Audience Effects in Sooty Mangabey Agonistic Behaviour

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Audience Effects in Sooty Mangabey Agonistic Behaviour

https://doi.org/10.21203/rs.3.rs-1836808/v2

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Aggression is a major behavioural mechanism for animals engaged in competitive interactions, such as when trying to repel predators, access resources or pursue other self-serving interests. However, aggression also has a secondary function as a partner control mechanism to coerce others into cooperation and tolerance. Both functions are available to higher-ranking individuals interacting with lower-ranking opponents, which raises the question of how lower-ranking individuals achieve their goals. Here, we investigated how free-ranging sooty mangabeys, a socially tolerant forest dwelling primate, used aggression during competitive interactions inside and outside food patches, in front of uninvolved bystanders. As predicted, subjects used aggression to displace lower-ranking competitors from food, but we also found two audience effects. First, individuals generally refrained from severe aggression in front of friends and small audiences and, second, mild aggression was significantly augmented in front of high-ranking audiences, often accompanied by vocalisations. We discuss these patterns of audience-dependent aggressive behaviour and conclude that, while mangabeys do seem to pursue immediate foraging goals, they are also capable of adjusting levels of aggression for social benefits when observed by socially relevant audiences, possibly to enhance the likelihood of future tolerance.

aggression

Cercocebus atys

audience effects

rank

cooperation

reciprocity

Social animals operate in webs of interdependencies with other group members that act both as competitors and as social assets. The social asset is mainly in terms of obtaining support when conflicts arise, for instance with predators, group members or other groups. However, supporting others does not come naturally between non-relatives but requires a baseline of trust and a sense of interdependence. It is therefore unsurprising that animals seek out higher-ranking group members as preferred social partners [1], presumably because of their clout during conflicts and their ability to control access to resources. As mentioned, obtaining the support of unrelated others requires proactive behavioural strategies that foster a favourable attitude, for instance with grooming or sharing food. This is likely to increase the chances of receiving help in moments of need and, if such patterns occur, they are usually interpreted as positive reciprocity governed by some sort of bookkeeping [2] But social tolerance can also be obtained in the opposite way, that is, by threatening to lower a partner’s fitness with aggression, so-called negative reciprocity [3,4]. For this to work individuals must use aggression in ways that ‘educate’ others to opt for tolerance in future interactions.

Interestingly, in social species individuals sometimes behave aggressively in the absence of obvious conflicts, suggesting that they simply try to establish their social position and secure future tolerance [5]. But, more typically, aggression is more of a punitive nature, used in competitive contexts against individuals that refuse to cooperate, for instance, by preventing access to a resource [3]. The key difference to competitive aggression is that, in this situation, the aggressor is not defending a resource but uses aggression to prevent another’s pursuit of selfish goals [6]. Here, aggression functions a partner control mechanism by increasing the costs of selfish behaviour therefore rendering the cooperative alternative as the more economical solution, a pattern termed ‘negative reciprocity’ in the cooperation literature [7].

In some species, punitive aggression can also be directed at third parties, a form of policing. Adult male chimpanzees, for example, can intervene in ongoing conflicts in a pacifying role [8,9]. Victims of aggression appear to be aware of the fact, by data showing that they occasionally exaggerate their screams in the presence of high-ranking audiences capable of intervention [10]. Tonkean macaques and other monkey species have also been seen to intervene in conflicts between others, although usually only in support of their own kin or friends [11]. Both chimpanzees and sooty mangabeys interfere in ongoing grooming interactions of others, presumably if the resulting relation has a negative impact on them [12].

More generally, such data show that primates are capable of monitoring the relations of others, as demonstrated by multiple studies on audience effects. Importantly, audience effects are by no means restricted to the primate order but have been reported across the animal kingdom. For instance, cichlid fish androgen levels change by simply watching other fishes fighting [13], dominant male red-bellied wood peckers reduce their aggressive displays towards competitors and increase social vocalisations as soon as a female arrives [14], and male fiddler crabs are more aggressive to intruders if they have witnessed aggressive signalling interactions before [15]. These and many other studies have shown that animals are generally affected by their audiences, but this is often limited to simple features, such as age/sex classes or behavioural displays. Humans evidently go beyond such basic features and take into account the interaction history and knowledge share with their audiences, which raises questions about primate cognitive evolution [16].

