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Multimodal floral recognition by bumblebees
Abstract
Flowers present information to their insect visitors in multiple simultaneous sensory modalities. Research has commonly focussed on information presented in visual and olfactory modalities. Recently, focus has shifted towards additional 'invisible' information, and whether information presented in multiple modalities enhances the interaction between flowers and their visitors. In this review, we highlight work that addresses how multimodality influences behaviour, focussing on work conducted on bumblebees (Bombus spp.), which are often used due to both their learning abilities and their ability to use multiple sensory modes to identify and differentiate between flowers. We review the evidence for bumblebees being able to use humidity, electrical potential, surface texture, and temperature as additional modalities, and consider how multimodality enhances their performance. We consider mechanisms, including the cross-modal transfer of learning that occurs when bees are able to transfer patterns learnt in one modality to an additional modality without additional learning.
... Bumble bees provide an excellent model in which to examine behavioural aspects of switching food resources. A great deal is known about cues used by bumble bees to find flowers (Chittka, 2022;Rands et al., 2023). How bumble bees perceive colour cues can be assessed using a colour coding system that is widespread in Hymenoptera (Chittka, 1992;Chittka et al., 1992;Lunau et al., 1996). ...
... The temperatures of floral surfaces, such as petals and reproductive structures, also influence how floral visitors respond to flowers. Differences in the temperature of the floral surfaces between flowers can influence pollinator foraging choices, acting as part of the flower's multimodal display (Hammer et al., 2009;Leonard et al., 2012;Raguso, 2004;Rands et al., 2023;Whitney et al., 2008). ...
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.
... Flowers provide a diversity of sensory information to pollinators (e.g. color, shape, patterning, electrostatic fields) (reviewed by Sommer et al. 2022 [16], Rands et al 2023 [17]). These signals are information-rich; improving detection, discrimination, and learning [18][19][20][21]. ...
Bumblebees rely on diverse sensory information to locate flowers while foraging. The majority of research exploring the relationship between visual and olfactory floral cues is performed at local spatial scales and applicable to understanding floral selection. Floral cue-use during search remains underexplored. This study investigates how the bumblebee Bombus impatiens uses visual versus olfactory information from flowers across behavioral states and spatial scales. At local spatial scales, non-flying animals in an associative learning paradigm will access learned multimodal cues in an elemental fashion - where a single component of the cue is capable of eliciting responses. However, bumblebees flying in a windtunnel shift cue-use strategy depending on the spatiotemporal scale of cue encounter. When both color and odor cues mimic local/ within patch spatial scale, bumblebees exhibit a gradient of elemental responses - with highest responses to the complete multimodal color+odor cue, followed by intact color, then intact odor. When cues mimic an intermediate/ between patch spatial scale, bumblebees exhibit configural responses to the learned cue - with high responses to only the learned color+odor cue. Thus the underlying physiological state, sensitive to both activity level and spatiotemporal scale of sensory information, is modulating encoding and utilization of multimodal floral cues.
The orchid family is renowned for its enormous diversity in pollination biology. Many orchid species use deception to attract pollinators, and the main strategy in terrestrial orchids is food deception. Food‐deceptive orchids usually show a low number of pollinator visitations, making field observations of pollinators difficult.
In this study visual census, pollinator capture and molecular analysis of pollinaria found on caught insects allowed us to obtain information on species composition of orchid pollinators.
A total of 321 insects were caught; most specimens were hymenopterans ( Apis mellifera , Bombus ruderatus and Eucera rufa ) and coleopterans ( Tropinota hirta and T. squalida ). The identity of species to which pollinaria found on the insect's body belonged was confirmed by molecular analysis. Moreover, some individuals of Billaea lata (Tachinidae, Diptera) were captured and photographed with the pollinaria on their head.
Two new and important results emerged clearly in this work: a dipteran, Billaea lata , pollinator of Anacamptis pyramidalis , and two beetles in the genus Tropinota are pollinators of Orchis italica . Our results confirm that generalized food‐deceptive orchids of the genera Orchis and Anacamptis show weak pollinator specificity.
Nectar foraging bees change their use of floral resources as plant species appear in the environment and disappear over their lifetimes. The new flowers used may involve different cues and different nectar extraction tactics. Although bumble bees can adapt to changes in floral cues and required tactics, little is known about whether bees prioritize switching tactics or floral cues when deciding which plant species to switch to. In a laboratory assay, we forced Bombus impatiens (common eastern bumble bee) workers either to switch the handling tactic they were using or to continue using the tactic but to switch the colour of artificial flowers foraged on. We examined whether bees’ tendency to change their tactics was influenced by how similar in colour novel flowers were to familiar ones. We conducted a 2 × 2 factorial experiment using artificial flowers, manipulating the handling tactic that bees were initially trained (legitimate visitation or nectar robbing) and the similarity between novel and trained colours (similar or distinct). We found that under most conditions bees preferred to switch flower colours and retain handling tactics. However, when given experience with legitimate visitation and when novel flowers were markedly different in colour from those they had experienced previously, bees tended to switch tactic while continuing to forage on flowers of the same colour. These findings suggest that the similarity in colour of a new floral resource to the currently exploited resource, along with the flower handling tactic employed by bees, jointly plays an important role in decision-making by foraging bumble bees.
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.
Recent investigations highlight the possibility of electroreception within
arthropods through charged mechanosensory hairs. This discovery raises questions about the influence of electrostatic interaction between hairs and surrounding electrical fields within this sensory modality. Here, we investigate these questions by studying electrostatic coupling in arrays of hairs. We establish the notion of sensitivity contours that indicate regions within which point charges deflect hairs beyond a given threshold. We then examine how the contour’s shape and size and the overall hair behaviour change in response to variations in the coupling between hairs. This investigation unveils synergistic behaviours whereby the sensitivity of hairs is enhanced or inhibited by neighbouring hairs. The hair spacing and ratio of a system’s electrical parameters to its mechanical parameters influence this behaviour.
Our results indicate that electrostatic interaction between hairs leads to
emergent sensory properties for biologically relevant parameter values.
The analysis raises new questions around the impact of electrostatic interaction on the current understanding of sensory hair processes, such as acoustic sensing, unveiling new sensory capabilities within electroreception such as amplification of hair sensitivity and location detection of charges in the environment.
Main conclusion
Using petrolatum gel as an antitranspirant on the flowers of California poppy and giant bindweed, we show that transpiration provides a large contribution to floral humidity generation.
