Alouatta Research Articles

Noise intensity modulates the responses of mantled howler monkeys to anthropophony.

Anthropogenic noise is a major global pollutant but its effects on primates are poorly understood, limiting our ability to develop mitigation actions that favor their welfare and conservation. In this study, we used an experimental approach to determine the impact of variation in noise intensity on mantled howler monkeys (Alouatta palliata). We conducted the study at Los Tuxtlas (México), where we studied the physiological stress (proxied via fecal glucocorticoid metabolites, fGCM) and behavioral responses of 16 males. We played back chainsaw noise at two intensities (40 and 80 dB) and used days in which groups were not exposed to noise as matched controls. With increased noise intensity fGCM increased, vigilance and vocalizations were longer, and vigilance, vocalizations, and flight occurred quicker. Physiological and behavioral responses occurred even after low-intensity noise playbacks (i.e., 40 dB). Therefore, noise intensity is a significant factor explaining the responses of mantled howler monkeys to anthropogenic noise. These results imply that management actions aimed at eradicating anthropogenic noise are required for the conservation and welfare of mantled howler monkeys at Los Tuxtlas.

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.

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.

Primate richness and abundance is driven by both forest structure and conservation scenario in Costa Rica.

Variation in tropical forest management directly affects biodiversity and provisioning of ecosystem services on a global scale, thus it is necessary to compare forests under different conservation approaches such as protected areas, payments for ecosystem services programs (PES), and ecotourism, as well as forests lacking any formal conservation plan. To examine the effectiveness of specific conservation approaches, we examined differences in forest structure and tree recruitment, including canopy cover; canopy height; seedling, sapling, and adult tree density; and average and total diameter at breast height (DBH) across 78 plots in 18 forests across Costa Rica representing protected areas, private forests utilizing PES and/or ecotourism, and private forests not utilizing these economic incentives. The effectiveness of conservation approaches in providing suitable primate habitat was assessed by conducting broad primate census surveys across a subset of eight forests to determine species richness and group encounter rate of three primate species: mantled howler monkey (Alouatta palliata), Central American spider monkey (Ateles geoffroyi), and the white-faced capuchin monkey (Cebus imitator). Only canopy height was significantly different across the three approaches, with protected areas conserving the tallest and likely oldest forests. Canopy height was also significantly associated with the group encounter rate for both mantled howler and spider monkeys, but not for capuchins. Total group encounter rate for all three monkey species combined was higher in incentivized forests than in protected areas, with capuchin and howler monkey group encounter rates driving the trend. Group encounter rate for spider monkeys was higher in protected areas than in incentivized forests. Incentivized conservation (PES and ecotourism) and protected areas are paragons of land management practices that can lead to variation in forest structure across a landscape, which not only protect primate communities, but support the dietary ecologies of sympatric primate species.

Differences in mammal communities between forest fragments and restoration areas in the Atlantic Forest

AbstractThe persistence of larger mammals in fragmented forest landscapes depends not only on the protection of remaining habitats but also on ecological restoration sites. It is known that the landscape context is an important predictor of species persistence, abundance and distribution. Here we evaluate how landscape characteristics influence the recovery of larger mammals in ecological restoration sites. We assess the richness and composition of mammals in forest fragments and restoration sites using landscape metrics such as forest cover and connectivity. Forest fragments and restoration sites present the same richness (n = 26), but differ in species composition. Some seed‐dispersing mammals were absent in restoration areas, such as Alouatta guariba (brown howler monkey) and Coendou spinosus (paraguayan hairy dwarf porcupine). The percentage of forest cover in the landscape was responsible for 29.09% of the variation in species composition between the evaluated forest formations, exerting a positive or negative influence depending on the species requirements. The results demonstrate the importance of considering not only landscape metrics in an ecological restoration plan, but also the historical landscape context, such as the fauna composition before the disturbance and how these species respond to environmental changes, thus improving the success of future ecological restoration measurements and policies.

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).

