Michael D. Wasserman

Determinants of colobine monkey abundance: the importance of food energy, protein and fibre content

A fundamental ecological question is what determines the abundance of animals? Answering this question is vital in the formulation of effective management plans for endangered or threatened species. However, there are few general hypotheses proposed to account for variation in animal abundance. Studies of folivorous primates are a notable exception. In this group, the protein to fibre ratio of mature leaves is a significant predictor of biomass. However, Dasilva (1992) suggested that the availability of energy may play a critical role in colobine behaviour and ecology. Here we evaluate the importance of food energy content for the red colobus (Procolobus badius) and black-and-white colobus (Colobus guereza) monkeys of Kibale National Park, Uganda. Energy was found to be of little importance. None of the eight groups studied selected high-energy foods: there was no correlation between food energy content and foraging effort. For all groups, estimates of energy expenditure [daily energy expenditure (DEE) and average daily metabolic needs (ADMN)] were less than estimates of energy consumption. Finally, the average energy content of mature leaves from the 20 most abundant tree species at four sites was not related to colobine biomass. In contrast, the protein and fibre content of foods was important to both colobine species. Seven of the eight groups selected foods with a high-protein, low-fibre content. The average protein to fibre ratio of mature leaves from the 20 most abundant tree species at four sites was correlated positively with colobine biomass. This study provides further validation of the protein to fibre model, suggesting the importance of this model for conservation and management of colobus monkeys, with the potential application to other small mammalian herbivores.

Bigger groups have fewer parasites and similar cortisol levels: a multi-group analysis in red colobus monkeys.

If stress and disease impose fitness costs, and if those costs vary as a function of group size, then stress and disease should exert selection pressures on group size. We assessed the relationships between group size, stress, and parasite infections across nine groups of red colobus monkeys (Procolobus rufomitratus) in Kibale National Park, Uganda. We used fecal cortisol as a measure of physiological stress and examined fecal samples to assess the prevalence and intensity of gastrointestinal helminth infections. We also examined the effect of behaviors that could potentially reduce parasite transmission (e.g., increasing group spread and reducing social interactions). We found that cortisol was not significantly related to group size, but parasite prevalence was negatively related to group size and group spread. The observed increase in group spread could have reduced the rate of parasite transmission in larger groups; however, it is not clear whether this was a density‐dependent behavioral counter‐strategy to infection or a response to food competition that also reduced parasite transmission. The results do not support the suggestion that gastrointestinal parasitism or stress directly imposed group‐size‐related fitness costs, and we cannot conclude that they are among the mechanisms limiting group size in red colobus monkeys. Am. J. Primatol. 70:1072–1080, 2008.

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.

Measuring physical traits of primates remotely: the use of parallel lasers

Physical traits, such as body size, and processes like growth can be used as indices of primate health and can add to our understanding of life history and behavior. Accurately measuring physical traits in the wild can be challenging because capture is difficult, disrupts animals, and may cause injury. To measure physical traits of arboreal primates remotely, we adapted a parallel laser technique that has been used with terrestrial and marine mammals. Two parallel lasers separated by a known distance (4 cm) and mounted onto a digital camera are projected onto an animal. When a photograph is taken, the laser projections on the target provide a scale bar. We validated the technique for measuring the physical traits of identifiable red colobus monkeys (Procolobus rufomitratus) in Kibale National Park, Uganda. First, we photographed the tails of monkeys with laser projections and compared these with measurements previously obtained when the animals were captured. Second, we manually measured the distance between two markers placed on tree branches at similar heights to those used by monkeys, and compared them with the measurements obtained through digital photographs of the markers with parallel laser projections. The mean tail length of the monkeys via manual measurements was 63.3±4.4 cm, and via remote measurements was 63.0±4.1 cm. The mean distance between the markers on tree branches via manual measurements was 13.8±3.59 cm, and via remote measurements was 13.9±3.58 cm. The mean error using parallel lasers was 1.7% in both cases. Although the needed precision will depend on the question asked, our results suggest that sufficiently precise measurements of physical traits or substrates of arboreal primates can be obtained remotely using parallel lasers. Am. J. Primatol. 70:1191–1195, 2008.

Going, Going, Gone: A 15-Year History of the Decline of Primates in Forest Fragments near Kibale National Park, Uganda

Given accelerating trends of deforestation and human population growth, immediate and innovative solutions to conserve biodiversity are sorely needed. Between 1995 and 2010, we regularly monitored the population size and structure of colobus monkey populations in the forest fragments outside of Kibale National Park, Uganda. Through this monitoring we assessed the monkeys’ gastrointestinal parasites and fecal cortisol levels. Over 15 years, we documented a rapid decline in the number of fragments that supported primates, largely as a result of tree removal. Fecal cortisol levels of primates found in the fragments were consistently higher than in populations found in the continuous forest of the national park. The fragment populations also harbored gastrointestinal parasites rarely found in the main forest and exchanged bacteria with nearby people and livestock at high rates, suggesting that fragmentation facilitates disease transmission. Fragments supported the fuelwood needs of an average of 32 people living immediately adjacent to the fragment, and partially supported families up to three farms away (~400 m, representing 576 people). Intensive fuelwood harvesting occurred when neighboring households engaged in brewing beer (an average of 9.6 % of the households), distilling gin (8.8 %), or producing charcoal (14.5 %). Our data suggest that the future of small and unprotected forest fragments is bleak; a scenario that is unfortunately typical outside protected areas in many tropical regions.

