Dr Julie Teichroeb started a new research site near Lake Nabugabo in Uganda. This site is home to a subspecies of colobus that very little was known about, Colobus angolensis ruwenzorii. We have started putting together the puzzle pieces to understand the basic social organization and social structure of this subspecies, as well as how these are impacted by their ecology.

Lake Nabugabo field site in Uganda

Aren’t colobus folivores?

Colobines are a group of monkeys that have evolved complex, multi-chambered stomachs (much like a cow or other ruminant) to help them digest a diet that largely consists of leaves. Because leaves, and mature leaves in particular, are low in energy and high in toxic compounds, most colobines need to spend a lot of time resting so that they can digest their low-quality forage and conserve energy.

In examining the diet of the Nabugabo population, we found that their diet consists of 31% fruit, 65% young leaves, and only 3% mature leaves (Arseneau-Robar et al. 2020 Folia Primatologica). They were highly selective for fruits and ate them at any time of year that they were available (see below). These are levels of fruigivory that are quite unique among the African colobines. When we examined specific foods that were preferred vs avoided, we found that this population has access to preferred food resources all year round. Thus, it appears that the colobus at Lake Nabugabo have access to abundant, high-quality food resources that allow them to maintain a high-quality diet of fruits and young leaves.

(b) Food availability index scores for the different plant parts consumed. (c) The monthly diet of Colobus angolensis ruwenzorii near Lake Nabugabo, Uganda.

When we looked at their activity budgets, they spent 40% of their time resting, 25% moving, 28% feeding and 7% of their time socializing (Arseneau-Robar et al. 2020 Folia Primatologica). They maintained a fairly consistent activity budget throughout the year (see below). Most other colobines populations spend at least 50% of their time resting, so the low levels of forced resting-time in this population suggest that their high-quality diet allows them to employ an energy maximization strategy, similar to most frugivorous primate species.

Monthly activity budget for Colobus angolensis ruwenzorii near Lake Nabugabo

Other work by Dr Teichroeb and Sam Stead has shown that this population lives in a large, multi-level society (Stead and Teichroeb 2019 PLOS One) in which core units associated preferentially into clans, and clans into bands. Core units in this population spend a lot of time in close association with one or more other core units, and so are often found in large aggregations. And we are currently investigating the extent to which their high-quality diet, and particularly the availability of fruit, enables these large aggregations to form (Frances Adams et al., In Preparation).

Why don’t other African colobines form such large groups?

There are other subspecies/populations of Colobus angolensis that have been studies and not all of them form large groups. While having access to a high-quality diet likely enables large aggregations to form, observations of very small groups in this species suggests that diet is not the only important factor regulating group size. Perhaps their social structure (i.e. who forms close relationships with who) also plays a role?

We investigated social relationships among different age-sex classes in the Colobus angolensis ruwenzorii living at Lake Nabugabo (Arseneau-Robar et al. 2017 Primates). After examining association and grooming patterns, we found that adult males tended to have the strongest relationships with adult females, but also spent a considerable amount of time grooming with other males. These high levels of tolerance amongst adult males are atypical in other species of colobus, and may be key to producing the high levels of inter-unit tolerance that are necessary for large aggregations to form. These high levels of male-male tolerance may arise because dispersal in this population seems to be female biased (Stead and Teichroeb 2019 PLOS One). While males typically disperse out of their natal core unit, they do not tend to leave their band; conversely, females tend to disperse outside of their band. These dispersal patterns likely cause high levels of male relatedness within bands, promoting higher levels of male-male, and therefore inter-unit tolerance.

Why are these findings so exciting?

Through much of our evolutionary history, humans are also thought to have formed multi-level societies. At the lowest level is the family unit, which is typically a monogamous male-female pair and their offspring, although some families are were polygynous. Families lived together in a camp, and these families were highly interdependent on one another as they shared food and helped each other raise offspring. Although dispersal patterns were flexible, female exogamy and marriage outside the band was common. Male patrilocality facilitates male-male bonding, and strong male bonds within camps is thought to have been critical to humans evolving our incredible propensity to hunt cooperatively and engage in cooperative intergroup violence (i.e. warfare). Because Colobus angolensis ruwenzorii also live in multi-level societies, show female exogamy and high levels of male tolerance, this species may be an excellent model to understand the pressures underlying the evolution of some key traits present in humans.


