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 populations or 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.

Intergroup encounters in pair-living primates: Comparative analysis and a case study of pair-living and monogamous owl monkeys (Aotus azarae) of Argentina.

The function of intergroup encounters (IGEs) may differ substantially among species of different group sizes and social organizations. Research in group-living primates has shown that the behavioral responses during IGEs can vary widely from affiliative to neutral or aggressive interactions; still, little is known about IGEs in pair-living taxa. We conducted a systematic literature review to find relevant studies on the functions of IGEs in pair-living nonhuman primates that could inform analyses of IGE data (n = 242 IGEs, 21 groups and 10 solitary individuals, 1997-2020) from wild owl monkeys, a pair-living, monogamous primate with extensive biparental care. We identified 1315 studies published between 1965 and 2021; only 13 of them (n = 10 species) contained raw data on the number of IGEs. Our review of those studies showed that IGEs are common, but highly variable in their nature and characteristics in pair-living primates. To examine the non-mutually exclusive hypotheses of resource-, and mate defense, and infanticide avoidance we analyzed data from the Owl Monkey Project 27-year long database to build first an a priori model set. To incorporate prior knowledge from the literature review, we conducted our analyses as a consecutive series of binomial logistic regressions. All IGEs including all biologically relevant parameters (N = 156) were codified into three different behavioral categories (Reaction, Agonism, and Physical Aggression). The analysis showed that owl monkeys regularly engaged in IGEs, most of which were agonistic. They showed more reaction when infants were present, but reactions were less physically aggressive when infants and pregnant females were involved. Overall, our results lend more support for the infant and mate defense hypotheses than they do for the resource defense one.

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.

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.

BACKGROUND: 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. METHODS: 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. RESULTS AND CONCLUSION: 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.

Associations between fecal cortisol and biparental care in a pair-living primate.

OBJECTIVES: We quantified variation in fecal cortisol across reproductive periods in Azara's owl monkeys (Aotus azarae) to examine physiological mechanisms that may facilitate biparental care. Specifically, we evaluated evidence for the explanation that owl monkeys have hormonal mechanisms to mobilize energy during periods when each sex is investing heavily in reproduction, that is, the gestation period for females and the infant care period for males. MATERIALS AND METHODS: Between 2011 and 2015, we monitored 10 groups of Azara's owl monkeys from a wild population in Formosa, Argentina and collected fecal samples from 26 adults (13 males, 13 females). Using enzyme-linked immunosorbent assays, we quantified fecal cortisol as a proxy for evaluating stress responses, including energetic demands, on both sexes during periods of reproduction and parental care. RESULTS: Male cortisol was lowest during periods when they were caring for young infants (<3 months) compared with periods with older infants or no infant. Female cortisol was elevated during gestation compared with other periods. Mean fecal cortisol in both males and females was lower when an infant was present compared with when females were gestating. DISCUSSION: Our results do not support the hypothesis that owl monkey males have elevated fecal cortisol during periods when they need to mobilize energy to provide intensive infant care. Our findings are also inconsistent with the Maternal Relief hypothesis. However, results from studies measuring fecal cortisol must be interpreted with care and alternative explanations, such as seasonal fluctuations in diet and thermoenergic demands, should be considered when drawing conclusions.

Ultrasonography-guided oocyte recovery in owl monkeys (aotus azarai infulatus).

The study evaluated an echo-guided oocyte recovery technique in owl monkeys. Twelve females were selected for the transabdominal ovum retrieval technique. This procedure collected twenty-six follicles, of which nine oocytes were recovered, without harm to the animals. The technique is feasible and is a minimally invasive protocol for neotropical primates.

Comparison of three reversible injectable chemical restraint protocols in Spix´s Owl monkeys (Aotus vociferans) using ketamine, xylazine and midazolam.

BACKGROUND: There is scarce information detailing clinical and physiological effects of reversible injectable protocols of chemical restraint on Neotropical primates. METHODS: Nineteen captive Spix´s Owl monkeys (Aotus vociferans) were assessed in a double-blind randomized crossover study using the following: ketamine/xylazine [KX], ketamine/midazolam [KM] and ketamine/xylazine/midazolam [KXM]. During immobilization, respiratory and pulse rates, rectal temperature, haemoglobin oxygen saturation and arterial blood pressure were recorded at 5-minute intervals during a 20-minute period; afterwards, antagonist drugs (yohimbine for xylazine and flumazenil for midazolam) were, respectively, administered. Quality and duration of induction, immobilization and recovery periods were recorded. RESULTS: Ketamine/xylazine increased manipulation sensitivity and produced poor muscle relaxation. KM maintained all assessed parameters within physiological ranges. KXM produced depressant cardiorespiratory effects and hypotension. All protocols produced hypothermia. CONCLUSIONS: Based on its adequate anaesthetic depth and minimum effects on physiological parameters, KM is suitable for immobilizing A vociferans and performing short-term procedures lasting around 20 minutes.

