Negligible cycling of terrestrial carbon in many lakes of the arid circumpolar landscape

Abstract

High-latitude environments store nearly half of the planet’s below-ground organic carbon (OC), mostly in perennially frozen permafrost soils. Climatic changes drive increased export of terrestrial OC into many aquatic networks, yet the role that circumpolar lakes play in mineralizing this carbon is unclear. Here we directly evaluate ecosystem-scale OC cycling for lakes of interior Alaska. This arid, low-relief lake landscape is representative of over a quarter of total northern circumpolar lake area, but is greatly under-represented in current studies. Contrary to projections based on work in other regions, the studied lakes had a negligible role in mineralizing terrestrial carbon; they received little OC from ancient permafrost soils, and had small net contribution to the watershed carbon balance. Instead, most lakes recycled large quantities of internally derived carbon fixed from atmospheric CO2, underscoring their importance as critical sites for material and energy provision to regional food webs. Our findings deviate from the prevailing paradigm that northern lakes are hotspots of terrestrial OC processing. The shallow and hydrologically disconnected nature of lakes in many arid circumpolar landscapes isolates them from terrestrial carbon processing under current climatic conditions.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Distribution and carbon chemistry of lakes within arid, flat landscapes of the northern circumpolar permafrost landscape.
Fig. 2: Seasonal metabolism in YFB lakes.
Fig. 3: Decreased contribution of terrestrial vascular plant material in hydrologically disconnected lakes.
Fig. 4: Linking NEP to lake properties.
Fig. 5: Under-ice inorganic C patterns.

Code availability

Code associated with oxygen isotopic mass balance calculations for lake metabolism is available at https://github.com/MattBogard/LakeO18Metabolism.

Data availability

Data supporting the findings of this study are accessible within freely available and referenced databases, and within Supporting Information File 1 (CO2 meta-analysis). All original data generated in this study are available from the corresponding author and will be made freely available on ScienceBase (https://www.sciencebase.gov/catalog/item/5bb786b0e4b0fc368e906b09) shortly after publication.

References

  1. 1.

    Wrona, F. J. et al. Transitions in Arctic ecosystems: ecological implications of a changing hydrological regime. J. Geophys. Res. Biogeosci. 121, 650–674 (2016).

    Article  Google Scholar 

  2. 2.

    Gauthier, S., Bernier, P., Kuuluvainen, T., Shvidenko, A. Z. & Schepaschenko, D. G. Boreal forest health and global change. Science 349, 819–822 (2015).

    Article  Google Scholar 

  3. 3.

    Striegl, R. G., Aiken, G. R., Dornblaser, M. M., Raymond, P. A. & Wickland, K. P. A decrease in discharge-normalized DOC export by the Yukon River during summer through autumn. Geophys. Res. Lett. 32, L21413 (2005).

    Article  Google Scholar 

  4. 4.

    Larsen, S., Andersen, T. & Hessen, D. O. Climate change predicted to cause severe increase of organic carbon in lakes. Glob. Chang Biol. 17, 1186–1192 (2011).

  5. 5.

    Feng, X. et al. Differential mobilization of terrestrial carbon pools in Eurasian Arctic river basins. Proc. Natl Acad. Sci. USA 110, 14168–14173 (2013).

    Article  Google Scholar 

  6. 6.

    Anthony, K. M. W. et al. A shift of thermokarst lakes from carbon sources to sinks during the Holocene epoch. Nature 511, 452–456 (2014).

    Article  Google Scholar 

  7. 7.

    Schuur, E. A. G. et al. Climate change and the permafrost carbon feedback. Nature 520, 171–179 (2015).

    Article  Google Scholar 

  8. 8.

    Hastie, A. et al. CO2 evasion from boreal lakes: revised estimate, drivers of spatial variability, and future projections. Glob. Change Biol. 24, 711–728 (2018).

  9. 9.

    Stackpoole, S. M. et al. Inland waters and their role in the carbon cycle of Alaska. Ecol. Appl. 27, 1403–1420 (2017).

    Article  Google Scholar 

  10. 10.

