Alouatta Guariba Clamitans Research Articles

Prevalence and description of dental disorders in skulls of free-living wild primates from Paraná State, Brazil.

Non-human primates can present oral diseases. However, differences among the dentition of the various species make it difficult to understand their dental features and associated diseases. This research hypothesizes that the prevalence of dental disorders varies in the species studied according to distinct types of diet. Forty-five syncraniums of the species Alouatta caraya, Alouatta guariba clamitans, Sapajus nigritus, Callithrix jacchus, and Callithrix penicillata were evaluated by visual inspection, magnifying glasses, and on cone-beam computed tomography. Disorders identified consisted of missing teeth before death, agenesis, dental calculus, dental wear, dental staining, dental fracture, exposure of pulp chamber, alveolar bone resorption, tooth discoloration, and persistence of deciduous teeth. Alouatta guariba clamitans presented the most disorders. The results suggest that neotropical primates have a high prevalence of dental changes, even in free-living conditions, and that the differences observed among them may be associated with different diet patterns.

Medium-sized and large mammals of the Floresta da Cicuta Area of Relevant Ecological Interest, a protected area in southeastern Brazil

The Atlantic Forest is one of the most biodiverse biomes in the world and has been severely degraded and fragmented, with the extirpation of most medium-sized and large vertebrates from the forest remnants. Here we present the results of a survey of medium-sized and large mammals in an area of protected seasonal semideciduous forest, the Floresta da Cicuta Area of Relevant Ecological Interest (ARIE-FC), Rio de Janeiro, Brazil, part the Atlantic Forest biome. We used camera traps (2,257 camera days) and direct observations over a 23-month period. We recorded 19 species (including two domestic species), seven of which are classified as at-risk, such as Leopardus guttulus (Hensel, 1872), Sylvilagus tapetillus Thomas, 1913, Alouatta clamitans Cabrera, 1940, and Chrysocyon brachyurus (Illiger, 1815). A diverse terrestrial mammal assemblage in the ARIE-FC reinforces the importance of small forest fragments for the conservation of biodiversity in human-modified landscapes of the Brazilian Atlantic Forest.

Wischnewski Spots and Black Oesophagus in Suspected Fatal Hypothermia in a Brown Howler Monkey (Alouatta guariba clamitans) and a Rabbit (Oryctolagus cuniculus)

Fatal hypothermia represents a diagnostic challenge in veterinary pathology. Wischnewski spots (WS) and black oesophagus (BO) have been described in human cases of fatal hypothermia but rarely in animals. We now describe WS and BO in suspected fatal hypothermia in a free-ranging brown howler monkey (Alouatta guariba clamitans) and a pet rabbit (Oryctolagus cuniculus). Both animals had dark spots resembling WS on the gastric mucosa and the monkey also had BO with haematin deposition. In both cases, stress factors and relatively cold environmental conditions were present prior to death.

Flower consumption, ambient temperature and rainfall modulate drinking behavior in a folivorous-frugivorous arboreal mammal.

Water is vital for the survival of any species because of its key role in most physiological processes. However, little is known about the non-food-related water sources exploited by arboreal mammals, the seasonality of their drinking behavior and its potential drivers, including diet composition, temperature, and rainfall. We investigated this subject in 14 wild groups of brown howler monkeys (Alouatta guariba clamitans) inhabiting small, medium, and large Atlantic Forest fragments in southern Brazil. We found a wide variation in the mean rate of drinking among groups (range = 0-16 records/day). Streams (44% of 1,258 records) and treeholes (26%) were the major types of water sources, followed by bromeliads in the canopy (16%), pools (11%), and rivers (3%). The type of source influenced whether howlers used a hand to access the water or not. Drinking tended to be evenly distributed throughout the year, except for a slightly lower number of records in the spring than in the other seasons, but it was unevenly distributed during the day. It increased in the afternoon in all groups, particularly during temperature peaks around 15:00 and 17:00. We found via generalized linear mixed modelling that the daily frequency of drinking was mainly influenced negatively by flower consumption and positively by weekly rainfall and ambient temperature, whereas fragment size and the consumption of fruit and leaves played negligible roles. Overall, we confirm the importance of preformed water in flowers to satisfy the howler's water needs, whereas the influence of the climatic variables is compatible with the 'thermoregulation/dehydration-avoiding hypothesis'. In sum, we found that irrespective of habitat characteristics, brown howlers seem to seek a positive water balance by complementing the water present in the diet with drinking water, even when it is associated with a high predation risk in terrestrial sources.

