Population densities and geographic distribution of night monkeys (Aotus nancymai and Aotus vociferans) (cebidae: Primates) in Northeastern Peru

Population densities of two species of night (or owl) monkeys (Aotus nancymai and Aotus vociferans) were estimated using transect census methods. Densities of Aotus nancymai were approximately 46.3 individuals/km² in lowland forests and 24.2 individuals/km² in highland forests. For Aotus vociferans densities were 33.0 individuals/km² in lowland forests and 7.9 individuals/km² in highland forests. A. vociferans occurs north of the Río Amazonas-Marañon and A. nancymai south of it, except for the northern enclave between the Ríos Tigre and Pastaza. The two species are nowhere sympatric. However, the two known karyotypic forms of A. vociferans occupy the same habitats throughout the Peruvian range of the species.     

Anatomical distribution of developing trophozoites and schizonts of Plasmodium vivax in Aotus lemurinus lemurinus and Saimiri sciureus

Organ distribution of developing trophozoite- and schizont-infected erythrocytes of Plasmodium vivax and night monkeys, Aotus lemurinus lemurinus, and squirrel monkeys, Saimiri sciureus, was determined. The primary site for the infection in both species was the splenic vasculature. Secondary organ involvement differed between hosts although some overlapping did occur.     

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.     

Use of spatial, visual, and olfactory information during foraging in wild nocturnal and diurnal anthropoids: A field experiment comparing Aotus, Callicebus, and Saguinus

Early in their evolution, the ancestors of anthropoid primates radiated from a nocturnal to a diurnal niche. Foraging during the night differs from foraging during the day in terms of the availability of light and color cues, and in the movement of odor molecules through the canopy. In this study, we compared the ability of nocturnal and diurnal New World monkeys to use perceptual cues (i.e., the sight or smell of food) and spatial information (place predictability) in within-patch foraging decisions. An experimental field study was conducted on wild groups of night monkeys (Aotus nigriceps), tamarins (Saguinus imperator imperator and S. fuscicollis weddelli), and titi monkeys (Callicebus cupreus) at the Zoobotanical Park/UFAC, Rio Branco, Brazil. Our research design included the construction of feeding stations located in the home range of the study groups. Each feeding station consisted of eight visually identical feeding platforms located in a circular arrangement. In all test settings, two platforms at each feeding station contained a food reward (banana), and the remaining six platforms contained a sham reward (yellow plastic or inaccessible banana). In the night-monkey experiments, each feeding platform was illuminated by a 40-W red bulb to aid the researcher in observing their behavior. When the location of reward sites was predictable over time, individuals in all four species successfully relocated food rewards based solely on spatial information. Each species was also successful in using visual information to distinguish real from sham food rewards. However, only night monkeys and one group of emperor tamarins used olfactory information alone to locate food rewards. Overall, the species' performances did not clearly differentiate Aotus from diurnal New World primates in these experiments.     

Urinary excretion of catecholamines in the night monkey (Aotus trivirgatus) (Primates, Cebidae)

A seasonal variation in the urinary catecholamines output has been demonstrated in two simians kept under constant ambient conditions : the nocturnal Aotus and the diurnal Sa?miri sciureus. In Aotus, catecholamines output (NA + A), in spring, is higher than in other Primates including man and even more so in winter. Cold exposure increases the NA + A excretion in Aotus as it does in squirrel monkey and rat but the A output is particularly prominent in Sa?miri. Fasting does not alter significantly the catecholamines excretion. Associated fasting and cold exposure do not modify the adrenosympathetic response observed in Aotus in cold conditions alone, but depresses the sympathetic activity and greatly enhance the adrenomedullary excretion in squirrel monkey, as it is the case in rat. Associated fasting and cold represents a highly stressful situation for squirrel monkey but not for night monkey. Catecholamines metabolites (MN, NMN, DOPAC, HVA, VMA and MHPG) are found in urine of both species, DOPAC and VMA being predominant in Aotus but DOPAC and MHPG in Sa?miri. The proportions of conjugated forms vary according to the metabolite : DOPAC and VMA are mainly under free form but NMN, MN and MHPG are mostly conjugated in both species. The daily output of pooled adrenergic metabolites (expressed as ng/mg creatinine) is higher in Aotus than in Sa?miri and man. Both monkey species display a high adrenosympathetic activity which does not correlate with their resting metabolic rate.     

Adaptation of the AMRU-1 strain of Plasmodium vivax to Aotus and Saimiri monkeys and to four species of anopheline mosquitoes.

