Pollen Presentation Research Articles

1015. INULA RHIZOCEPHALA: Compositae

SummaryInula rhizocephala Schrenk (Compositae: Inuleae: Inulinae) is described and illustrated, together with a commentary on the discovery of Kew's current plant stock. Notes on cultivation, propagation, pests and diseases and availability are provided. It is highly likely that I. rhizocephala is an annual or biennial, or possibly a short‐lived perennial, since no perennating rootstock has been retained in either pot grown or Rock Garden plantings at Kew. The position of Inula rhizocephala in the genus, and within the tribe Inuleae subtribe Inulinae, is discussed. The author citation of the binomial Inula rhizocephala is also discussed as is the type material of I. rhizocephaloides, a synonym of I. rhizocephala, and aspects of the pollen presentation in the disc florets.

Flower orientation influences floral temperature, pollinator visits and plant fitness.

Effective insect pollination requires appropriate responses to internal and external environmental cues in both the plant and the pollinator. Helianthus annuus, a highly outcrossing species, is marked for its uniform eastward orientation of mature pseudanthia, or capitula. Here we investigate how this orientation affects floral microclimate and the consequent effects on plant and pollinator interactions and reproductive fitness. We artificially manipulated sunflower capitulum orientation and temperature in both field and controlled conditions and assessed flower physiology, pollinator visits, seed traits and siring success. East-facing capitula were found to have earlier style elongation, pollen presentation and pollinator visits compared with capitula manipulated to face west. East-facing capitula also sired more offspring than west-facing capitula and under some conditions produced heavier and better-filled seeds. Local ambient temperature change on the capitulum was found to be a key factor regulating the timing of style elongation, pollen emergence and pollinator visits. These results indicate that eastward capitulum orientation helps to control daily rhythms in floral temperature, with direct consequences on the timing of style elongation and pollen emergence, pollinator visitation, and plant fitness.

Floral anatomy, embryology, seed, and fruit development in Cephalanthus (Naucleeae-Rubiaceae), with emphasis on C. glabratus.

Information on the reproductive anatomy in genera of the tribe Naucleeae, particularly Cephalanthus, is scarce and fragmented. Of the six species in the genus, only the mature megagamethophyte of Cephalanthus occidentalis has been described. This study aims to provide information on embryological aspects in flowers of C. glabratus and to analyze the morphology and anatomy of the flowers, fruit, and seed in the six species of the genus. Cephalanthus glabratus have imperfect flowers: pistillate (PF) and staminate (SF). In the PF, the ovules are functional, while in the SF, they atrophy during the formation of the embryo sac. The mature ovule has a single integument, corresponds to the Phyllis type and the embryo sac is a Polygonum type, forming only in the PF. The presence of pollenkitt and secondary presentation of pollen were observed in the SF, as well as in the pollen formation previously described, whereas in the PF, they are absent, due to the collapse of the pollen grains inside the indehiscent anthers. The analysis of the ontogeny of the ovular excrescence in C. glabratus determined its funicular origin, calling it an aril. Its development is a pre-anthesis event, initiated during megasporogenesis. In seeds, the aril is a fleshy, white appendage which almost completely envelops the seeds of Cephalanthus, except for Cephalanthus natalensis where it is noticeably more reduced. Studies of the fruit in Cephalanthus species indicate that the infructescence is a dry schizocarp which separates into uni-seminated mericarps, except in C. natalensis that has fleshy indehiscent fruit.

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.

Reproductive and pollination biology of the Critically Endangered endemic Campanula vardariana in Western Anatolia (Turkey)

