Lying to Pinocchio: floral deception in an orchid pollinated by long-proboscid flies

Plants that lack floral rewards may nevertheless attract pollinators if their flowers sufficiently resemble those of rewarding plants. Flowers of the South African terrestrial orchid Disa nervosa are similar in floral dimensions and spectral reflectance to those of a sympatric nectar-producing irid ( Watsonia densiflora s.l. ). Observations showed that the orchid and Watsonia share the same pollinator, a long-proboscid tabanid fly Philoliche aethiopica . These flies visited inflorescences of both species during their foraging bouts and most (64%) observed or captured on Watsonia inflorescences carried pollinaria of the orchid on their proboscides. They probe an average of 6.3 flowers on Watsonia inflorescences, but just 1.9 flowers on the Disa inflorescences, a behaviour which would strongly promote cross-pollination in the self-compatible orchid. The orchid generally achieves high levels of pollination success, with approximately 50% of flowers receiving or exporting pollen at some sites. Pollination success was also high at one site that lacked Watsonia plants, suggesting that the orchid does not have an obligate dependence on Watsonia . Its pollination system may therefore be characterized as intermediate between generalized food deception and specific floral mimicry.  © 2006 The Linnean Society of London, Botanical Journal of the Linnean Society , 2006, 152 , 271–278.     

Evidence for Bastesian mimicry in a butterfly-pollinated orchid

Observations in the Cape Province, South Africa, showed that Disa ferruginea (Orchidaceae) is dependent on a single butterfly species— Meneris tulbaghia (Nymphalidae: Satyrinae)—for pollination. The flowers of D. ferruginea contain no food reward and, instead, appear to secure pollinator visits by imitating flowers which are nectar sources for the butterfly. A red-flowered form of D. ferruginea appears to mimic the red nectar-producing flowers of Tritoniopsis triticea (Iridaceae) in the south-western Cape, while an orange-flowered form of D. ferruginea appears to mimic the orange nectar-producing flowers of Kniphofia uvaria (Asphodelaceae) in the Langeberg Mountains. Reflectance spectra of the orchid's flowers closely match those of its putative models. Analysis of foraging movements of the butterfly in a mixed stand of D. ferruginea and T. triticea indicated that it does not discriminate between the nectarless orchid and the nectar-producing model. Populations of D. ferruginea which are sympatric with T. triticea have relatively high levels of pollination and fruit production, compared with populations where the orchid grows alone. Although other studies have reported relatively low fecundity in deceptive orchids, pollination and fruiting success in D. ferruginea compares favourably with a nectar-producing congener, Disa uniflora , which is also pollinated solely by M. tulbaghia.     

Armament imbalances: match and mismatch in plant-pollinator traits of highly specialized long-spurred orchids

Background

Some species of long-spurred orchids achieve pollination by a close association with long-tongued hawkmoths. Among them, several Habenaria species present specialized mechanisms, where pollination success depends on the attachment of pollinaria onto the heads of hawkmoths with very long proboscises. However, in the Neotropical region such moths are less abundant than their shorter-tongued relatives and are also prone to population fluctuations. Both factors may give rise to differences in pollinator-mediated selection on floral traits through time and space.

Methodology/Principal Findings

We characterized hawkmoth assemblages and estimated phenotypic selection gradients on orchid spur lengths in populations of three South American Habenaria species. We examined the match between hawkmoth proboscis and flower spur lengths to determine whether pollinators may act as selective agents on flower morphology. We found significant directional selection on spur length only in Habenaria gourlieana, where most pollinators had proboscises longer than the mean of orchid spur length.

Conclusions/Significance

Phenotypic selection is dependent on the mutual match between pollinator and flower morphologies. However, our findings indicate that pollinator-mediated selection may vary through time and space according to local variations in pollinator assemblages.     

Pollination by megachilid bees and determinants of fruit-set in the Cape orchid Disa tenuifolia

Wild-fires near Cape Town, South Africa, stimulated mass-flowering in several populations of Disa tenuifolia (Orchidaceae). We found that the bright yellow flowers of the orchid are pollinated by various carder and leafcutter bees (Megachilidae) and occasionally monkey beetles (Scarabaeidae: Hopliini). The highly elongate pollinaria become attached to the underside of the pollinator's thorax. The bees showed strong fidelity towards the orchid, despite the lack of nectar in its flowers. The orchid does not appear to mimic other rewarding species. It was concluded that the pollination system of D. tenuifolia depends on exploitation of instinctive foraging and territorial behaviour of male megachilid bees. The fruiting success of D. tenuifolia at the study site was pollinator-limited as supplementary hand-pollinations resulted in a two-fold increase in the percentage of flowers which set fruit.     

