Time budgets ofMacaca mulatta

We measured the amount of time that 20 rhesus monkeys,Macaca mulatta, (four adult males, 10 adult females, four juvenile males, and two juvenile females) contained in two enclosed social groups devoted to 16 activities. For 14 of these 16 behaviors we found significant differences between age-sex classes. For 14 behaviors, there were also differences between individual monkeys. Twelve of the 16 activities showed significant diurnal variations. We discuss the relation between the use of time and social position, the adaptive significance of diurnal variation, and compare our data with that available for free ranging rhesus.     

The human Duffy blood group in rhesus monkeys1

There is good evidence that susceptibility to Plasmodium vivax infection and to P. knowlesi erythrocyte invasion is influenced by certain human Duffy (Fy) blood group antigens. Since P. knowlesi readily infects rhesus monkeys (Macaca mulatto), it was not surprising to find an Fy-like antigen on rhesus erythrocytes. Using human Fy antisera in elution and absorption experiments, we found that all 40 rhesus monkeys tested displayed the Fy(a-b +) phenotype. Furthermore, the rhesus Fy^bantigen was inactivated by chymotrypsin but not by trypsin, suggesting that it is homologous to the human Fy^bantigen. Preliminary serological analyses and enzyme hydrolysis experiments suggest that none of the 13 blood group systems that we have described in rhesus are analogous to the human Fy system. Thus, it appears that there is no Duffy-like polymorphism in rhesus monkeys.     

Fetotoxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) for rhesus macaques (Macaca mulatta)

The fetotoxic and teratogenic potential of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) for rhesus macaques (Macaca mulatta) was tested through oral administration to monkeys early in pregnancy. A single or divided dose, 1 μg of TCDD/kg of body weight, was followed by abortion in 13 of 16 pregnant monkeys treated between days 20 and 40 of gestation. One of four aborted at 0.2 μg/kg, and two of two at 5 μg/kg. None of the mothers given 0.2 μg/kg showed signs of toxicity. Eight of the monkeys aborting at 1 μg/kg showed clinical toxicity 44 to 111 days after aborting, and three died. Both given 5 μg/kg became toxic soon after abortion and died. No malformations except for two minor palatal abnormalities of questionable significance were found in the six fetuses that were not aborted at doses of 0.2 and 1.0 μg/kg. These results indicate (1) that TCDD is fetotoxic at doses that frequently have delayed toxicity to the mother, but that conclusions about teratogenicity cannot be drawn, and (2) that pregnant rhesus females are more sensitive to the toxic effects of TCDD than any species tested but the guinea pig.     

Inoculation of baboons and macaques with simian immunodeficiency virus/Mne, a primate lentivirus closely related to human immunodeficiency virus type 2

A primate lymphotropic lentivirus was isolated on the human T-cell line HuT 78 after cocultivation of a lymph node from a pig-tailed macaque (Macaca nemestrina) that had died with malignant lymphoma. This isolate, originally designated M. nemestrina immunodeficiency virus (MnIV) and now classified as simian immunodeficiency virus (SIV/Mne), was inoculated intravenously into three juvenile rhesus monkeys (Macaca mulatta), three juvenile pig-tailed macaques (M. nemestrina), and two juvenile baboons (Papio cynocephalus). All six macaques became viremic by 3 weeks after inoculation, whereas neither of the baboons developed viremia. One pig-tailed macaque died at 15 weeks with suppurative peritonitis secondary to ulcerative, necrotizing colitis. Immunologic abnormalities included a marked decrease in CD4+ peripheral blood lymphocytes. Although five macaques mounted an antibody response to SIV/Mne, the animal that died at 15 weeks remained antibody negative. Three other macaques (two rhesus and one pig-tailed) died 66 to 87 weeks after inoculation after exhibiting progressive weight loss, anemia, and diarrhea. Histopathologic findings at necropsy included various manifestations of immune deficiency, nephropathy, subacute encephalitis, pancreatitis, adenocarcinoma, and lymphoid atrophy. SIV/Mne could be readily isolated from the spleens and lymph nodes of all necropsied macaques, and from the cerebrospinal fluid, brains, bone marrow, livers, and pancreas of some of the animals. SIV antigens were localized by avidin-biotin immunohistochemistry to pancreatic islet cells and to bone marrow endothelial cells. The data suggest that African baboons may be resistant to infection by SIV/Mne, whereas Asian macaques are susceptible to infection with this pathogenic primate lentivirus.     

