, Volume 133, Issue 3, pp 347–364 | Cite as

Using oxygen stable isotopes to quantify ecosystem metabolism in northern lakes

  • Matthew J. Bogard
  • Dominic Vachon
  • Nicolas F. St.-Gelais
  • Paul A. del Giorgio


In remote regions of the world, whole lake metabolic estimates are scarce, largely because long incubations, intensive sampling and deployment of monitoring equipment are impractical. The oxygen isotope (δ18O) mass balance approach represents a simple and efficient alternative to measure whole-lake gross primary production (GPP) and respiration (R) from a single point sample, yet this option has not been extensively explored in habitats such as remote northern lakes. Here, we explored the applicability of the method using a sensitivity analysis on simulated data, showing that in large, heterotrophic (i.e., R > GPP) lakes, model outputs are sensitive to input terms for isotopic fractionation and air–water gas exchange. Despite these sensitivities, field applications of the δ18O method generated promising results that were generally consistent with parallel, free-water diel DO metabolic modelling, but greater than in vitro incubation measurements. The isotopic approach captured both wide-ranging metabolic conditions in in situ experimental mesocosms, and the seasonal trends in GPP and R in a shallow, dystrophic lake. In a clearer, deeper heterotrophic lake, the isotope approach integrated a fraction of metalimnetic metabolism missed by diel DO metabolic estimates. Overall, metalimnetic contributions to surface δ18O–DO dynamics had the greatest impact on model outputs, but with accurate information on air–water gas exchange, mixing depth, and the vertical DO and light regime of a given system, these effects can be accounted for and the isotopic approach can yield well constrained, spatio-temporally integrated rates of GPP and R. The approach is clearly suitable for use in oligo- and mesotrophic lakes, especially in remote regions where sampling is logistically difficult.


Metabolism Oxygen Stable isotope Primary production Respiration Lake Net ecosystem production 



We thank Carolina Garcia Chaves, Simon Gauthier-Fautaux, Juan Pablo Nino Garcia, Cynthia Soued, Marilyne Robidoux, and Anthony Merante for field and laboratory assistance, and Alison Derry for use of the mesocosms. Annick St. Pierre, Alice Parks and the employees of the Station de biologie des Laurentides de l’Université de Montréal provided logistical support. We thank Amber Ulseth, Erin Hotchkiss, and Yves Prairie for helpful discussions on lake metabolism and the use of DO stable isotopes, Biel Obrador for providing published data, and Bob Hall plus one anonymous reviewer for providing constructive comments that improved the paper. M.J.B. was supported by doctoral grants from the National Science and Engineering Research Council of Canada (NSERC) and the Université du Québec a Montréal. This project is part of the program of the NSERC/HQ Industrial Research Chair in Carbon Biogeochemistry in Boreal Aquatic Systems (CarBBAS), co-funded by grants from NSERC and Hydro-Québec (to P.A.d.G.).

Supplementary material

10533_2017_338_MOESM1_ESM.docx (214 kb)
Supplementary material 1 (DOCX 213 kb)


