/forest:2006038
Bässler C, Müller J, Dziock F, Brandl R, 2010. Effects of resource availability and climate on the diversity of wood-decaying fungi. J Ecol 98: 822-832. https://doi.org/10.1111/j.1365-2745.2010.01669.x
Berbeco MR, Melillo JM, Orians CM, 2012. Soil warming accelerates decomposition of fine woody debris. Plant Soil 356: 405-417. https://doi.org/10.1007/s11104-012-1130-x
Bernicchia A, 2005. Fungi Europaei. Polyporaceae s.l. Candusso, Alassio, Italy. 808 pp.
Bîrsan C, Tănase C, Mardari C, Cojocariu A, 2014. Diversity and ecological determinants of dead wood fungi in tree natural reserves of broad leaved forests from Suceava county. J Plant Develop 21: 153-160.
Boddy L, 1993. Saprotrophic cord-forming fungi: warfare strategies and other ecological aspects. Mycol Res 97(6): 641-655. https://doi.org/10.1016/S0953-7562(09)80141-X
Brazee NJ, Lindner DL, D'Amato AW, Fraver S, Forrester JA, Mladenoff DJ, 2014. Disturbance and diversity of wood-inhabiting fungi: effects of canopy gaps and downed woody debris. Biodivers Conserv 23: 2155-2172. https://doi.org/10.1007/s10531-014-0710-x
Breitenbach J, Kränzlin F, 1986. Champignons de Suisse. Tome 2. Champignons sans lames. Mykologia Luzern, Lucerne, Switzerland. 412 pp.
Buée M, Maurice J-P, Zeller B, Andrianarisoa S, Ranger J, Courtecuisse R, Marçais B, Le Tacon F, 2011. Influence of tree species on richness and diversity of epigeous fungal communities in a French temperate forest stand. Fungal Ecol 4(1): 22-31. https://doi.org/10.1016/j.funeco.2010.07.003
Burnham KR, Anderson DR., 2002. Model selection and multimodel inference - A practical information - theoretic approach. 2nd ed. Springer, New York, US. 488 pp.
Chaudhary A, Burivalova Z, Koh LP, Hellweg S, 2016. Impact of forest management on species richness: Global meta-analysis and economic trade-offs. Sci Rep 6: 23954. https://doi.org/10.1038/srep23954
Coates D, Rayner ADM, 1985. Fungal population and community development in cut beech logs. I. Establishment via the aerial cut surface. New Phytol 101(1): 153-171. https://doi.org/10.1111/j.1469-8137.1985.tb02823.x
Conrad O, Bechtel B, Bock M, Dietrich H, Fischer E, Gerlitz L, Wehberg J, Wichmann V, Böhner J, 2015. System for Automated Geoscientific Analysis (SAGA) v. 2.1.4. Geosci Model Dev 8: 2272-2312. https://doi.org/10.5194/gmdd-8-2271-2015
Copoț O, Balaeș T, Bîrsan C, Petre CV, Cojocariu A, Tănase C, 2018. Climatic predictors influences VFWD fungal diversity through dominant tree' ecology in beech forests in the North-Eastern Romania. J Plant Develop 25: 119-134. https://doi.org/10.33628/jpd.2018.25.1.119
Copoț O, Tănase C, 2019. Dead wood, forest fragmentation and elevation influences macrofungal diversity on downed coarse woody debris in beech and oak old forest ecosystems from Northeastern Romania. J Plant Develop 26:161-172. https://doi.org/10.33628/jpd.2019.26.1.161
Courtecuisse R, Duhem B, 2013. Champignons de France et d'Europe. Delachaux et Niestlé, Paris, France. 542 pp.
Dvořák D, Vašutová J, Hofmeister J, Beran M, Hošek J, Běťák J, Burel J., Deckerová H, 2017. Macrofungal diversity patterns in central European forests affirm the key importance of old-growth forests. Fungal Ecol 27: 145-154. https://doi.org/10.1016/j.funeco.2016.12.003
Eurostat, 2019. Your key to European statistics. http://ec.europa.eu/eurostat/web/regions/data/database/
Ellis JB, Everhart DM, 1966. The North American Pyrenomycetes. A contribution to mycologic botany. Johnson Reprint Corporation, New York, US. 793 pp.
