Records of past mid-depth ventilation : Cretaceous ocean anoxic event 2 vs . Recent oxygen minimum zones

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 under the Peruvian upwelling and < 5 μmol kg 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. Chondrites has not been reported in Peruvian sediments but centimetre-sized crab burrows appeared around 10 μmol kg, 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 kyr 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. Sediments deposited at > 10 μmol kg 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.


Introduction
In the present day ocean, most of the water column is well ventilated as a consequence of thermohaline circulation processes that lead to subduction of cold, oxygen rich and dense water masses in high northern and southern latitudes (e.g.Kuhlbrodt et al., 2007).Exceptions are restricted basins, in which the limited exchange with the oxygen rich water masses of the open ocean is not sufficient to counteract oxygen consumption by organic matter respiration such as in the Black Sea (Murray et al., 1989).In the open ocean, strongly oxygen depleted water bodies occur underlying highly productive surface waters such as in the major upwelling areas off the western continental margins of Africa and the Americas or below the monsoon-driven upwelling of the Arabian Sea (Helly and Levin, 2004).In the geological past, regional or global ventilation of the ocean underwent significant changes on different time scales due to a variety of reasons, including changes in atmospheric and ocean circulation, stratification, temperature or tectonic processes.It is, however, difficult to quantify the past spatial extent and intensity of oxygen minima because the oxygen concentration of the water column is not directly recorded in the sediments.As a consequence, derivative proxies have been applied to reconstruct past ocean oxygenation.
A characteristic feature of marine low-oxygen environments on various time scales are black, organic-rich, and laminated sediments (Kemp, 1996;Meyer and Kump, 2008).They are known to date back to the late Precambrian (Tucker, 1983).Widespread and contemporaneous occurrences of these deposits in Devonian, Permian, early Jurassic, early and late Cretaceous, and mid-Miocene successions depict periods of sluggish ocean circulation or extensive highly productive seas (Schlanger and Jenkyns, 1976;Buggisch, 1991;Flower and Kennett, 1993;Wignall and Twitchett, 1996;Trabucho-Alexandre et al., 2010).The question of whether these laminated sediments were formed due to enhanced primary production or due to restricted ventilation of near-bottom waters has fuelled a long-lasting debate (e.g.Calvert, 1987).Yet the discovery of laminated sediments in the Arabian Sea during the International Indian Ocean Expedition in 1965 revealed that this sedimentary facies is confined to oxygen minimum zones (OMZs) at mid-depth (Schott et al., 1970).Laminated sediments at the south-west African, Peruvian and Californian margin provided further evidence for their association with today's OMZs (van Andel, 1964;Reimers and Suess, 1983;Struck et al., 2002).In contrast, basin-wide stagnation events resulting in the deposition of organic-rich, at least partially laminated sediments were recorded during short time intervals with specific environmental settings from the Pliocene to early Holocene in the eastern Mediterranean (sapropels) and in the Sea of Japan (Stein and Stax, 1990;Rohling and Hilgen, 1991).They are, however, not considered potential analogues for the extensively occurring black, laminated shales of the Mesozoic including the Cretaceous ocean anoxic events (OAEs; Erbacher et al., 2001).
Stable carbon isotope data obtained from Devonian, Toarcian, Aptian and Cenomanian-Turonian successions revealed that the organic-rich beds recorded profound perturbations of the global biogeochemical cycles, of which the Cenomanian-Turonian boundary interval (OAE 2) was probably the most extensive event (e.g.Jenkyns et al., 1994;Hesselbo et al., 2000;Joachimski et al., 2002;Herrle et al., 2004).Detailed investigations of the geochemistry, microfossil assemblages, and sedimentary structures of both recent and fossil strata were performed to unravel the interplay of local, regional and global processes driving their formation, and to enforce a mutual understanding of late Quater-nary OMZs and Cretaceous OAEs (Thiede and Suess, 1983;Anbar and Rouxel, 2007;Dale et al., 2012;Owens et al., 2013).These studies were complemented by oceanographic, biological and biochemical studies in Recent upwelling systems and OMZs.However, this actualistic approach has been hampered by long periods of burial, diagenesis, and evolution of the biosphere since their deposition in Mesozoic times.
Geochemical redox proxies were extensively explored on Cretaceous black shales in order to constrain past ocean oxygenation, in particular trace metals (Brumsack, 2006;van Bentum et al., 2009;Dale et al., 2012), sulfur isotopes (Hetzel et al., 2009;Owens et al., 2013), and iron isotopes (Owens et al., 2012).Some of these proxies have also been measured on surface sediments and sediment cores from the Peruvian OMZ, in particular U/Mo ratios (Böning et al., 2004, Scholz et al., 2011, 2014a, b).However, only a very few data points are available for a regional U/Mo -bottomwater oxygen calibration in the Peruvian OMZ (Scholz et al., 2011).They strongly differ from corresponding data obtained from other OMZs (McManus et al., 2006).This hampers a quantitative reconstruction of past oxygenation with U/Mo ratios for the Peruvian OMZ as well as for black shales from the Cretaceous OAE 2.
Besides geochemical redox indicators, there are only a few other reliable parameters that have been sufficiently explored to investigate palaeo low-oxygen conditions in the Mesozoic and Cenozoic, which are trace fossils, laminations, and organic carbon accumulation rates.Their potential, constraints, and implications for an assessment of past water column oxygenation are addressed in this review.Particular emphasis is put on the comparison of Holocene OMZ sediments from the upwelling area off Peru with deposits of Cretaceous OAE 2 from the Moroccan shelf.

