Untargeted Metabolomics Reveals Fruit Secondary Metabolites Alter Bat Nutrient Absorption.

The ecological interaction between fleshy fruits and frugivores is influenced by diverse mixtures of secondary metabolites that naturally occur in the fruit pulp. Although some fruit secondary metabolites have a primary role in defending the pulp against antagonistic frugivores, these metabolites also potentially affect mutualistic interactions. The physiological impact of these secondary metabolites on mutualistic frugivores remains largely unexplored. Using a mutualistic fruit bat (Carollia perspicillata), we showed that ingesting four secondary metabolites commonly found in plant tissues affects bat foraging behavior and induces changes in the fecal metabolome. Our behavioral trials showed that the metabolites tested typically deter bats. Our metabolomic surveys suggest that secondary metabolites alter, either by increasing or decreasing, the absorption of essential macronutrients. These behavioral and physiological effects vary based on the specific identity and concentration of the metabolite tested. Our results also suggest that a portion of the secondary metabolites consumed is excreted by the bat intact or slightly modified. By identifying key shifts in the fecal metabolome of a mutualistic frugivore caused by secondary metabolite consumption, this study improves our understanding of the effects of fruit chemistry on frugivore physiology.

Patterns of variation in fleshy diaspore size and abundance from Late Triassic-Oligocene.

Vertebrate-mediated seed dispersal is a common attribute of many living plants, and variation in the size and abundance of fleshy diaspores is influenced by regional climate and by the nature of vertebrate seed dispersers among present-day floras. However, potential drivers of large-scale variation in the abundance and size distributions of fleshy diaspores through geological time, and the importance of geographic variation, are incompletely known. This knowledge gap is important because fleshy diaspores are a key mechanism of energy transfer from photosynthesis to animals and may in part explain the diversification of major groups within birds and mammals. Various hypotheses have been proposed to explain variation in the abundance and size distribution of fleshy diaspores through time, including plant-frugivore co-evolution, angiosperm diversification, and changes in vegetational structure and climate. We present a new data set of more than 800 georeferenced fossil diaspore occurrences spanning the Triassic-Oligocene, across low to mid- to high palaeolatitudes. We use this to quantify patterns of long-term change in fleshy diaspores, examining the timing and geographical context of important shifts as a test of the potential evolutionary and climatic explanations. We find that the fleshy fruit sizes of angiosperms increased for much of the Cretaceous, during the early diversification of angiosperms from herbaceous ancestors with small fruits. Nevertheless, this did not cause a substantial net change in the fleshy diaspore size distributions across seed plants, because gymnosperms had achieved a similar size distribution by at least the Late Triassic. Furthermore, gymnosperm-dominated Mesozoic ecosystems were mostly open, and harboured low proportions of specialised frugivores until the latest Cretaceous, suggesting that changes in vegetation structure and plant-frugivore co-evolution were probably not important drivers of fleshy diaspore size distributions over long timescales. Instead, fleshy diaspore size distributions may be largely constrained by physical or life-history limits that are shared among groups and diversify as a plant group expands into different growth forms/sizes, habitats, and climate regimes. Mesozoic gymnosperm floras had a low abundance of fleshy diaspores (<50% fleshy diaspore taxa), that was surpassed by some low-latitude angiosperm floras in the Cretaceous. Eocene angiosperm floras show a mid- to high latitude peak in fleshy fruit abundance, with very high proportions of fleshy fruits that even exceed those seen at low latitudes both in the Eocene and today. Mid- to high latitude proportions of fleshy fruits declined substantially over the Eocene-Oligocene transition, resulting in a shift to more modern-like geographic distributions with the highest proportion of fleshy fruits occurring in low-latitude tropical assemblages. This shift was coincident with global cooling and the onset of Southern Hemisphere glaciation, suggesting that rapid cooling at mid- and high latitudes caused a decrease in availability of the climate conditions most favourable for fleshy fruits in angiosperms. Future research could be focused on examining the environmental niches of modern fleshy fruits, and the potential effects of climate change on fleshy fruit and frugivore diversity.

Thermal niche breadth and their relationship with sturnira bat species diversification.

