Pollination system and its significance on isolation and hybridization in JapaneseEpimedium (Berberidaceae)

Observations on native populations of JapaneseEpimedium have revealed that two types of effective pollinators can be recognized. One of the two types, which consists of small bees (mainlyAndrena spp. andLasioglossum spp.), is characterized by nondiscriminating behavior for collecting pollen and is commonly found inEpimedium. The other type, which comprises medium sizedTetralonia nipponensis and largerBombus diversus queens as main components, showed flower-dependent foraging fidelity associated with nectar-sucking behavior.T. nipponensis with a shorter proboscis pollinated flowers with a shorter spur ofE. trifoliatobinatum and of a part ofE. s sempervirens, while the queen ofB. diversus with a longer proboscis pollinated longer spurred flowers ofE. grandiflorum andE. sempervirens. In the populations of putative hybrid-derivatives which show gradational variations of spur length, bees of the pollencollecting type pollinated any flower non-discriminately while bees of the nectar-foraging type tended to visit the flowers with spur lengths corresponding to their proboscis length. These observations suggest that the pollen-collecting bees play an important role for gene flow among theEpimedium species, and the nectar-foraging bees reinforce the isolation between the species by their selective pollination. Reproductive isolation between species ofEpimedium is discussed in relation with some practical behavior, such as flying power, of the pollinators.     

FORAGING BEHAVIOR OF BOMBUS (HYMENOPTERA: APIDAE) IN RELATION TO AQUILEGIA POLLINATION

Observations on native and cultivated plants indicated that the ruby-throated hummingbird (Archilochus colubris L.) and at least four species of Bombus are probably effective pollinators of Aquilegia canadensis L. in southeastern Wisconsin. Bombus affinis Cresson perforated more than 90% of 2173 nectar spurs of flowers at full anthesis on wild plants. Cinematographic and stereo-photographic records of insects revealed a general behavioral pattern of mandibular perforation following exploration by antennae, maxillae, and tongue. Pollen-foraging behavior on 19 cultivated Aquilegia species and varieties was uniform, but nectar-foraging behavior varied with flower form and position and not with color variation within one flower form. Observations on marked insects showed that workers tended to forage in one manner on one plant variety, while queens foraging in one or more ways visited up to five different flower forms on one flight. Initial observations on neonate workers from a cultivated B. affinis colony suggested that a probably innate mandibular perforation behavior is not instinctively directed toward nectar-bearing floral parts, and that foraging behavior is capable of rapid establishment and considerable versatility.     

POLLINATION IN FLORAL SCENT MORPHS OF POLEMONIUM VISCOSUM: A MECHANISM FOR DISRUPTIVE SELECTION ON FLOWER SIZE

Plants of Polemonium viscosum have flowers that are either sweet or skunky in scent. The two morphs are preferentially pollinated by insects of strongly contrasting body size: bumblebee queens specialize on sweet flowers, flies on skunky ones. In this study 13 characters were examined in plant specimens from five populations to identify major components of intraspecific variation in flower and inflorescence morphology and test their correlation with floral scent. Factor analysis identified four major axes of morphological variation. The first explained 22% of the variance among specimens and correlated strongly with four flower size characters: sepal length, corolla tube length, corolla lobe width, and corolla lobe length. Floral scent morphs differed significantly in the multivariate representation of flower size defined by these characters. Sweet flowers had wider corolla lobes, longer corolla tubes, and longer sepals than skunky ones. Corolla lobe width accounted for the greatest amount of intermorph divergence. Divergence in flower size between morphs was maintained in mixed populations at four locations in alpine Colorado, with corollas of sweet flowers significantly broader or more flared than those of skunky flowers. Patterns of pollen receipt suggest that this difference is adaptive. In the sweet morph, pollination intensity and purity increased significantly with corolla flare. Conversely, in the skunky morph, corolla flare had little influence on pollination intensity and had a strong negative effect on purity. These findings suggest that selection for effective pollination should favor intraspecific divergence in flower size in Polemonium viscosum.     

