Linking pollen limitation and seed dispersal effectiveness.

Seed production and dispersal are crucial ecological processes impacting plant demography, species distributions and community assembly. Plant-animal interactions commonly mediate both seed production and seed dispersal, but current research often examines pollination and seed dispersal separately, which hinders our understanding of how pollination services affect downstream dispersal services. To fill this gap, we propose a conceptual framework exploring how pollen limitation can impact the effectiveness of seed dispersal for endozoochorous and myrmecochorous plant species. We summarize the quantitative and qualitative effects of pollen limitation on plant reproduction and use Optimal Foraging Theory to predict its impact on the foraging behaviour of seed dispersers. In doing so, we offer a new framework that poses numerous hypotheses and empirical tests to investigate links between pollen limitation and seed dispersal effectiveness and, consequently, post-dispersal ecological processes occurring at different levels of biological organization. Finally, considering the importance of pollination and seed dispersal outcomes to plant eco-evolutionary dynamics, we discussed the implications of our framework for future studies exploring the demographic and evolutionary impacts of pollen limitation for animal-dispersed plants.

Assembly, Persistence, and Disassembly Dynamics of Quaternary Caribbean Frugivore Communities.

AbstractHow communities assemble and restructure is of critical importance to ecological theory, evolutionary theory, and conservation, but long-term perspectives on the patterns and processes of community assembly are rarely integrated into traditional community ecology, and the utility of communities as an ecological concept has been repeatedly questioned in part because of a lack of temporal perspective. Through a synthesis of paleontological and neontological data, I reconstruct Caribbean frugivore communities over the Quaternary (2.58 million years ago to present). Numerous Caribbean frugivore lineages arise during periods coincident with the global origins of plant-frugivore mutualisms. The persistence of many of these lineages into the Quaternary is indicative of long-term community stability, but an analysis of Quaternary extinctions reveals a nonrandom loss of large-bodied mammalian and reptilian frugivores. Anthropogenic impacts, including human niche construction, underlie the recent reorganization of frugivore communities, setting the stage for continued declines and evolutionary responses in plants that have lost mutualistic partners. These impacts also support ongoing and future introductions of invader complexes: introduced plants and frugivores that further exacerbate native biodiversity loss by interacting more strongly with one another than with native plants or frugivores. This work illustrates the importance of paleontological data and perspectives in conceptualizing ecological communities, which are dynamic and important entities.

Land-use homogenization reduces the occurrence and diversity of frugivorous birds in a tropical biodiversity hotspot.

Understanding how human-modified landscapes maintain biodiversity and provide ecosystem services is crucial for establishing conservation practices. Given that responses to land-use are species-specific, it is crucial to understand how land-use changes may shape patterns of species diversity and persistence in human-modified landscapes. Here, we used a comprehensive data set on bird distribution from the Brazilian Atlantic Forest to understand how species richness and individual occurrences of frugivorous bird species responded to land-use spatial predictors and, subsequently, assess how ecological traits and phylogeny modulated these responses. Using Bayesian hierarchical modeling, we reveal that the richness of frugivorous birds was positively associated with the amount of native forest and negatively with both agriculture and pasture amount at the landscape scale. Conversely, the effect of these predictors on species occurrence and ecological traits was highly variable and presented a weak phylogenetic signal. Furthermore, land-use homogenization (i.e., the conversion of forest to pasture or agriculture) led to pervasive consequences for forest-dependent bird species, whereas several generalist species thrived in deforested areas, replacing those sensitive to habitat disturbances.

Examining the structure of plant-lemur interactions in the face of imperfect knowledge.

