Owl Monkeys Research Articles

The social and defensive function of olfactory behaviors in a pair-living sexually monogamous primate.

Olfactory behaviors serve a wide variety of social functions in mammals. Odor may signal information about attributes of individuals important for mating and reproduction. Olfactory behaviors, such as scent-marking, may also function as part of home range or resource defense strategies. We assessed the potential social and home range defense functions of olfactory behavior in a pair-living and sexually monogamous primate, Azara's owl monkey (Aotus azarae), in the Argentinian Chaco. This is the most extensive investigation of owl monkey olfactory behaviors in the wild. Individuals regularly performed olfactory behaviors (group mean + SD = 1.3 + 0.5 per hour). The patterns were generally comparable to those observed in studies of captive owl monkeys, except that urine washing was the most common behavior in the wild, as opposed to scent-marking and genital inspections. Most olfactory behaviors were performed by adults, and there were striking sex differences in genital inspections: almost all consisted of an adult male inspecting the paired adult female. These findings suggest that olfactory behaviors play an important role in signaling and coordinating reproduction among owl monkeys, particularly during periods of female conception and pregnancy. Additionally, our research indicates that these behaviors may also serve as a defense strategy for maintaining the core area of their home ranges. This study offers the first assessment of the role of olfactory behaviors in reproductive contexts and home range defense in pair-living, monogamous platyrrhine primates.

Anointing behavior with millipedes by a wild group of Caribbean night monkeys (Aotus griseimembra) in Colombia

Anointing behavior with millipedes by a wild group of Caribbean night monkeys (Aotus griseimembra) in Colombia

Inbreeding avoidance, competition and natal dispersal in a pair-living, genetically monogamous mammal, Azara's owl monkey (Aotus azarae).

Natal dispersal is an important life-history stage influencing individual fitness, social dynamics of groups and population structure. Understanding factors influencing dispersal is essential for evaluating explanations for the evolution and maintenance of social organization, including parental care and mating systems. The social and mating systems of Azara's owl monkeys (Aotus azarae) are infrequent among mammals; these primates are pair-living, serially and genetically monogamous and both sexes directly care for offspring. To evaluate the role that competition and inbreeding avoidance play in shaping dispersal patterns, we used 25 years of demographic and genetic data to examine how variation in timing of natal dispersal is related to social (adult replacements, step-parents, births and group size) and ecological factors (seasonal abundance of resources) in a wild population of A. azarae in Formosa, Argentina. We found that all males and females dispersed from their natal groups, but subadults delayed dispersal when a step-parent of the opposite sex joined the group, indicating that they may perceive these step-parents as potential mates. Dispersal was more probable when resource conditions were better, regardless of age. Overall, agonistic conflict over food and potential mates with adults in the natal group, as well as inbreeding avoidance, contribute to regulating dispersal.

Correction: Owl monkeys: biology, adaptive radiation, and behavioral ecology of the only nocturnal primate in the Americas, edited by Eduardo Fernandez-Duque

Correction: Owl monkeys: biology, adaptive radiation, and behavioral ecology of the only nocturnal primate in the Americas, edited by Eduardo Fernandez-Duque

The human malaria-Aotus monkey model: a historical perspective in antimalarial chemotherapy research at the Gorgas Memorial Laboratory-Panama.

The human malaria-Aotus monkey model has served the malaria research community since its inception in 1966 at the Gorgas Memorial Laboratory (GML) in Panama. Spanning over five decades, this model has been instrumental in evaluating the in vivo efficacy and pharmacokinetics of a wide array of candidate antimalarial drugs, whether used singly or in combination. The animal model could be infected with drug-resistant and susceptible Plasmodium falciparum and Plasmodium vivax strains that follow a characteristic and reproducible course of infection, remarkably like human untreated and treated infections. Over the years, the model has enabled the evaluation of several synthetic and semisynthetic endoperoxides, for instance, artelinic acid, artesunate, artemether, arteether, and artemisone. These compounds have been evaluated alone and in combination with long-acting partner drugs, commonly referred to as artemisinin-based combination therapies, which are recommended as first-line treatment against uncomplicated malaria. Further, the model has also supported the evaluation of the primaquine analog tafenoquine against blood stages of P. vivax, contributing to its progression to clinical trials and eventual approval. Besides, the P. falciparum/Aotus model at GML has also played a pivotal role in exploring the biology, immunology, and pathogenesis of malaria and in the characterization of drug-resistant P. falciparum and P. vivax strains. This minireview offers a historical overview of the most significant contributions made by the Panamanian owl monkey (Aotus lemurinus lemurinus) to malaria chemotherapy research.

