Research papers

Distribution of living planktonic foraminifera in relationto oceanic processes on the southeastern continental Brazilianmargin (231S–251S and 401W–441W)

S.H.M. Sousa a,n, S.S. de Godoi a, P.G.C Amaral a, T.M. Vicente a, M.V.A. Martins b,c,M.R.G.S. Sorano a, S.A. Gaeta a, R.F. Passos a, M.M. Mahiques a

a Cidade Universitária Butantã, Instituto Oceanográfico, Departamento de Oceanografia Física, Química e Geológica, Praça do Oceanográfico, 191, CEP 05508-120 São Paulo, Brazilb Universidade do Estado do Rio de Janeiro, Faculdade de Geologia, Departamento de Estratigrafia e Paleontologia, Rua Francisco Xavier, 524, CEP 20550-013,Rio de Janeiro, RJ, Brazilc Universidade de Aveiro, Dpto. Geociências, GeoBioTec, CESAM, Campus de Santiago, 3810-193, Aveiro, Portugal

a r t i c l e i n f o

Article history:Received 17 January 2013Received in revised form13 November 2013Accepted 22 November 2013Available online 17 December 2013

Keywords:Planktonic foraminiferaWater-column habitatOligotrophic areaUpwellingPaleoceanographic proxies

a b s t r a c t

The vertical distribution (0 to 100 m) of planktonic foraminifera was investigated based on 40 tow samplesthat were collected in eight stations, during the austral summer of 2002, in a geographically restricted area(231S–251S and 401W–441W) on the southeastern Brazilian continental margin. Species' abundances arelow (less than 10 specimens/m3), which is typical of an oligotrophic area. The foraminifera assemblage ismainly composed of warmwater species (Globigerinoides ruberwhite and pink forms), with a predominanceof spinose and symbiont-bearing species. Temperature and inorganic nutrient enrichment of the surface arethe main factors that control foraminiferal abundance and diversity; nevertheless salinity can also influencethe ecological descriptors. The role of the deep chlorophyll maximum (DCM) in the distribution offoraminifera is not always clear, but the increase in the abundance of G. ruber (white and pink) seems tobe related to a deeper DCM, and high salinities (S436.5). The ecological habitat of these species is affectedby the depth of the mixed layer, with a predominance of the white form in deeper layers. Increases in theforaminiferal diversity are related to the dynamics of the Brazil Current system, which displaces the area ofhigh productivity in the euphotic zone off the coast. The abundances of Globigerina bulloides, Globigerinafalconensis, Globigerinella calida and Globigerinella siphonifera follow the nutrient enrichment of the surfacewater mass, corroborating the usefulness of these species as paleoproductivity proxies in the study area.These data confirm the use of diversity measurements and assemblages composition for reconstructing pastwater column structures in subtropical oceans.

& 2013 Elsevier Ltd. All rights reserved.

1. Introduction

Among the open ocean pelagic organisms, planktonic foramini-fera is one of the most abundant groups. Their calcite skeletons areabundantly preserved in oceanic sediments, covering more than50% of the sea floor (Bé and Tolderlund, 1971). These organisms alsoexhibit a widespread distribution due to their passive transport byocean currents, and their spatial distribution, assemblage variabilityand test properties (e.g., wall texture, individual shell size-range)are strongly influenced by environmental parameters (Fairbankset al., 1980, 1982; Boltovskoy et al., 1996, 2000; Bergami et al., 2009,among others). Due to their specific environmental requirements,

such as water temperature, salinity and food availability (Bé andHutson, 1977; Fairbanks and Wiebe, 1980; Hemleben et al., 1989;Bijma et al., 1990; Kuroyanagi and Kawahata, 2004), the presence ofspecies of this group may be used to infer water mass properties(Ottens, 1991; Oberhänsli et al., 1992; Ufkes et al., 1998). Therefore,planktonic foraminifera have been used for paleoenvironmentaland paleoceanographic reconstructions. However, a better under-standing of the relationship between horizontal and vertical for-aminiferal distribution in the water column and the oceanographicsettings is a prerequisite for improving our knowledge of theenvironmental factors that control the modern distribution of theseorganisms, and, consequently, refining past reconstructions.

Also, biogeographical studies are strongly dependent on analyses ofvertical and horizontal distribution patterns and seasonal changes inthe composition of planktonic foraminifera assemblages (Boltovskoy,1981, 1994; Hemleben and Kemmle-von Mucke, 1999; Boltovskoyet al., 1996, 2000). According to Boltovskoy (1994), living taxain the water column have broad horizontal distribution ranges that

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Continental Shelf Research

0278-4343/$ - see front matter & 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.csr.2013.11.027

n Corresponding author. Tel.: þ55 1130916655; fax: þ55 1130916610.E-mail addresses: smsousa@usp.br,

silviahelenamello@gmail.com (S.H.M. Sousa).

Continental Shelf Research 89 (2014) 76–87

do not correspond to climatic zones on the ocean's surface, and cantherefore mislead the biogeographic interpretation of sediment-basedsurveys.

Knowledge about the ecology and distribution of living plank-tonic foraminifera is scarce and fragmentary for the southeasternBrazilian continental margin, which is characterised by oligotrophicwaters (Ciotti and Kampel, 2001). As mentioned by Boltovskoy(1994), plankton samples represent an insignificant proportion ofthe total time at which seasonal and inter-annual variability operate,compared to sediment trap samples, which provide more informa-tion. However, many of the gaps in our knowledge require analysesof planktonic material. Therefore, the present study focuses on thefactors that control planktonic foraminifera population during theaustral summer of 2002 in the surface waters of the south-westernAtlantic Ocean, between 231S–251S and 401W–441W. The region islocated in the subtropical faunal province (thermic regimes between18 and 24 1C) according to Bé and Tolderlund (1971).