Background and aims – Campanula vardariana (Campanulaceae) is a critically endangered endemic chasmophyte with a single population situated in the west of Turkey. Very little is known about the reproductive biology of C. vardariana and more information is needed to develop a sound conservation strategy for this endemic species.Material and methods – Floral traits such as flower morphology, nectar, and sugar concentration, as well as pollen viability and stigma receptivity were measured in different floral phases. We observed insect visitations to the flowers and identified pollinators. Additionally, we investigated the effect of cross and self-pollination on fruit and seed production.Key results – The flowers of C. vardariana are protandrous. The length of the styles, which were 8.74 mm during the pollen loading phase, reached 11.35 mm during the pollen presentation phase. The visitor observations made on the C. vardariana flowers revealed 11 visitor species from 5 families: 5 Halictidae, 3 Apidae, and one species each from Megachilidae, Colletidae, and Bombyliidae. Lasioglossum spp. touched the anthers and stigma using several parts of their bodies and were significant pollinators of C. vardariana. Under natural conditions, the mean number of seeds per fruit was around 60 after cross pollination, while no fruits were formed when pollinators were excluded.Conclusion – Campanula vardariana is entirely dependent on pollinators for its reproductive success, and bees, especially Halictidae and to a lesser extent Apidae, play an important role. Campanula vardariana is restricted to cracks in calcareous rocks and its population is threatened by goat overgrazing and mining activities (quarry formation). Since seed production is abundant in this population, anthropogenic activities currently form the biggest threat to its existence.

Darwin's vexing contrivance: a new hypothesis for why some flowers have two kinds of anther.

Heteranthery, the presence of two or more anther types in the same flower, is taxonomically widespread among bee-pollinated angiosperms, yet has puzzled botanists since Darwin. We test two competing hypotheses for its evolution: the long-standing ‘division of labour' hypothesis, which posits that some anthers are specialized as food rewards for bees whereas others are specialized for surreptitious pollination, and our new hypothesis that heteranthery is a way to gradually release pollen that maximizes pollen delivery. We examine the evolution of heteranthery and associated traits across the genus Clarkia (Onagraceae) and study plant–pollinator interactions in two heterantherous Clarkia species. Across species, heteranthery is associated with bee pollination, delayed dehiscence and colour crypsis of one anther whorl, and movement of that anther whorl upon dehiscence. Our mechanistic studies in heterantherous species show that bees notice, forage on and export pollen from each anther whorl when it is dehiscing, and that heteranthery promotes pollen export. We find no support for division of labour, but multifarious evidence that heteranthery is a mechanism for gradual pollen presentation that probably evolved through indirect male–male competition for siring success.

Illuminating the incredible journey of pollen

Illuminating the incredible journey of pollen

Gender expression in Sedum praealtum A. DC. (Crassulaceae) in Central Veracruz, Mexico

Inflorescence type and design determine the position of reproductive meristems and sequence of flowers opening. I examined the gender expression over two entire flowering seasons in Sedum praealtum A. DC. (Crassulaceae) in Central Veracruz, Mexico. Specifically, I studied the floral longevity, sexual-phase duration, flower opening within an inflorescence and sex ratio in the species. I observed that the 8-days flower initiated in male-phase and then switched to female-phase. An extended time of pollen presentation by gradual anthers dehiscence caused an incomplete protandry in the species. The basal-positioned floral buds reached anthesis sooner than the distal-positioned floral buds, resembling an acropetal flowering sequence. Inflorescences production ceased in the middle of the flowering season, whereas flower opening remained constant over reproductive season of the species. The opening of flowers in successive cohorts linked to changes in the flower sexual-phase phenology caused an initial sex expression toward maleness and a balanced sexual expression from the peak to the end of reproductive season in the population sampled. This study highlights the important influence that variations in onset and duration of sexual-phase of flowers can have on sex expression in flowering plants.

Pollen release in the Proteaceae

Pollen dispersal is the step in higher plant mating systems over which the parent plant has the least control as it is dependent on the vagaries of weather conditions (anemophily) or animal behaviour (animal pollinator activity). While many families have passive release from the anther the Proteaceae has a diversity of pollen dispersal methods. Flowers from a range of species in the Proteaceae, covering the majority of genera from each of the four main subfamilies, were examined to determine how pollen is dispersed and to gain an overall view of how male function varies within the family. This provides a basis for predicting the degree of the six likely fates of pollen released in this family. Only one group (subfamily Persoonioideae) and four genera in one other subfamily (Proteoideae) dispense pollen directly from the anthers onto a flower visitor. Five genera in the Proteoideae have explosive pollen release, while Symphionema may require vibration to release the pollen. All the remaining Proteoideae genera, the single species of Bellendenoideae, and all genera of the Grevilleoideae (except Sphalmium) have a pollen presenter where pollen is dispersed from the style of the flower. Ancestral Proteaceae were likely to have been insect pollinated and had relatively small flowers. Taxa with explosive pollen release may have evolved early in the family and may have been more abundant early in the fossil record. However, the taxa with pollen presenters became much more abundant throughout the Tertiary when many developed robust gynoecia that can accommodate larger vertebrate pollinators.

