Skip to main content
SpringerLink
Log in

Spatial and Temporal Variability in the Ecosystem Metabolism of a High-elevation Lake: Integrating Benthic and Pelagic Habitats

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

We characterized spatial and temporal variability in net ecosystem production (NEP), community respiration (CR), and gross primary production (GPP) over an ice-free season in an oligotrophic high-elevation lake using high-frequency measurements of dissolved oxygen. We combined the use of free-water and incubation chamber measurements to compare pelagic and benthic habitats and estimate their relative contributions to whole-lake metabolism. Despite a brief period of predominant heterotrophy after snowmelt, both free-water and incubation chamber measurements confirmed autotrophy of the epilimnion in all habitats throughout the ice-free season. In contrast, benthic incubation chambers showed the benthos to be consistently heterotrophic. Although temperature was the strongest seasonal driver of benthic metabolism, bacterioplankton density and indexes of organic matter quality explained the most variability in pelagic metabolism. Driven largely by benthic metabolism, free-water measurements of GPP and CR were twice as high in littoral than pelagic habitats. However, rates of water column primary production overlying the littoral benthos were high enough to overcome net benthic heterotrophy, and seasonal mean NEP in littoral habitats remained positive and not significantly different from pelagic habitats. Benthic rates averaged about 25% of whole-lake metabolism. Pelagic metabolism measurements were affected by littoral rates about half the time, with the degree of isolation between the two a function of advection and water column stability. These results emphasize the importance of characterizing spatial and temporal variability in metabolism within the context of physical dynamics and challenge the notion that benthic metabolism will necessarily be larger than pelagic metabolism in oligotrophic lakes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  • Aberg J, Jansson M, Karlsson J, Naas KJ, Jonsson A. 2007. Pelagic and benthic net production of dissolved inorganic carbon in an unproductive subarctic lake. Freshw Biol 52:549–60.

    Article  Google Scholar 

  • Admiraal W. 1977. Influence of light and temperature on growth-rate of estuarine benthic diatoms in culture. Mar Biol 39:1–9.

    Article  Google Scholar 

  • Andersen JM, Sand-Jensen K. 1980. Discrepancies between the O2 and 14C methods for measuring phytoplankton gross photosynthesis at low light levels. Oikos 35:359–64.

    Article  CAS  Google Scholar 

  • Andersson E, Brunberg AK. 2006. Net autotrophy in an oligotrophic lake rich in dissolved organic carbon and with high benthic primary production. Aquat Microb Ecol 43:1–10.

    Article  Google Scholar 

  • Ask J, Karlsson J, Persson L, Ask P, Bystrom P, Jansson M. 2009. Whole-lake estimates of carbon flux through algae and bacteria in benthic and pelagic habitats of clear-water lakes. Ecology 90:1923–32.

    Article  PubMed  Google Scholar 

  • Barsdate RJ, Alexander V. 1971. Geochemistry and primary productivity of the Tangle Lake system and Alaskan alpine watershed. Arct Alp Res 3:27–41.

    Article  CAS  Google Scholar 

  • Biddanda B, Ogdahl M, Cotner J. 2001. Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnol Oceanogr 46:730–9.

    Article  Google Scholar 

  • Brainerd KE, Gregg MC. 1995. Surface mixed and mixing layer depths. Deep Sea Res Part I 42:1521–43.

    Article  Google Scholar 

  • Borsheim KY, Andersen S. 1987. Grazing and food size selection by crustacean zooplankton compared to production of bacteria and phytoplankton in a shallow Norwegian mountain lake. J Plankton Res 9:367–79.

    Article  Google Scholar 

  • Carignan R, Blais AM, Vis C. 1998. Measurement of primary production and community respiration in oligotrophic lakes using the Winkler method. Can J Fish Aquat Sci 55:1078–84.

    Article  Google Scholar 

  • Carignan R, D’arcy P, Lamontagne S. 2000. Comparative impacts of fire and forest harvesting on water quality in Boreal Shield lakes. Can J Fish Aquat Sci 57:105–17.

    Article  CAS  Google Scholar 

  • Cole JJ, Caraco NF, Kling GW, Kratz TK. 1994. Carbon dioxide supersaturation in the surface waters of lakes. Science 265:1568–70.

    Google Scholar 

  • Cole JJ, Caraco NF. 1998. Atmospheric exchange of carbon dioxide in a low-wind oligotrophic lake measured by the addition of SF6. Limnol Oceanogr 43:647–56.

    Article  CAS  Google Scholar 

  • Cole JJ, Pace ML, Carpenter SR, Kitchell JF. 2000. Persistence of net heterotrophy in lakes during nutrient addition and food web manipulations. Limnol Oceanogr 45:1718–30.

    Article  Google Scholar 

  • Cotner JB, Biddanda BA. 2002. Small players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5:105–21.

