Chapter 41 Algal Bloom Toxicity in Marine Animals
Harmful algal blooms (HABs) are becoming more frequent along all coasts of the United States and throughout the world1,2 (www.whoi.edu/redtide). The microalgal species within these blooms, including diatoms and dinoflagellates, produce a variety of marine biotoxins that may be harmful to marine organisms and people. Although marine organisms have likely coexisted with algal blooms for eons, the increased magnitude and severity of exposure to HABs and the acute and often fatal nature of the intoxications seem to have led to minimum evolutionary adaptation. Thus, all taxa of marine organisms, from invertebrates to marine mammals, have died from the algal marine biotoxins. Massive “fish kills” and unusual mortality events involving large species, such as manatees, sea lions, whales, small cetaceans, and giant squid, have been particularly remarkable.
Several well-recognized intoxications are named for the symptoms experienced by humans, who are largely exposed through the consumption of filter-feeding shellfish containing the marine biotoxins (Table 41-1).25 Briefly, these are paralytic shellfish poisoning (PSP) caused by saxitoxins; neurotoxic shellfish poisoning (NSP) resulting from brevetoxins; amnesic shellfish poisoning (ASP) from domoic acid; diarrheic shellfish poisoning (DSP) from okadaic acid, yessotoxin, and other toxins; azaspiracid shellfish poisoning (AZP); and ciguatera fish poisoning (CFP, ciguatera) caused by ciguatoxin and maitotoxin. Except in the case of ciguatera, shellfish are the usual vectors, although increasing evidence suggests that crustaceans and finfish may also be important in tropic transfer of all the algal biotoxins.10,36,43
|Toxin and Clinical Syndrome||Wildlife Species Affected (Vectors and/or Victims)||Location|
|Saxitoxins||Seabirds, whales, sea otters||North Atlantic, Northeastern U.S., Pacific Northwest and Alaska, Europe, Japan, Australasia|
|Paralytic shellfish poisoning (PSP)||Fish: herring, salmon, menhaden, sandlance, mackerel, puffer fish|
|Mussels, surfclams, softshell clams, sea scallops, butterclams, ocean quahogs, oysters, gastropods, lobsters, crabs, and other benthic invertebrates|
|Squid and zooplankton|
|Brevetoxins||Sea birds, manatees, dolphins||Subtropical regions: Gulf of Mexico, southern U.S. Atlantic coast|
|Neurotoxic shellfish poisoning (NSP)||Fish, sea turtles|
|Bay scallops, surf clams, oysters, southern quahogs, coquinas|
|Tunicates, sponges, coral|
|Domoic acid (DA)||Numerous bivalves, squid, crustaceans, fish, seabirds||Eastern Canada, west coasts of U.S. and Mexico, Gulf of California|
|Amnesic shellfish poisoning (ASP)|
|Otariid seals, sea otters|
|Humpback and blue whales|
|Ciguatoxin, maitotoxin||Fish: grouper, snapper, mackerel, jack, barracuda, parrot fish, tang, goat fish, and other finfish||Caribbean|
|Ciguatera fish poisoning (CFP)||Hawaii, South Pacific|
|Okadaic acid, dinophysistoxins, pectinotoxins, yessotoxin||Fish and shellfish as vectors, but no “fish kills”||Japan, Europe, Chile, Thailand, Canada (Nova Scotia), Australia, New Zealand|
|Experimental fish embryo death and deformities|
|Diarrheic shellfish poisoning (DSP)|
|Azaspiracid toxins||Shellfish vectors: mussels, oysters||Ireland|
|Azaspiracid shellfish poisoning (AZP)*||Incompletely studied||Not yet in North American waters|
Of these intoxications, brevitoxicosis (NSP) has had the most impact on wildlife historically and currently, especially in Florida. Domoic acid intoxication is increasingly recognized as a cause of pinniped, otter, seabird, and possibly cetacean mortality on the U.S. West Coast, but blooms of Pseudonitzschia spp. are not accompanied by the fish kills associated with red-tide blooms of Karenia brevis–secreting brevetoxins. Saxitoxicosis has been associated with deaths of marine birds and mammals. Ciguatera has been implicated in rare cases of pinniped mortality. The diarrheic shellfish toxins and those of the azaspiracid group to date have not been associated with wildlife mortality. These latter two conditions are not covered in this chapter, except to mention that experimental work suggests that they may have an effect on fish embryos.
