Effect of stressor factors on the behavior of monkeys. III. The behavior of rhesus macaques during immobilization stress

The three-hour immobilizational stress in two groups of males of rhesus monkeys at the age of 7-8 and 10-12 years has been investigated. The reaction on the stress has been established to depend on the age of animals. The young males bear the stress easier, their behaviour after it is practically normal. The normal behaviour of the elder animals restores during 24 hours after immobilization. A comparative analysis of hamadryas baboons and rhesus monkeys behaviour during this type of stress has been carried out. These species differ by their reaction on stress: Papio hamadryas serve as a model of hard depressive stress, the rhesus monkeys--a model of slight-stimulative stress. The peculiarities of stress bearing depend on the selected species, age of the animal, the type of social organization and individual features of behaviour.     

Changes in masculine sexual behavior, corticosterone and testosterone in response to acute and chronic stress in male rats

Chronic exposure to stressors increases HPA axis activity and concomitantly reduces HPG axis activity. This antagonistic relationship between both these axes has been proposed to underlie the inhibition of reproductive function due to stress. Sexual behavior in males may be the most vulnerable aspect of male reproduction to acute and chronic stress and it has been suggested that alterations in sexual behavior during stress are due to the antagonistic relationship between testosterone and corticosteroids. However, only in a few studies has a correlation between the levels of testosterone and corticosterone, and sexual behavior been made. In this study, we evaluated the effects of different stressors, applied both acute and chronically, on masculine sexual behavior and whether or not these effects on sexual behavior are accompanied by changes in plasma levels of corticosterone and testosterone. Additionally, we evaluated the effect of testosterone treatment on the effects of stress on sexual behavior. Sexually experienced male rats were exposed to one of the following stressors: immobilization (IMB), electric foot shocks (EFS) or immersion in cold water (ICW). Sexual behavior and plasma levels of testosterone and corticosterone were assessed on days 1, 5, 10, 15, and 20 of stress. In a second experiment, males were castrated, treated with 3 different doses of testosterone propionate (TP) and exposed to ICW for 20 consecutive days. Sexual behavior was assessed on days 1, 5, 10, 15, and 20 and steroids were evaluated on day 20. Parameters of masculine sexual behavior were modified depending on the characteristics of each stressor. Mount, intromission and ejaculation latencies increased significantly, the number of mounts increased, and ejaculations decreased significantly in males exposed to EFS and to ICW but not in males exposed to IMB. Associated with these effects, testosterone decreased in the EFS and ICW groups on days 1, 15, and 20. However, corticosterone increased only in males exposed to ICW. In castrated males, TP treatment failed to block the effects of stress by ICW on sexual behavior and corticosterone. These results indicate that the effects of stress on sexual behavior depend on the characteristics of each stressor, and these effects, as well as the decrease in testosterone are not necessarily associated with the increase in corticosterone. The fact that testosterone treatment did not prevent the effects of stress on sexual behavior suggests that other mediators could be involved in the alterations of sexual behavior caused by stress.     

Social status modifies estradiol activation of sociosexual behavior in female rhesus monkeys

Estrogen (E2) has activational effects on sexual motivation and mitigating effects on anxiety-like behaviors that can be attenuated with chronic exposure to psychosocial stress. Some studies suggest that this attenuation can be overcome by higher doses of E2, while others show that chronic psychosocial stress may alter the mechanisms of E2 function, thus reducing any positive benefit from higher doses of E2. To determine the interaction between psychosocial stress and E2 dose on behavior, we examined the scope of attenuation across a suite of socioemotional behaviors, including reproduction, affiliation, aggression, submission, and anxiety-like behaviors on 36 ovariectomized female rhesus monkeys. Females were exposed to graded psychosocial stress, established by an intrinsic female dominance hierarchy, where subordinate animals receive high amounts of harassment. Our data show that E2 dose-dependently increased sexual motivation and male-affiliation in dominant (e.g. low-stress) females, while subordinate females showed no positive effects of E2, even at higher doses. In addition, contact aggression was attenuated in dominant females, while non-contact aggression was attenuated in both dominant and middle-ranking females. These results suggest that the stress-induced attenuation of E2's activational effects on sexual behavior and affiliation with males may not be overcome with higher doses of E2. Furthermore, the observed behavioral consequences of psychosocial stress and E2 dose may be dependent on the behaviors of all the females in the social-group, and better resolution on these effects depends on isolating treatment to individuals within the group to minimize alterations in social-group interactions.     

