Diet and seed dispersal of bearded capuchin monkeys (Sapajus libidinosus) in Brasilia National Park.

The dietary ecology of a species can provide information on habitat requirements, food resources, and trophic interactions, important to guide conservation efforts of wildlife populations in endangered habitats. In this study, we investigated the dietary ecology of bearded capuchin monkeys (Sapajus libidinosus) in Brasilia National Park, in the endangered Cerrado biome of central Brazil. To obtain diet composition and evaluate the role of these primates as seed dispersers of local tree species, fecal sample collections and feeding observations were performed for a 7-month period. To determine whether seeds germinated better after passing through a primate gut, we conducted germination trials with (i) pulped seeds from trees, (ii) depulped seeds from trees, (iii) seeds from feces planted with feces, and (iv) seeds from feces planted without feces. During experimental procedures, 7308 seeds from 8 families and 10 species were planted. We found that S. libidinosus spent more time feeding on fruits than on any other food item and the diet consisted of 33 plant species from 21 families. However, 20% of their diet consisted of anthropic food. Most seeds planted with feces germinated faster compared to seeds in other experimental treatments, suggesting that passing through the gut and being deposited with fecal material is advantageous. The bearded capuchins also defecated many medium- (5 species) and large-sized (2 species) seeds that may be inaccessible to smaller arboreal frugivores. The results obtained emphasize the important role of bearded capuchins as seed dispersers for the maintenance and conservation of the endangered Cerrado biome.

Negative density dependence characterizes mutualistic interactions between birds and fruiting plants across latitudes.

Negative density dependence (NDD) in biotic interactions of interference such as plant-plant competition, granivory and herbivory are well-documented mechanisms that promote species' coexistence in diverse plant communities worldwide. Here, we investigated the generality of a novel type of NDD mechanism that operates through the mutualistic interactions of frugivory and seed dispersal among fruit-eating birds and plants. By sampling community-wide frugivory interactions at high spatial and temporal resolution in Pennsylvania, Puerto Rico, Peru, Brazil and Argentina, we evaluated whether interaction frequencies between birds and fruit resources occurred more often (selection), as expected, or below expectations (under-utilization) set by the relative fruit abundance of the fruit resources of each plant species. Our models considered the influence of temporal scales of fruit availability and bird phylogeny and diets, revealing that NDD characterizes frugivory across communities. Irrespective of taxa or dietary guild, birds tended to select fruits of plant species that were proportionally rare in their communities, or that became rare following phenological fluctuations, while they mostly under-utilized abundant fruit resources. Our results demonstrate that negative density-dependence in frugivore-plant interactions provides a strong equalizing mechanism for the dispersal processes of fleshy-fruited plant species in temperate and tropical communities, likely contributing to building and sustaining plant diversity. This article is part of the theme issue 'Diversitydependence of dispersal: interspecific interactions determine spatial dynamics'.

Spatio-temporal variation of seed rain between urban and rural fragments of humid tropical forests / Variación espacio-temporal de la lluvia de semillas entre fragmentos urbanos y rurales de bosques tropicales húmedos

Introduction: The type of land use surrounding the remnants of tropical forest may generate changes in the characteristics of plant populations and communities. Consequently, there may be a significant reduction in processes of pollination and diasporas dispersion. Therefore, causing changes in some parameters of seed rain. Objective: To characterize and compare seed density, species richness, floristic composition, habit, dispersal syndrome, and successional category of seed rain between urban and rural fragments of Atlantic Forest, in the 2015 and 2016 weather seasons. Methods: The study areas were defined after mapping and quantification of urban and rural occupations around the remnants, based on satellite images. In each fragment, were installed 36 collectors of 0.25 m2. The material was collected monthly during two consecutive years. Results: Seed rain richness was higher in the urban fragment during the rainy season in the two years, whereas it was similar between the fragments in the dry season. The seed density in the rural fragment was higher than in the urban during the rainy season; did not vary in urban between years or between seasons; and it was higher in the rural fragment in the rainy season of one year. There was a difference in the floristic composition of the seed rain between the fragments along time. The variations in the functional attributes of habit, dispersal syndrome, and successional category, were explained by the variables fragment, season, and year. Conclusions: Differences in the characteristics of the seed rain between the fragments might reflect the spatial and temporal heterogeneity, due to the diverse uses of the soil and external pressures (anthropogenic actions) present in the surroundings of the forest fragments and temporal variation in precipitation.

