Taxonomy and morphology of Calciopappus curvus sp. nov. (Syracosphaeraceae, Prymnesiophyceae), a novel appendage-bearing coccolithophore.

Based on scanning electron microscopy observations, a new species of the coccolithophore genus Calciopappus (Syracosphaeraceae, Prymnesiophyceae) is described from the surface waters off Bergen and from the lower photic zone of sub-tropical and tropical waters. Morphological, coccolith rim structure and biometric analyses strongly support separation of this morphotype from the two described Calciopappus species, but inclusion of it within the genus. The new form differs from the other species in being noticeably smaller and in morpho-structural details of each of the three coccolith types that form the coccosphere: (1) the body coccoliths have an open central area; (2) the whorl coccoliths have a wide central opening and two thumb-like protrusions; and (3) the appendage coccoliths are curved. On this basis, the species is formally described as Calciopappus curvus sp. nov., its systematic affinity is discussed and compared with other extant coccolithophores.

Rapid diversification underlying the global dominance of a cosmopolitan phytoplankton.

Marine phytoplankton play important roles in the global ecosystem, with a limited number of cosmopolitan keystone species driving their biomass. Recent studies have revealed that many of these phytoplankton are complexes composed of sibling species, but little is known about the evolutionary processes underlying their formation. Gephyrocapsa huxleyi, a widely distributed and abundant unicellular marine planktonic algae, produces calcified scales (coccoliths), thereby significantly affects global biogeochemical cycles via sequestration of inorganic carbon. This species is composed of morphotypes defined by differing degrees of coccolith calcification, the evolutionary ecology of which remains unclear. Here, we report an integrated morphological, ecological and genomic survey across globally distributed G. huxleyi strains to reconstruct evolutionary relationships between morphotypes in relation to their habitats. While G. huxleyi has been considered a single cosmopolitan species, our analyses demonstrate that it has evolved to comprise at least three distinct species, which led us to formally revise the taxonomy of the G. huxleyi complex. Moreover, the first speciation event occurred before the onset of the last interglacial period (~140 ka), while the second followed during this interglacial. Then, further rapid diversifications occurred during the most recent ice-sheet expansion of the last glacial period and established morphotypes as dominant populations across environmental clines. These results suggest that glacial-cycle dynamics contributed to the isolation of ocean basins and the segregations of oceans fronts as extrinsic drivers of micro-evolutionary radiations in extant marine phytoplankton.

Triton, a new species-level database of Cenozoic planktonic foraminiferal occurrences.

Planktonic foraminifera are a major constituent of ocean floor sediments, and thus have one of the most complete fossil records of any organism. Expeditions to sample these sediments have produced large amounts of spatiotemporal occurrence records throughout the Cenozoic, but no single source exists to house these data. We have therefore created a comprehensive dataset that integrates numerous sources for spatiotemporal records of planktonic foraminifera. This new dataset, Triton, contains >500,000 records and is four times larger than the previous largest database, Neptune. To ensure comparability among data sources, we have cleaned all records using a unified set of taxonomic concepts and have converted age data to the GTS 2020 timescale. Where ages were not absolute (e.g. based on biostratigraphic or magnetostratigraphic zones), we have used generalised additive models to produce continuous estimates. This dataset is an excellent resource for macroecological and macroevolutionary studies, particularly for investigating how species responded to past climatic changes.

Dataset of characteristic remanent magnetization and magnetic properties of early Pliocene sediments from IODP Site U1467 (Maldives platform).

This data article describes data of magnetic stratigraphy and anisotropy of isothermal remanent magnetization (AIRM) from "Magnetic properties of early Pliocene sediments from IODP Site U1467 (Maldives platform) reveal changes in the monsoon system" [1]. Acquisition of isothermal magnetization on pilot samples and anisotropy of isothermal remanent magnetization are reported as raw data; magnetostratigraphic data are reported as characteristic magnetization (ChRM).

Repeated species radiations in the recent evolution of the key marine phytoplankton lineage Gephyrocapsa.

Phytoplankton account for nearly half of global primary productivity and strongly affect the global carbon cycle, yet little is known about the forces that drive the evolution of these keystone microscopic organisms. Here we combine morphometric data from the fossil record of the ubiquitous coccolithophore genus Gephyrocapsa with genomic analyses of extant species to assess the genetic processes underlying Pleistocene palaeontological patterns. We demonstrate that all modern diversity in Gephyrocapsa (including Emiliania huxleyi) originated in a rapid species radiation during the last 0.6 Ma, coincident with the latest of the three pulses of Gephyrocapsa diversification and extinction documented in the fossil record. Our evolutionary genetic analyses indicate that new species in this genus have formed in sympatry or parapatry, with occasional hybridisation between species. This sheds light on the mode of speciation during evolutionary radiation of marine phytoplankton and provides a model of how new plankton species form.

