Polymerase Chain Reaction (PCR) is a Useful and Low-Cost Tool for Molecular Sexing Psittaciformes under Human Care: An Example of a Collaborative Approach in Mexico.

Sex determination in monomorphic birds is a precondition for captive breeding programs and management and conservation strategies for threatened species. Most species of the order Psittaciformes often present complications since these birds lack external sexual phenotypic traits, making it impossible to differentiate males and females. In the present study, we used molecular techniques to determine the sex of 31 individuals belonging to nine species of the order Psittaciformes kept under human care at the Akumal Monkey Sanctuary & Rescued Animals in Quintana Roo, Mexico. This is a useful and low-cost methodology based on the analysis of the conserved region of the CHD1 gene, which was amplified by PCR with two sets of primers: P8/P2 and 2550F/2718 R. All individuals were successfully sexed with the first set of primers, while only 28 out of 31 samples (90%) could be amplified with the second set. Out of the 31 individuals analyzed, fifteen are female, and seventeen are male. This information represents a handy tool for adequately managing birds under human care, resulting in their reproduction and eventual reintegration into their natural habitat.

A simple assay for measuring tannin-protein precipitation capacity offers insights into the diet and food choice of black howler monkeys (Alouatta pigra).

Phenolics, like tannins, are plant-specialized metabolites that play a protective role against herbivory. Tannins can reduce palatability and bind with proteins to reduce digestibility, acting as deterrents to feeding and impacting nutrient extraction by herbivores. Some assays measure tannin and total phenolics content in plants but lack determination of their biological effects, hindering the interpretation of tannin function in herbivory and its impacts on animal behavior and ecology. In this study, we successfully applied the radial diffusion assay to assess tannin protein precipitation (PP) capacity and evaluate the anti-nutritional effects of tannins in food plants (n = 24) consumed by free-ranging black howler monkeys (Alouatta pigra) in Tabasco, Mexico. We found PP rings in five plant species consumed by the monkeys. The mature fruit of Inga edulis was the most consumed food plant, despite having a high tannin PP capacity (56.66 mg tannic acid equivalent/g dry matter). These findings highlight the presence of tannins in the black howler diet and provide insight into the primates' resilience and potential strategies for coping with anti-nutritional aspects of the diet.

Lead exposure and its relationship with fecal cortisol levels in black howler monkeys (Alouatta pigra).

Efficiently detecting early environmental threats to wildlife is vital for conservation. Beyond obvious dangers like habitat loss or deforestation, our study focuses on one of the most hazardous toxic metals for wildlife: lead (Pb). Pb is a widespread, cumulative, and insidious environmental pollutant that can trigger a wide range of physiological, biochemical, and behavioral disorders. In fact, Pb can cause permanent dysfunction of the major stress system, the hypothalamic pituitary adrenal (HPA) axis. We analyzed Pb and cortisol concentrations in fecal samples from Alouatta pigra in southern Mexico. Fecal samples were collected across six sites categorized as free-ranging (n = 65; conserved and disturbed) and from captive animals (n = 58). Additionally, we collected soil samples (n = 35). We found that Pb was present in 28% of fecal samples and 83% of soil samples. There was a positive relation between fecal and soil Pb levels, and fecal Pb concentration was negatively associated with cortisol levels. However, the claim of Pb being a direct interference with HPA axis requires further investigation. Given our findings, assessing wildlife exposure can be a valuable tool for understanding potential Pb exposure levels in the environment and its possible implications for human health. It can also serve as an early warning system of these consequences.

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.

The Primate Cultural Significance Index: applications with Popoluca Indigenous people at Los Tuxtlas Biosphere Reserve.

