New marine data and age accuracy of the Romualdo Formation, Araripe Basin, Brazil

A combined biostratigraphic and palaeoecological study of foraminifera, ostracodes and microfacies was carried out on the Aptian in the Sítio Sobradinho section of the Araripe Basin, northeast Brazil. The analysed section represents a deepening-upward sequence with mid-ramp shoal and outer ramp to basin facies associations on a mixed siliciclastic-carbonate marine ramp. The analysed rocks are dominated by Early Cretaceous planktic foraminifera (Hedbergella aptiana, H. praelippa, H. sigali, Blesfucuiana cf. cumulus, Microhedbergella miniglobularis, Gorbachikella cf. kugleri, Pseudoguembelitria blakenosensis, Globigerinelloides clavatus, Globigerinelloides aff. aptiensis, Gubkinella sp. and Loeblichella sp.). Ostracoda fauna is composed mainly of Pattersoncypris crepata and Pattersoncypris micropapillosa. The occurrence of P. crepata associated with the Aptian planktic foraminifera demonstrates the potential of this ostracode species to date this interval. The planktic foraminifera from the upper Aptian (Microhedbergella miniglobularis Zone) of the Araripe Basin show characteristical Tethyan affinities.


Scientific RepoRtS
| (2020) 10:15779 | https://doi.org/10.1038/s41598-020-72789-8 www.nature.com/scientificreports/ recognition of the Aptian marine transgression into the basin and the posterior retreat registered by the Araripe Group. Subsurface data of the Romualdo Formation are quite scarce, and hence, vertical stratigraphic sections in outcrops are essential to better understand its stratigraphy. The Romualdo Formation comprises a wide range of lithologies, including stratified conglomerates, fine-to medium-grained sandstones, laminated limestones, marls, shales and coquinas, which characterize a coastal to marine environment 22 . Along the slopes of the Araripe Plateau are known good outcrops of this unit, such as the Sítio Sobradinho outcrop, which reaches a thickness of ~ 100 m and is the most representative outcrop showing the vertical stratigraphic section of the Romualdo Formation, allowing detailed studies. According to Custódio et al. 23 , the absence of the Ibupi Formation in the Sítio Sobradinho section causes nearshore deposits to rest unconformably atop the carbonate-siliciclastic facies of the Crato Formation. Four facies associations are related to a transgressive system track stacking pattern and the posterior highstand system track 23 . Many discrepancies remain among the studies regarding how seawater reached the Araripe Basin [24][25][26][27] , as illustrated in the Fig. 1. Tectonic and geodynamical models show the opening of the South Atlantic Ocean beginning from the south. According to Heine et al. 28 , SW-directed extension had already started during the latest Jurassic in the southern part of the South Atlantic Rift System; in addition, break-up and seafloor spreading started near 138 Ma (mid-Berriasian), during which time E-W-directed extension between South America and Africa occurred at very low extensional velocities until the Hauterivian (~ 126 Ma), when rift activity in the equatorial Atlantic started to increase significantly with significant rotation towards NE-SW. From the base of the Aptian onwards, diachronous lithospheric breakup occurred along the central South Atlantic Rift, and the final breakup between South America and Africa occurred in the Santos-Benguela segment at approximately 113 Ma and in the equatorial Atlantic between the Ghanaian Ridge and the Piauí-Ceará margin at 103 Ma 28 . On the other hand, eustasy studies demonstrate that the sea level remained higher than the present-day mean throughout the Cretaceous, though the Aptian and early Albian eustatic sea level went into a long period of stasis, during which the sea level varied only by a relatively moderate amplitude (between 25 and 75 m) 29 .
