Status of self-pollen in bee pollination efficiency of white clover (Trifolium repens L.)

Flowers of white clover (Trifolium repens L.) are hermaphrodite and self-incompatible; their cross-pollination depends entirely on insect visitors, mainly bees (Apoidea). Because self-pollination of white clover occurs before flower anthesis, we determined whether selfing affected the pollination efficiency of a honeybee visit. We compared pollen deposition in emasculated and intact flowers following (1) a single honeybee visit, (2) open-pollination for a day and (3) enclosure in a cloth bag to prevent insect visits. In emasculated flowers, open-pollination resulted in more pollen deposited than after one visit (+30%) which is consistent with flowers being visited more than once by pollinators during the course of a day. On intact flowers, saturation of the stigma was achieved after the first visit of a honeybee (near 280 grains) because of self-pollination. Additional visits did not increase pollen deposits, but they improved pollen efficiency in terms of numbers of pollen tubes reaching the ovules. In such a context of easily saturated stigmas, self-pollen does not inhibit cross-pollen activity, but represents a constraint for pollination which demands multiple bee visits to each flower to achieve maximum fertilization. Received: 20 May 1997 / Accepted: 25 October 1997     

Heterostylous morph differences in pollen transfer and deposition patterns in Primula sieboldii on a visitation by a queen bumblebee, measured with a semi-natural experimental system

Abstract Under a semi-natural setting the between-morph pollen exchange patterns were studied in distylous Primula sieboldii flowers by measuring pollen removal from the anthers on a single visit by a Bombus diversus tersatus queen, and stigmatic pollen deposition along the sequence of the visitation of the opposite-morph flowers by the bee. Despite the twofold larger number of pollen grains produced in a single flower of the long-styled morph compared to that of the short-styled morph, no significant difference in pollen removal from a flower was found between the morphs. The stigmas of the long-styled morph received significantly more opposite-morph pollen grains than those of the short-styled morph on a single visit by the bee. Sufficient legitimate pollen grains, surpassing the ovule number, were loaded on the stigmas of 27% and 17% of visited flowers of the long- and short-styled morphs, respectively. The short-styled morph could more efficiently donate pollen to the opposite morph stigmas than the long-styled morph.     

The phenology of gender in homogamous flowers: temporal change in the residual sex function of flowers of Oil-seed Rape (Brassica napus)

1. We investigated the phenology of the male and female sexual functions in flowers of Oil-seed Rape ( Brassica napus ) that were exposed to pollinators in an experimental garden. The female 'residual sex function' (RSF) of flowers was measured by hand-pollinating with genetically marked pollen in order to determine the proportion of ovules that remained available for fertilization by incoming pollen. Male RSF was measured by estimating the proportion of pollen grains that remained in dehiscing anthers.
2. Following flower opening, an average flower's male and female sexual functions each required for completion c. 13 h of exposure to pollinators. One hour after opening, c. 50% of a flower's ovules were unavailable to incoming pollen whereas only c. 10% of pollen was removed. Therefore, a flower's sexual function was predominantly female for the first hour and predominantly male thereafter.
3. We found a fairly close correspondence between the proportion of the stigma covered with pollen and the depletion of female RSF.
4. On average, floral senescence occurred after c. 14·5 h of exposure to pollinators. Our observations are fairly consistent with a simple, economic model of optimal senescence time because the flowers remained open for approximately the same length of time as was necessary for the completion of their sexual functions.
5. A flower's senescence was hastened when pollen was removed from the anthers, but not when pollen was deposited on the stigma.
6. When flowers were either left undisturbed or hand-pollinated, senescence occurred after c. 24 h. Pollen removal caused senescence after c. 13 h, which also approximated the longevity of flowers in the experimental garden. Apparently, pollen removal governed floral longevity under field conditions.     

