Changes in macrofaunal groups before, during and after the Cenomanian–Turonian biotic crisis in north Eastern Desert, Egypt

The stratigraphic distribution of the different faunal groups of the upper Cenomanian–lower Turonian deposits in the north Eastern Desert, Egypt, is investigated. Variations in species richness, faunal diversity, extinction and origination rates before, during, and after the globally known Oceanic Anoxic Event (OAE) 2 are documented. The OAE2 interval is constrained by the first occurrence of the marker ammonite species Vascoceras cauvini and the last occurrence of Vascoceras proprium, along with the positive δ13C excursions, previously identified from the Wadi El-Burga section. A prominent decline in species richness and diversity, high extinction rates, and low origination rates of the recorded macrofaunal elements are reported during the OAE2 interval. Such faunal bottleneck was attributed to the prevailing major palaeoclimatic and palaeoenvironmental perturbations during that time. Besides oceanic anoxia, changes in sea water palaeotemperature and sea level are discussed. It can be concluded that oceanic anoxia, warming, and /or transgressive episodes were the major driving mechanisms of the faunal crisis reported in the present work.

In Egypt, the OAE2 was reported based on the positive δ 13 C excursion, rather than the presence of organic-rich shales (El-Sabbagh et al. 2011;Nagm et al. 2014Nagm et al. , 2021)).Despite the extensive literature on the faunal content of the upper Cenomanian-lower Turonian deposits in north Eastern Desert (Kassab and Ismael 1996;Bauer et al. 2001;Hewaidy et al. 2003;Abdel-Gawad et al. 2007;Boukhary et al. 2009;El-Qot et al. 2009;Shahin and El-Baz 2010;Nagm et al. 2010a;Ayoub-Hannaa and Fürsich 2011;El-Sabbagh et al. 2011;Nagm and Wilmsen 2012;Ayoub-Hannaa et al. 2014;Nagm 2015;Boukhary et al. 2017;Nagm 2019), these studies were mainly focused on the taxonomy of the faunal groups and biostratigraphic subdivision of the studied intervals, except for the work of Nagm et al. (2021).Nagm et al. (2021) provided only a general view Maghra El-Hadida Formation, corresponding to the global mid-late Cenomanian SB Ce5 (Wilmsen andNagm 2012, 2013).This sequence boundary is characterised by abrupt facies change from the highstand shaley facies and deep subtidal bioclastic floatstone facies of the Galala Formation at Umm Khayshar and Askhar El-Bahari areas, respectively, to the intertidal sandstone facies of the Maghra 3).Only the lower part of the Maghra El-Hadida Formation is investigated in the present study, dominated by open-marine carbonate rocks (Figs. 2, 3;Wilmsen and Nagm 2012).It is made up of brownish yellow, fine-grained, calcareous sandstones, followed by highly fossiliferous, fine-grained marly and dolomitic limestones, with diverse ammonoid content of late Cenomanian and early Turonian age (Figs. 2, 3).The Maghra El-Hadida Formation suggests deposition on a homoclinal carbonate ramp with sub-environments ranging from deep-subtidal basin to intertidal back-ramp (Wilmsen and Nagm 2012).
Based on the presence of upper Cenomanian cephalopods in the upper part of the Galala Formation and the lower part of Maghra El-Hadida Formation, the boundary between the two formations lies below the Cenomanian-Turonian boundary, unlike that has been reported in the previous studies (e.g.Hewaidy et al. 2003).

Materials and methods
Two complete stratigraphic sections across the upper Cenomanian-lower Turonian successions at the Northern and Southern Galala Plateaus, north Eastern Desert, Egypt, were measured and investigated (Askhar El-Bahari section: 29° 03′ 04″ N and 32° 01′ 09″ E and Umm Khayshar section: 28° 51′ 54″ N and 32° 9′ 50″ E; Fig. 1b).Fossils were gathered bed-by-bed from the highly fossiliferous intervals and identified to the species level (Online Resources.1, 2).The stratigraphic ranges of the identified macrofaunal species were carefully traced (Figs. 2, 3).The ammonites were investigated and their stratigraphic ranges were used for biostratigraphic subdivision of the studied interval.
The high-resolution δ 13 C excursions (OAE2), generated from the Wadi El-Burga section (Nagm et al. 2014), about 40 km to the south of the study area, were incorporated in the present study using the age-defining ammonite biozones (Fig. 4).A sample-species occurrence matrix of the macrofossils was generated for further quantitative analyses (Online Resource.3).The diversity is calculated for each faunal group, expressed by the species richness (the number of species, with low species richness =<5 species, moderate =5-15 species, and high >15 species) and Shannon-Wiener diversity index (H;Shannon 1948) for each interval.The diversity changes of the different faunal groups across the Cenomanian-Turonian boundary were documented in order to identify the different bioevents.The extinction and origination rates are defined following Kurihara (2012), where the Extinction rate = (number of species absent in an interval) / (total number of species in the preceding interval) × 100%, and the Origination rate = (number of species present in an interval and not present in the preceding one) / (total number of species present in the former interval) × 100%.All material is hosted in the Geological Museum, Helwan University, Cairo, Egypt.

