Aquatic Sciences

, Volume 74, Issue 1, pp 15–29 | Cite as

The metabolism of aquatic ecosystems: history, applications, and future challenges

  • Peter A. Staehr
  • Jeremy M. Testa
  • W. Michael Kemp
  • Jon J. Cole
  • Kaj Sand-Jensen
  • Stephen V. Smith
Overview

Abstract

Measurements of the production and consumption of organic material have been a focus of aquatic science for more than 80 years. Over the last century, a variety of approaches have been developed and employed for measuring rates of gross primary production (Pg), respiration (R), and net ecosystem production (Pn = Pg − R) within aquatic ecosystems. Here, we reconsider the range of approaches and applications for ecosystem metabolism measurements, and suggest ways by which such studies can continue to contribute to aquatic ecology. This paper reviews past and contemporary studies of aquatic ecosystem-level metabolism to identify their role in understanding and managing aquatic systems. We identify four broad research objectives that have motivated ecosystem metabolism studies: (1) quantifying magnitude and variability of metabolic rates for cross-system comparison, (2) estimating organic matter transfer between adjacent systems or subsystems, (3) measuring ecosystem-scale responses to perturbation, both natural and anthropogenic, and (4) quantifying and calibrating models of biogeochemical processes and trophic networks. The magnitudes of whole-system gross primary production, respiration and net ecosystem production rates vary among aquatic environments and are partly constrained by the chosen methodology. We argue that measurements of ecosystem metabolism should be a vital component of routine monitoring at larger scales in the aquatic environment using existing flexible, precise, and durable sensor technologies. Current and future aquatic ecosystem studies will benefit from application of new methods for metabolism measurements, which facilitate integration of process measurements and calibration of models for addressing fundamental questions involving ecosystem-scale processes.

Keywords

Aquatic ecosystems Metabolism Methods History Applications Future 

Notes

Acknowledgments

This paper was supported by (1-for P.A. Staehr) the Danish Natural Research Council, STENO grant no 272-05-0277, a Copenhagen faculty research grant no 10-08716, and the Danish Centre for lake restoration (CLEAR); (2-for J.M. Testa and W.M. Kemp) the United States National Oceanographic and Atmospheric Administration (NOAA) Coastal Hypoxia Research Program (CHRP; CHRP-NAO7NOS4780191), the United States National Science Foundation Chesapeake Bay Environmental Observatory (CBEO; CBEO-3 BERS-0618986), and by the State of Maryland Department of Natural Resources (K00B920002). We are thankful to Nathaniel E. Ostrom for comments on the methods section. This is contribution #4497 from the University of Maryland Center for Environmental Science.

Supplementary material

27_2011_199_MOESM1_ESM.doc (103 kb)
Supplementary material 1 (DOC 103 kb)

