Floral Cues Research Articles

Mosquito taste responses to human and floral cues guide biting and feeding.

The taste system controls many insect behaviours, yet little is known about how tastants are encoded in mosquitoes or how they regulate critical behaviours. Here we examine how taste stimuli are encoded by Aedes albopictus mosquitoes-a highly invasive disease vector-and how these cues influence biting, feeding and egg laying. We find that neurons of the labellum, the major taste organ of the head, differentially encode a wide variety of human and other cues. We identify three functional classes of taste sensilla with an expansive coding capacity. In addition to excitatory responses, we identify prevalent inhibitory responses, which are predictive of biting behaviour. Certain bitter compounds suppress physiological and behavioural responses to sugar, suggesting their use as potent stop signals against appetitive cues. Complex cues, including human sweat, nectar and egg-laying site water, elicit distinct response profiles from the neuronal repertoire. We identify key tastants on human skin and in sweat that synergistically promote biting behaviours. Transcriptomic profiling identifies taste receptors that could be targeted to disrupt behaviours. Our study sheds light on key features of the taste system that suggest new ways of manipulating chemosensory function and controlling mosquito vectors.

Variations of floral temperature in changing weather conditions.

Floral temperature is a flower characteristic that has the potential to impact the fitness of flowering plants and their pollinators. Likewise, the presence of floral temperature patterns, areas of contrasting temperature across the flower, can have similar impacts on the fitness of both mutualists. It is currently poorly understood how floral temperature changes under the influence of different weather conditions, and how floral traits may moderate these changes. The way that floral temperature changes with weather conditions will impact how stable floral temperatures are over time and their utility to plants and pollinators. The stability of floral temperature cues is likely to facilitate effective plant-pollinator interactions and play a role in the plant's reproductive success. We use thermal imaging to monitor how floral temperatures and temperature patterns of four plant species (Cistus 'snow fire' and 'snow white', Coreopsis verticillata and Geranium psilostemon) change with several weather variables (illumination, temperature; windspeed; cloud cover; humidity and pressure) during times that pollinators are active. All weather variables influenced floral temperature in one or more species. The directionality of these relationships was similar across species. In all species, light conditions (illumination) had the greatest influence on floral temperatures overall. Floral temperature and the extent to which flowers showed contrasting temperature patterns were influenced predominantly by light conditions. However, several weather variables had additional, lesser, influences. Furthermore, differences in floral traits, pigmentation and structure, likely resulted in differences in temperature responses to given conditions between species and different parts of the same flower. However, floral temperatures and contrasting temperature patterns that are sufficiently elevated for detection by pollinators were maintained across most conditions if flowers received moderate illumination. This suggests the presence of elevated floral temperature and contrasting temperature patterns are fairly constant and may have potential to influence plant-pollinator interactions across weather conditions.

Floral Trait Preferences of Three Common wild Bee Species.

The interaction between bees and flowering plants is mediated by floral cues that enable bees to find foraging plants. We tested floral cue preferences among three common wild bee species: Lasioglossum villosulum, Osmia bicornis, and Bombus terrestris. Preferences are well studied in eusocial bees but almost unknown in solitary or non-eusocial generalist bee species. Using standardized artificial flowers altered in single cues, we tested preferences for color hue, achromatic contrast, scent complexity, corolla size, and flower depth. We found common attractive cues among all tested bees. Intensively colored flowers and large floral displays were highly attractive. No preferences were observed in scent complexity experiments, and the number of volatiles did not influence the behavior of bees. Differing preferences were found for color hue. The specific behaviors were probably influenced by foraging experience and depended on the flower choice preferences of the tested bee species. In experiments testing different flower depths of reward presentation, the bees chose flat flowers that afforded low energy costs. The results reveal that generalist wild bee species other than well-studied honeybees and bumblebees show strong preferences for distinct floral cues to find potential host plants. The diverse preferences of wild bees ensure the pollination of various flowering plants.

Onion (Allium cepa L.) Attracts Scoliid Wasps by Means of Generalist Floral Volatiles.

Onion flowers require pollinator-mediated cross-pollination. However, the cues that pollinators use to locate the flowers are not well understood. The floral scent, along with floral visual cues, might acts as important signal to pollinators in order to locate the floral resources. We used electrophysiological methods combined with behavioural assays to determine which compounds in a floral scent are more attractive and thus biologically important to foraging scollid wasps. The majority of the molecules identified as floral fragrances in onions are common compounds that are already known from other angiosperms, and onion floral scents were predominately composed of aromatic components. The antennae of scoliid wasps responded to a large number of compounds, among them o-cymene, cis-β-ocimene, benzaldehyde and allo-ocimene were behaviourally active. In contrast to other wasp flowers investigated nectar analysis demonstrated the dominance of hexose sugars over sucrose. Our findings provide fresh insights into the floral volatile chemistry of a key vegetable crop grown around the world. We demonstrate here that onion is using generalist floral volatiles to attract floral visitors. This insight could be utilised to make onion blooms more attractive to minor pollinators as well as major pollinators in order to maximise seed set.

