Translator Disclaimer
1 November 2002 Retinal Topography of Ganglion Cells and Putative UV-Sensitive Cones in Two Antarctic Fishes: Pagothenia borchgrevinki and Trematomus bernacchii (Nototheniidae)
Author Affiliations +
Abstract

Accessory corner cones (ACC) have recently been suggested to be UV-sensitive photoreceptor cells. With a view toward explaining prey detection, we examined the topography of retinal ganglion cells and ACCs in two Antarctic nototheniids occupying different ecological niches: the cryopelagic Pagothenia borchgrevinki and the benthic Trematomus bernacchii. Isodensity maps of retinal ganglion cells showed that the main visual axis, coincident with the feeding vector, was in a forward direction in both species. Visual acuity was determined as 3.64 and 4.77 cycles/degree for the respective species. In P. borchgrevinki the highest density of ACCs was associated with the eye's main visual axis. This suggested that this species uses UV-vision during forward-swims and probably in encounters with prey. On the other hand, T. bernacchii possessed two horizontal band-shaped high-density areas of ACCs, which stretched from temporal to nasal and ventral to peripheral retinal regions. Therefore, this species appears to use UV-vision to watch prey across the entire circumference of the lateral area and in the water column above its head.

INTRODUCTION

The presence of UV-absorbing visual pigment in the single cone at the corner of the retinal square cone mosaic, named accessory corner cone (ACC), has been reported in many freshwater fishes and euryhaline fishes by using microspectrophotometrical and/or molecular analyses (Avery et al., 1983; Hárosi and Hashimoto, 1983; Whitmore and Bowmaker, 1989; Archer and Lythgoe, 1990; Bowmaker et al., 1991; Hawryshyn and Hárosi, 1991; Raymond et al., 1993; Hisatomi et al., 1996, 1997). Furthermore, in juveniles of some salmonids species (Salmo trutta, Salmo gairdneri (=Oncorhynchus mykiss), Salmo salar, Oncorhynchus nerka) and yellow perch Perca flavescens, the loss of UV-photosensitivity associated with the almost complete disappearance of ACCs from the retinal cone mosaic has been confirmed (Bowmaker and Kunz, 1987; Hawryshyn et al., 1989; Loew and Wahl, 1991; Kunz et al., 1994; Novales-Flamarique, 2000).

Recently, we reported the presence of ACCs histologically from the eyes of adults of seven Antarctic nototheniid species as follows: Trematomus bernacchii, Trematomus newnesi, Trematomus hansoni, Trematomus pennellii, Trematomus scotti, Pagothenia borchgrevinki, Lepidonotothen squamifrons (=kempi) (Miyazaki et al., 2001). Although several specific visual tasks for UV-vision have been proposed (foraging, navigation, and/or communication) and we have very few direct observations on visual feeding in Antarctic fishes, we suggested that Antarctic fishes could increase their feeding efficiency and stock energy by making use of UV-vision during the summer month (Miyazaki et al., 2001).

Topographical analyses of retinal ganglion cells as well as cone photoreceptors can provide us with valuable information on the visual capabilities of fishes. In adult teleosts, the position of the “area centralis (AC)” is related to both habitat and main visual vector of feeding behaviour (Collin and Pettigrew, 1988b, c; Williamson and Keast, 1988; Browman et al., 1990). Furthermore, the distribution of cone photoreceptors determines how the spectral sensitivity of a fish eye changes across its visual field, for different kinds of cones may contain visual pigments with different spectral absorption characteristics (McFarland and Munz, 1975; Beaudet et al., 1997).

