Let's not use it! A dynamic no-use zone between the home ranges of two spider monkey groups.

It is common that neighboring groups of the same species use some of the same areas, resulting in home-range overlap. Areas between the home ranges of neighboring groups not used by either group (no-use zone or NUZ) are rarely reported. Here, we report the existence of a NUZ between the home ranges of two Geoffroy's spider monkey groups, and examine its spatial changes over time and the ecological and behavioral underpinnings of such phenomenon. Although its size and location changed between 2017 and 2022, the NUZ was always present. We did not find any differences in the vegetation structure and composition between the NUZ and the ranging areas and in the monkeys' activity patterns between areas adjacent to the NUZ and the other parts of the ranging areas. The number of monkey vocalizations was lower and subgroup size was smaller (although the number of males did not differ) in areas adjacent to the NUZ than in the other parts of the ranging areas. Both changes possibly reflect the tendency to conceal their presence to the neighboring group. Our findings contribute to the understanding of primate space use and highlight the need to focus on the areas delimiting home ranges.

SARS-CoV-2 infection in brown-headed spider monkeys (Ateles fusciceps) at a wildlife rescue center on the coast of Ecuador-South America.

Human populations can be affected in unpredictable ways by the emergence and spread of zoonotic diseases. The COVID-19 (coronavirus disease of 2019) pandemic was a reminder of how devastating these events can be if left unchecked. However, once they have spread globally, the impact of these diseases when entering non-exposed wildlife populations is unknown. The current study reports the infection of brown-headed spider monkeys (Ateles fusciceps) at a wildlife rescue center in Ecuador. Four monkeys were hospitalized, and all tested positive for SARS-CoV-2 (Severe acute respiratory syndrome coronavirus 2) by RT-qPCR (Quantitative Reverse Transcription PCR). Fecal samples (n = 12) from monkeys at the rescue center also tested positive; three zookeepers responsible for feeding and deworming the monkeys also tested positive, suggesting human-animal transmission. Whole genome sequencing identified most samples' omicron clade 22B BA.5 lineage. These findings highlight the threat posed by an emerging zoonotic disease in wildlife species and the importance of preventing spillover and spillback events during epidemic or pandemic events.IMPORTANCEAlthough COVID-19 (coronavirus disease of 2019) has been primarily contained in humans through widespread vaccination, the impact and incidence of SARS-CoV-2 (Severe acute respiratory syndrome coronavirus) and its transmission and epidemiology in wildlife may need to be addressed. In some natural environments, the proximity of animals to humans is difficult to control, creating perfect scenarios where susceptible wildlife can acquire the virus from humans. In these places, it is essential to understand how transmission can occur and to develop protocols to prevent infection. This study reports the infection of brown-headed spider monkeys with SARS-CoV-2, a red-listed monkey species, at a wildlife recovery center in Ecuador. This study reports the infection of brown-headed spider monkeys with SARS-CoV-2, indicating the potential for transmission between humans and wildlife primates and the importance of preventing such events in the future.

First whole-genome sequence and assembly of the Ecuadorian brown-headed spider monkey (Ateles fusciceps fusciceps), a critically endangered species, using Oxford Nanopore Technologies.

The Ecuadorian brown-headed spider monkey (Ateles fusciceps fusciceps) is currently considered one of the most endangered primates in the world and is classified as critically endangered [International union for conservation of nature (IUCN)]. It faces multiple threats, the most significant one being habitat loss due to deforestation in western Ecuador. Genomic tools are keys for the management of endangered species, but this requires a reference genome, which until now was unavailable for A. f. fusciceps. The present study reports the first whole-genome sequence and assembly of A. f. fusciceps generated using Oxford Nanopore long reads. DNA was extracted from a subadult male, and libraries were prepared for sequencing following the Ligation Sequencing Kit SQK-LSK112 workflow. Sequencing was performed using a MinION Mk1C sequencer. The sequencing reads were processed to generate a genome assembly. Two different assemblers were used to obtain draft genomes using raw reads, of which the Flye assembly was found to be superior. The final assembly has a total length of 2.63 Gb and contains 3,861 contigs, with an N50 of 7,560,531 bp. The assembly was analyzed for annotation completeness based on primate ortholog prediction using a high-resolution database, and was found to be 84.3% complete, with a low number of duplicated genes indicating a precise assembly. The annotation of the assembly predicted 31,417 protein-coding genes, comparable with other mammal assemblies. A reference genome for this critically endangered species will allow researchers to gain insight into the genetics of its populations and thus aid conservation and management efforts of this vulnerable species.

Serological evidence for potential yellow fever virus infection in non-human primates, southeastern Mexico.

