Floral resource partitioning of coexisting bumble bees: Distinguishing species-, colony-, and individual-level effects.

Resource partitioning is considered a key factor in alleviating competitive interactions, enabling coexistence among consumer species. However, most studies have focused on resource partitioning between species, ignoring the potentially critical role of intraspecific variation in resource use. We investigated floral resource partitioning across species, colonies, and individuals in a species-rich bumblebee community in the diversification center of bumblebees. We used a total of 10,598 bumblebees belonging to 13 species across 5 years in the Hengduan Mountains of southwest China. First, we evaluated the influence of a comprehensive set of floral traits, including both those related to attractiveness (flower color and shape) and rewards (pollen, sugar ratio, nectar volume, sugar concentration, and amino acid content) on resource partitioning at the species level in bumblebee-plant networks. Then, we explored intraspecific resource partitioning on the colony and individual levels. Our results suggest that bumblebee species differ substantially in their use of the available floral resources, and that this mainly depends on flower attractiveness (floral color and shape). Interestingly, we also detected floral resource partitioning at the colony level within all commonest bumblebee species evaluated. In general, floral resource partitioning between bumblebee individuals decreased with species- and individual-level variation in body size (intertegular span). These results suggest that bumblebee species may coexist via the flexibility in their preferences for specific floral traits, which filters up to support the co-occurrence of high numbers of species and individuals in this global hotspot of species richness.

The interplay between scale, pollination niche and floral attractiveness on density-dependent plant-pollinator interactions.

Pollinators mediate interspecific and intraspecific plant-plant indirect interactions (competition vs. facilitation) via density-dependent processes, potentially shaping the dynamics of plant communities. However, it is still unclear which ecological drivers regulate density-dependent patterns, including scale, pollination niches (i.e., the main pollinator functional group) and floral attractiveness to pollinators. In this study, we conducted three-year field observations in Hengduan Mountains of southwest China. By gathering data for more than 100 animal-pollinated plant species, we quantified the effect (positive vs. negative) of conspecific and heterospecific flower density on pollination at two scales: plot-level (4 m2) and site-level (100-5000 m2). Then, we investigated how pollination niches and floral attractiveness to pollinators (estimated here as average per-flower visitation rates) modulated density-dependent pollination interactions. Pollinator visitation depended on conspecific and heterospecific flower density, with rare plants subjected to interspecific competition at the plot-level and interspecific facilitation at the site-level. Such interspecific competition at the plot-level was stronger for plants pollinated by diverse insects, while interspecific facilitation at the site-level was stronger for bee-pollinated plants. Moreover, we also found stronger positive conspecific density-dependence for plants with lower floral attractiveness at the site-level, meaning that they become more frequently visited when abundant. Our study indicates that the role of pollination in maintaining rare plants and plant diversity depends on the balance of density-dependent processes in species-rich communities. We show here that such balance is modulated by scale, pollination niches and floral attractiveness to pollinators, indicating the context-dependency of diversity maintenance mechanisms.

Integrating public engagement to intensify pollination services through ecological restoration.

Globally, human activities impose threats to nature and the provision of ecosystem services, such as pollination. In this context, ecological restoration provides opportunities to create managed landscapes that maximize biodiversity conservation and sustainable agriculture, e.g., via provision of pollination services. Managing pollination services and restoration opportunities requires the engagement of distinct stakeholders embedded in diverse social institutions. Nevertheless, frameworks toward sustainable agriculture often overlook how stakeholders interact and access power in social arenas. We present a perspective integrating pollination services, ecological restoration, and public engagement for biodiversity conservation and agricultural production. We highlight the importance of a comprehensive assessment of pollination services, restoration opportunities identification, and a public engagement strategy anchored in institutional analysis of the social arenas involved in restoration efforts. Our perspective can therefore guide the implementation of practices from local to country scales to enhance biodiversity conservation and sustainable agriculture.

Data standardization of plant-pollinator interactions.

BACKGROUND: Animal pollination is an important ecosystem function and service, ensuring both the integrity of natural systems and human well-being. Although many knowledge shortfalls remain, some high-quality data sets on biological interactions are now available. The development and adoption of standards for biodiversity data and metadata has promoted great advances in biological data sharing and aggregation, supporting large-scale studies and science-based public policies. However, these standards are currently not suitable to fully support interaction data sharing. RESULTS: Here we present a vocabulary of terms and a data model for sharing plant-pollinator interactions data based on the Darwin Core standard. The vocabulary introduces 48 new terms targeting several aspects of plant-pollinator interactions and can be used to capture information from different approaches and scales. Additionally, we provide solutions for data serialization using RDF, XML, and DwC-Archives and recommendations of existing controlled vocabularies for some of the terms. Our contribution supports open access to standardized data on plant-pollinator interactions. CONCLUSIONS: The adoption of the vocabulary would facilitate data sharing to support studies ranging from the spatial and temporal distribution of interactions to the taxonomic, phenological, functional, and phylogenetic aspects of plant-pollinator interactions. We expect to fill data and knowledge gaps, thus further enabling scientific research on the ecology and evolution of plant-pollinator communities, biodiversity conservation, ecosystem services, and the development of public policies. The proposed data model is flexible and can be adapted for sharing other types of interactions data by developing discipline-specific vocabularies of terms.