Material and methods
The Peruvian Margin study is based on stratigraphic and sedimentological data from 136 sediment cores within and below today's OMZ off the western South American continental margin.They are located between the Equator and 18 • S and were retrieved from water depths between 180 and 2200 m (Fig. 1).Data of 94 cores were taken from the literature and 42 new cores recovered during R/V METEOR cruises M77-1 and M77-2 in 2008 were assessed as part of this study (Table A1 in the Appendix).The cruises were performed in the framework of Collaborative Research Centre (SFB) 754 "Climate Biogeochemistry Interactions in the Tropical Ocean", through which supplementary data for the environmental interpretation of the sedimentary records are available.
In particular, oxygen concentrations along the Peruvian continental margin were measured during R/V METEOR cruises M77-1, M77-2 (Krahmann, 2012) and M77-3 (Kalvelage et al., 2013).We considered 159 CTD stations with a maximum water depth of 1750 m and a maximum dis- tance of 175 km to the shore (online Supplement M77-1-3_CTD_Data.xls).Other CTD casts further offshore were not included because they already showed significantly elevated oxygen concentrations compared to proximal locations at the same latitude.Kalvelage et al. (2013) observed an offset of ∼ 2 µmol kg −1 between the CTD attached optode oxygen sensors and the more sensitive STOX sensors, which are based on a Clark-type oxygen sensor, and corrected the optode data by 2 µmol kg −1 during the cruises M77-3 and M77-4.The oxygen data presented in our study were not corrected for a 2 µmol kg −1 offset since the STOX sensors were not deployed during M77-1 and M77-2.
We considered visual core descriptions, physical property data, in particular dry bulk densities, sand content and abundances of biogenic, terrigenous and diagenetic components, and organic carbon contents.The chronostratigraphy of the cores was established with radiocarbon datings on monospecific samples of planktonic or benthic foraminifera, or bulk sedimentary organic carbon.
The age models of the cores from M77-1 and M77-2 cruises are based on Mollier-Vogel et al. (2013).Otherwise, published, conventional radiocarbon ages and new 14 C accelerator mass spectrometer (AMS) datings were calibrated using the software "Calib 7.0" (Stuiver and Reimer, 1993) and by applying the marine calibration set "Ma-rine13" (Reimer et al., 2013).Reservoir age corrections ( R) were carried out using the Marine Reservoir Correction Database (http://calib.qub.ac.uk/marine/).Regionally weighted mean R values ranged from 89 to 338 years for the eastern Pacific off Peru.The uncertainties of the source data ranged from ±31 to ±82 years (2-sigma).For the pre-Holocene part of the records, the radiocarbon-based chronologies were supplemented with planktonic and ben-thic oxygen isotope curves correlated to stacked reference records (e.g.Liesicki and Raymo, 2005) or Antarctic ice cores (e.g.EPICA Community Members, 2006).Subrecent sedimentation rates were constrained by 210 Pb excess activity profiles (Reimers and Suess, 1983;Mosch et al., 2012).All ages are given in calendar years before 1950 AD (abbreviated as cal.ka).Organic carbon and bulk sediment accumulation rates (g cm −2 kyr −1 ) were calculated from linear sedimentation rates (cm 10 −3 years) and bulk dry densities (g cm −3 ) following van Andel et al. (1975).
The M77-1 and M77-2 cores included in this study were described immediately after opening aboard R/V METEOR (Pfannkuche et al., 2011).Two parallel series of volumedefined samples were taken in 5 or 10 cm intervals with cutoff syringes.One series of 10-cc samples was freeze-dried and physical properties were determined from wet sample volumes and the weight loss after drying applying standard protocols and a pore-water density of 1.026 g cm −3 (Boyce, 1976).The other series of 20-cc samples dedicated to isotopic measurements, microfossil, and sand-fraction examination was washed gently with tap water through a 63 µm sieve within a few hours after sampling.Washing of fresh, wet samples facilitates a better preservation of delicate calcareous microfossils, which otherwise may have been corroded or even dissolved by oxidation products of ferrosulfides and labile organic matter (Schnitker et al., 1980).The residues were dried at 50 • C and weighed.For stable oxygen and carbon isotope analyses, about 30 specimens of the planktonic foraminiferal species Globigerinoides ruber (white), Neogloboquadrina dutertrei or 3-6 specimens of the benthic species Uvigerina striata, U. peregrina or Globobulimina pacifica were picked from the size fractions 250-355 µm or > 63 µm, respectively.We used these species be-cause they were abundant in the cores studied and incorporate stable oxygen isotopes in equilibrium with the surrounding pore and supernatant bottom waters (e.g.McCorkle et al., 1990).Oxygen and carbon isotopes were measured with a Thermo Fisher Scientific 253 Mass Spectrometer coupled to a CARBO KIEL automated carbonate preparation device at GEOMAR, Kiel.The long-term analytical precision (1sigma) for δ 18 O and δ 13 C was better than 0.06 and 0.03 ‰ on the VPDB scale, respectively, based on more than 1000 measurements of an in-house carbonate standard during the respective measurement sessions.Replicate measurements of benthic foraminifera from the same sample showed an external reproducibility of ±0.1 ‰ for δ 18 O.For radiocarbon analyses, 33-179 specimens of Planulina limbata or 229-250 specimens of Neogloboquadrina dutertrei were picked from the size fraction > 63 µm or 5-20 mg of ground bulk sediment was prepared.AMS measurements were performed at the Leibniz Laboratory for Radiometric Dating and Stable Isotope Research, University of Kiel (CAU) and at Beta Analytic Inc. Dried samples used for physical property measurements were ground with an agate mortar.Aliquot subsamples of 3-20 mg were analysed for total carbon and organic carbon content with a Carlo-Erba Element Analyzer (NA1500) at GEOMAR, Kiel.The long-term precision was ±0.6 % of the measured values as revealed by repeated measurements of two internal carbon standards.
Since the pioneering work of Einsele and Wiedmann (1975), Cenomanian to Lower Campanian organicrich marlstones of the Tarfaya Basin in southern Morocco have been studied as a type locality of Cretaceous upwellingrelated sediments at the eastern margin of the central North Atlantic (Wiedmann et al., 1978;Leine et al., 1986;Kuhnt et al., 1997Kuhnt et al., , 2001Kuhnt et al., , 2005;;Kolonic et al., 2005;Aquit et al., 2013).Numerical climate and circulation models of the mid-Cretaceous Atlantic support a prevalence of cool and nutrient-rich intermediate deep water masses in this area along the north-west African margin (Poulsen et al., 2001;Topper et al., 2011).The late Cenomanian to early Turonian OAE 2 sediments discussed here were examined in outcrop sections during five field expeditions of the Kiel Micropaleontology Group in 1997Group in , 1998Group in , 2000Group in , 2003Group in and 2009. .In addition, core material from two commercial wells (S13 and S75), and a 350 m deep research well drilled in October-December 2009 (Tarfaya SN • 4) were considered in this study (Fig. 1).
Analytical methods applied to samples from outcrops and drill cores were detailed in Kuhnt et al. (2005) and Aquit et al. (2013).Core sections from the new exploration well Tarfaya SN • 4 were cut lengthwise and described.Line scan measurements and photographs were acquired with a Ja CVL 1073 CCD colour line scan camera with 3 sensors of 2048 pixels and a dichroic RGB beam splitter prism (RGB channels at 630, 535 and 450 nm) at the Institute of Geosciences, Kiel University.Colour measurement in L*a*b* units are from RGB digital images.Scanning was performed (reso-lution of 143 pixel per 70 micron) on the polished surface of oriented cores.Intensity of lamination vs. bioturbational homogenisation of the sediment was estimated using highresolution lightness ( L*) measurements for cores of SN • 4. We calculated a lamination index based on a moving window standard deviation of the lightness values, similar to the method previously applied on core S75 (Kuhnt et al., 2005).Organic carbon and carbonate contents of SN • 4 core samples were measured with a Carlo-Erba Element Analyzer (NA1500) at GEOMAR, and with a conventional carbonate bomb at the Institute of Geosciences, Kiel University.

