Complex floral traits shape pollinator attraction to ornamental plants

Background and AimsOrnamental flowering plant species are often used in managed greenspaces to attract and support pollinator populations. In natural systems, selection by pollinators is hypothesized to result in convergent multimodal floral phenotypes that are more attractive to specific pollinator taxa. In contrast, ornamental cultivars are bred via artificial selection by humans, and exhibit diverse and distinct phenotypes. Despite their prevalence in managed habitats, the influence of cultivar phenotypic variation on plant attractiveness to pollinator taxa is not well resolved.MethodsWe used a combination of field and behavioural assays to evaluate how variation in floral visual, chemical and nutritional traits impacted overall attractiveness and visitation by pollinator taxonomic groups and bee species to 25 cultivars of five herbaceous perennial ornamental plant genera.Key resultsDespite significant phenotypic variation, cultivars tended to attract a broad range of pollinator species. Nonetheless, at the level of insect order (bee, fly, butterfly, beetle), attraction was generally modulated by traits consistent with the pollination syndrome hypothesis. At the level of bee species, the relative influence of traits on visitation varied across plant genera, with some floral phenotypes leading to a broadening of the visitor community, and others leading to exclusion of visitation by certain bee species.ConclusionsOur results demonstrate how pollinator choice is mediated by complex multimodal floral signals. Importantly, the traits that had the greatest and most consistent effect on regulating pollinator attraction were those that are commonly selected for in cultivar development. Though variation among cultivars in floral traits may limit the pollinator community by excluding certain species, it may also encourage interactions with generalist taxa to support pollinator diversity in managed landscapes.     

Floral plasticity: Herbivore‐species‐specific‐induced changes in flower traits with contrasting effects on pollinator visitation

Plant phenotypic plasticity in response to antagonists can affect other community members such as mutualists, conferring potential ecological costs associated with inducible plant defence. For flowering plants, induction of defences to deal with herbivores can lead to disruption of plant–pollinator interactions. Current knowledge on the full extent of herbivore‐induced changes in flower traits is limited, and we know little about specificity of induction of flower traits and specificity of effect on flower visitors. We exposed flowering Brassica nigra plants to six insect herbivore species and recorded changes in flower traits (flower abundance, morphology, colour, volatile emission, nectar quantity, and pollen quantity and size) and the behaviour of two pollinating insects. Our results show that herbivory can affect multiple flower traits and pollinator behaviour. Most plastic floral traits were flower morphology, colour, the composition of the volatile blend, and nectar production. Herbivore‐induced changes in flower traits resulted in positive, negative, or neutral effects on pollinator behaviour. Effects on flower traits and pollinator behaviour were herbivore species‐specific. Flowers show extensive plasticity in response to antagonist herbivores, with contrasting effects on mutualist pollinators. Antagonists can potentially act as agents of selection on flower traits and plant reproduction via plant‐mediated interactions with mutualists.     

How to be an attractive male: floral dimorphism and attractiveness to pollinators in a dioecious plant

Background  

Sexual selection theory predicts that males are limited in their reproductive success by access to mates, whereas females are more limited by resources. In animal-pollinated plants, attraction of pollinators and successful pollination is crucial for reproductive success. In dioecious plant species, males should thus be selected to increase their attractiveness to pollinators by investing more than females in floral traits that enhance pollinator visitation. We tested the prediction of higher attractiveness of male flowers in the dioecious, moth-pollinated herb Silene latifolia, by investigating floral signals (floral display and fragrance) and conducting behavioral experiments with the pollinator-moth, Hadena bicruris.     

