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Photosymbiosis in planktonic foraminifera across the Paleocene–Eocene thermal maximum

Published online by Cambridge University Press:  05 March 2021

Jack O. Shaw*
Affiliation:
Department of Earth and Planetary Sciences, 21 Sachem Street, Yale University, New Haven, Connecticut06511, U.S.A. E-mail: [email protected], [email protected]
Simon D'haenens
Affiliation:
Department of Earth and Planetary Sciences, 21 Sachem Street, Yale University, New Haven, Connecticut06511, U.S.A. E-mail: [email protected], [email protected]
Ellen Thomas
Affiliation:
Department of Earth and Planetary Sciences, 21 Sachem Street, Yale University, New Haven, Connecticut06511, U.S.A. E-mail: [email protected], [email protected]
Richard D. Norris
Affiliation:
Scripps Institution of Oceanography, University of California, San Diego, California92093, U.S.A. E-mail: [email protected]
Johnnie A. Lyman
Affiliation:
High Tech High North County, 1420 West San Marcos Boulevard, San Marcos, California92078, U.S.A. E-mail: [email protected]
André Bornemann
Affiliation:
Bundesanstalt für Geowissenschaften und Rohstoffe, Stilleweg 2, 30655Hannover, Germany. E-mail: [email protected]
Pincelli M. Hull
Affiliation:
Department of Earth and Planetary Sciences, 21 Sachem Street, Yale University, New Haven, Connecticut06511, U.S.A. E-mail: [email protected], [email protected]
*
*Corresponding author.

Abstract

Under stress, corals and foraminifera may eject or consume their algal symbionts (“bleach”), which can increase mortality. How bleaching relates to species viability over warming events is of great interest given current global warming. We use size-specific isotope analyses and abundance counts to examine photosymbiosis and population dynamics of planktonic foraminifera across the Paleocene–Eocene thermal maximum (PETM, ~56 Ma), the most severe Cenozoic global warming event. We find variable responses of photosymbiotic associations across localities and species. In the NE Atlantic (DSDP Site 401) PETM, photosymbiotic clades (acarininids and morozovellids) exhibit collapsed size-δ13C gradients indicative of reduced photosymbiosis, as also observed in Central Pacific (ODP Site 1209) and Southern Ocean (ODP Site 690) acarininids. In contrast, we find no significant loss of size-δ13C gradients on the New Jersey shelf (Millville) or in Central Pacific morozovellids. Unlike modern bleaching-induced mass mortality, populations of photosymbiont-bearing planktonic foraminifera increased in relative abundance during the PETM. Multigenerational adaptive responses, including flexibility in photosymbiont associations and excursion taxon evolution, may have allowed some photosymbiotic foraminifera to thrive. We conclude that deconvolving the effects of biology on isotope composition on a site-by-site basis is vital for environmental reconstructions.

Type
Articles
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of The Paleontological Society

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Footnotes

Present address: Research Coordination Office and Data Science Institute, Hasselt University, Agoralaan Building D, 3590 Diepenbeek, Belgium. E-mail: [email protected].

