Dear Dr. Mehta,

Thank you very much for submitting your manuscript "Emergent competition shapes the ecological properties of multi-trophic ecosystems" for consideration at PLOS Computational Biology. As with all papers reviewed by the journal, your manuscript was reviewed by members of the editorial board and by several independent reviewers. The reviewers appreciated the attention to an important topic. Based on the reviews, we are likely to accept this manuscript for publication, providing that you modify the manuscript according to the review recommendations.

Please prepare and submit your revised manuscript within 30 days. If you anticipate any delay, please let us know the expected resubmission date by replying to this email.

When you are ready to resubmit, please upload the following:

[1] A letter containing a detailed list of your responses to all review comments, and a description of the changes you have made in the manuscript. Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out

[2] Two versions of the revised manuscript: one with either highlights or tracked changes denoting where the text has been changed; the other a clean version (uploaded as the manuscript file).

Important additional instructions are given below your reviewer comments.

Thank you again for your submission to our journal. We hope that our editorial process has been constructive so far, and we welcome your feedback at any time. Please don't hesitate to contact us if you have any questions or comments.

Sincerely,

Jacopo Grilli

Academic Editor

PLOS Computational Biology

Natalia Komarova

Section Editor

PLOS Computational Biology

***********************

A link appears below if there are any accompanying review attachments. If you believe any reviews to be missing, please contact ploscompbiol@plos.org immediately:

Reviewer's Responses to Questions

Comments to the Authors:

Please note here if the review is uploaded as an attachment.

Reviewer #1: One of the outstanding puzzles regarding natural ecosystems is how the interaction of multiple species, each with its own particular attributes, leads collective states of the ecosystem as a whole. One aspect of this puzzle is how interactions among multiple trophic layers, e.g. primary producers, initial consumers, secondary consumers, etc. shape overall ecosystem states. The authors address this question within the well-established framework of consumer resource models (CRMs). What is new is applying to CRMs the perspective that complex interactions can be treated as random parameters. While this approach may be debatable, there is no question that the results of the current study admirably account for a remarkable number of observations about real ecosystems. Furthermore, the authors apply an analytic approach (the cavity method) that both agrees quantitatively with simulations and provides some important simple insights into overall behavior, e.g. whether a particular system is controlled from the bottom up or from the top down. Overall, I believe this work makes an important contribution to our understanding of multi-trophic ecosystems and will be of interest to a broad audience. Finally, the paper was a pleasure to read. I have only a few points for the authors to address:

1. The general reader would benefit from some simplified examples. For example, the coupling between species at the central trophic level due to a shared resource or a shared predator could be explained using a model with only three species, in each case. Even more important would be a simple example of a situation leading to bottom up control vs. one leading to top down control. While ecologists may already understand these ideas, they are likely to be unfamiliar to many readers. Simple "toy models" that capture these behaviors would therefore be a big help. I leave it up to the authors whether some of these examples can be relegated to the supplement.

2. There are a great number of variables, so simplification of the notation would be helpful. For example, in Eq. 1 it would be easier to parse of Q was replaced by P, beta by alpha, and j by i. I don't see any problem with using the same variable name in the summations, and it would be easier to understand the equations. (In fact, the authors have made at least one mistake by having too many variables - in the last box of Fig. 1e the Q should be a P. Above Eq. 2, the two appearances of d_ia should be d_alpha i).

3. The histograms in Fig. 1c appear to be the combined results of many independent simulations (and this number should be stated in the caption). However, a given ecosystem only has one set of species. What does that distribution look like for one realization of parameters? It would be helpful to show such individual distributions - ideally along with some measure of agreement between individual distributions and the expected average distribution - as a function of the total number of species. Also, in Fig. 1c, there is a difference between the simulation results and the cavity results for X and N at the lowest bar in the histogram. Given the essentially perfect agreement for the rest of the distribution, some discussion of this deviation is called for.

4. There is a great deal of discussion in the ecology literature about rank-abundance curves, so it would be appropriate to discuss how the distributions of species abundances in the current model compare to actual rank-abundance curves.

5. There are a few misspellings and missing words, so another careful reading of the manuscript would be helpful.

Reviewer #2: The review is uploaded as an attachment.

Reviewer #3: In this manuscript, Feng et al examine the role of trophic structure on ecosystem assembly. The authors' analysis exploits the cavity method, which helps analyzing ecosystems with randomized interactions, and provides powerful intuition about how different observables (e.g., species diversity, biomass) depend on the underlying parameters (e.g., mean and variance in predation rate, species pool size). In particular, the authors use this technique to quantify the relative extent to which an ecosystem is sensitive to changes in primary producers (bottom-up) versus predators or tertiary consumers (top-down). Their analysis shows that the key quantities that determine ecosystem sensitivity or control are the species packing fractions, i.e., the fraction of occupied of niches in each trophic level.

The manuscript is clearly-written and addresses a long-recognized ecological question. I found the "order parameters" suggested by the authors particularly useful and simple to quantify, and the cavity method provides a solid theoretical basis to deploy them. The work also synthesizes and unifies a lot of observations and hypotheses about trophic levels in the ecological literature through a nice extension of MacArthur's classical model, and is thus well-suited for publication in PLoS Computational Biology.

However, to be more widely appreciated by ecologists, I suggest a few points of clarifications about assumptions, as well as a few outstanding questions that the authors could either choose to address in a revision, or alternatively leave a comment in the Discussion. The paper already contains enough results to make the manuscript suitable for publication --- my comments contain suggestions and curiosities.

