Calcareous nannofossils, biostratigraphy, and paleobiogeography of the Aptian/Albian Romualdo Formation in the Araripe Basin, North-Eastern Brazil

Abstract The objectives of this study were the biostratigraphic and paleobiogeographic interpretations of the calcareous nannofossil records of the Romualdo Formation (Aptian-Albian) in the south-central portion of the Araripe Basin. The methods used to process the samples were decanting, smear slide, centrifugation, and ultra-thin section confection. The taxonomic and biostratigraphic interpretations were carried out through qualitative and quantitative investigations. A total of 11 genera and 17 species of calcareous nannofossils, namely, Biscutum constans, Biscutum sp., Braarudosphaera africana, Braarudosphaera sp., Calculites sp., Discorhabdus ignotus, Hayesites albiensis, Hayesites sp., Nannoconus bucheri, Nannoconus sp., Retecapsa surirella, Rhagodiscus sp., Thoracosphaera sp., Watznaueria barnesiae, Watznaueria sp., Zeughrabdotus erectus, and Zeughrabdotus noeliae were identified. The integrated analysis of three outcrops suggests two distinct marine phases: the first in the Aptian, recognized in two outcrops, and during the Albian age. The genera Hayesites and Nannoconus suggest a strong Tethyan affinity. Differently, other calcareous nannofossils such as Watznaueria, Thoracosphaera, and Braarudosphaera recorded here are considered more resistant, cosmopolitan, and/or opportunistic species. Biscutum and Zeughrabdotus are sensitive calcareous nannofossils because they are more susceptible to dissolution and cannot be surely used to define this paleobiogeography and biostratigraphic range.


INTRODUCTION
The Araripe Basin and the Romualdo Formation have been the focus of many taxonomic, biostratigraphic, paleoenvironmental, and paleogeographic studies that have aimed to understand the composition of the fossil communities and marine incursions in the interior of northeastern Brazil during the Early Cretaceous (Arai et al. 1994, Arai 2014, 2016;Araripe et al. 2021, Araripe et al. 2022, Assine et al. 2014, Assine et al. 2016, Barreto et al. 2022, Beurlen 1963, 1966, Mabesoone et al. 1999, Prado et al. 2015, Valença et al. 2003).
Many microfossil groups from the Romualdo Formation have been well studied, as well as those from other nearby units (Antonietto et al. 2012, Arai 2014, 2016, Araripe et al. 2021, Coimbra et al. 2002, Melo et al. 2020, Rios-Netto et al. 2012).However, the first record of calcareous nannofossils from this formation and from the Araripe Basin was reported by Araripe et al. (2022).Our study details and records new species of this fossil group recovered in the PE-01-SA section (Araripe et al. 2022) and in two more distinct outcrops (PE-02-CD and PE-03-ZG), all located in the south-central Calcareous nannofossils, biostratigraphy, and paleobiogeography of the Aptian/Albian Romualdo Formation in the Araripe Basin, North-Eastern Brazil region of the basin in the municipality of Exu, Pernambuco (Fig. 1).The occurrence and detailed analysis of calcareous nannofossils provide valuable taxonomic, biostratigraphic, and paleogeographic information that sheds new light on the paleoenvironments of the Lower Cretaceous Romualdo Formation.The recent discovery of calcareous nannofossils in the Romualdo Formation has stimulated new discussions and studies with an emphasis on microfossils and shows that this formation lacks index fossils for high-resolution biostratigraphic dating.

