Alouatta Guariba Clamitans Research Articles

Growth and allometric curves of southern brown howler monkey (Alouatta guariba): Insights on its ontogeny and conservation.

Ontogenetic sexual dimorphism is observed in different primate species, with ecological and evolutionary relationships explaining this pattern. Understanding the growth of the southern brown howler monkey elucidates not only the ecology and evolution but also contributes to conservation projects for this species. Throughout 20 years of the Centro de Pesquisas Biológicas de Indaial-Projeto Bugio, Brazil, we collected morphological data on 105 howlers of the Alouatta guariba species to identify the growth differences between ontogenetic categories and sexes and generate a growth curve to estimate the age of rescued individuals. Linear measurements were employed to obtain body length as well as the dimensions of the head and limbs. All individuals were also weighed to obtain body mass. We assessed growth rate and duration using allometric analysis based on the individuals' ages. We compared growth rate and duration among infant, juvenile, and adult howlers and between sexes. We provide growth curves for body size for both sexes using the Von Bertalanffy model. Infants have accelerated growth rate in comparison to the juveniles and adults, with no differences between sexes in establishing body length at this ontogenetic stage. Males have a prolonged development duration from the juvenile stage, reaching adulthood later than females, which explains the body length differences found in this species. Variables of head and limbs analyzed also showed differences in growth rate and duration, but not so consistently among ontogenetic stages. Mass was not a good variable to understand the growth differences of the animals, since many arrived feeble in the project and may have lost mass due to different circumstances in old age. Therefore, growth curves were obtained only for body length, allowing the estimation of the age of these animals when rescued from the wild to more effectively provide needed care in captivity.

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

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). 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. 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. 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 20min. 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.

Successful treatment of Trypanoxyuris sp. infection in naturally infected southern brown-howlers (Alouatta guaribaclamitans)

Southern brown-howler monkeys (Alouatta guariba clamitans) may harbor Trypanoxyuris sp., a pinworm parasite with documented fatal consequences in this species. Despite this risk, effective treatment protocols remain unclear. Therefore, the present study aimed to evaluate the efficacy of two anthelmintic protocols against natural infections in two brown-howler monkeys received at the Wild Animal Care and Rehabilitation Sector (SARAS-CAV-UDESC). The protocols utilized pyrantel pamoate & praziquantel (600.0 mg, PO, single dose) and albendazole (20.0 mg, PO, daily for 5 days). Fecal egg counts were carried out daily at the Laboratory of Parasitology and Parasitic Diseases (LAPAR-CAV-UDESC) before and after drug administration. Both treatments successfully eliminated Trypanoxyuris sp. infections. The animal treated with pyrantel pamoate & praziquantel achieved egg clearance by day 6 (144 h), demonstrating effectiveness with a single administration. Albendazole cleared the infection within 2 days of treatment, indicating its potential as a fast-acting treatment. No adverse effect were observed in the treated monkeys. These findings contribute to the development of evidence-based treatment protocols for Trypanoxyuris sp. in primates, enhancing animal health and welfare of captive and wild populations.

Urban Matrices Threaten Patch Occurrence of Howler Monkeys in Anthropogenic Landscapes

Habitat modification due to human activities threatens species survival. While some species can inhabit habitat patches in anthropogenic landscapes, their occurrence often depends on landscape structure. We assessed the effects of landscape structure on brown howler monkey (Alouatta guariba clamitans) occurrence in an urban scenario. We conducted censuses in 59 forest patches from 2014 to 2016 in Rio Grande do Sul State, Brazil. We evaluated patch occurrence (presence/absence) in response to landscape composition (forest cover, arboreal crops, urban areas, open areas, and water) and configuration (patch density), considering the scale of effect. Water, urban, and open areas were the most important predictors of howler presence. Their presence was notably higher in landscapes with more water, likely because these landscapes consist of rural areas with low urbanization, less farming, and relatively high forest cover. Presence of howlers was positively associated with forest cover and negatively related to urban areas, open areas, and arboreal crops. Resource scarcity and increased mortality risks from human pressures, such as domestic dog attacks, electrocution, and roadkill on these land covers may explain these relationships. We highlight the importance of conserving and increasing forest cover in anthropogenic landscapes to protect species reliant on forested habitats, like howler monkeys.

