Peer Review History
Original SubmissionSeptember 12, 2019 |
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PONE-D-19-25653 Exploring individual variation in associative learning abilities through an operant conditioning task in wild baboons PLOS ONE Dear Dr. Carter, 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. Unfortunately, Reviewer 1 was no longer available, and a new reviewer was invited. Both reviewers found that your study is valuable and that performing cognitive studies in the wild is extremely challenging, and I share their view. However, whereas Reviewer 1 (previously Reviewer 2) was quite happy with your revision, the current Reviewer 2 asked for further work on the paper, before it can be considered acceptable. Please address the comments provided by both reviewers, along with my suggestions, listed below. We would appreciate receiving your revised manuscript by Jan 09 2020 11:59PM. When you are 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. If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. To enhance the reproducibility of your results, we recommend that if applicable 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. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols Please include the following items when submitting your revised 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. We look forward to receiving your revised manuscript. Kind regards, Elsa Addessi Academic Editor PLOS ONE Journal Requirements: When submitting your revision, we need you to address these additional requirements. 1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at http://www.journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and http://www.journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf 2. We note that you have stated that you will provide repository information for your data at acceptance. Should your manuscript be accepted for publication, we will hold it until you provide the relevant accession numbers or DOIs necessary to access your data. If you wish to make changes to your Data Availability statement, please describe these changes in your cover letter and we will update your Data Availability statement to reflect the information you provide. 3. Please include a copy of Table 2 which you refer to in your text on page 23. Additional Editor Comments (if provided): ll 39-40: please modify as follows: “current environmental challenges associated with conducting cognitive tests of animals in the wild” Ll 494-495 “We also found that troop membership determined the likelihood of eating a higher proportion of correct kernels across trials.”: couldn’t it be done to color preference? Did you test color preference before administering the differently flavored kernels? Although I appreciated the answers you provided in reply to the comments of the previous reviewers on this issue, this aspect should be accounted for in the Discussion. L 529 “and the interaction that was contrary to prediction in trial 2”: please remind the reader what is the interaction you are mentioning here L 533: “that” repeated twice (typo) [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: Yes ********** 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: General comments This study aimed to assess associative learning performance of individuals in two groups of wild baboons. The manuscript represents a significant amount of work and while it is unfortunate that the authors were not able to detect learning, I believe the trial was thoughtfully conducted. There remains a paucity of studies investigating cognition in wild populations (it is challenging!) and studies such as the current one are useful building blocks for future attempts. The authors have done a nice of addressing the concerns/ suggestions raised in the previous two reviews, as such I only have minor comments. Minor comments: 1. L51 – As there are only a small number of studies that have looked at the fitness consequences of associative learning (adaptive value) in natural environments, it would be good to cite them all here. Also, as the authors correctly point out, differences in learning are likely to reflect adaptions. The only study currently cited reports a positive correlation between learning performance and fitness correlates, but two other studies report negative relationships: Ashton B.J., Ridley A.R., Edwards E.K., Thornton A. 2018 Cognitive performance is linked to group size and affects fitness in Australian magpies. Nature 554 (7692), 364-367 (doi:10.1038/nature25503). Madden JR, Langley EJG, Whiteside MA, Beardsworth CE, van Horik JO (2018) The quick are the dead: pheasants that are slow to reverse a learned association survive for longer in the wild. Philosophical Transactions of the Royal Society B: Biological Sciences 373 Evans LJ, Smith KE, Raine NE (2017) Fast learning in free-foraging bumble bees is negatively correlated with lifetime resource collection. Scientific Reports 7:496 2. L52 – This sentence should be modified to improve clarity. I suggest inserting ‘while ultimately differences in…’ removing also from ‘individuals within a species also differ…’ and including ‘genotype or epigentic changes due to the developmental trajectory environment experienced during their lifetime. 3. L85 – Incorrect references inserted, should be references ‘3’ (bumble bees) and ‘4’ (humingbirds). It doesn’t seem as though reference ‘5’ has been used at all – so it would pay to double check all references align as intended. 4. L86 – Rather than including a second reference for bumble bees can you reference a study that has looked at associative colour learning in foraging mammals? Or a least a different taxon e.g. butterflies, jumping spiders. 