Disorders of the eye in finfish

Annud Printed

Rev. ofFish Diseases, in the USA. All rights

pp. 95-117, reserved.

1991

DISORDERS

Copyright

0

0959.8030/91 $3.00 + .oo 1991 Pergamon Press plc

OF THE EYE IN FINFISH William J. Hargis, Jr.

Virginia Institute of Marine Science, School of Marine Science, The College of William and Mary, Gloucester Point, VA 23062, USA

Abstract. As fish have been brought into confinement for display and culture, eye diseases have often caused difficulties, sometimes major. Types and possible etiological factors vary. All eyeball (orb) parts and attached organs and tissues (adnexa) are affected. Most common are exophthalmos (pop-eye), cataracts, keratopathy (several cornea1 lesions), various retinopathies, and uveitis (choroid and iris system lesions). Less frequent in cultured or feral fishes are: aphakia (no lens); choroid gland disease; cyclopia; edema of various tissues-including the lens; endophthalmos (sunken-eye); hyperemia of all parts; microphthalmos (small-eye); neoplasia of cornea, retina, and other parts; and others. These lesions may result from poor water quality, including gas imbalances (causing exophthalmos), toxicants (cataract, hyperemia, keratitis, and retinitis), low temperatures and osmotic imbalances (cataract); nutritional deficiencies (cataract, corneal, and retinal diseases); parasitemias (exophthalmos, cataract, keratitis, etc.); radiation damage (cataract, keratitis); trauma of careless handling; and injuries from unsafe culture systems. All conditions are exacerbated by stresses associated with culture, including overcrowding and aggressive behavior. Immunological deficiencies and genetic factors are also involved. In display aquaria, hatcheries, and nurseries, eye disease may not be fatal but often affects growth and is unsightly. Further, cataracts can indicate serious nutritional problems leading to other diseases. Exophthalmos, ocular hyperemia, cloudy corneas, cataracts, and granular and inflamed eye tissues may signal unfavorable water supply or parasitemia resulting from poor sanitation. Unthriftiness and deaths may result. Chances of survival or responsive behavior of released vision-impaired fish are markedly reduced and purposes of culture and release programs negated. Also, buyers, believing they reflect poor product quality, may reject animals with abnormal-appearing eyes. Whichever occurs, stock, biomass, time, and monetary losses can be significant. Eye diseases of fish, their possible causes, significance, and prevention or treatment, if any, are described and discussed. Keywords. Eye-disease, Fish aquaculture, Feral fish populations, Etiology, Medicine

itself or as a sign of other syndromes, is recognized as a factor in the general health and survival of finfish and as affecting the immediate or ultimate success of aquacultural activities (4,5). This review, intended to complement those of Dukes (4) and Wilcox and Dukes (6) on eye disease in general, and Hughes (5) on nutritional diseases in salmonids, is devoted to diseases of teleost ocular tissues, especially those under aquaculture conditions. Also included is information on results of experiments or observations on feral fish species of economical or ecological importance likely to be of significance in finfish aquaculture or of interest to culturists even though they may not be currently under culture.

INTRODUCTION Many studies, some published as early as 1744 (l), have been devoted to effects of infectious and noninfectious diseases on fish health in general, and on certain organs like the integument, including skin, fins and gills, liver, pancreas, kidneys, and gastrointestinal tract in particular. In spite of

the fact that Marking (2) stated that eye disease in fisheries has been recognized and recorded since the late 1800s or early 19OOs,specific attention has rarely been given to effects of disease on ocular tissues or, where mention has occurred, it has only been in passing or as an associated effect of various other maladies. Fortunately, neglect of finfish eye disease is changing as the significance of ocular tissues as readily visible indicators of environmental stress, intoxication, or infection (3), and of the concomitant effects of these factors on eyes have been recognized. Increasingly, eye disease, in

THE TELEOST EYE: MORPHOLOGY NORMAL HISTOLOGY

AND

Finfish have adapted successfully to occupy all but the most inhospitable fresh, brackish, and saltwaters of earth and inhabit every conceivable ecological niche in those waters. Since conditions of

Contribution No. 1649 of the Virginia Institute of Marine Science. 95

W. J. Hargis, Jr.

96

available light and requirements for image reception and interpretation vary so much in some of the habitats occupied, fish eyes have evolved into many shapes and developed different light response capabilities. A number of eye designs and arrangements are bizarre, such as the tubular telescope-like eyes of Opisthoproctus soleatus or Gigantura chuni or the stalked eyes of larvae of Zdiacanthusa fasciola, all of which are deep sea fish. In some species residing in continuous darkness, such as abyssal waters and caves, eyes are much reduced, or even lacking. Eyes of the foureyed fish, Anableps anableps, which lives at the water-air interface, are adapted to both media. Eyes of pelagic and benthic fish differ in location, orientation, sensitivity, and possession of accessory structures such as adipose lids and luminescent organs. Despite variations in ocular structural detail among fish species, the basic ocular features of most living teleosts are essentially similar morphologically and physiologically. Consequently, findings regarding the ocular diseases, their impacts, and possible preventatives or cures made on one species or group may be readily transferred to others. The basic plan of the eyeball, orbit, and adnexa (accessory structures such as muscles and ligaments

attached to the orb) seen in higher vertebrates applies to finfish. Most teleost eyes face laterally on each side of the head, like those of many higher vertebrates, and not forwardly, as those of man and other primates. Being laterally placed, the eyes of many fish “see” independently, and, in many species, are capable of independent movement and, undoubtedly, focus. Contrary to the recent contention of Wilcox and Dukes (6), a number of teleosts can and do move their eyeballs independent of head or whole body movements to change their field of view, as Fernald (7) reported. The observations of Fernald (7) on the movement of the eyes in the African cichlid fish, Haplochromis burtoni, have been confirmed by recent observations of independent

eye movements

of the eyes of the look-

down, Selene vomer, and other species in the aquarium of our institute (Hargis, unpublished). However, a number of teleosts do move their entire bodies to alter the field(s) of view. Figure 1, a diagrammatic representation of a longitudinal (or sagittal) section of a typical teleost eye, Figure 2, a diagram of a sagittal section of the lens, and Figure 3, a sagittal section of a normal teleost eye, will serve to supply the essentials of teleost ocular morphology required to understand the organs and tissues affected by the diseases dis-

Dorsal

Posterior chamber w. vitreous humor

Lens retractor muscle

Ventral

Fig. 1. Diagrammatic representation of a teleost eye showing essential anatomical features. Diagram contains both a choroid gland, or choroid rete, and falciform process. Choroid glands and pseudobranchs usually accompany one another in the same species. Those without pseudobranchs have no choroid gland. Most teleosts have a falciform process of greater or lesser prominence that contains blood vessels, presumably serving to nourish interior “organs” and tissues. Species without the falciform process, or only vestigial, distal remnants the surface or fundus of the retina, presumably serving the same function.

thereof,

have hyaloid

blood vessels on

Disorders of fish eyes

91

Fig. 2. Diagrammatic representation of typical teleost lens. Lens is seated mostly in the posterior, or vitreous, chamber. It frequently protrudes significantly into the anterior (aqueous) chamber, sometimes almost touching the cornea. Epithelial cell layer mitotically active, producing budding lens fibers at nuclear bow area. New lens fibers elongate and push anteriorly and posteriorly under the epithelial layer and capsule, respectively. Fiber cell nuclei eventually “fade away” and lens fibers become “crystalline.” New cortical (outermost) fiber cells overlay nuclear (central or deeper) ones like layers of an onion. Capsule, or basement membrane, is produced and maintained by epithelial cells.

cussed below. The comprehensive treatise by Walls (8) on the development and adaptive radiation of vertebrate eyes, first published in 1942, remains the best and most comprehensive report on the evolution, embryology, morphology, and function of the teleost and elasmobranch eye available. Recently Wilcox and Dukes (6) published their very useful paper on the morphology and systemic pathology of the teleost eye with some emphasis on salmonids. Both volumes should be consulted by anyone wishing greater detail than presented here on these topics. While the basic plan of the higher vertebrate eye applies to finfish, there are certain differences of form and, perhaps, function that should be noted. Most fish eyeballs (orbs) are not spherical or globular in shape but are elongated in the horizontal plane, compressed in the vertical, and often narrowed horizontally (i.e. front to back of eye, or lateromedially). The long axis is oriented fore and aft to the body of the fish (truly anterioposteriorly). They are an oblate-spheroid, shaped somewhat like a North American football with blunt, rounded ends. As indicated above, a large majority of teleost eyes face laterally; very few open dorsally or anteriorly. The lens often protrudes through the pupil into the anterior chambers thus providing the

wide-angle vision so well exemplified by the wideangle, or “fish-eye,” photographic lens. In some fish a binocular field of view is possible regularly, or only at times, depending on orientation of the eyes, degree of interference of the snout, and positioning of the lens in the eyeball. In most teleost eyes, “anterior” is really lateral; “posterior” is medial. The equator of the eyeball is not circular but oval in outline. For these reasons application of mammalian terms to fish eyeballs, a common practice, must be done with care. In many teleosts the ventral suture of the embryonic optic cup does not close completely. A portion of the choroid may protrude into the vitreous chamber, extending toward the lens. This structure, usually well supplied with blood vessels and often providing attachment for the retractor lentis muscle, is called the falciform process. Prominent in some species and vestigial in others, it can cause diagnostic problems for the unwary pathologist and result in false diagnoses of retinal swellings or other disorders. In species without falciform processes, hyaloid blood vessels traverse the surface of the retina, i.e. the fundus. Most teleost lenses (Figs. 2 and 3) are spherical, or globular. Like that applied to the orb or eyeball, terminology commonly applied to the lens is based

