A deepening understanding of animal culture suggests lessons for conservation

A key goal of conservation is to protect biodiversity by supporting the long-term persistence of viable, natural populations of wild species. Conservation practice has long been guided by genetic, ecological and demographic indicators of risk. Emerging evidence of animal culture across diverse taxa and its role as a driver of evolutionary diversification, population structure and demographic processes may be essential for augmenting these conventional conservation approaches and decision-making. Animal culture was the focus of a ground-breaking resolution under the Convention on the Conservation of Migratory Species of Wild Animals (CMS), an international treaty operating under the UN Environment Programme. Here, we synthesize existing evidence to demonstrate how social learning and animal culture interact with processes important to conservation management. Specifically, we explore how social learning might influence population viability and be an important resource in response to anthropogenic change, and provide examples of how it can result in phenotypically distinct units with different, socially learnt behavioural strategies. While identifying culture and social learning can be challenging, indirect identification and parsimonious inferences may be informative. Finally, we identify relevant methodologies and provide a framework for viewing behavioural data through a cultural lens which might provide new insights for conservation management.

Ln 181-190: This paragraph is important and could be strengthened using an example (or two) from the literature to help non-experts solidly understand the potential consequences of applying the ethnographic approach. If an example of the potential 'pitfalls' of this approach are absent in the literature, offering a hypothetical example would be helpful. : This is an important discussion that, to my understanding, is not well resolved in the literature. Using neutral genetic markers (i.e., those not under selection) to demonstrate correlation or clustering of behavioral variants among related individuals does indeed suggest inheritance of said behavior. Nevertheless, whether such inheritance of behavior has a genetic or socially learned basis cannot be determined via a correlational approach because genes that exert control of behavior may tag along with neutral genetic markers. Thus, correlation alone does not allow researchers to disentangle a genetic versus a socially learned basis of behavior (Laland and Janik 2006). Despite substantial effort, our ability to identify genes that control specific aspects of behavior are extremely limited (e.g., and with regards to migration, see Franchini et al. 2017 and references within), meaning determining the mode of inheritance usually requires an experiment. To deal with this issue, previous authors suggest transplant experiments as a viable approach for teasing apart genetic versus learned aspects of behavior (e.g., Laland and Janik 2006). As currently written, it seems the authors are suggesting that any evidence of inheritance of behavior can be viewed as evidence of social learning. For this reason, I suggest adding further discussion regarding the unresolved and complex associations between genotypic data and behavior. adaptation to various aspects of global change.
Figure 2: In the case of bighorn sheep in North America, the mitigation strategy suggested by the authors is not viable. In Jesmer et al. 2018, bighorn sheep and moose were translocated into areas of their historic range where the species was previously extirpated. So, there were no knowledgeable individuals to translocate because no individuals had experience on those landscapes. I do not see a way to introduce/translocate knowledgeable individuals in reintroduction efforts. One potential mitigation strategy would be to perform some sort of 'assisted migration' (not in the way the term is typically used) where humans harness emulation or local enhancement to 'seed' knowledge in a subset of individuals (perhaps by training captive reared individuals in the natural setting a la Mueller et al. 2013, Science) about where and when to migrate, then see/hope if that information diffuses through a population.
Although space is always limited in print journals, and authors often feel forced to shift as much information as possible to supplemental materials (myself included), I strongly suggest a 7th column of references be added here. The information in the supplement will relatively rarely be read and authors of these works will not get appropriate accreditation. Given most of the studies used in this table are cited in the main text, I do not think it will add too many citations to the author's reference section to add a references column. ). These acronyms are not used over and over throughout the manuscript, so spelling them out will not cost much space but will certainly make the manuscript easier to read for non-experts. Also, with regards to using acronyms in figure 3, non-expert readers will have to search through the main text or supplemental materials to decipher the acronyms and interpret the figure.
Also, a more minor point regarding figure 3 is that bighorn lambs do not have full-curl horns. Suggest finding a silhouette with no or very small horns or using image editing software to delete the horns on the current silhouette.
Minor comments: Ln 163: What are "precautionary principles"? If this is jargon, I suggest defining. If the authors are referring to discussion preceding this paragraph, it remains unclear as to what these principles are.
Ln 175-179: This is an important message that I think will be appreciated by those interested in studying animal culture in wild populations where such 'gold standards' are impractical or impossible to implement. Thank you.
Ln 209: Suggest describing what is meant by "viewing culture in isolation" or reword. Unclear what is meant here.
Ln 219: Two complete sentences combined with a comma (i.e., run on sentence).
Ln 389: Typo. Should read "may not yet be" Ln 389-393: Reads awkwardly, suggest moving "thus providing a fertile area for on-going research" to the end of the sentence.
Ln 438-441: Suggest moving this sentence to after the sentence on the use of genetic pedigrees. Otherwise, the sentence on biologging interrupts the logical linkage between the first and third sentences about the use of genotypic data.
Decision letter (RSPB-2020(RSPB- -2718.R0) 21-Dec-2020 Dear Dr Brakes: Your manuscript has now been peer reviewed and their comments (not including confidential comments to the Editor) are included at the end of this email for your reference. As you will see, the reviewers have raised a fair number of concerns with your manuscript but, overall, they were both positive about the goals and overall pitch of the review. So, I would like to invite you to revise your manuscript to address their concerns.
