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'.

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.

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.

Rasgos funcionales de frutos con importancia particular para los dispersores de semillas en el bosque seco tropical

Introducción: La frugivoría es un proceso ecológico determinante para la estructuración y regeneración de los bosques. En los trópicos, donde la diversidad de plantas y animales frugívoros es alta, las relaciones interespecíficas son complejas y requieren estudio. Objetivo: Identificar las especies de plantas ecológicamente importantes en dos redes de interacción, y el papel de los rasgos funcionales de los frutos en esas interacciones en un bosque seco. Métodos: Recolectamos 10 frutos por planta de 10 plantas de cada especie de interés en un bosque seco colombiano, calculamos el índice de importancia de las plantas a partir de la relevancia de aves y mamíferos frugívoros en la estructura de las redes. Esta relevancia se relaciona directamente con el potencial del animal como dispersor efectivo de semillas. Utilizamos modelos lineales generalizados para estimar el tamaño, color, estrato, y tipo de pulpa, en el índice. Resultados: Las plantas más importantes son especies de los géneros Miconia, Ficus, Cecropia, Bursera, Casearia y Trichilia, también identificadas como recursos importantes para los frugívoros de los trópicos en otros estudios. Las plantas con frutos carnosos, rojos y de menor tamaño son los mejores para dispersores de semillas. El índice de importancia de las plantas tiene alta variación; esto sugiere que un conjunto de especies frugívoras beneficiadas por cada especie de planta tiene una contribución diferenciada en procesos ecológicos derivados de la dispersión de semillas. Conclusiones: Programas de restauración para este tipo de bosque tropical seco debería incluir una variedad de plantas, incluyendo especies con frutos pequeños, rojos y carnosos.

Introduction: Frugivory is a pivotal ecological process for the structure and regeneration of forests. In the tropics, where the diversity of plants and frugivorous animals is high, interspecific relationships in the interaction networks are complex and need study. Objective: To identify ecologically important plant species in two interaction networks, and the role of functional fruit traits in those interactions in a dry forest. Methods: We collected 10 fruits per plant from 10 plants of each species of interest in a Colombian dry forest, we calculated the Plant Importance Index based on the bird and mammal frugivores relevance for network structure. This relevance is directly related to the animal's potential as effective seed dispersers. We used generalized linear models to estimate the effect of fruit size, color, stratum, and type of pulp, on the index. Results: The most important plants are species of the genera Miconia, Ficus, Cecropia, Bursera, Casearia and Trichilia, also identified as important resources for tropical frugivores in other studies. Plants with small, red, and fleshy fruits are the best for seed dispersers. The plant importance index has a high variation; this suggests that the set of frugivore species benefited by each plant species has a differential contribution to the ecological processes derived from seed dispersal. Conclusions: Restoration programs for this kind of tropical dry forest should include a variety of plants, including species with small, red, and fleshy fruits.

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.

Urbanization shapes phenotypic selection of fruit traits in a seed-dispersal mutualism.

Urbanization is currently one of the trademarks of the Anthropocene, accelerating evolutionary processes and reshaping ecological interactions over short time scales. Species interactions represent a fundamental pillar of diversity that is being altered globally by anthropogenic change. Urban environments, despite their potential impact, have seldom been studied in relation to how they shape natural selection of phenotypic traits in multispecies interactions. Using a seed-dispersal mutualism as a study system, we estimated the regime and magnitude of phenotypic selection exerted by frugivores on fruit and seed traits across three plant populations with different degrees of urbanization (urban, semiurban, and rural). Urbanization weakened phenotypic selection via an indirect positive impact on fruit production and fitness and, to a lesser extent, through a direct positive effect on species visitation rates. Our results show that urban ecosystems may affect multifarious selection of traits in the short term and highlight the role of humans in shaping eco-evolutionary dynamics of multispecies interactions.

Invasive Plant Species Driving the Biotic Homogenization of Plant-Frugivore Interactions in the Atlantic Forest Biodiversity Hotspot.

