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。     

Pollination Ecology of Pedicularis punctata Decne. (Scrophulariaceae) in the Kashmir Himalaya

Abstract The pollination ecology of Pedicularis punctata was studied in the Pir Panjal Range of the Kashmir Himalaya in the summer of 1989. Its nectarless, rostrate, long-tubed flower was found to be pollinated exclusively by Bombus foragers vibrating pollen while the stigma contacted pollen in the pollinator's cervical crevice. Workers of Bombus tunicatus and B. flavothoracicus comprised 95% of its pollinators. Pollen-foraging fidelity of its pollinators was greatest where diversity of Bombus -pollinated plant species in three plant communities was least. Foragers on other plants carried virtually no Pedicularis pollen. P. punctata is a mid-season blooming species similar in its pollination syndrome to comparable species in other geographic regions. The enigmatic function of its long, nectarless corolla tube, even more exaggerated in other Asiatic species, requires further investigation.     

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.     

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。     

Intrinsic and extrinsic factors acting on the reproductive process in alpine‐snowbed plants: roles of phenology,biological interaction,and breeding system

Pollinator activity and competition for pollinators lead to quantitative and qualitative pollen limitations on seed production and affect the reproductive success of plant species, depending on their breeding system (e.g., self‐compatibility and heterospecific compatibility) and genetic load (e.g., inbreeding depression and hybrid inviability). In alpine ecosystems, snowmelt regimes determine the distribution and phenology of plant communities. Plant species growing widely along a snowmelt gradient often grow with different species among local populations. Their pollinators also vary in their abundance, activity, and behavior during the season. These variations may modify plant–pollinator and plant–plant interactions. We integrated a series of our studies on the alpine dwarf shrub, Phyllodoce aleutica (Ericaceae), to elucidate the full set of intrinsic (species‐specific breeding system) and extrinsic factors (snow condition, pollinator activity, and interspecific competition) acting on their reproductive process. Seasonality of pollinator activity led to quantitative pollen limitation in the early‐blooming populations, whereas in the late‐blooming populations, high pollinator activity ensured pollination service, but interspecific competition for pollinators led to qualitative and quantitative pollen limitation in less competitive species. However, negative effects of illegitimate pollen receipt on seed‐set success might be reduced when cryptic incompatibility systems (i.e., outcross pollen grains took priority over self‐ and heterospecific pollen grains) could effectively prevent ovule and seed discounting. Our studies highlight the importance of species‐specific responses of plant reproduction to changing pollinator availability along environmental gradients to understand the general features of pollination networks in alpine ecosystems.     

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。     

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。     

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.     

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.     

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.     

Comparative Studies on Pollination Biology of Mosla hangchouensis and M.chinensis (Labiatae)

Mosla hangchouensis Matsuda and M. chinensis Maxim. are sibling species. The former is endemic to the coastal areas of Zhejiang Province, and the latter occupies southern China. Their morphological differences were associated with their different breeding systems indicated by pollen-ovule ratio (P/O). M. hangchouensis was predominantly outcrossing with P/O ranging from 756 to 6163 due to the variation among populations. Floral characters also showed that M. hangchouensis is an outcrosser: corolla tube 5～10 mm long, 3~5 mm wide, bright red: style 6～15 mm long; stigma 1.5～2.0 mm horizontally away from anthers. On the contrary, M. chinensis was predominantly a selfer with a low P/O ratio (P/O= 110). Its floral parameters contrasted sharply with M. hangchouensis: corolla tube 3.0 mm long, 1.0 ～ 1.5 mm wide, pale colored; style 2.5 mm long. stigma close to or touching anthers. The pollinators of M. hangchouensis most frequently seen are: Bombus trifascitus Smith., Scolia spp., Apis cerana Fabricius, Hylaeus sp. and Lasioglossum spp. These pollinators began to visit flowers at about 8:00 am, when flower buds were ready to open. When insects entered corolla tube for honey and (or) pollen, the stigmata touched the insects body hairs to which pollen grains adhered, and pollen grains were transferred to the stigmata. Meanwhile the hairs collected pollen from anthers under the upper lips of corolla as the insects thrusted their bodies forward. Bumble bees and honey bees were considered more efficient pollinators because they were hair-rich and their body size fitted corolla tube fairly well. Due to the'short flight distance of pollinators between two visits (average flight distances of honey bees and solitary bees were 0.52 m and 0.32 m respectively), pollen dispersal was probably restricted. Pollen vectors were important for the reproductive success of M. hangchouensis because 84.3 % of its seed-set depended on the pollinators' visitation. Although insects did pay visits to M. chinensis occasionally, such visitation was insignificant in seed-set due to cleistogamy. Discussions are made on the evolutionary significance of breeding system divergence between M. hangchouensis and M. chinensis, and the contribution of studies on pollination biology to conservation biology. Further studies are suggested for more thorough understanding of pollination biology of M. hangchouensis.     