To determine the factors that control the vertical distribution offoraminifera, we conducted plankton tows along the southeasternBrazilian margin in regions that are affected by different hydro-graphic regimes. The material was collected in the upper 100 mof the water column, along with measurements of temperature,salinity, and chlorophyll-a. The distribution of selected livingspecies in the water column and their occurrence in the surfacesediments (Passos, 2006; Sorano, 2006) were also compared. The goalwas to contribute to a better understanding of the sedimentarydistribution pattern and to provide guidelines for the application ofplanktonic foraminifera to the fossil record in paleoceanographicreconstructions.

2. Oceanographic setting

In the southeastern Brazilian continental margin, the currentstructure is linked to the displacement of the South Atlantic westernboundary current system. According to Silveira et al. (2000) thissystem is composed of Brazil Current (BC), Intermediate WesternBoundary Current (IWBC) and Deep Western Boundary Current(DWBC). This structure associated with the water masses is dia-grammed in Fig. 1 (upper panel), which is based on the pattern flowdiagram of the large-scale circulation retrieved from Stramma andEngland (1999) and adapted from Soutelino (2008). Between 101Sand 201S, the South Equatorial Current (SEC) bifurcates and itsnorthern and southernmost branches constitute, respectively, theBC and the North Brazil Current (NBC) (Stramma and England, 1999).

In the study area, the BC flows south-southwest from the surfaceto approximately 500 m depth, and transports Tropical Water (TW)and South Atlantic Central Water (SACW). The BC can flow atmaximum speeds of approximately 0.8 m/s. The TW (T420 1C;S436) occupies the oceanic mixed layer, and its vertical distribu-tion is restricted to the upper 150 m. According to Mémery et al.(2000), the TW core is associated with the subsurface salinitymaximum (S437). Beneath the TW, the SACW (6 1CoTo20 1C;34.6oSo36) is defined as the pycnocline water mass and extendsvertically from 150 m to approximately 500 m depth.

Coastal Water (CW), which is a result of the mixture of thecontinental freshwater discharge and waters of the continentalshelf, flows between the coast and inner shelf. This water mass ischaracterized by salinities lower than 34, mainly due to thecombined effect of many small and medium rivers in the region(Castro et al., 2006).

The IWBC flows north-northeast below the pycnocline, trans-porting Antarctic Intermediate Water (AAIW). In the deeper layers,the DWBC, flows south-southwest, transporting North AtlanticDeep Water (NADW).

Since our focus is on the upper 100 m of the water column,information about water masses and current structures will berestricted to the surface layer and the first few metres of thepycnocline.

Fig. 1 (lower panel) exhibits coastal and oceanic processeswhich occur in the study area. Coastal upwelling and the CaboFrio eddy are observed year-round offshore Cabo Frio. Anotherfeature in this area is the inner front of the BC, which is formed bythe BC, its meanders, eddies and the adjacent coastal currentsystem. Lorenzzetti et al. (2009) used satellite observations tostudy this front and reported that the gradients of sea surfacetemperatures have a seasonal variability of approximately 0.24 1C/kmduring summer and 0.33 1C/km during autumn.

A seasonal cycle in the direction of the prevailing wind in theCabo Frio area establishes a seasonal Ekman-driven upwellingregion. During summer, the dominant NE wind direction favoursthe CW motion offshore and subsurface penetration of the SACWto shallower areas. The coastal upwelling process is normallycharacterised by an outcropping of the 18 1C isotherm and the36 isohaline, which correspond to the 26 kg/m3 isopycnal (Castroet al., 2006). The chlorophyll-a concentration varies between 0.0and 2.35 mg/m3 during winter and between 0.0 and 25.5 mg/m3

during summer (Gaeta and Brandini, 2006).Similarly to other western boundary fronts (i.e., Oda and

Yamasaki, 2005), the BC frontal interface plays an important rolein the biogeochemical cycle in the region. The occurrence ofcyclonic eddies along the BC front can increase primary produc-tivity (Matsuura, 1986; Gaeta et al., 1999; Ciotti and Kampel, 2001).The eddy's orbital circulation advects productive shallow watersfrom the upwelling front offshore. This process can introduce coldand inorganic nutrient-rich water, which can modify the oligo-trophic conditions in the oceanic regions and enhance primaryproductivity in the superficial waters (Ciotti and Kampel, 2001).Occasionally, shelf break upwelling can occur, with penetration ofthe SACW into the euphotic zone in the shallower regions, asnoted by Campos et al. (2000) and Silveira et al. (2000).

Based on a numerical simulation, Calado et al. (2010) recog-nised that near Cabo de São Tomé, the coastal and oceanic systemsinteract, and the presence of the BC and its cyclonic meanders canenhance coastal upwelling. According to these authors, this eddy-induced upwelling may intensify the prevalent coastal upwellingdue to wind and topographic effects.

3. Material and methods

The analysed material was collected during austral summer(January 2002) as part of the DEPROAS expedition (Dinâmica doEcossistema de Plataforma da Região Oeste do Atlântico Sul) to thesoutheastern Brazilian continental margin. Samples were collectedalong 14 transects that were perpendicular to the coastline. In thepresent study, we discuss the results obtained from five of thetransects (Fig. 1—lower panel, and Table 1).

Temperature and salinity measurements were collected with aconductivity, temperature and depth (CTD) profiler—FallmouthScientific Instruments (FSI), model BCTD-BPBIO. Two to six litres ofseawater samples were used for chlorophyll-a collection usingWhatman-GF/F glass microfiber filters (o10 mm Hg). Chlorophyll-a concentrations were obtained by using a Turner fluorometer 10-AU-005, at the Primary Productivity Laboratory of the OceanographicInstitute of the University of São Paulo, following the methodologysuggested by Welschmeyer (1994).

