Pollinator-mediated facilitation alleviates pollen limitation in a plant-hummingbird network.

Facilitation and competition among plants sharing pollinators have contrasting consequences for plant fitness. However, it is unclear whether pollinator-mediated facilitation and competition may affect pollen limitation (potential contribution of pollination to fitness) in pollination networks. Here, we investigated how pollinator sharing affects pollen limitation in a tropical hummingbird-pollinated community marked by facilitation. We employed indices describing how much a plant species potentially affects the pollination of other co-flowering species through shared pollinators (acting degree) and is affected by other co-flowering species (target degree) within the plant-hummingbird network. Since facilitation often increases pollination quantity but not necessarily quality, we expected both indices to be associated with reductions in pollen limitation estimates that depend on pollination quantity (fruit set and seed number) rather than estimates more strictly related to quality (seed weight and germination). We found that both indices were associated with reductions in pollen limitation only for seed weight and germination. Thus, facilitation occurred via qualitative estimates of pollen limitation. Our results suggest that facilitation may enhance plant fitness estimates even if quantitative components of plant fecundity are already saturated. Overall, we showed that pollinator-mediated indirect effects in a multispecies context are important drivers of plant fitness estimates with consequences for coexistence in diverse communities.

Pollination generalization and reproductive assurance by selfing in a tropical montane ecosystem.

Pollination and reproduction are important processes for understanding plant community dynamics. Information regarding pollination and reproduction is urgent for threatened ecosystems, such as tropical montane ecosystems. In tropical mountains, pollination patterns are expected to conform to the reproductive assurance theory (due to low pollinator activity) and old, climatically buffered and infertile landscapes (OCBIL) theory (due to restricted plant range size). For 82 plant species of the Itatiaia National Park (including endemic and endangered species), we evaluated at least one of the following features: pollinator identity, flower color and size, flowering phenology, and pollinator dependence. Most plant species (ca. 60%) were pollinated by two or more functional groups of pollinators (generalized pollination), with high importance of flies as pollinators. There was low pollinator activity overall (less than one visit per flower per hour). Notably, the invasive honeybee Apis mellifera L. performed half of the visits to this entire plant community, suggesting an impact on the native pollinator fauna and consequently on the native flora. Most endemic plants were generalized with white and small flowers, while endangered species were pollination-specialized with colorful and large flowers. Thus, endangered species are susceptible to changes in pollinator fauna. Flowering seasonality reflected the importance of climatic constraints in this environment. One-third of the plant species were autogamous. Our data suggest that pollinator scarcity may have promoted reproductive assurance strategies such as generalization and pollinator independence. Our community-level study highlighted consistent pollination patterns for tropical mountains and emphasized threats for specialized endangered species.

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.

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

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

Plant traits moderate pollen limitation of introduced and native plants: a phylogenetic meta-analysis of global scale.

The role of pollination in the success of invasive plants needs to be understood because invasives have substantial effects on species interactions and ecosystem functions. Previous research has shown both that reproduction of invasive plants is often pollen limited and that invasive plants can have high seed production, motivating the questions: How do invasive populations maintain reproductive success in spite of pollen limitation? What species traits moderate pollen limitation for invaders? We conducted a phylogenetic meta-analysis with 68 invasive, 50 introduced noninvasive and 1931 native plant populations, across 1249 species. We found that invasive populations with generalist pollination or pollinator dependence were less pollen limited than natives, but invasives and introduced noninvasives did not differ. Invasive species produced 3× fewer ovules/flower and >250× more flowers per plant, compared with their native relatives. While these traits were negatively correlated, consistent with a tradeoff, this did not differ with invasion status. Invasive plants that produce many flowers and have floral generalisation are able to compensate for or avoid pollen limitation, potentially helping to explain the invaders' reproductive successes.

The potential indirect effects among plants via shared hummingbird pollinators are structured by phenotypic similarity.

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.

More than euglossines: the diverse pollinators and floral scents of Zygopetalinae orchids.

