Abstract
Wood-inhabiting fungi and saproxylic beetles are threatened by habitat degradation. Our understanding of the importance of macroclimate and local factors determining their taxonomic diversity has increased, but determinants of functional and phylogenetic diversity are poorly understood. We investigated assemblages of wood-inhabiting fungi and saproxylic beetles along a 1000 m elevational gradient of a temperate low mountain range. We (i) tested the relative importance of macroclimate (i.e. elevation) and local variables (microclimate, i.e. canopy closure, amount and diversity of dead wood) in determining observed and rarefied diversities and (ii) explored whether determinants of observed functional and phylogenetic diversities match those of taxonomic diversity. For both taxa, the determinants of observed phylogenetic and functional diversities largely matched those of taxonomic diversity. The diversity of wood-inhabiting fungi was predominantly determined by local variables, whereas that of saproxylic beetles was determined by both local variables and elevation. Taxonomic and phylogenetic diversities of saproxylic beetles decreased with increasing elevation, but standardized functional richness and entropy of both groups increased with increasing elevation. Diversities of wood-inhabiting fungi increased with canopy closure, while diversities of saproxylic beetles decreased with increasing canopy closure. Microclimate and dead-wood amount and diversity affected the observed and rarefied diversity of both saproxylic taxa, which justifies conservation actions that focus on attributes of dead wood and canopy cover. The contrasting responses of fungi and beetles highlight the need for amounts of diverse dead wood in the various microclimates to preserve functional and phylogenetic diversities of saproxylic organisms.
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Abrego N, Salcedo I (2013) Variety of woody debris as the factor influencing wood-inhabiting fungal richness and assemblages: is it a question of quantity or quality? For Ecol Manag 291:377–385. https://doi.org/10.1016/j.foreco.2012.11.025
Abrego N, Norberg A, Ovaskainen O (2016) Measuring and predicting the influence of traits on the assembly processes of wood-inhabiting fungi. J Ecol 105:1070–1081. https://doi.org/10.1111/1365-2745.12722
Albrecht L (1990) Grundlagen, Ziele und Methodik der waldökologischen Forschung in Naturwaldreservaten, Naturwaldreservate in Bayern. Schriftenr. Bayer. Staatsministeriums für Ernährung, Landwirtschaft und Forsten, 75–88
Baber K, Otto P, Kahl T, Gossner MM, Wirth C, Gminder A, Bässler C (2016) Disentangling the effects of forest-stand type and dead-wood origin of the early successional stage on the diversity of wood-inhabiting fungi. For Ecol Manag 377:161–169. https://doi.org/10.1016/j.foreco.2016.07.011
Bässler C, Förster B, Moning C, Müller J (2009) The BIOKLIM Project: biodiversity research between climate change and wilding in a temperate montane forest—the conceptual framework aims and structure of the BIOKLIM Project. Waldökologie-Online 7:21–34
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
Bässler C, Hothorn T, Brandl R, Müller J (2013) Insects overshoot the expected upslope shift caused by climate warming. PLoS ONE. https://doi.org/10.1371/journal.pone.0065842
Bässler C, Ernst R, Cadotte M, Heibl C, Müller J (2014) Near-to-nature logging influences fungal community assembly processes in a temperate forest. J Appl Ecol 51:939–948. https://doi.org/10.1111/1365-2664.12267
Bässler C, Cadotte MW, Beudert B, Heibl C, Blaschke M, Bradtka JH, Langbehn T, Werth S, Müller J (2016) Contrasting patterns of lichen functional diversity and species richness across an elevation gradient. Ecography 39:689–698. https://doi.org/10.1111/ecog.01789
