Risk-taking incentives predict aggression heuristics in female gorillas

Reviewer #1 (Public review):

Summary:

This work aims to improve our understanding of the factors that influence female-on-female aggressive interactions in gorilla social hierarchies, using 25 years of behavioural data from five wild groups of two gorilla species. Researchers analysed aggressive interactions between 31 adult females, using behavioural observations and dominance hierarchies inferred through Elo-rating methods. Aggression intensity (mild, moderate, severe) and direction (measured as the rank difference between aggressor and recipient) were used as key variables. A linear mixed-effects model was applied to evaluate how aggression direction varied with reproductive state (cycling, trimester-specific pregnancy, or lactation) and sex composition of the group. This study highlights the direction of aggressive interactions between females, with most interactions being directed from higher- to lower-ranking adult females close in social rank. However, the results show that 42% of these interactions are directed from lower- to higher-ranking females. Particularly, lactating and pregnant females targeted higher-ranking individuals, which the authors suggest might be due to higher energetic needs, which increase risk-taking in lactating and pregnant females. Sex composition within the group also influenced which individuals were targeted. The authors suggest that male presence buffers female-on-female aggression, allowing females to target higher-ranking females than themselves. In contrast, females targeted lower-ranking females than themselves in groups with a larger ratio of females, which supposes a lower risk for the females since the pool of competitors is larger. The findings provide an important insight into aggression heuristics in primate social systems and the social and individual factors that influence these interactions, providing a deeper understanding of the evolutionary pressures that shape risk-taking, dominance maintenance, and the flexibility of social strategies in group-living species.

The authors achieved their aim by demonstrating that aggression direction in female gorillas is influenced by factors such as reproductive condition and social context, and their results support the broader claim that aggression heuristics are flexible. However, some specific interpretations require further support. Despite this, the study makes a valuable contribution to the field of behavioural ecology by reframing how we think about intra-sexual competition and social rank maintenance in primates.

Strengths:

One of the study's major strengths is the use of an extensive dataset that compiles 25 years of behavioural data and 6871 aggressive interactions between 31 adult females in five social groups, which allows for a robust statistical analysis. This study uses a novel approach to the study of aggression in social groups by including factors such as the direction and intensity of aggressive interactions, which offers a comprehensive understanding of these complex social dynamics. In addition, this study incorporates ecological and physiological factors such as the reproductive state of the females and the sex composition of the group, which allows an integrative perspective on aggression within the broader context of body condition and social environment. The authors successfully integrate their results into broader evolutionary and ecological frameworks, enriching discussions around social hierarchies and risk sensitivity in primates and other animals.

Weaknesses:

Although the paper has a novel approach by studying the effect of reproductive state and social environment on female-female aggression, the use of observational data without experimental manipulation limits the ability to establish causation. The authors suggest that the difference observed in female aggression direction between groups with different sex composition might be indicative of male presence buffering aggression, which seems speculative, as no direct evidence of male intervention or support was reported. Similarly, the use of reproductive state as a proxy for energetic need is an indirect measure and does not account for actual energy expenditure or caloric intake, which weakens the authors' claims that female energetic need induces risk-taking. Overall, this paper would benefit from stronger justification and empirical support to strengthen the conclusions of the study about the mechanisms driving female aggression in gorillas.

Reviewer #2 (Public review):

Summary:

The authors' aim in this study is to assess the factors that can shift competitive incentives against higher- or lower-ranking groupmates in two gorilla species.

Strengths:

This is a relevant topic, where important insights could be gained. The authors brought together a substantial dataset: a long-term behavioral dataset representing two gorilla species from five social groups.

Weaknesses:

The authors have not fully shown the data used in the model and explored the potential of the model. Therefore, I remain cautious about the current results and conclusions.

Some specific suggestions that require attention are

(1) The authors described how group size can affect aggression patterns in some species (line 54), using a whole paragraph, but did not include it as an explanation variable in their model, despite that they stated the overall group size can "conflate opposing effects of females and males" (line 85). I suggest underlining the effects of numbers of males or/and females here and de-emphasizing the effect of group size in the Introduction.

