Deceptive pollination in two subspecies of Disa spathulata (Orchidaceae) differing in morphology and floral fragrance

The non-rewarding flowers of Disa spathulata (L.f) Sw. have a highly elongated scent-producing lip that varies in size and form between the two subspecies of this orchid. We investigated whether this unusual morphology is associated with the evolution of a specialized scent-based pollination system. Field observations carried out in South Africa showed that flowers of D. spathulata are pollinated solely by bees belonging to the genus Tetraloniella (Anthophoridae). Flowers of D. spathulata subsp. spathulata were visited by Tetraloniella brevikeraia, while flowers of D. spathulata subsp. tripartita (Lindl.). H. P. Linder were visited by Tetraloniella junodi. The floral fragrance of D. spathulata is emitted by the lip blade and differs markedly between the two subspecies (only 24 [42.1] of the 57 compounds identified were shared). Fragrance of D. spathulata subsp spathulata is dominated by the fatty acid derivatives decyl actetate, octanol, and decanol, while that of D. spathulata subsp. tripartita is dominated by the terpenoids (E) - ocimene, caryophyllene, and (E) nerolidol. Both male and female Tetraloniella bees were strongly attracted to cut flowers of D. spathulata subsp spathulata, even at sites where the orchid does not naturally occur. Bees visit the orchids repeatedly despite the lack of rewards in their flowers. Sexual deception in D. spathulata can be excluded by the attraction of both male and female bees, and yet the manner in which bees are attracted seems too intense and species-specific to be characterized as food-deception. This implies the existence in D. spathulata of a system of scent-based deception of insects that has not been described previously in plants.     

Orchid Mimics Honey Bee Alarm Pheromone in Order to Attract Hornets for Pollination

Approximately one-third of the world's estimated 30,000 orchid species are deceptive and do not reward their pollinators with nectar or pollen [1]. Most of these deceptive orchids imitate the scent of rewarding flowers or potential mates [2] and [3]. In this study, we investigated the floral scent involved in pollinator attraction to the rewardless orchid Dendrobium sinense, a species endemic to the Chinese island Hainan that is pollinated by the hornet Vespa bicolor. Via chemical analyses and electrophysiological methods, we demonstrate that the flowers of D. sinense produce (Z)-11-eicosen-1-ol and that the pollinator can smell this compound. This is a major compound in the alarm pheromones of both Asian (Apis cerana) and European (Apis mellifera) honey bees [4] and [5] and is also exploited by the European beewolf (Philanthus triangulum) to locate its prey [6]. This is the first time that (Z)-11-eicosen-1-ol has been identified as a floral volatile. In behavioral experiments, we demonstrate that the floral scent of D. sinense and synthetic (Z)-11-eicosen-1-ol are both attractive to hornets. Because hornets frequently capture honey bees to feed to their larvae, we suggest that the flowers of D. sinense mimic the alarm pheromone of honey bees in order to attract prey-hunting hornets for pollination.     

Breeding system and pollination by mimicry of the orchid Tolumnia guibertiana in Western Cuba

The mimicry of malpighiaceous oil‐flowers appears to be a recurrent pollination strategy among many orchids of the subtribe Oncidiinae. These two plant groups are mainly pollinated by oil‐gathering bees, which also specialize in pollen collection by buzzing. In the present study, the floral ecology of the rewardless orchid Tolumnia guibertiana (Oncidiinae) was studied for the first time. The orchid was self‐incompatible and completely dependent on oil‐gathering female bees (Centris poecila) for fruit production. This bee species was also the pollinator of two other yellow‐flowered plants in the area: the pollen and oil producing Stigmaphyllon diversifolium (Malpighiaceae) and the polliniferous and buzzing‐pollinated Ouratea agrophylla (Ochnaceae). To evaluate whether this system is a case of mimetism, we observed pollinator visits to flowers of the three plant species and compared the floral morphometrics of these flowers. The behavior, preferences and movement patterns of Centris bees among these plants, as well as the morphological data, suggest that, as previously thought, flowers of T. guibertiana mimic the Malpighiaceae S. diversifolium. However, orchid pollination in one of the studied populations appears to depend also on the presence of O. agrophylla. Moreover, at the two studied populations, male and female pollination successes of T. guibertiana were not affected by its own floral display, and did not differ between populations. The results are discussed in relation to the behavior and preferences of Centris bees, as well as the differential presence and influence of each of the two floral models.     

