Increased cage size does not alter heart rate or behavior in female rhesus monkeys

Newly proposed federal regulations will mandate that singly caged non-human primates be kept in cages larger than the current minimum standard, or be given 4 hours in an exercise cage per week. In order to evaluate the effectiveness of increasing cage size in improving well-being, the behavioral and heart rate responses of 10 female rhesus monkeys (Macaca mulatta) to three different cage sizes were measured. With the exception of vocalizations, no significant differences in behavior were obtained. Grunts increased in the largest cage, following the birth of an infant in a cage within view of the test cages. No differences with respect to cage size were found in heart rate or activity level, although there were significant variations at different times of day. We conclude that modest increases in cage size are less likely to enrich the environment of singly caged laboratory primates than are changes in social opportunities or increases in environmental complexity.     

Effects of puzzle feeders on pathological behavior in individually housed rhesus monkeys

Self-injurious behavior (SIB) occurs in about 10% of individually housed monkeys. Monkeys with SIB bite their own bodies frequently, occasionally inflicting wounds as a result. At present, there is no standard treatment for this phenomenon. We examined the effectiveness of puzzle feeders in alleviating SIB in monkeys with a veterinary record of self-inflicted wounding. Two groups of monkeys (SIB and controls) were exposed to puzzle feeders for a 6 week period. Three levels of maze difficulty were examined. All monkeys used the feeders, but manipulation was confined to a brief period immediately after the feeders were loaded each day (1000 h) and was infrequent during the later sampling periods (1100 and 1400 h). The most difficult maze yielded a slight increase in usage at 1100 h. During the puzzle feeder phase, whole body stereotypies, including pacing and rocking, were reduced substantially in all monkeys at 1000 h when feeder manipulation was at its highest. However, self-biting in the SIB group was unchanged. Some monkeys actually bit themselves while manipulating the feeder. Long-term effects on abnormal behavior were assessed by comparing behavior during the feeder phase to baseline periods and to a phase in which the monkeys were provisioned with treats placed directly into their food box. Whole body stereotypies, including pacing, were reduced during both treatment phases; however, the reduction was associated only with the 1000 h observation. Puzzle feeders were more effective than treats alone in alleviating whole body stereotypies. Self-biting was unchanged through all phases. Puzzle feeders are beneficial from the perspective of eliciting manipulation. They also yield transient reductions in whole body stereotypy, an effect that does not extend beyond the direct manipulation of the feeder. Puzzle feeders are ineffective in alleviating self-injurious behavior. Am. J. Primatol. 46:213–227, 1998. © 1998 Wiley-Liss, Inc.     

Changes in somatodendritic but not terminal dopamineregulation in aged rhesus monkeys

For these studies, young (8-9 years), middle-aged (14-17 years) and aged (23-28 years) rhesus monkeys were used as a model of normal aging in humans to investigate changes in dopamine (DA)-containing neurons in senescence. Aged monkeys exhibited significant age-related motoric declines as compared to the young animals. In vivo microdialysis studies showed that basal levels of the DA metabolites, homovanillic acid (HVA) and 3,4-dihydroxyphenylacetic acid (DOPAC) were diminished by 44% and 79%, respectively, in the substantia nigra (SN) of aged monkeys. In addition, d-amphetamine-evoked overflow of DA in the SN was diminished by 30% in the middle-aged animals and 67% in the aged monkeys. Post-mortem measures of DA and DA metabolites showed significant decreases in DA (20%), DOPAC (47%) and HVA (22%) levels in the putamen and a 25% decline in HVA tissue levels in the SN of the aged monkeys as compared to the young animals. Unbiased stereological cell counting of tyrosine hydroxylase (TH)-immunoreactive neurons in the SN showed a small (15-20%) but significant age-related decline in TH-positive neurons. In addition, there was a small (15-20%) but significant decline in TH-positive fiber density and TH-positive cell size. In comparison to the massive loss of DA neurons responsible for the movement dysfunctions seen in Parkinson's disease, pronounced functional changes in DA release in the SN and putamen may significantly contribute to the motoric dysfunctions characterizing normal aging in rhesus monkeys.     