Abstract
Floral humidity, an area of elevated humidity in the headspace of flowers, is believed to be produced predominantly through a combination of evaporation of liquid nectar and transpirational water loss from the flower. However, the role of transpiration in floral humidity generation has not been directly tested and is largely inferred by continued humidity production when nectar is removed from flowers. We test whether transpiration contributes to the floral humidity generation of two species previously identified to produce elevated floral humidity, Calystegia silvatica and Eschscholzia californica. Floral humidity production of flowers that underwent an antitranspirant treatment, petrolatum gel which blocks transpiration from treated tissues, is compared to flowers that did not receive such treatments. Gel treatments reduced floral humidity production to approximately a third of that produced by untreated flowers in C. silvatica, and half of that in E. californica. This confirms the previously untested inferences that transpiration has a large contribution to floral humidity generation and that this contribution may vary between species.
Gaze direction is closely coupled with body movement in insects and other animals. If movement patterns interfere with the acquisition of visual information, insects can actively adjust them to seek relevant cues. Alternatively, where multiple visual cues are available, an insect’s movements may influence how it perceives a scene. We show that the way a foraging bumblebee approaches a floral pattern could determine what it learns about the pattern. When trained to vertical bicoloured patterns, bumblebees consistently approached from below centre in order to land in the centre of the target where the reward was located. In subsequent tests, the bees preferred the colour of the lower half of the pattern that they predominantly faced during the approach and landing sequence. A predicted change of learning outcomes occurred when the contrast line was moved up or down off-centre: learned preferences again reflected relative frontal exposure to each colour during the approach, independent of the overall ratio of colours. This mechanism may underpin learning strategies in both simple and complex visual discriminations, highlighting that morphology and action patterns determines how animals solve sensory learning tasks. The deterministic effect of movement on visual learning may have substantially influenced the evolution of floral signals, particularly where plants depend on fine-scaled movements of pollinators on flowers.
Electricity, the interaction between electrically charged objects, is widely known to be fundamental to the functioning of living systems. However, this appreciation has largely been restricted to the scale of atoms, molecules, and cells. By contrast , the role of electricity at the ecological scale has historically been largely neglected, characterised by punctuated islands of research infrequently connected to one another. Recently, however, an understanding of the ubiquity of electrical forces within the natural environment has begun to grow, along with a realisation of the multitude of ecological interactions that these forces may influence. Herein, we provide the first comprehensive collation and synthesis of research in this emerging field of electric ecology. This includes assessments of the role electricity plays in the natural ecology of predator-prey interactions, pollination, and animal dispersal, among many others, as well as the impact of anthropogenic activity on these systems. A detailed introduction to the ecology and physiology of electroreception-the biological detection of ecologically relevant electric fields-is also provided. Further to this, we suggest avenues for future research that show particular promise, most notably those investigating the recently discovered sense of aerial electroreception.
Buzz pollination encompasses the evolutionary convergence of specialised floral morphologies and pollinator behaviour in which bees use vibrations (floral buzzes) to remove pollen. Floral buzzes are one of several types of vibrations produced by bees using their thoracic muscles. Here I review how bees can produce these different types of vibrations and discuss the implications of this mechanistic understanding for buzz pollination. I propose that bee buzzes can be categorised according to their mode of production and deployment into: (1) thermogenic, which generate heat with little mechanical vibration; (2) flight buzzes, which combined with wing deployment and thoracic vibration, power flight, and (3) non-flight buzzes in which the thorax vibrates but the wings remain folded, and include floral, defence, mating, communication, and nest-building buzzes. I hypothesise that the characteristics of non-flight buzzes, including floral buzzes, can be modulated by bees via modification of the biomechanical properties of the thorax through activity of auxiliary muscles, changing the rate of activation of the indirect flight muscles, and modifying flower handling behaviours. Thus, bees should be able to fine-tune mechanical properties of their floral vibrations, including frequency and amplitude, depending on flower characteristics and pollen availability to optimise energy use and pollen collection.
Floral 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 which produced higher floral humidity. Furthermore, learning experiments showed that bumblebees are able to use differences in floral humidity to distinguish between rewarding and nonrewarding 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.
Some species of bees restrict foraging to the twilight period before sunrise or after sunset. Among the plants sought by these nocturnal bees are species described as chiropterophilous, such as Caryocar brasiliense. The flowers of this species open in the evening and provide resources until dawn. We determined the pattern of flower visitation by nocturnal bees and their role in pollination and fruit set of C. brasiliense and evaluated its importance as floral resource for nocturnal bees. We analyzed the pollen composition of cell provisions of nocturnal bees of Ptiloglossa (Colletidae) and compared its scent with floral scent compounds of C. brasiliense. Moreover, we conducted a pollinator exclusion experiment to determine the contribution of nocturnal bees to its fruit set. Disregarding bats, Ptiloglossa latecalcarata and two species of Megalopta (Halictidae) were consistent nectar and pollen gathering visitors, along with some social diurnal bees. The visitor exclusion experiment revealed that bee visits do not result in fruit set, which only occurs through visits by bats. The flowers supply a significant amount of pollen for nocturnal bees, as demonstrated through pollen analysis of brood cells and scopa loads. This interaction, therefore, is only beneficial to the commensalist bees. The scent collected from brood cells was dominated by hexanoic acid and 1-hexanol and differed strongly from the floral scent of C. brasiliense. These results substantiate that bat-pollinated flowers are an important part of the food niche of nocturnal bees, which implies that they are sensorially equipped to recognize floral traits shaped by bats.
Similar to animal communication displays, flowers emit complex signals that attract pollinators. Signal complexity could lead to higher cognitive load, impairing performance, or might benefit pollinators by facilitating learning, memory and decision-making. Here, we evaluate learning and memory in foragers of the bumble bee Bombus impatiens trained to simple (unimodal) vs. complex signals (bimodal) under restrained conditions. Use of a proboscis extension response protocol enabled us to control the timing and duration of stimuli presented during absolute and differential learning tasks. Overall, we observed broad variation in the performance under the two conditions, with bees trained to compound bimodal signals learning and remembering as well as, better, or more poorly than bees trained to unimodal signals. Interestingly, the outcome of training was affected by the specific colour-odour combination. Among unimodal stimuli, the performance with odour stimuli was higher than with colour stimuli, suggesting that olfactory signals played a more significant role in the compound bimodal condition. This was supported by the fact that after 24 h, most bimodal-treatment bees responded to odour but not visual stimuli. We did not observe differences in latency of response, suggesting that signal composition affected decision accuracy, not speed. We conclude that restrained bumble bee workers exhibit broad variation of responses to bimodal stimuli and that components of the bimodal signal may not be used equivalently. The analysis of bee performance under restrained conditions enables accurately control the multimodal stimuli provided to individuals and to study the interaction of individual components within a compound.
