Secondary Pollen Presentation Research Articles

Compensating for the corolla? Pollen exposure is not associated with pollen collecting hair length.

Secondary pollen-presentation, the relocation of pollen from the anthers to elsewhere on the flower, has evolved multiple times across many plant families. While hypotheses suggest it evolved to promote outcrossing, a byproduct of relocation may be protection of pollen from loss due to abiotic factors. In Campanulaceae pollen is presented on pollen-collecting hairs along the style and the hairs retract over time and release pollen for transfer. Campanulaceae taxa vary in the degree to which pollen is exposed to environmental factors due to variation in the corolla shape and size. We tested the protective function of pollen-collecting hairs by assessing whether there was a tradeoff between the protection provided by the corolla and the pollen-collecting hairs. We used phylogenetic comparative methods to test for associations between pollen-collecting hair length, floral shape and size metrics, and pollen exposure traits across 39 species. We anticipated longer pollen-collecting hairs in taxa with more exposed pollen presentation but found there was no relationship between estimates of pollen exposure and pollen-collecting hair length. However, pollen-collecting hair length scaled allometrically with floral size, and variation in pollen-collecting hairs, as well as most floral traits, was phylogenetically structured. These results indicate that variation in pollen exposure across species does not structure variation in the pollen-collecting hairs, rather hair length scales allometrically and is phylogenetically constrained, therefore pollen-collecting hairs are unlikely to facilitate protection from environmental pressures.

Biphyly of the genus Wendlandia and establishment of a new tribe Clavistigmateae and a new genus Clavistigma of Rubiaceae from Asia

AbstractWendlandia, as currently circumscribed, is a genus of Rubiaceae comprising about 90 species mainly in tropical and subtropical Asia. By sampling species from all four series (Clavigerae, Euexsertae, Montigenae, Subinclusae) and all tribes in the subfamily Dialypetalanthoideae, we examined the monophyly of Wendlandia based on phylogenetic reconstruction using the nuclear ribosomal internal transcribed spacer and four plastid DNA regions. Wendlandia was resolved as biphyletic, consisting of two distantly related lineages that correspond to the monotypic series Clavigerae (Wendlandia pendula), sister to the Chinese endemic genus Trailliaedoxa, and a clade containing the remainder sampled members of Wendlandia. Based on the isolated phylogenetic position of W. pendula and its unique morphological characteristics compared to the recognized tribes of the Vanguerieae alliance, we herein erect a new monotypic genus, Clavistigma, and a new tribe, Clavistigmateae to accommodate the unique species. The secondary pollen presentation and the unique seed morphology were firstly described for the species. The divergence time between Clavistigma and Trailliaedoxa was dated back to 13.8 mya, coinciding with the climate change in northwestern Yunnan driven by the uplift Tibet Plateau and the river incision in the Hengduan Mountains during the Miocene and Late Pliocene.

Reproductive biology of Santolina ligustica Arrigoni, a rare narrow-ranged species: implications for conservation

Abstract Santolina ligustica is a rare narrow-ranged species endemic to Liguria (Italy) for which a likely trend of decline has been recorded. For this reason, it would be important to assess the reproductive biology of this endemic species. In this study, we investigated the plant–pollinator interactions, the reproductive mode of the plant, and we evaluated both reproductive efficiency and seeds’ germination performances. Santolina ligustica is an obligate cross-pollinating species with a generalist pollination system. The most frequent insects are Coleoptera belonging to the genus Oedemera. Seed set is low, but the seeds germinate under a wide range of temperatures. Taken together, our results indicate that S. ligustica is an insect pollinated and self-incompatible plant, in which low visitation rate, secondary pollen presentation and/or lack of compatible mate may cause a low seed set per capitulum. Nevertheless, the high number of capitula per plant and the high percentage of germination may assure high number of seedlings. Thus, the survival of S. ligustica is probably threatened by other factors such as fragmented distribution and habitat reduction because of land-use change. Under this scenario, we proved that species’ decline is not directly related to reproductive failure and different studies are desirable to provide suggestions for the species conservation.

Gradual pollen presentation in Vaccinium corymbosum 'Bluecrop': an adaptive mechanism to improve pollination efficiency and outcrossing.

