Flowering biology of Aspidistra (Asparagaceae): new data on pollination by dipteran insects

The genus Aspidistra comprises about 160 species of herbaceous plants. In previous investigations, different authors suggested that Aspidistra is pollinated by flies, fungus gnats, slugs, amphipods and even collembolans. The vast majority of data was based on only one species, A. elatior, and was not confirmed by direct observations. Recent field observations of anthetic plants confirm the idea of pollination by flies for two other species of the genus. The present study summarizes direct observations of flowering phenology and pollination of five previously unstudied species of Aspidistra. Flowering biology was studied using visual observations as well as video and photo monitoring. Flowers and captured pollinators were investigated using scanning electron microscopy. As a result, knowledge of the flowering biology of Aspidistra has been increased. The absence of heat production and an ultraviolet pattern were verified. The present data show that flowers of Aspidistra can serve as a food resource for animals. The investigated species of Aspidistra are pollinated by dipteran insects: A. formosa, A. marasmioides and A. subrotata are pollinated by fungus gnats; A. multiflora and A. oviflora are pollinated by flies. The occurrence of fungus‐gnat pollination was directly demonstrated for the first time in the genus Aspidistra. The present study confirmed the idea of myiophily in the genus Aspidistra. Apparently, myiophily is common and diverse in Aspidistra. More likely, pollinators are attracted by scent, which is undetectable by humans, but the attraction mechanism is still not completely clear.     

Specialized pollination by fungus gnats in the introduced population of <Emphasis Type="Italic">Aspidistra elatior</Emphasis>

The monocot genus Aspidistra comprises rhizomatous perennials that are distributed in tropical to warm temperate regions of Asia. Little is known about the pollinators of almost all the species, probably due to the inconspicuous nature of Aspidistra flowers. Nevertheless, the unusual floral morphology suggests biotic pollination, since pollen grains are hidden under each flower’s stigma. Aspidistra elatior has been suspected to have a very peculiar pollination ecology. So far, pollination by mollusks, crustaceans, or collembolans has been suspected. However, a recent study showed that A. elatior is mainly pollinated by species of fungus gnats in Kuroshima Island, southern Japan, which is its natural habitat. Here, we investigated the pollination ecology of A. elatior in Shiga Prefecture, central Japan, which is the introduced population, to reveal whether fungus gnats are also the main pollinator in the introduced population. Our study confirmed fungus gnats pollination in the investigated pollination. Furthermore, the main pollinators (i.e., Cordyla sixi and Bradysia sp.) are the same in both Kuroshima and Shiga Prefecture. Therefore, A. elatior mainly depends on a narrow taxonomic group of fungus gnats for pollination. In contrast, we failed to document any terrestrial amphipods visiting the A. elatior flowers, in spite of a relatively high fruit set in natural conditions. This fact will refute the amphipod pollination hypothesis proposed by previous studies. We consider that A. elatior is pollinated by fungus gnats through fungal mimicry, due to its superficial similarity to mushroom fruiting bodies and strong, musky floral scent.     

Pollination of Aristolochia pallida Willd. (Aristolochiaceae) in the Mediterranean

A first study of the pollination biology of a Mediterranean Aristolochia species in its natural habitat is presented. In all, 183 flowers of Aristolochia pallida Willd. were investigated, which in total contained 73 arthropods, dominated by two groups of Diptera, black fungus gnats (Sciaridae representing 37%) and scuttle flies (Phoridae representing 19%), respectively. However, only Phoridae are regarded as potential pollinators, since pollen has been found exclusively on the body of these insects. All Phoridae belong to the genus Megaselia and are recognised as three morpho-species. The measurements of flower and insect dimensions suggest that size is an important constraint for successful pollination: (a) the insects must have a definitive size for being able to enter the flower and (b) must be able to get in touch with the pollen. Only very few insect groups found in A. pallida fulfil these size requirements. However, size alone is not a sufficient filter as too many fly species of the same size might be trapped but not function as pollinators. Instead, specific attraction is required as otherwise pollen is lost. Since all trapped Phoridae are males, a chemical attraction (pheromones) is proposed as an additional constraint. Since the flowers are protogynous, the record of Megaselia loaded with pollen found in a flower during its female stage proves that this insect must have had visited at least one different flower during its male stage before. Further on, this observation provides strong evidence that the flowers are cross-pollinated. All these factors indicate a highly specialised pollination of A. pallida by Megaselia species.     

