Effect of stress-inducing factors on the behavior of monkeys. I. The behavior of monkeys under acute emotional stress

The behavior of Papio hamadryas pubertal males under the immobilizational stress conditions has been studied. It has been established that this very type of stress appeared to be a powerful irritant for the individuals of this species and age leading them into the depression state. The process of normalization of behavior after the 2-hour immobilization lasted for about 72 h. The main consequences of the stress were the violation of locomotion, the reception by individuals of unnatural postures, the trembling of limbs and the violation of coordination. The reaction of stress was greatly influenced by the position of individual in the hierarchic system. The dominant (alpha) and the most subdominant (z) males bore the stress easier. The intensification of food activity was marked within the male z. In certain period after the immobilization the tendency of the growth of friendly contacts between the individuals was found. The frequency of aggressive behavior after the stress lowered. The violation of manipulation activity was also marked. These regularities are of great importance for the reconstruction of group social behavior models of protohominid's societies.     

The comparative action of relanium and oxytocin on higher nervous activity in lower monkeys]

Effects of relanium and oxytocin on higher nervous activity was studied in four rhesus monkeys (Macaca mulatta) and two baboons (Papio hamadryas). During observation of the animals in enclosure tranquilizing effect was seen only after relanium administration. Under the same conditions oxytocin practically did not change the general behaviour pattern of monkeys. However, steady behavioural transformations were observed under the conditions of competitive food-procuring behaviour and during the operant goal-directed reaction. Decreasing aggressiveness of dominants oxytocin in contrast to relanium had no negative effect upon their general motor activity and sensory perception. Differences in effects of the tranquilizer and the peptide were seen also at the unit activity level of the neurons. The first drug lowered the unit activity level and the degree of the functional connections in neuronal populations in a number of cortical structures. Administration of the second one led to selective shifts of the unit activity mainly in the frontal cortex of the monkeys.     

Changes in the structure of group behavior in callosotomized rhesus monkeys

The studies were performed on 4 intact and 3 callosotomized adult male rhesus monkeys that comprised one social group. Group behaviour of all the monkeys was investigated by the frequency method of social contacts registration. Both aggressive and friendly contacts were registered. The results obtained have shown a considerable decrease in social contacts of callosotomized rhesus monkeys, as compared to normal animals. The aggressive contacts prevailed in the behaviour of the operated monkeys. The data suggest that callosotomy does not only significantly decrease the frequency, but also alters the structure of social contacts in the rhesus monkeys.     

Effect of stress-inducing factors on monkey behavior. II. Hormonal indices and their relation to behavior in the modelling of emotional stress in hamadryas baboons

The behavioural and hormonal indexes of adult males Papio hamadryas have been examined under condition of immobilized stress. The intercommunication between the hormonal status of the individual and its position in the hierarchical structure of the group is marked. The leader of the group possesses the mostly constant hormonal content during the different periods of the stress. The equal speed of reconstruction of hormonal concentration and behavioural indexes has been found. The different types of correlation between the level of adrenaline, cortisol and testosterone secretion and the frequency of aggressive behaviour have been observed.     

Psychopathological and hormonal manifestations of alcoholic intoxication and emotional stress in monkeys

Ethological approach to studying mature P. hamadryas and M. mulatta males has revealed a wide spectrum of changes in individual and zoosocial behaviour in response to the administration of different alcohol doses and stress stimuli. It has been established that neuroendocrine basis for the depression of psychic and locomotor activities developing in conditions of alcohol intoxication and emotional stress is an extremely high release of catecholamines and the increase of glucocorticoid secretion accompanied by a sharp decrease in androgen products. It should be noted that the exposure to stress stimuli during consumption of small alcohol doses intensifies depression-like stress-induced behaviour of monkeys.     