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Please submit a copy of your revised paper, idealy within three weeks. If we do not hear from you within this time your manuscript will be rejected. If you are unable to meet this deadline please let us know as soon as possible, as we may be able to grant a short extension. We do understand that this is Christmas and we all deserve a holiday! Thank you for submitting your manuscript to Proceedings B; we look forward to receiving your revision. If you have any questions at all, please do not hesitate to get in touch. Referee: 2 Comments to the Author(s) This manuscript covers an interesting and important topic-the significance of understanding and harnessing animal culture to improve conservation outcomes. In general, the authors nicely articulate the multitude of ways that exploiting knowledge of social learning and cultural transmission of behavior can be used to bolster conservation capacity. I believe that this manuscript will be of interest to a broad readership, including both behavioral ecologists and conservation biologists. It is in my opinion, however, that several topics (e.g., limitations of the ethnographic approach, gene-culture association, cultural evolution, phylogenetic approaches) lacked depth or were partially or vaguely described. Further, and in attempt to adhere to journal word/page limits (I assume), the authors relegated many citations for empirical evidence needed support their messaging to the supplemental material. I focused my review on constructive ways to strengthen the manuscript and I hope the authors find my comments helpful.
Major comments: Ln 111-113: A central promise of the manuscript is "to provide recommendations (table S1) and a framework (figure 3) to guide the integration of culture and social learning into current conservation efforts". For this reason, I suggest moving table S1 into the main manuscript (it could feature as a full-page table). I understand that space is limited, but if the editor is willing to accommodate space for this table, I think it will strengthen the manuscript. The table would benefit from some horizontal lines that delineate and organize the various topics/ideas. As currently constructed, the table is difficult to follow.
Ln 181-190: This paragraph is important and could be strengthened using an example (or two) from the literature to help non-experts solidly understand the potential consequences of applying the ethnographic approach. If an example of the potential 'pitfalls' of this approach are absent in the literature, offering a hypothetical example would be helpful.
Ln 192-207: This is an important discussion that, to my understanding, is not well resolved in the literature. Using neutral genetic markers (i.e., those not under selection) to demonstrate correlation or clustering of behavioral variants among related individuals does indeed suggest inheritance of said behavior. Nevertheless, whether such inheritance of behavior has a genetic or socially learned basis cannot be determined via a correlational approach because genes that exert control of behavior may tag along with neutral genetic markers. Thus, correlation alone does not allow researchers to disentangle a genetic versus a socially learned basis of behavior (Laland and Janik 2006). Despite substantial effort, our ability to identify genes that control specific aspects of behavior are extremely limited (e.g., and with regards to migration, see Franchini et al. 2017 and references within), meaning determining the mode of inheritance usually requires an experiment. To deal with this issue, previous authors suggest transplant experiments as a viable approach for teasing apart genetic versus learned aspects of behavior (e.g., Laland and Janik 2006). As currently written, it seems the authors are suggesting that any evidence of inheritance of behavior can be viewed as evidence of social learning. For this reason, I suggest adding further discussion regarding the unresolved and complex associations between genotypic data and behavior. Laland, K. N., and V. M. Janik. 2006 Ln 380: Suggest expanding this section a bit and discussing gene-culture evolution (Whitehead et al. 2019, Nature Comm., already cited in manuscript) in more detail than is currently presented in the manuscript.
Ln 401: Cultural conservatism of migration routes is not mentioned in main text but is featured in figure 3. Suggest a sentence or two on conservatism. Also, such conservatism is generally referred to "site fidelity" (e.g., see Switzer 1993), and in the migration literature as "route fidelity" (e.g., see Morrison et al. in press, Wyckoff et al. 2018, Berger et al. 2006, Sawyer and Kauffman 2011   Ln 501: Here and in figure 3, the authors need to provide more information about how assessing phylogenetic propensity for social learning/cultural transmission would be accomplished. Even if it is just a sentence or two with some citations. Otherwise, the proposed approach is vague and requires the reader to guess and make leaps of faith as to what the authors are suggesting. Ln 518-521: Here and other areas of the manuscript, particularly the section on resilience, resistance, and recovery, is an opportune place to integrate some discussion of the role of cultural evolution in conservation outcomes. For example, cultural evolution may be a source of rapid adaptation to various aspects of global change. historic range where the species was previously extirpated. So, there were no knowledgeable individuals to translocate because no individuals had experience on those landscapes. I do not see a way to introduce/translocate knowledgeable individuals in reintroduction efforts. One potential mitigation strategy would be to perform some sort of 'assisted migration' (not in the way the term is typically used) where humans harness emulation or local enhancement to 'seed' knowledge in a subset of individuals (perhaps by training captive reared individuals in the natural setting a la Mueller et al. 2013, Science) about where and when to migrate, then see/hope if that information diffuses through a population.
Although space is always limited in print journals, and authors often feel forced to shift as much information as possible to supplemental materials (myself included), I strongly suggest a 7th column of references be added here. The information in the supplement will relatively rarely be read and authors of these works will not get appropriate accreditation. Given most of the studies used in this table are cited in the main text, I do not think it will add too many citations to the author's reference section to add a references column. ). These acronyms are not used over and over throughout the manuscript, so spelling them out will not cost much space but will certainly make the manuscript easier to read for non-experts. Also, with regards to using acronyms in figure 3, non-expert readers will have to search through the main text or supplemental materials to decipher the acronyms and interpret the figure.
Also, a more minor point regarding figure 3 is that bighorn lambs do not have full-curl horns. Suggest finding a silhouette with no or very small horns or using image editing software to delete the horns on the current silhouette.
Minor comments: Ln 163: What are "precautionary principles"? If this is jargon, I suggest defining. If the authors are referring to discussion preceding this paragraph, it remains unclear as to what these principles are.
Ln 175-179: This is an important message that I think will be appreciated by those interested in studying animal culture in wild populations where such 'gold standards' are impractical or impossible to implement. Thank you.
Ln 209: Suggest describing what is meant by "viewing culture in isolation" or reword. Unclear what is meant here.
Ln 219: Two complete sentences combined with a comma (i.e., run on sentence).
Ln 389: Typo. Should read "may not yet be" Ln 389-393: Reads awkwardly, suggest moving "thus providing a fertile area for on-going research" to the end of the sentence.
Ln 438-441: Suggest moving this sentence to after the sentence on the use of genetic pedigrees. Otherwise, the sentence on biologging interrupts the logical linkage between the first and third sentences about the use of genotypic data.

