PCSY-D-24-00133Exploring Temperature Effects on Tick Population Dynamics: What are Agent-Based Models Saying?PLOS Complex SystemsDear Dr. Chenaoui,Thank you for submitting your manuscript to PLOS Complex Systems. After careful consideration, we feel that it has merit but does not fully meet PLOS Complex Systems'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.Please submit your revised manuscript within 60 days Jan 13 2025 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 complexsystems@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pcsy/ 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 editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'. This file does not need to include responses to any formatting updates and technical items listed in the 'Journal Requirements' section below.* 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, competing interests statement, or data availability statement, please make these updates within the submission form at the time of resubmission. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.We look forward to receiving your revised manuscript.Kind regards,Corentin BriatAcademic EditorPLOS Complex SystemsCorentin BriatAcademic EditorPLOS Complex SystemsHocine CherifiEditor-in-ChiefPLOS Complex Systems

 Journal Requirements:

1. We ask that a manuscript source file is provided at Revision. Please upload your manuscript file as a .doc, .docx, .rtf or .tex.

2. We have amended your Competing Interest statement to comply with journal style. We kindly ask that you double check the statement and let us know if anything is incorrect.

Additional Editor Comments (if provided):

I have received three mixed reviews. The reviewers make several comments regarding certain technical choices in the paper that will need to be better motivated or justified in the revised version of the manuscript. Please carefully address all the comments of the reviewers carefully and indicate in colored text all the major changes in the manuscript to facilitate the review process.

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Reviewers' Comments:

Reviewer's Responses to Questions

Comments to the Author

1. Does this manuscript meet PLOS Complex Systems’s publication criteria? Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe methodologically and ethically rigorous research with conclusions that are appropriately drawn based on the data presented.

Reviewer #1: Yes

Reviewer #2: Partly

Reviewer #3: Partly

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

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: I don't know

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3. Have the authors made all data underlying the findings in their manuscript fully available (please refer to the Data Availability Statement at the start of the manuscript PDF file)?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception. 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

Reviewer #3: Yes

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4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS Complex Systems 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: Yes

Reviewer #2: Yes

Reviewer #3: Yes

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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: The manuscript explores the impact of temperature fluctuations on tick population dynamics using an agent-based model. It simulates how variations in temperature affect tick populations across different life stages and scenarios over a ten-year period. The paper results highlight temperature's important role in tick population growth and the importance of seasonal variability.

General remarks :

- The manuscript is relevant, addressing climate change and vector-borne disease modeling.

- The focus on ABM applied to tick populations is well-founded, but the authors should emphasize why they chose ABM approach.

- The methodology is thorough and the statistical analysis is robust.

- The papers isolates the effect of temperature on tick population growth and mentions other factors (like humidity).

- The discussion effectively highlights the role of temperature in driving tick population growth. However, it does not address the broader epidemiological implications as the relevance of tick populations lies in their role as disease vectors.

Recommendations:

- Motivate more the use of ABMs, how do they compare to other models in this particular case. The paper needs more in-depth comparisons with previous studies / models.

- Extend the discussion to include :

o More epidemiological context and the role of ticks in driving disease

o Highlight future work to take account of other factors like humidity.

- The writing is generally clear however some sections are overly verbose. Avoid redundancies and complex sentence structures.

Decision: The paper is promising but minor revisions required.

Reviewer #2: The manuscript looks at a good question to seek the potential outcome for tick populations during warming climate. My biggest concern for this paper is that the system is set up based on a two-host tick for the hosts, but then the parameters are taken from Ixodes scapularis, which is a three host tick. Additionally, Ixodes scapularis also are not known to feed on cattle so that is an odd choice for the host. It seems the model is based on a wide mixture of tick species, which makes it difficult to assess the validity of the outcomes. The authors need to pick a single tick species or a couple and then build on that to allow for better results. Additionally, findings for one tick species are not likely to be applicable to other species given the wide variety of phenological timing, host preferences, and environmental survival that each species has. It would also be helpful to have a better model description, e.g., using the ODD design (Grimm V, Railsback SF, Vincenot CE, Berger U, Gallagher C, DeAngelis DL, Edmonds B, Ge J, Giske J, Groeneveld J, Johnston AS. The ODD protocol for describing agent-based and other simulation models: A second update to improve clarity, replication, and structural realism. Journal of Artificial Societies and Social Simulation. 2020 Jan 1;23(2).)

Overall, the model is sound computationally, but the results are not useful to interpret given the mixture of inputs.

Reviewer #3: Chenaoui et al. PLoSComplexSystems

This is an article on a subject of much interest. Whilst I’m not competent on the details of the ABMs employed, I am a little lost as there seems to be not much information on the models themselves, particularly that of the vertebrate hosts. The Figures that follow the manuscript don’t seem to be in order nor accessible through clicking on the link where they are stated in the txt which doesn’t help know which figure is what.

