Effects of contrasting upwelling–downwelling on benthic foraminiferal distribution in the Ría de Vigo (NW Spain)

Journal of Marine Systems 60 (2006) 1 – 18 www.elsevier.com/locate/jmarsys

Effects of contrasting upwelling–downwelling on benthic foraminiferal distribution in the Rı´a de Vigo (NW Spain) Paula Diz a,*, Guillermo France´s a, Gabriel Roso´n b a

Departamento de Xeociencias Marin˜as e Ordenacio´n do Territorio, Universidad de Vigo, Facultad de Ciencias del Mar, Vigo 36200, Spain b Departamento de Fı´sica Aplicada, Universidad de Vigo, Facultad de Ciencias del Mar, Vigo 36200, Spain Received 13 July 2005; received in revised form 4 November 2005; accepted 6 November 2005 Available online 5 January 2006

Abstract Live benthic foraminifera in the superficial sediments from the muddy central axis of the Rı´a de Vigo were examined under two contrasting hydrographic conditions: downwelling and upwelling. During downwelling conditions the abundance of benthic foraminifera does not show large differences between sites with different organic carbon contents. The arrival of labile organic carbon to the seafloor delivered during upwelling events causes an increase in the abundance of the most significant species and the appearance of new species in the life assemblage. This suggests that benthic foraminiferal faunas strongly depend on high quality organic carbon supply and the sedimentary organic carbon is not a good indicator of food availability to benthic foraminifera. The response of benthic foraminifera to phytoplankton blooms differs between outer and inner sites. In outer and middle areas benthic foraminiferal assemblages show quick population growth in reaction to phytoplankton blooms (r-strategists), whereas in inner sites the most abundant species displays both growth and reproduction (k-strategists). It is suggested that r-strategy results of adaptation to perturbations on short time-scales (downwelling/upwelling cycles) under favourable microenvironmental conditions, while the k-strategy represents the adaptation to long term perturbations, such as relatively low oxygen concentrations and/or reducing microenvironmental conditions in the sediment. D 2005 Elsevier B.V. All rights reserved. Keywords: Live Benthic foraminifera; Ecology; Organic carbon; Rı´a de Vigo; Spain; Upwelling–downwelling cycles

1. Introduction The organic benthic known.

relationship between the flux of particulate carbon to the sea floor and the distribution of foraminifera in deep sea sediments is well The abundance and spatial distribution of

* Corresponding author. Present address: School of Earth, Ocean and Planetary Sciences, Cardiff University, Main Building, Park Place, Cardiff CF10 3YE, U.K. Tel.: +44 2920874573; fax: +44 2920874326. E-mail addresses: [email protected] (P. Diz), [email protected] (G. France´s), [email protected] (G. Roso´n). 0924-7963/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.jmarsys.2005.11.001

deep-sea benthic foraminifera respond to primary production and organic carbon flux patterns in the Atlantic and Pacific Oceans (Loubere and Fariduddin, 1999a; Herguera, 2000), the Arctic Ocean (Wollenburg and Kuhnt, 2000), the China Sea (Kuhnt et al., 1999) and the Mediterranean Sea (De Stigter et al., 1998; De Rijk et al., 2000). Foraminiferal biomass is also closely related to food availability below 1000 m (Altenbach and Struck, 2001). Above that depth and, in particular, in shallow water environments (b300 m) there does not seem to be a clear relationship between flux rates of organic carbon and the biomass of benthic foraminifera (Altenbach and Struck, 2001). Seasonal variability and

2

P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18

lateral advection in the organic flux to the sea floor, other organic carbon sources (sewage, bacteria, algal mats and algal coatings on sediments grains), and the development of anoxia, determine the relationship between either organic carbon with biomass, abundance or benthic foraminiferal assemblages composition in shallow water environments, which are difficult to assess (see review in Loubere and Fariduddin, 1999b). Apart from the quantity of food, another factor that controls the composition of communities and the vertical distribution of benthic foraminifera is the quality of food particles (van der Zwaan et al., 1999; Fontanier et al., 2002, 2003; Licari et al., 2003). This parameter is very important in the deep sea environment which can be disturbed episodically or seasonally by pulses of labile organic matter (phytodetritus) derived from the euphotic zone (see reviews by Gooday, 2002 and Beaulieu, 2002). The role of deep-sea benthic foraminifera in the rapid processing of fresh organic carbon sinking in the deep sea floor has been demonstrated by in situ tracer experiments (Linke et al., 1995; Moodley et al., 2002; Witte et al., 2003; Kitazato et al., 2003; Nomaki et al., 2005), microcosm experiments (Altenbach, 1992; Gross, 2000; Heinz et al., 2001, 2002; Ernst and van der Zwaan, 2004) and field studies (Gooday, 1988, 1993, 1996; Ohga and Kitazato, 1997; Kitazato et al., 2000; Ohkushi and Natori, 2001; Gooday and Hudges, 2002, Fontanier et al., 2002, 2003; Suhr et al., 2003). In shallow coastal environments the pulses of organic matter sometimes yield the majority of the annual organic carbon input to the benthos, however, little is known about the expression of these pulses on the seafloor. The few laboratory experiments carried out in shallow marine environments showed contradictory results in assessing the role of labile organic carbon availability on benthic foraminifera. Widbom and Frithsen (1995) demonstrated that foraminifera showed a remarkable low preference for fresh detritus. On the contrary, Moodley et al. (2000) examined the ability of benthic foraminifera in taking up freshly deposited 13Clabelled algal carbon in intertidal estuarine sediments and showed that labile carbon is rapidly taken up by the dominant species. Field studies have shown that some shallow benthic foraminiferal species respond to a certain extent to phytoplankton blooms in eutrophic environments (Alve and Murray, 1994; Murray and Alve, 2000; Gustafsson and Nordberg, 1999, 2000, 2001). Shallow marine environments affected by seasonal upwelling are a unique habitat with which to explore the influence of pulsed labile organic carbon inputs to the seafloor on benthic foraminiferal species and assemblages. A further advantage of these systems compared

to open ocean settings is that the time involved between the development of surface water chlorophyll maxima and the arrival of the organic aggregates to the bottom is short. Consequently, the decay of organic carbon through the water column is less important and therefore the response of benthic foraminifera to phytoplankton blooms may not be delayed. In the present study we document the record of live benthic foraminifera along the muddy central axis of the Rı´a de Vigo (NW Spain), a shallow marine environment affected by seasonal upwelling/downwelling cycles. Superficial sediment sampling under two contrasting hydrographical conditions, downwelling (January 1998) and upwelling (September 1998) enabled us to compare the standing crop and assemblage composition of benthic foraminifera feeding on refractory organic carbon (downwelling season) from those affected by sinking labile organic carbon (upwelling season). We demonstrate: 1) how benthic foraminifera from organic-rich eutrophic environments can be limited by the quality of the food and 2) that the response of benthic foraminiferal assemblages to labile organic carbon flux depends on the reproductive strategy of the species that constitute the assemblages, which should be the result of particular microenvironmental conditions in the sediment. 2. Study area The Rı´a de Vigo (428 N, Fig. 1) is situated at the boundary between the subpolar and temperate regimes of the Eastern North Atlantic coastal upwelling system. At this location, upwelling-favourable northerly winds predominate from March–April to September–October in response to the southward migration of the Azores High (Varela et al., 2005). During the rest of the year, downwelling favourable southerly winds prevail (Bakun and Nelson, 1991). The coupling between remote shelf winds and the residual (subtidal) circulation of the Rı´a de Vigo has been successfully verified by complementary approaches, such as kinematic inverse models (Gilcoto et al., 2001), hydrodynamic numerical models (Souto et al., 2003) and direct current measurements (Piedracoba et al., 2005). These studies concluded that shelf winds are mainly responsible for the changes observed in the hydrography of the Rı´a de Vigo. These changes are compatible with the two-layered residual circulation pattern, characteristic of partially mixed estuaries. The positive residual circulation is enlarged (inflow through the bottom layer and outflow through surface layer) under the influence of northerly shelf winds. Abrupt changes of bathymetry

P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18

3

Fig. 1. Location of the Rı´a de Vigo, sampling sites (circles) and approximate situation of the hydrographic sampling stations (triangles).

