The relationships between box turtle gut microbiomes and personality

Kaija Harlow; Elizabeth K. Service; Jace E. Geiger; Bradley E. Carlson; Steven J.A. Kimble

doi:10.1371/journal.pone.0339132

Peer Review History

Original SubmissionJuly 25, 2025
6 Oct 2025 Decision Letter - Bernd Schierwater, Editor PONE-D-25-40604The Relationships Between Box Turtle Gut Microbiomes and PersonalityPLOS ONE Dear Dr. Harlow, 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. Please submit your revised manuscript by Nov 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 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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In your statement, please include the full name of the IRB or ethics committee who approved or waived your study, as well as whether or not you obtained informed written or verbal consent. If consent was waived for your study, please include this information in your statement as well. 5. Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information. 6. If the reviewer comments include a recommendation to cite specific previously published works, please review and evaluate these publications to determine whether they are relevant and should be cited. There is no requirement to cite these works unless the editor has indicated otherwise. [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: Yes Reviewer #2: Partly ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: No ****** 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 ****** 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: Yes Reviewer #2: No ****** 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 authors have created a very interesting, detailed, and well-written manuscript with the commendable objective of providing novel information to assist in the management and protection of the threatened Eastern Box Turtle species. Although the sample size is quite limited, this is understandable given the species studied. It is also appreciated that the discussion acknowledges the need for increased sample size overall and the need to balance sexes in future studies. The paper is acceptable, however there are several minor notes: The references section does not include numbers that would correspond to the in-text citations. In addition, page numbers are missing. It is stated that a total of 12 turtles were collected but only 11 total turtles deemed bold/shy (first mentioned in Figure 1) with no mention of the 12th. It could be confused that this was either the turtle that supposedly did not emerge after 600 seconds where the trail was terminated (is it not mentioned if this turtle was included with the list of shy individuals or not), or the immature unknown sex individual for sex comparison studies, although only the 10 adults had their sexes determined; so this could be more clearly stated. In addition, cloacal, oral, and skin samples were not taken from all 12 turtles (only either 10 or 11) with no apparent mention for this reason, even though it is mentioned that samples were taken from each encountered individual. In regards to Figure 2: Is there a reason only the Bray-Curtis distance analysis is shown in a figure and not the other tests for beta diversity? Additionally, this figure may work better if “Skin”, “Oral”, and “Cloacal” were shown by their respective A-C designated letters as was included in Figure 1. The text also includes “combined” as a sample type for this test which does not appear in the figure. Lastly, the ellipses are not “shaded”. Side Note: Although not required, consider en dashes for ranges, and not starting a sentence directly with a bracketed citation. Reviewer #2: This interesting study investigates the relationship of Eastern Box Turtle behaviour and their microbiome, on a sample of 12 turtles, collected from several testing sites and tested in a time-to-head-emergence essay that was linked with microbiome analyses from the turtles’ cloacal, skin and oral swabs. The Authors found that females and shy turtles had significantly higher alpha microbiome diversity than males and bold turtles, and there was no significant difference in beta diversity. The Authors also found several overabundant microbial taxa, pathways and modules that differed between bold and shy turtles. The steroid biosynthesis pathway was overrepresented in bold turtles, whereas bile acid biosynthesis pathway and purine degradation to urea module were overrepresented in shy turtles. While the results are overall interesting, I could not identify the main “take home messages” and conclusions of this manuscript. There are many aspects of the manuscript that should be improved before it can be considered for publication, and I list these major and minor point below, hoping they will be helpful for the Authors in revising their manuscript. Major points. Labelling throughout the manuscript should be improved. As the Authors did not conduct repeated testing (L181), labelling behaviours as ‘personality’, ‘boldness’ or ‘shyness’ is misleading, instead of using ‘personality’ as a term, the Authors should use ‘behaviour’. Furthermore, why do Authors make a distinction between “microbiome” and “microbiota” (L76-78) and then use them interchangeably in the text? Was the overall aim of the manuscript just to get more data on Eastern Box Turtles because they are “reptiles and long-lived, non-model organisms” (L28) or that “and that they were used because of “the dire need for more data on their behaviour and microbiome as reptiles and non-model organism” (L15-151). This is a bit weak reason. Methods and data collection are unclear. For instance, it seems that some turtles were already captured and tracked beforehand (“many turtles encountered in this study had been previously captured and tracked” L157-158; “some turtles” L164), but how many turtles were captured of the ones tested in this manuscript is not precisely given. Further, how were the tests done, was the “time-to-head-emergence” test conducted first, then the measurements, then the swabs or did you follow other