Publications by year
Collett TS, Hempel de Ibarra N
(2023). An 'instinct for learning': the learning flights and walks of bees, wasps and ants from the 1850s to now. The Journal of experimental biology
An 'instinct for learning': the learning flights and walks of bees, wasps and ants from the 1850s to now
The learning flights and walks of bees, wasps and ants are precisely coordinated movements that enable insects to memorise the visual surroundings of their nest or other significant places such as foraging sites. These movements occur on the first few occasions that an insect leaves its nest. They are of special interest because their discovery in the middle of the 19th century provided perhaps the first evidence that insects can learn and are not solely governed by instinct. Here, we recount the history of research on learning flights from their discovery to the present day. The first studies were conducted by skilled naturalists and then, over the following 50â€ Abstract
years, by neuroethologists examining the insects' learning behaviour in the context of experiments on insect navigation and its underlying neural mechanisms. The most important property of these movements is that insects repeatedly fixate their nest and look in other favoured directions, either in a preferred compass direction, such as North, or towards preferred objects close to the nest. Nest facing is accomplished through path integration. Memories of views along a favoured direction can later guide an insect's return to its nest. In some ant species, the favoured direction is adjusted to future foraging needs. These memories can then guide both the outward and homeward legs of a foraging trip. Current studies of central areas of the insect brain indicate what regions implement the behavioural manoeuvres underlying learning flights and the resulting visual memories.
Collett TS, Robert T, Frasnelli E, Philippides A, Hempel de Ibarra N
(2023). How bumblebees coordinate path integration and body orientation at the start of their first learning flight. Journal of Experimental Biology
How bumblebees coordinate path integration and body orientation at the start of their first learning flight
. The start of a bumblebee's first learning flight from its nest provides an opportunity to examine the bee's learning behaviour during its initial view of the nest's unfamiliar surroundings. Like many other hymenopterans, bumblebees store views of their nest surroundings while facing their nest. We found that a bumblebee's first fixation of the nest is a coordinated manoeuvre in which the insect faces the nest with its body oriented towards a particular visual feature within its surroundings. This conjunction of nest fixation and body orientation is preceded and reached by means of a translational scan during which the bee flies perpendicularly to its preferred body orientation. The utility of the coordinated manoeuvre is apparent during the bees' first return flight after foraging. Bees then adopt a similar preferred body orientation when close to the nest. How does a bee, unacquainted with its surroundings, know when it is facing its nest? a likely answer is through path integration, which gives bees continuously updated information about the current direction of their nest. Path integration also gives bees the possibility to fixate the nest when their body points in a desired direction. The three components of this coordinated manoeuvre are discussed in relation to current understanding of the central complex in the insect brain, noting that nest fixation is egocentric, whereas the preferred body orientation and flight direction that the bee adopts within the visual surroundings of the nest are geocentric.
Chapman KE, Cozma NE, Hodgkinson ABJ, English R, Gaston KJ, Hempel de Ibarra N (2022). Bumble bees exploit known sources but return with partial pollen loads when foraging under low evening light. Animal Behaviour, 194, 127-137.
Nicholls E, Rands SA, Botias C, Hempel De Ibarra N
(2022). Flower sharing and pollinator health: a behavioural perspective. Philosophical Transactions of the Royal Society B: Biological Sciences
Flower sharing and pollinator health: a behavioural perspective
Disease is an integral part of any organisms’ life, and bees have evolved immune responses and a suite of hygienic behaviours to keep them at bay in the nest. It is now evident that flowers are another transmission hub for pathogens and parasites, raising questions about adaptations that help pollinating insects stay healthy while visiting hundreds of plants over their lifetime. Drawing on recent advances in our understanding of how bees of varying size, dietary specialisation and sociality differ in their foraging ranges, navigational strategies and floral resource preferences, we explore the behavioural mechanisms and strategies that may enable foraging bees to reduce disease exposure and transmission risks at flowers by partitioning overlapping resources in space and in time. By taking a novel behavioural perspective, we highlight the missing links between disease biology and the ecology of plant-pollinator relationships, critical for improving the understanding of disease transmission risks and the better design and management of habitat for pollinator conservation. Abstract
Yilmaz A, Hempel de Ibarra N, Kelber A
(2022). High diversity of arthropod colour vision: from genes to ecology. Philosophical Transactions of the Royal Society B: Biological Sciences
High diversity of arthropod colour vision: from genes to ecology
Colour vision allows animals to use the information contained in the spectrum of light to control important behavioural decisions such as selection of habitats, food or mates. Among arthropods, the largest animal phylum, we find completely colour-blind species as well as species with up to 40 different opsin genes or more than 10 spectral types of photoreceptors, we find a large diversity of optical methods shaping spectral sensitivity, we find eyes with different colour vision systems looking into the dorsal and ventral hemisphere, and species in which males and females see the world in different colours. The behavioural use of colour vision shows an equally astonishing diversity. Only the neural mechanisms underlying this sensory ability seems surprisingly conserved—not only within the phylum, but even between arthropods and the other well-studied phylum, chordates. The papers in this special issue allow a glimpse into the colourful world of arthropod colour vision, and besides giving an overview this introduction highlights how much more research is needed to fill in the many missing pieces of this large puzzle. Abstract
. This article is part of the theme issue ‘Understanding colour vision: molecular, physiological, neuronal and behavioural studies in arthropods’.
Hempel de Ibarra N (2022). Insect navigation: Some memories like it hot. Current Biology, 32(2), R81-R84.
Gonzales D, Hempel de Ibarra N, Anderson K
(2022). Remote Sensing of Floral Resources for Pollinators – New Horizons from Satellites to Drones. Frontiers in Ecology and Evolution
Remote Sensing of Floral Resources for Pollinators â€“ New Horizons from Satellites to Drones
Insect pollinators are affected by the spatio-temporal distribution of floral resources, which are dynamic across time and space, and also influenced heavily by anthropogenic activities. There is a need for spatial data describing the time-varying spatial distribution of flowers, which can be used within behavioral and ecological studies. However, this information is challenging to obtain. Traditional field techniques for mapping flowers are often laborious and limited to relatively small areas, making it difficult to assess how floral resources are perceived by pollinators to guide their behaviors. Conversely, remote sensing of plant traits is a relatively mature technique now, and such technologies have delivered valuable data for identifying and measuring non-floral dynamics in plant systems, particularly leaves, stems and woody biomass in a wide range of ecosystems from local to global scales. However, monitoring the spatial and temporal dynamics of plant floral resources has been notably scarce in remote sensing studies. Recently, lightweight drone technology has been adopted by the ecological community, offering a capability for flexible deployment in the field, and delivery of centimetric resolution data, providing a clear opportunity for capturing fine-grained information on floral resources at key times of the flowering season. In this review, we answer three key questions of relevance to pollination science – can remote sensing deliver information on (a) how isolated are floral resources? (b) What resources are available within a flower patch? and (c) how do floral patches change over time? We explain how such information has potential to deepen ecological understanding of the distribution of floral resources that feed pollinators and the parameters that determine their navigational and foraging choices based on the sensory information they extract at different spatial scales. We provide examples of how such data can be used to generate new insights into pollinator behaviors in distinct landscape types and their resilience to environmental change. Abstract
Hempel de Ibarra N, Holtze S, BÃ¤ucker C, Sprau P, Vorobyev M
(2022). The role of colour patterns for the recognition of flowers by bees. Philosophical Transactions of the Royal Society B: Biological Sciences
The role of colour patterns for the recognition of flowers by bees
Bees discriminate between many different colours of flower petals, but it is not well understood how they perceive and learn patterns frequently found in flowers with colourful structures. We used multispectral imaging to explore chromatic cues in concentric flower patterns as they are seen through the low-resolution eyes of a honeybee. We find a diversity of colour combinations, which suggests that plants could exploit the sensory capabilities of pollinators, like bees, that learn colours easily. A consistent feature is that the surround of the pattern has a stronger chromatic contrast to the foliage background than the centre. This could potentially serve as a feature filter for the fast identification of colours in a scene as flower objects during a forager’s approach. We also trained and tested bees with three types of concentric patterns. Bees recognised and discriminated them accurately in most tests relying flexibly on both chromatic and spatial cues. Only in few situations, depending on the training stimulus, chromatic cues dominated and pattern cues were ignored. The variability of floral designs and the bees’ flexibility in recalling colour and spatial information suggest a role for colour vision in pattern processing. Implications for the signalling strategies of flowers are discussed Abstract
Langridge KV, Wilke C, Riabinina O, Vorobyev M, Hempel de Ibarra N
(2021). Approach Direction Prior to Landing Explains Patterns of Colour Learning in Bees. Frontiers in physiology
Approach Direction Prior to Landing Explains Patterns of Colour Learning in Bees.
