Nutritional benefits of crematogaster mimosae ants and acacia drepanolobium gum for patas monkeys and vervets in laikipia,Kenya

Patas monkeys (Erythrocebus patas) are midsized primates that feed extensively on the gum of Acacia drepanolobium and the ants are housed in swollen thorns of this Acacia. Their diet resembles that expected more of smaller bodied primates. Patas monkeys are also more like smaller bodied primates in reproducing at high rates. We sought to better understand the convergence of patas monkeys with smaller bodied primates by comparing their feeding behavior on ants and gum with that of closely related, sympatric vervets (Chlorocebus pygerythrus), and analyzing the nutrient content of the gum of A. drepanolobium and of Crematogaster mimosae, the most common ant species eaten by patas monkeys in Laikipia, Kenya. All occurrences of feeding and moving during focal animal sampling revealed that 1) patas monkeys seek A. drepanolobium gum but vervets avoid it; 2) both species open swollen thorns most often in the morning when antsare less active; 3) patas monkeys continually feed onswollen thorns and gum while moving quickly throughout the day, whereas vervets reduce their consumption of these items and their travel rate at mid‐day, and; 4) vervets eat young swollen thorns at a higher rate than patas monkeys. Patas monkeys are able to spend little time acquiring substantial amounts of energy, protein, and minerals from A. drepanolobium gum and C. mimosae ants each day. These findings, when coupled with evidence of causes of infant and adult female mortality, suggest that reproductive success of female patas monkeys is more immediately affected by illness, disease, interactions between adults and infants, and access to water than by food. Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

Locomotor activity differences between sympatric patas monkeys (Erythrocebus patas) and vervet monkeys (Cercopithecus aethiops): Implications for the evolution of long hindlimb length in Homo

Homo erectus is notable for its taller stature and longer lower limbs relative to earlier hominids, but the selective pressures favoring such long limbs are unclear. Among anthropoid primates, patas monkeys (Erythrocebus patas) and extant hominids share several extreme characteristics involved with foraging and movement, including the relatively longest lower limb proportions, longest daily travel distances and largest home ranges for their body or group size, occupancy of some of the driest habitats, and very efficient thermoregulatory systems. We suggest that patas monkeys are an appropriate behavioral model with which to speculate on the selective pressures that might have operated on H. erectus to increase lower limb length. Here, in a comparison of the locomotor activities of patas monkeys and sympatric, closely related vervet monkeys (Cercopithecus aethiops), we provide evidence for the hypothesis that patas use their long stride more to increase foraging efficiency while walking than to run, either from predators or otherwise. Am J Phys Anthropol 105:199–207, 1998. © 1998 Wiley-Liss, Inc.     

Difference in food selection between patas monkeys (Erythrocebus patas) and tantalus monkeys (<Emphasis Type="Italic">Cercopithecus aethiops tantalus</Emphasis>) in Kala Maloue National Park,Cameroon, in relation to nutrient content

Phytochemical or nutrient analyses of primate diets have revealed clues to their food selection in a single species. On the other hand, few interspecific comparisons of phytochemical or nutrient composition of primate diets have been made, although diets are considered to differ in phytochemical or nutrient content from primate species to species, since different species have different body weights and different morphological and physiological characteristics. I compared the nutrient content of diet between patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus) living sympatrically in Cameroon. Patas subsisted on a smaller number of food items, most of which were also tantalus food items. Then, I compared the protein–fiber ratio and the available energy content of the food items eaten by patas (patas foods) with those items eaten only by tantalus (tantalus foods). Both variables were higher in patas than tantalus foods, although there was no significant difference in available energy of plant foods. Next, when I performed discriminant analysis for patas foods and tantalus foods, employing the above two variables, a discriminant function with positive coefficients for both variables was obtained. The mean discriminant-function score of patas foods was higher than that of tantalus foods. Despite being somewhat larger in weight, patas selectively fed on a smaller number of foods of higher quality than did tantalus. I discuss why the results are inconsistent with a well known body weight–diet relationship (Jarman–Bell principle). Energy-efficient locomotion enables patas to exploit not only small dispersed food items of high quality but also areas where high-quality foods are distributed in clumps. Electronic Publication     

