, Volume 28, Issue 1, pp 39–47 | Cite as

Tree species identity and diversity drive fungal richness and community composition along an elevational gradient in a Mediterranean ecosystem

  • Alessandro SaittaEmail author
  • Sten Anslan
  • Mohammad Bahram
  • Luca Brocca
  • Leho Tedersoo
Original Article


Ecological and taxonomic knowledge is important for conservation and utilization of biodiversity. Biodiversity and ecology of fungi in Mediterranean ecosystems is poorly understood. Here, we examined the diversity and spatial distribution of fungi along an elevational gradient in a Mediterranean ecosystem, using DNA metabarcoding. This study provides novel information about diversity of all ecological and taxonomic groups of fungi along an elevational gradient in a Mediterranean ecosystem. Our analyses revealed that among all biotic and abiotic variables tested, host species identity is the main driver of the fungal richness and fungal community composition. Fungal richness was strongly associated with tree richness and peaked in Quercus-dominated habitats and Cistus-dominated habitats. The highest taxonomic richness of ectomycorrhizal fungi was observed under Quercus ilex, whereas the highest taxonomic richness of saprotrophs was found under Pinus. Our results suggest that the effect of plant diversity on fungal richness and community composition may override that of abiotic variables across environmental gradients.


Biodiversity Ectomycorrhizal fungi Metabarcoding Quercus ilex Sicily 


Funding information

This study was funded by the Estonian Research Foundation grant (PUT1317).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Alday JG, de Aragón JM, de-Miguel S, Bonet JA (2017) Mushrooms biomass and diversity are driven by different spatio-temporal scales along Mediterranean elevation gradients. Sci Rep 7:45824. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aponte C, García L, Maraņķn T, Gardes M (2010) Indirect host effect on ecto-mycorrhizal fungi: leaf fall and litter quality explain changes in fungal communities on the roots of co-occurring Mediterranean oaks. Soil Bio Biochem 42:788–796. CrossRefGoogle Scholar
  3. Bahram M, Põlme S, Kõljalg U, Zarre S, Tedersoo L (2012) Regional and local patterns of ectomycorrhizal fungal diversity and community structure along an altitudinal gradient in the Hyrcanian forests of northern Iran. New Phytol 193:465–473. CrossRefPubMedGoogle Scholar
  4. Barbera G (1996) Il sistema agricolo dell’isola di Pantelleria. In: AA. VV. (eds.) Piano territoriale Paesistico dell’isola di Pantelleria, p 58Google Scholar
  5. Bödeker ITM, Lindahl BD, Olson Ä, Clemmensen KE (2016) Funct Ecol 30:1967–1978. CrossRefGoogle Scholar
  6. Brooks TM, Mittermeier RA, Mitiermeie CG, da Fonseca GAB, Rylands AB, Konstant WR et al (2002) Habitat loss and extinction in the hotspots of biodiversity. Conserv Biol 16:909–923. CrossRefGoogle Scholar
  7. Bruns TD, Bidartondo MI, Taylor DL (2002) Host specificity in ectomycorrhyzal communities: what do the exceptions tell us? Integr Comp Biol 42(2):352–359. CrossRefPubMedGoogle Scholar
  8. Calò C, Henne PD, Eugster P et al (2013) 1200 years of decadal-scale variability of Mediterranean vegetation and climate at Pantelleria Island, Italy. The Holocene 23(10):1477–1486. CrossRefGoogle Scholar
  9. Coince A, Cordier T, Lengellé J, Defossez E, Vacher C, Robin C, Buée M, Marçais B (2014) Leaf and root-associated fungal assemblages do not follow similar elevational diversity patterns. PLoS One 9(6):e100668. CrossRefPubMedPubMedCentralGoogle Scholar
  10. David TS, Henriques MO, Kurz-Besson C, Nunes J, Valente F, Vaz M, Pereira JS, Siegwolf R, Chaves MM, Gazarini LC, David JS (2007) Water-use strategies in two co-occurring Mediterranean evergreen oaks: surviving the summer drought. Tree Physiol 27(6):793–803. CrossRefPubMedGoogle Scholar
