Dinoflagellate vertical migration fuels an intense red tide.

Harmful algal blooms (HABs) are increasing globally, causing economic, human health, and ecosystem harm. In spite of the frequent occurrence of HABs, the mechanisms responsible for their exceptionally high biomass remain imperfectly understood. A 50-y-old hypothesis posits that some dense blooms derive from dinoflagellate motility: organisms swim upward during the day to photosynthesize and downward at night to access deep nutrients. This allows dinoflagellates to outgrow their nonmotile competitors. We tested this hypothesis with in situ data from an autonomous, ocean-wave-powered vertical profiling system. We showed that the dinoflagellate Lingulodinium polyedra's vertical migration led to depletion of deep nitrate during a 2020 red tide HAB event. Downward migration began at dusk, with the maximum migration depth determined by local nitrate concentrations. Losses of nitrate at depth were balanced by proportional increases in phytoplankton chlorophyll concentrations and suspended particle load, conclusively linking vertical migration to the access and assimilation of deep nitrate in the ocean environment. Vertical migration during the red tide created anomalous biogeochemical conditions compared to 70 y of climatological data, demonstrating the capacity of these events to temporarily reshape the coastal ocean's ecosystem and biogeochemistry. Advances in the understanding of the physiological, behavioral, and metabolic dynamics of HAB-forming organisms from cutting-edge observational techniques will improve our ability to forecast HABs and mitigate their consequences in the future.

Timing is everything: Drivers of interannual variability in blue whale migration.

Blue whales need to time their migration from their breeding grounds to their feeding grounds to avoid missing peak prey abundances, but the cues they use for this are unknown. We examine migration timing (inferred from the local onset and cessation of blue whale calls recorded on seafloor-mounted hydrophones), environmental conditions (e.g., sea surface temperature anomalies and chlorophyll a), and prey (spring krill biomass from annual net tow surveys) during a 10 year period (2008-2017) in waters of the Southern California Region where blue whales feed in the summer. Colder sea surface temperature anomalies the previous season were correlated with greater krill biomass the following year, and earlier arrival by blue whales. Our results demonstrate a plastic response of blue whales to interannual variability and the importance of krill as a driving force behind migration timing. A decadal-scale increase in temperature due to climate change has led to blue whales extending their overall time in Southern California. By the end of our 10-year study, whales were arriving at the feeding grounds more than one month earlier, while their departure date did not change. Conservation strategies will need to account for increased anthropogenic threats resulting from longer times at the feeding grounds.

A view of physical mechanisms for transporting harmful algal blooms to Massachusetts Bay.

Physical dynamics of Harmful Algal Blooms in Massachusetts Bay in May 2005 and 2008 were examined by the simulated results. Reverse particle-tracking experiments suggest that the toxic phytoplankton mainly originated from the Bay of Fundy in 2005 and the western Maine coastal region and its local rivers in 2008. Mechanism studies suggest that the phytoplankton were advected by the Gulf of Maine Coastal Current (GMCC). In 2005, Nor'easters increased the cross-shelf surface elevation gradient over the northwestern shelf. This intensified the Eastern and Western MCC to form a strong along-shelf current from the Bay of Fundy to Massachusetts Bay. In 2008, both Eastern and Western MCC were established with a partial separation around Penobscot Bay before the outbreak of the bloom. The northeastward winds were too weak to cancel or reverse the cross-shelf sea surface gradient, so that the Western MCC carried the algae along the slope into Massachusetts Bay.

Effects of warming and eutrophication on coastal phytoplankton production.

Phytoplankton production in coastal waters influences seafood production and human health and can lead to harmful algal blooms. Water temperature and eutrophication are critical factors affecting phytoplankton production, although the combined effects of warming and nutrient changes on phytoplankton production in coastal waters are not well understood. To address this, phytoplankton production changes in natural waters were investigated using samples collected over eight months, and under 64 different initial conditions, established by combining four different water temperatures (i.e., ambient T, +2, +4, and + 6 °C), and two different nutrient conditions (i.e., non-enriched and enriched). Under the non-enriched conditions, the effect of warming on phytoplankton production was significantly positive in some months, significantly negative in others, or had no effect. However, under enriched conditions, warming affected phytoplankton production positively in all months except one, when the salinity was as low as 6.5. These results suggest that nutrient conditions can alter the effects of warming on phytoplankton production. Of several parameters, the ratio of initial nitrate concentration to chlorophyll a concentration [NCCA, µM (µg L-1)-1] was one of the most critical factors determining the directionality of the warming effects. In laboratory experiments, when NCCA in the ambient or nutrient-enriched waters was ≥1.2, warming increased or did not change phytoplankton production with one exception; however, when NCCA was <1.2, warming did not change or decreased production. In the time series data obtained from the coastal waters of four target countries, when NCCA was 1.5 or more, warming increased phytoplankton production, whereas when NCCA was lower than 1.5, warming lowered phytoplankton production, Thus, it is suggested that NCCA could be used as an index for predicting future phytoplankton production changes in coastal waters.