Bioturbation
Organisms dwelling in sediments below the redox boundary commonly rely on oxygen supply from the above nearbottom waters (Savrda and Bottjer, 1991).They disappear if bottom-water oxygenation drops below a certain limit (Rhoads and Morse, 1971;Savrda et al., 1984).Observations from Recent OMZs suggested that deposit-feeding gastropods, in particular Astyris permodesta, may temporarily enter dead zones for grazing on fresh organic detritus or sulfur bacterial filaments (Levin et al., 1991;Mosch et al., 2012).These gastropods leave small biodeformational structures on the sea bed, which are not, however, usually preserved (Schäfer, 1956).Sediments from oxygen-depleted environments are therefore characterised by scarcity or absence of ichnofossils (Savrda and Bottjer, 1987).Only a few ichnogenera are recognisable, in particular the millimetre-sized Chondrites.Their diameter correlates with oxygenation although food availability or substrate properties also exert an influence (Bromley and Ekdale, 1984;Fu, 1991;Kröncke, 2006).In eastern Pacific hypoxic environments, a covariance of the highest average burrow size and oxygen content of near-bottom water was recognised for an oxygen range of 5-45 µmol kg −1 in the San Pedro Basin (Savrda et al., 1984).This relationship was based on 6-10 burrows identified per xray image.An assignment to particular ichnotaxa other than Arenicolites was not attempted, even though many ichnogenera have a well constrained range of dimensions (e.g.Wetzel, 2008).
The general inverse relationship of burrow diameter and oxygenation has been challenged by sea-floor observations with a photo sledge and shallow multicorer samples taken during R/V METEOR cruise M77-1 (Mosch et al., 2012).Surprisingly, it was not Chondrites, but centimetre-sized open crab burrows that were recognised as the first biogenic structures at bottom-water oxygen concentrations approaching 10 µmol kg −1 close to the lower OMZ boundary where endobenthic macrofauna were able to exist.Chondrites bur- rows have not been reported to date from any of the Peruvian OMZ sediment cores, even though the responsible organism, a nematode, most likely pursues chemotrophy at anaerobic conditions (Fu, 1991).
Older strata, such as Mesozoic sediments were usually subjected to a high degree of compaction altering the shape and size of burrows (e.g.Gaillard and Jautee, 2006;Gingras et al., 2010).A correct identification of ichnogenera may not then be possible any more.Burrows have been preserved at their genuine dimensions in carbonate-rich sediments (e.g.Savrda and Bottjer, 1986;Ekdale and Bromley, 1991).In particular, Chondrites-rich layers were reported from Cenomanian-Turonian limestones and marls deposited during OAE 2 in north-west Europe (Schönfeld et al., 1991;Hilbrecht and Dahmer, 1994;Rodríguez and Uchmann, 2011).As this ichnogenus is apparently missing from the Peruvian OMZ, bioturbation structures do not offer a detailed comparison between Pleistocene to Recent OMZs and Cretaceous OAEs.The only feature in common is the scarcity or absence of bioturbation in both laminated Cretaceous shales and Holocene to Pleistocene sediments deposited under dysoxic to anoxic conditions below the Peruvian upwelling.