  11. Davison J, Moora M, Öpik M, Adholeya A, Ainsaar L, Bâ A, Burla S, Diedhiou AG, Hiiesalu I, Jairus T, Johnson NC, Kane A, Koorem K, Kochar M, Ndyaie D, Pärtel M, Reier Ü, Saks Ü, Sing R, Vasar M, Zobel M (2015) Fungal symbionts. Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349(6251):970–973. CrossRefPubMedGoogle Scholar
  12. Fu L, Niu B, Zhu Z, Wu S, Li W (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28(23):3150–3152. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gai JP, Tian H, Yang FY, Christie P, Li XL, Klironomos JN (2012) Arbuscular mycorrhizal fungal diversity along a Tibetan elevation gradient. Pedobiologia 55:145–151. CrossRefGoogle Scholar
  14. Gamfeldt L, Snäll T, Bagchi R et al (2013) Higher levels of multiple ecosystem services are found in forests with more tree species. Nat Commun 4:1340. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gao C, Shi NN, Chen L, Ji NN, Wu BW, Wang YL, Xu Y, Zheng Y, Mi XC, Ma KP, Guo LD (2016) Relationships between soil fungal and woody plant assemblages differ between ridge and valley habitats in a subtropical mountain forest. New Phytol 213(4):1874–1885. CrossRefPubMedGoogle Scholar
  16. Geml J (2017) Altitudinal gradients in mycorrhizal symbiosis. Ecol Stud 230:107–123CrossRefGoogle Scholar
  17. Geml J, Pastor N, Fernandez L, Pacheco S, Semenova TA, Becerra AG, Wicaksono CY, Nouhra ER (2014) Large-scale fungal diversity assessment in the Andean Yungas forests reveals strong community turnover among forest types along an altitudinal gradient. Mol Ecol 23:2452–2472. CrossRefPubMedGoogle Scholar
  18. Geml J, Morgado LN, Semenova-Nelsen TA, Schilthuizen M (2017) Changes in richness and community composition of ectomycorrhizal fungi among altitudinal vegetation types on Mount Kinabalu in Borneo. New Phytol.
  19. Gianguzzi L (1999) Il paesaggio vegetale dell'Isola di Pantelleria. Collana Sicilia Foreste 8, Azienda Foreste Demaniali della Regione Siciliana, pp. 192. PalermoGoogle Scholar
  20. Gómez-Hernández M, Williams-Linera G, Guevara R, Lodge DJ (2012) Patterns of macromycete community assemblage along an altitudinal gradient: options for fungal gradient and metacommunity analyses. Biodivers Conserv 21:2247–2268. CrossRefGoogle Scholar
  21. Guarino R (2006) On the origin and evolution of the Mediterranean dry grasslands. Berichte Der Reinhold-Tuxen-Gesellschaft 18:195–206Google Scholar
  22. Hiiesalu I, Pärtel M, Davison J, Gerhold P, Metsis M, Moora M, Öpik M, Vasar M, Zober M, Wilson SD (2014) Species richness of arbuscular mycorrhizal fungi: associations with grassland plant richness and biomass. New Phytol 203:233–244. CrossRefPubMedGoogle Scholar
  23. Ishida TA, Nara K, Hogetsu T (2007) Host effects on ectomycorrhizal fungal communities: insight from eight host species in mixed conifer–broadleaf forests. New Phytol 174:430–440. CrossRefPubMedGoogle Scholar
  24. Kernaghan G, Harper KA (2001) Community structure of ectomycorrhizal fungi across an alpine/subalpine ecotone. Ecography 24:181–188. CrossRefGoogle Scholar
  25. Kõljalg U, Nilsson RH, Abarenkov K et al (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277. CrossRefPubMedGoogle Scholar
  26. Lugo MA, Negritto MA, Jofré M, Anton A, Galetto L (2012) Colonization of native Andean grasses by arbuscular mycorrhizal fungi in Puna: a matter of altitude, host photosynthetic pathway and host life cycles. FEMS Microbiol Ecol 81:455–466. CrossRefPubMedGoogle Scholar
  27. McCain CM, Grytnes JA (2010) Elevational gradients in species richness. In: Encyclopedia of Life Sciences (ELS). John Wiley & Sons, Ltd: Chichester. doi:
