Skip to main content
    • Aa
    • Aa

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

  • Aaron Meilijson (a1), Sarit Ashckenazi-Polivoda (a2), Peter Illner (a3), Heiko Alsenz (a4), Robert P. Speijer (a5), Ahuva Almogi-Labin (a6), Shimon Feinstein (a1), Wilhelm Püttmann (a4) and Sigal Abramovich (a1)...

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.

Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

L. Alegret , and E. Thomas . 2009. Food supply to the seafloor in the Pacific Ocean after the Cretaceous/Paleogene boundary event. Marine Micropaleontology 73:105116.

L. Alegret , E. Molina , and E. Thomas . 2001. Benthic foraminifera at the Cretaceous-Tertiary boundary around the Gulf of Mexico. Geology 29:891894.

A. Almogi-Labin , A. Bein , and E. Sass . 1993. Late Cretaceous upwelling system along the Southern Tethys margin (Israel): Interrelationship between productivity, bottom water environments and organic matter preservation. Paleoceanography 8:671690.

A. Alsenz , P. Illner , S. Ashckenazi-Polivoda , A. Meilijson , S. Abramovich , S. Feinstein , A. Almogi-Labin , Z. Berner , and W. Püttmann . 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.

A. Amrani , M. D. Lewan , and Z. Aizenshtat . 2005. Stable sulfur isotope partitioning during simulated petroleum formation as determined by hydrous pyrolysis of Ghareb Limestone, Israel. Geochimica et Cosmochimica Acta 69:53175331.

S. Ashckenazi-Polivoda , Y. Edelman-Furstenberg , A. Almogi-Labin , and C. Benjamini . 2010. Characterization of lowest oxygen environments within ancient upwelling environments: Benthic foraminifera assemblages. Palaeogeography, Palaeoclimatology, Palaeoecology 289:134144.

S. Ashckenazi-Polivoda , S. Abramovich , A. Almogi-Labin , A. Schneider-Mor , S. Feinstein , W. Puttmann , and Z. Berner . 2011. Paleoenvironments of the latest Cretaceous oil shale sequence, Southern Tethys, Israel, as an integral part of the prevailing upwelling system. Palaeogeography, Palaeoclimatology, Palaeoecology 305:93108.

H. A. Austin , W. E. Austin , and D. M. Paterson . 2005. Extracellular cracking and content removal of the benthic diatom Pleurosigma angulatum (Quekett) by the benthic foraminifera Haynesina germanica (Ehrenberg). Marine Micropaleontology 57:6873.

A. Bein , A. Almogi-labin , and E. Sass . 1990. Sulfur sinks and organic-carbon relationships in Cretaceous organic-rich carbonates - implications for evaluation of oxygen-poor depositional-environments. American Journal of Science 290:882911.

F. Behar , V. Beaumont , H. L. De , and B. Penteado . 2001. Rock-Eval 6 technology: performances and developments. Oil & Gas Science and Technology – Revue d’IFP 56:111134.

R. A Berner . 1970. Sedimentary pyrite formation. American Journal of Science 268:123.

J. M Bernhard . 2003. Potential symbionts in bathyal foraminifera. Science 299:861861.

J. M. Bernhard , and S. S. Bowser . 1999. Benthic foraminifera of dysoxic sediments: chloroplast sequestering and functional morphology. Earth-Science Reviews 46:149165.

J.M. Bernhard , and C. E. Reimers . 1991. Benthic foraminiferal population fluctuations related to anoxia: Santa Barbara Basin. Biogeochemistry 15:127149.

J. M. Bernhard , and B. K. Sen Gupta . 1999. Foraminifera of oxygen-depleted environments. Pp. 201216in B.K. Sen Gupta, ed. Modern foraminifera. Kluwer Academic Publishers, Dordrecht.

J. M. Bernhard , P. T. Visscher , and S. S. Bowser . 2003. Submillimeter life positions of bacteria, protists, and metazoans in laminated sediments of the Santa Barbara Basin. Limnology and Oceanography 48:813828.

J. M. Bernhard , A. Habura , and S. S. Bowser . 2006. An endobiont-bearing allogromiid from the Santa Barbara Basin: Implications for the early diversification of foraminifera. Journal of Geophysical Research: Biogeosciences 111:G03002.