98

W. J. Hargis, Jr.

Fig. 3. Comparison section (sagittal) of a normal eye of the sciaenid fish, the spot (Leiostomusxanthurus) showing normal choroid gland (G), retina (R) and lens (L). The small anteriorly located area of bulging, “loose” lens epithelium and capsule is a processing artifact. (PAS stain).

largely on human ophthalmology. As indicated above, in most fish species the eyeball “opens” laterally and not anteriorly. Therefore, terminology based upon mammalian orientation can cause confusion in fish lens morphology. Because the fish lens is spherical and not “lenticular” or biconvex as

in man, the morphological terms developed for human lenses must be applied and interpreted with caution as well. For example, in most fish lenses the “anterior pole” is really lateral, the “posterior pole” is really medial, and the equator is not the edge of a biconvex “disk” (where the ciliary muscles attach, as in the human lens) but merely the circumference of a sphere, an imaginary line around the lens that is halfway between the poles and usually oriented anterioposteriorly. There is no ring of ciliary muscles per se and the shape of the spherical lens cannot be changed as can human lenses for purposes of focus. Instead the whole lens must be moved.

The lens is surrounded by a capsule that is usually thickest anteriorly and thinnest posteriorly (Fig. 2). Immediately under the capsule is a single layer of epithelial cells. This growing, dividing epithelium produces the fiber cells at the nuclear bow area of the lens which elongate, move, lose their nuclei and eventually become completely “crystalline.” Young, recently generated fiber cells grow around older ones like the “rings” or layers of an onion. The youngest fiber cells make up the cortex of the lens, the oldest ones the central nucleus. The process apparently continues throughout life in most teleosts but slows with advancing age, as in mammals. The different elements of the lens are often involved in cataract formation and are altered in the process. Some forms of cataract involve only the lens fiber cells and appear as opacities around sutures (at the junctions of the ends of the lens fibers). This condition apparently occurs in ocean-run salmonids as affected migrating smolts move from low salinity natal fresh water rivers to higher salinity ocean waters. This type of cataract, apparently caused by temporary osmotic imbalance, is reversible in some stages, as will be discussed below. Most other types of cataract are almost undoubtedly irreversible. That is, once they develop, the opaque portions of most cataracts resulting from epithelial damage, lens fiber derangement, coloration, or vacuolization will always remain even if causes are eliminated and normal fiber-cell creation is resumed-if it, indeed, can be. Such cataracts may involve hyperplasia of the epithelium, production of abnormal epithelial cells or abnormal cortical or nuclear fibers, discolored crystalline fiber cells, liquefaction of cortex and nucleus, vacuolizations in or between all types of cells, etc. Where the entire epithelium, i.e. all of the epithelial cell layer (or probably even a significant portion of it) is damaged, reversal has to be impossible since the epithelial cells are the only lens components known to be able to replace themselves and initiate resumption of normal fiber cell production. Indeed, it is most likely that disruption of even small but critical areas of the epithelial cell layer important to further fiber cell development, results in irreversible damage. Unlike that of higher vertebrates, the iris in most teleosts cannot be varied to change pupillary diameter and reduce light entry. Indeed, in most sections of sciaenid eyes examined at our institute (Hargis, unpublished data Fig. 3) and in some photographs taken through the slit biomicroscope, the

Disorders of fish eyes

Fig. 4. Series of photographs of lake trout (Salvelinus mayucush) eyes showing development of cataracts normal eye (A), to early crescent-like opacification cortex (B), to general but still faint, homogeneous ity (C), Light transmission in C is reduced by about Cataract from nutritional imbalances.

na-

from in the opac25%.

iris does not appear to separate anterior and pos-

terior chambers completely (Figs. 4 and 5). What influence this incomplete separation may have on the aqueous and vitreous humors and on movement of materials within and between the chambers is unknown. In many fish, control of light entering the posterior chamber is accomplished by alteration of iridiophores in the iris, which reduce light transmission. Some species, however, are able to modify pupil shape to control light and field of view. Also, some have accessory structures serving to control internal light intensity, such as tapetal layers. Between the sclera and the choroid coat or dark layer surrounding the retina and extending into the iris, in the “space” called by some the choroid space, the blood vessels supplying the eyeball develop, by undergoing extreme convolution and recurving, a rete of capillaries (variously called the

99

Fig. 5. Continuing series of lake trout (Salvelinus numashowing further development of cataract, the lens becomes increasingly opaque (A and B) until light transmission is reduced to 0% in (C). All exposures made through a slit biomicroscope. (Figs. 4 and 5 taken from 25 by permission).

yu~h)

choroid gland, choroid rete, or ocular rete mirabile) that is interposed between the central and peripheral (choroid or hyaloid) blood vessels. This uniquely teleost structure often loops around the optic nerve like a horseshoe. According to existing reports the choroid rete occurs only in those species with pseudobranchs. It is variations such as the lack of a Canal of Schlemm with substitution of other mechanisms for maintenance of hydraulic balance in the eyeball that may account for the lack of reports of glaucoma in teleost eyes as Wilcox and Dukes (6) indicate. The interconnecting chambers resulting from the nonocclusive iris may be involved as well. Also, the choroid gland and persistence of hyaloid blood vessels reaching toward the lens in some finfish may provide pathways for plasma-borne materials, beneficial and deleterious alike, to reach the lens, directly or indirectly (or in greater amounts) than

W. J. Hargis, Jr.

100

simply via the aqueous or vitreous humors as is postulated for mammals. INTERACTIONS

BETWEEN

AND FUNCTIONS

EYE STRUCTURE

AND DISEASES

Thus, teleost eyes possess certain differences in structure and function, and possibly pathways through which components of the environment, e.g. chemical pollutants, can reach the internal tissues of the teleost eyeball, especially the lens. These must be considered as the several teleost ocular diseases, and their causes, are examined. The few differences noted do not detract seriously from the applicability of many findings on disease effects observed in eyes of mammals to those of fish and vice versa. The extensive research on diseases of mammalian eyes can definitely assist in development of understanding of the pathogenesis of ocular disease in finfish. Like eyes of mammals, finfish eyes are subject to a wide range of disease syndromes and to trauma; however, there are some differences. For example, teleost eyes are generally unlidded, usually protrusive, and otherwise more or less permanently exposed. Consequently, mechanical damage probably happens more frequently to fish eyes than to those of most higher vertebrates, especially under conditions of mass culture as animals brush against container surfaces and each other or are damaged in catching, handling, and transporting activities. In contrast to territorial animals, whose external eye surfaces and lungs are exposed mostly to air and whose food is mostly “dry” when ingested, teleost eye surfaces and branchial chambers are constantly bathed by environmental waters, which are also taken in with their food. Consequently, toxic materials borne by those environmental waters have direct access to the corneal, pseudobranch, gill, and intestinal surfaces, as well as the skinand in full strength. Any toxicant or infectious agent arriving at those surfaces capable of crossing the membranes involved, actively or passively, can gain access to the eye, directly or indirectly. Eyes of most teleost species are necessary for normal development and growth of postembryonic stages even though some fish can survive in aquaria or hatcheries with partial or total blindness, supported by the several other sensory systems useful in locating food and avoiding collision and predation (9). Eye-damaged fish can also survive for some time in the wild, since bilaterally cataractous fish, many of which have other eye diseases as well, are caught regularly in some heavily contam-

inated estuaries (10-12) or near-shore coastal waters (13). Because of the heavy silt and plankton burdens of the waters of many estuaries, fish (or their life stages) living in them must be wellendowed with sense organs adapted to such murky waters; hence, their dependence upon vision is much less than those from clearer waters. Fish inhabiting clear rivers, lakes, lagoons and fjords, and transparent ocean waters are extremely dependent on sight. GENERAL

ASPECTS

OPHTHALMIC

OF TELEOST

DISORDERS

Scientific reports of ocular pathology caused by various pathogens (such as viruses, bacteria, fungi, protozoans, and especially helminths) in feral fishes are numerous. Few deal with eye lesions caused by other diseases. Recently, several reports, including those of research efforts at our institute dealing with wild and laboratory-exposed Sciaenidae (as well as from other families) have discussed eye disease, including cataracts. Some have related those conditions to environmental contaminants (lo-12,14). Such studies are extremely interesting to those concerned with the effects of environmentally induced intoxication or other stress on the health of wild finfish. They may also be of direct interest to aquaculturists as in the recent Exxon Valdez oil spill that, according to media accounts, threatened hatchery-reared or penned salmonids in Prince William Sound off of the northeastern Gulf of Alaska. Among the ocular diseases affecting wild and cultured teleosts are (alphabetically arranged): aphakia (absence of lenses); choroid gland disease; cornea1 cloudiness (mistakenly called cataract by some); cyclopia; edema of many tissues including the whole lens, which may become enlarged and be “abnormally soft and compressible” (15); endophthalmos (sunken eyes); exophthalmos (popeyes); hyperemia (hemorrhages) in different parts of the eye and adnexa, lens opacities (true cataracts of various types); neoplasia of various tissues; nervous tissue abnormalities; and retinal disturbances (Table 1). These pathological conditions may be caused by developmental malfunctions (teratogenesis); nutritional deficiencies; environmental intoxication and other environmental stresses including other aspects of poor water quality, crowding and aggressive behavior; and invasion by viral, bacterial, or fungal organisms, or by protozoan or metazoan parasites (16-35). Several of these diseases may occur in the same individual or population of fishes at the same time. Reduced immune responses are

