Retinal morphology of cyprinid fishes: A quantitative histological study of ontogenetic changes and interspecific variation

0042-6989/91 S3.00+ 0.00 Copyright 0 1991 Pergamon Press plc

Vision Res. Vol. 31, NO. 3, pp. 383-394, 1991 Printed in Great Britain. All rights reserved

RETINAL STRUCTURE; PHYSIOLOGY AND PHARMACOLOGY RETINAL MORPHOLOGY OF CYPRINID FISHES: A QUANTITATIVE HISTOLOGICAL STUDY OF ONTOGENETIC CHANGES AND INTERSPECIFIC VARIATION MONKA ZAUNREITER,* HEIDI JUNGER

and

KURT KOIXSCHAL

Zoologisches Institut der UniversitPt Salzburg, HellbrunnerstraBe 34, A-5020 Salzburg, Austria (Received 5 January 1990; in revised form 20 April 1990) Abstract-Morphological patterns of the retina, cone size and density, rod density, ro&cone ratio, ganglion cell density, convergence of receptor cells, resolving power (RP) and regionalization were examined throughout life history in roach and in adults of asp, bream, common carp, roach and sabre carp. The retina of hatchlings is packed with small cones. During larval and juvenile growth the retina stretches, cones increase in diameter and rods are present in increasing numbers. Photopic and scotopic sensitivity as well as resolving power increase. Comparison of adults shows distinct interspecific differences in retinal parameters, which can be related to life style. ZusPmmenfsssnng-Die Retina-Morphologie wurde wIhrend der Entwicklung von Rotaugen und bei adulten Individuen von Rapfen, Brachse, Karpfen, Rotauge und Sichling untersucht. ZapfengriiDe und -dichte, das Verhlltnis von Stlbchen zu Zapfen, Ganglienzelldichte, Konvergenz der Rezeptoren, Resolving power (RP) und Regionalisierung wurden dafiir herangezogen. Die Retina frisch geschliipfter Rotaugen besteht aus kleinen, dicht gepackten Zapfen. Wgihrend des larvalen und juvenilen Wachstums streckt sich die Retina, Zapfen werden grijBer, Stibchen werden vermehrt gebildet. Auf diese Weise steigt die photopische und die scotopische Empfindlichkeit, sowie die RP. Bei den adulten Individuen der untersuchten Arten kiinnen die morphologischen Unterschiede mit den unterschiedlichen Lebensweisen korreliert werden. Ecomorphology tivity Vision

Photopic resolving power

Retinal topography

INTRODUCTION

The retinal morphology of teleost fishes is highly diversified (Ali & Klyne, 1985; Engstriim, 1963a; Locket, 1970; Lyall, 1957; McEwan, 1938; Wagner, 1972, 1975) and has been found to correlate with habitat type (Ali & Hanyu, 1963; Collin & Pettigrew, 1988a, b; Henderson & Northcote, 1988; Locket, 1970; Menezes, Wagner & Ali, 198 1; Muntz, 1982; O’Connell, 1963; Wagner, Menezes & Ali, 1976) and life styles (Ahlbert, 1968, 1976; Williamson & Keast, 1988). Retinal structure at different developmental stages has been described (Blaxter, 1975; Fernald, 1985; Locket, 1980; Sandy & Blaxter, 1980) and selected retinal *Present address: Department of Anatomy and Cell Biology, University of Marburg, Robert-Koch-StraBe 6, D-3550 Marburg, F.R.G.

Scotopic system

Sensi-

parameters have been repeatedly compared between species and during ontogeny (e.g. the cone mosaic: Ahlbert, 1976; Boehlert, 1978; Engstrijm, 1960, 1963b). However, data on the dynamics of retinal ontogeny are still rare (Bijhlert, 1979; Guma’a, 1982; Otten, 1981; Wagner, 1974). Cyprinidae is the most “successful” teleost family in the freshwaters of the northern hemisphere (Nelson, 1984). The various species exhibit a variety of different life styles (Schiemer, 1985) and, according to brain morphology, they may be divided into four major sensory groups: generalized, advanced generalized (abramine), chemosensory and octave-lateralis (Kotrschal & Junger, 1988; Kotrschal, Brandstitter, Gomahr, Junger, Palzenberger & Zaunreiter, 1990). Although cyprinids (particularly the goldfish, Cara.ssius auratus), have been favoured