Sexual dimorphism in the loud calls of Azara's owl monkeys (Aotus azarae): evidence of sexual selection?

Primates use different types of vocalizations in a variety of contexts. Some of the most studied types have been the long distance or loud calls. These vocalizations have been associated with mate defense, mate attraction, and resource defense, and it is plausible that sexual selection has played an important role in their evolution. Focusing on identified individuals of known sex and age, we evaluated the sexual dimorphism in a type of loud calls (hoots) in a population of wild owl monkeys (Aotus azarae) in Argentina. We found evidence of sexual dimorphism in call structure, with females and males only emitting one type of call, each differing in dominant frequency and Shannon entropy. In addition, both age-related and sex-specific differences in call usage were also apparent in response to the removal of one group member. Future acoustic data will allow us to assess if there are individual characteristics and if the structure of hoot calls presents differences in relation to the social condition of owl monkeys or specific sex responses to variants of hoot calls' traits. This will provide deeper insights into the evolution of vocal mechanisms regulating pair bonding and mate choice strategies in this and other primate species.

Testing the weekend effect hypothesis: Time of day and lunar phase better predict the timing of births in laboratory-housed primates than day of week.

The weekend effect hypothesis proposes that captive primates are more likely to give birth during times of low disturbance and reduced staff activity. The hypothesis specifically predicts that laboratory-housed primates will be more likely to give birth during the weekend than weekdays when staff activity is reduced. To date, support for the weekend effect hypothesis has been mixed and based on studies with relatively few subjects. To further examine the hypothesis, we analyzed the birthing patterns of three genera of laboratory-housed primates: squirrel monkeys (Saimiri species, N = 2,090 births), owl monkeys (Aotus species, N = 479 births), and rhesus macaques (Macaca mulatta, N = 2,047 births). Contrary to predictions derived from the weekend effect hypothesis, the frequencies of births during weekends for all taxa were not significantly different from rates that would be expected by chance. However, while there was no variance across days of the week, all three taxa gave birth at nighttime, when staff was absent. This parallels reports of births in wild and captive monkeys, both diurnal and nocturnal, which are more likely to give birth during the night; plausibly a time when the environmental and social disturbance is lowest and the mother is safest to bond with her newborn infant. As all births occurred at night, we also explored the relationship between the lunar cycle and the timing of births timing. While the diurnal primates (i.e., Saimiri and Macaca) were no more likely to give birth on "bright" nights than "dark" nights, owl monkeys (Aotus) had a much higher frequency of births on bright nights than darker ones, and at rates that deviated from chance. Our data provide a more detailed understanding on how the environment may influence captive monkey births but do not support the oft-cited weekend effect hypothesis.

Are olfactory traits in a pair-bonded primate under sexual selection? An evaluation of sexual dimorphism in Aotus nancymaae.

OBJECTIVES: Sexual selection has seemingly influenced chemical communication in numerous non-human primates, although it is unclear whether it has influenced strictly pair-living and pair-bonded taxa. The physical similarities between male and female owl monkeys suggest that disruptive selection has not played a role in this taxon. However, given their nocturnality, olfactory traits may show differing patterns of sexual selection than visual traits. If sexual selection has influenced chemical communication in owl monkeys, we expect larger scent glands and greater scent-marking in females given the high degree of paternal care, as has been proposed for callitrichines. MATERIALS AND METHODS: We evaluated sex differences in the qualitative and quantitative descriptions of the subcaudal and perianal glandular regions of captive male (n = 39) and female (n = 36) owl monkeys (A. nancymaae), and in the olfactory behaviors performed within breeding pairs (n = 16). RESULTS: Males had larger areas of secretion retained in the hairs covering the subcaudal gland, and females had more and darker secretion than males covering the perianal region. Males inspected the genital region of their partners more frequently than females did, but the sexes did not differ much in other investigative and marking behaviors. DISCUSSION: The observed sex differences and variation in olfactory traits are consistent with the hypothesis that sexual selection has influenced chemical communication in owl monkeys, with males having larger subcaudal glands and spending more time investigating odors. Still, sex differences in monogamous owl monkeys were less extreme than those in other, non-monogamous, taxa.