Vertical profiles of temperature, salinity, chlorophyll-a and stand-ing stock (specimens/m3) for selected planktonic foraminifera spe-cies, between the surface and 100 m depth, were constructed for allof the plankton tow stations (see Fig. 1—lower panel). Based on these

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profiles, cross-shelf sections of temperature, salinity, conventionaldensity (sigma-T) and chlorophyll-a were constructed for threetransects (T1 to T3) in order to get a better understanding of theecological controls affecting the vertical distribution of foraminifera.The transects for these properties were prepared using objectiveanalysis anisotropic techniques (Bretherton et al., 1976; Carter andRobinson, 1987), with horizontal and vertical correlation lengthsequal to 50 km and 50 m, respectively. The mean square error was0.05 (Silveira et al., 2004). In order to enhance the gradients,

chlorophyll-a cross-shelf sections were presented in log scale. Wealso calculated the total vertically integrated chlorophyll-a concen-tration (μg m�2) over the water column at each station.

The plankton tows were conducted using a multi-planktonsampler (63 μm mesh size) in the upper 100 m of the watercolumn and were divided into five depth intervals (0 to 20 m, 20to 40 m, 40 to 60 m, 60 to 80 m and 80 to 100 m) at eightoceanographic sites (Fig. 1—lower panel) between 6:00 a.m. and6:00 p.m. Plankton tow samples were stored in a 4% formaldehyde

26˚S

25˚S

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23˚S

22˚S

21˚S

−200m

−1000

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7110

7120

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7144

7154

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Brazil

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Sepetiba

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Plankton tow stations

Oceanografic stations

Transects

Legend:

Brazil Current

Cabo Frio cyclonic eddy

Cabo Frio upwelling L

L

T1 to T5

Fig. 1. (Upper panel)—Schematic representation of the vertical structure of the western boundary currents and associated water masses off the eastern and southeasternBrazilian coast: Coastal Water (CW—green); Brazil Current (BC)—Tropical Water (TW—red) and South Atlantic Central Water (SACW—turquoise); Intermediate WesternBoundary Current (IWBC)—Antarctic Intermediate Water (AAIW—cyan); North Atlantic Deep Water (NADW—blue); Deep Western Boundary Current (DWBC); SouthEquatorial Current (SEC); North Brazil Current (NBC); North Brazil Undercurrent (NBUC). Based on Stramma and England (1999) and Soutelino (2008). (Lower panel)—Mapwith the location of the oceanographic stations, plankton tow stations during the January 2002 DEPROAS expedition, austral summer. General oceanographic features of theBrazil Current, Cabo Frio cyclonic eddy and Cabo Frio upwelling in the southeastern Brazilian continental margin. (For interpretation of the references to color in this figurelegend, the reader is referred to the web version of this article.)

S.H.M. Sousa et al. / Continental Shelf Research 89 (2014) 76–8778

solution that was buffered with sodium borate (pH48). We didnot use Rose Bengal solution in order to distinguish Globigerinoidesruber (pink) and G. ruber (white). The total volume of filteredwater from each station was calculated according to Tanaka (1973).

In the laboratory, the samples were filtered through a 100 mmmesh, according to Boltovskoy et al. (1996), to separate the juvenilespecimens, which could not be accurately identified. The planktonicforaminifera specimens that were present in the fraction that wassieved through the 100 mmmesh size were isolated, counted andidentified to the species level following Postuma (1971), Kennett andSrinivasan (1983), Hemleben et al. (1989) and Jones (1994), amongothers.

In order to have a better insight into the general response ofplanktonic foraminifera to the abiotic factor, we calculated diver-sity using the Shannon–Weaver index (H0, loge) (Shannon andWeaver, 1963), although in most of the stations the abundance waslower than 100 individuals. According to some authors (e.g.,Al-Sabouni et al., 2007), 300 individuals would be the minimumsample-size for the estimation of diversity values of planktonicforaminifera species present in sediments.

The Spearman correlation analysis was performed consid-ering po0.05 as the significant level. The species from all thestations were correlated with temperature, salinity, sigma-T andchlorophyll-a. In addition, species composition and diversity

measurements were correlated with total vertically integratedchlorophyll-a values.

4. Results

4.1. T1—Ilha Grande transect (planktonic tow stations 7110, 7109)

Eight planktonic foraminifera species were identified alongtransect T1. The assemblage was composed of Globigerina bulloides,Globigerina falconensis, G. ruber (white and pink), Globigerinoidessacculifer, Globigerinella siphonifera, Globorotalia menardii, Neoglo-boquadrina dutertrei and Orbulina universa (Fig. 2). G. ruber (white)and G. ruber (pink) were the most abundant species at stations7109 and 7110, with the sum of both forms reaching 75% of thetotal for the transect. Other species had relative abundances thatwere lower than 7%, with the exception of G. siphonifera, whichreached 21% at station 7110 (Fig. 2, Table 2). Here, the greatestabundance of G. ruber (white) and G. ruber (pink) (1.4 and0.5 specimens/m3, respectively) occurred in the 40–60 m depthinterval. Also in this depth interval, an increase in the abundanceof G. siphonifera (1.0 specimens/m3) was observed. At station 7109,G. ruber (white and pink) reached its maximum abundance(1.1 and 0.6 specimens/m3, respectively) in the depth intervalfrom 0 to 40 m (Fig. 3a and b).

At station 7110, the deep chlorophyll maximum (DCM)occurred at approximately 77 m depth, and was observed at100 m depth at station 7109 (Fig. 3a and b).

4.2. T2—Sepetiba transect (planktonic tow stations 7121, 7120)

Along T2, five planktonic foraminiferal species were identified.The assemblage was composed of G. bulloides, G. ruber (white andpink), G. sacculifer, G. siphonifera and N. dutertrei (Fig. 2). Similar totransect T1, the most abundant species was G. ruber (white andpink). The maximum relative abundance of this species was 82%,while the other species reached 10% of the maximum relative

Fig. 2. Histograms showing the relative abundances of the foraminifera species in the water column from surface to 100 m depth: T1—Ilha Grande, T2—Sepetiba, T3—CaboFrio, T4—Northern Cabo Frio and T5—Cabo de São Tomé transects.

