Better few than hungry: flexible feeding ecology of collared lemurs Eulemur collaris in littoral forest fragments

Background

Frugivorous primates are known to encounter many problems to cope with habitat degradation, due to the fluctuating spatial and temporal distribution of their food resources. Since lemur communities evolved strategies to deal with periods of food scarcity, these primates are expected to be naturally adapted to fluctuating ecological conditions and to tolerate a certain degree of habitat changes. However, behavioral and ecological strategies adopted by frugivorous lemurs to survive in secondary habitats have been little investigated. Here, we compared the behavioral ecology of collared lemurs (Eulemur collaris) in a degraded fragment of littoral forest of south-east Madagascar, Mandena, with that of their conspecifics in a more intact habitat, Sainte Luce.

Methodology/Principal Findings

Lemur groups in Mandena and in Sainte Luce were censused in 2004/2007 and in 2000, respectively. Data were collected via instantaneous sampling on five lemur groups totaling 1,698 observation hours. The Shannon index was used to determine dietary diversity and nutritional analyses were conducted to assess food quality. All feeding trees were identified and measured, and ranging areas determined via the minimum convex polygon. In the degraded area lemurs were able to modify several aspects of their feeding strategies by decreasing group size and by increasing feeding time, ranging areas, and number of feeding trees. The above strategies were apparently able to counteract a clear reduction in both food quality and size of feeding trees.

Conclusions/Significance

Our findings indicate that collared lemurs in littoral forest fragments modified their behavior to cope with the pressures of fluctuating resource availability. The observed flexibility is likely to be an adaptation to Malagasy rainforests, which are known to undergo periods of fruit scarcity and low productivity. These results should be carefully considered when relocating lemurs or when selecting suitable areas for their conservation.     

Effects of Habitat Quality and Seasonality on Ranging Patterns of Collared Brown Lemur (Eulemur collaris) in Littoral Forest Fragments

Degraded forest habitats typically show low fruit availability and scattered fruit tree distribution. This has been shown to force frugivorous primates either to move further in search of food, resulting in large home ranges, or to use energy saving strategies. Malagasy lemurs are known to face pronounced seasonality and resource unpredictability, which is amplified by the overall reduction in food availability due to the human-driven habitat disturbance on the island. To explore lemur flexibility to habitat disturbance, we examined the ranging behavior of collared brown lemurs (Eulemur collaris) in two differently degraded fragments of littoral forest of southeastern Madagascar. We collected data from February 2011 to January 2012 on two groups living in a degraded area and two groups living in a less disturbed forest. We calculated annual ranges, monthly ranges, and daily distance traveled. We then ran repeated measures ANOVAs using seasonality as dichotomous, intrasubject factor and site/group as intersubject nested factors. In the degraded forest, the lemurs had larger monthly ranges, and their annual ranges were either fragmented or characterized by multiple core areas. They were able to use a habitat mosaic that also included nonforested areas and swamps. In addition, they shortened their daily path length, possibly to preserve energy, and used different areas of their annual home ranges seasonally. Although a number of possible confounding factors may have been responsible for the observed differences between sites, our findings highlight the ranging flexibility of collared brown lemurs in littoral forest fragments.     

Ecological Flexibility as Measured by the Use of Pioneer and Exotic Plants by Two Lemurids: <Emphasis Type="BoldItalic">Eulemur collaris</Emphasis> and <Emphasis Type="BoldItalic">Hapalemur meridionalis</Emphasis>

Primate responses to habitat alteration vary depending on the species’ dietary guild and forest type. Leaves from secondary vegetation can provide nutritious resources to folivorous primates, whereas frugivores, burdened with a scattered spatial and temporal distribution of fruiting resources, require larger home ranges, potentially limiting their ability to cope with altered landscapes. Within coastal southeastern Madagascar, we sought to determine whether two lemur species occupying contrasting ecological niches respond differently to the changing features of their degraded and fragmented habitat. We conducted behavioral observations between 2011 and 2013 on frugivorous collared brown lemurs (Eulemur collaris) and folivorous southern bamboo lemurs (Hapalemur meridionalis). To estimate the ability of lemurs to use pioneer species, we categorized all plants used for feeding and resting as fast growing, mid-growing, or slow growing. We fitted general linear mixed-effects models, one for each plant growth category with monthly proportional use rates as the dependent variable, and included species (E. collaris and H. meridionalis), activity (feeding and resting), and season (dry and wet) as fixed effects. Our results show that E. collaris used both slow- and mid-growing plant species most often, while H. meridionalis were more likely to use fast-growing plants, which indicated an ability to use secondary/disturbed vegetation. Frugivorous E. collaris appear more limited by climax plants, while folivorous H. meridionalis appear to be slightly more adaptable, a finding that is consistent with that for other primate folivores.     

