Alouatta Pigra Research Articles

The Influence of Loud Calls on Intergroup Spacing Mechanism in Black Howler Monkeys (Alouatta pigra)

Long-distance vocalizations form an integral part of intergroup spacing mechanisms. The decision to approach, retreat, or ignore loud calls of neighboring groups might be influenced by resource availability, location in the home range, presence of fertile females or infants, or differential resource-holding potentials, and can alter intergroup encounter rates. During a 19-mo study (February 2016–August 2017), we examined navigation decisions relative to neighbor’s loud calls for five groups of black howler monkeys (Alouatta pigra) in Palenque National Park, Mexico. Study groups encountered any of their neighbors at a mean rate of one every 3.5 days and the same neighbor at a mean rate of one every 16.7 days, which was significantly more frequent than would be expected based on a simulation model that randomized observed daily paths. These results are consistent with mutual attraction. Based on 368 travel bouts relative to nearby (50–300 m) calls of neighbors, study groups were more likely to approach calls of neighbors than would be expected by chance, but only when neighbors were close by (50–150 m), suggesting that the imminence of threat by opponents played a role. Of the nine social and ecological predictor variables considered, availability of ripe fruits and of flowers was an important driver of their navigation choices and groups were more likely to move toward neighbors’ calls when ripe fruits were scarce and to move away when flowers were abundant. We found no evidence that the presence of fertile females or unweaned infants influenced navigation decisions. Nor did relative competitive abilities of opposing groups, measured as numeric superiority in group size or male group size, affect navigation decisions. This study provides evidence that black howler monkeys incorporate information on resource availability and neighbors’ current locations into their navigation decisions and intergroup spacing patterns.

Spatial aggregation of fruits explains food selection in a neotropical primate (Alouatta pigra)

The availability and spatial distribution of food resources affect animal behavior and survival. Black howler monkeys (Alouatta pigra) have a foraging strategy to balance their nutrient intake that involves mixing their consumption of leaves and fruits. The spatial aggregation of food items should impact this strategy, but how it does so is largely unknown. We quantified how leaf and fruit intake combined (here termed food set selection) was spatially aggregated in patches and how food aggregation varied across seasons. Using variograms we estimated patch diameter and with Generalized Least Square models determined the effect of food spatial aggregation on food selection. Only fruits were structured in patches in the season of highest availability (dry-season). The patches of food set selection had a diameter between 6.9 and 14 m and were explained by those of mature fruit availability which were between 18 and 19 m in diameter. Our results suggest that the spatial pattern of food selection is influenced by patches of large fruit-bearing trees, not by particular species. Fruit also occur along spatial gradients, but these do not explain food selection, suggesting that howlers maximize food intake in response to local aggregation of fruit that are limiting during certain seasons. We demonstrate how the independent spatial modelling of resources and behavior enables the definition of patches and testing their spatial relationship.

Arboreal route navigation in a Neotropical mammal: energetic implications associated with tree monitoring and landscape attributes

BackgroundAlthough navigating along a network of routes might constrain animal movement flexibility, it may be an energetically efficient strategy. Routinely using the same route allows for visually monitoring of food resources, which might reduce the cognitive load and as such facilitate the process of movement decision-making. Similarly, locating routes in areas that avoid costly landscape attributes will enhance their overall energy balance. In this study we determined the benefits of route navigation in an energy minimiser arboreal primate, the black howler monkey (Alouatta pigra).MethodsWe monitored five neighbouring groups of black howler monkeys at Palenque National Park, Mexico from September 2016 through August 2017. We recorded the location of the focal group every 20 m and mapped all travel paths to establish a route network (N = 1528 travel bouts). We constructed linear mixed models to assess the influence of food resource distribution (N = 931 trees) and landscape attributes (slope, elevation and presence of canopy gaps) on the location of routes within a route network.ResultsThe number of food trees that fell within the visual detection distance from the route network was higher (mean: 156.1 ± SD 44.9) than randomly simulated locations (mean: 121.9 ± SD 46.4). Similarly, the number of food trees found within the monkey’s visual range per meter travelled increased, on overage, 0.35 ± SE 0.04 trees/m with increasing use of the route. In addition, route segments used at least twice were more likely to occur with increasing density of food resources and decreasing presence of canopy gaps. Route segments used at least four times were more likely to occur in elevated areas within the home ranges but only under conditions of reduced visual access to food resources.ConclusionsRoute navigation emerged as an efficient movement strategy in a group-living arboreal primate. Highly used route segments potentially increased visual access to food resources while avoiding energetically costly landscape features securing foraging success in a tropical rainforest.

