Reproduction of the owl monkey (Aotus spp.) in captivity

Abstract: The reproduction performance of captive owl monkeys, a breed used extensively in biomedical research, was observed at the Battelle Primate Facility (BPF). The colony grew through captive breeding, imports from the Peruvian Primatological Project, and others to a peak size of 730. It included seven karyotypes of Aotus sp. Results showed that owl monkeys can breed successfully in a laboratory in numbers sufficient to sustain modest research programs. Reproductive success increases when pairs are compatible, of the same karyotype, and stabilized; however, mated pairs of different karyotype are also productive. Under conditions of controlled lighting and heating, owl monkeys at BPF showed no birth peak nor birth season.     

Effects of management practices on the timing of captive chimpanzee births

Most wild and captive nonhuman primates give birth nocturnally. Circadian rhythm mechanisms are a principal determinant of the nonrandom initiation of labor, but it has been suggested that the decreased human activity and increased seclusion over the weekend in laboratory primate colonies may result in an effect whereby births are confined mainly to the quiet periods. This study tests for such an effect in the timing of 153 live, term births in chimpanzees (Pan troglodytes) housed in three institutions with various management practices. Eighty-four percent of births occurred nocturnally, and peak delivery time was between 2400 and 0700 hours. When the total number of births was examined, significantly fewer births occurred on Wednesdays and Thursdays, during the mid-week peak in colony activity, and significantly more births occurred on Sundays and Mondays. In facilities having marked alterations between weekday and weekend activity, significantly more births occurred Sunday and Monday. In the colonies where weekend and weekday surveillance and activity were similar, births were more evenly distributed throughout the week. These data suggest that parturition may be inhibited by routine colony activities that are perceived as stressful by some animals, and that the decreased activity and increased privacy on weekends may allow relaxation of parturient females, resulting in delivery during or immediately following the weekend. Colony managers should minimize colony activities that are potentially stressful to prepartal females in order to reduce risks to the fetus that may occur with delay or disruption of normal parturition. © 1992 Wiley-Liss Inc.     

Two new karyotypes in the Peruvian owl monkey (Aotus trivirgatus)

The observation of remarkable karyotypic variation in owl monkeys (Aotus trivirgatus) stimulated us to study the chromosomal evolution of this New World genus. As an extension of this project, we examined the chromosome complement of a “phenotype-B” Aotus population from Peru. In addition to karyotype V(2n = 46), two new karyotypes with diploid numbers of 47 and 48 were identified. A G-band comparison of these karyotypes indicated that the chromosome number polymorphism in these Peruvian owl monkeys resulted from a single fusion or fission event involving a single metacentric and two acrocentric chromosome pairs. This mechanism is also known to be responsible for the chromosome number polymorphism in at least two other populations of phenotype B Aotus, one from Colombia and the other from Panama.     

Erythrocyte glyoxalase I polymorphism in the owl monkey,Aotus

Three erythrocyte glyoxalase I phenotypes were observed in a sample of 235 karyotypically defined New World owl monkeys, Aotus. The selective distribution of glyoxalase I allele (GLO¹, GLO²) is related to the karyotype of each animal. Owl monkeys with a karyotype VI had an equal distribution of GLO¹ and GLO² genes in the population. Aotus with karyotype II, III, IV, or V had, exclusively, the GLO² allele (expressed as the fast electrophoretic phenotype), in contrast with monkeys with karyotype I or VII, which had only the GLO¹ allele (expressed as the slow electrophoretic phenotype).     

Diurnal births and perinatal behavior among wild patas monkeys: Evidence of an adaptive pattern

Data from a 2-year field study of patas monkeys (Erythrocebus patas) in Kenya support our earlier suggestion that diurnal births are a species-typical pattern of patas. In this respect patas are very unusual, as all existing information shows that nocturnal births are typical of both captive and freeranging monkeys. Patas do not give birth at night because to do so would render ineffective their night-resting strategy which reduces vulnerability to predation at night. Giving birth during the day, however, does not eliminate the risk of being preyed on; nor are all times of day equally favorable for giving birth. Our field data suggest that a patas female gives birth at those times of day when she is least likely to lose contact with her group or to encounter predators.     

TheAotus from northern Argentina

Eight specimens ofAotus from Argentina were studied. Their geographic distribution, pelage phenotype, diploid number, chromosome measurements and morphology and C- and G-banding patterns have been reported in the present work. Cytogenetic analysis with Giemsa showed 2N=50 in the females and 2N=49 in a male. C- and G-banding patterns differed from those published for owl monkeys from other geographic regions.     

