Lingual neoplasia in nonhuman primates: Description of five cases and a literature review.

BACKGROUND: Documentation of lingual tumors is scarce in nonhuman primates. METHODS: Through a multi-institutional retrospective study we compile cases of primary and metastatic neoplasia in non-human primates. RESULTS: We describe five cases of lingual neoplasia. Three cases are primary lingual tumors: chondro-osteoblastic lipoma in a howler monkey, squamous cell carcinoma, and fibroma in two baboons. We describe two cases of metastatic lymphoma in the tongue in rhesus macaques. A literature review of published lingual neoplasia in nonhuman primates is included in this manuscript. CONCLUSION: Lingual neoplasia is seldom reported in non-human primates.

The Speaker Method: A Novel Release Method for Offspring Mammals and 5-Year Study on Three Costa Rican Mammals.

Nowadays, wild animals are threatened by humans, with the number of species and individuals decreasing during recent years. Wildlife rescue centers play a vital role in the conservation of wildlife populations. This study aims to describe a new release technique, the Speaker Method, to rescue and facilitate the reunion of different baby mammals that arrived at a wildlife rescue center with their mothers within their natural habitat, avoiding the need for captivity. This method is based on a recorded baby's cry played on a speaker to make a "call effect" in the mother. The efficacy of the Speaker Method for babies' reunion with their mothers was 45.8% in Hoffmann's two-toed sloths (Choloepus hoffmanni) and 91.9% in brown-throated sloths (Bradypus variegatus). Among the mantled howler monkeys (Alouatta palliata), 50% of the babies could be released using this new technique. The findings suggest that the method could be helpful in the early release of young individuals, highlighting higher release outcomes in these three species compared to traditional nursery care provided by human caretakers, who face inherent difficulties in raising young animals without their mothers.

Ciclo estral de Alouatta palliata y Alouatta seniculus: una revisión / Alouatta palliata and Alouatta seniculus oestrus: a review

RESUMEN El mono aullador rojo colombiano (A. seniculus) y mono aullador de manto (A. palliata) son representantes del género Alouatta en Colombia y, según análisis de la Unión Internacional para la Conservación de la Naturaleza (UICN), sus poblaciones tienden a decrecer por múltiples factores. Esto sugiere la necesidad de orientar acciones para su conservación, para ello se requiere conocimiento de sus dinámicas reproductivas como la identificación y caracterización del ciclo estral. Se examinaron documentos bajo los criterios Alouatta seniculus, Alouatta paliatta, Alouatta, ciclo estral y reproducción en Scielo, Google Scholar, PubMed, Web of Science, Wiley, Science Direct y SpringerLink. Se encontraron quince artículos, cuatro libros, cuatro tesis de maestría y una monografía; en estos estudios se abordaban aspectos sobre comportamientos sexuales, cambios en los genitales y medición de hormonas. Los estudios han establecido una duración promedio del ciclo para A. seniculus de 17 y de 29,5 ±1,5 días, lo que muestra un rango amplio en comparación con lo hallado para A. palliata, donde los estudios evidencian una duración de 16,3; 15,52 ±4,88 y 16,08 ±4,27 días. Se concluye que algunos aspectos comunes entre las especies son la estacionalidad de los nacimientos durante la época seca, la relevancia del rango social del macho en las solicitudes de cópula por parte de las hembras en estro y algunos comportamientos como el olfateo y el lamido de genitales durante la receptividad sexual. Asimismo, es necesario conducir estudios en las especies de Alouatta en Colombia que, además de abordar las dinámicas reproductivas, consideren la influencia de factores medioambientales y sociales sobre estas.

Abstract The Colombian red howler monkey (A. seniculus) and mantled howler monkey (A. palliata) are representatives of the genus Alouatta in Colombia and according to IUCN (for its name in Spanish) analysis their populations tend to decrease due to multiple factors. This suggests the need to guide actions for their conservation, which requires knowledge of their reproductive dynamics, such as the identification and characterization of the estrous cycle. Papers were examined under the criteria Alouatta seniculus, Alouatta paliatta, Alouatta, estrus cycle, and reproduction in Scielo, Google Scholar, PubMed, Web of Science, Wiley, Science Direct, and SpringerLink. 15 articles, 4 books, 4 master's theses and 1 monograph were found; these studies addressed aspects of sexual behaviors, changes in genitalia and hormone measurement. The studies have established an average cycle length for A. seniculus of 17 and 29.5 ±1.5 days, thus showing a wide range compared to what was found for A. palliata where the studies evidenced a cycle length of 16.3, 15.52 ±4.88 and 16.08 ±4.27 days. The conclusion is that some common aspects among the species are the seasonality of births during the dry season, the relevance of the male's social rank in copulation requests by females in estrus and some behaviors such as sniffing and genital licking during sexual receptivity. Likewise, it is necessary to conduct studies on Alouatta species in Colombia that not only address reproductive dynamics but also consider the influence of environmental and social factors on them.

