Pedro Cermeño

The role of nutricline depth in regulating the ocean carbon cycle

Carbon uptake by marine phytoplankton, and its export as organic matter to the ocean interior (i.e., the “biological pump”), lowers the partial pressure of carbon dioxide (pCO2) in the upper ocean and facilitates the diffusive drawdown of atmospheric CO2. Conversely, precipitation of calcium carbonate by marine planktonic calcifiers such as coccolithophorids increases pCO2 and promotes its outgassing (i.e., the “alkalinity pump”). Over the past ≈100 million years, these two carbon fluxes have been modulated by the relative abundance of diatoms and coccolithophores, resulting in biological feedback on atmospheric CO2 and Earths climate; yet, the processes determining the relative distribution of these two phytoplankton taxa remain poorly understood. We analyzed phytoplankton community composition in the Atlantic Ocean and show that the distribution of diatoms and coccolithophorids is correlated with the nutricline depth, a proxy of nutrient supply to the upper mixed layer of the ocean. Using this analysis in conjunction with a coupled atmosphere–ocean intermediate complexity model, we predict a dramatic reduction in the nutrient supply to the euphotic layer in the coming century as a result of increased thermal stratification. Our findings indicate that, by altering phytoplankton community composition, this causal relationship may lead to a decreased efficiency of the biological pump in sequestering atmospheric CO2, implying a positive feedback in the climate system. These results provide a mechanistic basis for understanding the connection between upper ocean dynamics, the calcium carbonate-to-organic C production ratio and atmospheric pCO2 variations on time scales ranging from seasonal cycles to geological transitions.

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.

Controls on Diatom Biogeography in the Ocean

Monitoring Massive Microbial Dispersal Quantifying the relative influence of present-day environmental conditions and geological history on the spatial distribution of species represents a major challenge in microbial ecology. Ecological approaches to distinguish between these two biogeographic controls are limited by environmental variability both in space and through time (see the Perspective by Patterson). Using a 1.5-million-year fossil record of marine diatoms, Cermeño and Falkowski (p. 1539) show that, even at the largest (global) spatial scale, the dispersal of marine diatoms is not very limited. Environmental factors are the primary control shaping the global biogeography of marine diatom morphospecies. Thermophilic microorganisms are routinely detected in permanently cold environments from deep sea sediments to polar soils. Hubert et al. (p. 1541) provide a quantitative analysis of a potentially large-scale dispersion of thermophilic bacteria in the ocean. Approximately 108 thermophilic spores are deposited each year on every square meter of Arctic sediment. Fossil records show that the dispersal of diatoms from ocean plankton has not been constrained by geographical barriers. The extent to which the spatial distribution of marine planktonic microbes is controlled by local environmental selection or dispersal is poorly understood. Our ability to separate the effects of these two biogeographic controls is limited by the enormous environmental variability both in space and through time. To circumvent this limitation, we analyzed fossil diatom assemblages over the past ~1.5 million years from the world oceans and show that these eukaryotic microbes are not limited by dispersal. The lack of dispersal limitation in marine diatoms suggests that the biodiversity at the microbial level fundamentally differs from that of macroscopic animals and plants for which geographic isolation is a common component of speciation.

Global relationship between phytoplankton diversity and productivity in the ocean

The shape of the productivity–diversity relationship (PDR) for marine phytoplankton has been suggested to be unimodal, that is, diversity peaking at intermediate levels of productivity. However, there are few observations and there has been little attempt to understand the mechanisms that would lead to such a shape for planktonic organisms. Here we use a marine ecosystem model together with the community assembly theory to explain the shape of the unimodal PDR we obtain at the global scale. The positive slope from low to intermediate productivity is due to grazer control with selective feeding, which leads to the predator-mediated coexistence of prey. The negative slope at high productivity is due to seasonal blooms of opportunist species that occur before they are regulated by grazers. The negative side is only unveiled when the temporal scale of the observation captures the transient dynamics, which are especially relevant at highly seasonal latitudes. Thus selective predation explains the positive side while transient competitive exclusion explains the negative side of the unimodal PDR curve. The phytoplankton community composition of the positive and negative sides is mostly dominated by slow-growing nutrient specialists and fast-growing nutrient opportunist species, respectively.

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.

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 Biogeography and Community Stability in the Ocean

Background Despite enormous environmental variability linked to glacial/interglacial climates of the Pleistocene, we have recently shown that marine diatom communities evolved slowly through gradual changes over the past 1.5 million years. Identifying the causes of this ecological stability is key for understanding the mechanisms that control the tempo and mode of community evolution. Methodology/Principal Findings If community assembly were controlled by local environmental selection rather than dispersal, environmental perturbations would change community composition, yet, this could revert once environmental conditions returned to previous-like states. We analyzed phytoplankton community composition across >104 km latitudinal transects in the Atlantic Ocean and show that local environmental selection of broadly dispersed species primarily controls community structure. Consistent with these results, three independent fossil records of marine diatoms over the past 250,000 years show cycles of community departure and recovery tightly synchronized with the temporal variations in Earths climate. Conclusions/Significance Changes in habitat conditions dramatically alter community structure, yet, we conclude that the high dispersal of marine planktonic microbes erases the legacy of past environmental conditions, thereby decreasing the tempo of community evolution.

