Florivory indirectly decreases the plant reproductive output through changes in pollinator attraction

Species often interact indirectly with each other via their traits. There is increasing appreciation of trait‐mediated indirect effects linking multiple interactions. Flowers interact with both pollinators and floral herbivores, and the flower‐pollinator interaction may be modified by indirect effects of floral herbivores (i.e., florivores) on flower traits such as flower size attracting pollinators. To explore whether flower size affects the flower‐pollinator interaction, we used Eurya japonica flowers. We examined whether artificial florivory decreased fruit and seed production, and also whether flower size affected florivory and the number of floral visitors. The petal removal treatment (i.e., artificial florivory) showed approximately 50% reduction in both fruit and seed set in natural pollination but not in artificial pollination. Furthermore, flower size increased the number of floral visitors, although it did not affect the frequency of florivory. Our results demonstrate that petal removal indirectly decreased 75% of female reproductive output via decreased flower visits by pollinators and that flower size mediated indirect interactions between florivory and floral visitors.     

A bee’s eye view of remarkable floral colour patterns in the south-west Australian biodiversity hotspot revealed by false colour photography

Background and AimsColour pattern is a key cue of bee attraction selectively driving the appeal of pollinators. It comprises the main colour of the flower with extra fine patterns, indicating a reward focal point such as nectar, nectaries, pollen, stamens and floral guides. Such advertising of floral traits guides visitation by the insects, ensuring precision in pollen gathering and deposition. The study, focused in the Southwest Australian Floristic Region, aimed to spot bee colour patterns that are usual and unusual, missing, accomplished by mimicry of pollen and anthers, and overlapping between mimic-model species in floral mimicry cases.MethodsFloral colour patterns were examined by false colour photography in 55 flower species of multiple highly diverse natural plant communities in south-west Australia. False colour photography is a method to transform a UV photograph and a colour photograph into a false colour photograph based on the trichromatic vision of bees. This method is particularly effective for rapid screening of large numbers of flowers for the presence of fine-scale bee-sensitive structures and surface roughness that are not detectable using standard spectrophotometry.Key ResultsBee- and bird-pollinated flowers showed the expected but also some remarkable and unusual previously undetected floral colour pattern syndromes. Typical colour patterns include cases of pollen and flower mimicry and UV-absorbing targets. Among the atypical floral colour patterns are unusual white and UV-reflecting flowers of bee-pollinated plants, bicoloured floral guides, consistently occurring in Fabaceae spp., and flowers displaying a selective attractiveness to birds only. In the orchid genera (Diuris and Thelymitra) that employ floral mimicry of model species, we revealed a surprising mimicry phenomenon of anthers mimicked in turn by model species.ConclusionThe study demonstrates the applicability of ‘bee view’ colour imaging for deciphering pollinator cues in a biodiverse flora with potential to be applied to other eco regions. The technique provides an exciting opportunity for indexing floral traits on a biome scale to establish pollination drivers of ecological and evolutionary relevance.     

Floral antagonists counteract pollinator‐mediated selection on attractiveness traits in the hummingbird‐pollinated Collaea cipoensis (Fabaceae)

Pollinator‐mediated selection toward larger and abundant flowers is common in naturally pollen‐limited populations. However, floral antagonists may counteract this effect, maintaining smaller‐ and few‐flowered individuals within populations. We quantified pollinator and antagonist visit rates and determined a multiplicative female fitness component from attacked and non‐attacked flowers of the Brazilian hummingbird‐pollinated shrub Collaea cipoensis to determine the selective effects of pollinators and floral antagonists on flower size and number. We predicted that floral antagonists reduce the female fitness component and thus exert negative selective pressures on flower size and number, counteracting the positive effects of pollinators. Pollinators, mainly hummingbirds, comprised 4% of total floral visitation, whereas antagonist ants and bees accounted for 90% of visitation. Nectar‐robbers involved about 99% of floral antagonist visit rates, whereas florivores comprised the remaining 1%. Larger and abundant flowers increased both pollinator and antagonist visit rates and the female fitness component significantly decreased in flowers attacked by nectar‐robbers and florivores in comparison to non‐attacked flowers. We detected that pollinators favored larger‐ and many‐flowered individuals, whereas floral antagonists exerted negative selection on flower size and number. This study confirms that floral antagonists reduce female plant fitness and this pattern directly exerts negative selective pressures on flower size and number, counteracting pollinator‐mediated selection on floral attractiveness traits.     