Floral bagging differentially affects handling behaviours and single-visit pollen deposition by honey bees and native bees

1. Measurements of pollinator performance are crucial to pollination studies, enabling researchers to quantify the relative value of different pollinator species to plant reproduction. One of the most widely employed measures of pollinator performance is single-visit pollen deposition, the number of conspecific pollen grains deposited to a stigma after one pollinator visit. To ensure a pollen-free stigma, experimenters must first bag flowers before exposing them to a pollinator. 2. Bagging flowers, however, may unintentionally manipulate floral characteristics to which pollinators respond. In this study, we quantified the effect of bagging on nectar volume in watermelon (Citrullus lanatus) flowers, and how this affects pollinator performance and behaviour. 3. Experimental bagging resulted in roughly 30-fold increases in nectar volume relative to unmanipulated, open-pollinated field flowers after only a few hours. Honey bees, but not native bees, consistently displayed elevated handling times and single-visit pollen deposition on unmanipulated bagged flowers relative to those from which we removed nectar to mimic volumes in open-pollinated flowers. 4. Furthermore, we identify specific bee foraging behaviours during a floral visit that account for differences in pollen deposition, and how these differ between honey bees and native bees. 5. Our findings suggest that experimental bagging of flowers, without accounting for artificially accumulated nectar, can lead to biased estimates of pollinator performance in pollinator taxa that respond strongly to nectar volume. We advise that pollination studies be attentive to nectar secretion dynamics in their focal plant species to ensure unbiased estimates of pollinator performance across multiple pollinator species.     

Selfing rates in natural populations of Echium vulgare: a combined empirical and model approach

1. We quantified geitonogamous selfing in Echium vulgare , a self-compatible, bumble-bee pollinated plant. A maximum estimate of selfing was determined using a paternity analysis with RAPDs. In the first experiment, bumble-bees visited a sequence of virgin flowers. The percentage selfing increased rapidly from 12% in the first flower visited, up to 50% in the 15th flower visited in the sequence. In the second experiment, when bees visited plants in a natural population, the average selfing of plants increased with the number of open flowers from 0% to maximally 33%.
2. The results obtained in both experiments are consistently lower than predicted by our model on pollen dynamics ( Rademaker, de Jong & Klinkhamer 1997 ). We modified the model on pollen dynamics to link it more to the field situation with observations on flower stage, flower opening and bumble-bee preference, so that the bumble-bees encounter a variable number of pollen grains per flower. We also adjusted the parameters. If less pollen adheres to the bee (25% instead of 50%) after removal from the anthers, or if bees arrive at a plant with more pollen grains (6000 instead of 4448), the predictions of the model in regard to selfing could be improved but were still high compared with the observed selfing rates measured with RAPDs.
3. We suggest that the model is consistent with pollen dynamics in the field. However, post-pollination processes like selective abortion could play a role in E. vulgare .     

Patterns of pollen removal and deposition in tristylous Pontederia cordata L. (Pontederiaceae)

In tristylous Pontederia cordata (Pontederiaceae), conspicuous differences in the size of pollen grains and discrete variation in the length of reproductive organs provide a suitable experimental system for the study of fine-scale pollination events. At a population of P. cordata at Pothole Lake, Ontario, the majority of flowers are visited by bumble bees which remove on average 45% of the pollen during single visits to previously unvisited flowers. The amount and proportion of pollen removed are significantly different among floral morphs and stamen levels. Deposition of the three pollen types on the bodies of Bombus spp., Apis mellifera and Melissodes apicata is non-random: large- and medium-size pollen tends to remain in greatest concentrations where it is initially deposited, whereas small-size pollen is displaced from the proboscis to more posterior body parts, probably as a result of grooming activities. Stigmatic pollen loads of individual flowers following single bumble bee visits indicate that the mid-styled morph captures the largest total pollen load, and the short-styled morph the smallest. The largest proportion of compatible pollen grains is deposited on stigmas of the long-styled morph. Pollen load data from "single visit" flowers is in general agreement with previously published population surveys involving multiply-visited flowers.     

