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Article
Peer-Review Record

Incorporating Species-Conditional Co-Occurrence When Selecting Indicator Species to Monitor Restoration after Mangrove Removal from the Siangshan Wetland, Taiwan

J. Mar. Sci. Eng. 2021, 9(10), 1044; https://doi.org/10.3390/jmse9101044
by Ta-Jen Chu 1,2,3, Chun-Han Shih 3,4,*, Yu-Ming Lu 3,5, Yi-Jia Shih 1,2, Jia-Qiao Wang 1,2 and Liang-Ming Huang 1,2
Reviewer 1: Anonymous
Reviewer 2: Anonymous
J. Mar. Sci. Eng. 2021, 9(10), 1044; https://doi.org/10.3390/jmse9101044
Submission received: 4 September 2021 / Revised: 17 September 2021 / Accepted: 18 September 2021 / Published: 23 September 2021
(This article belongs to the Special Issue Interannual Variation of Planktonic Species and Fish Populations)

Round 1

Reviewer 1 Report

There appears to be a typo on Fig 1, satellite image, "Dense Reglens"??

Author Response

Ms. Ref. No.:  jmse-1388667
Title: Incorporating species-conditional co-occurrence when selecting indicator species to monitor restoration after mangrove removal from the Siangshan Wetland, Taiwan

Reviewer #1: Comments to jmse-1388667 by Chu et al. (please, also see annotated manuscript):

1.There appears to be a typo on Fig 1, satellite image, "Dense Reglens"??

Ans: We are much grateful for your careful reading of our manuscript and your valuable comments and suggestions to help improve the paper. We have now carefully revised the paper in light of all the comments and suggestions. Thanks for the reviewer's comments. This error is due to an old version of the submission. We have revised in the new submission. We have determined that this error does not exist.

 

Reviewer 2 Report

This study focuses on incorporating species-conditional co-occurrence when selecting indicator species to monitor restoration after mangrove removal from the Siangshan Wetland (Taiwan). I think the paper fits well the scope of the journal and addresses an important subject. However, a number of revisions are required before the paper can be considered for publication. There are some weak points that have to be strengthened. Below please find more specific comments:

 

*The abstract seems to be adequate.

*The relevant literature is discussed in the introduction section. I suggest checking for more recent and relevant studies that have been published over the last two years.

*Section 2.1: Please add a few sentences to justify the selection of the study area.

*One of the major weaknesses of this manuscript is a lack of good-quality images. Pretty much all the figures have low resolution and look kind of blurry. Please try to update the figures and improve the resolution.

*There are quite a few equations listed in the manuscript. However, these equations are not supported by any references. Please provide the relevant references to justify the selection of equations and basic modeling assumptions.

*Figure 2: again the resolution is very low, and it is difficult to read this figure.

*Overall, the presentation of the study results seems to be adequate. The only suggestion I have here is to create more supporting discussions where appropriate, so the readers can clearly understand the managerial implications from the conducted work.

*The conclusions section should expand on limitations of this study and future research needs. I suggest listing the bullet points.

 

Author Response

Reviewer #2: Comments to jmse-1388667 by Chu et al. (please, also see annotated manuscript):

This study focuses on incorporating species-conditional co-occurrence when selecting indicator species to monitor restoration after mangrove removal from the Siangshan Wetland (Taiwan). I think the paper fits well the scope of the journal and addresses an important subject. However, a number of revisions are required before the paper can be considered for publication. There are some weak points that have to be strengthened. Below please find more specific comments:

 

1.The abstract seems to be adequate.

Ans: Your affirmation gives us a lot of encouragement and confidence.

 

  1. The relevant literature is discussed in the introduction section. I suggest checking for more recent and relevant studies that have been published over the last two years.

Ans: We add and supplement this paragraph in the introduction section.

