Diet and habitat overlap in two sympatric primate species, the Tana crested mangabey Cercocebus galeritus and yellow baboon Papio cynocephalus

Diet and habitat overlap was studied in two sympatric primate species sharing two neighbouring patches of fragmented gallery forest in Tana River, Kenya. Systematic data on feeding and ranging behaviour was collected on one group each of the Tana crested mangabey Cercocebus galeritus and yellow baboon Papio cynocephalus between August 1992 and February 1993. When rainfall was low and fruit resources scarce, yellow baboons spent most of their foraging time in the open woodlands while mangabeys foraged within the forest. At this period, diet and habitat overlaps between the two species were low. As rainfall increased, followed by a gradual rise in fruit availability, yellow baboons shifted their foraging range and both species became confined to the forest habitat. Consequently, both diet and habitat overlaps increased, peaking at the end of the rainy season. Mangabeys showed a reduced within-group dispersal and also spent significantly less time foraging in a given forest patch when yellow baboons were also present within the same forest patch.
Increased habitat and diet overlaps during the wet season need not have resulted in increased interspecific competition for food because at this period, fruits were readily available in the forest.     

Brief communication: Puncture and crushing resistance scores of Tana river mangabey (Cercocebus galeritus) diet items

Cercocebus mangabeys are characterized by dental traits that have been interpreted as adaptations to eat hard diet items. Although there are data that mangabeys include a large proportion of fruit and especially seeds in their diets, no hardness measurements have been done on mangabeys' food items. This study measured puncture and crushing resistance of food items in the diet of the Tana River mangabey (C. galeritus). Feeding data were collected by the use of scan samples from one mangabey group from August 2000 to July 2001 and from July 2005 to June 2006. Food items were collected during the latter period only, and from the same tree in or under which mangabeys had been observed eating. A portable agricultural fruit tester was used to measure the puncture resistance of fruit and a valve spring tester was used to measure the crushing resistance of seeds. The average puncture resistance of fruit was 1.7 kg/mm², and the average crushing resistance of seeds was 12.8 kg. There were no correlations between puncture resistance, crushing resistance, or all resistance scores and frequency contribution to the diet. Resistance scores measured in this study were within the range of hardness scores of fruit and exceeded hardness scores of seeds eaten by other hard object feeders. Although this study supports the interpretation that Cercocebus dental traits are adaptations to hard object feeding, future research should investigate other material properties of food, as well as the role hard diet items play in niche separation and as fallback foods. Am J Phys Anthropol 2009. © 2009 Wiley‐Liss, Inc.     

The Value of Measuring Food Availability on the Ground for a Semiterrestrial Frugivore, the Tana River Mangabey (Cercocebus galeritus) of Kenya

Collecting phenological data, seasonal availability of plant resources that primates feed on, allows us to understand feeding ecology better. A number of primates are terrestrial or semiterrestrial frugivores, yet phenology is generally measured only in the canopy. I hypothesized that combining measurements of food availability on the ground with canopy measurements would more strongly correlate with diet than canopy measurements alone for a semiterrestrial frugivore, the Tana River mangabey (Cercocebus galeritus). From July 2005 until June 2006, I conducted monthly follows on a mangabey group. Phenology was measured in 105 individuals of their top seven food tree species. I measured canopy phenology on a 0–5 scale and counted fruits in three 1 m³ areas of the canopy, and measured ground phenology by counting fruits and seeds in four 1 m² quadrats under the canopy. I calculated each tree’s canopy volume and canopy shadow, and each species’ mean fruit weight, mean seed weight, and density. Monthly biomasses were calculated as kilograms per hectare. Spearman correlations were performed between diet contribution and canopy biomass, ground biomass, and total biomass. The hypothesis was not supported for seven species individually or combined. The hypothesis was supported for 3 of 12 diet items, although canopy biomass was also significant for 2 of those items. Two diet items correlated only with ground biomass. Studies of the Tana River mangabey may benefit from measuring ground phenology only for those items eaten exclusively on the ground. Primatologists studying terrestrial or semiterrestrial frugivores should consider feeding height when deciding on phenology methods.     

