Hostname: page-component-76fb5796d-zzh7m Total loading time: 0 Render date: 2024-04-26T05:11:06.142Z Has data issue: false hasContentIssue false
  • English
  • Français

Physicochemical controls on biogeographic variation of benthic foraminiferal test size and shape

Published online by Cambridge University Press:  28 April 2016

Caitlin R. Keating-Bitonti  and
Jonathan L. Payne
Caitlin R. Keating-Bitonti
Affiliation:
Department of Geological Sciences, Stanford University, Stanford, California 94305, U.S.A. E-mail: crkeatin@stanford.edu.
Jonathan L. Payne
Affiliation:
Department of Geological Sciences, Stanford University, Stanford, California 94305, U.S.A. E-mail: crkeatin@stanford.edu.
Get access Rights & Permissions [Opens in a new window]

Abstract

The sizes and shapes of marine organisms often vary systematically across latitude and water depth, but the environmental factors that mediate these gradients in morphology remain incompletely understood. A key challenge is isolating the individual contributions of many, often correlated, environmental variables of potential biological significance. Benthic foraminifera, a diverse group of rhizarian protists that inhabit nearly all marine environments, provide an unparalleled opportunity to test statistically among the various potential controls on size and volume–to–surface area ratio. Here, we use 7035 occurrences of 541 species of Rotallid foraminifera across 946 localities spanning more than 60 degrees of latitude and 1600 m of water depth around the North American continental margin to assess the relative influences of temperature, oxygen availability, carbonate saturation, and particulate organic carbon flux on their test volume and volume–to–surface area ratio. For the North American data set as a whole, the best model includes temperature and dissolved oxygen concentration as predictors. This model also applies to data from the Pacific continental margin in isolation, but only temperature is included in the best model for the Atlantic. Because these findings are consistent with predictions from the first principles of cell physiology, we interpret these statistical associations as the expressions of physiological selective pressures on test size and shape from the physical environment. Regarding existing records of temporal variation in foraminiferal test size across geological time in light of these findings suggests that the importance of temperature variation on the evolution of test volume and volume–to–surface area ratio may be underappreciated. In particular, warming may have played as important a role as reduced oxygen availability in causing test size reduction during past episodes of environmental crisis and is expected to inflict metabolic stress on benthic foraminifera over the next century due to anthropogenic climate change.

Type
Articles
Information
Paleobiology , Volume 42 , Issue 4 , November 2016 , pp. 595 - 611
Copyright
Copyright © 2016 The Paleontological Society. All rights reserved 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

ABBYY. 2011. ABBYY® FineReader, Version 11.Google Scholar
Alegret, L., Ortiz, S., Arenillas, I., and Molina, E.. 2010. What happens when the ocean is overheated? The foraminiferal response across the Paleocene–Eocene thermal maximum at the Alamedilla section (Spain). Geological Society of America Bulletin 122:1616–1624.Google Scholar
Antonov, J. I., Seidov, D., Boyer, T. P., Locarnini, R. A., Mishonov, A. V., Garcia, H. E., Baranova, O. K., Zweng, M. M., and Johnson, D. R.. 2010. World ocean atlas 2009, Vol. 2. Salinity In S. Levitus, ed. NOAA atlas NESDIS 69. Government Printing Office, Washington, D.C.Google Scholar
Armstrong, H. A., and Brasier, M. D.. 2005. Microfossils. Blackwell, Malden, Mass.Google Scholar
