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Litter Quality Modulates Effects of Dissolved Nitrogen on Leaf Decomposition by Stream Microbial Communities

Abstract

Rates of leaf litter decomposition in streams are strongly influenced both by inorganic nutrients dissolved in stream water and by litter traits such as lignin, nitrogen (N) and phosphorus (P) concentrations. As a result, decomposition rates of different leaf species can show contrasting responses to stream nutrient enrichment resulting from human activities. It is unclear, however, whether the root cause of such discrepancies in field observations is the interspecific variation in either litter nutrient or litter lignin concentrations. To address this question, we conducted a controlled laboratory experiment with a known fungal community to determine decomposition rates of 38 leaf species exhibiting contrasting litter traits (N, P and lignin concentrations), which were exposed to 8 levels of dissolved N concentrations representative of field conditions across European streams (0.07 to 8.96 mg N L−1). The effect of N enrichment on decomposition rate was modelled using Monod kinetics to quantify N effects across litter species. Lignin concentration was the most important litter trait determining decomposition rates and their response to N enrichment. In particular, increasing dissolved N supply from 0.1 to 3.0 mg N L−1 accelerated the decomposition of lignin-poor litter (e.g. < 10% of lignin, 2.9× increase ± 1.4 SD, n = 14) more strongly than that of litter rich in lignin (e.g. > 15% of lignin, 1.4× increase ± 0.2 SD, n = 9). Litter nutrient concentrations were less important, with a slight positive effect of P on decomposition rates and no effect of litter N. These results indicate that shifts in riparian vegetation towards species characterized by high litter lignin concentrations could alleviate the stimulation of C turnover by stream nutrient enrichment.

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References

  1. Chapin FS Jr, Matson PA, Mooney HA (2002) Principles of terrestrial ecosystem ecology. Springer-Verlag, New York

    Google Scholar 

  2. Wagener SM, Oswood MW, Schimel JP (1998) Rivers and soils: parallels in carbon and nutrient processing. BioScience 48:104–108

    Article  Google Scholar 

  3. Webster JR, Benfield EF (1986) Vascular plant breakdown in freshwater ecosystems. Annu Rev Ecol Syst 17:567–594

    Article  Google Scholar 

  4. Tank JL, Rosi-Marshall EJ, Griffiths NA, Entrekin SA, Stephen ML (2010) A review of allochthonous organic matter dynamics and metabolism in streams. Freshw Sci 29:118–146

    Google Scholar 

  5. Gessner MO, Swan CM, Dang CK, McKie BG, Bardgett RD, Wall DH, Hättenschwiler S (2010) Diversity meets decomposition. Trends Ecol Evol 25:372–380

    Article  PubMed  Google Scholar 

  6. Danger M, Gessner MO, Bärlocher F (2016) Ecological stoichiometry of aquatic fungi: current knowledge and perspectives. Fungal Ecol 19:100–111

    Article  Google Scholar 

  7. Enriquez S, Duarte CM, Sand-Jensen K (1993) Patterns in decomposition rates among photosynthetic organisms: the importance of detritus C:N:P content. Oecologia 94:457–471

    Article  CAS  PubMed  Google Scholar 

  8. Cross WF, Benstead JP, Frost PC, Thomas SA (2005) Ecological stoichiometry in freshwater benthic systems: recent progress and perspectives. Freshw Biol 50:1895–1912

    Article  CAS  Google Scholar 

  9. Hladyz S, Gessner MO, Giller PS, Pozo J, Woodward G (2009) Resource quality and stoichiometric constraints on stream ecosystem functioning. Freshw Biol 54:957–970

    Article  CAS  Google Scholar 

  10. Frainer A, Jabiol J, Gessner MO, Bruder A, Chauvet E, McKie BG (2016) Stoichiometric imbalances between detritus and detritivores are related to shifts in ecosystem functioning. Oikos 125:861–871

    Article  CAS  Google Scholar 

  11. Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison JF, Hobbie SE, Odell GM, Weider LJ (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 3:540–550

    Article  Google Scholar 

  12. Elser JJ, Dobberfuhl DR, MacKay NA, Schampel JH (1996) Organism size, life history, and N:P stoichiometry. BioScience 46:674–684

    Article  Google Scholar 

  13. Ostrofsky ML (1997) Relationship between chemical characteristics of autumn-shed leaves and aquatic processing rates. J N Am Benthol Soc 16:750–759

    Article  Google Scholar 

  14. Suberkropp K (1998) Effect of dissolved nutrients on two aquatic hyphomycetes growing on leaf litter. Mycol Res 102:998–1002

    Article  CAS  Google Scholar 

  15. Cheever BM, Kratzer EB, Webster JR (2012) Immobilization and mineralization of N and P by heterotrophic microbes during leaf decomposition. Freshw Sci 31:133–147

