Arturo González-Zamora

Diet of spider monkeys (Ateles geoffroyi) in Mesoamerica: current knowledge and future directions.

Here we review all published articles and book chapters, as well as unpublished theses and data of Ateles geoffroyi diet to (1) summarize the literature; (2) synthesize general feeding patterns; (3) document plant taxonomic similarity in diet across study sites; and (4) suggest directions for future research and conservation priorities. We found 22 samples from five countries: Mexico, Guatemala, El Salvador, Costa Rica and Panama. Tropical wet forest is the most studied habitat (N=13 samples), followed by tropical dry forest (6) and tropical moist forest (3). Most samples have been carried out in large protected forests. In spite of showing an overall high dietetic diversity (364 species, 76 families), A. geoffroyi concentrated the majority of feeding time on a few species in the families Moraceae and Fabaceae. At all study sites fruits were the most common food item in the diet followed by leaves. Furthermore, a greater variety of food items and less fruit were consumed in forest fragments. These findings suggest that fruit shortage in fragments results in primates using foods of presumably lower energetic content such as leaves. Similarity in diet was higher among groups geographically closer to each other than among distant groups, showing that the floristic and phenological characteristics of the forest can influence diet composition. We conclude that several years of data are required to fully describe the dietary list of A. geoffroyi at any one site, as studies of the same group over different years shared as little as 56% of species. As most populations of A. geoffroyi live in highly fragmented landscapes, it is crucial to carry out studies in these areas to evaluate (1) changes in diet and activity patterns that may negatively affect survival; and (2) habitat attributes that may favor their persistence in altered landscapes. Am. J. Primatol. 71:8–20, 2009.

Influence of climatic variables, forest type, and condition on activity patterns of geoffroyi's spider monkeys throughout Mesoamerica

Understanding how species cope with variations in climatic conditions, forest types and habitat amount is a fundamental challenge for ecologists and conservation biologists. We used data from 18 communities of Mesoamerican spider monkeys (Ateles geoffroyi) throughout their range to determine whether their activity patterns are affected by climatic variables (temperature and rainfall), forest types (seasonal and nonseasonal forests), and forest condition (continuous and fragmented). Data were derived from 15 published and unpublished studies carried out in four countries (Mexico, El Salvador, Costa Rica, and Panama), cumulatively representing more than 18 years (221 months, >3,645 hr) of behavioral observations. Overall, A. geoffroyi spent most of their time feeding (38.4 ± 14.0%, mean ± SD) and resting (36.6 ± 12.8%) and less time traveling (19.8 ± 11.3%). Resting and feeding were mainly affected by rainfall: resting time increased with decreasing rainfall, whereas feeding time increased with rainfall. Traveling time was negatively related to both rainfall and maximum temperature. In addition, both resting and traveling time were higher in seasonal forests (tropical dry forest and tropical moist forest) than in nonseasonal forests (tropical wet forest), but feeding time followed the opposite pattern. Furthermore, spider monkeys spent more time feeding and less time resting (i.e., higher feeding effort) in forest fragments than in continuous forest. These findings suggest that global climate changes and habitat deforestation and fragmentation in Mesoamerica will threaten the survival of spider monkeys and reduce the distributional range of the species in the coming decades. Am. J. Primatol. 73:1189–1198, 2011.

Sleeping Sites and Latrines of Spider Monkeys in Continuous and Fragmented Rainforests: Implications for Seed Dispersal and Forest Regeneration

Spider monkeys (Ateles geoffroyi) use sites composed of one or more trees for sleeping (sleeping sites and sleeping trees, respectively). Beneath these sites/trees they deposit copious amounts of dung in latrines. This behavior results in a clumped deposition pattern of seeds and nutrients that directly impacts the regeneration of tropical forests. Therefore, information on the density and spatial distribution of sleeping sites and latrines, and the characteristics (i.e., composition and structure) of sleeping trees are needed to improve our understanding of the ecological significance of spider monkeys in influencing forest composition. Moreover, since primate populations are increasingly forced to inhabit fragmented landscapes, it is important to assess if these characteristics differ between continuous and fragmented forests. We assessed this novel information from eight independent spider monkey communities in the Lacandona rainforest, Mexico: four continuous forest sites and four forest fragments. Both the density of sleeping sites and latrines did not differ between forest conditions. Latrines were uniformly distributed across sleeping sites, but the spatial distribution of sleeping sites within the areas was highly variable, being particularly clumped in forest fragments. In fact, the average inter-latrine distances were almost double in continuous forest than in fragments. Latrines were located beneath only a few tree species, and these trees were larger in diameter in continuous than fragmented forests. Because latrines may represent hotspots of seedling recruitment, our results have important ecological and conservation implications. The variation in the spatial distribution of sleeping sites across the forest indicates that spider monkeys likely create a complex seed deposition pattern in space and time. However, the use of a very few tree species for sleeping could contribute to the establishment of specific vegetation associations typical of the southeastern Mexican rainforest, such as Terminalia-Dialium, and Brosimum-Dialium.