Molecular detection of Apicomplexa protozoa in tissues from Alouatta guariba clamitans

ABSTRACT: The brown howler monkey (Alouatta guariba clamitans) is a primate species widely distributed in South America. Infections by protozoa are common in primates. However, studies on protozoa in primates in Brazil are scarce, so the goal of this study was to investigate DNA from the apicomplexan protozoa Neospora caninum, Sarcocystis spp. and Toxoplasma gondii in tissues of A. guariba clamitans. DNA extraction was performed on tissue samples from the heart, brain, liver, spleen, lung and intestine of six A. guariba clamitans from Santa Maria, Central Region of Rio Grande do Sul, Brazil. Conventional PCR was performed using 18S rRNA gene general primers for Apicomplexa and also specific primers to amplify Neosporaspp. and Toxoplasma gondii DNA. All animals were positive in the 18S PCR and the genetic sequencing confirmed the presence of Sarcocystis spp. DNA in the tissues of four animals belonging to at least two species (S. neurona and S. gigantea) and T. gondii DNA in the other two animals. One positive sample for T. gondii was genotypically characterized as atypical by the restriction fragment length polymorphism technique. N. caninum DNA was not detected in the tested samples. The presence of Apicomplexa protozoan DNA in the tissues of the six animals tested in this study highlights the importance of howler monkeys as maintainers of these pathogens in nature.

Fibular and metatarsal osteosynthesis in a southern brown howler monkey (Alouatta guariba clamitans)

Here we describe a successful surgical management of a distal fibular fracture combined with a tarsocrural luxation and multiple metatarsal fractures in the left foot of a southern brown howler monkey (Alouatta guariba clamitans). We achieved satisfactory outcome by applying intramedullary pinning for each of the bone fractures and closed reduction of joint luxation-kept in place only by bone alignment, without further ligament reconstruction. Bone healing occurred uneventfully within eight weeks and the monkey's foot regained its normal function. Therefore, we could properly release the patient back into the wild.

Attacks of domestic dogs on Common Long‐Nosed Armadillo Dasypusnovemcinctus and Southern Brown Howler Monkey Alouatta guariba in fragmented Atlantic Forest and implications in a region of high priority for biodiversity conservation

AbstractDomestic dogs can negatively impact natural systems, and understanding these dynamics is essential to mitigate their impact. We report two cases of attacks of domestic dogs on native mammals in a fragmented landscape of the Atlantic Forest, southern Brazil. Our records occurred in a region of high priority for the conservation of this biome. We observed two attacks, one on a Common Long‐Nosed Armadillo Dasypus novemcinctus and another on a Southern Brown Howler Monkey Alouatta guariba clamitans. Our records highlight additional threats to the wild and native fauna reinforcing the importance of accounting for the presence of domestic fauna when delineating conservation strategies in highly fragmented environments.

Clinical and pathological aspects of first report of Tunga penetrans infestation on southern brown howler monkey (Alouatta guariba clamitans) in Rio Grande do Sul, Brazil

Tungiasis is a neglected neotropical disease caused by penetration of Tunga spp. into the skin of the host. Two primates were rescued from nearby different indigenous villages, and the clinical, pathological, and parasitological features of tungiasis were described. Flea identification occurred through their morphometry and was confirmed with the use of a dichotomous key. Monkey 1 was parasitized by 23 sand fleas and, after treatment, was assigned to the animal rehabilitation center. Monkey 2 was in poor body condition and died shortly after clinical examination. At necropsy, this primate was parasitized by 26 specimens of sand fleas. Both animals altered their tree behavior by staying on the ground for long periods. This parasitic relationship implies the possibility of enlargement of the sand flea dispersion. Thus, this is the first record of Tunga penetrans occurrence in wild Alouatta guariba clamitans.

