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.

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.

Extreme Runoff of Chemical Species of Nitrogen and Phosphorus Threatens a Florida Barrier Island Lagoon

Extreme runoff of stormwater to poorly flushed barrier island lagoons often adds excess nitrogen (N) and phosphorus (P) that can promote subsequent, sometimes intense, harmful algal blooms (HABs). Successful management of such estuaries requires special appreciation of when and how to control concentrations and fluxes of chemical species of N and P during high flow. Toward that end, monthly surveys and episodic rain-event sampling were carried out from December 2015 to March 2018 for two contrasting tributaries of the Indian River Lagoon (IRL), a barrier island lagoon in Florida. One tributary, South Prong Saint Sebastian River, flows through predominantly agricultural, forested and open land, whereas the second tributary, Crane Creek, traverses mainly residential-commercial land. Concentrations of some N and P species in these tributaries increased with increased flow and could be described with statistically significant equations for concentration versus flow rate, thereby supporting flow-rate-dependent flux determinations. Drainage basin yields (fluxes per square km) varied with land cover/use. Calculated annual yields of dissolved organic N (DON) and dissolved inorganic P (DIP) averaged ∼70% greater for South Prong Saint Sebastian River from high flow through thicker, more organic- and P-rich soils. In contrast, yields of nitrate + nitrite were 100% higher for Crane Creek from widespread application of N-fertilizer to thin layers of turfgrass overlying sand, plus runoff of N-rich reclaimed water. Two major weather events highlighted our study and foreshadow impacts from climate change. Seven months of drought from November 2016 to May 2017 were followed in September-October 2017 by excess rain, runoff and flooding from Hurricane Irma. Consequently, >50% of freshwater fluxes and ∼60% of N and P fluxes from South Prong Saint Sebastian River, Crane Creek and other IRL tributaries occurred during 2 months in 2017. Lagoon-wide inputs provided enough bioavailable N and P to help support a nanoeukaryotic bloom for >5 months, with chlorophyll a values >50 μg L–1. The bloom was co-dominated by the brown tide alga, Aureoumbra lagunensis, and an unidentified nanoeukaryotic green alga. Decreased salinity, low concentrations of dissolved inorganic N and P, and decreasing dissolved organic P (DOP), combined with biological factors, diminished the IRL bloom by mid-2018.

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.

Cyclical Patterns and a Regime Shift in the Character of Phytoplankton Blooms in a Restricted Sub-Tropical Lagoon, Indian River Lagoon, Florida, United States

This paper examines the character of phytoplankton blooms in a restricted sub-tropical lagoon along the Atlantic coast of central Florida. The results of the 23-year study (1997–2020) provide evidence for multiple types of variability in bloom activity, including cyclical patterns, stochastic events, and most prominently a regime shift in composition and intensity. Cyclical patterns (e.g., El Niño/La Niña periods) and stochastic events (e.g., tropical storms) influenced rainfall levels, which in turn impacted nutrient concentrations in the water column and the timing and intensity of blooms. In 2011, a major change occurred in the character of blooms, with a dramatic increase in peak biomass levels of blooms and the appearance of new dominant taxa, including the brown tide species Aureoumbra lagunensis and other nanoplanktonic species. Results of quantitative analyses reveal system behavior indicative of a regime shift. The shift coincided with widespread losses of seagrass community and reduced drift algae biomass. A combination of exceptionally low water temperatures in the winters of 2009/2010 and 2010/2011, hypersaline conditions associated with drought conditions, and high light attenuation caused by blooms appear to have contributed to the widespread and protracted decline in seagrass and drift macroalgal communities in the lagoon, leading to shifts in distribution of internal and external nutrient sources toward phytoplankton.

