CSF testosterone and 5-HIAA correlate with different types of aggressive behaviors.

We studied the potential roles of testosterone and serotonin in various forms of aggressive and violent behaviors by measuring each biochemical and behaviour in free-ranging adolescent male nonhuman primates. Our results showed that (1) CSF free testosterone concentrations were positively correlated with overall aggressiveness, but not with measures of impulsivity. (2) CSF 5-HIAA concentrations were negatively correlated with impulsive behavior, and severe, unrestrained aggression, but not with overall rates of aggression. High rates of impulsive behavior were positively correlated with severe, unrestrained aggression, but not overall rates of aggression. (3) Dimensional analyses showed that while subjects with low CSF 5-HIAA exhibited high rates of aggression, high CSF testosterone further augmented rates and intensity of aggression in subjects with low CSF 5-HIAA. We conclude that high CSF free testosterone concentrations are associated with competitive aggression, while low CSF 5-HIAA concentrations are associated with severe aggression which results from impaired impulse control, and perseverance.

Excessive mortality in young free-ranging male nonhuman primates with low cerebrospinal fluid 5-hydroxyindoleacetic acid concentrations.

BACKGROUND: The purpose of this study was to assess the impact of central serotonin turnover rate on survival to adulthood among nonhuman primates living in a large, free-ranging colony. METHODS: The rate of mortality was ascertained over a 4-year period after obtaining blood and cisternal cerebrospinal fluid (CSF) samples from 49 free-ranging, 2-year-old prepubertal male rhesus monkeys. Cerebrospinal fluid was assayed for 5-hydroxyindoleacetic acid (5-HIAA), norepinephrine, 3-methoxy-4-hydroxyphenylgycol, and homovanillic acid. Blood plasma was assayed for adrenocorticotropic hormone, cortisol, and testosterone. Following the sampling of body fluids, records of scars and wounds and aggressive encounters were used to rank the subjects from low to high in aggressiveness. Direct observations of aggressive behavior were collected from 27 of the subjects over a 3-month period. RESULTS: Four years later, 6 of the 49 subjects were known to be dead and an additional 5 had been missing for more than 2 years and were presumed dead. The CSF 5-HIAA concentrations were predictive of which subjects died, with 46% of the subjects with low CSF 5-HIAA concentrations dead or presumed dead. None of the subjects from the highest CSF 5-HIAA concentration quartile were dead or missing. Indeed, 91% of the dead subjects came from the 2 lowest quartiles of CSF 5-HIAA concentrations. Direct observations of aggressive behavior showed that dead or missing subjects had initiated escalated aggression, a measure of unrestrained aggression that has a high probability of trauma or injury, at a higher rate than subjects that were known to be alive. The cause of death could be ascertained for 6 of the 11 missing subjects. The 4 subjects that were known to die as a consequence of aggressive encounters came from the lowest quartile of CSF 5-HIAA concentrations and had been rated as more aggressive during their initial capture. Subjects captured more than once possessed lower CSF 5-HIAA concentrations, were rated as more aggressive, and were more likely to suffer early death than those captured only once. CONCLUSION: These findings suggest that low CSF 5-HIAA concentrations quantified early in life is a powerful biological predictor of future excessive aggression, risk taking, and premature death among nonhuman primate males.

Correlation of CSF 5-HIAA concentration with sociality and the timing of emigration in free-ranging primates.

OBJECTIVE: The purpose of this study was to examine the relationship between behavior and serotonin in nonhuman primates. METHOD: During a routine capture and medical examination, 26 adolescent male rhesus macaques (Macaca mulatta) were selected as subjects from a free-ranging population of 4,500 rhesus monkeys inhabiting a 475-acre sea island. Blood samples (N = 23) and CSF samples (N = 22) were obtained, and each subject was fitted with a radio transmitter collar for rapid location. The subjects were released into their social groups, and quantitative behavioral observations were made over a 3-month period. RESULTS: CSF 5-hydroxyindoleacetic acid (5-HIAA) concentration was positively correlated with three measures of sociality: 1) total time spent grooming others, 2) total time spent in close proximity to other group members, and 3) mean number of neighbors within a 5-m radius. In addition, CSF 5-HIAA concentration was positively correlated with age at emigration from the natal group (in months). CONCLUSIONS: In adolescent male rhesus macaques living in naturalistic settings, CSF 5-HIAA concentration is positively correlated with affiliative sociality. Rhesus males with low CSF 5-HIAA concentrations exhibit less social competence and emigrate from their social groups at a younger age than do males with higher concentrations of CSF 5-HIAA.