Phylogeny and radiation of pollination systems in DISA (Orchidaceae)

We studied the patterns of adaptive radiation in Disa, a large orchid genus in southern Africa. A cladogram for 27 species was constructed using 44 morphological characters. Pollination systems were then mapped onto the phylogeny in order to analyze pathways of floral evolution. Shifts from one pollination system to another have been a major feature of the evolutionary diversification of Disa. Unlike many plant genera that are pollinated mainly by a single group of insects, radiation in Disa has encompassed nearly all major groups of pollinating insects; in all, 19 different specialized pollination systems have been found in the 27 species included in this analysis. Another striking pattern is the repeated evolution of broadly similar pollination systems in unrelated clades. For example, butterfly-pollinated flowers have evolved twice; showy deceptive flowers pollinated by carpenter bees, twice; long-spurred flowers pollinated by long-tongued flies, four times; night-scented flowers pollinated by moths, three times; and self-pollination, three times. This suggests that a few dominant pollinator species in a region may be sufficient to generate diversification in plants through repeated floral shifts that never retrace the same pathways.     

Eye Attached Hemipollinaria in the Hawkmoth and Settling Moth Pollination of Habenaria (Orchidaceae): A Study on Functional Morphology in 5 Species from Subtropical South America

Morphological adaptations to sphingophily and pollination by moths was studied in 5 South American Habenaria species. For H. gourlieana and H. hieronymi direct evidence of hawkmoth (Agrius cingulatus and Manduca sexta) and settling moth (Rachiplusia nu) pollination, respectively, by hemipollinaria attachment on the eyes, is presented. In two other species (H. paucofilia, H. rupicola) pollination by settling moths and eye attachment of the hemipollinaria can be inferred by indirect evidence (placement of scales and massulae on the flowers) and by flower structure. For the fifth species (H. montevidensis) pollination by small moths or mosquitoes with hemipollinaria attachment on the proboscis is postulated. A comparative study in floral features revealed clear morphological divergence between sphingophilous and phalaenophilous species. In addition to deeper spurs the former have slender, exerted, and upturned petal lobes (acting as mechanical guide to the hovering visitors), a much developed median rostellar lobe (acting as deflecting surface of the hawkmoths towards the viscidia), flexible and sinuous hemipollinarium caudicles (appropriate for frontal strikes against the stigma when hemipollinaria are brought by the hawkmoths dangling against the flower). Male efficiency was compared between 4 species with overlapping flowering time in the same area. Male efficiency factors were unexpectedly low in all species. Only in one species (H. hieronymi) each pollen donation accounted for more than one pollination. H. gourlieana is part of a more or less rich sphingophilous flora interacting with the same two long-tongued hawkmoth species. Interspecific competition for pollen placement on the pollinator's body surface is probably low on account of different pollination mechanisms.     

Exploitation of a specialized mutualism by a deceptive orchid

Plants that lack floral rewards may nevertheless attract pollinators through mimetic resemblance to the flowers of co-occurring rewarding plants. We show how a deceptive orchid (Disa nivea) successfully exploits a reciprocally specialized mutualism between a nectar-producing plant (Zaluzianskya microsiphon) and its long-proboscid fly pollinator (Prosoeca ganglbaueri). Disa nivea is a rare southern African orchid known only from habitats that support large populations of Z. microsiphon, which it closely resembles in both general morphology and floral spectral reflectance. Significant covariation in floral traits of Z. microsiphon and D. nivea was detected among populations. Where mimics are uncommon, flies do not appear to discriminate between the flowers of the two species. Pollination success in D. nivea was much higher at a site with abundant Z. microsiphon plants than at a site where Z. microsiphon was rare. Exploitation of a highly specialized mutualism appears to demand a high degree of phenotypic resemblance to a rewarding model by a deceptive mimic, as exemplified by D. nivea. The majority of deceptive orchids, on the other hand, exploit relatively generalized pollination systems and thus require only a vague resemblance to rewarding plants in the community in order to attract pollinators.     