In several Antarctic fish species, retinal organizations have been described for specific regions and estimates on visual resolution or photosensitivity were given (Meyer-Rochow and Klyne, 1982; Eastman, 1988; Pankhurst and Montgomery, 1989, 1990; Fanta et al., 1994, Meyer-Rochow et al., 1999). However, the topography of the ganglion cells or cone cells of the whole retina, and in particular the position of the ACs, is still poorly known. Our primary objective was to histologically examine the prey detection system in nototheniids. We also hoped to establish whether the ACCs, as the putative UV-sensitive cones, could assist the fish in prey detection and uptake. The UV-wavelength absorption of ACC's visual pigment has been shown by the previous studies mentioned above, although we have not verified about Antarctic fish yet. In this paper, we therefore examined the retinal topographies of ganglion cells and ACCs for entire retinas of two nototheniids with different habits, namely Pagothenia borchgrevinki and Trematomus bernacchii. We also determined the fish eyes' UV-visual fields. Finally, visual acuity and optical axes were estimated on the basis of retinal ganglion cell distributions, since retinal ganglion cells are providing the link between eyes and behavioural output via the optic nerve.

MATERIALS AND METHODS

Fish

P. borchgrevinki and T. bernacchii were caught by line-fishing from a depth of ca. 30 m in Lützow-Holm Bay near Syowa Station (69° S, 39° E). Total lengths of the P. borchgrevinki and T. bernacchii specimens used were 210 mm and 215 mm, respectively. According to Collin and Pettigrew (1988a), there is no remarkable difference in the topography of cells among specimens of the almost same size of the same species. Based on their observation results, we used a single specimen for each species. Following capture, the fish were anaesthetized with MS222 and then immediately fixed in 10% formalin. Thereafter the eyes were enucleated and cornea, iris, lens, and vitreous humor were removed. The remaining retinae were prepared as follows.

Examination of ganglion cells

The left retinae were radically incised and flatly mounted, and then whole-mount preparations were made following the protocol of Ito and Murakami (1984). The preparations were glued onto slides with the ganglion cell layer facing upward, and stained with crecyl violet. Ganglion cells numbers per 0.13×0.13 mm of each fish retina, about 20 mm in diameter in both fish, were counted at 2mm intervals, under a light microscope, using a calibrated eyepiece. In P. borchgrevinki and T. bernacchii, 127 and 98 sampling points were used. Values for the ganglion cells were converted into numbers of cells per mm2, and then isodensity counter maps of ganglion cells were constructed. The retinal resolving powers were calculated according to the protocol of Collin and Pettigrew (1989), the values thus obtained representing upper limits based on the following equations:

The distance from lens center to retinal focus (posterior nodal distance, PND) was calculated from lens radius (r; mm) and Matthiessen's ratio (2.55):

PND = 2.55r.
The angle (α), subtending 1mm on the retina was calculated by,
i0289-0003-19-11-1223-e01.gif
When the density of the ganglion cells is D (cells/mm2), the linear density is
i0289-0003-19-11-1223-e02.gif
Spatial resolution can be calculated by obtaining the number of cells subtended by one degree of visual arc, i.e.,
i0289-0003-19-11-1223-e03.gif
Since at least two ganglion cells are needed to distinguish the light and dark boundaries from one cycle of a grating of the highest resolvable frequency, visual acuity is given by
cycles per degree = 1/2 cells per degree

Examination of ACCs

Right retina of the P. borchgrevinki and T. bernacchii was divided into 24 and 30 topographical locations, respectively, and thus the position of each piece in the original retina was determined accurately. The pieces were dehydrated in alcohol and embedded in paraffin. Tangential sections were cut at 7 μm thickness and stained with haematoxylin and eosin. Cone photoreceptor layers were observed under the light microscope, and numbers of accessory corner cone cells per 0.1×0.1 mm were counted for respective retinal pieces.

RESULTS

Distribution of ganglion cells

All ganglion cells lying within the retinal ganglion cell layer in each fish species were counted. The averages of cell density, estimated from the counts of ganglion cells and counted number of points, were approx. 1.5×103 cells/mm2 in P. borchgrevinki and 2.5×103 cells/mm2 in T. bernacchii (Table 1). The calculated cell densities were upper estimates, which may include displaced amacrine cells.