POLLINATION ADAPTATION IN PEDICULARIS CANADENSIS

During the spring of 1966 and 1967, operation of the pollination mechanism of Pedicularis canadensis L. flowers by nectar- and pollen-foraging bumblebee (Bombus Latr.) queens was observed in an Iowa relict prairie and was recorded by high-speed cinematography. The stigma and style were found to sweep the forager's pronotum crevice as head and tongue were introduced into the 12-mm corolla tube. Pollen deposited in the crevice was not removed as the forager's middle leg only groomed pollen laterally deposited on head and scutum. Thirty corbicular pollen loads from 417 foragers collected on nine prairie plant species included pollen from Pedicularis canadensis, Aquilegia canadensis L., Dodecatheon meadia L., and two unidentified plants not found in the prairie. The pollination mechanism was considered closely adapted morphologically and phenologically to bumblebee queens of eight species found foraging on Pedicularis.     

THE POLLINATION ECOLOGY OF PEDICULARIS ON MOUNT RAINIER

Six native species of Pedicularis in Mount Rainier National Park in Washington State were studied for their reproductive relationships with animal pollinators. Cinematographic and stereophotographic records revealed pollination of the nectariferous P. bracteosa and P. rainierensis by upright, nectar-foraging queens and workers of five bumblebee (Bombus Latr.) species and by inverted workers scraping pollen from anthers concealed within the corolla galea. The nectarless, rostrate flowers of P. contorta, P. groenlandica, P. ornithorhyncha, and P. racemosa were pollinated by pollen-foraging workers and occasional queens virbrating pollen from concealed anthers. Insect exclosure methods revealed complete absence of fruiting in the absence of insects, and pollinator collections further indicate obligate dependence of the plants upon bumblebees for their sexual reproduction. Analysis of corbicular pollen loads from pollinators suggested that pollinator species are not monolectic but that individual pollinators range from monolectic to polylectic. Measurements indicated limited correlations between lengths of corolla tubes and tongues of nectar-foraging insects. Each nectarless Pedicularis species occupied a different, specific habitat, but P. bracteosa and the endemic P. rainierensis were sympatric in part. Each species had a unique spectral reflectance pattern from the corolla. Proximity of habitats and overlap of blooming periods of all Pedicularis species eliminate the possibility of contemporary geographic or phenological reproductive isolation. It is suggested that behavioral interactions of the plants and their insect pollinators may have been instrumental in the past in reproductively isolating these species, hybrids of which are unknown.     

Bumble bee behavior and selection on flower size in the sky pilot,Polemonium viscosum

Summary In alpine Polemonium viscosum, plants having sweet-scented flowers are primarily pollinated by queens of the bumble bee species, Bombus kirbyellus. In this paper we ask whether two aspects of the pollination effectiveness of bumble bees, visitation rate and pollination efficiency, vary significantly with flower size in sweet-flowered P. viscosum.(i) Bumble bees visited plants with large flowers on 80–90% of encounters, but visited those with smaller flowers on only 49% of encounters. (ii) However, the gain in pollination that large-flowered plants obtained via increased visitation was countered in part because bumble bees deposited fewer outcross pollen grains per visit on stigmas of large flowers than on those of small ones. When both visitation rate and pollination efficiency are taken into account, the predicted value of a single bumble bee encounter declines from 1.06 seeds for flowers larger than 18 mm in diameter to 0.55 seeds for flowers smaller than 12 mm in diameter. Our results suggest that bumble bee pollinators of P. viscosum prefer flower morphologies that are poorly suited for precise pollination. Such behavioral complexities are likely to place constraints on the evolution of optimal floral design.     

