Publications by authors named "Michal Kucera"

38 Publications

Planktonic foraminifera eDNA signature deposited on the seafloor remains preserved after burial in marine sediments.

Sci Rep 2020 11 23;10(1):20351. Epub 2020 Nov 23.

MARUM-Center for Marine Environmental Sciences, University of Bremen, Leobener Strasse 8, 28359, Bremen, Germany.

Environmental DNA (eDNA) metabarcoding of marine sediments has revealed large amounts of sequences assigned to planktonic taxa. How this planktonic eDNA is delivered on the seafloor and preserved in the sediment is not well understood. We address these questions by comparing metabarcoding and microfossil foraminifera assemblages in sediment cores taken off Newfoundland across a strong ecological gradient. We detected planktonic foraminifera eDNA down to 30 cm and observed that the planktonic/benthic amplicon ratio changed with depth. The relative proportion of planktonic foraminiferal amplicons remained low from the surface down to 10 cm, likely due to the presence of DNA from living benthic foraminifera. Below 10 cm, the relative proportion of planktonic foraminifera amplicons rocketed, likely reflecting the higher proportion of planktonic eDNA in the DNA burial flux. In addition, the microfossil and metabarcoding assemblages showed a congruent pattern indicating that planktonic foraminifera eDNA is deposited without substantial lateral advection and preserves regional biogeographical patterns, indicating deposition by a similar mechanism as the foraminiferal shells. Our study shows that the planktonic eDNA preserved in marine sediments has the potential to record climatic and biotic changes in the pelagic community with the same spatial and temporal resolution as microfossils.
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http://dx.doi.org/10.1038/s41598-020-77179-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7684305PMC
November 2020

Intraspecific size variation in planktonic foraminifera cannot be consistently predicted by the environment.

Ecol Evol 2020 Oct 28;10(20):11579-11590. Epub 2020 Sep 28.

Ocean and Earth Science National Oceanography Centre Southampton University of Southampton Waterfront Campus Southampton UK.

The size structure of plankton communities is an important determinant of their functions in marine ecosystems. However, few studies have quantified how organism size varies within species across biogeographical scales. Here, we investigate how planktonic foraminifera, a ubiquitous zooplankton group, vary in size across the tropical and subtropical oceans of the world. Using a recently digitized museum collection, we measured shell area of 3,799 individuals of nine extant species in 53 seafloor sediments. We first analyzed potential size biases in the collection. Then, for each site, we obtained corresponding local values of mean annual sea-surface temperature (SST), net primary productivity (NPP), and relative abundance of each species. Given former studies, we expected species to reach largest shell sizes under optimal environmental conditions. In contrast, we observe that species differ in how much their size variation is explained by SST, NPP, and/or relative abundance. While some species have predictable size variation given these variables (), other species show no relationships between size and the studied covariates (, , ). By incorporating intraspecific variation and sampling broader geographical ranges compared to previous studies, we conclude that shell size variation in planktonic foraminifera species cannot be consistently predicted by the environment. Our results caution against the general use of size as a proxy for planktonic foraminifera environmental optima. More generally, our work highlights the utility of natural history collections and the importance of studying intraspecific variation when interpreting macroecological patterns.
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http://dx.doi.org/10.1002/ece3.6792DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7593196PMC
October 2020

Thresholds for ecological responses to global change do not emerge from empirical data.

Nat Ecol Evol 2020 11 17;4(11):1502-1509. Epub 2020 Aug 17.

Theoretical Physics/Complex Systems, Institute for Chemistry and Biology of the Marine Environment, Carl von Ossietzky University Oldenburg, Oldenburg, Germany.

To understand ecosystem responses to anthropogenic global change, a prevailing framework is the definition of threshold levels of pressure, above which response magnitudes and their variances increase disproportionately. However, we lack systematic quantitative evidence as to whether empirical data allow definition of such thresholds. Here, we summarize 36 meta-analyses measuring more than 4,600 global change impacts on natural communities. We find that threshold transgressions were rarely detectable, either within or across meta-analyses. Instead, ecological responses were characterized mostly by progressively increasing magnitude and variance when pressure increased. Sensitivity analyses with modelled data revealed that minor variances in the response are sufficient to preclude the detection of thresholds from data, even if they are present. The simulations reinforced our contention that global change biology needs to abandon the general expectation that system properties allow defining thresholds as a way to manage nature under global change. Rather, highly variable responses, even under weak pressures, suggest that 'safe-operating spaces' are unlikely to be quantifiable.
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http://dx.doi.org/10.1038/s41559-020-1256-9DOI Listing
November 2020

Anaerobic metabolism of Foraminifera thriving below the seafloor.

ISME J 2020 10 8;14(10):2580-2594. Epub 2020 Jul 8.

MARUM-Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany.

