Microhabitat Selection of Benthic Foraminifera in Sediments Off the Rhône River Mouth (nw Mediterranean)

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MICROHABITAT SELECTION OF BENTHIC FORAMINIFERA IN SEDIMENTS OFF THE RHO ˆ NE RIVER MOUTH (NW MEDITERRANEAN)

MERYEMMOJTAHID^1,3,5, FRANCISCUSJORISSEN¹, BRUNOLANSARD^2,4ANDCHRISTOPHEFONTANIER¹ ABSTRACT

The microhabitats and the composition of living benthic foraminiferal faunas in the sediments deposited off the Rhoˆne River mouth are directly influenced by the Rhoˆne River input.

In this shallow-water environment (20–98 m water depth), the vertical distribution of the species is not well defined, probably due to the low penetration of oxygen into the sediment. We show the existence of two types of species:

‘‘predominantly superficial’’ taxa showing a density maximum in the topmost sediment layer, and ‘‘potentially/

predominantly infaunal taxa’’ that are also frequent in the topmost sediment, but which show considerable densities in anoxic deeper sediment layers as well. In the area that is strongly influenced by river input (near the river mouth and in the southwestern direction, following the river plume), the fauna is composed mostly of ‘‘potentially/predominantly infaunal’’ species adapted to a higher contribution of terrestrial organic matter, generally of lower quality, and to the low penetration of oxygen into the sediment. This fauna is composed of species tolerant to strong environmental stress (e.g., Nonionella turgida, Nonion scaphum, Rectuvigerina phlegeri, and Valvulineria bradyana). The stations less influenced by fluvial input (located south and east of the river mouth) are composed of species that colonize oxygenated interstices in the upper centimeter of sediment. The dominant species are mainly ‘‘predominantly superficial’’

taxa (e.g., Cassidulina carinata, Bulimina aculeata), which are known to react quickly to provisions of labile organic matter. The correlation between these two types of faunas and the two prevalent environmental factors suggests that the vertical distribution of living foraminifera in front of the Rhoˆne River mouth is primarily controlled by the quality of the organic matter and less by the quantity of the organic matter and depth of oxygen penetration into the sediment.

INTRODUCTION

In marine benthic environments, the organic-matter flux and the oxygenation and redox conditions at the bottom and in the interstitial waters are generally considered the major parameters controlling the density and composition of benthic foraminiferal faunas (e.g., Altenbach, 1988;

Altenbach and Sarnthein, 1989; Lutze and Thiel, 1989;

Mackensen and Douglas, 1989; Rathburn and Corliss, 1994; Jorissen and others, 1995; Rathburn and others, 1996;

Fariduddin and Loubere, 1997; Jorissen, 1999; Schmiedl and others, 2000; Morigi and others, 2001). On river- dominated ocean margins, large supplies of terrestrial organic matter, high primary production rates sustained by the high influx of nutrients, and limited water depth lead to organic-matter enrichment of the seafloor (McKee and others, 2004). This may eventually lead to an increase in the biomass and densities of benthic organisms, but also to hypoxia or anoxia at or just below the sediment-water interface, which can result in massive reduction or mortality of benthic faunas (e.g., Kemp and Boynton, 1992; Heip, 1995). With increased quantities of organic detritus reaching the seafloor, increased amounts of refractory organic matter tend to be preserved in the sediment (Westrich and Berner, 1984). Because high input of organic matter demands considerable amounts of oxygen for the consumption of its labile part, high organic flux in coastal environments often results in hypoxic bottom water, as higher-quality organic matter often accumulates at the sediment-water interface. In many continental shelf and marginal marine environments, oxygen penetrates only the top few millimeters to centimeters of the substrate (e.g., Jorgensen and Revsbech, 1989). Deeper in the sediment, conditions progressively change: oxygen concentration rapidly decreases, to attain a value of zero at several centimeters or millimeters depth. Oxygen penetrates deeper in sediments within oxic halos around metazoan burrows, in coarse substrates of high-energy, shallow-water environments, and in very oligotrophic deep-sea environments (e.g., Rutgers van der Loeff, 1990).

Higher-quality organic matter often accumulates at the sediment-water interface. With increasing depth in the sediment, any organic matter that has not been consumed by the macro- and meiofauna tends to contain more refractory components (Westrich and Berner, 1984), and will probably have lower nutritional value (Caralp, 1989;

Aller, 1994; Jorissen, 1999; Zegouagh and others, 1999).

Hence, benthic foraminifera tend to be most concentrated near the interface. However, those living in sediment, in some cases down to 10 cm, inhabit a succession of microhabitats (e.g., Basov and Khusid, 1983; Corliss, 1985; Lutze and Thiel, 1989; Corliss and Emerson, 1990;

Corliss, 1991; Loubere, 1991; Barmawidjaja and others, 1992; Rathburn and Corliss, 1994; Jorissen and others, 1998; Kitazato and others, 2000; Fontanier and others, 2002). According to the TROX-model (Jorissen and others, 1995) proposed for open-marine benthic foraminiferal faunas, epifaunal and superficial infaunal foraminifera profit from well-oxygenated conditions and from rather labile organic matter, whereas some deep infaunal foraminifera apparently tolerate interstitial anoxia (e.g., Bernhard and Reimers, 1991; Bernhard, 1992; Moodley and Hess,

3Present address: National Oceanography Centre, Southampton, Waterfront Campus, European way, Southampton SO14 3ZH, UK.

