Deceptive Species Research Articles

Higher seed number compensates for lower fruit set in deceptive orchids

Summary Floral deception is widespread in orchids, with more than one‐third of the species being pollinated this way. The evolutionary success of deceptive orchids is puzzling, as species employing this strategy are thought to have low reproductive success (less flowers yielding fruits) because of low pollination rates. However, direct measurements of total seed production in orchids – which is a better measure of reproductive success – are scarce due to the extremely small size of their seeds. Here, we quantified seed numbers in 1015 fruits belonging to 48 orchid species from the Pannonian ecoregion (central Europe) and obtained fruit set and thousand‐seed weight data for these species from the literature. We used phylogenetic comparative methods to test the hypothesis that deceptive species should compensate for their lower fruit set by having either more flowers, larger seeds or more seeds in a fruit. Similarly to previous studies, we found that deceptive orchids have substantially lower fruits‐set than nectar‐rewarding ones. Also, we found that deceptive species have more seeds in a fruit but not more flowers or larger seeds compared to nectar‐rewarding ones. Based on our results, deceptive species compensate for their lower fruit set by having higher seed numbers per fruit. As a consequence, their seed numbers per shoot do not differ from that of nectar‐rewarding ones. Together with other benefits of deceptive pollination (e.g. lower energy expenditure due to the lack of nectar production and higher genetic variability due to decreased probability of geitonogamous pollination), our results can explain why deceptive strategies are so widespread in the orchid family. Synthesis. Our results indicate that deceptive orchids can compensate for their lower fruit set by having more (but not larger) seeds in a fruit than rewarding species. These findings highlight possible ways in which plants can increase their reproductive success in face of pollinator limitation. We emphasize that fruit set in itself is an inappropriate measure of the reproductive success of orchids – the total number of seeds per shoot is a much better approximation.

– Reduced fecundity and genetic diversity in small populations of rewarding versus deceptive orchid species: a meta-analysis

Background and aims – Understanding how plant traits mediate the relationship between plant population size, fitness and genetic diversity is fundamental to conservation. Many orchid species are threatened, possibly due to their susceptibility to the consequences of habitat fragmentation and the associated decreasing population size. One third of all orchids do not produce nectar to entice pollinators, and this is believed to promote gene flow and outcrossing. Therefore, we hypothesised that deceptive orchids are less susceptible to reductions in population size than rewarding species. Methods – We reviewed the available literature and used traditional and phylogenetically independent meta-analyses to explore relationships between population size, fitness (fruit set) and genetic diversity. Key results – Results showed that orchids in general are highly susceptible to the consequences of small population size. Fruit set significantly decreased in small populations of rewarding, but not in deceptive species. Deceptive orchids were, however, as likely to lose genetic diversity in small populations, even though significantly less genetic differentiation (Fst) was present between populations of deceptive orchids. Finally, we found that homozygosity did not relate with population size, which may indicate a selection process against less fit homozygotes in small orchid populations. Conclusions – We conclude that reductions in population size most likely resulting from habitat loss and fragmentation represent major threats to the population viability of orchids. Fitness of rewarding orchids declines through ecological mechanisms, whereas deceptive orchids may be more susceptible to genetic loss as they are more susceptible to decreased gene flow.

Positive effect of the yellow morph on female reproductive success in the flower colour polymorphic Iris lutescens (Iridaceae), a deceptive species.

The deceptive Iris lutescens (Iridaceae) shows a heritable and striking flower colour polymorphism, with both yellow- and purple-flowered individuals growing sympatrically. Deceptive species with flower colour polymorphism are mainly described in the family Orchidaceae and rarely found in other families. To explain the maintenance of flower colour polymorphism in I.lutescens, we investigated female reproductive success in natural populations of southern France, at both population and local scales (within populations). Female reproductive success was positively correlated with yellow morph frequency, at both the population scale and the local scale. Therefore, we failed to observe negative frequency-dependent selection (NFDS), a mechanism commonly invoked to explain flower colour polymorphism in deceptive plant species. Flower size and local flower density could also affect female reproductive success in natural populations. Pollinator behaviour could explain the positive effect of the yellow morph, and our results suggest that flower colour polymorphism might not persist in I.lutescens, but alternative explanations not linked to pollinator behaviour are discussed. In particular, NFDS, although an appealingly simple explanation previously demonstrated in orchids, may not always contribute to maintaining flower colour polymorphism, even in deceptive species.

