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Peer-Review Record

Parasites in Imported Edible Fish and a Systematic Review of the Pathophysiology of Infection and the Potential Threat to Australian Native Aquatic Species

Diversity 2023, 15(4), 470; https://doi.org/10.3390/d15040470

by Michelle Williams^*

, Marta Hernandez-Jover

and Shokoofeh Shamsi

Reviewer 1: Anonymous

Reviewer 2: Anonymous

Reviewer 3: Anonymous

Diversity 2023, 15(4), 470; https://doi.org/10.3390/d15040470

Submission received: 20 February 2023 / Revised: 15 March 2023 / Accepted: 18 March 2023 / Published: 23 March 2023

(This article belongs to the Section Biodiversity Conservation)

Round 1

Reviewer 1 Report

Imported fish parasites and a review of their pathophysiology – Diversity

The premise behind this manuscript was to further our understanding of the risk posed by parasites present in imported edible fish to Australia. There were two aims, first to identify some ‘non-zoonotic’ parasites from a previous study of imported freshwater fish from Williams et al. that may pose a risk to Australian freshwater fish. Second, to explore the pathophysiology of parasites and the potential of each to develop a successful life cycle in Australia through a review of published literature. I really enjoyed reading this article and it was nice to see a little acknowledged pathway of parasite invasion receiving attention! The information was interesting, the article was overall easy to read, and will be of great interest to Diversity readers. However, my recommendation is to accept after relatively small major changes have been made. Many of my suggested changes are relatively minor and only require rewording. However, I think the issues I raise are important and require fixing or consideration before publication. I also have quite a few minor changes that will need to be made to help make the wording correct or to provide clarification in some instances. I encourage authors to take my comments on board where they can and I look forward to seeing this publication online as the premise is very interesting and will make for a good contribution to parasitology and assessing the risk of introduced parasites to Australian fish.

Major issues

As per the last paragraph of the introduction, the premise was to further our understand(ing) of the risk posed by parasites in imported edible fish to Australia. I felt that the two aims were quite disjoined in their current form. In fact, as is, this manuscript could be two manuscripts on their own. The first aim does not involve any pathophysiology (something seemingly important as the title includes), nor does it relate to which hosts may be most at risk to invasion, rather it presents a morphological identification of parasites found in unknown channid fish imported into Australia. Parasites that were found in results are missing from tables and in text throughout. The second aim does not actually make any connections to how these parasites may impact Australian fish, or which species might be at the most risk. Overall, I felt there was little depth connecting the parasites found in the first aim and what this means for the risk to Australian fish as per the literature review of the second aim. I suggest authors either 1) remove all literature review data on the species that are not explicitly morphologically identified here (the zoonotic ones found in Williams et al. previously) or relate the actual risk to Australian fish in each section of 3.3.X For example, are species of the genera known to host switch? Is this an event that could occur in Australian fish species? The pathophysiology is interesting, but the only connections that authors make to the risk in Aus fish is in the discussion. In this case, I would suggest authors move this information from discussion to the results for each parasite species and it’s risk potential.

Another major issue I have with this study was that the Channidae species investigated are not specified anywhere in text. In my opinion this is a significant missing part of the manuscript. The host species investigated may dictate which Australian fish species might be most at risk. Is this missing by accident? If so, please include. If all the ‘risky’ parasites come from one species of channid and the other channid fish do not host any risky parasites, then this means that only one species is risky, not at the Family level. I think this is super important to know, and if that data were obtainable somehow then this manuscript is the best place to present this data.

My last major issue with this manuscript concerns the parasite species recovered (as mentioned above). They are lumped to three Pallisentis, Senga and Genarchopsis, as presented in Tables and listed throughout. Reading the results carefully, I can see that authors have in fact presented on multiple species of Genarchopsis Pallisentis were recovered. These extra species need to be included in tables and in text. This will require rewording much of the MS to account for all species found, not just listing the three genera recovered. Furthermore, the use of spp. or sp. needs to be refined throughout too. If authors are not confident to assign Genarchopsis to species level they should still call them sp. 1, sp. 2 etc. This will make it clear how many species are involved. Each species could also be their own section (and the same with Pallisentis spp.), e.g.

