Living deep-sea benthic foraminifera from the warm and oxygen-depleted environment of the Sulu Sea

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Deep-Sea Research II 54 (2007) 145–176 www.elsevier.com/locate/dsr2

Living deep-sea benthic foraminifera from the warm and oxygen-depleted environment of the Sulu Sea Renata Szareka,c,, Hidetaka Nomakib, Hiroshi Kitazatoa a

Institute for Research on Earth Evolution (IFREE), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-Cho, Yokosuka-shi 237 0061, Japan b Ocean Research Institute, The University of Tokyo, 1-15-1 Minamidai, Nakano-ku, Tokyo 164 8639, Japan c Collegium Polonicum/University of Poznan, Kosciuszki 1, 69-100 Slubice, Poland Received 28 April 2005; received in revised form 27 February 2006; accepted 27 February 2006 Available online 26 January 2007

Abstract The semi-enclosed, oligotrophic Sulu Sea is characterised by warm (ca. 10 1C) and oxygen-depleted (o1.25 ml/l O2) waters in the meso- and bathypelagic zones of the basin. The main objectives of this study were to examine the present-day distribution patterns of deep-sea benthic foraminiferal assemblages in relation to unique environmental conditions in the bottom waters of the Sulu Sea. Multiple-core sediments were obtained at seven sites in the Sulu Sea during the R.V. Hakuho Maru KH-02-4 cruise at water depths between 534 and 4635 m. The investigation is based on the analysis of Rose Bengal-stained benthic foraminifera (432 mm) from 56 samples (from surface down to 5 cm). The stained foraminiferal assemblages of the Sulu Sea comprised 285 species, including 137 agglutinated and 148 calcareous species. Standing stock values ranged from 595 individuals/10 cm2 on the continental slope to 100 individuals/ 10 cm2 in the abyssal zone. Generally, in the low-productivity and low-oxygen environment of the Sulu Sea, stained assemblages are characterized by low-standing stock values, moderate dominance and low diversity. The combination of poor rates of C org flux and low dissolved oxygen content in bottom waters are the main factors controlling the deep-sea benthic fauna in the Sulu Sea. The foraminiferal abundances in the upper bathyal zone respond to both food fluxes and oxygen concentrations. Most of the epifaunal, oxyphilic species have their lower limit of occurrence at a water depth of approximately 2000 m (dissolved oxygen o1.25 ml/l) in the Sulu Sea. At constantly dysoxic (o1 ml/l O2) sites from the lower bathyal and abyssal zone, the assemblages comprised low-oxygen tolerant species and are more dependant on C org fluxes. The correlations between benthic foraminiferal faunas and C org flux and dissolved oxygen values are very good, with correlation coefficients of r2 ¼ 0:956 and 0.88, respectively. The living deep-sea foraminiferal assemblages consisted mainly of agglutinated tests, with dominant species such as Lagenammina difflugiformis, Ammoscalaria tenuimargo, various Reophax species, and small (o70 mm) trochamminaceans like Portatrochammina wiesneri. Stained individuals of the calcareous Parrelloides bradyi (type 2) occurred in low numbers at oxygen-poor sites, down to a depth of 5 cm in the sediment column. The only stained, calcareous, infaunal species found deeper than 4000 m was Valvulineria mexicana (average living depth of 3 cm). The general microhabitat preferences of

Corresponding author. Institute for Research on Earth Evolution (IFREE), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-Cho, Yokosuka-shi 237 0061, Japan. Tel.: +81 8060911264. E-mail addresses: [email protected], [email protected] (R. Szarek).

0967-0645/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2006.02.017

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common species were consistent with those from other studies, although due to the unique combination of poor food supply and dysoxic conditions, most of the infaunal species had shallower average living depths than those reported from other dysoxic locations. r 2006 Elsevier Ltd. All rights reserved. Keywords: Living deep-sea benthic foraminifera; Oxygen depletion; Vertical distribution patterns; Sulu Sea

1. Introduction Investigations of modern and ancient oxygendepleted environments are of interest in oceanography, since they represent major disturbances in the ocean system. The environmental settings of the Sulu Sea, a semi-enclosed, meso-to-oligotrophic basin in the western equatorial Pacific, characterized by warm (ca. 10 1C) and oxygen-depleted (o1.25 ml/l O2) deep-waters, are unique, because they bear a resemblance to conditions from the midCretaceous ocean. The analysis of living benthic foraminiferal assemblages distributed along a bathymetric transect of the Sulu Sea from the upper bathyal zone (534 m) to the abyssal plain (4635 m) offers an opportunity to evaluate the modern foraminiferal response to low annual organic carbon (C org) fluxes combined with low oxygen levels. The population dynamics of deep-sea benthic foraminifera in typical deep-sea environments are mainly controlled by two inversely related parameters, the organic matter flux to the seafloor and concentrations of oxygen in the sediment porewater (Jorissen, 1999; Van der Zwaan et al., 1999; Gooday and Rathburn, 1999; de Rijk et al., 2000; Kitazato et al., 2000; Geslin et al., 2004). In deep-sea environments, oxygen usually appears to be a less limiting factor for the benthic communities than the amount of C org (Jorissen et al., 1995; Ernst and Van der Zwaan, 2004). A summary of previous publications describing ‘‘living’’ deep-sea benthic faunas was recently presented by Hayward et al. (2002), Gooday (2003), and Ernst and Van der Zwaan (2004). Previous studies of modern, dead benthic foraminiferal assemblages from the Sulu Sea include investigations by Exon et al. (1981), Linsley et al. (1985), and Miao and Thunell (1993, 1996). Even though the deep-sea communities consist mainly of agglutinated and often small (50–120 mm) species, to date studies on living deepsea benthic foraminifera (4150 mm) have concentrated on the calcareous assemblages (e.g. Rathburn and Corliss, 1994; Rathburn and Miao, 1995;

Rathburn et al., 1996). This investigation focuses on the living, Rose Bengal stained, benthic foraminiferal assemblages (432 mm) from surface sediments and down to 5 cm in the sediment column. The aim of this study was to examine the presentday distribution patterns and community structure of living deep-sea foraminifera in the Sulu Sea in relation to the physical and chemical characteristics of its bottom water, which are both unique and relatively stable. 2. Study area The study area is located in the Sulu Sea basin. It extends from 8105.740 N, 118121.650 E to 7125.000 N, 121112.630 E (Fig. 1) with water depths ranging from 534 to 4635 m. The Sulu Sea is a semi-enclosed, marginal basin (348 000 km2) located between the South China Sea and the Western Equatorial Pacific, with a maximum depth of 5580 m (Wang, 1999). It extends northeastward from Borneo to the Philippines and the Sulu Archipelago. The Mindoro Strait in the northwestern Sulu Sea is the deepest (420 m) passage, which connects it to the South China Sea. Shallower passages connect the Sulu Sea to the Celebes Sea (e.g. Sibutu Strait, ca. 250 m) and through the Philippine archipelago (110 and 65 m) to the West Equatorial Pacific (Rosenthal et al., 2003). The modern climate of the Sulu Sea is strongly influenced by the East Asian monsoon, seasonal migrations of the intertropical convergence zone, and by the El Nin˜o southern oscillation (Beaufort et al., 2003; Oppo et al., 2003). Surface waters flow from the South China Sea into the Sulu Sea during the late summer monsoon and flow out during the late winter monsoon. The seasonal variations in the sea-surface salinity, ranging from 32.7 to 34.2 psu, are driven by factors such as the net precipitation, riverine discharge and surface water circulation (Wyrtki, 1961; Rosenthal et al., 2003; Oppo et al., 2003). The annual sea surface temperature (SST) in the Sulu Sea, seasonally varying by less than 2 1C, is

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11° Philippines

Hakuho Maru KH-02-4 Cruise 7th Nov. - 18th Dec. 2002 10°

500

an

Sulu Sea

2000

SU-8

1000 2000

SU-6 (2055 m)

500

8°

SU-4 (534 m)

(3774 m)

3000

4000

SU-5 (1053 m)

5000

100

SU-2 (4074 m)

7°

SU-3

ao

1000

SU-1 (4635 m)

an

9°

aw

nd

l Pa

Mi

South China Sea

3000

(3059 m)

2000

6° Celebes Sea Borneo 5N° 117E°

118°

119°

120°

121°

122°

123°

Fig. 1. Location of the study area and position of sites in the Sulu Sea basin.

generally higher than 29 1C (Yan et al., 1992). The central part of the Sulu Sea basin is regarded as an oligotrophic area, although higher concentrations of chlorophyll a and weak upwelling near a depth of 200 m have been observed near the Sulu Archipelago between the Sulu and Celebes seas. These enriched waters occasionally extend to the Sulu basin (Nishida and Gamo, 2002). The present annual primary production in the Sulu Sea varies from 60 to 100 g C/m2-yr (Berger, 1989). While the seasonally reversing monsoonal regime controls the sea-surface circulation and productivity patterns in the Sulu Sea down to ca. 250 m, the deep circulation is forced by an inflow of intermediate water from the South China Sea in late summer through the Mindoro Strait, which is the only source of deep water introduced into the Sulu Sea basin (Wyrtki, 1961; Nozaki et al., 1999; Chen et al., 2004). The mixed intermediate waters in the Sulu Sea range from depths of ca. 250–1000 m. The homogeneous deep waters extend from 1000 m to the bottom of the Sulu basin, with uniform salinities of approximately 34.5 psu (Miao and Thunell, 1993). Restricted exchange between the Sulu Sea

and other basins together with the tropical climate contribute to the warm (9.8–10 1C), oxygen-deficient (o1.25 ml/l) nature of the Sulu Sea deep waters and higher CaCO3 contents in its sediments (Kuehl et al., 1993). The carbonate compensation depth occurs between 4500 and 4800 m (Exon et al., 1981; Linsley et al., 1985). The Sulu Sea deep waters are under persistent oxygen depletion, but anoxic conditions do not exist at the sediment surface, as indicated by the lack of molybdenum enrichment in the sediments (Calvert et al., 1993). The sediments on the slopes of the Sulu Sea are mainly foraminiferal silts and clays, with 50–70% CaCO3 (Calvert et al., 1993). The Sulu Sea sedimentation rates are ca. 8–22 cm/kyr on the upper slope and rise, while on the abyssal plain (4200–5000 m) due to turbidites the rates reach 100 cm/kyr (Exon et al., 1981; Miao and Thunell, 1993). These turbidites consist mainly of benthic microorganism shells and volcanic and sedimentary rock fragments derived from the eastern shelves. The floor of the basin is underlain by up to 4000 m of Pleistocene and Quaternary sediments (Exon et al., 1981).

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(A)

SU-4 SU-5 SU-6 SU-3 SU-8 SU-2 SU-1 534 m 1053 m 2055 m 3059 m 3774 m 4074 m 4635 m WD (m)

0

(B)

DO (ml/l)

abyssal

4000

dissolved oxygen

temperature

10 10 5 0

(D) standing stock

ind./ SU-4 10 cm2 600

SU-5

SU-6

SU-3

SU-8

SU-2

SU-1 calc. org. agg.

400

200

fragm./ 10cm2 60 40 20 0

tubes

(E)

(F)

150

calc. tubes org. agg .

100 50 0

(G)

(H)

SU-4

SU-5

SU-6

SU-3

SU-8

SU-2

SU-1

SU-4

SU-5

SU-6

SU-3

SU-8

SU-2

SU-1

80 40 0 4.5 3.5 2.5

(I) E

1 0.5 0

(J)

ALD5

Fig. 2. Information on benthic foraminiferal assemblages along the depth transect: (A) water depth (WD) profile; (B) temperature (T, 1C, near-bottom temperatures) and dissolved oxygen (DO, ml/ l); (C) organic carbon (C org) flux (g/m2yr); (D) standing stock (individuals/10 cm2); (E) number of species (diversity indices); (F) Fisher’s a-index; (G) Shannon–Wiener index—[H(S)]; (H) evenness (E); and (I) average living depth (ALD5). Legend: agg.— agglutinated foraminifera, org.—organic-walled test, tubes—tubular forms (see species listed in Table A2), calc.—calcareous test.

lower bathyal

continental slope

10.5

C org-flux (g/m2yr)

(C)

2000

T (°C) 11

2.5 2 1.5 1 0.5

no. of species

The Sulu Sea samples were collected during R.V Hakuho Maru cruise KH-02-4 (Nishida and Gamo, 2002) from 7 November to 18 December 2002. Seven sites from the continental slope and abyssal plain, at water depths ranging from 534 to 4635 m (Fig. 2A and Table 1), were sampled with a multiple corer equipped with eight core tubes with internal diameters of 8.2 cm (surface area 52.8 cm2). The sediment was examined and sampled immediately after the coring device was placed on deck and kept in a cold-room. The maximum delay between core sampling and processing was about 3 h. Cores for meiofaunal vertical distribution analysis were sliced into 0.5 cm layers from the top to a sediment column depth of 3 cm, and subsequent downcore samples were sliced at 1-cm intervals. All samples, following Shimanaga et al. (2007) processing protocol, were fixed in a 5% solution of formaldehyde in seawater, neutralized with hexamethylenetetramine (C6H12N4) and 0.05 g/l Rose Bengal solution, and kept cool until onshore treatment. The seawater samples for the analyses of salinity and dissolved oxygen (DO) were collected with the CTD-water sampling system during KH-02-4 (Fig. 2B and C). The measurements were carried out onboard or shortly after the cruise in shore-based laboratories (Nishida and Gamo, 2002). In the laboratory, the samples were split into halves using a Folsom plankton splitter. The samples have two volumes of 13.2 cc for samples from surface down to 3 cm and 26.4 cc for samples below 3 cm. Next, one of these splits was rinsed over a sieve with 32-mm mesh, the remaining residue was oven-dried (50 1C) and sorted completely. The investigation was based on the analysis of Rose Bengal-stained (living) benthic foraminifera from 56 samples. The use of the 432-mm fraction ensured that almost all foraminifera have been retained. Because the two uppermost samples yielded a small amount of residue after sieving, the

432-mm residues were not sieved further into the commonly used size fractions, but checked throughout. All specimens of vividly pink benthic foraminifera,

Fisher'sAlpha

3. Materials and methods

H(S)

148

0 0.5 1 1.5 2 2.5 3 3.5

ADL5 agg. org. tubes calc.