Howler monkey tolerance to habitat shrinking: Lifetime warranty or death sentence?

Habitat loss and fragmentation are major threats to the conservation of nonhuman primates. Given that species differ in their responses to fragmented landscapes, identifying the factors that enable them to cope with altered environments or that cause their extirpation is critical to design conservation management strategies. Howler monkeys (Alouatta spp.) are good models for studying the strategies of tolerant arboreal taxa and how they cope with spatial restriction, because they live in habitats ranging from vast pristine forests to small disturbed fragments and orchards. While some aspects of their ecology and behavior are conserved, others vary in predictable ways in response to habitat shrinking and decreasing resource availability. We argue that the ability of individual howler monkeys to inhabit low-quality environments does not guarantee the long-term persistence of the small populations that live under these conditions. Their local extirpation explains why few forest fragments below a given area threshold are frequently inhabited in landscapes where recolonization and gene flow are compromised by long isolation distances or less permeable matrices. In sum, howlers’ ability to cope with habitat restriction at the individual level in the short-term may mask the inevitable fate of isolated populations, thereby compromising the persistence of the species at a regional scale in the long-term if howlers’ need for protection in large forests is undervalued.     

The Influence of Seasonal Variation on Chimpanzee (Pan troglodytes schweinfurthii) Fallback Food Consumption, Nest Group Size, and Habitat Use in Gishwati, a Montane Rain Forest Fragment in Rwanda

The increased number of primates living in fragmented habitats necessitates greater knowledge of how they cope with large-scale changes to their environment. Chimpanzees (Pan troglodytes) are exceptionally vulnerable to forest fragmentation; however, little is known about chimpanzee feeding ecology in fragments. Although chimpanzees have been shown to prefer fruit when it is available and fall back on more abundant lower quality foods during periods of fruit scarcity, our understanding of how chimpanzees use fallback foods in forest fragments is poor. We examined how chimpanzees cope with periods of fruit scarcity in Gishwati Forest Reserve, a disturbed montane rain forest fragment in Rwanda. We assessed seasonal changes in chimpanzee diet and the use of preferred and fallback foods through fecal and food site analysis. We also examined seasonal variation in nest group size and habitat use through marked nest censuses. We found that chimpanzees experienced a seasonal reduction in preferred fruit availability, which led to a seasonal diet shift to more fibrous foods, including several that functioned as fallback foods. Our results suggest that during periods of fruit scarcity the chimpanzees also reduced nest group size. However, we found that the chimpanzees did not alter their habitat use between high- and low-fruit seasons, which suggests that the small size of the forest limits their ability to change their seasonal habitat use. Consequently, fallback foods appear to be particularly important in small food-impoverished habitats with limited ranging options.     

Seasonal Differences in Activity Patterns of Geoffroyi´s Spider Monkeys (<Emphasis Type="BoldItalic">Ateles geoffroyi</Emphasis>) Living in Continuous and Fragmented Forests in Southern Mexico

Understanding how primates adjust their behavior in response to seasonality in both continuous and fragmented forests is a fundamental challenge for primatologists and conservation biologists. During a 15-mo period, we studied the activity patterns of 6 communities of spider monkeys (Ateles geoffroyi) living in continuous and fragmented forests in the Lacandona rain forest, Mexico. We tested the effects of forest type (continuous and fragmented), season (dry and rainy), and their interaction on spider monkey activity patterns. Overall, monkeys spent more time feeding and less time traveling in fragments than in continuous forest. A more leafy diet and the spatial limitations in fragments likely explain these results. Time spent feeding was greater in the rainy than in the dry season, whereas time spent resting followed the opposite pattern. The increase in percent leaves consumed, and higher temperatures during the dry season, may contribute to the observed increase in resting time because monkeys probably need to reduce energy expenditure. Forest type and seasonality did not interact with activity patterns, indicating that the effect of seasonality on activities was similar across all sites. Our findings confirm that spider monkeys are able to adjust their activity patterns to deal with food scarcity in forest fragments and during the dry season. However, further studies are necessary to assess if these shifts are adequate to ensure their health, fitness, and long-term persistence in fragmented habitats.     

