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Beginning in April 2002, three species of Florida puffer fish from around the state of Florida, USA were monitored for the presence of saxitoxin (STX). In total, 873 southern ( Sphoeroides nephelus ), 171 checkered ( S. testudineus ), and 53 bandtail ( S. spengleri ) puffer fish were collected between 2002 and 2006 from eight regions: Jacksonville, the Indian River Lagoon, Tequesta, the Florida Keys, Charlotte Harbor, Tampa Bay, Cedar Key, and Apalachicola. Emphasis was placed on collecting specimens from the Indian River Lagoon (IRL), where recreational harvesting of puffer fish led to 28 cases of saxitoxin puffer fish poisoning (SPFP) between January 2002 and May 2004. Southern puffer fish from the northern IRL routinely contained the highest concentrations of STX, with average levels in the skin of 1787 μg STXequiv./100 g tissue. Elevated concentrations were also found in the muscle (1102 μg STXequiv./100 g), gut contents (539 μg STXequiv./100 g), gonads (654 μg STXequiv./100 g), and liver (214 μg STXequiv./100 g). Lower, yet significant (above the action limit of 80 μg STXequiv./100 g tissue), concentrations of STX were also detected in the skin (599 μg STXequiv./100 g), muscle (233 μg STXequiv./100 g), gut contents (197 μg STXequiv./100 g), and gonads (239 μg STXequiv./100 g) of southern puffer fish from Tequesta in the southern IRL, as well as in the gonads (122 μg STXequiv./100 g) of Jacksonville southern puffer fish and the skin (265 μg STXequiv./100 g) of Tampa Bay southern puffer fish. STX concentrations above the action limit were also found in the skin of bandtail puffer fish from the IRL (620 μg STXequiv./100 g), Tequesta (374 μg STXequiv./100 g), and the Florida Keys (230 μg STXequiv./100 g). Checkered puffer fish collected from the IRL, Tequesta, and the Florida Keys on average were nontoxic, containing STX levels below the action limit in all tissues.

Brevetoxins and ciguatoxins are closely related potent marine neurotoxins. Although ciguatoxins accumulate in fish to levels that are dangerous for human consumption, live fish have not been considered as potential sources of brevetoxin exposure in humans. Here we show that, analogous to ciguatoxins, brevetoxins can accumulate in live fish by dietary transfer. We experimentally identify two pathways leading to brevetoxin-contaminated omnivorous and planktivorous fish. Fish fed with toxic shellfish and Karenia brevis cultures remained healthy and accumulated high brevetoxin levels in their tissues (up to 2675 ng g−1 in viscera and 1540 ng g−1 in muscle). Repeated collections of fish from St. Joseph Bay in the Florida panhandle reveal that accumulation of brevetoxins in healthy fish occurs in the wild. We observed that levels of brevetoxins in the muscle of fish at all trophic levels rise significantly, but not to dangerous levels, during a K. brevis bloom. Concentrations were highest in fish liver and stomach contents, and increased during and immediately following the bloom. The persistence of brevetoxins in the fish food web was followed for 1 year after the K. brevis bloom.