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Table 1 List of the sampling stations with: location, water depth, sediment type, depth of CTD profile, near-bottom temperature, salinity and dissolved oxygen values, annual primary production rate and C org-flux to the seafloor (after Suess, 1980) Sample

SU-4

SU-5

SU-6

SU-3

SU-8

SU-2

SU-1

Station no./core no. Latitude (N) Longitude (E) Water depth (m) Sediment type CTD (m) Temperature (1C) Salinity (psu) Dissolved oxygen (mmol/l) Dissolved oxygen (ml/l) Primary productivity (g/m2 yr) C org-flux (g/m2 yr)

7/MC-8 8105.740 118121.650 534 Calc. ooze 524 10.90 34.47 91.99 2.06 126 9.75

8B/MC-4 8107.640 118135.170 1053 Calc. ooze 1040 10.12 34.45 77.71 1.74 124 4.91

9/MC-2 8123.250 119102.990 2055 Calc. ooze 2031 10.15 34.46 54.93 1.23 123 2.50

6/MC-1 6154.470 119110.300 3059 Calc. ooze 2975 10.30 34.47 45.55 1.02 124 1.70

11/MC-4 8149.990 121105.720 3774 Calc. ooze 3668 10.41 34.48 45.11 1.01 117 1.30

5/MC-3 7133.800 120119.470 4074 Silty clay 4075 10.46 34.48 44.21 0.99 104 1.07

4/MC-6 7125.000 121112.630 4635 Silty clay 4476 10.56 34.48 43.32 0.97 102 0.92

containing stained protoplasm in at least one chamber were picked out under a stereo microscope with a moist brush down to 5 cm of core depth. Opaque calcareous or agglutinated tests were broken with a dissection needle if difficulties in recognizing stained protoplasm occurred. Fragments of Astrorhizidae (mainly Rhizammina indivisa, Rhizammina algaeformis, and Saccorhiza ramosa) were common in the samples of most multicores. These tubular foraminifera were fragmented during processing of the samples. Since counting small fragments of tubular-forms as individual specimens would overestimate their relative abundance, different methods have been used for the quantification of tubular species. Several authors have counted three size standardized fragments of tubular forms to gain a semiquantitative estimation of fragmented species (e.g. Kurbjeweit et al., 2000; Heinz and Hemleben, 2003). In this study fragments longer than 1000 mm and those with a proloculus irrespective of length were counted as single specimens (Hess, 1998), while the smaller fragments were combined to the cumulative length of approximately 1000 mm. Although arbitrary, this method enables us to obtain a very rough estimate of tubular specimens. Thus, we treated tubular forms separately from the other foraminiferal groups and excluded them from correspondence analysis (these species are listed on the end of Table A2). Further in text an expression ‘agglutinated foraminifera’ refers exclusively to non-tubular forms. An alphabetical list of identified species with references is presented in Table A1. For the generic

assignments, the concepts of Loeblich and Tappan (1987, 1994) were mainly used. For some genera of the family Lagenidae, the definitions of Jones (1984) were used. For genera of the family Trochamminidae, the terminology of Bro¨nnimann and Whittaker (1988) was followed. The four taxa not determined at the species level are left in open nomenclature (e.g. Reophax sp. 1). The abbreviation ‘‘spp.’’ is used for incomplete specimens (broken during sample processing) of particular genera grouped together. The micropaleontological slides with mounted specimens, as well as scanning electron microscopic specimen mounts and images, are housed for reference in the Institute for Research on Earth Evolution, Japan Agency for Marine– Earth Science and Technology. We standardized living foraminifera counts to a surface of 10 cm2 for standing stock analysis (down to 5 cm). For comparisons of vertical distribution patterns, volume of 10 cc was used (number of specimens in 10 cc of sediment). Counts are documented in Table A2 (species represented by single specimen were lumped together). We used Fisher’s a-index (Fisher et al., 1943) and the Shannon–Wiener index H(S) (Buzas and Gibson, 1969) as a measure of species diversity and the evenness index E (Buzas and Gibson, 1969) to measure equitability/dominance. Those diversity statistics were calculated using the free software Past (Hammer et al., 2001). To describe the vertical distribution of the individual species or total fauna microhabitat patterns, we used the average living depth (ALDx) following the formula of Jorissen et al. (1995). ALDs were calculated only

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when the abundance of particular species total up to at least five or more specimens at least in one core. Canonical correspondence analysis (CCA) was used to analyse the foraminiferal data sets (CANOCO 4.5 software of ter Braak and Smilauer, 2002) and relate them to available environmental data. CCA is designed to extract synthetic environmental gradients from ecological datasets, which are the basis for describing and visualizing the habitat preferences of species via an ordination diagram. A CCA ordination diagram consists of points representing species/sites and classes of qualitative environmental variables and arrows for quantitative environmental variables. The arrows point in the direction of maximum change in the value of the associated variable, and arrow length reflects the strength of the correlation (ter Braak and Verdonschot, 1995). The matrix used for CCA includes 172 species from seven sites located at water depths between 534 and 4635 m and values for five environmental parameters. The values of supplementary environmental data used as passive parameters for CCA are listed in Table 1. The annual primary production (PP) rates are estimated based on PP distribution maps (for 1997/1998) downloaded from /http:// marine.rutgers.edu/opp/S. The annual C org flux is calculated from the most commonly applied equation of Suess (1980)—C flux z ¼ C prod/(0.0238 z+0.212), where flux to depth (C flux z) is described as a function of the primary production of organic carbon in surface waters (C prod), scaled to depth below the sea surface (z). The water depth, temperature and DO were based on the KH-02-4 cruise report (Nishida and Gamo, 2002). There is no consensus on the terminology for bottom-water oxygen concentrations (see Tyson and Pearson, 1991). In this paper, we use the oxygen range limits as defined by Bernhard and Sen Gupta (1999), where oxic is 41.0 ml/l of O2 and dysoxic is 1.0–0.1 ml/l. 4. Results 4.1. Standing stock and distribution patterns In the study area, the highest benthic foraminiferal standing stock values occurred off Palawan on the continental slope. At water depth of 534 m, stained specimens reached 595 individuals/10 cm2 (down to 5 cm, 432 mm), while at a neighbouring deeper site (1053 m), standing stock decreased to

398 individuas/10 cm2 (Table 2 and Fig. 2D). In the sediments from water depths below 2000 m, stained foraminiferal densities varied between 167 off Borneo (SU-3 3059 m) and 100 at the deepest sampled site (SU-1 4635 m) close to Mindanao Island. Calcareous forms were more numerous than agglutinated at the shallowest site (534 m). Agglutinated foraminifera-dominated assemblages at all other studied sites, comprising more than 50% on the lower continental slope and more than 90% in the abyssal zone. The stained Astrorhizida alone, socalled tubular forms (e.g. Hyperammina, Rhabdammina or Rhizammina) were common at all sites (Fig. 2E). The highest number of their fragments was found at upper continental slope. The organic-walled foraminifera including some Allogromiida (e.g. Nodellum membranaceum, Resigella moniliformis) and Trochamminacea (e.g. Rotaliammina chitinosa, Remaneica helgolandica) generally composed less than 3.7% of living fauna in the Sulu Sea environment. Although not numerous, they occurred at all depths in the two uppermost centimetres of sediments. Calcareous fauna from 2 shallower sites were dominated by species belonging to Rotaliida (e.g. Nuttallides bradyi, Seabrookia pellucida, Bolivina spp.). They comprised up to 47% of species at a water depth of 534 m, but decreased rapidly with increasing depth. At 4635 m, only one species, Valvulineria mexicana, occurred below the sediment surface at 2.5–5 cm in the sediment column. 4.2. Species richness and diversity The Sulu Sea stained foraminiferal assemblages yielded 285 species, including 137 agglutinated and 148 calcareous species (Table 2). Only 7 species occurred in all assemblages studied despite the varying environmental conditions and were agglutinated species: Cribrostomoides subglobosus, Lagenammina difflugiformis, Reophax scorpiurus, Saccammina sphaerica, and three tubular-form species Rhizammina algaeformis, Rhizammina indivisa and Saccorhiza ramosa. Two other agglutinated species, Ammobaculites paradoxus and Ammoscalaria tenuimargo, occurred at all sites except the shallowest one (534 m). Only two calcareous species, Oridorsalis umbonatus and Parrelloides bradyi type 1, occurred in low abundance at all stations, but not at the deepest one (4635 m). More than 56% (160) of species occurred at a single location, usually in low abundance.

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Table 2 Information on stained benthic foraminiferal assemblages (432 mm) from the Sulu Sea down to 5 cm in the sediment column, with: water depth (m); standing stock (no. of individuals [indiv.]/10 cm2); agglutinated (A) to calcareous (C) A/C ratio (no. of individ./10 cm2, without tubular forms); number of species (S); diversity indices: Fisher’s a-index (Alpha), Shannon–Wiener index [H(S)], evenness (E); average living depth (ALD5) of 72 species (see Table 3) This study (for November/December 2002) Station no. SU-4 Water depth (m) 534

SU-5 1053

SU-6 2055

SU-3 3059

SU-8 3774

SU-2 4074

SU-1 4635

Standing stock Total individ./10 cm2 Agglutinated Organic-walled Calcareous

595.2 262.4 22.1 310.7

398.0 202.6 3.8 191.6

106.8 70.8 1.5 34.5

167.0 123.4 3.8 39.8

151.5 129.5 3.0 18.9

164.4 146.2 6.1 12.1

100.3 88.6 3.0 8.7

Tubular forms

66.0

52.3

40.1

48.5

34.5

42.4

26.5

A/C ratio

0.92

1.08

2.10

3.20

7.00

12.56

10.52

No. of species All species Agglutinated Organic-walled Tubular forms Calcareous

166 56 3 6 101

142 56 4 6 76

58 35 2 7 14

62 33 3 9 17

53 35 1 9 8

51 33 3 7 8

37 26 3 5 3

Diversity Indices (without tubular forms) Fisher’s a 70.78 H(S) 4.448 0.541 Evenness EH/S

70.53 4.124 0.462

32.59 3.154 0.478

24.19 3.189 0.476

19.19 3.24 0.608

18.7 3.222 0.597

14.94 2.843 0.554

ADL5 of 72 frequent sp. Agglutinated (33) Organic-walled (2) Tubular forms (7) Calcareous (30)

0.56 0.63 1.25 0.54 0.50

0.73 0.69

0.79 0.71

0.55 0.53

1.39 1.39

0.49 1.10

0.51 1.48

0.35 1.18

1.07 2.38

1.02 0.90 0.25 0.62 3.05

Data from Rathburn and Corliss, 1994 (for August 1988) 12 8 Station no. 510 1005 Water depth (m)

9 1995

20 3000

15 3995

18 4515

Total individ./50 cm2a Calc. individ./50 cm2b No. of calc. species

1576 415 39

1494 154 32

154 24 10

309 119 14

0.62 0.64 1.10 0.79 0.47

3721 1674 112

2982 1063 73

0 0

Data copied from Rathburn and Corliss, 1994. a Sum of agglutinated and calcareous foraminifera. b Sum of 63–150 mm and 4150 mm fractions.

