Black Howler Research Articles

Detection of Filariid Infections in Mexican Primate Populations Through qPCR.

Filariae are parasitic nematodes of high veterinary and medical importance, responsible for some acute tropical diseases. They are transmitted through the bite of hematophagous vectors such as biting midges and blackflies. Filariae are among the most prevalent vector-borne parasitoses in Neotropical primates in which severe infections can cause inflammatory reactions and tissue damage. Given the location inside the host (peritoneal cavity, bloodstream, and lymphatics), the detection of filariid nematodes is challenging and is mostly postmortem; hence the scarcity of studies on the prevalence of filariae in wild primate populations. Here, we report the prevalence of filariid infections in free-ranging populations of Geoffroy's spider (Ateles geoffroyi) and black howler (Alouatta pigra) monkeys across southern Mexico, using a combination of noninvasive sampling and molecular diagnostic techniques. Fecal samples were screened for filariid DNA by qPCR protocols. A total of 88 samples were examined with an overall prevalence of 26%. Filariae were slightly more common in spider monkeys compared to howler monkeys. This study constitutes the first report of the prevalence of infection of filariid nematodes in populations of wild spider monkey across southern Mexico, and the first reporting of filariae in black howler monkeys, as part of a new era of primate parasitology and the diagnostics of parasite infections in light of the everyday more affordable molecular tools.

IMMOBILIZATION OF BLACK HOWLER MONKEYS (ALOUATTA PIGRA) USING BUTORPHANOL, AZAPERONE, MEDETOMIDINE IS SAFE AND EFFECTIVE FOR NONINVASIVE PROCEDURES.

Administration of butorphanol, azaperone, and medetomidine (BAM) for immobilization of black howler monkeys (Alouatta pigra) has not been previously reported. In this observational study, 0.02 ml/kg of compounded BAM (butorphanol 27.3 mg/ml, azaperone 9.1 mg/ml, medetomidine 10.9 mg/ml) was administered IM in 10 captive black howler monkeys. Time to immobilization was recorded, an arterial blood gas performed, and at 5-min intervals, HR, RR, oscillometric arterial blood pressure, SPO2, and rectal temperature were measured. Naltrexone and atipamezole were administered IM at procedure completion and recovery times were recorded. If invasive procedures such as surgery were necessary and additional drugs needed, further data from that individual was removed from data analysis. Final BAM dosages were 0.55 ± 0.12 mg/kg butorphanol, 0.19 ± 0.04 mg/kg azaperone, and 0.22 ± 0.05 mg/kg medetomidine. Nine of 10 monkeys achieved sedation allowing for physical exam, venipuncture, and tuberculin skin testing within 4 ± 2 min. No monkeys reached a plane of immobilization allowing for intubation. Physiologic variables were acceptable for this species. Hypoxemia (SPO2 < 95%) was observed in three monkeys via pulse oximetry, and normoxemia was observed on arterial blood gas. Recovery was smooth and rapid. Therefore, BAM is a viable option for noninvasive procedures or as a premedication prior to induction of anesthesia in black howler monkeys.

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.

Detection and monitoring of the fauna of medium and large mammals using camera traps in a forest remnant area in the municipality of Água Fria de Goiás, Brazil – A tool for nature conservation

Despite the growing amount of information available, biodiversity is still under threat. Wildlife plays a crucial role in maintaining the ecological balance, and it is of logical and strategic importance to promote the further development of fauna recording and monitoring processes, emphasizing the need to strengthen the relationship between humans and nature. The aim was to record the species of medium and large mammals using camera traps. The study was conducted in the EcoCerrado Reserve in the municipality of Água Fria de Goiás, Brazil, between December 2020 and December 2022, using two camera traps in three different phytophysiognomies. 17 mammal species were recorded in 149 camera trap records, including species in the threatened category, such as Myrmecophaga tridactyla, Tapirus terrestrials, Chrysocyon brachyurus, Lycalopex vetulus, Panthera onca and Alouatta caraya. The mammal fauna observed in the study shows that this ecosystem can support populations of native species even in a modified landscape. This finding strengthens the basis for future initiatives aimed at environmental education, ecotourism, and more comprehensive legal protection for this region and other remnants of native vegetation in the Cerrado.

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

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. 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. 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. The IRT was effective to establish a parameter for facial and ocular temperatures of black-and-gold howler monkeys kept under human care.

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 80min 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, lipidperoxidation, 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.

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.

Individual vocal recognition and dear enemy effect in the black-and-gold howler monkey (Alouatta caraya)

Individual vocal recognition and dear enemy effect in the black-and-gold howler monkey (Alouatta caraya)

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.

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.

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.

