Outplants of the Threatened Coral Acropora cervicornis Promote Coral Recruitment in a Shallow-Water Coral Reef, Culebra, Puerto Rico

Round 1

Reviewer 1 Report

Need a map: the location, depht, exposure, size and distances between the sites is important and should be shown on a map.

Also an schematic of the sampling design would help and pictures of the quadrats with Acer and with no Acer, at the reference site and of the coral recruits.

There is a problem of pseudo-replication at the site level, you do discuss this and refer to some unpublished data, but it would be great if you could show that the substrate cover of the site and reference site are indeed similar and would not influence recruitment. 

Why didn´t you used the same design in the reference site, i.e. 3 transects with 90 quadrats, 45 quadrats with Acer transplants and 45 quadrats with no transplants? Although in the restored site your quadrats with no transplants received less recruits I wonder if the manipulation of the substrate to fix the transplants could have somehow increased the rugosity of the quadrat and that resulted in more recruits and not the presence of the transplants per se i.e. you lack a procedure control (which I image are small and with poor ramification?). 

In Figure 1: Acerv in the graph vs Acer in the description. Also the difference between non restored and restored (Fig. 1A) is due only by the Acer quadrats at the restored site but if your remove these no difference would be noticiable. 

Author Response

Reply to Comments by Reviewer #1:

First, we would like to thank you for the comments provided. We understand they have significantly improved our manuscript.

Comment 1: Need a map: the location, depth, exposure, size, and distances between the sites are important and should be shown on a map.

Response: We have added a map showing the study area. We also added more information to the description of the study sites, including depth, wave exposure, and distance between locations. See Figure 1. See lines 106-116

            “PMEL is a shallow-water reef, 1 to 5 meters deep, located within the Canal Luis Peña non-take Natural Reserve. The site benefits from calm waters due to its sheltered location, protected by Luis Peña Island, and boasts good water quality [22]”.

Comment 2: Also an schematic of the sampling design would help and pictures of the quadrats with Acer and with no Acer, at the reference site and of the coral recruits.

Response: We have added the recommended pictures of the quadrats as well as the coral recruits. See Fig.2 and Fig. 6

Comment 3: There is a problem of pseudo-replication at the site level, you do discuss this and refer to some unpublished data, but it would be great if you could show that the substrate cover of the site and reference site are indeed similar and would not influence recruitment. 

Response: We have added more information about the benthic composition to better explain the similarities in benthic composition between the localities.  

Lines 217-220:  “Macroalgae can lower coral recruitment rates by limiting the space accessible for the settlement of coral larvae. However, when comparing macroalga cover between coral- and non-coral quadrats, we found that the percent of alga cover, dominated by turf, did not vary statistically between PMEL (46%) and PMEL-Reference (40%)”.

Lines 242-244: “Specifically, the three most prevalent coral species, P. astreoides, P. porites, and S. radians, accounted for a significant portion of the total adult coral species observed at both the restored (62%) and reference locations (100%)”.

Comment 4: Why didn´t you used the same design in the reference site, i.e. 3 transects with 90 quadrats, 45 quadrats with Acer transplants and 45 quadrats with no transplants?

Response: We have added an explanation to explain the spatial difference in sampling units.

Lines 125-127: “The difference in sample size was primarily due to the limited available area at PMEL-Reference, which featured a higher presence of sandy patches. The smaller sample size at PMEL-Reference was deemed appropriate considering the site-specific constraints”.

Comment 5: Although in the restored site your quadrats with no transplants received less recruits I wonder if the manipulation of the substrate to fix the transplants could have somehow increased the rugosity of the quadrat and that resulted in more recruits and not the presence of the transplants per se i.e. you lack a procedure control (which I image are small and with poor ramification?). 

            Response: We understand that the methodology used to fix the corals to the substrate (nail and cable ties) may have a minimal impact on the rugosity of the reef substrate. We have added a sentence to better explain the methodology for coral outplanting. Moreover, control quadrats also have a nail with a numbered tag, see Fig. 2c.

Lines 115-116: “These coral colonies were attached to the substrate using a cost-effective technique involving nails and cable ties (Fig. 2a), chosen for its minimal environmental disruption (i.e., change in substrate rugosity)”.

