Benthic community structure and organic matter variation in response to oceanographic events on the Brazilian SE inner shelf

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Benthic community structure and organic matter variation in response to oceanographic events on the Brazilian SE inner shelf Betina G. Rodrigues Alves n, Arthur Ziggiatti Güth, Márcia Caruso Bícego, Salvador Airton Gaeta, Paulo Yukio Gomes Sumida Universidade de São Paulo, Instituto Oceanográfico, Departamento de Oceanografia Biológica, Praça do Oceanográfico 191, Cidade Universitária, São Paulo 05508-120, Brazil

art ic l e i nf o

a b s t r a c t

Article history: Received 21 November 2013 Received in revised form 16 June 2014 Accepted 22 June 2014

The present work provided monthly monitoring of sedimentary organic matter composition, benthic bacteria and macrofauna during 13 months in a permanent station in the inner shelf (
40 m depth) off Ubatuba, SE Brazil. Sediment organic matter compounds evaluated in the present study included the total organic matter, lipid biomarkers and phytopigments. The organic matter presented a complex distribution, typical of inner shelves, intimately related to coastal dynamics that drive the buildup (high primary production) or removal (high energy events) of labile organic matter from the sediments. Lipid biomarker composition revealed that particulate organic matter was mainly derived from autochthonous sources, such as plankton, sediment bacteria and benthic metazoan fauna. The benthic dynamics off Ubatuba coast is highly influenced by the intrusion of the South Atlantic Central Water (SACW) onto the shelf, bringing nutrients up to the euphotic zone and stimulating new phytoplanktonic production. This enhances the flux of organic matter to the bottom increasing benthic biota density. The results obtained in the present study suggest a strong and complex benthic–pelagic coupling, influenced by mesoscale oceanographic events (i.e. intrusion of SACW), and by local events (cold fronts) influencing the benthic system through the remobilization of sediments. & 2014 Elsevier Ltd. All rights reserved.

Keywords: Inner continental shelf Temporal variation Organic matter Ubatuba

Contents 1. 2.

3.

4.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 2.1. Study area . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 2.2. Sampling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 2.3. Statistical approach . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 3.1. Environmental conditions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 3.2. Sediment parameters. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 3.2.1. Total organic matter (TOM) and phytopigments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 3.3. Lipid classes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 3.4. Benthic bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 3.5. Macrofauna . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 3.6. CCA analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 4.1. Physical environment and organic matter quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 4.2. Organic matter sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 4.3. Interactions between bacteria and macrofauna abundance and environmental factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8

n

Corresponding author. E-mail addresses: [email protected], [email protected] (B.G. Rodrigues Alves), [email protected] (A. Ziggiatti Güth), [email protected] (M. Caruso Bícego), [email protected] (S. Airton Gaeta), [email protected] (P.Y. Gomes Sumida). http://dx.doi.org/10.1016/j.csr.2014.06.008 0278-4343/& 2014 Elsevier Ltd. All rights reserved.

Please cite this article as: Rodrigues Alves, B.G., et al., Benthic community structure and organic matter variation in response to oceanographic events on the Brazilian SE inner shelf. Continental Shelf Research (2014), http://dx.doi.org/10.1016/j.csr.2014.06.008i

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Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

1. Introduction Coastal marine sediments have a great importance in carbon cycling, with organic carbon fluxes to the seabed representing ca. 0.1% of the total reserve of marine organic carbon (Harvey, 2006). These fluxes are directly related to local planktonic primary production, sedimentation rates, water column depth, source of organic matter and oxygen exposure time (Hedges and Keil, 1995). Almost a quarter of the organic matter produced in the water column reaches the seabed in continental shelf areas, with faster accumulation rates than on the deep ocean floor (Killops and Killops, 2005). A fraction of this autochthonous organic matter is composed of smaller molecules such as carbohydrates, proteins, nucleic acids and lipids and is rapidly degraded on the benthos (Danovaro et al., 1999). Other macromolecules, such as humic and fulvic acids and long-chain alcohols, represent the refractory fraction of the organic matter, being slowly degraded and preserved in sediments (Fabiano and Danovaro, 1994; Bouillon and Boschker, 2006). The quality of organic matter is measured through several analyses, such as phytopigment (chl-a and phaeopigments) ratios and lipid biomarkers (Dell'Anno et al., 2002), being the chlorophyll-a an important proxy for the amount of labile organic matter (Wieking and Kröncke, 2005). In addition, lipid biomarkers can provide valuable information on the origin, transport pathways, alteration and transformation processes of organic matter due to their stability in aquatic environments, structure diversity and relative source specificity (Wakeham et al., 1997; Volkman, 2006). Sediment bacteria are particularly affected by fluctuations in the amount of labile organic matter (Sun et al., 1994; Fabiano et al., 1995). Their role degrading organic material make them key players in the benthic food web (Boschker et al., 2001), both in remineralization and also increasing the quality of organic matter through protein enrichment (Fabiano et al., 2004). Environmental factors (e.g. organic enrichment, oxygen deficiency, hydrodynamics) have been shown to play an important role in these processes (Zajac et al., 1998). For instance, benthic microbiota responds positively to increases in planktonic detritus supply due to upwelling enrichment (Sumida et al., 2005). The relationship between detrital supply to sediments, influenced by physical stress and benthic community structure has been extensively demonstrated in inner shelf areas in high latitudes (e.g. Albertelli et al., 1999; Stoeck and Kröncke, 2001; Hernández-Arana et al., 2003; Wieking and Kröncke, 2005; Chapman and Tolhurst, 2007; Montserrat et al., 2008). However, little is known about the temporal variation of organic matter composition and its influence on the structure and functioning of benthic communities in tropical and subtropical areas (Quijón et al., 2008; Quintana et al., 2010). Some oceanographic features in the southeastern coast of Brazil are related to the intrusion of the nutrient-rich South Atlantic Central Water (SACW) from the slope onto the inner shelf during the summer, generating strong stratification of the water column (Castro-Filho et al., 1987). SACW advection introduces nutrients into the mixing layer increasing phytoplankton biomass (Valentin et al., 1987; Ciotti et al. 1995; Rocha et al., 1998; Saldanha-Corrêa and Gianesella, 2004; Villac et al., 2008). This is considered the major phenomenon influencing the coastal ecosystem productivity in the SE Brazil, including the increase in fish stocks (Pires-Vanin, 1993; Rocha et al., 2003) and mega- and macrobenthic communities (Pires-Vanin, 1992; Sumida

