Interdemic variation in mixed-species association patterns: common diurnal primates of Kibale National Park, Uganda

We used interdemic variation in the tendency to form mixed-species groups to examine the costs and benefits of association among the primates of Kibale National Park, Uganda. A year-long survey of six sites revealed that the amount of time that the five common diurnal primates [red colobus (Procolobus tephrosceles), black-and-white colobus (Colobus guereza), redtail monkeys (Cercopithecus ascanius), blue monkeys (Cercopithecus mitis), and grey-cheeked mangabeys (Lophocebus albigena)] spent in mixed-species groups varied dramatically among sites. In many cases, the proportion of time that species associated was positively related to their densities. By using detailed behavioral observations of redtail monkeys and red colobus made over 4 years (2660 h) at four sites, we were able to reject the null hypothesis that associations occur by chance for only one of four sites. However, a correlative approach exploring the costs and benefits of association suggests that ecological variables do influence association patterns. We found that redtail monkeys and red colobus overlapped in diet (19.2% of their foraging effort) and traveled further when in mixed-species groups than when alone. Having demonstrated this, we examined the applicability of the ecological constraints model for predicting the proportion of the time spent in mixed-species groups based on food availability. For this analysis we concentrated on red colobus from the site with 35 months of observation and demonstrated that their tendency to be in mixed- species groups was related to food availability. We used two methods to examine if mixed-species associations function to decrease predation risk. First, chimpanzees are known to prey heavily on red colobus, but rarely kill other primates. The time red colobus spent in mixed-species groups was correlated to chimpanzee density, but it was not for the other monkey species, suggesting that mixed-species groups serve to decrease predation risk. Second, when red colobus groups contain more infants and are presumably at the greatest risk of predation, they form mixed-species groups most often. These results demonstrate that the costs and benefits of mixed-species associations vary dramatically over small spatial and temporal scales. If such variation is generally the case, then studies conducted at different locations or different times could easily highlight the importance of difference selective agents in favoring mixed-species associations. Received: 10 February 1999 / Received in revised form: 16 September 1999 / Accepted: 2 October 1999     

Predatory behavior of crowned hawk-eagles (Stephanoaetus coronatus) in Kibale National Park, Uganda

Evaluating the nature and significance of predation on populations of wild primates has been difficult given a paucity of data regarding the phenomenon. Here we addressed this problem in a 37-month study of the predatory behavior of crowned hawk-eagles living at the Ngogo study site in Kibale National Park, Uganda. We collected prey remains underneath the nests of two pairs of eagles and census data on potential prey species to investigate prey selection and the ecological impact of predation on the Ngogo primate population. Results indicate that primates form the vast majority of all prey items. Eagles prey selectively on monkeys according to sex and species. Male primates were taken more often than females, while two species, redtail monkeys and mangabeys, were captured significantly more and less, respectively, than chance expectation. In addition, there was no bias in the age of prey: adult and non-adults were killed in numbers roughly equal to their proportional representations in the forest. Further analyses indicate that a non-trivial fraction of the entire primate population at Ngogo succumbs to crowned hawk-eagle predation each year. These results reveal both parallels and contrasts with those reported previously. Some of the parallels are due to similarities in prey availability, while contrasts are likely related to methodological differences between studies, inter- individual variations in predator hunting styles, and differences in prey abundance, demography, and behavior. Received: 29 March 2000 / Revised: 6 June 2000 / Accepted: 15 October 2000     

Predation risk and the number of adult males in a primate group: a comparative test

The number of adult males in a bisexual primate group is thought to be determined mainly by the defensibility of mating access to the females. However, among primates, small groups sometimes contain several adult male. We evaluate the hypothesis that high predation risk may lead to greater male representation in primate groups, independent of the effect of group size. Male primates are known to be more vigilant than females, and may also be better at detecting potential predators. A comparative test was done using arboreal folivores in three continents, howler monkeys in the Neotropics, colobus monkeys in Africa and langurs in South and Southeast Asia. Howlers and colobus are exposed to predation by large monkey-eating eagles, whereas the langurs are not. We conducted regression analyses on group composition data of single populations and on mean group compositions among populations, and found that the arboreal langurs basically live in groups with only a single adult males whereas groups of howler and colobus monkeys of comparable size have multiple adult males (Fig. 3). Thus, the hypothesis was supported. Several alternative hypotheses do not account for this pattern.     