Binder M, Larsson K-H, Matheny PB, Hibbett DS (2010) Amylocorticiales ord. nov. and Jaapiales ord. nov.: early diverging clades of Agaricomycetidae dominated by corticioid forms. Mycologia 102:865–880
Bjørnstad ON, Falck W (2001) Nonparametric spatial covariance functions: estimation and testing. Environ Ecol Stat 8:53–70. https://doi.org/10.1023/A:1009601932481
Cadotte MMW, Cavender-bares J, Tilman D, Oakley THT (2009) Using phylogenetic, functional and trait diversity to understand patterns of plant community productivity. PLoS ONE 4:e5695. https://doi.org/10.1371/journal.pone.0005695
Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087. https://doi.org/10.1111/j.1365-2664.2011.02048.x
Cadotte M, Albert CH, Walker SC (2013) The ecology of differences: assessing community assembly with trait and evolutionary distances. Ecol Lett 16:1234–1244. https://doi.org/10.1111/ele.12161
Cadotte MW, Jonathan Davies T, Peres-Neto PR (2017) Why phylogenies do not always predict ecological differences. Ecol Monogr 87:535–551. https://doi.org/10.1002/ecm.1267
Cisneros LM, Fagan ME, Willig MR (2015) Effects of human-modified landscapes on taxonomic, functional and phylogenetic dimensions of bat biodiversity. Divers Distrib 21:523–533. https://doi.org/10.1111/ddi.12277
Clarke A, Gaston KJ (2006) Climate, energy and diversity. Proc R Soc B Biol Sci 273:2257–2266. https://doi.org/10.1098/rspb.2006.3545
Dehling DM, Fritz SA, Töpfer T, Päckert M, Estler P, Böhning-Gaese K, Schleuning M (2014) Functional and phylogenetic diversity and assemblage structure of frugivorous birds along an elevational gradient in the tropical Andes. Ecography 37:1047–1055. https://doi.org/10.1111/ecog.00623
Devictor V, Mouillot D, Meynard C, Jiguet F, Thuiller W, Mouquet N, Letters E (2010) Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecol Lett 13:1030–1040. https://doi.org/10.1111/j.1461-0248.2010.01493.x
Díaz S, Cabido M (2001) Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655. https://doi.org/10.1016/S0169-5347(01)02283-2
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973. https://doi.org/10.1093/molbev/mss075
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. https://doi.org/10.1016/0006-3207(92)91201-3
Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martínez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho PM, de Vries RP, Ferreira P, Findley K, Foster B, Gaskell J, Glotzer D, Górecki P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens JA, Kallen N, Kersten P, Kohler A, Kües U, Kumar TKA, Kuo A, LaButti K, Larrondo LF, Lindquist E, Ling A, Lombard V, Lucas S, Lundell T, Martin R, McLaughlin DJ, Morgenstern I, Morin E, Murat C, Nagy LG, Nolan M, Ohm RA, Patyshakuliyeva A, Rokas A, Ruiz-Dueñas FJ, Sabat G, Salamov A, Samejima M, Schmutz J, Slot JC, John F St, Stenlid J, Sun H, Sun S, Syed K, Tsang A, Wiebenga A, Young D, Pisabarro A, Eastwood DC, Martin F, Cullen D, Grigoriev IV, Hibbett DS (2012) The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719. https://doi.org/10.1126/science.1221748
Gaston KJ (2000) Global patterns in biodiversity. Nature 405:220–227. https://doi.org/10.1038/35012228
Gaston KJ, Fuller RA (2008) Commonness, population depletion and conservation biology. Trends Ecol Evol 23:14–19. https://doi.org/10.1016/j.tree.2007.11.001
Gossner MM, Lachat T, Brunet J, Isacsson G, Bouget C, Brustel H, Brandl R, Weisser WW, Müller J (2013) Current near-to-nature forest management effects on functional trait composition of saproxylic beetles in beech forests. Conserv Biol 27:605–614. https://doi.org/10.1111/cobi.12023