Context-dependent reproductive isolation mediated by floral scent and color

Reproductive isolation due to pollinator behavior is considered a key mode of speciation in flowering plants. Although floral scent is thought to mediate pollinator behavior, little is known about its effects on pollinator attraction and floral visitation in the wild. We used field experiments with wild hawkmoths and laboratory experiments with naïve hawkmoths to investigate attraction to and probing of flowers in response to indole, a volatile emitted by Ipomopsis tenuituba but not its close relative I. aggregata, both alone and in combination with floral color differences. We demonstrated that indole attracts wild hawkmoths to flowers, but has little effect on the rate at which those attracted moths probe flowers. In contrast, white flower color did not influence hawkmoth attraction in the field, but caused more attracted moths to probe flowers. Thus, the moths require both scent and high visual contrast, in that order, to feed at flowers at dusk. Their preference for indole-scented flowers is innate, but species-specific preference is mitigated by previous experience and plant spatial patterning. This context-dependent behavior helps explain why these Ipomopsis species show geographical variation in the extent of hybridization and may potentially explain formation of hybrid bridges in other systems of hawkmoth-pollinated plants.     

Plant reproductive strategies vary under low and high pollinator densities

Long‐term variation in the population density of honey bees Apis mellifera across landscapes has been shown to correlate with variation in the floral traits of plant populations in these landscapes, suggesting that variations in pollinator population density and foraging rates can drive floral trait evolution of their host plants. However, it remained to be determined whether this variation in plant traits is associated with adaptive variation in plant reproductive strategies under conditions of high and low pollinator densities. Here we conducted a reciprocal transplant experiment to examine how this variation in floral traits, under conditions of either high and low pollinator density, impacted seed production in the Tibetan lotus Saussurea nigrescens. In 2014 and 2015, we recorded the floral traits, pollinator visitation rates, and seed production of S. nigrescens populations grown in both home sites and foreign sites, where sites varied in honey bee population density. Our results demonstrated that the floral traits reflected those of their original population, regardless of their current location. However, seed production varied with both population origin and transplant site. Seed number was positively correlated with flower abundance in the pollinator‐rich sites, but with nectar production in the pollinator‐poor sites. Pollinator visitation rate was also positively correlated with flower number at pollinator‐rich sites, and with nectar volume at pollinator‐poor sites. Overall, the local genotype had higher seed production than nonlocal genotypes in home sites. However, when pollen is hand‐supplemented, plants from pollinator‐rich populations had higher seed production than plants from pollinator‐poor populations, regardless of whether they were transplanted to pollinator‐rich or ‐poor sites. These results suggest that the plant genotypic differences primarily drive variation in pollinator attraction, and this ultimately drives variation in seed: ovule ratio. Thus, our results suggest that flowering plant species use different reproductive strategies to respond to high or low pollinator densities.     

Factors affecting pollinator movement and plant fitness in a specialized pollination system

The rate of pollen exchange within and among flowers may depend on pollinator attraction traits such as floral display size and flowering plant density. Variations in these traits may influence pollinator movements, pollen receipt, and seed number. To assess how floral display size and flowering plant density affect parameters of pollinator visitation rate, pollen receipt per flower, seed number per fruit and the between-plant pollinator movements, we studied the self-incompatible plant, Nierembergia linariifolia. Per-flower pollinator visitation rate and bout length increased linearly with increasing floral display size. Pollen receipt per flower increased linearly with increasing flowering plant density. For seed number per fruit, a polynomial model describing an increased seed number per fruit at low density and a decreased seed number per fruit at high density provided a significant fit. Per-flower pollinator visitation rate was not associated with pollen receipt per flower and seed number per fruit. Bees visited plants located near to the center of the population more frequently than plants located at the periphery. Increases in both floral display size and flowering plant density led to an increased chance of a plant being chosen as the center of the pollinator foraging area. These results suggest that even though large floral displays and high flowering plant density are traits that attract more pollinators, they may also reduce potential mate diversity by restricting pollen movement to conspecific mates that are closely located.     

