Who’s Next? Non-Indigenous Cnidarian and Ctenophoran Species Approaching to the Italian Waters
Round 1
Reviewer 1 Report
Review
Paper title: Who's Next? Non-indigenous Cnidarian and Ctenophoran Species Approaching to the Italian Waters
The Mediterranean Sea is an important area in terms of fish production, aquaculture activities, potential for tourism, and ecosystem services. Biological invasions are today considered one of the most serious threats to biodiversity and habitat destruction. In Europe, impacts of biological invasions are considered as one of the many variables to address in management decisions. The number of introduced species is one of the descriptors needed for assessing ecological status of an area. Because the information concerning potential biological invaders belonged to the types Cnidaria and Ctenophora (CC NIS) is still lacking, the authors provided a survey of already confirmed CC NIS and created a list of the species which have the potential for introduction in Italian waters. Such information is important for the management of NIS.
All these reasons explain the relevance of the paper by Cinzia Gravili and Sergio Rossi submitted to "Water".
General scores.
The data presented by the authors are significant. The authors considered and comprehended relevant literature sources to provide an excellent overview in this field. We authors conducted careful work which will attract the attention of a wide range of specialists including scientists, stakeholders, and managers focused on biological invasions.
Specific comments.
I think that “Review” or "Opinion" is a more suitable article type for this paper than “Article” particularly as the authors mentioned that “The aims of the present paper were to review…” (Abstract).
Introduction
P 2-3. There no data about the central object of this study – cnidarian and ctenophore species. Their importance, role, potential negative impacts on their new habitats are not presented. Why the authors selected these groups? This should be described clear and precise.
P 2. The authors should consider replacing the text “The Italian Peninsula, in fact, is a biogeographical Mediterranean crossroads placed between the eastern and western basins, hosting more than 160 marine and brackish NIS along its coastline [39].” at the beginning of the section.
Methods
P 3. The last sentence of "Materials and methods". The authors should provide a detailed description of the methods they used to identify the species that have the potential for spread into Italian waters.
As I can imagine there were the following stages. 1) Summarizing the data about CC NIS in Italian waters. This information is well described above. 2) Determination of the donor regions for the CC invaders. 3) An analysis of CC biodiversity data in each region. The authors should provide here the sources they used (papers, checklists, on-line databases, etc) 4). Determination of new potential Italian invaders according to the data about CC invasive species in neighboring regions.
Also, the authors should clearly explain how they identified the "Invasiveness" of the potential invaders. It is unclear which species have "low" invasiveness and which species have "high" invasiveness.
Results
P 5. Figure 3. As I can see from this figure, there was a peak of new introductions in 1980–1984. The authors should provide explanations for this pattern in the Discussion.
Also, the data presented here are not continuous and, therefore, the use of curves is incorrect. Histograms are more suitable for such data. I suggest to re-draw this figure.
P 6. Table 1. The authors indicated "unknown" main way of introduction for some species. Can these species be considered as potential invaders in such a case? Please, clarify.
Discussion
Table 1 is the core of this study but it is not well discussed in the paper.
Moreover, the authors did not provide the response to their intriguing question "Who's next?". I think in the discussion they should indicate 1–3 species from their list which are expected to arrive into the Italian waters in the near future (probably according to their invasiveness, or the distance from a region where their introductions were registered to the nearest Italian sites, etc).
P 10. The sentence " These are generally factors not detectable by studies carried out on a single species or habitat, such as intrinsic characteristics of the system allowing a demographically successful of NIS population or the presence of external factors acting on the communities [94,95]." is difficult to understand. Please, rephrase.
References.
Reference [57] is the same as [61].
References [156–201] are not presented in the MS. Because the authors cite these sources in their Supplementary table, they should exclude these from the text and include them in the supplement.
Supplementary table.
The information for Species 1–97 is provided in alphabetical order. Species 98–99 are outliers. Please, correct.
I have also made some text revisions in the draft (see attached file).
Comments for author File: 
Comments.pdf
Author Response
Response to Reviewer 1 Comments
Point 1: I think that “Review” or "Opinion" is a more suitable article type for this paper than “Article” particularly as the authors mentioned that “The aims of the present paper were to review…” (Abstract).
Response 1: We agree with the Reviewer: Review is a more suitable article type for this paper and we now submitted again the manuscript as such.
Introduction
Point 2: P 2-3. There no data about the central object of this study – cnidarian and ctenophore species. Their importance, role, potential negative impacts on their new habitats are not presented. Why the authors selected these groups? This should be described clear and precise.
Response 2: This sentence was added in the introduction to satisfy the query:
‘In this study, the Mediterranean non-indigenous species of the taxa Cnidaria and Ctenophora (CC NIS) have been considered as a good proxy for changes in biodiversity in the plankton and in the benthos, because of their structuring and functional roles. They inhabit all aquatic ecosystems displaying a wide array of life-cycle strategies with potential negative impacts on biodiversity, ecosystem, tourism, fisheries, fish farms, and power plants. Their native distribution and the main introduction pathways have been examined jointly to time trends of species introductions in relation with the prevailing native distribution areas.
