, Volume 10, Issue 4, pp 588–606 | Cite as

Multiple Scales of Temporal Variability in Ecosystem Metabolism Rates: Results from 2 Years of Continuous Monitoring in a Forested Headwater Stream

  • Brian J. Roberts
  • Patrick J. Mulholland
  • Walter R. Hill


Headwater streams are key sites of nutrient and organic matter processing and retention, but little is known about temporal variability in gross primary production (GPP) and ecosystem respiration (ER) rates as a result of the short duration of most metabolism measurements in lotic ecosystems. We examined temporal variability and controls on ecosystem metabolism by measuring daily rates continuously for 2 years in Walker Branch, a first-order deciduous forest stream. Four important scales of temporal variability in ecosystem metabolism rates were identified: (1) seasonal, (2) day-to-day, (3) episodic (storm-related), and (4) inter-annual. Seasonal patterns were largely controlled by the leaf phenology and productivity of the deciduous riparian forest. Walker Branch was strongly net heterotrophic throughout the year with the exception of the open-canopy spring when GPP and ER rates were co-equal. Day-to-day variability in weather conditions influenced light reaching the streambed, resulting in high day-to-day variability in GPP particularly during spring (daily light levels explained 84% of the variance in daily GPP in April). Episodic storms depressed GPP for several days in spring, but increased GPP in autumn by removing leaves shading the streambed. Storms depressed ER initially, but then stimulated ER to 2–3 times pre-storm levels for several days. Walker Branch was strongly net heterotrophic in both years of the study, with annual GPP being similar (488 and 519 g O2 m−2 y−1 or 183 and 195 g C m−2 y−1) but annual ER being higher in 2004 than 2005 (−1,645 vs. −1,292 g O2 m−2 y−1 or −617 and −485 g C m−2 y−1). Inter-annual variability in ecosystem metabolism (assessed by comparing 2004 and 2005 rates with previous measurements) was the result of the storm frequency and timing and the size of the spring macroalgal bloom. Changes in local climate can have substantial impacts on stream ecosystem metabolism rates and ultimately influence the carbon source and sink properties of these important ecosystems.


primary production ecosystem respiration seasonal patterns inter-annual variability storms disturbance light periphyton bryophytes macroalgae Oedogonium leaf litter reaeration 



We thank Ramie Wilkerson (ORNL) for water chemistry analyses, Tilden Myers (NOAA) for barometric pressure data, and Paul Hanson (ORNL) for above forest canopy PAR data. PAR data above the forest canopy were obtained from the Walker Branch Throughfall Displacement Experiment (TDE) Data Archive ( funded by the Program for Ecosystem Research, Environmental Sciences Division, Office of Biological and Environmental Research, U.S. Department of Energy. Comments of Jon Cole and two anonymous reviewers greatly improved an earlier version of this manuscript. This project was supported by the U.S. Department of Energy’s Program for Ecosystem Research, in the Office of Science, Office of Biological and Environmental Research and by the Campus Research Board of the University of Illinois at Urbana-Champaign. Oak Ridge National Laboratory is managed by the University of Tennessee-Battelle LLC for the U.S. Department of Energy under contract DE-AC05-00OR22725.