Z

Epithelium Descemet’s membrane Endothelium

Epithelium

Ulceration of cornea

Cornea1 tumor

continued

Cornea1 epithelium and underlying tissues

Cornea

Eyeball (orb)

Orbital sinuses Adnexa Eyball (orb) Chorid rete Retina

Affected Organs/Tissues

Keratoconus Keratoglobus

Corneopathy/ Keratopathy Keratitis (Bum or dull eye)

Endophthalmos (Sunken-eye)

Exophthalmos @w-eye)

Disease

Growths on epithelium

Edema Inflammation Ulcers

Protruding cornea Irregular outer surface

Opacities Discoloration

Eyeball flattened or sunken

Bubbles in eyes and orbital tissue Protruded eyes Extruded eyes

Signs

Onchorhynchus masou virus

Irradiation damage Mechanical trauma

Irradiation damage Parasitic disease Secondary with worm cataract Mechanical trauma Nutritional imbalances

Trauma Osmotic imbalances Parasitic disease Riboflavin deficiencies

Parasitic disease: hemoprotozoans Intoxication (esp. Cl) Starvation

Environmental gas imbalances Parasitic diseases: Various viruses, bacteria, fungi, protozoans, and digeneans

Causes

Shading: suitable water depth Careful handling

Shading: Suitable water depth Disease prevention Careful handling Smooth-walled containers throughout Water quality control Proper nutrition

Smooth-walled containers Gas balance control Disease prevention

Disease prevention, water quality control

Gas balance control Sanitation Disease prevention Various possible chemical treatments

Prevention/ treatment

Table 1. Lesions of the eye and adnexa in cultured and other teleosts

Experimental infection Probably insignificant in cultured fish

Lesions of cornea commonly reported in cultured fish Blindness Unthriftiness Death

Apparently not common

Most commonly reported ocular disease in captive fishes Death common

Special remarks

26(E)

22,24

6,9,22-24,25(E)

4,6,19-21

4,9

4,6,8,9,16-18

References

Aphakia

Cataract (bum eye, dull eye, cloudy eye)

Lenticulitis (Lens Disease) Enlarged Lens

Vitreous hyperemia

Abnormalities of Humoral Chambers and Contents Aqueous hyperemia

Disease

Entire lens missing

Capsule Epithelium Cortex Nucleus

Entire lens

Vitreous humor Hyaloid blood vessels/Falciform process

Aqueous humor

Affected Organs/Tissues

Nutritional imbalances Intoxication Parasitic invasion (mostly strigeid larvae) Damaging irradiation Trauma Osmotic imbalances Genetic disposition

Teratological malformation Extrusion of lens due to gas bubble disease

Interior of vitreous chamber and fundus, visible through pupil Abnormal pupil

(E)

Opaque lens Swollen or thinned capsule Hyperplastic epithelium (multi-layered) Bladder cells Vacuoles Abnormal fibers Fiber cell lysis Abnormal interdigitations of fiber cells

Intoxication Petroleum hydrocarbons

Intoxication

Hyperemic vitreal chamber Engorged and enlarged falciform blood vessels

Abnormal diameter: Swollen lens

Intoxication

Causes

Hyperemic anterior chamber

Signs

Table 1. Continued

Water quality control

Balanced diet Water quality control Parasite control: prevent access of primary and secondary hosts Shading: suitable water depth Brood stock selection

Water quality control

Water quality control

Water quality control

Prevention/ treatment

Probably insignificant Discard affected individuals or process headless

Probably second most prevalent disease in cultured fish Blindness Unthriftiness Death “Suture cataract” resulting from early short-lived osmotic imbalances, reversible Majority cataracts irreversible

Experimental exposures (E) Same response likely in cultured fish

Special remarks

Hargis and Zwerner, unpublished (F)

4,1 l-13 (all F),l4(E), 15(E),22,24(E),28, 29-3 1 (all E), 32,33,34(E), Hargis and Zwerner, unpublished(F)

15,27(E)

Hargis and Zwerner, unpublished (F)

Hargis and Zwerner, unpublished (F)

References

5

Muscles

Optical nerve

Choroid gland

Inflammation and Granulation

Inflammation Granulation

Enlargement and engorgement Inflammation Disruption

Parasites

Parasites

Intoxication (F) Parasitic disease

Intoxication (F)

Proper sanitation Water quality control

Sanitation Water quality control

Sanitation Water quality control

Water quality control

Exposure to intoxicants (surfactants) Nutritional imbalances Intoxication Gram-negative, septicimea

Water quality control

Water quality, probably more

Water quality control

Intoxication Hypomesius pretiosus surf smelt (E)

Intoxication control

Intoxication

21,35(E)

Carp experimentally exposed to surfactants Also seen in “sekoke carp”

6(F)

603

Probably insignificant in cultured fish Probably significant in cultured fish

11(F)

Common in cases of PAH intoxication

6.1 l(F)

6

31(E)

All retinopathies common in cultured fishes than in literature

Probably more common in fishes than reported

25(E)

6,11(F)

All retinopathies common in cultured fishes than in literature

All retinopathies probably more common in cultured fishes than in literature

(Symbols: E = experimental; F = feral; other disease mostly in cultured species). Special Note: As employed here, the term parasitic disease means all diseases or lesions caused by any biological organism residing in or on the host animal, organ, tissue, or cell.

Diseases of Adnexa

Sclera

Choroid gland disease

Engorgement and enlargement

Capillaries in choroid and iris

White spots Dilated or engorged blood vessels

Hyperaemia Edema Inflammation

Retinal surface Hyaloid vessels

Fundal Disease Diabetic retinopathy

Receptor cells necrotic

Retina thicker than normal

Thinned layers Necrotic cells

Iris Chorid Falciform process

Photoreceptor and ganglia1 layers

Retinal degeneration, Photoreceptor degeneration, Neuronal damage

Uveitis/Choroiditis

Plexiform and ganglial layer Edema

All layers

Retinal swelling

Retinopathy Retinal thinning

104

W. J. Hargis, Jr.

known to be associated with various diseases, including those caused by intoxication. Genetic factors probably influence all ocular diseases. Eye disease can be viewed as a primary-level problem when the eye is the organ first or most severely affected, as in invasion and occupation of the eyeball or its parts by trematode larvae or in nutritional problems, both of which may affect specific portions of the eye solely or most heavily. Cataract, resulting from osmotic imbalances as smolts of various seaward-moving salmonids arrive in the ocean unprepared physiologically to accommodate to the changes in density of environmental waters (36,37), is also a primary-level response. Even in such cases where eyes are most regularly or heavily affected, side effects may be present in other portions of the body. Contrarily, in some diseases other portions of the body may be attacked first (by viruses, bacteria, and protozoa for example) and the eyes may exhibit secondary response. VARIOUS EYE DISEASES AND THEIR CAUSES The general discussion above serves to introduce the more specific aspects of eye disease in relation to commercially important finfishes under culture or capable of being cultured, which constitute the main thrust of this report. Before pursuing the consequences of eye disease in aquaculture and possible preventatives or corrective measures, a brief description of the types of diseases affecting teleosts is in order. As Table 1 indicates, every component of the eye and their tissues may be affected by disease ranging from trauma caused by direct mechanical

damage, with or without subsequent infectious consequences and inflammation, to apparently spontaneous neoplastic growths. All adnexal components are also affected. Exophthalmos

(Figs. 6 and 7)

Exophthalmos manifested as protruding eyeballs or pop-eye (unilateral or bilateral) was considered the most frequently reported ocular disorder by Dukes (4). Aquarists have long recognized exophthalmos, the disease in which the eye swells, becomes too large for the orbit, and protrudes as a possible result of gaseous imbalances in the water, other environmental stress, or parasitically induced disease. Swelling in the tissues of the adnexa, the organs attached to and associated with the eyeball, can cause protrusion of the eyeball as well. In some instances there is little apparent pathological change in the internal tissues of the eyes, themselves. In others, swelling can be such that the eye is completely extruded, lost and subsequently healed over as Van Duijn (9) described in a goldfish (Carassius aura&s). Frequently, gas bubbles appear within tissues of the orb (Fig. 7) or elsewhere in the body (2). In addition to mechanical trauma and oxygen or nitrogen supersaturation, exophthalmos can also result from viral (3) bacterial (3), fungal (38), protozoan, or metazoan infections (4). Endophthalmos Endophthalmos, sunken eyeballs, is common after death but rare in moribund animals. Nonetheless, it does occur (4,9) and appears to be due to intoxication and emaciation.

Fig. 6. Golden grouper (Epenephelus ulexandrina)with acute exophthalmos (gas-bubble disease) caused by gaseous imbalances. Golden grouper is cultured in the middle east for food. (Courtesy, Dr. Mohamed Faisal.)

