Multiple environmental controls on phytoplankton growth strategies determine adaptive responses of the N : P ratio

The controls on the 'Redfield' N:P stoichiometry of marine phytoplankton and hence the N:P ratio of the deep ocean remain incompletely understood. Here, we use a model for phytoplankton ecophysiology and growth, based on functional traits and resource-allocation trade-offs, to show how environmental filtering, biotic interactions, and element cycling in a global ecosystem model determine phytoplankton biogeography, growth strategies and macromolecular composition. Emergent growth strategies capture major observed patterns in marine biomes. Using a new synthesis of experimental RNA and protein measurements to constrain per-ribosome translation rates, we determine a spatially variable lower limit on adaptive rRNA:protein allocation and hence on the relationship between the largest cellular P and N pools. Comparison with the lowest observed phytoplankton N:P ratios and N:P export fluxes in the Southern Ocean suggests that additional contributions from phospholipid and phosphorus storage compounds play a fundamental role in determining the marine biogeochemical cycling of these elements.

A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization experiment in the equatorial Pacific Ocean

The seeding of an expanse of surface waters in the equatorial Pacific Ocean with low concentrations of dissolved iron triggered a massive phytoplankton bloom which consumed large quantities of carbon dioxide and nitrate that these microscopic plants cannot fully utilize under natural conditions. These and other observations provide unequivocal support for the hypothesis that phytoplankton growth in this oceanic region is limited by iron bioavailability.

Remote sensing of assimilation number for marine phytoplankton

Estimating primary production at large spatial scales is key to our understanding of the global carbon cycle. Algorithms to estimate primary production are well established and have been used in many studies with success. One of the key parameters in these algorithms is the chlorophyll-normalised production rate under light saturation (referred to as the light saturation parameter or the assimilation number). It is known to depend on temperature, light history and nutrient conditions, but assigning a magnitude to it at particular space-time points is difficult. In this paper, we explore two models to estimate the assimilation number at the global scale from remotely-sensed data that combine methods to estimate the carbon-to-chlorophyll ratio and the maximum growth rate of phytoplankton. The inputs to the algorithms are the surface concentration of chlorophyll, seasurface temperature, photosynthetically-active radiation af the surface of the sea, sea surface nutrient concentration and mixed-layer depth. A large database of in situ estimates of the assimilation number is used to develop the models and provide elements of validation. The comparisons with in situ observations are promising and global maps of assimilation number are produced.

Feeding and overwintering of Antarctic krill across its major habitats: The role of sea ice cover, water depth, and phytoplankton abundance

Antarctic krill (Euphausia superba) were sampled in contrasting habitats: a seasonally ice-covered deep ocean (Lazarev Sea), ice-free shelves at their northern range (South Georgia) and the Antarctic Peninsula (Bransfield Strait), and shelf and oceanic sites in the Scotia Sea. Across 92 stations, representing a year-round average, the food volume in krill stomachs comprised 71 +/- 29% algae, 17 +/- 21% protozoans, and 12 +/- 25% metazoans. Fatty acid trophic markers showed that copepods were consistently part of krill diet, not a switch food. In open waters, both diatom and copepod consumption increased with phytoplankton abundance. Under sea ice, ingestion of diatoms became rare, whereas feeding on copepods remained constant. During winter, larvae contained high but variable proportions of diatom markers, whereas in postlarvae the role of copepods increased with krill body length. Overwintering differed according to habitat. Krill from South Georgia had lower lipid stores than those from the Bransfield Strait or Lazarev Sea. Feeding effort was much reduced in Lazarev Sea krill, whereas most individuals from the Bransfield Strait and South Georgia contained phytoplankton and seabed detritus in their stomachs. Their retention of essential body reserves indicates that krill experienced most winter hardship in the Lazarev Sea, followed by South Georgia and then Bransfield Strait. This was reflected in the delayed development from juveniles to adults in the Lazarev Sea. Circumpolar comparisons of length frequencies suggest that krill growth conditions are more favorable in the southwest Atlantic than in the Lazarev Sea or off East Antarctica because of longer phytoplankton bloom periods and rewarding access to benthic food.

