Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-23T05:06:33.775Z Has data issue: false hasContentIssue false

Morphological and behavioral limit of visual resolution in temperate (Hippocampus abdominalis) and tropical (Hippocampus taeniopterus) seahorses

Published online by Cambridge University Press:  23 June 2011

HIE RIN LEE
Affiliation:
Australian Research Council Centre of Excellence in Vision Science, Canberra, Australia Division of Biomedical Science and Biochemistry, Research School of Biology, the Australian National University, Canberra, Australia
KEELY M. BUMSTED O’BRIEN*
Affiliation:
Australian Research Council Centre of Excellence in Vision Science, Canberra, Australia Division of Biomedical Science and Biochemistry, Research School of Biology, the Australian National University, Canberra, Australia
*
*Address correspondence and reprint requests to: Dr Keely M. Bumsted O’Brien, Research School of Biology, The Australian National University, Canberra ACT 0200, Australia. E-mail: [email protected]

Abstract

Seahorses are visually guided feeders that prey upon small fast-moving crustaceans. Seahorse habitats range from clear tropical to turbid temperate waters. How are seahorse retinae specialized to mediate vision in these diverse environments? Most species of seahorse have a specialization in their retina associated with acute vision, the fovea. The purpose of this study was to characterize the fovea of temperate Hippocampus abdominalis and tropical H. taeniopterus seahorses and to investigate their theoretical and behavioral limits of visual resolution. Their foveae were identified and photoreceptor (PR) and ganglion cell (GC) densities determined throughout the retina and topographically mapped. The theoretical limit of visual resolution was calculated using formulas taking into account lens radius and either cone PR or GC densities. Visual resolution was determined behaviorally using reactive distance. Both species possess a rod-free convexiclivate fovea. PR and GC densities were highest along the foveal slope, with a density decrease within the foveal center. Outside the fovea, there was a gradual density decrease towards the periphery. The theoretically calculated visual resolution on the foveal slope was poorer for H. abdominalis (5.25 min of arc) compared with H. taeniopterus (4.63 min of arc) based on PR density. Using GC density, H. abdominalis (9.81 min of arc) had a lower resolution compared with H. taeniopterus (9.04 min of arc). Behaviorally, H. abdominalis had a resolution limit of 1090.64 min of arc, while H. taeniopterus was much smaller, 692.86 min of arc. Although both species possess a fovea and the distribution of PR and GC is similar, H. taeniopterus has higher PR and GC densities on the foveal slope and better theoretical and behaviorally measured visual resolution compared to H. abdominalis. These data indicate that seahorses have a well-developed acute visual system, and tropical seahorses have higher visual resolution compared to temperate seahorses.