The interaction between climatic conditions and the ability of organisms to maintain homeostasis regulates the distribution of species on the planet. However, its influence on macroevolutionary dynamics is not well understood. It has been suggested that diversification rates will be different in lineages with narrow thermal niches (specialists) to diversification rates in generalist lineages, but the evidence for this is elusive. Here, we tested this hypothesis by using the most diverse (in species richness and geographic range variation) tropical bat genus within the Phyllostomidae family. We estimated the realized thermal niche breadth of Sturnira species from their geographic range and categorized them as generalists, cold specialists, or warm specialists. We compared dynamic evolutionary models that differ in 1) niche breadth evolution, 2) parental niche breadth inheritance, and 3) whether niche breadth evolution is associated with shifts in diversification rates. Our best-performing model indicates that most Sturnira species arose as specialists in warm climates and that over time, their niche breadth broadens, and just a subset of those species becomes specialists in cold environments. We found that the evolution of realized thermal niche breadth causes fluctuations in per-lineage rates of diversification, where warm specialists boast the highest speciation rates. However, we found no evidence of these changes in niche neither triggering nor being a result of speciation events themselves; this suggests that diversification events in Sturnira could instead depend on allopatric speciation processes such as the development of geographic barriers.

Reproductive phenologies of phyllostomid bat populations and ensembles from lowland Amazonia.

Natural selection should favor individuals that synchronize energy-demanding aspects of reproductive activity with periods of high resource abundance and predictability, leading to seasonal patterns of reproduction at the population level. Nonetheless, few studies-especially those on bats in the Neotropics-have used rigorous quantitative criteria to distinguish among phenological patterns for different populations from the same habitat or for the same species in different habitats. To explore such issues, we quantified annual patterns of reproduction in male and in female bats from lowland Amazonia (environs of Iquitos, Peru), and did so at the level of populations and ensembles. Five species exhibited unimodal patterns including Artibeus obscurus, A. planirostris, Carollia benkeithi, Phyllostomus hastatus, and Rhinophylla pumilio. Two species (A. lituratus and Glossophaga soricina) evinced bimodal patterns with reproductive peaks separated by patterns of inactivity, whereas four species (C. brevicauda, C. perspicillata, Sturnira lilium, and S. tildae) evinced a bimodal pattern in which peaks in activity occur in tandem, with the first peak generally markedly higher than the second peak. Frugivore, gleaning animalivore, and nectarivore ensembles exhibited bimodal, unimodal, and bimodal reproductive phenologies, respectively. Nonetheless, interannual variation in phenology (i.e., the monthly timing of peaks within a season rather than the number of peaks per year) characterized four (A. obscurus, C. brevicauda, C. perspicillata, and S. lilium) of the eight species and each of the three ensembles (frugivores, gleaning animalivores, and nectarivores) with adequate sampling. Regardless of interspecific variation in strategies, the phenology of reproduction enhances the likelihood that parturition and recruitment of young into the population occurs during the wet season, the period of likely highest resource abundance. Based on a comparison of our results with those from other well-studied bat populations, four species did not exhibit geographic variation in reproductive phenologies (A. obscurus, G. soricina, C. brevicauda, and R. pumilio), whereas three species evinced such geographic variation (A. lituratus, A. planirostris, and C. perspicillata). Climate change will likely alter the seasons and extents of propitious times for reproductive activities, as well as the reliability of proximate cues for initiating reproduction, compromising current reproductive strategies and leading to altered phenological patterns of reproduction or reproductive success, possibly resulting in local extinction of some species.

