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I confirm that the authors have addressed all of the reviewers' comments. I am happy with the current version.
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We have now received and reviewed the reports from three expert reviewers. Based on their feedback and our editorial assessment, we are pleased to inform you that your manuscript is potentially acceptable for publication pending minor revisions.
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The article is a work on the possibility of adapting and using the ChimpFACS tool on bonobos. The study is well-written and understandable, the structure is easy to follow and the arguments are solid. Every AU is thoroughly examined, clearly presenting not only the criteria for its identification but also discussing the morphological differences between chimpanzees and bonobos and the AUs that can possibly lead to false identifications. Images and videos are also extremely valuable additions.
Overall, I recommend this work for publication, although there are some aspects that could enhance the readability and the theoretical solidity of the study if revised. Apart from the specific suggestions provided below, the only broad point that I would raise here regards the overall justification for the need for a ChimpFACS bonobo extension. Its potential uses would certainly allow wider reliable cross-comparisons among ape species. However, some of the motivations presented to support the necessity of this extension (instead of using the first version of ChimpFACS) are less clear.
The authors did a great job at explaining all the differences between bonobos and chimpanzees (especially from a morphological point of view) but when it comes to discussing the opportunity of using a FACS protocol for other species, there are other cases that should have been included. More specifically, OrangFACS seems to be used without too many concerns about its applicability/validity across the three orangutan species, and the same can be said for the two gorilla species with GorillaFACS and for the gibbons with GibbonFACS.
It is true that, among the great apes, bonobos and chimpanzees are arguably more different than the three Pongo and the two Gorilla species, but many of these differences are ecological and behavioural, not anatomical. Therefore, given the muscle basis of FACS tools, it is not very clear why the Pan genus should be treated differently than the other great apes (see also lines 275-279). I believe that the inclusion of the other great ape species and their FACS tools in the discussion of the background of this study, would make the work more robust and strengthen some of its argument.
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I would avoid the use of the expression “gold standard” when referring to FACS and human facial behaviour. Although it is certainly true that FACS allows a level of depth that other tools don’t allow, it is also true that it is possible to conduct valuable and reliable research on the topic even without using FACS.
INTRODUCTION
59 it can be used for “non-brief” human facial movements too
104 the study from Waller and colleagues (2015) however, does a great job at warning the reader that their result cannot be taken as proof of the intentional use of facial expression in orangutans
102-110 if the aim of this part is to show that FACS has been useful in understanding the complexity of communication and emotion in NHP, it would be good to include some studies on chimpanzees too (e.g.: Davila-Ross et al., 2015, Crepaldi et al., 2024)
113 citation needed
146 are there any other bonobo studies that could be included here
165-167 I would suggest inserting (either here or in some other part of the study) how many core AUs have been found in humans, chimpanzees and bonobos for a more direct comparison. The information can be extrapolated from Tables S1 and S2, but it might be useful to readily find also within the text if/how many AUs have been observed only in some of the Homini species
196 citation needed
202-203 debatable/possibly incorrect. Bonobos are perhaps the least studied ape only if we cluster together the two gorillas and the three orangutan species. If the comparison is made between all the 7 extant non-human great apes, bonobos are hardly emerging as the least studies, and even less with regard to their social communication when compared to all the existing NHP
204-206 the number of individuals in the wild seems irrelevant to the aim of the study (plus, common chimpanzees are also classified as endangered, while all the orangutan and gorilla species are critically endangered, so bonobos do not stand out among the other great apes with this regard)
208 consider replacing the term “taxon” with “order”
210 citation needed
278 consider moving the brackets to line 275 after “recent”
304 double-check if bonobos and chimpanzees differ also on the degree of lip eversion
308-310 such as? More details would be good about these features (also remove the double point after “AUs”)
311 maybe “neotenic” would be a more appropriate term than “juvenile”
315-320 are these differences relevant to the use of FACS? If not, perhaps consider dedicating less time to these characteristics and this descriptive section in general
328 the study by Clark et al. 2020 is not about chimps or bonobos and does not mention white scleras
334-335 for example?