References

  1. 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 49:960–971Google Scholar
  2. Algesten G, Sobek S, Bergstrom AK, Agren A, Tranvik LJ, Jansson M (2004) Role of lakes for organic carbon cycling in the boreal zone. Glob Change Biol 10:141–147Google Scholar
  3. Allen AP, Gillooly JF, Brown JH (2005) Linking the global carbon cycle to individual metabolism. Funct Ecol 19:202–213Google Scholar
  4. Aoki T, Hayami Y, Fujiwara T, Mukai H, Tanaka Y (1996) Nutrient dynamics in the north basin of Lake Biwa.1. Changes in the vertical distribution of nutrients due to an internal surge induced by a strong typhoon. J Great Lakes Res 22:331–340Google Scholar
  5. Aristegi L, Izagirre O, Elosegi A (2009) Comparison of several methods to calculate reaeration in streams, and their effects on estimation of metabolism. Hydrobiologia 635:113–124Google Scholar
  6. Arnell NW (1999) The effect of climate change on hydrological regimes in Europe: a continental perspective. Glob Environ Change 9:5–23Google Scholar
  7. 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 90:1923–1932PubMedGoogle Scholar
  8. Barko JW, Murphy PG, Wetzel RL (1977) An investigation of primary production and ecosystem metabolism in a lake Michigan dune pond. Archiev für Hydrobiologie 2:155–187Google Scholar
  9. Barnes DJ (1983) Profiling coral reef productivity and calcification using pH and oxygen electrodes. J Exp Mar Biol Ecol 66:149–161Google Scholar
  10. Barth JA, Menge BA, Lubchenco J, Chan F, Bane JM, Kirincich AR, McManus MA, Nielsen KJ, Pierce SD, Washburn L (2007) Delayed upwelling alters nearshore coastal ocean ecosystems in the northern California current. Proc Natl Acad Sci USA 104:3719–3724PubMedGoogle Scholar
  11. Bates NR, Mathis JT (2009) The Arctic Ocean marine carbon cycle: evaluation of air-sea CO2 exchanges, ocean acidification impacts and potential feedbacks. Biogeosciences 6:2433–2459Google Scholar
  12. Bender M, Grande K, Johnson K, Marra J, Williams PJB, Sieburth J, Pilson M, Langdon C, Hitchcock G, Orchardo J, Hunt C, Donaghay P (1987) A comparison of four methods for determining planktonic community production. Limnol Oceanogr 32:1085–1098Google Scholar
  13. Bender ML, Dickson M-L, Orchardo J (2000) Net and gross production in the Ross Sea as determined by incubation experiments and dissolved O2 studies. Deep-Sea Res II 47:3141–3158Google Scholar
  14. Benoy G, Cash K, McCauley E, Wrona F (2007) Carbon dynamics in lakes of the boreal forest under a changing climate. Environ Rev 15:175–189Google Scholar
  15. Beyers RJ, Odum HT (1959) The use of carbon dioxide to construct pH curves for the measurement of productivity. Limnol Oceanogr 4:499–502Google Scholar
  16. Blenckner T (2005) A conceptual model of climate-related effects on lake ecosystems. Hydrobiologia 533:1–14Google Scholar
  17. Borges AV, Delille B, Schiettecatte LS, Gazeau F, Abril G, Frankignoulle M (2004) Gas transfer velocities of CO2 in three European estuaries (Randers Fjord, Scheldt, and Thames). Limnol Oceanogr 49:1630–1641Google Scholar
  18. Borges AV, Delille B, Frankignoulle M (2005) Budgeting sinks and sources of CO2 in the coastal ocean: diversity of ecosystems counts. Geophys Res Lett 32:L14601. doi: 10.1029/2005GL023053
  19. Borum J, Sand-Jensen K (1996) Is total primary production in shallow coastal marine waters stimulated by nitrogen loading? Oikos 76:406–410Google Scholar
  20. Bozec Y, Thomas H, Schiettecatte LS, Borges AV, Elkalay K, de Baar HJW (2006) Assessment of the processes controlling the seasonal variations of dissolved inorganic carbon in the North Sea. Limnol Oceanogr 51:2746–2762Google Scholar
  21. Breed GA, Jackson GA, Richardson TL (2004) Sedimentation, carbon export and food web structure in the Mississippi River plume described by inverse analysis. Mar Ecol Progr Ser 278:35–51Google Scholar
  22. Broecker WS, Takahashi T, Simpson HJ, Peng TH (1979) Fate of fossil-fuel carbon-dioxide and the global carbon budget. Science 206:409–418PubMedGoogle Scholar
  23. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789Google Scholar
  24. Caffrey JM (2003) Production respiration and net ecosystem metabolism in U.S. estuaries. Environ Monit Assess 81:207–219PubMedGoogle Scholar
  25. Caffrey JM (2004) Factors controlling net ecosystem metabolism in U.S. estuaries. Estuaries 27:90–101Google Scholar
  26. Caffrey JM, Cloern JE, Grenz C (1998) Changes in production and respiration during a spring phytoplankton bloom in San Francisco Bay, California, USA: implications for net ecosystem metabolism. Mar Ecol Progr Ser 172:1–12Google Scholar
  27. Caraco NF, Cole JJ (2004) When terrestrial material is sent down the river: the importance of allochthonous carbon inputs to the metabolism of lakes and rivers. In: Polis GA, Power ME, Huxel GR (eds) Food webs at the landscape level. University of Chicago Press, Chicago, pp 301–316Google Scholar