5Correspondence author. E-mail: [email protected]

4Present address: Earth & Planetary Sciences, McGill University, 3450 University Street, Montreal, Quebec H3A 2A7, Canada

1Laboratory of Recent and Fossil Bio-Indicators (BIAF), UPRES EA 2644, University of Angers 2, Boulevard Lavoisier, 49045 Angers Cedex, France, and Laboratoire d’Etude des Bio-Indicateurs Marins (LEBIM), Ker Chalon, 85350 Ile D’Yeu, France

2Laboratoire des Sciences du Climat et de l’Environnement (LSCE), UMR CEA-CNRS 1572 and Institut Pierre Simon Laplace (IPSL), Avenue de la terrasse, F-91198, Gif sur Yvette, France

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1992; Bernhard and others, 1997). In food-limited environments, which are commonly characterized by well-oxygenated bottom waters, both living foraminiferal standing stock and diversity are rather low, and the fauna largely consists of epifaunal and shallow infaunal species. In mesotrophic environments, standing stocks are moderately high, faunal diversity is at a maximum, and the corresponding fauna includes a variety of epifaunal and infaunal species. In eutrophic and strongly oxygen-limited environments, low-diversity faunas with high standing stocks prevail, mainly composed of deep-infaunal species tolerant of dysoxia (Jorissen and others, 1995). In such environments, the vertical species succession is often strongly compressed, and taxa that elsewhere occupy deep infaunal niches may be found near or at the surface. Unstable ecosystems, however, may provide exceptions to this scheme; several studies (e.g., Barmawidjaja and others, 1992; Gooday, 1993) suggest that certain opportunistic epifaunal species are very successful colonizers. Although a clear vertical succession of has been observed for deep-sea infaunal foraminifera, the profile in shallow substrates is more obscure (e.g., Buzas and others, 1993). This could be due to intensive and deep bioturbation or fine-grained sediments that restrict oxygen penetration. In shallow-water environments, most infaunal species of foraminifera have maximum live:dead ratios in the top centimeter of sediment.

Barmawidjaja and others (1992) recognize three types of infaunal foraminifera: 1) taxa that show a very strong maximum in the topmost centimeter, followed by rapid disappearance below; 2) taxa that are consistent in density for several centimeters of depth; and 3) taxa that live exclusively at or below the limit of oxygen penetration.

Following these distinctions, we adopt the following terms:

1) predominantly superficial taxa; 2) potentially infaunal taxa; and 3) predominantly infaunal taxa. However, in our study area, most infaunal taxa tend to be intermediate between the second and third types. In almost all cases, the topmost sediment layer contains significant numbers of

infaunal taxa. We therefore use the term ‘‘potentially/

predominantly infaunal’’ to describe species that can be found in significant abundance deeper in the sediment.

In muddy bottoms of the inner to middle shelf (0–90 m) of the Mediterranean Sea off France, dominant (.20%of fauna) benthic foraminifera include Ammonia spp. and Nonion commune. Other common (.10%) taxa are Non- ionella turgida,Bulimina aculeata,Textularia bocki,Textu- laria sagittula, Sigmoilopsis schlumbergeri, and Melonis barleeanus(Vene´c-Peyre´, 1984 in Murray, 2006).

The present study focuses on the vertical distribution of living benthic foraminifera in the.150-mm fraction of the same series of samples used in the recent study by Mojtahid and others (2009) on the foraminifera in the eutrophic ecosystem in front of the Rhoˆne River mouth (see below).

Our goal is to define the ecological requirements of the infaunal species and to gain a better understanding of the complex linkage between biological and geochemical processes at the sediment-water interface and within the surficial sediment layer.

FORAMINIFERA IN FRONT OF THE RHOˆ NE RIVER MOUTH

In a recent study, Mojtahid and others (2009) describe the geographical distribution of live benthic foraminifera in front of the Rhoˆne River mouth (see Fig. 1) for both the 63–150mm (top centimeter of the sediment) and .150-mm (top 5 cm) size fractions. The comparison of geochemical data with foraminiferal density and composition strongly suggests that the spatial distribution of foraminifera is primarily controlled by the quality and quantity of organic matter reaching the seafloor and more specifically, by the ratio between terrestrial and marine organic matter (Mojtahid and others, 2009). The total standing stock of stained foraminifera (.150-mm fraction) found in the 5-cm- deep sediment cores varied from 39 to 3,300 specimens for a surface area of 177 cm²(a total sediment volume of 883 cm³

FIGURE1. LeftSatellite image (MODIS image; 11/12/2002) of the eastern part of the Gulf of Lions showing the the river plume flowing to the southwest.RightLocation of the 23 sampling stations and bathymetry.

