Reward quality influences the development of learned olfactory biases in honeybees

Plants produce flowers with complex visual and olfactory signals, but we know relatively little about the way that signals such as floral scents have evolved. One important factor that may direct the evolution of floral signals is a pollinator''s ability to learn. When animals learn to associate two similar signals with different outcomes, biases in their responses to new signals can be formed. Here, we investigated whether or not pollinators develop learned biases towards floral scents that depend on nectar reward quality by training restrained honeybees to learn to associate two similar odour signals with different outcomes using a classical conditioning assay. Honeybees developed learned biases towards odours as a result of differential conditioning, and the extent to which an olfactory bias could be produced depended upon the difference in the quality of the nectar rewards experienced during conditioning. Our results suggest that differences in reward quality offered by flowers influence odour recognition by pollinators, which in turn could influence the evolution of floral scents in natural populations of co-flowering plants.     

Parallel chemical switches underlying pollinator isolation in Asian Mitella

Floral scents are among the key signals used by pollinators to navigate to specific flowers. Thus, evolutionary changes in scents should have strong impacts on plant diversification, although scent‐mediated plant speciation through pollinator shifts has rarely been demonstrated, despite being likely. To examine whether and how scent‐mediated plant speciation may have occurred, we investigated the Asimitellaria plant lineage using multidisciplinary approaches including pollinator observations, chemical analyses of the floral scents, electroantennographic analyses and behavioural bioassays with the pollinators. We also performed phylogenetically independent contrast analyses of the pollinator/floral scent associations. First, we confirmed that the pairs of the sympatric, cross‐fertile Asimitellaria species in three study sites consistently attract different pollinators, namely long‐tongued and short‐tongued fungus gnats. We also found that a stereoisomeric set of floral volatiles, the lilac aldehydes, could be responsible for the pollinator specificity. This is because the compounds consistently elicited responses in the antennae of the long‐tongued fungus gnats and had contrasting effects on the two pollinators, that is triggering the nectaring behaviour of long‐tongued fungus gnats while repelling short‐tongued fungus gnats in a laboratory experiment. Moreover, we discovered that volatile composition repeatedly switched in Asimitellaria between species adapted to long‐tongued and short‐tongued fungus gnats. Collectively, our results support the idea that recurrent scent‐mediated speciation has taken place in the Asimitellaria–fungus gnat system.     

Different rewards in female and male flowers can explain the evolution of sexual dimorphism in plants

Insects use floral signals to find rewards in flowers, transferring pollen in the process. In unisexual plants, the general view is that staminate (male) and pistillate (female) flowers obtain conspecific pollen transfers by advertising their rewards with similar floral signals. For female plants lacking food rewards, this can lead to floral mimicry and pollination by deceit. In this study, we challenge this view by presenting evidence for different rewards offered by flowers on females and males, as a mechanism promoting sexual dimorphism in Leucadendron xanthoconus (Proteaceae), a clearly sexually dimorphic shrub. The tiny beetle pollinators Pria cinerascens (Nitidulidae) depend entirely on the plants they pollinate for survival and reproduction. Male flowers provide mating and egglaying sites, and food for adults and larvae. Female flowers lack nectar and function to shelter pollinators from rain. Their flower heads have cup‐shaped display leaves, and are more closed than are those in males. On rainy days, flowers on females received 30% more visits than did flowers on males, and 90% more than they did on sunny days. When we removed display leaves in females, intact flower heads received 14 times more P. cinerascens visits than did manipulated flower heads, indicating that the cup shape attracts the beetles. In both sexes, having many flowers increased the probability of visits and the number of P. cinerascens visiting a plant. In males, the number of larvae was positively correlated with floral‐display size, while in females, seed set (pollen transfers) showed no relationship with floral‐display size. Ninety‐five per cent of the ovules received pollen and 52% matured into seeds. We explain the sexual dimorphism in L. xanthoconus as a result of an intimate partnership with P. cinerascens pollinators, in conjunction with a rainy climate. Pollinators favour large male floral displays, because they offer a reliable food source for adults and larvae. Frequent rains drive the P. cinerascens to leave males in search of the protection offered by females. Because females offer shelter, an essential resource that is not offered by male plants, they receive sufficient pollen independent of their floral‐display size. This pollination system promotes the evolution of sexually dimorphic floral signals, guiding pollinators to different rewards in male and female flowers. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85 , 97–109.     

