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The development of visual acuity in larval plaice (Pleuronectes platessa L.) and turbot (Scophthalmusmaximus L.)
J. Exp. Mar. Biol. Ecol., 1984, Vol. 78, pp. 167-175 Elsevier
167
JEM 272
THE DEVELOPMENT OF VISUAL ACUITY IN LARVAL PLAICE
(PLEURONECTES
PLATESSA
L.) AND TURBOT (SCOPHTHALMUS
MAXZMUS
L.)
D.A. NEAVE Scottish Marine Biological Association, Dunstaffnage Marine Research Laboratory, P.O. Box 3, Oban. Argyll. PA34 4AD, Scotland
Abstract: Developmental changes in the visual acuity of larval flatfish (plaice, Pleuronectesplatessa L., and turbot, Scophthalmus maximus L.) were investigated behaviourally (using the optomotor response) and histologically. Results were similar for the two species, but different for the two methods. Histological acuities improvedgradually from hatching onwards, while behavioural acuities showed a rapid improvement at the end of the yolk sac period, but this slowed down later. Histological acuities were initially better than the behavioural acuities; for first feeding larvae behavioural acuities were 6-7” in both species compared with histological acuities of 1 ’ in plaice and 1 “20’ in turbot. This situation later changed and by mid-metamorphosis the behavioural acuities were better than the histological ones; for metamorphosed fish behavioural acuities were 11’ in both species while histological acuities were 40’ in plaice and 20’ in turbot.
INTRODUCTION
Visual acuity is normally defined as the minimum angle which a stimulus can subtend at the eye and yet still be resolved. It can be determined either theoretically by means of histological measurements of the eye, or behaviourally by determining the smallest stimulus size which will elicit a particular response. Such determinations have been made for the adults of many species of fish (reviewed by Muntz, 1974), and it has been shown that acuity improves with growth (Baerends et al., 1960; Hairston et al., 1982; Breck & Gitter, 1983). However, little work has been done on fish larvae. Blaxter & Jones (1967) and Otten (1981) have calculated acuities for larval herring (&pea harengus) and Huplochromis eleguns respectively, and Rahmann et al. (1979) examined the changes in the behavioural visual acuity of rainbow trout (Sulmo guirdneri) from hatching to one year old. Larval flatfish show an optomotor response (Finger, 1976) and so it was decided to use this reaction to investigate the developmental changes in the behavioural visual acuity of plaice (Pleuronectes plufessa L.) and turbot (Scophthulmus muximus L.) and to undertake a comparative histological study.
METHODS LARVAE
Larvae of both species were reared from artificially fertilized eggs under an 18 : 6 L : D photoperiod of fluorescent striplights which gave a light intensity of 130 lux at the water 0022-0981/84/$03.00
0 1984 Elsevier Science Publishers B.V.
D.A. NEAVE
168
surface. Water temperatures were 7-l 1 ‘C for plaice and 20-22 ‘C for turbot. Turbot larvae were fed with rotifers for the first lo-14 days after hatching and thereafter with newly hatched Artemia nauplii; plaice larvae were fed with newly hatched Artemia nauplii only. For plaice the developmental stages of Ryland (1966) were used in this investigation. There is no comparably detailed staging system for turbot larvae, although Jones (1972) has described their development, and so Ryland’s stages were applied to this species. These stages are: Stage 1 (yolk sac), Stage 2 (post yolk sac), Stage 3 (pre-metamorphosis), Stage 4a (early metamorphosis), Stage 4b (late metamorphosis) and Stage 5 (metamorphosed). HISTOLOGICAL
DETERMINATION
If one assumes that acuity is limited by the density of cones in the retina, then a simple hypothesis is that a grating of black and white stripes will be just resolvable when the images of the white stripes fall upon alternate rows of cones and are separated by single rows of unstimulated cones (Helmholtz, 1924-5; cited in Muntz, 1974). Thus, acuity is given by the formula: sin cr=C
f'
where a is the minimum separable angle, c is the distance between the centres of adjacent cones and f is the focal length of the lens. Here cones were measured in numbers per 100 pm length of retina(d) and so the reciprocal of 10dgives the cone separation in mm. During processing the eyeball shrank by z 10%) thus, this expression must be multiplied by 1.11 to obtain the separation in life. The focal length of the lens can be calculated by multiplying its radius (r) by 2.55 (Matthiessen’s ratio; Matthiessen, 1880). This gives the following expression: sin a =
1.11 10d x 2.55r ’
Larvae were fixed in Bouin’s fluid, serially sectioned at 5 pm and stained with Delafield’s Haematoxylin. Using sections through the middle of each eye, cones were counted over six lOO+m lengths of retina and four diameter measurements were made on the widest lens section. The regressions of these two factors on age were calculated and the changes in theoretical acuity with age were worked out from these regression equations.
