Ocean acidification increases susceptibility to sub-zero air temperatures in ecosystem engineers and limit poleward range shifts

  1. Jakob Thyrring  Is a corresponding author
  2. Colin D Macleod
  3. Katie E Marshall
  4. Jessica Kennedy
  5. Réjean Tremblay
  6. Christopher DG Harley
  1. Aarhus University, Denmark
  2. University of Alberta, Canada
  3. University of British Columbia, Canada
  4. Université du Québec à Rimouski, Canada

Abstract

Ongoing climate change has caused rapidly increasing temperatures, and an unprecedented decline in seawater pH, known as ocean acidification. Increasing temperatures are redistributing species towards higher and cooler latitudes which are most affected by ocean acidification. Whilst the persistence of intertidal species in cold environments is related to their capacity to resist sub-zero air temperatures, studies have never considered the interacting impacts of ocean acidification and freeze stress on species survival and distribution. Here, a full-factorial experiment was used to study whether ocean acidification increases mortality in subtidal Mytilus trossulus and subtidal M. galloprovincialis, and intertidal M. trossulus following sub-zero air temperature exposure. We examined physiological processes behind variation in freeze tolerance using 1H NMR metabolomics, analyses of fatty acids, and amino acid composition. We show that low pH conditions (pH = 7.5) significantly decrease freeze tolerance in both intertidal and subtidal populations of Mytilus spp. Under current day pH conditions (pH = 7.9), intertidal M. trossulus was more freeze tolerant than subtidal M. trossulus and subtidal M. galloprovincialis. Conversely, under low pH conditions, subtidal M. trossulus was more freeze tolerant than the other mussel categories. Differences in the concentration of various metabolites (cryoprotectants), or in the composition of amino acids and cell membrane phospholipid fatty acids could not explain the decrease in survival. These results suggest that ocean acidification can offset the poleward range expansions facilitated by warming, and that reduced freeze tolerance could result in a range contraction if temperatures become lethal at the equatorward edge.

Data availability

All data produced and needed to replicate the work is deposited freely on the borealis data verse (https://borealisdata.ca) - https://doi.org/10.5683/SP3/DQ5PMQ

The following data sets were generated

Article and author information

Author details

  1. Jakob Thyrring

    Department of Ecoscience, Aarhus University, Aarhus C, Denmark
    For correspondence
    thyrring@ecos.au.dk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1029-3105
  2. Colin D Macleod

    Department of Biological Sciences, University of Alberta, Edmonton, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Katie E Marshall

    Department of Zoology, University of British Columbia, Vancouver, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Jessica Kennedy

    Department of Zoology, University of British Columbia, Vancouver, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Réjean Tremblay

    Institut des sciences de la mer, Université du Québec à Rimouski, Rimouski, Canada
    Competing interests
    The authors declare that no competing interests exist.
  6. Christopher DG Harley

    Department of Zoology, University of British Columbia, Vancouver, Canada
    Competing interests
    The authors declare that no competing interests exist.

Funding

H2020 Marie Skłodowska-Curie Actions (797387)

  • Jakob Thyrring

Danmarks Frie Forskningsfond (7027-00060B)

  • Jakob Thyrring

Natural Sciences and Engineering Research Council of Canada (RGPIN-2019-04239)

  • Katie E Marshall

Carlsbergfondet (CF21-0564)

  • Jakob Thyrring

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. David A. Donoso, Escuela Politécnica Nacional, Ecuador

Version history

  1. Received: June 15, 2022
  2. Preprint posted: July 3, 2022 (view preprint)
  3. Accepted: April 9, 2023
  4. Accepted Manuscript published: April 11, 2023 (version 1)
  5. Version of Record published: April 25, 2023 (version 2)

Copyright

© 2023, Thyrring et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Jakob Thyrring
  2. Colin D Macleod
  3. Katie E Marshall
  4. Jessica Kennedy
  5. Réjean Tremblay
  6. Christopher DG Harley
(2023)
Ocean acidification increases susceptibility to sub-zero air temperatures in ecosystem engineers and limit poleward range shifts
eLife 12:e81080.
https://doi.org/10.7554/eLife.81080

Share this article

https://doi.org/10.7554/eLife.81080

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