Reply on RC2

This research provides a detailed physical and biogeochemical characterization of a semienclosed coral reef lagoon in New Caledonia, remarkable for the presence of a diverse and healthy coral reef ecosystem. The authors carried out systematic sampling over a three years period, accomplishing the local characterization of diel and seasonal fluctuations. This work is definitively a valuable contribution to baseline knowledge of environmental conditions in natural laboratories, which can greatly contribute to shed light on the drivers of the biological responses of local organisms. Nevertheless, I have to draw the attention of the authors in two issues. The first one was already addressed by Referee1 (RC1) and I fully agree with RC1 that this site can’t be claimed as a natural analogue to future climate change conditions. However, since RC1 already provided a detailed argumentation on this regard, my comment about this will be very general. The second issue I must comment on, is the claim that local adaptation of these coral species could hold new hope for the future of coral reefs in general. I explain my position in detail in the “Specific comments” section.

This research provides a detailed physical and biogeochemical characterization of a semienclosed coral reef lagoon in New Caledonia, remarkable for the presence of a diverse and healthy coral reef ecosystem. The authors carried out systematic sampling over a three years period, accomplishing the local characterization of diel and seasonal fluctuations. This work is definitively a valuable contribution to baseline knowledge of environmental conditions in natural laboratories, which can greatly contribute to shed light on the drivers of the biological responses of local organisms. Nevertheless, I have to draw the attention of the authors in two issues. The first one was already addressed by Referee1 (RC1) and I fully agree with RC1 that this site can't be claimed as a natural analogue to future climate change conditions. However, since RC1 already provided a detailed argumentation on this regard, my comment about this will be very general. The second issue I must comment on, is the claim that local adaptation of these coral species could hold new hope for the future of coral reefs in general. I explain my position in detail in the "Specific comments" section.
Response: We thank Rev. #2 for recognising our study as a valuable contribution toward a better understanding of organisms' response to extreme environmental conditions. We fully agree that it was inappropriate to define our natural laboratory as a natural analogue for future conditions (natural analogues do not exist). We partially agree that local adaptation (if any) of the local corals could not hold new hope for the future (see below). While we agree and we thanks Rev. #2, it is important to note that our study aimed to describe the environmental fluctuations and give an extensive description of this unique natural laboratory. We certainly speculated on its potential use to address coral response to climate change, but this has only been evoked a few times throughout the ms.

SPECIFIC COMMENTS (individual scientific questions/issues)
-In general terms, the overall text could benefit from a better synthesis of ideas.

Response:
We revised the whole ms, and we thank both Rev. #1 and #2's comments. We have better organised our ideas about the relevance of this site to study the response of corals to environmental change.
-Along all the manuscript, it's advice to use "extreme environmental conditions" instead of "climate change-like conditions".

