Persistent domoic acid in marine sediments and benthic infauna along the coast of Southern California

Highlights

• Study reports first regional survey of domoic acid in the benthic environment

• Domoic acid was detected in 54% of continental shelf sediments

• Domoic acid was consistently measured in benthic infauna tissues for 16-months

• The uptake and retention of domoic acid may vary among infauna taxa

Abstract

Blooms of the diatom genus Pseudo-nitzschia occur annually in the Southern California Bight (SCB), and domoic acid (DA) associated with these events can contaminate fisheries, presenting both human and wildlife health risks. Recent studies have suggested that marine sediments may act as a reservoir for DA, extending the risk of food web contamination long after water column blooms have ended. In this study, we conducted a regional assessment of the extent and magnitude of DA in the benthic environment, and monthly observations of sediments and benthic infauna at multiple stations over a 16-month period. DA was widespread in continental shelf sediments of the SCB. The toxin was detected in 54% of all shelf habitats sampled. Detectable concentrations ranged from 0.11 ng/g to 1.36 ng/g. DA was consistently detected in benthic infauna tissues over the monthly timeseries, while the DA concentrations in sediments during the same period were commonly below detection or at low concentrations. The presence of DA in the benthic environment did not always have an apparent water column source, raising the possibility of lateral transport, retention/preservation in sediments or undetected blooms in subsurface waters. In most cases, DA was detected in tissues but not in the co-located surface sediments. Coarse taxonomic sorting of the infauna revealed that the accumulation of DA varied among taxa. We observed that DA was widespread among lower trophic level organisms in this study, potentially acting as a persistent source of DA to higher trophic levels in the benthos.

Introduction

Harmful algal blooms (HABs) and associated algal toxins have been a persistent and escalating issue in southern California's coastal and inland waterbodies (Anderson et al., 2006; Busse et al., 2006; Howard et al., 2021; Schnetzer et al., 2013; Shipe et al., 2008; Smith et al., 2018; Tatters et al., 2019; Umhau et al., 2018). Globally, HABs have increased in frequency, severity and spatial extent over the past decade, and anthropogenic nutrient inputs and warmer temperatures (i.e. climate change) are considered the most significant factors contributing to these increases (Anderson et al., 2021; Glibert et al., 2005; Gobler et al., 2017; Hallegraeff et al., 2004; O'Neil et al., 2012; Paerl et al., 2011).

The Southern California Bight (SCB) is a roughly 700 km portion of the U.S. West Coast that extends from Point Conception, California south to beyond the U.S. international border with Mexico. The most commonly observed HAB organisms in the SCB are species within the diatom genus Pseudo-nitzschia, several of which produce the neurotoxin domoic acid (DA). Annual blooms of Pseudo-nitzschia spp. and measurable concentrations of DA have been documented along the California coast since the 1990s and annually in the SCB since 2003. (Schnetzer et al., 2007). Trophic transfer of DA in the food web can contaminate fisheries, presenting both human and wildlife health hazards. Consumption of contaminated seafood is the cause of amnesic shellfish poisoning (ASP) in humans, resulting in symptoms of diarrhea, gastrointestinal pain, disorientation and memory loss, and in extreme cases, death (Bates et al., 1989). Stranding and mortality events in marine mammals and birds have also been attributed to exposure to DA (Fire et al., 2010; Lefebvre et al., 2002; Smith et al., 2018). DA events have also caused major socioeconomic impacts, including prolonged closures of key fish, bivalve and crab fisheries (McCabe et al., 2016; Moore et al., 2020).

A majority of work to date in the SCB has focused on characterizing DA within shellfish tissues and within suspended particulate material (i.e. plankton). Monitoring over the last 15 years has shown that DA has been observed in shellfish tissue on a near-annual basis in the region (Smith et al., 2018). Particulate DA concentrations observed during toxigenic blooms of Pseudo-nitzschia spp. in the SCB often exceed concentrations of 10 μg/L and some events have even exceeded 50 μg/L (Smith et al., 2018). Observations of dissolved DA concentrations have been more limited in the region, but recent work has indicated that dissolved DA may be a significant fraction of the total DA (particulate plus dissolved DA) pool with contributions as high as 50% (Umhau et al., 2018). Similarly, a few studies have demonstrated the rapid transport of DA into the benthos during bloom events in the SCB (Schnetzer et al., 2007; Sekula-Wood et al., 2011, 2009; Umhau et al., 2018), providing only limited insight into the presence or longevity of DA in benthic environments in the SCB.

The role of the benthos in extending the ecological and socioeconomic impacts of DA producing blooms is largely understudied, but recent events have underscored the need to resolve these dynamics. In 2015, a nearly West Coast wide bloom of Pseudo-nitzschia persisted for multiple months (Du et al., 2016; McCabe et al., 2016; Ryan et al., 2017) and resulted in extensive impacts on multiple species of marine mammals, birds, and fish (McCabe et al., 2016). The bloom also caused closures of both commercial and recreational Dungeness crab and razor clam fisheries along the U.S. West Coast that extended for over a year after the bloom ended due to prolonged contamination with DA (Ekstrom et al., 2020). The long-term impacts of the 2015 bloom were attributed to the presence of DA in the benthos. Several studies have indicated the prevalence of DA in benthic species (Kvitek et al., 2008; Lefebvre et al., 2002; Vigilant and Silver, 2007), suggesting marine sediments may be a long term reservoir for DA and temporally expand the impacts of DA producing blooms.

While the pelagic impacts of DA have been well studied, the fate and environmental persistence of DA has been historically understudied. The goal of this study was to address our knowledge gap relating to the long-term impacts and fate of DA in the coastal benthic habitat of the SCB. The overall objectives of this study were to determine the extent and magnitude of DA on the continental shelf sediments in the SCB as well as to determine how concentrations of DA vary in the sediments temporally in relation to toxin concentrations present in benthic infauna. We conducted, to our knowledge, the first regional assessment of DA presence in the benthic environment of any continental shelf ecosystem. This was complemented with a 16-month time-series to investigate how DA concentrations vary throughout the year in both the sediments and infauna.