PONE-D-21-07782

Infective prey leads to a partial role reversal in a predator-prey interaction

PLOS ONE

Dear Dr. Kaitala,

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.

My mind has been switching between “Major Revision” and “Rejection.” In the next set of reviews, I plan to invite someone who is familiar with infectious disease modeling. I encourage you to investigate infectious disease models (both SIR models and vector-born disease models). The presented model looks like that of a vector-born disease with a part of prey is infected with a pathogen. Please note that it is plausible that I might decide to reject the submission in the next round if the reviewer finds that the model already exist in the infectious disease literature. I provide more detailed comments separately.

Please submit your revised manuscript by Jun 04 2021 11:59PM. 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.

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We look forward to receiving your revised manuscript.

Kind regards,

Masami Fujiwara, PhD

Academic Editor

PLOS ONE

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Additional Editor Comments:

As reviewer 1 points out, it is not clear how representative the model is. Furthermore, you cannot stabilize a system that is already "stable". Looking at the figures, I think the system is already stable under a wide range of parameter space (including alpha=0).

You can have r_c=0 or positive as well as r_s=0 or positive, representing whether prey (or predator) is specialist or generalist. Analogous to mutualism models, we could also have k_c<0 or >0 as well as k_s<0 or >0, depending on whether they are obligate or facultative. I think investigating the dynamics of the model under each combinations of these conditions is potentially interesting (and some of them will produce “instability” without infection). -- just a suggestion for improvements.

As reviewer 2 points out, the model is also like SIR models. A large body of literature on SIR models exist. The model results should also be discussed in terms of the existing knowledge of the SIR models. I personally think the model is more like a vector-born disease model rather than an SIR model. Right now, the model is interpreted as having prey that is an energy source as well as pathogenic. However, it is more natural to interpret that the prey is carrying a pathogen (e.g. virus, bacteria, trematode, nematode, myxozoan, etc.). It may be easier to justify the model as a vector-born disease. Similarly to SIR models, there are a large body of literature on vector-born diseases. I would not be surprised if someone else already developed the model like the one presented (e.g. malaria infection model).

Reviewer 2 also raised some concerns with regard to the units of parameters. Some justifications of the parameter estimations should be presented.

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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: Partly

Reviewer #2: Yes

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: N/A

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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: Yes

Reviewer #2: Yes

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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

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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: Dear authors,

your study considers how role reversal in a predator-prey system may affect the persistence of the prey and the predator species. Although the focus of your study and thus the ecological question is very interesting, I am not entirely convinced that the current formulation of the model may significantly enlarge our understanding of the potential importance of role reversal within natural predator-prey systems (for further details see my complete review attached).

Sincerely yours

Reviewer #2: While the topic of the manuscript on a food web with the possibility of reversesd prey-predator roles is quite interesting, and could as such be relevant to a number of empirical systems, I think it is not yet matured enough to be ready for publication. First of all I think that the explanation of the food web, the role of the bacteria as prey as well as infectious disease should be more clearly explained using established nomenclature. Specifically the model should not only be described as a Lotka-Volterra predator-prey model, but as a combination of a standard Lotka-Volterra predator prey and a SIR model (an established approach to model infectious disease dynamics). There is a lot of confusion on terms throughout the manuscript, see the more detailed comments directly to the article in the attached pdf.

While the explanation on your parameters seems as such to be quite detailed, they are not at all clear. Specifically it is not clear to me what is the scientific basis that support the terms used, based on wet or dry-weight, to derive specific rates like assimilation efficiencies (L134-137). Also the units used are missing a relation to volume or area. The "attack rate" of the cucumber for bacteria to me would be better described as a 'filtration rate' and not an 'attack rate', where cucumbers filter a certain volume of sediment per unit time and therefore feed on bacteria proportional to the density of the bacteria in the sediment.

Why did the authors choose a model with state variables measured in terms of individuals instead of biomass? Since the body size of cucumber versus bacteria are several orders of magnitude apart from each other, I would find it more reasonable and easier to judge on the parameterization, if state variables and parameters would be indicated on a per unit biomass basis.

The result section is quite lengthy, but still not always on the point (see detailed comments in the pdf).

The authors could more clearly relate the analytical findings to the numerical results and specifically use the analytic findings to derive some general insight on the influence of certain parameters on coexistence and dominance patterns of prey and predator. These theoretical insights should then in the discussion be related to their relevance and implications for real systems, the specific study system, as well as other systems.

The discussion is not very well developed. The authors do neither highlight the main results nor put them adequately into context of existing work. The relevance of findings from this model for other model systems is very vague and it is not clear how and why the mentioned empirical systems for example the pike and stickleback system, or agriculture could be related to the investigated model system.