Effects of social and inanimate enrichment on the behavior of yearling rhesus monkeys

Certain types of inanimate environmental enrichment have been shown to positively affect the behavior of laboratory primates, as has housing them in appropriate social conditions. While social housing is generally advocated as an important environmental enhancement, few studies have attempted to measure the influence of social conditions on the effects of inanimate enrichment or to compare the relative merits of social and inanimate enhancements. In the present study, inanimate enrichment (predominately physical and feeding enhancements) resulted in increased species-typical behavior for socially restricted subjects. However, social enrichment (living in groups) appeared to be more beneficial for young rhesus monkeys, leading to increased species-typical activities and decreased abnormal activities. The behavior of one cohort of yearling rhesus monkeys (Macaca mulatta) housed in small peer groups was compared with the behavior of four yearling cohorts housed in single cages. Half the animals in each cohort received a three-phase enrichment program and the rest served as controls. Group-housed yearlings spent significantly more time feeding and exploring and significantly less time behaving abnormally, self-grooming, and drinking than did singly housed yearlings. Enriched subjects spent significantly more time playing by themselves, and significantly less time self-grooming and exploring than did controls. Among group-housed subjects only, there were no differences between enriched and control monkeys. Captive primates should be housed socially, whenever appropriate, as the first and most important step in an enrichment program, with the provision of inanimate enhancements being considerably less important. Limited resources for inanimate enrichment programs instead should be focused on those individuals who can not be housed socially. © 1996 Wiley-Liss, Inc.     

The reduction of abnormal behaviors in individually housed rhesus monkeys (Macaca mulatta) with a foraging/grooming board

A new environmental enrichment device, termed a “foraging/grooming board,” was presented to 8 individually housed rhesus monkeys for the explicit purpose of reducing the level of aberrant behaviors manifested by these animals. The device, consisting of a piece of plexiglass covered with artificial fleece, had particles of food treats rubbed into it and was attached to the outside of each animal's home cage. All animals foraged from the board to the point that a significant reduction in the level of abnormal behavior was noted. Most animals also groomed the fleece covering the board, utilizing the same motor patterns that would be directed toward grooming another monkey. These boards are inexpensive to construct and easy to sanitize, and do not require placing animal facility personnel at risk to maintain them.     

Effects of woodchips and buried food on behavior patterns and psychological well-being of captive rhesus monkeys

The effects of adding woodchip litter to bare-floored pens, burying monkey chow in the woodchips, and scattering sunflower seeds in woodchips was studied in 2 stable social groups of rhesus macaques (Macaca mulatta) to ascertain the effects of these manipulations on levels of foraging, exploration, abnormal behavior, social interactions, and urinary cortisol levels. The addition of woodchips increased exploration and feeding levels and decreased social interactions. Burial of regular monkey chow in woodchips had little effect on behavior beyond that of the woodchips alone, increasing exploration and decreasing passivity. The addition of sunflower seeds to the woodchips encouraged increased feeding and exploration and led to decreases in passivity and social interaction. There was little discernible effect of woodchip enrichment on urinary cortisol values. In contrast to some previous studies, there was no effect of wood chips or sunflower seeds on the occurrence of agonistic interactions, play, or abnormal behavior patterns.     

Assessment of motor function of the hand in aged rhesus monkeys

In the elderly, intact motor functions of the upper extremity are critical for the completion of activities of daily living. Many studies have provided insight into age-related changes in motor function. However, the precise nature and extent of motor impairments of the upper extremity remains unclear. In the current study we have modified two tasks to assess hand/digit function in both young and aged rhesus monkeys. We tested monkeys from 9 to 26 years of age on these tasks to determine the level of fine motor performance across the adult age range. Compared to young monkeys (9–12 years of age), aged monkeys (15–26 years of age) were mildly impaired on fine motor control of the digits. These findings are consistent with previous studies that have found age-related impairment in fine motor function. However, the magnitude and extent of impairment in the current study does differ from previous findings and is likely due to methodological differences in the degree of task complexity.     

