Pollination Ecology and Effect of Nectar Removal in Macleania bullata (Ericaceae)1

The floral syndrome of Macleania bullataYeo (Ericaceae) reflects its adaptation to hummingbird pollination. Its flowers, however, are subject to high levels of nectar robbing. I examined the floral visitor assemblage of M. bullata in a tropical montane wet forest in southwestern Colombia, focusing on the behavior of the visitors. I also tested for the presence of nocturnal pollination and the effects of nectar removal on new nectar production. The principal floral visitors were the nectar robbing hummingbirds Ocreatus underwoodii (19.1% of visits) and Chlorostilbon mellisugus (18.9%). Only two species of long–billed hummingbirds visited the flowers of M. bullata as “legitimate” pollinators: Coeligena torquata (14.7% of visits) and Doryfera ludoviciae (14.3%). The remaining visits constituted nectar robbing by bees, butterflies, and other species of hummingbirds. Nocturnal pollination took place, although fruit set levels were 2.4 times higher when only diurnal pollination was allowed as opposed to exclusively nocturnal pollination. Nectar robbers removed floral nectar without pollinating the flower. Treatments of experimental nectar removal were carried out to examine if flowers synthesize more nectar after nectar removal. Nectar removal increased the total volume of nectar produced by each flower without affecting sugar concentration. Thus, nectar robbing can impose a high cost to the plants by forcing them to replace lost nectar.     

So many visitors and so few pollinators: variation in insect frequency and effectiveness governs the reproductive success of an endemic milkwort

Plant–pollinator interactions are one of the most important and variable mutualisms having major implications for plant fitness. The present study evaluates the interactions between an endemic milkwort, Polygala vayredae, and its floral visitors by studying the temporal variability, foraging behaviour and effectiveness of floral visitors in three populations during three consecutive years. The flowers were visited by a diverse array of insects, totalling 24 different species. However, only four species were effective pollinators, depositing pollen on stigmas after one visit, while the remaining species behaved as nectar robbers, secondary nectar robbers or nectar thieves and were completely ineffective for pollination. Among the effective pollinators, two groups with distinct foraging behaviours were observed: the nectar collecting long-tongued bees Bombus pascuorum and Anthophora sp. and the pollen collectors Eucera longicornis and Halictus sp. No significant differences were observed among pollinators in their efficiency in pollen deposition on stigmas, but significant differences were observed in the foraging behaviour between nectarivorous and pollen collectors. Variation in the abundance and assemblage of floral visitors was observed at the temporal scale and among populations, with the effective pollinators being generally scarce. Consequently, the reproductive outcome in this species was low and significantly variable among populations and years. The results highlight the importance of studying floral visitor effectiveness when determining pollinator assemblages.     

Relative pollination effectiveness of floral visitors of Pitcairnia angustifolia (Bromeliaceae)

The effectiveness of flower visitors as pollinators will determine their potential role as selective agents on flower traits. Pitcairnia angustifolia has floral characters that would fit pollination by long-billed hummingbirds, and they should be the most effective pollinators for this plant. To test this prediction, we characterized the behavior of visitors toward flowers and their pollination effectiveness. Coereba flaveola (bananaquits) was the most frequent flower visitor and acted as a primary nectar robber; however, they pollinated incidentally and deposited pollen on stigmas. The endemic short-billed hummingbird Chlorostilbon maugaeus behaved as a secondary robber and did not pollinate flowers. As expected, the long-billed hummingbird, Anthracothorax viridis, was the most efficient visitor in terms of pollen deposition; however, it was the least frequent flower visitor. Introduced Apis mellifera (honeybees) were second in efficiency at depositing pollen and performed one third of the flower visits. Estimates of the expected rate of pollen deposition by each pollinator did not identify a single most effective pollinator. For P. angustifolia at least three flower visitors including an exotic bee and a nectar robber may be equally important to reproductive success. While these results limit our ability to make predictions on the role of hummingbird-pollination on current flower evolution, they do suggest the potential for pollination redundancy among flower visitors for P. angustifolia populations.     

