Article

Pathogenesis and epidemiology of spontaneous exophthalmos in the West Australian dhufish, Glaucosoma hebraicum Richardson

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Abstract

The West Australian dhufish, Glaucosoma hebraicum Richardson (family Glaucosomatidae) is a potentially valuable aquaculture species, but spontaneous exophthalmos is common in freshly caught and cultured dhufish. To investigate the epidemiology and pathogenesis of exophthalmos in tanks of wild-caught and captive-bred dhufish, records of culture conditions, the prevalence of lesions and pathological examinations were used to study the disease and associated environmental and management factors. Naturally occurring cases of exophthalmos that were examined were mostly unilateral and occurred more frequently in summer months during periods of increasing water temperature. In 15 affected eyes that were examined histologically gas bubbles and haemorrhages were consistently present in the choroid. In some, gas bubbles and haemorrhage were also present in retrobulbar tissues associated with perforation of the sclera. Oxygen concentrations were measured in 12 exophthalmic eyes and concentrations of 50–73% were recorded in gas bubbles in the anterior chamber of three of these that were acute cases. Very low oxygen tensions were recorded at the retinal–vitreal junction of four eyes with retrobulbar haemorrhages indicating that there may have been disruption of arterial blood supply to the choroid in chronic lesions or with perforation of the sclera. The results of experiments to determine the significance of exercise, high water temperature, sudden increases in light intensity, fish handling or tank cleaning indicate that exercise and/or high water temperature (25.5 °C) may be important risk factors for the development of exophthalmos in dhufish. Possible mechanisms for the formation of gas bubbles and haemorrhage in the choroid are discussed.

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... Acute exophthalmia due to unfavourable holding conditions has been reported to occur in juvenile cod kept in nitrogen-supersaturated water (Gunnarsli, Toften & Mortensen 2008) and during chronic CO 2 exposure (Moran et al. 2012). Stephens et al. (2001) found that excessive exercise and/or high water temperature may be important risk factors for the development of exophthalmia in West Australian dhufish Glaucosoma hebraicum Richardson. Dehadrai (1966) observed that 70% of trawlcaught cod gradually developed secondary uniand bilateral exophthalmia within 7 days after capture when kept in the laboratory. ...
... Gas emboli may also form as a result of lowered gas solubility when the pH is lowered due to an increase in lactate and carbon dioxide build-up (Parker et al. 2006). This can be caused by stress during capture (Stephens et al. 2001) and may affect the eye in particular due to the high retinal tensions. Hence, removal of the pseudobranch will cut the blood supply to the choroid gland and prevent secondary exophthalmia resulting from bloodborne gases. ...
Article
Capture-based aquaculture (CBA) of Atlantic cod (Gadus morhua) has become increasingly important in recent years, and increased attention is being paid to animal welfare issues linked to these activities. Earlier studies showed that some cod develop secondary exophthalmia in captivity. This study investigated the development of secondary exophthalmia in two groups of wild-caught cod, one of which was exposed to rapid decompression causing acute barotrauma (treatment group) while the other was not (control group). Photographs and radiographs before and up to 33 days after barotrauma revealed a significant increase in overall eye protrusion caused by an accumulation of gas in the orbita in the treatment group, first observed on day 9 after decompression, while no protrusions were observed in the control group. Barotrauma was thus identified as an important trigger for the development of secondary uni- or bilateral exophthalmia of wild-caught cod. Two underlying mechanisms are suggested, where the more likely is residual swim bladder gas taking the route of least resistance, while the less likely is the exsolution of gas from the blood. Our results have implications for a wide range of contexts in which cod are rapidly brought to the surface from great depth.
... As with the swim bladder lesions, the underlying cause is probably iatrogenic i.e., due to gas bubble disease induced by transporting the fish to the surface after capture in deep waters. However, spontaneous exophthalmia associated with gas bubbles in the eyes was recently reported in West Australian dhufish (Glaucosoma hebraicum) that were reared from hatching in captivity as well as in wild-caught fish (Stephens et al., 2001). Moreover, we have seen an identical condition in ling cod (Ophiodon elongatus) that were hatched in captivity. ...
... Moreover, we have seen an identical condition in ling cod (Ophiodon elongatus) that were hatched in captivity. Stephens et al. (2001) concluded that the likely cause of the lesions in captive-reared dhufish (and some other deep-water marine fishes) was a reduced ability to adapt to rapid changes in activity patterns or water quality differences, even if hatched in captivity. Stephens et al. (2002) suggested that susceptibility of captive dhufish to exophthalmos may be related to oxygen transport problems in the retina due to intracellular acidosis in erythrocytes. ...
