Downloaded from geology.gsapubs.org on July 21, 2015 Short-term euxinia coinciding with rotaliporid extinctions during the -Turonian transition in the middle-neritic eastern North Atlantic inferred from organic compounds

Masahiro Oba1*, Kunio Kaiho1, Takashi Okabe1, Marcos A. Lamolda2, and James D. Wright3 1Institute of Geology and , Tohoku University, Sendai 980-8578, Japan 2Departamento de Estratigrafía y Paleontología, Facultad de Ciencias, Universidad de Granada, 18002 Granada, Spain 3Department of Geological Sciences, Rutgers University, 610 Taylor Road, Piscataway, New Jersey 08854, USA

ABSTRACT 2009). However, the relation between foramini- Oceanic 2 (OAE2), which occurred during the Cenomanian-Turonian (C-T) fer extinction and water-column anoxia and/or transition and lasted 1 m.y., is characterized by a positive global carbon isotopic excursion and euxinia has not been addressed from an organic stepwise extinctions in marine biota. To examine temporal variations in the dissolved geochemical point of view. content of the water column, shallow-marine C-T from northern Spain were ana- This study addresses variations in water- lyzed for concentrations of dibenzothiophenes, which are indicators of euxinic depositional column euxinia during the C-T transition in environments, and 2,3,6-trimethylarylisoprenoids, which probably indicate photic-zone eux- from what was then the middle-neritic inia. The positive excursion in δ13C values of carbonates is accompanied by short-term (103– eastern North Atlantic , using organic 104 yr) and long-term (105 yr) increases in dibenzothiophene and 2,3,6-trimethylarylisopren- geochemical methods. The timing of short- oid concentrations, suggesting that the bottom water and of the eastern marginal term euxinic events relative to the extinction of the North Atlantic Ocean were euxinic. Two of the short-term increases in organic com- of rotaliporid planktonic foraminifers is also pound concentrations took place just after the last occurrence of the planktonic foraminifers investigated. The study section is located east of Rotalipora greenhornensis and R. cushmani. These transient maxima indicate that the extinc- Oviedo, at Arobes, in the province of Asturias, tion of both planktonic foraminifers was due to short-term OAEs lasting 103–104 yr. northern Spain (Fig. 1). The sedimentary suc- cession consists of , marl, and mud- INTRODUCTION minifera showed that the extinction horizon was stone (Fig. 2). Analytical methods are detailed The mid- was generally a time of consistent with low oxygen conditions, and the in the GSA Data Repository.1 extraordinarily warm climates, high sea levels, main cause of this extinction was suggested to and high atmospheric pCO2 levels (e.g., Sch- be the formation of dysoxic intermediate water RESULTS AND DISCUSSION langer et al., 1987; Haq et al., 1987; Clarke and (Kaiho and Hasegawa, 1994). Jenkyns, 1999; Huber et al., 2002; Wilson and Recent organic geochemical studies have Water Depth Norris, 2001). Certain intervals during the mid- sought to provide evidence for anoxic and/ Benthic foraminiferal assemblages in the Cretaceous were characterized by extensive or euxinic conditions in the water column and Arobes section are characterized by Rosalina, deposition of organic-carbon–rich black at the seafl oor during OAE2, especially in the Fursenkoina, Praebulimina, , Hap- across a wide range of marine settings. Because area of what was then the North Atlantic Ocean. lophragmoides, and Lenticulina (see the Data deposition of black shale is favored in oxygen- Molecular (sedimentary derivatives of Repository). This assemblage implies a shal- limited to oxygen-free (anoxic) environments, characteristic biomolecules) of specifi c pig- lower depositional environment than that of ben- these intervals have been interpreted as oceanic ments () biosynthesized by green thic foraminiferal assemblages (Praebulimina, anoxic events (OAEs; Schlanger and Jenkyns, sulfur were detected in C-T samples 1976). The most prominent and widespread of from Deep Sea Drilling Project (DSDP) cores the Cretaceous OAEs spans the Cenomanian- from various sites in the North Atlantic Ocean N 0 100 km Turonian (C-T; ca. 93.5 Ma) boundary and is (Sinninghe Damsté and Köster, 1998; Kuypers 4°E called OAE2, or the C-T boundary event. The et al., 2002, 2004) and exploration well cores Bay of Biscay beginning of OAE2 is marked by an increase in in northwestern Africa (Sinninghe Damsté and 44°N SPAIN the stable carbon isotopic ratio of marine sedi- Köster, 1998; Kuypers et al., 2002; Kolonic ment, in both carbonate and (e.g., et al., 2005). Given that Gijon`

