PONE-D-25-05158-->-->Do chimpanzees (Pan troglodytes) mentally represent collaboration?: Action-learning and communication in a partnered task-->-->PLOS ONE?>

Dear Dr. McEwen,

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Miquel Llorente, PhD

Academic Editor

PLOS ONE

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This work was supported by the European Union’s Seventh Q20 Framework Programme (FP7/2007–2013)/European Research Council Grant 609819 (SOMICS)

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We thank Eloise Dallas for conducting the reliability coding for these data, and Kate Grounds for her role as research coordinator at Edinburgh Zoo. We also thank the workshop team in the University of St Andrews School of Psychology and Neuroscience for their support with apparatus construction. We are grateful to the Royal Zoological Society of Scotland (RZSS) and the University of St Andrews for core financial support to the Edinburgh Zoo’s Budongo Research Unit where this project was carried out. We are grateful to the RZSS keeping and veterinary staff for their care of animals and technical 37 support throughout this project. This work was supported by the European Union’s Seventh Q20 Framework Programme (FP7/2007–2013)/European Research Council Grant 609819 (SOMICS). Edinburgh Zoo’s Budongo Research Unit is core supported by the Royal Zoological Society of Scotland (Registered charity number: SC004064) through funding generated by its visitors, members and supporters, and by the University of St Andrews (Registered charity number: SC013532) who core supports the maintenance and management costs of the research facility

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Additional Editor Comments:

Dear authors,

Thank you for submitting your manuscript to PLOS ONE. I have now received and carefully considered the reviews from two independent reviewers. Based on their assessments, I am pleased to inform you that your manuscript is generally well-received and offers a valuable contribution to the study of co-representation and problem-solving in captive chimpanzees. However, before it can be accepted for publication, minor revisions are required.

Reviewer 2 raised concerns about the sample size, noting that while small sample sizes are common in primatology, the limited number of successful participants in your study makes it difficult to draw strong conclusions. The reviewer acknowledges the methodological soundness of your approach but encourages additional discussion on the limitations imposed by the sample size and the potential implications for the robustness of your findings. While further data collection would be ideal, it is not a mandatory requirement at this stage; instead, clarifying the limitations in the discussion would be beneficial.

Reviewer 1 provided more specific recommendations regarding the structure and clarity of the manuscript. They highlighted the importance of introducing the distinction between cross-species vs. within-species collaboration earlier in the paper, particularly in the introduction. While this point is well-addressed in the discussion, the reviewer believes that a more explicit rationale at the beginning would improve the manuscript’s coherence and provide clearer context for the study’s design and findings.

Additionally, Reviewer 2 noted some redundancies in the introduction and suggested streamlining certain sections to enhance clarity and conciseness. They also raised a methodological consideration regarding the object condition, questioning whether the mere presence of a human observer might have influenced chimpanzees’ perceptions of the task. Furthermore, they suggested discussing the possibility of local enhancement as an alternative explanation for the observed behavior in the partner condition.

To address these concerns, please provide the following revisions:

- Clarify the limitations imposed by the sample size in the discussion.

- Introduce the issue of cross-species collaboration earlier in the manuscript, providing a clearer rationale for the study’s design.

- Streamline the introduction to reduce repetition and enhance clarity.

- Discuss the potential influence of human presence in the object condition.

- Consider the role of local enhancement as an alternative explanation in the discussion.

In addition, please carefully review the specific line-by-line comments provided by Reviewer 1 and 2 to address clarifications and edits.

I believe these revisions will significantly strengthen your manuscript and improve its clarity and impact. Please submit your revised version along with a point-by-point response detailing how each comment has been addressed.

I look forward to receiving your revised manuscript.