383

MONIKAZAUNREITER et al

384

models in vision research (Marc & Sperling, 1976; Mednick & Springer, 1986; Neumeyer, 1985; Scholes, 1975; Stell & Harosi, 1976), comparatively little effort has been made to investigate interspecific variation of the retina of these fish (Engstrom, 1960; Zaunreiter & Kotrschal, 1989). Studies of comparative brain morphology have revealed a distinct interspecific variation in relative volumes of cyprinid primary sensory lobes (Kotrschal & Junger, 1988) so questions arise as to whether and to what degree the retinal system also varies between species with different brain types. In the present study we compare retinal structure of five cyprinid species, each representing a different brain type (Kotrschal & Junger, 1988) and life style (Schiemer & Hofer, 1983; Schiemer, 1985). These are the piscivorous asp (Aspius aspius) (generalized brain), the omnivorous roach (Rutilus rutilus) (generalized brain), the bottom feeding and planktivorous bream (Abramis bruma) (abramine = advanced generalized brain), the benthivorous common carp (Cyprinus carpio) (chemosensory brain) and the surface and plankton feeding sabre carp (P&ecus culfratus) (octave-lateralis brain). Being aware of the effects of allometric growth on brain morphology (Brandstatter & Kotrschal, 1989, 1990), we examined retinal morphology during life history (from hatchlings to large adults) in roach. We consider this species a representative model, as it is the most common cyprinid in Europe, and has a generalized life style (Schiemer, 1985) and a generalized brain and sensory morphology (Kotrschal & Junger, 1988; Kotrschal et al., 1990).

Table 1. List of investigated specimens Species

ED (mm)

SL (mm)

Roach Roach Roach Roach Roach Roach

Origin

4.0 7.0 9.0 11.0 14.0 35.0

0.1 0.4 0.5 1.0 1.5 3.0

Laboratory reared, egg material from Stopfenreuther Au

Roach Roach Roach Roach Asp Bream Carp Sabre carp

52.0 95.0 145.0 230.0 357.0 335.0 345.0 355.0

3.8 6.8 8.5 12.0 14.5 15.2 15.8 18.8

Stopfenreuther Au

SL-standard

length, ED-eye

diameter.

After rinsing in phosphate buffer (pH 7.4) the retinae were dissected out of the eyeballs and lens diameters measured with sliding callipers to the nearest l/10 mm. For lens diameter measurements more individuals were used than for later quantitative analysis of the retina. Left eye retinae, which were used for tangential sectioning, were cut into 16 pieces and their retinal positions mapped. For cross sectioning a narrow horizontal band was cut out of the retinae of the right eyes, as well as one dorsoventrally orientated band out of each the remaining dorsal and ventral retinal segments. Pieces of retina were dehydrated in ethanol and

MATERIALS AND METHODS

Fish were collected by gill-netting in the Stopfenreuther Au, a Danube wetland area in the east of Austria. Common carp were purchased at a local fishmongers. Standard length (SL) was recorded prior to dissection (Table 1, Fig. 1). After deep MS 222 anaesthesia fish were perfused via the Bulbus arteriosus with buffered 10% formaldehyde solution. In small specimens (SL < 100 mm) the eyes were removed after anaesthesia, cut open dorsally and fixed by immersion in the same fixative. The eyes of all fish were stored in the fixative for at least 2 weeks, after eye diameters had been measured (Table 1) and dorsal incisions had been made for orientation.

Rutilwrutilus

ofthe

maeh

SL4-22Omm;

_

tutins n-10

I

Fig. 1. Diagram showing the two-dimensional approach of the present investigation. The intraspecific, ontogenetic retinal changes were considered in roach. The interspecific retinal variation was compared between adult individuals of five species. Standard lengths of specimens indicated.

385

Retinal morphology of cyprinid fishes

embedded in Historesin (Reichert). 3-pm sections were cut, mounted on glass slides and stained with Haematoxilin-Eosine. For quantification sections were examined in a light-microscope and projected onto a computer-digitizing tablet with the aid of a camera lucida. Counts and measurements were fed directly into an Apple Be computer. On each of the 16 tangentially sectioned pieces per retina, cone diameters were measured and cones per area counted on three different positions of each section, each counting area measuring 250pm2 (for specimens with SL < 100 mm), 640 pm2 (SL = lO(r200 mm), or 1220 pm2 (SL > 200 mm). Mean values were calculated and mapped. On the cross sections, the thickness of retinal layers was measured and the number of each category of retinal nuclei (rods, horizontal cells, bipolar cells, amacrine cells, ganglion cells) per 100 pm length of the section was recorded. The mean values of three measurements were calculated for each of nine different positions on the retina. Retinal resolving power (RP) was calculated according to Van der Meer and Anker (1984): RP = l/,/2 x n/360 x 2.55r x Jn where 2.55 is the Matthiesen’s ratio (eye ~ameter~lens diameter), r is the radius of the lens, and n the cone density per mm2.