Laminations
Laminated sediments have been studied in great detail to unravel the processes forming millimetre-scale interbedded sediments with the perspective that alternations between the varves reflect seasonal, annual or decadal environmental variability (von Stackelberg, 1972;Brodie and Kemp, 1994;Kemp, 1996).In the Arabian Sea, laminated sediments were found between 300 and 900 m water depth whereas the OMZ with oxygen concentrations of < 23 µmol kg −1 impinges the sea floor between 200 and 1200 m depth.Minimum values of 4.5 µmol kg −1 were reported (Schulz et al., 1996).No benthic macroinvertebrates were observed between 300 and 800 m where these low oxygen concentrations prevailed.The laminations form couplets of dark grey organic-rich summer varves and light grey winter varves of terrigenous detritus.Holocene average sedimentation rates were in the range of 0.9-1.5 mm yr −1 .Winnowing and reworking by slope currents or turbidites was common, which prevented the establishment of continuous long records of annual resolution (Schulz et al., 1996).Instead, cyclic alternations of laminated and bioturbated core sections suggested a spatial variability of the OMZ on longer time scales (von Rad et al., 1995).
In the California Borderland basins the laminae consist of dark lithogenic winter layers and light-coloured, nearly monospecific Thalassiothrix longissima diatom layers deposited during spring and early summer (Thunell et al., 1995).In the Soledad Basin off northern Mexico, whitish coccolith layers are intercalated as well (van Geen et al., 2003).Average sedimentation rates may exceed 1 mm yr −1 , and despite the pronounced seasonal or El Niño cyclicity of 3-6 years (Hagadorn, 1996), up to five biogenic sublaminae per year may be preserved (Pike and Kemp, 1997).The regional and intra-basinal distribution of laminations in the latest Holocene sediments was confined to bottom-water oxygen concentrations < 5 µmol kg −1 .In contrast, a decoupling of sediment banding and bottom-water oxygenation has been found at sites with a low primary production or where a less profound seasonality prevailed (van Geen et al., 2003).There, alterations of bioturbated glacial and stadial sediments and laminated Holocene and interstadial core sections suggested climatically driven variations in north-eastern Pacific OMZ intensity (Behl and Kennett, 1996;Cannariato and Kennett, 1999;Jaccard and Galbraith, 2012).
In the Peruvian OMZ, laminated sediments from the Salaverry and Pisco basins were described in great detail (Kemp, 1990;Wefer et al., 1990).The sediments showed 0.3-0.6 m thick intervals of laminated and sub-laminated sediments with intercalated homogenous bioturbated units.They are unconformably overlain by sand-rich layers with phosphorite pebbles representing periods of erosion due to strong near-bottom currents (Reimers and Suess, 1983;Garrison and Kastner, 1990).In banded core sections, the laminae form 0.3-0.7 mm thick couplets of clay-rich and siltrich layers probably reflecting depositional variability on seasonal timescales.Nearly monospecific Skeletonema or Chaetoceros diatom layers of 2-10 mm thickness are irregularly intercalated.These diatom ooze layers were often not preserved due to dissolution or grazing.Evidence for the latter is provided by microbioturbation within the laminated intervals and pellet-rich horizons of 5-30 mm thickness.These were created by epibenthic, vagile macrofauna during periods of elevated bottom-water oxygenation, which lasted for 8-16 years (Brodie and Kemp, 1994).A covariance of laminated core sections with certain climatic conditions was not identifiable whereas pebbly or sand-rich beds preferentially occurred during cold stages suggesting either stronger bottom currents or increased terrigenous sediment supply (Reimers and Suess, 1983;Rein et al., 2005;Mollier-Vogel et al., 2013).On decadal to subdecadal time scales, however, laminations were linked to changes in climate and ecosystem properties in the mid 19th century (Gutiérrez et al., 2006) (Imbrie et al., 1984;Wefer et al., 1990).Note that laminations were not recorded in sediments deposited between 6 and 8 cal.ka.
particular, periodical "regime shifts" in the Peruvian OMZ during the late Holocene were related to the variability of solar irradiance (Agnihotri et al., 2008).
Information on the presence of laminations is available for 74 of 136 sediment cores reported from the western South American margin between the Equator and 18 • S (Table A1 in the Appendix).From those, 36 showed laminated intervals whereas 38 cores were homogenised by bioturbation with the exception of sediment-transport related structures, sand or gravel beds.Laminated sediment sections are confined to a distinct area between 9 and 16 • S and were not retrieved from water depths below 600 m.With the exception of two cores from the continental shelf, the upper and lower distribution limits of laminated sediments match the outline of today's OMZ as depicted by the 7 µmol kg −1 isoline of bottomwater oxygen concentration.However, most laminated cores were retrieved from areas with bottom-water oxygen values of < 5 µmol kg −1 (Fig. 2).The distribution limits are not re-liably traceable further to the north and south due to sparse data coverage and rarely observed laminated sections.Sediment records may go as far back in time as marine oxygen isotope stage 11 and contain several unconformities representing extended times of non-deposition or erosion (Rein et al., 2005).
A reliable stratigraphic record is available for 9 sediment cores with laminated intervals.Laminations occurred at any time and water depth during the past 20 kyr with the exception of the 6-8 ka time interval (Fig. 3).This implies that there was no period of time during the late Pleistocene and Holocene during which the entire OMZ expanded and intensified, or contracted and weakened on a regional scale.Some of the shallowest locations showed weaker or no laminations during periods of inferred increased El Niño frequency marking seasonally decreased productivity and elevated oxygen levels in the bottom waters (Rein et al., 2005;Ehlert et al., 2013).Laminated deposits were rarely continuous and did not show a time-transgressive pattern as previously suggested (Reimers and Suess, 1983).Sections documenting periods of more than 2 kyr duration of laminated sediment deposition were recorded only between 11 and 13 • S and at water depths of 184-325 m, i.e. in the upper OMZ and underneath the most intense upwelling.

