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Cenozoic Deep-sea Benthic Foraminifera: A Tale of Three Turnovers
... Our knowledge about the colonization of the deep sea by demersal fishes during the Palaeogene and their evolution is still relatively scarce. Much better known is the history of bathybenthic foraminifera (Miller et al. 1992;Thomas 2007), and their fate could serve as a blueprint of what to expect in bathydemersal fish evolution. According to Miller et al. (1992), bathybenthic foraminifera survived the K/Pg boundary relatively unscathed in the Paleocene but became the subject of a deep-sea extinction event at the Paleocene-Eocene thermal maximum (PETM), which was presumably caused by the intrusion of warm, low-oxygenated and nutrient-poor water into the deep sea (Thomas 2007). ...
... Much better known is the history of bathybenthic foraminifera (Miller et al. 1992;Thomas 2007), and their fate could serve as a blueprint of what to expect in bathydemersal fish evolution. According to Miller et al. (1992), bathybenthic foraminifera survived the K/Pg boundary relatively unscathed in the Paleocene but became the subject of a deep-sea extinction event at the Paleocene-Eocene thermal maximum (PETM), which was presumably caused by the intrusion of warm, low-oxygenated and nutrient-poor water into the deep sea (Thomas 2007). Repopulation of the deep sea started again in the early Eocene at an initially slow pace (Miller et al. 1992). ...
... According to Miller et al. (1992), bathybenthic foraminifera survived the K/Pg boundary relatively unscathed in the Paleocene but became the subject of a deep-sea extinction event at the Paleocene-Eocene thermal maximum (PETM), which was presumably caused by the intrusion of warm, low-oxygenated and nutrient-poor water into the deep sea (Thomas 2007). Repopulation of the deep sea started again in the early Eocene at an initially slow pace (Miller et al. 1992). A gradual deep benthic foraminiferal turn-over occurred during the late Eocene and early Oligocene well-documented cooling (Miller et al. 1992;Thomas 2007), set off by the gradual change in the oceanic circulation from a halothermal to a termohaline regime, increasingly triggering the intrusion of cool, welloxygenated and nutrient-rich waters into the deep sea. ...
Few deepwater otolith associations from the Eocene have been found so far. The small assemblage of aragonitic-preserved otoliths from the Lillebælt Clay Formation described here therefore adds to the understanding of early Palaeogene deep-sea fish faunas. These otoliths were obtained from a level at about the Ypresian/Lutetian interface and may thus be older than the otoliths previously described from Trelde Næs from mold casts from carbonate concretions. Only 14 otoliths were recovered from about 6,000 kg processed bulk samples. The assemblage also differs in the composition and contains three new species and one new genus: Diaphus? duplex n. sp., Bregmaceros danicus n. sp. and the ophidiid Pronobythites schnetleri n. gen, n. sp. In addition, the new genus Treldeichthys n. gen. in Acanthomorpha incertae sedis is established for T. madseni (Schwarzhans, 2007). The small assemblage also differs in composition from comparable associations described from southwest France and northern Italy on the species level but shows some relationship on a higher systematic level. The mechanism and timing of the colonization of the deep sea by selected groups of fishes is discussed, particularly in respect to the depth migration of demersal fishes.
... Most compilations of deep-sea benthic foraminiferal data have focused on individual, relatively short events across the Paleogene. Integrated studies on the long-term evolution of benthic foraminifera are scarce, and generally use few sites (Miller et al., 1992;Thomas, 1992Thomas, , 2007Thomas and Gooday, 1996), or limited sets of taxa (Hayward et al., 2012), mainly due to taxonomic problems (Arreguín-Rodríguez et al., 2018). Because of the taxonomic problems, the longer-term discussions tend to include taxonomy by few (Thomas and Gooday, 1996) or one author (Kaiho, 1994;Thomas, 2007). ...
... Among epifaunal morphogroups, many species that were abundant during the Paleocene went extinct at the Paleocene/Eocene boundary (e.g., Stensioeina beccariiformis, Cibicidoides hyphalus, Nuttallinella florealis) or decreased in abundance towards the Eocene (Paralabamina hillebrandti, Paralabamina lunata, Gyroidinoides beisseli). Nuttallides truempyi was most common during the Paleocene and early to middle Eocene, gradually decreasing in abundance until its extinction at or close to the Eocene/Oligocene boundary (e.g., Thomas, 1985;Miller et al., 1992). ...
