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.

Photoacclimation of natural phytoplankton communities

Phytoplankton regulate internal pigment concentrations in response to light and nutrient availability. Chlorophyll to carbon ratios (Chl:Cphyto) are commonly reported as a function of growth irradiance (Eg) for evaluating the photoacclimation response of phytoplankton. In contrast to most culture experiments, natural phytoplankton communities experience fluctuating environmental conditions making it difficult to compare field and lab observations. Observing and understanding photoacclimation in nature is important for deciphering changes in Chl:Cphyto resulting from environmental forcings and for accurately estimating net primary production (NPP) in models which rely on a parameterized description of photoacclimation. Here we employ direct analytical measurements of Cphyto and parallel high-resolution biomass estimates from particulate backscattering (bbp) and flow cytometry to investigate Chl:Cphyto in natural phytoplankton communities. Chl:Cphyto observed over a wide range of Eg in the field was consistent with photoacclimation responses inferred from satellite observations. Field-based photoacclimation observations for a mixed natural community contrast with laboratory results for single species grown in continuous light and nutrient replete conditions. Applying a carbon-based net primary production (NPP) model to our field data for a north-south transect in the Atlantic Ocean results in estimates that closely match 14C depth-integrated NPP for the same cruise and with historical records for the distinct biogeographic regions of the Atlantic Ocean. Our results are consistent with previous satellite and model observations of cells growing in natural or fluctuating light and showcase how direct measurements of Cphyto can be applied to explore phytoplankton photophysiology, growth rates, and production at high spatial resolution in-situ.

Abundance of a chlorophyll a precursor and the oxidation product hydroxychlorophyll a during seasonal phytoplankton community progression in the Western English Channel

This study presents the first in-situ measurements of the chlorophyll a oxidation product, hydroxychlorophyll a as well as the chlorophyll a precursor, chlorophyll aP276 conducted over an annual cycle. Chlorophyll a oxidation products, such as hydroxychlorophyll a may be associated with the decline of algal populations and can act as an initial step in the degradation of chlorophyll a into products which can be found in the geochemical record, important for studying past climate change events. Here, hydroxychlorophyll a and chlorophyll aP276 were measured at the long-term monitoring station L4, Western Channel Observatory (UK, www.westernchannelobservatory.org) over an annual cycle (2012). Weekly measurements of phytoplankton species composition and abundance enabled detailed analysis of possible sources of hydroxychlorophyll a. Dinoflagellates, 2 diatom species, the prymnesiophyte Phaeocystis spp. and the coccolithophorid Emiliania huxleyi were all associated with hydroxychlorophyll a occurrence. However, during alternate peaks in abundance of the diatoms, no association with hydroxychlorophyll a occurred, indicating that the oxidation of chlorophyll a was dependant not only on species but also on additional factors such as the mode of mortality, growth limiting factor (i.e. nutrient concentration) or phenotypic plasticity. Surface sediment samples contained 10 times more hydroxychlorophyll a (relative to chlorophyll a) than pelagic particulate samples, indicating that more chlorophyll a oxidation occurred during sedimentation or at the sediment–water interface, than in the pelagic environment. In addition, chlorophyll aP276 correlated with chl-a concentration, thus supporting its assignment as a chl-a precursor.

Effect of ocean acidification and elevated fCO2 on trace gas production by a Baltic Sea summer phytoplankton community

