Review Reports - Environmental Drivers and Social Structure Features behind the Low Reproductive Success of Dusky Groupers Epinephelus marginatus (Lowe, 1834) in a Mediterranean Marine Protected Area

Round 1

Reviewer 1 Report

I read the MS "Environmental drivers and social structure features behind the
low reproductive success of dusky groupers in a Mediterranean
marine protected area".

The authoring team studied the reproductive behavior of the dusky grouper at Tabarca Island Marine Protected Area (TIMPA) in order to describe its temporal pattern, evaluate the relationships between reproductive behavior and environmental patterns and verify the effects of the social structure of the reproductive activity.

However, before it can be accepted; the manuscript must undergo some modifications and improvements.

This is an interesting piece of work.

However, before it can be accepted; the manuscript must undergo some modifications and improvements.

The English usage in some parts is poor and needs to be improved.

In the abstract problem, statement should be presented clearly.

To make the introduction more substantial, the author should provide several updated references to substantiate the claim made.

Author Response

Dear reviewer, many thanks for your suitable comments and suggestions. We proceeded as you have suggested. Specifically:

The English usage in some parts is poor and needs to be improved.

We re-examined the english usage and corrected all the mistakes. Moreover, we'll contract the english review service of the Editorial to improve the manuscript. Many thanks for your comment.

In the abstract problem, statement should be presented clearly.

We have re.written the abstract to summarize it and present more clearly the proposed statements. The new version of the abstract is:

"MPAs are considered a key tool to achieve the sustainability of coastal fisheries by allowing habitat and species conservation by means of use regulations and active management. The effects of protection are more visible in slow-growing, high site fidelity and mature late species such as dusky grouper, a flagship species for all the fishermen and divers in the Mediterranean Sea. We studied the reproductive behavior of dusky grouper at Tabarca Island Marine Protected Area (TIMPA) in order to: a) describe its temporal pattern; b) evaluate the relationships among reproductive behavior and environmental factors and c) verify the effects of the social structure on the reproductive activity. We observed all the behavior patterns previously reported in other studies unless the final spawn event. Our results evidenced that the monthly average density of dusky groupers tended to increase when temperature rose close to the seabed and without defined temporal limits for the reproductive behavior. Among the environmental factors considered, visibility exhibited a very strong effect on the reproductive behavior of dusky grouper, interacting significantly with sea bed temperature and thermocline. Regarding the effects of social structure, the reproductive activity was postively related with the presence of large size individuals. We discuss about the differential facts of the reproductive activity of dusky groupers observed at TIMPA relating the results to the biogeographical location, the patterns of the environmental drivers and the structure of the habitat. These negative results contrast with the existing knowledge and generate new working hypotheses useful to improve the efficiency of MPAs and the sustainability of coastal fisheries."

To make the introduction more substantial, the author should provide several updated references to substantiate the claim made.

We include some more recent references to substantiate the claims made, as proposed by the reviewer 1, although we limited the additions due to the recommendations of the journal.

Reviewer 2 Report

Dear Authors,

Overall, I feel that the information provided in this manuscript has some relevance to a broader audience. This paper addresses an important topic on the species dusky groupers about reproductive biology and protecion areas. Also the introduction and the purpose of the research are well organized. The manuscript has been written successfully. There are almost no deficiency between the references and the references in the content of the manuscript. I have recommended that the manuscript undergo with minor revisions (below) prior to its acceptance.

Comments for author File: Comments.pdf

Author Response

Dear reviewer, many thanks for your suitable comments and suggestions. We proceeded as you have suggested. We included all the suggestions over the manuscript. Please, check the new version of the manuscript to verify it.

Reviewer 3 Report

In the present manuscript the Authors described the behaviour, colour patterning of a "flagship species" for all the divers of the Mediterranean Sea and related their observation with seafloor traits and abiotic variables insisting on a MPA. In their effort, some important details (e.g., nomenclature, citations) were forgotten. See proposals of modification below.

Although I am not familiar with the species, nor with the statistical methods, I appreciated the manuscript, which left a lot of curiosities that may spark the interest of other readers. In particular, I would have detailed the description of colour patterning and behaviour, focussing on the importance of visual signals. Is there any other study outside the Mediterranean Sea, even on congeneric species, supporting your results? I believed that the "sixth sense" of the lateral line of teleosts would have overcome this limitation. Then, a curiosity: may scarse visibility have influenced your observations?

Furthermore, it is really interesting that no spawning event has been observed in the groupers' hotspot; Do you have any explanation to be added in the discussion section?

Here are my further comments:

Abstract

Please, verify the verb tense. For instance, at line 17 the Author switched to present tense.

