POLLINATION ADAPTATION IN PEDICULARIS LANCEOLATA

Cinematographic, stereophotographic, and visual observations have revealed that the zygomorphic, nectarless flower of Pedicularis lanceolata Michx. is pollinated in northeastern Ohio by pollen-foraging workers of three Bombus species. Foragers hang inverted from the asymmetrical corolla and remove pollen with their front and middle legs from anthers concealed by the galea. The stigma contacts pollen deposited especially on the median portion of the forager's first abdominal sterilite. Insect exclosures and pollinator collections demonstrated the obligate pollination dependence of the flower on Bombus workers. Of 152 corbicular pollen loads from workers foraging on P. lanceolata, Gentiana andrewsii, Prunella vulgaris and five composite species in the same habitat, 84.2% contained P. lanceolata pollen; 75.8% of the latter contained P. lanceolata pollen exclusively. Possible coadaptive relationships of Pedicularis flowers and pollinators are discussed.     

THE POLLINATION DYNAMICS OF SYMPATRIC SPECIES OF PEDICULARIS (SCROPHULARIACEAE)

Sympatric populations of Pedicularis oederi, P. cystopteridifolia, and P. groenlandica on the Beartooth Plateau (Montana) were obligately dependent on Bombus pollinators. Their corolla colors were mutually distinct to insect vision, but their nectars had identical sugar components. Analysis of corbicular pollen loads of pollinating insects indicated a high degree of polylecty. Queen/worker ratios of pollinators on plant species corresponded to the parallel phenological sequences of plant blooming and insect caste development. The total number of individual pollinators of each Bombus species on all plants was directly related to the number of plant species it pollinated, but a comparable relationship between the number of pollinators on a plant species to the number of Bombus species pollinating it was not found. Morphological and behavioral correspondence of floral mechanisms and pollinators form an integral part of the general pattern of coadaptive evolution of the floral ecology of Pedicularis in North America known from previous studies. Reproductive isolation between Pedicularis species in this study is attributed to internal barriers. Wide overlaps of blooming seasons, proboscis lengths of bumblebee species and castes, and pollinator species on Pedicularis species suggest resource sharing, rather than resource partitioning or competition for resources among plant and insect species and individuals.     

POLLINATION ADAPTATION IN PEDICULARIS CANADENSIS

During the spring of 1966 and 1967, operation of the pollination mechanism of Pedicularis canadensis L. flowers by nectar- and pollen-foraging bumblebee (Bombus Latr.) queens was observed in an Iowa relict prairie and was recorded by high-speed cinematography. The stigma and style were found to sweep the forager's pronotum crevice as head and tongue were introduced into the 12-mm corolla tube. Pollen deposited in the crevice was not removed as the forager's middle leg only groomed pollen laterally deposited on head and scutum. Thirty corbicular pollen loads from 417 foragers collected on nine prairie plant species included pollen from Pedicularis canadensis, Aquilegia canadensis L., Dodecatheon meadia L., and two unidentified plants not found in the prairie. The pollination mechanism was considered closely adapted morphologically and phenologically to bumblebee queens of eight species found foraging on Pedicularis.     

THE POLLINATION ECOLOGY OF PEDICULARIS ON MOUNT RAINIER

Six native species of Pedicularis in Mount Rainier National Park in Washington State were studied for their reproductive relationships with animal pollinators. Cinematographic and stereophotographic records revealed pollination of the nectariferous P. bracteosa and P. rainierensis by upright, nectar-foraging queens and workers of five bumblebee (Bombus Latr.) species and by inverted workers scraping pollen from anthers concealed within the corolla galea. The nectarless, rostrate flowers of P. contorta, P. groenlandica, P. ornithorhyncha, and P. racemosa were pollinated by pollen-foraging workers and occasional queens virbrating pollen from concealed anthers. Insect exclosure methods revealed complete absence of fruiting in the absence of insects, and pollinator collections further indicate obligate dependence of the plants upon bumblebees for their sexual reproduction. Analysis of corbicular pollen loads from pollinators suggested that pollinator species are not monolectic but that individual pollinators range from monolectic to polylectic. Measurements indicated limited correlations between lengths of corolla tubes and tongues of nectar-foraging insects. Each nectarless Pedicularis species occupied a different, specific habitat, but P. bracteosa and the endemic P. rainierensis were sympatric in part. Each species had a unique spectral reflectance pattern from the corolla. Proximity of habitats and overlap of blooming periods of all Pedicularis species eliminate the possibility of contemporary geographic or phenological reproductive isolation. It is suggested that behavioral interactions of the plants and their insect pollinators may have been instrumental in the past in reproductively isolating these species, hybrids of which are unknown.     

