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Approximately 20,000 species of flowering plant offer mainly pollen to their pollinators, generally bees. Stamen dimorphism, a floral trait commonly present in some pollen flowers, is thought to be associated with exclusive pollen provision for highly effective bee pollinators. Notwithstanding, little is known about how stamen dimorphism is related to other floral morphological traits and, consequently, plant-pollinator interactions at the community scale. Here we investigated the relationship between stamen dimorphism and other floral morphological traits, as well as the interactions with pollinators in plants of Melastomataceae. We characterized each plant species as stamen dimorphic or stamen isomorphic according to differences in size and shape between stamen sets. Data on interactions between the plants and their bee pollinators were analysed as quantitative bipartite networks. We found that petal and style size and shape were correlated to stamen dimorphism. Stamen dimorphic species present larger flowers and less variable style shapes than stamen isomorphic species. Furthermore, stamen dimorphism is associated with higher richness of visiting bees, i.e. higher ecological generalization. During the evolutionary history of Melastomataceae, the dependence on pollinators for fruit set has possibly favoured the evolution of larger flowers with dimorphic stamens, which in turn are able to make use of a larger spectrum of pollen-collecting bees, leading to ecological generalization.

Functional traits can determine pairwise species interactions, such as those between plants and pollinators. However, the effects of biogeography and evolutionary history on trait-matching and trait-mediated resource specialization remain poorly understood.We compiled a database of 93 mutualistic hummingbird-plant networks (including 181 hummingbird and 1,256 plant species), complemented by morphological measures of hummingbird bill and floral corolla length. We divided the hummingbirds into their principal clades and used knowledge on hummingbird biogeography to divide the networks into four biogeographical regions: Lowland South America, Andes, North & Central America, and the Caribbean islands. We then tested: (a) whether hummingbird clades and biogeographical regions differ in hummingbird bill length, corolla length of visited flowers and resource specialization, and (b) whether hummingbirds' bill length correlates with the corolla length of their food plants and with their level of resource specialization.Hummingbird clades dominated by long-billed species generally visited longer flowers and were the most exclusive in their resource use. Bill and corolla length and the degree of resource specialization were similar across mainland regions, but the Caribbean islands had shorter flowers and hummingbirds with more generalized interaction niches. Bill and corolla length correlated in all regions and most clades, that is, trait-matching was a recurrent phenomenon in hummingbird-plant associations. In contrast, bill length did not generally mediate resource specialization, as bill length was only weakly correlated with resource specialization within one hummingbird clade (Brilliants) and in the regions of Lowland South America and the Andes in which plants and hummingbirds have a long co-evolutionary history. Supplementary analyses including bill curvature confirmed that bill morphology (length and curvature) does not in general predict resource specialization.These results demonstrate how biogeographical and evolutionary histories can modulate the effects of functional traits on species interactions, and that traits better predict functional groups of interaction partners (i.e. trait-matching) than resource specialization. These findings reveal that functional traits have great potential, but also key limitations, as a tool for developing more mechanistic approaches in community ecology.A free Plain Language Summary can be found within the Supporting Information of this article.

Indirect interactions are central to ecological and evolutionary dynamics in pollination communities, yet we have little understanding about the processes determining patterns of indirect interactions, such as those between pollinators through shared flowering plants. Instead, research has concentrated on the processes responsible for direct interactions and whole-network structures. This is partly due to a lack of appropriate tools for characterising indirect interaction structures, because traditional network metrics discard much of this information. The recent development of tools for counting motifs (subnetworks depicting interactions between a small number of species) in bipartite networks enables detailed analysis of indirect interaction patterns. Here we generate plant–hummingbird pollination networks based on three major assembly processes—neutral effects (species interacting in proportion to abundance), morphological matching and phenological overlap—and evaluate the motifs associated with each one. We find that different processes produce networks with significantly different patterns of indirect interactions. Neutral effects tend to produce densely connected motifs, with short indirect interaction chains, and motifs where many specialists interact indirectly through a single generalist. Conversely, niche-based processes (morphology and phenology) produced motifs with a core of interacting generalists, supported by peripheral specialists. These results have important implications for understanding the processes determining indirect interaction structures. A free Plain Language Summary can be found within the Supporting Information of this article.

