Do White and Green Look the Same to a Bee?

M. Vorobyev (Y), N. Hempel de Ibarra, R. Brandt, M. Giurfa

Institut fr Neurobiologie, Freie Universitt Berlin, Knigin-Luise-Strasse 2830, D-14195 Berlin, Germany e-mail: Vorobyev6zedat.fu-berlin.de, Tel.: c49-30-8386441, Fax: c49-30-838-5455
Received: 22 March 1999 / Accepted in revised form: 2 July 1999

Abstract The hexagon model of color vision predicts that white flowers which reflect ultraviolet light resemble green foliage to a bees eye, whereas, according to other models of the bee color vision, UVreflecting white is discriminable from foliage green. The hexagon model is widely used in ecologically and evolutionary oriented literature, and the predicted similarity between white and green has been recently presented as a well established fact (Waser and Chittka 1998). We show that bees detect UVreflecting white objects presented on a green background, a finding that is in disagreement with the predictions of the hexagon model. The question of how flower colors look in the eyes of a potential pollinator is central for understanding the evolution of flower colors and has practical consequences in horticulture. Flowers that are difficult to detect against their background are likely to attract only few pollinators and are therefore selected against. According to the hexagon model of the bee color space (Chittka 1992), UV-reflecting white and green of leaves occupy color loci that are very close to each other, and thus they must look similar (Chittka et al. 1994). The alleged similarity between white and green has been widely advertised to ecologists, and it has been suggested that UV-reflecting white flowers are scarce because pollinators fail to detect them (Kevan et al. 1996). Furthermore, Waser and Chittka (1998) have recently suggested that white mutants of the snapdragon Antirrhinum majus produce less fruit than do the violet wild-type plants because flower white is perceived to be similar to leaf green by insect pollinators. Since the reflectance spectra of green leaves differ substantially from white in both shape and average reflectance (Fig. 1a), it is difficult to imagine that insects such as bees with well developed color vision cannot discriminate between these two colors.
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Honeybee color vision has been extensively studied (for review see Menzel and Backhaus 1991) and several models have been proposed to describe it (for review see Vorobyev and Brandt 1997). All models assume that bees use only chromatic cues for color discrimination, whereas achromatic cues are ignored (for review see Vorobyev and Brandt 1997). Chromatic vision, which is mediated by color opponent interactions between the receptors, is by definition sensitive to changes in the shape of the stimulus spectrum but not to changes in intensity of the light stimulus. Because bees possess three spectral types of photoreceptors (Autrum and Zwell 1964; Menzel and Blakers 1976) the receptor signals may combine, forming two independent color opponent mechanisms. These mechanisms define a two-dimensional color opponent space (Backhaus 1991). Detectability of a colored object against a differently colored background is predicted by the distance, DS, between the chromatic loci of the two colors in the animals color space; the larger the distance, the better the detectability is. The distance in turn increases with increasing of the signal-to-noise ratio (SNR) of chromatic mechanisms, which is generally a function of the intensity of the light stimulus. The models of the bee vision can be classified according to the postulated dependence of the SNR on the light intensity, which may remain invariant, decrease, or increase. For example, a color-triangle model (Wyscecki and Stiles 1982, pp. 120, 121; for application to honeybee vision see Neumeyer 1981) postulates that SNR and thus detectability is independent of light intensity. By comparison, the photon-noise-limited color opponent model (Vorobyev and Osorio 1998; Vorobyev et al. 1998) postulates that the SNR increases with increasing light intensity, thus making bright stimuli easy to detect. Finally, the color-hexagon model (Chittka 1992) assumes that receptor signals saturate when the target
Naturwissenschaften 86, 592594 (1999) Q Springer-Verlag 1999

