SELECTION ON POLEMONIUM BRANDEGEEI (POLEMONIACEAE) FLOWERS UNDER HUMMINGBIRD POLLINATION: IN OPPOSITION,PARALLEL, OR INDEPENDENT OF SELECTION BY HAWKMOTHS?

Particular floral phenotypes are often associated with specific groups of pollinators. However, flowering plants are often visited, and may be effectively pollinated by more than one type of animal. Therefore, a major outstanding question in floral biology asks: what is the nature of selection on floral traits when pollinators are diverse? This study examined how hummingbirds selected on the floral traits of Polemonium brandegeei, a species pollinated by both hummingbirds and hawkmoths. In array populations of P. brandegeei, we measured pollen movement, and female (seeds set) and male (seeds sired) fitness under hummingbird pollination. We then compared the patterns of selection by hummingbirds with our previous study examining selection by hawkmoths. We documented contrasting selection on sex organ positioning through female function, with hummingbirds selecting for stigmas exserted beyond the anthers and hawkmoths selecting for stigmas recessed below the anthers. Furthermore, hummingbirds selected for longer and wider corolla tubes, and hawkmoths selected for narrower corolla tubes. Therefore, contrasting selection by hawkmoths and hummingbirds may account for variation in sex organ arrangements and corolla dimensions in P. brandegeei. We documented how floral traits under selection by multiple pollinators can result in either an intermediate “compromise” between selective pressures (sex organs) or apparent specialization (corolla tube length) to one pollinator.     

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

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

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.     

'Anti-bee' and 'pro-bird' changes during the evolution of hummingbird pollination in Penstemon flowers

Floral phenotypes may be as much the result of selection for avoidance of some animal visitors as selection for improving the interaction with better pollinators. When specializing on hummingbird-pollination, Penstemon flowers may have evolved to improve the morphological fit between bird and flower, or to exclude less-efficient bees, or both. We hypothesized how such selection might work on four floral characters that affect the mechanics of pollen transfer: anther/stigma exsertion, presence of a lower corolla lip, width of the corolla tube, and angle of flower inclination. We surgically modified bee-pollinated P. strictus flowers changing one trait at a time to make them resemble hummingbird-pollinated P. barbatus flowers, and measured pollen transfer by bumblebees and hummingbirds. Results suggest that, apart from 'pro-bird' adaptations, specific 'anti-bee' adaptations have been important in shaping hummingbird-flowers. Moreover, some trait changes may have been selected for only if changing in concert with other traits.     

Breeding system of Macromeria viridiflora (Boraginaceae) and geographic variation in pollinator assemblages

This study explores the association between variation in pollinator type and flower size in Macromeria viridiflora (Boraginaceae) by studying the breeding system of the plant and the pollinator effectiveness of floral visitors. Studies were conducted at two sites where plants differ in flower size and floral visitors. Breeding system studies showed that while plants are self-compatible and occasionally produce seed autogamously, pollinators are important for reproductive success in the plants. However, plants are not pollinator-limited at these sites. Combining visitation rate and pollen deposition as measures of pollinator effectiveness, I found hummingbirds to be the most effective pollinators at both sites. Although hawkmoths also pollinate the flowers, they visit the flowers less frequently and, at one of the two sites, deposit less pollen. These results are consistent with the hypothesis that geographic variation in corolla size is the result of selection by different hummingbird species.     

Pollination ecology of Penstemon roseus (Plantaginaceae), an endemic perennial shifted toward hummingbird specialization?