Pollen transfer efficiency and its effect on inflorescence size in deceptive pollination strategies.

Pollination systems differ in pollen transfer efficiency, a variable that may influence the evolution of flower number. Here we apply a comparative approach to examine the link between pollen transfer efficiency and the evolution of inflorescence size in food and sexually deceptive orchids. We examined pollination performance in nine food-deceptive, and eight sexually deceptive orchids by recording pollen removal and deposition in the field. We calculated correlations between reproductive success and flower number (as a proxy for resources allocated during reproductive process), and directional selection differentials were estimated on flower number for four species. Results indicate that sexually deceptive species experience decreased pollen loss compared to food-deceptive species. Despite producing fewer flowers, sexually deceptive species attained levels of overall pollination success (through male and female function) similar to food-deceptive species. Furthermore, a positive correlation between flower number and pollination success was observed in food-deceptive species, but this correlation was not detected in sexually deceptive species. Directional selection differentials for flower number were significantly higher in food compared to sexually deceptive species. We suggest that pollination systems with more efficient pollen transfer and no correlation between pollination success and number of flowers produced, such as sexual deception, may allow the production of inflorescences with fewer flowers that permit the plant to allocate fewer resources to floral displays and, at the same time, limit transpiration. This strategy can be particularly important for ecological success in Mediterranean water-deprived habitats, and might explain the high frequency of sexually deceptive species in these specialised ecosystems.

THERE IS MORE TO POLLINATOR-MEDIATED SELECTION THAN POLLEN LIMITATION

Spatial variation in pollinator-mediated selection (Δβpoll ) is a major driver of floral diversification, but we lack a quantitative understanding of its link to pollen limitation (PL) and net selection on floral traits. For 2-5 years, we quantified Δβpoll on floral traits in two populations each of two orchid species differing in PL. In both species, spatiotemporal variation in Δβpoll explained much of the variation in net selection. Selection was consistently stronger and the proportion that was pollinator-mediated was higher in the severely pollen-limited deceptive species than in the rewarding species. Within species, variation in PL could not explain variation in Δβpoll for any trait, indicating that factors influencing the functional relationship between trait variation and pollination success govern a major part of the observed variation in Δβpoll . Separating the effects of variation in mean interaction intensity and in the functional significance of traits will be necessary to understand spatiotemporal variation in selection exerted by the biotic environment.

Presence, distribution and effect of white, pink and purple morphs on pollination in the orchid Orchis mascula

How floral polymorphism of flowering plants can be maintained in evolutionary time has long intrigued ecologists and is still debated. In particular, how floral colour polymorphism influences reproductive success is still poorly understood. Here, we investigated the case of Orchis mascula, a deceptive orchid species in which the presence of rare white-flowered individuals is known to increase the percentage pollination of co-occurring coloured morphs. In a brief review, we report all the orchid species for which rare colour morphs are recorded and show that colour polymorphism occurs in most orchid genera occurring in France. In this study, more than 20,000 individuals of O. mascula were surveyed and some rare clear pink morphs were recorded. The frequencies of white-flowered and clear pink-flowered individuals were 0.59% and 0.28%, respectively. These two rare-colour flowered individuals were not randomly distributed and restricted to a few populations. In addition, the presence of pink-flowered individuals and the use of experimental pink lures resulted in an increase in the percentage pollination of surrounding purple-flowered individuals, as previously shown for white-flowered individuals and white lures. These new observations favour kin selection as the means by which floral colour polymorphism is maintained in this species. We suggest conducting comparative studies of other species in order to evaluate the importance of this mechanism in orchid pollination and that of other plant families.