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FIGURE2. Figure summarizing Mojtahid and others (2009) data on living benthic foraminifera (.150-mm fraction,$5%in at least one station).a Total density (standardized for 100 cm²sediment surface), species richness (number of species), biodiversity (Shannon Wiener index), and the average living depth (ALD5) [new data].bRelative abundance of taxa typical of the stations close to the river mouth.cRelative abundance of taxa typical of stations under the river plume.dRelative abundance of taxa typical of distal stations. Stations have been grouped by Mojtahid and others (2009) on the basis of general similarity of foraminiferal assemblage composition and their response to the environmental conditions in front of the Rhoˆne River mouth.

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was studied), corresponding to a density of 22 to 1,880 individuals below a 100 cm²sediment surface (Fig. 2a). The total standing stock generally increases with distance from the river mouth (Fig. 2a) to the south, east, and west. In the .150-mm fraction, three principal foraminiferal assemblages occur. Assemblage I is present in the vicinity of the river mouth (stations 1, 3, and 5) where densities and diversity are low. It is dominated byNonionella turgida (averaging 18%at the stations close to the river mouth), Leptohyalis scottii (19%), Eggerella scabra (17%), Quinqueloculina seminula (7%), Ammonia beccarii (7%), and Elphidium macellum (2%) (Fig. 2b). 2) Assemblage II dominates the stations influenced by the river plume (stations 2, 6, 8, 12, 14, and 18). It is principally composed ofNonion scaphum (averaging 42% at the stations under the river plume), Valvulineria bradyana (15%), and Rectuvigerina phlegeri (5%) (Fig. 2c). 3) Assemblage III occupies the deepest substrates that are most distal from the river outflow (stations 16, 17, 19, 20, 22 and 24). It is characterized by Cassidulina carinata (averaging 23%), Bulimina aculeata (11%), andMelonis barleeanus(2%), which in some stations (especially to the east) are accompanied by the agglutinants Textularia agglutinans(5%),Recurvoides trochamminiformis (3%), and Adercotryma glomeratum (2%) (Fig. 2d). The foraminiferal assemblages at the eastern stations are probably less influenced by river outflow. Four stations have anomalous associations: stations 9 and 11 have a mixture of the three assemblage types, while stations 15 and 10 have Assemblage III, which is typical of the more distal stations (Fig. 2).

ENVIRONMENTAL SETTING

The Gulf of Lions is located in the northwestern Mediterranean Sea and represents a prograding margin with a wide, crescent-shaped shelf and a continental slope incised by numerous canyons descending to the abyssal floor of the Algero-Balearic basin (Monaco and others, 1990). It receives terrestrial sediment from the Rhoˆne River, one of the largest rivers in the Mediterranean region, and from numerous torrential rivers along the western Languedoc–Roussillon coast. The Rhoˆne River accounts for most (averaging.90%) of the fluvial discharge into the Gulf of Lions. The hydrological regime of the Rhoˆne River is characterized by a large difference between low (,700 m³ s²¹) and high (.3,000 m³ s²¹) water discharges (Pont and others, 2002).

Sediment discharge ranges 7–103 10⁶ t yr²¹ according to different estimates (Sempe´re´ and others, 2000; Pont and others, 2002; Bourrin and Durrieu de Madron, 2006), with very marked interannual variations. River discharge is fed by oceanic fronts, snowmelt, and marine storms, and exhibits marked summer lows, spring and autumn peaks, and strong interannual variability. The largest floods, which are generally associated with storm events, transport most of the sediment; for example, 80%of sediment discharge into the Rhoˆne occurs when water discharge exceeds 3,000 m³s²¹ (Pont and others, 2002).

The investigated sites of this study are located off the Rhoˆne River mouth covering an area of about 250 km² (Fig. 1). Sources of its organic matter include the terrain of its watershed and marine biological production (Gadel and

others, 1990; Monaco and others, 1990; Buscail and Germain, 1997). During the wet seasons of autumn and winter, the inflow of terrestrial organic matter increases.

Primary production is highly seasonal and mostly controlled by nutrient supply, shoaling of the mixed layer, and availability of sunlight. Sediments of the study area consist mostly of silty mud (Durrieu de Madron and others, 2003) with a high content of organic carbon (1–2%; see Mojtahid and others, 2009). Three sedimentary units are present, as defined by Aloı¨si (1986): 1) the silty sand delta front (5–20 m water depth), 2) the silty clay prodelta (20–60 m water depth), and 3) the clayey distal zone (60–100 m water depth). Sediment-accumulation rates in the region range from very high on the prodelta (300–500 mm yr²¹), then progressively decrease seaward (2–6 mm yr²¹ at 20-km offshore (Miralles and others, 2005). Particle distribution and sedimentation in this area are mostly controlled by hydrodynamics and wind. Organic preservation in the delta is enhanced by the high sediment-accumulation rates, but it is negatively impacted, particularly in the shallow substrates, by sediment resuspension during storms and flooding events (Gre´mare and others, 1997, 1998, 2003;

