Peer Review History
| Original SubmissionJune 16, 2020 |
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PONE-D-20-18486 The role of migration barriers for dispersion of Proliferative Kidney Disease – balance between disease emergence and habitat connectivity PLOS ONE Dear Dr. Schmidt-Posthaus, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. ============================== ACADEMIC EDITOR: Dear Authors of the manuscript Number PONE-D-20-18486 entitled "The role of migration barriers for dispersion of Proliferative Kidney Disease – balance between disease emergence and habitat connectivity". I read myself this interesting manuscript and I obtained comments from three eminent experts in Malacosporean parasite and PKD disease. Despite the divergent opinions from these three reviewers, I think the manuscript has still merit for being published in Plos ONE. As expressed from the three reviewers, there are some main concerns that involve the possibility to make inference about the results obtained. This is especially true if looking at the fact that the study was 1) limited in the sample size of fish host (brown trout) analysed and 2) lacking of relevant information concerning the environmental features that characterize the study area and 3) most importantly concerning the occurrence of freshwater bryozoan hosts (mostly Fredericella sultana) in both the areas investigated. The latter point is essential to understand the results here obtained that suggest how connectivity in the fish host is not affecting the introduction of the parasite in the area that was free from the parasite before the reopening of migratory barriers in 2014. In fact, the lack of bryozoan hosts in the area reopened to fish connectivity might be the reason for such a pattern considering that the availability for a bryozoan host is a determining factor in the ability of the parasite Tetracapsuloides bryosalmonae to complete the life cycle and being carried around by the intermediate (fish) host. The manuscript is also limited to a very narrow area and the authors should have better described the features of the area here studied and express this limit in the discussion. As a minor consideration, I would recommend a better figure (in terms of quality) of the studied area because it is essential for the main aim of this manuscript. I`d like to open up to the possibility to publish this manuscript if the authors can cover these gaps, especially providing proof that both areas here investigated show viable freshwater bryozoan populations that can sustain the interpretation of their results. Therefore, I`m going to suggest "major revision". ============================== Please submit your revised manuscript by 30 November 2020. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. Please include the following items when submitting your revised manuscript:
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Competing interests can arise in relationship to an organization or another person. Please follow this link to our website for more details on competing interests: http://journals.plos.org/plosone/s/competing-interests [Note: HTML markup is below. Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #1: No Reviewer #2: Partly Reviewer #3: Partly ********** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: No Reviewer #2: No Reviewer #3: Yes ********** 3. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: No Reviewer #2: No Reviewer #3: Yes ********** 4. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: No Reviewer #2: No Reviewer #3: Yes ********** 5. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: I have several major conceptual criticisms of this work, which I will expand upon below. I understand that word limits often restrict methods details, but the methods, as they are described in the submission, are not detailed enough to be repeated. In addition, the manuscript does not seem like it is ready for submission, as there are several formatting anomalies. The methods of the study do not address the objective as it is outlined in the introduction: “The aim of the study was to investigate the role of a migration barrier in limitation of pathogen transport by migrating fish…”. These data are not generalizable to other diseases and the study design is incapable of addressing this objective. As is pointed out in the manuscript, PKD generally manifests in naïve fish, which are generally YOY. As is also pointed out in the manuscript, YOY brown trout generally do not migrate into tributary streams from larger bodies of water. So the study’s conclusion that “the benefit of restoration of the river corridor seems to exceed the risk of transmission of infectious agents” is based on an extremely biased data set because the fish that are migrating are the same ones that are least likely to succumb to, be susceptible to, or to release parasite spores due to PKD. Another major flaw is that the study completely ignores the primary bryozoan hosts of T. bryosalmonae. There was no mention of any effort to confirm the presence of bryozoans in the Ehrenbach, which would be necessary for the complete life cycle of T. bryosalmonae, because spores released from infected fish cannot, as far as we know, ever infect other fish. If bryozoans are not present in the Ehrenbach, might the results have been dramatically different if bryozoans were there? On a similar note, the absence of parasite in fish is not necessarily an accurate