Blood analytes of electrocuted mantled howler monkeys (Alouatta palliata) in the Nicoya peninsula of Costa Rica.

BACKGROUND: Several species of Costa Rican wildlife are suffering terrible injuries along the power lines in rural areas of the country due to the increasing human development in rural areas, but this has also brought the problem of poorly designed electric infrastructure, where arboreal mammals find their normal tree routes cut down so that the only way for them to cross is on the power lines where they can get electrocuted. METHODS: Blood samples for complete blood count (CBC) and biochemistry panels (alkaline phosphatase, aspartate aminotransferase, amylase, total bilirubin, plasma urea, Ca, P, creatinine, glucose, Na, K, total protein, globulins, and albumin) were collected from 34 electrocuted mantled howler monkeys (Alouatta palliata) individuals that arrived at the Nosara Refuge for Wildlife between May 2018 and May 2019. RESULTS: From the total sample, 18 were males (11 juveniles and eight adults), and 16 were females (six juveniles and 10 adults). From those individuals, 13 animals survived: five females (three juveniles and two adults) and eight males (six juveniles and two adults). Then, 22 animals died after the event from 1 to 102 days (22.41 ± 31.17) after they arrived at the center. Of these 22 animals, 11 were females (three juveniles and eight adults), and 11 were males (six juveniles and five adults). CONCLUSIONS: The preliminary results showed significant differences in the plasma glucose, with adults being significantly higher than the juveniles, and there was also a significant difference in the plasma urea with the deceased ones being higher than the ones that survived the incident. These results may provide a better way to understand and predict the possible outcome of an electrical accident with these primates and assist with returning them back to their natural environment in the least time possible.

Environmental factors associated With Toxoplasma gondii Exposure in Neotropical Primates of Costa Rica.

The apicomplexan parasite Toxoplasma gondii (T. gondii) has been found in more than 350 species of homoeothermic vertebrates in diverse climates and geographic areas. In most animals, T. gondii produces mild or asymptomatic infection. However, acute and hyperacute toxoplasmosis is associated with high mortality rates observed in Neotropical primates (NP) in captivity. These primates are distributed in 20 countries across the Americas, and although infection has been reported in certain countries and species, toxoplasmosis in the wild and its impact on NP population survival is unknown. Differences among species in exposure rates and disease susceptibility may be due in part to differences in host behavior and ecology. Four species of NP are found in Costa Rica, i.e., howler (Alouatta palliata), spider (Ateles geoffroyi), capuchin (Cebus imitator), and squirrel monkeys (Saimiri oerstedii). This study reports NP exposure to T. gondii using the modified agglutination test in 245 serum samples of NP (198 wild and 47 from captivity) from Costa Rica. Associations of serostatus with environmental (forest cover, annual mean temperature), anthropogenic (human population density), and biological (sex) variables in howler and capuchin monkeys were evaluated. The seroprevalence among wild NP was 11.6% (95% CI = 7.7-17.34), compared with 60% in captive monkeys (95% CI = 44.27-73.63), with significant differences between species (X 2 = 20.072; df = 3, p = 0.000164), suggesting an effect of behavior and ecology. In general, antibody titers were low for wild NP (<1:128) and high for captive NP (>1:8192), suggesting higher exposure due to management factors and increased life span in captivity. Seropositivity in howler monkeys was positively related to forest cover and inversely related to annual rainfall. For capuchins, annual rainfall was inversely related to seropositivity. Surveillance of T. gondii exposure in NP in captivity and in the wild is required to understand drivers of the infection and develop novel strategies to protect them.

Sexual dimorphism and growth in Alouatta palliata based on 20+ years of field data.