Exine micromorphology and ultrastructure in Neottieae (Epidendroideae, Orchidaceae)

The diverse epidendroid orchid tribe Neottieae is characterized by multiple transitions between autotrophy and mycoheterotrophy, allogamous and autogamous mating systems, pollen released as tetrads or monads, and pollen exine tectate or semitectate. We use transmission and scanning electron microscopy on pollen of ten species of Neottieae to investigate whether the differences in pollen aggregation and exine micromorphology and ultrastructure reflect phylogenetic relationships, or whether this variation is subject to ecological constraints. Our results showed that differences in exine micromorphology are mostly concordant with phylogenetic relationships in Neottieae, i.e. an ascending tendency of pollen ornamentation from tectate (Cephalanthera) to semitectate (e.g. Neottia). In contrast, pollen aggregation, when plotted on the most recent phylogeny, shows repeated transitions between monads and tetrads that could be related to ecological constraints. Tetrads are present in species that are nectar rewarding, whereas monads are common in deceptive species. Cephalanthera is characterized by recalcitrant pollen, including the frequent occurrence of collapsed pollen. In this genus, the observed shifts from allogamous to autogamous or cleistogamous mating systems could help to reduce pollen damage caused by exposure to dry habitats.

Effects of habitat fragmentation on plant reproductive success and population viability at the landscape and habitat scale

Habitat fragmentation can significantly affect plant reproductive success and ultimately population viability, but little is known about the magnitude, direction or time scale of these impacts on plant–pollinator mutualisms. In this study, four species of terrestrial orchid with specialist and generalist pollination syndromes were used to investigate the effects of fragmentation on capsule set in urban bushland remnants. Supplementary pollination showed pollination limitation, but not resource limitation, occurs across all species. Habitat and landscape scale fragmentation predictor variables were used to build parsimonious models that explained capsule set data collected over 2years. We found the sexually deceptive species, Caladenia arenicola, to be sensitive to interactions between landscape (perimeter to area ratio) and habitat scale (bare ground cover and population size) predictor variables. The effect of perimeter to area ratio was heavily tempered by the significant negative influence of bare ground cover, where values of over 40% bare ground cover resulted in reproductive failure. We found that generalist pollinated species had significant interactions at the habitat scale including significant positive interactions between capsule set and population size and litter cover. Our results suggest the effects of habitat fragmentation at the landscape and habitat scale are important drivers of population viability. Our results suggest population viability will depend on the sensitivity of the pollination syndrome and the pollinator involved. This study highlights the need for research into reproductive success across multiple spatial scales to improve and inform conservation efforts.

Orchis × colemanii hybridization: Molecular and morphological evidence, seed set success, and evolutionary importance

Despite highly specialized pollination strategies, hybridization is a common phenomenon among Mediterranean deceptive orchids. Food-deceptive species sire a progeny of F1 unfertile plants, which work as a late post-zygotic barrier. Conversely, when pre-zygotic barriers of sexually deceptive (Ophrys) species are absent, the hybrids are fertile and an extensive introgression may occur. Here, we have performed molecular analysis and hand pollination treatments to characterize a hybrid zone of two food-deceptive species, O. mascula and O pauciflora. Hybrids (called O.×colemanii) have shown different amounts of parental nrDNA, strongly supporting that they are F2 and/or successive hybrid generations. Comparable high levels of reproductive success have been detected in natural conditions and in experimental crosses suggesting the absence of effective reproductive barriers either between hybrids, either between hybrids and parental species. In light of ecological and distributional features of O.×colemanii across its distribution range, we hypothesize that these populations have originated by secondary contact in the periglacial belt of Apennines. Moreover, the rare and localized O. pauciflora could benefit a genetic enrichment by hybridizing with a widespread related species. O.×colemanii is not a dead end population, but may have a role as potential reserve of adaptive variability and is an unusual stage along the speciation process.

