Mesozooplankton Community Dynamics and Grazing Potential Across Algal Bloom Cycles in a Subtropical Estuary

Mesozooplankton, as abundant grazers of microalgae in coastal systems, have the potential to prevent or mitigate harmful algal blooms (HABs) and their effects. The Indian River Lagoon (IRL) is a subtropical estuary in eastern Florida (United States) where repeated blooms, dominated by the toxic dinoflagellate Pyrodinium bahamense, the brown tide species Aureoumbra lagunensis, pico/nano planktonic cyanobacteria and other nano-eukaryotes, have highlighted the need to better understand fluctuations in the grazing potential of mesozooplankton populations across bloom cycles. Mesozooplankton and abiotic environmental data were collected at five sites in the northern IRL system at 6-week intervals from November 2013 through June 2016. A total of 107 taxa from 14 phyla were detected. Communities varied across sites, dates and between bloom and non-bloom periods, with densities up to 338 individuals L–1. Eight taxa comprising 85–94% of the total population at each site were identified as primary potential grazers, including barnacle nauplii, cladocerans, adult copepods, gastropod veligers, larvaceans, and polychaete metatrochophores. Although abundant, the estimated grazing potential of the primary taxa, calculated from their measured densities and previously published grazing rates, suggest that mesozooplankton lack the capacity to suppress phytoplankton once they reach bloom levels. These findings illustrate the utility of monitoring data and underscore the importance of systematically evaluating algal bloom controls with a consideration for the dynamic conditions of each unique ecosystem.

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

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 6 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 identify 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.

Biological Abundance and Diversity in Organic-Rich Sediments From a Florida Barrier Island Lagoon

Organic-rich sediments in estuaries and the coastal ocean are often a product of land clearing, runoff of excess nutrients and other human activities. They can harbor pollutants, oxygen-consuming microbes and toxic hydrogen sulfide (H2S), thereby creating a hostile environment for infauna. In one barrier island lagoon, the Indian River Lagoon (IRL), Florida, layers of organic-rich sediments have increased substantially in thickness and areal extent over the past 60 years. Geochemical properties of these muddy sediments have been described; however, less is known about their habitability. We analyzed infauna and geochemical properties of 102 samples taken during wet and dry seasons at 17 locations spanning 60 km of the lagoon. We quantified infaunal abundance and diversity (Shannon-Wiener, H′) and determined Pearson’s correlation coefficients for effective number of species (ENS = eH′) vs. sediment porosity (ϕ = 0.69–0.95), organic carbon (1–8%), nitrogen (0.1–0.7%), silt + clay (16–99%), porewater H2S (5–3,600 μM), and other environmental variables. Small bivalves accounted for 70% of the organisms collected, followed by gastropods, polychaetes and other biota. The bivalves were predominantly Macoma spp., Mulinia lateralis and Parastarte triquetra with average abundances of 3,896, 2,049, and 926 individuals per m2, respectively. High abundance of some species, such as Macoma, showed that these opportunists had adapted to poor quality sediments. More than two-thirds of the 35 species collected were present at <100 individuals per m2 of sediment. Cluster analysis identified four groups of stations with significantly different geochemical properties. Permutation analyses of variance indicated that the four groups also represented statistically different infaunal communities. Diversity decreased with increasing sediment concentrations of organic carbon, nitrogen and silt + clay; however, community richness at our most prolific station along the perimeter of muddy deposits was ∼7 times lower than found previously in sandy sediments from the IRL. The results identified areas where infaunal communities have experienced the greatest stress due to accumulation of organic-rich sediments. Results from this study help support management plans for remediation of organic-rich mud and improvement of sediment and water quality, especially in areas identified with low ENS.

Restored Coastal Habitat Can “Reel In” Juvenile Sportfish: Population and Community Responses in the Indian River Lagoon, Florida, USA

Coastal habitats are declining worldwide, which has impacted economically important fisheries, especially in the Indian River Lagoon, Florida. As a result, extensive intertidal oyster reef and living shoreline restoration projects have been implemented. Restoration can also theoretically benefit predator populations, but this relationship is understudied. Here, the impact of habitat restoration on juvenile predatory fish (i.e., sportfish) populations (abundance) and communities (species richness, diversity, and assemblage) was assessed prior to and following oyster reef restoration and living shoreline stabilization for up to three years, and incorporated the influence of 17 environmental predictor variables. Juvenile sportfish abundance and richness (n = 11) were variable over time but collectively higher on restored oyster reefs compared to controls, and similar between control and stabilized shorelines. Sportfish abundance was best described by a combination of biotic features of the site (e.g., reef height and benthic substrate cover), prey abundance, decreasing distance to the nearest ocean inlet and dissolved oxygen. Results suggest future restoration site selection should emphasize adequate dissolved oxygen (~6 mg/L), oyster densities above 50/m2 and reef height above 55 mm, and minimum shoreline vegetation coverage of 50% to support macrofaunal prey and subsequently attract sportfish. These findings can help natural resource managers better use habitat restoration as a tool for enhancing fish populations in the future.

