Continuous reproduction of planktonic foraminifera in laboratory culture.

Planktonic foraminifera were long considered obligate sexual outbreeders but recent observations have shown that nonspinose species can reproduce by multiple fission. The frequency of multiple fission appears low but the survival rate of the offspring is high and specimens approaching fission can be distinguished. We made use of this observation and established a culturing protocol aimed at enhancing the detection and frequency of fission. Using this protocol, we selectively cultured specimens of Neogloboquadrina pachyderma and raised the frequency of reproduction by fission in culture from 3% in randomly selected specimens to almost 60%. By feeding the resulting offspring different strains of live diatoms, we obtained a thriving offspring population and during the subsequent 6 months of culturing, we observed two more successive generations produced by fission. This provides evidence that in nonspinose species of planktonic foraminifera, reproduction by multiple fission is likely clonal and corresponds to the schizont phase known from benthic foraminifera. We subsequently tested if a similar culturing strategy could be applied to Globigerinita glutinata, representing a different clade of planktonic foraminifera, and we were indeed able to obtain offspring via multiple fission in this species. This work opens new avenues for laboratory-based experimental work with planktonic foraminifera.

Large-scale culturing of the subpolar foraminifera Globigerina bulloides reveals tolerance to a large range of environmental parameters associated to different life-strategies and an extended lifespan.

The subtropical to subpolar planktic foraminifera Globigerina bulloides is a calcifying marine protist, and one of the dominant foraminiferal species of the Nordic Seas. Previously, the relative abundance and shell geochemistry of fossil G. bulloides have been studied for palaeoceanographic reconstructions. There is however a lack of biological observations on the species and a poor understanding of its ecological tolerances, especially for high latitude genotypes. Here, we present observations from the first extensive culturing of G. bulloides under subpolar conditions, including the first low temperature (6-13°C) and variable salinity (30-38) experiments. Carbonate chemistry (pH and [CO3 2-]) was also manipulated. Experimental conditions were chosen to reflect a range of plausible past and future scenarios for the Nordic Seas. We found G. bulloides to be tolerant of environmental conditions well outside their optimal range (<10°C, salinity <33, pH <8). Observed life span was up to three months, which was attributed to a microalgal diet. Two alternative life strategies were employed, whereby individuals either experienced rapid growth and death, or a prolonged lifespan with minimal growth and death via slow decay. We posit this could help explain differences in geochemical signals recorded from different size fractions of fossil specimens used for palaeoceanographic reconstructions.

The global genetic diversity of planktonic foraminifera reveals the structure of cryptic speciation in plankton.

The nature and extent of diversity in the plankton has fascinated scientists for over a century. Initially, the discovery of many new species in the remarkably uniform and unstructured pelagic environment appeared to challenge the concept of ecological niches. Later, it became obvious that only a fraction of plankton diversity had been formally described, because plankton assemblages are dominated by understudied eukaryotic lineages with small size that lack clearly distinguishable morphological features. The high diversity of the plankton has been confirmed by comprehensive metabarcoding surveys, but interpretation of the underlying molecular taxonomies is hindered by insufficient integration of genetic diversity with morphological taxonomy and ecological observations. Here we use planktonic foraminifera as a study model and reveal the full extent of their genetic diversity and investigate geographical and ecological patterns in their distribution. To this end, we assembled a global data set of ~7600 ribosomal DNA sequences obtained from morphologically characterised individual foraminifera, established a robust molecular taxonomic framework for the observed diversity, and used it to query a global metabarcoding data set covering ~1700 samples with ~2.48 billion reads. This allowed us to extract and assign 1 million reads, enabling characterisation of the structure of the genetic diversity of the group across ~1100 oceanic stations worldwide. Our sampling revealed the existence of, at most, 94 distinct molecular operational taxonomic units (MOTUs) at a level of divergence indicative of biological species. The genetic diversity only doubles the number of formally described species identified by morphological features. Furthermore, we observed that the allocation of genetic diversity to morphospecies is uneven. Only 16 morphospecies disguise evolutionarily significant genetic diversity, and the proportion of morphospecies that show genetic diversity increases poleward. Finally, we observe that MOTUs have a narrower geographic distribution than morphospecies and that in some cases the MOTUs belonging to the same morphospecies (cryptic species) have different environmental preferences. Overall, our analysis reveals that even in the light of global genetic sampling, planktonic foraminifera diversity is modest and finite. However, the extent and structure of the cryptic diversity reveals that genetic diversification is decoupled from morphological diversification, hinting at different mechanisms acting at different levels of divergence.

Uncovering hidden structures: previously undescribed pseudopodia and ectoplasmic structures in planktonic foraminifera.

The trophic strategies of cold-water planktonic foraminifera are not well understood due to the challenge of culturing them in polar conditions. Here, we identify previously unknown ectoplasmic and cytoplasmic projections in three species of planktonic foraminifera thriving in polar and subpolar marine environments: Globigerina bulloides, Neogloboquadrina incompta and Neogloboquadrina pachyderma. These structures were observed during routine monitoring of cultured specimens sampled from the Norwegian coast, Greenland Sea and Baffin Bay. Two types of projections were discovered, including permanent and non-permanent structures such as ectoplasmic roots, twigs and twig-like projections, similar to those observed in benthic taxa Cibicides and Cibicidoides. Additionally, a previously undescribed filopodia-like projection was observed in N. pachyderma. We discuss the function, the ecological significance and the potential impact on pelagic processes of the presence of these structures in foraminifera species that occupy diverse niches in the water column. Our findings suggest that these structures may play an important role in the trophic strategies of cold-water planktonic foraminifera, and further research and observations are necessary to fully comprehend their significance in the carbon cycle.