La selección natural debería favorecer a individuos que sincronicen aspectos de alta demanda de energía en su actividad reproductiva con períodos de alta abundancia y previsibilidad de recursos, lo que conduciría a patrones estacionales de reproducción a nivel poblacional. No obstante, pocos estudios, especialmente estudios sobre murciélagos en el Neotrópico, han utilizado criterios cuantitativos rigurosos para distinguir entre patrones fenológicos ya sea para diferentes poblaciones dentro del mismo hábitat o para la misma especie en diferentes hábitats. Para explorar este tema, cuantificamos los patrones anuales de reproducción de murciélagos machos (porcentaje de la población con testículos escrotales) y hembras (porcentaje de la población embarazada o lactante) en regiones bajas de la Amazonía (alrededores de Iquitos, Perú) a nivel de poblaciones y de ensamblajes. Cinco especies exhibieron patrones unimodales, incluidos Artibeus obscurus, Artibeus planirostris, Carollia benkeithi, Phyllostomus hastatus, y Rhinophylla pumilio. Dos especies (Artibeus lituratus y Glossophaga soricina) mostraron patrones bimodales, con picos reproductivos separados por patrones de inactividad, mientras que cuatro especies (Carollia brevicauda, Carollia perspicillata, Sturnira lilium, y Sturnira tildae) mostraron un patrón bimodal en el que los picos de actividad ocurren en tándem, con un primer pico considerablemente más alto que el segundo. Los grupos de frugívoros, animalívoros y nectarívoros exhibieron fenologías reproductivas bimodales, unimodales y bimodales respectivamente. No obstante, la variación interanual en la fenología (es decir, el mes dentro de una temporada en que ocurren los picos en lugar del número de picos por año) caracterizó a cuatro (A. obscurus, C. brevicauda, C. perspicillata y S. lilium) de las ocho especies y cada uno de los tres ensamblajes (frugívoros, animalívoros y nectarívoros) con un tamaño de muestra adecuado. Independientemente de la variación en las estrategias, la fenología en la reproducción aumenta la probabilidad de que el parto y el reclutamiento de crías en la población ocurran en la estación húmeda, el período de mayor abundancia de recursos. Cuando comparamos nuestros resultados con los de otras poblaciones de murciélagos mejor estudiadas, cuatro especies no mostraron variación geográfica en sus estrategias reproductivas (A. obscurus, G. soricina, C. brevicauda y R. pumilio), mientras que tres especies si mostraron esta variación geográfica (A. lituratus, A. planirostris y C. perspicillata). Es probable que el cambio climático altere las estaciones y la duración de los periodos propicios para el desarrollo de actividades reproductivas de alta demanda de energía, así como la regularidad de las señales activantes para iniciar la actividad reproductiva, comprometiendo las estrategias reproductivas actuales y conllevando a patrones fenológicos de reproducción alterados, lo que para algunas especies podría resultar en extinciones locales.

High flexibility in diet and ranging patterns in two golden monkey (Cercopithecus mitis kandti) populations in Rwanda.

Many primates exhibit behavioral flexibility which allows them to adapt to environmental change and different habitat types. The golden monkey (Cercopithecus mitis kandti) is a little-studied endangered primate subspecies endemic to the Virunga massif and the Gishwati forest in central Africa. In the Virunga massif, golden monkeys are mainly found in the bamboo forest, while in the Gishwati forest they live in mixed tropical montane forest. Here we describe and compare the diet of golden monkeys in both fragments. Over 24 consecutive months from January 2017 we used scan sampling to record feeding and ranging behavior of two Virunga groups and one Gishwati group totaling ca. 240 individuals. We also examined the phenology of bamboo and fruit trees, key seasonal food plant species for the monkeys. Golden monkeys fed on more than 100 plant species. The Virunga groups were mostly folivorous (between 72.8% and 87.16% of the diet) and fed mostly on young bamboo leaves and bamboo shoots, while 48.69% of the diet of the Gishwati group consisted of fruit from 22 different tree and shrub species. Bamboo shoots and fruit are seasonally available foods and were consumed regularly throughout the period when they were available. Despite being the smallest of the three study groups, the Gishwati group had a larger home range area (150.07 ha) compared to both Virunga groups (25.24 and 91.3 ha), likely driven by the differences in availability and distribution of fruit and bamboo in the habitats. Like other blue monkey subspecies, golden monkeys appear to have a flexible dietary strategy enabling them to adjust diet and ranging behavior to local habitats and available food resources. Additional studies and continuing conservation efforts are needed to better understand how variation in feeding and ranging ecology affects reproduction, population growth, and carrying capacity.

Foraging strategies, craniodental traits, and interaction in the bite force of Neotropical frugivorous bats (Phyllostomidae: Stenodermatinae).