Lipofuscin in the corpus luteum of macaque ovaries

The present study examined the histochemistry of pigments in the corpus luteum of the ovaries of cynomolgus monkeys (Macaca fascicularis), Japanese monkeys (Macaca fuscata), and rhesus monkeys (Macaca mulatta). Yellowish brown pigments were found in the regressing corpus luteum cells. Histochemical studies revealed that these pigments consisted of lipofuscin, the so-called age pigment. The findings obtained suggest that accumulation of lipofuscin might be related to cellular aging of the corpus luteum.     

The distribution pattern of rhesus and Assamese monkeys in Nepal

Surveys of the distribution and some ecological characteristics of rhesus monkeys (Macaca mulatta) and Assamese monkeys (M. assamensis) in Nepal were conducted during 234 days in 1976, 1978, and 1984. Rhesus monkeys dominated in the tropical, subtropical, and temperate forests below 3,000 m a.s.l. all over Nepal. Assamese monkeys were patchily distributed along rivers in the tropical and subtropical areas. Both species principally utilized forests parapatrically. The mean troop size of rhesus monkeys (29.5) was significantly larger than that of Assamese monkeys (19.1). Discontinuous distribution of Assamese monkeys probably appeared as a result of the expansion of rhesus monkey distribution in the mid- and late-Pleistocene. Because of small distribution areas and small numbers of monkeys, urgent conservation policy must be pursued.     

A test of the randomness of paternity of members of maternal sibships in six captive groups of rhesus monkeys (Macaca mulatta)

Results of previous studies have shown that in captive groups of rhesus monkeys (Macaca mulatto)fathers associate more frequently with their own offspring than with those of other males and that mothers are most permissive of physical contact between their own infant and a juvenile when that juvenile shares the same father with her infant. These two observations suggest that the identity of offspring born in captive groups of rhesus monkeys is recognized by at least some adult members of the group. Consistent patterns of mating among mating seasons might explain this apparent recognition of offsprings’ paternity. Fathers, for example, might regularly associate with young who maintain a close relationship with females with whom they have previously mated, and mothers might selectively permit juveniles who maintain a close relationship with males with whom they have previously mated to associate with their infants. This hypothesis is tested in this paper by comparing the observed distribution of 70 maternal sibships, members of which were fathered by the same or by different adult males over a 4-year period in six captive groups of rhesus monkeys, with that distribution expected based on random mating from season to season. Seasonal mating patterns were found to be random. Preparations are now underway to test this hypothesis in several free-ranging groups.     

Conservation note: Socioecology and conservation of macaques and langurs in Varanasi,India

A survey of rhesus monkeys (Macaca mulatta) and hanuman langurs (Presbytis entellus) was conducted in urban and forest areas of Varanasi, India. Data were collected on group size and composition. Nine groups of rhesus monkeys inhabited various urban niches, but langurs were completely absent from urban areas. Approximately 159 rhesus monkeys and 720 langurs lived in the forested area. Both the urban and the forested habitats of this area are being reduced in size, and it is suggested that these populations be moved to nearby forest preserves.     

Video-task acquisition in rhesus monkeys (Macaca mulatta) and chimpanzees (Pan troglodytes): A comparative analysis

This study describes video-task acquisition in two nonhuman primate species. The subjects were seven rhesus monkeys (Macaca mulatta) and seven chimpanzees (Pan troglodytes). All subjects were trained to manipulate a joystick which controlled a cursor displayed on a computer monitor. Two criterion levels were used: one based on conceptual knowledge of the task and one based on motor performance. Chimpanzees and rhesus monkeys attained criterion in a comparable number of trials using a conceptually based criterion. However, using a criterion based on motor performance, chimpanzees reached criterion significantly faster than rhesus monkeys. Analysis of error patterns and latency indicated that the rhesus monkeys had a larger asymmetry in response bias and were significantly slower in responding than the chimpanzees. The results are discussed in terms of the relation between object manipulation skills and video-task acquisition.     

Vitamin C deficiency in captive nonhuman primates fed commercial primate diet

Scurvy was diagnosed in 19 rhesus monkeys (Macaca mulatta) and four squirrel monkeys (Saimiri sciureus) from a colony of nonhuman primates maintained on a commercial diet. Signs of weakness, reluctance to move, gingival hemorrhage, bruising, proximal and distal metaphyseal fractures, weight loss and anemia appeared in juvenile and young adult rhesus monkeys over a 2 week period. Clinical signs subsided after 5 days of vitamin C therapy. At the same time, cephalohematomas and weakness developed in squirrel monkeys, which failed to respond to treatment. These cases were associated with manufacturer's admitted error in preparation of the commercially prepared monkey diet.     

