Post-extinction recovery of the Phanerozoic oceans and biodiversity hotspots.

The fossil record of marine invertebrates has long fuelled the debate as to whether or not there are limits to global diversity in the sea1-5. Ecological theory states that, as diversity grows and ecological niches are filled, the strengthening of biological interactions imposes limits on diversity6,7. However, the extent to which biological interactions have constrained the growth of diversity over evolutionary time remains an open question1-5,8-11. Here we present a regional diversification model that reproduces the main Phanerozoic eon trends in the global diversity of marine invertebrates after imposing mass extinctions. We find that the dynamics of global diversity are best described by a diversification model that operates widely within the exponential growth regime of a logistic function. A spatially resolved analysis of the ratio of diversity to carrying capacity reveals that less than 2% of the global flooded continental area throughout the Phanerozoic exhibits diversity levels approaching ecological saturation. We attribute the overall increase in global diversity during the Late Mesozoic and Cenozoic eras to the development of diversity hotspots under prolonged conditions of Earth system stability and maximum continental fragmentation. We call this the 'diversity hotspots hypothesis', which we propose as a non-mutually exclusive alternative to the hypothesis that the Mesozoic marine revolution led this macroevolutionary trend12,13.

Continental erosion and the Cenozoic rise of marine diatoms.

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.

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.

Marine planktonic microbes survived climatic instabilities in the past.

In the geological past, changes in climate and tectonic activity are thought to have spurred the tempo of evolutionary change among major taxonomic groups of plants and animals. However, the extent to which these historical contingencies increased the risk of extinction of microbial plankton species remains largely unknown. Here, I analyse fossil records of marine planktonic diatoms and calcareous nannoplankton over the past 65 million years from the world oceans and show that the probability of species' extinction is not correlated with secular changes in climatic instability. Further supporting these results, analyses of genera survivorship curves based on fossil data concurred with the predictions of a birth-death model that simulates the extinction of genera through time assuming stochastically constant rates of speciation and extinction. However, my results also show that these marine microbes responded to exceptional climatic contingencies in a manner that appears to have promoted net diversification. These results highlight the ability of marine planktonic microbes to survive climatic instabilities in the geological past, and point to different mechanisms underlying the processes of speciation and extinction in these micro-organisms.

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 Kleiber's 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.

Particulate and dissolved fluorescent organic matter fractionation and composition: Abiotic and ecological controls in the Southern Ocean.

Phytoplankton-derived organic matter sustains heterotrophic marine life in regions away from terrestrial inputs such as the Southern Ocean. Fluorescence spectroscopy has long been used to characterize the fluorescent organic matter (FOM) pool. However, most studies focus only in the dissolved FOM fraction (FDOM) disregarding the contribution of particles. In order to assess the dynamics and drivers of the dissolved and particulate fractions of FOM, we used a Lagrangian approach to follow the time evolution of phytoplankton proliferations at four different sites in the Southern Ocean and compared the FOM in filtered and unfiltered seawater aliquots. We found that filtration had little effects on FOM visible spectrum fluorescence intensities, implying that most of this signal was due to dissolved fluorophores. On the other hand, protein-like fluorescence was strongly supressed by filtration, with fluorescence of particles accounting for up to 90 % of the total protein-like FOM. Photobleaching was identified as the main driver of visible FDOM composition, which was better described by indices of phytoplankton photoacclimation than by measurements of the incident solar radiation dose. In contrast, protein-like FOM intensity and fractionation were primarily related to abundance, composition and physiological state of phytoplankton proliferations. The chlorophyll a concentration from non-diatom phytoplankton explained 91 % of the particulate protein-like FOM variability. The proportion of protein-like fluorescence found in the dissolved phase was predicted by the combination of potential viral and grazing pressures, which accounted for 51 and 29 % of its variability, respectively. Our results show that comparing FOM measurements from filtered and unfiltered seawater provides relevant information on the taxonomic composition and cell integrity of phytoplankton communities. A better understanding of the commonly overlooked FOM fractionation process is essential for the implementation of in situ fluorescence sensors and will also help us better understand the processes that govern OM cycling in marine systems.

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 (pCO(2)) in the upper ocean and facilitates the diffusive drawdown of atmospheric CO(2). Conversely, precipitation of calcium carbonate by marine planktonic calcifiers such as coccolithophorids increases pCO(2) and promotes its outgassing (i.e., the "alkalinity pump"). Over the past approximately 100 million years, these two carbon fluxes have been modulated by the relative abundance of diatoms and coccolithophores, resulting in biological feedback on atmospheric CO(2) and Earth's 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 CO(2), 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 pCO(2) variations on time scales ranging from seasonal cycles to geological transitions.