A chloroquine-resistant strain of Plasmodium vivax (AMRU-1) from Papua New Guinea has been adapted to grow in 4 species of Aotus monkeys (Aotus lemurinus griseimembra, Aotus vaciferans, Aotus nancymai, and Aotus azarae boliviensis), hybrid Aotus monkeys, and Saimiri boliviensis monkeys. Whereas it was possible to infect Saimiri monkeys with this parasite by inoculation of parasitized erythrocytes, only 42% of Saimiri monkeys became infected, compared to 92% of Aotus monkeys attempted. Comparative mosquito feedings showed that only A. vociferans, A. l. griseimembra, and Saimiri boliviensis monkeys produced infections in mosquitoes. Oocysts were observed on the guts of the 4 species of mosquitoes used (Anopheles gambiae, Anopheles stephensi, Anopheles freeborni, and Anopheles dirus), but sporozoite transmission was effected only with the intravenous inoculation of sporozoites from An. dirus into an A. l. griseimembra monkey.     

Species tree estimation for a deep phylogenetic divergence in the New World monkeys (Primates: Platyrrhini)

The estimation of a robust phylogeny is a necessary first step in understanding the biological diversification of the platyrrhines. Although the most recent phylogenies are generally robust, they differ from one another in the relationship between Aotus and other genera as well as in the relationship between Pitheciidae and other families. Here, we used coding and non-coding sequences to infer the species tree and embedded gene trees of the platyrrhine genera using the Bayesian Markov chain Monte Carlo method for the multispecies coalescent (?BEAST) for the first time and to compared the results with those of a Bayesian concatenated phylogenetic analysis. Our species tree, based on all available sequences, shows a closer phylogenetic relationship between Atelidae and Cebidae and a closer relationship between Aotus and the Cebidae clade. The posterior probabilities are lower for these conflictive tree nodes compared to those in the concatenated analysis; this finding could be explained by some gene trees showing no concordant topologies between Aotus and the other genera. Moreover, the topology of our species tree also differs from the findings of previous molecular and morphological studies regarding the position of Aotus. The existence of discrepancies between morphological data, gene trees and the species tree is widely reported and can be related to processes such as incomplete lineage sorting or selection. Although these processes are common in species trees with low divergence, they can also occur in species trees with deep and rapid divergence. The sources of the inconsistency of morphological and molecular traits with the species tree could be a main focus of further research on platyrrhines.     

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.     

Abundance, diversity, and patterns of distribution of primates on the Tapiche River in Amazonian Peru

This work presents data on the relative diversity, abundance, and distribution patterns of primates in a 20 km2 area of the Tapiche River in the Peruvian Amazon. Population data were collected while the study area was both inundated and dry (March to September 1997) using conventional line-transect census techniques. Survey results reflected the presence of 11 primate species, but population parameters on only eight of the species will be presented, including saddleback tamarins (Saguinus fuscicollis), Bolivian squirrel monkeys (Saimiri boliviensis), brown capuchins (Cebus apella), white-fronted capuchins (Cebus albifrons), monk sakis (Pithecia monachus), red titi monkeys (Callicebus cupreus), red uakaris (Cacajao calvus), and red howler monkeys (Alouatta seniculus). Woolly monkeys (Lagothrix lagotricha), night monkeys (Aotus nancymaae), and pygmy marmosets (Callithrix pygmaea) were also seen in the area. The data for the smaller-bodied primates is similar to that reported almost 18 years earlier, but the data for the larger-bodied primates reflect a loss in the number of animals present in the area. Pressure from hunters and the timber industry may account for declining numbers of large-bodied primates, while it appears that natural features peculiar to the conservation area contribute to the patchy pattern of distribution.     

Visual capacities of the owl monkey (Aotus trivirgatus): temporal contrast sensitivity.

Aotus monkeys were tested in a forced-choice discrimination task to determine their ability to discriminate sinusoidally flickering lights varying in temporal frequency and luminance contrast. Under conditions of moderate light adaptation this primate is maximally sensitive to lights flickering at 10 Hz while the highest frequency they can discriminate is about 42 Hz. At very low light levels (10(-5) ft L) maximum sensitivity is for 2.2--5 Hz flicker. The highest flicker rate that could be discriminated under these conditons was about 29 Hz. In comparison to humans tested in the same situation. Aotus monkeys show relatively lower sensitivity to temporal flicker under conditions of light adaptation but relatively higher sensitivity at very low light levels.     

Sharing of sleeping sites betweenAotus vociferans with other mammals in the Peruvian Amazon

In studies performed during 1986, 1987, 1990, and 1991, in the seasonally flooded forest of the Napo and Nanay river basin, we recorded seven instances of cohabitation in night monkeys,Aotus vociferans. Cohabitation refers to the sharing of a sleeping site of one species of animal with other different species of animals (Aquino & Encarnacion, 1986). We also recorded two instances of cooccupation of night monkeys with other species of nocturnal mammals. Cooccupation refers to the independent use of different sleeping sites within the same tree by two or more species of animals. This study is the first report of cooccupation within the generaAotus. Forty-five sleeping trees with entrance holes were used by the night monkeys. In addition, one sleeping site was observed in a small concavity of the foliar sheath on aMauritia flexuosa palm.     