  Comment 6: In Figure 1: Acerv in the graph vs Acer in the description. Also, the difference between non restored and restored (Fig. 1A) is due only by the Acer quadrats at the restored site but if your remove these no difference would be noticiable. 

      Response:       We agree with the reviewer. We expressed such a pattern in the result section.

            Lines 182-184: “The difference was driven by the positive association between A. cervicornis and coral recruits (Dunn test; p<0.001) because no significant differences were found when comparing quadrats with no coral outplant (Dunn test; p>0.05)”.

Reviewer 2 Report

Line 30   this makes it sound like there are two alternatives, one is outplanting and the other is regaining functionality.  That is surely not what you intend to say.  You want to say that outplanting is designed to help reefs regain functionality, don’t you?

Line 40   what is “examining the immediacy” mean??  Are you saying you recommend outplanting A. cervicornis to restore coral recruitment?

Line 47  The #1 reference, however, is based on very few early points in their graph, and a survey of what older scientists recall coral reef cover to be.  The loss of coral in their graph was primarily in early days before there was much data, and shows much less decline recently when there has been much more data.  Another study summarizing worldwide monitoring data (Souter, GCRMN) found much less decline.

Line 49,  Caribbean and Florida reefs certainly have shown almost no ability to recover from disturbance, but Indo-Pacific reefs often show the ability to recover, as explored by the paper by Roff and Mumby, and by the AIMS monitoring program (the GBR has fully recovered coral cover after heavy losses, and it is not the only place in the Indo-Pacific that has done that).  There has been recovery documented on a variety of other Indo-Pacific reefs.    Roff, G. and Mumby, P. J. 2012. Global disparity in the resilience of coral reefs. Trends in Ecology and Evolution 27: 404-419.  

Lines 70-71  why is this sentence in italics?

Line  108  I assume that all coral recruits of all species were counted, not just A cervicornis.  You need to state that or that only A cervicornis recruits were counted.  It is clear from the end of the results section that you did count recruits of all species, but it would be good to state that in the methods section.

Line 155  and survivorship might be higher in the Caribbean than Florida.  Is there data to support that?

Line 249, 289   species name needs to be italicized

Author Response

Reply to Comments by Reviewer #2:

We would like to thank you for the comments provided. We understand they have significantly improved our manuscript.

Comment 1: Line 30   this makes it sound like there are two alternatives, one is outplanting and the other is regaining functionality.  That is surely not what you intend to say.  You want to say that outplanting is designed to help reefs regain functionality, don’t you?

Response: We have modified the abstract. Now it read as follows:

            “Coral reef degradation poses a significant challenge in the Greater Caribbean, prompting a surge in restoration efforts. Among these, transplanting nursery-reared coral colonies has emerged as a prevalent strategy to rejuvenate degraded reefs and reinstate critical ecosystem processes like coral recruitment. This study aimed to test the hypothesis that reintroducing the threatened Acropora cervicornis to a degraded coral reef enhances coral recruitment. To our hypothesis, we compared coral recruitment between an area populated with A. cervicornis outplants and a reference location devoid of the coral. Our findings revealed a notable 73% increase in coral recruitment within the restored area. Interestingly, within the restored site, proximity to A. cervicornis colonies correlated with higher recruitment rates, suggesting a positive association. These results underscore the potential of active coral outplanting to bolster the resilience of deteriorating coral reef ecosystems. Our research contributes valuable insights into the intricate dynamics of coral restoration and recruitment, emphasizing the merits of incorporating A. cervicornis into restoration initiatives.”

Comment 2: Line 40   what is “examining the immediacy” mean??  Are you saying you recommend outplanting A. cervicornis to restore coral recruitment?

Response: We agreed with the reviewer in that the sentence is somewhat confusing. We have deleted the sentence:

Comment 3: Line 47  The #1 reference, however, is based on very few early points in their graph, and a survey of what older scientists recall coral reef cover to be.  The loss of coral in their graph was primarily in early days before there was much data, and shows much less decline recently when there has been much more data.  Another study summarizing worldwide monitoring data (Souter, GCRMN) found much less decline.