may still enhance the upward advection of waters in inner zones. Conversely, when winds change to southerly, the circulation pattern reverses (inflow through the surface layer and outflow through the bottom layer). These changes may be preceded by relaxation periods, characterised by slow winds. During the upwelling-favourable season, recurrent upwelling pulses (14 F 4 days) cause the high-nutrient Eastern North Atlantic Central Water (ENACW) to enter into the rı´a. The vertical advection injects new nutrients into the base of the pycnocline or even may erode it. Under these extreme cases ENACW reaches the photic layer causing an enhancement of the primary productivity, which is mainly generated by blooms of diatoms (Nogueira and Figueiras, 2005). In this sense, the Rı´a de Vigo acts as a nutrient trap as well as a sink of atmospheric CO2. This situation yields high fluxes of deposition of organic carbon to the sediment (0.54 g C m 2 d 1), which can be as high as 68% of the Net Community Production (0.79 g C m 2 d 1, AlvarezSalgado et al., 2001) at the time-scale of an upwelling event. This number is much higher than the world

average deposition over the bottom (32% of the world total production) proposed by Wollast (1991, 1993). However, it is in good agreement with the value proposed by Waldron et al. (1998) for the Benguela upwelling system, where 66% of new production was incorporated in continental shelf sediments. Additionally, residence times (b 1 week) associated with frequent upwelling pulses of well-oxygenated ENACW are high enough to allow the phytoplankton adaptation to the light and nutrient conditions, but low enough to preclude anoxia in the bottom layer (where net mineralization occurs). Due to the absence of studies concerning sedimentation rates during the downwelling period in the Rı´a de Vigo, we have extrapolated the results obtained in the adjacent Rı´a de Arousa, since both systems behave similarly from a physical and biogeochemical point of view. Under downwelling conditions, a strong reversal in estuarine circulation takes place, with the upwelled water being rapidly evacuated through the bottom of the rı´a. Reverse circulation enhances sediment mobilization, yielding high fluxes from the sediments to the

4 P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18 Fig. 2. Illustration of the hydrographic conditions during the sampling periods. (a, e) Upwelling Index pre winter and summer sampling programme respectively (data from Lavin et al., 2000). Distribution of temperature (b,f), salinity (c,g) and chlorophyll a (d,h) along the main axis of the Rı´a de Vigo during both samplings and oxygen (i) for the summer sampling period. For location of the hydrographic stations see Fig. 1. Data shown in (b), (c), (d), (f), (g), (h), (i) were provided by CCCMM (Centro de Control da Calidade do Medio Marin˜o, Consellerı´a de Pesca, Marisqueo e Acuicultura da Xunta de Galicia).

P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18

water column (0.53 g C m 2 d 1). This process partially contributes to the high regeneration of carbon and nutrients in the water column, also favoured by the oxidation of suspended particulate organic carbon (POC). Therefore, the rate of organic carbon mineralization is high (0.66 g C m 2 d 1, Roso´n et al., 1999). Residence times associated with downwelling pulses are also short (b 1 week) and sinking of high oxygen surface waters to the bottom also prevents anoxia in bottom waters. 3. Material and methods 3.1. Hydrographic conditions during the sampling periods Sediment samples used in this study were collected from the Rı´a de Vigo (Fig. 1) during two cruises, in January 1998 (26–30) and in September 1998 (21–26). Fig. 2 represents the hydrographic conditions along the main axis of the rı´a during both sampling cruises. It includes upwelling index data and distributions of temperature, salinity and chlorophyll-a in the water column for representative days of the January (26/01/98) and September (22/09/98) sampling periods. Oxygen concentration is also provided for the summer cruise. The upwelling index quantifies the intensity of the upwelling or downwelling (currently expressed as the volume transport perpendicular to one linear kilometre of coast) and denotes the hydrographic conditions. This consists of an estimation of the daily Ekman transport off the rı´a (if positive, upwelling) or towards the rı´a (negative, downwelling, see Piedracoba et al., 2005 for details). Values nearly zero (typically 500 to 500 m3 s 1 km 1) during several consecutive days are indicative of a period of relaxation of the upwelling. With the aim of establishing the most likely hydrographic conditions during the reproduction and growth of benthic foraminifera, the upwelling index was extended from 8 weeks before each sampling period (Fig. 2a, e). Despite the hydrodynamic conditions during December 97–January 98 (Fig. 2a) being dominated by strong downwelling (average 1007 F 1433 m3 s 1 km 1) the sampling took place during a 5 days period of wind relaxation (average 331 F 226 m3 s 1 km 1). On January 26th, the hydrographic situation in the rı´a was typical of winter: relatively low surface temperatures (b 14 8C) and salinities (b32x) mainly associated with the intense river plume in the surface waters (Fig. 2b,c), thermal inversion in the water column and a high vertical salinity gradient (both intensified in the inner rı´a). Chlorophyll-a concentration, which roughly

5

reflects the productivity of the rı´a, is relatively low, although a maximum in the photic layer of the outer rı´a is recorded (Fig. 2d). The situation during the 8 weeks before summer sampling showed clear upwelling (average 377 F 784 m3 s 1 km 1), only interrupted by a weak downwelling event in early September (Fig. 2e). The upwelling index during the 5 previous days prior to sampling showed a situation of upwelling relaxation (average 179 F 114 m3 s 1 km 1), also corroborated by the high surface temperatures (N 18 8C) and the establishment of a strong thermal stratification (Fig. 2f) mainly due to high sun irradiation. The absence of a sloping thermocline is associated with upwelling relaxation conditions. As a consequence of the low river discharge, the vertical salinity gradient is weaker than in January (Fig. 2g). The moderate upwelling situation is related to slow horizontal advection of outer nutrients to the bottom layer of the rı´a, followed by relatively slow water renewal. The development of primary production at the base of the thermocline is favoured, yielding high values of Chlorophyll-a (Fig. 2h). Oxygen concentrations in the water column are always higher than N 4.0 ml/l indicating full oxygenated conditions (Fig. 2i). 3.2. Sampling sites and methods Fourteen stations located along the muddy central axis of the Rı´a de Vigo were selected for this study (Fig. 1 and Supplementary Table 1). In both sampling periods, samples were recovered with a box corer. Each box core was sliced into 1 cm horizontal sections (every 1 cm for the first 5 cm). In order to evaluate the immediate response of benthic foraminifera to downwelling/ upwelling cycles only benthic foraminifera living in the upper 1 cm layer were considered for this study. A small proportion of sediment recovered during the September cruise was reserved for carbon and nitrogen measurements. Samples destined for foraminiferal analysis were subsampled using a stainless steel box 10  5  1 cm high. The selected volume (50 cm3) is suitable for live benthic foraminifera studies, since it is considered that areas greater than 30 cm2 are representative of the biocenosis (Murray, 1991). On the ship, and immediately after collection, subsamples were immersed into a mixture of methanol and Rose Bengal stain in order to discriminate between live (red-stained protoplasm) and dead individuals. All samples were shaken for several minutes in order to obtain a homogeneous mixture. Although dead individuals may retain undecayed protoplasm for weeks (Bernhard, 1988), the use of non vital Rose Bengal stain method is the most

6

P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18

commonly used technique to differentiate foraminifera living at the time of the collection and gives as reliable results as other methods (Murray and Bowser, 2000). Once onshore, all samples were kept at 4 8C until further treatment. 3.3. Benthic foraminifera counting and size distribution Samples destined for foraminiferal analyses were wet sieved into three different size classes: 63–125, 125–250 and N 250 Am, and then dried. Fractionating the sample makes the handling more practicable and helps quantifying the size distribution of the benthic foraminifera. In order to avoid extrapolating the abundance of benthic foraminifera, sediment samples were not split, and all well stained (bright red/rose) foraminifera from each size interval were picked, identified, counted and mounted in micropaleontological slides which are stored at the Departamento de Xeociencias Marinas, Universidad de Vigo. The generic assignments follow those of Loeblich and Tappan (1987) and most of species designations given in this work were published by Diz et al. (2004). Density of live benthic foraminifera is given as the number of live individuals (N 63 Am) of the whole community or a particular species per 50 cm3. Description of the spatial distribution of live benthic foraminifera is dependent on whether the foraminiferal results are expressed as standing stock or relative abundance for each species. On the one hand, the standing stock of each species is a useful parameter to determine the possible factors controlling the spatial or temporal distribution of a particular species, independently of the contribution of other species to the total assemblage. On the other hand, the relative abundance is the only parameter that can be used to compare the results of this study with ones from other areas and the interpretation of the fossil record. It depends on the total absolute abundance of life assemblage and it does not necessarily represent the temporal or spatial limits of species distribution in relation to environmental variables (Altenbach et al., 2003). Both parameters are taken into account and discussed. 3.4. Carbon and nitrogen analysis Based on the hypothesis that differences in the organic carbon content between the two sampling periods are not significant for the aims of this work, the carbon and nitrogen content of the sediment was characterised from samples collected in the September sampling cruise. The sediment portion destined for inorganic