Seed fate and seedling recruitment in monkey latrines in rustic cocoa plantations and rain forest in southern Mexico

AbstractPrimates are important seed dispersers in natural ecosystems and agro-ecosystems, but the latter scenario remains under-studied. The degree to which primates favour plant regeneration greatly depends on post-dispersal processes. The main objective of this study was to compare patterns of seed/seedling fate and seedling recruitment in two habitats of the black howler monkey (Alouatta pigra Lawrence 1933), rustic cocoa and rain forest, and two types of seed-deposition locations, monkey latrines and control locations. Field experiments were carried out within the non-overlapping home ranges of six monkey groups, three in cocoa and three in forest. Seed and seedling fates were assessed for one focal tree species, Brosimum lactescens. The probabilities of seed survival (0.52), germination (0.72), seedling establishment (0.73) and early seedling survival (0.38) were not affected by habitat or seed-deposition location. Late seedling survival was similar in the two habitats but was higher in control locations (0.22) than in latrines (0.09). In cocoa, 4641 seedlings of 59 species were recorded, in forest 3280 seedlings of 68 species. Seedling recruitment was similar in both habitats, but latrines had higher densities than control locations. The importance of agro-ecosystems with low management intensity for the maintenance of ecological processes in anthropogenic landscapes is discussed.

Detection and prevalence of adenoviruses from free-ranging black howler monkeys (Alouatta pigra).

Adenoviruses are important pathogens known to infect vertebrate hosts, including a wide range of primates. Despite its importance, data on the diversity of these viruses in non-human primates living in their natural habitat remain scarce. In this study, we conducted a surveillance of adenoviral infection in wild black howler monkeys from two protected natural areas in Mexico. This was achieved by analyzing 67 fecal samples using a nested PCR that targets the adenovirus DNA polymerase gene. Adenoviral DNA was detected in 12 samples from both study sites, with an overall prevalence of 17.9%. The amplified DNA sequences shared 100% nucleotide identity and phylogenetic analyses revealed that the haplotype detected was novel, and clustered with Platyrrhini mastadenovirus A, which was previously described in captive New World monkeys. Our data, along with the previous evidence, confirm that monkeys native to the Americas are the original hosts of these adenoviruses.

Integrating expert knowledge and ecological niche models to estimate Mexican primates’ distribution

Ecological niche modeling is used to estimate species distributions based on occurrence records and environmental variables, but it seldom includes explicit biotic or historical factors that are important in determining the distribution of species. Expert knowledge can provide additional valuable information regarding ecological or historical attributes of species, but the influence of integrating this information in the modeling process has been poorly explored. Here, we integrated expert knowledge in different stages of the niche modeling process to improve the representation of the actual geographic distributions of Mexican primates (Ateles geoffroyi, Alouatta pigra, and A. palliata mexicana). We designed an elicitation process to acquire information from experts and such information was integrated by an iterative process that consisted of reviews of input data by experts, production of ecological niche models (ENMs), and evaluation of model outputs to provide feedback. We built ENMs using the maximum entropy algorithm along with a dataset of occurrence records gathered from a public source and records provided by the experts. Models without expert knowledge were also built for comparison, and both models, with and without expert knowledge, were evaluated using four validation metrics that provide a measure of accuracy for presence-absence predictions (specificity, sensitivity, kappa, true skill statistic). Integrating expert knowledge to build ENMs produced better results for potential distributions than models without expert knowledge, but a much greater improvement in the transition from potential to realized geographic distributions by reducing overprediction, resulting in better representations of the actual geographic distributions of species. Furthermore, with the combination of niche models and expert knowledge we were able to identify an area of sympatry between A. palliata mexicana and A. pigra. We argue that the inclusion of expert knowledge at different stages in the construction of niche models in an explicit and systematic fashion is a recommended practice as it produces overall positive results for representing realized species distributions.

