Abstract

Parrotfish (family Scaridae) are diurnal, largely herbivorous, marine fish of primarily tropical waters. All species (numbering 79) have non-protractile mouths with teeth that are coalesced into a powerful parrot-like beak. Parrotfish forage over reefs and similar substrate, grazing and nibbling on rocks and corals (usually dead) to obtain algae growing on or just below the surface. In the process a substantial amount of calcareous material is ingested with on average 75 percent of the gut contents composed of this inorganic sediment. Broad, bony pharyngeal teeth plates grind the grit into tiny bits, and a specialized alimentary tract extracts the food. Remaining waste is often voided in long plumes as the fish swims. Other items in the parrotfish diet include uncalcified tips of algal bushes, sea grass blades, occasional crustaceans, and rarely sponges.^2,4

Parrotfish come in a wide array of colors and patterns, and are covered with large hard cycloid scales. Commonly exhibited in aquaria, most species are considered moderately hardy, but some are very delicate. Given their specialized anatomy and eating behavior, acclimating and maintaining parrotfish on captive diets can be difficult. The family exhibits complex social and mating systems including the ability of females to change sex (protogynous hermaphroditism), and have not been bred in captivity. Some members of the genus Scarus, such as the queen parrotfish (Scarus vetula) rest at night in a transparent mucus cocoon secreted from their mouths. Cloaked in this structure, it is believed to mask their scent from night predators.^2,4,6

Methods and results

For this report a retrospective evaluation of medical, necropsy, and husbandry information for all parrotfish that died over five years (1998-2002) was performed. Nine Caribbean species are represented in this report. Parrotfish that were recovered too decomposed for evaluation and had no history of an ongoing or recent medical/husbandry problem were removed from the study set.

Of the 49 cases evaluated, infectious disease made up 37 percent (Table 1). Of these, 13 cases (72 percent of infectious disease cases) had a fungal etiology. All of these fungal infections were characterized by the presence of progressive cutaneous ulcerative mycotic disease (PCUMD).

Lesions of PCUMD were found on either the body or the jaw/beak and involved multiple tissues (Table 2). All cases had ulcerative necrotizing dermatitis and cellulitis with loss of scales and/or epidermal tissue of varying severity. In most of the body lesions skeletal muscle was invaded with myositis and myonecrosis present. In two of these cases ulceration and necrosis of the body wall resulted in perforation of the coelomic cavity and visceral invasion. In these two cases and three additional body lesion cases, fungal hyphae infiltrated the vasculature and disseminated to various other organs including the gills, heart, spleen, and liver. In several of the jaw/beak cases and those with lesions over the skull region, osteolysis +/- cartilage necrosis occurred due to invasion of skeletal structures by the fungal elements. In most jaw/beak cases, loss of large portions of the beak was noted.

Fungal hyphae were identified within the lesions in all 13 cases, many of which had the morphological characteristics of Fusarium solani. Culture of wounds from two cases (one midnight and one queen parrotfish) yielded Fusarium solani and one other case (rainbow parrotfish) yielded Pseudoallescheria boydii. In addition to fungal elements, two cases had concomitant bacterial infections with intralesional bacteria identified on histopathology.

In those cases presented for treatment, progression of the condition was often quite rapid. Most treatment attempts were aimed at covering secondary bacterial infections and were not successful. Several fish were euthanized due to the severity of the condition and grave prognosis.

The second largest category of mortality was environmental, representing 33 percent of the cases. A total of ten out of sixteen environmental cases (63 percent) represented newly acquired parrotfish that failed to thrive following collection and through the quarantine period. Included in this category was also parrotfish on exhibit that were out competed by tank mates or succumbed to adverse changes in water quality parameters. The trauma (predation, aggression, handling injury) and idiopathic mortality categories were similar in number, collectively equaling 30 percent of the cases (Table 1).

Discussion

Fungal infections in marine fish have historically been considered rare. However, significant mortality can occur in both wild and captive populations. In aquaria, sporadic deaths of individual fish often occur with absence of full histological evaluation due to decomposition/consumption of the specimen, lack of available funds or staff, or an assumption that the cause of death is known and full pathologic assessment is of limited value. Consequently, fungal infections are likely under-diagnosed in aquaria. Of the cases falling into the trauma and idiopathic mortality categories, 11/15 (73 percent) had cutaneous ulcerative lesions (Table 3). Of these cases, few received necropsies and no histopathology was performed. Given the strong correlation between cutaneous ulcerative lesions and PCUMD, it is likely that some of these cases would have been placed in the fungal infection category if histopathologic assessment had been performed.

