Owl Monkeys Research Articles

Owl Monkey Alu Insertion Polymorphisms and Aotus Phylogenetics.

Owl monkeys (genus Aotus), or "night monkeys" are platyrrhine primates in the Aotidae family. Early taxonomy only recognized one species, Aotus trivirgatus, until 1983, when Hershkovitz proposed nine unique species designations, classified into red-necked and gray-necked species groups based predominately on pelage coloration. Recent studies questioned this conventional separation of the genus and proposed designations based on the geographical location of wild populations. Alu retrotransposons are a class of mobile element insertion (MEI) widely used to study primate phylogenetics. A scaffold-level genome assembly for one Aotus species, Aotus nancymaae [Anan_2.0], facilitated large-scale ascertainment of nearly 2000 young lineage-specific Alu insertions. This study provides candidate oligonucleotides for locus-specific PCR assays for over 1350 of these elements. For 314 Alu elements across four taxa with multiple specimens, PCR analyses identified 159 insertion polymorphisms, including 21 grouping A. nancymaae and Aotus azarae (red-necked species) as sister taxa, with Aotus vociferans and A. trivirgatus (gray-necked) being more basal. DNA sequencing identified five novel Alu elements from three different taxa. The Alu datasets reported in this study will assist in species identification and provide a valuable resource for Aotus phylogenetics, population genetics and conservation strategies when applied to wild populations.

Arthropofauna consumed by the Andean night monkey (Aotus lemurinus) in a forest fragment at the Cordillera Central Colombia

Los artrópodos son alimento importante para primates como los monos nocturnos (Aotus spp.) debido a que proveen proteínas y grasas fáciles de digerir. No obstante, el registro de su consumo ha sido subestimado por la naturaleza oportunista de su captura y por las dificultades en la identificación. Describimos el consumo de artrópodos por parte de un grupo del mono nocturno andino en un bosque fragmentado de Colombia. Entre marzo y junio de 2016, recogimos muestras fecales a partir de seguimientos nocturnos y visitas al dormidero de un grupo de 4 individuos del mono nocturno andino (Aotus spp.). Preservamos las muestras en alcohol al 96 % y posteriormente las visualizamos a partir de un estereoscopio. Se inspeccionaron las heces en búsqueda de fragmentos de artrópodos que posteriormente fueron determinados a nivel taxonómico de orden y familia. En 12 de las 15 heces analizadas encontramos 48 fragmentos de artrópodos, de los cuales se clasificaron 38 a nivel de orden y 16 a nivel de familia. En total, identificamos 7 órdenes de artrópodos (6 insectos y 1 arácnido) y 9 familias de insectos (5 Coleoptera, 3 Hemiptera y 1 Hymenopera). Los órdenes con mayor cantidad de fragmentos en las heces fueron Coleoptera (21), Hemiptera (5) y Orthoptera (5) y las familias más frecuentes fueron Elateridae y Curculionidae con 5 y 4 fragmentos, respectivamente. Reportamos por primera vez el consumo del orden Isoptera, así como 2 nuevas familias de Hemiptera (i.e., Coreidae and Pentatomidae) y 5 familias de Coleoptera (i.e., Chrysomelidae, Coccinellidae, Curculionidae, Elateridae y Staphylinidae) en la dieta de los monos nocturnos (Aotus spp.). La gran cantidad de fragmentos de escarabajos en las heces del mono nocturno andino podría ser debido a la composición quitinosa de sus exoesqueletos que los hace difícil de degradar. Este estudio aporta información novedosa sobre la variedad de artrópodos consumidos por el mono nocturno andino y recopila toda la información sobre el consumo de este ítem para todo el género.

Cebidae Alu Element Alignments and a Complex Non-Human Primate Radiation.

