Investigating the etiology of ocular changes in Monodactylus argenteus housed in a shoaling ring exhibit

Nicole E. Himebaugh Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, NC

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R. Kent Passingham Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, NC

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Megan L. Cabot Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, NC

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Christopher Gaudette Department of Population Health and Pathobiology, College of Veterinary Medicine, North Carolina State University, Raleigh, NC

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LaTisha N. Knight Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, NC

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Gregory A. Lewbart Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, NC

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Abigail R. Armwood Department of Population Health and Pathobiology, College of Veterinary Medicine, North Carolina State University, Raleigh, NC

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Annie Oh Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, NC

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Abstract

OBJECTIVE

To evaluate the pathologic ocular changes in a population of aquarium-housed Monodactylus argenteus and investigate potential underlying causes for the large number of affected fish in this exhibit.

ANIMALS

11 Monodactylus argenteus were evaluated from a shoaling ring exhibit within an aquarium, and 19 control fish without ocular abnormalities were obtained from commercial fish suppliers.

METHODS

Physical and ocular examinations were performed antemortem. Postmortem samples of liver, heart, dorsal epaxial muscle, and lenses of affected and control fish were analyzed for amino acid profiles. The aqueous humor from affected and control fish was collected postmortem, and osmolality was analyzed. Tissues from affected and control fish were submitted for histopathology.

RESULTS

Ocular abnormalities in affected fish included corneal lesions, cataracts, lens capsule rupture, and unilateral left-sided lens luxation and buphthalmos. Lens luxation and buphthalmos were directly correlated. Aqueous humor osmolality in control fish differed significantly compared to affected fish but was not correlated to lens abnormality score. Affected fish had significantly lower lens concentrations of arginine, asparagine, glycine, isoleucine, serine, and tyrosine than control fish. One affected fish had severe buphthalmos, cataracts, and panophthalmitis caused by gram-positive cocci.

CONCLUSIONS

Cataracts and traumatic lesions were common in affected M argenteus. Dietary amino acid content and aqueous humor osmolality imbalances were not likely a cause of the cataracts. Differences in lens amino acid concentrations between affected and control fish may be related to cataract formation.

CLINICAL RELEVANCE

Consideration of species-appropriate tank parameters may mitigate ocular lesions including cataracts in aquarium fish.

Abstract

OBJECTIVE

To evaluate the pathologic ocular changes in a population of aquarium-housed Monodactylus argenteus and investigate potential underlying causes for the large number of affected fish in this exhibit.

ANIMALS

11 Monodactylus argenteus were evaluated from a shoaling ring exhibit within an aquarium, and 19 control fish without ocular abnormalities were obtained from commercial fish suppliers.

METHODS

Physical and ocular examinations were performed antemortem. Postmortem samples of liver, heart, dorsal epaxial muscle, and lenses of affected and control fish were analyzed for amino acid profiles. The aqueous humor from affected and control fish was collected postmortem, and osmolality was analyzed. Tissues from affected and control fish were submitted for histopathology.

RESULTS

Ocular abnormalities in affected fish included corneal lesions, cataracts, lens capsule rupture, and unilateral left-sided lens luxation and buphthalmos. Lens luxation and buphthalmos were directly correlated. Aqueous humor osmolality in control fish differed significantly compared to affected fish but was not correlated to lens abnormality score. Affected fish had significantly lower lens concentrations of arginine, asparagine, glycine, isoleucine, serine, and tyrosine than control fish. One affected fish had severe buphthalmos, cataracts, and panophthalmitis caused by gram-positive cocci.

CONCLUSIONS

Cataracts and traumatic lesions were common in affected M argenteus. Dietary amino acid content and aqueous humor osmolality imbalances were not likely a cause of the cataracts. Differences in lens amino acid concentrations between affected and control fish may be related to cataract formation.

CLINICAL RELEVANCE

Consideration of species-appropriate tank parameters may mitigate ocular lesions including cataracts in aquarium fish.

The Silver Moony is a popular tropical fish in the family Monodactylidae and is native to Indo-Pacific waters.1,2 It is a brackish-water teleost fish that can survive in marine or freshwater and typically migrates to spawn in saltwater. They are omnivores, naturally feeding on plankton, detritus, and small decapods, and prefer to swim in schools. Monodactylus argenteus are shown to have excellent salinity tolerance making them good aquarium specimens.3

Cataracts, in addition to progressive ocular abnormalities, were observed in a school of aquarium housed M argenteus living in a uniquely shaped shoaling ring aquarium tank over 5-plus years. In general, the affected fish were in good body condition and exhibited normal swimming and feeding behaviors. The overall mortality rate was considered normal or better than normal for most large public aquarium marine exhibits.

