Global change drives modern plankton communities away from the pre-industrial state.

The ocean-the Earth's largest ecosystem-is increasingly affected by anthropogenic climate change1,2. Large and globally consistent shifts have been detected in species phenology, range extension and community composition in marine ecosystems3-5. However, despite evidence for ongoing change, it remains unknown whether marine ecosystems have entered an Anthropocene6 state beyond the natural decadal to centennial variability. This is because most observational time series lack a long-term baseline, and the few time series that extend back into the pre-industrial era have limited spatial coverage7,8. Here we use the unique potential of the sedimentary record of planktonic foraminifera-ubiquitous marine zooplankton-to provide a global pre-industrial baseline for the composition of modern species communities. We use a global compilation of 3,774 seafloor-derived planktonic foraminifera communities of pre-industrial age9 and compare these with communities from sediment-trap time series that have sampled plankton flux since AD 1978 (33 sites, 87 observation years). We find that the Anthropocene assemblages differ from their pre-industrial counterparts in proportion to the historical change in temperature. We observe community changes towards warmer or cooler compositions that are consistent with historical changes in temperature in 85% of the cases. These observations not only confirm the existing evidence for changes in marine zooplankton communities in historical times, but also demonstrate that Anthropocene communities of a globally distributed zooplankton group systematically differ from their unperturbed pre-industrial state.

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.

Past and future decline of tropical pelagic biodiversity.

A major research question concerning global pelagic biodiversity remains unanswered: when did the apparent tropical biodiversity depression (i.e., bimodality of latitudinal diversity gradient [LDG]) begin? The bimodal LDG may be a consequence of recent ocean warming or of deep-time evolutionary speciation and extinction processes. Using rich fossil datasets of planktonic foraminifers, we show here that a unimodal (or only weakly bimodal) diversity gradient, with a plateau in the tropics, occurred during the last ice age and has since then developed into a bimodal gradient through species distribution shifts driven by postglacial ocean warming. The bimodal LDG likely emerged before the Anthropocene and industrialization, and perhaps ∼15,000 y ago, indicating a strong environmental control of tropical diversity even before the start of anthropogenic warming. However, our model projections suggest that future anthropogenic warming further diminishes tropical pelagic diversity to a level not seen in millions of years.

Decadal trend of plankton community change and habitat shoaling in the Arctic gateway recorded by planktonic foraminifera.

The Fram Strait plays a crucial role in regulating the heat and sea-ice dynamics in the Arctic. In response to the ongoing global warming, the marine biota of this Arctic gateway is experiencing significant changes with increasing advection of Atlantic species. The footprint of this 'Atlantification' has been identified in isolated observations across the plankton community, but a systematic, multi-decadal perspective on how regional climate change facilitates the invasion of Atlantic species and affects the ecology of the resident species is lacking. Here we evaluate a series of 51 depth-resolved plankton profiles collected in the Fram Strait during seven surveys between 1985 and 2015, using planktonic foraminifera as a proxy for changes in both the pelagic community composition and species vertical habitat depth. The time series reveals a progressive shift towards more Atlantic species, occurring independently of changes in local environmental conditions. We conclude that this trend is reflecting higher production of the Atlantic species in the Nordic Seas, from where they are advected into the Fram Strait. At the same time, we observe the ongoing extensive sea-ice export from the Arctic and associated cooling-induced decline in density and habitat shoaling of the subpolar Turborotalita quinqueloba, whereas the resident Neogloboquadrina pachyderma persists. As a result, the planktonic foraminiferal community and vertical structure in the Fram Strait shift to a new state, driven by both remote forcing of the Atlantic invaders and local climatic changes acting on the resident species. The strong summer export of Arctic sea ice has so far buffered larger plankton transformation. We predict that if the sea-ice export will decrease, the Arctic gateway will experience rapid restructuring of the pelagic community, even in the absence of further warming. Such a large change in the gateway region will likely propagate into the Arctic proper.

Climate change decouples oceanic primary and export productivity and organic carbon burial.