VISUAL BEHAVIOURAL
ACUITY
OF LARVAL
169
FLATFISH
DETERMINATION
The optomotor response apparatus consisted of a horizontal white Perspex disc on which clear Perspex cylinders, 11 cm high and either 9.5 or 15.5 cm in diameter, could be placed. An electric motor rotated the disc clockwise or anticlockwise at speeds between 2 and 15 r.p.m. The stimulus consisted of paper cylinders photographically printed with equal width black and white stripes and held inside the Perspex cylinders. The stripes varied in width from 18.0 to 0.15 mm and subtended angles of 30” to 11’ at the fish container. The latter was a 2-cm diameter glass tube held stationary at the centre of the stimulus cylinder. The apparatus, apart from the top of the fish container, was covered with a white paper lid. Experiments were performed in constant temperature rooms at 10 “C (plaice) and 20 “C (turbot) under overhead illumination of = 200 lux. Individual larvae were observed from above while the stimulus cylinder was rotated. Simple swimming in the same direction as the cylinder did not constitute a positive response. For a positive response both swimming speed and direction had to vary as the stimulus rotation speed and direction were varied. In larvae which were completing metamorphosis and had settled, nystagmus (optical tracking of the stimulus) was looked for rather than swimming. On average eight plaice and four turbot were tested at each stage.
RESULTS
HISTOLOGICAL
ACUITY
The changes in lens diameters and cone densities are shown in Figs. 1 and 2. In both species lens diameter increases with age, while cone density decreases; this results in Stage 1
1
2a
1 2b 1 3a
1 3b bcl 4a 1
Lb
I5
Age OJaysl Fig. 1. Changes in lens diameter (+ ) and cone density (0) with age in plaice larvae: calculated regression lines are shown, the equations for these lines are y = 1.733x + 102.44 for lens diameter and y = -0.153x + 44.76 for cone density.
D.A. NEAVE
170
only a slight rise in histological acuity between hatching and the end of metamorphosis (Figs. 3 and 4). At first feeding plaice have a histological acuity of lo and turbot have one of 1’ 20’ ; these values improve to 40’ and 20’ respectively by the end of metamor-
2
01
0
131
10
4a
stage I
20
4b
30
5
I
40
120
Age (Days) Fig. 2. Changes in lens diameter ( + ) and cone density (0) with age in turbot larvae: calculated regression lines are shown, the equations for these lines are y = 10.179x + 48.75 for lens diameter and y = - 0.363x + 47.09 for cone density.
phosis. Plaice larvae do not possess an area (a region of increased cone density which gives better acuity) (Blaxter, 1968), nor was one observed in turbot. BEHAVIOURAL
ACUITY
‘The changes in the behaviourally determined visual acuities of plaice and turbot are shown in Figs. 3 and 4 respectively. The filled circles indicate the stimulus angles to which all the larvae tested at a particular stage showed a positive response. Occasionally, however, one or two larvae gave a positive response and/or an inconsistent response to the next narrower stimulus. The stepped appearance of the graphs is due to the abrupt changes in stripe width between successive stimuli sizes. Turbot, unlike plaice, do not show an optomotor response in the first two days after hatching, the turbot eye being rudimentary at this time. In both species the improvement in acuity is rapid once the eye develops, and acuity is ~6-7” at first feeding (late
171
VISUAL ACUITY OF LARVAL FLATFISH
Stage 1). The rate of improvement slows down later and reaches the best value determinable with the apparatus (11’) during Stage 4b. However, the acuity of plaice attains a value of 22’ during Stage 3b, while turbot do not attain this value until the start of Stage 4b.
t
1
I
2a
Stage f 2b 1 3a
09
,p--c-O-+-S--I m--T-/ pd ,?-’ I /
10. _ 20.