Population level behavioural responses to variation in habitat quality across multiple locations in a fragmented landscape

Population level behavioural responses to variation in habitat quality across multiple locations in a fragmented landscape

A record of diurnal birth and placentophagia in an urban-dwelling female black and gold howler monkey (Alouatta caraya, Primates: Atelidae) in the City of Pilar, south-west Paraguay

Placentophagia, the postpartum consumption of the afterbirth by a mother, is widespread among eutherian mammals and linked to both endocrinological and ecological advantages. However, its occurrence in urban-dwelling arboreal primates, including the genus Alouatta, is not well represented in the literature. This is the first recorded instance of diurnal birth and placentophagia in an urban environment by a female black-and-gold howler monkey (Alouatta caraya) in Pilar, Paraguay. Observations were made as part of the Para La Tierra Urban Howler Project. A total of 165-minutes of observations during the postpartum period are reported presently, including behaviours of the mother, neonate, and other group members. The mother exhibited self- and allogrooming of the infant, and consumption of the placenta and umbilical cord, which aligns with known Alouatta post-parturition behaviors, despite the novel urban setting. This event indicates the species' behavioral flexibility and suggests potential adaptation to urban habitats, that are absent of natural predators but present novel anthropogenic stressors. Understanding a species’ adaptability is vital for development of robust conservation strategies as primates increasingly inhabit urban landscapes.

Disappearance of infants following male takeovers in the Belizean black howler monkey (&lt;i&gt;Alouatta pigra&lt;/i&gt;)

No abstract

Serological evidence for potential yellow fever virus infection in non-human primates, southeastern Mexico

BackgroundArthropod-borne flaviviruses like dengue virus (DENV) and yellow fever virus (YFV) are major human pathogens. In Latin America, YFV is maintained in sylvatic cycles involving non-human primates (NHP) and forest-dwelling mosquitos. YFV supposedly does not circulate north of Panama.MethodsWe conducted a serologic study for flaviviruses and other emerging viruses in NHP from southeastern Mexico. A total of thirty sera of black-handed spider monkeys (Ateles geoffroyi, n = 25), black howler monkeys (Alouatta pigra, n = 3), and mantled howler monkeys (Al. palliata, n = 2) sampled in 2012 and 2018 were screened by an indirect immunofluorescence assay (IFA) to detected IgG antibodies against DENV, YFV, Zika virus (ZIKV), West Nile virus (WNV), Rift Valley fever virus, Crimean-Congo hemorrhagic fever virus, Middle East respiratory syndrome coronavirus, and Zaire Ebola virus, and confirmed by plaque reduction neutralization tests (PRNT90) representing all mosquito-borne flavivirus serocomplexes circulating in the Americas.ResultsA total of 16 sera (53.3%; 95% CI, 34.3–71.7) showed IFA reactivity to at least one tested flavivirus with end-point titers ranging from 1:100 to 1:1000. No serum reacted with other viruses. Monotypic and high mean PRNT90 endpoint YFV titers of 1:246 were found in 3 black-handed spider monkey sera (10.0%; 95% CI, 2.1–26.5) sampled in 2018 in Tabasco, compared to all other flaviviruses tested. Monotypic endpoint PRNT90 titers of 1:28 for Ilheus virus and 1:22 for WNV in serum of black howler monkeys sampled in 2018 in Tabasco suggested additional flavivirus exposure.ConclusionsOur findings may suggest unnoticed YFV circulation. Intensification of YFV surveillance in NHP and vectors is warranted in Mexico and potentially other areas considered free of yellow fever.

Opportunistic meat-eating by urban folivorous-frugivorous monkeys.

The consumption of vertebrate tissues and eggs (hereinafter "meat") is relatively common among some primates that are highly frugivorous or eclectic omnivores, but rare or absent in those that are highly folivorous. The Neotropical howler monkeys (Alouatta spp.) belongin the latter group. Here we report the consumption of meat by free-ranging urban blackandgold howler monkeys (Alouatta caraya) and discuss the potential role of the consumed meat as a source of energy, protein, or micronutrients. We studied three groups of howler monkeys (comprising four to seven individuals), living in city squares (0.6, 1.5, and 1.9ha) in south Brazil, from July 2022 to May 2023 (65days; 797h of observations). All of the study groups were spontaneously supplemented daily by peoplewith variable amounts and types of food provided. Meat was only offered in the two larger squares. The groups' diets included leaves (42-49% scan sampling feeding records), fruit (3-20%), and flowers (2-5%) from 13 to 20 plant species, and considerable amounts of supplemented food (27-50%). We recorded 33 individual events of ingestion of supplemented cooked meat, three individual events of dove egg predation, and three bird nest inspections without egg consumption. All members of the two groups in the larger squares, except an infant male, ingested meat at least once. Meat accounted for 1% of total scan feeding records of both groups with access to this supplement. We conclude that whereas the opportunistic consumption of meat probably contributed only minor amounts of energy and protein to the study subjects, it may have benefitted them with micronutrients that are scarce in plant foods.

