Honeybees (Apis mellifera) Learn Color Discriminations via Differential Conditioning Independent of Long Wavelength (Green) Photoreceptor Modulation

Abstract

BackgroundRecent studies on colour discrimination suggest that experience is an important factor in how a visual system processes spectral signals. In insects it has been shown that differential conditioning is important for processing fine colour discriminations. However, the visual system of many insects, including the honeybee, has a complex set of neural pathways, in which input from the long wavelength sensitive (‘green’) photoreceptor may be processed either as an independent achromatic signal or as part of a trichromatic opponent-colour system. Thus, a potential confound of colour learning in insects is the possibility that modulation of the ‘green’ photoreceptor could underlie observations.Methodology/Principal FindingsWe tested honeybee vision using light emitting diodes centered on 414 and 424 nm wavelengths, which limit activation to the short-wavelength-sensitive (‘UV’) and medium-wavelength-sensitive (‘blue’) photoreceptors. The absolute irradiance spectra of stimuli was measured and modelled at both receptor and colour processing levels, and stimuli were then presented to the bees in a Y-maze at a large visual angle (26°), to ensure chromatic processing. Sixteen bees were trained over 50 trials, using either appetitive differential conditioning (N = 8), or aversive-appetitive differential conditioning (N = 8). In both cases the bees slowly learned to discriminate between the target and distractor with significantly better accuracy than would be expected by chance. Control experiments confirmed that changing stimulus intensity in transfers tests does not significantly affect bee performance, and it was possible to replicate previous findings that bees do not learn similar colour stimuli with absolute conditioning.ConclusionOur data indicate that honeybee colour vision can be tuned to relatively small spectral differences, independent of ‘green’ photoreceptor contrast and brightness cues. We thus show that colour vision is at least partly experience dependent, and behavioural plasticity plays an important role in how bees exploit colour information.

Learning context modulates aversive taste strength in honey bees

“…Our results thus confirm findings from experiments in which freeflying bees were trained to discriminate a visual target paired with sucrose solution from one or various visual distracters paired with quinine solution, under the assumption that quinine would act as a strong penalty favoring learning and discrimination (Chittka et al, 2003;Dyer and Chittka, 2004;Avargues-Weber et al, 2010;Reser et al, 2012;Avargues-Weber and Giurfa, 2014). In our experiments, bees did not fly within the small Y-maze, but as in the works just mentioned, they could move, explore the maze and compare the odor stimuli and their corresponding outcomes through sampling.…”

Why colour is complex: Evidence that bees perceive neither brightness nor green contrast in colour signal processing

“…The role of brightness as a visual cue has been previously investigated using behavioural experiments (Lunau and Maier 1995;Giurfa et al 1996;Kelber 2005) and, therefore, might be an important visual signal in bee-pollinated flowers. Brightness perception is the ability to perceive stimulus intensity differences (Wyszecki and Stiles 1982;Reser et al 2012), where intensity is related to the total amount of energy reflected by a stimulus. To understand whether intensity is a meaningful signal for bee pollinators it is important to test visual perception while isolating other confounding chromatic cues (Reser et al 2012).…”

Innate colour preferences of the Australian native stingless bee Tetragonula carbonaria Sm.

“…For subsequent analyses it was important to reduce factors based upon the biological plausibility of cause. Studies on honeybee vision suggest brightness is not a major perceptual mechanism when colour is being processed Backhaus 1991;Reser et al 2012), and since this factor correlates with purity, it is reasonable to remove this potential factor from the model whilst retaining purity. Furthermore, studies on bumblebee (Lunau 1990;Lunau et al 1996;Rohde et al 2013) and honeybee ) perception show that for similar colours, purity is an honest signal that some bee pollinators do show an innate preference towards; therefore, it is biologically relevant to retain this factor and remove the correlating factor of chromatic contrast from the model.…”

“…For honeybees and bumblebees, there exist detailed data on how receptor signals facilitate colour processing at a neural level by opponent mechanisms in the brain (Kien and Menzel 1977;Yang et al 2004;Paulk et al 2009;Dyer et al 2011) which facilitates trichromatic colour perception as demonstrated in behavioural experiments (von Frisch 1914;Daumer 1956;von Helversen 1972;Giurfa 2004;Dyer et al 2008;Reser et al 2012). This detailed knowledge has allowed for the development of colour space models Chittka 1992;Vorobyev and Brandt 1997;Kemp et al 2015) to facilitate analyses of how flower signals are distributed in different environments (Chittka et al 1994;Chittka and Wells 2004).…”