Owl Monkeys: Biology, Adaptive Radiation, and Behavioral Ecology of the Only Nocturnal Primate in the Americas, edited by Eduardo Fernandez-Duque

Owl Monkeys: Biology, Adaptive Radiation, and Behavioral Ecology of the Only Nocturnal Primate in the Americas, edited by Eduardo Fernandez-Duque

Structurally divergent and recurrently mutated regions of primate genomes

We sequenced and assembled using multiple long-read sequencing technologies the genomes of chimpanzee, bonobo, gorilla, orangutan, gibbon, macaque, owl monkey, and marmoset. We identified 1,338,997 lineage-specific fixed structural variants (SVs) disrupting 1,561 protein-coding genes and 136,932 regulatory elements, including the most complete set of human-specific fixed differences. We estimate that 819.47 Mbp or ∼27% of the genome has been affected by SVs across primate evolution. We identify 1,607 structurally divergent regions wherein recurrent structural variation contributes to creating SV hotspots where genes are recurrently lost (e.g., CARD, C4, and OLAH gene families) and additional lineage-specific genes are generated (e.g., CKAP2, VPS36, ACBD7, and NEK5 paralogs), becoming targets of rapid chromosomal diversification and positive selection (e.g., RGPD gene family). High-fidelity long-read sequencing has made these dynamic regions of the genome accessible for sequence-level analyses within and between primate species.

Scientific activism to protect the world's primates and their environments from extinction: Introduction to the special issue.

Nonhuman primates and their habitats are facing an impending extinction crisis. Approximately 69% of primate species are listed by the International Union for Conservation of Nature as threatened and 93% have declining populations. Human population growth (expected to reach 10.9 billion by the year 2100), the unsustainable demands of a small number of consumer nations for forest-risk commodities, deforestation and habitat conversion, the expansion of roads and rail networks, cattle ranching, the hunting and trapping of wild primate populations, and the potential spread of infectious diseases are among the primary drivers of primate population decline. Climate change will only exacerbate the current situation. The time to act to protect primate populations is now! In this special issue of the American Journal of Primatology, we present a series of commentaries, formulated as "Action Letters."These are designed to educate and inform primatologists, conservation biologists, wildlife ecologists, political leaders, and global citizens about the conservation challenges faced by particular primate taxa and particular world regions, and present examples of specific actions that one can take, individually and collectively, to promote the persistence of wild primate populations and environmental justice for local human populations and impacted ecological communities. As scientists, researchers, and educators, primatologists are in a unique position to lead local, national, and international efforts to protect biodiversity. In this special issue, we focus on primates of the Brazilian Amazon, lemurs of northeast Madagascar, Temminck's red colobus monkey (Piliocolobus badius temminckii), night monkeys (Aotus spp.), long-tailed macaques (Macaca fascicularis), the primate pet trade, and professional capacity building to foster conservation awareness and action. We encourage primatologists, regardless of their research focus, to engage in both advocacy and activism to protect wild primate populations worldwide.

Sterile protection against P. vivax malaria by repeated blood stage infection in the Aotus monkey model.

The malaria parasite Plasmodium vivax remains a major global public health challenge, and no vaccine is approved for use in humans. Here, we assessed whether P. vivax strain-transcendent immunity can be achieved by repeated infection in Aotus monkeys. Sterile immunity was achieved after two homologous infections, whereas subsequent heterologous challenge provided only partial protection. IgG levels based on P. vivax lysate ELISA and protein microarray increased with repeated infections and correlated with the level of homologous protection. Parasite transcriptional profiles provided no evidence of major antigenic switching upon homologous or heterologous challenge. However, we observed significant sequence diversity and transcriptional differences in the P. vivax core gene repertoire between the two strains used in the study, suggesting that partial protection upon heterologous challenge is due to molecular differences between strains rather than immune evasion by antigenic switching. Our study demonstrates that sterile immunity against P. vivax can be achieved by repeated homologous blood stage infection in Aotus monkeys, thus providing a benchmark to test the efficacy of candidate blood stage P. vivax malaria vaccines.