Pseudocopulatory pollination in lepanthes (orchidaceae: pleurothallidinae) by fungus gnats

BACKGROUND AND AIMS: Lepanthes is one of the largest angiosperm genera (>800 species). Their non-rewarding, tiny and colourful flowers are structurally complex. Their pollination mechanism has hitherto remained unknown, but has been subject of ample speculation; the function of the minuscule labellum appendix is especially puzzling. Here, the pollination of L. glicensteinii by sexually deceived male fungus gnats is described and illustrated. METHODS: Visitors to flowers of L. glicensteinii were photographed and their behaviour documented; some were captured for identification. Occasional visits to flowers of L. helleri, L. stenorhyncha and L. turialvae were also observed. Structural features of flowers and pollinators were studied with SEM. KEY RESULTS: Sexually aroused males of the fungus gnat Bradysia floribunda (Diptera: Sciaridae) were the only visitors and pollinators of L. glicensteinii. The initial long-distance attractant seems to be olfactory. Upon finding a flower, the fly curls his abdomen under the labellum and grabs the appendix with his genitalic claspers, then dismounts the flower and turns around to face away from it. The pollinarium attaches to his abdomen during this pivoting manoeuvre. Pollinia are deposited on the stigma during a subsequent flower visit. The flies appear to ejaculate during pseudocopulation. The visitors of L. helleri, L. stenorhyncha and L. turialvae are different species of fungus gnats that display a similar behaviour. CONCLUSIONS: Lepanthes glicensteinii has genitalic pseudocopulatory pollination, the first case reported outside of the Australian orchid genus Cryptostylis. Since most species of Lepanthes have the same unusual flower structure, it is predicted that pollination by sexual deception is prevalent in the genus. Several morphological and phenological traits in Lepanthes seem well suited for exploiting male fungus gnats as pollinators. Correspondingly, some demographic trends common in Lepanthes are consistent with patterns of male sciarid behaviour.     

广西蜘蛛抱蛋(Aspidistra retusa)的传粉生物学研究

蜘蛛抱蛋属植物的花部结构丰富多样,且常常贴地表开花,但其传粉生物学研究鲜有报道。广西蜘蛛抱蛋(Aspidistra retusa)是广西特有植物,为揭示该物种的自然传粉机制,在蜘蛛抱蛋属世界分布和分化中心的广西境内,开展了广西蜘蛛抱蛋开花物候、访花昆虫及繁育系统的野外观测研究。结果表明:广西蜘蛛抱蛋的花部结构中雄蕊高于雌蕊,但自交不亲和,为异花传粉;双翅目瘿蚊属成虫(Cecidomyia sp.,Cecidomyiidae,Diptera)为其专性传粉者,作为回报,广西蜘蛛抱蛋为瘿蚊提供理想的交配场所,同时提供大量的花粉供雌瘿蚊取食以补充生殖所需能量,并为受精卵的孵化以及幼虫的发育提供舒适的环境。该研究用实地现场观察第一手数据验证了前人有关蜘蛛抱蛋属植物瘿蚊传粉的推测,为中国蜘蛛抱蛋属植物传粉生物学研究的首次报道,然而蜘蛛抱蛋属植物花部结构极具多样性,应存在更多样的传粉方式,还有待更深入的调查研究。     

Pollination by fungus gnats in four species of the genus Mitella (Saxifragaceae)