The relative strength of different floral visitors driving floral evolution within a <Emphasis Type="Italic">Primula secundiflora</Emphasis> population

Floral visitor assemblages within plant populations are usually composed of different visitors, and the relative abundance of these visitors also varies. Therefore, identifying the relative strength of these floral visitors driving floral evolution within the population is an important step in predicting the evolutionary trajectory of floral traits. Using supplemental hand pollination and nectar-robbing exclusion treatments, we experimentally identified the relative strengths of legitimate pollinators (that visit flowers through the corolla tube entrance) and nectar robbers (that visit flowers by biting a hole in the corolla tube or using an existing hole) driving floral evolution within the Primula secundiflora population. We also estimated legitimate pollinator- and nectar robber-mediated selection separately for pin and thrum flowers. Both legitimate pollinators and nectar robbers mediated selection on pollination efficiency traits in P. secundiflora population. Legitimate pollinators mediated selection for wider corolla tubes, whereas nectar robbers mediated selection for longer corolla tubes. In addition, nectar robber-mediated selection on corolla tube length marginally varied between the pin and thrum flowers. Nectar robber mediated selection for longer corolla tube length in the pin flowers not in the thrum flowers. These results indicate that legitimate pollinators and nectar robbers within a population can drive differential evolutionary trajectories of floral traits.     

Visitation rate of pollinators and nectar robbers to the flowers and inflorescences of Tabebuia aurea (Bignoniaceae): effects of floral display size and habitat fragmentation

Large floral displays favour pollinator attraction and the import and export of pollen. However, large floral displays also have negative effects, such as increased geitonogamy, pollen discounting and nectar/pollen robber attraction. The size of the floral display can be measured at different scales (e.g. the flower, inflorescence or entire plant) and variations in one of these scales may affect the behaviour of flower visitors in different ways. Moreover, the fragmentation of natural forests may affect flower visitation rates and flower visitor behaviour. In the present study, video recordings of the inflorescences of a tree species (Tabebuia aurea) from the tropical savannah of central Brazil were used to examine the effect of floral display size at the inflorescence and tree scales on the visitation rate of pollinators and nectar robbers to the inflorescence, the number of flowers approached per visit, the number of visits per flower of potential pollinators and nectar robbers, and the interaction of these variables with the degree of landscape disturbance. Nectar production was quantified with respect to flower age. Although large bees are responsible for most of the pollination, a great diversity of flower insects visit the inflorescences of T. aurea. Other bee and hummingbird species are highly active nectar robbers. Increases in inflorescence size increase the visitation rate of pollinators to inflorescences, whereas increases in the number of inflorescences on the tree decrease visitation rates to inflorescences and flowers. This effect has been strongly correlated with urban environments in which trees with the largest floral displays are observed. Pollinating bees (and nectar robbers) visit few flowers per inflorescence and concentrate visits to a fraction of available flowers, generating an overdispersed distribution of the number of visits per inflorescence and per flower. This behaviour reflects preferential visits to young flowers (including flower buds) with a greater nectar supply.     

Novel nectar robbing negatively affects reproduction in Digitalis purpurea

With many plant–pollinator interactions undergoing change as species’ distributions shift, we require a better understanding of how the addition of new interacting partners can affect plant reproduction. One such group of floral visitors, nectar robbers, can deplete plants of nectar rewards without contributing to pollination. The addition of nectar robbing to the floral visitor assemblage could therefore have costs to the plant´s reproductive output. We focus on a recent plant colonist, Digitalis purpurea, a plant that in its native range is rarely robbed, but experiences intense nectar robbing in areas it has been introduced to. Here, we test the costs to reproduction following experimental nectar robbing. To identify any changes in the behavior of the principal pollinators in response to nectar robbing, we measured visitation rates, visit duration, proportion of flowers visited, and rate of rejection of inflorescences. To find the effects of robbing on fitness, we used proxies for female and male components of reproductive output, by measuring the seeds produced per fruit and the pollen export, respectively. Nectar robbing significantly reduced the rate of visitation and lengths of visits by bumblebees. Additionally, bumblebees visited a lower proportion of flowers on an inflorescence that had robbed flowers. We found that flowers in the robbed treatment produced significantly fewer seeds per fruit on average but did not export fewer pollen grains. Our finding that robbing leads to reduced seed production could be due to fewer and shorter visits to flowers leading to less effective pollination. We discuss the potential consequences of new pollinator environments, such as exposure to nectar robbing, for plant reproduction.     

