Propagation of interspecies sexual behaviour between Japanese macaques and Sika deer: First evidence
Cédric Sueur1, 2, 3, Atsuyuki Ohshima4, Marie Pélé2
1IPHC UMR7178, CNRS, Université de Strasbourg, Strasbourg, France
2ANTHROPO-LAB, ETHICS EA 7446, Université Catholique de Lille, Lille, France
3 Institut Universitaire de France, Paris, France
4Atsuyuki Ohshima photography, Kyoto
This study presents a series of observation of interspecies sexual behaviour involving Japanese macaques (Macaca fuscata yakui) and Sika deer (Cervus Nippon yakushimae) on Yakushima Island, Japan. The initial observation in 2015 revealed a male macaque’s attempt to engage in sexual activity with female deer, displaying mate-guarding behaviour. Subsequent observations in 2020, 2021 and 2023 showed the continuation of this behaviour and propagation to other macaques. We categorised this rare behaviour as a case of reproductive interference and explored hypotheses regarding its functionality. While some suggest nutritional benefits for the deer, others propose learning, incomplete species recognition, or mate deprivation hypotheses. Furthermore, we hypothesise that the observed propagation may underlie social transmission and highlight the potential cognitive capacities of Japanese macaques involving social learning mechanisms and the willingness to adopt non-instinctual behaviours.
Keywords: tradition, culture, reproductive interference, primate, cervid, behaviour
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Review of « Propagation of interspecies sexual behaviour between Japanese macaques and Sika deer: First evidence » by Sueur et al.
Reviewers:
Elisa Bandini & Benjamin Robira, Department of Evolutionary Biology and Environmental Sciences, University of Zürich, Switzerland
Summary: This manuscript is a follow-up to a previous report describing the first observation by humans of interspecies sexual behaviour from a male Japanese macaque towards Sika deer living on Yakushima Island in Japan (Sueur et al., 2017). This follow-up manuscript describes the same behaviour in the same group, this time by two females (and perhaps another individual, although it is unclear from the current version of the manuscript how many other individuals exactly participated in this behaviour). The behaviour was first reported in 2015 by a photographer and then was subsequently observed between 2020-2021, this time by a visitor to the park. These first observations involved a male macaque (or two different individuals, a fully confident ID for both observations could not be made). Soon after, two female macaques in the same group as the presupposed male who had first been observed doing the behaviour are also reported to have mounted deer. The authors mention a similar form of interspecies sexual behaviour between macaques and deer in a different group, 600 km from the current observed group, suggesting that this is not a unique behaviour to these macaques (Gunst et al., 2018). Following this reading, we open the discussion around three major criticisms, and pinpoint minor corrections which would be welcome.
Major comments
(1) Observational reports should be labelled as such, and not as quantitative results.
The vocabulary used by the authors throughout the manuscript is, in our opinion, strong and not appropriate for the unsystematic observational nature of the report. For example, the authors repeatedly refer to this manuscript as a “study” (e.g., L10, 71, 118, 209, 235, 256) and mention having conducted “analysis” (L192; see also section titles: L70, 143, 170). The use of these terms is misleading, as this manuscript stands as a “naturalistic note” on observations that are seemingly quite rare (or perhaps not so rare, as the other groups in the same population were not studied, and even the groups observed specifically for this behaviour were not tracked thoroughly). On this note, none of the claims made by the authors on the mechanisms potentially driving the behaviour (e.g., mutualistic behaviour, L143-168; social transmission, L204-208, cognitive complexity, L195-203) can be supported by the present report, due to its unsystematic observational nature (in line with the repetitive “if”s that are used throughout the all manuscript). Consequently, we encourage the authors to reduce and tone down speculation in this regard (e.g., L132, use of “significant findings”; L251 “illuminate”). We discuss this in more detail in the following point (2).
(2) Speculations should be labelled as such explicitly, and alternative explanations fully explored.
While we commend the authors for acknowledging the existence of some of the limitations (L209-221) of their report, the discussion of these is still very brief, and not all limitations are adequately mentioned and explained. The alternative explanations should also be discussed in as much detail as the ones favoured by the authors (only two lines, L220-221), and these should be explicitly labelled as speculations, due to the lack of systematic and concrete data on these aspects of the behaviour. One example of this is the discussion on social learning and culture throughout the manuscript.
The authors make several claims on the mechanisms driving the observed behaviour. Most prominently, they argue that social learning (or “cultural transmission” processes) similar to those hypothesized by some (but note, not by all researchers) for other primate behaviours (which they mention are mechanisms such as “imitation”) are responsible for the observation of this behaviour in various individuals of the group. Whilst we appreciate the authors taking the time to publish a follow-up report of this behaviour in other individuals in the group (or at least, new observations for the researchers), given the lack of systematic study of the observations, currently we cannot make any robust inferences on the mechanisms driving the innovation or presupposed propagation of the behaviour. To assess the learning mechanisms driving this behaviour, data would be required on several aspects (which is, due to the opportunistic nature of the observations, naturally missing from the current report): 1) knowledge on the timing of innovation of the behaviour, and how long it has been in the group. The authors only infer that this behaviour first started in 2015, because it was the first report of it, but it is unlikely that the true first occurrence of the behaviour happened to be observed and caught on camera. To the best of our knowledge, this group is not continuously followed and behaviour recorded, therefore making it impossible to assess the time depth of deer mounting. 2) Whether other individuals were already practicing the behaviour before the second observation, in which females were seen mounting deer. As with point 1, due to the lack of long-term, systematic, data collection on this behaviour, it is also very possible that the other females in the group were mounting deer before the first human observations of it, and that they started doing so at the same time as the male (or even before). Therefore, we have no clear data on who was the ‘innovator’ and who the behaviour may have been ‘passed on to’, or whether this process happened at all. Indeed, it is just as likely that the members of the group all started individually mounting deer, and that no social transmission occurred. On that note, to truly assess if and what types of social learning are driving the behaviour, we would need 3) data from controlled experiments targeting this specific behaviour. These experiments would require testing naïve individuals, for which we had confident data on their naivety to deer mounting and providing them with the social stimulus for the behaviour to emerge in a controlled manner (the information would have to be provided in a scaffolded manner so that the mechanism driving it could be assessed). As this behaviour has been observed in another group of macaques (Gunst et al., 2018), a more parsimonious assumption would be that ‘complex’ innovation or imitation abilities are not required for it to emerge, but it may merely be a reaction to exposure to the stimulus: in this case, deer. Due to the lack of all this data (again, this is not the fault of the authors but is merely due to the opportunistic nature of these observations), we would urge the authors to remove all discussion on the mechanisms driving the behaviour and its label as “cultural”, until a more systematic study has been conducted.
