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Effect of a Jurassic Oceanic Anoxic Event on Belemnite Ecology and Evolution

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Effect of a Jurassic Oceanic Anoxic Event on Belemnite Ecology and Evolution Effect of a Jurassic oceanic anoxic event on belemnite ecology and evolution Clemens Vinzenz Ullmanna,1, Nicolas Thibaulta, Micha Ruhla,b, Stephen P. Hesselbob,2, and Christoph Kortea aDepartment of Geosciences and Natural Resource Management, University of Copenhagen, 1350 Copenhagen, Denmark; and bDepartment of Earth Sciences, University of Oxford, Oxford OX1 3AN, United Kingdom Edited by James P. Kennett, University of California, Santa Barbara, CA, and approved May 29, 2014 (received for review October 25, 2013) The Toarcian oceanic anoxic event (T-OAE; ∼183 million y ago) is intruded organic-rich substrates (5) and biogenic methane from possibly the most extreme episode of widespread ocean oxygen ocean floor clathrates (7, 10). deficiency in the Phanerozoic, coinciding with rapid atmospheric Constraining the causes and magnitude of the observed p CO2 increase and significant loss of biodiversity in marine faunas. changes in the carbon cycle relies on analytical results from the The event is a unique past tipping point in the Earth system, where sedimentary record. Major obstacles for these reconstructions rapid and massive release of isotopically light carbon led to a major arise because the commonly analyzed bulk samples always rep- perturbation in the global carbon cycle as recorded in organic and resent mixtures of different phases, which may also have been inorganic C isotope records. Modern marine ecosystems are pro- affected by postdepositional alteration. Samples of macrofossil jected to experience major loss in biodiversity in response to calcite may occur only sparsely and are isotopically more het- enhanced ocean anoxia driven by anthropogenic release of green- erogeneous than bulk materials, and signals can be complicated house gases. Potential consequences of this anthropogenic forcing by habitat and vital effects. Macrofossil calcite can, however, be can be approximated by studying analog environmental perturba- assessed for its preservation state and carry significant in- tions in the past such as the T-OAE. Here we present to our knowl- formation about environmental change and the faunal response edge the first organic carbon isotope record derived from the to it. For the Jurassic and Cretaceous, the bullet-shaped fossil- organic matrix in the calcite rostra of early Toarcian belemnites. ized remains (calcite rostra) of belemnites, extinct marine We combine both organic and calcite carbon isotope analyses of predatory cephalopods, are one of the prime sources for marine individual specimens of these marine predators to obtain a refined paleoenvironmental reconstruction. The globally observed early reconstruction of the early Toarcian global exogenic carbon cycle Toarcian negative CIE, which is well known from bulk organic perturbation and belemnite paleoecology. The organic carbon iso- tope data combined with measurements of oxygen isotope values and carbonate carbon isotope records, is either small or absent in from the same specimens allow for a more robust interpretation of the calcite of the rostra (12, 13). This missing expression of the the interplay between the global carbon cycle perturbation, envi- negative CIE in belemnite calcite has led some researchers to ronmental change, and biotic response during the T-OAE. We infer question whether the T-OAE has been a climatic event of global that belemnites adapted to environmental change by shifting their extent (12, 13). habitat from cold bottom waters to warm surface waters in re- Isotopic investigations of belemnites have so far only focused – sponse to expanded seafloor anoxia. on the inorganic matrix of the rostra (12 14). The isotopic composition of the organic matrix, which is embedded in the calcite of the rostrum, has previously not been studied, even limatic and environmental change driven by anthropogenic Cgreenhouse gases is predicted to severely compromise though its presence has been known for several decades (15, 16). modern-day marine ecosystems through ocean anoxia and pos- sibly ocean acidification (1, 2). Expanded and intensified oxygen Significance minimum zones, accompanied by deposition of organic-rich ∼ EARTH, ATMOSPHERIC, sediments, have occurred multiple times in the past and are The Toarcian oceanic anoxic event (OAE; 183 million y ago) is AND PLANETARY SCIENCES termed oceanic anoxic events (OAEs) (3). The Early Jurassic marked by one of the largest carbon cycle perturbations in Toarcian oceanic anoxic event (T-OAE) is among the best- Earth history, rapid climate change, widespread ocean oxygen deficiency, and strong changes in marine ecosystems. The studied of OAEs and represents an interval of