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.     

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.     

Demography and Life Histories of Sympatric Patas Monkeys, <Emphasis Type="Italic">Erythrocebus patas</Emphasis>, and Vervets, <Emphasis Type="Italic">Cercopithecus aethiops</Emphasis>, in Laikipia,Kenya

Mortality patterns are thought to be strong selective forces on life history traits, with high adult mortality and low immature mortality favoring early and rapid reproduction. Patas monkeys (Erythrocebus patas) have the highest potential rates of population increase for their body size of any haplorhine primate because they reproduce both earlier and more often. We report here 10 yr of comparative demographic data on a population of patas monkeys and a sympatric population of vervet monkeys (Cercopithecus aethiops), a closely related species differing in aspects of social system, ecology, and life history. The data reveal that 1) adult female patas monkeys have significantly higher mortality than adult female vervets; 2) infant mortality in patas monkeys is relatively low compared to the norm for mammals because it is not significantly different from that of adult female patas monkeys; and 3) infant mortality is significantly higher than adult female mortality in vervets. For both species, much of the mortality could be attributed to predation. An epidemic illness was also a major contributor to the mortality of adult female patas monkeys whereas chronic exposure to pathogens in a cold and damp microenvironment may have contributed to the mortality of infant vervets. Both populations experienced large fluctuations during the study period. Our results support the prediction from demographic models of life history evolution that high adult mortality relative to immature mortality selects for early maturation.     

Pattern of maternal circulating CRH in laboratory‐housed squirrel and owl monkeys

The anthropoid primate placenta appears to be unique in producing corticotropin‐releasing hormone (CRH). Placental CRH is involved in an endocrine circuit key to the production of estrogens during pregnancy. CRH induces cortisol production by the maternal and fetal adrenal glands, leading to further placental CRH production. CRH also stimulates the fetal adrenal glands to produce dehydroepiandrostendione sulfate (DHEAS), which the placenta converts into estrogens. There are at least two patterns of maternal circulating CRH across gestation among anthropoids. Monkeys examined to date (Papio and Callithrix) have an early‐to‐mid gestational peak of circulating CRH, followed by a steady decline to a plateau level, with a possible rise near parturition. In contrast, humans and great apes have an exponential rise in circulating CRH peaking at parturition. To further document and compare patterns of maternal circulating CRH in anthropoid primates, we collected monthly blood samples from 14 squirrel monkeys (Saimiri boliviensis) and ten owl monkeys (Aotus nancymaae) during pregnancy. CRH immunoreactivity was measured from extracted plasma by using solid‐phase radioimmunoassay. Both squirrel and owl monkeys displayed a mid‐gestational peak in circulating CRH: days 45–65 of the 152‐day gestation for squirrel monkeys (mean±SEM CRH=2,694±276 pg/ml) and days 60–80 of the 133‐day gestation for owl monkeys (9,871±974 pg/ml). In squirrel monkeys, circulating CRH declined to 36% of mean peak value by 2 weeks before parturition and then appeared to increase; the best model for circulating CRH over gestation in squirrel monkeys was a cubic function, similar to previous results for baboons and marmosets. In owl monkeys, circulating CRH appeared to reach plateau with no subsequent significant decline approaching parturition, although a cubic function was the best fit. This study provides additional evidence for a mid‐gestational peak of maternal circulating CRH in ancestral anthropoids that has been lost in the hominoid lineage. Am. J. Primatol. 72:1004–1012, 2010. © 2010 Wiley‐Liss, Inc.     

Comparing measures of travel distances in primates: Methodological considerations and socioecological implications

Travel costs can influence numerous aspects of the lives of primates, including net energy balance (and therefore reproductive success of females) and maximum group size. Despite their potential impact, there has been no systematic comparison of different measures of travel distance. We compared three measures of travel distance in 30 min (actual distance of individuals, straight‐line distance of individuals, and straight‐line distance of groups) and their ratios in a small group and a large group of vervet monkeys (Cercopithecus aethiops) and between the large group of vervets and a group of patas monkeys (Erythrocebus patas) of roughly similar size. The large group of vervets traveled farther than the small group regardless of the measure used, but the ratios of the different measures were not significantly different between those groups. Patas monkeys traveled significantly farther than the large group of vervets regardless of the measure used. In both vervets and patas, straight‐line distances of individuals (ISLD) and groups (GSLD) underestimated actual distances traveled by individuals (IAD), but the degree to which they did so differed between species. IAD is more accurate than the other two measures and is preferred for studies of energetics and individual reproductive success, although ISLD or GSLD may be substituted when the ratios of IAD/ISLD or IAD/GSLD do not differ between groups or species. The ratio of IAD/ISLD was larger in vervets than in patas, suggesting that individual vervets meander more over short periods of time than patas. The ratio of ISLD/GSLD was larger in patas than in vervets, suggesting that patas move at angles or across the group's center‐of‐mass whereas vervets move more consistently along with others in their group. This has implications for the formation of spatial subgroups and alliances within groups. Am. J. Primatol. 48:87–98, 1999. © 1999 Wiley‐Liss, Inc.     

