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.

Related papers:

title: Closing the seed dispersal loop
abstract: Seed dispersal links the end of the reproductive cycle of adult plants with the establishment of their offspring, and is widely accepted to have a profound effect on vegetation structure. Confirming and quantifying this effect, however, has proven to be a challenge. Recent research on animal-mediated seed dispersal has brought us closer to this goal: ecologists have been explicitly examining the processes that mediate seed deposition and seedling recruitment. Exciting new techniques, such as the analysis of stable isotope ratios and molecular genetic markers, are making it possible to relate dispersed seeds and seedlings back to parent plants. Meanwhile, evidence from plant demography research is revealing that seed dispersal might have an important role in determining patterns of tree diversity and distribution. The continued synergy between seed dispersal research and the study of plant demography should help researchers link seed dispersal and adult vegetation structure, closing the seed dispersal loop.

title: Spatial patterns of seed dispersal, their determinants and consequences for recruitment.
abstract: Growing interest in spatial ecology is promoting new approaches to the study of seed dispersal, one of the key processes determining the spatial structure of plant populations. Seed-dispersion patterns vary among plant species, populations and individuals, at different distances from parents, different microsites and different times. Recent field studies have made progress in elucidating the mechanisms behind these patterns and the implications of these patterns for recruitment success. Together with the development and refinement of mathematical models, this promises a deeper, more mechanistic understanding of dispersal processes and their consequences.

title: Primate Seed Dispersal Linking Behavioral Ecology with Forest Community Structure
abstract: The role of animals in seed dispersal is well recognized. As many as 75% of tropical tree species produce fruits presumably adapted for animal dispersal (Frankie et al. 1974, Howe and Smallwood 1982), and animals are estimated to move more than 95% of tropical seeds (Terborgh et al. 2002). Some vertebrate groups may be particularly important seed dispersers. Primates, for example, comprise between 25% and 40% of the frugivore biomass in tropical forests (Chapman 1995), eat large quantities of fruit, and defecate or spit large numbers of viable seeds (Lambert 1999). Primate frugivory and seed dispersal have been quantified by studies in South America (Garber 1986, Julliot 1996, Stevenson 2000, Dew 2001, Vulinec 2002), Central America (Estrada and CoatesEstrada 1984, 1986; Chapman 1989a), Africa (Gautier-Hion 1984; Gautier-Hion et al. 1985; Wrangham et al. 1994; Chapman and Chapman 1996; Kaplin and Moermond 1998; Lambert 1999; Voysey et al. 1999a,b), and Asia (Corlett and Lucas 1990, Davies 1991, Leighton 1993, Lucas and Corlett 1998, McConkey 2000). This research has illustrated that primates disperse significant numbers of seeds. For example, on Borneo, a single gibbon group (Hylobates mulleri × agilis) dispersed a minimum of 16,400 seeds · km−2 · year−1 of 160 species; and since the survival rate of seeds to 1 year was 8%, a group of gibbons effectively dispersed 13 seedlings · ha−1 · year−1 (McConkey 2000). Although it is clear that primates play an important role in dispersing many seeds throughout tropical forests, the ecological and evolutionary significance of these activities is not well understood. The objective of this chapter is to review the role that primate seed dispersal plays in shaping the ecology of tropical forests and to shed light on inconsistencies in the literature in order to point to new directions for research. We first evaluate how variation among primate species in traits such as digestive anatomy, body size, social structure, movement patterns, and diet influences the spatial distribution of dispersed seeds (the seed shadow, App. 31.1) and thereby produces a diversity of seed shadows. We then consider how traits of fruiting species, including patch characteristics and fruit and seed traits, influence the seed shadow that different primates generate. Few studies have quantified primate-generated seed shadows. However, to understand their effect on plants, it is important to consider primate seed shadows in light of plant population and community ecological theory. To this end, we next review current theories and concepts and evaluate the role that primate seed dispersal plays in plant ecological processes. This analysis of variation in seed shadows points to two critical areas in which our understanding of primates’ roles is currently lacking: the significance of primates dispersing seeds in clumped versus scattered patterns and the consequences of primate seed dispersal to different distances away from the parent tree. We conclude by discussing potential conservation implications related to changes in the nature of primate–plant interactions.