indicator for the absence of the parasite in bryozoans in the same location. This disease is extremely complex and there are several variables which might decouple infection in the two hosts. If I am reading the methods correctly, only fish from the Wutach were pit-tagged, which means that there is no movement data for fish that were above the barrier before its removal. These fish may have very different patterns of movement across the two water bodies. This missing information represents a large gap for any epidemiological model of this system. Reviewer #2: This paper aims to assess whether removal of migration barriers to fish in rivers results in upstream movement of fish and whether their associated parasites also disperse with the fish. This aim is communicated clearly. The research focuses on a relatively rare opportunity to track parasite dispersal in a real river system, centering on a removal of a migration barrier in one river. The paper presents novel results from a field observational experiment. Prevalence of infection was monitored upstream and downstream of a migration barrier one year before the barrier removal, followed by monitoring in five years after the removal of the barrier. The premise of the study is of applied importance for many river restoration efforts. The research rationale and methodology is in principle presented well, however, not enough details of the study system are given to understand how the parasite might disperse to the upstream reaches of the river, and at what time scales that might be expected to occur. Regardless, the study design and methodology appear sound. The main concern is that the results are based on a single site. However, it is clear that such investigations are exceedingly difficult to replicate in wild. Regardless it is very important to highlight this issue in the discussion and perhaps recommend ways to improve monitoring in future restoration projects, and highlight the focus on parasite spread. I unfortunately was not able to find Table 3 and the line numbering disappeared around the discussion start, making in difficult to highlight specific issues. I hope the comments will nevertheless be possible to be tracked by the authors. The writing is clear, and the authors have done a very competent job of the scientific discussion and arguments, BUT editing of English language is needed throughout to improve sentence structure in particular. Otherwise the article is clearly written and logically organised, it is relatively easy to follow. Appropriate controls and confirmatory techniques are taken in most parts. I was not able to correct all the grammar issues as that would have required a substantial amount of work, but have provided a .doc document where I have highlighted particularly noticeable problems in yellow highlight. If the authors address the suggestions made below, in my opinion this manuscript appears suitable for publication in PLoSOne. Introduction - Line 45: why “developing”? Suggest removing “Nowadays” - Line 47: fragment sentence starting on this line “Thus,…” – please revise. - Line 49-52: punctuation missing, sentence is really long, and hard to follow due to odd grammar. - Line 55: “…several current projects” suggests some specific projects are implied (also indicated by the pers. com reference). Suggest revising this sentence to be more general and providing a reference to primary literature. - Line 59: clearly transmission is important for parasites, but here its combined with the dispersal of the parasite (“transport”). Transmission and dispersal are very different concepts and the sentence should be re-written to distinguish this better. - Line 61-62: replace “was classified as” with “is”. Classified sounds too formal in this context. - Line 69: Please review most recent terminology – actinospores and myxospores refer to mxosporeans, suggest using malacospores and fish malacospores instead. - Does fish to fish transmission occur? Please provide information here e.g. Line 71. - Line 79: please articulate the sentence above as a question or change wording here. It is not clear what the specific, testable idea (hypothesis) is here. What is being tested? Whether infected fish can move upstream? Whether the parasite is transmitting in the upstream section? Whether the parasite spreads to the new upstream area? It should be pointed out here that migration of adult fish was monitored and disease status in the upstream and downstream YOY populations was also monitored. Please revise this section to be explicit about what the experiment really tests. - Line 81: It is difficult to understand the extent of this barrier without further information. Please describe what this barrier is like, does it prevent up and downstream movement of fish? What is it exactly? Why is it being removed? What was involved in its removal? - Finally, it is confusing that the disease manifests in the YOY but these are not migrating. Please provide more information regarding what is known about migration habits of different age classes and what the expectations are relative to the spread and disease in fish populations. Are the migrating adult fish competent hosts and transmit the parasite to other hosts? Please provide references. - In general the introduction needs a thorough checking of English to improve sentence structure. There are many incomplete sentences and incorrect wordings, which make it tough to follow. Methods - Line 99: “own investigation”: whose? Please cite pers comm. NAME if no other reference is available. - Line 98: It would be important to know if the fish sampled were YOY or adult fish. - Line 101: When in 2014? - Line 112: not clear what the “respectively, “ refers to. Please revise. - Line 122: please use consistent terminology for qPCR or RT PCR or RT qPCR…. - Line 144-147: Are these the same as in the referenced paper? Consider deleting? - Line 159: was the infection status of these fish checked? Or the infection status of a peer group captured at the same time? Previous investigations showed that prevalence was high in the YOY fish but was that the case for the older fish too? Is it possible the infected fish more less and do not take part in migration? - The statistics section is not sufficient. This should describe the analyses conducted to a detail where they could be repeated following the description provided here. What tests were done on what data? Please ensure all analyses presented in results section are covered here. Results - Table 1: What does the +/- refer to? Please define. - Figure 1 should be redrawn – the satellite imaging shot does not show the river clearly and its hard to see the confluence. Also, the red font on busy background is difficult to see. The zoomed in map should be presented in a larger context in an inset figure – e,g, its difficult to understand where the border is and where the site is located. - Figure 2 is not particularly informative. Could be easily deleted or replaced. - Where is Table 3? - Line numbers disappers and it difficult to provide direct comments from here forwards… - Can the possible invasion be really linked to the migrating trout? Using the methods employed here, it does not seem be possible to make a direct link, although such effects may be implied. Please reword to take account of this ambiguity. - Reporting of Cq values is relatively meaningless. Would it be possible to provide copy numbers per unit of kidney, this would make comparisons more relevant. Taking means of Cq values across samples is also confusing and should be avoided in the table. - Is the section starting with “From 2016 to..” referring to Wutach? Please add. - The results section could be made clearer by combining the fish parameters with the PKD monitoring section as these presumably pertain to the same fish. The migration fish are a different batch of animals. - Table 2: please make separate column for prevalence. - “On 15th…” migrating from Wutach? - Did the fish collected and tagged from Ehrenbach move upstream too? The monitoring station was only 20m upstream – is this considered a migration? Why were fish tagged in the Ehrenbach – is the data reported? Suggest reporting results separately for the fish tagged in Wutach and Ehrenbach. Were the same fish detected in multiple years? - What is the significance of the non-consecutive days? Discussion - The discussion needs a re-write, to improve flow and English. Comparisons to other research in the field is limited to the considerations of PKD, it would be interesting to see further discussion relating this research to other disease systems in aquatic context. - A section on future research directions in this field would be useful, for example, investigations across the full life-cycle. - It seems one limitation of this study is that the infection status of the tagged fish was not known, and it is not clear if PKD impacted adult fish migrate normally. This should be discussed further. - The start of discussion should be improved with more details regarding the e.g. wh is restoration “more significant”. Perhaps this is not the wording the authors mean? Referencing here is completely lacking. E.g. “unambiguous benefits” should be backed up by references. - Include references that discuss or test the spreading of pathogens in association with restoration of connecitivity - Discuss further the implications of complex life-cycle of parasite for the likelihood of spreading with migration. - Is the temperature difference significant? In relation to the triggers of PKD and the parasite development and the development of the invertebrate hosts? - Reference the lack of spore excretion during winter. - How does the last sentence of the discussion relate to the results generatated in this experiment? Please tie it in better. - References are not provided in a consistent format. Reviewer #3: General Comments This is a straightforward study with only few, albeit incomplete datasets reported. It describes the migratory movements of salmonids native to Wutach river in Switzerland in the context of PKD infectivity. The manuscript is generally well written, although spelling / grammar could be improved in a few places, as descibed under “Specific Comments” below. Although datasets are not complete due to equipment failure, the study is of a publishable quality, subject to addressing specific points below. Specific Comments • Lines 37-39: This sentence needs to be rephrased as it, currently, isn’t very clear. • Liines 49-54: This is a very long sentence. Please rephrase. • Lines 69-76: It is not correct to refer to T. bryosalmonae stages as myxopsores and actinospores, it’s a malacosporean not a myxosporean. • Lines 103-104: Could the authors provide a clear justification for the chosen sampling period (24th Aug – 15th Sept) • Lines 109-111: The authors need to justify why only a single electrofishing site was chosen on the Ehrenbach tributary and two on the Wurach