Social status modifies estradiol activation of sociosexual behavior in female rhesus monkeys

Estrogen (E2) has activational effects on sexual motivation and mitigating effects on anxiety-like behaviors that can be attenuated with chronic exposure to psychosocial stress. Some studies suggest that this attenuation can be overcome by higher doses of E2, while others show that chronic psychosocial stress may alter the mechanisms of E2 function, thus reducing any positive benefit from higher doses of E2. To determine the interaction between psychosocial stress and E2 dose on behavior, we examined the scope of attenuation across a suite of socioemotional behaviors, including reproduction, affiliation, aggression, submission, and anxiety-like behaviors on 36 ovariectomized female rhesus monkeys. Females were exposed to graded psychosocial stress, established by an intrinsic female dominance hierarchy, where subordinate animals receive high amounts of harassment. Our data show that E2 dose-dependently increased sexual motivation and male-affiliation in dominant (e.g. low-stress) females, while subordinate females showed no positive effects of E2, even at higher doses. In addition, contact aggression was attenuated in dominant females, while non-contact aggression was attenuated in both dominant and middle-ranking females. These results suggest that the stress-induced attenuation of E2's activational effects on sexual behavior and affiliation with males may not be overcome with higher doses of E2. Furthermore, the observed behavioral consequences of psychosocial stress and E2 dose may be dependent on the behaviors of all the females in the social-group, and better resolution on these effects depends on isolating treatment to individuals within the group to minimize alterations in social-group interactions.     

Styles of male social behavior and their endocrine correlates among low-ranking baboons

We have previously studied the relationship between social subordinance (by approach-avoidance criteria) and physiology among male olive baboons (Papio anubis) living freely in a national park in Africa. In stable hierarchies, subordinate individuals have elevated basal glucocorticoid concentrations and a blunted glucocorticoid response to stress, as well as a prompt suppression of testosterone concentrations during stress. These facets have been interpreted as reflecting the chronic stress of social subordinance. In the present report, we find that these endocrine features do not mark all subordinate individuals. Instead, endocrine profiles differed among subordinate males as a function of particular stylistic traits of social behavior. A subset of subordinate males was identified who had significantly high rates of consortships, a behavior usually shown only by high-ranking males. Such behavior predicted the beginning transition to dominance, as these males were significantly more likely than other subordinates to have moved to the dominant half of the hierarchy over the subsequent 3 years. In keeping with this theme of emerging from subordinance, these individuals also had significantly larger glucocorticoid stress-responses, another feature typical of dominant males. However, these subordinate males also had significantly elevated basal glucocorticoid concentrations; it is suggested that this reflects that stressfulness of their overt and precocious strategy of reproductive competition. In support of this, subordinate males with high rates of covert “stolen copulations” did not show elevated basal glucocorticoid concentrations. A second subset of subordinate males were the most likely to initiate fights or to displace aggression onto a third party after losing a fight. These males had significantly or near-significantly elevated testosterone concentrations, compared to the remaining subordinate cohort. Moreover, these males had significantly lower basal glucocorticoid concentrations; this echoes an extensive literature showing that the availability of a displacement behavior (whether aggressive or otherwise) after a stressor decreases glucocorticoid secretion. In support of this interpretation suggesting that it was the initiation of these aggressive acts which attenuated glucocorticoid secretion, there was no association between glucocorticoid concentrations and participation (independent of initiation) in aggressive interactions. Thus, these findings suggest that variables other than rank alone may be associated with distinctive endocrine profiles, and that even in the face of a social stressor (such as subordinance), particular behavioral styles may attenuate the endocrine indices of stress. Am. J. Primatol. 42:25–39, 1997. © 1997 Wiley-Liss, Inc.     

Grooming behavior of spider monkeys (Ateles geoffroyi) on barro colorado Island,Panama

Quantitative grooming data are presented for free-ranging black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Republic of Panama. A total of 126 grooming sessions was recorded, with an average session length of 2.0 min (range, 0.1 to 10.0 min). Grooming was an infrequent behavior; on average, individuals allocated only 2.5% of their daily activity to grooming. Two daily peaks of grooming activity were observed, one near midday and another in the late aftermoon between 1600 and 1700. Adult females groomed most frequently, followed by males and then juveniles. Juveniles were the most frequent recipients of grooming, followed by females and then males. Individual preferences were observed primarily between mother-offspring, male-male, and juvenile-male grooming partners in this male-bonded fission-fusion, species. Grooming interactions reflect many of the social characteristics of spider monkey societies: intraclass grouping preferences, long period of juvenile dependence, male philopatry, and female dispersal.     