353 I did not understand what the “Mean” and “SD” within brackets are referring to
381 remove the capital letter from “Bonobos”
386-393 the high number of brackets makes it a bit difficult to follow, consider reducing them
439 see comments on lines 165-167
574 use bold for the image numbers
650 what does the acronym IOT stand for? Please explicit it
689 is AU6 always observed in both eyelids even when it is only weakly activated?
705 wrong name of the action unit
730 change “lip corner puller” to “Lip Corner Puller” (the AU’s names have been written with capital initials throughout the paper)
758 “the lower lip protrudes” could possibly generate confusion as this morphological change is more typical of AD160
762 given the examples in the figures, good to mention that this AU can also occur asymmetrically (and the same goes for other AUs that can be produced on one side only of the face, as it has been done in lines 846–848 for example)
769 and in gorillas (Carrera-Caeiro et al., 2024)
814–821 what about in gorillas? If a comparison with other ape species for which we have a FACS tool is needed, it is recommended to include here all of them
857–866 perhaps it would be important to highlight the differences between AU18 and AU22 too, as these two AUs can also be confused, especially when they occur in only one of the lips (as shown in some of the images)
921 maybe good to try to provide less vague criteria than “small” and “large” to distinguish AU26 from AU27
933 Vick et al. 2007 actually reads “Although not described in detail here, we have also identified AU24 Lip Press and AU28 Lip Suck”
978 the expression “last of the apes” could be debatable, see comments on lines 202-203
982 “more expressive” could sound quite vague, consider providing more context
983 as pointed out before, the study by Waller et al. 2015 is actually explicitly warning the reader about taking their results as an indication of intentionality in orangutans. This misreading is a bit surprising given that two of the authors of the current study were also involved in the Waller publication
986 good to at least mention here a couple of studies that investigated the ontogenetic development of facial expressions in apes
991 AU6 seems actually to be included in ChimpFACS (Vick et al. 2007: see Table 2 and the dedicated paragraph on the following page). It has also been identified in studies that used ChimpFACS as a coding tool (e.g. Parr et al. 2007; Davila-Ross et al. 2015; Crepaldi et al. 2024)
999 remove the symbol (a little square) after the dot
1006 AU6: see the previous comment about line 991. Also, lines 610-611 and 620-621 of the current study seem to contradict this claim
1037 are bonobos really “more expressive”? Please provide some supportive literature
1051-1052 good to clarify what the expression “more expressive” means; also remove one of the two “seem”
1053-1055 although there seems to be partially contrasting data from bonobos in captivity
1073-1074 human FACS actually allows the coding for intensity too, and a similar approach has been used also in studies using MaqFACS (Clark et al., 2020, 2022)
FIGURES AND TABLES
S13 does not seem to fit as well as S11 and S12 when discussing AU1+2
Table S1 is a very useful tool for other researchers. The table nicely sums up the presence/detection of the AUs in chimpanzees, bonobos and our species. However, from the point of view of a researcher, it might be more useful to know which AUs have been detected since the manuals were made available rather than what they included in the first place. This is particularly relevant for chimpanzees. I would suggest a similar table, but including also the AUs that have been detected by other researchers using ChimpFACS (e.g.: Parr et al. 2007; Davila-Ross et al. 2015; Crepaldi et al. 2024) and not just the ones present in the original manual. Something similar has been done for example by Bard et al. 2011 in Table 8.1.
MANUSCRIPT FEEDBACK:
General comment: Explain why you are using the term facial “expressions” instead of facial “signals” or some other equivalent throughout the manuscript. The authors have previously indicated uncertainty about whether facial muscle movement always reflects underlying emotional experiences. Wouldn’t a more neutral term, like signals, configurations, etc., be appropriate?
Line 66: The FACS also contains information on how to code asymmetrical movements, head/eye positions, etc. Might be good to mention here!