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.

Areas Requiring Restoration Efforts are a Complementary Opportunity to Support the Demand for Pollination Services in Brazil.

Crop pollination is one of Nature's Contributions to People (NCP) that reconciles biodiversity conservation and agricultural production. NCP benefits vary across space, including among distinct political-administrative levels within nations. Moreover, initiatives to restore ecosystems may enhance NCP provision, such as crop pollination delivered by native pollinators. We mapped crop pollination demand (PD), diversity of pollinator-dependent crops, and vegetation deficit (VD) (vis-a-vis Brazilian legal requirements) across all 5570 municipalities in Brazil. Pollinator-dependent crops represented ∼55% of the annual monetary value of agricultural production and ∼15% of the annual crop production. Municipalities with greater crop PD (i.e., higher degree of pollinator dependence of crop production) also had greater VD, associated with large properties and monocultures. In contrast, municipalities with a greater diversity of pollinator-dependent crops and predominantly small properties presented a smaller VD. Our results support that ecological restoration prompted by legal requirements offers great potential to promote crop productivity in larger properties. Moreover, conservation of vegetation remnants could support food security in small properties. We provided the first steps to identify spatial patterns linking biodiversity conservation and pollination service. Using Brazilian legal requirements as an example, we show that land-use management policies may be successfully used to ensure agricultural sustainability and crop production.

Flower Conspicuousness to Bees Across Pollination Systems: A Generalized Test of the Bee-Avoidance Hypothesis.

Flower signals of bee- and bird-pollinated plants have converged via pollinator-mediated evolution, driven by the visual system of their respective pollinators. For bird flowers, sensory exclusion of less effective bees is also important and such exclusion is also mediated by floral morphological filters. Likewise, other systems based on pollination by red-sensitive insects are also associated with red flowers displaying lower short-wavelength secondary peaks of reflectance, which decreases detectability to animals that are less sensitive to red, such as bees. These flowers often also present long tubes. Here, we tested a generalization of the bee-avoidance hypothesis in order to assess if it holds only for bird flowers or for other non-bee pollination systems as well. For this, we compared flower contrasts and spectral purity in bee visual systems as proxies for conspicuousness among four kinds of pollination systems: bee-visited flowers, insect-visited flowers (including bees and other insects), non-bee insect flowers (flowers visited by red-sensitive insects such as flies, butterflies and beetles, but not bees), and bird-visited flowers. We also assessed the association between conspicuousness to bees and flower depth, used as a proxy for morphological exclusion of bees. Overall, flower conspicuousness to bees differed only between insect (all three groups) and bird flowers, due to lower visual signals for the latter. This suggests that bee sensory exclusion via color signals is exclusive to bird flowers, while non-bee insect flowers might use other sensory channels to exclude bees, such as olfactory signals. Visual bee avoidance might be a mechanism exclusive to plants pollinated by specific guilds of red-sensitive insects not well represented in our sample. We also found a negative association between flower conspicuousness to bees and flower depth, suggesting an interplay of morphological and spectral traits in discouraging bee visits. Our results support the bee-avoidance hypothesis exclusively for bird flowers and an overall association between lower visual signals to bees and long tubes.

Pollination outcomes reveal negative density-dependence coupled with interspecific facilitation among plants.

Pollination is thought to be under positive density-dependence, destabilising plant coexistence by conferring fitness disadvantages to rare species. Such disadvantage is exacerbated by interspecific competition but can be mitigated by facilitation and intraspecific competition. However, pollinator scarcity should enhance intraspecific plant competition and impose disadvantage on common over rare species (negative density-dependence, NDD). We assessed pollination proxies (visitation rate, pollen receipt, pollen tubes) in a generalised plant community and related them to conspecific and heterospecific density, expecting NDD and interspecific facilitation due to the natural pollinator scarcity. Contrary to usual expectations, all proxies indicated strong intraspecific competition for common plants. Moreover interspecific facilitation prevailed and was stronger for rare than for common plants. Both NDD and interspecific facilitation were modulated by specialisation, floral display and pollinator group. The combination of intraspecific competition and interspecific facilitation fosters plant coexistence, suggesting that pollination can be a niche axis maintaining plant diversity.