Reproductive biology of Syagrus coronata (Arecaceae): sex‐biased insect visitation and the unusual case of scent emission by peduncular bracts

• Several monoecious species of palms have developed complex strategies to promote cross‐pollination, including the production of large quantities of floral resources and the emission of scents that are attractive to pollinators. Syagrus coronata constitutes an interesting model with which to understand the evolution of plant reproductive strategies in a monoecious species adapted to seasonally dry forests.
• We monitored blooming phenology over 1 year, during which we also collected and identified floral visitors and putative pollinators. We identified potential floral visitor attractants by characterizing the scent composition of inflorescences as well as of peduncular bracts, during both male and female phases, and the potential for floral thermogenesis.
• Syagrus coronata produces floral resources throughout the year. Its inflorescences are predominantly visited by a diverse assortment of small‐sized beetles, whose richness and abundance vary throughout the different phases of anthesis. We did not find evidence of floral thermogenesis. A total of 23 volatile compounds were identified in the scent emitted by the inflorescences, which did not differ between male and female phases; whereas the scent of the peduncular bracts was composed of only 4‐methyl guaiacol, which was absent in inflorescences.
• The composition of floral scent chemistry indicates that this palm has evolved strategies to be predominantly pollinated by small‐sized weevils. Our study provides rare evidence of a non‐floral scent emitting structure involved in pollinator attraction, only the second such case specifically in palms. The peculiarities of the reproductive strategy of S. coronata might play an important role in the maintenance of pollination services and pollen dispersion.

     

Floral scent composition predicts bee pollination system in five butterfly bush (Buddleja,Scrophulariaceae) species

Traditionally, plant–pollinator interactions have been interpreted as pollination syndrome. However, the validity of pollination syndrome has been widely doubted in modern studies of pollination ecology. The pollination ecology of five Asian Buddleja species, B. asiatica, B. crispa, B. forrestii, B. macrostachya and B. myriantha, in the Sino‐Himalayan region in Asia, flowering in different local seasons, with scented inflorescences were investigated during 2011 and 2012. These five species exhibited diverse floral traits, with narrow and long corolla tubes and concealed nectar. According to their floral morphology, larger bees and Lepidoptera were expected to be the major pollinators. However, field observations showed that only larger bees (honeybee/bumblebee) were the primary pollinators, ranging from 77.95% to 97.90% of total visits. In this study, floral scents of each species were also analysed using coupled gas chromatography and mass spectrometry (GC‐MS). Although the five Buddleja species emitted differentiated floral scent compositions, our results showed that floral scents of the five species are dominated by substances that can serve as attractive signals to bees, including species‐specific scent compounds and principal compounds with larger relative amounts. This suggests that floral scent compositions are closely associated with the principal pollinator assemblages in these five species. Therefore, we conclude that floral scent compositions rather than floral morphology traits should be used to interpret plant–pollinator interactions in these Asian Buddleja species.     

Innate attractant for long‐tongued bumblebee,Bombus diversus diversus in floral scent of bumblebee‐pollinated epiparasitic plant,Monotropastrum humile (Ericaceae)

The epiparasitic plant Monotropastrum humile (D. Don) Hara is pollinated by workers of the long‐tongued bumblebee, Bombus diversus diversus (Smith). The interaction between the floral scents of this plant and bumblebee was investigated using electrophysiological and behavioral techniques. Three components (linalool, α‐terpineol and geraniol) elicited strong responses in antennae from B. d. diversus workers and are innate attractants, suggesting floral scents play an important role in attracting these pollinators and successful pollination.     

Generalized pollination system: Are floral traits adapted to different pollinators?