105

Disorders of fish eyes

‘ellow perch (Percaflavescens) with experimentally-induced exophthalmos, or gas-bubble disease. Side view Fig. dorsal view (bottom). Note bubbles in cornea (white arrows). (Courtesy, Dr. L. L. Marking, National Fish (top) Rese arch Center, U.S. Fish and Wildlife, Department of interior Service, La Crosse, Wisconsin, USA.)

Microphthalmos

Keratopathy

The condition characterized by abnormally small eyes (undersized eyeballs) has apparently been induced in the popular aquarium species zebrafish (Brachydanio rerio) (4). It has been seen in feral fishes as well. A teratogenic abnormality, the cause or causes have apparently not been carefully investigated.

Several lesions, cloudy or opaque cornea, protruding cornea (keratoconus and keratoglobus), and surficial ulcerations, among others, are included in this general disease category. The unsightly condition of cloudy cornea (sometimes mistakenly called cataract), not uncommon in aquarium fishes, detracts from their aesthetic value and obstructs vision. Opacities of the cornea are common in cultured food fishes as well. They frequently accompany other eye lesions, such as lens opacity (true cataract) and hemorrhage of the anterior and vitreous chambers. Causes range from mechanical damage to primary infection as well as indirect consequences of infectious disease. Dietary imbalances and associated factors can

Cyclopia The one-eyed condition has been mentioned as having occurred in a number of abnormal salmonid embryos from one or more New York State hatcheries and perhaps in other fish (4). Obviously a teratogenic disorder, the cause or causes have apparently not been carefully studied.

(keratitis) (Figs. 8 and 9)

106

W. J. Hargis, Jr.

Fig. 8. Young coho salmon (Oncorhynchus kisutch) with acute keratitis (opacity and ulcerations of cornea) related. (Courtesy, Dr. J. C. Hnath, Wolf Lake Hatchery, Fish Pathology Laboratory, Mattawan, Michigan, USA.)

cause various types of keratitis, i.e. cornea1 opacity, keratoconus, and keratoglobus, in salmonids in culture facilities. Hnath et al. (20) reported large-scale occurrences of keratitis (Figs. 8 and 9) in coho salmon (Oncorhynchus kisutch) cultures destined for release into the Great Lakes system to help restore fishery production. Excessive sunlight also causes cornea1 opacities, keratoconus, and ulcerative keratitis as has been shown in lake trout (Salvelinus namuycush) in laboratory experiments (24). Tolerance to ultraviolet exposure is speciesspecific. Deep-dwelling lake trout are more susceptible to this type of ocular injury than other salmonids. Exposure to toxic substances may also cause cornea1 lesions.

Lenticular pathology (lenticulitis) A number of conditions affecting the lenses have been reported in cultured, display, experimental, and feral fishes. These include cataract, the most common lens lesion; softening and swelling of the entire lens as reported by Hawkes (15) in rainbow trout (Salmo gairdneri) and Hawkes and Stehr (31) in the surf smelt (Hypomesus pretiosus) exposed to crude oil; and aphakia, absence of the lens, as occasionally seen in some sciaenids in the wild. Swelling of the lens has not been reported from cultured or display fishes but may occur in them as well. Aphakia, which probably does occur in them, is likely uncommon.

Fig. 9. Young coho salmon (0. kisutch) with acute keratitis (keratoglobus and opacity of cornea). (Courtesy, J. C. Hnath)

Disorders of fish eyes

Cataract (Figs. 4, 5, and IO) True cataracts (opacities of the lens), grey cataract, or Cataracta traumatica of Van Duijn (9), make fish less attractive. They also negatively affect feeding and survival in animals such as the clear-water salmonids that depend upon sight. Many of the cataractous conditions noted below also occur in higher vertebrates, including humans. Cataract has been recognized as a significant disease of cultured salmonids since at least the report of Hess (39) in 1935. Opacities of the lens are also common in feral and cultured fish, as recent literature indicates. Among cultured salmonids cataracts most commonly result from animals being fed nutritionally unbalanced diets (Figs. 4 and 5). A large portion of the literature on ocular diseases in cultured fishes deals with nutrition-related cataracts. Lens opacities also can result from osmotic imbalances between internal and external fluids (36,37,40). These have been noticed most frequently in association with movement of salmon

Fig. 10. Sagittal section of a “diseased” eye of the sciaenid Atlantic croaker (Micropogonias undulatus) showing enlarged and engorged choroid gland or rete (G), swollen area of retina (R) and severely cataractous lens (L), all believed related to polycyclic aromatic hydrocarbon pollution. (PAS stain).

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smolts from freshwater into sea water, which may be hyperosmotic physiologically. Loss of internal water creates cloudiness within the lens, particularly at the sutures of the ends of the crystalline fibers (36,37). Osmoregulatory difficulties would be more common among aquatic vertebrates than terrestrial ones. Unlike the majority of cataracts, whatever the cause, osmotically related lens opacities are reversible, provided the causes of such imbalances are corrected in timely fashion. Intoxication has been shown to have produced lens cataracts in teleosts. Recently, cataract involving various abnormalities in the capsule, epithelial layer, cortex, or nuclear portions of the lens, in three feral sciaenids (Atlantic croaker (Micropogonias undulatus), spot (Leiostomus xanthurus), and weakfish, (Cynoscion regalis)) was linked to exposure to estuarine sediments heavily contaminated by polycyclic aromatic hydrocarbons (PAH), among other anthropogenic contaminants found in the polluted site (lo-12,14,41; Fig. 10). Mayer et al. (42) produced cataracts in rainbow trout (Salmo gairdneri) by exposing them to phosphate ester hydraulic fluids in experimental conditions. Undoubtedly, pollutant-related cataracts can occur in cultured populations and must always be considered. Wilcox and Dukes concluded similarly (6). Exposure to sunlight in shallow hatchery raceways has been related (along with other symptoms of sunburn) to production of cataracts, along with the keratitis mentioned above, in lake trout (Salvelinus namayacush). Exposure to extreme cold (-10-20 “C) causes fish lenses to become “turbid” under experimental conditions according to Wilcox and Dukes (6). The condition is apparently only partially reversed upon warming. It is not known whether such cataractous damage is likely to occur in nature or under culture conditions. As will be shown, incidence of cataracts in salmonids can be related to the particular strain of salmon stocks one is dealing with. While this phenomenon appears to have been noted only among salmonids it will undoubtedly be seen in other species as careful observations increase. Genetic mediation of various ocular characteristics has long been recognized. For example, certain strains of goldfish (Carassius auratus) with protruding or dorsally placed, upward-gazing eyes have been prized by some ornamental fish fanciers and purposely bred for these features for many years. Abnormalities and contents

of humorai chambers

While glaucoma, resulting from extreme pressure and fluid build up within the “anterior” chamber

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W. J. Hargis, Jr.

of the orb, has not been reported, other conditions do affect it, and the “posterior” chamber and their contents. In both cultured and wild fishes, hyperemia has been reported in the anterior, or aqueous chamber. Extravasation from the rich blood vessels in the iris seems the predominant cause. Such hemorrhagic disease has been related to trauma, infection, and intoxication. The posterior or vitreal chamber may also contain enlarged blood vessels or large numbers of red and white blood cells in the vitreous humor. The blood involved in these hyperemic lesions may come from the fundal blood vessels (on the internal surface of the retina) found in some species of fish (mostly those without falciform processes) or from abnormally enlarged and engorged blood vessels associated with the falciform process, which occurs in many others. Such hemorrhagic lesions have been seen in feral fishes exposed to high concentrations of PAH and undoubtedly will be found in cultured animals subject to similar intoxication.

Hargis and Zwerner (11) reported that choroid gland disease, enlargement and engorgement of the choroid rete (Fig. 10) and the choriocapillaries were associated with PAH contamination. Wilcox and Dukes (6) reported a similar condition of the choriocapillaries in the choroid and iris caused by poor water quality. Septicemia of the choroid rete and associated blood vessels, associated with gram-negative bacteria, has also been observed (6). These same lesions undoubtedly can occur in culture or display animals should they be exposed to water of poor quality or become infected. Scleral and adnexal lesions Wilcox and Dukes (6) have indicated that lesions caused by parasite invasions have been observed in the scleral and adnexal retrobulbar tissues of some feral fish. These lesions undoubtedly also occur in animals in confinement but are probably insignificant. Ocular tumors

Retinopathy

(Fig. IO)

Fundal disease manifested as white spots on the fundus (i.e. the internal or vitreal surface of the retina) has been reported from carp (Cyprinus carpio) experimentally exposed to various surfactants by Kohbara et al. (35). Dilation or engorgement of the hyaloid blood vessels is also associated with surfactant exposure of whole fish. Roberts (21) has described similar conditions as occurring in diabetic or “sekoke” carp, resulting from nutritional imbalances. Retinal thinning and retinal swelling (edema) have been observed in PAH-intoxicated feral fishes by Hargis and Zwerner (11) and swelling, as exemplified by edema of the plexiform and ganglia1 layer caused by nutritional imbalances by Poston et al. (25). Hawkes and Stehr (31) observed photoreceptor and neuronal degeneration in surf smelt (Hypomesus pretiosus) experimentally exposed to Prudhoe Bay crude oil. Uveitis, choroiditis (Figs. 3 and 10) The uveal system of fishes includes the choroid and choroid chamber and the iris with associated blood vessels (Figs. 1, 3, and 10). In many teleosts the elaborate choroid rete or choroid gland is interposed between the external circulation and the small blood vessels distributed around the entire eyeball in the choroid layer and extending into the iris. The system of smaller blood vessels in the choroid and iris is called the choriocapillaris. The falciform process, also well supplied with small blood vessels, is involved in uveitis at times.