The area of space immediately around the floral display is likely to have an increased level of humidity relative to the environment around it, due to both nectar evaporation and floral transpiration. This increased level of floral humidity could act as a close-distance cue for pollinators or influence thermoregulation, pollen viability and infection of flowers by fungal pathogens. However, with a few exceptions, not much is known about the patterns of floral humidity in flowering plants or the physiological traits that result in its generation. We conducted a survey of 42 radially symmetrical flower species (representing 21 widely spread families) under controlled conditions. Humidity was measured using a novel robot arm technique that allowed us to take measurements along transects across and above the floral surface. The intensity of floral humidity was found to vary between different flower species. Thirty of the species we surveyed presented levels of humidity exceeding a control comparable to background humidity levels, while twelve species did not. Patterns of floral humidity also differed across species. Nevertheless, floral humidity tended to be highest near the center of the flower, and decreased logarithmically with increasing distance above the flower, normally declining to background levels within 30 mm. It remains unclear how physiological traits influence the diversity of floral humidity discovered in this survey, but floral shape seems to also influence floral humidity. These results demonstrate that floral humidity may occur in a wide range of species and that there might be greater level of diversity and complexity in this floral trait than previously known.
Floral guides are signal patterns that lead pollinators to floral rewards after they have located the flower, and increase foraging efficiency and pollen transfer. Patterns of several floral signalling modalities, particularly colour patterns, have been identified as being able to function as floral guides. Floral temperature frequently shows patterns that can be used by bumblebees for locating and recognising the flower, but whether these temperature patterns can function as a floral guide has not been explored. Furthermore, how combined patterns (using multiple signalling modalities) affect floral guide function has only been investigated in a few modality combinations. We assessed how artificial flowers induce behaviours in bumblebees when rewards are indicated by unimodal temperature patterns, unimodal colour patterns or multimodal combinations of these. Bees visiting flowers with unimodal temperature patterns showed an increased probability of finding rewards and increased learning of reward location, compared to bees visiting flowers without patterns. However, flowers with contrasting unimodal colour patterns showed further guide-related behavioural changes in addition to these, such as reduced reward search times and attraction to the rewarding feeder without learning. This shows that temperature patterns alone can function as a floral guide, but with reduced efficiency. When temperature patterns were added to colour patterns, bees showed similar improvements in learning reward location and reducing their number of failed visits in addition to the responses seen to colour patterns. This demonstrates that temperature pattern guides can have beneficial effects on flower handling both when alone or alongside colour patterns.
The epidermal cells of flowers come in different shapes and have different functions, but how they evolved remains largely unknown. Floral micro‐texture can provide tactile cues to insects, and increases in surface roughness by means of conical (papillose) epidermal cells may facilitate flower handling by landing insect pollinators. Whether flower microstructure correlates with pollination system remains unknown.
Here, we investigate the floral epidermal microstructure in 29 (congeneric) species pairs with contrasting pollination system. We test whether flowers pollinated by bees and/or flies feature more structured, rougher surfaces than flowers pollinated by non‐landing moths or birds and flowers that self‐pollinate.
In contrast with earlier studies, we find no correlation between epidermal microstructure and pollination system. The shape, cell height and roughness of floral epidermal cells varies among species, but is not correlated with pollinators at large. Intriguingly, however, we find that the upper (adaxial) flower surface that surrounds the reproductive organs and often constitutes the floral display is markedly more structured than the lower (abaxial) surface.
We thus conclude that conical epidermal cells probably play a role in plant reproduction other than providing grip or tactile cues, such as increasing hydrophobicity or enhancing the visual signal.
Neonicotinoid pesticides can impair bees’ ability to learn and remember information about flowers, critical for effective foraging. Although these effects on cognition may contribute to broader effects on health and performance, to date they have largely been assayed in simplified protocols that consider learning in a single sensory modality, usually olfaction. Given that real flowers display a variety of potentially useful signals, we assessed the effects of acute neonicotinoid exposure on multimodal learning in freeflying
bumblebees. We found that neonicotinoid consumption differentially
impacted learning of floral stimuli, impairing scent, but not colour, learning. These findings raise questions about the mechanisms by which pesticides might differentially impair sensory systems, with implications for how neonicotinoids affect multiple aspects of bee ecology.
Background:
Obtaining an optimal flower temperature can be crucial for plant reproduction because temperature mediates flower growth and development, pollen and ovule viability, and influences pollinator visitation. The thermal ecology of flowers is an exciting, yet understudied field of plant biology.
Scope:
This review focuses on several attributes that modify exogenous heat absorption and retention in flowers. We discuss how flower shape, orientation, heliotropic movements, pubescence, coloration, opening-closing movements and endogenous heating contribute to the thermal balance of flowers. Whenever the data are available, we provide quantitative estimates of how these floral attributes contribute to heating of the flower, and ultimately plant fitness.
Outlook:
Future research should establish form-function relationships between floral phenotypes and temperature, determine the fitness effects of the floral microclimate, and identify broad ecological correlates with heat capture mechanisms.
Bumblebees Bombus terrestris are good at learning to distinguish between patterned flowers. They can differentiate between flowers that differ only in their patterning of scent, surface texture, temperature, or electrostatic charge, in addition to visual patterns. As recently shown, bumblebees trained to discriminate between nonvisual scent patterns can transfer this learning to visually patterned flowers that show similar spatial patterning to the learnt scent patterns. Bumblebees can, therefore, transfer learnt patterns between different sensory modalities, without needing to relearn them. We used differential conditioning techniques to explore whether cross-modal transfer of learnt patterns also occurred between visual and temperature patterns. Bumblebees that successfully learnt to distinguish rewarding and unrewarding temperature patterns did not show any preferences for the corresponding unlearnt visual pattern. Similarly, bumblebees that learnt visual patterns did not transfer these to temperature patterns, suggesting that they are unable to transfer learning of temperature and visual patterns. We discuss how cross-modality pattern learning may be limited to modalities that have potentially strong neurological links, such as the previously demonstrated transfer between scent and visual patterns.
Trouble at the hive
Neonicotinoid pesticides cause mortality and decline in insect pollinators. One repeatedly noted effect is a reduction in bee colony size. However, the mechanism behind this reduction is unclear. Crall et al. performed complex real-time monitoring of bumblebee behavior within their nests (see the Perspective by Raine). Neonicotinoid exposure reduced nurse and caretaking behaviors, which affected productivity and harmed colony thermoregulation. These changes in behavior acted together to decrease colony viability, even when exposure was nonlethal.
Science , this issue p. 683 ; see also p. 643
Flowers act as multisensory billboards to pollinators by using a range of sensory modalities such as visual patterns and scents. Different floral organs release differing compositions and quantities of the volatiles contributing to floral scent, suggesting that scent may be patterned within flowers. Early experiments suggested that pollinators can distinguish between the scents of differing floral regions, but little is known about how these potential scent patterns might influence pollinators. We show that bumblebees can learn different spatial patterns of the same scent, and that they are better at learning to distinguish between flowers when the scent pattern corresponds to a matching visual pattern. Surprisingly, once bees have learnt the spatial arrangement of a scent pattern, they subsequently prefer to visit novel unscented flowers that have an identical arrangement of visual marks, suggesting that multimodal floral signals may exploit the mechanisms by which learnt information is stored by the bee.