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.

Inaccurate recording of Mansonella perstans in free-ranging primates outside its endemic area in Brazil?

In the study undertaken by Souza et al. [Primates 64(1):153-159, 2022; https://doi.org/10.1007/s10329-022-01038-5 ], published in the most recent volume of this journal, the blood samples of two Alouatta guariba clamitans (Primates, Atelidae) from two municipalities in the state of Rio Grande do Sul, southern Brazil were reported to be positive for Mansonella perstans. This is the first reported finding of M. perstans in A. guariba clamitans, as well as the first time that M. perstans has been recorded in Brazil outside the Amazon region. We would like to express our concern about this finding, specifically with respect to the geographical distribution of M. perstans in Brazil, as, up until this study, this filaria had only been found in the upper Rio Negro region in São Gabriel da Cachoeira, Amazonas, Brazil. Moreover, species identification was performed using partial sequences of three gene fragments, namely internal transcribed spacer 2, 12S, and 18S, yet neither the phylogenetic trees nor the BLAST alignments of these sequences provided supporting evidence that they belong to M. perstans.

Evaluation of Dental Enamel Thickness in Maxillary Teeth of Alouatta guariba clamitans, Alouatta caraya, and Sapajus nigritus by Cone Beam Computed Tomography.

Tooth enamel thickness is widely studied in primates and is important in differentiating taxa and in interpreting diet and feeding behavior. The objective of this study was to measure enamel thickness and discuss whether the results can be associated with different feeding patterns. Thirty-four syncraniums of Alouatta guariba clamitans, Alouatta caraya, and Sapajus nigritus were subjected to cone beam computed tomographic (CBCT) scans, and the dental enamel was measured in different regions of the crown using the multiplanar reconstruction tool. The differences observed indicate that for many variables and teeth, A. guariba clamitans showed significantly higher values compared to the other 2 species, with the exception of the cuspid region. Although the A. guariba clamitans is a folivorous species, it showed thicker enamel for most of the variables. CBCT was efficient in performing the measurements, allowing analysis of the syncraniums.

Pathological findings associated with Dipetalonema spp. (Spirurida, Onchocercidae) infection in two species of Neotropical monkeys from Brazil.

Among vector-borne helminths, filarioids of the genus Dipetalonema (Spirurida: Onchocercidae) localize in several tissues and body cavities of several animal species, causing mild to moderate lesions. The pathological findings associated with Dipetalonema spp. infection in Neotropical monkeys from southern Brazil are herein described, along with a fatal case due to filarial polyserositis and entrapment of an intestinal segment. At necropsy, nematodes were observed in abdominal and thoracic cavities, or in the pericardium of 37 (31.3%) out of the 118 individuals examined (i.e., 35 Alouatta guariba clamitans and two Sapajus nigritus). In addition, at histology, 27.0% of positive animals presented microfilarie (inside blood vessels of lung, spleen, liver, and brain) and 8.1% presented adult nematodes in the heart, lung, and liver. In two cases, cross-sections of filarioids were associated with areas of epicardial thickening with intense fibrosis and pyogranulomatous inflammation in the brain, heart, liver, lungs, or spleen. The DNA fragment was amplify using the cox1 gene, sequenced and analyzed to identify the nematode species collected; presence of Wolbachia was assessed in the filarioids using the 16S rRNA gene. At BLAST analysis of the cox1 gene, 10 sequences showed 91.7% nucleotide identity with Dipetalonema gracile, and two with D. gracile (98.5%) and Dipetalonema graciliformis (98.3%). Phylogenetic analyses clustered sequences ofthe cox1 obtained in this study in two clades corresponding with the host species. Wolbachia sp. endosymbiont was detected in four samples. Data herein reported provide a description of pathological lesions associated with the infection by Dipetalonema spp., suggesting that they may cause disease in Neotropical monkeys. In addition, a better understanding of diversity and biology of Dipetalonema spp. in South America is needed to assess the impact they may cause in native non-human primates from Brazil.