Gotelli NJ (2000) Null model analysis of species co-occurrence patterns. Ecology 81:2606–2621. https://doi.org/10.1890/0012-9658(2000)081[2606:NMAOSC]2.0.CO;2
Gower JC (1971) A general coefficient of similarity and some of its properties. Biometrics 27:857–871. https://doi.org/10.2307/2528823
Grove SJ (2002) Saproxylic insect ecology and the sustainable management of forests. Annu Rev Ecol Syst 33:1–23. https://doi.org/10.1146/annurev.ecolsys.33.010802.150507
Heck KL, van Belle G, Simberloff D (1975) Explicit calculation of the rarefaction diversity measurement and the determination of sufficient sample size. Ecology 56:1459–1461. https://doi.org/10.2307/1934716
Heikkala O, Seibold S, Koivula M, Martikainen P, Müller J, Thorn S, Kouki J (2016) Retention forestry and prescribed burning result in functionally different saproxylic beetle assemblages than clear-cutting. For Ecol Manag 359:51–58. https://doi.org/10.1016/j.foreco.2015.09.043
Heilmann-Clausen J, Christensen M (2004) Does size matter? On the importance of various dead wood fractions for fungal diversity in Danish beech forests. For Ecol Manag 201:105–117. https://doi.org/10.1016/j.foreco.2004.07.010
Heilmann-Clausen J, Aude E, van Dort K, Christensen M, Piltaver A, Veerkamp M, Walleyn R, Siller I, Standovár T, Òdor P (2014) Communities of wood-inhabiting bryophytes and fungi on dead beech logs in Europe—reflecting substrate quality or shaped by climate and forest conditions? J Biogeogr 41:2269–2282. https://doi.org/10.1111/jbi.12388
Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon F, Eriksson OE, Huhndorf S, James T, Kirk PM, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Bauer R, Begerow D, Benny GL, Lisa A, Crous PW, Dai Y-C, Gams W, Geiser DM, Griffith GW, Hosaka K, Humber RA, Hyde KD, Ironside JE, Kurtzman CP, Larsson K-H, Lichtwardt R, Mia J, Mozley-Standridge S, Oberwinkler F, Parmasto E, Sampaio P, Rogers JD, Roux C, Ryvarden L, Sugiyama J, Thorn RG, Tibell L, Wendy A, Walker C, Wang Z, Weir A, Weiss M, Cannon PF, Lücking R, Lumbsch TH, Lutzoni F, Aptroot A, Castlebury LA, Gueidan C, Hawksworth DL, Hestmark G, Koljalg U, Longcore J, Miadlikowska J, Miller A, Moncalvo J-M, Reeb V, Sampaio JP, Schüßler A, Untereiner WA, White MM, Winka K, Yao Y-J, Zhang N (2007) A higher-level phylogenetic classification of the fungi. Mycol Res 111:509–547. https://doi.org/10.1016/j.mycres.2007.03.004
Hunt T, Bergsten J, Levkanicova Z, Papadopoulou A, John OS, Wild R, Hammond PM, Ahrens D, Balke M, Caterino MS, Gomez-Zurita J, Ribera I, Barraclough TG, Bocakova M, Bocak L, Vogler AP (2007) A comprehensive phylogeny of beetles reveals the evolutionary origins of a superradiation. Science 318:1913–1916. https://doi.org/10.1126/science.1146954
Katoh K, Kuma KI, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518. https://doi.org/10.1093/nar/gki198
Krah F-S, Seibold S, Brandl R, Baldrian P, Müller J, Bässler C (2018) Independent effects of host and environment on the diversity of wood-inhabiting fungi. J. Ecol 106:1428–1442. https://doi.org/10.1111/1365-2745.12939
Kuhn TS, Mooers A, Thomas GH (2011) A simple polytomy resolver for dated phylogenies. Methods Ecol Evol 2:427–436. https://doi.org/10.1111/j.2041-210X.2011.00103.x
Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24. https://doi.org/10.1890/0012-9615(1999)069[0001:DBRATM]2.0.CO;2
Lindhe A, Lindelöw Å, Åsenblad N (2005) Saproxylic beetles in standing dead wood density in relation to substrate sun-exposure and diameter. Biodivers Conserv 14:3033–3053. https://doi.org/10.1007/s10531-004-0314-y
Mayfield MM, Levine JM (2010) Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecol Lett 13:1085–1093. https://doi.org/10.1111/j.1461-0248.2010.01509.x