Pollen biodiversity – why are pollen grains different despite having the same function? A review

AbstractThe main morphological, cytological and physiological characters of ripe pollen are described, compared, analysed and discussed individually, in multiple combinations and in respect to the female counterpart and the biotic and abiotic components of the environment. This is to try to understand the reasons why pollen grains have the same reproductive function, but at dispersal are morphologically and physiologically different in many respects. The considered characters are: one or more types of grain per species; shape and size; number of cells; types of pollen dispersal unit; sporoderm stratification, furrows, colpori and other kinds of apertures; pollen presentation and array; water content percentage; and mature pollen reserves and osmotics. Some of the pollen features are correlated between themselves, some with the female counterpart or male and female competition, and others with the different components of the environment where the species lives, when it flowers and when pollen presentation occurs.

Unique and highly specific cyanogenic glycoside localization in stigmatic cells and pollen in the genus Lomatia (Proteaceae).

Floral chemical defence strategies remain understudied despite the significance of flowers to plant fitness, and the fact that many flowers contain secondary metabolites that confer resistance to herbivores. Optimal defence and apparency theories predict that the most apparent plant parts and/or those most important to fitness should be most defended. To test whether within-flower distributions of chemical defence are consistent with these theories we used cyanogenic glycosides (CNglycs), which are constitutive defence metabolites that deter herbivores by releasing hydrogen cyanide upon hydrolysis. We used cyanogenic florets of the genus Lomatia to investigate at what scale there may be strategic allocation of CNglycs in flowers, what their localization reveals about function, and whether levels of floral CNglycs differ between eight congeneric species across a climatic gradient. Within-flower distributions of CNglycs during development were quantified, CNglycs were identified and their localization was visualized in cryosectioned florets using matrix-assisted laser desorption ionization mass spectrometry imaging (MALDI-MSI). Florets of all congeneric species studied were cyanogenic, and concentrations differed between species. Within florets there was substantial variation in CNglyc concentrations, with extremely high concentrations (up to 14.6 mg CN g-1 d. wt) in pollen and loose, specialized surface cells on the pollen presenter, among the highest concentrations reported in plant tissues. Two tyrosine-derived CNglycs, the monoglycoside dhurrin and diglycoside proteacin, were identified. MALDI-MSI revealed their varying ratios in different floral tissues; proteacin was primarily localized to anthers and ovules, and dhurrin to specialized cells on the pollen presenter. The mix of transient specialized cells and pollen of L. fraxinifolia was ~11 % dhurrin and ~1.1 % proteacin by mass. Tissue-specific distributions of two CNglycs and substantial variation in their concentrations within florets suggests their allocation is under strong selection. Localized, high CNglyc concentrations in transient cells challenge the predictions of defence theories, and highlight the importance of fine-scale metabolite visualization, and the need for further investigation into the ecological and metabolic roles of CNglycs in floral tissues.

Pollen reinforces learning in honey bee pollen foragers but not in nectar foragers.

Searching for reward motivates and drives behaviour. In honey bees Apis mellifera, specialized pollen foragers are attracted to and learn odours with pollen. However, the role of pollen as a reward remains poorly understood. Unlike nectar, pollen is not ingested during collection. We hypothesized that pollen (but not nectar) foragers could learn pollen by sole antennal or tarsal stimulation. Then, we tested how pairing of pollen (either hand- or bee-collected) and a neutral odour during a pre-conditioning affects performance of both pollen and nectar foragers during the classical conditioning of the proboscis extension response. Secondly, we tested whether nectar and pollen foragers perceive the simultaneous presentation of pollen (on the tarsi) and sugar (on the antennae) as a better reinforcement than sucrose alone. Finally, we searched for differences in learning of the pollen and nectar foragers when they were prevented from ingesting the reward during the conditioning. Differences in pollen-reinforced learning correlate with division of labour between pollen and nectar foragers. Results show that pollen foragers performed better than nectar foragers during the conditioning phase after being pre-conditioned with pollen. Pollen foragers also performed better than nectar foragers in both the acquisition and extinction phases of the conditioning, when reinforced with the dual reward. Consistently, pollen foragers showed improved abilities to learn cues reinforced without sugar ingestion. We discussed that differences in how pollen and nectar foragers respond to a cue associated with pollen greatly contribute to the physiological mechanism that underlies foraging specialization in the honeybee.

