Efeitos indiretos mediados por polinizadores em comunidades de plantas

Orientadores: Marlies Sazima, Marina Wolowski TorresTese (doutorado) - Universidade Estadual de Campinas, Instituto de BiologiaResumo: As plantas com flores frequentemente compartilham polinizadores, levando a efeitos indiretos mediados por estes. Apesar de muitos estudos terem avaliado estes efeitos entre pares de espécies de plantas, ainda não é clara a relação entre efeitos indiretos e processos ecológicos ao nível da comunidade. Assim, é incerto que fatores ecológicos determinam a direção dos efeitos indiretos mediados por polinizadores (de competição à facilitação) e como estes efeitos influenciam padrões e processos em comunidades de plantas. Neste sentido, caracterizar a denso-dependência na polinização e incorporar medidas de sucesso reprodutivo podem elucidar como os efeitos indiretos atuam em comunidades de plantas. Avaliamos os efeitos indiretos mediados por polinizadores ao nível da comunidade a partir da denso-dependência coespecífica e heteroespecífica na polinização e suas implicações na coexistência (Capítulo 1) e como esses efeitos indiretos afetam a estrutura e dinâmica (Capítulo 2) de uma comunidade de plantas de campos de altitude. Além disso, desenvolvemos um arcabouço teórico e analítico a partir da teoria de redes ecológicas para estudar efeitos indiretos mediados por polinizadores e o aplicamos à uma comunidade de plantas de dunas mediterrâneas (Capítulo 3) e à flora ornitófila de floresta tropical montana (Capítulo 4). Encontramos denso-dependência negativa (evidenciando competição intraspecífica em espécies abundantes) e facilitação interespecífica principalmente para espécies raras na polinização dos campos de altitude, uma combinação que favorece a coexistência nesta comunidade com baixa atividade de polinizadores. Além disso, especialização, display floral e grupo funcional de polinizador foram características ecológicas importantes que determinaram a direção da denso-dependência e de interações indiretas interespecíficas. Além disso, períodos com alta abundância de flores e baixa diversidade funcional de atributos reprodutivos estavam associados a maior sucesso reprodutivo nos campos de altitude. Estes padrões estruturais da comunidade evidenciam a prevalência de facilitação entre espécies com atributos reprodutivos similares entre si. Contudo, identificamos predominância de competição interespecífica na polinização influenciando o sucesso reprodutivo das plantas nas dunas mediterrâneas e facilitação interespecífica na polinização diminuindo a limitação polínica na flora ornitófila de floresta montana. Nestas duas comunidades os efeitos indiretos foram assimétricos: espécies de plantas generalistas e atrativas atuaram como as que causam os efeitos indiretos, enquanto que espécies especialistas e menos atrativas como as que recebem estes efeitos. Com isso, demonstramos como os efeitos indiretos mediados por polinizadores influenciam padrões e processos em comunidades de plantas. Em conclusão, fornecemos evidências que a polinização é um eixo importante do nicho, mediando interações entre plantas ao nível da comunidadeAbstract: Flowering plants often share pollinators, leading to pollinator-mediated indirect effects. Although several studies have evaluated pollinator-mediated effects between plant species pairs, it is still unclear how indirect effects determine ecological processes at the community-level. It is uncertain which ecological factors determine the direction of the pollinator-mediated indirect effects (from competition to facilitation) and how such effects influence patterns and processes in plant communities. In this context, assessments of density-dependence in pollination and the incorporation of fitness estimates may improve the understanding about how pollinator-mediated indirect effects act on plant communities. We evaluated pollinator-mediated indirect effects at the community-level by characterizing conspecific and heteroespecific density-dependence in pollination and its implications in coexistence (Chapter 1) and how such effects influence the structure and dynamics (Chapter 2) of a tropical highland grassland plant community. We also developed a theoretical and analytical framework using network theory to study pollinator-mediated indirect effects and applied it to a mediterranean dune plant community (Chapter 3) and to an ornithophilous flora of a tropical montane forest Park (Chapter 4). We found negative density-dependence (showing intraspecific competition for abundant plant species) and interspecific facilitation most for rare plant species in pollination of the highland grasslands, a combination that fosters coexistence in this community marked by low pollinator activity. Moreover, ecological factors such as specialization, floral display and pollinator functional group determined the direction of the density-dependence and interspecific indirect interactions. Otherwise, periods with high floral abundance and low functional diversity of reproductive traits were associated with high fitness in the highland grasslands. These structural community patterns highlight the prevalence of facilitation among species with similar reproductive traits. Nevertheless, we identified a predominance of interspecific competition in pollination influencing plant fitness in the mediterranean dunes and interspecific facilitation in pollination alleviating pollen limitation of the ornithophilous floral in the montane forest. The indirect effects were asymmetrical in these two communities: generalized and attractive plant species acted as the ones causing the indirect effects, whereas specialized and less attractive species as the ones receiving such effects. Thereby, we showed how pollinator-mediated indirect effects influence patterns and processes in plant communities. In summary, we provided evidence on how pollination is an important niche axis, mediating plant-plant interactions at the community-levelDoutoradoEcologiaDoutor em Ecologia2016/06434-0140254/2016-1FAPESPCNPq