Use of a radioreceptorassay (RRA) for human luteinizing hormone/chorionic gonadotropin (hLH/CG) for detection of early pregnancy and estimation of time of ovulation in macaques

A radioreceptorassay (RRA) for macaque luteinizing hormone (LH)/chorionic gonadotropin (CG) was adapted from the clinical RRA for human LH/CG, Biocept-G?, for the purposes of detection of pregnancy prior to day 20 of gestation and for estimation of the time of ovulation in macaques. The 90-min assay procedure was simple, accurate, and reliable. Seventy-five rhesus monkeys (Macaca mulatta) and 20 crab-eating monkeys (Macaca fascicularis) were tested for the presence of CG in the serum on estimated days 17–20 of pregnancy. Of a total of 160 tests, four false negative and 0 false positive tests were obtained, for an accuracy of 97.5%. The preovulatory LH peak was detected in 19 rhesus monkeys by semiquantitative RRA of LH/CG. Ovulation was confirmed in these 19 animals by the presence of a fresh corpus luteum at laparotomy 2–10 days after ovulation, collection of an embryo, pregnancy, or subsequent cycle history. The short, simple assay procedure and the low inter-and intraassay coefficients of variation (7.3 and 3.7%, respectively) allow use of this assay in an economical, predictive, as well as retrospective, capacity for estimation of the time of ovulation in rhesus monkeys. The sensitivity, reliability, species nonspecificity, simplicity, and rapidity of performance of this RRA for LH/CG are features which add up to a useful new management tool for breeding macaques for research purposes.     

The monkey's perspective

The sequencing of the genome of a female rhesus macaque (Macaca mulatta) of Indian origin will provide us with biomedical and evolutionary insights into both humans and Old World monkeys.     

How laboratory-raised Japanese monkeys (Macaca fuscata) perceive rotated photographs of monkeys: Evidence for an inversion effect in face perception

Five laboratory-raised Japanese monkeys (Macaca fuscata) were presented various types of photographs of Japanese and rhesus monkeys (Macaca mulatta) in upright, horizontal, and inverted orientations in a sensory-reinforcement experiment. The ratio of the duration of potential viewing time for the photographs which the subjects controlled to the interval between subject-controlled presentations of them (the D/I score) was used as a measure of preference for the photographs. When inverted photographs were presented, the D/I scores were lower than for upright photographs. The difference in D/I scores between photographs of the two species, which indicated discriminability between them, also diminished when the photographs were inverted. The results obtained suggest an inversion effect in face perception in macaque monkeys.     

Do young rhesus macaques know what others see?: A comparative developmental perspective

Humans undergo robust ontogenetic shifts in the theory of mind capabilities. Are these developmental changes unique to human development or are they shared with other closely related non-human species? To explore this issue, we tested the development of the theory of mind capacities in a population of 236 infant and juvenile rhesus macaques (Macaca mulatta). Using a looking-time method, we examined what developing monkeys know about others’ perceptions. Specifically, we tested whether younger monkeys predict that a person will reach for an object where she last saw it. Overall, we found a significant interaction between a monkey's age and performance on this task (p = .014). Juvenile monkeys (between two and 5 years of age) show a nonsignificant trend towards human infant-like patterns of performance, looking longer during the unexpected condition as compared to the expected condition, though this difference is nonsignificant (p = .09). However, contrary to findings in human infants, infant rhesus macaques show a different trend. Infant monkeys on average look slightly longer on average during the expected condition than the unexpected condition, though this pattern was not significant (p = .06). Our developmental results in monkeys provide some hints about the development of the theory of mind capacities in non-humans. First, young rhesus macaques appear to show some interest in the perception of other agents. Second, young rhesus seems able to make predictions based on the visual perspective of another agent, though the developmental pattern of this ability is not as clear nor as robust as in humans. As such, though an understanding of others’ perceptions is early-emerging in human infants, it may require more experience interacting with other social agents in our non-human relatives.     

Polyspecific groups of macaques on the kowloon peninsula,new territories,Hong Kong

Three polyspecific groups of free-ranging macaques were observed in July and August of 1980 and 1981 in the forests of the New Territories of mainland Hong Kong. Two groups were composed of rhesus monkeys (Macaca mulatta) and long-tailed or crab-eating monkeys (M. fascicularis), and one group was composed of both the former plus Japanese macaques (M. fuscata). All three groups contained hybrids between M. mulatta and M. fascicularis. This combination of species within the same social group is an unusual circumstance in natural habitats, and it offers a unique opportunity for field studies in primate ecology and behavior.     