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. Abstract
Harrap MJM, Hempel De Ibarra N, Knowles HD, Whitney HM, Rands SA
(2021). Bumblebees can detect floral humidity. The Journal of Experimental Biology
, 224 (12)
Bumblebees can detect floral humidity
AbstractFloral humidity, a region of elevated humidity proximal to 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.Summary statementWe demonstrate for the first time that bumblebees show a preference to elevated floral humidity and can learn to distinguish flowers that differ in floral humidity levels. Abstract
Hempel de Ibarra N, Vorobyev M
(2021). Insect Color Vision. In (Ed)
, Oxford University Press.
Insect Color Vision
Hall K, Robert T, Gaston KJ, Hempel de Ibarra N
(2021). Onset of morning activity in bumblebee foragers under natural low light conditions. Ecology and Evolution
Onset of morning activity in bumblebee foragers under natural low light conditions
Foraging on flowers in low light at dusk and dawn comes at an additional cost for insect pollinators with diurnal vision. Nevertheless, some species are known to be frequently active at these times. To explore how early and under which light levels colonies of bumblebees, Bombus terrestris, initiate their foraging activity, we tracked foragers of different body sizes using RFID over 5 consecutive days during warm periods of the flowering season. Bees that left the colony at lower light levels and earlier in the day were larger in size. This result extends the evidence for alloethism in bumblebees and shows that foragers differ in their task specialization depending on body size. By leaving the colony earlier to find and exploit flowers in low light, larger-sized foragers are aided by their more sensitive eyes and can effectively increase their contributions to the colony's food influx. The decision to leave the colony early seems to be further facilitated by knowledge about profitable food resources in specific locations. We observed that experience accrued over many foraging flights determined whether a bee started foraging under lower light levels and earlier in the morning. Larger-sized bees were not more experienced than smaller-sized bees, confirming earlier observations of wide size ranges among active foragers. Overall, we found that most foragers left at higher light levels when they could see well and fly faster. Nevertheless, a small proportion of foragers left the colony shortly after the onset of dawn when light levels were below 10 lux. Our observations suggest that bumblebee colonies have the potential to balance the benefits of deploying large-sized or experienced foragers during dawn against the risks and costs of foraging under low light by regulating the onset of their activity at different stages of the colony's life cycle and in changing environmental conditions. Abstract
Hempel de Ibarra N, Rands S (2021). Pollination: Influencing bee behaviour with caffeine. Current Biology, 31(18), R1090-R1092.
Frasnelli E, Robert T, Chow PKY, Scales B, Gibson S, Manning N, Philippides AO, Collett TS, Hempel de Ibarra N
(2021). Small and Large Bumblebees Invest Differently when Learning about Flowers. Current Biology
Small and Large Bumblebees Invest Differently when Learning about Flowers
Honeybees1 and bumblebees2 perform learning flights when leaving a newly discovered flower. During these flights, bees spend a portion of the time turning back to face the flower when they can memorize views of the flower and its surroundings. In honeybees, learning flights become longer when the reward offered by a flower is increased.3 We show here that bumblebees behave in a similar way, and we add that bumblebees face an artificial flower more when the concentration of the sucrose solution that the flower provides is higher. The surprising finding is that a bee's size determines what a bumblebee regards as a “low” or “high” concentration and so affects its learning behavior. The larger bees in a sample of foragers only enhance their flower facing when the sucrose concentration is in the upper range of the flowers that are naturally available to bees.4 in contrast, smaller bees invest the same effort in facing flowers whether the concentration is high or low, but their effort is less than that of larger bees. The way in which different-sized bees distribute their effort when learning about flowers parallels the foraging behavior of a colony. Large bumblebees5,6 are able to carry larger loads and explore further from the nest than smaller ones.7 Small ones with a smaller flight range and carrying capacity cannot afford to be as selective and so accept a wider range of flowers. Video Abstract: [Formula presented] Frasnelli et al. find that a bee's size sets what it memorizes on learning flights after drinking from flowers. Large bees only perform effective learning flights from flowers with rich rewards. Small bees spend less effort and memorize equally flowers with high or low rewards. This effect of size mirrors the foraging ranges of these bees. Abstract
Harrap MJM, Hempel de Ibarra N, Knowles HD, Whitney HM, Rands SA (2020). Floral Humidity in Flowering Plants: a Preliminary Survey. Frontiers in Plant Science, 11
Harrap MJM, Hempel de Ibarra N, Whitney HM, Rands SA
(2020). Floral temperature patterns can function as floral guides. Arthropod-Plant Interactions
Floral temperature patterns can function as floral guides
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. Abstract
(2020). The Effects of Landscape and Experience on the Navigation and Foraging Behaviour of Bumblebees, Bombus terrestris.
The Effects of Landscape and Experience on the Navigation and Foraging Behaviour of Bumblebees, Bombus terrestris
Bumblebees live in an environment where the spatial distribution of foraging resources is always changing. In order to keep track of such changes, bumblebees employ a variety of different navigation and foraging strategies. Although a substantial amount of research has investigated the different navigation and foraging behaviours of bumblebees, much less is known of the effects that landscape features have on bumblebee behaviour. In this thesis, a series of experiments were conducted in order to investigate the role that landscape features have on the navigation and foraging behaviour of Bombus terrestris and whether individuals’ experience influences such behaviour. A hedgerow situated next to the colony was not found to significantly shape the flight paths or foraging choices of naïve bumblebees. Homing success was investigated and used as a proxy for foraging range in different environment types. Both the release distance and the type of environment were found to have Abstract
a significant effect on the homing success of Bombus terrestris workers. Previous experience of the landscape was also found to significantly affect the time it took bumblebees to return to the colony (homing duration) as well as the likelihood of staying out overnight before returning to the colony. When focusing on the first five flights of a naïve bumblebee worker, experience was not found to significantly affect flight duration. Experience, however, significantly affected the weight of pollen foraged. The observed behaviour of bumblebee gynes provisioning their maternal colony with pollen was also investigated. The influx of pollen into the colony was found to affect this behaviour, suggesting that gynes will provision the maternal colony in response to its nutritional needs. The overall results are also discussed within the context of informing landscape management practices. The results presented in this thesis point to the critical role that factors such as the physical landscape and individual experience play in influencing bumblebee behaviour.