OBJECTIVES: Alouatta palliata patterns of growth and sexual dimorphism are evaluated using 20 plus years of field data. Comparisons are made to other species of Alouatta and other New World primates. MATERIALS AND METHODS: Records of 92 A. palliata from Guanacaste Province, Costa Rica, were used to generate growth curves for body mass and linear measurements. Timing of growth for the properties was compared, and males and females were contrasted. Slopes and elevations for periods of rapid growth were evaluated. Growth allometry and proportion ratios were also explored. RESULTS: Body mass growth is rapid during the first 2 years. Males and females begin to diverge around a year of age as male growth increases and female growth slows. Adult mass for both is reached about 4 years of age. Linear measurements show rapid growth the first 18 months for both sexes. Differences develop as males continue the same rate of linear growth while female growth slows. Adult size is reached for head and body length around 3 years, and for hind-foot and tail lengths around 2 years. DISCUSSION: A. palliata males grow in mass more rapidly than females, while both grow similarly in linear dimensions, so that dimorphism is more pronounced in mass. This pattern is seen in other dimorphic New World primates. Male A. palliata may grow more rapidly than A. seniculus, reflecting earlier emigration for A. palliata males. Linear dimensions reach adult proportions earlier than body mass. For hind-foot and tail, this is probably an adaptation for gripping.

Potential Food Availability Influences Social Interactions of Young Individuals in a Neotropical Primate (Alouatta palliata).

Deforestation is widely recognised as an agent of human disturbance that causes widespread destruction of species habitats and can result in animals occupying forest patches with limited food resources. When animals are forced to change habitats, they must also adjust their diet, activity budgets and social behaviour in response to facing new ecological and environmental conditions. Only a few studies have analysed the influence of habitat conditions on social interactions of immature howler monkeys. In this study, we examined the effects of variation in food availability on social interactions of young howler monkeys (Alouatta palliata mexicana). This was accomplished by observing infant and juvenile members of two groups inhabiting a continuous forest habitat (640 ha) and three groups living in different-sized forest fragments (4, 42 and 93 ha) for a 15-month non-consecutive period. We quantified the Potential Food Availability Index (PFAI) for each habitat type based on the basal area, the Shannon-Wiener diversity index and abundance of food tree species. We used 15-min focal animal sampling to record the occurrence and/or duration of affiliative and agonistic behaviours. In habitats with higher PFAI, we observed more social play and proximity in infants aged 4-7 months, grooming in infants aged 8-14 months and social play in juveniles. Conversely, juveniles' grooming rates and 0- to 3-month-old infants' proximity rates decreased as PFAI increased. Our results suggest that food resource variation influences young howler monkeys' social interactions. The reduction in social interactions due to low food availability may represent an energy-saving strategy to cope with limited resources in habitats disturbed by anthropogenic activities.

From Mexico to Michigan and back: An international collaboration investigating primate behavior, ecology, and evolution from multiple perspectives.

Evolutionary research benefits form the integration of laboratory and field components to determine factors and processes that affect the evolutionary trajectories of species. Our shared interest in understanding hybridization with genetic admixture as a process that may impact social, behavioral, and ecological features of primates, brought us together in a collaborative project aimed at addressing how vocal variation in two species of howler monkeys in Mexico affects and is affected by hybridization. To achieve this goal, we joined our academic expertise in studying primate genetics, ecology, and behavior under different natural and experimental conditions. We took advantage of decades of experience studying and handing wild howler monkeys for translocation projects to safely sample and study wild populations for this project. Here, we describe the history of our collaboration highlighting how our different perspectives, academic realities, and individual strengths built the foundation for our successful collaboration. We also share our perspectives on how this collaboration opened up new academic venues, broadened our individual perspectives on the integration of different research approaches to address a complex topic, and allowed us to recognize the strength of international collaboration.

Maternal condition and maternal investment during lactation in mantled howler monkeys.

OBJECTIVES: Lactation is a costly reproductive state for females, as it may entail decreased body condition, increased morbidity, and increased mortality risk. To offset these costs, mothers should allocate investment in infant care as a function of their physical condition. Here, we assessed the relationship between maternal condition and maternal investment in wild mantled howler monkeys (Alouatta palliata) to determine: (1) whether maternal physical condition varied as a function of food availability, activity levels and feeding effort throughout lactation; (2) whether maternal investment was affected by maternal condition and offspring age. MATERIALS AND METHODS: We studied six adult females while rearing their immature offspring. We determined weekly food availability, C-peptide levels (as a measure of energy balance) in urine samples (306 samples), mothers' time budgets, feeding rates, time spent vigilant, and time spent carrying their offspring (for two years; 600 observation hours). RESULTS: C-peptide levels were positively related to food availability. Maternal care in terms of vigilance and offspring carrying peaked at early lactation and decreased progressively with offspring age. Carrying was positively related to C-peptide levels and was also influenced by variation in maternal condition throughout lactation. DISCUSSION: These results converge with previous theoretical and empirical studies on this topic and contribute to the growing evidence that nonhuman primate mothers allocate maternal care based on their current condition to maximize lifetime reproductive success.

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.

