Efficacy of various survey methods to detect an experimental population of spot-tailed earless lizards: A case study

Evan Drake Rangel; Scott E. Henke; David B. Wester; Gabriel Andrade-Ponce; Ruby A. Ayala; Cord B. Eversole

doi:10.1371/journal.pone.0336129

Peer Review History

Original SubmissionMarch 29, 2025
1 Jul 2025 Decision Letter - Edvard Mizsei, Editor Dear Dr. Henke, 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 Aug 15 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. 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'. 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To do this, go to ‘Update my Information’ (in the upper left-hand corner of the main menu), and click on the Fetch/Validate link next to the ORCID field. This will take you to the ORCID site and allow you to create a new iD or authenticate a pre-existing iD in Editorial Manager. 4. Your ethics statement should only appear in the Methods section of your manuscript. If your ethics statement is written in any section besides the Methods, please move it to the Methods section and delete it from any other section. Please ensure that your ethics statement is included in your manuscript, as the ethics statement entered into the online submission form will not be published alongside your manuscript. Additional Editor Comments (if provided): I note several areas where the manuscript would benefit from clarification and greater consistency: Method nomenclature: Please harmonise the names of your survey techniques throughout. For example, lines 220–223 refer to “rock-mound trapping,” whereas elsewhere you use “rock mounds.” Survey chronology: The temporality of your surveys is difficult to follow. I recommend adding a schematic (e.g. a figure or table) with time on the x-axis and survey method on the y-axis to illustrate the sequence and any overlap of techniques. eDNA interpretation: Clarify whether and how environmental DNA may have accumulated over the course of the study. Modelling approaches: I was surprised that the authors did not consider occupancy and n-mixture models, both of which have variants for single- and multiple-visit sampling scenarios (see MacKenzie, Royle & Sólymos). Please discuss why these frameworks were omitted or, preferably, reanalyse your data using one or both methods. Detectability fundamentals: I suggest incorporating more of the foundational sampling and analytical methods suitable for situations in which detectability is less than one and not constant (see Murray & Sandercock’s Population Ecology in Practice, Fig. 3.1). Please address these editorial points alongside all comments raised by the reviewers in your revised submission. [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? Reviewer #1: Yes Reviewer #2: Yes ******** 2. Has the statistical analysis been performed appropriately and rigorously? -->?> Reviewer #1: Yes Reviewer #2: Yes ****** 3. Have the authors made all data underlying the findings in their manuscript fully available??> The PLOS Data policy Reviewer #1: No Reviewer #2: Yes ****** 4. Is the manuscript presented in an intelligible fashion and written in standard English??> Reviewer #1: Yes Reviewer #2: Yes ****** Reviewer #1: I am aware of the limitations of the model, species, and space, but some of the biology of the species might be missing from the discussion. STELs normal behaviours might be inhibited due to the translocation, Cooper (2003) found that lizards from that genus change behaviour due to severe changes in body condition (autotomy), they might do it too when translocated, and be less active when that happens, so detectability might be less. Cooper and Guilette (1991) found sexual dimorphic changes in their behaviour too. What sex where the individuals you translocated? Telemetry, particularly some pit tags, or other short-distance telemetry would be able to answer those kind of questions and let you know if the lizards where there but you couldn't detect them. Comparing your results to trying to count them on the field, where they naturally live would be a great next step, maybe there the other methods might be more useful, as individuals would be in their natural habitat. Is it possible that the time needed for eDNA (and chemicals detected by dogs) to be available in sufficient amounts was too short in your study? The individuals translocated where left there? If so, doesn´t it places an ethical dilemma? Both species do not occur naturally in the same place. Could they reproduce between both of them? Couldn't the project take the 39 living ones back to their natural habitat? It might be important as at least the Tamaulipecan one is endangered. Aren't numbers of STELs found by both direct systematic search and cross road search too small for statistics to have enough power to bring solid conclusions? I would need to see the model structure, results, residuals and the data, at least a summary for me to be able to reach a conclusion. I can asume those earless lizards are very sensitive to vibrations in the ground, so could ATVs be bothering or scaring them so they hide resulting in a lower detectability and observation rate, compared to a human walking over a dirt road? The habitat you translocated them to was different from the one they lived in, so you had to take out the native vegetation and allow something somewhat alike their habitat to grow? Could that be accounted for to explain the low detection ratio? More attractive and informative figures, including maps would be appreciated, together with STELs pictures, as this is an online only journal they wouldn't cost more, but could enrich the manuscript I would be delighted to read a revised version of this manuscript Reviewer #2: The STEL were placed in a novel environment, which may represent the most vulnerable aspect of the experimental design. Any research involving these two species—or closely related ones—regarding animal personality in unfamiliar settings or other ethological factors should be taken into account. Such studies are essential for contextualizing and refining the interpretation of these results. Accordingly, this limitation should be acknowledged in the discussion and explicitly mentioned as a cautionary note in the abstract. ****** 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: EDGARD DAVID MASON-ROMO, PhD 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.0336129.r001