Biotic interactions, such as plant-animal seed dispersal mutualisms, are essential for ecosystem function. Such interactions are threatened by the possible extinction of the animal partners. Using a data set that includes plant-lemur interactions across Madagascar, we studied the current state of knowledge of these interactions and their structure to determine which plant species are most at risk of losing dispersal services due to the loss of lemurs. We found substantial gaps in understanding of plant-lemur interactions; data were substantially skewed toward a few lemur species and locations. There was also a large gap in knowledge on the interactions of plants and small-bodied or nocturnal lemurs and lemurs outside a few highly studied locations. Of the recorded interactions, a significant portion occurred between lemurs and endemic plants, rather than native or introduced plants. We also found that lemur species tended to primarily consume closely related plant species. Such interaction patterns may indicate the threats to Malagasy endemic plants and highlight how lemur population loss or reductions could affect plant phylogenetic diversity. When examining the impacts of lemur extinction, losing critically endangered species left 164 plant species with no known lemur frugivore partners. Despite phylogenetic patterns in lemur diet, plants for which the only known lemur frugivore is critically endangered were not closely related. These results emphasize the need for further studies to complete our knowledge on these essential interactions and to inform conservation priorities.

Análisis de la estructura de las interacciones entre lémures y plantas de cara al conocimiento incompleto Resumen Las interacciones bióticas, como el mutualismo entre plantas y animales para la dispersión de semillas, son esenciales para que el ecosistema funcione. Dichas interacciones se encuentran amenazadas por la posible extinción del animal que participa en ellas. Usamos un conjunto de datos que incluye las interacciones entre lémures y plantas en Madagascar para estudiar el estado actual del conocimiento de estas interacciones y su estructura. Con lo anterior determinamos cuáles especies botánicas tienen mayor riesgo de perder la dispersión de semillas debido a la extinción de los lémures. Encontramos vacíos sustanciales en el entendimiento de las interacciones entre lémures y plantas; los datos estaban sesgados para unas cuantas especies de lémures y localidades. Hubo un gran vacío de conocimiento para las interacciones entre las plantas y los lémures pequeños o nocturnos y aquellos fuera de unas cuantas localidades estudiadas. De las interacciones registradas, una porción importante ocurrió entre los lémures y plantas endémicas, en lugar de plantas nativas o introducidas. También encontramos que las especies de lémures tienden a consumir especies botánicas con filogenia cercana. Dichos patrones de interacción podrían indicar las amenazas para las plantas endémicas de Madagascar y enfatizar cómo la pérdida o reducción de las poblaciones de lémures podrían afectar la diversidad filogenética de las plantas. Cuando examinamos el impacto de la extinción de los lémures, la pérdida de especies en peligro crítico dejó a 164 especies de plantas sin un lémur frugívoro mutualista. A pesar de los patrones filogenéticos en la dieta de los lémures, las plantas cuyo único lémur frugívoro se encuentra en peligro crítico no tienen una filogenia cercana. Estos resultados resaltan la necesidad de más estudios para completar nuestro conocimiento sobre estas interacciones esenciales y para guiar las prioridades de conservación.

The effects of diet-shifting from invertebrates towards fruit on the condition of autumn-migrant Catharus thrushes.

Migration is an energetically challenging and risky life history stage for many animals, but could be supported by dietary choices en route, which may create opportunities to improve body and physiological condition. However, proposed benefits of diet shifts, such as between seasonally available invertebrates and fruits, have received limited investigation in free-living animals. We quantified diet composition and magnitude of autumn diet shifts over two time periods in two closely-related species of migratory songbirds on stopover in the northeastern U.S. (Swainson's thrush [Catharus ustulatus], long-distance migrant, N = 83; hermit thrush [C. guttatus], short-distance migrant, N = 79) and used piecewise structural equation models to evaluate the relationships among (1) migration timing, (2) dietary behavior, and (3) morphometric and physiological condition indices. Tissue isotope composition indicated that both species shifted towards greater fruit consumption. Larger shifts in recent weeks corresponded to higher body condition in Swainson's, but not hermit thrushes, and condition was more heavily influenced by capture date in Swainson's thrushes. Presence of "high-antioxidant" fruits in fecal samples was unrelated to condition in Swainson's thrushes and negatively related to multiple condition indices in hermit thrushes, possibly indicating the value of fruits during migration is related more to their energy and/or macronutrient content than antioxidant content. Our results suggest that increased frugivory during autumn migration can support condition, but those benefits might depend on migration strategy: a longer-distance, more capital-dependent migration strategy could require stricter regulation of body condition aided by increased fruit consumption.