The Baltic Sea is a unique environment as the largest body of brackish water in the world. Acidification of the surface oceans due to absorption of anthropogenic CO2 emissions is an additional stressor facing the pelagic community of the already challenging Baltic Sea. To investigate its impact on trace gas biogeochemistry, a large-scale mesocosm experiment was performed off Tvärminne Research Station, Finland in summer 2012. During the second half of the experiment, dimethylsulphide (DMS) concentrations in the highest fCO2 mesocosms (1075–1333 μatm) were 34 % lower than at ambient CO2 (350 μatm). However the net production (as measured by concentration change) of seven halocarbons analysed was not significantly affected by even the highest CO2 levels after 5 weeks exposure. Methyl iodide (CH3I) and diiodomethane (CH2I2) showed 15 % and 57 % increases in mean mesocosm concentration (3.8 ± 0.6 pmol L−1 increasing to 4.3 ± 0.4 pmol L−1 and 87.4 ± 14.9 pmol L−1 increasing to 134.4 ± 24.1 pmol L−1 respectively) during Phase II of the experiment, which were unrelated to CO2 and corresponded to 30 % lower Chl-ɑ concentrations compared to Phase I. No other iodocarbons increased or showed a peak, with mean chloroiodomethane (CH2ClI) concentrations measured at 5.3 (± 0.9) pmol L−1 and iodoethane (C2H5I) at 0.5 (± 0.1) pmol L−1. Of the concentrations of bromoform (CHBr3; mean 88.1 ± 13.2 pmol L−1), dibromomethane (CH2Br2; mean 5.3 ± 0.8 pmol L−1) and dibromochloromethane (CHBr2Cl, mean 3.0 ± 0.5 pmol L−1), only CH2Br2 showed a decrease of 17 % between Phases I and II, with CHBr3 and CHBr2Cl showing similar mean concentrations in both Phases. Outside the mesocosms, an upwelling event was responsible for bringing colder, high CO2, low pH water to the surface starting on day t16 of the experiment; this variable CO2 system with frequent upwelling events implies the community of the Baltic Sea is acclimated to regular significant declines in pH caused by up to 800 μatm fCO2. After this upwelling, DMS concentrations declined, but halocarbon concentrations remained similar or increased compared to measurements prior to the change in conditions. Based on our findings, with future acidification of Baltic Sea waters, biogenic halocarbon emissions are likely to remain at similar values to today, however emissions of biogenic sulphur could significantly decrease from this region.

An assessment of phytoplankton primary productivity in the Arctic Ocean from satellite ocean color/in situ chlorophyll-abased models

We investigated 32 net primary productivity (NPP) models by assessing skills to reproduce integrated NPP in the Arctic Ocean. The models were provided with two sources each of surface chlorophyll-a concentration (chlorophyll), photosynthetically available radiation (PAR), sea surface temperature (SST), and mixed-layer depth (MLD). The models were most sensitive to uncertainties in surface chlorophyll, generally performing better with in situ chlorophyll than with satellite-derived values. They were much less sensitive to uncertainties in PAR, SST, and MLD, possibly due to relatively narrow ranges of input data and/or relatively little difference between input data sources. Regardless of type or complexity, most of the models were not able to fully reproduce the variability of in situ NPP, whereas some of them exhibited almost no bias (i.e., reproduced the mean of in situ NPP). The models performed relatively well in low-productivity seasons as well as in sea ice-covered/deep-water regions. Depth-resolved models correlated more with in situ NPP than other model types, but had a greater tendency to overestimate mean NPP whereas absorption-based models exhibited the lowest bias associated with weaker correlation. The models performed better when a subsurface chlorophyll-a maximum (SCM) was absent. As a group, the models overestimated mean NPP, however this was partly offset by some models underestimating NPP when a SCM was present. Our study suggests that NPP models need to be carefully tuned for the Arctic Ocean because most of the models performing relatively well were those that used Arctic-relevant parameters.

Ecological equivalence of species within phytoplankton functional groups

1.There are tens of thousands of species of phytoplankton found throughout the tree of life. Despite this diversity, phytoplankton are often aggregated into a few functional groups according to metabolic traits or biogeochemical role. We investigate the extent to which phytoplankton species dynamics are neutral within functional groups. 2.Seasonal dynamics in many regions of the ocean are known to affect phytoplankton at the functional group level leading to largely predictable patterns of seasonal succession. It is much more difficult to make general statements about the dynamics of individual species. 3.We use a 7 year time-series at station L4 in the Western English Channel with 57 diatom and 17 dinoflagellate species enumerated weekly to test if the abundance of diatom and dinoflagellate species vary randomly within their functional group envelope or if each species is driven uniquely by external factors. 4.We show that the total biomass of the diatom and dinoflagellate functional groups is well predicted by irradiance and temperature and quantify trait values governing the growth rate of both functional groups. The biomass dynamics of the functional groups are not neutral and each has their own distinct responses to environmental forcing. Compared to dinoflagellates, diatoms have faster growth rates, and grow faster under lower irradiance, cooler temperatures, and higher nutrient conditions. 5.The biomass of most species vary randomly within their functional group biomass envelope, most of the time. As a consequence, modelers will find it difficult to predict the biomass of most individual species. Our analysis supports the approach of using a single set of traits for a functional group and suggests that it should be possible to determine these traits from natural communities.