title: Herbivores and the Number of Tree Species in Tropical Forests
abstract: A high number of tree species, low density of adults of each species, and long distances between conspecific adults are characteristic of many low-land tropical forest habitats. I propose that these three traits, in large part, are the result of the action of predators on seeds and seedlings. A model is presented that allows detailed examination of the effect of different predators, dispersal agents, seed-crop sizes, etc. on these three traits. In short, any event that increases the efficiency of the predators at eating seeds and seedlings of a given tree species may lead to a reduction in population density of the adults of that species and/or to increased distance between new adults and their parents. Either event will lead to more space in the habitat for other species of trees, and therefore higher total number of tree species, provided seed sources are available over evolutionary time. As one moves from the wet lowland tropics to the dry tropics or temperate zones, the seed and seedling predators in a habitat are hypothesized to be progressively less efficient at keeping one or a few tree species from monopolizing the habitat through competitive superiority. This lowered efficiency of the predators is brought about by the increased severity and unpredictability of the physical environment, which in turn leads to regular or erratic escape of large seed or seedling cohorts from the predators.

title: Recruitment of Black Howler Fruit Trees in Fragmented Forests of Northern Belize
abstract: We examined recruitment of trees whose seeds are dispersed by black howler monkeys (Alouatta pigra) in forest fragments within the Community Baboon Sanctuary in north-central Belize. In the fragments, most other large frugivores are absent and howlers dominate the large frugivore community. Consequently, we expected to observe an increased representation of howler fruit trees among the sapling community. To test this prediction preliminarily we observed howler feeding behavior for one year and conducted adult tree and sapling transects in 6 locations where howlers were present. We sampled a seventh site where howlers were absent for vegetation only. We found that in 4 of 6 sites there were proportionately fewer howler fruit saplings when compared to adult tree samples. However, when recruitment of howler fruit trees in the 6 sites was compared to a site where howlers were absent, 11 of 12 species had relatively higher recruitment. The lack of recruitment among howler fruit trees in general likely reflects differences in responses of individual species, as well as disruptions from human activities to natural processes within the forests. The observed lower recruitment patterns of howler trees suggest that over time, the abundance of the trees will likely decline and thus affect the foraging behavior and possibly survival of howlers in the fragmented forests.

title: The impact of seed dispersal by black and gold howler monkeys on forest regeneration
abstract: In Neotropical humid forest, the majority of tree species have seeds dispersed by vertebrates. Seed deposition by vertebrates is often spatially aggregated and a low per capita survival for seeds and seedlings is predicted. However, mortality factors could be saturated by high densities. I evaluated whether recruitment of saplings of species dispersed by black and gold howlers (Alouatta caraya) in latrines is higher than at control sites: (1) below parent trees, (2) in trees not used by monkeys to sleep, (3) randomly chosen sites within the forest, and determined whether howlers may influence current floristic composition of the Paraná River flooded forest. I recorded saplings several years old in the territories of five monkey groups. In total, I found four times more saplings in latrines than in the other areas, and results suggest that latrines are recruitment foci for most species, though larger samples would be required to assess this for every species. Frequency distribution of the diameter of tallest saplings of more abundant species reflected recruitment over time. I found saplings of more species growing in latrines than outside of them. Saplings higher than 1 m of two species of laurels (Ocotea diospyrifolia and Nectandra megapotamica) and one species of Myrtaceae (Eugenia punicifolia) had higher densities in latrines than below parent trees. Results suggest that mortality factors were saturated in latrines and that sapling may grow at a higher rate in latrines. In relation to the influence on floristic composition E. burkartiana, an uncommon species in the forest, could increase in abundance as consequence of seed dispersal by howlers.

title: Ecology of Seed Dispersal
abstract: Identification of the selective forces on plant dispersal engenders theoretical argument, empirical study, and speculation. We separate evidence, testable hypotheses, and conjecture surrounding two major questions in dispersal ecology. The first asks what ecological, and ultimately evolutionary, advantages exist in seed dispersal. Astonishingly little is known about the advantages to a parent plant that are actually conferred by investment in dispersal structures. Does dispersal enable seeds and ultimately seedlings to escape mortality near the parent? Is continual recolonization of unstable habitats the primary advantage? Must seeds find rare microhabitats suitable for reestablishment? Such issues are addressed through joint consideration of dispersal and establishment-those stages both mediated by parental provisioning and subject to the highest mortality in the life of a plant. The second broad question asks what general and explicit environmental forces influence the timing and mode of dispersal. Do climates or seasons favor one dispersal mode over another? Do differences in number, size, morphology, or nutritional quality of fruits influence frugivore choice, and consequently differential dispersal of species or individuals within species? Studies of dispersal process and mode should be intimately connected. A general objective of this paper is to explore the degree to which they are integrated and, in so doing, to catalyze their union. We emphasize topics most in need of critical attention: the evolutionary ecology of dispersal process and mode. Excellent recent reviews consider such related topics as dispersal mechanism (131, 184), seed dormancy (1, 30), phytogeography (11, 115, 146), masting and predator satiation (105, 156), and succession (68, 69, 189).