Behavior,Ecology, and Demography of <Emphasis Type="Italic">Aotus vociferans</Emphasis> in Yasuní National Park,Ecuador

Given its broad geographical distribution, Aotus is a productive genus for comparative studies that evaluate how different ecological factors influence the morphology, behavior, ecology, and demography of closely related species. During 18 mo we collected demographic, ranging, and activity data from owl monkeys (Aotus vociferans) in Yasuní National Park in eastern Ecuador. To collect demographic data, we monitored the trail system several times per week searching for groups. To characterize patterns of activity, we recorded the time when the subjects began and ended their nocturnal activity, and we collected data on range use and daily path length during 12 full-moon and 12 new-moon night follows of 1 radiocollared group. They ranged in size between 3 and 5 individuals (n = 4 groups). All groups were strictly nocturnal, beginning their activity between 1800 and 1900 h and finishing it between 0500 and 0600 h. The territory size of the radiocollared group was 6.3 ha. On average, the subjects traveled 645 m per night (±286 m) and ranged farther during full-moon than new-moon nights. The owl monkeys used a small number of preferred daytime sleeping trees. Our data conform well with previous studies of other tropical owl monkeys from Colombia and Perú. A comparison of tropical owl monkeys with more temperate Aotus azarai from the Argentinean Gran Chaco reveals that grouping patterns, day range length, and territory size are relatively conserved across the genus despite dramatic differences in body size and activity pattern.     

Living together: behavior and welfare in single and mixed species groups of capuchin (Cebus apella) and squirrel monkeys (Saimiri sciureus)

There are potential advantages of housing primates in mixed species exhibits for both the visiting public and the primates themselves. If the primates naturally associate in the wild, it may be more educational and enjoyable for the public to view. Increases in social complexity and stimulation may be enriching for the primates. However, mixed species exhibits might also create welfare problems such as stress from interspecific aggression. We present data on the behavior of single and mixed species groups of capuchin monkeys (Cebus apella) and squirrel monkeys (Saimiri sciureus) housed at the Living Links to Human Evolution Research Centre in the Royal Zoological Society of Scotland's Edinburgh Zoo. These species associate in the wild, gaining foraging benefits and decreased predation. But Cebus are also predators themselves with potential risks for the smaller Saimiri. To study their living together we took scan samples at ≥15 min intervals on single (n=109) and mixed species groups (n=152), and all occurrences of intraspecific aggression and interspecific interactions were recorded. We found no evidence of chronic stress and Saimiri actively chose to associate with Cebus. On 79% of scans, the two species simultaneously occupied the same part of their enclosure. No vertical displacement was observed. Interspecific interactions were common (>2.5/hr), and equally divided among mildly aggressive, neutral, and affiliative interactions such as play. Only one aggressive interaction involved physical contact and was non‐injurious. Aggressive interactions were mostly (65%) displacements and vocal exchanges, initiated almost equally by Cebus and Saimiri. Modifications to the enclosure were successful in reducing these mildly aggressive interactions with affiliative interactions increasing in frequency and diversity. Our data suggest that in carefully designed, large enclosures, naturally associating monkeys are able to live harmoniously and are enriched by each other. Am. J. Primatol. 72:33–47, 2010. © 2009 Wiley‐Liss, Inc.     

Infant Development and Parental Care in Free-Ranging <Emphasis Type="Italic">Aotus azarai azarai</Emphasis> in Argentina

Studies of infant development and parental behavior in free-ranging owl monkeys have been constrained by their nocturnal habits. Taking advantage of the cathemeral activity pattern of Aotus azarai azarai in the Argentinean Chaco, we describe the development of a cohort of free-ranging infants born in an owl monkey population in Formosa Province. We observed 7 infants, whose birth dates are known to the nearest week, to record details of their development and care between October 1999 and March 2000. We collected 92 h of behavioral data in 76 sessions. The infants were almost never off the parents during the first 4 wk of life, and we observed no infant being transported by a nonadult. The parent carrying the infant traveled most frequently in the middle of the group, sometimes first, but rarely last. The mean duration of 33 nursing episodes is 69 sec. After nursing, the infant was more likely to return to the nonnursing adult than to remain with the mother suggesting that in owl monkeys the infant may be primarily attached to the adult male in the group. Infants began to explore, to manipulate and to consume solid foods during the second month. Our observations are comparable to ones on captive breeding groups of Colombian owl monkeys (Aotus lemurinus) and Bolivian owl monkeys (A. azarai boliviensis) under controlled conditions of temperature, illumination and food availability.     

