The structure of tropical bat-plant interaction networks during an extreme El Niño-Southern Oscillation event.

Interaction network structure reflects the ecological mechanisms acting within biological communities, which are affected by environmental conditions. In tropical forests, higher precipitation usually increases fruit production, which may lead frugivores to increase specialization, resulting in more modular and less nested animal-plant networks. In these ecosystems, El Niño is a major driver of precipitation, but we still lack knowledge of how species interactions change under this influence. To understand bat-plant network structure during an extreme El Niño-Southern Oscillation event, we determined the links between plantivorous bat species and the plants they consume by DNA barcoding seeds and pulp in bat faeces. These interactions were recorded in the dry forest and rainforest of Costa Rica, during the dry and the wet seasons of an extreme El Niño year. From these we constructed seasonal and whole-year bat-plant networks and analysed their structures and dissimilarities. In general, networks had low nestedness, had high modularity, and were dominated by one large compartment which included most species and interactions. Contrary to our expectations, networks were less nested and more modular in drier conditions, both in the comparison between forest types and between seasons. We suggest that increased competition, when resources are scarce during drier seasons and habitats, lead to higher resource partitioning among bats and thus higher modularity. Moreover, we have found similar network structures between dry and rainforests during El Niño and non-El Niño years. Finally, most interaction dissimilarity among networks occurred due to interaction rewiring among species, potentially driven by seasonal changes in resource availability.

Consumers' active choice behaviour promotes coevolutionary units in antagonistic networks.

Individual behaviour and local context can influence the evolution of ecological interactions and how they structure into networks. In trophic interactions, consumers can increase their fitness by actively choosing resources that they are more likely to explore successfully. Mathematical modelling is often employed in theoretical studies to understand the coevolutionary dynamics between consumers and resources. However, they often disregard the individual consumer behaviour since the complexity of these systems usually requires simplifying assumptions about interaction details. Using an individual-based model, we model a community of several species that interact antagonistically. Each individual has a trait (attack or defence) that is explicitly modelled and the probability of the interaction to occur successfully increases with increased trait-matching. In addition, consumers can actively choose resources that guarantee greater fitness. We show that active consumer choice can generate coevolutionary units over time. It means that the traits of both consumers and resources converge into multiple groups with similar traits and the species interactions stay restricted to these groups over time. We also observed that network structure is more dependent on the parameter that delimits active consumer choice than on the intensity of selective pressure. Thus, our results support the idea that consumer active choice behaviour plays an important role in the ecological and evolutionary processes that structure interacting communities.

Spatio-temporal effects of climate change on the geographical distribution and flowering phenology of hummingbird-pollinated plants.

BACKGROUNDS AND AIMS: Tropical plant species are already suffering the effects of climate change and projections warn of even greater changes in the following decades. Of particular concern are alterations in flowering phenology, given that it is considered a fitness trait, part of plant species ecological niche, with potential cascade effects in plant-pollinator interactions. The aim of the study was to assess the potential impacts of climate change on the geographical distribution and flowering phenology of hummingbird-pollinated plants. METHODS: We implemented ecological niche modelling (ENM) to investigate the potential impacts of different climate change scenarios on the geographical distribution and flowering phenology of 62 hummingbird-pollinated plant species in the Brazilian Atlantic Forest. KEY RESULTS: Distribution models indicate future changes in the climatic suitability of their current habitats, suggesting a tendency towards discontinuity, reduction and spatial displacement. Flowering models indicate that climate can influence species phenology in different ways: some species may experience increased flowering suitability whereas others may suffer decreased suitability. CONCLUSIONS: Our results suggest that hummingbird-pollinated species are prone to changes in their geographical distribution and flowering under different climate scenarios. Such variation may impact the community structure of ecological networks and reproductive success of tropical plants in the near future.

Local drivers of the structure of a tropical bird-seed dispersal network.

