Tafonomy of macroinvertebrates and Albian marine ingression as recorded by the Romualdo Formation ( Cretaceous , Araripe Basin , Brazil )

Manuscript ID: 20180048. Received on: 04/24/2018. Approved on: 06/29/2018. ABSTRACT: The Romualdo Formation, Araripe Basin, crops out in the municipality of Exu, Pernambuco State, exposing coquinas. Fauna survey, taphonomic analysis of the macrobenthos, and identification of sedimentary facies of the outcrop were carried out to contribute to paleoenvironmental understanding of the Romualdo Formation. The association of molluscs (Cerithium sp., Tylostoma ranchariensis, Aguileria dissita, Brachidontes araripensis and unidentified cassiopids) and echinoids of the species Bothryopneustes araripensis suggests sedimentation in the marine environment. The taphonomic similarities made possible the grouping of coquinas into two types. Coquinas type 1 exhibit characteristics of transport and reworking of bioclast generated by storms in proximal setting. Coquinas type 2 demonstrates echinoids in situ and articulated with spines connected to shells, suggesting a fast sedimentation by distal tempestite. Regarding sedimentary facies, the concentrations of invertebrates would have been formed in the transitional offshore zone of siliclastic platform. The results presented here evidence a broader distribution of echinoids and expand the geographic limits of the shallow marine environment in the Romualdo Formation.


INTRODUCTION
Taphonomic analysis based on concentrations formed by molluscs and echinoids has frequently been used to aid in the interpretation of paleoenvironment and fossilization processes (García andAguirre 2004, Olóriz et al. 2008).This fact is due to the predominance of molluscs in most fossil associations (Staff and Powell 1988), and echinoids, given the structure of their multi-articulated skeleton, are considered good indicators of biostratinomic processes (Nebelsick 1999b).
Toward the top of the Romualdo Formation, there are different limestone and calciferous sandstones strata, mostly forming coquinas, which occur widespread in the Araripe Basin and can reach one meter in thickness (Sales 2005, Assine et al., 2014).These shell-rich rocks are formed by marine molluscs and echinoderms, cleary suggesting a marine ingression in the basin (Beurlen 1966, 1971, Assine 1992, 2007, Sales 2005, Assine et al. 2014).
Coquinas in the Romualdo Formation were taphonomically identified as being a result of storm wave's action in shallow marine environment (Sales 2005).However, most of the studied coquinas were from the state of Ceará, and are exclusively formed by molluscs (Sales 2005, Prado et al. 2014, Batista et al. 2015).Echinoid-bearing coquinas had only been found in the west border of the basin, Araripina county, Pernambuco State, Brazil (Beurlen 1966, Prado et al. 2015, 2016) (Fig. 1).Taphonomic studies classified them as proximal tempestite and obrution deposits (sensu Brett 1995) formed in the marine environment (Sales 2005, Prado et al. 2015, 2016).On the other hand, sedimentological studies interpreted coquinas as residual lags originated above ravine surface and analyzed as a stratigraphic framework (Assine 2007).
The new outcrop on the Cedro site, Exu county, Pernambuco State, has the most complete record of echinoids in the Araripe Basin so far, considering its abundance of fossil at various intervals in the sedimentary succession and distinct stages of disarticulation preserved.Taphonomic analyses, faunal survey and sedimentary facies analysis were performed to contribute to the interpretation of the Albian transgression in the Araripe sedimentary Basin.