The role of visual and olfactory floral cues in twilight foraging by Ptiloglossa and Xylocopa bees

The role of visual and olfactory floral cues in twilight foraging by Ptiloglossa and Xylocopa bees

Floral signals of the dimorphic oil-producing Byrsonima sericea (Malpighiaceae): is the eglandular morph deceptive?

ABSTRACT Background Presence of eglandular individuals (lacking floral oil glands) within populations of several neotropical Malpighiaceae is intriguing, with ecological and evolutionary implications so far unexplored. This floral dimorphism (glandular and eglandular individuals) is hypothesised to be related to energetic costs of oil production and pollinator deception. Aims To evaluate whether eglandular individuals of Byrsonima sericea deceive oil-collecting bees and obtain higher reproductive success (fruit production) compared to glandular individuals. Methods We monitored flower visitation and quantified and identified floral cues (visual and olfactory) associated with glandular and eglandular individuals, and measured fruit set. Results Both morphotypes exhibited similar visual cues and proportions of visits by oil-collecting bees and similar fruit set. Floral scent via headspace analysis indicated no between-morphotype differences in biogenic volatile organic compounds, whilst flower extract samples showed a clear difference in chemical composition. Conclusions Absence of oil production in B. sericea was not associated with changes in floral cues used in pollinator attraction at long distances. Maintenance of floral cues may be a deceptive mechanism that maintains the oil-collecting behaviour of bees on flowers that lack oil glands. Higher fruit set was not observed in eglandular individuals, suggesting that energetic costs associated with oil production do not involve fruit production.

Colletes hederae bees are equally attracted by visual and olfactory cues of inconspicuous Hedera helix flowers

Wild bees are heavily declining worldwide except for a few species, such as Colletes hederae, which is spreading in its distribution throughout Europe. Colletes hederae mainly forages on ivy (Hedera helix) which is widespread in Europe and the plants’ availability is thought to contribute to the successful spread of C. hederae. A rapid location of the plants using visual and/or olfactory floral cues would allow the bee to efficiently forage. Beside bee visitors, the flowers attract a high variety of other insects, such as Vespula wasps that were recently investigated regarding their floral-cue preferences. The aim of this study was to investigate the communication between C. hederae and its H. helix host flowers, and to compare the results with that previously obtained with V. germanica wasps. We identified headspace compounds detectable by the bees using gas chromatography coupled to electroantennography (GC-EAD) and performed behavioral experiments to both compare the attractiveness of visual and olfactory floral cues and to determine the attractiveness of a synthetic mixture composed of physiologically active compounds. In the GC-EAD analyses, bees responded to 15 flower-specific compounds of various chemical classes, of which 4-oxoisophorone, (E)-linalool-oxide furanoid, and acetophenone were the most abundant in the floral scent. In the bioassays, visual and olfactory flower cues were equally attractive for bees, but a combination of both cues was needed to elicit not only approach responses but also landings. A synthetic mixture of the EAD-active compounds was attractive to the bees, but to a lesser extent than the natural scent of H. helix flowers. The bees’ integrations of different floral-cue modalities in its search image and its strong antennal responses elicited by various floral scent compounds make C. hederae highly effective in finding its host flowers. In comparison to V. germanica wasps, the bees relied stronger on visual cues than the wasps do, but both species showed the highest attraction when presented with a combination of the cues.

Characterization of Leaf Transcriptome in a Tropical Tree Species, <i>Shorea curtisii</i>, over a Flowering Season

General flowering (GF) is a synchronous flowering phenomenon in the Southeast Asian tropical rainforests that occurs at irregular intervals of multiple years. While in this study, the leaf transcriptome of a GF species, Shorea curtisii obtained from three-time points – before and after floral initiation, and post-flowering stage – was sequenced, the unpredictable intervals of GF raise conservation concerns for these under-researched forests with rich economically and ecologically important species. We assembled 243,759,478 sequencing reads into 39,943 non-redundant unigenes including 677 putative homologs of Arabidopsis thaliana flowering-related genes. Differential expression analysis conducted on pairwise comparisons of the time points identified 930 differentially expressed unigenes, which includes 17 flowering-related homologs. The differential expression of unigenes with significant enrichments of functions related to drought corroborated the involvement of drought as an environmental cue for GF, with the outcomes of this study offering an insight into the conservation of floral regulatory genes and pathways in Shorea and possibly being used as a model to better understand the floral initiation cues and regulation of GF trees.

