Brevetoxicosis: red tides and marine mammal mortalities

Abstract

Potent marine neurotoxins known as brevetoxins are produced by the 'red tide' dinoflagellate Karenia brevis. They kill large numbers of fish and cause illness in humans who ingest toxic filter-feeding shellfish or inhale toxic aerosols. The toxins are also suspected of having been involved in events in which many manatees and dolphins died, but this has usually not been verified owing to limited confirmation of toxin exposure, unexplained intoxication mechanisms and complicating pathologies. Here we show that fish and seagrass can accumulate high concentrations of brevetoxins and that these have acted as toxin vectors during recent deaths of dolphins and manatees, respectively. Our results challenge claims that the deleterious effects of a brevetoxin on fish (ichthyotoxicity) preclude its accumulation in live fish, and they reveal a new vector mechanism for brevetoxin spread through food webs that poses a threat to upper trophic levels.

Figure 1. Brevetoxin concentrations in seagrass and fish during mass-mortality events

a, Density of red-tide algae Karenia brevis (red bars) and brevetoxin concentrations in seagrass (Thalassia testudinum) (dark blue bars; ng g⁻¹) and in sea water (light blue bars; ng ml⁻¹), collected during and after the 2002 manatee mortality event in Charlotte Harbor, Florida. Error bars, standard deviation between samples collected from four sites. b, Brevetoxin concentrations in dolphin stomach contents (SC), in undigested menhaden, and in fish collected live (light blue, in muscle; dark blue, in viscera) (flounder, Paralichthys lethostigma; herring, Opisthonema oglinum; mackerel, Scomberomorus maculatus; bluefish, Pomatomus saltatrix; codling, Urophycis floridana; pinfish, Lagodon rhomboides; spot, Leiostomus xanthurus; and sea trout, Cynoscion nebulosus) from St Joseph Bay, Florida, in spring 2004. Red arrow, regulation limit for brevetoxin in shellfish. Error bars, standard deviation between individual fish, except for pinfish and spot (pooled). Inset, toxins identified by liquid chromatography and mass spectroscopy in selected samples, as numbered in the main bar chart; those in dolphin stomach contents and in menhaden (1, 2) differed from the profile found in fish collected live two weeks after the onset of the mortality (3–5). Bars: dark red, brevetoxin-2; light red, brevetoxin-3; grey, brevetoxin-2 disulphide metabolite. For methods, see supplementary information.

Florida manatees (3 metres long, on average) are susceptible to toxins from the red tide alga Karenia brevis (inset; cell diameter, 30-35 mm)