Recommendation
Reject -article is not of sufficient interest (we will consider a transfer to another journal) Scientific importance: Is the manuscript an original and important contribution to its field? Good General interest: Is the paper of sufficient general interest? Good Quality of the paper: Is the overall quality of the paper suitable? Good Is the length of the paper justified? Yes Should the paper be seen by a specialist statistical reviewer? No Do you have any concerns about statistical analyses in this paper? If so, please specify them explicitly in your report. No It is a condition of publication that authors make their supporting data, code and materials available -either as supplementary material or hosted in an external repository. Please rate, if applicable, the supporting data on the following criteria.

Do you have any ethical concerns with this paper? No
Comments to the Author This is the second time I have reviewed "A deepening understanding of animal culture brings novel perspectives to conservation". The authors did a good job addressing most of my previous comments and I thank them for taking the time to do so. However, I still can't help but get the feeling that this paper primarily about animal social learning and culture and the conservation aspect is only considered secondarily. Perhaps I am just not getting it -but I still don't feel like the link to conservation is very strong and I still found that many of the examples are great in the context of culture and social learning, but they are less relevant for the conservation and management of species. For example, that culture is related to survival in bottlenose dolphins (a very common species) is not particularly relevant for the conservation of any other species.
Within section 3 'Conservation through the lens of social learning and culture' -I found the link to conservation to be tenuous. The introductory section provides examples are only vaguely linked to potential conservation issues through things like "resource scarcity" -an ecological process that happens in all environments for all species (so this is not special for species at risk). See below for comments on the specific line numbers.
As this section progresses through section (a) to section (b) I felt as though I was reading a review on the link between culture and demography, not culture and conservation. Conservation certainly includes aspects of demography and the role of culture and social learning on vital rates is very important, but I still feel like the link to conservation is not as central as it could be. Specifically, I think the implication here is that if culture or social learning influence survival or reproduction than this is good for conservation. Sure, this may be true, but I feel I do think the golden lion tamarin example is a good one, but I find the bottlenose dolphin example to be a bit more tangential -aren't bottlenose dolphins one of the most common dolphin species in the world? I think the dots need to be better connected from social learning -> survival -> conservation efforts (in the tamarin example, the authors do this, but I think the dolphin example on line 297-301 one falls short).
Similarly in section (b), I find the bottlenose dolphin example between lines 321-324 is really interesting and important -but what is the link to conservation? Same thing goes for the sperm whale example between lines 329-333 -what is the link to conservation?
One general comment I have is that in many places, conservation is focused on habitat protection and less focused on protecting a single species -but this does not really come up except only indirectly in the migration section. What is the relevance of culture or social learning within the context of protecting large swathes of habitats?
Perhaps the authors might considering shifting the focus of the paper away from the extensive series of examples provided in text and using this space to focus more generally on the link between culture/social learning and the variable of interest (i.e. survival, reproduction, units to conserve, foraging, migration, or communication). I think having the examples in Figure 2 is great, but so many of the in text examples don't have a connection to conservation. I think getting more into the ecological and evolutionary underpinnings of culture and social learning and linking these general ideas to the conservation and management of species or habitats might be a more compelling way to demonstrate the importance of culture/social learning. With this type of narrative the authors could then develop more of a theoretical framework that does not rely on so many disparate empirical examples and they could focus on providing more detail on a smaller number of examples (e.g. the golden lion tamarin example).
I hope my review has been helpful and apologize if it is disappointing or if I am wrong in my assessment.

03-Mar-2021
Dear Dr Brakes: This is a tricky one --I asked you to revise your manuscript because one referee was extremely positive and the criticisms of the other referee looked as though they could be addressed without too much difficulty. However, having sent the revision back to the latter referee, they have come back not impressed... and now I see the nub of their problem. If I'd picked up on this earlier, I would have rejected the manuscript first time round, but now I feel I have led you too far down an encouraging route to deliver that slap in the face. The problem is that the title "A deepening understanding of animal culture brings novel perspectives to conservation" does not describe the paper. As the referee says, below, there is a very good review of social earning and animal culture, and some suggestions about how this MIGHT bring new perspectives to conservation, but it is definitely not a review of HOW deepening understanding of animal culture brings novel perspectives to conservation. As the referee says, the case studies are either not about animals of conservation concern or, when they are, the impacts are often speculative. The referee does recommend 'reject' on this basis, but also suggests that the ms by be saved by reframing it (not least with a change of title) as a review of our understanding of animal culture and how this might have lessons for conservation. I think that message is an important one, which is why I am giving you a second chance to revise and resubmit. I stress that this is a reframing issue, not any problem with examples you use or the arguments you put forward.
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Electronic supplementary material: All supplementary materials accompanying an accepted article will be treated as in their final form. They will be published alongside the paper on the journal website and posted on the online figshare repository. Files on figshare will be made available approximately one week before the accompanying article so that the supplementary material can be attributed a unique DOI. Please try to submit all supplementary material as a single file.
Online supplementary material will also carry the title and description provided during submission, so please ensure these are accurate and informative. Note that the Royal Society will not edit or typeset supplementary material and it will be hosted as provided. Please ensure that the supplementary material includes the paper details (authors, title, journal name, article DOI). Your article DOI will be 10.1098/rspb.[paper ID in form xxxx.xxxx e.g. 10.1098/rspb.2016.0049].
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Thank you for submitting your manuscript to Proceedings B; we look forward to receiving your revision. If you have any questions at all, please do not hesitate to get in touch.

Best wishes, Innes
Prof Innes Cuthill Reviews Editor, Proceedings B mailto: proceedingsb@royalsociety.org Reviewer(s)' Comments to Author: Referee: 1 Comments to the Author(s) This is the second time I have reviewed "A deepening understanding of animal culture brings novel perspectives to conservation". The authors did a good job addressing most of my previous comments and I thank them for taking the time to do so. However, I still can't help but get the feeling that this paper primarily about animal social learning and culture and the conservation aspect is only considered secondarily. Perhaps I am just not getting it -but I still don't feel like the link to conservation is very strong and I still found that many of the examples are great in the context of culture and social learning, but they are less relevant for the conservation and management of species. For example, that culture is related to survival in bottlenose dolphins (a very common species) is not particularly relevant for the conservation of any other species.
Within section 3 'Conservation through the lens of social learning and culture' -I found the link to conservation to be tenuous. The introductory section provides examples are only vaguely linked to potential conservation issues through things like "resource scarcity" -an ecological process that happens in all environments for all species (so this is not special for species at risk). See below for comments on the specific line numbers.
As this section progresses through section (a) to section (b) I felt as though I was reading a review on the link between culture and demography, not culture and conservation. Conservation certainly includes aspects of demography and the role of culture and social learning on vital rates is very important, but I still feel like the link to conservation is not as central as it could be. Specifically, I think the implication here is that if culture or social learning influence survival or reproduction than this is good for conservation. Sure, this may be true, but I feel I do think the golden lion tamarin example is a good one, but I find the bottlenose dolphin example to be a bit more tangential -aren't bottlenose dolphins one of the most common dolphin species in the world? I think the dots need to be better connected from social learning -> survival -> conservation efforts (in the tamarin example, the authors do this, but I think the dolphin example on line 297-301 one falls short).
Similarly in section (b), I find the bottlenose dolphin example between lines 321-324 is really interesting and important -but what is the link to conservation? Same thing goes for the sperm whale example between lines 329-333 -what is the link to conservation?
One general comment I have is that in many places, conservation is focused on habitat protection and less focused on protecting a single species -but this does not really come up except only indirectly in the migration section. What is the relevance of culture or social learning within the context of protecting large swathes of habitats?
Perhaps the authors might considering shifting the focus of the paper away from the extensive series of examples provided in text and using this space to focus more generally on the link between culture/social learning and the variable of interest (i.e. survival, reproduction, units to conserve, foraging, migration, or communication). I think having the examples in Figure 2 is great, but so many of the in text examples don't have a connection to conservation. I think getting more into the ecological and evolutionary underpinnings of culture and social learning and linking these general ideas to the conservation and management of species or habitats might be a more compelling way to demonstrate the importance of culture/social learning. With this type of narrative the authors could then develop more of a theoretical framework that does not rely on so many disparate empirical examples and they could focus on providing more detail on a smaller number of examples (e.g. the golden lion tamarin example).
I hope my review has been helpful and apologize if it is disappointing or if I am wrong in my assessment.