title: Quantity, Quality and the Effectiveness of Seed Dispersal by Animals
abstract: Disperser effectiveness is the contribution a disperser makes to the future reproduction of a plant. Although it is a key notion in studies of seed dispersal by animals, we know little about what determines the effectiveness of a disperser. The role of the present paper is to review the available information and construct a hierarchical framework for viewing the components of disperser effectiveness.

title: Seed dispersal by woolly monkeys (Lagothrix lagothricha) at Tinigua National Park, Colombia: Dispersal distance, germination rates, and dispersal quantity
abstract: The purpose of this study was to describe seed dispersal patterns of woolly monkeys (Lagothrix lagothricha) in terms of dispersal quantity and two factors related to dispersal quality: germination rates of dispersed seeds and the distance of dispersal to parental trees. The possible influence of retention time, travel distance, seed size, activity patterns, and fruit abundance on dispersal distance was also analyzed. Observations on activity, diet, daily movements, and seed dispersal were made on focal individuals of a group of woolly monkeys at a tropical rain forest in Tinigua National Park (Colombia). Sixty hours of focal samples per month were completed during 1 year. A total of 753 depositions were collected during the study. Each dropping contained seeds from an average of 2.68 different species (range 0 to 9). Collected depositions contained an underestimated total of 50,168 seeds (>1 mm). Given a population density of 30 individuals/km2, the woolly monkeys in the study area disperse more than 25,000 seeds/km2/day. These seeds belong to 112 different plant species. Germination rates of dispersed seeds are usually similar or higher than those of non‐swallowed seeds. It was possible to determine dispersal distance in 264 cases when the focal animal was continuously followed from ingestion at the parental tree to deposition. Only 1% of these depositions landed in close proximity (<15 m) of the parental tree. It was very common that the droppings were deposited between 100 and 500 m from the parent tree, and up to 1.5 km. Higher retention times and longer travel distances were not correlated with increased dispersal distance. Two main reasons for this result were the prolonged and variable passage rates (avg=11.2 hr ± 6.5 SD.) and the circuitous routes of monkeys in this forest.  2000.

title: Seed dispersal by spider monkeys and its importance in the maintenance of neotropical rain-forest diversity
abstract: Seed dispersal by frugivores is thought to play an important role in the maintenance of tropical forest diversity. Spider monkeys (Ateles spp.) are amongst the most frugivorous primates known, and they incorporate a diverse array of fruit species in their diets. In a 1-y study in lowland Ecuador, 670 h of focal observations and data on 916 faecal depositions were collected, and these data are used to describe the seed dispersal patterns of one group of wild spider monkeys (Ateles belzebuth) in terms of both the quantity of seeds dispersed and the primary seed shadows generated. Spider monkeys fed on the fruits of at least 152 plant species and swallowed seeds from more than 98% of these. Collected faecal samples contained seeds from at least 133 different plant species, with an average of 1.9 species (range: 0–7) per defecation. Individual spider monkeys dispersed a minimum of ∼195 000 seeds >1 mm in diameter per year, ∼35 000 of which were >3 mm in diameter. Mean retention time for seeds was 4.5 h. Seed dispersal distances averaged 443 m, but some seeds were moved >1250 m away from parental sources. These results suggest that declines in populations of spider monkeys might have a direct effect on forest dynamics, especially if other disperser species cannot compensate for their lost ecological services.

title: Diet of spider monkeys (Ateles geoffroyi) in Mesoamerica: current knowledge and future directions
abstract: 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.  2009.

title: Effectiveness of Spider Monkeys (Ateles geoffroyi vellerosus) as Seed Dispersers in Continuous and Fragmented Rain Forests in Southern Mexico
abstract: Seed dispersal is considered a key process determining spatial structure and dynamics of plant populations, and has crucial implications for forest regeneration. We evaluated the effectiveness of spider monkeys (Ateles geoffroyi) as seed dispersers in continuous and fragmented habitats to test if this interaction is altered in forest fragments. We documented fruit and seed handling, defecation patterns, diversity and composition of seeds in feces, and seed germination of defecated and control seeds in the Lacandona rainforest, Mexico. For most species contributing to 80% of total fruit feeding time, monkeys swallowed and spat seeds, but swallowing was the most frequent seed handling category in continuous and fragmented forests. However, the proportion of feeding records of swallowed seeds was higher in continuous forest (0.59) than in fragments (0.46), whereas the opposite was true for proportion of dropped seeds (0.16 vs. 0.31). This pattern was reflected in the number of fecal samples containing seeds, which was greater in continuous (95.5%) than in fragmented forests (82.5%). Seeds in fecal samples included a total of 71 species from 23 plant families. The numbers of defecated seed species were similar between forest conditions, and in both cases most seeds (>86%) were undamaged. Defecated seeds showed greater germination percentages than control seeds in all of the five species evaluated. Although we identified some differences in seed handling and the percentage of feces with seeds between continuous forest and fragments, our results indicate that, in general terms, spider monkeys are effective seed dispersers in both forest conditions.