In palaeoclimatic terms, the Aptian (∼ 125 to ∼ 113 Ma) was characterized by climatic changes and profound environmental perturbations, including Oceanic Anoxic Event (OAE) 1a (∼ 120 Ma), representing a global phenomenon of organic matter burial in oxygen-depleted oceans [30][31][32][33][34] . Apart from the terminal Cretaceous extinction, the planktic foraminiferal turnover across the Aptian/Albian boundary interval is the most dramatic event in the Cretaceous evolutionary history of planktic foraminifera, with a change from large-sized and heavily ornamented species in the latest Aptian to small-sized, globigeriniform specimens in the earliest Albian [35][36][37][38] . In the Araripe Basin, the occurrence of foraminifera associations has previously been recognized, inferring a marine ingression into the Araripe Basin recorded in the Romualdo Formation, but their taxonomy and distribution are not documented in detail 39,40 . On the other hand, palynoforaminifers (chitinous linings present in palynological preparations) are usually rare and related to benthic taxa [41][42][43][44] . Goldberg et al. 44 especially recovered palynoforaminifera in the infra-Ipubi strata of the Araripe Basin, indicating that marine ingression occurred before evaporitic deposition. The ostracodes from the Araripe Basin have received the attention of several authors due to their abundance, diversity and excellent preservation 6,45,46 , including an unusual record of ostracodes with phosphatized appendages and eggs in deposits from the Romualdo Formation 3,47-49 . The absence of reliable index fossils has led to constant debates about the age of the Romualdo Formation, being positioned on the Alagoas local stage (Ostracoda Zone RT-011) in the Aptian-Albian 17,22 . To constrain the chronostratigraphic position of this interval, we report robust marine data from the Romualdo Formation represented by a set of microfossils, including planktic and benthic foraminifera, ostracodes and calcispheres of Early Cretaceous age from the Araripe Basin. The significance of this study lies in the calibration of Aptian planktic foraminiferal events with ostracode species.

Methods
A lithostratigraphic section of the maximum flooding zone of the Romualdo Formation at the Sítio Sobradinho outcrop was performed. According to the lithological variation, thirteen samples were collected for micropalaeontological analysis, and six petrographic slides were prepared for microfacies analyses. Petrographic analysis was carried out with a Zeiss Axio Scope.A1 microscope equipped with a Zeiss AxioCam MRc camera at the Applied Micropaleontology Laboratory (LMA) of the Federal University of Pernambuco, Brazil. Microphotographs of petrographic slides and selected carbonate microfossils were obtained from a Phenom XL scanning electron microscope (SEM) at the LMA.
For the studies of carbonate microfossils, approximately 60 g of sediment was used, and mechanical disaggregation of the lithic samples was performed on smaller fragments (⁓5 mm), followed by immersion in water. After a period of 24 h, the sample was washed in water using different sizes of sieves (> 500 μm, > 250 μm, > 18 0 μm, > 63 μm and > 45 μm) and dried at 50 °C. This technique allows the extraction of planktic foraminifera, as well as benthic foraminifera, ostracodes, and other microfossils, without destroying or corroding the microfossils. Specimens that remained with the aggregated sediment were treated in an ultrasound bath at variable times. Picking was performed under a Zeiss Stemi 305 stereomicroscope at all fractions, from > 250 μm and > 180 μm fractions, all specimens were collected. The smallest fractions samples (> 63 μm and > 45 μm) displayed high abundance and were quartered; the picking process reached 300 specimens from each fraction sample. The age of the sedimentary section studied here was attributed based on the known biostratigraphic ranges of the recovered species using the scheme by Huber and Leckie 50 and Petrizzo et al. 51 as the basis. The specimens presented here were deposited in the LMA, under the collection numbers LMA-00029 to LMA-00073.

Results
The stratigraphic interval here studied is characterized by a general fining-upward gradation from fine-grained sandstone to siltstone, laminated claystone and an organic-rich shale succession with carbonate rocks (Fig. 2). From the base to the top, eight lithofacies were identified, and the microfacies of seven of these were analysed. Lithofacies A is a massive, fine-grained calcareous quartz arenite with chlorite, muscovite and pellets or foliated grains of glauconite ( Fig. 2a-d). Lithofacies B corresponds to a massive medium-grey to light yellow siltstone (the same for sample 4BAr01E and calciferous sample 4BAr01D). Lithofacies F is a laminated and lenticular organic-rich claystone with pyrite. From a laterally continuous level, lithofacies G is defined as a massive wackestone with abundant ostracodes and foraminifera, pyrite grains are also observed ( Fig. 2e-h). From a sample concretion, lithofacies I corresponds to a laminated ostracode wackestone with rare foraminifera and silica grains ( Fig. 2i-l). Lithofacies K corresponds to a shale package containing interbeds, concretions and lenses of limestone, its microfacies is characterized by wavy carbonaceous and clay laminae with intercalated ostracode valves ( Fig. 2m-p). Lithofacies L, which is a laterally discontinuous lens, corresponds to a calcisphere mudstone with rare foraminifera and ostracodes ( Fig. 2q-t).
The recovered microfossil assemblages are mainly represented by foraminifera, ostracodes and calcispheres, which have a constant presence in the middle portion (samples 4BAr01G-4BAr01L) of the section, with moderate diversity and an abundance of recovered specimens. The first samples corresponding to the base of the section are sterile, one possibility could had been due to dissolution during diagenesis. In the upper portion of the section, there is a decrease in the occurrence of ostracodes and foraminifera, and microgastropod specimens, bivalves, bone fragments and plant fragments (bryophyte capsules) are recovered. The distribution and abundance of the different taxonomic groups recovered are shown in Fig. 3.