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.

     

Functional differentiation in pollination processes among floral traits in Serapias species (Orchidaceae)

Floral displays, influencing attractiveness to insects, increase the number of pollinator visits and the efficiency of each visit in terms of pollen exchange and thus affect the plant reproductive success. Here, we conducted an in situ manipulation experiment to investigate whether the floral modifications affect reproductive success in natural orchid populations of Serapias lingua and Serapias vomeracea. We estimated male and female reproductive success of three treatment groups, disassembly of floral tube, cutting of lip, and painting of the callus surface, in terms of pollinaria removed/deposited and fruit production. Results revealed that phenotypic modification had opposite effects on reproductive success of two examine species. Indeed, reproductive success was significantly increased by the detached of the petals and sepals, and decreased, due to callus painting and lip removal, in S. lingua. On the contrary, unmanipulated plants of S. vomeracea showed significantly higher value of pollinaria removed and deposited and fruit set than manipulated ones. The differences between S. lingua and S. vomeracea agree to the different pollination strategy of examined species. S. vomeracea shows shelter imitation strategy, and thus, the disassembly of tunnel‐like corolla does not allow the insects to use the flower as a refuge, while S. lingua is a sexually deceptive orchid and therefore the opening of the flower made more visible callus (visible at a greater distance) increasing the pollinators attraction. This study provides evidence that pollinators were largely sensitive to the experimental modification of the flower phenotype, which is consistent with the presence of significant selection on individual floral characters. Our experimental investigations of the effects of variation in display on pollinator visitation provide insights into the evolution of floral morphology in orchid with shelter imitation strategy.     

On the roles of colour and scent in a specialized floral mimicry system

Background and Aims

Sexually deceptive orchids achieve cross-pollination by mimicking the mating signals of female insects, generally hymenopterans. This pollination mechanism is often highly specific as it is based primarily on the mimicry of mating signals, especially the female sex pheromones of the targeted pollinator. Like many deceptive orchids, the Mediterranean species Ophrys arachnitiformis shows high levels of floral trait variation, especially in the colour of the perianth, which is either green or white/pinkinsh within populations. The adaptive significance of perianth colour polymorphism and its influence on pollinator visitation rates in sexually deceptive orchids remain obscure.

Methods

The relative importance of floral scent versus perianth colour in pollinator attraction in this orchid pollinator mimicry system was evaluated by performing floral scent analyses by gas chromatography-mass spectrometry (GC-MS) and behavioural bioassays with the pollinators under natural conditions were performed.

Key Results

The relative and absolute amounts of behaviourally active compounds are identical in the two colour morphs of O. arachnitiformis. Neither presence/absence nor the colour of the perianth (green versus white) influence attractiveness of the flowers to Colletes cunicularius males, the main pollinator of O. arachnitiformis.

Conclusion

Chemical signals alone can mediate the interactions in highly specialized mimicry systems. Floral colour polymorphism in O. arachnitiformis is not subjected to selection imposed by C. cunicularius males, and an interplay between different non-adaptive processes may be responsible for the maintenance of floral colour polymorphism both within and among populations.     

Strong pollinator‐mediated selection for increased flower brightness and contrast in a deceptive orchid

Contrasting flower color patterns that putatively attract or direct pollinators toward a reward are common among angiosperms. In the deceptive orchid Anacamptis morio, the lower petal, which makes up most of the floral display, has a light central patch with dark markings. Within populations, there is pronounced variation in petal brightness, patch size, amount of dark markings, and contrast between patch and petal margin. We tested whether pollinators mediate selection on these color traits and on morphology (plant height, number of flowers, corolla size, spur length), and whether selection is consistent with facilitated or negative frequency‐dependent pollination. Pollinators mediated strong selection for increased petal brightness (Δβ_poll = 0.42) and contrast (Δβ_poll = 0.51). Pollinators also tended to mediate stabilizing selection on brightness (Δγ_poll = –0.27, n.s.) favoring the most common phenotype in the population. Selection for reduced petal brightness among hand‐pollinated plants indicated a fitness cost associated with brightness. The results demonstrate that flower color traits influence pollination success and seed production in A. morio, indicating that they affect attractiveness to pollinators, efficiency of pollen transfer, or both. The documented selection is consistent with facilitated pollination and selection for color convergence toward cooccurring rewarding species.     