Time-calibrated molecular phylogeny of pteropods.

Pteropods are a widespread group of holoplanktonic gastropod molluscs and are uniquely suitable for study of long-term evolutionary processes in the open ocean because they are the only living metazoan plankton with a good fossil record. Pteropods have been proposed as bioindicators to monitor the impacts of ocean acidification and in consequence have attracted considerable research interest, however, a robust evolutionary framework for the group is still lacking. Here we reconstruct their phylogenetic relationships and examine the evolutionary history of pteropods based on combined analyses of Cytochrome Oxidase I, 28S, and 18S ribosomal rRNA sequences and a molecular clock calibrated using fossils and the estimated timing of the formation of the Isthmus of Panama. Euthecosomes with uncoiled shells were monophyletic with Creseis as the earliest diverging lineage, estimated at 41-38 million years ago (mya). The coiled euthecosomes (Limacina, Heliconoides, Thielea) were not monophyletic contrary to the accepted morphology-based taxonomy; however, due to their high rate heterogeneity no firm conclusions can be drawn. We found strong support for monophyly of most euthecosome genera, but Clio appeared as a polyphyletic group, and Diacavolinia grouped within Cavolinia, making the latter genus paraphyletic. The highest evolutionary rates were observed in Heliconoides inflatus and Limacina bulimoides for both 28S and 18S partitions. Using a fossil-calibrated phylogeny that sets the first occurrence of coiled euthecosomes at 79-66 mya, we estimate that uncoiled euthecosomes evolved 51-42 mya and that most extant uncoiled genera originated 40-15 mya. These findings are congruent with a molecular clock analysis using the Isthmus of Panama formation as an independent calibration. Although not all phylogenetic relationships could be resolved based on three molecular markers, this study provides a useful resource to study pteropod diversity and provides general insight into the processes that generate and maintain their diversity in the open ocean.

The abrupt onset of the modern South Asian Monsoon winds.

The South Asian Monson (SAM) is one of the most intense climatic elements yet its initiation and variations are not well established. Dating the deposits of SAM wind-driven currents in IODP cores from the Maldives yields an age of 12. 9 Ma indicating an abrupt SAM onset, over a short period of 300 kyrs. This coincided with the Indian Ocean Oxygen Minimum Zone expansion as revealed by geochemical tracers and the onset of upwelling reflected by the sediment's content of particulate organic matter. A weaker 'proto-monsoon' existed between 12.9 and 25 Ma, as mirrored by the sedimentary signature of dust influx. Abrupt SAM initiation favors a strong influence of climate in addition to the tectonic control, and we propose that the post Miocene Climate Optimum cooling, together with increased continentalization and establishment of the bipolar ocean circulation, i.e. the beginning of the modern world, shifted the monsoon over a threshold towards the modern system.

Recent Reticulate Evolution in the Ecologically Dominant Lineage of Coccolithophores.

The coccolithophore family Noëlaerhabdaceae contains a number of taxa that are very abundant in modern oceans, including the cosmopolitan bloom-forming Emiliania huxleyi. Introgressive hybridization has been suggested to account for incongruences between nuclear, mitochondrial and plastidial phylogenies of morphospecies within this lineage, but the number of species cultured to date remains rather limited. Here, we present the characterization of 5 new Noëlaerhabdaceae culture strains isolated from samples collected in the south-east Pacific Ocean. These were analyzed morphologically using scanning electron microscopy and phylogenetically by sequencing 5 marker genes (nuclear 18S and 28S rDNA, plastidial tufA, and mitochondrial cox1 and cox3 genes). Morphologically, one of these strains corresponded to Gephyrocapsa ericsonii and the four others to Reticulofenestra parvula. Ribosomal gene sequences were near identical between these new strains, but divergent from G. oceanica, G. muellerae, and E. huxleyi. In contrast to the clear distinction in ribosomal phylogenies, sequences from other genomic compartments clustered with those of E. huxleyi strains with which they share an ecological range (i.e., warm temperate to tropical waters). These data provide strong support for the hypothesis of past (and potentially ongoing) introgressive hybridization within this ecologically important lineage and for the transfer of R. parvula to Gephyrocapsa. These results have important implications for understanding the role of hybridization in speciation in vast ocean meta-populations of phytoplankton.