Comparison of pollen transfer dynamics by multiple floral visitors: experiments with pollen and fluorescent dye

BACKGROUND AND AIMS: Most plant species are visited by a diversity of floral visitors. Pollen transfer of the four most common pollinating bee species and one nectar-robbing bee of the distylous plant Gelsemium sempervirens were compared. METHODS: Naturally occurring pollen loads carried by the common floral visitor species of G. sempervirens were compared. In addition, dyed pollen donor flowers and sequences of four emasculated recipient flowers in field cages were used to estimate pollen transfer, and the utility of fluorescent dye powder as an analogue for pollen transfer was determined. KEY RESULTS: Xylocopa virginica, Osmia lignaria and Habropoda laboriosa carried the most G. sempervirens pollen on their bodies, followed by Bombus bimaculatus and Apis mellifera. However, B. bimaculatus, O. lignaria and H. laboriosa transferred significantly more pollen than A. mellifera. Nectar-robbing X. virginica transferred the least pollen, even when visiting legitimately. Dye particles were strongly correlated with pollen grains on a stigma, and therefore provide a good analogue for pollen in this system. The ratio of pollen : dye across stigmas was not affected by bee species or interactions between bee species and floral morphology. However, dye transfer was more sensitive than pollen transfer to differences in floral morphology. CONCLUSIONS: The results from this study add to a growing body of literature highlighting that floral visitors vary in pollination effectiveness, and that visitors carrying the most pollen on their bodies may not always be the most efficient at depositing pollen on stigmas. Understanding the magnitude of variability in pollinator quality is one important factor for predicting how different pollinator taxa may influence the evolution of floral traits.     

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.     

Evidence for mutualism between a flower-piercing carpenter bee and ocotillo: use of pollen and nectar by nesting bees

Abstract.

• 1 Carpenter bees (Xylocopa californica arizonensis) in west Texas, U.S.A., gather pollen and ‘rob’ nectar from flowers of ocotillo (Fouquieria splendens). When common, carpenter bees are an effective pollen vector for ocotillo. We examined ocotillo's importance as a food source for carpenter bees.
• 2 The visitation rate of carpenter bees to ocotillo flowers in 1988 averaged 0.51 visits/flower/h and was 4 times greater than that of queen bumble bees (Bombus pennsylvanicus sonorus), the next most common visitor. Nectar was harvested thoroughly and pollen was removed from the majority of flowers. Hummingbird visits were rare.
• 3 Pollen grains from larval food provisions were identified from sixteen carpenter bee nests. On average, 53% of pollen grains sampled were ocotillo, 39% were mesquite (Prosopis glandulosa), and 8% were Zygophyllaceae (Larrea tridentata or Guaiacum angustifolium). Carpenter bee brood size averaged 5.8 per nest.
• 4 We measured the number of flowers, and production of pollen and nectar per flower by mature ocotillo plants, as well as the quantity of pollen and sugar in larval provisions. An average plant produced enough pollen and nectar sugar to support the growth of eight to thirteen bee larvae. Ocotillo thus has the potential to contribute significantly to population growth of one of its key pollinators.
• 5 Although this carpenter bee species, like others, is a nectar parasite of many plant species, it appears to be engaged in a strong mutualism with a plant that serves as both a pollen and as a nectar source during carpenter bee breeding periods.

     

Do consecutive flower visits within a crown diminish fruit set in mass‐flowering Hancornia speciosa (Apocynaceae)?

Hancornia speciosa is a self-incompatible, mass-flowering, sphingophilous fruit crop (mangaba) of northeast and central Brazil. The flowers have a precise pollination apparatus, which optimizes pollen transfer between flower and pollinator. While the pollination mechanism avoids self-pollination, mass-flowering promotes geitonogamy. During a flower visit, almost half of the exogenous pollen grains adhering to the proboscis are deposited on the stigma surface. A pollination experiment with a nylon thread simulating six consecutive flower visits within a crown revealed that only the first two flowers visited (positions 1 and 2) are highly likely to set fruit. Super-production of flowers, and consequently obligate low fruit set, seem to be part of the reproductive strategy of the obligate outcrossing plant, Hancornia speciosa.     

Sexual interference within flowers of Chamerion angustifolium

Hermaphroditism is prevalent in plants but may allow interference between male function (pollen removal and dispersal) and female function (pollen receipt and seed production) within a flower. Temporal or spatial segregation of gender within a hermaphroditic flower may evolve to reduce this interference and enhance male and female reproductive success. We tested this hypothesis using Chamerion angustifolium (Onagraceae), in which pollen removal (male) and pollen deposition (female) were measured directly on hermaphroditic and experimentally produced unisexual flowers. During a single flower visit in the field, bees deposited 159±24 (SE) pollen grains on a stigma and removed 1058±198 grains from each flower. Anther removal did not alter deposition rates. In the laboratory, bees removed 2669±273 pollen grains and deposited 209±72.3 cross-pollen and 120±28.4 facilitated self-pollen grains per visit. The presence of anthers significantly reduced cross-pollen deposition on the stigma. In contrast, pollen removal was not affected by presence of the pistil. These results suggest that within-flower interference affects female function and represents a fitness cost that can be reduced through temporal segregation of gender within the flower. Co-ordinating editor: S.-M. Chang     

