Responses of microbially driven leaf litter decomposition to stream nutrients depend on litter quality
- 299 Downloads
Abstract
The present study aims to understand how microbial decomposition of leaf litter from two riparian tree species differing in their quality varies among streams covering a gradient of nutrient concentrations. We incubated leaf litter from alder (Alnus glutinosa) and sycamore (Platanus × hispanica) in 3 streams with low human pressure and 2 streams influenced by wastewater treatment plant effluents. We quantified leaf litter decomposition rates (k) and examined the temporal changes in the leaf litter concentrations of carbon (C) and nitrogen (N) throughout the incubation period. We measured the extracellular enzyme activities involved in degradation of C (i.e., cellobiohydrolase) and organic phosphorus (i.e., phosphatase). Results showed that alder k decreased with increasing nutrient concentrations, while sycamore decomposed similarly among streams. For both species, leaf litter N concentrations were positively related to in-stream dissolved N concentrations. However, we found different temporal patterns of leaf litter N concentrations between species. Finally, we found relevant differences in the enzymatic activities associated to each leaf litter species across the nutrient gradient. These results suggest that the intrinsic characteristics of the leaf litter resources may play a relevant role on the microbially driven leaf litter decomposition and mediate its response to dissolved nutrient concentrations across streams.
Keywords
Stream Leaf litter decomposition Leaf litter quality Nitrogen Phosphorus Microbial exoenzymatic activityNotes
Acknowledgements
The authors would like to thank R. Ventosa for the chemical analyses done at the Nutrient Analysis Service of CEAB. We thank the anonymous reviewers whose comments contributed to improve the present study. The financial support was provided by the Spanish Ministry of Science and Innovation through the MED-FORESTREAM (ref: CGL2011-30590-C02-02) project. E. Bastias was granted by a FPI PhD fellowship from the Spanish Ministry of Science and Innovation through the MED-FORESTREAM project. M. Ribot was supported by a technical training contract also associated to MED-FORESTREAM project. Funding was provided by Consejo Superior de Investigaciones Científicas (Grant No. BES-2012-053358).
Supplementary material
References
- Albelho, M. & M. A. S. Graça, 2006. Effects of nutrient enrichment on decomposition and fungal colonization of sweet chestnut leaves in an Iberian stream (Central Portugal). Hydrobiologia 560: 239–247.CrossRefGoogle Scholar
- Allison, S. D. & P. M. Vitousek, 2005. Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biology & Biochemistry 37: 937–944.CrossRefGoogle Scholar
- American Public Health Association (APHA), 1998. Standard methods for examination of water and wastewater, 20th ed. United Book Press, Baltimore, MD.Google Scholar
- Artigas, J., A. M. Romaní & S. Sabater, 2004. Organic matter decomposition by fungi in a mediterranean forested stream: contribution of streambed substrata. Annales de Limmologie 40: 269–277.CrossRefGoogle Scholar
- Artigas, J., A. Gaudes, I. Muñoz, A. M. Romaní & S. Sabater, 2011. Fungal and bacterial colonization of submerged leaf litter in a Mediterranean stream. International Review of Hydrobiology 96: 221–234.CrossRefGoogle Scholar
- Baldy, V., V. Gobert, F. Guérold, E. Chauvet, D. Lambrigot & J. Y. Charcosset, 2007. Leaf litter breakdown budgets in streams of various trophic status: effects of dissolved inorganic nutrients on microorganisms and invertebrates. Freshwater Biology 52: 1322–1335.CrossRefGoogle Scholar