The focus of this study is on whether primates use aggressive behaviour as a pre-emptive measure to impact on potentially non-cooperative group members. To address this, we investigated whether sooty mangabeys, a highly social and generally tolerant forest monkey, showed signs of awareness of the fact that uninvolved bystanders may take notice of ongoing aggressive behaviours and that this may have consequences. Displaying aggression in front of others is informative insofar as it displays an individual’s aggressive propensities and fighting ability [17,18,19], a useful strategy especially for lower-ranking individuals that otherwise struggle in escalated conflicts. Being aggressive towards less powerful adversaries in front of more powerful adversaries may thus function as a preventive advertisement strategy to lower chances of being aggressed in the future.

Sooty mangabeys are mainly terrestrial and live in groups of up to 100 individuals, with large group spread and inter-individual distances. One consequence of this social system is that individuals only interact with a small proportion of the group at any given time. Although mangabey groups do not fission, individuals spend much of their time foraging in small parties through the forest leaf-litter in search of insects and plant matter, such as the fallen fruits of Anthonota spp., Saccoglotis gabonensis and Dialium spp. [20,21,22]. Although the species has generally low levels of aggression, conflicts can occur in and outside of food patches, during which individuals produce grunts, twitters, growls and screams [23,24]. Prior studies on sooty mangabey aggression were mainly conducted in captivity, involving the introduction of new group members and formation of new groups [6,25], situations that are unsuitable to test evolutionary questions about the function of behaviour.

To address the role and relative importance of competitive and retaliatory aggression we conducted a field study on a well habituated sooty mangabey group during which we monitored natural agonistic interactions between group members in front of different audiences. For competitive aggression, we predicted individuals to be more aggressive inside than outside food patches, along the established dominance relations. For retaliatory aggression, we predicted that, if mangabeys were concerned about being attacked by bystanders, higher-ranking audiences should have inhibiting effects on aggression, whereas social allies in the audience should have the opposite effect. However, if mangabeys are to advertise their aggressive potential to bystanders, then we predicted the opposite patterns, i.e., aggressive behaviour in front of higher-ranking audiences but not in front of social allies.

Study Site and Subjects

The study was conducted in Taï National Park in South-western Ivory Coast (5°50’N, 7°21’ W). The park is the largest remaining major block of primary forest in West Africa and covers approximately 454,000 ha of continuous forest. With a mean annual temperature of 24°C, a mean annual rainfall of 1,875 mm (average of 2012–2015; Taï Monkey Project long term data) and a distinct dry season in December–January, the forest is classified as ‘tropical moist’ [26]. The study area of about 7 km² was situated near the western border of the park, approximately 20 km southeast of the township Taï. The study group’s home range contained a 2-km² core area where groups of several monkey species had been studied since 1991 as part of a long-term research project [27]. The study group had been under constant observation since 1997 and was well habituated to human observers [20,24,28]. Data collection was during group follows from dawn to dusk over a period of 20 months (92 days) during different periods: August 2013 to July 2014 and January to September 2015. During the study period the group size was around 80 individuals.

Observational data

Data collection was in the form of focal animal and instantaneous sampling [29] on N=33 adult individuals (5 males and 28 females). Subjects were identified by physical features, such as scars, body size and shape. Focal samples were 1 hour long and individuals were not sampled twice during the same day. A total of 371 hours of focal sampling was carried out on all individuals. Observer ID was entered into the analyses as a fixed factor. During focal animal sampling, data collection included details of all social interactions. These data were also used for establishing the dominance hierarchy through ‘Elo-Rating’ [30]. Social bonds between the individuals were calculated through DSI (Dyadic Composite Sociality Index) [31], using the following behaviours as variables: ‘approach’, ‘inspection’, ‘presenting groom’, ‘contact’, ‘groom’, ‘handle baby’ and ‘hug’. For vocal behaviour, we focused on direct, close-range social interactions, when one individual approached another individual to less than 1m [see 25, 20, 28, for detailed description of social interactions], assuming that, in these situations, any call produced was socially directed. Every 15 minutes we collected an instantaneous sample, which also included information on the general activity of the focal individual. Call discrimination was based on the classification scheme of Range & Fischer [23]. Data were always collected by at least two observers following one-month training with the help of local field assistants.