Phylogenetic relationships of the New World monkeys (Primates, platyrrhini) based on nuclear G6PD DNA sequences

In order to test hypotheses about the phylogenetic relationships among living genera of New World monkeys, 1.3 kb of DNA sequence information was collected for two introns of the glucose-6-phosphate dehydrogenase (G6PD) locus, encoded on the X chromosome, for 24 species of New World monkeys. These data were analyzed using a maximum parsimony algorithm. The strict consensus of the three most-parsimonious gene trees that result shows support for the following clades: a pitheciine clade including Callicebus within which Chiropotes and Cacajao are sister taxa, an Alouatta-atelin clade within which Brachyteles is the sister taxon of Lagothrix and which is sister to another clade containing the callitrichines, and a callitrichine/Aotus/Cebus/Saimiri clade. Within the callitrichines, Callimico is the sister taxon of Callithrix. Cebus and Saimiri form a clade. These results are broadly consistent with previously published DNA sequence analyses of platyrrhine phylogeny and provide additional support for groupings provisionally proposed in those earlier studies. Nevertheless, questions remain as to the relative phylogenetic placement of Leontopithecus and Saguinus, the branching order within the Aotus/Cebus/Saimiri/callitrichine clade, and the placement of the pitheciine clade relative to the atelines and the callitrichines.     

Platelet kinetics and other hematological profiles in experimental Plasmodium falciparum infection: a comparative study between Saimiri and Aotus monkeys.

Levels of platelets and other hematological values were monitored in 21 Saimiri and 12 Aotus monkeys over a period of three weeks post-infection with monkey-adapted Indochina CDC-1 strain of Plasmodium falciparum. In both Saimiri sciureus boliviensis and Aotus nancymai karyotype-1 monkeys the severest thrombocytopenia was observed at 14 days post-infection coinciding with peak parasitemia, neutropenia, lymphocytosis, and anemia associated with severe hemoglobinemia and elevated fibrinogen degeneration products(FDP's). MCH and MCV profiles in Aotus monkeys decreased with ascending parasitemia. In contrast, these parameters in Saimiri were characterized by a significant compensatory increase correlating with parasitemia. In general, thrombocytopenia was one of the earliest clinical manifestations of the infection with the platelets returning to normal levels shortly after peak parasitemia at 14 days. Platelet kinetics had a strong correlation with hematologic and parasitologic values in the Aotus model. No consistent associations were observed between platelet kinetics and other parameters in the Saimiri model. These data indicate that the Aotus model for malaria is more predictable than the Saimiri. Further, platelet turnover rates and recovery provide a useful prognostic parameter during malaria infection. The results are discussed in relation to the value of the two species of monkeys as models for the pathogenesis of human malaria.     

Endemic infections of Parastrongylus (=Angiostrongylus) costaricensis in two species of nonhuman primates, raccoons, and an opossum from Miami, Florida

Parastrongylus (=Angiostrongylus) costaricensis was first reported in the United States from cotton rats, Sigmodon hispidus, in Texas in 1979. Here, we report the findings of P. costaricensis in a siamang (Hylobates syndactylus) from the Miami MetroZoo, in 2 Ma's night monkeys (Aotus nancymaae) from the DuMond Conservancy located at Monkey Jungle in Miami, in 4 raccoons (Procyon lotor) trapped near the MetroZoo, and in an opossum (Didelphis virginiana) trapped at the MetroZoo. These records are the first records of P. costaricensis from all 4 species of hosts. All of the primates were zoo-born, and the raccoons and opossum were native, indicating that this parasite is now endemic at these 2 sites.     

Dark switch in the entrainment of circadian activity rhythms in night monkeys. Aotus trivirgatus humboldt

1. The locomotor activity of the night monkey (Aotus trivirgatus) has been shown to be related to light intensity by an optimum function; here entrainment by LD cycles is examined to see whether the mechanism of synchronization of circadian periodicity in Aotus is based on this function. 2. Eleven night monkeys of various ages, previously in either a free-running phase or in LD 12:12 (10(2):10(-1) lux), were recorded in LD 12:12 with the optimal intensity (10(-1) lux) in the light part of the cycle and a suboptimal intensity (10(-3) lux) in the dark part. 3. In all cases the monkeys synchronized in such a way that their activity phase fell in the dark part of the LD cycle. 4. The implication is that Aotus is a true dark-active species, that the illumination-dependent activity maximum at 10(-1) lux does not affect the synchronization mechanism, and that the differential (direction of change) rather than proportional (absolute level) actions of light provide the decisive cue for synchronization of the circadian activity rhythm.     

