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.

Behavioural and morphological traits influence sex-specific floral resource use by hummingbirds.

Research on resource partitioning in plant-pollinator mutualistic systems is mainly concentrated at the levels of species and communities, whereas differences between males and females are typically ignored. Nevertheless, pollinators often show large sexual differences in behaviour and morphology, which may lead to sex-specific patterns of resource use with the potential to differentially affect plant reproduction and diversification. We investigated variation in behavioural and morphological traits between sexes of hummingbird species as potential mechanisms underlying sex-specific flower resource use in ecological communities. To do so, we compiled a dataset of plant-hummingbird interactions based on pollen loads for 31 hummingbird species from 13 localities across the Americas, complemented by data on territorial behaviour (territorial or non-territorial) and morphological traits (bill length, bill curvature, wing length and body mass). We assessed the extent of intersexual differences in niche breadth and niche overlap in floral resource use across hummingbird species. Then, we tested whether floral niche breadth and overlap between sexes are associated with sexual dimorphism in behavioural or morphological traits of hummingbird species while accounting for evolutionary relatedness among the species. We found striking differences in patterns of floral resource use between sex. Females had a broader floral niche breadth and were more dissimilar in the plant species visited with respect to males of the same species, resulting in a high level of resource partitioning between sexes. We found that both territoriality and morphological traits were related to sex-specific resource use by hummingbird species. Notably, niche overlap between sexes was greater for territorial than non-territorial species, and moreover, niche overlap was negatively associated with sexual dimorphism in bill curvature across hummingbird species. These results reveal the importance of behavioural and morphological traits of hummingbird species in sex-specific resource use and that resource partitioning by sex is likely to be an important mechanism to reduce intersexual competition in hummingbirds. These findings highlight the need for better understanding the putative role of intersexual variation in shaping patterns of interactions and plant reproduction in ecological communities.

La investigación sobre la partición de recursos en los sistemas mutualistas planta-polinizador se concentra principalmente en los niveles de especies y comunidades, mientras que las diferencias entre machos y hembras suelen ser ignoradas. Sin embargo, los polinizadores suelen mostrar grandes diferencias sexuales en su comportamiento y morfología, lo que puede dar lugar a patrones específicos de uso de recursos para cada sexo con el potencial de afectar de forma diferencial la reproducción y la diversificación de las plantas. Se estudió la variación en los rasgos de comportamiento y morfológicos entre sexos de las especies de colibríes como posibles mecanismos que explican el uso de recursos florales específicos para cada sexo en las comunidades ecológicas. Para ello, se recopiló un conjunto de datos de interacciones planta-colibrí con base en las cargas de polen de 31 especies de colibríes de 13 localidades en las Américas, además de datos sobre su comportamiento territorial (territorial o no territorial) y rasgos morfológicos (longitud y curvatura del pico, longitud del ala y masa corporal). Se evaluaron las diferencias intersexuales en la amplitud y el solapamiento del nicho en el uso de los recursos florales para las distintas especies de colibríes. Posteriormente, se comprobó si la amplitud del nicho floral y el solapamiento entre sexos están asociados con el dimorfismo sexual en los rasgos de comportamiento o morfológicos de las especies de colibríes, teniendo en cuenta el parentesco evolutivo entre las especies. Se encontraron diferencias notables en los patrones de uso de los recursos florales entre sexos. Las hembras presentaron una mayor amplitud de nicho floral y fueron más disímiles en las especies de plantas visitadas con respecto a los machos de la misma especie, lo que resultó en un alto nivel de partición de recursos entre los sexos. Se encontró que tanto la territorialidad como los rasgos morfológicos están relacionados con el uso de recursos específicos por sexo en las especies de colibríes. En particular, el solapamiento de nicho entre sexos fue mayor para las especies territoriales que para las no territoriales y, además, el solapamiento de nicho se asoció negativamente con el dimorfismo sexual en la curvatura del pico en las especies de colibríes. Estos resultados revelan la importancia de los rasgos conductuales y morfológicos de las especies de colibríes en el uso de recursos según el sexo y que la partición de recursos entre sexos es probablemente un mecanismo importante para reducir la competencia intersexual en los colibríes. Estos resultados ponen de manifiesto la necesidad de comprender mejor el rol que tiene la variación intersexual en los patrones de interacción y en la reproducción de las plantas en las comunidades ecológicas.

