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.     

Nonadditive effects of flower damage and hummingbird pollination on the fecundity of Mimulus luteus

Flower herbivory and pollination have been described as interactive processes that influence each other in their effects on plant reproductive success. Few studies, however, have so far examined their joint effects in natural populations. In this paper we evaluate the influence of flower damage and pollination by the hummingbird Oreotrochilus leucopleurus on the fecundity of the Andean monkey flower Mimulus luteus. We performed a 2×2 factorial experiment, with artificial clipping of lower petals and selective exclusion of the hummingbird as main factors. In spite of the relatively low proportion (27.5%) of the variance in seed production accounted for by the full factorial model, artificial damage and hummingbird exclusion, as well as their interaction, were highly significant, indicating nonadditive effects of factors on plant fecundity. In the presence of hummingbirds, undamaged flowers had a seed production that was 1.7-fold higher than for damaged flowers, suggesting that the effect of flower damage on female reproductive success occurs probably as a consequence of hummingbird discrimination against damaged corollas. This result indicates that the impact of flower herbivory on plant fecundity was contingent on the presence or absence of hummingbirds, suggesting that pollinators may indirectly select for undamaged and probably resistant flower phenotypes. A second interaction effect revealed that undamaged flowers produced 78.5% more seeds in the absence of rather than in the presence of O. leucopleurus, raising the question of the ecological mechanism involved. We suggest that the strong territorial behavior exhibited by the bee Centris nigerrima may confine the foraging activities of the remaining bee species to safe sites within exclosures. Overall, our results provide evidence that hummingbird pollination and flower herbivory have interdependent effects on M. luteus fecundity, which indicates that it will be difficult to predict their ecological and evolutionary consequences unless interactions are analyzed in an integrated form.     

Pollination biology ofSymphonia globulifera (Clusiaceae)

The pollination biology ofSymphonia globulifera was studied in Central Amazonia, Brazil. As suggested by the bird syndrome of the flowers, these are mainly pollinated by hummingbirds. Occasional visits by other birds, butterflies and more rarely bees, as well as tamarin monkeys were also observed.Trigona bees partly destroy the flower tube to rob nectar. The possibility thatS. globulifera may not be primarily adapted to hummingbird pollination is discussed. The pollen is intermixed in an oily fluid secreted by the anthers (antheroil). Each of the five stigmas consists of a pore-like opening at the apex and a small chamber behind it. The antheroil mixed with pollen is absorbed by capillarity into the chamber when deposited on the pore. the pollen germinates inside the stigma. The presence of antheroil and pore-like stigmas in the flowers of the closely relatedPlatonia insignis indicate a similar mode of pollination. The results of this study are compared with observations in some otherClusiaceae (Caraipa, Clusia, Garcinia, Mahurea), where floral oils or floral resin occur. The role of these substances in the pollination process and their relation to the evolution of flower biology inClusiaceae are briefly discussed.     

Effect of floral orifice width and shape on hummingbird-flower interactions

Nectar guides are common among insect-pollinated plants, yet are thought to be rare or absent among hummingbird-pollinated plants. We hypothesize that the lower lips and trumpet-shaped orifices of many hummingbird flowers act as nectar guides to direct hummingbirds to the flowers' nectar and orient the birds for pollination. To test this hypothesis we conducted laboratory experiments using flowers of Monarda didyma (bee balm) and M. fistulosa (wild bergamot), which have orifice widths of about 4 mm and 2 mm, respectively, and latex flowers with orifice widths of 4 mm and 2 mm and three orifice shapes (trumpet, lipped, and lipless). Rubythroated hummingbirds (Archilochus colubris) made fewer errors during bill insertion and spent a smaller proportion of their feeding visit in error at M. didyma flowers than at M. fistulosa flowers, and at unaltered flowers of both species than at flowers with lower lips removed. Handling times were longer at both lipped and lipless flowers of M. didyma than at those of M. fistulosa, and at lipped than at lipless flowers of M. didyma. The average duration of contact between a hummingbird and a flower's anthers and stigma was longer at M. didyma than at M. fistulosa for both lipped and lipless flowers, and at lipped than at lipless M. didyma flowers. Hummingbirds missed the openings of latex flowers with their bills more frequently and spent a greater percentage of their total feeding visit in error at (i) 2-mm than at 4-mm flowers of all three shapes, (ii) lipless flowers than at trumpet or lipped flowers, and (iii) lipped flowers than at trumpet flowers of both widths. The duration of hummingbird/anther contact was longer at (i) 2-mm than at 4-mm flowers of all shapes, (ii) lipped than at trumpet or lipless flowers, and (iii) lipless than at trumpet flowers for both widths. No significant differences in handling times of hummingbirds were observed among any of the latex flower shapes or widths. Our results demonstrate that orifice shapes can act as guides by reducing the frequency of feeding errors by visiting hummingbirds, and that effects of orifice shape on pollination must be considered in conjunction with flower widths and locations of anthers and stigmas.     