Foraminifera are single-celled eukaryotes (protists) of large ecological importance, as well as environmental and paleoenvironmental indicators and biostratigraphic tools. In addition, they are capable of surviving in anoxic marine environments where they represent a major component of the benthic community. However, the cellular adaptations of Foraminifera to the anoxic environment remain poorly constrained. We sampled an oxic-anoxic transition zone in marine sediments from the Namibian shelf, where the genera Bolivina and Stainforthia dominated the Foraminifera community, and use metatranscriptomics to characterize Foraminifera metabolism across the different geochemical conditions. Relative Foraminifera gene expression in anoxic sediment increased an order of magnitude, which was confirmed in a 10-day incubation experiment where the development of anoxia coincided with a 20-40-fold increase in the relative abundance of Foraminifera protein encoding transcripts, attributed primarily to those involved in protein synthesis, intracellular protein trafficking, and modification of the cytoskeleton. This indicated that many Foraminifera were not only surviving but thriving, under the anoxic conditions. The anaerobic energy metabolism of these active Foraminifera was characterized by fermentation of sugars and amino acids, fumarate reduction, and potentially dissimilatory nitrate reduction. Moreover, the gene expression data indicate that under anoxia Foraminifera use the phosphogen creatine phosphate as an ATP store, allowing reserves of high-energy phosphate pool to be maintained for sudden demands of increased energy during anaerobic metabolism. This was co-expressed alongside genes involved in phagocytosis and clathrin-mediated endocytosis (CME). Foraminifera may use CME to utilize dissolved organic matter as a carbon and energy source, in addition to ingestion of prey cells via phagocytosis. These anaerobic metabolic mechanisms help to explain the ecological success of Foraminifera documented in the fossil record since the Cambrian period more than 500 million years ago.
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http://dx.doi.org/10.1038/s41396-020-0708-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7490399PMC
October 2020

High dispersal capacity and biogeographic breaks shape the genetic diversity of a globally distributed reef-dwelling calcifier.

Ecol Evol 2020 Jun 14;10(12):5976-5989. Epub 2020 May 14.

MARUM University of Bremen Bremen Germany.

Understanding the role of dispersal and adaptation in the evolutionary history of marine species is essential for predicting their response to changing conditions. We analyzed patterns of genetic differentiation in the key tropical calcifying species of large benthic foraminifera to reveal the evolutionary processes responsible for its biogeographic distribution. We collected specimens from 16 sites encompassing the entire range of the species and analyzed hypervariable fragments of the 18S SSU rDNA marker. We identified six hierarchically organized genotypes with mutually exclusive distribution organized along a longitudinal gradient. The distribution is consistent with diversification occurring in the Indo-West Pacific (IWP) followed by dispersal toward the periphery. This pattern can be explained by: (a) high dispersal capacity of the species, (b) habitat heterogeneity driving more recent differentiation in the IWP, and (c) ecological-scale processes such as niche incumbency reinforcing patterns of genotype mutual exclusion. The dispersal potential of this species drives the ongoing range expansion into the Mediterranean Sea, indicating that is able to expand its distribution by tracking increases in temperature. The genetic structure reveals recent diversification and high rate of extinction in the evolutionary history of the clade suggesting a high turnover rate of the diversity at the cryptic level. This diversification dynamic combined with high dispersal potential, allowed the species to maintain a widespread distribution over periods of geological and climatic upheaval. These characteristics are likely to allow the species to modify its geographic range in response to ongoing global warming without requiring genetic differentiation.
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http://dx.doi.org/10.1002/ece3.6335DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7319125PMC
June 2020

Past and future decline of tropical pelagic biodiversity.

Proc Natl Acad Sci U S A 2020 06 26;117(23):12891-12896. Epub 2020 May 26.

Faculty of Science, University of the Ryukyus, 903-0213 Okinawa, Japan.

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.
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http://dx.doi.org/10.1073/pnas.1916923117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7293716PMC
June 2020

Genetic and morphological divergence in the warm-water planktonic foraminifera genus Globigerinoides.

PLoS One 2019 5;14(12):e0225246. Epub 2019 Dec 5.

MARUM Center for Marine Environmental Sciences, University of Bremen, Leobener Strasse, Bremen, Germany.

The planktonic foraminifera genus Globigerinoides provides a prime example of a species-rich genus in which genetic and morphological divergence are uncorrelated. To shed light on the evolutionary processes that lead to the present-day diversity of Globigerinoides, we investigated the genetic, ecological and morphological divergence of its constituent species. We assembled a global collection of single-cell barcode sequences and show that the genus consists of eight distinct genetic types organized in five extant morphospecies. Based on morphological evidence, we reassign the species Globoturborotalita tenella to Globigerinoides and amend Globigerinoides ruber by formally proposing two new subspecies, G. ruber albus n.subsp. and G. ruber ruber in order to express their subspecies level distinction and to replace the informal G. ruber "white" and G. ruber "pink", respectively. The genetic types within G. ruber and Globigerinoides elongatus show a combination of endemism and coexistence, with little evidence for ecological differentiation. CT-scanning and ontogeny analysis reveal that the diagnostic differences in adult morphologies could be explained by alterations of the ontogenetic trajectories towards final (reproductive) size. This indicates that heterochrony may have caused the observed decoupling between genetic and morphological diversification within the genus. We find little evidence for environmental forcing of either the genetic or the morphological diversification, which allude to biotic interactions such as symbiosis, as the driver of speciation in Globigerinoides.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0225246PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6894840PMC
March 2020

An extinction event in planktonic Foraminifera preceded by stabilizing selection.

