Abstract
In the autumn of 1996, two clown fish (Amphiprion ocellaris; approximate length = 80 mm and width = 38 mm) at the London Zoo were observed exhibiting signs of buoyancy deficits and signs of being hydrodynamically unsound. These clinical abnormalities were noted after they were attacked by a damsel fish (Abudefduf oxyodon; approximate length = 110 mm and width = 75 mm). Physical examination revealed moderately distended coelomic cavities in both animals. Both fish were anesthetized to obtain lateral and dorsoventral radiographic views utilizing mammography film. Their moderately distended swim bladders were deflated at this time utilizing a 27-g needle on a tuberculin syringe and the radiographs were repeated. Enrofloxacin was administered IM at 14 mg/kg for antibacterial prophylaxis. Morphometric measurements indicated the swim bladders of these fish were multiple times larger prior to deflation than after deflation. When fully recovered from anesthesia, both fish were hydrodynamically sound.
Introduction
The swim bladder of fish is utilized to regulate buoyancy and maintain gravitational equilibrium at various depths in the water column. Fish are classified into four major groups based on the macromorphology, the micromorphology, and the physiology of their swim bladders.18 There are four major classes of swim bladders.2,15,17 Physostomes have a tubular connection between the swim bladder and the digestive tract that is retained in adult life. Physoclists have no communication between the swim bladder and the digestive tract. Euphysoclists (sub-classification of physoclists) have separate compartments for gaseous secretion and gaseous resorption. Paraphysoclists (sub-classification of physoclists) have no distinct compartments for gaseous secretion and gaseous resorption.
The clown fish (Amphiprion ocellaris) has a well-developed musculo-skeletal system, making it denser than water. The density of seawater is 1.025 g/cm3 and while muscle is 1.05 g/cm3 and fat is 0.9 g/cm3. Marine fish inhabiting depths above 950 meters usually have swim bladders while they are less frequently found in fishes inhabiting depths deeper than 1000 meters.1,16 Gas bladders or swim bladders are only used by ray finned fishes (sub-class Actinopterygii). Other species of fish such as sharks use their propulsive motion of swimming to remain buoyant at specific depths. (The swim bladder on average occupies 5% of the total body volume of a fish,18 but follows Boyle’s Law within a wide range of temperature and pressure.2,3 A fish can remain effortlessly poised with an air-filled swim bladder.9 The gas filled swim bladder enables the fish to have a density less than water and by varying the volume of gas in the swim bladder, the fish is able to remain at specific depths.
The swim bladder wall consists of multiple membranes with an abundance of nerves and vessels. The external connective tissue or tunica externa has a glistening white to silvery serosal surface18 and contains dense connective tissue with collagen fibers. The submucosa is a loose, gelatinous tissue through which nerves and vessels pass to the mucosa. The mucosa of a euphysoclist fish consists of secretory and resorbent components. The epithelium of the secretory component has gas gland cells and that of the resorbent component consists of flat thin cells. The muscularis mucosa is usually thicker in the area of the secretory component compared to the muscularis mucosa in the area of the resorbent component. The mucosal surface of the resorbent part has flat epithelial cells while the mucosal surface of the secretory part has cuboidal epithelial cells. The gas gland or diffuse layer of glandular cells is associated with the counter-current capillary system.