The pollination biology of two species of Helicteres (Malvaceae) with different mechanisms of pollen deposition

Species of Helicteres are pollinated mainly by hummingbirds and bats. Most species pollinated by hummingbirds have a mechanism of depositing pollen on the top of the pollinator's head such as is shown in this work for Helicteres sacarolha. H. brevispira has an unusual mechanism of depositing pollen grains under the tail or on the abdomen of the hummingbirds. The top of the birds’ head may be considered an efficient place to transport pollen grains, because it is plain, easily accessible for deposition and donation of pollen and not easily accessible for grooming, while the tail is movable and inclined. Thus, H. brevispira pollinators may carry or transfer fewer amounts of pollen grains than H. sacarolha pollinators from one flower to another. If a large amount of pollen grains is lost, a higher quantity of flower or pollen has to be produced to guarantee reproductive success. Plants of H. brevispira set higher number of flowers and pollen grains per flower than H. sacarolha and have also higher rates of fruit and flower abortion. Thus, pollination efficiency of H. brevispira may be reached by high pollen and flower production. Flower change mechanism presented in this species may be also involved with the optimization of pollinator feeding and pollination efficiency.     

Flowering phenology,pollen flow and fruit production in the andean shrub Befaria resinosa

Summary In the eastern Andes of Colombia, the shrub Befaria resinosa (Ericaceae) has peaks of flowering that are separated by extended periods of low flower production. The effect that these fluctuations in flower production have on pollen flow was investigated by using fluorescent dye as a pollen analog. Dye applied to open flowers was dispersed over long distances more often during low flower production than during high flower production. Whether enhanced pollen dispersal during flowering lows is of benefit to individual plants is not clear. The proportion of flowers that set fruit is positively correlated with flower abundance, negating the possibility that increased pollen dispersal results in a higher rate of fruit production due to outbreeding effects. It is also difficult to attribute the pattern of fruit production to changes in pollinator visitation rates, which are negatively correlated with flower abundance in the case of hummingbirds and not correlated at all with flower abundance in the case of insects. An opportunistic, large-bodied hummingbird (Colibri coruscans) visits B. resinosa during high flowering and may be a particularly effective pollinator, accounting for some of the increase in the proportion of flowers setting fruit. Rainfall is positively correlated with flower production and may be an important factor in shaping flowering phenology, but it is not significantly correlated with the proportion of flowers setting fruits. The possibility that low-level flowering may counteract inbreeding that results from peak flowering is discussed.     

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.     

Variation in the intensity of pollination inDrosera tracyi: Selection is strongest when resources are intermediate

Summary I propose that the strength of selection is greatest when resource levels are intermediate. This idea was partially tested using artificial character variation for petal size inDrosera tracyi. This plant opens one flower each morning, with stigmas becoming available and pollen being presented simultaneously throughout the population. Bees remove all the pollen that can be removed and deposit all the pollen that can be deposited in one or two visits. Visitation rates track blooming density, as do pollen removal and deposition. I measured selection as the difference in pollen removal and deposition between flowers with trimmed petals versus flowers with normal petals. In one meadow, I found a wide range of levels of pollination and corresponding levels of selection, and selection was strongest at intermediate levels of pollination. This might mean that organisms are adapted to conditions when resources are at intermediate levels even though they may experience those conditions relatively rarely.     