Ecological correlates of abundance in the Tana mangabey (Cercocebus galeritus)

I investigated the ecological correlates of abundance in the Tana mangabey (Cercocebus galeritus), one of the world's most endangered primates, with the goal of recommending management strategies. I systematically selected 31 forest fragments throughout the mangabey's 60-km distribution along the lower Tana River in southeastern Kenya. Within the 31 fragments, I measured vegetation structure, food abundance, and human forest product use in 107 belt transects, and conducted 370 mangabey surveys. I used a weighted multiple regression analysis to determine whether there was a dependence between the selected forest attributes and the mean number of mangabey groups per fragment. Fragment area and density of trees > or =10 cm diameter at breast height (DBH) were the only variables that significantly correlated with the variation in mangabey abundance. No additional variables were significant when the analysis was limited to forest fragments inside the Tana River Primate National Reserve (TRPNR) or to fragments outside the TRPNR. When I estimated the resources available before recent human forest product use by adding nonharvested and harvested variables, the total basal area of the top 15 food species became significant. This was only within the TRPNR, however. Management, therefore, should focus on increasing forest area, density of trees > or =10 cm DBH, and coverage of food trees throughout the mangabey's distribution. Solutions must be found for the problem of forest clearing, and forest product use must be better managed to protect the habitat of this critically endangered primate. The significance of food abundance only within the TRPNR suggests a need to collect dietary data from mangabey groups in fragments toward the southern limit of the mangabey's distribution, where plant species composition differs from that in fragments in which dietary data have been previously collected.     

Food competition in captive female sooty mangabeys (Cercocebus torquatus atys)

We studied the social and foraging behavior of two captive groups of sooty mangabeys under two different spatial food situations. These food conditions were clumped (food was placed in a box) and dispersed (food was dispersed over the entire enclosure). In each group five adult females and two adult males were observed. As a criterion for food competition, individual differences in the relative food intake were used. Adult female mangabeys had a linear, stable, and unidirectional dominance hierarchy. Access to food was rank dependent among females only under clumped food distribution, as current models of the evolution of primate social systems predict. However, feeding success appeared to be mediated not by female but by male agonistic behavior toward females. High-ranking females received relatively less aggression from males and could, therefore, stay and feed longer in the feeding area. Male tolerance of higher-ranking females seems to mediate female feeding success under restricted food resources. The establishment of a special relationship with a high-ranking male might, therefore, be a strategy to get better access to food. This study demonstrates that female competition for access to food should not be analyzed separately from male influences on females and suggests that a more integral role of males in socioecological models of the evolution of primate social systems should be considered.     

Ecological consequences of a group fission event in the Tana River mangabey (Cercocebus galeritus)

A group of Tana River mangabeys Cercocebus galeritus studied in 2000–2001 fissioned into two daughter groups in 2004, the first reported case of fission in Cercocebus. Data were collected on each daughter group in 2005–2006 to investigate how the groups divided the parent group's range, the quality of habitat used by each group, and if fruit abundance was correlated with the spatial relationships between the groups. Six days of ranging data were collected each month and input into ArcView GIS 3.3 to measure home ranges and core areas. Phenological data were collected from nine important food species. Habitat quality was measured by counting all reproductive‐sized individuals of those nine food species in the ranges. The daughter groups shared the parent group's home range and core area, although the larger group used more of those areas than the smaller group. The two groups got equal quality home ranges and core areas as measured by per capita food trees, but the larger group had access to a larger and richer exclusive area. Proximity of the groups to each other was not correlated with fruit abundance. This study contributes to the small body of literature that addresses ecological consequences of primate group fission.     

