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Evidence for specific adaptations of fossil benthic foraminifera to anoxic–dysoxic environments

Published online by Cambridge University Press:  26 October 2015

Aaron Meilijson ,
Sarit Ashckenazi-Polivoda ,
Peter Illner ,
Heiko Alsenz ,
Robert P. Speijer ,
Ahuva Almogi-Labin ,
Shimon Feinstein ,
Wilhelm Püttmann  and
Sigal Abramovich
Aaron Meilijson
Affiliation:
Department of Geological and Environmental Sciences, Post Office Box 653, Ben-Gurion University of the Negev, Beer Sheva 84105, Israel. E-mail: shimon@bgu.ac.il, sigalabr@bgu.ac.il.
Sarit Ashckenazi-Polivoda
Affiliation:
Dead Sea and Arava Science Center, Neve Zohar, Dead Sea 86910, Israel. E-mail: sarit@adssc.org
Peter Illner
Affiliation:
Institute for Mineralogy and Geochemistry, Karlsruhe University 76131 Karlsruhe, Germany. E-mail: peter.illner@kit.edu
Heiko Alsenz
Affiliation:
Institute of Atmospheric and Environmental Sciences, Department of Environmental and Analytical Chemistry, Goethe-University, Altenhöferallee 1 60438 Frankfurt am Main, Germany. E-mail: alsenz@iau.uni-frankfurt.de, puettmann@iau.uni-frankfurt.de
Robert P. Speijer
Affiliation:
Department of Earth and Environmental Sciences, KU Leuven, Celestijnenlaan 200E, B- 3001 Leuven, Belgium. E-mail: robert.speijer@ees.kuleuven.be
Ahuva Almogi-Labin
Affiliation:
Geological Survey of Israel, Malkhe Israel 30, Jerusalem 95501, Israel. E-mail: almogi@gsi.gov.il
Shimon Feinstein
Affiliation:
Department of Geological and Environmental Sciences, Post Office Box 653, Ben-Gurion University of the Negev, Beer Sheva 84105, Israel. E-mail: shimon@bgu.ac.il, sigalabr@bgu.ac.il.
Wilhelm Püttmann
Affiliation:
Institute of Atmospheric and Environmental Sciences, Department of Environmental and Analytical Chemistry, Goethe-University, Altenhöferallee 1 60438 Frankfurt am Main, Germany. E-mail: alsenz@iau.uni-frankfurt.de, puettmann@iau.uni-frankfurt.de
Sigal Abramovich
Affiliation:
Department of Geological and Environmental Sciences, Post Office Box 653, Ben-Gurion University of the Negev, Beer Sheva 84105, Israel. E-mail: shimon@bgu.ac.il, sigalabr@bgu.ac.il.
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Abstract

It has generally been argued that the majority of fossil benthic foraminifera, the most common proxy for paleo bottom oceanic conditions, could not tolerate anoxia. Here we present evidence that fossil foraminifera were able to successfully colonize anoxic–dysoxic bottom waters, by using adaptations similar to those found in living species. Our study is based on a multi proxy micropaleontological and geochemical investigation of the Upper Cretaceous sediments from the Levant upwelling regime. A shift from buliminid to diverse trochospiral dominated assemblages was recorded in an interval with a distinct anoxic geochemical signature coinciding with a regional change in lithology. This change was triggered by an alteration in the type of primary producers from diatoms to calcareous nannoplankton, possibly causing modifications in benthic foraminiferal morphological and physiological adaptations to life in the absence of oxygen.

Our data show that massive blooms of triserial (buliminid) benthic foraminifera with distinct apertural and test morphologies during the Campanian were enabled by their ability to sequester diatom chloroplasts and associate with bacteria, in a similar manner as their modern analogs. Diverse trochospiral forms existed during the Maastrichtian by using nitrate instead of oxygen for their respiratory pathways in a denitrifying environment. Species belonging to the Stilostomellidae and Nodosariidae families might have been affected by the change in food type arriving to the seafloor after the phytoplankton turnover at the Campanian/Maastrichtian boundary, in a similar manner as their mid Pleistocene descendants prior to their extinction. This study promotes the need for a re-evaluation of the current models used for interpreting paleoceanographic data and demonstrates that the identification of adaptations and mechanisms involved in promoting sustained life under anoxic to dysoxic conditions should become a standard in faunal paleoceanographic studies.

