Mesoscale oceanographic meanders influence protist community function and structure in the southern Indian Ocean.

The interface between the nutrient-rich Southern Ocean and oligotrophic Indian Ocean creates unique environmental conditions that can strongly influence biological processes. We investigated protist communities across a mesoscale meander of the Subtropical Front within the Southern Indian Ocean. 18S V9 rDNA metabarcoding suggests a diverse protist community in which the dinoflagellates and parasitic Syndiniales were abundant. Diversity was highest in frontal waters of the mesoscale meander, with differences in community structure inside and outside the meander. While the overall community was dominated by mixotrophic taxa, the frontal boundary of the meander had increased abundances of heterotrophic taxa, with potential implications for net atmospheric CO2 drawdown. Pulse amplitude modulated (PAM) fluorimetry revealed significant differences in the photophysiology of phytoplankton communities inside and outside the meander. By using single-cell PAM microscopy, we identified physiological differences between dinoflagellate and coccolithophore taxa, which may have contributed to changes in photophysiology observed at community level. Overall, our results demonstrate that frontal areas have a strong impact on the composition of protist communities in the Southern Ocean with important implications for understanding biological processes in this region.

Osmotrophy of dissolved organic compounds by coccolithophore populations: Fixation into particulate organic and inorganic carbon.

Coccolithophores are typically thought of as photoautotrophs, yet a few genera inhabit sub-euphotic environments with insufficient light for photosynthesis, suggesting that other carbon acquisition strategies are likely. Field experiments were performed in the northwest Atlantic (a region with potentially abundant coccolithophores). Phytoplankton populations were incubated with 14C-labeled dissolved organic carbon (DOC) compounds, acetate, mannitol, and glycerol. Coccolithophores were sorted from these populations 24 hours later using flow cytometry, and DOC uptake was measured. DOC uptake rates were as high as 10-15 moles cell-1 day-1, slow relative to photosynthesis rates (10-12 moles cell-1 day-1). Growth rates on the organic compounds were low, suggesting that osmotrophy plays more of a survival strategy in low-light situations. Assimilated DOC was found in both particulate organic carbon and calcite coccoliths (particulate inorganic carbon), suggesting that osmotrophic uptake of DOC into coccolithophore calcite is a small but notable part of the biological carbon pump and alkalinity pump paradigms.

The influence of particle concentration and bulk characteristics on polarized oceanographic lidar measurements.

Oceanographic lidar measurements of the linear depolarization ratio, δ, contain information on the bulk characteristics of marine particles that could improve our ability to study ocean biogeochemistry. However, a scarcity of information on the polarized light-scattering properties of marine particles and the lack of a framework for separating single and multiple scattering effects on δ have hindered the development of polarization-based retrievals of bulk particle properties. To address these knowledge gaps, we made single scattering measurements of δ for several compositionally and morphologically distinct marine particle assemblages. We then used a bio-optical model to explore the influence of multiple scattering and particle characteristics on lidar measurements of δ made during an expedition to sample a mesoscale coccolithophore bloom. Laboratory measurements of linear depolarization revealed a complex dependency on particle shape, size, and composition that were consistent with scattering simulations for idealized nonspherical particles. Model results suggested that the variability in δ measured during the field expedition was driven predominantly by shifts in particle concentration rather than their bulk characteristics. However, model estimates of δ improved when calcite particles were represented by a distinct particle class, highlighting the influence of bulk particle properties on δ. To advance polarized lidar retrievals of bulk particle properties and to constrain the uncertainty in satellite lidar retrievals of particulate backscattering, these results point to the need for future efforts to characterize the variability of particulate depolarization in the ocean and to quantify the sensitivity of operational ocean lidar systems to multiple scattering.

Changing Hydrographic, Biogeochemical, and Acidification Properties in the Gulf of Maine as Measured by the Gulf of Maine North Atlantic Time Series, GNATS, Between 1998 and 2018.

