Erythrocytes and erythrocyte morphologies of healthy and colony-born owl monkeys (Aotus lemurinus griseimembra)

Inadequate availability of hematological reference data seriously restricts optimal utilization of the owl monkey (Aotus lemurinus griseimembra) as an experimental model. The current study investigated erythrocytic morphology in peripheral blood of healthy, colony-born owl monkeys. The blood of the subjects contained discoid erythrocytes, poikilocytes, and showed considerable anisocytosis. Also observed were nucleated erythrocytes, erythrocytes with Howell-Jolly bodies, and reticulocyte types I, II, and III. Heinz bodies were not detected.     

Chromosome evolution in the owl monkey,Aotus

We have reported nine distinct karyotypes for Aotus, of four pelagic phenotypes, and suggest that this single species has undergone extensive subspeciation. We reconstruct the mechanism of chromosomal evolution and propose a hypothesis about the events of subspeciation in Aotus. We speculate that isolated groups of ancestral individuals living in several confined areas have separately accumulated a fusion or inversion pair as a result of inbreeding. A subsequent reassociation of descendants from these individuals led to the formation of offspring with mixtures of fusion or inversion pairs in their complements. They, in turn, radiated into different ecological niches accompanied by adaptive genetic changes and eventually gave rise to the present forms of Aotus distinguishable by their karyotypes, but not easily recognizable by ordinary taxonomic criteria.     

Internal desynchronization of the circadian activity and feeding rhythm in an owl monkey (Aotus lemurinus griseimembra): a case study

In the free-running circadian locomotor activity rhythm of a 7-year-old male owl monkey (Aotus lemurinus griseimembra) kept under constant light and climatic conditions (LL 0.2 lux, 25°C ± 1°C, 60 ± 5% relative humidity [RH]), a second rhythm component developed that showed strong relative coordination with the free-running activity rhythm of 24.4h and a 24h rhythm. The simultaneously recorded feeding activity rhythm strongly resembled this rhythm component. Therefore, it seems justified to infer that there was an internal desynchronization between the two behavioral rhythms or their circadian pacemakers, that is, between the light-entrainable oscillator located in the suprachiasmatic nuclei (SCN) and a food-entrainable oscillator located outside the SCN. This internal desynchronization may have been induced and/or maintained by a zeitgeber effect of the (irregular) 24h feeding schedule on the food-entrainable oscillator. The weak relative coordination shown by the activity rhythm indicates a much weaker coupling of the light-entrainable oscillator to the food-entrainable oscillator than vice versa. (Chronobiology International, 17(2), 147-153, 2000)     

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.     

Puberty in the male owl monkey (Aotus trivirgatus griseimembra): A study of physical and hormonal development

In the male owl monkey (Aotus trivirgatus),the onset of puberty occurs at between 211 and 337 days (median, 313) as indicated by longitudinal measurements of plasma testosterone in six subjects. Larger rises in plasma testosterone were observed between 300 and 400 days. Pubertal increases in body weight and testicular volume are not pronounced in this species. Young animals first entered the weight range for adult males (800–1080 g) when they were between 370 and 520 days of age (median, 472). Marked growth of the subcaudal scentmarking gland occurred during puberty. The first signs of development of this gland (stiffening and discoloration of overlying hairs) were noted between 282 and 370 days (median 316), and it had attained an adult structure by 336–442 days (median, 397). These changes were androgen dependent as indicated by the fact that treatment of a prepubertal male with testosterone stimulated the subcaudal gland to develop prematurely. Hormonal and physical changes during puberty were the same whether males remained with their parents or were caged alone. There was no indication that puberty was retarded in males which had remained in their natal groups.     

Urinary enzyme concentrations in the owl monkey (Aotus nancymae)

The activity of three urinary enzymes, alkaline phosphatase (ALP), aspartate aminotransferase (AST), and N-acetyl-β-D-glucosaminidase (NAG), was evaluated in 71 adult owl monkeys. Fifty-six animals had normal renal function, while 15 had evidence of renal dysfunction. Urinary enzyme: urinary creatinine ratios (U_E:U_Cr) were also determined. The activity for NAG was similar to that of other species, while ALP and AST were higher. Regression analyses revealed that urinary enzymes and U_E:U_Cr were significantly correlated (P ≤ 0.0001) with indices of renal damage and could identify active renal disease.     

