兰科植物欺骗性传粉

植物与传粉动物的互利关系在生态系统中非常普遍。然而,有许多植物不为传粉者提供任何报酬,而是利用各种欺骗方式诱骗昆虫拜访,从而实现传粉,即欺骗性传粉。兰科是被子植物大科之一,其高度特化的繁殖器官和适应于昆虫传粉的精巧结构令人称奇。进化论创始人达尔文描述了许多兰花与昆虫精巧的传粉系统,但他忽视了欺骗性传粉的存在。事实上,近1/3的兰科植物都依赖于欺骗性传粉。欺骗性传粉可能是导致兰科植物多样性的重要原因之一。兰花利用或操作昆虫觅食、交配、产卵和栖息等行为,演化出各种各样的欺骗性传粉机制,常见的类型包括泛化的食源性欺骗、Batesian拟态、性欺骗、产卵地拟态和栖息地拟态。花的颜色、形态和气味在欺骗性传粉的成功实现中起到了重要作用。欺骗性兰花与传粉昆虫之间的演化可能是不同步的,兰花追踪昆虫的行为信号而发生分化,然而欺骗性传粉可能对昆虫造成一定的伤害,从而对昆虫也施加选择压力。由于昆虫的学习行为,欺骗性的兰花一般具有低的昆虫拜访率和结实率,其繁殖成功率受各种因素的影响。欺骗性加剧了兰花对传粉昆虫的依赖,使其具有更高的灭绝风险,传粉生物学的研究能为兰科植物的有效保护提供指导。在欺骗性传粉系统中,有报酬的伴生植物、拟态模型和其他拟态信号提供者对传粉成功有重要影响。因此,研究欺骗性传粉兰花、传粉昆虫和相关的生物和生态因子的网状进化关系具有重要理论和实践意义。     

A specialised pollination system using nectar‐seeking thynnine wasps in Caladenia nobilis (Orchidaceae)

• Caladenia is a diverse Australian genus that is exceptional among orchids in having both species pollinated by food‐seeking and sexually deceived insects. Here, we investigated the pollination of Caladenia nobilis, a species predicted to be food‐deceptive due to its large, cream‐coloured and apparently nectarless flowers.
• Pollinator observations were made using experimental clumps of flowers. Measurements of floral colour were undertaken with a spectrometer, nectar was tested using GC‐MS, and reproductive success was quantified for 2 years.
• While C. nobilis attracted nine species of insect, only males of the thynnine wasp Rhagigaster discrepans exhibited the correct size and behaviour to remove and deposit pollen. Male R. discrepans attempted to feed from the surface of the labellum, often crawling to multiple flowers, but showed no evidence of sexual attraction. Most flowers produced little or no nectar, although some may provide enough sucrose to act as a meagre reward to pollinators. Floral colouration was similar to a related Caladenia species pollinated by sexual deception, although the sexually deceptive species had a dull‐red labellum. Reproductive success was generally low and highly variable between sites and years.
• In addition to most visitors being of inappropriate size for pollinia removal, the lack of response to the orchid by several co‐occurring species of thynnine wasp suggests filtering of potential pollinators at the attraction phase. Our discovery of a pollination strategy that may be intermediate between food deception and food reward raises the question, how many putatively rewardless orchids actually produce meagre amounts of nectar?

     

Behaviour of sexually deceived ichneumonid wasps and its implications for pollination in Cryptostylis (Orchidaceae)

Pollination via sexual deception is hypothesised to be associated with more frequent outcrossing and greater pollen dispersal distances than strategies involving food‐foraging behaviour. In this study, we investigated the behaviour and movement distances of Lissopimpla excelsa (Hymenoptera: Ichneumonidae), and their implications for the pollination of the sexually deceptive Cryptostylis ovata (Orchidaceae). Pollinator observations revealed that while L. excelsa will alight on multiple flowers within a single visit to a patch of orchids, the frequency of attempted copulation decreases with successive visits, suggesting that pollinator learning may inhibit within‐patch pollen transfer. Mark‐recapture demonstrated that 25% of wasps revisited inflorescences within a day and 50% revisited within a week. Despite the apparent site fidelity of some individuals, L. excelsa often move over large distances (maximum = 625 m), and are capable of dispersing pollen between patches. To resolve the consequences of pollination by sexual deception of ichneumonids, we compared our results with those from studies of other sexually deceptive systems. While pollination rates were comparable with other sexually deceptive orchids, L. excelsa showed high rates of column contact and moved over large distances relative to other sexually deceived pollinators. Among sexually deceptive orchids in general, the frequency of column contact was not correlated either with the frequency of pseudocopulation or with pollination rate. These results suggest that the consequences of pollination by sexual deception may vary extensively between plant taxa due to variation in floral traits, and behavioural differences between pollinator groups.     