Field Methods for Capturing and Marking Azarai Night Monkeys

Long-term behavioral studies require the permanent identification of individuals. The need for individual identification is even more crucial for sexually monomorphic species since not even the sexes can be differentiated by the field observer. Owl monkeys (Aotus spp.) are sexually monomorphic primates inhabiting the forests of Central and South America. We report here on the methods and drug dosages used to capture, mark, and identify individual owl monkeys (Aotus azarai azarai) in Eastern Formosa, Argentina. We successfully captured 70 owl monkeys using blowpipes or a CO₂ rifle, but attempts to capture them with baited traps proved unsuccessful. During the marking and collaring procedures, we gave individuals on average a total of 50 mg of ketamine hydrochloride, including the dose in the dart. To mark them, we freeze-branded portions of their tails and fitted them with radio or bead collars. There was no death or physical life-threatening injury while capturing or marking individuals. The procedures we describe should allow one to safely capture and to mark small arboreal primates when trapping is not possible.     

Mated pairs of owl monkeys (Aotus nancymaae) exhibit sex differences in response to unfamiliar male and female conspecifics

In socially monogamous species, mate‐guarding could be a reproductive strategy that benefits both males and females, especially when males contribute to parental care. By actively guarding mates, males may reduce their chances of being cuckolded, whereas females that mate‐guard may reduce the likelihood that their mates will desert them or acquire additional mates, and hence limit or reduce paternal care of offspring. Owl monkeys (Aotus spp.) are socially monogamous with biparental care of young and, hence, potential beneficiaries of mate‐guarding. We presented mated pairs of captive owl monkeys (A. nancymaae) with unfamiliar male and female conspecifics, to determine if either member of the pair exhibits intraspecific aggression toward an intruder or stays close to its mate, behaviors indicative of mate‐guarding. Male mates were more responsible for the maintenance of close proximity between mates than females. Male mates also exhibited elevated levels of behavior that signify arousal when presented with a male conspecific. These responses by mated male owl monkeys are consistent with patterns that may help prevent cuckoldry. Am. J. Primatol. 72:942–950, 2010. © 2010 Wiley‐Liss, Inc.     

The normal and abnormal owl monkey (Aotus sp.) heart: looking at cardiomyopathy changes with echocardiography and electrocardiography

Background Cardiovascular disease, especially cardiomyopathy, was the major cause of death among owl monkeys (Aotus sp.) at a major colony and threatened colony sustainability. For this study, echocardiography (echo) and electrocardiography (ECG) normal values were established, and cardiomyopathy animals identified. Methods Forty‐eight owl monkeys were studied, 30 older than 10 years of age (‘aged’) and 8 of age 5 years (‘young’). Eight aged owl monkeys had cardiomyopathy. Results and Conclusions Aged Aotus had increased left ventricular posterior wall thickness over young animals. Left ventricular diameter and ejection fraction appeared to be the best identifying measurements for cardiomyopathy. There were no differences in the ECG.     

MHC class I genes in the owl monkey: mosaic organisation, convergence and loci diversity

The MHC class I molecule plays an important role in immune response, pathogen recognition and response against vaccines and self- versus non-self-recognition. Studying MHC class I characteristics thus became a priority when dealing with Aotus to ensure its use as an animal model for biomedical research. Isolation, cloning and sequencing of exons 1–8 from 27 MHC class I alleles obtained from 13 individuals classified as belonging to three owl monkey species (A. nancymaae, A. nigriceps and A. vociferans) were carried out to establish similarities between Aotus MHC class I genes and those expressed by other New and Old World primates. Six Aotus MHC class I sequence groups (Ao-g1, Ao-g2, Ao-g3, Ao-g4, Ao-g5 and Ao-g6) weakly related to non-classical Catarrhini MHC were identified. An allelic lineage was also identified in one A. nancymaae and two A. vociferans monkeys, exhibiting a high degree of conservation, negative selection along the molecule and premature termination of the open reading frame at exon 5 (Ao-g5). These sequences high conservation suggests that they more likely correspond to a soluble form of Aotus MHC class I molecules than to a new group of processed pseudogenes. Another group, named Ao-g6, exhibited a strong relationship with Catarrhinis classical MHC-B-C loci. Sequence evolution and variability analysis indicated that Aotus MHC class I molecules experience inter-locus gene conversion phenomena, contributing towards their high variability.     