Behavioral effects of enrichment on pair-housed juvenile rhesus monkeys

Among captive primates, inanimate environmental enrichment can lead to measurable changes in behavior indicative of an improvement in psychological well-being. Although this has been demonstrated repeatedly for singly caged primates, the relationship is not as well studied for pairhoused animals. Study of the pair-housed setting has become increasingly relevant because of the social housing mandate of the Animal Welfare Act regulations. We therefore observed 68 juvenile rhesus monkeys born in 1988 and 1989 and living in mixed-sex pairs from the ages of 2 to 3 years. All pairs were compatible. Half of the pairs received two types of enrichment, while the remaining pairs served as controls. Enriched and control juvenile subjects differed in the amount of time that they spent being inactive, playing, and drinking, but did not differ in the amount of time they spent interacting with their partner. Grooming and play were the two most common socially directed activities in both groups, a species-appropriate pattern. Males played more and vocalized less than did females. Overall, enriched and control subjects spent equivalent amounts of time located within a social distance of one another, but there was some difference between groups in allocation of behaviors while near the pairmate. Environmental enhancers were frequently utilized, and led to relatively small changes in behavior between control and enriched subjects, suggesting that the presence of a partner for juvenile rhesus monkeys acts as a form of enrichment that may dilute the effects of inanimate environmental enhancements. © 1994 Wiley-Liss, Inc.     

Control of postpartum mating behavior in free-ranging rhesus monkeys

This paper explores the effect that a dependent rhesus macaque infant (Macaca mulatta) has on the timing of its mother's resumption of mating. Toward this end, behavioral data from the rhesus populations at Tughlaqabad, India, and Cayo Santiago, Puerto Rico, are compared. Specifically, the intervals between parturition and subsequent resumption of mating for individual parous females are examined in order to shed light on the relative importance of environmental and internal factors (such as lactational infertility) in the control of rhesus mating behvior. At both study sites it was found that the later a given female gave birth during a birth season the shorter was her parturition-mating interval and the younger was her infant when she resumed mating activity. It is suggested that this finding is the result of an interaction of environmental and internal factors; both act in concert to determine how soon after parturition a particular rhesus female will resume mating activity.     

Molecular analyses of mtDNA deletion mutations in microdissected skeletal muscle fibers from aged rhesus monkeys

Mitochondrial DNA (mtDNA) deletion mutations co-localize with electron transport system (ETS) abnormalities in rhesus monkey skeletal muscle fibers. Using laser capture microdissection in conjunction with PCR and DNA sequence analysis, mitochondrial genomes from single sections of ETS abnormal fibers were characterized. All ETS abnormal fibers contained mtDNA deletion mutations. Deletions were large, removing 20-78% of the genome, with some to nearly all of the functional genes lost. In one-third of the deleted genomes, the light strand origin was deleted, whereas the heavy strand origin of replication was conserved in all fibers. A majority (27/39) of the deletion mutations had direct repeat sequences at their breakpoints and most (36/39) had one breakpoint within or in close proximity to the cytochrome b gene. Several pieces of evidence support the clonality of the mtDNA deletion mutation within an ETS abnormal region of a fiber: (a) only single, smaller than wild-type, PCR products were obtained from each ETS abnormal region; (b) the amplification of mtDNA from two regions of the same ETS abnormal fiber identified identical deletion mutations, and (c) a polymorphism was observed at nucleotide position 16103 (A and G) in the wild-type mtDNA of one animal (sequence analysis of an ETS abnormal region revealed that mtDNA deletion mutations contained only A or G at this position). Species-specific differences in the regions of the genomes lost as well as the presence of direct repeat sequences at the breakpoints suggest mechanistic differences in deletion mutation formation between rodents and primates.     