ELife digest
Bees experience the world in a different way to humans. The plants that they visit exploit the bee’s senses to make sure that a searching bee can easily find, handle and pollinate flowers. For example, bumblebees can learn to choose between flowers that are different temperatures, using heat as a way of identifying the best flowers.
Some wild flowers are warmer than others when they grow in their natural environment. Recent advances in technology mean that scientists are now able to take a more detailed look at flower temperature than ever before. Harrap et al. used this technology to look at 118 species of plant, including daisies, rockroses and poppies.
Over half of the plants examined had flowers with complex patterns of heat across their petals, echoing the colourful patterns that we see with our own eyes. On average, some parts of the petals were 4–5°C warmer than the rest. In further experiments, artificial flowers that replicated these patterns showed that bumblebees are able to tell apart flowers with different temperature patterns across their petals.
These newly discovered floral heat patterns appear widespread in nature. It is likely that these patterns are a hidden signal to pollinators that, together with other cues like colour and scent, attracts them to the flowers and helps them locate any reward, like nectar.
As well as opening up a new field of research in understanding the interactions between plants and their pollinators, these findings are potentially important given current concerns about climate change. If pollinators are partly reliant on subtle differences in temperature across the surface of a petal, then even small changes in the temperature of the environment could have a large and unanticipated influence on how efficient bees and other pollinators are when they are visiting flowers with hidden heat patterns.
The majority of floral displays simultaneously broadcast signals from multiple sensory modalities, but these multimodal displays come at both a metabolic cost and an increased conspicuousness to floral antagonists. Why then do plants invest in these costly multimodal displays? The efficacy backup hypothesis suggests that individual signal components act as a backup for others in the presence of environmental variability. Here, we test the efficacy backup hypothesis by investigating the ability of bumblebees to differentiate between sets of artificial flowers in the presence of either chemical interference or high wind speeds, both of which have the potential to impede the transmission of olfactory signals. We found that both chemical interference and high wind speeds negatively affected forager learning times, but these effects weremitigated in the presence of a visual signal component. Our results suggest that visual signals can act as a backup for olfactory signals in the presence of chemical interference and high wind speeds, and support the efficacy backup hypothesis as an explanation for the evolution of multimodal floral displays.
Significance
The coeveolution of flowers and pollinators is well known, but how generalist pollinators identify suitable flowers across environments and flower species is not well understood. Hoverflies, which are found across the globe, are one of the most important alternative pollinators after bees and bumblebees. Here we measured, predicted, and finally recreated multimodal cues from individual flowers visited by hoverflies in three different environments (hemiboreal, alpine, and tropical). We found that although “flower signatures” were unique for each environment, some cues were ubiquitously attractive, despite not resembling cue combinations from real flowers. Our results provide unique insights into how a cosmopolitan pollinator identifies flower objects across environments, which has important implications for our understanding of pollination as a global ecological service.
Our understanding of how floral visitors integrate visual and olfactory cues when seeking food, and how background complexity affects flower detection is limited. Here, we aimed to understand the use of visual and olfactory information for bumblebees (Bombus terrestris terrestris L.) when seeking flowers in a visually complex background. To explore this issue, we first evaluated the effect of flower colour (red and blue), size (8, 16 and 32 mm), scent (presence or absence) and the amount of training on the foraging strategy of bumblebees (accuracy, search time and flight behaviour), considering the visual complexity of our background, to later explore whether experienced bumblebees, previously trained in the presence of scent, can recall and make use of odour information when foraging in the presence of novel visual stimuli carrying a familiar scent. Of all the variables analysed, flower colour had the strongest effect on the foraging strategy. Bumblebees searching for blue flowers were more accurate, flew faster, followed more direct paths between flowers and needed less time to find them, than bumblebees searching for red flowers. In turn, training and the presence of odour helped bees to find inconspicuous (red) flowers. When bees foraged on red flowers, search time increased with flower size; but search time was independent of flower size when bees foraged on blue flowers. Previous experience with floral scent enhances the capacity of detection of a novel colour carrying a familiar scent, probably by elemental association influencing attention.
Floral displays are often composed of areas of contrasting stimuli which flower visitors use as guides, increasing both foraging efficiency and the likelihood of pollen transfer. Many aspects of how these displays benefit foraging efficiency are still unexplored, particularly those surrounding multimodal signals and the spatial arrangement of the display components. We compare the nectar discovery times of forager bumblebees (Bombus terrestris) when presented with artificial flowers with unimodal or compound displays of visual and/or olfactory stimuli, positioned in either radiating or non-radiating arrangements. We found that the addition of individual display components from either modality reduces nectar discovery time but there was no time benefit to bimodal displays over unimodal displays or any benefit to radiating stimuli arrangements over non-radiating arrangements. However, preference tests revealed a time advantage to radiating unimodal visual patterns over non-radiating unimodal visual patterns when both types were displayed simultaneously. These results suggest that the benefits of multimodal stimuli arrangements to pollinators are unrelated to benefits in nectar discovery time. Our results also suggest that spatial patterns of scent can be used as nectar guides and can reduce nectar discovery times without the aid of visual stimuli.
Bees and flowering plants have a long-standing and remarkable co-evolutionary history. Flowers and bees evolved traits that enable pollination, a process that is as important to plants as it is for pollinating insects. From the sensory ecological viewpoint, bee-flower interactions rely on senses such as vision, olfaction, humidity sensing, and touch. Recently, another sensory modality has been unveiled; the detection of the weak electrostatic field that arises between a flower and a bee. Here, we present our latest understanding of how these electric interactions arise and how they contribute to pollination and electroreception. Finite-element modelling and experimental evidence offer new insights into how these interactions are organised and how they can be further studied. Focussing on pollen transfer, we deconstruct some of the salient features of the three ingredients that enable electrostatic interactions, namely the atmospheric electric field, the capacity of bees to accumulate positive charge, and the propensity of plants to be relatively negatively charged. This article also aims at highlighting areas in need of further investigation, where more research is required to better understand the mechanisms of electrostatic interactions and aerial electroreception.
