Flowering dynamics and pollination system of the sedge Rhynchospora ciliata (Vahl) Kükenth (Cyperaceae): does ambophily enhance its reproductive success?

Cyperaceae are characteristically anemophilous, but there are some reports of species re‐adapted to entomophily, such as Rhynchospora ciliata. Our objective was to investigate: (1) the distribution pattern of flowers in inflorescences of Rhynchospora ciliata; (2) the dynamics of its anthesis; and (3) whether R. ciliata is pollinated by bees, by wind or by both. Additionally, we tested the hypotheses: (i) the hypsophylls and/or anthers attract pollinators, and (ii) biotic vectors enhance the reproductive success of R. ciliata. We analysed floral biology, dynamics of anthesis, frequency and behaviour of insects visiting flowers; we also carried out experiments on flower attractiveness, pollination by wind and reproductive success. Rhynchospora ciliata has flowers with anemophilous attributes, including anthers exposed during anthesis; however, the anthers (here considered a mixed trait) together with the white hypsophylls can be considered as attributes that favour entomophily. Both wind and four species of bee were considered as pollen vectors of R. ciliata. Through flower attractiveness tests, we observed that the hypsophylls do not affect the frequency of pollinating bees and that the absence of exposed anthers affects the average number of visits, probably because pollen is the only floral resource. Reproductive tests indicate that R. ciliata is self‐incompatible and that ambophily enhances its reproductive success.     

The movement of involucral bracts of Syngonanthus elegans (Eriocaulaceae-Poales): Anatomical and ecological aspects

Syngonanthus elegans flowers are distributed in capitula whose involucral bracts open and close in a diurnal rhythm. The anatomy of these bracts was studied to understand how such movements occur and how it influences reproductive ecology of the species. The involucral bracts have a single layered epidermis composed of thick-walled cells on the abaxial surface, which are responsible for the movement. Since they are hygroscopic, these cells swell when they absorb water from the surrounding environment, causing the bracts to bend and the capitula to close. In natural conditions, the capitula open by day, when temperature increases and the relative air humidity decreases, and close at night, when temperature decreases and the relative air humidity increases. The involucral bracts may thus protect the flowers from abiotic factors, exposing them only at the time of the day when temperature is higher and insects are more active, favoring pollination by small insects. The closed capitula do not only protect the flowers, but they also function as a shelter for floral visitors as Brachiacantha australe (Coccinellidae) and Eumolpini sp. (Chrysomelidae). These small Coleoptera pollinate the flowers of S. elegans during the day and remain within the closed capitula during the night, in a possible mutualistic relationship.     

Relative abundance of an invasive alien plant affects native pollination processes

One major characteristic of invasive alien species is their occurrence at high abundances in their new habitat. Flowering invasive plant species that are visited by native insects and overlap with native plant species in their pollinators may facilitate or disrupt native flower visitation and fertilisation by forming large, dense populations with high numbers of flowers and copious rewards. We investigated the direction of such a proposed effect for the alien invasive Rhododendron ponticum in Irish habitats. Flower visitation, conspecific and alien pollen deposition, fruit and seed set were measured in a self-compatible native focal plant, Digitalis purpurea, and compared between field sites that contained different relative abundances of R. ponticum. Flower visitation was significantly lower at higher alien relative plant abundances than at lower abundances or in the absence of the alien. Native flowers experienced a significant decrease in conspecific pollen deposition with increasing alien abundance. Heterospecific pollen transfer was very low in all field sites but increased significantly with increasing relative R. ponticum abundance. However, lower flower visitation and lower conspecific pollen transfer did not alter reproductive success of D. purpurea. Our study shows that indirect interactions between alien and native plants for pollination can be modified by population characteristics (such as relative abundance) in a similar way as interactions among native plant species. In D. purpurea, only certain aspects of pollination and reproduction were affected by high alien abundances which is probably a result of high resilience due to a self-compatible breeding system. Native species that are more susceptible to pollen limitation are more likely to experience fitness disadvantages in habitats with high relative alien plant abundances.     

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.     