Floral volatile organic compounds (VOCs) play important roles in plant-pollinator interactions. We investigated the reproductive ecology and floral VOCs of Zygopetalinae orchids to understand the relationship between floral scents and pollinators. We performed focal observations, phenological censuses and breeding system experiments in eight species in southeast Brazil. Floral scents were collected and analysed using SPME/GC-MS. We performed multivariate analyses to group species according to affinities of their VOCs and define compounds associated to each plant. Dichaea cogniauxiana was pollinated by weevils which use their developing ovules, while D. pendula was pollinated by the same weevils and perfume-collecting male euglossine bees. The other species were deceit-pollinated by bees. Zygopetalum crinitum was pollinated by carpenter bees, while W. warreana, Z. mackayi and Z. maxillare were bumblebee-pollinated. The latter was also pollinated by Centris confusa. Breeding system varied widely with no association to any pollinator group. Most VOCs are common to other floral scents. Zygopetalum crinitum presented an exclusive blend of VOCs, mainly composed of benzenoids. The scents of Pabstia jugosa, Promenaea xanthina and the Zygopetalum spp. were similar. The bumblebee-pollinated species have flowering periods partially overlapped, thus neither phenology nor pollinators constitute hybridization barriers among these species. Euglossines are not the only pollinators of Zygopetalinae. Different VOCs, size and lifespan of flowers are associated with distinct pollinators. A distinctive VOC bouquet may determine specialisation in carpenter bees or male euglossines within bee-pollinated flowers. Finally, visitation of deceit-pollinated flowers by perfume-collecting euglossines allows us to hypothesise how pollination by this group of bees had evolved.

Community-wide assessment of pollen limitation in hummingbird-pollinated plants of a tropical montane rain forest.

BACKGROUND AND AIMS: Although pollen limitation of reproduction (PL) has been widely studied, our understanding of its occurrence in tropical communities, especially for bird-pollinated plants, is underdeveloped. In addition, inclusion of both quantity and quality aspects in studies of PL are generally lacking. Within hummingbird-pollinated plants, a prediction was made for higher PL for the quality than quantity aspects and a minor effect of temporal variation because hummingbirds are constant and efficient pollen vectors but they may transfer low quality pollen. METHODS: Field hand and open pollination experiments were conducted on 21 species in a tropical montane rain forest over 2 years. The quantity (fruit set and seeds per fruit) and quality (seed weight and germination) aspects of reproduction were assessed as the response to open pollination relative to outcross hand pollination. The relationships between the effect size of quantity and quality aspects of reproduction and predictive plant features (self-incompatibility, autogamy, density and pollinator specialization level) were assessed with phylogenetic generalized linear models. KEY RESULTS: Just over half of all the species expressed PL for one or more response variables. On average, the severity of PL was strong for one quality variable (seed germination; 0·83), but insignificant for another (seed weight; -0·03), and low to moderate for quantity variables (0·31 for seeds per fruit and 0·39 for fruit set). There was only a minor contribution of temporal variation to PL within the studied species. Common predictors of PL, i.e. phylogenetic relatedness, self-incompatibility, autogamy, plant density and pollinator specialization level, did not adequately explain variation in PL within this community. CONCLUSIONS: Despite the measurable degree of PL within these hummingbird-pollinated plants, the causes of pollen quality and quantity insufficiency are not clear. Variables other than those tested may contribute to PL or causes of PL may vary among species and cannot adequately be accounted for when assessed from the within-community perspective.

Predominance of self-compatibility in hummingbird-pollinated plants in the Neotropics.

Both plant traits and plant-pollinator interactions are thought to influence plant mating systems. For hummingbird-pollinated plants, foraging strategy (territorial or traplining) is also expected to influence plant mating. We hypothesize that the traplining behavior of hermits promotes outcrossing, whereas the behavior of non-hermits favours self-incompatibility. Thus, selection is expected to maintain self-incompatibility in plants pollinated by non-hermits. We explore the incidence of self-incompatibility in Neotropical hummingbird-pollinated plants and its association with hummingbird behavior and plant traits. We conducted a literature review (56 species) and performed hand-pollination experiments in 27 hummingbird-pollinated plants in an Atlantic rainforest. We found that self-incompatibility (measured as <0.3 for the Index of Self-incompatibility [ISI]) occurred in only 33 % of the Neotropical hummingbird-pollinated plants. The interaction of hummingbird and habit type affected ISI, as did phylogenetic relationships. Specifically, herbs pollinated by non-hermits had higher ISI than woody plants pollinated by non-hermits, and herbs pollinated by both hermits and non-hermits. For the Atlantic rainforest plant guild, 30 % of the species were self-incompatible. ISI was higher in herbs than in woody species and increased with plant aggregation but was not dependent on foraging behavior, plant density, or floral display. Although hummingbirds differ in their foraging strategies, these behavioral differences seem to have only a minor influence on the incidence of self-incompatibility. Phylogenetic relatedness seems to be the strongest determinant of mating system in Neotropical hummingbird-pollinated plants.

