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Disproportionate increase in freshwater methane emissions induced by experimental warming

Nature Climate Change volume 10, pages 685–690 (2020)Cite this article

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Abstract

Net emissions of the potent GHG methane from ecosystems represent the balance between microbial methane production (methanogenesis) and oxidation (methanotrophy), each with different sensitivities to temperature. How this balance will be altered by long-term global warming, especially in freshwaters that are major methane sources, remains unknown. Here we show that the experimental warming of artificial ponds over 11 years drives a disproportionate increase in methanogenesis over methanotrophy that increases the warming potential of the gases they emit. The increased methane emissions far exceed temperature-based predictions, driven by shifts in the methanogen community under warming, while the methanotroph community was conserved. Our experimentally induced increase in methane emissions from artificial ponds is, in part, reflected globally as a disproportionate increase in the capacity of naturally warmer ecosystems to emit more methane. Our findings indicate that as Earth warms, natural ecosystems will emit disproportionately more methane in a positive feedback warming loop.

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Fig. 1: Ongoing divergence in methane emissions from the surfaces of our ponds mirrors natural warming.
Fig. 2: Long-term warming increases methane production over methanogen abundance.
Fig. 3: Long-term warming provides a mechanism to selectively alter the methanogen community.
Fig. 4: Methane oxidation is conserved and the growth of methanotrophy is impaired under warming.
Fig. 5: Positive climate warming feedback loop revealed by our long-term experiment.

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Data availability

The data that support the findings of this study are available from the corresponding author upon request. The DNA sequences are in the National Center for Biotechnology Information database, under BioProject ID PRJNA484117. Source data are provided with this paper.

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Acknowledgements

This study was supported by Queen Mary University of London and the UK Natural Environment Research Council (grant nos NE/M02086X/1 and NE/M020886/1). We thank I. Sanders and F. Shelley for technical and fieldwork assistance, J. Pretty for mesocosm pond maintenance, M. Rouen for designing and installing the Campbell control and data-logging system, H. Prentice for collecting sediments and for DNA extraction, C. Economou and M. Struebig for help with the molecular work, and P. K. H. Lee for providing the mcrA database and related documents for the bioinformatics analysis. We thank the principal investigators of the methane flux data products, including W. Quinton, O. Sonnentag, G. Wohlfahrt, S. Gogo, T. Schuur, K. Krauss, A. Desai, G. Bohrer, R. Vargas, D. Baldocchi, J. Chen, H. Chu, H. Iwata, M. Ueyama and Y. Harazono. We also thank the funding agencies that supported their flux measurements.

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Authors and Affiliations

  1. School of Biological and Chemical Sciences, Queen Mary University of London, London, UK

    Yizhu Zhu, Özge Eyice, Lidong Shen, Sarah F. Harpenslager & Mark Trimmer

  2. School of Life Sciences, University of Warwick, Coventry, UK

    Kevin J. Purdy

  3. Institute of Ecology, School of Applied Meteorology, Nanjing University of Information Science and Technology, Nanjing, China

    Lidong Shen

  4. Department of Ecosystem Research, Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), Berlin, Germany

    Sarah F. Harpenslager

  5. Environment and Sustainability Institute, University of Exeter, Penryn Campus, Penryn, UK

    Gabriel Yvon-Durocher

  6. School of Life Sciences, University of Essex, Colchester, UK

    Alex J. Dumbrell

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Contributions

M.T., Y.Z. and K.J.P conceived the study. Y.Z. conducted the vast majority of the experiments and analysed the data. Y.Z., M.T., K.J.P., G.Y.-D. and A.J.D. discussed the data. Y.Z., M.T. and K.J.P. wrote the manuscript, and all authors contributed to revisions. Y.Z. and S.F.H. set up the chamber system. Y.Z., O.E. and L.S. performed the molecular analyses.

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Correspondence to Mark Trimmer.

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Extended data

Extended Data Fig. 1 Schematic of experimental pond set-up and dynamic chamber measurements.

Twenty artificial ponds, with 10 warmed (red) by 4 °C above 10 ambient (blue) ponds, were paired in a randomized block design (a) and controlled via two temperature sensors (T1, T2), a thermocouple (T-stat) and a solid-state relay (SSR) (b). Dynamic LI-COR chambers, floating on lifebuoys, were installed on 7 each of the warmed and ambient ponds (c). Each floating chamber was connected to one of the inlet ports on the MIU and the MIU outlet port was connected to the gas inlet port of Ultra-Portable Greenhouse Gas Analyzer (LGR) (d). A dynamic chamber is sequentially triggered to close by a customised Campbell control unit (CCU) for 30 minutes for gas measurements while the other chambers remain open. When a chamber is triggered to close, the MIU switches simultaneously to the inlet connected to the closing chamber to direct its gas flow to the LGR. See Methods and Extended Data Fig. 2 for further details on methane emissions.

Extended Data Fig. 2 Consistent seasonal patterns in daily methane emissions under warming but with ongoing divergence over 10 years (200735, 201320 and 2017 (this study)).

The seasonal patterns in all 3 years are very similar, despite the use of different techniques but the frequent measurements (three times daily) using dynamic chambers in 2017 captured far more details in emissions compared to 2007 and 2013 when static chambers were used to measure methane emission on 7 and 12 occasions over each year, respectively. Note the natural log scale for methane emissions.

Extended Data Fig. 3 Methane emissions at night and during the day.

Methane emissions during the day (a) and at night (b) follow similar seasonal patterns; yet methane emissions at night are significantly greater than during the day (c).

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Supplementary Figs. 1–6, Tables 1–10 and discussion.

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Source Data Fig. 1

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Source Data Fig. 2

Statistical source data.

Source Data Fig. 3

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Source Data Fig. 4

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Source Data Extended Data Fig. 3

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Zhu, Y., Purdy, K.J., Eyice, Ö. et al. Disproportionate increase in freshwater methane emissions induced by experimental warming. Nat. Clim. Chang. 10, 685–690 (2020). https://doi.org/10.1038/s41558-020-0824-y

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