Flowers that are pollinated both during the day and at night could exhibit two different groups of pollinators and produce two different sets of attractants and rewards. We explored the patterns of emission of flower scents and production of nectar in the cactus Echinopsis chiloensis ssp. chiloensis, in relation to the patterns of activity of its diurnal and nocturnal pollinators. We measured frequency of flower visitors, analyzed floral scents, measured nectar production and sugar concentration, and performed pollination exclusion experiments. Bees were the main visitors at daytime and hawkmoths at nighttime. Diurnal scents were dominated by several compounds that can attract a wide range of pollinators, whereas nocturnal scents were less diverse and were dominated by (E)-nerolidol, a compound eliciting antennal responses in hawkmoths. Nectar volume and sugar concentration at night were similar to those recorded in hawkmoth-pollinated flowers. Daytime nectar volume was higher than those commonly found in bee-pollinated flowers, but similar to those found in flowers pollinated by several pollinators. Daytime sugar concentration was similar to those recorded in bee-pollinated flowers. Flowers of E. chiloensis ssp. chiloensis seem morphologically adapted to hawkmoth pollination, but diurnal and nocturnal pollinators contribute to similar extents to reproductive success. Additionally, diurnal and nocturnal pollinators showed a synergic effect on the product of fruit set and seed set. The results are discussed in terms of the linkage between floral traits and perception abilities and requirements of pollinators.     

Variation in floral characters,particularly floral scent,in sapromyophilous Stemona species

Flowers or inflorescences often deploy various signals, including visual, olfactory, and gustatory cues, that can be detected by their pollinators. In many plants, these cues and their functions are poorly understood. Deciphering the interactions between floral cues and pollinators is crucial for analyzing the reproductive success of flowering plants. In this study, we examined the composition of the fetid floral scents produced by several Stemona species, including nine S. tuberosa populations from across China, using dynamic headspace adsorption, gas chromatography, and mass spectrometry techniques. We compared variations in floral phenotype, including floral longevity, nectar rewards, pollinator behavior, and flower length and color among the Stemona species. Of the 54 scent compounds identified, the major compounds include fetid dimethyl disulfide, dimethyl trisulfide, 1‐pyrroline, butyric acid, p‐cresol, isoamyl alcohol, and indole. We detected striking differentiation in floral scent at both the species and population level, and even within a population of plants with different colored flowers. Floral characteristics related to sapromyophily and deceptive pollination, including flower color mimicking livor mortis and a lack of nectar, were found in five Stemona species, indicating that Stemona is a typical sapromyophilous taxon. Species of this monocot genus might employ evolutionary tactics to exploit saprophilous flies for pollination.     

Generalized food deception: colour signals and efficient pollen transfer in bee‐pollinated species of Eulophia (Orchidaceae)

Non‐rewarding plants use a variety of ruses to attract their pollinators. One of the least understood of these is generalized food deception, in which flowers exploit non‐specific food‐seeking responses in their pollinators. Available evidence suggests that colour signals, scent and phenology may all play key roles in this form of deception. Here we investigate the pollination systems of five Eulophia spp. (Orchidaceae) lacking floral rewards. These species are pollinated by bees, notably Xylocopa (Anthophorinae, Apidae) or Megachile (Megachilidae) for the large‐flowered species and anthophorid (Anthophorinae, Apidae) or halictid (Halictidae) bees for the small‐flowered species. Spectra of the lateral petals and ultraviolet‐absorbing patches on the labella are strongly contrasting in a bee visual system, which may falsely signal the presence of pollen to bees. All five species possess pollinarium‐bending mechanisms that are likely to limit pollinator‐mediated self‐pollination. Flowering times extend over 3–4 months and the onset of flowering was not associated with the emergence of pollinators, some of which fly year round. Despite sharing pollinators with other plants and lacking rewards that would encourage fidelity, the Eulophia spp. exhibited relatively high levels of pollen transfer efficiency compared with other rewarding and deceptive orchids. We conclude that the study species employ generalized food deception and exploit food‐seeking bees. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013 , 171 , 713–729.     

Pollination of Campomanesia phaea (Myrtaceae) by night‐active bees: a new nocturnal pollination system mediated by floral scent