Made available in DSpace on 2022-04-28T19:41:18Z (GMT). No. of bitstreams: 0 Previous issue date: 2022-01-01 Idea Wild Villum Fonden Many ecosystems have been modified by humans, creating novel habitats that include human-provided resources. Gardens adjacent to native habitats may affect plant–pollinator interactions by altering the determinants of interactions and species specialization. Here, we characterized a network comprising plants and hummingbirds interacting in a birdwatching garden with human-provided resources (nectar feeders and exotic plants) and adjacent Andean cloud forest in Colombia. Specifically, we investigated the proportion of hummingbirds visiting feeders and native/exotic plants to evaluate the connection between the habitats and the ecological determinants of the interaction network. Hummingbirds relied heavily on artificial nectar feeders in the garden, leaving the natural cloud forest for resources. Morphological matching was the single most important predictor of the observed pairwise interactions, for both hummingbirds and plants. At the species level, longer flowering phenology and a higher amount of sugar in nectar led to a higher degree for plants (i.e. the number of visiting hummingbird species). In contrast, a longer floral corolla was associated with lower specialization. Abundance was the best predictor of the number of partners for hummingbirds. The garden created for birdwatching attracted most, but not all, hummingbird species beyond their natural cloud forest habitat. Interestingly, the most frequently visited plants in the garden were native, especially the endemic and endangered tree Zygia lehmannii (Fabaceae). Our results show that some ecological mechanisms determining interactions in natural communities still hold in intensively modified habitats. Furthermore, a compromise between conservation and hummingbirds’ attraction to birding lodges/gardens is possible, for instance by favouring native and endemic plant species that are highly attractive for pollinators. Programa de Doctorado en Ciencias-Biología Departamento de Biología Facultad de Ciencias Naturales y Exactas Universidad del Valle Sede Meléndez, Calle 13 # 100-00 Grupo Ecología y Diversidad Vegetal Departamento de Biología Facultad de Ciencias Naturales Universidad del Valle, Calle 13 # 100-00 Laboratório de Ecologia da Polinização e Interações – LEPI Instituto de Biociências Universidade Estadual Paulista “Júlio de Mesquita Filho”, Distrito de Rubião Junior s/n; Cx. Postal 510 Center for Global Mountain Biodiversity GLOBE Institute University of Copenhagen, Universitetsparken 15 Centro de Síntese Ecológica e Conservação Departamento de Genética Ecologia e Evolução ICB Universidade Federal de Minas Gerais, CEP 31270-901 Laboratório de Ecologia da Polinização e Interações – LEPI Instituto de Biociências Universidade Estadual Paulista “Júlio de Mesquita Filho”, Distrito de Rubião Junior s/n; Cx. Postal 510 Villum Fonden: 25925

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.

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.

Cities harbour considerable biodiversity and there has been an increased concern about the conservation of pollinators in urban environments. Here, we evaluated how urbanization affects plant-hummingbird interactions at two spatial scales. First, in a medium-sized city from southeastern Brazil (>600,000 inhabitants), we contrasted interaction networks from urban and natural areas, and used artificial nectar feeder stations to evaluate changes in the composition of hummingbird assemblages across an urbanization gradient. Second, we compiled data on six urban plant-hummingbird interaction networks from south and southeastern Brazil to identify the characteristics associated with the most important plants. Locally, urbanization affected hummingbird communities by promoting higher generalization and dominance by more aggressive hummingbirds. Notably, specialized long-billed hermits were absent both in the urban interaction network and at feeder stations from more urbanized areas. Across networks, trees were more important for hummingbirds than shrubs/herbs as were specialized ornithophilous flowers in relation to non-ornithophilous flowers. Plant origin (native or exotic) did not matter. Our results indicate that urban plant-hummingbird communities are organized differently than their counterparts from natural areas, which usually feature key hermits and few trees. Since hermits provide important pollination services, especially for specialized ornithophilous plants, initiatives such as green corridors and preference for native plants with specialized hummingbird-pollinated flowers in urban landscaping may contribute to community restoration and ecosystem functioning.

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.

The temporal dynamics of plant phenology and pollinator abundance across seasons should influence the structure of plant–pollinator interaction networks. Nevertheless, such dynamics are seldom considered, especially for diverse tropical networks. Here, we evaluated the temporal variation of four plant–pollinator networks in two seasonal ecosystems in Central Brazil (Cerrado and Pantanal). Data were gathered on a monthly basis over 1 year for each network. We characterized seasonal and temporal shifts in plant–pollinator interactions, using temporally discrete networks. We predicted that the greater floral availability in the rainy season would allow for finer partitioning of the floral niche by the pollinators, i.e. higher specialization patterns as previously described across large spatial gradients. Finally, we also evaluated how sampling restricted to peak flowering period may affect the characterization of the networks. Contrary to our expectations, we found that dry season networks, although characterized by lower floral resource richness and abundance, showed higher levels of network‐wide interaction partitioning (complementary specialization and modularity). For nestedness, though, this between‐seasons difference was not consistent. Reduced resource availability in the dry season may promote higher interspecific competition among pollinators leading to reduced niche overlap, thus explaining the increase in specialization. There were no consistent differences between seasons in species‐level indices, indicating that higher network level specialization is an emergent property only seen when considering the entire network. However, bees presented higher values of specialization and species strength in relation to other groups such as flies and wasps, suggesting that some plant species frequently associated with bees are used only by this group. Our study also indicates that targeted data collection during peak flowering generates higher estimates of network specialization, possibly because species activity spans longer periods than the targeted time frame. Hence, depending on the period of data collection, different structural values for the networks of interactions may be found. Synthesis. Plant–pollinator networks from tropical environments have structural properties that vary according to seasons, which should be taken into account in the description of the complex systems of interactions between plants and their pollinators in these areas.