Point 3: P 2. The authors should consider replacing the text “The Italian Peninsula, in fact, is a biogeographical Mediterranean crossroads placed between the eastern and western basins, hosting more than 160 marine and brackish NIS along its coastline [39].” at the beginning of the section.
Response 3: The sentence was changed:
‘Moreover, evaluation of their invasiveness, also through the analysis of some case studies, could allow anticipatory NIS forecast based on biogeographical and ecological analyses of the CC NIS identified as good candidates to become future immigrants of Italian waters that, to date, host more than 160 marine and brackish NIS along its coastline [39].’
Materials and Methods
Point 4: P 3. The last sentence of "Materials and methods". The authors should provide a detailed description of the methods they used to identify the species that have the potential for spread into Italian waters.
Response 4: The sentence has been changed:
‘Finally, CC NIS have been investigated through the evaluation of their invasiveness (depending on the species ability to rapidly conquer new spaces, spread and generate various impacts) by identifying the possible future immigrants of the Italian waters, and considering also the distribution of CC NIS already established in the Italian seas through the following steps: 1) summarize the data about CC NIS in the Italian waters; 2) determine the origin regions for the CC invaders; 3) analyze CC biodiversity data in each region; 4) determine of new potential Italian invaders according to the data about CC invasive species in neighbouring regions (information extracted from Appendix A).’
Point 5: Also, the authors should clearly explain how they identified the "Invasiveness" of the potential invaders. It is unclear which species have "low" invasiveness and which species have "high" invasiveness.
Response 5: The Invasiveness was defined in Material and methods (p. 2) where ‘invasive’ (able to disseminate from their area of initial introduction).
Moreover, (p. 3) this sentence has been added: “Finally, CC NIS have been investigated through the evaluation of their invasiveness (depending on the species ability to rapidly conquer new spaces, spread and generate various impacts) by identifying the possible future immigrants of the Italian waters……”
Results
Point 6: P 5. Figure 3. As I can see from this figure, there was a peak of new introductions in 1980–1984. The authors should provide explanations for this pattern in the Discussion.
Reponse 6: Following the advise of the reviewer, this sentence has been added in the Discussion:
‘A surge in the records in the 1980s reflects probably the publication of the results of specific programs in the Levant Sea in which the target was looking for new introduced species (see Galil [67] for more details). Moreover, the increase in shipping transported CC NIS may be attributed to the increase in shipping volume throughout the Mediterranean basin resulting in new shipping routes, a result of a significant shift in global economy trends. In the same way, the increase in commercial introductions follows the increase of shellfish production in aquaculture facilities [68].
Point 7: Also, the data presented here are not continuous and, therefore, the use of curves is incorrect. Histograms are more suitable for such data. I suggest to re-draw this figure.
Response 7: Figure 3 has been changed using histograms as suggested by the reviewer.
Point 8: P 6. Table 1. The authors indicated "unknown" main way of introduction for some species. Can these species be considered as potential invaders in such a case? Please, clarify.
Response 8: Yes, also if the main way of introduction, at the moment, is unknown for some species, other factors, as the origin region and the diffusion in neighbour areas adjacent to the Italian seas, makes these species probable potential invaders of the Italian waters.
Discussion
Point 9: Table 1 is the core of this study but it is not well discussed in the paper.
Response 9: Table 1 has been considered throughout the text now, in the updated version is properly discussed.
Point 10: Moreover, the authors did not provide the response to their intriguing question "Who's next?". I think in the discussion they should indicate 1–3 species from their list which are expected to arrive into the Italian waters in the near future (probably according to their invasiveness, or the distance from a region where their introductions were registered to the nearest Italian sites, etc).
Response 10: In the discussion 3 species (Macrorhynchia philippina, Oulastrea crispata and Eucheilota paradoxica) have been indicated as species expected to arrive into the Italian waters.
These sentences have been added to respond to the referee’s comment:
According to the CC NIS invasiveness, and the distance from a region where their introductions were registered, three of the fifteen CC NIS potential invaders of the Italian waters (Table 1) deserve special attention.
The first species, Macrorhynchia philippina Kirchenpauer, 1872, native of the southern Pacific Ocean region, is one of the alien hydroid species most widely spread and well established in the Levant Sea [116,138]. This Lessepsian invader, found in shallow waters, can create dense populations and has been recorded also in the Aegean Sea introduced by shipping [78,138] being characterized by a high invasive potential. It is now a worldwide species in all tropical and sub-tropical oceans [66] and there are also records from temperate regions [79]. M. phylippina is a stinging species and the increase of its density and abundance in the Mediterranean basin could have a negative impact on local economies [78,138].
The second species, Oulastrea crispata (Lamarck, 1816), a non-indigenous zooxanthellate scleractinian coral, has been found in shallow water on the west coast of Corsica [158]. It is a species native on near-shore coral reefs in the central Indo-Pacific and a successful colonizer being able to settle on a wide variety of substrata and utilizes various reproductive strategies. Being widespread in temperate and subtropical waters, it is likely that it will be able to find a suitable temperature regime in the Mediterranean basin for further range expansion due to the ‘tropicalization’ of this area [62].