Positively selected variants in functionally important regions of TLR7 in Alouatta guariba clamitans with yellow fever virus exposure in Northern Argentina.

In 2007-2009, a major yellow fever virus (YFV) outbreak in Northern Argentina decimated the local howler monkey (Alouatta) population. To evaluate whether the surviving howler monkeys possess advantageous genetic variants inherited from monkeys alive prior to the YFV outbreak, we explored the relationship between Toll-like receptor (TLR) 7 and TLR8 gene variation and YFV susceptibility. We used samples from Alouatta individuals in Misiones, Argentina alive before the YFV outbreak, individuals that died during the outbreak, and individuals that survived the outbreak and are alive today. We measured genetic divergence between Alouatta YFV exposure groups and evaluated Alouatta-specific substitutions for functional consequences. We did not find different allele frequencies in the post-YFV exposure Alouatta group compared to the pre-exposure group. We identified three nonsynonymous variants in TLR7 in Alouatta guariba clamitans. Two of these substitutions are under positive selection in functionally important regions of the gene. Our results did not indicate that surviving howler monkey spossess advantageous genetic variants at greater frequency than those alive before the YFV outbreak. However, the positively selected unique coding differences in A. guariba clamitans are in the region important in pathogen detection which may affect YFV resistance. Morework is necessary to fully explore this hypothesis.

Encounter rate and behavior of Alouatta guariba clamitans in the Ilha Grande State Park, Rio de Janeiro state, Brazil

Alouatta guariba clamitansCabrera, 1940 is an endemic species of the Atlantic Forest that occurs from south Bahia, Brazil, extending south to the province of Misiones, Argentina. In Rio de Janeiro state, the species was classified as threatened, indicating that attention is needed for the conservation of this taxon. Additionally, an outbreak of yellow fever spread throughout the southeastern states of Brazil from January 2017 until March 2018 seriously threatening Rio de Janeiro populations of the species. Herein, we aimed to provide the first estimates ofA. g. clamitansencounter rate, density, and population size in the Ilha Grande State Park (PEIG), which is part of the Atlantic Forest biome of Brazil. Data were collected in two different periods, the first between December 2003 and May 2005, and the second from August 2009 to May 2010, and information on encounter rates and behavior was collected to better understand aspects of species' ecology. The estimated encounter rate in the first period through the distance sampling method was 0.04 ± 0.01 individuals per kilometer. Nine groups were recorded in the second period of the study, with 47 individuals along 3 km. Our estimates of encounter rate, density and population size were low and reinforces the need to initiate species monitoring and assess the impact that yellow fever outbreaks may have on PEIG populations. The results presented here can be a starting point to support future strategic actions for the species, to measure impacts and to the management of the species, and for a conservation program.

Comparison of midazolam and butorphanol combined with ketamine or dexmedetomidine for chemical restraint in howler monkeys (Alouatta guariba clamitans) for vasectomy.

This study evaluated and compared cardiorespiratory and blood gas parameters, as well as sedation, analgesia and recovery of two protocols: ketamine (10mg/kg) or dexmedetomidine (10μg/kg), with midazolam (0.5mg/kg) and butorphanol (0.3mg/kg), IM (KBM and DBM, respectively) in brown howler monkeys (Alouatta guariba clamitans). Twelve brown howler monkeys were selected in two groups and evaluated for cardiorespiratory parameters and sedation, from 5-30minutes after latency. Blood gas and arterial lactate were taken at 5 and 30minutes. In the end, time and quality of recovery were evaluated. The HR in DBM group was significantly lower at all times. The sedation score was higher in DBM. Recovery in DBM was faster. All animals had moderate hypoxaemia. Both protocols produce satisfactory anaesthesia and analgesia, but DBM provides deeper sedation with faster recovery. Oxygen supplementation is recommended in both due to hypoxaemia.

Successful adoption of an orphan infant in a wild group of brown howler monkeys.

