Ocean acidification increases the sensitivity of and variability in physiological responses of an intertidal limpet to thermal stress

Wang, Jie; Russell, Bayden D.; Ding, Meng-Wen; Dong, Yun-Wei

doi:https://doi.org/10.5194/bg-15-2803-2018

Articles | Volume 15, issue 9

https://doi.org/10.5194/bg-15-2803-2018

© Author(s) 2018. This work is distributed under
the Creative Commons Attribution 3.0 License.

https://doi.org/10.5194/bg-15-2803-2018

© Author(s) 2018. This work is distributed under
the Creative Commons Attribution 3.0 License.

Articles | Volume 15, issue 9

Research article

|

09 May 2018

Research article |

| 09 May 2018

Ocean acidification increases the sensitivity of and variability in physiological responses of an intertidal limpet to thermal stress

Jie Wang, Bayden D. Russell, Meng-Wen Ding, and Yun-Wei Dong

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Final revised paper (published on 09 May 2018)
Preprint (discussion started on 07 Mar 2017)

Interactive discussion

Status: closed

AC: Author comment | RC: Referee comment | SC: Short comment | EC: Editor comment

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- Supplement

RC1: 'Review of Wang et al.', Maria Byrne, 10 May 2017
- AC1: 'Responses to comments of M. Byrne (Referee) on “Ocean acidification increases the sensitivity and variability of physiological responses of an intertidal limpet to thermal stress”', Yunwei Dong, 02 Jul 2017
RC2: 'MS No.: bg-2017-47', Anonymous Referee #2, 31 May 2017
- AC2: 'Responses to comments of anonymous referee #2 “Ocean acidification increases the sensitivity and variability of physiological responses of an intertidal limpet to thermal stress”', Yunwei Dong, 02 Jul 2017

Peer-review completion

AR: Author's response | RR: Referee report | ED: Editor decision

ED: Reconsider after major revisions (05 Jul 2017) by Carol Robinson

AR by Yunwei Dong on behalf of the Authors (13 Aug 2017) Author's response Manuscript

ED: Referee Nomination & Report Request started (25 Aug 2017) by Carol Robinson

RR by Maria Byrne (11 Sep 2017)

Suggestions for revision or reasons for rejection

This manuscript by Wang et al is an interesting study of the impact of climate change stressors on limpets. Several aspects still to be revised. For instance the significance of doing both the inducible and constitutive forms of HSP needs to be explained in the introduction. Most readers will not appreciate the difference in the two HSPs and what to expect with regard to their expression. What have other studies found? Interestingly the ramping method to assess HSP inducible is different from other more typical 1 hr shock, 1 hr recovery ‘heat shock’ studies. From a comparative perspective this is important to consider in the discussion.

I think the authors may have under sold their work. I do not think that heart beat and both HSPs have been investigated previously as combined response variables in warming-acidification studies. The authors should clearly state what is novel about this study.

I am concerned that the experimental design is psuedoreplicated.

Title and overall interpretations need some consideration (see below)
- increasing sensitivity - is this a good or a bad thing?
- The variability increases but I do not know what can be said about this because all the limpets per treatment were housed together in one tank and so were competing in a lab environment. This may have influence the outcome.
- The limpets may have been collected from different microclimates. This would influence the outcome.

In essence - these considerations and potential caveats need to be presented and identify potential limitations of what can be said.

Abstract
I am not convinced that the authors have demonstrated physiological plasticity. To identify this every animal would have to be treated exactly the same, but if they were in the same tank inter-individual interactions may have influence outcome.
Individuals from the same population - state from where and that they are intertidal.
Context at lines 107 and 111 need to be added to the abstract - i.e. treatments - what are the control treatments and what based on (e.g. annual mean, temperature at time of collection etc). Where the limpets collected from exactly the same level on the shore and the same aspect wrt to insolation?
Let the reader know that both the inducible and constitutive forms of HSP were investigated …and to address for what aspect each are useful/or why used.
I do not understand “better to cope physiologically”.
Also provide pH levels in the abstract. Because local TA can differ regionally the levels of ppm used are not easy to compare between studies.

Introduction
L. 43 - better to replace “acidity” with “decreased pH” - as per Gatusso’s paper on how OA should be presented.
L. 56 replace “climate change” with “increased temperate” so the reader understands the focus.
L. 61 - correct the Gibson reference - this is the editor of the volume not the author of the paper!
The main response variables are heart rate, hspc and hspi. All of these and their use as indicators should be introduced. It will suffice to say that heart beat is often used with molluscs in stress studies (REF). Does an increase in heart rate indicate the animal is coping or is in stress - i.e. what does heart rate measures indicate (with refs). Similarly the two HSP markers need to be introduced. How do these differ? Why do both? Cite a few previous studies. One of he autjors, Dr Dong has done great research on HSPs and so will be able to address this. Is this the first study to combine these physiological markers with heart rate? Here the authors can clearly state what is novel about this study.