Understanding responses of oceanic primary productivity, carbon export, and burial to climate change is essential for model-based projection of biological feedbacks in a high-CO2 world. Here we compare estimates of productivity based on the composition of fossil diatom floras with organic carbon burial off Oregon in the Northeast Pacific across a large climatic transition at the last glacial termination. Although estimated primary productivity was highest during the Last Glacial Maximum, carbon burial was lowest, reflecting reduced preservation linked to low sedimentation rates. A diatom size index further points to a glacial decrease (and deglacial increase) in the fraction of fixed carbon that was exported, inferred to reflect expansion, and contraction, of subpolar ecosystems that today favor smaller plankton. Thus, in contrast to models that link remineralization of carbon to temperature, in the Northeast Pacific, we find dominant ecosystem and sea floor control such that intervals of warming climate had more efficient carbon export and higher carbon burial despite falling primary productivity.

Geochemical signatures of benthic foraminiferal shells from a heat-polluted shallow marine environment provide field evidence for growth and calcification under extreme warmth.

Shallow marine calcifiers play an important role as marine ecosystem engineers and in the global carbon cycle. Understanding their response to warming is essential to evaluate the fate of marine ecosystems under global change scenarios. A rare opportunity to test the effect of warming acting on natural ecosystems is by investigation of heat-polluted areas. Here, we study growth and calcification in benthic foraminifera that inhabit a thermally polluted coastal area in Israel, where they are exposed to elevated temperatures reaching up to ~42°C in summer. Live specimens of two known heat-tolerant species Lachlanella sp. 1 and Pararotalia calcariformata were collected over a period of 1 year from two stations, representing thermally polluted and undisturbed (control) shallow hard bottom habitats. Single-chamber element ratios of these specimens were obtained using laser ablation, and the Mg/Ca of the most recently grown final chambers were used to calculate their calcification temperatures. Our results provide the first direct field evidence that these foraminifera species not only persist at extreme warm temperatures but continue to calcify and grow. Species-specific Mg/Ca thermometry indicates that P. calcariformata precipitate their shells at temperatures as high as 40°C and Lachlanella sp. 1 at least up to 36°C, but both species show a threshold for calcification at cold temperatures: calcification in P. calcariformata only occurred above 22°C and in Lachlanella sp. 1 above 15°C. Our observations from the heat-polluted area indicate that under future warming scenarios, calcification in heat-tolerant foraminifera species will not be inhibited during summer, but instead the temperature window for their calcification will be expanded throughout much of the year. The observed inhibition of calcification at low temperatures indicates that the role of heat-tolerant foraminifera in carbonate production will most likely increase in future decades.

Nomenclature for the Nameless: A Proposal for an Integrative Molecular Taxonomy of Cryptic Diversity Exemplified by Planktonic Foraminifera.

Investigations of biodiversity, biogeography, and ecological processes rely on the identification of "species" as biologically significant, natural units of evolution. In this context, morphotaxonomy only provides an adequate level of resolution if reproductive isolation matches morphological divergence. In many groups of organisms, morphologically defined species often disguise considerable genetic diversity, which may be indicative of the existence of cryptic species. The diversity hidden by morphological species can be disentangled through genetic surveys, which also provide access to data on the ecological distribution of genetically circumscribed units. These units can be identified by unique DNA sequence motifs and allow studies of evolutionary and ecological processes at different levels of divergence. However, the nomenclature of genetically circumscribed units within morphological species is not regulated and lacks stability. This represents a major obstacle to efforts to synthesize and communicate data on genetic diversity for multiple stakeholders. We have been confronted with such an obstacle in our work on planktonic foraminifera, where the stakeholder community is particularly diverse, involving geochemists, paleoceanographers, paleontologists, and biologists, and the lack of stable nomenclature beyond the level of formal morphospecies prevents effective transfer of knowledge. To circumvent this problem, we have designed a stable, reproducible, and flexible nomenclature system for genetically circumscribed units, analogous to the principles of a formal nomenclature system. Our system is based on the definition of unique DNA sequence motifs collocated within an individual, their typification (in analogy with holotypes), utilization of their hierarchical phylogenetic structure to define levels of divergence below that of the morphospecies, and a set of nomenclature rules assuring stability. The resulting molecular operational taxonomic units remain outside the domain of current nomenclature codes, but are linked to formal morphospecies as regulated by the codes. Subsequently, we show how this system can be applied to classify genetically defined units using the SSU rDNA marker in planktonic foraminifera and we highlight its potential use for other groups of organisms where similarly high levels of connectivity between molecular and formal taxonomies can be achieved.