Response: We have modified the introduction to focus on the Greater Caribbean. For example:

            Lines 46-48: “Coral reefs across the Greater Caribbean have faced severe degradation, primarily due to a combination of human activities such as unplanned shoreline development, biological factors like diseases, and physical disturbances, including hurricanes [1,2]”.

Comment 4: Line 49,  Caribbean and Florida reefs certainly have shown almost no ability to recover from disturbance, but Indo-Pacific reefs often show the ability to recover, as explored by the paper by Roff and Mumby, and by the AIMS monitoring program (the GBR has fully recovered coral cover after heavy losses, and it is not the only place in the Indo-Pacific that has done that).  There has been recovery documented on a variety of other Indo-Pacific reefs.    Roff, G. and Mumby, P. J. 2012. Global disparity in the resilience of coral reefs. Trends in Ecology and Evolution 27: 404-419.  

Response: See the answer provided to comment #3. We added the suggested reference to our introduction.

Comment 4: Comment Lines 70-71  why is this sentence in italics?

Response: Corrected

Comment 5: Line  108  I assume that all coral recruits of all species were counted, not just A cervicornis.  You need to state that or that only A cervicornis recruits were counted.  It is clear from the end of the results section that you did count recruits of all species, but it would be good to state that in the methods section.

            Response: We added the following sentence to clarify:

            Lines 143-145: “ Since no coral was present in the fixed quadrats at the start of the study, any coral of any species observed at the end of the year was considered a recruit”.

Comment 6: Line 155  and survivorship might be higher in the Caribbean than Florida.  Is there data to support that?

Response: We rephrase the sentence. It now read as follow “A study by Ware et al. [30] found that the survivorship probabilities of A. cervicornis outplants over a seven-year period varied between 0% to 10%”.

Comment 7: Line 249, 289   species name needs to be italicized

Response: Corrected

Reviewer 3 Report

given in review report

Comments for author File: Comments.pdf

a through revision is required for langauage in terms grammer and sentence arrangement.

Author Response

Response to Reviewer #3

We would like to thank you for the comments provided. We understand they have significantly improved our manuscript.

Abstract •

Comment 1: The study did not control for other factors that could have influenced the results, such as the quality of the water or the presence of predators.

Response:  We modified the methods to include evidence that the studied locations did not vary in water quality.

            Lines 133-134: “Studies by Hernández-Delgado and Ortiz-Flores [22] along the western coast of Culebra, where our study sites are located, have reported consistent water quality conditions”.

We agreed with the reviewer in that we were unable to control for predation. However, we understand that predation, if any, may not significantly influence our results. We discussed this issue in the manuscript.

Lines 205- 215:” A. cervicornis is a morphologically complex coral known to serve as a habitat for many reef species, i.e., fish [33-34]. Indeed, Calle-Triviño et al. [18] demonstrated that fish biodiversity in areas restored by outplanting A. cervicornis was much higher than in non-restored sites. In this sense, we observed that herbivore fish were evidently abundant and diverse at PMEL (e.g., parrotfish, grunts, surgeonfish, damselfish, personal observations). In contrast at PMEL-reference, fish species were limited to small labrid fishes (e.g., Thalassoma spp. personal observations) and juveniles of the territorial damselfish, Stegastes diencaeus. Enhanced herbivore populations would result in lower macroalga cover and higher nutrient delivery, which facilitates coral recruitment [34-35]. The high number of coral recruits at PMEL (compared to PMEL-Reference) may support such a contention. However, recruitment rates did not vary statistically when A. cervicornis was absent from the quadrats regardless of restoration status (e.g., restored vs. non-restored). This finding suggests that coral recruitment dynamics at the studied sites cannot be explained solely by variation in fish abundance or diversity”. 

Lines 230-234:” Another plausible explanation is that the branching complexity of A. cervicornis protects the newly settled coral larvae against reef grazers (e.g., fish and sea urchins). These grazers could inadvertently consume and remove recruits when foraging on algal mats in open areas [42]. Further experimental studies are needed to determine whether the explanations proposed above indeed play a role in shaping the recruitment pattern observed in this study”.

Comment 2: The study did not measure the survival of the coral outplants or the recruits.