Fire acts as an ecological filter determining species diversity and composition of communities. In tropical savannas in Central Brazil, natural fire happens through lightning, but anthropogenic fire is also common, either controlled fire prescribed for management of vegetation and to promote grass growth or accidental and intentional fires related to deforestation and land use changes. Frequent fire events can have a negative effect on biodiversity by causing deaths of susceptible organisms, as well as through the homogenization of vegetation. Besides the composition of plant and animal species, fire also modifies biotic interactions, such as pollination, which impact ecosystem functioning. Here, we evaluated how time since the last fire event (hereafter postfire time interval) affects the structure, beta diversity of interactions and specialization of plants and floral visitors in a naturally burned Cerrado area. Postfire time interval had no effect on the structure of interaction networks and community diversity metrics, including beta-diversity of interactions. We did, however, find a positive relationship between flower abundance and postfire time intervals, and a negative effect of postfire time intervals on floral visitor species-level specialization. Thus, the negative effect of postfire time intervals on floral visitor specialization may be explained by the lower resource availability in areas recently burnt. The lack of strong and consistent effect of time interval since the last fire on plant-pollinator interactions from the Cerrado probably results from the resilience of these interactions to natural fires, which is a common element in this ecosystem. Increased frequency of more intense anthropogenic fires, however, may have stronger effects on biodiversity, and deserves further investigation in this biodiversity hotspot.

Plant species within communities may overlap in pollinators' use and influence visitation patterns of shared pollinators, potentially engaging in indirect interactions (e.g., facilitation or competition). While several studies have explored the mechanisms regulating insect-pollination networks, there is a lack of studies on bird-pollination systems, particularly in species-rich tropical areas. Here, we evaluated if phenotypic similarity, resource availability (floral abundance), evolutionary relatedness and flowering phenology affect the potential for indirect effects via shared pollinators in hummingbird-pollinated plant species within four communities in the Brazilian Atlantic forest. Among the evaluated factors, phenotypic similarity (corolla length and anther height) was the most important variable, while resource availability (floral abundance) had a secondary importance. On the other hand, evolutionary relatedness and flowering phenology were less important, which altogether highlights the relevance of convergent evolution and that the contribution of a plant to the diet of the pollinators of another plant is independent of the level of temporal overlap in flowering in this tropical system. Interestingly, our findings contrast with results from multiple insect-pollinated plant communities, mostly from temperate regions, in which floral abundance was the most important driver, followed by evolutionary relatedness and phenotypic similarity. We propose that these contrasting results are due to high level of specialization inherent to tropical hummingbird-pollination systems. Moreover, our results demonstrated that factors defining linkage rules of plant-hummingbird networks also determinate plant-plant potential indirect effects. Future studies are needed to test if these findings can be generalized to other highly specialized systems. Overall, our results have important implications for the understanding of ecological processes due resource sharing in mutualistic systems.

Ecological network approaches may contribute to conservation practices by quantifying within-community importance of species. In mutualistic plant-pollinator systems, such networks reflect potential pollination of the plants and a considerable portion of the energy consumption by the pollinators, two key components for each party. Here, we used two different sampling approaches to describe mutualistic plant-hummingbird networks from a cloud forest in the Colombian Western Andes, home to the Colorful Puffleg Eriocnemis mirabilis, an endemic and critically endangered hummingbird. We contrast networks between two localities (a protected area inside a National park vs. its buffer zone) and across sampling methods (floral visitation vs. pollen loads) to assess how the network structure and the importance of each hummingbird species within the networks may change. Visitation networks were characterized as having higher sampling completeness, yet pollen load network recorded more pollen types than plant species recorded by visitation. Irrespective of the sampling methods, the Colorful Puffleg was one of the most important hummingbird species in the network within the protected area inside the National park, but not in the buffer zone. Moreover, most species-level network indices were related to hummingbirds’ abundance. This suggests that conservation initiatives aimed at the endangered Colorful Puffleg may both help on the survival of this endangered hummingbird, as well as on maintaining its key role in the mutualistic interaction network inside the National Park. Our study illustrates how conservation practitioners could assess the local importance of endangered species using interaction network approaches.