The influence of social experience on the behavior of male cockroaches,Nauphoeta cinerea

The influence of social experience on rates of agonistic behavior was investigated in a cockroach, Nauphoeta cinerea. Social experience was manipulated by establishing three types of groups of four identically aged males: (1) ran-domly chosen, socially naive males (control); (2) males of similar status and activity level (from treatment 1); and (3) males returned to their original hierarchy after experiencing treatment 2. In the control groups, we found stable hierarchies, significant differences in the rate of agonistic behaviors exhibited among different status males, and a significant relationship between social status and level of agonism. We also compare activity levels within and among groups after males had novel social experiences. Among similar status individuals, we found less activity than when they wereintheir original groups. When males were returned to their original groups, the level of activity increased compared to the level of activity before treatment. The social status of males was unstable after these treatments. Losing tended to result in relatively more subordinate behavior, and winning in relatively more dominant behavior by a male. Within groups, the rate of agonism also increased over 5 days in groups of males that had no previous interactions with each other, while the rate of agonism remained the same in groups of familiar males. We interpret these results in light of male-male assessment and the maintenance of social status in this species.     

The acute physiological response of polar bears to helicopter capture

Many wildlife species are live captured, sampled, and released; for polar bears (Ursus maritimus) capture often requires chemical immobilization via helicopter darting. Polar bears reduce their activity for approximately 4 days after capture, likely reflecting stress recovery. To better understand this stress, we quantified polar bear activity (via collar-mounted accelerometers) and body temperature (via loggers in the body core [T_abd] and periphery [T_per]) during 2–6 months of natural behavior, and during helicopter recapture and immobilization. Recapture induced bouts of peak activity higher than those that occurred during natural behavior for 2 of 5 bears, greater peak T_per for 3 of 6 bears, and greater peak T_abd for 1 of 6 bears. High body temperature (>39.0°C) occurred in T_per for 3 of 6 individuals during recapture and 6 of 6 individuals during natural behavior, and in T_abd for 2 of 6 individuals during recapture and 3 of 6 individuals during natural behavior. Measurements of T_abd and T_per correlated with rectal temperatures measured after immobilization, supporting the use of rectal temperatures for monitoring bear response to capture. Using a larger dataset (n = 66 captures), modeling of blood biochemistry revealed that maximum ambient temperature during recapture was associated with a stress leukogram (7–26% decline in percent lymphocytes, 12–21% increase in percent neutrophils) and maximum duration of helicopter operations had a similar but smaller effect. We conclude that polar bear activity and body temperature during helicopter capture are similar to that which occurs during the most intense events of natural behavior; high body temperature, especially in warm capture conditions, is a key concern; additional study of stress leukograms in polar bears is needed; and additional data collection regarding capture operations would be useful.     

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.     

外源性皮质酮对雄性根田鼠交配行为的作用

本文研究了皮质酮对雄性根田鼠交配行为的作用。实验个体分别注射0.10 ug/ g体重、0. 60 ug / g体重和1.00 ug/ g体重剂量的皮质酮,1 h后测定每只雄性根田鼠的交配行为。结果显示,3 个处理组动物具有射精能力的个体比率及其爬跨、抽动和射精潜伏期与对照组动物相比均无显著差异,爬跨和抽动频次也无显著变化。不同处理组个体的血浆睾酮含量无显著差异。因此,皮质酮没有影响雄性根田鼠的交配行为和性激素的分泌。该结果提示,哺乳动物在急性应激条件下所分泌的皮质酮可能不参与对性行为的调控。     

Effect of neurotensin on the behavior of rats with damaged serotoninergic neurons under immobilization stress

It was shown that the immobilization of animals has led to reducing of vertical and horizontal locomotor activity in the "open field" and decreasing of number of conditioned food-procuring reactions into T-maze. The damages of serotoninergic neurons produced via local injections of selective neurotoxin 5, 7-dihydroxytriptamine into dorsal raphe nucleus intensified behavior alterations. Neurotensin administrations reduced effects of neurotoxin: the rats locomotor activity and quantity of conditioned reactions into T-maze were kept at the phone level just after immobilization as well as next two days. The results indicate the important protective significance of neurotensinergic brain structures for ensuring of adaptive behavior of animals with damaged serotoninergic neurons under emotional stress conditions. It is supposed that neurotensin normalizing influences on behavior is connected to a restoration of balance of dopamine-and serotoninergic brain structures interaction.     

Gonadal hormones and sexual behavior in groups of adult talapoin monkeys (Miopithecus talapoin).