Ashton, K. G., Tracy, M. C., and de Queiroz, A.. 2000. Is Bergmann’s rule valid for mammals? American Naturalist 156:390–415.Google Scholar
Bernhard, J. M. 1986. Characteristic assemblages and morphologies of benthic foraminifera from anoxic, organic-rich deposits: Jurassic through Holocene. Journal of Foraminiferal Research 16:207–215.Google Scholar
Bernhard, J. M., Buck, K. R., Farmer, M. A., and Bowser, S. S.. 2000. The Santa Barbara Basin is a symbiosis oasis. Nature 403:77–80.CrossRefGoogle Scholar
Bernhard, J. M., Buck, K. R., and Barry, J. P.. 2001. Monterey Bay cold-seep biota: assemblages, abundance, and ultrastructure of living foraminifera. Deep-Sea Research I 48:2233–2249.Google Scholar
Bernhard, J. M., Casciotti, K. L., McIlvin, M. R., Beaudoin, D. J., Visscher, P. T., and Edgcomb, V. P.. 2012. Potential importance of physiologically diverse benthic foraminifera in sedimentary nitrate storage and respiration. Journal of Geophysical Research 117:G03002.Google Scholar
Bijma, J., Pörtner, H., Yesson, C., and Rogers, A. D. 2013. Climate change and the oceans—what will the future hold? Marine Pollution Bulletin 74:495–505.Google Scholar
Blackmon, P. D., and Todd, R.. 1959. Mineralogy of some foraminifera as related to their classification and ecology. Journal of Paleontology 33:1–15.Google Scholar
Boltovskoy, E. 1988. Size change in the phylogeny of Foraminifera. Lethaia 21:375–382.CrossRefGoogle Scholar
Bopp, L., Resplandy, L., Orr, J. C., Doney, S. C., Dunne, J. P., Gehlen, M., Halloran, P., Heinze, C., Ilyina, T., Seferian, R., and Tjiputra, J.. 2013. Multiple stressors of ocean ecosystems in the 21st century: projections with CMIP5 models. Biogeosciences 10:6225–6245.CrossRefGoogle Scholar
Broecker, W. S., and Peng, T. H.. 1982. Tracers in the sea. Lamont-Doherty Geological Observatory, Palisades, N.Y.Google Scholar
Brown, J. H. 1995. Macroecology. University of Chicago Press, Chicago.Google Scholar
Buzas, M. A., Collins, L. S., and Culver, S. J.. 2002. Latitudinal difference in biodiversity caused by higher tropical rate of increase. Proceedings of the National Academy of Sciences USA 99:7841–7843.Google Scholar
CARINA Group. 2009. Carbon in the Arctic Mediterranean Seas region—the CARINA Project: results and data. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, Tennessee.Google Scholar
Chapelle, G., and Peck, L. S.. 1999. Polar gigantism dictated by oxygen availability. Nature 399:114–115.Google 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
Culver, S. J., and Buzas, M. A.. 1980. Distribution of recent benthic foraminifera off the North American Atlantic coast. Smithsonian Institution Press, Washington, D.C.Google Scholar
Culver, S. J., and Buzas, M. A.. 1981. Distribution of recent benthic foraminifera in the Gulf of Mexico. Smithsonian Institution Press, Washington, D.C.Google Scholar
Culver, S. J., and Buzas, M. A.. 1982. Distribution of recent benthic foraminifera in the Caribbean region. Smithsonian Institution Press, Washington, D.C.Google Scholar
Culver, S. J., and Buzas, M. A.. 1985. Distribution of recent benthic foraminifera off the North American Pacific coast from Oregon to Alaska. Smithsonian Institution Press, Washington, D.C.Google Scholar
Culver, S. J., and Buzas, M. A.. 1986. Distribution of recent benthic foraminifera off the North American Pacific coast from California to Baja. Smithsonian Institution Press, Washington, D.C.Google Scholar
Culver, S. J., and Buzas, M. A.. 1987. Distribution of recent benthic foraminifera off the Pacific coast of Mexico and Central America. Smithsonian Institution Press, Washington, D.C.CrossRefGoogle Scholar
DeLong, J. P., Okie, J. G., Moses, M. E., Sibly, R. M., and Brown, J. H.. 2010. Shifts in metabolic scaling, production, and efficiency across major evolutionary transitions of life. Proceedings of the National Academy of Sciences USA 107:12941–12945.Google Scholar