  28. Chapin FS, Woodwell GM, Randerson JT, Rastetter EB, Lovett GM, Baldocchi DD, Clark DA, Harmon ME, Schimel DS, Valentini R, Wirth C, Aber JD, Cole JJ, Goulden ML, Harden JW, Heimann M, Howarth RW, Matson PA, McGuire AD, Melillo JM, Mooney HA, Neff JC, Houghton RA, Pace ML, Ryan MG, Running SW, Sala OE, Schlesinger WH, Schulze ED (2006) Reconciling carbon-cycle concepts, terminology, and methods. Ecosystems 9:1041–1050Google Scholar
  29. Chen CTA, Borges AV (2009) Reconciling opposing views on carbon cycling in the coastal ocean: Continental shelves as sinks and near-shore ecosystems as sources of atmospheric CO2. Deep-Sea Res Part II Topical Stud Oceanogr 56:578–590Google Scholar
  30. Christensen V, Walters CJ (2004) Ecopath with Ecosim: methods, capabilities and limitations. Ecol Modell 172:109–139Google Scholar
  31. Cole JJ, Fisher SG (1978) Annual metabolism of a temporary pond ecosystem. Am Midl Nat 100:15–22Google Scholar
  32. Cole JJ, Caraco NF, Kling GW, Kratz TK (1994) Carbon-dioxide supersaturation in the surface waters of lakes. Science 265:1568–1570PubMedGoogle Scholar
  33. Cole JJ, Pace ML, Carpenter SR, Kitchell JF (2000) Persistence of net heterotrophy in lakes during nutrient addition and food web manipulations. Limnol Oceanogr 45:1718–1730Google Scholar
  34. Cole JJ, Carpenter SR, Pace ML, Van de Bogert MC, Kitchell JL, Hodgson JR (2006) Differential support of lake food webs by three types of terrestrial organic carbon. Ecol Lett 9:558–568PubMedGoogle Scholar
  35. Cole JJ, Prairie YT, Caraco NF, McDowell WH, Tranvik LJ, Striegl RG, Duarte CM, Kortelainen P, Downing JA, Middelburg JJ, Melack J (2007) Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems 10:171–184Google Scholar
  36. Coloso JJ, Cole JJ, Hanson PC, Pace ML (2008) Depth-integrated, continuous estimates of metabolism in a clear-water lake. Can J Fish Aquat Sci 65:712–722Google Scholar
  37. Crossland CJ, Kremer HH, Marshall Crossland JI, Le Tissier MDA (2005) Coastal fluxes in the anthropocene. The land–ocean interactions in the coastal zone project of the International Geosphere-Biosphere Programme. 1-232. Global Change, The IGBP SeriesGoogle Scholar
  38. D’Avanzo C, Kremer JN, Wainright SC (1996) Ecosystem production and respiration in response to eutrophication in shallow temperate estuaries. Mar Ecol Progr Ser 141:263–274Google Scholar
  39. De Angelis DL (1992) Dynamics of nutrient cycling and food webs. Chapman & Hall, New YorkGoogle Scholar
  40. del Giorgio PA, Williams PJB (2005) Respiration in aquatic ecosystems, Oxford University Press. Inc., OxfordGoogle Scholar
  41. del Giorgio PA, Cole JJ, Caraco NF, Peters RH (1999) Linking planktonic biomass and metabolism to net gas fluxes in northern temperate lakes. Ecology 80:1422–1431Google Scholar
  42. Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929PubMedGoogle Scholar
  43. Dillon PJ, Molot LA (1997) Effect of landscape form on export of dissolved organic carbon, iron, and phosphorus from forested stream catchments. Water Resour Res 33:2591–2600Google Scholar
  44. Dineen CF (1953) An ecological study of a Minnesota pond. Am Midl Nat 50:349–376Google Scholar
  45. Dodds WK, Cole JJ (2007) Expanding the concept of trophic state in aquatic ecosystems: it’s not just the autotrophs. Aquat Sci 69:427–439Google Scholar
  46. Doney SC, Lima I, Feely RA, Glover DM, Lindsay K, Mahowald N, Moore JK, Wanninkhof R (2009) Mechanisms governing interannual variability in upper-ocean inorganic carbon system and air–sea CO2 fluxes: physical climate and atmospheric dust. Deep-Sea Res Part II Topical Stud in Oceanogr 56:640–655Google Scholar
  47. Duarte CM, Agusti S (1998) The CO2 balance of unproductive aquatic ecosystems. Science 281:234–236PubMedGoogle Scholar
  48. Duarte CM, Prairie YT (2005) Prevalence of heterotrophy and atmospheric CO2 emissions from aquatic ecosystems. Ecosystems 8:862–870Google Scholar
  49. Duarte CM, Regaudie-de-Gioux A (2009) Thresholds of gross primary production for the metabolic balance of marine planktonic communities. Limnol Oceanogr 54:1015–1022Google Scholar
  50. Duarte CM, Agusti S, Vaque D, Agawin NSR, Felipe J, Casamayor EO, Gasol JM (2005) Experimental test of bacteria-phytoplankton coupling in the Southern Ocean. Limnol Oceanogr 50:1844–1854Google Scholar
  51. Fisher SG, Likens GE (1973) Energy flow in Bear Brook, New Hampshire: integrative approach to stream ecosystem metabolism. Ecol Monogr 43:421–439Google Scholar
  52. Flöder S, Sommer U (1999) Diversity in planktonic communities: an experimental test of the intermediate disturbance hypothesis. Limnol Oceanogr 44:1114–1119Google Scholar
  53. Frankignoulle M, Abril G, Borges A, Burge I, Canon C, Delille B, Libert E, Théate J-M (1998) Carbon dioxide emmision from European estuaries. Science 282:434–436PubMedGoogle Scholar
  54. Gaarder T, Gran HH (1927) Investigations of the production of plankton in the Oslo Fjord. Rapp Et Proc Verg Cons Int Explor Mer 42:1–48Google Scholar