Yoshimizu et al. (26) exposed chum (Onchorhynchus keta) and masu (0. masou) salmon to 0. masou virus (OMV). Epithelial tumors developed on the jaws of both species. Histological examination showed them to have been composed of epithelial cells which proliferated and invaded nearby connective tissues. Tumors with similar characteristics developed on the corneal epithelium and inner opercular of the chum salmon. The numbers involved were small. Consequently, the significance of their finding for salmon culture was not established. However, culturists should be aware of possible effects of epithelially active viruses on tissues associated with the eyes. Other neoplasms have been reported in teleost eyes, such as melanomas and retinoblastomas. These neoplastic diseases probably are of little significance to mass culture operations. PRINCIPAL CAUSES OF EYE DISEASE The various causes of ocular diseases likely to affect fishes in hatcheries, culture facilities, large aquaria, and home aquaria can be reduced to a few principal ones. The main causes are, in order of importance as gauged by number of applicable literature reports: a) nutritional imbalances; b) various parasitemias (including infections by viruses, bacteria, fungi, and protozoans and metazoan infestations); c) poor water quality (including gas imbalances and abnormal temperature, osmotic imbalances and chronic or acute intoxication from wastes, metabolites, and introduced toxicants); and d) ultraviolet radiation. Responses in all of the dis-

Disorders of fish eyes

eases caused by one or more of these primary causes are affected by the general health of the animals, which is influenced in turn by all types of stresses such as confinement, overcrowding, aggressive behavior, and careless handling. Generally, all responses will be mediated by the genetic qualities of the populations or individuals being cultured or held. It will be useful to consider the primary causes in some detail. Nutrition and eye disease

Hughes (5) published a valuable review of nutritionally associated diseases of salmonids. Several related reports have appeared since. In 1953 coho salmon (Oncorhynchus kisutch) fry with hemorrhage of the optic nerve and retinal swellings were reported in hatcheries of the Pacific northwest of the United States. In 1962 Allison (43) reported cataracts as occurring among hatchery-reared lake trout (Salvelinus namayacush). In the early 1970s culturists working at several hatcheries in various parts of Japan recorded frequent occurrence of cataract in several salmonids, including 0. masou, 0. rhodurus, 0. nerka, 0. kisutch, and Salmo gairdneri (29,30). These same authors devoted special study to cataracts found in masu salmon (0. masou) at Mori, Southern Hokkaido, noting two main types of cortical and nuclear cataracts. In 1977, lake trout (S. namayacush) and later rainbow trout (S. gairdneri) at the Tunison hatchery in central New York State developed lens opacities. As Riis (44) and Richardson et al. (34) reported, a number of salmon hatcheries in the USA (Washington State) and Canada (British Columbia) experienced large-scale outbreaks of bilateral cataract disease in 1981 in their chinook (0. tshawytscha) and coho (0. kisutch) salmon stocks. Cataracts in cultured salmonids have also been reported in Africa by Lee et al. (45) and in Iceland. Subsequent clinical and experimental investigations, some quite exquisite in design and conduct, revealed nutritional deficiencies to have been the major cause in most of these cases of eye disease. The several studies, for example Richardson et al. (34), have shown that diets especially high in fish bone ash, phytic acid (sodium phytate-a chelating agent that binds zinc), calcium, phosphorus, and tryptophan or deficient in riboflavin, as reported in Philips et al. (46) and Barash et al. (47), or zinc (28) can result in cataract. Halver (48) reported cataract, along with cornea1 abnormalities in riboflavin deprived fish. Likewise, Poston et al. (25) reported cornea1 lesions and cataracts in rainbow trout fingerlings fed riboflavin deficient diets. They also indicated that riboflavin-deficient chan-

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nel catfish (Ictalurus punctatus) developed cataracts. Other reports confirm that zinc deficiency produces cataracts in the eyes of salmonids along with fin erosion (3). In the same paper Egidius (3) reported that good recovery in several Atlantic salmon cultures was obtained after zinc was added to their diet. Since most growth-related cataracts are irreversible because damaged elements are overlain and incorporated into the inner layers of the cortex and nucleus of the lens it would be interesting to learn what constituted “good recovery” in this case. It probably meant that the occurrence of new cases dropped after suitable diet was supplied. As indicated above, where the epithelial layer of the lens is severely damaged no recovery in individuals is possible. Halver (48,49) reviewed the literature on vitamin deficiencies. Lall(50) reviewed that pertaining to minerals. However, as the Reference sections below show, a number of investigations have been reported since. When properly balanced diets were developed and presented, prevalences of developing cataracts dropped. These results in teleosts coincided with those of mammalian eye researchers who found that diets deficient in vitamin E, methionine, or zinc, or high in calcium, tryptophan, or phytic acid, among other nutritional imbalances, to be primary nutritional causes of this eye disease. Parasites and eye diseases

Occlusion caused by one or more digenean platyhelminths (worm cataract or Cataracta parasitica of Van Duijn; 9) can also occur in farmed, ornamental, and wild fish. The larval worms (metacercariae) can lodge in the anterior chamber between cornea and lens or even in the lens or posterior (vitreous) chamber and completely destroy sight. Secondary infection and death usually follow. Increasing morbidity and even death may follow eye disease, especially if it is a secondary effect. Ability to find food is not often a problem for most aquarium fishes; therefore, poorly functioning eyes can be overcome by use of other sense organs in such a milieu. However, decline in aesthetic value is serious. Economic loss from these and other eye pathologies can be significant when rare or expensive individual specimens are affected. When entire shipments of wild-caught or cultured ornamentals, or when nursery stocks suffer eye disease, losses can be especially costly. Strigeid larvae affect salmonids, cichlids, and other cultured species as well (6). In such species they can have an effect on production levels. Monogeneids have been implicated in producing cloudy corneas in the spadefish, Chaetodipterus faber, at

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the New York Aquarium (D.A. Thoney, The New York Aquarium, Brooklyn, N.Y., USA, personal communication). Egidius (3) reported that exophthalmos occurred in cultured salmonids associated with Viral Hemorrhagic Septicemia (VHS - Egtved disease) of rainbow trout (Salmo gairdneri) in northern Europe; Infectious Hematopoietic Necrosis (IHN -cold water disease) of sockeye (Oncorhynchus nerka) and chinook (0. tshawytscha) salmon, first in the North Pacific and more recently in the American northeast; Enteric Redmouth Disease (caused by the enterobacterium, Yersinia ruckeri); and Bacterial Kidney Disease (BKD - caused by Renibacterium salmonarum) in Atlantic salmon, Salmo salar, in Scotland and other salmonids in Europe and North America. The yeast, Rhodotorula sp. has been shown to produce exophthalmia in Sparus aurata by Faisal(38). The fish is cultured in the region of Alexandria, Egypt. In most of these cases the infection caused inflammation and edema of ocular or adnexal tissues that produced bulging of the orb itself or pushed the eyeball outward. Other environmental stresses and eye disease

Environmental stress can take several forms as in exposure to high-density ocean waters by smolts before their physiological process are adapted to such changes in osmolarity. It may also be caused by excess 02 or N2 in the water under conditions of hypersaturation. Gaseous imbalances may not only produce bubbles in the tissues of one or both eyeballs but also in tissues and spaces around them. Exophthalmos results (2). Poor water quality may also cause stress and impair the fish’s ability to defend themselves from disease, whatever the immediate etiological agent. Allison (43,51) reported being able to induce cataract using ultraviolet light. The same has been done in mammals. As indicated elsewhere, it is highly probable that exposure to excessive sunlight is involved in cataract formation in lake trout (Salvelinus namayacush ) , the light-sensitive species involved in the genetic studies mentioned above. Eyes of other species can, most probably, be damaged by excessive exposure to sunlight or other sources of ultraviolet light. There is some possibility that exposure to sunlight is involved in production of PAH-related eye diseases, such as cataracts (Hargis, unpublished), a factor that must be investigated further. Should this be true, managers of hatcheries and other culture facilities must consider control of exposure to sunlight, along with contaminant control, for rea-

sons other than preventing “sunburn” effects in salmonids and other fish under mass culture. Kincaid (H. G. Kin&d, National Fishery Research and Development Laboratory, U.S. Fish and Wildlife Service, Wellsboro, PA, USA, personal communication) postulates that environmental stress is involved in expression of the geneticallymediated nuclear cataracts in hatchery stocks of lake trout discussed in some detail below. Intoxication and eye diseases