PLoS One 2019 14;14(10):e0223490. Epub 2019 Oct 14.

Center for Marine Environmental Sciences (MARUM), Universität Bremen, Bremen, Germany.

Unless they adapt, populations facing persistent stress are threatened by extinction. Theoretically, populations facing stress can react by either disruption (increasing trait variation and potentially generating new traits) or stabilization (decreasing trait variation). In the short term, stabilization is more economical, because it quickly transfers a large part of the population closer to a new ecological optimum. However, stabilization is deleterious in the face of persistently increasing stress, because it reduces variability and thus decreases the ability to react to further changes. Understanding how natural populations react to intensifying stress reaching terminal levels is key to assessing their resilience to environmental change such as that caused by global warming. Because extinctions are hard to predict, observational data on the adaptation of populations facing extinction are rare. Here, we make use of the glacial salinity rise in the Red Sea as a natural experiment allowing us to analyse the reaction of planktonic Foraminifera to stress escalation in the geological past. We analyse morphological trait state and variation in two species across a salinity rise leading to their local extinction. Trilobatus sacculifer reacted by stabilization in shape and size, detectable several thousand years prior to extinction. Orbulina universa reacted by trait divergence, but each of the two divergent populations remained stable or reacted by further stabilization. These observations indicate that the default reaction of the studied Foraminifera is stabilization, and that stress escalation did not lead to the emergence of adapted forms. An inherent inability to breach the global adaptive threshold would explain why communities of Foraminifera and other marine protists reacted to Quaternary climate change by tracking their zonally shifting environments. It also means that populations of marine plankton species adapted to response by migration will be at risk of extinction when exposed to stress outside of the adaptive range.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0223490PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6791547PMC
March 2020

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

Nature 2019 06 22;570(7761):372-375. Epub 2019 May 22.

MARUM - Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany.

The ocean-the Earth's largest ecosystem-is increasingly affected by anthropogenic climate change. Large and globally consistent shifts have been detected in species phenology, range extension and community composition in marine ecosystems. However, despite evidence for ongoing change, it remains unknown whether marine ecosystems have entered an Anthropocene 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 coverage. 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 age 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.
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http://dx.doi.org/10.1038/s41586-019-1230-3DOI Listing
June 2019

Unassigned diversity of planktonic foraminifera from environmental sequencing revealed as known but neglected species.

PLoS One 2019 21;14(3):e0213936. Epub 2019 Mar 21.

MARUM-Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany.

Most research on extant planktonic foraminifera has been directed towards larger species (>0.150 mm) which can be easily manipulated, counted and yield enough calcite for geochemical analyses. This has drawn attention towards the macroperforate clade and created an impression of their numerical and ecological dominance. Drawing such conclusions from the study of such "giants" is a dangerous path. There were times in the evolutionary history of planktonic foraminifera when all species were smaller than 0.1 mm and indeed numerous small taxa, mainly from the microperforate clade, have been formally described from the modern plankton. The significance of these small, obscure and neglected species is poorly characterized and their relationship to the newly discovered hyperabundant but uncharacterized lineages of planktonic foraminifera in metabarcoding datasets is unknown. To determine, who is hiding in the metabarcoding datasets, we carried out an extensive sequencing of 18S rDNA targeted at small and obscure species. The sequences of the newly characterized small and obscure taxa match many of the previously uncharacterized lineages found in metabarcoding data. This indicates that most of the modern diversity in planktonic foraminifera has been taxonomically captured, but the role of the small and neglected taxa has been severely underestimated.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0213936PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6428320PMC
December 2019

Thermal tolerance and range expansion of invasive foraminifera under climate changes.

Sci Rep 2019 03 12;9(1):4198. Epub 2019 Mar 12.

Ben-Gurion University of the Negev, Beer Sheva, Israel.

The Eastern Mediterranean is experiencing a large-scale invasion of alien tropical species from the Red Sea. This "Lessepsian invasion" began with the opening of the Suez Canal and is promoted by the ongoing oceanic warming. The environmental differences between the Red Sea and the Mediterranean act as a buffer allowing the invasion of certain species. This provides an opportunity to study the differences in temperature sensitivity between two sibling species of the cosmopolitian foraminifera Amphistegina. Both species are very common in the Red Sea. Whilest, only one is a successful invader and the other is absent in the Eastern Mediterranean. Here we show that the two species are different in their temperature sensitivity, which explains their selective invasion into the Mediterranean. These differences demonstrate that in respect to climate change resilient marine species can be distinguished by their ability to compensate for temperature changes by adjusting their physiological performance and by having tolerance to a wider temperature range. Moreover, we demonstrate that selective filtering mechanisms during invasion can prefer species that are more resilient to colder rather than expected warmer temperatures.
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http://dx.doi.org/10.1038/s41598-019-40944-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6414502PMC
March 2019

Putative sponge biomarkers in unicellular Rhizaria question an early rise of animals.

Nat Ecol Evol 2019 04 4;3(4):577-581. Epub 2019 Mar 4.

Max Planck Institute for Biogeochemistry, Jena, Germany.

