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1.  Reproductive isolation and pollination success of rewarding Galearis diantha and non-rewarding Ponerorchis chusua (Orchidaceae) 
Annals of Botany  2010;107(1):39-47.
Background and Aims
Increasing evidence challenges the conventional perception that orchids are the most distinct example of floral diversification due to floral or prezygotic isolation. Regarding the relationship between co-flowering plants, rewarding and non-rewarding orchids in particular, few studies have investigated whether non-rewarding plants affect the pollination success of rewarding plants. Here, floral isolation and mutual effects between the rewarding orchid Galearis diantha and the non-rewarding orchid Ponerorchis chusua were investigated.
Flowering phenological traits were monitored by noting the opening and wilting dates of the chosen individual plants. The pollinator pool and pollinator behaviour were assessed from field observations. Key morphological traits of the flowers and pollinators were measured directly in the field. Pollinator limitation and interspecific compatibility were evaluated by hand-pollination experiments. Fruit set was surveyed in monospecific and heterospecific plots.
Key Results
The species had overlapping peak flowering periods. Pollinators of both species displayed a certain degree of constancy in visiting each species, but they also visited other flowers before landing on the focal orchids. A substantial difference in spur size between the species resulted in the deposition of pollen on different regions of the body of the shared pollinator. Hand-pollination experiments revealed that fruit set was strongly pollinator-limited in both species. No significant difference in fruit set was found between monospecific plots and heterospecific plots.
A combination of mechanical isolation and incomplete ethological isolation eliminates the possibility of pollen transfer between the species. These results do not support either the facilitation or competition hypothesis regarding the effect of nearby rewarding flowers on non-rewarding plants. The absence of a significant effect of non-rewarding P. chusua on rewarding G. diantha can be ascribed to low levels of overlap between the pollinator pools of two species.
PMCID: PMC3002470  PMID: 20961923
Galearis diantha; Ponerorchis chusua; rewarding and non-rewarding; mechanical isolation; ethological isolation; pollinator limitation; fruit set
2.  The pollination of a self-incompatible, food-mimic orchid, Coelogyne fimbriata (Orchidaceae), by female Vespula wasps 
Annals of Botany  2009;104(3):565-571.
Background and Aims
The study of specialized interactions between species is crucial to our understanding of processes in evolutionary ecology due to their profound effect on life cycles and diversification. Obligate pollination by a single wasp species is rare in Orchidaceae except in species with sexually deceptive flowers that are pollinated exclusively by male insects. The object of this study was to document pollination of the food-deceptive flowers of Coelogyne fimbriata, a species pollinated exclusively by female wasps.
Field observations and experiments were conducted in two populations of C. fimbriata. Floral phenology was recorded, and functional floral architecture was measured. Insect visitors to flowers were observed from 2005 to 2007. Bioassay experiments were conducted to check whether the floral odour attracted pollinators. Natural (insect-mediated) rates of pollinarium removal, pollinium deposition on stigmas, and fruit set were recorded. To determine the importance of cross-pollination, the breeding system was assessed via controlled, hand-pollination experiments.
Key Results
Two populations of C. fimbriata with fragrant, nectarless flowers are pollinated by females of the same Vespula species (Vespidae, Hymenoptera). Experiments on wasps show that they crawl towards the source of the odour. The flowering period appears to coincide with an annual peak in Vespula colony expansion when additional workers forage for carbohydrates. Rates of pollinarium removal (0·069–0·918) and pollinium deposition on stigmas (0·025–0·695) are extremely variable. However, fruit set in C. fimbriata is always low (0·014–0·069) and appears to be based on self-incompatibility coupled with intraclonal (geitonogamous) deposition of pollinia.
Coelogyne fimbriata and Steveniella satyrioides are now the only orchid species known to have food-deceptive flowers that are pollinated exclusively by eusocial, worker wasps. In C. fimbriata, floral odour appears to be the major attractant. Sub-populations may go through flowering seasons when pollinators are abundant or infrequent, but fruit set always remains low because the obligate pollinator does not often appear to transfer pollinaria between intercompatible genets.
PMCID: PMC2720650  PMID: 19218578
Coelogyne fimbriata; Vespula wasps; food deception; floral odour; pollinarium removal; pollinium deposition; self-incompatibility
3.  Molecular phylogenetics and morphological reappraisal of the Platanthera clade (Orchidaceae: Orchidinae) prompts expansion of the generic limits of Galearis and Platanthera 
Annals of Botany  2009;104(3):431-445.
Background and Aims
The Platanthera clade dominates the North American orchid flora and is well represented in eastern Asia. It has also generated some classic studies of speciation in Platanthera sections Platanthera and Limnorchis. However, it has proved rich in taxonomic controversy and near-monotypic genera. The clade is reviewed via a new molecular phylogenetic analysis and those results are combined with brief reconsideration of morphology in the group, aiming to rationalize the species into a smaller number of larger monophyletic genera and sections.
Nuclear ribosomal internal transcribed spacer (ITS) sequences were obtained from 86 accessions of 35 named taxa, supplemented from GenBank with five accessions encompassing a further two named taxa.
Key Results
Using Pseudorchis as outgroup, and scoring indels, the data matrix generated 30 most-parsimonious trees that differed in the placement of two major groups plus two closely related species. Several other internal nodes also attracted only indifferent statistical support. Nonetheless, by combining implicit assessment of morphological divergence with explicit assessment of molecular divergence (when available), nine former genera can be rationalized into four revised genera by sinking the monotypic Amerorchis, together with Aceratorchis and Chondradenia (neither yet sequenced), into Galearis, and by amalgamating Piperia, Diphylax and the monotypic Tsaiorchis into the former Platanthera section Platanthera. After further species sampling, this section will require sub-division into at least three sections. The present nomenclatural adjustments prompt five new combinations.
