- Email: [email protected]
Visual Optics: The Shapes of Pupils
Dispatch R167
CO2. Planta 218, 152–158. 6. Norby, R.J., Wullschelger, S.D., Gunderson, C.A., Johnson, D.W., and Ceulemans, R. (1999). Tree responses to rising CO2 in field experiments: implications for the future forest. Plant Cell Environ. 22, 683–714. 7. Gifford, R.M. (2003). Plant respiration in productivity models: conceptualization, representation and issues for global terrestrial carbon-cycle research. Funct. Plant Biol. 30, 171–186. 8. Gifford, R.M. (1992). Interactions of carbon dioxide with growth limiting environmental factors in vegetation productivity: Implications for the global carbon cycle. Adv. Bioclimatol. 1, 25–58. 9. Birks, H.J.B., and Birks, H.H. (2004). The rise and fall of forests. Science 305, 484–485. 10. Reich, P.B. (2005). Global biogeochemistry of plant chemistry: filling in the blanks. New Phytol. 168, 263–266. 11. Lynch, J.P., and St. Clair, S.B. (2004). Mineral stress: the missing link in understanding how global climate change will affect plants in real world soils. Field Crops Res. 90, 101–115. 12. Ward, J.K., Harris, J.M., Cerling, T.E., Wiedenhoeft, A., Lott, M.J., Dearing, M.-
13.
14.
15.
16.
17.
D., Coltrain, J.B., and Ehleringer, J.R. (2005). Carbon starvation in glacial trees recovered from the La Brea tar pits, southern California. Proc. Natl. Acad. Sci. USA 102, 690–694. Hessen, D.O., Ågren, G.I., Anderson, T.R., Elser, J.J., and de Ruiter, P.C. (2004). Carbon sequestration in ecosystems: the role of stoichiometry. Ecology 85, 1179–1192. Hughes, L., and Bazzazz, F.A. (2001). Effects of elevated CO2 on five aphidplant interactions. Entomol. Exp. Appl. 99, 87–96. Atkin, O.K., Bruhn, D., Hurry, V.M., and Tjoelker, M.G. (2005). The hot and the cold: unravelling the variable response of plant respiration to temperature. Funct. Plant Biol. 32, 87–105. Centritto, M., Luc, H.S.J., and Jarvis, P.G. (1999). Long-term effects of elevated carbon dioxide concentration and provenance on four clones of Sitka spruce (Picea sitchensis). I. Plant growth, allocation and ontogeny. Tree Physiol. 19, 799–806. Gielen, B., Calfapietra, C., Lukac, M., Wittig, V.E., De Angelis, P., Janssens, I.A., Moscatelli, M.C., Grego, S., Cotrufo, M.F., and Godbold, D.L. (2005). Net carbon storage in a poplar plantation
Visual Optics: The Shapes of Pupils The eyes of many terrestrial vertebrates have slit-shaped pupils. A new hypothesis links this pupil shape to the way that vertebrate lenses compensate for chromatic aberration. Michael F. Land Human eyes have circular pupils, but a great many animals have pupils that are oval or slit-shaped. These slits/ovals may be oriented vertically (as in crocodiles, vipers, cats and foxes), or horizontally (as in some rays, flying frogs, mongooses and ungulates such as sheep and hippopotami). The explanation usually given for the use of a slit pupil is that it can exclude light more effectively than a circular pupil, and so slit pupils tend to be found in the eyes of animals with a crepuscular or nocturnal lifestyle that need to protect their eyes during daylight [1]. The slit pupil of a cat, for example, can change the intensity on the retina 135-fold, compared to 10-fold in man [2]. This has never seemed to be an entirely convincing explanation, however, as some animals (such as the tarsier) have circular pupils that can close down very effectively, to a diameter of about half a
millimeter [1], and in many ungulates the rather rectangular pupils do not close to a narrow slit in bright light. A recent paper by Malmström and Kröger [3] offers a much more intriguing explanation of the oval pupil; it relates to the way that vertebrate lenses have evolved to handle color. It has been known at least since James Clerk Maxwell, who famously contemplated the eye of his breakfast herring [4,5], that spherical fish lenses are well corrected for spherical aberration — the tendency for peripheral rays to be focused too close to the lens. This correction results from the lens having a particular near-parabolic gradient of refractive index [5,6]. Chromatic aberration, however, in which blue light is focused substantially closer to the lens than red light, was thought until recently to be uncorrected. This is because protein solutions cannot be produced with different chromatic dispersions, and thus achromatic
18.