The Araripe Sedimentary Basin and the Romualdo Formation
The Araripe Basin is in northeastern Brazil, covering the boundary zones between the states of Pernambuco, Piauí, and Ceará (38º30' to 40º55'W -7º07' to 7º49'S).It is an inverted intracontinental graben originated during the Mesozoic over a Paleozoic intracratonic syneclises, and records pre-rift, rift and post-rift (I and II) strata formed mainly by fluvial and lacustrine strata (Assine 2007, Marques et al. 2014) (Figs. 1 and 2).
According to Custódio et al. (2017), the Romualdo Formation comprises transgressive and highstand system tracts.The coastal alluvial and tide-dominated facies represents the transgressive systems tract, the marine black shales corresponding to the maximum flooding zone, and the shell beds record brief transgressive events during stillstand phases.
It should be noted that the maximum flood surface has already been reported by Assine (2007) for the coquina level.
The Romualdo Formation crops out in the municipality of Exu (Pernambuco State, Brazil) showing strata of shales with limestone concretions followed by bioclastic-rich limestones which contain the macroinvertebrates.

MATERIALS AND METHODS
Sedimentary and taphonomic data of the Romualdo Formation were acquired from a 5,5 m thick section outcropping at the Cedro site, Exu county (UTM N 0434996, E 9172325), located about 100 km from Araripina, Pernambuco State (Fig. 1).The levels of rocks that contained the macroinvertebrates had their base and top marked.
About 34 samples were collected and deposited in the Palaeontology Collection of the Geology Department (DGEO), Center of Technology and Geosciences (CTG), at Federal University of Pernambuco (UFPE), Pernambuco, Brazil.In the laboratory, a mean of 120 bioclasts (≥ 2 mm) was analyzed in each skeletal accumulation, as proposed by Kidwell et al. (2001), to obtain reliable taphonomic results.
Regarding paleoecological features, life habits, composition (whenever possible, specimens were identified taxonomically to species or genus level) and relative abundance of the taxa were observed, considering as few abundant, abundant and very abundant those that represented < 20%, ≥ 20 and ≤ 80%, and > 80% of the fossil associations, respectively.Regarding the stratigraphic features, the thickness and stratigraphic contacts of the strata were analyzed.The genetic classification of the concentrations was performed according to Fürsich and Oschmann (1993).
At the Cedro site, the Romualdo Formation shows a succession of fossil-bearing shales (mainly fish remains and plant fossils in calcareous nodules -facies F1) interfingered by sandstone strata with planar and climbing ripple laminations (facies Sh and Sp), and thin layers of coquinas (Cq), labeled Layers of Cedro-LCE.Fifteen layers of calciferous sandstone (LCE1-LCE15) were observed.These layers are limited at the base by abrupt contacts, sometimes with incipient wavy truncated laminations (LCE1, LCE4, LCE5), intercalated with layers of laminated mudstones (Fml) or shales (Fl), apparently non-fossiliferous in LCE1-LCE5 and LCE6-LCE14 (Fig. 3).

Survey of Macrobenthos
Macroinvertebrates form fossiliferous concentrations in all layers, except in LCE11, which has a single unidentified closed articulated bivalve.Since samples with less than 20 specimens are not reliable to determine taphonomic  signatures in single taxa assemblages (Kidwell et al. 2001), LCE11 has not been considered for analysis.
Brachidontes araripensis is abundant in all layers and only becomes less abundant in LCE4 and LCE5, in which echinoids are very abundant.Echinoids occur in all layers, except in LCE1 and LCE6, in which the species Tylostoma ranchariensis and Brachidontes araripensis are abundant.Cerithium sp.occurs where echinoids are predominant and are less abundant in LCE4 and LCE5, but abundant in LCE15.Cassiopids are less abundant, and Aguileria dissita ranges from less abundant to abundant along the layers (Fig. 3).

Taphonomic data
The shell-beds show high levels of fragmentation and or disarticulation, except the gastropods present in LCE1, LCE2, LCE7 and LCE8 (Fig. 3).The coquinas have low abrasion and no sign of bioerosion or corrosion.Bioclast orientation is concordant and polymodal regarding bedding plans, with concavities facing both upwards and downwards.Chaotic distribution, as displayed by vertical sections, is less frequent.
There is a predominance of fragmented individuals in the layers where echinoids occur (stages 3 and or 4).Stages 1 and 2 occur mainly in type 2 coquina (Fig. 3), sometimes

Laminated Shale
Light gray to whitish gray shales, laminated, layered with lateral continuity and centimetric thickness, with horizontal lamination and expressive scattered fossil content.There is often the occurrence of centimetric to decimetric discoidal calcareous concretions in the fossils, rich in remains of plants and fish.
Decanting of clays in calm waters.The light coloring suggests oxidizing conditions at the depositional site.Fall-out deposits.