Lenticular changes in teleost fish have been extensively studied within the aquaculture setting as these lesions decrease life quality and result in economic losses.46 There are many reports of a high prevalence of cataracts in groups of farmed salmonids related to environmental, genetic, infectious, toxicological, and nutritional factors.7,8 Notably, histidine, an essential amino acid that is transformed to N-acetylhistidine within the lens, has been identified as a key preventative dietary factor in the development of cataracts in Atlantic salmon smolt.4,5,9

The goal of this study was to evaluate the pathologic ocular changes in the aquarium housed M argenteus and to investigate possible underlying causes for the large number of affected fish in this single aquarium. We hypothesized that the ocular changes are due to either nutrition, specifically inadequate histidine in the diet, or osmotic imbalances resulting in increased osmolality of aqueous humor in the affected fish. The results of this study will help provide husbandry recommendations to improve the health and welfare of the fish in this style of aquarium exhibit and insight into cataract formation in aquarium fish.

Methods

Animals

Affected M argenteus fish (n = 11) were obtained from the SEA LIFE Aquarium. Acquired by the aquarium in 2016, the adult Monodactylus were approximately 6 years old at the time of this study. They were housed in a 360° shoaling ring saltwater exhibit with a total water volume of 21,500 L. The tank was ring-shaped with glass forming the inner wall and solid acrylic forming the outer wall. The depth of the tank was 1.6 m, and the width of the corridor that the fish swam through was 0.6 m. The Monodactylus tended to school and swam counterclockwise with their left side facing the glass and their right side facing the wall. This was promoted by a continuous, singularly directed counterclockwise laminar flow weak enough for the fish to comfortably swim with and against it. The average water temperature of the exhibit ranged from 24.4 to 25 °C. The tank light cycle was 11 hours on and 12.5 hours off with 15 minutes of dim lighting at each transition time. Exhibit lighting consisted of 2 types of light-emitting diodes: the first was strong, focused blue spotlights dispersed around the tank, and the second was sets of narrow strip lights comprised of small white and blue diodes.

Water quality was checked weekly. Historically, the tank experienced elevated nitrate levels of 450 ppm due to an insufficient nitrate removal process. A new denitrification system was added in 2022 before the start of this study. The tank was cleaned on a routine schedule. Aquarists dived to deep clean the tank every 2 weeks, which consisted of scrubbing tank structures, removing clam shells used for feeding, and rearranging tank décor.

Approximately 140 M argenteus were in the exhibit, of which 60% to 75% were estimated to have progressive ocular changes first observed 2 years before this study. The tank also hosted 1 golden damselfish (Amblyglyphidodon aureus), 1 saddle anemonefish (Amphiprion ephippium), 1 tomato clownfish (Amphiprion frenatus), 2 spotfin butterflyfish (Chaetodon ocellatus), 2 oblique-lined dottyback (Cypho purpurascens), and 1 Caribbean spiny lobster (Panulirus argus), which were not affected by obvious ocular abnormalities. The M argenteus were fed a varied diet on a rotating schedule comprised of the following: commercial fish gel, small bay scallops, minced fish, krill, mysis shrimp, and live brine shrimp. A marine formulation supplement (Vita chem; Boyd Enterprises) was added to the food.

Ten of the affected M argenteus fish were transported to North Carolina State University College of Veterinary Medicine from the aquarium inside double-layered poly bags filled with aquarium water and placed in an insulated cooler. During a separate visit, 1 additional affected Monodactylus was euthanized at the aquarium and submitted for histopathology immediately after euthanasia. Control M argenteus fish (n = 19) were acquired from LiveAquaria aquatics supplier. These fish were reared in brackish water in their early life stage per their natural life cycle10 and shipped via next-day air. The time from the acquisition of the fish to sampling was reduced as much as possible to avoid additional stress.

Salinity (ppt), total solids (g/L), and specific gravity of the home tank water for affected aquarium and control fish were measured using a refractometer (A300CL; Atago). The pH and dissolved oxygen (DO) were measured using a handheld multimeter (HQ40d; Hach). The ammonia, nitrite, and nitrate of the system were measured using a benchtop spectrophotometer (3900; Hach).