Detection of Plasmodium simium gametocytes in non-human primates from the Brazilian Atlantic Forest

BackgroundPlasmodium species of non-human primates (NHP) are of great interest because they can naturally infect humans. Plasmodium simium, a parasite restricted to the Brazilian Atlantic Forest, was recently shown to cause a zoonotic outbreak in the state of Rio de Janeiro. The potential of NHP to act as reservoirs of Plasmodium infection presents a challenge for malaria elimination, as NHP will contribute to the persistence of the parasite. The aim of the current study was to identify and quantify gametocytes in NHP naturally-infected by P. simium.MethodsWhole blood samples from 35 NHP were used in quantitative reverse transcription PCR (RT-qPCR) assays targeting 18S rRNA, Pss25 and Pss48/45 malaria parasite transcripts. Absolute quantification was performed in positive samples for 18S rRNA and Pss25 targets. Linear regression was used to compare the quantification cycle (Cq) and the Spearman's rank correlation coefficient was used to assess the correlation between the copy numbers of 18S rRNA and Pss25 transcripts. The number of gametocytes/µL was calculated by applying a conversion factor of 4.17 Pss25 transcript copies per gametocyte.ResultsOverall, 87.5% of the 26 samples, previously diagnosed as P. simium, were positive for 18S rRNA transcript amplification, of which 13 samples (62%) were positive for Pss25 transcript amplification and 7 samples (54%) were also positive for Pss48/45 transcript. A strong positive correlation was identified between the Cq of the 18S rRNA and Pss25 and between the Pss25 and Pss48/45 transcripts. The 18S rRNA and Pss25 transcripts had an average of 1665.88 and 3.07 copies/µL, respectively. A positive correlation was observed between the copy number of Pss25 and 18S rRNA transcripts. Almost all gametocyte carriers exhibited low numbers of gametocytes (< 1/µL), with only one howler monkey having 5.8 gametocytes/µL.ConclusionsFor the first time, a molecular detection of P. simium gametocytes in the blood of naturally-infected brown howler monkeys (Alouatta guariba clamitans) was reported here, providing evidence that they are likely to be infectious and transmit P. simium infection, and, therefore, may act as a reservoir of malaria infection for humans in the Brazilian Atlantic Forest.

New records of Amblyomma ticks parasitizing neotropical primates in Brazil

Amblyomma is an important tick genus for animal and human health, with some species being the vectors of zoonotic pathogens, such as Rickettsia rickettsii, in the Neotropical region. Knowing their hosts may help to understand the distribution of these agents and decrease the occurrence of clinical cases. Primates are intelligent and adaptable animals that can get close to humans in the search for food. So, they may be an important epidemiological link for the spread of these ticks. Beyond that, primates also suffer from these infections, serving as sentinels for different diseases. Thus, the present study aims to report the parasitism by Amblyomma spp. on six species of Neotropical primates from different locations in Brazil. The 337 collected ticks were morphologically identified using stereomicroscopes and taxonomic keys, and six distinct species of ticks were identified. We report here the first record of nymphs of the tick species Amblyomma cajennense sensu stricto on Alouatta belzebul, a male of Amblyomma fuscum on Alouatta guariba clamitans, nymphs of Amblyomma sculptum on Leontopithecus chrysopygus and Callithrix aurita, as well as nymphs of Amblyomma geayi on Saimiri collinsi. Of the 337 tick specimens collected, 256 (75,96%) were nymphs. The importance of primates in the life cycle of these species remains to be elucidated.

Influence of landscape structure on previous exposure to Leptospira spp. and Brucella abortus in free-living neotropical primates from southern Brazil.

