Advertisement

Oecologia

, Volume 158, Issue 1, pp 95–107 | Cite as

Phenolic-rich leaf carbon fractions differentially influence microbial respiration and plant growth

  • Courtney L. Meier
  • William D. Bowman
Ecosystem Ecology - Original Paper

Abstract

Phenolics can reduce soil nutrient availability, either indirectly by stimulating microbial nitrogen (N) immobilization or directly by enhancing physical protection within soil. Phenolic-rich plants may therefore negatively affect neighboring plant growth by restricting the N supply. We used a slow-growing, phenolic-rich alpine forb, Acomastylis rossii, to test the hypothesis that phenolic-rich carbon (C) fractions stimulate microbial population growth and reduce plant growth. We generated low-molecular-weight (LMW) fractions, tannin fractions, and total soluble C fractions from A. rossii and measured their effects on soil respiration and growth of Deschampsia caespitosa, a fast-growing, co-dominant grass. Fraction effects fell into two distinct categories: (1) fractions did not increase soil respiration and killed D. caespitosa plants, or (2) fractions stimulated soil respiration and reduced plant growth and plant N concentration while simultaneously inhibiting root growth. The LMW phenolic-rich fractions increased soil respiration and reduced plant growth more than tannins. These results suggest that phenolic compounds can inhibit root growth directly as well as indirectly affect growth by reducing pools of plant available N by stimulating soil microbes. Both mechanisms illustrate how below-ground phenolic effects may influence the growth of neighboring plants. We also examined patterns of foliar phenolic concentrations among populations of A. rossii across a natural productivity gradient (productivity was used as a proxy for competition intensity). Concentrations of some LMW phenolics increased significantly in more productive sites where A. rossii is a competitive equal with the faster growing D. caespitosa. Taken together, our results contribute important information to the growing body of evidence indicating that the quality of C moving from plants to soils can have significant effects on neighboring plant performance, potentially associated with phytoxic effects, and indirect effects on soil biogeochemistry.

Keywords

Allelopathy Low-molecular-weight phenolics Mineral nutrition Phenolics Plant growth Plant secondary compounds Plant–soil interactions Soil nitrogen Tannins 

Notes

Acknowledgments

Field and laboratory assistance for this study were provided by Heather Bechtold, Kimberly Lohnas, Torrin Hultgren, Damaris Means, and Anthony Darrouzet-Nardi. Ann Hagerman and Jack Schultz provided germane advice for phenolic extraction and analyses. Helpful editorial comments on an earlier version of this manuscript were contributed by Deane Bowers, Noah Fierer, Anthony Darrouzet-Nardi, Sasha Reed, Nataly Ascarrunz, and Ann Hagerman. Funding sources included the Andrew W. Mellon Foundation, the NSF-sponsored Niwot Ridge LTER program, the John Marr Memorial Ecology Fund, and a Department of Ecology and Evolutionary Biology grant awarded to CLM. All experiments complied with current USA law.