  55. Garnier J, Billen G (2007) Production vs. respiration in river systems: an indicator of an “ecological status”. Sci Total Environ 375:110–124PubMedGoogle Scholar
  56. Gattuso J-P, Pichon M, Delesalle B, Frankignoulle M (1993) Community metabolism and air–sea CO2 fluxes in a coral reef ecosystem (Moorea, French Polynesia). Mar Ecol Progr Ser 96:259–267Google Scholar
  57. Gattuso JP, Frankignoulle M, Smith SV (1999) Measurement of community metabolism and significance in the coral reef CO2 source-sink debate. Proc Natl Acad Sci USA 96:13017–13022PubMedGoogle Scholar
  58. Gazeau F, Borges AV, Barron C, Duarte CM, Iversen N, Middelburg JJ, Delille B, Pizay MD, Frankignoulle M, Gattuso JP (2005a) Net ecosystem metabolism in a micro-tidal estuary (Randers Fjord, Denmark): evaluation of methods. Mar Ecol Progr Ser 301:23–41Google Scholar
  59. Gazeau F, Duarte CM, Gattuso J-P, Barron C, Navarro N, Ruiz S, Prairie YT, Calleja M, Delille B, Frankignoulle M, Borges AV (2005b) Whole-system metabolism and CO2 fluxes in a Mediterranean Bay dominated by seagrass beds (Palma Bay, NW Mediterranean). Biogeosciences 2:43–60Google Scholar
  60. Gazeau F, Gattuso JP, Middelburg JJ, Brion N, Schiettecatte LS, Frankignoulle M, Borges AV (2005c) Planktonic and whole system metabolism in a nutrient-rich estuary (the Scheldt estuary). Estuaries 28:868–883Google Scholar
  61. Giddings J, Eddlemon GK (1978) Photosynthesis/respiration ratios in aquatic microcosms under arsenic stress. Water Air Soil Pollut 9:207–212Google Scholar
  62. Gordon DC, Boudreau Jr PR, Mann KH, Ong JE, Silvert WL, Smith SV, Wattayakorn G, Wulff F, Yanagi T (1996) LOICZ biogeochemical modeling guidelines, vol 5, LOICZ reports and studies, Texel, pp 1–96Google Scholar
  63. Green RE, Bianchi TS, Dagg MJ, Walker ND, Breed GA (2006) An organic carbon budget for the Mississippi River turbidity plume and plume contributions to air–sea CO2 fluxes and bottom water hypoxia. Estuaries Coasts 29:579–597Google Scholar
  64. Guadayol O, Peters F, Marrase C, Gasol JM, Roldan C, Berdalet E, Massana R, Sabata A (2009) Episodic meteorological and nutrient-load events as drivers of coastal planktonic ecosystem dynamics: a time-series analysis. Mar Ecol Progr Ser 381:139–155Google Scholar
  65. Gucker B, Boechat IG, Giani A (2009) Impacts of agricultural land use on ecosystem structure and whole-stream metabolism of tropical Cerrado streams. Freshw Biol 54:2069–2085Google Scholar
  66. Hagy JD, Sanford LP, Boynton WR (2000) Estimation of net physical transport and hydraulic residence times for a coastal plain estuary using box models. Estuaries 23:328–340Google Scholar
  67. Hanson PC, Carpenter SR, Armstrong DE, Stanley EH (2006) Lake dissolved inorganic carbon and dissolved oxygen: Changing drivers from days to decades. Ecol Monogr 76:343–363Google Scholar
  68. Hanson PC, Carpenter SR, Kimura N, Wu C, Cornelius SP, Kratz TK (2008) Evaluation of metabolism models for free-water dissolved oxygen methods in lakes. Limnol Oceanogr Methods 6:454–465Google Scholar
  69. Harris LA, Duarte CM, Nixon SW (2006) Allornetric laws and prediction in estuarine and coastal ecology. Estuar Coasts 29:340–344Google Scholar
  70. Heath M (1995) An holistic analysis of the coupling between physical and biological processes in the coastal zone. Ophelia 42:95–125Google Scholar
  71. Heip CHR, Goosen NK, Herman PMJ, Kromkamp J, Middelburg JJ, Soetaert K (1995) Production and consumption of biological particles in temperate tidal estuaries. Oceanogr Mar Biol Annu Rev 33:1–149Google Scholar
  72. Hesslein RH, Broecker WS, Quay PD, Schindler DW (1980) Whole-lake radiocarbon experiment in an oligotrophic lake at the experimental lakes area, Northwestern Ontario. Can J Fish Aquat Sci 37:455–463Google Scholar
  73. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742PubMedGoogle Scholar
  74. Holtgrieve GW, Schindler DE, Branch TA, A’Mar ZT (2010) Simultaneous quantification of aquatic ecosystem metabolism and reaeration using a Bayesian statistical model of oxygen dynamics. Limnol Oceanogr 55:1047–1063Google Scholar
  75. Hopkinson CS, Giblin AE, Tucker J, Garritt RH (1999) Benthic metabolism and nutrient cycling along an estuarine salinity gradient. Estuaries 22:863–881Google Scholar
  76. Houghton RA (2007) Balancing the global carbon budget. Annu Rev Earth Planet Sci 35:313–347Google Scholar
  77. Howarth RW, Schneider R, Swaney DP (1996) Metabolism and organic carbon fluxes in the tidal freshwater Hudson river. Estuaries 19:848–865Google Scholar
  78. Howarth RW, Swaney DP, Butler TJ, Marino R (2000) Climatic control on eutrophication of the Hudson River estuary. Ecosystems 3:210–215Google Scholar
  79. Jenkins WJ (1977) Tritium–helium dating in Sargasso Sea: measurement of oxygen utilization rates. Science 196:291–292PubMedGoogle Scholar