Specialized pollination in the African milkweed Xysmalobium orbiculare: a key role for floral scent in the attraction of spider-hunting wasps

Specialized pollination by prey-hunting wasps is poorly documented in rewarding plants. Furthermore, the mechanisms of achieving specialization are not clear since flowers typically produce exposed nectar and have no morphological adaptations (such as long spurs) to exclude non-pollinating visitors. We investigated the pollination of Xysmalobium orbiculare and explored the functional roles of floral scent and nectar in attracting pollinators and deterring nectar robbers. Floral visitor observations showed that this milkweed is visited almost exclusively by pompilid wasps in the genus Hemipepsis. These wasps were the only insects to carry pollinia, and a cage experiment confirmed their effectiveness in removing and inserting pollinia on flowers. Hand-pollinations showed that plants are genetically self-incompatible and thus reliant on pollinators for seed set. Palatability experiments with honeybees showed that nectar is distasteful to non-pollinating insects and is therefore likely to play a functional role in deterring nectar thieves. Choice experiments in the field showed that the wasp pollinators are attracted primarily by floral scent rather than visual cues. Analysis of spectral reflectance of flowers revealed that flowers are dull colored and are unlikely to stand out from the background vegetation. We conclude that X. orbiculare is specialized for pollination by spider-hunting wasps in the genus Hemipepsis and utilizes floral scent to selectively attract its pollinators and unpalatable nectar to deter non-pollinating visitors.     

Changes in Florets’ Vertical Direction within Inflorescence Affects Pollinator Behavior,and Fitness in <i>Trifolium repens</i>

Ecological interactions between flowers and pollinators greatly affect the reproductive success. To facilitate these interactions, many flowers are known to display their attractive qualities, such as scent emission, flower rewards and floral vertical direction, in a rhythmic fashion. However, less is known about how plants regulate the relationship between these flower traits to adapt to pollinator visiting behavior and increase reproduction success. Here we investigated the adaptive significance of the flower bending from erect to downward in Trifolium repens. We observed the flowering dynamic characteristics (changes of vertical direction of florets, flowering number, pollen grain numbers, pollen viability and stigma receptivity over time after blossom) and the factors affecting the rate of flower bending in T. repens. Then we altered the vertical direction of florets in inflorescence of different types (upright and downward), and compared the pollinator behaviors and female reproductive success. Our results showed that florets opened sequentially in inflorescence, and then bend downwards slowly after flowering. The bending speed of florets was mainly influenced by pollination, and bending angle increased with the prolongation of flowering time, while the pollen germination rate, stigma receptivity and nectar secretion has a rhythm of “low-high-low” during the whole period with the time going. The visiting frequency of all the four species of pollinators on upward flowers was significantly higher than that of downward flowers, and they especially prefer to visit flowers with a bending angle of 30°–60°, when the flowers was exactly of the highest flower rewards (nectar secretion and number of pollen grains), stigma receptivity and pollen germination rate. The seed set ratio and fruit set ratio of upward flowers were significantly higher than downward flowers, but significantly lower than unmanipulated flowers. Our results indicated that the T. repens could increase female and male fitness by accurate pollination. The most suitable flower angle saves pollinators’ visiting energy and enables them to obtain the highest nectar rewards. This coordination between plants and pollinators maximizes the interests of them, which is a crucial factor in initiating specialized plant-pollinator relationships.     

