Abstract
The retinal ganglion cell distribution, which is known to reflect fish feeding behavior, was investigated in juvenile Pacific bluefin tuna Thunnus orientalis. During the course of examination, regularly arrayed cells with a distinctive larger soma, which may be regarded as motion-sensitive cells, were found. The topographical distribution of ordinary-sized ganglion cells, which is usually utilized to estimate fish visual axis and/or visual field characteristics, showed that the highest-density area, termed the area centralis, was localized in the ventral-temporal retina. The retinal topography of ordinary-sized ganglion cells seems to reflect the bluefin tuna’s foraging behavior; while cruising, cells in the area centralis may signal potential prey, such as small schooling pelagic fishes or squids, that are present in the upward-forward direction. Judging from morphological characteristics, the large ganglion cells localized in the small temporal retinal area seem to be equivalent to physiologically categorized off-center Y-cells of cat, which are stimulated by a transient dark spot in a bright visual field. It was inferred that presumed large off-center cells in the temporal retina detect movements of agile prey animals escaping from bluefin tuna as a silhouette against environmental light.
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References
Balanov AA, Radchenko VI (1998) New data on the feeding and consumption behaviors of Anotopterus pharao. J Ichthyol 38:447–453
Browman HI, Gordon WC, Evans BI et al (1990) Correlation between histological and behavioral measures of visual acuity in a zooplanktivorous fish, the white crappie (Pomoxis annularis). Brain Behav Evol 35:85–97
Calderone JB, Reese BE, Jacobs GH (2003) Topography of photoreceptors and retinal ganglion cells in the spotted hyena (Crocuta crocuta). Brain Behav Evol 62:182–192
Collin SP, Pettigrew JD (1988a) Retinal topography in reef teleosts. I. Some species with well-developed area but poorly-developed streaks. Brain Behav Evol 31:269–282
Collin SP, Pettigrew JD (1988b) Retinal topography in reef teleosts. II. Some species with prominent horizontal streaks and high-density area. Brain Behav Evol 31:283–295
Collin SP, Hoskins RV, Partridge JC (1998) Seven retinal specializations in the tubular eye of the deep-sea pearleye, Scopelarchus michaelsarsi: a case study in visual optimization. Brain Behav Evol 51:291–314
Dragovich A (1969) Review of studies of tuna food in the Atlantic Ocean. US Fish Wildl Servo Spec Sci Rep Fish 593:1–21
Famiglietti EV, Kolb H (1976) Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194:193–195
Famiglietti EV, Kaneko A, Tachibana M (1977) Neuronal architecture of ON and OFF pathways to ganglion cells in carp retina. Science 198:1267–1268
Fritsches KA, Marshall NJ, Warrant EJ (2003) Retinal specializations in the blue marlin: eyes designed for sensitivity to low light levels. Mar Fresh Res 54:333–341
Fritsches KA, Brill RW, Warrant EJ (2005) Warm eyes provide superior vision in swordfish. Curr Biol 15:55–58
Fukuda Y, Stone J (1974) Retinal distribution and central projections of Y-, X-, and W-cells of the cat’s retina. J Neurophysiol 37:749–772
Fukuda Y, Hsiao CF, Watanabe M et al (1984) Morphological correlates of physiologically identified Y-, X- and W-cells in cat retina. J Neurophysiol 52:999–1013
Hayes BP, Brooke M (1990) Retinal ganglion cell distribution and behaviour in procellariiform seabirds. Vision Res 30:1277–1289
HSiao SC, Tester AL (1955) Reaction of tuna to stimuli, 1952–53. Part II: response of tuna to visual and visual-chemical stimuli. US Fish and Wildlife Service. Spec Sci Rep Fish 130:63–76
Ito H, Murakami T (1984) Retinal ganglion cells in two teleost species, Sebastiscus marmoratus and Navodon modestus. J Comp Neurol 229:80–96
Kawamura G, Nishimura W, Ueda S et al (1981) Vision in tunas and marlins. Mem Kagoshima Univ Res Cent S Pac 1:3–47
Kawamura G, Masuma S, Tezuka N et al (2003) Morphogenesis of sense organs in the bluefin tuna Thunnus orientalis. The Big Fish Bang. Institute of Marine Research, Bergen, pp 123–135
Kino M, Miyazaki T, Iwami T et al (2009) Retinal topography of ganglion cells in immature ocean sunfish, Mola mola. Environ Biol Fish 85:33–38
Kitagawa T, Nakata H, Kimura S et al (2001) Thermoconservation mechanism inferred from peritoneal cavity temperature recorded in free swimming Pacific bluefin tuna (Thunnus thynnus orientalis). Mar Ecol Prog Ser 220:253–263
Kitagawa T, Kimura S, Nakata H et al (2004) Diving behavior of immature, feeding Pacific bluefin tuna (Thunnus thynnus orientalis) in relation to season and area: the East China Sea and the Kuroshio–Oyashio transition region. Fish Oceanogr 13:161–180