Medernach and others, 2001). Due to the weak tidal currents in the Gulf of Lions (i.e., ,0.3-m tidal range), there is little mixing (Sabatier et al., 2006) and the water column near the river mouth stratifies (Maillet and others, 2006). Fine-grained material precipitating from the surface plume increases the turbidity below (Naudin and Cauwet, 1997). Both the delta front and proximal part of the prodelta serve as temporary sinks for fine-grained sediments (and associated particle-reactive chemical components; Radakovitch and others, 1999), which are remobi- lized during stormy weather and transported westward (Chassefiere, 1990; Courp and Monaco, 1990; Roussiez and others, 2005). Oceanographic circulation is dominated by the cyclonic Liguro-Provencal Current (LPC), which flows along the continental margin from the coast of Provence to the Catalonian Sea (Millot, 1990). Northerly (Mistral), northwesterly (Tramontane), and southerly to southeasterly (Marine) winds predominate. The Mistral and Tramontane are more frequent in winter and spring and induce distinctive and opposite circulation cells on the shelf, leading to the intrusion of slope waters in the eastern and central parts of the shelf and the export of shelf water at its southwestern end (Estournel and others, 2003; Petrenko and others, 2005) (see satellite image on Fig. 1). The Gulf of Lions shows intense circulation along the continental slope, deep-water formation on and beyond the continental shelf, and seasonal stratification with intermittent mixing events associated with strong winds (Millot, 1990). Stratification of the surface layer generally persists from April to October. On the shelf, the seasonal thermocline is 10–20- m thick; in summer, surface-water ranges 20–25uC while bottom-water temperatures remain fairly constant at 13–

14uC. In winter, the water column becomes homogeneous throughout the region (Sempe´re´ and others, 2000). During our sampling in June 2005, bottom-water temperatures in the study area varied from 13uC at the deepest station (96 m) to 18uC at the shallowest station (20 m), whereas surface- water temperatures were 16–19uC. Surface salinity was 33 in front of the Rhoˆne River mouth and increased with

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distance from it to 38, while bottom-water salinity was uniform at ,38. During sampling, a steep gradient of decreasing organic carbon (OC) and total nitrogen (TN) existed from the river mouth (OC < 1.80% d.w. [dry weight]; TN < 0.21% d.w.) to the deepest and eastern stations (OC< 0.80%d.w.; TN<0.13%d.w.). The C/N atomic ratio andd¹³C_OCvalues reflect a change in quality of organic carbon, showing a clear tendency from a strong terrestrial signature close to the river mouth (C/N<10.00;

d¹³C_OC<227%) to a more marine signature seaward (C/N

< 6.00; d¹³C_OC < 223%) (Lansard and others, 2009;

Mojtahid and others, 2009). Oxygen penetration depths increase seaward from the Rhoˆne River mouth, where they are,1 mm at station 1 (20 m water depth) and 2–3 mm at stations 3–6 (40–63 m water depth); at the deepest stations (74–85 m water depth), they are 3–6 mm at stations 13, 14, 17, and 22 west of the delta and,8 mm at station 16 east of the delta (Lansard and others, 2009; Mojtahid and others, 2009).

MATERIAL AND METHODS

Twenty-three stations were sampled from 10–17 June 2005 in front of the Rhoˆne River during the Minercot 2 cruise aboard of the RVTethys II(Fig. 1). Sediments were collected between 20–98 m water depth using a Bowers and Connelly Mark VI multicorer. This corer contains four Plexiglas tubes, 50-cm long and with an inside diameter 15 cm. Sampling methods, core slicing strategy for foraminiferal analyses, and methodology of measurements for physico-chemical analyses (OC, TN, d¹³C_OC, oxygen) are described in detail in Mojtahid and others (2009). In this study, only the fraction.150mm is investigated (down to 5 cm depth).

For stations where oxygen measurements were not taken, we estimated oxygen penetration depth by using Surfer Software contour lines (published in Mojtahid and others, 2009). The Surfer contouring method is based on an inverse distance weighted model, where points nearby contribute more to the estimated value than points farther away.

To describe the foraminiferal vertical distribution (.150- mm fraction), the average living depth (ALD₅) of individual species and of the total fauna in the top 5 cm of sediment was calculated according to Jorissen and others (1995):

ALD5~ X

i~0, 5

(ni|Di)=N

where ‘‘5’’ is the lower boundary of the deepest sample interval i, n is the total number of specimens in interval i, D_i is the midpoint of sample interval i, and N is the total number of individuals for all levels. For all stations, ALD5

was calculated for the whole fauna, as well as for individual taxa.

For a more generalized description of the microhabitat tendency of each taxon in all stations, as well as in the grouped stations (see Appendix 1), we used a weighted ALD₅(Fontanier and others, 2003):

ALD5~Xⁿ

y~1,n

(ALD^y₅|ny) ,Xⁿ

y~1,n

ny

where n is total number of cores, ALD^y₅is the average living depth for the first 5 cm of the core y, and n_yis the number of specimens in the core y.

For each station, the Shannon index (H) of biodiversity (Buzas and Gibson, 1969) was calculated as:

H~{X^s

i~1

p_i ln p_i

in which S is the number of species, and p is the relative frequency of the ith species.

RESULTS

For all cores taken together, living foraminifera average (arithmetic mean percentage at all individual stations) 34%

in the top half-centimeter, 57%in the first centimeter, and 78% in the first two centimeters of the sediment.