4b
f S
Qp%.t-4
dlJ/ I 1 f ; I * I !
3O. 40. 5s
,df ,I
g 60.
p-o- - dl ,I/
3 7o-
2
f 3b bd 4a !
80.
.!!! 2-
*
6
&__,*’ :
i
I
! I
Ii
i0
io
io
ti
Sk
Bo
7b
Age (Days)
Fig. 3. Changes in the visual acuity of plaice larvae with age: solid line indicates histological acuity; broken lines indicate behavioural acuity (0, positive response by all larvae at that stage; 0, inconsistent response and/or a positive response by a few larvae).
D.A. NEAVE
172
Stage [II
2
131
4a
1
4b
I
5
I
0
IO
20
30
40
Age (Days) Fig. 4. Changes in the visual acuity of turbot larvae with age; solid line indicates histological acuity: broken lines indicate behavioural acuity (0, positive response by all larvae at that stage; 0, inconsistent response and/or a positive response by a few larvae).
DISCUSSION
One of the most interesting aspects of this work is that it allows a comparison to be made between acuities determined behaviourally and those determined histologically. The results show two differences between these two acuities: in the early stages of development, when the histological acuity is better than the behavioural, and in the later stages when the situation is reversed. Of the two differences, histological acuity being better than behavioural acuity is the more easily explained since the larvae are not responding to the full range of visual information which their eyes can theoretically supply them with. As Rahmann et al. (1979) have pointed out, during early development visual acuity may be determined by the degree of differentiation and development of the optic tectum rather than by the optics of the eye. Thus, early improvement in acuity is probably due to growth of the optic tectum, not to growth of the eye. There are several possible explanations of the situation in the later developmental
VISUAL
ACUITY
OF LARVAL
FLATFISH
173
stages, when the larvae are responding to information which, theoretically, their eyes cannot supply. One possibility is that of errors in the formula for histological acuity. If lens shrinkage occurred, then the lens diameter (and hence focal length) would be greater than was actually measured. However, the fish lens is only 60% water, two thirds of which is protein-bound (Racz et al., 1979), and so one would not expect shrinkage to cause a significant underestimate of acuity. Errors may arise if Matthiessen’s ratio of 2.55 (Matthiessen, 1880) does not apply to larval flatfish. Sroczynski (1977) and Fernald & Wright (1983) have reported values ranging from 2.10 to 2.49 depending on the species, but, if these values are used here they cause acuity to be worse than was originally calculated. Otten (1981) found that in larval Huplochromis eleguns the ratio reached values of up to 2.90, but this is insufficient to account for the discrepancies seen here. It is possible that the histological acuities (based on the eye viewing static stimuli) are correct, but that acuities are better for moving stimuli (Muntz, 1974). Westheimer & McKie (1975) investigated the effects of stimulus motion on visual acuity in humans and, while they did not find that this consistently improved acuity, they did find that vernier tasks (distinguishing whether two lines are offset from one another, rather than separate) could be accomplished to a precision of a fifth of a receptor diameter at image motion rates of up to 300 receptors/s. Thus, when they respond to stimuli of very fine lines, metamorphosing and metamorphosed plaice and turbot may not be distinguishing individual lines, but may merely be responding to the stimulus movement. This obviously requires a well developed optic tectum, which both species possess as adults (De Groot, 197 1). The earlier, rapid improvements in acuity may well indicate that the optic tecta of the two species are well developed at this time. Muntz (1974) has reviewed much data, particularly for fish, which show that histological and behavioural acuities are generally similar. However, some histological acuities are based on the formula of Tamura (1957) which, as Northmore & Dvorak (1977) have pointed out, gives twice the minimum separable angle; here such acuities have been corrected. In this investigation the best behavioural acuities (attained in Stage 5) were 11’ for both species, while the best histological acuities were 40’ for plaice and 20’ for turbot. Blaxter & Jones (1967) found that the best histological acuities in