Response: No coral outplant die after one year. Mortality occurred after Hurricane Fiona and alga blooms. We addressed these issues in:

 Lines 151-157: “Unfortunately, our study was discontinued after December 2021 due to a series of events that significantly altered the reef structure. These events included a mass mortality event of the sea urchin Diadema antillarum, multiple blooms of the alga Cottoniella filamentosa, and the impact of Hurricane Fiona. The dramatic changes in reef structure, including the mortality of many coral outplants, prompted the decision to halt the study. Continuing the study under such altered conditions could have introduced confounding factors that would have compromised the integrity of the results”.

We also addressed the limitation of not following the fate of the coral recruits.

 Lines 260-262: “. However, the scope of our study was constrained to one observation point and one coral reef, preventing a comprehensive understanding of spatiotemporal recruitment dynamics, including settlement and survival rates. Consequently, the generalization of our findings may be limited [12]”.

 Comment 3: The study did not consider the cost of coral outplanting or the environmental impact of the restoration process.

Response:  We added the following sentences to our methodology to clarify.

Lines 115-116:” These coral colonies were attached to the substrate using a cost-effective technique involving nails and cable ties (Fig. 2a), chosen for its minimal environmental disruption (i.e., change in substrate rugosity)”.

Introduction

Comment 4: The author could cite more sources to support the claims made in the introduction.

            Response: Suggestion accepted; we added relevant references to sustain our arguments.

Comment 5: The author could use more specific language when describing the different approaches to coral reef restoration

Response: Suggestion accepted; we modified our introduction to address the suggestion.

Lines 52-53: “To address the ongoing degradation of reefs, conservationists have turned to human-assisted coral propagation, which leverages corals' ability to reproduce sexually through gamete spawning or brooding propagules, as well as asexually through fragmentation. In the context of sexual reproduction, laboratory protocols have been developed to enhance coral egg fertilization and improve coral larvae's chances of settling on suitable substrates [5]. Following metamorphosis, settled larvae are subsequently translocated to selected reefs [5]. On the other hand, human-assisted asexual propagation involves cultivating coral fragments in ocean or land-based propagation units until they reach ecologically relevant sizes, after which they are reintroduced to the reefs. This "nursery phase" is vital as it significantly improves the survival and growth of early-stage coral colonies compared to those left directly on the reefs [6,7,8]. The practice of outplanting nursery-reared coral colonies into degraded coral reefs has gained significant attention in the last couple of decades, especially in the Caribbean, where 64% of restoration programs employ such an approach to increase the abundance of the major reef-forming species Acropora cervicornis, A. palmata, and Orbicella spp. [9].

Comment 6: The author could provide more detail on the specific goals of the study.

            Response: We improve our closing paragraph to provide more details about our goal.

            Lines 92-103:” Despite the critical role of coral recruitment in coral reef dynamics, it has often been overlooked in the assessment of coral restoration programs. This oversight has led to ongoing debates regarding whether coral outplanting effectively promotes natural coral recruitment [12, 20-21], creating a gap in our understanding of this vital aspect of coral reef health. In this study, we aim to address this gap by testing the hypothesis that restoring a population of the threatened coral A. cervicornis would enhance the recruitment of coral larvae. To do this, the number of corals that recruited in a restored area was compared to that of a reference location where no action was taken. We further explored the relationship between A. cervicornis and recruitment by comparing the number of recruits that were established in the presence and absence of a coral outplant. Examining coral recruitment rates in the context of coral restoration will provide valuable insights into the potential impact of A. cervicornis reintroduction on the overall health of degraded coral reefs. If restoration efforts are shown to significantly boost coral recruitment, it will highlight the importance of continued support for such initiatives in protecting and rebuilding coral reefs. This study is a contribution towards such an end”.

Comment 7: The author could discuss the potential impacts of the study on the environment.

            Response: See answer to comment 3.

Comment 8: The author could provide more detail on the specific methods and techniques

that will be used in this study. For example, how will the coral recruitment rates

be measured? How will the areas with and without A. cervicornis outplants be

selected?

            Response: We have modified the Methods to clarify.  For instance:

Lines 115-117:” These coral colonies were attached to the substrate using a cost-effective technique involving nails and cable ties (Fig. 2a), chosen for its minimal environmental disruption (i.e., change in substrate rugosity)”.