As indicated above, cataracts have been observed in several sciaenids exposed to PAH in a subestuary, some of whose sediments contain extremely high levels, i.e. up to 3900 mg /kg of dry sediments (lo-12,14). Cataracts were also observed in spot (Leiostomus xanthurus) exposed experimentally to the same sediments (14). Animals from clean waters did not have cataracts. (Spot have been cultured for experimental purposes and probably can be for other uses as well.) Hawkes (15,27) and Hawkes and Stehr (3 1) observed several other lens abnormalities in crude oil exposed fishes. Mayer et al. (42) produced cataracts, retinal degeneration, and pigment alteration, as well as degeneration of the retractor lentis muscle in rainbow trout (Salmo gairdneri) fry by exposing them to several hydraulic fluids. Intoxication has also been shown to cause other eye disorders such as enlargement and engorgement of the choroid gland, choriocapillaries, hemorrhage in the iris and aqueous and vitreous chambers, and retinopathy as reported by Hargis and Zwerner (11) for some Sciaenidae. Hawkes and Stehr (31) induced morphological changes in the neuronal layer and elipsoid and myeloid (myoid) regions of the receptor cell inner segments in the retinas of embryos of surf smelt (H. pretiosus) to water-soluble fractions of crude oils. Undoubtedly oil contaminated water will produce similar eye diseases in hatchery fish or those held in sea pens exposed to such waters. Genetic factors and eye disease

Around 1984 scientists (32,33) working with various hatchery strains of lake trout (Salvelinus namayacush) began to suspect that various types of eye abnormalities, especially nuclear cataracts, possessed an heritable component. Apparently the expression of these nuclear cataracts, which are very small in size and difficult to see unless observers are especially careful, is triggered by some environmental stress. As stated by K&aid (personal communication), who is studying this phenome-

Disorders of fish eyes

non, nuclear cataracts occur in higher percentages in “cataractous families” in his controlled experimental work with lake trout employing constant and comparable conditions of culture with 28 genetic families of fish, embodying two different year classes. Kincaid also indicates that in four different strains of lake trout, the frequency of nuclear cataract ranged from 10-60’7’0at the Allegheny National Fish Hatchery, Warren, Pennsylvania, USA. That lake trout are more susceptible to this disease than other related salmonids is, in itself, evidence that genetic factors are involved in eye disease. Current research on this phenomenon also considers effects of cataract in fish after stocking in Lake Ontario and involves fish hatchery and field assessment personnel. Apparently, tagged groups of around 40,000 individuals are being released and followed. Researchers are also considering the question of whether genetically mediated cataract is strictly a hatchery phenomenon or occurs in feral stocks as well. Should these studies further support the strong indications of genetic involvement, culturists will wish to avoid those strains with strong propensity for this eye disease. Indeed, a major precept in any culture effort should be to secure the most suitable stocks possible. In fish, as in other husbanded animals, “blood lines” are important. It would seem likely that controlled breeding might produce strains with reduced predelection for cataracts as one possible preventative. IMPACTS

OF EYE DISEASE

GROWTH,

REPRODUCTION,

ON FISH HEALTH, AND UTILITY

The impacts of eye disease upon health and survival of fish or upon the socioeconomic activities that they support have been examined by several authors. In their paper dealing with interpretation of the impacts of cataracts on the Brazilian sciaenid teleost, Micropogonias furnieri, Vazzoler and Phan (13) discussed the possible influence of ocular disease on fish populations. In doing so they cited the works of Uspenskaya (52), that indicated that cataracts interfere with the fish’s ability to locate food thus resulting in a reduced nutritional state, and Sallman et al. (53), who reported reduction in rate of growth in weight. In interpreting their own research results with noncataractous and cataractous individuals of wild M. fumier& Vazzoler and Phan (13) indicated that the “condition index” values they calculated showed no significant differences between the two groups. However, because they found cataracts in juveniles only and not in adults and because they observed reduced survival rates for groups of individuals with a) one normal lens

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(55% survival); b) both lenses with early cataracts (30% survival); and c) both lenses with total cataracts (15% survival) these authors concluded that cataracts were a factor in producing “natural” mortality of affected Brazilian croaker. Petrushevski and Shulman (54) had reported great mortality in eye-diseased freshwater fish. Most of the eye diseases mentioned, cataract, corneal opacity, exophthalmos, and hemorrhage in the anterior or posterior chambers affect the passage of photons into and through the eyeball. Those that damage the retina or optic nerves would interfere with detection and transfer of visual images. Various levels of optical blindness would be the result of these several lesions. Survivability of vision-deficient fish is reduced because of impaired ability to escape predators or to feed. This last feature probably is serious in the wild, especially in clear-water species, and in the food-competitive environment found in many mass culture systems even though some behaviorally conditioned blind aquarium fish have shown remarkable longevity (9). Reduced ability to school, feed, navigate, or escape predation would be especially serious for species whose life cycles require several years of survival and migration and whose continued survival is heavily vision-dependent. Animals living in light transparent waters are generally quite heavily dependent upon effective sight. Sea-going salmonids fit this pattern. Productivity of culture-assisted populations conducted around the North Pacific rim and in the U.S. Great Lakes and many similar areas would be reduced. Indeed, Hnath (J. G. Hnath, Michigan Dept. of Natural Resources Fish Health Laboratory, Michigan, USA, personal communication) has indicated that survival of coho salmon released in the Great Lakes to establish self-replenishing stocks is reduced, apparently owing to eye disease and the propensity for such disease in the released fish. Success of recreational fishing dependent upon catching of released cultured fishes with vision deficiencies likely would be reduced. Reductions would be especially serious where acute vision is involved in detection, pursuit, and taking of baits and lures. Where fish are marketed in the round, or only gutted, sales could be reduced, since many wholesale and retail buyers consider eye condition to be an indicator of product quality. Fish with sunken, protruded, bloody, or cloudy eyes are rejected frequently. It has been reported that juvenile salmonids with developing nutritionally related cataracts

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(25,34,55) also suffer impaired growth. Judging from those reports it is likely that the impaired growth noted was related to the dietary imbalance responsible for the cataract and other ocular problems and not the eye lesions alone. However, there is little question that vision-damaged fish are generally at a disadvantage and that their growth and even relative survival rates are frequently reduced. One must conclude that any disease of eye or adnexa that interferes with the a) passage of photons to the retina, b) their focus thereon to provide a useful image, and c) passage to and appropriate interpretation of visual stimuli within the brain will produce the same results-reduction in survival after cultured animals are released into the wild for restocking or for put-and-take recreational fishing, especially in clear water fishes. There is a useful aspect of the appearance of the several readily visible ocular lesions; exophthalmos; opaque, bulging, or distorted corneas (keratoglobus or keratoconus); or cataracts. Where they occur in large numbers of the animals in a hatchery or other component of a mass culture system they indicate serious problems and the culturist should immediately check for gas imbalances or infectious or parasitic disease (exophthalmos), sunburning (keratitis or cataract), or difficulties with the food and feeding regime (keratitis or cataract). Eye condition should be regularly and closely monitored and used as an indicator of culture conditions. POSSIBLE

PROPHYLACTIC

MEASURES

AND CONTROL

FOR EYE DISEASE

Eye disease by itself is troublesome, even serious. As we have seen, many eye-damaged fish do not feed and grow normally, nor do they survive as well as those with normal vision. Certain types of lesions, such as exophthalmos, probably the most commonly reported ocular problem, are indicators of either unfavorable water quality or primary or secondary signs of parasitic or infectious disease. Cornea1 opacities, keratoconus, keratoglobus, or cornea1 ulcerations may reflect excessive exposure to damaging levels of sunlight, parasitic or infectious disease, inadequate diets, or other difficulties. Cataract can also indicate unbalanced diets (most common), metazoan invasion, toxic conditions, or (often accompanied by keratitis) excessive sunlight. Such conditions are generally inimitable to successful production of healthy fish at the minimum reasonable cost and also to obtaining maximum yields of attractive (for market) or viable (for stocking) fishes. Several of the most common eye maladies, exophthalmos, keratitis, and cataract, are readily

observable by nondestructive or noninvasive examination techniques. Consequently they can serve as indicators of unfavorable culture conditions. Taken individually or together and coupled with other signs, these eye diseases can suggest causes and corrective measures as well. The best approach to ocular, or any other, disease is prevention or avoidance. Continuous application of rigorous sanitation procedures and maintenance of appropriate water quality conditions are the most important preventative activities to be pursued in any breeding, display, or mass culture system. This means design and construction of culture facilities (or replacement components) that continually provide water whose quality is maximally suited to successful growth and survival of the species under culture and the least stressful environmental culture conditions economically and technologically possible. It also includes exercise of constant vigilance through appropriate monitoring and control techniques, with appropriate feedback, to prevent development of hypersaturation of oxygen or nitrogen, to maintain proper osmotic balances and other features of suitable water quality (including temperature) required by the species under culture. Control of “culture” and metabolic wastes is critical. Since stress is also an important component of disease, the culture facilities must be designed and constructed to provide the least stressful conditions of confinement possible. Social stress must be reduced as far as possible. To do either, the behavioral characteristics of the animals considered as candidates for culture must be carefully matched to the culture system and vice versa. Many cases of cataracts and other eye diseases reported in mass culture facilities have been traced to: a) “bargain basement diets” (6), i.e. those high in offal (horse (56) and pig organs), white fish meal, or other undesirable components such as phytic acid, calcium, etc.; b) diets deficient in zinc or other required minerals, vitamin A, riboflavin, and other chemicals; c) diets containing bacteria, fungi, or other contaminants; and d) diets that have been spoiled, gone rancid or become “denatured” from improper storage, or contain contaminants. Therefore, rigorous steps must be taken in preparation or purchase, storage, and feeding of adequate, but not excessive, amounts of especially tailored, nutritious diets. Uneaten food must be quickly removed. Like sanitation, proper ration management must be carefully planned, programmed, rigorous, and constant. Timing is important. Very young animals with yolk sacs can survive temporary deprivation of “outside” food but when internal food supplies are exhausted ad-