Comparative floral micromorphology in four sympatric species of Serapias (Orchidaceae)

A great variety of colours, shapes, scents, energy-rich rewards and other floral traits form an integrated system that increases pollination efficiency or reduces pollen loss. Flowers lacking energetic rewards possess a more elaborate morphology to ensure co-specific pollination. Despite the prevalence of deceptive species among Euro-Mediterranean orchids, the study of their floral micromorphology is still in its infancy. In this work, we examine the floral micromorphology of four sympatric species of the widespread Mediterranean genus Serapias. Electron microscopy (scanning, transmission) was performed on flowers of four sympatric species of the deceptive genus Serapias, the widespread S. cordigera, S. lingua, S. parviflora and S. vomeracea. Each species has a characteristic combination of specialized, secretory epidermal cells and trichomes on the labellum and, to a lesser extent, the petals. Serapias lingua is highly specialized in that it produces olfactory signals and has two types of trichome with secretory apical cells, one of which is also present in S. parviflora. In addition to striated, conical secretory cells, S. cordigera and S. vomeracea also have characteristic, atypical secretory trichomes with bilobulate or dome-like protuberances. The labellar micromorphology of S. lingua and S. parviflora is adapted for scent production, whereas S. vomeracea and S. cordigera possess trichomes that may also provide visual and/or tactile cues. Owing to the combined effect of the specific floral fragrance and labellar micromorphology in pollinator selection, the pollination ecology of Serapias spp. is even more specialized than previously thought. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 169, 714–724.

Are deception-pollinated species more variable than those offering a reward?

In most pollination systems, animals transfer pollen among plants of a given species. Pollinator visitations do not come without cost, so plants usually offer a reward. However, the flowers of some plant species, mostly orchids, lack rewards and deceive animals into visiting their flowers. Deceptive species are thought to have high levels of variation in traits associated with advertisement and pollinator attraction, which have been attributed to genetic drift, or disruptive selection due to pollinator behavior. Rewarding species are assumed to have less variation due to stabilizing selection. We compared variability in floral morphology and fragrance composition between deceptive and rewarding species. Because both suites of traits are often linked with floral advertisement and pollinator attraction, we expected variation to be greater in species with deceptive pollination systems than in those offering rewards. We obtained floral morphology metrics for 20 deceptive species and 41 rewarding species native or naturalized in Puerto Rico, Venezuela, and Ecuador. Floral fragrances were sampled from eight deceptive species and four rewarding species. We found that the amplitude of variation in floral morphology and fragrance composition covaries significantly. Comparison of coefficients of variation for morphology indicated that, overall, deceptive species show significantly higher variation than rewarding species, and this pattern was also found among just orchids or just nonorchids. There were no statistical differences in morphological variation between orchids and nonorchids within a functional pollination group. Fragrance variation, measured by Jaccard distance, tended to be greater for deceptive species than for rewarding species. Although overlap in measures of variation occurs between the two groups, the data support the hypothesis that populations of deception-pollinated species are more variable than rewarding species in traits associated with pollinator attraction.

Does facilitating pollinator learning impede deceptive orchid attractiveness? A multi-approach test of avoidance learning

It has often been proposed that nectarless deceptive orchid species exploit naïve pollinators in search of food before they learn to avoid their flowers, and that intraspecific floral trait polymorphism, often noted in this plant group, could prolong the time needed for learning, thus increasing orchid reproductive success. We tested the importance of avoidance learning in a European deceptive orchid, Anacamptis morio, which has been reported to have a highly variable fragrance bouquet among individuals. We used an indirect approach, i.e. we facilitated pollinators' ability to learn to avoid A.morio by adding anisaldehyde to selected inflorescences, a scent compound that is easily perceived by the natural pollinators and produced in large quantities by the closely related, nectar producing Anacamptis coriophora, a species that shares pollinator species with A.morio. In a series of three experiments (in artificial arrays, in natural populations and in bumblebee behavioural observations), we consistently found no difference either of reproductive success of or visitation rates to scent-added versus control inflorescences. We also found that the decrease of reproductive success over time in artificial populations of this deceptive species was not as important as expected. Together, these data suggest that pollinators do not fully learn to avoid deceptive inflorescences, and that pollinator avoidance behaviour alone may explain the lower reproductive success usually found in deceptive orchids. We discuss the possible explanations for this pattern in deceptive orchids, particularly in relation to pollinator cognition and learning abilities. Lastly, in light of our results, the potential for higher average reproductive success in deceptive orchids with high phenotypic variability driven by avoidance learning thus appears to be challenged.

Orchid pollination: specialization in chance?

