Reconciling Carbon-cycle Concepts, Terminology, and Methods

Abstract

Recent projections of climatic change have focused a great deal of scientific and public attention on patterns of carbon (C) cycling as well as its controls, particularly the factors that determine whether an ecosystem is a net source or sink of atmospheric carbon dioxide (CO2). Net ecosystem production (NEP), a central concept in C-cycling research, has been used by scientists to represent two different concepts. We propose that NEP be restricted to just one of its two original definitions—the imbalance between gross primary production (GPP) and ecosystem respiration (ER). We further propose that a new term—net ecosystem carbon balance (NECB)—be applied to the net rate of C accumulation in (or loss from [negative sign]) ecosystems. Net ecosystem carbon balance differs from NEP when C fluxes other than C fixation and respiration occur, or when inorganic C enters or leaves in dissolved form. These fluxes include the leaching loss or lateral transfer of C from the ecosystem; the emission of volatile organic C, methane, and carbon monoxide; and the release of soot and CO2 from fire. Carbon fluxes in addition to NEP are particularly important determinants of NECB over long time scales. However, even over short time scales, they are important in ecosystems such as streams, estuaries, wetlands, and cities. Recent technological advances have led to a diversity of approaches to the measurement of C fluxes at different temporal and spatial scales. These approaches frequently capture different components of NEP or NECB and can therefore be compared across scales only by carefully specifying the fluxes included in the measurements. By explicitly identifying the fluxes that comprise NECB and other components of the C cycle, such as net ecosystem exchange (NEE) and net biome production (NBP), we can provide a less ambiguous framework for understanding and communicating recent changes in the global C cycle.

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References

  1. Aber JD, Melillo JM. 1991. Terrestrial ecosystems. Orlando (FL): Saunders College Publishing

    Google Scholar 

  2. Aber JD, Melillo JM. 2001. Terrestrial ecosystems. 2nd ed. San Diego (CA): Harcourt–Academic Press

    Google Scholar 

  3. Andrews JA, Schlesinger WH. 2001. Soil CO2 dynamics, acidification, and chemical weathering in a temperate forest with experimental CO2 enrichment. Global Biogeochem Cycles 15:149–62

    CAS  Article  Google Scholar 

  4. Aubinet M, Heinesch B, Yernaux M. 2003. Horizontal and vertical CO2 advection in a sloping forest. Boundary Layer Meteorol 108:397–417

    Article  Google Scholar 

  5. Aumont O, Orr JC, Monfray P, Ludwig W, Amiotte-Suchet P, Probst J-L. 2001. Riverine-driven interhemispheric transport of carbon. Global Biogeochemical Cycles 15:393–405

    CAS  Article  Google Scholar 

  6. Baldocchi DD. 2003. Assessing the eddy covariance technique for evaluating carbon dioxide exchange rates of ecosystems: past, present and future. Global Change Biol 9:479–92

    Article  Google Scholar 

  7. Bousquet P, Peylin P, Ciais P, Le Quere C, Friedlingstein P, Tans PP. 2000. Regional changes in carbon dioxide fluxes of land and oceans since 1980. Science 290:1342–6

    PubMed  CAS  Article  Google Scholar 

  8. Chapin FS III, Matson PA, Mooney HA. 2002. Principles of terrestrial ecosystem ecology. New York: Springer-Verlag

    Google Scholar 

  9. Ciais P, Janssens J, Shvidenko A, Wirth C, Malhi Y, Grave J, Schulze E-D, Heimann M, Phillips O, Dolman AJ. 2005. The potential for rising CO2 to account for the observed uptake of carbon by tropical, temperate and boreal forest biomes. Griffith H, Jarvis P, editors. The Carbon Balance of Forest Biomes. Milton Park, UK: Taylor and Francis. p 109–150

    Google Scholar 

  10. Clark DA, Brown S, Kicklighter DW, Chambers JQ, Thomlinson JR, Ni J. 2001. Measuring net primary production in forests: concepts and field methods. Ecol Appl 11:356–70