The Gulf of Maine North Atlantic Time Series (GNATS) has been run since 1998, across the Gulf of Maine (GoM), between Maine and Nova Scotia. GNATS goals are to provide ocean color satellite validation and to examine change in this coastal ecosystem. We have sampled hydrographical, biological, chemical, biogeochemical, and bio-optical variables. After 2008, warm water intrusions (likely North Atlantic Slope Water [NASW]) were observed in the eastern GoM at 50-180 m depths. Shallow waters (<50 m) significantly warmed in winter, summer, and fall but cooled during spring. Surface salinity and density of the GoM also significantly increased over the 20 years. Phytoplankton standing stock and primary production showed highly-significant decreases during the period. Concentrations of phosphate increased, silicate decreased, residual nitrate [N*; nitrate-silicate] increased, and the ratio of dissolved inorganic nitrogen:phosphate decreased, suggesting increasing nitrogen limitation. Dissolved organic carbon (DOC) and its optical indices generally increased over two decades, suggesting changes to the DOC cycle. Surface seawater carbonate chemistry showed winter periods where the aragonite saturation (Ωar) dropped below 1.6 gulf-wide due to upward winter mixing of cool, corrosive water. However, associated with increased average GoM temperatures, Ωar has significantly increased. These results reinforce the hypothesis that the observed decrease in surface GoM primary production resulted from a switch from Labrador Sea Water to NASW entering the GoM. A multifactor analysis shows that decreasing GoM primary production is most significantly correlated to decreases in chlorophyll and particulate organic carbon plus increases in N* and temperature.

Osmotrophy of dissolved organic carbon by coccolithophores in darkness.

The evolutionary and ecological story of coccolithophores poses questions about their heterotrophy, surviving darkness after the end-Cretaceous asteroid impact as well as survival in the deep ocean twilight zone. Uptake of dissolved organic carbon might be an alternative nutritional strategy for supply of energy and carbon molecules. Using long-term batch culture experiments, we examined coccolithophore growth and maintenance on organic compounds in darkness. Radiolabelled experiments were performed to study the uptake kinetics. Pulse-chase experiments were used to examine the uptake into unassimilated, exchangeable pools vs assimilated, nonexchangeable pools. We found that coccolithophores were able to survive and maintain their metabolism for up to 30 d in darkness, accomplishing about one cell division. The concentration dependence for uptake was similar to the concentration dependence for growth in Cruciplacolithus neohelis, suggesting that it was taking up carbon compounds and immediately incorporating them into biomass. We recorded net incorporation of radioactivity into the particulate inorganic fraction. We conclude that osmotrophy provides nutritional flexibility and supports long-term survival in light intensities well below threshold for photosynthesis. The incorporation of dissolved organic matter into particulate inorganic carbon, raises fundamental questions about the role of the alkalinity pump and the alkalinity balance in the sea.

Polarized lidar and ocean particles: insights from a mesoscale coccolithophore bloom.

Oceanographic lidar can provide remote estimates of the vertical distribution of suspended particles in natural waters, potentially revolutionizing our ability to characterize marine ecosystems and properly represent them in models of upper ocean biogeochemistry. However, lidar signals exhibit complex dependencies on water column inherent optical properties (IOPs) and instrument characteristics, which complicate efforts to derive meaningful biogeochemical properties from lidar return signals. In this study, we used a ship-based system to measure the lidar attenuation coefficient (α) and linear depolarization ratio (δ) across a variety of optically and biogeochemically distinct water masses, including turbid coastal waters, clear oligotrophic waters, and calcite rich waters associated with a mesoscale coccolithophore bloom. Sea surface IOPs were measured continuously while underway to characterize the response of α and δ to changes in particle abundance and composition. The magnitude of α was consistent with the diffuse attenuation coefficient (Kd), though the α versus Kd relationship was nonlinear. δ was positively related to the scattering optical depth and the calcite fraction of backscattering. A statistical fit to these data suggests that the polarized scattering properties of calcified particles are distinct and contribute to measurable differences in the lidar depolarization ratio. A better understanding of the polarized scattering properties of coccolithophores and other marine particles will further our ability to interpret polarized oceanographic lidar measurements and may lead to new techniques for measuring the material properties of marine particles remotely.

Century-scale changes in phytoplankton phenology in the Gulf of Maine.

The phenology of major seasonal events is an important indicator of climate. We analyzed multiple datasets of in situ chlorophyll measurements from the Gulf of Maine dating back to the early 20th century in order to detect climate-scale changes in phenology. The seasonal cycle was consistently characterized by a two-bloom pattern, with spring and autumn blooms. The timing of both spring and autumn blooms has shifted later in the year at rates ranging from ∼1 to 9 days per decade since 1960, depending on the phenology metric, and trends only emerged at time scales of >40 years. Bloom phenology had only weak correlations with major climate indices. There were stronger associations between bloom timing and physical and chemical variables. Autumn bloom initiation correlated strongly with surface temperature and salinity, and spring bloom with nutrients. A later spring bloom also correlated with an increased cohort of Calanus finmarchicus, suggesting broader ecosystem implications of phytoplankton phenology.