The rarity of infant adoption in wild primates compromises our understanding of its consequences for the participating individuals. We report the first case of successful infant adoption in a wild group of brown howler monkeys (Alouatta guariba clamitans). We evaluated the potential costs of the behavior for the adoptive mother by comparing her activity budget and diet before and after the adoption. On 18 June 2013, a domestic dog killed the mother of a 2-month-old male infant (Victorio) as she attempted to cross a canopy gap. Victorio was immediately rescued from her belly by a researcher and released in a climber near another infant-carrying female (Sofia, his likely grandmother). Sofia recovered him 2min later. She carried and breastfed both infants during the next 4 weeks, when her own infant disappeared. We monitored Victorio until he reached adulthood in March 2018. Sofia fed more (mainly on immature leaves) when she nursed only Victorio than when nursing only her own or both infants. Assuming that the disappearance of Sofia's own infant was unrelated to the adoption of Victorio, we conclude that his successful adoption may contribute to Sofia's inclusive fitness if he sires his own infants.

Howler monkeys are the reservoir of malarial parasites causing zoonotic infections in the Atlantic forest of Rio de Janeiro.

BackgroundAlthough malaria cases have substantially decreased in Southeast Brazil, a significant increase in the number of Plasmodium vivax-like autochthonous human cases has been reported in remote areas of the Atlantic Forest in the past few decades in Rio de Janeiro (RJ) state, including an outbreak during 2015–2016. The singular clinical and epidemiological aspects in several human cases, and collectively with molecular and genetic data, revealed that they were due to the non-human primate (NHP) parasite Plasmodium simium; however, the understanding of the autochthonous malarial epidemiology in Southeast Brazil can only be acquired by assessing the circulation of NHP Plasmodium in the foci and determining its hosts.MethodologyA large sampling effort was carried out in the Atlantic forest of RJ and its bordering states (Minas Gerais, São Paulo, Espírito Santo) for collecting and examining free-living NHPs. Blood and/or viscera were analyzed for Plasmodium infections via molecular and microscopic techniques.Principal findingsIn total, 146 NHPs of six species, from 30 counties in four states, were tested, of which majority were collected from RJ. Howler monkeys (Alouatta clamitans) were the only species found infected. In RJ, 26% of these monkeys tested positive, of which 17% were found to be infected with P. simium. Importantly, specific single nucleotide polymorphisms–the only available genetic markers that differentiate P. simium from P. vivax–were detected in all P. simium infected A. clamitans despite their geographical origin of malarial foci. Interestingly, 71% of P. simium infected NHPs were from the coastal slope of a mountain chain (Serra do Mar), where majority of the human cases were found. Plasmodium brasilianum/malariae was initially detected in 14% and 25% free-living howler monkeys in RJ and in the Espírito Santo (ES) state, respectively. Moreover, the malarial pigment was detected in the spleen fragments of 50% of a subsample comprising dead howler monkeys in both RJ and ES. All NHPs were negative for Plasmodium falciparum.Conclusions/SignificanceOur data indicate that howler monkeys act as the main reservoir for the Atlantic forest human malarial parasites in RJ and other sites in Southeast Brazil and reinforce its zoonotic characteristics.

Supplemented howler monkeys eat less wild fruits, but do not change their activity budgets.

Research on the influence of food supplementation on primate behavior has focused on terrestrial and semiterrestrial species. Its effects on highly arboreal species are poorly known. We assessed the influence of food supplementation on the feeding behavior and activity budget of four adult female and two adult male brown howler monkeys (Alouatta guariba clamitans) belonging to two groups (JA and RO) that inhabited periurban forest fragments in southern Brazil. We used the "focal-animal" method during 6-8 full days per month from March to August 2017 (916 h of observation) to record the behavior of the study subjects. The feeding events of the focal individual were recorded using the "all occurrences" method. The supplementation was unevenly distributed during the day and accounted for 5-6% of all feeding events of male and female howlers, respectively. JA always received fruit in a platform, whereas RO had access to fruits and processed foods on roofs and directly from humans. The mean biomass of wild foods ingested by each adult per day was >300% higher than the ingested biomass of supplemented foods (females: 395 vs. 109 g/day; males: 377 vs. 120 g/day), but the ingestion rate of supplemented foods was ca. 400% higher than that of wild foods (females: 17 vs. 4 g/min; males: 19 vs. 5 g/min). The activity budgets of females and males were dominated by resting (66-72%) followed by feeding (18-14%), moving (12-11%), and socializing (2%). We found that food supplementation reduced the ingestion of wild fruits, but it did not affect the howlers' need to ingest a given amount of leaves per day and the time spent resting, feeding, moving, and socializing.