Altitude-related shift of relative abundance from insect to sunbird pollination in Elaeagnus umbellata (Elaeagnaceae)

The evolution of floral traits has been thought to be influenced by local, effective pollinators. However, little attention has been paid to the possibility that altitudinal variation in floral traits could be mediated by local pollinator functional groups, particularly a shift from bees to birds. Plant size, floral traits, pollinators and their pollination roles were investigated in the spring-flowering shrub Elaeagnus umbellata (Elaeagnaceae) at three altitudes (1160, 1676, and 2050 m) in Minshan, Sichuan Province, on the northern rim of the Hengduan Mountains, southwest China. Compared to lower altitudes, higher-altitude plants were smaller but the floral tubes were longer, with a larger volume of nectar of lower sugar concentration but with a greater proportion of sucrose. The visitation frequency of bees decreased with altitude, whereas the sunbirds did the opposite. Birds and bees foraged for nectar but not pollen, and birds deposited more pollen grains per visit relative to bees and least were syrphid flies. Excluding birds decreased seed set at high but not at mid- or low altitude. Our study of E. umbellata revealed an association between altitudinal variation in floral traits and a change in the relative abundance of the major pollinators with altitude from majority bees to majority sunbirds. Although abiotic factors also tend to vary with altitude and can affect floral traits, nectar properties of “pro-bird” pollination were observed at high altitude.     

Nectary tracks as pollinator manipulators: The pollination ecology of Swertia bimaculata (Gentianaceae)

Floral nectaries are closely associated with biotic pollination, and the nectar produced by corolla nectaries is generally enclosed in floral structures. Although some Swertia spp. (Gentianaceae), including S. bimaculata, evolved a peculiar form of corolla nectaries (known as “gland patches”) arranged in a conspicuous ring on the rotate corolla and that completely expose their nectar, little is known about the pollination of these plants. Two hypotheses were made concerning the possible effects of gland patches: visual attraction and visitor manipulation. The floral traits, mating system, and insect pollination of S. bimaculata were examined, and the pollination effects of gland patches were evaluated. A comparative study was made using Swertia kouitchensis, a species with fimbriate nectaries. Swertia bimaculata flowers were protandrous, with obvious stamen movement leading to herkogamy in the female phase and to a significant reduction in nectary–anther distance. The species is strongly entomophilous and facultatively xenogamous. The daily reward provided per flower decreased significantly after the male phase. The most effective pollinators were large dipterans, and the visiting proportion of Diptera was significantly higher in S. bimaculata than in S. kouitchensis. Most visitors performed “circling behavior” in S. bimaculata flowers. Removing or blocking the nectaries caused no reduction in visiting frequency but a significant reduction in visit duration, interrupting the circling behavior. The circling behavior was encouraged by nectar abundance and promoted pollen dispersal. Visitor species with small body size had little chance to contact the anthers or stigma, revealing a filtration effect exerted by the floral design. These results rejected the “visual attraction” hypothesis and supported the “visitor manipulation” hypothesis. The nectary whorl within a flower acted like a ring‐shaped track that urged nectar foragers to circle on the corolla, making pollination in S. bimaculata flowers more orderly and selective than that in classically generalist flowers.     

Hidden floral adaptation to nocturnal moths in an apparently bee‐pollinated flower,Adenophora triphylla var. japonica (Campanulaceae)

• The discrepancy between observed flower visitors and those predicted based on floral phenotype has often cast doubt on the pollination syndrome concept. Here we show that this paradox may be alleviated by gaining better knowledge of the contributions of different flower visitors to pollination and the effects of floral traits that cannot be readily perceived by humans in Adenophora triphylla var. japonica. The blue, bell‐shaped and pendant flowers of A. triphylla appear to fit a bee pollination syndrome. In contrast to this expectation, recent studies show that these flowers are frequented by nocturnal moths.
• We compared the flower visitor fauna, their visitation frequency and their relative contributions to seed set between day and night in two field populations of A. triphylla in Japan. We also determined the floral traits associated with temporal changes in the visitor assemblage, i.e. the timing of anthesis, the timing of changes in the sexual phase and the diel pattern of nectar production.
• While A. triphylla flowers were visited by both diurnal and nocturnal insects, the results from pollination experiments demonstrate that their primary pollinators are nocturnal settling‐moths. Moreover, the flowers opened just after sunset, changed from staminate to pistillate phase in successive evenings and produced nectar only during the night, which all conform to the activity of nocturnal/crepuscular moths.
• Our study illustrates that the tradition of stereotyping the pollinators of a flower based on its appearance can be misleading and that it should be improved with empirical evidence of pollination performance and sufficient trait matching.