(2) There should be more details given about how the authors calculated individual Elo-ratings (line 98). It seems that authors pooled all avoidance/displacement behaviors throughout the study period. But how often was the Elo-rating they included in the model calculated? By the day or by the month? I guess it was by the day, as they "estimate female reproductive state daily" (line 123). If so, it should be made clear in the text.

In addition, all groups were long-term studied, and the group composition seems fluctuant based on the Table 1 in Reference 11. When an individual enters/leaves the group with a stable hierarchy, it takes time before the hierarchy turns stable again. If the avoidance/displacement behaviors used for the rank relationship were not common, it would take a few days or maybe longer. Also, were the aggressive behaviors more common during rank fluctuations? In other words, if avoidance/displacement behaviors and aggressive behaviors occur simultaneously during rank fluctuations, how did the authors deal with it and take it into consideration in the analysis?

The authors emphasized several times in the text that gorillas "form highly stable hierarchical relationships". Also, in Reference 25, they found very high stabilities of each group's hierarchy. However, the number of females involved in that analysis was different from that used here. They need to provide more basic info on each group's dominance hierarchy and verify their statement. I strongly suggest that the authors display Elo-rating trajectories and necessary relevant statistics for each group throughout the study period as part of the supplementary materials.

(3) The authors stated why they differentiated the different stages based on female reproductive status. They also referred to the differences in energetic needs between stages of pregnancy and lactation (lines 127-128). However, in the mixed model, they only compared the interaction score between the female cycling stage and other stages. The model was not well explained, and the results could be expanded. I suggest conducting more pairwise comparisons in the model and presenting the statistics in the text, if there are significant results. If all three pregnancy stages differed significantly from cycling and lactating stages but not from each other, they may be merged as one pregnancy stage. More in-depth analysis would help provide better answers to the research questions.

Reviewer #3 (Public review):

Smit and Robbins' manuscript investigates the dynamics of aggression among female groupmates across five gorilla groups. The authors utilize longitudinal data to examine how reproductive state, group size, presence of males, and resource availability influence patterns of aggression and overall dominance rankings as measured by Elo scores. The findings underscore the important role of group composition and reproductive status, particularly pregnancy, in shaping dominance relationships in wild gorillas. While the study addresses a compelling and understudied topic, I have several comments and suggestions that may enhance clarity and improve the reader's experience.

(1) Clarification of longitudinal data - The manuscript states that 25 years of behavioral data were used, but this number appears unclear. Based on my calculations, the maximum duration of behavioral observation for any one group appears to be 18 years. Specifically:

• ATA: 6 years
• BIT: 8 years
• KYA: 18 years
• MUK: 6 years
• ORU: 8 years I recommend that the authors clarify how the 25-year duration was derived.

(2) Consideration of group size - The authors mention that group size was excluded from analyses to avoid conflating the opposing effects of female and male group members. While this is understandable, it may still be beneficial to explore group size effects in supplementary analyses. I suggest reporting statistics related to group size and potentially including a supplementary figure. Additionally, given that the study includes both mountain and wild gorillas, it would be helpful to examine whether any interspecies differences are apparent.

(3) Behavioral measures clarification - Lines 112-116 describe the types of aggressive behaviors observed. It would be helpful to clarify how these behaviors differ from those used to calculate Elo scores, or whether they overlap. A brief explanation would improve transparency regarding the methodology.

(4) Aggression rates versus Elo scores - The manuscript uses aggression rates rather than dominance rank (as measured by Elo scores) as the main outcome variable, but there is no explanation on why. How would the results differ if aggression rates were replaced or supplemented with Elo scores? The current justification for prioritizing aggression rates over dominance rank needs to be more clearly supported.