Phenotype–fitness relationships and pollen-transfer efficiency of five orchid species with different pollination strategies

Premise

Deceptive pollination, a fascinating mechanism that independently originated in several plant families for benefiting from pollinators without providing any reward, is particularly widespread among orchids. Pollination efficiency is crucial in orchids due to the aggregated pollen in a pollinarium, which facilitates pollen transfer and promotes cross-pollination as pollinators leave after being deceived.

Methods

In this study, we compiled data on reproductive ecology from five orchid species with different pollination strategies: three deceptive-strategy species (shelter imitation, food deception, sexual deception), one nectar-rewarding species, and one shelter-imitation but spontaneously selfing species. We aimed to compare the reproductive success (female fitness: fruit set; male fitness: pollinarium removal) and pollination efficiency of species representing these strategies. We also investigated pollen limitation and inbreeding depression among the pollination strategies.

Results

Male and female fitness were strongly correlated in all species but the spontaneously selfing species, which had high fruit set and low pollinarium removal. As expected, pollination efficiency was highest for the rewarding species and the sexually deceptive species. Rewarding species had no pollen limitation but did have high cumulative inbreeding depression; deceptive species had high pollen limitation and moderate inbreeding depression; and spontaneously selfing species did not have pollen limitation or inbreeding depression.

Conclusions

Pollinator response to deception is critical to maintain reproductive success and avoid inbreeding in orchid species with non-rewarding pollination strategies. Our findings contribute to a better understanding of the trade-offs associated with different pollination strategies in orchids and highlight the importance of pollination efficiency in orchids due to the pollinarium.

     

ECOLOGICAL AND GENETIC CONSEQUENCES OF POLLINATION BY SEXUAL DECEPTION IN THE ORCHID CALADENIA TENTACTULATA

Only orchids affect pollination by the deceptive sexual attraction of male insects, a syndrome particularly well developed in Australia. We examined the ecological and genetic consequences of exclusive pollination by sexually attracted male thynnine wasps in the orchid Caladenia tentaculata. Male wasps respond rapidly to flowers artificially presented in 1 × 1 m² experimental patches. Sixty of 287 wasps approached within centimeters of the flower, but did not land. Of the remaining 79% who made floral contact, only 7.5% attempted copulation, the step critical for pollination. Wasps only rarely moved among patches (19% of flights) and none attempted copulation a second time, resembling observations in natural populations. We confirmed outcrossing and long distance pollen flow by monitoring how colored pollen moved in natural populations. Pollen movements approximated a linear rather than a leptokurtic distribution (mean distance: 17 m; maximum: 58 m). Pollinator visits varied independently of flower density in three of four populations with most solitary flowers being visited. Allozyme analysis revealed within-population fixation indices (F) close to zero and low levels of differentiation (FST) among populations. Despite behavioral evidence for long distance pollen flow, significant local genetic structure exists, perhaps reflecting restricted seed dispersal. Long distance pollen flow in C. tentaculata may therefore promote outbreeding by minimizing pollen transfers among related neighbors. Although this species is self-compatible, outcrossed progeny develop significantly faster than selfed progeny. Effective pollination at low flower densities could accentuate this advantage. The data are consistent with the predictions that deceptive pollination will result in long distance pollen flow, which may be of selective advantage at low density. Comparative studies of how food reward, food deceptive, and sexual deceptive pollination systems vary within a phylogenetic framework could further illuminate the evolution of sexual deception.     