    Vonk, J. E. et al. Reviews and syntheses: effects of permafrost thaw on Arctic aquatic ecosystems. Biogeosciences 12, 7129–7167 (2015).

    Article  Google Scholar 

  11. 11.

    Messager, M. L., Lehner, B., Grill, G., Nedeva, I. & Schmitt, O. Estimating the volume and age of water stored in global lakes using a geo-statistical approach. Nat. Commun. 7, 13603 (2016).

    Article  Google Scholar 

  12. 12.

    Olefeldt, D. et al. Circumpolar distribution and carbon storage of thermokarst landscapes. Nat. Commun. 7, 13043 (2016).

    Article  Google Scholar 

  13. 13.

    Tranvik, L. J. et al. Lakes and reservoirs as regulators of carbon cycling and climate. Limnol. Oceanogr. 54, 2298–2314 (2009).

    Article  Google Scholar 

  14. 14.

    Lapierre, J. F. & del Giorgio, P. A. Geographical and environmental drivers of regional differences in the lake pCO2 versus DOC relationship across northern landscapes. J. Geophys. Res. Biogeosci. 117, 1–10 (2012).

    Article  Google Scholar 

  15. 15.

    Evans, C. D. et al. Variability in organic carbon reactivity across lake residence time and trophic gradients. Nat. Geosci. 10, 832–835 (2017).

    Article  Google Scholar 

  16. 16.

    Ask, J., Karlsson, J. & Jansson, M. Net ecosystem production in clear-water and brown-water lakes. Global. Biogeochem. Cycles 26, 1–7 (2012).

    Article  Google Scholar 

  17. 17.

    Bogard, M. J. & Butman, D. E. No blast from the past. Nat. Clim. Change 8, 99–100 (2018).

  18. 18.

    Elder, C. D. et al. Greenhouse gas emissions from diverse Arctic Alaskan lakes are dominated by young carbon. Nat. Clim. Change 8, 166–171 (2018).

  19. 19.

    Tank, S. E., Lesack, L. F. W. & Hesslein, R. H. Northern delta lakes as summertime CO2 absorbers within the arctic landscape. Ecosystems 12, 144–157 (2009).

    Article  Google Scholar 

  20. 20.

    Hugelius, G. et al. Estimated stocks of circumpolar permafrost carbon with quantified uncertainty ranges and identified data gaps. Biogeosciences 11, 6573–6593 (2014).

    Article  Google Scholar 

  21. 21.

    Wickland, K. P. et al. Dissolved organic carbon and nitrogen release from boreal Holocene permafrost and seasonally frozen soils of Alaska. Environ. Res. Lett. 13, 065011 (2018).

    Article  Google Scholar 

  22. 22.

    Anderson, L., Birks, J., Rover, J. & Guldager, N. Controls on recent Alaskan lake changes identified from water isotopes and remote sensing. Geophys. Res. Lett. 40, 3413–3418 (2013).

    Article  Google Scholar 

  23. 23.

    Tank, S. E., Lesack, L. F. W., Gareis, J. A. L., Osburn, C. L. & Hesslein, R. H. Multiple tracers demonstrate distinct sources of dissolved organic matter to lakes of the Mackenzie Delta, western Canadian Arctic. Limnol. Oceanogr. 56, 1297–1309 (2011).

    Article  Google Scholar 

  24. 24.

    Bogard, M. J. & del Giorgio, P. A. The role of metabolism in modulating CO2 fluxes in boreal lakes. Glob. Biogeochem. Cycles 30, 1509–1525 (2016).

  25. 25.

    Walvoord, M. A., Voss, C. I. & Wellman, T. P. Influence of permafrost distribution on groundwater flow in the context of climate-driven permafrost thaw: example from Yukon Flats Basin, Alaska, United States. Water Resour. Res. 48, W07524 (2012).

  26. 26.

    Heglund, P. J. & Jones, J. R. Limnology of shallow lakes in the Yukon Flats National Wildlife Refuge, Interior Alaska. Lake Reserv. Manag. 19, 133–140 (2003).

    Article  Google Scholar 

  27. 27.