The first example of pollination by fungus gnats in the eudicots is reported. The genus Mitella (Saxifragales) is characteristically produces minute, inconspicuous, mostly dull-coloured flowers with linear, sometimes pinnately branched, petals. To understand the function of these characteristic flowers, we studied the pollination biology of four Mitella species with different floral traits and different sexual expression: dioecious M. acerina , gynodioecious M. furusei var. subramosa , and hermaphroditic M. stylosa var. makinoi and M. integripetala. Flower-bagging experiments showed that wind pollination did not occur in the dioecious and gynodioecious species. Two years of observations of flower visitors at six study sites in Japan revealed that the principal pollinators of all four Mitella were specific species of fungus gnats (Mycetophilidae), which landed on the flowers with their long spiny legs settling on the petals. Characteristically, numerous pollen grains were attached to the fungus gnats in specific locations on the body. Although, on average, 1.3–2.6 fungus gnats visited each inflorescence per day, the fruit set of both bisexual and female flowers exceeded 63%. These results suggest that fungus gnats are highly efficient pollinators of Mitella spp., and that Mitella flowers are morphologically adapted to pollination by fungus gnats.  © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society , 2004, 144 , 449–460.     

Selective pollination by fungus gnats potentially functions as an alternative reproductive isolation among five Arisaema species

Background and AimsInterspecific difference in pollinators (pollinator isolation) is important for reproductive isolation in flowering plants. Species-specific pollination by fungus gnats has been discovered in several plant taxa, suggesting that they can contribute to reproductive isolation. Nevertheless, their contribution has not been studied in detail, partly because they are too small for field observations during flower visitation. To quantify their flower visitation, we used the genus Arisaema (Araceae) because the pitcher-like spathe of Arisaema can trap all floral visitors.MethodsWe evaluated floral visitor assemblage in an altitudinal gradient including five Arisaema species. We also examined interspecific differences in altitudinal distribution (geographic isolation) and flowering phenology (phenological isolation). To exclude the effect of interspecific differences in altitudinal distribution on floral visitor assemblage, we established ten experimental plots including the five Arisaema species in high- and low-altitude areas and collected floral visitors. We also collected floral visitors in three additional sites. Finally, we estimated the strength and contribution of these three reproductive barriers using a unified formula for reproductive isolation.Key ResultsEach Arisaema species selectively attracted different fungus gnats in the altitudinal gradient, experimental plots and additional sites. Altitudinal distribution and flowering phenology differed among the five Arisaema species, whereas the strength of geographic and phenological isolations were distinctly weaker than those in pollinator isolation. Nevertheless, the absolute contribution of pollinator isolation to total reproductive isolation was weaker than geographic and phenological isolations, because pollinator isolation functions after the two early-acting barriers in plant life history.ConclusionsOur results suggest that selective pollination by fungus gnats potentially contributes to reproductive isolation. Since geographic and phenological isolations can be disrupted by habitat disturbance and interannual climate change, the strong and stable pollinator isolation might compensate for the weakened early-acting barriers as an alternative reproductive isolation among the five Arisaema species.     

Notes on taxonomy and new taxa of Aspidistra (Ruscaceae) in the flora of Laos and Vietnam

One new species of Aspidistra, i.e. A. nutans, and one new variety, i.e. A. tillichiana var. latifolia, recently discovered in Vietnam are described and illustrated. In addition, the rank of species is proposed for A. formosa widely distributed in northern Vietnam but originally described as a variety of A. fungilliformis. Aspidistra subrotata is recorded as a new species for the flora of Laos. Data on ecology, phenology, natural variation, distribution and expected conservation status are provided for these plants.     

Pollination ecology in sympatric winter flowering Helleborus (Ranunculaceae)

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

Pollination mutualism between Alocasia macrorrhizos (Araceae) and two taxonomically undescribed Colocasiomyia species (Diptera: Drosophilidae) in Sabah, Borneo

