Acta Botanica Brasilica, Volume: 32, Issue: 3, Published: 2018
  • Floral biology and pollination in Brazil: history and possibilities Review

    Oliveira, Paulo Eugênio; Rech, André Rodrigo

    Abstract in English:

    ABSTRACT Pollination research in Brazil virtually started with Fritz Muller, whose insights supported Darwin's evolutionary theory. Pollination systems of Brazilian plants were studied mainly by travelling researchers until early last century when native or resident geneticists began to use floral biology information to deal with crop acclimatization and breeding, later applying similar experiments and techniques to investigate native plants. Bee geneticists studied common pollinators of crops, such as coffee and Citrus, and even the introduction of feral African honeybees, despite their associated problems, stimulated pollination research. Geneticists attracted Dobzhansky to Brazil, where his research on tree distribution in the Brazilian Amazon represented a turning point for tropical pollination research by prompting the discovery of long-distance pollinating bees, thus bringing pollination back to mainstream evolutionary research. Tropical pollination studies stimulated the emergence of research groups in the Amazon and São Paulo states. In 1998, a seminal conference held in São Paulo called for the need to conserve pollinators and pollination systems. Subsequent research has been integrated under the Brazilian Pollinators Initiative, with research groups established throughout the country. A revived International Pollination Course, a National Pollination Symposium, and cooperative efforts to tackle complex interaction networks may direct future pollination research in Brazil.
  • Towards a unified terminology for angiosperm reproductive systems Review

    Cardoso, João Custódio Fernandes; Viana, Matheus Lacerda; Matias, Raphael; Furtado, Marco Túlio; Caetano, Ana Paula de Souza; Consolaro, Hélder; Brito, Vinícius Lourenço Garcia de

    Abstract in English:

    ABSTRACT Angiosperms display an enormous diversity of forms, functions and strategies when it comes to reproduction. This multiplicity has been translated into several terminological concepts and contexts, which have facilitated further research. On the other hand, the use of terms that address the reproduction of flowering plants has been shown to be inconsistent in the literature, complicating communication among specialists. Key terms, such as “reproductive system”, “mating system” and “sexual system”, among others, have been frequently cited as synonyms, and even used in different circumstances. This review proposes to establish a consistent nomenclatural classification in the field of angiosperms reproductive biology in order to facilitate communication among researchers. Specific terms related to angiosperm reproduction are conceptualized and distributed into five general systems: four related to sexual reproduction (sexual, floral, incompatibility and mating systems); and one related to asexual reproduction (apomictic systems). Our proposal is not to establish a natural classification, but rather to provide a general overview of the main concepts that were grouped here in an artificial and functional manner. Our aim is to advance the field of reproductive biology of angiosperms with consistent and well-defined applications of relevant terminologies.
  • Anther specializations related to the division of labor in Microlicia cordata (Spreng.) Cham. (Melastomataceae) Articles

    Velloso, Mariana de Souza Carvalho; Brito, Vinícius Lourenço Garcia de; Caetano, Ana Paula Souza; Romero, Rosana

    Abstract in English:

    ABSTRACT In heterantherous flowers, some anthers have an attraction and feeding function, while others are related to plant reproduction. Microlicia cordata has dimorphic stamens organized in two cycles: the antesepalous one with large stamens and pink anthers, and the antepetalous one with small stamens and yellow anthers. Division of labor was analyzed using the parameters of structure, composition, amount and estimated viability of pollen, and the color of floral parts. The anthers of the pollinating stamens were larger than the anthers of the feeding stamens, although anatomically similar. There was a difference in the amount of pollen produced by the anthers of the two cycles, but no difference was found in pollen viability. Considering a bee color vision model, the color of the anthers of the pollinating stamens contrasted less with that of the corolla, and thus is probably less attractive to visitors. Conversely, the anthers of the feeding stamens and the ventral appendage of the connective of the pollinating stamens contrasted more with the corolla, presenting the same color to the pollinators. These results are in accordance with the idea of division of labor among anthers of heterantherous flowers, especially regarding the quantity of pollen and the color of the floral parts.
  • Functional specialization and phenotypic generalization in the pollination system of an epiphytic cactus Articles

    Martins, Cristiane; Freitas, Leandro

    Abstract in English:

    ABSTRACT Plant-pollinator interactions range from obligatory specialists to facultative generalists, and floral morphology and pollination system may not match completely. The floral biology, reproductive system and floral visitors of a species of the tribe Rhipsalideae were investigated with a focus on the consistency between the pollination system and the floral phenotype. Rhipsalis neves-armondii is an obligate xenogamous species, due to self-sterility. Its flowers are white, small and diurnal, and radially symmetrical. These features, along with their small amount of nectar, characterize the flowers as phenotypic generalists. The most frequent pollinators were a solitary oligolectic species of Andrenidae (Rhophitulus solani), two species of Meliponinae (Trigona spinipes and T. braueri) and Apis mellifera. Despite the generalist floral phenotype, the pollination system is functionally specialized, since only small bees performed effective visits. Flowers of R. neves-armondii may represent a case of cryptic floral specialization in which attributes other than morphology act as filters, restricting them to a single functional group of pollinators. Moreover, the four most frequent species of pollinators cover a spectrum ranging from solitary oligolectic to social polylectic bees, including an exotic species. These results illustrate the distinct dimensions of specialization-generalization that may occur in the pollination process of a single species.
  • Reproductive phenology differs between evergreen and deciduous species in a Northeast Brazilian savanna Articles

    Lacerda, Dinnie Michelle Assunção; Rossatto, Davi Rodrigo; Ribeiro-Novaes, Éville Karina Maciel Delgado; Almeida Jr., Eduardo Bezerra de

    Abstract in English:

    ABSTRACT Evergreen (EG) and deciduous (DEC) species exhibit distinct strategies to overcome dry periods and achieve adequate water status for reproduction and growth. Such particularities may result in distinct reproductive strategies between these groups. Thus, we evaluated the phenology of EG and DEC groups, comparing and differentiating their reproductive phenophases in an area of Brazilian savanna (cerrado sensu stricto), located in Mirador State Park, Maranhão State, by associating these patterns with leaf fall and flushing. Leaf fall, leaf flushing, flowering and fruiting data were monitored between April 2014 and March 2016 for 12 EG and 13 DEC species. To assess differences in flowering and fruiting patterns between EG and DEC, we compared phenological time, activity and intensity, and the duration of phenophases. We found earlier occurrence and longer duration of flowering for EG than for DEC; for fruiting, EG differed from DEC in activity throughout the year, with the intensity being greater for the EG group. These responses may reflect the distinct water-use strategies adopted by the EG and DEC groups, and confirm that differences in their ecophysiological strategies may exert an influence on their reproductive phenology.
  • Genetic diversity of populations of the dioecious Myrsine coriacea (Primulaceae) in the Atlantic Forest Articles

    Paschoa, Roberta Pena da; Christ, Jheniffer Abeldt; Valente, Cecília Silva; Ferreira, Marcia Flores da Silva; Miranda, Fábio Demolinari de; Garbin, Mário Luís; Carrijo, Tatiana Tavares

    Abstract in English:

    ABSTRACT Although a species’ sexual system may influence the genetic diversity of its populations in their natural environment, there have been few such studies involving indigenous species of the Atlantic Forest. Here we study Myrsine coriacea, a dioecious tree widely used in reforestation programs despite a lack of information about its natural interpopulation genetic variation. To address this knowledge gap, intra- and interpopulation genetic diversity were measured for male and female individuals of ten natural populations using ISSR markers. Greater intrapopulation genetic diversity indicated interpopulation gene flow, regardless of isolation and distance between populations. Multivariate analyses detected significant differences in genetic diversity between populations, but not between males and females, which indicates that genetic diversity did not differ between the two sex morphs. Distance between populations was unrelated to genetic diversity. Myrsine coriacea has not experienced a loss of genetic variability despite the characteristic segregated spatial distribution of its populations. These results suggest that obligatory cross-pollination and dispersal by birds may be important mechanisms for the maintenance of genetic diversity in natural populations of M. coriacea.
  • Are native bees and Apis mellifera equally efficient pollinators of the rupestrian grassland daisy Aspilia jolyana (Asteraceae)? Articles

    Maruyama, Pietro K.; Nunes, Carlos E. P.; Vizentin-Bugoni, Jeferson; Gustafsson, Simone; Morellato, Leonor Patricia Cerdeira

    Abstract in English:

    ABSTRACT Most angiosperms rely on animals for pollination, and insects, especially bees, are being the most frequent pollinators. Many native Neotropical plants are frequently visited by the invasive honeybee (Apis mellifera), but its role in the pollination of these plants has been little investigated. We assessed the contribution of various floral visitors, including native bees and the honeybee, on the pollination of a generalist rupestrian grassland daisy, Aspilia jolyana (Asteraceae), in Serra do Cipó, Espinhaço Mountain Range, Brazil. We recorded floral visitors and measured the seed set resulting from one single visitation. We observed a total of 442 visits, mostly by bees, with Bombus pauloensis and Apis mellifera being the most common floral visitors. Other visitors included many other species of bees, flies, hummingbirds, wasps and butterflies. Pollinators significantly increased seed set in comparison to non-visited (bagged) capitula. Moreover, there was no difference among bee species/groups in their contribution to seed set. Thus, A. jolyana benefits from its generalized pollination strategy, and frequent bee visitors, including several native species and the invasive honeybee, are equally effective pollinators for this generalist daisy of rupestrian grasslands.
  • Floral resins of Philodendron adamantinum (Araceae): secretion, release and synchrony with pollinators Articles

    Gonçalves-Souza, Patrícia; Schlindwein, Clemens; Paiva, Elder Antonio Sousa

    Abstract in English:

    ABSTRACT Philodendron is the only genus of Araceae in which resin release occurs in the inflorescence. The resinous secretion adheres to the smooth body surface of the pollinating scarab beetles and allows attachment of pollen grains, making its transport possible. In order to understand the process of resin synthesis and release to the external environment, we used structural, ultrastructural and histochemical analyses at different stages of development of the inflorescences of Philodendron adamantinum. Two types of secretory canals were observed in the spathe: small caliber canals near the abaxial face, and larger caliber canals in the adaxial region. Only the latter canals release secretion into the external environment. The secretory epithelium in these canals is formed by a layer of cuneiform cells, and exhibits secretory activity throughout the development of the spathe. Resin exudation is a peculiar characteristic of these canals and appears to result from pressure exerted by the secretory epithelium and by structural modifications in the wall of cells adjacent to the epidermis, which allow the formation of a separation zone whereby the resin is released. The observed synchrony between anther dehiscence and resin exudation of P. adamantinum enhances the role of this secretion in the pollination process.
  • Breeding system and pollination of Pleroma trichopodum DC. (Melastomataceae): a potential species for the restoration of Atlantic Forest in southern Brazil Articles

    Malucelli, Tiago Simões; Maia, Fabiano Rodrigo; Varassin, Isabela Galarda

    Abstract in English:

    ABSTRACT Plant-pollinator interactions and their reproductive implications are of central importance to the organization of plant populations and communities in restoration areas. We studied the breeding system and flower visitors of Pleroma trichopodum, a pioneer species of the Atlantic Forest. We attempted to answer three questions: (1) Is P. trichopodum dependent on pollinators and mates for reproduction? (2) What are the pollinators of P. trichopodum? (3) Do tree flower-density and flowering-tree density of P. trichopodum enhance the visitation rate of focal trees and their flowers? We tested the breeding system through pollination treatments. We performed focal observations on 10 trees and analyzed the relationship between tree and flower visitation rates, and the tree flower-density and flowering-tree density with Generalized Linear Mixed Models (GLMM). Pleroma trichopodum sets fruits by selfing and outcrossing, both of which occur only through pollinator visits. Bees visited P. trichopodum, and their visitation increased with tree flower-density. Thus, individuals with greater floral displays may function as magnet species, enhancing the pollination of nearby plant species. This characteristic, allied with the ability to reproduce without a mate (selfing) and a tolerance of soggy soils, make P. trichopodum a candidate for Atlantic Forest restoration.
  • Pollination biology of melittophilous legume tree species in the Atlantic Forest in Southeast Brazil Articles

    Pinheiro, Mardiore; Brito, Vinicius Lourenço Garcia de; Sazima, Marlies

    Abstract in English:

    ABSTRACT This study describes the floral phenology and morphology, reproductive biology and pollinators for eight legume tree species, Schizolobium parahyba, Senna macranthera, and Senna multijuga (Caesalpinioideae), as well as Andira fraxinifolia, Lonchocarpus cultratus, Pterocarpus violaceus, Swartzia oblata, and S. simplex (Papilionoideae), in the Atlantic Forest in Southeast Brazil. All the studied species showed an annual flowering pattern, and almost all are of the cornucopia-flowering type, with the only exception being Swartzia oblata, which was of the steady-state type. In general, the legume flowers studied are conspicuous, mostly medium-sized, and offer nectar and/or pollen as a resource. Self-incompatibility associated with the production of many flowers and consequent pollen discounting due to self-pollination may contribute to low fruit set of these species in natural conditions. Fifty bee species were recorded visiting the flowers, with medium to large-sized Apidae bees, such as Bombus morio, and species of Xylocopa, Centridini and Euglossina, which were among the most frequent visitors and major pollinators. These bees showed high floral constancy, thus they are significant to the reproductive success of these tree species. This study provides information regarding the interactions between bees and these eight legume species and evaluates the importance of pollinators for their sexual reproduction.
  • Nectar dynamics and reproductive biology of Passiflora actinia Hook. (Passifloraceae) in Araucaria Forest Articles

    Varassin, Isabela Galarda; Baggio, Ana Carolina; Guimarães, Paulo César; Prazeres, Luiz Carlos; Cervi, Armando Carlos; Bueno, Raquel de Oliveira

    Abstract in English:

    ABSTRACT Nectar production has an important role in pollinator attraction and successful fruit production in many self-incompatible angiosperm groups. The reproductive biology of Passiflora actinia was studied here and related to nectar dynamics. Passiflora actinia presented a temporal segregation of male and female functions at the beginning of anthesis. Due to the movements of floral verticils, the anthers were positioned in a way that favors pollination two hours before the stigmas reached the same position. The nectary consisted of an epidermis with stomata and a parenchyma rich in starch, which was hydrolyzed during anthesis. The nectary organization is probably associated with the continuous production of nectar during anthesis as well as with the high mean nectar concentration. Hand pollination tests indicated that Passiflora actinia is obligately xenogamous, depending on large bees for pollination, specifically the carpenter bee Xylocopa augusti. The continuous production of nectar may increase the number of bee visits, thus favoring pollen flow.
  • How are pollination and seed dispersal modes in Cerrado related to stratification? Trends in a cerrado sensu stricto woodland in southeastern Brazil, and a comparison with Neotropical forests Articles

    Gottsberger, Gerhard; Silberbauer-Gottsberger, Ilse

    Abstract in English:

    ABSTRACT A comprehensive census of a hectare of cerrado s.s. in southeastern Brazil, a small-tree and scrub woodland physiognomy, allowed the evaluation of whether pollination and dispersal modes are correlated with the stratification of the vegetation and if so, in what way. Generalist pollination, and pollination by small bees, as well as ornithophily and anemophily were more frequent in the lower layers (ground and scrub), while species pollinated by large bees and beetles are more or less equally distributed among the ground, scrub and tree layers. The three nocturnal pollination modes, phalenophily, sphingophily, and chiropterophily indicated a preference for the upper layers (tree and scrub). Zoochory predominated in the tree layer, but autochory increased towards the ground at the expense of anemochory and zoochory. We discuss possible reasons for the height distribution of pollination and seed dispersal modes and compare the situation in Cerrado with other Neotropical forests.
  • Trade off between quantity and size of pollen grains in the heterandrous flowers of Senna pendula (Fabaceae) Articles

    Pinheiro-Costa, Bruna Karen; Mesquita-Neto, José Neiva; Rego, Juliana Ordones; Schlindwein, Clemens

    Abstract in English:

    ABSTRACT Heteranthery, the presence of different types of stamens in a flower, may reduce the conflict between pollinators and plants by ensuring the resource for the pollinator without drastically affecting the availability of viable male gametes for fertilization, according to the division-of-labor hypothesis. We investigated whether the poricidal anthers of Senna pendula, a buzz-pollinated heterantherous species, present morphological and physiological differences among pollen grains from the three sets of stamens. We compared quantity, ornamentation, size and fecundity of pollen from long, medium and short stamens. The short feeding stamens produced larger but fewer pollen grains than the long pollinating stamens, which produced smaller pollen grains but in higher quantity. The total pollen volume of pollinating and feeding stamens per flower, however, was the same. The medium stamen produced less-fertile small pollen grains and seems to play no specific role in bee feeding and pollination. Our results indicate differential allocation of pollen for pollinating and feeding stamens mediated by heteranthery. The differences in volume versus quantity of pollen grains fit the division-of-labor hypothesis well for heterantherous pollen-only flowers with poricidal anthers.
  • Pollen has higher water content when dispersed in a tricellular state than in a bicellular state Articles

    Williams, Joseph H.; Brown, Chandler D.