Flower visits are complex encounters, in which animals are attracted by floral signals, guided toward the site of the first physical contact with a flower, land, and finally take up floral rewards. At close range, signals of stamens and pollen play an important role to facilitate flower handling in bees, yet the pollen stimuli eliciting behavioral responses are poorly known. In this study, we test the response of flower-naive bumblebees (Bombus terrestris) toward single and multimodal pollen stimuli as compared to natural dandelion pollen. As artificial pollen stimuli, we used the yellow flavonoid pigment quercetin, the scent compound eugenol, the amino acid proline, the monosaccharide glucose, and the texture of pollen-grain-sized glass pellets as a tactile stimulus. Three test stimuli, dandelion pollen, one out of various uni- and multimodal stimulus combinations, and a solvent control were presented simultaneously to individual bumblebees, whose response was recorded. The results indicate that bumblebees respond in an irreversible sequence of behavioral reactions. Bumblebees approached the visual stimulus quercetin as often as natural dandelion pollen. An additional olfactory stimulus resulted in slightly more frequent landings. The multimodal stimulus combinations including visual, olfactory, gustatory, and tactile stimuli elicited approaches, antennal contacts, and landings as often as natural pollen. Subsequent reactions like proboscis extension, mandible biting, and buzzing were more often but not regularly observed at dandelion pollen. Our study shows that visual signals of pollen are sufficient to trigger initial responses of bumblebees, whereas multimodal pollen stimuli elicit full behavioral response as compared to natural pollen. Our results suggest a major role of pollen cues for the attraction of bees toward flowers and also explain, why many floral guides mimic the visual signals of pollen and anthers, that is, the yellow and UV-absorbing color, to direct bumblebees toward the site where they access the floral rewards.
Significance
Electroreception in terrestrial animals is poorly understood. In bumblebees, the mechanical response of filiform hairs in the presence of electric fields provides key evidence for electrosensitivity to ecologically relevant electric fields. Mechanosensory hairs in arthropods have been shown to function as fluid flow or sound particle velocity receivers. The present work provides direct evidence for additional, nonexclusive functionality involving electrical Coulomb-force coupling between distant charged objects and mechanosensory hairs. Thus, the sensory mechanism is proposed to rely on electromechanical coupling, whereby many light thin hairs serve the detection of the electrical field surrounding a bumblebee approaching a flower. This finding prompts the possibility that other terrestrial animals use such sensory hairs to detect and respond to electric fields.
Attentional demands can prevent humans and other animals from performing multiple tasks simultaneously. Some studies, however, show that tasks presented in different sensory modalities (e.g. visual and auditory) can be processed simultaneously. This suggests that, at least in these cases, attention might be modality-specific and divided differently between tasks when present in the same modality compared with different modalities. We investigated this possibility in bumblebees (Bombus terrestris) using a biologically relevant experimental set-up where they had to simultaneously choose more rewarding flowers and avoid simulated predatory attacks by robotic 'spiders'. We found that when the tasks had to be performed using visual cues alone, bees failed to perform both tasks simultaneously. However, when highly rewarding flowers were indicated by olfactory cues and predators were indicated by visual cues, bees managed to perform both tasks successfully. Our results thus provide evidence for modality-specific attention in foraging bees and establish a novel framework for future studies of crossmodal attention in ecologically realistic settings.
Sensilla are the basic structures that allow the perception of environmental cues that play a role as mechanoreceptors, chemoreceptors, thermoreceptors and hygroreceptors associated with their morphology. Because bees have different degrees of sociability, they are a good model for the study of sensilla types and distribution linked with behaviour. This work identifies the types of sensilla in the antennae of bees with different degrees of sociability. The antennae of 18 species of bee were analysed with a scanning electron microscope. Trichoid and placoid sensilla are present in all antennomers of the species studied. The honey bee Apis mellifera and bumble bee Bombus pauloensis workers have higher diversity and sensillum distribution in comparison with males. In stingless bees, species of Melipona are representative of a homogeneous group for sensilla types and distribution. The types and distribution of sensilla in the antennae of bees seems to be associated with the degree of sociability.
Karl von Frisch's studies of bees' color vision and chemical senses opened a window into the perceptual world of a species other than our own. A century of subsequent research on bees' visual and olfactory systems has developed along two productive but independent trajectories, leaving the questions of how and why bees use these two senses in concert largely unexplored. Given current interest in multimodal communication and recently discovered interplay between olfaction and vision in humans and Drosophila, understanding multisensory integration in bees is an opportunity to advance knowledge across fields. Using a classic ethological framework, we formulate proximate and ultimate perspectives on bees' use of multisensory stimuli. We discuss interactions between scent and color in the context of bee cognition and perception, focusing on mechanistic and functional approaches, and we highlight opportunities to further explore the development and evolution of multisensory integration. We argue that although the visual and olfactory worlds of bees are perhaps the best-studied of any non-human species, research focusing on the interactions between these two sensory modalities is vitally needed.
Plants produce a remarkable variety of displays to attract animals that transfer pollen. These floral displays are usually complex, broadcasting various combinations of visual, olfactory, gustatory, tactile, and thermal stimuli (Raguso 2004a). Even acoustic stimuli may be involved, as in the case of structural nectar guides used by echolocating flower-feeding bats (von Helversen and von Helversen 1999). Yet these sensorially complex advertisements likely evolved from an ancestor that primarily transmitted only chemicals, serving a defensive function (Pellmyr and Thein 1986). The subsequent amplification and elaboration of floral stimuli therefore offers an intriguing opportunity to study signal evolution. However, at present, we know surprisingly little about why floral displays consist of so many elements. This contrasts with progress in other areas: recently, researchers studying topics as diverse as sexual selection, warning displays, animal learning, and parent–offspring communication have explored the function of signal complexity (Rowe 1999; Candolin 2003; Hebets and Papaj 2005; Partan and Marler 2005). Researchers studying plant–pollinator interactions, however, have not to date shown a comparable degree of interest in the topic of complex signals, as judged by an analysis of the research literature. An August 2010 search on the ISI Web of Science® database on journal articles published since 1995 returned only two on plant–pollinator topics containing the words “multimodal” and “signal-” in their titles, abstracts, or keywords (those articles being Raguso and Willis 2002; Kulahci et al. 2008). In comparison, the same search returned 59 articles on sexual selection topics.
Vibrations and sounds, collectively called vibroacoustics, play significant roles in intracolony communication in termites, social wasps, ants, and social bees. Modalities of vibroacoustic signal production include stridulation, gross body movements, wing movements, high-frequency muscle contractions without wing movements, and scraping mandibles or tapping body parts on resonant substrates. Vibroacoustic signals are perceived primarily via Johnston’s organs in the antennae and subgenual organs in the legs. Substrate vibrations predominate as vibroacoustic modalities, with only honey bees having been shown to be able to hear airborne sound. Vibroacoustic messages include alarm, recruitment, colony activation, larval provisioning cues, and food resource assessment. This review describes the modalities and their behavioral contexts rather than electrophysiological aspects, therefore placing emphasis on the adaptive roles of vibroacoustic communication. Although much vibroacoustics research has been done, numerous opportunities exist for continuations and new directions in vibroacoustics research.