Estruturação de comunidades e potencial para efeitos indiretos de plantas polinizadas por beija-flores na Floresta Atlântica

Orientador: Marlies SazimaDissertação (mestrado) - Universidade Estadual de Campinas, Instituto de BiologiaResumo: A interação entre plantas e polinizadores influencia a estruturação das comunidades de plantas. Espécies de plantas que compartilham polinizadores podem competir ou se facilitar por sua polinização, impactando as populações de plantas e por consequência, suas ocorrências nas comunidades. Porém, ainda são poucos os estudos que investigam a influência da polinização na estruturação das comunidades e por quais mecanismos as plantas compartilham polinizadores e potencialmente exercem efeitos indiretos entre si. Nesta dissertação, enfocamos comunidades de plantas polinizadas por beija-flores na Floresta Atlântica como modelo de estudo. Utilizando uma abordagem filogenética e funcional, investigamos como o parentesco evolutivo, diferentes atributos florais e abundâncias determinam a estruturação espacial e temporal destas comunidades (Capítulo 1) e a partilha de polinizadores entre as espécies de plantas (Capítulo 2). Encontramos estrutura filogenética aleatória e estrutura funcional e temporal agregadas, indicando que processos relacionados ao atributo das espécies são importantes na escala espacial avaliada. Plantas com atributos florais semelhantes e espécies mais abundantes tem maior potencial para efeitos indiretos por compartilharem mais beija-flores. O primeiro resultado reforça o acoplamento fenotípico como um mecanismo estruturando as interações entre plantas e beija-flores, enquanto o segundo mostra que abundâncias podem se tornar importantes ao avaliar efeitos indiretos entre plantas nas comunidades. Em geral, padrões em ecologia de comunidades são contingentes à história evolutiva e atributos das espécies. Neste estudo, demonstramos que comunidades de plantas polinizadas por beija-flores podem exibir uma estrutura nos atributos florais, possivelmente devido a interações indiretas entre plantas compartilhando beija-flores. Além disso, esta estrutura também pode levar a um maior potencial para efeitos indiretos entre estas plantasAbstract: Plant-pollinator interactions influence the assembly of plant communities. Plant species sharing pollinators engage on competitive or facilitative interactions for pollination, impacting plant populations and consequently, their occurrences in communities. However, there are few studies investigating how pollination influence community assembly and by which mechanisms plants have indirect effects when sharing pollinators. Here, we focused on hummingbird-pollinated plant communities of the Atlantic forest as study model. Using a phylogenetic and functional approach, we investigate how evolutionary relatedness, floral traits and abundances determine the spatial and temporal community assembly (Chapter 1) and pollinator-sharing among plant species (Chapter 2). We found random phylogenetic structure and clustered functional and temporal structure, indicating that trait-based processes increase in importance at the spatial scale evaluated. Plants with similar floral traits and abundant species have higher potential for indirect effects by sharing more hummingbird pollinators. The first result reinforces phenotypic match as a structuring mechanism of plant-hummingbird interactions, while the latter shows that abundance increases in importance when evaluating the indirect effects among plants in communities. In general, patterns in community ecology are contingent to the evolutionary history and traits of the species. Here we found that hummingbird-pollinated plant communities can exhibit a floral trait structure, possibly caused by indirect interactions between plants sharing pollinators. Moreover, these community structure can also lead to a higher potential for indirect effects between these plantsMestradoEcologiaMestre em Ecologia13188/2014-5CNP

Flower colour within communities shifts from overdispersed to clustered along an alpine altitudinal gradient