title: Aggregated Seed Dispersal by Spider Monkeys Limits Recruitment to Clumped Patterns in Virola calophylla
abstract: The initial spatial pattern of seed deposition influences plant population and community structure, particularly when that pattern persists through recruitment. In a vertebratedispersed rain forest tree, Virola calophylla, we found that spatially aggregated seed deposition strongly influenced the spatial structure of later stages. Seed dispersion was clumped, and seed densities were highest underneath V. calophylla females and the sleeping sites of spider monkeys (Ateles paniscus), the key dispersal agent. Although these site types had the lowest per capita seed-to-seedling survival, they had the highest seedling/sapling densities. Conversely, seed and seedling/sapling densities were lowest, and seed survival was highest, at sites of diurnal seed dispersal by spider monkeys. Negative density-dependent and positive distance-dependent seed survival thinned seed clumps. Nonetheless, the clumped dispersion at sleeping and parental sites persisted to the seedling/sapling stage because differences in seed deposition were large enough to offset differences in seed survival among these site types.

title: Incorporating animal behavior into seed dispersal models: implications for seed shadows.
abstract: Seed dispersal fundamentally influences plant population and community dynamics but is difficult to quantify directly. Consequently, models are frequently used to describe the seed shadow (the seed deposition pattern of a plant population). For vertebrate-dispersed plants, animal behavior is known to influence seed shadows but is poorly integrated in seed dispersal models. Here, we illustrate a modeling approach that incorporates animal behavior and develop a stochastic, spatially explicit simulation model that predicts the seed shadow for a primate-dispersed tree species (Virola calophylla, Myristicaceae) at the forest stand scale. The model was parameterized from field-collected data on fruit production and seed dispersal, behaviors and movement patterns of the key disperser, the spider monkey (Ateles paniscus), densities of dispersed and non-dispersed seeds, and direct estimates of seed dispersal distances. Our model demonstrated that the spatial scale of dispersal for this V. calophylla population was large, as spider monkeys routinely dispersed seeds >>100 m, a commonly used threshold for long-distance dispersal. The simulated seed shadow was heterogeneous, with high spatial variance in seed density resulting largely from behaviors and movement patterns of spider monkeys that aggregated seeds (dispersal at their sleeping sites) and that scattered seeds (dispersal during diurnal foraging and resting). The single-distribution dispersal kernels frequently used to model dispersal substantially underestimated this variance and poorly fit the simulated seed-dispersal curve, primarily because of its multimodality, and a mixture distribution always fit the simulated dispersal curve better. Both seed shadow heterogeneity and dispersal curve multimodality arose directly from these different dispersal processes generated by spider monkeys. Compared to models that did not account for disperser behavior, our modeling approach improved prediction of the seed shadow of this V. calophylla population. An important function of seed dispersal models is to use the seed shadows they predict to estimate components of plant demography, particularly seedling population dynamics and distributions. Our model demonstrated that improved seed shadow prediction for animal-dispersed plants can be accomplished by incorporating spatially explicit information on disperser behavior and movements, using scales large enough to capture routine long-distance dispersal, and using dispersal kernels, such as mixture distributions, that account for spatially aggregated dispersal.

title: Spider monkey sleeping sites: Use and availability
abstract: The behavior of spider monkeys (Ateles geoffroyi) at sleeping sites and the characteristics of these sites were studied in Santa Rosa National Park, Costa Rica. The spider monkeys tended to congregate just prior to dusk at a number of sleeping sites which were repeatedly used (81.6%), but occasionally they slept in trees which were only used once (18.4%). All of the regularly used sleeping trees were not used concurrently, but rather, there was a rotation between sites. In general, males were not encountered at regularly used sleeping sites as often as other age/sex classes, and when they were in all male subgroups, they did not sleep in repeatedly used sites. The trees used as regular sleeping sites tended to be large, but such trees were common in the group's home range. The size of the subgroups attending repeatedly used sleeping trees was large when food was abundant and small when food was scarce. It is suggested that this relationship reflects that the costs of travelling to the sleeping site would be more easily recovered when food was abundant than when food was scarce.

