Fungal Diversity

, Volume 66, Issue 1, pp 139–151 | Cite as

No plant functional diversity effects on foliar fungal pathogens in experimental tree communities

  • Lydia Hantsch
  • Uwe Braun
  • Josephine Haase
  • Oliver Purschke
  • Michael Scherer-Lorenzen
  • Helge Bruelheide
Article

Abstract

Foliar fungal pathogens affect forest ecosystem processes by exerting highly species-specific impacts on growth and survival of trees. As many ecosystem processes in forests depend on functional diversity of specific tree species, a close relationship is expected between this and foliar fungal pathogen infestation. Testing for such a relationship in the German tree diversity experiment BIOTREE (Bechstedt), we hypothesized that pathogen richness and pathogen load decline with increasing functional diversity of tree communities. Using macro- and microscopic analyses, we assessed pathogen richness and load on 16 tree species in plots that, although differing in functional diversity, had the same tree species richness. We found no effects of functional diversity on pathogen richness or load. However, we encountered strong species identity effects in plot species composition, as susceptible tree species contributed positively to each community’s pathogen richness and load. Furthermore, testing for effects of particular leaf traits and geographical range size of host species revealed a significant effect of total leaf phenolics, which was unexpected as pathogen richness increased with increasing content in polyphenolics. Our study showed that at the community level, host species’ identity was more important for foliar fungal pathogen richness and load than the functional diversity of host trees. The positive relationship between pathogen richness and phenolics in leaves, along with the finding that pathogen richness is very much conserved in tree species, point to an evolutionary arms race between hosts and fungi resulting from fungi increasing their capacity to infect tree leaves and trees boosting their defences.

Keywords

Biodiversity–ecosystem functioning BIOTREE experiment Host defence traits Phylogenetic pattern Polyphenolics Tree species identity effects 

Notes

Acknowledgments

We are grateful to M. Baudis for helping with the field work. For technical support on leaf trait analyses, we thank D. Eichenberg, C. Ristok, K. Schmon and S. Wedi-Pumpe. Thanks are due to G. Seidler for providing tree species’ range sizes. For the analysis of leaf areas, we used the free Lafore software (LeafAreaFOREveryone, © V. Lehsten, Oldenburg, Germany). A Graduate Scholarship of Saxony-Anhalt and a grant from the Scholarship Programme of the German Federal Environmental Foundation (DBU) are highly acknowledged. The research leading to these results also attracted funding from the European Union’s Seventh Framework Programme (FP7/2007–2013) under grant agreement no. 265171, project FunDivEUROPE as well as of the BACCARA project, which received funding from the European Commission’s Seventh Framework Programme (FP7/2007–2013), under grant agreement no. 226299. O.P. and H.B. also acknowledge the support of the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, funded by the German Science Foundation (FZT 118).

Supplementary material

13225_2013_273_MOESM1_ESM.docx (4.2 mb)
ESM 1 (DOCX 4283 kb)

