pp 1–19 | Cite as

Permafrost Hydrology Drives the Assimilation of Old Carbon by Stream Food Webs in the Arctic

  • Jonathan A. O’DonnellEmail author
  • Michael P. Carey
  • Joshua C. Koch
  • Xiaomei Xu
  • Brett A. Poulin
  • Jennifer Walker
  • Christian E. Zimmerman


Permafrost thaw in the Arctic is mobilizing old carbon (C) from soils to aquatic ecosystems and the atmosphere. Little is known, however, about the assimilation of old C by aquatic food webs in Arctic watersheds. Here, we used C isotopes (δ13C, Δ14C) to quantify C assimilation by biota across 12 streams in arctic Alaska. Streams spanned watersheds with varying permafrost hydrology, from ice-poor bedrock to ice-rich loess (that is, yedoma). We measured isotopic content of (1) C sources including dissolved organic C (DOC), dissolved inorganic C (DIC), and soil C, and (2) stream biota, including benthic biofilm and macroinvertebrates, and resident fish species (Arctic Grayling (Thymallus arcticus) and Dolly Varden (Salvelinus malma)). Findings document the assimilation of old C by stream biota, with depleted Δ14C values observed at multiple trophic levels, including benthic biofilm (14C ages = 5255 to 265 years before present (y BP)), macroinvertebrates (4490 y BP to modern), and fish (3195 y BP to modern). Mixing model results indicate that DOC and DIC contribute to benthic biofilm composition, with relative contributions differing across streams draining ice-poor and ice-rich terrain. DOC originates primarily from old terrestrial C sources, including deep peat horizons (39–47%; 530 y BP) and near-surface permafrost (12–19%; 5490 y BP). DOC also accounts for approximately half of fish isotopic composition. Analyses suggest that as the contribution of old C to fish increases, fish growth and nutritional status decline. We anticipate increases in old DOC delivery to streams under projected warming, which may further alter food web function in Arctic watersheds.


Arctic Dissolved organic matter Streams Permafrost Food webs Radiocarbon Carbon cycle 



This work was part of the U.S. Geological Survey (USGS) Changing Arctic Ecosystem Initiative and was supported by the Wildlife Program of the USGS Ecosystem Mission Area. Funding was also provided by the Fish Program of the USGS Ecosystem Mission Area and the USGS Water Mission Area. Additional support was provided by the National Park Service’s Arctic Inventory and Monitoring Network. The authors thank Mike Records, Ylva Sjoberg, and Dereka Chargualaf for assisting with field work, and Sara Breitmeyer (U.S. Geological Survey) for conducting laboratory analyses of DOM composition. We thank the editor, subject-matter editor, and two anonymous reviewers for their comments and edits, which greatly improved our manuscript. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Supplementary material

10021_2019_413_MOESM1_ESM.docx (162 kb)
Supplementary material 1 (DOCX 162 kb)