Table 1

Summery of ganglion cell counts and calculations of visual acuity in two nototheniids.

i0289-0003-19-11-1223-t01.gif

Ganglion cells were not uniformly distributed in the retinae of either species. Isodensity maps of P. borchgrevinki and T. bernacchii resembled each other in that in both species, the region of highest cell density, termed area centralis (AC), was located in the temporal retina (Figs. 1a and 1b). The position of the AC indicates that the visual axis was in a forward direction. In both species, however, a weak horizontal visual streak was also observed a little above the optic papilla (see in Figs. 1a and 1b).

Fig. 1

Isodensity counter maps of the distribution of Nissle-stained neurons (retinal ganglion plus displaced amacrine cells) located within the ganglion cell layer in the left eye of P. borchgrevinki (a) and T. bernacchii (b). All cell densities ×103 per mm2. T, temporal; V, ventral; D, dorsal; N, nasal. The arrows indicate the position of optic papilla.

i0289-0003-19-11-1223-f01.gif

Ganglion cell peak densities were 3313 and 6804 cells/mm2 in P. borchgrevinki and T. bernacchii, respectively, and the corresponding lens diameters were 5.65 mm and 5.15 mm. The PNDs, α s, and the numbers of ganglion cells sub-tended by one degree of visual arc in the respective species were calculated as shown in Table 1. Consequently, the upper limit of the theoretically derived visual acuity, based on ganglion cell counts, can be given as 3.64 and 4.77 cycles/degree in P. borchgrevinki and T. bernacchii, respectively.

Distribution of ACCs

Single and double cones were alternately and regularly aligned in the photoreceptor layer, and formed a square mosaic pattern in both species (Figs. 2a and 2b). The ACCs, which were located at the corners of the double cones, could be distinguished from the central single cones by the direction of the axes of the double cones (Figs. 2c and 2d). In both species, the ACCs were present in the entire retina, but the density varied across the retina. Figs.3a and 3b illustrate ACC density distributions in the retinae of P. borchgrevinki and T. bernacchii, respectively. The highest density of the ACCs was in the temporal retina of both species, which corresponded to the AC. Peak densities of the ACCs were 32 and 29 cells par 0.01mm2 in P. borchgrevinki and T. bernacchii, respectively.

Fig. 2

Photomicrographs of tangential sections through ellipsoid region of cone photoreceptors in the temporal retina of P. borchgrevinki (a) and T. bernacchii (b). (c) and (d) are tracings of a cone square mosaic on photograph (a) and (b), respectively. ACC, accessory corner cone; CC, central single cone; DC, double cone. The phenotype of the ACC and CC has been identified to be UV- and blue-visual pigment, and that of one of the DC is green- while another of the DC is red-visual pigment (Raymond et al., 1993; Hisatomi et al., 1996, 1997). Scale bar=20 μm.

i0289-0003-19-11-1223-f02.gif

Fig. 3

Maps showing the distribution of ACC densities in the right retina of P. borchgrevinki (a) and T. bernacchii (b). All cell densities per 0.01mm2. Tri. indicates presence of triple cones. (c) Photograph of triple cones in a section of T. bernacchii retina. Scale bar=20 μm. T, temporal; V, ventral; D, dorsal; N, nasal.

i0289-0003-19-11-1223-f03.gif

In P. borchgrevinki, ACC density was high near the optic papilla of the temporal retina. On the other hand, in T. bernacchii, the highest density was seen in the region of the horizontal streak just dorsal of the mid-retina. An additional, high density area was seen in the peripheral part of the ventral retina.

Triple cones were observed near the optic papilla in T. bernacchii (Fig. 3c), but not in P. borchgrevinki.

DISCUSSION

Both P. borchgrevinki and T. bernacchii belong to the Nototheniidae of the suborder Notothenioidei. However, the former species is cryopelagic, whereas the latter is benthic. Furthermore, the two differ in body shape and position of the eye. The body in P. borchgrevinki is laterally compressed and the eyes are positioned laterally. This body shape is commonly associated with fast-swimming fishes and, indeed, this species is often seen as small schools swimming just beneath the sea-ice (Meyer-Rochow, 1982; Meyer-Rochow and Klyne, 1982; Eastman and DeVries, 1985; Foster et al., 1987; Gon and Heemstra, 1990; Pankhurst and Montgomery, 1990). On the other hand, the head of T. bernacchii is broader, and the eye is situated higher on the head and directed anterolaterally. This body shape is typical of benthic fishes, such as gobies and sculpins.