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’.     

Evolution of honest reward signal in flowers

Some flowering plants signal the abundance of their rewards by changing their flower colour, scent or other floral traits as rewards are depleted. These floral trait changes can be regarded as honest signals of reward states for pollinators. Previous studies have hypothesized that these signals are used to maintain plant-level attractiveness to pollinators, but the evolutionary conditions leading to the development of honest signals have not been well investigated from a theoretical basis. We examined conditions leading to the evolution of honest reward signals in flowers by applying a theoretical model that included pollinator response and signal accuracy. We assumed that pollinators learn floral traits and plant locations in association with reward states and use this information to decide which flowers to visit. While manipulating the level of associative learning, we investigated optimal flower longevity, the proportion of reward and rewardless flowers, and honest- and dishonest-signalling strategies. We found that honest signals are evolutionarily stable only when flowers are visited by pollinators with both high and low learning abilities. These findings imply that behavioural variation in learning within a pollinator community can lead to the evolution of an honest signal even when there is no contribution of rewardless flowers to pollinator attractiveness.     

Floral colour change in Pedicularis monbeigiana (Orobanchaceae)

We examined the effects of the retention of colour-changed flowers on long- and short-distance attractiveness of bumblebees and the likelihood of successive flower visits by bumblebees in Pedicularis monbeigiana. The lower lip changed colour with age from white to purple. Hand geitonogamous pollination significantly reduced seed production. No pollen limitation occurred in this species. Purple-phase flowers contributed minimally to pollinator attractiveness at long distance. The combination of less reproductive flowers with a lower amount of reward and floral colour change enabled plants to direct pollinators to reproductive, highly rewarding white flowers at close range. A high percentage of purple-phase flowers in an inflorescence was associated with a marked reduction in the frequency of successive flower visits to individual plants. We suggest floral colour change in P. monbeigiana may serve as a mechanism for enhancing inter-individual pollen transfer and reducing intra-individual pollen transfer.     

Colour evolution within orchids depends on whether the pollinator is a bee or a fly

• Orchids are a classic angiosperm model for understanding biotic pollination. We studied orchid species within two species‐rich herbaceous communities that are known to have either hymenopteran or dipteran insects as the dominant pollinators, in order to understand how flower colour relates to pollinator visual systems.
• We analysed features of the floral reflectance spectra that are significant to pollinator visual systems and used models of dipteran and hymenopteran colour vision to characterise the chromatic signals used by fly‐pollinated and bee‐pollinated orchid species.
• In contrast to bee‐pollinated flowers, fly‐pollinated flowers had distinctive points of rapid reflectance change at long wavelengths and a complete absence of such spectral features at short wavelengths. Fly‐pollinated flowers also had significantly more restricted loci than bee‐pollinated flowers in colour space models of fly and bee vision alike.
• Globally, bee‐pollinated flowers are known to have distinctive, consistent colour signals. Our findings of different signals for fly pollination is consistent with pollinator‐mediated selection on orchid species that results from the distinctive features of fly visual systems.

     

Orchid pollination biology

Orchids display many unsurpassed floral specializations, as both rewarders and frauds in their interaction with animal pollinators. Accumulating evidence indicates that their floral evolution is driven by pollinator traits and that expenditure for maximized sexual reproduction is parcelled out over their lifetimes in strategies for coping with pollinator and resource limitations. Recent advances in orchid pollination biology center mainly on floral evolutionary processes, pseudocopulation and other deceptive pollination systems, and flower and fruit production in relation to costs of sexual reproduction.     

Where have all the blue flowers gone: pollinator responses and selection on flower colour in New Zealand Wahlenbergia albomarginata

Although pollinators are thought to select on flower colour, few studies have experimentally decoupled effects of colour from correlated traits on pollinator visitation and pollen transfer. We combined selection analysis and phenotypic manipulations to measure the effect of petal colour on visitation and pollen export at two spatial scales in Wahlenbergia albomarginata. This species is representative of many New Zealand alpine herbs that have secondarily evolved white or pale flowers. The major pollinators, solitary bees, exerted phenotypic selection on flower size but not colour, quantified by bee vision. When presented with manipulated flowers, bees visited flowers painted blue to resemble a congener over white flowers in large, but not small, experimental arrays. Pollen export was higher for blue flowers in large arrays. Pollinator preference does not explain the pale colouration of W. albomarginata, as commonly hypothesized. Absence of bright blue could be driven instead by indirect selection of correlated characters.     

