The effect of wild radish floral morphology on pollination efficiency by four taxa of pollinators

The effects of floral morphology on rates of pollen removal and deposition by different pollinators in generalist plant species are not well known. We studied pollination dynamics in wild radish, Raphanus raphanistrum, a plant visited by four groups of pollinators: honey bees, small native bees, butterflies, and syrphyd flies. The effects of anther position and other factors on pollen removal during single visits by all four pollinator taxa were measured. Flowers with high anther exsertion (i.e., anthers placed higher above the opening of the corolla tube) tended to have the highest numbers of pollen grains removed, but this effect was strongest for honey bees and butterflies. For all pollinator taxa, pollen removal increased with the number of pollen grains available on a flower and whowed a positive, decelerating relationship with the duration of the visit. The effects of stigma position and other factors on pollen deposition during single visits by honey bees and butterflies were also studied. The nectar-feeding butterflies had a higher pollination efficiency (percentage of pollen grains removed from anthers that were subsequently deposited on a stigma) than the nectar- and pollen-feeding honey bees. Flowers with intermediate stigma exsertion had the highest numbers of pollen grains deposited on their stigmas by butterflies, but stigma exsertion had no effect on deposition by honey bees. For both butterflies and honey bees, pollen deposition on the recipient flower increased with the amount of pollen removed from the donor flower, and there was a positive, decelerating relationship between deposition and time spent at the flower; these results are analogous to those for pollen removal. The effects of anther and stigma exsertion on pollen removal and denosition did not fit predictions based on patterns of floral correlations, but results for morphology, pollen availability, time spent per visit, and pollinator efficiency are in broad agreement with previous studies, suggesting the possible emergence of some general rules of pollen transfer.     

Floral biology and reproductive isolation by floral scent in three sympatric aroid species in French Guiana

We studied the reproductive biology of three sympatric Araceae species, Anthurium sagittatum, A. thrinax and Spathiphyllum humboldtii in French Guiana. The plants flowered simultaneously and were visited by scent‐collecting male euglossine bees, which were apparently their major pollinators. In total, each species was visited by 3–7 euglossine species, and 2–3 euglossine species accounted for at least 80% of all flower visits, with visits being plant species‐specific. Floral scent consisted of 6–10 main compounds, which made up 76–94% of the total amount of volatiles and were specific in these high amounts to each plant species. We suggest that the different floral scents lead to clear separation of the main pollinating euglossine species, providing a directed and efficient intraspecific pollen flow that results in high reproductive success. Since the simple floral (inflorescence) morphology of the studied plants does not support any morphological mechanisms to exclude visitors, as for example in euglossine‐pollinated perfume orchids, floral scent might be of major importance for the reproductive isolation and sympatric occurrence of these plants.     

Biotic Resource Needs of Specialist Orchid Pollinators

Orchid pollinators have highly varied life histories with complex biotic resource requirements, about which we have limited knowledge. Among the specialist orchid pollinators are insect predators and parasitoids with specific prey types such as aphids and subterranean scarab larvae; oligolectic bees that collect pollen from limited sources such as bellflowers; euglossine bees and butterflies that collect particular plant chemicals for reproduction and self defense; oil-collecting bees that provision their brood cells with floral oils from a few plants; bees that collect rare floral resins to construct their nest and brood cells; moths and butterflies that require specific larval host plants; mosquitos and horse flies that need blood; and fungus gnats and carrion flies tied to fungi and dead animals. Loss of critical biotic resources and relationships can reduce the abundance of orchid pollinators and/or their effectiveness. Protection of large, plant rich, pesticide-free orchid habitats is key to conserving essential pollinator resources.     

Fly pollination of Linum lewish (Linaceae)

This study examines the reproductive biology of Linum lewisii Pursh. (Linaceae), a polyphilic species visited by small bees and generalist flies in montane Colorado. L. lewisii plants growing at different sites experience large temporal and spatial variations in pollinator visits. Their ability to attract both dipteran and hymenopteran pollinators allows pollination under varying conditions as pollinator pool composition changes. Although L. lewisii is self-compatible, hand-pollination studies indicate that insects are required for seed production. The relative effectiveness of fly and bee pollinators is assessed in terms of per-visit pollen deposition. Insect visitation patterns are combined with per-visit effectiveness data to evaluate the relative importance of different pollinator groups. Overall, bees tend to be more effective than flies in depositing pollen. However, in many instances flies appear to be responsible for more pollen deposition due to their higher visitation rates.     