Phylogeography of the Mantled Howler Monkey (Alouatta palliata; Atelidae, Primates) across Its Geographical Range by Means of Mitochondrial Genetic Analyses and New Insights about the Phylogeny of Alouatta.

We analyzed 156 specimens of diverse howler monkey taxa (Alouatta; Atelidae, Primates) for different mitochondrial genes (5,567 base pairs), with special emphasis on A. palliata and related taxa. Our results showed no relevant differences among individuals of different putative taxa, A. p. palliata, A. p. aequatorialis, A. coibensis coibensis, and A. c. trabeata. We found no spatial differences in genetic structure of A. p. palliata throughout Costa Rica, Nicaragua, and Honduras. A. p. mexicana (genetic distance: 1.6-2.1%) was the most differentiated taxon within A. palliata. Therefore, we postulate the existence of only 2 clearly defined subspecies within A. palliata (A. p. palliata and A. p. mexicana). A. palliata and A. pigra (traditionally considered a subspecies of A. palliata) are 2 clearly differentiated species as was demonstrated by Cortés-Ortiz and colleagues in 2003, with a temporal split between the 2 species around 3.6-3.7 million years ago (MYA). Our results with the Median Joining Network procedure showed that the ancestors of the cis-Andean Alouatta gave rise to the ancestors of the trans-Andean Alouatta around 6.0-6.9 MYA. As Cortés-Ortiz et al. showed, A. sara and A. macconnelli are differentiable species from A. seniculus, although the first 2 taxa were traditionally considered subspecies of A. seniculus. Our findings agree with the possibility that the ancestor of A. sara gave rise to the ancestor of A. pigra in northern South America. In turn, the ancestor of A. pigra originated the ancestor of A. palliata. Two of our results strongly support the hypothesis that the South American A. palliata (the putative A. p. aequatorialis) was the original population of this species; it has high genetic diversity and no evidence of population expansion. The Central America A. palliata is the derived population. It has low genetic diversity and there is clear evidence of population expansion. However, A. palliata and A. pigra probably migrated into Central America by 2 different routes: the Isthmus of Panama (A. palliata) and Caribbean island arch (A. pigra). Finally, the red howler monkeys from the island of Trinidad in the Caribbean Sea were not A. macconnelli (= A. s. stramineus) as Groves maintained in his influential 2001 publication on primate taxonomy. This taxon is more related to A. s. seniculus, although it formed a monophyletic clade. Future molecular and karyotypic studies will show if the Trinidad red howler monkeys should be considered as an extension of the Venezuelan taxon, A. arctoidea, as a subspecies of A. seniculus(A. s. seniculus), or, in the case of extensive chromosomal rearrangements, even a new species.

Association of Anthropogenic Disturbances and Intestinal Parasitism in Ecuadorian Mantled Howler Monkeys, Alouatta palliata aequatorialis.

Forest disturbance and human encroachment have the potential to influence intestinal parasite communities in animal hosts by modifying nutritional health, physiological stress, host densities, contact rates, and ranging patterns. Anthropogenic disturbances also have the ability to affect the ecological landscape of parasitic disease, potentially impacting the health of both wildlife and people. Our research investigated the association of forest disturbance and human encroachment on intestinal parasite communities in mantled howler monkeys, Alouatta palliata aequatorialis. We found that individual parasite species prevalence was associated with group size and forest disturbance. Proximity to people was not a direct factor influencing intestinal parasitism; rather, several human proximity indices were related to group size, which was in turn related to overall species richness and the presence of specific parasite species. These results, coupled with previous findings, suggest that anthropogenic disturbances are likely influencing intestinal parasite communities. Though no single study has definitively explained all relationships between anthropogenic disturbances and intestinal parasitism, we propose that our models are appropriate for meta-analysis testing across other species and environments.

New Entamoeba group in howler monkeys (Alouatta spp.) associated with parasites of reptiles.

Our knowledge of the parasite species present in wildlife hosts is incomplete. Protozoans such as amoebae of the genus Entamoeba infect a large variety of vertebrate species, including NHPs. However, traditionally, their identification has been accomplished through microscopic evaluation; therefore, amoeba species have not always been identified correctly. We searched for Entamoeba spp. using a fragment of the small subunit rDNA in free-ranging howler monkeys (Alouatta palliata and A. pigra) from southeast Mexico. One hundred fifty five samples were collected, with 46 from A. palliata and 109 from A. pigra and 8 of the total samples were positive. We detected a new clade of Entamoeba, which was separated from other described species but closer to E. insolita, as well as an unnamed sequence typically found in iguana species with low shared identity values (<90%). We designated this new clade as conditional lineage 8 (CL8) and we have shown that members of this group are not exclusive to reptiles.