Change of floral orientation affects pollinator diversity and their relative importance in an alpine plant with generalized pollination system,Geranium refractum (Geraniaceae)

Floral orientation may affect pollinator attraction and pollination effectiveness, and its influences may differ among pollinator species. We, therefore, hypothesized that, for plant species with a generalized pollination system, changes in floral orientation would affect the composition of pollinators and their relative contribution to pollination. Geranium refractum, an alpine plant with downward floral orientation was used in this study. We created upward-facing flowers by altering the flower angle. We compared the pollinator diversity, pollination effectiveness, and pollinator importance, as well as female reproductive success between flowers with downward- and upward-facing orientation. Results indicated that the upward-facing flowers were visited by a wider spectrum of pollinators (classified into functional groups), with higher pollinator diversity than natural flowers. Moreover, due to influences on visitation number and pollen removal, the pollinator importance exhibited by the main pollinator groups differed between flower types. Compared with natural flowers, the pollination contribution of principal pollinators (i.e., bumblebees) decreased in upward-facing flowers and other infrequent pollinators, such as solitary bees and muscoid flies, removed more pollen. Consequently, stigmatic pollen loads were lower in upward- than in downward-facing flowers. These findings reveal that floral orientation may affect the level of generalization of a pollination system and the relative importance of diverse pollinators. In this species, the natural downward-facing floral orientation may increase pollen transfer by effective pollinators and reduce interference by inferior pollinators.     

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.     

Character displacement of male nuptial colour in threespine sticklebacks (Gasterosteus aculeatus)

To study the isolation mechanism of two commonly intermingled louseworts, Pedicularis rhinanthoides and Pedicularis longiflora , pollination biology in three mixed populations with the two species was investigated during a 3-year project. The results indicated that higher flowering density could help to enhance pollinator activity, and thus increase reproductive output. Bumblebees are the exclusive pollinator for the two louseworts and are essential for their reproductive success. Reproductive isolation between the two species is achieved by a combination of pre- and postzygotic isolation mechanisms. Although both species are pollinated by bumblebees, the present study indicates they successfully avoid interspecific pollen transfer due to floral isolation. Mechanical isolation is achieved by the stigma in the two species picking up pollen from different parts of the pollinator's body, whereas ethological isolation occurs due to flower constancy. Additionally, strong postzygotic isolation was demonstrated by non seed set after artificial cross-pollination even with successful pollen tube growth. We describe the hitherto unreported role of variation in the tightness and direction of the twist of the corolla beak in maintaining mechanical isolation between Pedicularis species. Although floral isolation in Pedicularis is incomplete, it is considered to be an important mechanism in maintaining species boundaries in the genus.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 37–48.     

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.     

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.     

Is the pollination biology of Bathysa and Schizocalyx consistent with their segregation? A first approach for two sympatric species in southeastern Brazil

Tribe Condamineeae appears to be well supported in recent phylogenetic studies. However, the species of Bathysa were divided into two clades, leading to restoration of Schizocalyx. We studied the reproductive biology of one species from each clade, which occur sympatrically in the montane Brazilian Atlantic forest. Flowering overlap was short (from December to March in B. australis and from February to June in S. cuspidatus). The flowers of both species are protogynous and homostylous and last for about 3 days. The unit of pollination in B. australis is the inflorescence. Its flowers have a greenish hypocrateriform corolla (tube about 5 mm long) and were mainly pollinated by bees and wasps in search of nectar. Schizocalyx cuspidatus has white flowers with an infundibuliform corolla (tube about 8 mm long), and its main pollinators were stingless bees in search of pollen. The pollination systems of the two species did not correspond to their pollination syndromes. Morphological differences between Bathysa and Schizocalyx were reflected in their pollination systems, with greater phenotypic specialization in S. cuspidatus, the flowers of which offer pollen as the main resource, an unusual feature within Rubiaceae. Schizocalyx cuspidatus showed higher reproductive capacity by having more inflorescences per plant, more ovules per flower, and twice the proportion of flowering individuals. However, the reproductive efficiency (fruit set, seed/ovule ratio) did not differ between the species, despite the higher frequency of visits by pollinators to S. cuspidatus. Self-compatibility in B. australis and self-incompatibility in S. cuspidatus seem to explain these results.     