Isodensity maps for judgement of retinal regionalization were constructed by plotting the cone density values of retinal samples according to their mapped positions. RESULTS

Unt~geny of the retina in roach Initial fast allometric growth of the eye during the larval and early juvenile period (SL < 20 mm) decreases markedly (Fig. 2). Significant changes with growth affect the retinal histology (Fig. 3). The size of receptor cells increases, and so does the density of nuclei within the outer nuclear layer, whereas nuclear density decreases within the inner nuclear layer (Fig. 3). These density shifts are due to the migration of rod precursors from the inner to the outer nuclear layer and to the formation of new rods (Raymond & Rivlin, 1987) in a retina which stretches during growth (Ali, 1964). Thicknesses of the plexiform layers remain relatively unchanged, whereas ganglion cell density decreases, due to retinal stretch (Fig. 3). Cone density decreases markedly during growth (Fig. 4). In parallel with the wider spacing, cones grow larger (Fig. 4). Both growth-related changes reach a plateau at SL > 160 mm. Due to the increase of eye diameter the resolving power increases steeply in fish up to 100 mm SL, despite the decrease in

10.00 -

3.20

0.01

-

1

4

I

I

I

I

J

QlO

25

63

158

398

SL(mm)

Fig. 2. Lens diameter (LD) plotted against standard length (SL) on a bi-logarithmic scale. Symbols: (+I roach; (8) sabre carp; (A) asp; (e) carp; ( x) bream.

386

MONIKAZAUNREITER et al.

I

300

e -SL

(mm)

Fig. 4. Ontogenetic development in roach, and interspecific comparison of photopic system parameters. All plotted against standard length (SL). (A-A) cone area in pm’; (m---W) resolvmg power in lines per degree of visual angle; (+-.-+) cone density per mm*.

cone density. In roach larger than 100 mm, RP still increases slightly (Fig. 4). Rods are not present in hatchlings, they appear within the first 3 days of life (see Raymond-Johns, 1982 for goldfish). Rod density increases steeply in larvae and juveniles and is maintained stable in specimens larger than 50-70 mm (Fig. 5). This means that rods are added at a high rate and the total number of rods increases throughout the life of the fish. Due to this increase, the ratio of rods to cones and necessarily the convergence of photoreceptors towards ganglion cells also increase life-long (Fig. 5). Despite the marked changes in cone receptor size and densities during growth, the regionalization of the retina is similar in juvenile and adult roaches (Fig. 6a, b). Based on cone densities, two acute zones are present, a prominent one in the dorso-temporal region, a second, less pronounced in the nasal retina. Ratios of cone densities and of resolving power between the acute zones and the retinal periphery remain relatively constant from juvenile to adult roach. Interspecijk

comparisons

Adult eye sizes and lens diameters are markedly different in the five investigated

species (Fig. 2). Sabre carp have the largest eyes, followed by bream, asp, roach and carp, respectively. Carp and sabre carp have the smallest cones, asp and bream the largest, adult roach is intermediary in cone size (Fig. 4). Cone densities are similar in all species, with slightly higher values in carp and sabre carp (Fig. 4), therefore eye size is the major determinant for resolving power. Not surprisingly the highest RP values are found in sabre carp, followed by bream, carp, asp and roach, respectively (Fig. 4). Rod density is very high in sabre carp, high in bream, intermediary in carp and roach, and low in asp. Therefore the rodxone ratio is high in sabre carp and bream, intermediary in roach, and low in carp and asp (Fig. 5). The convergence of photoreceptors towards ganglion cells is high in sabre carp (which has high cone and high rod densities), intermediary in roach (intermediary values in cone and rod densities) and bream (high rod densities, but slightly lower cone densities), and low in carp and asp (due to the low rod densities of these two species) (Fig. 5). All species show the same basic pattern of retina1 regionalization. There are two zones

Fig. 3. Cross sections through larval (a, SL-7 mm) and adult (b, SL = 230 mm) roach retinae showing changes in relative thickness of layers and nuclear densities with growth. (1) Pigment epithelium and photoreceptor layer; (2) outer nuclear layer; (3) outer plexiform layer; (4) inner nuclear layer; (5) inner plexiform layer; (6) ganglion cell layer; (7) nerve fibre layer. Scale bar: IOOpm.

387

a dorsal

temporal

nasal

ventral

Fig. 7. Micrographs of retinal tangential sections, all from historesin-embedded material, sectioned at 3 pm. Lines indicate row patterns, only present in roach (b) and bream (d). (a) The black square marks nasal retinal region where all micrographs are from. (b) Roach; (c) carp; (d) bream; (e) asp; (f) sabre carp. Scale bar: 20pm.