Humans are unique in the animal kingdom in the extent to which we cooperate with others. We perform multiple cooperative acts each day, help strangers we are unlikely to meet again, engage in highly dangerous activities like warfare, and we can coordinate highly effective collective actions, even in very large groups. Our prolific cooperation relies on our ability to flexibly use a number of different mechanisms to promote cooperation, and prevent defection, in any given context. Many cooperative investments are directed towards relatives and so provide inclusive fitness benefits. We reciprocally trade goods and services, form mutually beneficial social bonds, help others to maintain a good reputation or to advertise our willingness/ability to be a good cooperative partner. We behave cooperatively to receive rewards or other incentives, or because if we do not, we might be punished, fined, or sanctioned. My research asks questions like, how and why did we evolve this incredibly propensity to cooperate? Are all these mechanisms for promoting cooperation unique to humans or did some of them exist deeper in our evolutionary history? What were the selective pressures that drove the evolution of these mechanisms for cooperation?

My doctoral research on intergroup conflicts in vervet monkeys examines mechanisms that promote cooperative intergroup aggression, an evolutionary antecedent to human warfare. My ongoing research on food-for-sex exchanges in vervet monkeys will examine how the supply and demand of these two commodities impacts the bargaining power males and females each have when participating in this market. And, I am also conducting a study investigating the mechanisms driving spontaneous helping in humans. In particular, I am evaluating the role that competitive altruism plays in promoting this behaviour. That is to say, I am asking whether people use acts of kindness to signal to potential cooperation partners that they are available, willing, and able to form a mutually beneficial cooperative relationship (e.g. a friendship, relationship, or professional alliance).

Intergroup Conflicts in Vervet Monkeys

Females and males each fight in intergroup conflicts for different reasons.

High-ranking females, who stand to gain the most by defending monopolizable resources, and females without infants, who are less averse to the risks associated with fighting, are most active in intergroup conflicts. Females are primarily interested in defending access to food resources, but also defend important areas of their home range. (Arseneau-Robar et al. 2017 Animal Behaviour)

Males who are likely to have sired infants in the group are very protective, responding reactively when the other group is aggressive such that offspring might be at risk. Males often support females who are trying to instigate a fight, but they primarily do so during the mating season when doing so is associated with higher mating success. (Arseneau et al. 2015 Animal Behaviour, Arseneau-Robar et al. 2016 Scientific Reports)

Using Social Incentives to Resolve Conflicts of Interest

Conflicts of interest often arise between likely sires, who are averse to the risks intergroup conflicts pose to infants, and females, who need access to high-quality food resources to successfully produce and raise offspring.

When conflicts of interest arise, females use both punishment and rewards to obtain higher levels of male support. Females direct aggression towards males who are not participating; punished males are more likely to participate aggressively afterwards, and these increased levels of participation are higher than would be expected given each male’s baseline levels of participation in intergroup conflicts. (Arseneau-Robar et al. 2016 Proceedings of the Royal Society B)

Conversely, females preferentially groom males who have supported them in the intergroup conflict and males who receive this reward maintain their high levels of participation. The observed levels of participation after being rewarded are higher than each male’s baseline levels.

Males who are likely sires also have strategies for achieving more ideal outcomes when conflicts of interest arise. They use punishment/coercion to prevent encounters from escalating into intergroup fights that could put offspring at risk. Likely sires direct aggression towards group members who (try to) instigate a fight, and those who are punished/coerced are less likely to keep on fighting than would be expected given their baseline participation levels. Likely sires are most likely to use this strategy when they themselves are wounded, and so might feel unable to protect offspring should the need arise. (Arseneau-Robar et al. 2018 Proceedings of the Royal Society B)


Our findings highlight the heterogeneity that exists within social groups, and the consequences this heterogeneity has for the evolution of cooperation in social groups. Interindividual variability in the costs and benefits of intergroup aggression causes conflicts of interest to arise among group members. This creates selective pressure for female strategies that increase the odds of winning an intergroup conflict, and male strategies which prevent intergroup encounters from escalating into high-risk fights. Because the number of active participants, relative to the number in the opposing group, determines whether the group wins or loses, using punishment and rewards to recruit males likely improves the odds females win access to fitness-limiting resources. (Arseneau-Robar et al. 2016 Proceedings of the Royal Society B)

Conversely, male punishment/coercion was highly effective in preventing intergroup conflicts from erupting when used when the two groups were near to one another but no fighting had yet occurred. When males used punishment/coercion in the middle of an ongoing intergroup conflict, this strategy successfully ended the fight in ~50% of cases and intergroup conflicts tended to end sooner than expected. (Arseneau-Robar et al. 2018 Proceedings of the Royal Society B)