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Biochemical quality of basal resources in a forested stream: effects of nutrient enrichment

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Abstract

We studied biochemical changes in biofilm and suspended particulate and dissolved organic matter (OM) during the leaf emergence period (March–May 2008) in a forested headwater stream in response to a long-term (4 years, 2004–2008) experimental nutrient enrichment study. This study compared results from one reach upstream of the enrichment point and one reach downstream using moderate nutrient concentrations (nitrogen, N, from 388 to 765 μg L−1 and phosphorus, P, from 10 to 30 μg L−1, resulting in N:P ratios of 85–56). During the spring of 2008, we analysed the chlorophyll content, elemental composition (carbon, C, and N), bacterial density, and extracellular enzyme activities along with their biochemical composition (amino acids, fatty acids and sterols) on biofilm and OM. Nutrients caused changes in the biochemical composition of the biofilm, while changes in the OM were subtle. The C:N ratio of the biofilm decreased with nutrient enrichment likely due to the increase in protein (non-essential amino acids). The polysaccharide and total and essential fatty acid contents were higher when nutrient enrichment coincided with greater light availability. The peptidase extracellular activity was higher in the fertilised reach at early spring, while phosphatase activity decreased at late spring. The suspended and dissolved OM composition did not change due to the nutrient addition, likely due to the lower water residence time in the reach. Headwater systems are highly dynamic, and the biochemical composition of the biofilm changed in response to changes in nutrients but also to light in this study. These changes, although moderate, could influence higher trophic levels through modifications in their diet. This experiment exemplifies how small land use shifts may affect headwater streams.

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References

  • Acuña V, Giorgi A, Muñoz I, Uehlinger U, Sabater S (2004) Flow extremes and benthic organic matter shape the metabolism of a headwater Mediterranean stream. Freshw Biol 49(7):960–971

    Article  Google Scholar 

  • Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37(5):937–944

    Article  CAS  Google Scholar 

  • Anderson NH, Cummins KW (1979) Influences of diet on the life histories of aquatic insects. J Fish Res Board Can 36(3):335–342

    Article  Google Scholar 

  • Anderson TR, Boersma A, Raubenheimer D (2004) Stoichiometry: linking elements to biochemicals. Ecology 85(5):1193–1202

    Article  Google Scholar 

  • A.P.H.A. (ed) (1995) Standard methods for the examination of water and wastewater, 19th edn. American Publich Health Association, Washington

    Google Scholar 

  • Arnosti C (2003) Microbial extracellular enzymes and their role in dissolved organic matter cycling. In: Findlay SEG, Sinsabaugh RL (eds) Aquatic ecosystems: interactivity of dissolved organic matter. Academic, San Diego, pp 315–342

    Chapter  Google Scholar 

  • Bates SS, de Freitas ASW, Milley JE, Pocklington R, Quiliam MA, Smith JC, Worms J (1991) Controls on domoic acid production by the diatom Nitzschia pungens f. multiseries in culture: nutrients and irradiance. Can J Fish Aquat Sci 48:1136–1144

    Article  CAS  Google Scholar 

  • Benstead JP, Rosemond AD, Cross WF, Wallace JB, Eggert SL, Suberkropp K, Gulis V, Greenwood JL, Tant CJ (2009) Nutrient enrichment alters storage and fluxes of detritus in a headwater stream ecosystem. Ecology 90(9):2556–2566

    Article  PubMed  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Phys 37(8):911–917

    Article  CAS  Google Scholar 

  • Brett MT, Müller-Navarra DC (1997) The role of highly unsaturated fatty acids in aquatic food web processes. Freshw Biol 38(3):483–499

    Article  CAS  Google Scholar 

  • Butturini A, Álvarez M, Bernal S, Vázquez E, Sabater F (2008) Diversity and temporal sequences of forms of DOC and NO3-discharge responses in an intermittent stream: predictable or random succession? J Geophys Res 113(G3):G03016

    Article  Google Scholar 

  • Carr GM, Morin A, Chambers PA (2005) Bacteria and algae in stream periphyton along a nutrient gradient. Freshw Biol 50:1337–1350

    Article  Google Scholar 

  • Chanudet V, Filella M (2006) The application of the MBTH method for carbohydrate determination in freshwaters revisited. Int J Environ Anal Chem 86(9):693–712

    Article  CAS  Google Scholar 

  • Cross WF, Benstead JP, Rosemond AD, Bruce Wallace J (2003) Consumer-resource stoichiometry in detritus-based streams. Ecol Lett 6(8):721–732

    Article  Google Scholar 

  • Cross WF, Wallace JB, Rosemond AD, Eggert SL (2006) Whole-system nutrient enrichment increases secondary production in a detritus-based ecosystem. Ecology 87(6):1556–1565