Three heterosexual groups of six to eight monkeys were studied; all females were ovariectomized, whereas males were either intact or castrated. Aggressive hierarchies were evident in all groups, with females generally outranking males. When females were treated with estradiol, all males looked more frequently at the latters' sexual skin swellings, but only one male who was both dominant and intact copulated with them. Thus, either castration or low rank resulted in decreased levels of sexual behavior in male talapoins. The sexual behavior of dominant castrated males was restored by testosterone therapy, whereas subordinate castrates never copulated, even after large doses of testosterone, though penile erections and ejaculatory reflex (during masturbation) were restored. Following removal of a dominant male, the sexual behavior of the next male in rank was restored, provided he was not castrated and untreated. In contrast to males, female talapoins showed no consistent correlation between their rank and sexual activity. Estradiol therapy was without overall effect upon the frequency of female mounting behavior, though some females mounted and presented to one another more often. Estradiol treatment also caused females to present to males more frequently, but only to those that were sexually active (i.e., who mounted females).     

Effects of two types of restraint stress on spontaneous behavior of Sprague-Dawley and Lewis rats.

The purpose of this study was to evaluate the action of two types of stressors in Sprague-Dawley (S-D) and Lewis (LEW) rats differing in their hypothalamic-pituitary-adrenal axis activity on locomotion and rearing in an open space. Exposure to restraint immobilization alone (IMO) or this immobilization combined with cold water (22 degrees C) immersion (IMO+C) lasted for 1 h and started 2 or 5 h before the test. To evaluate the acute and persisting effects of both stressors, four trials were performed in one-week intervals; rats were exposed to the stressors in trial 1 and 3. While in LEW rats both acute stressors produced reduction of locomotion and rearing in all stressed groups, S-D rats responded with a decrease of both parameters only after IMO+C presented 2 h before testing. Neither strain displayed a changed performance one week after the first stress exposure. One week after the second stress exposure rats of both strains exhibited a tendency to an increase of both parameters reaching the significance in several experimental groups. The findings indicate: a) the IMO+C produced stronger behavioral alteration than IMO alone; b) the behavioral responses to stressors were more pronounced in LEW compared to S-D strain; c) change from the reduction of activity to its increase may be interpreted as bi-directional manifestation of long-term effects of immobilization stress.     

The effect of substance P on the individual and group behaviors of rhesus monkeys]

The tendencies in the substance P influence on the expression of individual and group behaviour of adult males of rhesus macaques have been studied on the background of cardiopathogenic emotional stress (CES) and without it. CES stimulated the general activity of rhesus macaques in the individual cages, while the substance P injection without CES increased the frequency and duration of pathologic behavioral patterns. The maximal influence of substance P was expressed on the 3-4 day of experiments. On the 5th day the intensification of locomotion and social activity was found during the settling of all individuals in the large cage. The definite regularity of connection between the value of arterial pressure before and after experiments and the individual's social ranks is found. The injection of substance P on the CES background and without it the second-ranking individuals stood more hard, the leader and the most subordinated individuals stood easier.     

Participation of ATP-sensitive potassium channel in autoregulation of coronary blood flow under the condition of limited motor activity

The aim of study involved detection of the effect of the K(ATP)-channel blocker glibenclamide on autoregulation of coronary flow, the expression of reactive hyperemia, the value of coronary dilatation reserve, and the myocardial contractile function in isolated rat hearts after a 6-hour immobilization stress. The experiments have been performed on 64 isolated rat hearts (female): into the cavity of left ventricle, a latex balloon connected with electromanometer has been introduced. Every experiment consisted of 2 stages. The heart has been perfused by Krebs-Henseleite solution in the first stage, and in the second stage--by the same solution with glibenclamide (1 mkM) or its combination with verapamile (10(-)6 M) or saponin (44 mcg/ml of coronary flow within 2 minutes) added to it. During the experiment, the perfusion pressure has been elevated step by step from 40 to 120 mm Hg with 20 mm Hg steps (coronary autoregulation). In rats after immobilization, the glibenclamide effect on cardiac vessel tone and expression of maximal hyperemic coronary flow (in contrast to its influence on myocardial contractile function) is lower than in control and depends on endotheliocyte presence which suggests an important role of endothelium in maintaining cardiac vessel smooth cell activity of K(ATP)-channels inhibited under the stress condition. After immobilization stress, the role of endothelium in the reactive hyperemia origin was enhanced, that of the K(ATP)-channels was reduced. The general activity of both mechanisms of tone regulation of cardiac vessels remains the same as in control. This suggests that the K(ATP)-channels as nitric monoxide and eicozanoids are the local system of myogenic tone regulation of the rat cardiac vessels; that the rat immobilization inhibits the activity KATp-channel's smooth cells of coronary vessels and creates a marked dependence of their activity on endothelium presence.     

Time course of hypothalamic CRF activity after the administration of two different stresses.