Flowering patterns of long-lived Heliconia inflorescences: implications for visiting and resident nectarivores

Summary Flowering patterns of four Heliconia (Heliconiaceae) species in Trinidad, West Indies were examined for their predictability and availability to the nectarivores that rely on Heliconia floral nectar. Principal flower visitors are trapling hermit hummingbirds; inflorescences are inhabited by nectarivorous hummingbird flower mites that move between inflorescences by riding in the hummingbirds' nares. Heliconia inflorescences flower for 40–200 days, providing long-term sources of copious nectar (30–60 l per flower), but each Heliconia flower lasts only a single day. As an inflorescence ages the interval increases between open flowers within a bract; wet-season inflorescences produce open flowers more slowly than dry-season conspecifics.Estimated daily energy expenditures for hermit hummingbirds demonstrate that slow production of short-lived open flowers plus low inflorescence density preclude territorial defense of Heliconia by the hermits. Heliconia flowering patterns are viewed as a means of (i) regulating reproductive investment by the plants through staggered flower production over long periods of time, and (ii) maintaining outcrossing by necessitating a traplining visitation pattern by its hummingbird pollinators. I suggest that Heliconia exhibit a two-tiered pollination system by using hermit hummingbirds primarily for outcrossing and using hummingbird flower mites primarily for self-pollination.     

Bees provide pollination service to Campsis radicans (Bignoniaceae), a primarily ornithophilous trumpet flowering vine

1. Pollination syndromes refer to stereotyped floral characteristics (flower colour, shape, etc.) that are associated with a functional group of pollinators (bee, bird, etc.).
2. The trumpet creeper Campsis radicans, endemic to the southeast and mid‐west United States, has been assigned to the hummingbird‐pollination syndrome, due mainly to its red, trumpet‐shaped flowers.
3. Previous studies demonstrated that the ruby‐throated hummingbird Archilochus colubris is C. radicans' primary pollinator, but anecdotal data suggest various bee species may provide pollination service when hummingbirds are absent.
4. This study characterised C. radicans nectar volume and concentration by time of day. Nectar volume was suitable for hummingbirds, but concentration was higher than typical hummingbird‐pollinated plants (～20% w/w); at ～30% w/w, it approached the concentration expected in bee‐pollinated plants (～50% w/w). We also found substantial amounts of nectar at night.
5. Two C. radicans populations received virtually no hummingbird visits, but the number of bees were markedly higher than in the populations previously described. Interestingly, there were no night‐time visitors despite the large quantity of nocturnal nectar.
6. Based on previously published pollen delivery per visit by various species, this study estimated that cumulative deposition by bees routinely reached pollen deposition thresholds for setting fruit in C. radicans. They are, unequivocally, the predominant pollinators in these populations, thus providing pollination service in the absence of hummingbirds.
7. These results highlight C. radicans as a food source for native bees and add to the understanding of how floral phenotypes can facilitate pollination by disparate functional groups.

     

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 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.     

Pollination Ecology and Effect of Nectar Removal in Macleania bullata (Ericaceae)1

The floral syndrome of Macleania bullataYeo (Ericaceae) reflects its adaptation to hummingbird pollination. Its flowers, however, are subject to high levels of nectar robbing. I examined the floral visitor assemblage of M. bullata in a tropical montane wet forest in southwestern Colombia, focusing on the behavior of the visitors. I also tested for the presence of nocturnal pollination and the effects of nectar removal on new nectar production. The principal floral visitors were the nectar robbing hummingbirds Ocreatus underwoodii (19.1% of visits) and Chlorostilbon mellisugus (18.9%). Only two species of long–billed hummingbirds visited the flowers of M. bullata as “legitimate” pollinators: Coeligena torquata (14.7% of visits) and Doryfera ludoviciae (14.3%). The remaining visits constituted nectar robbing by bees, butterflies, and other species of hummingbirds. Nocturnal pollination took place, although fruit set levels were 2.4 times higher when only diurnal pollination was allowed as opposed to exclusively nocturnal pollination. Nectar robbers removed floral nectar without pollinating the flower. Treatments of experimental nectar removal were carried out to examine if flowers synthesize more nectar after nectar removal. Nectar removal increased the total volume of nectar produced by each flower without affecting sugar concentration. Thus, nectar robbing can impose a high cost to the plants by forcing them to replace lost nectar.     