Integrating public engagement to intensify pollination services through ecological restoration.

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

Data standardization of plant-pollinator interactions.

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

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

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

Reproduction, pollination and seed predation of Senna multijuga (Fabaceae) in two protected areas in the Brazilian Atlantic forest.

One important subject is to determine the effectiveness of conservation areas, where different management categories are being applied, to maintain effective sexual reproduction in plants and their interactions with animal groups. To evaluate this issue, we compared the phenology, reproductive success, pollination and pre-dispersal seed predation of the legume tree Senna multijuga in two differently managed protected areas in Southeastern Brazil: the Itatiaia National Park and the Environmental Protection Area of Serrinha do Alambari, from December 2007 to December 2008. Vegetative and reproductive phenodinamycs were registered monthly in 80 individuals; other evaluations included 104 observation hours for pollination (March-May 2008) in 51 inflorescences; besides, fruit counts, fecundity and seed predation. Sexual reproduction of S. multijuga depends on the transfer of pollen by large bees (Bombus, Centris, Epicharis and Xylocopa), as the species is self-incompatible. Bruchidae species of the genus Acanthoscelides and Sennius predate seeds. Vegetative and reproductive phenodynamics differed among sites. Our results indicated that ecological interactions were lower at the protected area, but the reproductive processes in S. multijuga were not ruptured or critically degraded. This reinforces the idea that landscape areas with intermediate levels of protection, such as environmental protection areas, are suitable as buffer zones, and thus, relevant to the conservation of ecological processes when associated with more strictly protected areas.

Widespread vulnerability of flowering plant seed production to pollinator declines.

Despite evidence of pollinator declines from many regions across the globe, the threat this poses to plant populations is not clear because plants can often produce seeds without animal pollinators. Here, we quantify pollinator contribution to seed production by comparing fertility in the presence versus the absence of pollinators for a global dataset of 1174 plant species. We estimate that, without pollinators, a third of flowering plant species would produce no seeds and half would suffer an 80% or more reduction in fertility. Pollinator contribution to plant reproduction is higher in plants with tree growth form, multiple reproductive episodes, more specialized pollination systems, and tropical distributions, making these groups especially vulnerable to reduced service from pollinators. These results suggest that, without mitigating efforts, pollinator declines have the potential to reduce reproduction for most plant species, increasing the risk of population declines.

Chemical Basis of Floral Color Signals in Gesneriaceae: The Effect of Alternative Anthocyanin Pathways.

Changes in floral pigmentation can have dramatic effects on angiosperm evolution by making flowers either attractive or inconspicuous to different pollinator groups. Flower color largely depends on the type and abundance of pigments produced in the petals, but it is still unclear whether similar color signals rely on same biosynthetic pathways and to which extent the activation of certain pathways influences the course of floral color evolution. To address these questions, we investigated the physical and chemical aspects of floral color in the Neotropical Gesnerioideae (ca. 1,200 spp.), in which two types of anthocyanins, hydroxyanthocyanins, and deoxyanthocyanins, have been recorded as floral pigments. Using spectrophotometry, we measured flower reflectance for over 150 species representing different clades and pollination syndromes. We analyzed these reflectance data to estimate how the Gesnerioideae flowers are perceived by bees and hummingbirds using the visual system models of these pollinators. Floral anthocyanins were further identified using high performance liquid chromatography coupled to mass spectrometry. We found that orange/red floral colors in Gesnerioideae are produced either by deoxyanthocyanins (e.g., apigenidin, luteolinidin) or hydroxyanthocyanins (e.g., pelargonidin). The presence of deoxyanthocyanins in several lineages suggests that the activation of the deoxyanthocyanin pathway has evolved multiple times in the Gesnerioideae. The hydroxyanthocyanin-producing flowers span a wide range of colors, which enables them to be discriminated by hummingbirds or bees. By contrast, color diversity among the deoxyanthocyanin-producing species is lower and mainly represented at longer wavelengths, which is in line with the hue discrimination optima for hummingbirds. These results indicate that Gesnerioideae have evolved two different biochemical mechanisms to generate orange/red flowers, which is associated with hummingbird pollination. Our findings also suggest that the activation of the deoxyanthocyanin pathway has restricted flower color diversification to orange/red hues, supporting the potential constraining role of this alternative biosynthetic pathway on the evolutionary outcome of phenotypical and ecological diversification.