Flexible C : N ratio enhances metabolism of large phytoplankton when resource supply is intermittent

Phytoplankton cell size influences particle sinking rate, food web interactions and biogeographical distributions. We present a model in which the uptake, storage and assimilation of nitrogen and carbon are explicitly resolved in different-sized phytoplankton cells. In the model, metabolism and cellular C :N ratio are influenced by the accumulation of carbon polymers such as carbohydrate and lipid, which is greatest when cells are nutrient starved, or exposed to high light. Allometric relations and empirical data sets are used to constrain the range of possible C : N, and indicate that larger cells can accumulate significantly more carbon storage compounds than smaller cells. When forced with extended periods of darkness combined with brief exposure to saturating irradiance, the model predicts organisms large enough to accumulate significant carbon reserves may on average synthesize protein and other functional apparatus up to five times faster than smaller organisms. The advantage of storage in terms of average daily protein synthesis rate is greatest when modeled organisms were previously nutrient starved, and carbon storage reservoirs saturated. Small organisms may therefore be at a disadvantage in terms of average daily growth rate in environments that involve prolonged periods of darkness and intermittent nutrient limitation. We suggest this mechanism is a significant constraint on phytoplankton C :N variability and cell size distribution in different oceanic regimes.

Effect of phytoplankton size classes on bio-optical properties of phytoplankton in the Western Iberian coast: Application of models

Chlorophyll-a satellite products are routinely used in oceanography, providing a synoptic and global view of phytoplankton abundance. However, these products lack information on the community structure of the phytoplankton, which is crucial for ecological modelling and ecosystem studies. To assess the usefulness of existing methods to differentiate phytoplankton functional types (PFT) or phytoplankton size classes from satellite data, in-situ phytoplankton samples collected in the Western Iberian coast, on the North-East Atlantic, were analysed for pigments and absorption spectra. Water samples were collected in five different locations, four of which were located near the shore and another in an open-ocean, seamount region. Three different modelling approaches for deriving phytoplankton size classes were applied to the in situ data. Approaches tested provide phytoplankton size class information based on the input of pigments data (Brewin et al., 2010), absorption spectra data (Ciotti et al., 2002) or both (Uitz et al., 2008). Following Uitz et al. (2008), results revealed high variability in microphytoplankton chlorophyll-specific absorption coefficients, ranging from 0.01 to 0.09 m2 (mg chl)− 1 between 400 and 500 nm. This spectral analysis suggested, in one of the regions, the existence of small cells (< 20 μm) in the fraction of phytoplankton presumed to be microphytoplankton (based on diagnostic pigments). Ciotti et al. (2002) approach yielded the highest differences between modelled and measured absorption spectra for the locations where samples had high variability in community structure and cell size. The Brewin et al. (2010) pigment-based model was adjusted and a set of model coefficients are presented and recommended for future studies in offshore water of the Western Iberian coast.

Effects of increases in temperature and nutrients on phytoplankton community structure and photosynthesis in the Western English Channel

Anthropogenic climate change is exerting pressures on coastal ecosystems through increases in temperature, precipitation and ocean acidification. Phytoplankton community structure and photo-physiology are therefore adapting to these conditions. Changes in phytoplankton biomass and photosynthesis in relation to temperature and nutrient concentrations were assessed using a 14 year dataset from a coastal station in the Western English Channel (WEC). Dinoflagellate and coccolithophorid biomass exhibited a positive correlation with temperature, reaching the highest biomass at between 15 and 17°C. Diatoms showed a negative correlation with temperature, with highest biomass at 10°C. Chlorophyll a (chl a) normalised light-saturated photosynthetic rates (PBm) exhibited a hyperbolic response to increasing temperature, with an initial linear increase from 8 to 11°C, and reaching a plateau from 12°C. There was however no significant positive correlation between nutrients and phytoplankton biomass or PBm, which reflects the lag time between nutrient input and phytoplankton growth at this coastal site. The major phytoplankton groups that occurred at this site occupied distinct thermal niches, which in turn modified PBm. Increasing temperature, and higher water column stratification, was major factors in the initiation of dinoflagellates blooms at this site. Dinoflagellates blooms during summer also co-varied with silicate concentration, and acted as a tracer of dissolved inorganic nitrogen and phosphate from river run-off, which were subsequently reduced during these blooms. The data implies that increasing temperature and high river runoff during summer, will promote dinoflaglellates blooms in the WEC.

Mechanisms shaping size structure and functional diversity of phytoplankton communities in the ocean

The factors regulating phytoplankton community composition play a crucial role in structuring aquatic food webs. However, consensus is still lacking about the mechanisms underlying the observed biogeographical differences in cell size composition of phytoplankton communities. Here we use a trait-based model to disentangle these mechanisms in two contrasting regions of the Atlantic Ocean. In our model, the phytoplankton community can self-assemble based on a trade-off emerging from relationships between cell size and (1) nutrient uptake, (2) zooplankton grazing, and (3) phytoplankton sinking. Grazing 'pushes' the community towards larger cell sizes, whereas nutrient uptake and sinking 'pull' the community towards smaller cell sizes. We find that the stable environmental conditions of the tropics strongly balance these forces leading to persistently small cell sizes and reduced size diversity. In contrast, the seasonality of the temperate region causes the community to regularly reorganize via shifts in species composition and to exhibit, on average, bigger cell sizes and higher size diversity than in the tropics. Our results raise the importance of environmental variability as a key structuring mechanism of plankton communities in the ocean and call for a reassessment of the current understanding of phytoplankton diversity patterns across latitudinal gradients.