Solitary bee pollinators adjust pollen foraging to the unpredictable flower opening of a species of Petunia (Solanaceae)

AbstractDetails of the foraging patterns of solitary bees are much less well known than those of social species, and these patterns are often adjusted to exploit floral resources of one or only a few species. The specialized flower-visiting bees of Petunia are good models for investigating such foraging patterns. Here we analysed the floral biology and pollen presentation schedule of the endangered Petunia mantiqueirensis in mixed Araucaria forests of Serra da Mantiqueira, Brazil. Pollinators and their pollen foraging behaviour and food specialization were determined through analyses of scopa pollen loads. Flowers opened throughout the day and presented all their pollen resources within the first 30 min of anthesis, thus providing their pollen resources in an asynchronous fashion in one-flower packages throughout the day. Females of Pseudagapostemon fluminensis were the most frequent flower visitors, contacting stigmas in 96% of their visits, and were the unique effective pollinators of Petunia mantiqueirensis. These pollinators were responsible for the first three visits to 115 individually monitored flowers at any daylight hour, removing ~86% of a flower’s total pollen supply during the first visit. Although female bees harvest the majority of pollen resources of Petunia mantiqueirensis, analyses of scopa loads revealed that most of them also collect pollen from plants of other families while foraging for pollen in Petunia flowers.

Specialised protagonists in a plant-pollinator interaction: the pollination of Blumenbachia insignis (Loasaceae).

Analyses of resource presentation, floral morphology and pollinator behaviour are essential for understanding specialised plant-pollinator systems. We investigated whether foraging by individual bee pollinators fits the floral morphology and functioning of Blumenbachia insignis, whose flowers are characterised by a nectar scale-staminode complex and pollen release by thigmonastic stamen movements. We described pollen and nectar presentation, analysed the breeding system and the foraging strategy of bee pollinators. We determined the nectar production pattern and documented variations in the longevity of floral phases and stigmatic pollen loads of pollinator-visited and unvisited flowers. Bicolletes indigoticus (Colletidae) was the sole pollinator with females revisiting flowers in staminate and pistillate phases at short intervals, guaranteeing cross-pollen flow. Nectar stored in the nectar scale-staminode complex had a high sugar concentration and was produced continuously in minute amounts (~0.09μl·h-1 ). Pushing the scales outward, bees took up nectar, triggering stamen movements and accelerating pollen presentation. Experimental simulation of this nectar uptake increased the number of moved stamens per hour by a factor of four. Flowers visited by pollinators received six-fold more pollen on the stigma than unvisited flowers, had shortened staminate and pistillate phases and increased fruit and seed set. Flower handling and foraging by Bicolletes indigoticus were consonant with the complex flower morphology and functioning of Blumenbachia insignis. Continuous nectar production in minute quantities but at high sugar concentration influences the pollen foraging of the bees. Partitioning of resources lead to absolute flower fidelity and stereotyped foraging behaviour by the sole effective oligolectic bee pollinator.

Structure of floral nectaries and female-biased nectar production in protandrous species Geranium macrorrhizum and Geranium phaeum.