Direct modulation of activity and body temperature of owl monkeys (Aotus lemurinus griseimembra) by low light intensities

The activity pattern of Aotus lemurinus griseimembra can be predictably altered by varying the illuminance during the dark phase of a 12:12-hour light:dark rhythm. Intensities well below full-moon brightness (0.1-0.5 lx) severely inhibit activity. This modulation is not the result of a light-induced phase shift of the circadian rhythm, but it is primarily caused by masking due to direct effects of light on the motor system. Both proportional and differential effects of light are involved. Miniature transmitters were implanted intraperitoneally in two Aotus females so that the core temperature could be measured in parallel with locomotor activity. The responses to brief reductions of the dark-phase illuminance, from 10(-1) to 10(-3) lx, 10(-5) lx or physiological darkness, indicate that the direct effects of light that modulate the activity of the owl monkeys also affect their temperature time-course. The influence on the temperature rhythm, unlike that on the activity rhythm, varies greatly over the circadian period. The finding that the core temperature does not always change in parallel with locomotor activity and, to some extent, reacts differently to the light:dark alternation indicates that temperature does not simply follow activity passively, but rather is partially subject to a 'direct' masking influence of the light.     

Proliferative response of peripheral blood lymphocytes to mitogens in the owl monkey Aotus nancymae

The new world primate Aotus sp. has been recommended by the World Health Organization as a model for evaluation of malaria vaccine candidates, given its susceptibility to experimental infection with the human malaria parasites Plasmodium falciparum and P. vivax. The present study examined the in vitro proliferative response of peripheral blood mononuclear cells (PBMCs) isolated from Aotus monkeys, utilizing a wide range of mitogens. Results presented herein demonstrate that the in vitro proliferative response of PBMCs from the Aotus sp. is quite variable from monkey to monkey for each of the mitogens assessed. PBMCs from the Aotus monkey exhibited a delayed kinetic proliferative response and, particularly, a different sensitivity to proliferation in response to various concentrations of Phytohemagglutinin-P and favin lectins, the phorbol ester Phorbol myristate acetate and the calcium ionophore ionomycin. Altogether, our findings are consistent with the conclusion that the in vitro proliferative response of PBMCs from the Aotus differ in their activation requirements compared with PBMCs from humans.     

Two new species of night monkeys,genus Aotus (Cebidae,platyrrhini): A preliminary report on Aotus taxonomy

The nine allopatric species of Aotus recognized represent two natural groups distinguished by karyotype, color, and pelage patterns. Correlated with these group characters are reported differences in serum proteins and degrees of susceptibility or immunity to experimental infection with malarial parasites. The primitive gray-neck species group of Aotus contains A. brumbacki (new species), A. lemurinus (with subspecies lemurinus and griseimembra), A. trivirgatus, and A. vociferans. The derived red-neck group contains A. nancymai (new species), A. miconax. A. infulatus, and A. azarae (with subspecies azarae and boliviensis). Only the two new species are described but a key to the species and subspecies gives the diagnostic characters of each. The gray-neck group occurs almost entirely north of the Amazon, the red-neck group almost entirely south. The distributional exceptions are enclave populations resulting from river bend cutoffs. Formation of an enclave population of A. nancymai is discussed and available information on the biology of this species is reported.     

Reactivity of human T-lymphocyte-specific antibodies with peripheral blood mononuclear cells and spleen of Aotus azarae ssp. boliviensis (owl monkey)

Aotus monkeys offer one of the few models that can be used for the evaluation of the immunogenicity and efficacy of new vaccine candidates against the human malarias, Plasmodium falciparum and Plasmodium vivax. However, the tools available for evaluation of the immune responses in these New World primates are still limited. In the present study, a previously selected set of monoclonal antibodies that were raised against human T cell determinants and were reactive with at least one other primate species was investigated for its reactivity with Aotus lymphocytes using FACS analysis, indirect immunofluorescence (IFA) and immunohistochemistry. From a panel of 19 mAb, six were found to react consistently with Aotus lymphocytes using FACS analysis. Further evaluation of the mAb using IFA confirmed these findings. Analysis of the selected mAb on spleen sections of Aotus monkeys identified one anti-CD4 and one anti-CD8 mAb that can be used for immunohistochemical studies. The set of mAb identified in this study can be used for the detection of various T lymphocyte markers in peripheral blood and in tissues of Aotus monkeys. Together with data published by others, mAb are now identified for detection of six different markers of Aotus T lymphocytes. These mAb are very valuable for the characterisation of immune responses after vaccination and infection in the Aotus malaria models.     

