Evidence for a novel marine harmful algal bloom: cyanotoxin (microcystin) transfer from land to sea otters

• Published in: PloS one 2010-09, Vol.5 (9), p.e12576
• Main Authors: Miller, Melissa A, Kudela, Raphael M, Mekebri, Abdu, Crane, Dave, Oates, Stori C, Tinker, M Timothy, Staedler, Michelle, Miller, Woutrina A, Toy-Choutka, Sharon, Dominik, Clare, Hardin, Dane, Langlois, Gregg, Murray, Michael, Ward, Kim, Jessup, David A
• Format: Article
• Language: English
• Subjects: Algae; Animals; Aquatic ecosystems; Aquatic habitats; Bacterial Toxins - analysis; Bacterial Toxins - metabolism; Bacterial Toxins - toxicity; Bioaccumulation; Biochemical analysis; Biological magnification; Clostridium perfringens; Coastal environments; Coasts; Cyanobacteria; Cyanobacteria - metabolism; Depuration; Drinking water; Ecological monitoring; Endangered species; Enhydra; Enhydra lutris nereis; Environmental impact; Environmental Monitoring; Environmental protection; Fatalities; Fish; Fresh water; Fresh Water - analysis; Freshwater environments; Freshwater lakes; Freshwater pollution; Gastroenterology and Hepatology/Hepatology; Harmful Algal Bloom; Health aspects; Heat shock proteins; Hepatotoxicity; Intoxication; Invertebrates; Laboratories; Lakes; Lutrinae; Marine; Marine and Aquatic Sciences; Marine and Aquatic Sciences/Biological Oceanography; Marine and Aquatic Sciences/Climate Change; Marine and Aquatic Sciences/Ecology; Marine and Aquatic Sciences/Microbiology; Marine ecosystems; Marine environment; Marine invertebrates; Marine mammals; Marine toxins; Microbiology/Environmental Microbiology; Microcystins; Microcystins - analysis; Microcystins - metabolism; Microcystins - toxicity; Microcystis; Mollusks; Mussels; Nutrients; Oceans; Otters; Otters - abnormalities; Otters - metabolism; Oysters; Pathogens; Plesiomonas shigelloides; Poisoning; Predators; Prevention; Public health; Public Health and Epidemiology/Environmental Health; Public Health and Epidemiology/Epidemiology; Public Health and Epidemiology/Global Health; Rivers; Runoff; Science; Seawater - analysis; Shellfish; Threatened species; Tissue analysis; Tissues; Toxoplasma gondii; Tributaries; Trophic levels; Veterinary medicine; Vibrio; Water levels; Water Pollutants - metabolism; Water Pollutants - toxicity; Water pollution; Water quality; Wildlife conservation
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0012576

"Super-blooms" of cyanobacteria that produce potent and environmentally persistent biotoxins (microcystins) are an emerging global health issue in freshwater habitats. Monitoring of the marine environment for secondary impacts has been minimal, although microcystin-contaminated freshwater is known to be entering marine ecosystems. Here we confirm deaths of marine mammals from microcystin intoxication and provide evidence implicating land-sea flow with trophic transfer through marine invertebrates as the most likely route of exposure. This hypothesis was evaluated through environmental detection of potential freshwater and marine microcystin sources, sea otter necropsy with biochemical analysis of tissues and evaluation of bioaccumulation of freshwater microcystins by marine invertebrates. Ocean discharge of freshwater microcystins was confirmed for three nutrient-impaired rivers flowing into the Monterey Bay National Marine Sanctuary, and microcystin concentrations up to 2,900 ppm (2.9 million ppb) were detected in a freshwater lake and downstream tributaries to within 1 km of the ocean. Deaths of 21 southern sea otters, a federally listed threatened species, were linked to microcystin intoxication. Finally, farmed and free-living marine clams, mussels and oysters of species that are often consumed by sea otters and humans exhibited significant biomagnification (to 107 times ambient water levels) and slow depuration of freshwater cyanotoxins, suggesting a potentially serious environmental and public health threat that extends from the lowest trophic levels of nutrient-impaired freshwater habitat to apex marine predators. Microcystin-poisoned sea otters were commonly recovered near river mouths and harbors and contaminated marine bivalves were implicated as the most likely source of this potent hepatotoxin for wild otters. This is the first report of deaths of marine mammals due to cyanotoxins and confirms the existence of a novel class of marine "harmful algal bloom" in the Pacific coastal environment; that of hepatotoxic shellfish poisoning (HSP), suggesting that animals and humans are at risk from microcystin poisoning when consuming shellfish harvested at the land-sea interface.