Elsevier

Marine Micropaleontology

Volume 161, December 2020, 101924
Marine Micropaleontology

Research paper
What drove the evolutionary trend of planktic foraminifers during the Cretaceous: Oceanic Anoxic Events (OAEs) directly affected it?

https://doi.org/10.1016/j.marmicro.2020.101924Get rights and content

Highlights

  • Evolutionary trends of planktic foraminifers around global OAEs were examined.

  • Anoxic condition did not directly affect the species number and turnover ratio.

  • Turnover peaks were largely associated with a short-term eustatic curve.

Abstract

The oceanic redox state has played an essential role in the evolution of life on earth, and oceanic “anoxic events” have been proposed as one of the causal mechanisms for mass extinctions. During the mid-Cretaceous, oceanic anoxic events (OAEs) occurred several times and had a substantial impact on the biosphere. Planktic foraminifers are marine planktons with calcite tests, and their shells constitute approximately 30%–80% of modern deep-marine calcite; thus, they play a key role in the global carbon cycle. Previous studies have reported that at, or near, the times of major Cretaceous OAEs, planktic foraminifers have a high turnover (extinction and speciation) rate. However, the precise impact of anoxic conditions on the evolutionary trend of planktic foraminifers remained obscure. In this study, we investigate this by assessing the extinction/speciation rate of planktic foraminifers around OAEs. Our results suggest that the development of anoxia during OAEs would not have had a direct effect on the evolutionary trend (i.e., species number and turnover ratio). Two foraminiferal turnovers occurred around OAE1a and OAE2, however, all five turnover peaks seem to be largely associated with a relatively short-term (0.5–3 Myr) eustatic curve. Decreasing species numbers of planktic foraminifers are associated with a relatively lower sea eustatic level (second-order; ~20 Myr) and a small latitudinal temperature gradient around OAE1b, which are not anoxic conditions. Changes in oceanographical parameters (i.e., surface biological productivity, water column structure, carbonate chemistry, and nutrients) related to lowering sea-levels might have had a significant effect on foraminiferal evolutionary trends.

Introduction

The redox state is a fundamental concept in the marine biosphere. Raup and Sepkoski (1982) reported five mass marine animal extinctions: during the Ordovician (−12% diversity), the Devonian (−14%), the Permian (−52%), the Triassic (−12%), and the Cretaceous (−11%) periods. Several hypotheses have been proposed as the causal mechanisms for the mass extinctions, including: 1) asteroid impacts; 2) rapid sea-level fluctuations; 3) changes in climate and sea water composition leading to 3a) glaciations, 3b) salinity changes, or 3c) anoxic events; 4) volcanic catastrophes; and 5) increased cosmic radiation (Büggisch, 1991). For example, in the Frasnian–Famennian Kellwasser event/s of the Devonian period, extinction rates are clearly related to periods of anoxia (Büggisch, 1991). The mass extinction event at Permian/Triassic boundary—the largest extinction of marine fauna in the Phanerozoic (the number of families dropped to 52% (Raup and Sepkoski, 1982))—also coincided with a global oceanic anoxia (Newton et al., 2004; Cao et al., 2009). A mass extinction, however, means the beginning of an epoch for a new biocenosis. Thus, the oceanic oxygen concentration plays an important role in the evolutionary history of life on earth, as demonstrated by anoxic extinction events.

During the mid-Cretaceous period, widely known to be extremely warm (e.g., Forster et al., 2007), oceanic anoxic events (OAEs) occurred several times. Numerous studies have identified several OAEs during that time (e.g., Jenkyns, 2010). They are recognized in the geological record as a broad and synchronous deposition of organic, carbon-rich marine sediments, representing a distinct period of widespread ocean anoxia (Schlanger and Jenkyns, 1976). In general, both OAE1a (the Selli event, ~125–124 Ma) and OAE2 (the Bonarelli event, C/T OAE, ~94 Ma) are regarded as the major OAEs, while others (e.g., the Weissert Event, the Faraoni Event, OAE1b (the Paquier event, ~111 Ma), OAE1c, OAE1d, and OAE3) are relatively regional events in the Cretaceous period (e.g., Jenkyns, 2010). Therefore, we mainly focused on the major OAE1a and OAE2 for this study.

Planktic foraminifers are marine plankton with calcite tests, and their shells have been preserved in the ocean sediments since the Jurassic. In the modern ocean, they are generally omnivorous, upper ocean dwellers (e.g., Schiebel and Hemleben, 2017), and their reproduction cycle is mostly characterized by a semi-lunar/lunar periodicity (Bijma et al., 1990; Kawahata et al., 2002; Jonkers et al., 2015). Their calcium carbonate (CaCO3) shell productions contribute 0.36–0.88 Gt yr−1 to global surface sediments and constitute ~32%–80% of modern deep-marine calcite (Schiebel, 2002). Thus, they perform key functions in the global carbon cycle. As mentioned above, anoxic events generally seem to be associated with drastic mass extinctions. Premoli Silva and Sliter (1999) suggested that evolutionary changes in Cretaceous planktic foraminifers would be consistent with five paleoceanographic events, and two of these are the Selli (OAE1a) and Bonarelli (OAE2) events. Leckie et al. (2002) also reported that planktic foraminifers displayed a high turnover (extinction and speciation) rate at, or near, the major OAEs. They suggested that changes in oceanographic conditions might lead to a high turnover rate. However, a detailed mechanism of the high turnover ratio remained obscure. In this study, we investigated the causal linkage between anoxic conditions and the evolutionary trend of planktic foraminifers by assessing the turnover (extinction/speciation) rate using a latest timescale and biozone (GTS2016), and oceanographic situation, around Cretaceous OAEs.