Two taxonomically undescribed Colocasiomyia species were discovered from inflorescences of Alocasia macrorrhizos in Kota Kinabalu City, Sabah, Borneo, Malaysia. The aims of this study were to investigate the reproductive ecology of the flies and the plant, ascertain the importance of the flies as pollinators and examine the intimate association between flowering events and life history of the flies. We conducted sampling, observations and field pollination experiments. The flies were attracted by the odour of female‐phase inflorescences in the early morning on the first day of anthesis. They fed, mated and oviposited in the inflorescences for 1 day. On the second day, the flies, covered with pollen grains, left the male‐phase inflorescences for the next female‐phase inflorescences. The immature forms of both fly species hatched, developed and pupated within the infructescences without damaging the fruits, and developed adults emerged when the mature infructescences dehisced. The flowering events and fly behaviours were well synchronized. In field pollination experiments, inflorescences bagged with a fine mesh (insect exclusion) produced almost no fruits, whereas those bagged with a coarse mesh (bee exclusion) produced as many fruits as the open‐pollinated controls. These results indicate that these flies are the most efficient and specialised pollinators for their host, A. macrorrhizos. These flies, in return, depend on A. macrorrhizos for food and habitat through most of their life cycle. This study provides a deeper insight into the less recognised, highly intimate pollination mutualism between Araceae plants and Colocasiomyia flies.     

THE EFFECTIVENESS OF FUNGUS GNATS AS POLLINATORS

Fungus gnats (Sciaridae and Mycetophilidae) are the principal pollinators of Listera cordata (L.) R. Br. (Orchidaceae) and Scoliopus bigelovii Torr. (Liliaceae) in coastal redwood forests of northern California. Although primitive diptera have generally been regarded as relatively inefficient pollinators, fruit set for both species is high: 61–78% for L. cordata (1976–1978) and 94.3–98.5% for S. bigelovii (1978–1979). Since probability of pollination per visit is low, we attribute high fruit set to the large number of gnats present at our study sites and corresponding large number of visits to flowers. The relative frequency of geitonogamous vs. xenogamous pollen flow was estimated by emasculating flowers and subsequently comparing pollen reception or fruit set of emasculates with controls. Results for both species indicate that interplant movement of pollen is common. Thus, fungus gnats can be effective pollen vectors, both in terms of overall fruit set and potential for cross-pollination.     

Floral divergence and temporal pollinator partitioning in two synchronopatric species of <Emphasis Type="Italic">Vigna</Emphasis> (Leguminosae-Papilionoideae)

Exclusivity of pollinators, temporal partitioning of shared pollinators and divergence in pollen placement on the shared pollinators’ bodies are mechanisms that prevent interspecific pollen flow and minimize competitive interactions in synchronopatric plant species. We investigated the floral biology, flower visitors, pollinator effectiveness and seasonal flower availability of two syntopic legume species of the genus Vigna, V. longifolia and V. luteola, in ‘restinga’ vegetation of an island in southern Brazil. Our goal was to identify the strategies that might mitigate negative consequences of their synchronous flowering. Vigna longifolia and V. luteola were self-compatible, but depended on pollinators to set seeds. Only medium to large bees were able to trigger the ‘brush type’ pollination mechanism. Vigna longifolia, with its asymmetrical corolla and hugging mechanism, showed a more restrictive pollination system, with precise sites of pollen deposition/removal on the bee’s body, compared to V. luteola, with its zygomorphic corolla and cymbiform keel. There was a daily temporal substitution in flower visitation by the main pollinators. Vigna longifolia and V. luteola had overlapping flowering phenology but the densities of their flowers fluctuated, resulting in a seasonal partitioning of flower visitation. The differences in corolla symmetry and mainly the temporal partitioning among pollinators throughout the day and the flowering season proved to be important factors in maintaining the synchronopatry of V. longifolia and V. luteola.     