Behavioural responses of Diana monkeys to male long-distance calls: changes in ranging,association patterns and activity

Although much is known about the relationship between vigilance, group size and predation risk, behavioural responses to predation risk and their resultant costs are less clear. We investigated the response of Diana monkeys to increased predation risk by looking at behavioural changes associated with male long-distance calls, which are reliably given to certain predators. After male long-distance calls, group spread and nearest-neighbour distance decreased whilst travel and association rates for the group increased. The average height and exposure level of individuals in the group did not change after calls. Individual Diana monkeys changed their behaviour and were more likely to be vigilant or travel and less likely to engage in social or resting behaviours after long-distance calls. In addition, movement rates increased with the number of species the Diana monkeys were associated with. Diana monkey long-distance calls facilitate the joining of groups of other species. Black and white colobus and lesser spot-nosed monkeys were more likely to be in an association following a long-distance call than before. Behavioural responses, such as increased travel or association rates, that reduce foraging efficiency are interpreted as evidence of a non-lethal impact of increased predation risk.     

Variation in behavioral and hormonal responses of adult male gray-cheeked mangabeys (<Emphasis Type="Italic">Lophocebus albigena</Emphasis>) to crowned eagles (<Emphasis Type="Italic">Stephanoaetus coronatus</Emphasis>) in Kibale National Park,Uganda

Intensive study of arboreal forest-dwelling primates and their predators in Africa is increasingly revealing that crowned eagles (Stephanoaetus coronatus) are major predators of primates. Gray-cheeked mangabeys (Lophocebus albigena) are overrepresented in the diets of crowned eagles in Kibale National Park, Uganda, and adult male mangabeys are represented more than females. We focused on the behavior of adult male gray-cheeked mangabeys living in social groups in Kibale National Park (1) to clarify the interactions between mangabeys and eagles that might put adult males at greater risk and (2) to better understand individual variation in behavioral responses to predators. Adult male mangabeys in five groups responded to observer-confirmed presence of crowned eagles 88 times over a 13-month period. While all males gave alarm calls, only the highest-ranking male in each of four groups chased eagles. These males had elevated levels of fecal cortisol metabolites in the days immediately after they engaged in active defense, suggesting that they perceived such behavior as risky. In the one group where male ranks were unstable and there were no infants, no male was observed to chase eagles. We suggest that males pursue the dangerous tactic of chasing eagles only when they are likely to have offspring in the group. Males in larger groups also spent less time alarm calling to crowned eagles (from first to last call in a group), and our observations confirmed that the duration of their alarm calls was related to eagle presence. Thus, eagles spent less time around larger mangabey groups. Alarm calling by adult male mangabeys may signal to this ambush predator that it has been detected and should move on.     

Reproductive consequences of variation in the composition of howler monkey (Alouatta spp.) groups

At least three general categories of environmental pressure - predation, resource distribution, and demographics - shape the costs and benefits of group-living for animals. Among the demographic factors that influence individual survival and reproduction, the composition of social groups can play an important role. Census data drawn from 26 populations of howler monkeys (Alouatta spp.) were used to determine if the composition of groups explained variation in their reproductive performance. Each group's reproductive performance was estimated by calculating the difference between the observed number of immatures and the number expected from its population average. Of four group structure variables tested, only one - the residual of the adult and subadult sex ratio - was a consistent correlate of reproductive performance across the howler monkey populations. Groups with a greater proportion of adult and subadult males contained more juveniles than expected from the population average. I propose that the survival or retention of immatures within howler monkey groups depends in part on the behavior of resident males. Of particular importance, the relative proportions of resident males and females were more informative than the absolute number of males or females. On this basis, I evaluate the possible role of males in protection from predation, conspecific aggression, and resource competition. The techniques used here can also be used to forecast major changes in demographic structure within populations.     