Relationships between species’ floral traits and pollinator visitation in a temperate grassland

Knowledge about plant–plant interactions for pollinator service at the plant community level is still scarce, although such interactions may be important to seed production and hence the population dynamics of individual plant species and the species compositions of communities. An important step towards a better understanding of pollination interactions at the community level is to assess if the variation in floral traits among plant species explain the variation in flower visitation frequency among those species. We investigated the relative importance of various floral traits for the visitation frequency of all insects, and bumblebees and flies separately, to plant species by measuring the visitation frequency to all insect-pollinated species in a community during an entire flowering season. Visitation frequency was identified to be strongly positive related to the visual display area and the date of peak flowering of plant species. Categorical variables, such as flower form and symmetry, were important to the visitation frequency of flies only. We constructed floral similarity measures based on the species’ floral traits and found that the floral similarity for all species’ traits combined and the continuous traits separately were positively related to individual visitation frequency. On the other hand, plant species with similar categorical floral traits did not have similar visitation frequencies. In conclusion, our results show that continuous traits, such as flower size and/or density, are more important for the variation in visitation frequency among plant species than thought earlier. Furthermore, differences in visitation frequency among pollinator groups give a poor support to the expectations derived from the classical pollination syndromes.     

The invasive <Emphasis Type="Italic">Lespedeza cuneata</Emphasis> attracts more insect pollinators than native congeners in tallgrass prairie with variable impacts

Invasive plant species can potentially exert competitive or facilitative effects on insect pollination services of native species. Factors that influence these effects include the degree of shared pollinator species, synchronous flowering phenology, similar flower morphology and color, relatedness of invasive and natives, and showiness and densities of flowers. We investigated such plant-pollinator dynamics by comparing the invasive Lespedeza cuneata and three native congeners, all sympatric with synchronous flowering, using in situ populations over 2 years during peak floral displays. Insect visitation rates of the invasive were significantly higher per plant in both years than on the native species. The invasive exerted a competitive effect on visitation of the two native species with fewer shared pollinators, and a facilitative effect on visitation of the native species with the highest degree of shared insect visitors. Positive correlations were found between floral density and visitation rate per plant in all the native species. Although no such correlation was found for the invasive, floral density in L. cuneata was at least twenty times higher than in the native species and likely saturated the response of the pollinator community. Analyses of insect visitor taxonomic data indicated the insect communities visiting each of the Lespedeza species were generally similar though with species-specific differences. The main exception was that the common honeybee, Apis mellifera, was a primary visitor to the invasive plant species, yet was never observed on the native Lespedeza species.     

Effects of drought and N level on the interactions of the root hemiparasite Rhinanthus alectorolophus with a combination of three host species

• Increasing nitrogen deposition and more frequent drought events are likely to change plant interactions in natural grasslands. Both factors may also influence the interactions between hemiparasitic plants, regarded as keystone species in many grasslands, and their host species.
• We grew a combination of three suitable hosts, a grass, a forb and a legume, with and without the hemiparasite Rhinanthus alectorolophus at three levels of nitrogen (N) and two levels of water availability in a factorial design.
• Biomass of the hemiparasite and host community increased with N level and was reduced by drought to a similar degree. Larger plants in fertilised pots started to wilt earlier, and the presence of a hemiparasite further increased drought sensitivity. The hemiparasite strongly reduced biomass of the host community and overall productivity, and affected the competitive balance among host plants because it particularly reduced biomass of the dominant grass. These effects were the opposite of those of high N. The hemiparasite increased the root mass fraction of the hosts at all levels of N and water availability, indicating that the effect of the hemiparasite on the hosts was mainly due to loss of belowground resources.
• Our results indicate that hemiparasites will not always respond more strongly to increased N availability and drought than autotrophic plants, and that hemiparasites can have similarly strong effects on grassland communities as soil fertility and drought. By preferentially attacking dominant species the hemiparasites might alleviate the negative effects of nutrient enrichment on grassland diversity.