  1. Allen AP, Gillooly JF, Brown JH (2005) Linking the global carbon cycle to individual metabolism. Funct Ecol 19:202–213CrossRefGoogle Scholar
  2. Ask J, Karlsson J, Jansson M (2012) Net ecosystem production in clear water and brown water lakes. Global Biogeochem Cycles 26:GB1017CrossRefGoogle Scholar
  3. Barkan E, Luz B (2005) High precision measurements of 17O/16O and 18O/16O ratios in H2O. Rapid Commun Mass Spectrom 19:3737–3742CrossRefGoogle Scholar
  4. Barth JA, Tait A, Bolshaw M (2004) Automated analyses of 18O/16O ratios in dissolved oxygen from 12-mL water samples. Limnol Oceanogr Meth 2:35–41CrossRefGoogle Scholar
  5. Bender ML (1990) The δ18O of dissolved O2 in seawater: a unique tracer of circulation and respiration in the deep sea. J Geophys Res-Oceans 95:22243–22252CrossRefGoogle Scholar
  6. Bender ML, Grande KD (1987) Production, respiration, and the isotope geochemistry of O2 in the upper water column. Global Biogeochem Cycles 1:49–59CrossRefGoogle Scholar
  7. Bender M, Orchardo J, Dickson ML, Barber R, Lindley S (1999) In vitro O2 fluxes compared with 14C production and other rate terms during the JGOFS Equatorial Pacific experiment. Deep-Sea Res Pt I 46:637–654CrossRefGoogle Scholar
  8. Benson BB, Krause D (1984) The concentration and isotopic fractionation of oxygen dissolved in freshwater and seawater in equilibrium with the atmosphere. Limnol Oceanogr 29:620–632CrossRefGoogle Scholar
  9. Bocaniov SA, Schiff SL, Smith RE (2012) Plankton metabolism and physical forcing in a productive embayment of a large oligotrophic lake: insights from stable oxygen isotopes. Freshw Biol 57:481–496CrossRefGoogle Scholar
  10. Bocaniov SA, Schiff SL, Smith RE (2015) Non steady-state dynamics of stable oxygen isotopes for estimates of metabolic balance in large lakes. J Great Lakes Res 41:719–729CrossRefGoogle Scholar
  11. Bogard MJ, del Giorgio PA, Boutet L, Chaves MCG, Prairie YT, Merante A, Derry AM (2014) Oxic water column methanogenesis as a major component of aquatic CH4 fluxes. Nat Commun 5:5350CrossRefGoogle Scholar
  12. Borges A, 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 49:1630–1641CrossRefGoogle Scholar
  13. Bouvier TC, del Giorgio PA (2002) Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnol Oceanogr 47:453–470CrossRefGoogle Scholar
  14. Brandes JA, Devol AH (1997) Isotopic fractionation of oxygen and nitrogen in coastal marine sediments. Geochim Cosmochim Acta 61:1798–1801CrossRefGoogle Scholar
  15. Cantin A, Beisner BE, Gunn JM, Prairie YT, Winter JG (2011) Effects of thermocline deepening on lake plankton communities. Can J Fish Aquat Sci 68:260–276CrossRefGoogle Scholar
  16. Carignan R, Planas D, Vis C (2000) Planktonic production and respiration in oligotrophic Shield lakes. Limnol Oceanogr 45:189–199CrossRefGoogle Scholar
  17. Chomicki KM, Schiff SL (2008) Stable oxygen isotopic fractionation during photolytic O2 consumption in stream waters. Sci Tot Environ 404:236–244CrossRefGoogle Scholar
  18. Cole JJ, Caraco NF (1998) Atmospheric exchange of carbon dioxide in a low-wind oligotrophic lake measured by the addition of SF6. Limnol Oceanogr 43:647–656CrossRefGoogle Scholar
  19. Cole JJ, Pace ML, Carpenter SR, Kitchell JF (2000) Persistence of net heterotrophy in lakes during nutrient addition and food web manipulations. Limnol Oceanogr 45:1718–1730CrossRefGoogle Scholar
  20. Cory RM, Ward CP, Crump BC, Kling GW (2014) Sunlight controls water column processing of carbon in arctic fresh waters. Science 345:925–928CrossRefGoogle Scholar
  21. del Giorgio PA, Williams PJLB (2005) The global significance of respiration in aquatic ecosystems: from single cells to the biosphere. In: del Giorgio PA, Williams PJLB (eds) Respiration in aquatic ecosystems. Oxford, New York, pp 267–303CrossRefGoogle Scholar