- Bernot, M. J. & W. K. Dodds, 2005. Nitrogen retention, removal, and saturation in lotic ecosystems. Ecosystems 8: 442–453.CrossRefGoogle Scholar
- Canhoto, C. & M. A. S. Graça, 1999. Leaf barriers to fungal colonization and shredders (Tipula lateralis) consumption of decomposing Eucalyptus globulus. Microbial Ecology 37: 163–172.CrossRefPubMedGoogle Scholar
- Cornwell, W. K., J. H. C. Cornelissen, K. Amatangelo, E. Dorrepaal, V. T. Eviner, O. Godoy, S. E. Hobbie, B. Hoorens, H. Kurokawa, N. Pérez-Harguindeguy, H. M. Quested, L. S. Santiago, D. A. Wardle, I. J. Wright, R. Aerts, S. D. Allison, P. van Bodegom, V. Brovkin, A. Chatain, T. V. Callaghan, S. Díaz, E. Garnier, D. E. Gurvich, E. Kazakou, J. A. Klein, J. Read, P. B. Reich, N. A. Soudzilovskaia, M. V. Vaieretti & M. Westoby, 2008. Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecology letters 11: 1065–1071.CrossRefPubMedGoogle Scholar
- Chadwick, M. A. & A. D. Huryn, 2003. Effect of a whole-catchment N addition on stream detritus processing. Journal of the North American Benthological Society 22: 194–206.CrossRefGoogle Scholar
- Chauvet, E., V. Ferreira, P. S. Giller, B. G. McKie, S. D. Tiegs, G. Woodward, A. Elosegi, M. Dobson, T. Fleituch, M. A. S. Graça, V. Gulis, S. Hladyz, J. O. Lacoursière, A. Lecerf, J. Pozo, E. Preda, M. Riipinen, G. Rîşnoveanu, A. Vadineanu, L. B.-M. Vought & M. O. Gessner, 2016. Litter decomposition as an indicator of stream ecosystem functioning at local-to-continental scales: insights from the European RivFunction project. Advances in Ecological Research 55: 99–182.CrossRefGoogle Scholar
- Enríquez, S., C. M. Duarte & K. Sand-Jensen, 1993. Patterns in decomposition rates among photosynthetic organisms: the importance of detritus C:N: P content. Oecologia 94: 457–471.CrossRefPubMedGoogle Scholar
- Fernandes, I., S. Sahadevan, C. Pascoal & F. Cássio, 2014. Elevated temperature may intensify the positive effects of nutrients on microbial decomposition in streams. Freshwater Biology 59: 2390–2399.CrossRefGoogle Scholar
- Ferreira, V., B. Castagneyrol, J. Koricheva, V. Gulis, E. Chauvet & M. A. S. Graça, 2015. A meta-analysis of the effects of nutrient enrichment on litter decomposition in streams. Biological Reviews 90: 669–688.CrossRefPubMedGoogle Scholar
- Ferreira, V., J. Koricheva, S. Duarte, D. K. Niyogi & F. Guérold, 2016. Effects of anthropogenic heavy metal contamination on litter decomposition in streams – a meta-analysis. Environmental Pollution 20: 261–270.CrossRefGoogle Scholar
- Fisher, S. G. & G. E. Likens, 1973. Energy flow in Bear Brook, New Hampshire: an integrative approach to stream ecosystem metabolism. Ecological Monographs 43: 421–439.CrossRefGoogle Scholar
- Freeman, C. & M. Lock, 1992. Recalcitrant high molecular-weight material, an inhibitor of microbial metabolism in river biofilms. Applied and Environmental Microbiology 58: 2030–2033.PubMedPubMedCentralGoogle Scholar
- Gessner, M. & E. Chauvet, 1994. Importance of stream microfungi in controlling breakdown rates of leaf litter. Ecology 75: 1807–1917.CrossRefGoogle Scholar
- Gordon, N. D., T. A. McMahon & B. L. Finlayson, 2004. Stream hydrology: an introduction for ecologist. Wiley, Chichester.Google Scholar
- Gulis, V. & K. Suberkropp, 2003. Leaf litter decomposition and microbial activity in nutrient-enriched and unaltered reaches of a headwater stream. Freshwater Biology 48: 123–134.CrossRefGoogle Scholar
- Gulis, V., V. Ferreira & M. A. S. Graça, 2006. Stimulation of leaf litter decomposition and associated fungi and invertebrates by moderate eutrophication: implications for stream assessment. Freshwater Biology 51: 1655–1669.CrossRefGoogle Scholar
