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Biogeochemistry

, Volume 54, Issue 3, pp 297–340 | Cite as

Nitrogen uptake and transformation in a midwestern U.S. stream: A stable isotope enrichment study

  • Stephen K. Hamilton
  • Jennifer L. Tank
  • David F. Raikow
  • Wilfred M. Wollheim
  • Bruce J. Peterson
  • Jackson R. Webster
Article

Abstract

This study presents a comprehensive analysis ofnitrogen (N) cycling in a second-order forestedstream in southern Michigan that has moderatelyhigh concentrations of ammonium (mean,16 μg N/L) and nitrate (17 μg N/L). Awhole-stream 15NH4+ addition wasperformed for 6 weeks in June and July, and thetracer 15N was measured downstream inammonium, nitrate, and detrital and livingbiomass. Ancillary measurements includedbiomass of organic matter, algae, bacteria andfungi, nutrient concentrations, hydrauliccharacteristics, whole-stream metabolism, andnutrient limitation assays. The resultsprovide insights into the heterotrophic natureof woodland streams and reveal the rates atwhich biological processes alter nitrogentransport through stream systems.

Ammonium uptake lengths were 766–1349 m anduptake rates were 41–60 μg N m−2min−1. Nitrate uptake could not bedetected. Nitrification rates were estimatedfrom the downstream increase in15N-enriched nitrate using a simulationmodel. The ammonium was removed bynitrification (57% of total uptake),heterotrophic bacteria and fungi associatedwith detritus (29%), and epilithic algae(14%). Growth of algae was likely limited bylight rather than nutrients, and dissolvedO2 revealed that the stream metabolism washeterotrophic overall (P:R = 0.2). Incubationsof detritus in darkened chambers showed thatuptake of 15N was mostly heterotrophic.

Microbial N in detritus and algal N inepilithon appeared to reach isotopic steadystate with the dissolved ammonium, but theisotopic enrichment of the bulk detritus andepilithon did not approach that of ammonium,probably due to a large fraction of organic Nin the bulk samples that was not turning over. The actively cycling fraction of total N inorganic compartments was estimated from theisotopic enrichment, assuming uptake ofammonium but not nitrate, to be 23% forepilithon, 1% for fine benthic organic matter,5% for small woody debris, and 7% for leaves. These percentages agree with independentestimates of epilithic algal biomass, whichwere based on carbon:chlorophyll ratios in bulksamples and in algal fractions separated bydensity-gradient centrifugation in colloidalsilica, and of microbial N in the detritus,which were based on N released by chloroformfumigations.

