Invertebrates, fish, birds, and mammals can be harmed when they are exposed to Florida red tide toxins in the water, sediments, or aerosol.
Some harmful algal blooms (HABs) tend to be planktonic and visibly obvious. Their effects are fast acting and can lead to acute shellfish poisoning events or mass mortalities of aquatic organisms. These are the HABs about which most is known. Compared to those HAB species that are a risk to human health, far less is known about the origin, fate, or effects of many other HAB species and their effects on aquatic organisms.
Because many of the HAB species and their toxins have been investigated in terms of their effects on mammalian systems, the greatest amount of information is available for these groups. Some of these toxins may affect other aquatic organisms in similar or unsuspected ways (see 2005 Red Tide Impacts on Fish Spawning in Tampa Bay). Many HAB species that are nontoxic to humans or small mammals in bioassays, however, can have significant effects on aquatic organisms. Some microalgal species may produce multiple toxic compounds, although only a few of these toxins have been tested for toxicity to aquatic organisms. Typically, aquatic animals are exposed to toxic or harmful concentrations of algae when planktonic or epibenthic species bloom and dominate the food web, but there are also more subtle and insidious exposure mechanisms that are not so obvious.
Aquatic organisms can be exposed to harmful microalgae and their toxins through a variety of mechanisms, including direct ingestion of cells (filter feeders, such as sponges, zooplankton, mollusks, crustacea); exposure to waterborne toxin after cell lysis or exudation (fish, shellfish); aerosolized transport (e.g., respiratory irritation in mammals, turtles, birds); bioaccumulation through consumption of prey containing toxins or toxic cells (crustacea, gastropods, fish, birds, turtles, mammals); sediment sinks (benthic organisms) possibly through consumption of toxic benthic stages; and mechanical damage by spines, setae, or other anatomical features of the cells. Benthic communities such as submerged aquatic vegetation can be affected by surface blooms that decrease light penetration or produce bioactive metabolites.
Aquatic organisms may be exposed to toxins or harmful algae through four main routes: (1) the water that they inhabit, (2) inhalation of aerosolized toxins by air-breathing aquatic organisms, (3) exposure to toxins or toxic stages present in sediments or in other organisms and that are ingested as food, and (4) mechanical contact with cells.
Karenia brevis is one of the first species ever reported to have caused a HAB. Fish kills have been documented since 1844, but the causative dinoflagellate was not identified and named until the 1946-1947 outbreak.
Karenia brevis is principally distributed throughout the Gulf of Mexico, with occasional red tides in the mid- and south-Atlantic United States.
Although shellfish poisonings from eating bivalves in Florida were known since the 1880s, the cause was not identified until the 1960s.
Neurotoxic shellfish poisoning (NSP) is caused by the consumption of shellfish contaminated by brevetoxins and, thus far, has only been associated with bivalves and a whelk species.
The first written report of respiratory irritation due to a Florida red tide was made in 1917. People can suffer from respiratory effects when brevetoxins become aerosolized through the disruption of K. brevis cells by breaking waves, surf, or onshore winds.
Bubble-mediated transport has been shown to be a major factor in concentration of brevetoxins from Karenia brevis at the sea surface, with subsequent production of toxin-containing marine aerosol. Terrestrial organisms or air-breathing mammals and reptiles are potentially exposed to aerosolized toxins in this manner.
There have been several documented cases in the field where K. brevis blooms have killed invertebrates. Except for five benthic species of polychaetes and a brachiopod, at least 17 invertebrate species normally present in Tampa Bay, Florida, were absent immediately after a red tide. Dominant species killed included several amphipod species.
Other species have been acutely affected by exposure to K. brevis. The mollusk banded tulip (Fasciolaria lilium hunteria), crown conch (Melongema corona), and lettered olive (Oliva sayana) lost muscle control and could not right themselves. Mortality rates varied from 55.5-69 percent. Gross pathology and histopathology of internal tissues did not reveal any differences between exposed and control animals. Crabs did not retain toxins when fed toxic shellfish (Roberts et al., 1979).
Recruitment of the bay scallop, Argopecten irradians, was significantly affected by the North Carolina red tide of 1987. Bay scallops are a potential health risk, but they are usually safe if people only eat the adductor muscle, which has no brevetoxins.
Brevetoxins are potent ichthyotoxins and have been responsible for the death of billions of fish over the years. Fish mortalities associated with Karenia brevis events are very common and widespread. The mortalities affect hundreds of species during various stages of development. Brevetoxin is absorbed directly across the gill membranes of fish or through ingestion of K. brevis cells.
Intoxication begins with binding of PbTx to specific receptor sites in fish excitable tissues (Baden and Mende, 1982); toxin binds with high affinity, for example, to Tilapia brain synaptosomes (Stuart and Baden, 1988). Signs of intoxication in fish include violent twisting and corkscrew swimming, defecation and regurgitation, pectoral fin paralysis, caudal fin curvature, loss of equilibrium, quiescence, vasodilation, and convulsions, culminating in death due to respiratory failure.
In some instances, mortality from red tide is not acute but may occur over a period of days or weeks of exposure to subacute toxin concentrations.