    Google Scholar 

  11. Cox PM, Betts RA, Jones CD, Spall SA, Totterdell IJ. 2000. Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408:184–7

    PubMed  CAS  Article  Google Scholar 

  12. Falge E, Baldocchi D, Tenhunen J, Aubinet M, Bakwin P, Berbigier P, Bernhofer C, Burba G, Clement R, Davis KJ. 2002. Seasonality of ecosystem respiration and gross primary production as derived from FLUXNET measurements. Agricultural and Forest Meteorology 113:53–74

    Article  Google Scholar 

  13. Fisher SG, Likens GE. 1973. Energy flow in Bear Brook, New Hampshire: an integrative approach to stream ecosystem metabolism. Ecol Monogr 43:421–39

    Article  Google Scholar 

  14. Fung IY, Doney SC, Lindsay K, John J. 2005. Evolution of carbon sinks in a changing climate. Proc Nat’l Acad Sci 102:11201–6

    CAS  Article  Google Scholar 

  15. Guenther A. 2002. The contribution of reactive carbon emissions from vegetation to the carbon balance of terrestrial ecosystems. Chemosphere 49:837–44

    PubMed  CAS  Article  Google Scholar 

  16. Hanson PC, Bade DL, Carpenter SR, Kratz TK. 2003. Lake metabolism: relationships with dissolved organic carbon and phosphorus. Limnol Oceanogr 48:1112–9

    CAS  Article  Google Scholar 

  17. Heimann M, Esser G, Haxeltine A, Kaduk J, Kicklighter DW, Knorr W, Kohlmaier GH, McGuire AD, Melillo J, Moore B, Otto RD, Prentice IC, Sauf W, Schloss A, Sitch S, Wittenberg U, Wurth G. 1998. Evaluation of terrestrial carbon cycle models through simulations of the seasonal cycle of atmospheric CO2: First results of a model intercomparison study. Global Biogeochemical Cycles 12:1–24

    CAS  Article  Google Scholar 

  18. Howarth RW. 1984. The ecological significance of sulfur in the energy dynamics of salt marsh and marine sediments. Biogeochemistry 1:5–27

    CAS  Article  Google Scholar 

  19. Howarth RW, Teal JM. 1980. Energy flow in a salt marsh ecosystem: the role of reduced inorganic sulfur compounds. Am Nat 116:862–72

    CAS  Article  Google Scholar 

  20. Howarth RW, Michaels AF. 2000. The measurement of primary production in aquatic ecosystems. In: Sala OE, Jackson RB, Mooney HA, Howarth RW, editors. Methods in ecosystem science. New York: Springer-Verlag. p 72–85

    Google Scholar 

  21. Howarth RW, Schneider R, Swaney D. 1996. Metabolism and organic carbon fluxes in the tidal, freshwater Hudson River. Estuaries 19:848–65

    CAS  Article  Google Scholar 

  22. Jannasch HW, Mottl MJ. 1985. Geomicrobiology of deep-sea hydrothermal vents. Science 229:717–25

    CAS  Article  PubMed  Google Scholar 

  23. Janssens IA, Freibauer A, Ciais P, Smith P, Nabuurs GJ, Folberth G, Sehlamadinger B, Hutjes RWA, Ceulemans R, Schulze ED, Valentini D, Dolman AJ. 2003. Europe’s terrestrial biosphere absorbs 7 to 12% of European anthropogenic CO2 emissions. Science 300:1538–1542

    PubMed  CAS  Article  Google Scholar 

  24. Kesselmeier J, Ciccioli P, Kuhn U, Stefani P, Biesenthal T, Rottenberger S, Wolf A, Vitullo M, Valentini R, Nobre A, Kabat P, Andreae MO. 2002. Volatile organic compound emissions in relation to plant carbon fixation and the terrestrial carbon budget. Global Biogeochemical Cycles 16:10.1029/2001GB001813