BACKGROUND: Arthropod-borne flaviviruses like dengue virus (DENV) and yellow fever virus (YFV) are major human pathogens. In Latin America, YFV is maintained in sylvatic cycles involving non-human primates (NHP) and forest-dwelling mosquitos. YFV supposedly does not circulate north of Panama. METHODS: We conducted a serologic study for flaviviruses and other emerging viruses in NHP from southeastern Mexico. A total of thirty sera of black-handed spider monkeys (Ateles geoffroyi, n = 25), black howler monkeys (Alouatta pigra, n = 3), and mantled howler monkeys (Al. palliata, n = 2) sampled in 2012 and 2018 were screened by an indirect immunofluorescence assay (IFA) to detected IgG antibodies against DENV, YFV, Zika virus (ZIKV), West Nile virus (WNV), Rift Valley fever virus, Crimean-Congo hemorrhagic fever virus, Middle East respiratory syndrome coronavirus, and Zaire Ebola virus, and confirmed by plaque reduction neutralization tests (PRNT90) representing all mosquito-borne flavivirus serocomplexes circulating in the Americas. RESULTS: A total of 16 sera (53.3%; 95% CI, 34.3-71.7) showed IFA reactivity to at least one tested flavivirus with end-point titers ranging from 1:100 to 1:1000. No serum reacted with other viruses. Monotypic and high mean PRNT90 endpoint YFV titers of 1:246 were found in 3 black-handed spider monkey sera (10.0%; 95% CI, 2.1-26.5) sampled in 2018 in Tabasco, compared to all other flaviviruses tested. Monotypic endpoint PRNT90 titers of 1:28 for Ilheus virus and 1:22 for WNV in serum of black howler monkeys sampled in 2018 in Tabasco suggested additional flavivirus exposure. CONCLUSIONS: Our findings may suggest unnoticed YFV circulation. Intensification of YFV surveillance in NHP and vectors is warranted in Mexico and potentially other areas considered free of yellow fever.

Exploring the Relationship between Spontaneous Sister Chromatid Exchange and Genome Instability in Two Cryptic Species of Non-Human Primates.

There are extensive studies on chromosome morphology and karyotype diversity in primates, yet we still lack insight into genomic instability as a key factor underlying the enormous interspecies chromosomal variability and its potential contribution to evolutionary dynamics. In this sense, the assessment of spontaneous sister chromatid exchange (SCE) frequencies represents a powerful tool for evaluating genome stability. Here, we employed G-banding, fluorescence plus Giemsa (FPG), and chromosome orientation fluorescence in situ hybridization (CO-FISH) methodologies to characterize both chromosome-specific frequencies of spontaneously occurring SCE throughout the genome (G-SCE) and telomere-specific SCE (T-SCE). We analyzed primary fibroblast cultures from two male species of Ateles living in captivity: Ateles paniscus (APA) and Ateles chamek (ACH). High frequencies of G-SCEs were observed in both species. Interestingly, G-SCEs clustered on evolutionary relevant chromosome pairs: ACH chromosomes 1, 2, 3, 4, and 7, and APA chromosomes 1, 2, 3, 4/12, 7, and 10. Furthermore, a statistically significant difference between the observed and expected G-SCE frequencies, not correlated with chromosome size, was also detected. CO-FISH analyses revealed the presence of telomere-specific recombination events in both species, which included T-SCE, as well as interstitial telomere signals and telomere duplications, with APA chromosomes displaying higher frequencies, compared to ACH. Our analyses support the hypothesis that regions of Ateles chromosomes susceptible to recombination events are fragile sites and evolutionary hot spots. Thus, we propose SCE analyses as a valuable indicator of genome instability in non-human primates.

How visitation affects the behavior and welfare of different species of captive amazonian primates? / Como a visitação afeta o comportamento e o bem-estar de diferentes espécies de primatas cativos da Amazônia? / ¿Cómo visitas afectan el comportamiento y bienestar de diferentes especies de primates en cautiverio en Amazonia?

This study had the purpose of understanding the effects of visitation on behavioral patterns and on the well-being of primates in captivity. Five Amazonian primate species were observed using the focal animal method: Ateles chamek, Ateles belzebuth, Ateles paniscus, Lagothrix cana, and Sapajus apella. Two categories of visitor behavioral observations were adopted - active and passive. From the total number of records, the behavior of primates could be observed in 53.7% of the notes in the presence of visitors. The behavior of the visitors in front of the cages was considered passive in 91.2% of those records. The three species of Ateles reacted in different ways in the presence and absence of visitors. The type of visitor behavior had influence on the behavior of the primate (Chi-square=22.9, p<0.001). Stress indicating behaviors (CIE) represented 3.3% of the behavioral repertoire of the species (n=253 records). The primates presented a varied number of CIE, which included indexes of reduced well-being levels. A. belzebuth was ranked first as the species most affected by visitation. These results show the importance of understanding the stress effects on the behavioral pattern of captive primates in relation to visitation and other factors, leading to alternative actions for the zoo in order to improve the level of their welfare.(AU)

