Introduction

Angel fish, Pterophyllum scalare, are among the most popular aquarium fish. In 1986 reports of unusual and uncontrollable mortality of angel fish circulated throughout the pet industry. These concerns were soon reflected in the popular press (Birdsill, 1988; Dawes, 1988; Harbacek, 1988; Jones, 1988). A study designed to determine the cause of angel fish mortality on commercial farms in Florida was initiated in December, 1988. Parasitic and bacterial diseases were most commonly associated with angel fish mortality, however viral particles were identified in tissues of some sick fish (Table 1).

Table 1: Causes of mortality in angel fish from 71 case investigations during the period 1987 through 1989

 Virus 4 Cases*

 Bacteria 26 Cases

 Parasites 50 Cases

 Water Quality 2 Cases

 Nutrition 3 Cases

 Unknown 3 Cases

Note: Total number of cases tested for virus particles by electron microscopy scan of feces was 13. (Note: Some fish had more than one problem which could have been the primary cause of death).

At present the existence of a pathogenic viral disease in angel fish has not been proven. There is some, evidence, however, that some of the mortality problems referred to as "Singapore disease" (Dawes, 1988), and similar names may have a viral component. Until an agent is successfully grown in the laboratory and Koch's postulates fulfilled, it cannot be stated that there is a viral disease of angel fish. Still, a number of researchers have reported identification of virus-like particles from angel fish (Gratzek et al., 1990, Gratzek, 1989, Francis-Floyd et. al., 1989; Mellergaard and Bloch, 1988).

Herpesvirus-like Particles

The first report of viral particles was from Denmark (Mellergaard and Bloch, 1988) and involved 3 adult angel fish (P. altum) which had been imported from the Amazon. The fish had been maintained for 3 to 4 months in a home aquarium prior to showing signs of disease. Two days prior to becoming sick the aquarium had been rearranged. The sick fish had hemorrhagic lesions on the skin, including some ulcerations; gills were pale, and liver and spleen were distended. No parasites were noted and no bacteria were isolated from kidney swabs. Electron microscopic examination of splenic tissue revealed the presence of herpesvirus-like particles. Mellergaard and Bloch (1988) concluded that the wild caught fish may have had a latent herpesvirus infection and that clinical disease resulted following stress associated with manipulation of the aquarium. They noted that the other fish in the tank, which were home-bred P. scalare, did not develop the disease.

Paramyxovirus-like Particles

On-going studies at the University of Florida and the University of Georgia have revealed a number of virus particles in the feces and tissues of sick angel fish (P.scalare). At present, the feeling is that many of these are incidental findings. There is some concern however that a paramyxovirus may be associated with the mysterious malady of angel fish reported in the popular press. Paramyxoviruses cause a number of diseases in domestic animals including canine distemper and Newcastles disease in poultry. The only report of paramyxovirus in fish was reported by Winton et al. (1985). Paramyxovirus was isolated from pooled homogenates of kidney and spleen of healthy, wild-caught chinook salmon (Onchorynchus tshawytscha) and were not associated with disease (Winton, 1985; Wolf, 1989).

The evidence which supports the paramyxovirus as a cause of disease in angelfish is largely circumstantial. In three instances virus particles were found in the fecal material of sick angel fish from commercial farms using electron microscopy. In two of these cases paramyxovirus-like particles were found. Other virus-like particles were also found and included papovavirus, parvovirus, enterovirus, papillomavirus, and reovirus. In all cases sick fish were showing signs considered consistent with the new disease, but, as will be discussed below, these signs were non-specific. The strongest evidence which supported the paramyxovirus theory was from a transmission study. In this case healthy fish from a known source were injected with a cell-free filtrate taken from the tissues of an infected fish. The injected fish developed typical signs of the disease 3 weeks later and scientists at the Florida Department of Agriculture and Consumer Services Veterinary Diagnostic Laboratory located in Kissimmee, Florida found paramyxovirus-like particles only in the injected fish. No virus particles were found in control fish. Fish which were injected with sterile saline to test the injection method did not get sick and did not die.

Signs of the Suspected Viral Disease

Signs which were observed in sick angel fish which did have paramyxovirus-like particles in feces or tissues were similar to those reported in the popular press (Harbacek, 1988). These signs are, however, non-specific, which means that a number of different things can cause them. Fish affected with the suspected new disease initially would hang listlessly in corners of the tank and showed signs of fin rot. The caudal fin showed signs of erosion and sometimes appeared to have fungus growing on it. In light colored fish such as the gold veil, hemorrhagic streaks could be seen running parallel to the fin rays toward the eroded areas. Tiny pinpoint hemorrhages (petechiae) were noticeable at the base of the dorsal fin in light colored fish, and occasionally around the eyes and operculum. The abdomen frequently appeared enlarged and rounded. As the fish grew weaker they would assume a horizontal position and lie flat on the bottom of the tank or float listlessly at the surface. Fish would remain in this position for several days and several were observed to feed from their horizontal orientation. The most subtle sign evidenced by sick fish, in the author's opinion, was the production of excess mucus. Excess mucus production was noted along the dorsal body wall, anterior to the dorsal fin. It was most easily observed in dark color varieties such as marble angels and black angels, and then, with a flashlight or similar indirect light source.

