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First published online August 22, 2008
Journal of Experimental Biology 211, 2752-2758 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.018630
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Multifocal optical systems and pupil dynamics in birds

Olle E. Lind*, Almut Kelber and Ronald H. H. Kröger

1Department of Cell and Organism Biology, Lund University, Helgonavägen 3, 223 62 Lund, Sweden


Figure 1
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  		Fig. 1. Modes of operation of monofocal and multifocal lenses. The left side of the dotted line represents a chromatically uncorrected, monofocal lens and the right side a multifocal lens. The monofocal lens focuses green light properly on the retina, but blue and red light are focused in front and behind the retina, respectively, because of longitudinal chromatic aberration. The multifocal lens is, in this example, divided into three zones, each having the correct focal length for a narrow band of wavelengths (`colors'). The outer zone (b) is adjusted for blue, the intermediate zone (r) for red, and the inner zone (g) for green light. Blue, red and green are therefore all in focus, and a sharp color image is created. However, red light, for example, also passes through the outer B zone of the lens and is severely defocused. Such light that has passed through zones not suited to focus its particular wavelength generates a contrast-reducing background. In a terrestrial eye, the cornea and crystalline lens may together constitute an optical system that operates according to the same principle.

 

Figure 2
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  		Fig. 2. The advantage of a slit pupil in an eye with a multifocal optical system. (A) The eye has three zones of different refractive powers. The zones focus light in the blue (b), red (r) and green (g) ranges of the spectrum, represented by the same colors in the figure. The iris is the black outermost region. (B) The pupil constricts circularly and the iris shades the blue-focusing zone. (C) A slit pupil allows light to pass through all zones of the optical system irrespective of the state of pupil constriction.

 

Figure 3
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  		Fig. 3. Ray-tracing diagram showing the principle behind eccentric infrared slope-based videorefractometry. The ocular lens is bifocal with an outer zone of smaller refractive power than the centre. The lens is illustrated as it appears on the image taken by the camera. Reflected light that passes through the upper part of the outer zone enters the camera lens while the cover blocks light from the lower part. The opposite is true for the inner zone. This leads to ring-like patterns in the pupillary reflex captured by the camera.

 

Figure 4
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  		Fig. 4. Videorefractive images from bird eyes and manufactured lenses. (A) The reflex from a manufactured monofocal lens is smooth as is the reflex from (C) emu (Dromaius novaehollandiae; Struthioniformes) and (E) emperor penguin (Aptenodytes forsteri; Sphenisciformes). (A,C) Eyes in hyperopic refractive states relative to the camera have bright upper sides. (E) The eye of the emperor penguin is myopic and therefore has a bright lower side. (B) The reflex from an artificial bifocal lens with an outer zone of smaller refractive power than the inner zone. There is high similarity between the reflexes from the custom-made bifocal lens and the eyes of (D) the great horned owl (Bubo virginianus; Strigiformes) and (F) the lilac-breasted roller (Coracias caudatus; Coraciiformes). The reflexes from the eyes of the Psittaciformes (G) Tanimbar cockatoo (Cacatua goffiniana) and (H) grey parrot (Psittacus erithacus) are more complex, suggesting that the optical systems of these species consist of more than two zones of different refractive powers. Scale bars: 1 cm (A,B); 1 mm (C H).

 

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  		Fig. 5. Pupil dynamics in (A) humans [Homo sapiens sapiens, data from De Groot and Gebhard (De Groot and Gebhard, 1952Go)], (B) cats [Felis sylvestris; broken line; data from Wilcox and Barlow (Wilcox and Barlow, 1975Go)] and mice [Mus musculus; solid line; data from Grozdanic et al. (Grozdanic et al., 2003Go)], (C) snowy owls (Bubo scandiacus, N=2), (D) Ural owls (Strix uralensis, N=2), (E) blue-fronted parrots (Amazona aestiva, N=2), and (F) grey parrots (Psittacus erithacus, N=2). Pupil size is given as percentage area of the fully opened pupil. No systematic differences between individuals of the same species of bird were observed, and pupil sizes were averaged over both individuals, 8–10 samples/intensity level. The gradient bar in A illustrates rod (scotopic)-, rod and cone (mesopic)- and cone (photopic)-based vision in humans. The steepest portions of the curves were compared by their first derivatives [f'(x)]. The responsiveness of the pupillary light reflex is very high in mice and similar tendencies are present in parrots. Humans, cats and owls have pupil dynamics of lower gain. Furthermore, the parrot pupils open fully at illumination levels comparable to human mesopic conditions while the owl pupils reach this state in dimmer, human scotopic illumination. The horizontal broken line marks the relative size of the innermost zone of the multifocal optics (the line in B applies to the mice eyes only). The lens system can be regarded as multifocal for pupil sizes that exceed this level. Error bars are standard deviations.

 

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