The dawn of animals remains one of the most mysterious milestones in the evolution of life. The fossil lipids 24-isopropylcholestane and 26-methylstigmastane are considered diagnostic for demosponges-arguably the oldest group of living animals. The widespread occurrence and high relative abundance of these biomarkers in Ediacaran sediments from 635-541 million years (Myr) ago have been viewed as evidence for the rise of animals to ecological importance approximately 100 Myr before their rapid Cambrian radiation. Here we show that the biosynthesis of 24-isopropylcholestane and 26-methylstigmastane precursors is common among early-branching unicellular Rhizaria-heterotrophic protists that play an important role in trophic cycling and carbon export in the modern ocean. Negating these hydrocarbons as sponge biomarkers, our study places the oldest evidence for animals closer to the Cambrian Explosion. Cambrian silica hexactine spicules that are approximately 535 Myr old now represent the oldest diagnostic sponge remains, whereas approximately 558-Myr-old Dickinsonia and Kimberella (Ediacara biota) provide the most reliable evidence for the emergence of animals. The proliferation of predatory protists may have been responsible for much of the ecological changes during the late Neoproterozoic, including the rise of algae, the establishment of complex trophic relationships and the oxygenation of shallow-water habitats required for the subsequent ascent of macroscopic animals.
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http://dx.doi.org/10.1038/s41559-019-0806-5DOI Listing
April 2019

Diverse Internal Symbiont Community in the Endosymbiotic Foraminifera : Implications for Symbiont Shuffling Under Thermal Stress.

Front Microbiol 2018 11;9:2018. Epub 2018 Sep 11.

MARUM - Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany.

Many shallow-water tropical and subtropical foraminifera engage in photosymbiosis with eukaryotic microalgae. Some of these foraminifera appear to harbor a diverse consortium of endosymbiotic algae within a single host. Such apparent ability to contain different symbionts could facilitate change in symbiont community composition (symbiont shuffling) and mediate the ecological success of the group in a changing environment. However, the discovery of the intra-individual symbiont diversity was thus far based on symbiont culturing, which provides strong constraints on the vitality of the identified algae but provides poor constraints on their initial abundance and thus functional relevance to the host. Here we analyze the algal symbiont diversity in , a benthic foraminifera sampled at four stations, inside and outside of a thermal plume in the eastern Mediterranean coast of Israel. This species has recently invaded the Mediterranean, is unusually thermally tolerant and was described previously to host at least one different diatom symbiont than other symbiont-bearing foraminifera. Our results using genotyping and isolation of algae in culture medium, confirm multiple associations with different diatom species within the same individual. Both methods revealed spatially consistent symbiont associations and identified the most common symbiont as a pelagic diatom In one case, an alternative dominant symbiont, the diatom sp., was detected by genotyping. This diatom was the third most abundant species identified using standard algae culturing method. This method further revealed a spatially consistent pattern in symbiont diversity of a total of seventeen identified diatom species, across the studied localities. Collectively, these results indicate that hosts a diverse consortium of diatom endosymbionts, where different members can become numerically dominant and thus functionally relevant in a changing environment.
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http://dx.doi.org/10.3389/fmicb.2018.02018DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6141668PMC
September 2018

Foraminiferal single chamber analyses of heavy metals as a tool for monitoring permanent and short term anthropogenic footprints.

Mar Pollut Bull 2018 Mar 11;128:65-71. Epub 2018 Jan 11.

Ben-Gurion University of the Negev, Beer Sheva, Israel. Electronic address:

In order to establish environmentally sustainable industries there is a need for high-resolution temporal and spatial monitoring of heavy metal pollutants even at low concentrations before they become hazardous for local ecosystems. Here we present single chamber records of Cu, Zn and Pb in shells of two benthic foraminifera species with different shell types from two shallow coastal stations in Israel: An area adjacent to an electrical power plant and desalination factory (Hadera) and an industrially free nature reserve (Nachsholim). Records of both foraminifera species show elevated metal concentrations in Hadera clearly identifying the footprint of the local industrial facilities. Moreover, short-term events of elevated Cu and Pb concentrations were detected by single chamber analyses. This study demonstrates the potential of using heavy metals anomalies in foraminiferal single chambers as a tool for detecting the industrial footprint of coastal facilities as well as short term events of elevated heavy metals.
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http://dx.doi.org/10.1016/j.marpolbul.2018.01.002DOI Listing
March 2018

Disentangling thermal stress responses in a reef-calcifier and its photosymbionts by shotgun proteomics.

Sci Rep 2018 02 23;8(1):3524. Epub 2018 Feb 23.

Biogeochemistry and Geology, Leibniz Centre for Tropical Marine Research (ZMT), 28359, Bremen, Germany.