Although biological invasions are a common and intensively studied phenomenon, most studies often ignore the biotic interactions that invasive species play in the environment. Here, we evaluated how and why invasive plant species are interconnected within the overall frugivory network of the Brazilian Atlantic Forest, an important global biodiversity hotspot. To do this, we used the recently published Atlantic Frugivory Dataset to build a meta-network (i.e., a general network made of several local networks) that included interactions between 703 native and invasive plant species and 331 frugivore species. Using tools derived from complex network theory and a bootstrap simulation approach, we found that the general structure of the Atlantic Forest frugivory network (i.e., nestedness and modularity) is robust against the entry of invasive plant species. However, we observed that invasive plant species are highly integrated within the frugivory networks, since both native and invasive plant species play similar structural roles (i.e., plant status is not strong enough to explain the interactive roles of plant species). Moreover, we found that plants with smaller fruits and with greater lipid content play a greater interactive role, regardless of their native or invasive status. Our findings highlight the biotic homogenization involving plant-frugivore interactions in the Atlantic Forest and that the impacts and consequences of invasive plant species on native fauna can be anticipated based on the characteristics of their fruits.

Ecological Impacts of Exotic Species on Native Seed Dispersal Systems: A Systematic Review.

Exotic species are one of the main threats to biodiversity, leading to alterations in the structure and functioning of natural ecosystems. However, they can sometimes also provide ecological services, such as seed dispersal. Therefore, we assessed the ecological impacts of exotic species on native dispersal systems and the mechanisms underlying the disruption of mutualistic plant-disperser interactions. Exotic species negatively affect dispersal mutualisms by (i) altering dispersal behavior and visitation rates of native dispersers, (ii) predating native dispersers, (iii) transmitting forest pathogens, and (iv) predating seeds. Conversely, positive impacts include the dispersal of native plants, forest regeneration, and native habitat restoration via (i) increasing the visitation rates of frugivorous birds, (ii) facilitating the colonization and establishment of native forest trees, (iii) enhancing forest species seedling survival, and (iv) facilitating seed rain and seedling recruitment of early and late successional native plants. The reviewed studies provide similar results in some cases and opposite results in others, even within the same taxa. In almost all cases, exotic species cause negative impacts, although sometimes they are necessary to ensure native species' persistence. Therefore, exotic species management requires a comprehensive understanding of their ecological roles, since the resulting effects rely on the complexity of native-exotic species interactions.

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.

First record of the largest copro-necrophagous beetle in South America (Coprophanaeus lancifer) feeding on fruits / Primer registro del escarabajo coprófago más grande de América del Sur (Coprophanaeus lancifer) alimentándose de frutos

Coprophanaeus lancifer is a copro-necrophagous beetle endemic to the Amazon region. Although beetles belonging to the subfamily Scarabaeinae primarily feed on dung, some have a greater diet plasticity that includes carrion, fungi, rotten fruits and invertebrates. The diet of the scavenger beetle C. lancifer mainly consists of vertebrate carcasses, although it is also attracted to mammal faeces. Here, we describe the first record of this species feeding on fruits of the genus Nectandra.(AU)

Coprophanaeus lancifer es un escarabajo copro-necrófago endémico de la región amazónica. Aunque los escarabajos pertenecientes a la subfamilia Scarabaeinae se alimentan principalmente de excrementos, algunos tienen una mayor plasticidad dietética que incluye carroña, hongos, frutas podridas y invertebrados. La dieta del escarabajo carroñero C. lancifer consiste principalmente en cadáveres de vertebrados, aunque, también se siente atraído por heces de mamíferos. Aquí, describimos el primer registro de esta especie alimentándose de frutos del género Nectandra.(AU)

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.

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.

Saurochory in crocodiles does not favor seed dispersai and viability / Saurocoría en cocodrilos no favorece la dispersión y la viabilidad de semillas

RESUMEN La dispersión de semillas por reptiles (saurocoría) ha recibido atención recientemente y se ha reportado el consumo de frutos y semillas en cocodrilianos, actuando como potenciales dispersores de semillas. Evaluamos si la saurocoría en Crocodylus actus y C. moreletii afecta la viabilidad de tres especies de plantas Delonixregia, Inga sp. y Citrullus lanatus. Se Utilizaron tres individuos juveniles de cada especie de cocodrilo y se alimentaron con 22 semillas por especie de planta, para un total de 66 semillas por recinto (132 para ambos). Las semillas se mezclaron con la dieta habitual cada semana, las semillas no consumidas y las excretadas se recolectaron y sembraron en suelo tratado con composta para evaluar la tasa de germinación relativa. Un total de 99 semillas fueron consumidas pero solo se recuperaron de las heces 14 semillas de C. lanatus, y germinando solo una de ellas (7, 14 %) con respecto al 50 % en el grupo control. Los resultados indican que la saurocoría de C. acutus y C. moreletii tiene un efecto negativo sobre la viabilidad de las semillas de las especies vegetales estudiadas, concordando con otros estudios realizados en diferentes especies.