Makino A, Miyazaki T (2010) Topographical distribution of visual cell nuclei in the retina in relation to the habitat of five decapodiformes species. J Mollusc Stud 76:180–185
Mass AM (2004) A High-resolution area in the retinal ganglion cell layer of the Steller's Sea lion (Eumetopias jubatus): a topographic study. Dokl Biol Sci 396:187–190
Mass AM, Supin AY (1997) Ocular anatomy, retinal ganglion cell distribution, and visual resolution in the gray whale. Eschrichtius gibbosus. Aquat Mamm 23:17–28
Mass AM, Supin AY (2005) Ganglion cell topography and retinal resolution of the Steller sea lion (Eumetobias jubatus). Aquat Mamm 31:393–402
Masuma S, Kawamura G, Tezuka N et al (2001) Retinomotor responses of juvenile bluefin tuna Thunnus thynnus. Fish Sci 67:228–231
Masuma S, Tezuka N, Obana H et al (2003) Spawning ecology of captive bluefinn tuna Thunnus thynnus orientalis inferred by mitochondrial DNA analysis. Bull Fish Res Agency 6:9–14 in Japanese, with English abstract
Matsumoto T, Okada T, Sawada Y et al (2012) Visual spectral sensitivity of photopic juvenile Pacific bluefin tuna (Thunnus orientalis). Fish Physiol Biochem 38:911–917
Matsuura R, Sawada Y, Ishibashi Y (2010) Development of visual cells in the Pacific bluefin tuna Thunnus orientalis. Fish Physiol Biochem 36:391–402
Miyashita S, Sawada Y, Hattori N et al (2000) Mortality of northern bluefin tuna Thunnus thynnus due to trauma caused by collision during growout culture. World Aquac 31:632–639
Miyazaki T, Kohbara J, Takii K et al (2008) Three cone opsin genes and cone cell arrangement in retina of juvenile Pacific bluefin tuna Thunnus orientalis. Fish Sci 74:314–321
Nakamura EL (1968) Visual acuity of yellowfin tuna Thunnus albacares. FAO Fish Rep 62(3):463–468
Nelson R, Famiglietti EV, Kolb H (1978) Intracellular staining reveals different levels of stratification for on- and off-center ganglion cells in the cat retina. J Neurophys 41:472–483
Ohshimo S (1998) Distribution and stomach contents of Maurolicus muelleri in the Sea of Japan (East Sea). J Korean Soc Fish Res 1:168–175
Pankhurst NW (1989) The relationship of ocular morphology to feeding modes and activity periods in shallow marine teleosts from New Zealand. Environ Biol Fish 26:201–211
Peichel L, Wässle H (1981) Morphological identification of on- and off-centre brisk transient (Y) cells in the cat retina. Proc R Soc Lond B 212:139–153
Peichl L, Buhl EH, Boycott BB (1987) Alpha ganglion cells in the rabbit retina. J Comp Neurol 263:25–41
Saito H (1983) Morphology of physiologically identified X-, Y- and W-type retinal ganglion cells of the cat. J Comp Neurol 221:279–288
Saito H, Shimahara T, Fukada Y (1970) Four types of responses to light and dark spot stimuli in the cat optic nerve. Tohoku J Exp Med 102:127–133
Sawada Y, Okada T, Miyashita S et al (2005) Completion of the Pacific bluefin Tuna, Thunnus orientalis, life cycle under aquaculture conditions. Aquac Res 36:413–421
Sinopoli M, Pipitone C, Campagnuolo S et al (2004) Diet of young-of-the-year bluefin tuna, Thunnus thynnus (Linnaeus, 1758), in the southern Tyrrhenian (Mediterranean) Sea. J Appl Ichthyol 20:310–313
Tamura T, Wisbey SJ (1963) The visual sense of pelagic fishes especially the visual axis and accommodation. Bull Mar Sci Gulf Caribb 13:433–448
Tanabe T, Niu K (1998) Sampling juvenile skipjack tuna, Katsuwonus pelamis, and other tunas, Thunnus spp., using midwater trawls in the tropical western Pacific. Fish Bull 96:641–646
Torisawa S, Takagi T, Ishibashi Y et al (2007) Changes in the retinal cone density distribution and the retinal resolution during growth of juvenile Pacific bluefin tuna Thunnus orientalis. Fish Sci 73:1202–1204
Uemura M, Somiya H, Moku M et al (2000) Temporal and mosaic distribution of large ganglion cells in the retina of a daggertooth aulopiform deep-sea fish (Anotopterus pharao). Phil Trans R Soc Lond B 355:1161–1166
Acknowledgments
The author gratefully acknowledges the staff of the Fisheries Laboratory, Kinki University, for supplying experimental specimens. Two anonymous referees kindly provided valuable comments and constructive suggestions on earlier drafts. This study was supported by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (no. 23570113) and the Kakushin Educational Foundation from Kakuda Pearl Co. Ltd.
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Miyazaki, T. Retinal ganglion cell topography in juvenile Pacific bluefin tuna Thunnus orientalis (Temminck and Schlegel). Fish Physiol Biochem 40, 23–32 (2014). https://doi.org/10.1007/s10695-013-9820-8
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DOI: https://doi.org/10.1007/s10695-013-9820-8