Consequently, the weighted ALD₅ (average living depth) of the total fauna for all stations is ,1.3 cm, whereas oxygen penetration into the sediment averaged only 0.4 cm (Appendix 1). Maximum ALD5values are found at stations 1 and 16 (ALD₅<1.9). The shallowest microhabitat depth is observed at stations 19 and 24 (ALD5<0.6) (Appendix 1). We note that the difference between maximum and minimum ALD₅ values is not very conclusive. Also, this descriptor was originally proposed to describe the vertical distribution of foraminifera in deep-sea substrates. In the shallow-water environment in front of the Rhoˆne River mouth, the vertical distribution is compressed, primarily due to the shallow penetration of oxygen into the sediment.

For this reason and in consideration of the average living depth of infaunal foraminifera (Appendix 1), we use the depth of the maximum abundance of living foraminifera to describe vertical distributional patterns (Table 1).

For the 16 quantitatively most important species, the vertical variation in standing stocks is depicted in Figure 3.

Appendix 2 presents the raw data and Appendix 3 is the taxonomic reference list. Stations close to the river mouth are characterized by the shallowest oxygen penetration depths (averaging ,2.5 mm) and a weighted ALD₅ of 1.2 cm (Appendix 1). Assemblages at stations 1 and 3 are of low density and diversity, with the exception ofLeptohyalis scottii, which is present at station 3 with more than 700 individuals per 100 cm³. This species shows a clear preference for the surface layer. At station 4, four main species are present: Ammonia beccarii, Nonion scaphum, Nonionella turgida, andEggerella scabra. At this station,A.

beccariishows a predominantly superficial habitat, whereas N. scaphum, N. turgida, and E. scabra show maximal densities below the zero oxygen level. At station 5, A.

beccarii,N. scaphum, andN. turgidashow the same vertical distributional pattern as at station 4, whereas E. scabra prefers the uppermost layer. Cassidulina carinata and Bulimina aculeataare also present with surface maxima at this station.

Stations located southwest of the river mouth, in the main direction of the river plume, are characterized by intermediate oxygen-penetration depths (averaging ,3.5 mm) and by an average living depth for the total fauna of 1.4 cm (Appendix 1). At most of these stations,N.

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TABLE1. Summary of the depth in the sediment of maximum abundances for living foraminiferal species (main species in gray) at all stations. White circles indicate maximum density in the oxic layer, whereas black circles indicate maximum density in the anoxic layer. Half-white, half-black circles indicate maximum density in the oxic and anoxic layers. Weighted average living depth (ALD5) values are indicated for each species.

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FIGURE3. Vertical distribution of individual species occurring with more than 5%in at least one sample (x-coordinate: number of individuals standardized for 100 cm³sediment volume;y-coordinate: sediment depth in cm) and the weighted average living depth (ALD5) for each taxon at stations close to the river mouth, stations under the river plume, deep and eastern stations.a–kPredominantly superficial taxa.l–pPotentially/

predominantly infaunal taxa. The dashed lines represent the approximate oxygen penetration limit according to contours calculated by Surfer software on the basis of measurements performed at 10 stations. Note different scaling of axes.

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FIGURE3. Continued.

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FIGURE3. Continued.

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scaphum,Valvulineria bradyana,Rectuvigerina phlegeri, and N. turgidaare present in considerable amounts deep in the sediment. At some stations (2, 7, 13, 14, and 18), maximal abundances occur below the limit of oxygen penetration, especially for theN. scaphum andN. turgida(see Table 1).

On the contrary,C. carinataandB. aculeatagenerally show a clear superficial maximum where they are present (stations 8, 14, 18). E. scabra has a predominantly superficial distribution at stations 8 and 12, but occurs in significant densities in the anoxic part of the sediment at stations 2 and 7.

The deepest localities (stations 16, 17, 19, 20, 22, 23, and 24), which are least influenced by the river, are characterized by the deepest oxygen-penetration depth (,5 mm), and by a slightly deeper average living depth of the total fauna (ALD₅ < 1.2 cm) (Appendix 1). This biofacies is mainly composed ofC. carinata andB. aculeata, accompanied at some stations by the hyaline taxaA. beccarii,N. scaphum, N. turgida, V. bradyana, Q. seminula, and Melonis barleeanus, and by the agglutinated species E. scabra, Textularia agglutinans, andRecurvoides trochamminiformis.

In this distal area,C. carinata,B. aculeata,A. beccarii,Q.

seminula, E. scabra, T. agglutinans, and R. trochamminiformis all show an obvious preference for the uppermost oxygenated layer. Conversely, the other species (N.

scaphum, N. turgida, V. bradyana) show systematically infaunal maxima where they occur (stations 16, 17, 20, 22, and 24) (Table 1). In this zone, they appear to live deeper in the sediment compared to stations located under the river plume.

Eastern stations 9, 10, 11, and 15, which are less influenced by river outflow, are characterized by an intermediate oxygen-penetration depth (averaging ,4.0 mm) and by a fairly shallow average living depth (ALD₅

<1.0 cm) (Appendix 1). At these stations, similar to the deep distal stations,C. carinata,B. aculeata,Q. seminula,E.

scabra,T. agglutinans,R. trochamminiformis, andEratidus foliaceus exhibit a predominantly shallow microhabitat, with the exception of an infaunal maximum ofE. scabraat station 9. With the exception of station 9 close to river mouth, N. scaphum and V. bradyana have their infaunal maxima closer to the sediment surface and where they and N. turgida are at maximal density in the uppermost sediment (Table 1).