Also at: Department of Earth and Environmental Sciences, Wesleyan University, Middletown, Connecticut 06459, U.S.A. E-mail: [email protected]

References

Literature Cited

Aze, T., Pearson, P. N., Dickson, A. J., Badger, M. P. S., Bown, P. R., Pancost, R. D., Gibbs, S. J., Huber, B. T., Leng, M. J., Coe, A. L., Cohen, A. S., and Foster, G. L.. 2014. Extreme warming of tropical waters during the Paleocene–Eocene thermal maximum. Geology 42:739742.CrossRefGoogle Scholar
Bains, S., Corfield, R. M., and Norris, R. D.. 1999. Mechanisms of climate warming at the end of the Paleocene. Science 285:724727.CrossRefGoogle Scholar
Bard, E. 2001. Paleoceanographic implications of the difference in deepsea sediment mixing between large and fine particles. Paleoceanography 16:235239.CrossRefGoogle Scholar
Birch, H., Coxall, H. K., Pearson, P. N., Kroon, D., and O'Regan, M.. 2013. Planktonic foraminifera stable isotopes and water column structure: disentangling ecological signals. Marine Micropaleontology 101:127145.CrossRefGoogle Scholar
Bird, C., Darling, K. F., Russell, A. D., Davis, C. V., Fehrenbacher, J., Free, A., Wyman, M., and Ngwenya, B. T.. 2017. Cyanobacterial endobionts within a major marine planktonic calcifier (Globigerina bulloides, Foraminifera) revealed by 16S rRNA metabarcoding. Biogeosciences 14:901920.CrossRefGoogle Scholar
Bornemann, A., Norris, R. D., Lyman, J. A., D'haenens, S., Groeneveld, J., Röhl, U., Farley, K. A., and Speijer, R. P.. 2014. Persistent environmental change after the Paleocene–Eocene Thermal Maximum in the eastern North Atlantic. Earth and Planetary Science Letters 394:7081.CrossRefGoogle Scholar
Bornemann, A., D'haenens, S., Norris, R. D., and Speijer, R. P.. 2016. The demise of the early Eocene greenhouse—decoupled deep and surface water cooling in the eastern North Atlantic. Global and Planetary Change 145:130140.CrossRefGoogle Scholar
Bralower, T. J. 2002. Evidence of surface water oligotrophy during the Paleocene–Eocene thermal maximum: nannofossil assemblage data from Ocean Drilling Program Site 690, Maud Rise, Weddell Sea. Paleoceanography 17:13-113-12.CrossRefGoogle Scholar
Cramer, B. S., Wright, J. D., Kent, D. V., and Aubry, M. P.. 2003. Orbital climate forcing of δ13C excursions in the late Paleocene–early Eocene (chrons C24n-C25n). Paleoceanography 18.CrossRefGoogle Scholar
D'Haenens, S., Bornemann, A., Roose, K., Claeys, P., and Speijer, R. P.. 2012. Stable isotope paleoecology (δ13C and δ18O) of early Eocene Zeauvigerina aegyptiaca from the north Atlantic (DSDP site 401). Austrian Journal of Earth Sciences 105:179188.Google Scholar
D'Hondt, S., Zachos, J. C., Schultz, G., and Summer, N.. 1994. Stable isotopic signals and photosymbiosis in late Paleocene planktic foraminifera. 20:391–406.Google Scholar
Donner, S. D., Skirving, W. J., Little, C. M., Oppenheimer, M., and Hoegh-Gulberg, O.. 2005. Global assessment of coral bleaching and required rates of adaptation under climate change. Global Change Biology 11:22512265.CrossRefGoogle Scholar
Dunkley Jones, T., Lunt, D. J., Schmidt, D. N., Ridgwell, A., Sluijs, A., Valdes, P. J., and Maslin, M.. 2013. Climate model and proxy data constraints on ocean warming across the Paleocene–Eocene Thermal Maximum. Earth-Science Reviews 125:123145.CrossRefGoogle Scholar
