Pollination Ecology of Pedicularis megalantha D. Don (Scrophulariaceae) in the Himachal Himalaya

Abstract In the summer of 1990, the pollination ecology of Pedicularis megalantha was studied in the montane-subalpine spruce-fir forest zone (2750-3050 m) on the north slope of Mt. Huttoo at Narkanda, Himachal Pradesh, in the Indian Himalaya. Its yellow, long-tubed, nectarless flower with a curled rostrum overarched by a broad, inverted lower corolla lip was pollinated exclusively by Bombus albopleuralis and B. tunicatus workers hanging inverted from the corolla and vibrating pollen from introrse anthers concealed within the galea and releasing pollen through a small ventral opening in the galea base. The stigma, protruding from the tip of the rostrum, contacted pollen deposited on the ventral side of the insect's thorax. Corbicular pollen loads from P. megalantha pollinators indicated equal numbers of monolectic and oligolectic foragers. P. megalantha appeared to suffer from competition for pollinators by Cynoglossum wallichii at one site but to be favored in a mixed plant community with nectariferous species offering a forage resource complementary to Pedicularis pollen. As in P. punctata , the long, nectarless corolla tube of P. megalantha appears to function in extending the rostrate vibration pollination mechanism beyond the plant's foliage, which would interfere with its function. It is not an adaptation for nectar-foraging lepidopteran pollinators. P. megalantha was also found to be a root hemiparasite.     

Pollination Ecology and Endemic Adaptation of Pedicularis howellii Gray (Scrophulariaceae)

Abstract Pedicularis howellii , endemic to the Siskiyou Mountains of California-Oregon, is a root hemiparasite obligately dependent upon bumblebee pollinators that remove pollen by vibration from its short-tubed, nectarless, rostrate flowers, which reflect visible and ultraviolet (360nm) light attractive to Bombus foragers. All six Bombus species in the study area pollinated the plant, but only on P. howellii and P. racemosa were B. mixtus workers the most abundant pollinators among the seven bumblebee-pollinated plants studied, including Delphinium decorum, Dodecatheon jeffreyi, Penstemon newberryi, P. shastensis, and Phacelia heterophylla. Analysis of corbicular pollen loads of Bombus pollinators indicated that pollen foragers on Pedicularis species were less pollen-constant than all other bumblebee pollinators. Although P. howellii and P. racemosa blooming periods overlapped slightly, phenological isolation of blooming periods of plants sharing the same pollinators was not evident. Chemical soil analysis of its habitat and quadrat analysis of the population structure of Pedicularis howellii indicated that the plant grows in a moderately fertile forest soil and is restricted to the edge of forest canopy openings where sunlight favors development of plants to the flowering stage. The endemism of P. howellii is related to a similar "edge effect" survival of P. furbishiae in a boreal forest riparian habitat previously studied.     

大王马先蒿的传粉综合征状及其生物地理学意义

对云南西北部中甸和昆明黑龙潭的大王马先蒿（ＰｅｄｉｃｕｌａｒｉｓｒｅｘＣｌａｒｋｅＣ．Ｂ）的不同居群进行了传粉生物学观察。大王马先蒿花为黄色,花冠短管、无喙、具二齿、无蜜腺,是一种原始的花冠类型。该种由红腹熊蜂（ＢｏｍｂｕｓｆｒｉｓｅａｎｕｓＳｋｏｒｉｋｏｖ）和明亮熊蜂（ＢｏｍｂｕｓｌｕｃｏｒｕｍＬ．）的工蜂在直立的位置上,通过震动花粉背触式传粉;同时也观察到红腹熊蜂的工蜂在倒悬的位置上,通过震动花粉腹触式传粉。熊蜂的工蜂在大王马先蒿上的这两种传粉综合征状的发现,可能是仅存在于马先蒿原始类型中的一种特殊现象。     

The Pollination Syndrome of Pedicularis rex (Scrophulariaceae) and Its Biogeographic Significance

