Epidemiological characterization of oral focal epithelial hyperplasia in brown howler monkeys (Alouatta guariba clamitans).

BACKGROUND: Oral focal epithelial hyperplasia (FEH) is an uncommon infection affecting humans, chimpanzees, bonobos, and howler monkeys. This study describes 10 cases of free-ranging brown howler monkeys (Alouatta guariba clamitans) diagnosed with FEH and Alouatta guariba Papillomavirus 1 (AgPV 1). METHODS: We analyzed demographic characteristics, rescue conditions, clinical and pathological findings, and species-specific behavior factors in these cases. The study assessed the frequency of occurrence and potential contributing factors of FEH and AgPV 1 infection. RESULTS: The frequency of FEH was 8.13%. Most affected howlers were adult or geriatric males with comorbidities or stressful conditions. Clinical and pathological observations were consistent with AgPV 1 infection. Species-specific behaviors and environmental stressors were identified as contributing factors. CONCLUSIONS: FEH associated with AgPV 1 affected mainly adult or geriatric males with ongoing comorbidities or stressful conditions. Further research is needed to understand these factors for effective management.

Temporal variation and age influence activity budget more than sex and reproductive status in wild brown howler monkeys (Alouatta guariba clamitans) inhabiting a large, continuous forest.

Activity budget analyses are important for understanding how animals spend their time in daily activities like resting, foraging, moving and socializing. These behaviors are closely linked to energy management, so habitat quality and resource availability are known to influence the activity budgets of species. Therefore, many studies have examined the consequences of habitat loss and fragmentation on the energetic demands and activity budgets of species. However, we still have limited knowledge of how animals behave in large, continuous, and protected environments, as such habitats are currently rare. The present study analyzed how temporal variation, age, sex and reproductive status influenced the activity budget of wild red howler monkeys (Alouatta guariba clamitans), in one of the last Atlantic Forest remnants that remains large and protected. Between November 2017 and December 2018, we monitored two groups, G3 and G4, in Parque Estadual Carlos Botelho, São Paulo, Brazil. The groups were composed of one adult male, two adult females and their offspring and one (G3) or two (G4) subadult males, using scan sampling for behavioral for data collection every 20 min. The most common behavior was resting, followed by foraging, moving and social interactions, with inter-group differences. Temporal variation explained most of the fluctuations in the activity budget, so did age and sex, but to a lesser degree. The reproductive status of females did not alter their activity budget. These findings reveal that even neighboring groups display distinct and intricate relationships with their habitat. Future studies should be conducted in continuous forests to determine what is the expected range of variation in activity budget, particularly in those species considered as flexible and inhabiting endangered habitats, such as the Atlantic Forest.

Hematology and serum biochemistry of free-ranging mantled howler monkeys (Alouatta palliata) at La Pacifica, Costa Rica.

BACKGROUND: Hematologic and blood biochemical values are key tools for assessing primate health. A long-term behavioral study of howler monkeys at a single site (La Pacífica, Guanacaste, Costa Rica), afforded the opportunity to develop baseline values for a large group of animals, evaluating differences between adult males and females and comparing to a report in the same population two decades later. METHODS: In 1998, 64 free-ranging mantled howler monkeys were anesthetized and sampled for hematologic and biochemical analysis. RESULTS: Blood analysis is reported for 29 adult females, 9 juvenile females, 19 adult males and 3 juvenile males. Four adults were excluded due to external injury or disease. There were few significant differences between adult females, juvenile females, and adult males. CONCLUSIONS: Baseline blood parameters are useful for determining normal values for howler monkey populations. The values for total protein, blood urea nitrogen, glucose, liver enzymes and potassium differed from a later study in 2019 may indicate changes that are influencing howler monkey health.

Mantled howler monkeys (Alouatta palliata) show no preferential hand use in two self-directed behaviors.

Hand preference is the preferential use of one hand for a single task. Its study provides insight into the neural mechanisms underlying motor skills, perception, and cognitive functions. From a comparative perspective, it also offers a window into evolutionary history, shedding light on whether manual preferences stem from genetics, environmental influences, or a combination of both. However, there is a paucity of information on preferential hand use for several primate taxa. Here we examine hand preference for the first time in mantled howler monkeys (Alouatta palliata) to determine if there is preferential hand use at the individual and population level as well as sex differences in hand use. We followed 17 wild adult individuals for 10 months and used focal animal sampling (506 focal samples) to record hand use in two types of self-directed behaviors, touching (1246 events) and scratching (1115 events). According to the binomial tests, four individuals were right-hand-preferent, two were left-hand-preferent, and 11 were ambilateral during touching, whereas for scratching seven individuals were right-hand-preferent, two were left-hand-preferent, and eight were ambilateral. At the population level, there was ambilaterality in both behaviors. At the individual level, according to the HI index, hand preference in touching and scratching were not associated and did not vary between sexes. These findings concur with previous studies with howler monkeys and other taxa suggesting that population-level hand preference is not a universal trait across primates.