  25. Kirschbaum MUF, Farquhar GD. 1984. Temperature dependence of whole-leaf photosynthesis in Eucalyptus pauciflora Sieb. ex Spreng. Aust J Plant Physiol 11:519–38

    Google Scholar 

  26. Kling GW, Kipphut GW, Miller MC. 1991. Arctic lakes and streams as gas conduits to the atmosphere: implications for tundra carbon budgets. Science 251:298–301

    CAS  Article  PubMed  Google Scholar 

  27. Lieth H, 1975. Modeling the primary productivity of the world. In: Lieth H, Whittaker RH, editors. Primary productivity of the biosphere. Berlin: Springer-Verlag. p 237–63

    Google Scholar 

  28. Lindeman RL. 1942. The trophic-dynamic aspects of ecology. Ecology 23:399–418

    Article  Google Scholar 

  29. Long SP, Moya EG, Imbamba SK, Kamnalrut A, Piedade MTF, Scurlock JMO, Shen YK, Hall DO. 1989. Primary productivity of natural grass ecosystems of the tropics: A Reappraisal. Plant and Soil 115:155–66

    Article  Google Scholar 

  30. Loreto F, Delfine S, Di Marco G. 1999. Estimation of photorespiratory carbon dioxide recycling during photosynthesis. Aust J Plant Physiol 26:733–6

    Article  Google Scholar 

  31. Loreto F, Velikova V, Di Marco G. 2001. Respiration in the light measured by (CO2)-C-12 emission in (CO2)-C-13 atmosphere in maize leaves. Aust J Plant Physiol 28:1103–8

    Google Scholar 

  32. Lovett GM, Cole JJ, Pace ML. 2006. Is net ecosystem production equal to ecosystem carbon storage? Ecosystems. Forthcoming

  33. Matson PA, Parton WJ, Power AG, Swift MJ. 1997. Agricultural intensification and ecosystem properties. Science 227:504–9

    Article  Google Scholar 

  34. Odum EP. 1959. Fundamentals of ecology. Philadelphia: WB Saunders

    Google Scholar 

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

    Google Scholar 

  36. Ovington JD. 1962. Quantitative ecology and the woodland ecosystem concept. Adv Ecol Res 1:103–92

    Article  Google Scholar 

  37. Peterson BJ. 1980. Aquatic primary productivity and the 14C-CO2 method: a history of the productivity problem. Annu Rev Ecol Syst 11:359–85

    Article  Google Scholar 

  38. Prentice IC, Farquhar GD, Fasham MJR, Goulden ML, Heimann M, Jaramillo VJ, Kheshgi HS, Le Quéré C, Scholes RJ, Wallace DWR. 2001. The carbon cycle and atmospheric carbon dioxide. Houghton JT et al., editors. Climate Change 2001: The Scientific Basis. Cambridge: Cambridge University Press. p 183–237

    Google Scholar 

  39. Randerson JT, Chapin FS III, Harden J, Neff JC, Harmon ME. 2002. Net ecosystem production: a comprehensive measure of net carbon accumulation by ecosystems. Ecol Appl 12:937–47

    Google Scholar 

  40. Richey JE, Melack JM, Aufdenkampe AK, Ballester VM, Hess LL. 2002. Outgassing from Amazonian rivers and wetlands as a large tropical source of atmospheric CO2. Nature 416:617–20

    PubMed  CAS  Article  Google Scholar 

  41. Richter DD, Markewitz D, Trumbore SE. 1999. Rapid accumulation and turnover of soil carbon in a reestablishing forest. Nature 400:56–8

    CAS  Article  Google Scholar 

  42. Roberts BJ, Owens TG, Ostrom NE, Howarth RW. Aquatic ecosystem respiration rates are not constant over diel cycles: direct quantification using dissolved oxygen concentration and isotopic composition in experimental ponds. Limnol Oceanogr. Forthcoming