... These low-diversity assemblages commonly after later hyperthermals were dominated by the same taxa as were dominant directly after the PETM, but the temporary effects on the assemblages during these events cannot be resolved within the time resolution of this compilation (see ‗material and methods', and Table S3). The proliferation of the oligotrophic species Nuttallides truempyi (Miller et al., 1992;Thomas, 1998) during the early-middle Eocene in all oceans except the Southern Ocean contributed to the low diversity values (Fig. 8), and points to a higher food supply to the seafloor in the Southern Ocean as compared to other ocean basins during the early Eocene. This species has been argued to be CaCO 3 corrosion-resistant, similar to its extant descendant Nuttallides umbonifera (Thomas, 1998), but the dominance of calcareous taxa (>90% of the assemblages; Table S2) in all ocean basins except the Bay of Biscay rules out increased CaCO 3 -corrosivity of bottom waters as the main cause of its proliferation. ...
Benthic foraminifera are the most common meiofaunal unicellular deep-sea biota, forming skeletons used as proxies for past climate change. We aim to increase understanding of past non-analog oceans and ecosystems by evaluating deep-sea benthic foraminiferal responses to global environmental changes over latest Cretaceous through Oligocene times (67–23 million years ago). Earth suffered an asteroid impact at the end of the Cretaceous (~instantaneous; 66 Ma), episodes of rapid global warming during the Paleocene-Eocene Thermal Maximum (PETM; ~56 Ma) and other hyperthermals (millennial timescales), followed by gradual, but punctuated cooling (timescales of hundred thousands of years) from a world without polar ice sheets to a world with a large Antarctic ice sheet. Here we present the first compilation of quantitative data on deep-sea foraminifera at sites in all the world's oceans, aiming to build a first unique, uniform database that allows comparison of deep-sea faunal turnover across the uppermost Cretaceous through Paleogene. We document variability in space and time of benthic foraminiferal diversity: lack of extinction at the asteroid impact even though other marine and terrestrial groups suffered mass extinction; major extinction at the PETM followed by recovery and diversification; and gradual but fundamental turnover during gradual cooling and increase in polar ice volume (possibly linked to changes in the oceanic carbon cycle). High latitude cooling from ~45 Ma on, i.e., after the end of the Early Eocene Climate Optimum (53.2–49.2 Ma), may have made the middle Eocene a critical period of several millions of years of faunal turnover and establishment of latitudinal diversity gradients. This compilation thus illuminates the penetration of global change at very different rates into the largest and one of the most stable habitats on Earth, the deep sea with its highly diverse biota.
... However, the taxonomy of benthic foraminifera is problematic, since splitting of species is common, providing different names for morphologically indistinguishable species, especially for different geographic regions and for different age intervals. Compilations of Early Cretaceous-middle Miocene [7], Late Cretaceous-Cenozoic [7,8], Cenozoic [9], Late Cretaceous-Paleocene (K-Pg; [10]), and Paleocene-Eocene [11] faunas have been published, and benthic foraminiferal deep-sea biozones have been proposed for the Cenozoic [12][13][14][15][16]. In order to standardise descriptions of benthic foraminifera, Holbourn et al. [17] created a database of 300 deep-water species, including mostly taxa with stratigraphic and paleoecological significance, or those used in geochemical analyses. ...
... The Paleocene-Eocene boundary (56 Ma; [25]) was a critical threshold for deep-sea benthic foraminifera, since this group suffered their largest extinction of the Late Cretaceous-Cenozoic [11,13,15,[26][27][28][29][30]. The extinction resulted in reorganisation of the assemblages, including the last appearance of about a quarter to half of the species, the first appearance of some species (e.g., Anomalinoides capitatus and Hanzawaia ammophila; [12]), and migration of species from shallower waters into the deep sea (e.g., [11,28]). ...