Although marine toxins are most frequently a threat to free-living marine organisms, the potential for contamination of natural seawater used in exhibits or enclosures and food items fed to aquatic animals managed in captivity is real.44 Thus it is important for both zoo and wildlife veterinarians and pathologists to be familiar with the diagnosis, detection, and treatment of marine biotoxins in marine organisms. This chapter focuses on these aspects; for more detail about HABs, marine biotoxins, and experimental work in laboratory animals, consult review articles, government bulletins, and websites (www.rsmas.miami.edu/groups/niehs). *
Brevetoxins are produced by Karenia brevis (formerly Gymnodinium breve, Ptychodiscus breve) and a few other microalgae.57 Brevetoxin is actually a complex of several lipid-soluble polyether neurotoxins, designated PbTx 1 to 10, that open sodium-gated channels and cause influx of Na+ into cells. The toxins act on both the voluntary and the autonomic nervous system. Hemolytic toxins are also produced. Intoxication is by ingestion of contaminated prey or marine vegetation or through inhalation of toxins aerosolized during a bloom. Minimum effective concentration in food for humans is suspected to be about 78 to 120 μg/mg. Clinical signs of NSP caused by ingestion include diarrhea with abdominal pain, myalgia, ataxia, and temperature reversal (cold objects feel hot), and signs caused by inhalation include lacrimation, rhinorrhea, coughing, and potentiation of asthma.16
Saxitoxins (STX) are produced by dinoflagellates such as Alexandrium spp., Gymnodinium catenatum, and Pyrodinium bahamense.57 These toxins cause gastrointestinal (GI) signs and a variety of neurologic signs. Saxitoxins block sodium channels, preventing signal transmission along nerves. A dose of 1 to 4 mg of toxin is lethal in humans. Clinical signs of PSP include tingling and numbness beginning around the mouth, limb weakness, headache, nausea, and vomiting. Death may occur as acutely as within 4 hours of ingestion from respiratory paralysis.19
Domoic acid (DA) is a neuroexcitatory amino acid analog of L-glutamate produced by diatoms of the genus Pseudonitzschia, along with some macroalgae.26,57 DA binds to glutamate receptors in the central nervous system (CNS), causing sustained membrane depolarization and leading to neuronal excitotoxic death. Elevation of endogenous glutamate potentiates the process. Neurons in the limbic system, including the hippocampus, are most at risk. Vomiting, diarrhea, disorientation, memory loss, seizures, coma, and death have been reported in humans affected by ASP. Minimum effective concentration in ingested seafood for humans is suspected to be about 60 mg for GI signs and 270 mg for neurologic signs. Oral doses of 5 and 10 mg/kg in monkeys cause gagging and vomiting.55
Ciguatoxin and maitotoxin are the agents of CFP.54,57 These toxins are ingested in fish that have eaten the toxin-producing organisms Gambierdiscus toxicus, Prorocentrum spp., Ostreopsis spp., Coolia monotis, Thecadinium spp., and Amphidinium carterae. The toxins are highly potent, and ingestion of as little as 0.1 ng will cause clinical signs in humans. Serious, but not usually fatal, the clinical signs of ciguatera in humans include GI, neurologic, and cardiac effects such as arrhythmias and heart block. Neurocutaneous and systemic forms of illness may persist over a long time frame and may mimic multiple sclerosis or chronic fatigue syndrome.54
Invertebrate “shellfish,” principally bivalves and crustaceans, are important vectors for marine biotoxins, transferring the toxins to higher trophic levels. Some of the toxins (e.g., DA) are fairly rapidly excreted (depurated) by the invertebrates, whereas others (e.g., brevetoxins, saxitoxins) are lipophilic and may accumulate in tissues.