herring were l”30’ at 10 mm length and 25’ at 30 mm length (corrected values). Little other work has been done on larval fish, although Otten (1981) has calculated that the acuity of larval H. eleguns is lo (corrected value). Rahmann et al. (1979) used the optomotor response to examine the development of visual acuity in rainbow trout; their results are similar to those described here, with acuity rapidly reaching 2” shortly after hatching, but, once feeding starts, this improvement slows down and acuity is 18-28’ 68 days after hatching. Thus, the histological acuities calculated here are better than those found in the larvae of other species, while the behavioural acuities are about the same. Acuities calculated for adult fish are generally better than those found here: 2.1-7.7’ for 27 species (Tamura, 1957) and l-2’ for 10 species (Tamura & Wisby, 1963) (corrected values). However, Otten (1981) calculated that the acuity of adult H. eleguns was
174
D.A.NEAVE
only 15’ (corrected value). Behaviourally derived acuities are more comparable: 4.9-10.8’ for&e species (literature reviewed by Muntz, 1974), 14’ for 1-yr-old trout (Rahmann et.&, 1979) and 10-40’ .for bluegill sunfish (Lepomis macrochims) depending on size (Hairston et al., 1982; Breck & Gitter, 1983). There is a possibly important difference between the behavioural acuity changes in the two species in that plaice attain a relatively good acuity (22’) before starting metamorphosis, while turbot have only attained an acuity of l-2’ at this time. This may explain why the period just before metamorphosis is a critical one for tank reared turbot when large mortalities may occur for no apparent reason.
ACKNOWLEDGEMENTS
I wish to thank Dr. J. H. S. Blaxter and Dr. R. S. Batty for their helpful advice and encouragement, and also, together with Dr. A. J. Geffen, for assistance in rearing larvae. This work was supported by a grant from the Natural Environmental Research Council.
REFERENCES BAERENDS,G.P., B.E. BENNEMA& A.A.VOGELZANG,1960. Uber die Anderung der Sehscharfe mit dem Wachstum bei Aequidensportalegrensis (Hensel) (Pisces, Cichlidae). 2001. Jb. Geogr., Vol. 88, pp. 67-78. BLAXTER,J. H. S., 1968. Light intensity, vision and feeding in young plaice. J. Exp. Mar. Biol. Ecol., Vol. 2, pp. 293-307. BLAXTER,J. H. S. & M. P. JONES, 1967. The development of the retina and retinomotor responses in the herring. J. Mar. Biol. Assoc. U.K., Vol. 47, pp. 677-697. BRECK,J. E. & M. J. GITTER, 1983. Effect of fish size on the reactive distance of bluegill (Lepomis macrochirus) sunfish. Can. J. Fish. Aquat. Sci., Vol. 40, pp. 162-167. DE GROOT, S.J., 1971. On the interrelationships between morphology of the alimentary tract, food and feeding in flatfishes (Pisces: Pleuronectiformes). Neth. J. Sea Res., Vol. 5, pp. 121-196. FERNALD,R. D. & S. E. WRIGHT, 1983. Maintenance ofoptical quality during crystalline lens growth. Nature (London), Vol. 301, pp. 618-620. FINGER,T. E., 1976. An asymmetric optomotor response in developing flounder larvae (Pseudopleuronectes americanus). Vkion Res., Vol. 16, pp. 941-943. HAIRSTON,N. G., K. T. LI & S. S. EASTER,1982. Fish vision and the detection of planktonic prey. Science, Vol. 218, pp. 1240-1242. JONES, A., 1972. Studies on egg development and larval rearing of turbot, Scophthalmus maximus L., and brill, Scophthalmus rhombus L., in the laboratory. J. Mar. Biol. Assoc. U.K., Vol. 52, pp. 965-986. MAT~HIESSEN,L., 1880. Untersuchungen uber den Aplanatismus die Periscopie der Krystalllinsen in den Augen der Fische. pfliigprs Arch. Gesamte Physiol. Menschen Tiere, Vol. 21, pp. 287-307. MUNTZ,W. R. A., 1974. Comparative aspects in behavioural studies of vertebrate vision. In, The eye. Vol. 6. Comparative physiology, edited by H. Davson & L.T. Graham Jr., Academic Press, New York, pp. 155-227. NORTHMORE,D. P. M. & C. A. DVORAK,1979. Contrast sensitivity and acuity of the goldfish. Vision Res., Vol. 19, pp. 255-261. OTTEN, E., 1981. Vision during growth of a generalized Haplochromis species: H. elegans Trewavas 1933 (Pisces, Cichlidae). Nerh. J. Zool., Vol.31, pp. 650-700. RAcz, P., K. TOMPA& I. P&XC, 1979. The state of water in normal human, bird and fish eye lens. Exp. Eye Res., Vol. 29, pp. 601-608. RAHMANN,H., G. JESERICH& I. ZEUTZIUS,1979. Ontogeny of visual acuity of rainbow trout under normal conditions and light deprivation. Behaviour, Vol. 68, pp. 315-322.