Scaling of nectar foraging in orchid bees

Morphology influences the rate at which foraging bees visit nectar flowers, the quantity of nectar they must consume to fuel their activities, and, consequently, the profitability of flower species. Because feeding time is a major determinant of visitation rate, I used a biomechanical model to examine how energy intake rate (E) varies with sucrose concentration, body mass (M), and proboscis length in orchid bees (Apidae: Euglossini). Under geometric scaling, the optimal sugar concentration (Smax) should be largely independent of body size, and E proportional to M1.0. In a comparative study of 30 orchid bee species ranging from 50 to 800 mg, Smax fell between 35% and 40% w/w, but E proportional to M0.54, significantly less than model predictions. Proboscis length and radius scale geometrically with body mass, but proboscis length exhibits substantial size-independent variation, particularly in small bees. One cost of a long proboscis is a reduction in both E and Smax in accordance with the scaling model. This finding highlights a difference between the lapping mechanism used by bumblebees and the suction mechanism used by orchid bees. A field study confirms that orchid bees harvest nectars with between 34% and 42% sucrose, independent of body size.     

The floral biology ofThelymitra epipactoides (Orchidaceae), and the implications of pollination by deceit on the survival of this rare orchid

Thelymitra epipactoides has a highly variable visual display achieved through polychromatic flowers and variable inflorescence size, bearing between 7 and 31 flowers, which attract foraging polylectic bees. Only bees of the genusNomia were observed carrying pollinia and successfully pollinating the orchid. The genusNomia contains polylectic, pollen gathering species that store pollen in both the crop and scopa on the hind legs. The absence of a reward for the bees indicates the orchid is relying on deception to attract visitors. The relationship of deception to mimicry is discussed. Once on the flower, tactile, visual and possibly olfactory stimuli direct bees to the false anther formed by the voluminous column wings, where morphological adaptations of the flower ensure that the pollinarium is deposited on the gaster of the bee to effect pollination. — The lack of seed set observed on the Victorian coast appears to be due to the absence of pollinators from the heath and grassland communities in which the orchid grows. This may well be a consequence of the reduced number of plants flowering in the community (a result of the elimination of fire at these sites), thus not maintaining a floral community attractive to potential pollinators.     

Long Tongues and Loose Niches: Evolution of Euglossine Bees and Their Nectar Flowers1

I examined relationships between tongue length of orchid bees (Apidae: Euglossini) and nectar spur length of their flowers in the genera Calathea, Costus, and Dimerocostus using phylogenetically independent contrasts. Long‐tubed flowers have specialized on one or several species of long‐tongued euglossine bees, but long‐tongued bees have not specialized on long‐tubed flowers. Whereas long tongues may have evolved to provide access to a wider variety of nectar resources, long nectar spurs may be a mechanism for flowers to conserve nectar resources while remaining attractive to traplining bee visitors.     

Floral and pollination biology of the critically endangered insular orchid Calanthe amamiana: Implications for in situ conservation

Calanthe amamiana is a terrestrial orchid that thrives on the shady forest floors of broad-leaved forests on Amami Island, central Ryukyus, Japan. Here, I report on the floral and pollination biology of this critically endangered orchid based on a 7-year study conducted in the species' natural habitats. As the nectarless flowers are probably self-compatible but are unable to autonomously self-pollinate, they need to attract pollen vectors by deceit for pollination. To advertise themselves, the flowering inflorescences, which comprise a few to dozens of flowers, use whitish floral colors that are comparatively conspicuous against the shaded background. The exclusive pollinator was the long-horned bee Eucera okinawae, which nests in soils of the forest floor, although bee abundance varied considerably among study years. Natural fruit-set ratios were generally low but showed interannual variation. The annual fruit-set ratios were positively correlated with annual bee abundance, thereby suggesting that under natural conditions, the orchid is pollinator-limited. Given that C. amamiana is dependent exclusively on E. okinawae for pollination and is also probably pollinator-limited, conservation plans for this orchid should take into consideration the welfare of long-horned bees. In particular, as nectariferous flowers were unavailable within broad-leaved forests, to satisfy the foraging requirements of long-horned bees, conservation managers should be cognizant of conservation values of flowering plants distributed in sun-lit sites near orchid habitats, and manage those in an appropriate manner.     

