Centers of Endemism and The Potential of Zoos and Botanical Gardens in Conservation of Endemics

Round 1

Reviewer 1 Report

Thanks for your job. I consider that in its current form the manuscript is viable for publication in JZBG.

  In general, the quality of the language and edition is good and I cannot find serious faults

Author Response

Thanks a lot.

Reviewer 2 Report

The review article is quite well written, provides important and necessary information and will serve as a reference to guide objectives in zoos and botanical gardens that promote the conservation of endemic species.

There are few comments on spelling or syntax in the article, for example it is necessary to use a comma after the point in abbreviations (i. e., e. g., ). Missing a space on the line 386.

At the end of the article there is a statement with which I do not agree: "Compared to the benefits of zoos, aquaria and botanical gardens, little is known about the benefits of the regional and global biodiversity for cultural life and wellbeing." It depends on the region but for some countries there is a lot of information about it. For example:

Blancas, J., Casas, A., Ramírez-Monjaraz, H., Martínez-Ballesté, A., Torres-García, I., Abad-Fitz, I., ... & Vallejo, M. (2022). Ethnobotany of the Nahua Peoples: Plant Use and Management in the Sierra Negra, Puebla, Mexico.

Pérez-Valladares, C. X., Velázquez, A., Moreno-Calles, A. I., Mas, J. F., Torres-García, I., Casas, A., ... & Téllez-Valdés, O. (2019). An expert knowledge approach for mapping vegetation cover based upon free access cartographic data: the Tehuacán-Cuicatlán Valley, Central Mexico. Biodiversity and Conservation, 28(6), 1361-1388.

Solís, L., & Casas, A. (2022). Cuicatec Ethnobotany: Plants and Subsistence in San Lorenzo Papalo, Oaxaca.

In addition, there are gardens focused on ethnobotanical aspects (for example, the "Ethnobotanical Garden of Oaxaca, México"). The authors should appropriately review the existing information and based on this modify the text with which the article concludes.

Author Response

The review article is quite well written, provides important and necessary information and will serve as a reference to guide objectives in zoos and botanical gardens that promote the conservation of endemic species.

There are few comments on spelling or syntax in the article, for example it is necessary to use a comma after the point in abbreviations (i. e., e. g., ). Missing a space on the line 386.

This has been corrected.

At the end of the article there is a statement with which I do not agree: "Compared to the benefits of zoos, aquaria and botanical gardens, little is known about the benefits of the regional and global biodiversity for cultural life and wellbeing." It depends on the region but for some countries there is a lot of information about it. For example:

Blancas, J., Casas, A., Ramírez-Monjaraz, H., Martínez-Ballesté, A., Torres-García, I., Abad-Fitz, I., ... & Vallejo, M. (2022). Ethnobotany of the Nahua Peoples: Plant Use and Management in the Sierra Negra, Puebla, Mexico.

Pérez-Valladares, C. X., Velázquez, A., Moreno-Calles, A. I., Mas, J. F., Torres-García, I., Casas, A., ... & Téllez-Valdés, O. (2019). An expert knowledge approach for mapping vegetation cover based upon free access cartographic data: the Tehuacán-Cuicatlán Valley, Central Mexico. Biodiversity and Conservation, 28(6), 1361-1388.

Solís, L., & Casas, A. (2022). Cuicatec Ethnobotany: Plants and Subsistence in San Lorenzo Papalo, Oaxaca.

In addition, there are gardens focused on ethnobotanical aspects (for example, the "Ethnobotanical Garden of Oaxaca, México"). The authors should appropriately review the existing information and based on this modify the text with which the article concludes.

While we acknowledge this sentiment, it would open up the topic to another very big literature survey that is at best tangential to our main objective, which is endemism.We have thus eliminated the whole part of the text relating to this.

Reviewer 3 Report

The manuscript provides a good theoretical contextualization of rarity, endemism, and centers of endemism for several taxonomic groups. Although there is an imbalance between Africa and Europe x Asia and America,  in my opinion, the manuscript has the potential to be published in JZBG. To that, I suggest some modifications and inclusions to the text, as follows.