  1. Alexander RB, Smith RA, Schwartz GE. 2000. Effect of stream channel size on the delivery of nitrogen to the Gulf of Mexico. Nature 403:758–61PubMedCrossRefGoogle Scholar
  2. APHA (American Public Health Association). 1992. Standard methods for the examination of water and wastewater, 18th edn. American Public Health Association, WashingtonGoogle Scholar
  3. Baldocchi DD, Falge E, Gu L, Olson R, Hollinger D, Running S, Anthoni P, Bernhofer C, Davis K, Evans R, Fuentes J, Goldstein A, Katul G, Law B, Lee XH, Malhi Y, Meyers T, Munger W, Oechel W, U KTP, Pilegaard K, Schmid HP, Valentini R, Verma S, Vesala T, Wilson K, Wofsy S. 2001. FLUXNET: a new tool to study the temporal and spatial variability of ecosystem-scale carbon dioxide, water vapor, and energy flux densities. Bull Am Meteorol Soc 82:2415–34Google Scholar
  4. Bott TL. 1996. Primary productivity and community respiration. In: Hauer FR, Lamberti GA (eds). Methods in stream ecology. San Diego: Academic. pp 533–56Google Scholar
  5. Bott TL, Brock JT, Dunn CS, Naiman RJ, Ovink RW, Peterson RC. 1985. Benthic community metabolism in four temperate stream systems: an inter-biome comparison and evaluation of the river continuum concept. Hydrobiologia 123:3–45CrossRefGoogle Scholar
  6. Bott TL, Newbold JD, Arscott DB. 2006. Ecosystem metabolism in piedmont streams: reach geomorphology modulates the influence of riparian vegetation. Ecosystems 9:398–421CrossRefGoogle Scholar
  7. Cole JJ, Pace ML, Carpenter SR, Kitchell JF. 2000. Persistence of net heterotrophy in lakes during nutrient addition and food web manipulation. Limnol Oceanogr 45:1718–30CrossRefGoogle Scholar
  8. Cole JJ, Carpenter SR, Kitchell JF, Pace ML. 2002. Pathways of organic C utilization in small lakes: results from a whole-lake 13C addition and coupled model. Limnol Oceanogr 47:1664–75CrossRefGoogle Scholar
  9. Cole JJ, Carpenter SR, Pace ML, Van de Bogert MC, Kitchell JF, Hodgson JR. 2006. Differential support of lake food webs by three types of terrestrial organic carbon. Ecol Lett 9:558–68PubMedCrossRefGoogle Scholar
  10. Duffer WR, Dorris TC. 1966. Primary productivity in a southern great plains stream. Limnol Oceanogr 11:143–51Google Scholar
  11. Elwood JW, Newbold JD, Trimble AF, Stark RW. 1981. The limiting role of phosphorus in a woodland stream ecosystem: effects of P enrichment on leaf decomposition and primary producers. Ecology 62:146–58CrossRefGoogle Scholar
  12. Fellows CS, Valett HM, Dahm CN. 2001. Whole-stream metabolism in two montane streams: contribution of the hyporheic zone. Limnol Oceanogr 46:523–31CrossRefGoogle Scholar
  13. Fisher SG, Gray LJ, Grimm NB, Busch DE. 1982. Temporal succession in a desert stream ecosystem following flash flooding. Ecol Monogr 52:93–110CrossRefGoogle Scholar
  14. Flecker AS, Taylor BW, Bernhardt ES, Hood JM, Cornwell WK, Cassatt SR, Vanni MJ, Altman NS. 2002. Interactions between herbivorous fishes and limiting nutrients in a tropical stream ecosystem. Ecology 83:1831–44Google Scholar
  15. Genereux DP, Hemond HF. 1992. Determination of gas exchange rate constants for a small stream on Walker Branch Watershed, Tennessee. Water Resources Res 28:2365–74CrossRefGoogle Scholar
  16. Grattan RM, Suberkropp K. 2001. Effects of nutrient enrichment on yellow poplar leaf decomposition and fungal activity in streams. J North Am Benthol Soc 20:33–43CrossRefGoogle Scholar
  17. Grimm NB, Fisher SG. 1986. Nitrogen limitation in a Sonoran Desert stream. J North Am Benthol Soc 5:2–15CrossRefGoogle Scholar
  18. Grimm NB, Fisher SG. 1989. Stability of periphyton and macroinvertebrates to disturbance by flash floods in a desert stream. J North Am Benthol Soc 8:293–307CrossRefGoogle Scholar
  19. Hall RO, Tank JL. 2003. Ecosystem metabolism controls nitrogen uptake in streams in Grand Teton National Park, Wyoming. Limnol Oceanogr 48:1120–28CrossRefGoogle Scholar
  20. Hall RO, Tank JL. 2005. Correcting whole-stream estimates of metabolism for groundwater inputs. Limnol Oceanogr Methods 3:222–29Google Scholar
  21. Hill WR, Dimick SM. 2002. Effects of riparian leaf dynamics on periphyton photosynthesis and light utilization efficiency. Freshw Biol 47:1245–56CrossRefGoogle Scholar
  22. Hill WR, Knight AW. 1988. Nutrient and light limitation of algae in two northern California streams. J Phycol 24:125–32Google Scholar
  23. Hill WR, Boston HL, Steinman AD. 1992. Grazers and nutrients simultaneously limit lotic primary productivity. Can J Fish Aquat Sci 49:504–12Google Scholar