Seroepizootiology of Helicobacter pylori gastric infection in nonhuman primates housed in social environments.

We determined the seroepizootiology of Helicobacter pylori infection in rhesus monkeys. Plasma was obtained from 196 animals (age range, 1 to 22 years) that were housed in social environments, either in indoor gang cages, in outdoor corrals, or in free-ranging forested conditions. Plasma immunoglobulin G levels were determined with a specific enzyme-linked immunosorbent assay, and the cutoff immunoglobulin G value for H. pylori seropositivity was determined from a study of 25 monkeys whose infection status was assessed by light microscopy and culture. One-year-old animals of both genders in all housing conditions had the lowest rate of positivity (60% in monkeys 1 year old versus 81% in monkeys 2 to 10 years old, P = 0.026). In addition, females tended to have higher rates of positivity than males. Seroconversion during a 1-year observation period occurred in 7 (28%) of 25 seronegative animals. Seroreversion occurred in 3 (4%) of the 78 positive animals; all 3 of these animals had received antimicrobial agents during the year. These observations demonstrate that the epizootiology of H. pylori infection in rhesus monkeys may serve as a model for human infection.

Low CSF 5-HIAA concentrations and severe aggression and impaired impulse control in nonhuman primates.

OBJECTIVE: The purpose of this study was to examine the relationship between behavior and serotonin by using a nonhuman primate model of aggression and impulse control. METHOD: During a routine capture and medical examination, 26 adolescent male rhesus macaques (Macaca mulatta) were selected as subjects from a free-ranging population of 4,500 rhesus monkeys inhabiting a 475-acre sea island. Physiological data were obtained from 22-23 of the subjects. Blood and CSF samples were obtained, and each subject was fitted with a radio transmitter collar for rapid location. The subjects were released into their social groups, and quantitative behavioral observations were made over a 3-month period. RESULTS: CSF 5-hydroxyindoleacetic acid (5-HIAA) concentrations were inversely correlated with "escalated" aggression, i.e., a measure of more intense or severe aggression as defined by the ratio of chases and physical assaults to all aggressive acts. CSF 5-HIAA concentrations were significantly lower in those subjects who showed evidence of physical wounding than in subjects with no wounds. Low CSF 5-HIAA concentrations were also correlated with greater risk-taking as determined by an analysis of leaping behaviors in the forest canopy. The ratio of long leaps (leaps that traversed the longest distances at dangerous heights) to all leaps was negatively correlated with CSF 5-HIAA concentrations. CONCLUSIONS: Adolescent male rhesus macaques with low CSF 5-HIAA concentrations are at risk for 1) exhibiting more violent forms of aggressive behavior and 2) loss of impulse control as evidenced by greater risk taking during movement through the forest canopy.

Cerebrospinal fluid monoamine and adrenal correlates of aggression in free-ranging rhesus monkeys.

Clinical and preclinical studies involving several different mammalian species and research paradigms suggest a negative correlation between aggression and central serotonin activity. To test the generalizability of laboratory findings in rhesus monkeys that show a negative correlation between cerebrospinal fluid 5-hydroxyindoleacetic acid concentrations and aggression, we obtained cisternal cerebrospinal fluid and blood plasma samples from monkeys living in naturalistic conditions. During a semiannual trapping, 28 juvenile and adolescent male rhesus monkeys were chosen from a population of 4200 provisioned, free-ranging rhesus monkeys living on Morgan Island, a sea island located off the coast of South Carolina. Based on direct observations of participation or avoidance of aggressive behavior and examinations of apparent fight wounds, 18 monkeys were selected for cerebrospinal fluid taps and blood samples. The remaining 10 monkeys were selected at random. Descriptions of aggressive behavior and the number of old scars and recent wounds were carefully transcribed, and a photograph showing wounds and scars was obtained for each animal. Using the transcriptions and photographs, researchers experienced in rhesus monkey behavior, but blind to the subjects' monoamine and hormone concentrations, were asked to rank the monkeys from the most to the least aggressive. The results showed a significant negative correlation between high rankings for aggression and cerebrospinal fluid 5-hydroxyindoleacetic acid concentrations. There was evidence that aggression was associated with stress, in that cerebrospinal fluid, norepinephrine, and plasma corticotropin and cortisol concentrations were positively correlated with high rankings of aggression.