Moonstruck Primates: Owl Monkeys (Aotus) Need Moonlight for Nocturnal Activity in Their Natural Environment

Primates show activity patterns ranging from nocturnality to diurnality, with a few species showing activity both during day and night. Among anthropoids (monkeys, apes and humans), nocturnality is only present in the Central and South American owl monkey genus Aotus. Unlike other tropical Aotus species, the Azara''s owl monkeys (A. azarai) of the subtropics have switched their activity pattern from strict nocturnality to one that also includes regular diurnal activity. Harsher climate, food availability, and the lack of predators or diurnal competitors, have all been proposed as factors favoring evolutionary switches in primate activity patterns. However, the observational nature of most field studies has limited an understanding of the mechanisms responsible for this switch in activity patterns. The goal of our study was to evaluate the hypothesis that masking, namely the stimulatory and/or inhibitory/disinhibitory effects of environmental factors on synchronized circadian locomotor activity, is a key determinant of the unusual activity pattern of Azara''s owl monkeys. We use continuous long-term (6–18 months) 5-min-binned activity records obtained with actimeter collars fitted to wild owl monkeys (n = 10 individuals) to show that this different pattern results from strong masking of activity by the inhibiting and enhancing effects of ambient luminance and temperature. Conclusive evidence for the direct masking effect of light is provided by data showing that locomotor activity was almost completely inhibited when moonlight was shadowed during three lunar eclipses. Temperature also negatively masked locomotor activity, and this masking was manifested even under optimal light conditions. Our results highlight the importance of the masking of circadian rhythmicity as a determinant of nocturnality in wild owl monkeys and suggest that the stimulatory effects of dim light in nocturnal primates may have been selected as an adaptive response to moonlight. Furthermore, our data indicate that changes in sensitivity to specific environmental stimuli may have been an essential key for evolutionary switches between diurnal and nocturnal habits in primates.     

Chimpanzee (Pan troglodytes) birth patterns and human presence in zoological settings

In response to work demonstrating a negative correlation between human staff activity and parturition in laboratory-managed primates, this study examined the distribution of 231 captive chimpanzee (Pan troglodytes) births that occurred in accredited American zoological institutions by the day of the week on which the birth was discovered. We hypothesized that if chimpanzee parturition patterns displayed sensitivity to human presence, then fewer births per day would be reported during the weekend period, when the visitor density was high, as compared with the lower density working week. Analyses indicated that chimpanzee births were randomly distributed throughout the week. In the context of the questionable sensitivity of primate parturition to external influence, results suggest that variations in human presence do not affect the fine-level timing of birth in chimpanzees managed in a zoological setting.     

Factors associated with birth rate and live birth rate in multi-male breeding groups of rhesus monkeys

Reproductive records of 284 female rhesus monkeys housed in six multimale corrals at the California Primate Research Center were examined for the birth seasons 1977–1982 to determine possible associations between the probability of birth or live birth and female age, parity, origin, parturition in the previous season, infant birth date, and infant birth date in previous season. Multiple logistic regression analysis was used to identify and quantitate the effects of factors on the probability of birth or live birth, while controlling for the possibly confounding effects of other factors in the model. Females who had infants early in the previous season were 2.5 times as likely to give birth as those who had infants late in the previous season. Females with two or three previous births were 2.1 times as likely to give birth, and those with four or five previous births were 6.7 times as likely to give birth as were females with no or one previous birth. Controlling for other factors (age, parity, and timing of birth in the previous season), corralborn females were 3.3 times as likely to give birth as either wild-caught or domestic-born monkeys not native to the corrals. Domestic-born females who were not corral natives were 0.3 times as likely to have live births as wild-caught females. Births late in the season were 1.8 times as likely to result in live infants as births early in the season.     

The skin of primates. XLIV. Numerical taxonomy of primate skin

Data on 84 characteristics of the skin of 36 species of primates were extracted from a series of articles describing the histological and histochemical properties of the skin of primates. The data were subjected to a cluster analysis. The results were in reasonably good agreement with orthodox primate taxonomies although some exceptions were apparent. The species clustered into four main groups approximately comparable to Prosimii, Cercopithecoidea, Ceboidea, and Hominoidea. The internal arrangements of the Prosimii, Cercopithecoidea, and Hominoidea are commensurate with standard taxonomic practice. Within the Ceboidea, however, the Atelinae and Alouattinae tend to group with the Hominoidea, Aotus and Saimiri show variable placements, and Callimico groups with the Callithricidae.