The rete on the serosal surface of the swim bladder is well developed in most physoclists.9 It is formed by multiple distinct capillary bundles.18 The arterial and venous supply of the rete to the bladder are in intimate contact with each other. Electron microscopic analyses have demonstrated that the rete capillaries support passive diffusion of blood. Higher PO2 in rete venous blood in comparison to post-rete arterial blood results in a venous to arterial diffusion of O2. This cumulative process is the counter current mechanism (CCM).5 The CCM is one of the biophysical means by which oxygen and other gases are concentrated in the swim bladder. Blood flows into the rete with arterial pH and PO2 values. During passage through the rete it receives O2 and acid (CO2 and H+) from the venous blood draining the swim bladder. In addition to the CCM, oxygen and other gases are concentrated in the swim bladder by processes described by the Root effect, by the Bohr effect, and by salting out.5 Fish inhabiting depths close to the surface have swim bladders with a gas composition approximating that of air. In deep water fish, the PO2 and PN2 can be as high as 100 and 25 atmospheres, respectively. Fish can concentrate oxygen into the lumen of the swim bladder by a factor of 500. Swim bladder volume is homeostatically controlled by two reflex mechanisms; an inflatory reflex (gas deposition) and a deflatory reflex (gas reabsorption).16,19 The swim bladder is innervated by branches of the vagi and the coelic ganglia.
Case Report
On the October 17, 1996, two clown fish at the London Zoo were attacked by a damsel fish. Both clown fish were more than 2 years old. Fish #1 was observed floating upside-down on the surface of its aquarium tank. Fish #2, was able to swim upright and could swim downwards vertically in the water column. However, it was only able to bob its head to the surface. This fish also had deformed fins.
Fish #1 was anesthetized by immersion in a solution of tricaine methanesulphonate (Thompson & Joseph, T & J House, 119 Plumbstead Road, Norwich, NR1 4JT, England) at a concentration of 0.1 g/L of artificial sea water. A stage III level of anesthesia was achieved and lateral and dorso-ventral radiographs were taken utilizing mammography film (Agfa-Gevaert Osray M3 13×8 cm Mammography Films, KSRX-Ray, Boca Raton, FL 33497 USA). The swim bladder of fish #1 was observed to be distended with gas and was pressing ventrally against the visceral organs. Approximately 0.6 ml of gas was aspirated with a 27-g needle and 1 ml tuberculin syringe (Monoject, Sherwood, N. Ireland) from the right side. Enrofloxacin (14 mg/kg. IM, Bayer, Shawnee, Kansas, USA) was administered. It was returned to fresh artificial seawater and recovered from the anesthetic. It was able to swim normally and also submerge to the bottom of the container, remain submerged and balance with its pectoral fins. Unfortunately, this fish died two days after the procedure.
Fish #2 was anesthetized and radiographed utilizing the same methods employed for fish #1. Approximately 0.6 ml of gas was aspirated from the left side of the coelomic cavity. Towards the end of the aspiration a small amount of blood was withdrawn into the syringe. This fish also received enrofloxacin at 14 mg/kg IM. Upon recovery, the fish was positioned at the bottom of the recovery container and exhibited signs of hydrodynamic soundness and normal buoyancy.
Discussion
Based on the radiographic examinations both fish had over-inflated bladders most likely due to trauma induced damage of the duct or blockage or dysfunction of the muscular valve. The valve controls the release of gas from the swim bladder into the alimentary tract.19
Clownfish have physoclist swim bladders. The protracted hyperinflated swim bladder of fish #1 was most likely due to ductal stenosis or a malfunction of the valve controlling the release of gas into the alimentary tract from the swim bladder.7,8
Fish #1 most likely suffered damages to its lateral lines, neuro-cranial trauma, and spatial disorientation of its auditory ossicles.3,6,10 Fish #2 has only exhibited mild symptoms following its second deflation treatment and has been monitored daily by visual observation.
Angiographic studies with radio-opaque dyes or radioisotopes such as technetium 99 may aid in detecting vascular malfunctions. Ultrasonography may detect tumors,4 abscesses, granulomas or larval migrans obstructing the exit of gas from the swim bladder.8 A microprobe for small fish ultrasonography was unavailable for use on the surviving fish. A pneumocystectomy was unable to be performed on fish #2 due to its small size but may have corrected the persistent condition and improved its prognosis.11-15,17
Acknowledgments
The authors would like to thank the staff of the London Zoo, including the zookeepers. Thanks are especially extended to Dr. Sue Thornton for her support and encouragement in the diagnostic work and documentation of this case. Thanks are also extended to Mr. George Stadusky for his assistance in the image analysis and processing and to Christine Dean, VN (London Zoo). My gratitude is extended to Drs. Mark Fox and Tony Sainsbury, the directors of the MSc Wild Animal Health Program at the Royal Veterinary College, University Of London.
