Effects of flower number on estimated pollen transfer in natural populations of three hermaphroditic species: an experiment with fluorescent dye

The relationship between the number of open flowers and pollen transfer to stigmas was estimated in three insect-pollinated species (Cynoglossum officinale, Echium vulgare and Oenothera erythrocepala) in 1995 and 1996, using fluorescent dye as a pollen analogue. Dye was applied to an equal number of flowers on a small, a medium and a large individual and its pattern of dispersal to stigmas of conspecifics in local populations was observed. In Cynoglossum officinale and in Echium vulgare large individuals tended to receive more visits per flower. In Oenothera erythrocepala no difference in number of visits per flower was found between small and large individuals. Geitonogamous pollination clearly occurred in all species. In Cynoglossum officinale large individuals transferred more pollen per flower within the same plant (geitonogamy) and an equal or a slightly smaller amount between plants, compared to small individuals. As a result total pollen transfer per flower increased in both years with increasing flower number. In Echium vulgare and in Oenothera erythrocepala large individuals transferred more pollen per flower within the plant (pollen discounting), but a significantly lower amount per flower to other individuals in the populations compared to small individuals. For both these species, there is no difference in total pollen transfer between small and large individuals. In general, the male fitness curve, as estimated by pollen transfer, is a decelerating function of flower number. We discuss this in relation to optimal sex-allocation and the pollen donation hypothesis.     

Hysteresis in the responses of membrane potential, membrane resistance, and growth rate to cyclic temperature change

Measurements of electrical potential, membrane resistance, and elongation rate have been carried out on the developing pollen tube of Oenothera drummondii.     

Floral color change and the attraction of insect pollinators in lungwort (Pulmonaria collina)

We studied the effect of floral color change on long- and short-distance attraction of insect pollinators to the herb lungwort, Pulmonaria collina. Lungwort flowers change color with age from red to blue. Young red flowers had a significantly greater pollen and nectar reward and were significantly more often unpollinated than old blue ones. Red and blue flowers both influenced long-distance attractiveness of plants, defined as the number of insect approaches towards an individual plant. After reaching a plant, flower visitors preferred to visit young red flowers. Therefore, short-distance attractiveness, defined as the number of flowers visited successively on an individual plant, was influenced mainly by the number of young red flowers. The co-occurrence of the change in reproductive ability, in amount of reward, and in flower color enabled lungwort plants to direct pollinators to reproductive, highly rewarding red flowers. The data suggest that by maintaining changed flowers lungwort plants can increase their long-distance attraction and simultaneously enhance the probability of flower visits to pre-changed flowers. Thus, we propose floral color change as a mechanism that can increase the efficiency of pollen transfer to enhance plant fitness. Received: 2 November 1998 / Accepted: 14 July 1999     

Interaction between floral color change and gender transition in the protandrous weed Saponaria officinalis

Natural selection has directed the evolution of floral traits so that pollinator visits are manipulated to maximize the fitness of individual plants by directing which other individual sires its seeds. In some plants, flowers change color over time and may have the ability to direct pollinators to rewarding flowers. In addition, by varying when pollen is available and when stigmas are receptive, protandrous plants can show variation in selfing rates. In this study, the association between color change and gender transition in flowers of Saponaria officinalis was examined. Anthocyanins were extracted from flowers of each gender stage to measure color using spectrophotometry. Female‐phase flowers were found to have significantly higher anthocyanin concentration than male‐phase flowers in both natural populations and experimental plots. This color change corresponded to a decrease in male sexual function, which was measured by the percentage of pollen grains stained as viable by lactophenol aniline blue and germinated on Brewbaker–Kwack media. Color change was phenotypically plastic. Plants grown in full sun had a more extensive color change than those grown in shaded experimental plots, and this effect was reversed the following year when the shading was removed. Pollinator observations documented both diurnal and nocturnal insect visitation. Fruit and seed set were equivalent on inflorescences bagged during daylight versus night, indicating that both diurnal and nocturnal insects are effective pollinators. If pollinators discriminate based on color, this could potentially reduce within‐plant floral visits and also geitonogamy. This study is the first to document flower color change and moth pollination in Saponaria officinalis.     