Many studies, including species, communities, and ecosystems, have been identified and widely used in different fields. Such as IS, Corbula gibba and Flexopecten hyalinus, were used to characterize disturbed and undisturbed areas in terms of chlorophyll a concentration in Greece, respectively [20]. The xerophyte inland dune shrub community from Portugal was used to evaluate the relationship between the structure of dune community, local environmental conditions and the suitability of climatic conditions for its characteristic species [21]. While IS have rarely proven to be an effective tool for monitoring ecosystems and informing management decisions [22]. Use quantitative methods to determine that IS is also developing rapidly. Thus, Fleming et al., (2020) [22] extend the conceptual models of IS to include a direct relationship between an indicator species, ecosystem change drivers and latent processes and variables. It allows for latent‐state models to be tested empirically, facilitating the robust evaluation and practical use of indicator species for ecosystem science and management [22]. Fifteen species out of 89 plant species were found by principal components analysis to be an IS, which should be benefited for the vegetation change status and sustainable rangeland management under semiarid rangeland conditions [23]. A context-dependent joint species distribution model (JSDM) was built to estimate the residual associations, 161 plant species were selected based on community data from 8,660 vegetation plots [24].

 

  1. Section 2.1: Please add a few sentences to justify the selection of the study area.

Ans: We add and supplement this paragraph in the Section 2.1.

The mangroves were planted in 1969. A survey of mangroves found that there were as many as 5,300 stands in 1992. Mangrove areas were estimated in 0.1-ha areas by the Taiwan Endemic Species Research Institute in 1995. According to the report, the Siangshan Wetland Mangrove Removal and Benefit Assessment Program of the Hsin-chu Municipal Government in 2000, the mangrove area covered approximately 107 ha. Due to the continuous spreading of the mangrove in the coastal areas, the effects shown included habitat singularity, decline of species abundance, decline of biodiver-sity, infilling of estuaries, flooding, and small black mosquito breeding. And then, sev-eral small-scale mangrove-removal projects, ranging from 1 to 14 ha, were imple-mented from 2007 to 2014. Related projects are all entrusted to NGOs. A large-scale removal project was planned in October 2015. Therefore, two dense mangrove re-gions and a smaller seedling area within the reserve were selected for this study. The northern mangrove region is in the estuary of the Sanxing stream, and the other is in the northern part of the Haishan Fishing Port.

Hsinchu City’s industry is dominated by electronic component manufacturing, among which Hsinchu Science Park is an important pillar of Hsinchu’s economic de-velopment. The most serious threat to the Siangshan Wetland is pollution, its source comes from the inflow of sewage from rivers such as Keya Creek and Yanshui Creek. These pollutions mainly come from the Hsinchu Science Park. For many years, resi-dents living by the wetlands have had a high level of environmental protection awareness. So far, the problem of mangrove forests has also been reported by residents, and the government has dealt with the removal of mangroves in response to public opinion.

4.One of the major weaknesses of this manuscript is a lack of good-quality images. Pretty much all the figures have low resolution and look kind of blurry. Please try to update the figures and improve the resolution.

Ans: Thanks for the reviewer's comments. We have corrected the low resolution figures.

 

  1. There are quite a few equations listed in the manuscript. However, these equations are not supported by any references. Please provide the relevant references to justify the selection of equations and basic modeling assumptions.

Ans: Thanks for the reviewer's comments. We supplement and indicate relevant literature.

 

  1. Figure 2: again the resolution is very low, and it is difficult to read this figure.

Ans: Thanks for the reviewer's comments. We have corrected the low resolution figures.

 

 

  1. Overall, the presentation of the study results seems to be adequate. The only suggestion I have here is to create more supporting discussions where appropriate, so the readers can clearly understand the managerial implications from the conducted work.

Ans: Thanks for the reviewer's comments. We add and supplement this paragraph in the Section 3.2

Some studies have proved that it is possible to express environmental categories or changes. For example, Moraitis et al., (2018) [20] advocate the use of C. gibba as a proxy for eutrophication and the incorporation of this species in monitoring studies through SDM methods. For the Mediterranean Sea they suggest the use of F. hyalinus in SDM as an indicator of environmental stability and a possible forecasting tool for salinity fluctuations [20]. It is possible to screen out some meaningful IS from a variety of plants. through multivariate statistical methods, principal component analysis. These results are conducive to grasping the state of vegetation change and sustainable management under semi-arid rangeland conditions [23]. Cazelles et al (2016) [36] mention that species co-occurrences have been central in community ecology since the foundation of the discipline [36]. They think that a theory of species co-occurrence in ecological networks is needed to better inform interpretation of co-occurrence data. The procedure will analyze the relationship between biotic and abiotic factors for different community mechanisms. When a clear community mechanism is analyzed, it is conducive to policy formulation at the current stage and future maintenance and management. Melinda et al., (2021) [24] found that the interaction between species is increasingly recognized as an important driving factor for the distribution of species, but it is not clear whether changes in the interaction caused by pressure will affect the distribution of species [23].