5. Discussion – it would be good to briefly comment on baboon cognition generally. What would you expect to see in terms of their associative learning performance, based on their performance in other cognition assays, conducted either with captive or wild individuals? 6. L552 - It would be good to reinforce that studying cognition in wild populations is generally very challenging by citing the below studies: Huebner F, Fichtel C, Kappeler PM (2018) Linking cognition with fitness in a wild primate: fitness correlates of problem-solving performance and spatial learning ability. Philosophical Transactions of the Royal Society B: Biological Sciences 373 Morand-Ferron J., Cole E.F., Quinn J.L. 2016 Studying the evolutionary ecology of cognition in the wild: a review of practical and conceptual challenges. Biological Reviews 91(2), 367-389. (doi:10.1111/brv.12174). Reviewer #2: Note: I have not reviewed the original version of this manuscript submitted to PLOS ONE. This is an interesting study on individual differences in wild baboons’ abilities to learn a two-choice color/food discrimination. I applaud the authors for their careful efforts to conduct individual cognitive tests with wild, group-living animals. Although it is not clear what the baboons had learned, the finding that even seemingly simple behavior is strongly influenced or constrained by animals’ natural environment is important. Indeed, such factors should be more frequently considered in studies of captive animals as well. However, I have some concerns and suggestions about how to effectively present and analyze the data. INTRODUCTION This section provides a nice exposition but the motivation for the study is not obvious to the reader. Yes, we know little about this topic in the wild, but you could make clearer why people should want to study learning (and between- and within-species variability) in the first place. There is a gap, but why do we want to fill it? What we can learn from this more broadly? Lines 69-72: I’d add that, on the other hand, captive animals may also “fail” on problems they’d never encounter in the wild, which can distort our estimate of that species’ cognitive abilities in the other direction. Lines 111-113: Couldn’t you argue the opposite, that males would need to learn faster because they encounter new environments? But in general, how stable are these baboons’ environments outside of seasonal variability? Even if they disperse and go to a neighboring group, aren’t they still living in the same general habitat with the same food sources? Line 122: “because of their greater experience” I don’t fully follow this point. Greater experience with what? With that particular food item, with learning associations, something else ..? Lines 134-135: How can they be independent and considered opposites? Line 140-141: Why? If the idea is that neophilic individuals spend more time with the task (or would perhaps be less vigilant?) and therefore are more likely to learn, I suggest adding this explicitly – and then since you have the data, you should also test it statistically. Line 142: Please add a brief definition for vigilance. METHODS The authors collected a substantive data set including food choice in the learning task and individual differences in sex, rank, neophilia, age, and vigilance in prior trials. However, several reasons make it difficult to fully appreciate this data set. There are no indicators of reliability (except for a previous repeatability estimate for neophilia, which seems low to rely on a single measurement here). Line 221: When trials were interrupted, did that always end the trials? If so, please state. In lines 312-313, you say that a trial “was considered finished” when all kernels of one pile were eaten. 1) This information needs to be much earlier (move it into the Experimental Procedure section). 2) Did the experimenter remove the other pile at this point? Or was it just considered finished for data recording, but the baboon could still eat the other pile? Line 243: “(2) the colour of the first ten kernels consumed” – should this really be 10? not “all”? Lines 265-267: I’d add that this means all cases where they didn’t eat one pile in its entirety (20 kernels) first. It’s implied from having 20 kernels in each pile and you say this later in the manuscript, but it would be helpful for the reader here too. Table 1: The sums by row sum to trial 1-5: 34, 37, 38, 38, 32. Why can the number of individuals for trial 1 be lower than subsequent trials? And if the grand total here is 179 and interruptions were 22, does that not contradict the descriptives in lines 400-401 and 531? Table 1: But what is the proportion when they switched within the first 20 trials? E.g., 19 vs. 1 would still essentially be bulk feeding. The cutoff could be arbitrary, of course, but the distribution seems important because you use this criterion to subset your data. The number of observations is extremely variable, in part due to the natural distribution of traits in this population, in part due to practical constraints during data collection, and in part due to subsetting for statistical analyses. This is not a problem per se but could be presented in a more organized fashion. The eventual reader could consult the full data set, but making it available for review as well would be extremely helpful in evaluating the analytical approach. Line 284: You tested for multicollinearity but please add something like a correlation matrix or crosstabs to indicate which of