The screening game in plant–pollinator interactions

A central question in the field of plant–pollinator interactions is whether and how can plants choose the optimal pollinators when plants cannot directly assess the quality of floral visitors. To answer this question and to provide a new perspective to this problem, we develop a screening game modeling the plant–pollinator interaction. We propose that some floral traits could be interpreted as an entry barrier with a strategic cost the plants impose on floral visitors. The pollinators decide to further interact with the plant only if the cost is not prohibitive. Therefore, by imposing the right level of costs, the plants may achieve interactions only with high-quality pollinators without a priori knowing the quality of visitors.     

Floral variation in the generalist perennial herb Paeonia broteroi (Paeoniaceae): differences between regions with different pollinators and herbivores

This paper investigates the differences in floral phenotype in Paeonia broteroi (Paeoniaceae) in four populations at two distant mountainous regions in southern Spain. Paeonia broteroi flowers exhibit traits of a highly generalized pollination system, but previous studies have revealed that not all flower visitors are effective at pollen delivery. Plants differed between regions in the number of flowers per plant, petal size, number of stamens per flower, and ovules per carpel. Differences between regions could not be attributable to differences in the size structure of the plants. Flower visitors in the two regions differed in assemblage and body size at all the spatiotemporal scales. Larger visitors were more effective as pollinators in the region with the largest and more rewarding (as measured by the number of stamens) flowers, suggesting that pollinators may create opportunities for selection of certain floral traits. In contrast, the two regions did not differ in the probability of damage by herbivores, which did not select flowers based on any of the measured traits, nor affected maternal fecundity. Despite the differences in flower phenotype, potential maternal fecundity, and pollinator effectiveness, plants did not differ between regions in seed production. The role of pollinators as determinants of the differences between regions in floral phenotype, through male and female reproductive success, is discussed. Also, alternative explanations to divergence are addressed, with special reference to the patterns of resource allocation between sexual functions and genetic drift.     

Arranging the bouquet of disease: floral traits and the transmission of plant and animal pathogens

Several floral microbes are known to be pathogenic to plants or floral visitors such as pollinators. Despite the ecological and economic importance of pathogens deposited in flowers, we often lack a basic understanding of how floral traits influence disease transmission. Here, we provide the first systematic review regarding how floral traits attract vectors (for plant pathogens) or hosts (for animal pathogens), mediate disease establishment and evolve under complex interactions with plant mutualists that can be vectors for microbial antagonists. Attraction of floral visitors is influenced by numerous phenological, morphological and chemical traits, and several plant pathogens manipulate floral traits to attract vectors. There is rapidly growing interest in how floral secondary compounds and antimicrobial enzymes influence disease establishment in plant hosts. Similarly, new research suggests that consumption of floral secondary compounds can reduce pathogen loads in animal pollinators. Given recent concerns about pollinator declines caused in part by pathogens, the role of floral traits in mediating pathogen transmission is a key area for further research. We conclude by discussing important implications of floral transmission of pathogens for agriculture, conservation and human health, suggesting promising avenues for future research in both basic and applied biology.     

The relative strength of different floral visitors driving floral evolution within a <Emphasis Type="Italic">Primula secundiflora</Emphasis> population

Floral visitor assemblages within plant populations are usually composed of different visitors, and the relative abundance of these visitors also varies. Therefore, identifying the relative strength of these floral visitors driving floral evolution within the population is an important step in predicting the evolutionary trajectory of floral traits. Using supplemental hand pollination and nectar-robbing exclusion treatments, we experimentally identified the relative strengths of legitimate pollinators (that visit flowers through the corolla tube entrance) and nectar robbers (that visit flowers by biting a hole in the corolla tube or using an existing hole) driving floral evolution within the Primula secundiflora population. We also estimated legitimate pollinator- and nectar robber-mediated selection separately for pin and thrum flowers. Both legitimate pollinators and nectar robbers mediated selection on pollination efficiency traits in P. secundiflora population. Legitimate pollinators mediated selection for wider corolla tubes, whereas nectar robbers mediated selection for longer corolla tubes. In addition, nectar robber-mediated selection on corolla tube length marginally varied between the pin and thrum flowers. Nectar robber mediated selection for longer corolla tube length in the pin flowers not in the thrum flowers. These results indicate that legitimate pollinators and nectar robbers within a population can drive differential evolutionary trajectories of floral traits.     