International audience; Species are entangled within communities by their interactions in such a manner that their local extinction may unchain coextinction cascades and impact community dynamics and stability. Despite increasing attention, simulation models to estimate the robustness of interaction networks largely neglect the important role of interaction rewiring, that is, the ability of species to switch partners. Here we propose a new method to incorporate the potential of species to replace lost partners into a widely used coextinction model to estimate network robustness. In this model, species are allowed to rewire their interactions after initial loss of partners according to probabilities derived from well‐known mechanisms that determine mutualistic interactions, for example, trait matching, phenological overlap and abundances. To illustrate the use of this method, we analyzed a well‐sampled dataset of mutualistic plant–hummingbird interactions. We found that (a) in general, rewiring increases the estimated robustness, (b) networks are similarly robust to the loss of pollinators or plants, (c) morphological matching and phenological overlap leads to higher robustness, (d) when multiple rewiring mechanisms are combined, however, robustness increases little, and (e) rewiring tends to increase robustness more in scenarios when the loss of generalist species occurs first. Our results suggest that the same mechanisms known to drive plant–hummingbird network structure are relevant in buffering the effects of species loss via rewiring. The method proposed here can be applied to a wide range of interaction networks and is flexible to the inclusion of other variables important in determining interactions for specific systems. It also allows changes on the assumptions regarding the importance of distinct mechanisms, for instance including a hierarchical relationship, which facilitates insights into the relative importance of multiple variables influencing network disassembling. The analytical framework we offer here represents a step towards a more realistic estimation on how species loss may affect the integrity of interaction networks.

Abundant pollinators are often more generalised than rare pollinators. This could be because abundance drives generalisation: neutral effects suggest that more abundant species will be more generalised simply because they have more chance encounters with potential interaction partners. On the other hand, generalisation could drive abundance, as generalised species could have a competitive advantage over specialists, being able to exploit a wider range of resources and gain a more balanced nutrient intake. Determining the direction of the abundance-generalisation relationship is therefore a ‘chicken-and-egg’ dilemma. Here we determine the direction of the relationship between abundance and generalisation in plant-hummingbird pollination networks sampled from a variety of locations across the Americas. For the first time we resolve the direction of the abundance-generalisation relationship using independent data on animal abundance. We find evidence that hummingbird pollinators are generalised because they are abundant, and little evidence that hummingbirds are abundant because they are generalised. Additionally, a null model analysis suggests this pattern is due to neutral processes: most patterns of species-level abundance and generalisation were well explained by a null model that assumed interaction neutrality. These results suggest that neutral processes play a key role in driving broad patterns of generalisation in animal pollinators across large spatial scales.DeclarationsFunding – BIS is supported by the Natural Environment Research Council as part of the Cambridge Earth System Science NERC DTP [NE/L002507/1]. JVB was funded by CERL - Engineer Research and Development Center. PKM was funded by the São Paulo Research Foundation (FAPESP grant #2015/21457-4). PAC was funded by the David Lack studentship from the British Ornithologists’ Union and Wolfson College, University of Oxford. CL was funded by the ESDEPED-UAT grant. MAM acknowledges the Consejo Nacional para Investigaciones Científicas y Tecnológicas (Costa Rica), German Academic Exchange Service and the research funding program ‘LOEWE-Landes-Offensive zur Entwicklung Wissenschaftlichö konomischer Exzellenz’ of Hesse’s Ministry of Higher Education, Research, and the Arts (Germany). ROP was funded by CONACyT (project 258364). MAR was supported by the State of São Paulo Research Foundation (FAPESP) within the BIOTA/FAPESP, The Biodiversity Institute Program (www.biota.org.br) and the ‘Parcelas Permanentes’ project, as well as by Coordenação de Pessoal de Nível Superior (CAPES), Fundo de Apoio ao Ensino e à Pesquisa (FAEP)/Funcamp/Unicamp and The Nature Conservancy (TNC) of Brazil. LCR was supported by CNPq and Capes. MS was funded by CNPq (grant #302781/2016-1). AMMG is supported through a Marie Skłodowska-Curie Individual Fellowship (H2020-MSCA-IF-2016-704409). LVD was supported by the Natural Environment Research Council (grants NE/K015419/1 and NE/N014472/1). AMMG, JS, CR and BD thank the Danish National Research Foundation for its support of the Center for Macroecology, Evolution and Climate (grant no. DNRF96). WJS is funded by Arcadia.

• Floral visitors differ in their efficacy as pollinators and the impact of different pollinator species on the pollen flow and plant reproduction has been frequently evaluated. In contrast, the impact of within-species foraging changes on their efficacy as pollinators has been seldom quantified. • We studied a self-incompatible shrub Palicourea rigida (Rubiaceae) and its hummingbird pollinators which adjust their behaviour according to floral resources availability. Fluorescence microscopy was used to access pollen tube growth and incompatibility reaction in pistils after a single visit of territorial or intruder hummingbirds in two populations. To characterize the plant populations and possible differences on resource availability between areas we used a three-term quadrat variance method to detect clusters of floral resources. • Within species variation in foraging behaviour, but not the species identity affected pollinator efficacy. Effectively, hummingbirds intruding territories deposited more compatible pollen grains on P. rigida stigmas than territory holders in both study areas. Additionally, territory holders deposited more incompatible than compatible pollen grains. • Our results imply that intraspecific foraging behaviour variation has consequences for pollination success. Quantifying such variation and addressing the implications of intraspecific variability contribute to a better understanding of the dynamics and consequences of plant-pollinators interactions. This article is protected by copyright. All rights reserved.