This, in short, is also applicable to some of the other arguments made in this report. For example, mutualism is claimed because of the observation of one deer licking the males’ seminal liquid (which is a difficult argument to make based on a single observation, as this phenomenon is actually quite complex to demonstrate. The authors may wish to refer to the plethora of reviews existing on this subject, as we are not experts in this ourselves either (see Bronstein, 2009)). However, if this were to be the case, it is even more unclear as to why female monkeys and deer would also engage in this behaviour (L153), and it is more likely that simple biological processes can account for this behaviour (e.g., a fly or insect might be as likely to lick the fluid as a deer). The authors also argue that the macaques are potentially suffering from cognitive impairments that result in issues with identifying correct sexual partners (L200-203). Again, this is a strong argument to be made based on the paucity of observations. A more parsimonious explanation could be that normal hormonal fluctuations (perhaps in response to the high monkey density) could naturally trigger the emergence of these behaviours (as has also been observed in domestic animals; the authors also briefly mention this hormonal explanation L155).
(3) The vocabulary used, sentence construction, and the tone throughout the manuscript should remain neutral.
From our reading, we had the impression that the position taken by the researchers is biased in favour of some hypotheses rather than others, both explicitly (see point (2)) and implicitly. We find this approach problematic given the lack of quantitative data. Indeed, the tone and construction of the text (starting from the introduction, which seems to be entirely focused on “culture” and “social learning” despite the lack of concrete data on these aspects in the current report (see point 2)) seems to point the reader in a certain direction, even before the data (which, again, in this case do not exist) are discussed. This approach can be misleading for the readers, who might interpret these anecdotal findings as concrete, systematic, data. We therefore urge the authors to carefully consider how they formulate the manuscript, and the types of vocabulary they choose to use (see points above). For example, the authors could remove all mentions of “culture” and “propagation” from the introduction, to ensure that a more neutral report of the observations is provided (see also minor comments below).
Minor comments
1. In order to make the chronology of events, as well as their spatial location, clearer, we would encourage the authors to provide a figure showing a chronological timeline of events, accompanied by a map showing the location of observations (where possible) at this site (and the neighbouring sites mentioned).
2. L31: These behaviours should not be labelled as “culturally transmitted”, as we do not currently know how the behaviours are being transmitted in the wild, and this is still a source of discussion and debate amongst researchers in the field (see above and Galef, 1992; Laland & Janik, 2006). Or at least, mention of the other side of the debate should be made, with associated references.
3. L40: This reference seems to be for whales, not crows. The authors may consider changing the location of this reference before the comma and add the one for crows.
4. L41: What do the authors mean by “simpler cognitive abilities”? We find the implicit hierarchization of cognition problematic, especially as the mechanisms underlying learning in fruit flies are, so far, quite similar to what has been demonstrated in the rest of the animal kingdom.
5. L51: The authors may consider removing the “as noted by”.
6. L54: The authors may consider replacing “evolve” with a less evolutionary-connotated term (e.g., “change”) as no evolution happens per se (also true for L64).
7. L56: Could the authors explain in a bit more detail why they categorise this behaviour as a “unique co-culture”? Most definitions of culture require that some social learning is happening (see Hoppitt & Laland, 2003) but as mentioned above, we do not have data for or against this hypothesis yet. In addition, we would encourage reducing use of superlatives such as “unique”, as assessing the true uniqueness of a behaviour is quite complex and depends on the different definitions of the term (e.g., see Whiten et al., 2001 & Motes-Rodrigo & Tennie, 2021).
8. L63: Could the authors explain why they categorise this behaviour as “highly complex”? Most definitions of complexity require an in-depth study of the steps involved in the innovation and actions of the behaviour, which is currently yet to be conducted for this particular behaviour (see also comment 4 above).
9. L95: Consider removing the dot before the reference list.
10. L96: “Came back for a week”. “for” might be missing in this sentence. Also, remove “a” from before “social transmission” and consider adding a comma after “observed”. Also, we believe “closed” should be “close” in this context.
11. L131: Could the authors clarify what they mean by the sentence starting with: “the sexual behaviour of females is not looking like…”
12. L134: As mentioned above, these types of arguments require more data and evidence than the current observation can provide.
13. L139: The figure legend includes claims that the same male was observed across both reports on this behaviour. However, the authors acknowledge that identification is uncertain on L117. Thus, the authors may consider rephrasing.
14. L150: “left” rather than “let”
15. L154: Consider removing this sentence, as it seems redundant with the one right above. Otherwise, you may add “for” such as it reads “allow for”
16. L157-159: It is unclear how this sentence relates to the previous one. By “similar proximity”, do the authors mean the occurrence of heterospecific sexual behaviour?
17. L167: Consider turning this sentence into two, or adding a comma after “dominant” to improve legibility
18. L192-194: It is unclear to us what the authors mean by “Our analysis aims to clarify the distinction between the cognitive processes inferred from these behaviours and our hypothesis of social transmission”. In particular, we find it difficult to understand the point of paragraph 1 on cognitive abilities. Note also on L193 a “dot” should be deleted before the citation list.
19. L195: Again, it should be acknowledged that this is unlikely to be the first innovation of the behaviour, considering the lack of systematic long-term data collection and the fact that other populations have been observed doing the same.