Organic carbon accumulation rates
Accumulation rates of sedimentary organic carbon have been widely considered as a proxy for palaeoproductivity reconstructions (Stein and Stax, 1991;Sarnthein et al., 1992;McKay et al., 2004).While usually less than 1 % of organic matter exported from the photic zone is deposited on the sea floor and preserved in the fossil record under oxic conditions, the burial may increase to up to 18 % in low-oxygen environments (Müller and Suess, 1979).The preservation of organic substances in OMZ sediments from the Arabian Sea was enhanced at oxygen concentrations of < 22 µmol kg −1 suggesting a covariance between organic carbon accumulation rates and bottom-water oxygenation (Koho et al., 2013).Recent organic carbon accumulation rates ranged from 0.01 to 0.4 g C cm −2 kyr −1 in the Arabian Sea.
In the Peruvian OMZ, mid-to late Holocene and subrecent organic carbon accumulation rates varied substantially between 0.06 and 6.8 g C cm −2 kyr −1 with most values between 1 and 3 g C cm −2 kyr −1 (Table A2 in the Appendix), i.e. one magnitude higher than in the Arabian Sea.Dilution by seasonal terrigenous sediment input from Pakistan probably accounts for the difference (von Rad et al., 1995).
The organic carbon data from the Peruvian cores revealed distinct distribution patterns.Laminated sediments showed scattered values at bottom-water oxygen < 5 µmol kg −1 whereas bioturbated sediments depicted a well constrained inverse relationship of organic carbon accumulation and bottom-water oxygenation (Fig. 4).3.2 Organic-rich sedimentation during Cretaceous OAE 2 of the Tarfaya Basin

Laminations
The laminated intervals in sediments from the Tarfaya Basin as recovered from the SN • 4 well were usually 2-4 m thick organic-rich marlstones with intercalated bioturbated limestones of 0.5-2 m thickness.The laminations showed a high scatter in lightness (Fig. 5), which is depicted by a lamination index based on a moving window standard deviation of highresolution lightness data (L*).Intense lamination is indicated by high standard deviations, while standard deviations in homogenous sediments are close to zero.The average thicknesses of individual laminae was extremely variable ranging from sub-millimetre (mainly light layers composed of planktonic foraminiferal tests) to several millimetres (mainly kerogen-rich dark layers).Simple estimates from average sedimentation rates of 4-8 cm per thousand years suggest an average time of 25-12.5 years to account for the deposition of a 1 mm lamina, which points to a control on lamination by depositional or winnowing processes, rather than a control by periodical climatic variations on the formation of laminae.Wavelet spectral analyses of the 70 µm resolution linescan data of core SN • 4 also do not exhibit clear periodicity patterns.The most prominent periodicities are in the range of 4, 15 and 30 mm, which would correspond to approximately 100, 400 and 800 years at a sedimentation rate of 4 cm kyr −1 and clearly do not reflect seasonal variability or ENSO-type sub-decadal oscillations (3-7 years) (Fig. 6).
Sediment re-working and re-distribution through small scale erosion and/or winnowing by bottom currents appeared commonly in the deposition of organic-rich sediments during OAE 2. Low angle truncations, indicating small scale erosion surfaces occurred frequently in the upper part of the OAE 2 black shales in the Tarfaya Basin (i.e. in black shales at the base of the Turonian within the Amma Fatma outcrop section, Fig. 7).
Recent depositional environments off north-west Africa were distinctly different from those during OAE 2. In the modern upwelling zone off north-west Africa, textural upwelling indicators, such as organic-rich, laminated sediments, were virtually absent in shallow shelf sediments directly underlying upwelling cells (Fütterer, 1983).They were winnowed out by strong bottom currents, sediment particles were transported across the shelf and finally redeposited in deeper parts of the shelf or on the continental slope.The main depositional centre of organic-rich material is located today at water depths between 1000 and 2000 m, where finegrained material is accumulating as mid-slope mud lenses (Sarnthein et al., 1982).
The organic-rich sediments in the Cretaceous Tarfaya Basin also exhibited a range of sedimentary features pointing to an important role of re-suspension and lateral advection in the depositional processes.However, sedimentological (El Albani et al., 1999) and micropalaeontological evidence (Wiedmann et al., 1978;Gebhardt et al., 2004, Kuhnt et al., 2009) indicated that the main depositional centre of organic-rich sediments during OAE 2 were in the middle to outer shelf part of the Tarfaya Basin in relatively shallow water depths between approx.100 and 300 m.Such a setting would be in general agreement with the situation on the Peruvian shelf and upper slope today, where similar highaccumulation areas were recognised at depths of less than 300 m (Wefer et al., 1990).

Organic carbon accumulation rates during OAE 2 in the Tarfaya Basin
Organic matter accumulation rates were calculated in three cores (S13, S75, SN • 4) for individual cycles based on an orbitally tuned age model (Meyers et al., 2012) for the time interval from the onset of OAE 2 (late Cenomanian, upper part of the R. cushmani Zone) to the lower Turonian (end of the OAE 2 carbon isotope excursion in the H. helvetica Zone).This period represents a time span of ∼ 800 kyr (Sagemann et al., 2006;Meyers et al., 2012).Cores were correlated using density and natural gamma ray logs.We used density/NGR minima/maxima for each individual cycle as tie points, and, whenever possible, correlatable features within individual cycles.The overall pattern and number of cycles in the studied interval revealed that most of the regular density variations mirrored obliquity cycles, i.e. a periodicity of 41 kyr.The local cyclostratigraphic age model is then tied to the GTS2012 timescale chronology using the new radiometric age of 93.9 Ma for the  ).Morlet wavelet with 6 parameters, the contour levels are chosen so that 75, 50, 25, and 5% of the wavelet power is above each level, respectively (Torrence and Compo, 1998).
as continuous organic carbon estimates from NGR logging and lightness (L*) measurements (Fig. 8).