Towards an ecological solution to the folivore paradox: patch depletion as an indicator of within-group scramble competition in red colobus monkeys (Piliocolobus tephrosceles)

A number of socioecological models assume that within-group food competition is either weak or absent among folivorous primates. This assumption is made because their food resources are presumed to be superabundant and evenly dispersed. However, recent evidence increasingly suggests that folivore group size is food-limited, that the primates prefer patchily distributed high-quality foods, and display some of the expected responses to within-group scramble competition. To investigate this apparent contradiction between theoretical models and recent empirical data, we examined the foraging behaviour of red colobus monkeys (Piliocolobus tephrosceles) in Kibale National Park, Uganda. We found that red colobus monkeys foraged in a manner that suggests they deplete patches of preferred foods: intake rate slowed significantly during patch occupancy while movement rate, an index of foraging effort, increased. Furthermore, patch occupancy was related to the size of the feeding group and the size of the patch. These results suggest that within-group scramble competition occurs, may limit folivore group size, and should be considered in models of folivore behavioural ecology.     

Anti-predation behaviour of red colobus monkeys in the presence of chimpanzees

Predator-prey interactions are usually regarded as evolutionary “arms races”, but evidence is still scarce. We examined whether the anti-predation strategies of red colobus monkeys (Procolobus badius) are adapted to the hunting strategies of chimpanzees (Pan troglodytes) in the Taï National Park, Ivory Coast. Taï chimpanzees search for red colobus groups, approach them silently and hunt co-operatively. Our playback experiments and observations of natural encounters revealed that red colobus hid higher up the trees in positions where exposure to the forest floor is minimal and became silent, when chimpanzees were close. They moved away silently through the canopy, when chimpanzees were still at some distance. However, if a group of diana monkeys was nearby in the latter situation, red colobus sought their presence even if they had to move towards the chimpanzees. Chimpanzees refrained from hunting associated red colobus groups, probably because diana monkeys are excellent sentinels for predators approaching over the forest floor. Thus several elements of both the predator's and the prey's strategies correspond to each other. Finally, we compared the interactions between the two species in Taï and in Gombe, Tanzania. We suggest that the difference in size ratio between the two species at the two sites and adaptation of hunting techniques and of escape modes to different forest structures can explain why Gombe red colobus attack chimpanzees while Taï red colobus try to escape. We conclude that predator-prey interactions can indeed lead to evolutionary arms races, with the specific form of co-adaptations depending on environmental factors.     

Predator-specific alarm calls in Campbell's monkeys, Cercopithecus campbelli

One of the most prominent behavioural features of many forest primates are the loud calls given by the adult males. Early observational studies repeatedly postulated that these calls function in intragroup spacing or intergroup avoidance. More recent field experiments with Diana monkeys (Cercopithecus diana) of Taï Forest, Ivory Coast, have clearly shown that loud male calls function as predator alarm calls because calls reliably (1) label different predator classes and (2) convey semantic information about the predator type present. Here, I test the alarm call hypothesis another primate, the Campbell's monkey (C. campbelli). Like Diana monkeys, male Campbell's monkeys produce conspicuous loud calls to crowned hawk eagles (Stephanoaetus coronatus) and leopards (Panthera pardus), two of their main predators. Playback experiments showed that monkeys responded to the predator category represented by the different playback stimuli, regardless of whether they consisted of (1) vocalisations of the actual predators (crowned hawk eagle shrieks or leopard growls), (2) alarm calls to crowned hawk eagles or leopards given by other male Campbell's monkeys or (3) alarm calls to crowned hawk eagles or leopards given by sympatric male Diana monkeys. These experiments provide further evidence that non-human primates have evolved the cognitive capacity to produce and respond to referential labels for external events.     

The Near Extinction of Two Large European Predators: Super Specialists Pay a Price

Abstract:  Despite recovery plans, the Spanish Imperial Eagle ( Aquila adalberti ) and the Iberian lynx ( Lynx pardinus ) are in danger of extinction. These two flagship species tend to occur in pristine Mediterranean forests, and both prey preferentially on the rabbit ( Oryctologus cuniculus ). Spanish lynxes and eagles have sister species in continental Europe, the Eurasian lynx (  Lynx europaeus ) and the Eastern Imperial Eagle ( A. heliaca ), respectively. Recent genetic evidence indicates that these two pairs of species started to diverge from their ancestor species slightly less than 1 million years ago, when the longest-lasting Pleistocene glaciations covered Europe. We hypothesize that the Iberian lynx and the Spanish Imperial Eagle emerged as separate species in the Pleistocene refugia of southern Spain, where they hunted yet another locally evolved species, the rabbit, on which they have become dependent for survival. Two large predators that emerged at the same time may go extinct simultaneously because of their inability to shift to alternative prey. Many other relict species, including numerous species from oceanic islands, have naturally small populations because of evolutionary constraints and are permanently threatened with extinction. Recovery plans aimed at putting these species out of danger are unrealistic, as their populations are and have been chronically scarce. We suggest that what these species need are maintenance plans designed to buffer population declines due to either stochastic or human-induced events. A metaphor for this would be "emergency care units" for conservation.     