     

The role of local adaptation in the relationship between an endangered root hemiparasite Euphrasia rostkoviana, and its host, Agrostis capillaris

We experimentally studied the role of local adaptation and the co-evolutionary relationship between an annual, endangered root hemiparasite Euphrasia rostkoviana and its main host Agrostis capillaris. According to our hypothesis, the existence of local adaptation in hemiparasites should be observable in better hemiparasite performance when attached to A. capillaris hosts originating From Euphrasia populations. After one month of growth, the height and the number of leaves of hemiparasites were not affected by the origin of their hosts. The differences in growth were due to between population effects. The situation remained constant after three months. Hemiparasite biomass was not affected by the origin of the hosts. The percentage of hemiparasites surviving after one. two and three months was not affected by the origin of the hosts although there was a weak tendency towards better survival of hemiparasites with familiar hosts than with unfamiliar hosts. All variables used to measure hemiparasite performance during its complete life-cycle gave only limited support for the local adaptation hypothesis. Nevertheless, the familiar hosts suffered less from parasitism as indicated by their higher biomass after the experiment. This suggests that there may be some interactions between hemiparasites and their hosts based on their spatial population structure and common history as competitors.     

Host preference of a temperate mistletoe: Disproportional infection on three co‐occurring host species influenced by differential success

The mistletoe Tristerix verticillatus (Loranthaceae) parasitizes within a small area of the Yerba Loca Nature Sanctuary near Santiago, Chile, three co‐occurring hosts: Schinus montanus (Anacardiaceae), Fabiana imbricata (Solanaceae) and Berberis montana (Berberidaceae). Previous studies suggest that T. verticillatus may be favoured when parasitizing S. montanus relative to the other two host species. We hypothesize that infection of S. montanus is not proportional to its local abundance or appearance, that S. montanus is more intensively parasitized than other available hosts, and that host provenance is a determinant of the fate of the infecting seed. We compare the incidence of infection of T. verticillatus in relation to local availability and appearance variables, and the intensity of infection of T. verticillatus, on the three co‐occurring host species. We then test the effects of host provenance on mistletoe seed establishment success with a seed cross inoculation experiment varying the donor and receptor hosts. Finally, we test whether there are differences in establishment success between manually processed seeds and seeds defecated by the avian disperser Mimus thenca (Passeriformes: Mimidae). Our results show that the three hosts have an aggregated spatial distribution. Schinus montanus was parasitized at a higher rate than expected by its local availability and appearance, and inoculated seeds showed differential development depending on the origin of the seeds: seeds from T. verticillatus parasitizing S. montanus inoculated to S. montanus twigs showed higher germination and lower mortality than seeds from T. verticillatus parasitizing F. imbricata inoculated to S. montanus twigs. Furthermore, seeds defecated by the avian disperser, M. thenca, had higher adherence and reduced mortality when compared to manually processed seeds. The disproportional host infection found is discussed in terms of the differential establishment of mistletoe seeds, morphological characteristics of hosts and the behaviour of dispersing birds.     

Drought and leaf herbivory influence floral volatiles and pollinator attraction

The effects of climate change on species interactions are poorly understood. Investigating the mechanisms by which species interactions may shift under altered environmental conditions will help form a more predictive understanding of such shifts. In particular, components of climate change have the potential to strongly influence floral volatile organic compounds (VOCs) and, in turn, plant–pollinator interactions. In this study, we experimentally manipulated drought and herbivory for four forb species to determine effects of these treatments and their interactions on (1) visual plant traits traditionally associated with pollinator attraction, (2) floral VOCs, and (3) the visitation rates and community composition of pollinators. For all forbs tested, experimental drought universally reduced flower size and floral display, but there were species‐specific effects of drought on volatile emissions per flower, the composition of compounds produced, and subsequent pollinator visitation rates. Moreover, the community of pollinating visitors was influenced by drought across forb species (i.e. some pollinator species were deterred by drought while others were attracted). Together, these results indicate that VOCs may provide more nuanced information to potential floral visitors and may be relatively more important than visual traits for pollinator attraction, particularly under shifting environmental conditions.     

Phenotypic selection on floral scent: trade-off between attraction and deterrence?

Flowers emit a large variety of floral signals that play a fundamental role in the communication of plants with their mutualists and antagonists. We investigated phenotypic selection on floral scent and floral display using the rewarding orchid species Gymnadenia odoratissima. We found positive directional selection on inflorescence size, as well as positive and negative selection on floral scent compounds. Structural equation modeling showed that “active” compounds, i.e. those that were shown in earlier investigations to be detected by pollinator insects, were positively linked to fitness, whereas “non-active” were negatively linked to fitness. Our results suggest that different patterns of selection impact on different scent compounds, which may relate to the functions of compounds for attracting/deterring insects.     