Introducción: El tipo de uso del suelo que rodea los remanentes de bosque tropical puede generar cambios en las características de las poblaciones y comunidades vegetales. En consecuencia, puede haber una reducción significativa en los procesos de polinización y dispersión de las diásporas. Por lo tanto, provocando cambios en algunos parámetros de la lluvia de semillas. Objetivo: Caracterizar y comparar la densidad de semillas, la riqueza de especies, la composición florística, el hábito, el síndrome de dispersión y la categoría sucesional de la lluvia de semillas entre fragmentos urbanos y rurales de Mata Atlántica, en las estaciones climáticas del 2015 y 2016. Métodos: Las áreas de estudio se definieron luego del mapeo y cuantificación de las ocupaciones urbanas y rurales alrededor de los remanentes, con base en imágenes satelitales. En cada fragmento se instalaron 36 colectores de 0.25 m2. El material fue recolectado mensualmente durante dos años consecutivos. Resultados: La riqueza de lluvia de semillas fue mayor en el fragmento urbano durante la estación lluviosa en los dos años, mientras que fue similar entre los fragmentos en la estación seca. La densidad de semillas en el fragmento rural fue mayor que en el urbano durante la estación lluviosa; no varió en urbano entre años o entre estaciones; y fue mayor en el fragmento rural en la estación lluviosa del primer año. Hubo una diferencia en la composición florística de la lluvia de semillas entre los fragmentos a lo largo del tiempo. Las variaciones en los atributos funcionales de hábito, síndrome de dispersión y categoría sucesional, fueron explicadas por las variables fragmento, estación y año. Conclusiones: Las diferencias en las características de la lluvia de semillas entre los fragmentos podrían reflejar la heterogeneidad espacial y temporal, debido a los diversos usos del suelo y presiones externas (acciones antropogénicas) presentes en el entorno de los fragmentos de bosque y variación temporal de la precipitación.

Seed removal by the squirrel Notocitellus adocetus (Rodentia: Sciuridae) in Western México

Introduction: Seed dispersal and seed predation have important impacts on plant diversity and community structure. Rodents participate in both of these types of interactions. Objectives: To evaluate the removal of the seeds of Crescentia alata, Randia capitata, and Zea mays by the squirrel Notocitellus adocetus to determine how it affects these plant species, by dispersing or preying on their seeds. Methods: We studied 14 individuals for C. alata, 24 for R. capitata, and for Z. mays 35 individuals. We observed foraging and used camera traps to determine the part of the fruit (seed and/or pulp) consumed by the squirrels and the amount of fruit or seed consumed. We also placed fine sand traps (FST) to measure the percentage of seed removal. We quantified the fruits produced by the plant species studied and the percentage of damage caused by N. adocetus throughout the plots. Results: Notocitellus adocetus feeds on the seeds and pulp of C. alata and Z. mays. The species with the highest removal rate and the highest percentage of damage was C. alata. Zea mays was the plant species that had the highest percentage of removal from FST, the largest number of fruits, and the lowest percentage of damage. On FST, R. capitata had the lowest seed remotion. Conclusions: Notocitellus adocetus is considered a seed predator; however, due to its behavior and the characteristics of the fruits of C. alata and R. capitata, this rodent could make the seeds available to secondary seed dispersers.