From the ostracode fauna ( Fig. 5), it is possible to recognize three associations: the first is represented by representatives of the genera Alicenula, Ilyocypris and Damonella, being registered below the first occurrence of foraminifera; the second association is composed of an abundant and monospecific association of Pattersoncypris crepata with more than 2000 specimens, associated with an abundant and diverse assemblage of benthic and planktic foraminifera; the third ostracode association is composed of Pattersoncypris micropapillosa and juvenile specimens of Pattersoncypris spp., which occur in the uppermost portion of the studied section.

Discussion
The late Aptian-early Albian biotic turnover records a dramatic extinction event of large-sized Aptian planktic foraminifera taxa and the appearance of few new small-sized Albian species. Based on planktic foraminifera, the late Aptian-early Albian boundary is marked by the last occurrences of typically Aptian taxa, particularly Paraticinella rohri 36,[52][53][54][55] (Fig. 6). The Microhedbergella miniglobularis Zone occurs above the extinction of Paraticinella rohri species, co-occurring with the last long-ranging Aptian hedbergellids and the first occurrence of Microhedbergella renilaevis 50 , in addition to the complete absence of planktic foraminifera in the > 250 μm size fraction 51 . The Microhedbergella renilaevis Zone corresponds to the biostratigraphic interval from the first occurrence of Microhedbergella renilaevis to the first occurrence of Microhedbergella rischi.
The sedimentary succession from Sítio Sobradinho is assigned to the upper Aptian. The recovered association is composed of Hedbergella aptiana, H. praelippa, H. sigali, Blesfucuiana cf. cumulus, Gorbachikella cf. kugleri, Pseudoguembelitria blakenosensis and Microhedbergella miniglobularis, which allows a chronostratigraphic position in the upper Aptian, correlated with international foraminiferal zonal schemes 50,51,[55][56][57] . In addition, the co-occurrence of Pattersoncypris crepata, whose record is very characteristic of the middle-upper Aptian from Brazilian deposits, in the Araripe Basin 58 , Potiguar Basin 59 and Sergipe-Alagoas Basin 60 is correlated with a palynological zone coded as P-270 59 and corroborates the foraminifera dating. These data reinforce the potential   51 , the first occurrence of Microhedbergella renilaevis marks an important bioevent that represents a major step in the evolution and diversification of the Albian planktic fauna, an event that was not identified in the studied section. Furthermore, the chronostratigraphic positioning of the lithological section studied in the upper Aptian, can be corroborated by the occurrence of Sergipea variverrucata Palynozone P-270 [66][67][68] , which was identified throughout the Sítio Sobradinho section by Teixeira et al. 69 .
The aspects involving the age and direction of marine ingression into the Araripe Basin and northern South Atlantic Ocean have been the subject of active discussion for many years [24][25][26][27] , as illustrated in Fig. 1. In northeast Brazil, the Aptian transgression was sufficiently extensive that evaporites were deposited even in the interior basins. In the Araripe Basin, this transgression is represented by the Ipubi Formation and the typical marine fossil record towards the top of the Romualdo Formation. Based on the fossils, several routes have been hypothesized for the marine ingression into the Araripe Basin, that is, through the Parnaíba, Sergipe or Potiguar Brazilian basins, as a junction of three seaways that effectively connected these basins or (as a highly speculative hypothesis) via an extensive seaway from northwestern South America 25,26 . On the other hand, considering only stratigraphic and sedimentologic information, Assine et al. 27 suggested that the Parnaíba and Potiguar basins were set apart from each other and from the Araripe Basin, configuring marine transgression towards these respective basins from the north, northeast and southeast. This hypothesis and the available information on the fluvial southeastdirected palaeocurrents of the Barbalha Formation (the base of the Santana Group) flowing towards the Jatobá, Tucano and Recôncavo rift system indicates continental palaeodrainage 70 and reinforce the existence of an epeiric sea following upstream river valleys into the Araripe Basin from the southeast 23 . Nevertheless, the present structural framework of the Araripe Basin corresponds to a graben inverted into a high-standing horst due to the stress field imposed by ridge-push forces from the Mid-Atlantic Ridge to the west and from the Andes to the east mainly during the Quaternary, and