Line 19: “environmental drivers”, such as?

Line 22: the Keywords chosen should not be the exact words contained in the main title. Please, choose different keywords instead of “dusky groupers, marine protected area, environmental drivers”.

Introduction

Line 51: species name in Italics, so change to “Epinephelus marginatus”. Please, verify throughout the text.

Line 52: the species is “assessed as overexploited”, please add reference (e.g., IUCN).

Lines 57-61. Please, rephrase these tenses. Sounds not scientific. Furthermore, why smaller individuals should be exported outside the MPAs? I’m not experienced with the conservation of this species; maybe further details are needed to clarify the issue to the lecturers.

Lines 85-87: maybe a short summary of the aggregation patterns previously described (references from 17 to 25) would help the reader. The reader is not obliged to go and check each reference, so a glance about aggregative behaviours (common or very different traits) would be appreciated.

Line 103: please, delete the descriptor’s name; it was indicated in the introduction. No need to report it in all the manuscript. Please, check throughout the whole text.

Line 114: “Posidonia oceanica” in Italics and add the descriptor; please, check the scientific nominal names of any cited species throughout the text.

Line 122: “It serves as”; not sure about the subject of the sentence, the promontory? Please, be clarify.

Figure 2: although I really appreciate the map as presented, I am not sure this is the proper way to be presented to the Journal; please, verify the authors’ guidelines.

Line 157: I am not familiar with the species; are “defending or attack patterns” defined as/by colours?

Line 169: is there a link between the “position” variable with the “reproductive” one?

Line 180: change “quasi-likelihood but it” to “quasi-likelihood, but it”.

Results

Line 209: Please, help the reader with a short description of “livery 6”.

Line 227: change “Figures 4” in “Figure 4”.

Furthermore: is it correct talking about “reproductive symptoms”? Better “signals”?

Lines 229-230: Referring to “The earlier reproductive behaviors were detected in march of 2019 and the later ones in

december of 2018” I am confused; do you mean that in 2019 you recorded the earliest reproductive behaviours, while in 2018 you observed the latest reproductive” patterns? Please, clarify and modify the text accordingly (maybe invert the events of 2018 and then 2019?).

Figure 4: change “proportion” with capital letter “Proportion”. Please, check all the captions.

Discussion

Line 360: “[? ]” What is it?? Typo? Please, verify.

Author Response

Dear reviewer, many thanks for your suitable comments and suggestions. We proceeded as you have suggested. Specifically (responses in blue):

Furthermore, it is really interesting that no spawning event has been observed in the groupers' hotspot; Do you have any explanation to be added in the discussion section?.

We have some more explanations but fall within speculation. In the near future we will initiate research to collect information about them and try to clarify them. We have preferred not to add them to the manuscript.

Here are my further comments:

Abstract

Please, verify the verb tense. For instance, at line 17 the Author switched to present tense.

“We discuss” was changed to “We have discussed”

Line 19: “environmental drivers”, such as?

We included a summarized list of environmental drivers in this line. There is a extended list of environmental drivers explained in the material and methods section, such as the seabed temperature per day, the thermocline, the visibility, the stream force, the photoperiod and the divers per day.

Following your recommendation, “dusky grouper” was changed to “flagship species”;

“marine protected area” was changed to “marine reserve”,

"reproduction" was changed to "spawning aggregations",

“environmental drivers” and reproductive success were removed,

we included "protection" and "sustainability"

Introduction

Line 51: species name in Italics, so change to “Epinephelus marginatus”. Please, verify throughout the text.

We have verified all species names and changed the format to italic.

Line 52: the species is “assessed as overexploited”, please add reference (e.g., IUCN).

We added IUCN as a reference.

In the text, we added: (IUCN 2022) and in the reference list:

IUCN. 2022. The IUCN Red List of Threatened Species. Version 2021-3. https://www.iucnredlist.org. Accessed on [03 05 2022].

This paragraph was erased :

“This population dynamic is a problem in the face of fishing since it ends up leaving the population without males at the extreme of the large ages and it intensively exported small and medium-sized individuals to the outside of the MPA. Given that MPAs are designed to assure the viability and sustainable use of these species, it is important to assess and verify their effective reproduction into the limits of the managed area.”

and replaced by:

"In MPAs, E. marginatus may be adversely affected by some features of the species' inherent biology working synergistically with local fisheries. This is a sequential hermaphroditic protogynous species, reaching sexual maturity at five years of age. When their sizes are small and medium, individuals tend to look for new territories outside the reserve due to density-dependent factors linked with the territorial behavior of the species[10], where they are frequently caught by artisanal fleets. These captures, according to Sadovy de Mitcheson et al. [7], can eventually end up skewing the population of large-sized individuals or males. Given that MPAs were designed to assure the viability and sustainable use of these species, it is important to assess and verify their effective reproduction into the limits of the managed area."