Dietary Flexibility of the Brown Howler Monkey Throughout Its Geographic Distribution

Habitat loss and fragmentation constrain the survival of most forest‐living mammals, particularly strictly arboreal primates. Because fragment size directly affects food availability, primate survival in small fragments may depend on dietary flexibility. Here, we review the literature on the diet of 29 wild groups of Alouatta guariba clamitans inhabiting forest fragments in Brazil and Argentina. We identify general feeding patterns and analyze the influence of fragment size and latitude on diet composition. Brown howlers presented a diet composed of 402 plant species belonging to 227 genera and 80 families. Rarefaction curves suggest that the richness of top food species is similar among groups living in larger (>100 ha), medium (11–100 ha) or small (1–10 ha) fragments. On average, only 12% of the plant species used as food sources by a given group was also consumed by groups from other sites. The shorter the distance between sites, the higher the diet similarity among groups. Despite their diet flexibility, brown howlers spent >80% of the total feeding records on 6–24 species belonging to genera such as Ficus, Zanthoxylum, and Eugenia. Leaves and fruits were the plant items most consumed (65% and 22% of the total feeding records, respectively). Leaf consumption was not affected by fragment size, but it was inversely related to latitude, which may be linked to an increase in the concentration of secondary metabolites in leaves at higher latitudes. We suggest that the ability of brown howlers to exploit a large number of plant food species, including native and exotic trees, shrubs, vines, and lianas, is an important trait that contributes to their survival in highly fragmented habitats along the Atlantic forest. Similar meta‐analyses of data from other howler species are necessary to test whether such dietary flexibility is a genus‐wide pattern. Am. J. Primatol. 75:16‐29, 2013. © 2012 Wiley Periodicals, Inc.     

Fruit-feeding butterflies in edge-dominated habitats: community structure,species persistence and cascade effect

As old-growth forests are converted into edge-affected habitats, a substantial proportion of tropical biodiversity is potentially threatened. Here, we examine a comprehensive set of community-level attributes of fruit-feeding butterfly assemblages inhabiting edge-affected habitats in a fragmented Atlantic forest landscape devoted to sugar cane production. We also explored whether the consequences of habitat loss and fragmentation can interact and cause cascading ecosystem changes, with the pervasive simplification of tree assemblages inhabiting edge-dominated habitats, altering fruit-feeding butterfly persistence. Butterflies were sampled in three forest habitats: small fragments, forest edges and patches of forest interior of a primary forest fragment. Assemblage attributes, including taxonomic composition, correlated to some patch (patch size) and landscape (such as forest cover) metrics as well as habitat structure (tree density and richness). Fruit-feeding butterfly assemblages in the forest interior differed from those in small fragments due to an increased abundance of edge-specialist species. On the other hand, several forest-dependent species were missing in both small fragments and forest edges. Our results suggest that edge-affected habitats dominated by pioneer tree species support taxonomically distinct assemblages, including the presence of disturbance-adapted species, and butterfly community structure is highly sensitive to fragmentation- and plant-related variables, such as forest cover and pioneer tree species. In this way, while the establishment of human-modified landscapes probably results in the local extirpation of forest-dependent species, it allows the persistence of disturbance-adapted species. Thus, forest-dependent species conservation and the plant–animal interaction webs they support could be improved by retaining a significant amount of core forest habitat.     