Introducción: La dispersión y depredación de semillas tienen efectos importantes en la diversidad de plantas y estructura de las comunidades. Los roedores participan en estos tipos de interacciones. Objetivos: Evaluar la remoción de semillas de Crescentia alata, Randia capitata y Zea mays por la ardilla Notocitellus adocetus, para determinar su efecto en estas especies de plantas, dispersando o depredando semillas. Métodos: Estudiamos 14 individuos de C. alata, 24 para R. capitata y 35 individuos para Z. mays. Observamos el forrajeo y usamos cámaras trampas para determinar la parte del fruto (semilla y/o pulpa) consumida y la intensidad de consumo por las ardillas. También colocamos trampas de arena fina (FST) para medir el porcentaje de remoción de semillas. Cuantificamos los frutos producidos por las especies estudiadas y el porcentaje de daño ocasionado por N. adocetus, mediante parcelas. Resultados: Notocitellus adocetus se alimenta de las semillas y pulpa de C. alata y Z. mays. La especie que tuvo mayor tasa de remoción y mayor porcentaje de daño fue C. alata. La especie con mayor porcentaje de remoción, mayor número de frutos y menor daño en las FST fue Z. mays. En las trampas de arena fina, R. capitata tuvo la menor remoción de semillas. Conclusiones: Notocitellus adocetus es considerada depredadora de semillas, no obstante, por su comportamiento y las características de los frutos de C. alata y R. capitata, este roedor podría dejar disponibles las semillas a dispersores secundarios de semillas.

Moving towards a comprehensive view of the spatial processes in seed dispersal networks: Embracing metacommunities.

The current biodiversity crisis requires efficient approaches to address the ongoing impoverishment of natural communities and the depletion of ecosystem services and functions. In this sense, identifying key species that promote the functioning of ecological processes can be strategic to guide actions aiming at the conservation and restoration of biodiversity. Node-level metrics in interaction networks can be helpful to identify those key species, as they measure the role each species plays in organizing the interactions. Moreover, ecological correlates of species structural roles may vary between local and global networks of interactions, reflecting distinct mechanisms acting at different spatial scales. By studying local seed dispersal networks and one global meta-network combining those local networks, Moulatlet et al. identified the most important traits explaining bird species centrality at varying spatial scales. They found that body mass was the main trait explaining centrality at the local scale, whereas range size was the main predictor of species centrality at the global scale. In this contribution, besides assessing local interaction networks, Moulatlet et al. adopt a biogeographical perspective to seed dispersal systems, extending our knowledge about the possible mechanisms that underlie the organization of interacting assemblages when changing the spatial scale of observation. Future efforts on this field could include an intermediate scale, comprising the level of metacommunities, shedding light on the interplay between local and spatial processes, both embedded in biogeographical realms, when determining the organization of interactions and the ecological correlates of species roles.

A atual crise da biodiversidade requer abordagens eficientes para lidar com o empobrecimento contínuo das comunidades naturais e com o esgotamento das funções e dos serviços ecossistêmicos. Neste sentido, identificar espécies-chave que promovam o funcionamento dos processos ecológicos pode ser estratégico para guiar ações que visam a conservação e a restauração da biodiversidade. Métricas em nível dos nós em redes de interação podem ser úteis para identificar tais espécies-chave, já que quantificam o papel que cada espécie desempenha em organizar as interações. Além disso, os correlatos ecológicos dos papéis estruturais das espécies podem variar entre redes de interações locais e globais, refletindo os distintos mecanismos que atuam em diferentes escalas espaciais. Ao estudar redes de dispersão de sementes locais e uma meta-rede global que combina essas redes locais, Moulatlet et al. identificaram as características mais importantes para explicar a centralidade das espécies de aves em diferentes escalas espaciais. Eles encontraram a massa corporal como principal característica que explicava a centralidade na escala local, enquanto o tamanho da distribuição foi o principal preditor da centralidade das espécies na escala global. Nesta contribuição, além de avaliar redes de interação locais, Moulatlet et al. adotaram uma perspectiva biogeográfica ao tratar os sistemas de dispersão de sementes, ampliando nosso conhecimento sobre os possíveis mecanismos subjacentes à organização das interações quando mudamos a escala espacial de observação. Esforços futuros neste campo poderiam incluir uma escala intermediária, compreendendo o nível de metacomunidades, buscando esclarecer as relações entre processos locais e processos espaciais, ambos inseridos em domínios biogeográficos, ao determinar a organização das interações e os correlatos ecológicos dos papéis estruturais das espécies.