Deceptive pollination of the Lady's Slipper Cypripedium tibeticum (Orchidaceae)

To test whether the nectarless flowers of Cypripedium tibeticum attract pollinators through mimicry like the allied species C. macranthos var. rebunense, pollination biology of C. tibeticum was investigated in western China. Although C. tibeticum was also pollinated by bumble bee queens, i.e. Bombus lepidus , B. lucorum and B. hypnorum , no special, rewarding model plants were found in the habitat. Field experimentation confirmed that the flowers were self-compatible but insects were required to transfer orchid pollen to the stigma. Both Bombus queens and workers were visitors, but queens were much more frequent than workers and only queens were effective pollinators. Floral functional morphology analysis showed that it was large queens rather than small workers that fitted well with the flowers of C. tibeticum. With the faint sweet-fruity scent, the minor floral fragrance compound, ethyl acetate, probably plays a role in attracting bumble bees by food deception. The dark flowers with the inflated, trap-like labellum are hypothesized to mimic the nest site of queens. Therefore, bumble bee queens tend to be attracted by C. tibeticum through nest site mimic combined with food deception. Considering that the co-blooming flowers of C. flavum are pollinated by the Bombus workers, and C. smithii pollinated by a queen, we suggest that using the same bumblebees with different body sizes as the pollinators is the main reproductive isolation between interfertile C. tibeticum and C. flavum, while C. tibeticum and C. smithii tend to hybridize naturally.     

Fitness consequences of altering floral circadian oscillations for Nicotiana attenuata

Ecological interactions between flowers and pollinators are all about timing.Flower opening/closing and scent emissions are largely synchronized with pollinator activity,and a circadian clock regulates these rhythms.However,whether the circadian clock increases a plant's reproductive success by regulating these floral rhythms remains untested.Flowers of Nicotiana attenuata,a wild tobacco,diurnally and rhythmically open,emit scent and move vertically through a 140° arc to interact with nocturnal hawkmoths.We tethered flowers to evaluate the importance of flower positions for Manduca sexta-mediated pollinations;flower position dramatically influenced pollination.We examined the pollination success of phase-shifted flowers,silenced in circadian clock genes,NaZTL,NaLHY,and NaTOCi,by RNAi.Circadian rhythms in N.attenuata flowers are responsible for altered seed set from outcrossed pollen.     

The dimorphic heterostyly inAconogonon campanulatum (Polygonaceae)

Heterostyly is clearly confirmed inAconogonon campanulatum. This distylous species is dimorphic for tepals, styles, stigma surface, stamens, pollen grain size, and pollen sexine ornamentation. The floral shape is campanulate and thrum flowers are slightly larger than pin flowers. Small solitary bees were observed as flower visitors and probably effected pollination. The possible evolution of dioecy via heterostyly within the genusAconogonon is discussed.     

Consistent pollination services to Cypripedium macranthos var. rebunense (Orchidaceae) by Bombus pseudobaicalensis

Bombus pseudobaicalensis queens are known pollinators of the threatened orchid Cypripedium macranthos var. rebunense. However, whether other bumblebee species also pollinate this orchid has not yet been ascertained. A 10-year observation provided convincing evidence that B. pseudobaicalensis is the only consistent pollinator. B. beaticola moshkarareppus queens were newly found to rarely carry pollen smears of the orchid, whereas B. hypocrita sapporoensis and B. diversus queens were practically mere flower visitors. Why these three species do not equal B. pseudobaicalensis in pollination effectiveness remains unclear but differences in body size and individual abundance between B. pseudobaicalensis and the other species are considered as possible primary causes. Given the almost complete dependence of C. macranthos var. rebunense on B. pseudobaicalensis for pollination and its potential risk, conservation managers should take care not to reduce the bumblebee colonies.     

Plasticity of flower longevity in Corydalis ambigua

We investigated the longevity of individual flowers of Corydalis ambigua Cham. et Schlecht. during different periods of pollinator activity and at different temperatures. To measure potential (unpollinated) flower longevity of C. ambigua, this study was conducted at forest islands where pollinator visits were scarce. The longevity of individual flowers of C. ambigua indicated high plasticity. The longevity of unpollinated flowers in natural pollination ranged from 2 to 25 days and continuously decreased with the date of flower opening. The temperature increased as the flowering season progressed. Furthermore, the greenhouse transplanting experiment showed that higher temperatures shorten the life span of flowers. The longevity of pollinated flowers subjected to hand pollination of newly opened flowers was shorter than that of unpollinated flowers in natural pollination regardless of the date of flower opening. These results showed that not only high temperature but also pollination shortens flower longevity. We discuss the role of plasticity in flower longevity for C. ambigua in relation to pollination success and reduction in the maintenance cost of the flowers.     