... Among the black jewfish landed from 15-20 m, 5% had exophthalmos (Figure 9.15). This condition may result from the enlargement of gas bubble nuclei within the eye and/or in retrobulbar tissues (Stephens et al. 2001). The factors initiating the formation of gas bubble nuclei are poorly understood despite their importance in supersaturated tissues in decompression sickness in humans (Stephens et al. 2001). ...
... This condition may result from the enlargement of gas bubble nuclei within the eye and/or in retrobulbar tissues (Stephens et al. 2001). The factors initiating the formation of gas bubble nuclei are poorly understood despite their importance in supersaturated tissues in decompression sickness in humans (Stephens et al. 2001). ...
... Retinal development (Shand, 2001); Aquaculture (Stephens et al., 2001;; Parasitism (Hesp et al., 2002b); Age and mortality estimation (Craine et al., 2009); Acoustic tracking ; Effects of sanctuary zones ; Identification of microsatellite markers (Burridge and England, 2009); Simulation modeling for exploring implications of alternative management, catch and behavioural characteristics (Burch, 2009;Hesp et al., 2010;; Barotrauma ). ...
... To our knowledge, the role of head shape and eye placement in mediating susceptibility to exophthalmia has not been investigated. However, fish with a large choroid body that secretes oxygen to the eye (similar to the rete mirabile in the swim bladder, Wittenberg and Wittenberg 1974) seem more susceptible to exophthalmia (Stephens et al. 2001). This has not been linked directly with decompression injuries, but rather with spontaneous exophthalmia under aquaculture conditions, which relates to the release of oxygen into the orbital cavity during stress-induced blood acidosis (Herbert et al. 2002, Wells andDunphy 2009). ...
Technical Report
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Within the Murray-Darling Basin (MDB) many species undertake extensive downstream migrations as eggs, larvae, juveniles or adults and passage through river infrastructure has been shown to impact on their survival. The relative contribution that different stresses (such as rapid decompression and fluid shear) make to overall injury and mortality remains poorly understood, and this in turn makes it difficult to assess the risk associated with infrastructure projects or to develop engineering and operation guidelines to manage the downstream fish passage risks. This report details laboratory experiments that were used to determine the tolerance of various species and life stages of fish from the MDB to rapid decompression (in hypo/hyperbaric chambers) and elevated fluid shear (in a shear flume). Fish were exposed over a wide range of conditions so that the probability of injury and/or mortality could be modelled. In doing this, the ultimate goal was to determine critical thresholds for injury and mortality and develop criteria that if applied would protect downstream migrating fish at river infrastructure. We present criteria in an attempt to better inform policy relating to the development and management of mini-hydropower and irrigation infrastructure for the protection of downstream migrating fish.
... pH) (Stephens et al. 2002). In these species, increased blood acidosis or carbon dioxide during stress can decrease the partial pressure in the choroid rete and increase oxygen diffusion into the orbital cavities (Stephens et al. 2001; Herbert, Wells & Baldwin 2002). However, this pathway has yet to be explored in relation to exophthalmia induced by decompression, which is generally explained by an alternative mechanism (Hannah et al. 2008b). ...
Article
This study assessed the effects of different retrieval depths (2, 10 or 20 m), surface intervals (none or 15 min) and release methods (untreated, vented or recompressed) on the incidence of external and internal clinical signs of barotrauma (ECSB and ICSB) and post-release mortality in golden perch, Macquaria ambigua (Richardson). Fish were assessed for ECSB before and after surface intervals and either monitored for mortality over 3 days in two deep cages or killed for internal examination. When all fish were left untreated, short-term mortality increased with retrieval depth from 0% and 4.2% among 2 and 10-m fish, respectively, to 19.2% among 20-m fish; while surface interval only affected the incidence of two ECSB (excess buoyancy and a prolapsed cloaca). Mortality was also greater among 20-m fish that were subjected to a 15-min surface interval and left untreated (22.2%) or vented (22.2%) than those that were recompressed (5.6%). Of the ECSB, only exophthalmia was associated with increased mortality, with half of the affected fish dying. However, many fish retrieved from 10 and 20 m also sustained numerous ICSB, including compressed gonads or vital organs and ruptured or collapsed, haemorrhaging swimbladders that remained deflated for up to 3 days after release.