VISUAL ACUITY OF LARVAL FLATFISH
175
RYLAND,J. S., 1966. Observations on the development of larvae of the plaice, Pleuronecfes platessa L., in aquaria. J. Cons., Cons. Int. Explor. Mer., Vol. 30, pp. 177-195. SROCZY~SKI,S., 1977. Spherical abberation of crystalline lens in the roach, Rutilus rutilus L. J. Camp. Physiol. A., Vol. 121, pp. 135-144. TAMURA,T., 1957. A study on visual perception in fish, especially on resolving power and accomodation. Bull. Jpn. Sot. Scient. Fish., Vol. 22, pp. 536-557. TAMURA, T. & W.J. WISBY, 1963. The visual senses of pelagic fishes, especially the visual axis and accomodation. Bull. Mar. Sci. Cur Caribb., Vol. 13, pp. 433-448. WESTHEIMER,G. & S. P. MCKIE, 1975. Visual acuity in the presence of retinal-image motion. J. Opt. Sot. Am., Vol. 65, pp. 847-850.
167
JEM 272
THE DEVELOPMENT OF VISUAL ACUITY IN LARVAL PLAICE
(PLEURONECTES
PLATESSA
L.) AND TURBOT (SCOPHTHALMUS
MAXZMUS
L.)
D.A. NEAVE Scottish Marine Biological Association, Dunstaffnage Marine Research Laboratory, P.O. Box 3, Oban. Argyll. PA34 4AD, Scotland
Abstract: Developmental changes in the visual acuity of larval flatfish (plaice, Pleuronectesplatessa L., and turbot, Scophthalmus maximus L.) were investigated behaviourally (using the optomotor response) and histologically. Results were similar for the two species, but different for the two methods. Histological acuities improvedgradually from hatching onwards, while behavioural acuities showed a rapid improvement at the end of the yolk sac period, but this slowed down later. Histological acuities were initially better than the behavioural acuities; for first feeding larvae behavioural acuities were 6-7” in both species compared with histological acuities of 1 ’ in plaice and 1 “20’ in turbot. This situation later changed and by mid-metamorphosis the behavioural acuities were better than the histological ones; for metamorphosed fish behavioural acuities were 11’ in both species while histological acuities were 40’ in plaice and 20’ in turbot.
INTRODUCTION
Visual acuity is normally defined as the minimum angle which a stimulus can subtend at the eye and yet still be resolved. It can be determined either theoretically by means of histological measurements of the eye, or behaviourally by determining the smallest stimulus size which will elicit a particular response. Such determinations have been made for the adults of many species of fish (reviewed by Muntz, 1974), and it has been shown that acuity improves with growth (Baerends et al., 1960; Hairston et al., 1982; Breck & Gitter, 1983). However, little work has been done on fish larvae. Blaxter & Jones (1967) and Otten (1981) have calculated acuities for larval herring (&pea harengus) and Huplochromis eleguns respectively, and Rahmann et al. (1979) examined the changes in the behavioural visual acuity of rainbow trout (Sulmo guirdneri) from hatching to one year old. Larval flatfish show an optomotor response (Finger, 1976) and so it was decided to use this reaction to investigate the developmental changes in the behavioural visual acuity of plaice (Pleuronectes plufessa L.) and turbot (Scophthulmus muximus L.) and to undertake a comparative histological study.