  22. den Heyer C, Kalff J (1998) Organic matter mineralization rates in sediments: a within-and among-lake study. Limnol Oceanogr 43:695–705CrossRefGoogle Scholar
  23. Downing JA, Rath LC (1988) Spatial patchiness in the lacustrine sedimentary environment. Limnol Oceanogr 33:447–458CrossRefGoogle Scholar
  24. Downing JA et al (2006) The global abundance and size distribution of lakes, ponds, and impoundments. Limnol Oceanogr 51:2388–2397CrossRefGoogle Scholar
  25. Dubois K, Carignan R, Veizer J (2009) Can pelagic net heterotrophy account for carbon fluxes from eastern Canadian lakes? Appl Geochem 24:988–998CrossRefGoogle Scholar
  26. 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 66:1048–1058CrossRefGoogle Scholar
  27. Gat JR (1996) Oxygen and hydrogen isotopes in the hydrologic cycle. Annu Rev Earth Planet Sci 24:225–262CrossRefGoogle Scholar
  28. Goldman JA, Kranz SA, Young JN, Tortell PD, Stanley RH, Bender ML, Morel FM (2015) Gross and net production during the spring bloom along the Western Antarctic Peninsula. New Phytol 205:182–191CrossRefGoogle Scholar
  29. Granéli W, Lindell MS, Tranvik LJ (1996) Photo-oxidative production of dissolved inorganic carbon in lakes of different humic content. Limnol Oceanogr 41:698–706CrossRefGoogle Scholar
  30. Guillemette F, McCallister SL, del Giorgio PA (2013) Differentiating the degradation dynamics of algal and terrestrial carbon within complex natural dissolved organic carbon in temperate lakes. J Geophys Res Biogeo 118:963–973CrossRefGoogle Scholar
  31. Guy RD, Fogel ML, Berry JA (1993) Photosynthetic fractionation of the stable isotopes of oxygen and carbon. Plant Physiol 101:37–47CrossRefGoogle Scholar
  32. Hanson PC, Bade DL, Carpenter SR, Kratz TK (2003) Lake metabolism: relationships with dissolved organic carbon and phosphorus. Limnol Oceanogr 48:1112–1119CrossRefGoogle Scholar
  33. 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 6:454–465CrossRefGoogle Scholar
  34. 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 55:1047–1063CrossRefGoogle Scholar
  35. Hotchkiss ER, Hall RO Jr (2014) High rates of daytime respiration in three streams: use of δ18OO2 and O2 to model diel ecosystem metabolism. Limnol Oceanogr 59:798–810CrossRefGoogle Scholar
  36. Jähne B, Münnich KO, Bösinger R, Dutzi A, Huber W, Libner P (1987) On the parameters influencing air-water gas exchange. J Geophys Res-Oceans 92:1937–1949CrossRefGoogle Scholar
  37. Jobin VO, Beisner BE (2014) Deep chlorophyll maxima, spatial overlap and diversity in phytoplankton exposed to experimentally altered thermal stratification. J Plankton Res 36:933–942CrossRefGoogle Scholar
  38. Jonsson A, Meili M, Bergström AK, Jansson M (2001) Whole-lake mineralization of allochthonous and autochthonous organic carbon in a large humic lake (Örträsket, N. Sweden). Limnol Oceanogr 46:1691–1700CrossRefGoogle Scholar
  39. Karlsson J, Byström P, Ask J, Ask P, Persson L, Jansson M (2009) Light limitation of nutrient-poor lake ecosystems. Nature 460:506–509CrossRefGoogle Scholar
  40. Kiddon J, Bender ML, Orchardo J, Caron DA, Goldman JC, Dennett M (1993) Isotopic fractionation of oxygen by respiring marine organisms. Global Biogeochem Cycles 7:679–694CrossRefGoogle Scholar
  41. Knox M, Quay PD, Wilbur D (1992) Kinetic isotopic fractionation during air–water gas transfer of O2, N2, CH4, and H2. J Geophys Res 97:20335–20343CrossRefGoogle Scholar
  42. Kortelainen P et al (2006) Sediment respiration and lake trophic state are important predictors of large CO2 evasion from small boreal lakes. Global Change Biol 12:1554–1567CrossRefGoogle Scholar
  43. Kroopnick P, Craig H (1972) Atmospheric oxygen: isotopic composition and solubility fractionation. Science 175:54–55CrossRefGoogle Scholar
  44. Lapierre JF, Seekell DA, del Giorgio PA (2015) Climate and landscape influence on indicators of lake carbon cycling through spatial patterns in dissolved organic carbon. Global Change Biol 21:4425–4435CrossRefGoogle Scholar