One of the major challenges in ecology is to understand the relative importance of neutral- and niche-based processes structuring species interactions within communities. The concept of neutral-based processes posits that network structure is a result of interactions between species based on their abundance. On the other hand, niche-based processes presume that network structure is shaped by constraints to interactions. Here, we evaluated the relative importance of neutral-based process, represented by species' abundance (A) and fruit production (F) models, and niche-based process, represented by spatial overlap (S), temporal overlap (T) and morphological barrier (M) models, in shaping the structure of a bird-seed dispersal network from the Brazilian Atlantic Forest. We evaluated the ability of each model, singly or in combination, to predict the general structure [represented by connectance, nestedness (NODF), weight nestedness (WNODF), interaction evenness and complementary specialization] and microstructure of the network (i.e., the frequency of pairwise interactions). Only nestedness (both NODF and WNODF) was predicted by at least one model. NODF and WNODF were predicted by a neutral-based process (A), by a combination of niche-based processes (ST and STM) and by both neutral- and niche-based processes (AM). NODF was also predicted by F and FM model. Regarding microstructure, temporal overlap (T) was the most parsimonious model able to predict it. Our findings reveal that a combination of neutral- and niche-based processes is a good predictor of the general structure (NODF and WNODF) of the bird-seed dispersal network and a niche-based process is the best predictor of the network's microstructure.

Correction to: Local drivers of the structure of a tropical bird­seed dispersal network.

Unfortunately, the detailed description of the ESM material went wrong in the published version of the dataset.

Estimating seed and pollen dispersal kernels from genetic data demonstrates a high pollen dispersal capacity for an endangered palm species.

PREMISE OF THE STUDY: Seed and pollen dispersal are key processes shaping plant population dynamics and maintaining genetic diversity. The essence of these processes is the movement of propagules from a parental tree to the site of propagule establishment. The estimation of plant dispersal kernels has remained challenging due to the difficulty of making direct observations. We estimated the dispersal capacity of the endangered palm Euterpe edulis, whose seeds are dispersed by vertebrates and pollen by insects. METHODS: We used a hierarchical Bayesian model with genetic data from reproductive plants, juveniles, and embryos to estimate dispersal kernels. Our analyses account for genotyping error and uncertainty in parental assignment. KEY RESULTS: We found that seeds were dispersed at most a few hundred meters, but pollen was dispersed up to several kilometers. We hypothesize that this long-distance pollen dispersal is generated mainly by euglossine bees, whereas the main dispersal vectors for short-distance seed dispersal are thrushes. The long-distance dispersal of pollen suggests a high level of gene flow that should maintain genetic diversity of E. edulis. Despite the relation between long-distance dispersal and genetic diversity, we observed low genetic diversity and inbreeding within the local population, which are probably due to restricted gene flow due to the low density of this population and its aggregated spatial distribution. CONCLUSIONS: We conclude that if conservation actions are able to restore the population density of E. edulis, the recovery of its genetic diversity will be facilitated because of its high dispersal capacity, especially with regard to pollen.

High proportion of smaller ranged hummingbird species coincides with ecological specialization across the Americas.

Ecological communities that experience stable climate conditions have been speculated to preserve more specialized interspecific associations and have higher proportions of smaller ranged species (SRS). Thus, areas with disproportionally large numbers of SRS are expected to coincide geographically with a high degree of community-level ecological specialization, but this suggestion remains poorly supported with empirical evidence. Here, we analysed data for hummingbird resource specialization, range size, contemporary climate, and Late Quaternary climate stability for 46 hummingbird-plant mutualistic networks distributed across the Americas, representing 130 hummingbird species (ca 40% of all hummingbird species). We demonstrate a positive relationship between the proportion of SRS of hummingbirds and community-level specialization, i.e. the division of the floral niche among coexisting hummingbird species. This relationship remained strong even when accounting for climate, furthermore, the effect of SRS on specialization was far stronger than the effect of specialization on SRS, suggesting that climate largely influences specialization through species' range-size dynamics. Irrespective of the exact mechanism involved, our results indicate that communities consisting of higher proportions of SRS may be vulnerable to disturbance not only because of their small geographical ranges, but also because of their high degree of specialization.

