Description: Anthropogenic impacts are perturbing the global nitrogen cycle via warming effects and pollutant sources such as chemical fertilizers and burning of fossil fuels. Understanding controls on past nitrogen inventories might improve predictions for future global biogeochemical cycling. Here we show the quantitative reconstruction of deglacial bottom water nitrate concentrations from intermediate depths of the Peruvian upwelling region, using foraminiferal pore density. Deglacial nitrate concentrations correlate strongly with downcore δ13C, consistent with modern water column observations in the intermediate Pacific, facilitating the use of δ13C records as a paleo-nitrate-proxy at intermediate depths and suggesting that the carbon and nitrogen cycles were closely coupled throughout the last deglaciation in the Peruvian upwelling region. Combining the pore density and intermediate Pacific δ13C records shows an elevated nitrate inventory of 〉10% during the Last Glacial Maximum relative to the Holocene, consistent with a δ13C-based and δ15N-based 3D ocean biogeochemical model and previous box modeling studies.

Description: Benthic foraminifera are unicellular eukaryotes inhabiting sediments of aquatic environments. Several species were shown to store and use nitrate for complete denitrification, a unique energy metabolism among eukaryotes. The population of benthic foraminifera reaches high densities in oxygen-depleted marine habitats, where they play a key role in the marine nitrogen cycle. However, the mechanisms of denitrification in foraminifera are still unknown, and the possibility of a contribution of associated bacteria is debated. Here, we present evidence for a novel eukaryotic denitrification pathway that is encoded in foraminiferal genomes. Large-scale genome and transcriptomes analyses reveal the presence of a denitrification pathway in foraminifera species of the genus Globobulimina. This includes the enzymes nitrite reductase (NirK) and nitric oxide reductase (Nor) as well as a wide range of nitrate transporters (Nrt). A phylogenetic reconstruction of the enzymes' evolutionary history uncovers evidence for an ancient acquisition of the foraminiferal denitrification pathway from prokaryotes. We propose a model for denitrification in foraminifera, where a common electron transport chain is used for anaerobic and aerobic respiration. The evolution of hybrid respiration in foraminifera likely contributed to their ecological success, which is well documented in palaeontological records since the Cambrian period.

Description: Present day oceans are well ventilated, with the exception of mid-depth oxygen minimum zones (OMZs) under high surface water productivity, regions of sluggish circulation, and restricted marginal basins. In the Mesozoic, however, entire oceanic basins transiently became dysoxic or anoxic. The Cretaceous ocean anoxic events (OAEs) were characterised by laminated organic-carbon rich shales and low-oxygen indicating trace fossils preserved in the sedimentary record. Yet assessments of the intensity and extent of Cretaceous near-bottom water oxygenation have been hampered by deep or long-term diagenesis and the evolution of marine biota serving as oxygen indicators in today's ocean. Sedimentary features similar to those found in Cretaceous strata were observed in deposits underlying Recent OMZs, where bottom-water oxygen levels, the flux of organic matter, and benthic life have been studied thoroughly. Their implications for constraining past bottom-water oxygenation are addressed in this review. We compared OMZ sediments from the Peruvian upwelling with deposits of the late Cenomanian OAE 2 from the north-west African shelf. Holocene laminated sediments are encountered at bottom-water oxygen levels of 〈 7 μmol kg−1 under the Peruvian upwelling and 〈 5 μmol kg−1 in California Borderland basins and the Pakistan Margin. Seasonal to decadal changes of sediment input are necessary to create laminae of different composition. However, bottom currents may shape similar textures that are difficult to discern from primary seasonal laminae. The millimetre-sized trace fossil Chondrites was commonly found in Cretaceous strata and Recent oxygen-depleted environments where its diameter increased with oxygen levels from 5 to 45 μmol kg−1. Chondrites has not been reported in Peruvian sediments but centimetre-sized crab burrows appeared around 10 μmol kg−1, which may indicate a minimum oxygen value for bioturbated Cretaceous strata. Organic carbon accumulation rates ranged from 0.7 and 2.8 g C cm−2 kyr−1 in laminated OAE 2 sections in Tarfaya Basin, Morocco, matching late Holocene accumulation rates of laminated Peruvian sediments under Recent oxygen levels below 5 μmol kg−1. Sediments deposited at 〉 10 μmol kg−1 showed an inverse exponential relationship of bottom-water oxygen levels and organic carbon accumulation depicting enhanced bioirrigation and decomposition of organic matter with increased oxygen supply. In the absence of seasonal laminations and under conditions of low burial diagenesis, this relationship may facilitate quantitative estimates of palaeo-oxygenation. Similarities and differences between Cretaceous OAEs and late Quaternary OMZs have to be further explored to improve our understanding of sedimentary systems under hypoxic conditions.