Statistical Analyses

We recorded every social interaction that the focal animal had with every other member of the group. Whenever a social interaction occurred, we scored whether the interaction was agonistic or not (binary, hereafter: agonistic). As predictor variables we included whether the approaching individual produced a call (binary, hereafter ‘approacher call’), whether the approached individual produced a call (binary, here after ‘approachee call’) (individuals not necessarily vocalise when encountering others), the sex of the individual (binary, hereafter ‘sex’), whether or not the focal animal was inside a food patch (binary, hereafter ‘patch’; we used the same definitions of patches as F. Range [20], the number of audience members within 10m (numeric, hereafter ‘neighbours’), whether the focal animal was foraging or not (Binary: hereafter ‘forage’), the social status of the focal individual (determined by its Elo-rating score; numeric, hereafter ‘ranking’; [30]), whether the encountered individual was in or out of sight from the focal individual for more than 20s before the encounter (binary, hereafter ‘sight’), the presence of a bond partner in the audience (binary ‘friend’; defined by a DSI score >1; [31]), the presence of a high-ranking individual in the audience (binary, hereafter ‘HR’; defined by a neighbour’s Elo-rating score above 200 over the subject’s own score [30] and whether aggression was mild or severe (binary, hereafter ‘severe’). Severe aggression was defined as an individual having chased or having had a physical contact during aggression; mild aggression was defined as an individual having threated another by staring or growling at it but without chasing or physical contact (Mild=0, Severe=1). Finally, we scored whether aggression was from a higher towards a lower-ranking individual (binary, hereafter ‘LR’).

We explored the role of these factors during each encounter in two separate models, i.e., for (1) all aggression (GLMM) and (2) severe aggression only (Zero Inflated GLMM). For the first model, the response variable was ‘agonistic’, with all aggressive encounters during focal follows serving as data points. For the second model, the response variable was ‘severe’, with only severe aggressive encounter serving as data points.

Overall probability of aggression

We used generalized linear mixed models with a binomial error structure to test variation in aggressive interactions. All factors mentioned before were used, except for ‘severe’ and ‘LR’. The response variable was ‘agonistic’. We decided to include the interaction terms between ‘ranking’ and ‘neighbours’ with all the other variables, as they were most likely to influence aggression during encounters. We included random intercepts for focal subject ID. We then built an ‘informed null model’, which comprised all fixed terms except the main predictors. The random structure was identical to the full model. We then compared these models with a likelihood ratio test [32]. If the comparison between full and null model revealed a significant difference, we explored the full model with regards to the predictors of interest, i.e., those in the full but not in the null model.

Probability of severe aggression

We used zero-inflated generalized linear mixed models with a binomial error structure to assess the variation in severe aggression. All the factors mentioned before were used, except for ‘agonistic’. The response variable was ‘severe’. We explored interactions between all factors both automatically and manually. Since no interaction was significant, we kept the initial model as the main model. We tested the significance of this model with a likelihood ratio test between the full and a null model, as mentioned above.

For the analyses we used R v4.0.3 [33] with ‘lme4’ package [34] for the GLMMs, and the ‘glmmTMB’ package [35] for the Zero Inflated GLMMs, respectively.

Ethical note

We used non-invasive data collection by simply observing individuals habituated to humans in their natural habitat. Individuals were identified by physical features, such as scars, body size and shape. Research permission and ethical clearance were granted by the Ministère de la Recherche Scientifique et Technique de Côte d’Ivoire. The methods were in line with the Animal Behaviour Society Guidelines for the Use of Animals in Research.

Overall probability of aggression

We analysed N= 419 encounters collected from 30 individuals in 72 days of observations to determine the main factors influencing aggression rates. The full model was significantly different from the null model (^χ2 = 41.272 df = 16, p = 0.0005). We removed all interaction terms, as they were not significant to set up the final model (Table 1).