Gradual pollen presentation is a plant reproductive mechanism to improve pollination efficiency and accuracy and promote outcrossing. Vaccinium corymbosum 'Bluecrop' has a typical gradual pollen presentation mechanism. 'Bluecrop' exhibits an inverted bell-shaped flower with a white coloration. By investigating the flower syndrome, pollination characteristics, pollination efficiency, and breeding system of 'Bluecrop', this study aims to explore the adaptive significance of these traits. The results showed 'Bluecrop' released pollen gradually through anther poricidal dehiscence. Among different pollinators, Apis mellifera and Bombus can pollinate effectively, and the mechanism of gradual pollen presentation significantly improved the efficiency of pollen transfer. This characteristic limits the amount of pollen removed by the pollinators and prolongs pollen presentation, thus attracting more pollinators and thereby increasing male fitness. The nectar secretion of 'Bluecrop' is gradual, with a large nectar production and a long phase of nectar secretion, enhance visitation frequencies and the chances of successful pollination. At the same time, campanulate corolla can protect pollen as well as nectar from waste due to environmental factors and other effects. The breeding system of 'Bluecrop' relies mainly on outcrossing because of its low affinity for self-fertilization and good interaction with pollinating insects. Thus, the special floral syndrome and the mechanism of secondary pollen presentation are significant in improving pollination efficiency and promoting the reproductive success of 'Bluecrop' by outcrossing. It can provide a certain theoretical basis for the future propagation breeding of 'Bluecrop'.

Secondary pollen presentation: More than to increase pollen transfer precision

AbstractPollination precision and efficiency have been deemed to be important driving forces in floral evolution. Herkogamy reduction is a main mechanism to increase pollination precision. Secondary pollen presentation (SPP), by which pollen is presented on other floral organs especially pistils, has been widely accepted as a special mechanism to increase pollen transfer precision through spatial reduction of the anther–stigma distance, that is, minimized herkogamy. This overlooks a potential driving force, that is expanding the pollination niche through converting pollen thieves and nectar robbers into effective pollinators. We selected two species as study models with typical pistillate SPP, Pavetta hongkongensis Bremek. (Rubiaceae) and Scaevola taccada (Gaertn.) Roxb. (Goodeniaceae). In both species, two distinct pollinator functional groups were recognized. Short‐tongued bees and flies fed on pollen on stigmas but also stole pollen from anthers and robbed nectar, whereas long‐tongued hawkmoths and butterflies only collected nectar. Emasculation had no influence on long‐tongued pollinators, but significantly decreased the visitation frequency of short‐tongued visitors and fruit set, compared to intact flowers, demonstrating short‐tongued visitors did not effectively pollinate and acted merely as pollen thieves or nectar robbers when SPP was absent. Data from the two plant species clearly indicated pistillate SPP has additional adaptive advantages of converting ineffective visitors into pollinators and consequently widening the pollination niche, which could help plants overcome environmental stochasticity. Our results suggest that multiple selective forces drive the evolution of SPP and the minimization of herkogamy.

Pollination biology and breeding system of Desmodium grahamii (Fabaceae, Papilionoideae): functional aspects of flowers and bees

This study aims to understand the role of floral traits in determining the pollination and reproduction of Desmodium grahamii (Fabaceae, Papilionoideae) with explosive floral mechanism in populations occurring in a natural reserve and botanical garden in southern Mexico City. We assessed the breeding system by quantifying floral and pollinator activity, compatibility, pollination, and reproductive success, assisted by field and laboratory analyses. Results showed that cross-pollination and self-pollination coexist, but bees are required for fruit and seed set. Flower colour is the primary attractant. Floral scent is also likely important because the petals were covered with papillae, although no scent was perceptible. Morphological and functional observations of D. grahamii exhibit simultaneous pollen release and stigma receptivity when the flower is activated by a pollinator and there is no secondary pollen presentation; this contrasts with what has been reported on other species of Desmodium. Pollen is the pollinators’ only reward, and its deposition and collection must be done synchronically, occurring when a bee lands and introduces its proboscis in the flower. In this study, we identified seven floral visitors: five bee pollinators and two syrphid flies as pollen thieves. On some occasions, Apis mellifera also behaves as a pollen thief. Fruit and seed set of flowers that were isolated from visitors may indicate a delayed pollination mechanism. Pollination results also suggest that Apis bees and syrphid flies may contribute to fruit and seed production when they forage on flowers at post-anthesis.

Elaborated pollen packaging and dispensing mechanism induced by petal architecture from a Papaveraceae species.