  24. Hill WR, Ryon MG, Schilling EM. 1995. Light limitation in a stream ecosystem: responses by primary producers and consumers. Ecology 76:1297–309CrossRefGoogle Scholar
  25. Hill WR, Mulholland PJ, Marzolf ER. 2001. Stream ecosystem responses to forest leaf emergence in spring. Ecology 82:2306–19CrossRefGoogle Scholar
  26. Hornberger GM, Kelly MG, Eller RM. 1976. Relationship between light and photosynthetic rates in a river community and implications for water quality modeling. Water Resources Res 12:723–30CrossRefGoogle Scholar
  27. Houser JN, Mulholland PJ, Maloney KO. 2005. Catchment disturbance and stream metabolism: patterns in ecosystem respiration and gross primary production along a gradient of upland soil and vegetation disturbance. J North Am Benthol Soc 24:538–52Google Scholar
  28. Johnson DW, Van Hook RI. 1989. Analysis of biogeochemical cycling processes in Walker Branch watershed. New York: Springer-Verlag. pp 401Google Scholar
  29. Marzolf ER, Mulholland PJ, Steinman AD. 1994. Improvements to the diurnal upstream-downstream dissolved oxygen change technique for determining whole-stream metabolism in small streams. Can J Fish Aquat Sci 51:1591–99CrossRefGoogle Scholar
  30. Marzolf ER, Mulholland PJ, Steinman AD. 1998. Reply: improvements to the diurnal upstream–downstream dissolved oxygen change technique for determining whole-stream metabolism in small streams. Can J Fish Aquat Sci 55:1786–7CrossRefGoogle Scholar
  31. McMaster WC. 1963. Geologic map of the Oak Ridge Reservation, Tennessee. ORNL/TM-713. Oak Ridge: Oak Ridge National LaboratoryGoogle Scholar
  32. Mulholland PJ. 1992. Regulation of nutrient concentrations in a temperate forest stream: roles of upland, riparian, and in-stream processes. Limnol Oceanogr 37:1512–26CrossRefGoogle Scholar
  33. Mulholland PJ. 2004. The importance of in-stream uptake for regulating stream concentrations and outputs of N and P from a forested watershed: evidence from long-term chemistry records for Walker Branch Watershed. Biogeochemistry 70:403–26CrossRefGoogle Scholar
  34. Mulholland PJ, Hill WR. 1997. Seasonal patterns in streamwater nutrient and dissolved organic carbon concentrations: Separating catchment flow path and in-stream effects. Water Resources Res 33:1297–306CrossRefGoogle Scholar
  35. Mulholland PJ, Rosemond AD. 1992. Periphyton response to longitudinal nutrient depletion in a woodland stream: evidence of upstream–downstream linkage. J North Am Benthol Soc 11:409–19CrossRefGoogle Scholar
  36. Mulholland PJ, Marzolf ER, Webster JR, Hart DR, Hendricks SP. 1997a. Evidence that hyporheic zones increase heterotrophic metabolism and phosphorus uptake in forest streams. Limnol Oceanogr 42:443–51Google Scholar
  37. Mulholland PJ, Best GR, Coutant CC, Hornberger GM, Meyer JL, Robinson PJ, Stenberg JR, Turner RE, Vera-Herrera F, Wetzel RG. 1997b Effects of climate change on freshwater ecosystems of the south-eastern United States and the Gulf Coast of Mexico. Hydrol Process 11:949–70Google Scholar
  38. Mulholland PJ, Wilson GV, Jardine PM. 1990. Hydrogeochemical response of a forested watershed to storms: effects of preferential flow along shallow and deep pathways. Water Resources Res 26:3021–36CrossRefGoogle Scholar
  39. 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 70:471–93Google Scholar
  40. Mulholland PJ, Fellows CS, Tank JL, Grimm NB, Webster JR, Hamilton SK, Martí E, Ashkenas L, Bowden WB, Dodds WK, McDowell WH, Paul MJ, Peterson BJ. 2001. Inter-biome comparison of factors controlling stream metabolism. Freshw Biol 46:1503–17CrossRefGoogle Scholar
  41. Mulholland PJ, Thomas SA, Valett HM, Webster JR, Beaulieu J. 2006. Effects of light on nitrate uptake in small forested streams: diurnal and day-to-day variations. J North Am Benthol Soc 25:583–95CrossRefGoogle Scholar
  42. Newbold JD, Elwood JW, O’Neill RV, Sheldon AL. 1983. Phosphorus dynamics in a woodland stream ecosystem: a study of nutrient spiralling. Ecology 64:1249–65CrossRefGoogle Scholar
  43. Odum HT. 1956. Primary production in flowing waters. Limnol Oceanogr 2:102–17Google Scholar
  44. Ortiz-Zayas JR, Lewis WM, Saunders JF, McCutchan JH, Scatena FN. 2005. Metabolism of a tropical rainforest stream. J North Am Benthol Soc 24:769–83CrossRefGoogle Scholar
  45. Petersen RC, Cummins KW. 1974. Leaf processing in a woodland stream. Freshw Biol 4:343–68CrossRefGoogle Scholar
  46. Peterson BJ, Hobbie JE, Hershey AE, Lock MA, Ford TE, Vestal JR, McKinley JL, Hullar MAJ, Miller MC, Ventullo RM, Volk G (1985) Transformation of a tundra river from heterotrophy to autotrophy by additions of phosphorus. Science 229:1383–1386PubMedCrossRefGoogle Scholar