In the introduction and in the abstract, circumscribe and contextualize the work both for richness and levels of endemism. For example, there is little or none in the North, Central, and South Americas. Figure 2 talks about global richness, but looking for the origin of this information in the entire reference list makes the job very difficult. I suggest a table listing the references by topic (richness) (endemism) (centers of endemism) etc.

As a review article, I suggest comparing the amount of information (references) on each topic to give the reader an idea of the effort that has already been spent (and what remains to be done) on endemism and endemic centers on the continents. 

Bibliographic references: I strongly suggest changing the format of the references. Although it is very interesting to use Roman numerals, it is not efficient for a quick interpretation and search of the references in the text. 246 references to search make the work very time-consuming and discouraging for the reader.

Figure 1: This figure has too much text. I suggest the authors try to synthesize the first part into four levels (changes and threats, both quantitative and qualitative). And also separate the processes endemic x endangered taxa (since one can be only natural and the other can be natural and anthropogenic). The same for the second part. I suggest separating factors that act on the regional pool of species: spatial, climatic, biogeographic... in a more synthetic way.

The picture representing vascular plants is very difficult to visualize. I suggest changing it. The picture for reptiles is not good either. 

Figure 3: I think this figure is a little bit confusing. I suggest including the no-endemic as a rectangle of the same color written no-endemic for each group separately. 

Figure 4: It would be great if it were possible to include an order of magnitude on the level of endemicity to separate the low from the high. Even if it is a numerical interval for low and one for high.

Table 1: I think it would be more intuitive if this table were transposed or presented as one (or more) bar graphs.

The work is unbalanced regarding the theoretical contextualization x the role of zoos and botanical gardens in this context. The authors could further deepen this discussion by analyzing the quantitative and qualitative participation of in-situ conservation (zoos and BGs) for the taxonomic groups treated in these regions.

Author Response

The manuscript provides a good theoretical contextualization of rarity, endemism, and centers of endemism for several taxonomic groups. Although there is an imbalance between Africa and Europe x Asia and America,  in my opinion, the manuscript has the potential to be published in JZBG. To that, I suggest some modifications and inclusions to the text, as follows.

In the introduction and in the abstract, circumscribe and contextualize the work both for richness and levels of endemism.

Absolute richness and level of endemism as percentage value per region or country are important indicators. However, we wanted to review the diversity and meaning of other indicators as well. This is necessary since many publications used different measurements and indicators to characterize endemism and CoEs. We now modified the abstract according to this suggestion, with an emphasis of richness and level/proportion of endemics.

For example, there is little or none in the North, Central, and South Americas.

We cited many publications representing regions and countries all over the world including countries and regions in the Americas. However, in this review we focus primarily on the question what CoEs are, how these are characterized, and - with respect to zoos, aquaria and botanical gardens - how these institutions/organizations can support nature conservation with respect to endemics. Many of the great zoos and botanical gardens are located in cities and, thus, are far away from CoEs, as we have indicated in the text.

Figure 2 talks about global richness, but looking for the origin of this information in the entire reference list makes the job very difficult. I suggest a table listing the references by topic (richness) (endemism) (centers of endemism) etc.

Fig. 2 represents species numbers of several groups of organisms at global scales. We now transferred the refs. from the text to the heading of Fig. 2. Clearly, the numbers differ with respect to authors and calculation. On the other hand, the accuracy of the numbers is not that important since they depend on the species concept used and these concepts are seldom overtly articulated in such publications.

As a review article, I suggest comparing the amount of information (references) on each topic to give the reader an idea of the effort that has already been spent (and what remains to be done) on endemism and endemic centers on the continents.

We wanted to give an overview and open the discussion about the meaning of CoEs including different definitions and modes of calculation. Second, we tried to find out how endemism, CoEs, zoos, botanical gardens and aquaria interrelate. As indicated in our opening paragraph abovem to discuss what remains to be done is another long story. In any case this suggestion would require us to search for, and synthesize much more literature, diluting the focus of our paper.