Looking for clues to explain the low rate and unpredictability of the pollination of allogamous, epiphytic orchids in the context of the success of the orchid family in general, we compared the pollination of two miniature twig epiphytes in Mexico: Notylia barkeri, a ‘weedy’, rewarding species, and Erycina crista-galli, a rare, deceptive species. We measured the effects of the spatial organization of the flowers and various parameters of visibility and height above the ground in relation to the spatial organization of the seed capsules (which retrospectively measures the activity of the pollinators). The spatial presentation of the flowers of E. crista-galli explained only 5% of the distribution of the seed capsules. For N. barkeri, with compound flowers, the spatial presentation, considering individual flowers or inflorescences, explained 12% and 45% of the distribution of the seed capsules, respectively, and all other interactions between the variables were insignificant. Both the deceptive and reward strategies resulted in the production of large numbers of seeds despite a low pollination percentage (1–5%). Notylia barkeri produced 11.8 (2005–6) and 53.7 (2007–8) times more seeds in total than E. crista-galli. Furthermore, unlike E. crista-galli, N. barkeri responded to loss of individuals after high winds with an increased production of flowers per plant. We suggest that orchids have evolved to specialize in chance, and instead of maximizing pollinator attraction, they maximize the seed production resulting from every casual encounter. © 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 165, 251–266.

Differences in pollen viability in relation to different deceptive pollination strategies in Mediterranean orchids.

To date, current research involving pollen viability has been evaluated in a relatively low number of orchid species. In the present study, we focused on five related Mediterranean orchid genera (Anacamptis, Orchis, Dactylorhiza, Ophrys and Serapias) that are characterized by different types of deceptive pollination. The in vitro germination ability of increasingly aged pollinaria of eight food-, seven sexually and two shelter-deceptive species was evaluated. Pollination experiments on two food-, one sexually and one shelter-deceptive species were also performed and the percentage of embryonate seeds derived from the increasingly aged pollinaria was checked. All of the examined species showed long-term viabilities (=50 % pollen tube growth) that ranged from 8 to 35 d. Species with the same deceptive pollination strategies exhibited the same pollen viability trends. Interestingly, pollen viabilities of species groups with different deception types have shown significant differences, with sexually and shelter- deceptive species exhibiting a shorter life span than food-deceptive species. This study confirms the prolonged germination and fertilization capacities of orchid pollinaria, and to our knowledge is the first report demonstrating a clear relationship between pollen viability and pollination system. It is proposed that this relationship is attributed to the different types of reproductive barriers, pre- or post-zygotic, that characterize Ophrys and Serapias and the food-deceptive species, respectively.

Does floral trait variability enhance reproductive success in deceptive orchids?

Unusually high intra-specific floral trait variability has often been described within deceptive orchid populations, as opposed to rewarding ones. Such variability is traditionally thought to have consequences on reproduction in this orchid group, i.e. phenotypically variable deceptive species may have a reproductive success advantage compared to those with a constant floral display. The proposed reason for this hypothetic pattern is that floral trait variability decreases pollinator avoidance learning in dealing with nectarless flowers, hence increasing their visitation rate. However, despite an intuitive and appealing hypothesis and a possible mechanism to explain it, the often-cited higher reproductive success induced by floral trait variability still remains unsupported. Here, we review the literature and consider eight studies that have experimentally or correlatively tested this hypothesis in deceptive orchids. In all these experiments, we have found no difference in average reproductive success between populations with high versus low flower trait variability, either in scent variable or colour polymorphic species. We discuss possible explanations for the lack of this pattern including the incapability of pollinators in perceiving the variability, the scarce relevance of polymorphic traits in the choice of species to forage on, or a different pollinator behaviour than the one proposed. We suggest that the high phenotypic variability is not likely to enhance deceptive orchids’ reproductive success, but is more likely to be a consequence of relaxed selection by pollinators. Nonetheless, information regarding orchid pollination strategy or pollinator cognitive abilities is often superficial, hence calling researchers for additional investigations that can contribute to a better understanding of this debated and yet unsupported hypothesis.