For example in the methods (lines 100+) it is written: “Two distinct time steps are used for both agent behavior and actions. Ecological processes are executed every hour (e.g. host mobility etc.), and physiological processes for the vector agent (e.g. tick fecundity, mortality etc.) are executed daily. The process scheduling has a logical sequence of the various stages of the ticks life cycle (refer to Fig 2).”

It would be nice to at least know what were the key parameters/estimates for host mobility etc and what “etc” is. The associated figure seems to be the third one at the end of the text, but it’s not very obviously associated with what is written in the text. This could be a lot clearer.

There is a lot of explanation of the scenarios, which is good, but we really need more information on the ABMs themselves.

All in all it’s difficult to follow and the figures don’t seem to follow which makes it even harder to follow.

Given that this is all about temperature and simulating various changes in this variable, it would be good to know what the range of temperatures used were. It is well-known that above certain temperatures the ticks will no longer quest. In particular what are “extreme temperatures” that are cited throughout.

In short, it could be written in a more comprehensive fashion.

More minor comments below.

Line 72: The period of time for the development of a fed larva to a nymph stage has been estimated at longer time intervals (ie up to 3-4 months, which are temperature-dependent. MacLeod, J. 1934. Ixodes ricinus in relation to its physical environment. The influence of climate on development. Parasitology 26: 282–305. Vassallo, M. et al. (2000) Temporal distribution of the annual nymph stock of Ixodes ricinus. Exp.Appl. Acarol. 28: 1-9. Randolph SE et al. An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus. Int J Parasitol. 2002 Jul;32(8):979-89. doi: 10.1016/s0020-7519(02)00030-9.

Line 75: there is also the question of developmental diapause. Both this and behavioral diapause are well discussed in Gray et al. Developmental diapause is probably triggered by photoperiod as opposed to temperature. Gray JS, et al. Diapause in ticks of the medically important Ixodes ricinus species complex. Ticks Tick Borne Dis. 2016 Jul;7(5):992-1003. doi:10.1016/j.ttbdis.2016.05.006.

Line 91/92: Genera of ticks in italics.

Line 97: Probably need some justification as to why humidity was not considered important, even if it is not considered for purposes of simplicity.

Empirical validation paragraph (starting line 120: the authors use data from 3 published articles by Ogden et al. which concern Ixodes scapularis and thus the USA. I don’t know where in the USA the tick data were taken, but I imagine they would cover the whole of the East of the USA. Can the authors perhaps be more explicit about the geographical area and which temperatures were used, as the area will be very large.

Same paragraph: The paragraph starting line 126 actually gives results not methods. It is also hard to know what this means for the interpretation of the subsequent analyses of the differing scenarios.

Line 201 vs 275: This part is a bit confusingly written. It reads: “…introduces a parameter α that controls the curvature signal. The curvature is broad at low α values. The temperature reaches extreme values more rapidly than higher α values to enable more extended periods at extreme temperatures. When α tends asymptotically towards 0, the signal tends towards a square wave. For example, when α equals 5, the signal slowly to the extreme value…” This seems to contradict the results line 275 where it reads: “values of α, in the case of α = 5, representing a long duration of autumn and spring seasons,…”

Do small or high alpha values lead to extended seasons?

Discussion: This is quite good albeit a bit verbose.

There is, however, often stated that the predicted increases in temperatures cause an explosion of tick numbers. This would assume that the tick population is infinite, which it is not and there is no reference to the impact of temperature changes on the host density and behaviour, which will surely impact the tick densities over time.

The limitations paragraph is a bit cursory. It admits that other factors, such as humidity, are important but leaves it at that. It would be good to know, at least speculatively, what effect its inclusion might have on the results shown. The diapause issue needs to be discussed somewhere, possibly here. This is an important temperature-independent process in part (developmental diapause).

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6. 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.

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For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

Reviewer #3: No

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 [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.] Figure resubmission: 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. If there are other versions of figure files still present in your submission file inventory at resubmission, please replace them with the PACE-processed versions. Reproducibility: To enhance the reproducibility of your results, we recommend that authors of applicable studies deposit 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

PCSY-D-24-00133R1

Exploring Temperature Effects on Tick Population Dynamics: What are Agent-Based Models Saying?

PLOS Complex Systems

Dear Dr. Chenaoui,

Thank you for submitting your manuscript to PLOS Complex Systems. After careful consideration, we feel that it has merit but does not fully meet PLOS Complex Systems'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.

Please submit your revised manuscript within 60 days May 20 2025 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 complexsystems@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pcsy/ 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 editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'. This file does not need to include responses to any formatting updates and technical items listed in the 'Journal Requirements' section below.

* 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, competing interests statement, or data availability statement, please make these updates within the submission form at the time of resubmission. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

We look forward to receiving your revised manuscript.

Kind regards,

Corentin Briat

Academic Editor

PLOS Complex Systems

Corentin Briat

Academic Editor

PLOS Complex Systems

Hocine Cherifi

Editor-in-Chief

PLOS Complex Systems

Additional Editor Comments (if provided):

I have received mixed reviews. While two reviewers recommended acceptance, one raised key concerns that must be addressed:

- Your model focuses on temperature but omits humidity, which is equally important in tick biology. If adding humidity is not feasible, please emphasize this limitation more clearly as well as its impact on the validity of the model.

