Floral Deception Research Articles

Floral deception in dioecious Actinidia polygama (Actinidiaceae) revealed by differential nitrogen investment in male organs

AbstractAnimal‐pollinated plants have evolved rewards and advertisements to attract pollinators, which learn to associate advertisements with rewards. Pollen‐collecting insects, such as bees, associate stamens with pollen (a reward) essential for brood rearing. In some dioecious plants, female flowers have stamens with sterile pollen grains to mimic male flowers. It is not yet fully understood whether females offer less nutritious pollen to pollinators in order to conserve nutrition. Here, we tested this hypothesis in a perennial vine, Actinidia polygama, which bears nectarless flowers. We quantified flower production and measured the dry mass of floral parts as well as carbon and nitrogen concentrations in floral parts and pollen in both sexes. Males produced more flowers per inflorescence and more inflorescences per shoot than females, while the dry mass of each flower was greater in females. The carbon allocation pattern was similar to that of biomass, but nitrogen allocation exhibited a remarkable reduction in sterile stamens and pollen of female flowers. In addition, as sterile pollen of females was sparse, when compared at the same volume, it was lighter than the pollen of males. Sterile pollen produced in female flowers appears to be as voluminous as that of male flowers but extremely poor in nutrients, especially in nitrogen, which clearly suggests that A. polygama females deceive pollen‐collecting pollinators for brood rearing.

Structural anther mimics improve reproductive success through dishonest signaling that enhances both attraction and the morphological fit of pollinators with flowers.

Numerous studies have identified traits associated with anther mimicry; however, the processes underlying floral deception remain poorly documented for these structures. We studied the importance of pollinator attraction and mechanical fit of anther mimics in Tritonia laxifolia (Iridaceae) and their relative contributions to reproductive success. To determine anther mimics role in attraction, we offered bees’ binary choices to flowers painted with UV‐absorbent and UV‐reflecting paints. We also conducted preference experiments between flowers with excised anther mimics and unmanipulated controls, from which mechanical fit was assessed by allowing single visits. Anther mimics’ effects on female reproductive success were determined using similar treatments, but on rooted plants. Bees preferred UV‐absorbent over UV‐reflecting anther mimics. Bees did not discriminate between flowers with and without three‐dimensional anther mimics. Single visits resulted in more pollen deposition on unmanipulated controls over flowers with their anther mimics excised, which was directly linked to pollen‐collecting behavior. Controls with unmanipulated anther mimics had higher seed set than those with their anther mimics excised. This study provides insights into pollinator‐mediated selection on deceptive floral signals and shows that three‐dimensional anther mimics increases reproductive success through both attraction and pollen‐collecting behaviors.

Rotating Arrays of Orchid Flowers: A Simple and Effective Method for Studying Pollination in Food Deceptive Plants

Floral deception has been observed in several genera in angiosperms, but is most common in the Orchidaceae. Pollination mechanisms in food deceptive plants are often difficult to assess, as visitation frequency by insects requires numerous hours of field observations to ascertain. Here, for the first time, we describe in detail and validate a simple and effective method that extends previous approaches to increase the effectiveness of pollination studies of food deceptive orchids. We used an orchid of southwest Australia, Diuris brumalis (Orchidaceae), that visually mimics model plants belonging to the genus Daviesia (Faboideae). Arrays of orchid flowers were placed and moved systematically in proximity to model plants, resulting in rapid attraction of the pollinators of D. brumalis. We compared pollinaria removal (as an indicator of pollination success) in naturally growing orchids with pollinaria removal in arrays of orchid flowers in the same sites. We showed that the proposed method greatly enhances pollinator attractiveness in food deceptive systems with very low pollination rates, and we compared its efficiency with other similar methods. The approach can be used for observing pollinator behavioural patterns and confirming effective pollinators for food deceptive species with low insect visitation rates.

Pollination by sexual deception promotes outcrossing and mate diversity in self-compatible clonal orchids.