Enrong Y, Xihua W, Jianjun H, 2006. Concept and classification of coarse woody debris in forest ecosystems. Front Biol 1(1): 76-84. https://doi.org/10.1007/s11515-005-0019-y
Feurdean A, Wohlfarth B, Björkman L, Tantau I, Bennike O, Willis KJ, Farcaș S, Robertsson AM, 2007. The influence of refugial population on Lateglacial and early Holocene vegetational changes in Romania. Rev Palaeobot Palyno 145: 305-320. https://doi.org/10.1016/j.revpalbo.2006.12.004
Fick SE, Hijmans RJ, 2017. Worldclim 2: New 1-km spatial resolution climate surfaces for global land areas. Int J Climatol 37(12): 4302-4315. https://doi.org/10.1002/joc.5086
Fyfe RM, Woodbridge J, Roberts N, 2015. From forest to farmland: pollen-inferred land cover change across Europe using the pseudobiomization approach. Global Change Biol 21(3): 1197-1212. https://doi.org/10.1111/gcb.12776
Führer E, Horváth L, Jagodics A, Machon A, Szabados I, 2011. Application of new aridity index in Hungarian forestry practice. Idojaras 115(3): 205-216.
Goia I, Gafta D, 2018. Beech versus spruce dead wood as forest microhabitat: does it make any difference to bryophytes? Plant Biosyst 153(2): 187-194. https://doi.org/10.1080/11263504.2018.1448011
Gora EM, Battaglia LL, Schumacher HB, Carson WP, 2014. Patterns of coarse woody debris volume among 18 late-successional and mature forest stands in Pennsylvania. J Torrey Bot Soc 141(2): 151-160. https://doi.org/10.3159/TORREY-D-13-00066.1
Grünewald T, Bühler Y, Lehning M, 2014. Elevation dependency of mountain snow depth. Cryosphere 8: 2381-2394. https://doi.org/10.5194/tc-8-2381-2014
Hallett JG, Lopez T, O'Connell MA, Borysewicz MA, 2001. Decay dynamics and avian use of artificially created snags. Northwest Sci 75(4): 378-386.
Heilmann-Clausen J, Christensen M, 2003. Fungal diversity on decaying beech logs. implications for sustainable forestry. Biodivers Conserv 12: 953-973. https://doi.org/10.1023/A:1022825809503
Heilmann-Clausen J, Christensen M, 2004. Does size matter?: On the importance of various dead wood fractions for fungal diversity in Danish beech forests. Forest Ecol Manag 201(1): 105-117. https://doi.org/10.1016/S0378-1127(04)00519-5
Heilmann-Clausen J, Aude E, Christensen M, 2005. Cryptogam communities on decaying deciduous wood - does tree species diversity matter? Biodivers Conserv 14:2061-2078. https://doi.org/10.1007/s10531-004-4284-x
Holloway GL, Caspersen JP, Vanderwel MC, Naylor BJ, 2007. Cavity tree occurrence in hardwood forests of central Ontario. Forest Ecol Manag 239(1-3):191-199. https://doi.org/10.1016/j.foreco.2006.12.004
Hottola J, Siitonen J, 2008. Significance of woodland key habitats for polypore diversity and red-listed species in boreal forests. Biodivers Conserv 17:2559-2577. https://doi.org/10.1007/s10531-008-9317-4
Index Fungorum, 2019. http://www.indexfungorum.org/Names/Names.asp
Iršėnaitė R, Kutorga E, 2006. Diversity of fungi on decaying common oak coarse woody debris. Ekologija 4: 22-30.