• Bees are the most important diurnal pollinators of angiosperms. In several groups of bees a nocturnal/crepuscular habit developed, yet little is known about their role in pollination and whether some plants are adapted specifically to these bees. We used a multidisciplinary approach to investigate the reproductive biology and to understand the role of nocturnal/crepuscular bees in pollination of Campomanesia phaea (Myrtaceae), popularly named cambuci.
• We studied the floral biology and breeding system of C. phaea. We collected the floral visitors and tested the pollinators' effectiveness. We also determined the floral scents released at night and during daytime, and studied behavioural responses of crepuscular/nocturnal bees towards these scents.
• The flowers of cambuci were self‐incompatible and had pollen as the only resource for flower visitors. Anthesis lasted around 14 h, beginning at 04:30 h at night. The flowers released 14 volatile compounds, mainly aliphatic and aromatic compounds. We collected 52 species of floral visitors, mainly bees. Nocturnal and crepuscular bees (four species) were among the most frequent species and the only effective pollinators. In field bioassays performed at night, nocturnal/crepuscular bees were attracted by a synthetic scent blend consisting of the six most abundant compounds.
• This study describes the first scent‐mediated pollination system between a plant and its nocturnal bee pollinators. Further, C. phaea has several floral traits that do not allow classification into other nocturnal pollination syndromes (e.g. pollinator attraction already before sunrise, with pollen as the only reward), instead it is a plant specifically adapted to nocturnal bees.

     

Sexual and temporal variations in floral scent in the subdioecious shrub Eurya japonica Thunb

In many flowering plants, floral scents are a significant trait for visitors, playing an important role in attracting pollinators and/or detracting herbivores. The evolution of flowering plants from hermaphroditism to dioecy is often accompanied by sexual dimorphism in floral scent. In this study, floral scents emitted by different sexual morphs of the subdioecious shrub Eurya japonica Thunb. were collected using a dynamic headspace method, and sexual and temporal variations were evaluated by gas chromatography–mass spectrometry (GC–MS). Two volatiles, α‐pinene and linalool, were identified as the major components of floral scents in females, hermaphrodites, and males. The males emit higher amounts of floral scents, particularly α‐pinene, compared to females or hermaphrodites. Floral scents emitted by males generally decrease as flowers enter senescence, whereas those from females or hermaphrodites do not significantly differ. Intraspecific variations in floral scents of subdioecious species provided by this study would contribute to better understanding of sexual dimorphism in floral scent.     

Floral biology and reproductive isolation by floral scent in three sympatric aroid species in French Guiana

We studied the reproductive biology of three sympatric Araceae species, Anthurium sagittatum, A. thrinax and Spathiphyllum humboldtii in French Guiana. The plants flowered simultaneously and were visited by scent‐collecting male euglossine bees, which were apparently their major pollinators. In total, each species was visited by 3–7 euglossine species, and 2–3 euglossine species accounted for at least 80% of all flower visits, with visits being plant species‐specific. Floral scent consisted of 6–10 main compounds, which made up 76–94% of the total amount of volatiles and were specific in these high amounts to each plant species. We suggest that the different floral scents lead to clear separation of the main pollinating euglossine species, providing a directed and efficient intraspecific pollen flow that results in high reproductive success. Since the simple floral (inflorescence) morphology of the studied plants does not support any morphological mechanisms to exclude visitors, as for example in euglossine‐pollinated perfume orchids, floral scent might be of major importance for the reproductive isolation and sympatric occurrence of these plants.     

Floral traits of mammal‐pollinated Mucuna macrocarpa (Fabaceae): Implications for generalist‐like pollination systems

Floral traits are adapted by plants to attract pollinators. Some of those plants that have different pollinators in different regions adapt to each pollinator in each region to maximize their pollination success. Mucuna macrocarpa (Fabaceae) limits the pollinators using its floral structure and is pollinated by different mammals in different regions. Here, we examine the relationships between floral traits of M. macrocarpa and the external morphology of mammalian pollinators in different regions of its distribution. Field surveys were conducted on Kyushu and Okinawajima Island in Japan, and in Taiwan, where the main pollinators are the Japanese macaque Macaca fuscata, Ryukyu flying fox Pteropus dasymallus, and red‐bellied squirrel Callosciurus erythraeus, respectively. We measured the floral shapes, nectar secretion patterns, sugar components, and external morphology of the pollinators. Results showed that floral shape was slightly different among regions and that flower sizes were not correlated with the external morphology of the pollinators. Volume and sugar rate of nectar were not significantly different among the three regions and did not change throughout the day in any of the regions. However, nectar concentration was higher in Kyushu than in the other two regions. These results suggest that the floral traits of M. macrocarpa are not adapted to each pollinator in each region. Although this plant limits the number of pollinators using its flower structure, it has not adapted to specific mammals and may attract several species of mammals. Such generalist‐like pollination system might have evolved in the Old World.     

