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.     

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.     

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.     

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.     

THE POLLINATION ECOLOGY OF DICENTRA CUCULLARIA

In northeastern Iowa and southwestern Wisconsin the flowers of Dicentra cuculiarla were found to be pollinated almost exclusively by Bombus bimaculatus nectar-foraging queens, which were phenologically synchronized in their emergence from hibernation with the flower's anthesis. Cinematographic and stereophotographic evidence indicated that pollen transfer was effected by the ventral side of the insect's head and anterior thorax contacting essential flower parts and to a lesser degree by the front and middle legs contacting pollen-laden edges of the inner petals. Lepidoptera, Diptera, and small Hymenoptera occasionally encountered on the flowers were ineffective in pollination. Abundant Apis mellifera pollen-foraging workers regularly effected pollination, but being an introduced species it exhibits no naturally developed pollination adaptation to the flower. Nectar spur perforation by B. affinis nectar-foraging queens did not affect plant fertility, and this behavior was related only in part to forager tongue length. Nectar-foraging behavior of B. bimaculalus queens on the flowers was correlated with the phenological development of the annual insect colonies.     

POLLINATION ADAPTATION IN PEDICULARIS GROENLANDICA

Cinematographic and stereophotographic records indicate that Pedicularis groenlandica is pollinated in the Colorado Front Range by seven species of pollen-foraging bumblebees (Bombus sp.) to which the nectarless flower is intricately adapted functionally and structurally. Removing pollen by wing vibrations of an oscilloscopically identified frequency significantly distinct from flight vibration frequency, foragers carried pollen loads with up to three foreign pollen types in addition to Pedicularis pollen, which was found in all loads. No direct correlation was evident between flight vibration frequency and combined body-pollen load weight, ambient air temperature, or forager species. The flower is phenologically and morphologically adapted to the worker caste of apparently any Bombus species available to it throughout the plant's montane-alpine zone vertical-distribution range. The evolutionary position of the pollination mechanism is considered in relation to the floral morphology of other species in the genus Pedicularis.     

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.     

THE POLLINATION ECOLOGY OF AQUILEGIA ELEGANTULA AND A. CAERULEA (RANUNCULACEAE) IN COLORADO

Aquilegia elegantula Greene and A. caerulea James occur in montane and subalpine habitats in the southern Rocky Mountains of western North America. The red and yellow flowers of A. elegantula are nodding, odorless, protogynous, and secrete a concentrated (44%) sucrose nectar in the floral spurs. Seed set in flowers under pollinator exclosures was 12% while seed set in open-pollinated flowers was 65%. The flowers of A. elegantula are pollinated primarily by the Broad-tailed Hummingbird (Selasphorus platycercus [Swainson]) and by at least three species of pollen-foraging bumblebees, of which Bombus occidentalis Greene is the most common. The blue and white flowers of A. caerulea are erect, mildly fragrant, protandrous, and secrete a 26% sucrose nectar. Seed set in caged flowers in the field averaged 39%. in uncaged flowers 54%. The most important pollinators of A. caerulea are the crepuscular hawkmoth, Hyles (=Celerio) lineata (Fabricius) and ten species of pollen-foraging Bombus. The most abundant bumblebee species, B. occidentalis, is also a frequent nectar thief. Differences in pollination systems alone probably do not constitute an effective anti-hydridization mechanism between A. elegantula and A. caerulea, but do serve to reinforce differences in habitat and flowering time that distinguish the two species.     

Pollen advertisement: chemical contrasts between whole-flower and pollen odors

Odors of pollen and whole flowers were compared in taxonomically unrelated species that offer pollen as the only food reward to pollinators. Volatiles were collected using headspace adsorption and analyzed by gas chromatography and mass spectrometry. The odor of pollen was found to be chemically distinct from the total flower odor, and this pollen-odor distinctness varied among the three species. In Papaver rhoeas (Papaveraceae), the contrast between pollen and whole-flower odors was most subtle, with differences observed only in the proportions of individual volatiles (almost exclusively aliphatic hydrocarbons). In Filipendula vulgaris (Rosaceae), pollen volatiles were fewer than in the flowers (comprising mainly benzenoids and fatty-acid derivatives) and their relative proportions produced an odor dominated by 2-heptadecanone that contrasted strikingly with the flower odor dominated by 2-phenyl ethanol. In Lupinus polyphyllus (Fabaceae), the pollen odor contained fewer volatiles and in differing proportions than the flower fragrance (comprising almost exclusively isoprenoids). The findings add to earlier chemical evidence of odor contrasts between pollen and other flower parts in two other species. Drawing on information from pollination studies of these various species, it is suggested that pollen odor is used by pollen-foraging insects both to discriminate between plant species and to assess reward availability in individual flowers, and that it might in addition serve a protective function against destructive flower-feeding insects and pathogens.     

The superiority of bumblebees to honeybees as pollinators: insect visits to raspberry flowers

Abstract.