3.2.1.1 Genarchopsis sp. 1

3.2.1.2 Genarchopsis paithanensis

3.2.1.3 Genarchopsis sp. 2 (or G. folliculata) if authors are confident that this is that species.

Minor issues

Authors should specify which type of parasites they are working on. Pallisentis, Senga sp. and Genarchopsis sp. are from different phyla so I think this is important to specify, either the first time you introduce each parasite (e.g. Pallisentis sp. (Acanthocephala: Quadriguyridae), Senga sp. (Cestoda: Bothriocephalidae) etc.) or in the introduction (e.g. here, we investigate parasitic helminths…).

Materials and methods

Line 97 – Edible Channidae fish (n=103) – 103 species of fish or individuals?

Literature search

You state how you looked for papers but what did you DO with this? You could add a sentence here at the end of the paragraph stating something like: “For each paper, we compiled data on hosts infected, site of infection, geographic locality…. To provide an overview of the risk to XXX”.

Results

In my opinion, the results should begin with an overview of what was found. At this point in the manuscript, we have not been introduced to the number of fish species or parasites recovered. This information would be good to state here before you get into the morphological data for each species.

3.2.1.

Section 3.2.1. is confusing. It is hard to follow how many species of each Genarchopsis were recovered. This can be fixed by adding in a sentence: Overall, three? Species of Genarchopsis were recovered, including iGenarchopsis sp., G. paiothanensis, and G. folliculata. Then the rows in Table 2 should be explored further with each species of Genarchopsis as opposed to lumping them to one species. Surely there will be differences in prev, MI and MA which will influence in turn their ability to infect Australian fish species so I think this is important to change.

Also in this section Table 2 specifies that you recovered 36 specimens of Genarhopsis sp. but in fact you found 40 specimens of Genarchopsis spp based on the information presented in 3.2.1

Discussion

I really enjoyed the first paragraph of the discussion about at the time of the study fish were permitted to Australia chilled meaning the risk at least in 2020 was real. Have the regulations changed since? This is not clear.

I liked the discussion paragraph about freshwater snails!

Minor remarks

- Line 120 – change ‘parasite sp.,’ to ‘parasite species’

- Figure 2 – Species names are not itailisied. AND Figure 2C is not mentioned in the Figure caption explicitly and can be removed. It does not provide any new data.

- Figure 3 – caption needs more detail and would not stand on its own.

- Line 69 - 75 – authors need references for these statements.

- 2.3 each parasite species – otherwise it seems like this could be interpreted as all spp.

- References in Table 3 are inconsistent in format. Please fix this.

- Table 1 could be listed in text as opposed to a table.

- Table 2 – Total no. of parasites found should not have a decimal as this is only ever a whole number.

- I would remove Figure 3 and just state in section 3.3 how many papers were found for each species.

Author Response

#Reviewer 1

All authors are extremely appreciative of the time taken to provide such a comprehensive review of this MS. Authors are encouraged by the positive feedback and appreciation #Reviewer 1 has shown for the concepts presented in this MS. All of #Reviewer 1 suggestions have been actioned, track changed and highlighted in grey for consideration.

Major issues

Thank you. The aims at the end of the introduction have been amended. There are now three aims which authors believe sets the scene more effctively. The authors believe that pathophysiology of infection has been linked with the addition of several new paragraphs in the discussion which have been track changed and highlighted for #Reviewer 1 consideration.

Another major issue I have with this study was that the Channidae species investigated are not specified anywhere in text. In my opinion, this is a significant missing part of the manuscript. The host species investigated may dictate which Australian fish species might be most at risk. Is this missing by accident? If so, please include. If all the ‘risky’ parasites come from one species of channid and the other channid fish do not host any risky parasites, then this means that only one species is risky, not at the Family level. I think this is super important to know, and if that data were obtainable somehow then this manuscript is the best place to present this data.

Authors appreciate this comment and agree that it would be much better to specify the species of Channidae. It has been very difficult to present data in the many MS associated with this Thesis without actually naming the Country where the produce originated. Identifying the species would identify the exporting country. It has always been the authors intent not to disadvantage and exporting country. The present MS is missing a paragraph (similar paragraphs have been used in other published MS associated with this Thesis) to explain why exact species have not been detailed. A paragraph has now been inserted in the revised MS and highlighted in grey for #Reviewer 1 consideration.