Bibliographic references: I strongly suggest changing the format of the references. Although it is very interesting to use Roman numerals, it is not efficient for a quick interpretation and search of the references in the text. 246 references to search make the work very time-consuming and discouraging for the reader.

We always used normal arabic numbers for citation in the text. It may be that the numbers changed via the submission process. Clearly, we NEVER used Roman numerals. Again, we changed the numerals back and hope that NO Roman numerals find their way to the editors. Furthermore, if we are not successful, the editors and professionals can change the mode in a few moments.

Figure 1: This figure has too much text. I suggest the authors try to synthesize the first part into four levels (changes and threats, both quantitative and qualitative). And also separate the processes endemic x endangered taxa (since one can be only natural and the other can be natural and anthropogenic). The same for the second part. I suggest separating factors that act on the regional pool of species: spatial, climatic, biogeographic... in a more synthetic way.

We reworked the figure according to the suggestion. Now the text in the figure is reduced by 58 % to a minimum. As a result it is very compact.

The picture representing vascular plants is very difficult to visualize. I suggest changing it. The picture for reptiles is not good either.

We replaced the two pictures with vascular plants and reptiles, and reworked all figures along the suggestion of all reviewers.

Figure 3: I think this figure is a little bit confusing. I suggest including the no-endemic as a rectangle of the same color written no-endemic for each group separately.

We reworked Fig 3 according to reviewers 3 and 4, and added Costa Rica with respect to the representation of the Americas. We would like to make it clear that it is not our intention to present all continents in an equal manner, but only to show a few examples to give an idea. Hopefully with percentage values the message now is clearer.

Figure 4: It would be great if it were possible to include an order of magnitude on the level of endemicity to separate the low from the high. Even if it is a numerical interval for low and one for high.

As can be figured out with respect to Fig. 3, the differences often work in the same direction, but can differ widely. E.g., Austria has 18 % non-marine gastropods, Hawaii 98%, Austria has 1 % endemic vascular plants, Hawaii 78% (more or less -  the numbers change with level of knowledge). However, what we wanted to demonstrate is that the order is often the same or similar. It is impossible to give concrete numbers in this figure because one can easily find regions with zero or nearly 100 % for each group of organism.

Table 1: I think it would be more intuitive if this table were transposed or presented as one (or more) bar graphs.

We think that converting this to a figure with bars is not convincing as these are the result of different modes of calculation, taxonomic groups and regions. It was intensive work (years) to collect all these numbers. However, in the end these are examples indicating the diversity of current methodologies and regions. We have thus retained the Table.

The work is unbalanced regarding the theoretical contextualization x the role of zoos and botanical gardens in this context. The authors could further deepen this discussion by analyzing the quantitative and qualitative participation of in-situ conservation (zoos and BGs) for the taxonomic groups treated in these regions.

This is obviously an excellent idea, but as indicated in our opening one which diverges from our focus, which is on endemism.This proposed would be a topic for another review. However, we have put this suggestion in the text as an area of propose further research.

Reviewer 4 Report

Dear Authors,

Thank you for submitting this paper that explores species endemism and the role or the zoo and aquarium in their conservation. I found your manuscript to be engaging and several well considered points are made. The argument is well considered in some respects and the background on species endemism is well considered. There are several areas of this manuscript that require considerable revision, however. I have added specific comments to the manuscript: please also see the key areas to focus on below:

1. Legislation. The most important point that is currently missing in this manuscript is the consideration of barriers. While you have considered why it is important to keep, and manage, endemics, the discussion as to why this is less common is not included. Please provide some depth on legislation impacts (e.g. CITES) that may prevent importation, along with consideration of future directions. Consideration of husbandry needs (e.g. specialist endemics for narrow habitats / niches may be less tolerant of a range of husbandry styles.