Dutton, A., Lohmann, K. C., and Leckie, R. M.. 2005. Insights from the Paleogene tropical Pacific: foraminiferal stable isotope and elemental results from Site 1209, Shatsky Rise. Paleoceanography 20:116.CrossRefGoogle Scholar
Edgar, K. M., Bohaty, S. M., Gibbs, S. J., Sexton, P. F., Norris, R. D., and Wilson, P. A.. 2013. Symbiont “bleaching” in planktic foraminifera during the Middle Eocene Climatic Optimum. Geology 41:1518.CrossRefGoogle Scholar
Edgar, K. M., Hull, P. M., and Ezard, T. H. G.. 2017. Evolutionary history biases inferences of ecology and environment from δ13C but not δ18O values. Nature Communications 8:19.CrossRefGoogle Scholar
Ezard, T. H. G., Edgar, K. M., and Hull, P. M.. 2015. Environmental and biological controls on size-specific δ13C and δ18O in recent planktonic foraminifera. Paleoceanography 30:151173.CrossRefGoogle Scholar
Frieling, J., Reichart, G.-J., Middelburg, J. J., Röhl, U., Westerhold, T., Bohaty, S. M., and Sluijs, A.. 2017. Tropical Atlantic climate and ecosystem regime shifts during the Paleocene–Eocene Thermal Maximum. Climate of the Past 14:3955.CrossRefGoogle Scholar
Gaskell, D. E., and Hull, P. M.. 2019. Symbiont arrangement and metabolism can explain high δ13C in eocene planktonic foraminifera. Geology 47:11561160.CrossRefGoogle Scholar
Gibbs, S. J., Bown, P. R., Murphy, B. H., Sluijs, A., Edgar, K. M., Pälike, H., Bolton, C. T., and Zachos, J. C.. 2012. Scaled biotic disruption during early Eocene global warming events. Biogeosciences 9:46794688.CrossRefGoogle Scholar
Gutjahr, M., Ridgwell, A., Sexton, P. F., Anagnostou, E., Pearson, P. N., Pälike, H., Norris, R. D., Thomas, E., and Foster, G. L.. 2017. Very large release of mostly volcanic carbon during the Palaeocene–Eocene Thermal Maximum. Nature 548:573577.CrossRefGoogle ScholarPubMed
Hallock, P., Williams, D. E., Fisher, E. M., and Toler, S. K.. 2006. Bleaching in foraminifera with algal symbionts: implications for reef monitoring and risk assessment. Anuario do Instituto de Geociencias 29:108128.CrossRefGoogle Scholar
Hay, W. W., DeConto, R. M., Wold, C. N., Wilson, K. M., Voigt, S., Schulz, M., Wold, A. R., Dullo, W.-C., Ronov, A. B., Balukhovsky, A. N., and Söding, E.. 1999. Alternative global Cretaceous paleogeography. In E. Barrera and C. C. Johnson, eds. Evolution of the Cretaceous ocean-climate system. Geological Society of America Special Paper 332: 1–47.Google Scholar
Henehan, M. J., Foster, G. L., Bostock, H. C., Greenop, R., Marshall, B. J., and Wilson, P. A.. 2016. A new boron isotope-pH calibration for Orbulina universa, with implications for understanding and accounting for “vital effects.” Earth and Planetary Science Letters 454:282292.CrossRefGoogle Scholar
Henehan, M. J., Edgar, K. M., Foster, G. L., Penman, D. E., Hull, P. M., Greenop, R., Anagnostou, E., and Pearson, P. N.. 2020. Revisiting the Middle Eocene Climatic Optimum “carbon cycle conundrum” with new estimates of atmospheric pCO2 from boron isotopes. Paleoceanography and Paleoclimatology 35:e2019PA003713.CrossRefGoogle Scholar
Hughes, T. P., Kerry, J. T., Baird, A. H., Connolly, S. R., Dietzel, A., Eakin, C. M., Heron, S. F., Hoey, A. S., Hoogenboom, M. O., Liu, G., McWilliam, M. J., Pears, R. J., Pratchett, M. S., Skirving, W. J., Stella, J. S., and Torda, G.. 2018. Global warming transforms coral reef assemblages. Nature 556:492496.CrossRefGoogle ScholarPubMed