... All of the external signs of barotrauma observed under normal fishing conditions were duplicated in the tanks at similar pressure changes. In addition to simple pressure change, there is evidence that stress induced during capture increases the severity of barotrauma, especially in the eyes (Stephens et al. 2001). Ability to resorb gas (especially nitrogen) is limited by characteristics of plasma, as modulated by pH and pressure (Wittenburg et al. 1964; Bridges et al. 1998). ...
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Fishes with closed swim bladders regulate buoyancy during depth changes by secreting and resorbing swim bladder gases. Forced ascent during fishery capture results in barotrauma caused by rapid expansion and exsolution of gases from body fluids. Pressure changes in hyperbaric chambers were used to examine changes in swim bladder integrity and acclimation rates in two ecologically different, yet congeneric, species: Black rockfish Sebastes melanops and China rockfish S. nebulosus. We also conducted simulated-capture experiments to investigate the relationship between capture in a fishery, barotrauma from pressure change, and survival after release. Black rockfish acclimated faster than China rockfish to both increases and decreases in pressure, but both species were much slower to acclimate than other physoclists, such as Atlantic cod Gadus morhua. Black rockfish required up to 48 h to acclimate from 4 atmospheres absolute (ATA; depth equivalent of 30 m) to surface pressure and required up to 168 h to become neutrally buoyant at 4 ATA after starting from surface pressure. In contrast, China rockfish required over 250 h to become neutrally buoyant at 4 ATA after starting from surface pressure. All black rockfish exposed to a 3-ATA decrease in pressure during simulated capture had ruptured swim bladders. However, mortality from simulated capture and subsequent recompression was low; only 3.3 ± 1.7% (mean ±SE) mortality was observed after 21 d. In experiments with black rockfish, rapid recompression reversed visible barotrauma, suggesting that a quick return to depth could be used to minimize mortality of discarded black rockfish in nearshore fisheries.
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Fish eyes syndrome is often one of the causes which induce difficulties in the life of both wild and cultured fish. The clinical fish eye syndrome is either local or systemic. The most common syndromes affecting wild fish are exophthalmos (pop-eye) and cataracts while those recorded in cultured one are exophthalmos, cataracts and enophthalmos (sunken-eye). The syndrome is associated with various infectious causes such as parasitic, chemical, mechanical, traumatic and hormonal imbalance. The epidmiolgy of these syndromes depends on the cause of infection of the eye in both wild and cultured fishes of all species and ages. Also, the diagnosis of these syndromes depends on: case-history, behavioral abnormalities and clinical examination (clinical signs and laboratory diagnosis). Histopathological examinations of eye syndromes affecting wild and cultured fish are graded from inflammation in acute form (traumatic causes) to cataracts and keratitis in chronic form (parasitic causes), retro-retinal gas bubbles (GBD). Prevention and control of fish eyes' syndrome depends on strict hygienic measures including the use of profilactic treatment of parasitic and biological control. Treatment and removal of the causative agent are considered to be the most important factor in treating these diseases. In conclusion, eye affection syndrome is a group of non specific clinical signs which are associated with various infectious and non infectious diseases and the best approach to occular disease is the prevention or avoidance through either strict hygienic measures or treatment and removal of the causative agent.
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To better understand the possible role of deoxygenation of haemoglobin in the pathogenesis of exophthalmos in the West Australian dhufish, Glaucosoma hebraicum Richardson, some oxygen transport properties of haemoglobin from this species were determined and compared with haemoglobin from black bream, Acanthopagrus butcheri (Munro), snapper, Pagrus auratus (Bloch & Schneider) and King George whiting, Sillaginodes punctata (Cuvier). Dhufish had a single haemoglobin with a pronounced Root effect. Snapper and black bream blood had six and five types of haemoglobin, respectively. The magnitude of the Root effect of haemoglobins in the haemolysate was demonstrated by comparing oxygenation and total deoxygenation at pH 8 with relative deoxygenation at pH 6.9. Dhufish haemoglobin demonstrated a large Root effect, with the Root effect of King George whiting, snapper and black bream being of lesser magnitude. Deoxygenation of all haemolysates was more pronounced in the presence of adenosine triphosphate (ATP). Seasonal changes in haematological parameters and ATP content of dhufish blood were not evident. The Root effect is discussed in the context of its possible role in oxygen supply to the retina and adaptation to the fish's habitat and the environment.