The species richness decreased with increasing water depth, mainly due to the gradual disappearance of calcareous species (Fig. 2F). On the continental slope, the calcareous assemblage comprised 100 species, or 60% of the total number of species, while at water depths below 2000 m, calcareous species constituted less than 25%. In the abyssal zone at water depths 44000 m, single specimens of nine calcareous species were found living: Anomalinoides globulosus, Cibicides refulgens, Fontbotia wuellerstorfi, Oridorsalis umbonatus, Par-

afissurina subventricosa, Parrelloides bradyi type 1, Parrelloides bradyi type 2, Pullenia quinqueloba and Valvulineria mexicana. In addition, the species richness of agglutinated assemblages (including tubular-forms) also significantly decreased with increasing water depth, from 66 species on the continental slope to 34 in the abyssal zone. The total number of living species on the continental slope (534 m) was 166 species per sample, while in the deep-sea basin (4635 m) there were only 37 species. Generally, at water depths

ARTICLE IN PRESS R. Szarek et al. / Deep-Sea Research II 54 (2007) 145–176 Benthic foraminiferal abundances

SU-4 (534 m) SU-1 (4635 m)

SU-2 (4074 m)

SU-8 (3774 m)

SU-3 (3059 m)

4.3. Vertical distribution patterns The faunal densities and number of species per sediment interval down to 5 cm are shown in Fig. 3. The maximum abundance of living benthic foraminifera in all cores studied occurred at the surface (0–1 cm). On average, more than 80% of total living fauna occurred in the uppermost centimetre of sediment column, but not at the two abyssal sites SU-1 and SU-2, where, despite the low standing stock, 71% and 66% of stained individuals, respectively, occurred. In addition, three cores (SU-1, SU-2 and SU-6) differed from the others by having the highest densities not in the uppermost half centimetre, but at the 0.5–1-cm interval. Calcareous foraminifera such as Trifarina angulosa, Nuttallides bradyi, Seabrookia pellucida, Siphonina tubulosa, and Cibicidoides pachyderma occurred in greater abundance down to 2 cm at two sites, SU4 and SU-5, on the continental slope (Fig. 4). Scarcely any stained calcareous foraminifera were found deeper in the sediment, except for single specimens of Chilostomella ovoidea and Globobulimina pacifica. Between water depths of 2000 and 4000 m, within the uppermost 2 cm of the sediment column, species such as Parrelloides bradyi type 1, Oridorsalis umbonatus, Rotaliatinopsis semiinvoluta, and Cassidelina spp. occurred, while down to 5 cm mainly representatives of Parrelloides bradyi type 2 were present. An opposite pattern was observed at site SU-1 (4635 m), where not a single stained

Number of species

sediment No. of ind./10 cc interval

SU-5 (1053 m)

greater than 2000 m, the number of living species encountered at a single location varied between 62 and 37 species. Diversity values of Fisher’s a-index, Shannon–Wiener H(S) and evenness E for each studied site are plotted along the transect (Table 2 and Fig. 2G–I). On the continental slope in the Sulu Sea, the values of Fisher’s a-index for the ‘‘living’’ assemblages (a ¼ 70:8 and 70.5) are at least 2-fold higher than in the deep sea, where it varies from 32.6 to 14.9. Shannon–Wiener H(S) index values shown a similar pattern, decreasing rapidly from 44 in water depths shallower than 2000 m to values between 2.8 and 3.2. At site SU-8 located in the central part of the Sulu Sea basin, the H(S) value (3.24) was slightly higher than at the other sites. The evenness value was also the highest (0.6) at that site. The strongest dominance (0.46) was recognized at site SU-5, located off Palawan at a water depth of 1053 m, where the standing stock value was relatively high (398 individuals/10 cm2).

SU-6 (2055 m)

152

cm 0-0.5 0.5-1 1-1.5 1.5-2 2-2.5 2.5-3 3-4 4-5 cm 0-0.5 0.5-1 1-1.5 1.5-2 2-2.5 2.5-3 3-4 4-5 cm 0-0.5 0.5-1 1-1.5 1.5-2 2-2.5 2.5-3 3-4 4-5 cm 0-0.5 0.5-1 1-1.5 1.5-2 2-2.5 2.5-3 3-4 4-5 cm 0-0.5 0.5-1 1-1.5 1.5-2 2-2.5 2.5-3 3-4 4-5 cm 0-0.5 0.5-1 1-1.5 1.5-2 2-2.5 2.5-3 3-4 4-5 cm 0-0.5 0.5-1 1-1.5 1.5-2 2-2.5 2.5-3 3-4 4-5

cm 0-0.5 0.5-1 1-1.5 1.5-2 2-2.5 2.5-3 3-4 4-5 cm 0-0.5 0.5-1 1-1.5 1.5-2 2-2.5 2.5-3 3-4 4-5 cm 0-0.5 0.5-1 1-1.5 1.5-2 2-2.5 2.5-3 3-4 4-5 cm 0-0.5 0.5-1 1-1.5 1.5-2 2-2.5 2.5-3 3-4 4-5 cm 0-0.5 0.5-1 1-1.5 1.5-2 2-2.5 2.5-3 3-4 4-5 cm 0-0.5 0.5-1 1-1.5 1.5-2 2-2.5 2.5-3 3-4 4-5 cm 0-0.5 0.5-1 1-1.5 1.5-2 2-2.5 2.5-3 3-4 4-5

Fig. 3. Vertical distribution profiles of stained benthic foraminiferal abundance (no. of individuals [indiv.] per 50 cc) in the sediments down to 5 cm below the surface (fraction 432 mm) and number of species per sample.

SU-1 (4635 m)

SU-2 (4074 m)

SU-8 (3774 m)

SU-3 (3059 m)

SU-6 (2055 m)

SU-5 (1053 m)

SU-4 (534 m)

sediment interval cm 0.0 0.5 1.0 1.5 2.0 2.5 3.0 4.0 5.0 0.0 0.5 1.0 1.5 2.0 2.5 3.0 4.0 5.0 0.0 0.5 1.0 1.5 2.0 2.5 3.0 4.0 5.0 0.0 0.5 1.0 1.5 2.0 2.5 3.0 4.0 5.0 0.0 0.5 1.0 1.5 2.0 2.5 3.0 4.0 5.0 0.0 0.5 1.0 1.5 2.0 2.5 3.0 4.0 5.0 0.0 0.5 1.0 1.5 2.0 2.5 3.0 4.0 5.0 Adercotryma glomeratum Ammobaculites paradoxus Ammodiscus planorbis Ammoscalaria tenuimargo Bigenerina nodosaria Cribrostomoides subglobosus Glomospira gordialis Hormosina pilulifera Hormosina spiculifera Hormosinella guttifera Karreriella pupiformis Lagenammina difflugiformis Lagenammina sp.1 Marsipella cylindrica Martinottiella communis Nouria harrisii Paratrochammina challengeri Portatrochammina wiesneri Psammosphaera fusca Reophax bradyi Reophax dentaliniformis Reophax longicollaris Reophax scorpiurus Reophax sp. 1 Reophax spiculifer Reophax subfusiformis Resigella moniliformis Rotaliammina chitinosa Saccammina sphaerica Usbekistania charoides Astrononion novozealandicum Bolivina robusta Bolivina spathulata Cibicidoide spachyderma Cibicidoides robertsonianus Epistominella exigua Globocassidulina subglobosa Melonis affinis Neouvigerina ampullacea Nuttallides bradyi Oridorsalis umbonatus Parrelloides bradyi type 1 Parrelloides bradyi type 2 Seabrookia pellucida Siphonina tubulosa Trifarina angulosa Uvigerina auberiana Saccorhiza ramosa Rhizammina algaeformis Rhizammina indivisa

R. Szarek et al. / Deep-Sea Research II 54 (2007) 145–176

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agglutinated species

153

calcareous species

no. individ. / 10 cc

5 - 10

>10

1-5

>1

Fig. 4. Down-core occurrences of the common stained agglutinated and calcareous benthic foraminiferal species in the Sulu Sea sediments, with sites arranged according to increasing water depth.

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R. Szarek et al. / Deep-Sea Research II 54 (2007) 145–176

calcareous form appeared on the surface, but below 2.5 cm several living individuals of Valvulineria mexicana occurred. Some calcareous species did not occur in the surface layer (0–0.5 cm) of the sediment at all, but were present in the 0.5–1-cm interval and deeper (e.g. Globobulimina pacifica, Pullenia bulloides, Discorbinella araucana, and Valvulineria mexicana). The vertical distribution of agglutinated species in the Sulu Sea had a different pattern at each site studied (Fig. 3). The faunal composition of continental slope samples was similar at both sites SU-4 and SU-5 (Fig. 4), but at the shallower site SU-4 some species were dwelling deep in the sediment, while at site SU-5 they occurred in the uppermost 2 cm of sediment (e.g. Bigenerina nodosaria, Saccammina sphaerica, or even Rhizammina algaeformis). In addition, at site SU-4 many species occurred below the surface starting from the 0.5–1-cm layer down the sediment column, while at site SU-5 their maximum abundance occurred in the 0–0.5 surface layer (e.g. Reophax scorpiurus, Gavelinopsis translucens, Neouvigerina ampullacea). At water depths below 2000 m, the total number of agglutinated species decreased to approximately 40 species. The living assemblages in the uppermost 1 cm of sediment were dominated by Lagenammina difflugiformis, Reophax sp. 1, Reophax spiculifer, Ammoscalaria tenuimargo, and tubular forms Saccorhiza ramosa, Rhizammina indivisa, and Rhizammina algaeformis. The maximum abundance of certain species appeared down the sediment column, for example: Karreriella pupiformis, Cribrostomoides subglobosus, Usbekistania charoides, or Haplophragmoides bradyi. The stained agglutinated fauna at two abyssal sites were concentrated in the 0.5–1.5-cm layer of sediment. The faunal composition was similar to that of the other deep-sea sites, although higher densities of Adercotryma glomeratum, Ammobaculites paradoxus, Ammodiscus planorbis, and Ammoscalaria tenuimargo were observed. The organic-walled foraminifera occurred rarely and predominantly in the uppermost 1 cm of sediment. They were numerous only at SU-4 site, located at a water depth of 534 m. In the abyssal zone, single specimens of Resigella moniliformis, and Nodellum membranaceum were found in surface sediments. Organic-walled trochamminaceans such as Lepidodeuterammina ochracea and Rotaliammina chitinosa appeared at the surface at the deepest site (SU-1 5635 m).

Tubular forms were concentrated in the uppermost 2.5 cm of the sediment column, except for a few fragments of Rhizammina algaeformis at site SU-4. The most abundant at all sites were Saccorhiza ramosa and Rhizammina algaeformis. At site SU-6 (2055 m), tubular forms were very abundant, their fragments comprised great proportion of the total living assemblage. 4.4. ALD The overall ALD5 of living assemblages in the Sulu Sea surface and subsurface sediments is presented in Fig. 2J. It also summarizes the microhabitat preferences of calcareous and agglutinated foraminifera, plus organic-walled and tubular forms. The ALD values for calcareous species increased gradually with increasing water depth, from 0.47 cm at 534 m to 3.05 cm at 4635 m. The agglutinated species ALD values fluctuated within the 0.5–1.4 cm interval, regardless of water depth. Since agglutinated foraminifera dominated the living assemblage, the total ALD values followed the same pattern. However, there was a slight difference in the vertical distribution pattern of tubular forms. Their ALD values steadily decreased along the depth transect from 0.79 to 0.35 cm, but at two abyssal sites the ALDs deepened again. The ALD values of organic-walled foraminifera were relatively deep on the continental slope, between 1.1 and 1.25 cm. Single specimens occur in the 0–0.5 cm interval in the lower bathyal zone at water depths from 2000 to 4000 m. In the abyssal zone, they mainly occupied the 0.5–1-cm interval. In this study, we only considered the top 5 cm of the sediment, so the ALD would probably have increased if we had searched deeper sediment layers. However, the ALDs of the stations with a shallow microhabitat would not changed much, because in these stations (SU-5 and SU-8) the lowermost intervals hardly contained any stained foraminifera. The patterns for ALD values for individual species along the depth transect usually reflected one of three basic trends (Fig. 5). The ALDs of some species apparently deepened in the sediment column with increasing water depth, for example, Parrelloides bradyi type 1, Parrelloides bradyi type 2, Ammoscalaria tenuimargo, and Ammobaculites paradoxus. On the continental slope their ALDs were within the 0–0.5 cm interval, in the lower bathyal zone below 0.5 cm and still deeper in the abyssal zone down to 3 cm. Other species such as

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534

lower bathyal

abyssal

1053 2055 3059 3774 4074 4635

534

SU 4 SU 5 SU 6 SU 3 SU 8 SU 2 SU 1 0.5

0.5

lower bathyal

abyssal

1053 2055 3059 3774 4074 4635

Karreriella pupiformis

2.0

1.5

0.0

0.0

0.5

0.5

0.0 0.5

1.0

1.0 Ammobaculites paradoxus

1.0 Lagenammina difflugiformis

1.5 2.0

0.0 Ammoscalaria tenuimargo

Marsipella cylindrica

Reophax scorpiurus

0.5

0.5

1.0

1.0

1.0

1.5

1.5

1.5

0.0

0.0

0.0

0.5

0.5

0.5

1.0

1.0

2.0 0.0

Cibicidoides robertsonianus

1.5 2.0 0.0

Cribrostomoides nitidus 1.0

0.5

1.0 Melonis affinis Nouria harrisii

0.0 0.5 1.0

2.0

1.5

1.5

3.0 0.0

2.0

2.0

0.0

0.0

0.5 Glomospira gordialis

1.5 2.0

1.5

1.0 Oridorsalis umbonatus 1.5

0.0

0.0

0.5

0.5

0.5

1.0

1.0

1.5 0.0

1.5

1.5

0.0

0.0

0.5

0.5

0.0 Hormosina pilulifera

1.0 1.5 2.0

1.0

1.0

1.0 Parrelloides bradyi type 1

Hormosina spiculifera

Saccorhiza ramosa

1.5

1.5

0.0

0.0

0.0

0.5

1.0 Hyperammina cylindrica

1.5

0.5 1.0

2.0

1.0

Rhizammina indivisa

Rotaliammina chitinosa

Paratrochammina challengeri

0.5

Rhizammina algaeformis

0.5

1.0

1.0

Reophax sp. 1

1.5

1.0

0.5

Reophax bradyi

0.0

0.5

1.5

1053 2055 3059 3774 4074 4635

Portatrochammina wiesneri

1.5

0.0

abyssal

0.5

1.5

1.5

lower bathyal

SU 4 SU 5 SU 6 SU 3 SU 8 SU 2 SU 1

1.0

Adercotryma glomeratum

continent. slope

ADL5

1.0 1.5

1.0

155

534

SU 4 SU 5 SU 6 SU 3 SU 8 SU 2 SU 1 ADL5

ADL5

continent. slope

water depth

continent. slope

water depth

water depth

R. Szarek et al. / Deep-Sea Research II 54 (2007) 145–176

3.0

Parrelloides bradyi type 2

1.5 2.0

Usbekistania charoides

Fig. 5. Average living depth distribution of the selected species in relation to water depth (down to 5 cm). The grey field marks sites from dysoxic environments (DO o1 ml/l).

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Cribrostomoides nitidus, Marsipella cylindrica or Glomospira gordialis showed the opposite trend, with ALDs shallower in the lower bathyal zone than on the continental slope. Also, individuals of Nouria harrisii and Rotaliammina chitinosa occurred on the continental slope deeper in the sediment column, while under oxygen-depleted conditions they were found in the surface layer. However, the most common was the mixed pattern, where on the continental slope the ALDs suggested a shallow infaunal mode of life of the species, then at water depths between 2000 and 4000 m this same species lived close to the surface of sediment and its ALDs were shallow, while in the abyssal zone in dysoxic conditions the ALDs of species deepened again. This pattern was observed for species such as Hormosina spiculifera, Saccammina sphaerica, Saccorhiza ramose, and Resigella moniliformis. Almost a quarter of the species (75) were found at a single location or in very low densities. All these species were encountered at the surface layer. At two abyssal sites characterized by DO values lower than 1 ml/l, the ALDs for many species significantly differ. First, the ALDs at site SU-2 (water depth 4074 m), with DO above the sediment surface of approximately 0.99 ml/l, were usually 1–2 cm deeper in the sediment column than for the same species in the lower bathyal zone and more oxygenated environment. However, at the deeper site SU-1 (water depth 4635 m), with DO values less than o0.97 ml/l, the ALDs became markedly shallower again. This trend was observed for some commonly occurring deep-sea species, for example, for Cribrostomoides subglobosus the shift in ALD was 1.5 cm upward, for Saccorhiza ramosa, Ammobaculites paradoxus, and Cribrostomoides nitidus it was 0.8, 0.6 and 0.5 cm, respectively. Summarizing our observations on the dwelling depth of stained benthic fauna, the common species in the Sulu Sea assemblages show following microhabitat preferences (see also Table 3):





Epifaunal species (ALD5p1.0): Bolivina variabilis, Cibicides lobatulus, Epistominella exigua, Nuttallides bradyi, Siphonina tubulosa, Trifarina angulosa, Uvigerina auberiana. Shallow infaunal species (ALD5 1.0–1.5): Ammobaculites paradoxus, Ammoscalaria tenuimargo, Bolivina spathulata, Lagenammina difflugiformis, Marsipella cylindrica, Parrelloides bradyi var. 1,

 

Portatrochammina wiesneri, Reophax scorpiurus, Reophax sp. 1, Reophax spiculifer. Intermediate infaunal species (ALD5 1.5–2.5): Melonis affinis, Nouria harrisii, Oridorsalis umbonatus, Reophax bradyi, Usbekistania charoides. Deep infaunal species (ALD5 42.5): Ammodiscus planorbis, Parrelloides bradyi type 2, Valvulineria mexicana.

4.5. Correlation with environmental factors The eigenvalues obtained from CCA denote relatively good separation of the parameters along the axes. The first (A1) axis had the eigenvalue of l1 equal to 0.58 of the total dispersion of the species scores on the ordination axis, and the second (A2) axis had the eigenvalue of l2 equal to 0.35. The cumulative percentage variance of the species–environment relation for the four axes reached 89.9%. The scores formed an arched plot, and thus statistically relevant information was obtained (Shi, 1993) and can be further used for an environmental interpretation. The strongest correlation, in decreasing order of factor regression coefficients of given environmental parameters with faunal distribution is: C org flux, DO, water depth, temperature and PP rates. The vectors of environmental variables are presented on the CCA plot (Fig. 6). Dissolved oxygen and C org flux arrows are related to the A1 axis as well as water depth, which is inversely correlated with these two. One site from the upper continental slope, SU4 (534 m) occurs on the positive side of the A1 axis, whereas sites from the bathyal and abyssal zones are grouped together on negative side of the A1 axis. The positive loadings of A1 generally indicate an oxic (42 ml/l), more productive and shallower environment, and negative ones indicate deep-sea and oxygen-depleted conditions. The A2 ordination axis separates sites based on the near-bottom temperature with the boundary value of 10.25 1C. Thus only two sites, SU-5 and SU-6, with lower temperature cluster on the positive side of the A2 axis and the remaining five sites are grouped on the negative side of the A2 axis. However, the temperature between these extreme A2 loadings differs by less than 1 1C, and thus the pattern results from a statistical artefact rather than influence of temperature. Species loadings plotted close to each other on the CCA plot are usually related to the same environmental conditions. All species are plotted, but only

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157

Table 3 Average living depth (ALD5) of foraminiferal species and the number of individuals on which the calculation is based (in brackets) Max. ALD5

Water depth (m) Epifauna/shallow infauna Ammobaculites agglutinans Ammoglobigerina globulosa Astrononion novozealandicum Bolivina robusta Bolivina spathulata Bolivina variabilis Cibicides lobatulus Cibicidoides pachyderma Epistominella exigua Eponides pusillus Fontbotia wuellerstorfi Globocassidulina bisecta Globocassidulina subglobosa Glomospira gordialis Hippocrepinella alba Hormosina pilulifera Hyperammina cylindrica Hyperammina elongata Lacroixina cochleata Lagenammina sp.1 Lenticulina calcar Marsipella cylindrica Marsipella dextrospiralis Marsipella elongata Nuttallides bradyi Osangularia culter Paracassidulina minuta Paratrochammina challengeri Parvigenerina bigenerinoides Portatrochammina wiesneri Reophax hispidulus Reophax scorpiurus Reophax sp. 1 Reophax spiculifer Rhabdammina abyssorum Rhizammina indivisa Saccammina anglica Seabrookia pellucida Siphonina tubulosa Tolypammina vagans Trifarina angulosa Trochammina hadai Uvigerina auberiana

0.97 0.75 0.61 0.66 0.65 0.29 0.29 0.58 0.46 0.25 0.50 0.51 0.58 0.50 0.25 0.75 0.86 0.75 0.25 0.75 0.25 0.91 0.90 0.58 0.32 0.25 0.25 0.68 0.72 0.75 0.75 0.85 0.81 0.77 0.75 0.80 0.25 0.66 0.37 0.25 0.36 0.25 0.50

Shallow infauna Adercotryma glomeratum Ammobaculites paradoxus Ammoscalaria tenuimargo Bigenerina nodosaria Bolivina pacifica Cibicidoides robertsonianus Gavelinopsis translucens Hoeglundina elegans Hormosina spiculifera Lagenammina difflugiformis Parrelloides bradyi var. 1 Psammosphaera fusca Reophax longicollaris Rotaliammina chitinosa Saccorhiza ramosa

1.05 1.35 1.42 1.00 1.00 1.50 1.50 1.36 1.50 1.14 1.50 1.14 1.25 1.25 1.04

Station no. SU-4

SU-5

SU-6

SU-3

SU-8

SU-2

SU-1

534

1053

2055

3059

3774

4074

4635

0.51 0.61 0.66 0.65 0.29

(6) (8) (4) (11) (12)

0.36 (9) 0.46 (5)

0.51 (6) 0.29 (12)

0.97 0.75 0.25 0.36 0.40

(9) (2) (4) (9) (10)

0.29 0.58 0.32 0.25 0.50 0.25 0.58 0.50

(13) (6) (7) (9) (8) (3) (3) (2)

0.25 (1)

0.25 (1)

0.46 (7)

0.25 (1)

0.25 (5) 0.75 (1) 0.75 (2)

0.75 (3) 0.25 (5) 0.75 (1)

0.75 (3)

0.75 (1)

0.75 (3)

0.81 (24)

0.69 (9)

0.39 (4) 0.25 0.25 0.91 0.90 0.58 0.32 0.25 0.25

(11) (5) (26) (10) (8) (14) (11) (8)

0.25 0.61 0.25 0.25

(2) (5) (8) (7)

0.58 (6) 0.25 (2)

0.86 (9)

0.75 (15) 0.47 (9)

0.72 (15)

0.25 (1)

0.65 (5)

0.68 (7)

0.42 (3)

0.25 (1)

0.50 0.75 0.46 0.51 0.32

0.25 (3)

0.75 (3)

0.75 (16)

0.85 (5) 0.30 (19)

0.53 (20) 0.81 (9)

0.35 (10)

0.63 (20)

0.75 (1) 0.50 (2)

0.57 (11) 0.80 (20)

0.25 (1)

0.25 (6)

0.25 (2)

0.25 (2) 0.75 (10)

0.75 (1) 0.58 (6) 0.65 (10)

1.05 (5) 1.35 (10) 1.42 (7)

0.65 (28) 0.75 (2)

1.50 0.57 1.50 1.14

0.72 (17)

0.75 (2)

0.53 (27) 0.42 (35)

0.75 (4) 0.67 (6)

0.33 (13)

0.75 (1) 0.37 (17)

0.77 (37) 0.75 0.25 0.66 0.37

(3) (5) (13) (13)

0.36 (44) 0.25 (5) 0.42 (9)

0.96 1.00 0.25 1.50 1.36 0.60 0.56 0.34 0.25 0.51 1.14 0.56

(6) (7) (3) (2) (6) (6) (19) (12) (5) (6) (14) (47)

(2) (8) (7) (23) (15)

0.50 (4)

0.25 (1) 0.25 (4) 0.25 (1) 0.50 (14)

0.25 0.52 1.00 (11) 0.98 0.39

(4) (13) (4)

0.25 0.75 0.47 1.00

(3) (7) (9) (2)

0.25 (2) 0.75 (2) 0.50 (2)

(11) (7)

1.25 (1) 0.81 (26)

0.92 (6) 0.75 (2) 1.11 (11)

1.50 (2)

0.25 0.56 0.69 0.75

(1) (16) (8) (1)

0.51 (29)

0.75 (1) 0.53 (25) 0.50 (10)

0.49 (21)

0.25 (3)

(2) (14) (4) (4)

1.04 (14)

1.14 (14)

1.25 (14) 0.25 (1) 0.25 (2)

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158 Table 3 (continued )

Max. ALD5

Station no. SU-4

Septotrochammina gonzalezi

1.04

Intermediate infauna Cribrostomoides nitidus Gavelinopsis lobatulus Karreriella pupiformis Melonis affinis Neouvigerina ampullacea Nouria harrisii Oridorsalis umbonatus Reophax bradyi Rhizammina algaeformis Usbekistania charoides

2.21 1.75 1.75 1.75 1.75 1.90 1.75 1.58 2.00 1.65

Deep infauna Ammodiscus planorbis Parrelloides bradyi var. 2 Valvulineria mexicana

2.75 3.00 3.05

SU-5

SU-6

SU-3

SU-8

SU-2

SU-1

1.75 (1)

1.25 (1)

1.04 (13)

2.21 (7) 1.75 (1) 0.64 (8) 0.76 0.75 0.29 1.16

(20) (1) (12) (34)

0.50 1.25 1.15 1.75 1.90 1.04

(8) (1) (5) (1) (3) (7)

1.75 (2) 0.75 (1) 0.52 (11)

1.19 (9) 1.75 (1)

0.75 (1)

0.92 (3)

0.25 (4)

0.25 (4)

0.34 (22) 0.68 (7)

1.25 (1) 0.25 (2)

0.75 0.25 0.46 1.33

(2) (1) (14) (6)

0.25 (1)

2.75 (1) 1.31 (25)

1.93 (27)

0.33 (18) 0.75 (7)

1.75 1.58 2.00 1.65

(1) (3) (6) (5)

1.59 (12)

1.57 (15) 3.00 (8)

0.52 (11)

3.05 (14)

Only occurrences of X5 individuals in at least one core are shown.

1.5

tolerant species occur mostly in IV quadrant of CCA plot. The CCA plot of species scores shows also that certain species are placed closer to the origin of the axes (e.g. Nouria harrisii, Reophax spiculifer), and those species occur at sites in spite of the water depth. Species which nearly form a line on the edge of the plot occur at a single location. The distribution of site and species scores along the A1 ordination axis reflects their correlation with decreasing rates of C org flux and decreasing amounts of DO in the water column, with a correlation coefficient of r2 ¼ 0.956 and 0.88, respectively (Fig. 8A and B).

CCA - site scores / x flu th g- p or de C ter ng wa si ea ing cr as de cre in

1.0

SU-5

0.5

PP DO

SU-6

C org-flux

A2 SU-3

SU-4

-0.5

-1.0 -1.0

SU-8

Water depth Temperature

SU-2 SU-1

-0.5

5. Discussion

A1

0.5

1.0

1.5

Fig. 6. CCA plot showing the distribution of sites along A1 and A2 axes in relation to environmental parameters: water depth, C org flux, primary production (PP), dissolved oxygen (DO) and near bottom temperature.

species that significantly contribute to the factor values are shown on the graph (Fig. 7). The position of species along the A1 axis is determined mainly by their water depth-related occurrences and other factors such as C org flux or oxygen availability. The oxyphilic species occur mostly in quadrants I and II, while the low-oxygen

5.1. Environmental factors controlling deep-sea benthic foraminifera The environment in the deep-sea is generally food-limited and relatively stable in terms of its physico-chemical characteristics compared to the neritic zone (Gooday and Rathburn, 1999). Even so, benthic foraminiferal faunas inhabiting water depths from the shelf break (4200 m) down to the abyssal plain are exposed to various environmental factors that define and often limit their faunal composition and abundance. Among these factors, temporal variations in the C org flux and oxygen availability are the major parameters controlling the benthic foraminiferal ecological niche in the deep-

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CCA - species scores

Selected species with CCA weight

/ lux g-f epth or C er d ing at as g w cre in de reas inc

3.0

II

III

2.0

12

I

8

II 9

1.0

20 13

15 22 19

A2

17 21 25

24 26 23

18

11

16

10 14

3 1

28

III

7 4 6 2

5

-1.0 30 29 27

IV I

IV -2.0 -2.0

-1.0

A1

1.0

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1. Reophax spiculifer (39.25) 2. Trifarina angulosa (34.08) 3. Nouria harrisii (19.81) 4. Rotaliammina chitinosa (12.12) 5. Reophax bradyi (11.87) 6. Nuttallides bradyi (11.61) 7. Seabrookia pellucida (10.86) 8. Uvigerina auberiana (17.42) 9. Bolivina spathulata (16.15) 10. Siphonina tubulosa (12.62) 11. Cibicidoides pachyderma (12.12) 12. Cibicidoides robertsonianus (11.86) 13. Melonis affinis (11.12) 14. Globocassidulina subglobosa (11.11) 15. Reophax sp. 1 (69.68) 16. Marsipella cylindrica (62.73) 17. Reophax scorpiurus (56.8) 18. Parrelloides bradyi type 1 (33.83) 19. Usbekistania charoides (20.44) 20. Oridorsalis umbonatus (13.63) 21. Cribrostomoides subglobosus (11.74) 22. Paratrochammina challengeri (11.36) 23. Lagenammina difflugiformis (93.02) 24. Parrelloides bradyi type 2 (49.98) 25. Ammoscalaria tenuimargo (39.74) 26. Ammobaculites paradoxus (19.67) 27. Portatrochammina wiesneri (18.93) 28. Saccammina sphaerica (13.0) 29. Ammodiscus planorbis (11.74) 30. Adercotryma glomeratum (10.6)

2.0

Fig. 7. CCA plot showing the distribution of species along A1 and A2 axes (some important species are listed with their CCA weight).

(B) 2.5

(A) 12 by equation of Suess (1980)

y = 0.613x + 1.548 SU-4

r2=0.88

2.0

r2= 0.956

8

DO (ml/l)

C org-flux (g/m2yr)

y = 4.705x + 5.157

SU-5

SU-5

1.5 SU-6

4 SU-3 SU-8

0 -2

-1

SU-8

1.0

SU-6

SU-2 SU-1

A1

SU-4

SU-3 SU-2 SU-1

0.5 1

2

-2

-1

A1

1

2

Fig. 8. Regression of sites A1 loadings in the CCA against (A) C org flux rates calculated after Suess (1980) and (B) dissolved oxygen (DO) values.

sea (Jorissen, 1999; Loubere and Fariduddin, 1999; Van der Zwaan et al., 1999; Kitazato et al., 2000; Gooday, 2003). Other parameters such as water masses (Mackensen, 1997; Culver and Buzas, 2000), temperature (Rathburn et al., 1996), hydrodynamics of bottom water (Hall, 1994; Scho¨nfeld, 2002) or stability of the surrounding environments (Weaver et al., 1992) are believed to have a considerable impact on deep-sea benthic foraminifera.

5.1.1. Organic carbon flux The CCA solution plot (see Fig. 6) shows that C org flux, which is inversely correlated with water depth, is a major factor controlling the distribution patterns in the Sulu Sea. The decreasing rates of C org flux with water depth significantly influence the standing stock values in our study area (Fig. 2C and D). The standing stock values rapidly decreased along the bathymetric transect. In the abyssal zone,

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it was approximately 5-fold lower (126 individuals/ 10 cm2, 0–5 cm) than on the upper continental slope (534 m). This relationship between higher organic fluxes and greater densities of living foraminifera has been observed by Altenbach (1992) and later reported from eutrophic to oligotrophic environments (de Stigter, 1996; Heinz and Hemleben, 2003; Hess, 1998). It is also consistent with previous investigations in the Sulu Sea basin by Rathburn and Corliss (1994). It is important to note that the calculated fluxes of organic matter to the sea floor, which are used for analyses and interpretation, may significantly differ from the real organic inputs in the Sulu Sea. First of all, fluxes may be higher on the slope as a result of higher productivity particularly in upwelling regions, lateral advection from the shelf and direct terrigenous inputs (Gooday and Rathburn, 1999). However in the Sulu Sea Basin also at the at the deepest site (4635 m) the relatively high organic carbon values probably result from the transport of organic-rich sediments from shallower depths via turbidites (Rathburn et al., 1996). In tropical regions, the seasonally enhanced standing stock values are usually positively correlated to seasonal pattern of biological productivity in surface waters and C org flux, which are related to the monsoon circulation patterns (e.g. Jannink et al., 1998; Gooday et al., 2000; Heinz and Hemleben, 2003). However, Rathburn and Miao (1995) compared box core and gravity core-top benthic foraminiferal assemblages from 500 to 4000 m in the Sulu Sea and reported that most of the faunal patterns in the Sulu Sea are independent of seasonal variations. We have observed that the correlation between the living assemblage composition (factor 1 in CCA) and the annual C org flux (calculated with an empirical equation of Suess, 1980) is very close (see Fig. 8A). The linear correlation coefficient is r2 ¼ 0:956. Such a close correlation is usually obtained from analysis of total time-averaged assemblages (living and dead) rather then living, which usually reflects nutrient availability during the sampling season. Samples for this study were collected in higher productivity season, when Sulu Sea is influenced by winter monsoon. However, the standing stock values in the bathyal zone observed in this study for November/December 2002 were similar to the values observed by Rathburn and Corliss (1994) for August 1988 (see Table 2). Thus, our data may support the Rathburn and Miao (1995) assumption, that deep-sea faunal

abundances in the Sulu Sea appear not to vary much during the course of the year. In the abyssal zone, standing stock values in this study were significantly higher than observed by Rathburn and Corliss (1994). This difference might be explained by irregular organic matter input resulting from turbidites. Rathburn and Corliss (1994) reported, that in the area located near Mindanao Island, X-radiograph analysis revealed evidence for turbidite sedimentation. Increased supply of labile organic matter from turbidites, which may be periodic over long time scales (Weaver et al., 1992), may have impact on foraminiferal assemblages. Foraminiferal responses to irregular, non-seasonal organic matter inputs were discussed by Gooday and Rathburn (1999), who stated that turbidite deposits are exploited by species typical of high organic matter/low oxygen environments rather than by a specialised fauna. We observed at this site dominance of Portatrochammina wiesneri and Reophax longicollaris, both showed an epifaunal to shallow infaunal distribution. The faunal composition generally was similar to that of the other deep-sea sites, although higher densities of some infaunal species such as Adercotryma glomeratum, Ammobaculites paradoxus, Ammodiscus planorbis, and Ammoscalaria tenuimargo were observed. From deep-infaunal species only Valvulineria mexicana occurred below 2.5 cm at the 4635 m. According to Rathburn and Corliss (1994) Valvulineria mexicana is adapted to the low oxygen conditions and takes advantage of subsurface accumulations of organic carbon, including organic carbon from turbidite deposits. Thus, the benthic fauna at site SU-1 at 4635 m water depth is probably occasionally influenced by organic carbon transported from shallower regions by turbidites. 5.1.2. Oxygen concentrations The level of bottom-water oxygen concentrations limiting the benthic foraminiferal faunas is not strictly defined, but many authors (Jorissen et al., 1995; Levin et al., 2000; Gooday, 2003) agree that values of less than 1 ml/l of O2 begin to affect the community structure of benthos. Levin and Gage (1998) suggested an existence of oxygen threshold at o0.45 ml/l. In the Sulu Sea, the living benthic assemblages appear to be influenced to some extent by amounts of DO in the water column. The linear correlation coefficient for the living fauna (factor 1 in CCA) and DO values obtained from CTD measurements is r2 ¼ 0:88 (see Fig. 8B). The CCA

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results show that there is a close relationship among four deep-sea assemblages from water depths below 3000 m (Fig. 6). Two of them, SU-3 and SU-8, are from the lower bathyal zone, while the two others, SU-1 and SU-2, are from the abyssal zone (44000 m). Based on the CTD measurements, these two sites from the abyssal plain are considered dysoxic (o1 ml/l O2), while SU-3 and SU-8 from the lower bathyal zone are very close to the critical value, with DO values of 1.02 and 1.01 ml/l, respectively. At these four sites, the standing stock, faunal composition, diversity indices and ALDs were similar, but there were also important differences. At site SU-3 and especially SU-8, the maximum densities of living specimens occurred at the surface in 0–0.5 cm interval. While, at the two abyssal sites, abundances were 50% lower at the sediment–water interface than within the interval from 0.5 to 1 cm (see Fig. 3). At these sites, most species are low oxygen tolerant, and therefore the migratory behaviour of species is more likely induced by food supplies than by changes in oxygen concentrations. At the depths greater than 3000 m, the agglutinated foraminifera composed 80–95% of the living foraminiferal fauna. A small percentage (up to 3.7%) was organic-walled, nonfossilizable trochamminaceans (e.g. Deuterammina ochracea, Rotaliammina chitinosa). Only at the deepest site SU-1 (4635 m) did the epifaunal/shallow infaunal agglutinated species such as Portatrochammina wiesneri, Ammoscalaria tenuimargo or Adercotryma glomeratum appear in significant abundance. The stained individuals of Oridorsalis umbonatus or Cibicidoides bradyi (expected synonym of Parrelloides bradyi) reported by Rathburn and Corliss (1994) as dominant calcareous species below 3000 m, occurred in slightly lower numbers at related water depths. This can be related to the occurrences of these species deeper in the sediment layers (even down to 13 cm), which were not checked in this study. At sites with low oxygen levels (DOo1 ml/l O2), stained juvenile forms were found mostly in the uppermost centimetre of the sediments. Contrary to the statement of Rathburn and Corliss (1994), that adults and juveniles generally have similar sediment distribution patterns in the Sulu Sea sediments. On the continental slope, at the water depths 534 and 1053 m (SU-4 and SU-5), the uppermost 0.5 cm of the sediment were inhabited mainly by the calcareous species Trifarina angulosa, Nuttallides bradyi, Cibicides lobatulus, and Seabrookia pellucida

161

(see Fig. 4). The agglutinated individuals dominated the interval between 1 and 2 cm of the sediment, but calcareous species such as various Uvigerina, Bolivina, Epistominella, and Nonionella with infaunal microhabitat preferences and known for their tolerance of oxygen depletion (Lutze and Colbourn, 1984; Bernhard et al., 1997; Gooday and Rathburn, 1999) were also common. However, most of these calcareous species do not occur below 2000 m water depth. A similar calcareous faunal composition was reported from the Sulu Sea by Rathburn and Corliss (1994), with Cibicidoides, Uvigerina and Siphonina being dominant genera at related depths. At continental slope sites, agglutinated tubular foraminifera such as Saccorhiza ramosa, Marsipella cylindrica or Rhizammina algaeformis were very important. According to Kaminski et al. (1995) some genera such as Saccorhiza and Marsipella can tolerate moderate dysoxia, but not the more extreme conditions found within some OMZs and low oxygen basins. We observed, that these tubular genera may obviously withstand constantly dysoxic conditions. Although abundance of tubular fragments decreased with water depth, still they occurred in significant number at the greatest depths in the Sulu Sea (Fig. 4). 5.2. Diversity in relation to oxygen availability The influence of dysoxia on benthic foraminiferal species richness was observed along the water depth transect studied. The number of species decreases rapidly at depths below 2000 m. Also, the diversity indices Fisher’s a-index and Shannon–Wiener values rapidly decreased below 2000 m, and then remained almost at the same level down to abyssal depths. Levin and Gage (1998) suggest existence of an oxygen threshold (o0.45 ml/l), below which oxygen becomes a critical factor for macrofauna diversity. However, the benthic foraminiferal diversity in the Sulu Sea decreased rapidly when nearbottom oxygen levels were well above 1 ml/l. For DO varying from 1.23 to 0.97 ml/l the H(S) values ranged from 3.1 to 3.4. The sharp reduction in the number of stained species by more than half below the water depth of 2000 m (see Fig. 2F) is probably related to the disappearance of some epifaunal species such as Hoeglundina elegans, Lenticulina spp., Gavelinopsis spp. or Rosalina spp. as a result of the low oxygen concentrations. These species have been described by Kaiho (1994) and Jannink (2001) as oxyphilic species.