Effects of individual and population parameters on reproductive success in three sexually deceptive orchid species

Reproductive success (RS) in orchids in general, and in non-rewarding species specifically, is extremely low. RS is pollinator and pollination limited in food deceptive orchids, but this has rarely been studied in sexually deceptive orchid species. Here, we tested the effects of several individual (plant height, inflorescence size, nearest neighbour distance and flower position) and population (patch geometry, population density and size) parameters on RS in three sexually deceptive Ophrys (Orchidaceae) species. Inter-specific differences were observed in RS of flowers situated in the upper versus the lower part of the inflorescence, likely due to species-specific pollinator behaviour. For all three species examined, RS increased with increasing plant height, inflorescence size and nearest neighbour distance. RS generally increased with decreasing population density and increasing patch elongation. Given these results, we postulate that pollinator availability, rather than pollinator learning, is the most limiting factor in successful reproduction for sexually deceptive orchids. Our results also suggest that olfactory 'display' ( i.e. versus optical display), in terms of inflorescence size (and co-varying plant height), plays a key role in individual RS of sexually deceptive orchids. In this regard, several hypotheses are suggested and discussed.     

Looks matter: changes in flower form affect pollination effectiveness in a sexually deceptive orchid

Many species of the sexually deceptive genus Ophrys are characterized by insect‐like flowers. Their form has been traditionally considered to play an important role in pollinator attraction and manipulation. Yet, the evolution of the floral form remains insufficiently understood. We hypothesize that pollinator‐mediated selection is essential for driving floral form evolution in Ophrys, but that form components are being subjected to varying selection pressures depending on their role in mediating interactions with pollinators. By using the Eucera‐pollinated Ophrys leochroma as a model, our aim has been to assess whether and in what manner pollination effectiveness is altered by experimental manipulation of the flower form. Our results show that floral form plays an essential and, so far, underestimated role in ensuring effective pollination by mechanically guiding pollinators towards the reproductive structures of the flower. Pollinators are significantly less effective in interacting with flowers having forms altered to resemble those of species pollinated by different hymenopteran genera. Further, those components used by pollinators as gripping points were found to be more effective in ensuring pollinia transfer than those with which pollinators do not directly interact. Thus, mechanically active and inactive components appear to be under different selection pressures. As a consequence, mechanically active components of the flower form could reflect adaptations to the interaction with particular pollinator groups, whereas mechanically inactive components can vary more freely. Disentangling selection patterns between the functionally different components of flower form may provide valuable insights into the mechanisms driving the morphological diversification of sexually deceptive pollination systems.     

Male mate‐seeking and mating behaviors of Eucera nipponensis (Hymenoptera: Apidae) at a nectarless orchid habitat: Are empty flower patches a profitable rendezvous site?

Male solitary bees typically use emergence‐nesting areas and/or flower patches of food plants, where receptive females are relatively numerous, as rendezvous sites. However, mate‐seeking males have been also observed at food‐deceptive orchid patches, where numerous encounters with foraging females can hardly be expected, owing to the lack of floral rewards. Here, we describe the male mate‐seeking and mating behaviors of the Japanese long‐horned bee Eucera nipponensis at habitats of the food‐deceptive orchid Cymbidium goeringii. On the basis of the results, we report empty flower patches are not necessarily fruitless sites for mate‐seeking males because naive female bees, which are highly likely to be recently emerged and unmated, can be attracted to non‐rewarding orchids. We also suggest a possibility that a small number of the males could receive a “sexual reward” (i.e. mating opportunities), owing to the food‐deceptive orchid, in return for their pollination work. This occasional interaction could represent the initial stage in the evolution of sexually deceptive orchids from food‐deceptive orchids.     

Patterns of reproductive isolation in Mediterranean deceptive orchids

The evolution of reproductive isolation is of central interest in evolutionary biology. In plants, this is typically achieved by a combination of pre- and postpollination mechanisms that prevent, or limit, the amount of interspecific gene flow. Here, we investigated and compared two ecologically defined groups of Mediterranean orchids that differ in pollination biology and pollinator specificity: sexually deceptive orchids versus food-deceptive orchids. We used experimental crosses to assess the strength of postmating prezygotic, and postzygotic reproductive isolation, and a phylogenetic framework to determine their relative rates of evolution. We found quantitative and qualitative differences between the two groups. Food-deceptive orchids have weak premating isolation but strong postmating isolation, whereas the converse situation characterizes sexually deceptive orchids. Only postzygotic reproductive isolation among food-deceptive orchids was found to evolve in a clock-like manner. Comparison of evolutionary rates, within a common interval of genetic distance, showed that the contribution of postmating barriers was more relevant in the food-deceptive species than in the sexually deceptive species. Asymmetry in prezygotic isolation was found among food-deceptive species. Our results indicate that postmating barriers are most important for reproductive isolation in food-deceptive orchids, whereas premating barriers are most important in sexually deceptive orchids. The different rate of evolution of reproductive isolation and the relative strength of pre- and postmating barriers may have implication for speciation processes in the two orchid groups.     