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

title: Partitioning diversity into independent alpha and beta components.
abstract: Existing general definitions of beta diversity often produce a beta with a hidden dependence on alpha. Such a beta cannot be used to compare regions that differ in alpha diversity. To avoid misinterpretation, existing definitions of alpha and beta must be replaced by a definition that partitions diversity into independent alpha and beta components. Such a unique definition is derived here. When these new alpha and beta components are transformed into their numbers equivalents (effective numbers of elements), Whittaker's multiplicative law (alpha x beta = gamma) is necessarily true for all indices. The new beta gives the effective number of distinct communities. The most popular similarity and overlap measures of ecology (Jaccard, Sorensen, Horn, and Morisita-Horn indices) are monotonic transformations of the new beta diversity. Shannon measures follow deductively from this formalism and do not need to be borrowed from information theory; they are shown to be the only standard diversity measures which can be decomposed into meaningful independent alpha and beta components when community weights are unequal.

title: Estimators of Fruit Abundance of Tropical Trees
abstract: Many types of b~ological s t ~ ~ i l ~ e s require rht. estirnatio~i of food ahu~iil,ince In tropical fi~resrs, and a variety of mt.thods have been used to estimatt. this parameter. I-lere we cornpare the ;iccuracy .inii prec~sion of three lnerhods for estlmatlng the fruit ahucldaclce (hiomass and numhcr) of tropical rree specles. rree diameter, crown vo lu~ne , anil v~sua l cstlrnatlocl. D ~ ~ i m e r e r low levels of ~nrerobserver a t breast height (DBF-I)was tht. most consistently accurate methoit and e x h ~ b ~ t e i l variahility. Generally. crou7n volume a7Lis neither precise nor ,lccurare. The v~sua l estlrnatlon mt.rhod was aiiiirare for trees with very large fruit, bu t t . xh~b~ te i l h ~ g h ~nterobservrr va r~~ ib~ l i t ! Key zc,o&: DBH: croufn zjoiiime:.fvtiil nblindrrnt-r: i i ; t . t b~$~/ ' i~~) : twe i/ia)12ater:trop~t.al triei; LJgnndtr THEQUANTIFICATION OF FRUIT AVAILABILITY has been a primary objective in many studies which focus on the ecology of tropical fruiting trees and/or their frugivore consumers ( Leighton 1982, Terborgh 1981, Chapman 1990, Leighton, in press). Such estimates are often related to the behavior of the frugivores (Clutton-Brock 1977, Raemakers 1980, Chapman & Lefebvre 199O), or used to examine interannual variability in the production of fruit (Milton et al. 1982). Although a variety of methods have been used to estimate fruit abundance, differences in the accuracy and precision of the different methods have rarely been quantified. Consequently, it is difficult to state the extent to which different methodologies contribute to variation among studies as opposed to other factors of biological significance, such as differences between species, habitats, or seasons. In addition, there are few guidelines available to indicate which procedures are most appropriate in different situations (see Peters et a / . 1988). Tlie objective of this study was to examine the applicability of three methods for estimating fruit number and biomass for different species of rain forest trees in the Kibale Forest Reserve, Uganda. For all tree species, we docun~ented the relationships between three different estimates of fruit abundance, and the degree of variation benveen observers. In addition, for two tree species we determined the accuraq of the different methods of estimating fruit

title: Forest Fragmentation Modifies Habitat Quality for Alouatta palliata
abstract: Fragmentation reduces habitat area, increases the number of habitat patches, decreases their size, and increases patch isolation. For arboreal mammals such as howlers (Alouatta palliata), canopy modifications from fragmentation processes could also negatively affect habitat quality. We analyzed changes in the composition and plant structure of 15 fragments (1–76 ha) and compared them with vegetation from a continuous tropical rain forest reserve (700 ha) in Los Tuxtlas, Mexico. At each site, we sampled 1000 m2 of all trees, shrubs, and lianas with a diameter at breast height (DBH) ≥10 cm. We obtained estimates of species richness, density, and basal area for different ecological groups, DBH ranges, and top food resources for howlers. We used a stepwise multiple regression analysis to determine relationships between fragment characteristics (size, shape index, and isolation) and plant variables. Compared to continuous forest, fragments have altered composition and plant structure, with large trees absent from the canopy. The basal area of top food resources is higher in continuous forest. Fragment size is the best explanation for the differences in composition and plant structure. The largest fragments had greater basal area of top food resources and more large primary trees in the canopy. Overall, our results suggest that fragmentation altered the habitat quality for howlers.