Synthetic fertilizers alter floral biophysical cues and bumblebee foraging behavior.

The use of agrochemicals is increasingly recognized as interfering with pollination services due to its detrimental effects on pollinators. Compared to the relatively well-studied chemical toxicity of agrochemicals, little is known on how they influence various biophysical floral cues that are used by pollinating insects to identify floral rewards. Here, we show that widely used horticultural and agricultural synthetic fertilizers affect bumblebee foraging behavior by altering a complex set of interlinked biophysical properties of the flower. We provide empirical and model-based evidence that synthetic fertilizers recurrently alter the magnitude and dynamics of floral electrical cues, and that similar responses can be observed with the neonicotinoid pesticide imidacloprid. We show that biophysical responses interact in modifying floral electric fields and that such changes reduce bumblebee foraging, reflecting a perturbation in the sensory events experienced by bees during flower visitation. This unveils a previously unappreciated anthropogenic interference elicited by agrochemicals within the electric landscape that is likely relevant for a wide range of chemicals and organisms that rely on naturally occurring electric fields.

Among-years rain variation is associated with flower size, but not with signal patch size in Iris petrana.

Among-years rain variation is associated with flower size, but not with signal patch size in Iris petrana.

Pollinator shifts and the evolution of floral advertising traits in the genus Ferraria (Iridaceae)

One of the most compelling explanations for floral trait diversification and speciation in angiosperms is the process of pollinator shifts. The African genus, Ferraria, is a relatively small and understudied group of irises which interacts with many distinct pollinator groups and exhibits large variation in floral scent and colour. We built a phylogeny for the genus using three chloroplast gene regions and reconstructed the joint evolutionary history of pollination systems and floral traits. We found evidence for several historical shifts amongst pollinator functional groups and associations between pollinators and certain floral visual cues and mechanical fit traits. We also found evidence that colour divergence in Ferraria flowers evolved through non-random evolution. This indicates that pollinators may have played an important role in the diversification of visual floral traits within the genus. On the other hand, we found no association between pollinators and the overall scent chemistry of the flowers that they visited. This indicates that various olfactory cue combinations may attract similar pollinator assemblages, or that chemical compounds involved in pollinator attraction comprise only a small subset of all emitted compounds. Overall, these results suggest that adaptations to pollinators have influenced floral trait evolution within Ferraria.

Unique neural coding of crucial versus irrelevant plant odors in a hawkmoth.

The sense of smell is pivotal for nocturnal moths to locate feeding and oviposition sites. However, these crucial resources are often rare and their bouquets are intermingled with volatiles emanating from surrounding 'background' plants. Here, we asked if the olfactory system of female hawkmoths, Manduca sexta, could differentiate between crucial and background cues. To answer this question, we collected nocturnal headspaces of numerous plants in a natural habitat of M. sexta. We analyzed the chemical composition of these headspaces and used them as stimuli in physiological experiments at the antenna and in the brain. The intense odors of floral nectar sources evoked strong responses in virgin and mated female moths, most likely enabling the localization of profitable flowers at a distance. Bouquets of larval host plants and most background plants, in contrast, were subtle, thus potentially complicating host identification. However, despite being subtle, antennal responses and brain activation patterns evoked by the smell of larval host plants were clearly different from those evoked by other plants. Interestingly, this difference was even more pronounced in the antennal lobe of mated females, revealing a status-dependent tuning of their olfactory system towards oviposition sites. Our study suggests that female moths possess unique neural coding strategies to find not only conspicuous floral cues but also inconspicuous bouquets of larval host plants within a complex olfactory landscape.

Memory and the value of social information in foraging bumble bees.

Not all information should be learned and remembered. The value of information is tied to the reliability and certainty of that information, which itself is determined by rates of environmental change, both within and across lifetimes. Theory of adaptive forgetting and remembering posits that memory should reflect the environment, with more valuable information remembered for longer amounts of time. Theory on biological preparedness predicts that rates of reliability through evolutionary time should influence what is learned and remembered. We use these ideas to predict that differential memory use will reflect the underlying value of the information being learned. We test this by comparing the learning and memory of social information versus floral information in foraging bumble bees. Bumble bees are extremely flexible in their use of both types of information and evidence suggests that social information is "special," reflecting biological preparedness. Our experiment tests how bumble bees learn and remember social and floral information when their reliabilities, and thus value, differ. We find that bees learn both types of information at a similar speed. Bees show a decrement of memory of the trained associations in both treatments, but retain trained socially reliable information for longer, at both 4-hour and 8-hour retention intervals. Both training treatments influence whether bees match or avoid the locations of demonstrators, and this interacts with retention interval. Bees trained under reliable floral cues and unreliable social cues avoid conspecifics after 8-hr and 24-hr retention intervals. Bees thus learn about the reliability or unreliability of social cues and use this to modify their choices across time.