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Paleobiology , Volume 42 , Issue 1 , February 2016 , pp. 77 - 97
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Copyright © 2015 The Paleontological Society. All rights reserved 

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References

Literature Cited

Alegret, L., and Thomas, E.. 2009. Food supply to the seafloor in the Pacific Ocean after the Cretaceous/Paleogene boundary event. Marine Micropaleontology 73:105–116.CrossRefGoogle Scholar
Alegret, L., Molina, E., and Thomas, E.. 2001. Benthic foraminifera at the Cretaceous-Tertiary boundary around the Gulf of Mexico. Geology 29:891–894.2.0.CO;2>CrossRefGoogle Scholar
Almogi-Labin, A., Bein, A., and Sass, E.. 1993. Late Cretaceous upwelling system along the Southern Tethys margin (Israel): Interrelationship between productivity, bottom water environments and organic matter preservation. Paleoceanography 8:671–690.CrossRefGoogle Scholar
Almogi-Labin, A., Ashckenazi-Polivoda, S., Edelman-Furstenberg, Y., and Benjamini, C.. 2012. Anoxia-Dysoxia at the sediment-water interface of the Southern Tethys in the Late Cretaceous: Mishash Formation, southern Israel. Pp. 553–572in A. V. Altenbach, J. M. Bernhard, and J. Seckbach, eds. Anoxia, evidence for eukaryote survival and paleontological strategies. Springer, Dordrecht.CrossRefGoogle Scholar
Alsenz, A., Illner, P., Ashckenazi-Polivoda, S., Meilijson, A., Abramovich, S., Feinstein, S., Almogi-Labin, A., Berner, Z., and Püttmann, W.. 2015. Geochemical evidence for the link between sulfate reduction, sulfide oxidation and phosphate accumulation in a late Cretaceous upwelling system. Geochemical Transactions 16, doi: 10.1186/s12932-015-0017-1.CrossRefGoogle Scholar
Altenbach, A. V., Bernhard, J. M., and Seckbach, J., eds. 2012. Anoxia, evidence for eukaryote survival and paleontological strategies. Springer, Dordrecht.CrossRefGoogle Scholar
Amrani, A., Lewan, M. D., and Aizenshtat, Z.. 2005. Stable sulfur isotope partitioning during simulated petroleum formation as determined by hydrous pyrolysis of Ghareb Limestone, Israel. Geochimica et Cosmochimica Acta 69:5317–5331.CrossRefGoogle Scholar
Ashckenazi-Polivoda, S., Edelman-Furstenberg, Y., Almogi-Labin, A., and Benjamini, C.. 2010. Characterization of lowest oxygen environments within ancient upwelling environments: Benthic foraminifera assemblages. Palaeogeography, Palaeoclimatology, Palaeoecology 289:134–144.CrossRefGoogle Scholar
Ashckenazi-Polivoda, S., Abramovich, S., Almogi-Labin, A., Schneider-Mor, A., Feinstein, S., Puttmann, W., and Berner, Z.. 2011. Paleoenvironments of the latest Cretaceous oil shale sequence, Southern Tethys, Israel, as an integral part of the prevailing upwelling system. Palaeogeography, Palaeoclimatology, Palaeoecology 305:93–108.CrossRefGoogle Scholar
Austin, H. A., Austin, W. E., and Paterson, D. M.. 2005. Extracellular cracking and content removal of the benthic diatom Pleurosigma angulatum (Quekett) by the benthic foraminifera Haynesina germanica (Ehrenberg). Marine Micropaleontology 57:68–73.CrossRefGoogle Scholar
Bein, A., Almogi-labin, A., and Sass, E.. 1990. Sulfur sinks and organic-carbon relationships in Cretaceous organic-rich carbonates - implications for evaluation of oxygen-poor depositional-environments. American Journal of Science 290:882–911.CrossRefGoogle Scholar