Expression of adult female patterns of sexual behavior by male, female, and pseudohermaphroditic female rhesus monkeys

Gonadally intact pseudohermaphroditic female and normal female and neonatally castrated male rhesus monkeys were given estrogen treatment as adults and evaluated for attractivity, proceptivity, and receptivity during tests with a tethered stud male. Pseudohermaphrodites were produced by injecting their mothers during pregnancy with either testosterone propionate (TP) or dihydrotestosterone propionate (DHTP). Castrated males had reliably lower attractivity than normal females on all indicator responses shown by the tethered males. Additionally, castrated males showed reliably fewer proceptive responses on 4 of 5 measures than normal females. Receptivity could not be assessed in this situation for castrated males, because tethered males never contacted them unless the castrated males were displaying presentation. No reliable differences were observed between pseudohermaphrodites produced by prenatal treatments with TP or DHTP. Pseudohermaphrodites generally showed reliably less attractivity and proceptivity than normal females and reliably more of these traits than castrated males. Attractivity scores for pseudohermaphrodites were not different from those for normal females until proximity to the tethered male was established. Receptivity was not different in pseudohermaphrodites compared with normal females. Results indicate prenatal androgenization and its developmental sequelae lead to a defeminization in adulthood which, in this testing situation, was principally manifested by a deficiency in the performance of proceptive behaviors. Additionally, defeminization in rhesus monkeys, unlike that demonstrated in rodents, does not depend upon actions of an aromatizable androgen.     

Etiological aspects of leukemias in primates including man

Attempts have been made to induce viral leukemia in monkeys (Papio hamadryas and Macaca arctoides) by inoculating them with blood from humans with different types of leukemias. In hamadryas baboons, the disease spread horizontally. By today 218 P. hamadryas and 5 M. arctoides monkeys had died of malignant lymphoma. The following viruses have been isolated from sick monkeys: lymphotropic baboon herpes virus (HVP), endogenous baboon C type viruses--xenotropic (BILN), and ecotropic (EVPG). C type oncovirus called "plasmic", which differs immunologically from the endogenous one, was also detected in the blood of sick animals. Altogether 165 sera from baboons, different species of macacas and chimpanzee were examined by the immunofluorescent technique for antibodies to HTLV virus isolated recently from sick humans with T cell leukemia/lymphoma. Antibodies to HTLV virus were detected only in monkeys (P. hamadryas and M. arctoides) with malignant lymphomas or in those which had been in close contact with them. Possible origin of simian HTLV-like virus is discussed. It originates either from leukemic patients or there is a family of primate HTLV like viruses related to the occurrence of leukemia.     

Serum dehydroepiandrosterone sulfate concentrations across the life span of laboratory-housed rhesus monkeys

Cross-sectional studies of humans have shown that dehydroepiandrosterone sulfate (DHEAS) peaks shortly after sexual maturation and declines thereafter, suggesting that the progressive reduction in DHEAS may play a role in the aging process and in the development of age-related morbidity. The present study examines changes in DHEAS concentrations across the life span of rhesus monkeys as part of the development of this primate model for studies of aging. Serum concentrations of DHEAS were measured in 792 laboratory-housed rhesus monkeys (Macaca mulatta) aged 0.5-36 years (527 females, 265 males). DHEAS concentrations in all monkeys were used to formulate an equation that describes two levels of decline of DHEAS with age. The most rapid decline occurs from infancy until approximately 5 years of age. The decline then occurs gradually with increasing age. There were no signs of an andrenarche just prior to sexual maturation, as is seen in humans or the great apes. This equation can be used to predict the expected mean serum DHEAS concentration and normal ranges of male or female rhesus monkeys at any age greater than 5 months.     

Chemical characterization of oligosaccharides in the milk of six species of New and Old world monkeys