Hummingbirds are the most common group of vertebrate pollinators in the Neotropics, associated with pollination of ornithophilous flowers. The group can be divided into hermits and non-hermits, in which hermits are often regarded as the most specialized group closely associated with more specialized ornithophilous plants. In this study, we investigated the association of ornithophilous flowers and hummingbirds in two small fragments of forest surrounded by an urban matrix. We characterized the species composition, abundance and phenology of the hummingbirds and ornithophilous plants and related pollinator abundance to floral resource availability. Our results were compared to published data from other forest areas from the Cerrado. In our study areas, the diversity of ornithophilous plants and hummingbirds was similar to what has been reported for forest fragments in the Cerrado. Nevertheless, we found Thalurania furcata, a non-hermit, acting as the most frequent hummingbird pollinator in contrast to more preserved areas in which a hermit, Phaethornis pretrei, is commonly found as the main pollinator for ornithophilous plants. The nectar energy availability at the plant population level was the only factor associated with hummingbird visitation rates, suggesting that a higher availability of nectar resources in the fragments attracts greater abundance of birds. The unusual setting of having a non-hermit species as the main hummingbird pollinator in forest areas suggests that habitat fragmentation can favor more generalist hummingbird species, and this potentially has consequence for the pollination of associated plants.

Elucidating the factors determining the occurrence of florivorous organisms is an essential step for comprehending arthropod–plant interactions, especially when considering florivores that use flowers/inflorescences as microhabitats. In this study, we characterize the interaction between florivorous thrips (Thysanoptera) and Palicourea rigida (Rubiaceae), a distylous hummingbird-pollinated shrub. We investigated the relative role of different factors in determining thrips occurrence in the flower and inflorescence microhabitats. Furthermore, we experimentally examined the protective role of corolla influencing thrips exploration of floral buds. Frankliniella musaeperda (Thripidae) was the only species recorded on P. rigida, feeding on floral tissue, pollen and nectar. Thrips occurrence was not related to distyly, but rather to floral stage. Open flowers presented the highest abundance of thrips, followed by senescent flowers and then buds. The experimental opening of buds translated in increased thrips occurrence, indicating that F. musaeperda manage to explore the microhabitat offered by the floral chamber, as long as there is an opening in the corolla. In inflorescences, thrips abundance was negatively related to the number of ants visiting extrafloral nectaries. We found that the marked difference between floral morphs of distylous plants is not necessarily reflected in the abundance of florivores. Thrips seek for floral cavities, preferentially those with fresh tissue, which may confer nutrient-rich food and protection. Buds also provide this; however, the enclosed petals are an effective barrier against F. musaeperda entrance. At inflorescence scale, presence of mutualistic ants in high numbers can drive away these flower-feeding insects. Despite the abundance of thrips in the flowers, there was no evidence of any functional relationship, either of pollination for flowers or of breeding for insects. We demonstrate here that in the flower/inflorescence microhabitat, structural and biotic factors play a key role in the exploitation and occupation by insect florivores.

Author(s): Araujo, AC; Martin Gonzalez, AM; Sandel, B; Maruyama, PK; Fischer, E; Vizentin-Bugoni, J; de Araujo, FP; Coelho, AG; Faria, RR; Kohler, G; Las-Casas, FMG; Lopes, AV; Machado, AO; Machado, CG; Machado, IC; McGuire, JA; Moura, AC; Oliveira, GM; Oliveira, PE; Rocca, MA; Rodrigues, LDC; Rodrigues, M; Rui, AM; Sazima, I; Sazima, M; Varassin, IG; Wang, Z; Dalsgaard, B; Svenning, JC | Abstract: Aim: We examined the effects of space, climate, phylogeny and species traits on module composition in a cross-biomes plant–hummingbird network. Location: Brazil, except Amazonian region. Methods: We compiled 31 local binary plant–hummingbird networks, combining them into one cross-biomes metanetwork. We conducted a modularity analysis and tested the relationship between species’ module membership with traits, geographical location, climatic conditions and range sizes, employing random forest models. We fitted reduced models containing groups of related variables (climatic, spatial, phylogenetic, traits) and combinations of groups to partition the variance explained by these sets into unique and shared components. Results: The Brazilian cross-biomes network was composed of 479 plant and 42 hummingbird species, and showed significant modularity. The resulting six modules conformed well to vegetation domains. Only plant traits, not hummingbird traits, differed between modules, notably plants’ growth form, corolla length, flower shape and colour. Some modules included plant species with very restricted distributions, whereas others encompassed more widespread ones. Widespread hummingbirds were the most connected, both within and between modules, whereas widespread plants were the most connected between modules. Among traits, only nectar concentration had a weak effect on among-module connectivity. Main conclusions: Climate and spatial filters were the main determinants of module composition for hummingbirds and plants, potentially related to resource seasonality, especially for hummingbirds. Historical dispersal-linked contingency, or environmental variations not accounted for by the explanatory factors here evaluated, could also contribute to the spatial component. Phylogeny and morphological traits had no unique effects on the assignment of species to modules. Widespread species showed higher within- and/or among-module connectivity, indicating their key role connecting biomes, and, in the case of hummingbirds, communities within biomes. Our results indicate that biogeography and climate not only determine the variation of modularity in local plant–animal networks, as previously shown, but also affect the cross-biomes network structure.