A trade-off between the frequency and duration of bumblebee visits to flowers

Pollinator behavior influences plant reproduction in many ways. A traditional measure of pollination, the number of visits received, may be a poor predictor of plant reproductive success, particularly when there are trade-offs between visit quantity and components of visit quality. For example, the duration of pollinator visits may be negatively correlated with the number of visits received by a flower. We tested for a trade-off between the number of bumblebee visits and the duration of those visits in an experimental population of snapdragons (Antirrhinummajus: Scrophulariaceae). The duration of a bumblebee visit to a flower increased significantly with the time interval since the flower had last been visited. Over the lifetime of a flower the correlation between the total number and average duration of visits received by a flower was weakly negative. However, at the whole-plant level the correlation was positive: plants whose flowers received more visits also received visits of longer duration. Factors affecting the relationship between quantity and duration of pollinator visits to flowers also were investigated. Two factors weakened the negative dependence of average visit duration on number of visits received by individual snapdragon flowers: (1) the correlation between the total number of visits to a flower and the average interval between visits was only −0.53, as visits to individual flowers were not very evenly spaced over time, and (2) newly opened flowers received fewer and shorter visits than older flowers. Comparing whole plants, nectar production per flower varied dramatically across individuals, a probable explanation for the positive correlation between visit number and average duration per flower observed at the plant level. The potential for a trade-off between these two components of pollinator service exists when visit duration depends on reward quantity; whether the trade-off is realized will depend on variation in nectar production and on whether pollinators forage systematically. Received: 3 October 1997 / Accepted: 16 June 1998     

A test of the effect of floral color change on pollination effectiveness using artificial inflorescences visited by bumblebees

Floral color change has been recognized as a pollination strategy, but its relative effectiveness has been evaluated insufficiently with respect to other floral traits. In this study, effects of floral color change on the visitation pattern of bumblebees were empirically assessed using artificial flowers. Four inflorescence types were postulated as strategies of flowering behavior: type 1 has no retention of old flowers, resulting in a small display size; type 2 retains old flowers without nectar production; type 3 retains old flowers with nectar; and type 4 retains color-changed old flowers without nectar. Effects of these treatments varied depending on both the total display size (single versus multiple inflorescences) and the pattern of flower-opening. In the single inflorescence experiment, a large floral display due to the retention of old flowers (types 2–4) enhanced pollinator attraction, and the number of flower visits per stay decreased with color change (type 4), suggesting a decrease in geitonogamous pollination. Type-4 plants also reduced the foraging time of bees in comparison with type-2 plants. In the multiple inflorescence experiment, the retention of old flowers did not contribute to pollinator attraction. When flowering occurred sequentially within inflorescences, type-4 plants successfully decreased the number of visits and the foraging time in comparison with type-2 plants. In contrast, floral color change did not influence the number of visits, and it extended the foraging time when flowering occurred simultaneously within inflorescences but the opening of inflorescences progressed sequentially within a plant. Therefore, the effectiveness of floral color change is highly susceptible to the display size and flowering pattern within plants, and this may limit the versatility of the color change strategy in nature.     

Floral color change in Weigela middendorffiana (Caprifoliaceae): reduction of geitonogamous pollination by bumble bees

We examined the significance of retaining color-changed flowers in pollination success of Weigela middendorffiana through a single visit of bumble bees. Inner parts of flowers changed color with age from yellow to red. In an investigation of the mating system, duration of each color phase, reproductive ability of each of the color-phase flowers, and the effects of color-changed flowers on bumble bee behavior (1) flowers of this species were self-incompatible, (2) color-changed flowers provided little reward to pollinators and little residual reproductive ability, (3) the timing of floral color change was delayed with the progress of flowering season within individual plants, while the duration of the red phase shortened with the progress of flowering season, and (4) red-phase flowers did not attract bumble bees at a distance but did contribute to reducing the number of successive flower visits during a single stay within the plants. Red-phase flowers seemed to indicate the low reward level of old flowers and functioned as a cue to discourage pollinators from staying longer on the same plant. Our results predict that the retention of color-changed flowers without sexual function can enhance the pollination success of a whole plant through male function by reducing successive flower visits during a single stay of pollinators, i.e., geitonogamous pollination.     