2. Purpose and outcomes. As readers of this work are likely to be of a zoo / aquarium audience, please explain how your findings could be applied.

3. References and citations. Please ensure these are reformatted to the stylistic requirements of the journal.

4. Methods. Currently, I am unsure if this is a review; it seems more of an opinion piece. Either structure as a review (e.g. explain briefly what search terms) or structure into a different style of manuscript.

With these revisions the work should be in a stronger position overall.

Comments for author File: Comments.pdf

Author Response

Dear Authors,

Thank you for submitting this paper that explores species endemism and the role or the zoo and aquarium in their conservation. I found your manuscript to be engaging and several well considered points are made. The argument is well considered in some respects and the background on species endemism is well considered. There are several areas of this manuscript that require considerable revision, however. I have added specific comments to the manuscript: please also see the key areas to focus on below:

1. Legislation. The most important point that is currently missing in this manuscript is the consideration of barriers. While you have considered why it is important to keep, and manage, endemics, the discussion as to why this is less common is not included. Please provide some depth on legislation impacts (e.g. CITES) that may prevent importation, along with consideration of future directions. Consideration of husbandry needs (e.g. specialist endemics for narrow habitats / niches may be less tolerant of a range of husbandry styles.

As with several other comments, we agree that such a discussion would be most interesting, but is better addressed as a review in its own right. Independent of legislation, which should also be discussed by other experts, we have shown that the possibilities and information networks of zoos, aquaria and botanical gardens could be intensified. On the other hand, the representation of endemics is definitely limited e.g., with respect to the legislation or taxonomic group, and would most likely be highly country-specific. The representation of endemic invertebrates e.g. might be possible in the case of some endemic butterflies because of their attractiveness. In other cases this is impossible because of lack of knowledge, legislation, costs and motivation of vistors (?). However, we are no experts in this field. We tried to highlight some examples since a representation of systematic studies on this topic may not be available and would be a little bit out of the focus of our review.

2. Purpose and outcomes. As readers of this work are likely to be of a zoo / aquarium audience, please explain how your findings could be applied.

We now have enhanced the discussion in the last part of our review. Nevertheless, this is only possible in general terms.

3. References and citations. Please ensure these are reformatted to the stylistic requirements of the journal.

Yes, we have been working hours and hours to do our very best. We now checked the reference list again. We additionally asked the editors and experts of MDPI, and got the information that they will correct the reference list as a last step wherever this is necessary.

4. Methods. Currently, I am unsure if this is a review; it seems more of an opinion piece. Either structure as a review (e.g. explain briefly what search terms) or structure into a different style of manuscript.

This is an interesting comment, and not easy to address. We acknowledge that in part it is an opinion piece, but more overtly a review with a series of (not exhaustive) examples, We thus feel that it is not easy to adapt the manuscript with respect to this statement. Our goal was to give an overview about CoEs, and the ex situ conservation of the diversity of a range of endemic taxa. With respect to the topic of the journal and the invitation of the editors of the special issue, we tried to describe some aspects in the middle of the triangle of  CoEs (definition, indication) - endemism/endemics (different groups) - zoos/aquaria/botanical gardens (presentation, possibilities, limitation).

With these revisions the work should be in a stronger position overall.

Answers and comments to remarks of reviewer 4 in the document.

Line 16/17

Provide a clearer explanation of the purpose of your review.

We now reworked the abstract to make the purpose clearer.

Line 21/22

explain this point further.

We have tried to better explain this in the last part of the review.

Line 29/30

incorrect format: this should be [1-3]

We tried to change the format of "[1, 2, 3]" to "[1-3]", and invested more than two hours to solve only this problem of formalities. Afterwards we asked the editors/MDPI professionals. The answer was that they can easily change this mode of citation.

 Line 46

The full term is needed on first mention

We now formulated the text in a more common way.