Parallel chemical switches underlying pollinator isolation in Asian Mitella

Floral scents are among the key signals used by pollinators to navigate to specific flowers. Thus, evolutionary changes in scents should have strong impacts on plant diversification, although scent‐mediated plant speciation through pollinator shifts has rarely been demonstrated, despite being likely. To examine whether and how scent‐mediated plant speciation may have occurred, we investigated the Asimitellaria plant lineage using multidisciplinary approaches including pollinator observations, chemical analyses of the floral scents, electroantennographic analyses and behavioural bioassays with the pollinators. We also performed phylogenetically independent contrast analyses of the pollinator/floral scent associations. First, we confirmed that the pairs of the sympatric, cross‐fertile Asimitellaria species in three study sites consistently attract different pollinators, namely long‐tongued and short‐tongued fungus gnats. We also found that a stereoisomeric set of floral volatiles, the lilac aldehydes, could be responsible for the pollinator specificity. This is because the compounds consistently elicited responses in the antennae of the long‐tongued fungus gnats and had contrasting effects on the two pollinators, that is triggering the nectaring behaviour of long‐tongued fungus gnats while repelling short‐tongued fungus gnats in a laboratory experiment. Moreover, we discovered that volatile composition repeatedly switched in Asimitellaria between species adapted to long‐tongued and short‐tongued fungus gnats. Collectively, our results support the idea that recurrent scent‐mediated speciation has taken place in the Asimitellaria–fungus gnat system.     

中国蜘蛛抱蛋属二新记录种

首次报道了黄瓣蜘蛛抱蛋(Aspidistra lutea H.-J.Tillich)和吉婆岛蜘蛛抱蛋(A.arnautovii H.-J.Tillich)在中国的分布。这两种植物分别被发现于广西西南部的靖西县、龙州县。文中提供了形态学描述和图片。凭证标本存放于广西植物标本馆(IBK)。     

Pollinator Specificity and Convergence in Fly-pollinated Pleurothallis(Orchidaceae) Species: A Multiple Population Approach

We studied the floral biology of 12 populations of five rupicolousPleurothallis(Orchidaceae) species occurring in campo rupestre vegetationat nine localities in Brazil. All of these species are pollinatedby flies belonging to the families Chloropidae and Phoridae.In the five Pleurothallis species studied, all conspecific populationsattracted the same pollinator species. All pollinators werefemales; they laid eggs in flowers of the two nectarless species,but never in the flowers of nectar-presenting species. The twopairs ofPleurothallis species with similar flower morphologiesand odours attracted the same pollinators: P. johannensis -P. fabiobarrosii, pollinated by Tricimba sp. (Chloropidae) andP. teres - P. ochreata pollinated by Megaselia spp. (Phoridae).There was no overlap in the distribution of thePleurothallisspecies that shared pollinators. Despite similarities in floralmorphology and odour, genetic data show that these species pairsare not each other's closest relatives. We hypothesize thatthese similarities are due to convergence in allopatric speciesthat evolved similar pollination mechanisms. Conversely, thereare reasons to believe that adaptation to different pollinationmechanisms occurred in the closely related species P. johannensisand P. teres.Copyright 2001 Annals of Botany Company Pleurothallis, Orchidaceae, floral biology, fly-pollination, Chloropidae, Phoridae, pollinator specificity, campo rupestre     

Diverse pollination systems of the twin-spurred orchid genus Satyrium in African grasslands

The large terrestrial orchid genus Satyrium underwent evolutionary radiations in the Cape floral region and the grasslands of southern and eastern Africa. These radiations were accompanied by tremendous diversification of the unusual twin-spurred flowers that characterize the genus, but pollination data required to interpret these patterns of floral evolution have been lacking for grassland species in the genus. Here we document pollinators, nectar properties, and levels of pollination success for 11 grassland Satyrium species in southern and south-central Africa. Pollinators of these species include bees, beetles, butterflies, hawkmoths, noctuid moths, long-proboscid flies, and sunbirds. Most species appear to be specialized for pollination by one functional pollinator group. Long-proboscid fly pollination systems are reported for the first time in Satyrium (in S. macrophyllum and a high-altitude form of S. neglectum). Floral morphology, especially spur length and rostellum structure, differs markedly among plants with different pollinators, while nectar volume, concentration, and sugar composition are fairly uniform across species. Most taxa exhibited high levels of pollination success (>50% of flowers pollinated), a trend that can be attributed to the presence of nectar in the twin spurs.     