and Pires-Vanin, 1997; Muniz et al., 2000; De Léo and Pires-Vanin, 2006). During autumn and winter, the SACW retreats and the region is subjected to strong southwesterly winds, due to the intensification of cold fronts passages, causing water column mixing and sediment resuspension (Mahiques et al., 2004). Despite the effects of sediment resuspension on infaunal communities are not yet fully understood in the SE Brazilian coast (Quintana et al., 2010), it may also affect sediment biogeochemistry (Wainright and Hopkinson, 1997). Recent studies have demonstrated the relationship between water column parameters and the quality of sedimentary organic matter (Sumida et al., 2005; Quintana et al., 2010; Venturini et al., 2011). However, none of these have dealt with seasonality. In the present work we provide a monthly monitoring of sedimentary organic matter composition, benthic bacteria and macrofauna, in a permanent station in the inner shelf off Ubatuba, SE Brazil, and relate them with the main physical and biological forcings in the area. This work is part of a long-term monitoring program (ANTARES) with the aim of looking at ecosystem change in response to climate change.

2. Materials and methods 2.1. Study area The sampling area (23136.79S–44153.46W) is located on the continental shelf near Ubatuba (SE Brazil) at 42 m depth (Fig. 1). This region is under the influence of three water masses: Coastal Water (CW), characterized by high temperature ( 425 1C) and low salinity (32–33); Tropical Water (TW) with intermediate temperature (20–23 1C) and high salinity (ca. 36); and South Atlantic Central Water (SACW) with low temperature (16–18 1C) and high salinity (35–36) (Silveira et al., 2000). During the summer, the nutrient-rich SACW moves onshore and is often found in the central and outer portions of the continental shelf (20–100 m), while the CW is found along a narrow band inshore. This results in a vertical stratification over the inner shelf, with a strong thermocline at intermediate depths. In winter, when SACW is restricted to the outer shelf, horizontal and vertical thermal gradients are reduced and almost no stratification is observed on the inner shelf. The intrusion of the SACW in the continental shelf is related to meanders and eddies formed by the Brazil Current (BC, the interaction of TW and SACW) (Castro and Miranda, 1998). In terms of geomorphology, a mixture of grain sizes is observed, with significant deposits of mud in the inner shelf and a complex pattern of sedimentary patches (Mahiques et al., 2004). 2.2. Sampling Monthly cruises were done between October 2006 and October 2007. Total organic matter (TOM), phytopigments and bacterial density and biomass were not sampled in January 2007 and July 2007 due to rough weather conditions. Water column temperature and salinity profiles were done using a SeaBirdsCTD profiler (conductivity, temperature and depth). Water samples from surface and one meter above bottom were collected using van Dorn bottles and later analyzed for dissolved oxygen by Winkler titration (Strickland and Parsons, 1968).

Please cite this article as: Rodrigues Alves, B.G., et al., Benthic community structure and organic matter variation in response to oceanographic events on the Brazilian SE inner shelf. Continental Shelf Research (2014), http://dx.doi.org/10.1016/j.csr.2014.06.008i

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Fig. 1. Permanent station located in the southeastern Brazilian shelf.

Undisturbed sediment was collected using acrylic corers (9.4 cm inner diameter and 60 cm in length) mounted in a multicore. Three sediment replicates were used for the analysis of TOM, phytopigments and bacteria counting. One sediment replicate was collected for lipid analysis. Chlorophyll-a and phaeopigment were analyzed according to Lorenzen (1967), modified for sediment by Sünback (1983). In laboratory, chlorophyll-a concentrations were measured spectrophotometrically (absorbance read at 430 and 665 nm) after extraction with 100% acetone. Phaeopigments were determined after acidification with 0.1 N HCl (Plante-Cuny, 1978). Organic matter content was determined by calcination at 450 1C (Byers et al., 1978). Sediment was treated with 10% hydrochloric acid to remove carbonates that could interfere with organic-matter assessment (Buchanan and Kain, 1971). The results were expressed as percentage of total organic matter in each sample. Lipids biomarkers were extracted according to Yoshinaga et al. (2008), with minor modifications. The total lipid extract (TLE) was saponified using aqueous 0.5 N KOH and neutral (non-saponifiable) lipids were extracted from the basic solution at pH 413 using hexane. The solution was acidified by adding HCl to pH o 2 to give an acid fraction. Neutral lipids were fractionated into constituent classes: n-alcohols, sterols and alkenones. Acidic lipids were fractionated into: long chain fatty acids (LCFA), short chain fatty acids (SCFA), polyunsaturated fatty acids (PUFA), monounsaturated fatty acids (MUFA) and branched chain fatty acids (BRANCH). Lipids were analyzed on Agilente Technologies 6890 high-resolution gas chromatograph equipped with flame ionization detector (GC-FID). Data were acquired and processed with Agiolente Chemestation Software. Selected samples were analyzed using Agilent 6890 gas chromatograph coupled to a 5973 N mass spectrometer (GC–MS) operated in electron ionization mode (70 eV) to confirm compound identity and peak purity.

Three replicate sediment samples (ca. 1 cm3) were collected and fixed with 10 ml of 0.2 mm filtered seawater formaldehyde (2% vol/vol) solution to estimate bacterial density. Samples were sonicated four times (Thorton T14) at 100 W for 1 min. Subsamples were diluted 1000 times, stained for 5 min with acridine orange (Meyer-Reil, 1983) and filtered on black Nuclepore 0.2 mm pore size filters. Bacteria cells were counted with a 40-place grid counting chamber on a fluorescence microscope (Cassel, 1965). Bacterial biomass (μg C ml  1 sediment) was estimated measuring the length (L) and width (W) of the cell, calculating its volume [Vcell ¼ (π/4)W2(L W/3)], and converting it to the total biovolume (Vtotal ¼ cells ml  1 of sediment X average Vcell; Bratbak, 1985). Biomass was estimated using a conversion factor of 3  10  13 g C μm  3 biovolume (Børsheim et al., 1990). The benthic macrofauna was collected with a 0.05 m2 van Veen grab. Three samples were obtained for each period, in a total of 39 samples. They were washed in situ on a 0.5 mm sieve and the retained material was preserved in 70% alcohol for later sorting and identification under stereomicroscope. Benthic organisms were counted and identified to the lowest possible taxonomic level. Most taxa were identified to the species level. Biomass was determined as blotted wet weight after drying the specimens on absorbent paper for a few seconds (Witte, 2000). Individuals of Mollusca were weighed with shell. 2.3. Statistical approach One way Analysis of Variance (ANOVA) was carried out to test for temporal differences among months. A post-hoc Tukey test was used for pairwise comparisons when significant differences were found. The macrofauna data was transformed [(log(xþ 1)] to meet the assumptions of normality and homogeneity of variances (Zar, 1999). Canonical Correspondence Analysis (CCA; CANOCO 4.5 and Canodraw Q11 4.5; ter Braak and Smilauer, 2000) was performed to evaluate the

Please cite this article as: Rodrigues Alves, B.G., et al., Benthic community structure and organic matter variation in response to oceanographic events on the Brazilian SE inner shelf. Continental Shelf Research (2014), http://dx.doi.org/10.1016/j.csr.2014.06.008i

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influence of sediment parameters on variations on the macrobenthic community. Monte Carlo permutation test (999 permutations) was applied to compute significances of hypothetical relations.

3. Results 3.1. Environmental conditions Over the sampling months, there was substantial variation in direction and intensity of the wind. From mid November06 to March07 NE winds predominated, favoring the intrusion of SACW on the inner shelf. There were also periods marked by the passage of cold fronts (i.e. prevalence of S-SW winds) in from May to October 2007 (Fig. 2). Sea surface temperature ranged from 19.7 (August07) to 28.4 1C (March07) and bottom-water from 15.0 to 21.6 1C (Fig. 2). The lower bottom temperature values in September and October07 (austral spring) were related to the presence of the SACW forming a sharp thermocline in water column. In May–June07, bottom temperatures were higher and the water column more homogeneous. Surfacewater salinity varied from 30.9 to 35.6 and bottom-water from 35.3 to 35.6 (Fig. 2). Dissolved oxygen (DO) concentrations of surface water ranged from 3.20 ml L  1 in October07 to 5.07 ml L  1 in October06. Bottom-water DO was lower than in surface ranging from 2.11 in March07 to 4.59 in July07 (Fig. 2).