Chemical composition of glandular secretions from a pair-living monogamous primate: Sex, age, and gland differences in captive and wild owl monkeys (Aotus spp.).

Broadening our knowledge of olfactory communication in strictly monogamous systems can inform our understanding of how chemosignals may facilitate social and reproductive behavior between the sexes. Compared to other social and mating systems, relatively little is known about olfactory communication in strictly monogamous non-human primates. Furthermore, platyrrhines are not well represented in chemical analyses of glandular secretions. We conducted semi-quantitative headspace gas chromatography with mass spectrometry to investigate the chemical components of glandular secretions from the subcaudal and pectoral glands of a strictly pair-living platyrrhine, the owl monkey (Aotus spp.). In this study, the first chemical analysis of a wild platyrrhine population, our goals were to (1) conduct a robust analysis of glandular secretions from both captive and wild owl monkey populations and (2) identify whether biologically relevant traits are present in glandular secretions. We also compared and contrasted the results between two Aotus species in different environmental contexts: wild Aotus azarae (N = 33) and captive A. nancymaae (N = 104). Our findings indicate that secretions from both populations encode sex, gland of origin, and possibly individual identity. These consistent patterns across species and contexts suggest that secretions may function as chemosignals. Our data also show that wild A. azarae individuals are chemically discriminated by age (adult or subadult). Among the captive A. nanycmaae, we found chemical differences associated with location, possibly caused by dietary differences. However, there was no noticeable effect of contraception on the chemical profiles of females, nor evidence that closely related individuals exhibit more similar chemical profiles in A. nancymaae. Overall, our data suggest that glandular secretions of both wild and captive Aotus convey specific information. Future studies should use behavioral bioassays to evaluate the ability of owl monkeys to detect signals, and consider whether odor may ultimately facilitate social and sexual relationships between male and female owl monkeys.

Evolutionary Origin of OwlRep, a Megasatellite DNA Associated with Adaptation of Owl Monkeys to Nocturnal Lifestyle.

Rod cells of many nocturnal mammals have a "non-standard" nuclear architecture, which is called the inverted nuclear architecture. Heterochromatin localizes to the central region of the nucleus. This leads to an efficient light transmission to the outer segments of photoreceptors. Rod cells of diurnal mammals have the conventional nuclear architecture. Owl monkeys (genus Aotus) are the only taxon of simian primates that has a nocturnal or cathemeral lifestyle, and this adaptation is widely thought to be secondary. Their rod cells were shown to exhibit an intermediate chromatin distribution: a spherical heterochromatin block was found in the central region of the nucleus although it was less complete than that of typical nocturnal mammals. We recently demonstrated that the primary DNA component of this heterochromatin block was OwlRep, a megasatellite DNA consisting of 187-bp-long repeat units. However, the origin of OwlRep was not known. Here we show that OwlRep was derived from HSAT6, a simple repeat sequence found in the centromere regions of human chromosomes. HSAT6 occurs widely in primates, suggesting that it was already present in the last common ancestor of extant primates. Notably, Strepsirrhini and Tarsiformes apparently carry a single HSAT6 copy, whereas many species of Simiiformes contain multiple copies. Comparison of nucleotide sequences of these copies revealed the entire process of the OwlRep formation. HSAT6, with or without flanking sequences, was segmentally duplicated in New World monkeys. Then, in the owl monkey linage after its divergence from other New World monkeys, a copy of HSAT6 was tandemly amplified, eventually forming a megasatellite DNA.

The role of intragroup agonism in parent-offspring relationships and natal dispersal in monogamous owl monkeys (Aotus azarae) of Argentina.