BACKGROUND: The study of the cultural significance (CS) of biodiversity provides key information to develop conservation strategies consistent with traditions and perceptions of human communities. In Los Tuxtlas Biosphere Reserve (TBR) in Mexico, the mantled howler monkeys (Alouatta palliata mexicana) and the black-handed spider monkeys (Ateles geoffroyi vellerosus) have historically coexisted with Popoluca Indigenous Peoples. This study sought to determine how the presence of a natural protected area (TBR location) and a range of sociodemographic factors (gender, age, origin, language proficiency, education level, religion) relate to the CS held by the Popoluca Indigenous People in relation to these two endangered primate species. METHODS: The first Primate Cultural Significance Index (PCSI) was designed as a composed index of 11 cultural variables (sub-indices) and was applied randomly to a representative size sample of people over 15 years old in two Popolucas communities, one within the TBR (Piedra Labrada = 81 people) and another outside (Los Mangos = 91). U Mann-Whitney tests were used to compare the PCSI between communities and Generalized Linear Models (GLM) to evaluate the sociodemographic factors of participants that influenced the sub-indices in the PCSI. RESULTS: The cultural significance of spider monkeys held by the Popolucas was higher for the community within the TBR than for the community outside, while for howler monkeys it was higher outside. For both primate species across the two communities, the most relevant sub-indices were (1) interest in conservation and (2) touristic significance of primates. Sociodemographic factors of participants influenced nine sub-indices of cultural significance out of the possible 10 sub-indices applied for each primate species. The demographic factors that most influenced each sub-index for both species were location and gender. CONCLUSIONS: The main differences found between communities may be linked to the conservation and sustainable development programs promoted by the reserve, as well as the greater persistence of Popolucan ancestral traditions within the boundaries of the reserve. We recommend that conservation efforts should focus on people less interested about primate conservation (women, non-natives and residents outside the reserve), and turn to the leadership of people more interested (native men who reside inside the reserve).

Salivary proteome of a Neotropical primate: potential roles in host defense and oral food perception.

BACKGROUND: Saliva contains a very complex mixture of proteins for defense against microbiological pathogens and for oral food perception. Howler monkeys are Neotropical primates that can consume a mostly leaf diet. They are well known to thrive in highly disturbed habitats where they may cope with a diversity of dietary challenges and infection risks. We aimed to describe the salivary proteome of howlers to contribute to better understanding of their physiology. METHODS: We analyzed the salivary proteins of wild black howler monkeys (Alouatta pigra), by SDS-PAGE-1-D and Nano LC-MS/MS and categorized them by their function involved in host defense and oral food perception. RESULTS: Our proteomic analysis identified 156 proteins in howler saliva including a number of host defense peptides that are the first line of defense in mammals, such as defensin, cathelicidin, dermcidin, and lactotransferrin, and proteins with anti-bacterial, anti-fungal, and anti-viral capacity, such as IgA, IgG, IgM, BPI, salivary heat shock 70 kDa protein, beta-2-microbulin, and protein S-100. We also identified key proteins necessary for taste perception, including salivary carbonic anhydrase VI, cystatin D, IgA, and fatty acid-binding protein. Proteins to detect astringent foods were identifying, including four members of cystatins (A, B, C and D), lactoperoxidase, and histidine-rich proteins. No chitinase and amylase were identified as would be expected because howlers do not eat insects and little starch. These findings provide basic information to future studies in oral biology, ingestive physiology, and physiological ecology of mammals and non-human primates.

Primates Can Be a Rallying Symbol to Promote Tropical Forest Restoration.

With 60% of all primate species now threatened with extinction and many species only persisting in small populations in forest fragments, conservation action is urgently needed. But what type of action? Here we argue that restoration of primate habitat will be an essential component of strategies aimed at conserving primates and preventing the extinctions that may occur before the end of the century and propose that primates can act as flagship species for restoration efforts. To do this we gathered a team of academics from around the world with experience in restoration so that we could provide examples of why primate restoration ecology is needed, outline how primates can act as flagship species for restoration efforts of tropical forest, review what little is known about how primate populations respond to restoration efforts, and make specific recommendations of the next steps needed to make restoration of primate populations successful. We set four priorities: (1) academics must effectively communicate both the value of primates and the need for restoration; (2) more research is needed on how primates contribute to forest restoration; (3) more effort must be put into Masters and PhD level training for tropical country nationals; and finally (4) more emphasis is needed to monitor the responses of regenerating forest and primate populations where restoration efforts are initiated. We are optimistic that populations of many threatened species can recover, and extinctions can be prevented, but only if concerted large-scale efforts are made soon and if these efforts include primate habitat restoration.

