Tyler R. Bonnell

Are Primates Ecosystem Engineers

Animals can play important roles in structuring the plant communities in which they live. Some species are particularly influential in that they modify the physical environment by changing, maintaining, and/or creating new habitats; the term ecosystem engineer has been used to describe such species. We here assess the two major foraging strategies of primates, frugivory and folivory, in terms of the potential for primates to function as ecosystem engineers. We argue that whereas the role of primates as seed dispersers has received a great deal of attention, the potential role that folivorous primates play in structuring their environment through herbivory has received much less attention. Further, while quantifying if frugivorous primates are ecosystem engineers through their seed dispersal has proved very difficult, it is not as difficult to ascertain whether folivorous primates are ecosystem engineers. We document situations in which folivorous primates act as ecosystem engineers by 1) eating the leaves and/or bark of trees to the extent that they kill trees, 2) feeding on trees to the degree that they slow their growth relative to nonpreferred tree species, 3) eating the flowers of species to the extent that it does not set fruit, or 4) feeding on plants in such a way as to increase their productivity and abundance. Because evidence from the literature is very limited, where possible we present new evidence of these processes from the colobus monkeys at our long-term field site in Kibale National Park, Uganda. We conclude by discussing promising research programs that could be established to refine our understanding of the role primates play in shaping the structure of plant communities, especially tropical forests.

Competing pressures on populations: long-term dynamics of food availability, food quality, disease, stress and animal abundance

Despite strong links between sociality and fitness that ultimately affect the size of animal populations, the particular social and ecological factors that lead to endangerment are not well understood. Here, we synthesize approximately 25 years of data and present new analyses that highlight dynamics in forest composition, food availability, the nutritional quality of food, disease, physiological stress and population size of endangered folivorous red colobus monkeys (Procolobus rufomitratus). There is a decline in the quality of leaves 15 and 30 years following two previous studies in an undisturbed area of forest. The consumption of a low-quality diet in one month was associated with higher glucocorticoid levels in the subsequent month and stress levels in groups living in degraded forest fragments where diet was poor was more than twice those in forest groups. In contrast, forest composition has changed and when red colobus food availability was weighted by the protein-to-fibre ratio, which we have shown positively predicts folivore biomass, there was an increase in the availability of high-quality trees. Despite these changing social and ecological factors, the abundance of red colobus has remained stable, possibly through a combination of increasing group size and behavioural flexibility.

Increasing Group Size Alters Behavior of a Folivorous Primate

Group size influences many aspects of mammalian social life, including stress levels, disease transmission, reproductive rates, and behavior. However, much of what is known about the effects of group size on behavioral ecology has come from comparisons across multiple groups of different sizes. These findings may be biased because behavioral differences across groups may be more indicative of how environmental variation influences animal behavior, rather than group size itself. To partially circumvent this limitation, we used longitudinal data to examine how changes in group size across time affect the behavior of folivorous red colobus monkeys (Procolobus rufomitratus) of Kibale National Park, Uganda. Controlling for food availability, we demonstrated that increasing group size resulted in altered activity budgets, based on 6 yr of data on a group that increased from 57 to 98 members. Specifically, as group size increased, individuals spent less time feeding and socializing, more time traveling, and increased the diversity of their diet. These changes appear to allow the monkeys to compensate for greater scramble competition apparent at larger group sizes, as increasing group size did not show the predicted relationship with lower female fecundity. Our results support recent findings documenting feeding competition in folivorous primates. Our results also document behavioral flexibility, an important trait that allows many social mammals to maximize the benefits of sociality (e.g., increased vigilance), while minimizing the costs (e.g., increased feeding competition).

Is Markhamia lutea's abundance determined by animal foraging?

Understanding the determinants of tropical forest tree richness and spatial distribution is a central goal of forest ecology; however, the role of herbivorous mammals has received little attention. Here we explore the potential for red colobus monkeys (Procolobus rufomitratus) to influence the abundance of Markhamia lutea trees in a tropical forest by feeding extensively on the trees flowers, such that this tree population is not able to regularly set fruit. Using 14 years of data from Kibale National Park, Uganda, we quantify M. lutea flower and fruit production. Similarly, using 21 years of data, we quantify temporal changes in the abundance of stems in size classes from 1 m tall and above. Our analyses demonstrate that M. lutea is rarely able to produce fruit and that this corresponds to a general decline in its abundance across all size classes. Moreover, using 7 years of feeding records, we demonstrate that red colobus feed on M. lutea, consuming large amounts of leaf and flower buds whenever they were available, suggesting that this behavior limits fruit production. Therefore, we suggest that red colobus are presently important for structuring the distribution and abundance of M. lutea in Kibale. This dynamic raises the intriguing question of how a large M. lutea population was able to originally establish. There is no evidence of a change in red colobus population size; however, if this old-growth forest is in a non-equilibrium state, M. lutea may have become established when red colobus ate a different diet.