    Article  CAS  PubMed  Google Scholar 

  • Dauwe B, Middelburg JJ (1998) Amino acids and hexosamines as indicators of organic matter degradation state in North Sea sediments. Limnol Oceanogr 43:782–798

    Article  CAS  Google Scholar 

  • Dauwe B, Middelburg JJ, Herman PMJ, Heip CHR (1999) Linking diagenetic alteration of amino acids and bulk organic matter reactivity. Limnol Oceanogr 44(7):1809–1814

    Article  CAS  Google Scholar 

  • Davis JM, Rosemond AD, Eggert SL, Cross WF, Wallace JB (2010) Long-term nutrient enrichment decouples predator and prey production. PNAS 107(1):121–126

    Article  CAS  PubMed  Google Scholar 

  • Deshpande V, Eriksson KE (1988) 1,4-β-Glucosidases of Sporotrichum pulverulentum. Methods Enzymol 160:415–424

    Article  CAS  Google Scholar 

  • Desvilettes C, Bourdier G, Breton JC, Combrouze P (1994) Fatty acids as organic markers for the study of trophic relationships in littoral cladoceran communities of a pond. J Plankton Res 16:643–659

    Article  Google Scholar 

  • Desvilettes C, Bourdier G, Amblard C, Barth B (1997) Use of fatty acids for the assessment of zooplankton grazing on bacteria, protozoans and microalgae. Freshw Biol 38(3):629–637

    Article  CAS  Google Scholar 

  • FAO Agricultural Development Economics Division (2012) World agriculture towards 2030/2050: the 2012 revision. Global Perspective Studies Team ESA Working Paper No. 12-03

  • Dodds WK, Smith VH, Lohman K (2002) Nitrogen and phosphorus relationships to benthic algal biomass in temperate streams. Can J Fish Aquat Sci 59(5):865–874

    Article  Google Scholar 

  • Espeland EM, Francoeur SN, Wetzel RG (2001) Influence of algal photosynthesis on biofilm bacterial production and associated glucosidase and xylosidase activities. Microb Ecol 42(4):524–530

    Article  CAS  PubMed  Google Scholar 

  • Fellman JB, Hood E, Spencer RGM (2010) Fluorescence spectroscopy opens new windows into dissolved organic matter dynamics in freshwater ecosystems: a review. Limnol Oceanogr 55(6):2452–2462

    Article  CAS  Google Scholar 

  • Francoeur SN, Wetzel RG (2003) Regulation of periphytic leucine-aminopeptidase activity. Aquat Microb Ecol 31(3):249–258

    Article  Google Scholar 

  • Frost PC, Stelzer RS, Lamberti GA, Elser JJ (2002) Ecological stoichiometry of trophic interactions in the benthos: understanding the role of C: N: P ratios in lentic and lotic habitats. J N Am Benthol Soc 21(4):515–528

    Article  Google Scholar 

  • Gaudes A, Ocaña J, Muñoz I (2012) Meiofaunal responses to nutrient additions in a Mediterranean stream. Freshw Biol 57:956–968

    Article  CAS  Google Scholar 

  • Gordon ND, McMahon TA, Finlayson BL (1992) Stream hydrology: an introduction for ecologists, vol First. Prentice-Hall, Upper Saddle River

    Google Scholar 

  • Greenwood JL, Rosemond AD (2005) Periphyton response to long-term nutrient enrichment in a shaded headwater stream. Can J Fish Aquat Sci 62(9):2033–2045

    Article  CAS  Google Scholar 

  • Greenwood JL, Rosemond AD, Wallace JB, Cross WF, Weyers HS (2007) Nutrients stimulate leaf breakdown rates and detritivore biomass: bottom-up effects via heterotrophic pathways. Oecologia 151(4):637–649

    Article  PubMed  Google Scholar 

  • Gremare A, Amouroux JM, Charles F, Dinet A, RiauxGobin C, Baudart J, Medernach L, Bodiou JY, Vetion G, Colomines JC, Albert P (1997) Temporal changes in the biochemical composition and nutritional value of the particulate organic matter available to surface deposit-feeders: a two year study. Mar Ecol Prog Ser 150(1–3):195–206

    Article  CAS  Google Scholar 

  • Hepinstall JA, Fuller RL (1994) Periphyton reactions to different light and nutrient levels and the response of bacteria to these manipulations. Archiv fur Hydrobil 131:161–173

    Google Scholar 

  • Hill WR, Mulholland PJ, Marzolf ER (2001) Stream ecosystem responses to forest leaf emergence in spring. Ecology 82(8):2306–2319

    Article  Google Scholar 

  • Hill WR, Rinchard J, Czesny S (2011) Light, nutrients and the fatty acid composition of stream periphyton. Freshw Biol 56(9):1825–1836