Summary Pink-flowered tubular Penstemon roseus (Plantaginaceae), which has shifted partially to hummingbird pollination, blooms on high-elevation slopes in the mountains in Tlaxcala, Mexico. We studied the interactions between pollinator visitation rates to flowers, pollen removal and deposition, flower size, and nectar removal frequency on seed production in P. roseus. We combine observational and experimental studies in two contrasting natural populations. Our manual pollinations revealed that P. roseus is fully self-compatible. Autonomous self- and manual self-pollinated flowers matured as many seeds as when outcrossed, but outcrossing seems to become better than selfing as the flowering season progressed. Early in the season flowers that were bagged and hand-selfed, hand-outcrossed, or autonomously selfed, or unbagged and naturally pollinated had equal seed set in all four treatments. But later in the season, outcross pollen gave approximately twice as much seed set as the two self-treatments. Low levels of pollen receipt and pollen removal were consistent with the long time elapsed for a given plant to be visited by hummingbirds, which suggests pollen shortage in both sites. Despite differences in pollinator visitation rates to flowers, probability of flower visitation, removal and deposition of pollen, and nectar production rates between populations, we found that total nectar production had no effect on seed production at either site. The daily nectar secretion rate of 0.3–0.65 mg sugar per flower per 1–3 days was low relative to other hummingbird-adapted Penstemon species (typical range: 1.5–5 mg sugar per flower), and it might be intermediate between hummingbird- and bee-adapted Penstemon flowers. Our results support the hypothesis about a shift toward hummingbird pollination, and provide an example of a ‘despecialized’ Penstemon species, which attracts high-energy pollinators (hummingbirds) and profits from outcrossing, but retains bee-syndrome floral traits and low sugar production rates.     

An Assemblage of Hummingbird-pollinated Flowers in a Montane Forest in Southeastern Brazil

Relationships between ornithophilous flowers and hummingbirds have been little studied in southern South America, where hummingbird species richness is low. We studied an ornithophilous flower assemblage and the hummingbird pollinators in a montane forest in southeastern Brazil. Twenty-three native hummingbird-pollinated plant species in 21 genera and 14 families were observed. Bromeliaceae, Fabaceae, Gesneriaceae, and Lobeliaceae are represented by more than one species within the assemblage. Flower shapes vary from narrow tube to bowl-shape, but tubular flowers prevail. The variety of flower shapes and sizes results in diverse pollen placement on the body parts of hummingbird visitors, although pollen is deposited mostly on the bill. Sugar concentration in nectar averages 22.1%, and nectar volume per flower averages 16.9 μl. The plant populations bloom for one month to year-round, and their flowering approaches the steady-state pattern. Four flower subsets may be defined within the assemblage, each subset related to the bill size and foraging habits of the most frequent bird visitor. Of the six species of hummingbirds recorded at the study site, four are common and largely resident. The four hummingbirds differ in bill size, body mass, and favoured foraging sites, attributes which reflect their favoured flower subsets. One hermit and one trochiline hummingbird share most of the flower species they use, these two birds being the major pollinators within the flower assemblage. This montane forest community may be viewed as medium-rich in ornithophilous flower species and poor in hummingbird species.     

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.     

Long corollas as nectar barriers in <Emphasis Type="Italic">Lonicera implexa</Emphasis>: interactions between corolla tube length and nectar volume

Long corollas are a classical example of nectar barriers, because they prevent undesired visitors from consuming the reward intended for more effective pollinators. As the investment in nectar barriers increases, flower attractiveness and nectar rewards may also increase to maintain loyal visitation of most effective pollinators; and flowers may become more prone to nectar robbing. We evaluated the effect of nectar barriers (corolla tube length), two related traits (nectar volume and upper lip size) and the associated risk of nectar robbing, on the fecundity of Lonicera implexa plants from three populations differing in the abundance of its most efficient pollinator, the hummingbird hawkmoth Macroglossum stellatarum. Corolla tube length varied most among individuals within populations (45–46 % of total variance) and inflorescences within individuals (23–32 %), and showed little variation among populations (0.2–11 %). Longer corolla tubes were always associated with larger nectar volumes and larger upper lips, although the strength of the relationships varied across populations and years. Robbing frequency increased with corolla tube length, decreased with nectar volume and upper lip size, and its weak effects on fecundity were predominantly positive. Plant fecundity peaked at two different optima: long corollas with little nectar and short corollas with abundant nectar. However, the exact shape of the interaction between corolla length and nectar volume, as well as the combination of traits showing the highest fecundity, differed between populations and years. This variation could be explained by among-population differences in pollinator assemblages, and inter-annual changes in resources dedicated to reproduction. Our study shows that large nectar volumes can modulate the effect of corolla length as a nectar barrier, and that the combination of these two traits that maximises fecundity may be related to the identity of pollinators within each population.     