RELATIVE POLLINATOR EFFECTIVENESS AND EVOLUTION OF FLORAL TRAITS IN SPATHIPHYLLUM FRIEDRICHSTHALII (ARACEAE)

We studied the relative effectiveness of different pollinators of Spathiphyllum friedrichsthalii Schott for 15 months on Barro Colorado Island, Panama. Pollen-foraging stingless bees (Apidae: Trigona) made 87% of floral visits. Experiments showed that these bees pollinate flowers, and correlations of fruit- and seed-set with visitation frequencies and floral contact times suggested that they were responsible for the majority of seeds produced. Fifteen species of fragrance-foraging, male euglossine bees (Apidae: Euglossini) collectively accounted for a small portion of seed-set in fewer than 27% of the inflorescences. Neocorynura (Halictidae) were pollen thieves and were unimportant as pollinators. We propose that euglossine and stingless bees differentially influence outcrossing rates and the evolution of floral traits of S. friedrichsthalii. Foraging behavior of male euglossines should allow for more long-distance pollen flow whereas stingless bees are likely to promote near-neighbor and geitonogamous pollinations. We discuss why the prolonged male phase of anthesis in this protogynous species may be maintained through pollination by stingless bees rather than male euglossines. Furthermore, although the floral fragrance is attractive to many species of male euglossines, it attracts few individuals. This condition may represent an intermediate step in the evolution of predominant pollination by male euglossines.     

Butterfly pollination and high-contrast visual signals in a low-density distylous plant

In low-density butterfly-pollinated Mussaenda frondosa (Rubiaceae), flowers attract pollinators at short distances while conspicuous, non-rewarding accessory bracts are detectable at long distances by long-ranging pollinators such as the birdwing butterfly Troides minos that did not detect flower-bearing plants in the absence of these bracts. However, even in the absence of flowers, the white, ultraviolet-absorbing bracts attracted butterflies that visited flowerless plants. Although flower visits by short-ranging territorial butterflies declined significantly on removal of bracts, they did not cease completely. Nectar-robbing carpenter bees and birds did not change their behaviour following bract removal. Bract removal caused a significant decline in fruit set, indicating their importance as visual signals to pollinators.     

Honey bees and wild pollinators differ in their preference for and use of introduced floral resources

Introduced plants may be important foraging resources for honey bees and wild pollinators, but how often and why pollinators visit introduced plants across an entire plant community is not well understood. Understanding the importance of introduced plants for pollinators could help guide management of these plants and conservation of pollinator habitat. We assessed how floral abundance and pollinator preference influence pollinator visitation rate and diversity on 30 introduced versus 24 native plants in central New York. Honey bees visited introduced and native plants at similar rates regardless of floral abundance. In contrast, as floral abundance increased, wild pollinator visitation rate decreased more strongly for introduced plants than native plants. Introduced plants as a group and native plants as a group did not differ in bee diversity or preference, but honey bees and wild pollinators preferred different plant species. As a case study, we then focused on knapweed (Centaurea spp.), an introduced plant that was the most preferred plant by honey bees, and that beekeepers value as a late‐summer foraging resource. We compared the extent to which honey bees versus wild pollinators visited knapweed relative to coflowering plants, and we quantified knapweed pollen and nectar collection by honey bees across 22 New York apiaries. Honey bees visited knapweed more frequently than coflowering plants and at a similar rate as all wild pollinators combined. All apiaries contained knapweed pollen in nectar, 86% of apiaries contained knapweed pollen in bee bread, and knapweed was sometimes a main pollen or nectar source for honey bees in late summer. Our results suggest that because of diverging responses to floral abundance and preferences for different plants, honey bees and wild pollinators differ in their use of introduced plants. Depending on the plant and its abundance, removing an introduced plant may impact honey bees more than wild pollinators.     

