PCLM-D-21-00002One Hundred and Fifty Years of Warming on Caribbean Coral Reefs

PLOS Climate

Dear Dr. Bove,

Thank you for submitting your manuscript to PLOS Climate. After careful consideration, we feel that it has merit but does not fully meet PLOS Climate’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

After the reviewers' independent assessment and my own reading, we request you to make revisions to your manuscript. You will see in particular that the two reviewers are all positive about the quality of the manuscript and agree on the merits of your work but ask additional clarifications on the methodological section, highlight some points that deserve further discussion in the manuscript, and suggest many ways to improve the readability of the manuscript.

Please submit your revised manuscript by Sep 11 2021 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at climate@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pclm/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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We look forward to receiving your revised manuscript.

Kind regards,

Andrea Storto

Academic Editor

PLOS Climate

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Does this manuscript meet PLOS Climate’s publication criteria? Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe methodologically and ethically rigorous research with conclusions that are appropriately drawn based on the data presented.

Reviewer #1: Yes

Reviewer #2: Partly

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: I don't know

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3. Have the authors made all data underlying the findings in their manuscript fully available (please refer to the Data Availability Statement at the start of the manuscript PDF file)?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception. The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

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4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS Climate does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: General comments

The work offers a complete analysis of the SST in the wider Caribbean; it has interesting results that contribute to the description of the variation in ocean warming in the marine ecosystems of the region.

The methods are adequate, although the temporal autocorrelation of the residuals obtained from the statistical models used need to be answered. The quantitative approximations used are robust, but it is necessary to review the temporal autocorrelation of the residuals of the generalized and linear models used. In case of observing a high temporal autocorrelation, it would be necessary to use methods that allow to consider it, for example, to include the AR1 function in the generalized or linear models. It is very interesting to see that complementary databases are used, which allowed the authors to have a broader perspective on temporal variation. However, it is important to mention what are the disadvantages of these databases and how they are statistically related. What is the correlation between the databases in the region?

The figures and tables seem adequate. Results show a good presentation, and they are in the right order, but it is necessary to include an analysis of the relationship between the databases compared and to include these results in the manuscript. Discussion have the necessary and pertinent information, but I think it lacks in some important points: 1) in some results there is brief discussion of the progress made in other works done before this manuscript, it is necessary to include a better comparison of the results obtained in this work with others that have used other metrics such as DHW or TSA; 2) MHW are assumed as the best metric to predict the impact on coral reefs. This is exaggerated and incorrect; it is necessary to have a more objective discussion that includes the mention of the different metrics of heat stress, citing works that evaluate multiple metrics and not only MHW.

Specific comments

Line 17:

“especially on coral reefs of the Caribbean” is not accurate. The evidence of heat stress and temperature increase in the world’s reefs shows that the Caribbean is one of the areas with the highest exposure, but it is not especially the region with the highest warming. Just “especially on coral reefs” would make the sentence more accurate.

Line 31

It seems to me that it is also important to include the duration of the MHW events, this would give a clearer context of the results and the importance for coral reefs.

Lines 137 to 139

In the case of the slope of the regression model at the pixel level, a justification is needed for not using a method that allows the inclusion of temporal autocorrelation. Also, it is necessary to mention why a “Normal” or linear distribution is assumed.

Lines 187 to 196

Same comment as the previous part. It is necessary to check the assumptions of temporal autocorrelation and the residuals of the OLS and GLM models. It is mentioned that the data were transformed, but there is no mention that, if the assumptions were met, nor the test that was used to check them. I recommend that if you use R, you could do the gvlma test (with the library of the same name) to check the assumptions of the models. I understand that for pixel-level analysis this test is not practical, but for temporal variation it would be appropriate to perform them.

Line 200 to 202

In graph 2A, it is not clear the overlap of spring temperature with exceed annual highs (September) observed in the late 19th century.

Lines 205 to 208

It would be interesting to do a correlation analysis and a qqplot to see how these databases are related. The difference between databases deserves a discussion of the repercussion of using two different data and how this may influence the estimates. Throughout the manuscript, the results of the two databases are mentioned, but the differences in the estimates between the databases need to be discussed at the beginning.

Lines 252 to 255

These results are very interesting. The results are fundamental for the identification of temporal change points in thermal stress and ocean warming, which can give us information about thermal regimes and the changes over a long period. However, other papers that have similar previous analyses are not considered. Also, must discuss what may be the large-scale patterns (AMO, ENSO, NAO, etc.) that may influence the identified change points.

I recommend these papers to expand the discussion on these points.

