PONE-D-20-33086

Current trends and future directions in coral transplantation for reef restoration

PLOS ONE

Dear Dr. Ferse,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’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.

Your manuscript entitled “Current trends and future directions in coral transplantation for reef restoration” has now been assessed by two experts in the field of coral reef restoration. While both Reviewers and I see the importance of the study in advancing knowledge on the work being undertaken by a diverse array of practitioners, there are some major concerns that need to be addressed before the manuscript can be considered for publications. Firstly, some key questions appear absent from the questionnaire that would greatly aid the interpretation of the results. A follow-up questionnaire is highly recommended to provide the additional information noted by both Reviewers. At a minimum, the manuscript needs to have an expanded discussion section to address the points raised by the Reviewers. Secondly, while I appreciate that additional data collection is not always feasible, as noted by Reviewer 1, the study would greatly benefit from information from Australia, given the immense work taking place by diverse practitioners in this region.  Finally, I urge consideration of the tone of the manuscript as noted by Reviewer 1 when conducting the revisions. Consequently, I am recommending major revisions to allow you the opportunity to consider some of the additional data collection suggested by the Reviewers, as well as addressing the tone of the manuscript noted by Reviewer 1. I look forward to seeing a revised version of this manuscript.

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PLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

Reviewer #2: Yes

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

Reviewer #1: Yes

Reviewer #2: Yes

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3. Have the authors made all data underlying the findings in their manuscript fully available?

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Reviewer #1: Yes

Reviewer #2: Yes

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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: The manuscript titled “Current trends and future directions in coral transplantation for reef restoration” is intended to be a review of global coral transplanting projects to evaluate under-represented restoration projects from around the world as most published literature only comes from projects in the Caribbean. It highlights the concern that there are few venues for presenting data and lessons learned by projects which may not have the means to publish within peer-reviewed literature. Also, this manuscript highlights the common concern of restoration practitioners that long-term monitoring is needed to evaluate the success of restoration activities. Through a survey disseminated to active practitioners, the authors identifies the types of practitioners conducting coral transplantation, their overall objectives, the morphology of coral used in their work, the type of pre- and post-assessment that is conducted, and the source of coral used. This manuscript has many admirable objectives and identifies several interesting trends, but could benefit from some edits, re-writes, and expanded discussion.

The title may not represent actual context of manuscript (i.e., current trends and future direction are a bit misleading as the trends are those represented within the 43 projects outlined in the surveys and the future directions are those perceived as most important by the authors). Title should include “a survey of” or “review”.

Within the first paragraph of the intro, I suggest placing the two sentences addressing anthropogenic stressors next to each other for continuity.

One of the arguments of this manuscript is that coral transplantation is not a useful ecological tool for reefs where natural coral recruitment is successful as first mentioned by Edwards and Clark (1998). The authors of this manuscript argue that few, if any, practitioners even consider coral recruitment when conducting coral transplantation. Based on the status of coral populations, especially in the Caribbean, many local researchers can probably say with much confidence that current coral cover does not support healthy coral recruitment. The time and resources required to conduct coral recruitment studies or modeling prior to starting the lengthy and costly process of coral restoration may prohibit such studies from being conducted. Additionally, the authors stress the need to know the root causes of reef degradation and emphasize that unless the causes are removed, coral restoration will not be successful. This has long been the argument against coral restoration. But as time goes on, coral reefs continue to be faced by the same, as well as additional biological and anthropogenic stressors. So much so that unless actions are taken to preserve some genetic and species diversity, there will be nothing left to restore. Therefore, I would suggest that the authors consider reducing their focus on these potential reasons for not conducting coral transplantation and instead highlight management strategies and conservation techniques that utilize transplantation and other science-based recovery approaches.

Lines 82-89: “Yet, if coral transplantation and restoration in general are gaining interest and popularity as reef management strategies, the methods should be used within a wider set of resilience-based integrated frameworks that simultaneously or pre-emptively address the source of threats and disturbances. Restoration should be the last point of action in a carefully planned management framework. Understanding the cause of coral mortality, the barriers to natural recovery, and the type of repair necessary to initiate recovery are all important considerations that need to be elucidated prior to undertaking transplantation.” These lines raise very interesting discussion topics but are not sufficiently addressed by the authors. What other type of management strategies should incorporate coral transplantation? Please describe some of the integrated frameworks that could address threats and disturbances which may alleviate the need for transplantation. It would benefit the manuscript if the authors could expand on these ideas within the discussion to provide some insight into developing resilience-based integrated frameworks.