Fruit and seed traits and vertebrate-fruit interactions of tree species occurring in Guyana, Suriname, and French Guiana.

Seed dispersal is widely considered an important mechanism for the conservation of plant diversity. In tropical regions, over 80% of woody plant species are dispersed by vertebrates, often through the consumption of fruits. Our understanding of what drives interactions between vertebrates and fruits is limited. Through a systematic literature search, we compiled a database of fruit and seed traits and vertebrate-fruit interactions for tree and vertebrate species occurring in the Guianas, with the aim of facilitating research into seed dispersal and seed predation of tree species in the Guianas. The database was compiled by extracting data from 264 published sources. It consists of 21,082 records, of which 19,039 records contain information about 19 different fruit and seed traits belonging to 1622 different tree species. The other 2043 records contain information on vertebrate-fruit interactions between 161 vertebrate species and 464 tree species. Our analyses showed a taxonomic bias, particularly in the interaction data, toward large-bodied vertebrates, with most interactions recorded for the bearded saki (Chiropotes chiropotes), followed by the lowland tapir (Tapirus terrestris). For plants we found an overrepresentation of the Sapotaceae and Moraceae families and an underrepresentation of the Rubiaceae, Myrtaceae, and Lauraceae families in the interactions. There are no copyright restrictions on the data set; please cite this publication when using these data.

Spatial aggregation patterns in four mistletoe species: ecological and environmental determinants.

Plant spatial distribution is an important topic in ecology as it determines species coexistence and biodiversity dynamics. Usually, plants show clustered distributions in nature. Mistletoes are a good example of aggregated distributions, as they form dense aggregations due to several factors (availability of competent hosts, seed dispersal vectors, microclimate conditions). We analysed four native mistletoe species with divergent life histories and host ranges: Desmaria mutabilis and Tristerix corymbosus from the temperate rainforests of southern Chile; and Tristerix aphyllus and Tristerix verticillatus from the northern semi-desert zone. While T. corymbosus and T. verticillatus have a wide host range, T. aphyllus and D. mutabilis are specialists that can parasitize only a few plant species. We hypothesized that specialized species would be more aggregated due to ecological and environmental restrictions. We used heterogeneous Poisson models to quantify spatial aggregation. Three of the four mistletoe species were spatially clustered at both environments, with aggregation being stronger in the temperate rainforest of southern Chile and particularly in the host-specialist species. Our results suggest that environmental constraints are more important than ecological constraints (host range) in shaping mistletoe spatial structure. Mistletoe aggregated spatial distribution depends primarily on the environment that they inhabit, which conditions host spatial availability, and arrangement.

Seasonality of reproduction in an ever-wet lowland tropical forest in Amazonian Ecuador.

Flowering and fruiting phenology have been infrequently studied in the ever-wet hyperdiverse lowland forests of northwestern equatorial Amazonía. These Neotropical forests are typically called aseasonal with reference to climate because they are ever-wet, and it is often assumed they are also aseasonal with respect to phenology. The physiological limits to plant reproduction imposed by water and light availability are difficult to disentangle in seasonal forests because these variables are often temporally correlated, and both are rarely studied together, challenging our understanding of their relative importance as drivers of reproduction. Here we report on the first long-term study (18 years) of flowering and fruiting phenology in a diverse equatorial forest, Yasuní in eastern Ecuador, and the first to include a full suite of on-site monthly climate data. Using twice monthly censuses of 200 traps and >1000 species, we determined whether reproduction at Yasuní is seasonal at the community and species levels and analyzed the relationships between environmental variables and phenology. We also tested the hypothesis that seasonality in phenology, if present, is driven primarily by irradiance. Both the community- and species-level measures demonstrated strong reproductive seasonality at Yasuní. Flowering peaked in September-November and fruiting peaked in March-April, with a strong annual signal for both phenophases. Irradiance and rainfall were also highly seasonal, even though no month on average experienced drought (a month with <100 mm rainfall). Flowering was positively correlated with current or near-current irradiance, supporting our hypothesis that the extra energy available during the period of peak irradiance drives the seasonality of flowering at Yasuní. As Yasuní is representative of lowland ever-wet equatorial forests of northwestern Amazonía, we expect that reproductive phenology will be strongly seasonal throughout this region.