Kebli H, Brais S, Kernaghan G, Drouin P, 2012. Impact of harvesting intensity on wood-inhabiting fungi in boreal aspen forests of Eastern Canada. Forest Ecol Manag 279: 45-54. https://doi.org/10.1016/j.foreco.2012.05.028
Klockow PA, D'Amato AW, Bradford JB, Fraver S, 2014. Nutrient concentrations in coarse and fine woody debris of Populus tremuloides Michx.-dominated forests, northern Minnesota, USA. Silva Fenn 48(1): 962. https://doi.org/10.14214/sf.962
Kubart A, Vasaitis R, Stenlid J, Dahlberg A, 2016. Fungal communities in Norway spruce stumps along a latitudinal gradient in Sweden. Forest Ecol Manag 371: 50-58. https://doi.org/10.1016/j.foreco.2015.12.017
Kubartová A, Ranger J, Berthelin J, Beguiristain T, 2009. Diversity and decomposing ability of saprophytic fungi from temperate forest litter. Environ Microbiol 58: 98-107. https://doi.org/10.1007/s00248-008-9458-8
Kutsegi G, Siller I, Dima B, Takács K, Merényi Z, Varga T, Turcsányi G, Bidló A, Ódor P, 2015. Drivers of macrofungal species composition in temperate forests, West Hungary: functional groups compared. Fungal Ecol 17: 69-83. https://doi.org/10.1016/j.funeco.2015.05.009
LifeWatch Belgium, 2019. http://www.lifewatch.be/en/data/
Lombardi F, Cherubini P, Tognetti R, Cocozza C, Lasserre B, Marchetti M, 2013. Investigating biochemical processes to as-sess dead wood decay of beech and silver fir in Mediterranean mountain forests. Ann Forest Sci 70: 101−111. https://doi.org/10.1007/s13595-012-0230-3
Méndez-Toribio M, Meave JA, Zermeño-Hernández I, Ibarra-Manríquez G, 2016. Effects of slope aspect and topographic position on environmental variables, disturbancce regime and tree community attributes in a seasonal tropical dry forest. J Veg Sci 27(6): 085002. https://doi.org/10.1111/jvs.12455
Milescu I, Alexe A, Nicovescu H, Suciu P, 1967. Fagul. Ed. Agro-Silvică, București, Romania. 581 pp. [In Romanian]
Morrissey RC, Jenkins MA, Saunders MR, 2014. Accumulation and connectivity of coarse woody debris in partial harvest and unmanaged relict forests. PLoS One 9(11): e113323. https://doi.org/10.1371/journal.pone.0113323
Ostrogović MZ, Marjanović H, Balenović I, Sever K, Jazbec A, 2015. Decomposition of fine woody debris from main tree species in lowland oak forests. Pol J Ecol 63(2): 247-259. https://doi.org/10.3161/15052249PJE2015.63.2.008
Nordén B, Götmark F, Tönnberg M, Ryberg M, 2004. Dead wood in semi-natural temperate broadleaved woodland: contribution of coarse and fine dead wood, attached dead wood and stumps. Forest Ecol Manag 194(1-3): 235-248. https://doi.org/10.1016/j.foreco.2004.02.043
Ódor P, Heilmann-Clausen J, Christensen M, Aude E, van Dort KW, Piltaver A, Siller I, Veerkamp MT, Walleyn R, Standovár T, et al., 2006. Diversity of dead wood inhabiting fungi and bryophytes in semi-natural beech forests in Europe. Biol Conserv, 131(1): 58-71. https://doi.org/10.1016/j.biocon.2006.02.004
Paliwal R, Giri K, Rai JPN, 2015. Microbial Lignolysis: Avenue for Natural Ecosystem Management. In: Handbook of Research on Uncovering New Methods for Ecosystem Management through Bioremediation; Singh S, Srivastana K (eds). pp: 120-144. Information Science Reference, Hershey, US. https://doi.org/10.4018/978-1-4666-8682-3.ch006
Perry RW, Thill RE, 2013. Comparison of snag densities among regeneration treatments in mixed pine-hardwood forests. Can J Forest Res 43(7): 619-626. https://doi.org/10.1139/cjfr-2013-0005
Petritan AM, Biriș IA, Merce O, Turcu DO, Petritan IC, 2012. Structure and diversity of a natural temperate sessile oak (Quercus petraea L.) - European Beech (Fagus sylvatica L.) forest. Forest Ecol Manag 280: 140-149. https://doi.org/10.1016/j.foreco.2012.06.007
Preikša Z, Brazaitis G, Marozas V, Jaroszewicz B, 2015. Dead wood quality influences species diversity of rare cryptogams in temperate broadleaved forests. iForests 9: 276-285. https://doi.org/10.3832/ifor1483-008
Quan C, Han S, Utescher T, Zhang C, Liu YSC, 2013. Validation of temperature-precipitation based aridity index: Paleoclimatic implications. Paleogeogr Paleocl 386: 86-95. https://doi.org/10.1016/j.palaeo.2013.05.008
R Core Team, 2018. R: A language and environment for statistical computing. http://www.R-project.org/
Rabinowitsch-Jokinen R, Vanha-Majamaa I, 2010. Immediate effects of logging, mounding and removal of logging residues and stumps on coarse woody debris in managed Boreal Norway spruce stands. Silva Fenn 44(1): 51-62. https://doi.org/10.14214/sf.162
Roth TR, Nolin AW, 2017. Forest impacts on snow accumulation and ablation across an elevation gradient in a temperate montane environment. Hydrol Earth Syst Sc 21: 5427-5442. https://doi.org/10.5194/hess-21-5427-2017
Rudolph S, Maciá-Vicente JG, Lotz-Winter H, Shcleuning M, Piepenbring M, 2018. Temporal variation of fungal diversity in a mosaic landscape in Germany. Studi Mycol 89:95-104. https://doi.org/10.1016/j.simyco.2018.01.001
Runnel K, Lõhmus A, 2017. Dead wood-rich managed forests provide insights into the old-forest association of wood-inhabiting fungi. Fungal Ecol 27(Part B): 155-167. https://doi.org/10.1016/j.funeco.2016.09.006
Ryvarden L, 1976. The Polyporaceae of North Europe. vol. 1. Albatrellus - Incrustoporia. Fungiflora, Oslo, Norway. 214 pp.