Simple SummaryRelationships among the small monkeys living in the Americas such as the squirrel monkeys, owl monkeys (the ‘night monkeys’), marmosets and capuchins (the ‘organ grinder’ monkeys) are still under debate. This study utilized multi-species DNA sequence alignments to investigate these relationships. Each alignment contained a unique Alu element insertion, a genetic marker considered ‘identical by descent’ such that the absence of the Alu element is the ancestral state. Alu element diversity reveals that the emergence and radiation of these different primate lineages was rapid and complex. The close relationship between squirrel monkey and capuchins was confirmed while the placement of owl monkey with respect to the marmoset remains unresolved. The results of this study will assist in research and conservation strategies for America’s monkeys.Phylogenetic relationships among Cebidae species of platyrrhine primates are presently under debate. Studies prior to whole genome sequence (WGS) availability utilizing unidirectional Alu repeats linked Callithrix and Saguinus as sister taxa, based on a limited number of genetic markers and specimens, while the relative positions of Cebus, Saimiri and Aotus remained controversial. Multiple WGS allowed computational detection of Alu-genome junctions, however random mutation and evolutionary decay of these short-read segments prevented phylogenetic resolution. In this study, WGS for four Cebidae genomes of marmoset, squirrel monkey, owl monkey and capuchin were analyzed for full-length Alu elements and each locus was compared to the other three genomes in all possible combinations using orthologous region sequence alignments. Over 2000 candidates were aligned and subjected to visual inspection. Approximately 34% passed inspection and were considered shared in their respective category, 48% failed due to the target being present in all four genomes, having N’s in the sequence or other sequence quality anomalies, and 18% were determined to represent near parallel insertions (NP). Wet bench locus specific PCR confirmed the presence of shared Alu insertions in all phylogenetically informative categories, providing evidence of extensive incomplete lineage sorting (ILS) and an abundance of Alu proliferation during the complex radiation of Cebidae taxa.

Asymmetric dimethyl arginine in captive owl monkeys(Aotussp).

Only four of 40 animals had measurable asymmetric dimethyl arginine (ADMA) levels. The young primate had the lowest value (53.4ng/ml) when compared with the two adults (218.8 ± 9.3ng/ml) and the elderly one (320.5ng/ml). The ADMA levels in this study may relate to the echocardiographic abnormalities found, and possible hypertensive individuals.

Variation in population density of the Andean night monkey (Aotus lemurinus) in areas with different landscape characteristics

In the Colombian Andes, most of the populations of Andean night monkeys (Aotus lemurinus) are found in fragmented landscapes due to the predominant changes in land use in the region. Thus, forest fragments differ in shape, size, degree of isolation, and availability of resources. These factors have had a differential effect on the ecology and permanence of their populations. In order to determine the effect of fragmentation on A. lemurinus, we estimated its population density in a protected area of 489 ha of sub-Andean forest - at Otún Quimbaya Wildlife Sanctuary- which is structurally connected with other protected areas; then, we compared it with another study carried out in the unprotected Sub-andean forest fragments (900 ha) of Dapa, at the Valle del Cauca department. To estimate its density, the distance sampling method was used with 31 linear transects, and the data were analyzed with the software Distance. Landscape metrics was estimate with patch analyses tools with a Corine Land Cover information 1:100,000 scale. The plant structure and diversity were measurement with transects to 50 x 4 m and taking account the trees with diameter at breast height over 10 cm. We use average comparison to evaluate the similarities between patrons of the population density and explanatory variables. A population density of 39 ind/km2 was found in our study, which is lower than the 113 ind/km2 found in the Dapa. This relation was similar to relations of mean shape index, mean patch size and mean diameter at breast height, and inverse with the relations of proportion of the forest in the area, weighted cover index, plant diversity and density of trees. It is likely that the protected area, by being connected and having a greater diversity of primates and trees, allows this population not to suffer from a crowding phenomenon, and that the population does not increase it carrying capacity due to the low presence of competing species, conversely to what could be occurring in the unprotected fragments. Conversely, high density in Dapa could be reflect a system depletion in diversity and ecological processes.

Observations on the diet of Aotus nigriceps (Primates: Cebidae) in an urban and peri-urban area in Rondônia state, Brazil

The black-headed night monkey (Aotus nigriceps) is a predominantly frugivorous nocturnal neotropical primate. As such, records of different dietary items are fundamental. In the present study, we describe the first record of the consumption of Calliandra brevipes inflorescence in the peri-urban, and Cocos nucifera inflorescence, Eugenia uniflora fruits, and arthropods in the urban, region of the city of Porto Velho, in the southwestern Brazilian Amazon

Lipid profile, apolipoproteins A-1 and B in owl monkeys (Aotus infulatus) in captivity.