As predicted by the competitive aggression hypothesis, we found that sooty mangabeys were more likely to display agonistic behaviours when they were higher-ranking than their targets (beta ± SE = 3.09 ± 1.14 p = 0.007; Table 1), when inside rather than outside a food patch (beta ± SE = 1.79 ± 0.54 p = 0.0008; Table 1), when the target was already in sight before the encounter (>20s; beta ± SE = 1.491 ± 0.425 p = 0.0004; Table 1, Fig. 1) and when the target itself was inside a food patch (beta ± SE = 0.021 ± 0.51 p = 0.0219; Table 1). Finally, subjects were more likely to call when being aggressive rather than non-aggressive (beta ± SE = 1.52 ± 0.44 p = 0.0006; Table 1).

As predicted by retaliatory (audience-dependent) aggression hypothesis, subjects were more likely to be aggressive when a higher-ranking individual was present in the audience within 10m than not (beta ± SE = 0.021 ± 0.51 p = 0.0219; Table 1, Fig. 2).

Table 1. Model results for overall probability of aggression

Variables

Estimate

Pr(>|z|)

Competition hypothesis

Encounter inside food patch

Aggressor rank

Victim in sight

Audience hypothesis

Aggressor sex

1.7595

3.2985

1.2427

2.1168

0.5458

1.2439

0.4304

1.6909

3.224

2.652

3.310

1.252

<0.002

<0.009

<0.001

>0.2

Audience size

Aggressor calls

Friend in audience

Victim calls

High-ranker in audience

0.2315

1.4052

-0.6681

0.2987

1.3869

0.2123

0.4578

0.4509

0.5336

0.5400

1.090

3.070

-1.484

0.560

2.568

>0.2

<0.003

>0.1

>0.5

<0.011

We analysed N= 128 encounters collected from 26 individuals in 72 days to determine the main factors influencing the severity of aggression. The full model was significantly different from the null model (^χ2 = 15.496 df = 7, p = 0.03). We found that individuals were more likely to show severely aggressive behaviours when outside than inside a food patch (beta ± SE = -0.95 ± 0.5 p = 0.058; Table 2, Fig. 3) with increasing audience sizes (beta ± SE = 0.58 ± 0.21 p = 0.008; Table 2, Fig. 4) and when no social allies were in the audience (beta ± SE = -0.95 ± 0.5 p = 0.058; Table 2, Fig. 5).

Table 2. Model results for the probability of severe aggression only

Variables

Estimate

Pr(>|z|)

Competition hypothesis

Encounter inside a food patch

Aggressor rank

Victim in sight

Aggressor sex

Audience hypothesis

-1.8430

0.2130

-0.2939

-0.2404

0.7643

0.2154

0.4305

0.4177

-2.411

0.989

-0.683

-0.575

<0.016

0.32275

0.49482

0.56500

Aggressor calls

Victim calls

High-ranked in audience

Aggressor is higher-ranking than victim

Friend in audience

Audience size

0.7799

0.5715

-0.3704

0.5538

-0.9561

0.5805

0.4357

0.5590

0.4692

0.4803

0.5063

0.2199

1.790

1.022

-0.789

1.153

-1.888

2.640

0.07349

0.30663

0.42987

0.24890

0.059

0.009

We were interested in the patterns of sooty mangabey aggressive behaviour to address a basic question in animal behaviour, the degree to which aggression is used to enforce future cooperative behaviour or tolerance in others. Aggression is certainly essential during competition over resources, but it can further function more generally as a partner control mechanism, to keep others from pursuing their selfish goals and instead opt for cooperative alternatives. We restricted our study to the feeding context since physical proximity in food patches is particularly prone to aggression, where animals have to decide between tolerated co-feeding or active displacement, if they have the means to do so.