Heron, S.F., Maynard, J.A., van Hooidonk, R., Eakin, C.M., 2016. Warming Trends and Bleaching Stress of the World’s Coral Reefs 1985–2012. Sci. Rep. 6, 38402. https://doi.org/10.1038/srep38402

Lough, J.M., Anderson, K.D., Hughes, T.P., 2018. Increasing thermal stress for tropical coral reefs: 1871–2017. Sci. Rep. 8, 6079. https://doi.org/10.1038/s41598-018-24530-9

Donner, S.D., Knutson, T.R., Oppenheimer, M., 2007. Model-based assessment of the role of human-induced climate change in the 2005 Caribbean coral bleaching event. Proc. Natl. Acad. Sci. 104, 5483–5488. https://doi.org/10.1073/pnas.0610122104

Muñiz-Castillo, A.I., Rivera-Sosa, A., Chollet, I., Eakin, C.M., Chollett, I., Eakin, C.M., Andrade-Gómez, L., McField, M., Arias-González, J.E., 2019. Three decades of heat stress exposure in Caribbean coral reefs: a new regional delineation to enhance conservation. Sci. Rep. 9, 11013. https://doi.org/10.1038/s41598-019-47307-0

Line 252 to 261

There is a lack of discussion of temperature variation among ecoregions. For example, the Gulf of Mexico has an extensive range of variations compared to the Southwestern Caribbean. What implications might this have for the conservation of the different ecoregions?

Lines 329 to 335

This part is biased. I recognize the importance that MHW can have as an excellent indicator of acute heat stress, which can be an important driver of coral bleaching. However, there is little published evidence of the usefulness of MHW as a predictor of coral bleaching, so to say that this metric expresses (because in the end, it is only one of many heat stress metrics that exist) the major cause of massive coral mortality is an oversight. In the work proposed by the authors, the importance of MHW as a predictor of heat stress is assumed, but coral bleaching is not tested, so it seems to be incorrect to make these assertions. It is valid and necessary to discuss the importance, advantages, and disadvantages of using MHW as an indicator of heat stress in coral reefs, but this discussion needs to be more documented and comprehensive. I recommend reviewing these articles and discussing how MHW enter the predictive framework of coral bleaching, here can be further nurtured by including the discussion about various metrics that are known today, including the MHW.

McClanahan, T.R., Darling, E.S., Maina, J.M., Muthiga, N.A., ’agata, S.D., Jupiter, S.D., Arthur, R., Wilson, S.K., Mangubhai, S., Nand, Y., Ussi, A.M., Humphries, A.T., Patankar, V.J., Guillaume, M.M.M., Keith, S.A., Shedrawi, G., Julius, P., Grimsditch, G., Ndagala, J., Leblond, J., 2019. Temperature patterns and mechanisms influencing coral bleaching during the 2016 El Niño. Nat. Clim. Chang. 9, 845–851. https://doi.org/10.1038/s41558-019-0576-8

Muñiz-Castillo, A.I., Arias-González, J.E., 2021. Drivers of coral bleaching in a Marine Protected Area of the Southern Gulf of Mexico during the 2015 event. Mar. Pollut. Bull. 166. https://doi.org/10.1016/j.marpolbul.2021.112256

Safaie, A., Silbiger, N.J., McClanahan, T.R., Pawlak, G., Barshis, D.J., Hench, J.L., Rogers, J.S., Williams, G.J., Davis, K.A., 2018. High frequency temperature variability reduces the risk of coral bleaching. Nat. Commun. 9, 1671. https://doi.org/10.1038/s41467-018-04074-2

Sully, S., Burkepile, D.E., Donovan, M.K., Hodgson, G., van Woesik, R., 2019. A global analysis of coral bleaching over the past two decades. Nat. Commun. 10, 1264. https://doi.org/10.1038/s41467-019-09238-2

Somewhere in the discussion, the differences in the spatial and temporal patterns obtained from the use of MHW and other metrics used in the region, for example, DHW and TSA, should be mentioned, I recommend reviewing these works and discuss the differences in the variation of heat stress.

Selig, E. R., Casey, K. S. y Bruno, J. F. (2010) “New insights into global patterns of ocean temperature anomalies: Implications for coral reef health and management”, Global Ecology and Biogeography, 19(3), pp. 397–411. doi: 10.1111/j.1466-8238.2009.00522.x.

Muñiz-Castillo, A.I., Arias-González, J.E., 2021. Drivers of coral bleaching in a Marine Protected Area of the Southern Gulf of Mexico during the 2015 event. Mar. Pollut. Bull. 166. https://doi.org/10.1016/j.marpolbul.2021.112256

Heron, S.F., Maynard, J.A., van Hooidonk, R., Eakin, C.M., 2016. Warming Trends and Bleaching Stress of the World’s Coral Reefs 1985–2012. Sci. Rep. 6, 38402. https://doi.org/10.1038/srep38402

Something that it is very interesting is to know why such different results are obtained in the spatial dimension, but similar in the temporal dimension, what repercussions this may have on the use of complementary metrics for conservation strategies in coral reefs.