Effect of heterospecific pollen deposition on pollen tube growth depends on the phylogenetic relatedness between donor and recipient.

Co-flowering plant species may interact via pollinators leading to heterospecific pollen transfer with consequences for plant reproduction. What determines the severity of heterospecific pollen effect on conspecific pollen performance is unclear, but it may depend on the phylogenetic relatedness of the interactors (pollen donors and recipient). The heterospecific pollen effect might also depend on the extent to which plants are exposed to heterospecific pollen over ecological or evolutionary timescales. For instance, generalist-pollinated plant species might tolerate heterospecific pollen more than specialists. Here, we tested whether heterospecific pollen effects are stronger between closely related species than phylogenetically distant ones in a tropical highland community. Then, based on these results, we determined whether responses to heterospecific pollen were stronger in generalized vs. specialized plant species. We applied heterospecific pollen from close (congeneric) or distant (different families) donors alone or with conspecific pollen on stigmas of three recipient species (one generalist, Sisyrinchium wettsteinii; and two specialists, Fuchsia campos-portoi and Fuchsia regia) and scored pollen tube performance in styles. In all species, pollen from closely related donors grew pollen tubes to the base of the style indicating a high potential to interfere with seed set. Conversely, distantly related heterospecific pollen had no effect on either specialist Fuchsia species, whereas enhanced performance of conspecific pollen was observed in generalist S. wettsteinii. The strong effect of phylogenetic relatedness of donor and recipient might have obscured the role of pollination specialization, at least for the three species examined here. Therefore, phylogenetic relatedness mediated the effect of heterospecific pollen on post-pollination success, with possible consequences for reproductive trait evolution and community assembly for further studies to explore.

Land use and pollinator dependency drives global patterns of pollen limitation in the Anthropocene.

Land use change, by disrupting the co-evolved interactions between plants and their pollinators, could be causing plant reproduction to be limited by pollen supply. Using a phylogenetically controlled meta-analysis on over 2200 experimental studies and more than 1200 wild plants, we ask if land use intensification is causing plant reproduction to be pollen limited at global scales. Here we report that plants reliant on pollinators in urban settings are more pollen limited than similarly pollinator-reliant plants in other landscapes. Plants functionally specialized on bee pollinators are more pollen limited in natural than managed vegetation, but the reverse is true for plants pollinated exclusively by a non-bee functional group or those pollinated by multiple functional groups. Plants ecologically specialized on a single pollinator taxon were extremely pollen limited across land use types. These results suggest that while urbanization intensifies pollen limitation, ecologically and functionally specialized plants are at risk of pollen limitation across land use categories.

The contribution of the BIOTA/FAPESP Program to the knowledge on pollination and plant reproduction / Contribuição do Programa BIOTA/FAPESP para o conhecimento sobre polinização e reprodução em plantas