ammonium 15nitrification nitrogen stable isotopes streams 

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References

  1. Alexander RB,Smith RA &Schwarz GE (2000) Effect of stream channel size on the delivery of nitrogen to the Gulf of Mexico. Nature 403: 758–761Google Scholar
  2. Allan JD (1995) Stream ecology: Structure and Function of Running Waters. Chapman and Hall, LondonGoogle Scholar
  3. Aminot A,Kirkwood DS &Kérouel R (1997) Determination of ammonia in seawater by the indophenol-blue method: Evaluation of the ICES NUTS I/C 5 questionnaire. Mar. Chem. 56: 59–75Google Scholar
  4. Bansal MK (1977) Nitrification in natural streams. J. Wat. Pollut. Control Fed. 48: 2380–2393Google Scholar
  5. Battaglin WA &Goolsby DA (1997) Statistical modeling of agricultural chemical occurrence in midwestern rivers. J. Hydrol. 196: 1–25Google Scholar
  6. Bencala KE &Walters RA (1983) Simulation of solute transport in a mountain pool-and-riffle stream: A transient storage model. Water Resources Research 19: 718–724Google Scholar
  7. Brookes PC,Kragt JF,Powlson DS &Jenkinson DS (1985a) Chloroform fumigation and the release of soil N: The effects of fumigation time and temperature. Soil Biol. Biochem. 17: 831–835Google Scholar
  8. Brookes PC,Landman A,Pruden G &Jenkinson DS (1985b) Chloroform fumigation and the release of soil N: A rapid direct extraction method to measure microbial biomass N in soil. Soil Biol. Biochem. 17: 837–842Google Scholar
  9. Cabrera ML &Beare MH (1993) Alkaline persulfate oxidation for determining total nitrogen in microbial biomass extracts. Soil Sci. Soc. Am. J. 57: 1007–1012Google Scholar
  10. Caraco NF,Lampman G,Cole JJ,Limburg KE,Pace ML &Fischer D (1998) Microbial assimilation of DIN in a nitrogen rich estuary: Implications for food quality and isotope studies. Mar. Ecol. Prog. Ser. 167: 59–71Google Scholar
  11. Caraco N &Cole JJ (1999) Human impact on nitrate export: An analysis using major world rivers. Ambio 28: 167–170Google Scholar
  12. Cummins KW &Klug MJ (1979) Feeding ecology of stream invertebrates. Ann. Rev. Ecol. Syst. 10: 147–172Google Scholar
  13. Cummins KW,Klug MJ,Ward GM,Spengler GL,Speaker RW,Ovink DC,Mahan DC &Petersen RC (1981) Trends in particulate organic matter fluxes, community processes and macroinvertebrate functional groups along a Great Lakes Drainage Basin river continuum. Verh. Internat. Verein. Limnol. 21: 841–849Google Scholar
  14. Fenchel T,King GM &Blackburn TH (1998) Bacterial Biogeochemistry: The Ecophysiology of Mineral Cycling. Academic Press, San DiegoGoogle Scholar
  15. Fenn ME,Poth MA,Aber JD,Baron JS,Bormann BT,Johnson DW,Lemly AD,McNulty SG,Ryan DF &Stottlemyer R (1998) Nitrogen excess in North American ecosystems: Predisposing factors, ecosystem responses, and management strategies. Ecol. Applic. 8: 706–733Google Scholar
  16. Galloway JN,Schlesinger WH,Levy H. II,Michaels A &Schnoor J (1995) Nitrogen fixation: Anthropogenic enhancement-environmental response. Global Biogeochem. Cycles 9: 235–252Google Scholar
  17. Goolsby DA (2000) Mississippi basin nitrogen flux believed to cause Gulf hypoxia. Eos, Transactions, American Geophysical Union 81: 321–327Google Scholar
  18. Grasshoff K,Ehrhardt M &Kremling K (Eds) (1983) Methods of Seawater Analysis. Verlag Chemie, WeinheimGoogle Scholar
  19. Hall RO Jr,Peterson BJ &Meyer JL (1998) Testing a nitrogen-cycling model of a forest stream by using a nitrogen-15 tracer addition. Ecosystems 1: 283–298Google Scholar
  20. Hall RO Jr &Meyer JL (1998) The trophic significance of bacteria in a detritus-based stream food web. Ecology 79: 1995–2012Google Scholar
  21. Hamilton SK &Lewis WM Jr (1992) Stable carbon and nitrogen isotopes in algae and detritus from the Orinoco River floodplain, Venezuela. Geochim. Cosmochim. Acta 56: 4237–4246Google Scholar
  22. Hart DR (1995) Parameter estimation and stochastic interpretation of the transient storage model for solute transport in streams. Water Resources Res. 31: 323–328Google Scholar
  23. Hedges JI &Stern JH (1984) Carbon and nitrogen determination of carbonate-containing solids. Limnol. Oceanogr. 29: 657–663Google Scholar
  24. Hedin LO,Von Fisher JC,Ostrom NE,Kennedy BP,Brown MG &Robertson GP (1998) Thermodynamic constraints on nitrogen transformations and other biogeochemical processes at soil-stream interfaces. Ecology 79: 684–703Google Scholar
  25. Holmes R,McClelland W,Sigman DM,Fry B &Peterson BJ (1998) Measuring 15N-NH+ 4 in marine, estuarine, and fresh waters: an adaptation of the ammonium diffusion method for samples with low ammonium concentrations. Mar. Chem. 60: 235–243Google Scholar
  26. Howarth RW,Billen G,Swaney D,Townsend A,Jaworski N,Lajtha K,Downing J,Elmgren R,Caraco N,Jordan T,Berendse F,Freney J,Kudeyarov V,Murdoch P &Zhao-Liang Z (1996) Regional nitrogen budgets and riverine N & P fluxes for the drainages to the North Atlantic Ocean: natural and human influences. Biogeochemistry 35: 75–139Google Scholar
  27. Kaushik NK,Robinson JB,Stammers WN &Whitely HR (1981) Aspects of nitrogen transport and transformation in headwater streams. In: Lock MA &Williams DD (Eds) Perspectives in Running Water Ecology (pp 113–139). Plenum Press, New YorkGoogle Scholar
  28. King DK (1982) Community metabolism and autotrophic-heterotrophic relationships of woodland stream riffle sections. Doctoral dissertation, Michigan State University (Kellogg Biological Station and Dept. of Fisheries and Wildlife), 356 ppGoogle Scholar