Population, Diet and Conservation of Malayan Flying Lemurs in Altered and Fragmented Habitats in Singapore

The Malayan flying lemur (Cynocephalus variegatus) is a nocturnal mammalian arboreal folivore that inhabits the forests of Southeast Asia. Surveys were conducted from August to November 2003 to estimate the population density of Malayan flying lemurs for the first time in the Singapore Zoological Gardens. The study area consisting of Singapore Zoo and Night Safari was located in the Central Catchment Nature Reserve, where most of Singapore’s remaining natural forest is found. The Zoo consisted of 28 ha of landscaped habitat and the adjacent Night Safari consisted of 40 ha of secondary rainforest. The density estimates of flying lemurs in the Zoo and Night Safari were 15 and 24 individuals respectively. Seven plant species that were the preferred food items and an additional 10 plants that were common in the sites but not eaten by the flying lemurs were analysed to compare the mineral and phytochemical contents. Flying lemurs consumed leaves containing significantly less potassium and nitrogen but higher tannin (p < 0.05). The study shows that flying lemurs are able to survive in altered and fragmented landscapes. Conservation and management strategies are essential to protect the shrinking habitats in Singapore.     

High Energy or Protein Concentrations in Food as Possible Offsets for Cyanide Consumption by Specialized Bamboo Lemurs in Madagascar

Plants producing toxic plant secondary metabolites (PSMs) deter folivores from feeding on them. Animals that can cope with noxious PSMs have a niche with a competitive advantage over other species. However, the ability to cope with toxic PSMs incurs the costs of detoxification. To assess possible compensations for the ingestion of toxic PSMs, we compare the chemical quality of plants consumed by bamboo lemurs (genera Hapalemur and Prolemur; strepsirrhine primates of Madagascar) in areas with and without bamboo. Some bamboo lemurs consume bamboo containing concentrations of cyanogenic substances 10–50 times above the average lethal dosage for mammals, and we postulate that animals consuming cyanogenic substances need supplementary protein or readily available energy for detoxification. We compared the chemical composition of food consumed by three species of bamboo lemurs that feed mainly (>80% of their time) on bamboo in the evergreen rainforest of Ranomafana (Madagascar) with published data of the diets of bamboo lemurs at two sites without highly cyanogenic plants (reed beds of Lac Alaotra and the evergreen littoral forest of Mandena) and with food of sympatric folivorous lemur species that do not feed on bamboo. Lemurs feeding on bamboo consumed up to twice as much protein as bamboo lemurs in areas without bamboo and sympatric lemur species that feed on leaves of trees. Concentrations of nonstructural carbohydrates (a source of energy) showed the opposite trend. This result supports the hypothesis that feeding on cyanogenic plants is linked to high protein intake, either as a source of protein or for sulfur-containing amino acids that can be used for detoxification. Owing to the high protein concentrations in bamboo, however, we cannot distinguish between the hypothesis that lemurs that eat bamboo target additional food items with higher protein from the hypothesis that lemurs feeding on bamboo unavoidably obtain higher concentrations of protein than animals feeding on leaves of trees, without an added nutritional benefit.     

Frugivory,Post‐feeding Flights of Frugivorous Birds and the Movement of Seeds in a Brazilian Fragmented Landscape

Habitat fragmentation can break down the movement processes of frugivorous animals, thus influencing the relationship between plants and their seed dispersers by altering the number and identity of seed dispersers, and their relative contribution to seed dispersal. We studied the assemblages of frugivorous birds, their composition, species richness, and visitation rates to fruiting plants growing in the different landscape elements (forest fragments, live fences, and trees isolated in pastures) embedded in a Brazilian fragmented, agricultural landscape. By following the post‐feeding movements of frugivorous birds, we inferred the direction of seed movement from and to each of these landscape elements. Fruiting trees growing at different landscape elements were visited by frugivorous birds at similar rates. Isolated trees attracted a greater and distinct bird assemblage than trees in forest fragments or live fences. Judging by the post‐feeding flights of birds, the seeds of isolated trees were the most likely to reach all the landscape elements considered, but the contribution of isolated trees to the seeds falling in forested habitats or pastures depended on their degree of isolation. A few bird species were able to move widely, visiting fruiting plants in all landscape elements, and promoting long‐distance dispersal for plants. These few birds are of special interest because they are mobile links that connect habitats in fragmented landscapes with their seed dispersal services. Abstract in Spanish is available at http://www.blackwell‐synergy.com/loi/btp .     