In the present investigation, the main visual axis, thought to provide a clue for the high resolving power of the AC (Shand et al., 2000), was determined to be forward-looking in both species, which is in agreement with the AC's location in the temporal retina. Therefore, the best vision in both species to detect prey items must be considered to lie in front of the fish. Earlier workers have also suggested that T. bernacchii has a forward-directed feeding vector, since it has a large anterior aphakic space. As for P. borchgrevinki, it lacks the anterior aphakic space and may therefore posses an extended visual field (Pankhurst and Montgomery, 1989; Macdonald and Montgomery, 1991; Eastman, 1993).

The binocular visual field, based on eye position and body morphology in T. bernacchii, is broader than that of P. borchgrevinki but less far-reaching. On the contrary, P. borchgrevinki appears to be able to detect prey further away from the body than T. bernacchii (Fig. 4). Consequently, it is likely that P. borchgrevinki can focus earlier on prey during cruising, while T. bernacchii waits and watches prey over a wide range before it initiates an attack. A similar difference in visual fields has been noted between two other nototheniids, namely Gobionotothen gibberifrons and Trematomus newnesi. The latter two species share the same environmental depth of 40–80 m bottom, but they differ in their feeding-behavioural strategies (Fanta et al., 1994). The expansion of fish visual field should also be discussed based on the eye movement. Regarding eye movement of nototheniids, the maximum eye rotation has been reported as about 15 and 20 degree for P. borchgrevinki and Dissoticus mawsonii, respectively (Montgomery and Macdonald, 1985). Nevertheless, although we don't know how nototheniids use monocular and binocular vision for their visual interest, the eye movement might allow fish to observe its surroundings without moving head or body (Fritsches and Marshall, 2002). Both of P. borchgrevinki and T. bernacchii may be able to aim prey with the expansion of visual covering range by eye movement.

Fig. 4

Schematic diagrams of the binocular visual fields based on eye position, body orientation and position of AC in the retina of P. borchgrevinki (a) and T. bernacchii (b).

i0289-0003-19-11-1223-f04.gif

Regarding visual acuity, there was no remarkable difference in the present two species. The correlation between the visual acuity level of fishes and their swimming types has not been clearly shown in Tamura (1957). Retinal resolving power in cycles per degree can be converted to that of minutes of arc (Murayama and Somiya, 1998), e.g., according to the equation

i0289-0003-19-11-1223-e04.gif
If that is done, values of 8.2′ and 6.3′ result for P. borchgrevinki and T. bernacchii, respectively. These values are almost the same as those in other marine teleosts, which were derived from maximum cone densities (Pagrus major: 6.4′ for a fish of 200 mm in body length; Lateolabrax japonicus: 8.5′ for an 180 mm long fish; Sebastiscus marmoratus: 6.7′ also for an 180 mm long fish, Tamura, 1957).

Meyer-Rochow and Klyne (1982) have counted cone and ganglion cells in both species (P. borchgrevinki: approx. 8300 cells/mm2 for a fish of approx. 200 mm total body length; T. bernacchii: approx. 4200 cells/mm2 for a fish of approx. 240 mm total body length: converted from original data). Furthermore, there have been studies on the theoretical visual acuity calculated from retinal cone densities for both species (P. borchgrevinki: 25–50′ for fish of 63–220 mm total body length: Pankhurst and Montgomery, 1990; T. bernacchii: 10′ in the temporal retina for a fish of 192 mm total body length; Miyazaki, unpublished data). Some differences between earlier values and our present values might have been caused by differences in fish size or retinal region analyzed for each examination. Nevertheless, a close agreement between values based on cone cell and ganglion cell estimates, as well as behavioural tests clearly exists (Collin and Pettigrew, 1989; Arrese et al., 2000).