Female and male fitness of a sexually deceptive orchid with a narrow distribution area: from phenotypic traits to spatial distribution patterns

• The Orchidaceae family presents one of the most extravagant pollination mechanisms: deception. While many studies on reproductive success have been performed on food‐deception orchids, less have been performed on sexually deceptive orchids. Here, we focused on Ophrys balearica P. Delforge, an endemic orchid of the Balearic Islands, to study its reproductive ecology, the spatio‐temporal variation of its reproductive success and the individual (floral display and geospatial position) and population parameters (patch size, shape and density) that affect its reproductive success.
• We performed hand‐pollination experiments, along with the recording of floral display parameters and GPS position of over 1,100 individuals from seven populations in two consecutive years. We applied, for the first time, GIS tools to analyse the effects of individual’s position within the population on the reproductive success. Reproductive success was measured both in male (removed pollinia) and female (fruit set) fitness.
• The results confirm that this species is pollinator‐dependent and mostly allogamous, but also self‐compatible. This species showed high values for the cumulative inbreeding depression index and high pollen limitation. Male fitness was almost equal to female fitness between years and populations, and reproductive success exhibited huge spatio‐temporal variation.
• Although we did not find strong correlations between floral display and reproductive success, patches with low‐plant density and individuals in the external portion of the population showed significantly higher plant fitness. These findings must be considered in conservation actions for endangered orchid species, especially considering that most orchids are strongly dependent on pollinators for their species’ fitness.

     

Chemical ecology and pollinator-driven speciation in sexually deceptive orchids

Sexually deceptive orchids mimic females of their pollinator species to attract male insects for pollination. Pollination by sexual deception has independently evolved in European, Australian, South African, and South American orchid taxa. Reproductive isolation is mainly based on pre-mating isolation barriers, the specific attraction of males of a single pollinator species, mostly bees, by mimicking the female species-specific sex-pheromone. However, in rare cases post-mating barriers have been found. Sexually deceptive orchids are ideal candidates for studies of sympatric speciation, because key adaptive traits such as the pollinator-attracting scent are associated with their reproductive success and with pre-mating isolation.During the last two decades several investigations studied processes of ecological speciation in sexually deceptive orchids of Europe and Australia. Using various methods like behavioural experiments, chemical, electrophysiological, and population-genetic analyses it was shown that minor changes in floral odour bouquets might be the driving force for pollinator shifts and speciation events. New pollinators act as an isolation barrier towards other sympatrically occurring species. Hybridization occurs because of similar odour bouquets of species and the overlap of flowering periods. Hybrid speciation can also lead to the displacement of species by the hybrid population, if its reproductive success is higher than that in the parental species.     

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'.     

Pollen limitation and fruiting failure related to canopy closure in Calypso bulbosa (Orchidaceae), a northern food‐deceptive orchid with a single flower

Natural fruit set is constrained by pollen limitation and fruiting failure, and pollen limitation is expected to be especially severe in deceptive orchids. We performed hand cross‐pollinations in ten populations of a food‐deceptive orchid, Calypso bulbosa, under sparse and dense canopies in three non‐consecutive years. We explored the relationships between natural fruit set, pollen limitation and fruiting failure. Mean natural fruit set over the years was 60%, which is exceptionally high for a deceptive orchid. On average, hand cross‐pollination increased fruit set by 23%. Among open‐pollinated plants that did not set a fruit, 55.5% were estimated to be pollen limited and 44.5% to be limited by fruiting failure, i.e. inability to set a fruit after pollination. In species with high natural fruit set, hand cross‐pollination experiments may not always detect statistically significant pollen limitation. In our case, pollen limitation tended to become significant when the natural fruit set dropped below 60%. Canopy cover had a significant effect on fruiting failure, which was more severe under a dense canopy. Although our results demonstrate pollen limitation in many cases, they also highlight the fact that food deception can be a very effective pollination strategy. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013 , 171 , 744–750.     