de Nooijer, L. J., Langer, G., Nehrke, G., and Bijma, J.. 2009. Physiological controls on seawater uptake and calcification in the benthic foraminifer Ammonia tepida . Biogeosciences 6:2669–2675.Google Scholar
Dickson, A. G. 1990. Thermodynamics of the dissociation of boric acid in synthetic seawater from 273.15 to 318.15 K. Deep-Sea Research A (Oceanographic Research Papers) 37:755–766.Google Scholar
Ellis, B. F., and Messina, A. R.. 1940–2006. Catalogue of foraminifera. American Museum of Natural History, New York.Google Scholar
Environmental Systems Research Institute. 2011. ArcGIS Desktop, Release 10. ESRI, Redlands, Calif.Google Scholar
Erez, J. 2003. The source of ions for biomineralization in foraminifera and their implications for paleoceanographic proxies. Pp 115–150. in P. M. Dove, J. J. De Yoreo, and S. Weiner, eds. Biomineralization. Mineralogical Society of America and Geochemical Society, Washington D.C.Google Scholar
Estes, J. A., Lindberg, D. R., and Wray, C.. 2005. Evolution of large body size in abalones (Haliotis): patterns and implications. Paleobiology 31:591–606.Google Scholar
Forster, J., Hirst, A. G., and Atkinson, D.. 2012. Warming-induced reductions in body size are greater in aquatic than terrestrial species. Proceedings of the National Academy of Sciences USA 109:19310–19314.Google Scholar
Foster, J. B. 1964. Evolution of mammals on islands. Nature 202:234–235.CrossRefGoogle Scholar
Garcia, H. E., Locarnini, R. A., Boyer, T. P., Antonov, J. I., Baranova, O. K., Zweng, M. M., and Johnson, D. R.. 2010. World ocean atlas 2009, Vol. 3. Dissolved oxygen, apparent oxygen utilization, and oxygen saturation In S. Levitus, ed. NOAA atlas NESDIS 70. U.S. Government Printing Office, Washington, D.C.Google Scholar
Gattuso, J.-P., Epitalon, J.-M., and Lavigne, H.. 2015. seacarb: seawater carbonate chemistry. R package, Version 3.0.11. https://CRAN.R-project.org/package=seacar.Google Scholar
Gerlach, S. A., Hahn, A. E., and Schrage, M.. 1985. Size spectra of benthic biomass and metabolism. Marine Ecology Progress Series 26:161–173.Google Scholar
Geslin, E., Risgaard-Petersen, N., Lombard, F., Metzger, E., Langlet, D., and Jorissen, F. J.. 2011. Oxygen respiration rates of benthic foraminifera as measured with oxygen microsensors. Journal of Experimental Marine Biology and Ecology 296:108–114.Google Scholar
Gillooly, J. F., Brown, J., West, G. B., Savage, V. M., and Charnov, E. L.. 2001. Effects of size and temperature on metabolic rate. Science 293:2248–2251.Google Scholar
Gooday, A. J., Levin, L. A., da Silva, A. A., Bett, B. J., Cowie, G. L., Dissard, D., Gage, J. D., Hughes, D. J., Jeffreys, R., Lamont, P. A., Larkin, K. E., Murty, S. J., Schumacher, S., Whitcraft, C., and Woulds, C.. 2009. Faunal responses to oxygen gradients on the Pakistan margin: a comparison of foraminiferans, macrofauna and megafauna. Deep-Sea Research II 56:488–502.Google Scholar
Gooday, A. J., Bett, B. J., Escobar, E., Ingole, B., Levin, L. A., Neira, C., Raman, A. V., and Sellanes, J.. 2010. Habitat heterogeneity and its influence on benthic biodiversity in oxygen minimum zones. Marine Ecology 31:125–147.Google Scholar
Gould, S. J. 1997. Cope’s rule as psychological artefact. Nature 385:199–200.Google Scholar
Groves, J. R., Rettori, R., Payne, J. L., Boyce, M. D., and Altiner, D.. 2007. End-Permian mass extinction of lagenide foraminifers in the southern Alps (northern Italy). Journal of Paleontology 81:415–434.Google Scholar
Gruber, N. 2011. Warming up, turning sour, losing breath: ocean biogeochemistry under global change. Philosophical Transactions of the Royal Society of London A 369:1980–1996.Google Scholar
Hadly, E. A., and Maurer, B. A.. 2001. Spatial and temporal patterns of species diversity in montane mammal communities of western North America. Evolutionary Ecology Research 3:477–486.Google Scholar