Pollinator‐mediated selection on floral display, spur length and flowering phenology in the deceptive orchid Dactylorhiza lapponica

• Nonrewarding animal-pollinated plants commonly experience severe pollen limitation, which should result in strong selection on traits affecting the success of pollination. However, the importance of pollinators as selective agents on floral traits in deceptive species has not been quantified experimentally. • Here, we quantified pollinator-mediated selection (Δβ(poll)) on floral morphology and start of flowering in the deceptive orchid Dactylorhiza lapponica by subtracting estimates of selection gradients for plants receiving supplemental hand-pollination from estimates obtained for open-pollinated control plants. • There was directional selection for taller plants with more flowers and longer spurs, but no statistically significant selection on corolla size or flowering start. Pollinator-mediated selection accounted for all observed selection on spur length (Δβ(poll) = 0.32), 76% of the selection on plant height (Δβ(poll) = 0.19) and 42% of the selection on number of flowers (Δβ(poll = 0.30). Sixteen per cent of developing fruits were consumed by insect herbivores, but fruit herbivory had only minor effects on the strength of pollinator-mediated selection. • Our results demonstrate that pollinators mediate selection on floral traits likely to affect both pollinator attraction and pollination efficiency, and are consistent with the hypothesis that deceptive species experience strong selection for increased display and mechanical fit between flower and pollinator.

Myrmecochorous plants use chemical mimicry to cheat seed‐dispersing ants

Summary 1. Deceptive species are a characteristic trait of insect–plant mutualisms. Deception of pollinators is essential for reproduction in diverse plant species; however, mimicry in seed dispersal is almost unknown. Myrmecochory, the dispersal of diaspores by ants, is a mutualism in which the elaiosome, a lipid‐rich seed appendage, works as an ant reward. This coevolved interaction may be exploited by cheating, non‐rewarding diaspores that mimic elaiosomes. 2. Our study assesses the impact of the morphology and fatty acid composition of diaspores on ant dispersal in rewarding and cheating myrmecochores and non‐myrmecochorous species. Four elaiosome types (defined by Sernander 1906) were included in our research: the ‘Viola odorata type’, with a clearly defined elaiosome, the similar but diplochorous ‘Euphorbia type’ with an additional ballistic dispersal of diaspores, and the ‘Puschkinia’ and ‘Hepatica’ types, which we classify as ‘cheaters’ as they mimic ant rewards by chemical cues. 3. We tested the influence of morphology, chemical composition of diaspores and presence of rewards on removal rates of diaspores, dummies impregnated with seed extracts and pure fatty acids and scent‐standardized diaspores in a population of Formica polyctena ants with 10 European spring ephemerals, mostly Ranunculaceae. The main free fatty acids of diaspores were identified by gas chromatography and mass spectrometric analysis. 4. Removal rates of diaspores and dummies treated with seed extracts were significantly influenced by their fatty acid composition. Discriminant function analysis confirmed oleic acid as the main trigger substance eliciting seed‐removal behaviour by ants in most species. Oleic acid content and removal rates differed among elaiosome types and were highest in rewarding myrmecochores, lower in cheaters and smallest in non‐myrmecochorous seeds. Removal rates of scent‐standardized diaspores did not differ among mutualists and cheaters suggesting a selective pressure for morphological adaptation and were lowest in non‐myrmecochorous species, thus corroborating an influence of diaspore morphology on ant‐removal patterns. 5. For the first time, we demonstrate chemical mimicry in myrmecochory as a means of seed dispersal. Evolutionary stability of the ant–seed mutualism is maintained by the ability of ants to discriminate between certain types of rewards and to respond with differential diaspore distribution rates.