Patterns of selective predation by juvenile,benthivorous fish on estuarine macrofauna

Benthic feeding on macrofauna was studied in juveniles of the sparids Lithognathus lithognathus and Rhabdosargus holubi in the upper reaches of the Gamtoos Estuary, South Africa. Fish and benthic macrofauna were sampled simultaneously, and the selection of invertebrate prey assessed. Both fish species strongly selected for corophioid amphipods and consumed other benthic taxa in low numbers. R. holubi also exploited aquatic autotrophs, while L. lithognathus had a narrow prey-spectrum, feeding almost exclusively on the tube-dwelling amphipod Grandidierella lignorum. G. lignorum was the most abundant prey species, both in the benthos and the fish's diet. This species also showed prominent behavioural differences between the sexes; males were markedly more active on the sediment surface than females, who rarely left their tubes during the day. Males switched from an infaunal to epifaunal microhabitat in search of receptive females, concurrently increasing their exposure to fish predators. Consequently, L. lithognathus selected significantly more males than female amphipods, causing a marked bias towards females in the sex ratio and age-structure of the amphipod population. Juvenile amphipods were less preyed upon, presumably as a result of lower prey-detection or capture efficiency by the predators. Accepting current notions about predation as an important structuring element for benthic communities, our data also stress the prominence of size-and sex-selective predation in structuring individual prey populations.     

Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups

The social organization of spider monkeys (Ateles geoffroyi) and chimpanzees (Pan troglodytes) appear remarkably similar. In this paper, field studies of these two species were used to (1) test a model of ecological constraints on animal group size which suggests that group size is a function of travel costs and (2) assess ecological and social factors underlying the social organization of these two species. Spider monkeys were studied over a 6-year period in Santa Rosa National Park, Costa Rica, and chimpanzees were studied for 6 years in Kibale National Park, Uganda. Adults of both species spent their time in small subgroups that frequently changed size and composition. Thus, unlike most primate species, spider monkeys and chimpanzees were not always in a spatially cohesive social group; each individual had the option of associating in subgroups of a different size or composition. Both species relied on ripe fruit from trees that could be depleted through their feeding activity. However, spider monkey food resources tended to occur at higher densities, were more common, less temporally variable, and did not reach the low levels experienced by chimpanzees. Analyses of the relationship between subgroup size and the density and distribution of their food resources suggested that travel costs limit subgroup size. However, these ecological factors did not influence all age/sex classes equally. For example, the number of adult males in a subgroup was a function of food density and travel costs. However, this was not the case for female chimpanzees, suggesting that the benefits of being in a subgroup for females did not exceed the costs, even when ecological conditions appeared to minimize subgroup foraging costs. Therefore, it seems likely that social strategies influenced the relationship between food resource variables and subgroup size.     

An agent-based model of red colobus resources and disease dynamics implicates key resource sites as hot spots of disease transmission

The effect of anthropogenic landscape change on disease in wildlife populations represents a growing conservation and public health concern. Red colobus monkeys (Procolobus rufomitratus), an endangered primate species, are particularly susceptible to habitat alteration and have been the focus of a great deal of disease and ecological research as a result. To infer how landscape changes can affect host and parasite dynamics, a spatially explicit agent-based model is created to simulate movement and foraging of this primate, based on a resource landscape estimated from extensive plot-derived tree population data from Kibale National Park, Uganda. Changes to this resource landscape are used to simulate effects of anthropogenic forest change. With each change in the landscape, disease outcomes within the simulated red colobus population are monitored using a hypothetical microparasite with a directly transmitted life cycle. The model predicts an optimal distribution of resources which facilitates the spread of an infectious agent through the simulated population. The density of resource rich sites and the overall heterogeneity of the landscape are important factors contributing to this spread. The characteristics of this optimal distribution are similar to those of logged sections of forest adjacent to our study area.     