J. M. Bernhard , K. L. Casciotti , M. R. McIlvin , D. J. Beaudoin , P. T. Visscher , and V. P. Edgcomb . 2012a. Potential importance of physiologically diverse benthic foraminifera in sedimentary nitrate storage and respiration. Journal of Geophysical Research: Biogeosciences 117, doi: 10.1029/2012JG001949.

J. S Boggs . 2009. Petrology of sedimentary rocks (2nd ed.). Cambridge University Press, Cambridge.

B. H Corliss . 1991. Morphology and microhabitat preferences of benthic foraminifera from the northwest Atlantic Ocean. Marine Micropaleontology 17:195236.

B. H. Corliss , and C. Chen . 1988. Morphotype patterns of Norwegian Sea deep-sea benthic foraminifera and ecological implications. Geology 16:716719.

B. M. Didyk , B. R. T. Simoneit , S. C. Brassell , and G. Eglinton . 1978. Organic geochemical indicators of palaeoenvironmental conditions of sedimentation. Nature 272:216222.

E Flügel . 2010. Microfacies of carbonate rocks. Springer, Heidelberg.

O Friedrich . 2010. Benthic foraminifera and their role to decipher paleoenvironment during mid-Cretaceous Oceanic Anoxic Events - the “anoxic benthic foraminifera” paradox. Revue de Micropaleontologie 53:175192.

E. D. Galbraith , M. Kienast , A. L. Albuquerque , M. A. Altabet , F. Batista , D. Bianchi , S. E. Calvert , S. Contreras , X. Crosta , R. De Pol-Holz , N. Dubois , J. Etourneau , R. Francois , T. C. Hsu , T. Ivanochko , S. L. Jaccard , S. J. Kao , T. Kiefer , S. Kienast , M. F. Lehmann , P. Martinez , M. McCarthy , A. N. Meckler , A. Mix , J. Mobius , T. F. Pedersen , L. Pichevin , T. M. Quan , R. S. Robinson , E. Ryabenko , A. Schmittner , R. Schneider , A. Schneider-Mor , M. Shigemitsu , D. Sinclair , C. Somes , A. S. Studer , J. E. Tesdal , R. Thunell , and J. Y. T. Yang . 2013. The acceleration of oceanic denitrification during deglacial warming. Nature Geoscience 6:579584.

E. Geslin , N. Risgaard-Petersen , F. Lombard , E. Metzger , D. Langlet , and F. Jorissen . 2011. Oxygen respiration rates of benthic foraminifera as measured with oxygen microsensors. Journal of Experimental Marine Biology and Ecology 396:108114.

E. Geslin , C. Barras , D. Langlet , M. P. Nardelli , J. H. Kim , J. Bonnin , E. Metzger , and F. Jorissen . 2014. Survival, reproduction and calcification of three benthic foraminiferal species in response to experimentally induced hypoxia. Pp. 163193in H. Kitazato, and J. M. Bernhard, eds. Approaches to Study Living Foraminifera. Springer, Japan.

N. Glock , J. Schönfeld , A. Eisenhauer , C. Hensen , J. Mallon , and S. Sommer . 2013. The role of benthic foraminifera in the benthic nitrogen cycle of the Peruvian oxygen minimum zone. Biogeosciences 10:47674783.

A. J. Gooday , J. M. Bernhard , L. A. Levin , and S. B. Suhr . 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 47:2554.

P. J. Grantham , and L. L. Wakefield . 1988. Variations in the sterane carbon number distributions of marine source rock derived crude oils through geological time. Organic Geochemistry 12:6173.

R. A Henderson . 2004. A Mid-Cretaceous association of shell beds and organic rich shale: bivalve exploitation of nutrient-rich, anoxic sea-floor environment. Palaios 19:156169.

M. B. Higgins , R. S. Robinson , J. M. Husson , S. J. Carter , and A. Pearson . 2012. Dominant eukaryotic export production during ocean anoxic events reflects the importance of recycled NH4+. Proceedings of the National Academy of Sciences USA 109:22692274.

S. Høgslund , N. P. Revsbech , T. Cedhagen , L. P. Nielsen , and V. A. Gallardo . 2008. Denitrification, nitrate turnover, and aerobic respiration by benthic foraminiferans in the oxygen minimum zone off Chile. Journal of Experimental Marine Biology and Ecology 359:8591.

A. C Hutton . 1987. Petrographic classification of oil shales. International Journal of Coal Geology 8:203231.

A. Hutton , S. Bharati , and T. Robl . 1994. Chemical and petrographic classification of kerogen/macerals. Energy and Fuels 8:14781488.