ABSTRACT Seed dispersal by reptiles (saurochory) has recently received attention, and the consumption of fruits and seeds has been reported in crocodilians despite being mainly carnivores, acting as potential seed dispersers. We evaluate whether saurochory by Crocodylus acutus and C. moreletii affect the seed viability of three species of plants (Delonix regia, Inga sp., and Citrullus lanatus). We performed feeding trials, using three juvenile individuals of each species of crocodile, and fed them 22 seeds per plant species for a total of 66 seeds per enclosure (132 for both species). Seeds were combined with the usual diet each week. The unconsumed and excreted seeds were collected and planted in soil treated with compost to evaluate the relative germination rate. A total of 99 seeds were consumed, of which only 14 seeds of C. lanatus were recovered from the faeces, and only one of those germinated (7.14 %) with respect to 50 % in the control group. The results indicate that saurochory by C. acutus and C. moreletii has a negative effect on seed viability and germination of the plant species studied, as found in other studies using different species.

Non-visual senses in fruit selection by the mantled howler monkey (Alouatta palliata).

There is extensive knowledge about the visual system and the implications of the evolution of trichromatic color vision in howler monkeys (genus Alouatta) related to food selection; however, information about the other sensory systems is limited. In this study we assessed the use of touch, sniffing, and taste in fruit evaluation by 20 adult mantled howler monkeys (Alouatta palliata) on Agaltepec Island, Mexico. During 9 months of observation, we recorded the frequency that each monkey used touch, sniffing, and taste in evaluating cryptic fruits (that remain green during their ripening process) and conspicuous fruits (with red, yellow, or orange colorations when they are ripe). Sucrose content and hardness measurements were made to establish the degree of ripeness of the fruits. We found that mantled howler monkeys used long behavioral sequences during conspicuous fruit investigations. Sniffing was used infrequently, but significantly more often in the evaluation of conspicuous-ripe and unripe fruits compared to cryptic-ripe and unripe fruits. During the evaluation of cryptic-ripe fruits, mantled howler monkeys increased the use of touch compared to evaluating cryptic-unripe fruits. We did not find significant differences in the use of taste in the evaluation of cryptic and conspicuous fruits (both ripe and unripe). Our results suggest that the non-visual senses play an essential role in fruit selection by howler monkeys, with differences in the behavioral strategy according to the fruit's conspicuity. The multimodal signals of ripe and unripe fruits allow the howler monkeys to assess their palatability before being consumed.

Florivory by the occupants of phytotelmata in flower parts can decrease host plant fecundity.

Some types of plant accumulate liquid in their inflorescences creating phytotelmata. These environments protect the flowers against florivory, although they may be colonized by aquatic or semi-aquatic florivorous insect larvae, whose effects on the fitness of the plants remain unclear. We tested the hypothesis of floral antagonism by the occupants of phytotelmata, which predicts that florivory by the occupants of the phytotelmata represents a cost to the female fitness of the plant, reducing its fecundity. We manipulated experimentally the infestation by 3 florivores larvae species occupants of phytotelmata in inflorescences of Heliconia spathocircinata (Heliconiaceae) to test for negative direct trophic effects on the fecundity of the flowering and fruiting bracts. We found that the foraging of the hoverfly (Syrphidae) and moth (Lepidoptera) larvae in the inflorescences contributed to a decline in the fecundity of the plant. While the lepidopteran impacted fecundity when foraging in both flowering and fruiting bracts, the syrphid only affected the fruiting bracts, which indicates that the nectar and floral tissue are the principal resource exploited by the hoverfly. By contrast, soldier fly (Stratiomyidae) had a neutral effect on fecundity, while foraging in flowering or fruiting bracts. These findings corroborate our hypothesis, that herbivory by the larval occupants represents cost to the host plant having phytotelmata. The negative influence of this foraging on plant fecundity will nevertheless depend on the consequences of the exploitation of resources, which vary considerably in ephemeral habitats such as the phytotalmanta of flower parts.

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.

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.

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.

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.