            Line 143:” Recruitment was defined as any new individual seen with the naked eye [26]”.

Comment 9: The author should also discuss the limitations of the study. For example, the

study is only being conducted in a small area, so it is not clear whether the

results would be generalizable to other coral reefs.

Response: We have discussed our limitation in the Discussion section

Lines 260-262:” However, the scope of our study was constrained to one observation point and one coral reef, preventing a comprehensive understanding of spatiotemporal recruitment dynamics, including settlement and survival rates. Consequently, the generalization of our findings may be limited [12]”.

Comment 10: The author could also discuss the implications of the study. For example, if the

study finds that coral outplanting does indeed facilitate coral establishment,

then this could have implications for the design and implementation of future

coral reef restoration projects.

            Response: See answer to comment 6.

Data and methods

Comment 11: The authors could have increased the power of the study by increasing the sample size. This could have been done by conducting the study in multiple locations or by using a larger number of quadrats.

Comment 12: The authors could have also collected data on other factors that could affect coral recruitment, such as water quality and nutrient levels. This would have helped to control for these factors and make the results of the study more generalizable.

Comment 13: • The authors could have also conducted a follow-up study to assess the longterm effects of coral outplanting. This would have helped to address the limitations of the current study and provide more information about the potential benefits of this restoration technique

Response: We agree that our study was limited. We addressed the necessity of more in depth study in the discussion section.  For instance:

Lines 260-262: “However, the scope of our study was constrained to one observation point and one coral reef, preventing a comprehensive understanding of spatiotemporal recruitment dynamics, including settlement and survival rates. Consequently, the generalization of our findings may be limited [12]”.

            Lines 266 -268: “To gain a more comprehensive understanding of the benefits of coral outplanting, collaborative research from various Caribbean locations and time periods is crucial, and we hope this study serves as a foundational contribution to such integrated research”.

Results

 Comment 14:  The authors should be careful about making causal inferences from their data. The fact that coral recruitment was higher in the restored area and in quadrats with an A. cervicornis outplant does not necessarily mean that the outplanting caused the increased recruitment. It is possible that other factors, such as water quality or nutrient levels, were responsible for the observed differences.

Comment 15: The authors should also be careful about generalizing their findings to other coral reefs. The study was conducted in a specific location and it is possible that the results would not be the same in other locations.

Response: See response to comments to the section Data and Methods above

Discussion

Comment 16:  The authors could have increased the power of their study by increasing the sample size and the duration of the study. This would have allowed them to make more confident conclusions about the effects of coral outplanting.

Comment 17:  The authors could have also conducted a follow-up study to assess the longterm effects of coral outplanting. This would have helped to determine whether the benefits of coral outplanting are sustained over time.

Comment 18:  The authors could have also explored the mechanisms by which coral outplanting promotes coral recruitment. This could have been done by collecting data on the behavior of coral larvae and the physical and chemical conditions of the reef.

Comment 19:  The authors should be careful about making causal inferences from their data. The fact that coral recruitment was higher in the presence of A. cervicornis outplants does not necessarily mean that the outplanting caused the increased recruitment. It is possible that other factors, such as water quality or nutrient levels, were responsible for the observed differences.

Comment 20:  The authors should also be careful about generalizing their findings to other coral reefs. The study was conducted in a specific location and it is possible that the results would not be the same in other locations.

            Response: We agree with the recommendations provided by the reviewer. Unfortunately, due to financial constraints (lack of funding), we are not in the position to continue our study; however, the recommendation was incorporated into our plan of work, and hopefully, in the near future, we can conduct a more robust study.  We conclude our manuscript by stating the following,  “To gain a more comprehensive understanding of the benefits of coral outplanting, collaborative research from various Caribbean locations and time periods is crucial, and we hope this study serves as a foundational contribution to such integrated research”.  

Round 2

Reviewer 3 Report

Article can be accepted now.

Article can be accepted now

Author Response

Dear Reviewer:

I hope this email finds you well. Thank you very much for calling to our attention the grammatical errors. We have worked on the manuscript thoroughly and have corrected them. 

Kind regards,