Search

Isotopic and trace-element signals in the calcite shells of the planktonic foraminifera Neogloboquadrina pachyderma represent key proxies to reconstruct past climatic conditions in northern high latitudes. A correct interpretation of these chemical signals requires knowledge of the habitat and trophic interactions of the species. Direct observations on the biological interactions of N. pachyderma in polar environments are lacking and to date no consensus exists on the trophic behavior of this species. Here, we use single-cell metabarcoding to characterize the interactions of 39 specimens of N. pachyderma from two sites in the Baffin Bay with the local eukaryotic pelagic community. Our results show that the eukaryotic interactome of the foraminifera is dominated by diatoms, accounting for >50% of the reads in 17 of the samples, but other groups such as Crustacea and Syndiniales are also present. The high abundance Syndiniales suggests that these parasites could infect N. pachyderma and may play an important role in its population dynamics. Moreover, the strong but taxonomically non-specific association with algae, existing irrespective of depth and occurring in specimens collected far below the photic zone indicates that opportunistically grazed diatom-fueled marine aggregates likely represent the main interaction substrate of N. pachyderma.

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.

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.

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 “source” region, from where they are advected into the Fram Strait. At the same time, we observe that the ongoing extensive sea-ice export from the Arctic and associated cooling-induced decline in density and habitat shoaling of the subpolarTurborotalita quinqueloba, whereas the residentNeogloboquadrina pachydermapersists. As a result, the planktonic foraminiferal community and vertical structure in the Fram Strait shifts 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.

Individual foraminifera analysis (IFA) holds promise to reconstruct seasonal to interannual oceanographic variability. Even though planktonic foraminifera are reliable recorders of environmental conditions on a population level, whether they also are on the level of individuals is unknown. Yet, one of the main assumptions underlying IFA is that each specimen records ocean conditions with negligible noise. Here we test this assumption using stable isotope data measured on groups of four shells of Neogloboquadrina pachyderma from a 16–19 d resolution sediment trap time series from the subpolar North Atlantic. We find a within-sample variability of 0.11 ‰ and 0.10 ‰ for δ18O and δ13C respectively that shows no seasonal pattern and exceeds water column variability in spring when conditions are homogeneous down to hundreds of metres. We assess the possible effect of life cycle characteristics and delay due to settling on foraminifera δ18O variability with simulations using temperature and δ18Oseawater as input. These simulations indicate that the observed δ18O variability can only partially be explained by environmental variability. Individual N. pachyderma are thus imperfect recorders of temperature and δ18Oseawater. Based on these simulations, we estimate the excess noise on δ18O to be 0.11±0.06 ‰. The origin and nature of the recording imprecision require further work, but our analyses highlight the need to take such excess noise into account when interpreting the geochemical variability among individual foraminifera.

Diurnal vertical migration (DVM) is a widespread phenomenon in the upper ocean, but it remains unclear to what degree it also involves passively transported micro- and meso-zooplankton. These organisms are difficult to monitor by in situ sensing and observations from discrete samples are often inconclusive. Prime examples of such ambiguity are planktonic foraminifera, where contradictory evidence for DVM continues to cast doubt on the stability of species vertical habitats, which introduces uncertainties in geochemical proxy interpretation. To provide a robust answer, we carried out highly replicated randomized sampling with 41 vertically resolved plankton net hauls taken within 26 hours in a confined area of 400 km2 in the tropical North Atlantic, where DVM in larger plankton occurs. Manual enumeration of planktonic foraminifera cell density consistently reveals the highest total cell concentrations in the surface mixed layer (top 50 m) and analysis of cell density in seven individual species representing different shell sizes, life strategies and presumed depth habitats reveals consistent vertical habitats not changing over the 26 hours sampling period. These observations robustly reject the existence of DVM in planktonic foraminifera in a setting where DVM occurs in other organisms.

Stable oxygen isotopes (δ18O) of planktonic foraminifera are one of the most used tools to reconstruct environmental conditions of the water column. Since different species live and calcify at different depths in the water column, the δ18O of sedimentary foraminifera reflects to a large degree the vertical habitat and interspecies δ18O differences and can thus potentially provide information on the vertical structure of the water column. To fully unlock the potential of foraminifera as recorders of past surface water properties, it is necessary to understand how and under what conditions the environmental signal is incorporated into the calcite shells of individual species. Deep-dwelling species play a particularly important role in this context, since their calcification depth reaches below the surface mixed layer. Here we report δ18O measurements made on four deep-dwelling Globorotalia species collected with stratified plankton tows in the Eastern North Atlantic. Size and crust effects on the δ18O signal were evaluated showing that a larger size increases the δ18O of Globorotalia inflata and Globorotalia hirsuta, and a crust effect is reflected in a higher δ18O in Globorotalia truncatulinoides. The great majority of the δ18O values can be explained without invoking disequilibrium calcification. When interpreted in this way the data imply depth-integrated calcification with progressive addition of calcite with depth to about 300 m for G. inflata and to about 500 m for G. hirsuta. In Globorotalia scitula, despite a strong subsurface maximum in abundance, the vertical δ18O profile is flat and appears dominated by a surface layer signal. In G. truncatulinoides, the δ18O profile follows equilibrium for each depth, implying a constant habitat during growth at each depth layer. The δ18O values are more consistent with the predictions of the Shackleton (1974) paleotemperature equation, except in G. scitula, which shows values more consistent with the Kim and O’Neil (1997) prediction. In all cases, we observe a difference between the level where most of the specimens were present and the depth where most of their shell appears to calcify.

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.

Isotopic and trace-element signals in the calcite shells of the planktonic foraminiferaNeogloboquadrina pachydermarepresent key proxies to reconstruct past climatic conditions in northern high latitudes. A correct interpretation of these chemical signals requires knowledge of the habitat and trophic interactions of the species. Direct observations on the biological interactions ofN. pachydermain polar environments are lacking and to date no consensus exists on the trophic behaviour of this species. Here we use single-cell metabarcoding to characterise the interactions of 39 specimens ofN. pachydermafrom two sites in the Baffin Bay with the local eukaryotic pelagic community. Our results show that the eukaryotic interactome of the foraminifera is dominated by diatoms, accounting for > 50% of the reads in 17 of the samples, but other groups such as Crustacea and Syndiniales are also present. The high abundance Syndiniales suggests that these parasites could infectN. pachydermaand may play an important role in its population dynamics. Moreover, the strong but taxonomically non-specific association with algae, existing irrespective of depth and occurring in specimens collected far below the photic zone indicates that opportunistically grazed diatom-fuelled marine aggregates likely represent the main interaction substrate ofN. pachyderma.