Laminated mudstones
Laminated mudstones laterally persistent in succession with up to 1 m thick.Features light gray to whitish color and light tints (cream, yellow) when altered.It is common the presence of carbonate nodules and discoidal calcareous concretions associated or not to the presence of fossil.Remains of fish (scales, teeth, and bones), coprolites, mollusks and rare plant fragments are common.
Deposition by decantation in calm waters, disoxic or anoxic conditions.Fall-out deposits.

Sm
Massive sandstones Tabular centimetric layers, or lenticular, of very fine to fine calcareous sandstones, well sorted.
Bottom currents associated with storm waves.

Sh Laminated Sandstones
Very fine sandstones, well sorted, light gray to whitish gray color, with horizontal lamination, arranged in centimetric to decimetric tabular layers.
Deposition by bottom currents in plane beds under conditions of upper flow regime.

Planar crossstratification sandstones
Fine sandstones with small and low angle planar crossstratification, arranged in decimetric tabular layers.Color is light gray to whitish.
Migrating forms of subaqueous beds of sinuous crest due to continued action of unidirectional currents.

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Brazilian Journal of Geology, 48(3): 519-531, September 2018 New marine shell beds from the Lower Cretaceous of Brazil  with spines attached to the shells, predominating those with the concavity facing upwards.

DISCUSSION
Unlike the outcrops located in the eastern border of Araripe Basin analyzed by Custódio et al. (2017) to identify transgressive and highstand tracts of the Romualdo Formation, on Cedro site the concretions-bearing shale occurs not only below the coquinas, but between them.Facies of shales and mudstones in most of the studied outcrop indicate an environment with a predominance of sedimentation under low-energy condition.The presence of marine fish (e.g.Lepidotes, Vinctifer, Cladocyclus and Rhinobatus) in the limestone concretions in these facies suggests the existence of a seaway between Araripe Basin and the open marine environment, which allowed these organisms to migrate to the area (Silva Santos & Valença 1968, Martill 1988, 2007, Assine 2007, Assine et al. 2014).
The Brachidontes araripensis occurs in all coquinas, indicating these organisms were highly adapted to local environmental conditions, perhaps because this species could tolerate variations in salinity as well as the living species of this genus (Terranova et al. 2007).However, the other identified taxa occur in marine waters (Wenz 1938, Stephenson 1952, Morter 1984, Hessel & Junior 1989, Cleevely & Morris 1988, Sälgeback & Savazzi 2006), indicating that, although there were variations in salinity, it would still be sufficient for the establishment of benthic marine communities with echinoids (Bothryopneustes araripensis), which are found in most of the coquinas.
Although coquinas are similar regarding their taxonomic composition, they differ in the abundance of groups.Thus, overtime, the environment would have maintained the abiotic conditions necessary for the establishment of a fauna with possible salinity variations that would favor the predominance of certain groups, as it has been already observed in previous studies (Pereira et al. 2015, Prado et al. 2016).
The species identified in the Cedro outcrop have an epifaunal and or semi-infaunal mode of life, i.e., they have a lower preservation potential in comparison with infaunal individuals.That is because they remain longer on the sediment-water interface and are more easily exposed to the turbulence of the environment in low sedimentation rate conditions, usually predominant in the day-to-day (Kidwell 1986, Best & Kidwell 2000), justifying the high index of fragmentation in the coquinas on the Cedro site.Preservation of the organism is also directly influenced by its skeletal type (Speyer & Brett 1988).Fragmentation and disarticulation is high in all taxonomic groups, especially in the echinoids (stages 3 and 4), because the structure of their multi-element skeleton (sensu Speyer & Brett 1988) is more susceptible to disarticulation, occurring from within a few hours up to a few days (Schäfer 1972).The exceptions are the gastropods, which due to their univalve skeleton and absence of ligament tissue are physically more resistant hence more frequently preserved (Speyer & Brett 1988).
The disarticulation and fragmentation seems to be more related to the high energy of the environment than to biological or chemical processes since it is observed in all taxonomic groups and because there are no signs of corrosion and bioerosion.The absence of corrosion and bioerosion also suggests that the individuals remained for a short time exposed to the water-sediment interface, being rapidly buried after dying (Davies et al. 1989).
The degree of packing ranges from dispersed to dense, suggesting there would be variations in the hydraulic selection of the matrix or in the availability of bioclasts (Kidwell et al. 1986, Holz & Simões 2002, Schmidt-Neto et al. 2014).