Diversity of gastrointestinal parasites and molecular characterization of Giardia duodenalis in free-living and captive howler monkeys (Alouatta guariba clamitans) in southern Brazil.

Non-human primates (NHPs) are the group that most share infectious agents with humans due to their close taxonomic relationship. The southern brown howler monkeys (Alouatta guariba clamitans) are endemic primates from Brazil and Argentina's Atlantic Forest. This study aimed to investigate the presence of intestinal parasites in free-living (FL) and captive (CA) southern brown howler monkeys. Thirty-nine stool samples were collected in two areas in southern Brazil, 15 FL and 24 CA. Stool sediments obtained by centrifugal sedimentation technique were used for microscopic analysis and direct immunofluorescence assay and evaluated by molecular analysis through amplification and sequencing of TPI fragments. Intestinal parasites Giardia duodenalis, Cryptosporidium spp., and Trypanoxyuris minutus were detected at coproparasitological analysis. This is the first report of the presence of Cryptosporidium spp. in free-living howlers. The molecular characterization of G. duodenalis isolates indicated assemblage B for the first time found in free-living A. guariba clamitans. The high prevalence of G. duodenalis transmission in CA howler monkeys can be explained by direct contact with humans and frequent soil contact. The presence of a potentially zoonotic assemblage in these animals indicates that the process of fragmentation and cohabitation with humans and livestock affects the wildlife, thus indicating a need for eco-health measures.

FIELD TECHNIQUES FOR VASECTOMY IN BLACK HOWLER MONKEYS (ALOUATTA PIGRA).

Three adult black howler monkeys (Alouatta pigra) were vasectomized for the purpose of population control. Two different surgical approaches (inguinal and pelvic) were used to vasectomize the animals under general anesthesia. One monkey was vasectomized with a pelvic approach, and the other two monkeys were vasectomized with an inguinal approach. The inguinal approach was minimally invasive and proved to be an effective field procedure, utilizing minimal surgical equipment with a mean operative time of 35 min. The inguinal approach allowed for better visualization of the spermatic cord, which prompted easier ligation and transection of the ductus deferens. Identification of the ductus deferens was successfully performed intraoperatively using a tuberculin syringe to aseptically aspirate cord contents, as histopathology was not available. All howler monkeys fully recovered without complication. The social hierarchy of the troop and mating behavior has not been affected. There have been no new pregnancies reported in the troop since the vasectomies were performed. The inguinal approach is preferred as it is minimally invasive and can be performed confidently in a field setting.

Natural mycobacterium tuberculosis complex infection in a brown howler monkey (Alouatta guariba clamitans) in Brazil.

Neotropical primates rarely exhibit active tuberculosis. A brown howler monkey was found injured in an urban area. Histopathology revealed granulomatous inflammation in the lungs, lymph nodes, and liver. Immunohistochemistry and molecular analysis confirmed the presence of Mycobacterium tuberculosis complex. The findings highlight the importance of TB surveillance in nonhuman primates.

Leadership and the finder's advantage in mantled howler monkeys.

Leading collective movements and arriving first at feeding sites may improve food acquisition. Specifically, the first individual to discover and exploit a feeding site may gain a feeding advantage known as the "finder's advantage." The aim of this research was to verify if the probability of leading group movements to feeding sites in mantled howler monkeys (Alouatta palliata) varied by sex and reproductive status, and whether finders had higher foraging success than followers. We studied 18 adult individuals from two groups in La Flor de Catemaco over a year (978 h), and sampled group movements (n = 211) and foraging behavior (n = 215 feeding episodes). Gestating females were leaders and finders of group movements to feeding sites more often than expected but were also replaced in the leading position more frequently than individuals of other sex/reproductive states. Feeding behavior was not influenced by the order of arrival at feeding sites per se, but gestating females had higher food intake rate, bite rate, and feeding time when arriving earlier (i.e., occupying front group positions) than later. Therefore, leadership and the finder's advantage occur in this species and are probably employed by gestating females to maintain their energetic condition.

Facial and ocular thermal mapping in black-and-gold howler monkey (Alouatta caraya) by infrared thermography: An ex situ study.