A brief report on the social behavior of the crested mangabey (Cercocebus galeritus galeritus) with a comparison to the sooty mangabey (C. torquatus atys)

A group of 38 free ranging crested mangabeys in the Tana River Primate Reserve was studied over a 6-week period for a total of 209.5 hr and behavioral comparisons made to a captive group of sooty mangabeys. Although quantitative comparisons between these two mangabey species are not possible, the present data suggest that these geographically separated mangabeys share several behavioral similarities. Copulatory behavior in both species involved a pattern of female darting and female vocalizing following the mount by the male. Several similarities in agonistic behavior also existed: 1) The victim often returned or stayed within 1 m of the aggressor following an agonistic episode; 2) retaliation in which the victim first fled or avoided the aggressor, then subsequently, chased or lunged at the aggressor, typically while screaming; and 3) frequent redirection of aggression by the victim following an agonistic episode. A dominance rank reversal occurred between the two adult male crested mangabeys with no severe wounding. The rank reversal seemed to be related to two subsequent behaviors which included infant carriage by the deposed alpha in the presence of the new alpha male and female demonstrations of extreme protectiveness of their infants in the presence of the new alpha male. Both of these behaviors have been reported in the sooty mangabey group.     

Gastrointestinal parasites of critically endangered primates endemic to Tana River, Kenya: Tana River red colobus (Procolobus rufomitratus) and crested mangabey (Cercocebus galeritus)

We conducted fecal egg counts of gastrointestinal parasites of 2 critically endangered primates endemic to the forest of Tana River, Kenya. We aimed to use the fecal egg counts as proxies to quantify the prevalence of gastrointestinal parasites between the 2 primates. The Tana River red colobus (Procolobus rufomitratus) and crested mangabey (Cercocebus galeritus) are of similar body size, but their behavioral ecology is very different. We predicted that mangabeys would have a higher prevalence of parasites because they are mostly terrestrial omnivores, live in larger social groups, and therefore range widely. We detected 10 nematodes and 3 protozoans in mangabeys and 7 nematodes and 2 protozoans in colobus. We detected a higher number of different parasite species in individual mangabeys, and 4 of the 5 nematodes requiring intermediate hosts were found in mangabeys. The overall prevalence of parasites was higher for mangabeys, but this difference was not statistically significant. For colobus, we found a trend whereby the number of different parasite species in individual monkeys was higher in males and in lactating females. However, there was no difference in the prevalence of parasites between the sexes or between lactating and nonlactating females.     

Pregnancy,gestation and parturition in free-ranging tana river crested mangabeys (Cercocebus galeritus galeritus)

Mean gestation for seven free-ranging Tana River crested mangabeys (Cercocebus galeritus galeritus) is 180 days (SE = 4.49). All females showed postconception sexual swellings after the first 2 months of pregnancy, and two of the seven copulated with males at this time. One birth was observed; observations of a second infant began less than 1 hr after birth. Details of parturition are given, with responses of group members to the events. Adult and juvenile females showed more sustained interest in the new infants than adult or juvenile males.     

Variability in diet and foraging behaviour between sexes and ploidy forms of the hybridogenetic Squalius alburnoides complex (Cyprinidae) in the Guadiana River basin, Portugal

Samples of the Squalius alburnoides complex, a hybridogenetic Iberian minnow composed of diploid, triploid and, less commonly, tetraploid forms, were collected from a tributary of the Ardila River (Guadiana River basin) between February 1999 and January 2001. Seasonal variation in diet was evident, and was probably linked to prey availability. Distinct foraging behaviours between ploidy forms were found towards several prey items, suggesting that diploid adult males fed mostly near the surface, whereas diploid adult females tended to feed near the bottom and submerged vegetation. Triploid females exhibited an intermediate foraging behaviour, although there was greater affinity towards diploid male feeding behaviour. Diploid males which, in contrast to diploid and triploid females, have non‐hybrid genomes in the Guadiana drainage, exhibited a higher specialization for food. Despite considerable dietary overlap, there appeared to be spatial segregation of feeding niches between the three forms, especially during dry periods when prey availability was lower, which may be a strategy for diminishing competition for food. Therefore, considering asexual generalist and specialist hypotheses, it appears that the different ploidy levels are generalist, opportunistic feeders that partition the resources when limited.     