Influence of Weather Conditions on Sleeping Patterns and Selection of Foliage Cover of Sleeping Trees in Black-and-Gold, Howler Monkeys (Alouatta caraya) in Northern Argentina

Influence of Weather Conditions on Sleeping Patterns and Selection of Foliage Cover of Sleeping Trees in Black-and-Gold, Howler Monkeys (Alouatta caraya) in Northern Argentina

The rep-handed howling monkey in the state of Pernambuco, north-east Brazil

No abstract

Differences in sperm morphology between Alouatta palliata and Alouatta pigra are consistent with the intensity of sperm competition in each species.

The intensity of sperm competition, in which sperm compete within the female reproductive tract to reach and fertilize her eggs, varies in species with different mating systems. Sperm competition is more intense in species where males cannot monopolize access to reproductive females and females mate with multiple males. In this scenario, a morphological change that increases the ability of sperm to reach and fertilize eggs should rapidly spread in the population, leading to sperm morphological differences between closely related species. Differences in sperm morphology have been reported among primate species with different mating systems. However, due to the inherent logistical and ethical difficulties to sample sperm from wild primates, the extent of variation in sperm morphology within species and among closely related species remains understudied. Here, we compared sperm morphological traits from two sister howler monkey species (Alouatta palliata and Alouatta pigra) that have different mating systems to investigate the effect of sperm competition on sperm morphological traits. We predicted that sperm from A. palliata, where females have more opportunities to mate with multiple males, would show differences in traits associated with increase sperm competitiveness compared to A. pigra where females mostly mate with the central male. We used linear mixed models to determine species differences in sperm morphology, controlling for individual variation. We found that midpieces and heads in A. palliata sperm were on average 26.2% and 11.0% longer, respectively, than those of A. pigra. Differences in these traits are important for sperm speed and hydrodynamic movement in other species and can affect fertilization success. This study provides empirical evidence of sperm morphological traits that evolved through sexual selection in sister primate species with different mating systems.

Serosurvey of Trypanosomatidae (Trypanosoma cruzi and Leishmania infantum) in Howler Monkeys from Southern Brazil: Risk Factor and Influence of Landscape Structure

Serosurvey of Trypanosomatidae (Trypanosoma cruzi and Leishmania infantum) in Howler Monkeys from Southern Brazil: Risk Factor and Influence of Landscape Structure

Behavioral responses of mantled howler monkeys to neighbor long-distance vocalizations.

Long-distance vocalizations are used by primates in a variety of contexts and may have different functions. The long-distance vocalizations of howler monkeys (Alouatta spp.) underlie the spatial regulation of neighboring groups and could be associated with the defense of food resources. Here, we test the hypothesis that the behavioral responses of mantled howler monkeys (A. palliata) to neighbor long-distance vocalizations are influenced by the potential for range defensibility while accounting for location within the home range and food availability. We studied two groups for 13 months and a total of 888 h at La Flor de Catemaco (Mexico). Group 1 had a 92-ha home range and Group 2 had a 24-ha home range. We recorded vocalizations (N = 178 calls) and movements (N = 74 movements) of focal groups following long-distance vocalizations produced by their neighbors. Movement responses, but not vocal responses, were predicted by range defensibility, location, and food availability. As predicted, the group living in the smaller and more defendable range showed stronger movement responses than the group in the larger home range. These movement responses had a shorter latency and longer duration in more valuable spatial and temporal contexts (i.e., the core area and during periods of low food availability). These results suggest that the tradeoff between the costs and benefits of range defense varies according to the interactions between home range size and both the spatial (core areas) and temporal (food availability) abundance of resources. Thus, the responses of mantled howler monkeys to neighbor long-distance vocalizations could be related to home range defensibility.

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.

Assessment of black and gold howler monkey (&lt;i&gt;Alouatta caraya&lt;/i&gt;, Humboldt, 1812) populations in two new study sites in northeastern Argentina

&#x0D; &#x0D; &#x0D; Alouatta caraya has the southernmost distribution of the howler monkeys. While information about most populations remains limited, the forests this species inhabits are being altered continuously. We present data about populations of A. caraya from two new study sites in northeastern Argentina: the “Laguna Oca” Biosphere Reserve (RLO) (26°14'S, 58°10'W), and the “Las Lomas” Private Reserve (RLL) (27°23'S, 58°22'W). We conducted censuses along roads within forest patches in both areas to find groups of A. caraya, counting all visible individuals, and classifying them by sex and age. We found only mixed sex groups in both areas, with a density of 1.12 individuals/ha in RLO and 2.05 individuals/ ha in RLL. At other study sites in Argentina, A. caraya population densities vary from 0.11 to 3.25 individuals/ha, where forest continuity may be important in determining densities. Maintaining long-term study sites of A. caraya across different habitats will allow comparative analyses to explore the underlying mechanisms of behavioral, ecological, and demographic variability.&#x0D; &#x0D; &#x0D;