  1. Aiken GR. 1992. Chloride interference in the analysis of dissolved organic carbon by the wet oxidation method. Environmental Science and Technology 26:2435–9.CrossRefGoogle Scholar
  2. Aiken GR, Spencer RGM, Striegl RG, Schuster PF, Raymond PA. 2014. Influences of glacier melt and permafrost thaw on the age of dissolved organic carbon in the Yukon River basin. Global Biogeochemical Cycles 28:525–37.CrossRefGoogle Scholar
  3. Barnes RT, Butman DE, Wilson HF, Raymond PA. 2018. Riverine export of aged carbon drive by flow path depth and residence time. Environmental Science & Technology 52:1028–35.CrossRefGoogle Scholar
  4. Battin TJ, Besemer K, Bengtsson MM, Romani AM, Packman AI. 2016. The ecology and biogeochemistry of stream biofilms. Nature Reviews 14:251–63.PubMedGoogle Scholar
  5. Beaupre SR, Druffel ERM, Griffin S. 2007. A low-blank photochemical extraction system for concentration and isotopic analyses of marine dissolved organic carbon. Limnology & Oceanography Methods 5:174–84.CrossRefGoogle Scholar
  6. Bellamy AR, Bauer JE. 2017. Nutritional support of inland aquatic food webs by aged carbon and organic matter. Limnology and Oceanography Letters 2:131–49.CrossRefGoogle Scholar
  7. Benfield EF. 1997. Comparison of litterfall input to streams. Journal of the North American Benthological Society 16:104–8.CrossRefGoogle Scholar
  8. Berggren M, Laudon H, Jansson M. 2009. Aging of allochthonous organic carbon regulates bacterial production in unproductive boreal lakes. Limnology & Oceanography 54:1333–42.CrossRefGoogle Scholar
  9. Besemer K, Peter H, Logue JB, Langenheder S, Lindstrom ES, Tranvik LJ, Battin TJ. 2012. Unraveling assembly of stream biofilm communities. The ISME Journal 6:1459–68.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Beverly RK, Beaumon W, Tauz D, Ormsby KM, von Reden KF, Santos GM, Southon JR. 2010. The Keck Carbon Cycle AMS Laboratory, University of California, Irvine: status report. Radiocarbon 52:301–9.CrossRefGoogle Scholar
  11. Butman D, Raymond PA, Butler K, Aiken G. 2012. Relationships between 14C and the molecular quality of dissolved organic carbon in rivers draining to the coast from the conterminous United States. Global Biogeochemical Cycles. Scholar
  12. Caraco N, Bauer JE, Cole JJ, Petsch S, Raymond P. 2010. Millennial-aged organic carbon subsidies to a modern river food web. Ecology 91:2385–93.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Carey MP, O’Donnell JA, Koch, JC. 2019. Carbon isotope concentrations in stream food webs of the Arctic Network National Parks, Alaska, 2014-2016: U.S. Geological Survey data release,
  14. Cory RM, McKnight DM, Chin YP, Miller P, Jaros CL. 2007. Chemical characteristics of fulvic acids from Arctic surface waters: Microbial contributions and photochemical transformations. Journal of Geophysical Research: Biogeosciences 112.
  15. Dean JF, Billett MF, Baxter R, Dinsmore KJ, Lessels JS, Street LE, Subke J-A, Tetzlaff D, Washbourne I, Wookey PA. 2016. Biogeochemistry of “pristine” freshwater stream and lake systems in the western Canadian Arctic. Biogeochemistry 130:191–213.CrossRefGoogle Scholar
  16. Dean JF, van der Velde Y, Garnett MH, Dinsmore KJ, Baxter R, Lessels JS, Smith P, Street LE, Subke J-A, Tetzlaff D. 2018. Abundant pre-industrial carbon detected in Canadian Arctic headwaters: implications for permafrost carbon feedback. Environmental Research Letters 13:034024. Scholar
  17. Dornblaser MM, Striegl RG. 2015. Switching predominance of organic versus inorganic carbon exports from an intermediate-size subarctic watershed. Geophysical Research Letters 42:386–94.CrossRefGoogle Scholar
  18. Drake TW, Wickland KP, Spencer RGM, McKnight DM, Striegl RG. 2015. Ancient low-molecular-weight organic acids in permafrost fuel rapid carbon dioxide production upon thaw. Proceedings of the National Academy of Sciences 112:13946–51.CrossRefGoogle Scholar
  19. Elder CD, Xu X, Walker J, Schnell JL, Hinkel KM, Townsend-Small A, Arp CD, Pohlman JW, Gaglioti BV, Czimczik CI. 2018. Greenhouse gas emissions from diverse Arctic Alaskan lakes are dominated by young carbon. Nature Climate Change 8:166–71.CrossRefGoogle Scholar