Nicholls E, Krishna S, Wright O, Stabler D, Krefft A, Somanathan H, Hempel de Ibarra N
(2019). A matter of taste: the adverse effect of pollen compounds on the pre-ingestive gustatory experience of sugar solutions for honeybees. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology
A matter of taste: the adverse effect of pollen compounds on the pre-ingestive gustatory experience of sugar solutions for honeybees
In addition to sugars, nectar contains multiple nutrient compounds in varying concentrations, yet little is known of their effect on the reward properties of nectar and the resulting implications for insect behaviour. We examined the pre-ingestive responses of honeybees to sucrose solutions containing a mix of pollen compounds, the amino acids proline or phenylalanine, or known distasteful substances, quinine and salt. We predicted that in taste and learning assays, bees would respond positively to the presence of nutrient compounds in a sucrose solution. However, bees’ proboscis extension responses decreased when their antennae were stimulated with pollen- or amino acid-supplemented sucrose solutions. Compared to pure sucrose, bees exhibited worse acquisition when conditioned to an odour with pollen-supplemented sucrose as the unconditioned stimulus. Such learning impairment was also observed with quinine-containing sucrose solutions. Our results suggest that bees can use their antennae to detect pollen compounds in floral nectars. Depending on the type and concentrations of compounds present, this may result in nectar being perceived as distasteful by bees, making it less effective in reinforcing the learning of floral cues. Such reward devaluation might be adaptive in cases where plants benefit from regulating the frequency of bee visitation. Abstract
Hempel de Ibarra N, Somanathan H
(2019). How are pollinators guided by colourful floral structures? a commentary on: ‘The role of pollinator preference in the maintenance of pollen colour variation’. Annals of Botany
How are pollinators guided by colourful floral structures? a commentary on: â€˜The role of pollinator preference in the maintenance of pollen colour variationâ€™
The diversity of colourful patterns and structures of flowers has attracted the attention of human observers for many centuries. In the 18th century, the German naturalist Christian Konrad Sprengel noted that they might serve to secure visits from insects in order to transfer pollen between plants. Since then, most attempts to classify interactions between insects and flowers have focused on striking and obvious features, such as the form and colour of petals and floral odours. However, floral traits that are less perceptible to humans have also been shown to influence the behaviour of pollinating insects. These include small colourful structures such as pollen on stamens, as reported by Ison and colleagues (2019) in the current issue. Abstract
Chow PKY, Lea S, Hempel de Ibarra N, Robert T
(2019). Inhibitory control and memory in the search process for a modified
problem in grey squirrels, Sciurus carolinensis. Animal Cognition
Inhibitory control and memory in the search process for a modified
problem in grey squirrels, Sciurus carolinensis
Inhibiting learned behaviours when they become unproductive and searching for an alternative solution to solve a familiar but different problem are two indicators of flexibility in problem solving. A wide range of animals show these tendencies spontaneously, but what kind of search process is at play behind their problem-solving success? Here, we investigated how Eastern grey squirrels, Sciurus carolinensis, solved a modified mechanical problem that required them to abandon their preferred and learned solution and search for alternative solutions to retrieve out-of-reach food rewards. Squirrels could solve the problem by engaging in either an exhaustive search (i.e. using trial-and-error to access the reward) or a ‘backup’ solution search (i.e. recalling a previously successful but non-preferred solution). We found that all squirrels successfully solved the modified problem on their first trial and showed solving durations comparable to their last experience of using their preferred solution. Their success and high efficiency could be explained by their high level of inhibitory control as the squirrels did not persistently emit the learned and preferred, but now ineffective, pushing behaviour. Although the squirrels had minimal experience in using the alternative (non-preferred) successful solution, they used it directly or after one or two failed attempts to achieve success. Thus, the squirrels were using the ‘backup’ solution search process. Such a process is likely a form of generalisation which involves retrieving related information of an experienced problem and applying previous successful experience during problem solving. Overall, our results provide information regarding the search process underlying the flexibility observable in problem-solving success. Abstract
Balamurali GS, Nicholls E, Somanathan H, Hempel de Ibarra N
(2018). A comparative analysis of colour preferences in temperate and tropical social bees. Science of Nature
A comparative analysis of colour preferences in temperate and tropical social bees
The spontaneous occurrence of colour preferences without learning has been demonstrated in several insect species; however, the underlying mechanisms are still not understood. Here, we use a comparative approach to investigate spontaneous and learned colour preferences in foraging bees of two tropical and one temperate species. We hypothesised that tropical bees utilise different sets of plants and therefore might differ in their spontaneous colour preferences. We tested colour-naive bees and foragers from colonies that had been enclosed in large flight cages for a long time. Bees were shortly trained with triplets of neutral, UV-grey stimuli placed randomly at eight locations on a black training disk to induce foraging motivation. During unrewarded tests, the bees’ responses to eight colours were video-recorded. Bees explored all colours and displayed an overall preference for colours dominated by long or short wavelengths, rather than a single colour stimulus. Naive Apis cerana and Bombus terrestris showed similar choices. Both inspected long-wavelength stimuli more than short-wavelength stimuli, whilst responses of the tropical stingless bee Tetragonula iridipennis differed, suggesting that resource partitioning could be a determinant of spontaneous colour preferences. Reward on an unsaturated yellow colour shifted the bees’ preference curves as predicted, which is in line with previous findings that brief colour experience overrides the expression of spontaneous preferences. We conclude that rather than determining foraging behaviour in inflexible ways, spontaneous colour preferences vary depending on experimental settings and reflect potential biases in mechanisms of learning and decision-making in pollinating insects. Abstract
Langridge KV, Wilke C, Riabinina O, Vorobyev M, Hempel de Ibarra N (2018). Approach direction prior to landing explains patterns of colour learning in bees. bioRxiv
Harrap MJM, De Ibarra NH, Whitney HM, Rands SA
(2018). Reporting of thermography parameters in biology: a systematic review of thermal imaging literature. Royal Society Open Science
Reporting of thermography parameters in biology: a systematic review of thermal imaging literature
Infrared (IR) thermography, where temperature measurements are made with IR cameras, has proven to be a very useful and widely used tool in biological science. Several thermography parameters are critical to the proper operation of thermal cameras and the accuracy of measurements, and these must usually be provided to the camera. Failure to account for these parameters may lead to less accurate measurements. Furthermore, the failure to provide information of parameter choices in reports may compromise appraisal of accuracy and replicate studies. In this review, we investigate how well biologists report thermography parameters. This is done through a systematic review of biological thermography literature that included articles published between years 2007 and 2017. We found that in primary biological thermography papers, which make some kind of quantitative temperature measurement, 48% fail to report values used for emissivity (an object's capacity to emit thermal radiation relative to a black body radiator), which is the minimum level of reporting that should take place. This finding highlights the need for life scientists to take into account and report key parameter information when carrying out thermography, in the future. Abstract
Frasnelli E, Hempel de Ibarra N, Stewart FJ (2018). The dominant role of visual motion cues in bumblebee flight control revealed through virtual reality. Frontiers in Physiology, 9, 1038 (1-11).
Potts R, Clarke RM, Oldfield SE, Wood LK, Hempel De Ibarra N, Cresswell JE (2018). The effect of dietary neonicotinoid pesticides on non-flight thermogenesis in
worker bumble bees (Bombus terrestris). Journal of Insect Physiology, 104, 33-39.
Potts R, Clarke RM, Oldfield SE, Wood LK, Hempel de Ibarra N, Cresswell JE
(2018). The effect of dietary neonicotinoid pesticides on non-flight thermogenesis in worker bumble bees (Bombus terrestris). Journal of Insect Physiology
The effect of dietary neonicotinoid pesticides on non-flight thermogenesis in worker bumble bees (Bombus terrestris)
For bumble bees (genus Bombus), the capacity for non-flight thermogenesis is essential for two fundamental processes undertaken by adult workers, namely recovery from torpor after chilling and brood incubation. Farmland bees can be widely exposed to dietary residues of neurotoxic neonicotinoid insecticides that appear in the nectar and pollen of treated bee-attractive crops, which may harm them. An earlier study shows that dietary neonicotinoids cause complex alterations to thermoregulation in honey bees, but their effect on the thermogenic capabilities of individual bumble bees has been untested previously. We therefore conducted laboratory trials involving separate dietary exposures of bumble bees to two neonicotinoids, imidacloprid and thiamethoxam, and we measured their effects on the thoracic temperatures of bees during recovery from chilling. Specifically, we used thermal imaging to measure the rates of rewarming by individual bees after chill-induced torpor and to quantify their equilibrated thoracic temperatures post-recovery. We found that both toxicants caused dose-dependent decreases in the rates of rewarming and in the equilibrated thoracic temperatures. As previously found in honey bees, the dose–response relationship for imidacloprid exhibited a biphasic hormesis with low-dose stimulation and high-dose inhibition, for which we propose a mechanism. Our present study is among the first to detect ecologically relevant effects on bees in neonicotinoid exposures involving dietary concentrations below 5 ppb. If the effects on thoracic temperatures that we observed over a short period were sustained, they could have ecologically significant impacts on farmland bumble bees. Abstract
Linander N, Dacke M, Baird E, Hempel de Ibarra N
(2018). The role of spatial texture in visual control of bumblebee learning flights. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology
The role of spatial texture in visual control of bumblebee learning flights
When leaving the nest for the first time, bees and wasps perform elaborate learning flights, during which the location of the nest is memorised. These flights are characterised by a succession of arcs or loops of increasing radius centred around the nest, with an incremental increase in ground speed, which requires precise control of the flight manoeuvres by the insect. Here, we investigated the role of optic flow cues in the control of learning flights by manipulating spatial texture in the ventral and panoramic visual field. We measured height, lateral displacement relative to the nest and ground speed during learning flights in bumblebees when ventral and panoramic optic flow cues were present or minimised, or features of the ground texture varied in size. Our observations show that ventral optic flow cues were required for the smooth execution of learning flights. We also found that bumblebees adjusted their flight height in response to variations of the visual texture on the ground. However, the presence or absence of panoramic optic flow did not have a substantial effect on flight performance. Our findings suggest that bumblebees mainly rely on optic flow information from the ventral visual field to control their learning flights. Abstract
Robert T, Frasnelli E, Hempel de Ibarra N, Collett TS
(2018). Variations on a theme: Bumblebee learning flights from the nest and from. flowers. Journal of Experimental Biology
, jeb172601 (1-15).