Best regards,

Dr. Miquel Llorente

Academic Editor, PLOS ONE

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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: Partly

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

Reviewer #1: Yes

Reviewer #2: Yes

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3. Have the authors made all data underlying the findings in their manuscript fully available??>

The PLOS Data policy

Reviewer #1: Yes

Reviewer #2: Yes

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

Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #1: This study is a well-thought out and thoroughly executed assessment of mechanisms underlying collaboration in captive chimpanzees. Through a two-step task, either with help of a human partner or a subject, the authors consider whether chimpanzees form some mental representation of the actions of their partner, and if they can integrate this information in their own actions. Using a between-subjects design, the authors tested chimpanzees’ performance on the task as well as their attempts to communicate with the human experimenter. They found that individuals in both the object and partner condition could successfully reproduce the necessary action, however, individuals in the partner condition were more likely to replicate the actions of the experimenter, while individuals in the object condition were more likely to find an alternative solution. Communication mostly occurred when chimpanzees had exhausted the possible actions they could take. The article is well-written, and I especially commend the good use of figures and supplementary material which make it very easy to follow the experimental set-up.

I appreciate the rigor and detail that went into planning the methodology and set-up of this study and in its execution. My main qualm with the manuscript in its current form does not lie in the content, but in the order in which it is presented, and I have a few minor comments.

Cross-species vs within-species collaboration

The authors acknowledge this point in the discussion, which I thought was a very well-presented consideration of this limitation, but I really missed this information earlier in the manuscript. The study presented here considers whether chimpanzees are capable of co-representing the mental state of a human partner, not a conspecific. It is very well possible that the mechanisms that underlie collaboration and mental perspective-taking cross-species are not entirely the same ones that underlie collaboration within-species. I understand the limitations of performing such experiments that led to the use of a human partner, but I would appreciate more discussion of this fact already in the introduction of the paper.

Can it truly be assumed that the cognitive capacities are the same for cross-species and within-species? In the rationale of the introduction, the authors explain how collaboration between individuals is crucial to survival of group-living species. Is collaboration with other species just as crucial? Or is it expected that if this capacity exists within species, it translates to between species without any issues? I think the choice of the authors to take a chimpanzee-human collaboration as analogue to a chimpanzee-chimpanzee collaboration merits some background in the introduction already, and some justification why between-species collaboration could be used as a proxy for assessing collaboration capacity within-species.

In the discussion, the authors actually refer to studies (629-633) which support the idea that chimpanzees represent collaboration with a conspecific and a human partner differently. Chimpanzees are actually more likely to collaborate with human partners. To me, this is very relevant information that should be discussed in the rationale and set-up of the experiment. In my view, these studies, and the finding of this manuscript, could reflect that captive chimpanzees specifically have become used to seeing humans as a source of food. Conspecifics are not, so they are less motivated to collaborate with conspecifics, since, unlike with humans, they are not sure a food reward would follow. To me this further signals that there might be a different process at work in cross-species collaboration than within-species, which certainly merits more discussion at earlier places in the manuscript (though I do think this paragraph in the discussion was excellent and very informative!).

Repetition/Lengthiness

Overall, I found the introduction quite lengthy, and felt as if it was at points repetitive. Especially the notion that primates’ ability for shared representations is not well understood was repeated several times. For instance, the paragraph from 142-157 could be rewritten to be much clearer and more concise. Now the same information is repeated for collaborative experiments and stag-hunt, when the relevant information from these studies is very similar. Also, this is likely a copy-paste error, but the paragraph in lines 536-549 is repeated in lines 550-563.

Object vs partner

After reading the manuscript and watching the supplementary material, I wonder to what extent the chimpanzees truly experienced the object condition as being devoid of human intervention. I understand why the current set-up was chosen, and I think it is a clever set up. However, I am not entirely sure if the mere presence of the human observer does not lead to the chimpanzee assuming the human had some kind of role in the flipping of the see-saw, even if they don’t see the exact mechanism. After all, in a zoo setting, chimpanzees are well-acquainted with humans making things happen of which they do not fully understand the mechanism and the causality is not clear (e.g., a caretaker pressing a button to open a hatch far away), so in that sense, I would not be surprised if in both conditions the chimpanzee assumes the human did something to flip the see-saw.