    Article  CAS  Google Scholar 

  • del Giorgio PA, Peters RH. 1993. Balance between phytoplankton production and respiration in lakes. Can J Aquat Sci 50:282–9.

    Article  Google Scholar 

  • del Giorgio PA, Peters RH. 1994. Patterns in planktonic P-R ratios in lakes—influence of lake trophy and dissolved organic-carbon. Limnol Oceanogr 39:772–87.

    Article  CAS  Google Scholar 

  • del Giorgio PA, Cole JJ, Cimbleris A. 1997. Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nature 385:148–51.

    Article  CAS  Google Scholar 

  • del Giorgio PA, Cole JJ. 1998. Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29:503–41.

    Article  Google Scholar 

  • del Giorgio PA, Cole JJ, Caraco NF, Peters RH. 1999. Linking planktonic biomass and metabolism to net gas fluxes in northern temperate lakes. Ecology 80:1422–31.

    Article  Google Scholar 

  • den Heyer C, Kalff J. 1998. Organic matter mineralization rates in sediments: a within- and among-lake study. Limnol Oceanogr 43:695–705.

    Article  Google Scholar 

  • Dodds WK, Cole JJ. 2007. Expanding the concept of trophic state in aquatic ecosystems: it’s not just the autotrophs. Aquat Sci 69:427–39.

    Article  CAS  Google Scholar 

  • Duarte CM, Agusti S. 1998. The CO2 balance of unproductive aquatic ecosystems. Science 281:234–6.

    Article  PubMed  CAS  Google Scholar 

  • Duarte CM, Agusti S, Vaque D. 2004. Controls on planktonic metabolism in the Bay of Blanes, northwestern Mediterranean littoral. Limnol Oceanogr 49:2162–70.

    Article  Google Scholar 

  • Duarte CM, Prairie YT. 2005. Prevalence of heterotrophy and atmospheric CO2 emissions from aquatic ecosystems. Ecosystems 8:862–70.

    Article  CAS  Google Scholar 

  • Ducklow HW, Purdie DA, Williams PJL, Davies JM. 1986. Bacterioplankton: a sink for carbon in a coastal marine plankton community. Science 232:865–7.

    Article  PubMed  CAS  Google Scholar 

  • Forget MH, Carignan R, Hudon C. 2009. Influence of diel cycles of respiration, chlorophyll, and photosynthetic parameters on the summer metabolic balance of temperate lakes and rivers. Can J Fish Aquat Sci 66:1048–58.

    Article  CAS  Google Scholar 

  • Goldman JC, Caron DA, Dennett MR. 1987. Regulation of gross growth efficiency and ammonium regeneration in bacteria by substrate C–N ratio. Limnol Oceanogr 32:1239–52.

    Article  CAS  Google Scholar 

  • Goldman CR, Jassby A, Powell T. 1989. Interannual fluctuations in primary production—meteorological forcing at two subalpine lakes. Limnol Oceanogr 34:310–23.

    Article  CAS  Google Scholar 

  • Hanson PC, Bade DL, Carpenter SR, Kratz TK. 2003. Lake metabolism: relationships with dissolved organic carbon and phosphorus. Limnol Oceanogr 48:1112–19.

    Article  CAS  Google Scholar 

  • Hicks BB. 1975. A procedure for the formulation of bulk transfer coefficients over water. Boundary-layer Meteorol 8:515–24.

    Article  Google Scholar 

  • Huettel M, Gust G. 1992. Solute release mechanisms from confined sediment cores in stirred benthic chambers and flume flows. Marine Ecol Prog Ser 82:187–97.

    Article  Google Scholar 

  • Idso SB. 1973. Concept of lake stability. Limnol Oceanogr 18:681–3.

    Article  Google Scholar 

  • Jahne B, Munnich KO, Bosinger R, Dutzi A, Huber W, Libner P. 1987. On the parameters influencing air-water gas-exchange. J Geophys Res Oceans 92:1937–49.

    Article  Google Scholar 

  • Jansson M, Bergstrom A, Blomqvist P, Drakare S. 2000. Allochthonous organic carbon and phytoplankton/bacterioplankton relationships in lakes. Ecology 8:3250–5.

    Article  Google Scholar 

  • Jassby A, Powell T. 1975. Vertical patterns of eddy diffusion during stratification in Castle Lake, California. Limnol Oceanogr 20:530–43.

    Article  Google Scholar 

  • Kemp WM, Smith EM, Marvindipasquale M, Boynton WR. 1997. Organic carbon balance and net ecosystem metabolism in Chesapeake Bay. Marine Ecol Prog Ser 150:229–48.

    Article  CAS  Google Scholar 

  • Kritzberg ES, Langenheder S, Lindstrom ES. 2006. Influence of dissolved organic matter source on lake bacterioplankton structure and function—implications for seasonal dynamics of community composition. Fems Microbiol Ecol 56:406–17.