... The test of C. eocaenus is small, nearly circular and unequally biconvex (may vary from planoconvex to biconvex), its umbilical side is somewhat cone-shaped, and the spiral side is somewhat less convex. The chambers (12)(13)(14)(15) are inflated, separated by curved and limbate sutures. Additionally, C. eocaenus has a distinct spiral suture line and frequently a prominent umbilical umbo [9]. ...
The early Eocene greenhouse world was marked by multiple transient hyperthermal events. The most extreme was the Paleocene-Eocene Thermal Maximum (PETM, ~56 Ma), linked to the extinction of the globally recognised deep-sea benthic foraminiferal Velasco fauna, which led to the development of early Eocene assemblages. This turnover has been studied at high resolution, but faunal development into the later early Eocene is poorly documented. There is no widely accepted early Eocene equivalent of the Late Cretaceous-Paleocene Velasco fauna, mainly due to the use of different taxonomic concepts. We compiled Ypresian benthic foraminiferal data from 17 middle bathyal-lower abyssal ocean drilling sites in the Pacific, Atlantic and Indian Oceans, in order to characterise early Eocene deep-sea faunas by comparing assemblages across space, paleodepth and time. Nuttallides truempyi, Oridorsalis umbonatus, Bulimina trinitatensis, the Bulimina simplex group, the Anomalinoides spissiformis group, pleurostomellids, uniserial lagenids, stilostomellids and lenticulinids were ubiquitous during the early Eocene (lower-middle Ypresian). Aragonia aragonensis, the Globocassidulina subglobosa group, the Cibicidoides eocaenus group and polymorphinids became ubiquitous during the middle Ypresian. The most abundant early Ypresian taxa were tolerant to stressed or disturbed environments, either by opportunistic behavior (Quadrimorphina profunda, Tappanina selmensis, Siphogenerinoides brevispinosa) and/or the ability to calcify in carbonate-corrosive waters (N. truempyi). Nuttallides truempyi, T. selmensis and other buliminids (Bolivinoides cf. decoratus group, Bulimina virginiana) were markedly abundant during the middle Ypresian. Contrary to the long-lived, highly diverse and equitable Velasco fauna, common and abundant taxa reflect highly perturbed assemblages through the earliest Ypresian, with lower diversity and equitability following the PETM extinction. In contrast, the middle Ypresian assemblages may indicate a recovering fauna, though to some extent persistently disturbed by the lower-amplitude Eocene hyperthermals (e.g., Eocene Thermal Maximum 2 and 3). We propose the name ‘Walvis Ridge fauna’ for future reference to these Ypresian deep-sea benthic foraminiferal assemblages.
... Between 36 and 33 Ma, a combination of geodynamic and paleoceanographic events led to a general restructuring of the global ocean system, including the isolation of Antarctica and formation of the (initial) Antarctic Circumpolar Current (Kennett 1977;Kennett and Exon 2004;Scher and Martin 2006;Barker et al. 2007;Strugnell et al. 2008;Katz et al. 2011;Houben et al. 2013), formation of the North Atlantic Deep Water Current induced by an increase in seawater density caused by polar cooling and following the submersion of the Arctic Ocean to North Atlantic swell for deep-water flow (Berger 2007; Katz et al. 2011;Borrelli et al. 2014;Coxall et al. 2018), demise of the Tethyan deep-water connection (Jovane et al. 2009;Steeman et al. 2009;Zhang et al. 2011), and denudation of adjacent uplifted terrains (Cermeño et al. 2015). The cooling and oxygenation of the deep oceanic masses induced migration of new taxa into the deep sea (Miller et al. 1992;Thomas 2007). Among fishes, these oceanographic changes resulted in an accelerated migration of benthopelagic fishes, for example, of the Macrouridae and Neobythitinae (Ophidiidae) (Nolf and Steurbaut 1988, 1990, 2004Lin et al. 2016;Schwarzhans 2019), into the deep sea. ...