Mortality typically occurs at cell concentrations of 2.5 x 105 K. brevis cells/L, which is often considered to be a lethal concentration. However, it is known that fish can die at lower cell concentrations and can also apparently survive in much higher concentrations (at 3 million cells/L).
Some of these toxicity differences will depend on the differential susceptibility of fish species to exposure to K. brevis strains involved, toxic components and concentration, stability of extracellular toxins, and exposure routes.
See Fish Kill information for instructions about reporting fish kills and other fish abnormalities.
BIRDS AND MAMMALS
In addition to the usual reports of dead fish during the Florida west coast K. brevis red tide of October 1973 to May 1974, large numbers of aquatic birds, particularly double-crested cormorants, Phalacrocorax auritus, red-breasted mergansers, Mergus merganser, and lesser scaup, Aythya affinis, were found moribund or dead in red tide areas. Over an eight-week period, several thousand lesser scaup died.
All scaup examined had substantial subcutaneous fat and normal breast muscles indicative of acute mortality. Most of the ducks had recently fed and the proventriculi contained turritellid, pyramidellid, and opisthobranch gastropods, as well as amethyst gemclams, Gemma gemma. Clinical signs included weakness, reluctance to fly, slumping of the head, clear nasal discharge, viscous oral discharge, oil gland dysfunction, excessive lacrimation, chalky yellow diarrhea, dyspnea, tachypnea, tachycardia, decreased blood pressure, depressed body temperature, diminished reflexes, and dehydration. White Pekin ducklings were exposed to red tide toxins either through force feeding with toxic northern quahogs, Mercenaria mercenaria, (assayed at 48 MU/100 g tissue) and/or red tide water containing 22 million Karenia brevis cells/L. Ducklings showed signs of toxicity two days after exposure and appeared lethargic. On Day 3, ducklings showed ataxia, spastic movements of the head and a tendency to droop the head to one side. Over the next few days, the ducks died, exhibiting signs similar to those in field observations of moribund birds. Reports of dead birds during red tide events are not unusual but are not necessarily documented in the scientific literature.
During 1946-1947 and 1953-1955, two of the largest K. brevis red tide events on record, with respect to both geographical distribution and longevity, occurred in central and southwest Florida. Catastrophic mortalities of marine animals were recorded from Tarpon Springs to Key West (some 150 miles of coastline). During these events, there were reports of dead bottlenose dolphins (Tursiops truncatus), sea turtles, and numerous fish species. Mass mortalities of dolphins were reported in north Florida in the last year (August-December 1999), during which more than 100 dolphins stranded (B. Mase, NOAA, personal communication). In other years, there have been numerous reports of individual dolphin strandings.
By far the largest K. brevis-associated dolphin mortality involved more than 740 bottlenose dolphin strandings along the Atlantic coast from June 1987 to May 1988. Estimates that more than 50 percent of the coastal migratory stock between New Jersey and Florida died during this period. Brevetoxin was suspected as the proximate cause of the mortality. Although infectious agents (Vibrio, virus) were found in numerous individuals, these were likely to be secondary to brevetoxicosis. The spatial and temporal patterns of mortality also lacked the hallmark of infectious disease.
Karenia brevis was implicated in deaths of the endangered Florida manatee, Trichechus manatus latirostris, in 1963, 1982, and 1996, when seven, 39, and 149 animals, respectively, died in southwest Florida during the winter/spring.
The circumstances surrounding the large-scale mortality of manatees in 1982 and 1996 were attributed to a set of unusual environmental conditions. Karenia brevis, which typically develops 18-74 km offshore at low concentrations, usually comes inshore during the fall/winter and then dissipates.
Red tides do not usually appear inshore during the winter/spring months when manatees are congregated in low- or zero-salinity areas in the warmer waters of the coastal power plants, at warm water spring refugia, or in residential canals. Unusually, in the winter/spring of 1982 and 1996, red tide encroached inside the barrier islands of southwest Florida. High-salinity areas (above 24 ppt) allowed persistently high concentrations of K. brevis cells (>1 x 105/L) to be maintained. In the spring, as the water temperature warms, manatees usually disperse downstream into the inshore bays. If red tide has come inshore during this period (as occurred in 1982 and 1996), then the likelihood of manatees being exposed to red tide during their post-winter movements is fairly high and depends on where manatees move and their proximity to the red tide bloom.
Presence of brevetoxins in nasal and lung tissue implicate the aerosol and lesions of the upper respiratory tract were the only severe and consistent inflammatory lesions seen in the manatees from the epizootic. Therefore, there are three potential routes of toxicosis: (1) toxic aerosol inhalation, (2) toxic food ingestion, and (3) toxic seawater intake.
Baden, D.G., and T.J. Mende. 1982. Toxicity of tow toxins from the Florida red tide marine dinoflagellate, Gymnodinium breve. Toxicon 20:457-461.
Roberts, B.S.A., Henderson, G.E., and Medlyn, R.A. 1979. The effect of Gymnodinium breve toxin (s) on selected mollusks and crustaceans. In: Toxic Dinoflagellate Blooms, eds. Taylor, D.L. & Seliger, H.H., Elsevier, North Holland, pp. 419-424.
Stuart, A.M., and D.G. Baden. 1988. Florida red tide brevetoxins and binding in fish brain synaptosomes. Aquat. Toxicol. 13:271-280.