Hannah, F., Rogerson, A., and Laybourn-Parry, J.. 1994. Respiration rates and biovolumes of common benthic foraminifera (protozoa). Journal of the Marine Biological Association of the UK 74:301–312.Google Scholar
Heinz, P., and Geslin, E.. 2012. Ecological and biological response of benthic foraminifera under oxygen-depleted conditions: evidence from laboratory approaches. Pp. 287–303. in A., Altenbach, J. M., Bernhard, and J. Seckbach, eds. Anoxia: evidence for eukaryote survival and paleontological strategies. Springer, Netherlands.Google Scholar
Helly, J. J., and Levin, L. A.. 2004. Global distribution of naturally occurring marine hypoxia on continental margins. Deep-Sea Research I 51:1159–1168.Google Scholar
Hohenegger, J., and Briguglio, A.. 2014. Methods for estimating individual growth of foraminifera based on chamber volumes. Pp 29–54. in H. Kitazato, and J. M. Bernhard, eds. Approaches to studying living foraminifera: collection, maintenance and experimentation. Springer, Tokyo.Google Scholar
Hunt, G., and Roy, K.. 2006. Climate change, body size evolution, and Cope’s rule in deep-sea ostracodes. Proceedings of the National Academy of Sciences USA 103:1347–1352.Google Scholar
Hunt, G., Wicaksono, S. A., Brown, J. E., and MacLeod, K. G.. 2010. Climate-driven body-size trends in the ostracod fauna of the deep Indian Ocean. Palaeontology 53:1255–1268.Google Scholar
IOC, IHO, and BODC. 2003. Centenary edition of the GEBCO digital atlas, published on CD-ROM on behalf of the Intergovernmental Oceanographic Commission and the International Hydrographic Organization as part of the General Bathymetric Chart of the Oceans, British Oceanographic Data Centre, Liverpool, U.K.Google Scholar
Jablonski, D. 1993. The tropics as a source of evolutionary novelty through geological time. Nature 364:142–144.Google Scholar
Joachimski, M. M., Lai, X., Shen, S., Jiang, H., Luo, G., Chen, B., Chen, J., and Sun, Y.. 2012. Climate warming in the latest Permian and the Permian–Triassic mass extinction. Geology 40:195–198.Google Scholar
Jorissen, F. J., de Stigter, H. C., and Widmark, J. G. V.. 1995. A conceptual model explaining benthic foraminiferal microhabitats. Marine Micropaleontology 26:3–15.CrossRefGoogle Scholar
Kaiho, K. 1999a. Effect of organic carbon flux and dissolved oxygen on benthic foraminifera oxygen index (BFOI). Marine Micropaleontology 37:67–76.CrossRefGoogle Scholar
Kaiho, K. 1999b. Evolution in the test size of deep-sea benthic foraminifera during the past 120 m.y. Marine Micropaleontology 37:53–65.Google Scholar
Kaiho, K., Takeda, K., Petrizzo, M. R., and Zachos, J. C.. 2006. Anomalous shifts in tropical Pacific planktonic and benthic foraminiferal size during the Paleocene–Eocene thermal maximum. Palaeogeography, Palaeoclimatology, Palaeoecology 237:456–464.Google Scholar
Key, R. M., Kozyr, A., Sabine, C. L., Lee, K., Wanninkhof, R., Bullister, J., Feely, R. A., Millero, F., Mordy, C., and Peng, T.-H.. 2004. A global ocean carbon climatology: results from Global Data Analysis Project (GLODAP). Global Biogeochemical Cycles 18:GB4031.Google Scholar
Koho, K., Piña-Ochoa, E., Geslin, E., and Risgaard-Petersen, N.. 2011. Survival and nitrate uptake mechanisms of foraminifers (Globobulimina turgida): laboratory experiments. FEM Microbiology Ecology 75:273–283.Google Scholar
Korsun, S., Hald, M., Panteleeva, N., and Tarasov, G.. 1998. Biomass of foraminifera in the St. Anna trough, Russian arctic continental margin. Sarsia 83:419–431.Google Scholar
Levin, L. A., and Gage, J. D.. 1998. Relationship between oxygen, organic matter and the diversity of bathyal macrofauna. Deep-Sea Research II 45:129–163.Google Scholar
Locarnini, R. A., Mishonov, A. V., Antonov, J. I., Boyer, T. P., Garcia, H. E., Baranova, O. K., Zweng, M. M., and Johnson, D. R.. 2010. World ocean atlas 2009, Vol. 1. Temperature In S. Levitus, ed. NOAA atlas NESDIS 68. U.S. Government Printing Office, Washington, D.C.Google Scholar