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Generally, in the Sulu Sea species diversity and faunal abundances of benthic foraminifera decrease with increasing water depth (Fig. 2G and H). This was before reported by Miao and Thunell (1993) and by Rathburn and Corliss (1994) from Sulu Sea. It also was observed in other basins for example by Ingle et al. (1980) and Corliss and Emerson (1990). 5.3. Distribution patterns of benthic foraminifera At the continental slope sites SU-4 (534 m) and SU-5 (1053 m), with the highest levels of organic matter and with DO level greater than 1.7 ml/l, the living benthic foraminifera were concentrated in the first 2 cm (Fig. 3). The community of epifaunal and shallow infaunal, mainly calcareous, foraminifera was very diverse (4130 species). The deep infaunal calcareous species such as Globobulimina pacifica and Chilostomella spp. occurred only at continental slope sites, below 2 cm in the sediment column. However, these species were found down to the abyssal depths by Rathburn and Corliss (1994). Globobulimina occurred between 8 and 10 cm and Chilostomella between 5 and 11 cm in the sediment in the Sulu Sea assemblages. Since we checked sediments only down to 5 cm, we may lack important information on these deep-infaunal species in our dataset. At the transitional site SU-6 (2055 m), the average faunal penetration of calcareous species and also of organic-walled species was slightly deeper. This is probably due to lower oxygen values, which could limit the occurrence of certain oxyphilic species, while enabling colonization of the deeper sediment layers by infaunal species. In the abyssal zone, standing stock and species richness were low, benthic faunas were the most abundant in the 0.5–1 cm of the sediment (Fig. 3). The fauna from deepest site SU-1 (4635 m) is probably affected by the increased supply of organic material brought in by turbidites. The high abundances of species having high recolonisation potential at the site SU-1 such as Reophax spp., Rhizammina algaeformis and Lagenammina difflugiformis (Kaminski, 1985; Hess and Kuhnt, 1996) may be related to disturbances caused by turbidity flows. In an oligotrophic, abyssal plain environment the shallow infaunal and intermediate infaunal species tend to migrate toward the surface in search of food (e.g. Ammobaculites paradoxus, Adercotryma glomeratum). Other infaunal species take ad-

vantage of refractory organic matter and stay deep below the surface (e.g. Cribrostomoides subglobosus, Ammodiscus planorbis). Based on our observations, the ecological requirements of some selected infaunal species have been summarized herein: Melonis affinis (synonymous with Melonis barleeanus) shows a distribution pattern varying between epifaunal to deep infaunal (Jannink et al., 1998) in response to varying food availability or changing environmental conditions. Rathburn et al. (1996) described Melonis affinis as transitional infaunal species (0–4 cm) in the Sulu Sea. Caralp (1989) demonstrated that Melonis barleeanum is able to feed on fresh and degraded organic material. In Sulu Sea assemblages, Melonis affinis (Reuss) occurred mainly in the uppermost 2 cm of sediment down to a water depth of 3000 m. Its ALD values increased with increasing water depth and decreasing food and oxygen concentrations, from 0.6 at a water depth of 534 m to 1.8 cm at a water depth of 3059 m, respectively (Table 3). Fontanier et al. (2002) reported similar ALD10 values from of 0.8 to 1.7 cm for this species from well-oxygenated (43 ml/l) environment in Bay of Biscay (Plates 1 and 2). Two morphologic types of Parrelloides (Cibicidoides) bradyi (Trauth) have been found in Sulu Sea residues (see Plate 3, Figs. (18) and (19)). These two types show clear microhabitat preferences, although they coexist at the same locations. Parrelloides bradyi type 1 occurs only in the uppermost centimetre of the sediment column at all studied sites (but not the deepest site SU-1), while Parrelloides bradyi type 2 occurs in low numbers down to a depth of 5 cm in the sediment column at all sites from water depths deeper than 2000 m but not the SU-1 site (see Fig. 4). Parrelloides bradyi type 2 is possibly an ecophenotype of type 1, showing adaptation to low oxygen levels. Type 2 differs from type 1 mainly in the height of its spiral. The differences in the test morphologies of this species were previously observed by Rathburn and Corliss (1994), who suggested that those are adaptation to low-oxygen conditions of deep-infaunal habitats. Rathburn et al. (1996) described Cibicidoides bradyi as transitional infaunal species living in sediment depths from 0 to 4 cm. The calcareous form Valvulineria mexicana Parker, 1954 (see Plate 3, Figs. (10) and (11)) occurred between 2.5 and 5 cm in the sediment column only at site SU-1 (water depth 4635 m). Moreover, this is

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Plate 1. (1) Bathysiphon macilentus Zheng, SU-2 (0–0.5), 1032 mm; (2) Hyperammina cylindrica Parr, SU-2 (0–0.5), 1099 mm; (3) Hyperammina laevigata (Wright), SU-3 (0.5–1), 1072 mm; (4) Marsipella cylindrica Brady, SU-2 (0–0.5), 1891 mm; (5) Marsipella elongata Norman, SU-4 (0.5–1), 1098 mm; (6) Rhizammina algaeformis Brady, SU-2 (0–0.5), 977 mm; (7) Saccorhiza ramosa (Brady), SU-2 (0.5–1), 1493 mm; (8) Nodellum membranaceum (Brady), SU-2 (0–0.5), 330 mm; (9,10) Resigella moniliformis (Resig), SU-2 (0–0.5), (10) 435, (11) 850 mm; (11) Dendronina arborescens Heron-Allen and Earland, SU-2 (4.0–5), 1543 mm; (12) Hippocrepinella alba Heron-Allen and Earland, SU-4 (0–0.5), 349 mm; (13) Sorosphaera confusa Brady, SU-1 (0.5–1), 167 mm; (14) Reophax longicollaris Zheng, SU-1 (1.5–2), 365 mm; (15) Reophax sp. 1, SU-2 (0.5–1), 766 mm; (16) Reophax dentaliniformis Brady, SU-2 (0–0.5), 1335 mm; (17) Reophax subfusiformis Earland, SU-1 (0.5–1), 645 mm; (18) Reophax scorpiurus de Montfort, SU-5 (0.5–1), 770 mm; (19) Reophax spiculifer Brady, SU-3 (0.–0.5), 1339 mm; (20) Lagenammina difflugiformis Brady, SU-1 (0–0.5), 345 mm; (21) Ammodiscus planorbis Ho¨glund, SU-2 (0–0.5), 500 mm; (22) Usbekistania charoides (Jones and Parker), SU-2 (0.5–1), 231 mm; (23) Glomospira gordialis (Jones and Parker), SU-8 (0.5–1), 265 mm; (24) Hormosina spiculifera Hofker, 1972, SU-1 (0.5–1), 913 mm; (25) Hormosinella guttifera (Brady), SU-2 (0–0.5), 685 mm; (26) Martinottiella communis (d’Orbigny), SU-6 (0.5–1), 689 mm; (27) Cribrostomoides subglobosus (M. Sars), SU-2 (4.0–5), 299 mm; (28) Haplophragmoides bradyi (Robertson), SU-4 (3.0–4), 307 mm, aperture.

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Plate 2. (1) Haplophragmoides sphaeriloculum Cushman, SU-4 (3.0–4), 459 mm; (2) Veleroninoides wiesneri (Parr), SU-2 (2–2.5), 399 mm; (3) Ammoscalaria tenuimargo (Brady), SU-1 (0–0.5), 327 mm; (4) Glaphyrammina americana (Cushman), SU-1 (0.5–1), 224 mm; (5) Adercotryma glomeratum (Brady), SU-1 (0–0.5), 182 mm; (6) Ammobaculites filiformis (Earland), SU-1 (1.5–2), 312 mm; (7) Ammobaculites sp., SU-8 (0–0.5), 420 mm; (8) Ammobaculites paradoxus Clark, SU-1 (0–0.5), 263 mm; (9) Parvigenerina bigenerinoides (Lacroix), SU-4 (0–0.5), 246 mm; (10) Lacroixina cf. cochleata (Lacroix), SU-1 (0–0.5), 138 mm; (11) Spiroplectammina biformis (Parker and Jones), SU-3 (0–0.5), 137 mm; (12) Textularia porrecta (Brady), SU-5 (0–0.5), 434 mm; (13) Recurvoides contortus Earland, SU-2 (0.5–1), 229 mm; (14) Trochammina subglobigeriniformis Mikhalevich, SU-1 (0.5–1), 110 mm, spiral; (15) Portatrochammina wiesneri (Parr), SU-1 (0.5–1), 141 mm, umbilical; (16) Globotrochamminopsis shannoni Bro¨nnimann and Whittaker, SU-1 (0.5–1), 117 mm, spiral; (17) Lepidodeuterammina ochracea (Williamson), SU-1 (0.5–1), 154 mm, spiral; (18) Remaneica helgolandica Rhumbler, SU-1 (0.5–1), 135 mm, umbilical; (19) Septotrochammina gonzalezi (Seiglie), SU-4 (0–0.5), 406 mm, spiral; (20) Rotaliammina chitinosa (Collins), SU-2 (0.5–1), 208 mm, umbilical; (21) Earlandammina inconspicua (Earland), SU-3 (0–0.5), 103 mm; (22) Karreriella bradyi (Cushman), SU-2 (1–1.5), 383 mm; (23) Karreriella pupiformis Zheng, SU-3 (0.5–1), 627 mm; (24) Clavulina pacifica Cushman, SU-4 (2.5–3), 1567 mm; (25) Ammoglobigerina globulosa (Cushman), SU-4 (0–0.5), 367 mm, spiral.

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Plate 3. (1) Seabrookia pellucida Brady, SU-4 (0–0.5), 250 mm; (2) Bolivina robusta Brady, SU-3 (0–0.5), 196 mm; (3) Bolivina spathulata (Williamson), SU-2 (0–0.5), 251 mm; (4) Bolivina variabilis (Williamson), SU-3 (0–0.5), 166 mm; (5) Aphelophragmina brittanica (Macfadyen), SU-3 (0.5–1), 142 mm; (6) Lernella inflata (LeRoy), SU-4 (0.5–1), 151 mm, umbilical; (7) Cassidelina complanata (Egger), SU8 (0–0.5), 264 mm; (8) Uvigerina auberiana d’Orbigny, SU-4 (0–0.5), 325 mm; (9) Trifarina angulosa (Williamson), SU-4 (0–0.5), 217 mm; (10,11) Valvulineria mexicana Parker, SU-1 (4.0–5), (10) 248 mm, umbilical, (11) 297 mm, spiral; (12) Globobulimina pacifica Cushman, SU-4 (2.5–3), 1375 mm; (13,14) Valvulineria minuta (Schubert), SU-6 (0.5–1), (13) 219 mm, spiral; (14) 271 mm, umbilical; (15,16) Gavelinopsis translucens (Phleger and Parker), SU-5 (0–0.5), (15) 272 mm, spiral; (16) 257 mm, umbilical; (17) Siphonina tubulosa Cushman, SU-4 (0–0.5), 335 mm, umbilical; (18) Parrelloides bradyi type 1 (Trauth), SU-5 (0–0.5), 273 mm, spiral; (19) Parrelloides bradyi type 2 (Trauth), SU-2 (4.0–5), 389 mm, spiral; (20) Epistominella exigua (Brady), SU-5 (0–0.5), 92 mm, umbilical; (21) Cibicidoides cicatricosus (Schwager), SU-3 (1–1.5), 399 mm, spiral; (22,23) Fontbotia wuellerstorfi (Schwager), SU-6 (0.5–1); (22) 512 mm, umbilical; (23) 514 mm, spiral; (24,25) Nuttallides bradyi (Earland), SU-3 (0.5–1), (24) 93 mm, umbilical, (25) 92 mm, spiral; (26) Astrononion novozealandicum Cushman and Edwards, SU-4 (0–0.5), 143 mm; (27) Oridorsalis umbonatus (Reuss), SU-2 (0–0.5), 234 mm; (28) Gyroidina neosoldanii Brotzen, SU-6 (0.5–1), 271 mm, spiral; (29) Gyroidinoides nipponicus (Ishizaki), SU-4 (0–0.5), 46 mm, aperture; (30) Rotaliella sp., SU-2 (0–0.5), 95 mm, umbilical.