The pollination biology of different populations of Pedicularis rex Clarke C B. was studied in Zhongdian of Northwest Yunnan and in Kunming of central Yunnan, respectively. Seed production depends exclusively upon pollination by bmnblebees ( Bombus Latr. ). The flowers are yellow, with short-tubed, erostrate and nectarless corolla. Two species of the bumblebee workers, Bombus friseanus Skorikov and B. lucorum L. foraged in an upright (nototribic) position for pollen. Meanwhile, Bombus friseanus workers also foraged in an inverted (stemotribic) position on P. rex, vibrating pollen from the anthers within the galea. This pollination syndrome was previously reported in the North American species, e.g.P, labradorica which has the same corolla-type with P. rex. A comparison of the corolla types and pollination syndrome on the species of Pediadaris in East Asia and North America indicates that such a pollination syndrome may be only found in the primitive corolla type of Pedicularis. In spite of the separation in the geological history, P. rex and P.labradorica share the same corolla type and pollination syndrome. Further study is needed to elucidate the biogeography of the Pedicularis.     

马先蒿属花冠形态的多样性与传粉式样的关系

马先蒿属(Pediculais)是有花植物中花冠形态多样化最为集中的属。该属主要的传粉者是熊蜂属(Bormbus)昆虫;在北美,熊蜂和蜂鸟是马先蒿植物一些种类有效的传粉者;也发现壁蜂(Osmia)为其传粉。不同的传粉机制要求某一特定的取食式样储藏和释放花粉。本文讨论了花冠类型的进化趋势与传粉式样和花粉形态的关系。传粉者的选择压力是决定花冠多样化的重要因素之一;花冠类型与传粉者和传粉行为紧密相关。马先蒿植物和传粉者的相互依赖与其花冠类型、功能和物候互相适应,但花冠类型与花粉形态两者之间似乎没有明显的一一对应关系。通过北美、日本和喜马拉雅不同地理分布马先蒿种类的比较研究表明,具有相同花冠类型的种类有着相同的传粉方式,花冠形态与传粉式样存在紧密的协同进化关系。     

马先蒿属植物花冠分化与繁殖适应的研究进展

结合已有的研究报道和作者近年来的工作,对马先蒿属（Pedicularis）植物的花冠多样化成因与繁殖适应特性进行了总结和探讨。通过对该属4种进化花冠型的花器官发生和分化的研究发现,花部各器官在发生和发育初期基本一致,后期上唇形态的分化是导致成熟花形态结构产生较大差异的重要阶段。孢粉学研究认为,花冠类型与花粉萌发孔类型之间具有显著相关性;萌发沟的演化可能与繁殖适应有一定的关系。分子系统学研究表明,多样化的花冠类型在不同的谱系内经过若干次的独立进化而表现出了高度的平行演化（parallelism）。传粉生物学研究证实,该属植物花冠多样化与其主要传粉者熊蜂属（Bombus）昆虫的传粉行为存在较为密切的关系。具有相同（似）花冠类型的马先蒿可能被同种或不同种的熊蜂以相同的方式访问,但在花粉落置位置上存在显著差异,这可能有助于同域分布重叠的物种间在生殖上的机械隔离,而花冠的分化在一定程度上促进了新的物种形成。     

Pollination Ecology and Endemism of Pedicularis pulchella Pennell (Scrophulariaceae)