  45. Lehmann MF et al (2009) Aerobic respiration and hypoxia in the Lower St. Lawrence Estuary: stable isotope ratios of dissolved oxygen constrain oxygen sink partitioning. Limnol Oceanogr 54:2157–2169CrossRefGoogle Scholar
  46. Lennon JT, Hamilton SK, Muscarella ME, Grandy AS, Wickings K, Jones SE (2013) A source of terrestrial organic carbon to investigate the browning of aquatic ecosystems. PLoS ONE 8:e75771CrossRefGoogle Scholar
  47. Lewis WM Jr (2011) Global primary production of lakes: 19th Baldi Memorial Lecture. Inland Waters 1:1–28CrossRefGoogle Scholar
  48. Luz B, Barkan E (2000) Assessment of oceanic productivity with the triple-isotope composition of dissolved oxygen. Science 288:2028–2031CrossRefGoogle Scholar
  49. 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 47:33–42CrossRefGoogle Scholar
  50. McCallister SL, del Giorgio PA (2008) Direct measurement of the δ13C signature of carbon respired by bacteria in lakes: linkages to potential carbon sources, ecosystem baseline metabolism, and CO2 fluxes. Limnol Oceanogr 53:1204–1216CrossRefGoogle Scholar
  51. Obrador B, Staehr PA, Christensen JP (2014) Vertical patterns of metabolism in three contrasting stratified lakes. Limnol Oceanogr 59:1228–1240CrossRefGoogle Scholar
  52. Ostrom NE, Russ ME, Field A, Piwinski L, Twiss MR, Carrick HJ (2005) Ratios of community respiration to photosynthesis and rates of primary production in Lake Erie via oxygen isotope techniques. J Great Lakes Res 31:138–153CrossRefGoogle Scholar
  53. Pace ML, Prairie YT (2005) Respiration in lakes. In: del Giorgio PA, Williams PJLB (eds) Respiration in aquatic ecosystems. Oxford, New York, pp 103–121CrossRefGoogle Scholar
  54. Parker SR, Poulson SR, Gammons CH, DeGrandpre MD (2005) Biogeochemical controls on diel cycling of stable isotopes of dissolved O2 and dissolved inorganic carbon in the Big Hole River, Montana. Environ Sci Technol 39:7134–7140CrossRefGoogle Scholar
  55. Pollard PC (2013) In situ rapid measures of total respiration rate capture the super labile DOC bacterial substrates of freshwater. Limnol Oceanogr 11:584–593CrossRefGoogle Scholar
  56. Quay PD, Emerson S, Wilbur DO, Stump C, Knox M (1993) The δ18O of dissolved O2 in the surface waters of the subarctic Pacific: a tracer of biological productivity. J Geophys Res 98:8447–8458CrossRefGoogle Scholar
  57. Quay PD, Wilbur D, Richey JE, Devol AH, Benner R, Forsberg BR (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 40:718–729CrossRefGoogle Scholar
  58. Quay PD, Peacock C, Björkman K, Karl DM (2010) Measuring primary production rates in the ocean: enigmatic results between incubation and non-incubation methods at Station ALOHA. Global Biogeochem Cycles 24:3CrossRefGoogle Scholar
  59. Quiñones-Rivera ZJ, Wissel B, Justic D, Fry B (2007) Partitioning oxygen sources and sinks in a stratified, eutrophic coastal ecosystem using stable oxygen isotopes. Mar Ecol Prog Ser 342:69–83CrossRefGoogle Scholar
  60. Quiñones-Rivera ZJ, Wissel B, Justić D (2009) Development of productivity models for the northern Gulf of Mexico based on oxygen concentrations and stable isotopes. Estuaries Coasts 32:436–446CrossRefGoogle Scholar
  61. Quiñones-Rivera ZJ, Finlay K, Vogt RJ, Leavitt PR, Wissel B (2015) Hydrologic, metabolic and chemical regulation of water-column metabolism and atmospheric CO2 exchange in a large continental reservoir during spring and summer. J Great Lakes Res 41:144–154CrossRefGoogle Scholar
  62. Read JS et al (2011) Derivation of lake mixing and stratification indices from high-resolution lake buoy data. Environ Modell Softw 26:1325–1336CrossRefGoogle Scholar
  63. Robidoux M, del Giorgio PA, Derry A (2015) Landscape-level variation among crustacean zooplankton lake populations in face of a humic stressor. Freshw Biol 60:1263–1278CrossRefGoogle Scholar