    Halm, D. R. & Griffith, B. Water-Quality Data from Lakes in the Yukon Flats, Alaska, 2010–2011 US Geological Survey Open-File Report 2014–1181 (USGS, 2014).

  28. 28.

    Lovett, G. M., Cole, J. J. & Pace, M. L. Is net ecosystem production equal to ecosystem carbon accumulation? Ecosystems 9, 152–155 (2006).

    Article  Google Scholar 

  29. 29.

    Solomon, C. T. et al. Ecosystem respiration: drivers of daily variability and background respiration in lakes around the globe. Limnol. Oceanogr. 58, 849–866 (2013).

    Article  Google Scholar 

  30. 30.

    Bogard, M. J., Vachon, D., St.-Gelais, N. F. & del Giorgio, P. A. Using oxygen stable isotopes to quantify ecosystem metabolism in northern lakes. Biogeochemistry 133, 347–364 (2017).

  31. 31.

    del Giorgio, P. & Williams, P. J. l. B. in Respiration in Aquatic Ecosystems (eds del Giorgio, P. A. & Williams, P. J. l. B.) 267–303 (Oxford Univ. Press, Oxford, 2005).

  32. 32.

    Johnston, S. E. et al. Flux and seasonality of dissolved organic matter from the northern Dvina (Severnaya Dvina) River, Russia. J. Geophys. Res. Biogeosci. 123, 1041–1056 (2018).

  33. 33.

    Spencer, R. G. M., Aiken, G. R., Wickland, K. P., Striegl, R. G. & Hernes, P. J. Seasonal and spatial variability in dissolved organic matter quantity and composition from the Yukon River Basin, Alaska. Glob. Biogeochem. Cycles 22, GB4002 (2008).

  34. 34.

    Keeling, C. D. et al. Exchanges of Atmospheric CO 2 and 13 CO 2 with the Terrestrial Biosphere and Oceans from 1978 to 2000. I. Global Aspects (Scripps Institution of Oceanography, UC San Diego, 2001).

  35. 35.

    Osburn, C. L. et al. Shifts in the source and composition of dissolved organic matter in southwest Greenland lakes along a regional hydro-climatic gradient. J. Geophys. Res. Biogeosci. 122, 3431–3445 (2017).

    Article  Google Scholar 

  36. 36.

    Waiser, M. J. & Robarts, R. D. Changes in composition and reactivity of allochthonous DOM in a prairie saline lake. Limnol. Oceanogr. 45, 763–774 (2000).

    Article  Google Scholar 

  37. 37.

    Beck, P. S. A. et al. Changes in forest productivity across Alaska consistent with biome shift. Ecol. Lett. 14, 373–379 (2011).

    Article  Google Scholar 

  38. 38.

    Edwards, M., Grosse, G., Jones, B. M. & McDowell, P. The evolution of a thermokarst-lake landscape: Late Quaternary permafrost degradation and stabilization in interior Alaska. Sediment. Geol. 340, 3–14 (2016).

    Article  Google Scholar 

  39. 39.

    Finlay, K. et al. Decrease in CO2 efflux from northern hardwater lakes with increasing atmospheric warming. Nature 519, 215–218 (2015).

    Article  Google Scholar 

  40. 40.

    Wetzel, R. G. Limnology: Lake and River Ecosystems (Academic Press, San Diego, 2001).

  41. 41.

    Holtgrieve, G. W., Schindler, D. E., Branch, T. A. & A’mar, Z. T. Simultaneous quantification of aquatic ecosystem metabolism and reaeration using a Bayesian statistical model of oxygen dynamics. Limnol. Oceanogr. 55, 1047–1062 (2010).

    Article  Google Scholar 

  42. 42.

    Striegl, R. G. et al. Carbon dioxide partial pressure and 13C content of north temperate and boreal lakes at spring ice melt. Limnol. Oceanogr. 46, 941–945 (2001).

    Article  Google Scholar 

  43. 43.

    Aiken, G. R. Chloride interference in the analysis of dissolved organic carbon by the wet oxidation method. Environ. Sci. Technol. 26, 2435–2439 (1992).