Continental erosion and the Cenozoic rise of marine diatoms

Significance Diatoms are silica-precipitating microalgae responsible for roughly one-fifth of global primary production. The mechanisms that led these microorganisms to become one of the most prominent primary producers on Earth remain unclear. We explore the linkage between the erosion of continental silicates and the ecological success of marine diatoms over the last 40 My. We show that the diversification and geographic expansion of diatoms coincide with periods of increased continental weathering fluxes and silicic acid input to the oceans. On geological time scales, the ocean’s biologically driven sequestration of organic carbon (the biological pump) is proportional to the input flux of inorganic nutrients to the oceans. Our results suggest that the strength and efficiency of the biological pump increased over geological time. Marine diatoms are silica-precipitating microalgae that account for over half of organic carbon burial in marine sediments and thus they play a key role in the global carbon cycle. Their evolutionary expansion during the Cenozoic era (66 Ma to present) has been associated with a superior competitive ability for silicic acid relative to other siliceous plankton such as radiolarians, which evolved by reducing the weight of their silica test. Here we use a mathematical model in which diatoms and radiolarians compete for silicic acid to show that the observed reduction in the weight of radiolarian tests is insufficient to explain the rise of diatoms. Using the lithium isotope record of seawater as a proxy of silicate rock weathering and erosion, we calculate changes in the input flux of silicic acid to the oceans. Our results indicate that the long-term massive erosion of continental silicates was critical to the subsequent success of diatoms in marine ecosystems over the last 40 My and suggest an increase in the strength and efficiency of the oceanic biological pump over this period.

Surface distribution of dissolved trace metals in the oligotrophic ocean and their influence on phytoplankton biomass and productivity

The distribution of bioactive trace metals has the potential to enhance or limit primary productivity and carbon export in some regions of the world ocean. To study these connections, the concentrations of Cd, Co, Cu, Fe, Mo, Ni, and V were determined for 110 surface water samples collected during the Malaspina 2010 Circumnavigation Expedition (MCE). Total dissolved Cd, Co, Cu, Fe, Mo, Ni, and V concentrations averaged 19.0 ± 5.4 pM, 21.4 ± 12 pM, 0.91 ± 0.4 nM, 0.66 ± 0.3 nM, 88.8 ± 12 nM, 1.72 ± 0.4 nM, and 23.4 ± 4.4 nM, respectively, with the lowest values detected in the Central Pacific and increased values at the extremes of all transects near coastal zones. Trace metal concentrations measured in surface waters of the Atlantic Ocean during the MCE were compared to previously published data for the same region. The comparison revealed little temporal changes in the distribution of Cd, Co, Cu, Fe, and Ni over the last 30 years. We utilized a multivariable linear regression model to describe potential relationships between primary productivity and the hydrological, biological, trace nutrient and macronutrient data collected during the MCE. Our statistical analysis shows that primary productivity in the Indian Ocean is best described by chlorophyll a, NO3, Ni, temperature, SiO4, and Cd. In the Atlantic Ocean, primary productivity is correlated with chlorophyll a, NO3, PO4, mixed layer depth, Co, Fe, Cd, Cu, V, and Mo. The variables salinity, temperature, SiO4, NO3, PO4, Fe, Cd, and V were found to best predict primary productivity in the Pacific Ocean. These results suggest that some of the lesser studied trace elements (e.g., Ni, V, Mo, and Cd) may play a more important role in regulating oceanic primary productivity than previously thought and point to the need for future experiments to verify their potential biological functions.

Differential response of microbial plankton to nutrient inputs in oligotrophic versus mesotrophic waters of the North Atlantic

Abstract The effects of inorganic and/or organic (glucose+AAs) inputs on phytoplankton and heterotrophic bacteria were assessed, using a microcosm approach, in two contrasting marine environments: an open ocean oligotrophic site (North Atlantic Subtropical Gyre) and a highly productive coastal embayment (Ría de Vigo, NW Spain). Overall, changes in microbial plankton biomass were smaller than those of metabolic rates. The largest increases in primary production, bacterial production and community respiration were measured in response to mixed ( ) nutrient additions in both sites. Primary production responded to additions only in oligotrophic waters. The distinct autotrophic responses to nutrient additions measured in these environments were related to the different initial composition of phytoplankton populations and, presumably, also to differences in grazing pressures in both marine ecosystems. Heterotrophic bacteria were limited by organic substrates in both ecosystems, although mixed additions further enhanced bacterial growth in the subtropical gyre. The differences detected in bacterial responses to nutrient additions may be related to differences in nutrient limitations and to the prevalence of different relationships between components of the microbial food web (e.g. coupling between heterotrophic bacteria and phytoplankton and predation pressure) in both environments. We found a more relevant role of inorganic nutrients in controlling the efficiency of bacterial growth in oligotrophic regions as compared with highly productive systems. Our results suggest that organic matter inputs into both ecosystems might result in a tendency towards heterotrophy and in increases in bacterial growth efficiency.