The importance of bees as pollinators in the short corolla bromeliad Aechmea caudata in southern Brazil

The majority of bromeliad species are pollinated by vertebrates, mainly hummingbirds and bats. However, bees are among the most frequent visitors in some short-corolla species with ornithophilous features, but only few studies identified insects as pollinators of these bromeliads. The importance of visitors for pollination success in Aechmea caudata (Bromeliaceae) was determined through the frequency and pollination effectiveness (measured as seed set/single visit) of its visitors in a secondary Atlantic forest area in southern Brazil. Aechmea caudata is self-incompatible and therefore pollinator-dependent. A total of 16 species were recorded visiting their flowers. Bees were the most rich and frequent taxon (91% of 647 visits). Bombus morio was the most frequent species (41%). Although the floral features of A. caudata, such as scentless, tubular corollas, yellow and red flowers, and nectar secretion during the whole diurnal anthesis, are related to ornithophily, the single hummingbird species Thalurania glaucopis failed to pollinate the flowers. Its low frequency (2.5%) apparently did not promote the pollen flux between conspecific bromeliads. Pollination tests showed that no seeds developed after hummingbird visits. Seeds were formed only at flowers visited by B. morio. We discuss our findings by contrasting them with the results on the similar and sympatric A. lindenii and by emphasizing the importance of bees for pollination of bromeliads with short corolla. Our results show that pollination effectiveness together with frequency data are necessary to analyze the complex interactions between plants and their flower visitors.     

The influence of insects and hummingbirds on the geographical variation of the flower phenotype in Mimulus luteus

We describe the geographical variation of corolla and nectar guide size in seven populations of Mimulus luteus (Phrymaceae) in central Chile, and examine whether flower phenotypes associate with taxonomic composition and flower visit patterns of pollinators across populations. Flowers showed higher variation in nectar guide size than corolla size. Mean corolla size increased with the proportion of bees and decreased with the proportion of lepidopterans in the pollinator assemblages. Nectar guide size increased with the proportion of hummingbirds in the pollinator assemblages. When the frequency of flower visits rather than taxonomic composition was considered, the results revealed similar patterns. Because these traits previously have been described as targets of bee- and hummingbird-mediated selection in M. luteus , our results have implications for understanding the processes that determine flower diversification in Chilean Mimulus . Although we cannot rule out ecological sorting as an explanation for the geographical association between pollinators and flower phenotypes, changes in the prevalence and importance of bees and hummingbirds across populations appear to account, at least in part, for the flower phenotypic variation across populations. The extent to which insect and hummingbird pollination in M. luteus produces pollinator-mediated divergence among populations needs to be examined in future studies.     

Geographical variation in floral traits of the tree tobacco in relation to its hummingbird pollinator fauna

Nicotiana glauca , a hummingbird pollinated plant, exhibits geographical variation in several floral traits. We examined whether geographical differentiation occurred for different flower characters and if this differentiation could be explained, at least in part, by the existence or abundance of different hummingbird species in the respective pollinator assemblages. The comparison between five populations showed significant variation in six floral traits and two female fitness measures. The traits that better discriminated between populations were corolla length and corolla width. There were metric correlations between corolla length and style length in all populations studied and, in four of the five populations, both corolla length and width were also correlated. Among plants in each population, seed weight was correlated positively and significantly with style exertion, suggesting that fruit quality is dependent on the degree of cross pollination. Assemblages of hummingbirds differed between populations in species composition, visitation frequencies, and bill length. Linear regression involving bill length of the more frequent hummingbird pollinators and corolla length yielded positive and significant relationships. Thus, there appears to be an adjustment between pollinators and flowers traits that have high incidence in the among population variation.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 657–667.     

