Johannes Spaethe

Comparative psychophysics of bumblebee and honeybee colour discrimination and object detection

Bumblebee (Bombus terrestris) discrimination of targets with broadband reflectance spectra was tested using simultaneous viewing conditions, enabling an accurate determination of the perceptual limit of colour discrimination excluding confounds from memory coding (experiment 1). The level of colour discrimination in bumblebees, and honeybees (Apis mellifera) (based upon previous observations), exceeds predictions of models considering receptor noise in the honeybee. Bumblebee and honeybee photoreceptors are similar in spectral shape and spacing, but bumblebees exhibit significantly poorer colour discrimination in behavioural tests, suggesting possible differences in spatial or temporal signal processing. Detection of stimuli in a Y-maze was evaluated for bumblebees (experiment 2) and honeybees (experiment 3). Honeybees detected stimuli containing both green-receptor-contrast and colour contrast at a visual angle of approximately 5°, whilst stimuli that contained only colour contrast were only detected at a visual angle of 15°. Bumblebees were able to detect these stimuli at a visual angle of 2.3° and 2.7°, respectively. A comparison of the experiments suggests a tradeoff between colour discrimination and colour detection in these two species, limited by the need to pool colour signals to overcome receptor noise. We discuss the colour processing differences and possible adaptations to specific ecological habitats.

Size determines antennal sensitivity and behavioral threshold to odors in bumblebee workers

The eusocial bumblebees exhibit pronounced size variation among workers of the same colony. Differently sized workers engage in different tasks (alloethism); large individuals are found to have a higher probability to leave the colony and search for food, whereas small workers tend to stay inside the nest and attend to nest duties. We investigated the effect of size variation on morphology and physiology of the peripheral olfactory system and the behavioral response thresholds to odors in workers of Bombus terrestris. Number and density of olfactory sensilla on the antennae correlate significantly with worker size. Consistent with these morphological changes, we found that antennal sensitivity to odors increases with body size. Antennae of large individuals show higher electroantennogram responses to a given odor concentration than those of smaller nestmates. This finding indicates that large antennae exhibit an increased capability to catch odor molecules and thus are more sensitive to odors than small antennae. We confirmed this prediction in a dual choice behavioral experiment showing that large workers indeed are able to respond correctly to much lower odor concentrations than small workers. Learning performance in these experiments did not differ between small and large bumblebees. Our results clearly show that, in the social bumblebees, variation in olfactory sensilla number due to size differences among workers strongly affects individual odor sensitivity. We speculate that superior odor sensitivity of large workers has favored size-related division of labor in bumblebee colonies.

Honeybee odometry: Performance in varying natural terrain

Recent studies have shown that honeybees flying through short, narrow tunnels with visually textured walls perform waggle dances that indicate a much greater flight distance than that actually flown. These studies suggest that the bees “odometer” is driven by the optic flow (image motion) that is experienced during flight. One might therefore expect that, when bees fly to a food source through a varying outdoor landscape, their waggle dances would depend upon the nature of the terrain experienced en route. We trained honeybees to visit feeders positioned along two routes, each 580 m long. One route was exclusively over land. The other was initially over land, then over water and, finally, again over land. Flight over water resulted in a significantly flatter slope of the waggle-duration versus distance regression, compared to flight over land. The mean visual contrast of the scenes was significantly greater over land than over water. The results reveal that, in outdoor flight, the honeybees odometer does not run at a constant rate; rather, the rate depends upon the properties of the terrain. The bees perception of distance flown is therefore not absolute, but scene-dependent. These findings raise important and interesting questions about how these animals navigate reliably.

Molecular characterization and expression of the UV opsin in bumblebees: three ommatidial subtypes in the retina and a new photoreceptor organ in the lamina

SUMMARY Ultraviolet-sensitive photoreceptors have been shown to be important for a variety of visual tasks performed by bees, such as orientation, color and polarization vision, yet little is known about their spatial distribution in the compound eye or optic lobe. We cloned and sequenced a UV opsin mRNA transcript from Bombus impatiens head-specific cDNA and, using western blot analysis, detected an eye protein band of ∼41 kDa, corresponding to the predicted molecular mass of the encoded opsin. We then characterized UV opsin expression in the retina, ocelli and brain using immunocytochemistry. In the main retina, we found three different ommatidial types with respect to the number of UV opsin-expressing photoreceptor cells, namely ommatidia containing two, one or no UV opsin-immunoreactive cells. We also observed UV opsin expression in the ocelli. These results indicate that the cloned opsin probably encodes the P350 nm pigment, which was previously characterized by physiological recordings. Surprisingly, in addition to expression in the retina and ocelli, we found opsin expression in different parts of the brain. UV opsin immunoreactivity was detected in the proximal rim of the lamina adjacent to the first optic chiasm, which is where studies in other insects have found expression of proteins involved in the circadian clock, period and cryptochrome. We also found UV opsin immunoreactivity in the core region of the antennal lobe glomeruli and different clusters of perikarya within the protocerebrum, indicating a putative function of these brain regions, together with the lamina organ, in the entrainment of circadian rhythms. In order to test for a possible overlap of clock protein and UV opsin spatial expression, we also examined the expression of the period protein in these regions.

Visual attention in a complex search task differs between honeybees and bumblebees

SUMMARY Mechanisms of spatial attention are used when the amount of gathered information exceeds processing capacity. Such mechanisms have been proposed in bees, but have not yet been experimentally demonstrated. We provide evidence that selective attention influences the foraging performance of two social bee species, the honeybee Apis mellifera and the bumblebee Bombus terrestris. Visual search tasks, originally developed for application in human psychology, were adapted for behavioural experiments on bees. We examined the impact of distracting visual information on search performance, which we measured as error rate and decision time. We found that bumblebees were significantly less affected by distracting objects than honeybees. Based on the results, we conclude that the search mechanism in honeybees is serial like, whereas in bumblebees it shows the characteristics of a restricted parallel-like search. Furthermore, the bees differed in their strategy to solve the speed–accuracy trade-off. Whereas bumblebees displayed slow but correct decision-making, honeybees exhibited fast and inaccurate decision-making. We propose two neuronal mechanisms of visual information processing that account for the different responses between honeybees and bumblebees, and we correlate species-specific features of the search behaviour to differences in habitat and life history.

Visual search and the importance of time in complex decision making by bees

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.

How to know which food is good for you: bumblebees use taste to discriminate between different concentrations of food differing in nutrient content

ABSTRACT In view of the ongoing pollinator decline, the role of nutrition in bee health has received increasing attention. Bees obtain fat, carbohydrates and protein from pollen and nectar. As both excessive and deficient amounts of these macronutrients are detrimental, bees would benefit from assessing food quality to guarantee an optimal nutrient supply. While bees can detect sucrose and use it to assess nectar quality, it is unknown whether they can assess the macronutrient content of pollen. Previous studies have shown that bees preferentially collect pollen of higher protein content, suggesting that differences in pollen quality can be detected either by individual bees or via feedback from larvae. In this study, we examined whether and, if so, how individuals of the buff-tailed bumblebee (Bombus terrestris) discriminate between different concentrations of pollen and casein mixtures and thus nutrients. Bumblebees were trained using absolute and differential conditioning of the proboscis extension response (PER). As cues related to nutrient concentration could theoretically be perceived by either smell or taste, bees were tested on both olfactory and, for the first time, chemotactile perception. Using olfactory cues, bumblebees learned and discriminated between different pollen types and casein, but were unable to discriminate between different concentrations of these substances. However, when they touched the substances with their antennae, using chemotactile cues, they could also discriminate between different concentrations. Bumblebees are therefore able to discriminate between foods of different concentrations using contact chemosensory perception (taste). This ability may enable them to individually regulate the nutrient intake of their colonies. Highlighted Article: Bumblebee workers are able to discriminate different concentrations of a food mixture and hence nutrients by using their sense of taste, which may enable them to individually regulate food intake.