Development of the Morgan Island rhesus monkey colony.

During the summer of 1979, the rhesus monkey breeding colony of the La Parguera facility of the Caribbean Primate Research Center was shipped to Morgan Island, South Carolina. During six shipments in 1979, and three more in 1980, over 1400 animals were translocated. Mortality from shipping, primarily in infants, was approximately 0.65%. Although the monkeys were not shipped in intact social groups, they restablished their groups shortly after subunits were released onto Morgan Island (MI). Since 1979 the colony has grown almost four-fold and now numbers almost 4000 animals. There has always been a strong female bias in the colony and today females comprise 75% of the total population. That portion of the colony comprising the aged animals, especially females, has grown steadily and today is 13% of the total. Except for the first year, when the colony was translocated during its mating season, reproduction at MI has been good, with a pooled average pregnancy rate of almost 80% and live birth rate of 71%. Juvenile females have also reproduced well, averaging 76% pregnancy and 70% live birth rates. This experience demonstrates that with proper planning and execution, a large, free-ranging colony can be moved long distances with minimal stress, trauma, mortality or disruption of social structure and reproduction.

Social stress and atherosclerosis in normocholesterolemic monkeys.

Socially stressed adult male cynomolgus monkeys (Macaca fascicularis) fed a low fat, low cholesterol diet developed more extensive coronary artery atherosclerosis than unstressed controls. Groups did not differ in serum lipids, blood pressure, serum glucose, or ponderosity. These results suggest that psychosocial factors may influence atherogenesis in the absence of elevated serum lipids. Psychosocial factors thus may help explain the presence of coronary artery disease (occasionally severe) in people with low or normal serum lipids and normal values for the other "traditional" risk factors.

Social status, environment, and atherosclerosis in cynomolgus monkeys.

The purpose of this experiment was to examine the effects of social environment and social status on coronary artery and aortic atherosclerosis in adult male cynomolgus monkeys (Macaca fascicularis). Thirty experimental animals were assigned to six groups of five members each, and all animals were fed a moderately atherogenic diet (43% of calories as fat, 0.34 mg cholesterol/Cal) for 22 months. Group memberships were changed periodically among 15 monkeys (unstable social condition) and remained fixed throughout the experiment in the remaining animals (stable social condition). Within each condition, individual monkeys were classified as either dominant or subordinate animals, based on dyadic patterns of aggression and submission. At necropsy, the coronary arteries were subjected to pressure fixation and five sections each were taken from the left anterior descending, left circumflex, and right coronary arteries. The mean intimal area measurement, based on all arterial sections, served as a coronary index for each animal. Results indicated that dominant animals in the unstable condition had significantly greater coronary artery atherosclerosis than dominant monkeys housed in stable social groups. Coronary artery atherosclerosis in the unstable dominants was also greater than among similarly housed (i.e., unstable) subordinates. A similar pattern was observed in the abdominal aorta, but was not statistically significant. No significant differences or similar patterns were seen in the thoracic aorta. Additional analyses revealed that the coronary artery effects were not due to concomitant differences in total serum cholesterol or high density lipoprotein cholesterol concentrations, blood pressures, ponderosity, or fasting glucose concentrations among the experimental animals. Behaviorally, manipulation of group memberships intensified agonistic encounters and disrupted patterns of affiliative interaction between dominant and subordinate monkeys. Overall, these results suggest that social dominance (an individual behavioral characteristic) is associated with increased coronary artery atherosclerosis, but only under social conditions that provide recurrent threats to the status of dominant animals (i.e., under behavioral challenge).