Floral ecology of Oreocharis pumila (Gesneriaceae): a novel case of sigmoid corolla

Attraction of pollinators and successful pollen transfer represent the primary targets of selection during flower evolution, leading to repeated evolutionary shifts between pollinators and consequently to the diversification of floral forms. However, most studies in floral evolution focus on the characteristics of flowers with straight corolla tube. Here, we report on an unusual form of sigmoid corolla combined with protandry and herkogamy in a Chinese species of Gesneriaceae, Oreocharis pumila (formerly Opithandra pumila). Contrary to species with sigmoid corollas studied previously, the base of the corolla tube of this species is inclined at an oblique angle downwards before the tube bends forward, and the stigma and anthers are included in the upper part of the corolla tube. The plants were found to be self‐compatible but incapable of autonomous selfing. Successful pollination was found to depend fully on the presence of insect pollinators (Nomia sp.) and pollen grains are the greatest reward for the visitors. Different from the other sigmoid flowers, the sigmoid corolla of O. pumila was not found to favor insect pollinators with long flexible proboscises. A mechanical fit between floral morphology and pollinator was found, in which only small insect visitors with specialized visiting behavior are legitimate pollinators. The protandry combined with herkogamy in the sigmoid corolla tube strongly ensures pollination efficiencies. Oreocharis pumila is the only species with sigmoid corolla in the genus Oreocharis. We hypothesize that such a corolla has arisen through selection due to inadequate pollination in early spring in the mountainous habitat that O. pumila occupies.     

Eight microsatellite markers for sympatric alpine shrubs,Phyllodoce aleutica and P. caerulea (Ericaceae)

Phyllodoce aleutica and Phyllodoce caerulea are sympatric alpine‐snowbed plants in northern Japan. They compete for pollinators (bumblebees) each other and the competitive situation varies depending on snow conditions. We isolated and characterized eight microsatellite loci in these species. Additionally, one of 13 primers developed for Rhododendron metternichii was available in these species. The expected heterozygosity of these nine markers ranged from 0.06 to 0.93 in P. aleutica and from 0.09 to 0.96 in P. caerulea. These markers may be useful to reveal the mating system evolution, patterns of pollen flow and the process of natural hybridization in these Phyllodoce species.     

Resource limitation and pollen source (self and outcross) affecting seed production in two louseworts, Pedicularis siphonantha and P. longiflora (Orobanchaceae)

Two animal-pollinated hermaphrodite plants, Pedicularis siphonantha and P. longiflora , have been used to investigate factors limiting seed production in natural populations. To evaluate the potential seed abortion due to resources limitation, seed development has been observed and seed count conducted twice. Seed production per capsule has been compared when flowers have been removed and in a control group. Open pollination has been investigated and pollen supplementation undertaken to estimate the possibility of pollen limitation. Results show that seed abortion is frequent. Stigmatic pollen load is significantly higher than ovule number per ovary under open pollination for both species. Additional self and outcross pollen did not affect seed production. Flower removal significantly increases seed production per capsule, which indicates that seed production of the studied species is limited by available resources. To detect differences in seed production between flowers pollinated by self and outcross pollen, hand pollination of bagged flowers has also been conducted in natural populations of the two Pedicularis species. Compared with open pollination, hand-pollinating self-pollen decreases, while outcross pollen increases seed production per capsule. Such results suggest that inbreeding depression in the two self-compatible species may also result in partial seed abortion under open pollination if mixed pollen is deposited on the stigma. Our results also suggest that pollen interference plays an important role in low female fertility in the two Pedicularis species.  © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society , 2005, 147 , 83–89.