The maximum distance (L; cm), at which a fish could recognize a prey item (φ; cm), can be estimated from the fish's visual acuity according to

i0289-0003-19-11-1223-e05.gif
provided optical properties in the sea (turbidity and light intensity) are neglected (Miyazaki and Nakamura, 1990; Miyazaki et al., 2000). On that basis, for example, the recognizable distance for a prey of 3 cm diameter would be about 12.6 m in P. borchgrevinki and 16.4 m in T. bernacchii.

While these figures do not seem to vary too greatly between the two species, the distribution of the ACCs in the retina, on the other hand, was quite dissimilar. In P. borchgrevinki, the region in which the density of the ACCs was highest coincided with the position of the AC. Therefore, UV-vision in P. borchgrevinki must be assumed to be most effective in a forward direction, and consequently P. borchgrevinki ought to principally recognize prey in the swimming direction from a larger distance than T. bernacchii (Cronin et al., 1994; Losey et al., 1999). As for T. bernacchii, the high-density area was the horizontal streak, which stretched from the temporal to the nasal retina. An additional area of high density was developed in the peripheral parts of the ventral retina. UV-vision in T. bernacchii, therefore, appears to be effective not only along the main visual axis of the forward-movement but also across a vast lateral area and into the upper water column itself. This extensive field could improve prey discovery, allowing T. bernacchii to remain relatively motionless in anticipation of prey. All of these conclusions are supported by the eye's morphology. We believe P. borchgrevinki detects pelagic prey, e.g. copepods (Hoshiai and Tanimura, 1981; Hoshiai et al., 1989) as silhouettes against downwelling light, whereas T. bernacchii relies mainly on laterally incident light to feed, since T. bernacchii in contrast to P. borchgrevinki displays an obvious corneal iridescence (Macdonald and Montgomery, 1991; Eastman, 1993), which screens out bright downwelling light.

The benefit for fish using UV-vision for feeding, lies in enhancing the contrast of prey against a UV-background and it is thought that UV-sensitivity is widespread in zooplanktivorous fishes (e.g., juvenile rainbow trout Oncorhynchus mykiss, pumpkinseed sunfish Lepomis gibbosus: Browman et al., 1994; juvenile yellow perch Perca flavescens: Loew and Wahl, 1991; Loew et al., 1993; pomacentrid fish Dascyllus trimaculatus, Pomacentrus coelestis, Chromis punctipinnis: McFarland and Loew, 1994). In Antarctic nototheniids, UV-vision may represent one strategy to increase foraging efficiency during the Antarctic summer, when light conditions are appropriate for visual feeding and a visual threshold of 2×109 photons cm−2 s−1 is reached (Morita et al., 1997). However, other and additional means of detecting predators and prey are entirely possible, especially if it is remembered that individuals with aberrant eyes can, apparently, reach full adulthood (Meyer-Rochow, 1990). To (a) determine the extent that nototheniids can make use of UV-light and (b) understand the role of triple cones, present in the retina of T. bernacchii (but not P. borchgrevinki), are thus our next goals.

Acknowledgments

We are thankful to members of 34th and 35th Japanese Antarctic Research Expedition for their kind support during respective research in Antarctica. This study was partly supported by the research fund of NIRS Brain Research Project.

REFERENCES

1.

S. N. Archer and J. N. Lythgoe . 1990. The visual pigment basis for cone polymorphism in the guppy, Poeciliaculata. Vision Res 30:225–233. Google Scholar

2.

C. Arrese, M. Archer, P. Runham, S. A. Dunlop, and L. D. Beazley . 2000. Visual system in a diurnal marsupial, the numbat (Myrmecobius fasciatus): retinal organization, visual acuity and visual fields. Brain Behav Evol 55:163–175. Google Scholar

3.

J. A. Avery, J. K. Bowmaker, M. B. A. Djamgoz, and J. E. G. Downing . 1983. Ultra-violet sensitive receptors in a freshwater fish. J Physiol 334:23–24. Google Scholar

4.