Selection of floral resources to optimise conservation of agriculturally-functional insect groups

Non-crop vegetation in agricultural landscapes can provide a means of conserving insects in farmed landscapes and optimising on-farm ecosystem services as a result. Inclusion of floral resources may be particularly useful in conserving many beneficial insects, where groups including pollinators and pest natural enemies often rely on nectar and pollen during (at least part of) their life-cycle. As not all flowers are equally suited to all beneficial insects, selection of appropriate flowering plants is key to ensuring that conservation targets are met and benefits to ecosystems services realised as a result. This short paper describes an experiment conducted to assess the ‘total temporal attractiveness’ of a range of British wildflowers to selected functional insect groups. The results obtained demonstrate that flowering period alone is a poor indicator of plant suitability to insects, where no relationship existed between this and attraction to insects overall. Data also suggest that, based on attraction over a season, certain flowering plants are more likely to be of general insect conservation value and/or benefit to functional insect groups than others. Attraction to pest insects was also considered, with relatively high catches of thrips and pollen beetles observed in flowering stands of some plants.     

Pollinator conservation at the local scale: flower density,diversity and community structure increase flower visiting insect activity to mixed floral stands

Insect pollinators play a keystone role in terrestrial ecosystems. The parallel declines in plant and pollinator communities emphasizes that plant-pollinator interactions at the community level are highly relevant for biodiversity conservation. Here we examine relationships between plants and flower-visiting insects (anthophiles) at the scale of local floral patches. We conducted a visitation survey during the spring flowering season, a peak time for pollinator activity in the threatened Cape Floristic Region, South Africa. We tested floral density, diversity and composition as predictors of anthophile diversity (measured at the family/family group level) and visitation rates in multispecies stands of flowers. Although different anthophile groups responded differently, generally anthophile visitation rates and diversity were positively affected by floral density, diversity and community structure. Anthophiles were more abundant and diverse in areas with a high density and diversity of flowers. Plant community structure affected both the likelihood of occurrence and activity of anthophiles in the plots. The two mass flowering species examined here, Relhania fruticosa and Salvia chamaeleagnea, were strong determinants of anthophile activity, greatly increasing visitation rates, even though there was, on average, lower floral density and diversity. Our results show that anthophile activity is affected by highly localised, small-scale factors, namely the density and diversity of flowers and community structure. Important among these factors are patches of high quality habitat, high in floral abundance and diversity, both of which should be included in landscape-level plans for pollinator conservation, providing stepping stones for these insects in transformed landscapes.     

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.     

POLLINATOR‐MEDIATED REPRODUCTIVE ISOLATION AMONG DIOECIOUS FIG SPECIES (FICUS,MORACEAE)

The extent of isolation among closely related sympatric plant species engaged in obligate pollination mutualisms depends on the fitness consequences of interspecies floral visitation. In figs (Ficus), interspecific gene flow may occur when pollinating wasps (Agaonidae) visit species other than their natal fig species. We studied reproductive isolation in a clade of six sympatric dioecious fig species in New Guinea. Microsatellite genotyping and Bayesian clustering analysis of the fig community indicated strong reproductive barriers among sympatric species. A total of 1–2% of fig populations consisted of hybrid individuals. A new experimental method of manipulating fig wasps investigated the reproductive consequences of conspecific and heterospecific pollinator visitation for both mutualists. Fig wasps introduced to Ficus hispidioides pollinated and oviposited in receptive figs. Seed development and seedling growth were largely comparable between conspecific and heterospecific crosses. Heterospecific pollinator fitness, however, was significantly less than that of conspecific pollinators. Heterospecific pollinators induced gall formation but offspring did not develop to maturity in the new host. Selection on pollinators maintaining host specificity appears to be an important mechanism of contemporary reproductive isolation among these taxa that could potentially influence their diversification.     