  43. Rodin LE, Bazilevich NI. 1967. Production and mineral cycling in terrestrial vegetation. Edinburgh: Oliver & Boyd

    Google Scholar 

  44. Rosenbloom NA, Doney SC, Schimel DS. 2001. Geomorphic evolution of soil texture and organic matter in eroding landscapes. Global Biogeochem Cycles 15:365–81

    CAS  Article  Google Scholar 

  45. Sala OE, Austin AT. 2000. Methods of estimating aboveground net primary productivity. In: Sala OE, Jackson RB, Mooney HA, Howarth RW, editors. Methods in ecosystem science. New York: Springer-Verlag. p 31–43

    Google Scholar 

  46. Schimel DS. 1995. Terrestrial ecosystems and the carbon cycle. Global Change Biol 1:77–91

    Article  Google Scholar 

  47. Schlesinger WH. 1985. The formation of caliche in soils of the Mojave Desert, California. Geochim Cosmochim Acta 49:57–66

    CAS  Article  Google Scholar 

  48. Schlesinger WH. 1990. Evidensce from chronosequence studies for a low carbon-storage potential of soils. Nature 348:232–4

    CAS  Article  Google Scholar 

  49. Schlesinger WH. 1997. Biogeochemistry: an analysis of global change. 2nd ed. San Diego (CA): Academic Press

    Google Scholar 

  50. Schlesinger WH, Melack JM. 1981. Transport of organic carbon in the world’s rivers. Tellus 33:172–87

    CAS  Article  Google Scholar 

  51. Schulze E-D, Heimann M. 1998. Carbon and water exchange of terrestrial systems. In: Halloway JN, Melillo J, editors. Asian change in the context of global change. Cambridge (UK): Cambridge University Press. p 145–61

    Google Scholar 

  52. Schulze E-D, Lloyd J, Kelliher FM, Wirth C, Rebmann C, Luhker B, Mund M, Knohl A, Milyhukova JM, Schulze W, Ziegler W, Varlagin AB, Sogachev AF, Valentini R, Dore S, Grigoriev S, Kolle O, Panfyorov MI, Tchebakova N, Vygodskaya NN. 1999. Productivity of forests in the Eurosiberian boreal region and their potential to act as a carbon sink—a synthesis. Global Change Biology 5:703–722

    Article  Google Scholar 

  53. Schulze E-D, Wirth C, Heimann M. 2000. Climate change: managing forests after Kyoto. Science 289:2058–9

    PubMed  CAS  Article  Google Scholar 

  54. Schulze E-D, Wirth C, Heimann M. 2002. Carbon fluxes of the Eurosiberian region. Environ Control Biol 40:249–58

    Google Scholar 

  55. Stallard RF. 1998. Terrestrial sedimentation and the carbon cycle: coupling weathering and erosion to carbon burial. Global Biogeochem Cycles 12:231–57

    CAS  Article  Google Scholar 

  56. Wigley TML, Richels R, Edmonds JA. 1996. Economic and environmental choices in the stabilization of atmospheric CO2 concentrations. Nature 379:240–3

    CAS  Article  Google Scholar 

  57. Woodwell GM, Whittaker RH. 1968. Primary production in terrestrial communities. Am Zool 8:19–30

    Google Scholar 

  58. Woodwell GM, Mackenzie FT. 1995. Biotic feedbacks in the global climatic system: will the warming feed the warming? New York: Oxford University Press

    Google Scholar 

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Acknowledgements

We thank Gus Shaver, Stuart Fisher, and the two anonymous reviewers for their insightful comments.

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Correspondence to F. S. Chapin III.

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Chapin, F.S., Woodwell, G.M., Randerson, J.T. et al. Reconciling Carbon-cycle Concepts, Terminology, and Methods. Ecosystems 9, 1041–1050 (2006). https://doi.org/10.1007/s10021-005-0105-7

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Keywords

  • net ecosystem production
  • net ecosystem carbon balance
  • gross primary production
  • ecosystem respiration
  • autotrophic respiration
  • heterotrophic respiration
  • net ecosystem exchange
  • net biome production
  • net primary production