Behar, F., Beaumont, V., De, H. L., and Penteado, B.. 2001. Rock-Eval 6 technology: performances and developments. Oil & Gas Science and Technology – Revue d’IFP 56:111–134.CrossRefGoogle Scholar
Berner, R. A. 1970. Sedimentary pyrite formation. American Journal of Science 268:1–23.CrossRefGoogle Scholar
Bernhard, J. M. 1993. Experimental and field evidence of Antarctic foraminiferal tolerance to anoxia and hydrogen sulfide. Marine Micropaleontology 20:203–213.CrossRefGoogle Scholar
Bernhard, J. M. 2003. Potential symbionts in bathyal foraminifera. Science 299:861–861.CrossRefGoogle ScholarPubMed
Bernhard, J. M., and Bowser, S. S.. 1999. Benthic foraminifera of dysoxic sediments: chloroplast sequestering and functional morphology. Earth-Science Reviews 46:149–165.CrossRefGoogle Scholar
Bernhard, J.M., and Reimers, C. E.. 1991. Benthic foraminiferal population fluctuations related to anoxia: Santa Barbara Basin. Biogeochemistry 15:127–149.CrossRefGoogle Scholar
Bernhard, J. M., and Sen Gupta, B. K.. 1999. Foraminifera of oxygen-depleted environments. Pp. 201–216in B.K. Sen Gupta, ed. Modern foraminifera. Kluwer Academic Publishers, Dordrecht.CrossRefGoogle Scholar
Bernhard, J. M., Visscher, P. T., and Bowser, S. S.. 2003. Submillimeter life positions of bacteria, protists, and metazoans in laminated sediments of the Santa Barbara Basin. Limnology and Oceanography 48:813–828.CrossRefGoogle Scholar
Bernhard, J. M., Habura, A., and Bowser, S. S.. 2006. An endobiont-bearing allogromiid from the Santa Barbara Basin: Implications for the early diversification of foraminifera. Journal of Geophysical Research: Biogeosciences 111:G03002.CrossRefGoogle Scholar
Bernhard, J. M., Goldstein, S. T., and Bowser, S. S.. 2010. An ectobiont-bearing foraminiferan, Bolivina pacifica, that inhabits microxic pore waters: cell-biological and paleoceanographic insights. Environmental Microbiology 12:2107–2119.CrossRefGoogle ScholarPubMed
Bernhard, J. M., Casciotti, K. L., McIlvin, M. R., Beaudoin, D. J., Visscher, P. T., and Edgcomb, V. P.. 2012a. Potential importance of physiologically diverse benthic foraminifera in sedimentary nitrate storage and respiration. Journal of Geophysical Research: Biogeosciences 117, doi: 10.1029/2012JG001949.CrossRefGoogle Scholar
Bernhard, J. M., Edgcomb, V. P., Casciotti, K. L., McIlvin, M. R., and Beaudoin, D. J.. 2012b. Denitrification likely catalyzed by endobionts in an allogromiid foraminifer. Multidisciplinary Journal of Microbial Ecology 6:951–960.Google Scholar
Berrocoso, A. J., MacLeod, K. G., Calvert, S. E., and Elorza, J.. 2008. Bottom water anoxia, inoceramid colonization, and benthopelagic coupling during black shale deposition on Demerara Rise (Late Cretaceous western tropical North Atlantic). Paleoceanography 23:PA3212. doi: 10.1029/2007PA001545.Google Scholar
Boggs, J. S. 2009. Petrology of sedimentary rocks (2nd ed.). Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Corliss, B. H. 1991. Morphology and microhabitat preferences of benthic foraminifera from the northwest Atlantic Ocean. Marine Micropaleontology 17:195–236.CrossRefGoogle Scholar
Corliss, B. H., and Chen, C.. 1988. Morphotype patterns of Norwegian Sea deep-sea benthic foraminifera and ecological implications. Geology 16:716–719.2.3.CO;2>CrossRefGoogle Scholar