     

贠建全:广东荷包岛维管束植物名录

以分布于秦岭的金花忍冬（Lonicera chrysantha Turcz.）、忍冬（L.japonica Thunb.）、葱皮忍冬（L.ferdinandii Franch.）和金银忍冬（L.maackii（Rupr.）Maxim.）为对象,通过定位观察、人工授粉实验、人为设置实验斑块的方法对忍冬属4种植物的开花生物学特性、繁育系统、花色变化现象、传粉过程进行了研究。结果表明,4种植物的单花花期、花部特征存在差异。人工授粉实验显示,4种植物均存在一定的花粉限制,自交不亲和。除葱皮忍冬外,其余3种植物随着花色由白变黄,花粉和花蜜报酬减少、雌雄生殖能力逐渐降低;葱皮忍冬花变色后花蜜量变化不显著,且仍保留较强的雌性生殖能力。变色花的保留被认为是植物的一种生殖策略,通过增大植物的花展示来扩大自身的吸引力,以吸引更多远距传粉者访花。人为控制白、黄花不同数量比的实验结果表明,大多数传粉者偏向访问白花（变色前的花）,且白花提供的报酬量和黄花（变色后的花）数量显著影响传粉者的访花频率,即当花蜜量减少或黄花数量增多时,传粉者访花频率随之降低。因此,我们认为忍冬属4种植物的花色变化可能除了增大植物对远距传粉者的吸引力外,对近距传粉者的访花行为也可能具有一定的影响。当传粉者接近植株时,变色后的花可能暗示其花蜜（花粉）报酬已经发生变化,并驱使昆虫离开并飞向同株或异株植物新开放的报酬丰富的白花,这既有利于提高传粉者的觅食效率,又能降低植物同株异花授粉的几率,对忍冬属植物及传粉者都具有重要意义,是植物长期与授粉昆虫相互适应的反映。     

The dynamics of pollen removal and deposition,and its effects on sexual phases in a protandrous plant: Glechoma longituba (Lamiaceae)

The duration of sexual phases in dichogamous plants are affected by many factors. Using both experimental and observational studies, we investigated natural patterns of pollen removal and deposition, visiting frequency of pollinators, patterns of nectar secretion, and effects of pollen removal and stigmatic pollen deposition on the duration of sexual phases in a protandrous plant, Glechoma longituba. We found that visiting frequency of pollinators correlated with the nectar secretion pattern. The nectar volume during the male phase was higher than during the female phase. In the morning, the main pollinator, the bee Anthophora plumipes, mainly foraged for nectar and showed no preference for flowers in male or female phase, despite male phase flowers producing higher amounts of nectar. However, in the afternoon, they changed their behavior and foraged mainly for pollen, and then showed a preference for flowers in male phase. Furthermore, the rates of pollen removal and stigmatic pollen deposition can affect the starting time and the duration of the female phase. When pollen removal and pollination rates are low due to scarcity of pollinator services, the sexual phase can be prolonged, leading to an overlap, and thereby enhance the chance for sexual reproduction through pollinator‐facilitated self‐pollination. We consider the variation of sexual phases in Glechoma longituba an adaptive mechanism prepared for both cross‐pollination enhancement and reproductive assurance depending on the available pollination services.     

Reloading the revolver – male fitness as a simple explanation for complex reward partitioning in Nasa macrothyrsa (Loasaceae,Cornales)