Effects of anthropogenic stress on the presence of parasites in a threatened population of black howler monkeys (Alouatta pigra)

Habitat disturbance disrupts the ecological interactions of mammals, leading to negative consequences for biodiversity. In particular, it is suggested that parasite-host interactions are affected in tropical ecosystems, with parasite diversity reduced as environmental perturbations take place. In this study, we examined whether the disruption of tropical forests affects the presence of parasites in a population of endangered black howler monkeys (Alouatta pigra) that inhabits a highly fragmented landscape in Balancan, Tabasco, Mexico. Our working hypothesis was that increased forest perturbation would negatively affect the incidence of parasitic infections (parasite presence and richness) in black howler monkeys. We conducted a parasitological study and collected stool samples from 65 adult individuals living in 30 forest fragments across a disturbance gradient. We recovered parasite eggs from stool samples using flotation and sedimentation techniques. We selected fragment size and distance from each forest fragment to the nearest village as measures of forest perturbation. We analyzed the effects of forest perturbation on parasite presence and richness using generalized linear models. Other driving factors such as seasonality, host density, and sex were also considered in the models. Gastrointestinal parasite infection was positively related to distance between forest fragments and the nearest human settlement (β = 0.55 ± SE 0.28, z = 2.0, P = 0.05). No effects of fragment size or any other variable considered in the model on the presence of parasite infection were observed. Parasite richness was not affected by any of the measures of forest perturbation, nor by any other variables considered in the analysis. Our findings suggest that an increase in forest perturbation may negatively affect the probability of parasite infection in black howler monkeys, as individuals living in close proximity to human settlements showed a lower presence of parasites. We proposed that the low parasite infection rates recorded in this monkey population reflect synergistic effects associated with both the alteration of the parasite-primate network, as well as the low resilience of parasites to thrive in a disrupted ecosystem.

Differential fruit choice in two simpatric monkey species and frugivorous bats in southern Mexico

Con el objetivo de examinar el papel que juegan las especies vegetales como fuentes alimenticias en la selección de frutos de agentes dispersores (Alouatta pigra, Ateles geoffroyi y murciélagos frugívoros), se realizó un estudio en selvas secas en el sureste de Yucatán, México. Se registraron los frutos consumidos por murciélagos usando colectores y, en el caso de los monos, se implementó el método de animal focal. El número de frutos consumidos registrados para ambas especies de primates y murciélagos fueron 342 y 386, respectivamente. Se determinó que los murciélagos depositaron frutos con pequeñas cantidades de pulpa, mientras que los monos contribuyeron mayormente con frutos totalmente despulpados (contrastes por pares LSD p < 0.05). Entre la variedad de especies de frutos en la dieta de los primates se detectó que A. pigra eligió frutos de las especies menos abundantes como Enterolobium cyclocarpum Jacq. Griseb. (1860) en vez de aquellas más abundantes (Manilkara zapota (L.) P. Royen (1953) y Brosimum alicastrum Sw. subsp. alicastrum C.C. Berg (1972)). El tipo de manejo de frutos y semillas causado por los primates sería más beneficioso para la germinación de las semillas que los aplicados por los murciélagos. Además, esta elección y manejo del fruto podría depender de sus características y la disponibilidad espacio-temporal de las especies de plantas como fuente de alimento.