Hull, P. M., Franks, P. J. S., and Norris, R. D.. 2011. Mechanisms and models of iridium anomaly shape across the Cretaceous–Paleogene boundary. Earth and Planetary Science Letters 301:98106.CrossRefGoogle Scholar
Hupp, B. N., and Kelly, D. C.. 2020. Delays, discrepancies, and distortions: Size-dependent sediment mixing and the deep-sea record of the Paleocene–Eocene Thermal Maximum from ODP Site 690 (Weddell Sea). Paleoceanography and Paleoclimatology 35:e2020PA004018.CrossRefGoogle Scholar
Hupp, B. N., Kelly, D. C., Zachos, J. C., and Bralower, T. J.. 2019. Effects of size-dependent sediment mixing on deep-sea records of the Paleocene–Eocene Thermal Maximum. Geology 47:749752.CrossRefGoogle Scholar
Katz, M. E., Katz, D. R., Wright, J. D., Miller, K. G., Pak, D. K., Shackleton, N. J., and Thomas, E.. 2003. Early Cenozoic benthic foraminiferal isotopes: species reliability and interspecies correction factors. Paleoceanography 18. doi: 10.1029/2002PA000798CrossRefGoogle Scholar
Kelly, D. C. 2002. Response of Antarctic (ODP Site 690) planktonic foraminifera to the Paleocene–Eocene thermal maximum: faunal evidence for ocean/climate change. Paleoceanography 17:23-123-13.CrossRefGoogle Scholar
Kelly, D. C., Bralower, T. J., Zachos, J. C., Silva, I. P., and Thomas, E.. 1996. Rapid diversification of planktonic foraminifera in the tropical Pacific (ODP Site 865) during the late Paleocene thermal maximum. Geology 24:423426.2.3.CO;2>CrossRefGoogle Scholar
Kelly, D. C., Zachos, J. C., Bralower, T. J., and Schellenberg, S. A.. 2005. Enhanced terrestrial weathering/runoff and surface ocean carbonate production during the recovery stages of the Paleocene–Eocene thermal maximum. Paleoceanography 20. doi: 10.1029/2005PA001163.CrossRefGoogle Scholar
Kelly, D. C., Nielsen, T. M. J., and Schellenberg, S. A.. 2012. Carbonate saturation dynamics during the Paleocene–Eocene thermal maximum: bathyal constraints from ODP sites 689 and 690 in the Weddell Sea (South Atlantic). Marine Geology 303:7586.CrossRefGoogle Scholar
Kennett, J. P., and Stott, L. D.. 1991. Abrupt deep-sea warming, palaeoceanographic changes and benthic extinctions at the end of the Palaeocene. Nature 353:225229.CrossRefGoogle Scholar
Kirtland Turner, S. 2018. Constraints on the onset duration of the Paleocene–Eocene Thermal Maximum. Philosophical Transactions of the Royal Society of London A 376:20170082.Google Scholar
Kirtland Turner, S., Hull, P. M., Kump, L. R., and Ridgwell, A.. 2017. A probabilistic assessment of the rapidity of PETM onset. Nature Communications 8:110.CrossRefGoogle ScholarPubMed
Kopp, R. E., Schumann, D., Raub, T. D., Powars, D. S., Godfrey, L. V., Swanson-Hysell, N. L., Maloof, A. C., and Vali, H.. 2009. An Appalachian Amazon? Magnetofossil evidence for the development of a tropical river-like system in the mid-Atlantic United States during the Paleocene–Eocene thermal maximum. Paleoceanography 24. doi: 10.1029/2009PA001783.CrossRefGoogle Scholar
Lombard, F., da Rocha, R. E., Bijma, J., and Gattuso, J. P.. 2009. Effect of carbonate ion concentration and irradiance on calcification in foraminifera. Biogeosciences Discussions 6:85898608.Google Scholar
Luciani, V., D'Onofrio, R., Dickens, G. R., and Wade, B. S.. 2017. Did photosymbiont bleaching lead to the demise of planktic foraminifer Morozovella at the Early Eocene Climatic Optimum? Paleoceanography 32:11151136.CrossRefGoogle Scholar