The proliferation of key marine ecological engineers and carbonate producers often relies on their association with photosymbiotic algae. Evaluating stress responses of these organisms is important to predict their fate under future climate projections. Physiological approaches are limited in their ability to resolve the involved molecular mechanisms and attribute stress effects to the host or symbiont, while probing and partitioning of proteins cannot be applied in organisms where the host and symbiont are small and cannot be physically separated. Here we apply a label-free quantitative proteomics approach to detect changes of proteome composition in the diatom-bearing benthic foraminifera Amphistegina gibbosa experimentally exposed to three thermal-stress scenarios. We developed a workflow for protein extraction from less than ten specimens and simultaneously analysed host and symbiont proteomes. Despite little genomic data for the host, 1,618 proteins could be partially assembled and assigned. The proteomes revealed identical pattern of stress response among stress scenarios as that indicated by physiological measurements, but allowed identification of compartment-specific stress reactions. In the symbiont, stress-response and proteolysis-related proteins were up regulated while photosynthesis-related proteins declined. In contrast, host homeostasis was maintained through chaperone up-regulation associated with elevated proteosynthesis and proteolysis, and the host metabolism shifted to heterotrophy.
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http://dx.doi.org/10.1038/s41598-018-21875-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5824892PMC
February 2018

Surface ocean metabarcoding confirms limited diversity in planktonic foraminifera but reveals unknown hyper-abundant lineages.

Sci Rep 2018 02 7;8(1):2539. Epub 2018 Feb 7.

Station Biologique de Roscoff, UMR7144, Sorbonne Universités UPMC Université Paris 06 & CNRS, Place Georges Teissier, 29680, Roscoff, France.

Since the advent of DNA metabarcoding surveys, the planktonic realm is considered a treasure trove of diversity, inhabited by a small number of abundant taxa, and a hugely diverse and taxonomically uncharacterized consortium of rare species. Here we assess if the apparent underestimation of plankton diversity applies universally. We target planktonic foraminifera, a group of protists whose known morphological diversity is limited, taxonomically resolved and linked to ribosomal DNA barcodes. We generated a pyrosequencing dataset of ~100,000 partial 18S rRNA foraminiferal sequences from 32 size fractioned photic-zone plankton samples collected at 8 stations in the Indian and Atlantic Oceans during the Tara Oceans expedition (2009-2012). We identified 69 genetic types belonging to 41 morphotaxa in our metabarcoding dataset. The diversity saturated at local and regional scale as well as in the three size fractions and the two depths sampled indicating that the diversity of foraminifera is modest and finite. The large majority of the newly discovered lineages occur in the small size fraction, neglected by classical taxonomy. These unknown lineages dominate the bulk [>0.8 µm] size fraction, implying that a considerable part of the planktonic foraminifera community biomass has its origin in unknown lineages.
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http://dx.doi.org/10.1038/s41598-018-20833-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5803224PMC
February 2018

Younger Dryas ice margin retreat triggered by ocean surface warming in central-eastern Baffin Bay.

Nat Commun 2017 10 18;8(1):1017. Epub 2017 Oct 18.

MARUM-Center for Marine Environmental Sciences, University of Bremen, Leobener Strasse 8, Bremen, 28359, Germany.

The transition from the last ice age to the present-day interglacial was interrupted by the Younger Dryas (YD) cold period. While many studies exist on this climate event, only few include high-resolution marine records that span the YD. In order to better understand the interactions between ocean, atmosphere and ice sheet stability during the YD, more high-resolution proxy records from the Arctic, located proximal to ice sheet outlet glaciers, are required. Here we present the first diatom-based high-resolution quantitative reconstruction of sea surface conditions from central-eastern Baffin Bay, covering the period 14.0-10.2 kyr BP. Our record reveals warmer sea surface conditions and strong interactions between the ocean and the West Greenland ice margin during the YD. These warmer conditions were caused by increased Atlantic-sourced water inflow combined with amplified seasonality. Our results emphasize the importance of the ocean for ice sheet stability under the current changing climate.
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http://dx.doi.org/10.1038/s41467-017-01155-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5715068PMC
October 2017

ForCenS, a curated database of planktonic foraminifera census counts in marine surface sediment samples.

Sci Data 2017 08 22;4:170109. Epub 2017 Aug 22.

MARUM Center for Marine Environmental Sciences, University of Bremen, Leobener Straße 8, Bremen 28359, Germany.

Census counts of marine microfossils in surface sediments represent an invaluable resource for paleoceanography and for the investigation of macroecological processes. A prerequisite for such applications is the provision of data syntheses for individual microfossil groups. Specific to such syntheses is the necessity of taxonomical harmonisation across the constituent datasets, coupled with dereplication of previous compilations. Both of these aspects require expert knowledge, but with increasing number of records involved in such syntheses, the application of expert knowledge via manual curation is not feasible. Here we present a synthesis of planktonic foraminifera census counts in surface sediment samples, which is taxonomically harmonised, dereplicated and treated for numerical and other inconsistencies. The data treatment is implemented as an objective and largely automated pipeline, allowing us to reduce the initial 6,984 records to 4,205 counts from unique sites and informative technical or true replicates. We provide the final product and document the procedure, which can be easily adopted for other microfossil data syntheses.
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http://dx.doi.org/10.1038/sdata.2017.109DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5566098PMC
August 2017

Reef calcifiers are adapted to episodic heat stress but vulnerable to sustained warming.

PLoS One 2017 6;12(7):e0179753. Epub 2017 Jul 6.

MARUM, Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany.