Energetic equivalence underpins the size structure of tree and phytoplankton communities.

The size structure of autotroph communities - the relative abundance of small vs. large individuals - shapes the functioning of ecosystems. Whether common mechanisms underpin the size structure of unicellular and multicellular autotrophs is, however, unknown. Using a global data compilation, we show that individual body masses in tree and phytoplankton communities follow power-law distributions and that the average exponents of these individual size distributions (ISD) differ. Phytoplankton communities are characterized by an average ISD exponent consistent with three-quarter-power scaling of metabolism with body mass and equivalence in energy use among mass classes. Tree communities deviate from this pattern in a manner consistent with equivalence in energy use among diameter size classes. Our findings suggest that whilst universal metabolic constraints ultimately underlie the emergent size structure of autotroph communities, divergent aspects of body size (volumetric vs. linear dimensions) shape the ecological outcome of metabolic scaling in forest vs. pelagic ecosystems.

Nutrient limitation suppresses the temperature dependence of phytoplankton metabolic rates.

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, Ea) of metabolism under different degrees of nitrogen (N) limitation. We show that both CO2 fixation and respiration rates increase with N supply but are largely insensitive to temperature. Ea of photosynthesis (0.11 ± 0.06 eV, mean ± SE) and respiration (0.04 ± 0.17 eV) under N-limited growth is significantly smaller than Ea 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.

Identification of flavonoid diglycosides in several genotypes of asparagus from the Huétor-Tájar population variety.

The qualitative and quantitative composition of flavonoids from the Huétor-Tájar population variety of asparagus (commonly known as " triguero") was investigated. Flavonoids were analyzed by reversed-phase high-performance liquid chromatography-diode array detection (HPLC-DAD). Liquid chromatography-mass spectrometry (LC-MS) under identical HPLC conditions was used to verify the identities of the flavonoid glycosides from triguero asparagus. The quantities of asparagus flavonoids were calculated according to concentration curves constructed with authentic standards. Total flavonoid contents, calculated as the sum of individual compounds, were determined and ranged from 400 to 700 mg/kg fresh weight. The most abundant was rutin, which represented 55-98% of the total flavonoid complement. Triguero asparagus were revealed to be an important source of not only quercetin derivatives but also kaempferol and isorhamnetin glycosides. Significant differences (p < 0.05) in the content and relative composition of flavonoids were found among the spears of the distinct asparagus genotypes from the Huétor-Tájar population variety.

Trophic and tectonic limits to the global increase of marine invertebrate diversity.

The marine invertebrate fossil record provides the most comprehensive history of how the diversity of animal life has evolved through time. One of the main features of this record is a modest rise in diversity over nearly a half-billion years. The long-standing view is that ecological interactions such as resource competition and predation set upper limits to global diversity, which, in the absence of external perturbations, is maintained indefinitely at equilibrium. However, the effect of mechanisms associated with the history of the seafloor, and their influence on the creation and destruction of marine benthic habitats, has not been explored. Here we use statistical methods for causal inference to investigate the drivers of marine invertebrate diversity dynamics through the Phanerozoic. We find that diversity dynamics responded to secular variations in marine food supply, substantiating the idea that global species richness is regulated by resource availability. Once diversity was corrected for changes in food resource availability, its dynamics were causally linked to the age of the subducting oceanic crust. We suggest that the time elapsed between the formation (at mid-ocean ridges) and destruction (at subduction zones) of ocean basins influences the diversity dynamics of marine invertebrates and may have contributed to constrain their diversification.

Invariant scaling of phytoplankton abundance and cell size in contrasting marine environments.

Scaling relationships such as the variation of population abundance with body size provide links between individual organisms and ecosystem functioning. Previous work, in marine pelagic ecosystems, has focused on the relationship between total phytoplankton abundance and the assemblage mean cell size. However, the relationship between specific population abundance and cell size in marine phytoplankton has received little attention. Here, we show that cell size accounts for a significant amount of variability in the population abundance of phytoplankton species across a cell volume range spanning seven orders of magnitude. The interspecific scaling of population abundance and cell size takes a power exponent near -3/4. Unexpectedly, despite the constraints imposed on large phytoplankton by limited resource acquisition, the size scaling exponent does not differ between contrasting marine environments such as coastal and subtropical regions. These findings highlight the adaptive abilities of individual species to cope with different environmental conditions and suggest that a general rule such as the 'energetic equivalence' constrains the abundance of phytoplankton populations in marine pelagic 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 >10(4) 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 Earth's 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.

Controls on diatom biogeography in the ocean.

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.