20. L207: As mentioned, this conclusion is not supported by any data and should therefore be removed.
21. L219: To provide the readers with a balanced and comprehensive understanding of the topic at hand, it would be appropriate to add references to the studies that have not found any evidence of observational learning or imitation in primates (e.g., Nagell et al., 1993: Tomasello & Call, 1994; Call et al., 2005; Tennie et al., 2006; 2012; Clay & Tennie, 2016; Neadle et al., 2021), or to remove this section.
22. L237-238: A reference should be used to support this claim.
23. L242: “which seem” may be rather “which seems”
24. L246 and 249: The authors speak about “cultural” behaviours and contrast them with “traditions”. The field makes a distinction between culture and tradition, and thus, the authors should rephrase for consistency (or remove these terms all together, see comments above).
25. We encourage the authors to end this report/note with an explicit concluding paragraph, as it currently finishes somewhat abruptly with evolutionary considerations that are only mentioned here for the first time and seem to be beyond the scope and scale of the current report.
26. References: There seem to be several problems with the formatting of references. This happens within the text (from L160 to L168, where references are suddenly numbered, or L186, where the authors appear in capitals) and within the reference list (e.g., L351, authors in capitals).
In summary, this manuscript provides an interesting report on interspecies sexual behaviour, which is relatively rarely observed in the animal kingdom, and therefore warrants further systematic investigation. This report, as acknowledged by the authors, was already the core of a previous publication (referred as 2016 in the text, but as 2017 in the reference list). Adding upon the singular 2016 observation can thus be of interest. Yet, due to the opportunistic, observational nature of the reports, and their rarity, however, we urge the authors to remove any strong claims on the mechanisms driving the behaviour from the current manuscript until the appropriate data are collected. We also urge the authors to be more considerate and balanced in their interpretation of these observations. We look forward to future reports in which these data are collected and discussed.
All the best, Elisa Bandini & Benjamin Robira
References
Bronstein, Judith L. “The evolution of facilitation and mutualism.” Journal of Ecology 97.6 (2009): 1160-1170.
Call, J., Carpenter, M., & Tomasello, M. (2005). Copying results and copying actions in the process of social learning: chimpanzees (Pan troglodytes) and human children (Homo sapiens). Animal cognition, 8, 151-163.
Clay, Z., & Tennie, C. (2018). Is overimitation a uniquely human phenomenon? Insights from human children as compared to bonobos. Child development, 89(5), 1535-1544.
Galef, B. G. (1992). The question of animal culture. Human nature, 3, 157-178.
Laland, K. N., & Hoppitt, W. (2003). Do animals have culture?. Evolutionary Anthropology: Issues, News, and Reviews: Issues, News, and Reviews, 12(3), 150-159.
Laland, K. N., & Janik, V. M. (2006). The animal cultures debate. Trends in ecology & evolution, 21(10), 542-547.
Motes‐Rodrigo, A., & Tennie, C. (2021). The M ethod of L ocal R estriction: in search of potential great ape culture‐dependent forms. Biological Reviews, 96(4), 1441-1461.
Neadle, D. L., Chappell, J., Clay, Z., & Tennie, C. (2021). Even under majority influence, great apes fail to copy novel actions.
Nagell, K., Olguin, R. S., & Tomasello, M. (1993). Processes of social learning in the tool use of chimpanzees (Pan troglodytes) and human children (Homo sapiens). Journal of comparative psychology, 107(2), 174.
Pelé, M., Bonnefoy, A., Shimada, M., & Sueur, C. (2017). Interspecies sexual behaviour between a male Japanese macaque and female sika deer. Primates, 58(2), 275-278.
Tennie, C., Call, J., & Tomasello, M. (2006). Push or pull: Imitation vs. emulation in great apes and human children. Ethology, 112(12), 1159-1169.
Tennie, C., Call, J., & Tomasello, M. (2012). Untrained chimpanzees (Pan troglodytes schweinfurthii) fail to imitate novel actions.
Tomasello, M., & Call, J. (1994). Social cognition of monkeys and apes. American Journal of Physical Anthropology, 37(S19), 273-305.
Whiten, A., Goodall, J., McGrew, W. C., Nishida, T., Reynolds, V., Sugiyama, Y., … & Boesch, C. (2001). Charting cultural variation in chimpanzees. Behaviour, 1481-1516
Authors’ responses inserted in review text, marked by AUTHORS
Review of « Propagation of interspecies sexual behaviour between Japanese macaques and Sika deer: First evidence » by Sueur et al.
Summary: This manuscript is a follow-up to a previous report describing the first observation by humans of interspecies sexual behaviour from a male Japanese macaque towards Sika deer living on Yakushima Island in Japan (Sueur et al., 2017). This follow-up manuscript describes the same behaviour in the same group, this time by two females (and perhaps another individual, although it is unclear from the current version of the manuscript how many other individuals exactly participated in this behaviour). The behaviour was first reported in 2015 by a photographer and then was subsequently observed between 2020-2021, this time by a visitor to the park. These first observations involved a male macaque (or two different individuals, a fully confident ID for both observations could not be made). Soon after, two female macaques in the same group as the presupposed male who had first been observed doing the behaviour are also reported to have mounted deer. The authors mention a similar form of interspecies sexual behaviour between macaques and deer in a different group, 600 km from the current observed group, suggesting that this is not a unique behaviour to these macaques (Gunst et al., 2018). Following this reading, we open the discussion around three major criticisms, and pinpoint minor corrections which would be welcome.
AUTHORS: We thank the two reviewers for their helpful. We answered all of them positively.
Major comments
(1) Observational reports should be labelled as such, and not as quantitative results.