Pollen transfer by hummingbirds and bumblebees, and the divergence of pollination modes in Penstemon

We compared pollen removal and deposition by hummingbirds and bumblebees visiting bird-syndrome Penstemon barbatus and bee-syndrome P. strictus flowers. One model for evolutionary shifts from bee pollination to bird pollination has assumed that, mostly due to grooming, pollen on bee bodies quickly becomes unavailable for transfer to stigmas, whereas pollen on hummingbirds has greater carryover. Comparing bumblebees and hummingbirds seeking nectar in P. strictus, we confirmed that bees had a steeper pollen carryover curve than birds but, surprisingly, bees and birds removed similar amounts of pollen and had similar per-visit pollen transfer efficiencies. Comparing P. barbatus and P. strictus visited by hummingbirds, the bird-syndrome flowers had more pollen removed, more pollen deposited, and a higher transfer efficiency than the bee-syndrome flowers. In addition, P. barbatus flowers have evolved such that their anthers and stigmas would not easily come into contact with bumblebees if they were to forage on them. We discuss the role that differences in pollination efficiency between bees and hummingbirds may have played in the repeated evolution of hummingbird pollination in Penstemon.     

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.     

Selection for pollination success and the mechanical fit of Imfiatiens flowers around bumblebee bodies

Selection on flowers has often been viewed as being particularly strict, constant, and responsible for species differences. Impatiens pallida and I . capensis flowers fit snugly around bees, leading one to expect a close relationship between floral morphology and pollination success. My studies on the amount of pollen removed from androecia and deposited on stigmas in single visits by bumblebees did not confirm this supposition. Trimming off parts of the floral vestibule with scissors and gluing in pleats had very little effect on die amount of pollen that bees moved. In reciprocal transfer experiments, flowers from different populations sometimes differed in the amount of pollen moved, but when the two species were compared in sympatry, pollen removal and deposition differed hardly at all. A comparison of the relationship between pollen movement and floral morphology among 15 populations showed that, although there was great heterogeneity in die amount of pollen moved, the observed differences were independent of floral morphology. None of this supports a belief in strong selection that fine-tunes the mechanical fit between bee and flower; selection for visitation success based on pollinator behaviour may have a much stronger influence on floral characters.     

An estimate of pollen carryover by ants in a natural population of Scleranthus perennis L. (Caryophyllaceae)

Summary Pollen carryover by ants was estimated in a natural population of Scleranthus perennis L. (Caryophyllaceae) using fluorescent dye as a pollen analogue.A highly significant exponential decrease in deposition of dye grains in a sequence of flowers visited by the main flowr visitor, Formica (S.) rufibarbis F., was observed with most grains being deposited in the first few flowers visited. At most 12 flowers were visited in a sequence.The mean between-flower transfer distance was estimated to be 6.2 cm, within-plant pollen transfers being recorded as zero. When all within-plant movements were excluded the mean was 22.5 cm. The distribution of transport distances differed from what I observed for honey-bees which occasionally foraged on dense stands of S. perennis. Calculations made on the deposition of dye grains transferred by ants showed that 7% of the dye grains deposited in the first flower visited after the dye source may reach a flower situated c. 30 cm from the dye source.     

Pollen placement and reproductive isolation between two brazilianPolygala species (Polygalaceae)

Polygala vauthieri andP. monticola var.brizoides have secondary pollen presentation from a basket-like structure on the style apex. This basket is loaded after the first visit by a bee. Pollen reception, therefore, can precede the issue of pollen. A sticky stigma secretion glues the pollen from the basket under the head of the bee visitor in an exactly predetermined spot on the left side only. This position mostly forms a kind of safe spot, where the bee can not remove the pollen. The exact position on the bee's head is determined by the species specific distance between style tip and nectary in the visited flower. In this way the two sympatric species deposit the pollen 2 mm apart on the visitor and so can avoid hybridization pollination, while being visited by the same group of bees.     