3.2. Sediment parameters 3.2.1. Total organic matter (TOM) and phytopigments Sediment TOM varied significantly monthly from 2.4%70.25 SD (Oct/07) to 6.5%70.95 SD (Oct/06) (F10,22 ¼3.87, p¼0.013) (Fig. 3A). Sediment chlorophyll-a concentrations ranged from 1.5 mg g  1 72.1 SD (Jun/07) to 7.8 mg g  1 72.1 SD (May/07), with a significant temporal variation (F10,22 ¼2.9437, p¼ 0.012). The post-hoc test of Tukey did not detect differences between the months. Phaeopigments were in the range of 18.2 mg g  1 71.6 SD (Sept/07)–40.9 mg g  1 711.4 SD (May/07) (Fig. 3B). Phaeopigment concentrations varied significantly (F10,22 ¼2.9784, p¼ 0.015), mainly in May/07, when values were higher than in Jun/07 (po0.01) and Aug/07 (po0.05) (Fig. 3B). The Chl-a/Phaeo ratios changed over time (F10,22 ¼ 2,97, p¼0,01) with values ranging from (0.170.005) in Oct/06 to (0.270.003) in Aug/ 07, otherwise remaining near 0.18 for the remainder sampling periods (po0.01) (Fig. 3B).

3.3. Lipid classes There was a predominance of saturated short-chain fatty acids (SCFA) (C14, C16, C18) with higher values in December06 and lower in September07, followed by monounsaturated fatty acids (MUFAs) and branched-chain fatty acids (BRANCHs) (Fig. 3C). Higher MUFA

Fig. 2. Temporal variation of wind field, the vectors are oriented in the west–east direction. The very small white balls indicate the sampling periods. Temporal variations of surface (A) and bottom (B) water temperature (1C), surface (C) and bottom (D) salinity and surface (E) and bottom (F) dissolved oxygen concentration in Ubatuba inner shelf, from October 2006 to October 2007.

Please cite this article as: Rodrigues Alves, B.G., et al., Benthic community structure and organic matter variation in response to oceanographic events on the Brazilian SE inner shelf. Continental Shelf Research (2014), http://dx.doi.org/10.1016/j.csr.2014.06.008i

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Fig. 3. Temporal changes in (A) total organic matter (TOM%) and (B) phytopigments (μg g  1) (chlorophyll-a and phaeopigments) in inner shelf sediments of Ubatuba (SE Brazil). (C) Temporal variability of lipid classes mean concentrations (mg g  1): PUFA: polyunsaturated fatty acids; MUFA: Monounsaturated fatty acids; BRANCH: branchedchain fatty acids; LCFA (C24–C32): Long-chain saturated fatty acids; SCFA (C14–C23): Short-chain saturated fatty acids; (D) LCOH (C24–C32): Long-chain alcohols; SCOH (C12–C22). (E) Temporal changes in the density (108 no cel. ml  1) and (F) biomass (μg ml  1) of benthic bacteria. There was no sampling in Jan/07 and Jul/07. Vertical bars are standard deviations.

concentrations, mainly C16:1ω7, C18:1ω7 and C18:1ω9, were recorded in October06 and minor values in April07. BRANCH (iso-C15, anteisoC15, 10-metil-C16) concentrations were similar almost during the entire period. LCFAs (C24–C30) and PUFAs (C20:4ω3, C20:5ω3) concentrations were lowest in all samples analyzed (Fig. 3C) (Table 1). Short-chain alcohols (SCOH) (C12—C22) were more abundant than long-chain alcohols (LCOH) (C24–C30) during most of the sampling period, except in November06 and August07. Phytol concentration was higher in August07, and lower in March07. Regarding the sterols,

there were two peaks of high abundance. The first was in November06, due to the 27Δ22 (cholestan-5,22-dien-3ß-ol) and 28Δ22 (24methylcholesta-5,22-dien-3ß-ol). The second was in August07, due to 28Δ0 (24-methyl-5α-cholest-24(28)-en-3ß-ol) and 28Δ5,24(28) (24methyl-5α-cholesta-22-en-3ß-ol) (Table 1). The composition was dominated by C27 sterols, mostly 27Δ5 (cholest-5-en-3ß-ol) and 27Δ5,22 (cholesta-5,22E-dien-3ß-ol) followed by C28 sterols. The same trend was found when comparing sterols and alcohols, the concentrations increasing from December06 to August07, decreasing in September07 and returning to increase in October07 (Fig. 3D)

Please cite this article as: Rodrigues Alves, B.G., et al., Benthic community structure and organic matter variation in response to oceanographic events on the Brazilian SE inner shelf. Continental Shelf Research (2014), http://dx.doi.org/10.1016/j.csr.2014.06.008i