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.     

The effects of temporary cover on the behavior of socially housed stumptailed macaques (Macaca arctoides)

To examine the effects of the provision of temporary cover on the behavior of stumptailed macaques (Macaca arctoides), a single group of 26 animals was observed during 25 testing periods over 7.5 months. During each testing period, the group was observed under two conditions. In the Cover condition, two solid temporary walls 9.6 m in length, were erected within the animals' living compound. In the No-Cover condition, the wall materials were stacked against one solid exterior wall of the compound. The provision of cover significantly reduced the levels of contact aggression, proximity between animals, and locomotion, and reduced the ability of the dominant male to monopolize copulations. It did not effect other measures of affiliation. Inconsistencies between these results and those of other published studies suggest that, while cover can have a significant influence on some kinds of social behavior in some situations, generalizations about the benefits of providing cover to captive animals may be premature.     

The effect of feeding enrichment methods on the behavior of captive Western lowland gorillas

Three feeding enrichment treatments were tested in an outdoor yard used by six Western lowland gorillas (Gorilla gorilla gorilla). In "Yard-toss," forage was thrown by hand over one third of the yard. In "Set-up," forage and browse were hand-scattered throughout the yard. "Set-up Enriched" was similar with the addition of either a hay- and forage-filled feeder or forage-filled boomer ball(s) suspended from a climbing structure. Each treatment was presented on 5 d. Behavior was recorded for 30 min before (baseline) and 30 min after the start of each treatment. All treatments led to more foraging and less inactivity compared with baseline (P80.05), but Yard-toss was the least effective, likely because resources were clumped and monopolized by dominant animals. In Set-up Enriched, dominant animals had the greatest increase in foraging (P=0.03), partly because they generally monopolized the suspended items, but this allowed others to forage at ground level. This separation of the animals likely explains why Set-Up Enriched led to more foraging than all other treatments (P80.05). Findings show that for these hierarchical animals, enrichment resources are most effective when distributed widely, including vertically, and that enrichment strategies must take social structure into account.     

Time budget of caged rhesus monkeys exposed to a companion,a PVC perch,and a piece of wood for an extended time

The present investigation assesses the percentage of time that rhesus monkeys (Macaca mulatta) are kept occupied by a more complex cage environment. Sixty animals were continuously exposed for at least 1.5 years to a compatible companion for social interaction, a suspended plastic pipe for perching, and a branch segment for gnawing. The behavior of the partners of each pair was recorded for 60 minutes when the animals were not distracted by human activities. Individuals spent an average of 23.5% of the time interacting with the companion, but only 10.4% with the plastic pipe and 4.8% with the branch segment. Differences were statistically significant. Females were socially more active than males. Subadult animals (3.5–4 years) used both inanimate objects significantly more than did adult animals (9–30 years). It was concluded that (1) a compatible companion, a suspended plastic pipe, and a loose branch segment remain effective stimuli for caged rhesus monkeys after more than 1 year of exposure and (2) a compatible companion is of greater stimulatory value–particularly for adults–than are inanimate objects.     

Behavioral responses of unrelated rhesus monkey females paired for the purpose of environmental enrichment

An attempt was made to socialize unrelated and unfamiliar adult rhesus monkey females that had lived in single cages for more than one year. Partners first were given the opportunity for noncontact familiarization in partitioned double cages. They were then transferred into an ordinary double cage. Clear-cut rank relationships were evident within the first 90 minutes of pair formation in 94% (17/18) of dyads tested. Only 28% (5/18) of pairs resorted to fighting (in no case with infliction of serious injury), while 50% (9/18) engaged in social grooming or hugging during this initial phase of pair formation. Eighty-three percent (15/18) of pairs were compatible, with none of the partners showing signs of depression and none inflicting serious injury on the other. Seventeen percent (3/18) of pairs were incompatible (two cases of depression, one serious tail injury) and were separated. It was concluded that the barren environment of singly caged rhesus monkey females can be enriched with little risk by carefully making them compatible companions.     