Molecular data aids pinworm diagnosis in night monkeys (Aotus spp., Primates: Aotidae) with the resurrection of a Trypanoxyuris species (Nematoda: Oxyuridae)

Neotropical primates (Platyrrhines) are commonly parasitized by pinworm nematodes of the genus Trypanoxyuris Vevers, 1923. The taxonomic identity of Trypanoxyuris sampled in night monkeys (Aotus Iliger) has been rather controversial. Two species have been described, namely T. microon (Linstow, 1907) and T. interlabiata (Sandosham, 1950). The latter was synonymized with T. microon considering that the observed morphological differences corresponded to different developmental stages of the nematode rather than to differences between both species. Here, we used an integrative taxonomy approach, based on morphological and molecular data along with host identity, in order to assess the validity of both species. Our results evidenced that these different morphotypes correspond to different and reciprocally monophyletic groups; thus, we propose the resurrection of T. interlabiata. We redescribe both pinworm species using specimens sampled in Aotus monkeys from Colombia and discuss the advantages of combining molecular and morphological data to uncover pinworm diversity, and to understand the potential forces determining the diversification process in pinworms from platyrrhine primates.

Fruit Consumption by the Endemic Brumback Night Monkey (Aotus brumbacki, Primates, Aotidae) in forest fragments of Colombian Llanos

Aotus brumbacki is a nocturnal primate endemic to the Llanos of Colombia. This is the first report of species consumed by A. brumbacki in forest fragments in the municipalities of San Martín and Cumaral. The observations were made during a study on vocalizations and density. The families consumed by A. brumbacki in fragmented zones that are also consumed in continuous zones are Anacardiacea, Arecaceae, Burseraceae, Melastomataceae, Moraceae and Myrtaceae, with some species in common: Socratea exhorriza, Crepidospermum rhoifolium and Pseudolmedia laevis. Five species of plants for human use were consumed by A. brumbacki, this consumption may be related to its use in crops and near houses, where the primate is often observed by people. This list can be used in restoration plans and to connect forest fragments where the species still persists.

Aotus nancymaae model predicts human immune response to the placental malaria vaccine candidate VAR2CSA

Placental malaria vaccines (PMVs) are being developed to prevent severe sequelae of placental malaria (PM) in pregnant women and their offspring. The leading candidate vaccine antigen VAR2CSA mediates parasite binding to placental receptor chondroitin sulfate A (CSA). Despite promising results in small animal studies, recent human trials of the first two PMV candidates (PAMVAC and PRIMVAC) generated limited cross-reactivity and cross-inhibitory activity to heterologous parasites. Here we immunized Aotus nancymaae monkeys with three PMV candidates (PAMVAC, PRIMVAC and ID1-ID2a_M1010) adjuvanted with Alhydrogel, and exploited the model to investigate boosting of functional vaccine responses during PM episodes as well as with nanoparticle antigens. PMV candidates induced high levels of antigen-specific IgG with significant cross-reactivity across PMV antigens by enzyme-linked immunosorbent assay. Conversely, PMV antibodies recognized native VAR2CSA and blocked CSA adhesion of only homologous parasites and not of heterologous parasites. PM episodes did not significantly boost VAR2CSA antibody levels or serum functional activity; nanoparticle and monomer antigens alike boosted serum reactivity but not functional activities. Overall, PMV candidates induced functional antibodies with limited heterologous activity in Aotus monkeys, similar to responses reported in humans. The Aotus model appears suitable for preclinical downselection of PMV candidates and assessment of antibody boosting by PM episodes.

Gastrointestinal tract pathology of the owl monkey (Aotus spp.).

Owl monkeys are small nocturnal new world primates in the genus Aotus that are most used in biomedical research for malaria. Cardiomyopathy and nephropathy are well-described common diseases contributing to their morbidity and mortality; less is known about lesions affecting the gastrointestinal tract. Records from a 14-year period (2008-2022) at the Keeling Center for Comparative Medicine and Research were queried to identify instances of spontaneous gastrointestinal disease that directly contributed to the cause of death from the 235 adult owl monkeys submitted for necropsy. Of the 235, 10.6% (25/235) had gastrointestinal disease listed as a significant factor that contributed to morbidity and mortality. Diagnoses included candidiasis (3/25), gastric bloat (4/25), and intestinal incarceration and ischemia secondary (11/25), which included intussusception (4/25), mesenteric rent (3/25), strangulating lipoma (2/25), intestinal torsion (1/25), and an inguinal hernia (1/25). Intestinal adenocarcinomas affecting the jejunum (4/25) were the most common neoplasia diagnosis. Oral squamous cell carcinoma (1/25) and intestinal lymphoma (2/25) were also diagnosed. This report provides evidence of spontaneous lesions in the species that contribute to morbidity and mortality.

The importance of auditory, olfactory, and visual cues for insect foraging in owl monkeys (Aotus nancymaae).

