mtDNA diversity in Azara's owl monkeys (Aotus azarai azarai) of the Argentinean Chaco

Owl monkeys (Aotus spp.) inhabit much of South America yet represent an enigmatic evolutionary branch among primates. While morphological, cytogenetic, and immunological evidence suggest that owl monkey populations have undergone isolation and diversification since their emergence in the New World, problems with adjacent species ranges, and sample provenance have complicated efforts to characterize genetic variation within the genus. As a result, the phylogeographic history of owl monkey species and subspecies remains unclear, and the extent of genetic diversity at the population level is unknown. To explore these issues, we analyzed mitochondrial DNA (mt DNA) variation in a population of wild Azara's owl monkeys (Aotus azarai azarai) living in the Gran Chaco region of Argentina. We sequenced the complete mitochondrial genome from one individual (16,585 base pairs (bp)) and analyzed 1,099 bp of the hypervariable control region (CR) and 696 bp of the cytochrome oxidase II (COII) gene in 117 others. In addition, we sequenced the mitochondrial genome (16,472 bp) of one Nancy Ma's owl monkey (A. nancymaae). Based on the whole mtDNA and COII data, we observed an ancient phylogeographic discontinuity among Aotus species living north, south, and west of the Amazon River that began more than eight million years ago. Our population analyses identified three major CR lineages and detected a high level of haplotypic diversity within A. a. azarai. These data point to a recent expansion of Azara's owl monkeys into the Argentinean Chaco. Overall, we provide a detailed view of owl monkey mtDNA variation at genus, species, and population levels.     

Density and population structure of owl monkeys (Aotus azarai) in the Argentinean Chaco

Owl monkeys are small monogamous primates ranging over a wide area extending from Panama to the Chaco region of northern Argentina. The Chaco, an alluvial plain covering over one million km2 of Argentina, Bolivia, Brazil, and Paraguay, consists of a mosaic of grasslands, savannas, xeric thorn forests, and gallery forests. The region shows significant seasonal variation in climate, rainfall, and food availability. The goal of this study was to determine the density, size, and structure of a population of Aotus azarai in the seasonal gallery forests of the eastern Argentinean Chaco. Reported population density, as well as group size and composition are based on data collected from 11 groups contacted on approximately 900 occasions, and observed for over 2,000 hours during a three-year period. Group and individual densities were 16 groups/km2 and 64 individuals/km2, respectively. Approximately half of the groups (n = 5) were small groups which had three individuals most of the time and never more than four, whereas the remaining groups were large groups composed of four or five individuals, and sometimes even six or seven individuals. This is the first study of A. azarai based on monitoring of a relatively large number of distinct groups. Our data suggest that owl monkeys in the seasonal subtropical forests of Formosa live at a density as high as those reported for owl monkey populations observed in tropical forests. The data also show that the social groups in the owl monkey population are of comparable size and composition to those characteristic of populations in the tropics.     

Rensch's rule, Bergmann's effect and adult sexual dimorphism in wild monogamous owl monkeys (Aotus azarai) of Argentina

Some monogamous primates are characterized by biparental care, territoriality, and a reduced level of physical dimorphism. In others, the relationship between those behavioral patterns and dimorphism is less clear. I tested Bergmann's and Rensch's rules using Aotus spp. body mass data and I characterized the extent of sexual dimorphism in body mass, dental and physical measurements in a socially monogamous owl monkey population (n = 91 adults) from the Argentinean Gran Chaco. A. azarai azarai from the Argentinean Chaco is larger than the more tropical owl monkey species (r = 0.7, N = 6 species), but there is no apparent increase in sexual dimorphism with increased body mass. The body masses of adult male and female A. a. azarai were remarkably similar (Mean = 1.26 kg); there were no marked sex differences in most skeletal measurements, but males had higher and wider upper and lower canines than did females. Body mass and neck circumference were positively and strongly related (r = 0.533, n = 52), and the body mass of adults was not a reliable indicator of their age (r = 0.03, n = 10). The data illustrate the complexities inherent in examining and summarizing within population variation in skeletal and nonskeletal measurements and contribute to a better understanding of the relationships between monogamous behavioral patterns and sexual dimorphism.     

Food transfers to young and mates in wild owl monkeys (Aotus azarai)

Accounts of food sharing within natural populations of mammals have focused on transfers to offspring or transfers of food items that are difficult to obtain (such as meat). Five groups of socially monogamous owl monkeys (Aotus azarai azarai) in Formosa, Argentina were observed during 107 hr to determine the pattern of food sharing under natural conditions. There were a total of 42 social interactions involving food with food being transferred on eight occasions. Adult males transferred food to young more often than did adult females. All types of food that were readily obtained and eaten by all age/sex classes were transferred to young. Adult females also transferred food to their mates. This type of food sharing is very rare among animals and may have social benefits specific to monogamous mammals with paternal care.     

