Molecular identification of Ammonia and Elphidium species (Foraminifera, Rotaliida) from the Kiel Fjord (SW Baltic Sea) with rDNA sequences

Ammonia and Elphidium collected in the Kiel Fjord for the present study were first identified on morphological bases as Ammonia beccarii (Linne´, 1758) and Elphidium excavatum (Terquem, 1876). Phylogenetic analyses based on partial SSU rDNA and LSU rDNA sequences show that Ammonia specimens sampled in the Kiel Fjord belong to the phylotype T6, which has a disjunct distribution (Wadden and Baltic Seas/China and Japan) and has been identified as Ammonia aomoriensis (Asano, 1951). Partial SSU rDNA sequence analyses indicate that Elphidium specimens from the Kiel Fjord belong to the clade E. excavatum, confirming the morphological identification. This clade can be further divided in three subclades. Kiel Fjord Elphidium belong to two of these subclades and were identified morphologically as the subspecies E. excavatum excavatum (Terquem, 1876) and E. e. clavatum Cushman, 1930

Drought recorded by Ba/Ca in coastal benthic foraminifera

Increasing occurrences of extreme weather events, such as the 2018 drought over northern Europe, are a concerning issue under global climate change. High-resolution archives of natural hydroclimate proxies, such as rapidly accumulating sediments containing biogenic carbonates, offer the potential to investigate the frequency and mechanisms of such events in the past. Droughts alter the barium (Ba) concentration of near-continent seawater through the reduction in Ba input from terrestrial runoff, which in turn may be recorded as changes in the chemical composition (Ba/Ca) of foraminiferal calcium carbonates accumulating in sediments. However, so far the use of Ba/Ca as a discharge indicator has been restricted to planktonic foraminifera, despite the high relative abundance of benthic species in coastal, shallow-water sites. Moreover, benthic foraminiferal Ba/Ca has mainly been used in openocean records as a proxy for paleo-productivity. Here we report on a new geochemical data set measured from living (CTG-labeled) benthic foraminiferal species to investigate the capability of benthic Ba/Ca to record changes in river runoff over a gradient of contrasting hydroclimatic conditions. Individual foraminifera (Bulimina marginata, Non-ionellina labradorica) were analyzed by laser-ablation ICP-MS over a seasonal and spatial gradient within Gullmar Fjord, Swedish west coast, during 2018-2019. The results are compared to an extensive meteorological and hydrological data set, as well as sediment and pore-water geochemistry. Benthic foraminiferal Ba/Ca correlates significantly to riverine runoff; however, the signals contain both spatial trends with distance to Ba source and species-specific influences such as micro-habitat preferences. We deduce that shallow-infaunal foraminifera are especially suitable as proxy for terrestrial Ba input and discuss the potential influence of water-column and pore-water Ba cycling. While distance to Ba source, water depth, pore-water geochemistry, and species-specific effects need to be considered in interpreting the data, our results demonstrate confidence in the use of Ba/Ca of benthic foraminifera from near-continent records as a proxy for past riverine discharge and to identify periods of drought.Peer reviewe

Ultrastructure and distribution of kleptoplasts in benthic foraminifera from shallow-water (photic) habitats

© The Author(s), 2017. This is the author's version of the work. It is posted here under a nonexclusive, irrevocable, paid-up, worldwide license granted to WHOI. It is made available for personal use, not for redistribution. The definitive version was published in Marine Micropaleontology 138 (2018): 46-62, doi:10.1016/j.marmicro.2017.10.003.Assimilation, sequestration and maintenance of foreign chloroplasts inside an organism is termed “chloroplast sequestration” or “kleptoplasty”. This phenomenon is known in certain benthic foraminifera, in which such kleptoplasts can be found both intact and functional, but with different retention times depending on foraminiferal species. In the present study, seven species of benthic foraminifera (Haynesina germanica, Elphidium williamsoni, E. selseyense, E. oceanense, E. aff. E. crispum, Planoglabratella opercularis and Ammonia sp.) were collected from shallow-water benthic habitats and examined with transmission electron microscope (TEM) for cellular ultrastructure to ascertain attributes of kleptoplasts. Results indicate that all these foraminiferal taxa actively obtain kleptoplasts but organized them differently within their endoplasm. In some species, the kleptoplasts were evenly distributed throughout the endoplasm (e.g., H. germanica, E. oceanense, Ammonia sp.), whereas other species consistently had plastids distributed close to the external cell membrane (e.g., Elphidium williamsoni, E. selseyense, P. opercularis). Chloroplast degradation also seemed to differ between species, as many degraded plastids were found in Ammonia sp. and E. oceanense compared to other investigated species. Digestion ability, along with different feeding and sequestration strategies may explain the differences in retention time between taxa. Additionally, the organization of the sequestered plastids within the endoplasm may also suggest behavioral strategies to expose and/or protect the sequestered plastids to/from light and/or to favor gas and/or nutrient exchange with their surrounding habitats.TJ was funded by the “FRESCO” project, a project supported by the Region Pays de Loire and the University of Angers. This work was also supported by a grant no. 200021_149333 from the Swiss National Science Foundation and the French national program EC2CO-LEFE (project ForChlo).JMB acknowledges the Robert W. Morse Chair for Excellence in Oceanography and the Investment in Science Fund at WHOI. Also, KK acknowledges the Academy of Finland (Project numbers: 278827, 283453)