Thank you. Channidae species (now described as Channa species) have been discussed in the introduction and highlighted in grey for #Reviewer 1 consideration. Channa species narrows down the country where these fish may be found without actually identifying the country where these fish originated. Channa species are all voracious carnivorous predators and can be become highly infected with intestinal parasites as a result. There has been a paragraph added in the introduction which discusses Channa species distribution, preferred habitat and carnivorous feeding habits.

3.2.1.1 Genarchopsis sp. 1

3.2.1.2 Genarchopsis paithanensis

3.2.1.3 Genarchopsis sp. 2 (or G. folliculata) if authors are confident that this is that species.

Thank you for the comment. Suggestions have been included in the revised MS and the Tables and captions have been revised accordingly

Minor issues

Thank you. A section has been added towards the end of the introduction to address #Reviewer 1 comment

Materials and methods

Line 97 – Edible Channidae fish (n=103) – 103 species of fish or individuals?

Thank you. Clarification has been provided

Literature search

Thank you. Reviewer suggestion has been incorporated into this section

Results

This information has now been included according to Reviewer suggestion

3.2.1.

Also in this section Table 2 specifies that you recovered 36 specimens of Genarhopsis sp. but in fact you found 40 specimens of Genarchopsis spp based on the information presented in 3.2.1

Authors apologise for the confusion in regard to Genarchopsis sp. There were 36 Genarchopsis sp. identified. Of these 36, three were Genarchopsis paithanensis and one was Genarchopsis folliculata. The sections of the MS which pertain to both Genarchopsis and Pallisentis species has been amended as has Table 2 (now Table 1) to make this clearer.

Discussion

Thank you. Yes, they are still permitted entry although at this point advice from BICON and the commodity codes supplied by the ABS seem in conflict. The big issue is that there are certain conditions which must be met for finfish from Country 22. Consumer ready fish as the Channa fish examined in this study were, should be eviscerated, head and gills removed and be clean. The reason so many parasites were recovered was because the processing standards were really poor and there were full/partial intestines, gills/head and brains still retained and lots of mud/vegetation/debris/snails/rusted fish hooks…… So poor processing is high risk for parasites but also bacteria. There is an MS which hopefully will be published soon if you are interested, “Bacteria of zoonotic interest identified in fish imported into Australia” which shows how poor processing increases the risk of zoonotic bacteria.

I liked the discussion paragraph about freshwater snails!

The authors thank the Reviewer for the comment.

Minor remarks

- Line 120 – change ‘parasite sp.,’ to ‘parasite species’

Changed

- Figure 2 – Species names are not itailisied. AND Figure 2C is not mentioned in the Figure caption explicitly and can be removed. It does not provide any new data.

The parasites in the figure 2 caption are italicised in the submitted MS and the copy sent back for revision. I am unsure what has occurred or why Reviewer copy was not italicised. Authors are keen to make all necessary changes so please advise further.

- Figure 3 – caption needs more detail and would not stand on its own.

Thank you. More detail has been provided

- Line 69 - 75 – authors need references for these statements.

Thank you. References provided

- 2.3 each parasite species – otherwise it seems like this could be interpreted as all spp.

This has been revised

- References in Table 3 are inconsistent in format. Please fix this.

Authors apologise for the inconsistent format which has now been rectified.

- Table 1 could be listed in text as opposed to a table.

Table 1 has been removed and necessary adjustment made to remaining Tables and in text references to Tables

- Table 2 – Total no. of parasites found should not have a decimal as this is only ever a whole number.

Amended

- I would remove Figure 3 and just state in section 3.3 how many papers were found for each species.

Thank you. Authors have been asked in the past, following review, for a Figure which shows the flow of the Literature search which is why this Figure has been included.

Reviewer 2 Report

Dear Authors,

the manuscript is interesting and full-bodied. Here are some advises:

The scientific names of the parasites should all be in italics; check please throughout the text.

M&M

Were the parasites stained for species identification?