The Influence of Leaf Consumption on Time Allocation in Black Howler Monkeys (Alouatta pigra)

The analysis of factors that determine variation in time budgets is important to understand the interactions between environment, behaviour and fitness. We tested the hypothesis that changes in the dietary patterns of black howler monkeys (Alouatta pigra) caused by a decrease in the availability of preferred foods are a main determinant of variation in time budgets. We predicted that individuals would trade off travel time for resting time (i.e., minimize energy expenditure) as the diet included more leaves. We conducted our study in the Mexican state of Campeche between 2005 and 2008, where we studied the behaviour of 28 adult males and 32 adult females belonging to 14 different groups for a total of 3,747.2 focal sampling hours. Study groups lived in forest fragments with variation in habitat quality. Individuals showed different rest:travel trade-offs in response to leaf consumption according to the quality of the forest fragments they lived in. Individuals that lived in high-quality fragments increased resting time under more folivorous regimes, whereas those living in low-quality fragments increased travel time. Our results suggest that howler monkeys living in low-quality fragments spend more time foraging to compensate for the low quality of the available resources.

Alouatta pigra males ignore A. palliata loud calls: A case of failed rival recognition?

When closely related species overlap geographically, selection may favor species-specific mate recognition traits to avoid hybridization costs. Conversely, the need to recognize potential same-sex rivals may select for lower specificity, creating the possibility that selection in one domain constrains evolution in the other. Despite a wealth of data on mate recognition, studies addressing rival recognition between hybridizing species are limited to a few bird species. Using naïve populations, we examine the extent to which failed rival recognition might have affected hybridization patterns when two species of howler monkeys (Alouatta pigra and A. palliata) first met after diverging in allopatry. We simulated first contact between naïve subjects using playback experiments in allopatric populations of the two purebred species. Using linear mixed models, we compared their look, move, and vocal responses to conspecific and heterospecific loud calls. Although not different in overall response strength to playbacks, the two species differed in reaction to heterospecific callers. Male A. pigra ignored calls from male A. palliata, but the reverse was not true. Despite striking differences in vocalizations, A. palliata respond equally to calls from both species whereas A. pigra respond only to conspecifics. This apparent failure of A. pigra males to recognize interspecific rivals might have biased hybridization (F1 hybrids = male A. palliata x female A. pigra), a pattern previously hypothesized based on genetic analysis of hybrids. Given that A. pigra males could be losing reproductive opportunities to heterospecific males, our findings add to growing evidence of potential costs for overly specific species recognition.

Salivary tannin-binding proteins are a pervasive strategy used by the folivorous/frugivorous black howler monkey.

Dietary tannins can affect protein digestion and absorption, be toxic, and influence food selection by being astringent and bitter tasting. Animals that usually ingest tannins may regularly secrete tannin-binding salivary proteins (TBSPs) to counteract the negative effects of tannins or TBSPs production can be induced by a tannin-rich diet. In the wild, many primates regularly eat a diet that contains tannin-rich leaves and unripe fruit and it has been speculated that they have the physiological ability to cope with dietary tannins; however, details of their strategy remains unclear. Our research details the salivary protein composition of wild and zoo-living black howler monkeys (Alouatta pigra) feeding on natural versus manufactured low-tannin diets, and examines differences in TBSPs, mainly proline-rich proteins (PRPs), to determine whether production of these proteins is dependent on the tannin content of their food. We measured the pH, flow rate, and concentration of total protein and trichloroacetic acid soluble proteins (an index of PRPs) in saliva. Howler monkeys produced slightly alkaline saliva that may aid in the binding interaction between tannin and salivary proteins. We used gel electrophoresis to describe the salivary protein profile and this analysis along with a tannin-binding assay allowed us to detect several TBSPs in all individuals. We found no differences in the characteristics of saliva between wild and zoo-living monkeys. Our results suggest that black howler monkeys always secrete TBSPs even when fed on foods low in tannins. This strategy of constantly using this salivary anti-tannin defense enables them to obtain nutrients from plants that sometimes contain high levels of tannins and may help immediately to overcome the astringent sensation of their food allowing howler monkeys to eat tanniferous plants.