24-Mar-2021
Dear Ms Brakes I am pleased to inform you that your manuscript entitled "A deepening understanding of animal culture suggests lessons for conservation" has been accepted for publication in Proceedings B.
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Sincerely, Proceedings B mailto: proceedingsb@royalsociety.org This manuscript is call to action of sorts for the inclusion of culture and social learning within the field of conservation biology. The manuscript is well written, comprehensive, and undoubtedly fills an important gap in the literature. I would agree with the authors in a broad sense that culture, social learning, and more broadly social behaviour are extremely important in our goal to conserve species at risk -especially highly social species. I have a number of broad comments that I think authors might consider either adding or emphasizing a little bit to ensure the manuscript is accessible to a broader audience.

Social species vs. non-social species:
The article is framed around the idea that culture and social learning are important to consider for conservation -which I very much agree with -but as is the case for most conservation issues, incorporating culture and social learning int conservation is not a one size fits all solution. For example, many of the examples in text as well as those provided in Table 1 and supplementary section S3 tend to be species that are highly social, cognitively 'advanced', and tend to live in fission-fusion societies. I don't necessarily think this bias is a fault of the manuscript -I think these are simply the species most studied in the context of culture/social learning.
But, it does beg the question: is culture/social learning only applicable when discussing the conservation of highly social/cognitively advanced/fission-fusion species? I would say not, but the authors might consider adding a caveat at some point (possibly around lines 111-113?) that this framework and the associated recommendations are most relevant for social species.
At line 113 they authors could say "to guide the integration of culture and social learning into current conservation efforts of highly social species" -or something to that affect. Another option would be to additional sections in the supplementary section S3 that detail some species that are not highly social and cognitively advanced, perhaps there are some examples from fish, invertebrates, or small mammals? If not, then I think the main text deserves a short section outlining the existing bias in the literature.
What about conservation behaviour? I found there is somewhat of a glaring omission of any discussion on the topic of conservation behaviour. Numerous systematic papers have come out in the last year that discuss conservation behaviour in a similar context to what the authors do in this manuscript. Specifically, Berger-Tal et al. 2016 Conservation Biology examines the number of papers that examine different axes of behaviour and conservation. Although they do not include culture in their analysis they do include learning (as well as communication, migration, and foraging -all behaviours the authors suggest can have cultural l underpinnings). Based on figure 1 from Berger-Tal et al. 2016, it looks like there are some studies that link learning to various conservation threats and solutions -something the authors discuss throughout the manuscript -but no mention is made of the past efforts of those tackling the same problem through the lens of conservation behaviour. I'd suggest the authors consider adding a sub-section (possibly in section 3) of the manuscript that outlines discusses and integrates the existing work that exists in the conservation behaviour literature.

Appendix A
Why should managers care? I ask this is somewhat of a rhetorical question. I couldn't agree more with the authors that culture, social learning, and social behaviour more generally are exceptionally important in the conservation and management of species at risk. However, in my own experience studying species at risk and communicating with managers, it is not necessarily something that scientists are great at communicating to managers and managers might not always be receptive to the idea that these things are important. Further, I think it is unlikely that any (or many) managers are going to be reading this article, so the onus then falls onto the researcher studying culture/social learning to pass along this information to managers they work with through regular briefing meetings or through research grants/proposals/reports. So, that being said, I would challenge the authors to consider providing advice or recommendations (possibly in a box or figure?) that provides guidance for researchers to communicate with managers. For example, if your student studying culture/social learning of an endangered species was meeting with a government or NGO conservation manager, what are 2-3 ways you would encourage them to justify the importance of culture (keeping in mind things like communicating in plain language and with concision/precision).
I realize much of this information is contained within the article and in Table S1, but I think it would be useful for students and others new to working directly with conservation managers to have a generic and accessible summary/rubric that they could follow.
Examples: there are a ton of examples throughout the paper, which is great! However, it isn't always clear whether the example is meant to simply be an example of an example that culture/social learning exists in a given context or whether it is meant to be an example of how culture/social learning was important in that context for managing/conserving an endangered species. E.g. Lines 399-400 -this example of elephant crop raiding is certainly an example of social learning and foraging, but it doesn't really have anything to do with the conservation of elephants. In fact, it's almost the opposite… elephants learning bad behaviour at the risk of being shot! I think for most of the examples in the main text it might be a bit more precise if the authors could make sure it is clear whether a given example is meant to simply demonstrate that a given ecological trait (e.g. foraging, migration, communication) is related to culture/social learning OR whether these things are related AND it had an impact on the conservation of that species. Other examples on lines 412-415 (banded mongoose), 431 (whooping cranes), line 432 (right whales), line 443 (Brent geese), line 463 (chickens), 474 (white crowned sparrows). I realize the details for some of these species are outlined further in the supplementary materials, but I think when possible, it is good to clarify in text exactly what the example is doing for the reader, e.g. is it a culture ~ foraging relationship or is it a culture ~ foraging relationship that had an impact on conservation.

Minor comments:
Section 3(d): this section is quite short (only 3 sentences). By contrast, section 3(c) is two paragraphs. I would suggest either expanding on the ideas here or removing it altogether -I am not sure 3 sentences does the topic justice. Figure 2: maybe the authors could add a column that has the IUCN red list listing for these species? Again, I think this comes back to my earlier comment about how it isn't always clear whether an example is simply an example of a relationship between culture and another variable or whether this relationship is relevant for conservation. I think providing information on the species listing will add clarity to this aspect of the manuscript. Figure 3: are the silhouettes under each question indicative that those species satisfy the requirements associated with the question? E.g. Q1.1 Is there an indication of culture? The silhouettes of a primate, bird, and sheep -does this mean these species have satisfied the requirement of culture? And does that necessarily mean that any species silhouettes under Q1.2 or Q1.3 have not met the requirement for culture? Please provide a more detailed caption specifically regarding the placement of silhouettes.

Re-submission of review article: 'A deepening understanding of animal culture brings novel perspectives to conservation'
Dear Dr Kren and Prof Cuthill, thank you for providing an extension for responding to the Reviewer's comments for our manuscript 'A deepening understanding of animal culture brings novel perspectives to conservation'. We thank the Reviewers for their support and also the constructive comments to improve, clarify and streamline our manuscript. We have endeavored to address all points raised within the length limitations of the manuscript. Line numbers provided here refer to the revised manuscript without track changes.