Carbon (Cinorg), organic Carbon (Corg) and Nitrogen (N) analysis was dried at 50 8C and ground. The content of total carbon (C) and Nitrogen was carried out on a LECO CN-2000 Analyser and Cinorg on a LECO CC-100 Analyser. Measurements are given in percent per dry weight of sample and were replicated at least twice to calculate their standard deviation. The Corg was calculated by subtracting the C values from Cinorg values. The Corg : N ratio (C / N) was also calculated, on the assumption that the inorganic nitrogen sources are negligible in sediments of high organic carbon content (Meyers, 1997). Dry weight C : N ratios were compared to molar C : N ratios from previously published POC data from the water column (Rı´os and Fraga, 1987; Doval et al., 1997; Torres-Lo´pez et al., 2005) in order to roughly estimate the degradation state of the sedimentary organic carbon. For this purpose, dry weight C : N ratios were multiplied by the molar relation 14 / 12 (1.16) in order to convert weight ratios into molar ratios. 4. Results 4.1. Corg, Cinorg and C / N The sediment lying on the deepest and innermost areas of the rı´a is composed mainly of mud (see Vilas et al., 2005 for a detailed cartography). Sand content is low with only Stations 4 and 29 containing some percentage of the sand fraction (b 30%) mainly bioclasts (Fig. 3a). Corg concentrations are high (Fig. 3b), and show a clear increasing trend from the outer sites (2–2.5%) to the innermost areas (3.5–4%). C / N values of the outer stations fluctuate between 10 and 13 whereas the inner stations show values N15, except for the stations 41 and 45 whose C / N values are similar to the outer stations (Fig. 3c). 4.2. Live benthic foraminifera Densities of live benthic foraminifera in surface sediments (0–1 cm) are shown in Fig. 4 and total numbers and counts separated into fractions N 63–125 Am, N 125– 250 Am and N 250 Am are displayed in Supplementary Table 1. Total foraminiferal standing stocks from the superficial sediments varied between 74 and 1358 individuals per 50 cm3. The highest abundance is recorded at the outer stations in September (Stations 12 and 18), whereas at the innermost stations the number of live foraminifera seldom exceeded 300 individuals/50 cm3 in both sampling periods. Differences in population densities between stations are more remarkable in Sep-

P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18

Fig. 3. Content of Cinorg (a), Corg (b) and Corg:N ratio (c) in surface sediments from the September sampling period. Continuous line in (c) represents the C : N dry weight ratio and dashed line represents the C : N molar ratio. Standard error is also given.

tember than in January (Fig. 4). At the outermost stations the abundance of live foraminifera differs between nearby stations. For example, at station 13 the standing

7

stock only increased by 27 individuals from January to September, whereas at stations 7 and 12 located less than 2 km away from station 13, the abundance of live foraminifera increased significantly. Comparison of Fig. 3b with Fig. 4 shows the absence of a clear relation between the Corg content of the sediments and the abundance of live benthic foraminifera, although there seems to be a threshold in the Corg values (~N 3.5%) at which the abundance of benthic foraminifera is low whatever the sampling period. The most abundant species of the outer area of the rı´a are Brizalina spathulata (Williamson), Brizalina dilatata (Reuss) and Stainforthia fusiformis (Williamson). The distinction between B. spathulata and B. dilatata becomes difficult sometimes because of the size of the individuals and the presence of intermediate forms. For discussion purposes both species are combined in a group (B. spathulata/dilatata). These species represent between 30% and 67% of the life assemblage from station 4 to station 36 (Fig. 5a,b). The change from downwelling (January sampling period) to upwelling (September sampling period) conditions is mainly recorded by the noticeable increase in the population of B. spathulata/dilatata (stations 12, 18 and 36; Fig. 5a) and S. fusiformis (stations 4, 12, 18 and 22; Fig. 5b). Such rise in the standing stocks is reflected in the relative contribution of these species to the life assemblage, except for S. fusiformis at station 4 and B. spathulata/dilatata at stations 12 and 18. B. spathulata/dilatata group shows a more

Fig. 4. Abundance of live benthic foraminifera (bars) expressed as total number of stained individuals N63 Am per 50 cm3 and relative abundance of live foraminifera confined to the 63–125 Am fraction (full and dashed lines) in both sampling periods.

8

P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18

widespread spatial distribution than S. fusiformis, which is restricted to the most outer parts of the rı´a (from station 4 to 22). Rectuvigerina phlegeri Le Calvez shows a similar spatial distribution to the

former species although its abundance is much lower (Fig. 5c). The inner rı´a is characterized by the dominance of an agglutinated species, Eggerelloides scaber (Williamson), with the highest relative abundance

Fig. 5. Absolute abundance (bars) and percentage (full and dashed lines) of the most significant live benthic foraminiferal species in both sampling periods. The absolute abundance is indicated as number of individuals N63 Am of a particular species per 50 cm3. Pie charts represent the size fraction distribution of each particular species. The percentage of each species in each fraction (63–125 Am, 125–250 Am and N250 Am) was calculated taking into account both sampling periods. Total and separate counts are shown in Supplementary Table 1.

P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18

9

Fig. 5 (continued).

of this taxon being recorded at station 41 in both sampling periods. During summer, the standing stock of E. scaber increased significantly at stations 36, 39, 40 and 44 (Fig. 5d). At station 44 the relative contribution of this species shows similar values to that of station 45 despite the latter station having almost half of the standing stock of station 44. Hopkinsina atlantica (Cushman) and Buliminella elegantissima (dVOrbigny) show a similar spatial distribution (Fig. 5e, f) and contribute b 20% to the life assemblage of the innermost part of the rı´a. Nonion commune (dOrbigny) and the group Bulimina gibba/elongata do not show any particular spatial or seasonal trend (Fig. 5g, h), with the exception of the peaks shown in summer by N. commune (Fig. 5g) and B. gibba/elongata (Fig. 5h) at station 26 and 36, respectively. Apart from the aforementioned taxa, four other species, Bolivinellina translucens (Phleger and Parker), Nonionella turgida (Williamson), Nonionella stella Cushman and Moyer and Leptohalysis scottii Chaster, show striking features: they are practically absent from the January life assemblage but their absolute and relative abundance increases significantly in the September sampling period and each of these species peaks in a particular station, where the other three species are almost excluded (Fig. 5i–l).

The majority of live benthic foraminifera occur in the fine size fraction (63–125 Am fraction, Fig. 4). The dominance of the finest fraction in the life assemblage is explained by most of the species being confined to that particular size fraction (pie charts in Fig. 5). For example, B. spathulata/dilatata, S. fusiformis, B. elegantissima, H. atlantica, N. stella, B. translucens and L. scottii are only found in the 63–125 Am fraction. On the contrary, N. turgida, N. commune and R. phlegeri are large species (125–250 Am), although some juvenile specimens can be found in the 63–125 Am fraction. Very few abundant species show similar number of tests in the 63–125 Am and 125–250 Am fractions. In particular, E. scaber and B. gibba/elongata are represented by both tiny tests (63–125 Am, probably juvenile forms) and large ones (for further details see Supplementary Table 1). 5. Discussion 5.1. Foraminiferal abundance and sedimentary Corg The Corg concentration in the sediments of the Rı´a de Vigo is high and shows typical values of fine grain sediments deposited in eutrophic environments (N 2– 4%, Fig. 3b). The abundance of live benthic foraminif-

10

P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18

era in the Rı´a de Vigo (Fig. 4) is comparable to the densities reported from other shallow water and organic carbon-rich environments. For example, Murray (1986) observed densities of 144–2092 individuals/30 cm3 (0– 1 cm interval) in muddy substrates of Lyme Bay (25–50 m depth); Gustafsson and Nordberg (1999) recorded abundances from 10 to 125 individuals/10 cm3 (0–3 cm interval) at very high organic carbon content settings (4.8–7.1% Corg) in the Koljo¨ fjord (18–43 m depth). At the Havstens fjord, Gustafsson and Nordberg (2000) showed live benthic foraminiferal densities of 1.13– 21.43 individuals/cm3 (0–2 cm interval) in samples containing 3–4.1% of Corg (12–40 m depth). However, if we compare the population densities found in the study area with the standing stocks displayed by some continental shelf areas, our values may be considered low. For example, Alve and Murray (1995) found densities of 98–120 individuals/cm3 (0–2 cm interval) on the continental shelf of Skagerrak in organic rich sediments (483–514 m depth and 3.3–4% of Corg) and Murray (2003) reported foraminiferal standing stocks higher than 221 individuals/10 cm3 (0–1 cm interval) on the continental shelf west of Scotland (167–218 m depth; 0.3–1.7% of Corg). Nevertheless, the densities displayed by Scott et al. (2003) at the Celtic Sea (41– 116 m depth) were similar (1.33 to 144.4 individuals/10 cm3, 0–1 cm interval) to those ones recorded in this study. The C / N of the sediments has been commonly considered as a proxy of organic carbon origin (see review in Meyers, 1997), however selective degradation of organic compounds during early diagenesis tends to modify (usually increase) C / N values in the water column. The C : N molar ratio of the total plankton in the Rı´a de Vigo is 6.1; with phytoplankton being 7.4 and marine detritus being 6.2 (Rı´os and Fraga, 1987). However, the C : N molar ratio measured in the particulate organic matter (POC/PON) is slightly higher. For example, Doval et al. (1997) determined values between 6.9 and 7.4 in the upper part of the water column (b 15 m) and values from 8.7 to 11 in the bottom water (40 m). Torres-Lo´pez et al. (2005) showed an increase in the C : N molar ratio with water depth, with values oscillating between 9.3 and 12 in the bottom waters depending on the intensity of the upwelling. The latter values are close to the C : N molar ratio measured in the sediments from the outer Rı´a de Vigo, therefore it could be assumed that C / N values V 12 are derived directly from the marine primary production. In the nearby Rı´a de Pontevedra, Dale and Prego (2002) demonstrated the importance of the N lost in the sediment–water interface, so that the intense

