Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Climate warming restructures food webs and carbon flow in high-latitude ecosystems

An Author Correction to this article was published on 19 June 2024

A Publisher Correction to this article was published on 09 January 2024

This article has been updated

Abstract

Rapid warming of high-latitude ecosystems is increasing microbial activity and accelerating the decomposition of permafrost soils. This proliferation of microbial energy could restructure high-latitude food webs and alter carbon cycling between above-ground and below-ground habitats. We used stable isotope analysis (δ13C) of amino acids to trace carbon flow through food webs exposed to warming and quantified changes in the assimilation of microbial carbon by Arctic tundra and boreal forest consumers. From 1990 to 2021, small mammals in boreal forests exhibited a significant reduction in the use of plant-based ‘green’ food webs and an increased use of microbially mediated ‘brown’ food webs, punctuated by a >30% rise in fungal carbon assimilation. Similarly, fungal carbon assimilation rose 27% in wolf spiders under experimental warming in Arctic tundra. These findings reveal a climate-mediated ‘browning’ of high-latitude food webs and point to an understudied pathway by which animals can impact carbon cycling under climate warming.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Food-web structure and carbon flow in boreal forest mammals.
Fig. 2: Food-web structure and carbon flow in Arctic wolf spiders.
Fig. 3: Carbon assimilated by boreal forest mammals.

Similar content being viewed by others

Data availability

All data56 used in this study are publicly archived at https://figshare.com/s/4eb07f4001aadc9a9a37, https://doi.org/10.6084/m9.figshare.22975145.

Code availability

All code56 used in this study72 is publicly archived at https://figshare.com/s/4eb07f4001aadc9a9a37, https://doi.org/10.6084/m9.figshare.22975145.

Change history

References

  1. IPCC Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) (Cambridge Univ. Press, 2013).

  2. Post, E. et al. The polar regions in a 2 °C warmer world. Sci. Adv. 5, eaaw9883 (2019).

    Article  CAS  Google Scholar 

  3. Post, E. et al. Ecological dynamics across the Arctic associated with recent climate change. Science 325, 1355–1358 (2009).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Schuur, E. A. G. et al. The effect of permafrost thaw on old carbon release and net carbon exchange from tundra. Nature 459, 556–559 (2009).

    Article  CAS  Google Scholar 

  6. McCalley, C. K. et al. Methane dynamics regulated by microbial community response to permafrost thaw. Nature 514, 478–481 (2014).

    Article  CAS  Google Scholar 

  7. Hicks Pries, C. E., Schuur, E. A. G., Natali, S. M. & Crummer, K. G. Old soil carbon losses increase with ecosystem respiration in experimentally thawed tundra. Nat. Clim. Change 6, 214–218 (2016).

    Article  CAS  Google Scholar 

  8. Schuur, E. A. G. et al. Vulnerability of permafrost carbon to climate change: implications for the global carbon cycle. Bioscience 58, 701–714 (2008).

    Article  Google Scholar 

  9. Jansson, J. K. & Taş, N. The microbial ecology of permafrost. Nat. Rev. Microbiol. 12, 414–425 (2014).

    Article  CAS  Google Scholar 

  10. Guillemette, F., Bianchi, T. S. & Spencer, R. G. M. Old before your time: ancient carbon incorporation in contemporary aquatic foodwebs. Limnol. Oceanogr. 62, 1682–1700 (2017).

    Article  CAS  Google Scholar 

  11. O’Donnell, J. A. et al. Permafrost hydrology drives the assimilation of old carbon by stream food webs in the Arctic. Ecosystems 23, 435–453 (2020).

    Article  Google Scholar 

  12. Berner, L. T. & Goetz, S. J. Satellite observations document trends consistent with a boreal forest biome shift. Glob. Change Biol. 28, 3275–3292 (2022).

    Article  CAS  Google Scholar 

  13. Berner, L. T. et al. Summer warming explains widespread but not uniform greening in the Arctic tundra biome. Nat. Commun. 11, 4621 (2020).

    Article  CAS  Google Scholar 

  14. Wirta, H. K. et al. Exposing the structure of an Arctic food web. Ecol. Evol. 5, 3842–3856 (2015).

    Article  Google Scholar 

  15. Steffan, S. A. & Dharampal, P. S. Undead food-webs: integrating microbes into the food-chain. Food Webs 18, e00111 (2019).

    Article  Google Scholar 

  16. Wolkovich, E. M. et al. Linking the green and brown worlds: the prevalence and effect of multichannel feeding in food webs. Ecology 95, 3376–3386 (2014).