Literature Cited
1. Bentley, T.B. and M.L. Wiley. 1982. Intra- and inter-specific variation in buoyancy of some estuarine fishes. Environ. Biol. Fishes 7 (1); 77–81.
2. Black, GA 1984. Swim bladder lesions in lake trout (Salvelinus namaycus) associated with mature Cystidicola stigmatura (Nematode). J. Parasit. 70 (3); 441–443.
3. Blackman, H; Nieman, U; and Fritzsch, B 1990. Peripheral and central aspects of the acoustic and lateral system of a bottom dwelling catfish, Ancistrus sp. J Comp. Neuro. 314(3);452–466.
4. Bowser, P.R., M.J. Wolfe, and T. Wallbridge. 1987. A lymphosarcoma in an Atlantic salmon (Salmo salar). J. Wild. Dis. 23 (4); 698–701.
5. Brittan , T. 1987. The Root effect. Comp. Biochem. Physiol. 86(3): 473–481.
6. Coombs, S., and A.N. Popper. 1982. Structure and function of auditory system in clown king fish (Notopterus chitala). J. Exp. Biol. 97; 225–239.
7. Gammill, J.F. 1912. Double Monstrosity [In] Gammill, The Teratology of Fishes. James Maclehose and Sons, Glasgow, Pp. 12, 15, & 18.
8. Goddard, P.J. 1995. Ultrasonic examination of fish. In CAB International, Wallingford, Oxon, Pp. 289–302.
9. Iasio, E.A. M. Bendayan, C.A. Goresky. 1994. The isolated rete. Biochem. and Mol. Biol. Fishes 3: 191–203.
10. Kelly, J.P. 1991. Topography and mechanics of the cupula in the fish lateral line I. Variation of cupular structure and composition in three dimensions. J. Morphol., 207 (1): 23–26.
11. Kita, J.C., T. Watanabe, Y. Tsukashima, and Fruitas. 1994. Lordotic deformation and development of the swim bladders in some hatchery-bred marine physoclistorous fish in Japan. J. World Aquac. Soc. 25 (1): 64–77.
12. Kovac, G.E. and G. Csaba. 1982. Studies on the protozoan etiology of swim bladder inflammation of common carp fry. Bull. Eur. Assoc. Fish Pathol. 2 (2): 22–24.
13. Kovac, G.E. 1983. Histopathological studies on protozoan swimbladder inflammation of common carp fry. Parasitol. Hung. 16: 39–46.
14. Lewbart, G.H., E.A. Stone, and N.E. Love. 1995. Pneumocystectomy in a Midas cichlid. J. Am. Vet. Med. Assoc. 207 (3): 319–321.
15. Marty, G.D. and D.E. Hinton. 1995. Oxygen consumption by larval Japanese medaka with inflated or uninflated swim bladders. Tran. Am. Fish. Soc. 124(4): 623–627.
16. Scholander, P.F., and L. Van Dam. 1953. Composition of the swim bladder gas in deep sea fishes. Biol. Bull. 104:75–86.
17. Sokolowski, M.S., and A.D.M. Dove. 2006. Histopathological examination of wild eels infected with Anguillicola crassus. J. Aquat. Health 18: 257–262.
18. Steen, J. 1970. The swim bladder as a hydrostatic organ. In: Hoar, W.S., and D.J. Randall (eds.) Fish Physiology. The Nervous System, Circulation and Respiration, Volume IV. Academic Press, London, Pp. 413–443.
19. Wagner, R.C., R. Froelich, F.E. Hossler, and S.B. Andrews. 1987. Ultrastructure of capillaries in the red body (rete mirabile) of the eel swim bladder. Microvasc. Res. 34 (3); 349–362.