Costello, A. B., and Osborne, J. W.. 2007. Best practices in exploratory factor analysis: four recommendations for getting the most from your analysis. Practical Assessment Research & Evaluation 10:1–8.Google Scholar
Didyk, B. M., Simoneit, B. R. T., Brassell, S. C., and Eglinton, G.. 1978. Organic geochemical indicators of palaeoenvironmental conditions of sedimentation. Nature 272:216–222.CrossRefGoogle Scholar
Dyni, J. R. 2005. Geology and resources of some world oil-shale deposits. U.S. Geological Survey Scientific Investigations Report 2005–5294.CrossRefGoogle Scholar
Emeis, K. C., and Kvenvolden, K. A.. 1986. Shipboard organic geochemistry on JOIDES RESOLUTION. Ocean Drilling Program Technical Report No. 7, Ocean Drilling Program, College Station, Texas.CrossRefGoogle Scholar
Eglinton, T. I., and Repeta, D. J.. 2011. Organic matter in the contemporary ocean. Pp. 145–180in H. D. Holland, and K. K., Turekian, eds. Geochemistry of earth surface systems: from the treatise on geochemistry. Elsevier/Academic Press, Amsterdam, Boston.Google Scholar
Fleischer, L., and Gafsou, R.. 2003). Top Judea Group- digital structural map of Israel (1:200.000). Geophysical institute of Israel Report 753/312/03.Google Scholar
Flügel, E. 2010. Microfacies of carbonate rocks. Springer, Heidelberg.CrossRefGoogle Scholar
Friedrich, O. 2010. Benthic foraminifera and their role to decipher paleoenvironment during mid-Cretaceous Oceanic Anoxic Events - the “anoxic benthic foraminifera” paradox. Revue de Micropaleontologie 53:175–192.CrossRefGoogle Scholar
Galbraith, E. D., Kienast, M., Albuquerque, A. L., Altabet, M. A., Batista, F., Bianchi, D., Calvert, S. E., Contreras, S., Crosta, X., De Pol-Holz, R., Dubois, N., Etourneau, J., Francois, R., Hsu, T. C., Ivanochko, T., Jaccard, S. L., Kao, S. J., Kiefer, T., Kienast, S., Lehmann, M. F., Martinez, P., McCarthy, M., Meckler, A. N., Mix, A., Mobius, J., Pedersen, T. F., Pichevin, L., Quan, T. M., Robinson, R. S., Ryabenko, E., Schmittner, A., Schneider, R., Schneider-Mor, A., Shigemitsu, M., Sinclair, D., Somes, C., Studer, A. S., Tesdal, J. E., Thunell, R., and Yang, J. Y. T.. 2013. The acceleration of oceanic denitrification during deglacial warming. Nature Geoscience 6:579–584.CrossRefGoogle Scholar
Geslin, E., Risgaard-Petersen, N., Lombard, F., Metzger, E., Langlet, D., and Jorissen, F.. 2011. Oxygen respiration rates of benthic foraminifera as measured with oxygen microsensors. Journal of Experimental Marine Biology and Ecology 396:108–114.CrossRefGoogle Scholar
Geslin, E., Barras, C., Langlet, D., Nardelli, M. P., Kim, J. H., Bonnin, J., Metzger, E., and Jorissen, F.. 2014. Survival, reproduction and calcification of three benthic foraminiferal species in response to experimentally induced hypoxia. Pp. 163–193in H. Kitazato, and J. M. Bernhard, eds. Approaches to Study Living Foraminifera. Springer, Japan.CrossRefGoogle Scholar
Glock, N., Schönfeld, J., Eisenhauer, A., Hensen, C., Mallon, J., and Sommer, S.. 2013. The role of benthic foraminifera in the benthic nitrogen cycle of the Peruvian oxygen minimum zone. Biogeosciences 10:4767–4783.CrossRefGoogle Scholar
Gooday, A. J., Bernhard, J. M., Levin, L. A., and Suhr, S. B.. 2000. Foraminifera in the Arabian Sea oxygen minimum zone and other oxygen-deficient settings: taxonomic composition, diversity, and relation to metazoan faunas. Deep-Sea Research Part II-Topical Studies in Oceanography 47:25–54.CrossRefGoogle Scholar