Lanternfishes currently represent one of the dominant groups of mesopelagic fishes in terms of abundance, biomass, and diversity. Their otolith record dominates pelagic sediments below 200 m in dredges, especially during the entire Neogene. Here we provide an analysis of their diversity and rise to dominance primarily based on their otolith record. The earliest unambiguous fossil myctophids are known based on otoliths from the late Paleocene and early Eocene. During their early evolutionary history, myctophids were likely not adapted to a high oceanic lifestyle but occurred over shelf and upper-slope regions, where they were locally abundant during the middle Eocene. A distinct upscaling in otolith size is observed in the early Oligocene, which also marks their earliest occurrence in bathyal sediments. We interpret this transition to be related to the change from a halothermal deep-ocean circulation to a thermohaline regime and the associated cooling of the deep ocean and rearrangement of nutrient and sil-ica supply. The early Oligocene myctophid size acme shows a remarkable congruence with diatom abundance , the main food resource for the zooplankton and thus for myctophids and whales. The warmer late Oligocene to early middle Miocene period was characterized by an increase in disparity of myctophids but with a reduction in their otolith sizes. A second and persisting secular pulse in myctophid diversity (particularly within the genus Diaphus) and increase in size begins with the "biogenic bloom" in the late Miocene, paralleled with diatom abundance and mysticete gigantism.
... Sediment drift accumulation in the North Atlantic and Pacific Oceans [e.g., Wold, 1994;Kerr et al., 2005], the presence of hiatuses in the North Atlantic and Southern Ocean [Miller and Tucholke, 1983;Mountain and Miller, 1992;Miller, 1993, 1996], and Ɛ Nd data from the Southern Ocean and South Atlantic Martin, 2004, 2006] in the late Eocene-early Oligocene indicate changes in deep ocean circulation. Microfossil communities also indicate circulation change and nutrient reorganization beginning in the late-middle Eocene: benthic foraminifera experienced stepwise extinctions and originations of new species in the late Eocene through early Oligocene [e.g., Miller et al., 1992;Thomas, 2007] with an increase in species that thrive in high levels of phytodetritus [Thomas and Gooday, 1996], while calcareous nannoplankton experienced a similar series of extinctions and originations that likely reflect changes in surface ocean nutrient distribution [Aubry and Bord, 2009]. ...
The Antarctic Circumpolar Current (ACC) is a dominant feature of modern
ocean circulation and climate, influencing meridional overturning
circulation, transition depth from surface to deep ocean, gas exchange
rate between atmosphere and deep ocean, and global surface heat
distribution. A proto-ACC began to develop in the late middle Eocene
(~40Ma) with shallow flow through the Drake Passage. Rapid deepening of
the Tasman gateway (late Eocene to early Oligocene), and more gradual
deepening of the Drake Passage through the Oligocene allowed the ACC to
deepen and strengthen. The impact of the ACC on ocean circulation at its
early stages of development has been debated for decades. New benthic
foraminiferal δ18O and δ13C records from Atlantic DSDP/ODP
Sites 366, 1053, and 1090, with comparisons to ASP-5 (Katz et al. 2011)
and isotope compilations (Cramer et al. 2009), show that increased
thermal differentiation of northern- and sourthern-sourced deepwaters
began following the Middle Eocene Climate Optimum (MECO) and increased
through the late Eocene. Published assemblage data from multiple
microfossil groups show that major biotic changes in the surface and
deep ocean began at this time. In the late Eocene, δ13C records
and published opaline silica data indicate enhanced primary productivity
at the northern edge of the polar front, consistent with model
predictions for the effects of proto-ACC development in the late Eocene.
In the early Oligocene, a large δ13C offset developed between
mid-depth (~600m) and deep (>1000m) western North Atlantic waters,
indicating development of intermediate-depth δ13C and O2 minima
linked in the modern ocean to northward incursion of Antarctic
Intermediate Water. At the same time, the ocean's coldest waters became
increasingly restricted to south of the ACC, likely forming a
bottom-ocean layer, as in the modern ocean. This indicates that the
modern four-layer ocean structure (surface, intermediate, deep, bottom)
developed by the early Oligocene as a consequence of the ACC. We
conclude that the (proto-)ACC impacted global ocean circulation by the
beginning of the late Eocene, with increasing influence through the
Oligocene. The timing of the oceanographic changes implies that the
development of the ACC likely influenced the climate transition to
continent-scale Antarctic glaciation.