rift-related normal faults concentrated along inherited shear zones were reactivated to form the main inversion faults 71 . The aforementioned palaeocurrents that exist along the generally inverted western margin of South America may be altered from their original orientations, and thus, interpretations of Cretaceous flowing directions based on these palaeocurrents should be re-evaluated. However, palaeobiogeographical differentiation is observed in the Aptian microfossil association of the South Atlantic as www.nature.com/scientificreports/ a result of the physical barrier in the Santos-Benguela segment that hinders the free circulation and mixing of seawater between the southern and central to equatorial South Atlantic 24 . In relation to foraminifera, the absence of several species of tropical/subtropical planktic foraminifera from the Aptian-Albian sedimentary successions in the southernmost sector of the northern South Atlantic Ocean (north of the Walvis Ridge-Rio Grande Rise), resulted in tentative zonal assignments based on the occurring assemblages, and this pattern has been interpreted as an effect of a possible Austral palaeobiogeographical affinity [72][73][74] . The studies of Koutsoukos 56 and Kochhann et al. 57 , which addressed the foraminiferal assemblages of the Sergipe Basin (Brazil) and DSDP Site 364 (offshore Angola), indicate a tropical/subtropical affinity for several species, suggesting that these areas had at least surface-water exchanges with the western Tethyan biogeographic provinces of the low-latitude central North Atlantic, possibly even at intermediate (epi-to mesopelagic) water depths. The last referred authors reinforced the theory of a surface-water connection between the proto-central Atlantic Ocean and the southernmost sector of the northern South Atlantic Ocean (north of the Walvis Ridge-Rio Grande Rise) during the late Aptian. The Aptian foraminiferal association presented here has a tropical/subtropical affinity when compared with previously described associations (Sabinas Basin, Mexico 75 50,75,[80][81][82][83][84] . Biogeographic evidence suggests that these globular forms can be considered indicators of warm sea surface temperatures, the occurrence of which is related to the emergence of possibly eutrophic and/or climatic (probably hot) oceanographic conditions 83,85,86 . Thus, the data presented herein support a surface-water marine connection with open-marine and shallow-water foraminiferal assemblages 38 between the central Atlantic Ocean by the late Aptian. This connection could be related to the global sea-level rise reported at that time 24,29,56,77,[87][88][89] .
The eight meters interval studied here corresponds to the maximum flooding zone identified by Custódio et al. 23 in the total ~ 100 m of the Romualdo Formation at the Sítio Sobradinho outcrop. The vertical distributions of the lithological and palaeontological macro-and microfacies in the stratigraphic interval result in the division into two facies associations related to a deepening-upward sequence on a ramp-type and mixed siliciclasticcarbonate marine shelf (Fig. 7). To the western of the Araripe Basin, Varejão et al. 90 described microbialites and stromatolites associated to rocky-protected lagoon, that corroborates our interpretation of a low-gradient ramp, deeper to the east of the basin where Sítio Sobradinho Section is located. The lower studied interval corresponds to the mid-ramp shoal facies association, which groups the glauconite-bearing calcareous quartz arenite and the siltstone to claystone overlaid strata. From this interval, rare freshwater and transitional ostracode occurrences, represented by the genera Damonella, Alicenula and Ilyocypris 46,91-96 , were recorded in samples below the first occurrences of foraminifera, suggesting the allochthonous origin of these ostracofauna. In addition, the marine phase in the basin is reinforced by the presence of glauconite as foliated and peloidal grains, which represent the seafloor synsedimentary glauconitization of detrital biotites and a diagenetic product, respectively, which formed especially during intervals of mildly reducing conditions 97,98 . Glauconite formation is a slow process that requires low rates of sediment accumulation to allow the long-term contact of detrital grains with seawater in primarily mid-to outer-shelf settings 97 . According to Flügel 99 , syndepositional authigenic glauconite indicates a break in sedimentation, commonly in deep subtidal and bathyal environments. The greatest period of glauconite formation occurred in the Cretaceous, notably along the continental margins of the widening North Atlantic Ocean, when the global sea level was high 100 .