Flotation techniques (FLOTAC and mini-FLOTAC) for detecting gastrointestinal parasites in howler monkeys

BackgroundAnalyses of environmental correlates of the composition of gastrointestinal parasite communities in black howler monkeys (Alouatta pigra) have been hindered by inadequate calibration techniques of detection and quantification methods of the parasites. Here we calibrate samples and compare the likelihood of parasite detection using two flotation techniques, FLOTAC and Mini-FLOTAC, and compare flotation solution, preservation method and dilution ratio for egg detection and counts of the most common parasites (Controrchis spp. and Trypanoxyuris spp.) in howler monkeys.ResultsFor samples preserved in 5% formalin, the Mini-FLOTAC technique was the best option for qualitative and quantitative copro-microscopic analysis. This technique displays an 83.3% and 100% detection of Controrchis spp. and Trypanoxyuris spp. infections, respectively. For the trematode Controrchis spp., more eggs per gram of feces (EPG) were recorded with the flotation solution (FS) #7 (zinc sulfate; specific gravity SG = 1.35) at 1:20 and 1:25 dilution than other methods. By contrast, for the nematode Trypanoxyuris spp., the best results were recorded with FS1 (sucrose and formaldehyde; SG = 1.20) at 1:10 dilution.ConclusionsWe recommend the Mini-FLOTAC technique for general use with parasite analysis on frugivore/folivores like the howler monkey, especially if many samples are analyzed. The technique has a high detection rate and the best EPG counts, allowing the qualitative and quantitative analysis of parasite load among the species or populations without the need for specialized equipment.

Through the eyes of children: Drawings as an evaluation tool for children's understanding about endangered Mexican primates.

This study seeks to understand children's perceptions and knowledge of endangered Mexican primates. The black howler monkey (Alouatta pigra) is a charismatic species endemic to Southern Mexico, Northern Belize, and Guatemala and is a symbol of the region that fosters a sense of local pride. Therefore, it can be considered a flagship species for the forests of Southern Mexico. We evaluated the perception and knowledge that 297 Mexican elementary school children (8-10 years old) have about black howler monkeys. Specifically, we analyzed and categorized drawings made by these children based on gender, geographic context (rural or urban), and residence within or outside of Protected Areas (PAs). Student drawings were categorized into three levels of knowledge (no familiarity, basic knowledge, and sophisticated knowledge). Common misconceptions and important landscape elements for black howler conservation were gathered from these visual representations. Children were largely unfamiliar with black howlers, despite sharing the same geographical location. Knowledge was affected by context and residence, with students living within PAs more aware of black howlers than students living outside of PAs. However, overall the children showed a deep understanding of the current forest conservation situation in Southern Mexico; meaning they could be presenting a shifting baseline syndrome. The study highlights the value of assessing children's drawings as a tool that can be used to help policy makers and educational practitioners in fine-tuning educational, environmental, and marketing programs. More importantly, it is a methodology that can be applied in future research for understanding children's perceptions and knowledge about endangered species and environmental change in deciding how to improve the effectiveness of conservation messaging.

Maternal glucocorticoid levels affect sex allocation in black howler monkeys

AbstractWhen sons and daughters impart different fitness benefits, mothers should bias investment according to offspring sex, in some cases modifying offspring sex ratios. Sex allocation in monotocous organisms is expected to be costlier than for polytocous species, as it imposes a greater loss of reproductive effort in terms of mating and fertilization. Here, we show that variation in glucocorticoid concentrations around the time of conception predicts infant sex in a monotocous anthropoid, the black howler monkey (Alouatta pigra), suggesting that sex allocation is linked to a hormonal mechanism that affects early embryonic development. Glucocorticoids signal environmental conditions, and in our study, their variation was positively related to factors affecting infant survival. These results offer insight into sex allocation strategies in monotocous organisms.