Convergent reproductive traits in non-related plants may be the result of similar environmental conditions and/or specialised interactions with pollinators. Here, we documented the pollination and reproductive biology of Bionia coriacea (Fabaceae), Esterhazya splendida (Orobanchaceae) and Ananas ananassoides (Bromeliaceae) as case studies in the context of hummingbird pollination in Cerrado, the Neotropical savanna of Central South America. We combined our results with a survey of hummingbird pollination studies in the region to investigate the recently suggested association of hummingbird pollination and self-compatibility. Plant species studied here differed in their specialisation for ornithophily, from more generalist A. ananassoides to somewhat specialist B. coriacea and E. splendida. This continuum of specialisation in floral traits also translated into floral visitor composition. Amazilia fimbriata was the most frequent pollinator for all species, and the differences in floral display and nectar energy availability among plant species affect hummingbirds' behaviour. Most of the hummingbird-pollinated Cerrado plants (60.0%, n = 20), including those studied here, were self-incompatible, in contrast to other biomes in the Neotropics. Association to more generalist, often territorial, hummingbirds, and resulting reduced pollen flow in open savanna areas may explain predominance of self-incompatibility. But it is possible that mating system is more associated with the predominance of woody hummingbird plants in the Cerrado plant assemblage than to the pollination system itself.

Aim To investigate the association between hummingbird–plant network structure and species richness, phylogenetic signal on species' interaction pattern, insularity and historical and current climate. Location Fifty-four communities along a c. 10,000 km latitudinal gradient across the Americas (39° N–32° S), ranging from sea level to c. 3700 m a.s.l., located on the mainland and on islands and covering a wide range of climate regimes. Methods We measured the level of specialization and modularity in mutualistic plant–hummingbird interaction networks. Using an ordinary least squares multimodel approach, we examined the influence of species richness, phylogenetic signal, insularity and current and historical climate conditions on network structure (null-model-corrected specialization and modularity). Results Phylogenetically related species, especially plants, showed a tendency to interact with a similar array of mutualistic partners. The spatial variation in network structure exhibited a constant association with species phylogeny (R2 = 0.18–0.19); however, network structure showed the strongest association with species richness and environmental factors (R2 = 0.20–0.44 and R2 = 0.32–0.45, respectively). Specifically, higher levels of specialization and modularity were associated with species-rich communities and communities in which closely related hummingbirds visited distinct sets of flowering species. On the mainland, specialization was also associated with warmer temperatures and greater historical temperature stability. Main conclusions Our results confirm the results of previous macroecological studies of interaction networks which have highlighted the importance of species richness and the environment in determining network structure. Additionally, for the first time, we report an association between network structure and species phylogenetic signal at a macroecological scale, indicating that high specialization and modularity are associated with high interspecific competition among closely related hummingbirds, subdividing the floral niche. This suggests a tighter co-evolutionary association between hummingbirds and their plants than in previously studied plant–bird mutualistic systems.

Interactions between flowers and their visitors span the spectrum from mutualism to antagonism. The literature is rich in studies focusing on mutualism, but nectar robbery has mostly been investigated using phytocentric approaches focused on only a few plant species. To fill this gap, we studied the interactions between a nectar-robbing hermit hummingbird, Phaethornis ruber, and the array of flowers it visits. First, based on a literature review of the interactions involving P. ruber, we characterized the association of floral larceny to floral phenotype. We then experimentally examined the effects of nectar robbing on nectar standing crop and number of visits of the pollinators to the flowers of Canna paniculata. Finally, we asked whether the incorporation of illegitimate interactions into the analysis affects plant-hummingbird network structure. We identified 97 plant species visited by P. ruber and found that P. ruber engaged in floral larceny in almost 30% of these species. Nectar robbery was especially common in flowers with longer corolla. In terms of the effect on C. paniculata, the depletion of nectar due to robbery by P. ruber was associated with decreased visitation rates of legitimate pollinators. At the community level, the inclusion of the illegitimate visits of P. ruber resulted in modifications of how modules within the network were organized, notably giving rise to a new module consisting of P. ruber and mostly robbed flowers. However, although illegitimate visits constituted approximately 9% of all interactions in the network, changes in nestedness, modularity, and network-level specialization were minor. Our results indicate that although a flower robber may have a strong effect on the pollination of a particular plant species, the inclusion of its illegitimate interactions has limited capacity to change overall network structure.