Contagious Deposition of Seeds in Spider Monkeys' Sleeping Trees Limits Effective Seed Dispersal in Fragmented Landscapes

The repeated use of sleeping sites by frugivorous vertebrates promotes the deposition and aggregation of copious amounts of seeds in these sites. This spatially contagious pattern of seed deposition has key implications for seed dispersal, particularly because such patterns can persist through recruitment. Assessing the seed rain patterns in sleeping sites thus represents a fundamental step in understanding the spatial structure and regeneration of plant assemblages. We evaluated the seed rain produced by spider monkeys (Ateles geoffroyi) in latrines located beneath 60 sleeping trees in two continuous forest sites (CFS) and three forest fragments (FF) in the Lacandona rainforest, Mexico. We tested for differences among latrines, among sites, and between forest conditions in the abundance, diversity (α-, β- and, γ-components) and evenness of seed assemblages. We recorded 45,919 seeds ≥5 mm (in length) from 68 species. The abundance of seeds was 1.7 times higher in FF than in CFS, particularly because of the dominance of a few plant species. As a consequence, community evenness tended to be lower within FF. β-diversity of common and dominant species was two times greater among FF than between CFS. Although mean α-diversity per latrine did not differ among sites, the greater β-diversity among latrines in CFS increased γ-diversity in these sites, particularly when considering common and dominant species. Our results support the hypothesis that fruit scarcity in FF can ‘force’ spider monkeys to deplete the available fruit patches more intensively than in CFS. This feeding strategy can limit the effectiveness of spider monkeys as seed dispersers in FF, because (i) it can limit the number of seed dispersers visiting such fruit patches; (ii) it increases seed dispersal limitation; and (iii) it can contribute to the floristic homogenization (i.e., reduced β-diversity among latrines) in fragmented landscapes.

Habitat-population density relationship for the white-tailed deer Odocoileus virginianus during the dry season in a Pacific Mexican tropical dry forest

Abstract The habitat-population density relationship in the white-tailed deer Odocoileus virginianus was analyzed in a tropical dry forest of the Zicuirán-Infiernillo Biosphere Reserve in the Pacific region of Mexico. In 2008, pellet groups were sampled in strip-transects during the dry season to estimate population density in five locations. Habitat variables (physical, vegetation, and human) were obtained during field sampling and through the use of geographic information systems. Principal component analysis and stepwise multiple regression were used to analyze the habitat-density relationships. The mean population density of white-tailed deer for the region was 6.7 ind/km2; however, this varied significantly among sites (1.9–11.3 ind/km2). Higher densities were found in sites with lower human activity, irregular topography, dense understory cover, and well-developed tree strata. In contrast, sites with lower deer density presented high human activities such as livestock and crop production, which act to modify the tropical dry forest. We discuss the management and conservation implications.