Human and great ape milks contain a diverse array of milk oligosaccharides, but little is known about the milk oligosaccharides of other primates, and how they differ among taxa. Neutral and acidic oligosaccharides were isolated from the milk of three species of Old World or catarrhine monkeys (Cercopithecidae: rhesus macaque (Macaca mulatta), toque macaque (Macaca sinica) and Hamadryas baboon (Papio hamadryas)) and three of New World or platyrrhine monkeys (Cebidae: tufted capuchin (Cebus apella) and Bolivian squirrel monkey (Saimiri boliviensis); Atelidae: mantled howler (Alouatta palliata)). The milks of these species contained 6-8% total sugar, most of which was lactose: the estimated ratio of oligosaccharides to lactose in Old World monkeys (1:4 to 1:6) was greater than in New World monkeys (1:12 to 1:23). The chemical structures of the oligosaccharides were determined mainly by (1)H-NMR spectroscopy. Oligosaccharides containing the type II unit (Gal(β1-4)GlcNAc) were found in the milk of the rhesus macaque, toque macaque, Hamadryas baboon and tufted capuchin, but oligosaccharides containing the type I unit (Gal(β1-3)GlcNAc), which have been found in human and many great ape milks, were absent from the milk of all species studied. Oligosaccharides containing Lewis x (Gal(β1-4)[Fuc(α1-3)]GlcNAc) and 3-fucosyl lactose (3-FL, Gal(β1-4)[Fuc(α1-3)]Glc) were found in the milk of the three cercopithecid monkey species, while 2-fucosyl lactose (5'-FL, Fuc(α1-2)Gal(β1-4)Glc) was absent from all species studied. All of these milks contained acidic oligosaccharides that had N-acetylneuraminic acid as part of their structures, but did not contain oligosaccharides that had N-glycolylneuraminic acid, in contrast to the milk or colostrum of great apes which contain both types of acidic oligosaccharides. Two GalNAc-containing oligosaccharides, lactose 3'-O-sulfate and lacto-N-novopentaose I (Gal(β1-3)[Gal(β1-4)GlcNAc(β1-6)]Gal(β1-4)Glc) were found only in the milk of rhesus macaque, hamadryas baboon and tufted capuchin, respectively. Further research is needed to determine the extent to which the milk oligosaccharide patterns observed among these taxa represent wider phylogenetic trends among primates and how much variation occurs among individuals or species.     

Stereotypic and self-injurious behavior in rhesus macaques: a survey and retrospective analysis of environment and early experience

Abnormal behavior in captive rhesus monkeys can range from active whole-body and self-directed stereotypies to self-injurious behavior (SIB). Although abnormal behaviors are common in singly-housed rhesus monkeys, the type and frequency of these behaviors are highly variable across individual animals, and the factors influencing them are equally varied. The purpose of this investigation was to survey abnormal behavior in a large population of rhesus macaques, to characterize the relationship between stereotypies and self-injury, and to identify potential risk factors for these aberrant behaviors. Behavioral assessments of 362 individually housed rhesus monkeys were collected at the New England Regional Primate Research Center (NERPRC) and combined with colony records. Of the 362 animals surveyed, 321 exhibited at least one abnormal behavior (mean: 2.3, range: 1-8). The most common behavior was pacing. Sex differences were apparent, with males showing more abnormal behavior than females. SIB was also associated with stereotypies. Animals with a veterinary record of self-injury exhibited a greater number of self-directed stereotypies than those that did not self-injure. Housing and protocol conditions, such as individual housing at an early age, longer time housed individually, greater number of blood draws, and nursery rearing, were shown to be risk factors for abnormal behavior. Thus, many factors may influence the development and maintenance of abnormal behavior in captive primates. Some of these factors are intrinsic to the individual (e.g., sex effects), whereas others are related to colony management practices, rearing conditions, and research protocols.     

α-Defensins from blood leukocytes of the monkey Papio hamadryas

Three antimicrobial peptides named PHD1-3 (Papio hamadryas defensin) have been isolated from hamadryas baboon blood leukocytes using preparative electrophoresis and reverse-phase HPLC. The primary structures of these peptides have been determined by automated Edman degradation and mass-spectrometry. The results suggest that the peptides belong to the alpha-defensin family. Structural homology analysis reveals that among alpha-defensins from other animal species, PHD3 is the most closely related to RMAD5 (rhesus macaque alpha-defensin) (90% homology) from rhesus macaque leukocytes and also highly similar to human alpha-defensin HD5 (60% homology), which is produced by intestinal Paneth cells. The homology of PHD3 with human neutrophil alpha-defensin HNP1 (human natural peptide) was 30%. The primary structures of PHD1 and PHD2 are most similar to RED1 (rhesus enteral defensin), one of six enteral alpha-defensins of rhesus monkeys. PHD1-3 have been shown to be active against the Gram-positive bacteria Listeria monocytogenes and Staphylococcus aureus, the Gram-negative bacterium Escherichia coli, and the fungus Candida albicans, similarly to the human HNP1 defensin.     

