Emilio Marañón

Unimodal size scaling of phytoplankton growth and the size dependence of nutrient uptake and use

Phytoplankton size structure is key for the ecology and biogeochemistry of pelagic ecosystems, but the relationship between cell size and maximum growth rate (μ(max) ) is not yet well understood. We used cultures of 22 species of marine phytoplankton from five phyla, ranging from 0.1 to 10(6) μm(3) in cell volume (V(cell) ), to determine experimentally the size dependence of growth, metabolic rate, elemental stoichiometry and nutrient uptake. We show that both μ(max) and carbon-specific photosynthesis peak at intermediate cell sizes. Maximum nitrogen uptake rate (V(maxN) ) scales isometrically with V(cell) , whereas nitrogen minimum quota scales as V(cell) (0.84) . Large cells thus possess high ability to take up nitrogen, relative to their requirements, and large storage capacity, but their growth is limited by the conversion of nutrients into biomass. Small species show similar volume-specific V(maxN) compared to their larger counterparts, but have higher nitrogen requirements. We suggest that the unimodal size scaling of phytoplankton growth arises from taxon-independent, size-related constraints in nutrient uptake, requirement and assimilation.

Cell Size as a Key Determinant of Phytoplankton Metabolism and Community Structure

Phytoplankton size structure controls the trophic organization of planktonic communities and their ability to export biogenic materials toward the oceans interior. Our understanding of the mechanisms that drive the variability in phytoplankton size structure has been shaped by the assumption that the pace of metabolism decreases allometrically with increasing cell size. However, recent field and laboratory evidence indicates that biomass-specific production and growth rates are similar in both small and large cells but peak at intermediate cell sizes. The maximum nutrient uptake rate scales isometrically with cell volume and superisometrically with the minimum nutrient quota. The unimodal size scaling of phytoplankton growth arises from ataxonomic, size-dependent trade-off processes related to nutrient requirement, acquisition, and use. The superior ability of intermediate-size cells to exploit high nutrient concentrations explains their biomass dominance during blooms. Biogeographic patterns in phytoplankton size structure and growth rate are independent of temperature and driven mainly by changes in resource supply.

Phytoplankton biomass and production in shelf waters off NW Spain: spatial and seasonal variability in relation to upwelling

SummaryChlorophyll-a and primary production on the euphotic zone of the N-NW Spanish shelf were studied at 125 stations between 1984 and 1992. Three geographic areas (Cantabrian Sea, Rías Altas and Was Baixas), three bathymetric ranges (20 to 60 m, 60 to 150 m and stations deeper than 200 m), and four oceanographic stages (spring and autumn blooms, summer upwelling, summer stratification and winter mixing) were considered. One of the major sources of variability of chlorophyll and production data was season. Bloom and summer upwelling stages have equivalent mean and maximum values. Average chlorophyll-a concentrations approximately doubled in every step of the increasing productivity sequence: winter mixing — summer stratification — high productivity (upwelling and bloom) stages. Average primary production rates increased only 60% in the described sequence. Mean (± sd) values of chlorophyll-a and primary production rates during the high productivity stages were 59.7 ± 39.5 mg Chl-a m−2 and 86.9 ± 44.0 mg C m−2 h−1, respectively. Significant differences in both chlorophyll and primary production resulted between geographic areas in most stages. Only 27 stations showed the effects of the summer upwelling that affected coastal areas in the Cantabrian Sea and Rías Baixas shelf, but also shelf-break stations in the Rías Altas area. The Rías Baixas area had lower chlorophyll than both the Rías Altas and the Cantabrian Sea areas during spring and autumn blooms, but higher during summer upwelling events. On the contrary, primary production rates were higher in the Rías Baixas area during blooms in spring and autumn. Mid-shelf areas showed the highest chlorophyll concentrations during high productivity stages, probably due to the existence of frontal zones in all geographic areas considered. The estimated phytoplankton growth rates were comparable to those of other coastal upwelling systems, with average values lower than the maximum potential growth rates. Doubling rates for upwelling and stratification stages in the northern and Rías Altas shelf areas were equivalent, despite larger biomass accumulations during upwelling events. Low turnover rates of the existing biomass in the Rías Baixas shelf in upwelling stages suggests that the accumulation of phytoplankton was due mainly to the export from the highly productive rías, while the contribution of in situ production to these accumulations was relatively lower.