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Table 1 Concentrations of most abundant lipids and major lipid classes (mg g  1) in inner shelf sediments of Ubatuba (SE Brazil). Oct06

Nov06

80.9 59.5 57.7 36.6 33.4 122.8 78.5 78.9 69.4 26.1 30.0 1.6 2.4

35.5 22.3 28.4 25.4 17.7 31.8 93.5 41.6 50.7 8.5 10.7 0.8 3.8

Alcohols ∑SCOH ∑LCOH Phytol ∑SCOH/∑LCOH MarOH/TerrOH

31.0 50.1 74.2 0.6 1.8

626.6 488.8 91.7 1.3 1.4

Sterols 26Δ5,22 27Δ5,22 27Δ5 28Δ5 29Δ5,22 29Δ5 30Δ22

5.8 1.6 8.0 14.1 3.8 10.5 1.2

93.9 79.7 35.1 11.7 50.7 17.2 13.9

Fatty acids C14 iC15 aC15 C15 10metilC16 16:1ω7 18:1ω9 18:1ω7 C18 20:5w3 20:4ω3 ∑16:1ω7/∑18:1ω7 ∑SCFA/∑LCFA

Dec06

Feb07

Mar07

Apr07

66.6 49.4 47.4 33.6 18.0 71.0 66.1 57.8 94.8 17.2 17.8 1.2 2.9

73.7 58.0 52.6 32.5 26.6 108.1 52.0 87.2 47.9 15.7 20.2 1.2 4.0

45.2 31.3 31.7 24.5 17.8 61.9 38.2 50.2 35.1 7.6 11.1 1.2 5.1

25.0 17.5 16.8 11.2 11.1 36.8 39.8 43.0 82.9 5.5 5.9 0.8 8.9

20.7 120.3 72.3 0.2 0.7

51.0 141.4 111.4 0.4 1.1

142.4 142.6 39.7 1.0 1.2

1.5 2.2 1.7 nd nd 2.4 nd

19.0 12.3 105.4 12.1 14.0 39.3 3.6

1.8 5.2 3.1 4.0 10.0 8.3 8.4

May07

Jun07

Aug07

Sep07

Oct07

70.3 42.9 47.8 28.0 35.8 22.1 50.7 57.4 43.1 nd nd 0.4 11.1

60.5 37.9 50.0 23.0 17.8 17.8 53.2 49.1 44.1 9.0 16.6 0.4 4.1

48.5 38.2 43.7 21.6 5.7 14.3 41.5 49.5 32.7 5.5 10.6 0.3 3.8

40.1 27.9 37.4 17.8 27.5 70.3 33.8 39.0 28.0 35.7 44.8 1.8 4.9

77.5 43.7 45.2 23.6 13.9 155.8 54.4 73.3 38.2 10.2 11.7 2.1 4.3

264.4 209.9 44.3 1.3 1.4

419.9 249.7 40.7 1.7 2.0

467.3 393.6 122.3 1.2 1.5

542.2 563.2 488.8 1.0 1.8

143.8 112.6 40.9 1.3 1.6

377.8 311.1 51.5 1.2 1.5

6.0 3.6 8.2 4.1 6.7 3.4 39.1

15.9 17.6 83.4 35.7 7.6 17.1 46.6

15.0 4.3 10.1 8.7 10.8 7.1 2.7

5.0 24.2 15.8 36.7 70.3 5.9 9.9

1.1 1.5 0.4 2.1 3.4 1.7 1.4

15.0 7.8 13.1 8.6 8.9 3.4 5.5

Fatty Acids: Monounsaturated (MUFAs): C14, C15, C18; BRANCH: iso and anteiso C15 (iC15 and aC15) and 10metilC16; Polyunsaturated (PUFAs): C16:1, C18:1, C20:5, C20:4; SCFA: Short-Chain Fatty Acidso C23; LCFA:Long-Chain fatty Acids4C24; SCOH: Short-Chain Alcohols ( o C22); LCOH: Long-Chain Alcohols ( 4C24); ∑MarOH: Sum of marine alcohols (C14–C22 plus phytol); ∑TerrOH: Sum of terrestrial alcohols (C24–C32); C26 sterols (26Δ5,22); C27 sterols (27Δ5, 27Δ5,22); C28 sterols (28Δ5); C29 sterols ( 29Δ5); C30 sterols (30Δ22)

(Table 1). The C37 and C38 alkenones occurred in all sampling period, except in July07, with higher values in November06, May07 and August07, the lowest in Mar07 (Table 1). The ratio ∑SCFA/∑LCFA was applied to find temporal variations in the contribution of marine (SCFA) vs. terrestrial sources (LCFA) for the saturated fatty acids (Table 1). Higher values were detected in May07 (11.1) and April07 (8.9), and the lowest values in October06 (2.43) (Table 1). The ratio C16:1ω7/C18:1ω7 was employed to check a possible dominance of different phytoplankton species contributing to the study area. Values ranged from 0.3 (August07) to 2.1 (October07). In six out of eleven sampling months C16: 1ω7/C18: 1ω7 values were greater than 1.0, suggesting dominance of phytoplankton contribution for the study region. The temporal variability of marine and terrestrial derived alcohols was calculated via the ratio MarOH/TerrOH (∑MarOH: SCOH plus Phytol; ∑TerrOH: ∑LCOH). The lowest value was found in December06 (0.7), whereas the highest in May07 (2.0). This results were similar to those found for fatty acids (short-chain prevalence, Table 1), reflecting the predominance of marine-derived alcohols during all sampling period.