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the only species found 3 cm below the surface. Site SU-1 in our study is located in an area described by Exon et al. (1981) as frequently disturbed by southern calcareous and terrigenous turbidites originating from the slopes off Mindanao. Rathburn and Corliss (1994) found stained specimens of Valvulineria mexicana in the Sulu Sea turbidite sediments at a location very close to our site SU-1 and at a similar water depth (4515 m). There, this species had the same microhabitat preferences (with maximum at 2.5–3 cm interval), co-occurring with Chilostomella oolina and Globobulimina spp. They noted, that Valvulineria mexicana can possibly be regarded as a dysoxic-tolerant species adapted to turbidite-disturbed environments, feeding on the organic matter delivered with turbidite. 6. Summary We studied 56 samples collected from seven multiple-core sampling sites in the Sulu Sea. The following conclusions were drawn from analysis of stained benthic foraminiferal assemblages: 1. The surface sediments (down to 5 cm) of the Sulu Sea yielded 285 living species of benthic foraminifera. Standing stock values varied from 595 individuals/10 cm2 on the continental slope to 100 individuals/10 cm2 on the abyssal plain. The low productivity and low oxygen conditions in the abyssal zone of the Sulu Sea are characterized by low standing stock values and low diversity. In the Sulu Sea species diversity and faunal abundances of benthic foraminifera decrease with increasing water depth. 2. Most epifaunal, oxyphilic species have a lower limit of occurrence at a water depth of approximately 2000 m (DOo1.25 ml/l) in the Sulu Sea. 3. Nonfossilizable, organic-walled species belonging to Allogromiida and Trochamminaceans constitute at most 3.7% of total living assemblages in the Sulu Sea.

4. We believe that low levels of C org flux and the combination of low DO content in bottom waters are the main factors controlling the deep-sea benthic fauna in the Sulu Sea. The foraminiferal faunas in the Sulu Sea reflect the contrast between continental slope, with higher food fluxes and higher oxygen concentrations, and lower bathyal to abyssal environmental conditions. The species in the upper bathyal zone respond to food fluxes as well as to oxygenation of bottom and pore waters. At constantly dysoxic (o1 ml/l O2) sites from the lower bathyal and abyssal zones, low oxygentolerant species prevailed in the assemblages. These species respond mainly to fluxes of organic carbon originating from surface primary production or brought by turbidity flows. 5. The general microhabitat preferences of common species are consistent with those from other studies, although due to the unique combination of poor food supply and dysoxic conditions a clear shift up the sediment column was observed for most infaunal species. Acknowledgements The authors heartily thank chief scientist Professor S. Nishida of R.V. Hakuho Maru cruise KH-024, the crew and shipboard scientific party for collecting multiple core samples. This research was supported by a Research Grant (P03561) from the Japan Society for the Promotion of Science Postdoctoral Fellows to R.T. Szarek. We are grateful to A.J. Gooday and two anonymous reviewers, whose valuable comments and suggestions have significantly improved this manuscript. Appendix For the species list of living benthic foraminifera from Sulu Sea, and the counting list of Rose Bengal stained benthic foraminifera see Tables A1 and A2, respectively.

Table A1 Species list of living benthic foraminifera from Sulu Sea, with references to representative illustrations Agglutinated species Adercotryma glomeratum (Brady, 1878) Ammobaculites agglutinans (d’Orbigny, 1846) Ammobaculites filiformis (Earland, 1934) Ammobaculites paradoxus (Clark, 1994) Ammodiscus catinus (Ho¨glund, 1947)

Jones, 1994, p. 41, pl. 34, Figs. 15–18 Jones, 1994, p. 39, pl. 32, Figs. 19, 20, 24–26 Jones, 1994, p. 39, pl. 32, Fig. 22 Hess, 1998, pl. 4 Ho¨glund, 1947, p. 122, pl. 8, Figs 1, 7; pl. 28, Figs 19–23

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Table A1 (continued ) Ammodiscus planorbis (Ho¨glund, 1947) Ammodiscus tenuis (Brady, 1881) Ammoglobigerina globulosa (Cushman, 1920) Ammomarginulina rostrata (Heron–Allen and Earland, 1929) Ammoscalaria tenuimargo (Brady, 1882) Argillotuba argillacea (Earland) Aschemonella scabra (Brady, 1879) Bigenerina nodosaria (d’Orbigny, 1826) Clavulina pacifica (Cushman, 1924) Cribrostomoides nitidus (Goe¨s, 1896) Cribrostomoides subglobosus (M. Sars, 1869) Crithionina pisum (Goe¨s, 1896) Cystammina pauciloculata (Brady, 1879) Dendronina arborescens (Heron–Allen and Earland, 1922) Deuterammina montagui (Bro¨nnimann and Whittaker, 1988) Discammina compressa (Goe¨s, 1882) Earlandammina drakensis (Bro¨nnimann and Whittaker, 1988) Earlandammina inconspicua (Earland, 1934) Eggerella bradyi (Cushman, 1911) Gaudryina flintii (Cushman, 1911) Glaphyrammina americana (Cushman, 1910) Globotrochamminopsis shannoni (Bro¨nnimann and Whittaker, 1988) Glomospira gordialis (Jones and Parker, 1860) Haplophragmoides bradyi (Robertson, 1891) Haplophragmoides sphaeriloculum (Cushman, 1910) Hippocrepinella alba (Heron–Allen and Earland, 1932) Hormosina pilulifera (Brady, 1884) Hormosina spiculifera (Hofker, 1972) Hormosinella distans (Brady, 1881) Hormosinella guttifera (Brady, 1881) Karreriella bradyi (Cushman, 1911) Karreriella pupiformis (Zheng, 1988 Karrerulina apicularis (Cushman, 1911) Lacroixina cf. cochleata (Lacroix, 1932) Lagenammina difflugiformis (Brady, 1879) Marsipella cylindrica (Brady, 1882) Marsipella dextrospiralis (Chapman and Parr, 1937) Marsipella elongata (Norman, 1878) Martinottiella communis (d’Orbigny, 1826) Nouria harrisii (Heron–Allen and Earland, 1914) Paratrochammina challengeri (Bro¨nnimann and Whittaker, 1988) Parvigenerina arenacea (Heron–Allen and Earland, 1922) Parvigenerina bigenerinoides (Lacroix, 1932) Portatrochammina wiesneri (Parr, 1950) Prolixoplecta exilis (Cushman, 1936) Psammosphaera fusca (Schulze, 1875) Pseudonodosinella cf. bacillaris (Brady, 1881) Recurvoides contortus (Earland, 1934 Reophax bilocularis (Flint, 1899) Reophax bradyi (Bro¨nnimann and Whittaker, 1980) Reophax dentaliniformis (Brady, 1881) Reophax hispidulus (Cushman, 1921,1920) Reophax longicollaris (Zheng, 1988) Reophax micaceus (Earland, 1934) Reophax scorpiurus (de Montfort, 1808) Reophax spiculifer (Brady, 1879)

Ho¨glund, 1947, p. 125, pl. 8, Figs 4, 9; pl. 28, Figs 13–16 Jones, 1994, p. 43, pl. 38, Figs 4–6 Loeblich and Tappan, 1994, p. 23, pl. 22, Figs. 1–6 Szarek, 2001, p.86, pl. 5, Fig. 5 Jones, 1994, p. 40, pl. 33, Figs 13–16 Loeblich and Tappan, 1987, p. 16, pl. 9, Fig 1 Jones, 1994, p. 35, pl. 27, Figs 1–2, 4–11 Loeblich and Tappan, 1994, p. 27, pl. 31, Figs 8–12; pl. 32, Figs 11–12 Loeblich and Tappan, 1994, p. 34, pl. 47, Figs 16–24 Zheng, 1988, p. 59, pl. 16, Figs 10–11; pl. 51, Fig. 6; text-Fig. 7 Jones, 1994, p. 40, pl. 34, Figs 8–10 Loeblich and Tappan, 1994, p. 13, pl. 3, Fig. 7 Jones, 1994, p. 45, pl. 41, Fig. 1 Loeblich and Tappan, 1987, p. 25, pl. 16, Figs 1–2 Bro¨nnimann and Whittaker, 1988, p. 112, Figs 41A–K, 42A–H Jones, 1994, p. 40, pl. 33, Figs 26–28 Bro¨nnimann and Whittaker, 1988, p. 131, Figs 47J–L Bro¨nnimann and Whittaker, 1988, p. 128, Figs 47A–I Loeblich and Tappan, 1994, p. 25, pl. 28, Figs 9–14 as Migros—Loeblich and Tappan, 1994, p. 32, pl. 19, Figs 10–13; pl. 44, Figs 11–13 Jones, 1994, p. 40, pl. 34, Figs 1–4 Bro¨nnimann and Whittaker, 1988, p. 38, Figs 15A–H Jones, 1994, p. 43, pl. 38, Figs 7–9 Szarek, 2001, p. 83, pl. 4, Fig. 3 Zheng, 1988, p. 57, pl. 16, Figs 1–2 Ho¨glund, 1947, p. 45, pl. 1, Figs 11–13; text–Fig. 17 Jones, 1994, p. 37, pl. 30, Figs 18–20 Zheng, 1988, p. 54, pl. 8, Figs 1–4 Jones, 1994, p. 38, pl. 31, Figs 18–22 Jones, 1994, p. 38, pl. 31, Figs 10–15 Loeblich and Tappan, 1994, p. 25, pl. 30, Figs 8–16 Zheng, 1988, p. 317, pl. 46, Figs 2–3; pl. 54, Fig. 7 Ujiie´, 1990, p. 14, pl. 1, Fig. 2 Loeblich and Tappan, 1987, p. 116, pl. 123, Figs 19–24 Jones, 1994, p. 36, pl. 30, Figs 1–3 Jones, 1994, p. 34, pl. 24, Figs 20–22 Zheng, 1988, p. 26, pl. 3, Fig. 4 Jones, 1994, p. 34, pl. 24, Figs 10–19 Jones, 1994, p. 52, pl. 48, Figs 1–8 Zheng, 1988, p. 100, pl. 15, Fig. 4 Bro¨nnimann and Whittaker, 1988, p. 48, Figs 16H–K Loeblich and Tappan, 1987, p. 116, pl. 123, Figs 13–16 as Textularia Ho¨glund, 1947, p. 181, pl.13, Fig. 6; text–Fig. 159 Bro¨nnimann and Whittaker, 1988, p. 68, Figs 25D–F; 26H–K; 27D–I Loeblich and Tappan, 1987, p. 131, pl. 139, Figs 1–3 Jones, 1994, p. 31, pl. 18, Figs 1–8 as Hormosina—Jones, 1994, p. 37, pl. 30, Figs 23–24 Loeblich and Tappan, 1994, p. 18, pl. 12, Figs 1–14 Zheng, 1988, p. 42, pl. 9, Figs 7–8 Bro¨nnimann and Whittaker, 1980, p. 264, Figs 13–16 Jones, 1994, p. 37, pl. 30, Figs 21–22 Zheng, 1988, p. 46, pl. 10, Figs 10–11; pl. 12, Fig. 9 Zheng, 1988, p. 47, pl. 8, Figs 11–12 Uchio, 1960, p. 50, pl. 1, Fig. 2 Hatta and Ujiie´, 1992a, p. 55, pl. 1, Figs 2–3; pl. 19, Fig. 1 Jones, 1994, p. 38, pl. 31, Figs 16–17

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Table A1 (continued ) Reophax subfusiformis (Earland, 1933) Reophax sp. 1 Saccammina anglica (Cushman, 1918) Saccammina sphaerica (G.O. Sars, 1872) Sorosphaera confusa (Brady, 1879) Spiroplectammina biformis (Parker and Jones, 1865) Subreophax aduncus (Brady, 1882) Textularia porrecta (Brady, 1884) Tritaxis challengeri (Hedley, Hurdle and Burdett, 1964) Trochammina hadai (Uchio, 1962) Trochammina subglobigeriniformis (Mikhalevich, 1972) Trochamminopsis parvus (Bro¨nnimann and Whittaker, 1988) Usbekistania charoides (Jones and Parker, 1860) Veleroninoides wiesneri (Parr, 1950)