Norris, R. D. 1998. Recognition and macroevolutionary significance of photosymbiosis in molluscs, corals, and foraminifera. Paleontological Society Papers 4:68100.CrossRefGoogle Scholar
Nunes, F., and Norris, R. D.. 2006. Abrupt reversal in ocean overturning during the Palaeocene/Eocene warm period. Nature 439:6063.CrossRefGoogle ScholarPubMed
Pandolfi, J. M., and Kiessling, W.. 2014. Gaining insights from past reefs to inform understanding of coral reef response to global climate change. Current Opinion in Environmental Sustainability 7:5258.CrossRefGoogle Scholar
Pardo, A., Keller, G., Molina, E., and Canudo, J. I.. 1997. Planktic foraminiferal turnover across the Paleocene–Eocene transition at DSDP Site 401, Bay of Biscay, North Atlantic. Marine Micropaleontology 29:129158.CrossRefGoogle Scholar
Pearson, P. N., Ditchfield, P. W., Singano, J., Harcourt-Brown, K. G., Nicholas, C. J., Olsson, R. K., Shackleton, N. J., and Hall, M. A.. 2001. Warm tropical sea surface temperatures in the Late Cretaceous and Eocene epochs. Nature 413:481487.CrossRefGoogle ScholarPubMed
Pearson, P. N., Olsson, R. K., Huber, B. T., Hemleben, C., and Berggren, W. A.. 2006. Atlas of Eocene planktonic foraminifera. Cushman Foundation for Foraminiferal Research Special Publication 41:513.Google Scholar
Penman, D. E., Hönisch, B., Zeebe, R. E., Thomas, E., and Zachos, J. C.. 2014. Rapid and sustained surface ocean acidification during the Paleocene–Eocene Thermal Maximum. Paleoceanography 29:357369.CrossRefGoogle Scholar
Petrizzo, M. R. 2007. The onset of the Paleocene–Eocene Thermal Maximum (PETM) at Sites 1209 and 1210 (Shatsky Rise, Pacific Ocean) as recorded by planktonic foraminifera. Marine Micropaleontology 63:187200.CrossRefGoogle Scholar
Plaziat, J. C., and Perrin, C.. 1992. Multikilometer-sized reefs built by foraminifera (Solenomeris) from the early Eocene of the Pyrenean domain (S. France, N. Spain): palaeoecologic relations with coral reefs. Palaeogeography, Palaeoclimatology, Palaeoecology 96:195231.CrossRefGoogle Scholar
Prazeres, M. 2018. Bleaching-associated changes in the microbiome of large benthic foraminifera of the Great Barrier Reef, Australia. Frontiers in Microbiology 9:2404.CrossRefGoogle ScholarPubMed
Rowan, R. 2004. Coral bleaching: thermal adaptation in reef coral symbionts. Nature 430:742742.CrossRefGoogle ScholarPubMed
Santavy, D. L., Summers, J. K., Engle, V. D., and Harwell, L. C.. 2005. The condition of coral reefs in South Florida (2000) using coral disease and bleaching as indicators. Environmental Monitoring and Assessment 100:129152.CrossRefGoogle ScholarPubMed
Scheibner, C., and Speijer, R. P.. 2008. Late Paleocene–early Eocene Tethyan carbonate platform evolution—a response to long-and short-term paleoclimatic change. Earth-Science Reviews 90:71102.CrossRefGoogle Scholar
Schiebel, R. 2002. Planktic foraminiferal sedimentation and the marine calcite budget. Global Biogeochemical Cycles 16:121.CrossRefGoogle Scholar
Schiebel, R., and Hemleben, C.. 2017. Planktic foraminifers in the modern ocean. Springer, Berlin.CrossRefGoogle Scholar
Schmidt, C., Titelboim, D., Brandt, J., Herut, B., Abramovich, S., Almogi-Labin, A., and Kucera, M.. 2016. Extremely heat tolerant photo-symbiosis in a shallow marine benthic foraminifera. Scientific Reports 6:30930.CrossRefGoogle Scholar