Complex networks of species interactions might be determined by species traits but also by simple chance meetings governed by species abundances. Although the idea that species traits structure mutualistic networks is appealing, most studies have found abundance to be a major structuring mechanism underlying interaction frequencies. With a well-resolved plant–hummingbird interaction network from the Neotropical savanna in Brazil, we asked whether species morphology, phenology, nectar availability and habitat occupancy and/or abundance best predicted the frequency of interactions. For this, we constructed interaction probability matrices and compared them to the observed plant-hummingbird matrix through a likelihood approach. Furthermore, a recently proposed modularity algorithm for weighted bipartite networks was employed to evaluate whether these factors also scale-up to the formation of modules in the network. Interaction frequencies were best predicted by species morphology, phenology and habitat occupancy, while species abundances and nectar availability performed poorly. The plant–hummingbird network was modular, and modules were associated to morphological specialization and habitat occupancy. Our findings highlight the importance of traits as determinants of interaction frequencies and network structure, corroborating the results of a previous study on a plant–hummingbird network from the Brazilian Atlantic Forest. Thus, we propose that traits matter more in tropical plant–hummingbird networks than in less specialized systems. To test the generality of this hypothesis, future research could employ geographic or taxonomic cross-system comparisons contrasting networks with known differences in level of specialization.

This study shows that three Frankliniella (Thysanoptera) species have species-specific associations with their hosts: F. varipes–Faramea cyanea (Rubiaceae); F. musaeperda–Hancornia speciosa (Apocynaceae) and F. fulvipes–Solanum lycocarpum (Solanaceae). All thrips species had a marked preference for flowers in anthesis, as in this stage flowers provide food and protection from environment. Frankliniella musaeperda and F. varipes populations were female-biased while F. fulvipes was male-biased. Since many species of Frankliniella have economic importance, studies on the ecology of these species are essential, given the possibility of invasion of agricultural systems in the future.

Species ofMiconiaare considered keystone plant resources for frugivorous birds in Neotropical forests, but for other ecosystems little of their ecological role is known. The fruiting phenology and the composition of frugivores of fourMiconiaspecies in savanna and palm swamp from the Brazilian Neotropical savanna were studied in three sites from November 2005 to May 2011. The hypothesis tested was that plants from different habitats share their frugivores and consequently promote links between habitats. Through focal plant observations (30–50 h per species in each site), 668 visits by 47 species of birds were recorded and plants from different habitats shared most of the frugivores (49–97%). The fruiting ofMiconia chamissoisin the palm swamp during the period of fruit scarcity (dry season) was accompanied by an enhancement in the frugivore bird richness and abundance in this habitat, providing indirect evidence of resource tracking. Bird species which primarily dwell in savanna recorded consuming fruits in palm swamps during the resource-scarce season is taken as evidence of landscape supplementation.Miconiaassemblage studied here seems to promote a link between two adjacent habitats in the Neotropical savanna from Central Brazil, a link which is likely to be common in this naturally patchy ecosystem.

Aim: To investigate the role of alien plants in mutualistic plant-hummingbird networks, assessing the importance of species traits, floral abundance and insularity on alien plant integration. Location: Mainland and insular Americas. Methods: We used species-level network indices to assess the role of alien plants in 21 quantitative plant-hummingbird networks where alien plants occur. We then evaluated whether plant traits, including previous adaptations to bird pollination, and insularity predict these network roles. Additionally, for a subset of networks for which floral abundance data were available, we tested whether this relates to network roles. Finally, we tested the association between hummingbird traits and the probability of interaction with alien plants across the networks. Results: Within the 21 networks, we identified 32 alien plant species and 352 native plant species. On average, alien plant species attracted more hummingbird species (i.e. aliens had a higher degree) and had a higher proportion of interactions across their hummingbird visitors than native plants (i.e. aliens had a higher species strength). At the same time, an average alien plant was visited more exclusively by certain hummingbird species (i.e. had a higher level of complementary specialization). Large alien plants and those occurring on islands had more evenly distributed interactions, thereby acting as connectors. Other evaluated plant traits and floral abundance were unimportant predictors of network roles. Short-billed hummingbirds had higher probability of including alien plants in their interactions than long-billed species. Main conclusions: Once incorporated into plant-hummingbird networks, alien plants appear strongly integrated and, thus, may have a large influence on network dynamics. Plant traits and floral abundance were generally poor predictors of how well alien species are integrated. Short-billed hummingbirds, often characterized as functionally generalized pollinators, facilitate the integration of alien plants. Our results show that plant-hummingbird networks are open for invasion. © 2016 John Wiley & Sons Ltd.

Mistletoes constitute an important food resource for animals in many ecosystems. However, these plants are considered pests in urban areas because of deleterious effects they have on the host trees. Studies in urban areas were mostly focused on listing host species or procedures to control the “pest”. In this sense, broader studies including several aspects of mistletoes ecology in urban ecosystems are still missing. We studied the interaction of the mistletoe, Phoradendron affine, with its dispersers and hosts in two urban sites in Uberlândia, Brazil. Phoradendron affine fruits were consumed almost exclusively by Euphonia chlorotica, which was crucial for seed germination. Parasitism was recorded in five hosts, two native (Handroanthus chrysotrichus and Tabebuia roseoalba) and three exotic species (Spathodea campanulata, Ligustrum lucidum and Melia azedarach). Mistletoes were found parasitizing larger host trees, a trend commonly reported for mistletoe-host interaction. Mistletoe seed germination was not affected by the trees species, whether host or non-host, but the radicle of germinated seeds could not penetrate the bark and seedlings invariably died in non-host species. We found a high prevalence of parasitism in our study, in comparison to what previous studies reported for natural areas. The spatial distribution of the hosts and high light incidence on isolated host trees may lead to this high prevalence in urban areas. Rather than eradicated, mistletoes in urban areas should be ecologically managed and their importance for bird species conservation must be considered. More studies to determine which bird species are favoured by mistletoe presence in urban areas will be essential for this purpose.