Origin and composition of laminae
Light laminae in Peruvian upwelling sediments represent diatom blooms, either resulting from seasonal variations or deposition during strong La Niña events (Kemp, 1990), whereas in the Tarfaya Basin light layers are mainly composed of planktonic foraminiferal tests, phosphate or fecal pellets, indicating periods of higher oxygenation of the water column with enhanced grazing activity of vagile benthic organisms.These events occurred on decadal-centennial timescales as brief interruptions of otherwise continuously dysoxic to anoxic conditions.
The different marine primary producers in the Cenomanian-Turonian may have influenced the stoichiometry and isotope composition of marine organic matter.Whereas Holocene to Recent organic-rich sediments in the Peruvian upwelling contain high proportions of diatoms, Cretaceous organic-rich sediments are dominated by haptophyte algae preserved as shields of coccolithophorids and nannoconids, archaeans, and cyanobacteria as revealed by biomarkers (Kuypers et al., 1999;Dumitrescu and Brassell, 2005).It is conceivable that such organisms may have induced higher C / P and C / N ratios under high pCO 2 conditions, exceeding the Redfield ratio (Sterner and Elser, 2002;Riebesell, 2004;Sterner et al., 2008;Flögel et al., 2011;Hessen et al., 2013).As a result, nutrient limitation for marine productivity may have been less severe during Cretaceous OAEs, than it was reached under low pCO 2 conditions during the last deglaciation and the Holocene.

Persistence of laminated sediments -dynamics of the OMZ
The geological record of OAE 2 in the Tarfaya Basin showed a cyclic sedimentation of variegated, laminated marlstone beds with low gamma-ray density and high organic carbon accumulation rates, which were intercalated with uniformly pale, bioturbated limestones showing low organic carbon values.A regular periodicity of cyclic sedimentation in the obliquity domain indicated climatic forcing that was different from Late Cretaceous times with well-ventilated oceans, when short and long precession, and eccentricity had a stronger influence (Gale et al., 1999;Voigt and Schönfeld, 2010).It has been suggested that changes in mid-depth ocean circulation during OAE 2 promoted the influence of a highsouthern latitude climatic signal in the Cretaceous North Atlantic (Meyers et al., 2012).
In the north-eastern Pacific, we also see alterations of bioturbated sediments deposited during the last glacial and stadial climatic intervals with laminated intervals deposited during the Holocene and late Pleistocene interstadials (Behl and Kennett, 1996;Cannariato and Kennett, 1999).Even though these alterations reflect much shorter periodicities than during the mid Cretaceous, they were climatically driven by intensified upwelling due to stronger trade winds and enhanced nutrient supply through Subantarctic Mode Water, thus again linked to processes in the Southern Ocean (Jaccard and Galbraith, 2012, and references therein).
Off Peru, laminations have neither been strictly linked to climatic periodicities nor were they continuously preserved in the fossil record.Numerous discontinuities, their timetransgressive nature, and phosphoritic sand layers are evidence for the impact of strong near-bottom currents and breaking internal waves (Reimers and Suess, 1983).On the other hand, eddies and warm, oblique filaments can facilitate a short-term supply of oxygen to the Peruvian OMZ (e.g.Stramma et al., 2013), and large burrowing or grazing organisms may invade the dead zone from below (Mosch et al., 2012), thus destroying recently deposited laminae.Therefore it is conceivable that a preservation of continuous laminated sediments has been an exception rather than the rule in the Peruvian OMZ.This exception was more likely to occur in the permanently anoxic centre of the OMZ underneath the most intense upwelling cell.Nonetheless, it has to be emphasised that many of the north-eastern Pacific cores were retrieved from marginal basins where a quiet depositional regime prevailed.Furthermore, the impact of near-bottom currents and redeposition is also documented in OAE 2 deposits from Tarfaya outcrop sections.We speculate that if there were a possibility to examine older Peruvian OMZ sediments in an outcrop section, many similar features will emerge, helping us to better understand the fragmentation of the stratigraphic record described above.

Organic carbon accumulation and bottom-water oxygenation
A large range of chemical, biological and oceanographic factors controlling organic detritus flux to the sea bed, decomposition and remineralisation, preservation and finally accumulation as refractory substances constitute the complex nature of organic matter turnover.Furthermore, organic carbon preservation strongly depends on the local circumstances of deposition (Hedges and Keil, 1995;Arndt et al., 2013), thus limiting the comparability of settings between regions and oceanic basins.There is an ongoing debate as to whether the proportion of organic matter, which is buried and preserved in marine sediments, is dependent on the ambient bottom-water oxygenation or not (Dale et al., 2014).The only assured perception is that carbon burial does not co-vary with bottom-water oxygenation at high sedimentation rates near continental margins (Betts and Holland, 1991;Canfield, 1994).At low sedimentation rates, the oxygenated nearsurface layer of sediments deposited under oxygenated bottom water increases in thickness and facilitates enhanced aerobic decomposition, while sediments deposited under lowoxic conditions remain anaerobic and decomposition is effected by nitrate and sulfate reduction (Hartnett and Devol, 2003).As a consequence, organic carbon burial correlates with oxygen exposure time of particulate organic carbon at the sea floor in oxic to suboxic environments, and shows no covariance in dysoxic zones (Hartnett et al., 1998).

Comparison of organic carbon accumulation rates:
Glacial-Holocene Peruvian upwelling vs.