Rank Differences in Ecological Behavior: A Comparative Study of Patas Monkeys (Erythrocebus patas) and Vervets (Cercopithecus aethiops)

One of the central dichotomies in primate behavior is between species in which there are relationships among females that include stable dominance relationships, and those in which the relationships include weak or unstable dominance relationships. This dichotomy has been attributed to differences in food resources, with stable dominance hierarchies occurring in species that feed on usurpable foods. We compared rank-related differences in nonagonistic behaviors considered to be tightly linked to ecology in broadly sympatric vervets (Cercopithecus aethiops) and patas monkeys (Erythrocebus patas), two closely related cercopithecines that are exemplars of this dichotomy, with the expectation that vervets would exhibit stronger rank differences than patas monkeys in these behaviors. Overall, rank explained more than twice as much variation among vervets as among patas monkeys in ranging behavior, activity budgets, and diet. Vervets did not, however, exhibit stronger rank differences when they used Acacia xanthophloea habitat, in which foods are more usurpable, compared to Acacia drepanolobium habitat, in which foods are less usurpable. In Acacia drepanolobium habitat, to which patas are restricted, higher-ranking vervets converged in behavior with patas monkeys to a greater extent than lower-ranking vervets, suggesting that social constraints interfere with the foraging efficiency of lower-ranking vervets even in habitats in which there are fewer opportunities to usurp foods.     

Reconciliation following aggression in patas monkeys,Erythrocebus patas

Following intra-group aggression, obvious conciliatory displays are absent from the behavioural repertoire of patas monkeys, Erythrocebus patas, while many other Old World primate species show special reconciliation gestures. When 10-min focal-animal samples that began after spontaneous aggression were compared with matched-control samples, captive adult female patas followed up on aggressive interactions, interacting sooner and more often with former opponents during post-conflict observations than during matched-control observations. Almost one-third of post-conflict observations included affiliative behaviour between former opponents, which is termed reconciliation. Matrilineally related opponents were more likely to reconcile with one another than were unrelated animals. No effect of the dominance hierarchy on tendency to reconcile was found. Thus, patas monkeys showed general patterns in post-conflict behaviour that were similar to those seen in other primates previously investigated.     

Seasonal, sex, and interspecific differences in activity time budgets and diets of patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus), living sympatrically in northern Cameroon

I examined seasonal, sex, and interspecific differences in activity time budgest and diets of patas (Erythrocebus patas) and sympatric tantalus monkeys (Cercopithecus aethiops tantalus) on the basis of 5-day data sets collected in three and two different seasons, respectively, by the method of focal animal sampling. The seasons included species-specific mating and birth seasons. As compared with not only the birth season but also conspecific females, both patas resident male and tantalus male spent less time feeding and more time resting, day and night, in their respective mating seasons. Given that day-resting time includes time for vigilance for non-resident males and receptive females, this may reflect that males should minimize time spent feeding to allow maximum participation in other fitness-increasing activities such as mating-relating activities asSchoener (1971) predicted. In both species, the males consumed fruits containing less protein but more calories and showed a high feeding rate to compensate for the shorter time spent feeding in the mating season. In contrast, females consumed protein-rich food types (i.e. animals, protein-rich seeds, leaves, and flowers) in the birth season to meet the high demand for protein due to pregnancy and lactation. Given that the season for males was considered to be not a calendar but a reproductive “season” (i.e. mating or birth season), both sexes of patas spent more time moving and less time day- and night-resting than did the tantalus counterparts irrespective of the “season”. Patas subsisted on fruits, gums, and supplementarily lipid-rich seeds as an energy source and animal matters and protein-rich seeds as a protein source. In contrast, tantalus subsisted on fruits and lipid-rich seeds as energy and flowers and leaves as protein.     