The vocabulary used by the authors throughout the manuscript is, in our opinion, strong and not appropriate for the unsystematic observational nature of the report. For example, the authors repeatedly refer to this manuscript as a “study” (e.g., L10, 71, 118, 209, 235, 256) and mention having conducted “analysis” (L192; see also section titles: L70, 143, 170). The use of these terms is misleading, as this manuscript stands as a “naturalistic note” on observations that are seemingly quite rare (or perhaps not so rare, as the other groups in the same population were not studied, and even the groups observed specifically for this behaviour were not tracked thoroughly). On this note, none of the claims made by the authors on the mechanisms potentially driving the behaviour (e.g., mutualistic behaviour, L143-168; social transmission, L204-208, cognitive complexity, L195-203) can be supported by the present report, due to its unsystematic observational nature (in line with the repetitive “if”s that are used throughout the all manuscript). Consequently, we encourage the authors to reduce and tone down speculation in this regard (e.g., L132, use of “significant findings”; L251 “illuminate”). We discuss this in more detail in the following point (2).
AUTHORS: We labelled our research as note and toned down speculation about propagation.
(2) Speculations should be labelled as such explicitly, and alternative explanations fully explored.
While we commend the authors for acknowledging the existence of some of the limitations (L209-221) of their report, the discussion of these is still very brief, and not all limitations are adequately mentioned and explained. The alternative explanations should also be discussed in as much detail as the ones favoured by the authors (only two lines, L220-221), and these should be explicitly labelled as speculations, due to the lack of systematic and concrete data on these aspects of the behaviour. One example of this is the discussion on social learning and culture throughout the manuscript.
The authors make several claims on the mechanisms driving the observed behaviour. Most prominently, they argue that social learning (or “cultural transmission” processes) similar to those hypothesized by some (but note, not by all researchers) for other primate behaviours (which they mention are mechanisms such as “imitation”) are responsible for the observation of this behaviour in various individuals of the group. Whilst we appreciate the authors taking the time to publish a follow-up report of this behaviour in other individuals in the group (or at least, new observations for the researchers), given the lack of systematic study of the observations, currently we cannot make any robust inferences on the mechanisms driving the innovation or presupposed propagation of the behaviour. To assess the learning mechanisms driving this behaviour, data would be required on several aspects (which is, due to the opportunistic nature of the observations, naturally missing from the current report): 1) knowledge on the timing of innovation of the behaviour, and how long it has been in the group. The authors only infer that this behaviour first started in 2015, because it was the first report of it, but it is unlikely that the true first occurrence of the behaviour happened to be observed and caught on camera. To the best of our knowledge, this group is not continuously followed and behaviour recorded, therefore making it impossible to assess the time depth of deer mounting. 2) Whether other individuals were already practicing the behaviour before the second observation, in which females were seen mounting deer. As with point 1, due to the lack of long-term, systematic, data collection on this behaviour, it is also very possible that the other females in the group were mounting deer before the first human observations of it, and that they started doing so at the same time as the male (or even before). Therefore, we have no clear data on who was the ‘innovator’ and who the behaviour may have been ‘passed on to’, or whether this process happened at all. Indeed, it is just as likely that the members of the group all started individually mounting deer, and that no social transmission occurred. On that note, to truly assess if and what types of social learning are driving the behaviour, we would need 3) data from controlled experiments targeting this specific behaviour. These experiments would require testing naïve individuals, for which we had confident data on their naivety to deer mounting and providing them with the social stimulus for the behaviour to emerge in a controlled manner (the information would have to be provided in a scaffolded manner so that the mechanism driving it could be assessed). As this behaviour has been observed in another group of macaques (Gunst et al., 2018), a more parsimonious assumption would be that ‘complex’ innovation or imitation abilities are not required for it to emerge, but it may merely be a reaction to exposure to the stimulus: in this case, deer. Due to the lack of all this data (again, this is not the fault of the authors but is merely due to the opportunistic nature of these observations), we would urge the authors to remove all discussion on the mechanisms driving the behaviour and its label as “cultural”, until a more systematic study has been conducted.
This, in short, is also applicable to some of the other arguments made in this report. For example, mutualism is claimed because of the observation of one deer licking the males’ seminal liquid (which is a difficult argument to make based on a single observation, as this phenomenon is actually quite complex to demonstrate. The authors may wish to refer to the plethora of reviews existing on this subject, as we are not experts in this ourselves either (see Bronstein, 2009)). However, if this were to be the case, it is even more unclear as to why female monkeys and deer would also engage in this behaviour (L153), and it is more likely that simple biological processes can account for this behaviour (e.g., a fly or insect might be as likely to lick the fluid as a deer). The authors also argue that the macaques are potentially suffering from cognitive impairments that result in issues with identifying correct sexual partners (L200-203). Again, this is a strong argument to be made based on the paucity of observations. A more parsimonious explanation could be that normal hormonal fluctuations (perhaps in response to the high monkey density) could naturally trigger the emergence of these behaviours (as has also been observed in domestic animals; the authors also briefly mention this hormonal explanation L155).
AUTHORS: We added this paragraph: “To fully understand the learning mechanisms underlying this behavior, additional data would be required on several fronts, as noted by reviewers. First, establishing the timing of behavior innovation and duration within the group is critical; although we noted the first recorded occurrence in 2015, this likely does not reflect the initial appearance of deer mounting. Second, without continuous monitoring, it remains unclear if other individuals practiced this behavior prior to the second observation, when females were noted engaging in deer mounting. We therefore lack data on the original innovator of the behavior and the potential pathways of social transmission within the group, if any. It is equally plausible that all members began engaging in this behavior independently, with no social learning involved. To rigorously assess the role of social learning, controlled experimental data would be essential, ideally involving naïve individuals exposed to social stimuli in a controlled setting. These experiments would require testing individuals confirmed to be naïve to deer mounting and systematically introducing the behavior to discern the mechanisms behind its emergence. Given that this behavior has also been observed in a separate group of macaques (Gunst et al., 2018), a simpler assumption may be that complex social learning mechanisms are not required for this behavior to manifest; rather, exposure to the stimulus—in this case, the deer—may be sufficient for its appearance.
(3) The vocabulary used, sentence construction, and the tone throughout the manuscript should remain neutral.