Reward partitioning and replenishment and specific mechanisms for pollen presentation are all geared towards the maximization of the number of effective pollinator visits to individual flowers. An extreme case of an apparently highly specialized plant–pollinator interaction with thigmonastic pollen presentation has been described for the morphologically complex tilt‐revolver flowers of Caiophora arechavaletae (Loasaceae) pollinated by oligolectic Bicolletes pampeana (Colletidae, Hymenoptera). We studied the floral biology of Nasa macrothyrsa (Loasaceae) in the field and in the glasshouse, which has very similar floral morphology, but is pollinated by polylectic Neoxylocopa bees (Apidae, Hymenoptera). We investigated the presence of thigmonastic anther presentation, visitor behaviour (pollinators and nectar robbers), co‐ordination of pollinator visits with flower behaviour and the presence of nectar replenishment. The aim of this study was to understand whether complex flower morphology and behaviour can be explained by a specialized pollination syndrome, or whether alternative explanations can be offered. The results showed that Nasa macrothyrsa has thigmonastic pollen presentation, i.e. new pollen is rapidly (<< 10 min) presented after a pollinator visit. Nectar secretion is independent of removal and averages 7–14 µL h^–1. The complex flowers, however, fail to exclude either native (hummingbirds) or introduced (honeybees) nectar robbers, nor does polylectic Neoxylocopa actively collect the pollen presented. The findings do not support a causal link between complex flower morphology and functionality in Loasaceae and a highly specialized pollination. Rapid pollen presentation is best explained by the pollen presentation theory: the large proportion of pollinators coming shortly after a previous visit find little nectar and are more likely to move on to a different plant. The rapid presentation of pollen ensures that all these valuable ‘hungry pollinators’ are dusted with small pollen loads, thus increasing the male fitness of the plant by increasing the likelihood of siring outcrossed offspring. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 124–131.     

Nectar Sugar Production across Floral Phases in the Gynodioecious Protandrous Plant Geranium sylvaticum

Many zoophilous plants attract their pollinators by offering nectar as a reward. In gynodioecious plants (i.e. populations are composed of female and hermaphrodite individuals) nectar production has been repeatedly reported to be larger in hermaphrodite compared to female flowers even though nectar production across the different floral phases in dichogamous plants (i.e. plants with time separation of pollen dispersal and stigma receptivity) has rarely been examined. In this study, sugar production in nectar standing crop and secretion rate were investigated in Geranium sylvaticum, a gynodioecious plant species with protandry (i.e. with hermaphrodite flowers releasing their pollen before the stigma is receptive). We found that flowers from hermaphrodites produced more nectar than female flowers in terms of total nectar sugar content. In addition, differences in nectar production among floral phases were found in hermaphrodite flowers but not in female flowers. In hermaphrodite flowers, maximum sugar content coincided with pollen presentation and declined slightly towards the female phase, indicating nectar reabsorption, whereas in female flowers sugar content did not differ between the floral phases. These differences in floral reward are discussed in relation to visitation patterns by pollinators and seed production in this species.     

Bee pollination and evidence of substitutive nectary in <Emphasis Type="Italic">Anadenanthera colubrina</Emphasis> (Leguminosae-Mimosoideae)

Anadenanthera colubrina (Vell.) Brenan (Leguminosae-Mimosoideae) is a widely-distributed tree in seasonally dry tropical forests of South America that was classified previously as lacking nectaries. However, some studies have stated that its flowers produce nectar, while others analyzed the composition of unifloral honey produced from A. colubrina flowers, raising the question about nectar production in the species. We studied the pollination and reproductive biology of A. colubrina var. cebil (Griseb.) Altschul in a natural population in the Caatinga, northeastern Brazil. Reproductive phenology, sexual system, floral biology, resource, and pollinators were investigated. We analyzed the breeding system through controlled pollinations for addressing its dependence on pollen vectors for reproduction. Anadenanthera colubrina flowered in the dry season, flower heads are heteromorphic, with staminate flowers at the base and perfect flowers at the apex of the inflorescence, characterizing andromonoecy. Anthesis is diurnal. We observed small drops of nectar at the apex of the petals of some flowers per inflorescence. Together with observations on flower visitor behavior and histochemical tests, we propose that A. colubrina produces floral nectar at the apex of the corolla, characterizing a substitutive nectary (sensu Vogel). This is the first record of substitutive nectary in the Mimosoideae and the first record of andromonoecy in the genus. Bees were the main pollinators (higher frequency), although other insects such as wasps, butterflies, and small beetles were also observed collecting nectar and/or pollen. The species is self-incompatible, thus depending on insect pollen vectors, mainly bees, for reproduction.     