Ileo-colonic lymph nodes in macaques and pavians of different ages]

Quantitative and qualitative alterations occurring in various structural components of the ileocolonic lymph nodes of Papio hamadryas at the age of 3.5 months and 5 years and Macaca rhesus at the age of 5 years were studied by means of mathematical methods. Cellular composition was counted in every histological preparation per 1,000 cells in cortical plateau, in myelin cords, in follicles with light centers and in follicles without light centers. Part (in %) of every cell variety was determined, as well as correlation of different structural components of the lymph nodes. Construcgion and cytoarchitectonics of the ileocolonic lymph nodes were stated to depend on the age of monkeys and their systematic differences.     

Cytological structure of the thymus gland in mature monkeys]

Histological sections of the thymus were studied morphometrically in 5 rhesus monkeys and 3 hamadryas baboons. The ratio of square surfaces of the cortical and cerebral substance, the percentage of Hassall's corpuscles and cellular elements (lymphocytes, stromal elements, blasts etc.) were established in the organ. Individual and species peculiarities of the structure of thymus elements were found. Less amount of parenchyma and growth of the stroma in baboons and a greater mitotic complex in rhesus monkeys show more pronounced involution processes in baboons.     

Sexual behavior of laboratory- and wild-born male Rhesus monkeys.

Rearing method has an important influence on the sexual performance of adult male rhesus monkeys. Testosterone levels and sexual behavior of laboratory-born and -reared adult males were compared with those of males born in the wild and brought to the laboratory as adults. The mean sexual performance level of colony-reared animals was significantly below that of males born in the wild but testosterone levels in the two groups did not differ significantly. Not all laboratory-reared males were sexually inadequate but less than 30% ejaculated in tests of sexual behavior. The sexual behavior and testosterone levels of adult males treated prenatally with testosterone propionate were found not to differ from those of untreated males reared in the same way. Conclusions about sexual adequacy based on 10-mm tests of sexual behavior differed very little from those based on 1-hr tests.     

Performance correlates of social behavior and organization: Effects of group formation on operant performance in rhesus monkeys (M. mulatta)

The performance of six adult rhesus monkeys on a fixed interval 1-min reinforcement schedule was examined under conditions where the reinforcement probabilities were either 1.00 or .80. The animals were tested with a reinforcement probability of 1.00 immediately after removal from their social group, tested again several months later with reinforcement probabilities of 1.00 and .80, and then retested with a reinforcement probability of .80 before, during, and after the formation of a new social group with the six monkeys. The results supported an earlier report in which it was found that high ranking animals responded at a lower rate under a reinforcement probability of 1.00 than did low ranking animals and that the former also had a higher ratio of nonreinforced to reinforced responses than the lower ranked animals. These relationships were present in five of the six animals immediately after removal of the animals from their original group and during and after formation of the new group. They did not appear on tests conducted after the animals had been out of a social group for several months. A third result was a suppression of operant performance which appeared in all animals following group formation. The magnitude and duration of this effect was inversely related to social rank and the time the animal had been a member of the group. The data are discussed in terms of a carry-over of the effects of recent social experience on two factors: a more deliberate rate of response by higher ranking animals under 100% reinforcement and an inhibition of response bursting following omission of reinforcement by the lower ranking monkeys. Supported by USAMRDC Contract No. DADA 17-73-C-3007.     

A review of sexual initiating behavior by male and female cynomolgus monkeys and some species comparisons

The sexual initiating behavior of male and female cynomolgus monkeys (Macaca fascicularis) observed during standard laboratory tests is reviewed and compared with that of rhesus monkeys (M. mulatta) observed under identical conditions. Species differences in sexual behavior are related here to differences in habitat, sexual dimorphism, and the dominance gradient between the sexes. Compared with rhesus monkeys, cynomolgus monkeys appear to be more arboreal, less sexually dimorphic, and have a smaller dominance gradient between the sexes. They exhibit a facultative single-mount copulatory pattern rather than the serial mount pattern of the rhesus monkey. Female cynomolgus monkeys are less dominated than rhesus females by their male partners. Direct aggression between mates is more frequent and redirected aggression occurs less often than in rhesus monkeys. These behavioral differences affect the interpretation of changes in initiation rates that occur (1) during the menstrual cycle, (2) when females are ovariectomized and given hormone replacement treatments, and (3) when males are castrated and treated with androgens. We conclude that estradiol in the female and testosterone in the male increase the sexual motivation of both the treated and the untreated partner. Valid interpretations of changes in initiation rates depend on accurate and exclusive definitions of behavior and on a consideration of the behavioral context in which they are made.     