From our reading, we had the impression that the position taken by the researchers is biased in favour of some hypotheses rather than others, both explicitly (see point (2)) and implicitly. We find this approach problematic given the lack of quantitative data. Indeed, the tone and construction of the text (starting from the introduction, which seems to be entirely focused on “culture” and “social learning” despite the lack of concrete data on these aspects in the current report (see point 2)) seems to point the reader in a certain direction, even before the data (which, again, in this case do not exist) are discussed. This approach can be misleading for the readers, who might interpret these anecdotal findings as concrete, systematic, data. We therefore urge the authors to carefully consider how they formulate the manuscript, and the types of vocabulary they choose to use (see points above). For example, the authors could remove all mentions of “culture” and “propagation” from the introduction, to ensure that a more neutral report of the observations is provided (see also minor comments below).
AUTHORS: Given the journal topics and aims, we think that it is better to focus the introduction on culture. However, we were careful in the rest of the manuscript about our interpretations.
Minor comments
1. In order to make the chronology of events, as well as their spatial location, clearer, we would encourage the authors to provide a figure showing a chronological timeline of events, accompanied by a map showing the location of observations (where possible) at this site (and the neighbouring sites mentioned).
AUTHORS: We added a figure with a timeline and a map (figure 2).
2. L31: These behaviours should not be labelled as “culturally transmitted”, as we do not currently know how the behaviours are being transmitted in the wild, and this is still a source of discussion and debate amongst researchers in the field (see above and Galef, 1992; Laland & Janik, 2006). Or at least, mention of the other side of the debate should be made, with associated references.
AUTHORS: We replaced with “cultural behaviours”. Thank for noting it.
3. L40: This reference seems to be for whales, not crows. The authors may consider changing the location of this reference before the comma and add the one for crows.
AUTHORS: We changed the location of the reference and added a new one.
4. L41: What do the authors mean by “simpler cognitive abilities”? We find the implicit hierarchization of cognition problematic, especially as the mechanisms underlying learning in fruit flies are, so far, quite similar to what has been demonstrated in the rest of the animal kingdom.
AUTHORS: Indeed, we removed this term.
5. L51: The authors may consider removing the “as noted by”.
AUTHORS: Done
6. L54: The authors may consider replacing “evolve” with a less evolutionary-connotated term (e.g., “change”) as no evolution happens per se (also true for L64).
AUTHORS; Done
7. L56: Could the authors explain in a bit more detail why they categorise this behaviour as a “unique co-culture”? Most definitions of culture require that some social learning is happening (see Hoppitt & Laland, 2003) but as mentioned above, we do not have data for or against this hypothesis yet. In addition, we would encourage reducing use of superlatives such as “unique”, as assessing the true uniqueness of a behaviour is quite complex and depends on the different definitions of the term (e.g., see Whiten et al., 2001 & Motes-Rodrigo & Tennie, 2021).
AUTHORS: We added a definition and a reference : (Co-culture is the mutual evolution of shared behaviors between different species that influence each other through direct or indirect interactions in a shared environment) (Sueur and Huffman 2024).
We removed the term “unique”.
8. L63: Could the authors explain why they categorise this behaviour as “highly complex”? Most definitions of complexity require an in-depth study of the steps involved in the innovation and actions of the behaviour, which is currently yet to be conducted for this particular behaviour (see also comment 4 above).
AUTHORS: We added a sentence: “These behaviors are categorized as ‘highly complex’ due to the active feedback loops between the species, which foster reciprocal adaptations, and the layered nature of their interactions—from foraging and grooming to intricate behaviors like riding and interspecies sexual activities—indicating cognitive processes, social transmission, and behavioral innovation that evolve through mutual influence.”
9. L95: Consider removing the dot before the reference list.
AUTHORS: Done
10. L96: “Came back for a week”. “for” might be missing in this sentence. Also, remove “a” from before “social transmission” and consider adding a comma after “observed”. Also, we believe “closed” should be “close” in this context.
AUTHORS: Done, thanks a lot.
11. L131: Could the authors clarify what they mean by the sentence starting with: “the sexual behaviour of females is not looking like…”
AUTHORS: We developed the sentence and added a reference: The sexual behavior displayed by female macaques toward male deer differs from the typical mating behaviors observed with male macaques, as the pelvic movements are slower, less rhythmic, and lack the thrusting intensity usually seen in heterosexual interactions. Instead, these movements resemble the slower pelvic motions often observed in female-female homosexual interactions among macaques (Leca et al. 2015).
12. L134: As mentioned above, these types of arguments require more data and evidence than the current observation can provide.
AUTHORS: We changed the sentence to: These observations indicate two significant findings: firstly, if it indeed is the original male observed in 2015, the macaque exhibited a continuation of the original behaviour, and secondly, these observations suggest possible propagation (Duboscq et al. 2016) of this behaviour to other group members though further data and evidence are needed to confirm this transmission.
13. L139: The figure legend includes claims that the same male was observed across both reports on this behaviour. However, the authors acknowledge that identification is uncertain on L117. Thus, the authors may consider rephrasing.
AUTHORS: We added “probably” to acknowledge the uncertainty.
14. L150: “left” rather than “let”
AUTHORS: Done.
15. L154: Consider removing this sentence, as it seems redundant with the one right above. Otherwise, you may add “for” such as it reads “allow for”
AUTHORS: Done
16. L157-159: It is unclear how this sentence relates to the previous one. By “similar proximity”, do the authors mean the occurrence of heterospecific sexual behaviour?
AUTHORS: We removed the sentence about dolphins.
17. L167: Consider turning this sentence into two, or adding a comma after “dominant” to improve legibility
AUTHORS: Done
18. L192-194: It is unclear to us what the authors mean by “Our analysis aims to clarify the distinction between the cognitive processes inferred from these behaviours and our hypothesis of social transmission”. In particular, we find it difficult to understand the point of paragraph 1 on cognitive abilities. Note also on L193 a “dot” should be deleted before the citation list.
AUTHORS: We entirely changed this paragraph.
19. L195: Again, it should be acknowledged that this is unlikely to be the first innovation of the behaviour, considering the lack of systematic long-term data collection and the fact that other populations have been observed doing the same.
