Abstract
Visual abilities of the honey bee have been studied for more than 100 years, recently revealing unexpectedly sophisticated cognitive skills rivalling those of vertebrates. However, the physiological limits of the honey bee eye have been largely unaddressed and only studied in an unnatural, dark state. Using a bright display and intracellular recordings, we here systematically investigated the angular sensitivity across the light adapted eye of honey bee foragers. Angular sensitivity is a measure of photoreceptor receptive field size and thus small values indicate higher visual acuity. Our recordings reveal a fronto-ventral acute zone in which angular sensitivity falls below 1.9°, some 30% smaller than previously reported. By measuring receptor noise and responses to moving dark objects, we also obtained direct measures of the smallest features detectable by the retina. In the frontal eye, single photoreceptors respond to objects as small as 0.6° × 0.6°, with >99% reliability. This indicates that honey bee foragers possess significantly better resolution than previously reported or estimated behaviourally, and commonly assumed in modelling of bee acuity.
Highlights
The visual cognitive abilities of the honey bee, Apis mellifera, have few rivals among invertebrates
The visual acuity in honey bees has been investigated since the first decades of last century[17], our data suggest it has been underestimated in prior work, both in terms of the angular sensitivity function and the minimum feature sizes resolvable by the retina
One possible factor reconciling the smaller estimates of Δρ(i.e. higher acuity) that we found compared with prior physiological studies might lie in differences in the photochemical and mechanical dynamics underlying the different adapted states of the eye, i.e. from dark-adapted to light-adapted[9,18]
Summary
The visual cognitive abilities of the honey bee, Apis mellifera, have few rivals among invertebrates. Flower detectability and the smallest visual angle that a bee can perceive has been investigated behaviourally, revealing that bees could not discriminate a dark object smaller than 3° when trained to fly to a sugar source in a double arm arena[6,7,8] While these behavioural estimates for the lower limit to object detection seem to be reasonably well matched to prior physiological data, the fact that the latter were from eyes in a dark-adapted state might lead to underestimates of the true resolution[9]. We recorded from photoreceptors adapted to bright light conditions, closer to those that foraging bees experience in nature (300 cd/m2) We estimated both the angular sensitivity Δρ(a measure of the receptive field size of single receptors, which limits resolution) and the smallest object a single cell can detect. Our results show that honey bee foragers have 30% better resolution than previous physiological estimates and a 5 times lower limit for feature detectability than has yet been estimated behaviourally
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