The response of deep-water benthic foraminiferal assemblages to changes in paleoproductivity during the Pleistocene (last 769.2 kyr), western South Atlantic Ocean

Palaeogeography, Palaeoclimatology, Palaeoecology 440 (2015) 201–212

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The response of deep-water benthic foraminiferal assemblages to changes in paleoproductivity during the Pleistocene (last 769.2 kyr), western South Atlantic Ocean Fabiana K. de Almeida a, Renata M. de Mello b,c, Karen B. Costa a, Felipe A.L. Toledo a a b c

Laboratório de Paleoceanografia do Atlântico Sul, Instituto Oceanográfico, Universidade de São Paulo, Praça do Oceanográfico, 191 Cidade Universitária, CEP 05508-120, São Paulo, SP, Brazil PETROBRAS-CENPES, Cidade Universitária, CEP 21949-948, Rio de Janeiro, RJ, Brazil University of Massachusetts, Dept. of Geosciences, 233 Morril Science Center, 611 N. Pleasant St., Amherst, MA 01003, USA

a r t i c l e

i n f o

Article history: Received 27 April 2015 Received in revised form 21 August 2015 Accepted 3 September 2015 Available online 12 September 2015 Keywords: Benthic foraminifera Phytodetritus species Paleoproductivity Santos Basin Pleistocene

a b s t r a c t Benthic foraminiferal assemblages and δ18O records in a core from Santos Basin (western South Atlantic, 2220 m water depth) were analyzed to investigate productivity changes during the Pleistocene. The sediment core recorded the last 770 kyr, including Marine Isotope Stages (MIS) 19 to 1. The four dominant benthic foraminiferal assemblages were identified using Q-mode Varimax Factor Analysis, and are represented by Globocassidulina crassa, Bolivina spp., Epistominella exigua and Alabaminella weddellensis. From 769.2 kyr (MIS 19) to ~300 kyr (MIS 8), the highest values of factor 2 (Bolivina spp. assemblage) indicate increased influx of organic matter to the seafloor and a slight decrease in the oxygen concentration at the sediment–water interface. This condition began to change in the stage 8 (~ 288.9 kyr to ~ 268.3 kyr), and it is characterized by high values of factor 1, when the G. crassa assemblage became dominant, indicating an increase in oxygen concentrations and a decrease in the influx of organic matter. Seasonally-pulsed organic matter resulting in a distinct phytodetritus layer accumulated mostly during the glacial MIS 14, 10, 8, 6, and 5.2–5.1, and in the interglacial stage 11 and the end of 9, as indicated by factor 3 (E. exigua assemblage) and factor 4 (A. weddellensis assemblage). The highest peak of the A. weddellensis assemblage during MIS 11 (~401.4 kyr) coincides with the Mid-Brunhes Event. The highest benthic foraminiferal accumulation rates occurred during mostly glacial stages, indicating delivery of more organic matter to the seafloor. The changes in benthic foraminifera assemblages in the glacial stages during the Pleistocene indicate changes in primary productivity in surface waters. Increasing the amount of organic matter delivered to the seafloor amplified the benthic foraminiferal response. © 2015 Elsevier B.V. All rights reserved.

1. Introduction During the Pleistocene, the deep-sea environment was strongly influenced by glacial–interglacial cycles. Benthic foraminiferal assemblages worldwide recorded glacial–interglacial cycles, reflecting changes in primary productivity in sea-surface waters (Thomas et al., 1995; Schmiedl and Mackensen, 1997; Sen Gupta et al., 2006). Within the Pleistocene, the global climate system underwent a major transition: the Mid-Brunhes Event (MBE), which is centered around 400 kyr BP (Jansen et al., 1986). The MBE is characterized by the global increase in pelagic carbonate production, probably linked to nutrient flux and upwelling intensity in the oceans (Flores et al, 2012). Productivity of surface waters determines, in part, the flux of organic matter through the water column, with a very small portion reaching the seafloor and even less ultimately buried in the sediment (Rullköter, 2000). Benthic foraminiferal assemblages respond to

E-mail address: [email protected] (F.K. de Almeida).

http://dx.doi.org/10.1016/j.palaeo.2015.09.005 0031-0182/© 2015 Elsevier B.V. All rights reserved.

changes in surface primary productivity (Schmiedl and Mackensen, 1997; Ohkushi et al., 2000; Sun et al., 2006). For this reason, benthic foraminiferal assemblages have been considered reliable proxies of paleoproductivity in paleoceanographic investigations (Mackensen et al., 2000). The input of organic matter, along with bottom-water oxygenation, seems to be the major factors that control the distributions and the abundances of benthic foraminifera in the deep ocean (Gooday, 1988, 1993, 2002; Fariduddin and Loubere, 1997; Altenbach et al., 1999; Fontanier et al., 2002, 2005; Enge et al., 2014). As proposed by Jorissen et al. (1995), the trophic oxygen (TROX) model predicts that the depth of foraminiferal microhabitats is a combination of oxygen penetration and food availability in the sediment. Therefore, benthic foraminifera distributions in oligotrophic and well oxygenated environments are primarily restricted to the sediment surface and assemblages consist largely of epifaunal species. On the contrary, in eutrophic and dysoxic environments, the foraminiferal assemblage is mainly dominated by infaunal taxa. The amount and quality of organic matter delivered into the seafloor appear to be essential factors that influence makeup and abundance of

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benthic foraminiferal assemblages (Corliss and Chen, 1988; Corliss, 1991; Smart et al, 1994; Gooday, 1996; Schmiedl and Mackensen, 1997). In oligotrophic regions, very little labile organic matter arrives at the seafloor and, what does, is rapidly consumed at the sediment– water interface (Carney, 1989). The benthic foraminiferal abundances are determined by this food supply (Jorissen et al., 1995; Schmiedl et al., 1997). Phytodetritus, which is a main food source for benthic microfauna (Lambshead and Gooday, 1990; Gooday and Hughes, 2002), typically reaches the seafloor in pulses delivered from seasonal increases in surface production (Gooday and Turley, 1990; Gooday, 2002). Phytodetritus contains a wide variety of planktonic remains, including live and dead phytoplankton, zooplankton, and fecal pellets held together by a gelatinous and membranous matrix (Gooday and Turley, 1990; Turley, 2002). A close coupling between the deposition of phytodetritus and foraminiferal population densities has been demonstrated because the labile food source triggers rapid population increases in opportunistic benthic foraminiferal species (Fontanier et al., 2003, 2006). Thus, changes in sea-surface primary productivity have a strong influence on the composition of benthic foraminiferal assemblages (Fariduddin and Loubere, 1997). The distribution of Recent deep-sea benthic foraminifera in areas of the South Atlantic Ocean has been documented by several authors (e.g., Lohmann, 1978; Peterson and Lohmann, 1982; Mackensen et al., 1995; Fariduddin and Loubere, 1997; Schmiedl et al., 1997; Schmiedl and Mackensen, 1997; Altenbach et al., 1999; Alperin et al., 2011 and others). However, the Brazilian continental slope has never been the focus of paleoproductivity studies in the Pleistocene based on benthic foraminifera (de Mello, 2006; Sousa et al., 2006; Barbosa, 2010; Eichler et al., 2014). In this study we attempt to investigate long-term fluctuations in the benthic foraminiferal assemblages over the last 769.2 kyr in the Santos Basin (Brazilian Continental Margin) response to changes in surface productivity. 2. Materials and methods 2.1. Study area The study area is located in the Santos Basin, which is one of the largest Brazilian continental basins, up to 350,000 km2, along the southeastern Brazilian continental slope. This basin has its northern limits at Cabo Frio High and southern limits at the Florianopolis High (Pereira and Feijó, 1994) (Fig. 1). Seismic–stratigraphic interpretation of the Late

Palaeogene to Recent section of the northern Santos Basin indicates the presence of the Santos Drift System, composed of several contourite deposits. Seismic evidence suggests that sedimentation during the Neogene was dominated by oceanic circulation, redistributing the sediments transferred to the basin during high and low stands of sea level. This pattern indicates the path and relative intensity of the bottom currents that passed through the Santos Basin in different climatic and oceanographic conditions (Duarte and Viana, 2007). Modern sedimentation on the Santos Basin slope is a combined response to bottom morphology, the cross-isobaths flow associated with meandering of the Brazil Current (BC), and seaward transport of coastal water (Mahiques et al., 2002). Surface waters of the Santos Basin are dominated by the southwardflowing, warm, saline and nutrient-depleted BC, which is the western boundary current associated with the anticyclonic South Atlantic Subtropical Gyre (Stramma and England, 1999; Campos et al., 2000). The BC flows southward along the Brazilian margin to the Subtropical Convergence Zone where, around 38°S, it encounters the Malvinas Current (MC). The MC transports cold, lower-salinity, nutrient-rich sub-Antarctic water masses northward along the Argentinean continental shelf (Gordon, 1989). The wind regime over the study area is dominated by the presence of the South Atlantic Convergence Zone (SACZ), with winds blowing predominantly from the northeast (Campos et al., 2000). In the western South Atlantic Ocean, primary production in surface waters is ≤ 50 gCm -2 yr 1, which is low compared with that of the eastern South Atlantic Ocean (Rühlemann et al., 1999). In terms of surface primary productivity, the Brazilian continental margin is a typical lowlatitude oligotrophic area (Gaeta and Brandini, 2006). The occurrence of upwelling in the study area is associated with the cyclonic meanders of the BC, occurring year around, and wind-driven inner-shelf upwelling that peaks during austral summer. These processes may be responsible for pumping the South Atlantic Central Water (SACW) onto the shelf, bringing cold, nutrient-rich SACW to the photic zone (Campos et al., 1995, 2000). Cold front incursions increase wind intensity, thereby destabilizing and mixing the water column, and delivering nutrients to the surface ocean (Nybakken and Bertness, 2005). There are no large rivers in the area, so the supply of terrigenous sediments to the slope is limited. However, under favorable wind conditions the La Plata River plume extends north into lower latitudes and enters the inner-shelf during winter, reaching to ~ 23°S (Campos et al., 1999; Pimenta et al., 2005; Piola et al., 2005; Pivel et al., 2013). La Plata River

Fig. 1. GL-854 core location in the western South Atlantic (Santos Basin).

F.K. de Almeida et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 440 (2015) 201–212

is the second largest river in South America, extending along a coastal strip of 1300 km; the seasonal variability of this river plume is controlled by the alongshore component of the wind stress (Piola et al., 2005). The Brazilian southeastern oceanographic setting is characterized by the stacking of several water masses: the Tropical Water (TW) and the South Atlantic Central Water (SACW) above about 600 m; the northward-flowing Antarctic Intermediate Water (AAIW) between 600 and 1000 m; the northward-flowing Circumpolar Water (CPW) between about 1000 and 2000 m; the southward-flowing North Atlantic Deep Water (NADW) between about 2000 and 4000 m; and finally the northward-flowing Antarctic Bottom Water (AABW) below 4000 m (Duarte and Viana, 2007). In the study area, the deep waters are strongly influenced by the NADW and to a lesser degree by CPW (Fig. 2). The CPW water mass is depleted in oxygen and its density is comparable to that of NADW flowing south. As a result, NADW splits CPW into an upper (UCPW) and a lower (LCPW) branch (Johnson, 1983; Mémery et al., 2000). 2.2. Material Our samples were selected from one piston core (25°12′S, 42°37′W, 2220 m water depth), during Fugro Explorer Campaign 2007 (Fig. 1). The core length is 20.38 m. The core lithology consists of marl, carbonate-rich mud (CaCO3 content 18–30%) and carbonate-poor mud (CaCO3 content 5–18%). 2.3. Stable isotope record and radiocarbon dating The samples for stable isotopic analysis were collected at 5 cm intervals along the core. Isotopic measurements were made at the Laboratori d' Anàlisi d' Isòtops Estables (IRMS), in the Universitat Autonoma de Barcelona on a Finnigan MAT 252 mass spectrometer with an integrated automated carbonate device and calibrated to Vienna Pee Dee Belemnite (VPDB) following standard procedures. At least 3 specimens of Cibicidoides wuellerstorfi (N 150 μm) were analyzed per sample. During the course of sample analysis, the external precision of the laboratory standards was δ18O = 0.09%. Three radiocarbon dates (Table 1) were acquired from tests of Globigerinoides ruber at the National Ocean Science Accelerator Mass Spectrometer Facility (NOSAMS) at Woods Hole Oceanographic Institution (WHOI). The radiocarbon ages were transformed into calendar ages by first subtracting an estimated reservoir age of 271 years, according to Butzin et al. (2005), using software available at http://radiocarbon.LDEO.columbia.edu/ and by applying the Fairbanks et al. (2005) calibration curve. The age model was built using the correlation of the benthic foraminiferal oxygen isotope record and the Lisiecki and Raymo (2005) stack using the software Analyseries

203

Table 1 Radiocarbon dating and respective calendar ages for core GL-854. Sample depth

14

C age

(cm) 0 14 51

3982 20,032 37,832

Error

Reservoir effect Calendar age

Error (1σ)

(14C yr)

(yr)

(yr)

(calendar age)

35 130 250

268 268 268

4442 23,931 42,850

40 164 275

2.0 (Paillard et al., 1996). The calendar ages of the three 14C AMS dates and the glacial terminations were used as control points in the model. The age model allowed estimation of a mean sedimentation rate of 4.3 cm/kyr throughout the core (Fig. 3). 2.4. Benthic foraminiferal analysis The benthic foraminiferal assemblage data came from 40 samples, taken between 20.35 m and 0 m, which correspond to 769.2 kyr and 4.4 kyr BP respectively. To obtain the dry bulk density (DBD; Table 2), the dry weight of each sample was determined and divided by the wet volume of the sample (~ 20 cm3). The samples were dried in an oven at 50 °C, weighed, soaked in distilled water and disaggregated using a laboratory shaker, washed under tapwater through a 63 μm sieve, dried and weighed again. Processed samples were split from N63 μm size fraction with a microsplitter to obtain at least 300 specimens of benthic foraminifera per sample. All benthic foraminifera were picked and included in the assemblage counts. A total of 88 taxa were identified, with 32 species contributing significantly to the total population (with relative abundances of more than 1% in at least two samples). The relative abundance of these 32 species was analyzed using Q-mode Varimax Factor Analysis, using the STATISTICA software package. The number of benthic foraminifera (BFN = number of benthic foraminifera/gram dry sediment) was calculated for each sample, as well the percentage of agglutinated, porcelaneous and calcareous hyaline tests. The microhabitat preference (epifaunal vs. infaunal) was recorded, based on the morphotypes of the tests as proposed by Corliss (1985) and Corliss and Chen (1988). The benthic foraminiferal accumulation rate (BFAR) has been used as additional tool to indicate primary productivity (Schmiedl and Mackensen, 1997; Ohkushi et al., 2000; Jorissen et al., 2007). This proxy seems to be correlated to organic matter flux rates that reach the seafloor (Herguera and Berger, 1991; Herguera, 1992, 2000). All specimens counted in the N 63 μm size fraction were used to calculate this index. BFAR was calculated as follows:BFAR = BF × LSR × DBD where BF is the number of benthic foraminifera/gram dry sediment, LSR is the linear sedimentation rate in cm/kyr, and DBD is the dry bulk density (g/cm3). The sedimentation rate was calculated for each sample based on the age model.

Fig. 2. Distributions of present water masses at the GL-854 core location based on oxygen concentration. South Atlantic Central Water (SACW), Antarctic Intermediate Water (AAIW), Upper Circumpolar Water (UCPW), Antarctic Bottom Water (AABW), Lower Circumpolar Water (LCPW) and North Atlantic Deep Water (NADW). Data from electronic atlas of WOCE hydrographic (Schlitzer, 2000).

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present (BP) and covering the marine isotope stages (MIS) 19 to 1. The GL-854 δ18O record correlated well with the global stack of LR04 record (Lisiecki and Raymo, 2005). The average for glacial δ18O overall was about 3.9‰, while interglacial δ18O was about 3.3‰. In general, the glacial–interglacial variations in δ18O reflected the global pattern for deep water. 3.2. Benthic foraminiferal distribution The BFN (benthic foraminiferal number/gram dry sediment) varies between 40 and 4135, with an overall median value of 859 and high values at the base and middle part of the core. In general, BFN values above the median are observed during the glacial stages 16, 12, 10, and the cold sub-stage 7.4. Peak values are also found in the middle of stage 8 and end of stage 6. High values are also found in the interglacial stages near the base of the core, which correspond to stages 19, 17, 15 and upward in 13 and 7 (Table 3, Figs. 5 and 7). In the near surface sediments, which correspond to stages 3, 2 and 1, the percentages of well-preserved agglutinated foraminiferal tests likely contribute to the

Fig. 3. Calendar age vs. depth plot for GL-854 core.

3. Results 3.1. Oxygen isotope record The age model for Core GL-854 was based upon the correlation between the benthic δ18O record (Fig. 4) and the LR04 stack. The age model revealed seven climate cycles, beginning at 772,000 yr before

Table 2 Oxygen isotope data, sedimentation rate (SR), and dry bulk density (DBD) for core GL-854. Depth in core

Age

(cm)

(kyr)

0 6 14 27 36 46 76 161 263 363 443 573 616 626 661 740 781 856 886 956 1036 1066 1106 1146 1191 1231 1271 1336 1395 1530 1555 1575 1630 1660 1720 1785 1845 1870 1935 2035

4.4 12.8 23.9 30.6 35.2 40.3 47.8 60.9 73.5 85 97.2 122.2 138.6 141.3 150.9 172.5 183.7 211.3 223.3 245 257.4 262.1 268.3 274.5 281.4 288.9 300 322.1 348.3 401.4 433.3 450.4 506.5 538.6 557 575.8 630.2 646.6 689 769.2

MIS

1 2 3

4 5

6

7 8

9 10 11 12 13 14 15 16 17 19

C. wuellerstorfi

SR

DBD

δ18O (‰)

(cm/kyr)

(g/cm3)

3.13 3.62 4.14 3.92 3.75 3.99 3.69 4.12 3.57 3.78 3.22 2.39 4.22 4.35 4.09 3.82 4.19 2.98 3.90 4.24 3.48 4.01 4.00 3.93 3.36 3.81 3.81 3.19 4.33 2.71 4.19 4.17 3.12 4.18 3.64 2.83 4.46 4.05 3.41 3.22

0.72 0.72 1.96 1.96 1.96 1.96 5.02 7.5 11.24 7.54 6.28 2.85 3.66 3.66 3.66 3.66 3.66 2.31 2.93 6.45 6.45 6.45 6.45 6.45 6.92 3.92 3.22 1.97 2.95 1.21 1.29 1.17 0.87 3.26 3.26 1.82 0.52 1.53 1.53 1.12

1.00 0.89 0.93 0.81 0.82 0.77 0.78 0.78 0.76 0.72 0.80 0.77 1.12 0.89 0.89 0.90 0.84 0.88 0.97 1.01 0.88 0.95 0.92 0.90 0.91 0.99 0.88 0.91 0.97 0.96 1.07 1.16 1.00 0.97 0.96 0.94 1.00 1.04 1.03 1.02

Fig. 4. GL-854 oxygen isotope record vs. LR04 stack (reference curve). Dotted lines indicate main control points. MIS: marine isotope stages.

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elevated BFN values. Benthic assemblages include a mixture of infaunal (mostly the shallow infaunal, e.g. Bolivina, Bulimina and Uvigerina) and epifaunal (e.g. Alabaminella, Cibicidoides, Epistominella, Oridorsalis and Pyrgo) morphogroups. However, the infaunal morphogroup usually dominates over epifaunal throughout the entire interval studied. Intervals where the percentage of the epifaunal morphogroup exceeds the infaunal morphogroup include stages 14, 11, 8 and 6. In general, the benthic foraminiferal tests are well-preserved. The calcareous hyaline taxa are dominant (≥ 86%) throughout the studied interval (Figs. 5, 6). The porcelaneous taxa peak (maximum 12%), during stages 14 and 5. The common porcelanous taxa are Cornuspira spp., Pyrgo murrhina, Quinqueloculina spp., Spirophitalmidium spp. and Triloculinella pseudooblonga. Agglutinated taxa are relatively uncommon (≤2%), with peaks occurring during the glacial stages. The most frequently encountered agglutinated taxa are Eggerella bradyi, Sigmoilopsis schlumbergeri, Siphotextularia affinis, Siphotextularia curta and Textularia spp. Considering the low proportions of agglutinated tests compared to calcareous tests and that, in general, the latter are well-preserved, we believe that if carbonate dissolution occurred, it did not seriously affect the assemblages. Other carbonate dissolution proxies are not considered in this study. The BFAR values vary between 114 and 24,569, with an overall median value of 1725 tests cm 2 kyr- 1. The BFAR values above the median are found during glacial stages 16, 12, 10, 4, as well during the cold sub-stage 7.4. In the middle of glacial stage 8, BFAR values are about three times higher than those observed in the end of glacial stage 6. Except for the interglacial stages 17, 15, 13 and 5, the highest BFAR values occurred during the glacial stages (see Table 3, Figs. 5 and 7). Thirty-two species have relative abundances of N 1% in at least two samples and fifteen species have relative abundances of N 5% in at least one sample. The relative abundances of the four dominant taxa, Bolivina spp., Globocassidulina crassa, Epistominella exigua and Alabaminella weddellensis, vary over the interval assessed, though their dominance correlates with specific intervals (Table 3, Fig. 6). Bolivina spp. are the most abundant taxa at the base of the core, and their abundance decreases toward the core-top. The highest values for Bolivina spp. occur from the end of stage 19 to stage 15, and during the glacial stages 12, 10, end of 8, and 6. Globocassidulina crassa is common in all samples, increasing upward starting at stage 8. Epistominella exigua and Alabaminella weddellensis are also common throughout. The highest relative abundances of Alabaminella weddellensis occur in stages 11, 10, end of 9 and 8, while those of E. exigua occur during stages 19, 14, 8, 6, and from 5.2 to 5.1.

205

Relative abundance of Bolivina inflata peaks in stages 15 and 9, and this species is common only from stages 16 to 9. The relative abundance of Cassidulina carinata reaches 23% during the transition from 5.2 to 5.1, with lesser peaks in stages 14, 12, and 6, indicating positive correlation with these glacial stages. Oridorsalis spp. has its highest abundance (up to 11%) on the boundary of stages 9 to 8, and then exhibits lesser peaks during glacial stages 8 and 6, suggesting that Oridorsalis spp. also thrives during glacial stages. The unilocular group exhibits relative abundance up to 10%, and is represented by Fissurina, Lagena and Parafissurina. The relative abundance of Eponides alabaminaeformis is up to 8% and is highest abundance in the glacial stage 8. Globocassidulina subglobosa (up to 7%) abundances increase in stages 9, 5.2 to 5.1, 4 and 3. Globocassidulina minuta (up to 7%) exhibits higher values during interglacial stages 19, 17, and 11. Gavelinopsis versiformis (up to 6%) is more abundant during glacial stages, with higher peaks during stages 16, 12, 8, 6 and 2. Pullenia quinqueloba (up to about 5%) has its highest abundance next to the end of the stage 9. Also at the end of the stage 9 (~ 300 kyr), some deep infaunal species (Bulimina aculeata and Uvigerina peregrina) are more abundant, with abundances values varying from 1% to 7%. Bulimina aculeata (up to 7%) is more abundant in glacial stage 4 and cold sub-stage 7.4. Relative abundance of U. peregrina (up to 5%) fluctuates during stage 8 and peaks in substage 7.4 and during the transition from 5.2 to 5.1. 3.3. Statistical analysis Results of Q-mode Varimax Factor Analysis allowed us to identify four dominant factors that accounted for 95% of the total variance. The scores (Table 4) indicate the weight of each species relative to the respective Q-mode factor, and the loadings explain the importance of the individual factors in each sample. The characteristics of the four factors are mainly explained by the most abundant species (Fig. 7). Factor 1 accounts for 63.5% of the total variance and is defined by the relative abundance of Globocassidulina crassa (score = 5.3). Loading values of this factor gradually increase up core to a first peak in the beginning of stage 8 (~288.9 kyr), and then continue to increase up core, with two notable declines at stage 6 and sub-stage 5.2. Factor 2 accounts for 15.8% of the total variance and is dominantly linked to the relative abundance of Bolivina spp. (score = 5.2). This factor exhibits relatively high loading values from stages 19 to 15 and then from stages 13 to 12, with peaks also occurring in stages 9, 8 and 6 (~322.1, ~268.3 and ~138.6 kyr respectively). Factor 3 represents 10.3% of the total variance and reflects the relative abundance of Epistominella exigua (score =

Table 3 Comparison of median values for glacial and interglacial intervals of the BFN, BFAR, and relative abundances of key taxa. For intervals that have only one sample, the values expressed are the same as those found by the calculation of each data. MIS

No. samples

BFN (N°/g)

BFAR (N°/cm−2 kyr−1)

A. weddellensis

E. exigua

Bolivina spp.

G. crassa

1 2 3 4 5 (5.2–5.1) 5 6 7 7 (7.4) 8 9 10 11 12 13 14 15 16 17 18 19

2 1 4 1 1 3 5 1 1 7 2 1 1 2 1 2 1 2 1 – 1

1047 1695 1479 351 316 552 470 1024 1784 273 221 1142 821 2486 2901 437 1171 1638 1895 – 1198

707 3105 2556 2049 1724 2763 1530 2087 5044 1704 418 3252 955 3418 2513 1373 2007 1793 2989 – 1370

7 1 2 3 4 10 2 12 7 7 18 26 28 4 5 4 10 4 3 – 2

1 3 5 4 33 11 16 16 15 24 6 2 16 16 13 27 20 15 16 – 24

18 25 26 5 5 8 14 11 15 14 15 27 14 38 34 18 27 45 38 – 30

36 32 43 57 22 28 23 29 38 24 10 11 8 7 3 7 2 2 6 – 2

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Fig. 5. δ18O values from Cibicidoides wuellerstorfi, BFN and BFAR. Percentage of benthic foraminiferal with microhabitat epifaunal vs. infaunal (note that fields filled in black on the plot correspond to intervals where benthic foraminiferal was dominated by epifaunal morphogroups).The percentages proportion of benthic foraminiferal species agglutinated, porcelaneous and calcareous hyaline tests in core GL-854.

5.1). The highest loadings values of this factor occur during glacial stages 14, 8, 6 and particularly in the transition of sub-stage 5.2 to 5.1. Finally, factor 4 accounts for 5.3% of the total variance, and reflects the relative abundance of Alabaminella weddellensis (score = 5.0). High loading values of this factor occur during stages 11, 10 and in the end of stage 9. 4. Discussion Benthic foraminiferal assemblages can be directly related to surface productivity, or to the organic material that actually reaches the seafloor (Ohkushi et al., 2000). In this study, we investigated the down-core fluctuations of benthic foraminiferal assemblages compared with oxygen stable isotope data to reconstruct the effects of paleoproductivity on the benthic microfauna of the western South Atlantic Ocean. In general, the highest BFAR values are related to the glacial stages and cold sub-stages, as previously reported by Schmiedl and Mackensen (1997) for the Southwest African Continental slope. Such increases in BFAR values during cold intervals have been correlated to enhanced surface productivity and subsequent export of organic matter to the seafloor (Schmiedl and Mackensen, 1997; Guichard et al., 1999; Ohkushi et al., 2000; Zhang et al., 2007; Nagai et al., 2010; Diester-Haass et al., 2011). Thus, BFAR fluctuations observed in the Santos Basin indicate that the flux of organic matter is greater during the cold stages than in the warm stages. The factor analysis reflects the distribution of four assemblages along the core: Globocassidulina crassa (factor 1), Bolivina spp. (factor 2),

Epistominella exigua (factor 3) and Alabaminella weddellensis (factor 4). These taxa have been associated with influx of organic matter to the seafloor, though Globocassidulina also may be associated with strong bottom currents (Mackensen et al., 1995; Smart, 2008). Benthic foraminiferal assemblages dominated by Bolivina spp. are considered to be an indicator of high, continuous flux of organic matter to the seafloor, most likely associated with reduced bottom-water oxygenation (Gooday, 1994; Mackensen et al., 1995; Schmiedl et al., 1997; Bernhard and Gupta, 1999) or due an increase of more refractory organic matter (Abu-Zied et al., 2008). At Campos Basin (southeastern Brazilian Continental margin), Bolivina spp. were associated with low oxygen levels at the seafloor (Sousa et al., 2006). Barbosa (2010) interpreted the dominance of bolivinids in a distinct biofacies to indicate a paleoenvironment with high organic flux, low oxygen concentration and cold waters during the Upper Quaternary. From 769.2 kyr (MIS 19) to ~ 300 kyr (beginning of MIS 8), the highest values of factor 2 (Bolivina spp.) indicate a relatively high flux of organic matter to the seafloor and a slightly oxygen concentration decrease in the sediment–water interface. This condition began to change in the stage 8 (~ 288.9 kyr and then ~ 268.3 kyr), as indicated by high values of factor 1 (G. crassa). However, it was during stage 7 (~223.3kyr) that this assemblage became more dominant, indicating a possible increase in oxygen concentrations and a reduction in influx organic matter. Despite some variation, the G. crassa assemblage was dominant until stage 1. This setting is more consistent with the current low productivity environment in the Southwestern Atlantic (Rühlemann et al., 1999). Although low productivity surface waters

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prevailed after stage 8, the intervals that registered high factor 2 values indicated phases with increased organic matter influx to the core site. Thus, surface productivity appears to have been enhanced during the end of stage 6 (from ~ 141.3 to ~ 138.6 kyr), and with minor intensity, during stage 3 (from ~ 35.2 to ~ 30.6 kyr) and 2 (~ 23.9 kyr). Gooday (1988) reported that the calcareous species Alabaminella weddellensis and Epistominella exigua have greenish protoplasm, suggesting these taxa ingest phytodetritus. Several authors have speculated that A. weddellensis and E. exigua feed on phytodetritus (then so-called ‘phytodetritus species’) and respond to seasonally pulsed inputs of labile organic matter with rapid growth and reproduction (Gooday, 1988, 1993). Therefore, the abundances of A. weddellensis and E. exigua in a benthic assemblage have led to attempts to use these species as indicators of seasonal phytodetritus inputs (Gooday, 1994, 2003; Smart et al., 1994; Mackensen et al., 1995; Fariduddin and Loubere, 1997; Schmiedl and Mackensen, 1997; Ohkushi et al., 2000; Hayward et al., 2002; Sun et al., 2006; Jorissen et al., 2007; Smart, 2008; Gooday et al., 2010), and seem to reflect seasonality in paleoproductivity in the fossil record (Thomas et al., 1995; Thomas and Gooday, 1996). High organic matter fluxes without strong seasonal changes limited the distribution of E. exigua in the eastern South Atlantic (Schmiedl and Mackensen, 1997). According to Thomas and Gooday (1996), abundant “phytodetritus species” will be expressed in the fossil record only if phytodetritus accumulated predictably in a particular area. Such paleontological records could be used to identify intervals with seasonal productivity and, consequently, seasonal phytodetritus deposition (Smart et al., 1994; Thomas et al., 1995). Intervals dominated by factor 3 (E. exigua) and factor 4 (A. weddellensis) may reflect lower overall food supply and higher oxygen concentration than intervals dominated by factor 2 (Bolivina spp.), and a pulsed, seasonal delivery of food to the seafloor. These results indicate seasonally pulsed organic matter, with a distinct phytodetritus layer mostly during the glacial stages 14, 8, 6, and from 5.2 to 5.1, as indicated by the E. exigua assemblage, and during the stages 11, 10, and from the end of 9 to 8, as indicated by the A. weddellensis assemblage. The highest peak of A. weddellensis assemblage during stage 11 (~ 401.4 kyr) coincides with the transitional climatic event the MidBrunhes Event (MBE) (Candy et al., 2010). This event is centered about 400 kyr and it is marked by an abrupt shift toward lower δ18O values during interglacial stages beginning with MIS 11 (Hodell et al., 2003). Jansen et al. (1986) proposed a Mid-Brunhes transition to more humid, interglacial conditions in the southern hemisphere. Besides other parameters, the MBE coincides with the increase in global carbonate production from pelagic sources, mainly related to the proliferation of the coccolithophore Gephyrocapsa, which represents an episode of higher nutrient availability at the ocean surface (Flores et al., 2012). A correlation analysis indicates that the high relative abundance of one species (E. exigua or A. weddellensis) is not a strong indicator of either primary productivity or seasonality (Sun et al., 2006). Some researchers have interpreted the opposite abundance trend of these species as a subtle difference in their environmental preferences in Recent environments (Gooday and Turley, 1990; Gooday, 1993, 1996). Off northwestern Africa, Fariduddin and Loubere (1997) found that A. weddellensis was more dominant in very high surface productivity regions and, as productivity decreases, its occurrence becomes less important and E. exigua increases in abundance. The abundance of A. weddellensis was associated with an area of highest productivity in the North Atlantic whereas E. exigua was associated with regions of high seasonality (Sun et al., 2006). Ferreira et al. (2014) also reported an opposite trend between these species along two cores retrieved in the Brazilian Continental margin. Perhaps A. weddellensis is more common during deposition of phytodetritus with a high proportion of needle-shaped diatoms (King et al., 1998; Ohkushi et al., 2000). Although previous studies suggest a close relation between these species

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distributions and the type of food (phytodetritus), no correlation was observed in our samples. The relationship between benthic foraminiferal and the accumulation of organic matter is useful for palaeoceanographic reconstructions (Herguera and Berger, 1991). Benthic foraminiferal faunas provide information not directly on surface productivity, but on the organic material that reaches the seafloor (Ohkushi et al., 2000). The productivity history of the last 796.2 kyr over the Santos Basin indicates a strong variation in seasonality and organic matter influx, simultaneously with the oxygen concentrations on the seafloor. Although this region has been classified as low productivity (Rühlemann et al., 1999) and a lowlatitude oligotrophic area (Gaeta and Brandini, 2006), we observed that, on the Santos Basin slope, the influx of organic matter was higher during glacial stages of the western South Atlantic, based on BFAR and benthic foraminiferal assemblages dominated by Bolivina species. Schmiedl and Mackensen (1997) suggested that the enhanced organic matter fluxes during glacial stages in the eastern South Atlantic occurred as a consequence of higher surface water productivity driven by the intensity of the trade winds, which control the lateral extension of the coastal upwelling off Namibia. Our results indicate that oceanic processes were responsible for enhanced of nutrient flux into the surface ocean in the Santos Basin during glacial stages. Consequently, there was an increase in organic matter delivered on the seafloor. The benthic foraminiferal assemblage distribution showed a strong correlation to the quantity and quality of organic material that reached the seafloor (Ohkushi et al., 2000). Several possible mechanisms for increased surface productivity in the Santos Basin can be proposed. Moreover, these mechanisms likely acted in concert, with variations in the influx of organic matter to the seafloor likely associated with changes in the influence of one or more of the mechanisms. One such mechanism is increased delivery of nutrients by extension of the influence of the La Plata River plume. In modern conditions, this plume extends over the continental shelf; during glacial intervals, with lower sea level and a narrower continental shelf, the influence of the plume could extend into the Santos Basin (Pivel, 2010). The seasonal variability of the river plume is controlled by the alongshore component of the wind stress (Piola et al., 2005). Several studies suggest that under favorable winds, the low salinity and productive waters of the La Plata River plume can extend northward over the shelf, in winter penetrating to latitudes as high as 23° (Campos et al., 1999; Pimenta et al., 2005; Piola et al., 2005). A numerical model demonstrated that the plume can shift farther up-coast and may possibly reach 23.8°S latitude under favorable southwesterly winds conditions blowing over the southwestern Atlantic shelf (Pimenta et al, 2005). The La Plata River contribution to the Santos Basin is supported by sedimentological evidence since the Oligocene (Cobbold et al., 2001). The transport of the La Plata River plume northward would have been enhanced during colder intervals via the enhanced influence of the Malvinas Current, which reaches its northern limits in the wintertime (Matano et al., 1993). According to Gaeta and Brandini (2006), the intrusion of the plume is one of the main mechanisms that enrich the photic zone of shelf waters with new nutrients. Thus, nutrient availability on the surface, provided by continental waters from the La Plata River plume, led to higher surface productivity and increased organic flux to the seafloor (Pivel et al., 2013). Another possible oceanic process is the shelf-break upwelling driven by BC cyclonic meanders. The SACW is nutrient-rich water mass but because of the thermocline stability, nutrients usually remain trapped in the subsurface (Lopes et al., 2006). Some physical processes (e.g., internal waves) can disrupt the thermocline, bringing the SACW to the surface and, as a result, fertilizing the photic zone by promoting coastal upwelling (Gaeta and Brandini, 2006). Cyclonic meanders of the BC are responsible for a relatively strong upwelling regime that pumps the SACW to the upper slope and continental shelf. During the summer, when the winds blow predominantly from the northeast

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Fig. 7. δ18O values of Cibicidoides wuellerstorfi, BFN, BFAR and factor loadings of the first four factors extracted based on Q-mode factor analysis of the benthic foraminiferal relative abundance data in core GL-854.

(NE), coastal upwelling occurs in response to the offshore Ekman transport near the surface. In the presence of meander-induced upwelling near the shelf-break, the combination of the two effects results in a strong mechanism capable of bringing the SACW from the slope regions to near the coast. On the other hand, during the winter, when coastal upwelling is diminished, the mechanism responsible for pumping the SACW onto the shelf is mainly by the meander-induced shelf-break upwelling (Campos et al., 2000). During glacial intervals, with lower sea level and a narrower continental shelf, the shelf-break upwelling would have enriched the ocean surface of the Santos Basin, increasing flux of organic matter to the seafloor. Higher influx of Aeolian dust to the Santos Basin during glacial intervals could be another potential fertilization mechanism, since dust supplies iron and other essential limiting micronutrients to the ocean surface (Martínez-Garcia et al., 2011). Flores et al. (2012) noted that iron fertilization of Subantarctic waters in the glacial ocean may account for the increased coccolithophorid abundance and surface productivity. In a study at Argentine Continental Margin, based on benthic foraminiferal assemblages, García-Chapori et al. (2014) observed that, during glacial intervals, the flux of carbon to the seafloor was generally enhanced and related the organic matter source to high quantities of dust produced in Patagonia and Argentinean Pampas, which was transported eastward into the South Atlantic by the westerly winds. Large quantities of dust over Argentine Continental Margin would have result in more nutrients available to the ocean surface in the southwestern Atlantic. Cold glacial climates shifted westerly winds equatorward (Toggweiler

et al., 2006). Thus, with stronger westerly winds blowing in a northernmost position, the ocean surface could have been enriched by nutrients carried by the higher flux of Aeolian dust. Finally, these mechanisms all likely contributed to enhanced primary productivity that provided organic matter to the Santos Basin, amplifying the response of benthic foraminiferal assemblages in the deep sea. Any organic matter that reaches the seafloor can influence the benthic ecosystem, but only the fresh material produced in the surface waters is indicative of real paleoproductivity in the surface water above the site (Guichard et al., 1999). Stronger seasonal productivity was indicated by peaks in relative abundances of E. exigua and A. weddellensis. Intervals with high abundance of these “phytodetritus species” can indicate seasonal deposition of phytodetritus from the ocean surface.

5. Conclusions Variations in surface productivity during the last 796.2 kyr over the southeastern Brazilian continental slope, induced by variations in seasonality and nutrient flux in surface waters, and that influenced influx of organic matter and oxygen concentrations at the seafloor, are recorded in benthic foraminiferal assemblages and accumulation rates. Data obtained from core GL-854 (Santos Basin) indicated that the organic matter influx was higher during glacial than interglacial stages. The dominance of Bolivina spp. assemblage from 769.2 kyr (MIS 19) to ~ 300 kyr (beginning of MIS 8), combined to higher BFAR values,

Fig. 6. Time series plots of benthic foraminiferal taxa with relative abundances N5% in at least one sample in core GL-854. (A) Relative abundance of benthic foraminiferal. (B) Relative abundance of dominant benthic foraminiferal species.

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Table 4 Factor scores of the first four factors from the Q-mode factor analysis of the benthic foraminiferal relative abundance data of core GL-854. Species Sigmoilopsis schlumbergeri Pyrgo spp. Quinqueloculina spp. Triloculinella pseudooblonga Alabaminella weddellensis Bolivina inflata Bolivina spp. Brizalina fragilis Bulimina aculeata Bulimina marginata Bulimina spp. Bulimina striata Buliminella elegantissima Cassidulina carinata Cibicidoides wuellestorfi Discorbis spp. Epistominella exigua Eponides alabaminaeformis Gavelinopsis versiformis Globocassidulina crassa Globocassidulina minuta Globocassidulina subglobosa Lobatula lobatula Loxostomum truncatum Nonion spp. Oridorsalis spp. Oridorsalis variapertura Paracassidulina sp. Pullenia quinqueloba Trifarina angulosa Uvigerina peregrina Uniloculares

Factor 1

Factor 2

Factor 3

Factor 4

−0.23 −0.23 −0.23 −0.20 −0.23 −0.65 0.95 −0.15 −0.10 −0.13 −0.26 −0.25 −0.19 −0.09 −0.22 −0.18 −0.90 −0.25 0.00 5.27 −0.30 0.05 −0.24 −0.24 −0.10 −0.10 −0.25 −0.23 −0.22 −0.02 −0.21 0.11

−0.27 −0.26 −0.23 −0.27 −0.54 0.50 5.18 −0.31 −0.28 −0.27 −0.30 −0.30 0.03 0.14 −0.25 −0.25 1.18 −0.16 0.00 −0.88 −0.04 −0.18 −0.21 −0.29 −0.06 −0.37 −0.27 −0.12 −0.28 −0.23 −0.34 −0.07

−0.19 −0.23 −0.26 −0.26 0.24 −0.59 −1.17 −0.16 −0.20 −0.22 −0.22 −0.22 −0.26 1.09 −0.16 −0.29 5.09 −0.01 −0.45 0.87 −0.15 −0.17 −0.25 −0.24 −0.34 −0.11 −0.19 −0.30 −0.17 −0.23 −0.01 −0.27

−0.26 −0.28 −0.16 −0.24 5.09 0.92 0.32 −0.19 −0.39 −0.39 −0.14 −0.15 −0.45 −1.46 −0.32 −0.28 0.00 −0.01 −0.44 0.07 −0.18 −0.18 −0.30 −0.16 −0.26 0.36 −0.30 −0.33 0.14 −0.22 −0.16 0.36

indicated a relatively high organic matter influx at the seafloor and reduced oxygen concentration at the sediment–water interface. Sea-surface productivity increased during glacial intervals in the Santos Basin, western South Atlantic, probably due to a combination of mechanisms including: (1) increased influence of the La Plata River plume associated with lower sea level and northern extension of the Malvinas Current, (2) shelf-break upwelling driven by BC cyclonic meanders, and (3) the higher flux of Aeolian dust to the ocean surface due to stronger westerly winds. From the interglacial MIS 7 (~223.3 kyr) this condition changed with the establishment of the Globocassidulina crassa assemblage, indicating a decrease in influx of organic matter influx and an increase in oxygen concentrations at the seafloor, becoming more similar to the modern low productivity environment in the western South Atlantic. Foraminiferal assemblages from subsequent glacial stages (MIS 6, 3 and 2) indicated more limited enhancement of surface primary productivity. Epistominella exigua and Alabaminella weddellensis assemblages indicated seasonal surface productivity. Intervals dominated by these assemblages indicated seasonal pulses of phytodetritus and high oxygen concentrations at the seafloor, which mostly occurred during the MIS 14, 11, 10, 9, 8, 6 and during the transition of sub-stages 5.2 to 5.1. The highest peak of the A. weddellensis assemblage during stage 11 (~401.4 kyr) coincides with the Mid-Brunhes Event, which according to previous research, is related to more humid interglacial conditions and the highest global carbonate production in response to the bloom of coccolithophore Gephyrocapsa, which may correspond to higher nutrient availability in the western South Atlantic during this interval. Acknowledgments This study greatly benefited from the contributions of Applied Micropaleontology Program funded by PETROBRAS S.A, São Paulo Research Foundation (FAPESP) grant 2013/50224-2, and bilateral

collaborative research council for international research between Salamanca University (Spain) and University of São Paulo (Brazil) grant 2011-9. The authors are thankful to PETROBRAS S.A for providing the samples to our study. Juliana P. Quadros is kindly acknowledged for building the age model and for helpful discussions. The fellow researchers Edmundo Camillo Jr. and Ana Claudia A. Santarosa provided beneficial discussions. Dr. Pamela Hallock Muller (University of South Florida, USA) is especially acknowledged for help to proofread on an early version of this manuscript, and two anonymous reviewers are acknowledged for their constructive criticisms and relevant comments, which led to substantial improvements. We are grateful to the Laboratório de Paleoceanografia do Atlantico Sul (LaPAS-IO/USP) staff for samples preparation.

Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.palaeo.2015.09.005.

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