SUMMARY OFRESULTS

The comparison of the 16 profiles shows that there is no clear-cut distinction between exclusively infaunal and exclusively surficial taxa, and that the vertical distribution of the main foraminiferal species is very similar in the whole area. However, it is possible to distinguish two vertical distributional patterns:

1) Some taxa generally show a strong maximum in the top half-centimeter (Fig. 3a–e, Table 1), followed by a rapid decrease downward. The top half-centimeter usually corresponds to the oxygenated layer of the sediment.

2) Other taxa found in significant numbers in the top half- centimeter usually have maximum densities in the anoxic layer (Fig. 3m–p, Table 1).

In addition, several taxa show an intermediate vertical distribution (Fig. 3f–l). Q. seminula, A. glomeratum, E.

scabra, E. foliaceus, and T. agglutinansare generally very abundant in the top half-centimeter, but in some stations, they are in considerable densities deeper in the sediment.

The vertical distribution pattern of Melonis barleeanus is inconsistent among the five stations where it is.5%of each assemblage; nevertheless, its high density at station 20 (92 m water depth) includes a strong maximum 0.5–1 cm below the oxygenated interval. No taxa were observed to be exclusively infaunal, as all were in significant quantities in the topmost sediment.

On the basis of the vertical distributional patterns, we can group the 16 main species into two major categories:

1) Predominantly superficial taxa with a strong maximum in the oxygenated layer: e.g.,A. beccarii,B. aculeata,C.

carinata,E. macellum,Q. seminula,A. glomeratum,E.

scabra, E. foliaceus, L. scottii, R. trochamminiformis, andT. agglutinans; and

2) Potentially/predominantly infaunal taxa that generally have a strong maximum in deeper sediment levels, mostly below the oxygen-penetration depth: e.g., N.

scaphum,N. turgida,R. phlegeri,V. bradyana, andM.

barleeanus.

At stations near the river mouth, low densities of foraminifera do not allow us to distinguish a clear vertical distribution of the species. However, at stations influenced by the river plume, most species (especially potentially/

predominantly infaunal taxa) show maximal values in the oxic layer, whereas in the other zones, even more species show maximum abundances in the anoxic layer (Table 1, Fig. 3). N. scaphum, N. turgida, R. phlegeri, and V.

bradyana all show a slightly shallower microhabitat at stations under the river plume (respectively, ALD₅ <1.5, 1.7, 0.9, 0.9) than at deep distal stations (respectively, ALD₅

<1.6, 1.9, 1.6, 1.2).

Figure 4 presents the spatial distribution of cumulative percentages of previously determined ‘‘predominantly superficial’’ and ‘‘potentially/predominantly infaunal’’ taxa.

‘‘Potentially/predominantly infaunal’’ taxa strongly dominate the southwestern stations that are under the influence of the river plume. The ‘‘predominantly superficial’’ taxa dominate at the deeper and eastern stations, which are less influenced by river input, and also at station 3, which is in the immediate vicinity of the river mouth. However, the fauna at station 3 is very peculiar because of the very strong dominance of L. scottii, which occupies a predominantly superficial niche at this station.

DISCUSSION

Our data on the vertical distribution of benthic foraminiferal faunas show relatively limited geographical variability. At all sites, there is a strong maximum of foraminifera living close to the sediment surface, and densities drop rapidly in the first centimeters, reaching zero at 2–5 cm.

Also, when comparing the vertical distribution of individual species, the differences are rather limited. Almost all taxa show maximal densities at the surface, and the main difference is the rapidity of the downward density decrease.

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In more detail, our data on the vertical distribution of individual taxa in front of the Rhoˆne River mouth reveal two primary patterns. The first profile shows a very clear maximum in the topmost 0.5 cm, which usually corresponds to the oxygenated layer of the cores; however, abundant species in this continental shelf environment are always found in significant numbers at levels below. We refer to those species as ‘‘predominantly superficial’’ taxa. The second profile shows comparable densities in successive intervals with or without a clear maximum in the anoxic layer and characterizes ‘‘potentially/predominantly infaunal’’ taxa. These two patterns are generally distinct in the study area, but some species have intermediate patterns, and one species (E. scabra) shows inconsistent patterns.