Response:
We changed it, also accordingly to Rev. #1.
-I fully agree that coral reefs growing on extreme environments are remarkable and perfect natural laboratories to study local adaptation. However, I disagree with the idea of using these ecosystems to predict the general response of coral reefs under future projected changes, as the rate of change is totally different (different time scales). The fact that some coral species currently thrive in extreme environments (such as volcanic CO vents, semi-enclosed lagoons and mangrove estuaries) resulted from an extensive period of exposition to these particular conditions, therefore adaptation. This is not the case under future projections, where the exposition time will be considerably shorter and it is very likely that coral species growing on "more stable" environments (other than volcanic CO vents, semi-enclosed lagoons and mangrove estuaries) won't be able to adapt to this rate of change. And even if they do, probably it would be due to acclimation but not necessarily adaptation.
Response: Respectfully, we believe that adaptation in corals might be much faster than previously thought. Coral adaptation is a timely and debated field of research and we recognise that pieces of evidence are scant. However, microbiome's role in the coral host adaptation (e.g., Voolstra and Ziegler 2020, BioEssays) have been already largely demonstrated. Several studies showed that plasticity in some physiological traits might be heritable and help corals cope with the rapid environmental change (e.g., Donelson et al. We agree that corals in Bouraké have been exposed for a long period (i.e., certainly > 80 y) to similar conditions and such long exposure might allow them eventually to adapt (which would be great). However, it is not so simply since Bouraké is an open system and larvae can come from outside, where the conditions are at ambient level. It is always tricky to affirm if they have adapted through a multi-generation selection or acclimated just within a generation. We will never be able to correctly test the effect of climate change until we find a natural magic lab that started ca. 100 y ago gradually, but fast as projected, to change in at least the main environmental parameters. With such magic lab, and with the certainty that larvae from surrounding normal conditions do not set into this site, we would be able to affirm that corals can adapt (or acclimate, and this would be even better than an adaptation) to climate change.
All this said and taking into account a recent publication regarding persistence of coral reefs under future ocean acidification and warming conditions (Cornwall et al. 2021, PNAS), I disagree with the authors (lines 16-17) when they state that the sole presence of "diverse and high cover reefs that already thrive under extreme conditions" contradict the projections of coral reefs disappearing under the CO2 business-as-usual scenario.
Response: We used this sentence once, in the abstract. We wrote: "..seems to contradict these projections" and respectfully is not wrong when looking to the extreme conditions where they live. However, we smoothed this sentence in: "However, recent discoveries of diverse and high cover reefs that already thrive under extreme conditions seem to suggest that some corals might be able to thrive well under hot, high pCO 2 and deoxygenated seawater". With regard to the recent awesome study by Cornwall, Comeau et al. (2021), their models on existing data from lab and field-based experiments to real reef showed that future climatic projections would cause the decline of coral reef, mostly due to the reduced coral cover due to bleaching event and subsequent mortality. What this study does not consider (because the lack of robust evidence) is the ability to rapidly adapt to climate change. This study assumes that "The fast rate of environmental change relative to the time required for adaptation suggests it will be difficult for corals to maintain their current role, especially those with longer generation times". Respectfully, this does not take into account recent findings on the potential ability of corals to adapt rapidly. We understood, thanks to the Reviewers' comments that we were wrong saying that our results can be used as a model to study future response to climate change, and we changed the ms accordingly.
Even if you bear to consider these special sites as future analogues to future conditions, you must keep in mind that these coral species with high diversity and coral cover are thriving because they were able to adapt to these local environmental conditions over a long time scale. Therefore, they won't be a good worldwide model to "explore how reefs could keep pace with climate change" (lines 19-20). The way as I see it, you are dealing with two different issues: in one hand you have the physical location per se (site), which could be a great natural scenario to explore how coral species would respond to future-like conditions, by transplanting coral species from other "stable" locations. And on the other hand, you can study the adaptation of the local coral species currently living on these natural laboratories. But you can't extrapolate the response of all coral reefs to future conditions by using these local "super corals" broad as models.
Response: We agree that this unique site (as all unique areas found so far) is not an analogue to future conditions. We also agree that corals at such natural laboratories are not an excellent worldwide model to explore how reefs could keep pace with climate change. It currently seems to be a normal practice in the literature to extrapolate the response of coral reefs worldwide from a single site, mechanisms, species or general findings (examples could be numerous). We made our best to avoid such speculation in the revised ms. Many thanks to the Reviewers. About the experiments suggested, both are underway.
Based on their results, the authors can definitively draw a future projection for the Bouraké coral reefs. But they must be cautious and restrain themselves from extrapolating these conclusions to coral reefs in general (L818-819).