    Article  Google Scholar 

  17. Manlick, P. J., Cook, J. A. & Newsome, S. D. The coupling of green and brown food webs regulates trophic position in a montane mammal guild. Ecology 104, e3949 (2023).

    Article  Google Scholar 

  18. Koltz, A. M., Asmus, A., Gough, L., Pressler, Y. & Moore, J. C. The detritus-based microbial–invertebrate food web contributes disproportionately to carbon and nitrogen cycling in the Arctic. Polar Biol. 41, 1531–1545 (2018).

    Article  Google Scholar 

  19. Summerhayes, V. S. & Elton, C. S. Contributions to the ecology of Spitsbergen and Bear Island. J. Ecol. 11, 214–284 (1923).

    Article  Google Scholar 

  20. Hodkinson, I. D. & Coulson, S. J. Are high Arctic terrestrial food chains really that simple? The Bear Island food web revisited. Oikos 106, 427–431 (2004).

    Article  Google Scholar 

  21. Zou, K., Thébault, E., Lacroix, G. & Barot, S. Interactions between the green and brown food web determine ecosystem functioning. Funct. Ecol. 30, 1454–1465 (2016).

    Article  Google Scholar 

  22. Schmitz, O. J. et al. Animating the carbon cycle. Ecosystems 17, 344–359 (2014).

    Article  CAS  Google Scholar 

  23. Schmitz, O. J. & Leroux, S. J. Food webs and ecosystems: linking species interactions to the carbon cycle. Annu. Rev. Ecol. Evol. Syst. 51, 271–295 (2020).

    Article  Google Scholar 

  24. Koltz, A. M., Gough, L. & McLaren, J. R. Herbivores in Arctic ecosystems: effects of climate change and implications for carbon and nutrient cycling. Ann. N. Y. Acad. Sci. 1516, 28–47 (2022).

    Article  Google Scholar 

  25. Leroux, S. J., Wiersma, Y. F. & Vander Wal, E. Herbivore impacts on carbon cycling in boreal forests. Trends Ecol. Evol. 35, 1001–1010 (2020).

    Article  Google Scholar 

  26. Olofsson, J., Tømmervik, H. & Callaghan, T. V. Vole and lemming activity observed from space. Nat. Clim. Change 2, 880–883 (2012).

    Article  Google Scholar 

  27. Pastor, J., Naiman, R. J., Dewey, B. & McInnes, P. Moose, microbes, and the boreal forest. Bioscience 38, 770–777 (1988).

    Article  Google Scholar 

  28. Wu, X., Duffy, J. E., Reich, P. B. & Sun, S. A brown-world cascade in the dung decomposer food web of an alpine meadow: effects of predator interactions and warming. Ecol. Monogr. 81, 313–328 (2011).

    Article  Google Scholar 

  29. Schmitz, O. J., Buchkowski, R. W., Smith, J. R., Telthorst, M. & Rosenblatt, A. E. Predator community composition is linked to soil carbon retention across a human land use gradient. Ecology 98, 1256–1265 (2017).

    Article  Google Scholar 

  30. Manlick, P. J. & Newsome, S. D. Stable isotope fingerprinting traces essential amino acid assimilation and multichannel feeding in a vertebrate consumer. Methods Ecol. Evol. 13, 1819–1830 (2022).

    Article  Google Scholar 

  31. Larsen, T., Taylor, D. L., Leigh, M. B. & O’Brien, D. M. Stable isotope fingerprinting: a novel method for identifying plant, fungal, or bacterial origins of amino acids. Ecology 90, 3526–3535 (2009).

    Article  Google Scholar 

  32. Larsen, T. et al. Tracing carbon sources through aquatic and terrestrial food webs using amino acid stable isotope fingerprinting. PLoS ONE 8, e73441 (2013).

    Article  CAS  Google Scholar 

  33. Sterner, R. W. & Elser, J. J. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere (Princeton Univ. Press, 2002).

  34. Wendler, G. & Shulski, M. A century of climate change for Fairbanks, Alaska. Arctic 62, 295–300 (2009).

    Article  Google Scholar 

  35. Grodzinksi, W. Energy flow through populations of small mammals in Hie Alaskan Taiga Forest. Acta Theriol. XVI, 231–275 (1971).