Neodymium Isotope Geochemistry of a Subterranean Estuary

Rare earth elements (REE) and Nd isotope compositions of surface and groundwaters from the Indian River Lagoon in Florida were measured to investigate the influence of submarine groundwater discharge (SGD) on these parameters in coastal waters. The Nd flux of the terrestrial component of SGD is around 0.7±0.03 μmol Nd/day per m of shoreline across the nearshore seepage face of the subterranean estuary. This translates to a terrestrial SGD Nd flux of 4±0.2 mmol/day for the entire 5,880 m long shoreline of the studied portion of the lagoon. The Nd flux from bioirrigation across the nearshore seepage face is 1±0.05 μmol Nd/day per m of shoreline, or 6±0.3 mmol/day for the entire shoreline. The combination of these two SGD fluxes is the same as the local, effective river water flux of Nd to the lagoon of 12.7±5.3 mmol/day. Using a similar approach, the marine-sourced SGD flux of Nd is 31.4±1.6 μmol Nd/day per m of shoreline, or 184±9.2 mmol/day for the investigated portion of the lagoon, which is 45 times higher than the terrestrial SGD Nd flux. Terrestrial-sourced SGD has an εNd(0) value of −5±0.42, which is similar to carbonate rocks (i.e., Ocala Limestone) from the Upper Floridan Aquifer (−5.6), but more radiogenic than the recirculated marine SGD, for which εNd(0) is −7±0.24. Marine SGD has a Nd isotope composition that is identical to the εNd(0) of Fe(III) oxide/oxyhydroxide coated sands of the surficial aquifer (−7.15±0.24 and −6.98±0.36). These secondary Fe(III) oxides/oxyhydroxides formed during subaerial weathering when sea level was substantially lower during the last glacial maximum. Subsequent flooding of these surficial sands by rising sea level followed by reductive dissolution of the Fe(III) oxide/oxyhydroxide coatings can explain the Nd isotope composition of the marine SGD component. Surficial waters of the Indian River Lagoon have an εNd(0) of −6.47±0.32, and are a mixture of terrestrial and marine SGD components, as well as the local rivers (−8.63 and −8.14). Nonetheless, the chief Nd source is marine SGD that has reacted with Fe(III) oxide/oxyhydroxide coatings on the surficial aquifer sands of the subterranean estuary.

High Densities of a Prochlorophyte (Unresolved Species) Inhibit Grazing by the Herbivorous Copepod Parvocalanus crassirostris

Harmful algal blooms (HABs) are increasing in frequency and severity, underscoring the importance of understanding potential top-down controls of blooms. In the Indian River Lagoon (IRL), a shallow subtropical estuary, one harmful bloom was co-dominated by an unresolved prochlorophyte in the Family Prochlorothricaceae, which reached densities of > 106 cells ml–1 engendering the term “Superbloom.” Experiments were conducted to evaluate grazing rates and the potential for top-down control by an abundant herbivorous copepod, Parvocalanus crassirostris, on the prochlorophyte. Those grazing rates were lower than the rates on a palatable alternative algal food, Isochrysis galbana, when both algal species were presented in monocultures with identical densities. Grazing on the prochlorophyte decreased or ceased at densities over 4.8 × 105 cells ml–1. When the prochlorophyte and the palatable alternative each comprised half of the total density, both species were consumed, but grazing on I. galbana was reduced compared to the grazing rates in a monoculture of this species, especially at higher cell densities. Copepod mortality was observed in treatments with high concentrations of the prochlorophyte, and these treatments contained mucilage. Experiments simulating viscosities produced by prochlorophyte mucilage yielded results consistent with the original grazing experiments (i.e., copepods showed lower grazing rates and higher mortality rates in higher viscosity treatments). Results reveal potential limitations of top-down controls by this grazer on prochlorophyte blooms and HABs that produce mucilage.