 

 

  1. The conclusions section should expand on limitations of this study and future research needs. I suggest listing the bullet points.

Ans: Thanks for the reviewer's comments. We add and supplement this paragraph in the Conclusion.

We believe that this research still has limitations, such as the inability to clearly ex-plain the ecological meanings of species-conditional co-occurrence, how to prove that IS is an effective tool for monitoring ecosystems and informing management decisions and how to integrate biodiversity-oriented policies. Especially, it must justify the selection of IS and be able to assess that IS can accurately reflect or predict environmental conditions. At the same time, it shows the quality of the species as a surrogate for its environment, and the relationship between species and ecological variation. Therefore, more research is needed in further.

 

All [page number] and [line number] represented below are referred to the revised manuscript.

 

 

Round 2

Reviewer 2 Report

The authors have adequately addressed my original concerns regarding the manuscript. The quality and presentation of the manuscript have been improved. Therefore, I recommend acceptance.

This manuscript is a resubmission of an earlier submission. The following is a list of the peer review reports and author responses from that submission.


Round 1

Reviewer 1 Report

  The author's concept of a new approach to include conditional co-occurrence probability of species in indicator-species selection is an interesting, but conceptually challenging, idea. Although the fieldwork seems to be set-up with care, I've a series of remarks to improve the understanding and validity of the results and the readability of the paper:
  1. The conceptual link between the observed diversity of crab species and general biodiversity of the assessed wetland areas should be strengthened in the text. The authors now focus too much on putting in a lot of terminogy instead of working out a real scientific hypothesis. Just calculating some "diversity" indices doesn't say a lot about biodversity in general. For a novel approach this link needs to be better worked out, underpinned with clear results, and not just casually mentioned.
  2. The final total used method to come to a series of five species isn't described very clear. Technically it's very clear what the conditional co-occurrence probability method is doing, but as it appears in the text, this isn't the whole methodology. Part of the assessment is also a clustering of species. The role of the clustering in the final method and the clustering method itself needs to be described much more as one method. See my comment about the clustering in the PDF itself 3- Statistically I have some doubts the way the fieldwork seemed to be set-up, but also not with the way the results are presented. For me it's not clear if the sampled areas/locations are all part of a mangrove removal scheme. If this is the case then the short period of time (two years, one with / one without mangrove removal), and the expected potential variabilitiy of all other factors (e.g. temperature, rain, storms, competition etc) over both years can cause a lot of noise in the found number and community type of species. It's very difficult to prove that mangrove removal will be the (only/major?) cause of the differences in numbers and composition of species, since you do not have a series of comparable sites WITHOUT mangrove removal. The Increase in mangrove-removed areas can be caused by be the weather or other normal fluctuation or whatever condition you can think of. ...just looking at it from a negative point of view, but it's important for a scientific paper to consider this. So from my point of view you have to present what you can, but also what you cannot say based on the generated data. Please correct me if did not understand the setup of the experiment, but then it should be written down more clearly.

However even without these results this should not hamper too much the focus of the paper on novel indicator-species selection.

See my comment directly in the PDF

Comments for author File: Comments.pdf

Author Response

                                                                                                                                                            No.59, Hun Shan Rd., Yen Chau Village, Kaohsiung City 824, Taiwan R.O.C.

                                                                                 

08-20-2021

Dear Editors,

 

We would like to submit the research article entitled “Incorporating biodiversity contribution when selecting indica-tor species to monitor restoration after mangrove removal at the Siangshan Wetland, Taiwan” by Chu et al. for publication in Journal of Marine Science and Eenineering.

We sincerely thank the anonymous referees for valuable comments to improve the context of our manuscript. I follow all comments to revise my manuscript, and changes were listed as followed.

 

 

 

Sincerely yours,

 

                        Chun-han Shih

 

             Author to whom correspondence should be addressed;

E-Mail: f92b45028@ntu.edu.tw ;

Tel: +886–7-6158000 ext 3412 Fax: +886–7-6158000 ext 3499.