Santander 2° Arthur et al., 1988; Kuypers et al., 1999, 2002; require both light and hydrogen sulfi de (H2S) Oviedo Scopelliti et al., 2008). for inorganic carbon fi xation, and are therefore Arobes Bilbao OAE2 induced major changes in the marine indicators of photic-zone euxinia, these studies Vitoria Leon` Pamplona biota, as indicated by an estimated global concluded that photic-zone euxinia developed Logroño extinction rate across the C-T boundary of 26% in the North Atlantic during the C-T transi- 42° 6° Burgos at the generic level and 33%–53% at the spe- tion. Sediment cores through the C-T interval cies level (Sepkoski, 1989, 1996). A study of in northwestern Africa exhibit a high S/C ratio Figure 1. Location of Arobes section in benthic and planktonic across the (>0.36) and an abundance of organic sulfur com- northern Spain. C-T boundary showed that ~50% of deep-water pounds, refl ecting deposition in anoxic deposi- foraminifera, but <20% of surface-dwelling tional environments (Nzoussi-Mbassani et al., 1GSA Data Repository item 2011169, analytical foraminifera, became extinct (Kaiho, 1994). 2005). C-T boundary event black shale is also methods and stratigraphic distribution of benthic and planktonic foraminifers, is available online at www The morphology of the benthic fora- present in South Atlantic and Tethyan settings .geosociety.org/pubs/ft2011.htm, or on request from and has been studied using organic geochemical [email protected] or Documents Secretary, *E-mail: [email protected]. methods (Forster et al., 2008; Sepúlveda et al., GSA, P.O. Box 9140, Boulder, CO 80301, USA.

© 2011 Geological Society of America. For permission to copy, contact Copyright Permissions, GSA, or [email protected]. GEOLOGY,Geology, June June 2011; 2011 v. 39; no. 6; p. 519–522; doi:10.1130/G31805.1; 2 fi gures; Data Repository item 2011169. 519 Downloaded from geology.gsapubs.org on July 21, 2015

Rosalina, Gyroidinoides, Gavelinella, and gradual return to preexcursion values. It is com- to bottom-water anoxia. This interval can be Bolivina) in the Ganuza section, which accu- monly accepted that the positive δ13C excursion presumed to have undergone the most anoxic mulated in a middle to outer shelf environment (phases A and B) refl ects a prominent change conditions of OAE2. (Colin et al., 1982; Lamolda and Peryt, 1995). in the global atmospheric-oceanic pool of inor- The total organic carbon (TOC) content of Together with the abundance of , ganic carbon resulting from a global increase in the sediment ranges between 0.11% and 0.53% the foraminiferal assemblage indicates that the the burial rate of 13C-depleted organic carbon (Fig. DR1; see the Data Repository). The TOC Arobes C-T section was deposited on a middle- (Arthur et al., 1988). According to Kuypers et content of mudstone is higher than that of lime- neritic shelf in the eastern North Atlantic Ocean. al. (2002), OAE2 is the main phase of enhanced stone. The vertical profi le of TOC content indi- carbon burial and should be coeval with phases cates that TOC in beds 1, 2, and 16 is relatively Stable Carbon Isotope and Total Organic A and B of the carbon isotope excursion (a span high (>0.4%). No difference is evident between Carbon Content of ~0.7 m.y., as estimated by the occurrence of the TOC contents of phases A, B, and C. The δ13C values of bulk carbonates show planktonic foraminifers and calcareous nanno- a pronounced positive excursion between the ; Fig. 2). Organic Molecules base and top of the measured section at Arobes The depth profi le of δ13C values of brachio- Dibenzothiophene (DBT) and alkyl DBTs

(Fig. 2A). This excursion has been suggested pod shells from the Arobes section is similar (C1- and C2-) and 2,3,6-trimethylarylisopren- to be global and divisible into three principal to that of carbonates (Fig. 2A); the detailed oids, ranging from C14 to C21 with the excep- δ13 phases (Kuypers et al., 2002): phase A, a rapid C profi le of the interval between tion of C17, are present in all sediment samples increase in δ13C values in the uppermost Rot- beds 15A and 19 (top) cannot be determined due from the Arobes section (Figs. 2B and 2C; alipora cushmani ; phase B, a plateau to the absence of brachiopods. The absence of Fig. DR2). The vertical profi les of DBTs and of maximum δ13C values in the lower Whit- brachiopods during this interval suggests that the arylisoprenoids are shown in Figures 2B einella archaeocretacea biozone; and phase C, a they were unable to survive in this area owing and 2C, respectively. The vertical trend of