these factors covaried. That’s interesting in its own right but also important to assess your models. Appendix S3: How/why were these divided into low, medium, and high? Aren’t these both continuous variables? --Models-- The analytical approach is confusing. Couldn’t you combine Models T1, T2, …, and T5 into a single model and add trial number as a fixed effect and with interactions, like in Model T2-5? If they only learned in trial 1 and then only chose palatable trials, you’d see an interaction between trial and kernel number. If they relearned the association every time (at the same rate), you wouldn’t expect an interaction. I also still don’t understand why you couldn’t use the full data set here too? Including the current proportion of palatable/unpalatable kernels as a fixed effect seems odd because it’s itself dependent on prior choices, which are the measure of interest. I understand the motivation to account for this change in proportion, but this seems statistically unsound. --Simulations-- I like this approach a lot (running simulations of the proposed processes to see what the data should look like), but this needs some work. 1. Why not also do this for between-trial learning? 2. Please provide more detail about how the simulations work. E.g., how many runs per scenario? What were the probabilities? Scenario 1: What kernel number is meant by “then” (line 362)? Scenario 2: What precisely is meant by “intermittently” (line 365) and how was it determined whether 1, 2, or 3 kernels were sampled? 3. Does “baseline probability” mean the ratio of remaining palatable/(palatable + unpalatable)? If so, “baseline” may not be the best word because it suggests the initial probability (i.e., 50%) and could therefore cause confusion. 4. Importantly, if you simulate these processes for 38 baboons, and run the same analyses that you run on the actual data (minus individual variability), can you extract these patterns? It’s not clear whether that is how you derived Table 2 (if so, state so explicitly and add the actual parameter estimates). Given the multicollinearity concerns and criticisms of stepwise regressions, I agree with the previous Reviewer that a model selection/information theoretic approach might be more appropriate (Burnham & Anderson, 1998). It also lets you avoid overfitting, but in an arguably more principled manner (specifically, by including a penalty term for each added parameter). RESULTS Some descriptives (medians, ranges) for neophilia, vigilance, time spent on the task would be nice. Lines 405-406: How many kernels did they leave uneaten in subsequent trials? Table 3: This might change depending on changes to your analytical approach, but it’s hard to extract what probabilities/odds ratios for kernel choice these models actually predict. This would be much aided by a plot with the model fit overlaid (see also below). FIGURES The current figures do not convey a lot of information and only in aggregated form. And the arguably most useful figure (S4) to get a quick sense of the baboons’ behavior in the learning task is hidden in the supplemental material. The figures could be used to much greater effect to include e.g. a line + uncertainty band to indicate model fit, the number of observations (e.g., as labels or proportional to point size) or individual points/trajectories (e.g., in semi-transparent, small points or thin lines) having Fig. S4 in the same format as Fig. 2 (simulations) would also really help comparison to the different learning processes. Fig. 2 should have the same x- and y-axis scales throughout, to aid comparison (i.e., kernel size always from 1-5 to 36-40, baseline probability always from 0 to 1, proportion palatable always from 0 to 1). Fig. 4 should have ranges as the labels (i.e., 1-10 instead of “10” etc.), also make the y go from 0 to 1 Fig. 4 how were low and medium determined? Also, isn’t this a continuous variable? If the categorization was just for visualization purposes, please state so in the caption. DISCUSSION Assuming that the general finding holds (no evidence of learning as measured by [exclusive] preference of palatable kernels, let alone individual differences), this seems fine. I appreciate the discussion of how things can go awry in the field. Two minor points to perhaps discuss in more depth: The novel food wasn’t really novel, as the baboons had all eaten corn before. Just the color and bitter taste were new. To what extent do you think their previous experience/learning explains why they didn’t learn (more) here? If they already knew that it was nutritious and not poisonous, they may well have learned that one tasted bitter, but that might have simply not been enough to outweigh a free meal (especially when food is scarce, as you mention). Is there any other evidence in the literature that individual differences play less of a role during times of food scarcity because everybody is similarly limited in what they can do? If so, that may be worth including. TYPOS, WORDING SUGGESTIONS, & REFERENCES: The use of “incorrect/correct” kernels sounds a bit awkward and seems unnecessary. I suggest simply using “unpalatable/palatable” throughout the manuscript. Please carefully check your references. Some refs listed in the list are not listed in the text (e.g., [5, 36, 63, 64]) and refs [58] and [59] are identical. Line 35: should be “individuals’ phenotypes” (with an s) Line 47: should be “aspects such as foraging behavior” (add “as”) Lines 90, 93, 95: I’d recommend italics instead of all-caps to emphasize the either/or’s Line 110: better “female baboons would” (instead of “will”) Line 203: should be “prior experience with corn kernels” (instead of “of”) Line 388: should be Table 2 (instead of 1) ********** 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: No 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 to be viewed.] 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 us at figures@plos.org. Please note that Supporting Information files do not need this step. |
