Fruit availability has a complex relationship with fission-fusion dynamics in spider monkeys.

Understanding the ecological and social factors that influence group size is a major focus of primate behavioural ecology. Studies of species with fission-fusion social organizations have offered an insightful tool for understanding ecological drivers of group size as associations change over short temporal and spatial scales. Here we investigated how the fission-fusion dynamics of spider monkeys (Ateles geoffroyi) at Runaway Creek, Belize were affected by fruit availability. When males and females were analyzed together, we found no association between fruit availability and subgroup size. However, when females were analyzed separately, we found that when fruit availability increased, so did subgroup size. In all analyses, higher fruit availability did not influence subgroup spatial cohesion. Our results point to the complexity of understanding grouping patterns, in that while ecological factors make groups of specific sizes advantageous, social factors also play an important determining role.

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.

Using multiplex networks to capture the multidimensional nature of social structure.

Network analysis has increasingly expanded our understanding of social structure in primates and other animal species. However, most studies use networks representing only one interaction type, when social relationships (and the emerging social structure) are the result of many types of interactions and their interplay through time. The recent development of tools facilitating the integrated analysis of multiple interaction types using multiplex networks has opened the possibility of extending the insight provided by social network analysis. We use a multiplex representation of interactions among the members of a group of wild Geoffroy's spider monkeys (Ateles geoffroyi), to study their social structure. We constructed a six-layered multiplex network based on three indices of overt social interactions (aggression, embraces, grooming) and three distance-based indices (contact, proximity, and association). With tools provided by the MuxViz software, we assessed the relevance of including all six indices in our analysis, the role of individuals in the network (through node versatility), and the presence of modules and non-random triadic structures or motifs. The multiplex provided information which was not equivalent to any individual layer or to the simple aggregation of layers. Network patterns based on associations did not correspond with those observed for overt-interactions or for the multiplex structure. Males were the most versatile individuals, while multiplex modularity and motifs highlighted the relevance of different interaction types for the overall connectivity of the network. We conclude that the multiplex approach improves on previous methods by retaining valuable information from each interaction type and how it is patterned among individuals.

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.

Elección diferencial de frutos en dos especies simpátricas de monos y murciélagos frugívoros en el sureste de México / Differential fruit choice in two simpatric monkey species and frugivorous bats in southern mexico

ABSTRACT In order to identify the role played by plant species as a food source in the fruit election of dispersing agents (Alouatta pigra Lawrence 1933, Atelesgeoffroyi Kuhl 1820 and frugivorous bats), we developed a study in dry tropical forests in Yucatan, Mexico. We recorded the fruits consumed by frugivorous bats using collectors and, for monkeys, we implemented the focal animal method. The number of fruits consumed by primates (A. pigra and A. geoffroyi) and bats were recorded, 342 and 386, respectively. It was determined that bats deposited fruits with some percentage of pulp, while monkeys contributed more with a fruits without pulp (pairwise LSD contrast p < 0.05). Among the variety of fruit species in the diet of primates, we detected that A. pigra chose mostly not an abundant species such as Enterolobium cyclocarpum Jacq. Griseb. (1860) instead of those more abundant (Manilkara zapota (L.) P. Royen (1953) and Brosimum alicastrum Sw. subsp. alicastrum C.C. Berg (1972)). The type of fruit and seed handling caused by primates would be more beneficial to seed germination than those applied by bats. Moreover, this election and fruit handling could depend on the characteristics of fruits and space-temporal availability of plant species as a food source.

RESUMEN 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.

How Survey Design Affects Monkey Counts: A Case Study on Individually Recognized Spider Monkeys (Ateles geoffroyi).

The fast movement and high degree of fission-fusion dynamics of spider monkeys (Ateles spp.) make them notoriously difficult to survey. We examined which aspects of survey design affect spider monkey sightings along transects in a group of individually recognized spider monkeys (Ateles geoffroyi) in Punta Laguna, Yucatan, Mexico. We calculated the number of monkeys and subgroups sighted per transect walk. Using generalized linear models, we found no effect of the number of observers, transect type (new vs. existing), walking speed, or time of day on individual monkey counts or subgroup counts. Recounting of individuals was relatively rare and occurred when transects were walked relatively slowly. We missed more young than adult monkeys. The group composition based on survey data was similar to the known group composition. Based on our findings we recommend that surveys performed on relatively flat terrain be conducted at speeds similar to or faster than the moving speed of spider monkeys to minimize recounting of individuals and that young:adult female ratios based on survey data be interpreted as conservative indicators of population health. The novel methods presented to determine sources of bias in population estimates are applicable to a wide range of primates that are difficult to survey.