Reciprocity and interaction effectiveness in generalised mutualisms among free-living species.

Mutualistic interactions among free-living species generally involve low-frequency interactions and highly asymmetric dependence among partners, yet our understanding of factors behind their emergence is still limited. Using individual-based interactions of a super-generalist fleshy-fruited plant with its frugivore assemblage, we estimated the Resource Provisioning Effectiveness (RPE) and Seed Dispersal Effectiveness (SDE) to assess the balance in the exchange of resources. Plants were highly dependent on a few frugivore species, while frugivores interacted with most individual plants, resulting in strong asymmetries of mutual dependence. Interaction effectiveness was mainly driven by interaction frequency. Despite highly asymmetric dependences, the strong reliance on quantity of fruit consumed determined high reciprocity in rewards between partners (i.e. higher energy provided by the plant, more seedlings recruited), which was not obscured by minor variations in the quality of animal or plant service. We anticipate reciprocity will emerge in low-intimacy mutualisms where the mutualistic outcome largely relies upon interaction frequency.

Seed dispersal syndrome predicts ethanol concentration of fruits in a tropical dry forest.

Studying fruit traits and their interactions with seed dispersers can improve how we interpret patterns of biodiversity, ecosystem function and evolution. Mounting evidence suggests that fruit ethanol is common and variable, and may exert selective pressures on seed dispersers. To test this, we comprehensively assess fruit ethanol content in a wild ecosystem and explore sources of variation. We hypothesize that both phylogeny and seed dispersal syndrome explain variation in ethanol levels, and we predict that fruits with mammalian dispersal traits will contain higher levels of ethanol than those with bird dispersal traits. We measured ripe fruit ethanol content in species with mammal- (n = 16), bird- (n = 14) or mixed-dispersal (n = 7) syndromes in a Costa Rican tropical dry forest. Seventy-eight per cent of fruit species yielded measurable ethanol concentrations. We detected a phylogenetic signal in maximum ethanol levels (Pagel's λ = 0.82). Controlling for phylogeny, we observed greater ethanol concentrations in mammal-dispersed fruits, indicating that dispersal syndrome helps explain variation in ethanol content, and that mammals may be more exposed to ethanol in their diets than birds. Our findings further our understanding of wild fruit ethanol and its potential role as a selective pressure on frugivore sensory systems and metabolism.

The turnover of plant-frugivore interactions along plant range expansion: consequences for natural colonization processes.

Plant-animal mutualisms such as seed dispersal are key interactions for sustaining plant range shifts. It remains elusive whether the organization of interactions with seed dispersers is reconfigured along the expansion landscape template and, if so, whether its effects accelerate or slow colonization. Here we analyse plant-frugivore interactions in a scenario of rapid population expansion of a Mediterranean juniper. We combined network analyses with field surveys, sampling interactions between individual plants and frugivores by DNA-barcoding and phototrapping over two seasons. We assess the role of intrinsic and extrinsic intraspecific variability in shaping interactions and we estimate the individual plant contributions to the seed rain. The whole interaction network was highly structured, with a distinct set of modules including individual plants and frugivore species arranged concordantly along the expansion gradient. The modular configuration was partially shaped by individual neighbourhood context (density and fecundity) and phenotypic traits (cone size). Interaction reconfiguration resulted in a higher and more uneven propagule contribution, with most effective dispersers having a prominent role at the colonization front stand, where a distinct subset of early arriving plants dominated the seed rain. Our study offers new insights into the key role of mutualistic interactions in colonization scenarios by promoting fast plant expansion processes.

Africa as an evolutionary arena for large fruits.