The difference in performance between the object and partner condition, with chimpanzees being more likely to copy the experimenter’s action in the partner condition, could possibly also be attributed to local enhancement. The chimpanzees observe the human experimenter touching the side of the see-saw, and as a result, are more likely to interact with this specific location themselves, resulting in the flip. This alternative would be less cognitively complex than chimpanzees representing their human partner’s mental state, and I think it warrants some mention in the discussion section.

Specific comments line by line

15: So here I would add “cross-species” in front of co-representation, to be very clear.

79: Is the partner in the Joint Simon studies presented here a conspecific or a heterospecific?

225: In what context was the female experimenter familiar? This warrants some more information. Did the subjects have experience with the experimenter providing food? Or was she a neutral observer to them? If food was given in the past, had all chimpanzees experienced this?

271-274: This section was vague to me, and I do think it is important information being shared here that now does not come across. If I understood correctly, trials in the blocked condition did continue if a conspecific of the same experimental condition was present, right? I would re-word this to be a) entirely clear in which situations trials continued with others present b) include justification why you made the decision to continue or interrupt some trials with an audience but others not, and c) in the results, I’d expect to see some information in how many trials conspecifics were present in the trial types where you did allow this. I think you probably have good reasons for deciding on this protocol, but as a reader it is not clear on what grounds these decisions were made, when I think this is relevant information.

446: how many subjects never succeeded?

516: There’s a punctuation mark too many behind “see-saw”.

609-628: I thought this was a very interesting discussion and good interpretation of the authors’ findings!

651: I think it is fascinating that we find this difference, to me it indicates that chimpanzees might be very intelligent in the sense that they are aware of when their efforts would be wasted vs when they are likely to get a food reward. It’s another reason why I think it is important to expand on the previous experience the chimpanzees in this study had with the experimenter specifically, since if they already associated her with food rewards they might be more inclined to cooperate/communicate.

Reviewer #2: The manuscript describes a study investigating the possibility for co-representation in captive chimpanzees collaborating with a human partner or an automatic mechanism in a simple food acquisition task. The manuscript is generally well-written and describes a novel approach to the problem of identifying co-representation in this context. As a minor concern, the style of writing could be simplified to make the content more accessible to a broader audience. This is an important consideration given the scope of the journal. Specific corrections are provided in the feedback.

The methodology appears to be sound and seemingly addresses the question that is being posed. The only major issue evident in this study is the limited sample size, complicated by the fact that only six of the ten individuals successfully completed the task. The small sample makes it difficult to discern what the responses of the animals mean but also whether the test itself is as appropriate in addressing the question posed as it seems. It also complicates the interpretation of potential causal factors in addition to those already mentioned which may have driven the responses of the subjects (e.g. differences in cognitive ability, age/sex differences). To their credit, the authors do identify the sample size as a problem in the study but, as a reviewer, it is difficult to look past this limitation in order to determine the scientific implications of the findings. I would urge the authors to increase their sample size in order to improve the confidence that the reader can place in the outcomes and improve the scientific impact that the study could have.

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Reviewer #1: Yes:  Zoë Goldsborough

Reviewer #2: No

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Do chimpanzees (Pan troglodytes) mentally represent collaboration?: Action-learning and communication in a partnered task

PONE-D-25-05158R1

Dear Dr. McEwen,

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.

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Kind regards,

Miquel Llorente, PhD

Academic Editor

PLOS ONE

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

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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

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4. Have the authors made all data underlying the findings in their manuscript fully available??>

The PLOS Data policy

Reviewer #1: Yes

Reviewer #2: (No Response)

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

Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #1: (No Response)

Reviewer #2: (No Response)

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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:  Zoë Goldsborough

Reviewer #2: No

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