  28. Meier CL, Rapp J, Bowers RM, Silman M, Fierer N (2010) Fungal growth on a common wood substrate across a tropical elevation gradient: temperature sensitivity, community composition, and potential for above-ground decom-position. Soil Bio Biochem 42:1083–1090. CrossRefGoogle Scholar
  29. Merckx VSFT, Hendriks KP, Beentjes KK, Mennes CB, Becking LE, Peijnenburg KTCA, Afendy A, Arumugam N, de Boer H, Biun A et al (2015) Evolution of endemism on a young tropical mountain. Nature 524:347–350. CrossRefPubMedGoogle Scholar
  30. Miyamoto Y, Nakano T, Hattori M, Nara K (2014) The mid-domain effect in ectomycorrhizal fungi: range overlap along an elevation gradient on Mount Fuji, Japan. ISME J 8:1739–1746. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Miyamoto Y, Sakai A, Hattori M, Nara K (2015) Strong effect of climate on ectomycorrhizal fungal composition: evidence from range overlap between two mountains. ISME J 9:1870–1879. CrossRefPubMedPubMedCentralGoogle Scholar
  32. Nadrowski K, Wirth C, Scherer-Lorenzen M (2010) Is forest diversity driving ecosystem function and service? Curr Opin Env Sust 2:75–79. CrossRefGoogle Scholar
  33. Nouhra E, Urcelay C, Longo S, Fontenla S (2012) Differential hypogeous sporocarp production from Nothofagus dombeyi and N. pumilio forests in southern Argentina. Mycologia 104:45–52. CrossRefPubMedGoogle Scholar
  34. Ortega A, Lorite J (2007) Macrofungi diversity in cork-oak and holm-oak forests in Andalusia (southern Spain); an efficient parameter for establishing priorities for its evaluation and conservation. Cent Eur J Biol 2:276–296. Google Scholar
  35. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol S 37:637–669. CrossRefGoogle Scholar
  36. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. CrossRefPubMedGoogle Scholar
  37. Peay KG, Bruns TD, Kennedy PG, Bergemann SE, Garbelotto M (2007) A strong species–area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi. Ecol Lett 10:470–480. CrossRefPubMedGoogle Scholar
  38. Pecoraro L, Angelini P, Arcangeli A, Bistocchi G, Gargano ML, La Rosa A, Lunghini D, Polemis E, Rubini A, Saitta A, Venanzoni R, Zervakis GI (2014) Macrofungi in Mediterranean maquis along a seashore and altitudinal transects. Plant Biosyst 148(2):367–376. CrossRefGoogle Scholar
  39. Pellisier L, Niculita-Hirzel H, Dubuis A et al (2014) Soil fungal communities of grasslands are spatially structured at a regional scale in the Alps. Mol Ecol 23:4274–4290. CrossRefGoogle Scholar
  40. Querejeta JI, Barea JM, Allen MF et al (2003) Oecologia 135:510–515.
  41. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  42. Richard F, Moreau PA, Selosse MA, Gardes M (2004) Diversity and fruiting patterns of ectomycorrhizal and saprobic fungi in an old-growth Mediterranean forest dominated by Quercus ilex L. Can J Bot 82:1711–1729. CrossRefGoogle Scholar
  43. Richard F, Millot S, Gardes M, Selosse MA (2005) Diversity and specificity of ectomycorrhizal fungi retrieved from an old-growth Mediterranean forest dominated by Quercus ilex. New Phytol 166:1011–1023. CrossRefPubMedGoogle Scholar
  44. Richard F, Roy M, Shahin O, Sthultz C, Duchemin M, Joffre R, Selosse MA (2011) Ectomycorrhizal communities in Mediterranean forest ecosystem dominated by Quercus ilex: season dynamics and response to drought in the surface organic horizon. Ann Forest Sci 68:57–68. CrossRefGoogle Scholar
  45. Rincón A, Santamaría-Pérez B, Rabasa SG, Coince A, Marçais B, Buée M (2015) Compartmentalized and contrasted response of ectomycorrhizal and soil fungal communities of Scots pine forests along elevation gradients in France and Spain. Environ Microbiol 17:3009–3024. CrossRefPubMedGoogle Scholar
  46. Roberts N, Eastwood WJ, Kuzucuoglu C, Fiorentino G, Caracuta V (2011) Climatic, vegetation and cultural change in the eastern Mediterranean during the mid-Holocene environmental transition. The Holocene 21(1):147–162CrossRefGoogle Scholar