Line 49/50

Please explain and name these more carefully

This is complicated because a quantification of "range" and "rarity" has been part of an ongoing discussion. We did not want to go into detail because otherwise the publication would become too large. We feel we wish to retain our text as it is We have cited two very important publications where many problems of and implications of "rarity" have been discussed in detail.

Line 56/57

check wording here - what is a narrow endemic?

We changed the term to "endemic" without "narrow" because the meaning of the term "narrow endemics" which indeed is also used in different ways, is not that important here.

Line 94

Explain more clearly what this figure is and how and from where it was developed

We have now transformed this figure in a somewhat more general form.

Line 99

Give some examples of the criteria for CoEs. You can then bring in the fact that this varies later, but the lack of a true definition is challenging.

We gave a definition in the first sentence (line 97) and cited five refs. We now added two examples in the second sentence.

Line 151

citation is needed

We added a citation.

Line 156

include supporting citations when including information that is not common knowledge

We added a citation.

Line 169

include citations here

We added a citation.

Line 176

Be specific here on the sources of information. This is diffictult to interpret: what is green, blue or the pictures? There are no x or y axis labels, and some taxa are omitted?

To make it more clear and specific we have now defined the colors exactly. The x-axis is defined by the name of taxonomic groups plus symbols, and the y-axis by species numbers. These are estimates representing the current knowledge.

Line 184

Based on proportions or richness?

This is now specified.

Line 186/187

cite here

Is cited now.

Line 196/197

This needs to be more clearly explained. Is this presence / absence?

To make the figure more clear, we totally reworked the image and heading. We added Costa Rica because one reviewer critized the lack of regions of the Americas and we added percentage values.

Line 201

This needs to be more explicitly stated. Do you have supporting values?

This is just a hypothetical order reflecting the differences and orders in Fig. 3. It will be interesting to get further numbers of level of endemism from other regions in the world.

Table 1

what is div?

We now have written "diverse" in the table.

Line 234

explain the term on first mention

The sentence includes a definition now.

Line 244

support with citations as evidence

We added two refs.

Line 278/279

This argument is self-evident as animals endemic to an island have to therefore be endemic to the archipelago if viewed from this level. Consider argument structure.

Yes, every endemic of an island is at the same time endemic to the archipelago. However, the degree of endemism of an island or archipelago depends on both, the amount and composition of endemics and non-endemics. And also the composition of non-endemics normally differs from island to island. Thus, also the number of non-endemics is important for the level of endemism of an island and archipelago. Theoretically, the level of endemism of an island can be higher than the level of endemism of the whole archipelago, even if this is not very likely. To make this more clear, we now added a few sentences.

Line 312

include supporting citation

This is now included.

Line 315

Not quite - it shows a dwindling average number of species of birds.

This is now corrected.

Line 324

as a very

Yes, thank you very much. We corrected this part of the text according to your recommendation.

Line 353/354

Very true - include supporting citation here.

We added a ref. here.

References 1

These shoud be formatted as numbers. Please see author guidelines or a published paper and revise accordingly.

We already used the numerals according to author guidelines. Hopefully, the arabic numbers will not change to Roman ones during the submission process.

References 2

Check author spacing as per author guidelines.

We checked author spacing again, and corrected a few citations again.

References 3

Please include the dois consistently.

We intensified the search and added dois wherever we found these numbers. According to personal MDPI information, it is not necessary to give the doi in every case, and the organization will help.

References 4

pages, volume?

This information is now added.

References 5

no need for 'and' here

Please see guidelines and ensure reference style is consistent

The 'and' is now eliminated.

References 6

check initials and punctuation

We checked the intials and punctuation, and corrected the citation.

References 7

Journal is just called Zoo Biology

This has been corrected.

References 8

spacing

We tried to correct the style according to formalities, and were not successful in this case. Hopefully, MDPI will be able to do this within a short time (seconds).

References 9

pages?

Numbers are now added.

Round 2

Reviewer 3 Report

I am pleased with the changes in the manuscript. I think this article opens up possibilities to further explore the functions of ex-situ collections in the context of endemism and endangered species also.