Chemical study of the flowers of the orchid Oncidium baueri Lindley and their visiting bees Trigona spinipes Fabricius

Oncidium baueri Lindley is a South American orchid characterized by the production of numerous yellow-brown flowers, arranged in inflorescences that reach up to four meters long. Herein, the chemical study of the flowers led to the identification of compounds present in the floral oil, such as long chain acids and methyl esters, including the first report of the occurrence of rare compound byrsonic acid in orchids in the free form. In addition to this, steroids and the flavonoid glycosides acacetin-7-O-rutinoside, pectolinarin, oncibauerins A and B were identified in large amounts. Finally, the flower-insect visit by Trigona spinipes Fabricius bees was also studied. Video analyses of the process revealed that the bees spend a long time collecting material from the flower labellum callus. The chemical analyses of bees and flowers showed the presence of palmitic acid and stearic acid in both samples, leading to suspicious about the attraction of bees by flowers oils as floral rewards.     

Solitary invasive orchid bee outperforms co-occurring native bees to promote fruit set of an invasive Solanum

Our understanding of the effects of introduced invasive pollinators on plants has been exclusively drawn from studies on introduced social bees. One might expect, however, that the impacts of introduced solitary bees, with much lower population densities and fewer foragers, would be small. Yet little is known about the potential effects of naturalized solitary bees on the environment. We took advantage of the recent naturalization of an orchid bee, Euglossa viridissima, in southern Florida to study the effects of this solitary bee on reproduction of Solanum torvum, an invasive shrub. Flowers of S. torvum require specialized buzz pollination. Through timed floral visitor watches and two pollination treatments (control and pollen supplementation) at three forest edge and three open area sites, we found that the fruit set of S. torvum was pollen limited at the open sites where the native bees dominate, but was not pollen limited at the forest sites where the invasive orchid bees dominate. The orchid bee’s pollination efficiency was nearly double that of the native halictid bees, and was also slightly higher than that of the native carpenter bee. Experiments using small and large mesh cages (to deny or allow E. viridissima access, respectively) at one forest site indicated that when the orchid bee was excluded, the flowers set one-quarter as many fruit as when the bee was allowed access. The orchid bee was the most important pollinator of the weed at the forest sites, which could pose additional challenges to the management of this weed in the fragmented, endangered tropical hardwood forests in the region. This specialized invasive mutualism may promote populations of both the orchid bee and this noxious weed. Invasive solitary bees, particularly species that are specialized pollinators, appear to have more importance than has previously been recognized. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Observations of putative pollinators of Hemipilia flabellata Bur.et Franch.(Orchidaceae) in north-west Yunnan Province, China

Interactions between Hemipilia flabellata and anthophilous insects were studied in northwestern Yunnan, China during June-July of 1996 and 1997. Twenty-seven species of insects were seen visiting the flowers of this species, although only male and female individuals of the bee Anthophora mangkamensis Wu were observed carrying the pollinaria. The frequency of visits by A.mangkamensis to this orchid was rather low. Pollinating bees normally sampled only the lowermost flowers in an inflorescence, staying for 1–3 seconds. This species is also characterized by low pollination, low fruit set (1–22%) and a very striking decrease in fruit production from bottom to top of the inflorescence. All of these indicate that the orchid may rely on deception to attract visitors. Ajuga forrestii Diels (Labiatae) appears to be the main or exclusive subsidiary nectar source for A.mangkamensis during the flowering period of H.flabellata . It appears that H.flabellata utilizes a food deceit pollination strategy for pollination. The orchid benefits from the great variation or flowers in colour and shape. Phenological, functional-morphometric and distribution data indicate that A.mangkamensis is an optimal pollinator of H.flabellala and thus the anthecological adaptation of the orchid to the pollen vector may be unique.     