    Article  Google Scholar 

  44. 44.

    Weishaar, J. L. et al. Evaluation of specific ultraviolet absorbance as an indicator of the chemical composition and reactivity of dissolved organic carbon. Environ. Sci. Technol. 37, 4702–4708 (2003).

    Article  Google Scholar 

  45. 45.

    Révész, K. & Coplen, T. B. in Methods of the Reston Stable Isotope Laboratory: US Geological Survey Techniques and Methods (eds Révész, K. & Coplen, T. B.) Ch. 2 (USGS, 2008).

  46. 46.

    Butman, D., Raymond, P. A., Butler, K. & Aiken, G. Relationships between Δ14C and the molecular quality of dissolved organic carbon in rivers draining to the coast from the conterminous United States. Glob. Biogeochem. Cycles 26, GB4014 (2012).

    Article  Google Scholar 

  47. 47.

    Kalbitz, K., Schmerwitz, J., Schwesig, D. & Matzner, E. Biodegradation of soil-derived dissolved organic matter as related to its properties. Geoderma 113, 273–291 (2003).

    Article  Google Scholar 

  48. 48.

    Vachon, D. & Prairie, Y. T. The ecosystem size and shape dependence of gas transfer velocity versus wind speed relationships in lakes. Can. J. Fish. Aquat. Sci. 70, 1–8 (2013).

    Article  Google Scholar 

  49. 49.

    Crusius, J. & Wanninkhof, R. Gas transfer velocities measured at low wind speed over a lake. Limnol. Oceanogr. 48, 1010–1017 (2003).

    Article  Google Scholar 

  50. 50.

    Jahne, B. et al. On the parameters influencing air-water gas exchange. J. Geophys. Res. 92, 1937–1949 (1987).

    Article  Google Scholar 

  51. 51.

    Wanninkhof, R. Relationship between wind speed and gas exchange over the ocean. J. Geophys. Res. 97, 7373–7382 (1992).

    Article  Google Scholar 

  52. 52.

    Koehler, B., Landelius, T., Weyhenmeyer, G. A., Machida, N. & Tranvik, L. J. Sunlight-induced carbon dioxide emissions from inland waters. Glob. Biogeochem. Cycles 28, 696–711 (2014).

  53. 53.

    Barkan, E. & Luz, B. High precision measurements of 17O/16O and 18O/16O ratios in H2O. Rapid Commun. Mass Spectrom. 19, 3737–3742 (2005).

    Article  Google Scholar 

  54. 54.

    Knox, M., Quay, P. D. & Wilbur, D. Kinetic isotopic fractionation during air-water gas transfer of O2, N2, CH4, and H2. J. Geophys. Res. 97, 335–343 (1992).

    Article  Google Scholar 

  55. 55.

    Benson, B. B. & Krause, D. The concentration and isotopic fractionation of oxygen dissolved in freshwater and seawater in equilibrium with the atmosphere. Limnol. Oceanogr. 29, 620–632 (1984).

    Article  Google Scholar 

  56. 56.

    Guy, R. D., Fogel, M. L. & Berry, J. A. Photosynthetic fractionation of the stable isotopes of oxygen and carbon. Plant Physiol. 101, 37–47 (1993).

    Article  Google Scholar 

  57. 57.

    Winslow, L. A. et al. LakeMetabolizer: an R package for estimating lake metabolism from free-water oxygen using diverse statistical models. Inl. Waters 6, 622–636 (2016).

    Article  Google Scholar 

  58. 58.

    Schneider, U. et al. GPCC Full Data Reanalysis Version 7.0 at 0.5°: Monthly Land-Surface Precipitation from Rain-Gauges Built on GTS-based and Historic Data https://doi.org/10.5676/DWD_GPCC/FD_M_V7_050 (2015).

  59. 59.

    Olefeldt, D. et al. Arctic circumpolar distribution and soil varbon of thermokarst landscapes, 2015. ORNL DAAC https://doi.org/10.3334/ORNLDAAC/1332 (2016).

  60. 60.