BACKGROUND: This study used infrared thermography (IRT) for mapping the facial and ocular temperatures of howler monkeys, to determine parameters for the diagnosis of febrile processes. There are no published IRT study in this species. METHODS: Were evaluated images of a group of monkeys kept under human care at Sorocaba Zoo (São Paulo, Brazil). The images were recorded during 1 year, in all seasons. Face and eye temperatures were evaluated. RESULTS: There are statistically significant differences in face and eye temperatures. Mean values and standard deviations for facial and ocular temperature were respectively: 33.0°C (2.1) and 36.5°C (1.9) in the summer; 31.5°C (4.5) and 35.3°C (3.6) in the autumn; 30.0°C (4.3) and 35.6°C (3.9) in the winter; 30.8°C (2.9) and 35.5°C (2.1) in the spring. CONCLUSIONS: The IRT was effective to establish a parameter for facial and ocular temperatures of black-and-gold howler monkeys kept under human care.

A simple assay for measuring tannin-protein precipitation capacity offers insights into the diet and food choice of black howler monkeys (Alouatta pigra).

Phenolics, like tannins, are plant-specialized metabolites that play a protective role against herbivory. Tannins can reduce palatability and bind with proteins to reduce digestibility, acting as deterrents to feeding and impacting nutrient extraction by herbivores. Some assays measure tannin and total phenolics content in plants but lack determination of their biological effects, hindering the interpretation of tannin function in herbivory and its impacts on animal behavior and ecology. In this study, we successfully applied the radial diffusion assay to assess tannin protein precipitation (PP) capacity and evaluate the anti-nutritional effects of tannins in food plants (n = 24) consumed by free-ranging black howler monkeys (Alouatta pigra) in Tabasco, Mexico. We found PP rings in five plant species consumed by the monkeys. The mature fruit of Inga edulis was the most consumed food plant, despite having a high tannin PP capacity (56.66 mg tannic acid equivalent/g dry matter). These findings highlight the presence of tannins in the black howler diet and provide insight into the primates' resilience and potential strategies for coping with anti-nutritional aspects of the diet.

Cryopreservation of spermatozoa from black-and-gold howler monkeys (Alouatta caraya) using egg yolk-based or soy lecithin-based extenders.

There are more than 200 species and subspecies of Neotropical Primates of which more than 40% are listed as threatened by the IUCN Red List of Threatened Species. Both in situ and ex situ conservation programs can benefit from the use of assisted reproductive technologies. The objective of this study was to evaluate, for the first time, cryopreservation techniques for Alouatta caraya semen. Semen samples were collected from five adult males, analyzed, and frozen in either Test-egg yolk or Test-soy lecithin-based extenders containing either 3 or 4% glycerol. Frozen-thawed samples were analyzed at 10, 40, and 80 min post-thaw. Egg yolk-based extenders were overall better than soy lecithin-based extenders. There was no significant difference between 3 and 4% glycerol in any of the parameters analyzed, however, 4% glycerol in egg yolk-based extender produced more favorable results for total motility, intact plasma membrane, lipid peroxidation, and DNA fragmentation index. This study brought novel information on semen characteristics and cryopreservation aspects for A. caraya, which can help shape future experiments to improve the outcome of frozen-thawed sperm for this and other species of Neotropical primates.

Potential effects of brown howler monkey extinction on dispersal services in fragmented forests void of large dispersers.

The dispersal of large-seeded species strongly depends on medium-sized and large frugivores, such as primates, which are highly susceptible to population declines. In the Atlantic Forest, brown howler monkeys Alouatta guariba are medium-sized folivorous-frugivorous species that are likely to occur in small to large fragments where the largest frugivores are extinct. However, populations of this primate have been suffering from forest fragmentation, habitat loss, hunting, and the direct and indirect effects of yellow fever outbreaks, which increase the importance of understanding their role as seed dispersers and the impacts of their potential loss. The richness and abundance of large-seeded species might also be reduced in smaller fragments, which could directly affect the magnitude of the potential impact of disperser extinction on plant recruitment. Here, we tested the following mutually exclusive predictions on the effect of fragment size on plant richness and relative density of medium- and large-seeded species consumed by brown howler monkeys in fragments smaller than 1500 ha: the number and the relative density of plant species potentially affected by the local extinction of these monkeys will be (1) directly related to forest fragment size, or (2) not related to forest fragment size. Plant richness and the relative density of large- and medium-sized seed species consumed by brown howler monkeys did not vary with fragment size, corroborating our second prediction. Thus, the local extinction of brown howler monkeys would have a similar potentially negative impact on plant regeneration for the range of tested fragment sizes. We discuss the limitations of our results and suggest other lines of enquiry for the refinement of our conclusions.