Visual and olfactory cues are the first interface between flowers and their visitors and are adaptations to facilitate successful pollination. Initial responses to and associative learning of multimodal cues by flower visitors are based on the perception of colours and volatiles. In this study, we tested how visual, olfactory and multimodal stimuli affect the behaviour of bumblebees (Bombus terrestris) and correlated the properties of 28 stimuli in relation to the insects’ sensory equipment to these behaviours. Initial responses and associative learning were recorded using a radio frequency identification system, tracking the visitation sequences of individual bumblebees to artificial flowers treated with naturally occurring pigments and/or volatiles. The salience of the stimuli was evaluated as the colour contrast to the background and as electroantennogram responses. The main finding was that both initial responses and learning performance were positively correlated to the salience of the stimuli, suggesting that salience is a key feature of flower cues in the interactions with insects. The salience of compound stimuli consisting of two or more pigments and/or volatiles was largely additively determined by the saliences of individual compounds. Potentially, the valence of the stimuli may interfere with the positive relationship between salience and behaviour, which is indicated by our results, too. The salience of multimodal cues depends on the species-specific equipment of visual and olfactory receptors and thus enables flowers to be advertising for some but rather inconspicuous for other flower visitors.
Floral traits that correlate with nectar availability or are linked functionally to nectar production carry the potential to enable remote assessment of energy rewards by pollinators. Such floral traits can be considered "honest" in the sense that they convey information about the quality or profitability of a flower to a pollinator. Recently a new sensory channel used in plant-pollinator interactions was identified. We demonstrated that evaporation of water from the nectar itself and the petals create local humidity gradients above Oenothera cespitosa (Onagraceae) flowers. Since these humidity gradients are directly linked to nectar volume, they convey reliable information about nectar rewards to hawkmoth pollinators (Sphingidae). Several studies document a variety of sensory cues that constitute honest signaling between plants and pollinators, and shed light on the central question of when the two parties should communicate honestly. In the following sections, I will comment on different honest signals mediating plant-pollinator interactions, with a special emphasis on our recent findings about floral humidity gradients.
Flowers and Bees Have “Sparks”
Plants and their pollinators have very intimate interactions, as emphasized by the many classic cases of coevolution among species of each. Such close relationships require signaling between plant and pollinator. Coordination between plant signals and pollinator perception has been shown to exist in flower color, shape, and odor. Clarke et al. (p. 66 , published online 21 February) report the potential for a distinct mode of plant–pollinator communication, electric fields. Natural floral electric fields, which are impacted by visits from naturally charged bees, were easily discriminated by bees, based on their level, pattern, and structure, and improved the rate at which bees remembered the location of a nectar reward.
Flowers produce local humidity that is often greater than that of the surrounding environment, and studies have shown that insect pollinators may be able to use this humidity difference to locate and identify suitable flowers. However, environmental humidity is highly heterogeneous, and is likely to affect the detectability of floral humidity, potentially constraining the contexts in which it can be used as a salient communication pathway between plants and their pollinators. In this study, we use differential conditioning techniques on bumblebees Bombus terrestris audax (Harris) to explore the detectability of an elevated floral humidity signal when presented against different levels of environmental noise. Artificial flowers were constructed that could be either dry or humid, and individual bumblebees were presented with consistent rewards in either the humid or dry flowers presented in an environment with four levels of constant humidity, ranging from low (~20% RH) to highly saturated (~95% RH). Ability to learn was dependent upon both the rewarding flower type and the environment: the bumblebees were able to learn rewarding dry flowers in all environments, but their ability to learn humid rewarding flowers was dependent on the environmental humidity, and they were unable to learn humid rewarding flowers when the environment was highly saturated. This suggests that floral humidity might be masked from bumblebees in humid environments, suggesting that it may be a more useful signal to insect pollinators in arid environments.
Biotremology is a field of study focused on an ancient way of communication by ani- mals endowed with specialized organs for emission and reception of substrate-borne vibrations. Established as a scientific discipline of its own, formally separated from bio- acoustics only recently, biotremology is now rapidly spreading throughout the scientific community, offering valuable cooperation also to numerous other scientific disciplines. Insects, make significant use of substrate-borne vibrational signals and cues for inter- and intraspecific communication, to accomplish many different behaviours. In this chapter, after highlighting the main relations, and differences, between insect acoustic and vibrational communication, we provide a detailed, comprehensive overview of the knowledge and ongoing research in the field of insect biotremology. We particularly emphasise the mechanisms of sensory detection of vibrational signals and cues, and the central neural processing of the received information; the latter especially being dis- cussed in relation to insect auditory processing. In addition, we dedicate considerable attention to the behavioural and ecological aspects of insect vibrational communica- tion, to the methods and instruments of research in neurophysiology and behavioural ecology, as well as the use of acquired basic knowledge in practical applications. Whilst some topics in biotremology, such as the neuronal basis of behaviour, need highly increased research attention, the interest in applied biotremology is rising especially quickly for the high potential offered by substrate-borne vibrations as semiophysicals for pest control. Hence, insects are both the elected study model for basic biotremology research and strongly relevant for agricultural and resource management issues.
Objectives
Floral structures may be warmer than their environment, and can show thermal patterning, where individual floral structures show different temperatures across their surface. Pollinators can differentiate between artificial flowers that mimic both naturally warmed and thermally patterned ones, but it has yet to be demonstrated that these patterns are biologically meaningful. To explore the relationship between pollinators and temperature patterning, we need to know whether there is diversity in patterning, and that these patterns are not simply a by-product of floral architecture constrained by ancestry. We analysed a dataset of 97 species to explore whether intrafloral temperature differences were correlated within clades (phylogenetic signal), or whether the variation seen was diverse enough to suggest that floral temperature patterns are influenced by the abiotic or pollinator-related niches to which plant species are adapted.
Results
Some phylogenetic signal was observed, with both the Asteraceae and species of Pelargonium being more similar than expected by chance, but with other species surveyed not showing signal. The Asteraceae tend to have large temperature differences across the floral surface, which may be due to floral architecture constraints within the family. Other families show no correlation, suggesting that patterning is influenced by pollinators and the environment.
Neonicotinoids have been implicated in the large declines observed in insects such as bumblebees, an important group of pollinators. Neonicotinoids are agonists of nicotinic acetylcholine receptors that are found throughout the insect central nervous system and are the main mediators of synaptic neurotransmission. These receptors are important for the function of the insect central clock and circadian rhythms. The clock allows pollinators to coincide their activity with the availability of floral resources and favorable flight temperatures, as well as impact learning, navigation, and communication. Here we show that exposure to the field-relevant concentration of 10 μg/L imidacloprid caused a reduction in bumblebee foraging activity, locomotion, and foraging rhythmicity. Foragers showed an increase in daytime sleep and an increase in the proportion of activity occurring at night. This could reduce foraging and pollination opportunities, reducing the ability of the colony to grow and reproduce, endangering bee populations and crop yields.