Relative pollination effectiveness of floral visitors of Pitcairnia angustifolia (Bromeliaceae)

The effectiveness of flower visitors as pollinators will determine their potential role as selective agents on flower traits. Pitcairnia angustifolia has floral characters that would fit pollination by long-billed hummingbirds, and they should be the most effective pollinators for this plant. To test this prediction, we characterized the behavior of visitors toward flowers and their pollination effectiveness. Coereba flaveola (bananaquits) was the most frequent flower visitor and acted as a primary nectar robber; however, they pollinated incidentally and deposited pollen on stigmas. The endemic short-billed hummingbird Chlorostilbon maugaeus behaved as a secondary robber and did not pollinate flowers. As expected, the long-billed hummingbird, Anthracothorax viridis, was the most efficient visitor in terms of pollen deposition; however, it was the least frequent flower visitor. Introduced Apis mellifera (honeybees) were second in efficiency at depositing pollen and performed one third of the flower visits. Estimates of the expected rate of pollen deposition by each pollinator did not identify a single most effective pollinator. For P. angustifolia at least three flower visitors including an exotic bee and a nectar robber may be equally important to reproductive success. While these results limit our ability to make predictions on the role of hummingbird-pollination on current flower evolution, they do suggest the potential for pollination redundancy among flower visitors for P. angustifolia populations.     

Bimodal pollination system of the bromeliad Aechmea nudicaulis involving hummingbirds and bees

In order to compare the effectiveness of birds and insects as pollinators, we studied the floral biology of the bromeliad Aechmea nudicaulis (L.) Grisebach in the biome of the Atlantic rain forest, southern Brazil. On Santa Catarina Island, flowering extends from mid-September to the end of December, with diurnal anthesis. The reproductive system is obligatory xenogamy, thus pollinator-dependent. Flowers secrete 31.84 μl of nectar per day, with a mean sugar concentration of 23.2%. Highest nectar volume and sugar concentration occur at the beginning of anthesis. Most floral traits are characteristic for ornithophily, and nectar production appears to be adapted to the energy demand of hummingbirds. Continued secretion of the sucrose-dominated nectar attracts and binds visitors to inflorescences, strengthening trapline foraging behaviour. Experiments assessing seed set after single flower visits were performed with the most frequent visitors, revealing the hummingbird Thalurania glaucopis as the most effective pollen vector. In addition, bees are also functional pollinators, as substantiated by their high visitation frequency. We conclude that this pollination system is bimodal. Thus, there is redundancy in the pollination service provided by birds and bees, granting a high probability of successful reproduction in Ae. nudicaulis.     

Nectar robbing in Ipomopsis aggregata : effects on pollinator behavior and plant fitness

Hummingbirds foraging in alpine meadows of central Colorado, United States, face a heterogeneous distribution of nectar rewards. This study investigated how variability in nectar resources caused by nectar-robbing bumblebees affected the foraging behavior of hummingbird pollinators and, subsequently, the reproductive success of a host plant (Ipomopsis aggregata). We presented hummingbirds with experimental arrays of I. aggregata and measured hummingbird foraging behavior as a function of known levels of nectar robbing. Hummingbirds visited significantly fewer plants with heavy nectar robbing (over 80% of available flowers robbed) and visited fewer flowers on those plants. These changes in hummingbird foraging behavior resulted in decreased percent fruit set as well as decreased total seed set in heavily robbed plants. These results indicate that hummingbird avoidance of nectar-robbed plants and flowers reduces plant fitness components. In addition, our results suggest that the mutualisms between pollinators and host plants may be affected by other species, such as nectar robbers. Received: 22 April 1998 / Accepted: 12 May 1998     

Plant–hummingbird interactions in the West Indies: floral specialisation gradients associated with environment and hummingbird size

Floral phenotype and pollination system of a plant may be influenced by the abiotic environment and the local pollinator assemblage. This was investigated in seven plant–hummingbird assemblages on the West Indian islands of Grenada, Dominica and Puerto Rico. We report all hummingbird and insect pollinators of 49 hummingbird-pollinated plant species, as well as six quantitative and semi-quantitative floral characters that determine visitor restriction, attraction and reward. Using nonmetric multidimensional scaling analysis, we show that hummingbird-pollinated plants in the West Indies separate in floral phenotypic space into two gradients—one associated with the abiotic environment and another with hummingbird size. Plants pollinated by large, long-billed hummingbirds had flowers with long corolla tube, large amounts of nectar and showy orange-red colouration. These attracted few or no insect species, whereas plants pollinated by small, short-billed hummingbirds were frequently pollinated by insects, particularly lepidopterans. The separation of plants related to environmental factors showed that species in the wet and cold highlands produced large amounts of dilute nectar, possessed no or a weak odour, and were associated with few insects, particularly few hymenopterans, compared to plants in the dry and warm lowlands. The most specialised hummingbird-pollinated plants are found in the West Indian highlands where they are pollinated by mainly large, long-billed hummingbirds. At the other extreme, highly generalised plants growing in the dry and warm lowlands are pollinated by small, short-billed hummingbirds and numerous insect species. This illustrates that, even within the hummingbird-pollinated flora, pollination syndrome and the degree of specialisation may vary tremendously depending on pollinator morphology and environment. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Nectar extraction by hummingbirds: response to different floral characters