Transfer of pollinaria on birds’ feet: a new pollination system in orchids

We report the discovery of a new mechanism of pollination in orchids: transfer of pollinaria on the feet of birds. Observations carried out in South Africa and Malawi showed that the orchids Disa chrysostachya Sw. and Disa satyriopsis Kraenzl. are pollinated by sunbirds. Pollinaria of these orchids become attached firmly to the birds toes when they perch on the tall narrow inflorescences which are packed tightly with numerous small orange flowers. Birds typically perch on the lower part of an inflorescence while reaching up to feed on nectar in flowers on the upper part, but occasionally reverse this position to probe the lower flowers. The nectar is contained within a short bulbous spur with a narrow entrance that permits entrance of a sunbirds slender tongue. Contrary to expectation, the pollination mechanism in D. chrysostachya is remarkably efficient with about 6.1% of pollen reaching stigmas on other plants and fruit set occurring in 95% of flowers at one site. Birds seldom move their feet once perched, thus minimizing the incidence of self-pollination, either within or between flowers on an inflorescence.     

Male interference with pollination efficiency in a hermaphroditic orchid

Hermaphroditism can lead to both intra‐ and intersexual conflict between male and female gender functions. However, the effect that such gender conflicts have on pollination efficiency has seldom been investigated. By artificially reducing the number of available male gametes on an individual, we quantified whether male interference with pollination efficiency occurs in the self‐compatible, moth‐pollinated orchid Satyrium longicauda. We partially emasculated S. longicauda inflorescences and compared pollination success and fecundity in these plants to intact controls. Pollen in both groups of plants was colour‐labelled so that its dispersal by pollinators could be tracked directly in the field. Intact flowers on partially emasculated inflorescences exported more pollen and received more cross‐pollen and less self‐pollen than those on intact inflorescences. Proportion of fruit set per plant was similar between the two treatments; however, fruits on partially emasculated plants had proportionally more viable seeds than those on intact controls. These results provide empirical evidence that male interference with pollination efficiency can occur in a hermaphroditic plant and that such interference can compromise fecundity. The most likely mechanism for such male interference is competition for placement on the proboscis of hawkmoth pollinators. Consequently, male competition for siring success may influence the evolution of sexual systems in hermaphroditic pollinator‐dependent plants.     

Generalized pollination,floral scent chemistry,and a possible case of hybridization in the African orchid Disa fragrans

Pollination systems in orchids tend to be specialized as a consequence of restrictive floral morphology and specific advertising signals. Here we document a notable exception: Disa fragrans subsp. fragrans, a taxon from the Drakensberg Mountains of South Africa, which is pollinated by insects belonging to at least four orders (flies, beetles, bees, and moths). Pollinaria of D. fragrans are attached to the feet of these visitors and pollination thus occurs in a rather haphazard fashion. Nevertheless, its pollination success and pollen transfer efficiency are comparable to those of its close relative, Disa sankeyi, which is pollinated by a single genus of wasps. D. fragrans has an exceptionally strong floral scent: volatile emission is 19–86 μg per inflorescence per hour, which is up to 100 fold greater than in D. sankeyi. The scent bouquet is comprised of at least 46 compounds, mostly benzenoids and phenylpropanoids, which are known to be general attractants to a wide range of insects. In contrast to D. sankeyi, the flowers of D. fragrans have a high level of spectral purity (chroma) as is typical of many generalist insect-pollinated plants. At a site where D. fragrans co-occurs with D. sankeyi we found a plant with intermediate characteristics that may be a hybrid between the two taxa. The novel case of generalist pollination in D. fragrans documented here serves as an example of how floral advertising traits might evolve during an evolutionary shift from specialized to generalized pollination.     

Hawkmoth pollination of aerangoid orchids in Kenya, with special reference to nectar sugar concentration gradients in the floral spurs

The African orchid flora has a high proportion of species with long-spurred white flowers. Few data exist to test the prediction that this floral syndrome pattern reflects an important role for hawkmoth pollination in the evolution and ecology of these orchids. The pollination biology of five aerangoid orchid species (Rangaeris amaniensis, Aerangis brachycarpa, A. confusa, A. thomsonii, and A. kotschyana) was investigated in Kenya. Four of these have long spurs (>10 cm) and were pollinated by Agrius convolvuli and Coelonia fulvinotata. Aerangis confusa, which has relatively short spurs (ca. 4 cm), was pollinated by the short-tongued hawkmoths Hippotion celerio and Daphnis nerii. Nectar frequently filled the entire spur in some of the study species, even at anthesis. Sugar concentration of the nectar of four species was found to vary from ca. 1% at the mouth of the spur to 20% at the tip. Gradients were expressed more strongly in species with long, straight spurs. Species with spirally twisted spurs showed both steep and shallow nectar gradients. These gradients, previously unknown in plants, may function as a "sugar trail," enticing long-tongued hawkmoths to probe deeply into spurs without incurring the cost of filling an entire spur with concentrated nectar. In addition, the most concentrated nectar is kept out of reach of short-tongued pollinators.     