Abstract Pedicularis pulchella Pennell, endemic to sparsely vegetated areas of alpine tundra scree in southwestern Montana and northwestern Wyoming, was found to be roat-hemiparasitic and obligately dependent for its pollination upon bumblebees of three non-tundra species that forage primarily in an inverted position for pollen scraped from anthers concealed in the galea, This sternotribic pollination syndrome is considered related to the short (5–6mm) proboscides of pollinators on flowers with deep (12.4mm), nectariferous corolla tubes and favoring pollen as an insect attractant. Photographic and spectropholomelric analysis of the red-purple floral color included prominent blue corolla and ultraviolet calyx reflections corresponding to dominant colors of bumblebee visual spectra. Nectar analysis by thin-layer chromatography and refractomctry indicated, respectively, the presence of fructose and sucrose, and a sucrose-equivalent concentration of dissolved solids exceeding 50%; both coincide with the general pattern of the genus. Analysis of pollen from corbicular loads of P. pulchella pollinators indicated relatively low pollen-constancy of insects and substantial foraging association with Vaccinium in the montane-subalpine zone. By contrast, pollinators on P. cystopteridifolia and Phyllodoce glanduliflora in a diverse tundra plant community on rich alpine turf revealed broad pollinator spectra (7–8 species), high pollen-foraging constancy on Pedicularis, and high nectar-foraging frequency on Phyllodoce : The pollination ecology and endemism of Pedicularis pulchtella are interpreted in terms of resource sharing, spatial competition of plant species, and selective stress of the physical environment.     

Division of labour within flowers: heteranthery,a floral strategy to reconcile contrasting pollen fates

In many nectarless flowering plants, pollen serves as both the carrier of male gametes and as food for pollinators. This can generate an evolutionary conflict if the use of pollen as food by pollinators reduces the number of gametes available for cross‐fertilization. Heteranthery, the production of two or more stamen types by individual flowers reduces this conflict by allowing different stamens to specialize in ‘pollinating’ and ‘feeding’ functions. We used experimental studies of Solanum rostratum (Solanaceae) and theoretical models to investigate this ‘division of labour’ hypothesis. Flight cage experiments with pollinating bumble bees (Bombus impatiens) demonstrated that although feeding anthers are preferentially manipulated by bees, pollinating anthers export more pollen to other flowers. Evolutionary stability analysis of a model of pollination by pollen consumers indicated that heteranthery evolves when bees consume more pollen than should optimally be exchanged for visitation services, particularly when pollinators adjust their visitation according to the amount of pollen collected.     

Pollination ecology and pollination system of Impatiens reptans (Balsaminaceae) endemic to China

BACKGROUND AND AIMS: China is one of the centres of geographical distribution of Impatiens L. Studies of the pollination ecology of this genus in China have, until now, been unreported. Impatiens reptans, a species endemic to China, was studied. The aims were to examine the pollination ecology and pollination system of this species, to compare its pollination ecology with other Impatiens species growing in Sumatra and Japan, and to discuss possible reasons for its limited distribution. METHODS: The pollination ecology of I. reptans was studied by carrying out continuous observations within three naturally growing populations. Its pollination system was studied using different pollination methods, marking and counting pollen grains, assessing pollen viability and observing pollinator behaviour. KEY RESULTS: The flowering phase of the protandrous I. reptans lasted for 89 d. The life span of an individual flower was 3.6 d. Primary pollinators were honey-bees and bumble-bees. Secondary pollinators were diurnal hawk moths and butterflies. Bombus briviceps and Bombus sp. were nectar gatherers. The mean nectar sugar concentration was 29.5 %, and the mean value of sucrose/glucose + fructose was 0.82. The proportion of seed set ranged from 0.857 to 0.873. Distances that seeds were ejected ranged from 0.58 to 1.17 m. Percentage seed germination under controlled conditions was 23.1. Pollen viability was highest on the day of anthesis and thereafter decreased. Ratios of pollen : ovules ranged from 958.8 to 970.6. CONCLUSIONS: Impatiens reptans reproduces by means of cross-pollination. Its dependence on a specialized habitat, a narrow environmental niche, a low percentage of seed germination, and habitat loss could be reasons for its limited distribution and endemism.     