Resolution of major groups should facilitate future species-level research on the Platanthera clade. Recent evidence suggests that ITS sequence divergence characterizes most species other than the P. bifolia group. The floral differences that distinguished Piperia, Diphylax and Tsaiorchis from Platanthera, and Aceratorchis and Chondradenia from Galearis, reflect various forms of heterochrony (notably paedomorphosis); this affected both the perianth and the gynostemium, and may have proved adaptive in montane habitats. Floral reduction was combined with lateral expansion of the root tubers in Piperia and Diphylax (including Tsaiorchis), whereas root tubers were minimized in the putative (but currently poorly supported) Neolindleya–Galearis clade. Allopolyploidy and/or autogamy strongly influenced speciation in Platanthera section Limnorchis and perhaps also Neolindleya. Reproductive biology remains an important driver of evolution in the clade, though plant–pollinator specificity and distinctness of the species boundaries have often been exaggerated.
PMCID: PMC2720662  PMID: 19383726
Aceratorchis; Amerorchis; Chondradenia; Diphylax; Galearis; generic delimitation; internal transcribed spacer; Neolindleya; orchid; Piperia; phylogeny; Platanthera; Pseudorchis; speciation; Tsaiorchis
4.  Reproductive success of non-rewarding Cypripedium japonicum benefits from low spatial dispersion pattern and asynchronous flowering 
Annals of Botany  2009;103(8):1227-1237.
Background and Aims
Outcrossing animal-pollinated plants, particularly non-rewarding species, often experience pollinator limitation to reproduction. Pollinator visitation is affected by various factors, and it is hypothesized that reproduction in non-rewarding plants would benefit from low spatial flower abundance and asynchronous flowering. In order to test this hypothesis, the influence of spatial pattern and flowering phenology on male and female reproductive success (RS) was investigated in a non-rewarding orchid, Cypripedium japonicum, in central China over two flowering seasons.
The probabilities of intrafloral self-pollination and geitonogamy caused by pollinator behaviours were estimated from field observations. Pollinator limitation was evaluated by hand-pollination experiments. RS was surveyed in different spatial flower dispersal patterns and local flower densities. The effects of flowering phenological traits on RS were assessed by univariate and multivariate regression analyses.
Key Results
Hand-pollination experiments revealed that fruit production was strongly pollen limited throughout the entire reproductive season – over two seasons, 74·3 % of individuals set fruit following hand pollination, but only 5·2–7·7 % did so under natural conditions. Intrafloral self-pollination and geitonogamy within the potential clones might be rare. Both male and female fitness were substantially lower in clustered plants than in those growing singly. An increase in local conspecific flower density significantly and negatively influenced male RS, but had no effect on female RS. Phenotypic selection analysis indicated that individuals flowering earlier have the greatest probability of RS. Over 85 % of sampled flowering individuals had a flowering synchrony value >0·7; however, highly synchronous flowering was not advantageous for RS, as indicated by the negative directional selection differentials and gradients, and by the positive quadratic selection gradients.
These results support the hypothesis that, as a consequence of density-dependent selection, low spatio-temporal flower abundance is advantageous for attracting pollinators and for reproduction in natural populations of non-rewarding C. japonicum.
PMCID: PMC2685325  PMID: 19318381
Cypripedium japonicum; pollen limitation; spatial dispersal pattern; flowering synchrony; reproductive success; selection differential; selection gradient; deceptive flower
5.  Pollination of Schisandra henryi (Schisandraceae) by Female, Pollen-eating Megommata Species (Cecidomyiidae, Diptera) in South-central China 
Annals of Botany  2007;99(3):451-460.
Background and Aims
The mutualistic interaction between insects and flowers is considered to be a major factor in the early evolution of flowering plants. The Schisandraceae were, until now, the only family in the ANITA group lacking information on pollination biology in natural ecosystems. Thus, the objective of this research was to document the pollination biology and breeding system of Schisandra henryi.
Field observations were conducted in three populations of S. henryi and the floral phenology, floral characters and insect activities were recorded. Floral fragrances were sampled in the field and analysed using TCT-GC-MS. Floral thermogenesis was measured with a TR-71U Thermo Recorder. Pollen loads and location of pollen grains on insect bodies (including the gut) were checked with a scanning electron microscope and under a light microscope.
Key Results
Schisandra henryi is strictly dioecious. Male flowers are similar to female flowers in colour, shape, and size, but more abundant than female flowers. The distance between tepals and the androecium or gynoecium is narrow. Neither male nor female flowers are fragrant or thermogenic. Schisandra henryi is pollinated only by adult female Megommata sp. (Cecidomyiidae, Diptera) that eat the pollen grains as extra nutrition for ovary maturation and ovipositing. Both male and female flowers attract the pollinators using similar visual cues and thus the female flowers use deceit as they offer no food.
Schisandra henryi exhibits a specialized pollination system, which differs from the generalized pollination system documented in other ANITA members. Pollen is the sole food resource for Megommata sp. and the female flowers of S. henryi attract pollinators by deceit. This is the first report of predacious gall midges utilizing pollen grains as a food source. The lack of floral thermogenesis and floral odours further enforces the visual cues by reducing attractants for other potential pollinators.
PMCID: PMC2802962  PMID: 17237212
Schisandra henryi; Schisandraceae; ANITA group; Megommata sp.; Cecidomyiidae; specialized pollination system; pollination by deceit

Results 1-5 (5)