Loope, G. R., Kump, L. R., and Arthur, M. A.. 2013. Shallow water redox conditions from the Permian–Triassic boundary microbialite: the rare earth element and iodine geochemistry of carbonates from Turkey and South China. Chemical Geology 351:195–208.Google Scholar
Lutz, M. J., Caldeira, K., Dunbar, R. B., and Behrenfeld, M. J.. 2007. Seasonal rhythms of net primary productivity and particulate organic carbon flux to depth describe the efficiency of biological pump in the global ocean. Journal of Geophysical Research 112:C10011.Google Scholar
Mayr, E. 1963. Animal species and evolution. Harvard University Press, Cambridge.Google Scholar
McClain, C. R., and Rex, M. A.. 2001. The relationship between dissolved oxygen concentration and maximum size in deep-sea turrid gastropods: an application of quantile regression. Marine Biology 139:681–685.Google Scholar
McClain, C. R., Boyer, A., and Rosenberg, G. 2006. The island rule and the evolution of body size in the deep sea. Journal of Biogeography 33:1578–1584.Google Scholar
McClain, C. R., Allen, A. P., Tittensor, D. P., and Rex, M. A.. 2012a. The energetics of life on the deep seafloor. Proceedings of the National Academy of Sciences USA 38:15366–15371.CrossRefGoogle Scholar
McClain, C. R., Gullett, T., Jackson-Ricketts, J., and Unmack, P. J.. 2012b. Increased energy promotes size-based niche availability in marine mollusks. Evolution 66:2204–2215.Google Scholar
Millien, V., Lyons, S. K., Olson, L., Smith, F. A., Wilson, A. B., and Yom-Tov, Y.. 2006. Ecotypic variation in the context of global climate change: revisiting the rules. Ecology Letters 9:853–896.Google Scholar
Moodley, L., Boschker, H. T. S., Middelburg, J. J., Pel, R., Harman, P. M. J., de Deckere, E., and Heip, C. H. R.. 2000. Ecological significance of benthic foraminifera: 13C labelling experiments. Marine Ecology Progress Series 202:289–295.Google Scholar
Murray, J. W. 1991. Ecology and paleoecology of benthic foraminifera. Longman Scientific and Technical, Essex, U.K.Google Scholar
Nardelli, M. P., Barras, C., Metzger, E., Mouret, A., Filipsson, H. L., Jorissen, F. J., and Geslin, E.. 2014. Experimental evidence for foraminiferal calcification under anoxia. Biogeosciences 11:4029–4038.Google Scholar
Park, M. Y., and Hastie, T.. 2013. glmpath: L1 regularization path for generalized linear models and cox proportional hazards model. R package, Version 0.97. https://CRAN.R-project.org/package=glmpath.Google Scholar
Payne, J. L., Summers, M., Rego, B. L., Altiner, D., Wei, J., Yu, M., and Lehrmann, D. J.. 2011. Early and middle Triassic trends in diversity, evenness, and size of foraminifers on a carbonate platform in south China: implications for tempo and mode of biotic recovery from the end-Permian mass extinction. Paleobiology 37:409–425.Google Scholar
Payne, J. L., Groves, J. R., Jost, A. B., Nguyen, T., Moffitt, S. E., Hill, T. M., and Skotheim, J. M.. 2012a. Late Paleozoic fusulinoidean gigantism driven by atmospheric hyperoxia. Evolution 66:2929–2939.Google Scholar
Payne, J. L., Jost, A. B., Wang, S. C., and Skotheim, J. M. 2012b. A shift in the long-term mode of foraminiferan size evolution caused by the end-Permian mass extinction. Evolution 67:816–827.Google Scholar
Peck, L. S., and Harper, E. M.. 2010. Variation in size of living articulated brachiopods with latitude and depth. Marine Biology 157:2205–2213.Google Scholar
Peters, R. H. 1983. The ecological implications of body size. Cambridge University Press, Cambridge.Google Scholar
Piña-Ochoa, E., Høgslund, S., Geslin, E., Cedhagen, T., Revsbech, N. P., Nielsen, L. P., Schweizer, M., Jorissen, F. J., and Rysgaard-Peterson, N.. 2010. Widespread occurrence of nitrate storage and denitrification among foraminifera and gromiids. Proceedings of the National Academy of Sciences USA 107:1148–1153.Google Scholar