Pollination Ecology and Endemic Trends in Pedicularis bracteosa var. atrosanguinea Pennell & Thompson (Scrophulariaceae) in North America

Abstract Pedicularis bracteosa var. atrosanguinea occurs locally in association with P. racemosa or P. groenlandica in the Olympic Mountains in Washington. Other plant species, e.g., Polygonum bistortoides, Lupinus argenteus var. parviflorus and Valeriana sitchensis compete for space and bumblebee pollinators within the study area. Pollinator sharing, resulting from such competition, may increase the frequency of unvisited flowers of P. bracteosa var. atrosanguinea. P. bracteosa var. atrosanguinea , with blood purple nectariferous flowers, is presumed to lack intense reflections of blue spectral components from its corollas in attracting bumblebees compared to those of P. racemosa and P. groenlandica . Six species of bumblebees ( Bombus ) and cuckoo bees ( Psithyrus ) pollinate P. bracteosa var. atrosanguinea . Of these, Bombus mixtus and B. occidentalis occur in higher frequencies and are the major pollinators of P. bracteosa var. atrosanguinea . Queen and larger worker bumblebees pollinate nototribically as they probe for nectar, while smaller worker bumblebees pollinate sternotribically while scraping pollen from anthers deeply hidden in the dome-shaped galea. Corbicular pollen loads of bumblebees collected in the study area contain Pedicularis pollen alone/in combination of Polygonum, Valeriana, Lupinus, Erigeron and Bidens , or exclusively of Polygonum or Valeriana. P. bracteosa var. atrosanguinea does not suffer seriously from deficient pollination but seedlings resulting from pollinated flowers may be subjected to natural selection pressure exerted by colonial plant species for space. P. bracteosa var. atrosanguinea does not propagate asexually but resumes aerial growth seasonally from the self-same underground root stocks. If seedlings are under continuous selection pressure for lack of space, P. bracteosa var. atrosanguinea is presumed to regenerate primarily by perennial root stocks. This behavior may favor endemism in P. bracteosa var. atrosanguinea .     

The Abundance and Pollen Foraging Behaviour of Bumble Bees in Relation to Population Size of Whortleberry (Vaccinium uliginosum)

Habitat fragmentation can have severe effects on plant pollinator interactions, for example changing the foraging behaviour of pollinators. To date, the impact of plant population size on pollen collection by pollinators has not yet been investigated. From 2008 to 2010, we monitored nine bumble bee species (Bombus campestris, Bombus hortorum s.l., Bombus hypnorum, Bombus lapidarius, Bombus pascuorum, Bombus pratorum, Bombus soroensis, Bombus terrestris s.l., Bombus vestalis s.l.) on Vaccinium uliginosum (Ericaceae) in up to nine populations in Belgium ranging in size from 80 m² to over 3.1 ha. Bumble bee abundance declined with decreasing plant population size, and especially the proportion of individuals of large bumble bee species diminished in smaller populations. The most remarkable and novel observation was that bumble bees seemed to switch foraging behaviour according to population size: while they collected both pollen and nectar in large populations, they largely neglected pollen collection in small populations. This pattern was due to large bumble bee species, which seem thus to be more likely to suffer from pollen shortages in smaller habitat fragments. Comparing pollen loads of bumble bees we found that fidelity to V. uliginosum pollen did not depend on plant population size but rather on the extent shrub cover and/or openness of the site. Bumble bees collected pollen only from three plant species (V. uliginosum, Sorbus aucuparia and Cytisus scoparius). We also did not discover any pollination limitation of V. uliginosum in small populations. We conclude that habitat fragmentation might not immediately threaten the pollination of V. uliginosum, nevertheless, it provides important nectar and pollen resources for bumble bees and declining populations of this plant could have negative effects for its pollinators. The finding that large bumble bee species abandon pollen collection when plant populations become small is of interest when considering plant and bumble bee conservation.     

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.     