References

  1. Allen E, van Ruijven J, Crawley MJ (2010) Foliar fungal pathogens and grassland biodiversity. Ecology 91:2572–2582CrossRefGoogle Scholar
  2. Azaiez A, Boyle B, Levée V, Séguin A (2009) Transcriptome profiling in hybrid poplar following interactions with Melampsora rust fungi. MPMI 22:190–200PubMedCrossRefGoogle Scholar
  3. Bagchi R, Swinfield T, Gallery RE, Lewis OT, Gripenberg S, Narayan L, Freckleton RP (2010) Testing the Janzen-Connell mechanism: pathogens cause overcompensating density dependence in a tropical tree. Ecol Lett 13:1262–1269PubMedCrossRefGoogle Scholar
  4. Blodgett JT, Herms DA, Bonello P (2005) Effects of fertilization on red pine defense chemistry and resistance to Sphaeropsis sapinea. For Ecol Manage 208:373–382CrossRefGoogle Scholar
  5. Blomberg SP, Garland T, Ives AR, Crespi B (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745PubMedCrossRefGoogle Scholar
  6. Böhnke M, Kröber W, Welk E, Wirth C, Bruelheide H (2013) Maintenance of constant functional diversity during secondary succession of a subtropical forest in China. J Veg Sci. doi: 10.1111/jvs.12114 Google Scholar
  7. Botta-Dukát Z (2005) Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. J Veg Sci 16:533–540CrossRefGoogle Scholar
  8. Bradley DJ, Gilbert GS, Parker IM (2003) Susceptibility of clover species to fungal infection: The interaction of leaf surface traits and environment. Am J Bot 90:857–864PubMedCrossRefGoogle Scholar
  9. Brandenburger W (1985) Parasitische Pilze an Gefäßpflanzen in Europa. Gustav Fischer Verlag, StuttgartGoogle Scholar
  10. Braun U, Cook RTA (2012) Taxonomic Manual of the Erysiphales (Powdery Mildews). CBS Biodiversity Series 11:1–707Google Scholar
  11. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67PubMedCrossRefGoogle Scholar
  12. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: Shaping the evolution of the plant immune response. Cell 124:803–814PubMedCrossRefGoogle Scholar
  13. Clay K, Kover PX (1996a) Evolution and stasis in plant-pathogen associations. Ecology 77:997–1003CrossRefGoogle Scholar
  14. Clay K, Kover PX (1996b) The red queen hypothesis and plant/pathogen interactions. Annu Rev Phytopathol 34:29–50PubMedCrossRefGoogle Scholar
  15. Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: de Boer PJ, Gradwell GR (eds) Dynamics of Populations. Center for Agricultural Publishing and Documentation, Wageningen, pp 298–312Google Scholar
  16. Crous PW, Braun U (2003) Mycosphaerella and its anamorphs: 1. Names published in Cercospora and Passalora. CBS Biodiversity Series 1:1–500Google Scholar
  17. Crous PW, Braun U, Hunter GC, Wingfield MJ, Verkley GJM, Shin HD, Nakashima C, Groenewald JC (2012) Phylogenetic lineages in Pseudocercospora. Stud Mycol 75:37–114PubMedCentralCrossRefGoogle Scholar
  18. Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc Lond B 205:489–511Google Scholar
  19. Díaz S, Hodgson JG, Thompson K, Cabido M, Cornelissen JHC, Jalili A, Montserrat-Martí G, Grime JP, Zarrinkamar F, Asri Y, Band SR, Basconcelo S, Castro-Díez P, Funes G, Hamzehee B, Khoshnevi M, Pérez-Harguindeguy N, Pérez-Rontomé MC, Shirvany FA, Vendramini F, Yazdani S, Abbas-Azimi R, Bogaard A, Boustani S, Charles M, Dehghan M, de Torres-Espuny L, Falczuk V, Guerrero-Campo J, Hynd A, Jones G, Kowsary E, Kazemi-Saeed F, Maestro-Martínez M, Romo-Díez A, Shaw S, Siavash B, Villar-Salvador P, Zak MR (2004) J Veg Sci 15:295–304CrossRefGoogle Scholar