  20. Ewing SA, O’Donnell JA, Aiken GR, Butler KD, Butman D, Windham-Myers L, Kanevskiy MZ. 2015. Long-term anoxia and release of ancient, labile carbon upon thaw of Pleistocene permafrost. Geophysical Research Letters 42:10730–38.CrossRefGoogle Scholar
  21. Fellman JB, Hood E, Raymond PA, Hudson J, Bozeman M, Arimitsu M. 2015. Evidence for the assimilation of ancient glacier organic carbon in a proglacial stream food web. Limnology and Oceanography 60:1118–28.CrossRefGoogle Scholar
  22. Finlay JC. 2004. Patterns and controls of lotic algal stable carbon isotope ratios. Limnology and Oceanography 49:850–61.CrossRefGoogle Scholar
  23. Frey KE, McClelland JW. 2009. Impacts of permafrost degradation on arctic river biogeochemistry. Hydrological Processes 23:169–82.CrossRefGoogle Scholar
  24. Gao P, Xu X, Zhou L, Pack MA, Griffin S, Santos GM, Southon JR, Liu K. 2014. Rapid sample preparation of dissolved inorganic carbon in natural waters using a headspace-extraction approach for radiocarbon analysis by accelerator mass spectrometry. Limnology and Oceanography: Methods 12:174–90.Google Scholar
  25. Guillemette F, Bianchi TS, Spencer RGM. 2017. Old before your time: ancient carbon incorporation in contemporary aquatic food webs. Limnology and Oceanography 62:1682–700.CrossRefGoogle Scholar
  26. Guo L, Ping CL, Macdonald RW. 2007. Mobilization pathways of organic carbon from permafrost to arctic rivers in a changing climate. Geophysical Research Letters 34.
  27. Hågvar S, Ohlson M. 2013. Ancient carbon from a melting glacier gives high 14 C age in living pioneer invertebrates. Scientific Reports 3:2820.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hood E, Fellman J, Spencer RGM, Hernes PJ, Edwards R, D’Amore D, Scott D. 2009. Glaciers as a source of ancient and labile organic matter to the marine environment. Nature 462(7276):1044.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hugelius G, Strauss J, Zubrzycki S, Harden JW, Schuur EAG, Ping CL, Schirrmeister L, Grosse G, Michaelson GJ, Koven CD, O’Donnell JA, Elberling B, Mishra U, Camill P, Yu Z, Palmtag J, Kuhry P. 2014. Estimated stocks of circumpolar permafrost carbon with quantified uncertainty ranges and identified data gaps. Biogeosciences 11:6573–93.CrossRefGoogle Scholar
  30. Hughes NF. 1998. A model of habitat selection by drift-feeding stream salmonids at different scales. Ecology 79:281–94.CrossRefGoogle Scholar
  31. Ishikawa NF, Uchida M, Shibata Y, Tayasu I. 2014. Carbon storage reservoirs in watersheds support stream food webs via periphyton production. Ecology 95(5):1264–71.CrossRefPubMedGoogle Scholar
  32. Ishikawa NF, Yamane M, Suga H, Ogawa NO, Yokoyama Y, Ohkouchi N. 2015. Chlorophyll a-specific Δ14C, δ13C and δ15N values in stream periphyton: implications for aquatic food web studies. Biogeosciences 12:6781–9.CrossRefGoogle Scholar
  33. Kanevskiy M, Shur Y, Fortier D, Jorgenson MT, Stephani E. 2011. Cryostratigraphy of late Pleistocene syngenetic permafrost (yedoma) in northern Alaska, Itkillik River exposure. Quaternary Research 75:584–96.CrossRefGoogle Scholar
  34. Keaveney EM, Reimer PJ, Foy RH. 2015. Young, old, and weathered carbon—part 1: using radiocarbon and stable isotopes to identify carbon sources in an alkaline, humic lake. Radiocarbon 57:407–23.CrossRefGoogle Scholar
  35. Kellerman AM, Guillemette F, Podgorski DC, Aiken GR, Butler KD, Spencer RG. 2018. Unifying concepts linking dissolved organic matter composition to persistence in aquatic ecosystems. Environmental Science & Technology 52:2538–48.CrossRefGoogle Scholar
  36. Kendall C, Mast M, Rice K. 1992. Tracing watershed weathering reactions with δ13C. In: Kharaka YK, Maest AS, Eds. Water-rock interaction. Rotterdam: Balkema. p 569–72.Google Scholar
  37. Koch JC, Ewing SA, Striegl R, McKnight DM. 2013. Rapid runoff via shallow throughflow and deeper preferential flow in a boreal catchment underlain by frozen silt (Alaska, USA). Hydrogeology Journal 21:93–106.CrossRefGoogle Scholar
  38. Mann PJ, Eglinton TI, McIntyre CP, Zimov N, Davydova A, Vonk JE, Holmes RM, Spencer RGM. 2015. Utilization of ancient permafrost carbon in headwaters of Arctic fluvial networks. Nature Communications 6:7856.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Mayorga E, Aufdenkampe AK, Masiello CA, Krusche AV, Hedges JI, Quay PD, Richey JE, Brown TA. 2005. Young organic matter as a source of carbon dioxide outgassing from Amazonian rivers. Nature 436:538–41.CrossRefGoogle Scholar
