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

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.

Fatty acid composition as a function of latitude in barnacle cyprid larvae

“…Membrane remodeling may also be critical for cyprid larvae to quickly adjust to the variable temperatures faced upon settlement (> 20 C daily oscillations found at all sampled intertidal regions). Although in some intertidal species there seems to be no correlation between membrane unsaturation state and freeze tolerance (Thyrring et al 2020(Thyrring et al , 2023, persistent exposure to water temperatures, either above or below those required to maintain optimal fluidity, initiates acclimatory (within the lifetime of an individual) or adaptational (over generations) membrane changes in fatty acid composition that may offset the direct effects of temperature on membrane lipid fluidity during the pelago-benthic transition (Hazel 1995).…”

The Eco-Immunological Relevance of the Anti-Oxidant Response in Invasive Molluscs

“…At the same time, climate change has also promoted an unanticipated reduction of sea water pH. This acidification has been demonstrated to modify the freeze tolerance of subtidal species, such as for instance M. galloprovincialis , and it will likely modify the area of distribution of subtidal and intertidal Mytilus species [ 90 ].…”