References

  1. Allen AS, Schlesinger WH (2004) Nutrient limitations to soil microbial biomass and activity in loblolly pine forests. Soil Biol Biochem 36:581–589CrossRefGoogle Scholar
  2. Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM (2003) Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301:1377–1380PubMedCrossRefGoogle Scholar
  3. Bate-Smith EC (1962) The phenolic constituents of plants and their taxonomic significance: I dicotyledons. J Linn Soc Lond 58:95–173Google Scholar
  4. Blum U, Shafer SR (1988) Microbial-populations and phenolic-acids in soil. Soil Biol Biochem 20:793–800CrossRefGoogle Scholar
  5. Bowman WD, Bilbrough CJ (2001) Influence of a pulsed nitrogen supply on growth and nitrogen uptake in alpine graminoids. Plant Soil 233:283–290CrossRefGoogle Scholar
  6. Bowman WD, Fisk MC (2001) Primary production. In: Bowman WD, Seastedt TR (eds) Structure and function of an Alpine ecosystem. Oxford University Press, New York, pp 177–197Google Scholar
  7. Bowman WD, Theodose TA, Fisk MC (1995) Physiological and production responses of plant-growth forms to increases in limiting resources in Alpine Tundra—implications for differential community response to environmental-change. Oecologia 101:217–227CrossRefGoogle Scholar
  8. Bowman WD, Steltzer H, Rosenstiel TN, Cleveland CC, Meier CL (2004) Litter effects of two co-occurring alpine species on plant growth, microbial activity and immobilization of nitrogen. Oikos 104:336–344CrossRefGoogle Scholar
  9. Brant JB, Sulzman EW, Myrold DD (2006) Microbial community utilization of added carbon substrates in response to long-term carbon input manipulation. Soil Biol Biochem 38:2219–2232CrossRefGoogle Scholar
  10. Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523PubMedCrossRefGoogle Scholar
  11. Chapin FS (1980) The mineral-nutrition of wild plants. Annu Rev Ecol Syst 11:233–260CrossRefGoogle Scholar
  12. Close DC, McArthur C (2002) Rethinking the role of many plant phenolics - protection from photodamage not herbivores? Oikos 99:166–172CrossRefGoogle Scholar
  13. Dearing MD (2001) Plant-herbivore interactions. In: Bowman WD, Seastedt TR (eds) Structure and function of an Alpine ecosystem. Oxford University Press, Oxford, pp 266–282Google Scholar
  14. Dunn RM, Mikola J, Bol R, Bardgett RD (2006) Influence of microbial activity on plant-microbial competition for organic and inorganic nitrogen. Plant Soil 289:321–334CrossRefGoogle Scholar
  15. Feild TS, Lee DW, Holbrook NM (2001) Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of red-osier dogwood. Plant Physiol 127:566–574PubMedCrossRefGoogle Scholar
  16. Fierer N, Schimel JP, Cates RG, Zou JP (2001) Influence of balsam poplar tannin fractions on carbon and nitrogen dynamics in Alaskan taiga floodplain soils. Soil Biol Biochem 33:1827–1839CrossRefGoogle Scholar
  17. Foster BL (1999) Establishment, competition and the distribution of native grasses among Michigan old-fields. J Ecol 87:476–489CrossRefGoogle Scholar
  18. Foster BL (2000) Competition at the population level along a standing crop gradient: a field experiment in successional grassland. Plant Ecol 151:171–180CrossRefGoogle Scholar
  19. Gallardo A, Schlesinger WH (1995) Factors determining soil microbial biomass and nutrient immobilization in desert soils. Biogeochemistry 28:55–68CrossRefGoogle Scholar
  20. Hagerman AE (2002) Tannin chemistry handbook (PDF). Available at: http://www.users.muohio.edu/hagermae/tannin.pdf
  21. Hagerman AE, Butler LG (1989) Choosing appropriate methods and standards for assaying tannin. J Chem Ecol 15:1795–1810CrossRefGoogle Scholar
  22. Hamer U, Marschner B (2005) Priming effects in different soil types induced by fructose, alanine, oxalic acid and catechol additions. Soil Biol Biochem 37:445–454CrossRefGoogle Scholar
  23. Hättenschwiler S, Hagerman AE, Vitousek PM (2003) Polyphenols in litter from tropical montane forests across a wide range in soil fertility. Biogeochemistry 64:129–148CrossRefGoogle Scholar
  24. Horner JD, Gosz JR, Cates RG (1988) The role of carbon-based plant secondary metabolites in decomposition in terrestrial ecosystems. Am Nat 132:869–883CrossRefGoogle Scholar
  25. Jonasson S, Vestergaard P, Jensen M, Michelsen A (1996) Effects of carbohydrate amendments on nutrient partitioning, plant and microbial performance of a grassland-shrub ecosystem. Oikos 75:220–226CrossRefGoogle Scholar
  26. Kraus TEC, Dahlgren RA, Zasoski RJ (2003) Tannins in nutrient dynamics of forest ecosystems—a review. Plant Soil 256:41–66CrossRefGoogle Scholar