    Abstract in English:

    ABSTRACT Pollen is generally dispersed in a sexually immature and somewhat dehydrated, metabolically quiescent state. Yet, in some species, pollen at anthesis is well-hydrated and metabolically active, and in 30 % of angiosperms pollen is dispersed after having formed its sperm cells. Pollen water content and sexual maturity may be correlated, either because both are subject to trade-offs between dispersal viability and post-pollination performance, or because the traits display developmental linkages. We inferred relative water content of sexually immature (“bicellular”) and sexually mature (“tricellular”) pollen of 30 species of angiosperms using a hydration index (HI) that ranges from zero to one, based on how near fresh pollen volume is to its minimal (dehydrated) or maximal (hydrated) volume. Tricellular pollen had 30 % higher HI than bicellular pollen (P < 0.005), after controlling for initial pollen size (larger pollen had higher HI; P < 0.05). A literature survey of 344 species indicated that the tricellular and hydrated states were strongly associated, although all four trait state combinations were present (P < 0.0001). Our results suggest that a common mechanism for the repeated origins of tricellular pollen has been via the loss of controlled pollen dehydration, which enables either accelerated or extended pollen development.
  • Pollinator availability, mating system and variation in flower morphology in a tropical savanna tree Articles

    Rech, André Rodrigo; Jorge, Leonardo Ré; Ollerton, Jeff; Sazima, Marlies

    Abstract in English:

    ABSTRACT Widely distributed organisms face different ecological scenarios throughout their range, which can potentially lead to micro-evolutionary differentiation at specific localities. Mating systems of animal pollinated plants are supposed to evolve in response to the availability of local pollinators, with consequent changes in flower morphology. We tested the relationship among pollination , mating system, and flower morphology over a large spatial scale in Brazilian savannas using the tree Curatella americana (Dilleniaceae). We compared fruit set with and without pollinators in the field, and analyzed pollen tube growth from self- and cross-pollinated flowers in different populations. Populations with higher natural fruit set also had lower fruit set in bagged flowers, suggesting stronger barriers to self-fertilization. Furthermore, higher levels of autogamy in field experiments were associated with more pollen tubes reaching ovules in self-pollinated flowers. Morphometric studies of floral and leaf traits indicate closer-set reproductive organs, larger stigmas and smaller anthers in populations with more autogamy. We show that the spatial variation in mating system, flower morphology and pollination previously described for herbs also applies to long-lived, perennial tropical trees, thus reemphasizing that mating systems are a population-based attribute that vary according to the ecological scenario where the plants occur.
  • Flower trade-offs derived from nectar investment in female reproduction of two Nicotiana species (Solanaceae) Articles

    Galetto, Leonardo; Araujo, Francielle Paulina; Grilli, Gabriel; Amarilla, Leonardo D.; Torres, Carolina; Sazima, Marlies

    Abstract in English:

    ABSTRACT Animal-pollinated flowers may orient resources for competing activities, such as nectar production for attracting flower visitors but then saving nectar (through inhibiting nectar production or by final resorption) for the subsequent maturation of fruits and seeds. Nectar production is continuous in Nicotiana longiflora and N. alata after flower opening, but early nectar removal reduces total secreted nectar. Resource trade-off between nectar investment and seed production were experimentally assessed in manually pollinated flowers experiencing different numbers of repeated nectar removals, while controlling for maternal effects. We expected that flowers with less nectar secretion produce larger seed sets. The results showed that for both species the earlier the nectar removal during flower anthesis, the lower the total nectar secreted and the higher the mass of seeds produced. This general pattern was clearer for N. longiflora. The link between decreased nectar production and the subsequent increase in the seed set implies that resources are limited. Consequently, nectar savings during the pollination process through early nectar removal by pollinators can be interpreted as a trade-off between resources secreted by flowers for pollinator attraction and those utilized during fruit and seed maturation.
  • Nectar ecology of the endemic epiphytic hummingbird-pollinated bromeliad Vriesea altodaserrae: secretion dynamics and pollinator visitation pattern Article

    Nunes, Carlos E. P.; Briet, Joseildo; Galetto, Leonardo; Sazima, Marlies; Amorim, Felipe W.