Autonomous self‐pollination in the nectarless orchid Pogonia minor

The pollination biology of the nectarless orchid Pogonia minor was investigated in central Japan. The investigation revealed that the solitary flowers failed to attract pollinators, while high rates of fruit set were observed in the natural population. Comparable levels of fruit set were obtained in bagged, artificial self‐pollinated and artificial cross‐pollinated plants, indicating that the species is not pollinator‐limited for fruit set under natural conditions. Autonomous self‐pollination in P. minor resulted from a reduced rostellum, which allowed contact between the pollinia and the stigma. Self‐pollination is thought to be an adaptive response that provides reproductive assurance under conditions of pollinator limitation. Since pollen limitation is generally known to be frequent among deceptive orchids, strong pollen limitation is probably a driving force in the autonomous self‐pollination mechanism in the nectarless orchid P. minor.     

A Preliminary Study of the Pollination Ecology of Pedicularis (Scrophulariaceae) in Japan

Abstract An introductory study of the pollination ecology of six Japanese species of Pedicularis conducted in 1982 and 1983 indicated a close parallel between characteristics of floral mechanisms in Japan and those previously investigated in North America. Floral color, floral form, total dissolved solids in floral nectar, and polinator behavior on flowers of Japanese species are similar to those of North American species. Blooming phenology of Japanese species also corresponds to the North American sequence of long-tongued, nectar-foraging queen bumblebees (Bombus Latr.) pollinating nectariferous , earlier-blooming species nototribically and short-tongued, pollen-foraging workers pollinating nectarless, rostrate flowers of later-blooming ones sternotribically. Electrofocus analysis of peroxidase systems in two Japanese species indicated considerable intrapopulational heterozygosity. Nectar component analysis of two transboreal species indicated intraspecific differences in kinds of sugars between widely disjunct Japanese and North American populations. A tentative conclusion is that the Japanese and North American Pedicularis floras have evolved in a parallel manner from Himalayan migrants, while their transboreal elements are in process of vicariant diversification.     

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.     

Experimental sympatry suggests geographic isolation as an essential reproductive barrier between two sister species of Pedicularis

Although mechanical isolation mediated by shared pollinators has been considered as a classic model of pollinator-mediated floral isolation in Pedicularis, a superdiverse genus in Hengduan Mountains, southwest China, there has been no empirical study of interspecific pollen flow between closely related species. We examined reproductive barriers at six different stages between Pedicularis cranolopha and Pedicularis tricolor, two sister species. The two sister species were geographically isolated from each other based on our field survey and the records of herbarium specimens. Translocation experiments showed that flowering phenology partly overlapped and bumblebee pollinators did not discriminate between flowers of the two species. Bumblebee interspecific moves could mediate interspecific pollination as traced using fluorescent powder, in which pollen analogs placed on one species were transferred to the stigmas of the other species in experimental plots containing both species. Heterospecific pollen tubes grew in the style as well as conspecific pollen in hand-pollination experiments. Reciprocal hybridization between the two species could produce (partially) viable seeds, suggesting weak post-pollination barriers. Our results showed that geographic isolation was an important barrier of two species, and the total reproductive isolation between two species was incomplete when without geographical isolation. The formation of Big Snow Mountains could introduce an important pre-zygotic reproductive barrier between the two sister species of Pedicularis; such geographical isolation could be responsible for allopatric speciation, giving a clue to understanding the rapid radiation on mountain areas.     

Pollination biology of the endangered orchid Cypripedium japonicum in a fragmented forest of Japan

Pollination biology studies of the endangered orchid Cypripedium japonicum were conducted in its natural habitat using pollinator observation and hand‐pollination experiments. The observed fruit set was as follows: artificial outcross‐pollinated, 100%; artificial self‐pollinated, 100%; pollinator‐excluded, 0%; and emasculated flowers, 0%. These results show that this species, although self‐compatible, is neither autogamous nor agamospermous. The fruit set for open‐pollinated flowers was 14.9%, which suggests that the study population was subject to pollinator limitation. The nectarless flowers of C. japonicum were exclusively visited and pollinated by the queens of two bumblebee species (Bombus ardens and B. diversus diversus). It is probable that the nectarless flowers of C. japonicum attract pollinators through a generalized food deceptive system.     