Hormonal correlates of development and natal dispersal in wild female owl monkeys (Aotus azarae) of Argentina

Pair-living and socially monogamous primates typically do not reproduce before dispersing. It is currently unclear whether this reproductive suppression is due to endocrine or behavioral mechanisms. Cooperatively breeding taxa, like callitrichids, may forego reproduction in natal groups because they reap inclusive fitness benefits and/or they are avoiding inbreeding. However, neither of these benefits of delayed reproduction appear to adequately explain the lack of reproduction prior to leaving the natal group in pair-living monogamous species. In this study, we determined whether wild Azara's owl monkeys (Aotus azarae) in the Argentinean Chaco establish reproductive maturity prior to dispersing. We utilized 635 fecal extracts to characterize reproductive hormone profiles of 11 wild juvenile and subadult females using enzyme immunoassays. Subadult females showed hormone profiles indicative of ovulatory cycling and had mean PdG and E1G concentrations approximately five times higher than juveniles. Contrary to expectations from the inbreeding avoidance hypothesis, female owl monkeys do not delay puberty, but rather commence ovarian cycling while residing in their natal group. Still, subadults appear to have a period during which they experience irregular, non-conceptive cycles prior to reproducing. Commencing these irregular cycles in the natal group may allow them to develop a state of suspended readiness, which could be essential to securing a mate, while avoiding costs of ranging solitarily. Our results indicate that reproductive suppression in female owl monkeys is not due to endocrine suppression. We suggest that adults likely use behavioral mechanisms to prevent subadults from reproducing with unrelated adult males in their natal group.     

Environmental Determinants of Birth Seasonality in Night Monkeys (Aotus azarai) of the Argentinean Chaco

The night monkeys (Aotus azarai) of Formosa, Argentina provide an opportunity to investigate the influences of ambient temperature and photoperiod on reproduction in a highly seasonal environment: the Chaco. Between 1997 and 2000, we collected data to evaluate the relationship between rainfall, ambient temperature, photoperiod and food availability and the annual distribution of mating behavior and births in 15 groups of monkeys in the forests of the Eastern Argentinean Chaco. Our data show that the area is highly seasonal, characterized by significant fluctuations in rainfall, temperature, photoperiod and food availability. There are two rain peaks in April and November and a dry season lasting from June to August. Monthly mean temperatures were on average 11°C lower during winter months than they were during summer months. Temperatures <10°C and >33°C were also frequent through the year. Days are 3 h longer during the summer than during the winter months. Insect abundance and the percentage of tree species producing fruits, flowers or new leaves reached a low in the coldest winter months. Mating was infrequent, and we only observed it between May and September. Half the births (n = 13) occurred during a 2-week period in October. Infant survival during the first 6 mo of life was high (96%). Our findings suggest an environmental control of reproduction. Changes in photoperiod and temperature may promote reproductive activity in females that might conceive and begin pregnancy at a time void of high temperatures that could be metabolically challenging.     

Disappearances of individuals from social groups have implications for understanding natal dispersal in monogamous owl monkeys (Aotus azarai)

The socially monogamous owl monkeys (Aotus spp.) live in small groups of two to five individuals. We used monthly demographic data collected from 16 social groups between 1997-2001 to estimate the age of disappearance from their natal groups and the timing of those disappearances in a population of owl monkeys (Aotus azarai azarai) in Formosa, Argentina. We applied survival analysis techniques to 48 months of observations of 47 individuals to construct age-specific probabilities of disappearance. Two-thirds of the individuals (eight of 12), for which disappearance could be well timed, disappeared at around 2 years of age. The average age at disappearance for these individuals was 29 months (+/-8), whereas the mean age of disappearance obtained from the survival analysis of censored and uncensored data was almost 3 years (mean+/-SD, 35+/-3 months). Ninety-two percent of all disappearances of adult size individuals (11 of 12) occurred around the birth season. Our data suggest that at least some individuals disperse soon after sexual maturation while others remain for up to 4 years in their natal groups.     

An optimized microsatellite genotyping strategy for assessing genetic identity and kinship in Azara's owl monkeys (Aotus azarai)

In this study, we characterize a panel of 20 microsatellite markers that reproducibly amplify in Azara's owl monkeys (Aotus azarai) for use in genetic profiling analyses. A total of 128 individuals from our study site in Formosa, Argentina, were genotyped for 20 markers, 13 of which were found to be polymorphic. The levels of allelic variation at these loci provided paternity exclusion probabilities of 0.852 when neither parent was known, and 0.981 when one parent was known. In addition, our analysis revealed that, although genotypes can be rapidly scored using fluorescence-based fragment analysis, the presence of complex or multiple short tandem repeat (STR) motifs at a microsatellite locus could generate similar fragment patterns from alleles that have different nucleotide sequences and perhaps different evolutionary origins. Even so, this collection of microsatellite loci is suitable for parentage analyses and will allow us to test various hypotheses about the relationship between social behavior and kinship in wild owl monkey populations. Furthermore, given the limited number of platyrrhine-specific microsatellite loci available in the literature, this STR panel represents a valuable tool for population studies of other cebines and callitrichines.     