Clinical examination

All fish were handled per IACUC guidelines and Guidelines for Ethical Research in Veterinary Ophthalmology, and the experimental protocol was approved by to North Carolina State University College of Veterinary Medicine. Before handling, fish were anesthetized with tricaine methanesulfonate (MS-222; Western Chemical Inc) buffered with equal parts (1:1) sodium bicarbonate at a final concentration of at least 250 mg/L. After about 10 minutes of immersion in buffered MS-222, the intraocular pressures (IOPs) of 9/11 affected fish were measured by rebound tonometry (Tono-Vet; iCare) with the fish held in an upright position out of water. One fish was euthanized before IOP was obtained, and 1 fish was euthanized by the aquarium before an examination could be performed. Intraocular pressures were measured using the “dog/cat” tonometer setting, and the lowest pressure reading was taken. Pressure readings of the control fish were not performed due to the small size of the eye.

Following sedated examination, all fish were euthanized per the AVMA euthanasia guidelines in a 2-step immersion and pithing process.11 The fish were reimmersed in buffered MS-222 until opercular movement and heartbeat were lost, and then the spinal cord was severed caudal to the skull using Mayo scissors. Immediately after euthanasia, fish were weighed, and a physical examination was performed taking note of any abnormalities of the fins and skin. The sex of the fish was recorded, if possible, based on the presence or absence of ovaries.

Ocular examinations were performed with slit lamp biomicroscopy (SL-17; Kowa) and any ocular abnormalities were noted. The degree of lens abnormalities was graded on a scale of 0 to 4 using scoring methods previously described in farmed fish to account for the presence of lens luxation or buphthalmos.12 The grading scheme was as follows: 0, no cataract; 1, incipient cataract; 2, immature cataract; 3, mature cataract; and 4, any cataract with lens luxation or buphthalmos. A clear visual axis was present in 3/11 affected fish; fundic exams and imaging (RetCam II; Clarity Medical Systems) were completed in these fish. One of the control fish had spectral domain optical coherence tomography (SD-OCT; Bioptigen Inc) imaging performed of the retina. Imaging this fish using the RetCam II was unsuccessful due to the small size of the eye.

Histopathology

The whole body of 1/19 control fish and 4/11 affected fish were submitted for histopathology. During preparation for fixation, the heads were transversely sectioned just caudal to the eyes and placed in a cassette, the coelomic viscera and the caudal aspect of the head were transversely sectioned and placed in cassettes, and the left body wall and tail caudal to the coelomic cavity were removed to enhance the Davidson fixative perfusion of tissues. Trimmed tissues were processed routinely, embedded in paraffin, sectioned at 5 µm, and stained with H&E and Gram stain. An additional section of the viscera of fish 8 was stained with Grocott Gomori methenamine silver to identify fungal organisms, a section of the eyes and head of fish 8 was stained with Von Kossa stain to highlight minerals, and a section of the viscera of fish 10 was stained with Ziehl Neelsen acid-fast stain to investigate for Mycobacterium sp. Fish 11 had both acid-fast and gram staining performed. Slides were scanned at 9,200 by a 3-D Histotech Midi digital scanner.

Aqueous humor osmolarity

After ocular examination, a sample of aqueous humor from each eye in 7/11 of the affected and 18/19 of the control fish was collected using a 27-g hypodermic needle attached to a 1-mL syringe. The highest possible volume of aqueous humor was collected per eye, and the sample was immediately transferred into a labeled 1.5-mL microcentrifuge tube. Aqueous humor samples for the control fish were combined in pairs (4 eyes from 2 fish per sample) due to the low aqueous humor volume in each eye.

The osmolarity of aqueous humor samples was analyzed at room temperature using a vapor pressure osmometer (VAPRO Vapor Pressure Osmometer Model 5600; ELITechGroup) and calibrated according to the user manual before each sample session. Each aqueous humor sample was 10 µL in volume. Measurements of osmolality were made in “normal” mode and recorded (mmol/kg). The mean and SD of aqueous humor osmolality were calculated for both the affected and control fish samples.

Amino acid analysis

In 7/11 affected fish and 6/19 control fish, fresh tissue samples of the liver, dorsal epaxial muscle, heart, and the whole lens from both eyes were collected postmortem. Samples of the liver, epaxial muscle, and heart weighed at least 5 mg each and were shipped overnight on ice on the day of collection to the University of California-Davis Molecular Structure Facility for amino acid analysis. A sample of the commercial fish gel fed to the affected fish from the SEA LIFE Aquarium was also sent for amino acid analysis.