Author's accepted version (postprint). This is an Accepted Manuscript of an article published by the National Academy of Sciences in PNAS on 26/05/2020. Available online: https://www.pnas.org/content/pnas/117/23/12891.full.pdf 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.

Planktonic foraminifera precipitate calcareous shells, which after the death of the organisms are exported from the sea surface to the sea floor, where they are preserved on geologically relevant timescales. The export flux of planktonic foraminifera shells constitutes globally up to a half, and in the studied region off Cap Blanc (Atlantic Ocean) about one third, of the marine pelagic calcite flux. Given their importance for the marine calcite budget and for the pelagic carbonate counter pump, which counteracts the biological pump in terms of oceanic capacity for intake of CO2, it is crucial to gain an understanding of factors modulating the export flux of planktonic foraminifera calcite. In principle, variability in the export flux of planktonic foraminifera calcite could depend within one species on i) shell flux, ii) shell size and iii) calcification intensity, and where shell size and calcification intensity differ among species also on the species composition of the deposited assemblage. To assess the importance of these aspects in modulating the export flux of planktonic foraminifera calcite, we investigated two annual time series (from 1990-1991 and 2007-2008) from sediment traps moored in the Cap Blanc upwelling area. We assessed the predictability of foraminifera calcite flux variability on seasonal and interannual time scales, by determining the variability in species-specific shell fluxes, shell sizes and weights with bi-weekly resolution. We find a remarkable discrepancy in the contribution of the controlling factors between seasonal and interannual scales. On the seasonal time scale, 80% of the variability of the calcite flux is explained by shell flux. On the inter-annual time scale, on the other hand, variations in shell size and calcification intensity are key to explain the calcite flux, since the time series from 2007-2008 yielded 58% larger and 11% heavier specimens. These results imply that for the global estimate of planktonic foraminifera calcite flux, shell flux is likely the most relevant predictor. However, a prediction of the temporal evolution of the calcite flux will likely require estimates of changes in shell size and calcification intensity of the involved foraminifera species.

Understanding the response of marine ecosystems to climate change requires knowledge of processes that operate over long time scales. Over the last decades, abundant data have been generated on the change in the composition of marine microplankton assemblages across the last deglaciation. These data were used to reconstruct various aspects of the ocean and climate system during this climatic upheaval; however, their potential to evaluate biotic response to climatic forcing has been rarely explored. Here, we compiled records of plankton response to the last deglaciation covering the entire North Atlantic Ocean. The records comprise assemblage composition data of marine zooplankton (planktonic foraminifera) and phytoplankton (coccolithophores, diatoms and dinoflagellates) covering the last 24 ka with a resolution of at least 1 ka. The comparability of the data is ensured by using either published age models or a combination of radiocarbon ages and correlated oxygen isotope data. We use these records to first determine the shape of the major compositional change in each record by principle components analyses and quantification of compositional turnover. The mean global response of the plankton to the deglaciation was then evaluated by an Empirical Orthogonal Function analysis of the main biotic trends across all sites. A preliminary analysis was run solely on the zooplankton data set as the phytoplankton data set is still work in progress. We find that the dominant response of the zooplankton consists of synchronous unidirectional shifts initiated between 16-17 ka BP, and progressing into the Holocene. When regressed on the global ocean temperature and CO2 trends, we can see a proportionate response to the forcing during the last glacial maximum, the deglaciation and the early Holocene. In contrast, the late Holocene is characterised by continued compositional change, which does not appear related to environmental forcing. We speculate that this decoupling indicates the existence of a multi-millennial delay in community change following the climatic forcing, likely due to biotic interactions acting on communities that have been newly assembled or geographically displaced due to abiotic forcing. We will present a similar analysis for marine phytoplankton and discuss the consequences of the observations for the understanding of community variability on millennial time scales.

La reconstrucción de la temperatura de la superficie del mar (TSM) ha estado durante mucho tiempo en el centro de la investigación paleoceanográfica. Los estudios en el Mediterráneo no han sido una excepción, ya que la reconstrucción cuantitativa de TSM en esta cuenca semicerrada es crucial para comprender el cambio climático pasado en la región. Muchos de estos métodos se basaron en foraminíferos planctónicos, tanto en su geoquímica de caparazón como en la composición de los ensamblajes (por ejemplo, funciones de transferencia). Comprender y modelar las relaciones entre el censo actual y las variables ambientales es la base para transformar los datos fósiles en estimaciones cuantitativas de estas variables. Aunque globalmente, los conjuntos de foraminíferos parecen estar determinados principalmente por la temperatura, en cuencas marginales como el Mediterráneo, In this study we attempt to determine which environmental parameters may control the variability of planktonic foraminifer assemblages in the modern Mediterranean. For this purpose, census counts of planktonic foraminifera assemblages from Mediterranean coretops (ForCenS data base) have been integrated with monthly estimates of SST, chlorophyll concentration, and vertical gradients of various parameters as proxies for water column stratification/mixing (WOA 1998). Redundancy Analysis (RDA) was used to evaluating the explanatory power and the collinearity among tested environmental parameters and a forward selection of variables was carried out to identify those explaining independently the largest share of the variance in the composition of planktonic foraminifera assemblages.Se identificaron nueve variables significativas. Tres de ellos corresponden a TSM, mientras que los otros seis se distribuyen entre las concentraciones de clorofila superficial (2) y los gradientes térmicos verticales (4). Las variables más explicativas son la TSM de junio (R 2 0.43) y el gradiente térmico vertical de diciembre (R 2 0.15).

Porosity in planktonic foraminifers (the proportion of the shell surface covered by pores) is a conspicuous quantitative trait, well preserved in fossil shells and implicated as a source of environmental information. Despite its potential, the functional importance of porosity remains poorly understood. It is likely that pores are important in gas exchange, and differences in shell porosity among species or within species may reflect differences in metabolic rates or ambient oxygen concentration. Theoretically, porosity also affects the weight of the shell; and differences in porosity may reflect an adaptation to the specific density of the seawater or differences in allocation of resources to calcification (shell calcification intensity). Finally, there is evidence that porosity may differ between closely related cryptic species. Here we analyzed the potential role of porosity as a regulator of calcification intensity in Orbulina universa by combining biometric measurements based on sediment surface samples from the western Atlantic with a modelling approach. Specimens of O. universa were analyzed concerning their shell size, shell thickness, and shell porosity under light and scanning electron microscopy, and weighed using a microbalance. The resulting empirically derived model shows an effect size of shell thickness that is 7.5 times larger than the effect of shell porosity on the overall shell calcification intensity. This indicates that porosity is unlikely to be used by this species to regulate calcification intensity. By implementing the model on literature data which analyzed calcification intensity in O. universa, we also show that porosity differences among cryptic species in O. universa are unlikely to explain the observed differences in calcification intensity within the species. These findings indicate that functional explanations for differences in porosity in planktonic foraminifers have to be sought outside of calcification or density regulation and, conversely, that the observed differences in calcification intensity are likely driven by shell thickness and their relationship with environmental forcing can be applied without correction for porosity.