Strong paleoclimatic change and few Late Quaternary megafauna extinctions make mainland Africa unique among continents. Here, we hypothesize that, compared with elsewhere, these conditions created the ecological opportunity for the macroevolution and geographic distribution of large fruits. We assembled global phylogenetic, distribution and fruit size data for palms (Arecaceae), a pantropical, vertebrate-dispersed family with > 2600 species, and integrated these with data on extinction-driven body size reduction in mammalian frugivore assemblages since the Late Quaternary. We applied evolutionary trait, linear and null models to identify the selective pressures that have shaped fruit sizes. We show that African palm lineages have evolved towards larger fruit sizes and exhibited faster trait evolutionary rates than lineages elsewhere. Furthermore, the global distribution of the largest palm fruits across species assemblages was explained by occurrence in Africa, especially under low canopies, and extant megafauna, but not by mammalian downsizing. These patterns strongly deviated from expectations under a null model of stochastic (Brownian motion) evolution. Our results suggest that Africa provided a distinct evolutionary arena for palm fruit size evolution. We argue that megafaunal abundance and the expansion of savanna habitat since the Miocene provided selective advantages for the persistence of African plants with large fruits.

When lizards shift to a more plant-based lifestyle: The macroevolution of mutualistic lizard-plant-interactions (Squamata: Sauria/Lacertilia).

Pollination and seed dispersal of plants by animals are key mutualistic processes for the conservation of plant diversity and ecosystem functioning. Although different animals frequently act as pollinators or seed dispersers, some species can provide both functions, so-called 'double mutualists', suggesting that the evolution of pollination and seed dispersal may be linked. Here, we assess the macroevolution of mutualistic behaviours in lizards (Lacertilia) by applying comparative methods to a phylogeny comprising 2,838 species. We found that both flower visitation (potential pollination; recorded in 64 species [2.3% of total] across 9 families) and seed dispersal (recorded in 382 species [13,5% of total] across 26 families) have evolved repeatedly in Lacertilia. Furthermore, we found that seed dispersal activity pre-dated flower visitation and that the evolution of seed dispersal activity and flower visitation was correlated, illustrating a potential evolutionary mechanism behind the emergence of double mutualisms. Finally, we provide evidence that lineages with flower visitation or seed dispersal activity have higher diversification rates than lineages lacking these behaviours. Our study illustrates the repeated innovation of (double) mutualisms across Lacertilia and we argue that island settings may provide the ecological conditions under which (double) mutualisms persist over macroevolutionary timescales.

On the adequacy of fruit removal as a proxy for fitness in studies of bird-mediated phenotypic selection.

PREMISE: In fleshy-fruited plants, fruit removal is widely used as a proxy for plant reproductive success. Nevertheless, this proxy may not accurately reflect the number of seeds dispersed, an assumed better proxy for total fitness (fruit removal × mean number of seeds dispersed per fruit). METHODS: We examined under what circumstances fruit removal can be reliable as a proxy for total fitness when assessing bird-mediated selection on fruit traits. In three populations of the Blue Passionflower (Passiflora caerulea), we used the number of fruits pecked per plant as a surrogate for fruit removal to estimate phenotypic selection on fruit and seed traits, and simulations of the effect of the fruit-seed number trade-off on the number of fruits removed. RESULTS: Fruit removal was a good indicator of fitness, accounting for 55 to 68% of the variability in total fitness, measured as total number of seeds removed. Moreover, multivariate selection analyses on fruit crop size, mean fruit diameter and mean seed number using fruit removal as a fitness proxy yielded similar selection regimes to those using total fitness. Simulations showed that producing more fruits, a lower number of seeds per fruit, and a higher variability in seed number can result in a negative relationship between fruit removal and total fitness. CONCLUSIONS: Our results suggest that fruit removal can be reliably used as a proxy for total fitness when (1) there is a weak fruit number-seed number trade-off, (2) fruit crop size and fruit removal correlate positively, and (3) seed number variability does not largely exceed fruit number variability.

The important role of animal social status in vertebrate seed dispersal.