Comparison of forest regeneration in two sites with different primate abundances in Northwestern Ecuador / Comparación de la regeneración del bosque en dos sitios con diferente abundancia de primates en el Noroccidente de Ecuador

AbstractThere is increasing evidence that large-bodied primates play important roles as seed dispersers and in the maintenance of tree diversity in forest ecosystems. In this study we compared forest regeneration at two sites with differing primate abundances in the Ecuadorian Chocoan rainforest. We predicted: (1) significant differences in primate abundance between the two sites; (2) higher understory tree species richness and density at the site with greater primate abundance; (3) the site with lower primate abundance characterized by tree species dispersed by non-primate biotic agents and/or abiotic factors. We compared two sites, Tesoro Escondido (TE) a campesino cooperative, and the El Pambilar (EP) wildlife refuge that both maintain populations of mantled howler monkey (Alouatta palliata), the brown-headed spider monkey (Ateles fusciceps fusciceps) and the capuchin monkey (Cebus capucinus). We characterized canopy structure by point-quadrant sampling, determined primate abundance and sampled seedlings/saplings in 1 m2 plots, classifying tree species based on three dispersal syndromes: adapted for primate dispersal, dispersed by other biological agents, and abiotic dispersal. We compared sites in terms of primate abundance (groups and individuals observed per day) and regeneration characteristics (overall density, species richness, and dispersal syndrome). We carried out within site comparisons and constructed understory tree species accumulation curves. Overall the forests were structurally similar - with significantly higher densities of A. f. fusciceps at TE. Encounter rates for the other two primate species were similar at both sites. Understory tree density and species richness was significantly higher in TE with no stabilization of tree species accumulation curves. The species accumulation curve for understory trees at EP stabilized. Higher densities and species richness of primate dispersed tree species were observed at TE, with non-primate biotically dispersed tree species the dominant dispersal syndrome at both sites. Our observations are consistent with those from other studies investigating the role of large-bodied frugivorous primates in forest regeneration, and point to a general pattern: future lowland tropical forest tree diversity depends on maintaining robust populations of large primate species in these systems. It is highly probable that the maintenance of high levels of tree diversity in Chocoan rainforests is dependent on the conservation of its largest resident primate, the critically endangered brown-headed spider monkey (A. f. fusciceps). Rev. Biol. Trop. 64 (2): 493-506. Epub 2016 June 01.

ResumenHa habido un incremento de la evidencia sobre el importante papel ecológico de los primates grandes como dispersores de semillas para el mantenimiento de la diversidad del bosque. Este estudio compara la regeneración del bosque en dos sitios con diferente abundancia de primates en el Chocó ecuatoriano. Las predicciones son: (1) la abundancia de primates será significativamente diferente en los dos sitios; (2) la riqueza de especies y la densidad de plantas del sotobosque será mayor en la localidad con mayor abundancia de primates y, (3) la localidad con menos primates tendrá mayor riqueza de especies y densidad de plantas que aquellas especies dispersadas por otros mecanismos bióticos. Se compararon dos sitios: una cooperativa campesina (TE) y un Refugio de Vida Silvestre (EP). Allí habitan tres especies de primates: el aullador negro (Alouatta palliata), el mono araña de cabeza café (Ateles fusciceps fusciceps) y el mono capuchino (Cebus capucinus). Se caracterizó la estructura del dosel usando muestreos en punto-cuadrante, se determinó la abundancia de primates y se muestrearon plántulas en parcelas de 1 m2, clasificando las especies de acuerdo con tres síndromes de dispersión: dispersadas por primates, dispersadas por otros agentes bióticos y dispersadas por agentes abióticos. Se compararon ambos sitios en términos de abundancia de primates (grupos e individuos por día) y características de la regeneración (densidad de plantas, riqueza de especies, y síndrome de dispersión). Se hicieron comparaciones en cada sitio y se construyeron curvas de acumulación de especies. El bosque fue estructuralmente similar, con una abundancia mayor de A. f. fusciceps en TE. Los encuentros para las otras dos especies de primates fueron similares en ambos sitios. La densidad y riqueza de plántulas del sotobosque fue significativamente mayor en TE y la curva de acumulación de especies no se estabilizó pero sí lo hizo en EP. Se observó mayor densidad y riqueza de plántulas dispersadas por primates en TE con dominancia del grupo de plántulas expuestas a otros agentes bióticos y abióticos en ambos sitios. Los resultados son consistentes con los de otros estudios que investigan el papel de los grandes primates frugívoros en la regeneración del bosque y puntualizan un patrón general: la diversidad futura de los bosques tropicales de tierras bajas podría depender del mantenimiento de poblaciones robustas de primates grandes. Es probable que la alta diversidad de árboles en los bosques lluviosos del Chocó dependa de la conservación de sus primates, entre ellos el mono araña de cabeza café, una especie críticamente amenazada.

