Gregory D. Bossart
Veterinary Reference Laboratories, Division of Marine Mammal Research and Conservation, Harbor Branch Oceanographic Institution, Ft. Pierce, FL
Harmful algal blooms (HABs) are composed of various micro algae, which harbor and amplify potent phytotoxins that have a wide range of pathologic effects.1 There is a global pandemic of HABs that has been interpreted to be a reflection of ecosystem instability and a threat to public health.2 Florida red tide is a notorious HAB, occurring on an annual basis and with increased frequency along Florida's coastlines.3 The dinoflagellate incriminated in Florida red tide, Gymnodinium breve, produces a group of biotoxins known as brevetoxins. Brevetoxins are potent neurotoxins and evidence is mounting that these toxins also inhibit cell-mediated immunity and cause bronchoconstriction.4,5,6,7,8 Florida red tide causes major wildlife epizootics, produces toxic shellfish when the dinoflagellate is filter-accumulated in clams and oysters and releases an irritating toxicant into the air when surf conditions are turbulent. The causative relationship between G breve red tide, brevetoxins and animal mortality events has come from the temporal and spatial association of events, determination of toxin levels in tissues and newly developed immuno-histochemical documentation of intracellular toxins. However, establishing an unambiguous connection between brevetoxins and marine mammal mortality can be difficult.
Extensive Florida manatee mortalities that coincided with G breve blooms were reported in 1963, 1982 and 1996.4,9,10 In 1996, at least 149 manatees died in an unprecedented epizootic along the southwest coast of Florida. At about the same time, a bloom of G breve was present in the same area. Brevetoxins were isolated in quantities from 2- to 15- fold above control levels in stomach contents, liver, kidney and lung from dead manatees using a synaptosomal binding assay. Grossly, severe nasopharyngeal, pulmonary, hepatic, renal and cerebral congestion was present in all cases. Nasopharyngeal and pulmonary edema and hemorrhage were also seen. Consistent microscopic lesions consisted of catarrhal rhinitis, pulmonary hemorrhage and edema, multiorgan hemosiderosis and nonsuppurative leptomeningitis. Immunohistochemical staining using a polycolonal primary antibody to brevetoxin (GAB) showed intense positive staining of lymphocytes and macrophages in the lung, liver and secondary lymphoid tissues. Additionally, lymphocytes and macrophages associated with the inflammatory lesions of the nasal mucosa and meninges were also positive for brevetoxin. These findings implicated brevetoxicosis as a component of and the likely primary etiology for the epizootic. Additionally, retrospective histopathologic and immunohistochemical studies demonstrated that the 1982 manatee epizootic was likely due to the incidental ingestion of filter-feeding ascidians that contained brevetoxins. The data suggest that manatee mortality resulting from brevetoxicosis may not necessarily be acute but may occur after chronic inhalation and/or ingestion. Immunohistochemical staining with interleukin-1-[3-converting enzyme showed positive staining with a cellular tropism similar to GAB. This suggested that brevetoxicosis might initiate apoptosis and/or the release of inflammatory mediators that culminate in fatal toxic shock.
Manatees from Florida's coastlines have continuous potential brevetoxin exposure because red tide blooms are common in these areas. Therefore mortality-associated brevetoxicosis may be cumulative and the result of high dose or prolonged low dose exposure to these biotoxins. Additionally, prolonged non-lethal toxin exposure may compromise normal immunologic responses predisposing these manatees to opportunistic disease. This mechanism could play a role in the poorly-characterized manatee "cold stress syndrome." Further controlled laboratory and field studies are indicated to investigate the pathogenesis of brevetoxicosis, especially in light of the increasing frequency of red tide events in Florida and the critically endangered status of the Florida manatee.
The author acknowledges the invaluable technical support of the staffs of the Marine Mammal Pathobiology Laboratory, Florida Marine Research Institute; Miami Seaquarium; Sea World of Florida; Lowry Park Zoo; Department of Pathology, College of Veterinary Medicine, University of Florida; Department of Pathology, University of Miami School of Medicine; and the US Fish and Wildlife Service.
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