Age at first pregnancy and reproductive outcome among colony-born squirrel monkeys (Saimiri sciureus, Brazilian).

In a colony of squirrel monkeys (Saimiri sciureus) of Brazilian origin, 40% of all first pregnancies occurred among females aged 3.5-4 years; 57% of all first pregnancies occurred between the ages of 3.5 and 5 years while 62% occurred between the ages of 2.5 and 4 years. A total of 79% of all first pregnancies occurred among females between the ages of 2.5 and 5 years. 70% of all first pregnancies and 67% of all second pregnancies were unsuccessful. Females with unsuccessful first pregnancies were those most likely to have an unsuccessful second. pregnancy, and vice versa. The most common reproductive event in the season immediately following first pregnancy was a failure to become pregnant (33%).

Reproductive performance in a breeding colony of Brazilian squirrel monkeys (Saimiri sciureus).

In a captive colony of Brazilian squirrel monkeys (Saimiri sciureus) a discrete birth season has been retained for 5 years although its duration increased from 3 months in 1972 to 6 months in 1976. The ages of breeder females in this colony ranged from 3 to 14 years, and within this range reproductive performance was not affected by age, although it was significantly better in feral than in colony-born females. The latter had a lower pregnancy rate and a higher incidence of neonatal and fetal deaths than did the feral monkeys. It is our belief that the reproductive and maternal capabilities of the colony-born females were adversely affected by the practice of removing neonates from their mothers at weaning and raising them with age-mates.

Contrasting effects of living in heterosexual pairs and mixed groups on the structure of social attraction in squirrel monkeys (Saimiri).

The structure of social attraction was assessed in pair- and group-living squirrel monkeys (Saimiri) using paired-comparison and single-stimulus preference tests. Effects of the social environment were most prominent in females. Females housed with a single male showed sharply increased attraction to like-sex strangers and less pronounced increase in attraction to opposite-sex strangers, as compared to group-living females. Differences between pair- and group-living males were in the same direction found with females, but less extreme. Most group-living monkeys strongly preferred familiar animals to strangers regardless of sex, and like-sex to opposite-sex familiars. Change in the structure of social attractions in response to variations in the composition of the social environment appears to be an important factor in the maintenance of the species-typical grouping pattern in the squirrel monkey.

Geographic distribution and habitat diversity of the Barbary Macaque sylvanus L.

During a 15-month behavioral study in Morocco and a 3-month survey in Morocco and Algeria, the present distribution of the Barbary macaque was determined. In Algeria, monkeys are found in seven constricted and disjunct localities in the Grande and Petite Kabylie mountain ranges. These localities are severely restricted in space and are located in remote or inaccessible areas which support only small populations. Their habitats include mixed cedar and holm oak forests, humid Portuguese and cork oak mixes and gorges dominated by scrub vegetation. In only two regions (Guerrouch and Agfadou) can population of reasonable size be found; even there they do not approach the abundance found in the central Middle Atlas zone of Morocco. Distribution was more extensive earlier in this century and some areas have become unoccupied within the past 15 years. Today, their absolute numbers and population densities are low in all but two locations. Algeria contains approximately 23% (5,500 maximum) of the total number of surviving Barbary macaques in North Africa. About 77% of the total number of Barbary macaques occur in Morocco. Moroccan habitats include high cedar forests, cedar/holm-oak mixtures and pure holm oak forests. Macaque distribution in the High Atlas is restricted to the Ourika valley where only a small relict population survives. There are between five and eight small, disjunct forest pockets in the Rif which support small groups of monkeys. In the Middle Atlas, monkeys are found in high numbers and in relatively wide stretches of distribution, although there are constricted areas of low densities in this region also. 65% (14,000 maximum) of the animals and their highest densities occur in the high mixed cedar forests of the Central zone, and mixed cedar forest appears to be the preferred habitat for the species. With the exception of the Central zone, their remaining distribution is typically disjunct and constricted, and population densities aer low. As in Algeria, distribution in Morocco was wider earlier this century, and several areas have recently become unoccupied.