Coccolith dissolution within copepod guts affects fecal pellet density and sinking rate.

The most common biomineral produced in the contemporary ocean is calcium carbonate, including the polymorph calcite produced by coccolithophores. The surface waters of the ocean are supersaturated with respect to calcium carbonate. As a result, particulate inorganic carbon (PIC), such as calcite coccoliths, is not expected thermodynamically to dissolve in waters above the lysocline (~4500-6000 m). However, observations indicate that up to 60-80% of calcium carbonate is lost in the upper 500-1000 m of the ocean. This is hypothesized to occur in microenvironments with reduced saturation states, such as zooplankton guts. Using a new application of the highly precise 14C microdiffusion technique, we show that following a period of starvation, up to 38% of ingested calcite dissolves in copepod guts. After continued feeding, our data show the gut becomes increasingly buffered, which limits further dissolution; this has been termed the Tums hypothesis (after the drugstore remedy for stomach acid). As less calcite dissolves in the gut and is instead egested in fecal pellets, the fecal pellet sinking rates double, with corresponding increases in pellet density. Our results empirically demonstrate that zooplankton guts can facilitate calcite dissolution above the chemical lysocline, and that carbon export through fecal pellet production is variable, based on the feeding history of the copepod.

Vertical Distributions of Coccolithophores, PIC, POC, Biogenic Silica, and Chlorophyll a Throughout the Global Ocean.

Coccolithophores are a critical component of global biogeochemistry, export fluxes, and seawater optical properties. We derive globally significant relationships to estimate integrated coccolithophore and coccolith concentrations as well as integrated concentrations of particulate inorganic carbon (PIC) from their respective surface concentration. We also examine surface versus integral relationships for other biogeochemical variables contributed by all phytoplankton (e.g., chlorophyll a and particulate organic carbon) or diatoms (biogenic silica). Integrals are calculated using both 100 m integrals and euphotic zone integrals (depth of 1% surface photosynthetically available radiation). Surface concentrations are parameterized in either volumetric units (e.g., m-3) or values integrated over the top optical depth. Various relationships between surface concentrations and integrated values demonstrate that when surface concentrations are above a specific threshold, the vertical distribution of the property is biased to the surface layer, and when surface concentrations are below a specific threshold, the vertical distributions of the properties are biased to subsurface maxima. Results also show a highly predictable decrease in explained-variance as vertical distributions become more vertically heterogeneous. These relationships have fundamental utility for extrapolating surface ocean color remote sensing measurements to 100 m depth or to the base of the euphotic zone, well beyond the depths of detection for passive ocean color remote sensors. Greatest integrated concentrations of PIC, coccoliths, and coccolithophores are found when there is moderate stratification at the base of the euphotic zone.

The Ecology, Biogeochemistry, and Optical Properties of Coccolithophores.

Coccolithophores are major contributors to phytoplankton communities and ocean biogeochemistry and are strong modulators of the optical field in the sea. New discoveries are changing paradigms about these calcifiers. A new role for silicon in coccolithophore calcification is coupling carbonate and silicon cycles. Phosphorus and iron play key roles in regulating coccolithophore growth. Comparing molecular phylogenies with coccolith morphometrics is forcing the reconciliation of biological and geological observations. Mixotrophy may be a possible life strategy for deep-dwelling species, which has ramifications for biological pump and alkalinity pump paradigms. Climate, ocean temperatures, and pH appear to be affecting coccolithophores in unexpected ways. Global calcification is approximately 1-3% of primary productivity and affects CO2 budgets. New measurements of the backscattering cross section of coccolithophores have improved satellite-based algorithms and their application in case I and case II optical waters. Remote sensing has allowed the detection of basin-scale coccolithophore features in the Southern Ocean.

Optical inversions of the water column based on glider measurements.

We demonstrate a method for estimating absorption and backscattering coefficients by inverting glider-measured profiles of the downwelling irradiance and upwelling radiance. The inversion method was validated against approximately 1,300 profiles of data from 22 glider missions within the Gulf of Maine over a 10 year period. The backscattering coefficient at 532 nm was estimated with a mean absolute error of 21% and bias of 0.01% compared to measured values. We could only quantitatively evaluate the absorption coefficient against the fluorometry data, but found that profiles of fluorescence and absorption were in quantitative agreement. With absorption and backscattering coefficients acting as a basis for studying the biogeochemical parameters of the constituents in the water column, these results show the potential of bio-optical gliders for studying marine ecosystems under varying sky conditions.