Line 103:

In my opinion, the Table1 is not necessary; the Authors could directly insert the references into the text (chapter 2.1); for example “…The morphometric characteristics of the parasites were studied under a light microscope by a calibrated eyepiece micrometre (BX-43….) and compared with descriptions in the literature (list of the references in brackets)”.

Line 144

Replace interior with lumen

Results and discussion

Although the pathophysiological aspects of zoonotic species are very interesting, for the linearity and harmony of this work, results and discussion should be concentrated on the species identified in this paper.

Table2:

The Authors could include the site of infection and the species identified in the table (i.e. G. paithanensis, ect)

Figure 2

If it is possible for the Authors, choose clearer images or with details that highlight the characteristics useful for the identification of the species. Check please the scientific names of the parasites in the capture.

Author Response

#Reviewer 2

Dear Authors,

the manuscript is interesting and full-bodied. Here are some advises:

All authors thank #Reviewer for the encouraging feedback and for providing a review of this MS. All changes have been track changed and highlighted in yellow for Reviewer consideration.

The scientific names of the parasites should all be in italics; check please throughout the text.

Thank you. The scientific names were all in italics when the MS was submitted however when the MS was transferred to the MDPI template some parasite names were converted to plain text. This has been rectified in the revised MS and hopefully will remain in italicized format

M&M

Were the parasites stained for species identification?

Yes, in the second last line of section of 2.1 it is stated that non-zoonotic parasites identified in this study were mounted with lactophenol. The preparation for Isoparorchis sp. and Euclinostomum sp. identified in “Williams, M., Hernandez-Jover, M., & Shamsi, S. (2022). Parasites of zoonotic interest in selected edible freshwater fish imported to Australia. Food and Waterborne Parasitology, 26, e00138” is described in detail in section 2.2 of Williams et al. (2022). Williams et al. (2022) is cited in the text of the present MS as the preparation method used for zoonotic parasites.

Line 103:

Thank you. Table 1 has been removed from the MS. Section 2.2. has been amended according to Reviewer suggestions and the publications used to identify each respective parasite included in Section 3.2 onwards which discusses the morphometric data for each parasite

Line 144

Replace interior with lumen

Changed

Results and discussion

Thank you. The same comment was made by #Reviewer 1. Please note the changes to the aims at the end of the Introduction and the sections highlighted in grey preceding the amended aims. Also, please see the sections added to the discussion also highlighted in grey.

Table2:

The Authors could include the site of infection and the species identified in the table (i.e. G. paithanensis, ect)

Thank you. The site of infection is discussed in section 3.1 of the MS and has now been included in Table 1, previously Table 2

Figure 2

Thank you. Unfortunately, due to relocation of the corresponding author, there is no possibility to recapture the images. The scientific names associated with image have been checked.

Reviewer 3 Report

Congratulations to the authors on a well thought out and written article. The manuscript presents author’s study of parasites in imported edible fish in Australia combine with a well-conducted review of the literature on the pathophysiology of fish caused by these parasites. The presented material corresponds to the research purpose. It should be noted the original drawings of the authors, photos of parasites and their description, which improve the perception of the article.

I have only minor remarks regarding mainly parasitological terminology, which will undoubtedly improve the article:

Line 9 – More suitable “digenetic parasites” or “digenetic trematodes”

Lines 15–17 – It is necessary to detail the stages of parasites: adults (marites or mature trematodes)… and metacercariae…

Line 26 – Please remove numbers from keywords.

Line 35 – More suitable “invasive parasites” or “invasive parasite species”

Lines 41-43, 80, 81 – According International Code of Zoological Nomenclature (ICZN), at the first mention of species, its full Latin name with the author and year of description should be given; in relation all species of parasites and their hosts (for example, Bothriocephalus acheilognathi Yamaguti, 1934, Gyrodactylus bullatarudis Turnbull, 1956, etc.).

It is also necessary for all parasites to give the authors and the year of description in Tables 1-3 and Supplementary Table. And it is preferable to insert “Trematodes”, “Cestodes” and the names of trematode and cestode families into Supplementary Table.

Table 3 – Please in the second column, open the brackets and give the authors and the year of the description of fish. And you should merge the cells in the first column where the names of the parasites are repeated.