As expected, we found that mainly higher-ranking individuals opted for aggressive behaviours inside food patches. However, we also found a secondary effect that could not be explained with basic resource competition. In particular, aggression was more likely when high-ranking individuals were within 10m and, remarkably, the aggressor vocalised in most of these encounters with grunts, growls or screams. It is less likely that this secondary effect was an attempt to recruit other group members to jointly attack the opponent. In many cases, the aggressors already outranked their victims, suggesting that recruiting higher-ranking bystanders would not bring additional benefits but result in additional costs due to feeding competition or other unwanted side-effects. We also found that the sudden arrival of out-of-sight individuals in the food patch did not increase the likelihood of aggression. Instead, individuals were more likely to be aggressive to those already in sight, implying some planning rather than impulsive reactions.

The key audience effect we report here, i.e., being overly aggressive in the presence of high-ranking bystanders, might be a tactic to increase future tolerance from them, similar to redirected aggression, which is thought to reduce a victim’s probability of being the object of further aggression [36]. This hypothesis, however, needs to be tested with future studies that take into account long-term effects of agonistic encounters beyond dyadic contests.

Severe aggression was positively related to audience size, especially when no friends were in the audience, suggesting that aggressors were aware that they could not expect any support in the ongoing conflict. Severe aggression, remarkably, was rarely observed inside food patches, suggesting that competitors specifically avoided it in this context. Pursuing selfish goals at all costs, in other words, was actively avoided, even by individuals that would have had the means to do so. Severe aggression occurred mainly outside food patches, suggesting functions other than competition over food.

These data suggest that the presence of friends in the audience has a pacifying role, at least regarding severe aggression, while high-ranking audiences have the opposite effect. We did not assess the proportion of severe aggression that started as mild aggression, and future research should investigate whether decisions about aggression are not only taken dyadically but include assessments of whether receiving help from audience members is likely, as reported for chimpanzees [10].

We also noted the absence of a number of predicted effects. Most importantly and against predictions, the presence of friends did not influence the overall occurrence of aggressive behaviour. In many species of primates, friends support each other during conflicts [37,38], suggesting that individuals might have felt empowered by the presence of friends. Male chimpanzees at Ngogo community in Uganda showed evidence of reciprocity in grooming and support [39], a finding also reported from captivity [40]. In vervet monkeys, there is evidence that closely ranked females have higher rates of grooming and are more likely to support each other during agonistic encounters against lower-ranking individuals [2,41] and there is similar evidence for other monkey species [42], including sooty mangabeys [20].

Also, we found no interaction effect between friendship and rank, against the prediction that low-ranking individuals were more likely to be aggressive when friends were near. For severe aggression, the presence of friends mattered, but in the opposite direction, i.e., severe aggression occurred mainly when they were absent. Regarding audience size, we initially predicted that an increasing number of group members make it more likely to recruit support during conflicts, but again we found no such evidence. However, outside food patches severe aggression was more common with large audiences, consistent with the idea that aggressors might seize the opportunity to display their willingness to escalate, whenever they were watched by many.

Aggression as a partner control mechanism

According to theory, cooperation can be enforced by what has been called ‘direct reciprocity’, which can be either positive or negative (“I help you, so you help me” vs. “I aggress you, so you help me”). In both cases, the relevant interactions are not just in the here-and-now but socially embedded in the relationship history, with endowments that can be reciprocated. This requires partners to keep track of past events in some ways, so that they can reciprocate positively by helping or negatively by increasing the costs for not cooperating. Social bonds (‘friendships’) are often good predictors of cooperation (e.g., ‘first-order alliances’ in dolphins), and are mediated psychologically by the trust and tolerance that emanates from them. The notion of ‘friendship’ in animals is still debated, especially because ‘true’ friendship should involve some sort of reciprocity, which require a tracking or accounting mechanism beyond the predictions of basic tolerance and proximity. Whether such book-keeping takes place in animals has remained unclear and is an ongoing topic of research. In our data, we also found the presence of friends (as measured in terms of DSI), but not high ranking group members, in the audience was linked with lower levels of severe aggression, suggesting that individuals took into account the potential impact of their behaviour on others.