A dynamic subtropical coastal hotspot of benthic foraminifera in the Southeastern Mediterranean indicates early-stage tropicalization.

Due to ongoing ocean warming, subtropical environments are becoming accessible to tropical species. Among these environments are the vermetid reefs of the Southeastern Mediterranean (SEM). In the last decades, these valuable coastal habitats witnessed the proliferation of numerous alien species of tropical origin. Among the meiofauna thriving on these reefs are benthic foraminifera, single cell marine organisms that make a significant contribution to global carbonate production. It has been widely recognized that benthic foraminifera, among other invasive species, thrive in the macroalgal cover, and it has been suggested that their populations are becoming a significant new source of sediment substrate. Here, we report on the first systematic assessment of the population size of the benthic foraminifera, allowing a comparison with data from the native tropical habitat of these species. Our study is based on a seasonal sampling of benthic foraminifera from confined sampling areas at four sites along the vermetid reef platforms of the Israeli SEM coast. Our survey reveals a patchy distribution of each species with peak population densities exceeding 100,000 specimens per m2, making the SEM a hotspot of benthic foraminifera, with population densities comparable to tropical coral reef environments. The assemblages of the SEM hotspot are dominated by cosmopolitan foraminiferal taxa and tropical invaders from the Indo-Pacific (e.g., Amphistegina lobifera, Pararotalia calcariformata, soritids, and Hauerina diversa). In contrast to foraminiferal hotspots in the tropics, which are completely dominated by larger symbiont-bearing taxa, the SEM hotspot stands out due to high abundances of non-symbiont-bearing species Textularia agglutinans and small miliolids. An intriguing observation is the significant heterogeneity in composition and density of foraminiferal assemblages between the vermetid reefs' southern and northern areas (Israel), indicating that the productivity of the dominant species are also modulated by local yet unknown environmental factors.

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.

ForCenS-LGM: a dataset of planktonic foraminifera species assemblage composition for the Last Glacial Maximum.

Species assemblage composition of marine microfossils offers the possibility to investigate ecological and climatological change on time scales inaccessible using conventional observations. Planktonic foraminifera - calcareous zooplankton - have an excellent fossil record and are used extensively in palaeoecology and palaeoceanography. During the Last Glacial Maximum (LGM; 19,000 - 23,000 years ago), the climate was in a radically different state. This period is therefore a key target to investigate climate and biodiversity under different conditions than today. Studying LGM climate and ecosystems indeed has a long history, yet the most recent global synthesis of planktonic foraminifera assemblage composition is now nearly two decades old. Here we present the ForCenS-LGM dataset with 2,365 species assemblage samples collected using standardised methods and with harmonised taxonomy. The data originate from marine sediments from 664 sites and present a more than 50% increase in coverage compared to previous work. The taxonomy is compatible with the most recent global core top dataset, enabling direct investigation of temporal changes in foraminifera biogeography and facilitating seawater temperature reconstructions.

Macroevolutionary patterns in intragenomic rDNA variability among planktonic foraminifera.

Ribosomal intragenomic variability in prokaryotes and eukaryotes is a genomic feature commonly studied for its inflationary impact on molecular diversity assessments. However, the evolutionary mechanisms and distribution of this phenomenon within a microbial group are rarely explored. Here, we investigate the intragenomic variability in 33 species of planktonic foraminifera, calcifying marine protists, by inspecting 2,403 partial SSU sequences obtained from single-cell clone libraries. Our analyses show that polymorphisms are common among planktonic foraminifera species, but the number of polymorphic sites significantly differs among clades. With our molecular simulations, we could assess that most of these mutations are located in paired regions that do not affect the secondary structure of the SSU fragment. Finally, by mapping the number of polymorphic sites on the phylogeny of the clades, we were able to discuss the evolution and potential sources of intragenomic variability in planktonic foraminifera, linking this trait to the distinctive nuclear and genomic dynamics of this microbial group.