Extinction, coextinction and colonization dynamics in plant-hummingbird networks under climate change.

Climate-driven range shifts may cause local extinctions, while the accompanying loss of biotic interactions may trigger secondary coextinctions. At the same time, climate change may facilitate colonizations from regional source pools, balancing out local species loss. At present, how these extinction-coextinction-colonization dynamics affect biological communities under climate change is poorly understood. Using 84 communities of interacting plants and hummingbirds, we simulated patterns in climate-driven extinctions, coextinctions and colonizations under future climate change scenarios. Our simulations showed clear geographic discrepancies in the communities' vulnerability to climate change. Andean communities were the least affected by future climate change, as they experienced few climate-driven extinctions and coextinctions while having the highest colonization potential. In North America and lowland South America, communities had many climate-driven extinctions and few colonization events. Meanwhile, the pattern of coextinction was highly dependent on the configuration of networks formed by interacting hummingbirds and plants. Notably, North American communities experienced proportionally fewer coextinctions than other regions because climate-driven extinctions here primarily affected species with peripheral network roles. Moreover, coextinctions generally decreased in communities where species have few overlapping interactions, that is, communities with more complementary specialized and modular networks. Together, these results highlight that we should not expect colonizations to adequately balance out local extinctions in the most vulnerable ecoregions.

Hummingbird contribution to plant reproduction in the rupestrian grasslands is not defined by pollination syndrome.

Floral traits mediate the roles of distinct animals as effective pollinators along a generalization/specialization continuum. Many plant species are visited by different pollinator functional groups and the specific contribution of each group is expected to reflect the set of floral characteristics defined by pollination syndromes. Although considered a highly specialized nectarivorous group, hummingbirds frequently visit flowers lacking apparent specialization to bird pollination. How they contribute to the reproduction of these plants, however, has not been evaluated through field experiments considering multiple non-related plant species simultaneously. Here, we investigated hummingbirds' contributions to the pollination of ten plant species comprising a gradient of adaptation to bird pollination in the Brazilian rupestrian grasslands. We excluded hummingbirds from flowers and evaluated their relative contribution in comparison to insects (mainly bees) on conspecific/heterospecific pollen deposition and fruit set. Floral traits that are typically associated with bird pollination were associated with increased pollen deposition, but not with fruit set in the presence of hummingbirds. With hummingbirds, conspecific and heterospecific pollen deposition increased in most species, while fruit set increased in four plant species with varying degrees of fit to ornithophily. Our results show that assessing the relative contribution of specific pollinator groups may depend on when this contribution is measured, i.e. pollen deposition or fruit set. Considering fruit set, our results indicate that hummingbirds contributed to plant reproduction independently of the fit to bird pollination syndrome. This emphasizes their importance as under-appreciated generalized pollinators in some communities.

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.

Plant-centred sampling estimates higher beta diversity of interactions than pollinator-based sampling across habitats.

When describing plant-animal interaction networks, sampling can be performed using plant- or animal-centred approaches. Despite known effects of sampling on network structure, how samplings affect the estimates of interaction ß-diversity across networks is still unresolved. We investigated how the sampling method affects the assessment of ß-diversity of interactions, turnover and rewiring. We contrasted plant- and animal-centred sampling methods applied to pollination networks across habitats in a heterogeneous tropical landscape, the Pantanal Wetlands. We also asked whether plant traits influence the difference in interaction specialization according to sampling. Plant-centred networks resulted in higher ß-diversity of interactions in space than animal-centred networks. Turnover explained most of the ß-diversity in both methods, but rewiring was proportionately more important when using the animal-centred method. While the plant-centred method indicated lower network modularity and specialization, floral traits modulated the effects of the sampling method on species-level network metrics. Combining animal- and plant-centred approaches returned intermediate values for ß-diversity of interactions and network metrics. Distinct methods may also be better suited for answering questions at different scales. Our results point out that the method choice, or combination of methods, should always reflect the appropriate scale of the factors determining the interactions being investigated.