  20. Díaz S, Lavorel S, Chapin FS, Tecco PA, Gurvich DE, Grigulis K (2007) In: Canadell J, Pataki DE, Pitelka LF (eds) Terrestrial Ecosystem in a Changing World. Springer, Berlin, pp 79–91Google Scholar
  21. Don A, Arenhövel W, Jacob R, Scherer-Lorenzen M, Schulze E-D (2007) Establishment success of 19 different tree species on afforestations – Results of a biodiversity experiment. AFJZ 178:164–171Google Scholar
  22. Duplessis S, Major I, Martin F, Séguin A (2009) Poplar and pathogen interactions: Insights from populus genome-wide analyses of resistance and defense gene families and gene expression profiling. Crit Rev Plant Sci 28:309–334CrossRefGoogle Scholar
  23. Durka W, Michalski SG (2012) Daphne: a dated phylogeny of a large European flora for phylogenetically informed ecological analyses. Ecology 93:2297Google Scholar
  24. Eisenhauer N, Beßler H, Engels C, Gleixner G, Habekost M, Milcu A, Partsch S, Sabais ACW, Scherber C, Steinbeiss S, Weigelt A, Weisser WW, Scheu S (2010) Plant diversity effects on soil microorganisms support the singular hypothesis. Ecology 91:485–496PubMedCrossRefGoogle Scholar
  25. Eisenhauer N, Milcu A, Allan E, Nitschke N, Scherber C, Temperton V, Weigelt A, Weisser WW, Scheu S (2011) Impact of above- and below-ground invertebrates on temporal and spatial stability of grassland of different diversity. J Ecol 99:572–582Google Scholar
  26. El-Hajj Z, Kavanagh K, Rose C, Kanaan-Atallah Z (2004) Nitrogen and carbon dynamics of a foliar biotrophic fungal parasite in fertilized Douglas-fir. New Phytol 163:139–147CrossRefGoogle Scholar
  27. Ellis MB, Ellis JP (1997) Microfungi on land plants: an identification handbook, 2nd edn. Richmond Pub, University of MichiganGoogle Scholar
  28. Fernández-Aparicio M, Prats E, Emeran AA, Rubiales D (2009) Characterization of resistance mechanisms to powdery mildew (Erysiphe betae) in beet (Beta vulgaris). Phytopathology 99:385–389PubMedCrossRefGoogle Scholar
  29. Gilbert GS, Webb CO (2007) Phylogenetic signal in plant pathogen–host range. PNAS 104:4979–4983PubMedCentralPubMedCrossRefGoogle Scholar
  30. Gilbert GS, Magarey R, Suiter K, Webb CO (2012) Evolutionary tools for phytosanitary risk analysis: phylogenetic signal as a predictor of host range of plant pests and pathogens. Evol Appl 5:869–878PubMedCentralPubMedCrossRefGoogle Scholar
  31. Hacquard S, Petre B, Frey P, Hecker A, Rouhier N, Duplessis S (2011) The poplar-poplar rust interaction: Insights from genomics and transcriptomics. J Pathog. doi: 10.4061/2011/716041 PubMedCentralPubMedGoogle Scholar
  32. Hajji M, Dreyer E, Marçais B (2009) Impact of Erysiphe alphitoides on transpiration and photosynthesis in Quercus robur leaves. Eur J Plant Pathol 125:63–72CrossRefGoogle Scholar
  33. Hantsch L, Braun U, Scherer-Lorenzen M, Bruelheide H (2013) Species richness and species identity effects on occurrence of foliar fungal pathogens in a tree diversity experiment. Ecosphere 4:81CrossRefGoogle Scholar
  34. Huang WY, Cai YZ, Hyde KD, Corke H, Sun M (2008) Biodiversity of endophytic fungi associated with 29 traditional Chinese medicinal plants. Fung Divers 33:61–75Google Scholar
  35. Humphries CJ, Cox JM, Nielsen ES (1986) Nothofagus and its parasites: a cladistic approach to coevolution. In: Stone AR, Hawksworth DL (eds) Coevolution and systematics. Clarendon Press, Oxford, pp 55–76Google Scholar