19.
20.
(POPFACE) after three years of free-air CO2 entichment. Tree Physiol. 25, 1399–1408. Raymond, P.A., and Cole, J.J. (2003). Increase in the export of alkalinity from. North America’s largest river. Science 301, 88–91. The Royal Society Policy Document 12/05. 2005. Ocean acidification due to. increasing atmospheric carbon dioxide. The Royal Society, London. Orr, J.C., Fabry, V.J., Aumont, O., Bopp, L., Doney, S.C., Feely, R.A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F., et al. (2005). Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 427, 681–686.
1University
of Dundee at SCRI, Scottish Crop Research Institute, Invergowrie, Dundee DD2 5DA, UK. E-mail: [email protected] 2Scottish Crop Research Institute, Invergowrie, Dundee DD2 5DA, UK. E-mail: [email protected]
DOI: 10.1016/j.cub.2006.02.041
lens combinations cannot be made from biological lens material. Fish lenses, however, have found another way round the problem. In 1999, Kröger and his colleagues [7] showed that the gradient in fish lenses is not exactly that predicted for perfect spherical correction. It has a systematically lumpy profile, which results in the lens having several different focal lengths for concentric zones at different distances from the center. Each of these focal zones produces an image at a different distance from the lens, and each such image has its own chromatic aberration, which one would think would make a bad situation even worse. But the beauty of the arrangement is that the red image from one zone actually coincides with the green image from another zone and the blue image from the third zone, meaning that there is one plane in which there is a sharp image for all the wavelengths relevant to the fish’s color vision system (Figure 1A). Of course much of the light is not well focused in this plane and this will reduce image contrast, so this is not a perfect solution, but it is much better than the alternative of having a single focal length with a sharp image for only one wavelength.
Current Biology Vol 16 No 5 R168
A
Figure 1. Principle of multifocal lens and effect of pupil shape. (A) Two-zone spherical lens in which the inner zone has a shorter average focal length than the outer zone. The longitudinal chromatic aberration in the images produced by the two zones make it possible to have infocus blue and red images in the same plane. (B) A lens as in (A) but with three chromatic zones contributing to the image. (C) The effect of a circular pupil on (B) is to eliminate the contributions of the outer zones. (D) With a slit pupil all three zones are still sampled.
B
C
D
In focus blue-red image
Current Biology
Most fish do not have contractile pupils, but most land vertebrates do. The terrestrial optical system is a little more complex than in fish, because of corneal refraction, but the same considerations apply: partial chromatic correction can be achieved by the use of multi-focal lenses. Using a non-invasive device — an infra-red videorefractometer [8] — which shows up zonal optical discontinuities in lenses as a series of rings, Malmström and Kröger [3] examined 20 species of amphibians, reptiles and mammals with a variety of pupil shapes. They found that all species with slit pupils had distinct rings in the photorefractive images and hence multi-focal optics, and all but two of the species with round pupils had mono-focal optics. The reason they give for this association between slit pupils and multi-focal optics is that a slit samples from the whole diameter of the lens, even in daylight when the pupil is constricted, whereas a constricted circular pupil will only sample the central zone of the lens (Figure 1B–D). Thus the multi-focal chromatic correction is preserved for slit pupils, but not for circular pupils.