    Article  PubMed  CAS  Google Scholar 

  • Lauster GH, Hanson PC, Kratz TK. 2006. Gross primary production and respiration differences among littoral and pelagic habitats in northern Wisconsin lakes. Can J Fish Aquat Sci 63:1130–41.

    Article  Google Scholar 

  • MacIntyre S, Melack JM. 1995. Vertical and horizontal transport in lakes: linking littoral, benthic, and pelagic habitats. J North Am Benthol Soc 14:599–615.

    Article  Google Scholar 

  • MacIntyre S, Romero JR, Kling GW. 2002. Spatial-temporal variability in surface layer deepening and lateral advection in an embayment of Lake Victoria, East Africa. Limnol Oceanogr 47:656–71.

    Article  Google Scholar 

  • MacIntyre S, Fram JP, Kushner PJ, Bettex ND, O’brien WJ, Hobbie JE, Kling GW. 2009. Climate-related variations in mixing dynamics in an Alaskan arctic lake. Limnol Oceanogr 54:2401–17.

    Article  Google Scholar 

  • MacIntyre S, Jonsson AJ, Jansson M, Aberg J, Turney D, Miller S. 2010. Buoyancy flux, turbulence, and the gas transfer coefficient in a stratified lake. Geophys Res Lett 37:L24604-1–L24604-5.

    Google Scholar 

  • Mcknight DM, Boyer EW, Westerhoff PK, Doran PT, Kulbe T, Andersen DT. 2001. Spectrofluorometric characterization of dissolved organic matter for indication of precursor organic material and aromaticity. Limnol Oceanogr 46:38–48.

    Article  CAS  Google Scholar 

  • Melack JM. 1982. Photosynthetic activity and respiration in an equatorial African soda lake. Freshw Biol 12:381–99.

    Article  Google Scholar 

  • Melack JM, Cooper SD, Holmes RW. 1987. Chemical and biological survey of lakes and streams located in the Emerald Lake watershed, Sequoia National Park. Santa Barbara: California Air Resources Board and University of California. p 345.

    Google Scholar 

  • Melack JM, Cooper SD, Jenkins TM. 1989. Chemical and biological characteristics of Emerald Lake and the streams in its watershed, and the responses of the lake and streams to acidic deposition. Santa Barbara: California Air Resources Board and University of California. p 377.

    Google Scholar 

  • Melack JM, Stoddard JL. 1991. Sierra Nevada. In: Charles DF, Ed. Acidic deposition and aquatic ecosystems: regional case studies. Berlin: Springer-Verlag. p 503–30.

    Google Scholar 

  • Millero FJ, Poisson A. 1981. International one-atmosphere equation of state of seawater. Deep Sea Res Part A 28:625–9.

    Article  Google Scholar 

  • Monismith SG, Imberger J, Morison ML. 1990. Convective motions in the sidearm of a small reservoir. Limnol Oceanogr 35:1676–702.

    Article  Google Scholar 

  • Nelson CE. 2008. The phenology, biogeography, and metabolism of bacteria in high-elevation lakes of the Sierra Nevada, California. Ph.D. thesis, University of California, Santa Barbara.

  • Nelson CE. 2009. Phenology of high-elevation pelagic bacteria: the roles of meteorologic variability, catchment inputs and thermal stratification in structuring communities. ISME J 3:13–30.

    Article  PubMed  CAS  Google Scholar 

  • Nelson CE, Sadro S, Melack JM. 2009. Contrasting the influences of stream inputs and landscape position on bacterioplankton community structure and dissolved organic matter composition in high-elevation lake chains. Limnol Oceanogr 54:1292–305.

    Article  CAS  Google Scholar 

  • Odum HT. 1956. Primary production in flowing waters. Limnol Oceanogr 1:102–17.

    Article  Google Scholar 

  • Perez MT, Sommaruga R. 2006. Differential effect of algal- and soil derived dissolved organic matter on alpine lake bacterial community composition and activity. Limnol Oceanogr 51:2527–37.

    Article  CAS  Google Scholar 

  • Pomeroy LR. 1974. The ocean’s food web, a changing paradigm. Bioscience 24:499–504.

    Article  Google Scholar 

  • Prairie YT, Bird DF, Cole JJ. 2002. The summer metabolic balance in the epilimnion of southeastern Quebec lakes. Limnol Oceanogr 47:316–21.

    Article  CAS  Google Scholar 

  • Sadro S, Nelson CE, Melack JM. 2011. Linking diel patterns in community respiration to bacterioplankton in an oligotrophic high-elevation lake. Limnol Oceanogr 56:540–50.