Bivalve and gastropod molluscs and octopi seem resistant to the effects of saxitoxin, and some accumulate high levels of the toxin without adverse affects.39,45 Some bivalves show adaptive aversion to toxic dinoflagellates.
Brevetoxins may be toxic to invertebrates. Loss of muscle control and decreased righting response are seen in crown conch (Melongema corona) and lettered olive (Oliva sayana), in which reported mortality rates varied from 55.5% to 69% (Florida Fish and Wildlife Institute, www.research.myfwc.com). No specific gross or histologic lesions could be attributed to the intoxication. Other invertebrates developing intoxication during Florida red-tide events caused by
Bivalves act as vectors of DA, and crabs such as the common sand crab also seem to uptake DA readily and may be vectors and useful monitors for the presence of DA in coastal environments.10,15 Effects of DA on bivalves have not been reported. A die-off of Humboldt squid (Dosidicus gigas) off the coast of California in 2005 was postulated to result from DA intoxication, and high DA levels have been found in digestive gland and branchial heart of cuttlefish (Sepia officinalis).11 Thus, cephalopods may serve as vectors of DA and may be victims as well.
Marine fish are also both vectors and victims of marine biotoxins. Periodic massive fish kills associated with K. brevis red tides have been reported since the 1800s in Florida’s coastal waters, where red tides are almost annual events (www.mote.org). For example, in the 1983 event, more than 150 tons of dead fish had to be removed from Tampa Bay. Clinical signs in fish include twisting and corkscrew swimming patterns that are sometimes quite violent, followed by abnormal orientation in the water, rapid shallow respiratory movements, respiratory failure, and death.57 Brevetoxin-like compounds may be secreted by HABs from Heterostigma spp. flagellates and have been associated with deaths of fish and invertebrates (including starfish) in Washington State.44 Postulated mechanisms of lethality include respiratory and cardiac paralysis, excessive mucus production coating the gills, and hypoxia from oxygen consumption by the blooms. No clinical signs other than death were reported, and lesions were not described. Hypoxic and anoxic zones have been reported in connection with blooms of marine algae, including K. brevis, such as that which occurred during the 2004–2005 red-tide event on the west coast of Florida near Tampa and Sarasota bays.40 These zones develop secondary to the presence of the blooms and decomposition of algal cells, dead fish, and other marine organisms and during the process of eutrophication.29
Fish mortality associated with saxitoxicosis has been reported in chub mackerel (Scomber japonicus), herring (Culpeus harengus), cod (Gadus morhua), and salmon (Oncorhynchus spp.).7,57,58 Clinical signs other than death have not been described. Other species of fish, such as puffer fish (Arothron spp.) and Atlantic mackerel (Scomber scombrus), appear to tolerate the toxin, and concentrations of saxitoxin in their livers increase with age and season, reaching a mean toxic concentration of 112.4 mg STX equivalent per 100 g of liver.7
Planktivorous fish such as Pacific sardines (Sardinops sagax) and northern anchovy (Engraulis mordax) are implicated as vectors of DA, and apparently they readily consume toxic diatoms. However, additional studies have confirmed that benthic fish may also contain this biotoxin.36,38 Anchovy exposed experimentally to DA have a variety of clinical signs, including spinning, inability to school, disorientation, and death.36 Fish consuming DA or gavaged orally quickly excrete (depurate) the toxin and thus are considered to be dangerous as vectors only during the course of an actual bloom.
Fish embryo and fingerling death and developmental anomalies may be induced experimentally by brevetoxins, saxitoxins, ciguatoxin, and azaspiracid in medaka (Oryzias latipes); saxitoxins in milkfish (Chanos chanos); and DA in zebra fish (Danio rerio).8,9,14,30,37,53 Effects have ranged from bradycardia and delayed development (azaspiracid-1) to scoliosis (ciguatoxins, brevetoxins) and encephaloceles (brevetoxin-1).