organic matter degradation processes both in the water column and in the benthic boundary layer might increase the sedimentary C / N values. Many sapropels from the eastern Mediterranean region derived from marine organic sources have C / N values in the range of land plants (N 15, see Bouloubassi et al., 1999 for an overview). These authors hypothesised that the intense diagenetic transformation of the organic matter in the sediment by sulphate-reducing bacteria is responsible for the relative high C / N values in the sapropels. The anaerobic mineralization of the organic detritus is important in the nearby Ria de Arosa and Ria de Muros (Tenore et al., 1982), and therefore it could be also applicable to the Rı´a de Vigo. The Bouloubassi et al. (1999) hypothesis could explain the high C / N values in the most inner areas of the Rı´a de Vigo, where the primary production and hence the organic carbon flux to the sea floor are enhanced (Prego, 1993; Gago, 2000). As a result we favour the idea that the organic carbon content along the longitudinal transect on the muddy central part of the Ria de Vigo is derived mainly from marine primary production on the euphotic zone. The spatial distribution of opal content in the Rı´a de Vigo shows a similar longitudinal trend to Corg, with relative low values in the most oceanic areas and high values (around 3% opal) in the innermost part of the rı´a (Berna´rdez et al., 2005), also suggesting the importance of phytoplankton production in the composition of organic matter. Therefore the spatial distribution of Corg in the superficial sediments records the yearly spatial trends in the water column primary productivity and the organic carbon flux to the rı´a bottom (Prego, 1993; Gago, 2000), indicating that there is a strong degree of pelagic–benthic coupling between the surface waters and the seabed. In spite of this coupling, the abundance of benthic foraminifera living in the first centimetre of the sediment seemingly is not clearly related to the Corg concentrations in the surface sediments (compare Fig. 3b with Fig. 4). It could be argued that in muddy shallow coastal and shelf environments it might be difficult to distinguish the influence of food and oxygen on benthic foraminiferal distribution patterns, as suggested by van der Zwaan et al. (1999).The degradation of high amounts of Corg could cause a high oxygen consumption resulting in a rapid decrease of the oxygen in the bottom and interstitial waters. Although suboxic or anoxic conditions do not have a direct lethal effect on the majority of species (Alve and Bernhard, 1995; Moodley et al., 1997, 1998; Duijnstee et al., 2003), low oxygenation levels in the sediment or particular redox gradients could limit benthic foraminiferal standing stocks and species distribution (van der Zwaan

P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18

et al., 1999). Whatever the sampling period the lowest benthic foraminiferal standing stocks are recorded at the innermost stations where the Corg concentration is higher than ~3.5%. The overconsumption of oxygen caused by the degradation of very high amounts of organic carbon, the development of anoxia and/or redox processes into the sediment could explain the low foraminiferal densities as well as the relative low number of species at these stations (e.g. stations 40, 44 and 45; Fig. 4). At Corg values lower than 3.5% the foraminiferal densities depend on the sampling period, so the availability of oxygen should not control the abundance of benthic foraminifera at those stations. The abundance of live benthic foraminifera in the samples taken in the January sampling period surprisingly do not show large differences between sites containing different organic carbon percentages (Fig. 4). During the downwelling season, the concentration of chlorophyll-a in the bottom waters is very low (Fig. 2d) and the box models predict a negative organic carbon flux to the sea bottom (Roso´n et al., 1999; Gago, 2000), which eventually would increase the oxygen concentration in the bottom waters and at the benthic boundary layer. Under these conditions, foraminifera would feed on organic material from the former upwelling events. Such organic compounds could consist of refractory organic debris, which could be in part inert and not available as a food source for foraminifera since the bacterial breakdown of refractory organic matter into labile organic matter is a slow process (Fenchel and Finlay, 1995). Consequently, the percentage of sedimentary organic carbon per se is not a good indicator of food availability and organic-rich sediments seem not to be potential food, at least not for the foraminifera living along the muddy central axis of the Rı´a de Vigo. This fact has also been shown in other organic rich environments (Gustafsson and Nordberg, 1999). 5.2. Response of benthic foraminifera to upwelling events In the September sampling period, the spatial distribution of live benthic foraminiferal standing stocks show several features: 1) certain degree of spatial heterogeneity and 2) a more marked increase in the abundance of benthic foraminifera in outer and middle sites (Fig. 4). The increase in the abundance of benthic foraminifera suggests that freshly deposited phytoplankton during the successive upwelling events that characterise the upwelling season is the most significant triggering mechanism for population growth. The influx of biologically labile material not only increases

11

the quality of food on the seafloor but could also enhance bacterial activity. Phytoplankton blooms enhancing bacteria growth and activity have been reported from field studies in deep sea sediments (Pfannkuche, 1993; Pfannkuche et al., 1999, 2000) and in continental margins (Pfannkuche and Soltwedel, 1998). Foraminifera could either feed directly on bacterial stocks or bacteria could degrade organic compounds that are not suitable for consumption by benthic foraminifera in their original form (Jorissen et al., 1998). Despite the fact that it has been suggested that the vertical distribution of benthic foraminifera might be influenced by the selective feeding of foraminifera on specific bacteria or nutritious particles produced by these bacteria (Jorissen et al., 1998) which in themselves are vertically distributed into the sediment according to the successive redox stages (van der Zwaan et al., 1999), the role of bacteria in the foraminiferal diet is not clear (see Langezaal et al., 2003). Some studies reported that bacteria can be an important food resource for some foraminiferal species (see, e.g. Bernhard and Bowser, 1992; Langer and Gehring, 1993), whilst others noted that foraminifera did not feed preferably on bacteria after the addition of food in laboratory experiments (Heinz et al., 2002). The input of organic carbon could benefit directly those benthic foraminifera able to rapidly reproduce and colonize the fresh deposited detrital aggregates, whilst bacteria might favour foraminifera that respond much slower to fresh food supply and therefore are at a disadvantage compared to the high opportunistic species. Patchy distributions are a common characteristic of benthic foraminiferal distributions in most shallow subtidal environments (Hohenegger et al., 1993; Murray and Alve, 2000), however field studies demonstrated that the spatial variability in species abundance does not obscure any temporal change (Silva et al., 1996; Fontanier et al., 2003). In this work we can not assess small-scale patchiness (metres or centimetres), but our data indicates that the differences in the foraminiferal standing stocks between stations separated a few kilometres (2–3 km) could be due to large-scale variability (Fig. 4). Such spatial heterogeneity is probably due to the same scale patchiness as the food supply. The record of higher live benthic foraminiferal densities in the outer and middle areas of the Rı´a de Vigo cannot be explained by longitudinal differences in the organic carbon quality, in agreement with the small size of the basin. The addition of organic material triggers an increase in foraminiferal populations as long as it does not cause a negative effect in the foraminiferal assemblages inhabiting the sediment before the bloom.

12

P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18

If the increase in organic carbon flux causes a rapid decrease of the oxygen and/or reducing conditions in the pore waters, benthic foraminiferal populations could diminish or remain in the same values as those in the January sampling period. This seems to occur in the innermost sites where the abundance of benthic foraminifera does not change significantly from the January to September sampling periods. Upwelling events, apart from increasing the standing stock of the most abundant species, lead to the appearance of four new species (B. translucens, N. stella, N. turgida, and L. scottii) (Fig. 5i–l). Except for N. turgida, which dominates in the N 125 Am fraction, N. stella, B. translucens and L. scottii are confined to the 63–125 Am fraction both in life and dead assemblages. The presence of L. scottii in the small fraction is justified by its long shape rather than its small size. N. turgida, N. stella, B. translucens and L. scotti may have been dormant until the arrival of fresh organic carbon, when they switch to an active state. This indicates that they are opportunistic species that react quickly to the input of labile organic matter, probably colonising the labile organic aggregates. The reproduction of theses species may have occurred a few weeks before the September sampling period. Corliss and Silva (1993) and Silva et al. (1996) found that N. stella matured in less than 3 months after a phytodetritus event and considered this species as opportunistic at San Pedro Basin (California). In contrast with our data, these

authors reported significant low numbers of N. stella in the 63–150 Am fraction and high densities in the N150 Am fraction. In the Rı´a de Vigo, N. stella is exclusive to the 63–125 Am. The absence of large individuals (N 125 Am) of N. stella in the death assemblage (unpublished data) suggests that it displays rapid reproduction but low growth rate. Gustafsson and Nordberg (2001) showed that deposited phytoplankton is the main food resource for S. fusiformis and N. turgida and that both species can reproduce from juvenile to adult in less than a month. In our study N. turgida is mainly observed in the N 125 Am fraction although some individuals were found in the 63–125 Am fraction. As far as we know, other field studies do not report both N. stella and N. turgida peaking in the same life assemblages. There might be different taxonomic assignations of the same species (e.g. Plate 1, Figs. 4 and 5 from Gustafsson and Nordberg, 2001 looks N. stella more than N. turgida) and/or both are juvenile (N. stella) and adult (N. turgida) morphotypes of the same species. The spatial distribution of these four species is erratic and it is uncommon that all of them peak in the same sample (Fig. 5i–l). It suggests that each of these species colonize the patchy distributed organic aggregates following their specific nutritional requirements (diatoms, bacteria, small algae, etc.). The species-specific food preferences or response times to fresh organic matter have also been suggested in situ

Fig. 6. Summary of the effects of downwelling (a) and upwelling (b) on live benthic foraminifera from the muddy central axis of the Rı´a de Vigo. Upper graphs represent the abundance of live benthic foraminifera in number of individuals (N63 Am) per 50 cm3 and down plots display the percentage of the E. scaber (continuous line), B. spathulata/dilatata + S. fusiformis (dashed line) and the percentage of B. translucens + N. stella + N. turgida + L. scottii (circles) in January (a) and September (b) sampling periods.