Scaling laws explain foraminiferal pore patterns

Due to climate warming and increased anthropogenic impact, a decrease of ocean water oxygenation is expected in the near future, with major consequences for marine life. In this context, it is essential to develop reliable tools to assess past oxygen concentrations in the ocean, to better forecast these future changes. Recently, foraminiferal pore patterns have been proposed as a bottom water oxygenation proxy, but the parameters controlling foraminiferal pore patterns are still largely unknown. Here we use scaling laws to describe how both gas exchanges (metabolic needs) and mechanical constraints (shell robustness) control foraminiferal pore patterns. The derived mathematical model shows that only specific combinations of pore density and size are physically feasible. Maximum porosity, of about 30%, can only be obtained by simultaneously increasing pore size and decreasing pore density. A large empirical data set of pore data obtained for three pseudocryptic phylotypes of Ammonia, a common intertidal genus from the eastern Atlantic, strongly supports this conclusion. These new findings provide basic mechanistic understanding of the complex controls of foraminiferal pore patterns and give a solid starting point for the development of proxies of past oxygen concentrations based on these morphological features. Pore size and pore density are largely interdependent, and both have to be considered when describing pore patterns

History of the introduction of a species resembling the benthic foraminifera Nonionella stella in the Oslofjord (Norway): morphological, molecular and paleo-ecological evidences

Specimens resembling the benthic foraminifera Nonionella stella (Cushman and Moyer, 1930), a morphospecies originally described from the San Pedro Basin, California, USA, were observed for the first time in the Oslofjord (Norway) in 2012. This study investigates the Oslofjord Nonionella population in order to confirm its non-indigenous species (NIS) status and assess its introduction time. Morphological characterisation based on SEM imaging complemented by molecular identification using small subunit (SSU) rDNA sequencing and assessment of the recent past record (sediment core), were performed on material collected in the Oslofjord in 2016. Examination of the dead fauna showed that specimens resembling N. stella only appeared recently in the Oslofjord, confirming the NIS status of this population. Moreover, DNA results indicate that the Oslofjord specimens differ genetically from N. stella sampled in the Santa Barbara Basin (California USA). Hence, we propose to use the name Nonionella sp. T1 for the specimens sampled in the Oslofjord for the time being. In the southern part of the Skagerrak, specimens morphologically similar to Nonionella sp. T1 were reported as NIS in the Gullmar fjord (Sweden) in 2011 and in the Skagerrak in 2015. Molecular data indicate that the two populations from Gullmar- and Oslofjords are identical, based on their SSU rDNA sequences. In addition, analyses of foraminiferal dead assemblages suggest that the population from the Gullmar fjord settled prior to the Oslofjord population, i.e. ~ 1985 and about 2010, respectively. This implies that Nonionella sp. T1 may have been transported from Sweden to Norway by northward coastal currents.Publisher PDFPeer reviewe

Assessing proxy signatures of temperature, salinity, and hypoxia in the Baltic Sea through foraminifera-based geochemistry and faunal assemblages

We acknowledge funding through the Swedish Research Council (VR) (project no. 621-2011-5090), the German Research Council (project GR 3528/3-1), the Lamm Foundation, the Centre for Environmental and Climate Research at Lund University for Jeroen Groeneveld’s guest research stay, NERC grants NE4/G018502/1 and NE/G020310/1 to William E. N. Austin, and the University of Bremen for covering the article processing costs for this open-access publication.Current climate and environmental changes strongly affect shallow marine and coastal areas like the Baltic Sea. This has created a need for a context to understand the severity and potential outcomes of such changes. The context can be derived from paleoenvironmental records during periods when comparable events happened in the past. In this study, we explore how varying bottom water conditions across a large hydrographic gradient in the Baltic Sea affect benthic foraminiferal faunal assemblages and the geochemical composition of their calcite tests. We have conducted both morphological and molecular analyses of the faunas and we evaluate how the chemical signatures of the bottom waters are recorded in the tests of several species of benthic foraminifera. We focus on two locations, one in the Kattegat (western Baltic Sea) and one in Hano Bay (southern Baltic Sea). We show that seawater Mn/Ca, Mg/Ca, and Ba/Ca (Mn/Casw, Mg/Casw, and Ba/Casw) variations are mainly controlled by dissolved oxygen concentration and salinity. Their respective imprints on the foraminiferal calcite demonstrate the potential of Mn/Ca as a proxy for hypoxic conditions, and Ba/Ca as a proxy for salinity in enclosed basins such as the Baltic Sea. The traditional use of Mg-Ca as a proxy to reconstruct past seawater temperatures is not recommended in the region, as it may be overprinted by the large variations in salinity (specifically on Bulimina marginata), Mg/Casw, and possibly also the carbonate system. Salinity is the main factor controlling the faunal assemblages: a much more diverse fauna occurs in the higher-salinity (similar to 32) Kattegat than in the low-salinity (similar to 15) Hano Bay. Molecular identification shows that only Elphidium clavatum occurs at both locations, but other genetic types of both genera Elphidium and Ammonia are restricted to either low-or high-salinity locations. The combination of foraminiferal geochemistry and environmental parameters demonstrates that in a highly variable setting like the Baltic Sea, it is possible to separate different environmental impacts on the foraminiferal assemblages and therefore use Mn/Ca, Mg/Ca, and Ba/Ca to reconstruct how specific conditions may have varied in the past.Publisher PDFPeer reviewe