Population density and primate conservation in the Noroeste Biosphere Reserve, Tumbes, Peru / Densidad poblacional y conservación de los primates de la Reserva de Biosfera del Noroeste, Tumbes, Perú

The Noroeste Biosphere Reserve (NBR) is home to at least 22 species of medium and large mammals including the primates Alouatta palliata aequatorialis and Cebus albifrons aequatorialis. Previous estimates of A. p. aequatorialis population density vary from 2.3-8.6 ind/km² in 1983 to 17-19 ind/km² in 2005 and 2006, respectively. While for C. a. aequatorialis there are no estimates of population density in the NBR. In order to calculate the population density estimates for both species we installed six transects in 10.5 km² within the Cerros de Amotape National Park (belonging to the NBR) from August 2012 to March 2013. Based on 112.3 km of transects we obtained a population density of 8.3 ± 3.6 ind/km² for A. p. aequatorialis. However, for the reduced number of Cebus albifrons aequatorialis sightings we were only able to calculate a group size from three to 12 individuals and an encounter rate of 0.3 ind/km. Even though A. p. aequatorialis has potentially increased in population density, it is not feasible to make comparisons with previous estimates in the same area because of the different employed methodologies and the lack of randomness in the data collection. We recommend a long-term monitoring plan, including C. a. aequatorialis which makes it a conservation priority for the NBR, this monitoring plan should include mitigation of potential threats such as illegal hunting and trapping for the pet trade.

La Reserva de Biósfera del Noroeste (RBN) alberga por lo menos 22 especies de mamíferos medianos y grandes entre las cuales se encuentran los primates Alouatta palliata aequatorialis y Cebus albifrons aequatorialis. Los estimados previos de la densidad poblacional de A. p. aequatorialis varían de 2.3‒8.6 ind/km² en 1983 a 17‒19 ind/km² en 2005 y 2006, respectivamente. Mientras que para C. a. aequatorialis no existen estimados poblacionales para la RBN. Para calcular la densidad poblacional de estas dos especies instalamos seis transectos lineales en 10.5 km² dentro del Parque Nacional Cerros de Amotape (perteneciente a la RBN) de agosto del 2012 a marzo del 2013. En base a 112.3 km de transectos se obtuvo una densidad poblacional de 8.3 ± 3.6 ind/km² para A. p. aequatorialis; sin embargo, por el reducido número de avistamientos de Cebus albifrons aequatorialis solo se pudo calcular el tamaño de grupo que varió de tres a 12 individuos y la tasa de encuentro de 0.3 ind/km. A pesar que la población del A. p. aequatorialis aparentemente ha aumentado, no es factible hacer comparaciones con los estimados anteriores debido a las diferentes metodologías empleadas y a la falta de aleatoriedad en la toma de datos. Recomendamos un plan de monitoreo a largo plazo, que incluya a C. a. aequatorialis como objeto y prioridad de conservación para la RBN, el cual debería incluir la mitigación de posibles amenazas como caza y captura para comercio de mascotas.

Genetic, spatial, and social relationships among adults in a group of howler monkeys (Alouatta palliata) from Barro Colorado Island, Panama.

Kinship plays an important role in the social behavior of many primate species, including patterns of intra-group affiliation and cooperation. Within social groups, kinship is strongly affected by dispersal patterns, with the degree of relatedness among group-mates expected to decrease as the tendency to disperse increases. In primate species characterized by bisexual dispersal, relatedness among adult group-mates is predicted to be low, with social interactions shaped largely by factors other than kinship. To date, however, few studies have examined the role of kinship in social interactions in bisexually dispersing species. Accordingly, we collected genetic, spatial and behavioral data on all adult members (three males, six females) in a group of free-ranging mantled howler monkeys (Alouatta palliata)--a bisexually dispersing species of atelid primate--from Barro Colorado Island (BCI), Panama. Analyses of microsatellite variation revealed that relatedness was greater among adult males in this group (mean pairwise relatedness = 0.32 for males versus 0.09 for females). Relatedness among individuals, however, was not associated with either spatial proximity or frequency of social interactions. Instead, sex was a better predictor of both of these aspects of social behavior. While relatedness among adults had no discernible effect on the intra-group social interactions documented in this study, we postulate that kinship may facilitate affiliative and cooperative behaviors among male group-mates when interacting competitively with neighboring howler groups over access to food or potential mates.

