Distinct responses to warming within picoplankton communities across an environmental gradient.

Picophytoplankton are a ubiquitous component of marine plankton communities and are expected to be favored by global increases in seawater temperature and stratification associated with climate change. Eukaryotic and prokaryotic picophytoplankton have distinct ecology, and global models predict that the two groups will respond differently to future climate scenarios. At a nearshore observatory on the Northeast US Shelf, however, decades of year-round monitoring have shown these two groups to be highly synchronized in their responses to environmental variability. To reconcile the differences between regional and global predictions for picophytoplankton dynamics, we here investigate the picophytoplankton community across the continental shelf gradient from the nearshore observatory to the continental slope. We analyze flow cytometry data from 22 research cruises, comparing the response of picoeukaryote and Synechococcus communities to environmental variability across time and space. We find that the mechanisms controlling picophytoplankton abundance differ across taxa, season, and distance from shore. Like the prokaryote, Synechococcus, picoeukaryote division rates are limited nearshore by low temperatures in winter and spring, and higher temperatures offshore lead to an earlier spring bloom. Unlike Synechococcus, picoeukaryote concentration in summer decreases dramatically in offshore surface waters and exhibits deeper subsurface maxima. The offshore picoeukaryote community appears to be nutrient limited in the summer and subject to much greater loss rates than Synechococcus. This work both produces and demonstrates the necessity of taxon- and site-specific knowledge for accurately predicting the responses of picophytoplankton to ongoing environmental change.

Seasons of Syn.

Synechococcus is a widespread and important marine primary producer. Time series provide critical information for identifying and understanding the factors that determine abundance patterns. Here, we present the results of analysis of a 16-yr hourly time series of Synechococcus at the Martha's Vineyard Coastal Observatory, obtained with an automated, in situ flow cytometer. We focus on understanding seasonal abundance patterns by examining relationships between cell division rate, loss rate, cellular properties (e.g., cell volume, phycoerythrin fluorescence), and environmental variables (e.g., temperature, light). We find that the drivers of cell division vary with season; cells are temperature-limited in winter and spring, but light-limited in the fall. Losses to the population also vary with season. Our results lead to testable hypotheses about Synechococcus ecophysiology and a working framework for understanding the seasonal controls of Synechococcus cell abundance in a temperate coastal system.

Dynamics and functional diversity of the smallest phytoplankton on the Northeast US Shelf.

Picophytoplankton are the most abundant primary producers in the ocean. Knowledge of their community dynamics is key to understanding their role in marine food webs and global biogeochemical cycles. To this end, we analyzed a 16-y time series of observations of a phytoplankton community at a nearshore site on the Northeast US Shelf. We used a size-structured population model to estimate in situ division rates for the picoeukaryote assemblage and compared the dynamics with those of the picocyanobacteria Synechococcus at the same location. We found that the picoeukaryotes divide at roughly twice the rate of the more abundant Synechococcus and are subject to greater loss rates (likely from viral lysis and zooplankton grazing). We describe the dynamics of these groups across short and long timescales and conclude that, despite their taxonomic differences, their populations respond similarly to changes in the biotic and abiotic environment. Both groups appear to be temperature limited in the spring and light limited in the fall and to experience greater mortality during the day than at night. Compared with Synechococcus, the picoeukaryotes are subject to greater top-down control and contribute more to the region's primary productivity than their standing stocks suggest.

Physiological and ecological drivers of early spring blooms of a coastal phytoplankter.

Climate affects the timing and magnitude of phytoplankton blooms that fuel marine food webs and influence global biogeochemical cycles. Changes in bloom timing have been detected in some cases, but the underlying mechanisms remain elusive, contributing to uncertainty in long-term predictions of climate change impacts. Here we describe a 13-year hourly time series from the New England shelf of data on the coastal phytoplankter Synechococcus, during which the timing of its spring bloom varied by 4 weeks. We show that multiyear trends are due to temperature-induced changes in cell division rate, with earlier blooms driven by warmer spring water temperatures. Synechococcus loss rates shift in tandem with division rates, suggesting a balance between growth and loss that has persisted despite phenological shifts and environmental change.

Rapid growth and concerted sexual transitions by a bloom of the harmful dinoflagellate Alexandrium fundyense (Dinophyceae).

Transitions between life cycle stages by the harmful dinoflagellate Alexandrium fundyense are critical for the initiation and termination of its blooms. To quantify these transitions in a single population, an Imaging FlowCytobot (IFCB), was deployed in Salt Pond (Eastham, Massachusetts), a small, tidally flushed kettle pond that hosts near annual, localized A. fundyense blooms. Machine-based image classifiers differentiating A. fundyense life cycle stages were developed and results were compared to manually corrected IFCB samples, manual microscopy-based estimates of A. fundyense abundance, previously published data describing prevalence of the parasite Amoebophrya, and a continuous culture of A. fundyense infected with Amoebophrya. In Salt Pond, a development phase of sustained vegetative division lasted approximately 3 weeks and was followed by a rapid and near complete conversion to small, gamete cells. The gametic period (∼3 d) coincided with a spike in the frequency of fusing gametes (up to 5% of A. fundyense images) and was followed by a zygotic phase (∼4 d) during which cell sizes returned to their normal range but cell division and diel vertical migration ceased. Cell division during bloom development was strongly phased, enabling estimation of daily rates of division, which were more than twice those predicted from batch cultures grown at similar temperatures in replete medium. Data from the Salt Pond deployment provide the first continuous record of an A. fundyense population through its complete bloom cycle and demonstrate growth and sexual induction rates much higher than are typically observed in culture.

Diel size distributions reveal seasonal growth dynamics of a coastal phytoplankter.

Phytoplankton account for roughly half of global primary production; it is vital that we understand the processes that control their abundance. A key process is cell division. We have, however, been unable to estimate division rate in natural populations at the appropriate timescale (hours to days) for extended periods of time (months to years). For phytoplankton, the diel change in cell size distribution is related to division rate, which offers an avenue to obtain estimates from in situ observations. We show that a matrix population model, fit to hourly cell size distributions, accurately estimates division rates of both cultured and natural populations of Synechococcus. Application of the model to Synechococcus at the Martha's Vineyard Coastal Observatory provides an unprecedented view that reveals a distinct seasonality in division rates. This information allows us to separate the effects of growth and loss quantitatively over an entire seasonal cycle. We find that division and loss processes are tightly coupled throughout the year. The large seasonal changes in cell abundance are the result of periods of time (weeks to months) when there are small systematic differences that favor either net growth or loss. We also find that temperature plays a critical role in limiting division rate during the annual spring bloom. This approach opens a path to quantify the role of Synechococcus in ecological and biogeochemical processes in natural systems.