... occurred from the late-middle Eocene to the early Oligocene (ca. 40-33 Ma), when (1) the small to nonexistent ice sheets of the early Paleogene greenhouse shifted to the continent-scale Antarctic ice sheets in the early Oligocene (e.g., Miller and Fairbanks, 1985;Barron et al., 1991;Ehrmann and Mackensen, 1992;Zachos et al., 1992Zachos et al., , 2001Browning et al., 1996;Kominz and Pekar, 2001;Lear et al., 2004Lear et al., , 2008Coxall et al., 2005;Miller et al., 2005Miller et al., , 2008aKatz et al., 2008;Cramer et al., 2009Cramer et al., , 2011Dawber and Tripati, 2011); and (2) the warm temperatures of the early Paleogene gave way to the cooler temperatures of the late Eocene-early Oligocene, as recorded in several proxies, for example planktonic and benthic foraminiferal d 18 O (e.g., Zachos et al., 1994;Diester-Haass and Zahn, 1996;Miller et al., 2008b;Cramer et al., 2009); planktonic and benthic foraminiferal Mg/Ca (e.g., Lear et al., 2008;Pusz et al., 2011); floral and faunal turnover (e.g., Miller et al., 1992;Thomas, 2007;Wade and Pearson, 2008;Aubry and Bord, 2009); and the organic paleothermometer TEX 86 (e.g., Liu et al., 2009;Wade et al., 2012). ...
... The late-middle Eocene to earliest Oligocene (ca. 38-33 Ma) was a period of transition to large-scale glaciation on Antarctica and cooling of the oceans (e.g., Miller and Fairbanks, 1985;Barron et al., 1991;Ehrmann and Mackensen, 1992;Miller et al., 1992Miller et al., , 2005Miller et al., , 2008aMiller et al., , 2008bMiller et al., , 2009Diester-Haass and Zahn, 1996;Zachos et al., 1996;Lear et al., 2004Lear et al., , 2008Coxall et al., 2005;Katz et al., 2008;Wade and Pearson, 2008;Pusz et al., 2011;Wade et al., 2012;Bijl et al., 2013). The transition from warmer to colder high-latitude ocean temperatures from the early Eocene to the Oligocene (ca. ...
Comparison of new benthic foraminiferal δ¹⁸O and δ¹³C records from Ocean Drilling Program (ODP) Site 1263 (Walvis Ridge, southeast Atlantic, 2100 m paleodepth) and Deep Sea Drilling Project (DSDP) Site 366 (Sierra Leone Rise, eastern equatorial Atlantic, 2200-2800 m paleodepth) with published data from Atlantic and Southern Ocean sites provides the means to reconstruct the development of deep-water circulation in the southeastern Atlantic from the late-middle Eocene to the earliest Oligocene. Our comparison shows that in the late-middle Eocene (ca. 40 Ma), the South Atlantic was characterized by a homogeneous thermal structure. Thermal differentiation began ca. 38 Ma. By 37.6 Ma, Site 1263 was dominated by Southern Component Water; at the same time, warm saline deep water filled the deeper South Atlantic (recorded at southwest Atlantic ODP Site 699, paleodepth 3400 m, and southeast Atlantic ODP Site 1090, paleodepth 3200 m). The deep-water source to eastern equatorial Site 366 transitioned to Northern Component Water ca. 35.6-35 Ma. Progressive cooling at Site 1263 during the middle to late Eocene and deep-water thermal stratification in the South Atlantic may be attributed at least in part to the gradual deepening and strengthening of the proto-Antarctic Circumpolar Current from the late-middle Eocene to the earliest Oligocene, as the Drake and Tasman gateways opened. Our isotopic comparisons across depth and latitude provide evidence of the development of deep-water circulation similar to modern-day Atlantic Meridional Overturning Circulation.
... We argue that N. truempyi may have been an oligotrophic species, as supported by its common occurrence at the deepest sites (Van Morkhoven et al., 1986;Miiller-Merz and Oberhiinsli, 1991;Thomas, 1998). This species shows its highest Cenozoic abundance in the middle Eocene at many locations in various oceans (Fig. 5.3;Miller et al.. 1992: Oberhiinsli, 1997, and became extinct during the period of gradual cooling of deep waters in the middlelate Eocene. We speculate that both N. truempyi and N. umboniJbra indicate relatively oligotrophic conditions, but that N. truempyi could not survive in the more corrosive waters that filled the deep oceans from the late Eocene onwards. ...