Effect of ancestry on behavioral variation in two species of howler monkeys (Alouatta pigra and A. palliata) and their hybrids.

Social differences between primate species may result from both flexible responses to current conditions or fixed differences across taxa, yet we know little about the relative importance of these factors. Here, we take advantage of a naturally occurring hybrid zone in Tabasco, Mexico to characterize the variation in social structure among two endangered howler monkey species, Alouatta pigra and A. palliata, and their hybrids. Work in pure populations has suggested that A. pigra females maintain closer proximity, exhibit higher rates of affiliation, and lower rates of agonism than A. palliata females, but we do not know what accounts for this difference. Using identical data collection and analysis methods across three populations, we first seek to confirm previously reported interspecific differences in social structure across all sexes. We next examine: (1) how female social relationships changed with ancestry (by comparing pure and hybrid individuals); (2) how female social relationships changed with group size (A. pigra have smaller groups than A. palliata); and (3) whether female social relationships differed between two taxonomic groups within a single forest fragment (thus controlling for ecological variation). We confirmed previously described species differences, including closer proximity among females than among males in all populations. We also found that smaller groups maintained closer proximity. However, even after accounting for variation in group size, A. pigra females had closer proximity and more affiliation than A. palliata females. Furthermore, differences between pigra-like and palliata-like hybrids paralleled differences between pure populations and persisted even after controlling for ecological variation. Together, our results suggest that flexibility cannot account for all of the social differences between A. pigra and A. palliata and indicate an important genetic component in primate social behavior.

Limited genetic diversity in the critically endangered Mexican howler monkey (Alouatta palliata mexicana) in the Selva Zoque, Mexico.

The Mexican howler monkey (Alouatta palliata mexicana) is a critically endangered primate, which is paleoendemic to Mexico. However, despite the potential significance of genetic data for its management and conservation, there have been no population genetic studies of this subspecies. To examine genetic diversity in the key remaining forest refuge for A. p. mexicana, the Selva Zoque, we amplified full-length mitochondrial control region sequences (1,100 bp) from 45 individuals and found 7 very similar haplotypes. Haplotype diversity (h = 0.486) and nucleotide diversity (π = 0.0007) were extremely low compared to other Neotropical primates. Neutrality tests, used to evaluate demographic effects (Tajima's D = -1.48, p = 0.05; Fu's F s = -3.33, p = 0.02), and mismatch distribution (sum of squares deviation = 0.006, p = 0.38; raggedness index = 0.12, p = 0.33) were consistent with a recent and mild population expansion and genetic diversity appears to be historically low in this taxon. Future studies should use a combination of mitochondrial and nuclear markers to fully evaluate genetic diversity and to better understand demographic history in A. p. mexicana. These studies should be undertaken throughout its geographic range in order to evaluate population structure and identify management units for conservation. Due to the limited distribution and population size of A. p. mexicana, future conservation strategies may need to consider genetic management. However, a more detailed knowledge of the population genetics of the subspecies is urgently recommended to maximise the conservation impact of these strategies.

Viabilidad poblacional de Alouatta palliata (Primates: Atelidae) y Cebus capucinus (Primates: Cebidae) en el Refugio de Vida Silvestre Privado Nogal, Sarapiquí, Heredia, Costa Rica / Population viability of Alouatta palliata (Primates: Atelidae) and Cebus capucinus (Primates: Cebidae) at Refugio de Vida Silvestre Privado Nogal, Sarapiquí, Heredia, Costa Rica

Population viability of Alouatta palliata (Primates: Atelidae) and Cebus capucinus (Primates: Cebidae) at Refugio de Vida Silvestre Privado Nogal, Sarapiquí, Heredia, Costa Rica. Habitat destruction may cause wildlife population fragmentation and is considered an important factor in small population species extinction. As wildlife populations become smaller, threats to their stability and persistence arise as a result of demographic, environmental and genetic stochastic factors. The aim of this work was to study the effects of population fragmentation on the long term viability of Alouatta palliata and Cebus capucinus populations, at Refugio de Vida Silvestre Privado Nogal, Sarapiquí (RVSPN), Heredia. For this we used the computer software VORTEX to run a population viability analysis (PVA) for both species. The input data of the PVA were taken from the demography structure of the RVSPN, literature sources from the species and from PVA related papers. We evaluated two sets of scenarios: small fragmented populations to reflect the population current state, and one larger and continuous population, to reflect the effect of reforestation actions followed by RVSPN to connect forest fragments. Results suggest that both A. palliata and C. capucinus can survive in isolated forest fragments. However, if different factors as inbreeding depression, catastrophes or habitat loss were incorporated to the scenarios, the small fragmented populations become unstable and the risk of extinction increased for both species. Continuous and larger populations were more robust against the threats incorporated in the scenarios when compared to the current situation of smaller and fragmented populations. The best management option for both species would be to continue reforestation efforts in the area to connect forest fragments, with the result of larger and continuous populations of both species. It is important to continue the observation of both species populations, and to promote a habitat management to reduce the negative effects of stochastic environmental events. Rev. Biol. Trop. 60 (2): 809-832. Epub 2012 June 01.