L. Beaudet, I. Novales-Flamarique, and C. W. Hawryshyn . 1997. Cone photoreceptor topography in the retina of sexually mature Pacific salmonid fishes. J Comp Neurol 383:49–59. Google Scholar

5.

J. K. Bowmaker and Y. W. Kunz . 1987. Ultraviolet receptors, tetrachromatic colour vision and retinal mosaics in the brown trout (Salmo trutta): age-dependent changes. Vision Res 27:2101–2108. Google Scholar

6.

J. K. Bowmaker, A. Thorpe, and R. H. Douglas . 1991. Ultraviolet-sensitive cones in the goldfish. Vision Res 31:349–352. Google Scholar

7.

H. I. Browman, W. C. Gordon, B. I. Evans, and W. J. O'Brien . 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. Google Scholar

8.

H. I. Browman, I. Novales-Flamarique, and C. W. Hawryshyn . 1994. Ultraviolet photoreception contributes to prey search behaviour in two species of zooplanktivorous fishes. J Exp Biol 186:187–198. Google Scholar

9.

S. P. Collin and J. D. Pettigrew . 1988a. Retinal ganglion cell topography in teleosts: a comparison between nissl-stained material and retrograde labelling from the optic nerve. J Comp Neurol 276:412–422. Google Scholar

10.

S. P. Collin and J. D. Pettigrew . 1988b. Retinal topography in reef teleosts. I. Some species with well-developed areae but poorly-developed streaks. Brain Behav Evol 31:269–282. Google Scholar

11.

S. P. Collin and J. D. Pettigrew . 1988c. Retinal topography in reef teleosts. II. Some species with prominent horizontal streaks and high-density areae. Brain Behav Evol 31:283–295. Google Scholar

12.

S. P. Collin and J. D. Pettigrew . 1989. Quantitative comparison of the limits on visual spatial resolution set by the ganglion cell layer in twelve species of reef teleosts. Brain Behav Evol 34:184–192. Google Scholar

13.

T. W. Cronin, N. J. Marshall, C. A. Quinn, and C. A. King . 1994. Ultraviolet photoreception in mantis shrimp. Vision Res 34:1443–1452. Google Scholar

14.

J. T. Eastman and A. L. DeVries . 1985. Adaptations for cryopelagic life in the Antarctic notothenioid fish Pagothenia borchgrevinki. Polar Biol 4:45–52. Google Scholar

15.

J. T. Eastman 1988. Ocular morphology in Antarctic notothenioid fishes. J Morphol 196:283–306. Google Scholar

16.

J. T. Eastman 1993. Antarctic Fish Biology, Evolution in a unique environment. Academic Press Inc. San Diego. Google Scholar

17.

E. Fanta, A. A. Meyer, S. R. Grötzner, and M. F. Luvizotto . 1994. Comparative study on feeding strategy and activity patterns of two Antarctic fish: Trematomus newnesi Boulenger, 1902 and Gobionotothen gibberifrons (Lönnberg, 1905) (Pisces, Nototheniidae) under different light conditions. Nankyoku Shiryô (Antarctic Record) 38:13–29. Google Scholar

18.

B. A. Foster, J. M. Cargill, and J. C. Montgomery . 1987. Planktivory in Pagothenia borchgrevinki (Pisces: Nototheniidae) in McMurdo Sound, Antarctica. Polar Biol 8:49–54. Google Scholar

19.

K. A. Fritsches and N. J. Marshall . 2002. Independent and conjugate eye movements during optokinesis in teleost fish. J Exp Biol 205:1241–1252. Google Scholar

20.

O. Gon and P. C. Heemstra . 1990. Fishes of the southern ocean. JLB Smith Institute of Ichthyology. Grahamstown. Google Scholar

21.

F. I. Hárosi and Y. Hashimoto . 1983. Ultraviolet visual pigment in a vertebrate: a tetrachromatic cone system in the dace. Science 222:1021–1023. Google Scholar

22.

C. W. Hawryshyn, M. G. Arnold, D. J. Chaisson, and P. C. Martin . 1989. The ontogeny of ultraviolet photosensitivity in rainbow trout (Salmo gairdneri). Visual Neurosci 2:247–254. Google Scholar

23.