Reconstruction of large scalp defect in a brown howler monkey (Alouatta guariba clamitans): A case report.

This case report describes different repair techniques used to reconstruct a large scalp defect in a brown howler monkey (Alouatta guariba clamitans) hit by a vehicle. Three reconstructive procedures were performed in two surgical stages. The repair techniques had successful outcomes on the patient's rehabilitation.

Predicting future climate change impacts on the potential distribution of the black howler monkey (Alouatta pigra): an endangered arboreal primate.

Climate change is one of the main factors affecting biodiversity worldwide at an alarming rate. In addition to increases in global extreme weather events, melting of polar ice caps, and subsequent sea level rise, climate change might shift the geographic distribution of species. In recent years, interest in understanding the effects of climate change on species distribution has increased, including species which depend greatly on forest cover for survival, such as strictly arboreal primates. Here, we generate a series of species distribution models (SDMs) to evaluate future projections under different climate change scenarios on the distribution of the black howler monkey (Alouatta pigra), an endemic endangered primate species. Using SDMs, we assessed current and future projections of their potential distribution for three Social Economic Paths (SSPs) for the years 2030, 2050, 2070, and 2090. Specifically, we found that precipitation seasonality (BIO15, 30.8%), isothermality (BIO3, 25.4%), and mean diurnal range (BIO2, 19.7.%) are the main factors affecting A. pigra distribution. The future climate change models suggested a decrease in the potential distribution of A. pigra by projected scenarios (from - 1.23 to - 12.66%). The highly suitable area was the most affected above all in the more pessimist scenario most likely related to habitat fragmentation. Our study provides new insights into the potential future distribution and suitable habitats of Alouatta pigra. Such information could be used by local communities, governments, and non-governmental organizations for conservation planning of this primate species.

Measuring mantled howler monkey (Alouatta palliata) testes via parallel laser photogrammetry: Expanding the use of noninvasive methods.

Parallel laser photogrammetry (PLP), which consists of attaching two or three parallel laser beams at a known inter-beam distance to a camera, can be used to collect morphological measurements of organisms noninvasively. The lasers project onto the photo being taken, and because the inter-beam distance is known, they act as a scale for image analysis programs like ImageJ. Traditionally, this method has been used to measure larger morphological traits (e.g., limb length, crown-rump length) to serve as proxies for overall body size, whereas applications to smaller anatomical features remain limited. To that end, we used PLP to measure the testes of 18 free-living mantled howler monkeys (Alouatta palliata) at La Selva Biological Station, Costa Rica. We tested whether this method could reliably measure this relatively small and globular morphology, and whether it could detect differences among individuals. We tested reliability in three ways: within-photo (coefficient of variation [CV] = 4.7%), between-photo (CV = 5.5%), and interobserver (intraclass correlation = 0.92). We found an average volume of 36.2 cm3 and a range of 16.4-54.4 cm3, indicating variation in testes size between individuals. Furthermore, these sizes are consistent with a previous study that collected measurements by hand, suggesting that PLP is a useful method for making noninvasive measurements of testes.

Radiographically guided femoral neck osteosynthesis with cannulated compressive titanium screw and anti-rotational component in a Brown Howler Monkey (Alouatta guariba clamitans).

A Brown Howler Monkey presented with a femoral neck fracture was successfully treated with a cannulated compressive screw and an anti-rotational component inserted with radiographically guided technique. Complete bone consolidation and functional recovery were observed 9 weeks after the surgery, and the monkey was released to his place of origin.

Mantled howler monkey males assess their rivals through formant spacing of long-distance calls.

Formant frequency spacing of long-distance vocalizations is allometrically related to body size and could represent an honest signal of fighting potential. There is, however, only limited evidence that primates use formant spacing to assess the competitive potential of rivals during interactions with extragroup males, a risky context. We hypothesized that if formant spacing of long-distance calls is inversely related to the fighting potential of male mantled howler monkeys (Alouatta palliata), then males should: (1) be more likely and (2) faster to display vocal responses to calling rivals; (3) be more likely and (4) faster to approach calling rivals; and have higher fecal (5) glucocorticoid and (6) testosterone metabolite concentrations in response to rivals calling at intermediate and high formant spacing than to those with low formant spacing. We studied the behavioral responses of 11 adult males to playback experiments of long-distance calls from unknown individuals with low (i.e., emulating large individuals), intermediate, and high (i.e., small individuals) formant spacing (n = 36 experiments). We assayed fecal glucocorticoid and testosterone metabolite concentrations (n = 174). Playbacks always elicited vocal responses, but males responded quicker to intermediate than to low formant spacing playbacks. Low formant spacing calls were less likely to elicit approaches whereas high formant spacing calls resulted in quicker approaches. Males showed stronger hormonal responses to low than to both intermediate and high formant spacing calls. It is possible that males do not escalate conflicts with rivals with low formant spacing calls if these are perceived as large, and against whom winning probabilities should decrease and confrontation costs increase; but are willing to escalate conflicts with rivals of high formant spacing. Formant spacing may therefore be an important signal for rival assessment in this species.