Schmidt, C., Morard, R., Romero, O., and Kucera, M.. 2018. Diverse internal symbiont community in the endosymbiotic foraminifera Pararotalia calcariformata: implications for symbiont shuffling under thermal stress. Frontiers in Microbiology 9. doi: 10.3389/fmicb.2018.02018.CrossRefGoogle ScholarPubMed
Si, W., and Aubry, M. P.. 2018. Vital effects and ecologic adaptation of photosymbiont-bearing planktonic foraminifera during the Paleocene–Eocene thermal maximum, implications for paleoclimate. Paleoceanography and Paleoclimatology 33:112125.CrossRefGoogle Scholar
Simpson, C., Kiessling, W., Mewis, H., Baron-Szabo, R. C., and Müller, J.. 2011. Evolutionary diversification of reef corals: a comparison of the molecular and fossil records. Evolution 65:32743284.CrossRefGoogle ScholarPubMed
Sluijs, A., and Dickens, G. R.. 2012. Assessing offsets between the δ13C of sedimentary components and the global exogenic carbon pool across early Paleogene carbon cycle perturbations. Global Biogeochemical Cycles 26. doi: 10.1029/2011GB004224.CrossRefGoogle Scholar
Speijer, R. P., Scheibner, C., Stassen, P., and Morsi, A. M. M.. 2012. Response of marine ecosystems to deep-time global warming: a synthesis of biotic patterns across the Paleocene–Eocene thermal maximum (PETM). Austrian Journal of Earth Sciences 105:616.Google Scholar
Spero, H. J. 1998. Life history and stable isotope geochemistry of planktonic foraminifera. Paleontological Society Papers 4:736.CrossRefGoogle Scholar
Spero, H. J., and DeNiro, M.. 1987. The influence of symbiont photosynthesis on the δ18O and δ13C values of planktonic foraminiferal shell calcite. Symbiosis 4:213228.Google Scholar
Spero, H. J., Lerche, I., and Williams, D. F.. 1991. Opening the carbon isotope “vital effect” black box, 2, quantitative model for interpreting foraminiferal carbon isotope data. Paleoceanography 6:639655.CrossRefGoogle Scholar
Spero, H. J., Bijma, J., Lea, D. W., and Bemis, B. E.. 1997. Effect of seawater carbonate concentration on foraminiferal carbon and oxygen isotopes. Nature 390:497500.CrossRefGoogle Scholar
Spezzaferri, S., El Kateb, A., Pisapia, C., and Hallock, P.. 2018. In situ observations of foraminiferal bleaching in the Maldives, Indian Ocean. Journal of Foraminiferal Research 48:7584.CrossRefGoogle Scholar
Stanley, G., and van de Schootbrugge, B.. 2018. The evolution of the coral–algal symbiosis and coral bleaching in the geologic past. Pp. 926 in van Oppen, M. J. H., Madeleine and Lough, J., eds. Coral bleaching: patterns, processes, causes and consequences. Springer International, Cham, Switzerland.CrossRefGoogle Scholar
Stap, L., Lourens, L., Van Dijk, A., Schouten, S., and Thomas, E.. 2010. Coherent pattern and timing of the carbon isotope excursion and warming during Eocene Thermal Maximum 2 as recorded in planktic and benthic foraminifera. Geochemistry, Geophysics, Geosystems 11. doi: 10.1029/2010GC003097.CrossRefGoogle Scholar
Stassen, P., Speijer, R. P., and Thomas, E.. 2014. Unsettled puzzle of the Marlboro clays. Proceedings of the National Academy of Sciences USA 111:e1066e1067.CrossRefGoogle ScholarPubMed
Sugarman, P. J., Miller, K. G., Browning, J. V., McLaughlin, P. P., Brenner, G. J., Buttari, B., Cramer, B. S., Harris, A., Hernandez, J., Katz, M. E., Lettini, B., Misintseva, S., Monteverde, D. H., Olsson, R. K., Patrick, L., Roman, E., Wojtko, M. J., Aubry, M., Feigenson, M. D., Barron, J. A., Curtin, S., Cobbs, G., Cobbs, G. III, Bukry, D., and Huffman, B. A.. 2005. Millville Site. Proceedings of the Ocean Drilling Program, Initial Reports 174AX (Suppl):1–94. College Station, Tex.Google Scholar
