Skin ulcers in estuarine fishes: A comparative pathological evaluation of wild and laboratory-exposed fish

The toxic dinoflagellate Pfiesteria piscicida Steidinger & Burkholder has r ecently been implicated as the etiologic agent of acute mass mortalities an d skin ulcers in menhaden, Brevoortia tyrannus, and other fishes from mid-A tlantic U.S. estuaries. However, evidence for this association is largely c ircumstantial and controversial. We exposed tilapia (Oreochromis spp.) to P fiesteria shurnwayae Glasgow & Burkholder (identification based on scanning electron microscopy and molecular analyses) and compared the resulting pat hology to the so-called Pfiesteria-specific lesions occurring in wild menha den. The tilapia challenged by high concentrations (2,000-12,000 cells/mL) of P. shurnwayae exhibited loss of mucus coat and scales plus mild petecchi al hemorrhage, but no deeply penetrating chronic ulcers like those in wild menhaden. Histologically, fish exhibited epidermal erosion with bacterial c olonization but minimal associated inflammation. In moribund fish, loss of epidermis was widespread over large portions of the body. Similar erosion o ccurred in the mucosa lining the oral and branchial cavities. Gills exhibit ed epithelial lifting, loss of secondary lamellar structure, and infiltrati on by lymphoid cells. Epithelial lining of the lateral line canal LLC) and olfactory organs exhibited severe necrosis. Visceral organs, kidney, and ne ural tissues (brain, spinal cord, ganglia, peripheral nerves) were histolog ically normal. An unexpected finding was the numerous P. shurnwayae cells a dhering to damaged skin, skin folds, scale pockets, LLC, and olfactory tiss ues. In contrast, histologic evaluation of skin ulcers in over 200 wild men haden from Virginia and Maryland portions of the Chesapeake Bay and the Pam lico Estuary, North Carolina, revealed that all ulcers harbored a deeply in vasive, highly pathogenic fungus now known to be Aphanomyces invadans. In m enhaden the infection always elicited severe myonecrosis and intense granul omatous myositis. The consistent occurrence of this fungus and the nature a nd severity of the resulting inflammatory response indicate that these ulce rs are chronic (age > 1 week) and of an infectious etiology, not the direct result of an acute toxicosis initiated by Pfiesteria toxin(s) as recently hypothesized. The disease therefore is best called ulcerative mycosis (UM). This study indicates that the pathology of Pfiesteria laboratory exposure is fundamentally different from that of UM in menhaden; however, we cannot rule out Pfiesteria as one of many possible early initiators predisposing w ild fishes to fungal infection in some circumstances.