The effects of nectar addition on pollen removal and geitonogamy in the non-rewarding orchid Anacamptis morio

It has been suggested that the absence of floral rewards in many orchid species causes pollinators to probe fewer flowers on a plant, and thus reduces geitonogamy, i.e. self-pollination between flowers, which may result in inbreeding depression and reduced pollen export. We examined the effects of nectar addition on pollinator visitation and pollen transfer by tracking the fate of colour-labelled pollen in Anacamptis morio, a non-rewarding orchid species pollinated primarily by queen bumble-bees. Addition of nectar to spurs of A. morio significantly increased the number of flowers probed by bumble-bees, the time spent on an inflorescence, pollinarium removal and the proportion of removed pollen involved in self-pollination through geitonogamy, but did not affect pollen carryover (the fraction of a pollinarium carried over from one flower to the next). Only visits that exceeded 18 s resulted in geitonogamy, as this is the time taken for removed pollinaria to bend into a position to strike the stigma. A mutation for nectar production in A. morio would result in an initial 3.8-fold increase in pollinarium removal per visit, but also increase geitonogamous self-pollination from less than 10% of pollen depositions to ca. 40%. Greater efficiency of pollen export will favour deceptive plants when pollinators are relatively common and most pollinaria are removed from flowers or when inbreeding depression is severe. These findings provide empirical support both for Darwin's contention that pollinarium bending is an anti-selfing mechanism in orchids and for the idea that floral deception serves to maximize the efficiency of pollen export.     

The interaction between pollinator size and the bristle staminode of Penstemon digitalis (Scrophulariaceae)

Penstemon digitalis, a prairie species whose flowers possess a large bristle staminode, is visited by eight bee species of varying size. Two sets of field experiments involving staminode removal were performed to test pollination efficiency in relation to bee size. Our data indicate that bristle staminode presence and function are influenced by size-dependent selection on bee body size and associated pollen transporting attributes. The first experiment compared staminode presence and removal in open-pollinated flowers. Staminode removal significantly reduced total pollen deposition but had no effect on total pollen removal. The second experiment utilized single bee visits to assess the interaction between pollinator size and staminode presence on the rate of pollen deposition and removal. This experiment indicated that staminode removal resulted in fewer pollen grains deposited on stigmas and less pollen removed from anthers for both large and small bees (the contrary was true for medium bees). Although the number of pollen grains deposited was greatly reduced for large bees, staminode removal reduced deposition efficiency most notably for small bees by 41.3%, reducing female reproductive success. Staminode removal increased pollen removal efficiency most notably for medium bees by 22.7%, reducing male reproductive success. Mechanisms of staminode function are discussed.     

Solitary and social bees as pollinators of Wahlenbergia (Campanulaceae): single-visit effectiveness, overnight sheltering and responses to flower colour

Solitary bees often form specialised mutualisms with particular plant species, while honeybees are considered to be relatively opportunistic foragers. Thus, it may be expected that solitary bees are more effective pollinators than honeybees when foraging on the same floral resource. To test this, we studied two Wahlenbergia species (Campanulaceae) in South Africa that are visited by both social honeybees and solitary bees, and which are shown here to be genetically self-incompatible and thus reliant on pollinator visits for seed production. Contrary to expectation, the solitary bee Lipotriches sp. (Halictidae) and social bee Apis mellifera (Apidae), which were the two most frequent visitors to flowers of the study species, were equally effective pollinators in terms of the consequences of single visits for fruit and seed set. Both bee species preferentially visited female phase flowers, which contain more nectar than male phase flowers. Male solitary bees of several genera frequently shelter overnight in flowers of both Wahlenbergia species, but temporal exclusion experiments showed that this behaviour makes little contribution to either seed production or pollen dispersal (estimated using a dye particle analogue). Manipulation of flower colour using a sunscreen that removed UV reflectance strongly reduced visits by both bee groups, while neither group responded to Wahlenbergia floral odour cues in choice tests. This study indicates that while flowers of Wahlenbergia cuspidata and W. krebsii are pollinated exclusively by bees, they are not under strong selection to specialise for pollination by any particular group of bees.     

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.