The majority of flowering plants rely on animals as pollen vectors. Thus, plant mating systems and pollen dispersal are strongly influenced by pollinator behaviour. In Australian sexually deceptive orchids pollinated by male thynnine wasps, outcrossing and extensive pollen flow is predicted due to floral deception, which minimizes multiple flower visitations within patches, and the movement of pollinators under mate-search rather than foraging behaviours. This hypothesis was tested using microsatellite markers to reconstruct and infer paternity in two clonal, self-compatible orchids. Offspring from naturally pollinated Chiloglottis valida and C.aff. jeanesii were acquired through symbiotic culture of seeds collected over three seasons. In both species, outcrossing was extensive (tm =0.924-1.00) despite clone sizes up to 11m wide. The median pollen flow distance based on paternity for both taxa combined was 14.5m (n=18, range 0-69m), being larger than typically found by paternity analyses in other herbaceous plants. Unexpectedly for orchids, some capsules were sired by more than one father, with an average of 1.35 pollen donors per fruit. This is the first genetic confirmation of polyandry in orchid capsules. Further, we report a possible link between multiple paternity and increased seed fitness. Together, these results demonstrate that deceptive pollination by mate-searching wasps enhances offspring fitness by promoting both outcrossing and within-fruit paternal diversity.

The latest news from biological interactions in orchids: in love, head to toe

The latest news from biological interactions in orchids: in love, head to toe

The evolution of floral deception in Epipactis veratrifolia (Orchidaceae): from indirect defense to pollination

BackgroundIt is estimated that floral deception has evolved in at least 7500 species of angiosperms, of which two thirds are orchids. Epipactis veratrifolia (Orchidaceae) is a model system of aphid mimicry as aphidophagous hoverflies lay eggs on false brood sites on their flowers. To understand the evolutionary ecology of floral deception, we investigated the pollination biology of E. veratrifolia across 10 populations in the Eastern Himalayas. We reconstructed the phylogeny of Epipactis and mapped the known pollination systems of previously studied species onto the tree.ResultsSome inflorescences of E. veratrifolia were so infested with aphids while they were still in bud that the some larvae of hoverflies developed to the third instar while flower buds opened. This indicated that adult female hoverflies were partly rewarded for oviposition. Although flowers failed to secrete nectar, they mimicked both alarm pheromones and aphid coloring of to attract female hoverflies as their exclusive pollinators. Phylogenetic mapping indicate that pollination by aphidophagous hoverflies is likely an ancestral condition in the genus Epipactis. We suggest that the biological interaction of aphid (prey), orchid (primary producer) and hoverfly (predator) may represent an intermediate stage between mutualism and deception in the evolution of pollination-by-deceit in E. veratrifolia.ConclusionsOur analyses indicate that this intermediate stage may be used as a model system to interpret the origin of oviposition (brood site) mimicry in Epipactis. We propose the hypothesis that some deceptive pollination systems evolved directly from earlier (partly) mutualistic systems that maintained the fidelity of the original pollinator(s) even though rewards (nectar/ brood site) were lost.

Ancestral deceit and labile evolution of nectar production in the African orchid genusDisa

An outstanding feature of the orchid family is that approximately 30-40% of the species have non-rewarding flowers and deploy various modes of deception to attract pollinators, whereas the remaining species engage in pollination mutualisms based on provision of floral rewards. Here, we explore the direction, frequency and reversibility of transitions between deceptive and rewarding pollination systems in the radiation of the large African genus Disa, and test whether these transitions had consequences for diversification. By optimizing nectar production data for 111 species on a well-resolved phylogeny, we confirmed that floral deception was the ancestral condition and that nectar production evolved at least nine times and was lost at least once. Transitions to nectar production first occurred ca 17 million years ago but did not significantly affect either speciation or extinction rates. Nectar evolved independently of a spur, which was lost and gained multiple times. These results show that nectar production can be a highly labile trait and highlight the need for further studies of the genetic architecture of nectar production and the selective factors underlying transitions between deception and mutualism.

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.