The significance of the episodic nature of atmospheric deposition to Low Nutrient Low Chlorophyll regions

In the vast Low Nutrient Low-Chlorophyll (LNLC) Ocean, the vertical nutrient supply from the subsurface to the sunlit surface waters is low, and atmospheric contribution of nutrients may be one order of magnitude greater over short timescales. The short turnover time of atmospheric Fe and N supply (<1 month for nitrate) further supports deposition being an important source of nutrients in LNLC regions. Yet, the extent to which atmospheric inputs are impacting biological activity and modifying the carbon balance in oligotrophic environments has not been constrained. Here, we quantify and compare the biogeochemical impacts of atmospheric deposition in LNLC regions using both a compilation of experimental data and model outputs. A metadata-analysis of recently conducted field and laboratory bioassay experiments reveals complex responses, and the overall impact is not a simple “fertilization effect of increasing phytoplankton biomass” as observed in HNLC regions. Although phytoplankton growth may be enhanced, increases in bacterial activity and respiration result in weakening of biological carbon sequestration. The application of models using climatological or time-averaged non-synoptic deposition rates produced responses that were generally much lower than observed in the bioassay experiments. We demonstrate that experimental data and model outputs show better agreement on short timescale (days to weeks) when strong synoptic pulse of aerosols deposition, similar in magnitude to those observed in the field and introduced in bioassay experiments, is superimposed over the mean atmospheric deposition fields. These results suggest that atmospheric impacts in LNLC regions have been underestimated by models, at least at daily to weekly timescales, as they typically overlook large synoptic variations in atmospheric deposition and associated nutrient and particle inputs. Inclusion of the large synoptic variability of atmospheric input, and improved representation and parameterization of key processes that respond to atmospheric deposition, is required to better constrain impacts in ocean biogeochemical models. This is critical for understanding and prediction of current and future functioning of LNLC regions and their contribution to the global carbon cycle.

Isometric size-scaling of metabolic rate and the size abundance distribution of phytoplankton

The relationship between phytoplankton cell size and abundance has long been known to follow regular, predictable patterns in near steady-state ecosystems, but its origin has remained elusive. To explore the linkage between the size-scaling of metabolic rate and the size abundance distribution of natural phytoplankton communities, we determined simultaneously phytoplankton carbon fixation rates and cell abundance across a cell volume range of over six orders of magnitude in tropical and subtropical waters of the Atlantic Ocean. We found an approximately isometric relationship between carbon fixation rate and cell size (mean slope value: 1.16; range: 1.03–1.32), negating the idea that Kleibers law is applicable to unicellular autotrophic protists. On the basis of the scaling of individual resource use with cell size, we predicted a reciprocal relationship between the size-scalings of phytoplankton metabolic rate and abundance. This prediction was confirmed by the observed slopes of the relationship between phytoplankton abundance and cell size, which have a mean value of −1.15 (range: −1.29 to −0.97), indicating that the size abundance distribution largely results from the size-scaling of metabolic rate. Our results imply that the total energy processed by carbon fixation is constant along the phytoplankton size spectrum in near steady-state marine ecosystems.

Decrease in the Autotrophic-to-Heterotrophic Biomass Ratio of Picoplankton in Oligotrophic Marine Waters Due to Bottle Enclosure

ABSTRACT We investigated the effects of bottle enclosure on autotrophic and heterotrophic picoplankton in North and South subtropical Atlantic oligotrophic waters, where the biomass and metabolism of the microbial community are dominated by the picoplankton size class. We measured changes in both autotrophic (Prochlorococcus, Synechococcus, and picoeukaryotes) and heterotrophic picoplankton biomass during three time series experiments and in 16 endpoint experiments over 24 h in light and dark treatments. Our results showed a divergent effect of bottle incubation on the autotrophic and heterotrophic components of the picoplankton community. The biomass of picophytoplankton showed, on average, a >50% decrease, mostly affecting the picoeukaryotes and, to a lesser extent, Prochlorococcus. In contrast, the biomass of heterotrophic bacteria remained constant or increased during the incubations. We also sampled 10 stations during a Lagrangian study in the North Atlantic subtropical gyre, which enabled us to compare the observed changes in the auto- to heterotrophic picoplankton biomass ratio (AB:HB ratio) inside the incubation bottles with those taking place in situ. While the AB:HB ratio in situ remained fairly constant during the Lagrangian study, it decreased significantly during the 24 h of incubation experiments. Thus, the rapid biomass changes observed in the incubations are artifacts resulting from bottle confinement and do not take place in natural conditions. Our results suggest that short (<1 day) bottle incubations in oligotrophic waters may lead to biased estimates of the microbial metabolic balance by underestimating primary production and/or overestimating bacterial respiration.

Resource supply overrides temperature as a controlling factor of marine phytoplankton growth.

