Ocean acidification increases susceptibility to sub-zero air temperatures in ecosystem engineers and limits poleward range shifts
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Curated by eLife
Evaluation Summary:
This paper is of broad interest to biologists and climate modelers that study the impact of environmental stress (especially multiple stressors) on marine life. The authors show that exposure to low pH (ocean acidification) decreases the ability of two mussel species to survive freezing stress. The authors measure multiple biochemical parameters to try and identify the mechanisms underlying the change in freeze tolerance, but future work will be needed to resolve the underlying mechanism in detail.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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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 toward higher and cooler latitudes that are most affected by ocean acidification. While 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 1 H 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 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.
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Evaluation Summary:
This paper is of broad interest to biologists and climate modelers that study the impact of environmental stress (especially multiple stressors) on marine life. The authors show that exposure to low pH (ocean acidification) decreases the ability of two mussel species to survive freezing stress. The authors measure multiple biochemical parameters to try and identify the mechanisms underlying the change in freeze tolerance, but future work will be needed to resolve the underlying mechanism in detail.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Reviewer #1 (Public Review):
Thyrring et al. provide a nice experiment testing the role of ocean acidification on the survival of two bivalve species. This novel work is fundamental in setting a more mechanistic understanding of the impacts of climate change on ocean species survival, and secondarily on their re-distribution across the globe. To me, the strength of the paper relies on the experimental setup, and on being honest about the limitations of metabolomics, fatty acids, and amino acids in explaining these results.
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Reviewer #2 (Public Review):
The authors conduct a novel study comparing the interaction of climate change stressors (ocean acidification and extreme cold) in two mussel species. While ocean acidification and warm temperatures have been studied together, this study is the first to study ocean acidification and low temperature stress, which are likely to affect species at their poleward range limits. This is particularly relevant for intertidal populations, which are likely to freeze when exposed to air at low tide. The authors show that even a short (10 days) exposure to ecologically-relevant low pH causes a decrease in freeze tolerance in both species (Mytilus trossulus and Mytilus galloprovincialis), and this is true for populations from both intertidal (often air-exposed) and subtidal (rarely air-exposed) populations of M. …
Reviewer #2 (Public Review):
The authors conduct a novel study comparing the interaction of climate change stressors (ocean acidification and extreme cold) in two mussel species. While ocean acidification and warm temperatures have been studied together, this study is the first to study ocean acidification and low temperature stress, which are likely to affect species at their poleward range limits. This is particularly relevant for intertidal populations, which are likely to freeze when exposed to air at low tide. The authors show that even a short (10 days) exposure to ecologically-relevant low pH causes a decrease in freeze tolerance in both species (Mytilus trossulus and Mytilus galloprovincialis), and this is true for populations from both intertidal (often air-exposed) and subtidal (rarely air-exposed) populations of M. trosssulus. Studying multiple stressors and their interactions is important for understanding ecologically-relevant organismal responses to their environment, especially under climate change scenarios.
The authors also measure a suite of metabolites (amino acids, other small soluble molecules) and phospholipid fatty acid composition in the gills of mussels exposed to control or low pH for 10 days. None of these biochemical parameters change sufficiently to explain the decreased freeze tolerance of mussels exposed to low pH. Further work (in future studies) will be needed to better understand the mechanisms that link low pH exposure to poor freeze tolerance.
The methods are explained and described extremely well, and limitations to any of the methods are openly described. All treatments and methods are validated in some way (e.g. pH was measured in two ways multiple times during the control vs. low pH exposures). The experimental design and statistical analyses are well thought out. The only analysis that does not seem to impact the conclusions of the paper (at the time of writing) is the correlation analysis between metabolites.
The authors interpret their results appropriately; that is the results generally support the conclusions.
This interesting paper sets the stage for lots of future work on the interacting stressors of ocean acidification and low temperatures on marine life.
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Reviewer #3 (Public Review):
The authors assess response to ocean acidification with three populations of mussels encompassing two species: Mytilus trossulus from the intertidal and subtidal and M. galloprovincialis from a subtidal aquaculture farm. All three species received an ambient of low pH treatment prior to a freezing treatment. The authors find species differences in freeze tolerance in mussels, with intertidal M. galloprovincialis showing the least freeze tolerance. The authors go a step further and do a comprehensive assessment of the metabolic capacity and molecular components with analyses of amino acids, fatty acids, and osmolytes and anaerobic byproducts.
The authors hypothesized metabolic changes due to OA and cold temperatures, yet they demonstrated a significant amount of stasis with high similarity among species at …
Reviewer #3 (Public Review):
The authors assess response to ocean acidification with three populations of mussels encompassing two species: Mytilus trossulus from the intertidal and subtidal and M. galloprovincialis from a subtidal aquaculture farm. All three species received an ambient of low pH treatment prior to a freezing treatment. The authors find species differences in freeze tolerance in mussels, with intertidal M. galloprovincialis showing the least freeze tolerance. The authors go a step further and do a comprehensive assessment of the metabolic capacity and molecular components with analyses of amino acids, fatty acids, and osmolytes and anaerobic byproducts.
The authors hypothesized metabolic changes due to OA and cold temperatures, yet they demonstrated a significant amount of stasis with high similarity among species at the molecular level. The fatty acids in the intertidal M trossulus, the most freeze tolerant, did not change. Further, there is little explanation of molecular/metabolic changes that could explain their results. Because of this somewhat unexpected lack of signal of these stressors, I would like to see an enhanced explanation of animal homeostasis. The authors mention previous results relating to heat stress, and I thought it would be beneficial to discuss how the lack of a molecular response to freezing is related to the strong responses seen in heat stress.
The idea that species in fluctuating environments (here, the intertidal) might respond differently to those in constant environments (here, the subtidal) has been explored in multiple systems. These general concepts could be elaborated on more in the paper to increase the connection to other studies.
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