Orchid pollination by sexual deception: pollinator perspectives

The extraordinary taxonomic and morphological diversity of orchids is accompanied by a remarkable range of pollinators and pollination systems. Sexually deceptive orchids are adapted to attract specific male insects that are fooled into attempting to mate with orchid flowers and inadvertently acting as pollinators. This review summarises current knowledge, explores new hypotheses in the literature, and introduces some new approaches to understanding sexual deception from the perspective of the duped pollinator. Four main topics are addressed: (1) global patterns in sexual deception, (2) pollinator identities, mating systems and behaviours, (3) pollinator perception of orchid deceptive signals, and (4) the evolutionary implications of pollinator responses to orchid deception, including potential costs imposed on pollinators by orchids. A global list of known and putative sexually deceptive orchids and their pollinators is provided and methods for incorporating pollinator perspectives into sexual deception research are provided and reviewed. At present, almost all known sexually deceptive orchid taxa are from Australia or Europe. A few sexually deceptive species and genera are reported for New Zealand and South Africa. In Central and Southern America, Asia, and the Pacific many more species are likely to be identified in the future. Despite the great diversity of sexually deceptive orchid genera in Australia, pollination rates reported in the literature are similar between Australian and European species. The typical pollinator of a sexually deceptive orchid is a male insect of a species that is polygynous, monandrous, haplodiploid, and solitary rather than social. Insect behaviours involved in the pollination of sexually deceptive orchids include pre-copulatory gripping of flowers, brief entrapment, mating, and very rarely, ejaculation. Pollinator behaviour varies within and among pollinator species. Deception involving orchid mimicry of insect scent signals is becoming well understood for some species, but visual and tactile signals such as colour, shape, and texture remain neglected. Experimental manipulations that test for function, multi-signal interactions, and pollinator perception of these signals are required. Furthermore, other forms of deception such as exploitation of pollinator sensory biases or mating preferences merit more comprehensive investigation. Application of molecular techniques adapted from model plants and animals is likely to deliver new insights into orchid signalling, and pollinator perception and behaviour. There is little current evidence that sexual deception drives any species-level selection on pollinators. Pollinators do learn to avoid deceptive orchids and their locations, but this is not necessarily a response specific to orchids. Even in systems where evidence suggests that orchids do interfere with pollinator mating opportunities, considerable further research is required to determine whether this is sufficient to impose selection on pollinators or generate antagonistic coevolution or an arms race between orchids and their pollinators. Botanists, taxonomists and chemical ecologists have made remarkable progress in the study of deceptive orchid pollination. Further complementary investigations from entomology and behavioural ecology perspectives should prove fascinating and engender a more complete understanding of the evolution and maintenance of such enigmatic plant-animal interactions.

Pollination Efficiency and the Evolution of Specialized Deceptive Pollination Systems

The ultimate causes of evolution of highly specialized pollination systems are little understood. We investigated the relationship between specialization and pollination efficiency, defined as the proportion of pollinated flowers relative to those that experienced pollen removal, using orchids with different pollination strategies as a model system. Rewarding orchids showed the highest pollination efficiency. Sexually deceptive orchids had comparably high pollination efficiency, but food-deceptive orchids had significantly lower efficiency. Values for pollinator sharing (a measure of the degree of generalization in pollination systems) showed the reverse pattern, in that groups with high pollination efficiency had low values of pollinator sharing. Low pollinator sharing may thus be the basis for efficient pollination. Population genetic data indicated that both food- and sexually deceptive species have higher degrees of among-population gene flow than do rewarding orchids. Thus, the shift from food to sexual deception may be driven by selection for more efficient pollination, without compromising the high levels of gene flow that are characteristic of deceptive species.

Pollinator attraction in Anacamptis papilionacea (Orchidaceae): a food or a sex promise?

AbstractThe Mediterranean orchid Anacamptis papilionacea, despite showing a typical food‐deceptive floral display, has also been reported to frequently attract male pollinators, suggesting a potentiality for sexual attraction. In a survey from a southern Italian population of A. papilionacea and their hybrids with Anacamptis morio, we collected 37 pollinators belonging to five bee species carrying 126 orchid pollinia. The main pollinator of A. papilionacea was Anthophora crinipes male (48.6%), but the number of females was not negligible (22.9%). We also found pollinator sharing between the hybrid and the parental species. Our findings confirm that, contrary to other food‐deceptive species, A. papilionacea mainly attracts male insects, but also that, in contrast to sexually deceptive species, this attraction is not specific. We suggest that A. papilionacea adopts a complex mix of food and sexually deceptive pollination and could represent a helpful model for studying the transition between different pollination strategies.