Permafrost Hydrology Drives the Assimilation of Old Carbon by Stream Food Webs in the Arctic
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.
KeywordsArctic 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.
- 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, https://doi.org/10.5066/P9NAUIQR.
- 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. https://doi.org/10.1029/2006JG000343.
- 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. https://doi.org/10.1088/1748-9326/aaa1fe.CrossRefGoogle Scholar
- 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
- 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. https://doi.org/10.1029/2007Gl030689.
- 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
- 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
- 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
- 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
- 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. https://doi.org/10.1029/2012GB004341.
- 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
- 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
- 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
- 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
- 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
- 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
- Soil Classification Working Group. 1998. The Canadian system of soil classification. Agriculture and agri-food Canada publication 1646:1–187.Google Scholar
- Staff SS. 1998. Keys to Soil Taxonomy. Blacksburg, Virginia: Pocahontas Press Inc.Google Scholar
- Stock BC, Semmens BX. 2013. MixSIAR GUI user manual, version 1.0. http://conserver.iugo-cafe.org/user/brice.semmens/MixSIAR.
- 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). https://doi.org/10.1029/2005GL024413.
- Team RC. 2014. R: A language and environment for statistical computing. https://www.R-project.org/.
- 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
- 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). https://doi.org/10.1029/2007GL030216.
- 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