  47. Peterson BJ, Wollheim WM, Mulholland PJ, Webster JR, Meyer JL, Tank JL, Martí E, Bowden WB, Valett HM, Hershey AE, McDowell WH, Dodds WK, Hamilton SK, Gregory S, Morrall DD. 2001. Control of nitrogen export from watersheds by headwater streams. Science 292:86–90PubMedCrossRefGoogle Scholar
  48. Poff NL. 1996. A hydrogeography of unregulated streams in the United States and an examination of scale-dependence in some hydrological descriptors. Freshw Biol 36:71–91CrossRefGoogle Scholar
  49. Poff NL, Ward JV. 1989. Implications of streamflow variability and predictability for lotic community structure: a regional analysis of streamflow patterns. Can J Fish Aquat Sci 46:1805–18Google Scholar
  50. Rathbun RE, Stephens DW, Schultz DJ, Tai DY. 1978. Laboratory studies of gas tracers for reaeration. J Environ Eng Divis Am Soc Civil Eng 104:215–29Google Scholar
  51. Rosemond AD. 1994. Multiple factors limit seasonal variation in periphyton in a forest stream. J North Am Benthol Soc 13:333–44CrossRefGoogle Scholar
  52. Rosemond AD, Mulholland PJ, Elwood JW. 1993. Top-down and bottom-up control of stream periphyton: effects of nutrients and herbivores. Ecology 74:1264–80CrossRefGoogle Scholar
  53. 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 57:66–75CrossRefGoogle Scholar
  54. Running SW, Baldochhi DD, Turner DP, Gower ST, Bakwin PS, Hibbard KA. 1999. A global terrestrial monitoring network integrating tower fluxes, flask sampling, ecosystem modeling and EOS satellite data. Remote Sensing Environ 70:108–27CrossRefGoogle Scholar
  55. Sartory DP, Grobbelaar JJ. 1984. Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis. Hydrobiologia 114:177–87Google Scholar
  56. Sinsabaugh RL. 1997. Large-scale trends for stream benthic respiration. J North Am Benthol Soc 16:119–22CrossRefGoogle Scholar
  57. Steinman AD. 1992. Does an increase in irradiance influence periphyton in a heavily-grazed woodland stream? Oecologia 91:163–70CrossRefGoogle Scholar
  58. Steinman AD, Boston HL. 1993. The ecological role of aquatic bryophytes in a woodland stream. J North Am Benthol Soc 12:17–26CrossRefGoogle Scholar
  59. Steinman AD, Mulholland PJ, Hill WR. 1992. Functional responses associated with growth form in stream algae. J North Am Benthol Soc 11:229–43CrossRefGoogle Scholar
  60. Tank JL, Webster JR. 1998. Interaction of substrate and nutrient availability on wood biofilm processes in streams. Ecology 79:2168–2179Google Scholar
  61. Uehlinger U. 1991. Spatial and temporal variability of periphyton biomass in a prealpine river (Necker, Switzerland). Archiv für Hydrobiol 123:219–37Google Scholar
  62. Uehlinger U. 2000. Resistance and resilience of ecosystem metabolism in a flood-prone river system. Freshw Biol 45:319–332CrossRefGoogle Scholar
  63. Uehlinger U. 2006. Annual cycle and inter-annual variability of gross primary production and ecosystem respiration in a floodprone river during a 15-year period. Freshw Biol 51:938–50CrossRefGoogle Scholar
  64. Uehlinger U, Naegeli MW. 1998. Ecosystem metabolism, disturbance, and stability in a prealpine gravel bed river. J North Am Benthol Soc 17:165–78CrossRefGoogle Scholar
  65. Uehlinger U, König C, Reichert P. 2000. Variability of photosynthesis-irradiance curves and ecosystem respiration in a small river. Freshw Biol 44:493–507CrossRefGoogle Scholar
  66. Webster JR, Benfield EF. 1986. Vascular plant breakdown in freshwater ecosystems. Annu Rev Ecol Syst 17:567–94CrossRefGoogle Scholar
  67. Wofsy SC, Goulden ML, Munger JW, Fan S-M, Bakwin PS, Daube BC, Bassow SL, Bazzaz FA. 1993. Net exchange of CO2 in a mid-latitude forest. Science 260:1314–17PubMedCrossRefGoogle Scholar
  68. Young RG, Huryn AD. 1996. Interannual variation in discharge controls ecosystem metabolism along a grassland river continuum. Can J Fish Aquat Sci 53:2199–211CrossRefGoogle Scholar
  69. 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 55:1784–5CrossRefGoogle Scholar
  70. Young RG, Huryn AD. 1999. Effects of land use on stream metabolism and organic matter turnover. Ecol Appl 9:1359–76CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Brian J. Roberts
    • 1
  • Patrick J. Mulholland
    • 1
  • Walter R. Hill
    • 2
  1. 1.Environmental Sciences DivisionOak Ridge National LaboratoryOak RidgeUSA
  2. 2.Division of Ecology and Conservation ScienceIllinois Natural History SurveyChampaignUSA

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