Ammonite biostratigraphy
The studied strata of the north Eastern Desert contain rich ammonite fauna, including the main index taxa of the upper Cenomanian-lower Turonian transition, allowing a high-resolution biostratigraphic subdivision for this time interval.Based on the stratigraphic distribution of the identified ammonite species in the studied sections (Figs. 2, 3), two upper Cenomanian ammonite zones (Neolobites vibrayeanus Zone and Vascoceras cauvini Zone) and two lower Turonian ammonite zones (Vascoceras proprium Zone and Choffaticeras segne Zone) have been differentiated.
The interval representing the OAE2 is equivalent to the uppermost Cenomanian Vascoceras cauvini Zone and the lower Fig. 5. Representative section for the studied Cenomanian-Turonian successions, showing changes in species richness, diversity, extinction and origination rates before, during, and after the OAE2 interval Turonian Vascoceras proprium Zone (Fig. 4).This interval contains diverse faunas, represented by cephalopods, bivalves, gastropods, and echinoids, with relatively moderate species richness (33 species) and high diversity (H = 2.74; Fig. 5).

Discussion
The Oceanic Anoxic Event 2 is not reflected in the study area by organic-rich shales, but the positive carbon isotope excursion (Nagm et al. 2014;Fig. 4) as well as its negative impact on the faunal diversity can be identified.Such impact on faunal content has been regarded as a global bioevent, being reported in many basins worldwide (Elder 1989;Gale et al. 2000;Keller et al. 2001;Keller and Pardo 2004;Caron et al. 2006;Monnet 2009;Gebhardt et al. 2010;Horne et al. 2011;Kurihara 2012;Ruban 2013;Joo and Sageman 2014;Nagm 2015;Nagm et al. 2017Nagm et al. , 2021;;Freymueller et al. 2019).
The stratigraphic ranges of the recorded macroinvertebrates in the Umm Khayshar and Askhar El-Bahari areas, north Eastern Desert, Egypt, illustrate significant faunal changes across the lower and upper boundaries of this mass extinction bioevent (Figs. 2, 3).The lower boundary is characterised by a great drop in the species richness and diversity of echinoids, gastropods, and bivalves across the top of the upper Cenomanian Neolobites vibrayeanus Zone.However, cephalopods show rather increase in the species richness and diversity (Fig. 5).
The upper boundary of this mass extinction bioevent is also characterised by a drop in the species richness and diversity of echinoids, gastropods, bivalves, and cephalopods across the top of the lower Turonian Vascoceras propium Zone (Fig. 5).In addition, about 87.9% of the total faunal taxa in the OAE2 interval went extinct (100% of echinoids, gastropods, and bivalves, and 63.6% of cephalopods), and about 33.3% of the cephalopod species recorded in the interval succeeding the OAE2 interval originated (Fig. 5).A nearly complete loss of infaunal taxa, and the dominance of carnivore taxa are observed (Fig. 6), suggesting a new, substantially different ecologic structure.This supports the hypothesis that oceanic anoxic events have most severe negative impact on the infauna than on any other ecological group (Freymueller et al. 2019).
The start of the bioevent coincides with the top of the uppermost Cenomanian Neolobites vibrayeanus Zone, about ca.400 ka before the Cenomanian-Turonian boundary (93.9Ma; Gradstein et al. 2004Gradstein et al. , 2012;;Nagm 2015).It continued across the Cenomanian-Turonian boundary, and its upper boundary coincides with the top of the lower Turonian Vascoceras proprium Zone, about ca.200 ka after the Cenomanian-Turonian boundary (Nagm 2009(Nagm , 2015)).Consequently, this bioevent lasted for 600 ka in the north Eastern Desert.
The faunal change reported in the present study temporally overlaps well with the OAE2 (Figs. 5, 6), with dramatic changes in species richness and diversity, and various palaeoenvironmental perturbations, e.g.oceanic anoxia, sea water palaeotemperature changes, and sea-level changes (Ruban 2013;Nagm et al. 2017).Oceanic anoxia during the OAE2 were developed in response of the progressive expansion of the oxygen minimum zone through the water column (Schlanger and Jenkyns 1976;Elder 1989;Harries and Little 1999;Kuypers et al. 2004;Monteiro et al. 2012;Pogge von Strandmann et al. 2013;Owens et al. 2018;Freymueller et al. 2019).
Several hypotheses have been introduced concerning the main cause of the OAE2 and the associated mass extinction.Hut et al. (1987), Kauffman (1995), and Kauffman and Hart (1995) hypothesised that a comet shower was the primary cause of that mass extinction.However, Monnet (2009) argued against this hypothesis as the known iridium anomalies were not associated with the faunal diversity decline.The relatively well-founded hypothesis of the cause of the OAE 2 is the emplacement of a large igneous province (LIP; Turgeon and Creaser 2008;Du Vivier et al. 2014;Papadomanolaki et al. 2022).This process resulted in a considerable temperature increase by CO 2 outgassing, enhanced chemical weathering, increased primary production, expansion of the oxygen minimum zone, and formation of black shales (Huber et al. 1995;Bornemann et al. 2005;Monnet 2009;Monteiro et al. 2012;Keller et al. 2021), ultimately triggering the mass extinction associated with OAE 2.
The transgressive episode characterising Egypt coincides with a prominent reduction in species richness and diversity, and high extinction rates of the recorded faunal groups (Fig. 5).It can be concluded that the faunal bottleneck reported from the north Eastern Desert, Egypt, during the OAE2 interval has been a response to one or combination of several palaeoenvironmental perturbations, e.g.oceanic anoxia, global warming, and/or considerable deepening.