    Abstract in English:

    ABSTRACT Hummingbirds are the main pollinators of most bromeliad species, whose nectar traits usually respond to the selective pressures imposed by pollinators. Considering the specialization of hummingbird-pollinated bromeliads, we expect a close relationship between nectar ecophysiology and the needs of the main pollinators. In this sense, we studied the nectar ecology of the endemic epiphytic bromeliad Vriesea altodaserrae by assessing its nectar traits to address the following questions: i) do flowers respond to successive experimental removals of nectar? ii) is hummingbird visitation frequency related to nectar secretion pattern? We found that V. altodaserrae depended completely on hummingbirds for sexual reproduction, and nectar composition was consistent with that of most hummingbird-pollinated species. Most of the nectar was secreted at bud stage and, if not removed, flowers reabsorb it at the end of their lifespan. Total nectar production did not change after successive removals, and nectar secretion rhythm did not affect the frequency of hummingbird visits. Vriesea altodaserrae was visited by two-thirds of the hummingbird species recorded at the study site, but especially by those of Trochilinae subfamily, suggesting specialization for this group of hummingbirds and highlighting the importance this endemic bromeliad as a keystone species in areas of highland Atlantic forest.
  • Reproductive phenology and germination of Eleocharis laeviglumis R. Trevis. & Boldrini (Cyperaceae) Articles

    Demeda, Camila Luisa Bernhardt; Seger, Guilherme Dubal dos Santos; Steiner, Neusa; Trevisan, Rafael

    Abstract in English:

    ABSTRACT Aquatic macrophytes are important components of freshwater ecosystems, of which Cyperaceae is the most diverse family. Many species of Cyperaceae form dense populations along lake margins of the southern coast of Brazil, but little is known about their sexual reproductive strategies. We characterized the reproductive life cycle of Eleocharis laeviglumis, an abundant emergent macrophyte of coastal wetlands in southern Brazil, by assessing its reproductive phenophases and estimating the number of its flowers and potentially viable fruits per inflorescence in a natural population. We also tested seed germinability and vigor for a period of four months during a single reproductive season. The species possesses dichogamous and protogynous spikelets with an average duration of 34 days (pre-anthesis, 1.7 d; anthesis, 6.9 d; fruit maturation, 22.3 d; fruit dispersion, 3.2 d). More than half of the flowers (62.2 %) developed into fruits, while only 5.5 % of the seeds germinated. Germinability and vigor decreased during the reproductive season. Some culms probably originate from asexual reproduction or sexual reproduction of clones. For restoration purposes, we suggest that E. laeviglumis should be propagated by sowing seeds collected at the beginning of the reproductive season, along with the transplantation of rhizomes.
  • Pollination of Peltogyne chrysopis: an endemic tree of the Atlantic Forest Articles

    Souza, Isys Mascarenhas; Funch, Ligia Silveira; Queiroz, Luciano Paganucci de

    Abstract in English:

    ABSTRACT Peltogyne chrysopis is an arboreal legume endemic to the Atlantic Forest and known only from the state of Bahia, Brazil. Focal observations were made of anthesis, pollen availability, stigma receptivity, nectar production, and the presence of osmophores and UV-reflective pigments for the species. Floral visitors were also observed and classified based on the timing and frequency of their visits and their foraging behavior. The breeding system was inferred from the pollen-ovule ratio and pollen tube growth after pollination treatments. Peltogyne chrysopis was found to be melittophilous, with anthesis occurring from 02h00min to 05h00min, and protogynous and xenogamous, with flower scent emission and pollen release before sunrise. Xenochlora nigrofemorata was the main pollinator, as it effectively collected and transferred pollen grains. Nectar production appears to be a secondary resource to ensure the attraction of a diversity of floral visitors and potential pollinators in the absence of effective pollinators. The results of the present study contribute to understanding the pollination mechanisms of Peltogyne, a genus that has been neglected with regard to its reproductive mechanism, and documents, for the first time, the role of the bee genus Xenochlora in plant pollination.
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