AUTHORS: We changed to: “The initial sightings in 2015 suggested a novel aspect of macaque behavior, although it is unlikely to be the first occurrence of this innovation given the absence of systematic, long-term data collection and similar behaviors observed in other populations. However, this was the first documented instance, as other colleagues regularly present in the field had never previously observed it.”
20. L207: As mentioned, this conclusion is not supported by any data and should therefore be removed.
AUTHORS: We changed to: The social transmission hypothesis is supported by observations from 2020 to 2023, during which macaques of both sexes exhibited similar interspecies interactions. These findings may align with the hypothesis that social learning and transmission are at play, as the spread of this behavior across different individuals, potentially from males to females, suggests an advanced form of social learning. This behavior indicates that macaques may be open to adopting behaviors through observation and interaction as indicated with other behaviors culturally transmitted in this species (Zhang and Watanabe 2007; Zhang et al. 2007; Huffman et al. 2010).
21. L219: To provide the readers with a balanced and comprehensive understanding of the topic at hand, it would be appropriate to add references to the studies that have not found any evidence of observational learning or imitation in primates (e.g., Nagell et al., 1993: Tomasello & Call, 1994; Call et al., 2005; Tennie et al., 2006; 2012; Clay & Tennie, 2016; Neadle et al., 2021), or to remove this section.
AUTHORS: We added this sentence and the references: We also acknowledge the possibility of alternative explanations for the observed behaviour, including individual learning or a shared environmental influence as some studies have not found any evidence of observational learning or imitation in primates (Nagell et al. 1993; Tomasello and Call 1994; Call et al. 2005; Tennie et al. 2006; Clay and Tennie 2018; Neadle et al. 2021).
22. L237-238: A reference should be used to support this claim.
AUTHORS: Done
23. L242: “which seem” may be rather “which seems”
AUTHORS: Done
24. L246 and 249: The authors speak about “cultural” behaviours and contrast them with “traditions”. The field makes a distinction between culture and tradition, and thus, the authors should rephrase for consistency (or remove these terms all together, see comments above).
AUTHORS: We replace traditions with behaviours.
25. We encourage the authors to end this report/note with an explicit concluding paragraph, as it currently finishes somewhat abruptly with evolutionary considerations that are only mentioned here for the first time and seem to be beyond the scope and scale of the current report.
AUTHORS: We added a conclusion.
26. References: There seem to be several problems with the formatting of references. This happens within the text (from L160 to L168, where references are suddenly numbered, or L186, where the authors appear in capitals) and within the reference list (e.g., L351, authors in capitals).
AUTHORS: Sorry, we corrected these mistakes.
In summary, this manuscript provides an interesting report on interspecies sexual behaviour, which is relatively rarely observed in the animal kingdom, and therefore warrants further systematic investigation. This report, as acknowledged by the authors, was already the core of a previous publication (referred as 2016 in the text, but as 2017 in the reference list). Adding upon the singular 2016 observation can thus be of interest. Yet, due to the opportunistic, observational nature of the reports, and their rarity, however, we urge the authors to remove any strong claims on the mechanisms driving the behaviour from the current manuscript until the appropriate data are collected. We also urge the authors to be more considerate and balanced in their interpretation of these observations. We look forward to future reports in which these data are collected and discussed.
AUTHORS: Thank you very much for your feedback. We hope the revisions we have made to the manuscript align well with your expectations and address your comments thoroughly.
References
Bronstein, Judith L. “The evolution of facilitation and mutualism.” Journal of Ecology 97.6 (2009): 1160-1170.
Call, J., Carpenter, M., & Tomasello, M. (2005). Copying results and copying actions in the process of social learning: chimpanzees (Pan troglodytes) and human children (Homo sapiens). Animal cognition, 8, 151-163.
Clay, Z., & Tennie, C. (2018). Is overimitation a uniquely human phenomenon? Insights from human children as compared to bonobos. Child development, 89(5), 1535-1544.
Galef, B. G. (1992). The question of animal culture. Human nature, 3, 157-178.
Laland, K. N., & Hoppitt, W. (2003). Do animals have culture?. Evolutionary Anthropology: Issues, News, and Reviews: Issues, News, and Reviews, 12(3), 150-159.
Laland, K. N., & Janik, V. M. (2006). The animal cultures debate. Trends in ecology & evolution, 21(10), 542-547.
Motes‐Rodrigo, A., & Tennie, C. (2021). The M ethod of L ocal R estriction: in search of potential great ape culture‐dependent forms. Biological Reviews, 96(4), 1441-1461.
Neadle, D. L., Chappell, J., Clay, Z., & Tennie, C. (2021). Even under majority influence, great apes fail to copy novel actions.
Nagell, K., Olguin, R. S., & Tomasello, M. (1993). Processes of social learning in the tool use of chimpanzees (Pan troglodytes) and human children (Homo sapiens). Journal of comparative psychology, 107(2), 174.
Pelé, M., Bonnefoy, A., Shimada, M., & Sueur, C. (2017). Interspecies sexual behaviour between a male Japanese macaque and female sika deer. Primates, 58(2), 275-278.
Tennie, C., Call, J., & Tomasello, M. (2006). Push or pull: Imitation vs. emulation in great apes and human children. Ethology, 112(12), 1159-1169.
Tennie, C., Call, J., & Tomasello, M. (2012). Untrained chimpanzees (Pan troglodytes schweinfurthii) fail to imitate novel actions.
Tomasello, M., & Call, J. (1994). Social cognition of monkeys and apes. American Journal of Physical Anthropology, 37(S19), 273-305.
Whiten, A., Goodall, J., McGrew, W. C., Nishida, T., Reynolds, V., Sugiyama, Y., … & Boesch, C. (2001). Charting cultural variation in chimpanzees. Behaviour, 1481-1516.
Review of « Propagation of interspecies sexual behaviour between Japanese macaques and Sika deer: First evidence » by Sueur et al.