Table 1Locations of the tow stations and sea-floor depths.

Tow station name Latitude Longitude Seafloor depth (m)

7109 24127.960S 43145.470W 7877110 24109.020S 43153.040W 1557120 24119.750S 43102.000W 11217121 24101.490S 43109.960W 2757142 23136.790S 41147.060W 1607144 24114.080S 41131.340W 19527154 23134.940S 41100.950W 15657165 23117.050S 40122.200W 2522

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Table 2Tow sampling depth, volume of filtered water (m3), standing stocks (specimens/m3) and absolute counts of planktonic foraminifera species collected at each station.

Stations Samples Volume of waterfiltered (m3)

Standing stock(specimens/m3)

Globigerinabulloides

Globigerinafalconensis

Globigerinellacalida

Globigerinoidesruber (pink)

G. ruber(white)

Globigerinoidessacculifer

Globigerinellasiphonifera

Globorotaliamenardii

Neogloboquadrinadutertrei

Orbulinauniversa

7109 0–20 22.86 1.66 3 0 0 14 20 1 0 0 0 0 3820–40 15.84 2.34 2 0 0 10 18 2 3 1 0 1 3740–60 14.84 0.74 0 0 0 2 4 0 2 1 0 1 1060–80 13.8 0 0 0 0 0 0 0 0 0 0 0 080–100 49.73 0.2 2 1 0 0 0 1 0 4 0 0 8

7110 0–20 20.71 0 2 0 0 8 3 0 1 0 0 0 1420–40 17.29 0.68 3 0 0 4 12 0 3 0 0 0 2240–60 16.49 3.09 1 0 0 8 23 1 17 0 1 0 5160–80 23.62 1.35 2 1 0 4 17 1 4 0 3 0 3280–100 69.07 0.33 5 1 0 2 9 0 2 0 4 0 23

7120 0–20 38 3.5 5 0 0 95 24 6 3 0 0 0 13320–40 11.82 2.12 1 0 0 15 6 0 1 0 2 0 2540–60 2.11 13.25 3 0 0 3 20 0 0 0 2 0 2860–80 10.12 1.28 4 0 0 3 4 1 0 0 0 0 1280–100 17.46 0 0 0 0 0 0 0 0 0 0 0 0

7121 0–20 46.61 1.39 0 0 0 46 17 1 1 0 0 0 6520–40 18.53 0 0 0 0 0 0 0 0 0 0 0 040–60 12.32 1.14 2 0 0 3 5 0 1 0 2 0 1360–80 14.22 0 0 0 0 0 0 0 0 0 0 0 080–100 23.28 0 0 0 0 0 0 0 0 0 0 0 0

7142 0–20 27.06 1.55 0 0 1 23 17 0 0 0 0 0 4120–40 20.22 0.3 3 0 0 2 1 0 0 0 0 0 640–60 26.41 0 0 0 0 0 0 0 0 0 0 0 060–80 20.14 0.5 3 0 1 2 1 0 1 0 1 1 1080–100 21.79 0.73 3 5 1 0 3 0 3 0 0 0 15

7144 0–20 13.24 6.57 4 0 3 33 39 0 1 5 1 1 8720–40 16.85 1.72 1 0 0 6 12 0 2 5 3 0 2940–60 22.9 1.4 4 0 0 5 17 0 2 2 0 1 3160–80 17.78 2.47 3 2 2 5 2 0 8 10 6 4 4280–100 14.54 0.83 0 1 1 0 5 1 3 0 1 0 12

7154 0–20 26.71 3.97 5 0 1 63 23 3 0 10 0 0 10520–40 15.15 4.95 3 0 1 55 14 0 0 2 0 0 7540–60 19.64 1.43 0 0 0 16 10 0 0 2 0 0 2860–80 54.51 0.9 1 0 0 8 40 0 0 0 0 0 4980–100 16.13 3.6 9 1 0 5 38 4 1 0 0 0 58

7165 0–20 31.73 7.91 16 0 1 112 102 6 0 15 0 0 25220–40 18.17 1.43 5 0 0 8 10 0 0 2 0 0 2540–60 24.39 0 0 0 0 0 0 0 0 0 0 0 060–80 29.57 0.34 1 0 1 2 2 0 0 1 1 1 980–100 28.43 0 0 0 0 0 0 0 0 0 0 0 0

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Fig. 3. Vertical distribution of the planktonic foraminifera species standing stocks (specimens/m3) and temperature (1C), salinity, sigma-T (kg/m3) and chlorophyll-aconcentration (μg/L): T1—Ilha Grande transect (a and b); T2—Sepetiba transect (c and d); T3—Cabo Frio transect (e and f); T4—Northern Cabo Frio transect (g) and T5—Cabode São Tomé transect (h). Gray diamonds indicate temperature, dark circles indicate salinity, white triangles indicate chlorophyll-a concentration and black stars indicatesigma-T.

S.H.M. Sousa et al. / Continental Shelf Research 89 (2014) 76–87 81

abundance (Fig. 2, Table 2). At station 7121, G. ruber (pink) was themost abundant species (0.99 specimens/m3), occurring mainly inthe surface layer (0 to 20 m water depth; Fig. 3c). Conversely, atstation 7120, G. ruber (white) was dominant (up to 9.48 speci-mens/m3), generally in the 40 to 60 m depth interval (Fig. 3d,Table 2). Similarly to station 7110, the DCM occurred at 77 mwaterdepth at stations 7121 and 7120 (Fig. 3c and d).