order of data collection? How were the turtles located? What motivated your decision to label turtles “bold” if they emerged in less than 10 and “shy” in more than 10 seconds – was there any biological reason for this? Why did the Authors conduct only one behavioural test, when they knew that repeated testing is needed to assess personality? Statistical analyses should be carefully conducted and results discussed with taking a small sample size that the Authors collected in mind (only 12 turtles, uneven number of females and males, comparisons with differing numbers e.g. 7 versus 2 animals, etc). Statistical details should not be reported under Figure and Table descriptions, but instead in the main text of the manuscript. The analyses conducted with linking behaviour and microbiome are not very clearly described, so the reader will be left somewhat puzzled what was done where. Do these analyses refer to L210-212? Which analyses were done to check the effect of personality, sex, age etc on microbiome? L250. What kind of interaction was found in terms of personality type & sex? L333-334. Here it seems that sex effects are convoluted with age, as IDs of unknown sex were also the juvenile and subadult ones? Please clarify. Literature coverage was made somewhat superficially, without giving specific examples. This is particularly true for Abstract (very generally written without discussion and conclusion sentences, giving general claims on phenomena that are quite underexplored; e.g. L21-22, L23-24, L24-25, L44-45). In general, details of previous studies are missing from the manuscript. Related point is that it is not clear from the Discussion what the Results represent and why they are important. Conclusion and overall messages that the reader can get from the manuscript are not clearly conveyed. References are very messy and unnumbered which makes it difficult to follow numbering in text. There is no consistent style in capitalization of words within a title. Editor names are given for journal articles which is not needed, links that are not doi identifiers, species names are not in italic, journal names are not capitalized etc. Minor points. L50-51 is redundant with L61-64. L54. “to explain variation in personality” can be omitted. L135. What does it mean that “the microbiomes will have significant beta diversities”? Fig 1. N=7 bold individuals? L275. Delete first “bold”. L301. “by personality” -> “between bold and shy”. L309. “project” -> “study” L312-313. “there would be significant beta diversities between them” -> beta diversities would significantly differ between them” L313. Delete second “predicted” L319-320. Delete “or show significant beta diversity” and exchange to “but did not differ significantly in alpha or beta diversity.” Delete “group” and “also”. L324. Exchange to “the resulting heightened levels of cortisol can lead to…” L326-327. Higher corticosterone than who? Also, please distinguish sentence on previous study and new finding from this study as otherwise it is confusing. L343. Male and female juveniles, or males and females? Please clarify why. L356-357. Latin name of species should be in italic. L377-378. Did you mean “were more abundant in oral and skin swabs of bold turtles” ? L388. Add a comma after “behavior” L390. Delete “for this taxon” L407. Delete “predicted” L410. Add “in” before “current study” L412. “study” -> “investigation” L431. Do you mean “cloacal swabs” instead of “gut microbiome swabs”? ****** 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. 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: Yes: Jason G. Randall Reviewer #2: 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. https://doi.org/10.1371/journal.pone.0339132.r001
Revision 1
25 Nov 2025 Author Response Reviewer 1: The references section does not include numbers that would correspond to the in-text citations. In addition, page numbers are missing. ● Numbers have been added to all references that correspond to the in-text citations. Pages have been numbered. It is stated that a total of 12 turtles were collected but only 11 total turtles deemed bold/shy (first mentioned in Figure 1) with no mention of the 12th. It could be confused that this was either the turtle that supposedly did not emerge after 600 seconds where the trail was terminated (is it not mentioned if this turtle was included with the list of shy individuals or not), or the immature unknown sex individual for sex comparison studies, although only the 10 adults had their sexes determined; so this could be more clearly stated. In addition, cloacal, oral, and skin samples were not taken from all 12 turtles (only either 10 or 11) with no apparent mention for this reason, even though it is mentioned that samples were taken from each encountered individual.: ● Thank you for your feedback. We came to the realization that one turtle was counted twice for a portion of the analyses. We corrected our sample size to 11, re-ran all analyses, and updated the statistics presented in the results section. There were no significant statistical changes after correcting for this. At least one type of sample was taken from each individual, however we were not able to collect all three types of samples from all individuals due to post-collection failures (L277–279). No turtle was entirely excluded from this study. In regards to Figure 2: Is there a reason only the Bray-Curtis distance analysis is shown in a figure and not the other tests for beta diversity? Additionally, this figure may work better if “Skin”, “Oral”, and “Cloacal” were shown by their respective A-C designated letters as was included in Figure 1. The text also includes “combined” as a sample type for this test which does not appear in the figure. Lastly, the ellipses are not “shaded”.: ● We chose not to include the other figures as to not overwhelm the manuscript with unnecessary graphics, but have included these in the Supplementary Information. The ellipses are now shaded. Figure 2 has been revised to show sample types by their A-C designated letters. Although not