  40. McGuire AD, Hayes DJ, Kicklighter DW, Manizza M, Zhuang Q, Chen M, Follows MJ, Gurney KR, McClelland JW, Melillo JM, Peterson BJ. 2010. An analysis of the carbon balance of the Arctic Basin from 1997 to 2006. Tellus B 62:455–74.CrossRefGoogle Scholar
  41. Merritt RW, Cummins KW, Berg MB, Eds. 2008. An introduction to the aquatic insects of North America. 4th edn. Dubuque, Iowa: Kendall Hunt Publishing.Google Scholar
  42. Mikan CJ, Schimel JP, Doyle AP. 2002. Temperature controls of microbial respiration in arctic tundra soils above and below freezing. Soil biology and biochemistry 34:1785–95.CrossRefGoogle Scholar
  43. Moore JW, Semmens BX. 2008. Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters 11:470–80.CrossRefPubMedGoogle Scholar
  44. Nakano S, Fausch KD, Kitano S. 2001. Flexible niche partitioning via a foraging mode shift: a proposed mechanism for coexistence in stream-dwelling charrs. Journal of Animal Ecology 68:1079–92.CrossRefGoogle Scholar
  45. O’Donnell JA, Harden JW, McGuire AD, Kanevskiy MZ, Jorgenson MT, Xu X. 2011. The effect of fire and permafrost interactions on soil carbon accumulation in an upland black spruce ecosystem of interior Alaska: implications for post-thaw carbon loss. Global Change Biology 17:1461–74.CrossRefGoogle Scholar
  46. O’Donnell JA, Aiken GR, Walvoord MA, Butler KD. 2012. Dissolved organic matter composition of winter flow in the Yukon River basin: Implications of permafrost thaw and increased groundwater discharge. Global Biogeochemical Cycles 26.
  47. O’Donnell JA, Aiken GR, Walvoord MA, Raymond PA, Butler KD, Dornblaser MM, Heckman K. 2014. Using dissolved organic matter age and composition to detect permafrost thaw in boreal watersheds of interior Alaska. Journal of Geophysical Research: Biogeosciences 119:2155–70.Google Scholar
  48. O’Donnell JA, Aiken GR, Trainor TP, Douglas TA, Butler KD. 2015. Chemical composition of rivers in Alaska’s Arctic Network, 2013-2014. Natural Resource Data Series, NPS/ARCN/NRDS, 809.Google Scholar
  49. O’Donnell JA, Aiken GR, Swanson DK, Panda S, Butler KD, Baltensperger AP. 2016. Dissolved organic matter composition of Arctic rivers: linking permafrost and parent material to riverine carbon. Global Biogeochemical Cycles 30:1811–26.CrossRefGoogle Scholar
  50. O’Donnell JA, Harden JW, Manies KL, Jorgenson MT, Kanevskiy MZ. 2013. Soil data from fire and permafrost-thaw chronosequences in upland Picea mariana stands near Hess Creek and Tok, Alaska. US Geological Survey Open-File Report 2013-1045, p 22Google Scholar
  51. Panda SK, Marchenko SS, Romanovsky VE. 2016. High-resolution permafrost modeling in the Arctic Network of National Parks, Preserves and Monuments. Natural Resource Report NPS/ARCN/NRR, 1366.Google Scholar
  52. Peterson BJ, Fry B. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18:293–320.CrossRefGoogle Scholar
  53. Peterson BJ, Deegan L, Helfrich J, Hobbie JE, Hullar M, Moller B, Ford TE, Hershey A, Hiltner A, Kipphut G, Lock MA, Fiebig DM, McKinley V, Miller MC, Vestal JR, Ventullo R, Volk G. 1993. Biological responses of a tundra river to fertilization. Ecology 74:653–72.CrossRefGoogle Scholar
  54. Phillips DL, Koch PL. 2002. Incorporating concentration dependence in stable isotope mixing models. Oecologia 130:114–25.CrossRefPubMedGoogle Scholar
  55. Raymond PA, Bauer JE. 2001. Use of 14C and 13C natural abundances for evaluating riverine, estuarine, and coastal DOC and POC sources and cycling: a review and synthesis. Organic Geochemistry 32:469–85.CrossRefGoogle Scholar
  56. Reynolds JB, Kolz AL. 2013. Electrofishing. In: Zale AV, Parrish DL, Sutton TM, Eds. Fisheries techniques. 3rd edn. Bethesda, Maryland: American Fisheries Society. p 305–61.Google Scholar
  57. Schell DM. 1983. Carbon-13 and carbon-14 abundances in Alaskan aquatic organisms: delayed production from peat in arctic food webs. Science 219:1068–71.CrossRefPubMedPubMedCentralGoogle Scholar