Estimating the impact of the illegal trade of primates in Mexico: a potential threat to wildlife.

The primates of Mexico, Ateles geoffroyi, Alouatta palliata, and Alouatta pigra, are seriously threatened by habitat loss, fragmentation, and illegal hunting and trade. Very little is known about the extent of illegal trade and its impacts on declining primate populations. Our study proposes a potential method based on estimating the number of individuals that die in the trade before being detected and those that probably cannot be detected. This facilitates estimating the number of animals extracted and allows an assessment of how trafficking impacts their populations. We derive estimates from seizure data of primates in Mexico between 2010 and 2019. To do this, we created wildlife detection rates and mortality rates from the existing literature (scientific articles, journalistic articles, and notes) to estimate the number of primates that die during capture, transport, and sale and the number of trafficked primates that were not detected by Mexican authorities. We estimate that 946 primates were removed from the wild for the pet trade each year (spider monkey Ateles geoffroyi= 854; black howler monkeys Alouatta pigra= 38, mantled howler monkey Alouatta palliata= 54). The annual reduction in population size caused by trafficking was greatest for Ateles geoffroyi (2.2%), followed by Alouatta pigra (1.3%), and Alouatta palliata (0.4%). Our estimates show the percentage of impacts that trafficking has on Mexican primate populations. Nevertheless, trade has the potential to impact declining populations and still must be addressed.

Activity Patterns of Howler Monkeys in Captivity

Howler monkeys are a diurnal genus of New World monkey whose diet may impact their frequency of activity and patterns of behavior. This study investigates this potential relationship by examining the activity frequency of black howler monkeys in captivity, where food is readily available. Captive howler monkeys were found to spend 77% of their time resting, 7% foraging or feeding, and 13% locomoting. When compared to wild specimens, these findings suggest that captivity and easy access to food are associated with more time resting, less time locomoting, and less time feeding or foraging. Future research should focus on investigating the effects of food accessibility on other primates in captivity to better understand how it influences their behavior and improve standards of captive primate care.

Hematology and blood biochemistry in a declining population of mantled howler monkeys (Alouatta palliata palliata) at La Pacifica, Costa Rica.

Alouatta palliata palliata are an ecologically flexible howler monkey subspecies that has recently been relisted as Endangered. Populations are declining through much of the subspecies' range, including at our study site at La Pacifica, Costa Rica. Our objectives were to screen blood hematology and biochemistry samples collected from this wild population to elucidate their baseline health. We collected blood samples from 38 adult individuals from across the study site and analyzed 13 hematology and 14 biochemistry parameters. Most hematology and blood biochemistry parameter values were similar between males and females. However, mean hemoglobin was significantly lower, and mean white blood cell count was significantly higher in females; and mean calcium and mean creatinine were significantly lower in females compared to males. Overall, the La Pacifica population appeared healthy based on the blood parameters analyzed from sampled individuals. Our results were also largely consistent with published data available from other populations of A. p. palliata, and with reference values for captive Alouatta caraya.

Fatal Simplexvirus humanalpha1 infection in howler-monkeys (Alouatta sp.) under human care: Clinical, molecular, and pathological findings.

Simplexvirus humanalpha1 (HuAHV-1) are common anthropozoonosis reported in marmosets but rare in howler monkeys (Alouatta sp.). Necropsy of two brown-howler monkeys (A. caraya) and one red-howler monkey (A. guariba clamitans) from different zoo collections were performed. Fragments of all organs were examined through microscopy. Samples were submitted to IHC for Simplexvirus humanalpha 2 (HuAHV-2) [sin. Herpesvirus simplex type 2] and PCR. Grossly, only the A. guariba showed liver lesions characterized by multifocal, pinpoint white areas corresponding microscopically as random necrotizing herpetic hepatitis and ulcerative glossitis. Both A. caraya showed necrotizing meningoencephalitis with Cowdry A-type body inclusions within neurons and astrocytes. Immunolabeling for HuAHV-1/2 was observed in the tongue, liver, and brain. HuAHV-1 was confirmed in all samples by PCR, Sanger sequencing, and phylogenetic analyses. Necrotizing meningoencephalitis was appreciated in 2/3 of animals, and it is associated with neurologic signs. Along with ulcerative glossitis, a hallmark lesion in marmosets, it was present in one animal. Regarding herpetic hepatitis, it is not frequent in monkeys and occurs mainly in immunocompromised animals. HuAHV-1 infection was confirmed corroborating with a human source. This is the second report on captive black-howler monkeys and the first gross, histologic, immunohistochemical, and molecular description of herpetic hepatitis and ulcerative glossitis in red-howler monkeys (A. guariba).