GEOLOGICAL SETTINGS
The evolution of the interior basins in northeastern Brazil is directly related to the fragmentation process of the Gondwana Supercontinent during the Mesozoic, which culminated in the installation of the South Atlantic Ocean (Matos 1992).Records of the sequences that precede and follow this rupture phase have been observed in the Araripe Basin, located between the states of Pernambuco, Piauí, and Ceará (Fig. 1).The Romualdo Formation is the uppermost unit of the Santana Group, recognized in the Post-Rift I phase (Assine 2007) of the stratigraphic basin sequence (Fig. 1).
For a long time, the deposition of the Santana Group was related to lacustrine and fluvial paleoenvironments, with the exception of the Romualdo Formation, where marine incursions are marked by the occurrence of typical marine fossils (Arai et al. 1994, Arai, 2014, 2016, Araripe et al. 2022, Assine 1992, 1994, Assine et al. 2016).This suggests a shallow marine storm-dominated environment (Custódio et al. 2017).However, new paleoenvironmental interpretations have been proposed for the Araripe Basin.Arai (2014) recorded microforaminifers in the Crato Formation.Also, Goldberg et al. (2019) found marine palynomorphs and microforaminifers, and Fauth et al. (2022) observed microfossils and ichnofossils, both studies interpreted as related to marine ingressions in the Crato and Barbalha formations, respectively.Sedimentological interpretations suggest that the deposition of conglomerates and sandstones occurred in coastal environments, while the dark shales are interpreted because of marine ingressions (Custódio et al. 2017).
The Romualdo Formation is characterized by marls and calcareous fossiliferous carbonate concretions, interspersed with shales, and often bearing gastropods, bivalves, and shrimps.Gastropod shell beds are very common at some points in the basin.The top of the Romualdo Formation is marked by bioclast concentrations, fine to coarse sandstone with trough crossbedding, ripples, and conglomerates (Chagas 2006, Custódio et al. 2017, Rodrigues et al. 2020, 2022) (Fig. 2).This formation overlies the evaporitic sequence of the Ipubi Formation and is unconformably overlain by alluvial sequences of the Araripina and Exu formations (Assine 2007, Assine et al. 2014, Martill 2007).
During the deposition of the Romualdo Formation, estimated to have occurred from Late Aptian to Early Albian, undisputed marine strata were deposited in the interior basins in northeastern Brazil, mainly indicated by its fossiliferous content (Arai and Assine 2020, Araripe et al. 2022, Barreto et al. 2022).

MATERIALS AND METHODS
Sample processing and analysis of calcareous nannofossils were performed in the Laboratório de Paleontologia
Five distinct methodologies were used to prepare each sample.These included decanting (Antunes 1997), decanting (mod.)(Antunes 1997), smear (Smear Slide, Bown 1998), centrifugation, performed at 1,000 r.p.m. for 15 s (short centrifuging, Brown and Young 1997), and ultra-thin section preparation (Bottini 2010).After processing, the fossil content of each slide was investigated using a polarized ZEISS Axion Vision Imager A.2 light microscope (100× objective) with an AxioCam MRc attached; the photomicrographs were produced using ZEN 3.4 Blue edition.Scanning electronic microscope (SEM) images were taken at the Programa de Pós-Graduação em Ciências dos Materiais (PGMTR -UFPE) using Tescan Mira3.A total of 110 slides were prepared for the PE-01-SA section, 150 for PE-02-CD, and 125 for PE-03-ZG.All the analyzed slides were deposited in the Scientific Collection of Microfossils of the Geology Department, Technology and Geosciences Center at the Universidade Federal de Pernambuco (DGEO-CTG-UFPE).Due to the absence of calcareous nannofossil records in the Romualdo Formation before Araripe et al. (2022), sample preparation was performed in a more detailed manner, using five distinct methodologies with the aim of identifying and excluding any possible loss and/or non-identification of species in the studied material.
For qualitative calcareous nannofossil analysis, we observed the slides prepared using the five described methods, and taxa identification was based on the taxonomy from Perch-Nielsen (1985), Bown et al. (1988), Burnett (1998), and Nannotax3 (Young et al. 2017).The quantitative analysis was only performed on the decanted (mod.)slides (Antunes 1997).For this quantification, the following criteria were adopted: abundance, classified as common (C) if one or more specimens were observed in each field of view of each slide; few (F) if, on average, a specimen could not be observed in 10 fields of each slide; and rare (R) if a specimen could be seen less than 10 times in all the slides.Preservation (P) was a subjective category that considered the state of the calcareous nannofossils registered in each sample.In general, preservation was classified as Poor (P) -broken specimens, without primary morphological characteristics; Moderate (M) -whole and broken specimens with alterations in primary morphological characteristics; and Good (G) -all specimens whole, with primary morphological characteristics and easy identification.Total species richness (TSR) was related to the total number of taxa registered in each sample (minimum value = 1; maximum value = 14).TSR should not be confused with diversity.The former only aims to estimate the total number of registered species, while the latter also considers the percentage that each taxon occupies in a sample.
In this study, we applied the most widely used biostratigraphic frameworks.Several calcareous nannofossil biozones have been previously proposed for the Cretaceous, such as Sissingh's (1977;CC zones) biozones.These biozones are based on cosmopolitan data including European and North African sections.In addition, the Roth's (1978; NC zones) biozone was established in the low-latitude region of the northwestern Atlantic Ocean (Burnett 1998).
Furthermore, faciological analyses were made from the three studied outcrops and correlated with the sedimentary facies described by Custódio et al. (2017) due to lithological similarities and macrofossils.
In the PE-01-SA section, the more favorable levels for the recovery of calcareous nannofossils occur in the inner shelf facies (FA-3) at the upper part of the section, in particular in the limestone levels, which present a greater abundance and richness of this group.The shale and siltstone levels are less fossiliferous.For section PE-02-CD, calcareous nannofossils were recovered from the limestone and shell bed (FA-5), but the levels composed of shale and siltstone present a higher richness and abundance.In the PE-03-ZG section, samples of calcareous nannofossils are only recorded at the top of the section, in limestone and shell beds from the storm-dominated facies (FA-5).The three more fossiliferous levels of this outcrop present an increase in abundance and diversity at the top of the section (Table 1).
In this study, the lithostratigraphy and facies correlation suggest that the marine ingressions evidenced in the sections PE-02-CD and PE-03-ZG are contemporary (FA-5), whereas the marine ingression recorded in the PE-01-SA section is more recent (FA-3).