The disease appeared to run its course in 3 to 5 days. Survivors would show signs of recovery by resuming a more normal position, though they remained lethargic and tended to hang in corners. A definitive sign seemed to be healing of the caudal fin. The author is not aware of a fish which showed regeneration of damaged fins and then died. Complete convalescence seemed to take 4 to 6 weeks, when fish seemed to be able to return to breeding activity. It was about 6 months, however, before production levels were fully restored. It must be emphasized that this recovery and return to productivity seemed dependent on superlative nursing care. It also must be emphasized that most of this information on course of disease and recovery is based on one case which was followed very closely for several months. It is unknown whether recovered fish remain a source of infection. The incubation period for the disease appeared to be 3 to 7 days and may vary with temperature. In commercial hatcheries transmission seemed to require 3 to 5 days at water temperatures around 27°C. In our laboratory, however, transmission seemed to take 7 to 10 days but water temperature averaged 23 to 25°C. During the transmission study mentioned above 22 days passed before the fish showed signs of disease, and they all became sick within the same 24 hour period. Water temperature was 24 to 26°C.

Case Management

Bases on electron microscopy studies, there have only been two field cases in which paramyxovirus was implicated as a possible cause of mortality. Recommendations to producers were directed towards alleviation of stress and prevention of secondary bacterial infection which could compromise recovery. First, avoid stressing the fish. This means maintain scrupulously clean water, do not handle or move the fish, and feed them all the good quality food they will eat.

Second, take active steps to control spread of the infection and decrease the number of infectious particles in the environment. Cover tanks so that infectious particles are not aerosolized. Increase the flush through the tanks if running water is available. If static systems are in place do partial (30 to 50%) water changes daily.

Third, only medicate fish to eliminate known parasitic or bacterial diseases. Noxious chemicals are a source of stress and may contribute to prolonged recovery. Indiscriminate use of medications has been actively discouraged.

Finally, sanitize nets, filters, air stones or any other item which may have come in contact with water containing infectious agents. This should be a standard practice in any commercial facility, whether a farm, transhipper, or pet store. Always sanitize tanks between groups of fish. Rinse these items well following chemical treatment.

Conclusions

The existence of a new viral disease of angel fish has not been proven. The presence of virus-like particles in feces and tissues of sick angel fish suggest that these may play a role in the disease process, particularly in the absence of other identifiable pathogens. The disease appears to have been transmitted through a cell-free filtrate to susceptible fish. The disease appears to be best managed by providing good nursing care and preventing secondary bacterial invasion. Results of this study do not support the hypothesis that a new viral disease is widespread throughout the pet fish industry, however so few fish have been tested for virus (by electron microscopy) that it is impossible to make sweeping statements about incidence. In addition, the presence of viral particles in fecal material is not diagnostic in any way and should not be interpreted as such. However, at present it is the best tool available.

Acknowledgment

Funding for this project was provided by the Division od Marketing, Florida Department of Agriculture and Consumer Services, Doyle Conner, Commissioner, under the Aquaculture Market Aid Development Program.

References

1.  Birdsill, B. 1988. Over The Counter, monthly column. Freshwater And Marine Aquarium. May, 1988 pp:54-55.

2.  Francis-Floyd, R.; Keefe, T.; Frazer, W.; Reed, P.; Watson,C. 1989. Investigations of angel fish mortality. International Cichlid Conference, Orlando, Florida, August 10, 1989.

3.  Gratzek, J.B., Lukert, P.D. Latimer, K.S. 1990. Angelfish Diseases. Pet Age Magazine. April, 1990. pp 50-55.

4.  Gratzek, J.B. 1989. Angel Fish Disease symposium. International Cichlid Conference, Orlando, Florida, August 10, 1989.

5.  Harbacek, L. 1988. The vanishing angels. Freshwater And Marine Aquarium. March, 1988 pp:82-87.

6.  Jones, P. 1988. Angels in trouble? Tropical Fish Hobbyist. March,1988. pp:6.

7.  Winton, J.R.; Lannan, C.N.; Ransom, D.P.; Fryer, J.L. 1985. Isolation of a new virus from Chinook salmon (Oncorhynchus tshawvtscha) in Oregon, USA. Fish Pathology 20:373-380.

8.  Wolf, K. 1989. Fish Viruses And Fish Viral Diseases. Cornell University Press. Ithica, NY.