388

Retinal morphology of cyprinid fishes

389

n

16 40

14 12 la 8 6

-20

‘SL (mm) Fig. 5. Ontogenetic development in roach, and interspecific comparison of scotopic system parameters. All plotted against standard length (SL). (0-a) rod density per mm*; (A---A) ratio rodsxones: (m...m) convergence of photoreceptors towards ganglion cells.

of high cone densities (Fig. 6). The more prominent one is situated dorso-temporally in roach and carp, medio-temporally in bream, and ventro-temporally in asp and sabre carp, indicating differences in directions of the major optical axis. A second zone is always located in the nasal region of the retina. In roach and carp it is located at the retinal equator, in bream, asp and sabre carp it is situated to the dorsal side of this line. The degree of retinal regionalization can be judged from the quotient of cone densities in the high acuity zones and in the periphery. Asp shows the most pronounced regionalization, cone densities being 3.3 times higher in the acute zones compared to the periphery, followed by bream (3 times higher), sabre carp (2.2 x ), adult roach (2.1 x ), carp (1.8 x ) and juvenile roach (1.7 x ). The presence of high acuity zones and the degree of regionalization has been related to life style particularly with the fixation of prey by other authors (Collin & Pettigrew, 1988a, b). Engstrom (1960) described row patterns in roach and bream, where rows of unequal double cones alternate with rows of single cones. The two halves of double cones stain differently, making it easy to visualize the alternating

arrangement of the double cones (Fig. 7b). We found a distinct row pattern in roach (Fig. 7b) and in bream (Fig. 7d), whereas cone distribution was irregular in the other species (Fig. 7c, e, f). DISCUSSION

Ontogeny The eyes of larval and early juvenile fishes are relatively large and grow fast (Fig. 2). This is related to the need of these tiny, mostly planktivorous vertebrates for a good resolving power, which depends on eye size and receptor density (Blaxter, 1975; Otten, 1981; Tamura & Wisby, 1963; Van der Meer & Anker, 1984). It has indeed been shown that eye size correlates with prey capture success (Li, Wetterer & Hairston, 1985; Meyer, 1986). As compared to the adults, larval retinae are very small and are tightly packed with small cones (Blaxter, 1975). Rods are mostly lacking at these early stages of life history (Raymond-Johns, 1982). Similar to most other larval fishes (Blaxter, 1975), cyprinids are visual feeders at high light levels. They need acute vision, particularly as other senses are largely immature (Brandstatter & Kotrschal, 1989). The gradual change to

MONIKA ZAUNREIIER

et al.

Fig. 6. Isodensity of plots of cones (bold numbers), with values of resolving power (light numbers), showing retinal regionalization. Left eyes of: (a) juvenile roach; (b) adult roach; (c) carp; (d) bream; (e) asp; (f) sabre carp. Each line represents a difference of 1000 cones per mm2, except in (a) where it means a difference of 2000 cones per mm*. N: nasal, T: temporal.

Retinal morphology of cyprinid fishes

twilight- and night-activity, to deeper water habitats (Mark, Hofer dz Wieser, 1987), and the shifts in diet composition (Mark et al., 1987) observed in juvenile fishes may be related to the characteristic growth-changes in retinal morphology (Ali, 1964; Blaxter & Staines, 1970; Biihlert, 1979; Fernald, 1985; Guma’a, 1982; Kotrschal et al., 1990; Raymond-Johns, 1981; Sandy & Blaxter, 1980; Wagner, 1974). The new formation and lifelong addition of rods may lead to a continuous increase in scotopic sensitivity and to more complex visual skills, such as movement and shape detection (Blaxter, 1975). In parallel with the increase of photopic sensitivity caused by the increase in cone size, photopic resolving power improves during growth, since the number of cones per visual angle increases steadily (Otten, 1981). Whether acuity increases by an increasing order in cone arrangement, is one of many open questions on the functional significance of growth-related shifts in retinal morphology (Fernald, 1981). In roach the typical row pattern could only be found in late juveniles and adults, although Ahlbert (1976) described a square mosaic for many teleost larvae. Simultaneous with the visual development, other sensory systems, such as gustation and mechanoreception may become more elaborate, as roach hatchlings show large and differentiated optic lobes, whereas other primary sensory brain regions are still undifferentiated (Brandstltter & Kotrschal, 1989). Negative allometric growth of the optic tectum combined with the late differentiation and outgrowth of primary sensory brainstem centres for gustation and octave-lateralis (Brandstatter & Kotrschal, 1989, 1990) lead to a decrease in the visual dominance during the life history. In summary these morphological results indicate continual improvements in the growing teleost visual system towards higher acuity, resolving power and sensitivity. Interspeel&

variation

Goldfish as the primary model in vision research has been used to define the cypriniform visual morphology (Northcutt & Wullimann, 1988). However, variety of sensory systems, particularly the visual sense, within cyprinids is relatively unknown, so it is difficult to judge whether the goldfish is really a representative cyprinid species. With respect to brain morphology this species seems to be close to the common carp (H. Junger, unpublished data),