Owl monkeys (Aotus infulatus) are frequently affected by heart diseases and, as in humans, dyslipidemia is one of the predisposing factors for adverse cardiovascular events. In view of this, the study of the lipid profile and plasma apolipoproteins can contribute to the clinical management of this neotropical primate species. Lipid profile as well as A-1 and B apolipoprotein values were analyzed in 60 owl monkeys, studying their relationship with body biometry and the presence of cardiac alterations. Animals suspected of having heart disease did not show significant differences (p < .05) in terms of biometry or in relation to lipid profile and apolipoproteins A-1 and B values; however, higher values of LDL and ApoB and ApoB/ApoA-1 were observed in this group. This study is the first to describe the lipid profile and apolipoprotein values in owl monkeys, and further work will be needed to better elucidate the worthiness of LDL, ApoB, and the ApoB/ApoA-1 ratio in this primate species.

SM-COLSARSPROT: Highly Immunogenic Supramutational Synthetic Peptides Covering the World's Population.

Fifty ~20–amino acid (aa)–long peptides were selected from functionally relevant SARS-CoV-2 S, M, and E proteins for trial B-21 and another 53 common ones, plus some new ones derived from the virus’ main genetic variants for complementary trial C-21. Peptide selection was based on tremendous SARS-CoV-2 genetic variability for analysing them concerning vast human immunogenetic polymorphism for developing the first supramutational, Colombian SARS-protection (SM-COLSARSPROT), peptide mixture. Specific physicochemical rules were followed, i.e., aa predilection for polyproline type II left-handed (PPIIL) formation, replacing β-branched, aromatic aa, short-chain backbone H-bond-forming residues, π-π interactions (n→π* and π-CH), aa interaction with π systems, and molecular fragments able to interact with them, disrupting PPIIL propensity formation. All these modified structures had PPIIL formation propensity to enable target peptide interaction with human leukocyte antigen-DRβ1* (HLA-DRβ1*) molecules to mediate antigen presentation and induce an appropriate immune response. Such modified peptides were designed for human use; however, they induced high antibody titres against S, M, and E parental mutant peptides and neutralising antibodies when suitably modified and chemically synthesised for immunising 61 major histocompatibility complex class II (MHCII) DNA genotyped Aotus monkeys (matched with their corresponding HLA-DRβ1* molecules), predicted to cover 77.5% to 83.1% of the world’s population. Such chemically synthesised peptide mixture represents an extremely pure, stable, reliable, and cheap vaccine for COVID-19 pandemic control, providing a new approach for a logical, rational, and soundly established methodology for other vaccine development.

Comparison of PvLAP5 and Pvs25 qRT-PCR assays for the detection of Plasmodium vivax gametocytes in field samples preserved at ambient temperature from remote malaria endemic regions of Panama.

