Bivalve Feeding Responses to Microalgal Bloom Species in the Indian River Lagoon: the Potential for Top-Down Control

Abstract

In 2011, the Indian River Lagoon, a biodiverse estuary in eastern Florida (USA), experienced an intense microalgal bloom with disastrous ecological consequences. The bloom included a mix of microalgae with unresolved taxonomy and lasted for 7 months with a maximum concentration of 130 μg chlorophyll a L−1. In 2012, brown tide Aureoumbra lagunensis also bloomed in portions of this estuary, with reoccurrences in 2016 and 2018. To identify and understand the role of grazer pressure (top-down control) on bloom formation, we coupled DNA sequencing with bivalve feeding assays using three microalgae isolated from the 2011 bloom and maintained in culture. Feeding experiments were conducted on widely distributed bivalve species in the lagoon, including eastern oysters (Crassostrea virginica), hooked mussels (Ischadium recurvum), charru mussels (Mytella charruana), green mussels (Perna viridis), Atlantic rangia (Rangia cuneata), and hard clams (Mercenaria mercenaria), which were exposed to 3 × 104 cells mL−1 of five species of microalgae consisting of A. lagunensis and the three species clarified herein, the picocyanobacteria Crocosphaera sp. and ‘Synechococcus’ sp., and the picochlorophyte Picochlorum sp., as well as Nannochloropsis oculata used as a control. To ensure clearance rates were indicative of consumption and assimilation, the microalgae were isotopically (15N) labeled prior to feeding experiments. Clearance rates differed among bivalve and microalgal species, but enriched 15N values in bivalve tissue suggest that algal bloom species were assimilated by the bivalves. These results expand our understanding of the important ecosystem services that healthy, biodiverse filter feeder communities provide.

Bivalve Feeding on the Brown Tide Aureoumbra lagunensis in a Shallow Coastal Environment

“…The brown tide was immediately transported to the Smithsonian Marine Station at Fort Pierce (SMSFP) and kept in aerated buckets in the laboratory at 23 • C. Aureoumbra lagunensis cells were isotopically labeled by incubation with inorganic tracer compounds enriched in the heavy isotopes of C and N (98 atom percent [at%] 13 C or 15 N. These compounds (NaH 13 CO 3 [1.18 mM] and Na 15 NO 3 [0.117 mM]) were added directly into buckets holding A. lagunensis 24 h prior to the start of experiments following methods in Freeman et al (2013). We have shown previously that A. lagunensis assimilates Na 15 NO 3 (Galimany et al, 2020), but dual labels (both 13 C and 15 N) were still used for these experiments to ensure that A. lagunensis cells were adequately enriched in at least one isotope to allow for evidence of trophic transfer ( 13 C and/or 15 N enrichment in bivalve tissue).…”

“…One extra jar with an empty shell of each bivalve species at each algal concentration was left as a control. Bivalves were fed using a similar method described in Galimany et al (2020). Briefly, bivalves were fed 13 C-or 15 N-enriched A. lagunensis twice a day for four days: (1) early morning, each bivalve was transferred to a jar containing filtered estuarine water (26 ppt).…”

“…This altered feeding behavior may be a result of A. lagunensis cells producing exopolymer secretions that may affect the motility of cilia on the bivalves' gills (Liu and Buskey, 2000) or, simply, a physiological response to an excess of organic matter clogging their gills (Ward and Shumway, 2004). However, both bivalve species (M. mercenaria and C. virginica) fed on A. lagunensis (Gobler et al, 2013;Galimany et al, 2017bGalimany et al, , 2020, unlike other HABs, which generally cause bivalve closure and non-feeding (Shumway, 1990). Importantly, bivalves feed more efficiently on lower, pre-bloom densities of the brown tide, i.e., 10 4 cells mL −1 , and the hooked mussel (Ischadium recurvum) even increased its feeding on A. lagunensis over time when the density was sustained at pre-bloom conditions (Galimany et al, 2020).…”

“…However, both bivalve species (M. mercenaria and C. virginica) fed on A. lagunensis (Gobler et al, 2013;Galimany et al, 2017bGalimany et al, , 2020, unlike other HABs, which generally cause bivalve closure and non-feeding (Shumway, 1990). Importantly, bivalves feed more efficiently on lower, pre-bloom densities of the brown tide, i.e., 10 4 cells mL −1 , and the hooked mussel (Ischadium recurvum) even increased its feeding on A. lagunensis over time when the density was sustained at pre-bloom conditions (Galimany et al, 2020).…”

“…Bivalves provide important ecosystem services including water clarification through the removal of phytoplankton (Galimany et al, 2013(Galimany et al, , 2017bCranford, 2019). Previous studies in the IRL demonstrate that bivalves may remove A. lagunensis at low concentrations (Galimany et al, 2020) and some may even clear fully developed brown tides (Galimany et al, 2017b). However, there is a lack of information on the assimilation of this microalga by bivalves, including noncommercial species, to potentially ameliorate brown tides.…”