ATLANTIC POLLINATION: a data set of flowers and interaction with nectar-feeding vertebrates from the Atlantic Forest.

Flowering plant species and their nectar-feeding vertebrates exemplify some of the most remarkable biotic interactions in the Neotropics. In the Brazilian Atlantic Forest, several species of birds (especially hummingbirds), bats, and non-flying mammals, as well as one lizard feed on nectar, often act as pollinators and contribute to seed output of flowering plants. We present a dataset containing information on flowering plants visited by nectar-feeding vertebrates and sampled at 166 localities in the Brazilian Atlantic Forest. This dataset provides information on 1902 unique interactions among 515 species of flowering plants and 129 species of potential vertebrate pollinators and the patterns of species diversity across latitudes. All plant-vertebrate interactions compiled were recorded through direct observations of visits, and no inferences of pollinators based on floral syndromes were included. We also provide information on the most common plant traits used to understand the interactions between flowers and nectar-feeding vertebrates: plant growth form, corolla length, rate of nectar production per hour in bagged flowers, nectar concentration, flower color and shape, time of anthesis, presence or absence of perceptible fragrance by human, and flowering phenology as well as the plant's threat status by International Union for Conservation of Nature (IUCN) classification. For the vertebrates, status of threat by IUCN classification, body mass, bill or rostrum size are provided. Information on the frequency of visits and pollen deposition on the vertebrate's body is provided from the original source when available. The highest number of unique interactions is recorded for birds (1771) followed by bats (110). For plants, Bromeliaceae contains the highest number of unique interactions (606), followed by Fabaceae (242) and Gesneriaceae (104). It is evident that there was geographical bias of the studies throughout the southeast of the Brazilian Atlantic Forest and that most effort was directed to flower-hummingbird interactions. However, it reflects a worldwide tendency of more plants interacting with birds compared with other vertebrate species. The lack of similar protocols among studies to collect basic data limits the comparisons among areas and generalizations. Nevertheless, this dataset represents a notable effort to organize and highlight the importance of vertebrate pollinators in this hotspot of biodiversity on Earth and represents the data currently available. No copyright or proprietary restrictions are associated with the use of this data set. Please cite this data paper when the data are used in publications or scientific events.

Comparative anatomy and morphology of nectar-producing Melastomataceae.

BACKGROUND AND AIMS: Most neotropical Melastomataceae have bee-pollinated flowers with poricidal anthers. However, nectar rewards are known to be produced in about 80 species in eight genera from four different tribes. These nectar-producing species are pollinated by both vertebrates and invertebrates. METHODS: The floral morphology and anatomy of 14 species was studied in six genera of nectar-producing Melastomataceae (Blakea, Brachyotum, Charianthus, Huilaea, Meriania and Miconia). Anatomical methods included scanning electron microscopy, and serial sections of paraffin-embedded flowers. KEY RESULTS: All vertebrate-pollinated melastome flowers have petals that do not open completely at anthesis, thus forming a pseudo-tubular corolla, while closely related species that are bee pollinated have rotate or reflexed corollas. In most species, nectar secretion is related to stomatal or epidermal nectaries and not filament slits as previously reported. Moreover, the nectar is probably supplied by large vascular bundles near the release area. Blakea and Huilaea have nectary stomata located upon the dorsal anther connective appendages. Brachyotum also has nectary stomata on the anther connectives, but these are distributed lengthwise along most of the connective. Meriania may release nectar through the anther connective, but has additional nectary stomata on the inner walls of the hypanthium. Miconia has nectary stomata on the ovary apex. Charianthus nectaries were not found, but there is circumstantial evidence that nectar release occurs through the epidermis at the apex of the ovary and the lower portions of the inner wall of the hypanthium. CONCLUSIONS: Nectar release in Melastomataceae is apparently related to nectary stomata and not filament slits. The presence of nectary stomata on stamens and on ovary apices in different lineages suggests that the acquisition of nectaries is a derived condition. Nectary location also supports a derived condition, because location is strongly consistent within each genus, but differs between genera.