Florivory and Pollination Intersection: Changes in Floral Trait Expression Do Not Discourage Hummingbird Pollination.

Many flowers are fed on by florivores, but we know little about if and how feeding on flowers affects their visual and chemical advertisement and nectar resource, which could disrupt pollination. Here, we investigated if damages caused by florivores compromise a Neotropical hummingbird pollination system, by modifying the floral advertisements and the nectar resource. We surveyed natural florivory levels and patterns, examined short-term local effects of floral damages caused by the most common florivore, a caterpillar, on floral outline, intra-floral colour pattern and floral scent, as well as on the amount of nectar. Following, we experimentally tested if the most severe florivory pattern affected hummingbird pollination. The feeding activity of the most common florivore did not alter the intra-floral colour pattern, floral scent, and nectar volume, but changed the corolla outline. However, this change did not affect hummingbird pollination. Despite visual floral cues being important for foraging in hummingbirds, our results emphasise that changes in the corolla outline had a neutral effect on pollination, allowing the maintenance of florivore–plant–pollinator systems without detriment to any partner.

Leaf Induction Impacts Behavior and Performance of a Pollinating Herbivore

Flowering plants use volatiles to attract pollinators while deterring herbivores. Vegetative and floral traits may interact to affect insect behavior. Pollinator behavior is most likely influenced by leaf traits when larval stages interact with plants in different ways than adult stages, such as when larvae are leaf herbivores but adult moths visit flowers as pollinators. Here, we determine how leaf induction and corresponding volatile differences in induced plants influence behavior in adult moths and whether these preferences align with larval performance. We manipulated vegetative induction in four Nicotiana species. Using paired induced and control plants of the same species with standardized artificial flowers, we measured foraging and oviposition choices by their ecologically and economically important herbivore/pollinator, Manduca sexta. In parallel, we measured growth rates of M. sexta larvae fed leaves from control or induced plants to determine if this was consistent with female oviposition preference. Lastly, we used plant headspace collections and gas chromatography to quantify volatile compounds from both induced and control leaves to link changes in plant chemistry with moth behavior. In the absence of floral chemical cues, vegetative defensive status influenced adult moth foraging preference from artificial flowers in one species (N. excelsior), where females nectared from induced plants more often than control plants. Plant vegetative resistance consistently influenced oviposition choice such that moths deposited more eggs on control plants than on induced plants of all four species. This oviposition preference for control plants aligned with higher larval growth rates on control leaves compared with induced leaves. Control and induced plants of each species had similar leaf volatile profiles, but induced plants had higher emission levels. Leaves of N. excelsior produced the most volatile compounds, including some inducible compounds typically associated with floral scent. We demonstrate that vegetative plant defensive volatiles play a role in host plant selection and that insects assess information from leaves differently when choosing between nectaring and oviposition locations. These results underscore the complex interactions between plants, their pollinators, and herbivores.

Electric field detection as floral cue in hoverfly pollination

Pollinators can detect the color, shape, scent, and even temperature of the flowers they want to visit. Here, we present the previously unappreciated capacity of hoverflies (Eristalis tenax and Cheilosia albipila) to detect the electric field surrounding flowers. Using hoverflies as key dipteran pollinators, we explored the electrical interactions between flies and flowers—how a hoverfly acquired a charge and how their electrical sensing ability for target flowers contributed to nectar identification and pollination. This study revealed that rapid variations in a floral electric field were related to a nectar reward and increased the likelihood of the fly’s return visits. We found that thoracic hairs played a role in the polarity of hoverfly charge, revealing their electro-mechanosensory capability, as in bumblebees (Bombus terrestris). Electrophysiological analysis of the hoverfly’s antennae did not reveal neural sensitivity to the electric field, which favors the mechanosensory hairs as putative electroreceptive organs in both species of hoverflies.