Description: The Peruvian Oxygen Minimum Zone (OMZ) is one of the strongest and most pronounced OMZs in today’s world oceans and thus is a key area to understand changing redox conditions in relation with changing climate. Vertical and horizontal changes or an extension of the OMZ through time and space are investigated using a sediment core from the lower OMZ boundary. This core has a complete record since the Last Glacial Maximum. We focus on time intervals Late Holocene, Early Holocene, Bølling Allerød, Heinrich-Stadial 1 and Last Glacial Maximum to investigate changes in bottom-water oxygen conditions by using benthic foraminiferal assemblages. Living benthic foraminiferal faunas are structured with the prevailing bottom-water oxygen concentrations today (Mallon et al., 2012). Bolivina species are frequent at the most oxygen-depleted conditions. Cassidulina and Uvigerina species dominate the faunas under higher oxygen concentrations. Downcore distribution of benthic foraminiferal assemblages showed fluctuations in the abundance of the indicator species depicting variations in past bottom-water oxygenation. In addition, changes in bottom-water nitrate concentrations are reconstructed by using the pore density in tests of Bolivina spissa (Glock et al., 2011) for the same time intervals. Combination of both proxies will provide information on past bottom-water conditions and changes of oxygen concentrations for the Peruvian margin.

Description: Benthic foraminifera have been used as proxies for the prevailing conditions at the sediment–water interface. Their distribution patterns are thought to facilitate reconstruction of past environmental conditions. Variations of bottom water oxygenation can be traced by the downcore distribution of benthic foraminifera and some of their morphological characters. Being one of the strongest and most pronounced OMZs in today’s world oceans, the Peruvian OMZ is a key area to study such variations in relation with changing climate. Spatial changes or an extension of the OMZ through time and space are investigated using sediment cores from the lower OMZ boundary. We focus on time intervals Late Holocene, Early Holocene, Bølling Allerød, Heinrich-Stadial 1 and Last Glacial Maximum (LGM) to investigate changes in bottom-water oxygen and redox conditions. The recent distributions of benthic foraminiferal assemblages provide background data for an interpretation of the past conditions. Living benthic foraminiferal faunas from the Peruvian margin are structured with the prevailing bottom-water oxygen concentrations today (Mallon et al., 2012). Downcore distribution of benthic foraminiferal assemblages showed fluctuations in the abundance of the indicator species depicting variations and a decreasing trend in bottom water oxygen conditions since the LGM. In addition, changes in bottom-water oxygen and nitrate concentrations are reconstructed for the same time intervals by the pore density in tests of Planulina limbata and Bolivina spissa (Glock et al., 2011), respectively. The pore densities also indicate a trend of higher oxygen and nitrate concentrations in the LGM compared to the Holocene. Combination of both proxies provide information on past bottom-water conditions and changes of oxygen concentrations for the Peruvian margin. Glock et al., 2011: Environmental influences on the pore density of Bolivina spissa (Cushman), Journal of Foraminiferal Research, v. 41, no. 1, p. 22–32. Mallon et al., 2012: The response of benthic foraminifera to low-oxygen conditions of the Peruvian oxygen minimum zone, in ANOXIA, pp.305-322.