Pollen-Foraging Dynamics of Subalpine Bumblebees (Bombus Latr.)

Abstract A 23-year study on Mount Rainier of nectar-foraging hummingbirds and pollen-foraging bumblebees (Bom-bus Latr.) indicated a constant relative frequency of Bombus species in the area and a wide occurrence of insect species on flowers plus a wide range of flower species pollinated by a single insect. Early-blooming plants had a high queen/worker pollinator ratio, while workers predominated on later-blooming plants. No altitudinal difference in distribution of Bombus species occurred. Analysis of 955 corbicular pollen loads from 1158 bumblebees collected yielded 49.5% monolecty for queens and 34.5% for workers with a wider range for queens than for workers. Colors of corollas photographed in visible and ultraviolet light corresponded to the visual spectra of animal pollinators. In the stable plant-pollinator community investigated, pollinating insect activity appears phenologically controlled by floral anthesis and behaviorally related to floral form and function. Bumblebee tongue length, however. Is not a valid determinant for foraging niche separation except in Castilleja with a deep corolla tube accommodating long tongues of hummingbirds and bumblebees. It is concluded that in a biotic community well-coordinated with the physical environment, limited flower constancy of pollen-foraging pollinators appears to contribute a necessary degree of adaptive versatility through sharing of insect and floral resources. Flower constancy is primarily a function of the circumstance in which a pollinator operates and not simply a characteristic of the pollinator itself.     

Successful pollination of the Neotropical crop Solanum quitoense by Bombus terrestris: behaviour,efficiency and yield

The South American lulo (Solanum quitoense Lam.) is a crop plant of the Andes of Ecuador and Colombia, pollinated by South American bumblebees, such as, Bombus atratus Franklin. The cultivation of lulo outside of its native range, for example in European glasshouses, requires the presence of efficient pollinators to enable high fruit set and yield. Until now, the suitability of Bombus terrestris L., native to Europe and commonly used in agriculture, has been untested for this purpose. In this study, the pollen‐collecting behaviour of B. terrestris when visiting lulo flowers was investigated. It was shown that B. terrestris adopted the lulo as a pollen source, and on average visited three flowers per minute, had five buzzing events per stay and foraged for 15 s on a single flower, independently of the previous number of visits and level of bruising to the anthers. The pollination efficiency of five different treatments was evaluated: (i) exclusion of bees, (ii) single and (iii) multiple visits of B. terrestris, (iv) self‐ and (v) cross‐pollination by hand. The results clearly demonstrated that, for fruit set, pollination is crucial. It was also found that lulo flowers can be successfully self‐pollinated, but give 25% fewer fruit set compared with pollination via multiple bumblebee visits, or cross‐pollination by hand. Fruit set, seed set and fruit size were as high with pollination by B. terrestris as with cross‐pollination by hand, indicating that this bumblebee is an appropriate pollinator for lulo. However, B. terrestris was conspicuously less effective when a flower was visited only once. Therefore, when growing lulos commercially, multiple bumblebee visits should be encouraged, but it is likely that the behaviour of B. terrestris would ensure this anyway. Our results indicate that B. terrestris is a suitable and efficient pollinator for the production of lulo fruits.     

Intra‐floral resource partitioning between endemic and invasive flower visitors: consequences for pollinator effectiveness