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.

Foraminiferal Na/Ca in planktonic and benthic foraminifers is a promising new method to assess directly past seawater salinities, which complements existing approaches (e.g., paired shell Mg/Ca and δ18O, shell Ba/Ca). Recent culture and field calibration studies have shown a significant positive relationship of Na incorporation into foraminiferal calcite shells with increasing salinity [1, 2], as confirmed by our culture study of Trilobatus sacculifer [3]. However, we note that the sensitivity of Na/Ca in response to salinity changes is species-specific and regional dependent, whereas temperature could be excluded as a secondary influencing factor [2, 3, 5]. Na/Ca values vary from 1–3 mmol/mol for the same salinity within and between foraminiferal species, suggesting a dominant biological control. To further evaluate the robustness of Na/Ca for its application as a reliable proxy, we here examine possible secondary controls on foraminiferal Na/Ca with new data for commonly used species for paleoreconstructions (Globigerinoides elongatus, G. ruber (pink), Orbulina universa, Globigerina bulloides, Neogloboquadrina dutertrei) collected by plankton tows in the eastern tropical North Atlantic during R/V Meteor cruise M140. We performed laser ablation ICP-MS measurements on single foraminiferal shells from depth-resolved plankton tows in 20 m net-intervals from locations where salinity was essentially constant, while seawater pH and total alkalinity differed by ~0.5 and 100 µmol/kg, respectively. Plankton tow samples provide new insights into the possible effects of natural variations in carbonate system parameters on Na incorporation into calcite tests with increasing water depth. The comparison of living foraminifers to sedimentary shells gives further information about the preservation state of Na/Ca in calcite shells over time, whereas fossil shells have mostly undergone gametogenesis during their life-time, or were affected post mortem by early diagenesis (sedimentation) processes. Those foraminifers were collected from surface sediments (M65-1) located in proximity to plankton tows. Our results show that all measured species, either from plankton tows or buried in the sediment, are within the Na/Ca range of previous studies [1-5], which increases the confidence for a robust Na/Ca to salinity proxy. However, the offset of ~2-5 mmol/mol between living foraminifers collected in surface waters (0-20 m) and fossil assemblages of the same species could be related to spine loss at the end of a foraminiferal life cycle [4]. In addition, the usage of inconsistent test sizes could further influence the foraminiferal Na/Ca signal. Our results reveal significant (R = -0.97, p) decreasing Na/Ca values with increasing test sizes between 180-250 µm for G. ruber (pink, white), N. dutertei and T. sacculifer, whereas values increase again with larger size classes >355 µm (R = 0.87, p [1] Wit et al. (2013) Biogeosciences 10, 6375-6387. [2] Mezger et al. (2016) Paleoceanography 31, 1562-1582. [3] Bertlich et al. (2018) Biogeosciences 15, 5991–6018.[4] Mezger et al. (2019) Biogeosciences 16, 1147-1165, 2019. [5] Allen et al. (2016) Geochim. Cosmochim. Acta 193, 197-221.

The boron isotopic composition of planktonic foraminiferal shell calcite ( δ 11 B Cc ) provides valuable information on the pH of ambient water at the time of calcification. Hence, δ 11 B Cc of fossil surface-dwelling planktonic foraminifera can be used to reconstruct ancient aqueous p CO 2 if information on a second carbonate system parameter, temperature and salinity is available. However, pH and p CO 2 of surface waters may vary seasonally, largely due to changes in temperature, DIC, and alkalinity. As also the shell fluxes of planktonic foraminifera show species-specific seasonal patterns that are linked to intra-annual changes in temperature, it is obvious that δ 11 B Cc of a certain species reflects the pH and thus p CO 2 biased towards a specific time period within a year. This is important to consider for the interpretation of fossil δ 11 B Cc records that may mirror seasonal pH signals. Here we present new Multi-Collector Inductively Coupled Mass Spectrometry (MC-ICPMS) δ 11 B Cc coretop data for the planktonic foraminifera species Globigerina bulloides , Globigerinoides ruber , Trilobatus sacculifer and Orbulina universa and compare them with δ 11 B borate derived from seasonally resolved carbonate system parameters. We show that the inferred season-adjusted δ 11 B Cc / δ 11 B borate relationships are similar to existing calibrations and can be combined with published δ 11 B Cc field and culture data to augment paleo-pH calibrations. To test the applicability of these calibrations, we used a core drilled on the Walvis Ridge in the Southeast Atlantic spanning the last 330,000 years to reconstruct changes in surface-water p CO 2 . The reconstruction based on G. bulloides , which reflects the austral spring season, was shown to yield values that closely resemble the Vostok ice-core data indicating that surface-water p CO 2 was close to equilibrium with the atmosphere during the cooler spring season. In contrast, p CO 2 estimated from δ 11 B Cc of O. universa , T. sacculifer and G. ruber that predominantly lived during the warmer seasons, exhibits up to ∼50 ppmv higher values than the Vostok ice-core data. This is probably due to the higher austral summer and fall temperatures, as shown by Mg/Ca to be on average ∼4 °C higher than during the cooler spring season, accounting for an increase in p CO 2 of ∼4% per 1 °C. Our results demonstrate that paleo-pH estimates based on δ 11 B Cc contain a significant seasonal signal reflecting the habitat preference of the recording foraminifera species.