Secondary pollen presentation (SPP) is a reproductive strategy that enhances the efficiency of pollen transfer, which has been explored for more than 200 years, resulting in 10 identified types of SPP. The ephemeral plant Hypecoum erectum L. (Papaveraceae) has an elaborate petal structure. The middle lobe is a key functional organ in SPP. To explore the importance of the middle lobe structure, we measured the flowering process, the curling movement and growth of the middle lobe, pollination characteristics, pollination efficiency, and the mating system in H. erectum in the field. The yellow middle lobe structure had an important role in attracting pollinators. The middle lobes on the inner petals function as a redundant cucullate structure and wrapped about 84% of the total pollen grains as soon as the anthers dehisced. These then grew upward and gradually presented pollen to pollinators via the roll out of the middle lobes. One bee species, Colletes vestitus from Colletidae, was the only effective pollinator of H. erectum. The SPP mechanism increased the efficiency of pollen transfer by C. vestitus. The middle lobes, which wrapped pollen and grew upward, contacted the stigma and provided an advantage for self-pollination and outcrossing by growing upward higher than the corolla. Hypecoum erectum L. has a mixed mating system with selfing and outcrossing. Thus, the SPP mechanism plays a key role during the pollination process and is necessary for improving pollination efficiency and promoting reproductive success.

Dynamics of secondary pollen presentation in Campanula medium (Campanulaceae).

After several decades of research, dynamics and patterns of mating system in floral evolution remain incompletely understood, especially with regards to strategies that combine both outcrossing and selfing, as frequently recorded in the genus Campanula. Data about temporal and spatial dynamics of secondary pollen presentation are still scarce in literature: we investigated them using Campanula medium (Campanulaceae) as case study. Experimental pollinations were conducted under natural conditions, to characterise the breeding system of this species. Effects on stigma opening and stigma receptivity of stylar pollen presence were investigated in manipulated flowers. The temporal dynamics and fitness of male and female functional phases were estimated. Flower visitors and their interactions with sexual parts of the flower were also annotated. C. medium is xenogamous and self-incompatible, with a clear temporal separation between sexual functional phases. Floral lifespan is shortened by experimental outcrossing. Removal of pollen from the style shortened the time span of male function. Pollen viability was highest at the beginning of the anthesis, decreasing during the flowering period, whereas stigmatic receptivity shows an opposite trend. We found a severe pollen limitation in the studied population. Bees were the most frequent floral visitors. In some of these insects we observed stereotyped interactions with the reproductive structures of the flower, in particular with the pollen, exposed along the upper and median portion of the style. Sexual phases in C. medium are inversely correlated and finely spatially and temporally coordinated, since stigma maturation is scalar along its length and depends on pollen presence on the style. Overall, our findings push forward the knowledge on reproductive strategies in Campanula.

Secondary pollen presentation and foral traits of Heliconia psittacorum

The secondary presentation of pollen consists of a foral mechanism where the presentation of pollen occurs in other foral structures in addition to the anther, in order to increase the precision of the dispersion of the pollen by the vectors. This study aims to describe the temporal dynamics of secondary pollen presentation, and morphological and morphometric characteristics in stages of pre- anthesis and anthesis in genotypes of fve natural Heliconia psittacorum populations. For the study of foral morphometry traits of length of the fower, stamen, stigma and height of flament insertion in the petal in bud and fower were measured. The foral morphology of pre-anthesis buds and fowers in anthesis, the presence or absence of characteristics such as herkogamy, region of flament insertion in the petal, region of stylar hairs, and of secondary pollen deposition were evaluated. Treatments of controlled pollinations, self-pollination, geitonogamy, cross-pollination, natural pollination and growth to pollen tube were sampled. Floral herkogamy and pollen transfer to the adhered hairs in the stylar region were clearly observed during anthesis, constituting the frst record of occurrence of secondary pollen presentation in Heliconiaceae. Pollen tube growth was inhibited in the stigmatic, style and basal regions of the pistil. Natural fruiting produced little or no fruit. The positioning of the stamens above the stigma, pollen viability and stigma receptivity during anthesis of H. psittacorum fowers may favor self-pollination. The stylar hairs observed in all H. psittacorum populations’ help in the retention of pollen grains. The low fruiting rate in controlled and natural pollinations suggest that the main propagation form of H. psittacorum in the study areas is based on asexual reproduction.