4.3. T3—Cabo Frio transect (planktonic tow stations 7142, 7144)

T3 showed the highest number of species, (i.e., nine): G. bulloides,Globigerina calida, G. falconensis, G. ruber (white and pink),G. sacculifer, G. siphonifera, G. menardii, N. dutertrei and O. universa(Fig. 2). The two forms of G. ruber were also most abundant (63%)here. The species G. calida, which was not found in the southernmosttransects, was observed along T3, reaching 4.6% relative abundance.Along this transect, G. bulloides and G. falconensis showed the highestrelative abundance values (14.5 and 7%, respectively, at station 7142;Fig. 2, Table 2). Although a high diversity (number of species) wasobserved along T3, there were low abundance values (0.04 to0.8 specimens/m3) at station 7142 (Fig. 3e). G. ruber (pink) was thepredominant species at this station, mainly in the 0 to 20 m waterdepth interval. At station 7144, however, the abundance was higher,reaching nearly 3 specimens/m3 in the surface layer (0 to 20 mwaterdepth), and was dominated by G. ruber (white) (Fig. 3f). The DCMoccurred at 50 m depth at station 7142 and it was observed at 100 mdepth at station 7144 (Fig. 3e and f).

4.4. T4 – Northern Cabo Frio and T5 – Cabo São Tomé transects(planktonic tow stations 7154 and 7165)

At station 7154, seven planktonic foraminiferal species wereobserved: G. bulloides, G. calida, G. falconensis, G. ruber (white andpink), G. sacculifer, G. siphonifera and G. menardii. The two forms ofG. ruber (white and pink) were the most abundant (46 and 34%,respectively). Among the other species, G. bulloides showed thehighest relative abundance (10%) (Fig. 2, Table 2). In the watercolumn, the highest abundance of G. ruber (pink) was observedbetween 0 and 60 m water depth (ranging from 0.8 to 3.6 speci-mens/m3). In the 60 to 100 m water depth interval, the speciesG. ruber (white) was the predominant species, reaching 2.4 speci-mens/m3 (Fig. 3g).

The northernmost station (7165) showed seven planktonicforaminiferal species: G. bulloides, G. calida, G. ruber (white andpink), G. sacculifer, G. menardii, N. dutertrei and O. universa. Similarto the other stations, there was a predominance of G. ruber (white)(39%) and G. ruber (pink) (42%). G. bulloides (8%) and G. menardii(6%) were the most important accessory species (Fig. 2, Table 2).The highest abundance (3.5 specimens/m3) of species was found inthe surface layer (0 to 20 m water depth) (Fig. 3h, Table 2). TheDCM was observed at 100 m water depth at stations 7154 and7165 (Fig. 3g and h).

4.5. Cross-shelf sections

Three cross-shelf sections of temperature, salinity, sigma-T andchlorophyll-a at transects T1 (Fig. 4a–c, Fig. 5a), T2 (Fig. 4d–f,Fig. 5b) and T3 (Fig. 4g–i, Fig. 5c) are shown to illustrate the mainoceanographic features in the study area. Based on the verticalstructure of temperature and salinity, TW and SACW were identi-fied. The core of TW occurs at approximately 60 m depth, wheresalinity is greater than 37 (Fig. 4a–c).

The evolution of the depth of the thermal front between TWand SACW can be observed from transect T1 (Fig. 4a) to transect T2(Fig. 4d). The largest temperature and salinity ranges wereobserved at station 7110 (transect T1), where temperature varied

progressively from 24.74 1C at the surface to 16.08 1C at 100 mdepth, and salinity ranged from 35.2 to 36.8 (Figs. 3 and 4a). Onlyat transect T3 does the 18 1C isotherm reach the surface. Thishappened at approximately 10 km away from the coast, denotingthe coastal upwelling, which is marked by mixing of CW and SACW.In general, highest salinity values (S437) were found offshore,which characterise the BC core's maximum salinity at the subsur-face. As expected, the sigma-T vertical structure follows the samepattern as the temperature at transects T1 and T2 (Fig. 4c and f).At transect T3, the vertical structure of sigma-T (Fig. 4i) reveals thecoastal upwelling front between stations 7140 and 7141.

The vertical distribution of planktonic foraminiferal abundancereaches its maximum value (more than 10 specimens/m3)between 40 and 60 m water depth at transect T2 (station 7120)(Fig. 4d and e) and in shallow layers of transect T3 (station 7144)(Fig. 4g and h). In general, these values occurred at sites withmaximum salinity (S437) and temperature (T425 1C), whichcharacterise the presence of TW.

The cross-shelf sections of chlorophyll-a show a gradient fromthe inner shelf to offshore, which follows approximately thethermal front between the TW and the SACW. Maximum values(42 μg/L) are located from the coast to approximately 20 kmoffshore (Fig. 5a–c). At transect T3, where coastal upwelling isobserved, highest values (up to 0.6 μg/L) are observed from thesurface down to approximately 40 m water depth (Fig. 5c).

The maximum abundance values of G. ruber (white and pinkforms) occurred at sites offshore characterized by low chlorophyll-a values (less than 0.32 μg/L at T2, station 7120; and at T3, station7144) (Fig. 5b and c). Conversely, the maximum abundance ofG. bulloides, G. calida, G. falconensis and G. siphonifera (Figs. 2 and 3a,Table 2) is observed at transects T1 (station 7110) and T3 (station7142), characterized by an enrichment of chlorophyll-a in the watercolumn (values range from 0.32 to 1.0 μg/L) (Fig. 5a and c).

4.6. Foraminiferal diversity and chlorophyll-a concentrations

In order to identify a possible influence of total chlorophyll-aintegrated over the water column on diversity values, both datawere plotted together (Fig. 6). As a general feature, it is possible toidentify the occurrence of the highest diversity values in siteswhere the thermal front between TW and SACW is observed.These sites are characterized by higher integrated chlorophyll-aconcentrations (60.96 μg/m2 at T1, station 7110; 66 μg/m2 at T3,station 7142; 41.83 μg/m2 at T3, station 7144) and diversity values(1.47 at station 7110; 1.58 at station 7142; 1.78 at station 7144)(Fig. 6). The Spearman correlation analysis show that the verticallyintegrated chlorophyll-a values have a significant positive correla-tion with diversity measurements (ρ¼0.5714).

5. Discussion

In general, the abundance of planktonic foraminifera is low(from 0.01 to 9.5 specimens/m3), most likely due to the oligo-trophic conditions in the study area. Kuroyanagi and Kawahata(2004) observed a site located within the Kuroshio Current that isalso characterized by oligotrophic conditions and relatively lowforaminiferal standing stocks throughout the water column (from1.1 to 3.5 shells/m�3). As expected, an increase in the abundanceof planktonic foraminifera was observed towards offshore areas.

The assemblage of planktonic foraminifera was mainly com-posed of warm water species (e.g. G. ruber white and pink forms),with the exception of G. bulloides, which has either a higheraffinity for cold waters (Bé, 1977; Boltovskoy et al., 1996) or apreference for productive environments (Hemleben et al., 1989;Hilbrecht, 1996, among others), and O. universa, which seems to be

S.H.M. Sousa et al. / Continental Shelf Research 89 (2014) 76–8782

related only with sea surface salinity, with a maximum abundancebetween 35.5 and 36.0, according to Hilbrecht (1996). A predomi-nance of spinose and symbiont-bearing foraminifera species was

observed in the study area (e.g. G. ruber white and pink forms),excluding G. menardii, N. dutertrei (non spinose) and G.bulloides(symbiont barren), according to Hemleben et al. (1989).

Fig. 4. Cross-shelf sections of T1—Ilha Grande, T2—Sepetiba and T3—Cabo Frio transects: temperature (a, d and g); salinity (b, e and h) and sigma-T (c, f and i). White circlesrepresent the planktonic foraminifera frequencies (specimens/m3).

Fig. 5. Chlorophyll-a concentration (μg/L) cross-shelf sections, (a) T1—Ilha Grande, (b) T2—Sepetiba and (c) T3—Cabo Frio transects. The color scale is logarithmic. Whitecircles represent the planktonic foraminifera frequencies (specimens/m3). (For interpretation of the references to color in this figure legend, the reader is referred to the webversion of this article.)

S.H.M. Sousa et al. / Continental Shelf Research 89 (2014) 76–87 83

5.1. Factors controlling the vertical distribution of G. ruber (white)and G. ruber (pink)

The spinose G. ruber (white and pink) is considered a warm andsurface-dwelling species (Hemleben et al., 1989; Hilbrecht, 1996).This species prevails in food-poor oligotrophic regions (e.g., centralequatorial Pacific) because it obtains nutrients from its endosym-bionts (Watkins et al., 1996). Data obtained in this study demon-strate that the pink form peaked in abundance in warmer (betweenca. 24 and 26 1C) and surface (from 0 to 20 m) waters, with a meansalinity of 36.5 in most of the stations (Fig. 3). G. ruber (white) alsohad maxima in 0 to 20 m depth at stations 7144 and 7165 (Fig. 3fand h). Additionally, the white form peaked in abundance in 40 to60 m and 80 to 100 m water depth at stations 7120 and 7154,respectively (Fig. 3d and g). The significant positive and negativecorrelations of G. ruber (white and pink), respectively, with tem-perature (ρ¼0.5088 and ρ¼0.7054) and chlorophyll-a concentra-tion (ρ¼�0.3438 and ρ¼�0.4582), confirm their preference forwarmer temperatures (Hilbrecht, 1996; Conan et al., 2002) andoligotrophic conditions (Bé et al., 1985; Watkins et al., 1996).

The observed abundance of these two forms in the overlyingmixed layer supports previous works (Bé et al., 1985; Hemlebenet al., 1989). The vertical distribution of G. ruber (white) andG. ruber (pink) is mainly controlled by the thickness of the mixedlayer (Hemleben et al., 1989), with maximum frequencies of thewhite formwhen the mixed layer is deeper, as with the occurrenceof G. ruber (white) in the eastern South Atlantic Ocean (Ufkes et al.,1998). Our findings compare well with the sea surface tempera-ture (SST) tolerance range observed by Zaric et al. (2005). Addi-tionally, the increase in the abundance of G. ruber (white and pink)seems to be related to deeper DCM (Fig. 3d and f–h), in conditionsof maximum salinity (S436.5), due to the presence of the BC core(Fig. 4), lower phytoplankton biomass availability and diversityvalues (Fig. 6).

5.2. Factors controlling the vertical distribution of other species

In general, the abundances of the other species (i.e., G. bulloides,G. calida, G. falconensis, G. sacculifer, G. siphonifera, G. menardii,N. dutertrei and O. universa) were lower than G. ruber (Table 2). Theincrease in diversity observed at T1 and T3 (Fig. 6) may befavoured by the presence of the internal front between TW andSACW, which enhances the chlorophyll-a contents in the upperlayers of the water column (Fig. 5a and c). The Cabo Frio region ischaracterised by the upwelling of the SACW and the BC meanders(station 7144) (Fig. 1—lower panel). The simultaneous occurrence

of the coastal upwelling front, the Cabo Frio eddy, and the inner BCfront, identified by its meandering pattern, were evident in thestudy area, as illustrated in Fig. 7.

This scenario may be influenced by colder water from theupwelling coastal region in the proximity of the edge of thecyclonic eddy, which is advected and promotes the developmentof a relatively warmer “false” vortex core (Calado, 2006). Addi-tionally, the significant positive correlation between verticallyintegrated chlorophyll-a and diversity measurements demon-strates that the set of oceanographic processes in the study area,which enhanced the surface water stratification, most likelyincreased the diversity of species that were sampled at stations7110, 7142 and surroundings, corroborating with the findings ofAl-Sabouni et al. (2007) for mid-latitudes in the Atlantic Ocean.

