How can we apply decision-making theories to wild animal behavior? Predictions arising from dual process theory and Bayesian decision theory.

Our understanding of decision-making processes and cognitive biases is ever increasing, thanks to an accumulation of testable models and a large body of research over the last several decades. The vast majority of this work has been done in humans and laboratory animals because these study subjects and situations allow for tightly controlled experiments. However, it raises questions about how this knowledge can be applied to wild animals in their complex environments. Here, we review two prominent decision-making theories, dual process theory and Bayesian decision theory, to assess the similarities in these approaches and consider how they may apply to wild animals living in heterogenous environments within complicated social groupings. In particular, we wanted to assess when wild animals are likely to respond to a situation with a quick heuristic decision and when they are likely to spend more time and energy on the decision-making process. Based on the literature and evidence from our multi-destination routing experiments on primates, we find that individuals are likely to make quick, heuristic decisions when they encounter routine situations, or signals/cues that accurately predict a certain outcome, or easy problems that experience or evolutionary history has prepared them for. Conversely, effortful decision-making is likely in novel or surprising situations, when signals and cues have unpredictable or uncertain relationships to an outcome, and when problems are computationally complex. Though if problems are overly complex, satisficing via heuristics is likely, to avoid costly mental effort. We present hypotheses for how animals with different socio-ecologies may have to distribute their cognitive effort. Finally, we examine the conservation implications and potential cognitive overload for animals experiencing increasingly novel situations caused by current human-induced rapid environmental change.

Monkeys who experience more feeding competition utilize social information to learn foraging skills faster.

Animals must learn foraging skills to successfully survive and reproduce but the sources of interindividual variation in learning are poorly understood. For example, there is little consensus on the role motivation plays, even though it is a key factor impacting learning outcomes in humans. Here, we conduct a field experiment on a wild primate to investigate whether an individual's vulnerability to feeding competition impacts their motivation to learn a beneficial foraging technique. We provided a group of monkeys with a food reward (i.e., a half banana) that needed to be retrieved from a box. The monkeys discovered an efficient technique that consistently allowed them to retrieve the banana quickly, decreasing the risk of food loss to competitors. We found that individuals who frequently experienced feeding competition learned this efficient technique significantly faster than individuals who rarely foraged in the presence of a dominant competitor. They appeared to use social learning to learn faster as they were more attentive to the handling techniques others used and improved their foraging skills after opportunities to observe a skilled demonstrator. These findings support that an individual's vulnerability to feeding competition impacts their motivation to learn foraging skills that reduce food loss to competitors.

Temporal patterns in the social network of core units in Rwenzori Angolan colobus monkeys: Effects of food availability and interunit dispersal.

Multi-level societies are complex, nested social systems where basic social groups (i.e., core units) associate in a hierarchical manner, allowing animals to adjust their group sizes in response to variables such as food availability, predation, or conspecific threat. These pressures fluctuate over time and examining the extent to which this variation affects the clustering of core units into different tiers may be instrumental in understanding the evolution of multi-level societies.The goal of our study was to determine the degree of temporal variability in interunit associations in a multi-level society of Rwenzori Angolan colobus monkey (Colobus angolensis ruwenzorii), and to determine the social and ecological factors that underlie association patterns. The C. a. ruwenzorii multi-level society consists of at least three tiers, with core units clustering into clans that share a home range in a band tier.We performed social network analyses on 21 months of association data from 13 core units (totaling 139 identifiable individuals) at Lake Nabugabo, Uganda. We described the patterns of variation in core-unit associations over time and investigated how changes in rainfall, food availability, and interunit dispersals were correlated with these associations over the short-term (month to month) and long-term (year to year).Although clans were relatively stable, larger-scale changes in association patterns included the formation of an all-male unit and the transfer of one core unit between clans (within the band tier). Seasonally, core units associated significantly more when fruit, their preferred food source, was abundant (i.e., social networks were denser and more clustered) and there was no direct effect of rainfall seasonality or young leaf availability. Male dispersals also occurred more during periods of high fruit availability, suggesting that greater band cohesion allowed males to prospect and transfer between core units. Once males transferred, their previous and new units associated significantly more with one another than with other core units for 1-2 months postdispersal. The dispersal of five males from one core unit to another in a different clan co-occurred with this core unit switching its clan affiliation.By examining temporal shifts in social network structure among core units, this study shows the interconnected roles that food availability and dispersal have in shaping the C. a. ruwenzorii multi-level social system. Our findings highlight how ecological conditions can drive association patterns, impact interunit relationships, and influence social organization.

Diet and Activity Budget in Colobus angolensis ruwenzorii at Nabugabo, Uganda: Are They Energy Maximizers?