Summary Handling times of hummingbirds (Amazilia rutila and Cynanthus latirostris) visiting artificial flowers were a positive function of corolla length, nectar volume and nectar concentration. Corolla angle had no consistent effects on handling times. A multiple regression model explained 83% of the variation in handling times for these two species. The model also closely fit independent data from another hummingbird, Archilochus colubris, suggesting that it is general enough to apply to other medium-sized, short-billed hummingbird species. When examined across the range of variation normally encountered by hummingbirds in nature, corolla length and nectar volume had the largest effect on nectar extraction rates. At corolla lengths longer than a hummingbird's bill handling time increases markedly. Hummingbirds maximize their net rate of energy intake by selecting flowers with the shortest corolla, the highest nectar concentrations and the highest nectar volume. Since there is a positive relation between bill length and nectar extraction rate, it is surprising that most hummingbirds have relatively short bills.     

Stabilizing selection on nectar concentration in wild Petunia axillaris,as revealed by genetic analysis of pollen dispersal

Most animal-pollinated plants produce nectar as a pollinator reward. Despite the main role that nectar plays in plant-pollinator interactions, the impact of natural variation in nectar traits on realized male fitness is poorly known. Here, we assessed this relation for a wild Petunia axillaris population using paternity-based direct selection gradient analysis, which allowed us also to infer pollen dispersal patterns. Because male fecundity may depend on other traits which could be associated with nectar characteristics (i.e. volume and concentration), we also considered selection on other key reproductive traits. The analysis revealed that P. axillaris was a strict outcrosser, but that successful pollination occurred mainly among neighbours. Individual plants varied greatly in their male fecundity. Nectar concentration, a key feature of nectar that determines its profitability, was subjected to stabilizing selection. Selection through male function also affected corolla area (positive directional selection), corolla tube length (negative directional selection), and floral display size (stabilizing selection), but none of these traits were phenotypically correlated with nectar characteristics. Because nectar concentration affects the ability and foraging efficiency of different flower visitors to feed on nectar, stabilizing selection may reflect either the preference of the most effective pollinators, or antagonistic selection driven by pollinators and non-pollinating nectar consumers.     

云南草蔻花蜜分泌格局与访花动物行为及其对果实和种子产量的影响

依靠动物传粉的植物, 其繁殖成功 (胚珠受精与花粉散布 ) 很大程度上取决于访花动物的种类和拜访行为, 而访花动物的种类和行为又受植物提供给传粉者的回报, 主要是花蜜分泌格局的影响。通过对姜科山姜属植物云南草蔻 (Alpiniablepharocalyx) 花蜜分泌量及糖分含量的测定, 拜访动物种类、传粉昆虫拜访频率及停留时间的调查, 主要盗蜜者花松鼠 (Tamiopsswinhoei) 的盗蜜行为观察, 植物的结实率以及结籽量的分析等, 探讨花蜜分泌与传粉昆虫的关系以及盗蜜对果实及种子生产的影响。研究表明 :云南草蔻的两种花型花蜜的分泌量在一天的单花开花过程中呈现相反的格局, 花柱上举型花下午的花蜜分泌量高于上午, 而花柱下垂型花则上午略高于下午 ;两种花型花蜜的糖分浓度都随着开花时间而下降 ;共有 17种访花动物拜访云南草蔻的花, 其中 8种具有传粉作用 ;传粉昆虫的停留时间随拜访频率的不断增加而缩短 ;被盗蜜植株与未被盗蜜植株的结实率差异不显著而结籽量差异显著。