Cases of cutaneous ulceration due to fungal infections are well documented in the literature. More recent reports in wild fish include the implication of the highly pathogenic fungus, Aphanomyces invadans, in huge mass mortalities and skin ulcers in wild Menhaden (Brevoortia tyrannus) and other estuary fishes along the mid-Atlantic United States.¹⁰ Several fungal agents have been reported as causing cutaneous disease in captive aquaria fish including Cladosporium sp which was isolated from a deep dermal ulcer extending to bone in a tomato clownfish (Amphiprion frenatus),⁷ Exophiala pisciphila which was isolated from skin lesions in a smooth dogfish (Mustelus canis),⁵ and Fusarium solani which was isolated from dermal lesions during an outbreak in a group of angelfish (Family Pomacanthidae).⁹

Table 1. Categories of mortality in a captive population of parrotfish.

Table 2. Summary of tissue involvement in cases of Progressive Cutaneous Ulcerative Mycotic Disease (PCUMD) in captive parrotfish.

Table 3. Presence of cutaneous ulcerative lesions by mortality category in a captive population of parrotfish.

The fungus Fusarium solani was cultured from two cases of PCUMD and was morphologically identified in several others. Along with the angelfish mentioned above, Fusarium solani has been isolated from a cutaneous mass on a captive scrawled filefish (Aluterus scriptus)¹ and has been responsible for mortality in captive scalloped hammerhead (Sphyrna lewini) and bonnethead (Sphyrna tiburo) sharks.^3,8 Mortality in bonnethead sharks due to Fusarium solani has been documented at several other institutions including the authors' and it appear that this species is exquisitely sensitive to infection with this pathogen. Based on this report, it appears that parrotfish, at least those of the genus Scarus, are equally susceptible to fusariomycosis. Although a small sample size exists, it is interesting to note that no cases of PCUMD were identified among members of the genus Sparisoma. A literature search failed to identify Pseudoallescheria boydii, the other fungus that was isolated in one PCUMD case, as a pathogen of fish.

The development of all cases of PCUMD in this population of parrotfish are assumed to have developed following insult to the protective surface of the fish's skin. While this damage could have resulted from a number of different events, immune suppression likely contributes to the development and/or outcome of all cases. Potential contributing factors to the development and progressive of PCUMD in parrotfish are as follows:

1. Aggression /social stress: For most species, parrotfish society is typified by foraging herds of females and large, solitary males. Although usually peaceful, aggression between conspecifics does occur, particularly in males defending territories.^2,4 While intraspecific aggression has not been observed with great frequency in this collection, the behavior of males locking jaws during disputes could predispose these animals to developing the beak lesions seen in several cases of PCUMD.

Due to their preference for plentiful and rapidly renewable plant food, parrotfish tend to tolerate other species of fish in the wild. Interspecific aggression is, however, a factor in this collection and harassment and predation by tank mates, particularly during the quarantine period, has been observed. Even when significant wounds are not inflicted, the chronic stress on individuals at the receiving end of aggressive behaviors can contribute to a fish's inability to heal even the smallest wounds and combat infection.

2. Handling trauma and failure to acclimate: All parrotfish collected by the authors' institution are housed temporarily (< 1 week) at a collection facility in the Florida keys and then transported via highway to the institution. Once they arrive, all fish undergo a minimum 30-day quarantine whereby all individuals are treated with copper (14 days), praziquantel, fenbendazole, and metronidazole. At the end of quarantine a representative sample of the populations is anesthetized for diagnostic sampling (gill clip, skin scrape, cloacal wash, etc.). All parrotfish receive a freshwater dip prior to transport to exhibit. While aimed at preventing disease in the collection, this process imparts a certain level of stress on the fish. Not only do some fish develop traumatic wounds during transport and handling, but a portion of the fish fail to eat which certainly contributes to their overall immunocompromised state. Of the 13 cases of PCUMD, 4 (31 percent) developed in fish undergoing quarantine.