Effect of floral display on reproductive success in terrestrial orchids

Almost one-third of all species in the familyOrchidaceae offer no reward to insect pollinators. In the absence of a reward, floral display (number of flowers), may be the most important component of insect attraction but the role of floral display in capsule production of both deceptive (nectarless) and rewarding (nectariferous) orchids has not yet been satisfactorily explored. Based on our theoretical considerations, we propose and test here the following hypotheses: (i) deceptive species flower earlier than rewarding ones, (ii) reproductive success in deceptive species is lower than that in rewarding ones, (iii) reproductive success is independent of the number of flowers in the inflorescence in both deceptive and rewarding orchids. Our data supported hypotheses (i) and (ii). In 9 out of our 12 populations of deceptive species and in 10 out of 12 populations of rewarding species we found support for our hypothesis (iii).     

Review. Specificity in pollination and consequences for postmating reproductive isolation in deceptive Mediterranean orchids

The type of reproductive isolation prevalent in the initial stages of species divergence can affect the nature and rate of emergence of additional reproductive barriers that subsequently strengthen isolation between species. Different groups of Mediterranean deceptive orchids are characterized by different levels of pollinator specificity. Whereas food-deceptive orchid species show weak pollinator specificity, the sexually deceptive Ophrys species display a more specialized pollination strategy. Comparative analyses reveal that orchids with high pollinator specificity mostly rely on premating reproductive barriers and have very little postmating isolation. In this group, a shift to a novel pollinator achieved by modifying the odour bouquet may represent the main isolation mechanism involved in speciation. By contrast, orchids with weak premating isolation, such as generalized food-deceptive orchids, show strong evidence for intrinsic postmating reproductive barriers, particularly for late-acting postzygotic barriers such as hybrid sterility. In such species, chromosomal differences may have played a key role in species isolation, although strong postmating-prezygotic isolation has also evolved in these orchids. Molecular analyses of hybrid zones indicate that the types and strength of reproductive barriers in deceptive orchids with contrasting premating isolation mechanisms directly affect the rate and evolutionary consequences of hybridization and the nature of species differentiation.     

Genic rather than genome‐wide differences between sexually deceptive Ophrys orchids with different pollinators

High pollinator specificity and the potential for simple genetic changes to affect pollinator attraction make sexually deceptive orchids an ideal system for the study of ecological speciation, in which change of flower odour is likely important. This study surveys reproductive barriers and differences in floral phenotypes in a group of four closely related, coflowering sympatric Ophrys species and uses a genotyping‐by‐sequencing (GBS) approach to obtain information on the proportion of the genome that is differentiated between species. Ophrys species were found to effectively lack postpollination barriers, but are strongly isolated by their different pollinators (floral isolation) and, to a smaller extent, by shifts in flowering time (temporal isolation). Although flower morphology and perhaps labellum coloration may contribute to floral isolation, reproductive barriers may largely be due to differences in flower odour chemistry. GBS revealed shared polymorphism throughout the Ophrys genome, with very little population structure between species. Genome scans for F_ST outliers identified few markers that are highly differentiated between species and repeatable in several populations. These genome scans also revealed highly differentiated polymorphisms in genes with putative involvement in floral odour production, including a previously identified candidate gene thought to be involved in the biosynthesis of pseudo‐pheromones by the orchid flowers. Taken together, these data suggest that ecological speciation associated with different pollinators in sexually deceptive orchids has a genic rather than a genomic basis, placing these species at an early phase of genomic divergence within the ‘speciation continuum’.     

Ecological interactions of the sexually deceptive orchid Orchis galilaea

Plant species dependent on highly specific interactions with pollinators are vulnerable to environmental change. Conservation strategies therefore require a detailed understanding of pollination ecology. This two-year study examined the interactions between the sexually deceptive orchid, Orchis galilaea, and its pollinator Lasioglossum marginatum. Relationships were investigated across three different habitats known to support O. galilaea (garrigue, oak woodland, and mixed oak/pine woodland) in Lebanon. Visitation rates to flowers were extremely low and restricted to male bees. The reproductive success of O. galilaea under ambient conditions was 29.3% (±2.4), compared to 89.0% (±2.1) in plants receiving cross-pollination by hand. No difference in reproductive success was found between habitat types, but values of reproductive success were positively correlated to the abundance of male bees. Pollination limitation can have negative impacts on the population growth of orchids, and this study provides clear evidence for more holistic approaches to habitat conservation to support specific interactions.     

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 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 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.