Are pollinators the agents of selection on flower colour and size in irises?

Plant–pollinator interactions are believed to play a major role in the evolution of floral traits. Flower colour and flower size are important for attracting pollinators, directly influencing reproduction, and thus expected to be under pollinator‐mediated selection. Pollinator‐mediated selection is also proposed to play a role in maintaining flower colour polymorphism within populations. However, pigment concentrations, and thus flower colour, are also under selective pressures independent of pollinators. We quantified phenotypic pollinator‐mediated selection on flower colour and size in two colour polymorphic Iris species. Using female fitness, we estimated phenotypic selection on flower colour and size, and tested for pollinator‐mediated selection by comparing selection gradients between flowers open to natural pollination and supplementary pollinated flowers. In both species, we found evidence for pollen limitation, which set the base for pollinator‐mediated selection. In the colour dimorphic Iris lutescens, while pigment concentration and flower size were found to be under selection, this was independent of pollinators. For the polymorphic Iris pumila, pigment concentration is under selective pressure by pollinators, but only for one colour morph. Our results suggest that pollinators are not the main agents of selection on floral traits in these irises, as opposed to the accepted paradigm on floral evolution. This study provides an opposing example to the largely‐accepted theory that pollinators are the major agent of selection on floral traits.     

A test of phenotypic selection on petal form in the wild carnation,Dianthus inoxianus

Floral phenotypes are considered a product of pollinator‐mediated selection, which also has the side effect of decreasing floral variation within species. Correlates of flower visibility and function were studied in a carnation species (Dianthus inoxianus), which has crepuscular anthesis and scent‐based pollination by the hawkmoth Hyles livornica. We also assessed constancy of flower form in nature and in cultivation and, using fruit set as an estimate of plant relative fitness, tested whether the main pollinator exerted phenotypic selection on floral traits. Petal claw, which is roughly equivalent to the average depth at which an insect's proboscis must be inserted to reach nectar, was remarkably constant among wild plants (coefficient of variation 8%). In contrast, the area of the visible part of the petal, and the intensity of a coloured dot pattern on the petal was very variable (respectively CV = 34% and 102%). Cultivation in a common environment revealed significant variation among genotypes as regards petal area, degree of laciniation and extension of the dot pattern, but not petal claw length, which remained steady. Petal area, shape and colour did not affect relative fitness during the year of study, but plants with intermediate petal claws (i.e. floral tubes) set significantly more fruit. Results are compatible with low response of the main pollinator to variation in visual traits (petal area, laciniation, colour) and high responsiveness to variation in other aspects (tube length). Inconsistent phenotypic selection by pollinators may add to other causes of floral variation in the genus Dianthus, the causes of which are discussed.     

Pollinator community responses to the spatial population structure of wild plants: A pan-European approach

Land-use changes can alter the spatial population structure of plant species, which may in turn affect the attractiveness of flower aggregations to different groups of pollinators at different spatial scales. To assess how pollinators respond to spatial heterogeneity of plant distributions and whether honeybees affect visitation by other pollinators we used an extensive data set comprising ten plant species and their flower visitors from five European countries. In particular we tested the hypothesis that the composition of the flower visitor community in terms of visitation frequencies by different pollinator groups were affected by the spatial plant population structure, viz. area and density measures, at a within-population (‘patch’) and among-population (‘population’) scale. We found that patch area and population density were the spatial variables that best explained the variation in visitation frequencies within the pollinator community. Honeybees had higher visitation frequencies in larger patches, while bumblebees and hoverflies had higher visitation frequencies in sparser populations. Solitary bees had higher visitation frequencies in sparser populations and smaller patches. We also tested the hypothesis that honeybees affect the composition of the pollinator community by altering the visitation frequencies of other groups of pollinators. There was a positive relationship between visitation frequencies of honeybees and bumblebees, while the relationship with hoverflies and solitary bees varied (positive, negative and no relationship) depending on the plant species under study. The overall conclusion is that the spatial structure of plant populations affects different groups of pollinators in contrasting ways at both the local (‘patch’) and the larger (‘population’) scales and, that honeybees affect the flower visitation by other pollinator groups in various ways, depending on the plant species under study. These contrasting responses emphasize the need to investigate the entire pollinator community when the effects of landscape change on plant–pollinator interactions are studied.     