Variations on a theme: Bumblebee learning flights from the nest and from. flowers
On leaving a significant place to which they will come back, bees and wasps perform learning flights to acquire visual information to guide their returns. The flights occur in different contexts, like their nest or a flower, which are functionally and visually different. The permanent and inconspicuous nest hole of a bumblebee worker is locatable primarily through nearby visual features; whereas a more transient flower advertises itself by its colour and shape. We compared the learning flights of bumblebees leaving their nest or a flower in an experimental situation in which the nest hole, flower and their surroundings were visually similar. Consequently, differences in learning flights could be attributed to the bee's internal state when leaving the nest or flower rather than to the visual scene. Flights at the flower were a quarter as long as those at the nest and more focussed on the flower than its surroundings. Flights at the nest covered a larger area with the bees surveying a wider range of directions. For the initial third of the learning flight, bees kept within about 5 cm of the flower and nest hole and tended to face and fixate the nest, flower and nearby visual features. The pattern of these fixations varied between nest and flower and these differences were reflected in the bees' return flights to the nest and flower. Together these findings suggest that the bees' learning flights are tuned to their inherent expectations of the visual and functional properties of nests and flowers. Abstract
Nicholls E, Hempel de Ibarra N
(2017). Assessment of pollen rewards by foraging bees. Functional Ecology
Assessment of pollen rewards by foraging bees
The removal of pollen by flower-visiting insects is costly to plants, not only in terms of production, but also via lost reproductive potential. Modern angiosperms have evolved various reward strategies to limit these costs, yet many plant species still offer pollen as a sole or major reward for pollinating insects. The benefits plants gain by offering pollen as a reward for pollinating are defined by the behaviour of their pollinators, some of which feed on the pollen at the flower, while others collect pollen to provision offspring. We explore how pollen impacts on the behaviour and foraging decisions of pollen-collecting bees, drawing comparisons with what is known for nectar rewards. This question is of particular interest since foraging bees typically do not eat pollen during collection, meaning the sensory pathways involved in evaluating this resource are not immediately obvious. Previous research has focussed on whether foraging bees can determine the quality of pollen sources offered by different plant species, and attempted to infer the mechanisms underpinning such evaluations, mainly through observations of collection preferences in the field More recently experimental research has started to ask whether pollen itself can mediate the detection of, and learning about, pollen sources and associated floral cues. We review advancements in the understanding of how bees forage for pollen and respond to variation in pollen quality, and discuss future directions for studying how this ancestral floral food reward shapes the behaviour of pollinating insects. A lay summary is available for this article. Abstract
Chow PKY, Lea SEG, Hempel de Ibarra N, Robert T
(2017). How to stay perfect: the role of memory and behavioural traits in an experienced problem and a similar problem. Animal Cognition
How to stay perfect: the role of memory and behavioural traits in an experienced problem and a similar problem
When animals encounter a task they have solved previously, or the same problem appears in a different apparatus, how does memory, alongside behavioural traits such as persistence, selectivity and flexibility, enhance problem-solving efficiency? We examined this question by first presenting grey squirrels with a puzzle 22 months after their last experience of it (the recall task). Squirrels were then given the same problem presented in a physically different apparatus (the generalisation task) to test whether they would apply the previously learnt tactics to solve the same problem but in a different apparatus. The mean latency to success in the first trial of the recall task was significantly different from the first exposure but not different from the last exposure of the original task, showing retention of the task. A neophobia test in the generalisation task suggested squirrels perceived the different apparatus as a different problem, but they quickly came to apply the same effective tactics as before to solve the task. Greater selectivity (the proportion of effective behaviours) and flexibility (the rate of switching between tactics) both enhanced efficiency in the recall task, but only selectivity enhanced efficiency in the generalisation task. These results support the interaction between memory and behavioural traits in problem-solving, in particular memory of task-specific tactics that could enhance efficiency. Squirrels remembered and emitted task-effective tactics more than ineffective tactics. As a result, they consistently changed from ineffective to effective behaviours after failed attempts at problem-solving. Abstract
Robert T, Frasnelli E, Collett TS, Hempel de Ibarra N
(2017). Male bumblebees perform learning flights on leaving a flower but not when leaving their nest. The Journal of Experimental Biology
Male bumblebees perform learning flights on leaving a flower but not when leaving their nest
Female bees and wasps demonstrate, through their performance of elaborate learning flights, when they memorise features of a significant site. An important feature of these flights is that the insects look back to fixate the site that they are leaving. Females, which forage for nectar and pollen and return with it to the nest, execute learning flights on their initial departures from both their nest and newly discovered flowers. To our knowledge, these flights have so far only been studied in females. Here we describe and analyse putative learning flights observed in male bumblebees, Bombus terrestris L. Once male bumblebees are mature, they leave their nest for good and fend for themselves. We show that, unlike female foragers, males always flew directly away from their nest, without looking back, in keeping with their indifference to their natal nest. In contrast, after males had drunk from artificial flowers, their flights on first leaving the flowers resembled the learning flights of females, particularly in their fixations of the flowers. These differences in the occurrence of female and male learning flights seem to match the diverse needs of the two sexes to learn about ecologically relevant aspects of their environment. ("Recommended article", Faculty of 1000) Abstract
Harrap M, Rands S, Hempel de Ibarra N, Whitney H
(2017). The diversity of floral temperature patterns, and their use by pollinators. eLife
The diversity of floral temperature patterns, and their use by pollinators
Pollinating insects utilise various sensory cues to identify and learn rewarding flower species. One such cue is floral temperature, created by captured sunlight or plant thermogenesis. Bumblebees, honeybees and stingless bees can distinguish flowers based on differences in overall temperature between flowers. We report here that floral temperature often differs between different parts of the flower creating a temperature structure or pattern. Temperature patterns are common, with 55% of 118 plant species thermographed, showing within-flower temperature differences greater than the 2ºC difference that bees are known to be able to detect. Using differential conditioning techniques, we show that bumblebees can distinguish artificial flowers differing in temperature patterns comparable to those seen in real flowers. Thus, bumblebees are able to perceive the shape of these within-flower temperature patterns. Floral temperature patterns may therefore represent a new floral cue that could assist pollinators in the recognition and learning of rewarding flowers. Abstract
Hempel de Ibarra N (2016). How pollen affects learning in bees. 2016 International Congress of Entomology.
Collett TS, Philippides A, Hempel De Ibarra N
(2016). Insect navigation: How do wasps get home?. Current Biology
Insect navigation: How do wasps get home?