Seed dispersal directly affects plant establishment, gene flow and fitness. Understanding patterns in seed dispersal is, therefore, fundamental to understanding plant ecology and evolution, as well as addressing challenges of extinction and global change. Our ability to understand dispersal is limited because seeds may be dispersed by multiple agents, and the effectiveness of these agents can be highly variable both among and within species. We provide a novel framework that links seed dispersal to animal social status, a key component of behaviour. Because social status affects individual resource access and movement, it provides a critical link to two factors that determine seed dispersal: the quantity of seeds dispersed and the spatial patterns of dispersal. Social status may have unappreciated effects on post-dispersal seed survival and recruitment when social status affects individual habitat use. Hence, environmental changes, such as selective harvesting and urbanisation, that affect animal social structure may have unappreciated consequences for seed dispersal. This framework highlights these exciting new hypotheses linking environmental change, social structure and seed dispersal. By outlining experimental approaches to test these hypotheses, we hope to facilitate studies across a wide diversity of plant-animal networks, which may uncover emerging hotspots or significant declines in seed dispersal.

Anatomy and dietary specialization influence sensory behaviour among sympatric primates.

Senses form the interface between animals and environments, and provide a window into the ecology of past and present species. However, research on sensory behaviours by wild frugivores is sparse. Here, we examine fruit assessment by three sympatric primates (Alouatta palliata, Ateles geoffroyi and Cebus imitator) to test the hypothesis that dietary and sensory specialization shape foraging behaviours. Ateles and Cebus groups are comprised of dichromats and trichromats, while all Alouatta are trichomats. We use anatomical proxies to examine smell, taste and manual touch, and opsin genotyping to assess colour vision. We find that the frugivorous spider monkeys (Ateles geoffroyi) sniff fruits most often, omnivorous capuchins (Cebus imitator), the species with the highest manual dexterity, use manual touch most often, and that main olfactory bulb volume is a better predictor of sniffing behaviour than nasal turbinate surface area. We also identify an interaction between colour vision phenotype and use of other senses. Controlling for species, dichromats sniff and bite fruits more often than trichromats, and trichromats use manual touch to evaluate cryptic fruits more often than dichromats. Our findings reveal new relationships among dietary specialization, anatomical variation and foraging behaviour, and promote understanding of sensory system evolution.

Loss of endangered frugivores from seed dispersal networks generates severe mutualism disruption.

Many tropical seed-dispersing frugivores are facing extinction, but the consequences of the loss of endangered frugivores for seed dispersal is not well understood. We investigated the role of frugivore endangerment status via robustness-to-coextinction simulations (in this context, more accurately described as robustness-to-partner-loss simulations) using data from the Brazilian Atlantic Forest biodiversity hotspot. By simulating the extinction of endangered frugivores, we found a rapid and disproportionate loss of tree species with dispersal partners in the network, and this surprisingly surpassed any other frugivore extinction scenario, including the loss of the most generalist frugivores first. A key driver of this pattern is that many specialist plants rely on at-risk frugivores as seed-dispersal partners. Moreover, interaction compensation in the absence of endangered frugivores may be unlikely because frugivores with growing populations forage on fewer plant species than frugivores with declining populations. Therefore, protecting endangered frugivores could be critical for maintaining tropical forest seed dispersal, and their loss may have higher-than-expected functional consequences for tropical forests, their regeneration processes, and the maintenance of tropical plant diversity.

Fleshy fruit traits and seed dispersers: which traits define syndromes?

BACKGROUND AND AIMS: Fruit traits and their inter-relationships can affect foraging choices by frugivores, and hence the probability of mutualistic interactions. Certain combinations of fruit traits that determine the interaction with specific seed dispersers are known as dispersal syndromes. The dispersal syndrome hypothesis (DSH) states that seed dispersers influence the combination of fruit traits found in fruits. Therefore, fruit traits can predict the type of dispersers with which plant species interact. Here, we analysed whether relationships of fruit traits can be explained by the DSH. To do so, we estimated the inter-relationships between morphological, chemical and display groups of fruit traits. In addition, we tested the importance of each trait group defining seed dispersal syndromes. METHODS: Using phylogenetically corrected fruit trait data and fruit-seed disperser networks, we tested the relationships among morphological, chemical and display fruit traits with Pearson's correlations and phenotypic integration indices. Then, we used perMANOVA to test if the fruit traits involved in the analysis supported the functional types of seed dispersers. KEY RESULTS: Morphological traits showed strong intragroup relationships, in contrast to chemical and display traits whose intragroup trait relationships were weak or null. Accordingly, only the morphological group of traits supported three broad seed disperser functional types (birds, terrestrial mammals and bats), consistent with the DSH. CONCLUSIONS: Altogether, our results give some support to the DSH. Here, the three groups of traits interacted in different ways with seed disperser biology. Broad functional types of seed dispersers would adjust fruit consumption to anatomical limitations imposed by fruit morphology. Once this anatomical filter is sovercome, seed dispersers use almost all the range of variation in chemical and display fruit traits. This suggests that the effect of seed dispersers on fruit traits is modulated by hierarchical decisions. First, morphological constraints define which interactions can actually occur; subsequently, display and composition determine fruit preferences.