Genetic variability in natural populations of the Brazilian night monkey (Aotus infulatus)

Seventy-one night monkeys from both banks of the Tocantins River in Brazilian Amazonia were examined for 12 blood protein loci. The results indicate remarkable differences between the subpopulations of the two banks for the CA2, PGD, and GPI polymorphic systems. The average heterozygosity values of Aotusfor the west and east bank populations were 2.2 and 5.9, respectively. These results and the difficulties in delimiting species in this genus may indicate a relatively recent spur of evolutionary differentiation.     

Adaptation of a strain of Plasmodium vivax from India to New World monkeys, chimpanzees, and anopheline mosquitoes.

A strain of Plasmodium vivax from India was adapted to develop in splenectomized Saimiri boliviensis, Aotus lemurinus griseimembra, A vociferans, A. nancymai, A. azarae boliviensis, hybrid Aotus monkeys, and splenectomized chimpanzees. Infections were induced via the inoculation of sporozoites dissected from the salivary glands of Anopheles stephensi and An. dirus mosquitoes to 12 Aotus and 8 Saimiri monkeys; transmission via the bites of infected An. stephensi was made to 1 Aotus monkey and 1 chimpanzee. The intravenous passage of infected erythrocytes was made to 9 Aotus monkeys and 4 chimpanzees. Gametocytes in 13 Aotus monkeys and 4 chimpanzees were infectious to mosquitoes. Infection rates were markedly higher in mosquitoes fed on chimpanzees. PCR studies on 10 monkeys injected with sporozoites revealed the presence of parasites before their detection by microscopic examination. The India VII strain of P. vivax develops in Aotus and Saimiri monkeys and chimpanzees following the injection of parasitized erythrocytes, or sporozoites, or both. The transmission rate via sporozoites to New World monkeys of approximately 50% may be too low for the testing of sporozoite vaccines or drugs directed against the exoerythrocytic stages. However, the strain is highly infectious to commonly available laboratory-maintained anopheline mosquitoes. Mosquito infection is especially high when feedings are made with gametocytes from splenectomized chimpanzees.     

Hypometabolism in Aotus trivirgatus (Primates, Plathyrhini, Cebidae)]

The standard metabolism of Aotus trivirgatus (Night monkey, Owl monkey) is 22.5 to 46.2 per cent below Kleiber's prevision curve for mammals, which applies to other cebid monkeys like Saimiri sciureus and Alouatta. However the metabolic rate of Aotus is not reduced to the extent found in two hypometabolic prosimians Perodicticus potto and Nycticebus coucang. The low metabolism in Aotus is associated with a normal body temperature and a thick fur of high insulating power. These results are discussed.     

Chromosomal distribution of interstitial telomeric sequences in nine neotropical primates (Platyrrhini): possible implications in evolution and phylogeny

To localize interstitial telomeric sequences (ITSs) and to test whether their pattern of distribution could be linked to chromosomal evolution, we hybridized telomeric sequence probes (peptide nucleic acid, PNA) on metaphases of New World monkeys: Callithrix argentata, Callithrix jacchus, Cebuella pygmaea, Saguinus oedipus, Saimiri sciureus, Aotus lemurinus griseimembra, Aotus nancymaae (Cebidae), Lagothrix lagotricha (Atelidae) and Callicebus moloch (Pithecidae), characterized by a rapid radiation and a high rate of chromosomal rearrangements. Our analysis of the probe signal localization allowed us to show in all the species analysed, as normally, the telomeric location at the terminal ends of chromosomes and unexpected signal distributions in some species. Indeed, in three species among the nine studied, Aotus lemurinus griseimembra, Aotus nancymaae (Cebidae) and Lagothrix lagotricha (Atelidae), we showed a high variability in terms of localization and degree of amplification of interstitial telomeric sequences, especially for the ones found at centromeric or pericentromeric positions (het‐ITS). A comparative analysis, between species, of homologous chromosomes to human syntenies, on which we have found positive interspersed PNA signals, allowed us to explain the observed pattern of ITS distribution as results of chromosomal rearrangements in the neotropical primates analysed. This evidence permitted us to discuss the possible implication of ITSs as phylogenetic markers for closely related species. Moreover, reviewing previous literature data of ITSs distribution in Primates and in the light of our results, we suggest an underestimation of ITSs and highlight the importance of the molecular cytogenetics approach in characterizing ITSs, which role is still not clarified.     

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.