title: Differences in diet and activity pattern between two groups of Alouatta palliata associated with the availability of big trees and fruit of top food taxa
abstract: The threat that forest fragmentation and habitat loss presents for several Alouatta taxa requires us to determine the key elements that may promote the persistence of howler monkeys in forest fragments and to evaluate how changes in the availability of these elements may affect their future conservation prospects. In this study we analyzed the relationship between the availability of both big trees of top food taxa (BTTFT) (diameter at breast height>60) and fruit of top food taxa (FrTFT) in the home ranges of two groups of Alouatta palliata mexicana occupying different forest fragments in Los Tuxtlas, Mexico, and their diet and activity pattern. Both study groups preferred big trees for feeding and the group with lower availability of BTTFT in their home range fed from more, smaller food sources. Furthermore, both study groups also increased the number of food sources when their consumption of fruit decreased, and the group with lower availability of FrTFT in their home range fed from more food sources. The increase in the number of food sources used under such conditions, in turn, set up a process of higher foraging effort and lower rest. In summary, our results support other studies that suggest that the availability of big trees and fruit may be two important elements influencing the persistence of howler monkeys in forest fragments.  2009.

title: Patch depletion behavior differs between sympatric folivorous primates
abstract: Food competition in group-living animals is commonly accepted as a critical determinant of foraging strategies and social organization. Here we examine food patch depletion behavior in a leaf-eating (folivorous) primate, the guereza (Colobus guereza). Snaith and Chapman (2005) studied the sympatric folivorous red colobus (Procolobus rufomitratus), which shares many food resources with the guereza. They determined that red colobus deplete the patches (feeding trees) they use, while we found contrary evidence for guerezas using the same methods. We found that the time guerezas spent feeding in a patch was affected by neither tree size, an indicator of food abundance, nor the size of the feeding group, an indicator of feeding competition. For their principal food item (young leaves), intake rate remained constant and coincided with a decrease in the distance moved to find food within a patch, implying that guerezas do not deplete patches. This points to a fundamental difference in the use of food by guerezas and red colobus, which may be linked to the large difference in their group sizes and/or to a disparity in their digestive physiologies. However, further analyses revealed that the number of feeders within a patch did not affect patch depletion patterns in either species, leaving the potential for a physiological basis as the most plausible explanation. Our research highlights the need for a more critical examination of folivorous primate feeding ecology and social behavior, as all folivorous primates are typically lumped into a single category in socioecological models, which may account for conflicting evidence in the literature.

title: Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size.
abstract: We propose an integrated sampling, rarefaction, and extrapolation methodology to compare species richness of a set of communities based on samples of equal completeness (as measured by sample coverage) instead of equal size. Traditional rarefaction or extrapolation to equal-sized samples can misrepresent the relationships between the richnesses of the communities being compared because a sample of a given size may be sufficient to fully characterize the lower diversity community, but insufficient to characterize the richer community. Thus, the traditional method systematically biases the degree of differences between community richnesses. We derived a new analytic method for seamless coverage-based rarefaction and extrapolation. We show that this method yields less biased comparisons of richness between communities, and manages this with less total sampling effort. When this approach is integrated with an adaptive coverage-based stopping rule during sampling, samples may be compared directly without rarefaction, so no extra data is taken and none is thrown away. Even if this stopping rule is not used during data collection, coverage-based rarefaction throws away less data than traditional size-based rarefaction, and more efficiently finds the correct ranking of communities according to their true richnesses. Several hypothetical and real examples demonstrate these advantages.