We replaced lines 85-87 by:

“Preliminary observations confirm the aggregation of dusky groupers, with the social behaviour features similar described by prior literature [15,16,17,25]. It was observed a larger medium sizes proportion than large sizes, territory patrol behaviour by large males and the complete range of interactive corporal and colour patterns described by the cited works (Lozano-Quijada, unpublished data).”

Line 103: please, delete the descriptor’s name; it was indicated in the introduction. No need to report it in all the manuscript. Please, check throughout the whole text.

It was deleted the descriptor´s name and check it throughout the text.

Line 114: “Posidonia oceanica” in Italics and add the descriptor; please, check the scientific nominal names of any cited species throughout the text.

All scientific nominal names were changed to italic format

Line 122: “It serves as”; not sure about the subject of the sentence, the promontory? Please, be clarify.

It was replaced by: “This promontory serves as”

Figure 2: although I really appreciate the map as presented, I am not sure this is the proper way to be presented to the Journal; please, verify the authors’ guidelines.

We verify the authors guidelines and consulted with the editor. Here you can read the Sustainability journal guidelines for figures:

Preparing Figures, Schemes and Tables

File for Figures and Schemes must be provided during submission in a single zip archive and at a sufficiently high resolution (minimum 1000 pixels width/height, or a resolution of 300 dpi or higher). Common formats are accepted, however, TIFF, JPEG, EPS and PDF are preferred.
Sustainability can publish multimedia files in articles or as supplementary materials. Please contact the editorial office for further information.
All Figures, Schemes and Tables should be inserted into the main text close to their first citation and must be numbered following their number of appearance (Figure 1, Scheme I, Figure 2, Scheme II, Table 1, etc.).
All Figures, Schemes and Tables should have a short explanatory title and caption.
All table columns should have an explanatory heading. To facilitate the copy-editing of larger tables, smaller fonts may be used, but no less than 8 pt. in size. Authors should use the Table option of Microsoft Word to create tables.
Authors are encouraged to prepare figures and schemes in color (RGB at 8-bit per channel). There is no additional cost for publishing full color graphics.

We verify all them, and our figure 2 pass the checking. Many thanks for this comment.

Line 157: I am not familiar with the species; are “defending or attack patterns” defined as/by colours?

Zabala et al. 1197b and Louisy and Couliolioli 1999 [16], [17] described 8 different colour patterns (different liveries) linked to different behaviours and states of mind, age and sexual maturation. We learned to distinguish which indicates attack or defence. For example, a specimen showing a dark with three blotches or silver-streaked livery indicates aggressiveness. Attack and defence behaviours and their colour patterns linked are very easy to perceive by observing the specimen interactions in its natural habitat.

Line 169: is there a link between the “position” variable with the “reproductive” one?

Yes, there is. If you watch the table 2, the positions Hidden p (estimate -2,659) and Perched p (estimate -3,143) are significantly negative in relation to the reproductive state (0.001). In other words, a specimen who is resting on the seabed or hidden in its cave is not looking for sex. (It could be thinking in it, but we do not know).

Line 180: change “quasi-likelihood but it” to “quasi-likelihood, but it”.

It has been changed.

Results

Line 209: Please, help the reader with a short description of “livery 6”.

It was changed to:

We observed up to six dominant males exhibiting a silver-streaked livery, or “livery 6” according to Zabala´s description [16]

Line 227: change “Figures 4” in “Figure 4”.

It was changed.

Furthermore: is it correct talking about “reproductive symptoms”? Better “signals”?

All right, it was changed.

Lines 229-230: Referring to “The earlier reproductive behaviors were detected in march of 2019 and the later ones in

Yes, it does. We have changed the sentence to:

"Over an annual scale, the earlier reproductive behaviors were detected in march (2019) whereas the latter one were in december (2018), although it could be confused with territorial displays."

Figure 4: change “proportion” with capital letter “Proportion”. Please, check all the captions.

It was changed. Captions were checked.

Discussion

Line 360: “[? ]” What is it?? Typo? Please, verify.

This mistake has been rectified.

Round 2

Reviewer 3 Report

Dear authors,

thank you for your efforts. I found the MS overall improved. All the suggestions and modifications were addressed leading to a smooth reading where the topic is valorised. English tense was also improved. I happily recommend this MS for publication.