3. Diet/husbandry-related stressors: The diet fed to parrotfish in the collection is made up of a broadcasted mix (chopped fish, krill, shrimp, clams, peas, and commercial gel-food diet) and blocks of dental plaster impregnated with an enhanced Spirulina spp. algae pellets. Despite the provision of the "coral-like" product, the parrotfish spend a large amount of time grazing plant material from and chewing on exhibit "furniture" and support structures. One theory is that these items are potentially harder and or more abrasive than corals, which may initiate beak damage that develops into the jaw/beak-associated PCUMD lesions described above.

4. Thermal stress: At the authors' institution the development of fusariomycosis in bonnethead sharks is felt to have been precipitated by maintenance of the sharks in lower than optimal temperatures which presumably leads to suppression of the shark's immune system and/or favors the growth of the fungi. Following quarantine, parrotfish are housed in two major bodies of water: 1) The Living Seas (LS)--a large 5.7 million gallon indoor system with no communication to outside climate; and 2) Typhoon Lagoon (TL)--a large outdoor system designed for human recreation with exposure to full sunshine and the elements. A comparison of seasonal temperature ranges in these enclosures was made with those obtained at the collecting sites in the Florida Keys using NOAA's National Data Buoy Center information:

Despite being outdoors and under the Central Florida sunshine, temperatures across the year are cooler in the TL system compared with the LS system. In terms of mortality, more cases of PCUMD occurred among TL parrotfish (7/13 or 54 percent) than LS parrotfish (2/13 or 15.2 percent). Although the sample size is small, this data suggests that a direct relationship exists between maintaining parrotfish at low range temperatures and the development of PCUMD.

Conclusions

PCUMD appears to be a significant disease afflicting captive parrotfish. Any wounds noted on parrotfish should be considered significant and at least monitored closely for progression. Husbandry and veterinary staff should attempt to minimize trauma to the skin and integument when capturing, moving, or examining parrotfish. Institutions should make attempts at reducing stressors such as temperature, social, nutritional, and environmental to minimize immune suppression. Future investigations warranted include evaluating the effectiveness of aggressive debridement of lesions and anti-fungal therapies, and determining the importance of sustained low range temperature on immune function in parrotfish.

Acknowledgements

The authors thank Dr. Mark Stetter, Jane Capobianco, Dr. Andy Stamper, and the Aquarium Team of Epcot's The Living Seas for their assistance.

References

1.  Bruemmer TM, G Lewbart. 1996. Fusarium solani infection in a scrawled filefish (Aluterus scriptus). Proceedings of the International Association for Aquatic Animal Medicine, Tennessee. Pp. 23-24

2.  Burgess WE, H Axelrod, RE Hunziker III. Dr. Burgess's Atlas of Marine Aquarium Fishes, 2nd edition. T.F. H. Publications, Inc., Neptune City, New Jersey, Pp. 680-681.

3.  Crow GL, JA Brock, S Kaiser. 1995. Fusarium solani fungal infection of the lateral line canal system in captive scalloped hammerhead sharks (Sphyrna lewini) in Hawaii. Journal of Wildlife Diseases. 31:562-565.

4.  Deloach N. 1999. Reef fish behavior. Florida-Caribbean-Bahamas. New World Publications, Inc., Jacksonville, Florida. Pp. 280-299.

5.  Gaskins JE, PJ Cheung. 1986. Exophiala pisciphila. A study of its development. Mycopathologia. 93:173-184.

6.  Nelson JS. 1984. Fishes of the World, 2nd edition. John Wiley and Sons Inc., New York. Pp. 328.

7.  Silphaduang U, K Hatai S Wada, E Noga. 2000. Cladosporiosis in a tomato clownfish (Amphiprion frenatus). Journal of Zoo and Wildlife Medicine. 31:259-261.

8.  Smith AG, AG Muhvich, KH Muhvich, C Wood. 1989. Fatal Fusarium solani infections in baby sharks. 1989. Journal Medical and Veterinary Mycology. 27:83-91.

9.  Stetter MD, JM Choromanski. 1991. Fusarium solani infection in a group of marine angelfish.

10. Vogelbein WK, JD Shields, LW Haas, KS Reece, DE Zwerner. 2001. Skin ulcers in estuarine fishes: a comparative pathological evaluation of wild and laboratory-exposed fish. Environmental Health Perspectives. 109 Supplement 5:687-693.