river. This is important since its migration from the Wutach to the Ehrenbach that is under investigation. • Could the authors confirm the Ehrenbach tributary-Wutach river connectivity with a better-quality image. Current map is not clear enough. • Line 112: Define YOY • Line 117: The authors use “condition factor” here but “condition index” elsewhere • Line 129: What are the criteria that govern each histological grading score. Please define or refer to a previously published study • Line 131-132: Also define each poiint in the scoring system 0-6 in the context of parasite numbers. Is it numbers of parasites counted in X number of field of views per tissue section with Y number of sections analysed per fish kidney sample? Please properly define, it is currently not very clear. • Line 149: What is Exo IPC. Please define. • Lines 153-157: Can the authors provide more detail justifying the why those sites were chosen for the study. • Line 162: Figure 2 doesn’t provide real added value to the paper. Simply stating the size of tags in the Methods will suffice. • Line 169-174: Have the authors implemented the tag reading technology previously? If os, please provide a reference. • Lines 179-181: What do the authors means in saying the logger was lifted. Why? • Line 191: Line numbering ends here! • “(table 3). One animal showed chronic active changes with interstitial fibrosis and concurrent acute signs as described above. Severity of changes and parasite abundance are summarized in table 3”. No Table 3 provided. Presumably, this is a typo and should be Table 2. • Table 2 and legend need to be clearer and the authors need to describe, in the discussion, why only fish sampled in 2013 are PCR negative yet all other signs point to parasite infection / exposure. Parasite tissue distribution is unlikely to homogenous throughout the kidney and so could account for apparent differences between fixed tissue datasets versus qPCR results? Need to clarify that the “parasite abundance” and “pathology severity” columns originate from histological and parasite abundance datasets (from scores 0-6). Define “nd”. • “162 brown trout and two rainbow trout were PIT tagged. Length of tagged fish ranged from 90 to 471 mm (mean 270.9, median 282), weight from 9 to 1072 (mean 296.6, median 269.5) g. Condition index ranged from 0. 85 to 1.78 (mean 1.19)”. What were the weights / lengths of fish per sampling site? • “During the investigation period, 19 tagged brown trout and one rainbow trout were migrating from the Wutach into the Ehrenbach (12%) (Fig. 3)” How does this level compare to similar studies? As it wasn’t possible in this study to get a real idea of the number of tagged fish remaining in the Wutach via tag detection versus fish losses / mortalities, it is important in the discusion to refer to previous datasets. • So, only mature fish migrate with YOY fish remaining in the Wutach. Yet, the majority of mature fish also remain in the Wutach. Are there other known spawning sites within a few Kms of the study sites? Lack of PKD infectivity in mature migrating fish supports a link between fitness and migration with infected fish less inclined to migrate. This is needs to be mentioned in the discussion. • 2018 NOT 2918 • “Fig. 3. Temperature profiles from Ehrenbach and Wutach, 2013, 2017 and 2018. Red line marks 15°C, the temperature where PKD revealed to be clinically relevant” This is unclear, please clarify. • “bryozoan, the final host”: Please correct to “definitive host” • “Even if the minimum necessary number of days with high water temperature for the clinical outbreak of disease is not known and…………” Please re-structure this very long sentence. • “……..trout does not play a role”: In what? • “Considering the technical malfunction of the PIT antenna over cumulated 91 days, between October 2017 and March 2018………….” So, data was only used from one complete spawning season due to technical failure? • “This proves the importance of continuity…………”Change to “This supports the importance……” • “We thank the fishermen „Oberes Wutachtal Stühlingen e.V.“ for……” Please correct. • Figure 3 and 4 axes labels need to be improved re. quality. ********** 6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). 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The role of migration barriers for dispersion of Proliferative Kidney Disease – balance between disease emergence and habitat connectivity PONE-D-20-18486R1 Dear Dr. Schmidt-Posthaus , We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements. Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication. An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org. If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org. Kind regards, Paolo Ruggeri, PhD Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: |
| Formally Accepted |
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PONE-D-20-18486R1 The role of migration barriers for dispersion of Proliferative Kidney Disease – balance between disease emergence and habitat connectivity Dear Dr. Schmidt-Posthaus: I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department. If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org. If we can help with anything else, please email us at plosone@plos.org. Thank you for submitting your work to PLOS ONE and supporting open access. Kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. Paolo Ruggeri Academic Editor PLOS ONE |
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