391

both showing taste rather than visual sensory specializations (Kotrschal et al., 1990). Thus the generalized roach seems superior to goldfish as a research model for cyprinid sensory systems. The omnivorous roach proved to be intermediary in most retinal parameters (cone size, cone density, rod density, convergence), and has a low degree of regionalization. The obvious lack of specialized visual skills (i.e. high focussing, RP, movement detection) correlates with an omnivorous feeding habit (Brabrand, 1985). As a whole, roach possess moderately developed photopic and scotopic systems, the low RP values might be compensated by the regular cone arrangement (Fig. 7b), which should enhance colour vision (Levine & MacNicol, 1982; Marc & Sperling, 1976) and improve acuity (Fernald, 1981). The roach retina certainly contains the specific ultraviolet visual pigment (Douglas, 1986) which should lead to a further improvement of the photopic system. Asp as a pursuit hunting piscivore (Ladiges & Vogt, 1965) with a generalized brain, may be considered as visually specialized. It has low rod density, but large, hightly sensitive cones (Fig. 7e) which are loosely packed and irregularly arranged. This means that asp have a rather low RP as compared with other species. On the other hand it shows the highest degree of regionalisation among the species considered. There are two major visual axes: one rostro-dorsal, which is presumably important in feeding, since these fish prey mostly on bleak (Alburnus albumus), attacking from below; the second caudo-ventral axis may be used in other inter- and intraspecific contacts as in the other considered species. Ito and Murakami (1984) described similar high density zones in Navodon, as did Collin and Pettigrew (1988a) in Cephalophofis miniatus. In its optic tract the asp shows the highest proportion (35%) of large fibres corresponding to large ganglion cells within the retina (Kotrschal et al., 1990). Also, asp show the lowest convergence values of all investigated species. Thus we suggest that the retinal characteristics of asp may indicate specialized movement detection. Large, sensitive cones may have been used instead of rods as the major receptors of the asp visual system, since cones provide superior resolution and are faster than rods with respect to “primary events” (measured by flicker fusion experiments: Ali & Klyne, 1985).

392

MONIKAZAUNREITER et al.

The bream with its advanced generalized (abramine) brain type is a benthivore, which may switch to plankton feeding, probably depending on prey density (Ladiges & Vogt, 1965; Lammens, Geursen & McGillavry, 1987). It shows a relatively high rod density, large, sensitive cones, which are tighly packed in a regular row pattern (Fig. 7d), resulting in high sensitivity and high photopic resolving power. Regionalization is not as pronounced as in asp, but still with acute zones in positions similar to asp. The photopic as well as the scotopic system of bream seems to be well equipped for living in low light levels, which are met in the midwater habitats this species usually inhabits. Common carp is a representative of the chemosensory brain type, and possesses enhanced gustation (Sibbing & Uribe, 1985; Kotrschal et al., 1990). Its feeding is almost exclusively benthivorous. Rod density is intermediary compared to other species, and the small cones are tightly packed. Due to the relatively small eyes RP is lower than cone density might indicate. Convergence is low, so is the degree of regionalization. It seems as if carp is able to use its well developed photopic system at higher light levels, whereas the less developed scotopic system, used at low light levels, might be compensated by its well developed taste system (Sibbing & Uribe, 1985). The retina of sabre carp, with its octavolateralis brain, is characterized by a high rod density, whereas the tightly packed cones are small and may thus be low in sensitivity. RP values are highest in this species, so is convergence. The main visual axes are the same as in asp. Sabre carp feeds on insects from the water surface (Ladiges & Vogt, 1965; A. Herzig, personal communication), probably utilizing contrast, and on large planktonic items. High photopic resolution, a sensitive scotopic system (high convergence), and a well developed lateral line system characterizes this species as a specialized surface-dweller (Bleckmann, 1988; Bleckmann & Wilcox, 1988). The degree of regionalization is not only related to the type of prey, but to life style in general. Compared to day-active reef fishes (Collin & Pettigrew, 1988a, b), the regionalization of the day-, crepuscularand even night-active cyprinids is relatively moderate. However, even within these cyprinids, regionalization scales with life style, being highest in species which aim at individual prey. The general pattern of two acute zones in all species