Covariance of floral and vegetative traits in four species of Ranunculaceae: a comparison between specialized and generalized pollination systems

Theory predicts that tighter correlation between floral traits and weaker relationship between floral and vegetative traits more likely occur in specialized flowers than generalized flowers,favoring by precise fit with pollinators.However,traits and trait correlations frequently vary under different environments.Through detecting spatiotemporal variation in phenotypic traits (floral organ size and vegetative size) and trait correlations in four Ranunculaceae species,we examined four predictions.Overall,our results supported these predictions to a certain degree.The mean coefficient of variation (CV) of floral traits in two specialized species (Delphinium kamaonense and Aconitum gymnandrum) was marginally significantly lower than that of another two generalized species (Trollius ranunculoides and Anemone obtusiloba).The two specialized species also showed marginally significantly smaller CV in floral traits than vegetative size across the two species.The absolute mean correlation between floral and vegetative traits,or that between floral traits in species with specialized flowers was not significantly lower,or higher than that in generalized plants,weakly supporting the predictions.Furthermore,we documented a large variation in trait correlations of four species among different seasons and populations.Study of covariance of floral and vegetative traits will benefit from the contrast of results obtained from generalized and specialized pollination systems.     

Floral divergence, pollinator partitioning and the spatiotemporal pattern of plant–pollinator interactions in three sympatric Adenophora species

Floral divergence among congeners may relate to differential utilization of pollinators and contribute to reducing overlap in pollination niches. To investigate whether and how floral differences are associated with differential utilization of pollinators in three sympatric Adenophora species, we analyzed floral traits and evaluated the contribution of different visitors to pollination. We compared visitation rates of different pollinator categories in different years and sites. A suite of floral traits differed among the three Adenophora species, suggesting adaptation to diurnal versus nocturnal pollination and an intermediate condition. However, many visitor species were shared among the three plant species, suggesting that floral traits did not rigorously filter visitors. Effective pollinators were large bees and moths. The importance of large bees as pollinators decreased whereas that of moths increased along the gradient from typically bee-pollinated to moth-pollinated flowers. The intermediate species (A. khasiana) differed substantially from the other two species in pollinator species but not in pollinator categories. The principal pollinator category of each species was constant across years and sites except in the intermediate species where it differed between two sites. Overall, the three sympatric species of Adenophora partition pollinators by floral divergence and the principal pollinators coincide with the predictions based on floral syndromes.     

Pollen limitation,species’ floral traits and pollinator visitation: different relationships in contrasting communities

Failures in the process of pollen transfer among conspecific plants can severely impact female reproductive success. Thus, pollen limitation can cause selection on plant mating systems and floral traits. The relationships between pollen limitation and floral traits might be partly mediated by the quantity and identity of pollinator visits. However, very little is known about the relationship between pollinator visits and pollen limitation. We examined the relationships between pollen limitation and floral traits at the community level to connect them to community ecology processes. We used 48 plant species from two contrasting communities: one species‐rich lowland community and one species‐poor alpine community. In addition, we calculated visitation rates and ecological pollination generalization for 38 of the species to examine the relationship between pollinator visitation and pollen limitation at the community level. We found low overall levels of pollen limitation that did not differ significantly between the alpine and the lowland community. In both communities, species with evolutionary specialized flowers were more pollen limited than species with unspecialized flowers. Species’ visitation rates and selfing capability were negatively related to pollen limitation in the alpine community, where pollinators are scarcer. However, flower size/number, ecological generalization of plants and flowering onset had greater effects on pollen limitation levels at the lowland community, indicating that the identity of the visitors and plant‐plant competitive interactions are more decisive for plant reproduction in this species‐rich community. There, pollen limitation increased with flower size and flowering onset, and decreased with ecological generalization, but only in species with evolutionary specialized flowers. Our study suggests that selection on plant mating system and floral traits may be idiosyncratic to each particular community and highlights the benefits of conducting community‐level studies for a better understanding of the processes underlying evolutionary responses to pollen limitation.     