Assessing the influence of biotic, abiotic, and social factors on the physiological stress of a large Neotropical primate in Atlantic forest fragments

Wildlife physiological responses to environmental and human-related stressors provide useful clues on animal welfare. Non-invasive biomarkers, such as fecal glucocorticoid metabolites (fGCM), allow researchers to assess whether variations in habitat quality, behavior, and climate influence the animals' physiological stress. We examined the role of fragment size, ambient temperature, ripe fruit availability and consumption, percentage of records moving, sex, female reproductive state, and group composition as predictors of the level of fGCM in adult brown howler monkeys (Alouatta guariba clamitans) inhabiting three small (<10 ha) and three large (>90 ha) Atlantic Forest fragments in southern Brazil. We collected bimonthly behavioral data and fecal samples from adult individuals over three years, and used a multimodel inference framework to identify the main predictors of fGCM. We found that the mean (±SD) fGCM in the study groups ranged from 57 ± 49 ng/g to 93 ± 58 ng/g, which were within the known range for howler monkeys. We found 10 best models including five of the 17 tested variables. Sex and reproductive state were the only variables included in all these models. We found that fGCM was higher in nursing females (mean ± SD = 104 ± 73 ng/g) than in non-nursing females (64 ± 55 ng/g) and males (53 ± 40 ng/g, P < 0.05) and that it decreased with increasing ripe fruit consumption and minimum temperature. However, fragment size did not predict fGCM concentration (groups in small fragments = 71 ± 58 ng/g vs. groups in large fragments = 63 ± 54 ng/g, P > 0.05). We conclude that factors related to the energetic balance of individuals play major roles in modulating the physiological stress of brown howler monkeys. Future studies should investigate the consequences of higher levels of stress hormones on howler monkey health and demography.

Hematological and serum biochemistry data on southern brown howler monkeys (Alouatta guariba clamitans) in captivity in Brazil.

Physiological values reflect the health condition and responses of individuals to handling in captivity. The aim of this study was to establish hematological and serum biochemistry parameters of clinically healthy animals of the Alouatta guariba clamitans subspecies. We collected blood samples from adult males and females kept at the Center for Biological Research of Indaial after chemical containment with 3.9mg/kg of tiletamine hydrochloride and zolazepam. Significant differences between males and females were found in the levels of erythrocytes, hemoglobin, hematocrit, lymphocytes, neutrophils, platelets, mean corpuscular hemoglobin concentration (MCHC), and gamma-glutamyltranspeptidase (GGT). Our results suggest the existence of sexual dimorphism in some physiological parameters of Aguariba clamitans. The parameters reported herein can be used as reference values for other populations kept under similar conditions.

Capture of Alouatta guariba clamitans for the surveillance of sylvatic yellow fever and zoonotic malaria: Which is the best strategy in the tropical Atlantic Forest?