Pollination ecology of Synedrella nodiflora (l.) Gaertn. (Asteraceae)

Synedrella nodiflora (L.) Gaertn grows almost throughout the year if the soil is damp. It produces heterogamous capitula with female ray florets anthesing first day and bisexual disc florets anthesing on the next three consecutive days. Disc florets are dichogamous, herkogamous, self-compatible, self-pollinating (vector-mediated) and display secondary pollen presentation through an intermediate form of brush mechanism. Ray and disc florets exhibit facultative xenogamy. Butterflies are principal pollinators while bees, wasps and flies are supplementary pollinators. Thrips, Microcephalothrips abdominalis uses the florets as breeding and feeding sites; the feeding activity effects pollination. The ray and disc florets produce cypselas; the cypselas produced by ray florets are heavier, elliptical, membranous with upwardly-pointing teeth along the margins and 2 short terminal awns while those produced by disc floret are lighter, cylindrical and tangentially compressed with 2 or 3 stiff terminal divaricate awns. Seed dispersal is polychorous and represented by anemochory, anthropochory, zoochory and ombrohydrochory. Cypselas of ray florets disperse to short distances and germinate germinate under specific germination conditions either at parental sites or in similar habitats while those of disc florets disperse farther away from parental sites and germinate readily under a wide range of conditions. Therefore, bimorphic cypselas with different germination abilities enable the plant to grow as a widespread weed but not as an invasive weed.

Secondary pollen presentation on anther hairs enhances reproductive fitness in Brandisia hancei, a protogynous perennial with autonomous selfing

ABSTRACTBackground: Secondary pollen presentation (SPP) is a phenomenon where pollen is relocated from within the anthers to other floral structures for presentation.Aims: We report a new mechanism of androecial SPP on anther hairs, which is involved in increasing reproductive fitness in Brandisia hancei.Methods: The morphological change of anther hairs during floral ageing was recorded, and pollen grains were quantified after anther hair removal to clarify the roles played by hairs in pollen retention. Additionally, fruit set and seed set were assessed to investigate the efficiency of anther hairs to reproductive success.Results: Young flowers of B. hancei showed approach herkogamy, while autonomous selfing was achieved by changes in relative positions of the stigma and anthers during floral ageing. In B. hancei, anthers developed characteristic hairs of epidermal origin, and hairs originated along the furrow between the paired pollen sacs and were used for SPP after anther dehiscence. Anther hairs increased pollen retention by over 70% in later floral-age stages, and seed set decreased by about 30% after anther hairs had been removed.Conclusions: In the process of autonomous selfing, SPP on anther hairs enhances both the male and female functions of the flowers of B. hancei.

SECONDARY POLLEN PRESENTATION, PSYCHOPHILY AND ANEMOCHORY IN Lagascea mollis Cav. (ASTERACEAE)

Information on pollination ecology and seed dispersal aspects is essential to understand sexual reproduction in Lagascea mollis Cav. The study was aimed at providing details of pollen presentation system, pollination syndrome, pollinators and seed dispersal mode for L. mollis based mostly on field study. Paper chromatography technique was used for recording sugar and amino acid types in the nectar, since they are important to evaluate the pollination syndrome. The study indicated that L. mollis flowers during August-November. The plant produces synflorescences consisting of several capitula. Each capitulum produces a single disc floret. The plant is protandrous, temporally dioecious and exhibits secondary pollen presentation using brush mechanism to prevent autonomous selfing. The floral characteristics such as having synflorescence, narrow tubular corolla, production of sucrose-rich nectar with essential and non-essential amino acids and pollen charactersistics such as having spherical shape, tri-colpate apertures and strongly spinulose exine suggested that the plant is adapted for insect pollination. The plant is principally psychophilous. Other insects also visited the florets opportunistically and acted as supplementary pollinators. Further, thrips used this plant as breeding and feeding sites; their effect mostly geitonogamy. The fruit is an achene, anemochorous and also anthropochorous. Regeneration occurred from seeds and perennial root stock during rainy season.

Floral morphology and anatomy of Ophiocaryon, a paedomorphic genus of Sabiaceae.