The environments in which neotropical primates live have been undergoing an intense fragmentation process, constituting a major threat to the species' survival and causing resource scarcity, social isolation, and difficulty in dispersal, leaving populations increasingly vulnerable. Moreover, the proximity of wild environments to anthropized landscapes can change the dynamics of pathogens and the parasite-host-environment relationship, creating conditions that favor exposure to different pathogens. To investigate the previous exposure of free-living primates in Rio Grande do Sul State (RS), southern Brazil, to the bacterial agents Leptospira spp. and Brucella abortus, we investigated agglutinating antibodies against 23 serovars of Leptospira spp. using the microscopic agglutination test and B. abortus acidified antigen test in primate serum samples; 101 samples from primates captured between 2002 and 2016 in different forest fragments were used: 63 Alouatta caraya, 36 Alouatta guariba clamitans, and 02 Sapajus nigritus cucullatus. In addition, the forest remnants where the primates were sampled were characterized in a multiscale approach in radii ranging from 200 to 1400 m to investigate the potential relationship of previous exposure to the agent with the elements that make up the landscape structure. The serological investigation indicated the presence of antibodies for at least one of the 23 serovars of Leptospira spp. in 36.6% (37/101) of the samples analyzed, with titers ranging from 100 to 1600. The most observed serovars were Panama (17.8%), Ballum (5.9%), Butembo (5.9%), Canicola (5.9%), Hardjo (4.9%), and Tarassovi (3.9%); no samples were seropositive for Brucella abortus. Decreased forest cover and edge density were the landscape factors that had a significant relationship with Leptospira spp. exposure, indicating that habitat fragmentation may influence contact with the pathogen. The data generated in this study demonstrate the importance of understanding how changes in landscape structure affect exposure to pathogenic microorganisms of zoonotic relevance. Hence, improving epidemiological research and understanding primates' ecological role in these settings can help improve environmental surveillance and conservation strategies for primate populations in different landscapes.

Emergence of Mansonella sp. in free-ranging primates in southern Brazil.

Mansonellosis is a neglected and emerging tropical disease. Among all zoonotic filarial diseases, it is probably the most prevalent and least studied, with approximately 114 million people infected. The parasites of Mansonella spp. are among the most common blood parasitemias and are widely found in Africa and Latin America. Through molecular analysis of blood samples from free-ranging primates Sapajus nigritus (n 33) and Alouatta guariba clamitans (n 5) in the southern states of Brazil (Santa Catarina and Rio Grande do Sul), we identified samples positive for Mansonella perstans in two specimens of A. guariba clamitans. A fragment of 578bp from the ITS intergenic region (5.8S-ITS2-28S) was targeted for an initial PCR screening. Subsequently, positive samples were subjected to other PCR assays targeting a fragment of the 12S and the 18S genes. This is the first record of molecular detection of the agent in this host in the Pampa Biome. With a wide distribution across Brazil and Argentina, these primates may represent a potential wild reservoir for the zoonotic agent of mansonellosis. Entomological and transmission studies are essential to avoid the urbanization of mansonellosis and to understand the cycles of agents in different environmental scenarios.

Parasites and Other Infectious Agents in Non-human Primates of Argentina.

In Argentina, there are five non-human primate (NHP) species: Sapajus nigritus cucullatus, Sapajus cay, Alouatta caraya, Alouatta guariba clamitans, and Aotus azarae. All of them inhabit protected and non-protected areas and face severe threats due anthropization. We aim to summarize the information available about parasites and infectious diseases of these NHPs and suggest further research on primate diseases in Argentina. NHPs of Argentina are hosts of several parasites and pathogens important for conservation as well as public health. Alouatta species are lethally susceptible to yellow fever virus, which makes them suitable health sentinels of possible outbreaks. For other primate species, few parasite surveys have been carried out. Assessing the presence of infectious diseases and long-term surveillance on NHP allow the development of strategies to help in the early detection of pathogens that may threat public health. Increasing the knowledge about parasites and infectious diseases and their consequences in NHP of Argentina is needed, considering a One Health approach.

The Influence of Landscape Structure on the Occurrence of Neospora caninum, Toxoplasma gondii, and Sarcocystis spp. in Free-Living Neotropical Primates.

Habitat fragmentation is the main threat to primate survival in the world. Additionally, changes in the environments in which they live can also contribute to exposure to pathogens. To investigate some pathogens that free-living primates may be exposed to in Rio Grande do Sul State (RS; southern Brazil) and characterize the forest remnants in which they live, we investigated anti-Neospora caninum, Toxoplasma gondii, and Sarcocystis spp. antibodies in the serum of the animals. We analyzed 105 serum samples from 63 black howler monkeys (Alouatta caraya), 39 southern brown howler monkeys (Alouatta guariba clamitans), and 03 capuchin monkeys (Sapajus nigritus cucullatus), which were captured in forest fragments of RS. Indirect fluorescence antibody test (IFAT) and indirect hemagglutination assay (IHA) were used to detect antibodies to the agents. We then characterized the landscapes in a multiscale approach in radii from 200 to 1400m to investigate the relationship of the presence of the agents with landscape elements. In the IFAT-IgG, 13.3% (14/105) of the samples were seropositive for N. caninum, 4.8% (5/105) for T. gondii, and 5.7% (6/105) for Sarcocystis spp. In the IHA-IgM/IgG, 24.8% (26/105) were seropositive for T. gondii. The metrics that best explained exposure to agents were edge and patch density, forest cover, urban cover, and average Euclidean distance to the nearest patch. This study indicated that the primates were exposed to the agents studied, demonstrating that some landscape features are associated with exposures to the investigated pathogens.