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.

Invasion success of a Lessepsian symbiont-bearing foraminifera linked to high dispersal ability, preadaptation and suppression of sexual reproduction.

Among the most successful Lessepsian invaders is the symbiont-bearing benthic foraminifera Amphistegina lobifera. In its newly conquered habitat, this prolific calcifier and ecosystem engineer is exposed to environmental conditions that exceed the range of its native habitat. To disentangle which processes facilitated the invasion success of A. lobifera into the Mediterranean Sea we analyzed a ~ 1400 bp sequence fragment covering the SSU and ITS gene markers to compare the populations from its native regions and along the invasion gradient. The genetic variability was studied at four levels: intra-genomic, population, regional and geographical. We observed that the invasion is not associated with genetic differentiation, but the invasive populations show a distinct suppression of intra-genomic variability among the multiple copies of the rRNA gene. A reduced genetic diversity compared to the Indopacific is observed already in the Red Sea populations and their high dispersal potential into the Mediterranean appears consistent with a bridgehead effect resulting from the postglacial expansion from the Indian Ocean into the Red Sea. We conclude that the genetic structure of the invasive populations reflects two processes: high dispersal ability of the Red Sea source population pre-adapted to Mediterranean conditions and a likely suppression of sexual reproduction in the invader. This discovery provides a new perspective on the cost of invasion in marine protists: The success of the invasive A. lobifera in the Mediterranean Sea comes at the cost of abandonment of sexual reproduction.

Shared ancestry of algal symbiosis and chloroplast sequestration in foraminifera.

Foraminifera are unicellular organisms that established the most diverse algal symbioses in the marine realm. Endosymbiosis repeatedly evolved in several lineages, while some engaged in the sequestration of chloroplasts, known as kleptoplasty. So far, kleptoplasty has been documented exclusively in the rotaliid clade. Here, we report the discovery of kleptoplasty in the species Hauerina diversa that belongs to the miliolid clade. The existence of kleptoplasty in the two main clades suggests that it is more widespread than previously documented. We observed chloroplasts in clustered structures within the foraminiferal cytoplasm and confirmed their functionality. Phylogenetic analysis of 18S ribosomal RNA gene sequences showed that H. diversa branches next to symbiont-bearing Alveolinidae. This finding represents evidence of of a relationship between kleptoplastic and symbiotic foraminifera.. Analysis of ribosomal genes and metagenomics revealed that alveolinid symbionts and kleptoplasts belong to the same clade, which suggests a common ancestry.

Mg Doping of N-Polar, In-Rich InAlN.

Metal organic chemical vapor deposition was used to grow N-polar In0.63Al0.37N on sapphire substrates. P-doping was provided by a precursor flow of Cp2Mg between 0 and 130 nmol/min, reaching a Cp2Mg/III ratio of 8.3 × 10-3. The grain structure of 360 nm thick InAlN was spoiled by pits after introducing a flow of CP2Mg at 30 nmol/min. The surface quality was improved with a flow of 80 nmol/min; however, detrimental deterioration appeared at 130 nmol/min. This correlated with the XRD shape and determined density of dislocations, indicating a phase separation at the highest flow. Degenerated n-type conduction and a free carrier concentration of ~1019 cm-3 were determined in all samples, with a minor compensation observed at a CP2Mg flow of 30 nmol/min. The room temperature (RT) electron mobility of ~40 cm2/Vs of the undoped sample was reduced to ~6 and ~0.3 cm2/Vs with a CP2Mg flow of 30 and 80 nmol/min, respectively. Scattering at ionized acceptor/donor Mg-related levels is suggested. RT photoluminescence showed a red shift of 0.22 eV from the virgin 1.73 eV peak value with Mg doping. Mobility degradation was found to be the main factor by InAlN resistivity determination, which increased by two orders of magnitude, approaching ~0.5 Ωcm, at the highest Cp2Mg flow.

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.

Vertical niche partitioning between cryptic sibling species of a cosmopolitan marine planktonic protist.