Keywords

Type
Evolution and eye design
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barnstable, C.J. (1980). Monoclonal antibodies which recognize different cell types in the rat retina. Nature 286, 231235.CrossRefGoogle ScholarPubMed
Bergert, B. & Wainright, P. (1997). Morphology and kinetics of prey capture in the syngnathid fishes, Hippocampus erectus and Syngnathus floridae. Marine Biology 127, 563570.CrossRefGoogle Scholar
Boire, D., Dufour, J.S., Theoret, H. & Ptito, M. (2001). Quantitative analysis of the retinal ganglion cell layer in the ostrich, Struthio camelus. Brain, Behavior & Evolution 58, 343355.CrossRefGoogle ScholarPubMed
Boycott, B. & Wassle, H. (1999). Parallel processing in the mammalian retina: The Proctor Lecture. Investigative Ophthalmology & Visual Science 40, 13131327.Google ScholarPubMed
Browman, H.I., Gordon, W.C., Evans, B.I. & O’Brien, W.J. (1990). Correlation between histological and behavioral measures of visual acuity in a zooplanktivorous fish, the white crappie (Pomoxis annularis). Brain, Behavior & Evolution 35, 8597.CrossRefGoogle Scholar
Bumsted O’Brien, K.M., Cheng, H., Jiang, Y., Schulte, D., Swaroop, A. & Hendrickson, A.E. (2004). Expression of photoreceptor-specific nuclear receptor NR2E3 in rod photoreceptors of fetal human retina. Investigative Ophthalmology & Visual Science 45, 28072812.CrossRefGoogle ScholarPubMed
Campbell, F.W. & Green, D.G. (1965). Optical and retinal factors affecting visual resolution. The Journal of Physiology 181, 576593.CrossRefGoogle ScholarPubMed
Choo, C.K. & Liew, H.C. (2006). Morphological development and allometric growth patterns in the juvenile seahorse Hippocampus kuda Bleeker. Journal of Fish Biology 69, 426445.CrossRefGoogle Scholar
Collin, S.P. (1988). The retina of the shovel-nosed ray, Rhinobatos batillum (Rhinobatidae): Morphology and quantitative analysis of the ganglion, amacrine and bipolar cell populations. Experimental Biology 47, 195207.Google ScholarPubMed
Collin, S.P. & Collin, H.B. (1999). The foveal photoreceptor mosaic in the pipefish, Corythoichthyes paxtoni (Syngnathidae, Teleostei). Histology & Histopathology 14, 369382.Google ScholarPubMed
Collin, S.P. & Pettigrew, J.D. (1988). Retinal topography in reef teleosts. II. Some species with prominent horizontal streaks and high-density areae. Brain, Behavior & Evolution 31, 283295.CrossRefGoogle ScholarPubMed
Collin, S.P. & Pettigrew, J.D. (1989). Quantitative comparison of the limits on visual spatial resolution set by the ganglion cell layer in twelve species of reef teleosts. Brain, Behavior & Evolution 34, 184192.CrossRefGoogle ScholarPubMed
Curcio, C.A., Sloan, K.R., Kalina, R.E. & Hendrickson, A.E. (1990). Human photoreceptor topography. The Journal of Comparative Neurology 292, 497523.CrossRefGoogle ScholarPubMed
Curcio, C.A., Sloan, K.R. Jr, Packer, O., Hendrickson, A.E. & Kalina, R.E. (1987). Distribution of cones in human and monkey retina: Individual variability and radial asymmetry. Science 236, 579582.CrossRefGoogle ScholarPubMed
Dobson, V. & Teller, D.Y. (1978). Visual acuity in human infants: A review and comparison of behavioral and electrophysiological studies. Vision Research 18, 14691483.CrossRefGoogle ScholarPubMed
Easter, S.S. Jr (1992). Retinal growth in foveated teleosts: Nasotemporal asymmetry keeps the fovea in temporal retina. The Journal of Neuroscience 12, 23812392.CrossRefGoogle ScholarPubMed
Fekete, D.M. & Barnstable, C.J. (1983). The subcellular localization of rat photoreceptor-specific antigens. Journal of Neurocytology 12, 785803.CrossRefGoogle ScholarPubMed
Fernald, R.D. (1985). Growth of the teleost eye: Novel solutions to complex constraints. Environmental Biology of Fishes 13, 113123.CrossRefGoogle Scholar
Fernald, R.D. (1988). Aquatic adaptations in fish eyes. In Sensory Biology of Aquatic Animals, ed. Atema, J., Fay, R.R., Popper, A.N. & Tavolga, W.N., Berlin, Germany: Springer.Google Scholar
Fite, K.V. & Lister, B.C. (1981). Bifoveal vision in anolis lizards. Brain, Behavior & Evolution 19, 144154.CrossRefGoogle ScholarPubMed
Fite, K.V. & Rosenfield-Wessels, S. (1975). A comparative study of deep avian foveas. Brain, Behavior & Evolution 12, 97115.CrossRefGoogle ScholarPubMed
Foster, S.J. & Vincent, A.C.J. (2004). Life history and ecology of seahorses: Implications for conservation and management. Journal of Fish Biology 65, 161.CrossRefGoogle Scholar
Galifret, Y. (1968). Les diverses aires fonctionnelles de la retine du pigeon. Zeitschrift für Zellforschung und mikroskopische Anatomie 86, 535545.CrossRefGoogle Scholar
Garciá, M., Ruiz-Ederra, J., Hernández-Barbáchano, H. & Vecino, E. (2005). Topography of pig retinal ganglion cells. The Journal of Comparative Neurology 486, 361372.CrossRefGoogle Scholar
Harkness, L. & Bennet-Clark, H.C. (1978). The deep fovea as a focus indicator. Nature 272, 814816.CrossRefGoogle ScholarPubMed