    Pelletier, J. D., et al. Global 1-km gridded thickness of soil, regolith, and sedimentary deposit layers. ORNL DAAC https://doi.org/10.3334/ORNLDAAC/1304 (2016).

  61. 61.

    Danielson, J. J. & Gesch, D. B. Global Multi-resolution Terrain Elevation Data 2010 (GMTED2010) Report No. 2331-1258 (USGS, 2011).

  62. 62.

    Vermote, E., Justice, C., Claverie, M. & Franch, B. Preliminary analysis of the performance of the Landsat 8/OLI land surface reflectance product. Remote Sens. Environ. 185, 46–56 (2016).

    Article  Google Scholar 

  63. 63.

    Gorelick, N. et al. Google Earth Engine: planetary-scale geospatial analysis for everyone. Remote Sens. Environ. 202, 18–27 (2017).

    Article  Google Scholar 

  64. 64.

    Bailey, S. W. & Werdell, P. J. A multi-sensor approach for the on-orbit validation of ocean color satellite data products. Remote Sens. Environ. 102, 12–23 (2006).

    Article  Google Scholar 

  65. 65.

    Pienitz, R., Smol, J. P. & Lean, D. R. Physical and chemical limnology of 59 lakes located between the southern Yukon and the Tuktoyaktuk Peninsula, Northwest Territories (Canada). Can. J. Fish. Aquat. Sci. 54, 330–346 (1997).

    Article  Google Scholar 

  66. 66.

    Hamilton, P. B., Gajewski, K., Atkinson, D. E. & Lean, D. R. Physical and chemical limnology of 204 lakes from the Canadian Arctic Archipelago. Hydrobiologia 457, 133–148 (2001).

    Article  Google Scholar 

  67. 67.

    R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017).

  68. 68.

    Legendre, P. lmodel2: Model II Regression. R package version 1 (2013).

Download references

Acknowledgements

We thank D. Rey, B. Bloss, M. Wint, M. Haught, S. Wilson and B. Uhle for field and laboratory assistance. We also thank P. Raymond and P. Quay for the use of laboratory facilities during sample preparation for isotope analyses. We thank M. Walvoord, K. Finlay, R. Vogt, E. Hotchkiss and P. Leavitt for insightful discussions and input. Finally, we thank the many people who have graciously shared their data to make our lake CO2 meta-analysis possible. This project was supported by funding provided to M.J.B. from the Fonds de recherche du Québec—Nature et technologies (FRQNT) and the US Permafrost Association (USPA); to R.G.S., K.P.W., D.E.B. and R.G.M.S. from National Aeronautics and Space Agency, NASA-ABoVE Project 14-14TE-0012 (awards NNH16AC03I and NNX15AU14A); to D.E.B. from the University of Washington and the US Geological Survey Land Resources Mission Area and to R.G.S. and K.P.W. from the US Geological Survey Land Resources and Water Mission Areas.

Author information

Affiliations

Authors

Contributions

M.J.B. and D.E.B. designed the study and M.J.B. wrote the initial manuscript. C.D.K. and D.E.B. conducted all geospatial mapping and remote sensing analyses. M.J.B. conducted lake \(p_{\rm{CO}_2}\) meta-analysis. G.W.H. and M.J.B. analysed samples for DO and DIC isotopic ratios. S.E.J. analysed samples for lignin-phenol yield. K.P.W. and M.M.D. conducted the DOC biolability experiment. D.E.B., M.J.B., M.M.D., R.G.S. and S.E.J. conducted all other field and laboratory analyses. D.E.B., G.W.H., K.P.W., R.G.S. and R.G.M.S. provided materials. All authors contributed to manuscript preparation and revisions.

Corresponding author

Correspondence to Matthew J. Bogard.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary description, Figures 1–9 and Tables 1–3.

Supplementary Dataset

Meta-analysis of pan-arctic lake partial pressure of CO2.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bogard, M.J., Kuhn, C.D., Johnston, S.E. et al. Negligible cycling of terrestrial carbon in many lakes of the arid circumpolar landscape. Nat. Geosci. 12, 180–185 (2019). https://doi.org/10.1038/s41561-019-0299-5

Download citation

Further reading