Climatic determinants of diet and foraging behaviour in baboons

Baboons (Papio spp.) are characterised by a large degree of variation in foraging behaviour and dietary composition. Previous analyses have suggested that much of this can be traced to differences in ecological conditions between sites. The proximate mechanism underlying these relationships is assumed to be mediated via the impact of climatic conditions on food availability, and ultimately the impact that this has on dietary composition. This paper examines these relationships more explicitly. Data from 15 baboon populations were used to assess the relationship between foraging variables and dietary composition. Only feeding time showed significant relationships with dietary composition, with percentage of time spent feeding decreasing with proportion of fruit in the diet, and increasing with the proportion of subterranean items. No relationships were found between diet composition and moving time or day journey length, although significant relationships were found between these variables and group size. The proportions of feeding time spent feeding on fruit, subterranean items and leaves were functions of the ecological conditions experienced by that population, although no relationships were found for the percentage of feeding time devoted to flowers or animal material. The relationships between the proportion feeding time spent on fruits, leaves and subterranean items and ecological variables could be best explained through understanding the way in which bush and tree level vegetation respond to the climatic environment and the impact this has on fruit availability. In this respect, temperature and seasonality are the key climatic parameters. This provides good support for the idea that the proximate mechanism underlying the relationship between foraging time and ecological variables is mediated via the impact of the climatic environment on vegetation structure and food availability. Similar factors have been proposed to explain much of the geographic variation in species diversity, suggesting that these relationships have far wider relevance and may account for much of the observed geographical variation in mammalian behaviour.     

Feeding ecology and dietary differences between blue monkey (Cercopithecus mitis stuhlmanni Matschie) groups in logged and unlogged forest, Budongo Forest Reserve, Uganda

Several studies have investigated the effects of logging on primate population density, and attempted to relate density differences to changes in vegetation composition. As population density in some forest primates may be considerably influenced by dietary quality, it is important to understand how the effects of vegetation changes commonly associated with logging influence primate feeding ecology. Results are presented from a study carried out in the Budongo Forest Reserve in Uganda to investigate differences in blue monkey (Cercopithecus mitis stuhlmanni) feeding ecology in forest blocks with different logging history. Dietary composition differed between logged and unlogged forest, with a higher proportion of unripe fruit consumed in logged forest. By contrast, the proportion of young leaves, invertebrates and seeds in the diet was higher in unlogged forest. Variations in the intake of fruit was also higher in unlogged forest, but feeding patterns on other dietary items were more selective. These differences in diet reflect differences in availability of different categories of food items, as determined by tree species composition, abundance and plant phenological patterns. The observed differences between feeding ecology in logged and unlogged forest are discussed in relation to primate feeding ecology and habitat composition in Budongo.     

Foraging behaviour of the Brazilian squirrelSciurus aestuans (Rodentia, Sciuridae)

We describe the foraging behaviour of the Brazilian squirrelSciurus aestuans Linnaeus, 1776 in a natural free-living population, in an area with a high concentration of palm fruitsSyagrus romanzoffiana (Chamisso) Glassman. Our objective was to investigate if the abundance ofS. romanzoffiana fruits, an important food item for squirrels, temporally influenced the foraging behaviour of this population. The observations were carried out over an eight-month (April–November 2001) period. Fruiting phenology ofS. romanzoffiana was also monitored. The most consumed food item for this period was the fruit ofS. romanzoffiana (70%), followed by foods of human origin (14%). The percentage of time spent feeding increased in September, and the time spent travelling declined in September, October and November, when females were observed showing evidence of reproductive activity. At the same timeS. romanzoffiana fruits become available. The consumption of human items illustrates the opportunistic feeding habit of these squirrels, but variations in foraging behaviour detected probably were more strongly related to availability ofS. romanzoffiana fruits.     