Takagi, H., Kimoto, K., Fujiki, T., and Moriya, K.. 2018. Effect of nutritional condition on photosymbiotic consortium of cultured Globigerinoides sacculifer (Rhizaria, Foraminifera). Symbiosis 76:2539.CrossRefGoogle Scholar
Takagi, H., Kimoto, K., Fujiki, T., Saito, H., Schmidt, C., Kucera, M., and Moriya, K.. 2019. Characterizing photosymbiosis in modern planktonic foraminifera. Biogeosciences 16:33773396.CrossRefGoogle Scholar
Takeda, K., and Kaiho, K.. 2007. Faunal turnovers in central Pacific benthic foraminifera during the Paleocene–Eocene thermal maximum. Palaeogeography, Palaeoclimatology, Palaeoecology 251:175197.CrossRefGoogle Scholar
Thomas, D. J., Zachos, J. C., Bralower, T. J., Thomas, E., and Bohaty, S.. 2002. Warming the fuel for the fire: evidence for the thermal dissociation of methane hydrate during the Paleocene–Eocene thermal maximum. Geology 30:1067.2.0.CO;2>CrossRefGoogle Scholar
Thomas, E., 2003. Extinction and food at the sea floor: a high-resolution benthic foraminiferal record across the initial Eocene Thermal Maximum, Southern Ocean Site 690. In S. Wing, P. Gingerich, B. Schmitz, and E. Thomas, eds. Causes and consequences of globally warm climates of the Paleogene. Geological Society of America Special Paper 369:319–332.CrossRefGoogle Scholar
Thomas, E., and Shackleton, N. J.. 1996. The Paleocene–Eocene benthic foraminiferal extinction and stable isotope anomalies. Geological Society of London Special Publication 101:401441.CrossRefGoogle Scholar
Thomas, E., Zachos, J., and Bralower, T.. 2000. Deep-sea environments on a warm earth: latest Paleocene–early Eocene. Pp. 132160 in Huber, B., MacLeod, K., and Wing, S., eds. Warm climates in earth history. Cambridge University Press, Cambridge.Google Scholar
Tripati, A., and Elderfield, H.. 2005. Deep-sea temperature and circulation changes at the Paleocene–Eocene Thermal Maximum. Science 308:18941898.CrossRefGoogle Scholar
Wade, B. S., Al-Sabouni, N., Hemleben, C., and Kroon, D.. 2008. Symbiont bleaching in fossil planktonic foraminifera. Evolutionary Ecology 22:253265.CrossRefGoogle Scholar
Weiss, A. M., and Martindale, R. C.. 2019. Paleobiological traits that determined scleractinian coral survival and proliferation during the late Paleocene and early Eocene hyperthermals. Paleoceanography and Paleoclimatology 34:252274.CrossRefGoogle Scholar
Westerhold, T., Röhl, U., Donner, B., Mccarren, H. K., and Zachos, J. C.. 2011. A complete high-resolution Paleocene benthic stable isotope record for the central Pacific (ODP Site 1209). Paleoceanography 26:113.CrossRefGoogle Scholar
Winguth, A. M. E., Thomas, E., and Winguth, C.. 2012. Global decline in ocean ventilation, oxygenation, and productivity during the Paleocene–Eocene Thermal Maximum: implications for the benthic extinction. Geology 40:263266.CrossRefGoogle Scholar
Zachos, J. C., Wara, M. W., Bohaty, S., Delaney, M. L., Petrizzo, M. R., Brill, A., Bralower, T. J., and Premoli-Silva, I.. 2003. A transient rise in tropical sea surface temperature during the Paleocene–Eocene thermal maximum. Science 302:15511554.CrossRefGoogle ScholarPubMed
Zeebe, R. E., Bijma, J., and a Wolf-Gladrow, D.. 1999. A diffusion-reaction model of carbon isotope fractionation in foraminifera. Marine Chemistry 64:199227.CrossRefGoogle Scholar