Cost-free vigilance during feeding in folivorous primates? Examining the effect of predation risk,scramble competition,and infanticide threat on vigilance in ursine colobus monkeys (<Emphasis Type="Italic">Colobus vellerosus</Emphasis>)

Vigilance often decreases with increasing group size, due to lower predation risk or greater scramble competition for food. A group size effect on vigilance is seldom seen in primates, perhaps because scanning and feeding often occur simultaneously or because the distinction between routine and induced vigilance has not been investigated. We analyzed feeding and resting observations separately while distinguishing between routine and induced scans in four groups of wild ursine colobus monkeys (Colobus vellerosus) experiencing scramble competition for food and infanticide risk. We used linear mixed-effect models to test the effect of group size, age–sex class, number of neighbors, number of adult male neighbors, and height in the canopy on scanning rates (vigilance) with and without evident conspecific threat. Food type was also examined in the feeding models. Perceived predation risk affected vigilance more than scramble competition for food and infanticide risk. Routine and induced vigilance were greatest at lower canopy heights during feeding and resting and increased when individuals had fewer neighbors while resting. A group size effect was found on induced vigilance while resting, but scanning increased with group size, which probably indicates visual monitoring of conspecifics. Scanning rates decreased while feeding on foods that required extensive manipulation. This supports the idea that vigilance is relatively cost free for upright feeders when eating food that requires little manipulation, a common feature of folivore diets. In the presence of threatening conspecific males, close proximity to resident males decreased individual vigilance, demonstrating the defensive role of these males in the group.     

Extinction of a West African Red Colobus Monkey

Abstract: We provide the first documented case of the extinction in the twentieth century of a widely recognized primate taxon. During surveys in Ghana and Côte d'Ivoire in 1993–1999, we were unable to find any surviving populations of Miss Waldron's red colobus monkey (   Procolobus badius waldroni ), a primate taxon endemic to the forests of this part of West Africa. We conclude that this monkey, which at least one authority considers worthy of species status, is probably extinct. Hunting by humans appears to be the ultimate cause of the extinction. Until our surveys began, little attention had been paid to the plight of this red colobus monkey, despite its listing as endangered by the World Conservation Union. The extinction of other large animals in the Upper Guinea rainforest region is likely to follow soon unless more attention is paid to the full range of endangered forms and more resources are devoted to their rigorous protection.     

Diana monkeys, Cercopithecus diana, adjust their anti-predator response behaviour to human hunting strategies

In Taï National Park, Ivory Coast, humans with guns hunt monkeys for their meat. The poachers imitate animal calls to feign the presence of eagles or leopards, two predators to which monkeys react with high calling rates and approach. In the presence of humans, monkeys become silent and move off. A small area of the park is now avoided by poachers, due to the establishment of a field project on chimpanzees in 1979. This offered the opportunity to investigate whether sudden changes in predation pressure lead to a rapid alteration in prey behaviour. Playback experiments, using groups of Diana monkeys, Cercopithecus diana, as subjects, revealed that the poachers' strategy works well in the home range of the habituated chimpanzee group. However, monkeys which are frequently exposed to poachers are rarely fooled by the imitations. Adaptive discrimination abilities can thus be acquired or lost within the lifespan of individual monkeys.     

Hunting, law enforcement, and African primate conservation

Abstract: Primates are regularly hunted for bushmeat in tropical forests, and systematic ecological monitoring can help determine the effect hunting has on these and other hunted species. Monitoring can also be used to inform law enforcement and managers of where hunting is concentrated. We evaluated the effects of law enforcement informed by monitoring data on density and spatial distribution of 8 monkey species in Taï National Park, Côte d’Ivoire. We conducted intensive surveys of monkeys and looked for signs of human activity throughout the park. We also gathered information on the activities of law‐enforcement personnel related to hunting and evaluated the relative effects of hunting, forest cover and proximity to rivers, and conservation effort on primate distribution and density. The effects of hunting on monkeys varied among species. Red colobus monkeys (Procolobus badius) were most affected and Campbell's monkeys (Cercopithecus campbelli) were least affected by hunting. Density of monkeys irrespective of species was up to 100 times higher near a research station and tourism site in the southwestern section of the park, where there is little hunting, than in the southeastern part of the park. The results of our monitoring guided law‐enforcement patrols toward zones with the most hunting activity. Such systematic coordination of ecological monitoring and law enforcement may be applicable at other sites.     