... There was a major increase in ocean productivity (see summary in Berger, 2007), a very large drop in the calcite compensation depth (CCD) (Van Andel, 1975;Coxall et al., 2005;Rea and Lyle, 2005), and pulses of strongly eroding Antarctic bottom water (see summaries in Kennett [1977] and Wright and Miller [1996]) and Northern Component Water (see summaries in Tucholke and Mountain, 1979;Miller and Tucholke, 1983;. Paleontological evidence for cooling includes the development of psychrospheric ("cold-loving") ostracods (Benson , 1975), deep-sea and shelf benthic foraminiferal extinctions and appearances (e.g., Miller et al., 1992;Thomas, 1992), extinctions in tropical planktonic and larger foraminifera (Adams et al., 1986;Keller et al., 1992;Pearson et al., 2008;Wade and Pearson, 2008), and the decline of thermophilic calcareous nannoplankton (Aubry, 1992;Dunkley Jones et al., 2008). Terrestrial cooling is indicated by pollen changes (e.g., New Jersey; Owens et al., 1988) and a mammalian turnover (e.g., England; Hooker et al., 2004). ...
We present an overview of the Eocene-Oligocene transition from a marine perspective and posit that growth of a continent-scale Antarctic ice sheet (25 × 106 km3) was a primary cause of a dramatic reorganization of ocean circulation and chemistry. The Eocene-Oligocene transition (EOT) was the culmination of long-term (107 yr scale) CO2 drawdown and related cooling that triggered a 0.5%-0.9% transient precursor benthic foraminiferal δ18O increase at 33.80 Ma (EOT-1), a 0.8% δ18O increase at 33.63 Ma (EOT-2), and a 1.0% δ18O increase at 33.55 Ma (oxygen isotope event Oi-1). We show that a small (̃25 m) sea-level lowering was associated with the precursor EOT-1 increase, suggesting that the δ18O increase primarily reflected 1-2 °C of cooling. Global sea level dropped by 80 ± 25 m at Oi-1 time, implying that the deep-sea foraminiferal δ18O increase was due to the growth of a continent-sized Antarctic ice sheet and 1-4 °C of cooling. The Antarctic ice sheet reached the coastline for the first time at ca. 33.6 Ma and became a driver of Antarctic circulation, which in turn affected global climate, causing increased latitudinal thermal gradients and a "spinning up" of the oceans that resulted in: (1) increased thermohaline circulation and erosional pulses of Northern Component Water and Antarctic Bottom Water; (2) increased deep-basin ventilation, which caused a decrease in oceanic residence time, a decrease in deep-ocean acidity, and a deepening of the calcite compensation depth (CCD); and (3) increased diatom diversity due to intensified upwelling.
... The Cenozoic bathyal and abyssal succession was sorted into assemblage zones (Berggren and Miller 1989;Miller et al. 1992), and three (later, four) turnovers were distinguished as the basis for four (now five) faunas. A "Cretaceous fauna" persisted into the Paleocene until its abrupt extinction at the end of that epoch, indeed, the severest extinction of the entire Cenozoic (Thomas 1998). ...
The dense record of Cenozoic foraminifera simultaneously supplies a mosaic of biostratigraphy, a rich field for evolutionary studies and the vehicles for geochemical environmental proxies. Four groups are discussed: the larger foraminifera on the warm-water shelves and platforms, the planktonics, the deep-sea faunas and the southern-extratropical benthics. The environmental trajectory from greenhouse in the later Cretaceous and earlier Paleogene to icehouse in the Neogene is not smooth but punctuated, and there are two particularly critical intervals, later Eocene and early-middle Miocene. The foraminiferal record is not smooth but chunky at 107 years’ scale. There are several good examples of two powerful synchroneities, one being between the faunas of the different realms and the other between the fossil record and the physical-environmental record.
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