Author response:

Public Reviews:

Reviewer #1 (Public review):

Summary:

This work aims to improve our understanding of the factors that influence female-on-female aggressive interactions in gorilla social hierarchies, using 25 years of behavioural data from five wild groups of two gorilla species. Researchers analysed aggressive interactions between 31 adult females, using behavioural observations and dominance hierarchies inferred through Elo-rating methods. Aggression intensity (mild, moderate, severe) and direction (measured as the rank difference between aggressor and recipient) were used as key variables. A linear mixed-effects model was applied to evaluate how aggression direction varied with reproductive state (cycling, trimester-specific pregnancy, or lactation) and sex composition of the group. This study highlights the direction of aggressive interactions between females, with most interactions being directed from higher- to lower-ranking adult females close in social rank. However, the results show that 42% of these interactions are directed from lower- to higher-ranking females. Particularly, lactating and pregnant females targeted higher-ranking individuals, which the authors suggest might be due to higher energetic needs, which increase risk-taking in lactating and pregnant females. Sex composition within the group also influenced which individuals were targeted. The authors suggest that male presence buffers female-on-female aggression, allowing females to target higher-ranking females than themselves. In contrast, females targeted lower-ranking females than themselves in groups with a larger ratio of females, which supposes a lower risk for the females since the pool of competitors is larger. The findings provide an important insight into aggression heuristics in primate social systems and the social and individual factors that influence these interactions, providing a deeper understanding of the evolutionary pressures that shape risk-taking, dominance maintenance, and the flexibility of social strategies in group-living species.

The authors achieved their aim by demonstrating that aggression direction in female gorillas is influenced by factors such as reproductive condition and social context, and their results support the broader claim that aggression heuristics are flexible. However, some specific interpretations require further support. Despite this, the study makes a valuable contribution to the field of behavioural ecology by reframing how we think about intra-sexual competition and social rank maintenance in primates.

Strengths:

One of the study's major strengths is the use of an extensive dataset that compiles 25 years of behavioural data and 6871 aggressive interactions between 31 adult females in five social groups, which allows for a robust statistical analysis. This study uses a novel approach to the study of aggression in social groups by including factors such as the direction and intensity of aggressive interactions, which offers a comprehensive understanding of these complex social dynamics. In addition, this study incorporates ecological and physiological factors such as the reproductive state of the females and the sex composition of the group, which allows an integrative perspective on aggression within the broader context of body condition and social environment. The authors successfully integrate their results into broader evolutionary and ecological frameworks, enriching discussions around social hierarchies and risk sensitivity in primates and other animals.

Thank you for the positive assessment of our work and the nice summary of the manuscript!

Weaknesses:

Although the paper has a novel approach by studying the effect of reproductive state and social environment on female-female aggression, the use of observational data without experimental manipulation limits the ability to establish causation. The authors suggest that the difference observed in female aggression direction between groups with different sex composition might be indicative of male presence buffering aggression, which seems speculative, as no direct evidence of male intervention or support was reported. Similarly, the use of reproductive state as a proxy for energetic need is an indirect measure and does not account for actual energy expenditure or caloric intake, which weakens the authors' claims that female energetic need induces risk-taking. Overall, this paper would benefit from stronger justification and empirical support to strengthen the conclusions of the study about the mechanisms driving female aggression in gorillas.

We agree that experimental manipulation would allow us to extend our work. Unfortunately, this is not possible with wild, endangered gorillas.

We have now added more references (Watts 1994; Watts 1997) and enriched our arguments regarding male presence buffering aggression. Previous research suggests that male gorillas may support lower-ranking females and they may intervene in female-female conflicts (Sicotte 2002). Unfortunately, our dataset did not allow us to test for male protection. We conduct proximity scans every 10 minutes and these scans are not associated to each interaction, meaning that we cannot reliably test if proximity to a male influence the likelihood to receive aggression.

We have now clearly stated that reproductive state is an indirect proxy for energetic needs. We agree with your point about energy intake and expenditure, but unfortunately, we do not have data on energy expenditure or caloric intake to allow us to delve into more fine-grained analyses.

Overall, we have tried to enrich the justification and empirical support to strengthen our conclusions by clarifying the text and adding more examples and references.

Reviewer #2 (Public review):

Summary:

The authors' aim in this study is to assess the factors that can shift competitive incentives against higher- or lower-ranking groupmates in two gorilla species.

Strengths:

This is a relevant topic, where important insights could be gained. The authors brought together a substantial dataset: a long-term behavioral dataset representing two gorilla species from five social groups.