Bats in the family Phyllostomidae exhibit great diversity in skull size and morphology that reflects the degree of resource division and ecological overlap in the group. In particular, the subfamily Stenodermatinae has high morphological diversification associated with cranial and mandibular traits that are associated with the ability to consume the full range of available fruits (soft and hard).We analyzed craniodental traits and their relationship to the bite force in 343 specimens distributed in seven species of stenodermatine bats with two foraging strategies: nomadic and sedentary frugivory. We evaluated 19 traits related to feeding and bite force in live animals by correcting bite force with body size.We used a generalized linear model (GLM) and post hoc tests to determine possible relationships and differences between cranial traits, species, and sex. We also used Blomberg's K to measure the phylogenetic signal and phylogenetic generalized least-squares (PGLS) to ensure the phylogenetic independence of the traits.We found that smaller nomadic species, A. anderseni and A. phaeotis , have a similar bite force to the large species A. planirostris and A. lituratus; furthermore, P. helleri registered a bite force similar to that of the sedentary bat, S. giannae. Our study determined that all the features of the mandible and most of the traits of the skull have a low phylogenetic signal. Through the PGLS, we found that the diet and several cranial features (mandibular toothrow length, dentary length, braincase breadth, mastoid breadth, greatest length of skull, condylo-incisive length, and condylo-canine length) determined bite force performance among Stenodermatiane.Our results reinforce that skull size is a determining factor in the bite force, but also emphasize the importance of its relationships with morphology, ecology, and phylogeny of the species, which gives us a better understanding of the evolutionary adaptions of this highly diverse Neotropical bat group.

Germination success of large-seeded plant species ingested by howler monkeys in tropical rain forest fragments.

PREMISE: Primates are important seed dispersers, especially for large-seeded (>1 cm long) tropical species in continuous and fragmented rainforests. METHODS: In three forest fragments within the Montes Azules Biosphere Reserve, southern Mexico, we investigated the effect of seed passage through the gut of howler monkeys (Alouatta pigra) on the germination rate and maximum germination (%) of native, large-seeded species. One group of howler monkeys, per fragment, was followed and fresh feces collected. Large seeds were removed to compare their germination success with non-ingested seeds of the same species collected underneath parent plants. RESULTS: Feces contained large seeds from seven tree species (Ampelocera hottlei, Castilla elastica, Dialium guianense, Garcinia intermedia, Pourouma bicolor, Spondias mombin, Trophis racemosa) and one liana species (Abuta panamensis). Except for G. intermedia, ingested seeds germinated significantly faster than non-ingested seeds, which had negligible germination. Ingested seeds of D. guianense, P. bicolor, S. mombin, T. racemosa, and A. panamensis had significantly greater germination, while G. intermedia had significantly lower germination and seed ingestion had no apparent effect for A. hottlei and C. elastica. CONCLUSIONS: In general, seed ingestion by howler monkeys confers faster germination compared with non-ingested seeds. Faster germination reduces predation probabilities and increases seedling establishment in forest fragments. Primate dispersal services contribute to germination heterogeneity within plant populations of old-growth forest species and to their persistence in forest fragments.

Uniting niche differentiation and dispersal limitation predicts tropical forest succession.

Tropical secondary forests are increasingly important for carbon sequestration and biodiversity conservation worldwide; yet, we still cannot accurately predict community turnover during secondary succession. We propose that integrating niche differentiation and dispersal limitation will generate an improved theoretical explanation of tropical forest succession. The interaction between seed sources and dispersers regulates seed movement throughout succession, and recent technological advances in animal tracking and molecular analyses enable us to accurately monitor seed movement as never before. We propose a framework to bridge the gap between niche differentiation and dispersal limitation. The Source-Disperser Limitation Framework (SDLF) provides a way to better predict secondary tropical forest succession across gradients of landscape disturbance by integrating seed sources and frugivore behavior.

Frugivore species maintain their structural role in the trophic and spatial networks of seed dispersal interactions.

Trophic relationships have inherent spatial dimensions associated with the sites where species interactions, or their delayed effects, occur. Trophic networks among interacting species may thus be coupled with spatial networks linking species and habitats whereby animals connect patches across the landscape thanks to their high mobility. This trophic and spatial duality is especially inherent in processes like seed dispersal by animals, where frugivores consume fruit species and deposit seeds across habitats. We analysed the frugivore-plant interactions and seed deposition patterns of a diverse assemblage of frugivores in a heterogeneous landscape in order to determine whether the roles of frugivores in network topology are correlated across trophic and spatial networks of seed dispersal. We recorded fruit consumption and seed deposition by birds and mammals during 2 years in the Cantabrian Range (N Spain). We then constructed two networks of trophic (i.e. frugivore-plant) and spatial (i.e. frugivore-seed deposition habitat) interactions and estimated the contributions of each frugivore species to the network structure in terms of nestedness, modularity and complementary specialization. We tested whether the structural role of frugivore species was correlated across the trophic and spatial networks, and evaluated the influence of each frugivore abundance and body mass in that relationship. Both the trophic and the spatial networks were modular and specialized. Trophic modules matched medium-sized birds with fleshy-fruited trees, and small bird and mammals with small-fruit trees and shrubs. Spatial modules associated birds with woody canopies, and mammals with open habitats. Frugivore species maintained their structural role across the trophic and spatial networks of seed dispersal, even after accounting for frugivore abundance and body mass. The modularity found in our system points to complementarity between birds and mammals in the seed dispersal process, a fact that may trigger landscape-scale secondary succession. Our results open up the possibility of predicting the consumption pattern of a diverse frugivore community, and its ecological consequences, from the uneven distribution of fleshy-fruit resources in the landscape.