F. J. Jorissen , C. Fontanier , and E. Thomas . 2007. Paleoceanographical proxies based on deep sea benthic foraminiferal assemblage characteristics. Pp. 263325in C. Hillaire Marcel, and A. de Vernal, eds. Proxies in Late Cenozoic paleoceanography, Volume 1. Developments in marine geology. Elsevier, New York.

M. E. L. Kohnen , J. S. Sinninghe Damsté , and J. W. De Leeuw . 1990. Alkylthiophenes as sensitive indicators of paleoenvironmental changes: A study of a Cretaceous oil shale from Jordan. Pp. 444485in W. L. Orr, and C. M. White, eds. Geochemistry of Sulfur in Fossil Fuels. American Chemical Society Symposium Series 429.

T. Kuhnt , O. Friedrich , G. Schmiedl , Y. Milker , A. Mackensen , and A. Luckge . 2013. Relationship between pore density in benthic foraminifera and bottom-water oxygen content. Deep-Sea Research Part I-Oceanographic Research Papers 76:8595.

D. Langlet , C. Baal , E. Geslin , E. Metzger , M. Zuschin , B. Riedel , N. Risgaard-Petersen , M. Stachowitsch , and F. J. Jorissen . 2014. Foraminiferal species responses to in situ, experimentally induced anoxia in the Adriatic Sea. Biogeosciences 11:17751797.

M. F. Lehmann , S. M. Bernasconi , A. Barbieri , and J. A. McKenzie . 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 66:35733584.

A. Meilijson , S. Ashckenazi-Polivoda , L. Ron-Yankovich , P. Illner , H. Alsenz , R. P. Speijer , A. Almogi-Labin , S. Feinstein , Z. Berner , W. Püttmann , and S. Abramovich . 2014. Chronostratigraphy of the Upper Cretaceous high productivity sequence of the Southern Tethys, Israel. Cretaceous Research 50:187213.

M. R. Mello , P. C. Gaglianone , S. C. Brassell , and J. R. Maxwell . 1988. Geochemical and biological marker assessment of depositional-environments using Brazilian offshore oils. Marine and Petroleum Geology 5:205223.

P. A Meyers . 1994. Preservation of elemental and isotopic source identification of sedimentary organic-matter. Chemical Geology 114:289302.

P. A Meyers 2014. Why are the δ13Corg values in Phanerozoic black shales more negative than in modern marine organic matter? Geochemistry Geophysics Geosystems 15:30853106.

L. Moodley , G. J. van der Zwaan , P. M. J. Herman , L. Kempers , and P. van Breugel . 1997. Differential response of benthic meiofauna to anoxia with special reference to foraminifera (Protista: Sarcodina). Marine Ecology Progress Series 158:151163.

M. P. Nardelli , C. Barras , E. Metzger , A. Mouret , H. L. Filipsson , F. Jorissen , and E. Geslin . 2014. Experimental evidence for foraminiferal calcification under anoxia. Biogeosciences 11:40294038.

K. E. Peters , and J. M. Moldowan . 1991. Effects of source, thermal maturity, and biodegradation on the distribution and isomerization of homohopanes in petroleum. Organic Geochemistry 17:4761.

L. Pillet , C. de Vargas , and J. Pawlowski . 2011. Molecular Identification of sequestered diatom chloroplasts and kleptoplastidy in foraminifera. Protist 162:394404.

E. Piña-Ochoa , S. Høgslund , E. Geslin , T. Cedhagen , N. P. Revsbech , L. P. Nielsen , M. Schweizer , F. Jorissen , S. Rysgaard , and N. Risgaard-Petersen . 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 107:11481153.

F. Pucci , E. Geslin , C. Barras , C. Morigi , A. Sabbatini , A. Negri , and F. J. Jorissen . 2009. Survival of benthic foraminifera under hypoxic conditions: Results of an experimental study using the Cell Tracker Green method. Marine Pollution Bulletin 59:336351.

T. M. Quan , B. van de Schootbrugge , M. P. Field , Y. Rosenthal , and P. G. Falkowski . 2008. Nitrogen isotope and trace metal analyses from the Mingolshe core (Germany): evidence for redox variations across the Triassic–Jurassic boundary. Global Biogeochemical Cycles 22:114.