  64. Russ ME, Ostrom NE, Gandhi H, Ostrom PH, Urban NR (2004) Temporal and spatial variations in R:P ratios in Lake Superior, an oligotrophic freshwater environment. J Geophys Res 109:C10CrossRefGoogle Scholar
  65. Solomon CT et al (2013) Ecosystem respiration: drivers of daily variability and background respiration in lakes around the globe. Limnol Oceanogr 58:849–866CrossRefGoogle Scholar
  66. Staehr PA et al (2010) Lake metabolism and the diel oxygen technique: state of the science. Limnol Oceanogr-Meth 8:628–644CrossRefGoogle Scholar
  67. Staehr PA, Testa JM, Kemp WM, Cole JJ, Sand-Jensen K, Smith SV (2012) The metabolism of aquatic ecosystems: history, applications, and future challenges. Aquat Sci 74:15–29CrossRefGoogle Scholar
  68. Tobias CR, Böhlke JK, Harvey JW (2007) The oxygen-18 isotope approach for measuring aquatic metabolism in high productivity waters. Limnol Oceanogr 52:1439–1453CrossRefGoogle Scholar
  69. Vachon D, del Giorgio PA (2014) Whole-lake CO2 dynamics in response to storm events in two morphologically different lakes. Ecosystems 17:1338–1353CrossRefGoogle Scholar
  70. Vachon D, Prairie YT (2013) The ecosystem size and shape dependence of gas transfer velocity versus wind speed relationships in lakes. Can J Fish Aquat Sci 70:1757–1764CrossRefGoogle Scholar
  71. Vachon D, Prairie YT, Cole JJ (2010) The relationship between near-surface turbulence and gas transfer velocity in freshwater systems and its implications for floating chamber measurements of gas exchange. Limnol Oceanogr 55:1723–1732CrossRefGoogle Scholar
  72. Vachon D, Lapierre JF, del Giorgio PA (2016) Seasonality of photo-chemical dissolved organic carbon mineralization and its relative contribution to pelagic CO2 production in northern lakes. J Geophys Res Biogeo 121:864–878CrossRefGoogle Scholar
  73. Van de Bogert MC, Carpenter SR, Cole JJ, Pace ML (2007) Assessing pelagic and benthic metabolism using free water measurements. Limnol Oceanogr-Meth 5:145–155CrossRefGoogle Scholar
  74. Venkiteswaran JJ, Wassenaar LI, Schiff SL (2007) Dynamics of dissolved oxygen isotopic ratios: a transient model to quantify primary production, community respiration, and air–water exchange in aquatic ecosystems. Oecologia 153:385–398CrossRefGoogle Scholar
  75. Wang X, Depew D, Schiff S, Smith RE (2008) Photosynthesis, respiration, and stable isotopes of oxygen in a large oligotrophic lake (Lake Erie, USA-Canada). Can J Fish Aquat Sci 65:2320–2331CrossRefGoogle Scholar
  76. Wanninkhof R (1992) Relationship between wind speed and gas exchange over the ocean. J Geophys Res 97:7373–7382CrossRefGoogle Scholar
  77. Wassenaar LI (2012) Dissolved oxygen status of Lake Winnipeg: spatio-temporal and isotopic (δ18O–O 2) patterns. J Great Lakes Res 38:123–134CrossRefGoogle Scholar
  78. Wassenaar LI, Koehler G (1999) An on-line technique for the determination of the δ18O and δ17O of gaseous and dissolved oxygen. Anal Chem 71:4965–4968CrossRefGoogle Scholar
  79. Yang H, Andersen T, Dörsch P, Tominaga K, Thrane JE, Hessen DO (2015) Greenhouse gas metabolism in Nordic boreal lakes. Biogeochemistry 126:211–225CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Matthew J. Bogard
    • 1
    • 2
  • Dominic Vachon
    • 1
    • 3
  • Nicolas F. St.-Gelais
    • 1
  • Paul A. del Giorgio
    • 1
  1. 1.Groupe de Recherche Interuniversitaire En Limnologie, Département des Sciences BiologiquesUniversité du Québec à MontréalMontréalCanada
  2. 2.School of Environmental and Forest Sciences, College of the EnvironmentUniversity of WashingtonSeattleUSA
  3. 3.Department F.-A. Forel for Environmental and Aquatic Sciences (DEFSE), Faculty of ScienceUniversity of GenevaGenevaSwitzerland

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