RESUMEN Las relaciones tróficas tienen una dimensión espacial asociada a los sitios donde ocurren o tienen lugar sus efectos. Las redes tróficas entre especies pueden, por tanto, emparejarse con las redes espaciales que vinculan a las especies con sus hábitats, y donde los animales conectan parches gracias a su alta movilidad. Esta dualidad trófica y espacial es especialmente inherente a procesos como la dispersión de semillas, donde los animales frugívoros consumen distintas especies de plantas con fruto carnoso y depositan sus semillas en distintos hábitats. Aquí analizamos las interacciones frugívoro-planta y los patrones de deposición de semillas de un conjunto diverso de frugívoros en un paisaje heterogéneo, con el fin de determinar si el papel topológico de los frugívoros en la red trófica de dispersión de semillas se correlaciona con dicho papel en la red espacial de deposición. Para ello, registramos el consumo de frutos y la deposición de semillas por aves y mamíferos durante dos años en la Cordillera Cantábrica (N España). Construimos dos redes de interacciones, una trófica (frugívoro-planta) y otra espacial (frugívoro-hábitat de deposición de semillas), y estimamos la contribución de las especies animales a la estructura de cada red, en términos de anidamiento, modularidad y especialización. Analizamos si el papel estructural de los distintos frugívoros se correlacionaba a través de ambas redes, y evaluamos la influencia de la abundancia relativa y la masa corporal de los frugívoros en dicha relación. Encontramos un patrón general de modularidad y especialización tanto en la red trófica como en la espacial. Los módulos tróficos agruparon principalmente a aves de mediano tamaño con árboles con frutos carnosos, y a aves de pequeño tamaño y mamíferos con arbustos de fruto carnoso. Los módulos espaciales asociaron en general a las aves con hábitats arbolados y a los mamíferos con hábitats abiertos. Las especies de frugívoros mantuvieron su papel estructural tanto en la red trófica como en la espacial, incluso después de tener en cuenta la abundancia relativa y la masa corporal de los frugívoros. El patrón de modularidad detectado en el sistema apunta a una importante complementariedad funcional entre aves y mamíferos en el proceso de dispersión de semillas, de modo que puede favorecer la sucesión secundaria de la vegetación a escala de paisaje. Nuestros resultados abren la posibilidad de predecir el patrón de consumo de una comunidad diversa de frugívoros así como sus consecuencias ecológicas a partir de la distribución desigual de los recursos tróficos en el paisaje.

Introduction to the Special Issue: The role of seed dispersal in plant populations: perspectives and advances in a changing world.

Despite the importance of seed dispersal as a driving process behind plant community assembly, our understanding of the role of seed dispersal in plant population persistence and spread remains incomplete. As a result, our ability to predict the effects of global change on plant populations is hampered. We need to better understand the fundamental link between seed dispersal and population dynamics in order to make predictive generalizations across species and systems, to better understand plant community structure and function, and to make appropriate conservation and management responses related to seed dispersal. To tackle these important knowledge gaps, we established the CoDisperse Network and convened an interdisciplinary, NSF-sponsored Seed Dispersal Workshop in 2016, during which we explored the role of seed dispersal in plant population dynamics (NSF DEB Award # 1548194). In this Special Issue, we consider the current state of seed dispersal ecology and identify the following collaborative research needs: (i) the development of a mechanistic understanding of the movement process influencing dispersal of seeds; (ii) improved quantification of the relative influence of seed dispersal on plant fitness compared to processes occurring at other life history stages; (iii) an ability to scale from individual plants to ecosystems to quantify the influence of dispersal on ecosystem function; and (iv) the incorporation of seed dispersal ecology into conservation and management strategies.

Adapting Methodology Used on Captive Subjects for Estimating Gut Passage Time in Wild Monkeys.