Do pollinators simultaneously select for inflorescence size and amount of floral scents? An experimental assessment on Escallonia myrtoidea

Abstract Correlation among phenotypic traits may be explained by correlational selection, the simultaneous selection of more than one trait, or by genetic and/or developmental factors. In Escallonia myrtoidea, a tree with scented flowers from central Chile, inflorescence size and the amount of floral scents were positively correlated. Independent manipulation of scent and inflorescence size in a factorial design was used to assess the occurrence of pollinator‐mediated correlational selection. Dependency on pollinators for seed set was also assessed. If pollinator‐mediated correlational selection occurs, nonadditive effects of both traits are expected, albeit only when the effect of manipulating the state of such traits is disadvantageous with respect to the naturally occurring inflorescences, and provided that plants are not limited by pollinators for seed set and pollen export. Escallonia myrtoidea was very strongly pollinator‐limited for seed set and pollen export. Pollinator‐mediated additive effects were not observed in the frequency of visits by pollinators, pollen export, and seed set of E. myrtoidea after experiencing scent and inflorescence size manipulations. Consequently, there was no support for pollinator‐mediated correlational selection between those traits, suggesting the prevalence of genetic and/or developmental factors.     

Floral scent evolution in the section Pseudophrys: pollinator‐mediated selection or phylogenetic constraints?

• Sexually deceptive orchid species from the Mediterranean genus Ophrys usually interact with one or a few pollinator species by means of specific floral scents. In this study, we investigated the respective role of pollinator‐mediated selection and phylogenetic constraints in the evolution of floral scents in the section Pseudophrys.
• We built a phylogenetic tree of 19 Pseudophrys species based on three nuclear loci; we gathered a dataset on their pollination interactions from the literature and from our own field data; and we extracted and analysed their floral scents using solid phase microextraction and gas chromatography‐mass spectrometry. We then quantified the phylogenetic signal carried by floral scents and investigated the link between plant–pollinator interactions and floral scent composition using phylogenetic comparative methods.
• We confirmed the monophyly of the section Pseudophrys and demonstrated the existence of three main clades within this section. We found that floral scent composition is affected by both phylogenetic relationships among Ophrys species and pollination interactions, with some compounds (especially fatty acid esters) carrying a significant phylogenetic signal and some (especially alkenes and alkadienes) generating dissimilarities between closely related Pseudophrys pollinated by different insects.
• Our results show that in the section Pseudophrys, floral scents are shaped both by pollinator‐mediated selection and by phylogenetic constraints, but that the relative importance of these two evolutionary forces differ among compound classes, probably reflecting distinct selective pressures imposed upon behaviourally active and non‐active compounds.

     

Petunia flowers solve the defence/apparency dilemma of pollinator attraction by deploying complex floral blends

Flowers recruit floral visitors for pollination services by emitting fragrances. These scent signals can be intercepted by antagonists such as florivores to locate host plants. Hence, as a consequence of interactions with both mutualists and antagonists, floral bouquets likely consist of both attractive and defensive components. While the attractive functions of floral bouquets have been studied, their defensive function has not, and field‐based evidence for the deterrence of floral‐scent constituents is lacking. In field and glasshouse experiments with five lines of transgenic Petunia x hybrida plants specifically silenced in their ability to release particular components of their floral volatile bouquet, we demonstrate that the emission of single floral‐scent compounds can dramatically decrease damage from generalist florivores. While some compounds are used in host location, others prevent florivory. We conclude that the complex blends that comprise floral scents are likely sculpted by the selective pressures of both pollinators and herbivores.     