Hayward et al., 1999, p. 82, pl. 1, Figs 15–16 Jones, 1994, p. 37, pl. 30, Fig. 14; Szarek, 2001, p. 80 Zheng, 1988, p. 33, pl. 4, Fig. 14 Jones, 1994, p. 31, pl. 18, Figs 11–15, ? 17 Loeblich and Tappan, 1987, p. 28, pl. 19, Fig 1 Ho¨glund, 1947, p. 163, pl.12, Fig. 1; text Figs 140–141 Jones, 1994, p. 38, pl. 31, Figs 23–26 Jones, 1994, p. 48, pl. 43, Fig. 4 Jones, 1994, p. 46, pl. 41, Fig. 3 Loeblich and Tappan, 1994, p. 24, pl. 26, Figs 1–29 Bro¨nnimann and Whittaker, 1988, p. 30, Figs 11 H–N Bro¨nnimann and Whittaker, 1988, p. 91, Figs 33E–K Jones, 1994, p. 43, pl. 38, Figs 10–16 Jones, 1994, p. 45, pl. 40, Figs 14–15

Organic-walled foraminifera Lepidodeuterammina ochracea (Williamson, 1858) Nodellum membranaceum (Brady, 1879) Remaneica helgolandica (Rhumbler, 1938) Resigella moniliformis (Resig, 1982) Rotaliammina chitinosa (Collins, 1958) Septotrochammina gonzalezi (Seiglie, 1964)

Bro¨nnimann and Whittaker, 1988, p. 119, Figs 52A–F Jones, 1994, p. 38, pl. 32, Figs 1–4 Loeblich and Tappan, 1987, p. 129, pl. 137, Figs 9–11 Loeblich and Tappan, 1987, p. 17, pl. 9, Figs 11–12 Loeblich and Tappan, 1994, p. 24, pl. 27, Figs 4–9 Loeblich and Tappan, 1994, p. 25, pl. 28, Figs 1–5

Agglutinated tubular foraminifera Bathysiphon macilentus (Zheng, 1988) Hyperammina cylindrica (Parr, 1950) Hyperammina elongata (Brady, 1878) Hyperammina laevigata (Wright, 1891) Rhabdammina abyssorum (M. Sars, 1869) Rhizammina algaeformis (Brady, 1879) Saccorhiza ramosa (Brady, 1879) Tolypammina vagans (Brady, 1879)

Zheng, 1988, p. 306, pl. 2, Fig. 11 Jones, 1994, p. 33, pl. 23, Figs 4, 7 Jones, 1994, p. 33, pl. 23, Fig. 8 Jones, 1994, p. 33, pl. 23, Figs 9–10 Jones, 1994, p. 32, pl. 21, Figs 1–8, 10–13 Jones, 1994, p. 36, pl. 28, Figs 1–11 Jones, 1994, p. 33, pl. 23, Figs 15–19 Jones, 1994, p. 33, pl. 24, Figs 1–5

Calcareous species Alliatinella differens (McCulloch, 1977) Ammonia beccarii (Linne´, 1758) Amphicoryna hirsuta (d’Orbigny, 1826) Amphicoryna separans (Brady, 1884) Anomalinoides colligerus (Chapman and Parr, 1937) Anomalinoides globulosus (Chapman and Parr, 1937) Aphelophragmina brittanica (Macfadyen, 1942) Astrononion novozealandicum (Cushman and Edwards, 1937) Bolivina pacifica (Cushman and McCulloch, 1942) Bolivina robusta (Brady, 1881) Bolivina spathulata (Williamson, 1858) Bolivina variabilis (Williamson, 1858) Bulimina marginata (d’Orbigny, 1826 Bulimina rostrata (Brady, 1884) Bulimina striata (d’Orbigny, 1826) Cancris oblongus (d’Orbigny, 1839) Cassidelina complanata (Egger, 1893) Cassidulina carinata (Silvestri, 1896) Chilostomella oolina (Schwager, 1878) Chilostomella ovoidea (Reuss, 1850) Cibicides lobatulus (Walker and Jacob, 1798) Cibicides refulgens (de Montfort, 1808) Cibicidoides cicatricosus (Schwager, 1866) Cibicidoides pachyderma (Rzehak, 1886)

Loeblich and Tappan, 1994, p. 99, pl. 175, Figs 1–12; pl. 176, Figs 1–3 Hatta and Ujiie´, 1992b, p. 199, pl. 44, Figs 1–2 Jones, 1994, p. 75, pl. 63, Figs 12–15 Jones, 1994, p. 76, pl. 64, Figs 16–19 Loeblich and Tappan, 1994, p. 162, pl. 355, Figs 1–3 Loeblich and Tappan, 1994, p. 162, pl. 354, Figs 11–13; pl. 355, Figs 4–13 Loeblich and Tappan, 1994, p. 110, pl. 214, Figs 13–24 Hayward et. al., 1999, p. 157, pl. 15, Figs 8–9 Akimoto et al., 2002, p. 14, pl. 37, Fig. 3 Jones, 1994, p. 58, pl. 53, Figs 7–9 as Brizalina—Jones, 1994, p. 57, pl. 52, Figs 20–21 Loeblich and Tappan, 1994, p. 111, pl. 216, Figs 7–15 Loeblich and Tappan, 1994, p. 124, pl. 242, Figs 1–4 Jones, 1994, p. 56, pl. 51, Figs 14–15 Loeblich and Tappan, 1994, p. 125, pl. 242, Figs 8–14 Loeblich and Tappan, 1994, p. 134, pl. 265, Figs 11–13 Loeblich and Tappan, 1994, p. 117, pl. 230, Figs 1–10 Loeblich and Tappan, 1994, p. 114, pl. 220, Figs 7–12 Jones, 1994, p. 61, pl. 55, Figs 12–14, 17–18 Jones, 1994, p. 61, pl. 55, Figs 15–16, 19–23 Jones, 1994, p. 97, pl. 92, Fig. 10; pl. 93, Figs 1, 4–5; pl. 115, Figs 4–5 Loeblich and Tappan, 1994, p. 149, pl. 318, Figs 7–9 Jones, 1994, p. 98, pl. 94, Fig. 8 Jones, 1994, p. 98, pl. 94, Fig. 9

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Table A1 (continued ) Cibicidoides robertsonianus (Brady, 1881) Discorbinella araucana (d’Orbigny, 1839) Discorbinella bertheloti (d’Orbigny, 1839) Epistominella exigua (Brady, 1884) Eponides pusillus (Parr, 1950) Fissurina bradyiformata (McCulloch, 1977) Fontbotia wuellerstorfi (Schwager, 1866) Gavelinopsis lobatulus (Parr, 1950) Gavelinopsis translucens (Phleger and Parker, 1951) Globobulimina pacifica (Cushman, 1927) Globocassidulina bisecta (Nomura, 1983) Globocassidulina subglobosa (Brady, 1881) Gyroidina broeckhiana (Karrer, 1878) Gyroidina lamarckiana (d’Orbigny, 1839) Gyroidina neosoldanii (Brotzen, 1936) Gyroidina orbicularis (Parker, Jones and Brady, 1865) Gyroidinoides nipponicus (Ishizaki, 1944) Hoeglundina elegans (d’Orbigny, 1826) Laevidentalina filiformis (d’Orbigny, 1826) Laevidentalina inflexa (Reuss, 1866) Laevidentalina sidebottomi (Cushman, 1933) Lagena gibbera (Buchner, 1940) Lenticulina calcar (Linne´, 1758) Lenticulina submamilligera (Cushman, 1917) Lenticulina suborbicularis (Parr, 1950) Lernella inflata (LeRoy, 1944) Melonis affinis (Reuss, 1851) Neouvigerina ampullacea (Brady, 1884) Nonionoides grateloupi (d’Orbigny, 1826) Nuttallides bradyi (Earland, 1934) Oridorsalis umbonatus (Reuss, 1851) Osangularia culter (Parker and Jones, 1865) Paracassidulina minuta (Cushman, 1933) Parrelloides bradyi (Trauth, 1918) Pullenia bulloides (d’Orbigny, 1826) Pullenia quinqueloba (Reuss, 1851) Pullenia salisburyi (R.E. and K.C. Stewart, 1930) Pyrgo murrhina (Schwager, 1866) Rotaliatinopsis semiinvoluta (Germeraad, 1946) Rotaliella new sp. Seabrookia pellucida (Brady, 1890) Siphonina bradyana (Cushman, 1927) Siphonina tubulosa (Cushman, 1924) Trifarina angulosa (Williamson, 1858) Trifarina bradyi (Cushman, 1923) Triloculina tricarinata (d’Orbigny, 1826) Uvigerina auberiana (d’Orbigny, 1839) Valvulineria mexicana (Parker, 1954) Valvulineria minuta (Schubert, 1904)

Jones, 1994, p. 99, pl. 95, Fig. 4 Jones, 1994, p. 93, pl. 86, Figs 10–11 Hayward et al., 1999, p. 152, pl. 14, Figs 1–3 as Pseudoparrella Loeblich and Tappan, 1994, p. 146, pl. 307, Figs 1–7 Loeblich and Tappan, 1994, p. 135, pl. 270, Figs 1–10 Jones, 1994, p. 68, pl. 59, Fig. 26 Loeblich and Tappan, 1994, p. 150, pl. 319, Figs 7–12 as G. lobatula—Jones, 1994, p. 94, pl. 88, Fig. 1 Hess, 1998, p. 81, pl. 15, Figs 1–2 Loeblich and Tappan, 1994, p. 125, pl. 243, Figs 13–16 Loeblich and Tappan, 1994, p. 115, pl. 222, Figs 7–13 Jones, 1994, p. 60, pl. 54, Fig. 17 Jones, 1994, p. 106, pl. 107, Fig. 4 Loeblich and Tappan, 1994, p. 163, pl. 361, Figs 7–12 Loeblich and Tappan, 1994, p. 163, pl. 361, Figs 13–15; pl. 362, Figs 1–7 Jones, 1994, p. 114, pl. 115, Fig. 6 Ujiie´, 1990, p. 47, pl. 27, Fig. 1 Jones, 1994, p. 104, pl. 105, Figs 3–6 Hayward et al., 1999, p. 109, pl. 6, Figs 18–19 Loeblich and Tappan, 1994, p. 65, pl. 114, Figs 10–16, pl. 115, Fig. 6 Loeblich and Tappan, 1994, p. 65, pl. 113, Figs 13–19 Jones, 1994, p. 63, pl. 57, Figs 8–9, ?10 Jones, 1994, p. 81, pl. 70, Figs 9–12 Jones, 1994, p. 82, pl. 70, Figs 17–18 Loeblich and Tappan, 1994, p. 68, pl. 123, Figs 1–9 Loeblich and Tappan, 1994, p. 116, pl. 226, Figs 1–12 Jones, 1994, p. 107, pl. 109, Figs 8–9 Loeblich and Tappan, 1994, p. 126, pl. 246, Figs 9–19 Loeblich and Tappan, 1994, p. 158, pl. 342, Figs 1–5 Loeblich and Tappan, 1987, p. 603, pl. 669, Figs 17–23 Hayward et al., 1999, p. 160, pl. 15, Figs 24–26 Hess, 1998, p. 86, pl. 14, Figs 11–12 Loeblich and Tappan, 1994, p. 116, pl. 223, Figs 7–8 Loeblich and Tappan, 1994, p. 144, pl. 301, Figs 1–9 Jones, 1994, p. 92, pl. 84, Figs 12–13 Jones, 1994, p. 92, pl. 84, Figs 14–15 Ujiie´, 1990, p. 44, pl. 24, Figs 8–9 Loeblich and Tappan, 1994, p. 51, pl. 86, Figs 1–4 Loeblich and Tappan, 1994, p. 163, pl. 361, Figs 1–3 Loeblich and Tappan, 1987, p. 564 Loeblich and Tappan, 1994, p. 97, pl. 170, Figs 1–9 Loeblich and Tappan, 1994, p. 143, pl. 298, Figs 1–9 Loeblich and Tappan, 1994, p. 144, pl. 299, Figs 1–10 Loeblich and Tappan, 1994, p. 128, pl. 250, Figs 13–20 Loeblich and Tappan, 1994, p. 128, pl. 251, Figs 6–16 Loeblich and Tappan, 1994, p. 56, pl. 96, Figs 1–7 Jones, 1994, p. 86, pl. 75, Figs 6–9 Rathburn and Corliss, 1994 Loeblich and Tappan, 1994, p. 135, pl. 268, Figs 1–3

Table A2 Counting list of Rose Bengal stained benthic foraminifera in the 432 mm size fractions for 7 cores and all sediment intervals down to 5 cm.Numbers are not standardised for sediment volume

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