P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18

tracer experiments to explain different responses among species to algal carbon inputs (Nomaki et al., 2005). The hypothetical heterogeneity in the fresh organic carbon distribution is clearly showed in Fig. 5i–l. Station 13 experienced neither an increase in the abundance of benthic foraminifera nor was colonized by any of these four species. This indicates that this station did not experience the supply of fresh organic carbon. The inferred ecological attributions of N. turgida, N. stella, B. translucens and L. scottii differ between the Rı´a de Vigo and other regions. For example, some laboratory experiments and field studies have demonstrated the resistance of N. stella (Bernhard and Bowser, 1999; Bernhard et al., 2000) and N. turgida (Duijnstee et al., 2003) to reducing and/or very low oxygen conditions as well as the intolerance of L. scottii to severe dysoxic microenvironments (Moodley et al., 1997; Ernst et al., 2002; Duijnstee et al., 2003). Different ecological attributions of the same species may be an expected fact since the ecological niche of each species is controlled by threshold limits for each factor or different factors or a combination of factors may be limiting distributions spatially and temporally (Murray, 2001). The response of benthic foraminifera to seasonal upwelling events could be related to the reproductive strategy of the species. If the species that constitute the background assemblage (January assemblage) show a large reproductive potential (r-strategists), the response to fresh organic carbon input results in a significant rise of absolute abundance. On the contrary, if the assemblage is constituted by k-selected reproductive species which spend more energy on increasing the size, the resulting number of foraminifera will be lower than in the case of r-strategists. In the Rı´a de Vigo, these two reproductive strategies are clearly separated along the longitudinal axis: outer sites are characterised by different species of small size (63–125 Am) and inner areas are dominated by one species with representatives in small and large size fractions (Fig. 6). In the outer rı´a (stations 4–26), the most abundant species, B. spathulata/dilatata and S. fusiformis are exclusive to the fine fraction (63–125 Am) in both life (this study) and death assemblages (unpublished data) indicating that they do not reach an adult size. S. fusiformis is a tiny species and commonly found in the 63– 125 Am fraction (Alve, 2003), but B. spathulata/dilatata has been recorded in the N125 Am fraction in other areas (e.g. Jannink et al., 1998). Although laboratory experiments and field studies have demonstrated the resistance of B. spathulata, B. dilatata (Moodley et al., 1997;

13

Jannink et al., 1998) and S. fusiformis (Bernhard and Alve, 1996; Moodley et al., 1998) to reducing and/or very low oxygen conditions, in the Ria de Vigo the abundance of these species is mainly controlled by the changes induced by upwelling events (Fig. 5a,b). The opportunistic behaviour of B. spathulata/dilatata and S. fusiformis has been suggested by other authors (Jorissen et al., 1992; Alve, 2003). The role of small size foraminifera in oligotrophic deep sea environments has been underlined by several authors in the NE Atlantic (Gooday, 1986), Arctic Ocean (Schewe, 2001) and the Arabian Sea (Kurbjeweit et al., 2000; Heinz and Hemleben, 2003). Field studies on benthic meiofauna showed the importance of the small size class in deep sea environments affected by episodic phytodetritus deposition (Pfannkuche and Soltwedel, 1998; Pfannkuche et al., 1999, 2000). It could be argued that in highly productive environments, assemblages dominated by dwarf foraminifera are a consequence of the lack of dissolved oxygen into the sediment (Perez-Cruz and Machain-Castillo 1990; Boltovskoy et al., 1991), but it has been also suggested that under favourable conditions foraminifera populations are characterized by small individuals, as a result of rapid reproduction (Bernhard and Reimers, 1991). Recently, Rathburn et al. (2001) have pointed out the importance of the 63– 150 Am fraction in high productive and oxygen-poor settings. If smaller size was the product of unfavourable conditions, low numerical densities would be expected. Our data indicate that populations dominated by small size species in the outer rı´a are a consequence of rapid and intense reproduction of foraminiferal species with high opportunistic behaviour. Small benthic foraminiferal species (63–125 Am fraction) would have greater potential for rapid population growth (Altenbach, 1992) in response to phytoplankton blooms. So, smaller sizes seem to be an adaptation of benthic foraminifera to perturbations on short time scales (downwelling/upwelling cycles) and under favourable environmental conditions such as high quality food, high oxygen concentrations in the sediment and diminished biological interactions. The arrival of labile organic carbon triggers reproduction more than growth in benthic foraminifera resulting in enhanced population growth of the rstrategists species (Fig. 6). Whereas the most abundant species at the outer sites are confined to the finest fraction, in the inner areas of the rı´a the dominant species E. scaber is represented by small and large individuals (Fig. 5d). The bimodal size distribution of E. scaber would indicate that it spends

14

P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18

energy on both reproduction and growth and behaves as a k-strategist. This strategy is a consequence of the high adaptation of E. scaber to the microenvironmental conditions of the inner rı´a. E. scaber has been considered as an opportunistic species in polluted and organic carbon rich (Alve, 1991, 1995a) and low oxygen environments (Alve, 1995b; Gustafsson and Nordberg, 2000). In laboratory experiments, Moodley and Hess (1992) showed its resistance to very low oxygen conditions; however Ernst et al. (2002) considered that it is not a redox indicator species. Scott et al. (2003) suggested that this species has a poorer tolerance to low oxygen concentrations than some opportunists, but it has a great ability to withstand fluctuations in diverse parameters. In the Ria de Vigo, E. scaber seems to be fully adapted to very high organic carbon concentrations (3–4% Corg, Figs. 3 and 5d) which probably represents poor oxygenated and reducing conditions, especially in the innermost parts of the rı´a. The highly ability of E. scaber to endure that microenvironment, which ought to persist through most of the year, allows this species to behave as a k-strategist dwelling mainly in the habitat of the small-size fraction species (Fig. 6). For example, B. spathula/dilatata is a well adapted group to different environments in the Rı´a de Vigo. It inhabits coarse grain sediments under moderate bottom current regimes (Diz et al., 2004), characterizes the life assemblage of outer rı´a and dwells with low abundance at the inner sites. Diminished abundances of B. spathulata/dilatata and others small species as B. elegantissima and H. atlantica in the inner rı´a are likely not only due to unfavourable microenvironmental conditions but also to the great competitiveness of E. scaber for space. The size distribution in the inner parts of the rı´a seems to be an adaptation of benthic foraminifera to long time-scale perturbations under medium/poor environmental conditions into the sediment and enhanced biological interactions.

dation processes could cause low oxygen and/or reducing conditions in the sediment. The response of benthic foraminifera to high quality organic carbon inputs depends on the reproductive strategy of the species that constitute the assemblage. In the outer and middle areas of the Rı´a de Vigo, benthic foraminiferal assemblages are characterized by small sized species (B. spathulata/dilatata and S. fusiformis) which show rapid population growth in reaction to phytoplankton blooms (r-strategists). Such a strategy could be an adaptation of benthic foraminifera to perturbations on short time scales (downwelling/ upwelling cycle) under favourable microenvironmental conditions. At the inner sites the sediment is mainly inhabited by E. scaber which behaves as a k-strategist. This is a result of the adaptation of this species to long term perturbations, such as relative low oxygen and/or reducing microenviromental conditions, as well as to its ability to compete for space. At these sites the seasonal upwelling determines both reproduction and growth of the dominant species, hence the increase in population densities are diminished compared to the outer areas. Highly opportunistic species such as B. translucens, N. stella, N. turgida and L. scottii switch from a dormant to an active state after the deposition of fresh organic carbon. These four species should colonize the patchily distributed organic aggregates following their specific nutritional requirements. The response of benthic foraminiferal faunas to the seasonal input of high quality organic carbon suggests that organic carbon-rich environments can be also limited by food availability. Our results make clear the importance of the study of the N 63 Am fraction to the understanding of the ecology of modern benthic foraminifera, as well as the correct interpretation of the fossil record. If this study were based on the N125 Am we would not have recorded completely the fingerprint of the seasonal upwelling on benthic foraminiferal assemblages.

6. Conclusions Acknowledgments Live benthic foraminifera along the muddy central axis of the Rı´a de Vigo were examined under two contrasting hydrographic conditions, downwelling and upwelling. The study of the abundance and species composition reveals that sedimentary organic carbon is not a good indicator of food availability for benthic foraminiferal faunas as these depend on the arrival of fresh organic carbon from upwelling events. Only in the most inner settings benthic foraminifera populations seem to be affected negatively by the arrival of excessive amounts of organic carbon, which through degra-

The authors are very grateful to Elizabeth Molyneux for improving the English text. We appreciate the comments and suggestions from J.W. Murray and an anonymous reviewer that resulted in final ameliorations of the manuscript. We thank Centro de Control da Calidade do Medio Marin˜o (CCCMM) for providing the hydrographic data. This paper was written whilst the first author was financially supported by the post-doctoral research grant EX-2004-0918 funded by the Spanish Ministerio de Educacio´n y Ciencia.

P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18

Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/ j.jmarsys.2005.11.001. References Altenbach, A.V., 1992. Short term processes and patterns in the foraminiferal response to organic flux rates. Marine Micropaleontology 19, 119 – 129. Altenbach, A.V., Struck, U., 2001. On the coherence of organic carbon flux and benthic foraminiferal biomass. Journal of Foraminiferal Research 31, 79 – 85. Altenbach, A.V., Lutze, G.F., Schiebel, R., Scho¨nfeld, J., 2003. Impact of interrelated and interdependent ecological controls on benthic foraminifera: an example from the Gulf of Guinea. Palaeogeography, Palaeoclimatology, Palaeoecology 197, 213 – 238. Alvarez-Salgado, X.A., Gago, J., Mı´guez, B.M., Pe´rez, F.F., 2001. Net ecosystem production of dissolved organic carbon in a coastal upwelling system: the Ria de Vigo, Iberian margin of the North Atlantic. Limnology and Oceanography 46, 135 – 147. Alve, E., 1991. Benthic foraminifera in sediment cores reflecting heavy metal pollution in Sorfjord, western Norway. Journal of Foraminiferal Research 21, 1 – 19. Alve, E., 1995a. Benthic foraminiferal responses to estuarine pollution: a review. Journal of Foraminiferal Research 25, 190 – 203. Alve, E., 1995b. Benthic foraminiferal distribution and recolonization of formerly anoxic environments in Drammensfjord, southern Norway. Marine Micropaleontology 25, 169 – 186. Alve, E., 2003. A common opportunistic foraminiferal species as an indicator of rapidly changing conditions in a range of environments. Estuarine, Coastal and Shelf Science 57, 501 – 514. Alve, E., Bernhard, J.M., 1995. Vertical migratory response of benthic foraminifera to controlled oxygen concentrations in a experimental mesocosm. Marine Ecology. Progress Series 116, 137 – 151. Alve, E., Murray, J.W., 1994. Ecology and taphonomy of benthic foraminifera in a temperate mesotidal inlet. Journal of Foraminiferal Research 24, 18 – 27. Alve, E., Murray, J.W., 1995. Benthic foraminiferal distribution and abundance changes in Skagerrak surface sediments: 1937 (Ho¨glund) and 1992/1993 data compared. Marine Micropaleontology 25, 269 – 288. Bakun, A., Nelson, C.S., 1991. The seasonal cycle of wind-stress curl in subtropical eastern boundary current regions. Journal of Physical Oceanography 21, 1815 – 1834. Beaulieu, S.E., 2002. Accumulation and fate of phytodetritus on the sea floor. In: Gibson, R.N., Barnes, M., Atkinson, R.J.A. (Eds.), Oceanography and Marine Biology An Annual Review, vol. 40. Taylor and Francis, London, pp. 171 – 232. ´ lvarez, R., 2005. Berna´rdez, P., Prego, R., France´s, G., Gonza´lez-A Opal content in the Rı´a de Vigo and Galician continental shelf: biogenic silica in the muddy fraction as an accurate paleoproductivity proxy. Continental Shelf Research 25, 1249 – 1264. Bernhard, J.M., 1988. Postmortem vital staining in benthic foraminifera: duration and importance in population and distributional studies. Journal of Foraminiferal Research 18, 143 – 146. Bernhard, J.M., Alve, E., 1996. Survival, ATP pool, and ultrastructural characterization of benthic foraminifera from Drammensf-

15

jord (Norway): response to anoxia. Marine Micropaleontology 28, 5 – 17. Bernhard, J.M., Bowser, S.S., 1992. Bacterial biofilms as a trophic resource for certain benthic foraminifera. Marine Ecology. Progress Series 83, 263 – 272. Bernhard, J.M., Bowser, S.S., 1999. Benthic foraminifera of dysoxic sediments: chloroplast sequestration and functional morphology. Earth-Science Reviews 46, 149 – 165. Bernhard, J.M., Reimers, C.E., 1991. Benthic foraminiferal population fluctuations related to anoxia: Santa Barbara Basin. Biogeochemistry 15, 127 – 149. Bernhard, J.M., Buck, K.R., Farmer, M.A., Bowser, S.S., 2000. The Santa Barbara Basin is a symbiosis oasis. Nature 403, 77 – 80. Boltovskoy, E., Scott, D.B., Medioli, F.S., 1991. Morphological variations of benthic foraminiferal tests in response to changes in ecological parameters: a review. Journal of Paleontology 65, 175 – 185. Bouloubassi, I., Rullko¨tter, J., Meyers, P.A., 1999. Origin and transformation of organic matter in Pliocene–Pleistocene Mediterranean sapropels: organic geochemical evidence reviewed. Marine Geology 153, 177 – 197. Corliss, B., Silva, K.A., 1993. Rapid growth of deep sea benthic foraminifera. Geology 21, 991 – 994. Dale, A.W., Prego, R., 2002. Physico-biogeochemical controls on benthic–pelagic coupling of nutrient fluxes and recycling in a coastal upwelling system. Marine Ecology. Progress Series 235, 15 – 28. De Rijk, S., Jorissen, F.J., Rohling, E.J., Troelstra, S.R., 2000. Organic flux control on bathymetric zonation of Mediterranean benthic foraminifera. Marine Micropaleontology 40, 151 – 166. De Stigter, H.C., Jorissen, F.J., van der Zwaan, G.J., 1998. Bathymetric distribution and microhabitat partitioning of live (Rose Bengal stained) benthic foraminifera along a shelf to bathyal transect in the southern Adriatic Sea. Journal of Foraminiferal Research 28, 40 – 65. Diz, P., France´s, G., Costas, S., Souto, C., Alejo, I., 2004. Distribution of benthic foraminifera in coarse sediments, Rı´a de Vigo, NW Iberian margin. Journal of Foraminiferal Research 34, 258 – 275. ´ lvarez-Salgado, X.A., Pe´rez, F.F., 1997. Dissolved Doval, M.D., A organic matter in a temperate embayment affected by coastal upwelling. Marine Ecology. Progress Series 157, 21 – 37. Duijnstee, I.A.P., Ernst, S.R., van der Zwaan, G.J., 2003. Effect of anoxia on the vertical migration of benthic foraminifera. Marine Ecology. Progress Series 246, 85 – 94. Ernst, S., van der Zwaan, B., 2004. Effects of experimentally induced raised levels of organic flux and oxygen depletion on a continental slope benthic foraminiferal community. Deep-Sea Research I 51, 1709 – 1739. Ernst, S., Duijnstee, I., Van der Zwaan, B., 2002. The dynamics of benthic foraminiferal microhabitat: recovery after experimental disturbance. Marine Micropaleontology 46, 343 – 361. Fenchel, T., Finlay, B.J., 1995. Ecology and Evolution in Anoxic Worlds. Oxford University Press, Oxford. Fontanier, C., Jorissen, F.J., Licari, L., Alexandre, A., Anschutz, P., Carbonel, P., 2002. Live benthic foraminiferal faunas from the Bay of Biscay: faunal density, composition, and microhabitats. Deep-Sea Research I 49, 751 – 785. Fontanier, C., Jorissen, F.J., Chaillou, G., David, C., Anschutz, P., Lafon, V., 2003. Seasonal and interannual variability of benthic foraminiferal faunas at 550 m depth in the Bay of Biscay. DeepSea Research I 50, 457 – 494.