To measure amino acid content, samples were first hydrolyzed for 24 hours in HCl and dried. The dried material was then analyzed using an amino acid analyzer (L-8800; Hitachi) with ion-exchange chromatography (Hitachi High-Technologies Corporation) to quantify 19 amino acids (Supplementary Table S1).13 The total mass of amino acid per sample recorded (mg/dry matter wt) was calculated, and the total weight of each amino acid was calculated as a percentage of the total protein within the sample (% wt/wt) for comparison purposes.

Statistical analysis

Data was analyzed using the computerized statistical software GraphPad Prism for Mac v9 (GraphPad Software Inc). For aqueous humor osmolality, lens abnormality grade, and lens amino acid composition data, the right and left eyes were averaged. The differences in aqueous humor osmolality between the control and affected M argenteus were compared using the Mann-Whitney U test. A Spearman correlation coefficient was computed to assess the linear relationship between aqueous humor osmolality and lens abnormality grade. Differences in the amino acid compositions of the lens, skeletal muscle, heart, and liver samples between control and affected fish were analyzed using the Mann-Whitney U test. Significance was set at P ≤ .05. Data are presented as mean ± SD.

Results

Water parameters

The water salinity of the home tank water of the control fish was 25 ppt, the total solids was 2.6 g/dL, and the specific gravity was 1.019. The water salinity of the aquarium water of the affected fish was 33 ppt, the total solids was 3.2 g/dL, and the specific gravity was 1.025. Additional water parameters for the affected fish were as follows: pH, 7.34; DO, 96.2%; ammonia, 0 ppm; nitrite, 0.06 ppm; and nitrate, 224.5 ppm.

Clinical examination

No physical or ocular abnormalities were noted in the control fish on slit lamp biomicroscopy exam or SD-OCT imaging (Figure 1). For the control fish that were weighed (n = 18), weights ranged from 2.06 to 5.31 g with a mean of 2.97 ± 0.74 g. The SD-OCT imaging of a control fish retina identified the inner retina, outer nuclear layer, and outer retina. Due to small size and immaturity, the IOP and sex of the control fish could not be determined.

Figure 1
Figure 1

Control Monodactylus argenteus fish (A) and its left eye (B). C—Spectral domain optical coherence tomography image of the retina of a control fish. The inner retina (IR; red), outer nuclear layer (ONL; green), and outer retina (OR; blue) are labeled within the spectral domain optical coherence tomography image.

Citation: Journal of the American Veterinary Medical Association 2024; 10.2460/javma.24.05.0346

Signalment, IOP, physical and ophthalmic exam, and histopathology findings of the affected M argenteus are reported (Supplementary Table S2). Most of the affected fish had adequate body condition and no obvious bodily external injuries. Aquarists noted that fish 1 was considered a “poor-doer” and easily captured, while affected fish 5 had skin abrasions on the face. For the affected fish that were weighed (n = 10), weights ranged from 41.5 to 114.5 g with a mean of 60.1 ± 22.16 g. The sex of 10/11 affected fish were identified and included 6 females and 4 males. The IOP of 9/11 affected fish ranged from 3 to 20 mm Hg with a mean of 7.22 ± 4.31 mm Hg; the left eye in fish 10 had an IOP of 20 mm Hg.

In the affected M argenteus fish that received an ocular exam (n = 10), the lens could be evaluated in 19/20 eyes and cataracts were noted in all 19/19 (100.0%) eyes (Figure 2): 11/19 (57.9%) eyes had incipient cataracts, 6/19 (31.6%) eyes had an immature cataract, and 2/19 (10.5%) eyes had a mature cataract. The lens in the left eye of fish 2 could not be visualized due to posterior lens luxation. Additional ocular abnormalities affected 13/20 of examined eyes (65.0%): 6/20 (30.0%) eyes had corneal lesions (fibrosis, retrocorneal membranes, haze, and bulla), 6/20 (30.0%) eyes were buphthalmic, 6/20 (30.0%) eyes had posterior lens luxation, 3/20 (15.0%) eyes had aqueous flare, hyphema, and/or fibrin, 2/30 (10.0%) eyes had iridal hemorrhage, 2/20 (10.0%) eyes had anterior/posterior synechia, and 1/20 (5.0%) eyes had an iris cyst. Clinical signs of intraocular inflammation affected 5 (83.3%) left eyes out of the 6 eyes affected by uveitis. Buphthalmos and posterior lens luxations were also only observed in the left eyes of affected fish. Furthermore, all fish with buphthalmos (n = 6) had a posterior lens luxation and all fish with a posterior lens luxation (n = 6) were buphthalmic. Buphthalmos was not associated with an increase in IOP in affected fish. Fundus exam with retinal imaging of 3 affected fish revealed the suspected falciform process.