Reviewer 1
This manuscript is call to action of sorts for the inclusion of culture and social learning within the field of conservation biology. The manuscript is well written, comprehensive, and undoubtedly fills an important gap in the literature. I would agree with the authors in a broad sense that culture, social learning, and more broadly social behaviour are extremely important in our goal to conserve species at risk -especially highly social species. I have a number of broad comments that I think authors might consider either adding or emphasizing a little bit to ensure the manuscript is accessible to a broader audience.
Social species vs. non-social species: The article is framed around the idea that culture and social learning are important to consider for conservation -which I very much agree with -but as is the case for most conservation issues, incorporating culture and social learning into conservation is not a one size fits all solution. For example, many of the examples in text as well as those provided in Table 1 and supplementary section S3 tend to be species that are highly social, cognitively 'advanced', and tend to live in fission-fusion societies. I don't necessarily think this bias is a fault of the manuscript -I think these are simply the species most studied in the context of culture/social learning.
But, it does beg the question: is culture/social learning only applicable when discussing the conservation of highly social/cognitively advanced/fission-fusion species? I would say not, but the authors might consider adding a caveat at some point (possibly around lines 111-113?) that this framework and the associated recommendations are most relevant for social species.
At line 113 they authors could say "to guide the integration of culture and social learning into current conservation efforts of highly social species" -or something to that affect. Another option would be to additional sections in the supplementary section S3 that detail some species that are not highly social and cognitively advanced, perhaps there are some examples from fish, invertebrates, or small mammals? If not, then I think the main text deserves a short section outlining the existing bias in the literature.

A: We agree with the reviewer that incorporating culture and social learning into conservation is not a one size fits all solution. The species included in the text and tables are those for which the implications for conservation have been investigated and provide the best evidence. Noting this, we have endeavoured to mitigate bias by selecting as wide a variety of species examples as possible.
In providing these examples, we hope this manuscript will serve as a 'call to arms' for research on species that are not highly social/cognitively advanced/fission-fusion species.
We have incorporated the suggested wording into the manuscript L113 "Finally, we provide a framework ( figure 3) to guide the integration of culture and social learning into current conservation efforts for social species".
We further explicitly acknowledge the bias in the literature and have added the following text L116 "Acknowledging the bias in the existing literature towards the most studied species, which are often more social and/or viewed as cognitively 'advanced', we highlight the crucial role that cultural transmission can play in guiding effective conservation responses".
What about conservation behaviour? I found there is somewhat of a glaring omission of any discussion on the topic of conservation behaviour. Numerous systematic papers have come out in the last year that discuss conservation behaviour in a similar context to what the authors do in this manuscript. Specifically, Berger-Tal et al. 2016 Conservation Biology examines the number of papers that examine different axes of behaviour and conservation. Although they do not include culture in their analysis they do include learning (as well as communication, migration, and foraging -all behaviours the authors suggest can have cultural l underpinnings). Based on figure 1 from Berger-Tal et al. 2016, it looks like there are some studies that link learning to various conservation threats and solutions -something the authors discuss throughout the manuscript -but no mention is made of the past efforts of those tackling the same problem through the lens of conservation behaviour. I'd suggest the authors consider adding a sub-section (possibly in section 3) of the manuscript that outlines discusses and integrates the existing work that exists in the conservation behaviour literature.

A: We have edited the text to incorporate this important point. A subsection is not possible due to space limitations; instead, we have made this point explicit in the Introduction to alert the reader to this complementary literature. We thank the reviewer for the suggested reference to include. L101 "The importance of conservation behaviour has been increasingly recognized [2,3]. However, a systematic review of the literature reveals learning and social behaviours were 'rarely considered' in wildlife conservation and management [5 p.744]".
Why should managers care? I ask this is somewhat of a rhetorical question. I couldn't agree more with the authors that culture, social learning, and social behaviour more generally are exceptionally important in the conservation and management of species at risk. However, in my own experience studying species at risk and communicating with managers, it is not necessarily something that scientists are great at communicating to managers and managers might not always be receptive to the idea that these things are important. Further, I think it is unlikely that any (or many) managers are going to be reading this article, so the onus then falls onto the researcher studying culture/social learning to pass along this information to managers they work with through regular briefing meetings or through research grants/proposals/reports. So, that being said, I would challenge the authors to consider providing advice or recommendations (possibly in a box or figure?) that provides guidance for researchers to communicate with managers. For example, if your student studying culture/social learning of an endangered species was meeting with a government or NGO conservation manager, what are 2-3 ways you would encourage them to justify the importance of culture (keeping in mind things like communicating in plain language and with concision/precision).
I realize much of this information is contained within the article and in Table S1, but I think it would be useful for students and others new to working directly with conservation managers to have a generic and accessible summary/rubric that they could follow. Table S1 to provide headings to assist in clarity and highlight some important points a student or those new to the field could convey. We have added text to highlight two key points in the main manuscript L493 "Specifically, understanding linkages between culture and vitals rates, cultural evolution, and adaption to rapid global change, will be critical for incorporating culture into management plans".

A: We have edited
Examples: there are a ton of examples throughout the paper, which is great! However, it isn't always clear whether the example is meant to simply be an example of an example that culture/social learning exists in a given context or whether it is meant to be an example of how culture/social learning was important in that context for managing/conserving an endangered species. E.g. Lines 399-400 -this example of elephant crop raiding is certainly an example of social learning and foraging, but it doesn't really have anything to do with the conservation of elephants. In fact, it's almost the opposite… elephants learning bad behaviour at the risk of being shot! I think for most of the examples in the main text it might be a bit more precise if the authors could make sure it is clear whether a given example is meant to simply demonstrate that a given ecological trait (e.g. foraging, migration, communication) is related to culture/social learning OR whether these things are related AND it had an impact on the conservation of that species. Other examples on lines 412-415 (banded mongoose), 431 (whooping cranes), line 432 (right whales), line 443 (Brent geese), line 463 (chickens), 474 (white crowned sparrows). I realize the details for some of these species are outlined further in the supplementary materials, but I think when possible, it is good to clarify in text exactly what the example is doing for the reader, e.g. is it a culture ~ foraging relationship or is it a culture ~ foraging relationship that had an impact on conservation.

Minor comments:
Section 3(d): this section is quite short (only 3 sentences). By contrast, section 3(c) is two paragraphs. I would suggest either expanding on the ideas here or removing it altogether -I am not sure 3 sentences does the topic justice.