Ecological mechanisms explaining interactions within plant-hummingbird networks: morphological matching increases towards lower latitudes.

Interactions between species are influenced by different ecological mechanisms, such as morphological matching, phenological overlap and species abundances. How these mechanisms explain interaction frequencies across environmental gradients remains poorly understood. Consequently, we also know little about the mechanisms that drive the geographical patterns in network structure, such as complementary specialization and modularity. Here, we use data on morphologies, phenologies and abundances to explain interaction frequencies between hummingbirds and plants at a large geographical scale. For 24 quantitative networks sampled throughout the Americas, we found that the tendency of species to interact with morphologically matching partners contributed to specialized and modular network structures. Morphological matching best explained interaction frequencies in networks found closer to the equator and in areas with low-temperature seasonality. When comparing the three ecological mechanisms within networks, we found that both morphological matching and phenological overlap generally outperformed abundances in the explanation of interaction frequencies. Together, these findings provide insights into the ecological mechanisms that underlie geographical patterns in resource specialization. Notably, our results highlight morphological constraints on interactions as a potential explanation for increasing resource specialization towards lower latitudes.

Trait evolution, resource specialization and vulnerability to plant extinctions among Antillean hummingbirds.

Species traits are thought to predict feeding specialization and the vulnerability of a species to extinctions of interaction partners, but the context in which a species evolved and currently inhabits may also matter. Notably, the predictive power of traits may require that traits evolved to fit interaction partners. Furthermore, local abiotic and biotic conditions may be important. On islands, for instance, specialized and vulnerable species are predicted to be found mainly in mountains, whereas species in lowlands should be generalized and less vulnerable. We evaluated these predictions for hummingbirds and their nectar-food plants on Antillean islands. Our results suggest that the rates of hummingbird trait divergence were higher among ancestral mainland forms before the colonization of the Antilles. In correspondence with the limited trait evolution that occurred within the Antilles, local abiotic and biotic conditions-not species traits-correlate with hummingbird resource specialization and the vulnerability of hummingbirds to extinctions of their floral resources. Specifically, hummingbirds were more specialized and vulnerable in conditions with high topographical complexity, high rainfall, low temperatures and high floral resource richness, which characterize the Antillean Mountains. These findings show that resource specialization and species vulnerability to extinctions of interaction partners are highly context-dependent.

Citizen science data reveal ecological, historical and evolutionary factors shaping interactions between woody hosts and wood-inhabiting fungi.

Woody plants host diverse communities of associated organisms, including wood-inhabiting fungi. In this group, host effects on species richness and interaction network structure are not well understood, especially not at large geographical scales. We investigated ecological, historical and evolutionary determinants of fungal species richness and network modularity, that is, subcommunity structure, across woody hosts in Denmark, using a citizen science data set comprising > 80 000 records of > 1000 fungal species on 91 genera of woody plants. Fungal species richness was positively related to host size, wood pH, and the number of species in the host genus, with limited influence of host frequency and host history, that is, time since host establishment in the area. Modularity patterns were unaffected by host history, but largely reflected host phylogeny. Notably, fungal communities differed substantially between angiosperm and gymnosperm hosts. Host traits and evolutionary history appear to be more important than host frequency and recent history in structuring interactions between hosts and wood-inhabiting fungi. High wood acidity appears to act as a stress factor reducing fungal species richness, while large host size, providing increased niche diversity, enhances it. In some fungal groups that are known to interact with live host cells in the establishment phase, host selectivity is common, causing a modular community structure.

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.

Influences of sampling effort on detected patterns and structuring processes of a Neotropical plant-hummingbird network.