Study of capability for recognition of complex visual stimuli of different quantities in the lower monkeys

Capability of monkeys for identification of quantitative signs has been studied at recognition and comparison of two-and three-dimensional objects in quantities from 1 to 8. The work was carried out on two species of the lower monkeys: rhesus macaque (Macaca mulatto) and brown capuchins (Cebus apella). The studied representatives of the monkeys have been established to be able to differentiate planar images and casts of cherries in various quantity combinations from 1 to 8 and to identify identical signs of visual stimuli. The obtained data indicate the ability of monkeys to abstract and to form preverbal notions of quantitative signs of objects.     

Fatal outbreaks of proliferative enteritis caused by Lawsonia intracellularis in young colony-raised rhesus macaques.

Ten juvenile rhesus monkeys (Macaca mulatta) died acutely in two separate disease outbreaks. The animals had segmental thickening of the distal ileum with associated proliferative, rugous appearing mucosae. Microscopically, necrosis, exudative inflammation, mucosal ulceration, and crypt hyperplasia were present. Intracellular organisms were seen histochemically and ultrastructurally, and were confirmed to be Lawsonia intracellularis using a specific immunohistochemical method. Proliferative enteropathic conditions caused by L. intracellularis are reported in an ever-increasing range of hosts, suggesting that the infection may exist unrecognized in an even greater array of species, possibly including man.     

Midazolam as an effective intravenous adjuvant to prolonged ketamine sedation in young rhesus (Macaca mulatta) and Vervet (Cercopithecus aethiops sabaeus) monkeys: A preliminary report

The present study investigated a recently developed benzodiazepine, midazolam, as an intravenous adjuvant to ketamine in infant monkeys undergoing prolonged sedation during positron emission tomography of the brain and heart. Subjects were two rhesus macaque (Macaca mulatta) and ten vervet monkeys (Cercopithecus aethiops sabaeus) ranging in age from 26 to 260 days. Midazolam was an effective intravenous adjuvant to ketamine. This treatment regime resulted in complete immobilization of the animals. Ketamine infusion rates did not vary significantly with age for either species. Sensitivity to midazolam appeared to be age-dependent in vervets because significantly lower dose rates were sufficient to maintain anesthesia in older animals. For rhesus monkeys, midazolam dose rates decreased until approximately 4 months of age, and increased gradually thereafter. © 1993 Wiley-Liss, Inc.     

Primate phonation: Anterior cingulate lesion effects on response rate and acoustical structure

Four juvenile rhesus monkeys (Macaca mulatta) that were conditioned to emit a discriminative vocal response underwent unilateral and bilateral lesions of anterior cingulate gyrus in stepwise sequence. Pre- and post-lesion measures of vocal response rate and acoustical features (call duration, amplitude, and fundamental frequency) were obtained for the conditioned task and for vocalization in the home colony (spontaneous vocalization). Unilateral lesions produced little consistent change in spontaneous “coo” vocalization rate and call duration. Conditioned vocalization of the monkeys exhibited no significant change in rate at this stage, although call duration was reduced significantly. Bilateral lesions produced no further modifications in acoustic properties of spontaneous calls, while the vocal rate decreased slightly. Conditioned calls were not significantly altered in acoustic features at this stage, although the discriminative vocalization rate was significantly decreased for all monkeys. The results indicate limited control over vocal motor systems by anterior cingulate cortex, while suggesting that this region participates in initiation of voluntary phonation.     

Amino acids in the plasma of fasting Japanese monkeys (Macaca fuscata fuscata andM. f. yakui)

The plasma levels of 26 amino acids and related compounds were determined in five male and five female adult members of each of the two subspecies of Japanese monkeys,Macaca fuscata fuscata andM. f. yakui. Activities of L-asparaginase and histaminase in plasma were also measured.Numerous differences in amino acid levels between the sexes in the subspeciesfuscata were noted, with the female consistently exhibiting lower values. Few differences were observed between the sexes of the subspeciesyakui or between the two subspecies of Japanese monkeys. These monkeys were similar to other previously studied nonhuman primates in exhibiting measurable levels of 3-methylhistidine in plasma. There were numerous quantitative differences among Japanese monkeys and stump-tailed macaques, rhesus monkeys, chimpanzees, and man, with the Japanese monkeys usually exhibiting higher plasma levels.L-asparaginase activity was not detectable in these Japanese monkeys. Histaminase activity was similar to that previously measured in pig-tailed macaques and chimpanzees, lower than that in rhesus monkeys and stump-tailed macaques, and higher than that in man.