A large portion of the surface-ocean biomass is represented by microscopic unicellular plankton. These organisms are functionally and morphologically diverse, but it remains unclear how their diversity is generated. Species of marine microplankton are widely distributed because of passive transport and lack of barriers in the ocean. How does speciation occur in a system with a seemingly unlimited dispersal potential? Recent studies using planktonic foraminifera as a model showed that even among the cryptic genetic diversity within morphological species, many genetic types are cosmopolitan, lending limited support for speciation by geographical isolation. Here we show that the current two-dimensional view on the biogeography and potential speciation mechanisms in the microplankton may be misleading. By depth-stratified sampling, we present evidence that sibling genetic types in a cosmopolitan species of marine microplankton, the planktonic foraminifer Hastigerina pelagica, are consistently separated by depth throughout their global range. Such strong separation between genetically closely related and morphologically inseparable genetic types indicates that niche partitioning in marine heterotrophic microplankton can be maintained in the vertical dimension on a global scale. These observations indicate that speciation along depth (depth-parapatric speciation) can occur in vertically structured microplankton populations, facilitating diversification without the need for spatial isolation.

Plankton response to global warming is characterized by non-uniform shifts in assemblage composition since the last ice age.

Biodiversity is expected to change in response to future global warming. However, it is difficult to predict how species will track the ongoing climate change. Here we use the fossil record of planktonic foraminifera to assess how biodiversity responded to climate change with a magnitude comparable to future anthropogenic warming. We compiled time series of planktonic foraminifera assemblages, covering the time from the last ice age across the deglaciation to the current warm period. Planktonic foraminifera assemblages shifted immediately when temperature began to rise at the end of the last ice age and continued to change until approximately 5,000 years ago, even though global temperature remained relatively stable during the last 11,000 years. The biotic response was largest in the mid latitudes and dominated by range expansion, which resulted in the emergence of new assemblages without analogues in the glacial ocean. Our results indicate that the plankton response to global warming was spatially heterogeneous and did not track temperature change uniformly over the past 24,000 years. Climate change led to the establishment of new assemblages and possibly new ecological interactions, which suggests that current anthropogenic warming may lead to new, different plankton community composition.

Renewal of planktonic foraminifera diversity after the Cretaceous Paleogene mass extinction by benthic colonizers.

The biotic crisis following the end-Cretaceous asteroid impact resulted in a dramatic renewal of pelagic biodiversity. Considering the severe and immediate effect of the asteroid impact on the pelagic environment, it is remarkable that some of the most affected pelagic groups, like the planktonic foraminifera, survived at all. Here we queried a surface ocean metabarcoding dataset to show that calcareous benthic foraminifera of the clade Globothalamea are able to disperse actively in the plankton, and we show using molecular clock phylogeny that the modern planktonic clades originated from different benthic ancestors that colonized the plankton after the end-Cretaceous crisis. We conclude that the diversity of planktonic foraminifera has been the result of a constant leakage of benthic foraminifera diversity into the plankton, continuously refueling the planktonic niche, and challenge the classical interpretation of the fossil record that suggests that Mesozoic planktonic foraminifera gave rise to the modern communities.

In(Ga)N 3D Growth on GaN-Buffered On-Axis and Off-Axis (0001) Sapphire Substrates by MOCVD.

In(Ga)N epitaxial layers were grown on on-axis and off-axis (0001) sapphire substrates with an about 1100 nm-thick GaN buffer layer stack using organometallic chemical vapor deposition at 600 °C. The In(Ga)N layers consisted of a thin (~10-25 nm) continuous layer of small conical pyramids in which large conical pyramids with an approximate height of 50-80 nm were randomly distributed. The large pyramids were grown above the edge-type dislocations which originated in the GaN buffer; the dislocations did not penetrate the large, isolated pyramids. The large pyramids were well crystallized and relaxed with a small quantity of defects, such as dislocations, preferentially located at the contact zones of adjacent pyramids. The low temperature (6.5 K) photoluminescence spectra showed one clear maximum at 853 meV with a full width at half maximum (FWHM) of 75 meV and 859 meV with a FWHM of 80 meV for the off-axis and on-axis samples, respectively.