  27. Kraus TEC, Zasoski RJ, Dahlgren RA, Horwath WR, Preston CM (2004) Carbon and nitrogen dynamics in a forest soil amended with purified tannins from different plant species. Soil Biol Biochem 36:309–321CrossRefGoogle Scholar
  28. Kuiters AT (1990) Role of phenolic substances from decomposing forest litter in plant-soil interactions. Acta Bot Neerl 39:329–348Google Scholar
  29. Levin D (1971) Plant phenolics—an ecological perspective. Am Nat 105:157–181CrossRefGoogle Scholar
  30. McArthur C, Robbins CT, Hagerman AE, Hanley TA (1993) Diet selection by a ruminant generalist browser in relation to plant chemistry. Can J Zool–Rev Can Zool 71:2236–2243CrossRefGoogle Scholar
  31. McClaugherty CA (1983) Soluble polyphenols and carbohydrates in throughfall and leaf litter decomposition. Acta Oecol–Oecol Gen 4:375–385Google Scholar
  32. Meier CL, Suding KN, Bowman WD (2008) Carbon flux from plants to soil: roots are a below-ground source of phenolic secondary compounds in an alpine ecosystem. J Ecol 96:421–430CrossRefGoogle Scholar
  33. Moore BD, Palmquist DE, Seemann JR (1997) Influence of plant growth at high CO2 concentrations on leaf content of ribulose-1, 5-bisphosphate carboxylase/oxygenase and intracellular distribution of soluble carbohydrates in tobacco, snapdragon, and parsley. Plant Physiol 115:241–248PubMedGoogle Scholar
  34. Nilsson MC, Zackrisson O, Sterner O, Wallstedt A (2000) Characterisation of the differential interference effects of two boreal dwarf shrub species. Oecologia 123:122–128CrossRefGoogle Scholar
  35. Northup RR, Dahlgren RA, McColl JG (1998) Polyphenols as regulators of plant-litter-soil interactions in northern California’s pygmy forest: a positive feedback? Biogeochemistry 42:189–220CrossRefGoogle Scholar
  36. Nurmi K, Ossipov V, Haukioja E, Pihlaja K (1996) Variation of total phenolic content and individual low-molecular-weight phenolics in foliage of mountain birch trees (Betula pubescens ssp tortuosa). J Chem Ecol 22:2023–2040CrossRefGoogle Scholar
  37. Orwin KH, Wardle DA, Greenfield LG (2006) Ecological consequences of carbon substrate identity and diversity in a laboratory study. Ecology 87:580–593PubMedCrossRefGoogle Scholar
  38. Ren ZS, Mallik AU (2006) Selected ectomycorrhizal fungi of black spruce (Picea mariana) can detoxify phenolic compounds of Kalmia angustifolia. J Chem Ecol 32:1473–1489CrossRefGoogle Scholar
  39. Schimel JP, VanCleve K, Cates RG, Clausen TP, Reichardt PB (1996) Effects of balsam poplar (Populus balsamifera) tannins and low molecular weight phenolics on microbial activity in taiga floodplain soil: implications for changes in N cycling during succession. Can J Bot–Rev Can Bot 74:84–90CrossRefGoogle Scholar
  40. Schimel JP, Cates RG, Ruess R (1998) The role of balsam poplar secondary chemicals in controlling soil nutrient dynamics through succession in the Alaskan taiga. Biogeochemistry 42:221–234CrossRefGoogle Scholar
  41. Steltzer H, Bowman WD (1998) Differential influence of plant species on soil nitrogen transformations within moist meadow Alpine tundra. Ecosystems 1:464–474CrossRefGoogle Scholar
  42. Suding KN, Larson JR, Thorsos E, Steltzer H, Bowman WD (2004) Species effects on resource supply rates: do they influence competitive interactions? Plant Ecol 175:47–58CrossRefGoogle Scholar
  43. Suding KN, Ashton IW, Bechtold H, Bowman WD, Mobley ML, Winkleman R (2008) Plant and microbe contribution to community resilience in a directionally changing environment. Ecol Monogr 78:313–329CrossRefGoogle Scholar
  44. Thompson WR, Aneshans D, Meinwald J, Eisner T (1972) Flavonols—pigments responsible for ultraviolet-absorption in nectar guide of flower. Science 177:528–530Google Scholar
  45. Twolan-Strutt L, Keddy PA (1996) Above- and belowground competition intensity in two contrasting wetland plant communities. Ecology 77:259–270CrossRefGoogle Scholar
  46. Van Breemen N, Finzi AC (1998) Plant-soil interactions: ecological aspects and evolutionary implications. Biogeochemistry 42:1–19CrossRefGoogle Scholar
  47. Walton JD (1997) Biochemical plant pathology. In: Dey PM, Harborne JB (eds) Plant biochemistry. Academic Press, London, pp 487–502CrossRefGoogle Scholar
  48. Waterman PG, Mole S (1994) Analysis of phenolic plant metabolites. Blackwell, OxfordGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary Biology and Mountain Research Station, Institute of Arctic and Alpine ResearchUniversity of Colorado at BoulderBoulderUSA

Personalised recommendations