BackgroundAs the elimination of malaria in Mesoamerica progresses, detection of Plasmodium vivax using light microscopy (LM) becomes more difficult. Highly sensitive molecular tools have been developed to help determine the hidden reservoir of malaria transmission in low transmission settings. In this study we compare the performance of PvLAP5 and Pvs25 qRT-PCR assays to LM for the detection of Plasmodium vivax gametocytes in field samples preserved at ambient temperature from malaria endemic regions of Panama.MethodsFor this purpose, we collected a total of 83 malaria field samples during 2017-2020 preserved in RNAprotect (RNAp) of which 63 (76%) were confirmed P. vivax by LM and selected for further analysis. Additionally, 16 blood samples from local healthy malaria smear negative volunteers, as well as, from 15 malaria naïve lab-bred Aotus monkeys were used as controls. To optimize the assays, we first determined the minimum blood volume sufficient for detection of PvLAP5 and Pv18SrRNA using P. vivax infected Aotus blood that was preserved in RNAp and kept either at ambient temperature for up to 8 days before freezing or was snap-frozen at -80° Celsius at the time of bleeding. We then compared the mean differences in gametocyte detection rates of both qRT-PCR assays to LM and performed a multivariate correlation analysis of study variables. Finally, we determined the sensitivity (Se) and specificity (Sp) of the assays at detecting gametocytes compared to LM.ResultsBlood volume optimization indicated that a blood volume of at least 60 μL was sufficient for detection of PvLAP5 and Pv18SrRNA and no significant differences were found between RNA storage conditions. Both PvLAP5 and Pvs25 qRT-PCR assays showed a 37-39% increase in gametocyte detection rate compared to LM respectively. Strong positive correlations were found between gametocytemia and parasitemia and both PvLAP5 and Pvs25 gametocyte markers. However, no significant differences were detected in the Se and Sp of the Pvs25 and PvLAP5 qRT-PCR assays, even though data from control samples suggested Pvs25 to be more abundant than PvLAP5.ConclusionsThis study shows that the PvLAP5 qRT-PCR assay is as Se and Sp as the gold standard Pvs25 assay and is at least 37% more sensitive than LM at detecting P. vivax gametocytes in field samples preserved in RNAp at ambient temperature from malaria endemic regions of Panama.Author summaryPlasmodium vivax is one of the five species of malaria (P. falciparum, P. malariae, P. ovale and P. knowlesi) that are transmitted to man by the bite of female anopheles mosquitoes. It causes ~14.3 million cases mainly in Southeast Asia, India, the Western Pacific and the Americas annually. In the Americas, malaria remains a major problem in underdeveloped areas and indigenous communities in the Amazon region and eastern Panama, where it is endemic and difficult to eliminate. As malaria elimination progresses, detection of P. vivax by light microscopy (LM) becomes more difficult. Therefore, highly sensitive molecular tools have been developed that use genetic markers for the parasite to help determine the hidden reservoir of malaria transmission. This study compares the performance of two molecular assays based on the genetic markers of mature gametocytes PvLAP5 and Pvs25 with LM. The study shows that the PvLAP5 qRT-PCR assay is as sensitive and specific as the gold standard Pvs25 assay and is at least 37% more sensitive than LM at detecting P. vivax gametocytes. These data suggest that the PvLAP5 qRT-PCR assay can be a useful tool to help determine the hidden reservoir of transmission in endemic foci approaching elimination.

First observation of a diurnal birth in wild owl monkeys (Aotus azarae), Formosa, Argentina

Notas sobre Mamíferos Sudamericanos es una revista de la Sociedad Argentina para el Estudio de los Mamíferos (SAREM). Publica información acotada donde se describen nuevas localidades de registro, datos sobre comportamiento y aspectos ecológicos de mamíferos neotropicales.

Pathways to paternal care in primates.

Natural selection will favor male care when males have limited alternative mating opportunities, can invest in their own offspring, and when care enhances males' fitness. These conditions are easiest to fulfill in pair-bonded species, but neither male care nor stable "breeding bonds" that facilitate it are limited to pair-bonded species. We review evidence of paternal care and extended breeding bonds in owl monkeys, baboons, Assamese macaques, mountain gorillas, and chimpanzees. The data, which span social/mating systems and ecologies, suggest that there are multiple pathways by which conditions conducive to male care can arise. This diversity highlights the difficulty of making inferences about the emergence of male care in early hominins based on single traits visible in the fossil record. We discuss what types of data are most needed and the questions yet to be answered about the evolution of male care and extended breeding bonds in the primate order.

Plasmodium falciparum in Aotus nancymaae: A New Model for Placental Malaria

Plasmodium falciparum (Pf)-infected erythrocytes that display the variant surface antigen VAR2CSA bind chondroitin sulfate A (CSA) to sequester in placental intervillous spaces, causing severe sequelae for mother and offspring. Here, we establish a placental malaria (PM) monkey model. Pregnant Aotus infected with CSA-binding Pf-CS2 parasites during 3rd trimester developed pronounced sequestration of late-stage parasites in placental intervillous spaces that express VAR2CSA and bind specifically to CSA. Similar to immune multigravid women, a monkey infected with Pf-CS2 parasites over successive pregnancies acquired antibodies against VAR2CSA, with potent functional activity that was boosted upon subsequent pregnancy infections. Aotus also developed functional antibodies after multiple acute PM episodes and subsequent VAR2CSA immunization. In summary, Pf infections in pregnant Aotus monkeys recapitulate all the prominent features of human PM infection and immunity, and this model can be useful for basic mechanistic studies and preclinical studies to qualify candidate PM vaccines.