Made available in DSpace on 2022-04-29T08:28:26Z (GMT). No. of bitstreams: 0 Previous issue date: 2019-12-01 German Academic Exchange Service London Natural Environment Research Council Aim: Many clades display the macroevolutionary pattern of a negative relationship between standing diversity and diversification rates. Competition among species has been proposed as the main mechanism that explains this pattern. However, we currently lack empirical insight into how the effects of individual-level ecological interactions scale up to affect species diversification. Here, we investigate a clade that shows evidence for negative diversity-dependent diversification in the fossil record and test whether the clade's modern communities show a corresponding signal of interspecific competition. Location: World's oceans. Time period: Holocene. Major taxa studied: Planktonic Foraminifera (Rhizaria). Methods: We explore spatial and temporal ecological patterns expected under interspecific competition. Firstly, we use a community phylogenetics approach to test for signs of local competitive exclusion among ecologically similar species (defined as closely related or of similar shell sizes) by combining species relative abundances in seafloor sediments. Secondly, we analyse whether population abundances of co-occurring species covary negatively through time using sediment trap time-series spanning 1–12 years. Results: The great majority of the assemblages are indistinguishable from randomly assembled communities, showing no significant spatial co-occurrence patterns regarding phylogeny or size similarity. Through time, most species pairs correlated positively, indicating synchronous rather than compensatory population dynamics. Main conclusions: We found no detectable evidence for interspecific competition structuring extant planktonic Foraminifera communities. Species co-occurrences and population dynamics are likely regulated by the abiotic environment and/or distantly related species, rather than intra-clade density-dependent processes. This interpretation contradicts the idea that competition drives the clade's macroevolutionary dynamics. One way to better integrate community ecology and macroevolution is to consider that diversification dynamics are influenced by groups that interact ecologically even when distantly related. Ocean and Earth Science National Oceanography Centre Southampton University of Southampton Center for Marine Environmental Sciences University of Bremen Department of Zoology University of British Columbia Instituto de Física Teórica Universidade Estadual de São Paulo School of Geography Earth and Environmental Science University of Birmingham Instituto de Física Teórica Universidade Estadual de São Paulo German Academic Exchange Service London: DAAD 2016/17 57210260 Natural Environment Research Council: NE/J018163/1 Natural Environment Research Council: NE/P019269/1

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. Seafloor-derived planktonic foraminifera communities of pre-industrial age are compared with communities from sediment-trap time series and show that Anthropocene communities of a globally distributed zooplankton group differ from their unperturbed pre-industrial state.

Photosymbiosis has played a key role in the diversification of foraminifera and their carbonate production throughout geologic history. However, identification of photosymbiosis in extinct taxa remains challenging, and even among the extant species the occurrence and functional relevance of photosymbiosis remain poorly constrained. Here, we investigate photosymbiosis in living planktonic foraminifera by measuring active chlorophyll fluorescence with fast repetition rate fluorometry. This method provides unequivocal evidence for the presence of photosynthetic capacity in individual foraminifera, and it allows us to characterize multiple features of symbiont photosynthesis including chlorophyll a (Chl a) content, potential photosynthetic activity (Fv∕Fm), and light-absorption efficiency (σPSII). To obtain robust evidence for the occurrence and importance of photosymbiosis in modern planktonic foraminifera, we conducted measurements on 1266 individuals from 30 species of the families Globigerinidae, Hastigerinidae, Globorotaliidae, and Candeinidae. Among the studied species, 19 were recognized as symbiotic and 11 as non-symbiotic. Of these, six species were newly confirmed as symbiotic and five as non-symbiotic. Photosymbiotic species have been identified in all families except the Hastigerinidae. A significant positive correlation between test size and Chl a content, found in 16 species, is interpreted as symbiont abundance scaled to the growth of the host and is consistent with persistent possession of symbionts through the lifetime of the foraminifera. The remaining three symbiont-bearing species did not show such a relationship, and their Fv∕Fm values were comparatively low, indicating that their symbionts do not grow once acquired from the environment. The objectively quantified photosymbiotic characteristics have been used to design a metric of photosymbiosis, which allows the studied species to be classified along a gradient of photosynthetic activity, providing a framework for future ecological and physiological investigations of planktonic foraminifera.

Synopsis: Sea surface temperature (SST) refers to the state of the uppermost “mixed” layer of the ocean, typically only few tens of meters thick. Knowledge of past SST variability is important as it helps us to understand how the ocean behaves in times of climate change, it allows us to validate numerical climate models and assess the significance of current climate trends. Temperature affects a range of thermodynamic, metabolic and biological processes that leave their signature in the geological record. Past SST can be reconstructed from fossil remains of phyto- and zooplankton in marine sediments and from skeletons of hermatypic corals. Geochemical paleothermometers are based on the analysis of oxygen isotopes and Mg/Ca in planktonic foraminifera and oxygen isotopes and Sr/Ca in corals. Biomarker methods are based on the measurement of various types of alkenones produced by haptophyte algae and crenarchaeotal membrane lipids in the organic matter in sediments. The composition of microfossil assemblages (planktonic foraminifera, diatoms, radiolarians and dinoflagellate cysts) in modern sediments is used to develop transfer functions to convert census counts in fossil samples to SST. The standard errors of environmental calibrations of paleothermometers range between 0.5 and 2°C; resolution of SST reconstructions in marine sediments is typically 10-100 years, corals allow yearly to monthly resolution.

Planktonic foraminifera and calcareous nannoplankton were analyzed in core Ocean Drilling Program Site 975, located in the western Mediterranean, in order to study their response to environmental changes across the Mid-Brunhes interval and specifically through Marine Isotope Stage (MIS) 15 and 8 (ca. 650–230 ka). Multivariate analysis of assemblage composition revealed that the calcareous plankton dynamics were mainly driven by surface water temperatures both on glacial-interglacial and stadial-interstadial time scales. Throughout the studied interval, foraminiferal and nannoplankton assemblages responded to environmental forcing in concert, except during MIS 15, when multiple environmental factors appear to have been superimposed on the otherwise dominating effect of temperature variability. Sea surface temperature (SST) has been estimated from planktonic foraminiferal assemblages using the artificial neural networks method pointing out relevant seasonal variations through the record. Our reconstructions reveal that calcareous plankton assemblages also responded to other environmental factors than temperature, including modification in surface water stratification, nutrient availability and detrital input. Specifically, a more stable, stratified water column seems to have accompanied the interval through MIS 15–13. On the other hand, across the Mid-Brunhes interval, from MIS 12 onwards, the enhanced glacial strength affected both planktonic foraminifera and calcareous nannofossils: planktonic foraminifera indicate that mixed and productive surface waters developed during glacials and stadials, accompanied by episodes of increased detrital input as suggested by calcareous nannoplankton assemblages. Enhanced food availability was likely driven by wind-induced upwelling and/or by continental coastal input during dry conditions persisting in the Mediterranean region and over North Africa. Finally, spectral and wavelet analyses of calcareous plankton time series allowed to identify the pattern of periodic response of the plankton at Milankovitch cycles and, in some cases, at millennial variability. The dominant 100 kyr periodicity recorded in surface water temperature proxies clearly reflects a major response of the planktonic community to the global glacial-interglacial climate pattern. High-frequency variation (~ 5–8, ~ 11–13 ky) of surface water temperature proxies and of selected taxa abundance highlights the occurrence of millennial-scale instability superimposed on the paleoenvironmental modifications occurring through the Mid-Brunhes interval climate transition. This framework accounts for the occurrence of different surface water dynamics across the Mid-Brunhes interval and is in favor of the hypothesis that the millennial scale surface water temperature variations are modulated by the harmonics of the precession forcing.