examined indicates the presence of two major optical axes, a rostra1 and a caudal one. Whether these axes are aimed dorsally or ventrally depends on the position of the species in the water column. Asp and sabre carp may utilize the hue and contrast of prey viewed from below against the water surface and their major visual axis is orientated accordingly. In the more benthivorous species, the major visual axis also points towards the bottom. The present investigation revealed a remarkably high morphological variation within the cyprinid retina, which can be correlated to the adult interspecific variation of life styles as well as to ontogenetic niche shifts. This indicates that comparative morphology is a valuable tool for elucidating sensory diversification and for generating functional hypotheses. Acknowledgements-This study was funded by the Fond zur Fdrderung der wissenschaftlichen Forschung in t)sterreich (Project no S-35). Permanent support came from the local project coordinator Doz. Dr A. Goldschmid. We are grateful for the help by the Weber family in Loimersdorf and for the enduring field assistance by W. D. Krautgartner. We gratefully acknowledge the donation of laboratory reared roach by Mag. R. Brandstatter and would like to thank him and Dr J. Haslett for critical discussions of the manuscript. R. Hametner and K. Anrather provided photographic aid. REFERENCES Ahlbert, I. B. (1968). The organization of cone cells in the retinae of four teleosts with different feeding habits (Perca jluviatilis L., Lucioperca lucioperca L., Acerina cernus. L. and Coregonus albula L.). Archives of Zoology, 22, 445-181.

Ahlbert, I. B. (1976). Organization of cone cells in the retinae of salmon (Sulmo s&r) and trout (Salmo trutta trutta) in relation to their feeding habits. Acfu Zoologica, 57, 13-35.

Ah, M. A. (1964). Stretching of retina during growth of salmon (Salmo s&r). Growth, 28, 83-89. Ali, M. A. & Hanyu, I. (1963). A comparative study of retinal structure in some fishes from moderately deep waters of the western North Atlantic. Canadian Journal of Zoology, 41, 225-241.

Ah, M. A. & Klyne, M. A. (1985). Vision in vertebrates. New York: Plenum Press. Blaxter, J. H. S. (1975). The eyes of larval fish. In Vision in fishes (Edited by Ali, M. A.), pp. 427-443. New York: Plenum Press. Blaxter, J. H. S. & Staines, M. (1970). Pure-cone retinae and retinomotor responses in larvel teleosts. Journal of the Marine Biology Association, U.K., 50, 449-460.

Bleckmann, H. (1988). Prey identification and prey localization in surface-feeding fish and fishing spiders. In Atema, J., Fay, R. R., Popper, A. N. & Tavolga, W. N. (Eds.), Sensory biology of aquatic animals (pp. 619-642). New York: Springer. Bleckmann, H. & Wilcox, R. S. (1988). Surface wave reception in invertebrates and vertebrates. In Atema, J.,

Retinal morphology of cyprinid fishes Fay, R. R., Popper, A. N. 8c Tavolga, W. N. (Eds.), Sensory biology of aquatic animals (pp. 642464). New York: Springer. Bohlert, G. (1978). Intraspecific evidence for the function of single and double cones in the teleost retina. Science, 202, 309-3 11. Bohlert, G. W. (1979). Retinal development in postlarval through juvenile Sebastes diploproa: Adaptations to a changing photic environment. Revue Canadienne de Biologie, 38, 265-280.

Brabrand, A. (1985). Food of roach (Rutilus rutilus) and ide (LeucLcus idus): Significance of diet shifts for interspecific competition in omnivorous fishes. dkologia, 66, 461467. Brandstatter, R. & Kotrschal, K. (1989). Life history of roach, Rutilus rutilus (Cyprinidae, Teleostei). A qualitative and quantitative study on the development of sensory brain areas. Brain Behaviour and Evolution, 34, 3542. Brandstatter, R. & Kotrschal, K. (1990). Brain growth patterns in four european cyprinid fishes (Cyprinidae, Teleostei), roach (Rutilus rutilus), bream (Abramis brama), common carp (Cyprinus carpio) and sabre carp (Pelecus cultratus). Brain Behaviour and Evolution, 35, 195-211.

Collin, S. P. & Pettigrew, J. D. (1988a). Retinal topography in reef teleosts. I. Some species with well-developed areae but poorly developed streaks. Brain Behaviour and Evolution, 31, 269-282.