Response:
The sentence of conclusions said: "It was beyond the scope of this already multidisciplinary study to assess the contribution of environmental variability and nutrient imbalance to the organism' stress tolerance under extreme conditions. However, both coexist in the Bouraké lagoon, and we believe there is evidence of their contribution to the survival of organisms to future-like environmental conditions. Our study provides evidence that this is possible in nature, giving a glimmer of hope for the future of coral reefs." This sentence is correct and does not speculate over the future of coral reefs worldwide. At the same time, we agree to change future-like env. conditions with extreme env. Conditions. We prefer to maintain this sentence as it is, since we showed that survival is possible under extreme conditions, and this definitely gives a glimmer (not the certitude) of hope for the future of coral reefs. This study, as we mentioned, was not designed to investigate the mechanisms that allow organisms to survive in Bouraké, but what if we will demonstrate that they are not adapted and that their resistance is only physiological? Or that their microbiome itself allows them to survive? We see it as hope.
Additionally, precaution must be taken when drawing conclusions for these potential refuges (lines 98-99). It's true that these coral species can cope with a great environmental variability and thrive under extreme conditions. However, this not necessarily means that they will survive under future changes, as it's also possible that they are already living close to their environmental threshold and future conditions might push them beyond it (see Sánchez-Noguera et al. 2018, Biogeosciences). For example, this site already presents low-pH conditions as expected under climate change projections, but it's very likely that the pH values will continue decreasing in the future due to buffer capacity (TA) of its waters. Therefore, despite these corals thrive under current low-pH conditions, probably they will experience lower pH values (or "harsh conditions" as the authors state in L799-801) as CO2 uptake continues.

Response:
The Reviewer is right. We removed this pure speculation from the ms. Many thanks.

Material and methods
Glass electrodes (as the one from the Metrohm pHmeter and the SeaFET) are not very accurate and it's valuable that the authors carried out a calibration with TRIS buffer. Nevertheless, on top of the TRIS calibration, it's strongly advised that the authors validate their surface pH measurements with pH values calculated from TA and DIC samples.

Response:
We are a bit confused. We are quite sure that the SeaFET does not use glass electrodes but a new generation of electrode (ISFET, Martz et al. 2010, Limnology and Oceanography Methods). This kind of electrode reads stable and accurate pH even during long-term deployments (i.e., the effect of biofouling) and without an additional calibration (Bresnahan et al. 2014, Methods in Oceanography). Among the three SeaFET we used (L140) "Two SeaFETs were calibrated by the manufacturer, while the third was corrected before deployment by measuring its deviation from the two others in the same seawater." Likely, it would always be a best practice to check values also using another method such as the spectrophotometer technique, but if we consider the large variation in pH measured at the site, even if our measurements have a 0.05 pH error, results do not change. Concerning the seawater pH measurements, we did during the diel cycles in 2017 and 2019, and the use of a glass electrode coupled with a Metrohm pHMeter. We thought that having the Rolls Royce of the Metrohm electrodes (>1,000 euro the probe) and Tris calibration was enough as a guarantee of high accuracy. Our data did not differ from the range already measured in Camp et al. (2017, Scientific reports) for the same stations.
As suggested, we re-calculated pH with the Seacarb R package using TA, DIC, temperature, and a mean salinity of 35 since we did not measure it in parallel with the other parameters. Surprisingly, our results were consistently different from one we measured using the Metrohm probe and definitely far from reality. While at the control, where we should expect a typical ambient seawater pH, only few data were close to pH 8, and most of them around 7.7-7.8, at Bouraké pH was a couple of times 8.3 (too high) and down to 6.8 (too low). These differences could be due to several factors. Firstly, accurately measuring DIC and TA is not so easy, from the sample collection, through the sample preservation, and to its measurement. While we are pretty sure about the TA measurement since we used accurate standards, the DIC samples had to be sent overseas in France to be measured. In addition, we did not measure salinity, which might affect the recalculation of pH. This can affect the calculation. Secondly, another unexplored source of incertitude could be the chemical of the seawater in Bouraké, with high organic content, which could change the seawater carbonate chemistry, but this should not affect the control. We are terribly sorry we could not be able to validate our measurements using a different calculation as suggested. However, SeaFET loggers are accurate instruments worldwide validated. These data perfectly validated the pH measurements we made using an accurate glass electrode, calibrated using Dickson tris buffers. All these data are in agreement with data already presented for the same stations by Camp et al. (2017).