Lines 112-119, the authors raise the issue of accountability, an issue that has been mentioned in other reef restoration focused literature (Morrison 2020, Lirman and Schopmeyer 2016, France 2016). For example, “In recent years, reef restoration or coral transplantation projects are increasingly adopted by the dive and tourism industry or as part of corporate social responsibility programs, raising the question to what extent the principles of good practice set forth e.g. by Edwards and Clark and Edwards or lessons earned from the restoration of other ecosystems are implemented in current coral transplantation projects. Specifically, the questions arise whether causes of coral degradation are identified prior to the adoption of coral transplantation, whether there is a bias towards fast-growing (usually branching) species to produce quick results, and whether adequate follow-up monitoring of transplanted corals is carried out.” Unfortunately, I feel the tone of manuscript focuses the attention on the wrong thing. Rather than focusing on if the “principles of good practice….are implemented” by accountable practitioners who have the appropriate experience, the tone of the manuscript seems to focus on raising concerns over certain restoration practices. But, the problem is that the restoration practices of concern are those that are most likely conducted by practitioners without the appropriate experience, without oversight and most likely without accountability. As examples, experienced restoration practitioners are typically well versed in the causes of reef decline (e.g., chronic, acute, anthropogenic, biological, etc) in the areas where they work, or the causes would be known by local stakeholders. The time and effort that goes into restoration would not be wasted by experienced practitioners in an area where unknown circumstances may cause failure. Additionally, fast-growing species may be the first species available for restoration (other slower growing species may not yet be available especially when mariculture is being used), may be the species of choice due to recent losses due to bleaching/disease, or permits may not be available as collecting whole colonies or fragments of massive colonies is more damaging than from branching species. And, in many cases, monitoring, although sometimes not for as long as some would like, is required for restoration activities with any funding or permitting oversight. Therefore, the tone of this manuscript tends to lump all practitioners into one group rather than distinguishing between experienced and novice practitioners. A question within the survey that indicated the length of time that each group had been conducting restoration may have helped with this.

Line 146: I would use the word “focus” rather than “bias” when discussing the use of fast-growing or branching species for coral transplantation. The reasoning behind using fast growing species can be varied and is not necessarily non-altruistic.

Line 147: I would rephrase objective vi to simply state “the source of corals for transplantation”.

Line 182, change “were” to “where”.

It is unfortunate that only 43 programs responded to the survey and the paucity of responses may have skewed the overall outcome of the survey. With the number of list serves, consortiums, conference websites, webinars, and other social media outlets, I am curious what would happen if the survey was presented again. I believe that this is a big setback for the manuscript, especially the lack of projects from Australia, where large interest in active restoration is occurring due to recent losses on the Great Barrier Reef.

Lines 196-197: The authors mention that the distinction between “private” and “business” was not always clear for type of organization, therefore, the wording of the survey may have caused some issues with the results of the survey. For the most part, I believe that the authors handled the categorization of the answers well.

However, in the case of the funding sources, what were the intended differences between Business, NGO and Private?? For example, there are private businesses, NGOs that take private donations and government funding, etc. Without some explanation of the differences between funding types, there may be some discrepancies in the survey results.

Lines 211-212: what is the statistical support for the statement that “The scale of the projects did not differ significantly among the types of actors or regions”?

The “Lessons Learned” paragraph (Lines 313-332) provides some interesting information and highlights the overall objective for many of the practitioners which is successful outplanting. I feel this data could have been more valuable to the objectives and goals of the manuscript had they been incorporated into the questions within the survey.

Lines 335-338: “In this review, we provide an overview of coral transplantation projects from around the world beyond those reported in the scientific literature, including the private sector for which little information exists to date, and identify differences in the design of projects and use of methods among different types of practitioners.” Unfortunately, I don’t find this statement to be true. This manuscript focused on the organization, funding, morphology, substrate, and monitoring type, but did little to advance the science and data coming from such projects. In general, “design of projects” and “use of methods” typically includes information regarding outplanting technique (eg., nails, epoxy, cement, wedging, etc.), number of corals, number of species, outplanting design (eg., arrays, plots, rows, random, etc.), etc. But, this manuscript did more to outline the coral transplantation programs than the coral transplantation itself.