Conclusions
The upper Cenomanian and lower Turonian macrofauna (cephalopods, bivalves, gastropods, and echinoids) from the Umm Khayshar and Askhar El-Bahari sections at the Northern and Southern Galala Plateau, north Eastern Desert, Egypt, are studied.The studied interval is associated with the positive δ 13 C excursion, inferred from the previously studied Wadi El-Burga section, characterising the Ocean Anoxic Event 2. A precise biostratigraphic calibration of the interval was conducted using ammonite biozonation.
The interval representing the OAE2 in the study area is equivalent to the uppermost Cenomanian Vascoceras cauvini Zone and the lower Turonian Vascoceras proprium Zone.Remarkable changes in the macrofaunal distribution patterns are shown against the OAE2, represented by significant losses of most faunal elements, with a prominent decline in species richness and diversity, high extinction rates, and low origination rates.Such OAE2-linked faunal loss is analogous to that of Western Europe, United States, and Jordan.
In the study area, the start of OAE2 is characterised by the extinction of 93.3% of echinoids, 80% of gastropods, 64.1% of bivalves, and 100% of cephalopods.High extinction rates (100% of gastropods, bivalves, and echinoids, and 63.6% of cephalopods) characterise also the end of the OAE2.The dominance of carnivore, nektonic taxa following this biotic crisis indicates that the OAE2 has significantly affected the ecologic structure.The faunal bottleneck during the OAE2 interval reported has been attributed to one or more palaeoenvironmental changes, e.g.oceanic anoxia, warming, and/or a major episode of sea-level rise.

Fig. 1 .Fig. 2 .
Fig. 1. a Late Cenomanian palaeogeographic map, showing the position of the study area (after Scotese 2014).b Location of the study area, with indication for the studied and reference sections (Google Earth, earth.google.com/web/)

Fig. 6 .
Fig. 6.Representative section for the studied Cenomanian-Turonian successions, showing changes in life mode, feeding strategy, and proportions of faunal groups before, during, and after the OAE2 interval

Fig. 7 .
Fig. 7. Individual-based percentages of (a) bivalve families before the OAE2 interval.b echinoid families before the OAE2 interval.c gastropod families before the OAE2 interval.d bivalve families during