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Mycological Progress

, Volume 11, Issue 1, pp 47–59 | Cite as

Isotopic signatures and trophic status of Ramaria

  • Reinhard Agerer
  • Josef Christan
  • Christoph Mayr
  • Erik Hobbie
Original Article

Abstract

The genus Ramaria is composed of several subgenera that often correspond to specific trophic strategies. Because carbon and nitrogen isotopes can be used to assess fungal trophic status and nitrogen sources, we accordingly carried out an extensive survey of isotopic patterns in archived specimens of Ramaria from Germany and other locations. Isotopic patterns in species generally corresponded to subgeneric affiliations and to the range of different potential substrates, with fungi fruiting on wood and litter (subgenera Asteroramaria and Lentoramaria) much lower in δ15N (≈−3‰) than ectomycorrhizal taxa (≈12‰) (subgenus Ramaria) or taxa fruiting on soil (≈13‰) (subgenus Echinoramaria). Conversely, fungi fruiting on wood and litter were higher in δ13C (−23‰) than those fruiting on soil (≈−27‰), with ectomycorrhizal fungi intermediate (≈−24.5‰). Fungi colonizing mineral soil horizons were about 3‰ enriched in 15N relative to those colonizing both mineral and organic horizons. The high δ15N and low δ13C signatures of taxa fruiting on soil remains unexplained. The high degree of fidelity of isotopic signatures with subgeneric classifications and life history traits suggests that sporocarps are good integrators of patterns of carbon and nitrogen cycling for specific taxa. Archived specimens represent a useful trove of life history information that could be mined without requiring extensive supporting isotopic data from other ecosystem pools.

Keywords

δ15δ13Ramaria Sporocarps Fruitbodies 

Notes

Acknowledgements

This work was supported by NSF grant IOS-0843366 to Erik Hobbie. Comments of Steve Trudell improved the manuscript and are gratefully acknowledged.