    Article  Google Scholar 

  16. Cheever BM, Webster JR, Bilger EE, Thomas SA (2013) The relative importance of exogenous and substrate-derived nitrogen for microbial growth during leaf decomposition. Ecology 94:1614–1625

    Article  CAS  PubMed  Google Scholar 

  17. Gulis V, Kuehn KA, Schoettle LN, Leach D, Benstead JP, Rosemond AD (2017) Changes in nutrient stoichiometry, elemental homeostasis and growth rate of aquatic litter-associated fungi in response to inorganic nutrient supply. ISME J 11:2729–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Ferreira V, Gulis V, Graça MAS (2006) Whole-stream nitrate addition affects litter decomposition and associated fungi but not invertebrates. Oecologia 149:718–729

    Article  PubMed  Google Scholar 

  19. Gulis V, Suberkropp K (2003) Leaf litter decomposition and microbial activity in nutrient-enriched and unaltered reaches of a headwater stream. Freshw Biol 48:123–134

    Article  Google Scholar 

  20. Gulis V, Ferreira V, Graça MAS (2006) Stimulation of leaf litter decomposition and associated fungi and invertebrates by moderate eutrophication: implications for stream assessment. Freshw Biol 51:1655–1669

    Article  CAS  Google Scholar 

  21. Rosemond AD, Benstead JP, Bumpers PM, Gulis V, Kominoski JS, Manning DWP, Suberkropp K, Wallace JB (2015) Experimental nutrient additions accelerate terrestrial carbon loss from stream ecosystems. Science 347:1142–1145

    Article  CAS  PubMed  Google Scholar 

  22. Melillo JM, Aber JD, Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–626

    Article  CAS  Google Scholar 

  23. Gessner MO, Chauvet E (1994) Importance of stream microfungi in controlling breakdown rates of leaf litter. Ecology 75:1807–1817

    Article  Google Scholar 

  24. Lecerf A, Chauvet E (2008) Intraspecific variability in leaf traits strongly affects alder leaf decomposition in a stream. Basic Appl Ecol 9:598–605

    Article  Google Scholar 

  25. Kirk TK, Farrell RL (1987) Enzymatic “combustion”: the microbial degradation of lignin. Annu Rev Microbiol 41:465–505

    Article  CAS  PubMed  Google Scholar 

  26. Hatakka A, Hammel KE (2010) Fungal biodegradation of lignocelluloses. In: Hofrichter M (ed) Industrial applications. The Mycota, vol 10. Springer, Berlin, pp 319–340

    Google Scholar 

  27. Ferreira V, Castagneyrol B, Koricheva J, Gulis V, Chauvet E, Graça MAS (2015) A meta-analysis of the effects of nutrient enrichment on litter decomposition in streams. Biol Rev 90:669–688

    Article  PubMed  Google Scholar 

  28. Kominoski JS, Rosemond AD, Benstead JP, Gulis V, Maerz JC, Manning DWP (2015) Low-to-moderate nitrogen and phosphorus concentrations accelerate microbially driven litter breakdown rates. Ecol Appl 25:856–865

    Article  PubMed  Google Scholar 

  29. Ardón M, Stallcup LA, Pringle CM (2006) Does leaf quality mediate the stimulation of leaf breakdown by phosphorus in Neotropical streams? Freshw Biol 51:618–633

    Article  CAS  Google Scholar 

  30. Gessner MO (2005) Proximate lignin and cellulose. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition—a practical guide. Springer, Dordrecht, pp 115–120

    Chapter  Google Scholar 

  31. Gulis V, Marvanová L, Descals E (2005) An illustrated key to the common temperate species of aquatic hyphomycetes. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition—a practical guide. Springer, Dodrecht, pp 153–167

    Chapter  Google Scholar 

  32. Laitung B, Chauvet E (2005) Vegetation diversity increases species richness of leaf-decaying fungal communities in woodland streams. Arch Hydrobiol 164:217–235

    Article  Google Scholar 

  33. Suberkropp K, Arsuffi TL, Anderson JP (1983) Comparison of degradative ability, enzymatic activity, and palatability of aquatic hyphomycetes grown on leaf litter. Appl Environ Microbiol 46:237–244

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Core Team R (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  35. Woodward G, Gessner MO, Giller PS, Gulis V, Hladyz S, Lecerf A, Malmqvist B, McKie B, Tiegs SD, Cariss H, Dobson M, Elosegi A, Ferreira V, Graça MAS, Fleituch T, Lacoursière JO, Nistorescu M, Pozo J, Risnoveanu G, Schindler M, Vadineanu A, Vought LB-M, Chauvet E (2012) Continental-scale effects of nutrient pollution on stream ecosystem functioning. Science 336:1438–1440