required, consider en dashes for ranges, and not starting a sentence directly with a bracketed citation: ● En dashes are now used for ranges, and no sentences begin directly with a bracketed citation. Reviewer 2: Labelling throughout the manuscript should be improved. As the Authors did not conduct repeated testing (L181), labelling behaviours as ‘personality’, ‘boldness’ or ‘shyness’ is misleading, instead of using ‘personality’ as a term, the Authors should use ‘behaviour’. Furthermore, why do Authors make a distinction between “microbiome” and “microbiota” (L76-78) and then use them interchangeably in the text? ● L220–225: We have placed greater emphasis on the fact that several previous papers establish that the behavioral assay used is highly consistent in these turtles, making this behavioral measurement a reasonable proxy for personality, and added additional papers that indeed use this behavioral assay in this citation. In addition, there were logistical constraints due to concurrent research activities; we have added this statement to the manuscript as well. ● We have reviewed our use of the terms ‘microbiome’ and ‘microbiota’ and corrected the term used based on our given definition, changing some previous instances of ‘microbiome’ to ‘microbiota’. Was the overall aim of the manuscript just to get more data on Eastern Box Turtles because they are “reptiles and long-lived, non-model organisms” (L28) or that “and that they were used because of “the dire need for more data on their behaviour and microbiome as reptiles and non-model organism” (L15-151). This is a bit weak reason. ● L32–33, 37–40 153-166: Thank you for your feedback. We have revised the text in the abstract to clarify our overall aim. ● L153-166: We have also revised the description of our primary objectives in the last paragraph of the Introduction. Methods and data collection are unclear. For instance, it seems that some turtles were already captured and tracked beforehand (“many turtles encountered in this study had been previously captured and tracked” L157-158; “some turtles” L164), but how many turtles were captured of the ones tested in this manuscript is not precisely given. Further, how were the tests done, was the “time-to-head-emergence” test conducted first, then the measurements, then the swabs or did you follow other order of data collection? How were the turtles located? What motivated your decision to label turtles “bold” if they emerged in less than 10 and “shy” in more than 10 seconds – was there any biological reason for this? Why did the Authors conduct only one behavioural test, when they knew that repeated testing is needed to assess personality? ● L200-204: The order and rationale for the order has been specified. Head emergence assay was done first, then swab collection, then measurements. This prevented handling from influencing behavior measurements, and prevented measuring tools from contaminating the turtle prior to swabbing. ● L196–200: Turtles used in this study were not being tracked at the time of this study. Seven had been previously captured, and two of those had been previously radiotracked. This has been clarified in the manuscript. ● L220-221: We defined ‘bold’ and ‘shy’ based on a 10-second head-emergence cutoff using data from Kashon & Carlson 2018, who found mean emergence to be strongly bimodal in the same study population. Specifically, they found similar numbers of individual turtles to emerge within 7 seconds or less on average (across repeated trials) or after more than 58 seconds on average; they found no intermediate behavioral phenotypes. ● L221-228: Repeated testing: see previous justification related to the high repeatability. In addition, there were logistical constraints due to concurrent research activities. We have added this information into the manuscript Statistical analyses should be carefully conducted and results discussed with taking a small sample size that the Authors collected in mind (only 12 turtles, uneven number of females and males, comparisons with differing numbers e.g. 7 versus 2 animals, etc). ● L63–64, 518–520: Thank you for your feedback. In our Abstract, we now include that our results should be considered in the context of limited sample sizes (L63–64). We also added a sentence that addresses this in the Conclusion (L518–520). Throughout the Discussion, we also mention that an increase in sample size would be beneficial to increase support for our results. Statistical details should not be reported under Figure and Table descriptions, but instead in the main text of the manuscript. ● Thank you for your feedback. We found no requirements to exclude statistical details from figures and tables descriptions in the formatting requirements from PLOS One. We choose to have those details in the captions to help the figures and tables stand alone from the main text. The analyses conducted with linking behaviour and microbiome are not very clearly described, so the reader will be left somewhat puzzled what was done where. Do these analyses refer to L210-212? Which analyses were done to check the effect of personality, sex, age etc on microbiome? L250. What kind of interaction was found in terms of personality type & sex? L333-334. Here it seems that sex effects are convoluted with age, as IDs of unknown sex were also the juvenile and subadult ones? Please clarify. ● L302–311, 382–424: Thank you for your feedback. We edited the text (L302–311) to indicate in more detail the specific test and result found between the microbiome to sex and/or personality. In the Discussion (L382–424) we included more detail on the relationship between the microbiome, sex, and age. Literature coverage was made somewhat superficially, without giving specific examples. This is particularly true for Abstract (very generally written without discussion and conclusion sentences, giving general claims on phenomena that are quite underexplored; e.g. L21-22, L23-24, L24-25, L44-45). In general, details of previous studies are missing from the manuscript. ● Thank you for your