Exploring the boundary between pollination syndromes: bats and hummingbirds as pollinators of<Emphasis Type="Italic"> Burmeistera cyclostigmata</Emphasis> and<Emphasis Type="Italic"> B. tenuiflora</Emphasis> (Campanulaceae)

In this study I documented the degree of specialization in the pollination systems of Burmeistera cyclostigmata and B. tenuiflora (Campanulaceae) to explore the potential role of floral isolation in the diversification of the genus. I asked which floral characteristics are important in specializing on either bat or hummingbird pollination, and whether overlap between these floral syndromes can exist. I examined nocturnal and diurnal pollen deposition, pollinator visitation rates, and single visit effectiveness and related them to intra- and interspecific variation in Burmeistera floral characteristics at Monteverde, Costa Rica. Bats and hummingbirds visited both Burmeistera species, and bats pollinated both species. Owing to differences in floral morphology, however, hummingbirds effectively pollinated only B. tenuiflora. The generalized pollination system of B. tenuiflora demonstrates that there can be overlap in the boundary between ornithophily and chiropterophily, and that nectar production and timing of anthesis do not serve as barriers between these syndromes. The high intraspecific variation in floral color from green to red or purple did not correlate with either nocturnal or diurnal pollen deposition. Degree of flower accessibility did affect pollination; nocturnal pollen deposition significantly decreased as flowers become more obstructed. In Burmeistera, floral morphology and accessibility appear to be the most important floral characteristics for specialization at the boundary between ornithophily and chiropterophily.     

Pollen consumption by flower mites in three hummingbird-pollinated plant species

Laboratory studies suggest that pollen consumption by flower mites may decrease the male fitness of the plant by reducing the available pollen for dispersal. Here we assessed pollen consumption by flower mites under natural conditions in three plant species with long-lived, protandrous flowers, Moussonia deppeana (Gesneriaceae), Lobelia laxiflora and L. cardinalis (Lobeliaceae). Total pollen mass was measured after 24 and 48 h in flowers exposed to flower mites and excluded from hummingbirds, flowers exposed to mites and hummingbird visitation, and in flowers recently opened with dehisced anthers. Compared with recently opened flowers, pollen availability was reduced about half in the presence of flower mites and the same effect was observed in the three plant species. Our results suggest that flower mites are removing a great deal of pollen and the reduction of pollen implies the possibility of direct impact on pollen transfer.     

Notes on the floral morphology in Vivianiaceae (Geraniales)

The functional floral morphology of the three genera of Vivianiaceae (= Ledocarpaceae, Geraniales), Rhynchotheca, Viviania and Balbisia, is compared. Likely pollination mechanisms are inferred from morphology and field observations. The flowers of Viviania are nectariferous and apparently zoophilous with nectar as the (primary) pollinator reward. Balbisia has pollen flowers without nectaries, its showy corolla indicates that it is also zoophilous with pollen as sole pollinator reward; bees were observed as flower visitors. One taxon (B. gracilis) may be anemophilous. Rhynchotheca has flowers without petals, with large, pendulous anthers and lacks nectaries. It shows synchronous mass flowering in its natural populations and is evidently anemophilous. A comparison with other Geraniales shows that nectar flowers with small anthers are likely the ancestral condition in Vivianiaceae. This suggests that the pollen flowers with larger anthers of Balbisia and Rhynchotheca may represent an apomorphic condition. The documentation of pollen flowers and anemophily in Vivianiaceae expands the range of known floral and pollination syndromes in Geraniales.     

Evidence of rodent pollination inCajophora coronata (Loasaceae)

Vegetative and floral features ofCajophora coronata (Loasaceae) suggest adaptations to pollination by rodents: (1) mammal guard represented by a covering of stinging hairs; (2) geoflory; (3) white corolla; (4) open flowers with copious low concentration nectar; (5) abundant pollen; (6) maximum pollen and nectar presentation in the afternoon hours and in the night. Palynological analysis revealed pollen loads ofC. coronata on the nostrils and whiskers of captured rodents (Graomys griseoflavus, fam.Muridae). Pollen and anther remains were also found in faeces sampled in the surroundings. Additional evidence includes rodent footprints obtained by placing smoked plates beneath the flowers, which revealed flower visitation during the night. These observations are to our knowledge the first evidence of flower visitation by rodents in South America and the first in the New World outside the range of flower bats and bat flowers.     