    Article  CAS  PubMed  Google Scholar 

  36. Jabiol J, Cornut J, Tlili A, Gessner MO (2018) Interactive effects of dissolved nitrogen, phosphorus and litter chemistry on stream fungal decomposers. FEMS Microbiol Ecol 94(10). https://doi.org/10.1093/femsec/fiy151

  37. Danger M, Chauvet E (2013) Elemental composition and degree of homeostasis of fungi: are aquatic hyphomycetes more like metazoans, bacteria or plants? Fungal Ecol 6:453–457

    Article  Google Scholar 

  38. Godwin CM, Cotner JB (2015) Aquatic heterotrophic bacteria have highly flexible phosphorus content and biomass stoichiometry. ISME J 9:2324–2327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Sinsabaugh RL, Follstad Shah JJ (2012) Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol Syst 43:313–343

    Article  Google Scholar 

  40. Gessner MO (1991) Differences in processing dynamics of fresh and dried leaf litter in a stream ecosystem. Freshw Biol 26:387–298

    Article  CAS  Google Scholar 

  41. Stelzer RS, Heffernan J, Likens GE (2003) The influence of dissolved nutrients and particulate organic matter quality on microbial respiration and biomass in a forest stream. Freshw Biol 48:1925–1937

    Article  CAS  Google Scholar 

  42. Gulis V, Rosemond AD, Suberkropp K, Weyers HS, Benstead JP (2004) Effects of nutrient enrichment on the decomposition of wood and associated microbial activity in streams. Freshw Biol 49:1437–1447

    Article  Google Scholar 

  43. Shearer CA, Webster J (1991) Aquatic hyphomycete communities in the River Teign. IV. Twig colonization. Mycol Res 94:413–420

    Article  Google Scholar 

  44. Manning DWP, Rosemond AD, Gulis V, Benstead JP, Kominoski JS (2018) Nutrients and temperature additively increase stream microbial respiration. Glob Change Biol 24:e233–e247

  45. Boyero L, Graça MAS, Tonin AM, Pérez J, Swafford AJ, Ferreira V, Landeira-Dabarca A, Alexandrou MA, Gessner MO, McKie BG, Albariño RJ, Barmuta LA, Callisto M, Chará J, Chauvet E, Colón-Gaud C, Dudgeon D, Encalada AC, Figueroa R, Flecker AS, Fleituch T, Frainer A, Gonçalves Jr JF, Helson JE, Iwata T, Mathooko J, M’Erimba C, Pringle CM, Ramírez A, Swan CM, Yule CM, Pearson RG (2017) Riparian plant litter quality increases with latitude. Sci Rep 7:1–10

    Article  CAS  Google Scholar 

  46. Leroy CJ, Whitham TG, Wooley SC, Marks JC (2007) Within-species variation in foliar chemistry influences leaf-litter decomposition in a Utah river. J N Am Benthol Soc 26:426–438

    Article  Google Scholar 

  47. Leroy CJ, Wooley SC, Lindroth RL (2012) Genotype and soil nutrient environment influence aspen litter chemistry and in-stream decomposition. Freshwat Sci 31:1244–1253

    Article  Google Scholar 

  48. Makkonen M, Berg MP, Handa IT, Hättenshwiler S, van Ruijven J, van Bodegom PM, Aerts R (2012) Highly consistent effects of plant litter identity and functional traits on decomposition across a latitudinal gradient. Ecol Lett 15:1033–1041

    Article  PubMed  Google Scholar 

  49. Boisvert-Marsh L, Périé C, de Blois S (2014) Shifting with climate? Evidence for recent changes in tree species distribution at high latitudes. Ecosphere 5:1–33

    Article  Google Scholar 

  50. Tuchman NC, Wetzel RG, Rier ST, Wahtera KA, Teeri JA (2002) Elevated atmospheric CO2 lowers leaf litter nutritional quality for stream ecosystem food webs. Glob Change Biol 8:163–170

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Acknowledgments

The authors are grateful to Frédéric Julien and Wendy Amblas for litter CNP analyses.

Funding

This study is part of the FunctionalStreams project funded by the French National Research Agency (grant ANR-14-CE01-0009-01).

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Correspondence to Jérémy Jabiol.

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Jabiol, J., Lecerf, A., Lamothe, S. et al. Litter Quality Modulates Effects of Dissolved Nitrogen on Leaf Decomposition by Stream Microbial Communities. Microb Ecol 77, 959–966 (2019). https://doi.org/10.1007/s00248-019-01353-3

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  • DOI: https://doi.org/10.1007/s00248-019-01353-3

Keywords

  • Litter breakdown
  • Nutrient enrichment
  • Freshwater fungi
  • Litter lignin
  • Michaelis–Menten–Monod kinetics
  • Litter traits