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