Collin, S. P. & Pettigrew, J. D. (1988b). Retinal topography in reef teleosts. II. Some species with prominent horizontal streaks and high-density area. Brain Behaviour and Evolution, 31, 283-295.

Douglas, R. H. (1986). Photopic spectral sensitivity of a teleost fish, the roach (Rutilus rutilus), with special reference to its ultraviolet sensitivity. Journal of Comparative Physiology A, 159, 415-421.

Engstriim, K. (1960). Cone types and cone arrangement in the retinae of some cyprinids. Acta Zoologica, 41, 217-295.

Engstriim, K. (1963a). Cone types and cone arrangement in teleost retinae. Acta Zoologica, 44, 179-243. Engstriim, K. (1963b). Structure, organization and ultrastructure of the visual cells in the teleost family Labridae. Acta Zoologica, 44, 141. Femald, R. D. (1981). Chromatic organization of a cichhd fish retina. Vision Research, 21, 1749-1753. Femald, R. D. (1985). Growth of the teleost eye: Novel solutions to complex constraints. Environmental Biology of Fishes, 17, 113-123.

Guma’a, S. A. (1982). Retinal development and retinomotor responses in perch Perca jluviatilis L. Journal of Fish Biology, 20, 611618. Henderson, M. A. & Northcote, T. G. (1988). Retinal structure of sympatric and allopatric population of cut-throat trout (Salmo clarki clarki) and dolly varden char (Salvelinus malma) in relation to their spatial distribution. Canadian Journal of Fisheries and Aquatic Sciences, 45, 1321-1326.

Ito, H. & Murakami, T. (1984). Retinal ganglion cells in two teleost species Sebasticus marmoratus and Navodon modestus. Journal of Comparative Neurology, 229, 80-96.

Kotrschal, K. & Junger, H. (1988). Patterns of brain morphology in mid-European cyprinidae (Pisces, Teleostei): A quantitative histological study. Journal fur Hirnforschung,

29, 341-352.

393

Kotrschal, K., Brandstitter, R., Gomahr, A., Junger, H., Palzenberger, M. & Zaunreiter, M. (1990). Brain and sensory systems. In Winfield, I. & Nelson, J. S. @is.), The biology of cyprinids. London: Chapman & Hall. Ladiges, W. & Vogt, D. (1965). Die StiBwasserjsche Europas (p. 299). Hamburg & Berlin: Parey. Lammens, E. H. R. R., Geursen, J. & McGillavry, P. J. (1987). Diet shifts, feeding efficiency and co-existence of bream (Abramis brama), roach (Rutilis rutilus) and white bream (Blicca bj&kna) in hypertrophic lakes. Proceedings of the V Congress of European Ichthyologists, Stockholm,

pp. 153-162. Levine, J. S. & MacNicol, E. F. (1982). Colour vision in fishes. Scientific Amercian, 246, 108-l 17. Li, K. T., Wetterer, J. K. & Hairston, N. G. (1985). Fish size, visual resolution and prey selectivity. Ecology, 66, 1729-1735.

Locket, N. A. (1970). Deep-sea fish retinas. British Medical Bulletin, 26, 107-l

11.

Locket, N. A. (1980). Variation of architecture with size in the multiplebank retina of a deep-sea teleost, Chauliodus sloani. Proceedings of the Royal Society, London B, 208, 223-242.

Lyall, A. H. (1957). Cone arrangements in teleost retinae. Quarterly Journal of Microscopic Science, 98, 189-201.

Marc, R. E. & Sperling, H. G. (1976). The chromatic organization of the goldfish cone mosaic. Vision Research, 16, 1211-1224.

Mark, W., Hofer, R. & Wieser, W. (1987). Diet spectra and resource partitioning in the larvae and juveniles of 3 species and 6 cohorts of cyprinids from a subalpine lake. bkologie,

71, 388-396.

McEwan, M. R. (1938). A comparison of the retinae of the mormyrids with that of various other teleosts. Acta Zoologica, 19, 427465.

Mednick, A. S. & Springer, A. D. (1986). The goldfish retina has an area centralis. Anatomical Record, 214, 84A85A. Menezes, N. A., Wagner, H. J. & Ali, M. A. (1981). Retinal adaptations in fishes from a floodplain environment in the central Amazon basin. Revue Canadienne de Biologie, 40, 111-132.

Meyer, A. (1986). Changes in behaviour with increasing experience with a novel prey in fry of the Central American cichlid, Cichlasoma managuense (Teleostei: Cichlidae). Behauiour, 98, 145-167. Muntz, W. R. A. (1982). Visual adaptations to different light environments in amazonian fishes. Revue Canadienne de Biologie Experimentale,

41, 35-46.