Lines 64,65,403 – Please rephrase like “…parasites may successfully complete their life cycle by involving native aquatic or other species”.

88,89 – I propose to slightly change the sentence like “…and the potential of each parasite in successful implementation of their life cycles in Australia through a review of published literature.”

Table 1 – Please change the name of the first column – “Helminth genus or species” or simply: “Parasite”

In Section 2.2. there is no data on which works, keys the parasites were identified. You can take this information here from the Results. And make references according to the rules of MDPI (line 219).

Line 134 – Please expand subsection name: 3.1. Prevalence of Helminths in Fish

Line 148 - The subsection name is more appropriate for Materials and Methods. Here it is better to call “Parasites from consumer ready Channidae” or Helminths?

3.2.1., 3.2.2., 3.2.3., 3.3.1., 3.3.2., 3.3.3.,3.3.4. – italics.

Lines180-185 - italics for Latin names of parasites.

Lines 284,310 – digenetic.

Lines 416,421,423 – It is better to use the Latin names of fish. Please don't use the common name without Latin name or only after the previous citation in the text.

Lines 289,564,565,566 – Please open brackets and give authors and year of description.

The manuscript deserves to be published in Diversity, but minor corrections are needed.

Comments for author File: Comments.docx

Author Response

#Reviewer 3

Thank you. Such encouraging comments are greatly appreciated by all authors, particular #Reviewer 3 appreciation of the MS concept. Changes requested by #Reviewer 3 have been track changed and highlighted in green for consideration. Thank you. All authors are pleased that the original figures were well received.

I have only minor remarks regarding mainly parasitological terminology, which will undoubtedly improve the article:

Line 9 – More suitable “digenetic parasites” or “digenetic trematodes”

Now changed to digenetic trematodes

Lines 15–17 – It is necessary to detail the stages of parasites: adults (marites or mature trematodes)… and metacercariae…

Thank you. This has been done

Line 26 – Please remove numbers from keywords.

Authors will raise this with the journal as it appears to be a requirement for their publications

Line 35 – More suitable “invasive parasites” or “invasive parasite species”

Changed

Thank you, done

Thank you. Table 1 has been removed according to comment by another Reviewer. The other tables have all been amended

Amended

Lines 64,65,403 – Please rephrase like “…parasites may successfully complete their life cycle by involving native aquatic or other species”.

Thank you. Changed

Thank you. The aims have been revised following comments made by #Reviewer 1. Please see revised aims highlighted in grey

Table 1 – Please change the name of the first column – “Helminth genus or species” or simply: “Parasite”.

Table 1 has been removed

The publications used to identify parasites were removed from Table 1 and are now included in results section 3.2 onwards

Line 134 – Please expand subsection name: 3.1. Prevalence of Helminths in Fish

Changed

Line 148 - The subsection name is more appropriate for Materials and Methods. Here it is better to call “Parasites from consumer ready Channidae” or Helminths?

Thank you. Changed

3.2.1., 3.2.2., 3.2.3., 3.3.1., 3.3.2., 3.3.3.,3.3.4. – italics.

Thank you. The MS was reformatted by MDPI editorial office so authors are unsure about changing the formatting. Authors will check with MDPI.

Lines180-185 - italics for Latin names of parasites.

Thank you. Species names in the original submitted MS were all italicized. When the MS was transferred by MDPI editorial office to the correct template, some species names did not format correctly. The revised MS has been checked and species names have been re italicized.

Lines 284,310 – digenetic.

Changed

Lines 416,421,423 – It is better to use the Latin names of fish. Please don't use the common name without Latin name or only after the previous citation in the text.

Changed with scientific names following common names

Lines 289,564,565,566 – Please open brackets and give authors and year of description.

Thank you. All amended

The manuscript deserves to be published in Diversity, but minor corrections are needed.

Round 2

Reviewer 1 Report

I thank the authors for their effort in making changes to their manuscript based on my previous comments. I believe this manuscript is clear, well written and now in acceptable form for publication in Diversity. I really appreciate the authors making an effort to explain why they can not identify the fish species explicitly in the manuscript and for splitting each species for clarity in their tables.

Best wishes and congratulations on a nice paper!

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