Nocturnal mammals have unique sensory adaptations to facilitate foraging at night. Owl monkeys (Aotus spp.) are pair-living nocturnal platyrrhines adept at capturing insect prey under low-light conditions. Owl monkeys use acoustic and chemical cues in intraspecific communication and use olfaction to detect fruit as they forage. We conducted an experiment to determine which cues (auditory, olfactory, and visual) Aotus nancymaae rely upon when foraging for insects. We scored the behavior of 23 captive owl monkeys during a series of trials in which monkeys were provided sensory boxes with insect cues either present (experimental box) or absent (control box). Each cue was tested alone and in combination with all other cues (multimodal cues). We used generalized linear mixed models to determine which cues elicited the greatest behavioral response. Owl monkeys approached and spent more time near experimental boxes than control boxes. Male owl monkeys were quicker than their female partners to approach the sensory boxes, suggesting that males may be less neophobic than females. The owl monkeys exhibited behaviors associated with olfaction and foraging (e.g., sneezing, trilling) during trials with multimodal cues and when only olfactory cues were present. When only visual or auditory cues were present, owl monkeys exhibited fewer foraging-related behaviors. After approaching a sensory box, however, they often touched boxes containing visual cues. A. nancymaae may rely on olfactory cues at night to detect a food source from several meters away and then rely more on visual cues once they are closer to the food source. Their use of sensory cues during insect foraging differs from nocturnal strepsirrhines, possibly reflecting physiological constraints associated with phylogeny, given that owl monkeys evolved nocturnality secondarily from a more recent diurnal ancestor.

Vocal repertoire of wild Andean night monkeys (Aotus lemurinus) in an Andean forest in Colombia

Abstract Vocal communication is particularly important for nocturnal species as well as those living in dense forests, where visual abilities can be somewhat constrained. The Andean night monkey (Aotus lemurinus) is a nocturnal American primate living in mountain forests in the Northern Andes with scant information on its behavior and ecology. The main goal of this study is to describe the vocal repertoire of a group of wild Andean night monkeys and compare it with earlier bioacoustics studies on the only nocturnal platyrrhines. We recorded the vocal behavior of a group of night monkeys living in the eastern Andes of Colombia between August and December 2019. Based on an auditory and a visual inspection of the vocal records, and through a quantitative analysis of the acoustic parameters of the vocalizations, we were able to identify five different calls emitted by the Andean night monkey. Four of these calls are stereotyped while the fifth vocalization (Squeak) is more variable, having different forms. Additionally, one call (Acetate) was found to be unique to this species. The result of this study contributes to the scant information on the ecology and behavior of the Andean night monkey and sets baseline information on the vocal behavior of night monkeys that may be used in future studies on communication of these and other nocturnal primates.

A call-to-action to assist in efforts to protect owl monkeys (Aotus spp.).

The majority of the 11 species of owl monkeys (Aotus spp.) have declining populationsor are listed as data deficient. Deforestation due to agriculture, development, or logging poses threats to owl monkeys throughout their range. In some areas, Aotus are hunted for bushmeat or trapped for the wildlife trade. In Colombia, the country with the greatest number of Aotus species, owl monkeys are also threatened by civil unrest. To help combat these challenges, nonprofit organizations and field researchers in habitat countries have successfully implemented a variety of conservation projects such as censusing and monitoring owl monkey populations, establishing protected areas, reforesting degraded areas, filing lawsuits to protect wild populations, helping law enforcement with environmental regulation, and promoting environmental education. We highlight some of the conservation successes and suggest actions people around the world can take to contribute to these important efforts.

Cuterebra baeri Infecting Grey-Legged Night Monkeys (Aotus griseimembra) and Red Howler Monkeys (Alouatta seniculus) in Colombia.

Myiases are parasitic infections caused by the larval stages of some fly species. In American nonhuman primates (NHP), three bot fly species causing cutaneous myiasis have been reported: Cuterebra baeri, Cochliomyia hominivorax, and Dermatobia hominis. Studies on myiasis in NHP are scarce and mainly based on morphologic identification of larvae, while molecular approaches have been barely used. This study aimed to molecularly identify bot flies parasitizing two NHP species living sympatrically in central Colombia. Bot fly larvae were collected from two grey-legged night monkeys (Aotus griseimembra) and from a howler monkey (Alouatta seniculus). Larvae were measured and photographed for morphologic evaluation; subsequent molecular characterizations of a partial region of the cytochrome c oxidase subunit 1 mitochondrial gene were performed. Sequence analysis allowed the identification of all specimens as Cuterebra baeri, enabling confirmation of this species parasitizing Alouatta seniculus and Aotus griseimembra in Colombia.