  80. Jin X, Gruber N, Dunne JP, Sarmiento JL, Armstrong RA (2006) Diagnosing the contribution of phytoplankton functional groups to the production and export of particulate organic carbon, CaCO3, and opal from global nutrient and alkalinity distributions. Global Biogeochem Cycles 20:1–17Google Scholar
  81. Jonsson A, Algesten G, Bergstrom AK, Bishop K, Sobek S, Tranvik LJ, Jansson M (2007) Integrating aquatic carbon fluxes in a boreal catchment carbon budget. J Hydrol 334:141–150Google Scholar
  82. Juday C (1940) The annual energy budget of an inland lake. Ecology 21:438–450Google Scholar
  83. Justic D, Rabalais NN, Turner RE (1996) Effects of climate change on hypoxia in coastal waters: a doubled CO2 scenario for the northern Gulf of Mexico. Limnol Oceanogr 41:992–1003Google Scholar
  84. Justic D, Turner RE, Rabalais NN (2003) Climatic influences on riverine nitrate flux: implications for coastal marine eutrophication and hypoxia. Estuaries 26:1–11Google Scholar
  85. Kaldy JE, Onuf CP, Eldridge PM, Cifuentes LA (2002) Carbon budget for a subtropical seagrass dominated coastal lagoon: How important are seagrasses to total ecosystem net primary production? Estuaries 25:528–539Google Scholar
  86. Karl DM, Laws EA, Morris P, le PJ, Williams B, Emerson S (2003) Metabolic balance of the open sea. Nature 426:32PubMedGoogle Scholar
  87. Kelly MH, Fitzpatrick LC, Pearson WD (1978) Phytoplankton dynamics, primary productivity and community metabolism in a north-central Texas pond. Hydrobiologia 58:245–260Google Scholar
  88. Kemp WM, Boynton WR (1980) Influence of biological and physical processes on dissolved-oxygen dynamics in an estuarine system: implications for measurement of community metabolism. Estuar Coast Marine Sci 11:407–431Google Scholar
  89. Kemp WM, Testa JM (2011) Metabolic balance between ecosystem production and consumption. In: Wolansky E, McLusky D (eds), Treatise on estuarine and coastal science, vol 7, chap 6. Elsevier Ltd., Oxford (in press) Google Scholar
  90. Kemp WM, Lewis MR, Jones TW (1986) Comparison of methods for measuring production by the submersed macrophyte, Potamogeton perfoliatus L. Limnol Oceanogr 31:1322–1334Google Scholar
  91. Kemp WM, Sampou PA, Garber J, Tuttle J, Boynton WR (1992) Seasonal depletion of oxygen from bottom waters of Chesapeake Bay: roles of benthic and planktonic respiration and physical exchange processes. Mar Ecol Progr Ser 85:137–152Google Scholar
  92. Kemp PF, Falkowski PG, Flagg CN, Phoel WC, Smith SL, Wallace DWR, Wirick CD (1994) Modeling vertical oxygen and carbon flux during stratified spring and summer conditions on the continental-shelf, Middle Atlantic Bight, Eastern USA. Deep-Sea Res Part II Topical Stud Oceanogr 41:629–655Google Scholar
  93. Kemp WM, Smith EM, Marvin-Dipasquale M, Boynton WR (1997) Organic carbon balance and net ecosystem metabolism in Chesapeake Bay. Mar Ecol Prog Ser 150:229–248Google Scholar
  94. Kemp WM, Faganeli J, Puskaric S, Smith EM, Boynton WR (1999) Pelagic-benthic coupling and nutrient cycling. In: Malone TC, Maley A, Harding LW, Smodlaka N, Turner RE (eds) Coastal and estuarine studies, ecosystems at the land-sea margin: drainage basin to coastal sea. American Geophysical Union, Washington, DC, pp 295–339Google Scholar
  95. Kemp WM, Testa JM, Conley DJ, Gilbert D, Hagy JD (2009) Temporal responses of coastal hypoxia to nutrient loading and physical controls. Biogeosciences 6:2985–3008Google Scholar
  96. Kenney BE, Litaker W, Duke CS, Ramus J (1988) Community oxygen-metabolism in a shallow tidal estuary. Estuar Coast Shelf Sci 27:33–43Google Scholar
  97. Kettle H, Merchant CJ (2005) Systematic errors in global air–sea CO2 flux caused by temporal averaging of sea-level pressure. Atmos Chem Phys 5:1459–1466Google Scholar
  98. Kleypas J, Yates K (2009) Coral reefs and ocean acidification. Oceanography 22:108–117Google Scholar
  99. Kremer JN, Vaudrey JMP, Ullman DS, Bergondo DL, LaSota N, Kincaid C, Codiga DL, Brush MJ (2010) Simulating property exchange in estuarine ecosystem models at ecologically appropriate scales. Ecol Model 221:1080–1088Google Scholar
  100. Lamberti GA, Chaloner DT, Hershey AE (2010) Linkages among aquatic ecosystems. J North Am Benthol Soc 29:245–263Google Scholar
  101. Laursen AE, Seitzinger SP, Dekorsey R, Sanders JG, Breitburg DL, Osman RW (2002) Multiple stressors in an estuarine system: effects of nutrients, trace elements, and trophic complexity on benthic photosynthesis and respiration. Estuaries 25:57–69Google Scholar
  102. Laws EA, Falkowski PG, Smith WO, Ducklow H, McCarthy JJ (2000) Temperature effects on export production in the open ocean. Global Biogeochem Cycles 14:1231–1246Google Scholar
  103. Lee K (2001) Global net community production estimated from the annual cycle of surface water total dissolved inorganic carbon. Limnol Oceanogr 46:1287–1297Google Scholar
  104. Lehrter JC, Cebrian J (2010) Uncertainty propagation in an ecosystem nutrient budget. Ecol Appl 20:508–524PubMedGoogle Scholar