References

  1. Agerer R (1987-2008) Colour Atlas of Ectomycorrhizae. 1st–14th delivery. Einhorn, Schwäbisch GmündGoogle Scholar
  2. Agerer R (1996a) Ramaria subbotrytis (Coker) Corner + Quercus robur L. Descr Ectomyc 1:125–130Google Scholar
  3. Agerer R (1996b) Ramaria spinulosa (Fr.) Quel. + Fagus sylvatica. Descr Ectomyc 1:119–124Google Scholar
  4. Agerer R (1996c) Ramaria largentii Marr & D. E. Stuntz + Picea abies (L.) H. Karst. Descr Ectomyc 1:113–118Google Scholar
  5. Agerer R (1996d) Ramaria aurea (Schaeff.: Fr.) Quel. + Fagus sylvatica L. Descr Ectomyc 1:107–112Google Scholar
  6. Agerer R (2001) Exploration types of ectomycorrhizae. A proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114CrossRefGoogle Scholar
  7. Agerer R (2006) Fungal relationships and structural identity of their ectomycorrhizae. Mycol Prog 5:67–107CrossRefGoogle Scholar
  8. Agerer R (2007) Diversity of ectomycorrhizae as seen from below and above ground: the exploration types. Z Mykol 73:61–88Google Scholar
  9. Agerer R, Rambold G (2004–2009 [first posted on 2004-06-01; most recent update: 2009-01-26]). DEEMY – An Information System for Characterization and Determination of Ectomycorrhizae. München, GermanyGoogle Scholar
  10. Boström B, Comstedt D, Ekblad A (2008) Can isotopic fractionation during respiration explain the 13C-enriched sporocarps of ectomycorrhizal and saprotrophic fungi? New Phytol 177:1012–1029PubMedCrossRefGoogle Scholar
  11. Byrne AR (1988) Radioactivity in fungi in Slovenia, Yugoslavia, following the Chernobyl accident. J Environ Radioact 6:177–183CrossRefGoogle Scholar
  12. Christan J (2008) Die Gattung Ramaria in Deutschland. IHW, EchingGoogle Scholar
  13. Christan J, Hahn C (2005) The systematics of the genus Ramaria (Basidiomycota, Gomphales). Z Mykol 71:7–42Google Scholar
  14. Dämmrich F (2006) Studien der tomentelloiden Pilze in Deutschland - unter besonderer Berücksichtigung der Zeichnungen von Frau Dr. H. Maser aus den Jahren 1988–1974. Teil 1: Die Gattung Tomentella. Z Mykol 72:167–212Google Scholar
  15. Arbeitskreis für Bodensystematik der Deutschen Bodenkundlichen Gesellschaft (1998) Systematik der Böden und der Bodenbildenden Substrate Deutschlands, Kurzfassung. Mitt Dt. Bodenkundl Ges 86:135–180. OldenburgGoogle Scholar
  16. Eberhardt U, Oberwinkler F, Verbeken A, Rinaldi AC, Pacioni G, Comandini O (2000) Lactarius ectomycorrhizae on Abies alba: morphological dscription, molecular characterization, and taxonomic remarks. Mycologia 92:860–873CrossRefGoogle Scholar
  17. Emmerton KS, Callaghan TV, Jones HE, Leake JR, Michelsen A, Read DJ (2001) Assimilation and isotopic fractionation of nitrogen by mycorrhizal fungi. New Phytol 151:503–511CrossRefGoogle Scholar
  18. Gebauer G, Taylor AFS (1999) 15N natural abundance in fruit bodies of different functional groups of fungi in relation to substrate utilization. New Phytol 142:93–101CrossRefGoogle Scholar
  19. Giachini AJ, Hosaka K, Nouhra E, Spatafora J, Trappe JM (2010) Phlogenetic relationships of the Gomphales based on nuc-25S-rDNA, mit-12S-rDNA, and mit-atp6-DNA combined sequences. Fungal Biol 114:224–234PubMedCrossRefGoogle Scholar
  20. Griffith GW, Easton GL, Jones AW (2002) Ecology and diversity of waxcap (Hygrocybe spp.) fungi. Bot J Scotland 54:7–22CrossRefGoogle Scholar
  21. Hibbett DS, Gilbert LB, Donoghue MJ (2000) Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes. Nature 407:506–508PubMedCrossRefGoogle Scholar
  22. Hobbie EA (2005) Using isotopic tracers to follow carbon and nitrogen cycling of fungi. In: Dighton J, Oudemans P, White J (eds), The fungal community: its organization and role in the ecosystem. CRC Press, Boca Raton, pp 361–381Google Scholar
  23. Hobbie EA, Agerer R (2010) Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types. Plant Soil 327:71–83CrossRefGoogle Scholar
  24. Hobbie EA, Ouimette AP (2009) Causes of nitrogen isotope patterns in terrestrial soil profiles. Biogeochemistry 95:355–371CrossRefGoogle Scholar
  25. Hobbie EA, Macko SA, Shugart HH (1999) Insights into nitrogen and carbon dynamics of ectomycorrhizal and saprotrophic fungi from isotopic evidence. Oecologia 118:353–360CrossRefGoogle Scholar
  26. Hobbie EA, Weber NS, Trappe JM (2001) Mycorrhizal vs saprotrophic status of fungi: the isotopic evidence. New Phytol 150:601–610CrossRefGoogle Scholar
  27. Hobbie EA, Weber NS, Trappe JM, von Klinken GJ (2002) Using radiocarbon to determine the mycorrhizal status of fungi. New Phytol 156:129–136CrossRefGoogle Scholar