3.4. Benthic bacteria Bacterial density in the sediments of Ubatuba displayed higher values in Sep/07 (288.0  108 cel. ml  1 780.8) and Aug/07 (275.0  108 cel. ml  1 7170.8), and lower values in Oct/06 (12.5  108 cel. ml  1 784.4) and Mar/07 (12.3  108 cel. ml  1 770.6) (Fig. 3E). The differences were significant between sampling periods (F10,22 ¼3.2, p¼0.021), mainly in Sep/07, when values were higher than in Jun/07 and Aug/07 (po0.05). Bacterial biomass was highest in Oct/07 (1.8 mg ml  1 70.1) and lowest in Oct/06 (0.2 mg ml  1 70.06), with significant differences between sampling periods (F10,22 ¼3.8,

p¼0.004). Values found in Oct/06 were significantly lower than in Sep/07 and Oct/07 (po0.01) (Fig. 3F). 3.5. Macrofauna A total of 3850 individuals belonging to 226 species was recorded. Macrofaunal density was higher mainly in Oct/07 (217 ind. 0.05 m  2 7125.8 SD). The lowest density was found in Nov/06 (13 ind. 0.05 m  2 74.4 SD). There were significant differences among the sampling periods (F11,26 ¼8.34, p¼0.0001). Polychaeta was the most abundant group and its density varied significantly in time (F12,26 ¼3.2598, p¼0.0059), with the lowest density in Dec/06 (po0.05) (Fig. 4A). Among polychaetes, Ninoe brasiliensis and Goniada maculata were dominant, with higher density in May/07 and Sep/07 (Fig. 5A). The second group in density was Crustacea, with a significant temporal variability (F12,26 ¼5.3858, p¼0.0003). Higher values in Feb/07, May/07 and Oct/07 were mainly owing to high densities of Photis brevipes, Cyclaspis variabilis and Dyastilis fabrizioi (Fig. 5B). Among relatively less abundant taxa, Mollusca showed a significant temporal variation (F12,26 ¼2.93, p¼ 0.01), with greatest densities in May/07 and Sep/07, while no significant temporal change was detected in the densities of Echinodermata (F12,26 ¼ 1.31, p¼0.12) (Fig. 4A). Macrofaunal biomass was highest in Jul/07 (2.371.9 g m  2) and lowest in Nov/06 (0.170.06 g m  2) (Fig. 4). However, no significant temporal variations were found (F11,26 ¼1.90, p¼0.08) (Fig. 4B). 3.6. CCA analysis Macrofaunal densities presented significant positive relationship with environmental variables such as TOM, phaeopigments, alcohols and fatty acids, as well bacterial biomass (Fig. 6).

Please cite this article as: Rodrigues Alves, B.G., et al., Benthic community structure and organic matter variation in response to oceanographic events on the Brazilian SE inner shelf. Continental Shelf Research (2014), http://dx.doi.org/10.1016/j.csr.2014.06.008i

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Fig. 4. A. Temporal changes in the density (Ind. 0.05 m  2) of most common macrofaunal groups in inner shelf sediments of Ubatuba (SE Brazil). and (B) macrofaunal biomass (g m  2). Vertical bars are standard deviations.

High content of TOM and phaeopigments were related to the bivalve Adrana patagonica and the carnivorous polychaetes Pholoe sp. and Sthenelais limicola. The densities of crustaceans, especially gammaridean amphipods and cumaceans were related to the sedimentary fatty acid content. Deposit feeders such as cumaceans and Photis brevipes seem to be related to high fatty acid content whereas filter feeding species such as Ampelisca spp. and omnivore/predatory species such as Heterophoxus videns, Goniada sp. and Ninoe brasiliensis were related to low sedimentary fatty acid content (Fig. 6).