Flower biology of the cactus Coryphantha elephantidens in the tropical dry forest of Central Mexico

Floral traits and sexual systems in angiosperms are strategies that enhance outcrossing within hermaphrodite flowers and among individuals in a population. Sexual systems with unisexual flowers have also evolved among angiosperms, resulting in sex specialization. Furthermore, the interaction of floral traits and floral visitors determines successful plant reproduction. Globose cacti are bee pollinated, and variation in the diversity of their pollinator assemblages is strongly associated with floral phenotype. Our objective was to describe the floral biology of the cactus Coryphantha elephantidens and to determine its relationship with pollinators. Floral traits were studied by direct observations in live and fixed flowers. The breeding system was determined using two estimators based on floral morphology: pollen grains to ovules per flower (P/O) ratio and outcrossing index. Pollination treatments were conducted to determine the mating system. Floral visitors were recorded using direct observation. Flowers of C. elephantidens are variable in color, protandric, herkogamous and nectarless. Estimators of the breeding system indicated xenogamy, which is consistent with the obligate outcrossing revealed by the pollination experiment. Thirty-seven percent of the plants have female flowers that do not produce pollen, making this population functionally gynodioecious. Both fruit and seed set were high compared to other globose cacti. Pollinators included eight species of native bees, a more diverse pollinator assemblage than other globose cacti. Given the high pressure on pollen due to functional gynodioecy, nectarless flowers, an outcrossing mating system, and the necessity of pollinators to set seeds, we concluded that native bees are highly efficient pollinators that play a crucial role in the sexual reproduction of C. elephantidens.     

Novel adaptation to hawkmoth pollinators in Clarkia reduces efficiency,not attraction of diurnal visitors

Background and Aims

Plant populations experiencing divergent pollination environments may be under selection to modify floral traits in ways that increase both attractiveness to and efficiency of novel pollinators. These changes may come at the cost of reducing overall effectiveness of other pollinators. The goal of this study was to examine differences in attractiveness and efficiency between Clarkia concinna and C. breweri, sister species of annual plants with parapatric distributions.

Methods

An assessment was made as to whether observed differences in visitors between natural populations are driven by differences in floral traits or differences in the local pollination environment. Differences in floral attractiveness were quantified by setting out arrays of both species in the geographical range of each species and exposing both species to nocturnal hawkmoths (Hyles lineata) in flight cages. Differences in visitor efficiency were estimated by measuring stigma–visitor contact frequency and pollen loads for diurnal visitors, and pollen deposition on stigmas for hawkmoths.

Key Results

The composition of visitors to arrayed plants was similar between plant species at any particular site, but highly divergent among sites, and reflected differences in visitors to natural populations. Diurnal insects visited both species, but were more common at C. concinna populations. Hummingbirds and hawkmoths were only observed visiting within the range of C. breweri. Despite attracting similar species when artificially presented together, C. concinna and C. breweri showed large differences in pollinator efficiency. All visitors except hawkmoths pollinated C. concinna more efficiently.

Conclusions

Differences in the available pollinator community may play a larger role than differences in floral traits in determining visitors to natural populations of C. concinna and C. breweri. However, floral traits mediate differences in pollinator efficiency. Increased effectiveness of the novel hawkmoth pollinator on C. breweri comes at relatively little cost in attractiveness to other visitors, but at large cost in their efficiency as pollinators.     

The pollination biology of Burmeistera (Campanulaceae): specialization and syndromes