Out of the shadows: Multilocus systematics and biogeography of night monkeys suggest a Central Amazonian origin and a very recent widespread southeastward expansion in South America

Night monkeys (Aotus, Cebidae) are a widely distributed genus of Neotropical primates with a poorly understood taxonomy and biogeography. The number of species in the genus varies from one to nine, depending on the author, and there are at least 18 known karyotypes, varying from 2n = 46 to 2n = 58. Historically, night monkeys are divided into two species groups: red- and grey-necked groups from south and north of the Amazon-Solimões River, respectively. Here, we used 10 nuclear and 10 mitochondrial molecular markers from a wide taxonomic and geographic sample to infer phylogeny, divergence times, and biogeography of the genus. For phylogenetic reconstruction we used Maximum Likelihood (ML) and Bayesian Inferences (BI). Biogeographic models were generated using the ‘BioGeoBEARS’ software. We found support for nine taxa of Aotus and rejected the existence of monophyletic “red necked” and “grey necked” species groups. We suggest a taxonomic reclassification of the genus, which is better represented by two clades named northern group, which contains Aotus miconax, A. nancymae, A. trivirgatus, A. vociferans, A. lemurinus, A. griseimembra, A. zonalis, and A. brumbacki, and southern group, which contains A. nigriceps, A. boliviensis, A. infulatus, and A. azarae. The results suggest that the most recent common ancestor of all species of Aotus arose in the central Amazon basin in the Early Pliocene. The evolutionary history of night monkeys was guided by dispersal, vicariance and founder events. The end of the Andean uplift and the subsequent changes in the Amazon landscape, as well as the Amazon-Solimões and Tapajós rivers may have played an important role in the origin and diversification of Aotus, respectively. However, most of the Amazonian rivers seem not to have been geographical barriers to dispersal of night monkeys. The herein named southern group is fruit of a very recent diversification guided by dispersal, crossing the Tapajós, Xingú, Tocantins, and Guapore rivers and reaching the Cerrado in the last 1.6 My.

Thermoenergetic challenges and daytime behavioural patterns of a wild cathemeral mammal

The circadian thermoenergetics hypothesis (CTEH) suggests that endotherms benefit by being active during the warmer period of a 24 h cycle and by resting when temperatures drop, since this lowers energetic investment in thermoregulation. In accordance with the CTEH, cathemeral (i.e. active during both daytime and night-time) Azara's owl monkeys, Aotus azarae, of the Argentinean Chaco increase their daytime activity during the relatively cold winter compared to the summer. Still, it remains unclear whether these behavioural changes are explained by major shifts in energy balance. Thus, we sought to understand how thermal challenges influence the allocation of behaviours during the daytime that tend to conserve energy (resting), increase its availability (foraging) or expend it (travelling). We constructed a priori a set of linear models to evaluate the relationships between daytime behavioural patterns and photoperiod, moonlight, age, reproductive status and hourly, daily and weekly fluctuations in ambient temperatures, as well as some of their interactions. We analysed 4985 20-minute focal samples collected during 0600–2100 hours from 140 recognizable individuals from 15 groups across 13 years. Our results indicate that, from the warmest to the coldest months, daytime resting frequencies decreased by 31%, whereas daytime foraging frequencies increased by 131%, while travelling frequencies remained unchanged. Daytime activity patterns were explained by the interaction between weekly average temperatures and either lunar activity, age class or reproductive status. Generally, daytime activity increased as temperatures decreased seasonally, but this is effect was masked during full moons; and infants, juveniles, subadults and solitary adults used the daytime differently. Finally, travelling and foraging increased during longer days or at times of daily maximum temperatures but decreased when these two factors interacted (i.e. long summer days at daily maximum temperatures). In summary, daytime behaviours of A. azarae may be structured by thermoenergetic investment, as predicted by the CTEH.

Using a Phylogenetic Framework to Assess the Role of Fruit Size in Food Selection by the Andean Night Monkey (Aotus lemurinus)

Using a Phylogenetic Framework to Assess the Role of Fruit Size in Food Selection by the Andean Night Monkey (Aotus lemurinus)

Nonhuman Primate Paternal Care: Species and Individual Differences in Behavior and Mechanisms.