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Hormone-induced spawning of the West Australian dhufish, Glaucosoma hebraicum (Glaucosomatidae) is reported, and the artificially-reared eggs and larvae are described. Hormones tested were hCG, Ovaprim and LHRH analogue, the last both as implants and in a saline solution. Late-stage fertilized eggs are spherical (960–1200 µm), possess a pigmented oil globule (210–273 µm) anteriorly on the unsegmented yolk, and hatch in about 32 hours at ~23˚C. Newly hatched larvae (1.75–2.10 mm) have a prominent yolk sac which is resorbed after 3.3 days. The mouth becomes functional from Day 3, first feeding occurs from Day 3.5 and the inflated gas bladder is first observed from Day 4.3. Larvae examined (1.75–8.13 mm) have a moderately deep body, 24–25 myomeres, early-forming pelvic fins that are heavily pigmented by the postflexion stage, small to moderate head spination, no gap between anus and anal-fin origin, and a distinct pattern of pigmentation. Notochord flexion occurs between 3.42 (15 days) and 4.83 mm (25 days), and the transition to the juvenile stage starts from ~8 mm (45–46 days). Comparisons with taxa with similar larvae show that Glaucosoma larvae share some similarities with pempherid larvae, although the evidence is not sufficient to strengthen the view that both groups are closely related.
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The Western Australian dhufish (Glaucosoma hebraicum), an open-water marine finfish, has been identified as a potential species for aquaculture and a 4 y research project has concentrated on broodstock collection and maintenance, spawning and larval rearing. This paper describes treatments which were developed for the ectoparasites and diseases of broodstock fish. These included bacterial and fungal infections, Cryptocaryon irritans, Haliotremasp., an unidentified axinid monogenean, the isopod Aega cyclops and copepod Caligus sp. Treatments based on betadine, formalin, freshwater, malachite green, oxytetracycline (terramycin), 2-phenoxyethanol, potassium permanganate and trichlorphon (neguvon) were all tried. The most effective treatments against parasites were a freshwater bath or a combined freshwater bath and anaesthesia with 2-phenoxyethanol. Monogeneans on the gills were difficult to control and exophthalmia was an unresolved problem.
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1.1. The Root effect was evaluated in hemolysates from 26 species of bony fish and 20 species of cartilaginous fish found on the Brazilian southeastern coast.2.2. Teleost Root shifts, with a single exception, are correlated with the presence of the choroid rete mirabile but not with its counterpart in the swimbladder.3.3. Five ray species displayed weak and moderate Root effects despite the absence of choroid and swimbladder rete.4.4. The presence and intensity of the Root effect is probably primarily related to the high oxygen demand of the retina and with the importance of visual perception in fish.5.5. In marine teleosts the magnitude of the Root effect seems to be associated with the presence and size of both the choroid rete and the pseudobranch.6.6. An antioxidant protection of the fish eyes can be advocated for the pseudobranch.
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The adult hemoglobins of 15 species of teleost and the midgestation fetal hemoglobin of the seaperch Embiotoca lateralis show a pronounced decrease in oxygen-carrying capacity at low pH, a Root effect. All of these fishes lack a functional swim bladder, which is generally thought to be the likely site of Root effect hemoglobin function. All of the teleosts examined, including the fetal sea perch, however, have a choroid rete, a structure that is proposed to be involved in oxygen secretion to the eye. The data are inconsistent with the generalization that only fishes with swim bladders possess Root effect hemoglobins, and that the only function of Root effect hemoglobins is in the secretion of oxygen to a swim bladder. The data for the fishes examined in this study suggests that a better correlation may exist between Root effect hemoglobins and the presence of a choroid rete. This is consistent with the hypothesis that Root effect hemoglobins may be involved in the physiology of the eye in many fishes.
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Two groups of healthy chinook salmon (Oncorhynchus tshawytscha) were experimentally exposed to gas supersaturated groundwater. Gross lesions consistent with gas bubble disease (GBD) developed. Vascular lesions associated with intravascular gas bubbles were examined with light and scanning electron microscopy. Dermal blood vessels containing gas bubbles were severely dilated. Additionally, the gas bubbles were spatially associated with endothelial lesions ranging from cellular degeneration to exfoliation. The resulting regions of exposed subendothelial connective tissue were sparsely covered by small unidentified adherent cells and strands of fibrin. In the light of these findings, the similarities in vascular pathology between GBD in fish and decompression disease in man are discussed, particularly with respect to the initiation of haemostatic disorders in both conditions.