Agonistic behaviors are common in many group-living taxa and may serve a variety of functions, ranging from regulating conflicts over reproduction to defending food resources. However, high rates of agonism are not expected to occur among close relatives or individuals in established mating relationships, which are characteristics of monogamous groups. To contribute to our understanding of agonism within socially monogamous groups, we collected behavioral and demographic data from Azara's owl monkeys (Aotus azarae) in the Gran Chaco of Argentina over 14 years. We examined factors related to age, sex, kinship, and behavioral context to evaluate predictions of the hypotheses that agonism functions to regulate dispersal and that it mediates competition for food and/or mates. Intragroup agonism was relatively rare: the group rate was approximately one event every three and a half hours. Rates of agonism were generally similar for both sexes, but there were marked differences among age categories. Agonism performed by adults was more frequently directed at subadults than at younger offspring. In contrast, agonistic interactions involving infants were very rare. Among interactions between adults and subadults, adults were much more frequently the actors than the recipients, suggesting that agonism from adults may influence natal dispersal of subadults. Agonistic events were most frequent during foraging, but also occurred more frequently than expected during bouts of social behavior. Overall, our results suggest that agonism in owl monkeys serves as a mechanism for regulating dispersal, and also likely plays a role in mediating mating and feeding competition.

Co-Opted Megasatellite DNA Drives Evolution of Secondary Night Vision in Azara's Owl Monkey.

Owl monkeys (genus Aotus) are the only taxon in simian primates that consists of nocturnal or otherwise cathemeral species. Their night vision is superior to that of other monkeys, apes, and humans but not as good as that of typical nocturnal mammals. This incomplete night vision has been used to conclude that these monkeys only secondarily adapted to a nocturnal lifestyle, or to their cathemeral lifestyle that involves high night-time activity. It is known that the rod cells of many nocturnal mammals possess a unique nuclear architecture in which heterochromatin is centrally located. This "inverted nuclear architecture", in contrast with "conventional nuclear architecture", provides elevated night vision by passing light efficiently to the outer segments of photoreceptors. Owl monkey rod cells exhibit an intermediate chromatin distribution, which may provide them with less efficient night vision than other nocturnal mammals. Recently, we identified three megasatellite DNAs in the genome of Azara's owl monkey (Aotus azarae). In the present study, we show that one of the three megasatellite DNAs, OwlRep, serves as the primary component of the heterochromatin block located in the central space of the rod nucleus in A. azarae. This satellite DNA is likely to have emerged in the Aotus lineage after its divergence from those of other platyrrhini taxa and underwent a rapid expansion in the genome. Our results indicate that the heterochromatin core in the A. azarae rod nucleus was newly formed in A. azarae or its recent ancestor, and supports the hypothesis that A. azarae, and with all probability other Aotus species, secondarily acquired night vision.

Allogrooming in Male-Female Pairs of Captive Owl Monkeys (Aotus nancymaae).

Owl monkeys (Aotus spp.) are socially monogamous, yet allogrooming is reported to be rare. Because Aotus are nocturnal and arboreal, allogrooming is difficult to observe in natural settings. We observed 21 male-female pairs of captive Aotus nancymaae during 2 nonconsecutive study periods in order to describe the details of allogrooming between mates (partner grooming). We found that grooming bouts are brief and consist of tugging the hair or skin with flexed fingers and/or the mouth. Males groomed females most often, and their rates of partner grooming were negatively related to age. Partner grooming occurred regardless of mating behavior. Camera trap data revealed that the rate of partner grooming (1.50 bouts/h) is greater than that recorded from our direct observations in the early evenings (0.51 bouts/h, in 2013; 0.37 bouts/h in 2003) given that most bouts occurred later in the night. A positive relationship between the rates of the parents' partner grooming and those of their offspring later in life suggests intergenerational transmission. This relationship is influenced by the fathers' rates of partner grooming. We conclude that allogrooming in Aotus is a normal part of their behavioral repertoire that likely serves social functions similar to those in other pair-bonded primates.

Social monogamy in wild owl monkeys (Aotus azarae) of Argentina: the potential influences of resource distribution and ranging patterns.

Using published and new data from a population of monogamous owl monkeys in the Argentinean Chaco, I examine the hypothesis that social monogamy is a default social system imposed upon males because the spatial and/or temporal distribution of resources and females makes it difficult for a single male to defend access to more than one mate. First, I examine a set of predictions on ranging patterns, use of space, and population density. This first section is followed by a second one considering predictions related to the abundance and distribution of food. Finally, I conclude with a section attempting to link the ranging and ecological data to demographic and life-history parameters as proxies for reproductive success. In support of the hypothesis, owl monkey species do live at densities (7-64 ind/km(2) ) that are predicted for monogamous species, but groups occupy home ranges and core areas that vary substantially in size, with pronounced overlap of home ranges, but not of core areas. There are strong indications that the availability of food sources in the core areas during the dry season may be of substantial importance for regulating social monogamy in owl monkeys. Finally, none of the proxies for the success of groups were strongly related to the size of the home range or core area. The results I present do not support conclusively any single explanation for the evolution of social monogamy in owl monkeys, but they help us to better understand how it may function. Moreover, the absence of conclusive answers linking ranging, ecology, and reproductive success with the evolution of social monogamy in primates, offer renewed motivation for continuing to explore the evolution of monogamy in owl monkeys.