A: In order to further elucidate Section 3(d), we moved section 3(c) to the electronic supplementary material (ESM, S3
) and added the following text beginning at L353: "Social learning and culture can promote demographic isolation between groups or populations with relevance to management and conservation (demographically independent populations (DIPs); figure 1, [48,61]). This demographic isolation can lead to genetic divergence and speciation through mechanisms such as assortative mating [62]. Figure 2 highlights examples where culture provides valuable data on the delineation of units to conserve at different scales (DIPs ([63,64]) and ESUs ([62,65]; figure 2). We direct readers to recent reviews [11,62] that delve into the role of culture as an evolutionary force leading population segments towards distinct evolutionary trajectories as ESUs ( figure 1, [41,66]), and highlight the role of gene-culture co-evolution in this process".
Figure 2: maybe the authors could add a column that has the IUCN red list listing for these species? Again, I think this comes back to my earlier comment about how it isn't always clear whether an example is simply an example of a relationship between culture and another variable or whether this relationship is relevant for conservation. I think providing information on the species listing will add clarity to this aspect of the manuscript. Figure 2. However, our feeling is that many of the IUCN global listing -where they do not include higher resolution assessments of regional populationsare too coarse to represent the finer-scale processes we are highlighting. For example, humpback whales are listed globally by the IUCN as of 'least concern' (LC), whereas the Oceania humpback whale population is listed as endangered (E). We articulate this issue in the text beginning at L510, where we state: "Thus, where salient, phenotypic variation arising from cultural, as well as ecological and genetic processes, could be informative for assessing demographic separation between potential units to conserve [61] and incorporated into national and international conservation frameworks (e.g., IUCN), following published examples (figure 2)". A key recommendation on this point is provided in the penultimate sentence (L526), which states: "Given that such an approach is common to preserving other aspects of biological diversity, and that culture and social learning can interface in multiple ways with conservation efforts, we recommend that the IUCN establish a cross-taxa specialist group to incorporate such information into IUCN assessments".

Reviewer 2
Comments to the Author(s) This manuscript covers an interesting and important topic-the significance of understanding and harnessing animal culture to improve conservation outcomes. In general, the authors nicely articulate the multitude of ways that exploiting knowledge of social learning and cultural transmission of behavior can be used to bolster conservation capacity. I believe that this manuscript will be of interest to a broad readership, including both behavioral ecologists and conservation biologists. It is in my opinion, however, that several topics (e.g., limitations of the ethnographic approach, gene-culture association, cultural evolution, phylogenetic approaches) lacked depth or were partially or vaguely described. Further, and in attempt to adhere to journal word/page limits (I assume), the authors relegated many citations for empirical evidence needed support their messaging to the supplemental material. I focused my review on constructive ways to strengthen the manuscript and I hope the authors find my comments helpful.

Major comments:
Ln 111-113: A central promise of the manuscript is "to provide recommendations (table S1) and a framework (figure 3) to guide the integration of culture and social learning into current conservation efforts". For this reason, I suggest moving table S1 into the main manuscript (it could feature as a full-page table). I understand that space is limited, but if the editor is willing to accommodate space for this table, I think it will strengthen the manuscript. The table would benefit from some horizontal lines that delineate and organize the various topics/ideas. As currently constructed, the table is difficult to follow.
A: We thank the reviewer for this suggestion. After discussions regarding space limitations with the editor, we now emphasise the framework (Fig. 3) which summarises the recommendations in table S1. We have further improved table S1 by adding horizontal lines and subheadings, as requested, following both Reviewer's suggestions for improvements.
Ln 181-190: This paragraph is important and could be strengthened using an example (or two) from the literature to help non-experts solidly understand the potential consequences of applying the ethnographic approach. If an example of the potential 'pitfalls' of this approach are absent in the literature, offering a hypothetical example would be helpful.

A: We have included two examples, as requested, to help non-experts understand the potential consequences of applying the ethnographic approach. L188 "However, the exclusion method is vulnerable to both over and under-attribution of cultural causes where researchers fail to recognise subtle environmental factors shaping individual plasticity or genetic change. For example, chimpanzees' use of long versus short stems to dip for ants was originally thought independent of habitat differences [26], but later detailed studies suggested the choice reflected local variations in the severity of ants' defensive biting [27].
Conversely the approach may neglect cultural behaviours that are adaptations to different local environments [24], such as tool use to crack shellfish in long-tailed macaques (Macaca fascicularis) [28]." : This is an important discussion that, to my understanding, is not well resolved in the literature. Using neutral genetic markers (i.e., those not under selection) to demonstrate correlation or clustering of behavioral variants among related individuals does indeed suggest inheritance of said behavior. Nevertheless, whether such inheritance of behavior has a genetic or socially learned basis cannot be determined via a correlational approach because genes that exert control of behavior may tag along with neutral genetic markers. Thus, correlation alone does not allow researchers to disentangle a genetic versus a socially learned basis of behavior (Laland and Janik 2006). Despite substantial effort, our ability to identify genes that control specific aspects of behavior are extremely limited (e.g., and with regards to migration, see Franchini et al. 2017 and references within), meaning determining the mode of inheritance usually requires an experiment. To deal with this issue, previous authors suggest transplant experiments as a viable approach for teasing apart genetic versus learned aspects of behavior (e.g., Laland and Janik 2006). As currently written, it seems the authors are suggesting that any evidence of inheritance of behavior can be viewed as evidence of social learning. For this reason, I suggest adding further discussion regarding the unresolved and complex associations between genotypic data and behavior. A: To expand upon some of these important issues, we have included the following new paragraph to help clarify the above discussion points (L215-237). However, as we cannot accommodate all requests for expansion of text, we explicitly direct readers to two excellent recent reviews discussing gene culture evolution which also cover the topic of section 3(c): "This approach has been questioned in the past due to the assumption that genetics plays a strong role in determining many behaviours [32]. However, the patterns of genetic diversity within populations and species are shaped by the demographic, adaptive and stochastic processes that govern genetic drift, gene flow, mutation and Darwinian selection. In this context, behavioural traits are likely determined by many genes that often have only small effect sizes and moderate heritability [33]. Neutral genetic markers typically used to assess relatedness and parentage are, by definition, less likely to be influenced by Darwinian selection than genes underpinning behavioural variants. While it is sometimes possible to conclusively rule out genetic effects in the described scenario by cross-fostering experiments to discover if they acquire their adopted or biological parents' foraging strategy [34,35], this is often not ethical or feasible for endangered species.
Culture can be one of many influences that shape behaviour and new modelling approaches now integrate ecological, social and genetic factors into analyses of behavioural variation (e.g., [36]). For example, network-based diffusion analysis (NBDA)