Impact of pre‐ and post‐pollination barriers on pollen transfer and reproductive isolation among three sympatric Pedicularis (Orobanchaceae) species

• Pedicularis is the largest genus in the Orobanchaceae (>300) with many species co‐occurring and co‐blooming in subalpine to alpine meadows in the Himalayas. Although it is well known that different Pedicularis species place pollen on different parts of the same bumblebee's body, thus reducing interspecific pollen transfer, it is not known whether post‐pollination components also contribute to reproductive isolation (RI).
• In this study, we quantified the individual strengths and absolute contributions of six pre‐ and post‐pollination components of RI between three sympatric species in two pairs; Pedicularis gruina × Pedicularis tenuisecta (gru × ten) and Pedicularis comptoniifolia × Pedicularis tenuisecta (com × ten).
• All three Pedicularis species shared the same Bombus species. Individual foragers showed a high, but incomplete, floral constancy for each species. Therefore, pre‐pollination barriers were potentially ‘leaky’ as Bombus species showed a low but consistent frequency of interspecific visitation. The RI strength of pre‐pollination was lower in com × ten than in gru × ten. In contrast, post‐pollination barriers completely blocked gene flow between both sets of species pairs. Two post‐pollination recognition sites were identified. Late acting rejection of interspecific pollen tube growth occurred in com♀ × ten♂, while seeds produced in bi‐directional crosses of gru × ten failed to germinate.
• We propose that, although floral isolation based on pollen placement on pollinators in the genus Pedicularis is crucial to avoid interspecific pollen transfer, the importance of this mode of interspecific isolation may be exaggerated. Post‐pollination barriers may play even larger roles for currently established populations of co‐blooming and sympatric species in this huge genus in the Himalayas.

     

THE POLLINATION ECOLOGY OF SOLANUM ROSTRATUM (SOLANACEAE)

The pollination mechanisms and pollen vectors of Solarium rostratum have been examined by greenhouse experiments and field studies. Although the capacity for autogamy exists in this weedy annual, it rarely occurs because of two factors: (1) the morphology of the flower and (2) the foraging behavior of the various species of Bombus, the primary pollen vector in the regions studied. The percentages of geitonogamy and xenogamy are dependent on the flight pattern of the bees and the number of open flowers on a plant.     

Pollen-Foraging Dynamics of Subalpine Bumblebees (Bombus Latr.)

Abstract A 23-year study on Mount Rainier of nectar-foraging hummingbirds and pollen-foraging bumblebees (Bom-bus Latr.) indicated a constant relative frequency of Bombus species in the area and a wide occurrence of insect species on flowers plus a wide range of flower species pollinated by a single insect. Early-blooming plants had a high queen/worker pollinator ratio, while workers predominated on later-blooming plants. No altitudinal difference in distribution of Bombus species occurred. Analysis of 955 corbicular pollen loads from 1158 bumblebees collected yielded 49.5% monolecty for queens and 34.5% for workers with a wider range for queens than for workers. Colors of corollas photographed in visible and ultraviolet light corresponded to the visual spectra of animal pollinators. In the stable plant-pollinator community investigated, pollinating insect activity appears phenologically controlled by floral anthesis and behaviorally related to floral form and function. Bumblebee tongue length, however. Is not a valid determinant for foraging niche separation except in Castilleja with a deep corolla tube accommodating long tongues of hummingbirds and bumblebees. It is concluded that in a biotic community well-coordinated with the physical environment, limited flower constancy of pollen-foraging pollinators appears to contribute a necessary degree of adaptive versatility through sharing of insect and floral resources. Flower constancy is primarily a function of the circumstance in which a pollinator operates and not simply a characteristic of the pollinator itself.     