  105. Lindeman RL (1942) The trophic-dynamic aspect of ecology. Ecology 23:399–417Google Scholar
  106. Lopez-Urrutia A, San Martin E, Harris RP, Irigoien X (2006) Scaling the metabolic balance of the oceans. Proc Natl Acad Sci USA 103:8739–8744PubMedGoogle Scholar
  107. Lovett GM, Cole JJ, Pace ML (2006) Is net ecosystem production equal to ecosystem carbon accumulation? Ecosystems 9:1–14Google Scholar
  108. Luz B, Barkan E (2000) Assessment of oceanic productivity with the triple-isotope composition of dissolved oxygen. Science 288:2028–2031PubMedGoogle Scholar
  109. Luz B, Barkan E, Bender ML, Thiemens MH, Boering KA (1999) Triple-isotope composition of atmospheric oxygen as a tracer of biosphere productivity. Nature 400:547–550Google Scholar
  110. Luz B, Barkan E, Sagi Y, Yacobi YZ (2002) Evaluation of community respiratory mechanisms with oxygen isotopes: a case study in Lake Kinneret. Limnol Oceanogr 47:33–42Google Scholar
  111. Martz TR, Johnson KS, Riser SC (2008) Ocean metabolism observed with oxygen sensors on profiling floats in the South Pacific. Limnol Oceanogr 53:2094–2111Google Scholar
  112. Matthews DA, Effler SW (2006) Long-term changes in the areal hypolimnetic oxygen deficit (AHOD) of Onondaga Lake: evidence of sediment feedback. Limnol Oceanogr 51:702–714Google Scholar
  113. McNiel CL, Katz DR, Ward B, McGillis WR, Johnson BD (2006) A method to estimate net community metabolism from profiles of dissolved O2 and N2. Hydrobiologia 571:181–190Google Scholar
  114. Moloney CL, Fields JG (1991) The size-based dynamics of plankton food webs 1. A simulation-model of carbon and nitrogen flows. J Plankton Res 13:1003–1038Google Scholar
  115. Najjar RG, Keeling RF (2000) Mean annual cycle of the air-sea oxygen flux: a global view. Global Biogeochem Cycles 14:573–584Google Scholar
  116. Nicholson D, Emerson S, Eriksen CC (2008) Net community production in the deep euphotic zone of the subtropical North Pacific gyre from glider surveys. Limnol Oceanogr 53:2226–2236Google Scholar
  117. O’Neill RV (1986) A hierarchical concept of ecosystems. Princeton University Press, New JerseyGoogle Scholar
  118. Odum HT (1956) Primary production in flowing waters. Limnol Oceanogr 1:102–117Google Scholar
  119. Odum HT (1957) Trophic structure and productivity of Silver Springs, Florida. Ecol Monogr 27:55–112Google Scholar
  120. Odum EP (1971) Fundamental of ecology. W.B. Saunders, PhiladelphiaGoogle Scholar
  121. Odum HT, Odum EP (1955) Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll. Ecol Monogr 25:291–320Google Scholar
  122. Ostrom NE, Carrick HJ, Twiss MR, Piwinski L (2005) Evaluation of primary production in Lake Erie by multiple proxies. Oecologia 144:115–124PubMedGoogle Scholar
  123. Oviatt CA, Keller AA, Sampou PA, Beatty LL (1986) Patterns of productivity during eutrophication: a mesocosm experiment. Mar Ecol Prog Ser 28:69–80Google Scholar
  124. Oviatt C, Doering PH, Nowicki BL, Zoppini A (1993) Net system production in coastal waters as a function of eutrophication, seasonality and benthic macrofaunal abundance. Estuaries 16:247–254Google Scholar
  125. Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (eds) (2007) Climate change 2007: impacts, adaptation and vulnerability: contribution of working group II to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  126. Peters RH (1983) The ecological implications of body size. Cambridge University Press, CambridgeGoogle Scholar
  127. Prowe AEF, Thomas H, Patsch J, Kuhn W, Bozec Y, Schiettecatte LS, Borges AV, de Baar HJW (2009) Mechanisms controlling the air–sea CO2 flux in the North Sea. Cont Shelf Res 29:1801–1808Google Scholar
  128. Quay PD, Wilbur DO, Richey JE, Devol AH (1995) The 18O:16O of dissolved oxygen in rivers and lakes in the Amazon Basin: determining the ratio of respiration to photosynthesis rates in freshwaters. Limnol Oceanogr 40:718–729Google Scholar
  129. Quinones-Rivera ZJ, Wissel B, Justic D (2009) Development of productivity models for the Northern Gulf of Mexico based on oxygen concentrations and stable isotopes. Estuar Coasts 32:436–446Google Scholar
  130. Rabalais NN, Gilbert D (2009) Distribution and consequences of hypoxia. In: Urban E, Sundby B, Malanotte-Rizzoli P (eds) Watersheds, bays and bounded seas. Island Press, pp 209–226Google Scholar
  131. Rabalais NN, Turner RE, Diaz RJ, Justic D (2009) Global change and eutrophication of coastal waters. ICES J Marine Sci 66:1528–1537Google Scholar
  132. Ram ASP, Nair S, Chandramohan D (2003) Seasonal shift in net ecosystem production in a tropical estuary. Limnol Oceanogr 48:1601–1607Google Scholar
  133. Reinthaler T, Van Aken HM, Herndl GJ (2010) Major contribution of autotrophy to microbial carbon cycling in the deep North Atlantic’s interior. Deep-Sea Res Part II Topical Stud Oceanogr 57:1572–1580Google Scholar
  134. Reuther R (1992) Arsenic introduced into a littoral freshwater model ecosystem. Sci Total Environ 115:219–237Google Scholar