Ophiocaryon is a lesser known genus in Sabiaceae. This study examines flowers of six Ophiocaryon species in comparison with Meliosmaalba, to identify taxonomically informative characters for understanding relationships within the family Sabiaceae, to imply previously unknown pollination mechanisms of Ophiocaryon, and to contribute to the placement of Sabiaceae within the early-diverging eudicots. Floral morphology and anatomy of six Ophiocaryon species and M. alba were studied and described using scanning electron microscopy, clearing techniques and resin sectioning. Novel characters of Ophiocaryon were identified, e.g. conical cells on petals, different kinds of orbicules in anthers, stomata on nectary appendage tips and ovary, two distinct surface patterns on stamens and ovary, tanniferous cell layers in the ovary wall, and acorn-shaped unitegmic ovules with very short integuments. Comparison of floral characters between Ophiocaryon and Meliosma found that the calyx, corolla, androecium and gynoecium of Ophiocaryon resemble an undeveloped state of the latter taxon, reflecting a paedomorphic regression of the flower of Ophiocaryon. The flower morphology and anatomy of Ophiocaryon was compared with its putative sister species M. alba, but no clear shared derived characters could be detected. Moreover, the findings of scent, presence of conical cells on petals and a nectary suggest flowers are pollinated by small insects with a secondary pollen presentation on the cupula of fertile stamens. We found that Ophiocaryon may be derived from ancestors that were similar to extant Meliosma in their flower structure and pollination mechanism. However, the lack of shared derived characters between Ophiocaryon and its phylogenetic sister group M. alba is puzzling and requires further investigations on the diversity of the latter species.

Comparing the efficiency of pollination mechanisms in Papilionoideae

The pump pollination mechanism is typical of basal clades within Papilionoideae and might be associated with less efficient pollen transfer systems, while the explosive tripping mechanism is considered more advanced and might represent the highest expression of the trend in pollen economy. Crotalaria pumila, C. stipularia, Desmodium incanum and D. subsericeum present secondary pollen presentation with pump and explosive pollination mechanisms, respectively. In the present study, we evaluate and compare (1) pollen removal, (2) pollen deposition and (3) pollen transfer efficiency of both mechanisms, considering single visits by Megachile spp., common pollinators of the four plant species in Salta Province, Argentina. Comparisons of visit durations are made in relation to the type of mechanism and rewards offered. We detected significant differences between both mechanisms in the proportion of pollen grains removed and deposited in a flower after a single visit of Megachile. We found that efficiency in pollen transfer was significantly higher for explosive mechanism (2.13 ± 0.42 pollen grains deposited per 100 removed) than for pump mechanism (0.33 ± 0.17 pollen grains deposited per 100 removed). This is the first study that compares efficiency between pollination mechanisms in this group of plants.

Three psychophilous Asteraceae species with distinct reproductive mechanisms in southeastern Brazil

ABSTRACTThe Asteraceae have a high diversity of reproductive mechanisms, as shown by studies conducted mainly with species from temperate regions. Aiming to contribute knowledge on the reproduction of tropical species, we compared the floral biology and breeding systems of the co-occurring species Adenostemma brasilianum, Bidens segetum and Grazielia intermedia, and additionally identified their pollinators. The study was conducted in a seasonal semideciduous forest fragment in southeastern Brazil. Florets opened in early morning and were protandrous. In the first day of anthesis, secondary pollen presentation occurred during the staminate phase, mainly in the morning. In the same day, the pistillate phase began, being long in A. brasilianum and B. segetum (up to 4 days) and short in G. intermedia (1 day). Pollen viability was high in all three species, except for two G. intermedia individuals which showed male sterility, thus characterising a gynodioecious population. Self-compatibility was observed in A. brasilianum and self-incompatibility in B. segetum. In G. intermedia, besides sexual reproduction, apomixis was also observed. This is the first report of apomixis in the genus Grazielia. Although the studied species show distinct reproductive mechanisms, all of them benefitted from cross-pollination, which was mostly done by butterflies.

Pollination ecology and fruiting behavior of Pavetta indica L. (Rubiaceae), a keystone shrub species in the southern Eastern Ghats forest, Andhra Pradesh, India

Pavetta indica is a massive bloomer for a brief period in May. The flowers are hermaphroditic, strikingly protandrous, self and cross-compatible, nectariferous and psychophilous. They possess secondary pollen presentation mechanism as a device to avoid autonomous autogamy but it does not prevent geitonogamy. The fruit set largely occurs through geitonogamy and xenogamy. Butterflies, especially papilionids, pierids, nymphalids, and sphingid hawk moth pollinate the flowers while collecting nectar. Honey bees and blue-banded digger bees feed on pollen and effect only accidental pollination. The nectar is sucrose-rich and contains essential and non-essential amino acids. Birds are seed dispersal agents. Seeds are non-dormant and germinate readily during rainy season but their continued growth and establishment is subject to the availability of soil moisture and nutrients. The plant is not able to populate itself in its natural area. The local uses of different parts of the plant have been found to be affecting its reproductive success and natural regeneration rate. Therefore, regulation of the uses of this plant is recommended for its survival and restoration of its population size in the natural areas due to its role as a keystone species for bees and butterflies during dry season.