Evidence-based conservation education in Mexican communities: Connecting arts and science.

Several studies suggest that 63% of primate species are currently threatened due to deforestation, pet-trade, and bushmeat hunting. Successful primate conservation strategies require effective educational programs capable of enhancing critical system-thinking and responsible behavior towards these species. Arts-based conservation education can simultaneously foster cognitive and emotional processes. In this paper, we evaluate an arts-based educational program focused on the conservation of black howler monkeys (Alouatta pigra). Our goals were to determine (1) whether children's knowledge changed with our educational techniques, (2) if there was a particular educational technique that better improved the children's learning, and (3) the children's emotional feedback regarding the whole program. A total of 229 children from communities located in primate-habitat areas, both inside and outside protected areas, participated in the study. Different educational techniques were tested (storytelling, theater and shadow puppets), contrasted with a control group, and evaluated through an analysis of drawings. Our results showed that children's knowledge increase with each art-based technique, with storytelling being the most effective for children's learning. Specific drawings indicators also revealed the increase of children's knowledge and a decrease of misconceptions between pre and post evaluations. Finally, a satisfaction survey about the program showed a high positive feedback. The study highlights the value of designing multidisciplinary projects, where arts-based education program (grounded in scientific information) has shown to be a successful way to communicate animal knowledge and promote conservation.

Games academics play and their consequences: how authorship, h-index and journal impact factors are shaping the future of academia.

Research is a highly competitive profession where evaluation plays a central role; journals are ranked and individuals are evaluated based on their publication number, the number of times they are cited and their h-index. Yet such evaluations are often done in inappropriate ways that are damaging to individual careers, particularly for young scholars, and to the profession. Furthermore, as with all indices, people can play games to better their scores. This has resulted in the incentive structure of science increasingly mimicking economic principles, but rather than a monetary gain, the incentive is a higher score. To ensure a diversity of cultural perspectives and individual experiences, we gathered a team of academics in the fields of ecology and evolution from around the world and at different career stages. We first examine how authorship, h-index of individuals and journal impact factors are being used and abused. Second, we speculate on the consequences of the continued use of these metrics with the hope of sparking discussions that will help our fields move in a positive direction. We would like to see changes in the incentive systems, rewarding quality research and guaranteeing transparency. Senior faculty should establish the ethical standards, mentoring practices and institutional evaluation criteria to create the needed changes.

Molecular detection of Bifidobacterium spp. in faeces of black howler monkeys (Alouatta pigra).

BACKGROUND: Bifidobacterium genus are considered to be beneficial bacteria for their hosts; however, knowledge about the specific species that are part of the gut microbiome of howler monkeys is scarce. Polymerase chain reaction (PCR) is a useful technique for the identification of non-cultivable or difficult to grow bacterial species. With the goal of detecting species of the genus Bifidobacterium in black howler monkeys, we used PCR on DNA derived from faecal samples. METHODS: We collected and extracted DNA from 40 faecal samples. Using specific primers, we performed PCR and nested PCR to detect members of the Bifidobacterium genus and a subset of species: Bifidobacterium adolescentis, Bifidobacterium bifidum, Bifidobacterium infantis, Bifidobacterium longum and Bifidobacterium animalis subsp. animalis. RESULTS: 97.5% (39/40) of the samples were positive for Bifidobacterium spp. We found B longum in 100% of the analysed samples. CONCLUSIONS: This is the first report of B longum in black howler monkey faeces.

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.

BACKGROUND: Analyses 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. RESULTS: For 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. CONCLUSIONS: We 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.

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

BACKGROUND: 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. METHODS: 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. RESULTS: 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. CONCLUSIONS: 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.

Contrasting time-based and weight-based estimates of protein and energy intake of black howler monkeys (Alouatta pigra).