Abstract Interactions between plant and pollinators are associated with the origin and maintenance of species diversity, as well as ecosystem functioning. The potential of pollination as an ecosystem service is evidenced by its association with food production. Understanding pollination at the landscape scale is essential for characterizing the pollination service for several crops that depend on pollinators for fruit and seed set that make up the human diet. Our aim was to carry out a literature review of studies and projects funded by BIOTA/FAPESP to illustrate the main research approaches developed in the field of Pollination Biology, especially related to plant-pollinator interactions. Plant-pollinator interactions in the Atlantic forest were leveraged as a result of this long-term research program, during which several papers were published in international journals. Pollination by bees (melittophily) was the most representative pollination system studied. In addition to melittophily, other interactions were studied such as pollination by hawkmoths (sphingophily), by hummingbirds (ornithophily) and by bats (chiropterophily). The specific mutualistic relationships between fig trees and fig wasps were also subject of studies within the Program. At the beginning of the BIOTA/FAPESP Program, there were many gaps in basic information about pollination and breeding systems of Brazilian native plant species. Thus, the Program was fundamental to fuel research on the natural history of plants and pollinators from the Atlantic forest. Overall, the Program funded studies that investigated themes such as functional pollination ecology, pollinator effectiveness, plant population genetics, structure and dynamics of plant-pollinator interaction networks, as well as geographic distribution and macroevolution of pollination systems, as well as genetic and molecular studies of native plant populations focusing on pollen flow and genetic structure of populations. Additionally, studies on pollination in the context of landscape ecology had the aim of assessing the effects of forest fragmentation on the functioning of plant populations and their interactions with pollinators and the relationships between landscape structure and ecological processes, biodiversity, and ecosystem service. Therefore, the Program had a prominent role in producing basic data with great implications for understanding the ecology and promoting the conservation of plant-pollinator interactions.

Resumo A interação planta-polinizador está associada à origem e manutenção da diversidade de espécies de plantas e ao funcionamento dos ecossistemas. O potencial da polinização como serviço ecossistêmico é destacado quando associado à produção de alimentos. Compreender esta interação na escala da paisagem é essencial para caracterizar o serviço de polinização para muitos cultivos que dependem dos polinizadores para a formação de frutos e sementes que integram a dieta humana. O objetivo deste trabalho foi realizar uma revisão bibliográfica de estudos e projetos financiados pelo BIOTA/FAPESP para ilustrar as principais abordagens de pesquisa desenvolvidas no campo da Biologia da Polinização, especialmente relacionadas à interação planta-polinizador. As interações planta-polinizador na Mata Atlântica foram alavancadas como resultado desse programa de pesquisa de longo prazo, durante o qual vários artigos foram publicados em revistas internacionais. A polinização por abelhas (melitofilia) foi o sistema de polinização mais representativo estudado. Além da melitofilia, outras interações foram estudadas, como a polinização por mariposas (esfingofilia), por beija-flores (ornitofilia) e por morcegos (quiropterofilia). As relações mutualísticas específicas entre figueiras e vespas do figo também foram objeto de estudos no âmbito do Programa. No início do Programa BIOTA/FAPESP, havia muitas lacunas sobre informações básicas sobre polinização e sistemas de reprodução de espécies vegetais nativas brasileiras. Assim, o Programa foi fundamental para desenvolver pesquisas sobre a história natural de plantas e polinizadores da Mata Atlântica. No geral, o Programa financiou estudos que investigaram temas como ecologia funcional da polinização, eficácia de polinizadores, genética de populações de plantas, estrutura e dinâmica de redes de interação planta-polinizador, bem como distribuição geográfica e macroevolução dos sistemas de polinização, além de estudos genéticos e moleculares de populações de plantas nativas com foco no fluxo de pólen. Adicionalmente, estudos sobre polinização no contexto da ecologia da paisagem tiveram como objetivo avaliar os efeitos da fragmentação florestal no funcionamento das populações de plantas e suas interações com os polinizadores e as relações entre a estrutura da paisagem e os processos ecológicos, biodiversidade e serviços ecossistêmicos. Portanto, o Programa teve um papel de destaque na produção de dados básicos com grandes implicações para o entendimento da ecologia e promoção da conservação das interações planta-polinizador.

Meta-analysis of pollen limitation reveals the relevance of pollination generalization in the Atlantic forest of Brazil.