During buzz pollination, bees use their indirect flight muscles to produce vibrations that are transmitted to the flowers and result in pollen release. Although buzz pollination has been known for >100 years, we are still in the early stages of understanding how bee and floral characteristics affect the production and transmission of floral vibrations. Here we analysed floral vibrations produced by four closely related bumblebee taxa (Bombus spp.) on two buzz-pollinated plants species (Solanum spp.). We measured floral vibrations transmitted to the flower to establish the extent to which the mechanical properties of floral vibrations depend on bee and plant characteristics. By comparing four bee taxa visiting the same plant species, we found that peak acceleration (PA), root mean-squared acceleration (RMS) and frequency varies between bee taxa, but that neither bee size (intertegular distance) or flower biomass (dry weight) affect PA, RMS or frequency. A comparison of floral vibrations of two bee taxa visiting flowers of two plant species, showed that, while bee species affects PA, RMS and frequency, plant species affects acceleration (PA and RMS) but not frequency. When accounting for differences in the transmission of vibrations across the two types of flowers, using a species-specific “coupling factor”, we found that RMS acceleration and peak displacement does not differ between plant species. This suggests that bees produce the same initial acceleration in different plants but that transmission of these vibrations through the flower is affected by floral characteristics.
Bumblebees are familiar and charismatic insects, occurring throughout much of the world. They are increasingly being used as a model organism for studying a wide range of ecological and behavioural concepts, such as social organization, optimal foraging theories, host-parasite interactions, and pollination. Recently they have become a focus for conservationists due to mounting evidence of range coBIOL15ANIB and catastrophic extinctions with some species disappearing from entire continents (e.g. in North America). Only by improving our understanding of their ecology can we devise sensible plans to conserve them. The role of bumblebees as invasive species (e.g. Bombus terrestris in Japan) has also become topical with the growing trade in commercial bumblebee nests for tomato pollination leading to establishment of non-native bumblebees in a number of countries. Since the publication of the first edition of the book, there have been hundreds of research papers published on bumblebees. There is clearly a continuing need for an affordable, well-illustrated, and appealing text that makes accessible all of the major advances in understanding of the behaviour and ecology of bumblebees that have been made in the last 30 years.
This chapter discusses sense of hearing among insects. Using sound, vertebrates and insects are often capable of sensing, identifying, and locating their predators, prey, conspecific rivals, and mates by hearing their intentional or unintentional acoustic signals. Natural selection has shaped the form and function of hearing organs (ears) in insects over evolutionary time. In this respect, the ears of insects show much greater diversity than those of vertebrates, for reasons that will be apparent in our discussion. There is tremendous morphological diversity of insect ears. The multitude of different ear designs and locations reflects the unique physical and behavioral challenges faced by each insect. Yet despite their many differences, most ears follow a similar morphological plan. Each typically consists of three identifiable substructures: a tympanal membrane, a tracheal air chamber, and a chordotonal sensory organ. Ears of many nocturnal Lepidoptera, for example, are so thin that they are transparent. Such fragile membranes are typically protected within body cavities or by external flaps of cuticle. In contrast, the thicker, opaque tympanal membranes of some diurnal butterflies or grasshoppers are conspicuously positioned on the outer surface of the body.
The basic building blocks of communication are signals, assembled in various sequences and combinations, and used in virtually all inter- and intra-specific interactions. While signal evolution has long been a focus of study, there has been a recent resurgence of interest and research in the complexity of animal displays. Much past research on signal evolution has focused on sensory specialists, or on single signals in isolation, but many animal displays involve complex signaling, or the combination of more than one signal or related component, often serially and overlapping, frequently across multiple sensory modalities. Here, we build a framework of functional hypotheses of complex signal evolution based on content-driven (ultimate) and efficacy-driven (proximate) selection pressures (sensu Guilford and Dawkins 1991). We point out key predictions for various hypotheses and discuss different approaches to uncovering complex signal function. We also differentiate a category of hypotheses based on inter-signal interactions. Throughout our review, we hope to make three points: (1) a complex signal is a functional unit upon which selection can act, (2) both content and efficacy-driven selection pressures must be considered when studying the evolution of complex signaling, and (3) individual signals or components do not necessarily contribute to complex signal function independently, but may interact in a functional way.
1. Many floral displays are visually complex, transmitting multi‐coloured patterns that are thought to direct pollinators to nectar rewards. These ‘nectar guides’ may be mutually beneficial, if they reduce pollinators’ handling time, leading to an increased visitation rate and promoting pollen transfer. Yet, many details regarding how floral patterns influence foraging efficiency are unknown, as is the potential for pollinator learning to alter this relationship.
2. We compared the responses of bumblebee ( Bombus impatiens Cresson) foragers to artificial flowers that either possessed or lacked star‐like patterns. By presenting each bee with two different foraging scenarios (patterned flowers rewarding/plain flowers unrewarding, plain flowers rewarding/patterned flowers unrewarding) on different days, we were able to assess both short‐ and long‐term effects of patterns on bee foraging behaviour.
3. Bees discovered rewards more quickly on patterned flowers and were less likely to miss the reward, regardless of whether corollas were circular or had petals. Nectar guides’ effect on nectar discovery was immediate (innate) and persisted even after experience, although nectar discovery itself also had a learned component. We also found that bees departed patterned flowers sooner after feeding. Finally, when conditions changed such that flowers no longer provided a reward, bees visited the now‐unrewarding flowers more persistently when they were patterned.
4. On the time‐scale of a single foraging bout, our results provide some of the first data on how pollinators learn to forage efficiently using this common floral trait. Our bees’ persistent response to patterned flowers even after rewards ceased suggests that, rather than being consistently mutually beneficial to plant and pollinator, nectar guide patterns can at times promote pollen transfer for the plant at the expense of a bee’s foraging success.
1. Conical cells in the petal epidermis are common across many diverse flowering plant species, and it was recently shown that in difficult‐to‐handle flowers, pollinators prefer conical cells because they increase grip. However, this does not explain the prevalence of conical cells amongst other, simpler, flowers.
2. The movement of objects is an integral part of the world and is of particular importance to bees because the relative motion of objects is essential to a bee's 3 D vision. The motion of flowers can increase pollinator attraction; however, it also makes flowers more difficult for a bee to handle. This makes foraging more metabolically expensive. To explore whether conical petal cells make handling moving flowers easier, we tested bumblebee ( B ombus terrestris ) preference for conical‐ or flat‐celled P etunia ( P etunia hybrida ) flowers under different conditions of motion. We also used differently coloured P etunia flowers to test how colour and visibility interact with tactile cues to form a pollinator's preferences.