Buzz-pollination in Neotropical bees:genus-dependent frequencies and lack of optimal frequency for pollen release

Over 50 genera of bees release pollen from flower anthers using thoracic vibrations,a phenomenon known as buzz-pollination.The efficiency of this process is directly affected by the mechanical properties of the buzzes,namely the duration,amplitude,and frequency.Nonetheless,although the effects of the former two properties are well described,the role of buzz frequency on pollen release remains unclear.Furthermore,nearly all of the existing studies describing vibrational properties of natural buzz-pollination are limited to bumblebees(Bombus)and carpenter bees(Xvlocopa)constraining our current understanding of this behavior and its evolution.Therefore,we attempted to minimize this shortcoming by testing whether flower anthers exhibit optimal frequency for pollen release and whether bees tune their buzzes to match these(optimal)frequencies.If true,certain frequencies will trigger more pollen release and lighter bees will reach buzz frequencies closer to this optimum to compensate their smaller buzz amplitudes.Two strategies were used to test these hypotheses:(i)the use of(artificial)vibrational playbacks in a broad range of buzz frequencies and amplitudes to assess pollen release by tomato plants(Solarium Ivcopersicum L.)and(ii)the recording of natural buzzes of Neotropical bees visiting tomato plants during pollination.The playback experiment indicates that although buzz frequency does affect pollen release,no optimal frequency exists for that.In addition,the recorded results of natural buzz-pollination reveal that buzz frequencies vary with bee genera and are not correlated with body size.Therefore,neither bees nor plants are tuned to optimal pollen release frequencies.Bee frequency of buzz-pollination is a likely consequence of the insect flight machinery adapted to reach higher accelerations,while flower plant response to buzz-pollination is the likely result of its pollen granular properties.     

AN EXPERIMENTAL STUDY OF THE FLORAL ECOLOGY OF DODECATHEON MEADIA

An established colony of Dodecatheon meadia on glacial drift in southeastern Wisconsin was observed for its insect pollination interrelationships. Twelve randomly distributed plants from which insects were excluded failed to produce seed, while plants exposed to insect visits set abundant seed. Female solitary bees of 2 species, viz., Augochloropsis metallica fulgida (Smith) and Lasioglossum forbesii (Robertson), and queens and workers of 7 species of Bombus were observed collecting pollen from the pendant anther cone by rapid wing vibration, while hanging inverted from the cone tip. This behavior—cinematographically recorded—was found fundamentally identical to that of females of the same species of solitary bees and of queens and workers of 5 species of Bombus on Solanum dulcamara, and of females of Lasioglossum forbesii (Robertson) and workers of 2 species of Bombus on Lycopersicum esculentum Mill. No other insects were found to pollinate these morphologically similar flowers in this manner, and crepuscular pollinators were not observed. Experimental modifications of form, function, and position of Dodecatheon flowers were offered to the pollinators, and behavioral changes of the insects were noted. Constituents of insect pollen loads were examined, and relationships of the pollinators to the flora of the region were noted. The detailed ecological study of insect pollen vector behavior as an aid in discovering biosystematic relationships of plant populations is suggested.     

Variation in stigma morphology – How does it contribute¶to pollination adaptation in Pedicularis (Orobanchaceae)?

 Stigma morphology in Pedicularis and its role in pollination have not been evaluated. This paper reports for the first time the relationship between stigma morphology and other aspects of floral design. 17 species of Pedicularis representing all the different types of corolla structure in the genus were studied in the field and in the laboratory. Results indicate that the stigmatic surface morphology of Pedicularis species is related to the type of corolla structure occurring in the species. Pollination studies in eight Pedicularis species demonstrated adaptation between stigmatic surface morphology and other aspects of floral biology. Species with larger, more corrugated stigmatic surfaces always possess a subsidiary construction (“tooth” or “beak”) on the galea. In addition, they have relatively longer flower tubes, higher stigmatic pollen loads, bigger pollen size and a shorter blooming period for individual flowers. Finally, the authors discuss the evolutionary significance of floral design in genus Pedicularis. Received April 8, 2002; accepted June 11, 2002 Published online: December 11, 2002     