Figure 2
Figure 2

Ocular exam findings in affected Monodactylus argenteus fish. A—Anterior cortical incipient cataract (white arrow) in fish 3. B—Early immature cataract (white arrow) in fish 1 with corneal bulla (white arrowhead). C—Buphthalmos (black arrow) in fish 6. D—Posterior lens luxation (white arrow) in fish 6. E—Iridal hemorrhage (white arrow) in fish 2. F—Retcam II fundus imaging in fish 9 revealed the suspected falciform process (*).

Citation: Journal of the American Veterinary Medical Association 2024; 10.2460/javma.24.05.0346

Histopathology

Three affected fish had lymphocytic and granulocytic keratitis, which was most severe in fish 8. Anterior synechia and anterior lymphocytic uveitis were observed in both eyes of fish 8 in addition to an antemortem lens capsule rupture with associated cataractous change in the left eye (Figure 3). Cataractous changes, such as Morgagnian globules, bladder cells, epithelial hyperplasia, and posterior lens epithelial cell migration, were appreciated in fish 9, 10, and 11 on histopathology. The iridocorneal angle of fish 11 was expanded and occluded by macrophages, cellular debris, and erythrocytes. For this fish, the entire uveal tract, entire retina, and multifocal areas of the sclera were infiltrated and effaced by abundant macrophages and lymphocytes indicative of panophthalmitis. Gram staining of fish 11 revealed abundant gram-positive cocci, while gram staining of the other affected fish was negative.

Figure 3
Figure 3

Histopathology of various ocular structures from a control and affected fish (H&E stain). A—Normal anatomical structures from a control fish: fused eyelids (E), cornea (C), iris (I), lens (L), scleral cartilage (SC), retina (R), and choroid rete (CR) (scale bar = 700 µm). B—The lens (L) and lens capsule rupture in fish 8 with coiling of the lens capsule (LC) (scale bar = 400 µm). Note the extruded eosinophilic lens material (*). C—Cataract in fish 9 with Morgagnian globules (^) (scale bar = 60 µm). D—gram-positive cocci, neutrophils, and macrophages from fish 11 diagnosed with panophthalmitis (scale bar = 20 µm).

Citation: Journal of the American Veterinary Medical Association 2024; 10.2460/javma.24.05.0346

Fish 10 and 11 had multifocal granulomas within the intestines, mesentery, or kidneys measuring up to 0.07 mm in diameter. Ziehl-Neelsen acid-fast stain was applied to slide sections containing the granulomas, and no acid-fast bacilli were seen.

Aqueous humor osmolality

One of the pooled control fish aqueous humor samples could not be read by the osmometer making a total of 8 usable values. Individual aqueous humor samples from each eye of 7 affected fish were obtained (14 aqueous humor samples). The mean osmolality of the aqueous humor of the control fish was 265.13 ± 29.81 mmol/kg, ranging from 229 to 333 mmol/kg. The mean osmolality for the affected fish was 350 ± 10.39 mmol/kg, ranging from 325 to 364 mmol/kg. There was a significant difference between the aqueous humor osmolality of the affected fish and control fish (P = .0003; Figure 4).

Figure 4
Figure 4

A—Mean, SD, and range of aqueous humor osmolality of control (black squares) and affected (white circles) Monodactylus argenteus. Affected fish had significantly higher aqueous humor osmolality compared to the control fish (P = .0003). B—Correlation of aqueous humor osmolality vs lens abnormality grade (rs = −0.1793; P = .705). There was no significant correlation between aqueous humor osmolality and lens abnormality grade as determined by the Spearman correlation coefficient. ***P ≤ .001.