has been used to investigate the social transmission of behaviours in chimpanzees [37], humpback whales (Megaptera novaeangliae [38]), and bottlenose dolphins (Tursiops sp. [39]) by quantifying the extent to which social network structure explains the spread of a behaviour [36]."
Ln 401: Cultural conservatism of migration routes is not mentioned in main text but is featured in figure 3. Suggest a sentence or two on conservatism. Also, such conservatism is generally referred to "site fidelity" (e.g., see Switzer 1993), and in the migration literature as "route fidelity" (e.g., see Morrison et al. in press, Wyckoff et al. 2018, Berger et al. 2006 https://eprints.gla.ac.uk/226574/ A: We have included the following edits to address this point (L408) and have brought information from the ESM into the main body of the manuscript. We also now specifically mention route and/or site fidelity in this section: "In contrast, in some group-living species or those with extended periods of parental care, the first migration of an individual's life is often with conspecifics. The migration route and/or site learnt can therefore be horizontally transferred from conspecifics [71] or vertically transmitted from parent to offspring (e.g.,in whooping cranes,Grus americana [72] and southern right whales, Eubalaena australis [29]: see figure 2) helping ensure that offspring are able to find ephemeral resources in highly patchy environments [73]. Individuals can maintain these socially learned migratory behaviours across time, leading to a form of cultural conservatism, which can be of relevance to conservation. For example, migratory route fidelity influences management unit designation and the spatially patchy recovery from hunting of some baleen whale species [40]." Ln 403-405: Suggest adding a hypothetical or literature-based example here. Otherwise, reads as an unsupported assertion (which it is not).  Jesmer et al. 2018 in the main text, by adding the following sentence L430: "For example, translocation experiments for exploring the cultural basis of migratory behaviour, such as those conducted on big horn sheep (Ovis canadensis) and moose (Alces alces), provide strong evidence for the importance of cultural behaviour for conservation reintroductions [76], (see ESM S4b)." This reference is also now included in Figure 2 (along with other species references; see below).

A: This information is included in the expanded genetics section and as a Section in the ESM (S4b). We have directed readers towards evidence on translocation experiments provided by
Ln 501: Here and in figure 3, the authors need to provide more information about how assessing phylogenetic propensity for social learning/cultural transmission would be accomplished. Even if it is just a sentence or two with some citations. Otherwise, the proposed approach is vague and requires the reader to guess and make leaps of faith as to what the authors are suggesting.

A: We have removed reference to phylogenetic inferences.
Ln 518-521: Here and other areas of the manuscript, particularly the section on resilience, resistance, and recovery, is an opportune place to integrate some discussion of the role of cultural evolution in conservation outcomes. For example, cultural evolution may be a source of rapid adaptation to various aspects of global change.
A: Due to space requirements, Section 3c Resilience, has been moved to the ESM. However, to emphasise this important point, we have included the following text in Section 5 at L483: "Social learning and thus cultural evolution may provide opportunities for adaptive behaviours to spread in response to environmental change [84]. Conversely, social learning may prevent the spread of adaptive behaviour, potentially hindering recovery, if conformity is high or some other mechanism promotes cultural 'conservatism' [48]. It may also have a subtle and complex role in resistance to disturbance as the result of knowledgeable elders acting as repositories of social knowledge, as for example in African elephants and killer whales [56,85]." A: Additional text has been included in Section 5 to bring forward this link, and the link between culture and vital rates, for managers. L493 "Specifically, understanding linkages between culture and vitals rates, cultural evolution, and adaption to rapid global change ,will be critical for incorporating culture into management plans". their historic range where the species was previously extirpated. So, there were no knowledgeable individuals to translocate because no individuals had experience on those landscapes. I do not see a way to introduce/translocate knowledgeable individuals in reintroduction efforts. One potential mitigation strategy would be to perform some sort of 'assisted migration' (not in the way the term is typically used) where humans harness emulation or local enhancement to 'seed' knowledge in a subset of individuals (perhaps by training captive reared individuals in the natural setting a la Mueller et al. 2013, Science) about where and when to migrate, then see/hope if that information diffuses through a population.
A: To clarify this point, under the mitigation strategy column for bighorn sheep in Figure 2, we have edited the text from: "Introduce with knowledgeable individuals", to "Potential to harness emulation or local enhancement by intervening to seed knowledge in a sub-set of individuals".
Although space is always limited in print journals, and authors often feel forced to shift as much information as possible to supplemental materials (myself included), I strongly suggest a 7th column of references be added here. The information in the supplement will relatively rarely be read and authors of these works will not get appropriate accreditation. Given most of the studies used in this table are cited in the main text, I do not think it will add too many citations to the author's reference section to add a references column.  ). These acronyms are not used over and over throughout the manuscript, so spelling them out will not cost much space but will certainly make the manuscript easier to read for non-experts. Also, with regards to using acronyms in figure 3, non-expert readers will have to search through the main text or supplemental materials to decipher the acronyms and interpret the figure.
A: To address these points and increase clarity we have added common names under the silhouettes in Figure 3. We have also spelled out each acronym in Q3.2 and Q3.3 to ensure it is easily understandable to non-experts.
Also, a more minor point regarding figure 3 is that bighorn lambs do not have full-curl horns. Suggest finding a silhouette with no or very small horns or using image editing software to delete the horns on the current silhouette.
A: The horns on the lamb have been removed.
Minor comments: Ln 163: What are "precautionary principles"? If this is jargon, I suggest defining. If the authors are referring to discussion preceding this paragraph, it remains unclear as to what these principles are. (ESM S2) to ensure clarity for those not familiar with this management approach. ESM S2, Pg 2: "Precautionary principle: At its most basic, the precautionary principle is a principle of public decision making that requires decision makers in cases where there are 'threats' of environmental or health harm not to use 'lack of full scientific certainty' as a reason for not taking measures to prevent such harm [10]."

A: We have included a definition of this term in the Glossary
Ln 175-179: This is an important message that I think will be appreciated by those interested in studying animal culture in wild populations where such 'gold standards' are impractical or impossible to implement. Thank you.
A: Thank you.
Ln 209: Suggest describing what is meant by "viewing culture in isolation" or reword. Unclear what is meant here.
A: This sentence has been reworded for clarity L230 "Culture can be one of many influences that shape behaviour and new modelling approaches now integrate ecological, social and genetic factors into analyses (e.g.,[36])." Ln 219: Two complete sentences combined with a comma (i.e., run on sentence).

A: Edited to two sentences (now L239-241).
Ln 389: Typo. Should read "may not yet be" Ln 389-393: Reads awkwardly, suggest moving "thus providing a fertile area for on-going research" to the end of the sentence.
A: Typo fixed and sentence reworked (L369). "While linkages to vital rates and conservation impacts may not yet be established for many species, we hope the examples (ESM S4a-c, figure 2) will encourage readers to re-examine their data using a cultural lens to investigate whether social learning is important for conserving their focal species." Ln 438-441: Suggest moving this sentence to after the sentence on the use of genetic pedigrees. Otherwise, the sentence on biologging interrupts the logical linkage between the first and third sentences about the use of genotypic data.