Pollen-Ovule Ratio and Gamete Investment in Pedicularis （Orobanchaceae）

The Pedicularis species provides ideal materials to study floral evolution because of their substantial flower variation based on a narrow genetic basis, even though they are almost exclusively pollinated by bumblebee. These traits allow us to detect the evolutionary trends of floral parameters without considering genetic background and the difference of pollination vectors. The pollen-ovule ratio is widely used to estimate the pattern of resource investment in two sexual functions in flowering plants. Forty species representing all of the corolla types in Pedicularls were used to study pollen-ovule ratio, gamete investment, and their correlations. Results show that pollen-ovule ratio does not differ among both different corolla types and taxonomic groups. It is therefore suggested that pollen-ovule ratio should be a parallel evolution. The correlations between pollen-ovule ratio and pollen size （-）, and ovule size （＋） can be successfully explained in terms of sex allocation theory. The biological significance of such relationships was also discussed. Additionally, we analyzed the pattern of resource investment into female gamete, which has been somewhat neglected, and found that plants have different patterns of gamete investment between the two sexual functions.     

Inflorescence Height Affects Visitation Behavior of Bees–A Case Study of an Aquatic Plant Community in Bolivia1

We studied the bee fauna visiting a plant community of 10 species of flowering aquatic plants in an inundated savanna region in Bolivia. In total we observed 36 bee species in 17 genera at the flowers. Cluster analysis of the similarities among the plant species in terms of their visitor spectra showed a division into two groups: plants with inflorescence heights shorter than the grass height and plants with inflorescences projecting out of the surrounding vegetation. Larger bees of the genera Apis, Melipona, Bombus, and Xylocopa were observed only at flowers above the surrounding vegetation. Smaller, mainly solitary bees (e.g., Augochlorella, Ancyloscelis) visited flowers in the dense vegetation near the water surface. Analyses of the pollen loads revealed that most individuals were highly flower constant. When bees carried different pollen types, it was generally pollen from flowers within a single stratum. We discuss specialization, flower constancy, competition, and different foraging strategies as possible reasons for stratum fidelity.     

Bees assess pollen returns while sonicating Solanum flowers

Summary Can bees accurately gauge accumulating bodily pollen as they harvest pollen from flowers? Several recent reports conclude that bees fail to assess pollen harvest rates when foraging for nectar and pollen. A native nightshade (Solanum elaeagnifolium Cavanilles) that is visited exclusively for pollen by both solitary and social bees (eg. Ptiloglossa and Bombus) was studied in SE Arizona and SW New Mexico. The flowers have no nectaries. Two experiments were deployed that eliminated pollen feedback to the bees by experimentally manipulating flowers prior to bee visits. The two methods were 1) plugging poricidal anthers with glue and 2) emptying anthers of pollen by vibration prior to bee visitation. Both experiments demonstrated that bees directly assess pollen harvest on a flower-by-flower basis, and significantly tailor their handling times, number of vibratile buzzes per flower and grooming bouts according to the ongoing harvest on a given flower. In comparison to experimental flowers, floral handling times were extended for both Bombus and Ptiloglossa on virgin flowers. Greater numbers of intrafloral buzzes and numbers of times bees groomed pollen and packed it into their scopae while still on the flower were also more frequent at virgin versus experimental flowers. Flowers with glued andreocia received uniformly brief visits from Bombus and Ptiloglossa with fewer sonications and virtually no bouts of grooming. Curtailed handling with few buzzes and grooms also characterized visits to our manually harvested flowers wherein pollen was artificially depleted. Sonicating bees respond positively to pollen-feedback while harvesting from individual flowers, and therefore we expect them to adjust their harvesting tempo according to the currency of available pollen (standing crop) within Solanum floral patches.     

Do specialized flowers promote reproductive isolation? Realized pollination accuracy of three sympatric Pedicularis species

Background and Aims

Interest in pollinator-mediated evolutionary divergence of flower phenotype and speciation in plants has been at the core of plant evolutionary studies since Darwin. Specialized pollination is predicted to lead to reproductive isolation and promote speciation among sympatric species by promoting partitioning of (1) the species of pollinators used, (2) when pollinators are used, or (3) the sites of pollen placement. Here this last mechanism is investigated by observing the pollination accuracy of sympatric Pedicularis species (Orobanchacae).