feedback. We heavily edited the Abstract to better summarize the content of the paper and meet the 300 word-limit requirement. We now have a Discussion sentence that notes our limited sample size and better contextualizes our results. In our Introduction, we go into more detail on the general phenomena that seem underexplored in our limited Abstract (i.e., individual personality shaping an ecosystem [L77-80], boldness/shyness [L84-94], microbial composition [95-105], the influence of the gut microbiome [L106-116] and specific examples [L117-128]). Related point is that it is not clear from the Discussion what the Results represent and why they are important. ● L373-374, 514-521: Thank you for your feedback. Additional information has been added to the beginning of the discussion (L373-374) and the conclusion (L514–521) to help convey the results, and their implications and importance. Conclusion and overall messages that the reader can get from the manuscript are not clearly conveyed. ● Thank you for your feedback. Additional information has been added to the conclusion (L514–521) to help convey the results, their implications and importance, and limitations. References are very messy and unnumbered which makes it difficult to follow numbering in text. There is no consistent style in capitalization of words within a title. Editor names are given for journal articles which is not needed, links that are not doi identifiers, species names are not in italic, journal names are not capitalized etc. • Capitalization has been fixed to sentence-case. Editors are now only named in cited chapters in books, as per ICJME reference examples on the NIH website (https://www.nlm.nih.gov/bsd/uniform_requirements.html#journals). Links that are not DOI identifiers are now cited for online journal articles only, as per ICJME references on the NIH website (see above link). All species names are now in italics, and journal names are now in NLM abbreviated form and capitalized. L50-51 is redundant with L61-64. – Corrected; lines 61-64 have been omitted. L54. “to explain variation in personality” can be omitted. – Corrected L135. What does it mean that “the microbiomes will have significant beta diversities”? – Corrected; further context added (L160–162) Fig 1. N=7 bold individuals? – Corrected to N = 6 L275. Delete first “bold”. – Corrected L301. “by personality” -> “between bold and shy”. – Corrected L309. “project” -> “study” – Corrected L312-313. “there would be significant beta diversities between them” -> beta diversities would significantly differ between them” – Corrected L313. Delete second “predicted” – Corrected L319-320. Delete “or show significant beta diversity” and exchange to “but did not differ significantly in alpha or beta diversity.” Delete “group” and “also”. – Corrected L324. Exchange to “the resulting heightened levels of cortisol can lead to…” – Corrected L326-327. Higher corticosterone than who? Also, please distinguish sentence on previous study and new finding from this study as otherwise it is confusing. – Corrected; clarified (L387-396) L343. Male and female juveniles, or males and females? Please clarify why. – Corrected; clarified (L 408–412). L356-357. Latin name of species should be in italic. – Corrected L377-378. Did you mean “were more abundant in oral and skin swabs of bold turtles” ? – Yes; corrected L388. Add a comma after “behavior” – Corrected L390. Delete “for this taxon” – Corrected L407. Delete “predicted” – Corrected L410. Add “in” before “current study” – Corrected L412. “study” -> “investigation” – Corrected L431. Do you mean “cloacal swabs” instead of “gut microbiome swabs”? – Yes; corrected Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0339132.r002
2 Dec 2025 Decision Letter - Bernd Schierwater, Editor The Relationships Between Box Turtle Gut Microbiomes and Personality PONE-D-25-40604R1 Dear Dr. Harlow, 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 will be generated when your article is formally accepted. Please note, if your institution has a publishing partnership with PLOS and your article meets the relevant criteria, all or part of your publication costs will be covered. Please make sure your user information is up-to-date by logging into Editorial Manager at Editorial Manager® and clicking the ‘Update My Information' link at the top of the page. For questions related to billing, please contact billing support. 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, Bernd Schierwater, Ph.D Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0339132.r003
Formally Accepted
Acceptance Letter - Bernd Schierwater, Editor PONE-D-25-40604R1 PLOS One Dear Dr. Harlow, I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS One. Congratulations! Your manuscript is now being handed over to our production team. At this stage, our production department will prepare your paper for publication. This includes ensuring the following: * All references, tables, and figures are properly cited * All relevant supporting information is included in the manuscript submission, * There are no issues that prevent the paper from being properly typeset You will receive further instructions from the production team, including instructions on how to review your proof when it is ready. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few days to review your paper and let you know the next and final steps. Lastly, 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. You will receive an invoice from PLOS for your publication fee after your manuscript has reached the completed accept phase. If you receive an email requesting payment before acceptance or for any other service, this may be a phishing scheme. Learn how to identify phishing emails and protect your accounts at https://explore.plos.org/phishing. If we can help with anything else, please email us at customercare@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 Prof. Bernd Schierwater Academic Editor PLOS One https://doi.org/10.1371/journal.pone.0339132.r004

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