L. 85 how did the authors measure plasticity - was this based on CV?? If so state this here and justify with refs>

Methods
The animals are from fluctuating habitats (e.g. L. 51,77) but the treatments are static. I understand that it is difficult to mimic intertidal flux conditions in the lab, but the fact that the experimental conditions used do not reflect the natural conditions needs to be acknowledged and some justification of the approach stated - perhaps add ‘potential’ insights?

We are told what the habitat temperature is. What is the range of the habitat pCO2?
L. 64 - microclimate is mentioned - indeed this is very important. For instance the Lathlean papers (infra red studies) and others show that depending on aspect of the habitat rocks to the sun and even rock colours, that limpets and other intertidal invertebrates have very different thermal environments. The reader needs to be assured that the experimental animals had a similar thermal history and cite some of these studies.

As I read the design - 100 limpets were maintained in a single container per acclimation treatment. This is pseudoreplication. The authors must acknowledge this. L. 125 - were randomly selected - that helps … potentially to get around pseudo rep??/

However the ramping was done on an individual basis.

L 177 This is confusing and may be due to English. What does “stands for” mean. It is important that the definition is clear.
L. 179 replace “is seen” … perhaps with “was determined”?
ABT - I suggest spell out each use eg. L. 209

Results
L 208 and 219 “indicating ….” This is discussion text - delete from results.

Discussion
L. 242,254 - what is the bottom line - is sensitivity a good or bad outcome? What is the take home? Move up sentence L. 245 and 271-272. We need to understand what does change in sensitivity mean for the prospects of the limpets in the future.

L. 251 - Does this indicate a synergistic negative effect?

The HSP text is confusing - let the reader know that one paragraph is on the inducible and the other is on the constitutive forms AND the significance of these - with citations.

Para starting L. 295. Could the “variation” (based on CV) interpreted here as “plasticity” be due to variable environmental history not still present despite a 7 day acclimation. This needs to be considered here. A longer acclimation time would be needed. Also plasticity is reversible. Essentially speak to the data and potential caveats.

The caveat of flux (natural) -vs- stable (exp) needs to be stated.

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RR by Anonymous Referee #3 (16 Oct 2017)

ED: Reconsider after major revisions (02 Nov 2017) by Carol Robinson

AR by Yunwei Dong on behalf of the Authors (04 Dec 2017) Author's response Manuscript

ED: Referee Nomination & Report Request started (14 Dec 2017) by Carol Robinson

RR by Stephen J. Hawkins (08 Mar 2018)

Suggestions for revision or reasons for rejection

This is an interesting paper that deserves a wide audience. The authors have dealt well with the comments of the previous referees. My comments are minor to enhance readability, clarity and rectify some typos ( the last author has not done a good job here in checking the English/proofing before submission).

General Comments

This is a very general readership journal. At first mention in the introduction clearly explain what "constitutive" means (perhaps in a bracket).

Specific Comments by line
Abstract
31 "showed increased sensitivity" is better
34 replace "acidic" with "reduced pH" - the pHs are above 7 - therefore alkaline...
Introduction
50 "resistance of an organism (try to avoid apostrophes with the possessive)
53 I would contend these are "responses" not "options". Options implies conscious choice.
Sessile and sedentary organisms do not "shift their ranges" - their ranges shifts as individuals occur in different places. Highly mobile species may actually shift their ranges but not limpets. This sloppy wording (and I have done it too) permeates the climate change literature - species do not consciously shift their ranges - their ranges shift.

Suggested rephrase: Organisms can respond in three ways: exhibit shifts in distributional ranges (...), evolve adaptive changes (), or perish ().

80 not a huge amount of space is saved by abbreviating Heart Rate - in full throughout? (I would not like confusion with Human Resources...)
83 ...... Breakpoint Temperature - start with capitals as a term.
100 ecosystems
104 rephrase - do you mean "subtropical high pressure systems" ???
107 from what pH to what pH
116 "show increased..."
118 "Our study, by measuring both heart rate and heatshock proteins,..."
Methods
126 "ensured" not ensure and delete "is to"
136,155 field not filed and check throughout.
187 "the foot muscle..."
247 - far too much code - in full at first mention for the different treatments to help the reader.
276 ...condition: .... (replace comma with colon)
Discussion
301 Spend not cost
302 Somero not Semero
355 combining not combing
358 "the response of an organism..."
Table A1 could go in the main text near the methods - this is important information.
Figure 1A - it would be good to fit individual light lines for each individual limpet as well as the population average - this shows the individual variability and hence plasticity at the heart of the paper.

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ED: Publish subject to minor revisions (review by editor) (12 Apr 2018) by Carol Robinson

AR by Yunwei Dong on behalf of the Authors (14 Apr 2018) Author's response Manuscript

ED: Publish as is (22 Apr 2018) by Carol Robinson

AR by Yunwei Dong on behalf of the Authors (23 Apr 2018)

Short summary

To understand ecological impacts of CO₂-induced ocean acidification and temperature rise, a key question is if organisms become more vulnerable under multiple stressors. Here we tested heart rate and gene expression levels of a limpet under varying pCO₂ and temperature. Results showed that while many individuals are more vulnerable to heat stress under high CO₂ and increased temperature, some animals have the ability to alter their physiology to help them survive under future conditions.