- Hall, R. & J. L. Meyer, 1998. The trophic significance of bacteria in a detritus-based stream food web. Ecology 79: 1995–2012.CrossRefGoogle Scholar
- Kaushik, N. K. & H. B. N. Hynes, 1971. The fate of the dead leaves that fall into streams. Archiv für Hydrobiologie 68: 465–515.Google Scholar
- Lecerf, A., P. Usseglio-Polatera, J. Y. Charcosset, D. Lambrigot, B. Bracht & E. Chauvet, 2006. Assessment of functional integrity of eutrophic streams using litter breakdown and benthic macroinvertebrates. Archiv für Hydrobiologie 165: 105–126.CrossRefGoogle Scholar
- Melillo, J., A. Janetos, D. Schimel & T. Kittel, 2001. Vegetation and biogeochemical scenarios. Chapter 2. In Melillo, J. M., A. C. Janetos & T. R. Karl (eds), Climate Change Impacts on the United States: The Potential Consequences of Climate Variability and Change, Report for the US Global Change Research Program. Cambridge University Press, Cambridge.Google Scholar
- Molinero, J., J. Pozo & E. Gonzalez, 1996. Litter breakdown in streams of the Agüera catchment influence of dissolves nutrients and land use. Freshwater Biology 36: 745–756.CrossRefGoogle Scholar
- Pascoal, C. & F. Cássio, 2004. Contribution of fungi and bacteria to leaf litter decomposition in a polluted river. Applied and Environmental Microbiology 70: 5266–5273.CrossRefPubMedPubMedCentralGoogle Scholar
- Pereira, A., P. Geraldes, E. Lima-Fernandes, I. Fernandes, F. Cássio & C. Pascoal, 2016. Structural and functional measures of leaf-associated invertebrates and fungi as predictors of stream eutrophication. Ecological Indicators 69: 648–656.CrossRefGoogle Scholar
- Petersen, R. & K. Cummins, 1974. Leaf processing in a woodland stream. Freswater Biology 4: 345–368.Google Scholar
- Pozo, J., A. Basaguren, A. Elosegui, J. Molinero, E. Fabre & E. Chauvet, 1998. Afforestation with Eucalyptus globulus and leaf litter decomposition in streams of northern Spain. Hydrobiologia 373(374): 101–109.CrossRefGoogle Scholar
- Richarson, J. S., C. R. Shaughnessy & P. G. Harrison, 2004. Litter breakdown and invertebrate association with three types of leaves in a temperate rainforest stream. Archiv für Hydrobiologie 159: 309–325.CrossRefGoogle Scholar
- Rogers, H. J., 1961. The assimilation of high molecular weight organic substances. In Gunsalus, I. C. & R. Y. Stanier (eds), The Bacteria. Academic Press, New York: 261–318.Google Scholar
- Romaní, A. M., A. Giorgi, V. Acuña & S. Sabater, 2004. The influence of substratum type and nutrient supply on biofilm organic matter utilization in streams. Limnololy & Oceanography 49: 1713–1721.CrossRefGoogle Scholar
- Romaní, A. M., H. Fischer, C. Mille-Lindblom & L. J. Tranvik, 2006. Interactions of bacteria and fungi on decomposing litter: differential extracellular enzyme activities. Ecology 87: 2559–2569.CrossRefPubMedGoogle Scholar
- Romaní, A.M., J. Artigas & I. Ylla, 2012. Extracellular enzymes in aquatic biofilms: microbial interactions versus water quality effects in the use of organic matter. In: Microbial Biofilms: Current Research and Applications (Gavin Lear and Gillian D. Lewis), pp. 153–174. Lincoln University, Christchurch, New Zealand and University of Auckland, New Zealand.Google Scholar
- Rosemond, A. D., C. M. Pringle, A. Ramírez, M. J. Paul & J. Meyer, 2002. Landscape variation in phosphorus concentration and effect on detritus-based tropical streams. Limnology & Oceanography 47: 278–289.CrossRefGoogle Scholar
- Rosemond, A. D., J. P. Benstead, P. M. Bumpers, V. Gulis, J. S. Kominoski, D. W. P. Manning, K. Suberkropp & J. B. Wallace, 2015. Experimental nutrient additions accelerate terrestrial carbon loss from stream ecosystems. Science 347: 1142–1145.CrossRefPubMedGoogle Scholar