Genetic classification of the concentrations
According to Aigner and Reineck (1982) and Aigner (1985), sedimentary records in siliciclastic platforms are controlled mainly by tempestite events.However, even though they are formed by the same type of event, the fossiliferous concentrations have peculiar taphonomic features along the shallow to deep-water gradient (Fürsich & Oschmann 1993).
Coquinas type 1 has characteristics of bioclastic transport and reworking through storm waves, such as the presence of well-selected bioclasts and nested valves (Allen 1990, Kidwell Table 2. Main taphonomic features of coquinas type 1 and 2 and their interpretations.

Taphonomic signatures Interpretation
Type 1 High levels of fragmentation and or disarticulation, low abrasion and bioerosion and corrosion absent.Good sorted and loose to dense packed fossil assemblage.Bioclast orientation on bedding plans is concordant and polymodal, with the concavities facing both upwards and downwards.In cross section, chaotic distribution is less frequent.Presence of nesting of bivalves.
Transport and reworking of bioclastic through storm waves in proximal setting of transitional offshore zone.
Type 2 High levels of fragmentation and or disarticulation, low abrasion and abrasion and bioerosion and corrosion absent.Poor sorted and loose to disperse packed fossil assemblage.Bioclast orientation on bedding plans is concordant and polymodal, with the concavities facing both upwards and downwards.In cross section, chaotic distribution is less frequent.Presence of articulated echinoids with spines attached to the shells.
Rapid sedimentation of echinoids in situ by storms in more distal setting of transitional offshore zone.
& Bosence 1991).Because they present a typical transport biofabric with few signs of abrasion, these coquinas would have been formed by para-autochthonous and allochthonous individuals through short-term currents such as those generated by storm in proximal settings (Fig. 7) (Simões et al. 2000, Fürsich & Oschmann 1993).The absence of any sedimentary structure that could indicate the action of storm events is justified possibly due to the high availability of bioclasts that would have obliterated the sedimentary record.For bioclastic concentrations in storm-influenced shelf environments, Kidwell & Bosence (1991) estimate a time-averaging ranging from a few decades to a few thousands of years.
In coquinas Type 2, the transport seems to have been less significant as suggested, for example, by the poor selection of bioclasts and preservation of several whole specimens.The presence of articulated concave-upwards echinoid shells (stages 1 and 2) with the concavity facing upward, sometimes with spines, indicates that a rapid sedimentation process buried the echinoid still alive in situ (obrution deposits), representing the best evidence of autochthony.The few signs of abrasion indicate that coquinas were formed in areas of low hydrodynamic energy, and the stability of the bottom of this area was only altered by episodic events, i.e. storms (Schmidt-Neto et al. 2014).
Obrution deposits are generated from sudden sedimentological events, of which identification is facilitated by the presence of well-preserved epifaunal benthic organisms (Brett 1995).This type of fossil association is most often identified at the final transgressive stage or at the beginning of the highstand deposits (Brett & Seilacher 1991), and corresponds to what Kidwell and Bosence (1991) denominate census assemblages, which is the type of fossil accumulation most similar to the original communities, with no time-averaging or time-averaging ranging from days to hundreds of years (Kidwell & Bosence 1991, Kidwell 1997)  the platform (Fig. 7), due to the decrease of turbidity currents that settle the suspended sediment (Brett et al. 1986, 1997, Donovan 1991, Walker & Plint 1992).In fact, the echinoid Bothryopneustes araripensis identified in the Type 2 coquinas has also been interpreted as typical of low energy marine environments (Manso & Hessel 2012).
Sedimentation in the bioclastic sandstone seems to have occurred in an offshore-transition zone due to the sandy granulometry and the presence of sedimentary structures related to storm events, such as truncated laminations, usually preserved in these areas (Reading & Collinson 1996).Moreover, a better preservation of regular echinoids is also expected in the transition zone, where there would be less physical and biological reworking (Kidwell & Baumiller 1990).
In coquinas Type 2, articulated echinoid shells are also found, not in a life position (concavity facing downwards).According to Brett et al. (1997), echinoids can be transported still articulated in few hours after their death.Fragments in these coquinas indicate the influence of mixed taphonomic processes, related to energy events that would have carried remains of fossil from other areas and incorporated them into the bottom sediment for longer periods (Speyer & Brett 1991, Reid et al. 2015).Therefore, part of the fauna preserved in these coquinas would have represented para-autochthonous and or allochthonous individuals.Nebelsick (1999a) observed that the radial fissure in sand dollars (an irregular echinoid of the order Clypeasteroida) resulted from the sediment load on the fossil shells.Postdepositional changes of this type may also be related to the preservation of radially collapsed and cracked echinoids in the coquinas Type 2, as already suggested by Sales (2005).

