Trophic transfer of domoic acid in food webs of the future greenhouse coastal ocean

David A. Hutchins, Professor, University of Southern California
Feixue Fu, Assistant Research Professor, University of Southern California

Project Overview:

The coastal ocean is currently changing rapidly as it responds to anthropogenic climate change and warming. Among the most biologically significant human impacts on ocean climate and chemistry are greenhouse warming and ocean acidification. The ocean surface as a whole is predicted to experience greenhouse warming of between 1-6oC over the next 100 years (Bopp et al. 2001, Alley et al. 2007), while at the same time surface seawater pH will fall by at least 0.2 units, to levels that have not been experienced by extant marine organisms for millions of years (Royal Society 2005, Hutchins et al. 2009). Both ocean acidification and warming are likely to have major implications for harmful algal blooms (Hallegraef 2010, Fu et al. 2010, 2012), such as the massive regional toxic Pseudo-nitschia blooms that occur most years along the coastlines of California and the Pacific Northwest.

Previous USC Sea Grant-supported work has shown that both warming and ocean acidification can greatly increase the cell-specific toxicity of our local Pseudo-nitzschia species.  A reasonable hypothesis is that these enhanced toxin levels in diatom prey cells may in turn result in higher domoic acid levels in the planktonic and benthic grazers that eat them. These secondary consumers then act as vectors to transfer and further concentrate the toxin in marine food webs. This would further exacerbate the negative impacts of Pseudo-nitzschia blooms on higher trophic levels (including marine mammals, birds, fish, and humans) that feed directly or indirectly on these secondary consumers.

To fully predict the future impacts of domoic acid-producing blooms on critical economic activities in our area such as shellfish hatcheries and growers and squid and finfish fisheries, though, we need to go beyond just demonstrating how the toxin levels of Pseudo-nitzschia cells will increase under greenhouse conditions. We also need to be able to predict how ocean acidification and warming will affect toxin transfer to planktonic and benthic grazers, since they are the first key step in the trophic bio-concentration process that determines how much domoic acid ultimately ends up in valuable harvested resources such as mussels, oysters, squid, and fish.

Consumption of toxic Pseudo-nitzschia cells by benthic filter-feeding bivalves has been widely documented, including mussels, oysters, razor clams, and scallops (Bates et al. 1989, Perl et al. 1990, Busse et al. 2006, Blanco et al. 2006a,b, Litaker et al. 2008, Mafra et al. 2010a,b). Of course, any of the various routes detailed above can result in upper trophic levels, including marine mammals, seabirds and humans, being exposed to dangerous levels of domoic acid. Shellfish, either wild or aquacultured, are probably the most problematic vector for potential human exposure. For instance, in one such event in Canada, consumption of contaminated aquacultured mussels resulted in 107 confirmed cases of domoic acid poisoning and three deaths (Bates et al. 1989, Perl et al. 1990).

Therefore, accurately predicting the future responses of Pseudo-nitzschia blooms to interactions between acidification and warming is a top priority for everyone who must deal with the negative impacts of these toxic algal blooms, including marine resource managers, policy makers, governmental management agencies, and particularly marine resource users such as the fishing and aquaculture industries.

2016 Research Update:

Results show that increases in both water temperatures and CO2 levels (similar to those seen in the 2015 warm water event off California) resulted in increased toxicity and growth rates of local Pseudo-nitzschia populations. The experiments also demonstrated that the relative abundance of Pseudo-nitzschia always increases compared to other co-occurring diatom species when temperatures are elevated, thus this diatom is more toxic, grows faster, and outcompetes all others at warmer temperatures. These experiments suggest that ecologically and economically devastating toxic events like the one in 2015 are likely to become more common in the future as the California coastal regime continues to warm, and CO₂concentrations continue to rise. 

These results are in review for two publications and demonstrate how global climate change may affect the prevalence of toxic algal blooms off the U.S. West Coast.

Previously Funded Research

• Short- Versus Long-Term Responses To Changing Co2 In A Coastal Dinoflagellate Bloom: Implications For Interspecific Competitive Interactions And Community Structure

Publications

• High CO₂ promotes the production of paralytic shellfish poisoning toxins by Alexandrium catenella from Southern California waters

• Short- and long-term conditioning of a temperate marine diatom community to acidification and warming

• Microbial biogeochemistry of coastal upwelling regimes in a changing ocean 
• Global change and the future of harmful algal blooms in the ocean