Despotic wild patas monkeys (Erythrocebus patas) in Kala Maloue, Cameroon

The socio-ecological model predicts that the quality, distribution, and patch size of food resources determines the dominance hierarchy of female monkeys based on the type of food competition they experience. Comparative studies of closely related species have evaluated the socio-ecological model and confirmed its validity. For example, female patas monkeys in Laikipia, Kenya, form a nonlinear and unstable dominance hierarchy (i.e., egalitarian), whereas females of sympatric, closely related savannah monkeys form a linear and stable dominance hierarchy (i.e., despotic), in accordance with the model's predictions of the characteristics of food resources. I compared agonistic interactions involving food between patas monkeys (Erythrocebus patas) and sympatric savannah monkeys (Cercopithecus aethiops) in Kala Maloue, Cameroon. I found linear dominance hierarchies not only in savannah monkeys, but also in patas monkeys in Kala Maloue. The rates of agonistic interactions during feeding between patas monkeys were equivalent to those between savannah monkeys in Kala Maloue; further, these rates were significantly higher than those of both Laikipia patas and savannah monkeys. The results imply that patas monkeys in Kala Maloue are not egalitarian, but are despotic, similar to savannah monkeys. Disparity in the dominance hierarchies of patas monkeys between Kala Maloue and Laikipia were attributable to the differences in the characteristics of food resources. Although patas monkeys in Laikipia subsist on small and dispersed food resources within a high-density area, those in Kala Maloue subsisted on food resources that were clumped in intermediate-sized patches within a low-density area. This study shows that the socio-ecological model is applicable not only for interspecific comparisons but also for intraspecific comparisons.     

Interspecific and temporal variation of ant species within Acacia drepanolobium ant domatia, a staple food of patas monkeys (Erythrocebus patas) in Laikipia, Kenya

The ants that live in the swollen thorns (domatia) of Acacia drepanolobium are staple foods for patas monkeys (Erythrocebus patas). To obtain a better understanding of these insects as resources for patas monkeys, we sampled the contents of 1,051 swollen thorns (ant domatia) over a 22-month period from December 1999 to September 2001, in Laikipia, Kenya. First, we confirmed that of the four species of ants that live on A. drepanolobium, Crematogaster sjostedti, the competitively dominant ant in this system, does not rear significant brood in the swollen thorns and is therefore not a major food item of patas monkeys. Second, across the other three species that do use swollen thorns for rearing their brood, C. nigriceps, C. mimosae, and Tetraponera penzigi, the number of worker ants per swollen thorn increased with increasing competitive dominance. Third, although there was considerable month-to-month variation in the number of workers, immatures, and especially alates (winged reproductives) within species, there was less variation across species because ant production was asynchronous. Variation in domatia contents was poorly related to rainfall for each of the three species. Finally, distal thorns held more alates and fewer workers than interior thorns, and branches higher off the ground held more alates and more workers than lower branches. For the numerically dominant C. mimosae, higher branches held significantly more immature ants than did lower branches. Ants are reliable food resources for patas monkeys, and are probably more reliable than many plant resources in this highly seasonal environment. We estimate that patas monkeys may get as much as a third of their daily caloric needs from these ants year-round. As ants and other insects are widely consumed by primates, we suggest that greater consideration be given to species differences in animal food choices and that further studies be conducted to examine the degree to which ants influence energy intake and reproduction in other primates.     

Comparison of responses to alarm calls by patas (Erythrocebus patas) and vervet (Cercopithecus aethiops) monkeys in relation to habitat structure

We studied responses to alarm calls of sympatric patas (Erythrocebus patas) and vervet (Cercopithecus aethiops) monkeys in relation to habitat structure, with the intention of understanding the relationship between the environment and predator avoidance. Patas and vervet monkeys are phylogenetically closely related and overlap in body size. However, while patas monkeys are restricted to nonriverine habitats at our study site, vervets use both nonriverine and riverine habitats, allowing us to "vary" habitat structure while controlling for effects of group size, composition, and phylogeny. Patas monkeys in the nonriverine habitat responded to mammalian predator alarm calls with a greater variety of responses than did vervets in the riverine habitat, but not when compared with vervets in the nonriverine habitat. Ecological measurements confirm subjective assessments that trees in the riverine habitat are significantly taller and occur at lower densities than trees in the nonriverine habitat. Despite the lower density of trees in the riverine habitat, locomotor behavior of focal animals indicates that canopy cover is significantly greater in the riverine than the nonriverine habitat. Differences in responses to alarm calls by the same groups of vervets in different habitat types, and convergence of vervets with patas in the same habitat type, suggest that habitat type can be a significant source of variation in antipredator behavior of primates.     

