Subsurface seeding of surface harmful algal blooms observed through the integration of autonomous gliders, moored environmental sample processors, and satellite remote sensing in southern California

An observational study was performed in the central Southern California Bight in Spring 2010 to understand the relationship between seasonal spring phytoplankton blooms and coastal processes that included nutrient input from upwelling, wastewater effluent plumes, and other processes. Multi-month Webb Slocum glider deployments combined with MBARI environmental sample processors (ESPs), weekly pier sampling, and ocean color data provided a multidimensional characterization of the development and evolution of harmful algal blooms (HABs). Results from the glider and ESP observations demonstrated that blooms of toxic Pseudo-nitzschia sp. can develop offshore and subsurface prior to their manifestation in the surface layer and/or near the coast. A significant outbreak and surface manifestation of the blooms coincided with periods of upwelling, or other processes that caused shallowing of the pycnocline and subsurface chlorophyll maximum. Our results indicate that subsurface populations can be an important source for “seeding” surface Pseudo-nitzschia HAB events in southern California. Coastal continental shelf regions are areas of high ocean primary production and efficient energy transfer to higher trophic levels, contributing to their ecological and economical value. These shelf regions are also vulnerable to harmful algal blooms (HABs), which are defined as significant increases in phytoplankton biomass with harmful consequences such as toxin production or the accumulation of biomass that negatively impacts food-web dynamics and ecosystem structure. Globally, the occurrence of HABs has been increasing for decades accompanied by longer bloom duration and increased toxicity (e.g., Hallegraeff 1993). The diatom Pseudo-nitzschia, a predominant HAB genus of concern, produces the neurotoxin domoic acid (DA) that threatens the health of humans and wildlife from invertebrates to marine mammals and birds. Further details on Pseudo-nitzschia, including its physiology, toxicity, and global impacts of toxic events, have been thoroughly summarized in reviews by Anderson et al. (2012), Lelong et al. (2012), and Trainer et al. (2012). The negative ecological and economic impacts of HABs have resulted in a desire for increased understanding of the physical, chemical, and biological variables influencing their success in natural phytoplankton communities. Many HAB events are studied opportunistically or have limited synoptic sampling, resulting in an inability to resolve the bloom initiation and subsequent evolution. In addition, HAB research often relies on remote sensing and surface sampling and, therefore, limits observations to the near-surface region. A fundamental drawback of this approach is that it visualizes only a fraction of the water column and the euphotic zone. In the Southern California Bight (SCB), much focus has been given to the upwelling nutrient dynamics influence on HABs (Kudela et al. 2005, 2010; Pitcher et al. 2010). A variety of predictive models that typically rely on nutrient concentrations and ratios, temperature, mixed layer depth, and stratification strength have been developed to better understand the conditions under which Pseudo-nitzschia blooms develop, but these models have had limited predictive power (e.g., Lane et al. 2009; Anderson et al. 2011). The models often focus on the availability of upwelled nutrients in surface waters to support growth and accumulation of the surface *Correspondence: [email protected] 1 LIMNOLOGY and OCEANOGRAPHY Limnol. Oceanogr. 00, 2015, 00–00 VC 2015 Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10082 phytoplankton community into blooms. The models tend to overlook subsurface phytoplankton communities that are upwelled along with the nutrients into the surface layer and affect surface plankton community composition and bloom initiation. Unfortunately, much of the subsurface structure and dynamics are often missed by standard monitoring methods. Studies have shown that HABs can be entrained into surface water masses that can advect cells great distances both along shore and cross-shelf. Trainer et al. (2002) and MacFadyen et al. (2008) documented this transport of Pseudonitzschia and its impact on coastal waters along the Washington coast. More recently, the importance of subsurface thin layers as a source for surface HAB events was hypothesized as an explanation for the sudden appearance of HAB species and events (Rines et al. 2002; McManus et al. 2008). Tilstone et al. (2000) showed that Iberian upwelling could transport diatoms on the shelf and Crespo et al. (2007) suggested that surface currents could then transport the diatoms. Field observations have shown the potential importance of upwelling transport of subsurface dinoflagellate populations to initiate and maintain surface blooms (e.g., Tyler and Seliger 1978; Pitcher et al. 1998, 2010). Modeling results have also shown wind-driven subsurface Ekman flow could move subsurface phytoplankton population into surface layers initiating blooms (Janowitz and Kamykowski 2006), yet these types of movements and initiation events have been unobserved for diatoms. The goal of this effort was to better understand the onset and connections between subsurface and surface blooms of the toxic diatom, Pseudo-nitzschia, off the southern California coast. Toxic blooms of Pseudo-nitzschia are a recurring problem in this area with some of the highest DA concentrations per cell reported for natural populations (Schnetzer et al. 2007, 2013). San Pedro Bay, in the central SCB, is strongly influenced by both anthropogenic urban inputs and coastal upwelling, both of which can contribute to phytoplankton blooms and HAB events. Major sources of anthropogenic nutrients in this region include two ocean outfall diffusers operated by the Orange County Sanitation District (OCSD) and the Los Angeles County Sanitation District and three channelized riverine sources (Los Angeles River, San Gabriel River, Santa Ana River). Wastewater effluent from the subsurface outfalls contains concentrations of nitrogen and phosphorus that are up to three orders of magnitude greater than maximal ambient nutrient concentrations, and the buoyant effluent plumes also entrain deeper, nutrient enriched, sub-nutricline water as they rise to their equilibrium depth. These nutrient fluxes contribute significantly to total nutrient budgets in this coastal region (Howard et al. 2014), and therefore, may contribute to the growth of subsurface populations of Pseudo-nitzschia. This project combined multi-month glider deployments, mooring and pier phytoplankton community composition and temperature data, and remotely sensed satellite ocean color and temperature data, which allowed for the monitoring of conditions associated with the evolution of a Pseudo-nitzschia bloom from onset to demise. The moored environmental sample processors (ESPs) confirmed an offshore subsurface population of Pseudo-nitzschia and the glider data showed that upwelling moved the subsurface plankton communities into the surface waters, which resulted in a Pseudo-nitzschia bloom and demonstrated for the first time that upwelled subsurface phytoplankton populations can initiate HABs in the region.