Lines 346 and 354

This is a simplification of the results and leaves out some of the most important points of the work. It is not only the increase in temperature; it is also the increase in the frequency and duration of heat stress events (MHW). The conclusion must be expanded; it is more interesting to mention the increase in frequency and duration of MHW than the increase in temperature alone.

Reviewer #2: This is an interesting and timely article, and I am happy to recommend publication after the issues outlined in the attached review are addressed. Please see attached review document and annotated ms for details. I would also recommend changing the title of the article to make it more informative.

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Reviewer #1: No

Reviewer #2: No

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PCLM-D-21-00002R1

A century of warming on Caribbean reefs

PLOS Climate

Dear Dr. Bove,

Thank you for submitting your manuscript to PLOS Climate. After careful consideration, we feel that it has merit but does not fully meet PLOS Climate’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

In particular, you will see requests for further discussions and, sometimes, clarifications, from one of the the two reviewers, which I agree with. I recommend you to extend either the Discussion or the Conclusions section accordingly.

Please submit your revised manuscript by Dec 22 2021 11:59PM. Including a Track Change document showing your modifications will help us check that the manuscript is suitable for publication. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at climate@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pclm/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

• A rebuttal letter that responds to each point raised by the editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
• A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
• An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

We look forward to receiving your revised manuscript.

Kind regards,

Andrea Storto

Academic Editor

PLOS Climate

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Additional Editor Comments (if provided):

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: (No Response)

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2. Does this manuscript meet PLOS Climate’s publication criteria? Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe methodologically and ethically rigorous research with conclusions that are appropriately drawn based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

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4. Have the authors made all data underlying the findings in their manuscript fully available (please refer to the Data Availability Statement at the start of the manuscript PDF file)?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception. The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS Climate does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

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6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The manuscript is much improved in abstract, introduction, methods results and discussion. Nevertheless, the manuscript can improve in three aspects:

A better explanation of the difference that exists when three different databases are analyzed is still needed. Researchers would like to know the validity, significance, and disadvantages of using different databases. For example, why did you use OISST for the marine heatwaves and not Pathfinder for the daily data? Also, as shown in Table 1, there are considerable differences in the estimates obtained with the different databases. Still, the table alone does not explain these differences or help the reader understand the results obtained.

Few typos, for example:

Line 46: there is a dot before the references [4,5].

Line 218: 0.17 °C per decade is quoted, but Table 1 says 0.16.

Line 220: 0.19 °C per decade is quoted, but Table 1 says 0.20.

The conclusion needs to be a little clearer and not be biased only to the impact of thermal stress or temperature increase. There have been other causes equally or more critical in the collapse of coral reefs. In addition, here you are talking about a generalized collapse, but with fish, overfishing has caused mainly the collapse of populations. With corals, there are several causes, such as pollution, disease outbreaks, increased coastal development, etc. My recommendation is to be more explicit in this sentence, talk about the other stressors and focus on the synergistic effect and thermal stress and increased temperature. I understand that the work is focused on temperature and climate change as stressors or drivers of change in coral reefs and other marine ecosystems in the Caribbean. Still, I think it is necessary to be more objective in this type of assertion and recognize the relevance of different stressors.

Reviewer #2: Please see attached document with comments and suggestions.

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7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

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For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

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[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

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A century of warming on Caribbean reefs

PCLM-D-21-00002R2

Dear Dr Bove,

We are pleased to inform you that your manuscript 'A century of warming on Caribbean reefs' has been provisionally accepted for publication in PLOS Climate.

Before your manuscript can be formally accepted you will need to complete some formatting changes, which you will receive in a follow up email. A member of our team will be in touch with a set of requests.

Please note that your manuscript will not be scheduled for publication until you have made the required changes, so a swift response is appreciated.

IMPORTANT: The editorial review process is now complete. PLOS will only permit corrections to spelling, formatting or significant scientific errors from this point onwards. Requests for major changes, or any which affect the scientific understanding of your work, will cause delays to the publication date of your manuscript.

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Thank you again for supporting Open Access publishing; we are looking forward to publishing your work in PLOS Climate.

Best regards,

Andrea Storto

Academic Editor

PLOS Climate

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The authors have addressed all the minor points, which mostly concerned some requests for further discussion, and I am then glad to recommand the manuscript for publication.

Reviewer Comments (if any, and for reference):