A BC D Figure 2. Schematic stratigraphic column for δ13C carbonate ( ) Total C0-C2 Total 2,3,6-trimethyl- Cenomanian-Turonian in- δ13 C brachiopoda ( ) dibenzothiophenes arylisoprenoids terval of Arobes section. (‰ versus PDB) ( : μg/g TOC) ( : μg/g TOC) A: Profi le of δ13C values Age Biozone Lithology Bed number Samples for foraminifera Thickness (m) 3 4 56 0.1 1.0 10 0.01 0.1 1.0 (versus Peedee belem- 34 spp. Whiteinella spp. Dicarinella spp. Rotalipora nite standard, PDB) for carbonate sediment and 15 33 brachiopod shells. B: Concentration of C – 32 0 C2 dibenzothiophenes 31 (logarithmic scale). 30 TOC—total organic car- 29 Phase C bon; sed.—sediment. C: Concentration of total Early Turonian 28 10 FO of Q. gartneri 2,3,6-trimethylaryliso- 27 (93.2 Ma) prenoids (logarithmic

26 Recovery of planktonic foraminifera scale). D: Occurrence of 25 planktonic foraminifers 24 23 (dashed lines indicate 22 beds with no planktonic 21 20 foraminifer). Gray zone Top indicates proposed 5 19 stratigraphic range of Base oceanic anoxic event 2 (OAE2) based on δ13C ex- 18 cursion (Kuypers et al., Phase B 2002). Solid horizontal 17 lines show last occur- rence (LO) of Rotalipora

16 Barren of brachiopods greenhornensis and R. R. cushmani Temporary disappearance of Temporary >125 μ m planktonic foraminifera 0 C cushmani (spp.—spe- 15B LO of A R. cushmani cies). Numerical ages of 14B (93.90 Ma) LO of R. greenhornen- A sis, LO of R. cushmani, Late Cenomanian C 13B and fi rst occurrence A 12 (FO) of Quadrum gart- 10 neri are from Keller and 8 Pardo (2004), Hardenbol 6 -5 Phase A et al. (1998), and Erba et 4 al. (1995), respectively. C 3B Overall analytical repro-

A R. greenhornensis

Rotalipora cushmani Whiteinella archaeocretacea 13 2 Beds 3B, 4, 8, 12 and 15 No planktonic foraminifera ducibility of δ C in this 1' 1 LO of R. study is estimated to be Pre- α OAE greenhornensis (93.95 Ma) 0.1 1.0 10 0.01 0.1 1.0 0.05‰ or better. Overall Limestone Marl ( : ng/g sed.) ( : ng/g sed.) uncertainties of δ13C are Nodular mudstone Mudstone within 0.2‰.

520 GEOLOGY, June 2011 Downloaded from geology.gsapubs.org on July 21, 2015 concentrations normalized by TOC is similar to be measured; thus the formation of arylisopren- ) that amplify in concentrations normalized by sediment weight. oids from other precursors (e.g., β-carotene) shelf environments (Schlanger and Jenkyns,

Elevated DBT concentrations are present in cannot be excluded (Koopmans et al., 1996). 1976; Schlanger et al., 1987) transfer H2S to the