Methods

Pollinator behaviour was observed on three species of Pedicularis (P. densispica, P. tricolor and P. dichotoma) in the Hengduan Mountains, south-west China. Using fluorescent powder and dyed pollen, the accuracy was assessed of stigma contact with, and pollen deposition on, pollinating bumble-bees, respectively.

Key Results

All three species of Pedicularis were pollinated by bumble-bees. It was found that the adaptive accuracy of female function was much higher than that of male function in all three flower species. Although peak pollen deposition corresponded to the optimal location on the pollinator (i.e. the site of stigma contact) for each species, substantial amounts of pollen were scattered over much of the bees'' bodies.

Conclusions

The Pedicularis species studied in the eastern Himalayan region did not conform with Grant''s ‘Pedicularis Model’ of mechanical reproductive isolation. The specialized flowers of this diverse group of plants seem unlikely to have increased the potential for reproductive isolation or influenced rates of speciation. It is suggested instead that the extreme species richness of the Pedicularis clade was generated in other ways and that specialized flowers and substantial pollination accuracy evolved as a response to selection generated by the diversity of co-occurring congeners.     

The pollination ecology of Pedicularis rex subsp. lipkyana and P. rex subsp. rex (Orobanchaceae) from Sichuan, southwestern China

Pedicularis is one of few genera for which pollination ecology has been studied extensively. Although over half of the species of Pedicularis are found in the mountains of southwestern China, pollination ecology has been studied there on a few species only. The present paper reports pollination ecology of Pedicularis rex subsp. lipskyana and P. rex subsp. rex from Sichuan, southwestern China. The two subspecies are nectariferous, with sugar content 28% in P. rex lipskyana and 22% in P. rex, respectively. The flowers of the two subspecies are adapted to pollination by bumblebee workers. Bumblebees are the primary and effective pollinators although honeybees were also observed pollinating P. rex subsp. lipskyana at one studied population. Usually bumblebees entered the corolla tube from the right side in an upright or a nearly half-inverted position to imbibe nectar located at the base of the corolla tube. The stigma usually contacts the side region of the thorax and abdomen or occasionally directly contacted pollen loads, leading to pollination of flowers. Much less commonly, bumblebees foraged on flowers of P. rex subsp. rex in an inverted position for pollen, which pollinated flowers sternotribically. We suggest that pollination mechanism is closely associated with floral morphology. Some important differences were found from a previous study on P. rex in floral morphology and the primary pollination mechanism.     

BUMBLEBEE POLLINATION RELATIONSHIPS ON THE BEARTOOTH PLATEAU TUNDRA OF SOUTHERN MONTANA

The coadaptive, dynamic relationship between the members of a floral community and their respective bumblebee pollinators was studied on the alpine-tundra of the Beartooth Plateau in southern Montana. A total of ten species of Bombus was observed foraging for pollen and/or nectar on Castilleja pulchella, Delphinium bicolor, Lupinus monticola, Mertensia ciliata, Oxytropis campestris, Penstemon procerus, and Trifolium dasyphyllum. The number of Bombus species per plant species ranged from 1 to 9. Based on relative percentage of pollen types in corbicular loads, monolectic foragers comprised 53.5% and polylectic foragers 46.5% of the bumblebees. Examinations of relative length of nectariferous corolla-tubes, tongue-length of pollinators, foraging frequency of pollinators, phenology of floral anthesis, and stature of plants did not indicate specific resource partitioning. Non-tundra-nesting bumblebees from lower elevations preferred adventive or typically non-tundra plants. Examination of perianth colors in visible light by reflectance spectrophotometry and in long-wave (360 nm) ultraviolet light by photography disclosed well-defined visible light reflectance spectra in all species but ultraviolet reflectance patterns only in D. bicolor. Insect collections and exclosure studies indicated all plant species except D. bicolor and P. procerus are highly reliant on bumblebee pollinators.     