Revision 1 |
PONE-D-19-25653R1 Exploring individual variation in associative learning abilities through an operant conditioning task in wild baboons PLOS ONE Dear Dr. Carter, 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. I require to address the following very minor points before the manuscript can be accepted: - L 40: two full stops (typo) - L72-73: the sentence is a bit unclear, I suggest to modify it as follows: “Conversely, the failure of captive animals to solve tasks that they would never encounter in the wild may equally distort our estimate of that species’ cognitive abilities”. - L 83: two square brackets (typo) - L 135: I suggest to delete the word “personality” here, since personality is a complex construct; similarly, on l 480 I suggest to replace “personality” with “neophilia” - L 323: the parenthesis at the end of the sentence is missing - L 422, 540 please replace the semicolon with a comma - L 544 (and 561) since “tendency” has a very precise meaning in statistics (0.05 < p < 0.1), unless this is the case, I suggest to replace this word with an alternative one - L 551 please erase the comma after “study” We would appreciate receiving your revised manuscript by Apr 18 2020 11:59PM. When you are 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. If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. To enhance the reproducibility of your results, we recommend that if applicable 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. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols Please include the following items when submitting your revised 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. We look forward to receiving your revised manuscript. Kind regards, Elsa Addessi Academic Editor PLOS ONE [Note: HTML markup is below. Please do not edit.] 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: All comments have been addressed ********** 2. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #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 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 ********** 5. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes Reviewer #2: Yes ********** 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: All minor corrections requested have been suitably addressed by authors. I look forward to seeing this work published. Reviewer #2: This paper details a study on individual differences in wild baboons’ abilities to learn a two-choice color/food discrimination. It nicely highlights that even well-designed and seemingly simple tests of animal behavior and cognition can be heavily affected by environmental conditions. I thank the authors for their clarifications in the manuscript and thoughtful responses to the comments/suggestions raised in the review process. ********** 7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: No 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 to be viewed.] 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 us at figures@plos.org. Please note that Supporting Information files do not need this step. |
Revision 2 |
Exploring individual variation in associative learning abilities through an operant conditioning task in wild baboons PONE-D-19-25653R2 Dear Dr. Carter, We are pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it complies with all outstanding technical requirements. Within one week, you will receive an e-mail containing information on the amendments required prior to publication. When all required modifications have been addressed, you will receive a formal acceptance letter and your manuscript will proceed to our production department and be scheduled for publication. Shortly after the formal acceptance letter is sent, an invoice for payment will follow. To ensure an efficient production and billing process, please log into Editorial Manager at https://www.editorialmanager.com/pone/, click the "Update My Information" link at the top of the page, and update your user information. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org. If your institution or institutions have a press office, please notify them about your upcoming paper to enable them to help maximize its impact. If they will be preparing press materials for this manuscript, you must inform our press team as soon as possible and 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. With kind regards, Elsa Addessi Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: |
Formally Accepted |
PONE-D-19-25653R2 Exploring individual variation in associative learning abilities through an operant conditioning task in wild baboons Dear Dr. Carter: I am pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department. If your institution or institutions have a press office, please notify them about your upcoming paper at this point, to enable them to help maximize its impact. If they will be preparing press materials for this manuscript, 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. For any other questions or concerns, please email plosone@plos.org. Thank you for submitting your work to PLOS ONE. With kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. Elsa Addessi Academic Editor PLOS ONE |
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