Cretaceous upwelling along the East Atlantic Margin
For a comparison of Cretaceous organic carbon accumulation rates with those of Recent OMZs, we considered Cretaceous sections with more than 90 % organic rich shales (Kuhnt et al., 1990).With reference to Recent OMZ sediments, we assumed a bottom water oxygenation < 5 µmol kg −1 at sites where fine laminations were preserved.The first estimates of TOC accumulation rates of Kuhnt et al. (1990) were based on a duration of 500 kyr for OAE 2 and on an average of a relatively small number of discrete organic carbon measurements over the entire interval.These rough estimates resulted in accumulation rates between 0.01 g C cm −2 kyr −1 for deep sea sites and 1.1 g C cm −2 kyr −1 for north-west African shelf basins with upwelling conditions, which showed the highest accumulation rates (Kuhnt et al., 1990).A re-evaluation of organic carbon accumulation rates in the Tarfaya Basin using an orbitally tuned age model and high-resolution measurements or continuous organic carbon estimates indicated variable carbon accumulation rates, which varied between 0.7 and 2.8 g C cm −2 kyr −1 and thus match the data range of the majority of laminated late Holocene sediments from the Peruvian Margin presently under bottom-water oxygen levels of < 5 µmol kg −1 (Fig. 4).
The palaeo water depths of the Tarfaya Basin during OAE 2 were slightly shallower than the centre of the Peruvian OMZ today.Based on molecular evidence, it was even suggested that the Cretaceous OMZ extended into the photic zone (Sinninghe Damsté and Köster, 1998).As such, decomposition and remineralisation of organic detritus while sinking to the sea floor was less likely (Martin et al., 1987).We therefore have to assume that the deposition rate of par-ticulate organic matter was very close to the export flux at 150 m water depth (Buesseler et al., 2007).An empirical relationship between the rain rate and Holocene burial rate of particulate organic carbon has been established by Flögel et al. (2011) for continental margin settings: where BUR POC is the burial rate of particulate organic carbon; RR POC is the rain rate of particulate organic carbon.
No significant difference between data from OMZs and wellventilated bottom waters is recognised (see Fig. 2 of Flögel et al., 2011).Applying Eq. ( 1) and considering a maximum organic carbon accumulation rate of 2.8 g C cm −2 kyr −1 , i.e. approximately 30 g C m −2 yr −1 to bring it up to a round figure, the maximum palaeo rain rate would be on the order of 126 g C m −2 yr −1 , i.e. about half the productivity that the present day Peruvian upwelling provides, ranging from 200 to > 400 g C m −2 yr −1 (Wefer et al., 1983).Even though this approximation includes many uncertainties, e.g.reliability of early sediment traps, variable burial efficiency (Dale et al., 2014), poorly constrained rates of Cretaceous primary production, it is reasonable to assume that part of the OAE 2 organic matter was lost during early diagenesis.It has to be emphasised that Holocene organic carbon accumulation rates in the centre of the Peruvian OMZ show a large scatter too, with maximum values of 6.8 g C cm −2 kyr −1 in core SO147-106KL, i.e. rounded up 70 g C m −2 yr −1 .If we likewise apply Eq. ( 1), we obtain a rain rate of 270 g C m −2 yr −1 .This value is in good agreement with today's productivity of the Peruvian upwelling, and it is derived from a core interval, where an unusually thick section of laminations was preserved.Nonetheless, the Recent carbon burial efficiency at 10 cm sediment depth close to the SO147-106KL coring site amounts to 62 % of the organic matter arriving at the sea floor (Dale et al., 2014).It is thus much higher than burial rate estimates for the late Holocene (Müller and Suess, 1979).The difference may either originate from a strong inter-annual variability, a subrecent rise in carbon accumulation since 1800 AD (Gutierrez et al., 2009), or from a further remineralisation of organic matter with time in the historical layer below 10 cm sediment depth and beyond.
For the laminated beds of OAE 2 in the Tarfaya Basin, a bottom water oxygenation of less than 5 µmol kg −1 is suggested with reference to the distribution of laminated sediments in Recent OMZs worldwide.The question arises of whether it is possible to assign a bottom-water oxygen estimate to the intercalated, pale bioturbated limestones from the Tarfaya sections.Indeed, benthic foraminifera from the non-laminated light-coloured interval at the base of cycle 0 in core S75 revealed a diverse benthic foraminiferal assemblage dominated by Bolivina species in high abundances.They indicate less dysoxic bottom waters (Kuhnt et al., 2005).The organic carbon accumulation rate was estimated at 1.1 g C cm −2 kyr −1 over this interval.If we apply the late Holocene relationship of organic carbon accumulation rates and bottom water oxygen for bioturbated sediments, an oxygenation of ca.38 µmol kg −1 is obtained.Such levels prevail at the Peruvian Margin today either below 800 m water depth, i.e. well below the OMZ, or above 90 m depth in the surface ocean mixed layer.Bolivina dominated faunas live in the centre of the Peruvian OMZ today, with high abundances between 150 and 520 m, and at oxygen concentrations of < 2 µmol kg −1 (Mallon, 2012).Between 800 and 900 m depth, the range to which the Cretaceous oxygen approximation points, Bolivina species were rare, accounting for less than 5 % of the living fauna.