Disorders of fish eyes

equate food must be readily available (55). The conditions “are right” for many diseases to eventually “take hold” in this critical early stage of development . Proper diet will not only prevent many types of ocular lesions but will also enhance survival, rate of growth, marketable biomass, and quality of product. Fish eyes are easily damaged mechanically. Therefore construction and maintenance of facilities and conduct of aquarium and culture operations should be directed at reduction of the possibility of container or handling trauma. Population levels and behavioral characteristics must be appropriately managed to reduce possibility of eye injuries. Eye damaging digeneid infestations should be carefully controlled by eliminating the snails, fisheating birds, and other predators that may serve as intermediate or final hosts to such parasites. Infectious diseases should be controlled by: rigorous and constant sanitation; mass immunization where possible; chemical treatment if feasible; or destruction of diseased individuals or populations if necessary. Appropriate importation controls and quarantine arrangements will help prevent introduction of stocks with or prone to eye disease. Apparently certain salmonid populations are susceptible to certain types of eye disease such as nuclear cataract by reason of genetically controlled factors. The same is likely true of susceptibility to other ocular disorders. Consequently, stocks for culture should be selected for their resistance to the several types of eye disease that might be affected by genetic factors. Continuous, responsible supervision of stock selection, handling procedures, water quality control, disease control, and food and feeding is essential in any culture operation if it is to be successful. SUMMARY

AND CONCLUSIONS

The eyes of teleosts are similar in basic plan to those of higher vertebrates, including man. However, there are some differences in structural detail and certain physiological processes related to the evolution of the eyes to facilitate life in various aquatic habitats to which the fishes have become adapted. Like the eyes of higher vertebrates, fish eyes are subject to a number of diseases that can affect every organ and tissue of the orb and orbit. The responses of the ocular organs and tissues common to all vertebrate groups to the various etiological agents responsible for eye disease are quite similar. The eyeballs and adnexa of may be damaged by parasites of many systematic groups (i.e. viruses,

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bacteria, fungi, protozoans, helminths, and crustaceans), poor nutrition, and excessive ultraviolet light. Unlike terrestrial vertebrates the majority of the 20,000-25,000 species of fish are wholly aquatic, constantly immersed in water, constantly taking waters into their branchial cavities and digestive tracts. Under such conditions the quality of the ambient water is critical. Imbalances in gas content (especially 02 and Nz) can produce gas bubbles in the tissues and fluids of the orbs and adnexa and severe exophthalmos (pop-eye) is a common result in aquaria and culture systems. Further, osmotic imbalances, abnormal temperatures (especially extremely low ones), and toxic substances in solution or suspension are capable of producing other lesions in teleost eyes. Among the diseases observed in wild (which probably can occur in captive populations as well) and cultured teleosts are lesions of the cornea (keratosis, including cloudy cornea, keratoglobus, and keratoconus); hemorrhage of the anterior and posterior chambers and the aqueous and vitreous humors; enlargement and engorgement of elements of the uvea (choroid, choroid gland, choriocapillaris, and iris); lenticulitis (including enlarged or edematous lenses and cataracts); retinopathies of various types; and several other lesions. Endopthalmos (sunken eye) and exophthalmus also occur. The latter is frequently reported in cultured and aquarium fishes. Of the lesions affecting components of the eyeball, those impacting the cornea, lens, the chambers and their contents, and the retina are not uncommon in salmonids, carp, and catfish under conditions of mass culture. Undoubtedly other frequently cultured food fishes such as Tiiapia spp. and milkfish (Charms charm) are similarly affected, though published reports of ocular disease among them are few. Exhibition fishes experience most of the eye diseases as well. Impacts of eye disease vary with type and severity. Should eye disease reach significant levels in brood stock, mass culture, or aquarium populations culturists must be concerned for two reasons. The first is the possible deleterious effects on the animals in question and on productivity of the culture enterprise. The second is the strong likelihood that the presence of eye lesions indicates poor water quality, poor nutrition, excessive radiation, parasitemia, or use of genetically impaired stocks. All signify culture conditions inimicable to maintenance of healthy stocks and mean that effective breeding performance and maximum conversion of the time and resources initiated in the culture effort to saleable biomass is impaired. Further, in those cultures intended to enhance wild stocks, ocular

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disease can be serious. Among salmonids and other species that live in comparatively clear waters and depend upon effective vision for survival or mating, eye damage is especially deleterious. Where eye disease appears in significant numbers of contained fish immediate attention must be given to determination and correction of the cause or causes. Allowing poor water quality, poor feeding regimes, or reinfection by parasites to continue only means that successive populations will be affected in similar fashion. Poor nutrition, signalled most often by cataracts and keratitis among the eye diseases, must be corrected quickly else extant and successive culture populations be unthrifty. Water quality faults must be corrected at once for continuing culture operations to improve or be successful. Few of the eye diseases noted, especially cataract caused by nutrition, ultraviolet radiation, intoxication, or parasites, can be cured. Severely affected fish should be fattened by presentation of adequate diets, harvested, and sold headless or processed. The same is true for animals suffering from eye disease caused by poor water quality. In the case of parasite-induced ocular lesions (to which eye disease is usually a secondary phenomenon- except in the case of the larvae of strigeid digeneids) prophylaxis (including immunization against some diseases), sanitation, careful control of imports, and treatment are possible. Immunization and treatment are usually most cost-effective when applied to smaller groups of individuals such as breeding stocks or display animals. However, “dip” immunization is feasible for larger numbers where suitable vaccines are available. Chemical treatment is usually only feasible where small numbers of animals are involved. Where infectious disease is widespread in mass cultures, options are few. As in swine and cattle herds or poultry flocks destruction is often in order. If less severe, culling might halt the development of infection in the population, or early harvest might be the most reasonable solution. As with other diseases, prevention is the most productive approach to control of all types of eye disease. Methods include: a) utilization of culture or aquarium systems designed to be as stress-free, trauma-free, and conducive to growth as possible; b) effective matches of species involved to physical and chemical conditions provided; c) careful selection of breeding stocks or of starter cultures for appropriate genetic, health, and growing qualities; d) avoidance of introduction of diseased fishes into the system (careful selection and quarantine); e) provision of adequate nutrition; f) constant maintenance of suitable water quality; g) careful handling

of all populations; h) elimination or reduction of the possibility of parasitic infection by excluding or controlling birds, snails, etc.; and i) timely harvest. Genetically suitable starter or brood stocks, proper nutrition, careful handling, suitable water quality, and freedom from unacceptable levels of disease are five essential features of successful fish husbandry. They can only be realized by selection of appropriate species and strains for culture, careful maintenance of facilities and proper diets and constant water quality control measures. Frequent monitoring and instant correction of faults are necessary. Suitably trained culture personnel subject to frequent, responsible, and knowledgeable supervision are essential. Constant attention to proper sanitation with appropriate feed-back control arrangements are critical! Acknowledgments-Mrs. Shirley 0. Sterling typed the many versions required, Mrs. Dianne A. Bowers drew the diagrams and William W. Jenkins prepared the photographs.

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(1969). Light transmission by corneas, aqueous humor and crystalline lenses of fishes. Vision Res. 9: 223-232. Poston, H.A., Riis, R.C., Ramsey, G.L., Ketola, G. (1978). Nutritionally induced cataracts in salmonids fed purified and practical diets. Mar. Fish Rev. 40: 45-46. Yoshimizu, M., Tanaka, M., Kimura, T. (1988). Histopathological study of tumors induced by Oncorhynchus masou virus (OMV) infection. Fish Pathol. 23(2): 133-138. Hawkes, J.W. (1980). The effects of xenobiotics on fish tissues: Morphological studies. FASEB Federation Proceedings 39(14): 3230-3236. Ketola, H.G. (1979). Influence of dietary zinc on cataracts in rainbow trout (Salmo gainhen’). J. Nutr. 109(6): 965-969. Watanabe, Y., Yamada, .I. (1980). Histological characteristics of cataractous eye lenses in cultures masu salmon. Bull. Fat. Fish. Hokkaido Univ. 31: 290-296. Watanabe, Y., Yamada, J. (1980). Water, electrolytes, and soluble proteins in cataractous eye lenses of masu salmon. Bull. Fat. Fish. Hokkaido Univ. 31: 297-305. Hawkes, J.W., Stehr, C.M. (1982). Cytopathology of the brain and retina of embryonic surf smelt (Hypomesus pretiosus) exposed to crude oil. Environmen. Res. 27(1982): 164-178. Kincaid, H.L. (1987). Inheritance of nuclear cataract in lake trout. Abstract 375 In: Program for 49th Midwest Fish and Wildlife Conference. Milwaukee, Wisconsin, Dec. 5-9. Kincaid, H.L., Elrod, J.H. (1987). Survival in Lake Ontario of hatchery-produced lake trout with and without nuclear cataracts. Abstract 376 In: Program for 49th Midwest Fish and Wildlife Conference Milwaukee, Wisconsin, Dec. 5-9. Richardson, N.L., Higgs, D.A., Beamer, R.M., McBride, J.R. (1985). Influence of dietary calcium, phosphorus, zinc, and sodium phytate level on cataract incidence, growth and histopathology in juvenile chinook salmon (Oncorhynchus tschawytscha). J. Nutr. 115: 553-567. Kohbara, J., Murachi, S., Nonba, K. (1987). Ocular abnormalities in carp chronically exposed to various surfactants. Nippon Suisan Gakkaishi 53: 979-983. Iwata. M., Nishioka, R.S.. Bern. H.A. (1987). Whole animal transepithelial potential (TEP) of coho salmon during the Parr-smolt transformation and effects of thyroxine, prolactin and hypophysectomy. Fish Phvsiol. Biochem. 3: 25-38. Iwata, M., Komatsu, S., Collie, N.L., Nishioka, R.S., Bern, H. A. (1987). Ocular cataract and seawater adaptation in salmonids. Aquaculture 66: 315-327. Faisal, M. (1986). Augenmykose bei Zucht fischen. Pilzdialog 3: 56. Hess, W.N. (1935). Production of nutritional cataract in trout. J. Exp. Zool. 70: 306-309. Iwata, M., Clarke, W.C. (1987). Culturing coho. Can. Aquaculture 3: 28-31. Huggett, R.J., Bender, M.E., Unger, M.A. (1987). Polynuclear aromatic hydrocarbons in the Elizabeth River, Virginia. In: Dickson, K.L., Maki, A.W., Brungs, W. (eds.) Fate and effects of sediment bound chemicals in aquatic systems. Pergamon Press, Oxford, pp. 327-341.