The floral traits of plants with specialized pollination systems both facilitate the primary pollinator and restrict other potential pollinators. To explore interactions between pollinators and floral traits of the genus Burmeistera, I filmed floral visitors and measured pollen deposition for 10 species in six cloud forest sites throughout northern Ecuador. Nine species were primarily bat-pollinated (84-100% of pollen transfer); another (B. rubrosepala) was exclusively hummingbird-pollinated. According to a principal components analysis of 11 floral measurements, flowers of B. rubrosepala were morphologically distinct. Floral traits of all species closely matched traditional ornithophilous and chiropterophilous pollination syndromes; flowers of B. rubrosepala were bright red, lacked odor, opened in the afternoon, and had narrow corolla apertures and flexible pedicels, which positioned them below the foliage. Flowers of the bat-pollinated species were dull-colored, emitted odor, opened in the evening, and had wide apertures and rigid pedicels, which positioned them beyond the foliage. Aperture width appeared most critical to restricting pollination; hummingbirds visited wide flowers without contacting the reproductive parts, and bats did not visit the narrow flowers of B. rubrosepala. Aperture width may impose an adaptive trade-off that favors the high degree of specialization in the genus. Other floral measurements were highly variable amongst bat-pollinated species, including stigma exsertion, calyx lobe morphology, and pedicel length. Because multiple species of Burmeistera often coexist, such morphological diversity may reduce pollen competition by encouraging pollinator fidelity and/or spatially partitioning pollinator's bodies.     

Temporal stability of pollinator preference in an alpine plant community and its implications for the evolution of floral traits

A traditional view of diverse floral traits is that they reflect differences in foraging preferences of pollinators. The role of pollinators in the evolution of floral traits has been questioned recently by broad community surveys, especially studies concerning variation in pollinator assemblages and visitation frequency, which suggest a diminished role of pollinators in floral evolution. Here, we investigate the relationships between six categories of floral traits of 29 species and 10 pollinator functional groups in an alpine meadow in the Hengduan Mountains of China, over three consecutive years. Simpson’s diversity index was used to estimate the level of pollinator generalization of each plant species by considering both pollinator groups and their relative visitation frequencies. Multivariate analyses indicated that eight of the ten pollinator groups showed constant preferences for at least two floral traits, leading to a relatively stable level of ecological generalization for most floral traits (two out of three categories), despite the fact that the level of generalization of the entire community varied across years. Shape preferences of butterflies, honeybees and beeflies varied such that open flowers exhibited a lower level of ecological generalization in 2007 than closed flowers, in contrast with the other 2 years. These results suggest that temporally stabilized preferences of diverse pollinators may contribute to the evolution of specialized versus generalized floral traits; however, their role may be moderated by variation in community structure, including both the composition and abundance of plants and pollinators.     

INFLUENCE OF POLLINATION SPECIALIZATION AND BREEDING SYSTEM ON FLORAL INTEGRATION AND PHENOTYPIC VARIATION IN IPOMOEA

Natural selection should reduce phenotypic variation and increase integration of floral traits involved in placement of pollen grains on stigmas. In this study, we examine the role of pollinators and breeding system on the evolution of floral traits by comparing the patterns of floral phenotypic variances and covariances in 20 Ipomoea species that differ in their level of pollination specialization and pollinator dependence incorporating phylogenetic relatedness. Plants with specialized pollination (i.e., those pollinated by one functional group or by few morphospecies) displayed less phenotypic variation and greater floral integration than generalist plants. Self‐compatible species also displayed greater floral integration than self‐incompatible species. Floral traits involved in pollen placement and pick up showed less variation and greater integration than floral traits involved in pollinator attraction. Analytical models indicate that both breeding system and the number of morphospecies had significant effects on floral integration patterns although only differences in the former were significant after accounting for phylogeny. These results suggest that specialist/self‐compatible plants experience more consistent selection on floral traits than generalist/self‐incompatible plants. Furthermore, pollinators and breeding system promote integration of floral traits involved in pollen placement and pick up rather than integration of the whole flower.     

Florivory indirectly decreases the plant reproductive output through changes in pollinator attraction

Species often interact indirectly with each other via their traits. There is increasing appreciation of trait‐mediated indirect effects linking multiple interactions. Flowers interact with both pollinators and floral herbivores, and the flower‐pollinator interaction may be modified by indirect effects of floral herbivores (i.e., florivores) on flower traits such as flower size attracting pollinators. To explore whether flower size affects the flower‐pollinator interaction, we used Eurya japonica flowers. We examined whether artificial florivory decreased fruit and seed production, and also whether flower size affected florivory and the number of floral visitors. The petal removal treatment (i.e., artificial florivory) showed approximately 50% reduction in both fruit and seed set in natural pollination but not in artificial pollination. Furthermore, flower size increased the number of floral visitors, although it did not affect the frequency of florivory. Our results demonstrate that petal removal indirectly decreased 75% of female reproductive output via decreased flower visits by pollinators and that flower size mediated indirect interactions between florivory and floral visitors.     