Pollination Ecology and Seed Production of Rhododendron Ponticum in Native and Exotic Habitats

Alien plants may be reproductively limited in exotic habitats because of a lack of mutualistic pollinators. However, if plants are adequately served by generalist pollinators, successful reproduction, naturalisation and expansion into exotic habitats may occur. Rhododendron ponticum is very successful, ecologically damaging invasive plant in Britain and Ireland, but is in decline in its native Iberian habitat. It spreads locally by sending out lateral branches, but for longer distance dispersal it relies on sexually produced seeds. Little is known about R. ponticum's pollination ecology and breeding biology in invaded habitats. We examined the flower-visiting communities and maternal reproductive success of R. ponticum in native populations in southern Spain and in exotic ones in Ireland. R. ponticum in flowers are visited by various generalist (polylectic) pollinator species in both native and exotic habitats. Although different species visited flowers in Ireland and Spain, the flower visitation rate was not significantly different. Insects foraging on R. ponticum in Spain carried less R. ponticum pollen than their Irish counterparts, and carried fewer pollen types. Fruit production per inflorescence varied greatly within all populations but was significantly correlated with visitation at the population level. Nectar was significantly depleted by insects in some exotic populations, suggesting that this invasive species is providing a floral resource for native insects in some parts of Ireland. The generality of the pollination system may be factor contributing to R.ponticum's success in exotic habitats.     

Flower visitation by birds in Europe

Most flowering plants depend on animal pollination. Several animal groups, including many birds, have specialized in exploiting floral nectar, while simultaneously pollinating the flowers they visit. These specialized pollinators are present in all continents except Europe and Antarctica, and thus, insects are often considered the only ecologically relevant pollinators in Europe. Nevertheless, generalist birds are also known to visit flowers, and several reports of flower visitation by birds in this continent prompted us to review available information in order to estimate its prevalence. We retrieved reports of flower–bird interactions from 62 publications. Forty‐six bird species visited the flowers of 95 plant species, 26 of these being exotic to Europe, yielding a total of 243 specific interactions. The ecological importance of bird–flower visitation in Europe is still unknown, particularly in terms of plant reproductive output, but effective pollination has been confirmed for several native and exotic plant species. We suggest nectar and pollen to be important food resources for several bird species, especially tits Cyanistes and Sylvia and Phylloscopus warblers during winter and spring. The prevalence of bird flower‐visitation, and thus potential bird pollination, is slightly more common in the Mediterranean basin, which is a stopover to many migrant bird species, which might actually increase their effectiveness as pollinators by promoting long‐distance pollen flow. We argue that research on bird pollination in Europe deserves further attention to explore its ecological and evolutionary relevance.     

Multifunctional bracts enhance plant fitness during flowering and seed development in Rheum nobile (Polygonaceae), a giant herb endemic to the high Himalayas

Specialized bracts are thought to be important for the successful reproduction of some plants and are regarded as adaptations to diverse driving forces. However, few empirical studies have quantified the adaptive significance of bracts within a cost–benefit framework. We explored the adaptive significance of large and showy bracts for reproduction in Rheum nobile, a giant herb endemic to the high Himalayas. We examined whether the bracts enhance reproductive success during flowering and seed development. Bracts increased flower and fruit temperature on sunny days, greatly decreased the intensity of ultraviolet-B (UV-B) radiation reaching flowers and fruits, and prevented pollen grains being washed away by rain. Experiments indicated that high temperature could promote pollen germination, while pollen grains exposed to rain and UV-B radiation at ambient levels were seriously damaged. Furthermore, bract removal decreased the number of pollinators visiting flowers. When bracts were removed before or after flowering, fecundity and progeny quality were adversely affected, but seed predation by larvae of pollinators decreased. A cost–benefit analysis demonstrated that the cost of bracts, i.e., increased seed predation, is modest. Our results suggest that the bracts of R. nobile promote pollen germination, protect pollen grains from rain and intense UV-B radiation, enhance pollinator visitation during flowering, and facilitate the development of fertilized ovules during seed development. We conclude that multifunctional bracts of R. nobile are an effective adaptive strategy in alpine environments and might have been selected for because of abiotic environmental conditions as well as for enhancing pollination success.     