  58. Schuur EA, McGuire AD, Schädel C, Grosse G, Harden JW, Hayes DJ, Hugelius G, Koven CD, Kuhry P, Lawrence DM, Natali SM. 2015. Climate change and the permafrost carbon feedback. Nature 520(7546):171.CrossRefPubMedGoogle Scholar
  59. Small GE, Bixby RJ, Kazanci C, Pringle CM. 2011. Partitioning stoichiometric components of epilithic biofilm using mixing models. Limnology and Oceanography: Methods 9:185–93.Google Scholar
  60. Soil Classification Working Group. 1998. The Canadian system of soil classification. Agriculture and agri-food Canada publication 1646:1–187.Google Scholar
  61. Spencer RGM, Mann PJ, Dittmar T, Eglinton TI, McIntyre C, Holmes RGM, Zimov N, Stubbins A. 2015. Detecting the signature of permafrost thaw in Arctic rivers. Geophysical Research Letters 42:2830–5.CrossRefGoogle Scholar
  62. Staff SS. 1998. Keys to Soil Taxonomy. Blacksburg, Virginia: Pocahontas Press Inc.Google Scholar
  63. Stock BC, Semmens BX. 2013. MixSIAR GUI user manual, version 1.0.
  64. Striegl RG, Aiken GR, Dornblaser MM, Raymond PA, Wickland KP. 2005. A decrease in discharge-normalized DOC export by the Yukon River during summer through autumn. Geophysical Research Letters 32(21).
  65. Stuiver M, Polach HA. 1977. Discussion reporting of 14C data. Radiocarbon 19(3):355–63.CrossRefGoogle Scholar
  66. Swanson DK. 2015. Environmental limits of tall shrubs in Alaska’s Arctic National Parks. PloS one 10(9):e0138387. Scholar
  67. Tank SE, Striegl RG, McClelland JW, Kokelj SV. 2016. Multi-decadal increases in dissolved organic carbon and alkalinity flux from the Mackenzie drainage basin to the Arctic Ocean. Environmental Research Letters 11(5):054015. Scholar
  68. Tape K, Sturm M, Racine C. 2006. The evidence for shrub expansion in Northern Alaska and the Pan-Arctic. Global Change Biology 12:686–702.CrossRefGoogle Scholar
  69. Team RC. 2014. R: A language and environment for statistical computing.
  70. Toohey RC, Herman-Mercer NM, Schuster PF, Mutter EA, Koch JC. 2016. Multidecadal increases in the Yukon River Basin of chemical fluxes as indicators of changing flowpaths, groundwater, and permafrost. Geophysical Research Letters 43:12120–30.CrossRefGoogle Scholar
  71. Torres ME, Mix AC, Rugh WD. 2005. Precise δ13C analysis of dissolved inorganic carbon in natural waters using automated headspace sampling and continuous-flow mass spectrometry. Limnology and Oceanography: Methods 3:349–60.Google Scholar
  72. Walvoord MA, Striegl RG. 2007. Increased groundwater to stream discharge from permafrost thawing in the Yukon River basin: Potential impacts on lateral export of carbon and nitrogen. Geophysical Research Letters 34(12).
  73. Walvoord MA, Voss CI, Wellman TP. 2012. Influence of permafrost distribution on groundwater flow in the context of climate-driven permafrost thaw: example from Yukon Flats Basin, Alaska. United States. Water Resources Research. Scholar
  74. Wauthy M, Rautio M, Christoffersen KS, Forsström L, Laurion I, Mariash HL, Peura S, Vincent WF. 2018. Increasing dominance of terrigenous organic matter in circumpolar freshwaters due to permafrost thaw. Limnology and Oceanography Letters 3:186–98.CrossRefGoogle Scholar
  75. Weishaar JL, Aiken GR, Bergamaschi BA, Fram MS, Fujii R, Mopper K. 2003. Evaluation of specific ultraviolet absorbance as an indicator of the chemical composition and reactivity of dissolved organic carbon. Environmental science & technology 37:4702–8.CrossRefGoogle Scholar
  76. Xu X, Trumbore SE, Zheng S, Southon JR, McDuffee KE, Luttgen M, Liu JC. 2007. Modifying a sealed tube zinc reduction method for preparation of AMS graphite targets: reducing background and attaining high precision. Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms 259:320–9.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature (This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply) 2019

Authors and Affiliations

  1. 1.National Park ServiceAnchorageUSA
  2. 2.Alaska Science CenterU.S. Geological SurveyAnchorageUSA
  3. 3.Keck Carbon Cycle AMS Facility, Department of Earth System ScienceUniversity of CaliforniaIrvineUSA
  4. 4.U.S. Geological SurveyBoulderUSA
  5. 5.Andre E Lalonde AMS LaboratoryUniversity of OttawaOttawaCanada

Personalised recommendations