Pollen in Bee-Flower Relations Some Considerations on Melittophily*

Pollen and nectar are usually lumped together as floral rewards for pollinating bees, but they play totally different roles for flowers and bees (Table 1), as well as in the relationship between them. While flowers are specialized for certain pollinators via nectar, bees specialize on certain flowers via pollen. While flowers need pollen as a prerequisite for pollination, it is the essential larval food in bees. Thus, there is a strong competition between them for pollen. Foraging for pollen must be divided into three phases: uptake in the flower, reloading into and homeward transport within a carrying container. Bees have specializations for transport but hardly any for pollen uptake - and thus for pollination. Bees actively harvesting pollen usually do not pollinate. This only happens as a consequence of contamination of the bee by pollen. From these data a scenario is provided for the evolution of bees and bee flowers. Specialized bee flowers are often characterized by their ability to hide pollen from the bees and at the same time use them as optimal pollinators. If the relationship of bees and flowers is mutualistic at all it is best described as a balanced mutual exploitation.     

Floral traits mediate the vulnerability of aloes to pollen theft and inefficient pollination by bees

Background and Aims

Pollen-collecting bees are among the most important pollinators globally, but are also the most common pollen thieves and can significantly reduce plant reproduction. The pollination efficiency of pollen collectors depends on the frequency of their visits to female(-phase) flowers, contact with stigmas and deposition of pollen of sufficient quantity and quality to fertilize ovules. Here we investigate the relative importance of these components, and the hypothesis that floral and inflorescence characteristics mediate the pollination role of pollen collection by bees.

Methods

For ten Aloe species that differ extensively in floral and inflorescence traits, we experimentally excluded potential bird pollinators to quantify the contributions of insect visitors to pollen removal, pollen deposition and seed production. We measured corolla width and depth to determine nectar accessibility, and the phenology of anther dehiscence and stigma receptivity to quantify herkogamy and dichogamy. Further, we compiled all published bird-exclusion studies of aloes, and compared insect pollination success with floral morphology.

Key Results

Species varied from exclusively insect pollinated, to exclusively bird pollinated but subject to extensive pollen theft by insects. Nectar inaccessibility and strong dichogamy inhibited pollination by pollen-collecting bees by discouraging visits to female-phase (i.e. pollenless) flowers. For species with large inflorescences of pollen-rich flowers, pollen collectors successfully deposited pollen, but of such low quality (probably self-pollen) that they made almost no contribution to seed set. Indeed, considering all published bird-exclusion studies (17 species in total), insect pollination efficiency varied significantly with floral shape.

Conclusions

Species-specific floral and inflorescence characteristics, especially nectar accessibility and dichogamy, control the efficiency of pollen-collecting bees as pollinators of aloes.     

Change of floral orientation affects pollinator diversity and their relative importance in an alpine plant with generalized pollination system,Geranium refractum (Geraniaceae)

Floral orientation may affect pollinator attraction and pollination effectiveness, and its influences may differ among pollinator species. We, therefore, hypothesized that, for plant species with a generalized pollination system, changes in floral orientation would affect the composition of pollinators and their relative contribution to pollination. Geranium refractum, an alpine plant with downward floral orientation was used in this study. We created upward-facing flowers by altering the flower angle. We compared the pollinator diversity, pollination effectiveness, and pollinator importance, as well as female reproductive success between flowers with downward- and upward-facing orientation. Results indicated that the upward-facing flowers were visited by a wider spectrum of pollinators (classified into functional groups), with higher pollinator diversity than natural flowers. Moreover, due to influences on visitation number and pollen removal, the pollinator importance exhibited by the main pollinator groups differed between flower types. Compared with natural flowers, the pollination contribution of principal pollinators (i.e., bumblebees) decreased in upward-facing flowers and other infrequent pollinators, such as solitary bees and muscoid flies, removed more pollen. Consequently, stigmatic pollen loads were lower in upward- than in downward-facing flowers. These findings reveal that floral orientation may affect the level of generalization of a pollination system and the relative importance of diverse pollinators. In this species, the natural downward-facing floral orientation may increase pollen transfer by effective pollinators and reduce interference by inferior pollinators.     

Secondary pollen presentation: More than to increase pollen transfer precision

Pollination 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.