Citation: Journal of the American Veterinary Medical Association 2024; 10.2460/javma.24.05.0346

Spearman correlation coefficient assessed the relationship between aqueous humor osmolality and lens abnormality grade in averaged right and left eyes of 7 affected fish. Lens abnormality grading was as follows: grade 0: 0 eyes; grade 1: 2 eyes; grade 2.5: 4 eyes; and grade 3: 1 eye. Results revealed a rs value of −0.1793 (P = .705), suggesting there was no correlation between aqueous humor osmolality and lens abnormality grade.

Amino acid analysis

Whole lenses, and tissue samples of the heart, liver, and dorsal epaxial muscle from 6/19 control fish and 7/11 affected were analyzed for 19 different amino acids (Figure 5). The lenses of the affected fish had significantly lower levels of asparagine (P = .0175), serine (P = .0175), glycine (P = .0163), isoleucine (P = .0175), tyrosine (P = .0175), and arginine (P = .0128) compared to the control fish. The concentration of phenylalanine in the heart tissue was significantly higher in the control fish than in the affected fish (P = .0350). The liver and skeletal muscle tissue samples did not differ in amino acid concentration between the affected and control fish. The lenses from the affected fish had a smaller total weight composition of amino acids (P = .0146) compared to the control fish. An analysis of the commercial fish food fed to affected fish for amino acid content is also provided (Supplementary Table S3).

Figure 5
Figure 5

Mean and SD of amino acid concentrations of lens (A), heart (B), and total weight as a percentage of total proteins of lens (C) in control (n = 6; gray columns) and affected (7; white columns) Monodactylus argenteus. Arg = Arginine. Asx = Asparagine. Gly = Glycine. Ile = Isoleucine. Phe = Phenylalanine. Ser = Serine. Tyr = Tyrosine. *P ≤ .05.

Citation: Journal of the American Veterinary Medical Association 2024; 10.2460/javma.24.05.0346

Discussion

This is the first known study investigating ocular changes in a group of M argenteus, an ornamental teleost fish popular in the aquarium industry. Results revealed that all affected Monodactylus fish sampled had cataractous changes. Most had bilateral involvement, and the most common stages were incipient (57.9%) and immature (31.6%). Sixty-five percent of affected fish eyes had other ocular abnormalities: unilateral or bilateral superficial corneal lesions, unilateral buphthalmia, posteriorly luxated lenses, and/or uveitis disproportionately affecting the left eyes. Cataracts in teleost fish have been attributed to several etiologies with bilateral involvement resulting from abnormal water quality, osmotic imbalances, nutritional imbalances, infectious diseases, inappropriate water temperature, UV radiation exposure, and genetic predisposition.36,1419

Water quality parameters are important in the health of aquarium fish, as cataract formation has been seen with increased environmental salinity in salmon.17 Increased salinity can cause organ stress and dysregulation of systemic osmolality if the osmoregulatory mechanisms are overwhelmed.20,21 In the wild, M argenteus spend early life in brackish water and adulthood in saltwater with reported optimal salinities of 15 ppt for juvenile M argenteus,3 20 to 35 ppt for rearing,3 and 35 ppt for spawning adults.2 Monodactylus argenteus are also tolerant of sudden changes in environmental salinity with a 100% survival rate.1 In this study, the salinity of the brackish water of the juvenile control fish was 25 ppt, and the salt water of the adult affected fish was 33 ppt, both of which are reportedly tolerated by this species. The acclimation period of the affected fish is not known, and currently, there is no literature linking acclimation time and cataract formation in fish.

Total solids, specific gravity, pH, DO, ammonia, and nitrites were within the expected range for marine and brackish water environments for the affected and control fish, respectively.22 Before and during the study, the affected fish were exposed to high nitrate levels (> 200 ppm); the recommended range is < 50 ppm.22 Elevated nitrate levels have not been associated with cataract formation in Atlantic salmon23 but have been associated with blindness without gross ocular lesions in hybrid striped bass24 and death in multiple species.22 Thus, it was unlikely that elevated nitrates were the cause of cataracts and ocular changes in the affected M argenteus, but it cannot be completely ruled out.

Lens opacities can also result from osmotic imbalances as influx of electrolytes or loss of water directly through the cornea may contribute to an increased osmolality of aqueous humor in fish.17,25 In this study, the aqueous humor osmolality was significantly higher in the affected M argenteus (350 ± 10.39 mmol/kg) compared to the controls (265.13 ± 29.81 mmol/kg). However, when aqueous humor osmolality values were compared to other euryhaline species, it was unlikely that osmotic imbalances caused cataracts and ocular changes in the affected M argenteus.6,17,26,27 Furthermore, there was no significant correlation between aqueous humor osmolality and lens abnormality grade. The significant difference between the aqueous humor osmolality of the affected versus control fish was most likely due to the water parameters and is expected to be tolerated in this life stage of euryhaline fish.