Pollen transfer in fragmented plant populations: insight from the pollen loads of pollinators and stigmas in a mass‐flowering species

Pollinator and/or mate scarcity affects pollen transfer, with important ecological and evolutionary consequences for plant reproduction. However, the way in which the pollen loads transported by pollinators and deposited on stigmas are affected by pollination context has been little studied. We investigated the impacts of plant mate and visiting insect availabilities on pollen transport and receipt in a mass‐flowering and facultative autogamous shrub (Rhododendron ferrugineum). First, we recorded insect visits to R. ferrugineum in plant patches of diverse densities and sizes. Second, we analyzed the pollen loads transported by R. ferrugineum pollinators and deposited on stigmas of emasculated and intact flowers, in the same patches. Overall, pollinators (bumblebees) transported much larger pollen loads than the ones found on stigmas, and the pollen deposited on stigmas included a high proportion of conspecific pollen. However, comparing pollen loads of emasculated and intact flowers indicated that pollinators contributed only half the conspecific pollen present on the stigma. At low plant density, we found the highest visitation rate and the lowest proportion of conspecific pollen transported and deposited by pollinators. By contrast, at higher plant density and lower visitation rate, pollinators deposited larger proportion of conspecific pollen, although still far from sufficient to ensure that all the ovules were fertilized. Finally, self‐pollen completely buffered the detrimental effects on pollination of patch fragmentation and pollinator failure. Our results indicate that pollen loads from pollinators and emasculated flowers should be quantified for an accurate understanding of the relative impacts of pollinator and mate limitation on pollen transfer in facultative autogamous species.     

POLLEN AND GENE DISPERSAL: THE INFLUENCES OF COMPETITION FOR POLLINATION

Pollinators that forage indiscriminately can transfer pollen from one species to another, reducing the amount that reaches conspecific flowers. I present evidence that the presence of another plant species visited by the same pollinators can also reduce pollen dispersal distances and outcrossing. This has the potential to influence gene flow and reproductive success. Pollen carryover and movement patterns were measured for the shared insect pollinators of Stellaria pubera and Claytonia virginica in North Carolina. Bee flies deposited similar amounts of Stellaria pollen on a series of pistillate Claytonia flowers as on a series of pistillate Stellaria flowers. In arrays of potted plants, flies and solitary bees visited most flowers on a plant before leaving and then flew to a nearby plant chosen independently of species; 95% of moves were to one of 12 nearest neighbors. These measures of pollen carryover and movement patterns were used in a set of computer simulations to predict pollen dispersal distances. The simulations suggested that C. virginica substantially reduces outcrossing and pollen flow in S. pubera. These predictions were tested by tracking dye movement from anthers in populations of potted plants. Addition of C. virginica reduced the mean squared distance moved by dye to receptive S. pubera flowers by 23% and reduced the amount of dye moved by 51%. The estimated pollen component of gene flow was also much lower in a natural population of 5. pubera mixed with C. virginica than in the synthetic single-species populations.     

Pollination Biology of Hosta sieboldiana (Lodd.) Engler and H. sieboldii (Paxton) J. Ingram (Liliaceae)

Abstract The pollination biology of Hosta sieboldiana and H. sieboldii is investigated comparatively in Central Japan. Both species have homogamous, one-day flowers pollinated by bumblebees. The abdomens of the bees touch the stigma on the extended style when they land on the anthers inside the herkogamous flower, and autogamy is effectively prevented. However, the flowers are fairly self-compatible, and geitonogamy may occur rather frequently because two or more flowers on a scape very often bloom at the same time and many ramets are contiguous. The pollen/ovule ratios suggest that these species are facultative outbreeders. The flower of H. sieboldii seems completely suited to bumblebee pollination. In H. sieboldiana the stigma of the flower, whose style strongly protrudes, is not always touched by bumblebees, but frequent visitation of bumblebees results in pollination of almost all the flowers. Both species have similar pollination systems but seem reproductively isolated by blooming times and habitats. Their common pollinators, however, may sometimes cause introgressive hybridization in contiguous populations.     

An assessment of pollinator visitation to Banksia spinulosa

Abstract Remote photo-monitoring of Banksia spinulosa inflorescences indicated that birds, mammals and insects were regular visitors. These included the sugar glider, brown antechinus, eastern pygmy possum, eastern spinebill, honeybee and several moth species. Eastern spine-bills were recorded at all inflorescences monitored while visitation by other animals was more sporadic. Inflorescences were visited at least once every 24 h, and visitation frequency was approximately evenly distributed during the day and night. Examination of pollen tube growth from experimental treatments indicated that pollination success was similar from both nocturnal and diurnal visitors. However, nocturnal visitors were more effective at removing pollen from newly opened flowers. The behaviour of mammals at inflorescences was such that they would transfer much more pollen to flowers than other visitors, and probably contact receptive stigmas more often. Overall, mammals were considered to be slightly more effective pollinators than the more obvious daytime visitors, eastern spinebills. Although insects visited regularly, they were thought to be less effective at pollinating flowers than vertebrate visitors. Moths carried very little pollen, and the foraging behaviour of other insects was unlikely to promote much pollination.     