Island–mainland difference in <Emphasis Type="Italic">Nicotiana glauca</Emphasis> (Solanaceae) corolla length: a product of pollinator-mediated selection?

A match between floral and pollinator traits, such as that between unique island plants and pollinators, is often thought to be the product of pollinator-mediated selection. I examined whether the floral morphology of an introduced hummingbird-pollinated plant, Nicotiana glauca (tree tobacco, Solanaceae), is under selection by pollinators on the California Channel Islands where it is a recent colonist. I first determined differences in floral morphology and pollinator composition between island and mainland populations of N. glauca. I found that island plants have detectably longer corollas (on average 1 mm) and are visited by hummingbird species with on average 1–2 mm longer bills than common mainland visitors. Corolla length differences were not found to be associated with site abiotic differences. Flower size does not vary consistently with season and corolla width is very consistent across sites. I tested whether island–mainland corolla length differences are the product of pollinator-mediated selection by measuring phenotypic selection and per visit effectiveness. Contrary to expectations, a longer corolla was not consistently associated with higher pollen transfer or seed count on the islands. Per visit effectiveness of longer and shorter-billed hummingbirds did differ; however, effectiveness did not depend on corolla length. Although I failed to detect expected patterns of selection for longer corollas on islands, I cannot rule out weak or past pollinator-mediated selection. It is also possible that despite the apparent match between pollinator and floral traits, island–mainland differences in corolla length are instead due to other environmental effects, selection unrelated to pollinators, or stochastic processes such as drift.     

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

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

Specialized pollination in the African milkweed Xysmalobium orbiculare: a key role for floral scent in the attraction of spider-hunting wasps

Specialized pollination by prey-hunting wasps is poorly documented in rewarding plants. Furthermore, the mechanisms of achieving specialization are not clear since flowers typically produce exposed nectar and have no morphological adaptations (such as long spurs) to exclude non-pollinating visitors. We investigated the pollination of Xysmalobium orbiculare and explored the functional roles of floral scent and nectar in attracting pollinators and deterring nectar robbers. Floral visitor observations showed that this milkweed is visited almost exclusively by pompilid wasps in the genus Hemipepsis. These wasps were the only insects to carry pollinia, and a cage experiment confirmed their effectiveness in removing and inserting pollinia on flowers. Hand-pollinations showed that plants are genetically self-incompatible and thus reliant on pollinators for seed set. Palatability experiments with honeybees showed that nectar is distasteful to non-pollinating insects and is therefore likely to play a functional role in deterring nectar thieves. Choice experiments in the field showed that the wasp pollinators are attracted primarily by floral scent rather than visual cues. Analysis of spectral reflectance of flowers revealed that flowers are dull colored and are unlikely to stand out from the background vegetation. We conclude that X. orbiculare is specialized for pollination by spider-hunting wasps in the genus Hemipepsis and utilizes floral scent to selectively attract its pollinators and unpalatable nectar to deter non-pollinating visitors.     

Pollinators cause stronger selection than herbivores on floral traits in Lobelia cardinalis (Lobeliaceae)

Measures of selection on floral traits in flowering plants are often motivated by the assumption that pollinators cause selection. Flowering plants experience selection from other sources, including herbivores, which may enhance or oppose selection by pollinators. Surprisingly, few studies have examined selection from multiple sources on the same traits. We quantified pollinator-mediated selection on six floral traits of Lobelia cardinalis by comparing selection in naturally and supplementally (hand-) pollinated plants. Directional, quadratic and correlational selection gradients as well as total directional and quadratic selection differentials were examined. We used path analysis to examine how three herbivores--slugs, weevils and caterpillars--affected the relationship between floral traits and fitness. We detected stronger total selection on four traits and correlational selection (γ(ij)) on three trait combinations in the natural pollination treatment, indicating that pollinators caused selection on these traits. Weak but statistically significant selection was caused by weevil larvae on stem diameter and anther-nectary distance, and by slugs on median-flower date. In this study, pollinators imposed stronger selection than herbivores on floral traits in L. cardinalis. In general, the degree of pollen limitation and rate of herbivory are expected to influence the relative strength of selection caused by pollinators or herbivores.     