Altitudinal gradients are interesting models to test the effect of biotic and abiotic drivers of floral colour diversity, since an increase in UV irradiance, decrease of pollinator availability and shifts from bee- to fly-pollination in high relative to low altitudes are expected. We tested the effect of altitude and phylogeny, using several chromatic and achromatic colour properties, UV-reflectance and pollinators’ discrimination capacity (Apis mellifera, Bombus terrestris, Musca do-mestica and Eristalis tenax), to understand the floral colour diversity in an alpine altitudinal gradi-ent. All colour properties were weakly related to phylogeny. We found a shift from overdispersed floral colours and high chromatic contrast with the background (for bees) in the low altitude, to clustered floral colours (UV and green range for bees and flies) and clustered chromatic and achro-matic properties in the high altitude. Different from flies, bees could discriminate floral colours in all altitudinal ranges. Low altitudes are likely to exhibit suitable conditions for more plant species, in-creasing competition for pollinators and floral colour divergence. Conversely, the increase in UV-irradiance in high altitudes may filter plants with specific floral UV-reflectance patterns. Overall, floral colour diversity suggests that both biotic (pollinator fauna) and abiotic (UV-irradiance) drivers shape floral communities, but their importance changes with altitude

WorldFAIR (D10.3) Agricultural biodiversity FAIR data assessment rubrics

The WorldFAIR Case Study on Agricultural Biodiversity (WP10) addresses the challenges of advancing interoperability and mobilising plant-pollinator interactions data for reuse. Previous efforts, reported in WorldFAIR Deliverable 10.1, ‘Agriculture-related pollinator data standards use cases report’ (Trekels et al., 2023), provided an overview of projects, good practices, tools, and examples for creating, managing and sharing data related to plant-pollinator interactions. It also outlined a work plan for conducting pilot studies. Deliverable 10.2 (Drucker et al., 2024) presented Agricultural Biodiversity Standards, Best Practices and Guidelines Recommendations. This deliverable presented results from six pilot studies that adopted standards and recommendations from the earlier report. The current report complements the efforts with Agricultural Biodiversity FAIR data assessment rubrics.We introduce a set of FAIR assessment tools tailored to the plant-pollinator interactions domain. These tools are designed to help researchers and institutions evaluate adherence to the FAIR principles. In the discovery phase, we found that a significant amount of data on plant-pollinator interactions is available as supplementary files of research articles, in a diversity of formats such as PDFs, Excel spreadsheets, and text files. The diversity of approaches and the lack of appropriate data vocabularies lead to confusion, information loss, and the need for complex data interpretation and transformation. Our proposed framework primarily targets researchers in this domain who wish to assess the FAIRness of the data they produce and take action to improve it. However, we believe it can also benefit data reviewers, data stewards, data repository managers and librarians dealing with plant-pollinator data. Our approach focuses on being as familiar as possible with the researcher's practices, language, and jargon. Ultimately, we aim to promote data publishing and reuse in the plant-pollinator interactions domain.We present a ‘Rubric for the assessment of Plant-Pollinator Interactions Data’ with examples from the data from the pilots developed in Deliverable 10.2 and in relation to the FAIR Implementation Profile (FIP) created by Work Package 10. We conduct ‘dataset assessments’ of available data from research projects surveyed in the discovery phase. Additionally, we describe in detail the ‘Automated FAIR-enabled Data Reviews’ generated by the Global Biotic Interactions (GLoBI) infrastructure, with examples from the pilots. We believe the tools described in this report will encourage data publishing and reuse in the plant-pollinator interactions domain. Moving from diverse approaches and siloed initiatives to widely available FAIR plant-pollination interactions data for scientists and decision-makers will enable the development of integrative studies that enhance our understanding of species biology, behaviour, ecology, phenology, and evolution

Meaningful Words in Crowd Noise: Searching for Volatiles Relevant to Carpenter Bees among the Diverse Scent Blends of Bee Flowers

Olfactory cues constitute one of the most important plant-pollinator communication channels. Specific chemical components can be associated with specific pollinator functional groups due to pollinator-mediated selection on flower volatile (FV) emission. Here, we used multivariate analyses of FV data to detect an association between FVs and the worldwide distributed pollinator group of the carpenter bees (Xylocopa spp.). We compiled FVs of 29 plant species: 9 pollinated by carpenter bees, 20 pollinated by other bee pollinator functional groups. We tested whether FV emission differed between these groups. To rule out any phylogenetic bias in our dataset, we tested FV emission for phylogenetic signal. Finally, using field assays, we tested the attractive function of two FVs found to be associated with carpenter bees. We found no significant multivariate difference between the two plant groups FVs. However, seven FVs (five apocarotenoid terpenoids, one long-chain alkane and one benzenoid) were significantly associated with carpenter bee pollination, thus being “predictor” compounds of pollination by this pollinator functional group. From those, β-ionone and (E)-methyl cinnamate presented the highest indicator values and had their behavioural function assessed in field assays. Phylogenetic signal for FVs emission was weak, suggesting that their emission could result from pollinator-mediated selection. In field assays, the apocarotenoid β-ionone attracted carpenter bees, but also bees from other functional groups. The benzenoid (E)-methyl cinnamate did not attract significant numbers of pollinators. Thus, β-ionone functions as a non-specific bee attractant, while apocarotenoid FVs emerge as consistent indicators of pollination by large food-foraging bees among bee-pollinated flowers