Direct care of offspring by the father (sire) is relatively rare in primates. Besides humans, there are a number of species where the male is essential for the survival of offspring: marmosets, tamarins, titis and owl monkeys, some lemurs, and siamangs. All these species show reduced sexual dimorphism, territoriality, and biparental care. However, timing and levels of direct care may vary among these species. Here, relying on both lab and field data, we address the variability found in father's involvement with his infants, the behavioral, neuroendocrine and sensory systems that are a cause and consequence of paternal care, and social bonds between the breeding pair. We integrate studies of laboratory animals (where detailed observations and experimentation are possible) with field studies (which illuminate the ecological and evolutionary functions of paternal care) and discuss the future directions for examining the proximate and ultimate mechanisms of paternal care in nonhuman primates.

Detection of early myocardial cell death in owl monkeys (Aotus nancymai) using complement component C9 immunohistochemistry in formalin-fixed paraffin-embedded heart tissues: A retrospective study.

Owl monkeys are commonly used in biomedical research which is affected by the high incidence of cardiomyopathy in this species. Occasionally, owl monkeys with no clinical signs of heart disease are found dead and at necropsy show no, or very mild, cardiomyopathy. A possible explanation for sudden death is acute myocardial infarction; however, early myocardial changes may be difficult to assess by conventional stains and light microscopy. Complement component C9 immunohistochemistry was performed in paraffin-embedded heart tissue samples from owl monkeys who died suddenly, or were euthanized due to sickness, to determine whether these animals suffered from acute myocardial infarcts. C9 deposits were found in the myocardium of 19 out of 20 (95%) animals. The findings in this study suggest owl monkeys suffer from acute myocardial infarcts, and complement component C9 immunohistochemistry may be a useful diagnostic tool.

Vascular, cardiac, and renal lesions attributed to primary systemic hypertension in western pygmy marmosets (Cebuella pygmaea).

In a retrospective study of a western pygmy marmoset (Cebuella pygmaea) colony, postmortem examination of 1/8 juvenile and 29/47 adult animals identified vascular, cardiac, and renal lesions consistent with systemic hypertension. This included frequent renal arteriolar hypertrophy, hyaline and proliferative arteriolosclerosis, fibrinoid necrosis of arterioles, glomerulosclerosis, and nephrosclerosis. Affected animals ranged from 0.6 to 12 years of age (mean 6 years) and had an observed male predominance. Genealogical relatedness was evident in several breeding pairs and spanned multiple generations. Concurrent cardiac and renal disease was commonly identified, although frequently subclinical, and both were important causes of morbidity and mortality in affected animals. Cardiomegaly and hypertrophy were typical features and were accompanied by left atrial thrombosis in 10 animals. Signs of heart failure included chronic pulmonary edema in 20 cases and body cavity effusions in 17. In the kidneys, 19 cases had glomerular disease and hypertensive vasculopathy, and 26 cases had nephrosclerosis or glomerulosclerosis. Common extrarenal secondary causes of hypertension were excluded by necropsy examination. The pathogenesis is suggested to involve primary hypertension leading to renal and cardiac disease. Elevated sympathetic activity might be an underlying factor in the frequent development of primary systemic hypertension in the pygmy marmoset, as for the owl monkey.

Occurrence and clinical significance of abnormal liver findings by ultrasound in captive owl monkeys.

Imaging diagnostic methods are essential for a complete understanding of the liver function and may aid in early detection of hepatic disorders. Sixty-nine owl monkeys were grouped in three age groups (AG): AG1 (<2years old, n=14), 2 (2-6years old, n=21), and 3 (>7years old, n=34). The animals were evaluated by ultrasound, liver function tests, and hemogram. The ultrasound revealed abnormal findings in the parenchyma ("starry sky" and steatosis) and/or in the gallbladder (cholelithiasis, septum, and wall edema) in 17 individuals, with higher incidence in AG3 individuals. Seven hepatic individuals showed alterations in the blood tests. Our study reported the occurrence of abnormal liver findings by ultrasound in owl monkeys and their associated clinical analyses. We recommend the regular use of ultrasound to evaluate liver condition in owl monkeys, particularly in old individuals.

Night on Earth

Night on Earth