Comparing diet, seed size and richness in fruit ingested by red howler monkeys (&lt;i&gt;Alouatta juara&lt;i&gt;&lt;/i&gt;&lt;/i&gt;) in two habitat types in Central Amazonia

&#x0D; &#x0D; &#x0D; Primates within the Alouatta genus (howler monkeys) inhabit a wide range of environments due to their flexible folivorous-frugivorous diet. However, the feeding ecology of Alouatta species that inhabit continuous and difficult-to-access forest environments, such as the Amazon, is poorly known. In this study, we compared diet composition, seed size, and richness of fruits ingested by Juruá red howler monkeys (Alouatta juara) in white-water flooded forest and upland for- est. Our analysis was based on 47 stomachs donated by subsistence hunters of central Amazonia in Brazil. We found no difference in the proportion of structural parts, reproductive parts, and animal matter (arthropods) ingested between these environments. However, we found a positive relationship between the richness of ingested seeds and the water level for the white-water flooded forest. This correlation was not observed for upland forest, where other environmental factors such as precipitation may influence tree phenology. The stomach analysis revealed a high diversity of seeds and a substantial percentage of whole seeds (73%) in the red-howler monkeys’ stomachs. This suggests that they have the potential to be effective seed dispersers for at least 40 taxa in the white-water flooded forest and 14 in the upland forest. The population decline or extinction of this species could have an impact on seed dispersal services, particularly for plant species with seeds larger than 20 mm of diameter, as the number of dispersing agents tends to be limited. Further studies are needed to investigate the environmental dynamics involved in the feeding ecology of red howler monkeys. These studies would help to understand the ecological impacts of local subsistence hunting and wild meat trading on seed dispersal, as well as the economic implications for human populations.&#x0D; &#x0D; &#x0D;

Pairing a user-friendly machine-learning animal sound detector with passive acoustic surveys for occupancy modeling of an endangered primate.

Population declines and range contractions due to habitat loss are pervasive among nonhuman primates, with 60% of species threatened with extinction. However, the extensive vocal activity displayed by many primates makes them excellent candidates for passive acoustic surveys. Passive acoustic survey data is increasingly being used to support occupancy models, which have proven to be an efficient means of estimating both population trends and distributions. Passive acoustic surveys can be conducted relatively quickly and at broad scales, but efficient audio data processing has long proven elusive. The machine learning algorithm BirdNET was originally developed for birds but was recently expanded to include nonavian taxa. We demonstrate that BirdNET can accurately and efficiently identify an endangered primate, the Yucatán black howler monkey (Alouatta pigra), by sound in passive acoustic survey data (collected in southeastern Chiapas, Mexico), enabling us to use a single-season occupancy model to inform further survey efforts. Importantly, we also generated data on up to 286 co-occurring bird species, demonstrating the value of integrated animal sound classification tools for biodiversity surveys. BirdNET is freely available, requires no computer science expertise to use, and can readily be expanded to include more species (e.g., its species list recently tripled to >3000), suggesting that passive acoustic surveys, and thus occupancy modeling, for primate conservation could rapidly become much more accessible. Importantly, the long history of bioacoustics in primate research has yielded a wealth of information about their vocal behavior, which can facilitate appropriate survey design and data interpretation.

Cuterebra baeri Infecting Grey-Legged Night Monkeys (Aotus griseimembra) and Red Howler Monkeys (Alouatta seniculus) in Colombia.