Hemmi, J.M. & Grunert, U. (1999). Distribution of photoreceptor types in the retina of a marsupial, the tammar wallaby (Macropus eugenii). Visual Neuroscience 16, 291302.CrossRefGoogle ScholarPubMed
Hodos, W., Ghim, M.M., Potocki, A., Fields, J.N. & Storm, T. (2002). Contrast sensitivity in pigeons: A comparison of behavioral and pattern ERG methods. Documenta Ophthalmologica 104, 107118.CrossRefGoogle ScholarPubMed
James, P. & Heck, K. (1994). The effects of habitat complexity and light intensity on ambush predation within a simulated seagrass habitat. Journal of Experimental Marine Biology and Ecology 176, 187200.CrossRefGoogle Scholar
Job, S. & Bellwood, D. (1996). Visual acuity and feeding in larval Premnas biaculeatus. Journal of Fish Biology 48, 952963.Google Scholar
Kuiter, R.H. (2000). Seahorses Pipefishes and Their Relatives, A Comprehensive Guide to Syngnathiformes. The Marine Fish Families Series. Chorleywood, UK: TMC Publishing.Google Scholar
Kuiter, R.H. (2003). Seahorses, Pipefishes and Their Relatives: A Comprehensive Guide to Syngnathiformes. Chorleywood, UK: TMC Publishing.Google Scholar
Mack, A.F., Sussmann, C., Hirt, B. & Wagner, H.J. (2004). Displaced amacrine cells disappear from the ganglion cell layer in the central retina of adult fish during growth. Investigative Ophthalmology & Visual Science 45, 37493755.CrossRefGoogle ScholarPubMed
Matthiessen, L. (1880). Untersuchungen über den Aplanatismus und die Periscopie der Krystalllinsen in den Augen der Fische. Pflügers Archiv European Journal of Physiology 21, 287307.CrossRefGoogle Scholar
Merigan, W.H. & Maunsell, J.H.R. (1993). How parallel are the primate visual pathways? Annual Review of Neuroscience 16, 369402.CrossRefGoogle ScholarPubMed
Miller, T., Crowder, L. & Rice, J. (1993). Ontogenetic changes in behavioural and histological measures of visual acuity in three species of fish. Environmental Biology of Fishes 37, 18.CrossRefGoogle Scholar
Mosk, V., Thomas, N., Hart, N.S., Partridge, J.C., Beazley, L.D. & Shand, J. (2007). Spectral sensitivities of the seahorses Hippocampus subelongatus and Hippocampus barbouri and the pipefish Stigmatopora argus. Visual Neuroscience 24, 345354.CrossRefGoogle ScholarPubMed
Neave, D.A. (1984). The development of visual acuity in larval plaice (Pleuronectes platessa L.) and turbot (Scophthalmusmaximus L.). Journal of Experimental Marine Biology and Ecology 78, 167175.CrossRefGoogle Scholar
Packer, O., Hendrickson, A.E. & Curcio, C.A. (1989). Photoreceptor topography of the retina in the adult pigtail macaque (Macaca nemestrina). The Journal of Comparative Neurology 288, 165183.CrossRefGoogle ScholarPubMed
Pankhurst, P.M., Pankhurst, N.W. & Montgomery, J.C. (1993). Comparison of behavioural and morphological measures of visual acuity during ontogeny in a teleost fish, Forsterygion varium, tripterygiidae (Forster, 1801). Brain, Behavior & Evolution 42, 178188.CrossRefGoogle Scholar
Partridge, J.C. (1990). The colour sensitivity and vision of fishes. In Light and Life in the Sea, ed. Herring, P.J., Campbell, A.K. & Whitfield, M., Cambridge, UK: Cambridge University Press.Google Scholar
Provis, J.M. (1979). The distribution and size of ganglion cells in the retina of the pigmented rabbit: A quantitative analysis. The Journal of Comparative Neurology 185, 121137.CrossRefGoogle ScholarPubMed
Pumphrey, R.J. (1948). The theory of the fovea. The Journal of Experimental Biology 25, 299312.CrossRefGoogle Scholar
Querubin, A., Lee, H., Provis, J. & Bumsted O’Brien, K. (2009). Photoreceptor and ganglion cell topographies correlate with information convergence and high acuity regions in the adult pigeon (Columba livia) retina. The Journal of Comparative Neurology 517, 711722.CrossRefGoogle ScholarPubMed
Salinas-Navarro, M., Mayor-Torroglosa, S., Jiménez-López, M., Avilés-Trigueros, M., Holmes, T.M., Lund, R.D., Villegas-Pérez, M.P. & Vidal-Sanz, M. (2009). A computerized analysis of the entire retinal ganglion cell population and its spatial distribution in adult rats. Vision Research 49, 115126.CrossRefGoogle ScholarPubMed
Schwassmann, H.O. (1968). Visual projection upon the optic tectum in foveate marine teleosts. Vision Research 8, 13371348, IN1-IN2.CrossRefGoogle ScholarPubMed
Slonaker, J.R. (1897). A comparative study of the area of acute vision in vertebrates. Journal of Morphology 13, 445494.CrossRefGoogle Scholar
Stone, J. (1965). A quantitative analysis of the distribution of ganglion cells in the cat’s retina. The Journal of Comparative Neurology 124, 337352.CrossRefGoogle ScholarPubMed
Walls, G.L. (1942). The Vertebrate Eye and Its Adaptive Radiation. Bloomfield Hills, MI: Cranbrook Institute of Science.Google Scholar
Wanzenbock, J. & Schiemer, F. (1989). Prey detection in cyprinids during early development. Canadian Journal of Fisheries and Aquatic Sciences 46, 9951001.CrossRefGoogle Scholar