Gut passage time of food has consequences for primate digestive strategies, which subsequently affect seed dispersal. Seed dispersal models are critical in understanding plant population and community dynamics through estimation of seed dispersal distances, combining movement data with gut passage times. Thus, developing methods to collect in situ data on gut passage time are of great importance. Here we present a first attempt to develop an in situ study of gut passage time in an arboreal forest guenon, the samango monkey (Cercopithecus albogularis schwarzi) in the Soutpansberg Mountains, South Africa. Cercopithecus spp. consume large proportions of fruit and are important seed dispersers. However, previous studies on gut passage times have been conducted only on captive Cercopithecusspp. subjects, where movement is restricted, and diets are generally dissimilar to those observed in the wild. Using artificial digestive markers, we targeted provisioning of a male and a female samango monkey 4 times over 3 and 4 days, respectively. We followed the focal subjects from dawn until dusk following each feeding event, collecting faecal samples and recording the date and time of deposition and the number of markers found in each faecal sample. We recovered 6.61 ± 4 and 13 ± 9% of markers from the male and the female, respectively, and were able to estimate a gut passage window of 16.63-25.12 h from 3 of the 8 trials. We discuss methodological issues to help future researchers to develop in situ studies on gut passage times.

Differentiation during fig ontogeny suggests opposing selection by mutualists.

Dioecy allows separation of female and male functions and therefore facilitates separate co-evolutionary pathways with pollinators and seed dispersers. In monoecious figs, pollinators' offspring develop inside the syconium by consuming some of the seeds. Flower-stage syconia must attract pollinators, then ripen and attract seed dispersers. In dioecious figs, male ("gall") figs produce pollen but not viable seeds, as the pollinators' larvae eat all seeds, while female ("seed") figs produce mostly viable seeds, as pollinators cannot oviposit in the ovules. Hence, gall and seed figs are under selection to attract pollinators, but only seed figs must attract seed dispersers. We test the hypothesis that seed and gall syconia at the flower stage will be similar, while at the fruiting stage they will differ. Likewise, monoecious syconia will be more similar to seed than gall figs because they must attract both pollinators and seed dispersers. We quantified syconium characteristics for 24 dioecious and 11 monoecious fig species and recorded frugivore visits. We show that seed and gall syconia are similar at the flower stage but differ at the fruit stage; monoecious syconia are more similar to seed syconia than they are to gall syconia; seed and gall syconia differentiate through their ontogeny from flower to fruit stages; and frugivores visit more monoecious and seed syconia than gall syconia. We suggest that similarity at the flower stage likely enhances pollination in both seed and gall figs and that differentiation after pollination likely enhances attractiveness to seed dispersers of syconia containing viable seeds. These ontogenetic differences between monoecious and dioecious species provide evidence of divergent responses to selection by pollinators and seed dispersers.

Long-term trends in fruit production in a tropical forest at Ngogo, Kibale National Park, Uganda.

Fruit production in tropical forests varies considerably in space and time, with important implications for frugivorous consumers. Characterizing temporal variation in forest productivity is thus critical for understanding adaptations of tropical forest frugivores, yet long-term phenology data from the tropics, in particular from African forests, are still scarce. Similarly, as the abiotic factors driving phenology in the tropics are predicted to change with a warming climate, studies documenting the relationship between climatic variables and fruit production are increasingly important. Here we present data from 19 years of monitoring the phenology of 20 tree species at Ngogo in Kibale National Park, Uganda. Our aims were to characterize short- and long-term trends in productivity and to understand the abiotic factors driving temporal variability in fruit production. Short-term (month-to-month) variability in fruiting was relatively low at Ngogo, and overall fruit production increased significantly through the first half of the study. Among the abiotic variables we expected to influence phenology patterns (including rainfall, solar irradiance, and average temperature), only average temperature was a significant predictor of monthly fruit production. We discuss these findings as they relate to the resource base of the frugivorous vertebrate community inhabiting Ngogo.

Foraging dispersion of Ryukyu flying-foxes and relationships with fig abundance in East-Asian subtropical island forests.