Despite the extensive knowledge of pollen limitation in angiosperms, its assessment within tropical forests is still limited. Especially lacking are large scale comparisons of species within this biome - one that is highly diverse but also becoming increasingly threatened. In fact, many tropical plant species depend upon pollinators for reproduction but evaluation of the impact of this dependence via different levels of pollination specialization has yet to be made at the biome scale. We assessed the occurrence and magnitude of pollen limitation for species in the Brazilian Atlantic forest and tested the association of pollination specialization, breeding system, and life habit with pollination efficiency. We compiled data from studies published between 1985 and 2012. We calculated species' effect size (d) from data on fruit set after hand cross-pollination and natural pollination and conducted standard and phylogenetically independent meta-analysis. Overall pollen limitation was moderate, with magnitude of 0.50, and 95% confidence interval [0.37, 0.62] for 126 species. Pollen limitation was observed in 39% of species. Pollination specialization was the factor that best explained the occurrence of pollen limitation. Specifically, phenotypic and ecological specialists (plants with zygomorphic flowers and pollinated by one species of pollinator, respectively) had higher pollen limitation than generalist plants (actinomorphic flowers and pollination by two or more species). Functional generalists (plants pollinated by three or more functional groups) were not pollen limited. On the other hand, breeding system and life habit were not associated to pollen limitation. Pollen limitation was observed in the Atlantic forest and its magnitude was comparable to that for angiosperms as a whole. The finding that pollination specialization was the strongest predictor of pollen limitation suggests that specialist plants in this biome may be most prone to the reproductive failure as a result of pollinator loss.

Reproduction, pollination and seed predation of Senna multijuga (Fabaceae) in two protected areas in the Brazilian Atlantic forest

One important subject is to determine the effectiveness of conservation areas, where different management categories are being applied, to maintain effective sexual reproduction in plants and their interactions with animal groups. To evaluate this issue, we compared the phenology, reproductive success, pollination and pre-dispersal seed predation of the legume tree Senna multijuga in two differently managed protected areas in Southeastern Brazil: the Itatiaia National Park and the Environmental Protection Area of Serrinha do Alambari, from December 2007 to December 2008. Vegetative and reproductive phenodinamycs were registered monthly in 80 individuals; other evaluations included 104 observation hours for pollination (March-May 2008) in 51 inflorescences; besides, fruit counts, fecundity and seed predation. Sexual reproduction of S. multijuga depends on the transfer of pollen by large bees (Bombus, Centris, Epicharis and Xylocopa), as the species is self-incompatible. Bruchidae species of the genus Acanthoscelides and Sennius predate seeds. Vegetative and reproductive phenodynamics differed among sites. Our results indicated that ecological interactions were lower at the protected area, but the reproductive processes in S. multijuga were not ruptured or critically degraded. This reinforces the idea that landscape areas with intermediate levels of protection, such as environmental protection areas, are suitable as buffer zones, and thus, relevant to the conservation of ecological processes when associated with more strictly protected areas. Rev. Biol. Trop. 59 (4): 1939-1948. Epub 2011 December 01.

Es importante determinar la eficacia de las áreas de conservación cuando se están implementando diferentes categorías de manejo, y una forma de hacerlo es conociendo si se mantiene una reproducción sexual efectiva en las especies de plantas y sus interacciones con grupos de animales. Para evaluar esta cuestión, se comparó la fenología, el éxito reproductivo, la polinización y la pre-dispersión de semillas depredadas de la leguminosa Senna multijuga en dos áreas protegidas sometidas a diferente tipos de manejo en el sureste de Brasil: el Parque Nacional de Itatiaia y el Área de Protección Ambiental de Serrinha de Alambari, de diciembre 2007 a diciembre 2008. La fenodinámica vegetativa y reproductiva fue registrada mensualmente en 80 individuos; otras evaluaciones incluyeron 104 horas de observación de la polinización (marzo-mayo 2008) en 51 inflorescencias, además del conteo de frutos, fecundidad y depredación de semillas. S. multijuga tiene una reproducción sexual que depende de la polinización de abejas grandes (Bombus, Centris, Epicharis y Xylocopa) y se considera una especie auto-incompatible. Las semillas son depredadas por especies de Bruchidae de los géneros Acanthoscelides y Sennius. La fenodinámica vegetativa y reproductiva difirió entre sitios. Nuestros resultados indican que las interacciones ecológicas fueron menores en el área protegida, pero los procesos reproductivos de S. multijuga no se vieron interrumpidos ni degradados de manera crítica. Esto refuerza la idea de que las zonas de paisaje con niveles intermedios de protección, tales como las áreas de protección ambiental, son adecuadas como zonas de amortiguamiento, y por lo tanto, relevantes para la conservación de los procesos ecológicos cuando se asocian con áreas en las que se da una protección más estricta.