A Catecholamine storage in the pancreatic A2-cells of owl monkey (Aotes trivirgatus)

Summary The fluorescence method ofFalck andHillarp was used to study the occurrence of biogenic monoamines in the islets of Langerhans of monkeys. A storage of a catecholamine was demonstrated in the A₂-cells of owl monkey, whereas no histochemically demonstrable amount of monoamines could be seen in the islet cells of marmoset,Rhesus monkey, squirrel monkey, andCebus monkey.Supported by grants from the Swedish Medical Research Council (No. B69-14x-712-04C) and by the National Institutes of Health (No. 06701-02).     

Hepatitis A and B: serologic survey of human and nonhuman primate sera

Sera of humans and seven species of nonhuman primates were tested by radioimmunoassay and enzyme immunoassay for the presence of hepatitis A antibody, hepatitis B surface antigen and antibody to hepatitis B surface antigen. The outcome of testing a total of 276 serum or plasma specimens was as follows: with the exception of squirrel monkeys (0%) and cotton-top marmosets (0%), a considerable percentage of all other species tested had detectable antibodies to hepatitis A virus: humans 45.9%, chimpanzees 36.6%, baboons 38.2%, vervets 57.9%, cebus monkeys 40.0% and common marmosets 50.0%. Only one human and two chimpanzees were carriers of hepatitis B surface antigen. Antibodies to hepatitis B surface antigen were detected in human (11.3%), chimpanzees (29.9%), baboons (36.2%) and squirrel monkeys (5%). Chimpanzees showed an increasing prevalence of antibodies to hepatitis A virus and hepatitis B surface antigen with age.     

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.     

Relation between phylogeny of African green monkey CD4 genes and their respective simian immunodeficiency virus genes

Abstract: An apparent species-specific relatedness of SIV_agm suggests a coevolution with their natural hosts. However, the exact species or subspecies classification of African green monkeys, AGM, is uncertain because current classification schemes rely on phenotype markers, while more definitive genetic data are lacking. In this study, the CD4 protein involved in tissue type recognition was genetically cloned and sequenced from PBMC RNA from all AGM species, including Barbados green monkeys (BGM). Phylogenetic trees were constructed that also included genomic CD4 nucleotide sequences from patas, sooty mangabeys, rhesus and pig-tail macaques, chimpanzees, and humans. Chimpanzees and humans consistently clustered together. Monkeys within the Cercopithecus genus formed a separate cluster which included pata monkeys, supporting its grouping as a member of Cercopithecus. Surprisingly, sooty mangabeys were genetically more closely related to Asian macaques than to other African species, which might explain why macaques are more susceptible to infection by the SIV_sm group than to infection by SIV_agm or HIV-1 and why patas, on the other hand, are highly susceptible to SIV_agm infection. Based on CD4 genetic data, tantalus, vervets, grivets, and sabaeus formed separate subgroups with BGM grouping closely with vervets. The branching order of the AGM species was related to that of their respective SIV_agm env sequences. The study suggests a strong correlation between CD4 phylogeny and the susceptibility of the host species to infection by a specific lentivirus and supports the assumption of a coevolution of SIV_agm and AGM. CD4 sequencing is suggested as a relevant method for genetic determination of primate species.     

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.     

Serum and urine biochemical diversity among adult wild-caught Aotus nancymae and Saimiri peruviensis

Serum and urine analytes were compared between adult wild-caught owl monkeys (Aotus nancymae) and adult wild-caught squirrel monkeys (Saimiri peruviensis) to determine if normative clinical pathology data were similar. An objective of the study was to confirm that species of neotropical primates are distinct with regard to physiologic parameters, and should not be considered interchangeable in biomedical research. Significant differences (P < 0.05) were noted in many serum and urine analytes between the two groups. The results suggest that reference data for wild-caught owl monkeys are not applicable to squirrel monkeys, and the differences are sufficiently large to be of clinical significance. These findings illuminate the diversity among species of neotropical primates.     