Two methods are commonly used to describe the feeding behavior of wild primates, one based on the proportion of time animals spent feeding on specific plant parts ("time-based" estimates) and one based on estimates of the actual amounts of different plant materials ingested ('"weight-based" estimates). However, studies based on feeding time may not be accurate for making quantitative assessments of animals' nutrient and energy intake. We analyzed the diet of two groups of Alouatta pigra living in forest fragments using two different methods (time- and dry weight-based estimates), to explore how these alternative approaches impact estimates of (a) the contribution of each food type to the diet and (b) the macronutrient composition of the diet, including available protein (AP), non-protein energy (NPE), and total energy (TE) intake. We conducted behavioral observations (N = 658 hr and N = 46 full day focal follows), from August 2012 to March 2013. For each feeding bout, we estimated both time spent feeding and actual fresh- and dry-weight consumption by counting the number of food items ingested during the bout. Using time-based estimates, A. pigra showed a predominantly leaf-based diet. In contrast, weight-based estimates described combined a fruit and leaf-based diet. There were no differences between methods when estimating AP intake; however, we found significant differences while estimating NPE and TE intake. Time-based estimates provide us with important information such as the foraging effort spent on food items, trees, or patches, while weight-based estimates may provide more accurate information concerning nutrient and energy intake. We suggest that quantitative estimates of nutrient intake in a primate's diet be based on observations of wet and/or dry weight actually ingested rather than extrapolated from time spent feeding.

Cascading impacts of anthropogenically driven habitat loss: deforestation, flooding, and possible lead poisoning in howler monkeys (Alouatta pigra).

To construct informed conservation plans, researchers must go beyond understanding readily apparent threats such as habitat loss and bush-meat hunting. They must predict subtle and cascading effects of anthropogenic environmental modifications. This study considered a potential cascading effect of deforestation on the howler monkeys (Alouatta pigra) of Balancán, Mexico. Deforestation intensifies flooding. Thus, we predicted that increased flooding of the Usumacinta River, which creates large bodies of water that slowly evaporate, would produce increased lead content in the soils and plants, resulting in lead exposure in the howler monkeys. The average lead levels were 18.18 ± 6.76 ppm in the soils and 5.85 ± 4.37 ppm in the plants. However, the average lead content of the hair of 13 captured howler monkeys was 24.12 ± 5.84 ppm. The lead levels in the animals were correlated with 2 of 15 blood traits (lactate dehydrogenase and total bilirubin) previously documented to be associated with exposure to lead. Our research illustrates the urgent need to set reference values indicating when adverse impacts of high environmental lead levels occur, whether anthropogenic or natural, and the need to evaluate possible cascading effects of deforestation on primates.

Black howler monkey (Alouatta pigra) activity, foraging and seed dispersal patterns in shaded cocoa plantations versus rainforest in southern Mexico.

Recent evidence has shown that primates worldwide use agroecosystems as temporary or permanent habitats. Detailed information on how these primates are using these systems is scant, and yet their role as seed dispersers is often implied. The main objective of this study was to compare the activity, foraging patterns and seed dispersal role of black howler monkeys (Alouatta pigra) inhabiting shaded cocoa plantations and rainforest in southern Chiapas, Mexico. We gathered data on three monkey groups living in shaded cocoa plantations and three groups living in rainforest, using focal sampling, and collecting fecal samples. General activity and foraging patterns were similar in both habitats, with the exception that monkeys in the cocoa habitat spent more time feeding on petioles. Monkeys in shaded cocoa plantations dispersed 51,369 seeds (4% were seeds ≥3 mm width) of 16 plant species. Monkeys in the rainforest dispersed 6,536 seeds (78% were seeds ≥3 mm width) of 13 plant species. Our data suggest that the difference between habitats in the proportion of large versus small seeds dispersed reflects differences in fruit species abundance and availability in cocoa versus forest. Mean seed dispersal distances were statistically similar in both habitats (cocoa = 149 m, forest = 86 m). We conclude that the studied cocoa plantations provide all elements necessary to constitute a long-term permanent habitat for black howler monkeys. In turn, howler monkeys living in these plantations are able to maintain their functional role as seed dispersers for those native tree and liana species present within their areas of activities.

Highly nested diets in intrapopulation monkey-resource food webs.