La destrucción del hábitat conlleva a la fragmentación de poblaciones de especies silvestres y se considera como uno de los principales factores en la extinción de especies A medida que las poblaciones se vuelven más pequeñas, surgen amenazas hacia su estabilidad y persistencia, como resultado de factores estocásticos demográficos, ambientales y genéticos. El objetivo de este trabajo fue estudiar los efectos de la fragmentación de poblaciones en la viabilidad de Alouatta palliata y Cebus capucinus en el Refugio de Vida Silvestre Privado Nogal (RVSPN), Sarapiquí, Heredia. Para esto se uso el programa VORTEX para correr un análisis de viabilidad de poblaciones (PVA) para ambas especies. La información utilizada en el PVA proviene de la estructura demográafica de las poblaciones del RVSPN, literatura sobre la historia natural de las especies y artículos relacionados con PVA. Los resultados sugieren que tanto A. palliata como C. capucinus pueden sobrevivir en fragmentos boscosos aislados. Sin embargo, si se incorporan factores como depresión por endogamia, catástrofes o perdida de hábitat, las pequeñas poblaciones fragmentadas se vuelven inestables y aumenta el riesgo de que desaparezcan. Las poblaciones continuas fueron más robustas ante las amenazas incorporadas, por lo que se recomienda continuar con la reforestación para unir los fragmentos boscosos. Es importante darle seguimiento a las poblaciones de ambas especies y tener un manejo de su hábitat para disminuir los efectos negativos de diferentes eventos estocásticos provocados por el ambiente.

Prevalence of fur mites (Acari: Atopomelidae) in non-human primates of Costa Rica

Parasites have been investigated for some New World primates; however, very little is known about ectoparasites and specifically fur mites. In this study, Alouatta palliata, Cebus capucinus, Saimiri oerstedii, and Ateles geoffroyi monkeys from different areas of Costa Rica were searched for fur mites. A total of 276 monkeys were evaluated, and 51 of them were positive for mites of the family Atopomelidae. Listrocarpus alouattae was identified on 22.3% of A. palliata; Listrocarpus capucinus on 12.8% of C. capucinus; and Listrocarpus costaricensis on 36.8% of S. oerstedii; No fur mites were found on A. geoffroyi. Sex was not considered a determinant of mite infestation, but prevalence was significantly higher in the Central Volcanic Mountain Range Conservation Area for L. alouattae (p=0.01) and in the Central Pacific Conservation Area for L. capucinus (p=0.002). These primate fur mites are highly host-specific. Differences in the geographical distribution may be due to monkey behavior and history, as well as to environmental conditions. Rev. Biol. Trop. 57 (1-2): 353-360. Epub 2009 June 30.

Muy poco se conoce sobre los ectoparásitos, específicamente de los ácaros del pelo, de primates del Nuevo Mundo. En este estudio se buscaron ácaros del pelo en monos Alouatta palliata, Cebus capucinus, Saimiri oerstedii y Ateles geoffroyi provenientes de diferentes áreas de Costa Rica. Se evaluaron 276 monos en total y 51 de ellos se encontraron positivos por ácaros de la familia Atopomelidae. Se identificó Listrocarpus alouattae en el 22.3% de los A. palliata, Listrocarpus capucinus en el 12.8% de los C. capucinus y Listrocarpus costaricensis en el 36.8% de los S. oerstedii. El sexo no fue un determinante de la infestación por ácaros, pero la prevalencia de L. alouattae fue significativamente mayor en el Área de Conservación Cordillera Volcánica Central (p=0.01) y la de L. capucinus fue mayor en el Área de Conservación Pacífico Central (p=0.002). Estos ácaros del pelo de primates son altamente específicos en relación con su hospedero. Las diferencias en la distribución geográfica podrían deberse al comportamiento e historia de los monos, así como a las condiciones ambientales.