 

All [page number] and [line number] represented below are referred to the revised manuscript.

Ms. Ref. No.:  jmse-1352909
Title: Incorporating biodiversity contribution when selecting indica-tor species to monitor restoration after mangrove removal at the Siangshan Wetland, Taiwan


Reviewer #1: Comments to jmse-1352909 by Chu et al. (please, also see annotated manuscript):

1) Introduction

1.1) Line 38-41: Whole introduction should be enhanced. it's going in multiple directions without much in-depth / useful information. This may be is true, but as stated here not very informative. What do the terms mean? Why do we need this information here? Then in the next sentence you introduce the term "Target species" and even further in the text "Umbrella species". So this sentence and the parapgrah needs to be clarified / modified / improved.

Answer: We fixed the “Biological indicators have been widely used to assess the effects of environmental impact or biological restoration [1–6]. Generally, indicator species (IS) are used to monitor environmental changes, assess the efficacy of management and provide warning signals for impending ecological shifts [7]. Most IS studies only use a single species as an indicator, and the rest use species groups as indicators [7]. IS, also termed umbrella [8-10], keystone [8,10-12], flagship [8,10,11] or foundation species [12], are living organisms that are easily monitored and whose status reflects or predicts the conditions of their environment [6,13–16]. In other words, the concept of IS is based on the hypothesis that the effects of environmental shifts are reflected in a change in the diversity, abundance or growth rate of species living in a given environment [15–18]. ” line 37-46.

 

 

1.2) Line 59-60: If you try to extract one indicator species covering all species, you are covering ecosystems. What's the difference with an ecosystem approach then?

In your final method you split your selection again selecting not one but five species (since they represent specific habitat conditions). So, what's hypothesis of the added value of using this method?

Answer: We have followed your comments and read related articles, and second and third paragraphs in introduction have been corrected. We fixed the “Ecologists or engineers select indicator species for the efficient assessment of the effects of management actions and as warning signals for ecological shifts based on their sensitivity to a particular environmental attribute. Selections may also take into account past published research, high abundance, a charismatic, endangered or invasive species character or any combination of these factors [7]. The ecoprofile method designed by Opdan et al. (2008) [27] combines the foundation of an ecosystem with the spatial conditions of a species metapopulation; the goal of this method is to integrate a suite of species as the core patterns of an ecosystem to allow the aspiration level to be modified during the planning process. This process infers a set of prerequisites for the effective use of biodiversity target setting methods, which can help multi-stakeholder decision making. ” line 71-80.

 

 

1.3) Line 61-63: Isn't this a clear definition of how umbrella species or "ecoprofiels" are defined?

Answer: We have followed your comments and read related articles, and second and third paragraphs in introduction have been corrected. We fixed the “Kuo et al. (2010) [6] defined indicator species as those whose presence denotes a large number of naturally co-occurring species, and they used algorithms of maximum co-occurrence probability to identify these candidates. Here, co-occurrence probability was defined based on the species that were found together in the same sites. However, it is not possible to distinguish such a relationship among species when using calculated joint probabilities. ” line 80-85.

We fixed the “The ecoprofile method designed by Opdan et al. (2008) [27] combines the foundation of an ecosystem with the spatial conditions of a species metapopulation; the goal of this method is to integrate a suite of species as the core patterns of an ecosystem to allow the aspiration level to be modified during the planning process. This process infers a set of prerequisites for the effective use of biodiversity target setting methods, which can help multi-stakeholder decision making.” line 75-80.

 

 

1.4) Line 69-73: "probabilities and expected values" of what? Existence? habitat prevalence? Environmental conditions? "....it is useful to put a specific condition on an appropriate random variable when calculating the desired probability or expectated value"

Answer: We have followed your comments, and fourth paragraphs in introduction has been corrected. We corrected these errors. We have followed your comments, and fourth paragraphs in introduction has been corrected. We corrected these errors. We fixed the “First, we calculate the presence probability of each species as a condition against other species to appear at the same time, and then further add up the sum of the probability of other species with this species as the condition. This allows for the calculation of probabilities and expected values when only partial survey data are available. We therefore establish the co-occurrence probability of each species with other species. Second, we compare the cumulative co-occurrence probability of each species as judgments, and choose the one with the highest co-occurrence probability as the indicator species. Third, this study hopes to use the selected indicator species as a monitoring tool during the mangrove removal project in the Siangshan Wetland Conservation Area, Hsinchu, Taiwan. ” line 88-97.

