Use of animal-operated folding perches by rhesus macaques (Macaca mulatta).

Providing captive or laboratory animals with the best possible living conditions has led to many ideas about how caging environments can be enhanced and the animals' lives can be enriched. This study focused primarily on 2 issues: more efficient use of existing caging and providing animals with a measure of control over their environments. We designed a new springloaded folding perching apparatus that, when modified for size, could be added to almost any caging system. Experiment 1 measured usage by animals in standard laboratory caging for rhesus macaque monkeys (Macaca mulatta). Experiment 2 measured usage by this same species in social groups in a 5-acre outdoor-indoor field setting, where several other forms of enrichment were available to the animals. Results indicated that the folding perches were used in both environments. Animals quickly learned to fold down the devices to use as a place to perch, even in the presence of permanent fixed perches. The folding perches did not significantly affect existing behavioral repertoires, but they altered how the animal used the cage. Increased animal presence near folding perches during experiment 2 suggests that these devices actually were preferred. The preference results can only partially be explained by novelty. The folding perches afforded animals a measure of control over their immediate environment without interfering in research or animal care efforts. Including at least 1 folding perch per cage satisfies both the letter and the spirit of regulations on environmental enhancement for captive primates.

Growth and developmental outcomes of three high-risk infant rhesus macaques (Macaca mulatta).

Infants classified as "high risk" are born with a greater chance of developing medical complications at birth, and may have cognitive and other developmental complications later in life. Very few reports exist regarding the survival and outcome of such infants in primate colonies. Here we present early growth and developmental data on three high-risk infant rhesus macaques (one female and two males) that were born either with intrauterine growth restriction (IUGR; born below the 1st birth weight percentile for gestational age) or extremely prematurely (at gestational days 128 and 140; mean full-term gestation=164 days). We compared the outcome of these infants with that of healthy controls born at term and found no gross developmental delays in these infants with respect to growth, neonatal reflex and motor skill development, early cognitive development, or social behavior. Neurological and cognitive assessments were compared in terms of both postnatal and gestational age. The survival of these infants was dependent on a 24-hr staffed nursery and a fluid protocol that catered to each high-risk infant's individual needs. When such measures are implemented, infants such as these have a good chance of survival and can serve as excellent models for high-risk human babies and their subsequent development.

Neonatal behavior and infant cognitive development in rhesus macaques produced by assisted reproductive technologies.

Assisted reproductive technologies (ART) used in fertility clinics include in vitro fertilization (IVF) and intracytoplasmic sperm injection (ICSI), followed by embryo transfer into the biological or a surrogate mother. Over 1,000,000 liveborn offspring--an estimated 1 in 150 United States newborns--have been produced worldwide by ART since 1978. IVF appears to produce healthy children in singleton pregnancies, though concerns remain regarding preterm deliveries, multiple pregnancies, as well as the longer-term consequences of all ART procedures. Clinical studies remain difficult to interpret and subject to confounding variables, as developmental problems may be due to a parent's reproductive conditions rather than, or in addition to, an ART procedure. Also, because of expense and time commitments, the United States ART clinical population is not fully representative of society diversities. This socio-economic skewing might compensate for negative effects, masking small, or modest developmental deficits. Embryo splitting (ES), an ART procedure used only with animals, can produce genetically identical offspring. ES involves dividing four- to eight-cell embryos into separate blastomeres and implanting them into empty zona pellucida, followed by embryo transfer. Although these ART techniques have produced nonhuman primate offspring, there has been no research on behavioral safety. Here, we report the first study of behavioral development by rhesus macaques infants produced through ES, ICSI, and IVF. We assessed neonatal reflexes, self-feeding ability, recognition memory, object concept attainment, simple discrimination learning and reversal, and learning set (LS) acquisition. Although the sample sizes are small, we found no overall ART group delayed development. Surprisingly, the ES and ICSI monkeys appeared to be accelerated in attaining age milestones involving sensory-motor behaviors and a difficult Well Hiding object concept task. We conclude that macaque monkeys may provide an excellent model for the study of early human development by offspring of parents with conditions requiring ART pregnancies, as well as a model for the behavioral study of genetic-environment interactions using identical twins produced by ES.

Trisomy 16 in a pigtailed macaque (M. nemestrina) with multiple anomalies and developmental delays.