Fig. 1. a) Reflectance spectra of a green leaf, of the green paper used in the experiments, and of UV-reflecting white and gray. b) Predictions for detectability by a honeybee eye of UV reflecting grays on green paper background using three published models. The reflectance of gray varies from 0.01 (close to black) to 1 (ideal white). The reflectance of the stimuli used in our study are labeled as Gray and White. Detectability of a color against a background is given by the distance in the color space to the background, DS, To simplify the comparison, DS is scaled to unity for the optimal gray reflectance as predicted by the hexagon model. The models calculate DS from the receptor quantum catches qS, qM, qL, where indexes S, M, L correspond, respectively, to short-, middle-, and long-wavelengths receptors. The quantum catches are scaled so that the quantum catch for the background is equal to unity. The color triangle presentation is obtained in the unit plane, qScqMcqLp1 and DSp;(Dx) 2c(Dy) 2 , where x and y denote two orthogonal directions in this plane (Neumeyer 1981). The color hexagon assumes that receptor signals are qi given by receptor excitations, which are calculated as Ei p . 1cqi Coding is performed by two unspecified color opponent mechanisms: xpsin (607) (ELES) and ypEM0.5 (ELcES), and DSp;(Dx) 2c(Dy) 2 (Chittka 1992). The photon-noise-limited color opponent model postulates that coding is performed by two unspecified color opponent mechanisms, whose accuracy is limited by the noise of receptor mechanisms (Vorobyev and Osorio 1998). The rela1 tive receptor noise is given by vipv 0 . And the color distance is i qi calculated as 2 2 2 v S (DfLPDfM) 2cvM (DfLPDfS) 2cvL(DfSPDfM) 2 (DS) 2 p , 2 2 (vS vM) c(vS vL) c(vM vL) 2 where fipln(qi), (Vorobyev et al. 1998). According to electophysio0 0 logical recording in single receptor cells vS p0.13, vM p0,06 and 0 vL p0.12 (Peitsch 1992)

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intensity exceeds that of the background (SNR decreases with increasing light intensity), thus making bright stimuli difficult to detect. According to the hexagon model the optimum detectability occurs when the average stimulus reflectance is similar to that of the background (Fig. 1b). Consequently a gray object presented on a green background would be easier to detect than a white object, while other models (Vorobyev and Brandt 1997) predict either that white and gray objects are equally well detected, or that white objects are easier to detect than are gray ones. To test the conflicting predictions of the various models we trained honeybees Apis mellifera L. to detect UV-reflecting white or gray targets presented on a green background. The intensity of gray was chosen so as to provide optimal detectability as predicted by the hexagon model. Our white was predicted to be indistinguishable from green. Backgrounds were made from a green cardboard (HKS58N, Stuttgart-Feuerbach, Germany) whose spectrum in the visible range of bees (300630 nm) was similar to that of leaves (Fig. 1a). The targets which reflect uniformly across the spectrum, includ-

ing the UV were created using BaSO4 powder (white) or a mixture of BaSO4 and carbon powder (gray). The experimental procedure was similar to that described elsewhere (Giurfa et al. 1996). Bees were trained to enter a Y-maze illuminated by natural daylight and collect there a 50% sucrose solution. A circular white or gray stimulus (8 cm diameter) was placed on the green background in one arm of the Y-maze (2025 cm from the entrance): the other arm presented the background alone. A sucrose reward was offered at the center of the disk, and the disk was presented alternately, in a pseudorandom order, in the right or the left arm. The first 30 choices of individual bees were recorded. After testing for homogeneity (x 2 test), the choices of individual bees were pooled and percentages of choices in favor of the arm with the disk were calculated. Contrary to the predictions of the hexagon model, our experiments show clearly that bees detect white objects on a green background (Fig. 2), whereas gray objects on the same background are detected less easily. This may indicate either that SNR of chromatic mechanisms increases with increasing
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Fig. 2. Results of detection experiments with individually marked free-flying honeybees. Error bars 95% confidence intervals (Fishers exact test). N Number of individual bees; n total number of choices

light intensity, as postulated by the photon-noiselimited color opponent model (Vorobyev and Osorio 1998; Vorobyev et al. 1998), or that achromatic vision is also used for detection of colored stimuli (Giurfa and Vorobyev 1998), or both. In any case, our results imply that the hexagon model does not provide adequate predictions for stimuli which differ in intensity, one of the most basic properties of visual stimuli. Bees as humans do see white flowers on green backgrounds. A number of evolutionary and ecological speculations (e.g., Chittka 1996, 1997; Chittka and Waser 1997; Chittka et al. 1994; Kevan et al. 1996; Waser and Chittka 1998) have been based on the color hexagon model. Since the predictions of the hexagon model are at odds with behavioral data, these speculations should be revised.
Acknowledgements We thank R. Menzel for fruitful discussions and valuable suggestions, M. Lehrer, E. Warrant, D. Osorio, J. Partridge, T. Cronin, and J. Marshall for helpful comments and corrections of the manuscript. M. Vorobyev and M. Giurfa were supported by Deutsche Forschungsgemeinschaft (AZ Me365/20-2), N. Hempel de Ibarra by the Academy of Science of Berlin-Brandenburg. This research was carried out according to regulations for animal experiments as stipulated in German law.

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