Effect of artificial feeders on pollen loads of the hummingbirds of Cerro de la Muerte, Costa Rica

Although sugar-water feeders are commonly used by enthusiasts to attract hummingbirds, little is known about how they affect hummingbird behavior and flower use. We studied the highland hummingbird assemblage of Cerro de La Muerte, Costa Rica, both at a site with permanent feeders (La Georgina Restaurant) and further from it. We examined how feeder use and monopolization affected seasonal changes in pollen loads during four sampling periods, including dry and wet seasons, from 2003-2005. We expected that species monopolizing the feeders would carry little or no pollen whatsoever, and would have pollen loads characterized by low floral diversity, in contrast with species less dependent on feeders. We obtained pollen samples from 183 individuals of four hummingbird species captured around the feeders using mist nets, which were compared with a pollen reference collection of plants with a pollination syndrome by hummingbirds. The same methods were implemented at a site 3km away from the feeders. Feeder usage was quantified by counting the number of times hummingbirds drank from the feeders in periods of 4min separated by 1min. The effects of hummingbird species and season on pollen load categories were assessed using a nominal logistic regression. The alpha species at the site, the Fiery-throated Hummingbird (Panterpe insignis), dominated the feeders during the dry season. Meanwhile, in the wet season, feeder usage was more evenly distributed across species, with the exception of the Volcano Hummingbird, Selasphorus flammula, which occupies the last place in the dominance hierarchy. Pollen loads of hummingbirds captured near feeders were low in abundance (more than 50% of captured individuals had zero or low pollen loads), and low in species richness (96% of the hummingbirds with pollen from only one plant genus, Centropogon). Overall pollen loads increased during the dry season coinciding with peaks in flower availability, although the majority of captured hummingbirds carried no pollen. Mist nets located 3km from La Georgina returned few captures (one-to-three specimens) per sampling date, contrasting with observations made before feeders were present. These results suggest that sugar-water feeders gather hummingbirds in over considerable distances drawing them away from flowers. The competitive and antagonistic pattern shown between feeders and flowers indicate that natural pollination system could be significantly altered. Supplementing hummingbirds with food seems likely to interfere with pollination networks already stressed by many anthropogenic effects.     

Notes on the pollination mechanisms ofMoraea inclinata andM. brevistyla (Iridaceae)

Individual flowers ofMoraea inclinata are nectariferous and last about six hours. They appear to be pollinated largely by bees in the familyHalictidae (Lasioglossum spp.,Nomia spp.,Zonalictus) and to a lesser extent by bees in the familyAnthophoridae (Amegilla). The mechanism of bee-pollination inM. inclinata is the Iris type; i.e., each flower consists of three pollination units (an outer tepal, a partly exserted anther, and the opposed style branch which terminates in a pair of petal-like crests). Bees rarely visit more than one pollination unit per flower. Transferral of pollen to the bee is passive and nototribic although all bees collected on the flowers were female and 55% of the bees carried pollen loads with 2–5 pollen taxa in their scopae.Moraea brevistyla flowers are nectariferous but lack scent and last two days. They are visited infrequently by bees and only one femaleLasioglossum spec. carried the pollen ofM. brevistyla. Unlike flowers ofM. inclinata those ofM. brevistyla deposit pollen only on the head and thorax. Bee-mediated autogamy in both species is avoided due to the erratic foraging patterns of the bees and the flexibility of each stigma lobe as the bee backs out of the flower. Approximately 2–4 flowers in the inflorescences of both species (6–8 flowers/infloresence) develop into capsules.     

INDIRECT SELECTION OF STIGMA POSITION IN IPOMOPSIS AGGREGATA VIA A GENETICALLY CORRELATED TRAIT

Experimental manipulation of a trait can be used to distinguish direct selection from selection of correlated traits and to identify mechanisms of selection. Here we use experiments to investigate phenotypic selection of stigma position in angiosperm flowers. In natural populations of the subalpine herb Ipomopsis aggregata, plants with more strongly exserted stigmas receive more pollen per flower, indicating selection favoring stigma exsertion during the pollination stage of the life cycle. We pose four hypotheses for this association, two involving direct selection on stigma position and two involving indirect selection of a correlated floral trait. The first three hypotheses were tested using hand pollinations that mimicked natural hummingbird visitation, and by presenting captive hummingbirds with a series of flowers that differed in stigma and anther positions, sex ratio, and presence of anthers. In these experiments, pollen deposition either was independent of stigma exsertion or was highest on inserted stigmas, suggesting direct selection against exserted stigmas. In natural populations, however, stigma exsertion is highly correlated with time spent by the protandrous flowers in the pistillate phase. When we manipulated the latter trait in the field, pollen deposition increased with duration of exposure to hummingbirds, indicating indirect selection for stigma exsertion. Stigma exsertion and time spent in the pistillate phase are genetically and phenotypically correlated, as shown by a quantitative genetic experiment conducted in the field with paternal half sibships. Our results suggest that the evolution of stigma position can be driven by selection of a genetically correlated trait.