Grantham, P. J., and Wakefield, L. L.. 1988. Variations in the sterane carbon number distributions of marine source rock derived crude oils through geological time. Organic Geochemistry 12:61–73.CrossRefGoogle Scholar
Hammer, Ø., and Harper, D. A. T.. 2006. Paleontological data analysis. Blackwell, Oxford.Google Scholar
Hammer, Ø., Harper, D. A. T., and Ryan, P. D.. 2001. PAST: palaeontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1), 9 pp.Google Scholar
Hart, M. B. 1996. Biotic recovery from mass extinction events. Geological Society of London Special Publication 102, London.Google Scholar
Hayward, B. W., Kawagata, S., Sabaa, A., Grenfell, H., Van Kerckhoven, L., Johnson, K., and Thomas, E.. 2012. The last global extinction (Mid-Pleistocene) of deep-sea benthic foraminifera (Chrysalogoniidae, Ellipsoidinidae, Glandulonodosariidae, Plectofrondiculariidae, Pleurostomellidae, Stilostomellidae), their Late Cretaceous-Cenozoic history and taxonomy. Cushman Foundation for Foraminiferal Research Special Publication 43.Google Scholar
Henderson, R. A. 2004. A Mid-Cretaceous association of shell beds and organic rich shale: bivalve exploitation of nutrient-rich, anoxic sea-floor environment. Palaios 19:156–169.2.0.CO;2>CrossRefGoogle Scholar
Higgins, M. B., Robinson, R. S., Husson, J. M., Carter, S. J., and Pearson, A.. 2012. Dominant eukaryotic export production during ocean anoxic events reflects the importance of recycled NH4+. Proceedings of the National Academy of Sciences USA 109:2269–2274.CrossRefGoogle ScholarPubMed
Høgslund, S., Revsbech, N. P., Cedhagen, T., Nielsen, L. P., and Gallardo, V. A.. 2008. Denitrification, nitrate turnover, and aerobic respiration by benthic foraminiferans in the oxygen minimum zone off Chile. Journal of Experimental Marine Biology and Ecology 359:85–91.CrossRefGoogle Scholar
Hutton, A. C. 1987. Petrographic classification of oil shales. International Journal of Coal Geology 8:203–231.CrossRefGoogle Scholar
Hutton, A. C 1991. Classification, organic petrography and geochemistry of oil shales. Proceedings 1990 Eastern Oil Shale Symposium. University of Kentucky Institute for Mining and Minerals Research, Lexington.Google Scholar
Hutton, A., Bharati, S., and Robl, T.. 1994. Chemical and petrographic classification of kerogen/macerals. Energy and Fuels 8:1478–1488.CrossRefGoogle Scholar
Jackson, M. L. 2005. Soil chemical analysis, advanced course, Revision of 2nd edition. Parallel, Wisconsin.Google Scholar
Jorissen, F. J., Fontanier, C., and Thomas, E.. 2007. Paleoceanographical proxies based on deep sea benthic foraminiferal assemblage characteristics. Pp. 263–325in C. Hillaire Marcel, and A. de Vernal, eds. Proxies in Late Cenozoic paleoceanography, Volume 1. Developments in marine geology. Elsevier, New York.CrossRefGoogle Scholar
Kohnen, M. E. L., Sinninghe Damsté, J. S., and De Leeuw, J. W.. 1990. Alkylthiophenes as sensitive indicators of paleoenvironmental changes: A study of a Cretaceous oil shale from Jordan. Pp. 444–485in W. L. Orr, and C. M. White, eds. Geochemistry of Sulfur in Fossil Fuels. American Chemical Society Symposium Series 429.CrossRefGoogle Scholar
Koho, K., and Piña-Ochoa, E.. 2012. Benthic foraminifera: inhabitants of low-oxygen environments. Pp. 249–285in A. V. Altenbach, J. M. Bernhard, and J. Seckbach, eds. Anoxia, evidence for eukaryote survival and paleontological strategies. Springer, Dordrecht.CrossRefGoogle Scholar