Foraging strategies of yakushima macaques (Macaca fuscata yakui )

I investigated the activity budget and diet of Yakushima macaques (Macaca fuscata yakui,)in warm temperate broad- leaved forest of Yakushima, Japan. Both time spent feeding and time spent moving varied considerably between half- months. However, total time spent in active behaviors— feeding time plus moving time— was stable. The composition of the diet also showed considerable variation between half- months. The macaques fed mainly on fruits, seeds,mature leaves, fallen seeds, flowers, and young leaves, each of which accounted for more than 30% of feeding time in at least 1 half- month. They also ate insects and fungi, but each of them comprised ≤ 25 and ≤ 8% of feeding time in any half- month, respectively. Time spent feeding on mature leaves, young leaves, flowers, or fallen seeds is positively correlated with total time feeding and is negatively correlated with time moving. In contrast, time feeding on fruits, seeds, insects or fungi is negatively correlated with time feeding and is positively correlated with time moving. Foraging on foods that have a low energy content, a high density, and a relatively even distribution— mature leaves— or that need much manipulation to be processed— flowers and fallen seeds— increased feeding time, while foraging on foods for which monkeys must search intensively in the forest— fruits, seeds, insects, and fungi— led to increased moving time. I examined foraging strategies of Yakushima macaques in terms of moving costs and the quality of food items. Regarding time feeding on fruits, which have more energy and may need less manipulation than other foods, as a benefit, and moving time as a cost, they seemed to employ a strategy that balanced the costs and benefits of foraging.     

Fallback Foods of Red Leaf Monkeys (Presbytis rubicunda) in Danum Valley, Borneo

Animals in Southeast Asia must cope with long periods of fruit scarcity of unpredictable duration between irregular mast fruiting events. Long-term data are necessary to examine the effect of mast fruiting on diet, and particularly on the selection of fallback foods during periods of fruit scarcity. No such data is available for colobine monkeys, which may consume substantial amounts of fruits and seeds when available. We studied the diet of red leaf monkeys (Presbytis rubicunda, Colobinae) in Danum Valley, Sabah, northern Borneo, using 25 mo of behavioral observation, phenology and vegetation surveys, and chemical analysis to compare leaves eaten with nonfood leaves. The monkeys spent 46% of their feeding time on young leaves, 38% on seeds, 12% on whole fruits, 2.0% on flowers, 1.0% on bark, and 1.2% on pith. They spent more time feeding on seeds and whole fruit when fruit availability was high and fed on young leaves of Spatholobus macropterus (liana, Leguminosae) as fallback foods. This species was by far the most important food, constituting 27.9% of the total feeding time, and the feeding time on this species negatively correlated with fruit availability. Consumed leaves contained more protein than nonconsumed leaves, and variation in time spent feeding on different leaves was explained by their abundance. These results suggest that red leaf monkeys show essentially the same response to the supra-annual increase in fruit availability as sympatric monogastric primates, increasing their seed and whole-fruit consumption. However, they depended more on young leaves, in particular Spatholobus macropterus, as fallback foods during fruit-scarce periods than did gibbons or orangutans. Their selection of fallback food appeared to be due to both nutrition and abundance.     

Differences Between Vervets (Cercopithecus aethiops) and Patas Monkeys (Erythrocebus patas) in Agonistic Interactions Between Adult Females

We examined agonistic interactions between adult females in wild, unprovisioned patas monkeys (Erythrocebus patas) and vervets (Cercopithecus aethiops). The dominance hierarchy of patas is far less clear than that of vervets. Patas had fewer interactions per dyad, fewer dyads with interactions, and a high percentage (18%) of reversals in which lower-ranking females won in agonistic interactions with higher-ranking females. Although the rank ordering of the kinds of interactions patas and vervets displayed is similar, with avoidance being the most frequently observed agonistic response to approaches by other females, patas were chased and supplanted more often than vervets were. The resources over which females were supplanted also differ between species. Supplants over food comprise smaller proportion of total supplants patas than for vervets. Patas appear to feed on less usurpable foods than vervets. We conclude that (1) Erythrocebus and Cercopithecus spp., except C. aethiops, should not be categorized with other Cercopithecinae, and C. aethiops should not be categorized with other Cercopithecus spp. and Erythrocebus, in discussions and analyses of relationships between females within groups and (2) ecological conditions, i.e., usurpability of foods, can override phylogenetic history as the selective pressure determining the nature of female competitive relationships within groups.     