Shallow marine ecosystems naturally experience fluctuating physicochemical conditions across spatial and temporal scales. Widespread coral-bleaching events, induced by prolonged heat stress, highlight the importance of how the duration and frequency of thermal stress influence the adaptive physiology of photosymbiotic calcifiers. Large benthic foraminifera harboring algal endosymbionts are major tropical carbonate producers and bioindicators of ecosystem health. Like corals, they are sensitive to thermal stress and bleach at temperatures temporarily occurring in their natural habitat and projected to happen more frequently. However, their thermal tolerance has been studied so far only by chronic exposure, so how they respond under more realistic episodic heat-event scenarios remains unknown. Here, we determined the physiological responses of Amphistegina gibbosa, an abundant western Atlantic foraminifera, to four different treatments--control, single, episodic, and chronic exposure to the same thermal stress (32°C)--in controlled laboratory cultures. Exposure to chronic thermal stress reduced motility and growth, while antioxidant capacity was elevated, and photosymbiont variables (coloration, oxygen-production rates, chlorophyll a concentration) indicated extensive bleaching. In contrast, single- and episodic-stress treatments were associated with higher motility and growth, while photosymbiont variables remained stable. The effects of single and episodic heat events were similar, except for the presumable occurrence of reproduction, which seemed to be suppressed by both episodic and chronic stress. The otherwise different responses between treatments with thermal fluctuations and chronic stress indicate adaptation to thermal peaks, but not to chronic exposure expected to ensue when baseline temperatures are elevated by climate change. This firstly implies that marine habitats with a history of fluctuating thermal stress potentially support resilient physiological mechanisms among photosymbiotic organisms. Secondly, there seem to be temporal constraints related to heat events among coral reef environments and reinforces the importance of temporal fluctuations in stress exposure in global-change studies and projections.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0179753PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5500281PMC
September 2017

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

Glob Chang Biol 2017 10 29;23(10):4346-4353. Epub 2017 May 29.

Ben-Gurion University of the Negev, Beer Sheva, Israel.

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.
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http://dx.doi.org/10.1111/gcb.13729DOI Listing
October 2017

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

Syst Biol 2016 Sep 12;65(5):925-40. Epub 2016 Apr 12.

MARUM Center for Marine Environmental Sciences, University of Bremen, Leobener Strasse, 28359 Bremen, Germany.

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.
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http://dx.doi.org/10.1093/sysbio/syw031DOI Listing
September 2016

Selective responses of benthic foraminifera to thermal pollution.

Mar Pollut Bull 2016 Apr 16;105(1):324-36. Epub 2016 Feb 16.

Ben-Gurion University of the Negev, Beer Sheva, Israel. Electronic address:

Persistent thermohaline pollution at a site along the northern coast of Israel, due to power and desalination plants, is used as a natural laboratory to evaluate the effects of rising temperature and salinity levels on benthic foraminifera living in shallow hard-bottom habitats. Biomonitoring of the disturbed area and a control station shows that elevated temperature is a more significant stressor compared to salinity, thus causing a decrease in abundance and richness. Critical temperature thresholds were observed at 30 and 35°C, the latter representing the most thermally tolerant species in the studied area Pararotalia calcariformata, which is the only symbiont-bearing species observed within the core of the heated area. Common species of the shallow hard-bottom habitats including several Lessepsian invaders are almost absent in the most exposed site indicating that excess warming will likely impede the survival of these species that currently benefit from the ongoing warming of the Eastern Mediterranean.
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http://dx.doi.org/10.1016/j.marpolbul.2016.02.002DOI Listing
April 2016

Seasonal Variation in Shell Calcification of Planktonic Foraminifera in the NE Atlantic Reveals Species-Specific Response to Temperature, Productivity, and Optimum Growth Conditions.

PLoS One 2016 9;11(2):e0148363. Epub 2016 Feb 9.

MARUM, University Bremen, Bremen, Germany.

Using shells collected from a sediment trap series in the Madeira Basin, we investigate the effects of seasonal variation of temperature, productivity, and optimum growth conditions on calcification in three species of planktonic Foraminifera. The series covers an entire seasonal cycle and reflects conditions at the edge of the distribution of the studied species, manifesting more suitable growth conditions during different parts of the year. The seasonal variation in seawater carbonate saturation at the studied site is negligible compared to other oceanic regions, allowing us to assess the effect of parameters other than carbonate saturation. Shell calcification is quantified using weight and size of individual shells. The size-weight scaling within each species is robust against changes in environmental parameters, but differs among species. An analysis of the variation in calcification intensity (size-normalized weight) reveals species-specific response patterns. In Globigerinoides ruber (white) and Globigerinoides elongatus, calcification intensity is correlated with temperature (positive) and productivity (negative), whilst in Globigerina bulloides no environmental forcing is observed. The size-weight scaling, calcification intensity, and response of calcification intensity to environmental change differed between G. ruber (white) and G. elongatus, implying that patterns extracted from pooled analyses of these species may reflect their changing proportions in the samples. Using shell flux as a measure of optimum growth conditions, we observe significant positive correlation with calcification intensity in G. elongatus, but negative correlation in G. bulloides. The lack of a consistent response of calcification intensity to optimum growth conditions is mirrored by the results of shell size analyses. We conclude that calcification intensity in planktonic Foraminifera is affected by factors other than carbonate saturation. These factors include temperature, productivity, and optimum growth conditions, but the strength and sign of the relationships differ among species, potentially complicating interpretations of calcification data from the fossil record.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0148363PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4747607PMC
July 2016

Recent Invasion of the Symbiont-Bearing Foraminifera Pararotalia into the Eastern Mediterranean Facilitated by the Ongoing Warming Trend.