    Article  Google Scholar 

  36. Rexstad, E. & Kielland, K. In Alaska’s Changing Boreal Forest (eds Chapin, F. S. III et al.) 121–132 (Oxford Univ. Press, 2006); https://doi.org/10.1093/oso/9780195154313.003.0013

  37. Koltz, A. M., Classen, A. T. & Wright, J. P. Warming reverses top-down effects of predators on belowground ecosystem function in Arctic tundra. Proc. Natl Acad. Sci. USA 115, E7541–E7549 (2018).

    Article  CAS  Google Scholar 

  38. Koltz, A. M. & Wright, J. P. Impacts of female body size on cannibalism and juvenile abundance in a dominant Arctic spider. J. Anim. Ecol. 89, 1788–1798 (2020).

    Article  Google Scholar 

  39. Boonstra, R. & Krebs, C. J. Population dynamics of red-backed voles (Myodes) in North America. Oecologia 168, 601–620 (2012).

    Article  Google Scholar 

  40. Sistla, S. A. et al. Long-term warming restructures Arctic tundra without changing net soil carbon storage. Nature 497, 615–617 (2013).

    Article  CAS  Google Scholar 

  41. Moore, J. C. & Hunt, H. W. Resource compartmentation and the stability of real ecosystems. Nature 333, 261–263 (1988).

    Article  Google Scholar 

  42. Potapov, A. M. et al. Feeding habits and multifunctional classification of soil-associated consumers from protists to vertebrates. Biol. Rev. 97, 1057–1117 (2022).

    Article  Google Scholar 

  43. Hättenschwiler, S., Tiunov, A. V. & Scheu, S. Biodiversity and litter decomposition in terrestrial ecosystems. Annu. Rev. Ecol. Evol. Syst. 36, 191–218 (2005).

    Article  Google Scholar 

  44. Waldrop, M. P. et al. Molecular investigations into a globally important carbon pool: permafrost-protected carbon in Alaskan soils. Glob. Change Biol. 16, 2543–2554 (2010).

    Article  Google Scholar 

  45. Talbot, J. M., Allison, S. D. & Treseder, K. K. Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct. Ecol. 22, 955–963 (2008).

    Article  Google Scholar 

  46. Pokarzhevskii, A. D., Van Straalen, N. M., Zaboev, D. P. & Zaitsev, A. S. Microbial links and element flows in nested detrital food-webs. Pedobiologia 47, 213–224 (2003).

    Article  Google Scholar 

  47. Mizukami, N. et al. New projections of 21st century climate and hydrology for Alaska and Hawaiʻi. Clim. Serv. 27, 100312 (2022).

    Article  Google Scholar 

  48. Krebs, C. J., Carrier, P., Boutin, S., Boonstra, R. & Hofer, E. Mushroom crops in relation to weather in the southwestern Yukon. Botany 86, 1497–1502 (2008).

    Article  Google Scholar 

  49. Thormann, M. N., Bayley, S. I. & Currah, R. S. Microcosm tests of the effects of temperature and microbial species number on the decomposition of Carex aquatilis and Sphagnum fuscum litter from southern boreal peatlands. Can. J. Microbiol. 50, 793–802 (2004).

    Article  CAS  Google Scholar 

  50. Allison, S. D. & Treseder, K. K. Climate change feedbacks to microbial decomposition in boreal soils. Fungal Ecol. 4, 362–374 (2011).

    Article  Google Scholar 

  51. Thakur, M. P. Climate warming and trophic mismatches in terrestrial ecosystems: the green–brown imbalance hypothesis. Biol. Lett. 16, 20190770 (2020).

    Article  Google Scholar 

  52. Bartley, T. J. et al. Food web rewiring in a changing world. Nat. Ecol. Evol. 3, 345–354 (2019).

    Article  Google Scholar 

  53. Hobbie, E. A. et al. Stable Isotopes and Radiocarbon Assess Variable Importance of Plants and Fungi in Diets of Arctic Ground Squirrels. Arctic, Antarct. Alp. Res. 49, 487–500 (2017).

    Article  Google Scholar 

  54. Estop-Aragonés, C. et al. Assessing the potential for mobilization of old soil carbon after permafrost thaw: a synthesis of 14C measurements from the northern permafrost region. Glob. Biogeochem. Cycles 34, e2020GB006672 (2020).

    Article  Google Scholar 

  55. Myers-Smith, I. H. et al. Complexity revealed in the greening of the Arctic. Nat. Clim. Change 10, 106–117 (2020).

    Article  Google Scholar 

  56. Manlick, P. J., Perryman, N. L., Koltz, A. M., Cook, J. A. & Newsome, S. D. Data from: ‘Climate warming restructures food webs and carbon flow in high-latitude ecosystems’. Figshare https://doi.org/10.6084/m9.figshare.22975145 (2023).

