PONE-D-22-24875Coral Gardens Reef, Belize: An Acropora spp. refugium under threat in a warming worldPLOS ONE

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Additional Editor Comments:

I received two sets of reviews that identify some issues with the manuscript. Both reviewers agreed that the manuscript was of great value, however one reviewer did notice an issue with the calculation of DHWs. I agree with them on this point and suggest that you look at using a more relevant climatology for calculating MMM. This may change some of your results and interpretation, so I've suggested major revision.

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Reviewers' comments:

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Reviewer #1: Yes

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

Reviewer #1: No

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Reviewer #1: No

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Reviewer #1: Yes

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5. Review Comments to the Author

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Reviewer #1: This manuscript describes an assessment of threats to one of the largest remaining healthy Acropora cervicornis patches in the Caribbean. Previous work by the lead author has identified this field site as a refugium of Acropora spp. and this paper expands that work with many years of intensive field monitoring and a variety of types of ancillary data to analyze the potential stability of the refugium. The manuscript is clearly written and generally a valuable contribution to the field. It is important for future conservation of endangered species to recognize refugia and recognize the potential threats that could destroy them and the species they protect.

In my review submission, I indicate that the data are not available because I could not find a supplement and the data were not all in the manuscript. There were summary tables in the text, but not all of the raw data. I would have expected a table of daily and monthly temperature data, as well as all of the live coral abundance data for each transect, the pH data, the substrate composition data, sediment size and composition data, canopy height, sediment thickness and depth to hardground, urchin counts, and damselfish survey data.

I have one main concern with the analysis as it is written. The authors use the concept of degree heating weeks, which has been used for many years to quantify coral bleaching risk. However, the calculations described in the present text indicate incorrect application of the concept, according to my understanding. The issue is that DHW is supposed to be relative to the mean maximum monthly temperature (MMM) during a base period when bleaching was not common. Using the monthly data for each year during the study period, 2012-2020, implicitly assumes instantaneous adaptation of coral populations to current warming trends, which is a bad assumption. NOAA coral reef watch, which has popularized this metric uses a base period of 1985–1990+1993 for historic reasons (see Heron et al 2015). I recommend using the same base period.

I understand that a problem with the 1980s-1990s base period is that you don’t have local in-situ data as you do for the 2012-2020 period. However global gridded SST products are widely available and often track local reef temperatures fairly well (Winter et al, 1998). A calibration of the monthly in-situ data with gridded data during the period of common data (as in Smith et al., 2006) will permit you to adjust the available gridded temperature to better match the expected larger variance of a local record during the earlier base period. I think this is will be a much better estimate of MMM against which to calculate DHW.

Another potential issue with the DHW concept as applied is that recent work (Lachs et al, 2021) indicates that a lower threshold of MMM+0 for 8 weeks duration may better capture thermal stress in corals. I am ambivalent about the need to use this lowered threshold as I agree with Lachs et al., 2021 that spatial variations in coral response are likely significant. However, I think you will find that by using a more reasonable base period for the climatological MMM, you will have substantially more accumulation of DHW during the course of the study, especially 2016.

Some specific comments for small corrections and a list of the references cited above follow.

SPECIFIC COMMENTS

Line 117 The description “high resolution” is very unclear for multiple reasons. Is the resolution over space or time, and how high is “high”? The compound adverb (which needs to be written “high-resolution” to be correct) describes the calculations, but I don’t think the calculations had high resolution, instead I think the spatial data used for the calculations were of cm-scale resolution. To a microscopy specialist, cm-scale is exceedingly low resolution. Further the syntax using “high-resolution” first makes a reader wonder if all the data in the list is “high-resolution”, or if the authors are only referring to the calculations of live coral cover.

Line 119. I would argue that all of the data in this list are observational data. Perhaps the authors mean “personal observations” of conditions at the site over the years.

Figure 1: This figure would be easier to see as a two-panel figure. The inset map is very small and highly detailed, yet the base map has little fine detail and is rather large. They would both be more appropriately sized if they were equal and side-by-side.

Figure 2: the caption describes a m2 quadrat, but I think this would be better described as a 1 m2 quadrat. Additionally, the caption describes the coral image traced with Adobe Photoshop, but in the text, Adobe Illustrator is attributed. This should be consistent.

REFERENCES

Heron, S.F.; Liu, G.; Eakin, C.M.; Skirving, W.J.; Muller-Karger, F.E.; Vera-Rodriguez, M.; de la Cour, J.L.; Burgess, T.F.R.; Strong, A.E. ; Geiger, E.F.; et al. Climatology Development for NOAA Coral Reef Watch’s 5-km Product Suite, NOAA Technical Report; NESDIS: Silver Spring, MD, USA, 2015; Volume 145.

Lachs, L.; Bythell, J.C; East, H.K; Edwards, A.J; Mumby, P.J; Skirving, W.J; Spady, B.L; Guest, J.R. Fine-Tuning Heat Stress Algorithms to Optimise Global Predictions of Mass Coral Bleaching. Remote Sens. 2021, 13, 2677. https://doi.org/10.3390/rs13142677

Smith, J. M., Quinn, T. M., Helmle, K. P., and Halley, R. B. (2006), Reproducibility of geochemical and climatic signals in the Atlantic coral Montastraea faveolata, Paleoceanography, 21, PA1010, doi:10.1029/2005PA001187.

A. Winter, R. S. Appeldoorn, A. Bruckner, E. H. Williams. Jr., C. Goenaga, Sea surface temperatures and coral reef bleaching off La Parguera, Puerto Rico (northeastern Caribbean Sea). Coral Reefs (1998) 17 : 377-382.

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Reviewer #1: No

Reviewer #2:

See attached PDF of paper - see comments in drop down tabs

Summary

1.  accept manuscript with revision

2.  limitation of study - one field visit (snapshot) per year - hard to infer causality for the intervening 11 months  Need to discuss this limitation

3.  No repeated measures of coral colonies during period of loss (mortality) -

4.  Can only guess as to the cause of mortality ???

5.  Agree that temperature is likely proximal driver of ACER loss

6.  Personal observation to my one visit to site = There is also a minor level of background WBD at Coral Gardens (~1%) - this could have jumped as temperatures reached their maximum in late summer /early fall causing a localized but temporally limited mortality event.

see the attached references

Randall, C.J. and van Woesik, R., 2015. Contemporary white-band disease in Caribbean corals driven by climate change. Nature Climate Change, 5(4), pp.375-379.

Gignoux-Wolfsohn, S.A., Precht, W.F., Peters, E.C., Gintert, B.E. and Kaufman, L.S., 2020. Ecology, histopathology, and microbial ecology of a white-band disease outbreak in the threatened staghorn coral Acropora cervicornis. Diseases of Aquatic Organisms, 137(3), pp.217-237.

7.  Just as easy to infer that disease/bleaching was as important as passage of hurricane

8.  Hurricane wave stress plus temperature stress may have led to shut down reaction (speculation on my part - but possible)

see SDR

Antonius, A., 1977. Coral mortality in reef: a problem for science and management. In: Proc. 3rd Int. Coral. Reef. Symp, 2, pp. 618–623.

9.  Manuscript is well written, stats ok, good use of references

10.  Broad implication for linking of climate change science with coral loss

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Coral Gardens Reef, Belize: An Acropora spp. refugium under threat in a warming world

PONE-D-22-24875R1

Dear Dr. Greer,

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