Weaknesses:

The authors have not fully shown the data used in the model and explored the potential of the model. Therefore, I remain cautious about the current results and conclusions.

Some specific suggestions that require attention are

(1) The authors described how group size can affect aggression patterns in some species (line 54), using a whole paragraph, but did not include it as an explanation variable in their model, despite that they stated the overall group size can "conflate opposing effects of females and males" (line 85). I suggest underlining the effects of numbers of males or/and females here and de-emphasizing the effect of group size in the Introduction.

We did not use group size as a main predictor, as has been commonly done in other species, because of potentially conflating opposing effects of males and females. To further stress this point, we have specifically added in the introduction: “group size, the overall number of individuals in the group, might not be a good predictor of aggression heuristics, as it can conflate the effects of different kinds of individuals on aggression (see Smit & Robbins 2024 for an example of opposing effects of the number of females and number of males on female gorilla aggression).”

We also “ran our analysis testing for group size (number of weaned individuals in the group), instead of the numbers of females and males, [and] its influence on interaction score was not significant (estimate=-0.001, p-value=0.682).”

(2) There should be more details given about how the authors calculated individual Elo-ratings (line 98). It seems that authors pooled all avoidance/displacement behaviors throughout the study period. But how often was the Elo-rating they included in the model calculated? By the day or by the month? I guess it was by the day, as they "estimate female reproductive state daily" (line 123). If so, it should be made clear in the text.

We rephrased accordingly: “We used all avoidance and displacement interactions throughout the study period and we used the function elo.seq from R package EloRating to infer daily individual female Elo-scores”. We also clarified that “This method takes into account the temporal sequence of interactions and updates an individual’s Elo-scores each day the individual interacted with another...”

In addition, all groups were long-term studied, and the group composition seems fluctuant based on the Table 1 in Reference 11. When an individual enters/leaves the group with a stable hierarchy, it takes time before the hierarchy turns stable again. If the avoidance/displacement behaviors used for the rank relationship were not common, it would take a few days or maybe longer. Also, were the aggressive behaviors more common during rank fluctuations? In other words, if avoidance/displacement behaviors and aggressive behaviors occur simultaneously during rank fluctuations, how did the authors deal with it and take it into consideration in the analysis?

We have shown in Reference 25 (Smit & Robbins 2025) after Reference 11 (Smit & Robbins 2024) that females form highly stable hierarchies, and that dyadic dominance relationships are not influenced by dispersal or death of third individuals. Notably, new immigrant females usually start at and remain low ranking, without large fluctuations in rank. Therefore, the presence of any fluctuation periods have limited influence in the aggressive interactions in our study system.

The authors emphasized several times in the text that gorillas "form highly stable hierarchical relationships". Also, in Reference 25, they found very high stabilities of each group's hierarchy. However, the number of females involved in that analysis was different from that used here. They need to provide more basic info on each group's dominance hierarchy and verify their statement. I strongly suggest that the authors display Elo-rating trajectories and necessary relevant statistics for each group throughout the study period as part of the supplementary materials.

In fact, the females involved in the present analysis and the analysis of Smit & Robbins 2025 are the same. Our present analysis is based on the hierarchies of Smit & Robbins 2025. Note that female gorillas disperse and occasionally immigrate to another study group. This is why some females may appear in the hierarchies of more than one group, giving the impression that there are more females involved in the analysis of Smit & Robbins 2025 (e.g. by counting the lines in the Elo-rating plots). We now specifically state that “We present these interactions and hierarchies in detail in Smit & Robbins 2025”, to clarify that the hierarchies are the same.

(3) The authors stated why they differentiated the different stages based on female reproductive status. They also referred to the differences in energetic needs between stages of pregnancy and lactation (lines 127-128). However, in the mixed model, they only compared the interaction score between the female cycling stage and other stages. The model was not well explained, and the results could be expanded. I suggest conducting more pairwise comparisons in the model and presenting the statistics in the text, if there are significant results. If all three pregnancy stages differed significantly from cycling and lactating stages but not from each other, they may be merged as one pregnancy stage. More in-depth analysis would help provide better answers to the research questions.