The time course of hypothalamic corticotropin-releasing factor (CRF) activity after the administration of ether stress was different from that after immobilization stress. The maximal response CRF activity was observed 2 min after ether stress, followed by a precipitous decrease 5 min after the stress. A gradual increase of CRF activity was subsequently observed for several minutes with fluctuated changes. Thus, response pattern was vibratory. But under immobilization stress, markedly fluctuant changes of CRF activity seen in the case of ether stress did not appear after the maximal response observed at 2 min, indicating that the response pattern was not vibratory. On the other hand, the concentration of plasma corticosterone increased significantly 5 min after the ether or immobilization stress with the peak value around 17 min.     

Effects of aversive experience on the behavior within a custom-made plus maze in the short-tailed fruit bat, Carollia perspicillata

Stress exposure evokes a variety of physiological and behavioral responses in an organism, enabling it to cope with stressful situations and changes in the environment. In a previous study, we found that subjecting individuals of Carollia perspicillata to a chronic immobilization stress paradigm resulted in a significant increase of fecal cortisol concentrations. In the present study, we investigated the influence of stress on the behavior of C. perspicillata, by adapting a commonly used behavioral paradigm for characterizing coping styles of animals (i.e., the elevated-plus maze) to bats. Adult bats were subjected 1?h/day to immobilization over a period of 10?days. On the subsequent day, the behavior of each animal was analyzed in a custom-made plus maze, consisting of four arms (two open and two enclosed ones) and designed 3D because of the bats' ability to fly. In this newly invented design, we compared the behaviors of stressed animals and controls. Changes in locomotor and exploratory behavior suggest two divergent adaptive behaviors in C. perspicillata following the chronic stress paradigm, possibly indicating different stress coping styles.     

Sex Differences in Reactivity of the Sympathoadrenal System in Rat Ontogenesis

Sex differences in reactivity of the sympathoadrenal system were studied in male and female Wistar rats of three age groups (22-day-old, 31-day-old, and adult). An essential increase of catecholamine excretion level in males between the 22nd and 31st day after the birth has been noted both after stress (immobilization water-immersion action) and after injection of ₂-adrenoblockator yohimbine. In females the response to stress and injection of yohimbine practically did not change at this age stage. The sex dimorphism revealed as a higher level of adrenaline excretion in the 22-day-old females, as compared with males, was characterized in older groups by a higher level of its excretion in males. It might be suggested that sex dimorphism in non-reproductive types of behavior can depend on two factors: on differences in the maturity rate between females and males and on direct or mediated effects of sex hormones on physiological processes and related behavioral reactions.     

Fur rubbing behavior in free-ranging black-handed spider monkeys (Ateles geoffroyi) in Panama

Members of the population of black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Panama, use the leaves of three Rutaceae species in a behavior that resembles fur rubbing in the white faced capuchin (Cebus capucinus). This behavior has not been reported from other sites where Ateles has been studied. During more than 1,200 hours of observation, 30 episodes of this behavior were recorded ad libitum. Adult males engage in this behavior more than adult females. Season did not impact the frequency of the behavior. The behavior described here differs in many respects from that reported for Cebus capucinus, and does not fit the hypotheses that the behavior functions in repelling insects or other antiseptic purposes. It is proposed that fur rubbing in this group of spider monkeys is a modification of a behavior previously recorded in Ateles and may function in scent marking.     

Modification of expression of neurohormones in hypothalamus of prenatally stressed male rats in model of posttraumatic stress disorder

By the method of quantitative immunohistochemistry there has been studied expression of corticotrophin-releasing hormone (CRH) and vasopressin in hypothalamic paraventricular nucleus (PVN) of prenatally stressed rats in the experimental model of the posttraumatic stress disorder-the paradigm “stress-restress”. The prenatal stress was modeled by immobilization of pregnant female rats for 1 h from the 15th to the 19th day of pregnancy. It has been shown that in sexually mature males-descendants of stressed mothers-a decrease in immunoreactivity to CRH and vasopressin is observed in the parvocellular and magnocellular PVN areas 10 days after the restress. In the control group males born by intact mothers the level of immunoreactivity to CRH was increased in both PVN areas, whereas with respect to vasopressin-in the magnocellular area. Only in the prenatally stressed males there is detected a decrease in the corticosterone level in the blood plasma 10 days after the restress. It is concluded that in the control group males the manifestation of the pathological state in the paradigm “stress-restress” consists in hyperactivation of the hypothalamic chain of regulation of the hypothalamus-pituitary-adrenocortical system, whereas in the prenatally stressed animals, on the contrary, there is observed a decrease in activity both of the central (PVN) and of the peripheral (adrenal cortex) chain of this hormonal axis.