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Reviewer #1: No

Reviewer #2: No

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Attachments

Attachment

Submitted filename: Review.docx

Attachment

Submitted filename: PONE-D-21-07782_reviewer.pdf

PONE-D-21-07782R1

Infective prey leads to a partial role reversal in a predator-prey interaction

PLOS ONE

Dear Dr. Kaitala,

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.

We received additional comments from a new reviewer. The comments agree with my assessment of the previous version (as well as the current version) of the manuscript. I would like to suggest three potential ways to mediate the issue: (1) provide a better connection with the existing literature in infectious disease models in general, (2) compare the model and results with the Nicholson-Bailey model, or (3) make the review comments available to the public. The originality of the research is one of the conditions for publication in the PLOS One, and the readers will need to know how the new knowledge is built on the existing ones. I am recommending Minor Revision because I think action (2) or (3) is straightforward. Action (1) can also be achieved quickly if you invite someone who is familiar with infectious disease models. However, it is probably important to note that Minor Revision is not the same as conditional acceptance (it is a minor in effort but still an important revision for the final decision).

Please submit your revised manuscript by Sep 06 2021 11:59PM. 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:

• A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
• A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
• An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Masami Fujiwara, PhD

Academic Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #3: (No Response)

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2. 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 #3: Yes

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #3: Yes

**********

4. 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 #3: Yes

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5. 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 #3: No

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6. 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 #3: Review for: Infective prey leads to a partial role reversal in a predator-prey interaction

I'm going to keep this review relatively short and in keeping with Plos One guidelines. The science (methods and results) appear sound, however, as a draft, lack of context or awareness of large bodies of important work is disconcerting, and as a consequence the science doesn't add much to our knowledge of ecology. Note that this is my first review of this, I did not participate in the first review.

The authors implement a straightforward Lokta-Voltera style coupled differential equation system to model predator-prey dynamics, though not grounded in any data, and describing this system as a predator-prey system seems a bit contrived. The results are unsurprising: when a "prey" species begins to behave increasingly like a pathogen, then the "predator" (it's hard for me to call a bacteriophage a predator) tends to die and the pathogen does better, while when a "prey" is less and less pathogenic (is more and more tasty), the predator does better.

Although I think the science is basically sound (though not particularly consequential), I have some issues with the way the authors have cast the system. The idea that this is a special case of a predator-prey system is a big stretch, and I feel the system is probably much better characterized as a special case of a host-pathogen system, for which there has been a great deal of previous thought, research, and modelling work to build upon and contextualize the system with. Although I was eventually convinced that could think of V. splendidus as a consequential food source, I had to do a lot of digging in the literature -- the authors did not cite any papers the indicated if the biomass of V. splendidus was significant in the bacterial community -- something they need to set up the model as they have. Instead, I had to convince myself that V. splendidus would form a significant fraction of the bacterial biomass in this or similar systems by reading other papers on the topic. If V. splendidus is never or rarely of significant biomass, the system *definitely* has to be considered host-pathogen problem and not a predator-prey problem. So evidence that V. splendidius is a large fraction of the bacterial biomass in some relevant circumstances needs to be provided in the introduction to set up the problem, otherwise the model simply isn't well enough grounded in any real system to be helpful or informative at all.

I think more problematic is the lack of recognition, citation, or development of the model presented's relationship to two other key bodies work. The first is the enormous body of epidemiological and host-pathogen models, which are of course highly informative of the dynamics modeled here. At least as important an oversight is the classic but uncited Nicholson-Bailey model (Nicholson, A.J. and Bailey, V.A., 1935. The Balance of Animal Populations), who built a Lokta-Voltera predator-parasitoid model very, very similar to the model presented in this paper (and did so 85 years ago), and the large body of work, papers, and model extensions that grew from that classic model. None of that body of work is cited here, and it seems the authors are unaware of it. This is a problem given its similarity in both form and substance. So that context needs to be added to both the intro and discussion.

Currently the discussion, which is normally the place where authors place their findings into the context of the larger body of scientific work, has no references (which is a-typical to say the least) and mostly serves to reiterated the results. That's just not acceptable.

Finally, the authors have made minimal effort in terms of labels, colors, font sizes, line width, legend, etc. with respect to making their figures intuitive and informative.

Altogether this paper just feels sloppy, it doesn't seem to be aware of other important and relevant bodies of work and is consequently reinventing the wheel to some degree with a contorted pitch about predator-prey role reversals. It's really a host-parasite or host-pathogen problem, which have been much better worked. If this were any other journal, I would not recommend publication. Here I can only ask that at the very least the authors work to better cite and ground their work in relevant literature and rework their figures so they are of reasonable quality and readability.

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7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #3: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

Infective prey leads to a partial role reversal in a predator-prey interaction

PONE-D-21-07782R2

Dear Dr. Kaitala,

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.

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Kind regards,

Masami Fujiwara, PhD

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments: