Paleoenvironmental significance of Benthic Foraminifera and Ostracoda from the late Quaternary of the Ceará Basin, Brazilian Equatorial Margin

Abstract Benthic foraminifera, ostracods and pteropods are reliable paleoenvironmental indicators in Quaternary deposits. However, in the Ceará Basin, on the Brazilian Equatorial Margin, these microfossils are poorly studied. This paper investigates environmental changes during the Pleistocene–Holocene transition in the Icaraí subbasin based on micropaleontological analysis of the core ANP 1011. Seventy-four taxa of benthic foraminifera, represented predominantly by Globocassidulina, Uvigerina, Pyrgo and Melonis, have been identified. The ostracod assemblages are composed mainly by the families Macrocyprididae, Cytheruridae, Trachyleberididae, Pontocyprididae and Krithidae, of which the genus Krithe was the most abundant. The composition of the ostracod assemblages identified in this study area differs somewhat from other regions of the Brazilian Margin. The assemblages of foraminifera and ostracod characterize a typical bathyal paleoenvironment. The occurrence of pteropods and dominance of epifaunal foraminifera taxa, mainly Pyrgo sp. and Miliolinella sp. in the lower portion of the core (Pleistocene), indicates higher phytodetritus input and oxygen concentration. A conspicuous environmental change was observed in the upper portion of the core, which corresponds to the Holocene, where the increase of infaunal foraminifera (e.g., Uvigerina, Globocassidulina and Melonis) suggests reduction in the organic matter input and, probably, increased bacterial density and depletion in dissolved oxygen in the sediment.


INTRODUCTION
Ecological studies using benthic foraminifera and ostracods are important for understanding present environments and interpreting past oceanic conditions (Morigi et al. 2001, Yasuhara et al. 2017, Bergue et al. 2021, De Almeida et al. 2022).Due to their adaptive potential, benthic foraminifera are spread in a variety of environments such as estuaries, lagoons and even extreme ecosystems such as abyssal plains and subduction zones (Murray 1991(Murray , 2001)).Benthic foraminifera can be differentiated by microhabitats in epifaunal, which live in the upper 1 cm of sediment, and infaunal, which burrow into soft sediment below 1 cm of the sediment (Corliss and Chen 1988, Corliss 1991, Murray 1991, Jorissen et al. 1995).Significant changes in diversity and abundance of benthic foraminifera are recorded worldwide in response to hydrological changes linked to glacial-interglacial cycles (Schnitker 1980, Lukashira andBashirova 2015) and their influence on productivity (Schmiedl andMackensen 1997, Ohkushi et al. 1999).
The distribution of deep-sea benthic foraminifera in the sediment is controlled by several factors, mainly the organic flux to the ocean floor (its quantity, quality and periodicity) and bottom water oxygenation (Fontanier et al. 2002, 2003, Hayward et al. 2002, Gooday et al. 2010, Murray 2001, Jorissen et al. 2007).In the deepest part of ocean basins, where strongly oligotrophic conditions prevail, the corrosiveness of the bottom waters (highest in the Antarctic Bottom Water [AABW]) may control the distribution of cosmopolitan taxa (Mackensen et al. 1995, Schmiedl et al. 1997, Jorissen et al. 2007).
Ostracods are microcrustaceans with a bivalve chitin-calcitic carapace and an abundant fossil record in both nonmarine and marine depositional sequences (Rodriguez-Lazaro and Ruiz-Muñoz 2012).As they are sensitive to changes in environmental parameters (e.g., temperature, salinity and productivity), ostracods are considered reliable paleoecological indicators (Armstrong andBrasier 2005, Rodriguez-Lazaro andRuiz-Muñoz 2012).Although taxonomic analysis provides essential data for the characterization of depositional environments, more Paleoenvironmental significance of Benthic Foraminifera and Ostracoda from the late Quaternary of the Ceará Basin, Brazilian Equatorial Margin accurate ecological interpretation also demands to differentiate autochthonous from allochthonous carapaces (van Harten 1986, Whatley 1988, Zhou and Zhao 1999, Boomer et al. 2003).
Despite their paleoceanographic potential, studies on bathyal Quaternary calcareous microfossils in the Brazilian Equatorial Margin are still scarce.The main objective of this work was to study benthic foraminifera, ostracods and pteropods from a sediment core from the offshore portion of the Ceará Basin during the Pleistocene-Holocene transition to reconstruct the environmental changes at this site.

STUDY AREA
The study area is part of the Icaraí subbasin (Ceará Basin), which lies between the Acaraú and Mundaú subbasins (Fig. 1).It is separated from the Mundaú subbasin by the Forquilha fault and from the Acaraú subbasin by the northern extension of the Transbrasiliano lineament (Antunes et al. 2008).
Surface waters of the Equatorial Atlantic Ocean are presently influenced by the North Brazilian Current (NBC), the North Equatorial Sub-Current, the North Equatorial Counter-Current and the North Equatorial Current (Silveira et al. 2004).The NBC stems from the bifurcation of the southern branch of the South Equatorial Current when it reaches the Brazilian Continental Margin, between 10°S and 15°S (Schott et al. 2004, Talley 2011).According to Johns et al. (1998), the mobility of NBC coincides with changes in surface transport, associated with the wind shear in the tropical Atlantic and the seasonal migration of the ITCZ.The NBC is the largest surface flow component of the Atlantic meridional overturning circulation, through the northward surface water transport and the inter-hemispheric oceanic heat exchange (Zhang et al. 2011).
A total of five water masses exert influence in the study area, from the surface to the 2,125 m water depth where the core ANP 1011 was obtained: the Tropical Water (the surface water TW, 0-150 m), the South Atlantic Central Water (the pycnoclinic water SACW, 150-500 m), the Antarctic Intermediate Water (the intermediate water AAIW, 500-1,300 m), the Upper Circumpolar Water (the intermediate water UCPW, 500-1,300 m), and the North Atlantic Deep Water (the deep water NADW, 1,300-3,500 m) (Silveira et al. 2020).The TW presents the highest values of temperature and salinity of the water column (Emilsson 1961).The SACW, near its origin in the tropics, is characterized by the largest variation of temperature and salinity due to its position at the pycnocline level (Tomczak and Godfrey 1994).The AAIW is characterized by the high values of oxygen and low salinity (Reid et al. 1977, Reid 1994).The UCPW presents lower oxygen concentrations and salinity and high dissolved nutrients associated with intense local silicate (Stramma andEngland 1999, Mémery et al. 2000).The NADW is characterized by high values of oxygen and temperature, a secondary salinity maximum and low local levels of nutrients (Maamaatuaiahutapu et al. 1994).Moreover, this water mass is not corrosive to aragonite (Gerhardt et al. 2000).
Sample preparation followed the standard methodology for Quaternary calcareous microfossils adapted from Murray (2006), which consists of washing in tap water on a sieve of 0.062-mm mesh and oven-drying at 60°C.After drying, another sieving on a 0.150-mm mesh was carried out, and from this residue, all the benthic foraminifera, ostracods, and pteropods were collected under a stereomicroscope and stored in micropaleontological slides (see Suppl.Mat.).In line with the objectives of this study, we chose to use only 0.150 mm for all groups studied.According to Cappelli and Austin (2019), the benthic foraminiferal assemblages picked from the large size fraction (> 150 mm) still provide useful information on prevailing environmental conditions and remain useful for an overview of environmental change.Well-preserved specimens of each morphotype were photographed and examined in a scanning electron microscope (SEM) PHENOM XL at Laboratório de Micropaleontologia Aplicada (LMA) of Universidade Federal de Pernambuco (UFPE).
The paleoecological interpretation of benthic foraminifera was based on Boltovskoy andWright (1976), van Morkhoven et al. (1986), Jones (1994), and Murray (1991Murray ( , 2006)), and microhabitats (epifaunal and infaunal) were based on test morphology (Corliss and Chen 1988, Murray 1991, Fontanier et al. 2003, Schweizer 2006).The relative abundance (RA) of benthic foraminifera and ostracods corresponds to the ratio between the number of individuals of a species (N) and the number of individuals of all species in the same sample (T): RA = (N × 100)/T.The RA values are expressed in percentage, and the data obtained were classified as rare (< 5%), common (5-19%), and abundant (> 20%).In addition, the RA for agglutinated, porcelaneous, and hyaline tests of benthic foraminifera was calculated for each sample.Because some samples presented low recovery of specimens, only samples with > 80 specimens were considered in the statistical analyses.The richness of ostracods corresponds to the absolute number of species.
The carbonate content in the samples was obtained through the digestion of approximately 0.5 g of sample in an Erlenmeyer flask with 10 mL of hydrochloric acid (HCl), stirred periodically over 24 h.Then, the supernatant was removed, and the decarbonated sample was washed with distilled water to remove HCl, residues.Later, the sample was oven-dried at 60°C and weighed again.The calcium carbonate content in the sample was calculated through the mass difference before and after decarbonation.To determine the content of organic matter and organic carbon, the method of Walkley (1947), as modified by Loring and Rantala (1992), was adopted.