16

P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18

Gago, J., 2000. Transformaciones Biogeoquı´micas y Flujos de Carbono en la Rı´a de Vigo. Ph.D. thesis, Universidad de Vigo, Spain, unpublished. ´ lvarez-Salgado, X.A., Pe´rez, F.F., 2001. Computing Gilcoto, M., A optimum estuarine residual fluxes with a multiparameter inverse method (OERFIM): application to the Ria de Vigo (NW Spain). Journal of Geophysical Research, C: Oceans 106, 31303 – 31318. Gooday, A.J., 1986. Meiofaunal foraminiferans from the bathyal Porcupine Seabight (north east Atlantic): size structure, standing stock, taxonomic composition, species diversity and vertical distribution in the sediment. Deep-Sea Research 33, 1345 – 1373. Gooday, A.J., 1988. A response by benthic foraminifera to the deposition of phytodetritus in the deep sea. Nature 332, 70 – 73. Gooday, A.J., 1993. Deep-sea benthic foraminiferal species which exploit phytodetritus: characteristic features and controls on distribution. Marine Micropaleontology 22, 187 – 205. Gooday, A.J., 1996. Epifaunal and shallow infaunal foraminiferal communities at three abyssal NE Atlantic sites subject to differing phytodetritus input regimes. Deep-Sea Research I 43, 1395 – 1421. Gooday, A.J., 2002. Biological responses to seasonally varying fluxes of organic matter to the ocean floor: a review. Journal of Oceanography 58, 305 – 332. Gooday, A.J., Hudges, J.A., 2002. Foraminifera associated with phytodetritus deposits at a bathyal site in the northern Rockall Trough (NE Atlantic): seasonal contrasts and a comparison of stained and dead assemblages. Marine Micropaleontology 46, 83 – 110. Gross, O., 2000. Influence of temperature, oxygen and food availability on the migrational activity of bathyal benthic foraminifera: evidence of microcosm experiments. Hydrobiologia 426, 123 – 137. Gustafsson, M., Nordberg, K., 1999. Benthic foraminifera and their response to hydrography, periodic hypoxic conditions and primary production in the Koljo¨ fjord on the Swedish west coast. Journal of Sea Research 41, 163 – 178. Gustafsson, M., Nordberg, K., 2000. Living (Stained) benthic foraminifera and their response to the seasonal hydrographic cycle, periodic hypoxia and to primary production in Havstens fjord on the Swedish West Coast. Estuarine, Coastal and Shelf Science 51, 743 – 761. Gustafsson, M., Nordberg, K., 2001. Living (Stained) benthic foraminiferal response to primary production and hydrography in the deepest part of the Gullmar fjord, Swedish west coast, with comparison to Ho¨glund’s 1927 material. Journal of Foraminiferal Research 31, 2 – 11. Heinz, P., Hemleben, Ch., 2003. Regional and seasonal variations of recent benthic deep-sea foraminifera in the Arabian Sea. Deep-Sea Research I 50, 435 – 447. Heinz, P., Kitazato, H., Schmield, G., Hemleben, Ch., 2001. Response of deep-sea benthic foraminifera from the Mediterranean Sea to simulated phytoplankton pulses under laboratory conditions. Journal of Foraminiferal Research 31, 210 – 227. Heinz, P., Hemleben, Ch., Kitazato, H., 2002. Time-response of cultured deep-sea benthic foraminifera to different algal diets. Deep-Sea Research I 49, 517 – 537. Herguera, J.C., 2000. Last glacial paleoproductivity patterns in the eastern equatorial Pacific: benthic foraminifera records. Marine Micropaleontology 40, 259 – 275. Hohenegger, J., Piller, W.E., Baal, C., 1993. Horizontal and vertical spatial microdistribution of foraminifers in the shallow subtidal Gulf of Trieste, Northern Adriatic Sea. Journal of Foraminiferal Research 23, 79 – 101.

Jannink, N.T., Zachariasse, W.J., Van der Zwaan, G.J., 1998. Living (Rose Bengal stained) benthic foraminifera from the Pakistan continental margin (northern Arabian Sea). Deep-Sea Research I 45, 1483 – 1513. Jorissen, F.J., Barmawidjaja, D.M., Puskaric, S., Van der Zwaan, G.J., 1992. Vertical distribution of benthic foraminifera in the northern Adriatic Sea: the relation with the organic flux. Marine Micropaleontology 19, 131 – 146. Jorissen, F.J., Wittling, I., Peypouquet, J.P., Rabouille, C., Relexans, J.C., 1998. Live benthic foraminiferal faunas off Cape Blanc, NW Africa: community structure and microhabitats. Deep-Sea Research I 45, 2157 – 2188. Kitazato, H., Shiryama, Y., Nakatsuka, T., Fujiwara, S., Shimanaga, M., Kato, Y., Okada, Y., Kanda, J., Yamaoka, A., Masuzawa, T., Suzuki, K., 2000. Seasonal phytodetritus deposition and responses of bathyal benthic foraminiferal populations in Sagami Bay, Japan: preliminary results from bProject Sagami 1996–1999Q. Marine Micropaleontology 40, 135 – 149. Kitazato, H., Nomaki, H., Heinz, P., Nakatsuka, T., 2003. The role of benthic foraminifera in deep-sea food webs at the sediment–water interface: results from in situ feeding experiments in Sagami Bay. Frontier Research on Earth Evolution 1, 227 – 232. Kuhnt, W., Hess, S., Jian, Z., 1999. Quantitative composition of benthic foraminiferal assemblages as a proxy indicator for organic carbon flux rates in the South China Sea. Marine Geology 156, 123 – 157. Kurbjeweit, F., Schmiedl, G., Schiebel, R., Hemleben, Ch., Pfannkuche, O., Wallman, K., Scha¨fer, P., 2000. Distribution, biomass and diversity of benthic foraminifera in relation to sediment geochemistry in the Arabian Sea. Deep-Sea Research II 47, 2913 – 2955. Langer, M.R., Gehring, C.A., 1993. Bacteria farming: a possible feeding strategy of some smaller, motile foraminifera. Journal of Foraminiferal Research 23, 40 – 46. Langezaal, A.M., Ernst, S.R., Haese, R.R., van Bergen, P.F., van der Zwaan, G.J., 2003. Disturbance of intertidal sediments: the response of bacteria and foraminifera. Estuarine, Coastal and Shelf Science 58, 249 – 264. Lavin, A., Diaz del Rı´o, G., Casas, G., Cabanas, J.M., 2000. Afloramiento en el noroeste de la Penı´nsula Ibe´rica. I´ndices de afloramiento para el punto 438N 118W. Perı´odo 1990–1999. Datos y Resu´menes Instituto Espan˜ol de Oceanografı´a 15, 25 pp. Licari, L.N., Schumacher, S., Wenzho¨fer, F., Zabel, M., Mackensen, A., 2003. Communities and microhabitats of living benthic foraminifera from the tropical East Atlantic: impact of different productivity regimes. Journal of Foraminiferal Research 33, 10 – 31. Linke, P., Altenbach, A.V., Graf, G., Heeder, T., 1995. Response of deep-sea benthic foraminifera to a simulated sedimentation event. Journal of Foraminiferal Research 25, 75 – 82. Loeblich, A.R., Tappan, H., 1987. Foraminifera Genera and Their Classification. Van Nostrand Reinhold, New York. Loubere, P., Fariduddin, M., 1999a. Quantitative estimation of global patterns of surface ocean biological productivity and its seasonal variation on timescales from centuries to millennia. Global Biogeochemical Cycles 13, 115 – 133. Loubere, P., Fariduddin, M., 1999b. Benthic foraminifera and the flux of organic carbon to the seabed. In: Sen Gupta, K. (Ed.), Modern Foraminifera. Kluwer Academic Publishers, The Netherlands, pp. 181 – 199. Meyers, P.A., 1997. Organic geochemical proxies of paleoceanographic, paleolimnologic, and paleoclimatologic processes. Organic Geochemistry 27, 213 – 250.