Virtually all empirical ecological interaction networks to some extent suffer from undersampling. However, how limitations imposed by sampling incompleteness affect our understanding of ecological networks is still poorly explored, which may hinder further advances in the field. Here, we use a plant-hummingbird network with unprecedented sampling effort (2716 h of focal observations) from the Atlantic Rainforest in Brazil, to investigate how sampling effort affects the description of network structure (i.e. widely used network metrics) and the relative importance of distinct processes (i.e. species abundances vs. traits) in determining the frequency of pairwise interactions. By dividing the network into time slices representing a gradient of sampling effort, we show that quantitative metrics, such as interaction evenness, specialization (H2 '), weighted nestedness (wNODF) and modularity (Q; QuanBiMo algorithm) were less biased by sampling incompleteness than binary metrics. Furthermore, the significance of some network metrics changed along the sampling effort gradient. Nevertheless, the higher importance of traits in structuring the network was apparent even with small sampling effort. Our results (i) warn against using very poorly sampled networks as this may bias our understanding of networks, both their patterns and structuring processes, (ii) encourage the use of quantitative metrics little influenced by sampling when performing spatio-temporal comparisons and (iii) indicate that in networks strongly constrained by species traits, such as plant-hummingbird networks, even small sampling is sufficient to detect their relative importance for the frequencies of interactions. Finally, we argue that similar effects of sampling are expected for other highly specialized subnetworks.

Determinants of bird species richness, endemism, and island network roles in Wallacea and the West Indies: is geography sufficient or does current and historical climate matter?

Island biogeography has greatly contributed to our understanding of the processes determining species' distributions. Previous research has focused on the effects of island geography (i.e., island area, elevation, and isolation) and current climate as drivers of island species richness and endemism. Here, we evaluate the potential additional effects of historical climate on breeding land bird richness and endemism in Wallacea and the West Indies. Furthermore, on the basis of species distributions, we identify island biogeographical network roles and examine their association with geography, current and historical climate, and bird richness/endemism. We found that island geography, especially island area but also isolation and elevation, largely explained the variation in island species richness and endemism. Current and historical climate only added marginally to our understanding of the distribution of species on islands, and this was idiosyncratic to each archipelago. In the West Indies, endemic richness was slightly reduced on islands with historically unstable climates; weak support for the opposite was found in Wallacea. In both archipelagos, large islands with many endemics and situated far from other large islands had high importance for the linkage within modules, indicating that these islands potentially act as speciation pumps and source islands for surrounding smaller islands within the module and, thus, define the biogeographical modules. Large islands situated far from the mainland and/or with a high number of nonendemics acted as links between modules. Additionally, in Wallacea, but not in the West Indies, climatically unstable islands tended to interlink biogeographical modules. The weak and idiosyncratic effect of historical climate on island richness, endemism, and network roles indicates that historical climate had little effects on extinction-immigration dynamics. This is in contrast to the strong effect of historical climate observed on the mainland, possibly because surrounding oceans buffer against strong climate oscillations and because geography is a strong determinant of island richness, endemism and network roles.

Pollination syndromes ignored: importance of non-ornithophilous flowers to Neotropical savanna hummingbirds.

Generalization prevails in flower-animal interactions, and although animal visitors are not equally effective pollinators, most interactions likely represent an important energy intake for the animal visitor. Hummingbirds are nectar-feeding specialists, and many tropical plants are specialized toward hummingbird-pollination. In spite of this, especially in dry and seasonal tropical habitats, hummingbirds may often rely on non-ornithophilous plants to meet their energy requirements. However, quantitative studies evaluating the relative importance of ornithophilous vs. non-ornithophilous plants for hummingbirds in these areas are scarce. We here studied the availability and use of floral resources by hummingbirds in two different areas of the Cerrado, the seasonal savannas in Central Brazil. Roughly half the hummingbird visited plant species were non-ornithophilous, and these contributed greatly to increase the overall nectar availability. We showed that mean nectar offer, at the transect scale, was the only parameter related to hummingbird visitation frequency, more so than nectar offer at single flowers and at the plant scale, or pollination syndrome. Centrality indices, calculated using hummingbird-plant networks, showed that ornithophilous and non-ornithophilous plants have similar importance for network cohesion. How this foraging behaviour affects reproduction of non-ornithophilous plants remains largely unexplored and is probably case specific, however, we suggest that the additional energy provided by non-ornithophilous plants may facilitate reproduction of truly ornithophilous flowers by attracting and maintaining hummingbirds in the area. This may promote asymmetric hummingbird-plant associations, i.e., pollination depends on floral traits adapted to hummingbird morphology, but hummingbird visitation is determined more by the energetic "reward" than by pollination syndromes.