METHODS LARVAE
Larvae of both species were reared from artificially fertilized eggs under an 18 : 6 L : D photoperiod of fluorescent striplights which gave a light intensity of 130 lux at the water 0022-0981/84/$03.00
0 1984 Elsevier Science Publishers B.V.
D.A. NEAVE
168
surface. Water temperatures were 7-l 1 ‘C for plaice and 20-22 ‘C for turbot. Turbot larvae were fed with rotifers for the first lo-14 days after hatching and thereafter with newly hatched Artemia nauplii; plaice larvae were fed with newly hatched Artemia nauplii only. For plaice the developmental stages of Ryland (1966) were used in this investigation. There is no comparably detailed staging system for turbot larvae, although Jones (1972) has described their development, and so Ryland’s stages were applied to this species. These stages are: Stage 1 (yolk sac), Stage 2 (post yolk sac), Stage 3 (pre-metamorphosis), Stage 4a (early metamorphosis), Stage 4b (late metamorphosis) and Stage 5 (metamorphosed). HISTOLOGICAL
DETERMINATION
If one assumes that acuity is limited by the density of cones in the retina, then a simple hypothesis is that a grating of black and white stripes will be just resolvable when the images of the white stripes fall upon alternate rows of cones and are separated by single rows of unstimulated cones (Helmholtz, 1924-5; cited in Muntz, 1974). Thus, acuity is given by the formula: sin cr=C
f'
where a is the minimum separable angle, c is the distance between the centres of adjacent cones and f is the focal length of the lens. Here cones were measured in numbers per 100 pm length of retina(d) and so the reciprocal of 10dgives the cone separation in mm. During processing the eyeball shrank by z 10%) thus, this expression must be multiplied by 1.11 to obtain the separation in life. The focal length of the lens can be calculated by multiplying its radius (r) by 2.55 (Matthiessen’s ratio; Matthiessen, 1880). This gives the following expression: sin a =
1.11 10d x 2.55r ’
Larvae were fixed in Bouin’s fluid, serially sectioned at 5 pm and stained with Delafield’s Haematoxylin. Using sections through the middle of each eye, cones were counted over six lOO+m lengths of retina and four diameter measurements were made on the widest lens section. The regressions of these two factors on age were calculated and the changes in theoretical acuity with age were worked out from these regression equations.
VISUAL BEHAVIOURAL
ACUITY
OF LARVAL
169
FLATFISH
DETERMINATION
The optomotor response apparatus consisted of a horizontal white Perspex disc on which clear Perspex cylinders, 11 cm high and either 9.5 or 15.5 cm in diameter, could be placed. An electric motor rotated the disc clockwise or anticlockwise at speeds between 2 and 15 r.p.m. The stimulus consisted of paper cylinders photographically printed with equal width black and white stripes and held inside the Perspex cylinders. The stripes varied in width from 18.0 to 0.15 mm and subtended angles of 30” to 11’ at the fish container. The latter was a 2-cm diameter glass tube held stationary at the centre of the stimulus cylinder. The apparatus, apart from the top of the fish container, was covered with a white paper lid. Experiments were performed in constant temperature rooms at 10 “C (plaice) and 20 “C (turbot) under overhead illumination of = 200 lux. Individual larvae were observed from above while the stimulus cylinder was rotated. Simple swimming in the same direction as the cylinder did not constitute a positive response. For a positive response both swimming speed and direction had to vary as the stimulus rotation speed and direction were varied. In larvae which were completing metamorphosis and had settled, nystagmus (optical tracking of the stimulus) was looked for rather than swimming. On average eight plaice and four turbot were tested at each stage.