Primate extirpation from rainforest fragments does not appear to influence seedling recruitment.

Primates are important seed dispersers, especially of large-seeded tree species, but the impact that these animals have on seedling recruitment is unclear. Evidence suggests that forest regeneration might be disrupted in forest fragments in which primates were extirpated. We tested this hypothesis by assessing seedling recruitment in 3 forest fragments occupied (OF) by primates, 3 fragments unoccupied (UF) by primates, and 3 areas within a continuous forest (CF) in the Lacandona rainforest, Mexico. Species and stem densities of tree, palm and liana seedlings were recorded over 16 months. Individuals were classified according to dispersal mode: large-seeded animal-dispersed (LS), small- and medium-seeded animal-dispersed (SS), and abiotically-dispersed species (AD). We assessed the influence of primate presence, adult tree assemblage, and fragment spatial metrics (size, age, distance to nearest fragment, and distance to continuous forest) on seedling assemblages. We recorded 6879 seedlings belonging to 90 species, and 59 genera in 405 1-m(2) plots. Both seedlings and adults showed similar differences in species and stem densities of LS, SS and AD species among forest types, suggesting that seedling assemblages were strongly influenced by the adult assemblages. The recruitment of each LS species varied among study sites, but evidence supporting higher recruitment enhancement of these species in continuous forest and occupied fragments was weak. Distance to continuous forest was the unique fragment spatial metric related (negatively) to the recruitment of LS species. Thus, primate extirpation does not appear to disrupt seedling assemblages in the Lancandona rainforest. Nevertheless, we cannot reject the hypothesis that certain LS species such as Spondias radlkoferi may be affected by the extirpation of primates.

Efecto del enriquecimiento ambiental en un grupo de monos araña (Ateles geoffroyi) en cautiverio / Effect of environmental enrichment in a group of captive spider monkeys (Ateles geoffroyi)

Los animales que viven en cautiverio padecen problemas relacionados con el estrés y la falta de estimulación. El enriquecimiento ambiental (EA) proporciona a los animales en esta situación un conjunto de actividades que los alienta a presentar conductas típicas de su especie. El objetivo de este trabajo fue analizar el efecto de un programa de EA en la conducta de una colonia de siete monos araña (Ateles geoffroyi). Se esperaba que la agresión, la coprofilia y las estereotipias fueran menos frecuentes entre los monos, mientras que la exploración y el juego se presentaran con mayor frecuencia. Para ello, la investigación se dividió en dos etapas: una etapa previa al EA y una etapa durante el EA. En cada etapa se registraron las siguientes categorías conductuales: agresión, coprofilia, estereotipias, exploración y juego. Se utilizó un muestreo focal por conducta en registros continuos de 1 hr., obteniéndose en cada etapa 40 hrs. de observación. Al comparar la frecuencia de dichas conductas con la prueba de los signos de Wilcoxon, se encontró que la agresión, las estereotipias y la coprofilia disminuyeron durante el EA. La exploración y el juego se incrementaron significativamente con el EA. No se observaron diferencias significativas al comparar el sexo de los individuos. El EA disminuye los problemas causados por el confinamiento, por lo que debe contemplarse como una herramienta indispensable que de manera constante mejore las condiciones de vida en individuos confinados.

Captive animals suffer from stress and lack of stimulation. Environmental enrichment (EE) provides them with a series of activities that encourages them to present species-specific behaviors. The objective of this work was to analyze the effect of an EE program in the behavior of a 7-spider monkey colony. It was expected that aggression, coprophilia and stereotypes would be less frequent, while exploration and play would increase. The study was divided in two stages: one previous to EE and one while EE was being implemented. A focal sampling per behavior was undertaken in 1-h continuous recordings for a total of 40 hours per stage. We compared the frequency of each behavior with a Wilcoxon's signal test. The results showed that aggression, stereotypes and coprophilia were reduced during EE, while exploration and play increased significantly. No significant differences were found between sexes. EE reduces the problems originated by confinement; therefore, it must be considered a necessary tool to be continuously employed to make an improvement into the life conditions of confined individuals.