Lenticular abnormalities in fish may result from an amino acid imbalanced diet. Amino acids are building blocks for protein and regulate essential cellular functions in an animal, such as lens metabolism.6 In aquaculture fish, amino acids have been described in 3 groups: (1) essential amino acids (arginine, histidine, isoleucine, leucine, lysine, methionine, phenylalanine, threonine, tryptophan, and valine, which cannot be synthesized by the animal and thus is acquired through diet; (2) nonessential amino acids (alanine, asparagine, aspartate, glutamate, glycine, serine, and tyrosine), which are synthesized by the animal; and (3) conditionally essential amino acids (cysteine, glutamine, hydroxyproline, proline, and taurine), which must be provided from the diet when rates of utilization are greater than rates of synthesis.28

When comparing essential amino acids in this study, 2 amino acids (isoleucine, and arginine) in the lens and 1 amino acid (phenylalanine) in the heart were significantly lower in the affected versus control M argenteus. Isoleucine plays a role in protein metabolism and affects fish growth.29,30 Arginine partakes in insulin and glucose metabolism in fish31,32 and has antioxidant properties, which are important in cataract prevention.18,33,34 Phenylalanine is required for protein synthesis and growth in young fish.28,35 Interestingly, the percentage of isoleucine (2.90% wt/wt) and phenylalanine (2.48% wt/wt) in the diet of the affected M argenteus were within or above the recommended feeding range for farm-raised fish; isoleucine is 0.90% to 3.58% wt/wt and phenylalanine is 1.79% to 2.1% wt/wt.30,36,37 The percentage of arginine in the diet of the affected fish (3.47% wt/wt) was below the recommended feeding requirement for most farm-raised fish, but within the normal range for some species (3.00% to 8.10% wt/wt).33 Studies assessing the recommended range and effects of dietary arginine in M argenteus are needed. Contrary to our hypothesis, histidine levels in the lens, liver, dorsal epaxial muscle, and heart were not significantly different between the affected and control M argenteus. The percentage of histidine in the diet of the affected fish (2.04% wt/wt) was also within the recommended minimum for cultivable fish (0.9% to 4.8% wt/wt) and above the minimum for most of the listed species.38 In this study, an amino acid-imbalanced diet was a less likely cause of cataracts and other ocular abnormalities. It is possible that the affected M argenteus may have been unable to adequately access or ingest enough food due to the tank design and/or vision deficits.

The levels of 4 nonessential amino acids, asparagine, serine, glycine, and tyrosine were significantly lower in the lens of affected versus control M argenteus. Glycine is reported to be useful in muscles for changes in water balances19 and plays a role in osmoregulation and glucose scavenging, mitigating cataract formation in humans and other mammals.39 Serine is reported to be an important component of ocular oxygen metabolism in humans,40 and tyrosine is important in fish for growth, neurotransmission, and hormone regulation.28 Low levels of these nonessential amino acids have not been associated with the formation of cataracts. The total weight as a percentage of protein in the lens was significantly lower in the affected versus control fish. Therefore, rather than being part of a major underlying mechanism, low levels of asparagine, serine, glycine, and tyrosine may be a sequela of cataract formation.41

Bacterial-induced endophthalmitis was identified in 1 fish; gram-positive cocci were identified on histopathology in fish 11. Although culture was not performed, Streptococcus sp or Lactococcus sp have been associated with buphthalmos and cataracts in fish as well as iridal hemorrhage.42,43 Other infectious agents, such as Diplostomum (the eye fluke),44 helminth infections,44 and various other bacteria,42 are reported to cause cataracts in fish.

Other potential factors in the formation of bilateral cataracts in fish that were not evaluated include changes in water temperature, UV radiation exposure, age, and hereditary factors. Higher water temperatures during the rearing stages of fish may increase the incidence of cataracts, moreover, if the diet is not ideal.18,19 However, the temperature in the 360° shoaling ring saltwater exhibit was strictly controlled at 24.4 to 25 °C, which was appropriate for the juvenile and adult M argenteus.45 Exposure to UV light in aquaculture, such as UV tank sterilizers, has been associated with cataract formation in juvenile cod,14 but the fish in this study were not exposed to UV radiation while cleaning. Age-related lens changes have not been identified in fish as a sole cause of cataract formation.46 There are also no known inherited risk factors for cataracts in M argenteus.