A test of the generalizability of the interval scale developed for social behavior of rhesus monkeys

An interval scale of behavior would be useful in the study of social relations because it would allow the whole behavioral repertory to be used simultaneously and would allow greater flexibility in statistical manipulation. Maxim has developed such a scale using isolated dyads of unfamiliar monkeys. The typical social environment of monkeys, however, consists of familiar monkeys in mixed age and sex groups. This study replicates Maxim's procedure and tests the applicability of a scale developed with isolated dyads to groups of familiar monkeys. The scale developed here differed substantially from Maxim's. Behavior of monkeys in these groups was much more variable than behavior of monkeys in Maxim's isolated dyads. Behaviors at the extremes of the scale were similarly arranged in both scales, but behaviors in the central region were more labile and disordered. Distances between behaviors at the extreme of this scale were significantly larger than those in the central region whereas there were no differences in Maxim's scale. While some of these differences may be accounted for by group size and familiarity, several difficulties remain. Some behaviors may change meaning across different contexts and social relationships. The generalizability of these scales, therefore, may be limited to the behavior of groups of similar composition and familiarity.     

The effects of olfactory stimulation on the behavior of captive ring‐tailed lemurs (Lemur catta)

Ring‐tailed lemurs reside in many animal collections worldwide. Lemur welfare may be a cause of concern due to some captive individuals exhibiting stereotypic behavior. Despite these concerns, there has been little exploration of methods of environmental enrichment for ring‐tailed lemurs. Olfactory stimulation can enhance captive animal welfare by encouraging species‐typical behaviors, enhancing behavioral diversity, and decreasing stereotypic behaviors. We aimed to investigate the effects of olfactory stimulation via lavender, peppermint, coconut, and prey odor upon the behavior of eight captive ring‐tailed lemurs. We exposed the lemurs to six individual odor conditions (odor control, novel object control, lavender, peppermint, coconut, and Morio worms) and observed them for 4 hr a day for 3 days with an intervening period of 4 days between conditions. We recorded the lemurs’ behavior under each condition using instantaneous scan sampling. We found significant effects of olfactory stimulation on the ring‐tailed lemurs’ behavior in the initial analysis but these did not survive correction for multiple testing. Overall, while our findings are suggestive of a general effect of olfactory stimulation on the captive ring‐tailed lemurs they did not indicate a marked influence of olfactory condition. However, further investigation with a larger sample size and more biologically relevant odors may be beneficial to fully examine potential effects of olfactory stimulation in captive lemurs.     

Infant-directed behavior in young rhesus monkeys: Sex differences and effects of prenatal androgens

Young (3–4 years old) laboratory-reared rhesus monkeys were observed in five 15-minute tests with 1–15-day-old infants. Males and females were equally likely to investigate infants. Females communicated more with infants by grin-lipsmacking and gurgling–-gestures that were not shown by any males. More females presented the ventrum to infants than did males. Females contacted infants more than did males by grooming, crouching over, and having full body contact with them. To see whether prenatal androgens produced the male pattern of response, we conducted similar tests with pseudohermaphrodites (prenatally androgenized genetic females) and neonatally castrated males. On most sexually dimorphic behaviors, pseudohermaphrodites behaved more like females than like males. Castrated males, like females and pseudohermaphrodites, crouched over infants more than did intact males. Castrated males differed from females only on one infant-directed response, the grin-lipsmack. These comparisons showed that defeminization of the repertoire of infant-directed responses was measurable only in intact males. We conclude accordingly that prenatal androgens alone are not responsible for defeminization of this repertoire and that a contribution from postnatal androgens is likely to be necessary.