Floral scent chemistry and pollination ecology in phytelephantoid palms (Arecaceae)

The subfamilyPhytelephantoideae comprises three genera (Ammandra, Aphandra, andPhytelephas) and seven species of dioecious palms. The floral scents ofAmmandra dasyneura, A. decasperma, Aphandra natalia, Phytelephas aequatorialis, P. macrocarpa, andP. seemannii were analyzed by gas chromatography-mass spectrometry. We studied the pollination biology ofA. natalia, P. aequatorialis, andP. macrocarpa, and tested how the synthetically produced main constituents of the floral scents ofAphandra andPhytelephas attracted insects in two natural populations ofPhytelephas. The genera are distinct in terms of floral scents.Ammandra has sesquiterpenes,Aphandra (+)-2-methoxy-3-sec-butylpyrazine, andPhytelephas p-methyl anisol. These constituents dominated the scents quantitatively and qualitatively. The similarity between scents of male and female inflorescences was 76.5% inAmmandra, 84.2% inAphandra, and >99% inPhytelephas. Different species ofAleocharinae (Staphylinidae) pollinateAphandra natalia andPhytelephas species and reproduce in their male inflorescences.Derelomini (Curculinoidae) andMystrops (Nitidulidae) only visit and pollinatePhytelephas in which male inflorescences they reproduce. A species ofBaridinae (Curculionidae) only visits and pollinatesAphandra natalia, and reproduces in its female inflorescence. The apparent reliance on one or a few floral scent constituents as attractants and few and specific pollinators may indicate co-evolution. Sympatric species ofPhytelephantoideae have different scents. We suggest that species with similar scents have allopatric distributions due to the absence of a pollinator isolation mechanism.     

ECOLOGICAL COSTS OF PLANT RESISTANCE TO HERBIVORES IN THE CURRENCY OF POLLINATION

In this paper, we examine how ecological costs of resistance might be manifested through plant relationships with pollinators. If defensive compounds are incorporated into floral structures or if they are sufficiently costly that fewer rewards are offered to pollinators, pollinators may discriminate against more defended plants. Here we consider whether directional selection for increased resistance to herbivores could be constrained by opposing selection through pollinator discrimination against more defended plants. We used artificial selection to create two populations of Brassica rapa plants that had high and low myrosinase concentrations and, consequently, high and low resistance to flea beetle herbivores. We measured changes in floral characters of plants in both damaged and undamaged states from these populations with different resistances to flea beetle attack. We also measured pollinator visitation to plants, including numbers of pollinators and measures of visit quality (numbers of flowers visited and time spent per flower). Damage from herbivores resulted in reduced petal size, as did selection for high resistance to herbivores later in the plant lifetime. In addition, floral display (number of open flowers) was also altered by an interaction between these two effects. Changes in floral traits translated into overall greater use of low-resistance, undamaged plants based on total amount of time pollinators spent foraging on plants. Total numbers of pollinators attracted to plants did not differ among treatments; however, pollinators spent significantly more time per flower on plants from the low-resistance population and tended to visit more flowers on these plants as well. Previous work by other investigators on the same pollinator taxa has shown that longer visit times are associated with greater male and female plant fitness. Because initial numbers of pollinators did not differ between selection regimes, palatability and/or amount of rewards offered by high- and low-resistance populations are likely to be responsible for these patterns. During periods of pollinator limitation, less defended plants may have a selective advantage and pollinator preferences may mediate directional selection imposed by herbivores. In addition, if pollinator preferences limit seed set in highly defended plants, then lower seed set previously attributed to allocation costs of defense may also reflect greater pollinator limitation in these plants relative to less defended plants.     

Discriminant conditioning of foragers in the Asian honey bees Apis cerana and A.dorsata

Abstract.

• 1 Nectivore foraging environments are typically modelled as choices among non-fluctuating rewards, but in reality they often consist of intermittent daily nectar and pollen sources. Intermittent rewards create two distinct foraging problems for colonial nectivores: re-recruitment (periodically returning to intermittent rewards) and re-allocation (finding new rewards).
• 2 The role of scent in learning and remembering the locations of discontinuous nectar rewards was examined by testing re-recruitment efficiency of Apis cerana and A.dorsata to reward-correlated scents (odour discriminant self-conditioning). Experiments examined the responses of non-naive foragers to an odour correlated with prior reward, and to odours not correlated with prior rewards, by placing different scents into a colony and observing the number of bees re-recruited to a feeding station.
• 3 Re-recruitment of non-naive foragers in both species was significantly greater in response to the conditioning scent than to the experimental controls. However, species behaviour differed in one aspect; re-recruited A.cerana foragers landed on the feeding station when unscented reward was offered, whereas re-recruited A.dorsata foragers returned but would not land without conditioning scent present in the reward.

     

Agri‐environment schemes targeting farmland bird populations also provide food for pollinating insects

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