High-resolution Spatiotemporal Dynamics of Harmful Algae in the Indian River Lagoon (Florida)-A Case Study of Aureoumbra lagunensis, Pyrodinium bahamense, and Pseudo-nitzschia.

Maria Célia Villac,Josée Nina Bouchard ,Shawna L. Landers,Edward J. Phlips,Douglas H. Adams,Leanne J. Flewelling ,Sugandha Shankar,Laura R. Markley,Susan Badylak,Stephanie Keller Abbe,Eric Muhlbach,Richard Paperno,Kyle B. Wald,Karen L. Henschen,Matthew Garrett,Ashley A. Parks,Jacob Schneider ,Colin P. Shea,Margaret A. Lasi,Lauren M. Hall,Cary B. Lopez,Dwayne D. Edwards,Autumn R. Biddle,Charles L. Tilney,Katherine A. Hubbard

doi:10.3389/fmars.2021.769877

Abstract

The Indian River Lagoon (IRL), located on the east coast of Florida, is a complex estuarine ecosystem that is negatively affected by recurring harmful algal blooms (HABs) from distinct taxonomic/functional groups. Enhanced monitoring was established to facilitate rapid quantification of three recurrent bloom taxa, Aureoumbra lagunensis, Pyrodinium bahamense, and Pseudo-nitzschia spp., and included corroborating techniques to improve the identification of small-celled nanoplankton (<10 μm in diameter). Identification and enumeration of these target taxa were conducted during 2015-2020 using a combination of light microscopy and species-specific approaches, specifically immunofluorescence flow cytometry as well as a newly developed qPCR assay for A. lagunensis presented here for the first time. An annual bloom index (ABI) was established for each taxon based on occurrence and abundance data. Blooms of A. lagunensis (>2×108 cells L-1) were observed in all six years sampled and across multiple seasons. In contrast, abundance of P. bahamense, largely driven by the annual temperature cycle that moderates life cycle transitions and growth, displayed a strong seasonal pattern with blooms (105-107 cells L-1) generally developing in early summer and subsiding in autumn. However, P. bahamense bloom development was delayed and abundance was significantly lower in years and locations with sustained A. lagunensis blooms. Pseudo-nitzschia spp. were broadly distributed with sporadic bloom concentrations (reaching 107 cells L-1), but with minimal concentrations of the toxin domoic acid detected (<0.02 μg L-1). In summer 2020, multiple monitoring tools characterized a novel nano-cyanobacterium bloom (reaching 109 cells L-1) that coincided with a decline in A. lagunensis and persisted into autumn. Statistical and time-series analyses of this spatiotemporally intensive dataset highlight prominent patterns in variability for some taxa, but also identifies challenges of characterizing mechanisms underlying more episodic yet persistent events. Nevertheless, the intersect of temperature and salinity as environmental proxies proved to be informative in delineating niche partitioning, not only in the case of taxa with long-standing data sets but also for seemingly unprecedented blooms of novel nanoplanktonic taxa.

Highlights

Harmful algal blooms (HABs) have occurred in the Indian River Lagoon (Florida, United States) for decades and can negatively affect water quality and ecosystem function and, in turn, hinder restoration efforts
A variety of sequencing was performed to confirm the identity of A. lagunensis in cultures and environmental DNA (eDNA) samples
Except for four ambiguously called bases, the 18S rRNA gene sequences derived from 2012, 2016, 2018, and 2020 IRL DNA samples were identical to the UTEX2796 isolate (1577 bp, except for 2012 which was only 903 bp, GenBank accession numbers MW812272-MW812281)

Summary

Introduction

Harmful algal blooms (HABs) have occurred in the Indian River Lagoon (Florida, United States) for decades and can negatively affect water quality and ecosystem function and, in turn, hinder restoration efforts. Recurring blooms of saxitoxin-producing Pyrodinium bahamense have caused regular shellfish harvest closures in the IRL system since the early 2000s (Anderson et al, 2021), and these blooms can reach high concentrations and often dominate summer algal biomass (Phlips et al, 2011). In the IRL in 2011, a still taxonomically unclassified small flagellate co-occurred with picocyanobacteria and exceeded 100 μg L−1 chlorophyll-a, which was higher than biomass levels typically observed during other blooms (SJRWMD, 2012). This “2011 superbloom” lasted 7 months and is thought to have contributed to the loss of over 40% of established seagrass beds in the area (SJRWMD, 2012; Lapointe et al, 2015; Phlips et al, 2015). Subsequent brown tide events were recorded throughout the system in 2013 and from 2016 through 2020, causing further seagrass losses, extensive fish kills in 2016, and negative effects on seagrass-dependent fisheries and wildlife (Morris et al, 2018; Lapointe et al, 2020)

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Conclusion