Seed source, seed traits, and frugivore habits: Implications for dispersal quality of two sympatric primates.

• Premise of the study: Frugivore selection of fruits and treatment of seeds together with seed deposition site are crucial for the population dynamics of vertebrate-dispersed plants. However, frugivore species may influence dispersal quality differently even when feeding on the same fruit species and, while animals disperse some seeds, others simply fall beneath the parent plant.• Methods: In southern Mexico, we investigated to see if within-species seed traits (i.e., length, width, weight, and volume) and germination success differed according to seed source. For five tropical tree species we obtained ingested seeds from two sources, howler monkey (Alouatta pigra) and spider monkey (Ateles geoffroyi) feces; and noningested seeds from two sources, the ground and tree crowns (with predispersed seeds used as control).• Key results: A principal components' analysis showed that traits of seeds ingested by howler monkeys differed from other sources while seeds ingested by spider monkeys were similar to noningested seeds. Howlers consumed on average the larger seeds in Ampelocera hottlei, Brosimum lactescens, and Dialium guianense. Both primate species consumed the smaller seeds in Spondias mombin, while no seed trait differences among seed sources were found in Spondias radlkoferi. For all five tree species, germination rate was greatest for seeds ingested by howler monkeys.• Conclusions: For the studied plant species, seed ingestion by howler monkeys confers higher dispersal quality than ingestion by spider monkeys or nondispersal. Dispersal services of both primate species, however, are not redundant and may contribute to germination heterogeneity within plant populations in tropical forests.

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.

The Effect of Human Development on Mammal Populations of the Punta Leona Private Wildlife Refuge, Costa Rica

The effect of human development on six diurnal mammal species was studied using transects in the Punta Leona Private Wildlife Refuge, Puntarenas, Costa Rica during the dry season months of March and April 2006. Individuals/km was recorded for each species in more developed (MD) (near paved roads, buildings, construction, or deforested trees) and less developed areas (LD) (secondary forest). The white-faced apuchin monkey (Cebus capucinus) (n = 233), coatimundi (Nasua narica) (n = 46), and Central American spider monkey (Ateles geoffroyi) (n = 36) demonstrated a preference for less-developed habitats. The nine-banded armadillo (Dasypus novemcinctus) (n = 4), tamandua (Tamandua mexicana) (n = 2) and variegated squirrel (Sciurus variegatoides) (n = 5) were observed infrequently. White-faced monkeys avoided construction areas, but received artificial food daily in developed areas. Coatimundis also received artificial foods daily and showed aggression towards guests. Rev. Biol. Trop. 57 (1-2): 441-449. Epub 2009 June 30.

Se estudiaron seis especies de mamíferos mediante transectos durante la estación seca tardía (marzo y abril) de 1996 en el Refugio de Vida Silvestre de Punta Leona, Puntarenas, Costa Rica. Se registró la cantidad de animales por km en lugares con mucho efecto humano (cerca del caminos pavimentados, edificios, construcción, y deforestación) y lugares con menos efecto. El mono carablanca (Cebus capucinus) (n = 233), el pizote (Nasua narica) (n = 46), y el mono araña centroamericano (Ateles geoffroyi) (n = 36) prefirieron lugares con menos efecto. Se observó pocos armadillos (Dasypus novemcinctus) (n = 4), osos hormigueros (Tamandua mexicana) (n = 2), y ardillas (Sciurus variegatoides) (n = 5). Los monos carablancas y pizotes aceptan alimentos artificiales y los pizotes fueron agresivos con los turistas. Los carablancas evitan los lugares con construcciones y los caminos pavimentados.