Colour similarity to rewarding model plants affects pollination in a food deceptive orchid, Orchis boryi

We studied the pollination of Orchis boryi at five different locations on the Greek mainland. Orchis boryi is food deceptive and obligatorily insect pollinated. Primary pollinators were Apis mellifera and Bombus spp., which foraged on rewarding plant species nearby and visited O. boryi in between. To analyse floral colour similarity among rewarding plants and O. boryi as perceived by bees, a model of bee colour vision was employed. For each food plant an index was calculated that described the probability of a bee foraging on it to subsequently choose an orchid flower. This choice probability correlated to colour distance according to the model of bee colour vision, indicating that bees chose the deceptive orchid more frequently if they foraged on more similarly coloured species. At different sites different plant species served as models. Bees foraging on food plants from which a high choice rate to the orchid was observed visited the orchid less often after approaching it than other bees, which is likely to reflect avoidance learning. In general, the pollination syndrome appears to be a generalized form of Batesian mimicry, in which similarity to rewarding plants determines reproductive success. As expected by negative density-dependent selection, individual fruit set and pollinia export rate correlated negatively with orchid density, but were unaffected by food plant density, orchid frequency, individual variation of labellum colour, labellum size, or mouth width of the flowers.     

Does bee or wasp mimicry by orchid flowers also deter herbivores?

General visual bee mimicry and specific chemical mimicry by flowers to solitary female bees or wasps are well known in several orchid genera, for example, the Mediterranean genus Ophrys, the Australian genera Cryptostylis and Chiloglottis, and the South-African Disa. This mimicry has been shown to attract solitary male bees or wasps, which are their species-specific pollinators. The visual and chemical signals are considered to be a type of deceptive pollination mechanism based on mimicry for the exploitation of perceptual biases of animals. We propose that in addition to this unique pollination mechanism, these plants exhibit another, rarely mentioned and practically forgotten, non-exclusive function of bee or wasp mimicry (Batesian mimicry). This mimicry may deter large mammalian herbivores, and possibly also insects from the plants and especially from their flowers by a type of visual and olfactory deceptive aposematism. While visiting the flowers, bees and wasps may add a Müllerian effect to this defense. We extend this hypothesis to many other rewarding flowers that are bee or wasp pollinated and propose that abundance of pollinating bees or wasps may deter herbivorous mammals and insects from the plants during their peak flowering season.     

Specialized pollination by carpenter bees in Calanthe striata (Orchidaceae), with a review of carpenter bee pollination in orchids

Calanthe striata has nectarless flowers that are self‐compatible, but pollinator dependent. Field observations showed that the flowers were pollinated exclusively by the carpenter bee Xylocopa appendiculata circumvolans, although the bees occasionally wasted pollen by delivering to the stigmatic surface pollinaria that retained their anther caps. Fruit set ratios at the population level varied spatiotemporally, but were generally low (8.3–17.3%). Calanthe striata blooms in spring when post‐overwintering carpenter bees have not yet started foraging for brood production. It can therefore exploit an abundance of opportunistic/naïve foragers. This timing may also increase the possibility of pollinator visits, because no rewarding co‐flowering plants are available in the orchid habitats. A literature review of Orchidaceae pollinated by carpenter bees revealed that at least 14 species of Orchidoideae and Epidendroideae have evolved flowers specialized for carpenter bee pollination. They typically have shallow pink/magenta flowers with a foothold for pollinators; pollinaria are attached to the head, ventral thorax or base of the middle legs of carpenter bees when they insert their heads and/or proboscises into flowers; pollination success is generally low, a probable consequence of the deceptive pollination systems. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013 , 171 , 730–743.     

The pollination mechanism in Trigonidium obtusum Lindl (Orchidaceae: Maxillariinae): sexual mimicry and trap-flowers

The pollination process in Trigonidium obtusum Lindl. (Epidendroideae: Maxillariinae) is documented. The flowers are pollinated by sexually excited drones of Plebeia droryana (Meliponinae). When attempting to copulate either with sepals or petals, these bees slip on the waxy perianth surface and become trapped in the funnel-like flower tube. Bees trying to escape from the flowers may instead access the space between the column and lip, fixing the pollinarium on their scutellum. Pollinarium-bearing bees may pollinate the flowers when repeating the above-mentioned steps, leaving pollinia on the concave stigmatic surface, thus effecting pollination. Recently removed pollinaria are too broad to enter the stigma but they begin to dehydrate and within 40 min of removal are small enough to fit the stigmatic cavity. This mechanism prevents insect-mediated self-pollination and promotes cross-pollination. Preliminary evidence based on experiments with cultivated plants suggests that they are self-compatible but that fruit set is pollinator-dependent. The data obtained are discussed in a phylogenetic context. It is suggested that the pseudocopulatory syndrome in Trigonidium could have evolved from rewardless (food advertising) ancestors. Pseudocopulation in the context of the long flowering period of this orchid species (about 7 months) is understandable since the eusocial Plebeia bees produce fertile individuals several times a year.     