Emergent group level navigation: An agent-based evaluation of movement patterns in a folivorous primate

The foraging activity of many organisms reveal strategic movement patterns, showing efficient use of spatially distributed resources. The underlying mechanisms behind these movement patterns, such as the use of spatial memory, are topics of considerable debate. To augment existing evidence of spatial memory use in primates, we generated movement patterns from simulated primate agents with simple sensory and behavioral capabilities. We developed agents representing various hypotheses of memory use, and compared the movement patterns of simulated groups to those of an observed group of red colobus monkeys (Procolobus rufomitratus), testing for: the effects of memory type (Euclidian or landmark based), amount of memory retention, and the effects of social rules in making foraging choices at the scale of the group (independent or leader led). Our results indicate that red colobus movement patterns fit best with simulated groups that have landmark based memory and a follow the leader foraging strategy. Comparisons between simulated agents revealed that social rules had the greatest impact on a group’s step length, whereas the type of memory had the highest impact on a group’s path tortuosity and cohesion. Using simulation studies as experimental trials to test theories of spatial memory use allows the development of insight into the behavioral mechanisms behind animal movement, developing case-specific results, as well as general results informing how changes to perception and behavior influence movement patterns.

Male endocrine response to seasonally varying environmental and social factors in a neotropical primate, Cebus capucinus

OBJECTIVE Circannual variation in reproduction is pervasive in birds and mammals. In primates, breeding seasonality is variable, with seasonal birth peaks occurring even in year-round breeders. Environmental seasonality is reportedly an important contributor to the observed variation in reproductive seasonality. Given that food availability is the primary factor constraining female reproduction, predictions concerning responsiveness to environmental seasonality focus on females, with studies of males focusing primarily on social factors. We examined the influence of both environmental and social factors on male fecal testosterone (fT) and glucocorticoids (fGC) in moderately seasonally breeding white-faced capuchin monkeys (Cebus capucinus) in Costa Rica. METHODS Over 17 months, we collected 993 fecal samples from 14 males in three groups. We used LMM to simultaneously examine the relative effects of photoperiod, fruit biomass, rainfall, temperature, female reproductive status (i.e., number of periovulatory periods, POPs), and male age and dominance rank on monthly fT and fGC levels. RESULTS Male age and rank had large effects on fT and fGC. Additionally, some hormone variation was explained by environmental factors: photoperiod in the previous month (i.e., lagged photoperiod) was the best environmental predictor of monthly fT levels, whereas fGC levels were best explained by lagged photoperiod, fruit biomass, and rainfall. POPs predicted monthly fT and fGC, but this effect was reduced when all variables were considered simultaneously, possibly because lagged photoperiod and POP were highly correlated. CONCLUSIONS Males may use photoperiod as a cue predicting circannual trends in the temporal distribution of fertile females, while also fine-tuning short-term hormone increases to the actual presence of ovulatory females, which may occur at any time during the year.

Analysing small-scale aggregation in animal visits in space and time: the ST-BBD method

Movement behaviour plays an important role in many ecological interactions. As animals move through the environment, they generate movement patterns, which are a combined result of landscape characteristics and species-specific behaviour. Measuring these ranging patterns is being facilitated by technological advances in collection methods, such as GPS collars, that are capturing movement on finer spatial and temporal scales. We propose the use of a novel spatiotemporal analytical framework (ST-BBD), based on the beta-binomial distribution (BBD) model, to measure small-scale aggregation in animal movement data sets, including two simulated and three collected primate data sets. We use this approach to distinguish different habitat uses of three primate species (red colobus, Procolobus rufomitratus , black howler, Alouatta pigra , and spider monkey, Ateles geoffroyi ) and quantify their specific use of the landscape in space and in time, using a parameter of the BBD that measures the variation in sites visited on a landscape. We found that estimates of aggregation in habitat use were higher in the frugivorous spider monkey, compared to the more folivorous howler monkey, and that in the red colobus, aggregation in site visits was dependent on group size and food availability. Applications of this framework to animal movement data could be useful in understanding ecological systems where habitat use is an important factor, such as the relationships between hosts and parasites, or parent plants and seed dispersers.