Lines 338- 340: “Being able to draw on the knowledge gained by projects not reported in the scientific literature is indispensable to obtain a better overview of current techniques and to tailor future recommendations.” This statement is so very true and was my hope for this manuscript. Unfortunately, this manuscript did not deliver any new trends or new techniques for coral transplantation. It would have been beneficial if the authors could have identified new information and a means for disseminating ideas and data from the private sector and from smaller projects which are often missing from the scientific literature.

Within the discussion regarding the use of fast-growing, branching species (Lines 371-389), I believe that the authors may miss the mark when interpreting the results of the survey. For example, half of the projects used massive or other morphologies which is considerably higher than what it would have been a decade ago. Techniques for propagating massive species have drastically changed over the last 10 years making it easier to raise them within nurseries and methods for fragmenting have also improved survival for collections in the wild. Many projects begin with fast-growing, branching species to create structure and then transplant massives once other species have become established. To date, most research shows that outplanting massive species is difficult due to high rates of predation. It’s not apples to apples when it comes to transplantation. Also, not all projects are able to collect/propagate all species at once whether it’s due to timing, funding, permitting, etc. it's not for a lack of want for using massive species, the technology and ability to use such species just isn't as advanced as that for branching species which are easier to use for restoration. Therefore, the simplicity of the survey questions may not have allowed the projects to fully explain why only branching corals were used (once again, the age of the project/program would be important to know).

What was the size of the projects that used non-maricultured corals? It's easier for smaller projects to source corals from the wild, but any project looking to outplant on a reef or ecological scale should consider mariculture to avoid detrimental collections from the wild. And it is true that more projects in the Caribbean are probably using nurseries (in or ex situ) as these projects have been operating on longer time scales and the availability of wild corals is much, much lower than on other global reefs.

Discussion of Assessment of Reef Condition: Although I understand the premise behind needing to know the underlying cause of coral mortality (i.e., there is no reason to outplant on a reef if a disease is just going to kill the outplants), sadly, the cause of coral cover loss over time is not usually in question and the solutions to prevent further losses are not simple. The need for baseline surveys prior to restoration is, however, completely relevant (Goergen et al 2020) and the push for better management and water quality standards continues but should not outweigh saving remaining diversity and resilience.

Lines 421-422: “coral transplantation may be a waste of time and resources unless the recipient site fails to recruit juvenile corals.” However, in the broader picture, a site can't recruit juvenile corals if there aren't any adults to contribute to the population.

Lines 423-424: “Furthermore, the absence or minimization of threats is a key attribute of ecosystems that are to be restored – transplantation is not likely to succeed unless chronic stressors are removed.” True, but populations that survive episodic stressors may provide recruitment in the meantime and allow a buildup of resilience while chronic stressors are handled?

Lines 425-427: “An in-depth understanding of the causes of degradation is also key to developing goals and objectives for a restoration project and optimizing site-selection so that the project has a chance to withstand future disturbances.” This is a great point to highlight and there have been some good progress on how to better select sites for multi-species restoration that consider past success and failures.

Lines 453-455: “Several of the projects included measures to address environmental conditions, such as water treatment, fishing regulations or closed areas.” What is meant by water treatment?

Lines 455-459: “However, our survey was unable to ascertain the presence of chronic stressors or the original cause of reef degradation, and we thus cannot assess to what extent root causes of degradation or chronic stressors were adequately recognized and addressed in each case, underlining the need for thorough documentation and explicit statement of goals in restoration projects.” The meaning of this statement is a bit unclear, but perhaps this is more of an issue with the survey rather than a problem with documentation?? This information may be available to the practitioners but may not have been outlined within your questionnaire.

Lines 465-469: “One of the most successful coral transplantation projects at a larger scale (>2ha) was initiated by private Corporate Social Responsibility initiative. Such projects may be at an advantage in terms of available funding (i.e. long-term financial sustainability), local social capital and institutional flexibility (i.e. less ‘red tape’) than government-run initiatives.” How are the authors determining “success” here? Assuming it’s based on the number of accompanying measures that were included in this project, I would hesitate to say that this promises “success” in terms of survival, growth, or habitat and species rehabilitation. In addition, what is the oversight for such projects? What type of accountability is there? It’s easy to look like a project is doing more if not everything is done properly?