Initiation of feeding by provisioned patas monkeys: Evidence for the protection hypothesis

The applicability of the baboon-based protection hypothesis was tested with data from a provisioned, free-ranging group of Erythrocebus patas.The age/sex class of the individual which first approached and fed from one of the food hoppers during early morning feeding sessions was noted for 114 mornings. The presence of an observer, and periodically, rhesus monkeys,near the hopper made these approaches analogous to progressions described for feral baboons. Adult patas of both sexes approached and ate first significantly more frequently than was expected based on their respective proportions in the group, and immature monkeys less often. For adult females,initiating feeding was not correlated with dominance rank, although females in the middle and lower thirds of the hierarchy (n = 6 in each third) initiated feeding more frequently than did the females in the top third. The protection hypothesis accounts for the observed behavioral pattern, while explanations based on competitive exclusion and dominance relationships do not adequately account for the results.     

The ecology of the introduced patas monkey (Erythrocebus patas) population of Southwestern Puerto Rico

This paper presents the results of a study on the introduced, free-ranging patas monkey population of Southwestern Puerto Rico (SWPR). It describes information on the population size, social group composition, diet, daily ranging patterns, and patas home range during a 3 year period. The patas monkey population in the study area consisted of approximately 120 individuals in four heterosexual groups and several all-male bands. Within their home ranges (26.8 km²), the population density was 4.47 individuals/km². Home range size among the population's four heterosexual groups varied from 3.72 km² to 15.39 km², and minimum daily distance traveled ranged from 0.8–2.0 km. In general, the social structure and mating system of this population parallels what has been described for African populations. However, habitat use, ranging behavior, and the quality of intergroup interactions suggests that patas of this population exhibit territorial behavior. Am. J. Primatol. 45:351–365, 1998. © 1998 Wiley-Liss, Inc.     

The ontogeny of sex differences in the behavior of patas monkeys

Many studies of sex differences in primates have been based on small experimental groups of peers in which only a limited range of social behavior could be expressed. In addition, the first few months of life are often the focus of such studies, with relatively little attention paid to older juveniles. In this study, 11 male and 9 female juvenile patas monkeys, living in a captive social group with all age-sex classes available, were observed between 1 and 4 years of age. A subset of seven patas monkeys was also observed between birth and 1 year of age. Here, we report the development of sex differences in independence, play, grooming, positioning behavior, and aggression over the juvenile period. Juvenile male patas monkeys played more and in longer bouts than females, but wrestling (rough-and-tumble play) was not more common among males. There were few differences in behaviors directed to male and female juveniles by other group members. Distinct differences emerged only in the behaviors of the juveniles themselves, with females being more active participants in social and aggressive interactions than males. In general, sex differences in patas monkeys show a mixture of patterns, some of which are predictive of adult sex differences and some of which appear to be specific to the particular demands of the juvenile period in this species     

Blood values of free-ranging patas monkeys (Erythrocebus patas)

Free-ranging patas monkeys (Erythrocebus patas) from El Guayacán island, Puerto Rico, were surveyed to establish values for the hemogram, serum biochemicals, calcium, and phosphorus. Results were tabulated for males and nonpregnant/nonlactating, pregnant, and lactating females. A summary of blood values from previous studies on captive patas monkeys was also tabulated for comparison.     

Body mass distribution and gait mechanics in fat-tailed dwarf lemurs (Cheirogaleus medius) and patas monkeys (Erythrocebus patas)