Bees and wasps are famous for many things, including elaborate flights to learn where their nest is. A new study provides precise, three-dimensional details of a wasp's head and body movements during such flights and reconstructs what the wasp sees. Abstract
Nicholls EK, Ehrendreich D, De Ibarra NH
(2015). Differences in color learning between pollen- and sucrose-rewarded bees. Communicative and Integrative Biology
Differences in color learning between pollen- and sucrose-rewarded bees
What bees learn during pollen collection, and how they might discriminate between flowers on the basis of the quality of this reward, is not well understood. Recently we showed that bees learn to associate colors with differences in pollen rewards. Extending these findings, we present here additional evidence to suggest that the strength and time-course of memory formation may differ between pollen- and sucrose-rewarded bees. Color-naïve honeybees, trained with pollen or sucrose rewards to discriminate colored stimuli, were found to differ in their responses when recalling learnt information after reversal training. Such differences could affect the decision-making and foraging dynamics of individual bees when collecting different types of floral rewards. Abstract
Hempel De Ibarra N, Langridge KV, Vorobyev M
(2015). More than colour attraction: behavioural functions of flower patterns. Current Opinion in Insect Science
More than colour attraction: behavioural functions of flower patterns
Flower patterns are thought to influence foraging decisions of insect pollinators. However, the resolution of insect compound eyes is poor. Insects perceive flower patterns only from short distances when they initiate landings or search for reward on the flower. From further away flower displays jointly form larger-sized patterns within the visual scene that will guide the insect's flight. Chromatic and achromatic cues in such patterns may help insects to find, approach and learn rewarded locations in a flower patch, bringing them close enough to individual flowers. Flight trajectories and the spatial resolution of chromatic and achromatic vision in insects determine the effectiveness of floral displays, and both need to be considered in studies of plant-pollinator communication. Abstract
Balamurali GS, Somanathan H, Hempel de Ibarra N
(2015). Motion cues improve the performance of harnessed bees in a colour learning task. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology
Motion cues improve the performance of harnessed bees in a colour learning task
The proboscis extension conditioning (PER) is a successful behavioural paradigm for studying sensory and learning mechanisms in bees. Whilst mainly used with olfactory and tactile stimuli, more recently reliable PER conditioning has been achieved with visual stimuli such as colours and looming stripes. However, the results reported in different studies vary quite strongly, and it remains controversially discussed how to best condition visual PER. It is particularly striking that visual PER leads to more limited performance as compared to visual conditioning of free-flying bees. It could be that visual PER learning is affected by the lack of movement and that the presence of visual motion cues could compensate for it. We tested whether bees would show differences in learning performances when conditioned either with a colour and motion stimulus in combination or with colour alone. Colour acquisition was improved in the presence of the motion stimulus. The result is consistent with the idea that visual learning might be tightly linked to movement in bees, given that they use vision predominantly during flight. Our results further confirm recent findings that successful visual PER conditioning in bees is achievable without obligatorily removing the antennae. Abstract
Shephard TV, Lea SEG, Hempel de Ibarra N
(2014). 'The thieving magpie'? No evidence for attraction to shiny objects. Animal Cognition
'The thieving magpie'? No evidence for attraction to shiny objects
It is widely accepted in European culture that magpies (Pica pica) are unconditionally attracted to shiny objects and routinely steal small trinkets such as jewellery, almost as a compulsion. Despite the long history of this folklore, published accounts of magpies collecting shiny objects are rare and empirical evidence for the behaviour is lacking. The latter is surprising considering that an attraction to bright objects is well documented in some bird species. The present study aims to clarify whether magpies show greater attraction to shiny objects than non-shiny objects when presented at the same time. We did not find evidence of an unconditional attraction to shiny objects in either captive or free-living birds. Instead, all objects elicited responses indicating neophobia in free-living birds. We suggest that humans notice when magpies occasionally pick up shiny objects because they believe the birds find them attractive, while it goes unnoticed when magpies interact with less eye-catching items. The folklore may therefore result from observation bias and cultural inflation of orally transmitted episodic events. © 2014 Springer-Verlag Berlin Heidelberg. Abstract
Nicholls E, Hempel de Ibarra N
(2014). Bees associate colour cues with differences in pollen rewards. J Exp Biol
Bees associate colour cues with differences in pollen rewards.
In contrast to the wealth of knowledge concerning sucrose-rewarded learning, the question of whether bees learn when they collect pollen from flowers has been little addressed. The nutritional value of pollen varies considerably between species, and it may be that bees learn the features of flowers that produce pollen best suited to the dietary requirements of their larvae. It is still unknown, however, whether a non-ingestive reward pathway for pollen learning exists, and how foraging bees sense differences between pollen types. Here we adopt a novel experimental approach testing the learning ability of bees with pollen rewards. Bumblebees were reared under controlled laboratory conditions. To establish which pollen rewards are distinguishable, individual bees were given the choice of collecting two types of pollen, diluted to varying degrees with indigestible α-cellulose. Bees preferentially collected a particular pollen type, but this was not always the most concentrated sample. Preferences were influenced by the degree of similarity between samples and also by the period of exposure, with bees more readily collecting samples of lower pollen concentration after five trials. When trained differentially, bees were able to associate an initially less-preferred contextual colour with the more concentrated sample, whilst their pollen preferences did not change. Successful learning of contextual cues seems to maintain pollen foraging preferences over repeated exposures, suggesting that fast learning of floral cues may preclude continuous sampling and evaluation of alternative reward sources, leading to constancy in pollen foraging. Abstract
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Riabinina O, Hempel de Ibarra N, Philippides A, Collett TS
(2014). Head movements and the optic flow generated during the learning flights of bumblebees. The Journal of Experimental Biology
Head movements and the optic flow generated during the learning flights of bumblebees
Insects inform themselves about the 3D structure of their surroundings through motion parallax. During flight, they often simplify this task by minimising rotational image movement. Coordinated head and body movements generate rapid shifts of gaze separated by periods of almost zero rotational movement, during which the distance of objects from the insect can be estimated through pure translational optic flow. This saccadic strategy is less appropriate for assessing the distance between objects. Bees and wasps face this problem when learning the position of their nest-hole relative to objects close to it. They acquire the necessary information during specialised flights performed on leaving the nest. Here, we show that the bumblebee's saccadic strategy differs from other reported cases. In the fixations between saccades, a bumblebee's head continues to turn slowly, generating rotational flow. At specific points in learning flights these imperfect fixations generate a form of ‘pivoting parallax’, which is centred on the nest and enhances the visibility of features near the nest. Bumblebees may thus utilize an alternative form of motion parallax to that delivered by the standard ‘saccade and fixate’ strategy in which residual rotational flow plays a role in assessing the distances of objects from a focal point of interest. Abstract
Hempel de Ibarra N, Vorobyev M, Menzel R
(2014). Mechanisms, functions and ecology of colour vision in the honeybee. Journal of Comparative Physiology A: sensory, neural, and behavioral physiology
Mechanisms, functions and ecology of colour vision in the honeybee
Research in the honeybee has laid the foundations for our understanding of insect colour vision. The trichromatic colour vision of honeybees shares fundamental properties with primate and human colour perception, such as colour constancy, colour opponency, segregation of colour and brightness coding. Laborious efforts to reconstruct the colour vision pathway in the honeybee have provided detailed descriptions of neural connectivity and the properties of photoreceptors and interneurons in the optic lobes of the bee brain. The modelling of colour perception advanced with the establishment of colour discrimination models that were based on experimental data, the Colour-Opponent Coding (COC) and Receptor-Noise Limited (RNL) models, which are important tools for the quantitative assessment of bee colour vision and colour-guided behaviours. Major insights into the visual ecology of bees have been gained combining behavioural experiments and quantitative modelling, and asking how bee vision has influenced the evolution of flower colours and patterns. Recently research has focussed on the discrimination and categorisation of coloured patterns, colourful scenes and various other groupings of coloured stimuli, with a major interest in the bees’ cognitive abilities. The identification of perceptual mechanisms remains a crucial step for correctly interpreting their performance and learning strategies in various behavioural tasks. Abstract
Davies TW, Bennie J, Inger R, Hempel de Ibarra N, Gaston KJ
(2013). Artificial light pollution: are shifting spectral signatures changing the balance of species interactions?. Glob Chang Biol
Artificial light pollution: are shifting spectral signatures changing the balance of species interactions?