    Article  CAS  Google Scholar 

  • Sadro S, Melack JM, MacIntyre S. 2011. Depth-integrated estimates of ecosystem metabolism in a high-elevation lake (Emerald Lake, Sierra Nevada, California). Limnol Oceanogr.

  • Sand-Jensen K, Borum J. 1991. Interactions among phytoplankton, periphyton, and macrophytes in temperate fresh-waters and estuaries. Aquat Bot 41:137–75.

    Article  Google Scholar 

  • Shay TJ, Gregg MC. 1986. Convectively driven turbulent mixing in the upper ocean. J Phys Oceanogr 16:1777–98.

    Article  Google Scholar 

  • Sickman JO, Melack JM. 1992. Photosynthetic activity of phytoplankton in a high-altitude lake (Emerald Lake, Sierra-Nevada, California). Hydrobiologia 230:37–48.

    Article  CAS  Google Scholar 

  • Sickman JO, Melack JM, Clow DW. 2003. Evidence for nutrient enrichment of high-elevation lakes in the Sierra Nevada, California. Limnol Oceanogr 48:1885–92.

    Article  CAS  Google Scholar 

  • Simon M, Cho BC, Azam F. 1992. Significance of bacterial biomass in lakes and the ocean—comparison to phytoplankton biomass and biogeochemical implications. Marine Ecol Prog Ser 86:103–10.

    Article  Google Scholar 

  • Smith SD. 1988. Coefficients for sea surface wind stress, heat flux, and wind profiles as a function of wind speed and temperature. J Geophys Res 93:15467–72.

    Article  Google Scholar 

  • Staehr PA, Sand-Jensen K. 2007. Temporal dynamics and regulation of lake metabolism. Limnol Oceanogr 52:108–20.

    Article  CAS  Google Scholar 

  • Staehr PA, Bade D, Van de Bogert MC, Koch GR, Williamson C, Hanson P, Cole JJ, Kratz T. 2010. Lake metabolism and the diel oxygen technique: state of the science. Limnol Oceanogr Methods 8:628–44.

    Article  CAS  Google Scholar 

  • Staehr PA, Testa JM, Kemp WM, Cole JJ, Sand-Jensen K, Smith SV. 2011. The metabolism of aquatic ecosystems: history, applications, and future challenges. Aquat Sci. DOI:10.1007/s00027-011-0199-2.

  • Vadeboncoeur Y, Steinman AD. 2002. Periphyton function in lake ecosystems. Sci World J 2:1–20.

    Google Scholar 

  • Vadeboncoeur Y, Jeppesen E, Vander Zanden MJ, Schierup H, Christoffersen K, Lodge DM. 2003. From Greenland to green lakes: cultural eutrophication and the loss of benthic pathways in lakes. Limnol Oceanogr 48:1408–18.

    Article  Google Scholar 

  • Vadeboncoeur Y, Peterson G, Vander Zanden MJ, Kalff J. 2008. Benthic algal production across lake size gradients: interactions among morphometry, nutrients, and light. Ecology 89:2542–52.

    Article  PubMed  Google Scholar 

  • Van De Bogert MC, Carpenter SR, Cole JJ, Pace ML. 2007. Assessing pelagic and benthic metabolism using free water measurements. Limnol Oceanogr Methods 5:145–55.

    Article  Google Scholar 

  • Vander Zanden MJ, Chandra S, Park SK, Vadeboncoeur Y, Goldman CR. 2006. Efficiencies of benthic and pelagic trophic pathways in a subalpine lake. Can J Fish Aquat Sci 63:2608–20.

    Article  Google Scholar 

Download references

Acknowledgments

We thank Kevin Skeen for field assistance. Sequoia-Kings Canyon National Park provided administrative support of for this research. Financial support was provided by the National Science Foundation (NSF) through the Graduate Research Fellowship Program (to SS) and through Division of Environmental Biology awards 0614207 (to JMM) and 0640953 (to SM). The comments of Craig Nelson, Michael Pace, and two anonymous reviewers helped improve this manuscript.

Author information

Authors and Affiliations

  1. Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, California, 93106-9610, USA

    Steven Sadro, John M. Melack & Sally MacIntyre

Authors
  1. Steven Sadro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John M. Melack
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sally MacIntyre
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Steven Sadro.

Additional information

Author Contributions

Sadro conceived the study, performed the research, analyzed the data, contributed models used in the analysis, and wrote the MS; Melack contributed to the study design, contributed to the methods, and edited the MS; MacIntyre contributed models used in the analysis and edited the MS.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sadro, S., Melack, J.M. & MacIntyre, S. Spatial and Temporal Variability in the Ecosystem Metabolism of a High-elevation Lake: Integrating Benthic and Pelagic Habitats. Ecosystems 14, 1123–1140 (2011). https://doi.org/10.1007/s10021-011-9471-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-011-9471-5

Key words

Search

Navigation