P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18 Moodley, L., Hess, C., 1992. Tolerance of infaunal benthic foraminifera for low and high oxygen concentrations. Biological Bulletin 183, 94 – 98. Moodley, L., van der Zwaan, G.J., Herman, P.M.J., Kempers, L., van Breugel, P., 1997. Differential response of benthic meiofauna to anoxia with special reference to foraminifera (Protista: Sarcodina). Marine Ecology. Progress Series 158, 151 – 169. Moodley, L., Schaub, B.E.M., van der Zwaan, G.J., Herman, P.M.J., 1998. Tolerance of benthic foraminifera (Protista: Sarcodina) to hydrogen sulphide. Marine Ecology. Progress Series 169, 77 – 86. Moodley, L., Boschker, H.T.S., Middelburg, J.J., Pel, R., Herman, P.M.J., de Deckere, E., Heip, C.H.R., 2000. Ecological significance of benthic foraminifera: 13C labelling experiments. Marine Ecology. Progress Series 202, 289 – 295. Moodley, L., Middelburg, J.J., Boschker, T.S., Duineveld, G.C.A., Pel, R., Herman, P.M.J., Heip, C.H.R., 2002. Bacteria and foraminifera: key players in a short-term deep-sea benthic response to phytodetritus. Marine Ecology. Progress Series 236, 23 – 29. Murray, J.W., 1986. Living and dead Holocene foraminifera of Lyme Bay, southern England. Journal of Foraminiferal Research 16, 347 – 352. Murray, J.W., 1991. Ecology and distribution of benthic foraminifera. In: Lee, J.J., Anderson, O.R. (Eds.), Biology of Foraminifera. Academic Press, London, pp. 221 – 250. Murray, J.W., 2001. The niche of benthic foraminifera, critical thresholds and proxies. Marine Micropaleontology 41, 1 – 7. Murray, J.W., 2003. Foraminiferal assemblage formation in depositional sinks on the continental shelf west of Scotland. Journal of Foraminiferal Research 33, 101 – 121. Murray, J.M., Alve, E., 2000. Major aspects of foraminiferal variability (standing crop and biomass) on a monthly scale in an intertidal zone. Journal of Foraminiferal Research 30, 177 – 191. Murray, J.W., Bowser, S.S., 2000. Mortality, protoplasm decay rate, and reliability of staining techniques to recognize blivingQ foraminifera: a review. Journal of Foraminiferal Research 30, 66 – 70. Nogueira, E., Figueiras, F.G., 2005. The microplankton succession in the Rı´a de Vigo revisited: species assemblages and the role of weather-induced, hydrodynamic variability. Journal of Marine Systems 54, 139 – 155. Nomaki, H., Heinz, P., Nakatsuka, T., Shimanaga, M., Kitazato, H., 2005. Species-specific ingestion of organic carbon by deep-sea benthic foraminifera and meiobenthos: in situ tracer experiments. Limnology and Oceanography 50, 134 – 146. Ohga, T., Kitazato, H., 1997. Seasonal changes in bathyal foraminiferal populations in response to the flux of organic matter (Sagamy Bay, Japan). Terra Nova 9, 33 – 37. Ohkushi, K., Natori, H., 2001. Living benthic foraminifera of the Hess Rise and Suiko Seamount, central North Pacific. Deep-Sea Research I 48, 139 – 1324. Perez-Cruz, L.L., Machain-Castillo, M.L., 1990. Benthic foraminifera of the oxygen minimum zone, Continental shelf of the Gulf of Tehuantepec, Mexico. Journal of Foraminiferal Research 20, 312 – 325. Pfannkuche, O., 1993. Benthic response to the sedimentation of particulate organic matter at BIOTRANS station, 478 N, 208 W. Deep-Sea Research II 40, 135 – 149. Pfannkuche, O., Soltwedel, T., 1998. Small benthic size classes along the N.W. European Continental Margin: spatial and temporal variability in activity and biomass. Progress in Oceanography 42, 189 – 207. Pfannkuche, O., Boetius, A., Lochte, K., Lundgreen, U., Thiel, H., 1999. Responses of deep-sea benthos to sedimentation patterns

17

in the North-East Atlantic in 1992. Deep-Sea Research I 46, 573 – 586. Pfannkuche, O., Sommer, S., Ka¨hler, A., 2000. Coupling between phytodetritus deposition and the small-sized benthic biota in the deep Arabian Sea: analyses of biogenic sediment compounds. Deep-Sea Research I 47, 2805 – 2833. ´ lvarez-Salgado, X.A., Roso´n, G., Herrera, J.L., Piedracoba, S., A 2005. Short-timescale thermohaline variability and residual circulation in the central segment of the coastal upwelling system of the Ria de Vigo (northwest Spain) during four contrasting periods. Journal of Geophysical Research, C: Oceans 110 (C3) Art. No. C03018. Prego, R., 1993. General aspects of carbon biogeochemistry in the ria of Vigo, northwestern Spain. Geochimica et Cosmochimica Acta 57, 2041 – 2052. Rathburn, A.E., Perez, M.E., Lange, C.B., 2001. Benthic-pelagic coupling in the Southern California Bight: Relationships between sinking organic material, diatoms and benthic foraminifera. Marine Micropaleontology 43, 261 – 271. Rı´os, A.F., Fraga, F., 1987. Composicio´n quı´mica elemental del plancton marino. Investigacio´n Pesquera 51, 619 – 632. Roso´n, G., Alvarez-Salgado, X.A., Perez, F.F., 1999. Carbon cycling in a large coastal embayment, affected by wind-driven upwelling: short-timescale variability and spatial differences. Marine Ecology. Progress Series 176, 215 – 230. Schewe, I., 2001. Small-sized benthic organisms of the Alpha Ridge, Central Arctic Ocean. International Review of Hydrobiology 86, 317 – 335. Scott, G.A., Scourse, J.D., Austin, W.E.N., 2003. The distribution of benthic foraminifera in the Celtic Sea: the significance of seasonal stratification. Journal of Foraminiferal Research 33, 32 – 61. Silva, K.A., Corliss, B., Rathburn, A.E., Thunell, R., 1996. Seasonality of living benthic foraminifera from San Pedro basin, California borderland. Journal of Foraminiferal Research 26, 71 – 93. Souto, C., Gilcoto, M., Farin˜a-Busto, L., Pe´rez, F.F., 2003. Modeling the residual circulation of a coastal embayment affected by wind-driven upwelling: circulation of the Ria de Vigo (NW Spain). Journal of Geophysical Research, C: Oceans 108 (C11) Art. No. 3340. Suhr, S.B., Pond, D.W., Gooday, A.J., Smith, C.R., 2003. Selective feeding by benthic foraminifera on phytodetritus on the western Antartic Peninsula shelf: evidence from fatty acid biomarker analysis. Marine Ecology. Progress Series 262, 153 – 162. Tenore, K.R., Boyer, L.F., Cal, R.M., Corral, J., Garcı´a-Ferna´ndez, G., Gonza´lez, N., Gonza´lez-Gurriaran, E., Hanson, R.B., Iglesias, J., Krom, M., Lo´pez-Jamar, E., McClain, J., Pamatmat, M.M., Pe´rez, A., Rhoads, D.C., de Santiago, G., Tietjen, J., Westrich, J., Windom, H.L., 1982. Coastal upwelling in the Rias Bajas, NW Spain: contrasting the benthic regimes of the Rı´as de Arosa and the Muros. Journal of Marine Research 40, 701 – 772. ´ lvarez-Salgado, X.A., Varela, R.A., 2005. OffTorres-Lo´pez, S., A shore export versus in situ fractionated mineralization: a 1-D model of the fate of the primary production of the Rı´as Baixas (Galicia, NW Spain). Journal of Marine Systems 54, 175 – 193. Van der Zwaan, G.J., Duijnstee, I.A.P., den Dulk, M., Ernst, S.R., Jannink, N.T., Kouwenhoven, T.J., 1999. Benthic foraminifers: proxies or problems? A review of paleoecological concepts. Earth-Science Reviews 46, 213 – 236. Varela, R.A., Roso´n, G., Herrera, J., Torres-Lo´pez, S., Ferna´ndezRomero, A., 2005. A general view of the hydrographic and dynamical patterns of the Rias Baixas adjacent shelf area. Journal of Marine Systems 54, 97 – 114.

18

P. Diz et al. / Journal of Marine Systems 60 (2006) 1–18

Vilas, F., Bernabeu, A.M., Me´ndez, G., 2005. Sediment distribution pattern in the Rias Baixas (NW Spain): main facies and hydrodynamic dependence. Journal of Marine Systems 54, 261 – 276. Waldron, H.N., Probyn, T.A., Brundrit, G.B., 1998. Carbon pathways and export associated with the southern Benguela upwelling system: a re-appraisal. South African Journal of Marine Science 19, 113 – 118. Widbom, B., Frithsen, J.B., 1995. Structuring factors in marine soft bottom community during eutrophication—an experiment with radio-labelled phytodetritus. Oecologia 101, 156 – 168. Witte, U., Wenzho¨fer, F., Sommer, S., Boetius, A., Heinz, P., Aberle, N., Sand, M., Cremer, A., Abraham, W.-R., Jorgensen, B.B., Pfannkuche, O., 2003. In situ experimental evidence of the fate

of a phytodetritus pulse at the abyssal sea floor. Nature 424, 763 – 766. Wollast, R., 1991. The coastal organic carbon cycle: fluxes, sources and sinks. In: Mantoura, R.F.C., Martin, J.M., Wollast, R. (Eds.), Ocean Margin Processes in Global Change. J. Wiley and Sons, pp. 365 – 381. Wollast, R., 1993. Interactions of carbon and nitrogen cycles in the coastal zone. In: Wollast, R., Mackenzie, F.T., Chou, L. (Eds.), Interactions of C, N, P and S Biogeochemical Cycles and Global Change, Berlin, pp. 195 – 210. Wollenburg, J.E., Kuhnt, W., 2000. The response of benthic foraminifers to carbon flux and primary production in the Arctic Ocean. Marine Micropaleontology 40, 189 – 231.