  36. Iason GR, Lennon JJ, Pakeman RJ, Thoss V, Beaton JK, Sim DA, Elston DA (2005) Does chemical composition of individual Scots pine trees determine the biodiversity of their associated ground vegetation? Ecol Lett 8:364–369CrossRefGoogle Scholar
  37. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–508CrossRefGoogle Scholar
  38. Jones CG, Lawton JH (1991) Plant chemistry and insect species richness of British Umbellifers. J Anim Ecol 60:767–777CrossRefGoogle Scholar
  39. Keen NT (1990) Gene-for-gene complementarity in plant-pathogen interactions. Annu Rev Genet 24:447–463PubMedCrossRefGoogle Scholar
  40. Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecol Lett 9:485–498PubMedCrossRefGoogle Scholar
  41. Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647–652Google Scholar
  42. Kloppholz S, Kuhn H, Requena N (2011) A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr Biol 21:1204–1209PubMedCrossRefGoogle Scholar
  43. Kröner A, Marnet N, Andrivon D, Val F (2012) Nicotiflorin, rutin and chlorogenic acid: phenylpropanoids involved differently in quantitative resistance of potato tubers to biotrophic and necrotrophic pathogens. Plant Physiol Biochem 57:23–31PubMedCrossRefGoogle Scholar
  44. Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, Dunne JA, Johnson PTJ, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J, Marquet PA, McLaughlin JP, Mordecai EA, Pascual M, Poulin R, Thieltges DW (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11:533–546PubMedCentralPubMedCrossRefGoogle Scholar
  45. Lavandero B, Labra A, Ramírez CC, Niemeyer HM, Fuentes-Contreras E (2009) Species richness of herbivorous insects on Nothofagus trees in South America and New Zealand: The importance of chemical attributes of the host. Basic Appl Ecol 10:10–18CrossRefGoogle Scholar
  46. Lavorel S, Garnier E (2002) Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct Ecol 16:545–556CrossRefGoogle Scholar
  47. Legendre P, Legendre L (2012) Numerical Ecology, 3rd English edn. ElsevierGoogle Scholar
  48. Lewinsohn TM, Novotny V, Basset Y (2005) Insects on plants: Diversity of herbivore assemblages revisited. Annu Rev Ecol Evol Syst 36:597–620CrossRefGoogle Scholar
  49. Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: Current knowledge and future challenges. Science 294:804–808PubMedCrossRefGoogle Scholar
  50. Maor R, Shirasu K (2005) The arms race continues: battle strategies between plants and fungal pathogens. Curr Opin Microbiol 8:399–404PubMedCrossRefGoogle Scholar
  51. Mason NWH, MacGillivray K, Steel JB, Wilson JB (2003) An index of functional diversity. J Veg Sci 14:71–578CrossRefGoogle Scholar
  52. McElrone AJ, Reid CD, Hoye KA, Hart E, Jackson RB (2005) Elevated CO2 reduces disease incidence and severity of a red maple fungal pathogen via changes in host physiology and leaf chemistry. Glob Chang Biol 11:1828–1836CrossRefGoogle Scholar
  53. Mitchell CE, Blumenthal D, Jarošik V, Pukett EE, Pyšek P (2010) Controls on pathogen species richness in plants introduced and native ranges: roles of residence time, range size and host traits. Ecol Lett 13:1525–1535PubMedCentralPubMedCrossRefGoogle Scholar
  54. Moore SM, Borer ET (2012) The influence of host diversity and composition on epidemiological patterns at multiple spatial scales. Ecology 93:1095–1105PubMedCrossRefGoogle Scholar
  55. Mouillot D, Villéger S, Scherer-Lorenzen M, Mason NWH (2011) Functional structure of biological communities predicts ecosystem multifunctionality. PLoS ONE 6:e17476PubMedCentralPubMedCrossRefGoogle Scholar