Differentiation of floral color and odor in two fly pollinated species ofMetrodorea (Rutaceae) from Brazil

We investigated if differences in morphological characters in two species ofMetrodorea (Rutaceae) from Brazilian semideciduous forests correspond to some pollination divergence.M. nigra andM. stipularis are sympatric species, display a similar floral morphology, are protandrous, self-incompatible, their flower periods overlap, and both are pollinated by flies.M. nigra main pollinators arePseudoptiloleps nigripoda (Muscidae) andFannia sp. (Fanniidae);M. stipularis major pollinators arePhaenicia eximia (Calliphoridae),Palpada sp. andOrnidia obesa (Syrphidae). The distinct floral odor (disagreeable inM. nigra and sweet inM. stipularis) and color (brownish violet vs. pale yellow) determine the differences on type and number of floral visitors observed. Several species from semideciduous forests initially considered to be pollinated by diverse insects, present flies as main pollinators, stressing the importance of fly pollination in such habitats.     

Caught in the act: pollination of sexually deceptive trap-flowers by fungus gnats in Pterostylis (Orchidaceae)

Background and Aims Pterostylis

is an Australasian terrestrial orchid genus of more than 400 species, most of which use a motile, touch-sensitive labellum to trap dipteran pollinators. Despite studies dating back to 1872, the mechanism of pollinator attraction has remained elusive. This study tested whether the fungus gnat-pollinated Pterostylis sanguinea secures pollination by sexual deception.

Methods

The literature was used to establish criteria for confirming sexual deception as a pollination strategy. Observations and video recordings allowed quantification of each step of the pollination process. Each floral visitor was sexed and DNA barcoding was used to evaluate the degree of pollinator specificity. Following observations that attraction to the flowers is by chemical cues, experimental dissection of flowers was used to determine the source of the sexual attractant and the effect of labellum orientation on sexual attraction. Fruit set was quantified for 19 populations to test for a relationship with plant density and population size.

Key Results

A single species of male gnat (Mycetophilidae) visited and pollinated the rewardless flowers. The gnats often showed probing copulatory behaviour on the labellum, leading to its triggering and the temporary entrapment of the gnat in the flower. Pollen deposition and removal occurred as the gnat escaped from the flower via the reproductive structures. The labellum was the sole source of the chemical attractant. Gnats always alighted on the labellum facing upwards, but when it was rotated 180 ° they attempted copulation less frequently. Pollination rate showed no relationship with orchid population size or plant density.

Conclusions

This study confirms for the first time that highly specific pollination by fungus gnats is achieved by sexual deception in Pterostylis. It is predicted that sexual deception will be widespread in the genus, although the diversity of floral forms suggests that other mechanisms may also operate.     

Pollination of the European food-deceptive Traunsteinera globosa (Orchidaceae): the importance of nectar-producing neighbouring plants

European food-deceptive orchids generally flower early in spring and rely on naïve pollinators for their reproduction. Some species however, flower later in the summer, when many other rewarding plants species are also in bloom. In dense flowering communities, deceptive orchids may suffer from competition for pollinator resources, or might alternatively benefit from higher community attractiveness. We investigated the pollination strategy of the deceptive species Traunsteinera globosa, and more specifically whether it benefited from the presence of coflowering rewarding species. We carried out a population survey to quantify the density and reproductive success of the orchid as well as the density of all coflowering species. Our results suggest that the deceptive orchid not only benefited from the presence of coflowering species, but that interestingly the density of the species Trifolium pratense was significantly positively correlated with the orchid's reproductive success. This species might simply act as a magnet species attracting pollinators near T. globosa, or could influence the orchid reproductive fitness through a more species-specific interaction. We propose that morphological or colour similarities between the two species should be investigated in more detail to decipher this pollination facilitation effect.     

Florivory and floral larceny by fly larvae decrease nectar availability and hummingbird foraging visits at Heliconia (Heliconiaceae) flowers

Insect larvae inhabit the corolla tubes of some Heliconia species (Heliconiaceae). In this study, we present the first evidence of the influence of these larvae on the pollination ecology of Heliconia plants. We provide experimental evidence that the flowers of Heliconia spathocircinata infested by flies have less nectar for pollinators and received fewer visits by hummingbird pollinators, in comparison with uninfested flowers.