Revision 1
15 Sep 2025 Author Response Comments of Editor and Reviewers and Responses of Authors to Comments Below are the comments of the Editor and two reviewers to our manuscript. The author(s) responses are listed below each comment and are highlighted in Red. Editor Comments: I note several areas where the manuscript would benefit from clarification and greater consistency: Method nomenclature: Please harmonise the names of your survey techniques throughout. For example, lines 220–223 refer to “rock-mound trapping,” whereas elsewhere you use “rock mounds.” The manuscript was checked and revised. Method names have been changed, as needed, to maintain consistency throughout the manuscript. Survey chronology: The temporality of your surveys is difficult to follow. I recommend adding a schematic (e.g. a figure or table) with time on the x-axis and survey method on the y-axis to illustrate the sequence and any overlap of techniques. A figure has been added to provide the chronology of events for each method at each STEL density. Hopefully the figure provides clarification as to what was done during each survey period. eDNA interpretation: Clarify whether and how environmental DNA may have accumulated over the course of the study. Greater explanation of the eDNA results have been provided within the Discussion section and we hope provides clarity as to why eDNA did not appear to accumulate over time as expected. Modelling approaches: I was surprised that the authors did not consider occupancy and n-mixture models, both of which have variants for single- and multiple-visit sampling scenarios (see MacKenzie, Royle & Sólymos). Please discuss why these frameworks were omitted or, preferably, reanalyse your data using one or both methods. The goal was to test differences in detectability efficiency among methods, not to estimate species density, which is already known. This is an important point the reviewer may be overlooking. Both occupancy and N-mixture models are designed to estimate abundance or presence while accounting for imperfect detection. Although these models can be used to make inferences about the detection process, this is not appropriate when the sole objective is to model detection itself. To explain this, it’s useful to briefly describe how hierarchical models are structured. In general, both occupancy and N-mixture models consist of two linked GLMs: one that models the ecological process (abundance or occupancy), and another that models the observational process (detection). In this case, we're specifically interested in the observational component, so there’s no point in adding the ecological component to the equation — since abundance is already known. Additionally, we wouldn't recommend hierarchical models in this case, as the sample size for each method is too small. In theory, sample sizes below 25, with six repetitions and low detection probability (as seen in the new analysis), can result in high bias in N-mixture models. Each methodology in our study has only five spatial replicates. Moreover, since we experienced convergence issues even with a GLM, hierarchical models would likely perform worse. This concern is supported by previous studies showing that small sample sizes and low detectability can produce unreliable estimates and strong biases in N-mixture models (Ficetola et al. 2018; Duarte et al. 2018). • Ficetola, G.F., Barzaghi, B., Melotto, A. et al. (2018). N-mixture models reliably estimate the abundance of small vertebrates. Scientific Reports, 8, 10357. • Duarte, A., Adams, M.J., & Peterson, J.T. (2018). Fitting N-mixture models to count data with unmodeled heterogeneity: Bias, diagnostics, and alternative approaches. Ecological Modelling, 374, 51–59. Detectability fundamentals: I suggest incorporating more of the foundational sampling and analytical methods suitable for situations in which detectability is less than one and not constant (see Murray & Sandercock’s Population Ecology in Practice, Fig. 3.1). To address the modeling and detectability concerns, we have added a binomial GLM, so that the response variable reflects detection probabilities. The predictors remain the same — abundance treatments and methodologies — but such a model would strengthen our conclusion because initially we failed to detect differences between road cruising and visual searches, but as pointed out, the power of test was low due to sample size. Adding the binomial GLM has greater power of the test, and with both methods displaying similar conclusions, strengthens the manuscript. Please address these editorial points alongside all comments raised by the reviewers in your revised submission. Reviewer's Responses to Questions 1. Is the manuscript technically sound, and do the data support the conclusions? Reviewer #1: Yes Reviewer #2: Yes ________________________________________ 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes ________________________________________ 3. Have the authors made all data underlying the findings in their manuscript fully available? Reviewer #1: No Data is available on FigShare – STEL Data file. Some data (i.e., location data) is restricted due to Texas State private properties regulations. New analyses will be added to this file so analyses are publicly available. Reviewer #2: Yes ________________________________________ 4. Is the manuscript presented in an intelligible fashion and written in standard English? Reviewer #1: Yes Reviewer #2: Yes ________________________________________ Review Comments to the Author Reviewer #1: I am aware of the limitations of the model, species, and space, but some of the biology of the species might be missing from the discussion. STELs normal behaviours might be inhibited due to the translocation, Cooper (2003) found that lizards from that genus change behaviour due to severe changes in body condition (autotomy), they might do it too when translocated, and be less active when that happens, so detectability might be less. Cooper and Guilette (1991) found sexual dimorphic changes in their behaviour too. What sex where the individuals you translocated? We now acknowledge that STEL behavior could have been altered and we have added the Cooper (2003) citation as suggested by the reviewer. We also added a statement of observed behavior during the study that suggests that STEL behavior may not have altered. Also, for greater clarity, we