Three major ecological biofacies can be distinguished with respect to the foraminiferal distribution in front of the Rhoˆne River mouth:

1) Biofacies I occupies the vicinity of the river mouth (see biofacies I, Fig. 7 in Mojtahid and others, 2009) where there is minimal oxygen penetration into the sediment (,2.5 mm) and a large input of predominantly terrestrial organic matter (OC < 2% and d¹³C_OC <

227%) (Mojtahid and others, 2009). All taxa (L.

scottii,N. turgida,N. scaphum,A. beccarii,Q. seminula, E. scabra, B. aculeata and C. carinata) present in Biofacies I occur in considerable densities within the sediment and apparently tolerate anoxia. Not surpris- ingly, they have all been referred to in the literature as stress-resistant taxa. For example, in a study of changes in foraminiferal assemblages influenced by the supply of human-derived nutrients to the northern Adriatic Sea, Barmawidjaja and others (1995) consid- eredN. turgidaas a stress-tolerant taxon and conclud- ed that its increase in abundance was due to increased nutrient load E. scabra is a shelfal species (e.g., Murray, 1991; Barmawidjaja and others, 1992) that lives in various microhabitats ranging from the oxygenated sediment surface to the deepest anoxic layers (e.g., Barmawidjaja and others, 1992; Jorissen and others, 1992; Ernst and others, 2002, 2005;

Duijnstee and others, 2003, 2004). Thus, it appears to tolerate strongly hypoxic conditions. For instance, E.

scabra is common in areas of the Adriatic Sea where seasonal degradation of abundant organic matter depletes oxygen content (Donnici and Serandrei- Barbero, 2002).E. scabraalso occurs in estuarine areas (e.g., Murray, 1991), in association with Elphidium excavatum, and in environments impacted by significant anthropogenic discharges (e.g., Debenay and others, 1996). Off the Rhoˆne River mouth, the

‘‘inflata’’ morphotype of A. beccarii is dominant (Mojtahid et al., 2009). Jorissen (1988) reported it in the Adriatic Sea at 20–50 m water depth in an area receiving abundant nutrients from the Po River. In the Ria de Arosa (Galicia, Spain; Van Voorthuysen, 1973), this morphotype lives on clayey bottoms enriched with nutrients as the result of coastal upwelling.

2) Biofacies II consists of stations under the influence of the river plume (see biofacies IV, Fig. 7 in Mojtahid and others, 2009). In this area, the substrate is characterized by an intermediate oxygen penetration depth (averaging ,3.5 mm) and still significant concentrations of organic matter (OC,1.4%), with a significant terrestrial signature (d¹³C_OC < 225.5%) (Mojtahid and others, 2009). The living assemblage is strongly dominated by three ‘‘potentially/predominantly infaunal’’ species (N. scaphum, R. phlegeri, and V.

bradyana). The ALD5of all stations located under the river plume averages 1.4 cm, which is deeper than at the most distal stations. In the literature, it has been suggested thatN. scaphum, an infaunally living taxon, may migrate to the sediment surface in response to increased organic matter input to the seafloor (Lange- zaal and others, 2004, 2006).N. scaphumhas also been described in the upwelling system off the Portugal continental margin (Levy and others, 1993).R. phlegeri prefers sediments close to the Tagus River plume in the western Iberian margin (Bartels-Jo´nsdo´ttir and others, 2006). In a previous study on the foraminiferal fauna of the western Mediterranean Sea, Bizon and Bizon (1984) found R. phlegeri at 40–100 water depth with strong abundance in the southwest. Jorissen (1987) reported a minimum water depth of 40 m for V.

FIGURE4. Geo-referenced contour maps of spatial distribution of the cumulative percentages of the ‘‘predominantly superficial’’ taxa and the ‘‘potentially/predominantly infaunal’’ taxa using a grid-based contour program, Surfer for Windows (Golden Software; version 6.02).

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bradyana in combination with stressed conditions in the Adriatic Sea. Morigi and others (2005) suggest that increased percentages of this species could eventually reflect a human impact on the marine environment, such as increased organic matter input associated with industrial development. In such cases, this taxon could move to superficial sediments and take over the niches of less resistant taxa (Morigi and others, 2005). In our samples, a similar tendency can be observed; V.

bradyana, which has its maximum in the uppermost layer of the sediment at the stations under the influence of the river plume, lives deeper in the sediment, in the anoxic layer, at the more distal stations (Table 1, Fig. 4).

3) Biofacies III is present at stations that are less influenced by river input (eastern and deepest stations) (see biofacies II [eastern stations] and biofacies III, Fig.

7 in Mojtahid et al., 2009). These stations are characterized by a slightly higher oxygen penetration (averaging ,5.0 mm) and relatively low amounts of organic carbon (OC < 0.8%), probably mostly of marine origin (d¹³C_OC<224%) (Mojtahid and others, 2009). This biofacies has the shallowest ALD₅ in the study area at 1.2 cm for the deepest stations and 1.0 cm for the eastern stations. This shallower living depth is due to the strong dominance of ‘‘predominantly superficial’’ taxa (i.e., C. carinata, B. aculeata, A.

glomeratum, R. trochamminiformis, E. foliaceus, T.

agglutinans) that prefer the uppermost oxygenated sediment layer.C. carinatais known to respond quickly to labile organic matter input by reproducing (Fonta- nier and others, 2003). B. aculeata is considered a shallow-infaunal species (e.g., Mackensen and others, 2000) and has been reported as an opportunist with high standing stocks in response to fresh organic- matter inputs (De Rijk and others, 2000).