马先蒿属植物花冠分化与繁殖适应的研究进展

结合已有的研究报道和作者近年来的工作, 对马先蒿属(Pedicularis)植物的花冠多样化成因与繁殖适应特性进行了总结和探讨。通过对该属4种进化花冠型的花器官发生和分化的研究发现, 花部各器官在发生和发育初期基本一致, 后期上唇形态的分化是导致成熟花形态结构产生较大差异的重要阶段。孢粉学研究认为, 花冠类型与花粉萌发孔类型之间具有显著相关性; 萌发沟的演化可能与繁殖适应有一定的关系。分子系统学研究表明, 多样化的花冠类型在不同的谱系内经过若干次的独立进化而表现出了高度的平行演化(p ara l lel ism )。传粉生物学研究证实, 该属植物花冠多样化与其主要传粉者熊蜂属(Bombus)昆虫的传粉行为存在较为密切的关系。具有相同(似)花冠类型的马先蒿可能被同种或不同种的熊蜂以相同的方式访问, 但在花粉落置位置上存在显著差异, 这可能有助于同域分布重叠的物种间在生殖上的机械隔离, 而花冠的分化在一定程度上促进了新的物种形成。     

Pollination niche overlap between a parasitic plant and its host

Niche theory predicts that species which share resources should evolve strategies to minimise competition for those resources, or the less competitive species would be extirpated. Some plant species are constrained to co-occur, for example parasitic plants and their hosts, and may overlap in their pollination niche if they flower at the same time and attract the same pollinators. Using field observations and experiments between 1996 and 2006, we tested a series of hypotheses regarding pollination niche overlap between a specialist parasitic plant Orobanche elatior (Orobanchaceae) and its host Centaurea scabiosa (Asteraceae). These species flower more or less at the same time, with some year-to-year variation. The host is pollinated by a diverse range of insects, which vary in their effectiveness, whilst the parasite is pollinated by a single species of bumblebee, Bombus pascuorum, which is also an effective pollinator of the host plant. The two species therefore have partially overlapping pollination niches. These niches are not finely subdivided by differential pollen placement, or by diurnal segregation of the niches. We therefore found no evidence of character displacement within the pollination niches of these species, possibly because pollinators are not a limiting resource for these plants. Direct observation of pollinator movements, coupled with experimental manipulations of host plant inflorescence density, showed that Bombus pascuorum only rarely moves between inflorescences of the host and the parasite and therefore the presence of one plant is unlikely to be facilitating pollination in the other. This is the first detailed examination of pollination niche overlap in a plant parasite system and we suggest avenues for future research in relation to pollination and other shared interactions between parasitic plants and their hosts.     

Effectiveness of buzz pollination in Pedicularis chamissonis: significance of multiple visits by bumblebees

Pollination success of plants is highly susceptible to the frequency of visits and foraging behavior of pollinators. Pollination of the nectarless flowers of Pedicularis species depends on bumblebee workers collecting pollen by vibrating the anthers (buzz pollination). However, little is known about the efficiency of the pollination system. Foraging behavior, pollen removal from anthers and pollen deposition on stigmas of P. chamissonis were studied to assess the effectiveness of buzz pollination in an alpine snowbed population of northern Japan. Although bumblebees tended to visit most of the flowers open at a given time within inflorescences during a single visit, pollen removal rate at the first visit was about 20%, and buzzing period decreased with increasing number of previous visits, resulting in a decreasing proportion of pollen removed per visit as the number of visits increased. These trends enable plants to provide pollen for more pollinators. The number of pollen grains deposited on stigmas was not saturated during the first visit and increased with additional visits. Irrespective of weak self-compatibility, evidence of interference between self and outcross pollen was lacking for seed production. Therefore, buzz pollination in P. chamissonis acts as a mechanism that improves the chance of cross-pollination upon multiple visits if pollinator visitation is frequent.