3. Bees preferred to visit conical‐celled P etunia flowers except when the conical‐celled flowers were harder to detect visually. The bees then favoured flowers that were easier to detect. But when flowers were moving and more difficult to handle, bees always learned to favour conical‐celled flowers, irrespective of visual difficulty.
4. By providing easier handling through better grip from conical cells, the plant can benefit from the natural visual attractant of flowers moving in the wind without losing pollinator preference for easier‐to‐handle flowers. Bee preference for conical‐celled flowers when flowers are moving shows how plants can use conical petal cells to take advantage of an attractant that would otherwise decrease pollinator preference by making handling difficult (movement). The selective pressure from pollinators choosing conical‐celled flowers when flowers are moving in the wind provides an explanation for the persistence of conical cells in so many diverse angiosperm species across evolutionary time.
Pollinating insects provide vital ecosystem services of enormous importance for economies and biodiversity. Yet, there is a concerning global trend of pollinator declines. Parasites and pesticides are among the suspected principle drivers of these declines. However, especially in the case of key wild pollinators, there are insufficient data on the relative impact of these individual environmental stressors and whether they interact to increase detrimental effects.
Using a fully crossed factorial design, we investigated how laboratory exposure to neonicotinoid insecticides, thiamethoxam and clothianidin, over a 9‐week period and a prevalent trypanosome gut parasite C rithidia bombi affects various crucial colony traits of the bumblebee B ombus terrestris .
We show that chronic dietary exposure from an early stage of colony development to doses of thiamethoxam and clothianidin that could be encountered in the field truncated worker production, reduced worker longevity and decreased overall colony reproductive success. Further, we demonstrate a significant interaction between neonicotinoid exposure and parasite infection on mother queen survival. The fate of the mother queen is intrinsically linked to colony success, and under combined pressure of parasite infection and neonicotinoid exposure, mother queen survival was lowest. This indicates increased detrimental effects of combined exposure on this crucial colony trait. Combined effects may be exacerbated in stressful natural environments where more pronounced parasite virulence is expected.
Synthesis and applications . Our findings reiterate that dietary exposure to neonicotinoids can impact on bumblebee colony performance and fitness. The indication of combined negative effects of ecologically relevant pressures suggests additional adverse consequences for long‐term population dynamics under complex field conditions. To help safeguard pollinator health, whole life‐cycle fitness assessments, particularly for non‐ A pis bees, stringently incorporating chronic and sublethal side effects of pesticides, as well as interactions with common natural stressors, such as prevalent parasites, should be considered in the corresponding test guidelines.
Why are animal displays so complex? In contexts ranging from courtship
and mating to parent-offspring communication to predator deterrence,
biological signals often involve a number of different visual, auditory
and/or olfactory components. Previous models of communication have
tended to ignore this complexity, assuming that only one kind of display
is available. Here, a new game-theoretical model of signalling is
described, in which signallers may use more than one display to
advertise their qualities. Additional displays may serve to enhance the
accuracy with which receivers assess a single quality (the `backup
signal' hypothesis), or to provide information about different qualities
(the `multiple message' hypothesis). Multiple signals are shown to be
stable, even when multiple receiver preferences entail significant
costs, provided that signalling costs are strongly accelerating. In such
cases, signallers bias their investment towards more efficient forms of
signal, but not to the exclusion of other display types. When costs are
not strongly accelerating, by contrast, individual signallers employ
only a single display at equilibrium. If different signals provide
information about different qualities, however, then the equilibrium may
feature alternative signalling strategies, with signallers who excel in
one quality employing one kind of display, and those who excel in
another quality employing another kind.
Carbon dioxide is a small, relatively inert, but highly volatile gas that not only gives beer its bubbles, but that also acts as one of the primary driving forces of anthropogenic climate change. While beer brewers experiment with the effects of CO on flavor and climate scientists are concerned with global changes to ambient CO levels that take place over the course of decades, many animal species are keenly aware of changes in CO concentration that occur much more rapidly and on a much more local scale. Although imperceptible to us, these small changes in CO concentration can indicate imminent danger, signal overcrowding, and point the way to food. Here I review several of these CO-evoked behaviors and compare the systems insects, nematodes, and vertebrates use to detect environmental CO.
Floral signals are typically emitted across multiple sensory modalities, although why they are multimodal is unclear. One possible explanation is that multimodal signalling ensures that at least one signal component will be transmitted effectively under varying environmental conditions (the 'efficacy backup' hypothesis). For example, by transmitting both component A and B, a signaller can communicate under environmental conditions where transmission of component A is reduced; component B 'backs up' A. To test this hypothesis, we determined whether a floral scent could back up a floral colour signal when light levels were low. We trained nectar-foraging bumblebees to discriminate rewarding and unrewarding targets that differed in colour, scent, or both colour and scent, and then presented the targets at different levels of illumination. We measured bees' accuracy at distinguishing the two targets and their rate of visits to the trained target. Performance on both measures declined under low light when targets were unscented. The presence of scent reduced the loss of accuracy under low light, supporting the efficacy backup hypothesis, but this effect depended upon the colour of the previously rewarded target. In contrast, the presence of scent did not affect the overall rate of correct visits under low light (correct visits/foraging time). A backup mechanism that maintains accuracy, but not rate of nectar collection, does not necessarily benefit the pollinator. However, it most likely benefits the plant through reduced pollen wastage. In short, multimodal floral signals may benefit the plant by improving pollen transfer, while not benefiting the pollinator.
We examined two aspects of the social control of nest climate in bumblebee colonies: which parameters of nest climate bumblebees actively down-regulate by fanning and the dynamics of the colony response as colony size increased. Colonies of Bombus terrestris were exposed to an increase in carbon dioxide, temperature or relative humidity. We performed 70 temperature trials (six colonies), 58 CO2 trials (four colonies) and four humidity trials (two colonies). An increase in CO2 concentration and temperature elicited a fanning response whereas an increase in relative humidity did not. This is the first report of fanning in bumblebee colonies to control respiratory gases. The number of fanning bees increased with stimulus intensity. The colony response to a CO2 concentration of 3.2% was comparable to the colony response to a temperature of 30°C. A marked fanning response occurred at 1.6% CO2, a concentration never exceeded in a large field nest during a pilot measurement of 10 days. We investigated the colony response over a wide range of colony sizes (between 10 and 119 workers). The proportion of the total workforce invested by colonies in nest ventilation did not change significantly; thus, the number of fanning workers increased with colony size. Furthermore, as colony size increased, the dynamics of the colony response changed: colonies responded faster to perturbations of their environment when they were large (60 or more individuals) than when they were small. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.