The upper studied interval corresponds to the outer ramp to basin facies association and is characterized by a carbonaceous and fossiliferous shale package interbedded by plankton-bearing wackestone and mudstone as continuous beds, lenses and concretions. A depositional environment with palaeodepths estimated between fifty and two hundred metres can be corroborated by the dominance of benthic foraminifera with a tubular form (the M1 morphogroup), infaunal organisms (Rhizammina and Bathysiphon), and less abundant but still frequent reophacellids (Falsogaudryinella) and ammodiscids (Glomospira), which indicate poorly oxygenated conditions in a middle neritic-upper bathyal environment represented by suspension feeders that prefer a low organic carbon flux and high dissolved oxygen content [101][102][103][104] . The lack of a continuous reef and the lack of shallow water-derived clasts in deeper-water sediments led to the characterization of the Sítio Sobradinho section as having been deposited on a ramp-type marine shelf without a steep slope at the edge (e.g., Flügel 99 ). In addition, the presence of a monospecific fauna, Pattersoncypris crepata, associated with agglutinated foraminifers indicates its tolerance to higher-salinity conditions, and thus, it is considered a holoeuryhaline species, as was interpreted from its record with the first marine incursion in the Potiguar Basin 59,105-107 . Furthermore, in the Sergipe-Alagoas Basin, the species Pattersoncypris crepata occurs at the same levels as the typical marine ostracodes of the genera Cytherella, Cytherelloidea, Patellacythere and Aracajuia 60 .
In the eastern part of the Araripe Basin, the Romualdo depositional sequence records a transgressive-regressive cycle comprising a transgressive system tract with tide-dominated coastal facies to outer-shelf black shales as the maximum flooding zone and a highstand system tract characterized by a progradational package that records gradual continentalization 23 . The two facies associations we recognized macro-and microscopically can be correlated with the inner to outer shelf, dysoxic to anoxic facies association identified by the previously mentioned authors with the important difference that no proximal facies were observed in the interval analysed herein. The textural framework and the carbonate grains ('allochems') determined in the studied carbonate microfacies indicate that the carbonate rocks associated with the organic-rich shale succession represent the 2 -5 ramp microfacies types (RMFs) (sensu Flügel 99 ), so it is assumed that the studied interval was deposited from the mid-ramp shoal to basin positions. This palaeoenvironmental interpretation is reinforced by the distribution of the identified foraminifera and ostracode microfossils.    www.nature.com/scientificreports/ The low diversity-assemblage of planktic foraminifera recovered from the Sítio Sobradinho section is predominantly composed of small hedbergellids (Hedbergella and Microhedbergella) and chilostomellids (Gubkinella), which are characteristic of late Aptian-early Albian deposits around the world 51,56,57,73,76,108 , whose deposition may be related to OAE 1b 35,109,110 . The post-Paraticinella rohri ecosystem promoted the proliferation of very small planktic foraminiferal taxa (i.e., microhedbergellids) and siliceous plankton (i.e., radiolarian), which thrived as opportunistic/disaster taxons 109,110 . According to Sabatino et al. 111 , the ecological behaviour of M. miniglobularis, whose record in the analysed section is abundant, seems to be that of a disaster opportunist since it occurred and thrived during a period of high but variable environmental stresses when no other planktic foraminifera are present, whereas it is rare or absent in normal environments. In addition, the abundant record of Gubkinella sp. supports the idea of a restricted environment after a rapid connection with the sea since representatives of this genus are generally less abundant in open-ocean environments and probably have broad ecological (eurytopic) tolerances, being especially characteristic of neritic environments, continental margins, epicontinental seas 75,108,112 and areas of upwelling 113 . According to Leckie 113,114 , the genus Gubkinella is one of the main representatives of the "Epicontinental Sea Fauna", composing an average of 4.5% of the assemblage. The variable abundance of Gubkinella (epicontinental plankton) relative to Hedbergella and Globigerinelloides (open-marine shallow-water plankton) suggests a relatively shallow continental margin and/or highly fertile surface waters (possibly within 500 m) in a restricted environment at the time of deposition based on the palaeoecological model of Leckie 113 . Moreover, abundances of these "Epicontinental Sea Fauna", described in the upper Aptian of northwest Africa 76 and along the Antarctic margin 114 , similar as we recorded, are perhaps associated with highly productive continental margins 113  www.nature.com/scientificreports/ and especially P. micropapillosa, may indicate a change in environmental conditions, with the beginning of a mixohaline to limnic environment 6,43,63 that can characterize very proximal conditions but with the high influence of components of marine origin, evidencing a proximal-distal transitional coastal marine environment 69 .
In summary, this integrated study of foraminifera, ostracodes and other microfossil data from the Romualdo Formation indicates that the local Alagoas Stage (Ostracoda Zone RT-011) can now be constrained to the Aptian. The foraminiferal assemblages show Tethyan affinities suggesting a marine route coming to the Araripe Basin from the equatorial South Atlantic with north seawater origin. www.nature.com/scientificreports/