- Royer, T. V. & G. W. Minshall, 2001. Effects of nutrient enrichment and leaf quality on the breakdown of leaves in a headwater stream. Freshwater Biology 46: 603–610.CrossRefGoogle Scholar
- Sala, M. M., M. Karner, L. Arin & C. Marrasé, 2001. Measurement of ectoenzyme activities as an indication of inorganic nutrient imbalance in microbial communities. Aquatic Microbial Ecology 23: 310–311.CrossRefGoogle Scholar
- Sabater, S., V. Acuña, A. Giorgi, E. Guerra, I. Muñoz & A. M. Romaní, 2005. Effects of nutrient inputs in a forested Mediterranean stream under moderate light availability. Archiv für Hydrobiologie 163: 479–496.CrossRefGoogle Scholar
- Schindler, M. H. & M. O. Gessner, 2009. Functional leaf traits and biodiversity effects on litter decomposition in a stream. Ecology 90: 1641–1649.CrossRefPubMedGoogle Scholar
- Sinsabaugh, R. L., R. K. Antibus, A. E. Linkins, C. A. McClaugherty, L. Rayburn, D. Repert & T. Weiland, 1993. Wood decomposition: nitrogen and phosphorous dynamics in relation to extracellular enzyme activity. Ecology 74: 1586–1593.CrossRefGoogle Scholar
- Sinsabaugh, R. L., M. P. Osgood & S. Findlay, 1994. Enzymatic models for estimating decomposition rates of particulate detritus. Journal of the North American Benthological Society 13: 160–169.CrossRefGoogle Scholar
- Sinsabaugh, R. L., M. E. Gallo, C. Lauber, M. P. Waldrop & D. R. Zak, 2005. Extracellular enzyme activities and soil organic matter dynamics for northern hardwood forests receiving simulated nitrogen deposition. Biogeochemistry 75: 201–215.CrossRefGoogle Scholar
- Suberkropp, K. & E. Chauvet, 1995. Regulation of leaf breakdown by fungi in streams: influences of water chemistry. Ecology 76: 1433–1445.CrossRefGoogle Scholar
- Tank, J. L. & J. R. Webster, 1998. Interaction of substrate availability and nutrient distribution on wood biofilm development in streams. Ecology 79: 2168–2179.CrossRefGoogle Scholar
- Tank, J. L., J. L. Meyer, D. M. Sanzone, P. J. Mulholland, J. R. Webster, B. J. Peterson, W. M. Wolheim & N. E. Leonard, 2000. Analysis of nitrogen cycling in a forest stream during autumn using a 15N-tracer addition. Limnology & Oceanography 45: 1013–1029.CrossRefGoogle Scholar
- Vannote, R. L., G. W. Minshall, K. W. Cummins, J. R. Sedell & C. E. Cushing, 1980. The river continuum concept. Canadian Journal of Fisheries and Aquatic Sciences 37: 130–137.CrossRefGoogle Scholar
- von Schiller, D., E. Martí, J. L. Riera, M. Ribot, A. Argerich, P. Fonollà & F. Sabater, 2008. Inter-annual, annual and seasonal variation of P and N retention in a perennial and an intermittent stream. Ecosystems 11: 670–687.CrossRefGoogle Scholar
- Webster, J. R. & E. F. Benfield, 1986. Vascular plant breakdown in freshwater ecosystems. Annual Review of Ecology and Systematics 17: 567–594.CrossRefGoogle Scholar
- Wallace, J. B., S. L. Eggert, J. L. Meyer & J. R. Webster, 1999. Effects of resource limitation on a detrital-based ecosystem. Ecological Monographs 69: 409–442.CrossRefGoogle Scholar
- Webster, J. R., J. D. Newbold, S. A. Thomas, M. H. Valett & P. J. Mulholland, 2009. Nutrient uptake and mineralization during leaf decay in streams – a model simulation. International Review of Hydrobiology 94: 372–390.CrossRefGoogle Scholar
- Woodward, G., M. O. Gessner, P. S. Giller, V. Gulis, S. Hladyz, A. Lecerf, B. Malmqvist, B. G. Mckie, S. D. Tiegs, H. Cariss, M. Dobson, A. Elosegi, V. Ferreira, M. A. S. Graça, T. Fleithuch, J. O. Lacoursière, M. Nitorescu, J. Pozo, G. Risnoveau, M. Schindler, A. Vadineanu, L. B.-M. Vought & E. Chauvet, 2012. Continental-scale effects of nutrient pollution on stream ecosystem functioning. Science 336: 1438–1440.CrossRefPubMedGoogle Scholar
- Zar, J. H., 1999. Biostatistics Analysis, 4th ed. Prentice-Hall, Englewood Cliffs, NJ.Google Scholar