Thank you for pointing this out. First, when we considered one pregnancy stage, pregnant females showed indeed a significantly greater interaction score than females in other reproductive stages. We have now included that in the manuscript. However, we still find relevant to test for the different stages of pregnancy, given the difference of energetic needs in these stages. We have now included the pairwise comparisons in a new table (Table 2).

Reviewer #3 (Public review):

Smit and Robbins' manuscript investigates the dynamics of aggression among female groupmates across five gorilla groups. The authors utilize longitudinal data to examine how reproductive state, group size, presence of males, and resource availability influence patterns of aggression and overall dominance rankings as measured by Elo scores. The findings underscore the important role of group composition and reproductive status, particularly pregnancy, in shaping dominance relationships in wild gorillas. While the study addresses a compelling and understudied topic, I have several comments and suggestions that may enhance clarity and improve the reader's experience.

(1) Clarification of longitudinal data - The manuscript states that 25 years of behavioral data were used, but this number appears unclear. Based on my calculations, the maximum duration of behavioral observation for any one group appears to be 18 years. Specifically:

• ATA: 6 years

• BIT: 8 years

• KYA: 18 years

• MUK: 6 years

• ORU: 8 years

I recommend that the authors clarify how the 25-year duration was derived.

Indeed none of the five study “groups” has been studied for 25 years in a row. However, MUK emerged from a fission of group KYA in early 2016. So, from the start of group KYA in October 1998 to the end of group MUK in December 2023, there are 25 years and 2 months. We have now rephrased to “...starting in 1998 in one of the mountain gorilla groups” in the introduction, and to “We use a long-term behavioural dataset on five wild groups of the two gorilla species, starting in 1998” in the abstract.

(2) Consideration of group size - The authors mention that group size was excluded from analyses to avoid conflating the opposing effects of female and male group members. While this is understandable, it may still be beneficial to explore group size effects in supplementary analyses. I suggest reporting statistics related to group size and potentially including a supplementary figure. Additionally, given that the study includes both mountain and wild gorillas, it would be helpful to examine whether any interspecies differences are apparent.

We have now added the suggested extra test: “When we ran our analysis testing for group size (number of weaned individuals in the group), instead of the numbers of females and males, its influence on interaction score was not significant (estimate=-0.001, p-value=0.682).”

Regarding species differences: In our analysis, we test for species (mountain vs western) and we find no significant differences between the two. This is stated in the results.

(3) Behavioral measures clarification - Lines 112-116 describe the types of aggressive behaviors observed. It would be helpful to clarify how these behaviors differ from those used to calculate Elo scores, or whether they overlap. A brief explanation would improve transparency regarding the methodology.

We now added short explanations into brackets for behaviours that are not obvious. We also added a sentence in the text to clarify the difference with the behaviours used to calculate Elo scores: “These two behaviours [avoidance and displacement] are ritualized, occurring in absence of aggression, they are considered a more reliable proxy of power relationships over aggression, and they are typically used to infer gorilla hierarchical relationships”.

(4) Aggression rates versus Elo scores - The manuscript uses aggression rates rather than dominance rank (as measured by Elo scores) as the main outcome variable, but there is no explanation on why. How would the results differ if aggression rates were replaced or supplemented with Elo scores? The current justification for prioritizing aggression rates over dominance rank needs to be more clearly supported.

The sentence we added above (“These two behaviours [avoidance and displacement] are ritualized, occurring in absence of aggression, they are considered a more reliable proxy of power relationships over aggression, and they are typically used to infer gorilla hierarchical relationships”) and the first paragraph of the results hopefully clarify that ritualized agonistic interactions are generally directionally consistent and more reliably capture the highly stable dominance relationships of female gorillas. This approach has been used to calculate dominance rank in gorillas in all studies that have considered it, dating back to the 1970s (namely in studies by Harcourt and Watts). On the other hand, aggression can be context dependent (we now clearly note that in the beginning of the Methods paragraph on aggressive interactions). Therefore, we use Eloscores inferred from ritualized interactions as base and a reliable proxy of power relationships; then we test if the direction of aggression within these relationships is driven also by energetic needs or the social environment.