Calcareous nannofossils
The first record of calcareous nannofossils from the Romualdo Formation was described for the PE-01-SA outcrop 4/13  by Araripe et al. (2022).However, in this study, new species are described from the outcrop PE-01-SA (Braarudosphaera ex.gr.B. africana, Braarudosphaera sp., Calculites sp., Discorhabdus ignotus, and Zeughrabdotus erectus), and additional calcareous nannofossils are also recovered from two new outcrops nearby the Exu area.The associations are not as rich as those recorded for PE-01-SA.However, there is a well-preserved association with less diverse and more abundant species richness.Among the slide analyses and descriptions, better results were obtained using only three methodologies (smear, decanting, and modified decanting).

Biostratigraphy
The base of the CC8 biozone is defined by the first occurrence (FO) of Prediscosphaera columnata, while the top is marked by the FO of Eiffelithus turriseiffelli and indicates the base of the Albian (Sissingh 1977).The FO of Hayesites albiensis defines the beginning of the NC8b biozone (Bralower andMutterlose 1995, Roth 1978), which corresponds to the base of the CC8 biozone (Sissingh 1977).Therefore, the presence of H. albiensis after P. columnata is also recognized as a marker of the Albian age.
Kennedy et al. (2017) described a Hayesites albiensis/ irregularis association in the CC7 biozone, in the Vocontian Basin (France), since they had difficulty in distinguishing these two species in the studied sections.However, Bruno et al. (2020) recorded both species individually in the Kwanza Basin (Angola), and Silva Jr. et al. (2020) recorded Hayesites albiensis specimens in the CC8 biozone in the Sergipe-Alagoas Basin.The occurrence of Hayesites albiensis in the 5.55 m sample from the PE-01-SA section suggests the beginning of the Albian (CC8/NC8b biozone) (Araripe et al. 2022).
In the PE-02-CD section, the described association was composed of Biscutum constans, Biscutum sp., Hayesites sp., Nannoconus sp., and Thoracosphaera sp., which can be observed at the highest levels of the section, at depths of 17.5,17.9,18,19,and 22 m (Fig. 5).Specimens of the genus Nannoconus were observed both from a lateral and basal view, preventing a secure identification at species level.The presence of the genus Hayesites within this association suggests an Aptian to Albian age, where the FO and last occurrence (LO) of this genus occur.
In the PE-03-ZG, the species Nannoconus bucheri, Nannoconus sp., Thoracosphaera sp., Watznaueria barnesiae, and Watznaueria sp. were recorded at the top of the section.Due to the absence of short temporal amplitude biostratigraphic markers, the presence of Nannoconus bucheri within the nannofossiliferous assemblage described suggests an Aptian age for the top of the outcrop (CC7 biozone, Fig. 5).