PLoS One 2015 13;10(8):e0132917. Epub 2015 Aug 13.

MARUM, Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany.

The eastern Mediterranean is a hotspot of biological invasions. Numerous species of Indo-pacific origin have colonized the Mediterranean in recent times, including tropical symbiont-bearing foraminifera. Among these is the species Pararotalia calcariformata. Unlike other invasive foraminifera, this species was discovered only two decades ago and is restricted to the eastern Mediterranean coast. Combining ecological, genetic and physiological observations, we attempt to explain the recent invasion of this species in the Mediterranean Sea. Using morphological and genetic data, we confirm the species attribution to P. calcariformata McCulloch 1977 and identify its symbionts as a consortium of diatom species dominated by Minutocellus polymorphus. We document photosynthetic activity of its endosymbionts using Pulse Amplitude Modulated Fluorometry and test the effects of elevated temperatures on growth rates of asexual offspring. The culturing of asexual offspring for 120 days shows a 30-day period of rapid growth followed by a period of slower growth. A subsequent 48-day temperature sensitivity experiment indicates a similar developmental pathway and high growth rate at 28°C, whereas an almost complete inhibition of growth was observed at 20°C and 35°C. This indicates that the offspring of this species may have lower tolerance to cold temperatures than what would be expected for species native to the Mediterranean. We expand this hypothesis by applying a Species Distribution Model (SDM) based on modern occurrences in the Mediterranean using three environmental variables: irradiance, turbidity and yearly minimum temperature. The model reproduces the observed restricted distribution and indicates that the range of the species will drastically expand westwards under future global change scenarios. We conclude that P. calcariformata established a population in the Levant because of the recent warming in the region. In line with observations from other groups of organisms, our results indicate that continued warming of the eastern Mediterranean will facilitate the invasion of more tropical marine taxa into the Mediterranean, disturbing local biodiversity and ecosystem structure.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0132917PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4536047PMC
May 2016

Fossil and genetic evidence for the polyphyletic nature of the planktonic foraminifera "Globigerinoides", and description of the new genus Trilobatus.

PLoS One 2015 28;10(5):e0128108. Epub 2015 May 28.

Department of Geosciences, University of Fribourg, Fribourg, Switzerland.

Planktonic foraminifera are one of the most abundant and diverse protists in the oceans. Their utility as paleo proxies requires rigorous taxonomy and comparison with living and genetically related counterparts. We merge genetic and fossil evidence of "Globigerinoides", characterized by supplementary apertures on spiral side, in a new approach to trace their "total evidence phylogeny" since their first appearance in the latest Paleogene. Combined fossil and molecular genetic data indicate that this genus, as traditionally understood, is polyphyletic. Both datasets indicate the existence of two distinct lineages that evolved independently. One group includes "Globigerinoides" trilobus and its descendants, the extant "Globigerinoides" sacculifer, Orbulina universa and Sphaeroidinella dehiscens. The second group includes the Globigerinoides ruber clade with the extant G. conglobatus and G. elongatus and ancestors. In molecular phylogenies, the trilobus group is not the sister taxon of the ruber group. The ruber group clusters consistently together with the modern Globoturborotalita rubescens as a sister taxon. The re-analysis of the fossil record indicates that the first "Globigerinoides" in the late Oligocene are ancestral to the trilobus group, whereas the ruber group first appeared at the base of the Miocene with representatives distinct from the trilobus group. Therefore, polyphyly of the genus "Globigerinoides" as currently defined can only be avoided either by broadening the genus concept to include G. rubescens and a large number of fossil species without supplementary apertures, or if the trilobus group is assigned to a separate genus. Since the former is not feasible due to the lack of a clear diagnosis for such a broad genus, we erect a new genus Trilobatus for the trilobus group (type species Globigerina triloba Reuss) and amend Globoturborotalita and Globigerinoides to clarify morphology and wall textures of these genera. In the new concept, Trilobatus n. gen. is paraphyletic and gave rise to the Praeorbulina/Orbulina and Sphaeroidinellopsis/Sphaeroidinella lineages.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0128108PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4447400PMC
April 2016

PFR²: a curated database of planktonic foraminifera 18S ribosomal DNA as a resource for studies of plankton ecology, biogeography and evolution.

Mol Ecol Resour 2015 Nov 15;15(6):1472-85. Epub 2015 Apr 15.

Centre National de la Recherche Scientifique, UMR 7144, EPEP, Station Biologique de Roscoff, 29680, Roscoff, France.