Estrogenic plant consumption predicts red colobus monkey (Procolobus rufomitratus) hormonal state and behavior

Numerous studies have examined the effects of anthropogenic endocrine disrupting compounds; however, very little is known about the effects of naturally occurring plant-produced estrogenic compounds (i.e., phytoestrogens) on vertebrates. To examine the seasonal pattern of phytoestrogen consumption and its relationship to hormone levels (407 fecal samples analyzed for estradiol and cortisol) and social behavior (aggression, mating, and grooming) in a primate, we conducted an 11-month field study of red colobus (Procolobus rufomitratus) in Kibale National Park, Uganda. The percent of diet from estrogenic plants averaged 10.7% (n=45 weeks; range: 0.7-32.4%). Red colobus fed more heavily on estrogenic Millettia dura young leaves during weeks of higher rainfall, and the consumption of this estrogenic item was positively correlated to both their fecal estradiol and cortisol levels. Social behaviors were related to estradiol and cortisol levels, as well as the consumption of estrogenic plants and rainfall. The more the red colobus consumed estrogenic plants the higher their rates of aggression and copulation and the lower their time spent grooming. Our results suggest that the consumption of estrogenic plants has important implications for primate health and fitness through interactions with the endocrine system and changes in hormone levels and social behaviors.

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).

Primates in Fragments 10 Years Later: Once and Future Goals

In 2010, the Food and Agriculture Organization of the United Nations (FAO) estimated that 16 million hectares of forest per year were lost globally in the 1990s (FAO 2010), and approximately 12.5 million hectares/year were lost in countries with primate populations, an area just smaller than Greece or the US State of Mississippi (Chapman and Peres 2001; Chapman and Gogarten 2012). In contrast, in the last decade (2000–2010), the rate of deforestation has decreased globally by approximately 5.2 million hectares/year, and reforestation and natural expansion of forests in some countries significantly reduced the net loss of forest (FAO 2010). This may be in part due to the lack of resonance in satellite imagery between secondary and primary forest regions, particularly in the tropics. Unfortunately, the increase in forested lands has principally affected temperate regions of Europe and eastern Asia (e.g., China, Japan), but deforestation of most tropical forests has continued steadily (e.g., annual loss: 0.5 % in Africa, 1.2 % in Mesoamerica, 0.5 % in South America, 0.4 % in southeastern Asia; FAO 2011).

Estrogenic plant foods of red colobus monkeys and mountain gorillas in uganda

Phytoestrogens, or naturally occurring estrogen-mimicking compounds, are found in many human plant foods, such as soybeans (Glycine max) and other legumes. Because the consumption of phytoestrogens may result in both health benefits of protecting against estrogen-dependent cancers and reproductive costs of disrupting the developing endocrine system, considerable biomedical research has been focused on the physiological and behavioral effects of these compounds. Despite this interest, little is known about the occurrence of phytoestrogens in the diets of wild primates, nor their likely evolutionary importance. We investigated the prevalence of estrogenic plant foods in the diets of two folivorous primate species, the red colobus monkey (Procolobus rufomitratus) of Kibale National Park and mountain gorilla (Gorilla beringei) of Bwindi Impenetrable National Park, both in Uganda. To examine plant foods for estrogenic activity, we screened 44 plant items (species and part) comprising 78.4% of the diet of red colobus monkeys and 53 plant items comprising 85.2% of the diet of mountain gorillas using transient transfection assays. At least 10.6% of the red colobus diet and 8.8% of the gorilla diet had estrogenic activity. This was mainly the result of the red colobus eating three estrogenic staple foods and the gorillas eating one estrogenic staple food. All estrogenic plants exhibited estrogen receptor (ER) subtype selectivity, as their phytoestrogens activated ERβ, but not ERα. These results demonstrate that estrogenic plant foods are routinely consumed by two folivorous primate species. Phytoestrogens in the wild plant foods of these two species and many other wild primates may have important implications for understanding primate reproductive ecology.

Physiological and Behavioral Effects of Capture Darting on Red Colobus Monkeys (Procolobus rufomitratus) with a Comparison to Chimpanzee (Pan troglodytes) Predation

Understanding how human activities affect wild primates is critical to the design of effective conservation strategies. Despite this need, few studies have examined the physiological and behavioral effects of field research methods in the wild. Here, we examine how the stress response, i.e., fecal cortisol, and behavior of Ugandan red colobus monkeys (Procolobus rufomitratus) in Kibale National Park are affected by chemical immobilization and collaring, i.e., capture. We compare this anthropogenic stressor to a naturally occurring stressor: a chimpanzee (Pan troglodytes) predation attack. Two adult males had peak cortisol levels of 283 and 284 ng/g 2–3 d after capture, which were 190% and 182% above their baseline levels, i.e., the first sample taken immediately after capture, but these peak levels did not remain elevated. Using long-term data, i.e., 11 mo of data, we found no difference in fecal cortisol levels between 10 darted and collared individuals and 14 individuals living in the same social group that were not darted or collared. For the chimpanzee attack, peak fecal cortisol levels (147–211% above baseline) were recorded 1–4 d after the attack, but these levels also did not remain elevated for long. These data show that darting and collaring and a chimpanzee predation attempt caused an acute stress response, but neither leads to sustained elevated cortisol levels. Thus, in situations in which research contributes significantly to the conservation of primates and cannot be conducted noninvasively, capture darting appears to be a useful technique with minimal long-term effects as long as injury and mortality are avoided. However, we encourage researchers to make similar physiological and behavioral comparisons in other field studies using similar techniques to provide a better understanding of the effects of research practices on the stress physiology and social behavior of wild primates.