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

Melissa A. Miller, Raphael M. Kudela, Abdu Mekebri, Dave Crane, Stori C. Oates, M. Timothy Tinker, Michelle Staedler, Woutrina A Smith, Sharon Toy-Choutka, Clare Dominik, Dane Hardin, Gregg Langlois, Michael Murray, Kim Ward, David A. Jessup

Research output: Contribution to journalArticle

160 Citations (Scopus)

Abstract

"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, mussls 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.

Original languageEnglish (US)
Article numbere12576
Pages (from-to)1-11
Number of pages11
JournalPLoS One
Volume5
Issue number9
DOIs
StatePublished - 2010

Fingerprint

Otters
Harmful Algal Bloom
cyanobacterial toxins
Enhydra lutris
microcystins
Fresh Water
algal blooms
Microcystins
Oceans and Seas
Shellfish
poisoning
Mammals
Ecosystem
Bivalvia
Invertebrates
Nutrients
Rivers
marine mammals
bioaccumulation
death

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Miller, M. A., Kudela, R. M., Mekebri, A., Crane, D., Oates, S. C., Tinker, M. T., ... Jessup, D. A. (2010). Evidence for a novel marine harmful algal bloom: Cyanotoxin (microcystin) transfer from land to sea otters. PLoS One, 5(9), 1-11. [e12576]. https://doi.org/10.1371/journal.pone.0012576

Evidence for a novel marine harmful algal bloom : Cyanotoxin (microcystin) transfer from land to sea otters. / Miller, Melissa A.; Kudela, Raphael M.; Mekebri, Abdu; Crane, Dave; Oates, Stori C.; Tinker, M. Timothy; Staedler, Michelle; Smith, Woutrina A; Toy-Choutka, Sharon; Dominik, Clare; Hardin, Dane; Langlois, Gregg; Murray, Michael; Ward, Kim; Jessup, David A.

In: PLoS One, Vol. 5, No. 9, e12576, 2010, p. 1-11.

Research output: Contribution to journalArticle

Miller, MA, Kudela, RM, Mekebri, A, Crane, D, Oates, SC, Tinker, MT, Staedler, M, Smith, WA, Toy-Choutka, S, Dominik, C, Hardin, D, Langlois, G, Murray, M, Ward, K & Jessup, DA 2010, 'Evidence for a novel marine harmful algal bloom: Cyanotoxin (microcystin) transfer from land to sea otters', PLoS One, vol. 5, no. 9, e12576, pp. 1-11. https://doi.org/10.1371/journal.pone.0012576
Miller, Melissa A. ; Kudela, Raphael M. ; Mekebri, Abdu ; Crane, Dave ; Oates, Stori C. ; Tinker, M. Timothy ; Staedler, Michelle ; Smith, Woutrina A ; Toy-Choutka, Sharon ; Dominik, Clare ; Hardin, Dane ; Langlois, Gregg ; Murray, Michael ; Ward, Kim ; Jessup, David A. / Evidence for a novel marine harmful algal bloom : Cyanotoxin (microcystin) transfer from land to sea otters. In: PLoS One. 2010 ; Vol. 5, No. 9. pp. 1-11.
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