La fenología de floración y fructificación ha sido poco estudiada en los bosques bajos, lluviosos e hiperdiversos de la Amazonía noroccidental. Estos bosques neotropicales son típicamente llamados no estacionales debido a su clima siempre lluvioso y se asume que son no estacionales con respecto a la fenología. Los límites fisiológicos a la reproducción de las plantas impuestos por la disponibilidad de agua y luz en estos bosques son difíciles de desentrañar debido a que estas variables están a menudo correlacionadas temporalmente y las dos se estudian usualmente por separado, lo que desafía nuestra comprensión de su importancia relativa como desencadenantes de la reproducción. Este es el primer estudio de largo plazo (18 años) de la fenología de floración y fructificación en un bosque hiperdiverso de la Amazonía noroccidental ecuatorial, Yasuní, ubicado al este de Ecuador, y el primero en incluir un completo set de datos climáticos mensuales. Usando censos quincenales de 200 trampas y > 1000 especies, examinamos si la reproducción en Yasuní es estacional a nivel de comunidad y de especies y analizamos las relaciones de las variables ambientales con la fenología. También nos interesaba probar si la estacionalidad en la fenología, en caso de que esté presente está causada por la irradiancia. Tanto a nivel de comunidad como de especies, los datos demuestran una fuerte estacionalidad reproductiva en Yasuní. La floración alcanzó un máximo en septiembre-noviembre y la fructificación alcanzó un máximo en marzo-abril, con una fuerte y consistente señal anual en las dos fenofases. A su vez, la irradiancia y la lluvia fueron también marcadamente estacionales, aunque ningún mes en promedio experimentó sequía (i.e. <100 mm de lluvia). La floración fue positivamente correlacionada con la irradiación, apoyando nuestra hipótesis de que la energía extra disponible durante los periodos de mayor irradiación causa la estacionalidad de la floración en Yasuní. Debido a que Yasuní representa a los bosques ecuatoriales lluviosos de tierras bajas de la Amazonía noroccidental, esperamos que la fenología reproductiva sea fuertemente estacional a lo largo de esta región.

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.

Germination of fruits eaten by the maned wolf Chrysocyon brachyurus (Illiger, 1815) (Carnivora, Canidae) / Germinação de frutos consumidos pelo lobo-guará Chrysocyon brachyurus (Illiger, 1815) (Carnivora, Canidae)

Abstract Zoochory is a fundamental process that can be the main mechanism for seed and plant dispersal for many species. Mammals of the Carnivora order are among the most important dispersing agents; however, little is known regarding the role of canids as seed dispersers. Although the maned wolf (Chrysocyon brachyurus) has a potentially important role in seed dispersal, given its relatively high consumption of fruits, few studies have investigated the germination rate of ingested seeds. Here, we used seeds removed from the feces of two captive specimens (maned wolf treatment) and those directly collected from unconsumed fruits (control) in germination essays to evaluate the germination rate and emergence velocity index (IVE). We used mature fruits from five species of trees in the Cerrado and Atlantic Forest in a 5 (species) × 2 (method of seed collection) factorial arrangement. The passage of seeds through the digestive tract of the maned wolf favored the germination of Genipa americana and Psidium guajava, delayed germination of Psidium cattleianum, and maintained the germination of Plinia cauliflora and Ficus obtusifolia. Our results revealed that germination occurred for all tested plant species consumed by the maned wolf; therefore, this canid species has high dispersal potential and can be an important ally in the restoration of the Cerrado and Atlantic Forest-Cerrado contact zone ecosystems.