 

 

2) Materials and Methods

2.1) Line 77-81: " Improve the English (punctiation, grammar).

 

Answer: We corrected these errors. We have used the English editors recommended by the journal.

 

2.2) Line 88: "Better explain why mangroves are considered to be an invasive species, and why prevention of expansion of mangroves in this area are is a priority. The global decline in mangrove area is considered a great issue for maintaining coastal biodiversity.

Answer: We have followed your comments and read related articles, and second and third paragraphs in introduction have been corrected. We fixed the “According to the "2011 National Important Wetland Ecological Environment Investigation and Rehabilitation Project—Hsinchu City Wild Animal Sanctuary Habitat Rehabilitation Program", as the mangroves continue to expand, the government will adopt mechanical methods to cut them down and transport them to an incinerator by truck. At this point, these implementations did not seem to solve the continuous expansion of mangroves. ” line 117-122.

 

 

2.3) Line 94-98: irrelevant sentence.

Answer: This sentence wants to express the situation in 2011. We have rewritten and corrected.

 

 

2.4) Line 132: What's "high" biodiversity? explain.

E.g.: When biodiversity is high, it means there are many different types of organisms and species, therefore indicator species are defined as those whose presence ..... etc.

Make it clear for the reader what you mean with this kind of terminology.

Answer: We have followed your comments and paragraph 2.5 has been corrected. We fixed the “Because conservation of high biodiversity is a fundamental goal of ecological restoration, indicator species are defined as those whose presence denotes the maximum number of naturally conditionally co-occurring species. The IS should appear in habitats with high biodiversity in either a particular habitat, community or ecosystem. We therefore formalize the quantities that can be calculated from species survey data to establish a quantitative method that may be used to determine an indicator species. For selecting indicator species, we use the concept of maximum conditional co-occurrence probability. ” line 132-138.

 

2.5) Line 134-138: So maximum probability of co-occurence in crab species is per definition a good indicator of high(er) ecosytem biodiversity? Proof should be given (references??). May be, may be not. It's merely about the definition you use. Are wetland ecosystems having more, and more diverse, crab species showing a better ecosystem performance? We have Alpha, Beta, Gamma and Temporal diversity, It's not clear to me why selecting the species with the highest co-occurence will give per definition a better indicator for higher ecosystem biodiversity values. Technically the method is clear, although later you also include clustering techniques to select groups, which you should also mention in "the model".

Answer: We have followed your comments and read related articles, and second and third paragraphs in introduction, paragraph 2.5 has been corrected. We fixed the “Usually, the conservation of higher biodiversity is a fundamental goal of ecological restoration. When biodiversity is high, it means there are many different types of organisms and species present, meaning greater biodiversity in ecosystems, species and individuals, leading to greater stability. Therefore, indicator species are defined as those whose presence denotes the maximum number of naturally conditionally co-occurring species. The IS should appear in habitats with high biodiversity in either a particular habitat, community or ecosystem. In addition, an umbrella species is defined as a species whose conservation is expected to confer protection to a large number of naturally co-occurring species; this concept has attracted greater attention in recent years because it provides a tool for the conservation of biodiversity [32]. When one protects the living environment of an asylum species, one also protects other species within this habitat. An umbrella species is usually widely distributed in a habitat and can show the needs of some or all species that inhabit the same locale. In other words, the habitat needs of this species are similar to those for other species living in the same community. Thus, when it is ensured that these groups can survive, the survival of other species in the same habitat is also stable. With limited funds, knowledge and time constraints, the most efficient conservation plan must be adopted to maintain biodiversity. However, it is difficult to comprehensively study all species in a given ecosystem, so scientists can only focus on some specific species, and asylum species play an important role in these studies. ” line 162-180.

 

  1. Results and discussion

3.1) Line 173-174: ...but not that mangrove removal was the cause, since you do not have a series of comparable sites WITHOUT mangrove removal. Increase can be caused by be the weather or other normal fluctuation or whatever condition you can think of. ...just to look at it from a negative point of view.

Answer: Thanks for the reviewer's comments.