Regarding negative direct reciprocity an interesting example is a study by Hauser [43] who claimed that rhesus macaques that failed to produce food calls when encountering food attracted aggression [43,44]. This is in line with the interpretation that aggression occurred as a result of individuals’ decision to refrain from a cooperative behaviour, but the finding will have to be replicated. In chimpanzees, food calls are also produced regularly when individuals find food and in response to others’ arriving at food trees, particularly if they are high-ranking or aggressively motivated [45,46]. Although this is in line with a negative direct reciprocity interpretation, we are not aware of evidence showing that individuals are targeted with aggression if they fail to call when finding food. Although retaliatory aggression is theoretically plausible as an enforcement strategy and driver of cooperation in non-related animals, research is needed to investigate the role of this mechanism in natural situations.

Partner control can also be in terms of indirect reciprocity, provided social interactions take place in front of audiences that can observe and remember content and outcome of social interactions. This will allow observers to classify group members as either mainly ‘cooperative’ or mainly ‘selfish’ [47], a form of reputation. Here again, a distinction has been made between positive and negative indirect reciprocity. Negative indirect reciprocity seems to be important in the function of human societies, by keeping antisocially behaving individuals under control by third-party punishment or ‘policing’ [48], a behaviour also reported in monkeys and apes [9,49]. Whether or not policing in primates is equivalent to what is seen in humans, i.e., impartial interventions by bystanders, is uncertain. For primates, it is possible that policing is done for selfish reasons to maintain social instability, without any human-like community concern or group-mindedness [50], in which case it might be better classified as (non-enforced) direct reciprocity.

There is an ongoing debate on whether reputation is actually a relevant factor in animal social behaviour, with effectively two mechanisms that could be in place, ‘image scoring’ [51] or ‘standing judgments’ [52,53]. In image scoring each helpful/selfish act adds or removes a point to the co-operator’s image. In standing judgments as scoring is partner-dependent, such that helping a co-operator raises an individual’s standing as much as failing to help a selfish individual [54]. Chimpanzees appear to assess each other in terms of cooperative motivation, but mainly from direct reciprocity experiences, but by observing others (indirect reciprocity, [55]. Whether or not the audience effect we found for mangabey aggression behaviour is related as a form or precursor of negative indirect reciprocity would have to be addressed with future research.

One aim of our study was to address the possibility that primates use aggression as a behavioural mechanism for negative (direct) reciprocity. Although some of our findings were consistent with this hypothesis we did not find any strong evidence beyond audience-dependent use of aggression. To better address the problem, future studies should look at the long-term effects of aggressive interactions, especially those that cannot be explained in terms of dyadic conflicts over access to resources. Predictions are that individuals that have aggressed others without direct resource competitions, should be more likely to obtain tolerance or cooperation in future interactions, regardless of whether they are competitive or otherwise. Also, they should be more likely to receive aggression from dominant individuals present when they were engaging in aggression.

In sum, our data have shown that the nature and composition of the audience are determinant factors on both the origins and the outcomes of aggressive behaviours and some patterns are in line with the notion of negative reciprocity.

AUTHORS' CONTRIBUTIONS

FQ and KZ: study design; ST, MM and FQ: data collection; FQ: statistical analysis; FQ and KZ: interpretation and drafting the article; KZ: provision of necessary tools and resources. All authors read and approved the final manuscript.

COMPETING INTERESTS

The authors declare no competing interests.

DATA AVALAIBILITY

The raw data used in the analyses in this study are available in the following link:

https://doi.org/10.6084/m9.figshare.20380347

ACKNOWLEDGMENTS

The research has been funded by the Swiss National Science Foundation (310030_143359), the Swiss National Centre of Competence in Research ‘Evolving Language’ (#51NF40 180888). We thank the Centre Suisse de Recherches Scientifiques (CSRS), the Ministère de la Recherche Scientifique, the Ministère de l’Agriculture et des Ressources Animales and the Office Ivoirien des Parcs et Réserves (OIPR) of Côte d’Ivoire for support and permission to conduct research in the Taï National Park. We thank the staff of the C.R.E. research station in Taï for logistical support. Paterson Kalo, Richard Peho, Benjamin Zehi and Gerard Gha assisted data collection. We thank Anderson Bitty for logistic support and Radu Slobodeanu for statistical advice.

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Audience Effects in Sooty Mangabey Agonistic Behaviour

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