Phytoplankton size structure controls the trophic organization of planktonic communities and their ability to export biogenic materials toward the ocean's 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.
Contrary to predictions by the allometric theory, there is evidence that phytoplankton growth rates peak at intermediate cell sizes. However, it is still unknown if this pattern may result from the ...effect of experimental temperature. Here we test whether temperature affects the unimodal size scaling pattern of phytoplankton growth by (1) growing Synechococcus sp., Ostreococcus tauri, Micromonas commoda and Pavlova lutheri at 18 °C and 25 °C, and (2) using thermal response curves available in the literature to estimate the growth rate at 25 °C as well as the maximum growth rate at optimal temperature for 22 species assayed previously at 18 °C. We also assess the sensitivity of growth rate estimates to the metric employed for measuring standing stocks, by calculating growth rates based on in vivo fluorescence, chlorophyll a concentration, cell abundance and biomass (particulate organic carbon and nitrogen content). Our results show that the unimodal size scaling pattern of phytoplankton growth, with a peak at intermediate cell sizes, is observed at 18 °C, 25 °C and at the optimal temperature for growth, and that it prevails irrespective of the standing-stock metric used. The unimodal size scaling pattern of phytoplankton growth is supported by two independent field observations reported in the literature: (i) a positive relationship between cell size and metabolic rate in the picophytoplankton size range and (ii) the dominance of intermediate-size cells in nutrient-rich waters during blooms.
Climate warming has the potential to alter ecosystem function through temperature-dependent changes in individual metabolic rates. The temperature sensitivity of phytoplankton metabolism is ...especially relevant, since these microorganisms sustain marine food webs and are major drivers of biogeochemical cycling. Phytoplankton metabolic rates increase with temperature when nutrients are abundant, but it is unknown if the same pattern applies under nutrient-limited growth conditions, which prevail over most of the ocean. Here we use continuous cultures of three cosmopolitan and biogeochemically relevant species (Synechococcus sp., Skeletonema costatum and Emiliania huxleyi) to determine the temperature dependence (activation energy, E
) of metabolism under different degrees of nitrogen (N) limitation. We show that both CO
fixation and respiration rates increase with N supply but are largely insensitive to temperature. E
of photosynthesis (0.11 ± 0.06 eV, mean ± SE) and respiration (0.04 ± 0.17 eV) under N-limited growth is significantly smaller than E
of growth rate under nutrient-replete conditions (0.77 ± 0.06 eV). The reduced temperature dependence of metabolic rates under nutrient limitation can be explained in terms of enzyme kinetics, because both maximum reaction rates and half-saturation constants increase with temperature. Our results suggest that the direct, stimulating effect of rising temperatures upon phytoplankton metabolic rates will be circumscribed to ecosystems with high-nutrient availability.
Trait diversity, a key component of biodiversity, mediates many essential ecosystem functions and services. However, the mechanisms behind such relationships at large spatial scales are not fully ...understood. Here we adopt the functional biogeography approach to investigate how the size composition of phytoplankton communities relates to primary production and export production along a broad latitudinal gradient. Using in situ phytoplankton size distribution data and a trait-based model, we find an increase in the average phytoplankton size, size diversity, primary production and export when moving from low to high latitudes. Our analysis indicates that the interplay between spatio-temporal heterogeneities in environmental conditions and a trade-off between the high affinity for nutrients of smaller cells and the ability to avoid predation by larger cells are the main mechanisms driving the observed patterns. Our results also suggest that variations in size diversity alone do not directly lead to changes in primary production and export. The trade-off thus introduces a feedback that influences the relationship between size diversity and ecosystem functions. These findings support the importance of environmentally mediated trade-offs as crucial mechanisms shaping biodiversity and ecosystem function relationships at large spatial scales.
Jensen's inequality predicts that the response of any given system to average constant conditions is different from its average response to varying ones. Environmental fluctuations in abiotic ...conditions are pervasive on Earth; yet until recently, most ecological research has addressed the effects of multiple environmental drivers by assuming constant conditions. One could thus expect to find significant deviations in the magnitude of their effects on ecosystems when environmental fluctuations are considered. Drawing on experimental studies published during the last 30 years reporting more than 950 response ratios (
= 5,700), we present a comprehensive analysis of the role that environmental fluctuations play across the tree of life. In contrast to the predominance of interactive effects of global-change drivers reported in the literature, our results show that their cumulative effects were additive (58%), synergistic (26%), and antagonistic (16%) when environmental fluctuations were present. However, the dominant type of interaction varied by trophic level (autotrophs: interactive; heterotrophs: additive) and phylogenetic group (additive in Animalia; additive and positive antagonism in Chromista; negative antagonism and synergism in Plantae). In addition, we identify the need to tackle how complex communities respond to fluctuating environments, widening the phylogenetic and biogeographic ranges considered, and to consider other drivers beyond warming and acidification as well as longer timescales. Environmental fluctuations must be taken into account in experimental and modeling studies as well as conservation plans to better predict the nature, magnitude, and direction of the impacts of global change on organisms and ecosystems.