    Article  CAS  Google Scholar 

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167(2):191–194

    CAS  Google Scholar 

  • Klotz RL (1992) Factors influencing alkaline phosphatase activity of stream epilithon. J Freshw Ecol 7(2):233–242

    Article  CAS  Google Scholar 

  • Kolmakova AA, Gladyshev MI, Kalachova GS, Kravchuk ES, Ivanova EA, Sushchik NN (2013) Amino acid composition of epilithic biofilm and benthic animals in a large Siberian river. Freshw Biol 58(10):2180–2195

    Article  CAS  Google Scholar 

  • Lamberti GA (1996) The role of periphyton in benthic food webs. In: Stevenson RJ, Bothwell ML, Lowe RL (eds) Algal ecology. Academic, San Diego, pp 533–572

    Chapter  Google Scholar 

  • Ledger ME, Hildrew AG (1998) Temporal and spatial variation in the epilithic biofilm of an acid stream. Freshw Biol 40(4):655–670

    Article  Google Scholar 

  • Lepš J, Šmilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, New York

    Google Scholar 

  • Mannino A, Harvey HR (2000) Biochemical composition of particles and dissolved organic matter along an estuarine gradient: sources and implications for DOM reactivity. Limnol Oceanogr 45(4):775–788

    Article  CAS  Google Scholar 

  • Martin-Creuzburg D, Ev Elert (2009) Ecological significance of sterols in aquatic food webs. In: Kainz M, Brett MT, Arts MT (eds) Lipids in aquatic ecosystems. Springer, New York, pp 43–64

    Chapter  Google Scholar 

  • Meybeck M (2003) Global analysis of river systems: from Earth system controls to Anthropocene syndromes. Philos Trans R Soc Lond Ser B Biol Sci 358(1440):1935–1955

    Article  CAS  Google Scholar 

  • Napolitano GE (1999) Fatty acids as trophic and chemical markers. In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer, New York, pp 21–44

    Chapter  Google Scholar 

  • Olsen Y (1999) Lipids and essential fatty acids in aquatic food webs: what can freshwater ecologists learn from mariculture? In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer, New York, pp 161–202

    Chapter  Google Scholar 

  • Pakulski JD, Benner R (1992) An improved method for the hydrolysis and MBTH analysis of dissolved and particulate carbohydrates in seawater. Mar Chem 40(3–4):143–160

    Article  CAS  Google Scholar 

  • Parrish CC (1999) Determination of total lipid, lipid classes, and fatty acids in aquatic samples. In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer, New York, pp 4–20

    Chapter  Google Scholar 

  • Phillips NW (1984) Role of different microbes and substrates as potential suppliers of specific, essential nutrients to marine detritivores. Bull Mar Sci 35(3):283–298

    Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York

    Book  Google Scholar 

  • Proia L, Romani AM, Sabater S (2012) Nutrient and light effects on stream biofilms: a combined assessment with CLSM, structural and functional parameters. Hydrobiologia 695:281–291

    Article  CAS  Google Scholar 

  • Romaní AM, Sabater S (2001) Structure and activity of rock and sand biofilms in a Mediterranean stream. Ecology 82(11):3232–3245

    Article  Google Scholar 

  • Romaní AM, Giorgi A, Acuña V, Sabater S (2004) The influence of substratum type and nutrient supply on biofilm organic matter utilization in streams. Limnol Oceanogr 49(5):1713–1721

    Article  Google Scholar 

  • Romaní AM, Artigas J, Ylla I (2012) Extracellular enzymes in aquatic biofilms: microbial interactions versus water quality effects in the use of organic matter. In: Lear G, Lewis G (eds) Microbial biofilms: current research and applications. Caister Academic, Norfolk, pp 153–174

    Google Scholar 

  • Rosemond AD, Mulholland PJ, Brawley SH (2000) Seasonally shifting limitation of stream periphyton: response of algal populations and assemblage biomass and productivity to variation in light, nutrients, and herbivores. Can J Fish Aquat Sci 57(1):66–75

    Article  Google Scholar 

  • 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 

  • Sabater S, Acuña V, Giorgi A, Guerra E, Muñoz I, Romaní AM (2005) Effects of nutrient inputs in a forested Mediterranean stream under moderate light availability. Arch Hydrobiol 163(4):479–496

    Article  CAS  Google Scholar 

  • Sabater S, Artigas J, Gaudes A, Muñoz I, Urrea G, Romaní AM (2011) Long-term moderate nutrient inputs enhance autotrophy in a forested Mediterranean stream. Freshw Biol 56(7):1266–1280

    Article  CAS  Google Scholar 

  • Smith VH, Joye SB, Howarth RW (2006) Eutrophication of freshwater and marine ecosystems. Limnol Oceanogr 51(1):351–355