Assessment of releases of translocated and rehabilitated Yucatán black howler monkeys (Alouatta pigra) in Belize to determine factors influencing survivorship.

Rehabilitation and reintroduction have become important to the management and welfare of primates worldwide. However, the suitability and success of these practices must be evaluated to determine their effectiveness as well as to improve programs and methods, as little is known about the factors influencing survival of released individuals. Between 2011 and 2014, 28 howler monkeys, Alouatta pigra, were released at Fireburn Reserve, northern Belize by the Primate Rehabilitation Centre of Belize: Wildtracks. From March to August 2015, field trips were made to determine the number and identity of surviving individuals to assess whether differences in individual outcomes (survived or disappeared) could be associated with specific characteristics or backgrounds of the monkeys. Fourteen of the twenty rehabilitated monkeys and seven of the eight translocated monkeys were found alive. The proportion of surviving individuals was not significantly different between rehabilitants and translocated animals, males and females, former pets and wild animals, short- and long-term rehabilitants, or different ages at release or intake. As mortality was low and none of the general factors analyzed influenced survivorship, it is suggested that chance or individual traits may be important in the outcomes of releases. This study provides an example of successful population reintroduction from both rehabilitation and translocation programs, and the first analyses of characteristics impacting the success of releases of howler monkeys.

Biochemical and hematological evaluations of black howler monkeys (Alouatta pigra) in highly degraded landscapes in Mexico.

Loss and fragmentation of Neotropical primates' habitat can alter the health and individual adaptation. Physiological parameters reflect health status and individuals responses to the habitat conditions. We captured six wild adult females and six adult males of Alouatta pigra to evaluate their physical condition (body mass, respiratory and heart rate, and rectal temperature), hematology and blood chemistry on fragmentation habitat condition at southeastern Mexico. The males weighed more than females, but the female' temperature, respiratory rate, and heart rate were higher. Low values of hemoglobin, hematocrit, and red blood cells suggest some degree of anemia in these howler monkeys. Low levels of the total protein, albumin, albumin/globulin Ratio, and low levels of blood urea nitrogen suggest that howler monkeys could have protein and carbohydrate deficiencies. Howler monkeys living under the highly degraded conditions at Balancán, Tabasco, could be showing adaptability by modifying their physiology, hematology, and blood chemistry in response to the conditions of their fragmented landscape.

The relative effects of reproductive condition, stress, and seasonality on patterns of parasitism in wild female black howler monkeys (Alouatta pigra).

Parasitic infections in wildlife are shaped by host-related traits including individual reproductive condition. It has been argued that female primates are more susceptible to infectious diseases during pregnancy due to short-term changes in immune function that result in reduced ability to combat infections. Likewise, lactation, which is the most energetically expensive state, may affect immunity and infection risk due to tradeoffs between milk production and maintenance of immune function. Here, we examine the degree to which parasite prevalence and parasite richness are affected by female reproductive condition and stress levels in wild female black howler monkeys (Alouatta pigra). Over the course of one year, we collected fresh fecal samples from 15 adult females belonging to seven black howler groups living in Escárcega, Mexico. Fecal samples were used for parasitological analysis and for measuring fecal glucocorticoid metabolites (i.e., stress biomarker). We found that the prevalence of intestinal parasites and parasite richness did not differ among non-pregnant, pregnant, and lactating females. Fecal glucocorticoid metabolite levels increased significantly during pregnancy and during the first month of lactation, and positively predicted the probability of Controrchis biliophilus infection. Parasite prevalence and richness decreased during the months of increased rainfall. We conclude that reproductive physiology has limited consequences on intestinal parasitic infection risk in female black howler monkeys and that seasonal environmental fluctuations have greater effects.

Patterns in Gut Microbiota Similarity Associated with Degree of Sociality among Sex Classes of a Neotropical Primate.