Multidecadal increase in North Atlantic coccolithophores and the potential role of rising CO2.

As anthropogenic carbon dioxide (CO2) emissions acidify the oceans, calcifiers generally are expected to be negatively affected. However, using data from the Continuous Plankton Recorder, we show that coccolithophore occurrence in the North Atlantic increased from ~2 to more than 20% from 1965 through 2010. We used random forest models to examine more than 20 possible environmental drivers of this change, finding that CO2 and the Atlantic Multidecadal Oscillation were the best predictors, leading us to hypothesize that higher CO2 levels might be encouraging growth. A compilation of 41 independent laboratory studies supports our hypothesis. Our study shows a long-term basin-scale increase in coccolithophores and suggests that increasing CO2 and temperature have accelerated the growth of a phytoplankton group that is important for carbon cycling.

Molecular detection of bioluminescent dinoflagellates in surface waters of the Patagonian shelf during early austral 2008.

We investigated the distribution of bioluminescent dinoflagellates in the Patagonian Shelf region using "universal" PCR primers for the dinoflagellate luciferase gene. Luciferase gene sequences and single cell PCR tests, in conjunction with taxonomic identification by microscopy, allowed us to identify and quantify bioluminescent dinoflagellates. We compared these data to coincidental discrete optical measurements of stimulable bioluminescence intensity. Molecular detection of the luciferase gene showed that bioluminescent dinoflagellates were widespread across the majority of the Patagonian Shelf region. Their presence was comparatively underestimated by optical bioluminescence measurements, whose magnitude was affected by interspecific differences in bioluminescence intensity and by the presence of other bioluminescent organisms. Molecular and microscopy data showed that the complex hydrography of the area played an important role in determining the distribution and composition of dinoflagellate populations. Dinoflagellates were absent south of the Falkland Islands where the cold, nutrient-rich, and well-mixed waters of the Falklands Current favoured diatoms instead. Diverse populations of dinoflagellates were present in the warmer, more stratified waters of the Patagonian Shelf and Falklands Current as it warmed northwards. Here, the dinoflagellate population composition could be related to distinct water masses. Our results provide new insight into the prevalence of bioluminescent dinoflagellates in Patagonian Shelf waters and demonstrate that a molecular approach to the detection of bioluminescent dinoflagellates in natural waters is a promising tool for ecological studies of these organisms.

Massive phytoplankton blooms under Arctic sea ice.

Phytoplankton blooms over Arctic Ocean continental shelves are thought to be restricted to waters free of sea ice. Here, we document a massive phytoplankton bloom beneath fully consolidated pack ice far from the ice edge in the Chukchi Sea, where light transmission has increased in recent decades because of thinning ice cover and proliferation of melt ponds. The bloom was characterized by high diatom biomass and rates of growth and primary production. Evidence suggests that under-ice phytoplankton blooms may be more widespread over nutrient-rich Arctic continental shelves and that satellite-based estimates of annual primary production in these waters may be underestimated by up to 10-fold.

Light scattering by coccoliths detached from Emiliania huxleyi.

We used in situ radiance/irradiance profiles to retrieve profiles of the spectral backscattering coefficient for all particles in an E. huxleyi coccolithophore bloom off the coast of Plymouth, UK. At high detached coccolith concentrations the spectra of backscattering all showed a minimum near approximately 550 to 600 nm. Using flow cytometry estimates of the detached coccolith concentration, and assuming all of the backscattering (over and above the backscattering by the water itself) was due to detached coccoliths, we determined the upper limit of the backscattering cross section (sigma(b)) of individual coccoliths to be 0.123+/-0.039 microm(2)/coccolith at 500 nm. Physical models of detached coccoliths were then developed and the discrete dipole approximation was used to compute their average backscattering cross section in random orientation. The result was 0.092 microm(2) at 500 nm, with the computed sigma(b) displaying a spectral shape similar to the measurements, but with less apparent increase in backscattering toward the red. When sigma(b) is computed on a per mole of calcite, rather than a per coccolith basis, it agreed reasonably well with that determined for acid-labile backscattering at 632 nm averaged over several species of cultured calcifying algae. Intact coccolithophore cells were taken into account by arguing that coccoliths attached to coccolithophore cells (forming a "coccosphere") backscatter in a manner similar to free coccoliths in random orientation. Estimating the number of coccoliths per coccosphere and using the observed number of coccolithophore cells resulted is an apparent backscattering cross section at 500 nm of 0.114+/-0.013 microm(2)/coccolith, in satisfactory agreement with the measured backscattering.