Morphological and Phylogenetic Characterization of New Gephyrocapsa Isolates Suggests Introgressive Hybridization in the Emiliania/Gephyrocapsa Complex (Haptophyta).

The coccolithophore genus Gephyrocapsa contains a cosmopolitan assemblage of pelagic species, including the bloom-forming Gephyrocapsa oceanica, and is closely related to the emblematic coccolithophore Emiliania huxleyi within the Noëlaerhabdaceae. These two species have been extensively studied and are well represented in culture collections, whereas cultures of other species of this family are lacking. We report on three new strains of Gephyrocapsa isolated into culture from samples from the Chilean coastal upwelling zone using a novel flow cytometric single-cell sorting technique. The strains were characterized by morphological analysis using scanning electron microscopy and phylogenetic analysis of 6 genes (nuclear 18S and 28S rDNA, plastidial 16S and tufA, and mitochondrial cox1 and cox3 genes). Morphometric features of the coccoliths indicate that these isolates are distinct from G. oceanica and best correspond to G. muellerae. Surprisingly, both plastidial and mitochondrial gene phylogenies placed these strains within the E. huxleyi clade and well separated from G. oceanica isolates, making Emiliania appear polyphyletic. The only nuclear sequence difference, 1bp in the 28S rDNA region, also grouped E. huxleyi with the new Gephyrocapsa isolates and apart from G. oceanica. Specifically, the G. muellerae morphotype strains clustered with the mitochondrial ß clade of E. huxleyi, which, like G. muellerae, has been associated with cold (temperate and sub-polar) waters. Among putative evolutionary scenarios that could explain these results we discuss the possibility that E. huxleyi is not a valid taxonomic unit, or, alternatively the possibility of past hybridization and introgression between each E. huxleyi clade and older Gephyrocapsa clades. In either case, the results support the transfer of Emiliania to Gephyrocapsa. These results have important implications for relating morphological species concepts to ecological and evolutionary units of diversity.

Coccolithophore calcification response to past ocean acidification and climate change.

Anthropogenic carbon dioxide emissions are forcing rapid ocean chemistry changes and causing ocean acidification (OA), which is of particular significance for calcifying organisms, including planktonic coccolithophores. Detailed analysis of coccolithophore skeletons enables comparison of calcite production in modern and fossil cells in order to investigate biomineralization response of ancient coccolithophores to climate change. Here we show that the two dominant coccolithophore taxa across the Paleocene-Eocene Thermal Maximum (PETM) OA global warming event (~56 million years ago) exhibited morphological response to environmental change and both showed reduced calcification rates. However, only Coccolithus pelagicus exhibits a transient thinning of coccoliths, immediately before the PETM, that may have been OA-induced. Changing coccolith thickness may affect calcite production more significantly in the dominant modern species Emiliania huxleyi, but, overall, these PETM records indicate that the environmental factors that govern taxonomic composition and growth rate will most strongly influence coccolithophore calcification response to anthropogenic change.

Responses of the Emiliania huxleyi proteome to ocean acidification.

Ocean acidification due to rising atmospheric CO2 is expected to affect the physiology of important calcifying marine organisms, but the nature and magnitude of change is yet to be established. In coccolithophores, different species and strains display varying calcification responses to ocean acidification, but the underlying biochemical properties remain unknown. We employed an approach combining tandem mass-spectrometry with isobaric tagging (iTRAQ) and multiple database searching to identify proteins that were differentially expressed in cells of the marine coccolithophore species Emiliania huxleyi (strain NZEH) between two CO2 conditions: 395 (∼current day) and ∼1340 p.p.m.v. CO2. Cells exposed to the higher CO2 condition contained more cellular particulate inorganic carbon (CaCO3) and particulate organic nitrogen and carbon than those maintained in present-day conditions. These results are linked with the observation that cells grew slower under elevated CO2, indicating cell cycle disruption. Under high CO2 conditions, coccospheres were larger and cells possessed bigger coccoliths that did not show any signs of malformation compared to those from cells grown under present-day CO2 levels. No differences in calcification rate, particulate organic carbon production or cellular organic carbon: nitrogen ratios were observed. Results were not related to nutrient limitation or acclimation status of cells. At least 46 homologous protein groups from a variety of functional processes were quantified in these experiments, of which four (histones H2A, H3, H4 and a chloroplastic 30S ribosomal protein S7) showed down-regulation in all replicates exposed to high CO2, perhaps reflecting the decrease in growth rate. We present evidence of cellular stress responses but proteins associated with many key metabolic processes remained unaltered. Our results therefore suggest that this E. huxleyi strain possesses some acclimation mechanisms to tolerate future CO2 scenarios, although the observed decline in growth rate may be an overriding factor affecting the success of this ecotype in future oceans.