  135. Roberts BJ, Mulholland PJ, Hill WR (2007) Multiple scales of temporal variability in ecosystem metabolism rates: results from 2 years of continuous monitoring in a forested headwater stream. Ecosystems 10:588–606Google Scholar
  136. Russ ME, Ostrom NE, Gandhi H, Ostrom PH (2004) Temporal and spatial variations in R:P ratios in Lake Superior, an oligotrophic freshwater environment. J Geophys Res 109:1–16Google Scholar
  137. Sanders IA, Heppell CM, Cotton JA, Wharton G, Hildrew AG, Flowers EJ, Trimmer M (2007) Emission of methane from chalk streams has potential implications for agricultural practices. Freshw Biol 52:1176–1186Google Scholar
  138. Sand-Jensen K, Staehr PA (2007) Scaling of pelagic metabolism to size, trophy and forest cover in small Danish lakes. Ecosystems 10:127–141Google Scholar
  139. Sand-Jensen K, Staehr PA (2011) CO2 dynamics along Danish lowland streams: water–air gradients, piston velocities and evasion rates. Biogeochemistry (in review)Google Scholar
  140. Sargent MC, Austin TS (1949) Organic productivity of an atoll. Trans Am Geophys Union 30:245–249Google Scholar
  141. Sargent MC, Austin TS (1954) Biologic economy of coral reefs. Bikini and nearby atolls. US Geol Survey Protess 260E:293–300Google Scholar
  142. Sarma VVSS, Abe O, Hashimoto S, Hinuma A, Saino T (2005) Seasonal variations in triple oxygen isotopes and gross oxygen production in the Sagami Bay, central Japan. Limnol Oceanogr 50:544–552Google Scholar
  143. Schindler DW (1998) Replication versus realism: the need for ecosystem-scale experiments. Ecosystems 1:323–334Google Scholar
  144. Smith SV (1973) Carbon dioxide dynamics: a record of organic carbon production, respiration, and calcification in the Eniwetok reef flat community. Limnol Oceanogr 18:106–120Google Scholar
  145. Smith SV, Hollibaugh JT (1993) Coastal metabolism and the oceanic organic carbon balance. Rev Geophys 31:75–89Google Scholar
  146. Smith SV, Hollibaugh JT (1997) Annual cycle and interannual variability of ecosystem metabolism in a temperate climate embayment. Ecol Monogr 67:509–533Google Scholar
  147. Smith EM, Kemp WM (1995) Seasonal and regional variations in plankton community production and respiration for Chesapeake Bay. Mar Ecol Prog Ser 116:217–231Google Scholar
  148. Smith SV, Key GS (1975) Carbon dioxide and metabolism in marine environments. Limnol Oceanogr 20:493–495Google Scholar
  149. Smith SV, Marsh JA (1973) Organic carbon production on the windward reef flat of Eniwek Atol. Limnol Oceanogr 18:953–961Google Scholar
  150. Smith SV, Hollibaugh JT, Dollar SJ, Vink S (1991) Tomales Bay Metabolism: C–N–P stoichiometry and ecosystem heterotrophy at the land sea interface. Estuar Coast Shelf Sci 33:223–257Google Scholar
  151. Smith SV, Swaney DP, Buddemeier RW, Scarsbrook MR, Weatherhead MA, Humborg C, Eriksson H, Hannerz F (2005a) River nutrient loads and catchment size. Biogeochemistry 75:83–107Google Scholar
  152. Smith SV, Buddemeier RW, Wulff F, Swaney DP (2005b) C, N, P fluxes in the coastal zone. In: Crossland CJ, Kremer HH, Lindeboom HJ, Marshall-Crossland JI, Le Tissier MDA (eds) Coastal fluxes in the anthropocene. Springer, Berlin, pp 95–143Google Scholar
  153. Sobek S, Tranvik LJ, Cole JJ (2005) Temperature independence of carbon dioxide supersaturation in global lakes. Global Biogeochem Cycles 19:1–10Google Scholar
  154. Squires MM, Lesack LFW, Hecky RE, Guildford SJ, Ramlal P, Higgins SN (2009) Primary production and carbon dioxide metabolic balance of a lake-rich arctic river floodplain: partitioning of phytoplankton, epipelon, macrophyte, and epiphyton production among lakes on the Mackenzie Delta. Ecosystems 12:853–872Google Scholar
  155. Staehr PA, Sand-Jensen K (2006) Seasonal changes in temperature and nutrient control of photosynthesis, respiration and growth of natural phytoplankton communities. Freshw Biol 51:249–262Google Scholar
  156. Staehr PA, Sand-Jensen K (2007) Temporal dynamics and regulation of lake metabolism. Limnol Oceanogr 52:108–120Google Scholar
  157. Staehr PA, Bade D, Van de Bogert MC, Koch GR, Williamson CE, Hanson PC, Cole JJ, Kratz T (2010a) Lake metabolism and the diel oxygen technique: state of the science. Limnol Oceanogr Methods 8:628–644Google Scholar
  158. Staehr PA, Sand-Jensen K, Raun AL, Nielsson B, Kidmose J (2010b) Drivers of metabolism and net heterotrophy in contrasting lakes. Limnol Oceanogr 55:817–830Google Scholar
  159. Staehr PA, Christensen JPA, Batt R, Read J (2011) Ecosystem metabolism in stratified lakes. Limnol Oceanogr (in review)Google Scholar
  160. Swaney DP, Howarth RW, Butler TJ (1999) A novel approach for estimating ecosystem production and respiration in estuaries: application to the oligohaline and mesohaline Hudson river. Limnol Oceanogr 44:1509–1521Google Scholar