title: Statistical Computing: An Introduction to Data Analysis Using S-PLUS
abstract: First, a clari cation: This book is not about traditional statistical computing topics, such as random number generation, approximation of probability distribution functions, least squares computations, and so forth. The book’s subtitle reveals what it is about: “An Introduction to Data Analysis using S-PLUS.” Crawley’s intention, as stated in the Preface, is to provide “both an introduction to and a reference manual for statistics and computing.” (The commercial package S-PLUS appears in the subtitle, but the Preface notes the availability of the freeware R system, which can be obtained at www.r-project.org. The author states that all the examples in the book will also work in R. Based on my experience with the two packages, some code tweaking may be required when using R, but you cannot beat the price.) My  rst reaction when I began to peruse this book was “wow”: More than 750 pages, covering a vast range of topics in statistical modeling. Roughly speaking, the  rst third of the book covers material suitable for a  rst course in statistics, the middle third covers basic applied linear models (regression and analysis of variance), and the  nal third covers a number of advanced statistical modeling methods, including generalized linear models, tree-based models, nonparametric smoothing, survival analysis, time series, mixed-effects models, and spatial statistics. There is a certain logic to the sequencing of topics in the text, but Crawley has made some nonstandard (one might even say quirky) decisions. For instance, power calculations are discussed three chapters before the classical hypothesis testing procedures are introduced. The early chapter on basic graphical techniques includes displays of tree-based models but excludes probability plotting. The formal introduction of probability distributions is quite thorough, but does not appear until Chapter 26, two-thirds of the way through the book. A number of examples involve the use of procedures that are not formally introduced until much later in the book. (Including more cross-referencing when this happens would make the book more effective as a self-study guide.) On balance, I can recommend this book for the intended audience, as long as they understand what they are in for. It contains a wealth of sage advice about the process of designing studies, analyzing data, and  tting statistical models and could become a treasured reference. However, the style is fairly terse and fast-paced, and neophytes may  nd it somewhat overwhelming. In the Preface, Crawley says “Learning S-PLUS will not be easy, but you won’t regret making the effort.” The same can be said for reading this book.

title: Modern statistics for the life sciences
abstract: Why use this book 1. An introduction to the analysis of variance 2.  Models, parameters and GLMs 4. Using more than one explanatory variable 5. Designing experiments - keeping it simple 6. Combining continuous and categorical variables 7. Interactions - getting more complex 8. Checking the models A: Independence 9. Checking the models B: The other three assumptions 10. Model selection I: Principles of model choice and designed experiments 11. Model selection II: Data sets with several explanatory variables 12. Random effects 13. Categorical data 14. What lies beyond? Answers to exercises Revision section: The basics  The meaning of p-values and confidence intervals Appendix II: Analytical results about variances of sample means Appendix III: Probability distributions Bibliography

title: Plant β‐diversity in fragmented rain forests: testing floristic homogenization and differentiation hypotheses
abstract: Land-use change is the main driver of global biodiversity loss, but its relative impact on species turnover (β-diversity) across multiple spatial scales remains unclear. Plant communities in fragmented rain forests can undergo declines (floristic homogenization) or increases (floristic differentiation) in β-diversity. 
We tested these alternative hypotheses analysing a large vegetation data base from a hierarchically nested sampling design (450 plots in 45 forest patches in 3 landscapes with different deforestation levels) at Los Tuxtlas rain forest, Mexico. Differences in β-diversity across spatial scales (i.e. among plots, among patches, and among landscapes) were analysed using multiplicative diversity decompositions of Hill numbers. 
Plant β-diversity among plots within forest patches decreased in landscapes with higher deforestation levels, leading to floristic homogenization within patches. This homogenization process can be explained by the loss of rare and shade-tolerant plant species, and the recruitment and dominance of disturbance-adapted species, and can limit the accumulation of species (γ-diversity) in landscapes with higher deforestation. 
Nevertheless, the landscape with the highest deforestation level showed the highest floristic differentiation among patches. This landscape showed the greatest isolation distances between patches; a landscape spatial pattern that can limit the interchange of seeds (and species) between patches. Because the study patches are undergoing secondary succession following disturbances (e.g. logging, edge effects), different disturbance regimes and increased distance among patches could lead to higher β-diversity. 
Synthesis. These findings indicate that patterns of floristic homogenization and differentiation depend on the landscape configuration and on the spatial scale of analysis. At the landscape scale, our results suggest that, in accordance with non-equilibrium dynamics and the landscape-divergence hypothesis, patches located in landscapes with different forest cover and different connectivity can experience contrasting successional pathways due to increasing levels of compositional differentiation between patches. These novel findings add further uncertainties to the maintenance of biodiversity in severely deforested tropical landscapes and have key ecological implications for biodiversity conservation planning.

title: The Unified Neutral Theory of Biodiversity and Biogeography
abstract: study of the issue indicates that it is not a serious problem for neutral theory, for reasons we discuss below. First, a bit of background. Hubbell (2001) derived the analytical expression for the stochastic mean and variance of the abundance of a single arbitrary species in a neutral community undergoing immigration from a metacommunity source area. However, his approach did not lend itself to an analytical solution for the distribution of relative species abundance (RSA) in a multispecies community for community sizes larger than a handful of individuals. As a result, all of Hubbell's RSA distributions for local communities were based on simulations. This problem was solved by Volkov et al. (2003), who derived an analytical expression for the RSA distribution in local communities of arbitrary size. However, as Chisholm and Burgman noted, there is sometimes a difference between some of the simulation-based results of Hubbell and the analytical results of Volkov et al. (2003). Chisholm and Burgman computed Volkov's equation and resimulated Hubbell's results for the four cases