    Article  CAS  Google Scholar 

  • Suberkropp K, Gulis V, Rosemond AD, Benstead JP (2010) Ecosystem and physiological scales of microbial responses to nutrients in a detritus-based stream: results of a five-year continuous enrichment. Limnol Oceanogr 55:149–160

    Article  Google Scholar 

  • Tant CJ, Rosemond AD, First MR (2013) Stream nutrient enrichment has a greater effect on coarse than on fine benthic organic matter. Freshwater Science 32:111–1121

    Article  Google Scholar 

  • Thurman EM (1985) Transport, origin and sources of dissolved organic carbon. In: Thurman EM (ed) Organic Geochemistry of Natural Waters. Martinus Nijhoff/Dr. W. Junk, Dordrecht, pp 67–85

    Chapter  Google Scholar 

  • Torres-Ruiz M, Wehr JD, Perrone AA (2007) Trophic relations in a stream food web: importance of fatty acids for macroinvertebrate consumers. J N Am Benthol Soc 26(3):509–522

    Article  Google Scholar 

  • Veraart AJ, Romaní AM, Tornes E, Sabater S (2008) Algal response to nutrient enrichment in forested oligotrophic stream. J Phycol 44(3):564–572

    Article  CAS  PubMed  Google Scholar 

  • Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277(5325):494–499

    Article  CAS  Google Scholar 

  • Vrba J, Callieri C, Bittl T, Šimek K, Bertoni R, Filandr P, Hartman P, Hejzlar J, Macek M, Nedoma J (2004) Are bacteria the major producers of extracellular glycolytic enzymes in aquatic environments? Int Rev Hydrobiol 89(1):102–117

    Article  CAS  Google Scholar 

  • Williams C, Scott A, Wilson H, Xenopoulos M (2012) Effects of land use on water column bacterial activity and enzyme stoichiometry in stream ecosystems. Aquat Sci 74(3):483–494

    Article  CAS  Google Scholar 

  • Ylla I, Romaní AM, Sabater S (2007) Differential effects of nutrients and light on the primary production of stream algae and mosses. Fundam Appl Limnol 170(1):1–10

    Article  CAS  Google Scholar 

  • Ylla I, Borrego C, Romaní AM, Sabater S (2009) Availability of glucose and light modulates the structure and function of a microbial biofilm. FEMS Microb Ecol 69(1):27–42

    Article  CAS  Google Scholar 

  • Ylla I, Sanpera-Calbet I, Vázquez E, Romaní AM, Muñoz I, Butturini A, Sabater S (2010) Organic matter availability during pre- and post-drought periods in a Mediterranean stream. Hydrobiologia 657:217–232

    Article  CAS  Google Scholar 

  • Ylla I, Sanpera-Calbet I, Muñoz I, Romaní AM, Sabater S (2011) Organic matter characteristics in a Mediterranean stream through amino acid composition: changes driven by intermittency. Aquat Sci 73:523–535

    Article  CAS  Google Scholar 

  • Zollner N, Kirsch K (1962) Uber die quantitative bestimmung yon lipoiden (mikromethode) mittels der vielen natiirliehen lipoiden (allen bekannten plasmalipoiden) gemeinsamen sulfophosphovanillin-reaktion. Z Gesamte Exp Med 135:545–561

    Article  Google Scholar 

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Acknowledgments

We kindly thank J. Artigas for his work in the stream fertilisation, L. Proia for his help during the sampling and J. Barbosa and A. Roubinet for their help in lipid analysis. Discharge values have been provided by A. Butturini. We thank the valuable comments of the anonymous reviewers. This work has been funded by the Spanish Ministry of Economy and Competitiveness with projects CGL2014-58760-C3-R. The analysis of fatty acids was performed at the Scientific and Technical Services Centre of the University of Barcelona. ISC held a doctoral fellowship from the University of Barcelona.

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Authors and Affiliations

  1. Departament d’Ecologia, Universitat de Barcelona (UB), Diagonal 643, 08028, Barcelona, Catalonia, Spain

    Isis Sanpera-Calbet & Isabel Muñoz

  2. Institut d’Ecologia Aquàtica, Universitat de Girona (UdG), Campus Montilivi, 17071, Girona, Catalonia, Spain

    Irene Ylla, Anna M. Romaní & Sergi Sabater

  3. Institut Català de Recerca de l’Aigua (ICRA), Emili Grahit 101, 17003, Girona, Catalonia, Spain

    Sergi Sabater

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  1. Isis Sanpera-Calbet
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  2. Irene Ylla
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Correspondence to Isabel Muñoz.

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Sanpera-Calbet, I., Ylla, I., Romaní, A.M. et al. Biochemical quality of basal resources in a forested stream: effects of nutrient enrichment. Aquat Sci 79, 99–112 (2017). https://doi.org/10.1007/s00027-016-0482-3

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