  56. Mraja A, Unsicker SB, Reichelt M, Gershenzon J, Roscher C (2011) Plant community diversity influences allocation to direct chemical defence in Plantago lanceolata. PLoS ONE 6:e28055PubMedCentralPubMedCrossRefGoogle Scholar
  57. Nadrowski K, Wirth C, Scherer-Lorenzen M (2010) Is forest diversity driving ecosystem function and service? Curr Opin Environ Sustainability 2:75–79CrossRefGoogle Scholar
  58. Naeem S, Li S (1997) Biodiversity enhances ecosystem reliability. Nature 390:507–509CrossRefGoogle Scholar
  59. Naeem S, Loreau M, Inchausti P (2002) Biodiversity and ecosystem functioning: the emergence of a synthetic ecological framework. In: Loreau M, Naeem S, Inchausti P (eds) Biodiversity and ecosystem functioning. Oxford University Press, Oxford, pp 3–11Google Scholar
  60. Petchey OL (2004) On the statistical significance of functional diversity effects. Func Ecol 18:297–303CrossRefGoogle Scholar
  61. Petchey OL, Gaston KJ (2002a) Extinction and the loss of functional diversity. Proc R Soc Lond 269:1721–1727CrossRefGoogle Scholar
  62. Petchey OL, Gaston KJ (2002b) Functional diversity (FD), species richness and community composition. Ecol Lett 5:402–411CrossRefGoogle Scholar
  63. Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758PubMedCrossRefGoogle Scholar
  64. Pociecha E, Płażek A, Janowiak F, Waligórski P, ZwierZykowski Z (2009) Changes in abscisic acid, salicylic acid and phenylpropanoid concentrations during cold acclimation of androgenic forms of Festulolium (Festuca pratensis × Lolium multiflorum) in relation to resistance to pink snow mould (Microdochium nivale). Plant Breed 128:397–403CrossRefGoogle Scholar
  65. Prell H (1996) Interaktionen von Pflanzen und phytopathogenen Pilzen. Gutav Fischer Verlag, Jena, StuttgartGoogle Scholar
  66. Proulx R, Wirth C, Voigt W, Weigelt A, Roscher C, Attinger S, Baade J, Barnard RL, Buchmann N, Buscot F, Eisenhauer N, Fischer M, Gleixner G, Halle S, Hildebrandt A, Kowalski E, Kuu A, Lange M, Milcu A, Niklaus PA, Oelmann Y, Rosenkranz S, Sabais A, Scherber C, Scherer-Lorenzen M, Scheu S, Schulze E-D, Schumacher J, Schwichtenberg G, Soussana J-F, Temperton VM, Weisser WW, Wilcke W, Schmid B (2010) Diversity Promotes Temporal Stability across Levels of Ecosystem Organization in Experimental Grasslands. PLoS ONE 5:e13382PubMedCentralPubMedCrossRefGoogle Scholar
  67. Rajala T, Velmala SM, Tuomivirta T, Haapanen M, Müller M, Pennanen T (2013) Endophyte communities vary in the needles of Norway spruce clones. Fung Biol 117:182–190CrossRefGoogle Scholar
  68. Rao CR (1982) Diversity and dissimilarity coefficients: A unified approach. Theor Popul Biol 21:24–43CrossRefGoogle Scholar
  69. R Core Team (2013) R: A language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing. http://www.R-project.org/. Assessed 28 November 2013
  70. Reich PB, Tilman D, Isbell F, Mueller K, Hobbie SE, Flynn DFB, Eisenhauer N (2012) Impacts of Biodiversity Loss Escalate Through Time as Redundancy Fades. Science 336:589–592PubMedCrossRefGoogle Scholar
  71. Roscher C, Weigelt A, Proulx R, Marquard E, Schumacher J, Weisser WW, Schmid B (2011) Identifying population- and community-level mechanisms of diversity–stability relationships in experimental grasslands. J Ecol 99:1460–1469CrossRefGoogle Scholar
  72. Sabais ACW, Scheu S, Eisenhauer N (2011) Plant species richness drives the density and diversity of Collembola in temperate grassland. Acta Oecol 37:195–202CrossRefGoogle Scholar