1.Transect A is located in the mangrove area, transect B and transect C are located in the non-mangrove area, and the three transect positions are designed by experimentally consideration to compare the differences in mangrove removal.

  1. The simultaneous changes in the number of three transects represent seasonal changes. This tells us that the number of species appears less in winter and more in summer. As in your opinion, this increase can be caused by be the weather condition.
  2. A1, A2, A3, and A5, the number of mangroves is significantly increased after mangroves removal. Although the number is less than B1, B2, B3 and B5, it still takes time to change the bottom quality, and the species still needs time to move and breed.

 

 

3.2) Line 195-196: No based on your approach you cannot say this!.

It indicates just and increase in the diversity of crab species.

Answer: We have corrected it to “These results of transect A illustrate that both indices increased after mangrove removal, indicating an increase in biodiversity.”

 

 

3.3) Line 220-221: What does the circle mean? similar communities?

Answer: In order to avoid misunderstandings, we have deleted and corrected it.

 

 

3.4) Line 220-221: Figure is unreadable, but very important, since the decision to select 1, 3, 5 or more species/groups. Clustering can be done in many different ways and it's not clear how a clustering method was chosen (figure caption says 'group-average linking of Bray-Curtis similarities" and why this method was considered to be reflecting the species clusters of interest.

Also not clear how this affects the "method". I think selection of nr. of groups is quite decisive compared to selection of species with the highest occurrence, but also heavily depending on the used method.

Answer: We have removed it and repaint.

 

 

3.5) Line 228-232: What's finally "the model"

1 - maximum conditional co-occurrence probability

2 - hierarchical clustering of monthly crab communities based on these probabilities

Reading the article, just doing step1 will not result in a useful selection, so step2 is needed.

Answer: We have completed four steps, and the results are shown in Table 1.

We have corrected it to “The maximum conditional co-occurrence probability, equation 1-4, was used to identify the most suitable indicator species include M. brevidactylus, M. banzai, U. arcuata, U. lacteal, U. borealis and H. formosensis.”

 

 

3.6) Line 232: So....

Answer: We have corrected it to “which clearly shows that the sorting varies monthly and seasonally.”

 

 

3.7) Line 238: What about the significance of the differences? As far as I understand ALL the selected sites were part of a mangrove removing regime (but mangroves were not everywhere present "A1, A2, A3 and A5 were in the densely forested mangrove regions"). So NO non-mangrove removed sites were selected in both years to compare the 2015 and 2016 situation. This is important to correct for yearly fluctuation in each population/species. So, basically we could simply look at a temporal fluctuation which is a normal situation between different years, and the increase is comparable in areas WITHOUT mangrove removal (you didn't sample). This could even be the case if we see the differences over regions A, B and C? If so, it's very difficult to say something statistically meaningful. I hope not...

Answer: We have corrected the content of the entire paragraph.

 

3.8) Line 261: If this is the case you also would expect lower densities in 2016 in the "nearby areas", since they returned to their original habitats. I do not see this in the results, or are the "nearby"areas not part of the sampled regions. In that case, you cannot say anything about this. What are these "nearby" areas, apparently suitable habitat where they can survive..... “these benthic organisms were forced to migrate from their original habitat to nearby ar-eas when the mangroves invaded”

Answer: In the past, the mangrove forest has not yet expanded, and we have other plans to investigate. "These benthic organisms were forced to migrate from their original habitat to nearby ar-eas when the mangroves invaded" is identifiable. And this time, it is also clearly observed that they gradually return to their original places.

 

 

3.9) Line 274-275: This is of course THE key finding of the paper. Where is this information?

Which table or figure refers to this "Strong relation"?

Answer: We have corrected the content of “The biodiversity indices calculated for the sites further indicate a strong relationship between biodiversity and these selected indicator species.”

 

 

 

3.10) Line 280-283: yes of course! if yo want to say something about biodiversity in general.

Answer: We quote Pander and Geist [28] (2013) to support our research.

 

 

 

3.11) Line 286-287: So, what is then finally the added value of your more complex indicator selection, if it not includes spatial- / ecosystem scale. This is also related to my earlier comments about "biodiversity". At what scales, for which (eco)systems?

Answer: We very much agree with your opinions and suggestions.

 

 

 

3.12) Line 288: Why not showing all sites here?