Puffer fish poisoning (PFP) is usually caused by ingestion of tetrodotoxins (TTXs) found naturally in certain species of puffer fish (Halstead 1967; Mosher and Fuhrmann 1984). In Japan, 20–100 people die annually from PFP, in spite of stringent controls by authorities (Ogura 1971). TTXs can cause fatal human poisoning, which is similar to paralytic shellfish poisoning (PSP) caused by saxitoxins (STXs). PSP is caused by the consumption of toxic shellfish (Shumway 1990) and rarely by fish that have have become toxic after feeding on STX-producing microalgae (Maclean 1979). As well as TTXs, STXs have also been found in at least 12 marine and freshwater puffer fish species in Asia (Ahmed et al. 2001; Kodama et al. 1983; Kungsuwan et al. 1997; Nakamura et al. 1984; Nakashima et al. 2004; Sato et al. 1997, 2000; Zaman et al. 1997), but their bioorigin has not been identified. TTXs are chemically distinct from STXs, but both neurotoxins produce similar symptoms in mammals because they act on site 1 of the voltage-dependent sodium channel, blocking the influx of sodium into excitable cells and restricting signal transmission along nerve and muscle membranes (Ahmed 1991). The symptoms of traditional PFP from TTXs and of PSP from STXs include tingling and numbness of the mouth, lips, tongue, face, and fingers; paralysis of the extremities; nausea; vomiting; ataxia; drowsiness; difficulty in speaking; progressively decreasing ventilatory efficiency; and finally in extreme cases, death by asphyxiation caused by respiratory paralysis (Ahmed 1991; Catterall 1985; Kao 1993). PFP cases in Europe (Kao 1993) and Mexico (Nunez-Vazquez et al. 2000) have occasionally been reported. In the United States, PFP has been associated with imports of puffer fish [Centers for Disease Control and Prevention (CDC) 1996]; rarely have fatalities occurred after the consumption of indigenous puffer fish. In Hawaii, white-spotted puffer fish, Arothron hispidus, were implicated in seven deaths (Ahmed 1991). Until 1974, seven PFP cases in Florida, outside of the Indian River Lagoon (IRL), were caused by the consumption of locally caught “blowfish” or puffer fish (Ahmed 1991; Benson 1956; Bigler 1999; Hemmert 1974; Mosher and Fuhrmann 1984). These cases included three fatalities, likely from TTX; for example, one woman died 45 min after consuming toxic liver from a checkered puffer fish (Sphoeroides testudineus) (Benson 1956). The toxins involved in the previous Florida PFP cases were not characterized, but because PFP is usually associated with TTX, investigators likely assumed that TTX was the cause (Benson 1956; Bigler 1999; Hemmert 1974). Tissues from Florida bandtail (Sphoeroides spengleri), checkered, and southern puffer fish (Sphoeroides nephelus) were found to be lethal in the mouse bioassay (MBA) (Burklew and Morton 1971; Lalone et al. 1963), but, again, the toxins were not determined. Until January 2002 the harvest and consumption of puffer fish from the IRL was not a risk to public health. Since then (until May 2004), however, 28 PFP cases occurring in Florida (n = 21), New Jersey (n = 3), Virginia (n = 2), and New York (n = 2) caused by puffer fish originating from the IRL were reported (Bodager 2002; CDC 2002a, 2002b). Analyses of toxins from unidentified puffer fish fillet remnants from one of the early 2002 PFP cases in New Jersey revealed STXs (Quilliam et al. 2004), not TTXs, a distinction that alone could not be made on the basis of consumer symptoms or traditional screening methods (i.e., MBA). During 2002–2004, all PFP cases were linked to puffer fish originating from the northern IRL and the Banana River on Florida’s east coast (Figure 1). Except for one case, where puffer fish were commercially harvested and reached a New Jersey fish market, puffer fish were caught recreationally [Bodager 2002; Florida Fish and Wildlife Conservation Commission (FWC) 2004]. In April 2002, state and federal officials issued health advisories, and the FWC banned puffer fish harvesting in the IRL, a ban that currently remains in effect. In New York on 14 October 2002, two PFP cases were caused from fish caught near Titusville, Florida, but frozen in March 2002 before the harvesting ban (Bodager D, personal communication). This case demonstrated the stability of toxins in puffer fish frozen for almost 9 months. Figure 1 Map showing locations (circles) in the Indian River Lagoon, Florida, where toxic puffer fish in the SPFP incidents originated (FWC 2004). Sample collections of puffer fish and Pyrodinium bahamense were conducted throughout this area and further south ... Because STXs had not previously been identified in Florida’s marine waters and their distribution, source, and origin were unknown in April 2002 (Abbott et al. 2003; Landsberg et al. 2002), we initiated an intensive survey of biota in the IRL. In this article we present a summary from 3 years of monitoring, as well as the first report of the putative toxin source.

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.

Unexpected brevetoxin vectors may account for deaths long after or remote from an algal bloom.