Grazing by herbivorous protists contributes to structuring plankton communities through its effect on the growth, biomass, and competitiveness of prey organisms and also impacts the transfer of ...primary production towards higher trophic levels. Previous evidence shows that heterotrophic processes (grazing rates,
g
) are more sensitive to temperature than autotrophic ones (phytoplankton growth rates,
μ
) and also that small cells tend to be more heavily predated than larger ones; however, it remains unresolved how the interplay between changes in temperature and cell size modulates grazing pressure (i.e.,
g
:
μ
ratio). We addressed this problem by conducting an experiment with four phytoplankton populations, from pico- to microphytoplankton, over a 12 °C gradient and in the presence/absence of a generalist herbivorous protist,
Oxyrrhis marina
. We found that highest
g
rates coincided with highest
μ
rates, which corresponded to intermediate cell sizes. There were no significant differences in either
μ
or
g
between the smallest and largest cell sizes considered. The
g
:
μ
ratio was largely independent of cell size and C:N ratios, and its thermal dependence was low although species-specific differences were large. We suggest that the similar
g
:
μ
found could be the consequence that the energetic demand imposed by rising temperatures would be a more important issue than the mechanical constriction to ingestion derived from prey cell size. Despite the difficulty of quantifying
μ
and
g
in natural planktonic communities, we suggest that the
g
:
μ
ratio is a key response variable to evaluate thermal sensitivity of food webs because it gives a more integrative view of trophic functioning than both rates separately.
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.
We conducted a meta-analysis of temperature, phytoplankton size structure, and productivity in cold, temperate, and warm waters of the world’s oceans. Our data set covers all combinations of ...temperature and resource availability, thus allowing us to disentangle their effects. The partitioning of biomass between different size classes is independent of temperature, but depends strongly on the rate of resource use as reflected in the rate of primary production. Temperature and primary production explained 2% and 62%, respectively, of the variability in the contribution of microphytoplankton to total biomass. This contribution increases rapidly with total biomass and productivity, reaching values > 80% when chlorophyll a concentration is > 2 μg L−1 or primary production is > 100 μg C L−1 d−1, irrespective of water temperature. Conversely, picophytoplankton contribution is substantial (> 40%), at all temperatures, only when chlorophyll a concentration is < 1 μg L−1 or primary production is < 50 μg C L−1 d−1. The temperature–size rule cannot explain these changes, which instead reflect fundamental reorganizations in the species composition of the assemblage, arising from taxon- and size-dependent differences in resource acquisition and use. Given that resource availability, rather than temperature per se, is the key factor explaining the relative success of different algal size classes, there will be no single, universal effect of global warming on phytoplankton size structure.
Phytoplankton size structure is key for the ecology and biogeochemistry of pelagic ecosystems, but the relationship between cell size and maximum growth rate (μmax) is not yet well understood. We ...used cultures of 22 species of marine phytoplankton from five phyla, ranging from 0.1 to 106 μm3 in cell volume (Vcell), to determine experimentally the size dependence of growth, metabolic rate, elemental stoichiometry and nutrient uptake. We show that both μmax and carbon‐specific photosynthesis peak at intermediate cell sizes. Maximum nitrogen uptake rate (VmaxN) scales isometrically with Vcell, whereas nitrogen minimum quota scales as Vcell0.84. 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 VmaxN 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.
Primary production and photoacclimation models are two important classes of physiological models that find applications in remote sensing of pools and fluxes of carbon associated with phytoplankton ...in the ocean. They are also key components of ecosystem models designed to study biogeochemical cycles in the ocean. So far, these two classes of models have evolved in parallel, somewhat independently of each other. Here we examine how they are coupled to each other through the intermediary of the photosynthesis-irradiance parameters. We extend the photoacclimation model to accommodate the spectral effects of light penetration in the ocean and the spectral sensitivity of the initial slope of the photosynthesis-irradiance curve, making the photoacclimation model fully compatible with spectrally resolved models of photosynthesis in the ocean. The photoacclimation model contains a parameter
, which is the maximum chlorophyll-to-carbon ratio that phytoplankton can attain when available light tends to zero. We explore how size-class-dependent values of
could be inferred from field data on chlorophyll and carbon content in phytoplankton, and show that the results are generally consistent with lower bounds estimated from satellite-based primary production calculations. This was accomplished using empirical models linking phytoplankton carbon and chlorophyll concentration, and the range of values obtained in culture measurements. We study the equivalence between different classes of primary production models at the functional level, and show that the availability of a chlorophyll-to-carbon ratio facilitates the translation between these classes. We discuss the importance of the better assignment of parameters in primary production models as an important avenue to reduce model uncertainties and to improve the usefulness of satellite-based primary production calculations in climate research.
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