'Floral' scent production by Puccinia rust fungi that mimic flowers

Crucifers (Brassicaceae) in 11 genera are often infected by rust fungi in the Puccinia monoica complex. Infection causes a 'pseudoflower' to form that is important for attracting insect visitors that sexually outcross the fungus. 'Pollinator' attraction is accomplished through visual floral mimicry, the presence of a nectar reward and floral fragrances. Here we used gas chromatography and mass spectrometry to identify and quantify fragrance production by these rust fungi on several Arabis hosts, and by co-occurring true flowers that share insect visitors. Fungal pseudoflowers produced distinctive floral fragrances composed primarily of aromatic alcohols, aldehydes and esters. Pseudoflower fragrances were chemically similar to noctuid-moth-pollinated flowers, such as Cestrum nocturnum and Abelia grandiflora , but were very different from host flowers, host vegetation and the flowers of coblooming, nonhost angiosperms. There was variation in the quantity and composition of fragrance profiles from different fungal species as well as within and among hosts. The evolution of scent chemistry is relatively conservative in these fungi and can be most parsimoniously explained in three steps by combining chemical data with a previously determined rDNA ITS sequence-based phylogeny. Pseudoflower scent does not appear to represent a simple modification of host floral or vegetative emissions, nor does it mimic the scent of coblooming flowers. Instead, we suspect that the unique fragrances, beyond their function as pollinator attractants, may be important in reducing gamete loss by reinforcing constancy among foraging insects.     

Refuse attracts? Effect of refuse dumps of leaf‐cutting ants on floral traits

The nutrient‐rich organic waste generated by ants may affect plant reproductive success directly by enhancing fruit production but also indirectly, by affecting floral traits related with pollinator attraction. Understanding how these soil‐nutrient hot spots influence floral phenotype is relevant to plant–pollination interactions. We experimentally evaluated whether the addition of organic waste from refuse dumps of the leaf‐cutting ant Acromyrmex lobicornis (Hymenoptera: Formicidae: Attini) alters floral traits associated with pollinator attraction in Eschscholzia californica (Ranunculales: Papaveraceae), an entomophilous herb. We analysed flower shape and size using geometric morphometric techniques in plants with and without the addition of refuse‐dumps soil, under greenhouse conditions. We also measured the duration of flowering season, days with new flowers, flower production and floral display size. Plants growing in refuse‐dumps soil showed higher flower shape diversity than those in control soil. Moreover, plants in refuse‐dumps soil showed bigger flower and floral display size, longer flowering season, higher number of flowering days and flower production. As all these variables may potentially increase pollinator visits, plants in refuse‐dumps soil might increase their fitness through enhanced attraction. Our work describes how organic waste from ant nests may enhance floral traits involved in floral attraction, illustrating a novel way of how ants may indirectly benefit plants.     

Effects of conspecific and heterospecific floral density on the pollination of two related rewarding orchids

Variation in within-population floral density can affect interactions between plants and pollinators, resulting in variable pollen export for plants. We investigated the effects of conspecific and heterospecific floral densities on pollination success both of two related, self-compatible, nectar-rewarding orchid species in Ireland, Spiranthes romanzoffiana (rare and listed as endangered) and its congener, S. spiralis (more abundant and not of conservation concern). Floral densities, insect visitation rates, and orchid pollen transport were recorded in multiple quadrats in four populations of both orchid species over their flowering season. We found that conspecific and heterospecific co-flowering plant density affected pollination in both orchid species. For S. romanzoffiana, higher heterospecific density increased pollen removal. For S. spiralis, higher conspecific visitation increased pollen removal and increased heterospecific density decreased pollen deposition. In addition, increased conspecific density increased pollen deposition in both species. This study shows that plants may interact to facilitate or compete for different components of the pollination process, namely; pollinator attraction, pollen removal and deposition. Such interactions have immediate consequences for endangered plant species, as increases in both conspecific and heterospecific coflowering density may ameliorate the negative effects of rarity on pollination, hence overall reproductive success.