Finally, the third species, Eucheilota paradoxica Mayer, 1900 is native of the tropical Atlantic region and its medusa stage has been recorded near the Italian coasts (along the Croatian coast [119] and the French coast [124,125] in the ’70s and ’90s, respectively), while the most recent records occurred along the African coasts [128].
Point 11: P 10. The sentence " These are generally factors not detectable by studies carried out on a single species or habitat, such as intrinsic characteristics of the system allowing a demographically successful of NIS population or the presence of external factors acting on the communities [94,95]." is difficult to understand. Please, rephrase.
Response 11: The sentence was rephrased:
‘These factors, not detectable by studies carried out on a single species or habitat, can contribute toward the development to a more complete understanding of the impacts of alien species from an ecosystem perspective [78,94,95].
References
Point 12: Reference [57] is the same as [61].
Response 12: It has been corrected and the references renumbered.
Point 13: References [156–201] are not presented in the MS. Because the authors cite these sources in their Supplementary table, they should exclude these from the text and include them in the supplement.
Response 13: The References not presented in the MS were included in the supplement.
Supplementary table.
Point 14: The information for Species 1–97 is provided in alphabetical order. Species 98–99 are outliers. Please, correct.
Response 14: Species 98 and 99 are outliers and at the end of the table because they belong to the taxon Ctenophora. In the Supplementary table the lines with the indication of the taxa Cnidaria and Ctenophora, respectively, have been added.
Point 15: I have also made some text revisions in the draft (see attached file).
Response 15: Reviewer’s comments were followed updating the manuscript text.
Reviewer 2 Report
In this manuscript a deep review of the knowledge about the Mediterranean non-indigenous species of taxa Cnidaria and Ctenophora (CC NIS) is presented.
In my opinion this is a very interesting work in which a very extensive bibliographic review has been made, that will be very useful for other researchers.
The text is well written and easy to read, what I really appreciate as a reader.
The supplementary file, appendix A, summarizes very well and clearly presents the information of the 98 species reported in the literature.
Figures 1 and 2 are correct but some modifications should be done (comments in the file)
In my opinion, the issue of temporal trends is not well explained. Figure 3 shows the number of new marine NIS introductions in Europe per 5-years intervals. First of all axis names don’t appear in the figure. Please include them. Secondly, I do not see a decreasing trend in the number of introductions, or at least I do not think it is possible to say it simply by looking at the figure. The data are presented as total number of introductions per 5 years interval, and no statistics analysis has been taken in consideration. It’s obvious that for example, the total amount of NIS introduction from Central Indo-Pacific reached its maximum in the period 1970-84, or during 1975-1989 for those from Western Indo –Pacific, but in order to talk about trends, it’s necessary to include some statistical analysis. For example, it could be interesting to calculate the temporal trend of the residuals, and evaluate exactly if this trend is positive or negative.
Some grammatical errors have been detected and are shown in the text as comments. I would like to clarify that this is not a deep revision of the English. In my opinion, English used is correct and appropriate.
Comments for author File: Comments.pdf
Author Response
Response to Reviewer 2 Comments
Abstract
Point 1: p. 1: equipped is correct?
Response 1: Yes, equipped is the word for gifted.
Point 2: Figure 2, p. 2 Increase the size of the axis titles.
Response 2: The size of the axis titles has been increased.
Point 3: Figure 3. Consider changing this figure.
Response 3: Figure 3 has been changed.
Point 4: In my opinion, the issue of temporal trends is not well explained. Figure 3 shows the number of new marine NIS introductions in Europe per 5-years intervals. First of all axis names don’t appear in the figure. Please include them.
Response 4: I included the axis names.
Point 5: Secondly, I do not see a decreasing trend in the number of introductions, or at least I do not think it is possible to say it simply by looking at the figure. The data are presented as total number of introductions per 5 years interval, and no statistics analysis has been taken in consideration. It’s obvious that for example, the total amount of NIS introduction from Central Indo-Pacific reached its maximum in the period 1970-84, or during 1975-1989 for those from Western Indo –Pacific, but in order to talk about trends, it’s necessary to include some statistical analysis. For example, it could be interesting to calculate the temporal trend of the residuals, and evaluate exactly if this trend is positive or negative.
Response 5: We understand the reviewer's point of view in suggesting to deepen the statistical analysis. However, after consulting fellow experts in the statistics field, we remain of the opinion that a descriptive analysis is more appropriate for this type of data, and that more accurate statistical tests cannot be applied. However, the figure was completed by calculating the 3-years moving averages.
Point 6: Some grammatical errors have been detected and are shown in the text as comments.
Response 6: Reviewer’s comments were followed updating the manuscript text.
Round 2
Reviewer 1 Report
Review
Paper title: Who's Next? Non-indigenous Cnidarian and Ctenophoran Species Approaching to the Italian Waters.
Authors: Cinzia Gravili and Sergio Rossi.
Recently I have reviewed this paper and indicated some concerns.
The authors have provided sufficient responses and updated their paper according to my suggestions.
I have no further comments and can recommend this excellent paper for publication in "Water".