Feeding ecology of bonobos living in forest‐savannah mosaics: Diet seasonal variation and importance of fallback foods

Primates along with many other animal taxa are forced to cope with large shifts in basic ecological conditions because of rapid anthropogenically induced changes of their habitats. One of the coping strategies for primates is to adjust their diet to these changes, and several studies have demonstrated the importance of fallback resources for this. Bonobos, like chimpanzees, might be particularly vulnerable to habitat fragmentation because of their high dependence on fruit availability. Little is known, however, about bonobo feeding ecology in fragmented habitats and their use of fallback resources. In this study, we investigate diet seasonal variation and the exploitation of preferred and fallback foods in a bonobo population living in forest‐savannah mosaics. Results show that bonobos have adapted to this fragmented habitat by feeding on only a few fruit species, including an important number of non‐tree species (liana, herb and savannah shrub), in comparison to populations living in dense forests. These non‐tree plants have been defined as fallback and non‐preferred foods, which are most probably consumed to maintain high frugivory. Interestingly, we identified that preferred foods are all typical of mature forests while fallback resources are mainly found in forest edges or disturbed areas. This finding indicates that bonobos prefer to use mature forests when feeding, as they do for nesting, but extend their range use to forest areas in close proximity to humans when the availability of preferred fruits is low. Finally, we show that bonobo diet relies heavily on two abundant fallback fruits: Musanga cecropioides and Marantochloa leucantha. Other studies have demonstrated that the selection of abundant fallback resources enables primates to subsist at high densities and to maintain cohesive groups, as observed at this study site. Our findings suggest that bonobos living in forest‐savannah mosaics can be considered as staple fallback food consumers. Am. J. Primatol. 77:948–962, 2015. © 2015 Wiley Periodicals, Inc.

     

Severe wear and tooth loss in wild ring-tailed lemurs (Lemur catta): a function of feeding ecology, dental structure, and individual life history

The ring-tailed lemurs at Beza Mahafaly Special Reserve, Madagascar, exhibit a high frequency of severe wear and antemortem tooth loss. As part of a long-term study, we collected dental data on 83 living adult ring-tailed lemurs during 2003 and 2004. Among these individuals, 192 teeth were scored as absent. The most frequently missing tooth position is M1 (24%). As M1 is the first tooth to erupt, its high frequency of absence (primarily a result of wear) is not remarkable. However, the remaining pattern of tooth loss does not correlate with the sequence of eruption. We suggest that this pattern is a function of 1) feeding ecology, as hard, tough tamarind fruit is a key fallback food of ring-tailed lemurs living in gallery forests; 2) food processing, as tamarind fruit is primarily processed in the P3-M1 region of the mouth; and 3) tooth structure, as ring-tailed lemurs possess thin dental enamel. The incongruity between thin enamel and use of a hard, tough fallback food suggests that ring-tailed lemurs living in riverine gallery forests may rely on resources not used in the past. When comparing dental health in the same individuals (n=50) between 2003 and 2004, we found that individual tooth loss can show a rapid increase over the span of one year, increasing by as much as 20%. Despite this rapid loss, individuals are able to survive, sometimes benefiting from unintentional assistance from conspecifics, from which partially processed tamarind fruit is obtained. Although less frequent in this population, these longitudinal data also illustrate that ring-tailed lemurs lose teeth due to damage and disease, similar to other nonhuman primates. The relationship between tooth loss, feeding ecology, dental structure, and individual life history in this population has implications for interpreting behavior based on tooth loss in the hominid fossil record.     

Sociality, ecology, and relative brain size in lemurs

The social brain hypothesis proposes that haplorhine primates have evolved relatively large brains for their body size primarily as an adaptation for living in complex social groups. Studies that support this hypothesis have shown a strong relationship between relative brain size and group size in these taxa. Recent reports suggest that this pattern is unique to haplorhine primates; many nonprimate taxa do not show a relationship between group size and relative brain size. Rather, pairbonded social monogamy appears to be a better predictor of a large relative brain size in many nonprimate taxa. It has been suggested that haplorhine primates may have expanded the pairbonded relationship beyond simple dyads towards the evolution of complex social groups. We examined the relationship between group size, pairbonding, and relative brain size in a sample of 19 lemurs; strepsirrhine primates that last share a common ancestor with monkeys and apes approximately 75 Ma. First, we evaluated the social brain hypothesis, which predicts that species with larger social groups will have relatively larger brains. Secondly, we tested the pairbonded hypothesis, which predicts that species with a pairbonded social organization will have relatively larger brains than non-pairbonded species. We found no relationship between group size or pairbonding and relative brain size in lemurs. We conducted two further analyses to test for possible relationships between two nonsocial variables, activity pattern and diet, and relative brain size. Both diet and activity pattern are significantly associated with relative brain size in our sample. Specifically, frugivorous species have relatively larger brains than folivorous species, and cathemeral species have relatively larger brains than diurnal, but not nocturnal species. These findings highlight meaningful differences between Malagasy strepsirrhines and haplorhines, and between Malagasy strepsirrhines and nonprimate taxa, regarding the social and ecological factors associated with increases in relative brain size. The results suggest that factors such as foraging complexity and flexibility of activity patterns may have driven selection for increases in brain size in lemurs.     