1. Sympatric flower visitor species often partition nectar and pollen and thus affect each other's foraging pattern. Consequently, their pollination service may also be influenced by the presence of other flower visiting species. Ants are solely interested in nectar and frequent flower visitors of some plant species but usually provide no pollination service. Obligate flower visitors such as bees depend on both nectar and pollen and are often more effective pollinators. 2. In Hawaii, we studied the complex interactions between flowers of the endemic tree Metrosideros polymorpha (Myrtaceae) and both, endemic and introduced flower‐visiting insects. The former main‐pollinators of M. polymorpha were birds, which, however, became rare. We evaluated the pollinator effectiveness of endemic and invasive bees and whether it is affected by the type of resource collected and the presence of ants on flowers. 3. Ants were dominant nectar‐consumers that mostly depleted the nectar of visited inflorescences. Accordingly, the visitation frequency, duration, and consequently the pollinator effectiveness of nectar‐foraging honeybees (Apis mellifera) strongly decreased on ant‐visited flowers, whereas pollen‐collecting bees remained largely unaffected by ants. Overall, endemic bees (Hylaeus spp.) were ineffective pollinators. 4. The average net effect of ants on pollination of M. polymorpha was neutral, corresponding to a similar fruit set of ant‐visited and ant‐free inflorescences. 5. Our results suggest that invasive social hymenopterans that often have negative impacts on the Hawaiian flora and fauna may occasionally provide neutral (ants) or even beneficial net effects (honeybees), especially in the absence of native birds.     

Pollination biology in Roepera (Zygophyllaceae): How flower structure and shape influence foraging activity

The foraging behavior of bees is a complex phenomenon that depends on numerous physical features of flowers. Of particular importance are accessibility of floral rewards, floral proportions, symmetry and orientation. The flowers of Roepera are characterized by the presence of staminal scales (SS), which play an important role in nectar protection. We studied two species of Roepera with different symmetry and flower orientation, which are mainly visited by honeybees (Apis mellifera). We aimed to show how the foraging behavior of honey bees is affected by the function of SS, floral symmetry and orientation. The foraging behavior was documented by video photography. Handling time, access to nectar, percentage of pollen/nectar foraging, percentage of pollen contact and pollen deposition site on the honey bee's body were assessed. The morphometric features of the honey bees and flowers were analyzed. We found that the SS restricted pollinator access to nectar. Our results indicated consistency of visitation patterns in zygomorphic, laterally oriented flowers of R. fuscata versus random patterns in actinomorphic, diversely oriented flowers of R. leptopetala. The relative proportions of SS and proboscis length appear to be crucial for the success of pollinators. The directionality of the honey bees' movement, together with the different positioning of reproductive organs, plays an important role in the accuracy of pollen transfer and pollination efficiency.     

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.     

Functional Significance of Interspecific Variation in Burmeistera Flower Morphology: Evidence from Nectar Bat Captures in Ecuador

What causes flowers to diverge? While a plant's primary pollinator should strongly influence floral phenotype, selective pressures may also be exerted by other flower visitors or competition with other plants for pollination. Species of the primarily bat‐pollinated genus Burmeistera (Campanulaceae) frequently cooccur, with up to four species in a given site, and broadly overlap in flowering phenology, typically flowering throughout the year. The genus displays extensive interspecific variation in floral morphology in the degree that the reproductive parts (anthers and stigma) are exserted outside of the corolla, and species can be roughly classified as either long or short‐exserted. I tested two hypotheses regarding the functional significance of such variation: (1) exsertion lengths correspond to pollination by bat species of different sizes; and (2) variation serves to partition pollinator's bodies spatially and thus reduces interspecific pollen transfer. I captured bats in Ecuador to evaluate the identity and location of the Burmeistera pollen they were carrying. Results show that exsertion does not correspond to specialization on different pollinators; different bat species carried pollen of both flower types just as frequently. In support of the second hypothesis, pollen from flowers of different exsertion lengths was found to occur on different regions of bats' heads. This may serve to reduce competition for pollination among coexisting Burmeistera.     