Technological developments in municipal lighting are altering the spectral characteristics of artificially lit habitats. Little is yet known of the biological consequences of such changes, although a variety of animal behaviours are dependent on detecting the spectral signature of light reflected from objects. Using previously published wavelengths of peak visual pigment absorbance, we compared how four alternative street lamp technologies affect the visual abilities of 213 species of arachnid, insect, bird, reptile and mammal by producing different wavelength ranges of light to which they are visually sensitive. The proportion of the visually detectable region of the light spectrum emitted by each lamp was compared to provide an indication of how different technologies are likely to facilitate visually guided behaviours such as detecting objects in the environment. Compared to narrow spectrum lamps, broad spectrum technologies enable animals to detect objects that reflect light over more of the spectrum to which they are sensitive and, importantly, create greater disparities in this ability between major taxonomic groups. The introduction of broad spectrum street lamps could therefore alter the balance of species interactions in the artificially lit environment. Abstract
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Philippides A, Hempel de Ibarra N, Riabinina O, Collett TS
(2013). Bumblebee calligraphy: the design and control of flight motifs in the learning and return flights of Bombus terrestris. The Journal of Experimental Biology
Bumblebee calligraphy: the design and control of flight motifs in the learning and return flights of Bombus terrestris.
Many wasps and bees learn the position of their nest relative to nearby visual features during elaborate learning flights that they perform on leaving the nest. Return flights to the nest are thought to be patterned so that insects can reach their nest by matching their current view to views of their surroundings stored during learning flights. To understand how ground-nesting bumblebees might implement such a matching process, we have video-recorded the bees learning and return flights and analysed the similarities and differences between the principal motifs of their flights. Loops that take bees away from and bring them back towards the nest are common during learning flights and less so in return flights. Zigzags are more prominent on return flights. Both motifs tend to be nest based. Bees often both fly towards and face the nest in the middle of loops and at the turns of zigzags. Before and after flight direction and body orientation are aligned, the two diverge from each other so that the nest is held within the bees' fronto-lateral visual field while flight direction relative to the nest can fluctuate more widely. These and other parallels between loops and zigzags suggest that they are stable variations of an underlying pattern, which enable bees to store and reacquire similar nest-focused views during learning and return flights. Abstract
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Leboulle G, NiggebrÃ¼gge C, Roessler R, Briscoe AD, Menzel R, Hempel de Ibarra N
(2013). Characterisation of the RNA interference response against the long-wavelength receptor of the honeybee. Insect Biochem Mol Biol
Characterisation of the RNA interference response against the long-wavelength receptor of the honeybee.
Targeted knock-down is the method of choice to advance the study of sensory and brain functions in the honeybee by using molecular techniques. Here we report the results of a first attempt to interfere with the function of a visual receptor, the long-wavelength-sensitive (L-) photoreceptor. RNA interference to inhibit this receptor led to a reduction of the respective mRNA and protein. The interference effect was limited in time and space, and its induction depended on the time of the day most probably because of natural daily variations in opsin levels. The inhibition did not effectively change the physiological properties of the retina. Possible constraints and implications of this method for the study of the bee's visual system are discussed. Overall this study underpins the usefulness and feasibility of RNA interference as manipulation tool in insect brain research. Abstract
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Collett TS, Hempel de Ibarra N, Riabinina O, Philippides A
(2013). Coordinating compass-based and nest-based flight directions during bumblebee learning and return flights. J Exp Biol
(Pt 6), 1105-1113.
Coordinating compass-based and nest-based flight directions during bumblebee learning and return flights.
Bumblebees tend to face their nest over a limited range of compass directions when learning the nest's location on departure and finding it on their approach after foraging. They thus obtain similar views of the nest and its surroundings on their learning and return flights. How do bees coordinate their flights relative to nest-based and compass-based reference frames to get such similar views? We show, first, that learning and return flights contain straight segments that are directed along particular compass bearings, which are independent of the orientation of a bee's body. Bees are thus free within limits to adjust their viewing direction relative to the nest, without disturbing flight direction. Second, we examine the coordination of nest-based and compass-based control during likely information gathering segments of these flights: loops during learning flights and zigzags on return flights. We find that bees tend to start a loop or zigzag when flying within a restricted range of compass directions and to fly towards the nest and face it after a fixed change in compass direction, without continuous interactions between their nest-based and compass-based directions of flight. A preferred trajectory of compass-based flight over the course of a motif, combined with the tendency of the bees to keep their body oriented towards the nest automatically narrows the range of compass directions over which bees view the nest. Additionally, the absence of interactions between the two reference frames allows loops and zigzags to have a stereotyped form that can generate informative visual feedback. Abstract
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Nicholls EK, Hempel de Ibarra N
(2013). Pollen elicits proboscis extension but does not reinforce PER learning in honeybees. Insects
Pollen elicits proboscis extension but does not reinforce PER learning in honeybees
The function of pollen as a reward for foraging bees is little understood, though there is evidence to suggest that it can reinforce associations with visual and olfactory floral cues. Foraging bees do not feed on pollen, thus one could argue that it cannot serve as an appetitive reinforcer in the same way as sucrose. However, ingestion is not a critical parameter for sucrose reinforcement, since olfactory proboscis extension (PER) learning can be conditioned through antennal stimulation only. During pollen collection, the antennae and mouthparts come into contact with pollen, thus it is possible that pollen reinforces associative learning through similar gustatory pathways as sucrose. Here pollen was presented as the unconditioned stimulus (US), either in its natural state or in a 30% pollen-water solution, and was found to elicit proboscis extension following antennal stimulation. Control groups were exposed to either sucrose or a clean sponge as the US, or an unpaired presentation of the conditioned stimulus (CS) and pollen US. Despite steady levels of responding to the US, bees did not learn to associate a neutral odour with the delivery of a pollen reward, thus whilst pollen has a proboscis extension releasing function, it does not reinforce olfactory PER learning. Abstract
Cresswell JE, Page CJ, Uygun MB, Holmbergh M, Li Y, Wheeler JG, Laycock I, Pook CJ, de Ibarra NH, Smirnoff N, et al (2012). Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid). Zoology
Cresswell JE, Page CJ, Uygun MB, Holmbergh M, Li Y, Wheeler JG, Laycock I, Pook CJ, Hempel de Ibarra N, Smirnoff N, et al
(2012). Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid). Zoology
Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid)
Currently, there is concern about declining bee populations and the sustainability of pollination services. One potential threat to bees is the unintended impact of systemic insecticides, which are ingested by bees in the nectar and pollen from flowers of treated crops. To establish whether imidacloprid, a systemic neonicotinoid and insect neurotoxin, harms individual bees when ingested at environmentally realistic levels, we exposed adult worker bumble bees, Bombus terrestris L. (Hymenoptera: Apidae), and honey bees, Apis mellifera L. (Hymenoptera: Apidae), to dietary imidacloprid in feeder syrup at dosages between 0.08 and 125 μg l Abstract
. Honey bees showed no response to dietary imidacloprid on any variable that we measured (feeding, locomotion and longevity). In contrast, bumble bees progressively developed over time a dose-dependent reduction in feeding rate with declines of 10-30% in the environmentally relevant range of up to 10 μg l
. but neither their locomotory activity nor longevity varied with diet. To explain their differential sensitivity, we speculate that honey bees are better pre-adapted than bumble bees to feed on nectars containing synthetic alkaloids, such as imidacloprid, by virtue of their ancestral adaptation to tropical nectars in which natural alkaloids are prevalent. We emphasise that our study does not suggest that honey bee colonies are invulnerable to dietary imidacloprid under field conditions, but our findings do raise new concern about the impact of agricultural neonicotinoids on wild bumble bee populations. © 2012 Elsevier GmbH. All rights reserved.
Vorobyev M, Hempel de Ibarra N
(2012). Honey bee vision in relation to flower patterns. In Galizia G, Eisenhardt D, Giurfa, M (Eds.) Honeybee Neurobiology and Behavior
, Heidelberg: Springer, 285-301.
Honey bee vision in relation to flower patterns
Linander N, Hempel de Ibarra N, Laska M
(2012). Olfactory detectability of L-amino acids in the European honeybee (Apis mellifera). Chem Senses
Olfactory detectability of L-amino acids in the European honeybee (Apis mellifera).
The honeybee is one of several insect model systems for the study of olfaction, yet our knowledge regarding the spectrum of odorants detectable by Apis mellifera is limited. One class of odorants that has never been tested so far are the amino acids, which are important constituents of floral nectar. Using the proboscis extension response paradigm, we assessed whether the odor of amino acids is detectable for honeybees and determined olfactory detection thresholds for those amino acids that were detectable. We found that honeybees are able to detect the odor of 5 of the 20 proteinogenic amino acids when presented at a concentration of 50 or 100 mM. Median olfactory detection thresholds for these 5 amino acids were 12.5 mM with L-tyrosine and L-cysteine, 50 mM with L-tryptophan and L-asparagine, and 100 mM with L-proline. All detection thresholds were much higher than reported concentrations of amino acids in floral nectars. We conclude that in the foraging and feeding context, honeybees are likely to detect amino acids through taste rather than olfaction. Across-species comparisons of the detectability of and sensitivity to amino acids suggest that the number of functional genes coding for olfactory receptors may affect both a species' sensitivity for odorants and the breadth of its spectrum of detectable odorants. Abstract
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Riabinina O, Hempel de Ibarra N, Howard L, Collett TS
(2011). Do wood ants learn sequences of visual stimuli?. J Exp Biol
Do wood ants learn sequences of visual stimuli?
The visually guided foraging routes of some formicine ants are individually stereotyped, suggesting the importance of visual learning in maintaining these routes. We ask here whether the wood ant Formica rufa learns a sequence of visual features encountered at different stages along a route, as reported for honeybees. We trained ants in several simple mazes to follow two alternative routes. Along each two-stage route, the ants first encountered one of two priming stimuli. The identity of the priming stimulus determined which of two choice stimuli was rewarded in the second stage of the route. As stimuli we used ultraviolet and yellow/green light panels, and two black-and-white patterns. Did ants learn to pair each colour with the appropriate black-and-white pattern? Ants learnt readily to discriminate between the two coloured stimuli or between the two black-and-white patterns. They could also pair coloured and black-and-white patterns, provided that the two were presented simultaneously. The ants' behaviour with sequential stimuli varied according to whether the priming stimulus was a coloured stimulus or a black-and-white pattern. When the priming stimulus was coloured, ants seemed to learn the two sequences, but tests showed that their success was probably caused by the after-effects of colour adaptation. With a black-and-white priming stimulus and a coloured second stage stimulus, robust sequential learning could not be demonstrated, although under certain experimental conditions a tiny proportion of ants did acquire the sequence. Thus, ants perform conditional discriminations reliably when priming and choice stimuli are simultaneous, but they usually fail when the stimuli are sequential. Abstract
Maloney LT, Hempel de Ibarra N
(2010). Blackawton bees: commentary on Blackawton, P. S. et al. Biol Lett
Blackawton bees: commentary on Blackawton, P. S. et al.
The creature in figure 1 is a buff-tailed bumble-bee (Bombus terrestris), a member of one of the most abundant bumble-bee species in Europe. It lives underground with its nest mates, often in the abandoned nest of a mouse and, while it spends much of its life foraging within 100–500 m of its nest  with occasional excursions further out, buff-tailed bumble-bees transported as far from their nest as 13 km can find their way home.This bumble-bee is a social creature, sharing information about food sources with its nest mates by motor displays and chemical signals (pheromones). Its foraging behaviour is an endless series of visits to flowers, typically flowers of a single species as noted long ago: ‘On each expedition the bee does not fly from a flower of one kind to a flower of another, but flies from one violet, say, to another violet, and never meddles with another flower until it has got back to the hive … ’ [2, p. 277]. In an elegant book about the economics of the bumble-bee, Bernd Heinrich  characterizes flower and bumble-bee as an essentially perfect example of an economic system. Bees and flowers need each other but their ‘interests’ do not always coincide. The bee disperses pollen from the flower, enhancing its rate of reproduction, and the flower provides the bee with its primary source of energy in the form of nectar. Abstract
The flower would benefit if it could produce less nectar and more pollen ceteris paribus. But ceteris paribus here implies that the bee would continue to disperse pollen as enthusiastically after what is in effect a cut in wages. Heinrich's characterization of a bee and a flower as a perfect economic system simply recognizes a brutal fact. The bee has no recourse against a cheating flower other than to vote with its wings and never visit such a flower again. There are no bee–flower contracts and no legal system to enforce them, no police, no politicians and no lawyers. The bumble-bee lives in a libertarian paradise.
NiggebrÃ¼gge C, Leboulle G, Menzel R, Komischke B, Hempel de Ibarra N
(2009). Fast learning but coarse discrimination of colours in restrained honeybees. Journal of Experimental Biology
Fast learning but coarse discrimination of colours in restrained honeybees
Colours are quickly learnt by free-moving bees in operant conditioning settings. In the present study, we report a method using the classical conditioning of the proboscis extension response (PER) in restrained honeybees (Apis mellifera), which allows bees to learn colours after just a few training trials. We further analysed how visual learning and discrimination is influenced by the quality of a stimulus by systematically varying the chromatic and achromatic properties of the stimuli. Using differential conditioning, we found that faster colour discrimination learning was correlated with reduced colour similarity between stimuli. In experiments with both absolute and differential conditioning, restrained bees showed poor colour discrimination and broad generalisation. This result is in strong contrast to the well-demonstrated ability of bees to finely discriminate colours under free-flight conditions and raises further questions about the temporal and perceptual processes underlying the ability of bees to discriminate and learn colours in different behavioural contexts. Abstract
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Hempel de Ibarra N, Vorobyev M
(2009). Flower patterns are adapted for detection by bees. J Comp Physiol a Neuroethol Sens Neural Behav Physiol
Flower patterns are adapted for detection by bees.
We have demonstrated previously that honeybees use brightness vision mediated by green (or L-) receptor to detect targets from a long distance. They detect circular targets having a dim, for the L-receptor, centre and bright surround from a longer distance than targets having bright centre and dim surround. Here we show that a majority of bee-pollinated flowers have a centre that, for the L-receptor, is dim with bright surround, i.e. have patterns that are easy for a bee to detect. Flowers with dim for the L-receptor surrounds tend to be larger than those with bright surrounds, indicating that flowers compensate for the impaired visibility of their patterns by increasing the size of their displays. Abstract
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Arnon R, Keasar T, Hempel de Ibarra N, Cohen D, Shmida A
(2009). Learning of colored targets with vertical and horizontal components by bumblebees (Bombus terrestris L.). ISRAEL JOURNAL OF PLANT SCIENCES
(3), 193-201. Author URL
Hempel de Ibarra N, Philippides A, Riabinina O, Collett TS (2009). Preferred viewing directions of bumblebees (Bombus terrestris L.) when learning and approaching their nest site (vol 212, pg 3193, 2009). J EXP BIOL, 212(22), 3769-3769.
Baddeley B, Philippides A, Graham P, de Ibarra NH, Collett T, Husbands P
(2009). What can be learnt from analysing insect orientation flights using probabilistic SLAM?. Biol Cybern
What can be learnt from analysing insect orientation flights using probabilistic SLAM?