CONCLUSION
The facies and fossils in the Romualdo Formation on the Cedro site indicate an environment with marine influence and predominantly calm sedimentation, represented by shales/mudstones with fossils of fish and vegetables, sometimes interrupted by tempestite sedimentation forming coquinas.The sedimentation of macrobenthos seems to have occurred in a transitional offshore marine environment, sometimes influenced by proximal storms, with coquinas exhibiting a transport biofabric and sometimes by more distal storms, representing the best evidence of in situ preservation of echinoids in the area.
The new occurrence of autochthonous echinoids in the municipality of Exu, Pernambuco, confirms the marine entry into Araripe and expands its paleogeographic boundaries to the west.

Figure 1 .
Figure 1.Location of echinoids-bearing coquinas in the Araripe Basin, northeast Brazil.The squares represent echinoid occurrences reported in previous studies, and the star shows the new occurrence on the Cedro site in Exu, Pernambuco State.

Figure 2 .
Figure 2. Stratigraphic chart of the Araripe Basin with emphasis on the Romualdo Formation, Post-rift I Megasequence.
sandstone facies with planar cross-stratification (Sp facies), horizontal lamination (Sh facies) and structureless (Sm facies) are related to the action of unidirectional currents, deposition by bottom currents under upper flow regime and bottom currents associated with storm waves, respectively.This facies association is typically for wave-influenced coastal environments (Walker & Plint 1992, James & Dalrymple 2010).The association of mudstones and bioclastic sandstones with incipient wavy truncated laminations indicates sedimentation in the offshore transition zone of siliclastic platforms (i.e., below the base level of fair weather waves and above the base level of storm waves; Reading & Collinson 1996, James & Dalrymple 2010, Mancosu et al. 2015, Horodyski et al. 2014) (Fig. 7).

Figure 7 .
Figure 7. Shoreface-offshore marine profile.Note the distribution of coquinas type 1 and 2 in the transitional offshore zone.

Table 1 .
Sedimentary facies of the Romualdo Formation in the study area.