毛茛状金莲花不同花期的花特征和访花昆虫的变化及表型选择

为了研究植物生长季内开花时间对花特征表型选择的影响,我们以青藏高原东缘高寒草地的毛茛状金莲花Trollius ranunculoides)为实验材料,在生长季内不同开花时间(花前期、花末期)测定花特征,观察访花昆虫的类群和访花频率,生长季结束后收集种子.根据昆虫访花的喜好和季节内类群与访花频率的变化,分析了不同开花时间毛茛状金莲花的花特征与昆虫的选择;并用种子产量表示雌性适合度,估计了毛茛状金莲花的花特征在不同开花时间所受的表型选择.结果表明:不同花期植物的花特征有显著差异,相应的访花昆虫的类群和频率也存在差异,不同类群昆虫访花喜好也不一样.蜂喜好花瓣和花萼较宽、花茎短和花茎数少的个体,这正符合花前期的特征,因而蜂的访花频率在花前期较高;蝇对花特征没有明显的偏好.而通过雌性适合度估计毛茛状金莲花花特征所受的表型选择则是:花前期,花茎较长和花茎数多的植株适合度大;花末期,花茎数多的植株适合度大.我们的研究表明:在植物生长季,花期的分化伴随着传粉昆虫活动的变化.不同花期,访花昆虫的变化可能对植物花特征的分化起了至关重要的作用.但是访花昆虫对花特征的选择与通过雌性适合度估计植物受到的选择不尽相同,这可能是由于其他因素造成的.     

Relationship of visual and olfactory signal parameters in a food-deceptive flower mimicry system

Pollinators such as bees are attracted to flowers by their visualdisplay and their scent. Although most flowers reinforce visitsby providing pollen and/or nectar, there are species—notablyfrom the orchid family—that do not but do resemble rewardingspecies. These mimicry relationships provide ideal opportunitiesfor investigating the evolution of floral signals and theirimpact on pollinator behavior. Here, we have reanalyzed a caseof specialized food mimicry between the orchid Orchis israeliticaand its model, the lily Bellevalia flexuosa. Based on currentknowledge of insect sensory physiology, we were able to characterizeboth the visual and olfactory signals of model and mimic, aswell as of two phylogenetically related orchids. By using acolor vision model, we mapped each species' visual signals tothe perceptual space of honeybees and found an apparent shiftof the mimic's visual signals towards the model. We confirmthat visual mimicry is present. We analyzed the flower odorsby using gas chromatography/mass spectroscopy. We related thesesignals to the perceptual space of the pollinators by testingthe scent extracts physiologically, using in vivo brain imaging.We found no evidence of olfactory mimicry. The results indicatethat evolutionary pressure acts on the visual, but not olfactory,traits of O. israelitica toward a higher similarity to its model.Apparently, odor mismatch does not prevent a bee from landingon a flower that has the expected visual display. The resultstherefore argue for the dominance of visual stimuli in short-distanceflower choice. The orchid may still depend on long-distanceolfactory attraction originating from neighboring model plants.     

Who helps whom? Pollination strategy of <Emphasis Type="Italic">Iris tuberosa</Emphasis> and its relationship with a sexually deceptive orchid

Reproductive success of plants may be affected by interactions with co-flowering species either negatively, through competition for pollinators, or positively, by means of a magnet species effect and floral mimicry. In this study, potential interactions between Iris tuberosa, a rewarding species, and Ophrys fusca, a sexually deceptive orchid, were explored in four populations in southern Italy. In each population plots showing different ratios of the examined species were arranged in the field, and in each plot the number of pollinators and fruit set were assessed. In addition, flower size and floral hydrocarbons produced by the two species were analysed. Morphological and scent data pointed out that flower size and aliphatic compounds did not differ significantly between the two species. Interestingly, both species shared tricosane and 11-nonacosene, electrophysiologically active compounds in the shared dominant pollinator Adrena. We have found that fruit production and number of pollinators in I. tuberosa varied significantly among plots, while percentage of capsules and number of pollinators of O. fusca captured showed no significant differences across plots. These results suggested, that the presence of O. fusca contributes differentially to pollinator attraction, and thus, to total reproductive success of I. tuberosa, according to a different ratio of aggregation. These findings suggest that I. tuberosa profits from the greater abundance of insects attracted by the presence of orchid specimens, and that a sexually deceptive orchid may be a magnet species in pollination strategy.