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Limulus vision in the ocean day and night: Effects of image size and contrast

Published online by Cambridge University Press:  02 June 2009

E. D. Herzog
Affiliation:
Department of Bioengineering and Neuroscience, Syracuse University, Syracuse
M. K. Powers
Affiliation:
Department of Psychology, Vanderbilt University, Nashville
R. B. Barlow Jr
Affiliation:
Department of Bioengineering and Neuroscience, Syracuse University, Syracuse

Abstract

Male horseshoe crabs, Limulus polyphemus, use their eyes to locate mates day and night. We investigated their ability to detect targets of different size and contrast in a mating area of Buzzards Bay, Cape Cod, MA. We found that males can see large, high-contrast targets better than small, low-contrast ones. For targets of the same size, animals must be about 0.1 m closer to a low-contrast target to see it as well as a high-contrast one. For targets of the same contrast, animals must be approximately 0.2 m closer to a small target to see it as well as one twice as large. A decrease of 0.05 steradians in the size of the retinal image of a target can be compensated by a four-fold increase in contrast. About 60% of the animals detect black targets subtending 0.110 steradians (equivalent to an adult female viewed from about 0.56 m), while only 20% detect targets subtending 0.039 steradians. This study shows that horseshoe crabs maintain about constant contrast sensitivity under diurnal changes in light intensity in their natural environment. As a consequence of circadian and adaptive mechanisms in the retina, male horseshoe crabs can detect female-size objects about equally well day and night.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Barlow, R.B. Jr. (1969). Inhibitory fields in the Limulus lateral eye. Journal of General Physiology 54, 383396.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr. (1983). Circadian rhythms in the Limulus visual system. Journal of Neuroscience 3, 856870.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr. (1988). Circadian rhythm in sensitivity of the Limulus retina nearly compensates for day-night changes in ambient illumination. Investigative Ophthalmology and Visual Science (Suppl.) 29, 350.Google Scholar
Barlow, R.B. Jr. (1990). What the brain tells the eye. Scientific American 262, 9095.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr., Bolanowski, S.J. & Brachman, M.L. (1977). Efferent optic nerve fibers mediate circadian rhythms in the Limulus eye. Science 197, 8689.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr. & Fraioli, A.J. (1978). Inhibition in the Limulus lateral eye in situ. Journal of General Physiology 71, 699720.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr., Chamberlain, S.C. & Levinson, J.Z. (1980). The Limulus brain modulates the structure and function of the lateral eyes. Science 210, 10371039.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr., Ireland, L.C. & Kass, L. (1982). Vision has a role in Limulus mating behavior. Nature 296, 6566.CrossRefGoogle Scholar
Barlow, R.B. Jr., Kaplan, E., Renninger, G.H. & Saito, T. (1985). Efferent control of circadian rhythms in the Limulus lateral eye. The Seventh Taniguchi International Symposium On The Visual Sciences, Katata, Japan, 01, S65S78.Google Scholar
Barlow, R.B. Jr., Powers, M.K., Howard, H. & Kass, L. (1986). Migration of Limulus for mating: Relation to lunar phase, tide height, and sunlight. Biological Bulletin 171, 310329.CrossRefGoogle Scholar
Barlow, R.B. Jr., Kaplan, E., Renninger, G.H. & Saito, T. (1987). Circadian rhythms in Limulus photoreceptors. 1. Intracellular studies. Journal of General Physiology 89, 353378.CrossRefGoogle Scholar
Barlow, R.B. Jr. & Kaplan, E. (1989). What is the origin of photoreceptor noise? Biological Bulletin 177, 321.Google Scholar
Barlow, R.B. Jr., Birge, R.R., Kaplan, E. & Tallent, J.R. (1993). On the molecular origin of photoreceptor noise. Nature 366, 6466.CrossRefGoogle ScholarPubMed
Batra, R. & Barlow, R.B. Jr. (1982). Efferent control of pattern vision in Limulus. Society for Neuroscience Abstracts 9, 849.Google Scholar
Batra, R. & Barlow, R.B. Jr. (1990). Efferent control of temporal response properties of the Limulus lateral eye. Journal of General Physiology 95, 229244.CrossRefGoogle ScholarPubMed
Britten, K.H., Shadlen, M.N., Newsome, W.T. & Movshon, J.A. (1992). The analysis of visual motion: A comparison of neuronal and psychometric performance. Journal of Neuroscience 12, 47454765.CrossRefGoogle Scholar
Brockmann, H.J. & Penn, D. (1992). Male mating tactics in the horseshoe crab, Limulus polyphemus. Animal Behavior 44, 653665.CrossRefGoogle Scholar
Brodie, S.E., Knight, B.W. & Ratliff, F. (1978). The spatiotemporal transfer function of the Limulus lateral eye. Journal of General Physiology 72, 167202.CrossRefGoogle ScholarPubMed
Chamberlain, S.C. & Barlow, R.B. Jr. (1979). Light and efferent activity control rhabdom turnover in Limulus photoreceptors. Science 216, 361362.CrossRefGoogle Scholar