Kuhnt, T., Friedrich, O., Schmiedl, G., Milker, Y., Mackensen, A., and Luckge, A.. 2013. Relationship between pore density in benthic foraminifera and bottom-water oxygen content. Deep-Sea Research Part I-Oceanographic Research Papers 76:85–95.CrossRefGoogle Scholar
Lafargue, E., Espitalié, J., Marquis, F., and Pilot, D.. 1998. Rock-Eval 6 applications in hydrocarbon exploration, production and soil contamination studies. Oil & Gas Science and Technology 53:421–437.Google Scholar
Langlet, D., Baal, C., Geslin, E., Metzger, E., Zuschin, M., Riedel, B., Risgaard-Petersen, N., Stachowitsch, M., and Jorissen, F. J.. 2014. Foraminiferal species responses to in situ, experimentally induced anoxia in the Adriatic Sea. Biogeosciences 11:1775–1797.CrossRefGoogle Scholar
Lehmann, M. F., Bernasconi, S. M., Barbieri, A., and McKenzie, J. A.. 2002. Preservation of organic matter and alteration of its carbon and nitrogen isotope composition during simulated and in situ early sedimentary diagenesis. Geochimica et Cosmochimica Acta 66:3573–3584.CrossRefGoogle Scholar
Leiter, C., and Altenbach, A. V.. 2010. Benthic foraminifera from the diatomaceous mud belt off Namibia: characteristic species for severe anoxia. Palaeontologia Electronica 13(2), 11A–19A. 19 p.Google Scholar
Maxwell, R. E., Cox, R. G., Ackman, R. G., and Hooper, S. N.. 1972. The diagenesis and maturation of phytol. The stereochemistry of 2,6,10,14-tetramethylpentadeeane from an ancient sediment. Pp. 177–291 in H. R. von Gaertner, and H. Wehner, eds. Advances in organic geochemistry. Proceedings of the 5th International Meeting on Organic Geochemistry, Hannover.Google Scholar
McKirdy, D. M., A. K. Alridge, and P. J. Ypma. 1983. Geochemical comparison of some crude oils from pre-Ordovician carbonate rocks. Pp. 99–107 in M. Bjoroy, et al., eds. Advances in organic geochemistry. Wiley & sons, New York.Google Scholar
Meilijson, A., Ashckenazi-Polivoda, S., Ron-Yankovich, L., Illner, P., Alsenz, H., Speijer, R. P., Almogi-Labin, A., Feinstein, S., Berner, Z., Püttmann, W., and Abramovich, S.. 2014. Chronostratigraphy of the Upper Cretaceous high productivity sequence of the Southern Tethys, Israel. Cretaceous Research 50:187–213.CrossRefGoogle Scholar
Mello, M. R., Gaglianone, P. C., Brassell, S. C., and Maxwell, J. R.. 1988. Geochemical and biological marker assessment of depositional-environments using Brazilian offshore oils. Marine and Petroleum Geology 5:205–223.CrossRefGoogle Scholar
Meyers, P. A. 1994. Preservation of elemental and isotopic source identification of sedimentary organic-matter. Chemical Geology 114:289–302.CrossRefGoogle Scholar
Meyers, P. A 2014. Why are the δ13Corg values in Phanerozoic black shales more negative than in modern marine organic matter? Geochemistry Geophysics Geosystems 15:3085–3106.CrossRefGoogle Scholar
Moldowan, J. M., Sundararaman, P., and Schell, M.. 1986. Sensitivity of biomarker properties to depositional environment and/or source input in the Lower Toarcian of S. W. Germany. Organic Geochemistry 10:915–926.CrossRefGoogle Scholar
Moodley, L., van der Zwaan, G. J., Herman, P. M. J., Kempers, L., and van Breugel, P.. 1997. Differential response of benthic meiofauna to anoxia with special reference to foraminifera (Protista: Sarcodina). Marine Ecology Progress Series 158:151–163.CrossRefGoogle Scholar