O entendimento dos efeitos da visitação nos padrões comportamentais e no bem-estar dos primatas em cativeiro foi o objetivo deste estudo. Por meio do método animal focal foram realizadas observações de cinco espécies de primatas amazônicos: Ateles chamek, Ateles belzebuth, Ateles paniscus, Lagothrix cana e Sapajus apella. Para observações comportamentais dos visitantes, foram adotadas duas categorias, ativo e passivo. Do total de registros, encontrou-se que os comportamentos dos primatas foram exibidos em 53,7% das anotações na presença de visitantes. O comportamento dos visitantes diante dos recintos foi em 91,2% considerado passivo. As três espécies de Ateles reagiram de formas diferentes na presença e ausência de visitantes. O tipo de comportamento dos visitantes teve influência no comportamento dos primatas (Chi-quadrado=22,9, p<0,001). Os comportamentos indicadores de estresse (CIE) representaram 3,3% do repertório comportamental das espécies (n=253 registros). Os primatas apresentaram um número variado de CIE, apresentando indicadores de reduzido grau de bem-estar. A. belzebuth esteve em primeiro lugar no ranking das espécies mais afetadas pela visitação. Estes resultados mostraram a importância de compreender os efeitos do estresse no padrão comportamental dos primatas cativos relacionados a visitação e outros fatores, levando ao zoológico alternativas que conduzam a ações para melhorar o grau de bem-estar.(AU)

Comprender los efectos de visitaciones en los estándares comportamentales y en el bienestar de los primates en cautiverio fue el objetivo de este estudio. Mediante el método de animales focales se realizaron observaciones en cinco especies de primates amazónicos: Ateles chamek, Ateles belzebuth, Ateles paniscus, Lagothrix cana y Sapajus apella. Para observaciones comportamentales de los visitantes, se adoptaron dos categorías, activa y pasiva. Del total de registros, se encontró que los comportamientos de los primates se mostraron en 53,7% de las notas en presencia de visitantes. El comportamiento de los visitantes frente a los recintos fue considerado pasivo en un 91,2%. Las tres especies de Ateles reaccionaron de manera diferente a la presencia y ausencia de visitantes. El tipo de comportamiento de los visitantes influyó en el comportamiento de los primates (Chi-cuadrado=22,9, p<0,001). Los comportamientos indicadores de estrés (CIE) representaron el 3,3% del repertorio conductual de la especie (n=253 registros). Los primates presentaron un número variado de CIE, mostrando indicadores de un reducido grado de bienestar. A. belzebuth ocupó el primer lugar en el ranking de las especies más afectadas por las visitas. Estos resultados mostraron la importancia de comprender los efectos del estrés en el estándar comportamental de los primates en cautivos relacionados con las visitas y otros factores, llevando al zoológico alternativas que conduzcan a acciones para mejorar el grado de bienestar.(AU)

Should I stay or should I go? How activity synchronization affects fission decisions.

Group-living animals need to deal with conflicting interests to maintain cohesion. When the costs of doing so outweigh the benefits, the group may (temporarily) split into two or more subgroups. Conflicting interests can concern what activity to pursue or the direction of travel. Temporary group separation is a common feature in species with a high degree of fission-fusion dynamics. We investigated the role activity synchronization played in fission decisions in a spider monkey group living in the Otoch Ma'ax Yetel Kooh Nature Reserve, Yucatan, Mexico. For 21 months, we recorded every fission event occurring in the followed subgroup, as well as the subgroup activity. We classified the activity as 'synchronized' when at least 75% of subgroup members performed the same activity (resting, foraging, socializing or travelling); otherwise, we classified it as 'non-synchronized'. We found that fission events occurred more often when the activity was non-synchronized. In addition, when the activity was synchronized, fission events occurred more often when spider monkeys were travelling than when they were engaged in other subgroup activities. Our findings highlight the role of conflicting interests over the activity to pursue and travel direction in fission decisions.

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.

Seasonal and sex differences in the fission-fusion dynamics of spider monkeys (Ateles geoffroyi yucatanensis) in Belize.