Partial characterization of the CD45 phosphatase cDNA in the owl monkey (Aotus vociferans)

CD45 is a protein tyrosine phosphatase implicated in T and B cell activation, differentiation, and development. It dephosphorylates specific tyrosine residues on its substrates, principally on the Src-family of protein tyrosine kinases, thus regulating T cell or B cell activation during the immune response. In this study, we present the partial CD45 nucleotide and deduced amino-acid sequences for the owl monkey (Aotus vociferens). There is 97% identity in the nucleotide sequence and 96% in the amino acid sequence with the human counterpart. Aotus CD45 undergoes alternative splicing on the extracelular N-terminal tail, and has several conserved features characteristic of other species. This includes the two Tyr phosphatase domains and some residues and/or motifs involved in docking of signaling molecules, intramolecular interactions, and CD45 activity and activity regulation (YINAS, GXGXXG, WPD, and YWP motifs, and the Cys residues). This suggests that the Aotus CD45 molecule is a functional enzyme and that initial lymphocyte activation in Aotus monkeys and humans is very similar. Together with previous reports from our laboratory, this work supports the contention that immune responses in Aotus are similar to those of humans, and supports the strategy for using this experimental model for studies on activation of T lymphocytes in response to specific antigens.     

Comparison of blood and urine analytes between two karyotypes of owl monkey,Aotus nancymae and Aotus vociferans

Serum and urine analytes were compared between two karyotypes of owl monkey, Aotus nancymae and A. vociferans, to determine if normative clinical pathology data obtained from one karyotype were applicable to the other. Statistically significant differences (P ≤ 0.05) were noted in serum calcium, serum phosphorus, serum sodium, serum potassium, serum urea nitrogen, urine calcium, calcium clearance, and fractional clearance of calcium between the two karyotypes. The results suggest that A. vociferans regulate calcium-phosphorus and electrolyte homeostasis in a manner different from that of A. nancymae.     

Spontaneous cardiomyopathy and nephropathy in the owl monkey (Aotus sp.) in captivity.

Clinical and pathologic data were reviewed for 72 owl monkeys that died between January 1987 and May 1990 at the Center for Reproduction and Conservation of Nonhuman Primates in Iquitos, Peru. Tissue samples from 39 animals were examined. Hypertrophic cardiac disease (51% of animals examined), dilative cardiomyopathy (26%), and nephropathy (87%) were the most common diagnoses. The incidence of all three diseases appeared to increase with time in captivity. Nephropathy was less severe in colony-born animals.     

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.     

Tuberculosis-like lesions arising from the use of Freund's complete adjuvant in an owl monkey (Aotus sp.)

An apparently normal, non-tuberculin-reacting, splenectomized owl monkey presented tuberculosis-like lesions of the lung at necropsy. Histological and bacteriological examination failed to demonstrate the presence of acid-fast organisms. Retrospective inquiry showed the animal had been inoculated using complete Freund's adjuvant during a malaria vaccine trial. Lesions observed were compatible with lipid embolism of the adjuvant in the lungs.     

Radiographic determination of bone maturation as an aid in predicting chronologic age in the owl monkey (Aotus trivirgatus)

The skeletal development of laboratory-bred owl monkeys (Aotus trivirgatus) ranging from 37 days to 58 months of age was examined radiographically. Femoral length, time of epiphyseal ossification, and fusion of various ossification centers were studied. Chronologic age can be predicted by femoral length determination up to 18 months. Initial ossification of calcaneal, tibial tuberosity, iliac crest, and ischial apophyses occurs between 5.5 and 14 months. Fusion of various secondary ossification centers allows age determination from 7.5 months to 58 months.     

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.     

Long-term effect of a simple nest-box on the reproductive efficiency and other life traits of an Aotus lemurinus lemurinus monkey colony: an animal model for malaria research

Background The long‐term effect of a PVC pipe nest‐box on the reproductive efficiency and other life traits of an Aotus monkey‐breeding colony have not been characterized. Methods and Results We analyzed laboratory records of the Gorgas Memorial Institute (GMI) Aotus monkey colony in Panama for the period 1999–2010 and found a 273% increase in the annual mean life births in the following 7 years after the introduction of a PVC pipe nest‐box in 2002, as well as increases in the mean body mass and survival of laboratory‐bred monkeys. Other life traits such as inter‐birth interval, parity, birth sex distribution, mortality, and longevity were also determined. Conclusions The use of a PVC pipe nest‐box significantly improved the reproductive efficiency and other life traits of the GMI Aotus breeding colony.     

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.