Reviewer:
Jean-Baptiste LECA, Ph.D. Associate Professor, Department of Psychology, University of Lethbridge, Lethbridge, Alberta, T1K 3M4, CANADA
This is a well-written manuscript providing a descriptive account of a seldom reported behavior that has the potential to improve our understanding of mixed-species associations. Even though the functional interpretations of this behavior are speculative, I have no issues with them being cautiously laid out here, as I agree with the authors that this list could drive further research on the topic, with the goal to test some of these hypothetical functions (if any… see below my point about this). For these reasons, I think it should be published.
However, there are two major points that I would like the authors to address in a possibly revised version of their manuscript. In short, I am sold about (1) the following statement “We categorised this rare behaviour as a case of reproductive interference” (Line 14-15), and (2) the argument that these few observed cases are the result of some form of behavioural “propagation” (title of the manuscript, but also throughout the text) that may be underlain by “social transmission” (Line 18, Line 141, Line 189-221). The authors should provide further evidence to convince me about the validity of these two claims.
First, how do you define “reproductive interference” (Line 144-145 provides a citation but not a definition), and how does this definition matches the reported behavioural observations? Without this extra explanation, the following claim sounds highly speculative: “The fact that female macaques have reproductive interference with male deer […]” (Line 201) and should be removed from the manuscript.
Second, while I praise the authors for their attempt to build an argument for a so-called “propagation” of the behaviour that would be scaffolded by some kind of social transmission process in the face of very little and sparse empirical behavioural evidence (Line 204-221)… I am sorry to say that I don’t think this case is strong enough, when considering the data set presented here.
Would it be possible to get more information about the beginning of the behaviour? Or even better: evaluate approximately when it may have started and whether the male whose behaviour is extensively described could have been the “inventor” of it (i.e., no reports or no observations of a similar case in this population before, despite significant research effort)? Finally, would it be possible collect more data on the social connections between performers of the behaviour and get a clearer pattern of behavioural contagion (in terms of timing of performance: let’s say a case of multiple monkeys performing the behaviour in the same area and within a short time window on a given day)? This would convince me that there might be some social influences going on.
Again, some of the presented evidence clearly indicates that the behaviour is not idiosyncratic and that it persists over time. However, I believe a stronger case should be made for a publication in a journal whose main scope is grounded in cultural phenomena. Currently, the methodological approach used to present the data is not systematic/consistent and largely based on anecdotal evidence. Specifically, we cannot rule out the probability that the acquisition and performance of this behaviour has been the result of independent motivational processes rather than “social transmission” (as acknowledged by the authors: Line 216). Therefore, it is my impression that the case for “social transmission”, which is one of the main angles of the current manuscript, is very weak.
Additional and minor points:
Line 72-73: (Pelé et al. 2017) — What is the point of this in-text citation in this specific context?
Line 130-132: The sexual behaviour of females is not looking like the ones displayed with males but the ones displayed during homosexual behaviours. — What do you mean here? Do female Japanese macaques display homosexual behaviours among each other? In this population/geographic area? Has this been reported? If so, could you please cite your sources and explain what makes you argue about such behavioural similarities between what you observed and what may have been reported?
Line 16-17 and Line 143-168: In addition to this list of possible functions for this intriguing behaviour, would it be possible to acknowledge that it may be selectively neutral, have no fitness benefits of its own, but simply be a behavioural by-product of other (potentially adaptive) interactions between these two species?
Line 159-165: Here, the in-text citations switched to the Vancouver style (and they don’t match any items in the References section). Please be consistent.
Reply by Cédric Sueur and co-authors: (reponses inserted into review marked by “AUTHORS”)
This is a well-written manuscript providing a descriptive account of a seldom reported behavior that has the potential to improve our understanding of mixed-species associations. Even though the functional interpretations of this behavior are speculative, I have no issues with them being cautiously laid out here, as I agree with the authors that this list could drive further research on the topic, with the goal to test some of these hypothetical functions (if any… see below my point about this). For these reasons, I think it should be published.
AUTHORS: We would like to thank you one more time to the time you devoted to review our paper and your comments.
However, there are two major points that I would like the authors to address in a possibly revised version of their manuscript. In short, I am sold about (1) the following statement “We categorised this rare behaviour as a case of reproductive interference” (Line 14-15), and (2) the argument that these few observed cases are the result of some form of behavioural “propagation” (title of the manuscript, but also throughout the text) that may be underlain by “social transmission” (Line 18, Line 141, Line 189-221). The authors should provide further evidence to convince me about the validity of these two claims.
AUTHORS: We changed and added paragraphs to better answer your comments:
“The observation of interspecies sexual behavior between Japanese macaques and Sika deer has revealed complex interactions that point to both cognitive capabilities and the potential for social transmission of behaviors. The objective here is to clarify the differences between the cognitive processes implied by these behaviors and the hypothesis regarding social transmission (Whiten 2000; Hoppitt and Laland 2013; Duboscq et al. 2016). Regarding cognitive capacities and behavioral innovation, the initial sightings in 2015 suggested a novel aspect of macaque behavior, although it is unlikely to be the first occurrence of this innovation given the absence of systematic, long-term data collection and similar behaviors observed in other populations. However, this was the first documented instance, as other colleagues regularly present in the field had never previously observed it.. These innovations illustrate the macaques’ ability to adapt and innovate by exploring mating opportunities outside their species, an indicator of behavioral flexibility and curiosity (Vancatova 2008; Aplin et al. 2015). Additionally, the guarding behavior observed may reflect a level of understanding in managing competition for mates. This guarding may serve not only as a reproductive strategy but also as a way to protect the deer as a social or play-related resource rather than as a direct mating partner (Vasey 2004; Gunst et al. 2018). The different responses observed in female macaques engaging in reproductive interference with male deer also raise intriguing questions about their ability to discern between potential mating partners. This behavior implies that some level of cognitive processing may be influencing their decision-making processes in these interactions (De Petrillo and Rosati 2021).
