Fossil Benthic Foraminifera Morphologic Adaptation (Kleptoplastidy) Within Low-Oxygen-Bottom Water Environments, Coupled with Geochemical Insights from the Late Cretaceous in the Levant Basin

Following a multi-proxy analysis of the Upper Cretaceous high-productivity sequence from proximal and distal basins in Israel, Meilijson et al. (Paleobiology 42:77-97, 2016) provided evidence indicating that different benthic foraminifera species could survive and sustain large populations under long-term anoxic to dysoxic bottom water conditions. They proposed that massive blooms of triserial (buliminid) benthic foraminifera with distinct apertural and test morphologies during the Campanian managed to survive anoxic conditions by their capability to sequester diatom chloroplasts (kleptoplastidy) and associate with bacteria, in a similar manner as their modern analogues. This advantageous capability as well as other adaptations such as using nitrate instead of oxygen for their respiratory pathways, or changes in food type arriving to the seafloor, were all affected by the substantial shift in the depositional environment following the Campanian/Maastrichtian boundary. However, several of the hypothesis and assumptions presented in this chapter called for a continued study of the Upper Cretaceous deposits in the Levant, to better constrain the oceanographic and bottom water process in which these organisms lived. Here we report on a high-resolution investigation focused on the inorganic geochemical properties of two sections within the high-productivity setting of the Late Cretaceous in the Levant. Benthic foraminiferal assemblages were compared with the trace metal enrichment, bottom water renewal and water column oxygen levels, on a high-productivity seafloor. Our work focused on the occurrence and distribution of redox-sensitive/sulphide-forming trace metals obtained by analytical approaches (bulk sediment composition, ED-and WD-XRF), in the organic-rich sediments. On basis of the bulk sediment geochemistry, a principal component analysis distinguished between two factors for both sections: Factor 1 mirrors the degree of bottom-water oxygenation (Cu, S, Ni, Zn, Cr and Corg) and includes elements representing enhanced phosphorite deposition (P2O5, U, As, Mo, Y). Factor 2 reflects the interplay between the input of biogenic carbonate (Ca) and terrigenous material (TiO2, Rb, SiO2, Fe2O3(t), Ce, Ga, V and Al2O3). An additional factor was used in the distal and deeper of the two sections to distinguish between times in which dominance of siliceous or calcareous biogenic sedimentation occurred. We observe that the lowest part of the Maastrichtian contained the strongest reducing conditions, whereas the upper part was affected by a lesser degree of oxygen deficiency. Geochemical results of the molybdenum-to-organic carbon ratio reveal a change in the water mass circulation to more restrictive condition within the lower Maastrichtian, which coincides with reported sea-level rise. Based on factor analysis of the elemental distribution we demonstrate a clear connection between diatom abundance and peaks in the abundance of foraminifera species thought to have used kleptoplastidy as a morphological adaptation to cope with environmental instability, advocating previous assumptions and hypothesis. Additionally, it is evident that along the section in which fluctuations in the relative abundance of primary producers occurred, substantial shifts also transpired in the relative contribution of terrigenic material to the accumulating sediments. The synchronous occurrence of abnormally high numbers of low-diversity benthic foraminifera demonstrates the existence and success of functional adaptations. Our identification of morphological adaptations in Praebulimina prolixa, which are identical to those recognized in modern diatom-based kleptoplastidy of benthic foraminifera, acts as the missing link for understanding this complex system. It does so by tying between productivity, oceanography, continental-marine interactions and remarkable biochemical reciprocity and adaptiveness of present and deep-time ecosystems.