4. Discussion 4.1. Physical environment and organic matter quality Particulate organic matter dynamics on the southeastern Brazilian continental shelf can be understood in terms of the water mass model proposed by Castro-Filho et al. (1987). According to this model, based on wind dynamics, the intrusion of the SACW promotes the displacement of the CW. The presence of the nutrient-rich SACW on the euphotic zone enhances primary production (Aidar et al., 1993; Gaeta et al., 1999), with a consequent increase in phytodetritus input to the seabed (Matsuura and Wada, 1994). Otherwise, the presence of S-SW winds causes the mixing producing a homogeneous water column. The intensity of these cold fronts also promotes the removal of particulate organic material from the sediment surface. Chlorophyll-a concentrations suggest deposition of labile organic matter is seasonal in Ubatuba, with peaks during summer months. Concentrations of chl-a found in the present study were

Fig. 5. Mean density of the most abundant macrofaunal species of (A) Crustacea and (B) Polychaeta sampled in inner shelf sediments of Ubatuba (SE Brazil). Vertical bars are standard deviations.

in the range of those reported in previous studies in Ubatuba inner shelf, but lower than in the upwelling region of Cabo Frio, where SACW is advected all the way to the surface (Sumida et al., 2005). The higher phaeopigment content compared to chl-a content, suggests an effective coupling between the pelagic and benthic processes (bacteria and fauna consumption) (Stephens et al., 1997). The low chl-a/phaeopigments ratios during almost all sampling period suggest a high degradation rate of labile organic matter (chl-a), generating fresh food to benthic community (Gooday and Turley, 1990; Dell'Anno et al., 2002). This indicates that the quality of organic matter influences overall benthic dynamics in the studied site. The similarity between temporal variation of phaeopigments, lipids and benthic assemblages highlight the dynamics. Similar results are documented in shallower areas from Ubatuba (Quintana et al., 2010) and in the existing literature (Danovaro et al., 1999; Soltwedel, 1997; Q13Q14 Wieking and Kröncke, 2005). 4.2. Organic matter sources Typical organisms from meso-oligotrophic tropical and subtropical waters (Susini-Ribeiro, 1999) such as phytoflagellates, diatoms and dinoflagellates dominate the planktonic community in the inner shelf of Ubatuba (Aidar et al., 1993). The high content of phytoplanktonic markers (MUFAs and PUFAs) in the sediment reveals the importance of pelagic sources to the local benthic community (Quintana et al., 2010). Such phyto and zooplanktonic materials reach the bottom partially degraded and are readily available for the benthic community.

Please cite this article as: Rodrigues Alves, B.G., et al., Benthic community structure and organic matter variation in response to oceanographic events on the Brazilian SE inner shelf. Continental Shelf Research (2014), http://dx.doi.org/10.1016/j.csr.2014.06.008i

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Fig. 6. Canonical correspondence analysis (CCA) of species on the inner shelf of Ubatuba. Only significantly correlated (p 40.05) environmental variables vectors are shown.

High concentrations of sterols and SCOH were present in Nov/ 06 and Aug/07, probably derived from mainly diatoms blooms e.g. Coscinodiscus concinnus; Aidar et al., 1993), and also from dinoflagellates (e.g. Ceratium sp.; Aidar et al., 1993) and coccolithophorids (e.g. Emiliana sp. and Ophiaster sp.; Metzler et al., 1997). These organisms are major contributors to phytoplankton production and biomass when SACW is present in inner shelf subsurface waters. High concentrations of cholesterol (27Δ5) in the same periods indicate zooplankton grazing since fecal pellets of salps, in particular (e.g. Thalia democratica; Katsuragawa et al., 1993), are the major contributor of 27Δ5 to inner shelf sediments of the Ubatuba region (Matsuura and Wada, 1994). Previous lipid biomarker studies in SE Brazilian coast (SEBC) also detected such events by the presence of SACW, confirming the physical influence on SEBC waters (Yoshinaga et al., 2008). In Aug/07, high concentrations of SCOH derived from phytoplanktonic sources (Sargent, 1976; Volkman, 1986) also suggest that physical disturbance, such as sediment resuspension, caused by the passage of cold fronts, more often in winter (Gaeta et al., 1995; Mahiques et al., 1998; 2004), can stimulate primary production and provide fresh organic matter for the benthic system. BRANCH lipids derived from bacterial sources (Kaneda, 1991) that were present in sediments indicate an intense bacterial reworking with a consequent increase in biomass during spring months. Sumida et al. (2005) found similar results in the Cabo Frio upwelling system (SE Brazilian coast). Seasonal patterns were unclear and the major contribution to sedimentary organic matter was marine-derived, but non-specific and with an intermediate degree of degradation (SCFA, SCOH, phytol and others). Terrestrial markers (LCFAs and LCOHs) contributions were modest, suggesting only little continental input to the study area (see Mahiques et al., 2004).