A: Moved as suggested (see L427-430).
We provide below the tracked-changes manuscript and supplement. Please note that in the supplement (ESM S4(a), p.7) we reference unpublished data for a manuscript which is currently under review. We would be grateful for your advice on how best to refer to this material in the supplement. Thank you for further consideration of our manuscript. If there are any further questions or comments, please do not hesitate to contact us.

Response to Referee
Reviewer(s)' Comments to Author: Referee: 1 Comments to the Author(s) This is the second time I have reviewed "A deepening understanding of animal culture brings novel perspectives to conservation". The authors did a good job addressing most of my previous comments and I thank them for taking the time to do so.
1. Thank you. We endeavoured to address all of your comments.
However, I still can't help but get the feeling that this paper primarily about animal social learning and culture and the conservation aspect is only considered secondarily. Perhaps I am just not getting it -but I still don't feel like the link to conservation is very strong and I still found that many of the examples are great in the context of culture and social learning, but they are less relevant for the conservation and management of species. For example, that culture is related to survival in bottlenose dolphins (a very common species) is not particularly relevant for the conservation of any other species.

First, the paper provides a strong background on social learning and animal culture,
and how it is studied, precisely because it is aimed at an audience that includes many relevant readers who are unlikely to be familiar with the field and the possible linkages to conservation. Our approach has been to highlight (1: Section 3) processes through which social learning and culture influence fitness and population parameters and therefore may be important for conservation and management (i.e., survival, reproduction), and (2: Section 4) areas of research that might be particularly fruitful to examine in the context of culture and conservation (i.e., migration, foraging, communication [20,22,37], consideration and utilisation of social learning has proved important for increasing survival in managed populations ([2], ESM S4a)." 10. L447-450 "These contexts are often the focus of conservation actions. Therefore, our aim is to provide a roadmap to understand the contexts under which social learning may be relevant and to consider ways the field can contribute to promoting conservation outcomes." 11. We also note that many species are managed that are not of conservation concern.
The following text has been included to clarify this point. Within section 3 'Conservation through the lens of social learning and culture' -I found the link to conservation to be tenuous. The introductory section provides examples are only vaguely linked to potential conservation issues through things like "resource scarcity" -an ecological process that happens in all environments for all species (so this is not special for species at risk). See below for comments on the specific line numbers.
13. This is an example of a processes driven link. While resource scarcity can be a general ecological process, the issue we are raising here is that social learning can result in different segments of the population being differentially affected by ecological perturbations, such as prey abundance e.g., if they are reliant on different prey resources. We refer the reviewer to Figure 1, which provides an overview of conservation units (ESUs, DIPs, CVs) and how they are used in current conservation frameworks. We have also added the following example of such a process to Section 3c. L424-432 "For example, killer whales (Orcinus orca) can exhibit highly conservative socially learnt prey specialisations to the extent that separate, endangered fish-eating Southern Resident killer whale social units forage on fish (e.g., chinook salmon, Oncorhynchus tshawytscha) specific to individual river systems [58]. The population abundance of this social unit has declined along with its preferred prey. This reliance on a single river system and cultural reluctance to switch food sources clearly links the importance of understanding foraging culture with conservation management." As this section progresses through section (a) to section (b) I felt as though I was reading a review on the link between culture and demography, not culture and conservation. Conservation certainly includes aspects of demography and the role of culture and social learning on vital rates is very important, but I still feel like the link to conservation is not as central as it could be. Specifically, I think the implication here is that if culture or social learning influence survival or reproduction than this is good for conservation. Sure, this may be true, but I feel [sic] 14. Please see our approach above (e.g., bullet points 2-4). To address this specific comment, we have clarified in the text that we are discussing both conservation AND management (where both the positive and potential negative implications of social learning and culture can play a role). We contend that effective management includes preventing species declining into threatened status. While many bottlenose dolphin populations may not be of immediate conservation concern, some jurisdictions actively manage these populations and monitor the threats that they face. Thus, understanding the implications of cultural processes for some of these populations -including the culturally mediated sub-groups that they can form -can be highly relevant to policy.
I do think the golden lion tamarin example is a good one, but I find the bottlenose dolphin example to be a bit more tangential -aren't bottlenose dolphins one of the most common dolphin species in the world? I think the dots need to be better connected from social learning -> survival -> conservation efforts (in the tamarin example, the authors do this, but I think the dolphin example on line 297-301 one falls short).  (CMS), and 2) highlights some of the data deficiencies that need to be addressed to better understand the impact of conservation threats and culture on these groupings. 20. We have also clarified the elephant example to emphasise that this information should be taken into account by managers when making any translocation or culling decisions. L377-387. "At a group scale, the sharing of social information by experienced older African elephant (Loxodonta africana) matriarchs increases group survival and reproductive success, by providing information on the level of threat posed by elephants from other social groups and by predators in the wider environment [53]. Management plans should incorporate the understanding that matriarchs act as 'repositories of knowledge' and that loss of these individuals (e.g., culling or translocation) can have population-level impacts that persist for decades [54]."

To
One general comment I have is that in many places, conservation is focused on habitat protection and less focused on protecting a single species -but this does not really come up except only indirectly in the migration section. What is the relevance of culture or social learning within the context of protecting large swathes of habitats?
21. This is a fair point, but it relates to species-focused conservation generally, not just the social learning approach we're taking here. However, an extensive examination of this topic is beyond the scope of the current manuscript, although we highlight the link to habitat and ecosytems based management in figure 3. There's already an extensive literature on species vs habitat-based conservation, which highlights that conservation efforts for flagship species/species that provide important ecosystem services will benefit habitats as a whole (see Simberloff 1998) 4 .
Perhaps the authors might considering shifting the focus of the paper away from the extensive series of examples provided in text and using this space to focus more generally on the link between culture/social learning and the variable of interest (i.e. survival, reproduction, units to conserve, foraging, migration, or communication). I think having the examples in Figure 2 is great, but so many of the in text examples don't have a connection to conservation. I think getting more into the ecological and evolutionary underpinnings of culture and social learning and linking these general ideas to the conservation and management of species or habitats might be a more compelling way to demonstrate the importance of culture/social learning. With this type of narrative the authors could then develop more of a theoretical framework that does not rely on so many disparate empirical examples and they could focus on providing more detail on a smaller number of examples (e.g. the golden lion tamarin example).
22. Above, we outlined our general approach (bullet points 2-3); to draw on the existing body of literature to highlight (1) processes through which social learning and culture influence fitness and population parameters (i.e., survival, reproduction) and (2) areas of research that might be particularly fruitful to examine in the context of culture and conservation (i.e., migration, foraging, communication). This seems to be along the lines of the 'links' based approach that the reviewer has suggested, and