Diet for a small primate: Insectivory and gummivory in the (large) patas monkey (Erythrocebus patas pyrrhonotus)

A 17 month field study of unprovisioned patas monkeys (Erythrocebus patas pyrrhonotus) in Laikipia, Kenya, using both ad libitum and scan sampling techniques, revealed that the diet of patas monkeys consists primarily of gum of Acacia drepanolobium, arthropods (both free-living and concentrated in the swollen thorns of A. Drepanolobium), and other animals. This type of diet is normally found only in smaller-bodied primates. Results from vegetational transects suggest that the larger-bodied patas monkey can subsist on such a diet because gum and arthropods are relatively easily found in their habitat, thereby minimizing search time. Patas monkeys also spend more time moving and less time feeding (while not moving) than other Old World primates. The characteristic long limbs of patas may have evolved in response to feeding on small, nonusurpable, and widely distributed foods, in which access to foods is maximized while time and energy spent in terrestrial travel between food sites are minimized. Am. J. Primatol. 45:381–398, 1998. © 1998 Wiley-Liss, Inc.     

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.     

Foraging energetics in patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus): implications for reproductive seasonality

The patas monkeys (Erythrocebus patas) in Kala Maloue, Cameroon, have their birth season in the mid-dry season, whereas closely related, sympatric tantalus monkeys (Cercopithecus aethiops tantalus) have their birth season in the wet season. To evaluate the optimality of a species-specific birth season, I estimated the daily intake of available energy and gross protein, and energy expenditure for one individual of each sex of each species between respective birth and mating seasons. The monkeys obtained a larger amount of available energy and gross protein in the birth season than in the mating season. No significant seasonal differences in energy expenditure between the birth and mating season were found. Thus, the birth season appears to be timed to the season when the monkeys can obtain more surplus energy and protein. Interspecific differences in the optimality of birth season were attributed to widely exploitative foraging, supported by the patas' high locomotive ability, which may enable them to obtain more energy from seeds of Acacia seyal and gums of A. sieberiana, and more protein from grasshoppers and seeds of A. seyal in the mid-dry season than the tantalus monkeys. A review of preceding studies suggests that the availability of seeds of Acacia fruiting during the dry season may exert the dominant influence on timing of birth not only in patas but also in savanna monkeys (Cercopithecus aethiops), which include the tantalus monkeys.     

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.     

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.     

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.     

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.     

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.     

Sexual harassment among captive patas monkeys (Erythrocebus patas)

Observations of the sexual harassment occurring within a captive group of patas monkeys are reported. Immature males performed most harassing attacks, while immature and adult females were infrequent harassers. The adult male of the group appeared to be the object of the majority of attacks, and on occasion the male’s copulatory behavior was modified by harassment. It is hypothesized that the harassing attacks performed by immature patas monkeys may be based upon (a) the excitatory effect of witnessing adult sexual interactions, and (b) the approach/withdraw conflict experienced during close approach to the adult male. The preservation of the one-male group structure is suggested as a possible function of sexual harassment.     

Observations of parturition among captive patas monkeys (Erythrocebus patas)

Six cases of labor and delivery by laboratory-housed patas monkeys (Erythrocebus patas) are described. Five of the births occurred during the daytime, and the sixth occurred just after the usual “lights out” time. Although it was impossible to determine the actual onset of labor, the final 1.5–0.5 hr before parturition were observed in all cases. Throughout labor, females tended to begin a contraction every 2–4 min and contractions usually lasted 35–60 sec. Females did not show common patterns of change in contraction frequency or duration as birth neared. It was not possible to describe patas monkey labor and delivery in terms of “stages.” Postpartum, females typically began cleaning their infants within 90 sec and picked them up within 5 min. Placental delivery times varied among females, as did the extent of placental consumption. One “mother-only” - reared female proved to be an inadequate mother.     

Allomaternal behavior in a group of free-ranging patas monkeys

A free-ranging group of patas monkeys (Erythrocebus patas) containing 18 individually identifiable adult females was observed for approximately 400 hours, equally distributed over two two-month periods corresponding to the breeding and birth seasons, at the La Parguera facility of the Caribbean Primate Research Center. The large number of infants born in the spring and early summer (n = 14) allowed for detailed observations of alloparental behaviors, with a focus on allomothering by the adult females. Seven types of alloparental behaviors were recorded: contact, nuzzling, grooming, agonism, close visual inspection, attempted kidnapping, and kidnapping. Adult females emitted the vast majority of allomaternal behavior, the patterning and frequency of which closely resembled the patterning and frequency of inter-adult female social grooming. Relative dominance status of the participants did not consistently predict the directionality of allomothering. The most commonly observed allomaternal behaviors were contact and nuzzling, which are primarily affiliative behaviors; agonism was rare. Successful kidnapping occurred eight times. Immature monkeys (n = 22) emitted an additional 32 alloparental acts. A propensity towards allomothering by experienced females would be most beneficial to patas infants due to the patas' tendency towards dispersed foraging and rapid flight in the presence of danger. It is possible that direct competition with groups of rhesus macaques for available resources on the island served as a proximal cause for the allomothering observed in this patas group.     