• 1 The behaviour and activity patterns of Apis mellifera and of five species of Bombus were analysed in relation to climatic variables and nectar quality on three varieties of unsprayed cultivated raspberry (Rubus idaeus) in eastern Scotland.
• 2 Stages of floral morphology and reward were similar for the three varieties: young flowers offered both nectar and pollen, but medium and old flowers offered nectar only, in diminishing quantities.
• 3 A wide range of insects visited raspberry flowers, but bees were dominant, bumblebees being responsible for about 60% of all visits and honeybees making up most of the remaining percentage. All bees had substantial pollen deposited on their bodies during visits, though few specifically collected it.
• 4 Bombus spp. were found to favour young (receptive) flowers strongly, especially early in the morning when pollen was most abundant: whilst Apis visited unselectively. Bumblebees also foraged over substantially longer periods of the day, and in poorer weather, some being present at most times of observation; and they foraged more quickly in terms of flower visits per minute.
• 5 Bombus carried more pollen on their bodies than Apis, and also deposited more pollen on raspberry stigmas, with B.lapidarius and B.terrestris being particularly effective and also being the most abundant species. All bumblebees also foraged over a longer range, moving between canes and rows more frequently than did honeybees.
• 6 Bumblebees are therefore likely to be substantially more important as pollinators of raspberries than are honeybees, especially as raspberries though moderately self-fertile may exhibit metaxenia. Reasons why Bombus may be the preferred pollinator in most sites of raspberry cultivation are discussed, together with implications for present and future growers.

     

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.     

Behavioral responses by bumble bees to variation in pollen availability

Summary Pollen-collecting bumble bees (Bombus spp.) detect differences between individual flowers in pollen availability and alter their behavior to capitalize on rewarding flowers. Specific responses by bees to increased pollen availability included: longer visits to flowers; visits to more flowers within an inflorescence, including an increased frequency of revisits; an increased likelihood of grooming while the bee flow between flowers within the inflorescence; and more protracted inter-flower flights, probably because of longer grooming bouts. The particular suite of responses that a bee adopted depended on the pollen-dispensing mechanism of the plant species involved. Bees buzzed previously-unvisited Dode-catheon flowers longer than empty flowers. In contrast, pollen availability did not significantly affect the duration of visits to Lupinus flowers, which control the amount of pollen that can be removed during a single visit. Simulation results indicate that the observed movement patterns of bumble bees on Lupinus inflorescences would return the most pollen per unit of expended energy. The increased foraging efficiency resulting from facultative responses by bees to variation in pollen availability, especially changes in the frequency and intensity of grooming, could correspondingly decrease pollen dispersal between plants.     

An exception to Darwin's syndrome: floral position,protogyny, and insect visitation in Besseya bullii (Scrophulariaceae)

Darwin pointed out that plants with vertical inflorescences are likely to be outcrossed if the inflorescence is acropetalous (flowers from the bottom up), the flowers are protandrous (pollen is dispersed before stigmas are receptive), and pollinators move upward on the inflorescence. This syndrome is common in species pollinated by bees and flies, and very few exceptions are known. We investigated flowering phenology and pollinator behavior in Besseya bullii (Scrophulariaceae) and found that it did not fit Darwin's syndrome. The vertical inflorescence was acropetalous but the flowers were distinctly protogynous, so flowers with newly receptive stigmas appeared on the inflorescence above those with dehiscing anthers. A number of small insects visited B. bullii; bees in the family Halictidae (Augochlorella striata and Dialictus spp.) were most common. When insects moved between gender phases within inflorescences, they moved up more often than down (61% versus 39% of observations, respectively) but this difference was only marginally significant. Most visits were to male-phase flowers only, and this preference was more pronounced for pollen-foraging insects than for nectar-foraging insects. B. bullii was self-compatible, so its flowering characteristics potentially could result in considerable self-pollination. However, an average of 38% of the lowermost flowers opened before any pollen was available on the same inflorescence; these solo females had a high probability of outcrossing (though fruit set was relatively low in the bottom portion of the inflorescence). Upper flowers may also be outcrossed because downward insect movement was not uncommon. Therefore protogyny in B. bullii may not necessarily lead to more selfing than would protandry.     

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.     

COMPARATIVE REPRODUCTIVE BIOLOGY OF ACER PENSYLVANICUM AND A. SPICATUM (ACERACEAE)

Pollination mechanisms and floral features affecting reproduction were examined in two closely-related species, Acer pensylvanicum and A. spicatum. Intra-specific crossing experiments, studies of pollen stainability and ovule number, and observations of the flowers in the field revealed that neither species bears functionally hermaphroditic flowers. Three flower-types were found in each species: staminate, pistillate, and a third type that is morphologically hermaphroditic. The latter form sheds viable pollen, but the pistil does not contain ovules. Pollen-ovule ratios of both species are in the range of expectation for a facultatively xenogamous reproductive system. Outcrossing is accomplished by entomophily in both species. A variety of insects from several orders visit the flowers; however bees in the genus Andrena (Hymenoptera: Andrenidae), especially A. milwaukeensis, are considered the most important pollinators of both maple species because of their fidelity to Acer, their intrafloral behavior, and their ability to carry pollen. However, flies are the most abundant visitors to A. pensylvanicum. Apomixis is an important means of reproduction in A. spicatum. Although floral phenology of these maple species overlaps within a geographical region they were never found blooming simultaneously when growing together.     

