Seeing the light: Illumination as a contextual cue to color choice behavior in bumblebees

Abstract

The principal challenge faced by any color vision system is to contend with the inherent ambiguity of stimulus information, which represents the interaction between multiple attributes of the world (e.g., object reflectance and illumination). How natural systems deal with this problem is not known, although traditional hypotheses are predicated on the idea that vision represents object reflectance accurately by discounting early in processing the conflating effects of illumination. Here, we test the merits of this general supposition by confronting bumblebees (Bombus terrestris) with a color discrimination task that can be solved only if information about the illuminant is not discounted but maintained in processing and thus available to higher-order learned behavior. We show that bees correctly use the intensity and chromaticity of illumination as a contextual cue to guide them to different target colors. In fact, we trained bees to choose opposite, rather than most similar, target colors after an illumination change. This performance cannot be explained with a simple color-constancy mechanism that discounts illumination. Further tests show that bees do not use a simple assessment of the overhead illumination, but that they assess the spectral relationships between a floral target and its background. These results demonstrate that bees can be color-constant without discounting the illuminant; that, in fact, they can use information about the illuminant itself as a salient source of information.color vision ͉ ecology ͉ vision

Improved color constancy in honey bees enabled by parallel visual projections from dorsal ocelli

“…Color signals captured in the bees' photoreceptors are sequentially processed along multiple neural pathways, including opponent neurons in the inner layer of the medulla, which seem to exhibit a capacity to adapt to stimulus input (19). Bumble bees are capable of sensing changes in overhead illumination and making complex foraging decisions (20)(21)(22), suggesting potential use of contextual information for perceiving variations in ambient illumination. For example, considering changes in the illumination from short to long wavelength-rich radiation, free flying bumblebees (23) and honey bees (17, 24) make reliable color decisions for most dynamic changing conditions.…”

Illumination preference, illumination constancy and colour discrimination by bumblebees in an environment with patchy light

“…Indeed, bees initially avoided switching between illumination conditions in patchy light, but gradually became indifferent to such transitions. The initial avoidance of switching between patches of different lighting clearly indicates that bees perceive changes in overhead light (Dyer, 2006;Lotto and Chittka, 2005), thus not 'discounting' the illumination as one might expect from a perfect colour constancy algorithm (von Helmholtz, 1896).…”

“…This was the default illumination for the arena, and also the illumination in the 'daylight' patches during patchy light experiments. The illumination spectrum is taken from Lotto and Chittka (Lotto and Chittka, 2005). We simulated leaf-shade in this setup with coloured filters placed above the arena to alter the intensity and spectral composition of the incoming light.…”

“…Colour distances in colour space correspond to subjective similarity of colours; therefore, the two colours are predicted to be somewhat harder to distinguish under green light than under unobscured daylight. Bees foraging in patchy light Signals for these reflectance spectra in the bees' UV, blue and green receptors were calculated using the integral of the spectral sensitivity curves of Bombus terrestris photoreceptors (Skorupski et al, 2007), the illumination spectrum with or without a green filter (Lotto and Chittka, 2005) and the reflectance spectrum of the flower type in question, using methods described in Chittka (Chittka, 1992); their colour hexagon coordinates are displayed in Fig.1B. The colour hexagon is a graphical representation of a bee's colour space where the discriminability of different colours correlates with the distance between them in colour space.…”

“…However, it has been demonstrated that bees directly perceive changes in illuminating light (Dyer and Chittka, 2004b;Dyer, 2006). Additionally, bees can use the illumination as a contextual cue in foraging tasks (Lotto and Chittka, 2005). Further studies (Dyer, 1998;Dyer, 1999) used data on bees' photoreceptor responses and the reflectance spectra of natural flowers to predict that some flowers would appear to change in colour to bees' eyes under altered lighting, indicating that bees' colour constancy might only be approximate.…”