Recently several studies have focused on the structure of ecological networks to provide insights into ecological and coevolutionary dynamics of interacting species. However, rarely have the tools of ecological networks been used to understand how feeding relationships vary among individuals of the same population. Here we use 7 years of data and network analyzed to examine the intrapopulation diet variation in a group of howler monkeys (Alouatta palliata). We show that individual monkey-resource food webs are nested, but not modular and the stability of these patterns is independent of time of day or season. Our findings indicated that individuals do not forage randomly when compared to null models and that the diets of more selective monkeys represent subsets of the diets of other individuals. Moreover, there are no subgroups that eat a particular set of available plant species more frequently than other sets, suggesting that the spatial strategy of group foraging plays an important role in the feeding ecology of each group given that individuals of the same group tend to share similar resources while the group remains at a feeding site. Since the diets of more selective individuals are a subset of other monkeys, we suggest that more selective monkeys are able to outcompete others for preferred foods. Additionally, we did not observe differences in nutritional content or spatial abundance of more frequently eaten plant species when compared with less frequently eaten species, but in most cases, the more frequently eaten plant species were Ficus (Moraceae). This reinforces the important role that Ficus trees play in howler monkey feeding ecology, likely due to its year-round availability.

Behavioral and physiological responses to subgroup size and number of people in howler monkeys inhabiting a forest fragment used for nature-based tourism.

Animals' responses to potentially threatening factors can provide important information for their conservation. Group size and human presence are potentially threatening factors to primates inhabiting small reserves used for recreation. We tested these hypotheses by evaluating behavioral and physiological responses in two groups of mantled howler monkeys (Alouatta palliata mexicana) at the "Centro Ecológico y Recreativo El Zapotal", a recreational forest reserve and zoo located in the Mexican state of Chiapas. Both groups presented fission-fusion dynamics, splitting into foraging subgroups which varied in size among, but not within days. Neither subgroup size nor number of people had an effect on fecal cortisol. Out of 16 behavioral response variables tested, the studied factors had effects on six: four were affected by subgroup size and two were affected by number of people. With increasing subgroup size, monkeys increased daily path lengths, rested less, increased foraging effort, and used more plant individuals for feeding. As the number of people increased, monkeys spent more time in lower-quality habitat, and less time engaged in social interactions. Although fecal cortisol levels were not affected by the factors studied, one of the monkey groups had almost twice the level of cortisol compared to the other group. The group with higher cortisol levels also spent significantly more time in the lower-quality habitat, compared to the other group. Our results suggest that particular behavioral adjustments might allow howler monkeys at El Zapotal to avoid physiological stress due to subgroup size and number of people. However, the fact that one of the monkey groups is showing increased cortisol levels may be interpreted as a warning sign, indicating that an adjustment threshold is being reached, at least for part of the howler monkey population in this forest fragment.

Potential distribution of Mexican primates: modeling the ecological niche with the maximum entropy algorithm.

We developed a potential distribution model for the tropical rain forest species of primates of southern Mexico: the black howler monkey (Alouatta pigra), the mantled howler monkey (Alouatta palliata), and the spider monkey (Ateles geoffroyi). To do so, we applied the maximum entropy algorithm from the ecological niche modeling program MaxEnt. For each species, we used occurrence records from scientific collections, and published and unpublished sources, and we also used the 19 environmental coverage variables related to precipitation and temperature from WorldClim to develop the models. The predicted distribution of A. pigra was strongly associated with the mean temperature of the warmest quarter (23.6%), whereas the potential distributions of A. palliata and A. geoffroyi were strongly associated with precipitation during the coldest quarter (52.2 and 34.3% respectively). The potential distribution of A. geoffroyi is broader than that of the Alouatta spp. The areas with the greatest probability of presence of A. pigra and A. palliata are strongly associated with riparian vegetation, whereas the presence of A. geoffroyi is more strongly associated with the presence of rain forest. Our most significant contribution is the identification of areas with a high probability of the presence of these primate species, which is information that can be applied to planning future studies and then establishing criteria for the creation of areas to primate conservation in Mexico.