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.     

FORAGING BEHAVIOR OF BOMBUS (HYMENOPTERA: APIDAE) IN RELATION TO AQUILEGIA POLLINATION

Observations on native and cultivated plants indicated that the ruby-throated hummingbird (Archilochus colubris L.) and at least four species of Bombus are probably effective pollinators of Aquilegia canadensis L. in southeastern Wisconsin. Bombus affinis Cresson perforated more than 90% of 2173 nectar spurs of flowers at full anthesis on wild plants. Cinematographic and stereo-photographic records of insects revealed a general behavioral pattern of mandibular perforation following exploration by antennae, maxillae, and tongue. Pollen-foraging behavior on 19 cultivated Aquilegia species and varieties was uniform, but nectar-foraging behavior varied with flower form and position and not with color variation within one flower form. Observations on marked insects showed that workers tended to forage in one manner on one plant variety, while queens foraging in one or more ways visited up to five different flower forms on one flight. Initial observations on neonate workers from a cultivated B. affinis colony suggested that a probably innate mandibular perforation behavior is not instinctively directed toward nectar-bearing floral parts, and that foraging behavior is capable of rapid establishment and considerable versatility.     

Convergent evolution of morphological specializations in Central European bee and honey wasp species as an adaptation to the uptake of pollen from nototribic flowers (Hymenoptera, Apoidea and Masaridae)

In the Central European apoid and masarid fauna, 13 bee species belonging to seven different taxonomic groups and one honey wasp species were found to be equipped with a specialized pollen-collecting apparatus on the face which is used to harvest pollen from nototribic flowers, viz. representatives of the Lamiaceae and the Scrophulariaceae. Pollen from these two plant families plays an important part in the larval nourishment of these hymenopteran species. The pollen-collecting apparatus consists of a peculiar facial pilosity composed of transformed hairs which are thickened at their base and either knobbed apically (Celonites abbreviatus) or extended into a thin tail which is either straight and bent at right angles ( Rophites spp., Anthophora borealis, A. furcata ) or wavy ( Anthidium spp., Anthocopa andrenoides, Osmia aurulenta, O. caerulescens ). Nototribic flowers are worked by pollen-collecting females by rubbing the facial area covered with the transformed hairs over the anthers (Celonites, Anthidium, Anthocopa, Osmia) , by buzzing the pollen amongst the transformed hairs (Anthophora Jurcata) or by a combination of rubbing movements and buzzing (Rophites) . Bee species lacking special morphological devices were observed to perform specialized behaviours when collecting pollen at nototribic flowers. Nototribic flowers, therefore, appear to be difficult to exploit for pollen. The raised position of the anthers in nototribic flowers as a possible means to reduce excessive pollen losses caused by pollen-collecting hymenopterans is discussed.     

THRIPS-MEDIATED SELF-POLLINATION OF TWO FACULTATIVELY XENOGAMOUS WETLAND SPECIES

Thrips and/or aphids played an important role in the self-pollination of two facultatively xenogamous herbs that inhabit wetlands in northwestern Iowa. In both Ranunculus sceleratus and Potentilla rivalis the fruit set and/or successful pollination of plants that were sprayed with malathion to kill thrips and aphids and caged to exclude typical flower visitors was substantially and significantly lower than that of open-pollinated and caged plants. We observed pollenbearing thrips and aphids on the flowers. The high fruit sets of emasculated flowers of R. sceleratus showed that insects moved pollen between flowers, and our observations of bees collecting pollen and moving between plants suggest that cross-pollination can occur in both species.     

Pollination ecology in sympatric winter flowering Helleborus (Ranunculaceae)

We studied biotic and abiotic factors that influence pollination in two sympatric winter flowering species. Helleborus foetidus and Helleborus bocconei flower simultaneously in winter. Although climatic conditions are not favorable for biotic pollination both species rely mainly on large bees of the genus Bombus. At the beginning of flowering, harsh climatic conditions are restrictive for insect visits. As flowering continues and temperatures rise, pollinator activity increases. The two plant species share pollinators that visit them indiscriminately. The flowers of the two species differ in form and insects visit H. foetidus by inserting their heads and H. bocconei ventrally: pollen load on insects is highly specialized. With the arrival of spring, many other species start to bloom and in spite of the large number of flowers still on the plants insects abandon Helleborus species. At the end of spring increasing biotic interactions take away pollinators from the Helleborus species.