A female pigtailed macaque (Macaca nemestrina) with unusual physical characteristics, deficits in learning and cognitive tasks, abnormal social behavior, and abnormal reflexes and motor control was followed from birth until 3 years of age and found to have trisomy 16, which is homologous to trisomy 13 in humans. The animal described here showed similar features to cases of trisomy 16 and 18 (human trisomy 13 and 18, respectively) reported previously in nonhuman primates. However, both significant differences and similarities were found when compared with the homologous human trisomy. Evaluation of the genetic components of these disorders as well as systematic developmental evaluation can lead to new insights into the genetic basis of speciation, development, and the underlying differences between humans and their closest living relatives.

Survival, growth, health, and reproduction following nursery rearing compared with mother rearing in pigtailed monkeys (Macaca nemestrina).

Nursery-reared primates do not experience psychological "maternal bonding" or immunological benefits of breast milk, so they are expected to be inferior to mother-raised monkeys in growth, health, survival, reproduction, and maternal abilities. Studies of nursery-reared monkeys support aspects of this prediction for infants deprived of social contact or raised in pairs. We present colony record data on 1,187 mother and 506 nursery-raised monkeys, 2-10 yr of age, living in mixed groups. We found no group differences in survival, growth, clinical treatments for disease or bite wounds, or pregnancy outcome and neonatal deaths. Nursery males given breeding opportunities produced an average of 24 offspring. In addition to 24-hr personnel present on every day of the year, we believe that three of our procedures account for differences between our results and other reports. Our infants received 1) intensive human handling, 2) daily social interaction in a playroom, and 3) success and failure experience during learning and cognitive testing. We do not advocate rearing primates without mothers, but we conclude that these procedures are sufficient for producing physical health and adaptive juvenile and adult social skills in nursery-raised monkeys.

Growth of nursery-raised Macaca nemestrina infants: Effects of feeding schedules, sex, and birth weight.

Ponderal growth, caloric intake, growth velocity, and growth efficiency were studied from birth through 90 days in 523 nursery-raised pigtailed macaque infants. The male and female subjects ranged in birth weight from the 1st through 100th centiles of the colony distribution and were all judged to be clinically healthy. One group of infants was fed on an ad lib schedule, with formula continuously available from dispensers which were replenished every 8 h. A second group was fed on a distributed regimen, with formula available on a 4-h-on/4-h-off schedule. The latter schedule was instituted because of bacterial growth in the milk after 4 h. Infants fed the distributed diet had 20-25% lower caloric intake than those fed ad lib, but equaled or exceeded ad lib infants in body weight, growth velocity, and grams gained per 100 kilocalories (growth efficiency). The poorer utilization of calories by the ad lib group was attributed to a combination of bacteria in the milk, which caused diarrhea, and inability to metabolize the excess nutrients gained from overconsumption of fluids. The effects of the distributed diet occurred for both males and females, and across the full range of birth weights. Peak velocity and growth efficiency for both males and females occurred at 2 weeks after birth for high-birth-weight (HBW) infants and at 3 weeks for low-birth-weight (LBW) infants. However, the growth efficiency of LBW infants was equal to, or greater than, that of HBW infants after postnatal day 2. Descriptive statistics and regression equations based on this large sample are presented for quantitative comparisons of growth parameters with those of other primate species reared in laboratory or field settings. © 1992 Wiley-Liss, Inc.

Rearing infant monkeys (Macaca nemestrina) in pairs produces deficient social development compared with rearing in single cages.

Many scientists and colony managers assume that social housing is a beneficial living condition for all captive primates. Several older studies of primate development question the generality of this assumption. We recently tested this assumption by comparing the social development of pigtailed macaque infants raised in pairs and those that were raised in individual cages. All animals received 30 min of daily socialization in a playroom. Infants paired from postnatal week 3 through month 4 developed a playroom behavioral repertoire consisting largely of mutual clinging, fear, and social withdrawal. This was especially true of females. Unlike the singly caged infants, pair-reared monkeys did not successfully adapt to living in a large social group at 8-10 months of age. In this situation, pair-reared infants were subordinate and spent almost all of their time huddling on the pen floor. It was concluded that rearing macaque infants in pairs produces a behavioral repertoire that is maladaptive with respect to social development.

Perinatal hypothermia and maternal temperature declines during labor in pigtailed macaques (Macaca nemestrina).

Body temperature, respiration, and heart rate were recorded for 90 perinatal pigtailed macaques (Macaca nemestrina) within the first hour after birth. Hypothermia and corresponding depressed respiration and heart rate were evident in all animals. Regression analysis revealed that time-since-birth accounted for most of the observed variance in all measures. Temperatures of three pregnant females were monitored during labor and delivery. Declines in maternal temperature during labor suggested that depressed maternal temperature influenced the observed hypothermia in newborns. Increases in ambient (cage) temperatures during labor indicated that the females were emitting heat while declining in temperature.