global warming temporal links between increasing atmospheric pCO , changes (3), high continental weathering intensity (3, 4), and increased 2 in ocean oxygen availability, and marine biotic response during atmospheric pCO2 (5). This event is associated with an enhanced this event are still poorly understood. Here we use isotopic ECOLOGY turnover of taxa, enhanced sedimentary organic matter accu- analyses of calcite and organic matter from belemnites, marine mulation, and perturbations in the geochemical cycles of essen- predators of that time, to address their response to bottom tial elements such as carbon, nitrogen, and sulfur and redox- water anoxia during the OAE. We infer that some belemnite sensitive elements such as molybdenum (3). Cyclostratigraphic taxa showed resilience to a strong reduction in ocean oxygen studies of the Toarcian sedimentary record suggest a short (<1 availability and occupied ecological niches in the Cleveland My) duration for the event and point to recurring, orbitally Basin (United Kingdom), enabling a strong evolutionary di- paced pulses of rapid environmental change (6–9). The exogenic versification after the event. carbon cycle was globally perturbed as evidenced by a large negative carbon isotope excursion (CIE), which is expressed in Author contributions: C.V.U. designed research; C.V.U. performed research; C.V.U., N.T., M.R., S.P.H., and C.K. participated in sample collection; C.V.U., N.T., and M.R. analyzed marine and terrestrial organic and inorganic carbon in the data; and C.V.U., N.T., M.R., S.P.H., and C.K. wrote the paper. northern and southern hemispheres (5, 10, 11). Various potential The authors declare no conflict of interest. triggers for the T-OAE have been identified. The event co- This article is a PNAS Direct Submission. incided with the extensive volcanic activity of the Karoo-Ferrar 1To whom correspondence should be addressed. Email: [email protected]. large igneous province (6–8). Changes in the global carbon cycle 2Present address: Camborne School of Mines, College of Engineering, Mathematics and through the T-OAE have been hypothesized to be forced by Physical Sciences, University of Exeter, Penryn TR10 9FE, United Kingdom. rapid and massive venting of isotopically depleted carbon This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. through the production of thermogenic methane from sill- 1073/pnas.1320156111/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1320156111 PNAS | July 15, 2014 | vol. 111 | no. 28 | 10073–10076 Downloaded by guest on September 27, 2021 organic and inorganic carbon of individual belemnite rostra. The Arctic Sea rostra are derived from the Cleveland Basin (Yorkshire, United Kingdom), a subbasin of the epicontinental Laurasian Seaway Greenland with water depths of ∼100 m during the early Toarcian (17) (Fig. 1). Using our newly generated organic carbon isotope data in 50° N combination with isotopic data from the calcite of individual rostra, we reassess the paleoenvironmental significance of the isotopic composition of rostral calcite. We suggest a solution to the apparent paradox of the missing negative CIE in the calcite of the rostra by incorporating the ecological and evolutionary response of belemnites to bottom water anoxia into the in- 40° N Fenno-Scandian Shield elevation terpretation of the isotope data. m asl Results Cleveland 0 Basin -40 Combined analytical results from organic shell matrix and car- -80 bonate of well-preserved belemnites from the sedimentary suc- 30° N -120 cessions of the Cleveland Basin are presented (see Materials and -160 Methods and Supporting Information for methodology and pres- -200 – -400 ervation criteria and Tables S1 S3 for results). The C isotope δ13 -600 record of belemnite calcite ( Cbel-carb) through the ten- 1000 km Tethys Ocean -800 uicostatum ammonite biozone is derived from the genus Passa- loteuthis and shows an average value of +2.3 ± 1.4‰ (2 SD, n = Fig. 1. Paleogeography of the Laurasian Seaway (or Viking Corridor), 94). The Passaloteuthis record of the top semicelatum subzone modified from ref. 17. Sampling location is marked by a yellow star. lacks the clear representation of a strong negative carbon isotope shift (CIE) observed in coeval bulk organic carbon (12, 13) (Fig. 2). The following falciferum zone is characterized by the disap- The organic matter in belemnite rostra can provide comple- pearance of Passaloteuthis and the appearance of Acrocoelites in mentary information about the animal’s habitat and mode of life. the Cleveland Basin (Fig. 2). Within the lower exaratum subzone, In this study we fill this gap by the analysis of the cogenetic a distinct negative CIE is observed in the belemnite calcite (Fig. 2). δ13C ‰ PDB Δ13C ‰ meters carb carb-org -1 1 3 5 24 26 28 30 32 34 45 comm. bifrons 40 35 Acrocoelites vulgaris falciferum 30 surface water
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