Rego, B. L., Wang, S. C., Altiner, D., and Payne, J. L.. 2012. Within- and among-genus components of size evolution during mass extinction, recovery, and background intervals: a case study of Late Permian through Late Triassic foraminifera. Paleobiology 38:627–643.CrossRefGoogle Scholar
Rex, M. A., and Etter, R. J.. 1998. Bathymetric patterns of body size: implications for deep-sea biodiversity. Deep-Sea Research II 45:103–127.Google Scholar
Rex, M. A., Etter, R. J., Morris, J. S., Crouse, J., McClain, C. R., Johnson, N. A., Stuart, C. T., Deming, J. W., Thies, R., and Avery, R.. 2006. Global bethymetric patterns of standing stock and body size in the deep-sea benthos. Marine Ecology Progress Series 317:1–8.Google Scholar
Risgaard-Petersen, N., Langezaal, A. M., Ingvardsen, S., Schmid, M. C., Jeten, M. S. M., Ob 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. Complete denitrification in a benthic foraminifer. Nature 443:93–96.Google Scholar
Romano, C., Goudemand, N., Vennemann, T. W., Ware, D., Schneebeli-Hermann, E., Hochuli, P. A., Bruhwiler, T., Brinkmann, W., and Bucher, H.. 2013. Climatic and biotic upheavals following the end-Permian mass extinction. Nature Geoscience 6:57–60.Google Scholar
Roy, K., Jablonski, D., and Martien, K. K.. 2000. Invarient size-frequency distributions along a latitudinal gradient in marine bivalves. Proceedings of the National Academy of Sciences USA 97:13150–13155.Google Scholar
Schweizer, M., Pawlowski, J., Kouwenhoven, T. J., Guiard, J., and van der Zwaan, B.. 2008. Molecular phylogeny of Rotaliida (Foraminifera) based on complete small subunit rDNA sequences. Marine Micropaleontology 66:233–246.Google Scholar
Sen Gupta, B. K. 1999. Modern Foraminifera. Kluwer Academic Publishers, Dordrecht, the Netherlands.Google Scholar
Sen Gupta, B. K., and Machain-Castillo, M. L.. 1993. Benthic foraminifera in oxygen-poor habitats. Marine Micropaleontology 20:183–201.Google Scholar
Song, H., Tong, J., and Chen, Z. Q.. 2011. Evolutionary dynamics of the Permian–Triassic foraminifer size: evidence for Lilliput effect in the end-Permian mass extinction and its aftermath. Palaeogeography, Palaeoclimatology, Palaeoecology 308:98–110.CrossRefGoogle Scholar
Sun, Y., Joachimski, M. M., Wignall, P. B., Yan, C., Chen, Y., Jiang, H., Wang, L., and Lai, X.. 2012. Lethally hot temperatures during the early Triassic greenhouse. Science 338:366–370.Google Scholar
Travis, J. L., and Bowser, S. S.. 1991. The motility of foraminifera. Pp. 91–155. in J. J. Lee, and O. R. Anderson, eds. Biology of Foraminifera. Academic Press, San Diego.Google Scholar
Van Valen, L. 1973. Pattern and the balance of nature. Evolutionary Theory 1:31–49.Google Scholar
Verberk, W. C. E. P., and Atkinson, D. T.. 2013. Why polar gigantism and Palaeozoic gigantism are not equivalent: effects of oxygen and temperature on the body size of ectotherms. Functional Ecology 27:1275–1285.Google Scholar
Verberk, W. C. E. P., Bilton, D. T., Calosi, P., and Spicer, J. I.. 2011. Oxygen supply in aquatic ectotherms: partial pressure and solubility together explain biodiversity and size patterns. Ecology 92:1565–1572.Google 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 40:263–266.Google Scholar
Woulds, C., Cowie, G. L., Levin, L. A., Andersson, A. J., Middelburg, J. J., Vandewiele, S., Lamont, P. A., Larkin, K. E., Gooday, A. J., Schumacher, S., Whitcraft, C., Jeffreys, R. M., and Schwartz, M.. 2007. Oxygen as a control on seafloor biological communities and their roles in sedimentary carbon cycling. Limnology Oceanography 52:1698–1709.Google Scholar
Zachos, J. C., Pagani, M., Sloan, L., Thomas, E., and Billups, K.. 2001. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–693.Google Scholar