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42. Mayer, EL., Adams, W. J., Finley, M.T., Michael, P.R., Mehrle, P.M. Saeger, V.W. (1981). Phosphate ester hydraulic fluids: An aquatic environmental assessment of Pydrauls 5OE and 115E. Special Technical Publication 737. Amer. Sot. for Testing and Materials, pp. 103-1230. 43. Allison, L.N. (1962). Cataract among hatcheryreared lake trout. Prog. Fish-Cult. 24: 155. 44. Riis, R.C. (1981). A report on cataracts. A report relevant to the high incidence of fish cataracts in Washington State Hatcheries to the Washington Department of Fisheries, Olympia, Washington, 45 pp. 45. Lee, W.R., Roberts, R.J., Shepherd, C.J. (1976). Ocular pathology in rainbow trout in Malawi (Zomba disease). J. Comp. Pathol. 86: 221-233. 46. Phillips, A.M., Podoliak, H.A., Brockway, D.R., Balzer, G.C. (1956), The nutrition of trout. Cortland Hatchery Report 26 for the Year 1956. N.Y. Conserv. Dept. Fish. Res. Bull. 21., 93 pp. 47. Barash, H., Poston, H. A., Rumsey, G.L. (1982). Differentiation of soluble proteins in cataracts caused by deficiencies of methionine, riboflavin or zinc in diets fed to Atlantic salmon, Salmo salar, rainbow trout, Salmo gairdneri, and lake trout, Salvelinus namaycush. Cornell Vet. 72: 361-371. 48. Halver, J.E. (1953). A vitamin-test diet for chinook salmon. The water soluble vitamin requirements of chinook salmon. Ph.D. thesis, Univ. Washington, Seattle, 88 pp. 49. Halver, J.E. (1979). Vitamin requirements of finfish. In: Halver, J.E., Tiews, K. (eds.) Finfish nutrition and fish feed technology. Heenlmann, Berlin 1: 45-50. 50. Lall, S.P. (1979). Minerals in finfish nutrition. In: Halver, J.E., Tiews, K. (eds.) Heenemann, Berlin 1, Finfish nutrition and fish feed technology, pp. 86-92. 51. Allison, L.N. (1963). Cataract in hatchery lake trout. Trans. Am. Fish Sot. 92: 34-38. 52. Uspenskaya, A.V. (1961). Some data on effects of helminthic cataract of the eye on the nutritional level of the rainbow trout. In: Petrushevski, G.K. (ed.) Parasites and Disease of Fish. Israel Program for Scient. Transl., Jerusalem, 328-329. (Original in Bull. All-Union Scient. Res. Inst. Lake and River Fish, 42.) 53. Sallman, L. von, Halver, J.E., Collins, E., Grimes, P. (1966). Thioacetamide-induced cataract with invasive proliferation of the lens epithelium in rainbow trout. Cancer Res. 26: 1819-1825. 54. Petrushevski, G.K., Shulman, S.S. (1961). The parasitic diseases of fishes in the natural waters of the USSR. In: Dogiel, V.A., Petrushevski, G.K., Polyanski, Yu, I. (eds.) Parasitology of fishes. Oliver and Boyd, Edinburgh, pp. 299-319. 55. Richardson, N.L., Higgs, D.A., Beamer, R.M. (1986). The susceptibility of juvenile chinook salmon (Oncorhynchus tschawytscha) to cataract formation in relation to dietary changes in early life. Aquaculture 52: 237-243. 56. Allison, L.N. (1951). Horse liver as a causative factor in white blindness of hatchery trout. Trans. Am. Fish Sot. 80: 140-147. ADDITIONAL READING Anonymous. (1986). Cataract as an outcome of zinc deficiency in salmon. Nutr. Rev. 44: 118-120.

Ashton, N., Brown, N., Easty, D. (1%9). Trematode cataract in freshwater fish. J. Small Anim. Pratt. 10: 471-478. Buterbaugh, G.L., Willoughby H. (1967). A feeding guide for brook, brown and rainbow trout. Prog. Fish-Cult. 29: 210-215. Clarke, W.C. (1982). Evaluation of seawater challenge tests as an index of marine survival. Aquaculture 28: 177-183. Clarke, W.C., Blackburn, J. (1978). Seawater challenge tests performed on hatchery stocks of chinook and coho salmon in 1977. Fish. Mar. Serv. Tech. Rep. 761, 19 pp. Dehadrai, P.V. (1966). Mechanisms of gaseous exophthalmia in the Atlantic cod. Gadus morhua L. J. Fish. Res. Bd. Can. 23: 909-919. Eckroat, L.R., Wright, J.E. (1969). Genetic analysis of soluble lens proteins polymorphism in brook trout, Salvelinus fontinalis. Copeia (3): 466-473. Elkan, E. (1962). Dermocystidium gasterostei nsp. a parasite of Gasterosteus aculeatus L. and Gasterosteus pungitius L. Nature (London) 196: 958-960. Ewing, R.D., Hemmingson, A.R., Everson, M.D., Lindsay, R.L. (1985). Gill (Na+K)-ATPase activity and plasma thyroxine concentrations do not predict time of release of hatchery coho (Oncorhynchus kisutch) and chinook salmon (Oncorhynchus tschawytscha) for maximum adult returns. Aquaculture 45: 359-373. Folman, L.C., Dickhoff, W.W., Mahnken, C.V.W., Waknitz, F.W. (1982). Stunting and pass-reversion during smoltification of coho salmon (Oncorhynchus kisutch). Aquaculture 28: 45-373. Ghittino, P. (1965). Viral hemorrhagic septecemia (VHS) in rainbow trout in Italy. Ann. N. Y. Acad. Sci. 126: 468-478. Ghittino, P. (1975). Rilieve clinici e patologici su un case di Cattarata Verminosa in Trotelle iridee d’alevamento. Riv. Italia Piscic. Ittiop. 10: 59-61. Gorbman, A., Dickhoff, W.W., Mighel, J.L., Prentice, E.F., Waknitz, F.W. (1982). Morphological indices of developmental progress in the Parr-smolt coho salmon, Oncorhynchus kisutch. Aquaculture 28: l-19. Hall, D.L., Iverson, E.S. (1967). Henneguya lagodon, a new species of myxosporidian parasitizing the pin&h Lagodon rhomboides. Bull. Mar. Sci. 17: 274-279. Hoffert, J.R. (1766). Observations on ocular fluid dynamics and carbonic anhydrase in tissues of lake trout (Salvelinus namaycush). Comp. Biochem. Physiol. 17: 107-l 14. Hughes, R.C., Hall, F.G. (1928). Studies on the Trematoda family Strigeidae, XVI. Diplostomium huronese. Pap. Mich. Acad. Sci.: 10. Klune. J.P. (1965). A aranulomatous disease of fish oroduced by flavobacteria. Pathol. Vet. 2: 545-552. Knapp, P. (1900). Zur Heilung von Linsen wunden beim Fisch. Z. Augenheilkunde 3: 510-518. Kohbara, J., Murachi, S., Nanba, K. (1987). Vascular pattern of hyaloid vessels in carp eye. Nippon Suisan, Gakkaishi 53: 219-222. Kubota, S.S. (1976). Cataract in fishes: Pathological changes in the lens. Fish. Pathol. 10: 191-197. Leibovitz, L., Riis, R.C. (1980). A viral disease of aquarium fish. J. Am. Vet. Med. Assoc. 177(5): 414-416. McLean, D.G., Yoder, W.G. (1970). Kidney disease among Michigan salmon in 1967. Prog. Fish Cult. 32: 26-30. Mahnken, C., Prentice, E., Waknitz, W., Moran, G.,

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