RESULTS
The analysis of the core ANP 1011 allowed identification of abundant and diversified assemblages of foraminifera (Figs. 2 and  3) and, to a lesser degree, of ostracods (Fig. 4) and pteropods (Fig. 3).The list of the taxa of benthic foraminifera and Ostracoda with their complete names (authors and dates), identified and cited in the present study, can be consulted in Suppl.Mat. 1 and 2.

Carbonate and organic matter content
The carbonate content analysis revealed values between 78.61 and 27.06% (Suppl.Mat.; Fig. 6).The highest values were observed in the middle (90-59 cm), decreasing toward the core top (6-0 cm).Concerning the organic matter content, the analyses revealed values between 0.9 and 2.3%, with an average of 1.4%, with the highest values at 70-67 and 42-39 cm (Fig. 6).Similar variation was observed in organic carbon levels, which ranged from 0.5 to 1.4%, with an average of 0.8%.The highest values also occur in the samples 70-67 and 42-39 cm (Fig. 6).

Foraminifera
The foraminifera assemblages of the core ANP 1011 characterize a typical bathyal paleoenvironment, as indicated by Cibicidoides wuellerstorfi (Schwager, 1866), Melonis pompilioides (Fichtel and Moll, 1798), Globocassidulina subglobosa, and Pyrgo murrhina (Douglas and Heitman 1979, Murray 1991, Rathburn and Corliss 1994).Murgese and De Deckker (2005) argued that the calcareous infaunal rate indicates high carbon influx and low dissolved oxygen, whereas the porcelaneous rate indicates high dissolved oxygen.Most miliolids are sensitive to oxygen depletion (Bernhard and Sen Gupta 1999); however, in deep environments, the vertical distribution of foraminifera is controlled mainly by food availability in oligotrophic settings (e.g., abyssal plains) ( Jorissen et al. 1995).Miliolids are associated with oxygen-rich North Atlantic Deep Water (Peterson and Lohmann 1982).
The linkage of foraminifera's assemblage composition with environmental parameters, such as occurrence, microhabitats, organic carbon flux, and dissolved oxygen (Table 1), allowed the characterization of two environmental settings (Fig. 6).
Species of Quinqueloculina are highly mobile in fine-grained sediments in both shallow (Severin et al. 1982)  waters (Gross 2000).These movements probably respond to the oxygen depletion in deeper layers combined with the presence of labile food at the water-sediment interface (Gooday et al. 2010).Some species migrate upward and downward in response to changes in the thickness of the oxygenated layer associated with the decomposition of organic matter (Ohga andKitazato 1997, Kitazato et al. 2000).

and deep
According to Gooday (2002), the accumulation of phytodetritus on the seabed usually occurs in areas with highly seasonal primary production.Our data demonstrate that epifaunal species are related to higher phytodetritus input and oxygen concentration during the Pleistocene (glacial period).Similar results were obtained by De Almeida et al. (2015) in the Santos Basin and Rodrigues et al. (2018) in the Pelotas Basin, where the phytodetritus influx was higher during the glacial stages than in the interglacial MIS 5.The decrease in infaunal species, calcium carbonate content, and organic carbon in the sample 110-107 cm results probably from the decrease in the availability of organic matter.In the present study, the high RA of porcelaneous foraminifera during the Pleistocene (Biozone Y, sample 122-119 cm) may be related to oxygenation (Murgese and De Deckker 2005).