OAE2, particularly between beds 17 (top) and However, the vertical profi le of total aryliso- sea surface, where it is oxidized. H2S cannot be 21 (an interval of ~0.4 m.y., assuming a constant prenoids is similar to that of DBTs (Figs. 2B retained in an oxic water column; its preserva- sedimentation rate). In addition, two short-term and 2C). Given that sediment in the Arobes sec- tion requires stagnation of oceanic circulation. increases in concentrations of these compounds, tion was deposited in middle-neritic conditions Therefore, the main cause of oxygen depletion each ~103 to 104 yr long, are just above each last (50–100 m water depth), the seafl oor was prob- is thought to be a decrease in oceanic circula- occurrence (LO) of R. greenhornensis and R. ably in the photic zone. This suggests that the tion. Reduced circulation may be caused by cushmani (Fig. 2D). The vertical profi le of the formation of DBTs and development of a green extraordinarily warm climates. During the C-T total concentration of arylisoprenoids roughly sulfur bacteria biomass were simultaneous. The transition, the North Atlantic was a semiclosed resembles that of DBTs (Figs. 2B and 2C). similarity of the vertical profi les supports the ocean basin, which would have promoted ocean DBTs are known to be present in various hypothesis that most of the arylisoprenoids in water stagnation. types of sediment and (e.g., Hughes the Arobes section were derived from green sul- The concentrations of dibenzothiophenes and et al., 1995). Organic sulfur–containing com- fur bacteria. Kuypers et al. (2002) documented arylisoprenoids in bed 16 are as low as those pounds such as DBTs are most commonly carotenoid isorenieratane in C-T sediment from from pre-OAE sediment, except for bed 16 formed by the reaction of reduced inorganic Shell exploration well S13 in the Tarfaya area, (10–15 cm), which records a brief OAE and the sulfur species with functionalized organic mol- Morocco. Their data showed that the concentra- extinction of R. cushmani. Reconstructed SSTs ecules during sediment deposition and early dia- tion of isorenieratane increased gradually over for the equatorial Atlantic during the C-T transi- genesis (Hughes, 1984; Sinninghe Damsté and time during OAE2, and resembled the depth tion using the TEX86 paleothermometry de Leeuw, 1990). The presence of DBTs prob- profi le of total arylisoprenoids from the Arobes (Forster et al., 2007) show marked cooling to ably refl ects the concentration of H2S at the sed- section. This similarity also supports derivation temperatures lower than pre-OAE2 conditions iment surface (Hughes et al., 1995), implying of the arylisoprenoids in the Arobes section in the early stages of OAE2 (phase A-B tran- the presence of sulfur-rich anoxic (i.e., euxinic) from green sulfur bacteria. sition). This interval corresponds to bed 16 of bottom waters. Increased DBT concentration Like the DBTs, the short-term relative the Arobes section, although there is a need to during OAE2 indicates that euxinic conditions abundances of 2,3,6-trimethylarylisoprenoids estimate the detailed SSTs of Arobes section by expanded. The two short-term increases in the increase just above the LO of R. greenhornensis TEX86. This cooling event may have driven the concentrations of DBTs, just after the LOs of and R. cushmani (Figs. 2C and 2D), indicating revival of oceanic circulation and reoxygenation both R. greenhornensis and R. cushmani (the the development of photic-zone euxinia. Analy- of the water column. upper bed or layer over the LO is the bed in sis of planktonic foraminiferal assemblages which extinction occurred), refl ect ephemeral from the Arobes section reveals that surface CONCLUSIONS but strongly euxinic depositional environments. dwellers (whiteinellids) and intermediate dwell- An organic geochemical study of the C-T These rotaliporids were deep-water species ers (dicarinellids and praeglobotruncanids) interval at Arobes, Spain, highlights variations that lived at or below the thermocline for most are temporarily absent in beds 3B and 4 and in water-column euxinia and relations between of their cycles (Norris and Wilson, 1998; between beds 16 and 20 (Fig. 2D). The relative oceanic euxinic events and planktonic foramini- Keller et al., 2001). Their extinction may have abundances of arylisoprenoids in beds 3B and fers. Extinctions of R. greenhornensis and R. been caused by the short-term euxinic events 16 (10–15 cm) are in good agreement with the cushmani resulted from short-term ocean eux- that occurred during deposition of bed 3B and temporary disappearance of planktonic fora- inic events that preceded the most stable and just above the base of bed 16 (10–15 cm). The minifers and strongly support the development persistent anoxic conditions of OAE2. This sug- relatively elevated concentrations of DBTs from of euxinic conditions in surface water, a condi- gests that variations during OAE2 bed 17 (top) to bed 21 suggest that the benthic tion that would not have supported planktonic were complex and may merit further study. euxinic conditions of this interval were the foraminifera. most stable and persistent of OAE2, consistent The gradual increase in arylisoprenoid con- ACKNOWLEDGMENTS with the temporary absence of all brachiopods centrations during deposition of beds 17 and 19 We thank R. Coccioni (Università di Urbino, Italy), P. A. Meyers (University of Michigan, USA), A. (Fig. 2A). (top) probably indicates that sulfi de-contain- Bechtel (University of Leoben, Austria), and anony- The arylisoprenoids identifi ed are thought ing water frequently entered the photic zone. mous reviewers for constructive review comments to have been derived from carotenoids that are Between beds 20 and 25, however, the concen- that helped us improve the earlier version of the man- specifi c to photosynthetic green sulfur bacteria tration of arylisoprenoids decreases sharply. The uscript. This work was supported by a Global Cen- (Chlorobiaceae; Summons and Powell, 1987). planktonic foraminiferal assemblages in bed 21 ter of Excellence Program on Global Education and Research Center for Earth and Planetary Dynamics at These organisms are phototrophic anaerobes closely mirror those in bed 16 (base), except Tohoku University (Leader E. Ohtani) fi nanced by the that require both light and H2S. In modern envi- for the absence of rotaliporids, suggesting a Ministry of Education, Culture, Sports, Science, and ronments, they appear in -containing weakening of anoxic and/or euxinic conditions Technology of Japan. water bodies that are quiescent and organic-rich in surface water. The dominant planktonic fora- enough to allow sulfi de production close to the minifers in bed 21 are opportunistic hedbergel- REFERENCES CITED photic zone (Summons, 1993). 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Geology

Short-term euxinia coinciding with rotaliporid extinctions during the Cenomanian-Turonian transition in the middle-neritic eastern North Atlantic inferred from organic compounds

Masahiro Oba, Kunio Kaiho, Takashi Okabe, Marcos A. Lamolda and James D. Wright

Geology 2011;39;519-522 doi: 10.1130/G31805.1

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