Our data confirm that sea surface temperature and inorganicnutrient enrichment at the surface are the determinant factors forthe diversity of planktonic foraminifera, most likely through thecontrol of the vertical niche separation in the water column, assuggested by Rutherford et al. (1999). This fact, associated with thelow abundance of planktonic foraminifera specimens, seems tocontradict Irigoien et al. (2004), who found that global zooplanktondiversity is a function of zooplankton biomass. Our results arecomparable to results from the Japan Sea, which is characterizedby the presence of the Kuroshio Current and, similarly to the BC, ismarked by warm and relatively low productivity waters (Kuroyanagiand Kawahata, 2004).

Moreover, at stations located at the interface between TW andSACW (7110, 7142), a greater abundance of asymbiotic speciesG. bulloides and symbiotic-bearing species G. siphonifera wasobserved (Fig. 2). The former species is generally considered tobe sub-polar (Bé, 1977; Hemleben et al., 1989) or transitional/subtropical (Boltovskoy et al., 1996, 2000; Hemleben et al., 1989)and also characteristic of nutrient-rich upwelling areas, such asthose in the eastern South Atlantic Ocean (Ufkes et al., 1998;Kemle-von Mücke and Oberhänsli, 1999, among others), ArabianSea (Zaric et al., 2005) and the Indian Ocean (Duplessy et al., 1981).

Fig. 7. Temperature (1C) map from CTD casts overlaid with geostrophic velocity (m/s)at 5 m depth, according to Calado (2006). The map was interpolated using isotropicobjective analysis (Carter and Robinson, 1987) to refine the main oceanographicfeatures.

0

10

20

30

40

50

60

70

1.0

1.2

1.4

1.6

1.8

7109 7110 7120 7121 7142 7144 7154 7165

Fig. 6. Diversity values as a function of total integrated chlorophyll-a over thewater column values for the stations 7109, 7110, 7120, 7121, 7142, 7144, 7154, 7165.

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According to Hilbrecht (1996), G. bulloides is most abundant inwater masses at high southern latitudes and has distinct max-imum in high northern latitudes and low latitude upwellingregions.

In contrast, Zaric et al. (2005) observed the highest relativeabundance of G. siphonifera at lower export production rates wherefluxes were comparably small. It should also be pointed out thatDNA based studies conducted by De Vargas et al. (2002) demon-strated the occurrence of four different genotypes of G. siphoniferain the Atlantic Ocean. According to these authors, each G. siphoniferagenotype is adapted to different chlorophyll concentrations.

The increase in relative abundance of G. siphonifera and ofG. bulloides at T1 and T3 indicate an influence of the nutrientenrichment of the euphotic zone on the development of thesespecies. We suggest that the nutrient enrichment is due to theoffshore advection of shallow waters from the Cabo Frio coastalupwelling by a cyclonic eddy (Fig. 7) (station 7142), and due to thepresence of the deep thermal front between TW and SACW. Thisfront is characterised by the 18 1C isotherm (station 7110) (Fig. 4a)and relatively high chlorophyll-a concentration (Fig. 5a and c).These findings support the notion that the distribution of thesespecies in the study area appears to be controlled mainly byvariations in primary production rather than by water tempera-ture, corroborating findings from Hemleben et al. (1989) andHilbrecht (1996).

Furthermore, G. falconensis and G. calida are found in theupwelling regions of the study area (Fig. 3a–c), in agreement withOrtiz and Mix (1992) and Duplessy et al. (1981). G. falconensisexhibits maximum fluxes in the near-shore area, most likely inresponse to coastal upwelling, as stated by Ortiz and Mix (1992).Additionally, the abundance of G. falconensis shows a significantnegative correlation with temperature (ρ¼�0.3405), and alsopositive correlation with total vertically integrated chlorophyll-a(ρ¼0.8539), which confirm their preference for productive envir-onments. The species G. calida was reported by Duplessy et al.(1981) as a prolific species in the tropical upwelling assemblage,together with G. bulloides and N. dutertrei, off the southern tip ofIndia. N. dutertrei has been observed from tropical to warmtransitional regions (Bé, 1977; Hemleben et al., 1989; Boltovskoyet al., 1996). We observed this species at the DCM (station 7110),and peaks in its abundance were observed at the base of orjust below the mixed layer (stations 7120, 7121, 7144). However,based on our data, the ecological inferences for this species areinconclusive.

The species G. menardii and O. universa are distributed fromtropical to warm transitional regions (Bé and Tolderlund, 1971;Hemleben et al., 1989; Boltovskoy et al., 1996). According toBoltovskoy et al. (1996), the former species can occur in negligibleproportions as far south as 371S–381S. The preferences ofG. menardii for warm sea surface temperatures, normal salinitiesand less stratified water masses (Hilbrecht, 1996) were demon-strated by the Spearman analysis, which show significant positivecorrelation with temperature (ρ¼0.6174) and salinity (ρ¼0.3656).Conversely, the maximum abundance of this species was foundwithin and below the thermocline, according to Bé et al. (1985),and was generally associated with the DCM in tropical andsubtropical water masses (Fairbanks et al., 1982). However, nosuch ecological inferences were distinguished in our study area,most likely due to the low level of resolution in our data.

O. universa has been reported in literature to inhabit the mixedlayer (Bé et al., 1985). This species is also found in the nutrient-richBenguela Current (Ufkes et al., 1998). In the study area, the highestabundance of this species was found in the mixed layer (e.g.,stations 7109, 7144), and its occurrence is apparently related to thenutrient-rich upwelling processes that were observed in the IlhaGrande and Cabo Frio transects (Fig. 3).

5.3. Sedimentary imprint of living planktonic assemblages

For the paleoceanographic purposes, we compared the distribu-tion of several species of planktonic foraminifera that can beconsidered proxies (e.g., G. ruber (white), G. ruber (pink), G. bulloidesand G. siphonifera), based on our data from the upper 100 m of thewater column in the study area and their geographic distribution insurface sediments, according to Passos (2006) and Sorano (2006)(Fig. 8). We use here the sum of G. bulloides and G. siphoniferabecause they have been considered to indicate nutrient-rich upwel-ling situations (Hemleben et al., 1989 among others, and this study).We recognize that this comparison can be hindered by variousartefacts (i.e., mesh size, seasonal an inter-annual variability, verticaldistribution, accumulation rate of planktonic foraminifera, amongother aspects), as mentioned by Boltovskoy et al. (1996) andAl-Sabouni et al. (2007). However, this comparison can confirmoceanographic processes already observed in the area, enabling abetter understanding of paleoceanographic interpretations.