Answer: There are several reasons for this:

We use the sampling sites nearby the mangrove removal, it can easily see the changes.

Secondly, it is not easy to discuss the relationship between the farer sampling sites such as transect C.

Thirdly, the sandy environment and species are also different in the long-distance survey points.

 

 

  1. Conclusion

4.1) Line 305: How? otherwise it's an empty statement

Answer: We delete these sentences.

 

 

Author Response File: Author Response.docx

Reviewer 2 Report

This is a well-written manuscript and I have no suggested edits regarding writing style. The topic is presented well and the methodology is sound. My concern with the project is that there is a seasonally consideration at play that cannot be discounted when assessing the changes occurring among the sampling sites. Perhaps the appearance of crabs in the restored sites is simply related to season and not removal of mangroves. Do data exist allow comparative analyses for the same seasons in different years? If not, I think the paper needs to dive deeper into explaining why the results are not simply a reflection of seasonal change. On Figure 7, is it possible to indicate when the removal occurred?

Author Response

                                                                                                                                                            No.59, Hun Shan Rd., Yen Chau Village, Kaohsiung City 824, Taiwan R.O.C.

                                                                                 

08-20-2021

Dear Editors,

 

We would like to submit the research article entitled “Incorporating biodiversity contribution when selecting indica-tor species to monitor restoration after mangrove removal at the Siangshan Wetland, Taiwan” by Chu et al. for publication in Journal of Marine Science and Eenineering.

We sincerely thank the anonymous referees for valuable comments to improve the context of our manuscript. I follow all comments to revise my manuscript, and changes were listed as followed.

 

 

 

Sincerely yours,

 

                        Chun-han Shih

 

             Author to whom correspondence should be addressed;

E-Mail: f92b45028@ntu.edu.tw ;

Tel: +886–7-6158000 ext 3412 Fax: +886–7-6158000 ext 3499.

 

All [page number] and [line number] represented below are referred to the revised manuscript.

 

 

Ms. Ref. No.:  jmse-1352909
Title: Incorporating biodiversity contribution when selecting indica-tor species to monitor restoration after mangrove removal at the Siangshan Wetland, Taiwan


Reviewer #2: Comments to jmse-1352909 by Chu et al. (please, also see annotated manuscript):

This is a well-written manuscript and I have no suggested edits regarding writing style. The topic is presented well and the methodology is sound. My concern with the project is that there is a seasonally consideration at play that cannot be discounted when assessing the changes occurring among the sampling sites. Perhaps the appearance of crabs in the restored sites is simply related to season and not removal of mangroves. Do data exist allow comparative analyses for the same seasons in different years? If not, I think the paper needs to dive deeper into explaining why the results are not simply a reflection of seasonal change. On Figure 7, is it possible to indicate when the removal occurred?

Answer: Thank you reviewer for your suggestion. We fixed the “2.3. Biological survey and experimental design. In this study, crabs were sampled monthly from October 2015 to September 2016. The A, B and C survey transects ran from north to south, and 5 sampling sites were positioned along each transect, resulting in 15 sampling sites as shown in Figure 1. Transect A was designed to understand the occurrence of species in the mangrove area. On the contrary, the sections B and C were designed to understand the occurrence of species in non-mangrove areas. Sites A1, A2, A3 and A5 were in the densely forested mangrove regions. A4 was located in the sparse mangrove seedling area. The three transects of space could help understand how species distribute and change in space, especially the changes before and after the removal of mangroves. Monthly sampling and spatial comparison could also help clarify the seasonal effects of species. ” line 130-147.

 

 

 

Author Response File: Author Response.docx

Round 2

Reviewer 2 Report

Line 130, delete second mention of "experimental design"

Line 230, are you talking about density at the non-mangrove sites or at the mangrove removal sites? It is not clear.

Lines 233-235, since you acknowledge that the species numbers change over season, how can you be certain the changes in density reflect mangrove removal rather than seasonal change?

Lines 242-244, again, it is not clear if you are talking about the non-mangrove sites or the mangrove removal sites. Why would we care about changes in biodiversity of the non-mangrove sites after mangrove removal?

It would help if the timing of mangrove removal were indicated throughout the paper. For example, in Figure 6, indicate the period of mangrove removal. Was the removal completed by Feb?

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