Section snippets

Materials and methods

We integrated data on the extinction/speciation rate of planktic foraminifers around Cretaceous OAEs with 1-Myr resolution. Leckie et al. (2002) compiled a biostratigraphic range of planktic foraminifers from the late Barremian to the late Turonian. They also calculated the rate of turnover (extinction plus speciation) based on their compiled evolutionary data. In our study, we re-organized their original data set within a latest geological timescale and biozone (GTS2016; Ogg et al., 2016;

Results

The total number of foraminiferal species generally showed more than 15, with a large minimum around 111 Ma throughout 128–90 Ma (Fig. 1, Fig. 2). The number of foraminiferal species increased from the Barremian to the early Aptian, when it showed a peak (124 Ma; n = 26), then decreased gradually to the early Albian (111 Ma; n = 8). After that, it increased again from the early to late Albian with no extinction (111–105 Ma), then the total number of species remained relatively stable (~20

Did the number of planktic foraminiferal species decline during OAEs?

Foraminiferal evolutionary data suggest that the development of oceanic anoxia at OAEs did not have a direct effect on the total number of foraminiferal species (Fig. 2). At OAE1a, one of the two major OAEs, our results show that the number of species increased across the event and then peaked after it (124 Ma). Furthermore, around OAE2, it remained relatively high (>25 species) despite the higher extinction/speciation rate (~20%) (Fig. 2). Thus, the anoxic condition of OAEs might not be

Conclusion

We examined the relationship between global oceanic anoxic events and the evolutionary trend of planktic foraminifers by assessing the turnover (extinction/speciation) rate of planktic foraminifers during the Cretaceous, with a particular focus on two major OAEs (OAE1a and OAE2). Our findings in summary were:

1. Foraminiferal evolutionary data suggested that the anoxic condition of OAEs had not directly affected the total number of planktic foraminiferal species; instead, decreasing species

Author statement

All authors have contributed to data curation and interpretation, and critically reviewed the manuscript.

Declaration of Competing Interest

The authors declare no conflicts of interest associated with this article.

Acknowledgments

The manuscript has been improved with the help of constructive comments by K. Husum and an anonymous reviewer. We gratefully acknowledge the assistance of J. Arimoto, E. Sakaki, and the staff of Tohoku University and Atmosphere and Ocean Research Institute (AORI) for their helpful suggestions and support. This study was carried out with the support of Japan Society for the Promotion of Science (JSPS) KAKENHI Grant (JP19K04053) and TUMUGU Fund (Tohoku University) to A. Kuroyanagi and JSPS

References (42)

  • K. Ozaki et al.

    Biogeochemical effects of atmospheric oxygen concentration, phosphorus weathering, and sea-level stand on oceanic redox chemistry: Implications for greenhouse climates

    Earth Planet. Sci. Lett.

    (2013)
  • D.C. Ray et al.

    The magnitude and cause of short-term eustatic Cretaceous sea-level change: A synthesis

    Earth Sci. Rev.

    (2019)
  • J.S. Sinninghe Damsté et al.

    A euxinic southern North Atlantic Ocean during the Cenomanian/Turonian oceanic anoxic event

    Earth Planet. Sci. Lett.

    (1998)
  • A. Ando et al.

    Onset of seawater 87Sr/86Sr excursion prior to Cenomanian-Turonian oceanic anoxic event 2? New late Cretaceous strontium isotope curve from the central Pacific Ocean

    J. Foraminiferal Res.

    (2009)
  • J. Bijma et al.

    Lunar and semi-lunar reproductive cycles in some spinose planktonic foraminifers

    J. Foraminiferal Res.

    (1990)
  • W. Büggisch

    The global Frasnian-Famennian ‘Kellwasser event

    Geol. Rundsch.

    (1991)
  • R. Coccioni et al.

    Planktonic foraminifera and environmental changes across the Bonarelli Event (OAE2, latest Cenomanian) in its type area: A high resolution study from the Tethyan reference Bottaccione section (Gubbio, Central Italy)

    J. Foraminifer. Res.

    (2004)
  • A. Forster et al.

    Tropical warming and intermittent cooling during the Cenomanian/Turonian oceanic anoxic event 2: sea surface temperature records from the equatorial Atlantic

    Paleoceanography

    (2007)
  • A.J. Fraass et al.

    Macroevolutionary history of the planktic foraminifera

    Annu. Rev. Earth Planet. Sci.

    (2015)
  • B.T. Huber et al.

    Planktic foraminiferal species turn- over across deep-sea Aptian/Albian boundary sections

    J. Foraminiferal Res.

    (2011)
  • B.T. Huber et al.

    Errata: Planktic foraminiferal species turnover across deep-sea Aptian/Albian boundary sections

    J. Foraminiferal Res.

    (2011)
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