Pollen size-number trade-off and pollen-pistil relationships in Pedicularis (Orobanchaceae)

Current patterns of floral design in Pedicularis must have undergone an evolutionary process of interacting among components of floral traits, and then formed internal relationships among these traits. To detect such correlations, which may provide insight to understand flower evolution, 40 Pedicularis species representing all corolla types of the genus were studied. Results show that, interspecifically, pollen size correlates negatively with pollen number, but positively with pistil length. This suggests that plants evolve an optimal pollen size, which balances the advantages of large pollen size for gametophytic competition against the fecundity disadvantages of fewer pollen grains. In contrast to sex allocation theory, this study does not find a trade-off, but an interspecific positive correlation between pollen and ovule number. This is consistent with the hypothesis that genetic variation for resource acquisition may in part be responsible for the lack of negative correlation between male and female function.This work was supported by the State Key Basic Research and Development Plan, China (Grant No. G2000046804) to YHG. The authors would like to thank Peter K. Endress and two anonymous reviewers for providing critical comments and helpful suggestions, Qing-Feng Wang, Jing-Yuan Wang and Jin-Ming Chen for their helpful suggestions. Shi-Guo Sun, Jing Xia, and Qian Yu are thanked for their assistance in both the field work and laboratory phases of the project.     

Buzz pollination in eight bumblebee-pollinated Pedicularis species: does it involve vibration-induced triboelectric charging of pollen grains?

MethodsEight sympatric buzz-pollinated species of Pedicularis that share bumblebee pollinator species were studied, giving a rare opportunity to compare sonication behaviour of a shared pollinator on different plant species.ConclusionsSonication behaviour of B. friseanus differs among Pedicularis species, not only because worker bees assort themselves among plant species by body size, but also because bees of a given size adjust the buzz frequency to achieve a vibration velocity corresponding to the floral traits of each plant species. These findings, and the floral traits that characterize these and other buzz-pollinated species, are compatible with the hypothesis of vibration-induced triboelectric charging of pollen grains.     

FLOWER VISITATION,POLLEN DEPOSITION,AND POLLEN-TUBE COMPETITION IN HIBISCUS MOSCHEUTOS (MALVACEAE)

The potential influence of pollen-tube competition on offspring “quality” has received considerable attention in recent years. Yet the prevalence of pollen competition in natural populations is largely unknown because few investigators have actually measured rates of pollen deposition on stigmas. In this study, we assess the potential for pollen-tube competition in natural populations of the self-compatible, pollinator-dependent herbaceous perennial, Hibiscus moscheutos. Individual flowers averaged two to four visits per 15 min by potential pollinators (Ptilothrix and Bombus), and about 34% of these visits involved contact with a stigma. The median number of pollen grains deposited on virgin stigmas per contact visit was 70 grains (values ranged from 0 to 889), and flowers averaged about four contact visits per hour. Approximately 360 pollen grains must reach stigmas for full seed set to occur in a typical flower (an average ovary has 139 ovules, and 2.6 pollen grains are required per seed). Within 2 and 3 hr exposure to pollinators, 65% and 97% of the flowers received excess pollen (>360 grains) and median stigmatic pollen loads exceeded the number of ovules by a factor of 4.0 and 5.4, respectively. Based on 3 yr observations, it is concluded that pollen competition may frequently occur in this species.     

MECHANISM OF SELECTION FAVORING A WIDE TUBULAR COROLLA IN CAMPANULA PUNCTATA

A previous study of Campanula punctata pollinated by Bombus diversus showed greater male reproductive success in plants with wider corollas when male reproductive success was measured by paternity analysis. Pollen removal alone was not a good measure of male reproductive success. The aim of the current study is to elucidate the mechanism underlying the selection on corolla width in C. punctata. Multiple regression analysis of male reproductive success in experimental populations revealed that the advantage of a wide corolla to the male is independent of the corolla width of pollen recipients, indicating that the position of pollen deposited on Bombus may not be an important factor for selection. However, the number of pollen grains that fell on the petal or off the flower and were lost at the first visit of Bombus (pollen fall) decreased with increasing corolla width, so that most pollen grains removed from a wide flower were deposited onto the pollinator. In a narrow flower, a greater proportion of the pollen removed was wasted through pollen fall. Pollen removal does not reflect male reproductive success, at least in part because of the loss of pollen in some flowers through pollen fall. The positive relationship between wider corollas and reduced loss of pollen through pollen fall is likely to lead to greater male reproductive success of wider flowers under repeated visits of pollinators. Decreased pollen fall, probably due to more gentle contact between pollen and bees in flowers with wider corollas, may be one of the mechanisms underlying the selection on corolla width of C. punctata.