In this study we examined the role of a gall-inducing nematode on the diversity of arthropods associated with Miconia albicans (Melastomataceae), acting as an ecosystem engineer. Nematode galls (i.e. leaves and infructescences) supported higher arthropod diversity than healthy plant structures, and some species were found only in the gall. Galled leaves and infructescences harbored species of different trophic levels, suggesting that galls provide distinct resources, such as food tissue and refuge. We conclude that the presence of gall has a strong effect on the diversity and composition of arthropod fauna and a gall inducer can be important microhabitat engineers where they are abundant, having considerable influence on the diversity of small organisms inhabiting plants.

Currently, pollination is seen as involving more generalist interactions than specialized ones. Supporting this trend, some nocturnal distylous flowers may also receive floral visitors during the day, and since the latter contribute to fruit set, the pollination system is mixed and less specialized. Common among the Rubiaceae, distyly has been regarded as a reproductive strategy which requires a precise and specialized pollination system, and in this important tropical family, environmental disturbance and pollination failure have been used to explain anomalies in distylous features. Faramea cyanea Mull. Arg. is a common tree species in forest formations in the increasingly threatened Cerrado biome, the Neotropical savannas in Central Brazil. We evaluated the floral morphology, pollination biology and breeding system of a population of F. cyanea. Despite their moth pollination features, flowers were visited by diurnal (bees) as well as nocturnal (moths) pollinators. Experimental results showed that both pollinator groups contributed equally to pollen flow and legitimate pollination. The population presented distyly, isoplethy and heteromorphic self-incompatibility. Although F. cyanea did not present exact reciprocal herkogamy between floral morphs, pollination and reproductive success were not impaired. Floral features, which allowed pollination by complementary groups of pollinators, may explain the absence of anomalies in the isoplethy and distylous features in the studied population, anomalies which have been observed in other sympatric distylous Rubiaceae.

Behavioural patterns of birds commonly vary according to flock size and daily activity pattern. Southern lapwing behaviours and their relation with flock size were studied, as well as the relationship between the frequency of behaviours and the period of the day. Results showed that the proportion of time spent in foraging and vigilance was higher during the morning, when small groups were more common, and decreased from midday on, when group size increased. Maintenance and inactivity (sleeping) behaviours presented the opposite pattern. Correlation between flock size and period of the day, and their similar effects on bird behaviour may be evidence that groups of different sizes could have different functions throughout the day. Our results show that southern lapwings seem to form smaller flocks for feeding in the beginning of the day and larger flocks later for different activities (e.g., maintenance and sleeping). In this sense, it is possible that group size variation throughout the day is related to different demands for specific behaviours (functions) of groups, according to the daily activity patterns of the birds.

Made available in DSpace on 2015-03-18T15:52:33Z (GMT). No. of bitstreams: 0 Previous issue date: 2014-11-01Bitstream added on 2015-03-18T16:29:28Z : No. of bitstreams: 1 WOS000344476500012.pdf: 1197331 bytes, checksum: bc084f306396871f48167363b5b8b10d (MD5) Carlsberg Foundation Danish Research Council \ Natural Sciences Weis-Fogh fund at Department of Zoology, University of Cambridge Faculty of Science and Technology at Aarhus University Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) Danish National Research Foundation Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) MADALGO - Center for Massive Data Algorithmics, a Center of the Danish National Research Foundation Aarhus University Research Foundation via the Center for Interdisciplinary Geospatial Informatics Research - CIGIR Arcadia 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. Univ Copenhagen, Nat Hist Museum Denmark, Ctr Macroecol Evolut & Climate, DK-2100 Copenhagen O, Denmark Univ Cambridge, Dept Zool, Conservat Sci Grp, Cambridge CB2 3EJ, England Aarhus Univ, Dept Biol Sci, DK-8000 Aarhus C, Denmark Univ Estadual Paulista UNESP, Inst Biociencias, Dept Bot, Plant Phenol & Seed Dispersal Grp, BR-13506900 Rio Claro, SP, Brazil Univ Estadual Campinas UNICAMP, Programa Posgrad Ecol, BR-13083865 Campinas, SP, Brazil Univ Estadual Paulista UNESP, Inst Biociencias, Dept Bot, Plant Phenol & Seed Dispersal Grp, BR-13506900 Rio Claro, SP, Brazil FAPESP: 11/22635-2 CAPES: 99999.012341/2013-04

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.