Following lenticular opacities, the next prominent ocular abnormalities in the affected M argenteus were unilateral buphthalmia, posteriorly luxated lenses, and/or uveitis predominantly affecting the left eyes. Interestingly, all buphthalmic eyes in affected fish had posteriorly luxated lenses and all eyes with posteriorly luxated lenses were buphthalmic, suggesting chronic buphthalmia leading to secondary lens luxation.

Common causes of unilateral buphthalmia in fish are trauma and neoplasia, with trauma-induced uveitis being the most likely primary cause in the affected M argenteus.22,42,44 First, neither ocular nor systemic neoplasia was reported on histopathology of the affected fish. Second, lesions associated with trauma involving the cornea (corneal fibrosis, bullae, and retrocorneal membrane) and uvea (aqueous flare, iridal hemorrhage, fibrin, hyphema, and posterior synechia) were found on examination and histopathology in several of the affected fish. While corneal lesions occurred unilaterally or bilaterally, unilateral buphthalmia, posteriorly luxated lenses, and/or uveitis predominantly observed in left eyes. The counterclockwise swimming direction of the M encouraged by the shoaling ring aquarium exhibit with a narrow corridor may have predisposed the left eye of the fish to injury against glass, objects, or other fish.

Surprisingly, IOP was not elevated in bupthalmic eyes of the affected M argenteus fish. On the contrary, IOP was lower in the buphthalmic eyes (4.2 ± 1.17 mm Hg) compared to nonbuphthalmic eyes (8.38 ± 4.52 mm Hg). Overall, IOPs measured with rebound tonometry of the affected fish (7.94 ± 5.66 mm Hg) were similar to previously reported mean IOPs in unaffected brook trout (8.82 mm Hg oculus dexter and 9.20 mm Hg oculus sinister) but higher than in unaffected koi (4.9 mm Hg).47,48 Only 1 eye with an incipient anterior cortical cataract had mildly elevated IOP (20 mm Hg). The effect of anesthesia on IOP in M argenteus is unknown. Buphthalmic eyes have been described in fish afflicted with gas bubble disease however, no signs of gas bubble disease were apparent in the affected fish within this population.22 The cause for buphthalmos in our study was likely related to chronic, end-stage intraocular disease.14,49

There were several limitations of the current study. A direct comparison of age-matched affected and control fish was not available, and the size of the control fish made it impossible to analyze individual aqueous humor samples and IOP. Amino acid composition could naturally vary with age in the Monodactylus. Additionally, the diet of the control fish was not evaluated due to a lack of access to a sample. Cysteic acid, methionine sulfonate, tryptophan, and taurine were not consistently measured because they were either absent, unstable, or too low to detect. Furthermore, N-acetylhistidine levels in the lens were not measured but may be useful in future studies. Additionally, elevated nitrate levels cannot be completely ruled out as a contributor to ocular changes and cataract formation in the fish. The suspected falciform process seen on fundic imaging was difficult to isolate histologically; therefore, verification of this structure on histopathology could not be achieved.

Overall, the results of the study revealed that the suspected causes of the ocular changes in these M argenteus were likely multifactorial: (1) trauma or (2) infection resulting in uveitis leading to secondary buphthalmia, cataract formation, and posteriorly luxated lenses. Osmotic imbalances and inadequate amino acid nutrition, including histidine, are unlikely causes of cataracts in the affected fish. The role of genetics, inappropriate acclimation periods, high nitrate levels, fluctuating water temperatures, or exposure to ultraviolet radiation on cataract formation cannot be ruled out. Consideration for ideal tank size, shape, and schooling density is also important. Future research involving a cohort study under different rearing conditions would be insightful.

Supplementary Materials

Supplementary materials are posted online at the journal website: avmajournals.avma.org.

Acknowledgments

The authors thank Erin Barr and Dr. Hans Westermeyer for image and OCT acquisition help. We also thank David Dorris and Dr. John Meitzen for their help with osmolality measurements and John Schulze for amino acid analysis measurements.

Disclosures

The authors have nothing to disclose. No AI-assisted technologies were used in the generation of this manuscript.

Funding

The authors have nothing to disclose.

ORCID

Nicole E. Himebaugh https://orcid.org/0000-0001-5874-5345

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