Interaction between flowers, ants and pollinators: additional evidence for floral repellence against ants

It has been commonly suggested that ants negatively affect plant pollination, particularly in the tropics. We studied ant–flower–pollinator interactions in a lowland rainforest in Borneo. Frequency and duration of pollinator visits were compared between flowers attended by ants and flowers from which ants were excluded. In all four plant species studied, the activity of ants decreased the rate and/or duration of the pollinators’ floral visits. For this and other reasons it is expected that plants repel ants from flowers during anthesis. We tested this prediction for a different set of plant species in which we observed the behaviour of Dolichoderus thoracicus ants when encountering flowers. In eight out of 18 plant species studied, ants showed a significantly higher rejection rate when they encountered flowers than when they encountered controls. Our results are thus consistent with the hypothesis that ants may negatively affect plant fitness by reduced intensity of pollinator visits and that ants are repelled from flowers of many tropical plant species, although this repellence is clearly not ubiquitous.     

Novel nectar robbing negatively affects reproduction in Digitalis purpurea

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

Effects of number of flowers per raceme and number of racemes per plant on bumblebee visits and female reproductive success in <Emphasis Type="Italic">Salvia nipponica</Emphasis> (Labiatae)

We studied the adaptive arrangement of raceme flowers in dense and sparse habitats of Salvia nipponica. We recorded bumblebee visits and collected mature seeds to estimate outcrossing rates from allozyme genotypes. To examine the resource investment in flowering stalks, we measured their length and dry mass. We found that a greater number of open flowers in a raceme enhanced bumblebee visits and successive probings in both density plots. However, greater height of a raceme did not enhance these in plots of either density. In the high-density plot, both a greater mean number of open flowers in a raceme and a greater number of flowering racemes on a plant enhanced bumblebee visits, successive probings, and also enhanced outcrossing rate in spite of an increase in successive probings. Although the number of flowers per raceme had a greater positive effect on seed-to-ovule ratios than did the number of racemes, the number of flowers per raceme may be constrained because a longer flowering stalk needs greater buckling strength. Hence, it may be advantageous for plants in high-density plots to increase both number of flowers per raceme and number of racemes. In the low-density plot, a greater number of flowering racemes on a plant enhanced pollinator visits, but a greater mean number of open flowers in a raceme did not. Hence, it may be advantageous for plants to increase the number of racemes while keeping the numbers of flowers per raceme small. Thus, the adaptive number of flowers per raceme and number of racemes per plant may differ between high- and low-density plots.     

Flowers respond to pollinator sound within minutes by increasing nectar sugar concentration

Can plants sense natural airborne sounds and respond to them rapidly? We show that Oenothera drummondii flowers, exposed to playback sound of a flying bee or to synthetic sound signals at similar frequencies, produce sweeter nectar within 3 min, potentially increasing the chances of cross pollination. We found that the flowers vibrated mechanically in response to these sounds, suggesting a plausible mechanism where the flower serves as an auditory sensory organ. Both the vibration and the nectar response were frequency‐specific: the flowers responded and vibrated to pollinator sounds, but not to higher frequency sound. Our results document for the first time that plants can rapidly respond to pollinator sounds in an ecologically relevant way. Potential implications include plant resource allocation, the evolution of flower shape and the evolution of pollinators sound. Finally, our results suggest that plants may be affected by other sounds as well, including anthropogenic ones.     