Line 88: I would just state “Using AnimalFACS” to avoid confusion.
Line 98: I would replace the word "tools" here, as it suggests that these systems automatically code video footage. However, it is more similar to a training course and a coding procedure for humans.
Line 192: I would add “do” between “why” and “bonobos”.
Line 197-199: Could you elaborate more on the relationship between IOR and establishing a new FACS? From my understanding, IOR for FACS (using Wexler’s Ratio) is used to assess agreement between two researchers coding the same video footage. But here, you are implying that it might be used to assess similarities/differences between species?
FEEDBACK ON THE ELECTRONIC SUPPLEMENT:
I've been pondering a question related to the AnimalFACS manuals. Is it possible to add arrows to indicate the movements being discussed in each section? Additionally, since other facial muscle movements may be present, could captions be generated for each image or video to indicate the presence or absence of these movements? A good reference for this is in S28.
MANUSCRIPT FEEDBACK:
Lines 309-310: Could you clarify the relationship between landmarks and AUs? Also, please check this paragraph for grammatical errors, as it was sometimes confusing to read.
Line 353: Can you please clarify whether the mean and standard deviation are associated with the duration of the video clips?
Lines 360-362: Do you have an approximate breakdown of the video footage for each category, even if it’s rough? Previous studies have shown that certain AUs are specific to certain signals and their associated contexts.
MANUSCRIPT FEEDBACK:
Lines 207-216: You could mention that comparative FACS studies with chimpanzees can be used to assess predictions related to socio-ecological variables. Demonstrate what kinds of studies/questions could be addressed. I would then rework lines 217-222 so the information is clear and concise.
Line 407: It seems to me, though, that this extension could be a useful opportunity to discuss other facial muscle movements that were left out of the original chimpFACS manual but are possible. For instance, there is only one mention of AU25 in the chimpFACS 2006 manual, and no mention of AU26 or AU27, although previous studies have found that all three are present in chimpanzees. Perhaps you could mention these discrepancies in their respective sections (lines 903-926) as well?
Lines 1008-1011 & 1025-1028: The human Facial Action Coding System (FACS) has codes that indicate visibility conditions. Since chimpanzees may produce these movements, it may be beneficial to include these codes in all FACS manuals moving forward. This is especially relevant as video footage quality continues to improve. The codes could remain the same as those used in human FACS.
It is both an honor and a privilege to review this manuscript. As a long-time user of AnimalFACS, I am particularly excited that bonobos—the last ape without FACS—will now be included. These FACS are crucial for addressing various unresolved research questions in the future. Similar to other FACS publications and associated manuals, the bonobo FACS outlined here is robust. I acknowledge the substantial time and effort you invested in creating this FAC System, as evidenced by the meticulous detail in this manuscript. However, I have a few revisions that would help clarify information and address some crucial coding questions.
Overall, I thought the paper was very clear and well written, and the necessity of developing a FACS (extension) that can be used with bonobos was justified with convincing background and argumentation. The AUs were clearly and thoroughly described and I particularly liked that the authors included which factors may lead to a wrongful identification of an AU, such as in lines 598-600. The accompanying supplemental materials are very pertinent for this and all other cases. My comments are mostly minor suggestions.
Lines 116-117 “This complexity of…” this sentence felt confusing and unclear to someone not very familiar with FACS, it could stand to be broken down and explained a bit better.
Line 192 Very minor but the title is a statement mixed with a question mark. I would either phrase the title as a question “Why do bonobos need a FACS?” or take out the question mark.
Line 202 “in specific” reads strangely
Line 310 contains double comma
Lines 359-360 Analyzed 43h of captive bonobos and 12h hours of wild bonobos. Would be good to address whether there is a possibility of difference in facial expression between these two types of groups, particularly if many of the captive bonobos were hand-reared.
Line 689 delete first “only”
Why are all figures and tables in the supplements? It’d be nice to have some key ones in the main manuscript.
n/a
good
see above
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