Mouillot D, Graham NAJJ, Villéger S, Mason NWH, Bellwood DR (2013) A functional approach reveals community responses to disturbances. Trends Ecol Evol 28:167–177. https://doi.org/10.1016/j.tree.2012.10.004
Müller J, Bütler R (2010) A review of habitat thresholds for dead wood: a baseline for management recommendations in European forests. Eur J For Res 129:981–992. https://doi.org/10.1007/s10342-010-0400-5
Müller J, Noss RF, Bussler H, Brandl R (2010) Learning from a “benign neglect strategy” in a national park: response of saproxylic beetles to dead wood accumulation. Biol Conserv 143:2559–2569. https://doi.org/10.1016/j.biocon.2010.06.024
Müller J, Jarzabek-Müller A, Bussler H, Gossner MM (2014) Hollow beech trees identified as keystone structures for saproxylic beetles by analyses of functional and phylogenetic diversity. Anim Conserv 17:154–162. https://doi.org/10.1111/acv.12075
Müller J, Brustel H, Brin A, Bussler H, Bouget C, Obermaier E, Heidinger IMM, Lachat T, Förster B, Horak J, Prochazka J, Köhler F, Larrieu L, Bense U, Isacsson G, Zapponi L, Gossner MM (2015) Increasing temperature may compensate for lower amounts of dead wood in driving richness of saproxylic beetles. Ecography 38:499–509. https://doi.org/10.1111/ecog.00908
Nordén J, Penttil R, Siitonen J, Tomppo E, Ovaskainen O, Nord J, Nordén J, Penttilä R (2013) Specialist species of wood-inhabiting fungi struggle while generalists thrive in fragmented boreal forests. J Ecol 101:701–712. https://doi.org/10.1111/1365-2745.12085
Pausas JG, Verdú M (2010) The jungle of methods for evaluating phenotypic and phylogenetic structure of communities. Bioscience 60:614–625. https://doi.org/10.1525/bio.2010.60.8.7
Penttilä R, Siitonen J, Kuusinen M (2004) Polypore diversity in managed and old-growth boreal Picea abies forests in southern Finland. Biol Conserv 117:271–283. https://doi.org/10.1016/j.biocon.2003.12.007
Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87:2614–2625. https://doi.org/10.1890/0012-9658(2006)87[2614:VPOSDM]2.0.CO;2
Petchey OL, Gaston KJ (2002a) Functional diversity (FD), species richness and community composition. Ecol Lett 5:402–411. https://doi.org/10.1046/j.1461-0248.2002.00339.x
Petchey OL, Gaston KJ (2002b) Extinction and the loss of functional diversity. Proc Biol Sci 269:1721–1727. https://doi.org/10.1098/rspb.2002.2073
Petchey OL, Evans KL, Fishburn IS, Gaston KJ (2007) Low functional diversity and no redundancy in British avian assemblages. J Anim Ecol 76:977–985. https://doi.org/10.1111/j.1365-2656.2007.01271.x
Purahong W, Wubet T, Krüger D, Buscot F (2018) Molecular evidence strongly supports deadwood-inhabiting fungi exhibiting unexpected tree species preferences in temperate forests. ISME J 12:289–295. https://doi.org/10.1038/ismej.2017.177
Reymond A, Purcell J, Cherix D, Guisan A, Pellissier L (2013) Functional diversity decreases with temperature in high elevation ant fauna. Ecol Entomol 38:364–373. https://doi.org/10.1111/een.12027
Rinaldi AC, Comandini O, Kuyper TW (2007) Ectomycorrhizal fungal diversity: separating the wheat from the claff. Fungal Divers 33:1–45
Schmidl J, Bußler H (2004) Ökologische Gilden xylobionter Käfer Deutschlands. Naturschutz und Landschaftsplan 36:202–218
Schowalter T (2006) Insect ecology: an ecosystem approach. Elsevier, San Diego
Seibold S, Bässler C, Brandl R, Gossner MM, Thorn S, Ulyshen MD, Müller J (2015a) Experimental studies of dead-wood biodiversity—a review identifying global gaps in knowledge. Biol Conserv 191:139–149. https://doi.org/10.1016/j.biocon.2015.06.006