Floral Cues of Non-host Plants Attract Oligolectic Chelostoma rapunculi Bees

Oligolectic bees are highly dependent on the availability of the host plants to which they are specialized. Nevertheless, females ofChelostoma rapunculihave recently been monitored occasionally to visitMalva moschataandGeranium sanguineumflowers, in addition to their well-knownCampanulaspp. hosts. The questions therefore arise which floral cues promote visits to non-host plants. As host-specific floral cues are key attractants for oligolectic bees, we have studied the attractiveness of olfactory and visual cues of the established hostCampanula tracheliumin comparison to the non-host plantsG. sanguineumandM. moschatain behavioral experiments. Chemical and electrophysiological analyses of the floral scent and spectral measurements of floral colors were used to compare and contrast host and non-host plants. The behavioral experiments showed that foraging-naïve bees, in particular, were attracted by olfactory cues of the non-host plants, and that they did not favor theCampanulahost scent in choice experiments. Many electrophysiologically active floral volatiles were present in common in the studied plants, although each species produced an individual scent profile. Spiroacetals, the key components that enableC. rapunculito recognizeCampanulahosts, were detected in trace amounts inGeraniumbut could not be proved to occur inMalva. The visual floral cues of all species were particularly attractive for foraging-experienced bees. The high attractiveness ofG. sanguineumandM. moschataflowers toC. rapunculibees and the floral traits that are similar to theCampanulahost plants can be a first step to the beginning of a host expansion or change which, however, rarely occurs in oligolectic bees.

Differential Evolutionary History in Visual and Olfactory Floral Cues of the Bee-Pollinated Genus Campanula (Campanulaceae).

Visual and olfactory floral signals play key roles in plant-pollinator interactions. In recent decades, studies investigating the evolution of either of these signals have increased considerably. However, there are large gaps in our understanding of whether or not these two cue modalities evolve in a concerted manner. Here, we characterized the visual (i.e., color) and olfactory (scent) floral cues in bee-pollinated Campanula species by spectrophotometric and chemical methods, respectively, with the aim of tracing their evolutionary paths. We found a species-specific pattern in color reflectance and scent chemistry. Multivariate phylogenetic statistics revealed no influence of phylogeny on floral color and scent bouquet. However, univariate phylogenetic statistics revealed a phylogenetic signal in some of the constituents of the scent bouquet. Our results suggest unequal evolutionary pathways of visual and olfactory floral cues in the genus Campanula. While the lack of phylogenetic signal on both color and scent bouquet points to external agents (e.g., pollinators, herbivores) as evolutionary drivers, the presence of phylogenetic signal in at least some floral scent constituents point to an influence of phylogeny on trait evolution. We discuss why external agents and phylogeny differently shape the evolutionary paths in floral color and scent of closely related angiosperms.

Comparison of color‐learning rates among eight species of three insect orders (Hymenoptera, Diptera, and Lepidoptera)

AbstractLearning plays an important role in food acquisition in a wide range of insect species. However, few studies have explored differences in the ability to learn floral cues among pollinator species across insect orders. In this study, we examined associative learning of flower color with nectar rewards for females or female workers in two bee species (an eusocial bumblebee [Bombus ignitus] and a solitary mason bee [Osmia orientalis]) and two hoverfly species (Eristalis cerealis and E. tenax). Prior data for females of four butterfly species (Idea leuconoe, Argyreus hyperbius, Pieris rapae, and Lycaena phlaeas) were included for analyses of flower color‐learning rate in a total of eight species of three insect orders (Hymenoptera, Diptera, and Lepidoptera). All eight species learned flower colors associated with food. Flower color‐learning rate was highest in B. ignitus, followed by the two larger butterflies (I. leuconoe and A. hyperbius), the two smaller butterflies (P. rapae and L. phlaeas), and the remaining species (E. cerealis, E. tenax, and O. orientalis). These results represent the first evidence that the ability to learn floral cues differs among flower‐visiting insects of different orders. We discuss the adaptive significance of superior learning abilities in bumblebees and butterflies and that of inferior learning abilities in the two hoverflies and mason bees.

Bumblebees can detect floral humidity.

ABSTRACTFloral humidity, a region of elevated humidity in the headspace of the flower, occurs in many plant species and may add to their multimodal floral displays. So far, the ability to detect and respond to floral humidity cues has been only established for hawkmoths when they locate and extract nectar while hovering in front of some moth-pollinated flowers. To test whether floral humidity can be used by other more widespread generalist pollinators, we designed artificial flowers that presented biologically relevant levels of humidity similar to those shown by flowering plants. Bumblebees showed a spontaneous preference for flowers that produced higher floral humidity. Furthermore, learning experiments showed that bumblebees are able to use differences in floral humidity to distinguish between rewarding and non-rewarding flowers. Our results indicate that bumblebees are sensitive to different levels of floral humidity. In this way floral humidity can add to the information provided by flowers and could impact pollinator behaviour more significantly than previously thought.