RESULTS
HISTOLOGICAL
ACUITY
The changes in lens diameters and cone densities are shown in Figs. 1 and 2. In both species lens diameter increases with age, while cone density decreases; this results in Stage 1
1
2a
1 2b 1 3a
1 3b bcl 4a 1
Lb
I5
Age OJaysl Fig. 1. Changes in lens diameter (+ ) and cone density (0) with age in plaice larvae: calculated regression lines are shown, the equations for these lines are y = 1.733x + 102.44 for lens diameter and y = -0.153x + 44.76 for cone density.
D.A. NEAVE
170
only a slight rise in histological acuity between hatching and the end of metamorphosis (Figs. 3 and 4). At first feeding plaice have a histological acuity of lo and turbot have one of 1’ 20’ ; these values improve to 40’ and 20’ respectively by the end of metamor-
2
01
0
131
10
4a
stage I
20
4b
30
5
I
40
120
Age (Days) Fig. 2. Changes in lens diameter ( + ) and cone density (0) with age in turbot larvae: calculated regression lines are shown, the equations for these lines are y = 10.179x + 48.75 for lens diameter and y = - 0.363x + 47.09 for cone density.
phosis. Plaice larvae do not possess an area (a region of increased cone density which gives better acuity) (Blaxter, 1968), nor was one observed in turbot. BEHAVIOURAL
ACUITY
‘The changes in the behaviourally determined visual acuities of plaice and turbot are shown in Figs. 3 and 4 respectively. The filled circles indicate the stimulus angles to which all the larvae tested at a particular stage showed a positive response. Occasionally, however, one or two larvae gave a positive response and/or an inconsistent response to the next narrower stimulus. The stepped appearance of the graphs is due to the abrupt changes in stripe width between successive stimuli sizes. Turbot, unlike plaice, do not show an optomotor response in the first two days after hatching, the turbot eye being rudimentary at this time. In both species the improvement in acuity is rapid once the eye develops, and acuity is ~6-7” at first feeding (late
171
VISUAL ACUITY OF LARVAL FLATFISH
Stage 1). The rate of improvement slows down later and reaches the best value determinable with the apparatus (11’) during Stage 4b. However, the acuity of plaice attains a value of 22’ during Stage 3b, while turbot do not attain this value until the start of Stage 4b.
t
1
I
2a
Stage f 2b 1 3a
09
,p--c-O-+-S--I m--T-/ pd ,?-’ I /
10. _ 20.
4b
f S
Qp%.t-4
dlJ/ I 1 f ; I * I !
3O. 40. 5s
,df ,I
g 60.
p-o- - dl ,I/
3 7o-
2
f 3b bd 4a !
80.
.!!! 2-
*
6
&__,*’ :
i
I
! I
Ii
i0
io
io
ti
Sk
Bo
7b
Age (Days)
Fig. 3. Changes in the visual acuity of plaice larvae with age: solid line indicates histological acuity; broken lines indicate behavioural acuity (0, positive response by all larvae at that stage; 0, inconsistent response and/or a positive response by a few larvae).
D.A. NEAVE
172
Stage [II
2
131
4a
1
4b
I
5
I
0
IO
20
30
40
Age (Days) Fig. 4. Changes in the visual acuity of turbot larvae with age; solid line indicates histological acuity: broken lines indicate behavioural acuity (0, positive response by all larvae at that stage; 0, inconsistent response and/or a positive response by a few larvae).