Interaction between scale and scheduling choices in simulations of spatial agents

ABSTRACT Spatial simulations are a valuable tool in understanding dynamic spatial processes. In developing these simulations, it is often required to make decisions about how to represent features in the environment and how events unfold in time. These spatial and temporal choices have been shown to significantly alter model outcomes, yet their interaction is less well understood. In this paper, we make use of a simple group foraging model and systematically vary how features are represented (cell size of the landscape) as well as how events unfold in time (order in which foragers take action) to better understand their interaction. Our results show similar nonlinear responses to changes in spatial representation found in the literature, and an effect of the order in which agents were processed. There was also a clear interaction between how features are represented and how events unfold in time, where, under certain environmental representations results were found to be more sensitive to the order in which individuals were processed. Furthermore, the effects of feature representation, scheduling of agents, and their interaction were all found to be influenced by the heterogeneity of the spatial surface (food), suggesting that the statistical properties of the underlying spatial variable will additionally play a role. We suggest that navigating these interactions can be facilitated through a better understanding of how these choices affect the decision landscape(s) on which agents operate. Specifically, how changes to representation affect aggregation and resolution of the decision surface, and thereby the degree to which agents interact directly or indirectly. We suggest that the challenges of dealing with spatial representation, scheduling, and their interaction, while building models could also present an opportunity. As explicitly including alternate representations and scheduling choices during model selection can aid in identifying optimal agent–environment representations. Potentially leading to improved insights into the relationships between spatial processes and the environments in which they occur.

Selection to outsmart the germs : the evolution of disease recognition and social cognition

The emergence of providing care to diseased conspecifics must have been a turning point during the evolution of hominin sociality. On a population level, care may have minimized the costs of socially transmitted diseases at a time of increasing social complexity, although individual care-givers probably incurred increased transmission risks. We propose that care-giving likely originated within kin networks, where the costs may have been balanced by fitness increases obtained through caring for ill kin. We test a novel hypothesis of hominin cognitive evolution in which disease may have selected for the cognitive ability to recognize when a conspecific is infected. Because diseases may produce symptoms that are likely detectable via the perceptual-cognitive pathways integral to social cognition, we suggest that disease recognition and social cognition may have evolved together. Using agent-based modeling, we test 1) under what conditions disease can select for increasing disease recognition and care-giving among kin, 2) whether providing care produces greater selection for cognition than an avoidance strategy, and 3) whether care-giving alters the progression of the disease through the population. The greatest selection was produced by diseases with lower risks to the care-giver and prevalences low enough not to disrupt the kin networks. When care-giving and avoidance strategies were compared, only care-giving reduced the severity of the disease outbreaks and subsequent population crashes. The greatest selection for increased cognitive abilities occurred early in the model runs when the outbreaks and population crashes were most severe. Therefore, over the course of human evolution, repeated introductions of novel diseases into naïve populations could have produced sustained selection for increased disease recognition and care-giving behavior, leading to the evolution of increased cognition, social complexity, and, eventually, medical care in humans. Finally, we lay out predictions derived from our disease recognition hypothesis that we encourage paleoanthropologists, bioarchaeologists, primatologists, and paleogeneticists to test.

Functional Social Structure in Baboons: Modelling Interactions Between Social and Environmental Structure in Group-Level Foraging

In mobile social groups, cohesion is thought to be driven by patterns of attraction at both the individual and group level. In long-lived species with high group stability and repeated interactions, such as baboons, individual-to-individual attractions have the potential to play a large role in group cohesion and overall movement patterns. In previous work, we used GPS mapping of a group of baboons in De Hoop, Western Cape, South Africa, to demonstrate the influence of such attractions on movement patterns. We also demonstrated the existence of emergent group-level structures, which arose as a consequence of individual social influence. Specifically, we found a core-periphery structure, in which a subset of influential animals exerted an influence on each other and those animals in the periphery, while those in the periphery were influenced by the core but did not exert any influence over others. Here, we use agent-based modelling of baboon groups to investigate whether this group-level structure has any functional consequences for foraging behaviour. By varying individual level attractions, we produced baboon groups that contained influence structures that varied from more to less centralized. Our results suggest that varying centrality affects both the ability of the group to detect resource structure in the environment, as well as the ability of the group to exploit these resources. Our models predict that foraging groups with more centralized social structures will show a reduction in detection and an increase in exploitation of resources in their environment, and will produce more extreme foraging outcomes. More generally, our results highlight the link between social and environmental structure on functional outcomes for mobile social groups of animals.