To fully understand the learning mechanisms underlying this behavior, additional data would be required on several fronts, as noted by reviewers. First, establishing the timing of behavior innovation and duration within the group is critical; although we noted the first recorded occurrence in 2015, this likely does not reflect the initial appearance of deer mounting. Second, without continuous monitoring, it remains unclear if other individuals practiced this behavior prior to the second observation, when females were noted engaging in deer mounting. We therefore lack data on the original innovator of the behavior and the potential pathways of social transmission within the group, if any. It is equally plausible that all members began engaging in this behavior independently, with no social learning involved. To rigorously assess the role of social learning, controlled experimental data would be essential, ideally involving naïve individuals exposed to social stimuli in a controlled setting. These experiments would require testing individuals confirmed to be naïve to deer mounting and systematically introducing the behavior to discern the mechanisms behind its emergence. Given that this behavior has also been observed in a separate group of macaques (Gunst et al., 2018), a simpler assumption may be that complex social learning mechanisms are not required for this behavior to manifest; rather, exposure to the stimulus—in this case, the deer—may be sufficient for its appearance.”
First, how do you define “reproductive interference” (Line 144-145 provides a citation but not a definition), and how does this definition matches the reported behavioural observations? Without this extra explanation, the following claim sounds highly speculative: “The fact that female macaques have reproductive interference with male deer […]” (Line 201) and should be removed from the manuscript.
AUTHORS: We added this paragraph: “They define reproductive interference as any interspecific interaction occurring during mate acquisition that detrimentally impacts the fitness of at least one species involved, resulting from incomplete species recognition. They categorize reproductive interference into seven distinct types: signal jamming, heterospecific rivalry, misdirected courtship, heterospecific mating attempts, erroneous female choice, heterospecific mating, and hybridization. However, the likelihood that Japanese macaques misrecognize sika deer as conspecifics is minimal. This improbability is underscored by the long-term coexistence and frequent interactions these two species share on Yakushima Island. Instead, the observed interspecies interactions, including sexual behaviors, likely emerge from the close proximity and the complex, reciprocal interspecies dynamics that have developed, rather than from errors in species recognition.”
Second, while I praise the authors for their attempt to build an argument for a so-called “propagation” of the behaviour that would be scaffolded by some kind of social transmission process in the face of very little and sparse empirical behavioural evidence (Line 204-221)… I am sorry to say that I don’t think this case is strong enough, when considering the data set presented here.
AUTHORS: We labelled our research as note and toned down speculation about propagation.
We added this paragraph: “To fully understand the learning mechanisms underlying this behavior, additional data would be required on several fronts, as noted by reviewers. First, establishing the timing of behavior innovation and duration within the group is critical; although we noted the first recorded occurrence in 2015, this likely does not reflect the initial appearance of deer mounting. Second, without continuous monitoring, it remains unclear if other individuals practiced this behavior prior to the second observation, when females were noted engaging in deer mounting. We therefore lack data on the original innovator of the behavior and the potential pathways of social transmission within the group, if any. It is equally plausible that all members began engaging in this behavior independently, with no social learning involved. To rigorously assess the role of social learning, controlled experimental data would be essential, ideally involving naïve individuals exposed to social stimuli in a controlled setting. These experiments would require testing individuals confirmed to be naïve to deer mounting and systematically introducing the behavior to discern the mechanisms behind its emergence. Given that this behavior has also been observed in a separate group of macaques (Gunst et al., 2018), a simpler assumption may be that complex social learning mechanisms are not required for this behavior to manifest; rather, exposure to the stimulus—in this case, the deer—may be sufficient for its appearance.
Would it be possible to get more information about the beginning of the behaviour? Or even better: evaluate approximately when it may have started and whether the male whose behaviour is extensively described could have been the “inventor” of it (i.e., no reports or no observations of a similar case in this population before, despite significant research effort)? Finally, would it be possible collect more data on the social connections between performers of the behaviour and get a clearer pattern of behavioural contagion (in terms of timing of performance: let’s say a case of multiple monkeys performing the behaviour in the same area and within a short time window on a given day)? This would convince me that there might be some social influences going on.
AUTHORS: We added a figure with a timeline and a map (figure 2).
Again, some of the presented evidence clearly indicates that the behaviour is not idiosyncratic and that it persists over time. However, I believe a stronger case should be made for a publication in a journal whose main scope is grounded in cultural phenomena. Currently, the methodological approach used to present the data is not systematic/consistent and largely based on anecdotal evidence. Specifically, we cannot rule out the probability that the acquisition and performance of this behaviour has been the result of independent motivational processes rather than “social transmission” (as acknowledged by the authors: Line 216). Therefore, it is my impression that the case for “social transmission”, which is one of the main angles of the current manuscript, is very weak.
AUTHORS: We toned down our speculation and added the paragraph indicated above.
Additional and minor points:
Line 72-73: (Pelé et al. 2017) — What is the point of this in-text citation in this specific context?
AUTHORS: We removed it.
Line 130-132: The sexual behaviour of females is not looking like the ones displayed with males but the ones displayed during homosexual behaviours. — What do you mean here? Do female Japanese macaques display homosexual behaviours among each other? In this population/geographic area? Has this been reported? If so, could you please cite your sources and explain what makes you argue about such behavioural similarities between what you observed and what may have been reported?
AUTHORS: We replaced with: “The sexual behavior displayed by female macaques toward male deer differs from the typical mating behaviors observed with male macaques, as the pelvic movements are slower, less rhythmic, and lack the thrusting intensity usually seen in heterosexual interactions. Instead, these movements resemble the slower pelvic motions often observed in female-female homosexual interactions among macaques.”
Line 16-17 and Line 143-168: In addition to this list of possible functions for this intriguing behaviour, would it be possible to acknowledge that it may be selectively neutral, have no fitness benefits of its own, but simply be a behavioural by-product of other (potentially adaptive) interactions between these two species?
AUTHORS: Done
Line 159-165: Here, the in-text citations switched to the Vancouver style (and they don’t match any items in the References section). Please be consistent.
AUTHORS: Done.