  28. Hobbie EA, Jumpponen A, Trappe J (2005) Foliar and fungal 15N:14N ratios reflect development of mycorrhizae and nitrogen supply during primary succession: testing analytical models. Oecologia 146:258–268PubMedCrossRefGoogle Scholar
  29. Högberg P, Plamboeck AH, Taylor AFS, Fransson PMA (1999) Natural 13C abundance reveals trophic status of fungi and host-origin of carbon in mycorrhizal fungi in mixed forests. Proc Natl Acad Sci USA 96:8534–8539PubMedCrossRefGoogle Scholar
  30. Kohzu A, Yoshioka T, Ando T, Takahashi M, Koba K, Wada E (1999) Natural 13C and 15N abundance of field-collected fungi and their ecological implications. New Phytol 144:323–330CrossRefGoogle Scholar
  31. Kõljalg U (1996) Tomentella (Basidiomycota) and related genera in temperate Eurasia. Fungiflora, OsloGoogle Scholar
  32. Lilleskov EA, Hobbie EA, Fahey TJ (2002) Ectomycorrhizal fungal taxa differing in response to nitrogen deposition also differ in pure culture organic nitrogen use and natural abundance of nitrogen isotopes. New Phytol 154:219–231CrossRefGoogle Scholar
  33. Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–20PubMedCrossRefGoogle Scholar
  34. Marr DC, Stuntz DE (1973) Ramaria of Western Washington. Bibliotheca Mycologica, vol 38. Cramer, StuttgartGoogle Scholar
  35. Mayor JR, Schuur EAG, Henkel TW (2009) Elucidating the nutritional dynamics of fungi using stable isotopes. Ecol Lett 12:171–183PubMedCrossRefGoogle Scholar
  36. Miller SL, Buyck B (2002) Molecular phylogeny of the genus Russula in Europe with a comparison of modern infrageneric classifications. Mycol Res 106:259–276CrossRefGoogle Scholar
  37. Nouhra ER, Horton TR, Cazares E, Castellano M (2005) Morphological and molecular characterization of selected Ramaria mycorrhizae. Mycorrhiza 15:55–59PubMedCrossRefGoogle Scholar
  38. Nuytinck J, Verbeken A (2003) Lactarius sanguifluus versus Lactarius vinosus - molecular and morpholgical analyses. Mycol Prog 2:227–234CrossRefGoogle Scholar
  39. Nuytinck J, Verbeken A, Miller SL (2007) Worldwide phylogeny of Lactarius section Deliciosi inferred from ITS and glyceraldehyde-3-phosphate dehydrogenase gene sequences. Mycologia 99:820–832PubMedCrossRefGoogle Scholar
  40. Ogawa M (1984) Ecological characters of ectomycorrhizal fungi and their mycorrhizae. An introduction to the ecology of higher fungi. Japan A R Q 18:305–314Google Scholar
  41. Raidl S, Scattolin L (2006) Ramaria formosa (Pers.) Quél. + Picea abies (L.) Karst. Descr Ectomycol 9(10):143–149Google Scholar
  42. Rinaldi AC, Comandini O, Kuyper TW (2008) Ectomycorrhizal fungal diversity: separating the wheat from the chaff. Fungal Divers 33:1–45Google Scholar
  43. Scattolin L, Raidl S (2006) Ramaria flavo-saponarea R. H. Petersen + Fagus sylvatica L. Descr Ectomycol 9(10):135–141Google Scholar
  44. Taylor AFS, Högbom L, Högberg M, Lyon AJE, Näsholm T, Högberg P (1997) Natural 15N abundance in fruit bodies of ectomycorrhizal fungi from boreal forests. New Phytol 136:713–720CrossRefGoogle Scholar
  45. Taylor AFS, Fransson PM, Högberg P, Högberg MN, Plamboeck AH (2003) Species level patterns in 13C and 15N abundance of ectomycorrhizal and saprotrophic fungal sporocarps. New Phytol 159:757–774CrossRefGoogle Scholar
  46. Thiers B (2009, continuously updated) Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. sciweb.nybg.org/science2/IndexHerbariorum.asp
  47. Trudell SA, Rygiewicz PT, Edmonds RL (2004) Patterns of nitrogen and carbon stable isotope ratios in macrofungi, plants and soils in two old growth conifer forests. New Phytol 164:317–335CrossRefGoogle Scholar
  48. Zeller B, Brechet C, Maurice J-P, Le Tacon F (2007) 13C and 15N isotopic fractionation in trees, soils and fungi in a natural forest stand and a Norway spruce plantation. Ann For Sci 64:419–429CrossRefGoogle Scholar

Copyright information

© German Mycological Society and Springer 2010

Authors and Affiliations

  • Reinhard Agerer
    • 1
  • Josef Christan
    • 2
  • Christoph Mayr
    • 3
    • 4
  • Erik Hobbie
    • 5
  1. 1.Department Biology and GeoBio-Center LMU, Division of Organismic BiologyLudwig-Maximilians-UniversityMünchenGermany
  2. 2.MünchenGermany
  3. 3.GeoBio-Center LMU, Department Geo- und UmweltwissenschaftenLudwig-Maximilians-UniversityMünchenGermany
  4. 4.Institut für Geographie, Friedrich-Alexander-Universität Erlangen-NürnbergNürnbergGermany
  5. 5.Complex Systems Research CenterUniversity of New HampshireDurhamUSA

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