  29. Marzolf ER,Mulholland PJ &Steinman AD (1994) Improvements to the diurnal upstreamdownstream dissolved oxygen change technique for determining whole-stream metabolism in small streams. Can. J. Fish. Aquat. Sci. 51: 1591–1599Google Scholar
  30. Minshall GW,Petersen RC,Cummins KW,Bott TL,Sedell JR,Cushing CE &Vannote RL (1983) Interbiome comparison of stream ecosystem dynamics. Ecol. Monogr. 53: 1–25Google Scholar
  31. Mueller DK &Helsel DR (1996) Nutrients in the Nation' Waters-Too Much of a Good Thing? USGS National Water-Quality Assessment Program Circular 1136Google Scholar
  32. Mulholland PJ,Newbold JD,Elwood JW,Ferren LA &Webster JR (1985) Phosphorus spiraling in a woodland stream: Seasonal variations. Ecology 66: 1012-1023Google Scholar
  33. Mulholland PJ,Steinman AD &Elwood JW (1990) Measurement of phosphorus uptake length in streams: comparison of radiotracer and stable PO4 releases. Can. J. Fish. Aquat. Sci. 47: 2351–2357Google Scholar
  34. Mulholland PJ,Tank JL,Sanzone DM,Wollheim WM,Peterson BJ,Webster JR &Meyer JL (2000) Nitrogen cycling in a forest stream determined by a 15N tracer addition. Ecol. Monogr. 70: 471–493Google Scholar
  35. Newbold JD,Elwood JW,O'Neill RV &Van Winkle W (1981) Measuring nutrient spiraling in streams. Can. J. Fish. Aquat. Sci. 38: 860–863Google Scholar
  36. Newell SY,Arsuffi TL &Fallon RD (1988) Fundamental procedures for determining ergosterol content of decaying plant material by liquid chromatography. Appl. Environ. Microbiol. 54: 1876–1869Google Scholar
  37. Peterson BJ,Wollheim WM,Mulholland PJ,Webster JR,Meyer JL,Tank JL,Martí E,Bowden WB,Valett HM,Hershey AE,McDowell WB,Dodds WK,Hamilton SK,Gregory S &Morrall DD (2001) Control of nitrogen export from watersheds by headwater streams. Science 292: 86–90Google Scholar
  38. Peterson BJ,Bahr M &Kling GW (1997) A tracer investigation of nitrogen cycling in a pristine tundra river. Can. J. Fish. Aquat. Sci. 54: 2361–2367Google Scholar
  39. Raikow DF &Hamilton SK (2001) Bivalve diets in a midwestern US stream: A stable isotope enrichment study. Limnol. Oceanogr. 46: 514–522Google Scholar
  40. Reynolds CS (1984) The Ecology of Freshwater Phytoplankton. Cambridge Univ. Press, CambridgeGoogle Scholar
  41. Riemann B,Simonsen P &Stensgaard L (1989) The carbon and chlorophyll content of phytoplankton from various nutrient regimes. J. Plankton Res. 11: 1037–1045Google Scholar
  42. Sigman DM,Altabet MA,Michener R,McCorkle DC,Fry B &Holmes RM (1997) Natural abundance-level measurement of the nitrogen isotopic composition of oceanic nitrate: an adaptation of the ammonia diffusion method. Mar. Chem. 57: 227–242Google Scholar
  43. Stream Solute Workshop (1990) Concepts and methods for assessing solute dynamics in stream ecosystems. J.N. Am. Benthol. Soc. 9: 95–119Google Scholar
  44. Suberkropp K &Klug MJ (1976) Changes in the chemical composition of leaves during processing in a woodland stream. Ecology 57: 720–727Google Scholar
  45. Suberkropp K &Chauvet E (1995) Regulation of leaf breakdown by fungi in streams: Influences of water chemistry. Ecology 76: 1433–1445Google Scholar
  46. Tank JL,Meyer JL,Sanzone DM,Mulholland PJ,Webster JR,Peterson BJ,Wollheim WM &Leonard NE (2000) Analysis of nitrogen cycling in a forest stream during autumn using a 15N tracer addition. Limnol. Oceanogr. 45: 11013–11029Google Scholar
  47. Tank JL &Webster JR (1998) Interactions of substrate and nutrient availability on wood biofilm processes in streams. Ecology: 79: 151–162Google Scholar
  48. Vitousek PM,Aber JD,Howarth RW,Likens GE,Matson PA,Schindler DW,Schlesinger WH &Tilman DG (1997) Human alteration of the global nitrogen cycle: Sources and consequences. Ecol. Applic. 7: 737–750Google Scholar
  49. Webster JV &Ehrman TP (1996) Solute dynamics. In: Hauer FR &Lamberti GA (Eds) Methods in Stream Ecology (pp 145–160). Academic Press, San DiegoGoogle Scholar
  50. Welshmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol. Oceanogr. 39: 1985–1992Google Scholar
  51. Wetzel RG &Likens GE (1991) Limnological Analyses. Second ed. Springer VerlagGoogle Scholar
  52. Winterbourn MJ (1990) Interactions among nutrients, algae, and invertebrates in a New Zealand mountain stream. Freshw. Biol. 23: 463–474Google Scholar
  53. Young RG &Huryn AD (1998) Comment: Improvements to the diurnal upstream-downstream dissolved oxygen change technique for determining whole-stream metabolism in small streams. Can. J. Fish. Aquat. Sci. 55: 1784–1785Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Stephen K. Hamilton
    • 1
  • Jennifer L. Tank
    • 2
  • David F. Raikow
    • 3
  • Wilfred M. Wollheim
    • 4
  • Bruce J. Peterson
    • 4
  • Jackson R. Webster
    • 5
  1. 1.Kellogg Biological Station and Department of ZoologyMichigan State UniversityHickory CornersUSA (Author for correspondence; e-mail
  2. 2.Department of Biological SciencesUniversity of Notre DameNotre DameUSA
  3. 3.Kellogg Biological Station and Department of ZoologyMichigan State UniversityHickory CornersUSA
  4. 4.Marine Biological LaboratoryEcosystems CenterWoods HoleUSA
  5. 5.Department of BiologyVirginia Polytechnic Institute and State UniversityBlacksburgUSA

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