Mixed bumblebee and blowfly pollination of Cypripedium flavum (Orchidaceae) in Sichuan,China

Most Cypripedium species are specialized orchids pollinated by, in a broad sense, bees or flies. Here we present the first evidence that a slipper orchid, Cypripedium flavum, is pollinated by both bees and flies, i.e., bumblebees and blowflies. Artificial pollination experiments demonstrated that the flowers of C. flavum are self-compatible, but need pollen vectors for successful reproduction. Field observations detected 25 insects visiting the flowers, and 14 of these insects entered into the labellum of the flowers, but only female bumblebees, Bombus hypnorum, B. remotus, and the blowfly Calliphora vomitoria exited of the labellum with pollen smears of C. flavum. The floral functional morphology of C. flavum appears to be more suited to bumblebees than to blowflies. The bumblebees are more efficient pollinators of the orchid, but blowflies are more frequent visitors, so they pollinated more flowers despite being less efficient.     

Notes on the pollination biology of <Emphasis Type="Italic">Notylia nemorosa</Emphasis> (Orchidaceae): do pollinators necessarily promote cross pollination?

The pollination biology of Notylia nemorosa was elucidated from field and ex situ observations. Field observations were carried out in Minas Gerais, southeastern Brazil, where this orchid is pollinated by males of Eulaema nigrita(Euglossini). Plants cultivated in Campinas (S?o Paulo State, southeastern Brazil) were eventually pollinated by males of Eulaema nigrita and Euglossa melanothricha(Euglossini). In both cases, Euglossini males collect aromatic compounds produced on the surface of the lip, fix the pollinaria on the dorsal surface of the labrum and perform pollination. This species is protandrous. Recently opened flowers present their stigmatic surfaces blocked and thus flowers act only as pollen donors. After 2-3 days the viscidium dries out and pollinaria cannot be removed anymore. Then, a narrow slit opens in the stigmatic cavity, allowing pollen deposition. Experiments performed with cultivated plants suggest that this orchid species is strongly, though not completely self-incompatible. Pollination experiments showed that bees tend to stay several minutes in each inflorescence. This behavior may promote some degree of geitonogamous pollination because flowers in male and female phases coexist in the same inflorescence. The combination of self-incompatibility with this specific pollinator behavior may explain the rarity of fruits in several neotropical reward-offering Orchidaceae.     

Environmental determinants of genetic diversity in Caragana microphylla (Fabaceae) in northern China

Non‐rewarding orchids rely on various ruses to attract their pollinators. One of the most common is for them to resemble flowers sought by insects as food sources. This can range from generalized food deception to the mimicry of specific sympatric food plants. We investigated the basis of pollinator deception in the European food‐deceptive orchid Traunsteinera globosa, which has unusually compact flowerheads resembling those of sympatric rewarding species of Knautia and Scabiosa (Dipsacaceae), and Valeriana (Caprifoliaceae). Visual signals of T. globosa are similar in both fly and bee vision models to those of the sympatric food plants used in the choice experiments, but scent signals are divergent. Field experiments conducted in Austria and the Czech Republic showed that both naive and experienced (with respect to visitation of T. globosa) insect species approached the orchids at the same rate as food plants, but direct contact with orchid flowers was taxon specific. Flies were most easily duped into probing the orchid, and, in doing so, frequently received and deposited pollinaria, whereas most bees and butterflies avoided landing on orchid flowers. We conclude that T. globosa is a mimic of a guild of fly‐pollinated plants, but the ecological dependence of the orchid on its models remains to be fully tested. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 180 , 269–294.     