Mechanisms and evolution of deceptive pollination in orchids

The orchid family is renowned for its enormous diversity of pollination mechanisms and unusually high occurrence of non-rewarding flowers compared to other plant families. The mechanisms of deception in orchids include generalized food deception, food-deceptive floral mimicry, brood-site imitation, shelter imitation, pseudoantagonism, rendezvous attraction and sexual deception. Generalized food deception is the most common mechanism (reported in 38 genera) followed by sexual deception (18 genera). Floral deception in orchids has been intensively studied since Darwin, but the evolution of non-rewarding flowers still presents a major puzzle for evolutionary biology. The two principal hypotheses as to how deception could increase fitness in plants are (i) reallocation of resources associated with reward production to flowering and seed production, and (ii) higher levels of cross-pollination due to pollinators visiting fewer flowers on non-rewarding plants, resulting in more outcrossed progeny and more efficient pollen export. Biologists have also tried to explain why deception is overrepresented in the orchid family. These explanations include: (i) efficient removal and deposition of pollinaria from orchid flowers in a single pollinator visit, thus obviating the need for rewards to entice multiple visits from pollinators; (ii) efficient transport of orchid pollen, thus requiring less reward-induced pollinator constancy; (iii) low-density populations in many orchids, thus limiting the learning of associations of floral phenotypes and rewards by pollinators; (iv) packaging of pollen in pollinaria with limited carry-over from flower to flower, thus increasing the risks of geitonogamous self-pollination when pollinators visit many flowers on rewarding plants. All of these general and orchid-specific hypotheses are difficult to reconcile with the well-established pattern for rewardlessness to result in low pollinator visitation rates and consequently low levels of fruit production. Arguments that deception evolves because rewards are costly are particularly problematic in that small amounts of nectar are unlikely to have a significant effect on the energy budget of orchids, and because reproduction in orchids is often severely pollen-, rather than resource-limited. Several recent experimental studies have shown that deception promotes cross-pollination, but it remains unknown whether actual outcrossing rates are generally higher in deceptive orchids. Our review of the literature shows that there is currently no evidence that deceptive orchids carry higher levels of genetic load (an indirect measure of outcrossing rate) than their rewarding counterparts. Cross-pollination does, however, result in dramatic increases in seed quality in almost all orchids and has the potential to increase pollen export (by reducing pollen discounting). We suggest that floral deception is particularly beneficial, because of its promotion of outcrossing, when pollinators are abundant, but that when pollinators are consistently rare, selection may favour a nectar reward or a shift to autopollination. Given that nectar-rewardlessness is likely to have been the ancestral condition in orchids and yet is evolutionarily labile, more attention will need to be given to explanations as to why deception constitutes an 'evolutionarily stable strategy'.

Lack of floral nectar reduces self-pollination in a fly-pollinated orchid

One explanation for the widespread absence of floral nectar in many orchids is that it causes pollinators to visit fewer flowers on a plant, and thus reduces self-pollination. This, in turn, could increase fitness by reducing inbreeding depression in progeny and promoting pollen export. The few previous investigations of this hypothesis have all involved bee-pollinated orchids and some have given contradictory results. We studied the effects of adding artificial nectar (sucrose solution) to the spurs of a non-rewarding long-proboscid fly-pollinated orchid, Disa pulchra. Addition of nectar significantly increased the number of flowers probed by flies (2.6-fold), the time spent on a flower (5.4-fold), the number of pollinia removed per inflorescence (4.8-fold) and the proportion of removed pollen involved in self-pollination (3.5-fold). The level of self-pollination increased dramatically with the number of flowers probed by flies. Experimental self-pollination resulted in fruits with only half as many viable seeds as those arising from cross-pollination. Pollinators were more likely to fly long distances (>40 cm) when departing from non-rewarding inflorescences than when departing from rewarding ones. These findings provide support for the idea that floral deception serves to reduce pollinator-mediated self-pollination.

Vaccination and the population structure of antigenically diverse pathogens that exchange genetic material.

Populations of antigenically diverse pathogens undergoing genetic exchange may be categorized into strains on the basis of a set of principal protective antigens. The extent to which polyvalent vaccines based on these protective antigens can alter the population structure of the pathogen is determined by the degree of cross-protection between strains. In the case where there is no cross-protection, vaccinating against a particular strain will have no effect on the others. As cross-protection increases, the strains containing the antigenic variants included in the vaccine will be diminished in prevalence, and those that do not will increase in prevalence. The rise in prevalence of the latter will become more and more exaggerated as cross-protection increases. However, beyond a critical level of cross-protection, in the absence of vaccination, the steady state of the system is asymmetric in that a certain subset of strains (with non-overlapping repertoires of antigenic variants) will dominate over the others in terms of prevalence. Under these circumstances, a vaccine consisting of the most immunogenic combinations of antigenic variants can cause a dramatic increase in frequency of a subset of rare strains.

Deceptive pollination of Dactylorhiza incarnata: an experimental test of the magnet species hypothesis

Floral deception, which mainly appears in highly evolved families such as Orchidaceae, was studied in Central Finland. In nectarless Dactylorhiza incarnata, the deceptive pollination system has been considered to function best in remote habitats such as marshes, where flowering plants attractive to pollinators are rare (remote habitats hypothesis). In contrast, the magnet-species theory predicts that a nectarless plant benefits from growing in the vicinity of nectarcontaining species. We tested these hypotheses by adding attractive, nectar-containg violets (Viola x wittrockiana) to orchid populations. The percentage of fruit set in D. incarnata was adversely affected by the violets, probably because interspecific exploitation competition for pollinators took place in favour of the violas at the expense of the orchids. This result gave no support for the magnet-species theory and supported the remote habitats hypothesis.