Environmental setting II
This interval corresponds to Biozone Z (Fig. 6) and is characterized by environmental instability with a tendency to increase (predominance of uvigerinids) or decrease (predominance of cassidulinids) oxygenation.Oxygen concentration and nutrient are highly influential on infaunal assemblages' composition (De Rijk et al. 1999, Jorissen et al. 2007).The increase in infaunal taxa (Uvigerina and Melonis) in the core ANP 1011 in the Pleistocene-Holocene transition indicates higher concentrations of organic carbon and nutrient and lower oxygenation (Miao and Thunell 1993, Gooday 1994, Mackensen et al. 1995, Fontanier et al. 2002, Martins et al. 2006, Murray 2006, Eichler et al. 2008, Nagai et al. 2009).
Higher abundances of Uvigerina peregrina Cushman 1923, Uvigerina auberiana, Uvigerina sp., Melonis barleeanum, and Globocassidulina subglobosa in the core top (Biozone Z) point to increased availability of organic carbon during warm intervals (Gupta and Thomas 2003).According to Lohmann (1978) and Streeter and Shackleton (1979), the presence of Uvigerina is usually congruent with low oxygenation between 2,000 and 4,000 m throughout the Atlantic.Higher Uvigerina percentages have also been observed in areas of high surface productivity and organic carbon-rich sediments (Woodruff and Douglas 1981, Boersma 1986, Lutze 1986, Boyle 1990, Maia et al. 2022).The species Uvigerina peregrina is typical of low-oxygen waters and/or organic-rich sediments in modern oceans (Peterson 1984, Mackensen et al. 1995).The common presence of Uvigerina proboscidea, at the top of the Pleistocene (Suppl.Mat.) in the core ANP 1011, demonstrates higher surface productivity and perhaps higher biogenic sediment accumulation (Kroon et al. 1991, Gupta andSrinivasan 1992).Uvigerina proboscidea is abundant in regions of high productivity in the Atlantic (Thomas et al. 1995), Indian (Gupta andThomas 1999, Almogi-Labin et al. 2008), and Pacific (Woodruff 1985), particularly when the productivity is high throughout the year and food supply presents low or absent seasonality (Ohkushi et al. 1999).In addition, Uvigerina proboscidea characterizes areas of high carbon flux and low dissolved oxygen concentration (Murgese and De Deckker 2005).
High abundances of Melonis barleeanum in both the North (Thomas et al. 1995) and South Atlantic (Schmiedl and Mackensen 1997) characterize high productivity with sustained flow of organic matter.On the contrary, in the Indian Ocean, Melonis barleeanum indicates moderate organic flow with intermediate to high seasonality (Murgese and De Deckker 2005).Table 1.Paleoecological inferences and microhabitat preferences of benthic foraminifera found in the core ANP 1011.

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The increase of the infaunal taxa Globocassidulina in the early Holocene indicates well-oxygenated deep waters with strongly pulsed food supply and good carbonate preservation in oligotrophic environments (Ohkushi et al. 1999, Singh andGupta 2004).The succession of low and high incidences of Globocassidulina subglobosa indicates variations in the intensity of organic matter input, probably in response to climatic and oceanographic changes (Rodrigues et al. 2018).Peterson and Lohmann (1982) related this taxon to the poorly oxygenated circumpolar deep water, while Corliss (1979) found it associated with the AABW in the southwestern Indian Ocean.This taxon is often abundant in regions with low organic matter input and strong bottom currents (Schmiedl et al. 1997, Nees andStruck 1999).According to Noucoucouk et al. (2020Noucoucouk et al. ( , 2021)), conditions of increased organic matter influx predominated in the study area, during the Holocene, causing environmental variations and affecting the distribution of the biota.

Ostracods
The ostracod assemblages registered are composed mostly of macrocypridids, krithids, trachyleberidids, pontocypridids, and cytherurids.The presence of Krithe, Argilloecia, Macromckenziea, Macropyxis, Ambocythere, Bythoceratina, and Rugocythereis (Suppl.Mat.) characterizes a typical bathyal environment, as observed in previous studies (e.g., Dingle et al. 1990, Bergue et al. 2006, 2016, 2021, Brandão 2010, Yasuhara et al. 2013, 2021, Maia et al. 2021, 2022).This is the first study on deep-sea ostracods from the Brazilian Equatorial Margin, but the paucity of material prevents detailed comparison with other studies in the Brazilian Margin.The macrocypridid Macromckenzia is widely distributed in bathyal regions along the Atlantic Ocean (Brandão 2010), but it is represented here by a species different from all others registered in the South Atlantic (Maddocks 1990, Brandão 2004a, 2004b, 2010).On the contrary, Macropyxis bathyalensis is a typical North Atlantic species, and it is registered for the first time in the Brazilian Equatorial Margin.Krithe morkhoveni and K. sinuosa have wide distribution in the Atlantic Ocean and Mediterranean (van den Bold 1960, Coles et al. 1994, Rodriguez-Lazaro and Cronin 1999).The highest species richness occurs in the sample 28-25 cm, where nine species are registered.In the samples 142-139 and 130-127 cm, Krithe was more frequently associated with the epifaunal foraminifera Pyrgo sp.In the samples 70-67 and 42-39 cm, the association occurred with the infaunal taxon Globocasidulina sp.The same zoogeographic pattern is presented by Bythoceratina scaberrima.
Two species of Ambocythere, a genus diverse in the Atlantic Ocean deep waters (Yasuhara et al. 2015), have been registered in this study.One of them has a strong similarity to Ambocythere circumporus, however, with stronger longitudinal ribs and a caudal process that is more acuminate and less spinose.Another species of the genus herein recorded, Ambocythere sp., differs in having a conspicuous perforate spine near the posterior cardinal angle and subdued ornamentation.The nearest study on deep-sea ostracods was carried out at ODP site 925, Ceará Rise (Yasuhara et al. 2009a(Yasuhara et al. , 2021)); however, the taxonomic similarity between the two sites is represented only by Argilloecia labri, possibly due to the low abundance of the material herein studied.