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Ocular lesions associated with natural and experimental outbreaks of gas bubble disease (GBD) in commercial salmonids were assessed histologically and by scanning electron microscopy. Small gas emboli were first detected in the choroid gland of the posterior uvea. In subacute and chronic cases, bubble size increased markedly and localization in retrobulbar and periocular sites was favoured. During the acute phase of GBD, ocular lesions were limited to anatomical displacement of tissue and local degeneration of compressed tissues around the perimeter of bubbles. Subacute sequelae included the formation of anterior synechia, lens cataract, and suppurative panophthalmitis. During chronic stages, when large retrobulbar bubbles had caused severe exophthalmia, there was stretching of the optic nerve and of retinal blood vessels and severe distortion of the posterior aspects of the globe. The sequential development, pathogenesis and persistence of ocular lesions associated with GBD in fish are discussed.
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Young specimens of trout, catfish, sculpin and salamanders were equilibrated with elevated gas pressures, then rapidly decompressed to ambient pressure. The newly hatched forms tolerated extremely high gas supersaturations; equilibration pressures of 80-120 atm argon or 150-250 atm helium were required for in vivo bubble formation. During subsequent larval development, the equilibration pressures required decreased to just 5-10 atm and bubbles originated in the fins. Anesthetising older fish before decompression prevented bubble formation in the fins; this suggests that swimming movements mechanically initiate bubbles, possibly by a tribonucleation mechanism.
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Aggressive behavior and whole brain neurochemistry were measured in stable and unstable pairs of male Coturnix coturnix japonica. Aggressive pecking peaked on day 5 of the daily regrouping regime and returned to a basal level on day 14. Aggressive behavior was associated with increased brain norepinephrine (NE), dopamine (DA), and acetylcholinesterase (AChE) in unstable pairs. Habituation (12-15 days) and DA response to daily regrouping and inanition were inversely related in unstable and stable pairs respectively. Normal whole brain NE increases were attenuated in unstable pairs.
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Considering the presently available data it is clear that the Root effect represents an exaggerated alkaline Bohr effect which occurs in the absence of a normal acid Bohr effect and is associated with a loss of oxygen binding capacity at low pH. Undoubtedly at the molecular level the presence of a Ser residue at position F9(94) beta in these haemoglobin is of primary importance. No Root effect haemoglobin has yet been identified which lacks this substitution. On the other hand however many haemoglobins are known which possess this Ser residue and at the same time lack a Root effect. Other factors arising from interactions at other sites in the haemoglobin molecule are obviously sufficient to negate the otherwise stabilizing effect of this critical Ser residue. The loss of cooperativity of Root effect systems as the pH is lowered is readily explained as due to stabilization of the low affinity T state to such a degree that the switch to the high affinity R state is suppressed even in the fully liganded molecule. The observation of Hill coefficients of less than unity requires that within the T state chain heterogeneity exists such that the alpha and beta chain haems demonstrate significantly different affinities for ligand. The physiological role of Root effect haemoglobins is demonstrably not inevitably linked to the swim bladder but more probably arose from the need to oxygenate the poorly vascularized retina of many fishes.(ABSTRACT TRUNCATED AT 250 WORDS)
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Several current theories of decompression sickness (DCS) presume the preexistence of gas bubble nuclei in tissue, because the de novo nucleation of gas bubbles in the body is thought to be theoretically impossible. Reexamination of nucleation theory reveals the overwhelming importance of two parameters: gas supersaturation and tissue surface tension (gamma). For the high gamma of pure water nucleation theoretically requires more than 1,000 ATA supersaturation. Lower values of gamma allow nucleation to occur with vastly smaller supersaturations. Application of homogeneous nucleation theory can provide reasonable fits to both rat and human pressure-reduction data with values of gamma within the range reported for biological fluids (below 5 dyn/cm). The initial bubble sizes predicted are 0.1 micron or less. The presence of heterogeneous sites, for example crevices and lipid surfaces, makes nucleation even more likely.
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BIOT1 first described the active secretion of oxygen gas. He found the gas mixture in the swim-bladders of fish captured from great depths in the Mediterranean to consist of 85 per cent of oxygen. At the hydrostatic pressure of 100 atmospheres obtaining at these depths, the partial pressure of oxygen in the swim-bladder must have been 85 atmospheres. Biot announced that the oxygen had entered the swim-bladder through ``secretion'', and his discovery has been abundantly verified2-4. However, no other instances of oxygen secretion have been obtained despite the interest of a number of physiologists, notably Krogh and J. S. Haldane. We have now found large oxygen tensions in the eyes of marine teleosts.
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