Why, then, do only some animals have slit pupils and multi-focal optics? This combination seems to be associated mainly with partial nocturnality. Diurnal animals such as ourselves operate mainly with a small pupil that gives a large depth of focus and minimises the effects of chromatic aberration. At night, when our pupils are open, vision is monochromatic and resolution is in any case poor, so that there is no need for multi-focal chromatic correction. But for animals that hunt in dim light, or that need to remain visually vigilant in dim conditions, a large pupil relative to the focal length is a necessity. This in turn means that image blur results from even small amounts of defocus, and a chromatically corrected optical system is needed. There are still some important gaps in this story. Most crepuscular land animals —active at dusk or dawn — have color vision: mammals are generally dichromats, with two cone types [9], and reptiles and amphibia are trichromats or tetrachromats [3]. We know very little, however, about the extent to which these animals make use of their color vision in dim light, which is when
their pupils would be wide open and multi-focal optics most valuable. If, like us, they switch completely to monochromatic rod vision then the case for multi-focal optics and slit pupils is weakened. Currently, dim light color vision has only been demonstrated in a nocturnal gecko, which has an allcone retina [10]. There are some other unexplained anomalies. Domestic cats have multi-focal optics and slit pupils but tigers have monofocal optics and round pupils. House mice have multi-focal optics in combination with a round pupil. Many monochromatic cephalopod molluscs such as Octopus have horizontal slit pupils. All this indicates that there is more to be found out, but nevertheless the association of multi-focal optics and slit pupils is strong, and provides an ecologically satisfying explanation for what had previously seemed a strangely arbitrary phenomenon. References 1. Walls, G.L. (1942). The Vertebrate Eye and its Adaptive Radiation. (Bloomington Hills Michigan: The Cranbrook Institute of Science). 2. Hughes, A. (1977). The topography of vision in mammals of contrasting life style: comparative optics and retinal organization. In Handbook of Sensory Physiology VII/5. F. Crescitelli, ed. (Berlin: Springer-Verlag) pp. 613–756. 3. Malmström, T., and Kröger, R.H.H. (2006). Pupil shapes and lens optics in the eyes of terrestrial vertebrates. J. Exp. Biol. 209, 18–25. 4. Maxwell, J.C. (1854). Some solutions of problems. Collected Works 1, 76–78. 5. Pumphrey, R.J. (1961). Concerning vision. In The Cell and the Organism, J.A. Ramsay, V.B. Wigglesworth, eds. (Cambridge, UK: Cambridge University Press), pp. 193–208. 6. Jagger, W.S. (1992). The optics of the spherical fish lens. Vision Res. 32, 1271–1284. 7. Kröger, R.H.H., Campbell, M.C.W., Fernald, R.D., and Wagner, H.-J. (1999). Multifocal lenses compensate for chromatic defocus in vertebrate eyes. J. Comp. Physiol. [A] 184, 361–369. 8. Schaeffel, F., Farkas, L., and Howland, H.C. (1987). Infrared photoretinoscope. Appl. Opt. 26, 1505–1509. 9. Jacobs, G.H. (1993). The distribution and nature of colour vision amongst the mammals. Biol. Rev. Camb. Philos. Soc. 68, 413–471. 10. Roth, L.S, Kelber, A. (2004). Nocturnal colour vision in geckos. Proc. Biol. Sci. B 271 (letters supplement), S485–S487.
Department of Biology and Environmental Science, University of Sussex, Brighton BN1 9QG, UK. E-mail: [email protected]. DOI: 10.1016/j.cub.2006.02.046
CO2. Planta 218, 152–158. 6. Norby, R.J., Wullschelger, S.D., Gunderson, C.A., Johnson, D.W., and Ceulemans, R. (1999). Tree responses to rising CO2 in field experiments: implications for the future forest. Plant Cell Environ. 22, 683–714. 7. Gifford, R.M. (2003). Plant respiration in productivity models: conceptualization, representation and issues for global terrestrial carbon-cycle research. Funct. Plant Biol. 30, 171–186. 8. Gifford, R.M. (1992). Interactions of carbon dioxide with growth limiting environmental factors in vegetation productivity: Implications for the global carbon cycle. Adv. Bioclimatol. 1, 25–58. 9. Birks, H.J.B., and Birks, H.H. (2004). The rise and fall of forests. Science 305, 484–485. 10. Reich, P.B. (2005). Global biogeochemistry of plant chemistry: filling in the blanks. New Phytol. 168, 263–266. 11. Lynch, J.P., and St. Clair, S.B. (2004). Mineral stress: the missing link in understanding how global climate change will affect plants in real world soils. Field Crops Res. 90, 101–115. 12. Ward, J.K., Harris, J.M., Cerling, T.E., Wiedenhoeft, A., Lott, M.J., Dearing, M.-
13.
14.
15.
16.
17.