Raissa L. Berg's contributions to the study of phenotypic integration,with a professional biographical sketch

Raissa L. Berg had a remarkable career in many respects and an impact on the study of phenotypic integration that continues to increase over 50 years after the publication of her seminal paper in that area. She was born and lived most of her life in Russia, with most of her research focused on measuring spontaneous mutation rates in Drosophila. She was forced to abandon this work during the height of Lysenko''s power in Russia, so she turned temporarily to the study of correlation patterns in plants; ironically, this work has had a more enduring impact than her main body of research. She showed that floral and vegetative traits become decoupled into separate correlation ‘pleiades’ in plants with specialized pollinators, but floral and vegetative traits remain correlated in plants that have less specialized pollination. Unfortunately, her plant work is often mis-cited as providing evidence for increased correlations among floral traits due to selection by pollinators for functional integration, a point she never made and one that is not supported by her data. Still, many studies of correlation pleiades have been conducted in plants, with the results mostly supporting Berg''s hypothesis, although more studies on species with generalized pollination are needed.     

A meta‐analysis of the agents of selection on floral traits

Floral traits are hypothesized to evolve primarily in response to selection by pollinators. However, selection can also be mediated by other environmental factors. To understand the relative importance of pollinator‐mediated selection and its variation among trait and pollinator types, we analyzed directional selection gradients on floral traits from experiments that manipulated the environment to identify agents of selection. Pollinator‐mediated selection was stronger than selection by other biotic factors (e.g., herbivores), but similar in strength to selection by abiotic factors (e.g., soil water), providing partial support for the hypothesis that floral traits evolve primarily in response to pollinators. Pollinator‐mediated selection was stronger on pollination efficiency traits than on other trait types, as expected if efficiency traits affect fitness via interactions with pollinators, but other trait types also affect fitness via other environmental factors. In addition to varying among trait types, pollinator‐mediated selection varied among pollinator taxa: selection was stronger when bees, long‐tongued flies, or birds were the primary visitors than when the primary visitors were Lepidoptera or multiple animal taxa. Finally, reducing pollinator access to flowers had a relatively small effect on selection on floral traits, suggesting that anthropogenic declines in pollinator populations would initially have modest effects on floral evolution.     

Floral ecology of Oreocharis pumila (Gesneriaceae): a novel case of sigmoid corolla

Attraction of pollinators and successful pollen transfer represent the primary targets of selection during flower evolution, leading to repeated evolutionary shifts between pollinators and consequently to the diversification of floral forms. However, most studies in floral evolution focus on the characteristics of flowers with straight corolla tube. Here, we report on an unusual form of sigmoid corolla combined with protandry and herkogamy in a Chinese species of Gesneriaceae, Oreocharis pumila (formerly Opithandra pumila). Contrary to species with sigmoid corollas studied previously, the base of the corolla tube of this species is inclined at an oblique angle downwards before the tube bends forward, and the stigma and anthers are included in the upper part of the corolla tube. The plants were found to be self‐compatible but incapable of autonomous selfing. Successful pollination was found to depend fully on the presence of insect pollinators (Nomia sp.) and pollen grains are the greatest reward for the visitors. Different from the other sigmoid flowers, the sigmoid corolla of O. pumila was not found to favor insect pollinators with long flexible proboscises. A mechanical fit between floral morphology and pollinator was found, in which only small insect visitors with specialized visiting behavior are legitimate pollinators. The protandry combined with herkogamy in the sigmoid corolla tube strongly ensures pollination efficiencies. Oreocharis pumila is the only species with sigmoid corolla in the genus Oreocharis. We hypothesize that such a corolla has arisen through selection due to inadequate pollination in early spring in the mountainous habitat that O. pumila occupies.