Nicotine in floral nectar pharmacologically influences bumblebee learning of floral features.

Many plants defend themselves against herbivores by chemical deterrents in their tissues and the presence of such substances in floral nectar means that pollinators often encounter them when foraging. The effect of such substances on the foraging behaviour of pollinators is poorly understood. Using artificial flowers in tightly-controlled laboratory settings, we examined the effects of the alkaloid nicotine on bumblebee foraging performance. We found that bumblebees confronted simultaneously with two equally rewarded nicotine-containing and nicotine-free flower types are deterred only by unnaturally high nicotine concentrations. This deterrence disappears or even turns into attraction at lower nectar-relevant concentrations. The alkaloid has profound effects on learning in a dose-dependent manner. At a high natural dose, bees learn the colour of a nicotine-containing flower type more swiftly than a flower type with the same caloric value but without nicotine. Furthermore, after experiencing flowers containing nicotine in any tested concentration, increasing numbers of bumblebees stay more faithful to these flowers, even if they become a suboptimal choice in terms of reward. These results demonstrate that alkaloids enhance pollinator flower constancy, opening new perspectives in co-evolutionary process between plants and pollinators.

Speed and accuracy in nest-mate recognition: a hover wasp prioritizes face recognition over colony odour cues to minimize intrusion by outsiders.

Social insects have evolved sophisticated recognition systems enabling them to accept nest-mates but reject alien conspecifics. In the social wasp, Liostenogaster flavolineata (Stenogastrinae), individuals differ in their cuticular hydrocarbon profiles according to colony membership; each female also possesses a unique (visual) facial pattern. This species represents a unique model to understand how vision and olfaction are integrated and the extent to which wasps prioritize one channel over the other to discriminate aliens and nest-mates. Liostenogaster flavolineata females are able to discriminate between alien and nest-mate females using facial patterns or chemical cues in isolation. However, the two sensory modalities are not equally efficient in the discrimination of 'friend' from 'foe'. Visual cues induce an increased number of erroneous attacks on nest-mates (false alarms), but such attacks are quickly aborted and never result in serious injury. Odour cues, presented in isolation, result in an increased number of misses: erroneous acceptances of outsiders. Interestingly, wasps take the relative efficiencies of the two sensory modalities into account when making rapid decisions about colony membership of an individual: chemical profiles are entirely ignored when the visual and chemical stimuli are presented together. Thus, wasps adopt a strategy to 'err on the safe side' by memorizing individual faces to recognize colony members, and disregarding odour cues to minimize the risk of intrusion from colony outsiders.

Information processing in miniature brains.

Since a comprehensive understanding of brain function and evolution in vertebrates is often hobbled by the sheer size of the nervous system, as well as ethical concerns, major research efforts have been made to understand the neural circuitry underpinning behaviour and cognition in invertebrates, and its costs and benefits under natural conditions. This special feature of Proceedings of the Royal Society B contains an idiosyncratic range of current research perspectives on neural underpinnings and adaptive benefits (and costs) of such diverse phenomena as spatial memory, colour vision, attention, spontaneous behaviour initiation, memory dynamics, relational rule learning and sleep, in a range of animals from marine invertebrates with exquisitely simple nervous systems to social insects forming societies with many thousands of individuals working together as a 'superorganism'. This introduction provides context and history to tie the various approaches together, and concludes that there is an urgent need to understand the full neuron-to-neuron circuitry underlying various forms of information processing-not just to explore brain function comprehensively, but also to understand how (and how easily) cognitive capacities might evolve in the face of pertinent selection pressures. In the invertebrates, reaching these goals is becoming increasingly realistic.

Biological significance of distinguishing between similar colours in spectrally variable illumination: bumblebees (Bombus terrestris) as a case study.

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.

Bumble bees alert to food with pheromone from tergal gland.

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.

Limits to the salience of ultraviolet: lessons from colour vision in bees and birds.

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.

Visual constraints in foraging bumblebees: flower size and color affect search time and flight behavior.

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.

The evolution of color vision in insects.

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.

Bees travel novel homeward routes by integrating separately acquired vector memories

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.

The knowledge base of bee navigation

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.

Ultraviolet as a component of flower reflections, and the colour perception of Hymenoptera.

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.

Opponent colour coding is a universal strategy to evaluate the photoreceptor inputs in Hymenoptera.

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.