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First published online February 15, 2006
Journal of Experimental Biology 209, 781-788 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02060
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Nocturnal colour vision – not as rare as we might think

Almut Kelber* and Lina S. V. Roth

Department of Cell and Organism Biology, Vision Group, Lund University, Helgonavägen 3, S-22362 Lund, Sweden


Figure 1
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Fig. 1. (A) Simple 4-stage model of colour discrimination with two spectral types of receptors. At receptor stage 1, the signals r1a, r1b and r2a, r2b arise when the animal looks at the two colours a and b. At the subsequent neural stage 2, two neural interactions are possible: summation of the receptor signals, resulting in the achromatic signals Saa and Sab, and subtraction (or comparison), resulting in the chromatic signals Scha and Schb. At stage 3, the signal arising from the two colours a and b are compared, and finally, a behaviour will occur with probability P. (Adapted from Kelber et al., 2003bGo.) (B) Natural light levels and limits of colour vision in different animals. Humans lose their colour vision ability in dim moonlight and so do diurnal honeybees Apis mellifera (Menzel, 1981Go). Nocturnal hawkmoths (Deilephila elpenor, Hyles lineata and H. gallii) can still see colour at dim starlight levels. Nocturnal geckos (Tarentola chezaliae) were tested at dim moonlight levels.

 

Figure 2
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Fig. 2. (A) Schematic drawing of an apposition compound eye. The aperture (A) is defined by the diameter of a single corneal lens (c). Pigment (p) between the crystalline cones (cc) isolates ommatidia optically. Rhabdom (rh) length (l) and diameter (d) influence sensitivity; f, focal length. (B) Schematic drawing of a superposition compound eye. The clear zone (cz) interspaced between the crystalline cones and rhabdoms allows light entering through a large number of facets to be focussed on one rhabdom. This enlarges the aperture by factor of up to 1000. (C) Superposition eye of Deilephila elpenor (photo courtesy of Pär Brannström). cz, clear zone; re, retina. (D) Schematic drawings of the structure of the rhabdom of D. elpenor (adapted from Schlecht et al., 1978). B, basement membrane; Rh, rhabdom; Tr, tracheal tapetum, N, nucleus. Receptors 1 and 2 are blue- or UV-sensitive; receptors 3–9 are green-sensitive. (E) About 1000 facets of D. elpenor that build the superposition aperture glow when the eye is illuminated and viewed from the same direction. Photo courtesy of Michael Pfaff. (F) Random arrays of ommatidial types in the crepuscular hawkmoth Manduca sexta (redrawn from White et al., 2003Go). White circles, ommatidia with all three receptor types; black circles, ommatidia with green and blue receptors; grey circles, ommatidia with green and UV receptors. Arrows show the eye horizon. (G) The effect of filtering in the long fused rhabdom of a dark-adapted nocturnal hawkmoth. The broken lines represent the sensitivities that would result from self-screening, if the long photoreceptors of D. elpenor had open rhabdoms. The solid lines represent the sensitivities resulting from filtering in the fused and tiered rhabdom.

 

Figure 3
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Fig. 3. (A) Anatomy of three anatomical types (A–C) of photoreceptor in diurnal (left) and nocturnal (right) geckos (modified from Underwood, 1970Go). Note the different lengths of the outer segments that cause different quantum captures. (B) Spectral sensitivities of the 5 µm short cones of a diurnal gecko (broken lines) and the 50 µm long cones of a nocturnal gecko (solid lines). UV, UV receptor; B, blue receptor; G, green receptor. (C) Cone mosaic of the nocturnal gecko Teratoscincus scincus (redrawn from Loew et al., 1996Go). Green circles, green-sensitive cones; blue circles, blue-sensitive cones; blue-green circles, double cones with a green and a blue receptor; grey-green circles, double cones with a green and a UV receptor.

 

Figure 4
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Fig. 4. The use of chromatic vision. (A) The reflectances of a typical yellow and a typical blue flower and a green leaf. (B) The spectral composition of direct sunlight and skylight in a shadow, measured shortly before sunset, on a summer day in Utah, USA. (C) The achromatic contrast between both flowers and the green leaf in both illuminations differ dramatically for the green receptor of D. elpenor. (D) The colour loci of all three stimuli in the colour triangle of D. elpenor are rather constant in both illuminations, even without the assumption of colour constancy. UV, UV light; B, blue light; G, green light. (For details and methods of all calculations, see Johnsen et al., 2006.)

 

Figure 5
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Fig. 5. At starlight intensities of illumination, nocturnal hawkmoths of the species Deilephila elpenor learned to discriminate a training colour from eight different shades of grey and from two other colours but not from brighter or darker shades of the training colour. (A) The animal choosing one of the stimuli in the set-up. Discrimination occurred when the training colour was blue (B) or yellow (C). (Data from Kelber et al., 2002Go.)

 

Figure 6
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Fig. 6. Two nocturnal geckos of the species Tarentola chezaliae learnt to take a cricket from forceps decorated with a pattern made from blue squares (right). The forceps decorated with a grey pattern (left) always held a salted cricket, which geckos always refused. Both geckos predominantly chose blue in all tests, independent of the overall intensity of the grey pattern (represented by the different shades of the grey patterns on the abscissa). (Data from Roth and Kelber, 2004Go.)

 





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