The role of submesoscale currents in structuring marine ecosystems.

From microbes to large predators, there is increasing evidence that marine life is shaped by short-lived submesoscales currents that are difficult to observe, model, and explain theoretically. Whether and how these intense three-dimensional currents structure the productivity and diversity of marine ecosystems is a subject of active debate. Our synthesis of observations and models suggests that the shallow penetration of submesoscale vertical currents might limit their impact on productivity, though ecological interactions at the submesoscale may be important in structuring oceanic biodiversity.

A swarm of autonomous miniature underwater robot drifters for exploring submesoscale ocean dynamics.

Measuring the ever-changing 3-dimensional (3D) motions of the ocean requires simultaneous sampling at multiple locations. In particular, sampling the complex, nonlinear dynamics associated with submesoscales (<1-10 km) requires new technologies and approaches. Here we introduce the Mini-Autonomous Underwater Explorer (M-AUE), deployed as a swarm of 16 independent vehicles whose 3D trajectories are measured near-continuously, underwater. As the vehicles drift with the ambient flow or execute preprogrammed vertical behaviours, the simultaneous measurements at multiple, known locations resolve the details of the flow within the swarm. We describe the design, construction, control and underwater navigation of the M-AUE. A field programme in the coastal ocean using a swarm of these robots programmed with a depth-holding behaviour provides a unique test of a physical-biological interaction leading to plankton patch formation in internal waves. The performance of the M-AUE vehicles illustrates their novel capability for measuring submesoscale dynamics.

California coastal upwelling onset variability: cross-shore and bottom-up propagation in the planktonic ecosystem.

The variability of the California Current System (CCS) is primarily driven by variability in regional wind forcing. In particular, the timing of the spring transition, i.e., the onset of upwelling-favorable winds, varies considerably in the CCS with changes in the North Pacific Gyre Oscillation. Using a coupled physical-biogeochemical model, this study examines the sensitivity of the ecosystem functioning in the CCS to a lead or lag in the spring transition. An early spring transition results in an increased vertical nutrient flux at the coast, with the largest ecosystem consequences, both in relative amplitude and persistence, hundreds of kilometers offshore and at the highest trophic level of the modeled food web. A budget analysis reveals that the propagation of the perturbation offshore and up the food web is driven by remineralization and grazing/predation involving both large and small plankton species.

Climatic control of upwelling variability along the western North-American coast.

The high biological production of the California Current System (CCS) results from the seasonal development of equatorward alongshore winds that drive coastal upwelling. While several climatic fluctuation patterns influence the dynamics and biological productivity of the CCS, including the El Niño-Southern Oscillation (ENSO), the Pacific Decadal Oscillation index (PDO) and the North Pacific Gyre Oscillation (NPGO), the mechanisms of interaction between climatic oscillations and the CCS upwelling dynamics have remained obscure. Here, we use Singular Spectral Analysis (SSA) to reveal, for the first time, low-frequency concordance between the time series of climatic indices and upwelling intensity along the coast of western North America. Based on energy distributions in annual, semiannual and low-frequency signals, we can divide the coast into three distinct regions. While the annual upwelling signal dominates the energy spectrum elsewhere, low-frequency variability is maximal in the regions south of 33°N. Non-structured variability associated with storms and turbulent mixing is enhanced at northerly locations. We found that the low-frequency signal is significantly correlated with different climatic indices such as PDO, NPGO and ENSO with the correlation patterns being latitude-dependent. We also analyzed the correlations between this upwelling variability and sea surface temperature (SST) and sea level pressure (SLP) throughout the North Pacific to visualize and interpret the large-scale teleconnection dynamics in the atmosphere that drive the low-frequency coastal winds. These results provide new insights into the underlying mechanisms connecting climatic patterns with upwelling dynamics, which could enhance our prediction and forecast capabilities of the effects of future oceanographic and climatic variability in the CCS.