Collection of X-ray micro computed tomography images of shells of planktic foraminifera with curated taxonomy.

Calcite shells of planktic foraminifera (Protista, Rhizaria) constitute a large portion of deep-sea sediments. The shells are constructed by sequential addition of partly overlapping chambers with diverse shapes, resulting in complex shell architectures, which are genetically fixed and diagnostic at the species level. The characterisation of the complete architecture requires three-dimensional imaging of the shell, including the partially or entirely covered juvenile chambers. Here we provide reconstructed x-ray micro computed tomography image stacks of 179 specimens of extant planktic foraminifera collected from plankton tows, sediment traps and surface sediments. The specimens have fully resolved and curated taxonomy and represent 43 of the currently recognised 48 holoplanktic species and subspecies. The image stacks form a basis for further applications, such as the characterisation of the architectural morphospace of the extant taxa, allowing studies of species functional ecology, calcification intensity and reconstructions of phylogenetic relationships.

Large-scale culturing of Neogloboquadrina pachyderma, its growth in, and tolerance of, variable environmental conditions.

The planktic foraminifera Neogloboquadrina pachyderma is a calcifying marine protist and the dominant planktic foraminifera species in the polar oceans, making it a key species in marine polar ecosystems. The calcium carbonate shells of foraminifera are widely used in palaeoclimate studies because their chemical composition reflects the seawater conditions in which they grow. This species provides unique proxy data for past surface ocean hydrography, which can provide valuable insight to future climate scenarios. However, little is known about the response of N. pachyderma to variable and changing environmental conditions. Here, we present observations from large-scale culturing experiments where temperature, salinity and carbonate chemistry were altered independently. We observed overall low mortality, calcification of new chambers and addition of secondary calcite crust in all our treatments. In-culture asexual reproduction events also allowed us to monitor the variable growth of N. pachyderma's offspring. Several specimens had extended periods of dormancy or inactivity after which they recovered. These observations suggest that N. pachyderma can tolerate, adapt to and calcify within a wide range of environmental conditions. This has implications for the species-level response to ocean warming and acidification, for future studies aiming to culture N. pachyderma and use in palaeoenvironmental reconstruction.

Isotopic evidence for an intensified hydrological cycle in the Indian sector of the Southern Ocean.

The hydrological cycle is expected to intensify in a warming climate. However, observational evidence of such changes in the Southern Ocean is difficult to obtain due to sparse measurements and a complex superposition of changes in precipitation, sea ice, and glacial meltwater. Here we disentangle these signals using a dataset of salinity and seawater oxygen isotope observations collected in the Indian sector of the Southern Ocean. Our results show that the atmospheric water cycle has intensified in this region between 1993 and 2021, increasing the salinity in subtropical surface waters by 0.06 ± 0.07 g kg-1 per decade, and decreasing the salinity in subpolar surface waters by -0.02 ± 0.01 g kg-1 per decade. The oxygen isotope data allow to discriminate the different freshwater processes showing that in the subpolar region, the freshening is largely driven by the increase in net precipitation (by a factor two) while the decrease in sea ice melt is largely balanced by the contribution of glacial meltwater at these latitudes. These changes extend the growing evidence for an acceleration of the hydrological cycle and a melting cryosphere that can be expected from global warming.

The FORCIS database: A global census of planktonic Foraminifera from ocean waters.

Planktonic Foraminifera are unique paleo-environmental indicators through their excellent fossil record in ocean sediments. Their distribution and diversity are affected by different environmental factors including anthropogenically forced ocean and climate change. Until now, historical changes in their distribution have not been fully assessed at the global scale. Here we present the FORCIS (Foraminifera Response to Climatic Stress) database on foraminiferal species diversity and distribution in the global ocean from 1910 until 2018 including published and unpublished data. The FORCIS database includes data collected using plankton tows, continuous plankton recorder, sediment traps and plankton pump, and contains ~22,000, ~157,000, ~9,000, ~400 subsamples, respectively (one single plankton aliquot collected within a depth range, time interval, size fraction range, at a single location) from each category. Our database provides a perspective of the distribution patterns of planktonic Foraminifera in the global ocean on large spatial (regional to basin scale, and at the vertical scale), and temporal (seasonal to interdecadal) scales over the past century.

Morphology, genome plasticity, and phylogeny in the genus ostreococcus reveal a cryptic species, O. mediterraneus sp. nov. (Mamiellales, Mamiellophyceae).

Coastal marine waters in many regions worldwide support abundant populations of extremely small (1-3 µm diameter) unicellular eukaryotic green algae, dominant taxa including several species in the class Mamiellophyceae. Their diminutive size conceals surprising levels of genetic diversity and defies classical species' descriptions. We present a detailed analysis within the genus Ostreococcus and show that morphological characteristics cannot be used to describe diversity within this group. Karyotypic analyses of the best-characterized species O. tauri show it to carry two chromosomes that vary in size between individual clonal lines, probably an evolutionarily ancient feature that emerged before species' divergences within the Mamiellales. By using a culturing technique specifically adapted to members of the genus Ostreococcus, we purified >30 clonal lines of a new species, Ostreococcus mediterraneus sp. nov., previously known as Ostreococcus clade D, that has been overlooked in several studies based on PCR-amplification of genetic markers from environment-extracted DNA. Phylogenetic analyses of the S-adenosylmethionine synthetase gene, and of the complete small subunit ribosomal RNA gene, including detailed comparisons of predicted ITS2 (internal transcribed spacer 2) secondary structures, clearly support that this is a separate species. In addition, karyotypic analyses reveal that the chromosomal location of its ribosomal RNA gene cluster differs from other Ostreococcus clades.