Seibold S, Brandl R, Buse J, Hothorn T, Schmidl J, Thorn S, Müller J (2015b) Association of extinction risk of saproxylic beetles with ecological degradation of forests in Europe. Conserv Biol 29:382–390. https://doi.org/10.1111/cobi.12427
Seibold S, Bässler C, Brandl R, Büche B, Szallies A, Thorn S, Ulyshen MD, Müller J (2016) Microclimate and habitat heterogeneity as the major drivers of beetle diversity in dead wood. J Appl Ecol 53:934–943. https://doi.org/10.1111/1365-2664.12607
Sibly RM, Brown JH, Kodric-Brown A (eds) (2012) Metabolic ecology: a scaling approach. Wiley. https://doi.org/10.1002/9781119968535
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Steffen W, Richardson K, Rockström J, Cornell SE, Fetzer I, Bennett EM, Biggs R, Carpenter SR, Vries W De, Wit CA De, Folke C, Gerten D, Heinke J, Mace GM, Persson LM, Ramanathan V, Reyers B, Sörlin S, Rockstrom J, Cornell SE, Fetzer I, Bennett EM, Biggs R, Carpenter SR, de Vries W, de Wit CA, Folke C, Gerten D, Heinke J, Mace GM, Persson LM, Ramanathan V, Reyers B, Sorlin S (2015) Planetary boundaries: guiding human development on a changing planet. Science 347:1259855. https://doi.org/10.1126/science.1259855
Stokland JN, Siitonen J, Jonsson BG (2012) Biodiversity in dead wood. Cambridge University Press, Octavo
Sverdrup-Thygeson A, Birkemoe T (2009) What window traps can tell us: effect of placement, forest openness and beetle reproduction in retention trees. J Insect Conserv 13:183–191. https://doi.org/10.1007/s10841-008-9141-x
Thorn S, Bässler C, Gottschalk T, Hothorn T, Bussler H, Raffa K, Müller J (2014) New insights into the consequences of post-windthrow salvage logging revealed by functional structure of saproxylic beetles assemblages. PLoS ONE 9:e101757. https://doi.org/10.1371/journal.pone.0101757
Thorn S, Bässler C, Svoboda M, Müller J (2017) Effects of natural disturbances and salvage logging on biodiversity—lessons from the Bohemian Forest. For Ecol Manag 388:113–119. https://doi.org/10.1016/j.comnet.2006.11.031
Thuiller W, Maiorano L, Mazel F, Guilhaumon F, Ficetola GF, Lavergne S, Renaud J, Roquet C, Mouillot D (2015) Conserving the functional and phylogenetic trees of life of European tetrapods. Philos Trans R Soc Lond B Biol Sci. https://doi.org/10.1098/rstb.2014.0005
Villeger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301. https://doi.org/10.1890/07-1206.1
Webb CO, Ackerly DD, Mcpeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505. https://doi.org/10.1146/annurev.ecolsys.33.010802.150448
Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098–2100. https://doi.org/10.1093/bioinformatics/btn358
Wikars L-O, Sahlin E, Ranius T (2005) A comparison of three methods to estimate species richness of saproxylic beetles (Coleoptera) in logs and high stumps of Norway spruce. Can Entomol 137:304–324. https://doi.org/10.4039/n04-104
Winter M, Devictor V, Schweiger O (2013) Phylogenetic diversity and nature conservation: where are we? Trends Ecol. Evol 28:199–204. https://doi.org/10.1016/j.tree.2012.10.015
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This research was supported by the Bavarian State Ministry of the Environment, Public Health, and Consumer Protection. We are grateful to Christoph Hahn and Heinrich Holzer for support in field work. We thank Karen A. Brune for linguistic revision of the manuscript.
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Thorn, S., Förster, B., Heibl, C. et al. Influence of macroclimate and local conservation measures on taxonomic, functional, and phylogenetic diversities of saproxylic beetles and wood-inhabiting fungi. Biodivers Conserv 27, 3119–3135 (2018). https://doi.org/10.1007/s10531-018-1592-0
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DOI: https://doi.org/10.1007/s10531-018-1592-0