C. W. Hawryshyn and F. I. Hárosi . 1991. Ultraviolet photoreception in carp: microspectrophotometry and behaviorally determined action spectra. Vision Res 31:567–576. Google Scholar

24.

O. Hisatomi, T. Satoh, L. K. Barthel, D. L. Stenkamp, P. A. Raymond, and F. Tokunaga . 1996. Molecular cloning and characterization of the putative ultraviolet-sensitive visual pigment of goldfish. Vision Res 36:933–939. Google Scholar

25.

O. Hisatomi, T. Satoh, and F. Tokunaga . 1997. The primary structure and distribution of killifish visual pigments. Vision Res 37:3089–3096. Google Scholar

26.

T. Hoshiai and A. Tanimura . 1981. Copepods in the stomach of a nototheniid fish, Trematomus borchgrevinki fry at Syowa Station, Antarctica. Mem Natl Inst Polar Res 34:44–48. Google Scholar

27.

T. Hoshiai, A. Tanimura, M. Fukuchi, and K. Watanabe . 1989. Feeding by the nototheniid fish, Pagothenia borchgrevinki on the ice-associated copepod, Paralabidocera antarctica. Proc NIPR Symp Polar Biol 2:61–64. Google Scholar

28.

H. Ito and T. Murakami . 1984. Retinal ganglion cells in two teleost species, Sebastiscus marmoratus and Navodon modestus. J Comp Neurol 229:80–96. Google Scholar

29.

Y. W. Kunz, G. Wildenburg, L. Goodrich, and E. Callaghan . 1994. The fate of ultraviolet receptors in the retina of the Atlantic salmon (Salmo salar). Vision Res 34:1375–1383. Google Scholar

30.

E. R. Loew and C. M. Wahl . 1991. A short-wavelength sensitive cone mechanism in juvenile yellow perch, Perca flavescens. Vision Res 31:353–360. Google Scholar

31.

E. R. Loew, W. N. McFarland, E. L. Mills, and D. Hunter . 1993. A chromatic action spectrum for planktonic predation by juvenile yellow perch, Perca flavescens. Can J Zool 71:384–386. Google Scholar

32.

G. S. Losey, T. W. Cronin, T. H. Goldsmith, D. Hyde, N. J. Marshall, and W. N. McFarland . 1999. The UV visual world of fishes: a review. J Fish Biol 54:921–943. Google Scholar

33.

J. A. Macdonald and J. C. Montgomery . 1991. The sensory biology of notothenioid fish. In “Biology of Antarctic fish”. Ed by G. Prisco, B. Maresca, and B. Tota . Springer-Verlag. Heidelberg. pp. 145–162. Google Scholar

34.

W. N. McFarland and F. W. Munz . 1975. Part III: The evolution of photopic visual pigments in fishes. Vision Res 15:1071–1080. Google Scholar

35.

W. N. McFarland and E. R. Loew . 1994. Ultraviolet visual pigments in marine fishes of the family Pomacentridae. Vision Res 34:1393–1396. Google Scholar

36.

V. B. Meyer-Rochow 1982. Lifeforms under Antarctic ice. Kagaku Asahi 42:16–19. in Japanese. Google Scholar

37.

V. B. Meyer-Rochow 1990. A case of abnormal eye enlargement in the Antarctic fish Pagothenia borchgrevinki (Pisces, teleostei, notothenioidei). NZ Antarctic Rec 10:28–31. Google Scholar

38.

V. B. Meyer-Rochow and M. A. Klyne . 1982. Retinal organization of the eyes of three nototheniid fishes from Ross Sea (Antarctica). Gegenbaurs Morphol Jahrb 128:762–777. Google Scholar

39.

V. B. Meyer-Rochow, Y. Morita, and S. Tamotsu . 1999. Immunocytochemical observations of the pineal organ and retina of the Antarctic teleosts Pagothenia borchgrevinki and Trematomus bernacchii. J Neurocytol 28:125–130. Google Scholar

40.