Spider monkeys (Ateles sp.) are characterized by high fission-fusion dynamics, meaning their social grouping pattern is fluid and consists of subgroups that vary in size, composition, and spatial cohesion over time. In this study, we quantify the fission-fusion dynamics of a group of spider monkeys at Runaway Creek Nature Reserve in Belize by measuring subgroup size, spatial cohesion, and stability using data spanning 5 years. We then test whether variation in these three subgroup measures differ according to season, subgroup sex composition, and the reproductive status of female subgroup members. Our results show that subgroups were larger in size and less stable in membership during the wet season compared to the dry season. All-female subgroups were less spatially cohesive but more stable in membership than all-male subgroups. Finally, we report that subgroups with one or more non-lactating females (i.e., without nursing young) were smaller on average than subgroups containing lactating females with nursing young. These data contribute to a growing body of research documenting the ecological and social dimensions along which grouping patterns might vary.

Predation Attacks on Wild Spider Monkeys (Ateles geoffroyi).

We report 2 cases of predation on an adult and a subadult spider monkey (Ateles geoffroyi) by a puma (Puma concolor) and an unidentified terrestrial predator at the natural protected area of Otoch Ma'ax yetel Kooh, in the Yucatan Peninsula, Mexico. Although spider monkeys are believed to experience overall low predation pressure compared to other primate species, our observations show that predation occurs in the study area and therefore behavioral strategies are likely to be in place to reduce predation risk. Our observations are further evidence that terrestrial predators are a threat for both young and full-grown spider monkeys.

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.

The influence of anthropogenic edge effects on primate populations and their habitat in a fragmented rainforest in Costa Rica.

When a forest is fragmented, this increases the amount of forest edge relative to the interior. Edge effects can lead to loss of animal and plant species and decreased plant biomass near forest edges. We examined the influence of an anthropogenic forest edge comprising cattle pasture, coconut plantations, and human settlement on the mantled howler (Alouatta palliata), white-faced capuchin (Cebus capucinus), Central American spider monkey (Ateles geoffroyi), and plant populations at La Suerte Biological Research Station (LSBRS), Costa Rica. We predicted that there would be lower monkey encounter rate, mean tree species richness, and diameter at breast height (DBH) in forest edge versus interior, and that monkeys would show species-specific responses to edge based on diet, body size, and canopy height preferences. Specifically, we predicted that howler monkeys would show positive or neutral edge effects due to their flexible folivorous diet, large body size, and preference for high canopy, capuchins would show positive edge effects due to their diverse diet, small body size, and preference for low to middle canopy, and spider monkeys would show negative edge effects due their reliance on ripe fruit, large body size, and preference for high upper canopy. We conducted population and vegetation surveys along edge and interior transects at LSBRS. Contrary to predictions, total monkey encounter rate did not vary between the forest edge and forest interior. Furthermore, all three species showed neutral edge effects with no significant differences in encounter rate between forest edge and interior. Interior transects had significantly higher mean tree species richness than edge transects, and interior trees had greater DBH than edge trees, although this difference was not significant. These results suggest that forest edges negatively impact plant populations at La Suerte but that the monkeys are able to withstand these differences in vegetation.

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.

Sustainability and comanagement of subsistence hunting in an indigenous reserve in Guyana.

Although hunting is a key component of subsistence strategies of many Amazonians, it is also one of the greatest threats to wildlife. Because indigenous reserves comprise over 20% of Amazonia, effective conservation often requires that conservation professionals work closely with indigenous groups to manage resource use. We used hunter-generated harvesting data in spatially explicit biodemographic models to assess the sustainability of subsistence hunting of indigenous Waiwai in Guyana. We collected data through a hunter self-monitoring program, systematic follows of hunters, and semistructured interviews. We used these data to predict future densities of 2 indicator species, spider monkeys (Ateles paniscus) and bearded sakis (Chiropotes sagulatus), under different scenarios of human population expansion and changing hunting technology. We used encounter rates from transect surveys and hunter catch-per-unit effort (CPUE) to validate model predictions. Paca (Cuniculus paca) (198 /year), Currosaw (Crax alector) (168), and spider monkey (117) were the most frequently harvested species. Predicted densities of spider monkeys were statistically indistinguishable from empirically derived transect data (Kolmogorov-Smirnov D = 0.67, p = 0.759) and CPUE (D = 0.32, p = 1.000), demonstrating the robustness of model predictions. Ateles paniscus and C. sagulatus were predicted to be extirpated from <13% of the Waiwai reserve in 20 years, even under the most intensive hunting scenarios. Our results suggest Waiwai hunting is currently sustainable, primarily due to their low population density and use of bow and arrow. Continual monitoring is necessary, however, particularly if human population increases are accompanied by a switch to shotgun-only hunting. We suggest that hunter self-monitoring and biodemographic modeling can be used effectively in a comanagement approach in which indigenous parabiologists continuously provide hunting data that is then used to update model parameters and validate model predictions.

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.

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.