In a world of white,flower colour matters: A white–purple transition signals lack of reward in an alpine Euphrasia

The New Zealand alpine flora displays a range of unusual characteristics compared with other alpine floras, in particular the high frequency of species with small white flowers. The presence of both white and bright purple flowers on the same plant in the New Zealand alpine annual creeping eyebright (Euphrasia dyeri Wettst.) provides an ideal opportunity to investigate the significance of flower colour in an environment where coloured flowers are rare. The relationships among flower age, gender phase, reward availability and petal colour were assessed in natural populations of E. dyeri. The effect of pollination on flower colour was tested using hand pollination of bagged flowers. Direct observations and videos of flowers were used to assess patterns of flower visitation by native and introduced pollinators. Unpollinated white E. dyeri flowers changed from white to purple within 6 days. However, pollination of white flowers triggered a significantly faster colour change, typically within 1–2 days. White flowers had receptive stigmas, large amounts of lipid‐rich pollen and small amounts of nectar, whereas stigmas of purple flowers are not receptive and flowers did not provide pollen or nectar rewards. Flowers were mainly visited by native syrphid flies. Both native syrphids and introduced Bombus bees showed a marked avoidance of purple flowers, tending to preferentially visit white flowers. Our study suggests that flower colour change from white to bright purple in E. dyeri functions to direct pollinators to rewarding, receptive flowers. As many Euphrasia L. species are described as having variably coloured flowers, this mechanism may be more widespread in the genus. Furthermore, our results add to the growing evidence that the dominance of white flowers in the New Zealand alpine is not simply due to a lack of colour discrimination among pollinators.     

Sunbird hovering behavior is determined by both the forager and resource plant

The long‐standing paradigm that pollination systems adapted to hovering birds evolved only in the New World was recently challenged by the discovery of hovering pollination by Old World specialized passerine pollinators. This raises the possibility that hovering pollination may evolve more easily than previously believed, given sufficient selective pressure on plant traits, on nectarivory, or both. We observed foraging behavior by the sunbird Cyanomitra oritis at flowers of the native Old World plant Impatiens sakeriana. We measured the length of pedicels and peduncles (PedPed length), which can make the flowers difficult to reach while the bird perches on the stem, and determined if it influenced sunbird hovering or perching at a flower. Detailed analyses of video recordings showed that sunbirds only hovered at flowers with a long PedPed, whereas they employed both foraging modes when an adequate perch was available. A hovering sunbird could deplete nectar in a shorter time than a perching one. The frequency of visits was not greater at flowers with longer PedPed or with more open I. sakeriana flowers in the vicinity. Our study provides evidence that sunbird behavior does not follow simple energetic models, and that some sunbird pollination systems in the Old World resemble highly specialized hummingbird systems in the New World much more than expected, especially the overall adaptation of the system to bird hovering.     

Modification of bumblebee behavior by floral color change and implications for pollen transfer in <Emphasis Type="Italic">Weigela middendorffiana</Emphasis>

Flowers of Weigela middendorffiana change the color from yellow to red. The previous study revealed that red-phase flowers no longer have sexual function and nectar, and bumblebees selectively visit yellow-phase flowers. The present study examined how retaining color-changed flowers can regulate the foraging behavior of bumblebees and pollen transport among flowers within (geitonogamous pollination) and between (outcrossing pollination) plants and how the behavior is influenced by display size (i.e., number of functional flowers) and visitation frequency. The visitation frequencies of bumblebees to plants and successive flower probes within plants were observed in the field using plants whose flower number and composition of the two color-phase flowers had been manipulated. To evaluate pollination efficiency over multiple pollinator visits, a pollen transport model was constructed based on the observed bumblebee behavior. In the simulation, three flowering patterns associated with display size and existence of color-changed flowers were postulated as follows: Type 1, large display (100 functional flowers) and no retention of color-changed flowers; Type 2, small display (50 functional flowers) and retention of color-changed flowers (50 old flowers), and; Type 3, large display (100 functional flowers) and retention of color-changed flowers (100 old flowers). Color-changed flowers did not contribute to increasing bumblebee attraction at a distance but reduced the number of successive flower probes within plants. Comparisons of pollen transfer between Types 1 and 3 revealed that the retention of color-changed flowers did not influence the total amount of pollen exported when pollinator visits were abundant (>100 visits) but decreased geitonogamous pollination. Comparisons between Types 2 and 3 revealed that the discouragement effect of floral color change on successive probes accelerated in plants with a large display size. Overall, the floral color change strategy contributed to reduce geitonogamous pollination, but its effectiveness was highly sensitive to display size and pollinator frequency.