Pteropods
Several studies have shown the sensitivity of late Quaternary pteropods to temperature, oxygen concentration, and salinity, proving their importance for paleoclimatic reconstructions (Herman 1971, Singh et al. 2005, Wall-Palmer et al. 2014, Giamali et al. 2020, 2021).Peaks of abundances of pteropods are positively correlated with aragonite saturation state, O 2 concentration, pH, salinity, and temperature and negatively correlated with nutrient concentration (Howes et al. 2015, Johnson et al. 2020, Giamali et al. 2021).Two genera of pteropods were identified in the present study: Heliconoides d'Orbigny, 1835 and Atlanta Lesueur, 1817; a third was tentatively identified as Creseis Rang, 1828.Two peaks of abundance are observed in the core ANP 1011 (base and top, Fig. 6), both associated with epifaunal foraminifera, reinforcing the hypothesis of a higher oxygenated paleoenvironment with a lower concentration of nutrients.The variations observed in the distribution of pteropods may be caused by displacement of water masses, with good preservation indicating NADW influence and poor preservation (due to corrosion) related to climatically induced variations of intermediate water masses (Gerhardt et al. 2000).

CONCLUSION
The integrated analysis of calcareous microfossils (i.e., foraminifera, ostracods, and pteropods) demonstrated to be a valuable approach for paleoceanographic studies in late Quaternary deposits in the Ceará Basin.Benthic foraminifera recovered in the > 0.150 mm fraction is abundant and diverse, although we are aware that our analysis would possibly benefit from an additional > 0.062 mm fraction.The model based on the ecological characteristics of the benthic foraminifers allowed the characterization of two ecological settings during the Pleistocene-Holocene transition.The environmental setting I corresponds to the glacial period (late Pleistocene), and it is characterized by the abundance of epifaunal species, high productivity, phytodetritus input, increased oxygen concentration, but lower organic carbon.The environmental setting II corresponds to the interglacial period (Holocene) and is characterized by environmental instability, with periods of lower oxygenation (predominance of uvigerinids) and higher oxygenation (predominance of cassidulinids).During this environmental setting, there is also a higher organic carbon, nutrient, and food supply.Studies focused on the fraction of >0.062 mm, however, are necessary for a more detailed paleoenvironmental scenario.The taxonomic composition of ostracod assemblages herein studied differs in some degree compared to other regions of the Brazilian Margin.The low richness of the ostracod fauna reflects probably the low abundance; however, the higher richness during the Holocene in relation to the Pleistocene is in accordance with previous studies in the Atlantic Ocean.
More studies focused on the taxonomy of ostracods are necessary to assess the actual diversity and relationship with adjacent oceanic areas.

Figure 1 .
Figure 1.Location map of the core ANP 1011 in the Ceará Basin showing the surface circulation in the Brazilian Equatorial Margin, the physiography of the study area, and current arrows are superimposed on their speed (Noucoucouk et al. 2021).

15 Figure 5 .
Figure 5. Graphic representation of (A) the relative abundance (RA) of main genera and species of benthic foraminifera and (B) of the absolute abundance (AA) ostracods identified in core ANP 1011.
High surface productivity with sustained flux of organic matter, carbon flux, and low dissolved oxygen concentrationsMorigi et al.