In this paper, we provide an analysis of orientation flights in bumblebees, employing a novel technique based on simultaneous localisation and mapping (SLAM) a probabilistic approach from autonomous robotics. We use SLAM to determine what bumblebees might learn about the locations of objects in the world through the arcing behaviours that are typical of these flights. Our results indicate that while the bees are clearly influenced by the presence of a conspicuous landmark, there is little evidence that they structure their flights to specifically learn about the position of the landmark. Abstract
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Krofczik S, Khojasteh, U. Hempel de Ibarra N, Menzel R
(2008). Adaptation of microglomerular complexes in the honeybee mushroom body lip to manipulations of behavioral maturation and sensory experience. Developmental Neurobiology
Adaptation of microglomerular complexes in the honeybee mushroom body lip to manipulations of behavioral maturation and sensory experience
Worker honeybees proceed through a sequence of tasks, passing from hive and guard duties to. foraging activities. The underlying neuronal changes accompanying and possibly mediating these behavioral transitions are not well understood. We studied changes in the microglomerular organization of the mushroom bodies, a brain region involved in sensory. integration, learning, and memory, during adult maturation. We visualized the MB lips’ microglomerular organization by applying double labeling of presynaptic projection neuron boutons and postsynaptic Kenyon cell spines, which form microglomerular complexes. Their number and density, as well as the bouton volume, were measured using 3D-based techniques. Our results show that the number of microglomerular complexes and the bouton volumes increased during maturation, independent Abstract
of environmental conditions. In contrast, manipulations of behavior and sensory experience caused a decrease in the number of microglomerular complexes, but an increase in bouton volume. This may indicate an outgrowth of synaptic connections within the MB lips during honeybee maturation. Moreover, manipulations of behavioral and sensory experience led to adaptive changes, which indicate that the microglomerular organization
of the MB lips is not static and determined by
maturation, but rather that their organization is plastic, enabling the brain to retain its synaptic efficacy.
Hempel de Ibarra N (2008). Colour vision in honeybees: behaviour, neural mechanisms and ecology. In (Ed) Insect Mimetics, Tokyo, Japan: NTS Inc. 294-304.
Wertlen AM, NiggebrÃ¼gge, C. Vorobyev, M. Hempel de Ibarra N
(2008). Detection of patches of coloured disks by bees. Journal of Experimental Biology
Detection of patches of coloured disks by bees
To find out how grouping of flowers into patches improves their detectability by hymenopteran pollinators, we trained honeybees Abstract
and bumblebees to detect groups of three spatially separated disks and compared results with the detection limit for single disks.
When the discs presented contrast to the long-wavelength-sensitive (L) receptor, grouping of disks improved the detectability.
The disks were optically resolvable for the honeybee eye. The improvement of detectability was stronger for bumblebees than for
honeybees. When disks did not present contrast to the L-receptor, the grouping did not improve the detectability, i.e. the detection
limit was set by the size of a single disk. We conclude that in bees the neural mechanisms that improve detectability ofgrouped
elements require input from the L-receptor. Our results indicate that grouping of flowers into sparse patches can improve their
detectability by bees, even when individual flowers can be optically resolved by the eyes of bees, as long as flowers can be
detected by the long-wavelength-sensitive receptor.
Benitez-Veiyra S, Hempel de Ibarra N, Wertlen AM, Cocucci AA
(2007). How to look like a mallow: evidence of floral mimicry between Turneraceae and Malvaceae. Proceedings of the Royal Society B Biological Sciences
How to look like a mallow: evidence of floral mimicry between Turneraceae and Malvaceae
Abundant, many-flowered plants represent reliable and rich food sources for animal pollinators, and may even sustain guilds of specialized pollinators. Contrastingly, rare plants need alternative strategies Abstract
to ensure pollinators’ visitation and faithfulness. Flower mimicry, i.e. the sharing of a similar flower
colour and display pattern by different plant species, is a means by which a rare species can exploit a
successful model and increase its pollination services. The relationship between two or more
rewarding flower mimic species, or Mu¨ llerian mimicry, has been proposed as mutualistic, in contrast
to the unilaterally beneficial Batesian floral mimicry. In this work, we show that two different
geographical colour phenotypes of Turnera sidoides ssp. pinnatifida resemble co-flowering Malvaceae in
colour as seen by bees’ eyes, and that these pollinators do not distinguish between them when
approaching flowers in choice tests. Main pollinators of T. sidoides are bees specialized for collecting
pollen in Malvaceae. We demonstrate that the similarity between at least one of the geographical
colour phenotypes of T. sidoides and co-flowering Malvaceae is adaptive, since the former obtains
more pollination services when growing together with its model than when growing alone. Instead of
the convergent evolution pattern attributed to Mu¨ llerian mimicry, our data rather suggest an
advergent evolution pattern, because only T. sidoides seems to have evolved to be more similar to its malvaceous models.
Brembs B, Hempel de Ibarra N (2006). Different parameters support generalization and discrimination learning in Drosophila at the flight simulator. Learning & Memory, 13(5), 629-637.
Collett TS, Graham P, Harris RA, Hempel de Ibarra N (2006). Navigational memories in ants and bees: Memory retrieval when selecting and following routes. Advances in the Study of Behavior, 36, 123-172.
Harris RA, Hempel de Ibarra N, Graham P, Collett TS (2005). Ant navigation: Priming of visual route memories. Nature, 438(7066).
Rodriguez I, Gumbert A, Hempel de Ibarra N, Kunze J, Giurfa M (2004). Symmetry is on the eye of the ‘beeholder’: Innate preference for bilateral symmetry in flower-naïve bumblebees. Naturwissenschaften, 91, 374-377.
NiggebrÃ¼gge C, Hempel de Ibarra N (2003). Colour-dependent target. detection by bees. Journal of Comparative Physiology A: sensory, neural, and behavioral physiology, A, 189, 915-918.
Hempel de Ibarra N, Giurfa M (2003). Discrimination of closed coloured shapes by honeybees requires only contrast to the long wavelength receptor type. Animal Behaviour, 66(5), 903-910.
Hempel de Ibarra N, Giurfa M, Vorobyev M
(2002). Discrimination of coloured patterns by honeybees through chromatic and achromatic cues. Journal of Comparative Physiology A: sensory, neural, and behavioral physiology
Discrimination of coloured patterns by honeybees through chromatic and achromatic cues.
We investigated pattern discrimination by worker honeybees, Apis mellifera, focusing on the roles of spectral cues and the angular size of patterns. Free-flying bees were trained to discriminate concentric patterns in a Y-maze. The rewarded pattern could be composed of either a cyan and a yellow colour, which presented both different chromatic and achromatic L-receptor contrast, or an orange and a blue colour, which presented different chromatic cues, but the same L-receptor contrast. The non-rewarded alternative was either a single-coloured disc with the colour of the central disc or the surrounding ring of the pattern, a checkerboard pattern with non-resolvable squares, the reversed pattern, or the elements of the training pattern (disc or ring alone). Bees resolved and learned both colour elements in the rewarded patterns and their spatial properties. When the patterns subtended large visual angles, this discrimination used chromatic cues only. Patterns with yellow or orange central discs were generalised toward the yellow and orange colours, respectively. When the patterns subtended a visual angle close to the detection limit and L-receptor contrast was mediating discrimination, pattern perception was reduced: bees perceived only the pattern element with higher contrast. Abstract
. Author URL
Vorobyev M, Marshall J, Osorio D, Hempel de Ibarra N, Menzel R
(2001). Colourful objects through animal eyes. Color Research and Application
Colourful objects through animal eyes
To understand how bees, birds, and fish may use colour vision for food selection and mate choice, we reconstructed views of biologically important objects taking into account the receptor spectral sensitivities. Reflectance spectra a of flowers, bird plumage, and fish skin were used to calculate receptor quantum catches. The quantum catches were then coded by "red," "green," and "blue" of a computer monitor; and powers, birds, and fish were visualized in "animal colours. " Calculations were performed for different illumination conditions. To simulate colour constancy, we used a von Kries algorithm, i.e. the receptor quantum catches were scaled so that the colour of illumination remained invariant. We show that on land this algorithm compensates reasonably well for changes of object appearance caused by natural changes of illumination, while in water failures of von Kries colour constancy are prominent. (C) 2000 John Wiley & Sons, Inc. Abstract
Hempel de Ibarra N, Giurfa M, Vorobyev M (2001). Detection of coloured pattern by honeybees through chromatic and achromatic cues. Journal of Comparative Physiology A, 187, 215-224.
Hempel de Ibarra N, Vorobyev M, Brandt R, Giurfa M (2000). Detection of dim and bright colours by honeybees. Journal of Experimental Biology, 203, 3289-3298.
Vorobyev M, Hempel de Ibarra N, Brandt R, Giurfa M (1999). Do “white” and “green” look the same to a bee?. Naturwissenschaften, 86, 592-594.