Food availability alters community co-occurrence patterns at fine spatiotemporal scales in a tropical masting system.

Patterns of co-occurrence among species can help reveal the structure and assembly of ecological communities. However, studies have been limited by measuring co-occurrence in either space or time but not both simultaneously. This is especially problematic in systems such as masting forests where resources are highly variable, meaning that spatial use and co-occurrence patterns can change on fine spatiotemporal scales. We develop an analytical framework for assessing species co-occurrence at fine spatial and temporal scales simultaneously and apply these models to a camera trapping dataset from Borneo. We sought to determine how substantial variation in food availability across space and time affects co-occurrence among terrestrial vertebrates. We detect many significant, mostly positive, co-occurrence patterns among species, but almost entirely in unlogged forest and during dipterocarp mast years. The most strongly co-occurring pair of species, bearded pig (Sus barbatus) and sambar (Rusa unicolor), only positively co-occur in areas and years when fruit is locally abundant. Species occurrences in logged forest and non-mast years are mostly random with respect to other species. This suggests that frugivore-granivore species positively co-occur when resources are plentiful (i.e., large trees are present and fruiting), likely because they use the same resources; these patterns disappear when food availability is lower. Our approach demonstrates the utility of measuring co-occurrence in space and time together and highlights the importance of resource abundance for driving the co-occurrence structure of communities. Furthermore, our method could be broadly applied to other systems to assess fine-scale spatiotemporal patterns across a range of taxa.

Clinal versus disruptive latitudinal variation in fruit traits of a South American mistletoe.

Fruit traits have historically been interpreted as plant adaptations to their seed dispersers. On the other hand, different environmental factors, which vary spatially and temporally, can shape fruit-trait variation. The mistletoe Tristerix corymbosus has a latitudinal distribution along the South American Pacific rim that encompasses two different biomes, the matorral of central Chile and the temperate forest that extends south of the matorral. This mistletoe shows contrasting fruiting phenology (spring vs summer), fruit color (yellow vs green), and seed dispersers (birds vs marsupial) in these two biomes. We characterized geographic variation of morphological and nutritional fruit traits of T. corymbosus to evaluate which macroecological factor, biome or latitude, better explains spatial variation in these variables. For each of 22 populations, we obtained environmental data (temperature, precipitation, and canopy cover), measured fruit and seed morphology traits (size, shape, and weight), and pulp moisture and nutritional content (fiber, protein, fat, carbohydrates, ash, and caloric content). Patterns of variation for each variable were described by fitting and comparing five different simple models varying in slope, intercept or both. Fruit morphology showed a clear biome-related disruptive pattern, seed morphological traits were unrelated to either biome or latitude, whereas nutritional variables showed diverse patterns. Different environmental factors seem to affect fruit development and phenology, determining the observed fruit characteristics, with seed dispersers playing a minor role in shaping these patterns. More generally, the contrasting plant-seed disperser associations we addressed can be interpreted as the outcome of an ecological-fitting rather than of a coevolutionary process.

Dental caries in wild primates: Interproximal cavities on anterior teeth.