Data from: Flower colour and visitation rates of Costus arabicus support the "bee avoidance" hypothesis for red-reflecting hummingbird-pollinated flowers

Floral colour mediates plant–pollinator interactions by often signalling floral resources. In this sense, hummingbird-pollinated flowers are frequently red-coloured, and there are two tentative hypotheses to explain this pattern: 1. hummingbirds are attracted to red due its easier detection and 2. bees are sensorially excluded from red flowers. The second hypothesis is based on bees’ red colour blindness, which lead them to be less frequent and less important than hummingbirds as pollinators of red-reflecting flowers. Here, we untangled the role of different flower traits mediating plant–pollinator interactions and empirically tested the above hypotheses. We chose Costus arabicus due to its synchronopatric white- and pink-flowered individuals and its bee and hummingbird pollination system. Although pink flowers are not totally achromatic as pure red ones, they show an achromaticity degree that could drive bee exclusion. Specifically, we tested whether differences on red reflectance work attracting hummingbirds or excluding bees and the consequent implications for the plant's reproduction. Flower colour morphs of C. arabicus do differ neither in morphology nor in nectar sugar content. Moreover, white and pink flowers can be discriminated by the bees’ and hummingbirds’ colour vision system. Both groups are able to discriminate the red colour variation morph on the flower petals, the white flowers being more easily detected by bees and the pink flowers by hummingbirds. Bees preferentially visited the white flowers, whereas hummingbirds visited both colours at the same rate – both patterns corroborating the second hypothesis. Pollen loads deposited on stigmas did not differ between flower colour morphs, indicating that bees and hummingbirds play a similar role in the overall pollen deposition. However, bees are more likely to self-pollinate than hummingbirds. Self-pollination limits C. arabicus reproduction, and red-reflecting flowers may be better pollinated by discouraging bee visitation. Therefore, the intraspecific colour variation is driving flowers to show colour-related different levels of generalization. Our results support the ‘bee avoidance’ rather than the ‘hummingbird preference’ hypothesis. Sensory exclusion of bees seems to be the pressure for red-reflecting flowers evolution, driving specialization in hummingbird-pollinated flowers due to the costs of bee pollination on plant reproduction

Pollinator movement behaviour on Costus arabicus

Bees and hummingbirds movement between Costus arabicus individuals while foraging on flower

Trait patterns across space and time suggest an interplay of facilitation and competition acting on Neotropical hummingbird-pollinated plant communities

Pollinators may influence plant community assembly through biotic filtering and/or plant-plant competition and facilitation. The relative importance of each process, however, vary according to the scale and how strongly plants share their pollinators, and possibly in relation to the pollinator groups considered. We here investigated the assembly of three Atlantic forest hummingbird-pollinated plant communities across space (among all species in the communities) and time, i.e. yearly flowering phenology (between pairs of co-flowering species), based on the pairwise distances of multiple floral traits (corolla length, anther and stigma height, colour and nectar). Because tropical hummingbird-pollinated plants are often subdivided in two pollination niches (hermits versus non-hermits), we also analyzed these groups separately. We found that trait structure across space was clustered for some floral traits, suggesting biotic filtering and facilitation. All floral traits had weak phylogenetic signal, indicating that closely related species were not more similar than distantly related species. Moreover, floral traits were randomly structured along the phenology when analyzing all plants together. On the other hand, we found similar corolla length but divergent anther height in co-flowering pairs within the same pollination niche. Thus, plants may benefit from flowering together and avoid competition through fine adjustments in reproductive traits. The results also suggest that clear signals of competition and facilitation among plants are only apparent when species strongly share their pollinators and depending on the traits that are considered. Our study illustrates a complex interplay of biotic filtering, facilitation and competition as processes structuring guilds of plants sharing the same functional group of pollinators1271116901700CONSELHO NACIONAL DE DESENVOLVIMENTO CIENTÍFICO E TECNOLÓGICO - CNPQCOORDENAÇÃO DE APERFEIÇOAMENTO DE PESSOAL DE NÍVEL SUPERIOR - CAPESFUNDAÇÃO DE AMPARO À PESQUISA DO ESTADO DE SÃO PAULO - FAPESP830514/1999-6; 303084/2011-1sem informação2013/15129-9; 2015/21457-