Food preferences and nutrient composition in captive Southern brown howler monkeys, Alouatta guariba clamitans.

Studies of food preferences in captive primates have so far mainly been restricted to frugivorous species. It was therefore the aim of the present study to assess the occurrence of spontaneous food preferences in a mainly folivorous primate, the captive Southern brown howler monkey, and to analyze whether these preferences correlate with nutrient composition. Using a two-alternative choice test, we presented ten male and five female adult Alouatta guariba clamitans with all possible binary combinations of ten types of food that are part of their diet in captivity and recorded their choice behavior. We found the howler monkeys to display the following rank order of preference: banana > mango > watermelon > papaya > beetroot > apple > pear > orange > cucumber > tomato. This preference ranking significantly and positively correlated with the total carbohydrate content and with the sucrose content of the food items. We also found significant positive correlations between the food preference ranking and the content of the minerals copper and magnesium. Male and female howler monkeys did not differ significantly in their food preference rankings. These results suggest this howler monkeys under human care are not opportunistic, but selective feeders with regard to maximizing their net gain of energy as only the content of carbohydrates, but not the contents of total energy, proteins, or lipids significantly correlated with the displayed food preferences. Thus, the food preferences of this primate are similar to those reported in several species of frugivorous primates tested with cultivated fruits and vegetables.

CAMPYLOBACTER HYOINTESTINALIS ISOLATION FROM HOWLER (ALOUATTA CARAYA) AND SPIDER MONKEYS (ATELES FUSCICEPS ROBUSTUS) AT A ZOOLOGIC FACILITY IN CENTRAL ILLINOIS.

Campylobacter hyointestinalis was initially isolated from an asymptomatic black howler monkey (Alouatta caraya) in a routine fecal culture examination. Fecal cultures from other individuals in this group and an adjacently housed black-headed spider monkey (Ateles fusciceps robustus) group recovered C. hyointestinalis from all but one of the individuals sampled (1.1 spider monkeys and 2.1 howler monkeys). Concurrently, one spider monkey presented with acute onset severe rectal prolapse and diarrhea. Whole-genome sequencing results of C. hyointestinalis isolates from all individuals were homologous and closely related to Campylobacter hyointestinalis subsp. hyointestinalis TTU_618, a strain typically associated with environmental samples. In addition, two cytolethal distending toxin (CDT) expressing gene clusters, cdt-I and cdt-II, were identified in all isolates. These results suggest C. hyointestinalis is transmissible to both howler monkeys and spider monkeys, though the origin of infection and whether it is transmissible between these species is undetermined.

Lead exposure and its relationship with fecal cortisol levels in black howler monkeys (Alouatta pigra).

Efficiently detecting early environmental threats to wildlife is vital for conservation. Beyond obvious dangers like habitat loss or deforestation, our study focuses on one of the most hazardous toxic metals for wildlife: lead (Pb). Pb is a widespread, cumulative, and insidious environmental pollutant that can trigger a wide range of physiological, biochemical, and behavioral disorders. In fact, Pb can cause permanent dysfunction of the major stress system, the hypothalamic pituitary adrenal (HPA) axis. We analyzed Pb and cortisol concentrations in fecal samples from Alouatta pigra in southern Mexico. Fecal samples were collected across six sites categorized as free-ranging (n = 65; conserved and disturbed) and from captive animals (n = 58). Additionally, we collected soil samples (n = 35). We found that Pb was present in 28% of fecal samples and 83% of soil samples. There was a positive relation between fecal and soil Pb levels, and fecal Pb concentration was negatively associated with cortisol levels. However, the claim of Pb being a direct interference with HPA axis requires further investigation. Given our findings, assessing wildlife exposure can be a valuable tool for understanding potential Pb exposure levels in the environment and its possible implications for human health. It can also serve as an early warning system of these consequences.