Analytical phytoplankton carbon measurements spanning diverse ecosystems

The measurement of phytoplankton carbon (Cphyto) in the field has been a long-sought but elusive goal in oceanography. Proxy measurements of Cphyto have been employed in the past, but are subject to many confounding influences that undermine their accuracy. Here we report the first directly measured Cphyto values from the open ocean. The Cphyto samples were collected from a diversity of environments, ranging from Pacific and Atlantic oligotrophic gyres to equatorial upwelling systems to temperate spring conditions. When compared to earlier proxies, direct measurements of Cphyto exhibit the strongest relationship with particulate backscattering coefficients (bbp) (R2=0.69). Chlorophyll concentration and total particulate organic carbon (POC) concentration accounted for ~20% less variability in Cphyto than bbp. Ratios of Cphyto to Chl a span an order of magnitude moving across and within distinct ecosystems. Similarly, Cphyto:POC ratios were variable with the lowest values coming from productive temperate waters and the highest from oligotrophic gyres. A strong relationship between Cphyto and bbp is particularly significant because bbp is a property retrievable from satellite ocean color measurements. Our results, therefore, are highly encouraging for the global monitoring of phytoplankton biomass from space. The continued application of our Cphyto measurement approach will enable validation of satellite retrievals and contribute to an improved understanding of environmental controls on phytoplankton biomass and physiology.

Phytoplankton phenology indices in coral reef ecosystems: Application to ocean-color observations in the Red Sea

Phytoplankton, at the base of the marine food web, represent a fundamental food source in coral reef ecosystems. The timing (phenology) and magnitude of the phytoplankton biomass are major determinants of trophic interactions. The Red Sea is one of the warmest and most saline basins in the world, characterized by an arid tropical climate regulated by the monsoon. These extreme conditions are particularly challenging for marine life. Phytoplankton phenological indices provide objective and quantitative metrics to characterize phytoplank- ton seasonality. The indices i.e. timings of initiation, peak, termination and duration are estimated here using 15 years (1997–2012) of remote sensing ocean-color data from the European Space Agency (ESA) Climate Change Initiative project (OC-CCI) in the entire Red Sea basin. The OC-CCI product, comprising merged and bias-corrected observations from three independent ocean-color sensors (SeaWiFS, MODIS and MERIS), and processed using the POLYMER algorithm (MERIS period), shows a significant increase in chlorophyll data cover- age, especially in the southern Red Sea during the months of summer NW monsoon. In open and reef-bound coastal waters, the performance of OC-CCI chlorophyll data is shown to be comparable with the performance of other standard chlorophyll products for the global oceans. These features have permitted us to investigate phytoplankton phenology in the entire Red Sea basin, and during both winter SE monsoon and summer NW monsoon periods. The phenological indices are estimated in the four open water provinces of the basin, and further examined at six coral reef complexes of particular socio-economic importance in the Red Sea, including Siyal Islands, Sharm El Sheikh, Al Wajh bank, Thuwal reefs, Al Lith reefs and Farasan Islands. Most of the open and deeper waters of the basin show an apparent higher chlorophyll concentration and longer duration of phyto- plankton growth during the winter period (relative to the summer phytoplankton growth period). In contrast, most of the reef-bound coastal waters display equal or higher peak chlorophyll concentrations and equal or lon- ger duration of phytoplankton growth during the summer period (relative to the winter phytoplankton growth period). The ecological and biological significance of the phytoplankton seasonal characteristics are discussed in context of ecosystem state assessment, and particularly to support further understanding of the structure and functioning of coral reef ecosystems in the Red Sea.

Influence of light in the mixed-layer on the parameters of a three-component model of phytoplankton size class

Phytoplankton size structure is an important indicator of the state of the pelagic ecosystem. Stimulated by the paucity of in situ observations on size structure, and by the sampling advantages of autonomous remote platforms, new efforts are being made to infer the size-structure of the phytoplankton from oceanographic variables that may be measured at high temporal and spatial resolution, such as total chlorophyll concentration. Large-scale analysis of in situ data has revealed coherent relationships between size-fractionated chlorophyll and total chlorophyll that can be quantified using the three-component model of Brewin et al. (2010). However, there are variations surrounding these general relationships. In this paper, we first revise the three-component model using a global dataset of surface phytoplankton pigment measurements. Then, using estimates of the average irradiance in the mixed-layer, we investigate the influence of ambient light on the parameters of the three-component model. We observe significant relationships between model parameters and the average irradiance in the mixed-layer, consistent with ecological knowledge. These relationships are incorporated explicitly into the three-component model to illustrate variations in the relationship between size-structure and total chlorophyll, ensuing from variations in light availability. The new model may be used as a tool to investigate modifications in size-structure in the context of a changing climate.