  73. Sanchez-Azofeifa A, Oki Y, Fernandes GW, Ball RA, Gamon J (2012) Relationships between endophyte diversity and leaf optical properties. Trees 26:291–299CrossRefGoogle Scholar
  74. Scherber C, Eisenhauer N, Weisser WW, Schmid B, Voigt W, Fischer M, Schulze E-D, Roscher C, Weigelt A, Allan E, Beßler H, Bonkowski M, Buchmann N, Buscot F, Clement LW, Ebeling A, Engels C, Halle S, Kertscher I, Klein A-M, Koller R, König S, Kowalski E, Kummer V, Kuu A, Lange M, Lauterbach D, Middelhoff C, Migunova VD, Milcu A, Müller R, Partsch S, Petermann JS, Renker C, Rottstock T, Sabais A, Scheu S, Schumacher J, Temperton VM, Tscharntke T (2010) Bottom up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468:553–556PubMedCrossRefGoogle Scholar
  75. Scherer-Lorenzen M (2008) Functional diversity affects decomposition processes in experimental grasslands. Func Ecol 22:547–555CrossRefGoogle Scholar
  76. Scherer-Lorenzen M, Schulze E-D, Don A, Schumacher J, Weller E (2007) Exploring the functional significance of forest diversity: A new long-term experiment with temperate tree species (BIOTREE). Perspect Plant Ecol Evol Syst 9:53–70CrossRefGoogle Scholar
  77. Schleuter D, Daufresne M, Massol F, Argillier C (2010) A user’s guide to functional diversity indices. Ecol Monogr 80:469–484CrossRefGoogle Scholar
  78. Schubert K, Ritschel A, Braun U (2003) A monograph of Fusicladium s.lat. (Hyphomycetes). Schlechtendalia 9:1–132Google Scholar
  79. Schuldt A, Bruelheide H, Durka W, Eichenberg D, Fischer M, Kröber W, Härdtle W, Keping M, Michalski SG, Palm WU, Schmid B, Welk E, Zhou H, Assmann T (2012) Plant traits affecting herbivory on tree recruits in highly diverse subtropical forests. Ecol Lett 15:732–739PubMedCrossRefGoogle Scholar
  80. Shanmugam V, Ronen M, Shalaby S, Larkov O, Rachamim Y, Hadar R, Rose MS, Carmeli S, Horwitz BA, Lev S (2010) The fungal pathogen Cochliobolus heterostrophus responds to maize phenolics: novel small molecule signals in a plant-fungal interaction. Cell Microbiol 12:1421–1434PubMedCrossRefGoogle Scholar
  81. Shetty R, Fretté X, Jensen B, Shetty NP, Jensen JD, Jørgensen HJL, Newman M-A, Christensen LP (2011) Silicon-induced changes in antifungal phenolic acids, flavonoids, and key phenylpropanoid pathway genes during the interaction between miniature roses and the biotrophic pathogen Podosphaera pannosa. Plant Physiol 157:2194–2205PubMedCentralPubMedCrossRefGoogle Scholar
  82. Sonnemann I, Baumhaker H, Wurst S (2012) Species specific responses of common grassland plants to a generalist root herbivore (Agriotes spp. larvae). Basic Appl Ecol 13:579–586CrossRefGoogle Scholar
  83. Specht J, Scherber C, Unsicker SB, Köhler G, Weisser WW (2008) Diversity and beyond: plant functional identity determines herbivore performance. J Anim Ecol 77:1047–1055PubMedCrossRefGoogle Scholar
  84. Spehn EM, Joshi J, Schmid B, Alphei J, Körner C (2000) Plant diversity effects on soil heterotrophic activity in experimental grassland ecosystems. Plant Soil 224:217–230CrossRefGoogle Scholar
  85. Suding KN, Lavorel S, Chapin FS III, Cornelissen JHC, Diaz S, Garnier E, Goldberg D, Hooper DU, Jackson ST, Navas M-L (2008) Scaling environmental change through the community-level: A trait-based response-and-effect framework for plants. Glob Chang Biol 14:1125–1140CrossRefGoogle Scholar