Soft-Sediment Communities of the Northern Indian River Lagoon, FL, United States

Understanding the structure and function of infaunal communities is useful in determining the biodiversity and ecosystem function of shallow estuaries. We conducted a survey of infaunal communities within three separate water basins [Mosquito Lagoon (ML), Indian River (IR), and Banana River (BR)] in the larger Northern Indian River Lagoon, FL, United States to establish a database of infaunal community structure and function. Twenty-seven sites were sampled quarterly from 2014 to 2016. Analysis of all samples determined that basin, season, and sediment composition were the primary drivers of macrobenthic community composition. Diversity was highest in the ML, and lower in spring compared to other seasons. The occurrence of a brown tide (Aureoumbra lagunensis) in 2016 allowed a comparison of winter and spring communities before (2015) and during (2016) a bloom event. Community composition and diversity at the BR sites were the most affected by the bloom event with the lowest diversity and abundances during the bloom. Diversity in the IR was also lower during the bloom, while the ML was unaffected by the bloom. Species of all feeding groups were affected by the bloom, with lower abundances found in all groups. In addition, to determine the overall trophic diversity of infaunal communities, we collected infaunal organisms from two of the quarterly sampled sites for isotope analyses. Values of δ13C and δ15N from infaunal tissue were compared to those of potential food sources at each site. Substantial interspecific variation in isotope values of infaunal organisms within a site suggests the presence of diverse nutritional modes that include suspension and deposit feeding and predation. Together, these data suggest that infaunal communities contribute to benthic pelagic coupling and nutrient cycling within the estuarine communities, but the overall function of these communities may be tightly linked to their species composition.

Genomics-Based Phylogenetic and Population Genetic Analysis of Global Samples Confirms Halophila johnsonii Eiseman as Halophila ovalis (R.Br.) Hook.f.

Halophila johnsonii is an endangered seagrass species that is restricted to the southeast coast of Florida, United States. Its taxonomic status has been called into question, in particular, given the close morphological and genetic similarity of H. johnsonii and the widely distributed and morphologically variable Halophila ovalis, which is largely restricted to the Indo-Pacific region. While a close relationship to H. ovalis is uncontroversial, it remains uncertain whether H. johnsonii represents a distinct lineage or is a recent introduction to the Florida region. Given the conservation status of H. johnsonii, distinguishing these alternatives has important implications for the management of the species and its habitat. Here, we develop molecular data sets for samples of H. johnsonii and H. ovalis including DNA sequences, genome-wide SNPs and microsatellites with the view to resolving the affinities of H. johnsonii with respect to the wider H. ovalis complex. Phylogenetic hypotheses based upon plastid (∼18000 bp) and low copy nuclear DNA (∼6500 bp) sequences derived from hybrid capture, along with 990 genome-wide ddRAD SNPs consistently resolved H. johnsonii within H. ovalis. Specifically, we found a close affinity between H. johnsonii and H. ovalis sampled from the east coast of Africa. In addition, Halophila specimens collected in Antigua, which are within the range of morphological variation typical for H. ovalis, are virtually identical to H. johnsonii and the East African H. ovalis samples based upon DNA sequence analyses and these group together using Bayesian clustering analyses of microsatellites and ddRAD SNPs. We conducted population genetic analyses using large number of H. johnsonii samples collected over a 17-year period. Genotypic data generated through microsatellites and ddRAD SNPs revealed genetic uniformity for all 132 H. johnsonii samples across the Indian River Lagoon, Florida, while samples of H. ovalis from Antigua shared the same genotype as H. johnsonii. We conclude that the lack of genetic diversity and the absence of sexual reproduction strongly indicates that the total range of H. johnsonii is actually one clone that is closely related to populations in Africa and Antigua and may be derived from a recent introduction from one of those regions.

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

Brown tides formed by Aureoumbra lagunensis decrease light penetration in the water column and are often followed by hypoxic events that result in the loss of fish and shellfish. To understand the ability of bivalve filter feeders to control and prevent A. lagunensis blooms, we exposed eastern oysters (Crassostrea virginica), hooked mussels (Ischadium recurvum), and hard clams (Mercenaria mercenaria) to a naturally co-occurring brown tide in the Indian River Lagoon (IRL), Florida, United States. Bivalves were exposed in the laboratory to multiple concentrations (104 to 106 cells mL–1) of isotopically labeled (13C and 15N) A. lagunensis cells. The standard clearance rate (herein clearance rate) of each bivalve species was calculated using flow cytometry to quantify A. lagunensis cell removal. The highest clearance rates were at 104 cells mL–1, but values varied across bivalve species (2.16 ± 0.30, 3.03 ± 0.58, and 0.41 ± 0.12 L h–1 for C. virginica, I. recurvum, and M. mercenaria, respectively). Although clearance rates decreased with increasing bloom concentrations, bivalves were still consuming algal cells at all concentrations and were retaining and assimilating more cells at the highest concentrations, as revealed by δ13C and δ15N values. We highlight interspecific differences among bivalve species in the removal of A. lagunensis, supporting the importance of healthy and diverse filter feeding communities in estuaries, especially as threats of brown tides and other HABs are increasing in the Anthropocene.