Rope bridges provide safe connectivity for the southern brown howler monkey (Alouatta guariba clamitans Cabrera, 1940) in an urban Atlantic Forest remnant

Abstract A southern brown howler monkey (Alouatta guariba clamitans) population occurs in a remnant of Atlantic Forest located inside an urban area of the municipality of São Paulo, Brazil. This population has been heavily anthropogenically impacted by collisions with vehicles, electrocutions on power lines, and falls onto roads. With the aim of reducing these impacts on howler monkeys, we installed four rope bridges in the forest canopy in Fontes do Ipiranga State Park (PEFI). We used mortality data collected within the PEFI to identify areas with high incident rates to place the bridges. The bridges were monitored continuously (24 hours per day) with camera traps for the 12 months following bridge installation (with one exception). The goal of this study was to evaluate the functionality of the bridges in road impact mitigation for the howler monkeys in the PEFI and for other arboreal species. We recorded use of three of the four rope bridges by five of the six arboreal mammal species known to occur in the PEFI with the following frequency: southern brown howler monkey – 60.5% of events, 70.8 events/month; orange-spined hairy dwarf porcupine – Coendou spinosus, 26.1% of events, 31 events/month; black-eared opossum – Didelphis aurita, 7.2% of events, 7.3 events/month, bare-tailed woolly opossum – Caluromys philander, 3.4% of events, 4.3 events/month and marmoset – Callithrix sp., 2.7% of events, 3.38 events/month. The time to first use of the bridges by howler monkeys in the two bridges for which there were data was 2 and 77 days, while other species took longer to habituate (113–344 days). Adult howler monkeys used all parts of the bridges to cross while younger howlers and the smaller species used mostly the longitudinal side lines. Given our findings of rope bridge use by five species in the PEFI, we recommend the installation of rope bridges of this design in other areas with similar species composition.

Impacto da urbanização sobre a fauna helmíntica em Alouatta, em 2 reservas biológicas, na região metropolitana de Porto Alegre - RS

The fragmentation of howler monkeys (Alouatta) habitat to make room for the urban environment, allows the spread of zoonotic diseases. The objective of this study was to verify the occurrence of helminth eggs in the feces of Alouatta guariba clamitans in 2 biological reserves located in Porto Alegre - RS. Lami and São Pedro, respectively, presented eggs of gastrointestinal parasites of the superfamilies Strongyloidea; Oxyuroidea, Trichuroidea and Rhabdiasoidea. The results demonstrate that in the more fragmented habitat there is a greater risk of parasitic infection together with multiparasitism, since the samples from the Lami neighborhood showed greater variability of parasites.

Wildlife is imperiled in peri-urban landscapes: threats to arboreal mammals

Urbanization and deforestation impose severe challenges to wildlife, particularly for forest-living vertebrates. Understanding how the peri-urban matrix impacts their survival is critical for designing strategies to promote their conservation. We investigated the threats faced by brown howler monkeys (Alouatta guariba clamitans) in peri-urban regions of Rio Grande do Sul (RS) and Santa Catarina (SC) states, southern Brazil, by compiling negative interaction events (hereafter NIE) reported over more than two decades. We assessed the major NIEs, their distribution among age-sex classes, and the predictors of NIE-related mortality. After 20+ years of monitoring, we compiled 540 NIEs (RS = 248 and SC = 292). Electrocution by power lines was the most frequent cause of death or injury (37%), followed by dog attack (34%), vehicle collision (17%), and human mistreatment (12%). The occurrence of lethal injuries ranged from 5% to 69% depending on the type of NIE and on which state it occurred in. The overall post-NIE mortality was 56%. Adults of both sexes were the most affected individuals in both study regions. The minimal adequate GLM model explained 83% of the variation in NIE-related mortality. State, NIE type, and age-sex class were the main predictors of mortality. Overall, mortality was lower in SC and higher among adult females than in the other classes. We found that the survival of brown howler monkeys in the forest-urban interface is constrained by both the urban infrastructure and the growing interactions with humans and domestic and stray dogs (Canis familiaris). We propose the placement of aerial bridges, road signs and speed bumps in areas of frequent animal crossing, the sterilization of stray dogs, and the sensitization of local inhabitants on the importance of respecting and protecting wildlife to reduce their NIEs with humans and domestic animals in the forest-urban interface.