The universal temperature dependence of metabolic rates has been used to predict how ocean biology will respond to ocean warming. Determining the temperature sensitivity of phytoplankton metabolism and growth is of special importance because this group of organisms is responsible for nearly half of global primary production, sustains most marine food webs, and contributes to regulate the exchange of CO2 between the ocean and the atmosphere. Phytoplankton growth rates increase with temperature under optimal growth conditions in the laboratory, but it is unclear whether the same degree of temperature dependence exists in nature, where resources are often limiting. Here we use concurrent measurements of phytoplankton biomass and carbon fixation rates in polar, temperate and tropical regions to determine the role of temperature and resource supply in controlling the large-scale variability of in situ metabolic rates. We identify a biogeographic pattern in phytoplankton metabolic rates, which increase from the oligotrophic subtropical gyres to temperate regions and then coastal waters. Variability in phytoplankton growth is driven by changes in resource supply and appears to be independent of seawater temperature. The lack of temperature sensitivity of realized phytoplankton growth is consistent with the limited applicability of Arrhenius enzymatic kinetics when substrate concentrations are low. Our results suggest that, due to widespread resource limitation in the ocean, the direct effect of sea surface warming upon phytoplankton growth and productivity may be smaller than anticipated.

Phytoplankton Size Structure

Cell size affects many aspects of phytoplankton physiology and ecology over several levels of organization, including individuals, populations, and communities. Small cell size is advantageous in terms of nutrient uptake, light absorption, and avoidance of sedimentation in stratified waters. These factors explain that small cells dominate phytoplankton assemblages in oligotrophic environments. The dominance of larger species in productive ecosystems can be explained by a combination of physiological and trophic mechanisms. First, large phytoplankton, in spite of geometrical constraints on resource acquisition, are able to sustain metabolic and growth rates as high as, or even higher than, those of smaller cells, particularly when resources are plentiful. Second, large phytoplankton, compared to their smaller counterparts, are less strictly controlled by grazing, as a result of the difference between their generation time and that of their predators. The size structure of phytoplankton strongly affects the efficiency of the biological pump. In unproductive ecosystems, where phytoplankton are dominated by small cells, most of the newly produced organic matter is remineralized within the euphotic layer, thus leaving little potential for export. By contrast, phytoplankton assemblages dominated by larger cells are typical of dynamic environments that are subject to perturbations leading to enhanced resource supply and productivity. In these ecosystems, production and consumption of organic matter are decoupled and the biological pump effectively transports biogenic carbon toward the oceans interior, thus contributing to CO2 sequestration.

Review of the main ecological features affecting benthic dinoflagellate blooms

Abstract Both benthic and planktic dinoflagellates can produce harmful algal blooms. However most of the studies conducted so far emphasized on planktic species. In the present review, we assessed the main ecological factors affecting the population dynamics of bloomforming benthic dinoflagellates, with particular emphasis on Ostreopsis and Gambierdiscus. Based on the basic equation of population dynamics, we mainly focused on growth, predation, mortality, immigration and dispersion. Factors determining the dynamics of benthic dinoflagellate populations are very different from the well-studied case of planktic dinoflagellates. The relative movement of cells and water is the main difference as benthic dinoflagellates depend on a fixed substratum while planktic dinoflagellates depend on a water body. Any alteration in the substratum will affect benthic dinoflagellate populations, as for example the changes in seaweeds concentrations due to predation by sea urchins. We also evaluated the impact of global changes on dinoflagellates bloom occurrence.

Intracellular carbon partitioning in the coccolithophorid Emiliania huxleyi

Experiments carried out with the coccolithophorid Emiliania huxleyi maintained in batch cultures showed that the patterns of photosynthetic carbon metabolism characteristic of this species are: (1) carbon incorporation into proteins only represents about 20% of total carbon fixation into organic carbon, (2) protein synthesis in darkness is a significant and growth-dependent process, (3) most of the carbon fixed photosynthetically (45–60%) flows towards the lipid fraction, (4) the relative contribution of lipid-C to cellular biomass is directly related to the amount of calcite-C present as coccoliths, (5) half of the carbon incorporated into polysaccharides during the light period is respired during the night, (6) dark 14C losses during the night generally represent 10–13% of gross photosynthesis, and (7) the release of dissolved organic carbon is related to growth stage and accounts for 2–6% of the total amount of carbon incorporated photosynthetically. Most of these patterns of carbon partitioning were validated in natural phytoplankton assemblages dominated by E. huxleyi during sampling conducted in the Norwegian fjords. The results are interpreted and discussed in terms of their potential ecological and biogeochemical significance.