Abstract
The toxic dinoflagellate Pfiesteria piscicida Steidinger & Burkholder has recently been implicated as the etiologic agent of acute mass mortalities and skin ulcers in menhaden, Brevoortia tyrannus, and other fishes from mid-Atlantic U.S. estuaries. However, evidence for this association is largely circumstantial and controversial. We exposed tilapia (Oreochromis spp.) to Pfiesteria shumwayae Glasgow & Burkholder (identification based on scanning electron microscopy and molecular analyses) and compared the resulting pathology to the so-called Pfiesteria-specific lesions occurring in wild menhaden. The tilapia challenged by high concentrations (2,000-12,000 cells/mL) of P. shumwayaeexhibited loss of mucus coat and scales plus mild petecchial hemorrhage, but no deeply penetrating chronic ulcers like those in wild menhaden. Histologically, fish exhibited epidermal erosion with bacterial colonization but minimal associated inflammation. In moribund fish, loss of epidermis was widespread over large portions of the body. Similar erosion occurred in the mucosa lining the oral and branchial cavities. Gills exhibited epithelial lifting, loss of secondary lamellar structure, and infiltration by lymphoid cells. Epithelial lining of the lateral line canal (LLC) and olfactory organs exhibited severe necrosis. Visceral organs, kidney, and neural tissues (brain, spinal cord, ganglia, peripheral nerves) were histologically normal. An unexpected finding was the numerous P. shumwayae cells adhering to damaged skin, skin folds, scale pockets, LLC, and olfactory tissues. In contrast, histologic evaluation of skin ulcers in over 200 wild menhaden from Virginia and Maryland portions of the Chesapeake Bay and the Pamlico Estuary, North Carolina, revealed that all ulcers harbored a deeply invasive, highly pathogenic fungus now known to be Aphanomyces invadans. In menhaden the infection always elicited severe myonecrosis and intense granulomatous myositis. The consistent occurrence of this fungus and the nature and severity of the resulting inflammatory response indicate that these ulcers 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 wild fishes to fungal infection in some circumstances.
Full Text
The Full Text of this article is available as a PDF (1.6 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Burkholder J. M., Noga E. J., Hobbs C. H., Glasgow H. B., Jr, Smith S. A. New 'phantom' dinoflagellate is the causative agent of major estuarine fish kills. Nature. 1992 Jul 30;358(6385):407–410. doi: 10.1038/358407a0. [DOI] [PubMed] [Google Scholar]
- Burkholder J. M. The lurking perils of Pfiesteria. Sci Am. 1999 Aug;281(2):42–49. doi: 10.1038/scientificamerican0899-42. [DOI] [PubMed] [Google Scholar]
- Grattan L. M., Oldach D., Perl T. M., Lowitt M. H., Matuszak D. L., Dickson C., Parrott C., Shoemaker R. C., Kauffman C. L., Wasserman M. P. Learning and memory difficulties after environmental exposure to waterways containing toxin-producing Pfiesteria or Pfiesteria-like dinoflagellates. Lancet. 1998 Aug 15;352(9127):532–539. doi: 10.1016/S0140-6736(98)02132-1. [DOI] [PubMed] [Google Scholar]
- Medlin L., Elwood H. J., Stickel S., Sogin M. L. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene. 1988 Nov 30;71(2):491–499. doi: 10.1016/0378-1119(88)90066-2. [DOI] [PubMed] [Google Scholar]