DISCUSSION
One of the most interesting aspects of this work is that it allows a comparison to be made between acuities determined behaviourally and those determined histologically. The results show two differences between these two acuities: in the early stages of development, when the histological acuity is better than the behavioural, and in the later stages when the situation is reversed. Of the two differences, histological acuity being better than behavioural acuity is the more easily explained since the larvae are not responding to the full range of visual information which their eyes can theoretically supply them with. As Rahmann et al. (1979) have pointed out, during early development visual acuity may be determined by the degree of differentiation and development of the optic tectum rather than by the optics of the eye. Thus, early improvement in acuity is probably due to growth of the optic tectum, not to growth of the eye. There are several possible explanations of the situation in the later developmental
VISUAL
ACUITY
OF LARVAL
FLATFISH
173
stages, when the larvae are responding to information which, theoretically, their eyes cannot supply. One possibility is that of errors in the formula for histological acuity. If lens shrinkage occurred, then the lens diameter (and hence focal length) would be greater than was actually measured. However, the fish lens is only 60% water, two thirds of which is protein-bound (Racz et al., 1979), and so one would not expect shrinkage to cause a significant underestimate of acuity. Errors may arise if Matthiessen’s ratio of 2.55 (Matthiessen, 1880) does not apply to larval flatfish. Sroczynski (1977) and Fernald & Wright (1983) have reported values ranging from 2.10 to 2.49 depending on the species, but, if these values are used here they cause acuity to be worse than was originally calculated. Otten (1981) found that in larval Huplochromis eleguns the ratio reached values of up to 2.90, but this is insufficient to account for the discrepancies seen here. It is possible that the histological acuities (based on the eye viewing static stimuli) are correct, but that acuities are better for moving stimuli (Muntz, 1974). Westheimer & McKie (1975) investigated the effects of stimulus motion on visual acuity in humans and, while they did not find that this consistently improved acuity, they did find that vernier tasks (distinguishing whether two lines are offset from one another, rather than separate) could be accomplished to a precision of a fifth of a receptor diameter at image motion rates of up to 300 receptors/s. Thus, when they respond to stimuli of very fine lines, metamorphosing and metamorphosed plaice and turbot may not be distinguishing individual lines, but may merely be responding to the stimulus movement. This obviously requires a well developed optic tectum, which both species possess as adults (De Groot, 197 1). The earlier, rapid improvements in acuity may well indicate that the optic tecta of the two species are well developed at this time. Muntz (1974) has reviewed much data, particularly for fish, which show that histological and behavioural acuities are generally similar. However, some histological acuities are based on the formula of Tamura (1957) which, as Northmore & Dvorak (1977) have pointed out, gives twice the minimum separable angle; here such acuities have been corrected. In this investigation the best behavioural acuities (attained in Stage 5) were 11’ for both species, while the best histological acuities were 40’ for plaice and 20’ for turbot. Blaxter & Jones (1967) found that the best histological acuities in herring were l”30’ at 10 mm length and 25’ at 30 mm length (corrected values). Little other work has been done on larval fish, although Otten (1981) has calculated that the acuity of larval H. eleguns is lo (corrected value). Rahmann et al. (1979) used the optomotor response to examine the development of visual acuity in rainbow trout; their results are similar to those described here, with acuity rapidly reaching 2” shortly after hatching, but, once feeding starts, this improvement slows down and acuity is 18-28’ 68 days after hatching. Thus, the histological acuities calculated here are better than those found in the larvae of other species, while the behavioural acuities are about the same. Acuities calculated for adult fish are generally better than those found here: 2.1-7.7’ for 27 species (Tamura, 1957) and l-2’ for 10 species (Tamura & Wisby, 1963) (corrected values). However, Otten (1981) calculated that the acuity of adult H. eleguns was
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only 15’ (corrected value). Behaviourally derived acuities are more comparable: 4.9-10.8’ for&e species (literature reviewed by Muntz, 1974), 14’ for 1-yr-old trout (Rahmann et.&, 1979) and 10-40’ .for bluegill sunfish (Lepomis macrochims) depending on size (Hairston et al., 1982; Breck & Gitter, 1983). There is a possibly important difference between the behavioural acuity changes in the two species in that plaice attain a relatively good acuity (22’) before starting metamorphosis, while turbot have only attained an acuity of l-2’ at this time. This may explain why the period just before metamorphosis is a critical one for tank reared turbot when large mortalities may occur for no apparent reason.
ACKNOWLEDGEMENTS
I wish to thank Dr. J. H. S. Blaxter and Dr. R. S. Batty for their helpful advice and encouragement, and also, together with Dr. A. J. Geffen, for assistance in rearing larvae. This work was supported by a grant from the Natural Environmental Research Council.
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