Spider Monkeys in Human-Modified Landscapes: The Importance of the Matrix

With the extant of tropical forest degradation, primates increasingly inhabit forest patches embedded in anthropogenic matrices. Such matrices are composed of different land cover types (e.g., agricultural lands and cattle pastures), but large uncertainty remains about the ability of primates to use these land covers. Here, we assessed the use of the landscape matrix by spider monkeys (Ateles geoffroyi) in 13 forest sites from three countries (Mexico, Costa Rica, and El Salvador). Based on ad libitum records from >212 months of field observations, we found that spider monkeys used four types of land covers for feeding or traveling: secondary vegetation, isolated trees, tree crops, and vegetation corridors. Secondary vegetation was more frequently used than the other land covers. The number of land covers present in the matrix was positively related to the number of land covers used for traveling and feeding. Monkeys consumed 53 plant species in the matrix, mostly native and old-growth or late-successional forest species, although they also used three cultivated tree species. Most species were trees, especially from preferred food species, although monkeys also used palms, lianas, and shrubs. Monkeys fed principally from fruits, but they also used leaves, wood, and flowers. Most species were used from secondary vegetation and isolated trees. These findings suggest that the landscape matrix can provide supplementary food sources for this endangered primate and opportunities for traveling (i.e., spatial connectivity) in human-modified landscapes—information that can be used to improve conservation strategies, especially under the context of land-sharing management strategies (e.g., agroforestry).

Sleeping-tree fidelity of the spider monkey shapes community-level seed-rain patterns in continuous and fragmented rain forests

Repeated use of sleeping trees (STs) by frugivores promotes the deposition and aggregation of copious amounts of seed, thus having key implications for seed dispersal and forest regeneration. Seed-rain patterns produced by this behaviour likely depend on the frequency of use of these sites, yet this hypothesis has been poorly tested. We evaluated community-level seed-rain patterns produced by the spider monkey (Ateles geoffroyi) over 13 mo in latrines located beneath 60 STs in the Lacandona rain forest, Mexico. Because this primate is increasingly ‘forced’ to inhabit fragmented landscapes, we tested whether sleeping-tree fidelity (STF) differed among sites and between continuous and fragmented forests. We also tested whether seed-rain patterns were associated with STF within each site and forest type. STF was highly variable among STs (average = 7 mo, range = 1–12 mo), but did not differ among study sites or forest types. STF was positively associated with seed abundance, species diversity and species turnover. Nevertheless, STF tended to be negatively related to seed community evenness. These results are likely due to the most frequently used STs being in areas with greater food density. Our results demonstrate that site fidelity shapes community-level seed-rain patterns and thus has key ecological implications.

Isolation and Characterization of Polymorphic Microsatellite Loci in Spondias radlkoferi (Anacardiaceae)

Premise of the study: Microsatellite markers were developed for Spondias radlkoferi to assess the impact of primate seed dispersal on the genetic diversity and structure of this important tree species of Anacardiaceae. Methods and Results: Fourteen polymorphic loci were isolated from S. radlkoferi through 454 GS-FLX Titanium pyrosequencing of genomic DNA. The number of alleles ranged from three to 12. The observed and expected heterozygosities ranged from 0.382 to 1.00 and from 0.353 to 0.733, respectively. The amplification was also successful in S. mombin and two genera of Anacardiaceae: Rhus aromatica and Toxicodendron radicans. Conclusions: These microsatellite loci will be useful to assess the genetic diversity and population structure of S. radlkoferi and related species, and will allow us to investigate the effects of seed dispersal by spider monkeys (Ateles geoffroyi) on the genetic structure and diversity of S. radlkoferi populations in a fragmented rainforest.

Parent-parent and parent-offspring distances in Spondias radlkoferi seeds suggest long-distance pollen and seed dispersal: evidence from latrines of the spider monkey

Pollen and seed dispersal are key ecological processes, directly impacting the spatial distribution, abundance and genetic structure of plant populations; yet, pollen- and seed-dispersal distances are poorly known. We used molecular markers to identify the parental origin (n = 152 adult trees) of 177 Spondias radlkoferi (Anacardiaceae) seeds deposited by the spider monkey ( Ateles geoffroyi ) in latrines located beneath 17 sleeping-trees in two continuous forest sites (CF) and two forest fragments (FF) in the Lacandona rain forest, Mexico. We estimated mean parent-offspring (PO) distances per latrine and, for those seeds (54% of seeds) with more than one candidate parent (i.e. the potential maternal and parental parents), we also estimated parent-parent (PP) distances per latrine, and tested if PO and PP distances differed between forest types. Global PO and PP distances per latrine averaged 682 m (range = 83–1741 m) and 610 m (range = 74–2339 m), respectively, and did not differ significantly between CF and FF. This suggests that pollen dispersal is extensive in both forest types and that long seed dispersal distances (>100 m) are common, thus supporting the hypothesis that the spider monkey is an effective seed disperser of S. radlkoferi in continuous and fragmented forests.