  86. Sun X, Ding Q, Hyde KD, Guo LD (2012) Community structure and preference of endophytic fungi of three woody plants in a mixed forest. Fung Ecol 5:624–632CrossRefGoogle Scholar
  87. Swenson NG, Anglada-Cordero P, Barone JA (2011) Deterministic tropical tree community turnover: evidence from patterns of functional beta diversity along an elevational gradient. Proc R Soc London, Ser B 278:877–884CrossRefGoogle Scholar
  88. Tedersoo L, Mett M, Ishida TA, Bahram M (2013) Phylogenetic relationships among host plants explain differences in fungal species richness and community composition in ectomycorrhizal symbiosis. New Phytol 199:822–831PubMedCrossRefGoogle Scholar
  89. Thompson JN (1999) The evolution of species interactions. Science 284:2116–2118PubMedCrossRefGoogle Scholar
  90. Thuiller W, Lavorel S, Sykes MT, Araújo MB (2006) Using niche-based modelling to assess the impact of climate change on tree functional diversity in Europe. Divers Distrib 12:49–60CrossRefGoogle Scholar
  91. Tilman D (2001) Functional diversity. In: Levin SA (ed) Encyclopedia of Biodiversity. Academic Press, San Diego, pp 109–120CrossRefGoogle Scholar
  92. Valkama E, Koricheva J, Salminen J-P, Helander M, Saloniemi I, Saikkonen K, Pihlaja K (2005) Leaf surface traits: overlooked determinants of birch resistance to herbivores and foliar micro-fungi? Trees 19:191–197CrossRefGoogle Scholar
  93. Villar R, Robleto JR, de Jong Y, Poorter H (2006) Differences in construction costs and chemical composition between deciduous and evergreen woody species are small as compared to differences among families. Plant Cell Environ 29:1629–1643PubMedCrossRefGoogle Scholar
  94. Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301PubMedCrossRefGoogle Scholar
  95. Walker BH (1992) Biodiversity and ecological redundancy. Conserv Biol 6:18–23CrossRefGoogle Scholar
  96. Walker B, Kinzig AP, Langridge J (1999) Plant attribute diversity, resilience, and ecosystem function: The nature and significance of dominant and minor species. Ecosystems 2:95–113CrossRefGoogle Scholar
  97. Weiher E, van der Werf A, Thompson K, Roderick M, Garnier E, Eriksson O (1999) Challenging Theophrastus: A common core list of plant traits for functional ecology. J Veg Sci 10:609–620CrossRefGoogle Scholar
  98. Whitfield TJS, Novotny V, Miller SE, Hrcek J, Klimes P, Weiblen GD (2012) Predicting tropical insect herbivore abundance from host plant traits and phylogeny. Ecology 93:S211–S222CrossRefGoogle Scholar
  99. Wright IJ, Reich PB, Westoby M, Ackerly D, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen H, Diemer M, Flexas J, Garnier E, Groom PK, Gullas J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827PubMedCrossRefGoogle Scholar

Copyright information

© Mushroom Research Foundation 2014

Authors and Affiliations

  • Lydia Hantsch
    • 1
  • Uwe Braun
    • 1
  • Josephine Haase
    • 2
    • 4
  • Oliver Purschke
    • 1
    • 3
  • Michael Scherer-Lorenzen
    • 4
  • Helge Bruelheide
    • 1
    • 3
  1. 1.Institute of Biology, Geobotany and Botanical GardenMartin Luther University Halle WittenbergHalle (Saale)Germany
  2. 2.Department of Environmental Systems Science, ETH ZurichEcosystem Management, Institute of Terrestrial EcosystemsZurichSwitzerland
  3. 3.German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzigGermany
  4. 4.Faculty of Biology, GeobotanyAlberts-Ludwigs University of FreiburgFreiburgGermany

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