Conclusions
The Pleistocene to Holocene and late Cenomanian to early Turonian stages are more than 94 million years apart in Earth's history.A direct comparison of their sedimentary record and environmental processes is hampered by burial diagenesis, evolution of marine biota, different continental and ocean configurations, and different climates, ocean circulation, and biogeochemical cycles.The late Cenomanian was marked by the onset of OAE 2. Sedimentological, faunistic and biogeochemical parameters suggested that large parts of the water column were devoid of dissolved oxygen, but the absolute levels are less well constrained.In an actualistic approach, we compared deposits of OAE 2 from the Moroccan shelf close to Tarfaya with deglacial and Holocene OMZ sediments from the upwelling area off Peru and found only a few parameters for a reliable investigation of palaeo low-oxygen conditions in both records, i.e. trace fossils, laminations and organic carbon accumulation rates.
The millimetre-sized trace fossil Chondrites was common in Cretaceous strata, in particular in the beds directly underlying OAE 2 black shales.It was also found in modern oxygen-depleted environments, where it is created by a nematode pursuing chemotrophy in anaerobic conditions.The burrow diameter increased with oxygen level from 5 to 45 µmol kg −1 in the San Pedro Basin, California.However, Chondrites has never been reported from Peruvian OMZ sediments.The oxygen-burrow size relationship is challenged by centimetre-sized crab burrows appearing at oxygen levels around 10 µmol kg −1 below the OMZ already.Crab burrows are also common in Cretaceous sediments.Their appearance in OAE 2 sediments may therefore indicate that a threshold of approximately 10 µmol kg −1 bottom-water oxygen has been exceeded.
Laminations are a more reliable indicator, but they display only one, very low oxygen level.In the Peruvian, northeastern Pacific and Pakistan OMZs, depositional laminae created by seasonal or multi-annual variations in sediment supply or composition were preserved at bottom-water oxygen concentrations of less than 5 µmol kg −1 .Coherent occurrences of laminated beds and biogeochemical indicators for oxygen drawdown in Tarfaya OAE 2 sediments supported the applicability of this feature for bottom-water oxygen estimates.The cyclic pattern of laminated and non-laminated intervals in Tarfaya sections and in sediment cores from the eastern Pacific suggested the impact of climatic variations with direct linkages to the high-latitude Southern Ocean as a source of nutrients and better ventilated intermediate waters.This regular cyclic pattern is blurred in Peruvian OMZ sediments by erosion, omission and redeposition due to nearbottom currents and breaking internal waves, making the preservation of laminated sediments an exception rather than the rule.Redeposition features were also observed in Tarfaya outcrop sections and reveal episodic, strong currents on the Cretaceous shelf and upper slope as an important process that was likely responsible for many observed unconformities in upper Cenomanian and lower Turonian formations.
Organic carbon accumulation rates of late Holocene sediments off Peru displayed a disjunct pattern.They showed a high scatter and a broad abundance maximum between 0.8 and 2.8, mode value at 1.3 µmol kg −1 , in laminated sediments under a Recent bottom-water oxygenation of < 5 µmol kg −1 .If we compare the carbon accumulation rates of the Tarfaya OAE 2 laminated sediments with late Holocene to Recent ones from the Peruvian OMZ, the Cretaceous rates between 0.7 and 2.8 g C cm −2 kyr −1 match the data range of the majority of late Holocene sediments very well.Taking into account the high burial efficiency of organic carbon deposited in OMZs, and calculating deposition fluxes from the photic zone, the maximum Cretaceous values would account for only half of the present-day export production under the Peruvian upwelling.Thermal maturation or the loss of volatile hydrocarbons from Tarfaya black shales may well account for this difference.Maximum Holocene carbon accumulation rates off Peru compare well to the present-day export production.This agreement is, however, valid only for sediments with a continuous, laminated record.All other cores exhibiting average carbon accumulation rates have most likely been subjected to instant winnowing and redeposition of organic detritus.
At higher oxygen levels, organic carbon accumulation rates showed an inverse exponential relationship with oxygen concentrations.This mirrors the successive bioirrigation and concomitant decomposition of organic matter through increasingly better ventilation below the Peruvian OMZ.Such a relationship has not been described before.Few available data from the Arabian Sea suggested a similar covariance conferring credibility to the pattern observed at the Peruvian Margin (Koho et al., 2013).The relationship has been used to assign a palaeo oxygen level to a well constrained, intermittently oxygenated interval at the base of cycle 0 (named the Plenus Cold Event) in the Tarfaya sections.The estimate of 38 µ mol kg −1 disagrees overall with the composition of the Cretaceous and Recent benthic foraminiferal assemblages prevailing at this oxygen level.
In summary, close similarities and distinct differences between the two periods of low oxygenation in the sedimen-

Figure 1 .
Figure 1.Location map of the sediment cores and wells studied.

Figure 2 .
Figure 2. Oxygen concentrations of a composite section along the Peruvian continental margin and locations of sediment cores.Triangles: cores with laminated intervals.Crosses: non-laminated cores.

Figure 4 .
Figure 4. Organic carbon accumulation rates versus bottom-water oxygen.Filled symbols indicate laminated sediment cores.

Figure 5 .Figure 6 .
Figure 5. Onset of OAE 2 in Tarfaya well SN • 4. The red box indicates transition from homogenous to laminated sediments.Note the increase in lightness variability.

Figure 7 .
Figure 7. Low angle truncations and small scale erosional surfaces indicating sediment reworking and re-distribution through small scale erosion and/or winnowing by bottom currents.(a) and (b) Coastal section near Shell-Onhym oil shale mine, lower Turonian; (c) and (d) Amma Fatma coastal section, base of Turonian.Scale: one dirham coin (24 mm diameter).

Figure 8 .
Figure 8. Organic carbon accumulation rates estimated from TOC measurements of 2 m continuously sampled and homogenised core sections, and density logging in Tarfaya well S13.Note the maximum between 94.4 and 93.75 Ma corresponding to the OAE 2 positive carbon isotope excursion.
. In Figure 3. Distribution of laminated intervals in sediment cores from the Peruvian OMZ.Triangles depict age control points.All cores were radiocarbon dated except IODP 112 680 and 686, which have been dated by graphic correlation of the benthic stable oxygen isotope curve with the SPECMAP stack C/T boundary (top cycle 3, FO Quadrum gartneri).Based on this age model, we calculated sedimentation rates for each individual cycle, dry bulk density from density logging and total organic carbon values from individual measurements as well www.biogeosciences.net/12/1169/2015/Biogeosciences, 12, 1169-1189, 2015

www.biogeosciences.net/12/1169/2015/ Biogeosciences, 12, 1169-1189, 2015 tary
record of the Cretaceous OAE 2 and the late Quaternary OMZs were recognised.More data are required to further constrain the organic carbon accumulation-oxygen relationship.This emerging palaeoproxy has to be complemented and corroborated by other, advanced bottom-water ventilation proxies, e.g.molybdenum isotopes or I / Ca ratios in foraminiferal shells in order to achieve more quantitative reconstructions of past oxygen levels and their controlling fac-