Effects of low-efficiency pollinators on plant fitness and floral trait evolution in <Emphasis Type="Italic">Campanula americana</Emphasis> (Campanulaceae)

Floral visitors vary in their pollination efficiency and their preferences for floral traits. If low-efficiency pollinators decrease the amount of pollen available to higher efficiency visitors, then low-efficiency visitors may actually have negative fitness consequences for the plants that they visit. We used experimental arrays in two populations to determine the floral preferences and the fitness effects of low-efficiency (or ugly) pollinators on Campanula americana. These ugly pollinators (halictid bees) preferentially visited flowers with pollen over flowers that had had their pollen removed. C. americana pollen color varies quantitatively from light tan to dark purple, and we found that natural variation in pollen color influenced the magnitude of halictid preferences for flowers with pollen. In general, preferences for flowers with pollen were stronger when the ugly pollinators foraged in arrays of flowers with tan-colored pollen than in arrays with purple-colored pollen. When plants received few visits by efficient Bombus pollinators, visits by ugly pollinators significantly decreased siring success relative to plants where visits by ugly pollinators were prevented. In contrast, ugly pollinators did not influence siring success when higher efficiency pollinators were more abundant. Thus, the relationship between low-efficiency pollinators and the plants that they visit varies from commensalistic to antagonistic depending on the presence of other pollinators in the community. Our findings suggest that the negative fitness effects and floral preferences of low-efficiency or ugly pollinators may contribute to the maintenance of a pollen color polymorphism in C. americana.     

Insights from measuring pollen deposition: quantifying the pre-eminence of bees as flower visitors and effective pollinators

Using our accumulated datasets from Kenyan savanna, Mediterranean garigue, UK gardens and heathland, involving 76 plants from 30 families, we present detailed data to quantify the superiority of bees as pollinators of most flowering plants when compared with other flower visitors. Bees provided the majority of visits to study species at all sites, and 33 of the 76 plants received more than 90% of their visits from bees. Furthermore, pollen deposition onto stigmas from single-visit events (SVD, a measure of pollination effectiveness) was significantly higher for bees than non-bees at all the four sites where a major proportion of the flora was sampled. Solitary bees, and also bumblebees in temperate habitats, were the best potential pollinators for most plants in this respect, and significantly out-performed honeybees. Only a few plants were well served by bombyliid flies, and fewer again by larger hoverflies, butterflies, or solitary wasps. Bees also achieved better matches of their visit timing to peak pollen availability (measured indirectly as peak SVD), and made much shorter visits to flowers than did non-bees, permitting a substantially greater visit frequency. Additionally, they deposited significantly lower levels of potentially deleterious heterospecific pollen on stigmas in heathland and Mediterranean garigue, though not in the UK garden with densely clustered high-diversity flowering, or in the Kenyan savanna site with particularly dispersed flowering patches and some specialist non-bee flowers. Our data provide a novel and quantified characterisation of the specific advantages of bees as flower visitors, and underline the need to conserve diverse bee communities.     

Pollinator visitation in populations of tristylous Eichhornia paniculata in northeastern Brazil

Summary The frequencies of floral morphs in populations of tristylous Eichhornia paniculata often deviate from the theoretical expectation of equality. This variation is associated with the breakdown of tristyly and the evolution of self-fertilization. Differences in morph frequencies could result from selection pressures due to variable levels of insect visitation to populations and contrasting foraging behavior among the floral morphs. We estimated pollinator densities in 16 populations and quantified visitation sequences to morphs in five populations of E. paniculata in northeastern Brazil. Foraging behavior among floral morphs was measured as the frequency of visits to morphs relative to their frequency in the population (preference) and number of flights between inflorescences of the same versus different morphs (constancy). Pollinator density (number/m²/minute) was not correlated with population size, plant density or morph diversity. Pollinator densities varied most among populations of less than 200 plants. Whether pollinators discriminated among the morphs, depended on whether they primarily collected nectar or pollen. In four populations, nectar-feeding bees (Ancyloscelis and Florilegus spp.) and butterflies showed no consistent preference or constancy among the morphs. In contrast, pollen-collecting bees (Trigona sp.) visited a lower proportion of longstyled inflorescences than expected and tended to visit more mid-and short-styled inflorescences in succession, once they were encountered. Pollinator constancy for morphs did not result from differences in inflorescence production or spatial patchiness among the morphs. Although non-random pollinator visitation to morphs in heterostylous populations could potentially affect mating and hence morph frequencies, the observed visitation patterns in this study do not provide evidence that pollinators play a major role in influencing floral morph frequencies.     