Survey dataset on mutualistic interactions among Euterpe edulis Mart. (Arecaceae) and floral and frugivorous visitors considering influence of neighborhood plant density and availability of resources.

The data are supporting the research article "Effects of neighborhood on pollination and seed dispersal of a threatened palm" (Santos et al., 2018). We recorded through focal observation mutualistic interactions with floral and frugivorous visitors and 11 individuals of the threatened Euterpe edulis palm in Brazil. We thus provide two datasets, one about interactions with floral visitors (Pollination data.xlsx) and other about interactions with frugivorous visitors (Seed dispersal data.xlsx). Both datasets are structured in eight spreadsheets: Two about observed interactions among Euterpe edulis palm and floral and frugivorous visitors; two response variables (frequency and assembly composition); four predictor variables (conspecific aggregation, basal area, number of rachillae/fruits, flower in anthesis/ripe fruits). We also report here sampling completeness measured from rarefaction of unique interactions versus interaction events recorded.

Pollinator guild organization and its consequences for reproduction in three synchronopatric species of Tibouchina (Melastomataceae)

Pollinator guild organization and its consequences for reproduction in three synchronopatric species of Tibouchina (Melastomataceae). In co-flowering plant species, pollinator sharing can result in interspecific pollen transfer and fecundity reduction. Competition will be relaxed whenever there is a large amount of initial pollen supply or if each plant species occupies different habitat patches. Reproduction in Tibouchina cerastifolia (Naudin) Cogn., T. clinopodifolia (DC.) Cogn. and T. gracilis (Bonpl.) Cogn. was studied in an area of Atlantic rainforest to examine whether synchronopatry induces time partitioning among pollinator species. Eleven bee species comprised the pollinator guild. Among pollinators, there were overlaps in bee species composition and in flower visitation time. Direct competition for pollen in Tibouchina Aubl. at the study site seems to lead to different activity periods among the bee species, in which Bombus pauloensis Friese,1913 was most active earlier, while the other species were active later in the day. Bombus pauloensis, the largest bee species recorded on Tibouchina flowers, was the most important and efficient pollinator. This species harvested pollen before the other species and had the shortest handling time. The plants reproduced sexually by selfing or outcrossing, and hybridization was not avoided by incompatibility reactions at the style. The avoidance of direct competition for pollen and no pollinator partitioning among the synchronopatric species of Tibouchina may reflect a facilitative interaction among these pioneer plants.

Organização da guilda de polinizadores e sua consequência para reprodução em três espécies sincropátricas de Tibouchina (Melastomataceae). Em espécies de plantas que co-florescem, a partilha de polinizadores pode resultar em transferência interespecífica de pólen e redução da fecundidade. A competição pode ser relaxada quando existe uma grande quantidade de suprimento de pólen ou se cada planta ocupa manchas distintas do hábitat. A reprodução de Tibouchina cerastifolia (Naudin) Cogn., T. clinopodifolia (DC.) Cogn. e T. gracilis (Bonpl.) Cogn. foi estudada em Floresta Atlântica para verificar se a sincronopatria levava à partilha temporal das espécies de polinizadores. Onze espécies de abelhas compuseram a guilda de polinizadores. Entre eles, houve sobreposição na composição de espécies de polinizadores e no período de visitação floral. A competição direta por pólen em Tibouchina Aubl. na área de estudo parece levar a distintos períodos de atividade entre as abelhas, onde Bombus pauloensis Friese,1913 foi mais ativa mais cedo enquanto que as outras espécies foram ativas mais tarde. Bombus pauloensis, a maior espécie de abelha registrada em nas flores de Tibouchina, foi o polinizador mais importante e eficiente. Esta espécie coletava pólen antes das outras abelhas e apresentou um menor tempo de manipulação das anteras. As plantas se reproduziram sexuadamente, por autogamia e xenogamia e a hibridação não foi inibida por reações de incompatibilidade no estilete. A ausência de competição direta por pólen e de partilha de polinizadores pode refletir uma interação de facilitação entre estas três espécies pioneiras e sincronopátricas de Tibouchina.