A global perspective on Campanulaceae: Biogeographic, genomic, and floral evolution.

The Campanulaceae are a diverse clade of flowering plants encompassing more than 2300 species in myriad habitats from tropical rainforests to arctic tundra. A robust, multigene phylogeny, including all major lineages, is presented to provide a broad, evolutionary perspective of this cosmopolitan clade. We used a phylogenetic framework, in combination with divergence dating, ancestral range estimation, chromosome modeling, and morphological character reconstruction analyses to infer phylogenetic placement and timing of major biogeographic, genomic, and morphological changes in the history of the group and provide insights into the diversification of this clade across six continents. Ancestral range estimation supports an out-of-Africa diversification following the Cretaceous-Tertiary extinction event. Chromosomal modeling, with corroboration from the distribution of synonymous substitutions among gene duplicates, provides evidence for as many as 20 genome-wide duplication events before large radiations. Morphological reconstructions support the hypothesis that switches in floral symmetry and anther dehiscence were important in the evolution of secondary pollen presentation mechanisms. This study provides a broad, phylogenetic perspective on the evolution of the Campanulaceae clade. The remarkable habitat diversity and cosmopolitan distribution of this lineage appears to be the result of a complex history of genome duplications and numerous long-distance dispersal events. We failed to find evidence for an ancestral polyploidy event for this clade, and our analyses indicate an ancestral base number of nine for the group. This study will serve as a framework for future studies in diverse areas of research in Campanulaceae.

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Loss of YABBY2-Like Gene Expression May Underlie the Evolution of the Laminar Style in Canna and Contribute to Floral Morphological Diversity in the Zingiberales

The Zingiberales is an order of tropical monocots that exhibits diverse floral morphologies. The evolution of petaloid, laminar stamens, staminodes, and styles contributes to this diversity. The laminar style is a derived trait in the family Cannaceae and plays an important role in pollination as its surface is used for secondary pollen presentation. Previous work in the Zingiberales has implicated YABBY2-like genes, which function in promoting laminar outgrowth, in the evolution of stamen morphology. Here, we investigate the evolution and expression of Zingiberales YABBY2-like genes in order to understand the evolution of the laminar style in Canna. Phylogenetic analyses show that multiple duplication events have occurred in this gene lineage prior to the diversification of the Zingiberales. Reverse transcription-PCR in Canna, Costus, and Musa reveals differential expression across floral organs, taxa, and gene copies, and a role for YABBY2-like genes in the evolution of the laminar style is proposed. Selection tests indicate that almost all sites in conserved domains are under purifying selection, consistent with their functional relevance, and a motif unique to monocot YABBY2-like genes is identified. These results contribute to our understanding of the molecular mechanisms underlying the evolution of floral morphologies.

A New Secondary Pollen Presentation Mechanism from a Wild Ginger (Zingiber densissimum) and Its Functional Roles in Pollination Process.

Background and AimsSecondary pollen presentation (SPP), a floral mechanism of reproductive adaptation, has been described for more than 200 years, with nine types SPP recorded. However, few studies have been done experimentally to link the floral mechanism of SPP to its functional roles in pollination process. This study aims to describe a new SPP mechanism from a wild ginger (Zingiber densissimum, Zingiberaceae) and explore how the pollen arrangement of SPP affects pollen removal during the interaction with different pollinators.Methodology/Principal FindingsField observations and experiments revealed that flowers lasted for less than one day. The breeding system was partially self-incompatible. Two bee species, Macropis hedini (which carried pollen dorsally) and Amegilla zonata (which carried pollen ventrally) were the primary pollinators. About a third of pollen grains were relocated from the anther to the labellum staminode of flowers through the adherence of aggregated pollen chains, while other grains were presented on the anther. In a single visit, each bee species removed pollen grains from both the labellum staminode and the anther. Macropis hedini was more effective than Amegilla zonata.Conclusions/SignificanceOur study describes a new SPP mechanism in angiosperms. The new SPP mode enables pollen grains presented on the anther and the labellum staminode simultaneously via the adherence of aggregated pollen chains, thus promoting pollen to be taken away by different pollinators. This SPP mechanism plays a key role during pollen removal and may have evolved under the pressure to improve male fitness.