Investigation of a Mass Stranding Event Reveals a Novel Pattern of Cascading Comorbidities in Northern Fulmars (Fulmarus glacialis).

During 2018, a seabird mortality event occurred in central California, US, that affected Northern Fulmars (Fulmarus glacialis), Common Murres (Uria aalge), and Cassin's Auklets (Ptychoramphus aleuticus). An increase in beachcast birds were reported on standardized surveys in conjunction with an increased number of live-stranded birds admitted to rehabilitation centers. Neurologic symptoms were noted during intake examination for some birds. Coincident with the mortality event, increased levels of the harmful algal bloom toxins domoic acid and saxitoxin were recorded in Monterey Bay and Morro Bay. Birds that died in care and beachcast carcasses were submitted to the California Department of Fish and Wildlife-Marine Wildlife Veterinary Care and Research Center for postmortem examination (n=24). All examined birds were emaciated. Examined Common Murres and Cassin's Auklets had no gross evidence of preexisting disease; however, all examined Northern Fulmars exhibited severe pyogranulomatous inflammation of the urogenital system at gross postmortem exam. Tissues from nine Northern Fulmars were examined by histopathology, and samples from two Northern Fulmars were tested for the presence of domoic acid and saxitoxin. Histopathology revealed moderate to severe kidney infection by Eimeria sp. and gram-negative bacteria, intratubular urate stasis, ureter rupture, and emaciation. Additionally, domoic acid and saxitoxin were detected simultaneously in tissues of some tested birds. This communication highlights a novel pattern of cascading comorbidities in native seabirds from a mass stranding event.

Domoic acid and saxitoxin in seabirds in the United States between 2007 and 2018.

As harmful algal blooms (HABs) increase in magnitude and duration worldwide, they are becoming an expanding threat to marine wildlife. Over the past decade, blooms of algae that produce the neurotoxins domoic acid (DA) and saxitoxin (STX) and documented concurrent seabird mortality events have increased bicoastally in the United States. We conducted a retrospective analysis of HAB related mortality events in California, Washington, and Rhode Island between 2007 and 2018 involving 12 species of seabirds, to document the levels, ranges, and patterns of DA and STX in eight sample types (kidney, liver, stomach, intestinal, cloacal, cecal contents, bile, blood) collected from birds during these events. Samples (n = 182) from 83 birds were examined for DA (n = 135) or STX (n = 17) or both toxins simultaneously (n = 30), using ELISA or LCMS at the National Oceanographic and Atmospheric Administration, National Marine Fisheries Service (NOAA-NMFS) Wildlife Algal-toxin Research and Response Network (WARRN-West) or the University of California, Santa Cruz (UCSC). DA or STX was detected in seven of the sample types with STX below the minimum detection limit in blood for the three samples tested. DA was found in 70% and STX was found in 23% of all tested samples. The ranges of detectable levels of DA and STX in all samples were 0.65-681,190.00 ng g-1 and 2.00-20.95 ng g-1, respectively. Cloacal contents from a Pacific loon (Gavia pacifica) collected in 2017 from Ventura County, California, had the highest maximum level of DA for all samples and species tested in this study. The highest level of STX for all samples and species was detected in the bile of a northern fulmar (Fulmarus glacialis) collected in 2018 from San Luis Obispo County, California. DA detections were consistently found in gastrointestinal samples, liver, bile, and kidney, whereas STX detections were most frequently seen in liver and bile samples. Co-occurring HAB toxins (DA and STX) were detected in white-winged scoters (Melanitta deglandi) in 2009, a Brandt's cormorant (Phalacrocorax penicillatus) in 2015, and a northern fulmar and common murre (Uria aalge) in 2018. This article provides DA and STX tissue concentrations and patterns in avian samples and shows the utility of various sample types for the detection of HAB toxins. Future research to understand the pharmacodynamics of these toxins in avian species and to establish lethal doses in various bird species would be beneficial.

Blurred lines: Multiple freshwater and marine algal toxins at the land-sea interface of San Francisco Bay, California.

San Francisco Bay (SFB) is a eutrophic estuary that harbors both freshwater and marine toxigenic organisms that are responsible for harmful algal blooms. While there are few commercial fishery harvests within SFB, recreational and subsistence harvesting for shellfish is common. Coastal shellfish are monitored for domoic acid and paralytic shellfish toxins (PSTs), but within SFB there is no routine monitoring for either toxin. Dinophysis shellfish toxins (DSTs) and freshwater microcystins are also present within SFB, but not routinely monitored. Acute exposure to any of these toxin groups has severe consequences for marine organisms and humans, but chronic exposure to sub-lethal doses, or synergistic effects from multiple toxins, are poorly understood and rarely addressed. This study documents the occurrence of domoic acid and microcystins in SFB from 2011 to 2016, and identifies domoic acid, microcystins, DSTs, and PSTs in marine mussels within SFB in 2012, 2014, and 2015. At least one toxin was detected in 99% of mussel samples, and all four toxin suites were identified in 37% of mussels. The presence of these toxins in marine mussels indicates that wildlife and humans who consume them are exposed to toxins at both sub-lethal and acute levels. As such, there are potential deleterious impacts for marine organisms and humans and these effects are unlikely to be documented. These results demonstrate the need for regular monitoring of marine and freshwater toxins in SFB, and suggest that co-occurrence of multiple toxins is a potential threat in other ecosystems where freshwater and seawater mix.

Evidence of freshwater algal toxins in marine shellfish: Implications for human and aquatic health.

The occurrence of freshwater harmful algal bloom toxins impacting the coastal ocean is an emerging threat, and the potential for invertebrate prey items to concentrate toxin and cause harm to human and wildlife consumers is not yet fully recognized. We examined toxin uptake and release in marine mussels for both particulate and dissolved phases of the hepatotoxin microcystin, produced by the freshwater cyanobacterial genus Microcystis. We also extended our experimental investigation of particulate toxin to include oysters (Crassostrea sp.) grown commercially for aquaculture. California mussels (Mytilus californianus) and oysters were exposed to Microcystis and microcystin toxin for 24h at varying concentrations, and then were placed in constantly flowing seawater and sampled through time simulating riverine flushing events to the coastal ocean. Mussels exposed to particulate microcystin purged the toxin slowly, with toxin detectable for at least 8 weeks post-exposure and maximum toxin of 39.11ng/g after exposure to 26.65µg/L microcystins. Dissolved toxin was also taken up by California mussels, with maximum concentrations of 20.74ng/g after exposure to 7.74µg/L microcystin, but was purged more rapidly. Oysters also took up particulate toxin but purged it more quickly than mussels. Additionally, naturally occurring marine mussels collected from San Francisco Bay tested positive for high levels of microcystin toxin. These results suggest that ephemeral discharge of Microcystis or microcystin to estuaries and the coastal ocean accumulate in higher trophic levels for weeks to months following exposure.