Age and sex-specific mortality of wild and captive populations of a monogamous pair-bonded primate (Aotus azarae).

In polygynous primates, a greater reproductive variance in males have been linked to their reduced life expectancy relative to females. The mortality patterns of monogamous pair-bonded primates, however, are less clear. We analyzed the sex differences in mortality within wild (NMales = 70, NFemales = 73) and captive (NMales = 25, NFemales = 29) populations of Azara's owl monkeys (Aotus azarae), a socially and genetically monogamous primate exhibiting biparental care. We used Bayesian Survival Trajectory Analysis (BaSTA) to test age-dependent models of mortality. The wild and captive populations were best fit by the logistic and Gompertz models, respectively, implying greater heterogeneity in the wild environment likely due to harsher conditions. We found that age patterns of mortality were similar between the sexes in both populations. We calculated life expectancy and disparity, the latter a measure of the steepness of senescence, for both sexes in each population. Males and females had similar life expectancies in both populations; the wild population overall having a shorter life expectancy than the captive one. Furthermore, captive females had a reduced life disparity relative to captive males and to both sexes in the wild. We interpret this pattern in light of the hazards associated with reproduction. In captivity, where reproduction is intensely managed, the risks associated with gestation and birth are tempered so that there is a reduction in the likelihood of captive females dying prematurely, decreasing their overall life disparity.

Ovarian function in captive owl monkeys (Aotus nancymaae and A. vociferans).

BACKGROUND: Ovarian function and morphology of owl monkeys (Aotus spp.) is inadequately known, but it is essential to describe this organ in detail to better understand reproductive patterns of the species. METHODS: This study reports the anatomical and histological features of the ovaries from 41 owl monkeys, considering their reproductive status and parity. RESULTS: The corpora lutea (CL) and reproductive state had a significant effect on ovarian volume. Follicles were observed in both pregnant and non-pregnant subjects. All females in the luteal phase and pregnant females showed at least one cyclic or pregnancy CL. Mean ovulation rate was 1.89 CL/female, and the mean ovum mortality was 37.5%. There were no significant differences in ovarian volume related to parity. CONCLUSIONS: These results contribute to the scarce information available on the reproductive biology of owl monkeys and can aid in the development of biotechnologies involved in assisted reproduction.

Evaluation of blood pressure in feline night monkeys (Aotus azarae infulatus) under different restraint protocols.

BACKGROUND: Feline night monkeys are very susceptible to stress when handled, and because of that, the use of anesthetic and physical restraint methods should be carefully evaluated. To ensure a safer anesthesia to the animals the present study aimed to observe the influence of four restraint protocols in the blood pressure of Aotus azarae infulatus. METHODS: Blood pressure was obtained from 10 animals subjected to restraining protocols using tiletamine and zolazepam, isoflurane, ketamine and midazolam, and physical restraint and results were evaluated to determine their effect on this exam. RESULTS: Among the restraint protocols tested, the anesthetic isoflurane promoted lower blood pressure values and no differences were observed between values measured in both arms in all groups. CONCLUSION: The results of our study suggest that all restraint protocols tested significantly alter blood pressure in this species of primates.

Functional morphology of the tubular genital organs in the female owl monkey (Aotus spp.).

BACKGROUND: Studies on reproductive morphology are important to understand the reproductive cycle of non-human primates. METHODS: This study describes the functional morphology of the adult female tubular genital organs in 41 Aotus (12.8 ± 6.8 years old, ranging from 3 to 25 years), with respect to reproductive status and number of parturitions. RESULTS: In females with developing embryos, endometrial glands showed a higher secretion than other females, and the embryo implantation occupied this secretive endometrium. Changes in the thickening, number of layers, and keratinization in the vaginal epithelium suggest that vaginal cytology may be an indicator of the estrous cycle. Non-pregnant multiparous females had a larger uterine body than nulliparous females. Number of parturitions and reproductive state had an impact on tubular genital organs in female owl monkeys. CONCLUSIONS: These results can be useful for the development of biotechnologies of reproduction and for improvement of the management of this species.