Pollination system of Corylopsis gotoana (Hamamelidaceae) and its stonefly (Plecoptera) co‐pollinator

The order Plecoptera is primarily known for its aquatic nymphs and their importance in many stream ecosystems. However, the biology and life history of Plecopteran terrestrial adults is mostly unknown, and hence interactions with plants have rarely been documented. Here, we report on insect visitation to flowers of Corylopsis gotoana (Hamamelidaceae) in a temperate forest of Japan, with emphasis on the behavior and pollination role of adults of a stonefly species, Strophopteryx nohirae (Taeniopterygidae), which were frequently observed in the flowers. The most frequent insect visitors to Corylopsis flowers were Bombylius major (Bombyliidae), Apis cerana (Apidae) and Bombus ardens (Apidae), all of which were considered main pollinators because of high rates of visitation and pollen attachment. Strophopteryx nohirae frequently visited Corylopsis trees, on which they foraged for pollen and mated. A field experiment on the pollination success of Corylopsis flowers visited by S. nohirae verified that this stonefly contributed to pollination.     

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.     

Correction to: The floral biology and the role of staminal connective appendages during pollination of the endoparasite Bdallophytum americanum (Cytinaceae)

Bdallophytum americanum (Cytinaceae) is an endoparasitic plant species, meaning only the flowers emerge from the host during the reproductive season. Reports on the pollination biology of this species state that its primary pollinators are carrion flies attracted by the smell of the flowers and nectar as a reward. However, the functional role of one of the most outstanding attributes of B. americanum has been neglected. These are the staminal appendages formed by the apical overgrowth of connective tissue during anther development. To determine whether these staminal appendages play a role in pollination, we monitored a nectarless population of B. americanum. We described the inflorescence emergence, floral movements, and pollination and performed field experiments to test whether the absence of the staminal connective appendages affected the visitation frequency. Male inflorescences emerge early, and both male and female flowers open during the day and do not close. Hoverflies are the most frequent visitors to both floral sexes and carry the most pollen. Moreover, the movement of staminal appendages matching the pollen viability changes is reported for the first time. The staminal appendages are the structures where pollinators land before foraging. The field experiments showed that the visitation frequency decreased sharply without staminal appendages. As a landing platform, the staminal connective appendages in B. americanum are crucial for pollinator positioning and collecting viable pollen.

     

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.     

The pollination of the gynomonoecious Bdallophytum oxylepis (Cytinaceae,Malvales)

Bdallophytum oxylepis is a rare and endemic species belonging to the Cytinaceae family, a root holoparasitic plant in which most resources are allocated to attracting pollinators. This species is gynomonoecious with intraindividual variation in flower size and sex. Moreover, the flowers exhibit sapromyophilous traits, as do other species of Bdallophytum. Firstly, this study aimed to determine whether all floral morphs can form seeds and be pollen donors (in the case of bisexual flowers). Secondly, as this species has floral traits hypothesized to adapt to particular types of pollen vectors (carrion flies), we also studied the pollination of B. oxylepis to confirm whether the syndromes correspond to what occurs in nature. Through pollination treatments, we determined that all floral morphs are functional. By monitoring the inflorescences, we found that pollination is specialized in the studied population. Stingless bees performed pollination, as they have a high visitation rate, frequency, and constancy, and they are unique visitors that deposit pollen on the stigmas. Thus, they appear to be effective pollinators rather than carrion flies, as predicted by the syndrome. As shown here, animal–plant interaction studies can help establish a basis for conserving rare species such as holoparasites. Moreover, knowledge about the reproductive aspects of B. oxylepis reveals essential clues about its life cycle and role in maintaining native pollinators with economic and cultural value, such as stingless bees.     