Germinación de semillas de Ficus insipida (Moraceae) defecadas por tucanes (Ramphastos sulfuratus) y monos araña (Ateles geoffroyi) / Germination of Ficus insipida (Moraceae) seeds from toucan (Ramphastos sulfuratus) and spider monkey (Ateles geoffroyi) feces

To test the null hypothesis that two vertebrate fructivores, toucans (Ramphastos sulfuratus) and spider monkeys (Ateles geoffroyi), are equally specialized in germinating Ficus insipida seeds after these have passed through their digestive tracts, we fed fruits to captive individuals. We extracted seeds from feces and placed them on filter paper in petri dishes under controled light, temperature and humidity. Control seeds had not passed through a digestive tract. We found that a greater proportion of seeds from A. geofroyi (65%) germinated (R. sulfuratus: 4%). The germinative value was also greater in seeds from monkey feces (rate=13.76; toucan 0.046; control group 0.172). If, despite individual variability of seeds and dispersers, future studies continue to show that A. geoffroyi favors germination more (maybe because of a longer digestion time), this would indicate that diet specialization is not necessarily related to dispersal efficiency.

Con el objetivo de evaluar y comparar el efecto que tiene el paso de las semillas del higo Ficus insipida Willd (Moraceae), por el tracto digestivo de dos especies de vertebrados frugívoros, se ofrecieron frutos a individuos cautivos de tucán (Ramphastos sulfuratus: Ramphastidae) y de mono araña (Ateles geoffroyi: Cebidae), en la hipótesis de que siendo ambos frugívoros especialistas deberían favorecer de manera similar a la germinación de semillas de esta especie arbórea. De las heces se separaron las semillas y se pusieron a germinar en cajas petri en condiciones controladas de luz, temperatura y humedad, con una muestra de semillas testigo que no pasaron por el tracto digestivo de ningún animal. Se calculó la latencia, la capacidad y velocidad de geminación, y el valor germinativo de las semillas de cada grupo experimental. El 65% de las semillas de frutos de F. insipida consumidos por A. geofroyi germinaron con éxito, mientras que de las obtenidas de las heces de tucán, apenas el 4% logró germinar. El valor germinativo fue mayor en las semillas extraídas de excretas de mono (índice=13.76), en comparación con las de tucán (0.046) y las del grupo testigo (0.172). A. geoffroyi fue la especie que favoreció más la germinación de semillas de F. insipida, siendo probable que esta condición se relacione con el mayor tiempo de digestión de este primate. Deberá considerarse ambién la dificultad de establecer siempre concordancia con estos resultados, debido a la gran variabilidad en la capacidad germinativa de las semillas de individuos arbóreos, a la diferencia entre las cosechas y periodos de fructificación, así como en la madurez y estado fisiológico de los animales utilizados en las pruebas. Se concluye que la especialización alimentaria no necesariamente se relaciona con la efectividad de la calidad de la dispersión.

Distribution, ecology, life history, genetic variation, and risk of extinction of nonhuman primates from Costa Rica

We examined the association between geographic distribution, ecological traits, life history, genetic diversity, and risk of extinction in nonhuman primate species from Costa Rica. All of the current nonhuman primate species from Costa Rica are included in the study; spider monkeys (Ateles geoffroyi), howling monkeys (Alouatta palliata), capuchins (Cebus capucinus), and squirrel monkeys (Saimiri oerstedii). Geographic distribution was characterized accessing existing databases. Data on ecology and life history traits were obtained through a literature review. Genetic diversity was characterized using isozyme electrophoresis. Risk of extinction was assessed from the literature. We found that species differed in all these traits. Using these data, we conducted a Pearson correlation between risk of extinction and ecological and life history traits, and genetic variation, for widely distributed species. We found a negative association between risk of extinction and population birth and growth rates; indicating that slower reproducing species had a greater risk of extinction. We found a positive association between genetic variation and risk of extinction; i.e., species showing higher genetic variation had a greater risk of extinction. The relevance of these traits for conservation efforts is discussed.

Some observations on the present distribution and conservation of Alouatta and Ateles in Southern Mexico.

Some information on the past and present distribution of Alouatta and Ateles in southern Mexico and on the impact of habitat destruction on their future existence is presented. Three surveys of primate populations and forest habitats were carried out between 1981 and 1983 in southeastern Mexico. Rapid destruction of the forest is reducing the number of forested areas where Alouatta and Ateles can exist and co-occur. Illegal hunting of the two primates also contributes to their rapid decline. Alouatta and Ateles live a precarious existence in a few large and small islands of forest, and efforts are needed to set aside some of these areas as reserves so that their future survival is ensured.