Most quadrupeds walk with lateral sequence (LS) gaits, where hind limb touchdowns are followed by ipsilateral forelimb touchdowns. Primates, however, typically walk with diagonal sequence (DS) gaits, where hind limb touchdowns are followed by contralateral forelimb touchdowns. Because the use of DS gaits is nearly ubiquitous among primates, understanding gait selection in primates is critical to understanding primate locomotor evolution. The Support Polygon Model [Tomita, M., 1967. A study on the movement pattern of four limbs in walking. J. Anthropol. Soc. Nippon 75, 120-146; Rollinson, J., Martin, R.D., 1981. Comparative aspects of primate locomotion, with special reference to arboreal cercopithecines. Symp. Zool. Soc. Lond. 48, 377-427] argues that primates' use of DS gaits stems from a more caudal position of the whole-body center of mass (COM) relative to other mammals. We tested the predictions of the Support Polygon Model by examining the effects of natural and experimental variations in COM position on gait mechanics in two distantly related primates: fat-tailed dwarf lemurs (Cheirogaleus medius) and patas monkeys (Erythrocebus patas). Dwarf lemur experiments compared individuals with and without a greatly enlarged tail (a feature associated with torpor that can be expected to shift the COM caudally). During patas monkey experiments, we experimentally shifted the COM cranially with the use of a weighted belt (7-12% of body mass) positioned above the scapulae. Examination of limb kinematics revealed changes consistent with systematic deviations in COM position. Nevertheless, footfall patterns changed in a direction contrary to the predictions of the Support Polygon Model in the dwarf lemurs and did not change at all in the patas monkey. These results suggest that body mass distribution is unlikely to be the sole determinant of footfall pattern in primates and other mammals.     

Foraging strategies of yakushima macaques(Macaca fuscata yakui)

I investigated the activity budget and diet of Yakushima macaques (Macaca fuscata yakui,)in warm temperate broad- leaved forest of Yakushima, Japan. Both time spent feeding and time spent moving varied considerably between half- months. However, total time spent in active behaviors— feeding time plus moving time— was stable. The composition of the diet also showed considerable variation between half- months. The macaques fed mainly on fruits, seeds,mature leaves, fallen seeds, flowers, and young leaves, each of which accounted for more than 30% of feeding time in at least 1 half- month. They also ate insects and fungi, but each of them comprised ≤ 25 and ≤ 8% of feeding time in any half- month, respectively. Time spent feeding on mature leaves, young leaves, flowers, or fallen seeds is positively correlated with total time feeding and is negatively correlated with time moving. In contrast, time feeding on fruits, seeds, insects or fungi is negatively correlated with time feeding and is positively correlated with time moving. Foraging on foods that have a low energy content, a high density, and a relatively even distribution— mature leaves— or that need much manipulation to be processed— flowers and fallen seeds— increased feeding time, while foraging on foods for which monkeys must search intensively in the forest— fruits, seeds, insects, and fungi— led to increased moving time. I examined foraging strategies of Yakushima macaques in terms of moving costs and the quality of food items. Regarding time feeding on fruits, which have more energy and may need less manipulation than other foods, as a benefit, and moving time as a cost, they seemed to employ a strategy that balanced the costs and benefits of foraging.     

Life-history parameters of a wild group of West African patas monkeys (Erythrocebus patas patas)

Based on long-term, although intermittent, observations (2 years 4 months of 14 years), we present data on birth seasonality, age at first birth, interbirth intervals, mortality rates, age at first emigration, and population change of a wild population of West African patas monkeys (Etythrocebus patas patas) in northern Cameroon. Birth season was from the end of December until the middle of February, corresponding to the mid-dry season. In spite of large body size, the patas females had the earliest age at first birth (36.5 monthsold) and the shortest interbirth intervals (12 months) compared to the closely related wild forest guenons. Age at first emigration of the males was considered to occur between 2.5 and 4.5 years. The group size of the focal group drastically decreased between 1984 and 1987, and steadily increased until 1994, then decreased again in 1997. The neighboring group also showed a similar trend in group size. The population decreases were likely to be caused by drought over 3 years. Annual crude adult mortality rate was 4% during population increase periods (PIP) between 1987 and 1994. It rose to 22% during all the periods (AP), including drought over 3 years. Despite their smaller body size, the rate of the wild forest guenons (Cercopithecus mitis) (4%) was the same and much lower than those of the patas during PIP and AP, respectively. The annual average juvenile mortality rate was 13% during PIP and it also rose to 37% during AP. That of wild forest guenons (C. ascanius) (10–12%) was a little lower and much lower than those of the patas during PIP and AP, respectively. These findings were consistent with Charnov's theoretical model of mammalian life-history evolution in that patas with high adult and juvenile mortality showed early and frequent reproduction in spite of large body size. Charnov also considered high adult mortality as a selective force and high juvenile mortality as a density-dependent consequence of high fecundity. Our results support the former but not the latter research findings.