Planktonic foraminifera (Rhizaria) are ubiquitous marine pelagic protists producing calcareous shells with conspicuous morphology. They play an important role in the marine carbon cycle, and their exceptional fossil record serves as the basis for biochronostratigraphy and past climate reconstructions. A major worldwide sampling effort over the last two decades has resulted in the establishment of multiple large collections of cryopreserved individual planktonic foraminifera samples. Thousands of 18S rDNA partial sequences have been generated, representing all major known morphological taxa across their worldwide oceanic range. This comprehensive data coverage provides an opportunity to assess patterns of molecular ecology and evolution in a holistic way for an entire group of planktonic protists. We combined all available published and unpublished genetic data to build PFR(2), the Planktonic foraminifera Ribosomal Reference database. The first version of the database includes 3322 reference 18S rDNA sequences belonging to 32 of the 47 known morphospecies of extant planktonic foraminifera, collected from 460 oceanic stations. All sequences have been rigorously taxonomically curated using a six-rank annotation system fully resolved to the morphological species level and linked to a series of metadata. The PFR(2) website, available at http://pfr2.sb-roscoff.fr, allows downloading the entire database or specific sections, as well as the identification of new planktonic foraminiferal sequences. Its novel, fully documented curation process integrates advances in morphological and molecular taxonomy. It allows for an increase in its taxonomic resolution and assures that integrity is maintained by including a complete contingency tracking of annotations and assuring that the annotations remain internally consistent.
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http://dx.doi.org/10.1111/1755-0998.12410DOI Listing
November 2015

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

Proc Natl Acad Sci U S A 2015 Jan 1;112(2):332-5. Epub 2014 Dec 1.

CEOAS, College of Earth, Ocean, and Atmospheric Sciences, Oregon State University, Corvallis, OR 97331.

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.
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http://dx.doi.org/10.1073/pnas.1410480111DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4299185PMC
January 2015

Phylogeography of the tropical planktonic foraminifera lineage globigerinella reveals isolation inconsistent with passive dispersal by ocean currents.

PLoS One 2014 24;9(3):e92148. Epub 2014 Mar 24.

Department of Palaeobiology, Swedish Museum of Natural History, Stockholm, Sweden.

Morphologically defined species of marine plankton often harbor a considerable level of cryptic diversity. Since many morphospecies show cosmopolitan distribution, an understanding of biogeographic and evolutionary processes at the level of genetic diversity requires global sampling. We use a database of 387 single-specimen sequences of the SSU rDNA of the planktonic foraminifera Globigerinella as a model to assess the biogeographic and phylogenetic distributions of cryptic diversity in marine microplankton on a global scale. Our data confirm the existence of multiple, well isolated genetic lineages. An analysis of their abundance and distribution indicates that our sampling is likely to approximate the actual total diversity. Unexpectedly, we observe an uneven allocation of cryptic diversity among the phylogenetic lineages. We show that this pattern is neither an artifact of sampling intensity nor a function of lineage age. Instead, we argue that it reflects an ongoing speciation process in one of the three major lineages. Surprisingly, four of the six genetic types in the hyperdiverse lineage are biogeographically restricted to the Indopacific. Their mutual co-occurrence and their hierarchical phylogenetic structure provide no evidence for an origin through sudden habitat fragmentation and their limitation to the Indopacific challenges the view of a global gene flow within the warm-water provinces. This phenomenon shows that passive dispersal is not sufficient to describe the distribution of plankton diversity. Rather, these organisms show differentiated distribution patterns shaped by species interactions and reflecting phylogenetic contingency with unique histories of diversification rates.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0092148PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3963880PMC
January 2015

Ancient origin of the modern deep-sea fauna.

PLoS One 2012 10;7(10):e46913. Epub 2012 Oct 10.

Geoscience Centre, University of Göttingen, Department of Geobiology, Göttingen, Germany.

The origin and possible antiquity of the spectacularly diverse modern deep-sea fauna has been debated since the beginning of deep-sea research in the mid-nineteenth century. Recent hypotheses, based on biogeographic patterns and molecular clock estimates, support a latest Mesozoic or early Cenozoic date for the origin of key groups of the present deep-sea fauna (echinoids, octopods). This relatively young age is consistent with hypotheses that argue for extensive extinction during Jurassic and Cretaceous Oceanic Anoxic Events (OAEs) and the mid-Cenozoic cooling of deep-water masses, implying repeated re-colonization by immigration of taxa from shallow-water habitats. Here we report on a well-preserved echinoderm assemblage from deep-sea (1000-1500 m paleodepth) sediments of the NE-Atlantic of Early Cretaceous age (114 Ma). The assemblage is strikingly similar to that of extant bathyal echinoderm communities in composition, including families and genera found exclusively in modern deep-sea habitats. A number of taxa found in the assemblage have no fossil record at shelf depths postdating the assemblage, which precludes the possibility of deep-sea recolonization from shallow habitats following episodic extinction at least for those groups. Our discovery provides the first key fossil evidence that a significant part of the modern deep-sea fauna is considerably older than previously assumed. As a consequence, most major paleoceanographic events had far less impact on the diversity of deep-sea faunas than has been implied. It also suggests that deep-sea biota are more resilient to extinction events than shallow-water forms, and that the unusual deep-sea environment, indeed, provides evolutionary stability which is very rarely punctuated on macroevolutionary time scales.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0046913PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3468611PMC
April 2013