Nardelli, M. P., Barras, C., Metzger, E., Mouret, A., Filipsson, H. L., Jorissen, F., and Geslin, E.. 2014. Experimental evidence for foraminiferal calcification under anoxia. Biogeosciences 11:4029–4038.CrossRefGoogle Scholar
Peters, K. E., and Moldowan, J. M.. 1991. Effects of source, thermal maturity, and biodegradation on the distribution and isomerization of homohopanes in petroleum. Organic Geochemistry 17:47–61.CrossRefGoogle Scholar
Peters, K. E., Walters, C. C., and Moldowan, J. M.. 2005. The biomarker guide. Cambridge University Press, Cambridge.Google Scholar
Pillet, L., de Vargas, C., and Pawlowski, J.. 2011. Molecular Identification of sequestered diatom chloroplasts and kleptoplastidy in foraminifera. Protist 162:394–404.CrossRefGoogle ScholarPubMed
Piña-Ochoa, E., Høgslund, S., Geslin, E., Cedhagen, T., Revsbech, N. P., Nielsen, L. P., Schweizer, M., Jorissen, F., Rysgaard, S., and Risgaard-Petersen, N.. 2010. Widespread occurrence of nitrate storage and denitrification among foraminifera and Gromiida. Proceedings of the National Academy of Sciences of the United States of America 107:1148–1153.CrossRefGoogle ScholarPubMed
Powell, T. G., and McKirdy, D. M.. 1973. Relationship between ratio of pristane to phytane, crude oil composition and geological environment in Australia. Nature 243:37–39.Google Scholar
Pucci, F., Geslin, E., Barras, C., Morigi, C., Sabbatini, A., Negri, A., and Jorissen, F. J.. 2009. Survival of benthic foraminifera under hypoxic conditions: Results of an experimental study using the Cell Tracker Green method. Marine Pollution Bulletin 59:336–351.CrossRefGoogle Scholar
Quan, T. M., van de Schootbrugge, B., Field, M. P., Rosenthal, Y., and Falkowski, P. G.. 2008. Nitrogen isotope and trace metal analyses from the Mingolshe core (Germany): evidence for redox variations across the Triassic–Jurassic boundary. Global Biogeochemical Cycles 22:1–14.CrossRefGoogle Scholar
Quan, T. M., James, D., and Falkowski, P. G.. 2013. Co-variation of nitrogen isotopes and redox states through glacial–interglacial cycles in the Black Sea. Geochimica et Cosmochimica Acta 112:305–320.CrossRefGoogle Scholar
Risgaard-Petersen, N., Langezaal, A. M., Ingvardsen, S., Schmid, M. C., Jetten, M. S. M., Op den Camp, H. J. M., Derksen, J. W. M., Piña-Ochoa, E., Eriksson, S. P., Nielsen, L. P., Revsbech, N. P., Cedhagen, T., and van der Zwaan, G. J.. 2006. Evidence for complete denitrification in a benthic foraminifer. Nature 443:93–96.CrossRefGoogle Scholar
Robinson, R. S., Kienast, M., Albuquerque, A. L., Altabet, M. A., Contreras, S., De Pol-Holz, R., Dubois, N., Francois, R., Galbraith, E., Hsu, T.C., Ivanochko, T., Jaccard, S., Kao, S. J., Kiefer, T., Kienast, S., Lehmann, M F., Martinez, P., McCarthy, M., Möbius, J., Pedersen, T., Quan, T. M., Ryabenko, E., Schmittner, A., Schneider, R., Schneider-Mor, A., Shigemitsu, M., Sinclair, D., Somes, C., Studer, A., Thunell, R., and Yang, J. Y.. 2012. Review of nitrogen isotopic alteration in marine sediments. Paleoceanography 27:PA4203. doi: 10.1029/2012PA002321.CrossRefGoogle Scholar
Rowland, S.J. 1990. Production of acyclic isoprenoid hydrocarbons by laboratory maturation of methanogenic bacteria. Organic Geochemistry 15:9–16.CrossRefGoogle Scholar