Dental caries has been reported in a variety of primates, although it is still considered rare in wild populations. In this study, 11 catarrhine primate taxa (n = 339 individuals; 7946 teeth) were studied for the presence of caries. A differential diagnosis of lesions in interproximal regions of anterior teeth was undertaken, since they had been previously described as both carious and non-carious in origin. Each permanent tooth was examined macroscopically, with severity and position of lesions recorded. Two specimens were examined further, using micro-CT scans to assess demineralization. Differential diagnosis confirmed the cariogenic nature of interproximal cavities on anterior teeth (ICATs). Overall results show 3.3% of all teeth (i.e., anterior and posterior teeth combined) were carious (n = 262), with prevalence varying among species from 0% to >7% of teeth affected. Those with the highest prevalence of ICATs include Pan troglodytes verus (9.8% of anterior teeth), Gorilla gorilla gorilla (2.6%), Cercopithecus denti (22.4%), Presbytis femoralis (19.5%), and Cercopithecus mitis (18.3%). ICATs make up 87.9% of carious lesions on anterior teeth. These results likely reflect dietary and food processing differences among species, but also between the sexes (e.g., 9.3% of all female P. troglodytes verus teeth were carious vs. 1.8% in males). Processing cariogenic fruits and seeds with the anterior dentition (e.g., wadging) likely contributes to ICAT formation. Further research is needed in living primate populations to ascertain behavioral/dietary influences on caries occurrence. Given the presence of ICATs in frugivorous primates, their diagnosis in archaeological and paleontological specimens may shed light on diet and food processing behaviors in fossil primates.

Linking howler monkey ranging and defecation patterns to primary and secondary seed dispersal.

To define the chances of a dispersed seed to produce a new recruit, it is essential to consider all stages of the dispersal process. Howler monkeys are recognized to have positive impacts on forest regeneration, acting as primary dispersers. Furthermore, dung beetles attracted to their feces protect the seeds against predators, and provide a better microenvironment for germination due to the removal of fecal matter, to seed burial, and/or by reducing the spatial aggregation of seeds in fecal clumps. Despite the recognized positive effects of primary seed dispersal through defecation by howler monkeys for plant recruitment, there are some important aspects of their behavior, such as the habit of defecating in latrines, that remain to be explored. Here, we investigated the fate of Campomanesia xanthocarpa seeds defecated by brown howlers, Alouatta guariba clamitans, and the secondary seed dispersal by dung beetles, considering how this process is affected by the monkey's defecation patterns. We found that brown howler monkeys dispersed seeds from several species away from fruit-feeding trees, partly because defecation under the canopy of such trees was not very frequent. Instead, most defecations were associated with latrines under overnight sleeping trees. Despite a very similar dung beetle community attracted to howler feces in latrines and fruit-feeding sites, seeds were more likely to be buried when deposited in latrines. In addition, C. xanthocarpa seeds showed higher germination and establishment success in latrines, but this positive effect was not due to the presence of fecal matter surrounding seeds. Our results highlight that A. guariba clamitans acts as a legitimate seed disperser of C. xanthocarpa seeds in a preserved context of the Brazilian Atlantic Forest and that defecations in latrines increase the dispersal effectiveness.

Ecological and evolutionary significance of primates' most consumed plant families.

Angiosperms have been essential components of primate diets for millions of years, but the relative importance of different angiosperm families remains unclear. Here, we assess the contribution and ecological and evolutionary significance of plant families to diets of wild primates by compiling an unprecedented dataset of almost 9000 dietary records from 141 primary sources covering 112 primate species. Of the 205 angiosperm plant families recorded in primate diets, only 10 were consumed by more than half of primate species. Plants of the Moraceae and Fabaceae families were the most widely and frequently consumed, and they likely represent keystone resources for primates. Over 75% of species fed on these two families, and together they made up a median of approximately 13% of primate diets. By analysing the relative proportion of different plant parts consumed, we found that Moraceae was mainly eaten as fruit and Fabaceae as non-fruit parts, with the consumption of these two families not showing a significant phylogenetic signal across primate species. Moraceae consumption was associated with small home range sizes, even though more frugivorous primates tended to have larger home ranges compared to more folivorous species, possibly due to the year-round availability of moraceous fruits and the asynchrony in their phenology. Our results suggest that primates may be intricately and subtly shaped by the plant families that they have consumed over millions of years, and highlight the importance of detailed dietary studies to better understand primate ecology and evolution.