Variation in pollinator abundance and selection on fragrance phenotypes in an epiphytic orchid

Extraordinary floral variation is common among some orchids that employ deception to attract pollinators. This variation may be maintained by frequency-dependent selection where rare phenotypes are preferred. Over a 2-yr period, 1993-1994, we monitored the reproductive success of Tolumnia variegata, an obligately outcrossing epiphytic orchid, at three localities in Puerto Rico that differed in pollinator service. Plants varied in floral morphology and fragrance characteristics. Artificial arrays of varying frequencies of scentless and fragrant phenotypes were established to test for frequency-dependent selection. Where pollinators were rare (Cambalache, range of census average = 0-0.2 bees/h), 0.9-1.2% of the flowers were effectively visited (pollinarium removals and pollinations). At Tortuguero where 0.4-1.1 bees/h were observed, 4-9.2% of the flowers were visited. At Pi;atnones where bees were the most abundant (1.4-5.2 bees/h), 20.9-25.0% of the flowers were visited. A significant portion of the variance in all measures of reproductive success (male, female, and combined) was explained by differences among populations, which we attribute mostly to variation in pollinator abundance. Neither the fragrance phenotype nor its frequency had a significant effect on success as revealed by a split-plot ANOVA. There was a significant interaction between population and phenotypic frequencies in all our measures of reproductive success, but only for the 1994 flowering season. Thus, variation in floral fragrance phenotypes is not likely maintained by frequency-dependent selection. High levels of variation remain unexplained.     

Phylogeny,diversification patterns and historical biogeography of euglossine orchid bees (Hymenoptera: Apidae)

The orchid bees constitute a clade of prominent insect pollinators distributed throughout the Neotropical region. Males of all species collect fragrances from natural sources, including flowers, decaying vegetation and fungi, and store them in specialized leg pockets to later expose during courtship display. In addition, orchid bees provide pollination services to a diverse array of Neotropical angiosperms when foraging for food and nesting materials. However, despite their ecological importance, little is known about the evolutionary history of orchid bees. Here, we present a comprehensive molecular phylogenetic analysis based on ～4.0 kb of DNA from four loci [cytochrome oxidase (CO1), elongation factor 1‐α (EF1‐α), arginine kinase (ArgK) and RNA polymerase II (Pol‐II)] across the entire tribe Euglossini, including all five genera, eight subgenera and 126 of the approximately 200 known species. We investigated lineage diversification using fossil‐calibrated molecular clocks and the evolution of morphological traits using disparity‐through‐time plots. In addition, we inferred past biogeographical events by implementing model‐based likelihood methods. Our dataset supports a new view on generic relationships and indicates that the cleptoparasitic genus Exaerete is sister to the remaining orchid bee genera. Our divergence time estimates indicate that extant orchid bee lineages shared a most recent common ancestor at 27–42 Mya. In addition, our analysis of morphology shows that tongue length and body size experienced rapid disparity bursts that coincide with the origin of diverse genera (Euglossa and Eufriesea). Finally, our analysis of historical biogeography indicates that early diversification episodes shared a history on both sides of Mesoamerica, where orchid bees dispersed across the Caribbean, and through a Panamanian connection, thus reinforcing the hypothesis that recent geological events (e.g. the formation of the isthmus of Panama) contributed to the diversification of the rich Neotropical biota. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 552–572.     

Pollinator limitaton in a deceptive orchid, Pogonia japonica, on a floating peat mat

Deceptive orchid species that offer no floral rewards to pollinators often experience pollinator limitation because they. The breeding system and fruit set were investigated in order to examine pollinator limitation for a population of a deceptive orchid, Pogonia japonica , on a floating peat mat in Mizorogaike Pond, western Japan. Fruit sets for outcross-pollinated, self-pollinated and pollinator-excluded flowers were 75%, 80%, and 0%, respectively. Thus, this species was self-compatible but neither autogamous nor apogamous. The fruit set for open-pollinated flowers was 22.9% and 17.4% in 1994 and 1995, suggesting that pollinator limitation did occur in the field. Larger flowers were more likely to develop into fruit than smaller ones in open pollination (36% vs 8%). Thus, flower size seems to affect fruiting of this species. No effective visits by major pollinators such as bees, which could carry pollinia, were observed during 16.5 h of observation during daytime. Instead, thrips were often found moving on gynostemium or pollinia and circumstantial evidence that suggests thrips may partly transfer pollen in pieces out of a granular pollinium of P. japonica was obtained. Pogonia japonica should come to use thrips as a pollinator to supplement low fruit set under limited flower visitation by major pollinators.