Lines 521-523: “Improving the application of recently developed monitoring guidelines and sharing of lessons learned among practitioners, managers, and academics is particularly important to further the understanding of coral restoration effectiveness.” Yes!! It is imperative that the value of consistent monitoring is spread throughout the restoration community.

Reviewer #2: This is a really useful piece of work that will enhance our understanding of real-world coral reef restoration projects. It stands out from other work in that it distinguishes between restoration ecology and ecological restoration, something that many people do not do (notably the most recent large-scale review of coral reef restoration that incorrectly categorises scientific studies as restoration projects). I think the fact that they recognise this distinction and that they have compiled a database of previously unpublished real-world restoration projects is of great value.

I just have a couple of major comments and a few minor comments below:

Main comments:

One problem with questionnaire for me is that the question about overall objectives is that it is grouped into 5 very broad categories, but those categories don’t really tell us anything about success. For example, the question about habitat restoration doesn’t ask what practitioners were trying to restore to. Two questions that would have been really great to ask are a) were there clear a priori goals against which to gauge success (if so, what were they) and b) did you identify a reference site against which to judge success. I guess it is too late to do anything about this now, but perhaps valuable to add a section in the discussion talking about the clear lack of adequate goal setting and the lack of reference sites in most restoration projects.

Research was given as an option for the purpose of the project and was reported as the main objective for 33% of the government projects. If research was the main objective, then I cannot really see how these projects can be considered as restoration projects. I think it is fine to leave these in, but it would be good to discuss this in more detail and ask why research would be a major motivation for an actual restoration project (when the main aim should be conservation, restoration or some socioeconomic goal).

Minor comments:

Line 182: “were” should be where.

Results: Lines 208-210: Were the number of transplants reported the total number of corals transplanted over the entire project, or did you try to get some idea of the number transplanted each year?

Line 343: “widely spread” should be wide-spread

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Reviewer #1: No

Reviewer #2: Yes: James Guest

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PONE-D-20-33086R1

A survey of current trends and suggested future directions in coral transplantation for reef restoration

PLOS ONE

Dear Dr. Ferse,

Thank you for submitting your manuscript to PLOS ONE. Both of the Reviewer's have recommended that the manuscript is accepted, and they appreciated the effort taken to address their comments. I have suggested minor edits to give you the chance to address the two additional minor comments made by Reviewer 2. The manuscript has been greatly improved by the change in tone and increased discussion and I commend the effort taken to address all points raised. Please address the two minor comments raised and re-submit. I am then happy to progress the manuscript for acceptance.

Please submit your revised manuscript by May 07 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 plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols

We look forward to receiving your revised manuscript.

Kind regards,

Emma F Camp, Ph.D.

Academic Editor

PLOS ONE

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.

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. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately 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?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). 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 ONE 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: (No Response)

Reviewer #2: I'm happy that the authors have addressed all of the comments. I think this is a valuable paper and have no hestitation recommending publication. I just have two fairly minor suggestions:

Lines 67-71: It’s not clear to me why this definition for coral reef systems is the correct one to use for coral reefs. Why not just use broadly accepted terms laid out by the SER? Is it useful to basically call any intervention that tries to promote resilience as “restoration”? I wonder if there’s an opportunity to compare and contrast restoration with rehabilitation and make the point that in fact, most reef “restoration” efforts are actually much closer to SERs definition of rehabilitation.

Lines 84-86: I’m not sure about this. Even for sexual propagation, you still have to collect corals from the wild in many cases. These parent colonies can be transplanted back to the reef, but they are often very stressed and die post-transplantation. I would say that the biggest advantages of sexual propagation are increased genetic diversity and access to large numbers of propagules. If gametes are collected in situ then you can also potentially reduce impact on donor reefs.

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Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: Yes: James Guest

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A survey of current trends and suggested future directions in coral transplantation for reef restoration

PONE-D-20-33086R2

Dear Dr. Ferse,

Thank you for addressing the minor comments of Reviewer 2. 

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Emma F Camp, Ph.D.

Academic Editor

PLOS ONE