Metadata standards and practical guidelines for specimen and DNA curation when building barcode reference libraries for aquatic life

DNA barcoding and metabarcoding is increasingly used to effectively and precisely assess and monitor biodiversity in aquatic ecosystems. As these methods rely on data availability and quality of barcode reference libraries, it is important to develop and follow best practices to ensure optimal quality and traceability of the metadata associated with the reference barcodes used for identification. Sufficient metadata, as well as vouchers, corresponding to each reference barcode must be available to ensure reliable barcode library curation and, thereby, provide trustworthy baselines for downstream molecular species identification. This document (1) specifies the data and metadata required to ensure the relevance, the accessibility and traceability of DNA barcodes and (2) specifies the recommendations for DNA harvesting and for the storage of both voucher specimens/samples and barcode data.info:eu-repo/semantics/publishedVersio

The genetic diversity, phylogeography and morphology of Elphidiidae (Foraminifera) in the Northeast Atlantic

Genetic characterisation (SSU rRNA genotyping) and Scanning ElectronMicroscope (SEM) imaging of individualtests were used in tandem to determine the modern species richness of the foraminiferal family Elphidiidae(Elphidium, Haynesina and related genera) across the Northeast Atlantic shelf biomes. Specimens were collectedat 25 locations fromthe High Arctic to Iberia, and a total of 1013 individual specimenswere successfully SEMimagedand genotyped. Phylogenetic analyses were carried out in combination with 28 other elphidiid sequencesfrom GenBank and seventeen distinct elphidiid genetic types were identified within the sample set, sevenbeing sequenced for the first time. Genetic types cluster into sevenmain cladeswhich largely represent their generalmorphologicalcharacter. Differences between genetic types at the genetic, morphological and biogeographiclevels are indicative of species level distinction. Their biogeographic distributions, in combination with elphidiidSSU sequences from GenBank and high resolution images from the literature show that each of them exhibitsspecies-specific rather than clade-specific biogeographies. Due to taxonomic uncertainty and divergent taxonomicconcepts between schools, we believe that morphospecies names should not be placed onto molecularphylogenies unless both the morphology and genetic type have been linked to the formally named holotype,or equivalent. Based on strictmorphological criteria,we advocate using only a three-stage approach to taxonomyfor practical application in micropalaeontological studies. It comprises genotyping, the production of a formalmorphological description of the SEM images associated with the genetic type and then the allocation of themost appropriate taxonomic name by comparison with the formal type description. Using this approach, wewere able to apply taxonomic names to fifteen genetic types. One of the remaining two may be potentially cryptic,and one is undescribed in the literature. In general, the phylogeographic distribution is in agreement with ourknowledge of the ecology and biogeographical distribution of the corresponding morphospecies, highlighting thegenerally robust taxonomic framework of the Elphidiidae in time and space

A New Integrated Approach to Taxonomy: The Fusion of Molecular and Morphological Systematics with Type Material in Benthic Foraminifera

This work was supported by NERC grant NE4/G018502/1 and NE/G020310/1 (Website: http://www.nerc.ac.uk). The authors also thank the following for their support the Carnegie Trust for the Universities of Scotland (Website: http://www.carnegie-trust.org) and the Estuarine Coastal and Shelf Science Association (Website: http://www.ecsanews.org). M.S. was also supported by the Swiss National Science Foundation (SNSF), fellowships for advanced researchers PA00P2_126226 and PA00P2_142065 (Website: http://www.snf.ch/en/Pages/default.aspx).A robust and consistent taxonomy underpins the use of fossil material in palaeoenvironmental research and long-term assessment of biodiversity. This study presents a new integrated taxonomic protocol for benthic foraminifera by unequivocally reconciling the traditional taxonomic name to a specific genetic type. To implement this protocol, a fragment of the small subunit ribosomal RNA (SSU rRNA) gene is used in combination with 16 quantitative morphometric variables to fully characterise the benthic foraminiferal species concept of Elphidium williamsoni Haynes, 1973. A combination of live contemporary topotypic specimens, original type specimens and specimens of genetic outliers were utilised in this study. Through a series of multivariate statistical tests we illustrate that genetically characterised topotype specimens are morphologically congruent with both the holotype and paratype specimens of E. williamsoni Haynes, 1973. We present the first clear link between morphologically characterised type material and the unique SSU rRNA genetic type of E. williamsoni. This example provides a standard framework for the benthic foraminifera which bridges the current discontinuity between molecular and morphological lines of evidence, allowing integration with the traditional Linnaean roots of nomenclature to offer a new prospect for taxonomic stability.Publisher PDFPeer reviewe