  161. Sweeney C, Hansell DA, Carlson CA, Codispoti LA, Gordon LI, Marra J, Millero FJ, Smith WO, Takahashi T (2000) Biogeochemical regimes, net community production and carbon export in the Ross Sea, Antarctica. Deep Sea Res Part II: Topical Stud Oceanogr 47:3369–3394Google Scholar
  162. Takahashi T, Sutherland SC, Sweeney C, Poisson A, Metzl N, Tilbrook B, Bates N, Wanninkhof R, Feely RA, Sabine C, Olafsson J, Nojiri Y (2002) Global sea–air CO2 flux based on climatological surface ocean pCO2, and seasonal biological and temperature effects. Deep-Sea Res Part II-Topical Stud Oceanogr 49:1601–1622Google Scholar
  163. Tank JL, Rosi-Marshall EJ, Griffiths NA, Entrekin SA, Stephen ML (2010) A review of allochthonous organic matter dynamics and metabolism in streams. J North Am Benthol Soc 29:118–146Google Scholar
  164. Testa JM, Kemp WM (2008) Variability of biogeochemical processes and physical transport in a partially stratified estuary: a box-modeling analysis. Mar Ecol Prog Ser 356:63–79Google Scholar
  165. Tobias CR, Bölke JK, Harvey W (2007) The oxygen-18 isotope approach for measuring aquatic metabolism in high-productive waters. Limnol Oceanogr 52:1439–1453Google Scholar
  166. Tobias CR, Bohlke JK, Harvey JW, Busenberg E (2009) A simple technique for continuous measurement of time-variable gas transfer in surface waters. Limnol Oceanogr Methods 7:185–195Google Scholar
  167. Tranvik LJ, Downing JA, Cotner JB, Loiselle SA, Striegl RG, Ballatore TJ, Dillon P, Finlay K, Fortino K, Knoll LB, Kortelainen PL, Kutser T, Larsen S, Laurion I, Leech DM, McCallister SL, McKnight DM, Melack JM, Overholt E, Porter JA, Prairie Y, Renwick WH, Roland F, Sherman BS, Schindler DW, Sobek S, Tremblay A, Vanni MJ, Verschoor AM, Von Wachenfeldt E, Weyhenmeyer GA (2009) Lakes and reservoirs as regulators of carbon cycling and climate. Limnol Oceanogr 54:2298–2314Google Scholar
  168. Tsai JW, Kratz TK, Hanson PC, Wu JT, Chang WYB, Arzberger PW, Lin BS, Lin FP, Chou HM, Chiu CY (2008) Seasonal dynamics, typhoons and the regulation of lake metabolism in a subtropical humic lake. Freshw Biol 53:1929–1941Google Scholar
  169. Twilley RR, Kemp WM, Staver KW, Stevenson JC, Boynton WR (1985) Nutrient enrichment of estuarine submersed vascular plant-communities.1. Algal growth and effects on production of plants and associated communities. Mar Ecol Prog Ser 23:179–191Google Scholar
  170. 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 51:950Google Scholar
  171. Uehlinger U, Kawecka B, Robinson CT (2003) Effects of experimental floods on periphyton and stream metabolism below a high dam in the Swiss Alps (River Spöl). Aquat Sci 65:199–209Google Scholar
  172. Vadeboncoeur Y, Lodge DM, Carpenter SR (2001) Whole-lake fertilization effects on distribution of primary production between benthic and pelagic habitats. Ecology 82:1065–1077Google Scholar
  173. Vadeboncoeur Y, Jeppesen E, Vander Zanden MJ, Schierup HH, Christoffersen K, Lodge DM (2003) From Greenland to green lakes: cultural eutrophication and the loss of benthic pathways in lakes. Limnol Oceanogr 48:1408–1418Google Scholar
  174. Van de Bogert MC, Carpenter SR, Cole JJ, Pace ML (2007) Assessing pelagic benthic metabolism using free water measurements. Limnol Oceanogr Methods 5:145–155Google Scholar
  175. Venkiteswaran JJ, Schiff SL, Wassenaar LI (2008) Aquatic metabolism and ecosystem health assessment using dissolved O2 stable isotope diel curves. Ecol Appl 18:965–982PubMedGoogle Scholar
  176. Wiegner TN, Seitzinger SP, Breitburg DL, Sanders JG (2003) The effects of multiple stressors on the balance between autotrophic and heterotrophic processes in an estuarine system. Estuaries 26:352–364Google Scholar
  177. Williams PJL (1998) The balance of plankton respiration and photosynthesis in the open oceans. Nature 394:55–57Google Scholar
  178. Williamson CE, Dodds W, Kratz TK, Palmer MA (2008) Lakes and streams as sentinels of environmental change in terrestrial and atmospheric processes. Front Ecol Environ 6:247–254Google Scholar
  179. Woodwell GM, Whittaker RH (1968) Primary production in terrestrial ecosystems. Am Zool 8:19–30Google Scholar
  180. Yvon-Durocher G, Jones JI, Trimmer M, Woodward G, Montoya JM (2010) Warming alters the metabolic balance of ecosystems. Philos Trans R Soc B Biol Sci 365:2117–2126Google Scholar

Copyright information

© Springer Basel AG 2011

Authors and Affiliations

  • Peter A. Staehr
    • 1
  • Jeremy M. Testa
    • 2
  • W. Michael Kemp
    • 2
  • Jon J. Cole
    • 3
  • Kaj Sand-Jensen
    • 4
  • Stephen V. Smith
    • 5
  1. 1.Department of Marine Ecology, National Environmental Research InstituteAarhus UniversityRoskildeDenmark
  2. 2.Horn Point Laboratory, Center for Environmental ScienceUniversity of MarylandCambridgeUSA
  3. 3.Cary Institute of Ecosystem StudiesMillbrookUSA
  4. 4.Freshwater Biological LaboratoryUniversity of CopenhagenHillerødDenmark
  5. 5.Departamento de GeologíaCentro de Investigación Cientifica y de Educación Superior de EnsenadaEnsenadaMexico

Personalised recommendations