BACKGROUND: Figs are widely distributed key resources to many tropical-subtropical animals, and flying-foxes are major consumers and seed dispersers of figs. Bat-fig interrelationships, however, may vary among species differing in fruiting traits, i.e., bat- versus bird-dispersed figs. We examined Ryukyu flying-fox foraging dispersion and the relationships with tree species composition and fig abundance in forests of Iriomote Island. RESULTS: Bat foraging dispersion showed no spatial patterns with respect to different areas of the island, and was not explained by heterogeneity, density, or basal area (BA) of total trees, nor by relative density or BA of fruiting trees or total fruiting figs among sites. Instead, bat densities were positively dependent on the relative density of total figs, and particularly the relative BA of bat-dispersed figs Ficus septica and F. variegata. Both species were dominant figs in forests, fruiting asynchronously with long crop seasons, and were used as predominant foods. Bats foraged mostly solitarily and the mean density was in a hump-shaped relationship with crop sizes of the dominant bat-figs. These two species and Ficus benguetensis are larger-sized bat-figs, all contained more seeds, higher dry-pulp mass and water mass, but not necessarily water content. By approximate estimation, higher proportions of seeds of these bat-figs would have been removed from fruits through the bat consumption, than that of small-sized bird-figs like F. virgata, F. superba, and F. microcarpa. CONCLUSIONS: The foraging dispersion of Ryukyu flying-foxes in forests depends on the availability of the most abundant bat-figs that serve as predominant foods. Intermediate levels of crop sizes of theses figs appear most fit with their solitary foraging. Our results suggest that as density and BA coverage of these dominant bat-figs are below a certain level, their effectiveness to attract bats may dwindle and so would their chance of dispersal by bats.

Atlantic frugivory: a plant-frugivore interaction data set for the Atlantic Forest.

The data set provided here includes 8,320 frugivory interactions (records of pairwise interactions between plant and frugivore species) reported for the Atlantic Forest. The data set includes interactions between 331 vertebrate species (232 birds, 90 mammals, 5 fishes, 1 amphibian, and 3 reptiles) and 788 plant species. We also present information on traits directly related to the frugivory process (endozoochory), such as the size of fruits and seeds and the body mass and gape size of frugivores. Data were extracted from 166 published and unpublished sources spanning from 1961 to 2016. While this is probably the most comprehensive data set available for a tropical ecosystem, it is arguably taxonomically and geographically biased. The plant families better represented are Melastomataceae, Myrtaceae, Moraceae, Urticaceae, and Solanaceae. Myrsine coriacea, Alchornea glandulosa, Cecropia pachystachya, and Trema micrantha are the plant species with the most animal dispersers (83, 76, 76, and 74 species, respectively). Among the animal taxa, the highest number of interactions is reported for birds (3,883) followed by mammals (1,315). The woolly spider monkey or muriqui, Brachyteles arachnoides, and Rufous-bellied Thrush, Turdus rufiventris, are the frugivores with the most diverse fruit diets (137 and 121 plants species, respectively). The most important general patterns that we note are that larger seeded plant species (>12 mm) are mainly eaten by terrestrial mammals (rodents, ungulates, primates, and carnivores) and that birds are the main consumers of fruits with a high concentration of lipids. Our data set is geographically biased, with most interactions recorded for the southeast Atlantic Forest.

Long-term consistency in spatial patterns of primate seed dispersal.

Seed dispersal is a key ecological process in tropical forests, with effects on various levels ranging from plant reproductive success to the carbon storage potential of tropical rainforests. On a local and landscape scale, spatial patterns of seed dispersal create the template for the recruitment process and thus influence the population dynamics of plant species. The strength of this influence will depend on the long-term consistency of spatial patterns of seed dispersal. We examined the long-term consistency of spatial patterns of seed dispersal with spatially explicit data on seed dispersal by two neotropical primate species, Leontocebus nigrifrons and Saguinus mystax (Callitrichidae), collected during four independent studies between 1994 and 2013. Using distributions of dispersal probability over distances independent of plant species, cumulative dispersal distances, and kernel density estimates, we show that spatial patterns of seed dispersal are highly consistent over time. For a specific plant species, the legume Parkia panurensis, the convergence of cumulative distributions at a distance of 300 m, and the high probability of dispersal within 100 m from source trees coincide with the dimension of the spatial-genetic structure on the embryo/juvenile (300 m) and adult stage (100 m), respectively, of this plant species. Our results are the first demonstration of long-term consistency of spatial patterns of seed dispersal created by tropical frugivores. Such consistency may translate into idiosyncratic patterns of regeneration.

Internal seed dispersal by parrots: an overview of a neglected mutualism.