Growth and microanatomy of the paranasal sinuses in two species of New World monkeys

Paranasal sinuses of living apes and humans grow with positive allometry, suggesting a novel mechanism for bone enlargement. Here, we examine the paranasal sinuses of the owl monkey (Aotus spp.) and a tamarin (Saguinus midas) across postnatal development. The prediction that paranasal sinuses grow disproportionately faster than the main nasal chamber is tested. We used diffusible iodine-based contrast-enhanced computed tomography and histology to study sinuses in eight Aotus and three tamarins ranging from newborn to adult ages. Sinuses were segmented at the mucosa-air cavity interface and measured in volume. All sinuses were lined by a ciliated respiratory epithelium, except for the ethmoid air cells in Aotus, which are lined in part by olfactory epithelium. An age comparison indicates that only the maxillary sinus and ethmoid air cells are present in newborns, and two additional sinuses (invading the orbitosphenoid and the frontal bone), do not appear until late infancy or later. Comparing newborns and adults, the main nasal airway is 10 times larger in the adult Aotus and ~ 6.5 times larger in adult Saguinus. In contrast, the maxillary sinus far exceeds this magnitude of difference: 24 times larger in the adult Aotus and 46 times larger in adult Saguinus. The frontal sinuses add significantly to total paranasal space volume in both species, but this growth is likely delayed until juvenile age. Results suggest ethmoid air cells expand the least. These results support our prediction that most paranasal sinuses have a distinctly higher growth rate compared to the main nasal chamber.

Cortical adaptation of the night monkey to a nocturnal niche environment: a comparative non-invasive T1w/T2w myelin study

Night monkeys (Aotus) are the only genus of monkeys within the Simian lineage that successfully occupy a nocturnal environmental niche. Their behavior is supported by their sensory organs’ distinctive morphological features; however, little is known about their evolutionary adaptations in sensory regions of the cerebral cortex. Here, we investigate this question by exploring the cortical organization of night monkeys using high-resolution in-vivo brain MRI and comparative cortical-surface T1w/T2w myeloarchitectonic mapping. Our results show that the night monkey cerebral cortex has a qualitatively similar but quantitatively different pattern of cortical myelin compared to the diurnal macaque and marmoset monkeys. T1w/T2w myelin and its gradient allowed us to parcellate high myelin areas, including the middle temporal complex (MT +) and auditory cortex, and a low-myelin area, Brodmann area 7 (BA7) in the three species, despite species differences in cortical convolutions. Relative to the total cortical-surface area, those of MT + and the auditory cortex are significantly larger in night monkeys than diurnal monkeys, whereas area BA7 occupies a similar fraction of the cortical sheet in all three species. We propose that the selective expansion of sensory areas dedicated to visual motion and auditory processing in night monkeys may reflect cortical adaptations to a nocturnal environment.

Prioritizing Areas for Primate Conservation in Argentina

Argentina lies within the southernmost distributional range of five neotropical primates, the brown howler monkey Alouatta guariba, the black-and-gold howler monkey Alouatta caraya, the black-horned capuchin Sapajus nigritus, the Azara’s capuchin Sapajus cay, and the Azara’s owl monkey Aotus azarae; the first three of which are globally threatened. These species occupy different ecoregions: the Alto Paraná Atlantic forest, the Araucaria moist forest, the humid Chaco, the Southern Cone Mesopotamian savanna, the Paraná Ffooded savanna, and the Southern Andean Yungas. The recently approved National Primate Conservation Plan of Argentina calls for identifying priority areas to focus conservation actions for these species. We used species distribution models to estimate species ranges and then used the Zonation software to perform a spatial conservation prioritization analysis based on primate habitat quality and connectivity to identify potential areas of importance at national and ecoregional levels. Only 7.2% (19,500 km2) of the area inhabited by primates in Argentina is under protection. Outside the current protected areas, the top-ranked 1% and 5% priority areas identified in our analysis covered 1894 and 7574 km2, respectively. The top 1% areas were in the Atlantic forest of Misiones province, where S. nigritus, A. guariba, and A. caraya are distributed, and in the humid portion of eastern Chaco and Formosa provinces, where A. azarae and A. caraya are present. The top 5% areas included portions of the Yungas, where S. cay is the only primate present. Priority areas in Chaco and Formosa provinces are particularly relevant because of the paucity of protected areas and the high deforestation rate. The endangered A. guariba population will benefit from the better protection of the priority areas of Misiones. The potential priority areas proposed herein, considered within a context of a broad participatory process involving relevant stakeholders and local people, will help guide new and innovative conservation policies and practices while supporting management objectives.