The use of planktonic foraminifera in paleoceanographic studies relies on the assumption that morphospecies represent biological species with ecological preferences that are stable through time and space. However, genetic surveys unveiled a considerable level of diversity in most morphospecies of planktonic foraminifera. This diversity is significant for paleoceanographic applications because cryptic species were shown to display distinct ecological preferences that could potentially help refine paleoceanographic proxies. Subtle morphological differences between cryptic species of planktonic foraminifera have been reported, but so far their applicability within paleoceanographic studies remains largely unexplored. Here we show how information on genetic diversity can be transferred to paleoceanography using Globorotalia inflata as a case study. The two cryptic species of G. inflata are separated by the Brazil-Malvinas Confluence (BMC), a major oceanographic feature in the South Atlantic. Based on this observation, we developed a morphological model of cryptic species detection in core top material. The application of the cryptic species detection model to Holocene samples implies latitudinal oscillations in the position of the confluence that are largely consistent with reconstructions obtained from stable isotope data. We show that the occurrence of cryptic species in G. inflata, can be detected in the fossil record and used to trace the migration of the BMC. Since a similar degree of morphological separation as in G. inflata has been reported from other species of planktonic foraminifera, the approach presented in this study can potentially yield a wealth of new paleoceanographical proxies.

The reproductive behavior of planktonic foraminifera is an important variable for the interpretation of paleoproxies based on their shells and for the understanding of the role of these organisms in oceanic carbonate flux. Observations from plankton tows have initially provided evidence for the existence of reproductive cycles synchronized with lunar phases in several species. However, subsequent observations from sediment traps yielded inconclusive results. Here we report shell flux data of four key species of planktonic foraminifera (Trilobatus sacculifer, Globigerinoides ruber, Orbulina universa and Neogloboquadrina dutertrei) from multiple deployments of a high-resolution (3-7 days) sediment trap in the southwestern Atlantic. Despite the potential bias related to lateral advection at the shallow deployment depths of the traps, the unusually high sampling resolution makes it possible to better constrain the short-term (lunar) dynamics of shell flux than most previous studies. Using periodic regression on the high-resolution series, we detected for all species evidence for a single flux maximum during one lunar cycle, occurring approximately 4-6 days after the full moon. In this series, 44-52 % of the shell flux in the deep (100 m) trap occurred during the last quarter. Different flux behavior between the shallow (50 m) and the deep (100 m) traps co-located on the same mooring revealed evidence for migration to deeper levels prior to reproduction in T. sacculifer. Although a monthly peak in shell flux was observed in the 3-day resolution deployment, its signature disappeared when all deployments were analyzed together. This analysis still reveals an elevated flux during the last quarter of the lunar cycle, but it seems that the period of the reproductive cycle is not fixed in time. Combined with aliasing at the sampling resolution of 5-7 days, this variable timing overwhelms the strictly periodic component of the shell flux series. We conclude that planktonic foraminifera shell flux and thus the carbonate export to the seafloor is affected by periodicity in the lunar band, but that reproduction does not seem to occur at exactly the same day of the lunar cycle in each month.

International audience; Planktonic foraminifer tests are major archives of environmental change and provide a multitude of proxies in paleoceanography and paleoclimatology. The application of such proxies is contingent upon a collaborative effort to better understand how the living organisms record the properties of their environment and how the resulting signals are recorded in marine sediments. In this contribution, we provide a review of the rapidly developing sub-fields of research, where new advances have been made possibleby technological developments, and by cross-disciplinary work of the scientific community. Following brief historical overviews of the sub-fields, we discuss the latest advances in planktonic foraminifer research and highlight the resulting new perspectives in ocean and climate research. Natural classification based on consistent species concepts forms the basis for analysis of any foraminifer-derived proxy. New approaches in taxonomy and phylogeny of Cenozoic planktonic foraminifers (Section 2) are presented, highlighting new perspectives on sensitivity and response of planktonic foraminifers to the changing climate and environment (Section 4). Calibration of foraminifer-specific data and environmental parameters is improving along with the technical development of probes and the access to samples from the natural environment (Section 3), enhancing our understanding of the ever-changing climate and ocean system. Comprehension of sedimentation and flux dynamics facilitates maximum gain of information from fossil assemblages (Section 5). Subtle changes in the physical (e.g., temperature), chemical (e.g., pH), and biological (e.g., food) conditions of ambient seawater affect the abundance of species and composition of assemblages as well as the chemical composition of the foraminifer shell and provide increasingly-detailed proxy data on paleoenvironments (Section 6).

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 (Trilobatus sacculifer, Globigerinoides conglobatus, Globigerinella siphonifera, Pulleniatina obliquiloculata, Globorotalia truncatulinoides), other species show no relationships between size and the studied covariates (Globigerinoides ruber, Neogloboquadrina dutertrei, Globorotalia menardii, Globoconella inflata). 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., Using a recently digitized museum collection, we investigate how planktonic foraminifera species vary in size across biogeographical scales. We found that the relationships between shell size and the explanatory variables (temperature, net primary productivity, and local relative abundance) differ among the nine studied species, contrary to the idea that species are largest at their environmental optima.

We demonstrate that the temperature signal in the planktonic foraminifera assemblage data from the North Atlantic typically does not originate from near surface waters and argue that this has the potential to bias sea surface temperature reconstructions using transfer functions calibrated against near surface temperatures if the thermal structure of the upper few hundred metres of ocean changes over time. CMIP5 climate models indicate that ocean thermal structure in the N Atlantic changed between the Last Glacial Maximum (LGM) and the pre-industrial (PI), with some regions, mainly in the tropics, of the LGM ocean lacking good thermal analogues in the PI. Transfer functions calibrated against different depths reconstruct a marked subsurface cooling in the tropical Atlantic during the last glacial, in contrast to previous studies that reconstructed only a modest cooling. These possible biases in temperatures reconstructions may affect estimates of climate sensitivity based on the difference between LGM and pre-industrial climate. Quantifying these biases has the potential to alter our understanding of Last Glacial Maximum climate and improve estimates of climate sensitivity.