Resumo A zoocoria é um processo fundamental para muitas espécies vegetais, podendo ser o principal mecanismo de dispersão de sementes e plantas. Os mamíferos da ordem Carnivora estão entre os agentes dispersores mais importantes, contudo, pouca atenção tem sido dada ao papel dos canídeos como dispersores de sementes. Embora o lobo-guará (Chrysocyon brachyurus) tenha um papel potencialmente importante na dispersão de sementes dado o seu consumo relativamente elevado de frutos, poucos estudos investigaram a taxa de germinação de sementes ingeridas. Aqui utilizamos sementes retiradas de fezes de dois exemplares em cativeiro (tratamento do lobo-guará) e diretamente retiradas de frutos não consumidos (controle) em ensaios de germinação para avaliar a taxa de germinação e o índice de velocidade de emergência (IVE). Utilizamos frutos maduros de cinco espécies de árvores que ocorrem no Cerrado e Mata Atlântica formando um arranjo fatorial de 5 (espécie) × 2 (forma de coleta de sementes). A passagem das sementes pelo trato digestivo do lobo-guará favoreceu a germinação de duas espécies, Genipa americana e Psidium guajava, atrasou a germinação de uma espécie, Psidium cattleianum e não afetou a germinação de duas espécies, Plinia cauliflora e Ficus obtusifolia. Com base nos nossos resultados, particularmente a descoberta de que todas as espécies vegetais testadas consumidas pelo lobo-guará germinaram, concluímos que esta espécie de canídeo tem um elevado potencial de dispersão, sendo um importante aliado na restauração de ecossistemas do Cerrado e da zona de contato entre Cerrado e Mata Atlântica.

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.

Efecto de la cobertura vegetal en escarabajos coprófagos (Coleoptera: Scarabaeinae) y sus funciones ecológicas en un bosque andino de Colombia / Effect of vegetation cover on dung beetles (Coleoptera: Scarabaeinae) and their ecological functions in an Andean forest of Colombia

Resumen Introducción: Los escarabajos coprófagos cumplen funciones importantes en los ecosistemas terrestres, pero las presiones antrópicas los afectan negativamente. Estos efectos están bien documentados en los bosques neotropicales de tierras bajas, pero se han estudiado poco en los bosques andinos. Objetivo: Evaluar cómo los atributos de los ensambles de escarabajos coprófagos y tres de sus funciones ecológicas difieren en tres tipos de cobertura vegetal, y determinar las relaciones entre atributos y funciones, y entre funciones. Métodos: Los escarabajos coprófagos se capturaron con trampas pitfall y se midieron las funciones ecológicas a través de un experimento de campo en la hacienda "El Ocaso" (Colombia), en tres tipos de cobertura vegetal: bosque secundario, bosque mixto y pastos para ganado (tres sitios independientes por cobertura). Los atributos del ensamble que se evaluaron fueron: abundancia, número de especies, biomasa y longitud corporal media ponderada; las funciones medidas fueron: remoción de estiércol, excavación del suelo y dispersión secundaria de semillas. Resultados: Se encontró que tanto los atributos del ensamble como las funciones ecológicas se vieron afectados negativamente en las coberturas vegetales más alteradas, particularmente en los pastos ganaderos. La mayoría de los atributos de ensamblaje se correlacionaron positivamente con las funciones; la excavación del suelo y la dispersión secundaria de semillas tuvieron una fuerte correlación positiva con la remoción de estiércol. Conclusiones: Los ensambles de escarabajos coprófagos juegan importantes funciones ecológicas y son sensibles a las alteraciones del ecosistema. Este estudio muestra cómo los escarabajos coprófagos y sus funciones se ven afectados negativamente cuando el bosque se transforma en pastizales para ganado en los ecosistemas forestales andinos poco estudiados y altamente fragmentados.

Abstract Introduction: Dung beetles perform important functions in terrestrial ecosystems, but anthropic pressures affect them negatively. These effects are well documented in neotropical lowland forests but have been studied little in Andean forests. Objective: To evaluate how the attributes of the dung beetle assemblages and three of their ecological functions differ in three types of vegetation cover, and to determine the relationships between attributes and functions, and among functions. Methods: Dung beetles were captured with pitfall traps, and ecological functions were measured through a field experiment in the farm "El Ocaso" (Colombia), in three types of vegetation cover: secondary forest, mixed forest and cattle pasture (three independent sites per cover). The assemblage attributes that were evaluated were abundance, number of species, biomass, and weighted mean body length; functions measured were dung removal, soil excavation, and secondary seed dispersal. Results: It was found that both the assemblage attributes and the ecological functions were negatively affected in the more disturbed vegetation covers, particularly in cattle pastures. Most of the assemblage attributes correlated positively with functions; soil excavation and secondary seed dispersal had a strong positive correlation with dung removal. Conclusions: Dung beetle assemblages play important ecological functions and they are sensitive to ecosystem disturbances. This study shows how dung beetles and their functions are affected negatively when forest is transformed to cattle pasture in the understudied and highly fragmented Andean forest ecosystems.