Howler monkey capture is an arduous and expensive task requiring trained and specialized professionals. We compared strategies and methods to most efficiently capture Alouatta guariba clamitans in remnants of the Atlantic Forest in Rio de Janeiro and its bordering states of Minas Gerais and São Paulo. We tested whether or not the success of expeditions in the forest with anesthetic darts, nets, and baited traps differed with and without the support of an information network, a contact chain built with key institutions and inhabitants to continuously monitor howler monkey presence. The influence of forest conditions (vegetation type and fragment size) upon darting success was also evaluated. We captured 24 free-living A. guariba clamitans. No howler monkey was caught with traps, probably due to the predominantly folivore feeding to high local plant diversity providing a great variety of food options. Captures based on an information network were significantly more efficient in terms of numbers of caught monkeys than without it. Captures with darts were considerably more efficient when performed in semideciduous forests and small forest fragments as opposed to ombrophilous forests or large woods. Although we walked great distances within the forest searching for howler monkeys, all but one animal were captured at the forest fringes. Hindrances to search and the darting method in the Atlantic Forest, for example, the steep terrain, high tree canopies, hunt pressure, and low A. guariba clamitans population density, were mitigated with the use of the information network in this monkey capture. Moreover, the information network enhanced the surveillance of zoonotic diseases, which howler monkeys and other nonhuman primates are reservoirs in Brazil, such as malaria and yellow fever.

Plasmodium infection and its association with biochemical and haematological parameters in free-living Alouatta guariba clamitans (Cabrera, 1940) (Primates: Atelidae) in Southern Brazil.

BACKGROUND The influence of Plasmodium spp. infection in the health of Southern brown howler monkey, Alouatta guariba clamitans, the main reservoir of malaria in the Atlantic Forest, is still unknown.OBJECTIVES The aim of this study was to investigate the positivity rate of Plasmodium infection in free-living howler monkeys in an Atlantic Forest fragment in Joinville/SC and to associate the infection with clinical, morphometrical, haematological and biochemical alterations.METHODS Molecular diagnosis of Plasmodium infection in the captured monkeys was performed by Nested-polymerase chain reaction (PCR) (18S rRNA and coxI). Haematological and biochemical parameters were compared among infected and uninfected monkeys; clinical and morphometrical parameters were also compared.FINDINGS The positivity rate of Plasmodium infection was 70% among forty captured animals, the highest reported for neotropical primates. None statistical differences were detected in the clinical parameters, and morphometric measures comparing infected and uninfected groups. The main significant alteration was the higher alanine aminotransferase (ALT) levels in infected compared to uninfected monkeys.MAIN CONCLUSIONS Therefore, Plasmodium infection in howler monkeys may causes haematological/biochemical alterations which might suggest hepatic impairment. Moreover, infection must be monitored for the eco-epidemiological surveillance of malaria in the Atlantic Forest and during primate conservation program that involves the animal movement, such as translocations.

Immigration of a female &lt;i&gt;Alouatta guariba clamitans&lt;/i&gt; into a group inhabiting a restinga forest in southern Brazil

No abstract

Surviving in the urban-rural interface: Feeding and ranging behavior of brown howlers (Alouatta guariba clamitans) in an urban fragment in southern Brazil.

Wild primates that live in urban areas face extreme threats that are less frequent in nonurban fragments, such as the presence of dangerous matrix elements (e.g., roads, power lines, buildings, and a high density of domestic dogs near food patches), that could influence their movements, feeding behavior, and survival. However, the scarcity of studies addressing this issue hinders our understanding of the behavioral adjustments that favor the survival of primates in urban areas. For 12 months, we studied a six-individual group of brown howlers (Alouatta guariba clamitans) in an urban fragment to determine (i) their diet richness and its relationships with food availability, (ii) their daily path length (DPL) and the matrix elements used during movement, and (iii) the main ecological drivers of the DPL. Sampling effort totaled 72 days, 787 hr, and 3,224 instantaneous scans. We found that the diet of brown howlers contained 35 plant species (including seven cultivated crops) belonging to 33 genera and 21 families. The consumption of fruits and young leaves was directly related to their temporal availability. The average DPL (446 m) was smaller than that reported for groups of howlers inhabiting large nonurban fragments. To move between food patches, animals used three main matrix elements: trees, power lines, and roofs. The number of plant species used during the day was the main driver of DPL. Our findings highlighted that the generalist-opportunistic diet of brown howlers and their ability to move across the anthropogenic matrix using artificial elements such as power lines, roofs, and wildlife crossings represent a remarkable part of their behavioral repertory in Lami. However, there are potential costs associated with these strategies, namely, electrocution and predation by domestic dogs. Thus, it is urgent to further investigate how these behaviors could affect the long-term survival of these animals.