In general, patterns in the water column and in the surfacesediments are very well coupled, with the exception of plankton–sediment mismatch of G. ruber (pink). This species reaches valuesof up to ca. 50% in surface waters of Sepetiba (station 7121) andnorth of Cabo Frio (station 7154) (Fig. 2). The regional distributionof the pink form in the underlying sediment indicates lowerabundance (up to ca. 10%). However, higher abundance in thesediment was observed offshore of Ilha Grande (between the 100and 200 m isobaths) and Sepetiba (ca. 200 m isobath). The highestvalues occur in the inner shelf offshore of Cabo Frio (Fig. 8), whichis characterised by coastal upwelling where, unfortunately, no towsample data are available. The decline of the pink form occursmainly in the southernmost study area (Fig. 8).

Boltovskoy et al. (1996) observed a slight difference in theoccurrence of G. ruber in the planktonic and sedimentary compart-ments of the south-western Atlantic (301S–601S). G. ruber isconsidered a very delicate species, with high susceptibility todissolution (Bé et al., 1985; Thiede et al., 1997; Conan et al.,2002). Additionally, studies carried out by Adelseck (1977) demon-strated that smaller specimens of G. ruber (with diameter less than250 μm) appear more resistant than the larger ones. In general,specimens of G. ruber (pink) are larger than the white form(Hemleben et al., 1989), which could explain their lower abun-dance in the sediments. According to Boltovskoy et al. (1996), theplankton sediment mismatch of this species is not necessarily dueto enhanced preservation, but also due to the random dispersionduring settling on the seafloor.

Conversely, the plankton–sediment mismatches of G. ruber(pink), observed along the 200 m isobath approximately, may berelated to the lowest sedimentation rate values found on the outershelf and upper slope in the study area. According to Mahiqueset al. (2011), the low sedimentation rates associated to a strongroughness sea bottom below the 140 m isobaths, indicate theeffectiveness of the BC moving over the outer shelf and upperslope between 231S and 271S, in reworking sediments (Silveiraet al., 2000). Thus, the planktonic foraminifera sedimentary recordon the outer shelf in the study area illustrate past environmentalconditions.

The living G. ruber white form, on the other hand, has peaks ofabundance offshore of Ilha Grande (stations 7109, 7110), Sepetiba(station 7120) and Cabo de São Tomé (station 7165) (Figs. 2 and 3).And its regional distribution in the underlying sediments has asimilar pattern, with frequencies of up to 70% offshore Sepetiba(ca. 200 m isobath) and north of Cabo Frio (Fig. 8). The peaksin abundance of living specimens of the species G. bulloides andG. siphonifera occur offshore of Ilha Grande (station 7110) and CaboFrio (station 7142). In the sediments, these species also reach theirmaximum values (ca. 40%) in the upwelling front areas (Fig. 7).

S.H.M. Sousa et al. / Continental Shelf Research 89 (2014) 76–87 85

The plankton–sediment mismatches of G. ruber (white), G. bulloidesand G. siphonifera are observed only on the outer shelf, where weobserve lower values of foraminifera species abundance in theplankton compared to the sedimentary record (Fig. 8). This dissim-ilarity between the plankton and the underlying thanatocoenosis isprobably related to the low sedimentation rates associated to theinteraction of the BC on the outer shelf (Mahiques et al., 2011).

6. Conclusions

The vertical distribution of planktonic foraminifera species(abundance, species composition and diversity) is largely con-trolled by temperature and phytoplankton biomass availability inthe water column, nevertheless salinity can also influence theecological descriptors. The occurrence of deeper DCM seems toenhance the abundance of G. ruber (white and pink forms), inconditions of higher salinity.

The ecological habitat of the two forms of G. ruber is affected bythe depth of the mixed layer, with a predominance of the whiteform in deeper layers.

The increase in species diversity is related to the dynamics ofthe BC, which cause the displacement of cold and high productiv-ity waters in the euphotic zone off the southeastern Brazilian coast(i.e., Ilha Grande and Cabo Frio regions). Conversely, the highestabundances of planktonic foraminifera are linked to a less strati-fied water column.

Our data demonstrate that the species G. bulloides, G. calida,G. falconensis and G. siphonifera can be used as proxies for relativelyeutrophic conditions in the southeastern Brazilian margin.

Our data confirm the use of diversity measurements andassemblages composition for reconstructing past water columnstructures in subtropical oceans.

Plankton tow sampling (0 to 100 m water depth) from thesoutheastern Brazilian continental margin contributed to a betterunderstanding of the ecological habitat of planktonic foraminiferain an oligotrophic region and improved the use of these organismsas proxies in paleoceanographic reconstructions.

Acknowledgments

The authors would like to thank Fundação de Amparo à Pesquisado Estado de São Paulo—FAPESP for financial support (Proc.no. 2002/06633-0) and CAPES for M.R. Sorano Master's grant.We also thank Marcelo Rodrigues for helping with the figures andthe DEPROAS project, funded by Conselho Nacional de Pesquisa—CNPq, for loaning the samples. We extend additional thanks toAndré Paloczy Filho, César Barbedo Rocha and Márcio KatsumiYamashita for their collaboration on the treatment of the hydro-graphic data. We would also like to thank the anonymousreviewers for their constructive comments. This paper is a con-tribution for the Project Geodinâmica de Bacias Sedimentares eimplicações para o potencial exploratório (petróleo, gás natural eágua subterrânea), GEOSEDex, Núcleo de Apoio à Pesquisa, USP.

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