Taxonomic structure of the fossil record is shaped by sampling bias.

Understanding biases that affect how species are partitioned into higher taxa is critical for much of paleobiology, as higher taxa are commonly used to estimate species diversity through time. We test the validity of using higher taxa as a proxy for species diversity for the first time by examining one of the best fossil records we have, that of deep-sea microfossils. Using a new, taxonomically standardized, data set of coccolithophorid species and genera recorded from 143 deep-sea drilling sites in the North Atlantic, Caribbean, and Mediterranean, we show that there is a two-stepped change in the ratio of species to genera over the last 150 myr. This change is highly unexpected and correlates strongly with changes in both the number of deep-sea sites yielding coccolithophorids that have been studied and with the number of taxonomists who have published on those sections. The same pattern is present in both structurally complex heterococcoliths and the simpler nannoliths, suggesting that increasing complexity is not the driving factor. As a stepped species-to-genus ratio exists even after subsampling to standardize either the numbers of sites or numbers of papers, both factors must be contributing substantially to the observed pattern. Although some limited biological signature from major extinction events can be recognized from changes in the species-to-genus ratio, the numbers of sites and the numbers of taxonomists combined explain some 82% of the observed variation over long periods of geological time. Such a strong correlation argues against using raw species-to-genus ratios to infer biological processes without taking sampling into account and suggests that higher taxa cannot be taken as unbiased proxies for species diversity.

The future of the past in the present: biodiversity informatics and geological time.

The biological and palaeontological communities have approached the problem of informatics separately, creating a divide between communities that is both technological and sociological in nature. In this paper we describe one new advance towards solving this problem - expanding the Scratchpads platform to deal with geological time. In creating this system we have attempted to make our work open to existing communities by providing a webservice of geological time data via the GBIF Vocabularies site. We have also ensured that our system can adapt to changes in the definition of geological time intervals and is capable of querying datasets independently of the format of geological age data used.

NEW EVIDENCE FOR MORPHOLOGICAL AND GENETIC VARIATION IN THE COSMOPOLITAN COCCOLITHOPHORE EMILIANIA HUXLEYI (PRYMNESIOPHYCEAE) FROM THE COX1b-ATP4 GENES(1).

Emiliania huxleyi (Lohmann) W. W. Hay et H. Mohler is a cosmopolitan coccolithophore occurring from tropical to subpolar waters and exhibiting variations in morphology of coccoliths possibly related to environmental conditions. We examined morphological characters of coccoliths and partial mitochondrial sequences of the cytochrome oxidase 1b (cox1b) through adenosine triphosphate synthase 4 (atp4) genes of 39 clonal E. huxleyi strains from the Atlantic and Pacific Oceans, Mediterranean Sea, and their adjacent seas. Based on the morphological study of culture strains by SEM, Type O, a new morphotype characterized by coccoliths with an open central area, was separated from existing morphotypes A, B, B/C, C, R, and var. corona, characterized by coccoliths with central area elements. Molecular phylogenetic studies revealed that E. huxleyi consists of at least two mitochondrial sequence groups with different temperature preferences/tolerances: a cool-water group occurring in subarctic North Atlantic and Pacific and a warm-water group occurring in the subtropical Atlantic and Pacific and in the Mediterranean Sea.

NO MECHANISTIC DEPENDENCE OF PHOTOSYNTHESIS ON CALCIFICATION IN THE COCCOLITHOPHORID EMILIANIA HUXLEYI (HAPTOPHYTA)(1).

There is still considerable uncertainty about the relationship between calcification and photosynthesis. It has been suggested that since calcification in coccolithophorids is an intracellular process that releases CO2 , it enhances photosynthesis in a manner analogous to a carbon-concentrating mechanism (CCM). The ubiquitous, bloom-forming, and numerically abundant coccolithophorid Emiliania huxleyi (Lohmann) W. W. Hay et H. Mohler was studied in nutrient-replete, pH and [CO2 ] controlled, continuous cultures (turbidostats) under a range of [Ca(2+) ] from 0 to 9 mM. We examined the long-term, fully acclimated photosynthesis-light responses and analyzed the crystalline structure of the coccoliths using SEM. The E. huxleyi cells completely lost their coccosphere when grown in 0 [Ca(2+) ], while thin, undercalcified and brittle coccoliths were evident at 1 mM [Ca(2+) ]. Coccoliths showed increasing levels of calcification with increasing [Ca(2+) ]. More robust coccoliths were noted, with no discernable differences in coccolith morphology when the cells were grown in either 5 or 9 mM (ambient seawater) [Ca(2+) ]. In contrast to calcification, photosynthesis was not affected by the [Ca(2+) ] in the media. Cells showed no correlation of their light-dependent O2 evolution with [Ca(2+) ], and in all [Ca(2+) ]-containing turbidostats, there were no significant differences in growth rate. The results show unequivocally that as a process, photosynthesis in E. huxleyi is mechanistically independent from calcification.