The ocean-the Earth's largest ecosystem-is increasingly affected by anthropogenic climate change

The transition from benthos to plankton requires multiple adaptations, yet so far it remains unclear how these are acquired in the course of the transition. To investigate this process, we analyzed the genetic diversity and distribution patterns of a group of foraminifera of the genus Bolivina with a tychopelagic mode of life (same species occurring both in benthos and plankton). We assembled a global sequence data set for this group from single-cell DNA extractions and occurrences in metabarcodes from pelagic environmental samples. The pelagic sequences all cluster within a single monophyletic clade within Bolivina. This clade harbors three distinct genetic lineages, which are associated with incipient morphological differentiation. All lineages occur in the plankton and benthos, but only one lineage exhibits no limit to offshore dispersal and has been shown to grow in the plankton. These observations indicate that the emergence of buoyancy regulation within the clade preceded the evolution of pelagic feeding and that the evolution of both traits was not channeled into a full transition into the plankton. We infer that in foraminifera, colonization of the planktonic niche may occur by sequential cooptation of independently acquired traits, with holoplanktonic species being recruited from tychopelagic ancestors

Past river run-off is an important measure for the continental hydrological cycle and the assessment of freshwater input into the ocean. However, paleosalinity reconstructions applying different proxies in parallel often show offsets between the respective methods. Here, we compare the established foraminiferal Ba/Ca and View the MathML source salinity proxies for their capability to record the highly seasonal Orinoco freshwater plume in the eastern Caribbean. For this purpose we obtained a data set comprising Ba/Ca and View the MathML source determined on multiple species of planktonic foraminifera from core tops distributed around the Orinoco River mouth. Our findings indicate that interpretations based on either proxy could lead to different conclusions. In particular, Ba/Ca and View the MathML source diverge in their spatial distribution due to different governing factors. Apparently, the Orinoco freshwater plume is best tracked by Ba/Ca ratios of G. ruber (pink and sensu lato morphotypes), while View the MathML source based on the same species is more related to the local precipitation-evaporation balance overprinting the riverine freshwater contribution. Other shallow dwelling species (G. sacculifer, O. universa) show a muted response to the freshwater discharge, most likely due to their ecological and habitat preferences. Extremely high Ba/Ca ratios recorded by G. ruber are attributed to Ba2+-desorption from suspended matter derived from the Orinoco. Samples taken most proximal to the freshwater source do not show pronounced Ba/Ca or View the MathML source anomalies. Here, the suspension loaded freshwater lid developing during maximum discharge suppresses foraminiferal populations. Both proxies are therefore biased towards dry season conditions at these sites, when surface salinity is only minimally reduced.

Deep-sea sediments constitute a unique archive of ocean change, fueled by a permanent rain of mineral and organic remains from the surface ocean. Until now, paleo-ecological analyses of this archive have been mostly based on information from taxa leaving fossils. In theory, environmental DNA (eDNA) in the sediment has the potential to provide information on non-fossilized taxa, allowing more comprehensive interpretations of the fossil record. Yet, the process controlling the transport and deposition of eDNA onto the sediment and the extent to which it preserves the features of past oceanic biota remains unknown. Planktonic foraminifera are the ideal taxa to allow an assessment of the eDNA signal modification during deposition because their fossils are well preserved in the sediment and their morphological taxonomy is documented by DNA barcodes. Specifically, we re-analyze foraminiferal-specific metabarcodes from 31 deep-sea sediment samples, which were shown to contain a small fraction of sequences from planktonic foraminifera. We confirm that the largest portion of the metabarcode originates from benthic bottom-dwelling foraminifera, representing the in-situ community, but a small portion (

International audience; 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. [Cryptic species; genetic diversity; planktonic foraminifera; molecular nomenclature; MOTUs.]

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.

article i nfo Recent SSU rDNA sequence data of the paleoceanographically important planktonic foraminifer species Globigerinoides ruber showed the presence of two distinct phylogenetic lineages within this morphotaxon. The first lineage (G. ruber sensu stricto) includes the genetic type that corresponds to pink-pigmented G. ruber, as well as three of the five genetic types recognised in individuals of "white" G. ruber (labelled Type Ia, Type Ib and Type Ib2). The remaining two genetic types of G. ruber (white), labelled as Types IIa and IIb, represent a distinct phylogenetic lineage (G. ruber sensu lato), closer related to Globigerinoides conglobatus. Here we combine molecular clock and morphometric analyses to shed light on the taxonomical and phylogenetic significance of the presence of these two distinct lineages within the morphotaxon G. ruber .A molecular clock approach suggests a rather recent origin of the G. ruber sensu stricto lineage in the late Miocene and a split between G. ruber (pink) and the "white" genotypes Ia, Ib and Ib2 around 6 Ma. This indicates that all records of G. ruber prior to the G. ruber "pseudo-extinction" event at 8 Ma refer to an unrelated species (Globigerinoides subquadratus) and that the G. ruber (pink) lineage is substantially older than the first appearance of the pink pigmentation in the fossil record. In order to establish the taxonomic identity of the G. ruber sensu lato phylogenetic lineage, we conducted morphometric measurements on (i) pictures of specimens with known genetic identity, (ii) shells from sediment samples, (iii) specimens assigned to G. ruber and Globigerinoides elongatus from a museum collection and (iv) pictures of G. ruber sensu lato morphotype from recent literature. Our results suggest that specimens of Type IIa that represent the G. ruber sensu lato lineage are morphologically identical to the concept of the G. ruber sensu lato morphotype in recent literature, and that these morphotypes are consistent with the species definition of Globigerinoides elongatus. We therefore propose that the name G. elongatus (sensu d'Orbigny) should be reinstated and used for the genetic Type IIa. The name G. ruber (sensu d'Orbigny) should be reserved for specimens of the pink chromotype. Specimens of Types Ia, Ib and Ib2 require new species names, but our data are not sufficient to provide a morphological character separating these species from their sister G. ruber (pink), other than by their shell colouration.

article i nfo The chemical composition of shells of the planktonic foraminifer Globigerinoides ruber (white) is frequently used to determine past sea surface conditions. Recently, it has been shown that arbitrarily defined morphotypes within this species exhibit different chemical and isotopic signatures. Here, we investigate the occurrence through time and in space of morphological types of G. ruber (white) in late Quaternary and Holocene sediments of the central and the eastern Mediterranean Sea. In 115 samples representing two distinct time intervals (MIS 1-2 and MIS 9-12) at ODP Site 964 and the piston core GeoTu-SL96, we have defined three morphological types within this species and determined their relative abundances and stable isotopic composition. A quantitative analysis of morphological variation within G. ruber (white) in four samples revealed that the subjectively defined morphotypes occupy separate segments of a continuous and homogenous morphospace. We further show that the abundance of the morphotypes changes significantly between glacials and interglacials and that the three morphotypes of G. ruber show significant offsets in their stable isotopic composition. These offsets are consistent within glacial and interglacial stages but their sign is systematically reversed between the two Sites. Since the isotopic shifts among the three G. ruber morphotypes are systematic and often exceed 1‰, their understanding is essential for the interpretation of all G. ruber-based proxy records for the paleoceanographic development of the Mediterranean during the late