Despite the fact that parrots (Psitacifformes) are generalist apex frugivores, they have largely been considered plant antagonists and thus neglected as seed dispersers of their food plants. Internal dispersal was investigated by searching for seeds in faeces opportunistically collected at communal roosts, foraging sites and nests of eleven parrot species in different habitats and biomes in the Neotropics. Multiple intact seeds of seven plant species of five families were found in a variable proportion of faeces from four parrot species. The mean number of seeds of each plant species per dropping ranged between one and about sixty, with a maximum of almost five hundred seeds from the cacti Pilosocereus pachycladus in a single dropping of Lear's Macaw (Anodorhynchus leari). All seeds retrieved were small (<3 mm) and corresponded to herbs and relatively large, multiple-seeded fleshy berries and infrutescences from shrubs, trees and columnar cacti, often also dispersed by stomatochory. An overview of the potential constraints driving seed dispersal suggest that, despite the obvious size difference between seeds dispersed by endozoochory and stomatochory, there is no clear difference in fruit size depending on the dispersal mode. Regardless of the enhanced or limited germination capability after gut transit, a relatively large proportion of cacti seeds frequently found in the faeces of two parrot species were viable according to the tetrazolium test and germination experiments. The conservative results of our exploratory sampling and a literature review clearly indicate that the importance of parrots as endozoochorous dispersers has been largely under-appreciated due to the lack of research systematically searching for seeds in their faeces. We encourage the evaluation of seed dispersal and other mutualistic interactions mediated by parrots before their generalized population declines contribute to the collapse of key ecosystem processes.

Dispersal limitation induces long-term biomass collapse in overhunted Amazonian forests.

Tropical forests are the global cornerstone of biological diversity, and store 55% of the forest carbon stock globally, yet sustained provisioning of these forest ecosystem services may be threatened by hunting-induced extinctions of plant-animal mutualisms that maintain long-term forest dynamics. Large-bodied Atelinae primates and tapirs in particular offer nonredundant seed-dispersal services for many large-seeded Neotropical tree species, which on average have higher wood density than smaller-seeded and wind-dispersed trees. We used field data and models to project the spatial impact of hunting on large primates by ∼ 1 million rural households throughout the Brazilian Amazon. We then used a unique baseline dataset on 2,345 1-ha tree plots arrayed across the Brazilian Amazon to model changes in aboveground forest biomass under different scenarios of hunting-induced large-bodied frugivore extirpation. We project that defaunation of the most harvest-sensitive species will lead to losses in aboveground biomass of between 2.5-5.8% on average, with some losses as high as 26.5-37.8%. These findings highlight an urgent need to manage the sustainability of game hunting in both protected and unprotected tropical forests, and place full biodiversity integrity, including populations of large frugivorous vertebrates, firmly in the agenda of reducing emissions from deforestation and forest degradation (REDD+) programs.

Parrots as key multilinkers in ecosystem structure and functioning.

Mutually enhancing organisms can become reciprocal determinants of their distribution, abundance, and demography and thus influence ecosystem structure and dynamics. In addition to the prevailing view of parrots (Psittaciformes) as plant antagonists, we assessed whether they can act as plant mutualists in the dry tropical forest of the Bolivian inter-Andean valleys, an ecosystem particularly poor in vertebrate frugivores other than parrots (nine species). We hypothesised that if interactions between parrots and their food plants evolved as primarily or facultatively mutualistic, selection should have acted to maximize the strength of their interactions by increasing the amount and variety of resources and services involved in particular pairwise and community-wide interaction contexts. Food plants showed different growth habits across a wide phylogenetic spectrum, implying that parrots behave as super-generalists exploiting resources differing in phenology, type, biomass, and rewards from a high diversity of plants (113 species from 38 families). Through their feeding activities, parrots provided multiple services acting as genetic linkers, seed facilitators for secondary dispersers, and plant protectors, and therefore can be considered key mutualists with a pervasive impact on plant assemblages. The number of complementary and redundant mutualistic functions provided by parrots to each plant species was positively related to the number of different kinds of food extracted from them. These mutually enhancing interactions were reflected in species-level properties (e.g., biomass or dominance) of both partners, as a likely consequence of the temporal convergence of eco-(co)evolutionary dynamics shaping the ongoing structure and organization of the ecosystem. A full assessment of the, thus far largely overlooked, parrot-plant mutualisms and other ecological linkages could change the current perception of the role of parrots in the structure, organization, and functioning of ecosystems.