Direct and Indirect Effects of Nectar Robbing on the Pollinating Behavior of Patagona gigas (Trochilidae)1

In central Chile, nectar robbing of Puya coerulea (Bromeliaceae) flowers by the austral blackbird, Curaeus curaeus, had a direct impact on the plant via removal of floral resources and, in some cases, damage or even destruction of flowers. These robbing visits also likely had an indirect impact on plant fitness due to the decreased rate of legitimate visits by the hummingbird Patagona gigas to inflorescences with many robbed flowers. The proportion of flowers within an inflorescence visited by P. gigas was inversely proportional to the ratio of robbed flowers.     

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.     

<Emphasis Type="Italic">Oenothera speciosa</Emphasis> versus <Emphasis Type="Italic">Macroglossum stellatarum</Emphasis>: killing beauty

Hovering and dead individuals of the diurnal hawk-moth Macroglossum stellatarum (Linnaeus, 1758) (Lepidoptera: Sphingidae) were found with proboscides got stuck into flowers of the ornamental plant Oenothera speciosa Nutt (Onagraceae). The phenomenon was observed in several locations in Bulgaria where the plant has been introduced. Microscopic examination revealed that the reason for this unusual interaction is pubescence of thick-walled basiscopically oriented trichomes in the basal part of the hypanthium and style of the plant. When a foraging moth inserts its proboscis into this area, the tips of the trichomes are inserted into the transverse grooves of proboscis and hamper its back movement. As a result the moths are suspended for a long time, sometimes until death. Other trapped moth species were also observed but they always effected self-release. This plant–insect interaction is also a conservation issue as an estimation of its impact on wild insect populations is lacking.     

Risk‐averse inflorescence departure in hummingbirds and bumble bees: could plants benefit from variable nectar volumes?

Most hermaphroditic, many-flowered plants should suffer reduced fitness from within-plant selfing (geitonogamy). Large inflorescences are most attractive to pollinators, but also promote many flower visits during a single plant visit, which may increase selfing and decrease pollen export. A plant might avoid the negative consequences of attractiveness through modification of the floral display to promote fewer flower visits, while retaining attractiveness. This report shows that increasing only the variance in nectar volume per flower results in fewer flower visits per inflorescence by wild hummingbirds ( Selasphorus rufus ) and captive bumble bees ( Bombus flavifrons ) foraging on artificial inflorescences. Inflorescences were either constant (all flowers contained the same nectar volume) or variable (half the flowers were empty, the other half contained twice as much nectar as in the constant flowers). Both types of inflorescence were simultaneously available to foragers. Risk-averse foraging behaviour was expressed as a patch departure preference: birds and bees visited fewer flowers on variable inflorescences, and this preference was expressed when resource variability could be determined only by concurrent sampling. When variance treatments were clearly labelled with colour and offered to hummingbirds, the departure effect was maintained; however, when preference was measured by inflorescence choice, birds did not consistently prefer to visit constant inflorescences. The reduced visitation lengths on variable inflorescences by both birds and bees documented in this study imply that variance in nectar production rates within inflorescences may represent an adaptive trait to avoid the costs of geitonogamy.     

Post‐ingestive effect of plant phenolics on the feeding behaviour of the honeybee Apis cerana

As the staple food of honey bees, honey is rich in plant phenolics derived from pollen, nectar and resin. Most studies concentrate on the temporary response of bees' peripheral chemoreceptors to these chemicals, and the post‐ingestive effects of plant phenolics are largely ignored. In the present study, a series of feeding experiments are conducted to test whether plant phenolics modulate the response thresholds and rhythmic behaviour of the honeybee Apis cerana (Ruttner). The results of the study demonstrate that bees fed with syrup containing high concentrations of phenlics reduce their response thresholds greatly, and shift their feeding rhythms significantly. Because the forager response thresholds determine their foraging choice, and their rhythmic behaviour is required for timing visits to flowers, enhanced plant phenolics as a result of global environment change may change the bees' pollination service in our changing world.     