have included a new table that addresses the sex ratios at each density for each species. Telemetry, particularly some pit tags, or other short-distance telemetry would be able to answer those kind of questions and let you know if the lizards where there but you couldn't detect them. We placed the STEL into the enclosure at known densities. We also addressed the timeframe of surveys so reproduction was not an issue, and the precautions that were used to reduce the likelihood of predation during the study. Therefore, densities of STEL were known. Comparing your results to trying to count them on the field, where they naturally live would be a great next step, maybe there the other methods might be more useful, as individuals would be in their natural habitat. We added statements concerning the habitat within our enclosure and STEL ‘natural’ habitat to clarify that the two are quite similar, so STEL placed within the enclosure was not completely foreign habitat. In addition, we did road cruising and walking transects for Tamaulipan STEL as the next step, which has been published, and we cite that work within this manuscript. Is it possible that the time needed for eDNA (and chemicals detected by dogs) to be available in sufficient amounts was too short in your study? We added statements concerning the eDNA and detector dogs that address climatic problems with longevity. The individuals translocated where left there? If so, doesn´t it places an ethical dilemma? Both species do not occur naturally in the same place. Could they reproduce between both of them? Couldn't the project take the 39 living ones back to their natural habitat? It might be important as at least the Tamaulipecan one is endangered. We added the reasoning for maintaining the STEL within the enclosure to the manuscript. In a nutshell, translocation was another component of the overall study. STEL were maintained to determine if translocation could be successful, do translocated STEL reproduce, survival after translocation, etc. (i.e., largest known population of Tamaulipan STEL occur on property that was recently purchased by Elon Musk for a lithium factory to make batteries for his Tesla cars. My fear is that the largest population of Tamaulipan STEL will not last if left on their own.) Aren't numbers of STELs found by both direct systematic search and cross road search too small for statistics to have enough power to bring solid conclusions? I would need to see the model structure, results, residuals and the data, at least a summary for me to be able to reach a conclusion. We have added a binomial GLM that has addressed the issue of small sample size. The analyses will be placed in a public repository, and if preferred, can be added as a supplement to this manuscript. I can assume those earless lizards are very sensitive to vibrations in the ground, so could ATVs be bothering or scaring them so they hide resulting in a lower detectability and observation rate, compared to a human walking over a dirt road? It is unknown if STEL react, positively or negatively, to ground vibration in terms of detectability. However, road cruising resulted in some of the best detectability so it does not appear that potential ground vibration caused lower detectability than other methods. We included a citation that compares road cruising vs. walking transects for Tamaulipan STEL to highlight this. The habitat you translocated them to was different from the one they lived in, so you had to take out the native vegetation and allow something somewhat alike their habitat to grow? Could that be accounted for to explain the low detection ratio? We added statements concerning the habitat within our enclosure and STEL ‘natural’ habitat to clarify that the two are quite similar, so STEL placed within the enclosure was not completely foreign habitat. More attractive and informative figures, including maps would be appreciated, together with STELs pictures, as this is an online only journal they wouldn't cost more, but could enrich the manuscript We’ve added additional tables and figures and photos of STEL as requested. Hopefully you find them attractive. I would be delighted to read a revised version of this manuscript Reviewer #2: The STEL were placed in a novel environment, which may represent the most vulnerable aspect of the experimental design. Any research involving these two species—or closely related ones—regarding animal personality in unfamiliar settings or other ethological factors should be taken into account. Such studies are essential for contextualizing and refining the interpretation of these results. Accordingly, this limitation should be acknowledged in the discussion and explicitly mentioned as a cautionary note in the abstract. We have acknowledged that STEL were translocated and how translocation may have altered their normal behavior, so caution should be exercised with interpretation. Attachments Attachment Submitted filename: Responses to Comments.docx https://doi.org/10.1371/journal.pone.0336129.r002
21 Oct 2025 Decision Letter - Edvard Mizsei, Editor Efficacy of various survey methods to detect an experimental population of spot-tailed earless lizards: A case study PONE-D-25-16961R1 Dear Dr. Henke, 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, Edvard Mizsei Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: Reviewer's Responses to Questions Comments to the Author Reviewer #1: All comments have been addressed Reviewer #2: All comments have been addressed ******** 2. Is the manuscript technically sound, and do the data support the conclusions??> Reviewer #1: Yes Reviewer #2: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? -->?> Reviewer #1: Yes Reviewer #2: Yes ****** 4. Have the authors made all data underlying the findings in their manuscript fully available??> The PLOS Data policy Reviewer #1: Yes Reviewer #2: Yes ****** 5. Is the manuscript presented in an intelligible fashion and written in standard English??> Reviewer #1: Yes Reviewer #2: Yes ****** Reviewer #1: All comments have been properly answered, thanks for your patience and politeness. I think this is a valuable contribution Reviewer #2: (No Response) ****** 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: Edgard David Mason Romo Reviewer #2: No ******** https://doi.org/10.1371/journal.pone.0336129.r003
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