The rapid loss, fragmentation and degradation of tropical forests threaten the survival of many animal species. However, the way in which these phenomena affect animal health has been poorly explored, thus limiting the design of appropriate conservation strategies. To address this, here we identified using linear mixed models the effect of proximal (diet, activity pattern, hunting and logging) and distal (sum of the basal areas of fruiting-tree species [SBAFS], landscape forest cover and degree of forest fragmentation) variables over fecal glucocorticoid metabolite (fGCM) levels–hormones associated with animal health and fitness–of six groups of spider monkeys (Ateles geoffroyi) inhabiting six landscapes with different spatial structures in Mexico. Proximal variables showed a stronger predictive power over fGCMs than distal. In this sense, increases in travel time, the occurrence of hunting, and reductions in rest time and fruit consumption resulted in higher fGCM levels. Regarding distal variables, increases in SBAFS were negatively related to fGCM levels, thus suggesting that food scarcity increases stress hormone levels. Nevertheless, contrary to theoretical expectations, spider monkeys living in smaller tracts of forest spent less time travelling, but the same time feeding on fruit as those in more forested areas. The lower net energy return associated with this combination of factors would explain why, contrary to theoretical expectations, increased forest cover was associated with increased levels of fGCMs in these groups. Our study shows that, at least in the short term, spider monkeys in fragmented landscapes do not always present higher levels of stress hormones compared to those inhabiting continuous forest, and the importance of preserving fruit sources and controlling hunting for reducing the levels of stress hormones in free ranging spider monkeys.
Understanding the response of species to changes in landscape configuration is required to design adequate management and conservation strategies. Yet, the most appropriate spatial scale (i.e., landscape size) to assess the response of species to changes in landscape configuration (so-called "scale of effect") is largely unknown. In this paper, we assess the impact of landscape forest cover, forest fragmentation, edge density, and inter-patch isolation distance on the diet and behavior of six communities of spider monkeys (Ateles geoffroyi) in the fragmented Lacandona rainforest, Mexico. We evaluated the strength of the relationship between each landscape predictor and each response variable within ten different-sized landscapes (range = 50-665 ha) to identify the landscape size that best predicted changes in diet and behavior. The strength of most associations varied across spatial scales, with the 126-ha landscape showing the strongest relationships between landscape predictors and response variables in many cases. Yet forest cover represented the main driver of the diet and behavior of spider monkeys, being positively associated with time traveling and time feeding on wood, but negatively related to time resting and time feeding on leaves. Although weaker, the impact of edge density was opposite to forest cover for most response variables. Forest fragmentation and isolation distance showed the weakest associations with the diet and behavior of this species. Our findings thus indicate that different landscape attributes operate on different response variables at different spatial scales. Therefore, the scale of effects cannot be generalized to all response variables and to all predictors, and a multi-scale analysis will be required to accurately assess the impact of landscape configuration on species' responses.
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).
Due to several factors such as ecological conditions, group size, and social organization, primates frequently spend time out of visual contact with individuals of their own group. Through the use of long-distance vocalizations, often termed "contact calls," primates are able to maintain contact with out-of-sight individuals. Contact calls have been shown to be individually distinct, and reverberation and attenuation provide information about caller distance. It is less clear, however, whether callers actively change the structure of contact calls depending on the distance to the presumed listeners. We studied this question in spider monkeys (Ateles geoffroyi), a species with complex spatial dynamics (fission-fusion society) that produces highly frequency modulated contact calls, denominated "whinnies." We determined the acoustic characteristics of 566 whinnies recorded from 35 free-ranging spider monkeys that belong to a community located in Mexico, and used cluster analyses, discriminant function analyses, and generalized linear mixed models to assess if they varied in relation to the presumed distance to the listener. Whinnies could be grouped into five subtypes. Since the lowest frequency subtype was mainly produced by spider monkeys that exchanged whinnies at longer distances, and lower frequency calls propagate across longer distances, our results suggest that whinnies vary in order to enhance vocal contact between individuals separated by different distances. Our results also revealed that whinnies convey potential information about caller immediate behaviors and corroborated that these calls are individually distinct. Overall, our results suggest that whinny acoustic variation facilitates the maintenance of vocal contact between individuals living in a society with complex spatial dynamics.
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