T. Miyazaki and Y. Nakamura . 1990. Single line acuity of 0-year-old Japanese parrotfish determined by the conditioned reflex method. Nippon Suisan Gakkaishi 56:887–892. in Japanese. Google Scholar

41.

T. Miyazaki, S. Shiozawa, T. Kogane, R. Masuda, K. Maruyama, and K. Tsukamoto . 2000. Developmental changes of the light intensity threshold for school formation in the striped jack Pseudocaranx dentex. Mar Ecol Prog Ser 192:267–275. Google Scholar

42.

T. Miyazaki, T. Iwami, M. Yamauchi, and H. Somiya . 2001. “Accessory corner cones” as putative UV-sensitive photoreceptors in the retinas of seven adult nototheniid fishes. Polar Biol 24:628–632. Google Scholar

43.

J. C. Montgomery and J. A. Macdonald . 1985. Oculomotor function at low temperature: Antarctic versus temperate fish. J Exp Biol 117:181–191. Google Scholar

44.

Y. Morita, V. B. Meyer-Rochow, and K. Uchida . 1997. Absolute and spectral sensitivities in dark- and light-adapted Pagothenia borchgrevinki, an Antarctic nototheniid fish. Physiol Behav 61:159–163. Google Scholar

45.

T. Murayama and H. Somiya . 1998. Distribution of ganglion cells and object localizing ability in the retina of three cetaceans. Fisheries Sci 64:27–30. Google Scholar

46.

I. Novales-Flamarique 2000. The ontogeny of ultraviolet sensitivity, cone disappearance and regeneration in the sockeye salmon Oncorhynchus nerka. J Exp Biol 203:1161–1172. Google Scholar

47.

N. W. Pankhurst and J. C. Montgomery . 1989. Visual function in four Antarctic Nototheniid fishes. J Exp Biol 142:311–324. Google Scholar

48.

N. W. Pankhurst and J. C. Montgomery . 1990. Ontogeny of vision in the Antarctic fish Pagothenia borchgrevinki (Nototheniidae). Polar Biol 10:419–422. Google Scholar

49.

P. A. Raymond, L. K. Barthel, M. E. Rounsifer, S. A. Sullivan, and J. K. Knight . 1993. Expression of rod and cone visual pigments in goldfish and zebrafish: A rhodopsin-like gene is expressed in cones. Neuron 10:1161–1174. Google Scholar

50.

J. Shand, S. M. Chin, A. M. Harman, S. Moore, and S. P. Collin . 2000. Variability in the location of the retinal ganglion cell area centralis is correlated with ontogenetic changes in feeding behavior in the black bream, Acanthopagrus butcheri (Sparidae, teleostei). Brain Behav Evol 55:176–190. Google Scholar

51.

T. Tamura 1957. A study of visual perception in fish, especially on resolving power and accommodation. Bull Jap Soc Sci Fish 22:536–557. Google Scholar

52.

A. V. Whitmore and J. K. Bowmaker . 1989. Seasonal variation in cone sensitivity and short-wave absorbing visual pigments in the rudd Scardinius erythrophthalmus. J Comp Physiol A 166:103–115. Google Scholar

53.

M. Williamson and A. Keast . 1988. Retinal structure relative to feeding in the rock bass (Ambloplites rupestris) and bluegill (Lepomis macrochirus). Can J Zool 66:2840–2846. Google Scholar
Taeko Miyazaki, Tetsuo Iwami, Hiroaki Somiya, and V. Benno Meyer-Rochow "Retinal Topography of Ganglion Cells and Putative UV-Sensitive Cones in Two Antarctic Fishes: Pagothenia borchgrevinki and Trematomus bernacchii (Nototheniidae)," Zoological Science 19(11), 1223-1229, (1 November 2002). https://doi.org/10.2108/zsj.19.1223
Received: 30 April 2002; Accepted: 1 August 2002; Published: 1 November 2002
JOURNAL ARTICLE
7 PAGES


SHARE
ARTICLE IMPACT
Back to Top