Red-gartered Coot Fulica armillata feeding on the grapsid crab Cyrtograpsus angulatus: advantages and disadvantages of an unusual food resource

The behaviour of Red-gartered Coots feeding on an unusual food source was examined at Mar Chiquita Coastal Lagoon, Argentina. The grapsid crab Cyrtograpsus angulatus made up all observed prey items, and 61% were small. Both handling and foraging duration increased with the size of captured crabs, but foraging efficiency decreased. Crab availability affected both the dive duration of the Coots and their foraging decisions with regard to prey-size selection. Two species of gull were observed kleptoparasitizing Coots, especially when the Coot was handling medium or large crabs. Feeding by Coots on Cyrtograpsus angulatus has not been previously documented and may be a feeding innovation. Our estimations suggest that Coots were foraging optimally, since smaller crabs were more energetically profitable.     

The nutritional value of feeding on crops: Diets of vervet monkeys in a humanized landscape

Anthropogenic influences have dramatically altered the environments with which primates interact. In particular, the introduction of anthropogenic food sources to primate groups has implications for feeding behaviour, social behaviour, activity budgets, demography and life history. While the incorporation of anthropogenic foods can be beneficial to primates in a variety of nutritional ways including increased energetic return, they also carry risks associated with proximity to humans, such as risk of being hunted, disease risk and risk of conflict. Given such risks, we initiated a 3‐year study where we sought to understand the underlying nutritional motivations for anthropogenic food resource use by vervet monkeys (Cercopithecus aethiops) in the humanized matrix surrounding the Nabugabo Field Station in central Uganda. Feeding effort, defined as proportion of feeding scans spent on anthropogenic food, was not associated with ripe fruit availability nor with crop availability as determined by phenological monitoring. Likewise, there was no difference in the protein, fibre, or lipid composition of crop food items compared to wild food items. Individuals spent less time feeding overall in months over the 3 years with a higher proportion of time spent feeding on crop foods, suggesting a potential benefit in terms of accessibility (reduction in the proportion of activity budget devoted to feeding).     

Crop Feeding by Brown Howlers (<Emphasis Type="Italic">Alouatta guariba clamitans</Emphasis>) in Forest Fragments: The Conservation Value of Cultivated Species

Primates inhabiting human-modified habitats often complement their diets with cultivated species. Although this flexible foraging behavior reduces feeding stress in animals inhabiting small or low-quality habitats, its potential economic costs may promote negative human–nonhuman primate interactions. It is critical to assess the importance of cultivated species to primate diets, the factors influencing their exploitation, and their associated economic costs to evaluate the conservation value of cultivated species and the impact of crop feeding on human–nonhuman primate coexistence. Based on a 30-months study of three groups of brown howlers (Alouatta guariba clamitans) inhabiting <10-ha forest fragments in Rio Grande do Sul State, southern Brazil, and semistructured interviews with landowners, we assessed 1) the cultivated species used as food sources, 2) the relationship between food availability and crop feeding, and 3) the potential economic costs of crop feeding and their impact on landowner–howler coexistence. Brown howlers exploited six cultivated species as fruit or seed sources. This exploitation was concentrated on ripe fruit of Psidium guajava, Citrus reticulata, Diospyros kaki, and Eriobotrya japonica, which together accounted for up to 32% of total feeding records during some months. Availability predicted fruit consumption for three of these species. The overall availability of cultivated fruit also predicted its consumption, whereas overall wild fruit availability did not. Despite potential economic costs of crop feeding (US$320–US$1141 per year), landowners reported no conflict with howlers arising from their behavior, an amicable response that supports the conservation value of cultivated plants in different landscape elements of the anthropogenic matrix.     