COCCOLITH FUNCTION AND MORPHOGENESIS: INSIGHTS FROM APPENDAGE-BEARING COCCOLITHOPHORES OF THE FAMILY SYRACOSPHAERACEAE (HAPTOPHYTA)(1).

The morphology of three remarkable genera of coccolithophores, Ophiaster, Michaelsarsia, and Calciopappus, is reviewed based on new images using field emission scanning electron microscopy. Each of these genera characteristically forms coccospheres with long appendages formed of highly modified coccoliths, which radiate from either the circum-flagellar pole of the coccosphere (Calciopappus and Michaelsarsia) or the antapical pole (Ophiaster). For each genus, it is shown that the appendage coccoliths can also occur in an alternative orientation appressed to the main coccosphere. It is hypothesized that the appendage coccoliths are initially deployed in the appressed orientation and that extension of the appendages is a dynamic response to environmental stress. The observations suggest that coccoliths are more sophisticatedly adapted to specific functions than has been assumed and that the cytoskeleton plays more active roles in coccolith morphogenesis and deployment than has previously been inferred.

Pseudo-cryptic speciation in coccolithophores.

Coccolithophores are a group of calcifying unicellular algae that constitute a major fraction of oceanic primary productivity, play an important role in the global carbon cycle, and are key biostratigraphic marker fossils. Their taxonomy is primarily based on the morphology of the minute calcite plates, or coccoliths, covering the cell. These are diverse and include widespread fine scale variation, of which the biological/taxonomic significance is unknown. Do they represent phenotypic plasticity, genetic polymorphisms, or species-specific characters? Our research on five commonly occurring coccolithophores supports the hypothesis that such variation represents pseudocryptic speciation events, occurring between 0.3 and 12.9 million years ago from a molecular clock estimation. This finding suggests strong stabilizing selection acting on coccolithophorid phenotypes. Our results also provide strong support for the use of fine scale morphological characters of coccoliths in the fossil record to improve biostratigraphic resolution and paleoceanographic data retrieval.

Potential and limitations of Sr/Ca ratios in coccolith carbonate: new perspectives from cultures and monospecific samples from sediments.

The Sr/Ca ratio of coccoliths was recently proposed as a potential indicator of past growth rates of coccolithophorids, marine algae, which play key roles in both the global carbonate and carbon cycles. We synthesize calibrations of this proxy through laboratory culture studies and analysis of monospecific coccolith assemblages from surface sediments. Cultures of coccolithophorids Helicosphaera carteri, Syracosphaera pulchra and Algirospira robusta confirm a 1-2% increase in Sr/Ca per degrees C previously identified in Emiliania huxleyi and Gephyrocapsa oceanica. This effect is not due merely to increases in growth rate with temperature and must be considered in palaeoceanographic studies. In light-limited cultures of E. huxleyi, Calcidiscus leptoporus and G. oceanica at constant temperature, coccolith Sr/Ca ratios vary by 10% across the range of possible growth and calcification rates for a given species. Among different species under similar culture conditions, Sr/Ca ratios vary by 30%. Although the highest ratios are in the cells with highest calcification and organic carbon fixation rates, at lower rates there is much scatter, indicating that different mechanisms control interspecific and intraspecific coccolith Sr/Ca variations. In field studies in the Equatorial Pacific and Somalia coastal region, coccolith Sr/Ca correlates with upwelling intensity and productivity. A more dynamic response is observed in larger coccoliths like C. leptoporus (23-55% variation in Sr/Ca) than in smaller coccoliths of G. oceanica or Florisphaera profunda (6-15% variation in Sr/Ca). This response suggests that, despite temperature effects, coccolith Sr/Ca has potential as an indicator of coccolithophorid productivity. If the variable Sr/Ca response of different species accurately reflects their variable productivity response to upwelling (and not different slopes of Sr/Ca with productivity), coccolith Sr/Ca could provide useful data on past changes in coccolith ecology. The mechanism of coccolith Sr/Ca variations remains poorly understood but is probably more closely tied to biochemical cycles during carbon acquisition than to chemical kinetic effects on Sr incorporation in the calcite coccolith crystals.