Foraging behavior affects pollen removal and deposition in Impatiens capensis (Balsaminaceae)

Flowers of most plant species are visited by a variety of animals. Some of these visitors are effective pollinators while others remove resources without transferring pollen. Studies comparing the effectiveness of different visitors as pollinators often compare taxa without considering variation in behavior within a taxon. Wilson and Thomson (Ecology 72: 1503-1507, 1991) documented the effects of honey bees and bumble bees on the pollination dynamics of Impatiens capensis. They found that pollen-collecting honey bees removed large numbers of pollen grains from anthers but deposited little of it on stigmas; bumble bees, which sought nectar, removed less pollen but deposited more of it on stigmas. It is unclear whether the low pollen transfer efficiencies of honey bees are explained by their morphology or by their pollen-collecting behavior. We repeated the work of Wilson and Thomson at a site where honey bees were foraging for nectar, not pollen. We measured the quantity of pollen remaining in anthers, the number of pollen grains deposited on stigmas, and seed production after single visits by honey bees and bumble bees. The differences between the taxa disappeared when they were foraging in a similar manner. Our results clearly demonstrate the importance of foraging behavior on the pollination effectiveness of floral visitors.     

Evaluation of pollinator effectiveness based on pollen deposition and seed production in a gynodieocious alpine plant,Cyananthus delavayi

Examining variations in pollinator effectiveness can enhance our understanding of how pollinators and plants interact. Pollen deposition and seed production after a single visit by a pollinator are often used to estimate pollinator effectiveness. However, seed production is not always directly related to pollen deposition because not all pollen grains that are deposited on a stigma are compatible or conspecific. In the field, we tested pollinator effectiveness based on pollen deposition and the resulting seed production after single visits by different pollinator groups in a gynodieocious alpine plant Cyananthus delavayi (Campanulaceae). Our results showed that mean pollen deposition was generally inconsistent with mean seed production when comparisons were performed among different pollinator groups and sexes. In general, the correlations were not significant between pollen deposition and seed production in both perfect and female flowers after single visits by halictid bees, bumble bees, and hoverflies. We suggest seed set of virgin flowers after single visits is a more reliable indicator of pollinator effectiveness than pollen deposition and would be a better indicator of pollinator effectiveness for future studies.     

Differences in pollinator effectiveness of birds and insects visiting Banksia menziesii (Proteaceae)

Summary The effectiveness of nectarivorous birds, introduced honey bees and staphylined beetles as pollinators of Banksia menziesii was assessed. Staphylinids removed substantial amounts of pollen but did not deposit any onto stigmata. Abundance of beetles on inflorescences was related to the mean number of florets opening per day. Honey bees collecting pollen were more likely to effect pollination than those collecting nectar which only contacted stigmata when arriving or leaving an inflorescence. Nectar-foraging birds probed between florets 10.2±0.8 (±SE) times, contacting 8–16 stigmata during each probe. Bees visited inflorescences ten times more frequently than birds although they deposited only 25% of the pollen that birds did on stigmata. Fruit set was ten times greater on inflorescences visited by birds than on inflorescences visited by bees. Bees were capable of removing as much pollen as birds but, because of direct pollen transfer to birds when florets opened during foraging, actual removal was probably much less. Selection for floret opening during nectar foraging by birds may have resulted from pollen removal by non-pollinating animals, such as staphylinids.     