- Since your data are drawn from Ixodes scapularis in North America, please specify that your results apply to this species and region.

- Clarify the terms "small" and "large" hosts to avoid confusion with livestock.

- Address missing references and justify parameters with unclear origins, particularly the upper lethal temperature values.

- Improve wording to better align with standard tick biology and ecology terminology.

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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 #1: All comments have been addressed

Reviewer #2: (No Response)

Reviewer #3: All comments have been addressed

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2. Does this manuscript meet PLOS Complex Systems's publication criteria? Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe methodologically and ethically rigorous research with conclusions that are appropriately drawn based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

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

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: I don't know

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4. Have the authors made all data underlying the findings in their manuscript fully available (please refer to the Data Availability Statement at the start of the manuscript PDF file)?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception. 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: (No Response)

Reviewer #3: Yes

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS Complex Systems 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: Yes

Reviewer #2: (No Response)

Reviewer #3: Yes

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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 #1: The authors have made the necessary revisions, and I am satisfied with the changes. I recommend acceptance.

Reviewer #2: I thank the authors for their responses to my previous questions and concerns. I am still very concerned about a couple fundamental items.

1. The current model looks strictly at temperature as part of climate change, and while temperature plays a crucial role in many aspects of tick biology, humidity at the micro-climate level is equally if not more critical. Increased temperatures by definition will alter the saturation deficit and thus humidity. This interplay is critical to understanding the future predictions for TBD. This is listed as a limitation, but the it would be helpful to be added to the model for more realistic results.

2. The authors state that they are drawing most of the data for their model from Ixodes scapularis in North America, and so this paper should be written to apply to that tick in that location. Tick species vary widely in their response to temperature plus their host usage, survival ability, and more. This model doesn't not represent the findings for all ticks, and thus should be restricted to the species and location from which the information is derived. This does not limit the value of the findings, but rather it keeps the findings in the biologically correct context.

3. The authors clarified that host types are meant to represent small and large hosts. I would encourage the authors to simply change the language to those terms to prevent confusion by the reader to interpret the large hosts as domestic livestock.

4. Many of the parameters in Supplemental Table 2 have "?" for the reference, which makes it impossible to understand where data like a maximum lethal temperature for various life stages comes from. I have not seen the upper limits that are listed there previous, and I am not sure how these are used. For example, I have collected plenty of adult ticks well above 35C.

Overall, there is a need to improve the terminology and phrases used in the paper to better reflect the common English terms for tick biology and ecology.

Reviewer #3: I thank the authors for addressing my comments. It reads much much clearer now.

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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.

Do you want your identity to be public for this peer review? If you choose “no”, your identity will remain anonymous but your review may still be made public.

For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

Reviewer #3: No

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[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.]

Figure resubmission:

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. If there are other versions of figure files still present in your submission file inventory at resubmission, please replace them with the PACE-processed versions.

Reproducibility:

To enhance the reproducibility of your results, we recommend that authors of applicable studies deposit 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

Exploring Temperature Effects on Tick Population Dynamics: What are Agent-Based Models Saying?

PCSY-D-24-00133R2

Dear Mrs Chenaoui,

We are pleased to inform you that your manuscript 'Exploring Temperature Effects on Tick Population Dynamics: What are Agent-Based Models Saying?' has been provisionally accepted for publication in PLOS Complex Systems.

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

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.

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 complexsystems@plos.org.

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

Best regards,

Louxin Zhang

Section Editor

PLOS Complex Systems

Hocine Cherifi

Editor-in-Chief

PLOS Complex Systems

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The revised manuscript presents a valuable study on the effects of temperature on tick population dynamics. As noted by the reviewers, the results are important and the methodology is sound.

The only issue raised by Reviewer 2 is minor and can be easily addressed. Therefore, I recommend acceptance of the manuscript. Of course, the authors should revise the ms to respond the only comment.

Reviewer Comments (if any, and for reference):

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 #2: (No Response)

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2. Does this manuscript meet PLOS Complex Systems's publication criteria? Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe methodologically and ethically rigorous research with conclusions that are appropriately drawn based on the data presented.

Reviewer #2: Yes

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

Reviewer #2: Yes

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4. Have the authors made all data underlying the findings in their manuscript fully available (please refer to the Data Availability Statement at the start of the manuscript PDF file)?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception. 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 #2: Yes

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS Complex Systems 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 #2: Yes

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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 #2: The authors have addressed my comments. I understand that the authors are using "Cattle" in a generic sense, but I would strongly argue that the authors need to change this to some other more realistic large mammal to prevent confusion by the reader. A simple search and replace of "cattle" with "deer" or even "large mammal" is critical for the validity of this model.

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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.

Do you want your identity to be public for this peer review? If you choose “no”, your identity will remain anonymous but your review may still be made public.

For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #2: No

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