Ocean acidification with (de)eutrophication will alter future phytoplankton growth and succession.

Human activity causes ocean acidification (OA) though the dissolution of anthropogenically generated CO2 into seawater, and eutrophication through the addition of inorganic nutrients. Eutrophication increases the phytoplankton biomass that can be supported during a bloom, and the resultant uptake of dissolved inorganic carbon during photosynthesis increases water-column pH (bloom-induced basification). This increased pH can adversely affect plankton growth. With OA, basification commences at a lower pH. Using experimental analyses of the growth of three contrasting phytoplankton under different pH scenarios, coupled with mathematical models describing growth and death as functions of pH and nutrient status, we show how different conditions of pH modify the scope for competitive interactions between phytoplankton species. We then use the models previously configured against experimental data to explore how the commencement of bloom-induced basification at lower pH with OA, and operating against a background of changing patterns in nutrient loads, may modify phytoplankton growth and competition. We conclude that OA and changed nutrient supply into shelf seas with eutrophication or de-eutrophication (the latter owing to pollution control) has clear scope to alter phytoplankton succession, thus affecting future trophic dynamics and impacting both biogeochemical cycling and fisheries.

Temporal variability in total, micro- and nano-phytoplankton primary production at a coastal site in the Western English Channel

Primary productivity and subsequent carbon cycling in the coastal zone have a significant impact on the global carbon budget. It is currently unclear how anthropogenic activity could alter these budgets but long term coastal time series of hydrological, biogeochemical and biological measurements represent a key means to better understand past drivers, and hence to predicting future seasonal and inter-annual variability in carbon fixation in coastal ecosystems. An 8-year time series of primary production from 2003 to 2010, estimated using a recently developed absorption-based algorithm, was used to determine the nature and extent of change in primary production at a coastal station (L4) in the Western English Channel (WEC). Analysis of the seasonal and inter-annual variability in production demonstrated that on average, nano- and pico-phytoplankton account for 48% of the total carbon fixation and micro-phytoplankton for 52%. A recent decline in the primary production of nano- and pico-phytoplankton from 2005 to 2010 was observed, corresponding with a decrease in winter nutrient concentrations and a decrease in the biomass of Phaeocystis sp. Micro-phytoplankton primary production (PPM) remained relatively constant over the time series and was enhanced in summer during periods of high precipitation. Increases in sea surface temperature, and decreases in wind speeds and salinity were associated with later spring maxima in PPM. Together these trends indicate that predicted increases in temperature and decrease in wind speeds in future would drive later spring production whilst predicted increases in precipitation would also continue these blooms throughout the summer at this site.

The combined effects of seasonal community succession and adaptive algal physiology on lipid profiles of coastal phytoplankton in the western English channel

Lipids are key constituents of marine phytoplankton, and some fatty acids (key constituents of lipids) are essential dietary components for secondary producers. However, in natural marine ecosystems the interactions of factors affecting seasonal phytoplankton lipid composition are still poorly understood. The aim of this study was to assess the roles of seasonal succession in phytoplankton community composition and nutrient concentrations, on the lipid composition of the phytoplankton community. Fatty acid and polar lipid composition in seston was measured in surface waters at the time series station L4, an inshore station in the Western English Channel, from January to December 2013. Redundancy analyses (RDA) were used to identify factors (abiotic and biotic) that explained the seasonal variability in phytoplankton lipids. RDA demonstrated that nutrients (namely nitrogen) explained the majority of variation in phytoplankton lipid composition, as well as a smaller explanatory contribution from changes in phytoplankton community composition. The physiological adaptations of the phytoplankton community to nutrient deplete conditions during the summer season when the water column was stratified, was further supported by changes in the polar lipid to phytoplankton biomass ratios (also modelled with RDA) and increases in the lipid to chlorophyll a ratios, which are both indicative of nutrient stress. However, the association of key fatty acid markers with phytoplankton groups e.g. 22:6 n-3 and dinoflagellate biomass (predominant in summer), meant there were no clear seasonal differences in the overall degree of fatty acid saturation, as might have been expected from typical nutrient stress on phytoplankton. Based on the use of polyunsaturated fatty acids (PUFA) as markers of ‘food quality’ for grazers, our results suggest that in this environment high food quality is maintained throughout summer, due to seasonal succession towards flagellated phytoplankton species able to maintain PUFA synthesis under surface layer nutrient depletion.