article i nfo The Red Sea is an extreme marine environment, with conditions limiting the application of standard geochemical proxies for the reconstruction of paleoclimate. In order to develop paleoenvironmental reconstruction methods which are not dependent on chemical signals, we investigated the distribution of planktonic foraminifera in the surface sediments and assessed the viability of constructing foraminiferal transfer functions in this basin. We find a distinct gradient in the faunal assemblage along the basin's axis, which is reflected in a high correlation between faunal composition and all considered environmental parameters (temperature, salinity, chlorophyll a concentration, stratification, and oxycline depth). As a result, transfer functions constructed by different methods (ANN, MAT, IKM, WA-PLS) appear to be able to estimate all of these parameters with a high average accuracy (15% of the parameter's range in the Red Sea). However, redundancy analysis of the distribution of foraminiferal assemblages in surface sediments alone did not yield unambiguous results in terms of which of the considered factors exerts a primary control on the foraminifera distribution and which of the observed relationships are the result of the mutual correlation among the environmental factors. To disentangle the effect of individual environmental parameters, we applied the obtained transfer functions on a newly generated Holocene record from the central Red Sea. The integration of published paleoclimate reconstructions with our data allowed us to identify productivity as the most likely primary control of the planktonic foraminifera distribution in the Red Sea. The generated transfer functions can estimate paleoproductivity with acceptable accuracy (RMSEP chlorophyll a=0.1 mg/m 3

We present SSU rDNA data resolving the seasonal and geographical distribution of 'cryptic' genetic types of the planktonic foraminifer morphospecies Globigerinoides ruber in the eastern Atlantic Ocean and the Mediterranean Sea. Analysis of 262 sequences revealed the presence of five genetic types belonging to two distinct lineages. Although the morphospecies G. ruber occurs throughout the investigated region, its constituent 'cryptic' genetic types show a pattern of widespread exclusion, which is difficult to reconcile with the concept of ubiquitous dispersal. One of the newly discovered genetic types was exclusively found at stations in the Mediterranean Sea, possibly representing the smallest-scale example of endemism known in planktonic foraminifera. In general, our results suggest that the geographical scale of mutual exclusion between the genotypes is negatively correlated with their phylogenetic relatedness: the most similar and most recently diverged pair of siblings showed the strongest evidence for small-scale competitive exclusion. This pattern is consistent with the concept of niche partitioning, implying decreasing level of competition between genetic types with increasing degree of genetic divergence.

Sea level during the last interglacial stood at least 4 m higher than at present, with evidence of short-term fluctuations of up to 10 m. A new continuous sea level record from the Red Sea and coral ages suggest that during these fluctuations, sea level changes were on the order of 1.6 m per century. The last interglacial period, Marine Isotope Stage (MIS) 5e, was characterized by global mean surface temperatures that were at least 2 ∘C warmer than present1. Mean sea level stood 4–6 m higher than modern sea level2,3,4,5,6,7,8,9,10,11,12,13, with an important contribution from a reduction of the Greenland ice sheet1,14. Although some fossil reef data indicate sea-level fluctuations of up to 10 m around the mean3,4,5,6,7,8,9,11, so far it has not been possible to constrain the duration and rates of change of these shorter-term variations. Here, we use a combination of a continuous high-resolution sea-level record, based on the stable oxygen isotopes of planktonic foraminifera from the central Red Sea15,16,17,18, and age constraints from coral data to estimate rates of sea-level change during MIS-5e. We find average rates of sea-level rise of 1.6 m per century. As global mean temperatures during MIS-5e were comparable to projections for future climate change under the influence of anthropogenic greenhouse-gas emissions19,20, these observed rates of sea-level change inform the ongoing debate about high versus low rates of sea-level rise in the coming century21,22.

Species distribution patterns in planktonic foraminiferal assemblages are fundamental to the understanding of the determinants of their ecology. Until now, data used to identify such distribution patterns was mainly acquired using the standard > 150 μm sieve size. However, given that assemblage shell size-range in planktonic foraminifera is not constant, this data acquisition practice could introduce artefacts in the distributional data. Here, we investigated the link between assemblage shell size-range and diversity in Recent planktonic foraminifera by analysing multiple sieve-size fractions in 12 samples spanning all bioprovinces of the Atlantic Ocean. Using five diversity indices covering various aspects of community structure, we found that counts from the > 63 μm fraction in polar oceans and the > 125 μm elsewhere sufficiently approximate maximum diversity in all Recent assemblages. Diversity values based on counts from the > 150 μm fraction significantly underestimate maximum diversity in the polar — and surprisingly also in the tropical provinces. Although the new methodology changes the shape of the diversity/sea-surface temperature (SST) relationship, its strength appears unaffected. Our analysis reveals that increasing diversity in planktonic foraminiferal assemblages is coupled with a progressive addition of larger species that have distinct, offset shell-size distributions. Thus, the previously documented increase in overall assemblage shell size-range towards lower latitudes is linked to an expanding shell-size disparity between species from the same locality. This observation supports the idea that diversity and shell size-range disparity in foraminiferal assemblages are the result of niche separation. Increasing SST leads to enhanced surface water stratification and results in vertical niche separation, which permits ecological specialisation. Specific deviations from the overall diversity and shell-size disparity latitudinal pattern are seen in regions of surface-water instability, indicating that coupled shell-size and diversity measurements could be used to reconstruct water column structures of past oceans.

The high-latitude planktonic foraminifera have proved to be particularly useful model organisms for the study of global patterns of vicariance and gene flow in the oceans. Such studies demonstrate that gene flow can occur over enormous distances in the pelagic marine environment leading to cosmopolitanism but also that there are ecological and geographical barriers to gene flow producing biogeographic structure. Here, we have undertaken a comprehensive global study of genetic diversity within a marine protist species, the high-latitude planktonic foraminiferan Neogloboquadrina pachyderma . We present extensive new data sets from the North Pacific and Arctic Oceans that, in combination with our earlier data from the North Atlantic and Southern Oceans, allow us to determine the global phylogeography of this species. The new genetic data reveal a pattern of Arctic circumpolar isolation and bipolar asymmetry between the Atlantic and Pacific Oceans. We show that the ancestry of North Pacific N. pachyderma is relatively recent. It lies within the upwelling systems and subpolar waters of the Southern Hemisphere and remarkably not within the neighboring Arctic Ocean. Instead, the Arctic Ocean population forms a genetic continuum with the North Atlantic population, which became isolated from the southern populations much earlier, after the onset of Northern hemisphere glaciation. Data from the planktonic foraminiferal morphospecies Globigerina bulloides is also introduced to highlight the isolation and endemism found within the subpolar North Pacific gyre. These data provide perspective for interpretation and discussion of global gene flow and speciation patterns in the plankton.

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.