Elimination of type D retrovirus infection from group-housed rhesus monkeys using serial testing and removal.

Type D retrovirus was successfully eliminated from an infected population of group-housed rhesus monkeys by serial testing of all animals for virus and antibody and subsequent removal of positives. This population of 53 rhesus had been housed together for 1 year prior to the initiation of the test and removal program, with six deaths from type D retrovirus-induced immunodeficiency disease occurring during this period. No new infections were detected after four rounds of testing. Of the 47 animals present at the start of the testing program, 17 (35%) remained after the elimination of type D virus from this group. These animals and their offspring have remained healthy and antibody negative for more than 2 years. These results demonstrate that elimination of type D retroviruses from rhesus macaque colonies is feasible, and that the objective of establishing and maintaining retrovirus-free colonies is realistic and achievable.     

Four-year study of controlled timed breeding of rhesus monkeys (Macaca mulatta)

As part of the timed breeding colony at Tulane National Primate Research Center, exogenous progesterone administration (5 mg/day for 10 days) has been used to select conception dates by inducing artificial luteal phases in female rhesus monkeys. A retrospective analysis of data obtained during four breeding seasons (1998-2001) revealed that conceptions occurred an average of 18 days after the last administration of progesterone. The age of the female to be bred, previous pregnancy history, and timing of breeding during the breeding season were determined to be critical factors in the success of the procedure. The benefit of this method of timed breeding is that it does not require tracking of menstrual cycles, which can be labor-intensive and requires that animals be monitored several months in advance of breeding to determine each female's individual cycle length. It also provided an efficient use of breeding-age males.     

Housing and care of monkeys and apes in laboratories: adaptations allowing essential species-specific behaviour

During the last two decades an increasing amount of attention has been paid to the housing and care of monkeys and apes in laboratories, as has been done with the housing and care of other categories of captive animals. The purpose of this review is to develop recommendations for adaptations of housing and care from our knowledge of the daily behavioural activity of monkeys and apes in natural conditions and in enriched laboratory conditions. This review deals mainly with adaptations of daily housing and care with respect to behaviour, and it is restricted to commonly-used species: Callitrichidae (Callitrix jacchus, Saguinus oedipus); Cebidae (Aotus trivirgatus, Saimiri sciureus, Cebus apella); Cercopithecidae (Macaca fascicularis, M. mulatta, M. nemestrina, M. arctoides, Chlorocebus aethiops, Papio hamadryas, P. cynocephalus); Pongidae (Pan troglodytes).     

Rhesus monkey (Macaca mulatta) model of Helicobacter pylori: noninvasive detection and derivation of specific-pathogen-free monkeys.

BACKGROUND AND PURPOSE: Development of the rhesus monkey model of Helicobacter pylori has been hampered by problems with serodetection and by the difficulty of identifying specific-pathogen (Helicobacter)-free animals. Our purpose was to determine whether detection could be improved and to determine if pathogen-free monkeys could be derived by nursery rearing. METHODS: An enzyme-linked immunoabsorbent assay (ELISA) and a [14C]urea breath test were compared to endoscopy to determine H. pylori infection status in rhesus macaques; 18 animals were hand raised in the nursery to determine whether pathogen-free animals could be selected. RESULTS: Helicobacter pylori infection was common in colony-raised young rhesus monkeys and was nearly universal by adulthood. Serodetection, using antigen from rhesus-derived H. pylori strains, was 95% sensitive and 94% specific. The [14C]urea breath test was 96% sensitive and 88% specific for detection of chronic Helicobacter infection in rhesus monkeys. Segregation of newborn animals within the first 24 h of life was a reliable method to obtain pathogen-free rhesus monkeys. CONCLUSION: Isolation of specific-pathogen-free animals, together with better detection methods, may improve the value of the rhesus monkey model for the study of H. pylori pathogenesis, immune response, and vaccine development.