Effects of distance from models on the fitness of floral mimics

• Rewardless plants can attract pollinators by mimicking floral traits of rewarding heterospecific plants. This should result in the pollination success of floral mimics being dependent on the relative abundance of their models, as pollinator abundance and conditioning on model signals should be higher in the vicinity of the models. However, the attraction of pollinators to signals of the models may be partially innate, such that spatial isolation of mimics from model species may not strongly affect pollination success of mimics.
• We tested whether pollination rates and fruit set of the rewardless orchid Disa pulchra were influenced by proximity and abundance of its rewarding model species, Watsonia lepida.
• Pollination success of the orchid increased with proximity to the model species, while fruit set of the orchid increased with local abundance of the model species. Orchids that were experimentally translocated outside the model population experienced reduced pollinaria removal and increased pollinator‐mediated self‐pollination.
• These results confirm predictions that the pollination success of floral mimics should be dependent on the proximity and abundance of model taxa, and thus highlight the importance of ecological facilitation among species involved in mimicry systems.

     

LONG-TONGUED FLY POLLINATION AND EVOLUTION OF FLORAL SPUR LENGTH IN THE DISA DRACONIS COMPLEX (ORCHIDACEAE)

Field studies in South Africa showed that floral spur length in the Disa draconis complex (Orchidaceae) varies enormously between populations in the southern mountains (means = 32–38 mm), lowland sandplain (mean = 48 mm), and northern mountains (means = 57–72 mm). We tested the hypothesis that divergence in spur length has resulted from selection exerted through pollinator proboscis length. Short-spurred plants in several southern mountain populations, as well as long-spurred plants in one northern mountain population, were pollinated by a horsefly, Philoliche rostrata (Tabanidae), with a proboscis length that varied from 22 to 35 mm among sites. Long-spurred plants on the sandplain were pollinated by the tanglewing fly, Moegistorynchus longirostris (Nemestrinidae), which has a very long proboscis (mean = 57 mm). Selection apparently favors long spurs in sandplain plants, as artificial shortening of spurs resulted in a significant decline in pollen receipt and fruit set, although pollinaria removal was not significantly affected. Fruit set in the study populations was limited by pollen availability, which further suggests that selection on spur length occurs mainly through the female component of reproductive success.     

Hawkmoth pollination of the African epiphytic orchid Mystacidium venosum, with special reference to flower and pollen longevity

 The pollination biology of Mystacidium venosum Harv. ex Rolfe, an epiphytic orchid endemic to southern Africa, was investigated. The white flowers of this orchid have long spurs (c 4.5 cm) and contain dilute sucrose-dominated nectar which is secreted during the afternoon and early evening. Scent, dominated by Jasmine lactone and (E, E)-Farnesol, is emitted in the evening. A breeding system experiment established that self pollination results in inferior quality fruits. Field observations at three sites in Kwa-Zulu Natal, South Africa, in 1998 and 1999 showed that hawkmoths were frequent visitors to the orchid shortly after dusk, and carry pollinaria along the length of their tongues. No evidence for directional selection on spur length was found at any of the three sites. Results showed that flower longevity is strongly reduced by pollination, while pollinaria removal had only a small effect. Pollinia removed from flowers remained viable for up to 20 days under outdoor conditions. Received August 15, 2000 Accepted April 17, 2001     

Interactions between hawkmoths and flowering plants in East Africa: polyphagy and evolutionary specialization in an ecological context

Hawkmoths (Lepidoptera, Sphingidae) are considered important pollinators in tropical regions, but the frequency and degree of reciprocal specialization of interactions between hawkmoths and flowers remain poorly understood. Detailed observations at two sites in Kenya over a two‐year period indicate that adult hawkmoths are routinely polyphagous and opportunistic, regardless of their proboscis length. About 700 individuals of 13 hawkmoth species were observed visiting a wide range of plant species at the study sites, including 25 taxa that appear to be specifically adapted for pollination by hawkmoths. We estimate that 277 plant species in Kenya (c. 4.61% of the total angiosperm flora) are adapted for pollination by hawkmoths. Floral tube lengths of these plants have a bimodal distribution, reflecting the existence of two hawkmoth guilds differing in tongue length. Hawkmoths exhibited strongly crepuscular foraging patterns with activity confined to a 20‐min period at dusk and, in some cases, a similar period just before dawn. Corolla tube length appears to act as a mechanical filter as the longest‐tubed plants were visited by the fewest hawkmoth species and these were exclusively from the long‐tongued guild. Tube length showed a strong positive relationship with nectar volume, even after phylogenetic correction, which implies that plants with long corolla tubes are under selection to offer relatively large amounts of nectar to entice visits by polyphagous long‐tongued hawkmoths. Our study shows that diffusely co‐evolved pollination systems involving long‐tongued hawkmoths are clearly asymmetrical, with plants exhibiting a high degree of floral specialization, while hawkmoths exhibit polyphagous behaviour. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 199–213.     

