Abstract: We review the rich literature on behavioural responses of aphids (Hemiptera: Aphididae) to stimuli of different colours. Only in one species there are adequate physiological data on spectral sensitivity to explain behaviour crisply in mechanistic terms. Because of the great interest in aphid responses to coloured targets from an evolutionary, ecological and applied perspective, there is a substantial need to expand these studies to more species of aphids, and to quantify spectral properties of stimuli rigorously. We show that aphid responses to colours, at least for some species, are likely based on a specific colour opponency mechanism, with positive input from the green domain of the spectrum and negative input from the blue and/or UV region. We further demonstrate that the usual yellow preference of aphids encountered in field experiments is not a true colour preference but involves additional brightness effects. We discuss the implications for agriculture and sensory ecology, with special respect to the recent debate on autumn leaf colouration. We illustrate that recent evolutionary theories concerning aphid–tree interactions imply far-reaching assumptions on aphid responses to colours that are not likely to hold. Finally we also discuss the implications for developing and optimising strategies of aphid control and monitoring.
Abstract: Innate sensory biases could play an important role in helping naïve animals to find food. As inexperienced bees are known to have strong innate colour biases we investigated whether bumblebee (Bombus terrestris) colonies with stronger biases for the most rewarding flower colour (violet) foraged more successfully in their local flora. To test the adaptive significance of variation in innate colour bias, we compared the performance of colour-naïve bees, from nine bumblebee colonies raised from local wild-caught queens, in a laboratory colour bias paradigm using violet (bee UV-blue) and blue (bee blue) artificial flowers. The foraging performance of the same colonies was assessed under field conditions. Colonies with a stronger innate bias for violet over blue flowers in the laboratory harvested more nectar per unit time under field conditions. In fact, the colony with the strongest bias for violet (over blue) brought in 41% more nectar than the colony with the least strong bias. As violet flowers in the local area produce more nectar than blue flowers (the next most rewarding flower colour), these data are consistent with the hypothesis that local variation in flower traits could drive selection for innate colour biases.
Abstract: Psychophysicists studying decision making in animals have overwhelmingly focused on choice accuracy, not speed. Results from human visual search, however, show that there might be a tight link between the two. Here we review both visual-sensory and cognitive mechanisms that affect decision speed in flower visiting bees. We show that decision times are affected by contrast of targets and background, by similarity between targets and distractors, numbers of distractors present in a scene, illuminating light intensity, presence or absence of punishment, and complexity of tasks. We explore between-individual and within-individual speed-accuracy tradeoffs, and show that bees resort to highly dynamic strategies when solving visual search tasks. Where possible, we attempt to link the observed search behaviour to the temporal and spatial properties of neuronal circuits underlying visual object detection. We demonstrate that natural foraging speed may not only be limited by factors such as food item density, flight energetics and scramble competition, as often implied. Our results show that understanding the behavioural ecology of foraging can substantially gain from knowledge about mechanisms of visual information processing.
Abstract: We wished to understand the effects on pollinator behaviour of single mutations in plant genes controlling flower appearance. To this end, we analysed snapdragon flowers (Antirrhinum majus), including the mixta and nivea mutants, in controlled laboratory conditions using psychophysical tests with bumblebees. The MIXTA locus controls petal epidermal cell shape, and thus the path that incident light takes within the pigment-containing cells. The effect is that mixta mutant flowers are pink in comparison to the wild type purple flowers, and mutants lack the sparkling sheen of wild type flowers that is clearly visible to human observers. Despite their fundamentally different appearance to humans, and even though bees could discriminate the flowers, inexperienced bees exhibited no preference for either type, and the flowers did not differ in their detectability in a Y-maze—either when the flowers appeared in front of a homogeneous or a dappled background. Equally counterintuitive effects were found for the non-pigmented, UV reflecting nivea mutant: even though the overall reflectance intensity and UV signal of nivea flowers is several times that of wild type flowers, their detectability was significantly reduced relative to wild type flowers. In addition, naïve foragers preferred wild type flowers over nivea mutants, even though these generated a stronger signal in all receptor types. Our results show that single mutations affecting flower signal can have profound effects on pollinator behaviour—but not in ways predictable by crude assessments via human perception, nor simple quantification of UV signals. However, current models of bee visual perception predict the observed effects very well.
Abstract: Most species of flower-visiting Hymenoptera are trichromatic, with photoreceptor spectral sensitivity peaks in the UV, blue and green regions of the spectrum. Red flowers, therefore, should be relatively difficult to detect for such insects. Nevertheless, in population biological studies in the bumblebee, Bombus terrestris, the Sardinian island population (B. t. sassaricus) displayed significantly higher responses to red artificial flowers (in tests of innate colour choice and detectability) than several mainland populations of the same species (Chittka et al. in Cognitive ecology of pollination, pp 106-126, 2001; Popul Ecol 46:243-251, 2004). Since there is relatively little physiological data on population differences in sensory systems, we used intracellular recording to compare photoreceptor spectral sensitivity in B. t. sassaricus and the southern European and Mediterranean population, B. t. dalmatinus. The results show both populations to be UV-blue-green trichromats, but with a small but significant increase in long-wave sensitivity in island bees. Spectral peaks were estimated at 348, 435 and 533 nm (B. t. dalmatinus) and 347, 436 and 538 nm (B. t. sassaricus) for UV, blue and green receptors, respectively. There were no significant differences in UV and blue receptor sensitivities. We found no photoreceptors maximally sensitive to red spectral light in the Sardinian population and model calculations indicate that the behavioural population differences in colour responses cannot be directly explained by receptor population differences.
Abstract: To investigate how bumblebees (Bombus terrestris) learn the complex motor skills involved in pollen foraging, we observed naïve workers foraging on arrays of nectarless poppy flowers (Papaver rhoeas) in a greenhouse. Foraging skills were quantified by measuring the pollen load collected during each foraging bout and relating this to the number of flowers visited and bout duration on two consecutive days. The pollen standing crop (PSC) in each flower decreased drastically from 0530 to 0900 hours. Therefore, we related foraging performance to the changing levels of pollen available (per flower) and found that collection rate increased over the course of four consecutive foraging bouts (comprising between 277 and 354 individual flower visits), suggesting that learning to forage for pollen represents a substantial time investment for individual foragers. The pollen collection rate and size of pollen loads collected at the start of day 2 were markedly lower than at the end of day 1, suggesting that components of pollen foraging behaviour could be subject to imperfect overnight retention. Our results suggest that learning the necessary motor skills to collect pollen effectively from morphologically simple flowers takes three times as many visits as learning how to handle the most morphologically complex flowers to extract nectar, potentially explaining why bees are more specialised in their choice of pollen flowers.
Abstract: To test the relative importance of long-term and working spatial memories in short-range foraging in bumblebees, we compared the performance of two groups of bees. One group foraged in a stable array of six flowers for 40 foraging bouts, thereby enabling it to establish a long-term memory of the array, and adjust its spatial movements accordingly. The other group was faced with an array that changed between (but not within) foraging bouts, and thus had only access to a working memory of the flowers that had been visited. Bees in the stable array started out sampling a variety of routes, but their tendency to visit flowers in a repeatable, stable order ("traplining") increased drastically with experience. These bees used shorter routes and converged on four popular paths. However, these routes were mainly formed through linking pairs of flowers by near-neighbour movements, rather than attempting to minimize overall travel distance. Individuals had variations to a primary sequence, where some bees used a major sequence most often, followed by a minor less used route, and others used two different routes with equal frequency. Even though bees foraging in the spatially randomized array had access to both spatial working memory and scent marks, this manipulation greatly disrupted foraging efficiency, mainly via an increase in revisitation to previously emptied flowers and substantially longer search times. Hence, a stable reference frame greatly improves foraging even for bees in relatively small arrays of flowers.
Abstract: Flower colours have evolved over 100 million years to address the colour vision of their bee pollinators. In a much more rapid
process, cultural (and horticultural) evolution has produced images of flowers that stimulate aesthetic responses in human observers.
The colour vision and analysis of visual patterns differ in several respects between humans and bees. Here, a behavioural ecologist and an installation artist present bumblebees with reproductions of paintings highly appreciated in Western society, such as Van
Gogh’s Sunflowers. We use this unconventional approach in the hope to raise awareness for between-species differences in visual perception, and to provoke thinking about the implications of biology in human aesthetics and the relationship between object representation and its biological connotations.
Abstract: Recent research on ants shows that running in tandem might serve the function of teaching naïve ants about the path to a target. Although these new experiments represent perhaps the most highly controlled study of teaching in animals to date, the findings prompt the question of how teaching formally differs from other forms of communication.
Abstract: The flowers of angiosperm plants present us with a staggering diversity of signal designs, but how did this diversity evolve? Answering this question requires us to understand how pollinators analyze these signals with their visual and olfactory sense organs, and how the sensory systems work together with post-receptor neural wiring to produce a coherent percept of the world around them. Recent research on the dynamics with which bees store, manage and retrieve memories all have fundamental implications for how pollinators choose between flowers, and in turn for floral evolution. New findings regarding how attention, peak-shift phenomena, and speed-accuracy tradeoffs affect pollinator choice between flower species show that analyzing the evolutionary ecology of signal-receiver relationships can substantially benefit from knowledge about the neural mechanisms of visual and olfactory information processing.
Abstract: Floral colour signals are used by pollinators as predictors of nutritional rewards, such as nectar. But as insect pollinators often need to invest energy to maintain their body temperature above the ambient temperature, floral heat might also be perceived as a reward. Here we show that bumblebees (Bombus terrestris) prefer to visit warmer flowers and that they can learn to use colour to predict floral temperature before landing. In what could be a widespread floral adaptation, plants may modulate their temperature to encourage pollinators to visit.
Abstract: For Immanuel Kant, time was the very form of the inner sense, the bedrock of our consciousness and also the origin of arithmetic ability. New research on bumblebees has shown that even an invertebrate with a brain the size of a pinhead can actively sense the passage of elapsed time, allowing it to predict when certain salient events will occur in the future.
Abstract: In humans, visual search tasks are commonly used to address the question of how visual attention is allocated in a specific task and how individuals search for a specific object (;target') among other objects (;distractors') that vary in number and complexity. Here, we apply the methodology of visual search experiments to honeybees, which we trained to choose a coloured disc (target) among a varying number of differently coloured discs (distractors). We measured accuracy and decision time as a function of distractor number and colour. We found that for all colour combinations, decision time increased and accuracy decreased with increasing distractor number, whereas performance increased when more targets were present. These findings are characteristic of a serial search in primates, when stimuli are examined sequentially. We found no evidence for parallel search in bees, which would be characterized by a ;pop out' effect, in which the slope of decision time (and accuracy) over distractor number would be near zero. Additionally, we found that decision time and number of errors were significantly higher when bees had to choose a blue target among yellow distractors compared with the inverse colour combination, a phenomenon known as search asymmetry in humans.
Abstract: When the frenzied and irregular food-recruitment dances of bumblebees were first discovered, it was thought that they might represent an evolutionary prototype to the honeybee waggle dance. It later emerged that the primary function of the bumblebee dance was the distribution of an alerting pheromone. Here, we identify the chemical compounds of the bumblebee recruitment pheromone and their behaviour effects. The presence of two monoterpenes and one sesquiterpene (eucalyptol, ocimene and farnesol) in the nest airspace and in the tergal glands increases strongly during foraging. Of these, eucalyptol has the strongest recruitment effect when a bee nest is experimentally exposed to it. Since honeybees use terpenes for marking food sources rather than recruiting foragers inside the nest, this suggests independent evolutionary roots of food recruitment in these two groups of bees.
Abstract: Australian crab spiders Thomisus spectabilis sit on the petals of flowers and ambush prey such as honeybees. White-coloured T. spectabilis reflect in the UV (UV+ spiders) and previous research has shown that their presence, curiously, attracts honeybees to daisies. We applied an UV-absorber (Parsol) to create UV-absorbing (UV-) spiders that did not reflect any light below 395 nm wavelength. These physical changes of visual signals generated by crab spiders caused honeybees to avoid flowers with UV- spiders on their petals. They also affected the perception of UV- spiders by honeybees and a potential avian predator (blue tits). Compared to UV+ spiders, UV- spiders produced less excitation of the UV-photoreceptors in honeybees and blue tits, which translated into a reduced UV-receptor contrast and a reduced overall colour contrast between UV- spiders and daisy petals. Our results reveal that a clean physical elimination of reflection in the UV range affects perception in predators and prey and ultimately changes the behaviour of prey.
Abstract: Although it has received less coverage than in vertebrates, the study of insect social learning has a rich history with spectacular examples of how individuals extract knowledge from other animals. Several new studies on crickets and social bees have now shown how insects can adjust their behaviour adaptively by making use of cues generated inadvertently by other individuals.
Abstract: Recognising individuals using facial cues is an important ability. There is evidence that the mammalian brain may have specialised neural circuitry for face recognition tasks, although some recent work questions these findings. Thus, to understand if recognising human faces does require species-specific neural processing, it is important to know if non-human animals might be able to solve this difficult spatial task. Honeybees (Apis mellifera) were tested to evaluate whether an animal with no evolutionary history for discriminating between humanoid faces may be able to learn this task. Using differential conditioning, individual bees were trained to visit target face stimuli and to avoid similar distractor stimuli from a standard face recognition test used in human psychology. Performance was evaluated in non-rewarded trials and bees discriminated the target face from a similar distractor with greater than 80% accuracy. When novel distractors were used, bees also demonstrated a high level of choices for the target face, indicating an ability for face recognition. When the stimuli were rotated by 180 degrees there was a large drop in performance, indicating a possible disruption to configural type visual processing.
Abstract: The mineral, total amino acid, and sterol compositions of pollen collected by Apis mellifera L. were compared with the pollen of a plant consumed by Bombus terrestris (L.): Arbutus unedo L. This plant provides the predominant food resource for the main autumn generation of B. terrestris in southern France. Honey bees also forage on this plant, although only for nectar. The mineral composition of 30 pollen samples collected by honey bees is close to the presently known requirements of A. mellifera, except for Cu and Mn, which are substantially lower. The total amino acid mean composition of a set of 54 pollen samples fits the basic requirements of honey bees except for valine, isoleucine, and methionine, which are present in lower concentrations in all the samples. For pollen of A. unedo, the amino acid balance is not very different from that of the survey. The main sterolic component in pollen of A. unedo, beta-sitosterol, is known to have antifeedant effects on A. mellifera. Honey bees cannot dealkylate C29 sterols like beta-sitosterol or delta5-avenasterol to obtain C27 cholesterol and ecdysteroids. Because these phytosterols as well as cholesterol are nearly absent from pollen of A. unedo, the metabolic capabilities of Apis seem unadapted to this plant. On the contrary, pollen of A. unedo is freely consumed by B. terrestris, which develops huge autumn populations solely on this food. These data indicate that the sterolic metabolisms of B. terrestris and A. mellifera differ, allowing separation in foraging activity.
Abstract: Australian crab spiders Thomisus spectabilis ambush pollinating insects, such as honeybees (Apis mellifera) on flowers, and can change their body colour between yellow and white. It is traditionally assumed that the spiders change their colour to match the flower colour, thus rendering them cryptic to insect prey. Here, we test this assumption combining state-of-the-art knowledge of bee vision and behavioural experiments. In the field, yellow spiders are only found on yellow daisies (Chrysanthemum frutescens), whereas white spiders are found on yellow and white daisies. These field patterns were confirmed in the laboratory. When given the choice between white and yellow daisies, yellow spiders preferred yellow daisies, whereas white spiders showed only a slight but non-significant preference for white flowers. Thus, T. spectabilis select background colours according to their own body colour. When viewed from a distance, bees use an achromatic signal produced by their green receptors for target detection. Through this visual channel, white spiders on white flowers, and yellow spiders on yellow flowers are virtually undetectable. From a closer distance of a few centimetres, when bees evaluate colour contrast, the combination of spider colour against different flower backgrounds affected the response of honeybees, but not in ways predicted by a classical crypsis/conspicuousness interpretation. Yellow spiders on yellow flowers are not perfectly matched when interpreted through the colour vision of a honeybee. Nevertheless, honeybees showed indifference to the presence of a spider, equally landing on vacant or spider-occupied flowers. Likewise, white spiders are poorly hidden on white flowers, as white spiders reflect ultraviolet light strongly, while white flowers do not. Surprisingly, bees are attracted to this contrast, and significantly more honeybees preferred white flowers occupied by white spiders. White spiders on yellow flowers produce the highest colour contrast and bees again preferred spider-occupied flowers. Yellow spiders on white flowers were the only pairing where bees rejected spider-occupied flowers, especially in cases where the contrast between the two was relatively strong. Thus, T. spectabilis select flower colours adaptively in a way that deceives honeybees, or at least does not deter them.
Abstract: Worldwide trade in non-native bumblebees remains largely unrestricted despite well-documented cases where introductions of non-native bees have gone dramatically wrong. Within Europe, indiscriminate importation of non-native populations of bumblebees (Bombus terrestris) for the pollination of glasshouse crops continues on a massive scale. However, no risk assessment has been conducted for these introductions, perhaps because B. terrestris is considered a native species, so shipping populations from one region to another has been implicitly assumed to present no risk. This view is clearly unjustified because Bombus terrestris populations differ significantly in their genetic makeup as demonstrated by strong differences in coat colour and behavioural traits. Therefore, for the first time we compare an important competitive trait, namely foraging performance, between commercially available B. terrestris populations in contrasting environments. We test whether commercially reared populations differ in their nectar foraging performance and whether this is influenced by both their source environment and the one they are introduced into. We do this by means of a reciprocal transplant experiment. Strong, consistent inter-population differences in performance occurred irrespective of test location: Canary Island bees (B. t. canariensis) were superior to Sardinian bees (B. t. sassaricus), which were generally superior to mainland European bees (B. t. terrestris). These inter-population differences in performance were largely explained by inter-population variation in forager size, with larger bees being superior foragers. However, even when body size was accounted for, "native" bees were not superior to transplanted non-native bees in all but one case. We conclude that non-native populations, especially those with large foragers, can be highly competitive foragers. This could lead to their establishment and displacement of native bees. Therefore, we recommend that unregulated movements of non-native B. terrestris populations within Europe should not be carried out without a full risk assessment.
Abstract: The principal challenge faced by any color vision system is to contend with the inherent ambiguity of stimulus information, which represents the interaction between multiple attributes of the world (e.g., object reflectance and illumination). How natural systems deal with this problem is not known, although traditional hypotheses are predicated on the idea that vision represents object reflectance accurately by discounting early in processing the conflating effects of illumination. Here, we test the merits of this general supposition by confronting bumblebees (Bombus terrestris) with a color discrimination task that can be solved only if information about the illuminant is not discounted but maintained in processing and thus available to higher-order learned behavior. We show that bees correctly use the intensity and chromaticity of illumination as a contextual cue to guide them to different target colors. In fact, we trained bees to choose opposite, rather than most similar, target colors after an illumination change. This performance cannot be explained with a simple color-constancy mechanism that discounts illumination. Further tests show that bees do not use a simple assessment of the overhead illumination, but that they assess the spectral relationships between a floral target and its background. These results demonstrate that bees can be color-constant without discounting the illuminant; that, in fact, they can use information about the illuminant itself as a salient source of information.
Abstract: Accurate recognition requires that visual systems must be able to discriminate between target and distractor stimuli. Flowers are learned and recognised by bees using visual cues including colour and shape. We investigated whether bees were able to learn to discriminate between colours differently depending upon absolute or differential conditioning. For absolute conditioning bees were rewarded with sucrose solution for visits to target flowers. When distractor stimuli were subsequently presented, a high level of discrimination was observed if there was a perceptually large colour distance separating distractors and targets, but for a perceptually small colour distance the bees generalised and did not discriminate between stimuli. When provided with differential conditioning where both target and distractors were present, the bees learnt to discriminate stimuli separated by a perceptually small colour distance. This shows that for bees to learn fine colour discrimination tasks it is important to use differential conditioning. The findings are discussed within the context of the necessity for plants to produce distinctive flower colours.
Abstract: Receiver-bias models of signal evolution predict that male sexually selected traits evolve through prior selection for other functions. Female three-spined sticklebacks (Gasterosteus aculeatus) in many populations show a mating preference for males with a red throat and jaw. It has been proposed that this preference evolved because the choice of males with red coloration confers direct and indirect benefits to females in accordance with the Fisher-Zahavi model of sexual selection. We present indirect evidence that the preference is an effect of a receiver bias in the perceptual or cognitive system of G. aculeatus for the colour red, which may have arisen in the context of foraging. In laboratory trials, male and female three-spined and nine-spined sticklebacks (Pungitius pungitius) responded most strongly to red objects outside a mating context. This result demonstrates a correlation between a sexually selected trait and an intrinsic attraction to red objects, and supports the sensory-exploitation model for the evolution of red nuptial coloration in three-spined sticklebacks.
Abstract: The performance of individual bumblebees at colour discrimination tasks was tested in a controlled laboratory environment. Bees were trained to discriminate between rewarded target colours and differently coloured distractors, and then tested in non-rewarded foraging bouts. For the discrimination of large colour distances bees made relatively fast decisions and selected target colours with a high degree of accuracy, but for the discrimination of smaller colour distances the accuracy decreased and the bees response times to find correct flowers significantly increased. For small colour distances there was also significant linear correlations between accuracy and response time for the individual bees. The results show both between task and within task speed-accuracy tradeoffs in bees, which suggests the possibility of a sophisticated and dynamic decision-making process.
Abstract: Bees often facilitate pollination of important greenhouse crops. Individual bumblebees Bombus terrestris were therefore tested in an indoor flight arena to evaluate whether or not search time to find flowers was influenced by the inclusion or exclusion of ultraviolet radiation. Plastic model flowers of similar spectral properties to flowers of tomato Lycopersicon esculentum Mill. were used to evaluate bee search efficiency. The results show that bumblebees perceive when ultraviolet radiation is either removed or added to an illumination source; however, the bumblebees rapidly learn to find model flowers with equal efficiency in either illumination environment. The behavioural results are interpreted in relation to a colorimetric analysis showing how bumblebees are capable of using their visual system to forage efficiently in environments that exclude ultraviolet radiation.
Abstract: Individual bumblebees were trained to choose between rewarded target flowers and non-rewarded distractor flowers in a controlled illumination laboratory. Bees learnt to discriminate similar colours, but with smaller colour distances the frequency of errors increased. This indicates that pollen transfer might occur between flowers with similar colours, even if these colours are distinguishable. The effect of similar colours on reducing foraging accuracy of bees is evident for colour distances high above discrimination threshold, which explains previous field observations showing that bees do not exhibit complete flower constancy unless flower colour between species is distinct. Bees tested in spectrally different illumination conditions experienced a significant decrease in their ability to discriminate between similar colours. The extent to which this happens differs in different areas of colour space, which is consistent with a von Kries-type model of colour constancy. We find that it would be beneficial for plant species to have highly distinctive colour signals to overcome limitations on the bees performance in reliably judging differences between similar colours. An exception to this finding was flowers that varied in shape, in which case bees used this cue to compensate for inaccuracies of colour vision.
Abstract: Bees returning from a feeder placed in a narrow tunnel that is lined with a chequered pattern will strongly overestimate travel distance. This finding supports the view that their distance estimation is based on integrating optic flow experienced during flight. Here, we use chequered tunnels with various colour combinations as a tool to identify the spectral channel used by bees to gauge travel distance. The probability of bees performing waggle dances after a short travel distance correlates only with the low range of the green contrast of the pattern in the tunnel. But it does not correlate with the pattern's chromatic contrast or brightness contrast. Distance estimation is therefore colour blind. We also evaluated the waggle runs as a function of colour pattern. Their duration is the code for the food source distance. Waggle run duration is entirely independent of the colour pattern used, implying that once green contrast is above detection threshold, distance estimation depends solely on the angular motion of the landscape passed in flight.
Abstract: Foragers of Bombus terrestris are able to alert their nestmates to the presence of food sources. It has been supposed that this happens at least partially through the distribution of a pheromone inside the nest. We substantiate this claim using a behavioral test in which an alerting signal is transmitted from one colony to another by long distance air transport, so excluding all other modalities of information exchange. We then investigated the source of the pheromone and were able to show that a hexane extract from tergites V-VII of bumble bee workers elicits higher activity, like a successful forager does. Extracts from other glands, such as the mandibular, labial, hypopharyngeal, and Dufour's gland as well as extracts from other parts of the cuticle had no effect. This suggests that bumble bees possess a pheromone-producing gland, similar to the Nasanov gland in honey bees. Indeed, an extract from the honey bee Nasanov gland also proved to alert bumble bee workers, suggesting a possible homology of the glands.
Abstract: In the eusocial bumblebees, distinct size variation occurs within the worker caste of a colony. We show that there are pronounced differences in compound eye optical quality between individual workers in Bombus terrestris. Using scanning electron microscopy and antidromic illumination techniques (the pseudopupil method), we demonstrate that large workers have extended facet diameters in conjunction with reduced interommatidial angles. Thus, both overall sensitivity and image resolution are superior in such individuals. Behavioural tests show that a 33% increase in body size is accompanied by 100% greater precision in single target detection. This improvement in spatial resolving power is much stronger than that predicted by surveying ommatidial arrays, indicating that measuring eye optics alone is insufficient for predictions of single object resolution, unless combined with behavioural tests. We demonstrate that in small bees the minimum number of ommatidia involved in target detection is seven, while in large workers a single ommatidium is sufficient for target detection. These findings have implications for foraging and division of labour in social insects.
Abstract: We review the physiological, molecular, and neural mechanisms of insect color vision. Phylogenetic and molecular analyses reveal that the basic bauplan, UV-blue-green-trichromacy, appears to date back to the Devonian ancestor of all pterygote insects. There are variations on this theme, however. These concern the number of color receptor types, their differential expression across the retina, and their fine tuning along the wavelength scale. In a few cases (but not in many others), these differences can be linked to visual ecology. Other insects have virtually identical sets of color receptors despite strong differences in lifestyle. Instead of the adaptionism that has dominated visual ecology in the past, we propose that chance evolutionary processes, history, and constraints should be considered. In addition to phylogenetic analyses designed to explore these factors, we suggest quantifying variance between individuals and populations and using fitness measurements to test the adaptive value of traits identified in insect color vision systems.
Abstract: Ultraviolet is an important component of the photic environment. It is used by a wide variety of animals and plants in mutualistic communication, especially in insect and flower inter-relationships. Ultraviolet reflections and sensitivity are also becoming well considered in the relationships between vertebrates and their environment. The relative importance of ultraviolet vis à vis other primary colours in trichromatic or tetrachromatic colour spaces is discussed, and it is concluded that ultraviolet is, in most cases, no more important that blue, green or red reflections. Some animals may use specific wavebands of light for specific reactions, such as ultraviolet in escape or in the detection of polarised light, and other wavebands in stimulating feeding, oviposition or mating. When colour vision and, thus, the input from more than a single spectral receptor type are concerned, we point out that even basic predictions of signal conspicuousness require knowledge of the neuronal wiring used to evaluate the signals from all receptor types, including the ultraviolet. Evolutionary analyses suggest that, at least in arthropods, ultraviolet sensitivity is phylogenetically ancient and undergoes comparatively little evolutionary fine-tuning. Increasing amounts of ultraviolet in the photic environment, as caused by the decline of ozone in the atmosphere, are not likely to affect colour vision. However, a case for which ultraviolet is possibly unique is in the colour constancy of bees. Theoretical models predict that bees will perform poorly at identifying pure ultraviolet signals under conditions of changing illumination, which may explain the near absence of pure ultraviolet-reflecting flowers in nature.
Abstract: In optimal foraging theory, search time is a key variable defining the value of a prey type. But the sensory-perceptual processes that constrain the search for food have rarely been considered. Here we evaluate the flight behavior of bumblebees (Bombus terrestris) searching for artificial flowers of various sizes and colors. When flowers were large, search times correlated well with the color contrast of the targets with their green foliage-type background, as predicted by a model of color opponent coding using inputs from the bees' UV, blue, and green receptors. Targets that made poor color contrast with their backdrop, such as white, UV-reflecting ones, or red flowers, took longest to detect, even though brightness contrast with the background was pronounced. When searching for small targets, bees changed their strategy in several ways. They flew significantly slower and closer to the ground, so increasing the minimum detectable area subtended by an object on the ground. In addition, they used a different neuronal channel for flower detection. Instead of color contrast, they used only the green receptor signal for detection. We relate these findings to temporal and spatial limitations of different neuronal channels involved in stimulus detection and recognition. Thus, foraging speed may not be limited only by factors such as prey density, flight energetics, and scramble competition. Our results show that understanding the behavioral ecology of foraging can substantially gain from knowledge about mechanisms of visual information processing.
Abstract: The question of whether bees can take novel short cuts between familiar sites has been central to the discussion about the existence of cognitive maps in these insects. The failure of bees to show this capacity in the majority of previous studies may be a result of the training procedure, because extensive training to one feeding site may have eliminated or weakened memories for other sites that were previously trained. Here we present a novel approach to this problem, by rewarding honey bees, Apis mellifera carnica, at two feeding sites, one (Sm, 630 m southeast from the hive) at which they could feed in the morning, and the other (Sa, 790 m northeast) at which they could feed in the afternoon. We then displaced bees to Sa in the morning and to Sm in the afternoon either from the other feeding site or from the hive. Bees were also displaced to two novel sites, one at a completely unfamiliar location (S4) and another that was located halfway between the two feeding sites (S3). Bees displaced from either of the feeding sites never took novel short cuts; instead, they used the homeward directions that would have been correct had they not been displaced. Bees caught at the hive entrance, however, chose the correct homeward direction not only when displaced to both feeding sites, but also when displaced to S3, although not from S4. Control bees that had been trained to only one of the feeding sites were not able to travel directly home from S3 excluding the possibility that bees used landmarks close to the hive. This is the first evidence that bees take a novel short cut by activating two vector memories simultaneously. The potential mechanisms of integrating the two memories are discussed. Since bees took novel short cuts in only one direction (to the hive) and only when displaced from the hive (not the feeders), we conclude that inference of a cognitive map in bees would be premature. Copyright 1998 The Association for the Study of Animal Behaviour.
Abstract: Navigation in honeybees is discussed against the background of the types of memories employed in the navigational task. Two questions are addressed. Do bees have goal-specific expectations, and when are novel routes travelled? Expectations are deduced from (1) context stimuli as determinants for local cue memories, (2) landmark-dependent path integration, (3) sequential learning of landmarks, and (4) motivation- and context-dependent memory retrieval. Novel routes are travelled under two conditions: (1) goal-cue-based piloting and (2) integration of simultaneously activated vector memories. Our data do not support the conclusion that memory integration in bees is organised by a cognitive map. The assumption of purely separate memories that are only retrieved according to the chain of events during navigational performance also appears to be inadequate. We favour the view that multiple memories are integrated using external and internal sources of information. Such configural memories lead to both specific expectations and novel routes.
Abstract: Based on the measurements of 1063 flower reflection spectra, we show that flower colours fall into distinct clusters in the colour space of a bee. It is demonstrated that this clustering is caused by a limited variability in the floral spectral reflectance curves. There are as few as 10 distinct types of such curves, five of which constitute 85% of all measurements. UV reflections are less frequent and always lower in intensity than reflections in other parts of the spectrum. A further cluster of colour loci is formed in the centre of the colour space. It contains the colour loci of green leaves, several other background materials and only very few flowers. We propose a system to classify the reflection functions of flowers, and a set of colour names for bee colours.
Abstract: Behavioural tests were carried out with 9 hymenopteran insect species, which ranked certain sets of coloured stimuli according to their subjective similarity to a previously memorized stimulus. Kendall's tau co-efficient is employed for the analysis of correlation between these similarity rankings and the colour distance rankings predicted by various models of neural colour computation. The models are based on the measured spectral sensitivities of photoreceptor colour types and use a variety of simple colour coding systems to derive hypothetical colour distances. The correlation between the predictions of the models and the behavioural results serves as a measure for the likelihood of existence of a colour coding system. In all species, the similarity rankings can be best explained by assuming that colour is coded on a perceptual level by two colour opponent mechanisms. Brightness differences are ignored, indicating that an intensity-coding sub-system is not used in colour discrimination by the insects investigated. The weighting factors of the colour opponent mechanisms differ between species in detail, but not in the principles involved. It is thus possible to employ a standard measure of perceptual colour distance (colour hexagon distance) to predict the capacities of colour discrimination adequately in all the tested insects.