Mobility of Impatiens capensis flowers: effect on pollen deposition and hummingbird foraging

Flexible pedicels are characteristic of birdpollinated plants, yet have received little attention in studies of hummingbird-flower interactions. A major implication of flexible pedicels is that flowers may move during pollination. We examined whether such motion affected interactions between ruby-throated hummingbirds (Archilochus colubris) and jewelweed (Impatiens capensis) by increasing pollen deposition and by altering the effectiveness of nectar removal. For I. capensis, flower mobility enhanced pollen deposition: birds had significantly longer contact with anthers and more pollen deposited on their bills and crowns when foraging at mobile flowers than at flowers that had been experimentally immobilized. In contrast, flower mobility imposed a cost on hummingbirds by significantly increasing their handling times and reducing their extraction rates relative to their interactions with immobile flowers. Field observations indicated that the motion observed during hummingbird visits did not occur when bees (Bombus spp., Apis mellifera) visited I. capensis flowers, which suggests that the mobility of I. capensis flowers is an adaptation for hummingbird pollination.     

Pollinator effectiveness of native and non‐native flower visitors to an apparently generalist Andean shrub,Duranta mandonii (Verbenaceae)

Not all visitors to flowers are pollinators and pollinating taxa can vary greatly in their effectiveness. Using a combination of observations and experiments we compared the effectiveness of introduced honeybees with that of hummingbirds, native bees and moths on both the male and female components of fitness of the Andean shrub Duranta mandonii (Verbenaceae). Our results demonstrated significant variation among flower visitors in rates of visitation, pollen removal ability and contribution to fruit set. This variation was not always correlated; that is, taxa that regularly visited flowers did not remove the most pollen or contribute to fruit set. Despite the taxonomic diversity of visitors, the main natural pollinators of this shrub are large native bees, such as Bombus spp. Introduced honeybees were found to be as effective as native bees at pollinating this species. Duranta mandonii has high apparent generalization, but low realized generalization and can be considered to be a moderate ecological generalist (a number of species of large bees provide pollination services), but a functional specialist (most pollinators belong to a single functional group). The present study has highlighted the importance of measuring efficiency components when documenting plant–pollinator interactions, and has also demonstrated that visitation rates may give little insight into the relative importance of flower visitors.     

The influence of distinct pollinators on female and male reproductive success in the Rocky Mountain columbine

Although there are many reasons to expect distinct pollinator types to differentially affect a plant's reproductive success, few studies have directly examined this question. Here, we contrast the impact of two kinds of pollinators on reproductive success via male and female functions in the Rocky Mountain columbine, Aquilegia coerulea . We set up pollinator exclusion treatments in each of three patches where Aquilegia plants were visited by either day pollinators (majority bumble bees), by evening pollinators (hawkmoths), or by both (control). Day pollinators collected pollen and groomed, whereas evening pollinators collected nectar but did not groom. Maternal parents, potential fathers and progeny arrays were genotyped at five microsatellite loci. We estimated female outcrossing rate and counted seeds to measure female reproductive success and used paternity analysis to determine male reproductive success. Our results document that bumble bees frequently moved pollen among patches of plants and that, unlike hawkmoths, pollen moved by bumble bees sired more outcrossed seeds when it remained within a patch as opposed to moving between patches. Pollinator type differentially affected the outcrossing rate but not seed set, the number of outcrossed seeds or overall male reproductive success. Multiple visits to a plant and more frequent visits by bumble bees could help to explain the lack of impact of pollinator type on overall reproductive success. The increase in selfing rate with hawkmoths likely resulted from the abundant pollen available in experimental flowers. Our findings highlighted a new type of pollinator interactions that can benefit a plant species.     

Diurnal and nocturnal pollination of Silene alba (Caryophyllaceae)

Flowers that are open for >12 h may be visited by both diurnal and nocturnal pollinators. I compared the effectiveness (measured as seed production and pollen movement distance) of diurnal and nocturnal pollinators of Silene alba, a species whose flowers open in evening but close by midmorning the following day. By bagging flowers either during evening hours or during daylight hours or both day and night, I compared seed production caused by diurnal and nocturnal pollinators. Flowers exposed only to nocturnal visitors (mostly sphingid and noctuid moths) produced significantly more seeds than flowers exposed only to diurnal visitors (bees, flies, and wasps). Fluorescent dye applied to anthers moved significantly further and to more stigmas at night than during the day. In both measures of pollination effectiveness, nocturnal-visiting moths are better pollinators of S. alba than are the diurnal-visiting bees, flies, and wasps. These data support the hypothesis that floral phenology is an adaptation to expose flowers to the most effective pollinators.     