  47. Saitta A, Bernicchia A, Gorjón SP, Altobelli E, Granito VM, Losi C, Lunghini D, Maggi O, Medardi G, Padovan F, Pecoraro L, Vizzini A, Persiani AM (2011) Biodiversity of wood-decay fungi in Italy. Plant Biosyst 145(4):958–968. CrossRefGoogle Scholar
  48. Smith ME, Douhan GW, Rizzo DM (2007) Ectomycorrhizal community structure in a xeric Quercus woodland based on rDNA sequence analysis of sporocarps and pooled roots. New Phytol 174:847–863. CrossRefPubMedGoogle Scholar
  49. Tedersoo L, Smith ME (2013) Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biol Rev 27:83–99. CrossRefGoogle Scholar
  50. Tedersoo L, Jairus T, Horton BM, Abarenkov K, Suvi T, Saar I, Koljalg U (2008a) Strong host preference of ectomycorrhizal fungi in a Tasmanian wet sclerophyll forest as revealed by DNA barcoding and taxon-specific primers. New Phytol 180:479–490. CrossRefPubMedGoogle Scholar
  51. Tedersoo L, Suvi T, Jairus T, Kõljalg U (2008b) Forest microsite effects on community composition of ectomycorrhizal fungi on seedlings of Picea abies and Betula pendula. Environ Microbiol 10:1189–1201. CrossRefPubMedGoogle Scholar
  52. Tedersoo L, Bahram M, Toots M, Diédhiou AG, Henkel TW, Kjøller R, Morris MH, Nara K, Nouhra E, Peay KG, Põlme S, Ryberg M, Smith ME, Kõljalg U (2012) Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol Ecol 21:4160–4170. CrossRefPubMedGoogle Scholar
  53. Tedersoo L, Bahram M, Dickie IA (2014a) Does host plant richness explain of ectomycorrhizal fungi? Re-evaluation of Gao et al. (2013) data sets reveals sampling effects. Mol Ecol 23:992–995. CrossRefPubMedGoogle Scholar
  54. Tedersoo L, Bahram M, Põlme S et al (2014b) Global diversity and geography of soil fungi. Science 346:1256688. CrossRefPubMedGoogle Scholar
  55. Tedersoo L, Anslan S, Bahram M et al (2015) Shotgun metagenomes and multiple primer pair-barcode combinations of amplicons reveal biases in metabarcoding analyses of fungi. MycoKeys 10:1–43. CrossRefGoogle Scholar
  56. Tedersoo L, Bahram M, Cajthaml T, Põlme S, Hiiesalu I, Anslan S, Harend H, Buegger F, Pritsch K, Koricheva J, Abarenkov K (2016) Tree diversity and species identity effects on soil fungi, protists and animals are context dependent. ISME J 10:346–362. CrossRefPubMedGoogle Scholar
  57. Teste FP, Kardol P, Turner BL, Wardle DA, Zemunik G, Renton M, Laliberté E (2017) Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Science 355(6321):173–176. CrossRefPubMedGoogle Scholar
  58. Toljander JF, Eberhardt U, Toljander YK, Paul LR, Taylor AFS (2006) Species composition of an ectomycorrhizal fungal community along a local nutrient gradient in a boreal forest. New Phytol 170:873–884. CrossRefPubMedGoogle Scholar
  59. Urbanova M, Snajdr J, Baldrian P (2015) Composition of fungal and bacterial communities in forest litter and soil is largely determined by dominant trees. Soil Bio Biochem 84:53–64. CrossRefGoogle Scholar
  60. Venturella G, Pecorella E, Saitta A, Zambonelli A, Morara M (2006) Ecology and distribution of hypogeous fungi from Sicily (southern Italy). Cryptogam Mycol 27(3):201–217Google Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Alessandro Saitta
    • 1
    Email author
  • Sten Anslan
    • 2
  • Mohammad Bahram
    • 2
    • 3
  • Luca Brocca
    • 4
  • Leho Tedersoo
    • 5
  1. 1.Department of Agricultural, Food and Forest SciencesUniversity of PalermoPalermoItaly
  2. 2.Department of Botany, Institute of Ecology and Earth SciencesUniversity of TartuTartuEstonia
  3. 3.Department of Organismal Biology, Evolutionary Biology CentreUppsala UniversityUppsalaSweden
  4. 4.Research Institute for Geo-Hydrological Protection, National Research CouncilPerugiaItaly
  5. 5.National History MuseumUniversity of TartuTartuEstonia

Personalised recommendations