Major comments

(1) Energy conservation and the 10% rule: Does the model conserve energy? It seems to me that it does not, in the sense that there is no strict bound on how much biomass can be derived from one trophic level and transferred to the next. This seems a bit strange, since in ecology, people typically think that every subsequent trophic level has ~10% the biomass of the previous one, as a result of dissipation and imperfect energy conversion. It would be nice to explore the consequences of such energy loss, since it would make the biomasses of the three trophic levels systematically different. I am curious to see to what extent this would influence the Dtop/Dbottom metrics. In case the authors do not wish to explore this, they could add a note somewhere in the paper.

(1.5) Consumption-conversion asymmetry: On a similar note, the authors assume no asymmetry between consumption and growth (biomass conversion), i.e., there is one set of c's and d's. To what extent does that influence the results? It would be nice to add a note about this assumption as well.

(2) Keystone species: Ecosystems can often experience dramatic changes due to the removal or addition of one "keystone" species. I am curious to understand if any of the surviving species in the simulated ecosystems in this paper are of this kind. Specifically, does the theory expect many keystone species or few? Due to the species in a trophic level being statistically similar, it was not clear to me. It seems like in addition to top down and bottom up control, where the carrying capacity or death rate of all species in a trophic level change, one could also compare the scale of these changes with keystone control, where only the presence of one species changes.

(3) Relation between sensitivity and number of levels: The authors show that many of their steady state properties are robust to including more trophic levels. I, however, could not understand if including more levels would suppress the sensitivity to the bottom-up or top-down controls considered here. For instance, would it be the case that whether an intermediate trophic level is controlled by top or bottom depends not just on the species packing fractions of the top or bottom levels, but also on the trophic distance to these levels?

Minor comments

(1) Is it possible to get multiple stable states in the model? The authors state that their model only has a unique stable steady state, but I saw no reference to a proof in the appendix, or a citation to the claim.

(2) It seems by looking at the figures that top-down control is rare --- most of the phase diagrams show blue (bottom-up control). Is this just by chance due to the parameters sampled, or is this a broader statement? Even in Fig. 3 the order parameters span three orders on the left of 1, while 2 orders to its right.

(3) In Fig. 2c and d, I would suggest plotting the yellow curves (middle trophic level) separately from all the others, since that is the one the reader should focus on. Since all the curves are changing, it took me a while to understand that the yellow one was the focus. This could be done by including the other curves in an inset, or just separately.

**********

Have the authors made all data and (if applicable) computational code underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data and code 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 and code 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 or code —e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

**********

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 #1: No

Reviewer #2: Yes: Onofrio Mazzarisi

Reviewer #3: No

Figure 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. 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 us at figures@plos.org.

Data Requirements:

Please note that, as a condition of publication, PLOS' data policy requires that you make available all data used to draw the conclusions outlined in your manuscript. Data must be deposited in an appropriate repository, included within the body of the manuscript, or uploaded as supporting information. This includes all numerical values that were used to generate graphs, histograms etc.. For an example in PLOS Biology see here: http://www.plosbiology.org/article/info%3Adoi%2F10.1371%2Fjournal.pbio.1001908#s5.

Reproducibility:

To enhance the reproducibility of your results, we recommend that you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. Additionally, PLOS ONE offers an option to publish peer-reviewed clinical study protocols. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols

References:

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.

Attachments

Attachment

Submitted filename: review-feng2023.pdf

Dear Dr. Mehta,

We are pleased to inform you that your manuscript 'Emergent competition shapes top-down versus bottom-up control in multi-trophic ecosystems' has been provisionally accepted for publication in PLOS Computational Biology.

Before your manuscript can be formally accepted you will need to complete some formatting changes, which you will receive in a follow up email. A member of our team will be in touch with a set of requests.

Please note that your manuscript will not be scheduled for publication until you have made the required changes, so a swift response is appreciated.

IMPORTANT: The editorial review process is now complete. PLOS will only permit corrections to spelling, formatting or significant scientific errors from this point onwards. Requests for major changes, or any which affect the scientific understanding of your work, will cause delays to the publication date of your manuscript.

Should you, your institution's press office or the journal office choose to press release your paper, you will automatically be opted out of early publication. We ask that you notify us now if you or your institution is planning to press release the article. All press must be co-ordinated with PLOS.

Thank you again for supporting Open Access publishing; we are looking forward to publishing your work in PLOS Computational Biology. 

Best regards,

Jacopo Grilli

Academic Editor

PLOS Computational Biology

Natalia Komarova

Section Editor

PLOS Computational Biology

***********************************************************

Reviewer's Responses to Questions

Comments to the Authors:

Please note here if the review is uploaded as an attachment.

Reviewer #1: The authors have satisfactorily addressed all my comments, and I am happy to recommend publication.

Reviewer #2: The Authors nicely addressed my comments.

Reviewer #3: I thank the authors for suitably addressing the comments by me and other reviewers. I believe the paper is now greatly strengthened and suitable for publication in PLOS Computational Biology. Congratulations to the authors for this nice work.

**********

Have the authors made all data and (if applicable) computational code underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data and code 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 and code 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 or code —e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

**********

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 #1: No

Reviewer #2: Yes: Onofrio Mazzarisi

Reviewer #3: No