How do visitation patterns vary among pollinators in relation to floral display and floral design in a generalist pollination system?

Diverse pollinator assemblages may impose complex selection and thus limit specialisation to particular pollinators. Previous work has concentrated on how visitation rates of different pollinators vary in space and time and how pollinators may vary in efficiency. In this study I quantify variation in visitation rates and foraging behaviour of different insect types (1) in space and time and (2) in relation to variation in floral design (flower size and form) and floral display (number of open flowers) for the distylous clonal shrub Jasminum fruticans. Mean visitation rate showed a significant interaction between insect type and population for seven populations in one year, and between insect types and years for a single population over 3 years. There was also a significant interaction between insect type and population for the proportion of flowers visited. In general the number of visits was positively related to the number of open flowers in a patch, but analyses by insect type showed that this was only true for bee flies and butterflies. Short-tongued bees showed a positive relationship between visitation rate and the number of open flowers on the focal stem, and hawkmoths and butterflies made more visits to plants with larger flowers. Hawkmoths were the only insect type to show a positive relation between the number of flowers visited per foraging bout and flower size. The significant differences between different insect types in patterns of variation in visitation rates in response to floral design and display may act to diversify selection on floral traits, and thereby constrain specialisation of the plant to particular pollinators.     

The relative importance of solitary bees and syrphid flies as pollinators of two outcrossing plant species in the New Zealand alpine

Pollinators vary in their relative contribution to the conspecific pollen deposited onto receptive stigmas, because of variation in both visitation rate and effectiveness of pollen transfer. Syrphid flies and short‐tongued solitary bees are common flower visitors in alpine New Zealand, yet their relative importance as pollinators is unknown. We measured pollinator performance of the New Zealand alpine endemics Hylaeus matamoko (Hymenoptera: Colletidae) and Allograpta spp. (Diptera: Syrphidae) on two New Zealand alpine herbs, Ourisia glandulosa (Plantaginaceae) and Wahlenbergia albomarginata (Campanulaceae). Ourisia glandulosa received visits by solitary bees and syrphid flies at equal frequencies, whereas W. albomarginata was mostly visited by H. matamoko. Based on single‐visit pollen deposition to virgin stigmas, H. matamoko was a much more effective pollinator than Allograpta spp., delivering 10 times as much pollen per visit to O. glandulosa stigmas and 3 times as much to W. albomarginata stigmas. By multiplying visitation frequency by single‐visit pollen deposition, we estimated that H. matamoko performed 90% and 95% of the pollination of O. glandulosa and W. albomarginata, respectively. Although H. matamoko bees are short‐tongued and small in size, they are critically important to plant reproductive success in the New Zealand alpine. These bees contributed most of the pollination, even to a species that received just as many visits by flies, underscoring the need to consider per‐visit effectiveness as well as visitation rate in assessing the importance of different pollinators.     

Effects of variation in inflorescence size and floral rewards on the visitation rates of traplining pollinators ofAralia hispida

Summary In field experiments withAralia hispida inflorescences, the following variables were manipulated: number of umbels per inflorescence, number of flowers per umbel, and amounts of pollen and nectar per flower. Visitation rates by bumble bees, the principal pollinators, were then observed. In the reward-variation experiments, bees appeared to learn the positions of nectar-rich shoots, and visited them significantly more often than nectar-poor shoots. They did not respond to similar variation in pollen production. The nectar preferences developed slowly after the treatments were imposed, and bees continued to favor sites that had been occupied by nectar-rich shoots even after the treatments were discontinued. Visitation rate was approximately proportional to flower number, making it unlikely that increases in inflorescence size produced a disproportionate gain in male reproductive success (a necessary condition in certain models for the evolution of dioecy). For a fixed number of flowers per inflorescence, bees preferred inflorescences with more umbels. In pairwise choice tests of male-phase and female-phase umbels of various sizes, bees preferred male-phase umbels and larger umbels; the preference for male-phase umbels is stronger in bees that had previously fed on male-phase umbels.