The influence of nectar production and floral visitors on the female reproductive success of Inga (Fabaceae): a field experiment

Floral morphology, nectar secretion strategies and the contribution of pollinators to the reproductive success of plants provide important clues regarding the levels of generalization or specialization in pollination systems. Anthesis throughout the day and night allows flowers to be visited by diurnal and nocturnal pollinators, promoting generalization or specialization. We studied three species in the diverse tropical genus Inga to: (1) quantify the response of flowers to successive nectar extractions and (2) determine the contribution of diurnal and nocturnal floral visitors to female reproductive success. Inga flowers could be clearly distinguished mainly on the basis of the staminal tube diameter and the quantities of filaments and pollen grains. Successive nectar removals led to a decrease of 60% in the total nectar secretion in I. vera and to increases of 20% in I. ingoides and 10% in I. striata. Despite these differences, the studied Inga spp. exhibited similar patterns of visitation rates and shared diurnal and nocturnal pollinators. Nocturnal pollinators contributed ten times more than diurnal pollinators to the female reproductive success of Inga. Floral morphology, nectar secretion patterns and pollination ecology data suggest an evolutionary trend towards specialization for nocturnal pollinators in Inga spp. with crepuscular or nocturnal flowers. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177 , 230–245.     

Floral colour change in Pedicularis monbeigiana (Orobanchaceae)

We examined the effects of the retention of colour-changed flowers on long- and short-distance attractiveness of bumblebees and the likelihood of successive flower visits by bumblebees in Pedicularis monbeigiana. The lower lip changed colour with age from white to purple. Hand geitonogamous pollination significantly reduced seed production. No pollen limitation occurred in this species. Purple-phase flowers contributed minimally to pollinator attractiveness at long distance. The combination of less reproductive flowers with a lower amount of reward and floral colour change enabled plants to direct pollinators to reproductive, highly rewarding white flowers at close range. A high percentage of purple-phase flowers in an inflorescence was associated with a marked reduction in the frequency of successive flower visits to individual plants. We suggest floral colour change in P. monbeigiana may serve as a mechanism for enhancing inter-individual pollen transfer and reducing intra-individual pollen transfer.     

Influence of environmental variation on the pollination of the ambophilous sedge <Emphasis Type="Italic">Rhynchospora ciliata</Emphasis> (Cyperaceae)

In typically anemophilous families, there are species, such as Rhynchospora ciliata (Cyperaceae), in which both wind and insects have been registered as pollen vectors (ambophily). However, the contribution of each vector to pollination of ambophilous species can change under different environmental conditions. Therefore, this study aimed to determine the primary pollination system, abiotic or biotic, of R. ciliata, comparing wet and dry seasons. We tested the following hypotheses: (1) in dry months, wind is the main pollen vector of R. ciliata; (2) in wet months, insects will contribute more to the reproductive success of R. ciliata and compensate for low fruit formation by the abiotic vector. Our hypothesis was not confirmed. We found that higher wind speed can favor pollination by wind in R. ciliata even in wetter months. Because insects were less susceptible to environmental variation, they contributed more in dry months when wind speed was low, thus compensating for lower fruit set by wind. High rainfall and humidity can result in faster settling of pollen grains suspended in the air; however, rainfall does not prevent pollination by wind. Since individuals of R. ciliata are located near the edge of the forest, grouped quite close together, and as the inflorescence is located at the apex of the floral scape, wind can act as pollen vector and the inhibiting effects of rainfall can be minimized. The contribution of each pollen vector is important to the reproductive success of R. ciliata and the effectiveness of wind varies with local environmental conditions.     

Mixed bumblebee and blowfly pollination of Cypripedium flavum (Orchidaceae) in Sichuan,China

Most Cypripedium species are specialized orchids pollinated by, in a broad sense, bees or flies. Here we present the first evidence that a slipper orchid, Cypripedium flavum, is pollinated by both bees and flies, i.e., bumblebees and blowflies. Artificial pollination experiments demonstrated that the flowers of C. flavum are self-compatible, but need pollen vectors for successful reproduction. Field observations detected 25 insects visiting the flowers, and 14 of these insects entered into the labellum of the flowers, but only female bumblebees, Bombus hypnorum, B. remotus, and the blowfly Calliphora vomitoria exited of the labellum with pollen smears of C. flavum. The floral functional morphology of C. flavum appears to be more suited to bumblebees than to blowflies. The bumblebees are more efficient pollinators of the orchid, but blowflies are more frequent visitors, so they pollinated more flowers despite being less efficient.