title: Multiple central place foraging by spider monkeys: travel consequences of using many sleeping sites
abstract: SummaryCentral place foraging models assume that animals return to a single central place such as a nest, burrow, or sleeping site. Many animals, however choose between one of a limited number of central places. Such animals can be considered Multiple Central Place Foragers (MCPF), and such a strategy could reduce overall travel costs, if the forager selected a sleeping site close to current feeding areas. We examined the selection of sleeping sites (central places) by a community of spider monkeys (Ateles geoffroyi) in Santa Rosa National Park, Costa Rica in relation to the location of their feeding areas. Spider monkeys repeatedly used 11 sleeping trees, and they tended to choose the sleeping site closest to their current feeding area. A comparison of the observed travel distances with distances predicted for a MCPF strategy, a single central place strategy, and a strategy of randomly selecting sleeping sites demonstrated (1) that the MCPF strategy entailed the lowest travel costs, and (2) that the observed travel distance was best predicted by the MCPF strategy. Deviations between the observed distance travelled and the values predicted by the MCPF model increased after a feeding site had been used for several days. This appears to result from animals sampling their home range to locate new feeding sites.

title: Forests without primates: Primate/plant codependency
abstract: Detailed studies of primates and fruiting trees have illustrated that these groups of organisms are involved in a very complex set of interactions, with primates relying on fruiting trees as important food resources and fruiting trees relying on frugivores for seed dispersal. Human activities that influence either primate seed dispersal or fruit production have the potential of having unanticipated effects on the other interactants. Here we evaluate what is known and what we still need to learn to evaluate the long‐term consequences of disrupting the interactions between primates and tropical forest trees. We do this by first assessing the potential importance of primates at dispersing the seeds of tropical forest trees. Second, we consider possible consequences of hunting primates on recruitment in tropical tree communities. Third, we address the converse by considering the impacts of decreasing resource availability for primates through either logging or through the extraction of nontimber forest products. Finally, we provide a case study from Kibale National Park, Uganda, that contrasts seedling recruitment in 20 forest fragments in which primate seed dispersers have been dramatically reduced with seedling recruitment in areas that have an intact frugivore community. In comparison to the intact forest, the fragments had lower seedling density and fewer species of seedlings. Furthermore, a greater proportion of the seedlings were from small‐seeded species that might not require primates for their dispersal, since they probably can be dispersed by small birds. All of these considerations suggest that disrupting the complex interactions between primates and fruiting trees can potentially have negative and possibly cascading effects on ecosystem processes.  1998.

title: Forest fragmentation drives Atlantic forest of northeastern Brazil to biotic homogenization
abstract: To examine whether the tree flora of the Atlantic forest of northeastern Brazil has experienced detectable taxonomic homogenization via the proliferation of native pioneer species in response to habitat loss and fragmentation. Location Biotic homogenization (BH) was examined across the Atlantic forest of northeast Brazil, i.e. a 56,000 km 2 piece of tropical forest and a distinct centre of species endemism in South America.

title: The 'few winners and many losers' paradigm revisited: Emerging prospects for tropical forest biodiversity
abstract: Despite its relevance to contemporary biodiversity conservation, the ecological mechanisms controlling nonrandom species replacements and biotic homogenization of native biotas remain poorly understood. Here, we advocate for the widespread occurrence of a pattern of winner–loser species turnover exhibited in tropical forest floras: the replacement of old-growth tree species by a small set of pioneer or successional tree species across edge-dominated habitats in hyper-fragmented landscapes. A growing body of evidence on biotic reassembly in human-degraded forest sites suggests that winner–loser replacements are often advanced by native rather than exotic plant species, leading to taxonomic homogenization at multiple spatial scales (i.e. from local to regional assemblages). This process does not rely on biological invasions and associated shifts in geographic ranges of nonindigenous species. Moreover, this form of biodiversity erosion is not limited to restricted-range and endemic species but can include any species of many ecological groups that are apparently intolerant to highly modified habitat conditions, such as desiccated/illuminated forest edges and fire-degraded forest fragments persisting in open-habitat matrices. This unidirectional pattern of species turnover is expected to set in motion devastating cascading effects onto higher trophic levels that will eventually disrupt the structure of the entire forest ecosystem. Our framework not only reaffirms the winner–loser replacement paradigm, but also contends that the proliferation of disturbance-adapted native organisms has a pivotal role in sealing the fate of tropical biodiversity in particular contexts.