We present a new reconstruction of Mediterranean sea surface temperatures (SST) during the last glacial maximum (LGM). A calibration data set based on census counts of 23 species of planktonic foraminifera in 129 North Atlantic and 145 Mediterranean core top samples was used to develop summer, winter and annual average SST reconstructions using artificial neural networks (ANNs) and the revised analogue method (RAM). Prediction errors determined by cross-validation of the calibration data set ranged between 0.5 and 1.1 °C, with both techniques being most successful in predicting winter SSTs. Glacial reconstructions are based on a new, expanded data set of 273 samples in 37 cores with consistent minimum level of age control. The new LGM reconstructions suggest that the east–west temperature gradient during the glacial summer was 9 °C, whereas during the glacial winter, the gradient was 6 °C, both some 4 °C higher than that existing today. In contrast to earlier studies, our results tend to suggest much cooler SST estimates throughout the glacial Mediterranean, particularly in the eastern basin where previous SST reconstructions indicated a decrease of only 1 °C. Our new SST reconstructions will provide the modelling community with a detailed and updated portrayal of the Mediterranean Sea during the LGM, setting new targets on which glacial simulations can be tested.

To understand the processes leading to the formation of Holocene sapropel S1 in the Eastern Mediterranean Sea, we integrated results from regional ocean-biogeochemical general circulation model experiments with biogeochemical and micropaleontological proxy records. Sapropel S1 formed during the Holocene insolation maximum, when strong Aegean north winds (Etesian) caused enhanced downwelling and mixing of warm surface waters in the Cretan and western Levantine seas accounting for the complex sea-surface temperature pattern derived from planktonic foraminiferal transfer functions. Our results support a scenario where sufficient organic matter for sapropel formation is buried under oligotrophic conditions in an anoxic water column refuting the “high-productivity” hypothesis. We reconstructed a synchronous shift in the state of deep-sea benthic ecosystems, documenting a rapid expansion of dysoxic to anoxic conditions with onset of S1 deposition. The recovery of benthic ecosystems during the terminal S1 phase was controlled by increasingly deeper convection and re-ventilation over a period of approximately 1,500 years.

International audience; Cryptic genetic species of planktonic Foraminifera often exhibit narrower biogeographic distributions and eco- logical preferences than the respective morphospecies. In theory, it should therefore be possible to improve the resolution of the paleoceanographic reconstructions based on sediment assemblages of these species. Here, we use observational data on the latitudinal distribution of 11 genotypes of Globigerina bulloides (including a newly described genotype), Orbulina universa, Truncorotalia truncatulinoides and Globoconella inflata in plank- ton tows from south Indian Ocean to model the relationship between their abundance and the sea surface tem- perature (SST). We then use this model to assess the potential benefit of knowing the ecological preferences of cryptic species on assemblage-based transfer functions. In doing so, we first apply this model to a database of as- semblage counts in 1334 surface sediment samples from the Southern Hemisphere and simulate the expected abundances of individual genotypes in sediment samples. This simulated dataset is used to calibrate three differ- ent transfer functions: the Imbrie and Kipp Method, Weighted Averaging Partial Least Squares and Modern Analog Technique. Trials show that such simulated splitting of morphospecies into their respective genotypes leads to a substantial (7 to 25%) overall reduction of the error rates of SST estimates in the calibration dataset. The degree of error rate reduction is sensitive to the increase of taxonomic richness in the simulated assemblages induced by the co-occurrence of genotypes of the same morphospecies. Although the studied species occur across a broad SST range, the largest reduction of error rate by the transfer functions is obtained within the 4 °C to 12 °C SST range, where most of the studied genotypes are found. Our results show that all genotypes are not expected to improve the accuracy of transfer functions at the same level: while integrating cryptic diver- sity in G. bulloides, T. truncatulinoides and G. inflata clearly improve assemblage-based SST reconstructions, geno- types of O. universa have a negligible effect.

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.

We present a new planktonic foraminifera model developed for the global ocean mixed-layer. The main purpose of the model is to explore the response of planktonic foraminifera to different boundary conditions in the geological past, and to quantify the seasonal bias in foraminifera-based paleoceanographic proxy records. This model is forced with hydrographic data and with biological information taken from an ecosystem model to predict monthly concentrations of the most common planktonic foraminifera species used in paleoceanography: N. pachyderma (sinistral and dextral varieties), G. bulloides, G. ruber (white variety) and G. sacculifer. The sensitivity of each species with respect to temperature (optimal temperature and range of tolerance) is derived from previous sediment-trap studies. Overall, the spatial distribution patterns of most of the species are in agreement with core-top data. N. pachyderma (sin.) is limited to polar regions, N. pachyderma (dex.) and G. bulloides are the most common species in high productivity zones, while G. ruber and G. sacculifer are more abundant in tropical and subtropical oligotrophic waters. For N. pachyderma (sin) and N. pachyderma (dex.), the season of maximum production coincides with that observed in sediment-trap records. Model and sediment-trap data for G. ruber and G. sacculifer show, in general, lower concentrations and less seasonal variability at all sites. A sensitivity experiment suggest that, within the temperature-tolerance range of a species, food availability may be the main parameter controlling its abundance.

Gradual evolution is a common phenomenon in the fossil record of marine microplankton, yet no theoretical model has so far been presented to explain the observed pattern of unidirectionality in trait evolution lasting over tens of millions of generations. Recent molecular genetic data show that the majority of microfossil-producing plankton groups harbors substantial cryptic diversity. Here, we examine the effect of cryptic diversity on apparent rates of lineage evolution. By using a theoretical approach, we show that under resource competition, an increasing number of sibling species within a hypothetical lineage leads to an exponential slowdown of the apparent rate of evolution. This mechanism explains both the remarkable variation in apparent rates of evolution observed in marine plankton, as well as the presence of long gradual evolutionary trends.

Publisher Summary This chapter focuses on the planktonic foraminifera as tracers of past oceanic environments. Paleoceanography has always been closely connected with the study of planktonic foraminifera. The prolific production and excellent preservation of foraminiferal fossils in oceanic sediments has produced probably the best fossil record on Earth, providing unparalleled archives of morphological change, faunal variations, and habitat characteristics. Planktonic foraminifera are the most common source of paleoceanographic proxies, be it through the properties of their fossil assemblages or as a substrate for extraction of geochemical signals. The steady rain of foraminiferal shells is responsible for the deposition of a large portion of deep-sea biogenic carbonate. Stable isotopic signals extracted from planktonic foraminifera soon became a standard tool for the recognition of glacial cycles and eventually facilitated the recognition of orbital pacing of the ice-ages. The chemical composition of foraminiferal calcite proved to be a fertile ground for the development of proxies. The chapter highlights the most common and most promising foraminiferal proxies and puts them in the context of modern biological knowledge.