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.

Heterochrony and repurposing in the evolution of gymnosperm seed dispersal units.

BACKGROUND: Plant dispersal units, or diaspores, allow the colonization of new environments expanding geographic range and promoting gene flow. Two broad categories of diaspores found in seed plants are dry and fleshy, associated with abiotic and biotic dispersal agents, respectively. Anatomy and developmental genetics of fleshy angiosperm fruits is advanced in contrast to the knowledge gap for analogous fleshy structures in gymnosperm diaspores. Improved understanding of the structural basis of modified accessory organs that aid in seed dispersal will enable future work on the underlying genetics, contributing to hypotheses on the origin of angiosperm fruits. To generate a structural framework for the development and evolution of gymnosperm fleshy diaspores, we studied the anatomy and histochemistry of Ephedra (Gnetales) seed cone bracts, the modified leaves surrounding the reproductive organs. We took an ontogenetic approach, comparing and contrasting the anatomy and histology of fleshy and papery-winged seed cone bracts, and their respective pollen cone bracts and leaves in four species from the South American clade. RESULTS: Seed bract fleshiness in Ephedra derives from mucilage accumulated in chlorenchyma cells, also found in the reduced young leaves before they reach their mature, dry stage. Cellulosic fibers, an infrequent cell type in gymnosperms, were found in Ephedra, where they presumably function as a source of supplementary apoplastic water in fleshy seed cone bracts. Papery-winged bract development more closely resembles that of leaves, with chlorenchyma mucilage cells turning into tanniniferous cells early on, and hyaline margins further extending into "wings". CONCLUSIONS: We propose an evolutionary developmental model whereby fleshy and papery-winged bracts develop from an early-stage anatomy shared with leaves that differs at the pollination stage. The ancestral fleshy bract state may represent a novel differentiation program built upon young leaf anatomy, while the derived dry, papery-winged state is likely built upon an existing differentiation pattern found in mature vegetative leaves. This model for the evolution of cone bract morphology in South American Ephedra hence involves a novel differentiation program repurposed from leaves combined with changes in the timing of leaf differentiation, or heterochrony, that can further be tested in other gymnosperms with fleshy diaspores.

NeoBat Interactions: A data set of bat-plant interactions in the Neotropics.

Data papers and open databases have revolutionized contemporary science, as they provide the long-needed incentive to collaborate in large international teams and make natural history information widely available. Nevertheless, most data papers have focused on species occurrence or abundance, whereas interactions have received much less attention. To help fill this gap, we have compiled a georeferenced data set of interactions between 93 bat species of the family Phyllostomidae (Chiroptera) and 501 plant species of 68 families. Data came from 169 studies published between 1957 and 2007 covering the entire Neotropical Region, with most records from Brazil (34.5% of all study sites), Costa Rica (16%), and Mexico (14%). Our data set includes 2571 records of frugivory (75.1% of all records) and nectarivory (24.9%). The best represented bat genera are Artibeus (28% of all records), Carollia (24%), Sturnira (10.1%), and Glossophaga (8.8%). Carollia perspicillata (187), Artibeus lituratus (125), Artibeus jamaicensis (94), Glossophaga soricina (86), and Artibeus planirostris (74) were the bat species with the broadest diets recorded based on the number of plant species. Among the plants, the best represented families were Moraceae (17%), Piperaceae (15.4%), Urticaceae (9.2%), and Solanaceae (9%). Plants of the genera Cecropia (46), Ficus (42), Piper (40), Solanum (31), and Vismia (27) exhibited the largest number of interactions. These data are stored as arrays (records, sites, and studies) organized by logical keys and rich metadata, which helped to compile the information on different ecological and geographic scales, according to how they should be used. Our data set on bat-plant interactions is by far the most extensive, both in geographic and taxonomic terms, and includes abiotic information of study sites, as well as ecological information of plants and bats. It has already facilitated several studies and we hope it will stimulate novel analyses and syntheses, in addition to pointing out important gaps in knowledge. Data are provided under the Creative Commons Attribution 4.0 International License. Please cite this paper when the data are used in any kind of publication related to research, outreach, and teaching activities.