  57. Yates, T. L., Jones, C. & Cook, J. A. In Measuring and Monitoring Biological Diversity: Standard Methods for Mammals (eds Wilson, E. et al.) 265–273 (Smithsonian Institution Press, 1996).

  58. Galbreath, K. E. et al. Building an integrated infrastructure for exploring biodiversity: field collections and archives of mammals and parasites. J. Mammal. 100, 382–393 (2019).

    Article  Google Scholar 

  59. Sikes, R. S. 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J. Mammal. 97, 663–688 (2016).

    Article  Google Scholar 

  60. Dalerum, F. & Angerbjörn, A. Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144, 647–658 (2005).

    Article  CAS  Google Scholar 

  61. Silfer, J. A., Engel, M. H., Macko, S. A. & Jumeau, E. J. Stable carbon isotope analysis of amino acid enantiomers by conventional isotope ratio mass spectrometry and combined gas chromatography/isotope ratio mass spectrometry. Anal. Chem. 63, 370–374 (1991).

    Article  CAS  Google Scholar 

  62. O’Brien, D. M., Fogel, M. L. & Boggs, C. L. Renewable and nonrenewable resources: amino acid turnover and allocation to reproduction in Lepidoptera. Proc. Natl Acad. Sci. USA 99, 4413–4418 (2002).

    Article  Google Scholar 

  63. Besser, A. C., Elliott Smith, E. A. & Newsome, S. D. Assessing the potential of amino acid δ13C and δ15N analysis in terrestrial and freshwater ecosystems. J. Ecol. 110, 935–950 (2022).

    Article  CAS  Google Scholar 

  64. Dombrosky, J. A ~1000-year 13C Suess correction model for the study of past ecosystems. Holocene 30, 474–478 (2020).

    Article  Google Scholar 

  65. Ripley, B. et al. Package ‘mass’ v.7.3-60 (2013).

  66. Oksanen, J. et al. Package ‘vegan’. Community ecology package v.2.9 (2013).

  67. Parnell, A. C. & Inger, R. Simmr: a stable isotope mixing model. R package v.0.3 (2016).

  68. Hopkins, J. B., Koch, P. L., Ferguson, J. M. & Kalinowski, S. T. The changing anthropogenic diets of American black bears over the past century in Yosemite National Park. Front. Ecol. Environ. 12, 107–114 (2014).

    Article  Google Scholar 

  69. Manlick, P. J., Petersen, S. M., Moriarty, K. M. & Pauli, J. N. Stable isotopes reveal limited Eltonian niche conservatism across carnivore populations. Funct. Ecol. 33, 335–345 (2019).

    Article  Google Scholar 

  70. Reimer, R. W. & Reimer, P. J. CALIBomb (2022).

  71. Hua, Q. et al. Atmospheric radiocarbon for the period 1950–2019. Radiocarbon 64, 723–745 (2022).

    Article  CAS  Google Scholar 

  72. Spiess, A. propagate: Propagation of Uncertainty (2018).

Download references

Acknowledgements

We thank A. Martinez for laboratory assistance and L. Berner for reviewing an early version of this manuscript. P.J.M. was supported by NSF (DBI- 2010712) and the USFS Pacific Northwest Research Station, with in-kind support from UNM-CSI and UNM-MSB. A.M.K. was supported by NSF (DEB-1210704) and the National Geographic Committee for Research and Exploration.

Author information

Authors and Affiliations

Authors

Contributions

P.J.M., N.L.P. and S.D.N. conceived of the study, and all authors collected data. P.J.M. and N.L.P. conducted laboratory and statistical analyses, and P.J.M. wrote the first draft of the manuscript. All authors contributed substantially to revisions.

Corresponding author

Correspondence to Philip J. Manlick.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Climate Change thanks Emily Arsenault, Matthias Pilecky and Ryan Stephens for their contribution to the peer review of this work.

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 Fig. 1, Tables 1–3 and Protocols 1–4.

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Manlick, P.J., Perryman, N.L., Koltz, A.M. et al. Climate warming restructures food webs and carbon flow in high-latitude ecosystems. Nat. Clim. Chang. 14, 184–189 (2024). https://doi.org/10.1038/s41558-023-01893-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41558-023-01893-0

Search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology