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.vision ͉ detection ͉ Bombus terrestris ͉ ultraviolet ͉ neuronal channel C hoosing flower types that involve minimal search times is critical in flower visitors for several reasons. Flight is energetically the most costly activity in insects (1), and even though pollinating insects often operate at the limit of sustaining their flight activity, their fitness depends on the surplus forage brought home to provision their young (2, 3). Most flowers offer only small quantities of nectar reward, to keep pollinators moving between plants and so maximize pollen transfer. Activities of many competing flower visitors further reduce those rewards. Bees have been widely used to study foraging decisions, and behavioral ecologists have made intriguing predictions on how pollinators should behave in complex situations where flowers of different species differ in detectability (4). But the perceptual dimensions that underlie search times, and the floral parameters involved, have been little addressed. Possibly for this reason, predictions of optimal foraging theory are often inconsistent with observations of natural foraging behavior (5-8). In our experiments, we attempted to identify the neuronal channels used in the natural approach of bees toward a flower. We also evaluated the bees' flight behavior to see whether the temporal limitations imposed by the underlying neural processes could account for the bees' observed searching strategy.To estimate the color contrast a flower makes with it...
SUMMARY 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.
Size polymorphism is an important life history trait in bumblebees with strong impact on individual behavior and colony organization. Within a colony larger workers tend to serve as foragers, while smaller workers fulfill inhive tasks. It is often assumed that size-dependent division of labor relates to differences in task performance. In this study we examined size-dependent interindividual variability in foraging, i. e. whether foraging behavior and foraging capability of bumblebee workers are affected by their size. We observed two freely foraging Bombus terrestris colonies and measured i) trip number, ii) trip time, iii) proportion of nectar trips, and iv) nectar foraging rate of different sized foragers. In all observation periods large foragers exhibited a significantly higher foraging rate than small foragers. None of the other three foraging parameters was affected by worker size. Thus, large foragers contributed disproportionately more to the current nectar influx of their colony. We provide a detailed discussion of the possible proximate mechanisms underlying the differences in foraging rate. measured at departure seems to be a good estimate of empty body mass because foragers take only very small nectar provisions with them when leaving their colony (Allen et al., 1978).
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 degrees , whilst stimuli that contained only colour contrast were only detected at a visual angle of 15 degrees . Bumblebees were able to detect these stimuli at a visual angle of 2.3 degrees and 2.7 degrees , 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.
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.
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