The disruption of a keystone interaction erodes pollination and seed dispersal networks.

Understanding the impacts of global change on ecological communities is a major challenge in modern ecology. The gain or loss of particular species and the disruption of key interactions are both consequences and drivers of global change that can lead to the disassembly of ecological networks. We examined whether the disruption of a hummingbird-mistletoe-marsupial mutualism by the invasion of non-native species can have cascading effects on both pollination and seed dispersal networks in the temperate forest of Patagonia, Argentina. We focused on network motifs, subnetworks composed of a small number of species exhibiting particular patterns of interaction, to examine the structure and diversity of mutualistic networks. We found that the hummingbird-mistletoe-marsupial mutualism plays a critical role in the community by increasing the complexity of pollination and seed dispersal networks through supporting a high diversity of interactions. Moreover, we found that the disruption of this tripartite mutualism by non-native ungulates resulted in diverse indirect effects that led to less complex pollination and seed dispersal networks. Our results demonstrate that the gains and losses of particular species and the alteration of key interactions can lead to cascading effects in the community through the disassembly of mutualistic networks.

Phylogenetic congruence between Neotropical primates and plants is driven by frugivory.

Seed dispersal benefits plants and frugivores, and potentially drives co-evolution, with consequences to diversification evidenced for, e.g., primates. Evidence for macro-coevolutionary patterns in multi-specific, plant-animal mutualisms is scarce, and the mechanisms driving them remain unexplored. We tested for phylogenetic congruences in primate-plant interactions and showed strong co-phylogenetic signals across Neotropical forests, suggesting that both primates and plants share evolutionary history. Phylogenetic congruence between Platyrrhini and Angiosperms was driven by the most generalist primates, modulated by their functional traits, interacting with a wide-range of Angiosperms. Consistently similar eco-evolutionary dynamics seem to be operating irrespective of local assemblages, since co-phylogenetic signal emerged independently across three Neotropical regions. Our analysis supports the idea that macroevolutionary, coevolved patterns among interacting mutualistic partners are driven by super-generalist taxa. Trait convergence among multiple partners within multi-specific assemblages appears as a mechanism favouring these likely coevolved outcomes.

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.

Bats and their vital ecosystem services: a global review.

Bats play crucial ecosystem services as seed dispersers, pollinators, controllers of insects, and nutrient recyclers. However, there has not been a thorough global review evaluating these roles in bats across all biogeographical regions of the world. We reviewed the literature published during the last two decades and identified 283 relevant studies: 78 dealt with the control of potential insect pests by bats, 80 related to the suppression of other arthropods, 60 on the dispersal of native or endemic seeds, 11 dealt with the dispersal of seeds of introduced plants, 29 on the pollination of native or endemic plants, 1 study on pollination of introduced plants, and 24 on the use of guano as fertilizer. Our literature search showed that queries combining the terms "seed dispersal," "insectivorous bats," "nectarivorous bats," "use of guano," and "ecosystem services" returned 577 studies, but half were experimental in nature. We found that the evaluation of ecosystem services by bats has been mostly conducted in the Neotropical and Palearctic regions. To detect differences across relevant studies, and to explain trends in the study of ecosystem services provided by bats, we performed generalized linear mixed models (GLMM) fitted with a Poisson distribution to analyze potential differences among sampling methods. We identified 409 bat species that provide ecosystem services, 752 insect species consumed by bats and 549 plant species either dispersed or pollinated by bats. Our review summarizes the importance of conserving bat populations and the ecological services they provide, which is especially important during the current pandemic.