Description: Highlights • Review of sediment archives from the Peruvian margin since the LGM. • Focus on the evolutionary feature of the hiatus found in archives. • Modern analogue for current-dominated environments for paleo reconstructions. • New results for erosional potential of the non-linear internal waves (NLIWs). Abstract The Peruvian continental margin is characterized by the presence of one of the strongest and most distinct Oxygen Minimum Zones (OMZs) in today's oceans. Therefore, it has long been in the focus of oceanographic and geological investigations. Observations indicate that OMZs are expanding in relation with currently changing climate. To advance understanding of the temporal evolution of OMZs and climate change, complete paleoceanographic and palaeoclimatological reconstructions are needed. However, the development of paleoenvironmental scenarios for the period since the Last Glacial Maximum at this region was hampered by a ubiquitous hiatus and short-term interruptions of the stratigraphical record. In the present study, we combined the stratigraphical information from 31 sediment cores from the Peruvian margin located between 3 and 18°S and water depths of 90 to 1300 m within and below today's OMZ, in order to determine the extent of the hiatus and assess the responsible mechanisms. A widespread unconformity and related erosional features, omission surfaces and phosphorites, were observed in sediment cores from the area south of 7°S, depicting a prograding feature on the continental slope from south to north during the deglaciation. Combining recent oceanographic and sedimentological observations, it is inferred that, tide-topography interaction and resulting non-linear internal waves (NLIWs) shape the slope by erosion, carry sediments upslope or downslope and leave widespread phosphoritic lag sediments, while the Peru Chile Undercurrent (PCUC) transports the resuspended sediments southward causing non-deposition. This exceptional sedimentary regime makes the Peruvian margin a modern analogue for such environments. Overall, our compilation of downcore records showed that enhanced bottom currents due to tide-topography interaction were progressively evolving and affected a wider area with the onset of the last deglaciation. Elevated tidal amplitudes and variability of mid-depth water masses (i.e.; density changes) and hydrodynamics in relation with changing climate were potential reasons of this evolving feature of erosion and reworking. Additionally, erosion and non-deposition was observed widest and even was encountered on the continental shelf during the early Holocene, potentially indicating a strong phase of the PCUC mirroring today's El Niño-like conditions.

Description: Oceanic oxygen decline due to anthropogenic climate change is a matter of growing concern. Tropical oxygen minimum zones (OMZs) are the most important areas of oxygen depletion in the modern oceans. A quantitative oxygen proxy in OMZs is highly desirable in order to identify and monitor recent dynamics as well as to reconstruct pre-Anthropocene changes in amplitude and extension of oxygen depletion. A previous study revealed that there are significant correlations between I/Ca ratios of foraminiferal bulk samples for different benthic foraminiferal species from the Peruvian OMZ. Nevertheless, species for which less specimens were available showed a higher variability between I/Ca ratios in different badges. To test if this might be related to intra- or inter-shell heterogeneity we focused on microanalyses of I/Ca ratios within these species in our present study. We developed a method for measuring benthic foraminiferal I/Ca ratios, a potential proxy for the reconstruction of marine oxygen concentrations. We applied 92 spot analyses in individual foraminiferal specimens from the Peruvian OMZ using secondary ion mass-spectrometry (SIMS). The I/Ca ratios on 8 of 11 cleaned Uvigerina striata and Planulina limbata specimens determined with SIMS showed no significant difference to previous ICP-MS measurements on bulk samples from the same species. This indicates that both techniques are suited to the analysis and that the applied cleaning protocols efficiently removed the strong iodine contaminations. Nevertheless, despite the highly significant correlation between bulk ICP-MS I/Ca ratios and bottom water oxygen concentrations for U. striata, no significant correlation was observed for the SIMS derived individual I/Ca ratios. This indicates that ICP-MS bulk analyses on pooled bulk samples might be more suitable for reliable oxygen reconstructions using I/Ca ratios. On the contrary, the strong intra-test (e.g. -shell) variations could be induced by the oxygen variability in the habitats of foraminifera. Therefore, the high resolution findings provide the perspective for tracking relative short term oxygen fluctuations by measuring ontogenetic changes in I/Ca ratios within individual foraminiferal tests. Measurements on cross-sections of uncleaned U. striata specimens revealed a strong contaminant iodine phase within the massive centre of the foraminiferal test walls which usually would be considered to be free of contamination. The contaminant iodine is probably associated to organic matter and located inside a microporous framework within the foraminiferal calcite. This might be related to microtubular structures which have been revealed in previous studies during early dissolution states of foraminiferal test walls.