Studies of human and domestic animal models indicate that related individuals and those that spend the most time in physical contact typically have more similar gut microbial communities. However, few studies have examined these factors in wild mammals where complex social dynamics and a variety of interacting environmental factors may impact the patterns observed in controlled systems. Here, we explore the effect of host kinship and time spent in social contact on the gut microbiota of wild, black howler monkeys (Alouatta pigra). Our results indicate that closely related individuals had less similar gut microbial communities than non-related individuals. However, the effect was small. In contrast, as previously reported in baboons and chimpanzees, individuals that spent more time in contact (0m) and close proximity (0-1m) had more similar gut microbial communities. This pattern was driven by adult female-adult female dyads, which generally spend more time in social contact than adult male-adult male dyads or adult male-adult female dyads. Relative abundances of individual microbial genera such as Bacteroides, Clostridium, and Streptococcus were also more similar in individuals that spent more time in contact or close proximity. Overall, our data suggest that even in arboreal primates that live in small social groups and spend a relatively low proportion of their time in physical contact, social interactions are associated with variation in gut microbiota composition. Additionally, these results demonstrate that within a given host species, subgroups of individuals may interact with the gut microbiota differently.

Vocal repertoire of free-ranging black howler monkeys' (Alouatta pigra): Call types, contexts, and sex-related contributions.

Alouatta species utter the most powerful primate vocalizations in the Neotropics and are well-known for their loud and long-lasting male howling bouts. However, the diversity of acoustic structures used in these howling bouts, as well as in non-howling contexts, and the relative contribution of the different group members to the entire vocal repertoire, needed to be explored further. This report provides the first detailed description of the vocal repertoire of black howler monkeys (Alouatta pigra), focusing on acoustic structures and contexts of emission of both loud and soft calls as well as on the contribution rate of males and females to the different call types. Three free-ranging social groups of black howler monkeys living in Palenque National Park, Mexico were monitored. We identified twelve acoustically discriminable call types, eight described previously and four described here for the first time. A few call types were systematically emitted either isolated or during howling bouts, but most of them could be heard in both calling contexts. Three call types were emitted only by females and two only by males. Adult males' call rates (for the seven shared call types) were higher than those of females but only when considering calls emitted within howling bouts. Our contextual analysis enabled us to divide call types into potential functional categories, according to their degree of contribution, to intra-group versus inter-group interactions and to neutral-positive versus negative situations. We then discussed how socio-ecological factors, notably sex differences in social behaviors, may explain the variability found in the vocal repertoire of this species and compared our findings with the literature on other primate species.

Metabolomic data suggest regulation of black howler monkey (Alouatta pigra) diet composition at the molecular level.

In addition to macronutrients, foods consist of a complex set of chemical compounds that can influence dietary selectivity and consumer physiology. Metabolomics allow us to describe this complexity by quantifying all small molecules, or metabolites, in a food item. In this study we use GC-MS based metabolomics to describe the metabolite profiles of foods consumed by one population of Mexican black howler monkeys (Alouatta pigra) over a 10-month period. Our data indicate that each food exhibited a distinct metabolite profile, and the average weekly intake of metabolites such as neochlorogenic acid and serotonin (5-hydroxytryptamine) was correlated with the consumption of certain plant parts. We speculate that these patterns result in temporal changes in howler monkey physiology such as food retention time. In contrast, variation in the weekly intake of metabolites such as oxalic acid was 70% less than variation in the concentration of the same metabolites across food items, suggesting that howler monkeys regulated the intake of these metabolites, possibly to avoid physiological consequences such as kidney stone formation. Finally, seasonal variation in the consumption of individual nutrient and non-nutrient metabolites were correlated with changes in the relative abundances of associated gut microbial taxa, implying indirect effects of food item metabolites on howler monkey nutritional ecology that likely drive foraging decisions. While additional research is needed to validate these findings, the patterns we report serve as important baseline data for understanding the effects of plant metabolites on the food choice in primates.