Schneider-Mor, A., Alsenz, H., Ashckenazi-Polivoda, S., Illner, P., Abramovich, S., Feinstein, S., Almogi-Labin, A., Berner, Z., and Puttmann, W.. 2012. Paleoceanographic reconstruction of the late Cretaceous oil shale of the Negev, Israel: Integration of geochemical, and stable isotope records of the organic matter. Palaeogeography, Palaeoclimatology, Palaeoecology 319:46–57.CrossRefGoogle Scholar
Sageman, B. B., and Bina, C. R.. 1997. Diversity and species abundance patterns in Late Cenomanian Black Shale Biofacies, Western Interior. U.S. Palaios 12:449–466.CrossRefGoogle Scholar
Sen Gupta, B. K. 1999. Modern foraminifera. Kluwer Academic Publishers, Dordrecht.Google Scholar
Shoval, S. 2004. Clay sedimentation along the southeastern Neo-Tethys margin during the oceanic convergence stage. Applied Clay Science 24:287–298.CrossRefGoogle Scholar
Sigman, D. M., Altabet, M. A., McCorkle, D. C., Francois, R., and Fischer, G.. 2000. The δ15N of nitrate in the Southern Ocean: Nitrogen cycling and circulation in the ocean interior. Journal of Geophysical Research-Oceans 105:19599–19614.CrossRefGoogle Scholar
Sinninghe Damsté, J. S., Kohnen, M. E. L., and de Leeuw, J. W.. 1990. Thiophenic biomarkers for palaeoenvironmental assessment and molecular stratigraphy. Nature 345:609–611.CrossRefGoogle Scholar
Sinninghe Damsté, J. S., Kenig, F., Koopmans, M. P., Koster, J., Schouten, S., Hayes, J. M., and de Leeuw, J. W.. 1995. Evidence for gammacerane as an indicator of water column stratification. Geochimica et Cosmochimica Acta 59:1895–1900.CrossRefGoogle ScholarPubMed
Soudry, D., Glenn, C. R., Nathan, Y., Segal, I., and VonderHaar, D.. 2006. Evolution of Tethyan phosphogenesis along the northern edges of the Arabian-African shield during the Cretaceous-Eocene as deduced from temporal variations of Ca and Nd isotopes and rates of P accumulation. Earth-Science Reviews 78:27–57.CrossRefGoogle Scholar
Suhr, D. 2009. Principal component analysis vs. exploratory factor analysis. Proceedings of the Thirtieth Annual SAS® Users Group International Conference. Cary, North Carolina.Google Scholar
Ten Haven, H. L., de Leeuw, J. W., Rullkotter, J., and Sinninghe-Damsté, J.. 1987. Restricted utility of the pristane/phytane ratio as a palaeoenvironmental indicator. Nature 330:641–643.CrossRefGoogle Scholar
Thomas, E. 1990. Late Cretaceous through Neogene deep-sea benthic foraminifers (Maud Rise, Weddell Sea, Antarctica). Pp. 571–594 in P. F. Barker, et al., eds. Proceedings of the Ocean Drilling Program, scientific results Volume 113. Ocean Drilling Program, College Station, Texas.CrossRefGoogle Scholar
Tissot, B. P., and Welte, D. H.. 1984. Petroleum formation and occurrence, 2nd edition. Springer, Berlin and New York.CrossRefGoogle Scholar
Tsuchiya, M., Toyofukua, T., Uematsub, K., Brüchertc, V., Collend, J., Yamamotoa, H., and Kitazatoa, H.. 2015. Cytologic and genetic characteristics of endobiotic bacteria and kleptoplasts of Virgulinella fragilis (foraminifera). Journal of Eukaryotic Microbiology 62:454–469.CrossRefGoogle ScholarPubMed
Widmark, J. G. V. 2000. Biogeography of terminal Cretaceous benthic foraminifera: deep-water circulation and trophic gradients in the deep South Atlantic. Cretaceous Research 21:367–379.CrossRefGoogle Scholar
Widmark, J. G. V., and Malmgren, B.. 1992. Benthic foraminiferal changes across the Cretaceous Tertiary boundary in the deep-sea - DSDP site-525, site-527, and site-465. Journal of Foraminiferal Research 22:81–113.CrossRefGoogle Scholar