Paleoenvironmental and paleobiogeographic interpretations
Previously, Araripe et al. (2022) studied the PE-01-SA section and used biostratigraphic markers (FO Hayesites albiensis and LO of the foraminifera Hedbergella aptiana) to indicate the Aptian/Albian boundary in the section and concluded that this outcrop may represent the upper portion of the Romualdo Formation.Barreto et al. (2022) studied the same section, and the absolute dating of U/Pb in fish teeth (110.5±7.4Ma) showed the Albian age, which may be extended to the Upper Aptian.
Considering the lithostratigraphy and facies correlation, it can be defined that the marine ingressions occurred in the sections PE-02-CD and PE-03-ZG are contemporary, whereas the marine ingression recorded in the PE-01-SA section is more recent.
Calcareous nannofossil species are typically widespread across a range of marine photic zone environments, but in some cases, more specific paleoecologies can be determined.These ecological preferences are usually determined using paleobiogeographic distribution analysis and by comparison with other paleontological and geochemical environmental proxies.The increase in diversity and abundance of calcareous nannofossils suggests a distal marine environment (Wise 1983, 1988, Bown 1998, Street and Bown 2000, Kanungo 2005, McAnena et al. 2013).

Marine ingression: Aptian
The marine ingression is evidenced in PE-02-CD and PE-03-ZG and is correlated with the FA-5 facies (storm-dominated marine), and it has been interpreted as a shallow marine environment characterized by warm surface water temperatures (Hayesites sp., Nannoconus bucheri, Nannoconus sp., and Watznaueria barnesiae) and a fertility index ranging from high (Biscutum constans, Biscutum sp.) to low (Watznaueria barnesiae).
The Albian marine ingression is marked by a higher diversity and abundance of calcareous nannofossils, suggesting a more distal marine environment than the Aptian marine ingression.
Hayesites albiensis seems to be mainly restricted to northern Africa (Bralower 1992)

CONCLUSION
The calcareous nannofossil association is characterized by 11 distinct genera and 17 species.This taxon's richness varies from 45 to 3 individuals; preservation is moderate; and abundance varies from rare to few.The calcareous nannofossils were recognized in the inner shelf facies, limestone, and shell bed levels.9/13 • The Romualdo Formation is characterized by marine ingressions in the Aptian and Albian, as highlighted in this study by the calcareous nannofossils and sedimentary facies; • The recorded assemblage in the studied outcrops has a strong Tethyan affinity, with the genera Hayesites and Nannoconus standing out.But the calcareous nannofossil assemblage also includes more resistant, cosmopolitan, and/or opportunistic species (Watznaueria, Thoracosphaera, and Braarudosphaera).

Figure 1 .
Figure 1.Map of the Araripe Basin, highlighting the location of the studied outcrops PE-01-SA, PE-02-CD, and PE-03-ZG in the Romualdo Formation.
and southern England, which may be a possible reflection of the Tethyan provincialism demonstrated by this species ( Jeremiah 2001).Pedrosa et al. (2019) and Silva Jr. et al. (2020) also observed a Tethyan affinity in the Sergipe-Alagoas Basin based on the occurrence of H. albiensis and Nannoconus spp.Araripe et al. (2022) endorsed the Tethyan influence with the occurrence of Hayesites spp.and Nannoconus spp.In this study, the presence of calcareous nannofossils in the outcrops PE-01-SA, PE-02-CD, and PE-03-ZG suggests the record of marine incursions in the Araripe Basin, and the presence of Hayesites, Nannoconus, and Rhagodiscus indicates a strong influence of Tethyan origin in the Central-West portion of the Araripe Basin (Fig. 6).

Figure 6 .
Figure 6.Paleogeographic reconstruction for Lower Cretaceous, highlights (blue) the Tethys Sea and its influence on the Araripe Basin.Modified from the map shown in Street and Bown map (2000).