INTRODUCTION: Colobine monkeys are specialized folivores that use foregut fermentation to digest leaves. The slow process of fermentation forces them to spend a lot of time resting and to minimize their energy expenditure to subsist on a lower-quality diet. METHODS: We recorded the diet and activity budget of Colobus angolensis ruwenzorii, which form a three-tiered multi-level society, at Lake Nabugabo, Uganda, over 12 months using scan sampling on adults and subadults, to determine whether they utilize the energy minimization strategy typical of colobines. RESULTS: We found that the annual diet was primarily comprised of high-quality food resources (young leaves 65% and fruit 31%), and fruits were the only plant part the monkeysselected when available. Both the fruits and young leaves of some species were preferred food items in some months, and mature leaf consumption correlated negatively with preferred food availability. Mature leaves appear to be a fallback food for this population but are rarely relied upon (3%). The C. a. ruwenzoriiat Nabugabo spent less time resting (40%) and more time moving (25%) than is typical for other species of black-and-white colobus. DISCUSSION/CONCLUSION: The high-quality diet of this population appears to allow them to utilize an energy maximization strategy. Their reliance on food items that tend to be clumped in space and time likely explains the frequent fission-fusion behaviour that we observe between core units. Our findings demonstrate that the foraging strategies of colobines may be more flexible than was previously thought and illustrate how food availability and distribution can impact primate social organization.

Male monkeys use punishment and coercion to de-escalate costly intergroup fights.

In numerous social species, males direct aggression towards female group members during intergroup fights, and this behaviour is commonly thought to function as mate guarding, even though males often target non-receptive females. In studying intergroup fights in a wild population of vervet monkeys, we found that male intragroup aggression was primarily directed towards individuals who had either just finished exhibiting, or were currently attempting to instigate intergroup aggression. Targeted females were less likely to instigate intergroup aggression in the future, indicating that male intragroup aggression functioned as coercion (when directed towards those who were currently trying to instigate a fight) and punishment (when directed towards those who had recently fought). These manipulative tactics effectively prevented intergroup encounters from escalating into fights and often de-escalated ongoing conflicts. Males who were likely sires were those most likely to use punishment/coercion, particularly when they were wounded, and, therefore, less able to protect vulnerable offspring should a risky intergroup fight erupt. This work, along with our previous finding that females use punishment and rewards to recruit males into participating in intergroup fights, highlights the inherent conflict of interest that exists between the sexes, as well as the role that social incentives can play in resolving this conflict. Furthermore, unlike other studies which have found punishment to be used asymmetrically between partners, these works represent a novel example of reciprocal punishment in a non-human animal.

Proximity and grooming patterns reveal opposite-sex bonding in Rwenzori Angolan colobus monkeys (Colobus angolensis ruwenzorii).

Close proximity and social grooming are important bonding mechanisms in primates. These behaviors show the social structure of a species and many studies have found positive correlations between the degree of kinship and grooming and proximity. We used 1 year of data collected via instantaneous scan sampling on a large "supertroop" of Colobus angolensis ruwenzorii at Lake Nabugabo, Uganda, to examine partner preferences for grooming and nearest neighbors in each age-sex class. Little is known about this species, so we based our hypotheses on congeners. Of the five species of black-and-white colobus, data on sex-biased dispersal patterns are available for three (C. guereza, C. vellerosus, and C. polykomos), all of which show male-biased dispersal with occasional female dispersal. We thus predicted that female C. a. ruwenzorii would be more strongly bonded than males, showing greater proximity and grooming. We did not expect bonding between the sexes since congeners do not show this pattern. We found that among adult dyads, males and females were more likely to be found in loose proximity, and to groom, than would be expected given group composition. Conversely, both males and females had relatively weak same-sex relationships. Between the sexes, adult males had higher proximity and grooming indices with adult females without infants than with females with infants. These observations indicate that this subspecies is cross-bonded and that both sexes may disperse. Furthermore, our findings suggest that the social organization and social structure of C. a. ruwenzorii differ greatly from other black-and-white colobus species.

Male food defence as a by-product of intersexual cooperation in a non-human primate.

Males in a number of group-living species fight in intergroup conflicts to defend access to food resources, a seemingly paradoxical behaviour, given that this resource does not usually limit male fitness directly. We investigated the mechanism(s) driving apparent male food defence in wild vervet monkeys (Chlorocebus aethiops pygerythrus) by testing the effect that female resource access, and female audience size and activity had on the response of focal males during simulated intergroup encounters. Males do not appear to defend food to increase the reproductive success of female group members because their response was not influenced by the presence of provisioning boxes that only females could access. Female audience size was also unimportant, suggesting males do not participate in intergroup encounters to advertise their quality to potential mates. However, focal males almost always followed/supported female group members who initiated an approach towards simulated intruders, supporting that male participation largely functions to gain status as a cooperative group member, and that apparent male food defence in this species arises as a by-product of intersexual cooperation. Our study highlights that considering audience composition and activity can reveal the presence of social incentives and illuminate the evolutionary mechanism(s) promoting joint action in intergroup aggression.