Diurnal births and perinatal behavior among wild patas monkeys: Evidence of an adaptive pattern

Data from a 2-year field study of patas monkeys (Erythrocebus patas) in Kenya support our earlier suggestion that diurnal births are a species-typical pattern of patas. In this respect patas are very unusual, as all existing information shows that nocturnal births are typical of both captive and freeranging monkeys. Patas do not give birth at night because to do so would render ineffective their night-resting strategy which reduces vulnerability to predation at night. Giving birth during the day, however, does not eliminate the risk of being preyed on; nor are all times of day equally favorable for giving birth. Our field data suggest that a patas female gives birth at those times of day when she is least likely to lose contact with her group or to encounter predators.     

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.     

Differential habitat utilization by patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus) living sympatrically in northern Cameroon.

In order to obtain reliable evidence for differences in habitat preferences between two closely related savanna-dwelling primate species, namely, patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus), I collected data on vegetation and patterns of range use concurrently at a single study site, Kala Maloue, Cameroon, in a similar manner for a group of each species. Kala Maloue consisted of 64% grassland mostly dominated by Gramineae spp. and the rest was woodland. Tantalus monkeys showed preference for woodland, especially gallery forest, much more than did the patas irrespective of the season. Moreover, patas preferentially established their home range in grassland in the wet season. Interspecific and seasonal differences in habitat preferences could be interpreted on the basis of interspecific and seasonal differences in preferences for main food. In dry season, tantalus utilized water-containing areas at a frequency closely in proportion to the availability of such areas while the patas utilized water-containing areas more frequently than expected. This is because tantalus established a smaller home range along the river where water was never completely depleted throughout the dry season. Both the patas and the tantalus preferred woodland to grassland as sleeping sites possibly owing to predation avoidance. Both the daily travel distance per group weight and the home range size per group weight were greater for patas than for tantalus partly because of higher preference for grassland with low habitat quality in the case of patas. It is suggested, however, that high locomotive ability enabled patas to effectively utilize small and widely dispersed items of food such as grasshoppers and to explore areas with high availability of food and water and with preferable sleeping sites.     

An assessment of dominance and kinship among patas monkeys

Kaplan andZucker (1980) argued that dominance and kinship do not function as important organizing features for intragroup behavior and social structure among patas monkeys (Erythrocebus patas). This paper reviews the available data pertinent to this argument and concludes that dominance probably is not a reliable structural variable for captive patas, despite its clear development in most groups. In contrast, kinship is a major organizing feature that strongly affects allogrooming and other affiliative interactions, and socialization.     

Naturally occurring Yersinia enterocolitica septicemia in patas monkeys (Erythrocebus patas)

Two cases of Yersinia enterocolitica septicemia occurred in a breeding group of 22 adult patas monkeys (Erythrocebus patas). Affected animals had acute clinical signs of depression, weakness, dehydration, hypothermia, hepatomegaly and pronounced leukopenia. Both animals died a few hours after treatment was initiated. Gross necropsy findings included jaundice, fluid in body cavities, hepatomegaly, splenomegaly, multiple white foci within the liver and spleen, generalized lymph node enlargement and numerous mucosal ulcerations in the colon. Primary histopathological lesions were multifocal hepatic necrosis, splenic necrosis, chronic ulcerative enteritis and diaphragmatic myositis with necrosis and edema. Yersinia enterocolitica was cultured from the liver, spleen, lung, jejunum and rectum. Wild rodents, particularly mice, may have been a source of infection for these animals, as the monkeys were housed in a rural, indoor-outdoor facility. A preliminary culture survey showed that some clinically normal patas monkeys harbored the organism in their intestinal tracts.     

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     

Distribution and abundance of patas monkeys (Erythrocebus patas) in Laikipia, Kenya, 1979-2004

Patas monkeys may be especially vulnerable to local extinction because they live in relatively small, female-philopatric groups at low densities and are strongly polygynous. We assessed a patas monkey population in Kenya's 9,700 km(2) Laikipia District over 25 years, using data collected in 1979-1981 and 1992-2004. The data were based on intensive observations of three study groups, "on the ground" counts, and surveys of Laikipia residents. In 1979-1981, a minimum of 415 patas monkeys lived in 14-15 groups. By 2000, the best estimate suggested 310-445 patas monkeys living in 13-17 groups over a greater surveyed area, suggesting that patas monkeys in Laikipia may have undergone a slight decline in numbers over time. Their distribution, however, was similar over time. The relative stability of this population has likely been the result of beneficial co-existence with large-scale cattle ranching. Outside Laikipia, substantial habitat alteration from rising human populations has coincided with the near disappearance of patas monkeys where they were previously more numerous. The small population in Laikipia, probably the largest remaining in Kenya, may therefore be critical to the continued existence of patas monkeys in that country and may be dependent on maintenance of large-scale ranches. Such land use provides patas monkeys with water and broad expanses of Acacia drepanolobium woodlands, the habitat to which patas are restricted in Laikipia.     

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.