Chamberlain, S.C. & Barlow, R.B. Jr. (1987). Control of structural rhythms in the lateral eye of Limulus: Interactions of natural lighting and circadian efferent activity. Journal of Neuroscience 7, 21352144.CrossRefGoogle ScholarPubMed
Croner, L.J. & Kaplan, E. (1995). Receptive fields of P and M ganglion cells across the primate retina. Vision Research 35, 724.CrossRefGoogle Scholar
Dodge, F.A., Knight, B.W. & Toyoda, J. (1968). Voltage noise in Limulus visual cells. Science 160, 8890.CrossRefGoogle ScholarPubMed
Dodge, F.A., Porcello, D.M., Dodge, S.A., Kaplan, E. and Barlow, R.B. (1994). Noise components in Limulus vision. Biological Bulletin 187, 261262.CrossRefGoogle ScholarPubMed
Duntley, S.Q. (1963). Light in the sea. Journal of Optical Society of America 53, 214233.CrossRefGoogle Scholar
Graham, N. (1977). Visual detection of aperiodic spatial stimuli by probability summation among narrowband channels. Vision Research 17, 637652.CrossRefGoogle ScholarPubMed
Hartline, H.K., Wagner, H.G. & Ratliff, F. (1956). Inhibition in the eye of Limulus. Journal of General Physiology 39, 651673.CrossRefGoogle ScholarPubMed
Herzog, E.D. (1994). Vision in Limulus: From optics to neurons to behavior. Ph.D. Thesis, Syracuse University.Google Scholar
Herzog, E.D. & Barlow, R.B. Jr. (1991). Ultraviolet light from the nighttime sky enhances retinal sensitivity of Limulus. Biological Bulletin 181, 321322.CrossRefGoogle ScholarPubMed
Herzog, E.D. & Barlow, R.B. Jr. (1992). The Limulus-eye view of the world. Visual Neuroscience 9, 571580.CrossRefGoogle ScholarPubMed
Kaplan, E. & Barlow, R.B. Jr. (1975). Properties of visual cells in the lateral eye of Limulus in situ: Extracellular recordings. Journal of General Physiology 66, 303326.CrossRefGoogle Scholar
Kaplan, E. & Barlow, R.B. Jr. (1980). Circadian clock in Limulus brain increases response and decreases noise of retinal photoreceptors. Nature 286, 393395.CrossRefGoogle ScholarPubMed
Kaplan, E., Barlow, R.B. Jr., Renninger, G. & Purpura, K. (1990 a). Circadian rhythms in Limulus photoreceptors. 2. Quantum bumps. Journal of General Physiology 96, 665685.CrossRefGoogle ScholarPubMed
Kaplan, E., Lee, B.B. & Shapley, R.M. (1990 b). New views of primate retinal function. In Progress in Retinal Research, Vol. 9, ed. Osborne, N.N. & Chader, G.J., pp. 273336. New York: Pergamon Press.Google Scholar
Lythgoe, J.N. (1979). The Ecology of Vision. Oxford: Clarendon Press.Google Scholar
Pomerat, C.M. (1933). Mating in Limulus polyphemus. Biological Bulletin 64, 243252.CrossRefGoogle Scholar
Powers, M.K. & Barlow, R.B. Jr. (1985). Behavioral correlates of circadian rhythms in the Limulus visual system. Biological Bulletin 169, 578591.CrossRefGoogle Scholar
Powers, M.K., Barlow, R.B. Jr. & Kass, L. (1991). Visual performance of horseshoe crabs day and night. Visual Neuroscience 7, 179189.CrossRefGoogle ScholarPubMed
Quick, R.F. (1974). A vector magnitude model of contrast detection. Kybernetik 16, 6567.CrossRefGoogle ScholarPubMed
Ratliff, F. (1974). Studies on Excitation and Inhibition in the Retina – A collection of papers from the Laboratory of H. Keffer Hartline. New York: The Rockefeller University Press.Google Scholar
Relkin, E.M. & Pelli, D.G. (1987). Probe tone thresholds in the auditory nerve measured by two-alternative forced-choice procedures. Journal of Acoustical Society of America 82, 16791691.CrossRefGoogle Scholar
Renninger, G.H. & Barlow, R.B. Jr. (1979). Lateral inhibition, excitation, and the circadian rhythm of the Limulus compound eye. Society for Neuroscience Abstracts 5, 804.Google Scholar
Renninger, G.H., Kaplan, E. & Barlow, R.B. Jr. (1984). Circadian changes in gain of Limulus lateral eye photoreceptors. Biological Bulletin 167, 501.Google Scholar
Renninger, G.H., Kass, L., Pelletier, J.L. & Schimmel, R. (1988). The eccentric cell of the Limulus lateral eye: Encoder of circadian changes in visual responses. Journal of Comparative Physiology A 163, 259270.CrossRefGoogle Scholar
Renninger, G.H., Schimmel, R. & Farrell, C.A. (1989). Octopamine modulates photoreceptor function in the Limulus lateral eye. Visual Neuroscience 3, 8394.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1965). Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Research 5, 583601.CrossRefGoogle ScholarPubMed
Rudloe, A.E. & Herrnkind, W.F. (1976). Orientation of Limulus polyphemus in the vicinity of breeding beaches. Marine Behavior and Physiology 4, 7589.CrossRefGoogle Scholar
Shuster, C.N. Jr. (1982). A pictorial review of the natural history and ecology of the horseshoe crab, Limulus polyphemus, with reference to other Limulidae. In Physiology and Biology of Horseshoe Crabs: Studies on Normal and Environmentally Stressed Animals, ed. Liss, A.R., New York: Liss, Inc.Google Scholar
Watson, A.B. (1979). Probability summation over time. Vision Research 19, 515522.CrossRefGoogle ScholarPubMed
Weibull, W. (1951). A statistical distribution function of wide applicability. Journal of Applied Mechanics 18, 292297.CrossRefGoogle Scholar
Weiner, W.W. & Chamberlain, S.C. (1993). The visual fields of American horseshoe crabs: Two different eye shapes in Limulus polyphemus. Visual Neuroscience 11, 333346.CrossRefGoogle Scholar