Nectar is a major floral reward offered to pollinators by plants. In dichogamous plant species, differences in nectar production across sexual phases often occur, but both the male- and female-phase flowers have to attract pollinators to achieve effective pollination. Nectar-producing structures, i.e. floral nectaries, are a key component of floral organisation and architecture, and the knowledge of their structure and function contributes to better understanding of the plant-pollinator interactions. In the present study, we investigated the morphology and structure of nectaries and the nectar production pattern in two protandrous species Geranium macrorrhizum and G. phaeum. The flowers of the studied species have been shown to exhibit varied availability of nectar for insect visitors. Their nectaries differ in the shape, size and thickness. The other differences include the localisation of the stomatal field, the size and number of nectarostomata, the presence of non-glandular and glandular trichomes, the presence of tannin idioblasts, the mode of secretion and the occurrence of plastids functioning probably as autophagosomes and autolysosomes, whose presence in nectary cells has been described for the first time. The flowers of the studied species started nectar secretion in the non-receptive phase before pollen presentation and nectar was produced throughout both sexual phases. The nectar production was gender biased towards the female phase in the nectar amount, nectar sugar concentration and total sugar secreted in the nectar. We postulate that the nectar production patterns in G. phaeum and G. macrorrhizum might have evolved as a response to pollinators' pressure.

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.

The cost of fidelity: foraging oligolectic bees gather huge amounts of pollen in a highly specialized cactus–pollinator association

Abstract Plant–pollinator interactions vary along a specialization–generalization continuum. Advances in understanding the evolutionary and ecological consequences of different degrees of specialization depend on precise data on plant–pollinator interdependency. We studied the association of Parodia neohorstii (Cactaceae) and its bee pollinators focusing on pollinator foraging behaviour, flower functioning, female and male reproductive success, and pollen fate. Parodia neohorstii showed synchronized flower opening and pollen presentation but discontinuous blooming. The apparently generalized flowers partition pollen through thigmonastic stamen movements that function as a mechanical filter against generalist bees by restricting access to the major pollen reservoir to bees that show flower handling ‘know-how’, thereby favouring the oligolectic bee Arhysosage cactorum. This pollinator adjusted its pollen foraging to flower opening, removed pollen hurriedly, and promoted maximal fruit and seed set, which was minimal in its absence. Estimates of pollen fate revealed that a huge amount of pollen flows to specialized pollinators (86.5%), and only 0.9% reaches conspecific stigmas. The specialized interaction between P. neohorstii and Arhysosage cactorum, both threatened species, is efficient but fragile. Any environmental modification that causes a mismatch between the partners is likely to result in reproductive failure.

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.

Kermadecia brinoniae (Proteaceae: Macadamieae), a new species from New Caledonia previously confused with K. elliptica

Hopkins, H.C.F. & Y. Pillon (2019). Kermadecia brinoniae (Proteaceae: Macadamieae), a new species from New Caledonia previously confused with K. elliptica. In English, English and French abstracts. Candollea 74: 85–92. DOI: http://dx.doi.org/10.15553/c2019v741a9Kermadecia brinoniae H.C. Hopkins & Pillon (Proteaceae), which occurs in southern New Caledonia, principally on ultramafic substrates, is described and illustrated. Material of this species was previously included in Kermadecia elliptica Brongn. & Gris. An amended description is given for the latter and a lectotype designated. These two species differ in the prominence of the venation on the lower leaf surface and in their ecology. Kermadecia brinoniae, like other species of Proteaceae growing on ultramafic substrates of New Caledonia, has a relatively high content of manganese in its leaves. A revised key to the species of Kermadecia Brongn. & Gris is provided as well as notes on the morphology of the pollen presenter.

Flowers anticipate revisits of pollinators by learning from previously experienced visitation intervals

ABSTRACTPlants – and their pollinating counterparts – display complex and sophisticated mechanisms to achieve successful pollination. It probably was only a matter of time for proof of plant intelligence in the context of floral ecology to surface, i.e. the memorization of previous events and a corresponding adjustment of flower behavior. In a recent study we presented a large experimental dataset on the evolution of stamen movement patterns observed in Loasaceae and the apparent role of plant behavior in the diversification of this plant group. The findings at species level suggest that individual plants may be able to adjust the timing of their pollen presentation to the actual pollination scenario they experience. Here we provide first evidence for a pre-emptive stamen presentation in Nasa poissoniana (Loasaceae), based on previously experienced pollinator visitation intervals. Using the unique ability of fast and precise stamen movements in response to a previous stimulus of the nectar scales, the plants should be able to reduce pollen loss and increase outbreeding success via optimizing the timing of male function. We discuss this behavior and its implications in the light of the recent literature and propose questions for future investigations.