Description: Benthic foraminifera populate a diverse range of marine habitats. Their ability to use alternative electron acceptors—nitrate (NO3−) or oxygen (O2)—makes them important mediators of benthic nitrogen cycling. Nevertheless, the metabolic scaling of the two alternative respiration pathways and the environmental determinants of foraminiferal denitrification rates are yet unknown. We measured denitrification and O2 respiration rates for 10 benthic foraminifer species sampled in the Peruvian oxygen minimum zone (OMZ). Denitrification and O2 respiration rates significantly scale sublinearly with the cell volume. The scaling is lower for O2 respiration than for denitrification, indicating that NO3− metabolism during denitrification is more efficient than O2 metabolism during aerobic respiration in foraminifera from the Peruvian OMZ. The negative correlation of the O2 respiration rate with the surface/volume ratio is steeper than for the denitrification rate. This is likely explained by the presence of an intracellular NO3− storage in denitrifying foraminifera. Furthermore, we observe an increasing mean cell volume of the Peruvian foraminifera, under higher NO3− availability. This suggests that the cell size of denitrifying foraminifera is not limited by O2 but rather by NO3− availability. Based on our findings, we develop a mathematical formulation of foraminiferal cell volume as a predictor of respiration and denitrification rates, which can further constrain foraminiferal biogeochemical cycling in biogeochemical models. Our findings show that NO3− is the preferred electron acceptor in foraminifera from the OMZ, where the foraminiferal contribution to denitrification is governed by the ratio between NO3− and O2.

Description: Oceanic oxygen decline due to anthropogenic climate change is a matter of growing concern. A quantitative oxygen proxy is highly desirable in order to identify and monitor recent dynamics as well as to reconstruct pre-Anthropocene changes in amplitude and extension of oxygen depletion. Geochemical proxies like foraminiferal I/Ca ratios seem to be promising redox proxies. Nevertheless, recent studies on microanalyses of benthic foraminiferal I/Ca ratios at the Peruvian oxygen minimum zone (OMZ) measured with secondary-ion mass spectrometry (SIMS) revealed a possible association of iodine with organic accumulations within the test. Here, we present a new study on the micro-distribution of nitrogen, sulfur, and iodine within the test walls of Uvigerina striata from the Peruvian OMZ measured with Nano-SIMS. A quantification of the foraminiferal I/Ca ratios from our NanoSIMS study is in good agreement with quantitative results from a previous SIMS study. Additionally, we compared uncleaned specimens with specimens that have been treated with an oxidative cleaning procedure. Both nitrogen and sulfur, which are used as tracer for organic matter, show a patchy distribution within the test walls of the uncleaned specimens and a statistically significant correlation with the iodine distribution. This patchy organic-rich phase has a different geochemical signature than the pristine calcitic parts of the test and another phase that shows a banding-like structure and that is characterized by a strong sulfur enrichment. All three elements, sulfur, nitrogen, and iodine, are strongly depleted in the cleaned specimens, even within the massive parts of the test walls that lack the connection with the test pores. These results indicate that the organic parts of the test walls are located inside a microporous framework within the foraminiferal calcite. This has to be considered in the interpretation of geochemical proxies on foraminiferal calcite, especially for microanalytical methods, since the chemical signature of these organic parts likely alters some element-to-calcium ratios within the foraminiferal test.

Description: Studies of carnivorous behaviour of benthic foraminifers are rare and mostly focused on laboratory experiments. Controlled experiments have shown that some agglutinated and intertidal species prey on meio- to macrofaunal metazoans. Here we present observations of the behaviour of specimens of the infaunal benthic foraminiferal species, Globobulimina auriculata and G. turgida, made within several hours of collection from ∼117 m depth in the Alsbäck Deep of the Gullmar Fjord, Sweden. We observed live nematodes within the tests of G. auriculata. Video observations recorded over a 17-hour period showed a G. auriculata specimen with a living nematode whose tail appeared to be entangled within the foraminifer's reticulopodial network. The nematode eventually coiled around the foraminifer's aperture and became much less active, though ingestion into the foraminifer's test was not documented. If these observations indicate feeding by G. auriculata, they differ from previous observations of predation by Ammonia tepida, which utilised external reticulopodial activity to extract the soft tissue of its prey. An alternative interpretation of the video observations, consistent with the observations of the live nematodes inside G. auriculata, was that the nematode was attempting to prey upon the foraminifer. The G. turgida specimens, in contrast, relatively quickly surrounded themselves in soft sediment spheres commonly seen in deposit-feeding foraminifers, and were never observed with nematodes within their tests. We speculate that these contrasting feeding strategies might reduce competition and facilitate the coexistence of these two globobuliminid species.