D., Coltrain, J.B., and Ehleringer, J.R. (2005). Carbon starvation in glacial trees recovered from the La Brea tar pits, southern California. Proc. Natl. Acad. Sci. USA 102, 690–694. Hessen, D.O., Ågren, G.I., Anderson, T.R., Elser, J.J., and de Ruiter, P.C. (2004). Carbon sequestration in ecosystems: the role of stoichiometry. Ecology 85, 1179–1192. Hughes, L., and Bazzazz, F.A. (2001). Effects of elevated CO2 on five aphidplant interactions. Entomol. Exp. Appl. 99, 87–96. Atkin, O.K., Bruhn, D., Hurry, V.M., and Tjoelker, M.G. (2005). The hot and the cold: unravelling the variable response of plant respiration to temperature. Funct. Plant Biol. 32, 87–105. Centritto, M., Luc, H.S.J., and Jarvis, P.G. (1999). Long-term effects of elevated carbon dioxide concentration and provenance on four clones of Sitka spruce (Picea sitchensis). I. Plant growth, allocation and ontogeny. Tree Physiol. 19, 799–806. Gielen, B., Calfapietra, C., Lukac, M., Wittig, V.E., De Angelis, P., Janssens, I.A., Moscatelli, M.C., Grego, S., Cotrufo, M.F., and Godbold, D.L. (2005). Net carbon storage in a poplar plantation
Visual Optics: The Shapes of Pupils The eyes of many terrestrial vertebrates have slit-shaped pupils. A new hypothesis links this pupil shape to the way that vertebrate lenses compensate for chromatic aberration. Michael F. Land Human eyes have circular pupils, but a great many animals have pupils that are oval or slit-shaped. These slits/ovals may be oriented vertically (as in crocodiles, vipers, cats and foxes), or horizontally (as in some rays, flying frogs, mongooses and ungulates such as sheep and hippopotami). The explanation usually given for the use of a slit pupil is that it can exclude light more effectively than a circular pupil, and so slit pupils tend to be found in the eyes of animals with a crepuscular or nocturnal lifestyle that need to protect their eyes during daylight [1]. The slit pupil of a cat, for example, can change the intensity on the retina 135-fold, compared to 10-fold in man [2]. This has never seemed to be an entirely convincing explanation, however, as some animals (such as the tarsier) have circular pupils that can close down very effectively, to a diameter of about half a
millimeter [1], and in many ungulates the rather rectangular pupils do not close to a narrow slit in bright light. A recent paper by Malmström and Kröger [3] offers a much more intriguing explanation of the oval pupil; it relates to the way that vertebrate lenses have evolved to handle color. It has been known at least since James Clerk Maxwell, who famously contemplated the eye of his breakfast herring [4,5], that spherical fish lenses are well corrected for spherical aberration — the tendency for peripheral rays to be focused too close to the lens. This correction results from the lens having a particular near-parabolic gradient of refractive index [5,6]. Chromatic aberration, however, in which blue light is focused substantially closer to the lens than red light, was thought until recently to be uncorrected. This is because protein solutions cannot be produced with different chromatic dispersions, and thus achromatic
18.
19.
20.
(POPFACE) after three years of free-air CO2 entichment. Tree Physiol. 25, 1399–1408. Raymond, P.A., and Cole, J.J. (2003). Increase in the export of alkalinity from. North America’s largest river. Science 301, 88–91. The Royal Society Policy Document 12/05. 2005. Ocean acidification due to. increasing atmospheric carbon dioxide. The Royal Society, London. Orr, J.C., Fabry, V.J., Aumont, O., Bopp, L., Doney, S.C., Feely, R.A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F., et al. (2005). Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 427, 681–686.
1University
of Dundee at SCRI, Scottish Crop Research Institute, Invergowrie, Dundee DD2 5DA, UK. E-mail: [email protected] 2Scottish Crop Research Institute, Invergowrie, Dundee DD2 5DA, UK. E-mail: [email protected]
DOI: 10.1016/j.cub.2006.02.041
lens combinations cannot be made from biological lens material. Fish lenses, however, have found another way round the problem. In 1999, Kröger and his colleagues [7] showed that the gradient in fish lenses is not exactly that predicted for perfect spherical correction. It has a systematically lumpy profile, which results in the lens having several different focal lengths for concentric zones at different distances from the center. Each of these focal zones produces an image at a different distance from the lens, and each such image has its own chromatic aberration, which one would think would make a bad situation even worse. But the beauty of the arrangement is that the red image from one zone actually coincides with the green image from another zone and the blue image from the third zone, meaning that there is one plane in which there is a sharp image for all the wavelengths relevant to the fish’s color vision system (Figure 1A). Of course much of the light is not well focused in this plane and this will reduce image contrast, so this is not a perfect solution, but it is much better than the alternative of having a single focal length with a sharp image for only one wavelength.
Current Biology Vol 16 No 5 R168
A
Figure 1. Principle of multifocal lens and effect of pupil shape. (A) Two-zone spherical lens in which the inner zone has a shorter average focal length than the outer zone. The longitudinal chromatic aberration in the images produced by the two zones make it possible to have infocus blue and red images in the same plane. (B) A lens as in (A) but with three chromatic zones contributing to the image. (C) The effect of a circular pupil on (B) is to eliminate the contributions of the outer zones. (D) With a slit pupil all three zones are still sampled.