How long to stay on a plant: the response of bumblebees to encountered nectar levels

This field study shows that the number of flowers visited per bee per plant (Anchusa officinalis) increases with the instantaneous nectar level at the plant. Observations during the season showed that a bee visits more flowers per plant of given nectar level, the lower the overall mean nectar level in the study area. These results agree with predictions from a model based on the ‘marginal value theorem’, but with assumptions and constraints adapted for nectar-foraging bees. It suggests that bumblebees assess the nectar level at a plant by sampling one or a few flowers, which is possible because within-plant nectar volumes are correlated. The bees compare encountered gains to an optimal plant switching threshold equal to the overall mean nectar level and leave an unrewarding plant as soon as possible, but continue to visit the flowers on a rewarding plant. However, the bees leave before having visited all flowers due to a searching constraint. The bees’ response to plant nectar levels results in systematic flower visitation, because visitation to recently depleted flowers is reduced, which reduces the variation of the inter-visit time per flower. Systematic flower visitation implies that the overall mean encountered gain per flower is higher than the overall mean standing crop, as predicted by a model of systematic foraging. However, the sampling and searching constraints on the bees’ response to plant nectar levels increase the variation of the inter-visit time per flower, and thereby limit the degree of systematic flower visitation and the effect on the mean encountered gain.     

Environment and pollinator-mediated selection on parapatric floral races of Mimulus aurantiacus

We tested whether selection by pollinators could explain the parapatric distribution of coastal red- and inland yellow-flowered races of Mimulus aurantiacus (Phrymaceae) by examining visitation to natural and experimental populations. As a first step in evaluating whether indirect selection might explain floral divergence, we also tested for local adaptation in early life stages using a reciprocal transplant experiment. Hummingbirds visited flowers of each race at similar rates in natural populations but showed strong (>95%) preference for red flowers in all habitats in experimental arrays. Hawkmoths demonstrated nearly exclusive (>99% of visits) preference for yellow flowers and only visited in inland regions. Strong preferences for alternative floral forms support a direct role for pollinators in floral divergence. Despite these preferences, measures of plant performance across environments showed that red-flowered plants consistently survived better, grew larger and received more overall pollinator visits than yellow-flowered plants. Unmeasured components of fitness may favour the yellow race in inland habitats. Alternatively, we document a marked recent increase in inland hummingbird density that may have caused a change in the selective environment, favouring the eastward advance of red-flowered plants.     

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

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

Nectar robbery by a hermit hummingbird: association to floral phenotype and its influence on flowers and network structure

Interactions between flowers and their visitors span the spectrum from mutualism to antagonism. The literature is rich in studies focusing on mutualism, but nectar robbery has mostly been investigated using phytocentric approaches focused on only a few plant species. To fill this gap, we studied the interactions between a nectar-robbing hermit hummingbird, Phaethornis ruber, and the array of flowers it visits. First, based on a literature review of the interactions involving  P. ruber, we characterized the association of floral larceny to floral phenotype. We then experimentally examined the effects of nectar robbing on nectar standing crop and number of visits of the pollinators to the flowers of Canna paniculata. Finally, we asked whether the incorporation of illegitimate interactions into the analysis affects plant–hummingbird network structure. We identified 97 plant species visited by P. ruber and found that P. ruber engaged in floral larceny in almost 30 % of these species. Nectar robbery was especially common in flowers with longer corolla. In terms of the effect on C. paniculata, the depletion of nectar due to robbery by P. ruber was associated with decreased visitation rates of legitimate pollinators. At the community level, the inclusion of the illegitimate visits of P. ruber resulted in modifications of how modules within the network were organized, notably giving rise to a new module consisting of P. ruber and mostly robbed flowers. However, although illegitimate visits constituted approximately 9 % of all interactions in the network, changes in nestedness, modularity, and network-level specialization were minor. Our results indicate that although a flower robber may have a strong effect on the pollination of a particular plant species, the inclusion of its illegitimate interactions has limited capacity to change overall network structure.