First skull of Antillothrix bernensis,an extinct relict monkey from the Dominican Republic

The nearly pristine remains of Antillothrix bernensis, a capuchin-sized (Cebus) extinct platyrrhine from the Dominican Republic, have been found submerged in an underwater cave. This represents the first specimen of an extinct Caribbean primate with diagnostic craniodental and skeletal parts in association, only the second example of a skull from the region, and one of the most complete specimens of a fossil platyrrhine cranium yet discovered. Cranially, it closely resembles living cebines but is more conservative. Dentally, it is less bunodont and more primitive than Cebus, with crowns resembling Saimiri (squirrel monkeys) and one of the oldest definitive cebines, the late Early Miocene Killikaike blakei from Argentina. The tricuspid second molar also resembles the enigmatic marmosets and tamarins, whose origins continue to present a major gap in knowledge of primate evolution. While the femur is oddly short and stout, the ulna, though more robust, compares well with Cebus. As a member of the cebid clade, Antillothrix demonstrates that insular Caribbean monkeys are not monophyletically related and may not be the product of a single colonizing event. Antillothrix bernensis is an intriguing mosaic whose primitive characters are consistent with an early origin, possibly antedating the assembly of the modern primate fauna in greater Amazonia during the La Venta horizon. While most Greater Antillean primate specimens are quite young geologically, this vanished radiation, known from Cuba (Paralouatta) and Jamaica (Xenothrix) as well as Hispaniola, appears to be composed of long-lived lineages like several other mainland clades.     

Capture,immobilization, and Global Positioning System collaring of olive baboons (Papio anubis) and vervets (Chlorocebus pygerythrus): Lessons learned and suggested best practices

As the value of Global Positioning System (GPS) technology in addressing primatological questions becomes more obvious, more studies will include capturing and collaring primates, with concomitant increased risk of adverse consequences to primate subjects. Here we detail our experiences in capturing, immobilizing, and placing GPS collars on six olive baboons (Papio anubis) in four groups and 12 vervet monkeys (Chlorocebus pygerythrus) in five groups in Kenya. We captured baboons with cage traps and vervets with box traps, immobilized them, and attached GPS collars that were to be worn for 1 year. Adverse consequences from the trapping effort included incidental death of two nonsubjects (an adult female and her dependent infant), temporary rectal prolapse in one baboon, superficial wounds on the crown of the head in two vervets, and failure to recapture/remove collars from two baboons and two vervets. Obvious negative effects from wearing collars were limited to abrasions around the neck of one vervet. A possible, and if so, serious, adverse effect was greater mortality for collared adult female vervets compared with known uncollared adult female vervets, largely due to leopard (Panthera pardus) predation. Collared animals could be more vulnerable to predation because trapping favors bolder individuals, who may also be more vulnerable to predation, or because collars could slow them down or make them more noticeable to predators. Along with recommendations made by others, we suggest that future studies diversify trapping bait to minimize the risk of rectal prolapse, avoid capturing the first individuals to enter traps, test the movement speeds of collared versus noncollared animals, include a release system on the collars to avoid retrapping failure, and publish both positive and negative effects of capturing, immobilizing, and collaring.     

Phylogeny of African monkeys based upon mitochondrial 12S rRNA sequences

The suborder Anthropoidea of the primates has traditionally been divided in three superfamilies: the Hominoidea (apes and humans) and the Cercopithecoidea (Old World monkeys), together comprising the infraorder Catarrhini, and the Ceboidea (New World monkeys) belonging to the infraorder Platyrrhini.We have sequenced an approximately 390-base-pair part of the mitochondrial 12S rRNA gene for 26 species of the major groups of African monkeys and apes and constructed an extensive phylogeny based upon DNA evidence. Not only is this phylogeny of great importance in classification of African guenons, but it also suggests rearrangements in traditional monkey taxonomy and evolution. Baboons and mandrills were found to be not directly related, while we could confirm that the known four superspecies of mangabeys do not form a monophyletic group, but should be separated into two genera, one clustering with baboons and the other with mandrills. Patas monkeys are clearly related to members of the genus Cercopithecus despite their divergence in build and habitat, while the talapoin falls outside the Cercopithecus clade (including the patas monkey). Correspondence to: A.C. van der Kuyl     