Habitat dependent pollination success in a Cape orchid

Summary We examined the pollination success of Disa uniflora (Orchidaceae) in two habitats. Plants occurring in a rocky gorge were far more successful than plants occurring in an adjacent open valley. More than 55% of flowers in the gorge were pollinated and set fruit compared with less than 25% of flowers in the valley. These differences are explained by the preference of Meneris tulbaghia (Satyridae), the exclusive pollinator of the orchid, for rocky, sheltered habitats. Fruit set of hand-pollinated flowers did not differ significantly between the two habitats, indicating that resources did not account for the variation in fruiting success.     

Disa albomagentea (Orchidaceae), a new species from the Hottentots Holland Mountains in the Cape Floristic Region, South Africa

A new orchid, Disa albomagentea, is described from the Hottentots Holland Mountains in the Western Cape Province of South Africa. It is an obligately fire-dependent species closely related to Disa obtusa (sect. Disella), from which it can be easily distinguished by the larger flowers, i.e. galea 7-9 mm long versus 4-7 mm long, which are patent and bicoloured, i.e. magenta, white and not spotted versus purple brown, white to cream to greenish, and variously purple spotted. It appears to be endemic to seeps and marshes on the high peaks.     

Coevolution Between Food-Rewarding Flowers and Their Pollinators

The concept of coevolution was first developed by Darwin, who used it to explain how pollinators and food-rewarding flowers involved in specialized mutualisms could, over time, develop long tongues and deep tubes, respectively. He famously predicted that Angraecum sesquipedale, a long-spurred Malagasy orchid, must be pollinated by a hawkmoth with an exceptionally long tongue. Darwin’s idea of a coevolutionary “race” was championed by contemporary naturalists, including Alfred Wallace, and a hawkmoth fitting the expected tongue-length profile was eventually discovered in Madagascar during the early twentieth century. However, strong empirical support for the mechanism behind Darwin’s coevolutionary model has been forthcoming only in the past two decades. It is now established that selection often strongly favors plants with floral tubes that exceed the length of their pollinator’s tongues. There is also evidence that pollinators gain an energetic benefit from having tongues that enable them to consume most or all of the nectar in deep tubular flowers. Alternative explanations for the evolution of long pollinator tongues, such as evasion of predators that use flowers as ambush sites, are considered much less compelling and lack quantitative support. Another important advance in coevolution research has been the development of approaches that explicitly predict a geographical mosaic of coevolution. The expectation that coevolution can lead to geographical diversification and trait covariation among strongly interacting organisms is strongly supported by studies of long-proboscid fly and oil-bee pollination systems in South Africa. Macro- and microevolutionary studies of pollination systems suggest that coevolution can operate alongside other one-sided evolutionary processes, such as shifts, in shaping plant and pollinator traits.     

Diversity of mycorrhizal fungi of terrestrial orchids: compatibility webs, brief encounters, lasting relationships and alien invasions

The diversity of mycorrhizal fungi associated with an introduced weed-like South African orchid (Disa bracteata) and a disturbance-intolerant, widespread, native West Australian orchid (Pyrorchis nigricans) were compared by molecular identification of the fungi isolated from single pelotons. Molecular identification revealed both orchids were associated with fungi from diverse groups in the Rhizoctonia complex with worldwide distribution. Symbiotic germination assays confirmed the majority of fungi isolated from pelotons were mycorrhizal and a factorial experiment uncovered complex webs of compatibility between six terrestrial orchids and 12 fungi from Australia and South Africa. Two weed-like (disturbance-tolerant rapidly spreading) orchids — D. bracteata and the indigenous Australian Microtis media, had the broadest webs of mycorrhizal fungi. In contrast, other native orchids had relatively small webs of fungi (Diuris magnifica and Thelymitra crinita), or germinated exclusively with their own fungus (Caladenia falcata and Pterostylis sanguinea). Orchids, such as D. bracteata and M. media, which form relationships with diverse webs of fungi, had apparent specificity that decreased with time, as some fungi had brief encounters with orchids that supported protocorm formation but not subsequent seedling growth. The interactions between orchid mycorrhizal fungi and their hosts are discussed.     

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.