4.3. Interactions between bacteria and macrofauna abundance and environmental factors The present study did not find a clear relationship between bacteria density and the amount of labile organic matter, despite the findings of other authors (Graf, 1989; Albertelli et al., 1999; Tselepides et al., 2000; Polymenakou et al., 2007). However, the density of bacteria in marine sediments is also influenced by several factors, including grain size, physical disturbance (e.g. turbulence/ resuspension), the availability of organic substrates and the predatory pressure due to their natural grazers (Danovaro, 1996; Danovaro et al., 1998; 2001). The continuous increase in bacteria density and biomass might also be related to refractory organic matter (Dauwe and Middelburg, 1998; Kröncke et al., 2004). A similar study on the coastal area of Ubatuba (10 m depth) found a relationship between bacteria biomass and labile OM input, Q3 mediated by different physical disturbances (Moraes et al., in preparation). The macrofauna density was comparable to other studies on the coast of Ubatuba (Santos and Pires-Vanin, 2004; Muniz et al., 2000; Quintana et al., 2010), with high densities occurring in parallel with the presence of labile organic matter (i.e. chl-a and labile lipid biomarkers). This suggests that the quality of organic matter available as food in sediments is of paramount importance for the macrobenthic communities (see Josefson et al., 2002). The macrofauna biomass was low in comparison with studies in the Northwest Atlantic (Wieking and Kröncke, 2005), estuarine areas from Mediterranean (Hermand et al., 2008) and in the rich Chilean coast (Gallardo et al., 1995; Galéron et al., 2000), which is related to the lower productivity found in the tropical Ubatuba coast. Changes in macrofauna biomass did not to follow the high food availability in Ubatuba (Aidar et al., 1993), as in high latitudes, like

Please cite this article as: Rodrigues Alves, B.G., et al., Benthic community structure and organic matter variation in response to oceanographic events on the Brazilian SE inner shelf. Continental Shelf Research (2014), http://dx.doi.org/10.1016/j.csr.2014.06.008i

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the North Atlantic (Heip et al., 2001) and Northwest Pacific (Quijón et al., 2008). High hydrodynamic conditions in the region (Mahiques et al., 1998; Galluci and Netto, 2004) can reduce food availability for macrofauna and constrain the organisms to smaller sizes due constant removal of the upper sediment layer and its inhabitants. Studies on macrofauna conducted by HernándezArana et al. (2003) in southern Gulf of Mexico show low densities and biomass related to high hydrodynamic energy (see also Flach et al., 2002 for the NE Atlantic coast). Indeed physical forcing (e.g. cold front passages, wind stress, sediment resuspension) is known to limit benthic secondary production and regulate benthic processes through disturbance of shallow shelf benthos (Emerson, 1989). Carnivorous polychaetes are not significantly dependent on any environmental variables (Paiva, 1993) and they showed no relation to the environmental variables measured in the present study. The numerical dominance of carnivorous polychaetes especially Ninoe brasiliensis and Goniada maculata, were relatively high and suggest a healthy ecosystem, given their higher position in the benthic food chain (Quintana et al., 2010; Muniz and Pires, 1999). The positive correlation of Pholöe sp., Sthenelais limicola with TOM and phaeopigments in multivariate analysis suggest that bacteria consumers and deposit-feeders are potential prey for carnivores (Dauwe et al., 1998). The high densities of the amphipod Photis brevipes, considered a suspensivore (Dauby et al., 2001), the cumaceans Cyclaspis variabilis and Dyastillis fabrizioi, both deposit-feeders (Woodin, 1978), appear to be related to periods of high organic matter quality. The presence of other groups, such as Ophiuroidea and Bivalvia in high densities suggests a relatively high stability of the local benthic community (Muniz and Pires, 1999). Sedimentary organic matter composition in terms of total organic matter, lipid biomarkers and phytopigments showed a complex distribuition, typical from inner shelves. This is related to ocean dynamics, which governs the main events of buildup or removal of labile organic matter in Ubatuba region. Lipid biomarker composition revealed that particulat organic matter was mainly derived from autochthonous sources, such as plankton, sediment bacteria activity and benthic fauna. The benthic dynamics on Ubatuba coastal waters is highly influenced by the intrusion of the SACW onto the shelf, which upwells nutrients to the euphotic zone stimulating new phytoplanktonic production. This enhances the flux of organic matter to the bottom increasing benthic biota density and biomass. The arrival of cold fronts promoting water column mixing and sediment resuspension is also fundamental in decreasing benthic community parameters (i.e. abundance and biomass). The results obtained in the present study suggest a complex benthic-pelagic coupling, influenced by mesoscale events (i.e. hundreds of kilometers; intrusion of SACW) on the one hand and, on the other, by cold fronts events influencing the benthic system on a local scale, through the remobilization of sediments.

Acknowledgments The authors acknowledge CNPq (National Counsel of Technological and Scientific Development) for providing a M.Sc. scholarship to B.G.R.A. The authors thank Dr. Marcos Rosa for help with figures and text, the master and crew of the B/P Véliger II and several colleagues of the Benthic Dynamics Laboratory and Primary Production Laboratory for help in the field and laboratory. References Aidar, E., Gaeta, S.A., Gianesella-Galvão, S.M.F., Kutner, M.B.B., Teixeira, C., 1993. Ecossistema costeiro tropical: nutrientes dissolvidos, fitoplâncton e clorofila-a,

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Please cite this article as: Rodrigues Alves, B.G., et al., Benthic community structure and organic matter variation in response to oceanographic events on the Brazilian SE inner shelf. Continental Shelf Research (2014), http://dx.doi.org/10.1016/j.csr.2014.06.008i