SUMMARY OFDISCUSSION

Stations under the influence of the Rhoˆne River input are rich in ‘‘potentially/predominantly infaunal’’ taxa. The dominance of infaunal taxa is a common phenomenon in high-productivity or low-oxygen settings (Sen Gupta and Machain-Castillo, 1993). A strong dominance of ‘‘potentially/predominantly infaunal’’ species in those stations influenced by river runoff suggests that they are more competitive than ‘‘predominantly superficial’’ taxa. Because the oxygen concentration at the sediment-water interface is relatively elevated (210–260 mmol/L) at all stations, this infaunal dominance cannot be explained by the disappearance of more surficial taxa due to low oxygen. The observation of all ‘‘predominantly superficial’’ taxa ap- pearing systematically in deeper anoxic sediment layers strongly suggests that other factors are involved in their preference for the uppermost sediment surface. We suggest that the segregation between superficial and ‘‘potentially/

predominantly infaunal’’ taxa reflects the latter’s greater tolerance of degraded food. At stations influenced by the river, low-quality terrestrial organic carbon prevails, whereas labile marine organic matter is relatively rare. As a consequence, infaunal taxa, which have a higher tolerance

for this low-quality food, strongly dominate the assemblage. Stress factors other than low-oxygen concentrations and large fluvial influx of low-quality organic matter also occur in the area, especially in the vicinity of the river mouth (e.g., turbidity, high sedimentation rate, waves), and these too can affect the spatial and vertical distributional patterns of benthic foraminifera. Predominantly superficial taxa occur at stations less influenced by the river, possibly in response to the higher-quality labile organic matter of marine origin. However, slow bacterial degradation of already low-quality organic carbon deeper in the sediment provides a continuous supply of food to the infaunal taxa that live deeper in the sediment. At most of these distal stations, maximal densities occur in the top 0.5 cm of sediment.

In order to elucidate the factors controlling the vertical distributional patterns, Figure 5 plots the cumulative percentages of ‘‘potentially/predominantly infaunal’’ taxa against oxygen penetration into the sediment, quantity of organic carbon (OC), the C/N ratio, andd¹³C_OC, the latter two of which reflect the quality of the organic matter.

Excluded is station 1, which is inhabited by only few individuals, and station 3, which has a peculiar fauna largely dominated by L. scottii. This graph reveals a significant positive correlation of ‘‘potentially/predominantly infaunal’’ taxa with increasing C/N and decreasing d¹³COC (R 5 0.69 and 0.59, respectively; p 5 ,0.01), indicating a greater importance of terrestrial organic carbon. Because the sum of the percentages of both microhabitat categories is almost 100% (we did not integrate the minor species with percentages less than 5%), there is a negative significant correlation of the cumulative percentages of the ‘‘predominantly superficial’’

taxa with increasing C/N and decreasingd¹³COC.

These faunas have weaker correlations with total organic carbon (R 5 0.35) and oxygen penetration into the sediment (R 5 0.49). This supports the notion that the quality of the organic matter is the major factor controlling the vertical distribution of the living foraminifera in front of the Rhoˆne River mouth, and that the amount of organic matter and oxygen have less impact on the foraminiferal faunas.

CONCLUSIONS

In sediments off the Rhoˆne River mouth, most foraminifera live in the topmost centimeter of its muddy substrate.

Two vertical distributional patterns are evident and they distinguish ‘‘predominantly superficial taxa’’ that charac- terize the oxygenated uppermost sediment from ‘‘potentially/predominantly infaunal’’ taxa that thrive deeper in the sediment.

In the area strongly influenced by Rhoˆne River outflow, the foraminiferal assemblages are dominated by ‘‘potentially/predominantly infaunal’’ taxa, which seem to profit from the fluvial inflow of relatively low-quality organic matter. These species tolerate the anoxic conditions deeper in the sediment.

Areas less influenced by river outflow are characterized by the dominance of ‘‘predominantly superficial’’ species, which apparently prefer the more labile organic matter of

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marine origin. These species live essentially in the oxygenated top layer of the sediment.

Our study is further evidence of the vertical heterogeneity of infaunal foraminiferal microhabitats within the same basic environment. More importantly, the correlation between the proportion of the two faunal groups and the environmental factors suggests that the quality of organic matter, not the quantity of organic matter nor the oxygen penetration depth, is the prime controlling factor in the

vertical distribution of Foraminifera in front of the Rhoˆne River mouth. We suspect that our conclusions apply to similar environments elsewhere, but further investigations are needed for confirmation.

ACKNOWLEDGMENTS

The authors acknowledge cruise ship members of the RV Tethys IIfor their excellent work and assistance during the MINERCOT 2 cruise, as well as Melissa Gaultier from BIAF, Angers, who helped a lot with laboratory sample treatments and analyses. We are grateful to Bruno Bombled and to Thibault Geoffroy from the LSCE for their technical support, the CNR (Compagnie Nationale du Rhoˆne) for access to their facilities in Port-Saint-Louis du Rhoˆne, and Caroline Gauthier and Christine Hatte´ for stable carbon isotope analyses. We acknowledge Christophe Rabouille from LSCE for the supervision and organization of the cruise. We are thankful to Dr. Y. Milker, Dr. G. Schmiedl, and a third anonymous reviewer, as well as Associate Editor Dr. B. W Hayward and Editor Dr. K. Finger, who invested much time in the correction of the first manuscript, leading to a strongly improved final version.

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