Development of the ocular adrenergic nerve supply in man and guinea-pig

Summary The development of adrenergic nerves to the anterior eye segment was studied in human and guinea-pig embryos. Adrenergic terminals had already appeared in the earliest human embryos available (4–6 cm). They first appeared mainly in nerve trunks in the primitive chorioid, especially in the region of the developing ciliary body. Adrenergic nerves then grow into different structures of the eye as these develop, but typical terminals in contact with effector cells appeared late during the development, about the 25–30 cm stage. No adrenergic nerves were observed in the chamber angle. Corneal adrenergic nerves (also intraepithelial terminals) appeared much more frequently in embryos than in adults. No adrenergic neurons were observed in the retina. In the guinea-pig, the first adrenergic fibres were observed at about gestation day 35. The general principle of the development was very similar to that of the humans. At gestation day 45 to 50, the supply of adrenergic fibres was essentially that of the adult animal, except that the corneal adrenergic fibres were increasing until just before birth and that the adrenergic terminals of the chamber angle appeared shortly before term.This work was supported by grants from the Association for the Aid of Crippled Children, H. Hiertas Stiftelse, and the Swedish Medical Research Council (Project no. B71-14X-2321-05B).     

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.     

Comparative anatomy and histology of the cervix uteri in non-human primates

The uterine cervix of rhesus macaque, crab-eating macaque, stump-tailed macaque, pig-tailed macaque, marmoset, baboon, patas, and squirrel monkeys was studied macroscopically and microscopically. Distribution of spermatozoa and leukocytes in the lumen and within the crypts and clefts was studied in rhesus and marmoset uterine cervix. The cervical canal of baboon, patas, marmoset, and stump-tailed monkeys is straight or slightly bent. The presence of variably developed ventral and dorsal colliculi in rhesus, crab-eating, and pig-tailed macaques causes the dorsoventral sinuosity of the cervical canal. The cervix of all investigated specimens is fundamentally fibrous tissue and the amount of muscle fibers increases toward the uterine corpus. The cervical mucosa of baboon, marmoset, and patas monkeys contains a large amount of clefts and tubular tunnels of variable structure, length, width, direction, and degree of branching. The cervical mucosa of macaques contains a large number of crypts of complex structure, length, width and degree of branching. The cervical crypts in macaques are usually longer in the ectocervix; whereas, in the midcervix, mucosa contains small crypts, clefts and long tunnels. Squamo-columnar junction is located near the external os in baboon, patas, marmoset, rhesus, crab-eating, and pig-tailed monkeys. In squirrel monkey, squamous epithelium is continuous through the external os, covers the vestibule and external surface of the cervical colliculi. In stump-tailed macaque, squamo columnar junction is located in the vagina, 1–3 cm from the external os of the cervix. The vaginal wall between the squamo-columnar junction and the external os of the cervix is covered with heavily branched mucosa lined with columnar epithelium. Ciliated cells of cervical epithelium occur in 9 to 19%. A large number of spermatozoa and a relatively low number of leucocytes have been found within crypts and clefts of cervical mucosa. The results are discussed in relation to the function of the cervix in different stages of the cycle, during pregnancy and parturition.This investigation was supported in part by Ford Foundation Grant No. 710-0287.     

Paracoccidioidomycosis in wild monkeys from Paraná State, Brazil

The aim of this study was to evaluate the seroprevalence of Paracoccidioides brasiliensis infection in wild New World monkeys (Cebus sp. and Alouatta caraya). A total of 93 animals (Cebus sp., n = 68 and Alouatta caraya, n = 25) were captured in the Paraná River basin, Paraná State, Brazil and the serum samples were analyzed by ELISA and immunodiffusion using P. brasiliensis gp43 and exoantigen as antigens, respectively. The seropositivity observed by ELISA was 44.1% and 60% for Cebus sp. and A. caraya, respectively, while by immunodiffusion test Cebus sp. showed positivity of 2.9% only. No significant difference was observed in relation to age and sex. This is the first report of paracoccidioidomycosis in wild capuchin monkeys and in wild-black and golden-howler monkeys. The high positivity to P. brasiliensis infection in both species evaluated in our study and the positivity by immunodiffusion test in Cebus sp. suggest that natural disease may be occurring in wild monkeys living in paracoccidioidomycosis endemic areas.     

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.