Myiases are parasitic infections caused by the larval stages of some fly species. In American nonhuman primates (NHP), three bot fly species causing cutaneous myiasis have been reported: Cuterebra baeri, Cochliomyia hominivorax, and Dermatobia hominis. Studies on myiasis in NHP are scarce and mainly based on morphologic identification of larvae, while molecular approaches have been barely used. This study aimed to molecularly identify bot flies parasitizing two NHP species living sympatrically in central Colombia. Bot fly larvae were collected from two grey-legged night monkeys (Aotus griseimembra) and from a howler monkey (Alouatta seniculus). Larvae were measured and photographed for morphologic evaluation; subsequent molecular characterizations of a partial region of the cytochrome c oxidase subunit 1 mitochondrial gene were performed. Sequence analysis allowed the identification of all specimens as Cuterebra baeri, enabling confirmation of this species parasitizing Alouatta seniculus and Aotus griseimembra in Colombia.

Dog barks influence the physiological stress and behavior of a wild primate

Non-lethal impacts of dogs on primates have seldom been assessed. We used an experimental approach to determine if mantled howler monkeys (Alouatta palliata) perceive dog barks as an aversive stimulus and thus display physiological and behavioral responses toward simulated barks. For one year (1754 h of observations) we studied 16 adult males belonging to five groups in Los Tuxtlas (Mexico), and recorded the occurrence of naturally occurring dog barks, their sound pressure level (SPL), and the behavioral responses of howler monkeys to barks. We then exposed males to bark playbacks at two SPL treatments, 40 and 80 dB in a total of 50 experiments. We assayed glucocorticoid metabolite concentrations in fecal samples (fGCM) as a marker of the physiological stress response of males. We also recorded the duration of vigilance, vocalizations, and flight in relation to playbacks. Naturally occurring barks were frequent and usually elicited behavioral responses by males. fGCM concentrations increased after bark playbacks and with stimuli intensity. Time spent vigilant increased following playbacks independently of stimuli intensity but both vocalizations and flight were linked to stimuli intensity: vocalizations were the longest after barks played-back at 80 dB, but males spent more time fleeing in response to 40 dB bark playbacks. These results provide evidence that dog barks are pervasive in the habitat of mantled howler monkeys living at Los Tuxtlas and disturb males, both physiologically and behaviorally. Although the potential costs of physiological and behavioral responses could not be determined, there is sufficient evidence to assume that they do have negative impacts on individuals. Therefore, our study provides avenues for future research on dog-wildlife interactions and valuable information for the design of conservation actions aimed at mitigating the impact of dogs on mantled howler monkeys.

Hematological and serum biochemistry evaluation in howler monkeys (Alouatta caraya) and capuchin monkeys (Sapajus apella): A comparative study.

Evaluation of blood parameters in captive non-human primates (NHPs) is crucial for monitoring their health and ensuring that their environment meets their physiological requirements. We performed hemogram, serum biochemistry, and parasitological exams in 20 howler monkeys and 21 capuchin monkeys. In both species, over 50% of the individuals presented at least one parasite. There was a negative effect of age on red blood cell (RBC), white blood cell, platelets, total protein, globulin, and alkaline phosphatase, and a positive effect on the A:G ratio, gamma-glutamyl transferase, and mean platelet volume (MPV). Capuchin monkeys presented the highest platelets and alanine aminotransferase (ALT) values and howler monkeys presented the highest MPV, aspartate aminotransferase, ALT, amylase, glucose, bilirubin, and triglycerides values. We observed an interaction between species and sex on RBC, Htc, mean corpuscular hemoglobin concentration, and cholesterol. Species differences found in blood parameters may reflect differences in physiological adaptations associated with ecological and morphological traits and are clinically relevant for evaluating animal health and the suitability of breeding programs.

Potential opportunistic behavior of crab-eating fox Cerdocyon thous (Carnivora, Canidae) in Itapuã State Park, RS, Brazil: possible cases of necrophagy

Abstract In this study we document two records related to potential food opportunism in crab-eating fox, Cerdocyon thous. The records were made in Itapuã State Park, Viamão, RS, Brazil, and were obtained through camera traps. These showed individuals of C. thous carrying a brown howler monkey and an unidentified fish, both already lifeless. There are no records of howler monkey consumption by this species of carnivore, and fish are considered as unusual taxa in its diet. We assume that the captures occurred with the animals already dead, illustrating the food opportunism of the species and the potential occurrence of scavenging by this canid.