A DNA Metabarcoding Study of a Primate Dietary Diversity and Plasticity across Its Entire Fragmented Range

In tropical regions, most primary ecosystems have been replaced by mosaic landscapes in which species must cope with a large shift in the distribution of their habitat and associated food resources. Primates are particularly vulnerable to habitat modifications. Most species persist in small fragments surrounded by complex human-mediated matrices whose structure and connectivity may strongly influence their dispersal and feeding behavior. Behavioral plasticity appears to be a crucial parameter governing the ability of organisms to exploit the resources offered by new matrix habitats and thus to persist in fragmented habitats. In this study, we were interested in the dietary plasticity of the golden-crowned sifaka (Propithecus tattersalli), an endangered species of lemur, found only in the Daraina region in north-eastern Madagascar. We used a DNA-based approach combining the barcoding concept and Illumina next-generation sequencing to (i) describe the species diet across its entire range and (ii) evaluate the influence of landscape heterogeneity on diet diversity and composition. Faeces from 96 individuals were sampled across the entire species range and their contents were analyzed using the trnL metabarcoding approach. In parallel, we built a large DNA reference database based on a checklist of the plant species of the Daraina region. Our results suggest that golden-crowned sifakas exhibit remarkable dietary diversity with at least 130 plant species belonging to 80 genera and 49 different families. We highlighted an influence of both habitat type and openness on diet composition suggesting a high flexibility of foraging strategies. Moreover, we observed the presence of numerous cultivated and naturalized plants in the faeces of groups living in forest edge areas. Overall, our findings support our initial expectation that P. tattersalli is able to cope with the current level of alteration of the landscape and confirm our previous results on the distribution and the dispersal ability of this species.     

Feeding Ecology and Dietary Flexibility of <Emphasis Type="Italic">Colobus angolensis palliatus</Emphasis> in Relation to Habitat Disturbance

Behavioral and dietary flexibility permits primates to survive in variable environments. It is clear that some species cope with habitat disturbance and fragmentation better than others. I examined the dietary flexibility of Colobus angolensis palliatus by studying three groups inhabiting structurally distinct ranges in Kenya’s Diani Forest. I predicted that the two groups inhabiting more disturbed areas would have reduced food availability and would respond by increasing dietary diversity and consuming greater proportions of lianas and exotic plant species compared to the group inhabiting the more intact area. Forest composition and overall plant part availability differed among home ranges; however, group diets did not differ in their proportions of different plant parts, nor did groups select plant parts in proportion to their availability. Diets differed dramatically with regard to species-specific plant parts, i.e., mean monthly dietary overlap among groups = 10.4%. Contrary to my predictions, all three groups exhibited considerable dietary diversity, i.e., 63–76 plant species, and relied heavily on lianas, i.e., 20.8–38.4% of the diet, and exotic plant species, i.e., 30.1–40.3% of the diet. The presence of exotic plant species in all three ranges suggests that even the most intact areas of the Diani Forest are perturbed and should be classified along a spectrum of habitat disturbance rather than intact vs. degraded. Nonetheless, this study emphasizes that diets can vary considerably among groups living in the same forest, and this degree of dietary flexibility likely enables C. a. palliatus to survive within increasingly disturbed habitats.     