Nelson, J. S. (1984). Fishes of the world (p. 523). New York: Wiley. Neumeyer, C. (1985). An ultraviolet receptor as a fourth receptor type in goldfish colour vision. Naturwissenschaften, 72, 162-163.

Northcutt, R. D. & Wullimann, M. F. (1988). The visual system in teleost fishes: Morphological patterns and trends. In Atema, J., Fay, R. R., Popper, A. N. 8~ Tavolga, W. N. (Eds.), Sensory biology of aquatic animals (pp. 515-552). New York: Springer. O’Connell, C. P. (1963). The structure of the eye of Sardinops caerulea, Engraulis mordax, and four other pelagic marine teleosts. Journal of Morphology, 113, 287-329. Otten, E. (1981). Vision during growth of a generalized Haplochromis species: H. elegans Trewawas 1933 (Pisces, Cichlidae). Netherlands Journal of Zoology, 31, 65&700.

MONIKAZAIJNREITER et al.

394

Raymond-Johns,

P. A. (1981). Growth

of fish retinae.

American Journal of Zoology, 21, 447-458.

Raymond-Johns, P. A. (1982). Formation of photoreceptors in larval and adult goldfish. Journal of Neuroscience, 2, 178-198. Raymond, P. A. & Rivlin, P. K. (1987). Germinal cells in the goldfish retina that produce rod photoreceptors. Developmental Biology, 122, 120-l 38.

Sandy, J. M. & Blaxter, J. H. S. (1980). A study on retinal development in larval herring and sole. Journal of the Marine Biology Association, U.K., 60, 59-71. Schiemer, F. (1985). Die Bedeutung der Augewiisser als Schutzzonen fiir die Fischfauna. &terreichische Wasserwirtschaft, 37, 239-245.

Schiemer, F. 8c Hofer, R. (1983). A contribution to the ecology of the fish fauna of the Parakrama Samudra Reservoir. In Schiemer, F. (Ed.), Lhnnology of Parakrama Sam&a, Sri Lanka (pp. 135-154). The Hague: Junk Publishers. Scholes, J. H. (1975). Colour receptors, and their synaptic connexions, in the retina of a cyprinid fish. Philosophical Transactions of the Royal Society B, 270, 61-l 18.

Sibbing, F. A. & Uribe, R. (1985). Regional specialization in the oropharyngeal wall and food processing in the carp (Cyprinus carpio L.). Netherlands Journal of Zoology, 35, 377-422.

Stell, W. K. & Harosi, F. I. (1976). Cone structure and visual pigment content in the retina of the goldfish. vision Research, 16, 647657.

Tamura, T. & Wisby, W. J. (1963). The visual sense of pelagic fishes especially the visual axis and accomodation.

BuNetin of Marine Science in the 433-448.

Gulfof Caribbean, I3.

Van der Meer, H. J. & Anker, G. C. (1984). Retinal resolving power and sensitivity of the photopic system in seven haplochromine species (Teleostei, Cichlidae). NetherlancIs Journal of Zoology, 34, 197-209.

Wagner, H. J. (1972). Vergleichende Untersuchungen iiber das Muster der Sehzellen und Horizontalen in der Teleostier-Retina (Pisces). Zeitschrft fir Morphologie und okologie der Tiere, 72, 77-130.

Wagner, H. J. (1974). Die Entwicklung der Netzhaut von Nannacara anomala (Regan) (Cichlidae, Teleostei) mit besonderer Beriicksichtigung regionaler Differenzierungsunterschiede. Zeitschrtytfiir Morphologie und dkologie der Tiere, 79, 113-131. Wagner, H. J. (1975). Comparative analysis of the patterns of receptor and horizontal cells in teleost fishes. In Ali, M. A. (Ed.), Vision in fishes (pp. 517-524). New York: Plenum Press. Wagner, H. J., Menezes, N. A. & Ali, M. A. (1976). Retinal adaptations in some Brazilian tide pool fishes (Teleostei). Zoomorphologie,

83, 209-226.

Williamson, M. & Keast, A. (1988). Retinal structure relative to feeding in the rock bass (Ambloplites rupestris) and bluegill (Lepomis macrochirus). Canadian Journal of Zoology, 66, 2840-2846.

Zaunreiter, M. & Kotrschal, K. (1989). Shifting retinal parameters during growth in roach (Rutilus rutilus, Cyprinidae, Teleostei). In Elsner, N. & Singer, W. (Eds.), Dynamics and plasticity in neuronal systems (p. 192).

Stuttgart: Thieme.