Linking howler monkey ranging and defecation patterns to primary and secondary seed dispersal.

To define the chances of a dispersed seed to produce a new recruit, it is essential to consider all stages of the dispersal process. Howler monkeys are recognized to have positive impacts on forest regeneration, acting as primary dispersers. Furthermore, dung beetles attracted to their feces protect the seeds against predators, and provide a better microenvironment for germination due to the removal of fecal matter, to seed burial, and/or by reducing the spatial aggregation of seeds in fecal clumps. Despite the recognized positive effects of primary seed dispersal through defecation by howler monkeys for plant recruitment, there are some important aspects of their behavior, such as the habit of defecating in latrines, that remain to be explored. Here, we investigated the fate of Campomanesia xanthocarpa seeds defecated by brown howlers, Alouatta guariba clamitans, and the secondary seed dispersal by dung beetles, considering how this process is affected by the monkey's defecation patterns. We found that brown howler monkeys dispersed seeds from several species away from fruit-feeding trees, partly because defecation under the canopy of such trees was not very frequent. Instead, most defecations were associated with latrines under overnight sleeping trees. Despite a very similar dung beetle community attracted to howler feces in latrines and fruit-feeding sites, seeds were more likely to be buried when deposited in latrines. In addition, C. xanthocarpa seeds showed higher germination and establishment success in latrines, but this positive effect was not due to the presence of fecal matter surrounding seeds. Our results highlight that A. guariba clamitans acts as a legitimate seed disperser of C. xanthocarpa seeds in a preserved context of the Brazilian Atlantic Forest and that defecations in latrines increase the dispersal effectiveness.

Necropsies disclose a low helminth parasite diversity in periurban howler monkeys.

Primate-parasite interactions are often investigated via coprological studies given ethical and conservation restrictions of collecting primate hosts. Yet, these studies are inadequate to recover adult helminths for taxonomic identification and to accurately assess their prevalence, intensity, abundance, and site of infection. Fresh carcasses found in anthropogenic landscapes come as informative and reliable alternatives. In this study, we identified the helminths of brown howler monkeys (Alouatta guariba clamitans) and their sites of infection, and measured their prevalence, intensity, and abundance of infection. We necropsied 18 adult males, 11 adult females, and 7 juvenile males that died in conflicts with the anthropogenic environment (domestic dog attacks, n = 11; electrocutions and road-kills, n = 10 each; unknown, n = 5) in periurban landscapes of southern Brazil between 2013 and 2019. We found three nematodes (Trypanoxyuris minutus, Dipetalonema gracile, and Parabronema bonnei) and one cestode (Bertiella cf. studeri), a diversity estimated to account for a sampling completeness of 99%. Prevalence ranged from 3% for P. bonnei to 100% for T. minutus. Mean abundance ranged from 2 (D. gracile and B. cf. studeri) to 55,116 (T. minutus) and mean intensity of infection ranged from 4 (B. cf. studeri) to 55,116 (T. minutus). Trypanoxyuris minutus sex ratio was strongly male-biased. The intensity of infection with T. minutus was higher in juvenile males and adult females than in adult males. The low parasite diversity and the helminths' mode of transmission are compatible with howlers' arboreality and folivorous-frugivorous diet. The howlers were not infected with soil-transmitted helminth parasites of humans and domestic animals on the ground and probably did not eat invertebrates to complement the diet. Given the lack of evidence of howler health problems, we suggest that the causes of death of the necropsied howlers are the major threats to the long-term conservation of the species at the study periurban landscapes.