Spatio‐temporal Genetic Structure of a Tropical Bee Species Suggests High Dispersal Over a Fragmented Landscape

Habitat destruction threatens biodiversity by reducing the amount of available resources and connectivity among geographic areas. For organisms living in fragmented habitats, population persistence may depend on dispersal, which maintains gene flow among fragments and can prevent inbreeding within them. It is centrally important to understand patterns of dispersal for bees living in fragmented areas given the importance of pollination systems and recently documented declines in bee populations. We used population and landscape genetic techniques to characterize patterns of dispersal over a large fragmented area in southern Costa Rica for the orchid bee species Euglossa championi. First, we estimated levels of genetic differentiation among forest fragments as ?_PT, an analog to the traditional summary statistic F_ST, as well as two statistics that may more adequately represent levels of differentiation, G’_ST and D_est. Second, we used a Bayesian approach to determine the number and composition of genetic groups in our sample. Third we investigated how genetic differentiation changes with distance. Fourth, we determined the extent to which deforested areas restrict dispersal. Finally, we estimated the extent to which there were temporal differences in allele frequencies within the same forest fragments. Within years we found low levels of differentiation even over 80 km, and no effect of land use type on level of genetic differentiation. However, we found significant genetic differentiation between years. Taken together our results suggest that there are high levels of gene flow over this geographic area, and that individuals show low site fidelity over time.     

Female Spider Monkeys (<Emphasis Type="Italic">Ateles geoffroyi</Emphasis>) Cope with Anthropogenic Disturbance Through Fission–Fusion Dynamics

Most primates live in habitats with some level of anthropogenic disturbance, and such disturbances have a larger impact on frugivorous primates that are more sensitive to ecological disruptions than folivores. Fecal glucocorticoid metabolites provide insight into how the external environment affects internal physiological state, and thus provide information on how anthropogenic pressures become embodied. Here, I examine how subgroup size and glucocorticoids vary with high and low fruit abundance, and how fruit abundance, subgroup size, and activity budget affect fecal glucocorticoid metabolites in female spider monkeys (Ateles geoffroyi) living in an anthropogenically disturbed habitat. I measured these variables via behavioral, ecological, and fecal sampling for 15 months in 17 female spider monkeys at El Zota Biological Field Station. Subgroup size was significantly larger during periods of high fruit abundance, but glucocorticoids did not differ between periods of low and high fruit abundance. Monthly fruit abundance predicted subgroup sizes significantly, but did not predict fecal glucocorticoid concentrations. Increased resting time and reproductive state predicted fecal glucocorticoid concentrations significantly, but travel and foraging time had no significant effect on glucocorticoid concentrations. Individual resting time over the study period correlated negatively with glucocorticoid concentrations. These results suggest that spider monkeys cope with variation in fruit abundance by adjusting subgroup size, and that these adjustments may mitigate environmental stress in this mildly seasonal environment. The large, relatively productive forest size at this site, and the availability of anthropogenic food sources, enable this population of spider monkeys to cope with human-induced habitat disturbance.     

Abundance responses of frugivorous bats (Stenodermatinae) to coffee cultivation and selective logging practices in mountainous central Veracruz,Mexico

Shifting and permanent cultivation, selective logging, cattle production and coffee plantations are among the most important factors in montane cloud forest conversion and disturbance. Although shaded-coffee plantations can contribute to the preservation of local species richness, abundance of organisms could be determined by habitat resource availability in agricultural landscapes. We compared abundance of Sturnira and Artibeus bats (Phyllostomidae, Stenodermatinae), in shade coffee plantations and disturbed cloud forest fragments, which represent habitats with different chiropterochorous plant density. We also investigated the relationship between bat species abundance and food plant richness, abundance and diversity. We captured 956 bats, 76% in cloud forest fragments and 24% in shaded coffee plantations. Abundance of Sturnira spp. (small bats) was greater in cloud forest than in coffee plantations, but Artibeus spp. (large bats) abundance was similar in both habitats. Chiropterochorous plant abundance was positively related with bat abundance for Sturnira spp., while chiropterochorous plant richness and diversity were negatively related for Artibeus spp. This suggests that frugivorous bats with different morphological and ecological characteristics respond differentially to anthropogenic activities. For landscape management purposes, the maintenance and augmentation of diverse food resources, for frugivorous bats with different foraging requirements in coffee plantations, will benefit the resilience of bats to modification of their natural habitat.