Size-structured planktonic ecosystems: constraints, controls and assembly instructions.

Here we present a nutrient-phytoplankton-zooplankton (NPZ) model that has arbitrary size-resolution within the phytoplankton- and zooplankton-state variables. The model assumes allometric scaling of biological parameters. This particular version of the model (herbivorous zooplankton only) has analytical solutions that allow efficient exploration of the effects of allometric dependencies of various biological processes on the model's equilibrium solutions. The model shows that there are constraints on the possible combinations of allometric scalings of the biological rates that will allow ecosystems to be structured as we observe (larger organisms added as the total biomass increases). The diversity (number of size classes occupied) of the ecosystem is the result of simultaneous bottom-up and top-down control: resources determine which classes can exist; predation determines which classes do exist. Thus, the simultaneous actions of bottom-up and top-down controls are essential for maintaining and structuring planktonic ecosystems. One important conclusion from this model is that there are multiple, independent ways of obtaining any given biomass spectrum, and that the spectral slope is not, in and of itself, very informative concerning the underlying dynamics. There is a clear need for improved size-resolved field measurements of biological rates; these will both elucidate biological processes in the field, and allow strong testing of size-structured models of planktonic ecosystems.

Cultivation and ecosystem role of a marine roseobacter clade-affiliated cluster bacterium.

Isolation and cultivation are a crucial step in elucidating the physiology, biogeochemistry, and ecosystem role of microorganisms. Many abundant marine bacteria, including the widespread Roseobacter clade-affiliated (RCA) cluster group, have not been cultured with traditional methods. Using novel techniques of cocultivation with algal cultures, we have accomplished successful isolation and propagation of a strain of the RCA cluster. Our experiments revealed that, in addition to growing on alga-excreted organic matter, additions of washed bacterial cells led to significant biomass decrease of dinoflagellate cultures as measured by in vivo fluorescence. Bacterial filtrate did not adversely affect the algal cultures, suggesting attachment-mediated activity. Using an RCA cluster-specific rRNA probe, we documented increasing attachment of these algicidal bacteria during a dinoflagellate bloom, with a maximum of 70% of the algal cells colonized just prior to bloom termination. Cross-correlation analyses between algal abundances and RCA bacterial colonization were statistically significant, in agreement with predator-prey models suggesting that RCA cluster bacteria caused algal bloom decline. Further investigation of molecular databases revealed that RCA cluster bacteria were numerically abundant during algal blooms sampled worldwide. Our findings suggest that the widespread RCA cluster bacteria may exert significant control over phytoplankton biomass and community structure in the oceans. We also suggest that coculture with phytoplankton may be a useful strategy to isolate and successfully grow previously uncultured but ecologically abundant marine heterotrophs.

BACTERIA-INDUCED MOTILITY REDUCTION IN LINGULODINIUM POLYEDRUM (DINOPHYCEAE)(1).

Biotic factors that affect phytoplankton physiology and behavior are not well characterized but probably play a crucial role in regulating their population dynamics in nature. We document evidence that some marine bacteria can decrease the swimming speed of motile phytoplankton through the release of putative protease(s). Using the dinoflagellate Lingulodinium polyedrum (F. Stein) J. D. Dodge as a model system, we showed that the motility-reducing components of bacterial-algal cocultures were mostly heat labile, were of high molecular weight (>50 kDa), and could be partially neutralized by incubations with protease inhibitors. We further showed that additions of the purified protease pronase E decreased dinoflagellate swimming speed in a concentration-dependent manner. We propose that motility can be used as a marker for dinoflagellate stress or general unhealthy status due to proteolytic bacteria, among other factors.

Swimming against the flow: a mechanism of zooplankton aggregation.

Zooplankton reside in a constantly flowing environment. However, information about their response to ambient flow has remained elusive, because of the difficulties of following the individual motions of these minute, nearly transparent animals in the ocean. Using a three-dimensional acoustic imaging system, we tracked >375,000 zooplankters at two coastal sites in the Red Sea. Resolution of their motion from that of the water showed that the animals effectively maintained their depth by swimming against upwelling and downwelling currents moving at rates of up to tens of body lengths per second, causing their accumulation at frontal zones. This mechanism explains how oceanic fronts become major feeding grounds for predators and targets for fishermen.