Metatranscriptome Library Preparation Influences Analyses of Viral Community Activity During a Brown Tide Bloom

There is growing interest in the use of metatranscriptomics to study virus community dynamics. We used RNA samples collected from harmful brown tides caused by the eukaryotic alga Aureococcus anophagefferens within New York (United States) estuaries and in the process observed how preprocessing of libraries by either selection for polyadenylation or reduction in ribosomal RNA (rRNA) influenced virus community analyses. As expected, more reads mapped to the A. anophagefferens genome in polyadenylation-selected libraries compared to the rRNA-reduced libraries, with reads mapped in each sample correlating to one another regardless of preprocessing of libraries. Yet, this trend was not seen for reads mapping to the Aureococcus anophagefferens Virus (AaV), where significantly more reads (approximately two orders of magnitude) were mapped to the AaV genome in the rRNA-reduced libraries. In the rRNA-reduced libraries, there was a strong and significant correlation between reads mappings to AaV and A. anophagefferens. Overall, polyadenylation-selected libraries produced fewer viral contigs, fewer reads mapped to viral contigs, and different proportions across viral realms and families, compared to their rRNA-reduced pairs. This study provides evidence that libraries generated by rRNA reduction and not selected for polyadenylation are more appropriate for quantitative characterization of viral communities in aquatic ecosystems by metatranscriptomics.

Transcriptomic Responses of Four Pelagophytes to Nutrient (N, P) and Light Stress

Pelagophytes are abundant picophytoplankton within open ocean ecosystems and the causative algae of harmful brown tide blooms in estuaries. The physiological capabilities facilitating the ecological success of pelagophytes in these diverse ecosystems remains poorly understood. Here, we investigated the transcriptional response of two coastal pelagophytes (Aureococcus anophagefferens and Aureoumbra lagunensis) and two open ocean pelagophytes (Pelagococcus subviridis and Pelagomonas calceolata) to conditions commonly found within the marine ecosystems where they thrive: low concentrations of nitrogen (N), phosphorus (P), or light. OrthoMCL was used to generate a total of 62,653 orthologous groups (OGs) with only a small fraction of these OGs (2,776 or 4.4%) being shared among all four pelagophytes. Of the commonly shared OGs, 8% were significantly differentially abundant under low N, P, or light with the majority associated with energy and lipid metabolism. Distinct responses among pelagophytes included increased abundance of transcripts encoding phosphate transporters (Aureococcus) and transcripts encoding a pyrophosphatase (Aureococcus and Pelagomonas) under low P, the expression of a suite of organic nitrogen-degrading enzymes under low N (Aureoumbra and Pelagomonas), increased abundance of transcripts encoding flavodoxins relative to ferredoxins (Pelagomonas) and transcripts encoding lysophospholipase (Pelagococcus) under low light, and both increases and decreases in abundance of transcripts encoding selenoproteins in all pelagophytes except Pelagococcus. Collectively, this study provides new information on the expressed gene compliment of these poorly characterized taxa and demonstrates that these pelagophytes possess a combination of shared and unique physiological features that likely facilitate their adaptation to distinct environmental conditions.

Laboratory Culture-Based Characterization of the Resting Stage Cells of the Brown-Tide-Causing Pelagophyte, Aureococcus anophagefferens

Life history (life cycle) plays a vital role in the ecology of some microalgae; however, the well-known brown-tide-causing pelagophyte Aureococcus anophagefferens has been barely investigated in this regard. Recently, based mainly on detections in marine sediments from China, we proved that this organism has a resting stage. We, therefore, conducted a follow-up study to characterize the resting stage cells (RSCs) of A. anophagefferens using the culture CCMP1984. The RSCs were spherical, larger than the vegetative cells, and smooth in cell surface and contained more aggregated plastid but more vacuolar space than vegetative cells. RSCs contained a conspicuous lipid-enriched red droplet. We found a 9.9-fold decrease in adenosine triphosphate (ATP) content from vegetative cells to RSCs, indicative of a "resting" or dormant physiological state. The RSCs stored for 3 months (at 4 °C in darkness) readily reverted back to vegetative growth within 20 days after being transferred to the conditions for routine culture maintenance. Our results indicate that the RSCs of A. anophagefferens are a dormant state that differs from vegetative cells morphologically and physiologically, and that RSCs likely enable the species to survive unfavorable conditions, seed annual blooms, and facilitate its cosmopolitan distribution that we recently documented.