Sex and Caste-Specific Variation in Compound Eye Morphology of Five Honeybee Species

Ranging from dwarfs to giants, the species of honeybees show remarkable differences in body size that have placed evolutionary constrains on the size of sensory organs and the brain. Colonies comprise three adult phenotypes, drones and two female castes, the reproductive queen and sterile workers. The phenotypes differ with respect to tasks and thus selection pressures which additionally constrain the shape of sensory systems. In a first step to explore the variability and interaction between species size-limitations and sex and caste-specific selection pressures in sensory and neural structures in honeybees, we compared eye size, ommatidia number and distribution of facet lens diameters in drones, queens and workers of five species (Apis andreniformis, A. florea, A. dorsata, A. mellifera, A. cerana). In these species, male and female eyes show a consistent sex-specific organization with respect to eye size and regional specialization of facet diameters. Drones possess distinctly enlarged eyes with large dorsal facets. Aside from these general patterns, we found signs of unique adaptations in eyes of A. florea and A. dorsata drones. In both species, drone eyes are disproportionately enlarged. In A. dorsata the increased eye size results from enlarged facets, a likely adaptation to crepuscular mating flights. In contrast, the relative enlargement of A. florea drone eyes results from an increase in ommatidia number, suggesting strong selection for high spatial resolution. Comparison of eye morphology and published mating flight times indicates a correlation between overall light sensitivity and species-specific mating flight times. The correlation suggests an important role of ambient light intensities in the regulation of species-specific mating flight times and the evolution of the visual system. Our study further deepens insights into visual adaptations within the genus Apis and opens up future perspectives for research to better understand the timing mechanisms and sensory physiology of mating related signals.

Blue colour preference in honeybees distracts visual attention for learning closed shapes

Spatial vision is an important cue for how honeybees (Apis mellifera) find flowers, and previous work has suggested that spatial learning in free-flying bees is exclusively mediated by achromatic input to the green photoreceptor channel. However, some data suggested that bees may be able to use alternative channels for shape processing, and recent work shows conditioning type and training length can significantly influence bee learning and cue use. We thus tested the honeybees’ ability to discriminate between two closed shapes considering either absolute or differential conditioning, and using eight stimuli differing in their spectral characteristics. Consistent with previous work, green contrast enabled reliable shape learning for both types of conditioning, but surprisingly, we found that bees trained with appetitive-aversive differential conditioning could additionally use colour and/or UV contrast to enable shape discrimination. Interestingly, we found that a high blue contrast initially interferes with bee shape learning, probably due to the bees innate preference for blue colours, but with increasing experience bees can learn a variety of spectral and/or colour cues to facilitate spatial learning. Thus, the relationship between bee pollinators and the spatial and spectral cues that they use to find rewarding flowers appears to be a more rich visual environment than previously thought.

Age‐related and light‐induced plasticity in opsin gene expression and in primary and secondary visual centers of the nectar‐feeding ant Camponotus rufipes

Camponotus rufipes workers are characterized by an age‐related polyethism. In the initial weeks of adult life, young workers perform tasks inside the nest before they switch to multimodal foraging tasks outside. We tested the hypothesis that this transition is accompanied by profound adaptations in the peripheral and central visual systems. Our results show that C. rufipes workers of all tested ages (between 1 and 42 days) express three genes encoding for ultraviolet (UV), blue (BL), and long‐wavelength (LW1) sensitive opsins in their retina, which are likely to provide the substrate for trichromatic color vision. Expression levels of all three opsin genes increased significantly within the first two weeks of adulthood and following light exposure. Interestingly, the volumes of all three optic neuropils (lamina, medulla, and lobula) showed corresponding volume increases. Tracing of connections to higher visual centers in the mushroom bodies (MBs) revealed only one optic pathway, the anterior superior optic tract, emerging from the medulla and sending segregated input to the MB‐calyx collar. The MB collar volumes and densities of synaptic complexes (microglomeruli, MGs) increased with age. Exposure to light for 4 days induced a decrease in MG densities followed by an increase after extended light exposure. This shows that plasticity in retinal opsin gene expression and structural neuroplasticity in primary and secondary visual centers comprise both “experience‐independent” and “experience‐dependent” elements. We conclude that both sources of plasticity in the visual system represent important components promoting optimal timing of the interior–forager transition and flexibility of age‐related division of labor.