Diet and feeding behaviour of samango monkeys (Cercopithecus mitis labiatus) in Ngoye Forest, South Africa

The samango monkey occurs at the southern limit of the range of Cercopithecus mitis. Greater climatic seasonality at this latitude results in more predictable fruiting patterns. In addition, there are no diurnal sympatric primate frugivores. Under these conditions, the diet and feeding strategies of samango monkeys would be expected to differ notably from those of central or east African C. mitis subspecies. Contrary to these expectations, the preliminary observations reported here indicate that diets of samango and blue monkeys differ only superficially in the proportions of items eaten. Similarities in feeding behaviour are especially marked during the dry season period when fruit is not abundant. Both samango and blue monkeys tend to be less selective in their choice of food species and to eat available food species regardless of their energy content; a shift toward less nutritious items such as leaves is also noted. Feeding behaviour during the summer wet season is characterized by the selection of fruits with high-energy values. A high proportion of visits by the monkeys to areas of greater food availability suggests a concentration of feeding effort in food patches and the selection of higher energy food species within patches.     

Food resources of the wild Barbary macaque (Macaca sylvanus) in high-altitude fir forest, Ghomaran Rif, Morocco

A small geographically isolated population of the Barbary macaque inhabits a high-altitude fir forest habitat ( Abies pinsapo ) in the Ghomaran region of the Rif mountains of northern Morocco. The climate of this region is Mediterranean, but the altitude (1600–2100 m) causes winters to be cold (as low as -8.0 C) with snow occurring from November to May (snowfall as deep as 1.5 m). The primary winter feeding adaptation is the ability to ingest high quantities of fir foliage; in spring, the macaques took a high diversity of leafy food items from all vegetation layers; in summer, the macaques foraged terrestrially for a high diversity of food items including seeds, small fruits, bulbous geophytes, and animal foods (including tadpoles from small streams); in autumn, the macaques returned to arboreal foraging, primarily feeding on oak acorns ( Quercus ilex ), fir seeds and yew fruit ( Taxus baccata ). The macaques were capable of ingesting 100 of 195 (51%) of all identified plant species in the region, although during the four-month winter, the macaques only averaged 12.5 common food items. A comparison of the study area with the prime habitat of the Barbary macaque-the high-altitude cedar forests of the Moroccan Moyen Atlas-indicates that climate and vegetation physiognomy are highly similar in both regions. Correspondingly, there is a high degree of similarity in macaque diet in both regions in terms of feeding behaviour by season, food diversity and specific feeding techniques. In the Ghomara, the winter feeding adaptation of fir foliage eating parallels that of the Barbary macaque in cedar forest (winter foraging for cedar foliage). This enables the Barbary macaque to exploit the Ghomaran fir forest habitat during the cold, snowy winters much the same as it does cedar forest habitat throughout a major portion of its geographical range.     

The role of phytochemistry in dietary choices of Tana River red colobus monkeys(Procolobus badius rufomitratus)

We conducted a phytochemical survey of tree species growing within the riverine forests of the Tana River National Primate Reserve in Kenya to understand better the feeding ecology of an endangered resident primate, the Tana River red colobus monkey (Procolobus badius rufomitratus).Young leaves, which make up a large percentage of this monkey's diet, are significantly higher in nitrogen and lower in acid detergent fiber than more abundant mature leaves are. Phenolic chemistry had little inhibitory effect on feeding by P. b. rufomitratus.Choice among tree species by P. b. rufomitratusappears to be influenced largely by leaf availability,once an acceptable threshold of nitrogen and fiber is reached When mature leaves are eaten, they selected species that are high in nitrogen and low in fiber. A significantly higher nitrogen content was found for the mature leaves of all leguminous versus nonleguminous tree species. Consequently, the availability of certain types of mature leaf species during periods of preferred food scarcity may prove critical to groups of Tana River red colobus monkeys.