Cardiomyopathy in captive owl monkeys (Aotus nancymae)

Dilated cardiomyopathy (DCM) was identified histopathologically in a colony of owl monkeys (Aotus nancymae) over a 15-year period. We characterized the incidence of cardiac disease echocardiographically in the colony over a 14-month period. Of 77 monkeys, 21 had systolic myocardial failure, and postmortem examination confirmed the antemortem diagnosis of DCM in eight animals. Monkeys with a questionable diagnosis at the first examination demonstrated progression of disease with time. Left ventricular end-systolic cross-sectional area and left ventricular fractional area change were the indices that most reliably discriminated between normal and diseased animals. Serum cardiac troponin I concentrations were below detectable limits in normal and diseased monkeys. The apparent high prevalence of disease in this colony precluded establishment of reference intervals for Aotus nancymae. Our study provides the first comprehensive echocardiographic evaluation of owl monkeys with cardiomyopathy.     

Mortality causes of owl monkeys (Aotus nancymae and Aotus vociferans) in captivity

To determine the main causes of death in "owl monkeys" (Aotus nancymae and A. vociferans) in captivity, 115 necropsies were performed. According to the macroscopic findings and clinical data, results are as follow: acute lobular pneumonia (25.2%), chronic nephropathy (10.4%), acute catarrhal enteritis (8.7%), acute hemorrhagic enteritis (7%), acute toxic hepatitis (5.2%), trauma (5.2%), and others.     

Uterine evaluation and gestation diagnosis in owl monkey (Aotus azarai infulatus) using the B mode ultrasound

BACKGROUND: Gynecological and obstetrical ultrasonography has become an indispensable tool in the routine management, health evaluation and research on captive non-human primates. METHODS: Ultrasound was used to evaluate the uterus and estimate the gestation of owl monkeys. Twelve couples were selected, where five were primiparous and seven multiparous females from the National Primate Center reproductive colony, Ananindeua-PA, Brazil. The procedures were carried out using the GE Logiq 100 MP, equipped with a 7.5 MHz linear probe. RESULTS: The females showed a simple uterus, of elongated shape, regular outline and homogeneous echogenic texture. In the uterine measurements craniocaudal diameter, dorsoventral diameter and uterine volume (UV), significant differences were identified (P < 0.05) between ultrasound examinations of primiparous and multiparous females. The UV showed a positive correlation with the number of births. The gestational sac and the embryonic echo were visible between 28 and 38 days after mating. Between 48 and 68 days after mating, embryonic death was identified in all the gestations. CONCLUSIONS: The chemical (use of tranquilizers) and husbandry factors (capture stress) may be related to the prenatal death. The establishing methods of conditioning the female to the ultrasonographic exam may offer a solution to this problem.     

Adaptation of Plasmodium vivax to growth in owl monkeys (Aotus nancymai)

The purpose of this study was reactivation and adaptation of a strain of Plasmodium vivax to Aotus nancymai monkeys. A need arose for malarial parasites for use in serologic and molecular studies and for teaching slides. This particular strain of parasite had been characterized previously as producing high-density parasitemia in splenectomized New World monkeys and therefore represented a good candidate for reactivation. P. vivax (Vietnam II), isolated in 1970, was reactivated after adaptation in Aotus lemurinus griseimembra monkeys nearly 33 years earlier and adapted to A. nancymai monkeys. Passage was achieved by intravenous inoculation of parasite blood stages into splenectomized A. nancymai monkeys. Parasitemia was determined by analyzing daily blood smears stained with Giemsa. Maximum parasite counts ranged from 10,630 to 94,000 parasites/microl; the mean maximum parasite count for the four animals was 39,565 parasites/microl. Parasite counts of > 10,000/microl were maintained for 2 to 64 days. After only three passages of the parasite, attempts to reactive were successful. A. nancymai proved a suitable animal model for the recovery of this parasite. In conclusion, successful reactivation and adaptation of this parasite offers the capability to perform a series of diagnostic, immunologic, and molecular studies as well as to provide otherwise potentially unavailable teaching materials to healthcare professionals.     

Social patterns of food sharing in monogamous owl monkeys

Captive owl monkeys (Aotus nancymaae, A. azarai) share food frequently within both families and pairs. In this study food sharing was observed in seven mated pairs and four families (i.e., four mated pairs and their offspring). Patterns of food sharing were examined with respect to age class, sex, and the presence or absence of dependent offspring. Within families, most food transfers were from adult males to developing offspring. Adult males and females transferred food to their mates in caged pairs as well as in family units. Food interactions between adults are as likely to result in food transfers as those between adults and offspring. This pattern of food sharing between mates in a monogamous species may serve both nutritional and social functions that differ from those in polygamous species.