Evidence for a Novel Marine Harmful Algal Bloom: Cyanotoxin (Microcystin) Transfer from Land to Sea Otters

“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

Mass Stranding of Marine Birds Caused by a Surfactant-Producing Red Tide

In November-December 2007 a widespread seabird mortality event occurred in Monterey Bay, California, USA, coincident with a massive red tide caused by the dinoflagellate Akashiwo sanguinea. Affected birds had a slimy yellow-green material on their feathers, which were saturated with water, and they were severely hypothermic. We determined that foam containing surfactant-like proteins, derived from organic matter of the red tide, coated their feathers and neutralized natural water repellency and insulation. No evidence of exposure to petroleum or other oils or biotoxins were found. This is the first documented case of its kind, but previous similar events may have gone undetected. The frequency and amplitude of red tides have increased in Monterey Bay since 2004, suggesting that impacts on wintering marine birds may continue or increase

Observations of chlorophyll, fluorescence, phytoplankton species composition, and occurrence of foam and red tide patches were available from a series of stations in Monterey Bay.

<p>Solid symbols (dashed line) represent total chlorophyll collected weekly from the Santa Cruz Municipal Wharf from August 15 to December 15, 2007 (labelled SCW on the inset map); the solid line represents daily chlorophyll fluorescence data for the same time period from the M0 mooring. Red bars along the x-axis denote visual observations of red tides from stations depicted in the map (inset), with the letters above the red bars denoting dominant species (C = <i>Ceratium</i> spp., Co = <i>Cochlodinium</i> spp., A = <i>Akashiwo sanguinea</i>). Green bars denote visual observation of foam at the Santa Cruz Municipal Wharf. The bird strandings coincided with the largest red tides (note the chlorophyll and fluorescence) dominated exclusively by <i>A. sanguinea</i> and co-occuring with foam.</p

Correspondence between the spatial and temporal patterns of seabird strandings and red tide during November-December 2007 in Monterey Bay.

<p>Black circles represent the approximate location and magnitude of morbidity and mortality, and satellite data represent the red tide for panels (A–C). Three pulses of seabird stranding were observed: A) focused along the northern bay, B) focused in the south-central portion of the bay, and C) in both northern and central portions of the bay. In (A) and (B) the MERIS data indicate extreme bloom conditions above MCI level of ∼0.3. Although ideal for red tide detection, MERIS coverage was not adequate for the third pulse. In (C) the reddish discoloration on the MODIS true color image during the third pulse (28 Nov) shows the spatial extent and location of the red tide. Panels (D) and (E) show increased seabird stranding during the November–December 2007 red tide event. Light bars are 10-year average (1997–2006) standardized monthly stranding counts on nine Monterey Bay beaches. Dark bars are 2007 counts for western/Clark's grebes and Northern fulmar, the species most affected during the mass-stranding event. Panel (D) corresponds to the first stranding event, while panel (E) corresponds to the second and third waves of strandings.</p

Natural and laboratory produced wetting of normal feathers.

<p>A) Normal breast feather from a brown pelican after dipping in clean seawater. Note the minimal wetting and matting of feather barbs. B) Normal seawater after agitation for 30 seconds, then resting for 2 hours. Note the absence of surface foam. C) Normal-appearing breast feathers from a Northern fulmar after dipping in the test tube containing normal seawater. D) Normal breast feather from a brown pelican after dipping in surface foam collected near an <i>A. sanguinea</i> bloom in Monterey Bay. Contact with the foam resulted in severe wetting and matting of feather barbs. E) Senescent laboratory culture of <i>A. sanguinea</i> after agitation for 30 seconds, then resting for 2 hours. Note the persistence of a thick surface layer of foam. F) Normal breast feathers from a Northern fulmar after dipping in the surface foam derived from the senescent <i>A. sanguinea</i> culture, resulting in severe wetting and matting of feather barbs.</p

Aerial photograph taken 26 November, 2007 off Pajaro Dunes Colony (rectangular inset) in central Monterey Bay.

<p>A dense front of red tide is visible in the left foreground. A distinct line of surface foam is spatially associated with the red tide, along with aggregations of marine birds. Circular inset: a single non-senescent <i>Akashiwo sanguinea</i> cell.</p

Map of Monterey Bay showing distribution of sea otters dying due to microcystin intoxication (yellow circles).

<p>Note spatial association of sea otter strandings with coastal locations of river mouths, harbors, coastal ponds and embayments. Habitat utilization distributions for 4 radio-tagged, microcystin-poisoned otters are plotted as kernel density distributions fit to daily re-sighting locations (red shading, with regions of most intense shading corresponding to the habitats most frequently utilized by affected animals). Locations of freshwater samples collected during a “Super-bloom” of <i>Microcystis</i> in 2007 are indicated by green circles, with numbers that correspond with the microcystin concentrations listed in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0012576#pone-0012576-g001" target="_blank">Figure 1</a>.</p

Variation in microcystin detection between conventional “grab” samples and Solid Phase Adsorption Toxin Tracking (SPATT).

<p>Comparison of microcystin (MCY-LR) detection in fresh water using intermittent “grab” sampling (sample periods indicated by black circles) and SPATT (solid line indicating weekly averaged toxin values) in Pinto Lake, demonstrating the higher sensitivity of SPATT for microcystin detection. Grab samples were collected at the beginning of each weekly SPATT deployment, and from the same sample location, so each 7-day integrated SPATT deployment is bracketed by two grab samples.</p

Stranding information and microcystin (MCY) concentrations (ppb wet weight) for wild, microcystin-positive sea otters and captive controls.

1<p>nd  =  microcystin concentration was below minimum detection limits on liquid chromatography-tandem mass spectrophotometry.</p

Microcystin detection in sea otter tissues was linked to bivalve consumption, liver damage and icterus.

<p>A.) Wild southern sea otter (<i>Enhydra lutris nerei</i>s) consuming a clam in Elkhorn Slough, Monterey Bay. B.) Diffuse icterus of oral mucous membranes of an otter poisoned by microcystin, due to severe hepatic damage and elevated plasma bilirubin. C.) Severe icterus of cartilage at the costochondral junction in a sea otter that died due to microcystin intoxication.</p