T. M. Quan , D. James , and P. G. Falkowski . 2013. Co-variation of nitrogen isotopes and redox states through glacial–interglacial cycles in the Black Sea. Geochimica et Cosmochimica Acta 112:305320.

N. Risgaard-Petersen , A. M. Langezaal , S. Ingvardsen , M. C. Schmid , M. S. M. Jetten , H. J. M. Op den Camp , J. W. M. Derksen , E. Piña-Ochoa , S. P. Eriksson , L. P. Nielsen , N. P. Revsbech , T. Cedhagen , and G. J. van der Zwaan . 2006. Evidence for complete denitrification in a benthic foraminifer. Nature 443:9396.

R. S. Robinson , M. Kienast , A. L. Albuquerque , M. A. Altabet , S. Contreras , R. De Pol-Holz , N. Dubois , R. Francois , E. Galbraith , T.C. Hsu , T. Ivanochko , S. Jaccard , S. J. Kao , T. Kiefer , S. Kienast , M F. Lehmann , P. Martinez , M. McCarthy , J. Möbius , T. Pedersen , T. M. Quan , E. Ryabenko , A. Schmittner , R. Schneider , A. Schneider-Mor , M. Shigemitsu , D. Sinclair , C. Somes , A. Studer , R. Thunell , and J. Y. Yang . 2012. Review of nitrogen isotopic alteration in marine sediments. Paleoceanography 27:PA4203. doi: 10.1029/2012PA002321.

S.J Rowland . 1990. Production of acyclic isoprenoid hydrocarbons by laboratory maturation of methanogenic bacteria. Organic Geochemistry 15:916.

B. B. Sageman , and C. R. Bina . 1997. Diversity and species abundance patterns in Late Cenomanian Black Shale Biofacies, Western Interior. U.S. Palaios 12:449466.

B. K Sen Gupta . 1999. Modern foraminifera. Kluwer Academic Publishers, Dordrecht.

S Shoval . 2004. Clay sedimentation along the southeastern Neo-Tethys margin during the oceanic convergence stage. Applied Clay Science 24:287298.

D. M. Sigman , M. A. Altabet , D. C. McCorkle , R. Francois , and G. Fischer . 2000. The δ15N of nitrate in the Southern Ocean: Nitrogen cycling and circulation in the ocean interior. Journal of Geophysical Research-Oceans 105:1959919614.

J. S. Sinninghe Damsté , M. E. L. Kohnen , and J. W. de Leeuw . 1990. Thiophenic biomarkers for palaeoenvironmental assessment and molecular stratigraphy. Nature 345:609611.

J. S. Sinninghe Damsté , F. Kenig , M. P. Koopmans , J. Koster , S. Schouten , J. M. Hayes , and J. W. de Leeuw . 1995. Evidence for gammacerane as an indicator of water column stratification. Geochimica et Cosmochimica Acta 59:18951900.

D. Soudry , C. R. Glenn , Y. Nathan , I. Segal , and D. VonderHaar . 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 78:2757.

H. L. Ten Haven , J. W. de Leeuw , J. Rullkotter , and J. Sinninghe-Damsté . 1987. Restricted utility of the pristane/phytane ratio as a palaeoenvironmental indicator. Nature 330:641643.

B. P. Tissot , and D. H. Welte . 1984. Petroleum formation and occurrence, 2nd edition. Springer, Berlin and New York.

M. Tsuchiya , T. Toyofukua , K. Uematsub , V. Brüchertc , J. Collend , H. Yamamotoa , and H. Kitazatoa . 2015. Cytologic and genetic characteristics of endobiotic bacteria and kleptoplasts of Virgulinella fragilis (foraminifera). Journal of Eukaryotic Microbiology 62:454469.

J. G. V Widmark . 2000. Biogeography of terminal Cretaceous benthic foraminifera: deep-water circulation and trophic gradients in the deep South Atlantic. Cretaceous Research 21:367379.

J. G. V. Widmark , and B. Malmgren . 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 22:81113.

J. M Bernhard . 1993. Experimental and field evidence of Antarctic foraminiferal tolerance to anoxia and hydrogen sulfide. Marine Micropaleontology 20:203213.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0094-8373
  • EISSN: 1938-5331
  • URL: /core/journals/paleobiology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Full text views

Total number of HTML views: 8
Total number of PDF views: 23 *
Loading metrics...

Abstract views

Total abstract views: 159 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 28th March 2017. This data will be updated every 24 hours.