Determinants of group size in the red colobus monkey (Procolobus badius): an evaluation of the generality of the ecological-constraints model

The ecological-constraints model proposes that increased group size increases within-group feeding competition, necessitating increased travel and, consequently, constraining group size. Previous studies have supported the model for frugivores, but its applicability to folivores remains untested. This study evaluated the generality of the model by re-examining the relationship between day range and group size for a folivorous species for which published accounts have not found a relationship between these factors. This study differs from earlier studies by accounting for variation in food availability, which may drive changes in day range. We quantified the relationships among food availability, day range, and group size for two red colobus groups at Kibale National Park, Uganda. Mean day range and home range were significantly greater for the group of 48 individuals compared to the group of 24 individuals. The large group traveled more and rested less than the small group. The large group also traveled more rapidly than the small group. Food availability significantly predicted mean day range for the large group, but not for the small group. Analyses of covariance demonstrated that the large and small group responded differently to changes in food availability. These observations suggest that the large red colobus group experiences greater levels of within-group feeding competition than the small group. This study provides added support for the generality of the ecological-constraints model and contributes toward an understanding of the mechanisms controlling feeding competition and social organization in primates.     

Shark-inflicted injury frequencies, escape ability, and habitat use of green and loggerhead turtles

Interactions between large marine predators and their prey are difficult to observe and little is known about the risk of predation faced by sea turtles. The frequency of predator-inflicted injuries, however, has afforded insights into the predation risk faced by many taxa. We measured the frequency of shark-inflicted injuries on green (Chelonia mydas) and loggerhead (Caretta caretta) sea turtles in Shark Bay, Western Australia with a view to determining differences between species and sex-classes in the risk of predation from tiger sharks (Galeocerdo cuvier). Furthermore, we investigated how escape ability and habitat use might influence the probability of turtles being injured by sharks. Shark-inflicted injuries were more frequent on loggerhead than on green turtles, and most frequent on adult male loggerhead turtles. Species effects could not be attributed to differences in habitat use, since green turtles were found in habitats favored by tiger sharks more often than were loggerhead turtles. Green turtles, however, were faster and maneuvered better than loggerhead turtles, suggesting that escape ability is a factor in interspecific differences in injury frequency. The sex-class difference in injury frequency of loggerhead turtles suggests that males face greater predation risk than females and may take more risks. For green turtles, the lack of a sex difference in injury frequency might be due to greater escape ability lowering overall predation risk or to no differences between sexes in the benefits of risk-taking.     

Risk-prone hunting by chimpanzees (<Emphasis Type="Italic">Pan troglodytes schweinfurthii</Emphasis>) increases during periods of high diet quality

Most studies suggest that during times of nutritional stress, an animal faced with two foraging choices should follow a risk-prone strategy, choosing the option with highest payoff variance. This “scarcity/risk” hypothesis was developed to account for the foraging patterns of small animals with high metabolic rates susceptible to the threat of starvation. In this paper, we propose that animals should also be risk-prone when their diet quality is particularly high, far exceeding that which is needed to survive. Under these circumstances, the costs of experiencing a low or negative payoff can easily be recouped. We suggest that large-bodied omnivores are most likely to adopt this “abundance/risk” strategy. We investigate this question among wild chimpanzees (Pan troglodytes) that choose between a risk-averse strategy of feeding on plant material and a risk-prone strategy of hunting red colobus monkeys. Using 14 years of data on the Kanyawara chimpanzees of Kibale National Park, Uganda, we find strong evidence that chimpanzees follow the “abundance/risk” strategy. Both hunting rate (hunts/100 observation hours) and the probability of hunting upon encountering red colobus monkeys were positively correlated with seasonal consumption of ripe drupe fruits, a class of preferred food associated with elevated reproductive performance by females. Critically, these results remained statistically significant after controlling for the potentially confounding effects of male chimpanzee party size and the presence of sexually receptive females. These findings suggest that the relationship between risk-sensitive foraging and diet quality depends upon the daily probability of starvation, the number of alternative foraging strategies, and the degree to which diet quality satisfies an animal’s nutritional requirements.