Ryvarden L, 1991. Genera of Polypores. Nomenclature and taxonomy. Synopsis Fungorum Series 5, Fungiflora, Oslo, Norway. 363 pp.
Ryvarden L, Gilbertson RL, 1994. European Polypores. Part 2. Meripilus - Tyromyces. Oslo, Fungiflora, Norway. 743 pp.
Schall P, Ammer C, 2013. How to quantify forest management intensity in Central European forests. Eur J Forest Res 132(2): 379-296. https://doi.org/10.1007/s10342-013-0681-6
Sefidi K, Etemad V, 2015. Dead wood characteristics influencing macrofungi species abundance and diversity in Caspian natural beech (Fagus orientalis Lipsky) forests. Forest Syst 24(2): eSC03. https://doi.org/10.5424/fs/2015242-06039
Sippola A-L, Similä M, Mönkkönen M, Jokimäki J, 2004. Diversity of polyporous fungi (Polyporaceae) in northern boreal forests: effects of forest site type and logging intensity. Scand J Forest Res 19(2): 152-163. https://doi.org/10.1080/02827580410026294
Tavankar F, Picchio R, Lo Monaco A, Bonyad AE, 2014. Forest management and snag characteristics in Northern Iran lowland forests. J For Sci 60(10): 431−441. https://doi.org/10.17221/77/2014-JFS
Tavankar F, Nikooy M, Picchio R, Venanzi R, Lo Monaco A, 2017. Long-term effects of single-tree selection cutting management on coarse woody debris in natural mixed beech stands in the Caspian forest (Iran). iForest 10(3): 652-658. https://doi.org/10.3832/ifor2091-010
Tănase C, Bîrsan C, Chinan V, Cojocariu A, 2009. Macromicete din România. Universitatea Alexandru Ioan Cuza, Iași, Romania. 564 pp. [In Romanian]
Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS, Wijesundera R, Ruiz LV, Vasco-Palacios AM, Thu PQ, Suija A, et al., 2015 Global diversity and geography of soil fungi. Science 346(6213): 1256688. https://doi.org/10.1126/science.1256688
Unar P, Janík D, Adam D, Vymazalová M, 2017. The colonization of decaying logs by vascular plants and the consequences of fallen logs for herb layer diversity in a lowland alluvial forest. Eur J Forest Res 136(4): 665-676. https://doi.org/10.1007/s10342-017-1063-2
Unterseher M, Otto P, Morawetz W, 2003. Studies of the diversity of lignicolous fungi in the canopy of a floodplain forest in Leipzig, Saxony. Boletus 26(2): 117-126.
van der Wal A, Gunnewiek PK, de Hollander M, de Boer W, 2017. Fungal diversity and potential tree pathogens in decaying logs and stumps. Forest Ecol Manag 406: 266-273. https://doi.org/10.1016/j.foreco.2017.08.018
Wirth C, Messier C, Bergeron Y, Frank D, Fankhänel A, 2009. Chapter 2: Old-growth forest definitions: a pragmatic view. In: Old-Growth Forests. Ecological Studies (Analysis and Synthesis), Vol. 207; Wirth C, Gleixner G, Heimann M. (eds). pp: 11-33. Springer, Berlin, Germany. https://doi.org/10.1007/978-3-540-92706-8_2
Wisdom MJ, Bate LJ, 2008. Snag density varies with intensity of timber harvest and human access. Forest Ecol Manag 255(7): 2085-2093. https://doi.org/10.1016/j.foreco.2007.12.027
Woodall CW, Liknes GC, 2008. Climatic regions as an indicator of forest coarse and fine woody debris carbon stocks in the Unites States. Carbon Balance and Manag 3(1): 1-8. https://doi.org/10.1186/1750-0680-3-5
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