B
C
D
In focus blue-red image
Current Biology
Most fish do not have contractile pupils, but most land vertebrates do. The terrestrial optical system is a little more complex than in fish, because of corneal refraction, but the same considerations apply: partial chromatic correction can be achieved by the use of multi-focal lenses. Using a non-invasive device — an infra-red videorefractometer [8] — which shows up zonal optical discontinuities in lenses as a series of rings, Malmström and Kröger [3] examined 20 species of amphibians, reptiles and mammals with a variety of pupil shapes. They found that all species with slit pupils had distinct rings in the photorefractive images and hence multi-focal optics, and all but two of the species with round pupils had mono-focal optics. The reason they give for this association between slit pupils and multi-focal optics is that a slit samples from the whole diameter of the lens, even in daylight when the pupil is constricted, whereas a constricted circular pupil will only sample the central zone of the lens (Figure 1B–D). Thus the multi-focal chromatic correction is preserved for slit pupils, but not for circular pupils.
Why, then, do only some animals have slit pupils and multi-focal optics? This combination seems to be associated mainly with partial nocturnality. Diurnal animals such as ourselves operate mainly with a small pupil that gives a large depth of focus and minimises the effects of chromatic aberration. At night, when our pupils are open, vision is monochromatic and resolution is in any case poor, so that there is no need for multi-focal chromatic correction. But for animals that hunt in dim light, or that need to remain visually vigilant in dim conditions, a large pupil relative to the focal length is a necessity. This in turn means that image blur results from even small amounts of defocus, and a chromatically corrected optical system is needed. There are still some important gaps in this story. Most crepuscular land animals —active at dusk or dawn — have color vision: mammals are generally dichromats, with two cone types [9], and reptiles and amphibia are trichromats or tetrachromats [3]. We know very little, however, about the extent to which these animals make use of their color vision in dim light, which is when
their pupils would be wide open and multi-focal optics most valuable. If, like us, they switch completely to monochromatic rod vision then the case for multi-focal optics and slit pupils is weakened. Currently, dim light color vision has only been demonstrated in a nocturnal gecko, which has an allcone retina [10]. There are some other unexplained anomalies. Domestic cats have multi-focal optics and slit pupils but tigers have monofocal optics and round pupils. House mice have multi-focal optics in combination with a round pupil. Many monochromatic cephalopod molluscs such as Octopus have horizontal slit pupils. All this indicates that there is more to be found out, but nevertheless the association of multi-focal optics and slit pupils is strong, and provides an ecologically satisfying explanation for what had previously seemed a strangely arbitrary phenomenon. References 1. Walls, G.L. (1942). The Vertebrate Eye and its Adaptive Radiation. (Bloomington Hills Michigan: The Cranbrook Institute of Science). 2. Hughes, A. (1977). The topography of vision in mammals of contrasting life style: comparative optics and retinal organization. In Handbook of Sensory Physiology VII/5. F. Crescitelli, ed. (Berlin: Springer-Verlag) pp. 613–756. 3. Malmström, T., and Kröger, R.H.H. (2006). Pupil shapes and lens optics in the eyes of terrestrial vertebrates. J. Exp. Biol. 209, 18–25. 4. Maxwell, J.C. (1854). Some solutions of problems. Collected Works 1, 76–78. 5. Pumphrey, R.J. (1961). Concerning vision. In The Cell and the Organism, J.A. Ramsay, V.B. Wigglesworth, eds. (Cambridge, UK: Cambridge University Press), pp. 193–208. 6. Jagger, W.S. (1992). The optics of the spherical fish lens. Vision Res. 32, 1271–1284. 7. Kröger, R.H.H., Campbell, M.C.W., Fernald, R.D., and Wagner, H.-J. (1999). Multifocal lenses compensate for chromatic defocus in vertebrate eyes. J. Comp. Physiol. [A] 184, 361–369. 8. Schaeffel, F., Farkas, L., and Howland, H.C. (1987). Infrared photoretinoscope. Appl. Opt. 26, 1505–1509. 9. Jacobs, G.H. (1993). The distribution and nature of colour vision amongst the mammals. Biol. Rev. Camb. Philos. Soc. 68, 413–471. 10. Roth, L.S, Kelber, A. (2004). Nocturnal colour vision in geckos. Proc. Biol. Sci. B 271 (letters supplement), S485–S487.
Department of Biology and Environmental Science, University of Sussex, Brighton BN1 9QG, UK. E-mail: [email protected]. DOI: 10.1016/j.cub.2006.02.046